SAJCH Vol 11, No 4 (2017)

CHILD HEALTH SOUTH AFRICAN JOURNAL OF

December 2017

Volume 11

Number 4

• Association between HIV and viral LRTI in PICU patients • Implementation of Road-to-Health booklet promotion messages at PHC facilities • Placental malaria and neonatal anti-tetanus antibody status • Predictors of obesity and cardiometabolic disease risk in SA children • Diandric triploidy in a live-born infant

CHILD HEALTH SOUTH AFRICAN JOURNAL OF

DECEMBER 2017

Volume 11

EDITOR J M Pettifor FOUNDING EDITOR N P Khumalo EDITORIAL BOARD Prof. M Adhikari (University of KwaZuluNatal, Durban) Prof. M Kruger (Stellenbosch University) Prof. H Rode (Red Cross War Memorial Children's Hospital, Cape Town) Prof. L Spitz (Emeritus Nuffield Professor of Paediatric Surgery, London) Prof. A Venter (University of the Free State, Bloemfontein) Dr T Westwood (Red Cross War Memorial Children's Hospital, Cape Town) Prof. D F Wittenberg (University of Pretoria)

Number 4

CONTENTS Editorial

153 Thoughts as we consider the legalisation of cannabis in South Africa

A Rothberg

HEALTH & MEDICAL PUBLISHING GROUP:

Research

CEO AND PUBLISHER Hannah Kikaya

154 Association between HIV and proven viral lower respiratory tract infection in paediatric intensive care unit patients at Inkosi Albert Luthuli Central Hospital, Durban, South Africa

N P Majozi, N Nkwanyana, S Thula, A Coutsoudis

159 Infant hearing screening in a developing country context: Status in two South

African provinces

EXECUTIVE EDITOR Bridget Farham

K Khoza-Shangase, A Kanji, L Petrocchi-Bartal, K Farr

MANAGING EDITORS Claudia Naidu Naadia van der Bergh TECHNICAL EDITORS Naadia van der Bergh Kirsten Morreira

164 Implementation of the Road-to-Health-Booklet health promotion messages at primary healthcare facilities, Western Cape Province, South Africa

PRODUCTION MANAGER Emma Jane Couzens

L M du Plessis, H E Koornhof, M L Marais, R Blaauw

DTP AND DESIGN Travis Arendse Clinton Griffin

170 Evaluation of culture-proven neonatal sepsis at a tertiary care hospital in South Africa M M Lebea, V Davies

174 Assessing the utilisation of a child health monitoring tool

R Blaauw, L Daniels, L M du Plessis, N Koen, H E Koornhof, M L Marais, E van Niekerk, J Visser

180 Placental malaria and neonatal anti-tetanus antibody status: Any association?

M F Bashir, H A Elechi, M G Ashir, A I Rabasa, A B Musa, R T Akuhwa, A G Farouk

186 Predictors of obesity and cardiometabolic disease risk in South African children

V K Moselakgomo, M van Staden

192 Community feedback on the JustMilk Nipple Shield Delivery System in the Vhembe District of Limpopo, South Africa

A Flynn, R Scheuerle, G Galgon, S Gerrard, V Netshandama

Case Report

198 Diandric triploidy in a liveborn infant with 3-4 syndactyly and a neural tube defect

C E Spencer, B Mofokeng, A Turner, F Nakwa, A Krause

201

CPD

CHIEF OPERATING OFFICER Diane Smith | Tel. 012 481 2069 Email: dianes@hmpg.co.za ONLINE SUPPORT Gertrude Fani | Tel. 021 532 1281 Email: publishing@hmpg.co.za FINANCE Tshepiso Mokoena HMPG BOARD OF DIRECTORS Prof. M Lukhele (Chair), Dr M R Abbas, Dr Mrs H Kikaya, Dr M Mbokota, Dr G Wolvaardt HEAD OFFICE Block F, Castle Walk Corporate Park, Nossob Street, Erasmuskloof Ext. 3, Pretoria, 0181 EDITORIAL OFFICE Suite 11, Lonsdale Building, Lonsdale Way, Pinelands, 7405 Tel. 021 532 1281 Email: publishing@hmpg.co.za ISSN 1999-7671

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ublished by the Health and Medical Publishing Group, P Suite 11, Lonsdale Building, Lonsdale Way Pinelands 7405

Cover: Litha, Red Cross War Memorial Children's Hospital Primary School

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EDITORIAL

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Thoughts as we consider the legalisation of cannabis in South Africa In the USA, President Trump is currently targeting the devastation caused by opioid addiction. Several statistics are being used to support this initiative, one of which is the apparently above-board sale of 9 million opioid pills over 2 years to a single pharmacy in a West Virginia town with a population of less than 400.[1] Consequently, doctors and pharmaceutical manufacturers are both regarded as being complicit in promoting opioid abuse and addiction. Along similar lines in South Africa (SA), one has to worry when a leading newspaper quotes the managing director of an SA phytopharmaceutical company with the statement that “Medicinal cannabis can be thought of as the gold rush of our time’.[2] In monetary terms, the current global market for cannabis/marijuana products is estimated to be USD3bn, with the potential to rise to USD56bn. The abovementioned company anticipates a significant share of that market. The foundations have already been laid through the acquisition of a licence to produce medical/medicinal marijuana (MM) in Lesotho, and then to deliver to countries in which MM and recreational marijuana have been legalised. Circumstances appear to be right for plans such as this, which not only leverage off the political correctness of commercialising phytopharmacy and legitimately exploiting the sub-continent’s natural flora, but also reflect what is happening in SA in terms of legislative processes around both MM and recreational marijuana use. In March 2017, the Medicines Control Council (MCC), which is soon to be replaced by the South African Health Products Regulatory Authority Board, issued guidelines for comment.[3] The 32-page document covers processes to regulate the growing, extraction and testing of cannabis, as well as the manufacture of medicines containing cannabis. The MCC and the Department of Health would grant permission to qualifying applicants, who would also have to meet stringent requirements in terms of product security and production. These guidelines were in anticipation of the government making progress in legalising MM. In this context, on 28 July 2017 the Government Gazette indicated that cannabidiol oil had been rescheduled as a schedule 6 drug for therapeutic purposes.

[4] This introduces an element of control as the product was previously available through various outlets but often of questionable quality and purity. Apparently, a few days later the Schedule 6 status was ‘downgraded’ to schedule 4 by the MCC. Other cannabinoids may follow. Marijuana is chemically complex: it is comprised of >480 compounds, including 70 distinct cannabinoids.[5] The two main types of cannabinoids are tetrahydrocannabinol (THC), which is primarily responsible for the drug’s psychoactive properties, and cannabidiol (CBD). Purified CBD, or hemp CBD oil, is commercially available, with emerging evidence of its medicinal properties. It usually contains minimal THC. Cannabinoid receptors are widely distributed in the body: CB-1 receptors are found primarily in the central and peripheral nervous system and CB-2 receptors are primarily located in the immune system (e.g. B lymphocytes and natural killer cells). CBD is purported to have components with multiple actions ranging from reduction of inflammation, inhibition of cancer cell growth and enhanced bone growth, to pain reduction, enhanced sleep, appetite stimulation and reduction in nausea and vomiting. Overall, it seems that efforts to legitimise and legalise cannabis are enjoying some success, certainly in the realm of MM. As such, it is appropriate that medical professionals consider if and when

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to prescribe the drug for their patients. In the US, while cannabis is still illegal at the federal level, some 29 states andWashington DC have legalised MM, and 9 have legalised recreational marijuana for adults.

MM does not specifically refer to particular derivatives of marijuana but rather to ‘the use of the drug for medical purposes.’ In fact, MM is simply defined as ‘cannabis and cannabinoids that are recommended by doctors for their patients’, so one may well be concerned that the opioid abuse experienced in West Virginia and other towns in the US may also reflect in future prescriptions of marijuana/cannabis for ‘medicinal purposes’. In the US, all the aforementioned states allow the use of MM for children with cancer or a terminal condition.

Apart from CBD, which is commercially available, the US FDA has approved a number of synthetic THC products for the treatment of chemotherapy-induced nausea and vomiting. In terms of research attesting to the value of cannabinoids in paediatrics, the subject has recently been reviewed by clinicians from New York and Boston.[5] It would appear that the opposition of the American Academy of Pediatrics (AAP) to the legalisation and the use of MM in paediatrics is not without foundation, as the evidence for its effectiveness in treating cancer, nausea and vomiting, anorexia and pain in children is thin.[6] However, the AAP acknowledges that MM might have a place in terminally ill children when conventional treatment is inadequate, but simultaneously calls for more research. There may be a place for the management of refractory seizures in children,[7] although the rate of adverse events appears to be fairly high, ranging from somnolence and diarrhoea to status epilepticus. Regarding legalisation and the recreational use of cannabis, the AAP is concerned about the emerging perceptions that cannabis is harmless, while evidence exists that its use during the early years may have long-term psychiatric and behavioural effects.

Alan Rothberg

Associate Professor School of Therapeutic Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa Alan.Rothberg@wits.ac.za S Afr J Child Health 2017;11(4):153. DOI:10.7196/SAJCH.2017.v11i4.1472

1. McElhinny B. Town of Kermit, population 400, sues five pharmaceutical giants. http://wvmetronews.com/2017/01/31/town-of-kermit-population-400-suesfive-pharmaceutical-giants/ (accessed 30 October 2017).

2. Hall J. Medical marijuana a huge opportunity for Africa. https://www.iol.co.za/ news/opinion/medical-marijuana-a-huge-opportunity-for-africa-11550668 (accessed 11 October 2017).

3. Medicines Control Council (MCC). Cultivation of cannabis and manufacture of cannabis-related pharmaceutical products for medicinal and research purposes.

Pretoria: MCC, 2017. https://daggacouple.co.za/wp-content/uploads/2017/03/ MCC-Cannabis-Cultivation-Guidelines-Mar17-.pdf (accessed 27 October 2017).

4. National Department of Health, South Africa. Medicines and Related Substances Act of 1965 (Act No. 101 Of 1965). Government Gazette No. 41009:708. 2017.

5. Ananth P, Reed-Watson A, Wolfe J. Medical marijuana in pediatric oncology: A review of the evidence and implications for practice. Pediatr Blood Cancer 2017:e26826. https://doi.org/10.1002/pbc.26826 6. Committee on Substance Abuse, Committee on Adolescence. The impact of marijuana policies on youth: Clinical, research, and legal update. Pediatrics 2015;135(3):584-587. https://doi.org/10.1542/peds.2014-4146 7. Devinsky O, Cross JH, Laux L, et al. Trial of cannabidiol for drug-resistant seizures in the Dravet syndrome. N Engl J Med 2017;376:2011-2020. https:// doi.org/10.1056/NEJMoa1611618

DECEMBER 2017 Vol. 11 No. 4

RESEARCH

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Association between HIV and proven viral lower respiratory tract infection in paediatric intensive care unit patients at Inkosi Albert Luthuli Central Hospital, Durban, South Africa N P Majozi,1 MB ChB, FC Paeds; N Nkwanyana,2 MSc (Statistics); S Thula,1 MB ChB, FC Paeds; A Coutsoudis,1 PhD 1 2

Department of Paediatrics and Child Health, Faculty of Health Sciences, University of KwaZulu-Natal, Durban, South Africa Department of Public Health Medicine, Faculty of Health Sciences, University of KwaZulu-Natal, Durban, South Africa

Corresponding author: N P Majozi (sitholenp@gmail.com) Background. Acute viral respiratory infections are common within the paediatric population. Nucleic acid amplification tests can identify a wide range of respiratory viruses. Virally infected patients can now be diagnosed early and more accurately in the acute phase of illness.

Objectives. To examine the association between HIV status and mortality in children with viral lower respiratory tract infection (LRTI) and to delineate the profile of identified viruses.

Methods. We conducted a retrospective review of charts of children aged from birth to 10 years of age who were admitted to the paediatric intensive care unit at Inkosi Albert Luthuli Central Hospital with a viral LRTI between December 2010 and May 2015. Only patients who had a positive respiratory viral multiplex test were eligible for entry into the study. Patients were grouped according to their HIV status and mortality was assessed.

Results. A total of 338 records were analysed in this study. Sixty-five patients tested HIV-positive (19.2%) and 80.8% were HIV-negative (n=273).

There were 55 mortalities: 12 were among the 65 HIV-positive patients (18.5%) and 43 among the 273 HIV-negative patients (15.8%). The difference in mortality according to HIV status was not statistically significant (p=0.595). Respiratory syncytial virus was the most prevalent virus identified overall, with adenovirus being most prevalent in the HIV-positive group.

Conclusion. The results showed that patients with viral LRTIs who required respiratory support had a similar mortality regardless of HIV status.

S Afr J Child Health 2017;11(4):154-158. DOI:10.7196/SAJCH.2017.v11i4.1236

Acute viral respiratory infections are common within the paediatric population, irrespective of HIV status, and are a common cause of admission to hospital in developed countries as well as a major cause of death in developing countries[1] These viral infections are responsible for a large number of lower respiratory tract infections (LRTIs), including bronchiolitis, croup, acute exacerbations of asthma or wheezing and pneumonia.[2] It is estimated that viral respiratory infections contribute between 40 and 80% of respiratory morbidity.[3] Virally infected patients may present with fever, myalgia, fatigue, cough, rhinitis and pharyngitis. Generally, the viruses causing respiratory illness have a short incubation period and are spread from person to person by direct contact with contaminated secretions or aerosolised droplets.

Viruses that have been identified as causing respiratory illness include respiratory syncytial virus (RSV), influenza A and B, adenovirus, rhinoviruses and parainfluenza viruses 1, 2 and 3.[2] In the 2000s, more viruses were discovered to cause respiratory infection.[1] These new viruses include human metapneumovirus, severe acute respiratory syndrome corona virus, parainfluenza 4, avian influenza viruses and enterovirus.[1] Rare causes include Epstein-Barr virus, cytomegalovirus, varicella-zoster virus, herpes simplex virus and measles. These pathogens generally have overlapping signs and symptoms, which makes it very difficult for attending physicians to make a distinction of the causative viral pathogen based on signs and symptoms alone without laboratory assistance.[1] It is also rather difficult to distinguish infection secondary to viral infection versus bacterial infection based on clinical presentation alone – this leads to a large number of patients being treated inappropriately with antibiotics for viral infections. Management is mainly symptomatic

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and supportive care and there are only a few antiviral agents available for use against specific viruses.

There are various ways of identifying viral respiratory infections, including identification of the virus by an immunofluorescence assay (IFA), serology tests which use the patient’s serum to detect virus-specific antibodies, and viral antigens using an enzyme-linked immunosorbent assay (ELISA).[5] These tests are of little use in the acute phase of the illness as a four-fold increase in viral titre is required to detect infection.[6] A second test involves the isolation of virus by cell culture from patient samples and identification of the virus by immunofluorescence assays (IFA).[5] However, cultures require a long incubation time and special incubation media, which makes them costly.[6] Previously, viral isolation and serology were the mainstay of laboratory diagnosis of respiratory viral infections.[1] However, nucleic acid amplification tests emerged in the 1980s and have now been developed for a wide range of illnesses, including those caused by respiratory viruses. These tests can detect very low levels of viral nucleic acids and have increased laboratory sensitivity for diagnosing viruses.[3] Respiratory samples used for diagnosis include endotracheal aspirates, broncho-alveolar lavage, nasopharyngeal swabs and aspirates, throat swabs, as well as sputum and tissue samples from lung biopsy. Infected patients can now be diagnosed early and more accurately in the acute phase of illness when they may still be shedding low levels of the virus.

This earlier and more accurate diagnosis is helpful in a number of ways. It allows the patient to receive more appropriate therapy earlier, where indicated, it allows for infection control measures to be instituted and it allows public health officials to be aware of what pathogens are circulating in the community and hospitals. The multiplex polymerase

DECEMBER 2017 Vol. 11 No. 4

RESEARCH chain reaction (PCR) tests are of even greater benefit as they test for a wide range of viruses simultaneously.

KwaZulu-Natal Province (KZN) has the highest prevalence of HIV infection in South Africa (SA), with a prevalence of 41.3% in 2013. The national HIV prevalence rate among antenatal women was estimated at 29.7% in 2013.[7] In January 2015, the SA government introduced the Option B+ approach to reduce mother-to-child transmission of HIV during pregnancy, delivery and the postnatal period.[8] Despite these improved interventions and low recently reported figures of transmission rates in KZN (1.3%),[9] the paediatric intensive care unit (PICU) at Inkosi Albert Luthuli Central Hospital (IALCH) still receives a sizeable number of HIV-infected patients.

The PICU at IALCH has in the past few years instituted respiratory viral multiplex PCR testing for children admitted with a respiratory disease in order to diagnose viral respiratory infection.

The aim of this study was to examine the association between HIV infection and viral LRTI in paediatric patients requiring intensive care. The primary outcome examined was mortality, as an association between HIV status and outcome of respiratory viral infection may assist physicians in the medical management of patients. A secondary aim of the study was to delineate the frequency of viruses associated with respiratory illness in our setting.

Methods

The study was approved by the University of KwaZulu-Natal Biomedical Research Ethics Committee (ref. no. BREC REF:515/14) and was conducted at the IALCH (Durban, KZN, SA), which is a tertiary referral hospital with a 14-bed PICU. The study involved a retrospective review of records of children aged from birth to 10 years who had been admitted to the PICU at IALCH with a viral LRTI between December 2010 and May 2015.

Demographics of study participants

The majority of the patients were males (58.9%; n=199/338). The participants’ age at presentation was classified into age range intervals ranging from 0 days to 10 years. The majority of the 338 patients (Fig. 1) in the study were within the age range ‘birth to 3 months of age’ and 13% (n=44) of all the study participants were born premature (<37 weeks’ gestation). In total, 292 of the study participants had their birth weight documented, which ranged from 900 g to 4 900 g, with a median birth weight of 2 800 g: 10.6% (n=31/292) weighed <1 500 g and were classified as very low-birth-weight infants, and 34.9% (n=102/292) were low-birth-weight infants, with a birth weight of <2 500g. The World Health Organization (WHO) weight-for-age Z-scores were assigned to 303 patients who had their weights documented on admission. Of the 303 patients, 65.3% (n=198) had normal weight-for-age; 15.2% (n=46) were underweight for their age; 14.9% (n=45) were severely underweight for their age; and 4.6% (n=14) were overweight for age.

Charts received (N=406)

Included (n=338)

No LRTI (n=17)

Excluded (n=68)

HIV status unknown (n=14)

Charts not found on system (n=15)

Charts with incomplete data (n=22)

Fig. 1. Diagram illustrating charts included and excluded in the study.

(LRTI = lower respiratory tract infection.)

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Clinical characteristics of the study participants

In total, 19.2% (n=65/338) of the patients tested HIV-positive and 80.8% (n=273/338) tested HIV-negative. Of the HIV-negative patients, 131, 117, and 25 were born to HIV-infected mothers, HIV-uninfected mothers and mothers with unknown HIV status, respectively. Details of the age categories of the different HIV status groups are shown in Table 1.

We examined those who had been exposed to maternal HIV (58.0%; n=196) to determine how many had participated in the prevention of mother-to-child transmission (PMTCT) programme. As there was no register to confirm who was part of the PMTCT programme, we accepted any documentation in the chart that the patient had received PMTCT and also included those paediatric patients who received either nevirapine (NVP), zidovudine (AZT) or NVP and AZT in the first 6 weeks of life as having been part of the programme. Of the HIV-positive patients, 47.7% (n=31/65) had not received PMTCT according to their records, 18.5% (n=12/65) received PMTCT and 33.8% (n=22/65) had no documentation of PMTCT. Of the HIV-negative patients, 48.0% (n=131/273) were HIV-exposed and 69.0% (n=89/131) of them had received PMTCT; however, it was not possible to distinguish patients that followed the entire PMTCT programme from those that only partially participated.

The majority of the HIV-positive patients were diagnosed for the first time in the PICU. This meant that they were not on highly active antiretroviral therapy (HAART) when they acquired the viral LRTI. Only 10.8% (n=7/65) were on HAART at the time of admission to the PICU. CD4% values were documented for 53 (n=53/65) patients and absolute CD4 counts for 51 (n=51/65) patients. Only 43 (n=43/65) patients had previously had a viral load test done.

Mortality and clinical outcomes

Overall, 16.3% (n=55) of the patients died and 83.7% (n=283) were discharged. There was no significant difference in the mortality rate based on gender, with the females having a slightly higher mortality rate compared with the males (18.0% v. 15.1%, respectively; p=0.476).

Although the mortality rate was highest (29.0%) among the very lowbirth-weight infants (<1 500 g), the association between mortality and birth weight was not significant (p=0.174).

The poorest outcome was found in the ‘severely underweightfor-age’ group, with a mortality rate of 26.7%, followed by the ‘underweight-for-age’ group, with a mortality rate of 19.6%. This association between mortality and weight-for-age was not significant (p=0.12).

There were 55 mortalities: 18.5% (n=12/65) of the HIV-infected patients and 15.8% (n=43/273) of the HIV-uninfected patients had died. The difference in mortality according to HIV status was not statistically significant (p=0.595). A breakdown of the 55 deaths based on age and HIV status is shown in Table 2. Of the 55 deaths, 21.8% (n=12/55) were in HIV-infected children (HIV+); 41.8% (n=23/55) were in HIV-exposed but uninfected children (HEU); 32.7% (n=18/55) were in HIV-unexposed infants (HUU); and 3.6% (n=2/55) were in the HEUU group.

Feeding options were examined in patients who were <1 year of age (n=298). Of these 298 patients, feeding options were only documented for 55.4% (n=165/298). Of these 165 patients, 50.9% (n=84/165) were exclusively breastfed, 41.2% (n=68/165) were exclusively formulafed and 7.9% (n=13/165) were mixed-fed. Feeding practice was only documented in 40.0% (n=22/55) of the deceased patients. The mortality rate was highest in the mixed-fed group (30.7%; p=0.192).

Most patients spent between 8 and 14 days in the PICU. The length of stay in the PICU was not affected by birth weight, feeding practice, nutritional status or HIV status.

Profile of viral infections

In total, 11 different viruses were identified by the respiratory viral multiplex PCR test. Ten patients had more than one virus identified.

DECEMBER 2017 Vol. 11 No. 4

RESEARCH Table 1. Association of age with HIV status (N=338) HIV status, n (%) Age range

N

HUU

HEU

HEUU

HIV+

0 - 3 months

215

67 (31.2)

94 (43.7)

13 (6.0)

41 (19.1)

4 - 6 months

52

19 (36.5)

18 (34.6)

2 (3.8)

13 (25.0)

7 - 9 months

17

4 (23.5)

5 (29.4)

4 (23.5)

4 (23.5)

10 - 12 months

14

7 (50.0)

5 (35.7)

0

2 (14.3)

1 - 2 years

19

12 (63.1)

6 (31.6)

0

1 (5.3)

2 - 3 years

10

4 (40.0)

3 (30.0)

2 (20.0)

1 (10.0)

3 - 5 years

5

3 (60.0)

0

2 (40.0)

0

>5 years

6

1 (16.7)

0

2 (33.3)

3 (50.0)

Total

338

117 (34.6)

131 (38.8)

25 (7.4)

65 (19.2)

HUU = HIV-unexposed and uninfected; HEU = HIV-exposed and uninfected; HIV+ = HIV-infected; HEUU = HIV exposure unknown and uninfected.

Table 2. Association of age with HIV status and mortality HIV status, n (%) Age range

Mortality, N

HUU

HEU

HEUU

HIV+

0 - 3 months

30

8 (26.7)

17 (56.7)

0

4 (13.3)

4 - 6 months

12

3 (25.0)

3 (25.0)

0

6 (50.0)

7 - 9 months

2

1 (50.0)

1 (50.0)

0

0

10 - 12 months

4

2 (50.0)

1 (25.0)

0

1 (25.0)

1 - 2 years

4

3 (75.0)

1 (25.0)

0

0

2 - 3 years

0

0

0

0

0

3 - 5 years

1

1 (100)

0

0

0

>5 years

3

0

0

2 (66.7)

1 (33.3)

Total

55

18 (32.7)

23 (41.8)

2 (3.6)

12 (21.8)

HUU = HIV-unexposed and uninfected; HEU = HIV-exposed and uninfected; HIV+ = HIV-infected; HEUU = HIV exposure unknown and uninfected.

Table 3. Microbes identified in relation to HIV status HIV status, n (%) Microorganism

N

HUU

HEU

HEUU

HIV+

RSV

156

58 (37.2)

72 (46.2)

12 (7.7)

14 (9.0)

Adenovirus

93

36 (38.7)

29 (31.2)

6 (6.5)

22 (23.7)

Parainfluenza 1

7

1 (14.3)

1 (14.3)

2 (28.6)

3 (42.9)

Parainfluenza 2

1

0

0

0

1 (100.0)

Parainfluenza 3

32

6 (18.8)

11 (34.4)

2 (6.3)

13 (40.6)

Parainfluenza 4

4

1 (25.0)

2 (50.0)

0

1 (25.0)

Influenza A

16

8 (50.0)

4 (25.0)

0

4 (25.0)

Influenza B

9

2 (22.2)

2 (22.2)

2 (22.2)

3 (33.3)

Human rhinovirus

21

7 (33.3)

8 (38.1)

1 (4.8)

5 (23.8)

Enterovirus

5

2 (40.0)

1 (20.0)

0

2 (40.0)

Influenza A H1N1

4

1 (25.0)

3 (75.0)

0

0

Human metapneumovirus

1

0

0

0

1 (100.0)

Cytomegalovirus

80

16 (20.0)

21 (26.3)

4 (5.0)

39 (48.8)

Fungi

44

15 (34.1)

15 (34.1)

1 (2.3)

13 (29.5)

Bacteria

150

51 (34.0)

55 (36.7)

14 (9.3)

30 (20.0)

Protozoa

16

1 (6.2)

4 (25.0)

1 (6.2)

10 (62.5)

RSV = respiratory syncytial virus; HUU = HIV-unexposed and uninfected; HEU = HIV-exposed and uninfected; HIV+ = HIV-infected; HEUU = HIV exposure unknown and uninfected.

156 SAJCH DECEMBER 2017 Vol. 11 No. 4

RESEARCH RSV was the most commonly identified virus (44.7%), followed by adenovirus , which accounted for 26.7% of all isolates. Other viruses included parainfluenza (types 1, 2, 3 and 4), influenza A and B, influenza A H1N1 (a subtype of the influenza A virus), human rhinovirus and enterovirus. Other microbes identified by various other methods included bacteria, fungi and Pneumocystis jirovecii pneumonia (PCP) and cytomegalovirus (CMV) (Table 3).

Although RSV was the most commonly identified virus, the mortality rate owing to RSV infection was only 14.7% (n=23/156). The highest mortality rate was in patients from whom influenza A H1N1 virus had been isolated â&#x20AC;&#x201C; there were only 4 patients in this category but the mortality rate was 50.0% (n=2/4). Adenovirus had a mortality rate of 21.5% (n=20/93), followed by influenza A with a mortality rate of 18.8% (n=3/16). The mortality rate in patients with concomitant infections was as follows: CMV infection 16.3% (n=13/80; p=0.995); fungal infection 43.2% (n=19/44) (p=0.0); and bacterial infection 23.3% (n=35/150; p=0.002).

Discussion

LRTIs remain a significant cause of morbidity and mortality in the paediatric community. Mortality in childhood pneumonia is highest in children <2 years of age[4] and is responsible for 45% of under-5 mortality globally.[10] Forty-four percent of under-5 deaths occur during the neonatal period owing to preterm birth complications, pneumonia and intrapartum-related complications.[10] A systematic review of the literature by Slogrove et al.[11] found that HEU infants were at a greater risk for infectious morbidity and mortality compared with HUU infants with more severe manifestation of disease and more frequent hospitalisation. The greatest relative difference between HEU and HUU infants in morbidity and mortality occurs beyond the neonatal period, as it wanes by the second year of life.

With the resource limitations and inadequate ICU bed availability in KZN, it is often challenging for medical personnel to decide ethically on which patients should be prioritised for respiratory support in PICUs. HIV-infected patients may present with various infections, recurrent

infections and prolonged infections. However, this study has shown that viral LRTIs are common in both immunocompetent and immunocompromised patients and that patients may require respiratory support regardless of their immune status. Furthermore, it may be expected that HIV-infected patients harbour a viral infection for longer with a longer period of viral shedding; however, this study showed that the overall length of stay in the PICU and the duration of respiratory support was between 8 and 14 days and 4 to 7 days, respectively, irrespective of HIV status.

Additionally, the mortality rate in patients with viral LRTIs was shown to be similar in HIV-positive patients and HIV-negative patients requiring respiratory support.

Our study confirmed that RSV is the most common cause of viral LRTI in SA, where a 2-fold increase in the annual incidence of hospitalisation and a higher case fatality ratio was found in HIV-infected children who were not on antiretroviral treatment and had severe RSV-associated acute LRTI. This increased risk was greatest during infancy. Even with HIV treatment, the case fatality ratio in SA remains higher in HIV-infected children compared with HIV-uninfected children.[12] CD4 cell counts and viral loads are surrogate markers of disease progression in children and adults. The normal absolute CD4 cell count varies widely with age, therefore CD4% is preferred in children <5 years of age. Both CD4% and viral load are independent predictors of clinical progression, although CD4% is the stronger predictor.[6] Only 9 of the 12 deaths that occurred in the HIV-positive group had documented CD4 cell counts and viral loads. As expected, more than half of them had CD4% values of <25.0% and viral loads of >10Â 000 copies/mL. Although these numbers are too small to be statistically significant, the immune status of these patients most likely played a role in their outcome.

Study limitations

One of the limitations of the study was that we only looked at viruses identified by the viral multiplex PCR test and therefore some of the viruses that cause significant respiratory morbidity and mortality were not included in this study. Measles has been described as causing

Table 4. Association of microbes with HIV status and mortality rates HIV status, n (%) Microorganism

Mortality, N

HUU

HEUU

HEU

HIV+

RSV

23

6 (26.1)

1 (4.4)

15 (65.2)

1 (4.4)

Adenovirus

20

8 (40.0)

1 (5.0)

4 (20.0)

7 (35.0)

Parainfluenza 1

0

0

0

0

0

Parainfluenza 2

0

0

0

0

0

Parainfluenza 3

5

0

1 (20.0)

0

4 (80.0)

Parainfluenza 4

0

0

0

0

0

Influenza A

3

2 (66.7)

0

1 (33.3)

0

Influenza B

1

1 (100)

0

0

0

Human rhinovirus

3

2 (66.7)

0

0

1 (33.3)

Enterovirus

0

0

0

0

0

Influenza A H1N1

2

1 (50.0)

0

1 (50.0)

0

Human metapneumovirus

0

0

0

0

0

Cytomegalovirus

13

2 (15.4)

0

5 (38.5)

6 (46.2)

Fungi

19

5 (26.3)

0

7 (36.8)

7 (36.8)

Bacteria

35

11 (31.4)

1 (2.9)

17 (48.6)

6 (17.1)

Protozoa

2

0

0

0

2 (100)

HUU = HIV-unexposed and uninfected; HEU = HIV-exposed and uninfected; HIV+ = HIV-infected; HEUU = HIV exposure unknown and uninfected; RSV = respiratory syncytial virus.

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RESEARCH more severe illness in immunocompromised patients but this virus is not detected by the multiplex PCR test. CMV has also been shown to be an opportunistic infection in immunocompromised patients with significant mortality but it is tested for using a different molecular test.

In this study we did not differentiate patients with only a viral infection from those who were co-infected with other microbes or had superimposed bacterial infection. Overall, HIV-positive patients were found to have a higher incidence of co-infection with other microbes.

A major limitation of the study was that this was a purposive retrospective sample of patients during a defined time period and as such may not have had the required power to show statistically significant differences between the HIV-infected and HIV-uninfected patients in terms of associations between mortality, birth weight and weight-for-age category.

Conclusion

Owing to resource constraints, viral multiplex PCR testing is not widely available in our public hospitals and therefore diagnosing viral infections in paediatric patients remains a clinical diagnosis in most parts of KZN. Although this study was a retrospective observational study of a small population, it showed that patients with viral LRTI who require respiratory support have a similar outcome regardless of HIV status.

Also of note, was the observation that 89.2% of the HIV-infected children were admitted without being on HIV treatment, which highlights the importance of increasing efforts to ensure adherence to the new SA guidelines of testing all HIV-exposed infants at birth and starting treatment for those that test HIV-positive immediately.[8] Acknowledgements. The authors would like to acknowledge Dr KE Letebele, medical manager at IALCH, for giving us permission to conduct this research at the hospital. We would also like to acknowledge the National Health Laboratory Service for providing us with essential information for this project to proceed.

Author contributions. NPM: Developed the initial draft, collected the data and worked on the project to completion. AC: Reviewed every draft and assisted with writing and editing; approved the final manuscript. ST: Conceptualised the project and assisted with editing. FN: Performed the statistical analysis and assisted with writing the final article.

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Funding. None.

Conflicts of interest. None.

1. Mahony JB. Detection of respiratory viruses by molecular methods. Clin Microbiol Rev 2008;21(4):716-747. https://doi.org/10.1128/cmr.00037-07 2. Pavia AT. Viral infections of the lower respiratory tract: Old viruses, new viruses, and the role of diagnosis. Clin Infect Dis 2011;52(S4):S284-S289. https://doi.org/10.1093/cid/cir043 3. Kitchin OP. The role and management of viruses in hospital and community aquired pneumonia. Paediatric Focus 2013;4(4):5-7.

4. Zar HJ. Childhood Pneumonia in Africa – a major challenge for child health.

S Afr Respir J 2013;19(4):114-116.

5. National Health Laboratory Service (NHLS). Clinician’s Handbook. Durban: NHLS, 2014.

6. Ozeas G, Ricardo FL, Bruno GB. Update on viral community-aquired pneumonia. Revista da Associacao Medica Bradileira 2013;59(1):78-84.

7. National Department of Health (NDoH). The 2013 National Antenatal Sentinel HIV Prevalence Survey South Africa. Pretoria: NDoH, 2015.

8. NDoH. National Consolidated Guidelines for PMTCT and the Management of HIV in Children, Adolescents and Adults. Pretoria: NDoH, 2015.

9. Mhlongo OB, Moyo F, Mazanderani AF, Sherman GG. HIV PCR testing at birth in KZN, South Africa – one year post introduction of the largest neonatal HIV testing programme. Abstract, Eighth International Workshop on Paediatrics. Durban, South Africa 15 - 16 July 2016. Rev Antiviral Ther Infect Dis 2016. http://www.infectiousdiseasesonline.com/wp-content/ uploads/2016/07/8th-HIVPediatrics_abstractbook_ 10. Liu L, Oza S, Hogan D, et al. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: An updated systematic analysis. Lancet 2015;385(9966):430-440. https://doi. org/10.1016/s0140-6736(14)61698-6 11. Slogrove L, Goetghebuer T, Cotton F, Singer J, Bettinger J. Pattern of infectious morbidity in HIV-exposed uninfected infants and children. Front Immunol 2016;7:Article 164. https://doi.org/10.3389/fimmu.2016.00164 12. Moyes J, Cohen C, Pretorius M, et al. Epidemiology of respiratory syncytial virusassociated acute lower respiratory tract infection hospitalizations among HIVinfected and HIV-uninfected South African children, 2010-2011. J Infect Dis 2013;208(Suppl 3):S217-S226. https://doi.org/10.1093/infdis/jit479

Accepted 10 May 2017.

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RESEARCH

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Infant hearing screening in a developing-country context: Status in two South African provinces K Khoza-Shangase, PhD (Audiology); A Kanji, PhD (Audiology); L Petrocchi-Bartal, MA (Audiology); K Farr, BA (Speech Hearing Ther) Department of Speech Pathology and Audiology, School of Human and Community Development, University of the Witwatersrand, Johannesburg, South Africa Corresponding author: K Khoza-Shangase (Katijah.Khoza@wits.ac.za) Background. Newborn hearing screening (NHS) programmes are an important step toward early detection of hearing loss and require careful examination and planning within each context. The Health Professions Council of South Africa (HPCSA) has recommended specific contexts in which to actualise early hearing detection and intervention (EHDI) application. It is therefore imperative to explore if, and how, the current experience measures up to these recommendations.

Objective. To explore the feasibility and the current status of the implementation of NHS at various levels of healthcare within the South African context.

Methods. A non-experimental, descriptive, cross-sectional survey research design was employed, using a combination of questionnaires and face-toface semi-structured interviews. Participants comprised 30 primary healthcare (PHC) nursing managers across two provinces (Gauteng and North West) and 24 speech-language therapists and/or audiologists directly involved with NHS in secondary and tertiary levels of care within Gauteng.

Results. Our findings indicated that there was a lack of formal, standardised, and systematic EHDI implementation at all three levels of health care (primary, secondary and tertiary) with valuable reasons such as insufficient knowledge, lack of equipment, budgetary constraints, and human resource challenges being provided for this. Regardless of the level of care and varied resource allocations and levels of specialisation,EHDI implementation as advocated by the HPCSA in its 2007 position statement currently does not seem feasible, unless the number of barriers identified are addressed, and NHS becomes mandated.

Conclusion. Our findings have highlighted the need to ensure that context-specific studies in EHDI are conducted to ensure that national position statements are sensitive to contextual challenges and therefore allow for evidence-based practice, particularly in developing countries where resource constraints dictate success and/or failure of any well-intended programme.

S Afr J Child Health 2017;11(4):159-163. DOI:10.7196/SAJCH.2017.v11i4.1267

There is a need for context-relevant research aimed at facilitating effective provision of early hearing detection and intervention (EHDI) services in South Africa (SA). Early detection of hearing loss is the initial stage in any EHDI programme, and is conducted by means of newborn hearing screening (NHS).[1] This has become standard practice in developed countries, with universal newborn hearing screening (UNHS) being implemented as a preferred mandated early childhood healthcare standard,[1] unlike in most developing countries where it is not mandated.

[2] Adherence to the early intervention principles as they pertain to audiology is the goal of any efficacious intervention programme.

These principles include a recommendation for diagnosis of hearing impairment with early intervention services implemented by 6 months of age internationally,[3] and by a maximum of 8 months of age in SA.[4] In SA, where different levels of healthcare exist, NHS programmes have not been standardised. Evidence indicates that where these programmes are implemented, there are differences between the public and private healthcare sectors, as well as between the various levels of healthcare from primary (such as primary healthcare clinics, community healthcare centres and midwife obstetric units) to secondary and tertiary levels, such as regional and provincial hospitals.[5] The current practice is that where hearing screening occurs, it does so at an individual level with ‘targeted’ hearing screening being the practice rather than UNHS, and this has also been implemented haphazardly.[6] Targeted hearing screening in babies with risk factors for hearing loss has its pitfalls, particularly where risk factors relevant to the context have not been well documented and categorised. SA, as a developing country, has not been able to implement UNHS or systematic and uniform targeted NHS as part of EHDI for various reasons.[6] Reasons for the lack of EHDI implementation have included, firstly, resource constraints

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that have forced the SA Department of Health to have key priorities within the health sector. These priorities tend to be focused on saving lives rather than addressing quality of life in individuals with nonthreatening conditions, such as hearing loss. Specifically, the burden of life-threatening diseases such as HIV/AIDS and tuberculosis receives higher priority ratings than habilitation services. Secondly, resource constraints in the form of personnel also impact the implementation of UNHS programmes nationally. There is a documented short supply of qualified audiologists in the country in relation to population size, with the public healthcare sector having the most obvious supplydemand mismatch.[7] It is because of this high patient-audiologist ratio that the current authors support de-specialisation of screening services to personnel other than audiologists who can be trained to perform hearing screening with regulated minimum standards to adhere to.

Such personnel could include nurses as well as the new planned cadre of professionals in the form of middle-level workers (i.e. audiology technicians). This alternative planning is important when one considers that the developing world is reported to be home to two-thirds of the world’s children with hearing loss. In SA, where the public sector sees the highest numbers of people born with hearing loss, the prevalence is 3 - 6 per 1 000 births[2] – this alternative planning is therefore crucial when one considers the negative impact of unidentified and/or late identified hearing impairment.

Detection of hearing impairment may be low on the priority list and presents with comparatively less urgency within the risk/benefit calculation of the DoH. However, there is evidence for the importance of normal hearing function in childhood development. Hearing impairment affects areas such as cognition, language, literacy development and educational competence, social and emotional competence, as well as

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RESEARCH

Methods

The aims of the research were to explore the current status of newborn and infant hearing screening (NIHS) at primary healthcare level (clinicbased) and to explore the current status of NIHS at secondary and tertiary care levels (hospital-based).

A non-experimental, descriptive, cross-sectional survey design was employed, using a combination of questionnaires and face-to-face semi-structured interviews. This was conducted within a variety of healthcare contexts, with sampling through non-probability purposive sampling. Participants comprised 30 primary healthcare (PHC) nursing managers across two provinces (Gauteng (GP) and North West (NWP)) and 24 speech-language therapists and/or audiologists who were directly involved with NIHS within Gauteng.

For the PHC nurses to be included in the current research, they were required to be in charge of the PHC clinic’s overall functioning, were

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to be working within either Gauteng or the North West Province; and needed to be conversant in English as the interviews were conducted in English. For the speech-language therapists and/or audiologists to be included in the research, they needed to be qualified and registered with the Health Professions Council of South Africa, be employed within public healthcare facilities at secondary and tertiary levels (hospital based); and be involved in neonatal screening programmes as part of their workload.

Ethical clearance was obtained from the University of the Witwatersrand ethics committee prior to the research being conducted (ref. no. M091040 & M1411105). The structured questionnaire consisted of demographic information, work context, hearing screening context, and information management and quality control. The interviews were also tape recorded. Data from the nursing managers were collected via verbatim documentation of respondents’ answers and audio recordings of interviews that were transcribed. Data from the speech-language therapists and/or audiologists were collected from self-administered questionnaires.

To ensure research reliability, controls were exercised pertaining to participant variables, questionnaire and interview parameter, as well as data analysis procedures. Site observations and an independent rater during data analysis, as well as pilot studies, were employed to ensure reliability and validity. Data were analysed qualitatively through descriptive statistics. Data were analysed qualitatively and through thematic content analysis where transcriptions were evaluated to determine and code the emerging themes. Quantitative data analysis, through the use of frequency calculations, were condensed into tabular format for ease of frequency comparisons, and these were then depicted into graphical presentations. Data from the PHC level were handled, analysed and presented separately from the secondary and tertiary levels.

Results

Primary healthcare level

As depicted in Figs 1 and 2, none of the PHC clinics reported offering formalised NIHS. None of the clinics had the necessary equipment to provide hearing screening, with significant reliance on otoscopy and medical record reviews. More than half of the respondents in the Gauteng Province (53.3%) and a quarter of those in the North West Province (26.7%) believed that general budgetary issues were probable reasons for the lack of hearing screening services at their clinics. All the participants in Gauteng and more than two-thirds in the North West (73.3%) cited human resource (HR) restrictions as a major factor in the lack of NIHS programmes in PHC in these provinces. Only 10% (n=3/30; NWP) of respondents cited district management decisions as the reason for the lack of NIHS, where district-level authorisation was Participants, %

the individual’s vocational and thus financial outcomes – this highlights the importance of EHDI to individuals, families, as well as to societies and governments.[7] It is important that EHDI receives attention in the planning and budgeting of any health department and this should include efficient and effective screening measures to ensure that NHS is conducted in a valid, reliable and ethical manner.

A variety of objective screening measures may be employed within an NHS programme.[4.6] These include otoacoustic emissions (OAEs), automated auditory brainstem response (AABR), or a combination of OAE and AABR. OAEs have been proven to be simple, fast, and cheaper, but have the disadvantages of providing limited assessment of the auditory system and being negatively impacted by vernix, middle-ear fluid and ambient noise. AABR is known to provide more information regarding the auditory system and has the added advantage of providing better detection of auditory neuropathy in infants. However, AABR does require more knowledge and expertise to conduct than OAEs, which limits the number of screening personnel who can utilise it unless they are trained. AABR is also typically more costly and requires a longer test time compared with OAEs.[6] These factors related to screening measures may influence the implementation of a comprehensive screening programme within different contexts.

Various EHDI position statements recommend the use of different screening measures for different screening contexts. As an example, the Joint Committee on Infant Hearing (JCIH) recommends the use of OAE or AABR for infants admitted to well-infant nurseries and AABR for infants admitted to the neonatal intensive care unit (NICU), while the Health Professions Council of South Africa’s (HPCSA)[4] position statement in 2007 recommended the use of AABR for infants who had been admitted to the NICU, and OAE for screening during immunisation visits at PHC clinics within the SA context.[3,4] While the ideal hearing screening measure within the SA context is yet to be defined, it is clear that the use of objective measures which are minimally invasive, and are quick to administer, is key to successful screening programmes.

Given SA’s socioeconomic, cultural and linguistic diversity, considerations of congruency in the implementation of international standards to the context is of paramount importance. The HPCSA has recognised the need for contextual and cultural congruency for EHDI to be effective within the SA context.[4] To ensure effective and relevant implementation of EHDI and to continuously improve the limited existing EHDI services, the authors argue for the importance of evidence-based assessments of these international standards within the SA healthcare context. Owing to the paucity of contextually relevant evidence, our study was conducted within the various levels of the public healthcare sector where it has been observed (and reported) that hearing screening is not peformed routinely. It is also within this context that clinical services are most commonly accessed by the majority of South Africans. Localising this research within these levels of public healthcare is also viewed as strategic, particularly with the re-engineering of primary healthcare with the new National Health Insurance plans.

100 80 60 40 20 0 Is formalised screening conducted?

Is formalised screening equipment available?

Are HPCSA screening guidelines followed?

Is budget allocation the reason for the lack of screening?

Is HR allocation the reason for the lack of screening?

NWP NO (n=15)

100

100

100

73.4

26.7

NWP YES (n=15)

0

0

0

26.7

73.3

GP NO (n=15)

100

100

100

46.7

0

GP YES (n=15)

0

0

0

53.3

100

Fig. 1. Infant hearing screening programmes at the primary healthcare level in the two provinces and factors influencing its implementation (N=30). (NWP = North West Province; GP = Gauteng Province.)

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RESEARCH

Secondary and tertiary level (hospital-based)

Participants, %

All 24 participants (audiologists and/or speech-language therapists) indicated that they were involved in NHS. Sixteen (67%) reported to be involved in ‘targeted’ (where only neonates with risk factors are screened) NHS programmes, while 8 (33%) conducted UNHS programmes; 7 of them were employed at tertiary healthcare facilities, which indicates that ‘targeted’ NHS is the predominant approach used within the hospital context. Regarding the risk factors used for ‘targeted’ NHS, 5 participants (21%) reported complying with the HPCSA risk factors, 4 (17%) reported using the JCIH recommendations and 4 (17%) reported using risk factors from both position statements. One participant mentioned the use of risk factors that had been adapted from the Gauteng Early Hearing Prevention and Intervention Guidelines (unpublished guidelines developed by the Gauteng National Forum of Audiologists), while 10 (42%) did not respond to the question. It is evident from these results that slightly less than 50% of the participants within the sample 100 90 80 70 60 50 40 30 20 10 0 Otoscopy

Behavioural responses through noise makers

6.7 93.3 6.7 93.3

NWP NO (n=15) NWP YES (n=15) GP NO (n=15) GP YES (n=15)

80 20 60 40

Medical records reviewed on indication of auditory problem

Medical record reviewed at immunisations or milestone review

13.3 86.7 33 67

26.7 73.3 46.7 53.3

Participants, %

Fig. 2. Measures used for infant hearing screening at the primary healthcare level in the two provinces (N=30). (NWP = North West Province; GP = Gauteng Province.)

100 90 80 70 60 50 40 30 20 10 0

NWP (n=15) GP (n=15)

were uncertain about the risk factors that informed their protocols and practices. Furthermore, it was evident that great variability exists among audiologists within the Gauteng PHC sector (secondary and tertiary) regarding the risk factors they employed in the NHS programmes – the variation in the age at which infants received their initial hearing screening. For UNHS programmes, all screenings were reported to be conducted before 3 months of age; while 6 months is the cut-off age for ‘targeted’ NHS. The most commonly listed age for the initial hearing screening was established as ‘below 1month of age’ by 42% (n=10/24) participants. Despite the great variability in our findings, all screening was conducted before 6 months of age.

The various contexts in which participants reported to conduct the initial NHS are shown in Fig. 4. The NICU was found to be the most common screening context reported by 58% of the participants, with screening at newborn follow-up clinics being second (54%) within these levels of healthcare – these values do not add up to 100% as participants could engage in screening at more than one context.

The measures used by participants to conduct initial hearing screenings (as shown in Fig. 5) were as follows: 75% (n=18/24) reported using both distortion product otoacoustic emmissions (DPOAE) and AABR, and 13 of them indicated the additional use of at least one outer-ear or middle-ear screening measure, such as otoscopy, highfrequency (1 000 Hz probe tone) and acoustic reflex screening; 21% (n=5/24) reported using DPOAE and AABR, with no use of outer and middle ear screening measures; 21% (n=5/24) reported using either DPOAE or AABR; and 1 participant reported using only otoscopy and tympanometry for NIHS. Of the 14 participants who screen in the NICU or at discharge from the NICU, 12 reported making use of AABR as one of the screening measures.

Inconsistencies were noted in the measures used by participants across the different facilities as well as within the same facility.

Participants, n

required for the execution of NIHS services. Fig. 3 shows the findings of an in-depth analysis of HR-related issues that were cited as factors influencing the implementation of NIHS, including the HR budget, reduced staff training, general budget issues, staff shortages, and space.

In both provinces, reduced staff training and staff shortages were the most frequently cited HR-related factors, with reduced staff training being the leading HR challenge cited by 66.7% of the respondents from Gauteng.

24 22 20 18 16 14 12 10 8 6 4 2 0

14

13

6 4

3

0 NICU Well-baby nurseries

ICs

Triage

NFUCs

KMC

1

1

DSC

DDC

2 PAC

Possible screening contexts in hospital

Fig. 4. Contexts at secondary and tertiary heathcare levels in which participants conduct newborn hearing screening in Gauteng (N=24). (NICU = neonatal intensive care unit; ICs = immunisation clinics; NFUCs = newborn followup clinics; KMC = kangaroo mothercare; DSC = Down syndrome clinic; DDC = developmental delay clinic; PAC = paediatric audiology clinic.)

4%

DPOAE and AABR with at least 1 outer- or middle-ear measure

21%

DPOAE and AABR with no outer- or middle-ear measures

HR budget

Reduced staff training

General budget issue

6.7 0

20 66.7

13.3 6.7

Staff shortage 13.3 13.3

Space

21%

6.7 0

0 6.7

Fig. 3. Human resources reasons for lack of infant hearing screening at the primary healthcare level in the two provinces. (HR = human resources; NWP = North West Province; GP = Gauteng Province.)

161

54%

Unsure

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DPOAE or AABR Only outer- or middle-ear measures

Fig. 5. The percentage of participants making use of various initial hearing screening measures at secondary and tertiary healthcare levels in Gauteng.

(DPOAE = distortion product otoacoustic emmissions; AABR = automated auditory brainstem response.)

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RESEARCH Discussion

Our results revealed that no PHC clinics within the North West and Gauteng were performing formalised hearing screening as endorsed by the HPCSA position statement. Budgetary and HR issues, mainly staff training and staff shortages, were underscored as the main reasons why this clinical service gap of EHDI exists. It was evident that financial reasons were significant factors influencing clinics’ staff training, staff complement, equipment availability and physical structure. The documented inequalities in district finance allocation[8] may explain the variation in the responses between the two provinces. Our findings indicate that the recommendations in the HPCSA’s 2007 position statement have not been successfully implemented at the PHC level, where 85% of South Africans access healthcare. The inability and failure to implement EHDI has significant repercussions that have been well documented. EHDI services are considered the basis for achieving the most favourable outcomes in infants with hearing loss.[2,4,6] Arguably, our findings might be rationalised within the context of considering the burden of HIV/AIDS and TB in SA, which continue to dominate the health priorities of the national government over non-life-threatening conditions, such as hearing loss.[7] Furthermore, EHDI in SA are in the early stages of development with very little contextual evidence for their effectiveness and applicability.[7] Reports in the literature confirm the importance of advocating for legislation to mandate EHDI,[2,6,7] instead of the current reliance on caregiver concern as the primary identifier of possible hearing loss. Our study aimed to provide contextual evidence to substantially guide the SA EHDI realisation process. Our findings strongly contend that the current HPCSA EHDI clinic guidelines are practicable. At present, fundamental barriers, including reduced resources, staff complement and training, and clinic budgets, preclude successful implementation of the guidelines. Despite these barriers, positive aspects were identified within the PHC immunisation schedule context – respondents were willing to implement formal hearing screening as part of the PHC immunisation schedule and patient return rates for immunisation would ensure a high patient yield.

This may relate to variation in the management of regional priorities and the higher level of authority that district-level governance is now able to employ.[8] To improve local accountability, decentralised management of health districts has been reinforced within the DoH strategic plan[8] and the HPCSA position statement recommends the inclusion of the accountable DoH division to jointly facilitate the appropriate hearing screening programme.[4] NIHS and the HSPCA 2007 guidelines need to be more adaptable to district-level hearing and screening practices, to make them fit for and applicable to the screening process. PetrocchiBartal and Khoza-Shangase[7] recognise that the SA PHC sector is frequently less resourced than the advanced private healthcare sector.

Theunissen and Swanepoel[9] referred to a shortage of equipment and staff as the main factors influencing NHS services in the SA context, and this is supported by our findings. The lack of staff training was stated as the main contributing factor to lack of NIHS in PHC. Although our study revealed important findings about the PHC context and SA EHDI initiatives, we included only 30 clinics from two provinces, which limits the generalisability of the findings.

The results from secondary and tertiary levels of care indicate the use of a ‘targeted’ approach to NHS. This is in contrast to the HPCSA’s call for the implementation of UNHS. This call for widespread UNHS was based on at least two studies,[6,10] which reported that reported 50% of congenital hearing losses would be missed in the case of ‘targeted’ NHS, as not all children with congenital hearing loss present with risk factors. Nine years after the position statement was released, it is evident that a complete move from ‘targeted’ to universal NHS has not been made. Theunissen and Swanepoel[9] found that UNHS was conducted in just 2% of the hospitals included in their study. Although the current research considered the protocols that are adhered to by individual

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audiologists and not the general hospital protocols, our findings suggest that adherance to UNHS protocols is increasing compared with those of Theunissen and Swanepoel.[9] Regarding the NHS protocols adhered to by participants, variation was noted between the participants from different research sites, as well as between participants employed within the same facility. Inconsistent responses were found with regard to the risk factors that were adhered to for NHS. This was noted for both the general risk factors as well as risk factors that are specific to the delayed-onset hearing loss. There was also variation in the age at which initial hearing screening was conducted.

The HPCSA[4] stipulates that the protocols that are developed and carried out may vary between contexts because they need to be tailored to the specific needs of the community and the facilities. Furthermore, the programmes need to be developed in a way that maximises followup and ensures minimal false-positive results.[4] However, the HPCSA position statement[4] outlines that a team of professionals who are responsible for the screening within each specific context must develop the protocol to ensure minimal variation within a healthcare facility.

Theunissen and Swanepoel[9] reported similar findings of variability and reported that screening procedures across Gauteng were unsystematic.

They also reported that hearing screening was not routinely conducted as per the recommendations in the HPCSA and JCIH EHDI position statements. The World Health Organization (WHO)[11] makes note of the existence of similiar protocol variations as were discovered in our study and states that this variation is not necessarily due to financial or technological differences but rather to educational differences and the varying value that is placed on NHS, which emphasises the importance of adequate NHS education in obtaining standardised procedures.

With regard to the measures used for screening, the majority of the participants reported having access to objective screening measures.

These measures are endorsed by the HPCSA[4] EHDI position statement because they display excellent sensitivity and specificity for hearing loss detection. The HPCSA endorses the use of both OAEs and AABR for different screening environments. As AABR is more sensitive to neural pathologies and infants who stay in the NICU are at a greater risk for developing neural pathologies, the HPCSA recommends AABR for screening in this environment.[6] We found that this stipulation was being complied with by the majority of the participants at the secondary and tertiary levels of care, as only two of the participants screening in NICU contexts reported not including the use of AABR in their test battery.

Conclusion

Our findings emphasise the importance of carefully structured studies evaluating the applicability of the HPCSA 2007 protocol implementation.

Continuously assessing hearing screening protocol guidelines and/ or position statements ensures evidence-based practice and enforces programme implementation that is contextually relevant and explicit at any given point in time. This is especially true where programme application can be significantly affected by barriers such as reduced resources. Current findings also illustrate the importance of political support for the implementation of programmes. Mandating NHS by the NDoH will not only ensure regulations around EHDI, but will also facilitate resource allocation to ensure that services are delivered.

Careful planning with regards to research focus within the SA context should have standardisation of NHS protocols as a priority in order to allow for evidence-based implementation. Successful implementation will require careful compilation of protocols, collaboration between staff at facilities within specific districts and/or provinces as well as between the various levels of healthcare, discussion at provincial and national forums, and the provision of in-service training of audiologists, and other professionals, about correct NHS practices and protocols may further aid the implementation of standardised practice. Additionally,

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RESEARCH there is a need for research on the NHS practices at a national level. This research should be ongoing to determine the changes in NHS practices and whether these practices are improving in terms of the alignment with HPCSA recommendations. Information from the research along with data on the benchmark and quality indicators stipulated in the HPCSA 2007 position statement will assist in continually evaluating the status of EHDI in SA. Further research may discover improved methods for ensuring that the NHS and post-neonatal care pathways are sustainable in the public healthcare sector.

Acknowledgements. None Author contributions. All authors contributed equally to the preparation of the manuscript.

Funding. None Conflicts of interest. None 1. Burke M, Shenton RC, Taylor MJ. The economics of screening infants at risk of hearing impairment: An international analysis. Int J Pediatric Otorhinolaryngol 2012;76:212-218. https://doi.org/10.1016/j.ijporl.2011.11.004 2. Khoza-Shangase K, Michal G. Early intervention in audiology: Exploring the current status from a developing country context. Br J Med Medic Res 2014;120(4):2238-2249. https://doi.org/10.9734/bjmmr/2014/7322 3. Joint Committee on Infant Hearing. Year 2007 position statement: Principles and guidelines for early hearing detection and intervention programs.

Pediatrics 2007;120(4):898-921. https://doi.org/10.1542/peds.2007-2333

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4. Health Professions Council of South Africa. Early Hearing Detection and Intervention Programmes in South Africa, Position Statement Year 2007. http://www.hpcsa.co.za/Uploads/editor/UserFiles/downloads/speech/early_ hearing_detection_statement.pdf (accessed 14 December 2017).

5. Cullinan K. Health services in South Africa: A basic introduction. 2006. http:// www.health-e.org.za/wp-content/uploads/2013/04/Health_services_briefing_ doc.pdf (accessed 15 April 2016).

6. Kanji A, Khoza-Shangase K. Feasibility of newborn hearing screening in a public hospital setting in South Africa: A pilot study. S Afr J Comm Disorders 2016;63(1):a142. https://doi.org/10.4102/sajcd.v63i1.150 7. Petrocchi-Bartal L, Khoza-Shangase K. Infant hearing screening at primary healthcare immunisation clinics in South Africa: The current status. S Afr J Child Health 2016;10(2):139-143. https://doi.org/10.7196/SAJCH.2016.v10i2.1114 8. National Department of Health (NDoH). Strategic plan 2010/11 -2012/13.

Pretoria: NDoH, 2010. http://www.nationalplanningcycles.org/sites/ default/files/country_docs/South%20Africa/south_africa_strategic_health_ plan_2010-2013.pdf (accessed 29 May 2010).

9. Theunissen M, Swanepoel DW. Early hearing detection and intervention services in the public health sector in South Africa. Int J Audiol 2008; 47(Suppl 1):S23-S29. https://doi.org/10.1080/14992020802294032 10. Chu K, Elimian A, Barbera J, Ogburn P, Spitzer A, Quirk JG. Antecedents of newborn hearing loss. Obstet Gynecol 2003;101(3):584-588. https://doi. org/10.1097/00006250-200303000-00027 11. World Health Organization. Newborn and Infant Hearing Screening: Current Issues and Guiding Principles for Action. Geneva: WHO, 2010.

Accepted 29 March 2017.

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RESEARCH

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Implementation of the Road-to-Health-Booklet health promotion messages at primary health care facilities, Western Cape Province, South Africa L M Du Plessis, PhD; H E Koornhof, M Nutr; M L Marais, M Nutr; R Blaauw, PhD Division of Human Nutrition, Department of Global Health, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa Corresponding author: L M du Plessis (lmdup@sun.ac.za) Background. Age-specific health promotion messages appear in the Road-to-Health booklet (RtHB), an assessment and monitoring tool for child health in South Africa. Healthcare workers should communicate health promotion messages to caregivers at each clinic visit. This investigation was part of a larger RtHB survey.

Objective. To assess the implementation of health promotion messages and identify barriers to its successful implementation.

Methods. A cross-sectional descriptive study with analytical components was conducted in the Western Cape Province. Knowledge and practices of caregivers and healthcare workers were assessed at 143 randomly selected primary healthcare facilities. Information was obtained through questionnaires, direct observation of consultations and recording of health promotion material in facilities.

Results. In total, 2 442 children (0 - 36 months; mean (standard deviation) age 5.10 (6.24) months), 2 481 caregivers and 270 healthcare workers were included. Caregivers’ educational level varied, with only 24.3% having completed Grade 12. Healthcare workers had a median of 5 (range 0.5 - 37.0) years᾽ work experience in primary healthcare. All healthcare workers indicated that health promotion messages were important, however, messages were only conveyed in 51% of observed consultations. When it was communicated, health promotion messages were age-appropriate in 97% of cases. Barriers to the implementation of health promotion messages hinged on time and staff constraints, workload and language barriers. Various forms of health promotion material were available in facilities.

Conclusions. Suboptimal implementation of the health promotion messages in the RtHB are apparent despite healthcare workers realising the importance of health promotion. Barriers to optimal implementation must be urgently addressed by the National Department of Health and healthcare workers in partnership with caregivers and with support from society to promote child health and care.

S Afr J Child Health 2017;11(4):164-169. DOI:10.7196/SAJCH.2017.v11i4.1414

With the conception of primary healthcare (PHC) at Alma Ata in 1978 to promote health for all, health promotion was included as one of the tools to address the inequality in healthcare globally.

The International Conference on Primary Health Care stated that health promotion was also vital to sustain global economic and social development.[1] South Africa (SA)’s first comprehensive Strategic Plan for Maternal, Newborn, Child and Women’s Health and Nutrition (2012 - 2016) was launched in 2012.[2] The plan embraces primary healthcare (PHC) and aims to reduce mortality and improve the health and nutritional status of women, mothers, newborns and children through promotion of healthy lifestyles and provision of integrated, high-quality health and nutrition services.

At PHC level, the National Department of Health (NDoH) replaced the Road-to-Health card with a Road-to-Health booklet (RtHB) as a national assessment and monitoring tool for child health in February 2011.[3] The RtHB is a comprehensive tool and includes records for the following interventions: immunisation; developmental screening; oral health; health promotion (HP); growth monitoring; infectious diseases, including HIV and tuberculosis; vitamin A supplementation; and deworming. The HP section includes agespecific health promotion messages (HPMs) related to infant and young child feeding, communication and play. It also includes messages about feeding during illness and the danger signs of childhood illnesses. The intention is that healthcare workers (HCWs) should communicate the applicable and age-appropriate messages to caregivers (CGs) at each clinic visit.[3] Our study formed part of a larger survey which aimed to evaluate the implementation of the RtHB among children aged 0 - 36 months and their CGs attending PHC facilities in the Western 164

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Cape Province (WC), SA. This section of the research aimed to assess the implementation of the health promotion component of the RtHB, and to identify barriers to its successful implementation.

The implementation of the HP component of the RtHB is reported separately from the larger survey, since this intervention differs from other interventions in the RtHB. While the other interventions in the RtHB are administered to or performed on children and require CGs to attend the clinic, the HP component is focused on behavioural changes in CGs and HCWs’ knowledge.

Methods

A full account of the study methodology has been described elsewhere.[4] For this part of the survey, the knowledge and practices of CGs and HCWs with regards to infant and young child feeding (IYCF) and care, and the role of the RtHB in this regard, were assessed.

This survey was conducted over a 3-year period (2012 - 2014) to coincide with the ongoing rollout of the RtHB. A total of 143 PHC facilities across all 6 health districts (Cape Town City, Cape Winelands, Central Karoo, Eden, West Coast and the Overberg) in the WC was surveyed. Two health districts were selected for each year of the survey. Lists of all functional PHC facilities (defined as operational facilities not being renovated or overly involved with other research activities) in each district were obtained from the WC DoH. A random proportional sample of 35% of all facilities was selected from each region. To optimise sample size, PHC facilities with annual attendance figures of <2 000 children aged <5 years were excluded.

All HCWs responsible for the implementation of the RtHB were recruited at each facility, provided informed consent was obtained.

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RESEARCH As the rollout of the RtHB continued, children aged 0 - 12 months, 0 - 24 months and 0 - 36 months, as well as their CGs were recruited during years 1 (2012), 2 (2013) and 3 (2014), respectively.

Data collection was conducted over 2 days at each facility to allow sufficient time for interviews and observations. At each facility, consecutive eligible children between the ages of 0 and 36 months were recruited. The CGs of these children were screened and those who met the selection criteria were included in the study. Only CGs with a child of suitable age qualified for participation in the survey.

CGs who were unable to converse in English, Afrikaans or isiXhosa, visiting the clinics for specialist services, private or emergency care or not in possession of their children’s RtHBs (n=123) ,were excluded.

CGs who qualified and who gave informed consent were interviewed using a researcher-administered questionnaire. All questionnaires were professionally translated and available in English, Afrikaans and isiXhosa, and a translator assisted researchers where required.

Furthermore, consultations with the HCW were observed.

A pilot project was conducted after all investigators had been trained and standardised. Data from the pilot project were not included in the final analysis. Questionnaires and checklists were tested for face validity during the pilot studies and for content validity by eight experts in the field of dietetics and nutrition.

The researcher-administered questionnaire consisted of two sections: (i) basic demographic information; and (ii) questions on CGs’ knowledge and IYCF practices. CGs were asked comprehensive questions about their young child’s food intake for the 24-hour period prior to the survey. These questions were structured to list all possible options for infants younger than 6 months and those older than 6 months.

Following the interview, the researcher accompanied the CG to the HCW consultation and completed the observation checklist, noting which messages were included in the consultation, the messages most frequently covered, whether the messages were age-appropriate, and if CGs’ understanding of the HPMs was assessed by HCWs. HCWs who conducted the consultations with the CGs, a maximum of 3 per clinic, were asked to complete a self-administered questionnaire after informed consent was obtained. This questionnaire obtained information on basic demographics, the training which HCWs had received relating to the RtHB, as well as HCWs’ knowledge and practices relating to IYCF and HP. HCWs were also asked to report how often they counselled CGs on the HPMs in the RtHB and on their perceived barriers to successful implementation of these messages.

A checklist was completed to assess the use of HP material in clinics, which included posters, pamphlets and other educational aids. The head nurse was also questioned about the existence and perceived success of HP programmes in the facility.

Other Other FV Vitamin A-rich FV Eggs MFC or organ meats Dairy products Legumes or nuts Cereals or potato

Data were captured and analysed using Microsoft Office Excel and STATISTICA version 12, (StatSoft Inc., USA). Data were presented using descriptive statistics or median (interquartile range (IQR)) values when not normally distributed. The latter were tested with the ShapiroWilk test. Contingency tables were used when comparing two nominal variables, and independence was tested using the maximum-likelihood (M-L) χ2 test; a p-value <0.05 was considered statistically significant. In cases where data did not reflect the total study population, the relevant numbers are indicated in brackets.

Ethics approval

Ethical approval was obtained from the Health Research Ethics Committee of the Faculty of Health Sciences, Stellenbosch University (ref. no. N11/09/270) and the research committee of the DoH in the WC. Written informed consent was obtained from the CGs of children visiting the facility, as well as from HCWs responsible for implementation of the RtHB. Participants received a copy of the signed consent form. Confidentiality was ensured by allocating a unique identification number to each participant, which was used throughout the survey.

Results

Demographic information

In total, 2 442 children, 2 481 CGs and 270 HCWs who met all the inclusion criteria were recruited to participate in the survey. The mean (standard deviation (SD)) age of the children included was 5.10 (6.24) months (range 6 weeks - 34.15 months); 50.3% were male (boys, n=1 229 v. girls, n=1 213 (49.7%)). Eleven percent of CGs (n=281/2 481) had received no education or had not completed primary school.

Although 44.5% (n=1 105/2 481) had entered secondary school (grades 8 - 12), only 24.3% (n=604/2 481) had completed Grade 12, and 14.7% (n=365/2 481) had achieved a tertiary qualification. The majority of CGs (73.2%; n=1 815/2 477) were in possession of a functional mobile phone. Of the 270 recruited HCWs, most were female (97%; n=262/270) and had received tertiary education (69.3%; n=187/270).

Forty-two percent (n=113/269) of HCWs were professional nurses, 16.2% (n=44/269) were enrolled nurses, and 14.1% (n=38/269) were chief professional nurses, all of whom had a median (range) of 5.0 (0.5 - 37.0) years of work experience in PHC.

Health promotion practices on the day of survey

HCWs conveyed HPMs to CGs in 50.8% (n=1 169/2 300) of the observed consultations. Where HPMs were conveyed to CGs during the consultations, the HCWs ensured that CGs understood the messages in 70.9% (n=829/1 169) of cases. The percentage of CGs counselled

by HCWs varied significantly between districts, with only HCWs in Eden (63.7%; n=366/575) and West Coast (55.1%; n=216/392) districts conveying HPMs in >50% of observed consultations (p=<0.0001; M-L χ2).

The main HPM discussed with CGs in terms of IYCF was reported to be age-appropriate in 97.2% of cases (n=1 128/1 160). The message most often communicated in the 0 - 6 months age group was that of exclusive breastfeeding (n=330); in the 6 - 12 month age group it was the combination of breastfeeding and complementary feeding (n=106); and for the 12 month - 5 year age group, eating a variety of foods featured most commonly (n=39).

HCWs᾽ knowledge, attitudes, and practices

Tea Water Breastmilk 0

10

20

30

40

50

60

70

80

90

100

Prevalence, %

Fig. 1. Reported dietary intake of children ≥6 months old (n=785).

(MFC = meat, fish or chicken; FV = fruits and vegetables.)

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Forty-six percent of the HCWs (n=124/269) indicated that they ‘always’ counselled CGs about the HPMs in the RtHB and the rest (except one, who indicated ‘never’) indicated that they ‘sometimes’ counselled CGs (53.5%; n=144/269). All of the HCWs indicated that HPMs were important. Their responses also indicated that they felt that they had received adequate training to communicate these messages comfortably (82.6%; n=219/265) to CGs.

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RESEARCH Only HCWs who do not always council CGs on HPMs were asked to indicate why they do so Responses were received from 15 HCWs. These reasons related mainly to time constraints (73%; n=11), workload (40%; n=6), staff shortages (60%; n=9), and language barriers (40%; n=6). This resulted in HCWs relaying information in a brief manner, depending on a caregiver’s inclination to listen.

HCWs indicated different methods used to communicate the health promotion messages to the mothers/CGs. These methods included among others: reading them to the mother (42.0%); asking questions to establish if the mother/CG understands the messages (76.6%); telling the mother to read the messages at home (55.0%), discussing the messages in detail (53.2%); giving the mother/CG time to ask questions and clarify any misunderstandings (61.7%); and referring the mother to the dietician, if needed (68.8%).

When asked ‘At what age do you recommend foods other than breastmilk or formula feeds to be introduced to an infant?’ HCWs’ answers averaged at ~6 months, with the mean (SD) age recorded as 6.08 (1.45) months. Only 122 HCWs responded to the question, ‘For how long do you recommend to a HIV-negative mother that she breastfeeds her infant?’ Responses varied between ‘2 years and beyond’ (38.5%), ‘between 12 and 24 months’ (22.9%) and ‘no longer than 6 months’ (14.8%). Some HCWs also stated that the mother and baby could continue to breastfeed for as long as they wanted to (15.5%). Other options included ‘no longer than 12 months’ (6.6%) and ‘she should not breastfeed at all’ (1.6%).

CG knowledge, and feeding practices

When questioned, 66.3% (n=1 644/2 481) of CGs indicated that they had read the HPMs in the RtHB. Nearly 80% of CGs responded that they understood the messages (79.6%; n=1 308/1 644), 68.7% (n=1 129/1 644) regarded the HPMs as very important and 59% (n=972/1 644) felt that they could make use of the messages.

Although in the minority, it was concerning to note that some CGs did not know why HPMs were included in the booklet (2.4%; n=39) and were unsure of what to do with the messages (2.9%; n=47). CGs who indicated that they had not read the HPMs in the RtHB claimed that they were unaware of the HPMs (28.9%; n=242/837), were too busy (33.2%; n=278/837), did not understand the language (8.4%; n=70/837) were illiterate (4.5%; n=38/837) and did not think that it was important (6.0%; n=50/837).

According to the CGs, HCWs’ assessment of CGs’ existing knowledge regarding HPMs was shown to be limited. On the day of survey, only 53.0% (n=402/759) of the CGs who reported that they had not yet read the HPMs in the RtHB, actually received counselling on HPM. In addition, in a similar proportion of cases, HCWs did not check to ensure CGs’ understanding of the HPMs delivered to those who reported not to have understood the content of the RtHB (25.0%; n=68/272) v. those who reported an understanding (30.5%; n=260/853).

When asked about the meaning of the term ‘exclusive breastfeeding’, 50.2% (n=1 243/2 478) of CGs were able to respond correctly.

CGs’ understanding of the term ‘exclusive breastfeeding’ increased significantly with level of education (p=0.0001, M-L χ2). Significantly more CGs who indicated that they had read the HPM were able to correctly describe the term ‘exclusive breastfeeding’ (54.4%) compared with those who could not describe the term correctly (45.5%) (p<0.0001; M-L χ2).

Data on feeding practices were recorded for children who were younger (n=651) and older than 6 months (n=785) for the preceding 24-hour period. More children who were <6 months of age received complementary food and drinks such as tea, thin porridge and semisolid or solid food (n=355; 52%) than those who were exclusively breastfed (n=280; 43%) or infant-formula fed (n=36; 5.5%).

The dietary intake of children (≥6 months old) over the previous 24-hour period is shown in Fig. 1. Cereals or potato (87.5%; 166

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n=687/785), water (84.3%; n=662/785) and tea (35%; n=275/785) were the most commonly consumed sources of solid foods and fluids, followed by dairy (75.4%; n=592/785), vitamin A-rich fruit and vegetables (60.3%; n=473/785) and meat, chicken, fish or organ meats (55.2%; n=433/785).

No significant differences were found between the feeding practices of CGs who reported that they understood the content of the RtHB (80.2%; n=522/651) compared with those who did not (19.8%; n=129/651) (p=0.88; M-L χ2). In addition, the level of CGs’ education was not associated with feeding choice for children who were <6 months old (p=0.702), with the practice of mixed feeding shown to be high among all education levels. The level of education of the CGs of children who were reportedly exclusively breastfed varied as follows: 15.8% (n=44/279) had an education level below Grade 7; 81% (n=226/279) had reached grades 8 - 12; and 3.2% (n=9/279) had a postgraduate qualification. Although more CGs indicated that they had read the HPMs (66%; n=1 644), the feeding practices of those who read the messages did not differ significantly from those who indicated that they had not read them (p=0.78; M-L χ2).

Health promotion programmes and material

The use of resources and materials supporting HP, such as posters, pamphlets, and educational aids, was observed at facilities (n=142).

The majority (96.4%; n=137/142) of facilities made use of at least one type of HP resource. Most facilities made use of posters (95.1%; n=135/142) and pamphlets (83.8%; n=119/142) in coloured print, which were mainly sourced from non-governmental organisations (NGOs). Additional sources identified included the DoH, commercial companies, and academic institutes. More specifically, posters and pamphlets on child health were observed in 71 and 57 facilities, respectively. Posters and pamphlets were available in all three predominant languages in the study area, in 68.1% (n=92/135) and 69.7% (n=83/119) of the facilities, respectively.

Half of the observed facilities used additional educational aids (n=62/141), such as oral rehydration stations, diagrams, flip charts, books and booklets. The majority of the facilities were running HP programmes (n=111/142) that head nurses perceived to be successful (n=46/51). No data were obtained on the availability of health promoters.

Discussion

This sub-investigation of a larger RtHB survey assessed the implementation of the HP messages, mostly related to IYCF, in the RtHB at the PHC clinic level in the WC, SA and aimed to identify barriers to its implementation.

Both HCWs and CGs expressed their belief in the importance of HP, and almost half of HCWs reported that they ‘always’ counselled CGs on the HP messages in the RtHB. Similarly, it was observed that half of the HCWs counselled CGs on the HP messages on the day of the survey. The majority of CGs who were counselled on HPMs received age-appropriate messages and HCWs checked the CGs’ understanding of the messages. The majority of CGs also indicated that they understood the messages. Two-thirds of CGs indicated that they had read the messages. It was concerning to note that a third of the CGs had not read the messages and were unaware of their presence in the RtHB. Reasons for not counselling CGs on the HPMs hinged on time and staff constraints, as well as workload and language barriers. These barriers correspond with those reported in a national evaluation of services rendered to children <5 years of age in SA. The report revealed that nutrition support, education and counselling is not happening as part of normal service delivery owing to staff shortages, heavy workload and a lack of nutrition-trained personnel.[5] Improving the nutrition of infants and young children is critical for the improvement of their growth, nutritional status and health,

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RESEARCH and for the development of these children.[6-10] HCWs are considered the key link between policy and practice, placing a responsibility on this cadre to convey, among other, IYCF messages to CGs.[11-15] In order to improve IYCF practices in the country, all contact opportunities between HCW and CG at PHC facilities should be fully utilised. Nutrition and nursing managers should therefore create awareness around the strategic importance of nutrition education and promotion at the PHC level, as stipulated in the Roadmap for Nutrition (2013 - 2017).[16] SA national data indicate a relatively high breastfeeding initiation rate of 88%,[17] but only ~8% of babies are exclusively breastfed at the age of 6 months. Considering the very low average exclusively breastfed practices in SA, the reported exclusively breastfed practices in this survey seem high. Only half of the CGs could correctly describe the term ‘exclusively breastfed’, and it is most likely that exclusively breastfed practices were therefore over-reported. Other studies conducted in SA have indicated that the term ‘exclusively breastfed’ was not well understood or practised.[15,18] A chapter dedicated to breastfeeding in the South African Demographic and Health Survey (2016),[19] concluded that breastfeeding interventions with a solid evidence base for impact were, among others, the education levels of mothers and HCWs on the topic. Consistent and persistent messages on exclusive breastfeeding should therefore be communicated by all HCWs to mothers as a matter of urgency.

SA national data and reviews of national data indicate that a large percentage of infants receive solid foods within the first few days after birth, with an average age of introduction of other liquids/ foods between two and three months.[17,20,21] This trend of introducing solids and other complementary foods or liquids too early has been confirmed by smaller studies in the country.[22-25] From the reported mixed-feeding practices – breastmilk and formula milk, breastmilk and solid food, formula milk and solid food, or a combination of all three feeds – in the current survey, it seems that a large proportion of babies were fed other foods and fluids before the age of 6 months.

Data on the complementary diet further revealed that cereal and potato, as well as water and tea, were commonly consumed. A monotonous diet, high in bulky starch and containing low levels of micronutrients, is often used by SA mothers when introducing complementary foods. Water and tea are also commonly introduced fluids. These fluids displace other nutrients in the complementary diet, and in combination with dense, bulky starches of low nutrient density lead to growth faltering.[20] In SA, both undernutrition and overnutrition are prevalent in young children, which is partly due to poor breastfeeding and complementary feeding practices.[16] Despite economic growth, political and social transition, and the implementation of national nutrition programmes over the past few decades, malnutrition, especially stunting (low height-for-age), remains a stubborn problem that negatively impacts economic growth and prosperity.[26] Combined and focused efforts to improve nutrition during the first 1 000 days of life (from conception to a child’s second birthday) can have the most significant impact on stunting. All mothers should therefore receive the best possible nutrition and care during pregnancy, and every mother should be supported to breastfeed her child and introduce safe, adequate, nutritious food from 6 months of age, with continued breastfeeding up to 2 years of age and beyond.

This support should, in part, come from HCWs, but should be backed by a whole-of-society approach.[19] HCWs were of the opinion that they had received adequate training to convey HP messages with confidence. Their knowledge on the period of exclusive breastfeeding and timing of introduction of complementary foods was correct. HCWs knowledge of breastfeeding in the context of HIV was not optimal. According to the Department

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of Performance Monitoring and Evaluation report, the knowledge and skills of nurses depended upon the amount of nutrition training they had received in the previous 2 years. The report described the nutrition knowledge of nurses as being superficial, and mentioned that this problem was not found in KwaZulu-Natal where nurses had received nutrition training from the University of KwaZulu-Natal.[5] This report also found that behaviour change interventions including nutrition education, breastfeeding support, complementary feeding counselling, and growth monitoring scored lower (<50%) than clinical interventions, which were more effectively implemented.[5] This finding corresponds with global data describing the slow progress on nutrition interventions that require behaviour change modification.[8] Training of HCWs in nutrition, specifically in IYCN, is a contentious issue, with various international and national research studies indicating the need for refresher courses and retraining of HCWs in basic nutrition messages.[13,14,27-30] The DMPE report suggests the development and implementation of service standards and norms for, among others, nutrition education and counselling, to scale up services and communication to enhance nutrition-related interventions.[5] Infant feeding practices of CGs who reported to have read and understood the content of the RtHB and those who had not read or understand it were not significantly different. The practice of EBF is more important than the ability to describe the term correctly, yet, significantly more CGs who indicated that they had read the HPM were able to correctly describe the term EBF. CGs’ understanding of the term EBF was also shown to increase significantly with their level of education. Creating awareness of the HPMs to CGs as well as a broader investment in human capital, particularly educating teenagers, who are the ‘bearers and carers’ of the next generation,[31] could improve IYCF in SA. It is acknowledged that there are challenges to conducting HP in the PHC setting.[32,33] Alternative venues and methods for HP should therefore be investigated. A HP programme initiated by the SA NDoH in 2014, the ‘MomConnect’ programme, uses cellular phone technology to register pregnant women in both public and private healthcare. The programme empowers women by providing them with all the information and instructions that could ensure a healthy pregnancy and delivery of a healthy baby.[34] After delivery, the messages switch over to focus on information on the health needs of a new-born (including messages on exclusive breastfeeding, immunisation, family planning for the mother, oral rehydration during diarrhoea and check-up periods at the clinic) and continue for up to one year after birth.[35] Since the majority of CGs in this survey owned a mobile phone that was in working condition, the ‘MomConnect’ programme holds promise as an additional tool to strengthen and reiterate the HPMs in the RtHB.

Study limitations

The format of questioning on EBF knowledge was not ideal. In-depth questioning is necessary to explore this specific practice. Owing to the extent of the questioning on all sections of the RtHB, there was a time limit during the survey that did not allow for in-depth questioning.

Ideally, qualitative data would have complemented the quantitative data collection in this research. Focus group discussions, for example, could have provided more detailed and rich data in this regard.

Conclusion and recommendations

Health promotion to CGs of infants and young children is of critical importance to address the inequality of the health system and to ensure a healthy and productive nation in years to come. HCWs should therefore provide consistent, evidence-based messages and

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RESEARCH guidelines to CGs of infants and young children. Updates, continuous training and retraining of HCWs are therefore self-evident. At present, suboptimal implementation of the HPMs in the RtHB is apparent despite HCWs’ understanding of the importance of HP and efforts to relay these messages. The barriers to optimal implementation must be addressed by the NDoH in partnership with HCWs and CGs as a matter of urgency and this should be supported by society to enable child health and care to become more promotion-oriented and less reactive.

A checklist of all age-appropriate HPMs could be included in the RtHB to ensure that CGs are counselled on all aspects of IYCF. Currently, the HPMs in the RtHB only appear in English. Pamphlets or pocket-sized folded cards with translated HPMs into local languages could be made available to CGs who are not fluent in English.

Educational DVDs could be screened in waiting room areas and other technology, including mobile phone applications, could be utilised to convey HPMs, with cognisance to the educational level of CGs. Acknowledgements. We would like to convey our sincere thanks to the Western Cape Department of Health, specifically the Sub-Directorate Nutrition, for granting permission to conduct the survey. In addition, we would like to convey our sincere gratitude to all the caregivers, infants and healthcare workers at each facility who participated in our survey. Lastly, we would like to thank all the members of the RtHB survey research group, as well as the administrative staff members of the Division of Human Nutrition and Prof D. Nel from the Centre for Statistical Consultation, Stellenbosch University, for his statistical advice and support.

Author contributions. All authors contributed equally to study conceptualisation and design, data collection, analysis and interpretion, as well as writing the manuscript.

Funding. RB: Stellenbosch University (Fund for Innovation in Rural Research, Harry Crossley Foundation) and Western Cape Department of Health. No funder had any role in the design, analysis or writing of this article.

Road to Health Survey Research Group. Bam N, Blaauw R, Boshoff H, Clarke P, Coetzee C, Daniels L, de Kock I, de Vos I, de Vries K, du Buisson L, du Plessis LM, du Preez U, Ehlers A, Engelbrecht C, Evans N, Ferreira N, Findlay A, Foot J, Fordjour V, Frey C, Groenewald L, Hallinan T, Hartman D, Jackson G, J van Rensburg S, Jooste M, Kamhoot A, Kapena C, Kelly T, Kerbelker R, Koen N, Koornhof HEK, Kotlowitz J, le Grange M, le Roux M, Lee T, Liebenberg S, Louw A, Louw S, Marais ML, Maritz A, Martens A, Meyer I, Mncwabe N, Moens M, Morris N, Naude K, Nel M, Nel S, Nkomani S, Nyenes R, Olivier L, Pienaar T, Pilditch K, Potgieter S, Richardson C, Rickard L, Robinson R, Röhrs S, Samuels S-L, Simjee Z, Slazus C, Smit L, Smit Y, Stander L, Stone P, Strydom E, Strydom K, Swanich L, Swartz P, Swart D, Taverner T, Taylor A, Teuchert N, Turner L, Uys M, van de Venter A, van der Merwe L, van der Schyff S, van Niekerk E, van Rhyn N, van Wyk N, van Zyl F, Venter B, Verster B, Verster J, Visser J, Visser ME, Wasserfall L, Wakelin M, Webber S, Wicomb R, Yeh E. 1. World Health Organization (WHO). Declaration of Alma-Ata. International Conference on Primary Health Care. Alma-Ata, USSR. Geneva: WHO, 1978. http://www.who.int/publications/almaata_declaration_en.pdf (accessed 6 June 2017).

2. National Department of Health (NDoH). National Strategic Plan for Maternal, Newborn, Child and Women’s Health and Nutrition 2012 - 2016. Pretoria: NDoH, 2012.

3. NDoH. 2nd Triennial Report of the Committee on Morbidity and Mortality in Children Under 5 Years (COMMIC). Pretoria: NDoH, 2014.

4. Blaauw R, Daniels L, du Plessis LM, et al. Assessing the utilisation of a child health monitoring tool. S Afr J Child Health 2017;11(4):174-179. https://doi. org/10.7196/SAJCH.2017.v11i4.1326 5. NDoH, Department of Social Development, Department of Performance Monitoring and Evaluation, South Africa. Diagnostic/Implementation Evaluation of Nutrition Interventions for Children from Conception to Age 5. Pretoria: NDoH, 2014. http://www.nutritionsociety.co.za/attachments/ article/76/Summary-Evaluation-of-Nutritional-Interventions-for-Childrenfrom-Conception-to-Age-5-.pdf (accessed 6 June 2017).

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6. Bhutta ZA, Ahmed T, Black RE, et al. What works? Interventions for maternal and child undernutrition and survival. Lancet 2008;371(9610):417-440. https:// doi.org/10.1016/S0140-6736(07)61693-6 7. Dewey KG, Huffman SL. Maternal, infant and young child nutrition: Combining efforts to maximise impacts on child growth and micronutrient status. Food Nutr Bull. 2009;30(2):S187-S189. https://doi.org/10.1016/S01406736(07)61693-6 8. International Food Policy Research Institute (IFPRI). Global nutrition report 2014: Actions and accountability to accelerate the world’s progress on nutrition. Washington, DC: International Food Policy Research Institute, 2014. http://www.ifpri.org/publication/global-nutrition-report-2014-actions-andaccountability-accelerate-worlds-progress (accessed 6 June 2017).

9. Martorell R, Horta BL, Adair LS, et al. Weight gain in the first two years of life is an important predictor of schooling outcomes in pooled analyses from five birth cohorts from low- and middle-income countries. J Nutr 2010;140(2):348354. https://doi.org/10.3945/jn.109.112300 10. Victora CG, Adair L, Fall C, et al. Maternal and child undernutrition: Consequences for adult health and human capital. Lancet 2008;371(9609):340357. https://doi.org/10.1016/S0140-6736(07)61692-4 11. WHO, Global Health Workforce Alliance. Scaling up, saving lives. Geneva: WHO, 2008. http://www.who.int/workforcealliance/documents/Global_ Health%20FINAL%20REPORT.pdf?ua=1 (accessed 6 June 2017).

12. Kassier SM, Veldman FJ. Cry, the beloved bottle: infant-feeding knowledge and the practices of mothers and caregivers in an urban township outside Bloemfontein, Free State province. S Afr J Clin Nutr 2013;26(1):17-22.

13. Davies A. PMTCT: How ‘informed ‘is the literate mother’s decision regarding infant feeding options in the Gert Sibande district, Mpumalanga province, South Africa. M Nutr Thesis. Stellenbosch: Stellenbosch University, 2005. http://scholar.sun.ac.za/handle/10019.1/4957 (accessed 6 June 2017).

14. Van der Merwe S, Du Plessis LM, Jooste H, Nel D. Comparison of infantfeeding practices in two health sub-districts with different baby-friendly status in Mpumalanga province. S Afr J Clin Nutr 2015;28(3):121-127.

15. NDoH. Roadmap for nutrition in South Africa 2013 - 2017. Pretoria: NDoH, 2013.

16. Doherty T, Chopra M, Nkonki L, Jackson D, Greiner T. Effect of the HIV epidemic on infant feeding in South Africa: ‘When they see me coming with the tins they laugh at me’. Bull World Health Organ 2006;84(2):90-96. http:// www.who.int/bulletin/volumes/84/2/90.pdf (accessed: 6 June 2017) 17. Mhlanga RE. Maternal, newborn and child health: 30 years on. In: Barron P, Roma-Reardon J, eds. South African Health Review 2008. Durban: Health Systems Trust, 2008:115-128. http://www.hst.org.za/publications/841 (accessed 6 June 2016).

18. Du Plessis LM, Pereira C. Commitment and capacity for the support for breastfeeding in South Africa. S Afr J Clin Nutr 2013;26(3 Suppl):S120-S128.

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21. NDoH Statistics South Africa (SSA), South African Medical Research Council (SAMRC) and ICF. South African Demographic and Health Survey 2016: Key Indicators. Pretoria: NDoH, 2017 22. Sibeko L, Dhansay MA, Charlton KE, Johns T, Grey-Donald K. Beliefs, attitudes, and practices of breastfeeding mothers from a peri-urban community in South Africa. J Hum Lact 2005;21(1):31-38. https://doi. org/10.1177/0890334404272388 23. Faber M, Benade AJS. Breastfeeding, complementary feeding and nutritional status of 6-12-month-old infants in rural KwaZulu-Natal. S Afr J Clin Nutr 2007;20(1):16-24.

24. Mushaphi LF, Mbhenyane XG, Khoza LB, Amey AK. Infant-feeding practices of mothers and the nutritional status of infants in the Vhembe District of Limpopo Province. S Afr J Clin Nutr 2008;21(2):36-41.

25. Ghuman MR, Saloojee H, Morris G. Infant feeding practices in a high HIV prevalence rural district of KwaZulu-Natal, South Africa. S Afr J Clin Nutr 2009;22(2):74-79.

26. Said-Mohamed R, Micklesfield L, Pettifor J, Norris S. Has the prevalence of stunting of South African children changed in 40 years? A systematic review.

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28. Savage-King F. Helping mothers to breastfeed. Rev ed. Nairobi: African Medical and Research Foundation, 1992.

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30. Menghini KG. Designing and evaluating parent education materials. Adv Neonatal Care 2005;5(5):273-283. https://doi.org/10.1016/j.adnc.2005.07.003 31. Black RE, Victora CG, Walker SP, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013;382(9890):427-451. https://doi.org/10.1016/S0140-6736(13)60937-X

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RESEARCH 32. Wills J, Rudolph M. Health promotion capacity building in South Africa. Glob Health Prom 2010;17(3):29-34. https://doi.org/10.1177/1757975910375167.

33. Onya H. Health promotion in South Africa. Promot Educ 2007;14(4):233-237. https://doi.org/10.1177/10253823070140041001.

34. NDoH. Minister Aaron Motsoaledi: Health Department Budget Vote 2015/16. Pretoria: NDoH, 2015. http://www.gov.za/speeches/minister-aaronmotsoaledi-health-dept-budget-vote-201516-5-may-2015-0000 (accessed 6 June 2017).

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35. Peter J, Barron P, Pillay Y. Using mobile technology to improve maternal, child and youth health and treatment of HIV patients. S Afr Med J 2016;106(1):3-4. https://doi.org/10.7196/SAMJ.2016.v106i1.10209

Accepted 17 July 2017.

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RESEARCH

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Evaluation of culture-proven neonatal sepsis at a tertiary care hospital in Johannesburg, South Africa M M Lebea, MB ChB, DCH, FCPaed, MMed (Paed); V Davies, MB ChB, DCH, FCPaed Department of Paediatrics and Child Health, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa Corresponding author: M M Lebea (Mamaila.Lebea@wits.ac.za) Background. Organisms causing neonatal sepsis differ by region and the organisms causing sepsis change over time in the same area. The antibiotic susceptibility of microorganisms also changes with time, with emergence of multidrug resistant organisms.

Objective. This study aimed to review the causes of neonatal sepsis and antibiotic sensitivity of organisms causing neonatal sepsis at Charlotte Maxeke Johannesburg Academic Hospital (CMJAH) neonatal unit over a 12-month period.

Methods. This was a retrospective descriptive study. All blood cultures obtained from the neonatal unit at CMJAH between 1 January 2012 and 31 December 2012 were reviewed. This was followed by a review of the clinical data of patients with a positive culture.

Results. During the period under study, there were 196 patients with blood-culture-proven neonatal sepsis. This gave an incidence of 10.3 per 100 admissions. Late-onset sepsis accounted for 83.7% of cases of neonatal sepsis. The predominant isolates were Klebsiella pneumoniae (32.2%), coagulase-negative Staphylococcus (23.7%) and methicillin-resistant Staphylococcus aureus (13.1%). The majority of the isolated K. pneumoniae were extended-spectrum beta-lactamase (ESBL) producing bacteria with resistance to ampicillin and gentamicin.

Conclusion. Neonatal sepsis is a common problem at the CMJAH neonatal unit. There has been an increase in the predominance of Gramnegative microorganisms as a cause of neonatal sepsis in the CMJAH neonatal unit over recent years, with ESBL-producing K. pneumoniae and Acinetobacter baumannii being the most prevalent Gram-negative causative agents of neonatal sepsis. Coagulase-negative Staphylococcus spp. remains an important cause of neonatal sepsis, and is the most prevalent Gram-positive organism isolated from the neonatal unit at CMJAH. Resistance to commonly used antibiotics regimens was noted to be high in the unit.

S Afr J Child Health 2017;11(3):170-173. DOI:10.7196/SAJCH.2017.v11i4.1310

Neonatal sepsis is a significant cause of morbidity and mortality in newborns.[1-4] It is the cause of 1.6 million deaths per annum in developing countries.[1] Organisms causing neonatal sepsis differ in different regions and also change with time in the same area.[1,4,5] The antibiotic susceptibility of microorganisms also changes with time, with the emergence of multidrug resistant organisms.[1,4,5] A periodic survey of the causes of sepsis and their antibiotic sensitivity patterns is essential in the design of effective infection control programmes and in guiding empirical antibiotic therapy.[1,4] Factors associated with neonatal sepsis are well described in the literature.[6-8] The aim of this study was to review the causes of neonatal sepsis at the Charlotte Maxeke Johannesburg Academic Hospital (CMJAH) neonatal unit and to compare these results with those of previous audits conducted in the same unit.

Methods

The research protocol was submitted and approved by the Human Research Ethics Committee of the University of the Witwatersrand (ref. no. M130350) and the NHLS Ethics Committee.

This was a retrospective descriptive study conducted in the neonatal unit at CMJAH, which is a tertiary care institution. The hospital provides secondary- and tertiary-level services and functions as a referral centre for surrounding clinics and hospitals. All blood cultures obtained from the neonatal unit at CMJAH between 1 January 2012 and 31 December 2012 were reviewed. A list of positive blood cultures was obtained from the National Health Laboratory Service (NHLS) computer data warehouse. This was followed by a review of the clinical data of patients with a positive culture, to identify patients with blood-culture-proven neonatal sepsis. The results of the study were compared with two previous similar studies conducted in the unit.

The following definitions were used in the study: • Neonate was defined as an infant in the first 28 days of life.

• Culture-proven sepsis was defined as a pathogenic organism, either

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bacterial or fungal, isolated on blood culture with other clinical and laboratory features consistent with infection.

• Laboratory features of sepsis included an abnormal white cell count, reduced platelet count and/or a C-reactive protein (CRP) >10 mg/L. Age-appropriate definitions of low or high white cell count and reduced platelets count were used.

The following organisms were considered to be contaminants and were excluded from analysis: Micrococcus spp.; Bacillus spp.; Corynebacterium spp.; and Streptococcus viridans.

Coagulase-negative Staphylococcus was considered significant if two blood cultures drawn within 72 hours of each other grew the same organism or if there was a single positive blood culture in association with other laboratory features of sepsis.

When one significant organism was isolated from the same patient within 7 days, this was considered to be a single episode of sepsis.

Sepsis was categorised as early-onset (EOS) or late-onset sepsis (LOS).

EOS was defined as sepsis occurring within 72 hours of life and LOS as sepsis occurring after the first 72 hours of life. Patients with bacteraemia, but with no other features suggestive of sepsis, were excluded from analysis. Infants who were in the neonatal unit and developed sepsis beyond 28 days of life were also excluded from the study. Data were entered into a Microsoft Excel spreadsheet for data management and analysed using Statistica (Dell, USA).

Results

There were 1 903 admissions to the neonatal unit during the study period. This number included babies born and babies not born at the CMJAH. The incidence of neonatal sepsis was 10.3 per 100 admissions, which was based on blood culture-positive results for 196 of the neonates. The majority of cases of neonatal sepsis were of late onset and the median (interquartile range (IQR)) age at the onset of neonatal

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RESEARCH sepsis was 7 (4 - 14) days. Based on blood culture results, the incidence of EOS was 1.7 per 100 admissions (n=33), while the incidence of LOS was 8.6 per 100 admissions (n=164), which accounted for 83.7% of cases of neonatal sepsis (Table1).

In total, 236 microorganisms were isolated on blood culture of 196 patients with culture-proven neonatal sepsis during the study period.

Of the 196 patients, 7 had two episodes of neonatal sepsis and 4 had

Table 1. Patient data Characteristic

All cases of neonatal sepsis (N=196), n (%)*

Sex Male

117 (59.7)

Place of birth Inborn Outborn Unknown

136 (69.4) 53 (27.0) 7 (3.6)

Maternal HIV status Negative Positive Unknown

102 (52.0) 60 (30.6) 34 (17.3)

Antenatal booking status Yes No Unknown

119 (60.7) 56 (28.6) 21 (10.7)

Mode of delivery NVD C/S Unknown

96 (49.0) 78 (39.8) 22 (11.2)

Birth weight (g), median (IQR)

1 300 (1 000 – 1 720)

Gestational age (weeks), median (IQR)

30 (28 - 32)

NVD = normal vertex delivery; C/S = caesarean section; IQR = interquartile range. *Unless otherwise specified.

three episodes. There were 10 cases of polymicrobial sepsis, i.e. more than one organism was isolated per episode. Gram-negative organisms were the most commonly isolated organisms in cases of culture-proven neonatal sepsis (49.2%; n=116/236). Among the cases with Gramnegative organisms, most were due to ESBL Klebsiella pneumoniae (65.5%; n=76/116), Acinetobacter baumannii (17.2%; n=20/116) and Escherichia coli (10.3%; n=12/116). Gram-positive organisms constituted 42.4% (n=100/236) of the isolated organisms. Coagulase-negative Staphylococcus (56%; n=56/100) and methicillin-resistant Staphylococcus aureus (31%; n=31/100) were the most commonly isolated Grampositive organisms. Yeasts accounted for 8.5% (n=20/236) of the isolated organisms (Table 2).

Table 3 shows the patterns of antibiotic susceptibility for the most commonly isolated Gram-negative organisms in our study. Susceptibility results were not available for all the isolated organisms. Overall, there were high levels of resistance to ampicillin (94.6%), gentamicin (86.7%) and ceftazidime (66.1%). Klebsiella pneumoniae was mostly sensitive to meropenem (98.4%; n=63/64), amikacin (89.4%; n=59/66) and piperacillin/ tazobactam (70.3%; n=45/64). K. pneumoniae was resistant to ampicillin, gentamicin and cefotaxime – all of the isolated strains were resistant to ampicillin and 98.4% were resistant to gentamicin and cefotaxime.

Acinetobacter baumannii was mostly sensitive to amikacin (65%; n=13/20) and ceftazidime (75%; n=15/20), with high levels of resistance to gentamicin (85%) and meropenem (80%). All of the isolated A. baumannii were resistant tazobactam/piperacillin. All of the isolated E. coli were sensitive to meropenem and cefotaxime, and a number of isolates were also sensitive to amikacin (65%; n=13/20) and tazobactam/ piperacillin (92.8%; n=13/14). Only 57.1% of the E. coli isolates were sensitive to gentamicin.

Bacterial isolates in the current study were considerably different from those obtained in a similar study in the same unit in 2002/3 audit, with some similarities to the 2009/2010 audit (Table 4).

Discussion

This study confirmed that pathogens causing neonatal sepsis change over time, and further emphasises the need for ongoing surveillance.[1,4,5] There has been a significant increase in the predominance of Gramnegative microorganisms as a cause of neonatal sepsis in the CMJAH

Table 2. Organisms causing neonatal sepsis Organism

Neonatal sepsis (N=236), n (%)

EOS (N=39), n (%)

LOS (N=197), n (%)

Gram-positive CONS MRSA Enterococcus faecalis GBS Enterococcus faecium Listeria monocytogenes

100 (42.3) 56 (23.7) 31 (13.1) 7 (3.0) 3 (1.3) 2 (0.8) 1 (0.4)

19 (48.7) 12 (30.8) 3 (7.7) 2 (5.1) 2 (5. 1) 0 0

81(41.1) 44 (22.3) 28 (14.2) 5 (2.5) 1 (0.5) 1 (0.5) 1 (0.5)

Gram-negative ESBL-producing Klebsiella pneumoniae Acinetobacter baumannii Escherichia coli Klebsiella oxytoca Klebsiella pneumoniae Pseudomonas aeruginosa Enterobacter cloacae

116 (49) 76 (32.2) 20 (8.5) 14 (5.9) 2 (0.8) 2 (0.8) 1 (0.40) 0

20 (51.3) 9 (23) 7 (17.9) 2 (5.1) 2 (5.1) 0 0 0

96 (48.7) 67 (34.0) 13 (6.6) 12 (6.1) 0 2 (1.0) 1 (0.5) 1 (0.5)

Fungi Candida albicans Candida parapsilosis Candida glabrata

20 (8.4) 13 (5.5) 5 (2.1) 2 (0.8)

0 0 0 0

20 (10.1) 13 (6.6) 5 (2.5) 2 (1.0)

EOS = early-onset sepsis; LOS = late-onset sepsis; CONS = coagulase-negative Staphylococcus; MRSA = methicillin-resistant Staphylococcus aureus; GBS = group B Streptococcus; ESBL = extended-spectrum beta-lactamase.

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RESEARCH pneumoniae. In 2012, a study by Ballot et al.[4] showed that 70.8% of the isolated K. pneumoniae were ESBL-producing strains compared with 97.3% in the current study. ESBL-producing isolates tend to be resistant to beta-lactam antibiotics, including third-generation cephalosporins and to other classes of drugs such as aminoglycosides, co-trimoxazole, tetracycline and fluoroquinolones.[15] These organisms pose a major challenge with limited therapeutic options, particularly in resourcechallenged countries.[15] S. aureus and A. baumannii are two other organisms that are becoming predominant in the unit. Ballot et al.[4] noted the importance of A. baumannii as a cause of neonatal sepsis in the unit, when this microorganism accounted for 10% of the bacterial isolates compared with the previous study where this organism was not isolated.[3] The emergence of resistant organisms causing neonatal sepsis is now a worldwide problem.[1] Reports of multiresistant bacteria causing neonatal sepsis in developing countries are on the increase.[1] The current study also showed increasing resistance to commonly used antibiotics. Most of the isolated K. pneumoniae and A. baumannii were resistant to ampicillin and gentamicin, which were the first-line antibiotic agents used in EOS. Overall, 94.6% and 86.7%, of the top 3 gram-negative organisms causing sepsis were resistant to ampicillin and gentamicin, respectively. These organisms also showed high resistance against the ceftazidime with an overall resistance of 66.1%, which is a major concern given that 40.9% of organisms isolated in cases of EOS were due to these organisms. Regarding the treatment of LOS, amikacin and tazobactam/piperacillin were used as first-line agents. Most of the

neonatal unit during recent years. The high proportion of Gram-negative microorganisms as a cause of neonatal sepsis is similar to the findings of surveillance studies in other developing countries, where Gram-negative organisms were shown to be the predominant causative agents in both EOS and LOS.[1,9] The most common isolate overall was K. pneumoniae, followed by CONS, MRSA and A. baumanii. The predominance of K. pneumoniae in the current study agrees with several reports from Nigeria and other developing countries.[9] CONS, a Gram-positive organism, was the most common isolate from cases with EOS. CONS has remained an important cause of neonatal sepsis in our unit and accounted for 23.7% of the microorganisms isolated in this study. This was contrary to reports from other developing countries where CONS was usually among the least commonly isolated organisms,[10] however, this may be because CONS is usually excluded from analysis, as it is often considered to be a contaminant, despite the fact that it is a pathogen in neonates, immunocompromised individuals and patients with foreign bodies such as central venous catheter.[10-12] Further evaluations, such as repeat blood cultures, are required to determine the clinical significance of CONS.[11,13] The importance of CONS as a cause of neonatal sepsis has been reported elsewhere in studies in developed countries and developing countries.[11,14] A one-year prospective study in 8 neonatal units in Australia reported that CONS was the most commonly isolated organism.[11] There has been a significant increase in the proportion of Klebsiella spp. isolated from our unit, with the emergence of ESBL-producing K.

Table 3. Sensitivity of the isolated Gram-negative organisms Bacteria Klebsiella pneumoniae

Acinetobacter baumannii

Escherichia coli

Antibiotics

NT

RS

%

NT

RS

%

NT

RS

%

Overall resistance, %

Ampicillin

64

64

64.0

15

13

86.0

4

11

78.6

94.6

Gentamicin

64

63

98.4

20

17

85.0

14

5

35.7

86.7

Amikacin

66

7

10.6

20

7

35.0

14

2

14.3

16.0

Tazobactam/ piperacillin

64

19

26.7

20

20

100

14

1

7.1

19.0

Meropenem

64

1

1.6

20

16

80.0

14

0

0

17.3

Cefotaxime

64

63

98.4

0

0

0

14

0

0

1.3

Ceftazidime

64

61

95.3

20

5

25.0

14

7

50.0

66.1

NT = number tested; RS = number of resistant strains.

Table 4. Bacterial isolates at Charlotte Maxeke Johannesburg Academic Hospital: 2002 - 2012 Organism

2002 - 2003, n/N (%)

2009 - 2010, n/N (%)

2012, n/N (%)

Gram-positive CONS Staphylococcus aureus Enterococcus faecalis GBS Enterococcus faecium Listeria monocytogenes Streptococcus viridans

79 (68.1) 65 (56.0) 4 (3.4) 4 (3.4) 2 (1.7) 0 0 4 (3.4)

134 (54.4) 62 (22.5) 23 (8.3) 13 (4.7) 10 (3.6) 11 (4.0) 0 15 (6.1)

100 (46.3) 56 (25.9) 31 (14.3) 7 (3.2) 3 (1.4) 2 (0.9) 1 (0.5) 0

Gram-negative Klebsiella spp.

Acinetobacter baumannii Escherichia coli Pseudomonas aeruginosa Other Gram-negative organisms

37 (31.9) 12 (10.3) 0 20 (17.2) 2 (1.7) 3 (2.6)

112 (40.5) 47 (18.3) 27 (11.0) 23 (9.3) 4 (1.6) 11 (4.5)

116 (53.7) 80 (37.0) 20 (9.2) 14 (6.5) 1 (0.5) 1 (0.5)

CONS = coagulase-negative Staphyloccus; GBS = group B Streptococcus.

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RESEARCH K. pneumoniae isolates were sensitive to these antibiotics, while A. baumannii was mostly sensitive to amikacin and ceftazidime.

Study limitations

There were some limitations, which resulted from the retrospective nature of the study. Study participants were identified based on blood culture results. Due to the retrospective nature of the study, researchers had no control over how the blood cultures were collected. If strict measures to ensure sterility were not employed while taking blood cultures, and if inadequate volumes were taken, the sensitivity and specificity of the blood cultures may have been affected. The susceptibility to antimicrobial agents only looked at commonly used agents and susceptibility results were not available for all of the isolates. A further limitation to this study is that the data were collected 4 years ago and therefore may be considered outdated. However, no recent data have been published from this unit and the change in different organisms isolated between the time period of this study and previously published studies from the same unit remains significant and emphasises the need for periodic surveillance to determine the prevalence of different organisms causing neonatal infections at different times. This information should inform decisions on rational antibiotic therapy.

Conclusion

Neonatal sepsis is a common problem in the CMJAH neonatal unit.

There has been an increase in the predominance of Gram-negative microorganisms as a cause of neonatal sepsis in the CMJAH neonatal unit over the years, with ESBL K. pneumoniae and A. baumannii being the most prevalent isolates. Coagulase-negative Staphylococcus remains an important cause of neonatal sepsis, and is the most commonly isolated Gram-positive organism. Resistance to commonly used antibiotic regimens was high. The increase in the predominance of Gram-negative microorganisms, especially resistant organisms, is of serious concern. We recommend that a prospective study be conducted to establish whether this indeed is true and, if so, that changes be made in the first-line regimens for EOS and LOS. Acknowledgements. ML would like to thank Dr Charl Verwey and Dr Kebashni Thandarayen for assistance with the statistics, as well as the staff at the CMJAH neonatal unit and NHLS. Author contributions. ML: primary author, analysed data; VC: supervised study, reviewed manuscript.

Funding. Self-funded Conflicts of interest. None.

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1. Vergnano S, Sharland M, Kazembe P, et al. Neonatal sepsis: An international perspective. Arch Dis Child Fetal Neonatal Ed 2005;90(3):F220-F224. https:// doi.org/10.1136/adc.2002.022863 2. Rasul C, Hassan M, Habibullah M. Neonatal sepsis and use of antibiotic in a tertiary care hospital. Pak J Med Sci 2007;23(1):78-81.

3. Motara F, Ballot D, Perovic O. Epidemiology of neonatal sepsis at Johannesburg Hospital. S Afr J Epidemiol Infect 2005;20(3):90-93. https://doi.org/10.1080/1 0158782.2005.11441243 4. Ballot D, Nana T, Sriruttan C, et al. Bacterial bloodstream infections in neonates in a developing country. ISRN Pediatrics 2012;1-6. https://doi. org/10.5402/2012/508512 5. Mackay C, Ballot D, Perovic O. Serum 1,3-beta-D-glucan assay in the diagnosis of invansive fungal disease in neonates. Pediatric Rep 2011;3(2):45-48. https:// doi.org/10.4081/pr.2011.e14 6. Shah G, Budhathoki S, Das B, et al. Risk factors in early neonatal sepsis.

Kathmandu Univ Med J 2006;4(2):187-191.

7. Chiesa C, Panero A, Osborn J, et al. Diagnosis of neonatal sepsis: A clinical and laboratory challenge. Clin Chem 2004;50(2):279-287. https://doi.org/10.1373/ clinchem.2003.025171 8. Stephanie J, Cutland C, Zell E, et al. Risk factors for neonatal sepsis and perinatal death among infants enrolled in the prevention of perinatal sepsis trial, Soweto, South Africa. Pediatr Infect Dis J 2012;31(8):821-826. https://doi. org/10.1097/inf.0b013e31825c4b5a 9. West B, Peterside O. Sensitivity pattern among bacterial isolates in neonatal septicaemia in Port Harcourt. Ann Clin Microbiol Antimicrob 2012;11(7):1-6. https://doi.org/10.1186/1476-0711-11-7 10. Gwee A, Coghlan B, Everett D, et al. Bacteraemia in Malawian neonates and young infants 2002-2007: A retrospective audit. BMJ 2012;2(3):1-7. https://doi. org/10.1136/bmjopen-2012-000906 11. McMillan J, Feign R, DeAngelis C, et al. Oski's Pediatrics: Principles and Practice. 4th ed. Philadelphia: Lippincot Williams & Wilkins, 2006.

12. Kliegman RM, Behrman RE, Jenson HB, Stanton BF. Nelson Textbook of Pediatrics. 18th ed. Oxford: Elsevier, 2007.

13. Cervilla J, Fraga J, Riestra G, et al. Neonatal sepsis: Epidemiologic indicators and relation to birth weight and length of hospitalization time. An Esp Pediatr 1998;48(4):401-408.

14. Isaacs D, Barfield C, Grimwood K, McPhee AJ, Minutillo C, Tudehope DI. Systemic bacterial and fungal infections in infants in Australian neonatal units.

Australian Study Group for Neonatal Infections. Med J Aust 1995;162(4):198-201.

15. Chandel D, Johnson, R Chaudhry, et al. Extended-spectrum b-lactamaseproducing Gram-negative bacteria causing neonatal sepsis in India in rural and urban settings. J Med Microbiol 2010;60(4):500-507. https://doi.org/10.1099/ jmm.0.027375-0

Accepted 29 March 2017.

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RESEARCH

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Assessing the utilisation of a child health monitoring tool R Blaauw, PhD (Nutr); L Daniels, MPH; L M du Plessis, PhD (Nutr); N Koen, PhD (Nutr); H E Koornhof, M Nutr; M L Marais, M Nutr; E van Niekerk, PhD (Nutr); J Visser, M (Nutr) Division of Human Nutrition, Tygerberg Academic Hospital, Stellenbosch University, Cape Town, South Africa Corresponding author: R Blaauw (rb@sun.ac.za) Background. The Road-to-Health booklet (RtHB), a standardised national tool for growth monitoring and the assessment of health among children from birth to five years of age, was introduced in South Africa in February 2011.

Objectives. The study assessed the implementation of growth monitoring and promotion, immunisation, vitamin A supplementation, and deworming sections of the RtHB. Caregivers’ (CGs) and healthcare workers’ (HCWs') knowledge, attitudes and practices were investigated as well as HCWs’ perceptions of barriers undermining implementation.

Methods. A cross-sectional descriptive study was conducted on a proportional sample of randomly selected primary healthcare facilities across six health districts (35%; n=143) in the Western Cape Province. HCWs involved in the implementation of the RtHB booklet, children (aged 0 - 36 months) and CGs were included. Information was obtained through scrutiny of the RtHB, observation of consultations and structured questionnaires.

Results. A total of 2 442 children, 2 481 CGs and 270 HCWs were recruited. Weight measurements (94.7%, n=2 251/2 378) were performed routinely. Less than half (40.2%; n=997/2 481) of CGs reported that their child’s growth had been explained to them. Sixty-eight percent of HCWs (n=178/260) correctly identified criteria for underweight classification, whereas only 55% (n=134/245) and 39% (n=95/245) could do so for stunting and wasting, respectively. The RtHB sections were completed adequately for immunisation (89.3%; n=2 171/2 431) and vitamin A supplementation (94.6%; n=1 305/1 379) but not for deworming (48.8%; n=176/361). Most HCWs (93%; n=209/223) knew the correct regimens for vitamin A supplementation, but few CGs knew when treatment was due for vitamin A supplementation (16.4%, n=409/1 646) and deworming (26.2%; n=650/2 481). Potential barriers identified related to inadequate training, staff shortages and limited time.

Conclusion. Focused efforts and resources should be channelled towards HCWs’ training and monitoring regarding growth monitoring and promotion to optimise utilisation of the RtHB. Mobilisation of community health workers is needed to strengthen community awareness of preventive health interventions.

S Afr J Child Health 2017;11(4):174-179. DOI:10.7196/SAJCH.2017.v11i4.1326

Nearly half of all deaths in children under five are caused by malnutrition.[1] This is not only due to a lack of sufficient and adequately nutritious and safe food, but also various processes that involve among others healthcare, education, sanitation and hygiene. Good nutritional status leads to higher individual earnings and mental acuity, which in turn support macroeconomic and societal growth.[2] Therefore, malnutrition impairs productivity, which poses a strain on national growth. In this regard malnutrition represents a barrier to the successful achievement of the Sustainable Development Goals (SDGs).[2] The importance of growth monitoring and promotion (GMP) as part of preventive and curative health to reduce malnutrition and mortality is recognised worldwide.[3] The South African (SA) government is committed to reducing mortality and morbidity among mothers and children as reflected in the key strategic outcomes for the health sector.[4] The Road-to-Health chart (RtHC), which was based on the National Centre for Health Statistics (NCHS) reference data, was previously used as a child health monitoring tool in SA. This two-page patient-held record was used to assess weight-for-age and to chart immunisations, deworming, and vitamin A supplementation;[5,6] however, appropriate implementation of this tool was a challenge.[6] In 2007, an evaluation of the RtHC conducted in three public healthcare centres in Gauteng Province showed that it was not used effectively as a curative, preventive or promotive tool for monitoring child health as neither healthcare workers (HCWs) nor parents utilised it optimally.[5] A revision of the RtHC in SA was necessary owing to the 2006 release of the World Health Organization (WHO) growth standards, the increasing prevalence of childhood stunting, overweight and obesity and changes made to childhood immunisation schedules. A

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28-page Road-to-Health booklet (RtHB) was developed to be used nationally as of February 2011. It includes the following preventive and treatment interventions: immunisation; developmental screening; oral health; health promotion; growth monitoring; infectious diseases (including human-immunodeficiency virus (HIV) and tuberculosis (TB)); vitamin A supplementation; and deworming.[7] This survey aimed to assess the implementation of the RtHB among infants and children (referred to collectively as children) aged 0 - 36 months and their caregivers (CGs) attending primary healthcare (PHC) facilities in the Western Cape Province (WC), SA. The objectives were to: (i) evaluate the implementation of GMP, immunisation, vitamin A supplementation (6 - 36 months), and deworming components of the RtHB; (ii) investigate the knowledge, attitudes and practices of both CGs and HCWs relating to these components; and (iii) identify HCWs’ perceptions of the barriers undermining appropriate implementation of the RtHB.

Methods

Ethical disclosure

The survey was approved by the Health Research Ethics Committee of Stellenbosch University (ref. no. N11/09/270) and the research committees of the Department of Health (DoH), WC, and the City of Cape Town.

Written informed consent was obtained from the CGs of children visiting the facility, as well as from HCWs responsible for implementation of the RtHB. Participants received a copy of the signed consent form.

Confidentiality was ensured by allocating a unique identification number to each participant, which was used throughout the survey.

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RESEARCH Sample selection

To coincide with the ongoing rollout of the RtHB, this survey was conducted over three phases during the period 2012 to 2014. A total of 143 PHC facilities across all 6 health districts in the WC were surveyed.

Two health districts were selected for each phase of the survey. Lists of all functional PHC facilities (defined as operational facilities not being renovated or overly involved with other research activities) in each district were obtained from the WC DoH. A random proportional sample of 35% of all facilities was selected from each region. To optimise the sample size, PHC facilities with annual attendance figures of <2 000 children aged <5 years were excluded.

During each phase of the survey, all HCWs responsible for the implementation of the RtHB were recruited at each facility, provided that informed consent was obtained. As the rollout of the RtHB continued, children aged 0 - 12 months, 0 - 24 months and 0 - 36 months, as well as their CGs, were recruited during phases 1, 2, and 3, respectively.

Children and their CGs were eligible for inclusion if CGs were present and in possession of the new RtHB, were able to communicate in English, Afrikaans or isiXhosa (the three official languages in the WC), and if they had resided in the WC for 6 months prior to the survey. Children and CGs were excluded if they attended the facility for a reason unrelated to the child, or if emergency medical care was required. In the case of more than one child per CG, only one child was selected with the use of a simple randomisation procedure. Where possible, children and their CGs were recruited consecutively, once informed consent was obtained.

Data collection

Data were collected over a period of 2 days at each facility. Investigators were required to scrutinise the RtHB of every child included in the study and attended consultations between HCWs, children and their CGs. Investigators used a checklist to document their observations which assessed the implementation of each component of the RtHB. In addition, clinical notes and referrals made by HCWs, as well as communication of return visits with CGs, were recorded. Missed opportunities – defined for the purposes of this survey as ‘the failure to provide appropriate monitoring, treatment, or intervention on the day of data collection’ – were also noted.

Anthropometric measurements performed by HCWs were observed and evaluated according to the guidelines described in the WC RtHB training package.[7] Based on guidelines described in the training package,[7] the checklist included a step-by-step description of all relevant anthropometric measuring and plotting procedures, including weightfor-age, length/height-for-age, and weight-for-length/height growth charts. The checklist also collected information on how each section of the RtHB had been completed by HCWs. An additional checklist was used to evaluate the accuracy and availability of anthropometrical apparatuses at each facility. Length boards were calibrated against a known 1 m non-flexible length and paediatric scales against known 2 kg, 5 kg, and 10 kg weights. Inaccurate equipment was corrected at each facility, where possible, once data collection was completed.

Questionnaires were used to document CGs’ and HCWs’ sociodemographic information, knowledge, attitudes, and practices (KAPs) relating to each component of the RtHB, as well as perceived barriers to the successful implementation of the tool. Self-administered questionnaires were completed by HCWs, whereas CG questionnaires were completed by investigators during a structured interview. All questionnaires were available in English, Afrikaans, and isiXhosa and were completed with the assistance of a translator where necessary.

All investigators underwent training and standardisation, followed by a pilot study. Data from the pilot study were not included in the final analysis. Questionnaires and checklists were tested for face validity during the pilot study and for content validity by 8 experts in the field of dietetics and nutrition.

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Anthropometric measurements were analysed using the WHO Anthro programme. Underweight, stunting and wasting were expressed as the proportion of individuals with Z-scores below –2 SD.[8,9] Overweight and obesity were expressed as the proportion of individuals with weight-for-length/height Z-scores above 2 SD and 3 SD, respectively.[8,9] In children who were ≥6 months old, a mid-upper arm circumference (MUAC) value of ≥11.5 cm and <12.5 cm was regarded as moderate acute malnutrition, while a MUAC value of <11.5 cm was classified as severe acute malnutrition.[10] Data were captured and analysed using Microsoft Office Excel and STATISTICA version 12 (StatSoft Inc., USA). Data are expressed using descriptive statistics. Contingency tables were used when comparing two nominal variables and independence was tested using the maximumlikelihood (M-L) χ2 test. Comparisons of data against reference values were done using 1-sample signed-rank non-parametric tests. A p-value of <0.05 was considered statistically significant. In cases where the data do not reflect the total study population, the relevant numbers are indicated in brackets.

Results

Demographic information

A total of 2 442 children, 2 481 CGs, and 270 HCWs participated in this survey (Fig. 1). The mean (standard deviation (SD)) age of children included in the study was 5.10 (6.24) months (range 6 weeks - 34.15 months), with nearly equal numbers of boys and girls (50.3%, n= 1 229 v. 49.7%, n= 1 213, respectively). Data collected from CGs indicated a mean (SD) age of 28.4 (8.2) years (range 13.8 - 73.0 years). Most CGs (92%; n=2 282/2 481) were the mother of the child and the primary CGs of one (42.5%; n=1 050/2 471) or two (31.8%; n=787/2 471) children.

Eleven percent of CGs (n=281/2 481) had received no schooling or had not completed primary school; only 24.3% (n=604/2 481) had completed grade 12 (secondary school). Fourteen percent (n=365/2 481) of CGs had received further tertiary education.

Of the 270 recruited HCWs, 14.1% (n=38/269) were chief professional nurses, 42% (n=113/269) were professional nurses, and 16.2% (n=44/269) enrolled nurses. Most were female (97%, n=262/270), had achieved a tertiary qualification (69.3%; n=187/270) and had a median period of 5.0 years (range 0.5 - 37.0 years) of experience working in PHC.

Growth monitoring and promotion

Growth monitoring on the day of survey

With the exception of weight, anthropometric measurements were not performed routinely for the majority of children aged 0 - 36 months, indicating poor implementation of this section of the RtHB. Fig. 2 shows

Infants aged 0 - 36 months screened at 143 PHC facilities (N=2 814)

Eligible for inclusion (N= 2 543)

Excluded owing to: • Language barrier (n=11) • Not resident in WC during previous 6 months (n=32) • Not accompanied by primary CG (n=81) • Not correct age group (n=24) • In posession of old RtHC (n=54) • Did not bring RtHB to facility (n=69)

Excluded owing to: • Refusal to participate (n=53) • Failure to collect data on infant (n=48) Infants (N=2 442) and CGs (N=2 484) included in analyses

Fig. 1. Screening and selection of children and CGs for inclusion in the survey.

(PHC = primary healthcare; CGs = caregivers; WC = Western Cape Province; RtHC = Road-to-Health chart; RtHB = Road-to-Health booklet.)

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RESEARCH

Head circumference

14

Length/height

Anthropometry performed, %

16.4

MUAC

Anthropometry not performed, %

19.7

Weight

94.7

0%

50%

100%

Fig. 2. Missed and used opportunities for growth monitoring of children aged 0 - 36 months (n=2 251) on the day of survey. (MUAC = mid-upper arm circumference.)

the concerning number of missed opportunities for appropriate growth monitoring on the day of survey.

Correct procedures, as described in WC provincial government guidelines, were followed for weight measurements in 68.1% (n=1 534/2 251) of cases, followed by head circumference (56%; n=186/332), length/height (18.3%; n=71/338), and MUAC (10.2%; n=31/304).

In cases where the relevant anthropometry was performed, weightfor-age and length/height-for-age values were plotted on the RtHB growth charts in 90.3% (n=1 186/1 314) and 62.9% (n=178/283) of cases, respectively. However, plotting of weight-for-length/height was omitted in more than half (54.4%, n=149/274) of the observed cases. When measurements were plotted, most (>90%) were done correctly.

Prevalence of malnutrition

A total of 262 children (12%) were classified as underweight, which was most prevalent among children aged 0 - 6 months (13%, n=181/1 323).

Owing to poor practices for length/height measurements, it was decided to omit results for stunting, wasting, overweight and obesity.

Table 1 shows the prevalence of acute malnutrition based on MUAC values for each of the age groups. It is clear that the younger children experienced the highest prevalence of malnutrition.

Anthropometric equipment available at PHC facilities

Forty-one PHC facilities (28.7%; n=41/143) did not have an infant length board available on site and in at least two facilities, length boards were being kept in storage. Fourteen facilities (9.8%; n=14/143) did not routinely measure standing height and measuring tapes were utilised in eleven facilities to measure length.

Facility equipment was found to be inaccurate with significant differences shown between standard 5 kg (p=0.000) and 10 kg (p=0.014) weights, as well as the mean value of the measurements displayed on facility scales. For the 2 kg weight, differences were not statistically significant (p=0.050).

HCW and CG knowledge, attitude, and practices regarding growth monitoring and promotion

Of those who completed this section, most HCWs were able to identify the correct frequency with which to perform various anthropometric

measurements: weight measurements (81.3%; n=100/123), length/height (66.7%; n=82/123), MUAC (58.5%; n=72/123), and head circumference (28.8%; n=36/125) (Figure 3). Although the majority of HCWs could correctly identify the criteria for underweight (68.4%; n=178/260), far fewer could do so for stunting (54.6%; n=134/245) and wasting (38.7%; n=95/245).

HCWs’ ability to classify MUAC measurements was limited. Only half (50.2%; n=63/125) were able to correctly interpret a MUAC of <11.5 cm in children 6 months or older as severe acute malnutrition. Most HCWs (82.2%; n=212/258) were however able to identify the correct technique used to measure MUAC, and were aware of the correct rounding off procedures for length/height measurements (72.8%; n=91/125).

The majority of CGs ‘strongly agreed’ (79.2%; n=1 963/2 478) or ‘agreed’ (20.1%; n=499/2 478) that it was important for children to be weighed regularly. However, less than half of CGs reported that their child’s growth was explained to them on the day of the survey (40.2%; n=530/1 320).

Immunisation

This section of the RtHB was deemed complete if a child had received all scheduled, age-appropriate immunizations and if all required documentation including date, batch number, and the HCW signature had been recorded in the booklet. The immunisation section of the RtHB was shown to be well implemented, with the records of 89.3% (n=2 171/2 431) of children up to date and fully completed. At the time of data collection, immunisations were due for 1 127 children, of which 92.5% (n=1 027/1 105) were administered. This indicates that few opportunities for immunisation were missed on the day of survey (7%; n=78/1 105).

HCWs were asked about their opinion on the changed immunisation schedule indicated in the RtHB by selecting one or more phrases which best represented their points of view. Only 39% (n=106) of HCWs chose to answer this question, of whom 79.8% indicated that ‘It improves the overall health of children’. Although in the minority, responses such as ‘a missed opportunity has no effect’ and ‘it is not culturally acceptable to all’ are concerning and require further investigation.

Vitamin A supplementation

The vitamin A supplementation section of the RtHB was fully completed (date and signature indicated) for 94.6% (n=1 305/1 379) of children aged ≥6 months. On the day of survey, vitamin A supplementation was due for 346 children and was administered to 91.2% (n=301/330) of those.

Nearly all (98.8%) of the HCWs were able to identify the correct frequency with which to administer vitamin A supplementation. Ageappropriate dosages of vitamin A were also known by the majority of HCWs – more than 93% (n=209/223) answered correctly for all age categories. For both frequency (p=0.625) and dosages (p=0.439), no significant difference was found between those who had received formal training on the RtHB and those who had not.

In contrast to the encouraging level of HCW knowledge, only a small number of CGs (16.4%; 409/1 646) knew that a young child should receive vitamin A supplements every 6 months. However, significantly more CGs who reported to know the purpose of the RtHB (71.6%; n=293/409) knew the correct frequency with which vitamin A should

Table 1. Prevalence of acute malnutrition of children aged 0 - 36 months based on mid-upper arm circumference (N=291) Age (months) Acute malnutrition

0 - 12, n/N (%)

13 - 24, n/N (%)

25 - 36, n/N (%)

0 - 36, n/N (%)

Moderate

12/218 (5.5)

1/67 (1.5)

0

13/291 (4.4)

Severe

8/218 (3.7)

2/67 (2)

0

10/291 (3.4)

Total

20/218 (9.2)

3/67 (4.5)

0

23/291 (7.9)

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Correct answers, %

80

Table 2. Potential barriers identified during the period of data collection

81.3 66.7

70

58.5

60

50 40

Area

Barriers identified

RtHB

Poor flow of booklet

20

Confusion surrounding correct use of the clinical notes section

10

Duplication of information

28.8

30

0

Weight

Length/height

MUAC

Insufficient writing space

Head circumference

Fig. 3. Healthcare workers’ knowledge on the appropriate frequency of taking anthropometric measurements. (MUAC = mid-upper arm circumference.)

Booklet only available in English HCWs

Staff shortages

be administered (p<0.01, χ2(1)=20) compared with 60% (n=1 244/2 072) who indicated that they knew the purpose of the RtHB but did not know the correct vitamin A frequency.

Deworming

Almost all HCWs (97.3%; n=262/269) knew the correct frequency with which to administer deworming treatment and no significant difference was found between those who had received formal training on the RtHB and those who had not. About two-thirds (67.6%, n=135/200) of children due for deworming on the day of survey received treatment. However, further examination of RtHBs revealed that for children aged >12 months, for whom data were available, this section was fully completed (dose, date and signature indicated) in only 48.8% (n=176/361) of all cases.

Only one in four CGs (26.2%; n=650/2 481) were aware that a child older than 1 year should receive deworming treatment every 6 months.

However, significantly more CGs who reported to know the purpose of the RtHB (73.3%) knew the correct frequency of deworming treatment compared with those who did not know the purpose of the RtHB (57.9%) (p<0.01, χ2(1)=50.2).

HCW and CG knowledge, attitudes, and perceived barriers pertaining to the RtHB

Three-quarters (75.2%; n=203/270) of the HCWs had received training on the implementation of the RtHB. Training consisted mainly of lectures of up to 2 hours long (32.8%; n=41/125), full-day workshops (23.2%; 29/125), and half-day workshops (14.5%; n=18/125). More than twothirds (66.3%; n=176/265) of HCWs reported that the implementation of the RtHB had ‘increased/significantly increased’ their workload.

However, two-thirds of HCWs (61%; n=164/269) indicated that they had sufficient time to complete the RtHB as part of their daily routine.

In addition to staff shortages and high patient numbers, insufficient stock supply was mentioned by some HCWs as a factor that hampered the effective implementation of the RtHB. Delayed delivery and no stock at the distributors or depots were mentioned as the main reasons for stock shortages. However, when asked the question ‘Are there adequate stock levels of the following products available at your PHC clinic?’ most HCWs indicated the ‘always’ response.

Two-thirds (61.9%; n=1 535/2 479) of the CGs indicated that they knew the purpose of the RtHB. Although 32% (n=796/2 479) of CGs indicated that all the information in the RtHB had been explained to them, 30.9% (n=767/2 479) indicated that no information had been explained to them. When asked whether they understood the content of the RtHB, 31.4% (n=774/2 464) CGs reported that they understood ‘everything’ and 23.4% (n=576/2 464) understood ‘none’.

Table 2 provides potential barriers to successful RtHB implementation, as observed by investigators and perceived by CGs and HCWs during the course of the survey. These potential barriers, in summary, related to: logistical problems experienced by HCW with reference to the RtHB and clinic demographics, staff management issues affecting HCWs, as well as knowledge and understanding of the RtHB by CGs.

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Lack of training opportunities Insufficient time to complete tasks Poor clarification of roles and ownership of tasks

CGs

Language barriers Lack of knowledge regarding RtHB Failure to present RtHB

Clinics

Poor patient flow with no logical order of events High patient numbers Stock control

RtHB = Road-to-Health booklet; HCWs = healthcare workers; CGs = caregivers.

Discussion

Since its adoption in 2011, the RtHB has replaced the RtHC in the majority of cases in all districts of the WC. While certain sections of the booklet were utilised and documented well, data from this survey suggest that the implementation of most components of the RtHB require strengthening. Owing to the observational nature of the survey, the following commentary is confined to what was observed on the day of data collection and from a retrospective review of RtHBs.

Growth monitoring and promotion

Early identification and appropriate classification of malnutrition is pivotal to appropriate and timely intervention, especially in children <5 years of age. Regular weighing, with correct plotting of the weight and height and interpretation of the growth curve on the RtHB, form the core of the GMP strategy.[4] With the exception of weight, anthropometric measurements (head circumference, height/length, MUAC) were not recorded routinely for the majority of children who were >6 months of age. The possible reasons why height/length measurements were not recorded routinely may include a lack of time, insufficient human resources, and the unavailability of equipment to measure length. Furthermore, although training was provided, HCWs may still not be clear on the purpose and importance of these measurements for determining a child’s health. For many years HCWs have been using only the weight-for-age measurements according to the RtHC, and therefore may not have realised the relevance of performing a length/height measurement.

Parallel to the actions required from the HCWs, the CGs need to understand that GMP may contribute to the prevention of child malnutrition, provided good quality measurements are performed.[6,11] This current survey found that less than half of CGs had their child’s growth explained to them. Previous studies also found that mothers were not provided with feedback on the growth assessment of their children, identifying missed opportunities in healthcare education.[11-14]

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RESEARCH In SA, time constraints and short staffing limit HCWs’ ability to fully comprehend guidelines, allocate adequate time to patients and provide the necessary nutrition counselling.[15] As key role-players in monitoring the development of children, the HCWs need to be familiar with growth monitoring charts and be able to perform measurements and interpret the results accurately.

Similar to other studies which indicated poor knowledge in terms of identification of malnutrition, most HCWs in the current survey were able to identify the correct frequency with which to perform weight measurements; however, fewer were able to do so for length/ height, MUAC and head circumference. A study conducted by Cloete et al.[16] in the Metropole region, WC, SA, found that only 52% and 38% of HCWs could correctly interpret the criteria for underweight and wasting, respectively. A study conducted in Limpopo Province, SA, found that only 40.6% of nurses could correctly identify stunting, 47.9% could identify underweight and only 11.5% could identify wasting.[6] Inaccurate plotting and interpretation of measurements were also reported in other studies.[6,15,17] Another factor hampering optimal implementation of growth monitoring were the inaccuracies noted in the current survey in facilities’ growth monitoring equipment. The chance that malnutrition may be properly managed is therefore slim, as children’s measurements may be incorrectly classified – this will hinder appropriate diagnosis, referral and follow-up treatment. The lack of appropriate height/length measurement resources found in this survey needs to be addressed, as almost a third of PHC facilities did not have the equipment available, which could lead to the use of inaccurate measuring tools, such as measuring tapes. This lack of growth monitoring equipment corresponds with the results reported in a diagnostic and implementation evaluation of nutrition programmes in SA.[15] Regular motivation from district PHC managers to reinforce this practice as well as regular monitoring could contribute to improved implementation in the long term. In addition, anthropometric apparatuses must be available and accurately calibrated for effective growth monitoring to occur.

Immunisation

As immunisation is regarded as a cost-effective intervention for reducing child morbidity and mortality,[18,19] the global Expanded Programme on Immunisation (EPI), launched by the WHO in 1974,[18] was introduced in SA (EPI-SA) in 1995. The current EPI-SA schedule has adopted a primary series of 6, 10 and 14 weeks, ensuring protection at the earliest age, with boosters where applicable, and an early measles vaccine at 9 months. The EPI-SA aims to offer daily immunisation services (provided free of charge at all PHC facilities in SA) in order to improve coverage, and reduce vaccine-preventable diseases and childhood mortality.

Despite these developments, the EPI programme in SA is facing a number of challenges, including low vaccination coverage in some areas and poor knowledge of the community of the immunisation programme and purpose.[20] Barriers to the successful implementation of the programme include insufficient knowledge of the EPI programme and immunisations in general by HCWs, as well as financial constraints that affect stock levels,[13,20] and insufficient staff numbers.[13] In the current survey, a promising 9 out of 10 children aged 0 - 36 months had received age-appropriate vaccines.

Vitamin A supplementation

The National DoH recommends that all children should be screened at every visit to ensure that vitamin A supplementation is up to date.[21] The results of the current survey are promising in that the vitamin A section of the RtHB was fully completed for the majority of children aged ≥6 months. Vitamin A supplementation was administered in 91% of due cases, which corresponds with results from previous studies.[15,23] Similar findings were reported in two different studies at PHC clinics in the WC, in that about a third (25% and 34%, respectively) of children received vitamin A supplementation when it was due and recording of the supplementation in the RtHC was made in 97% and 77% of cases, respectively.[14,22]

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A study of registered professional nurses in Limpopo Province, SA, indicated that more than half of participants (52.1%) knew the correct frequency of administering vitamin A supplementation and deworming medication.[6] Although nearly all of the HCWs in the current survey were able to identify the correct frequency with which to administer vitamin A supplementation, this knowledge was not transferred as only a small number of CGs knew that a young child should receive vitamin A supplementation every 6 months. It appears that knowledge had a positive effect as significantly more CGs who reported to know the purpose of the RtHB, knew the correct frequency with which vitamin A should be administered. Literature reports that relatively few CGs knew why their children should receive vitamin A supplementation, ranging from 24% to 39%.[14,22] If mothers and CGs had a better understanding of the benefits of routine nutrition interventions, they would be more likely to seek these services. This could result in CGs insisting on better service and a reduction in the number of missed opportunities.[22] Furthermore, in SA, results from diagnostic and implementation evaluation of nutrition programmes targeting children <5 years of age found that, given the workloads at most PHC facilities, interventions that involve education or counselling are not as readily provided as interventions that are ‘commodity-based’ such as medicines, or immunisations.[15]

Deworming

Children between 1 and 5 years of age are targeted for regular deworming as they are most burdened with soil-transmitted helminth infections and bilharzia. These infections adversely affect the growth, ability to learn and intellectual development of children.[4] Results from the current survey showed that approximately two-thirds of children due for deworming on the day of the survey received treatment.

However, the completion of this section in the RtHB was poor in ~50% of the cases.

A survey that assessed people’s knowledge, as well as attitudes and practices of intermittent deworming in Nigeria, found that only 44.8% of children <5 years of age were dewormed at 3-month intervals. These findings show a need for active health promotion programmes to enhance compliance to intermittent deworming.[23] Results from the current survey showed that only a quarter of the CGs were aware that a child older than 1 year should receive deworming treatment every 6 months. A study on missed opportunities at healthcare facilities in the City of Cape Town showed failure to dispense important disease prevention drugs such as vitamin A and deworming tablets. These missed opportunities contribute to the high incidence of child mortality and morbidity.[13]

Staff knowledge

This survey demonstrated clear gaps in HCWs’ knowledge relating to various components of the RtHB. Concerns over gaps in HCWs’ knowledge were further reinforced by a recent national evaluation report on nutrition interventions for children. [15] The report identified a lack of sufficient knowledge and skills among staff responsible for rendering nutritional interventions such as growth monitoring, nutrition education and counselling. Staff shortages and insufficient nutrition training were found to contribute to ineffective implementation across all departments.[15]

Conclusion and recommendations

Various barriers can influence the implementation of nutrition interventions at the PHC level, e.g. poor staff knowledge and skills, lack of time, staff shortages, and/or frequent staff changes of trained staff owing to attrition or rotation. Our survey revealed that the growth monitoring section of the RtHB requires improvement from a knowledge and implementation perspective. The survey also revealed a lack of appropriate height/length measurement resources. Administration of immunisations and vitamin A was performed adequately; however, knowledge of CGs on the frequency of deworming and vitamin A supplementation needs attention.

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RESEARCH Regular training and refresher training needs to be presented to all HCWs, especially related to the new growth indicators in the RtHB. Emphasis should be placed on the importance of performing the height/ length, MUAC and head circumference measurements regularly and accurately. Regular reinforcing of this practice by PHC facility managers, the provision of appropriate apparatuses and resources to perform the required anthropometric measurements, regular monitoring of HCWs’ practices, as well as dedicated efforts from all HCWs to optimally implement the RtHB are deemed essential to improve the implementation of this tool. If implementation is not adequately achieved, children will not be appropriately identified, classified and treated. Furthermore, community health workers can be more actively involved to assist the HCWs to create awareness of these preventive services and the importance of the RtHB as a monitoring tool in the broader community.

To be consistent with international guidelines and national policy, sufficient focus, effort and resources should be channelled towards early identification of nutritionally at-risk children. Continuous training of HCWs, evaluation, and monitoring of each intervention will be necessary to achieve successful implementation of the RtHB and securing integrated healthcare for all infants and young children. This will require a shift away from task-oriented behaviour to preventive and promotive practices by HCWs. Acknowledgements. We would like to convey our sincere thanks to the Western Cape Department of Health, specifically the Sub-Directorate Nutrition, for granting permission to conduct the survey. In addition, we would like to convey our sincere gratitude to all the caregivers, infants and HCWs at each facility who participated in our survey. Lastly, we would like to thank all the members of the RtHB survey research group (mentioned below) as well as the administrative staff members of the Division of Human Nutrition and Prof. D Nel from the Centre for Statistical Consultation, Stellenbosch University, for his help with statistical analyses.

Author contributions. Study conception and design: RB, LD, LdP, HEK, NK, MLM, EvN, JV. Data collection: RB, LD, LdP, HEK, MLM, EvN, JV. Data analysis and interpretation: RB, LD, LdP, HEK, NK, EvN, JV. Conceptualising and writing the manuscript: RB, LD, LdP, HEK, NK, MLM, EvN, JV. Funding. RB: Stellenbosch University (Fund for Innovation in Rural Research, Harry Crossley Foundation) and Western Cape Department of Health. No funder had any role in the design, analysis or writing of this article.

Conflicts interest. None.

Road-to-Health Survey Research Group. Bam N, Blaauw R, Boshoff H, Clarke P, Coetzee C, Daniels L, de Kock I, de Vos I, de Vries K, du Buisson L, du Plessis LM, du Preez U, Ehlers A, Engelbrecht C, Evans N, Ferreira N, Findlay A, Foot J, Fordjour V, Frey C, Groenewald L, Hallinan T, Hartman D, Jackson G, J van Rensburg S, Jooste M, Kamhoot A, Kapena C, Kelly T, Kerbelker R, Koen N, Koornhof HEK, Kotlowitz J, le Grange M, le Roux M, Lee T, Liebenberg S, Louw A, Louw S, Marais ML, Maritz A, Martens A, Meyer I, Mncwabe N, Moens M, Morris N, Naude K, Nel M, Nel S, Nkomani S, Nyenes R, Olivier L, Pienaar T, Pilditch K, Potgieter S, Richardson C, Rickard L, Robinson R, Röhrs S, Samuels S-L, Simjee Z, Slazus C, Smit L, Smit Y, Stander L, Stone P, Strydom E, Strydom K, Swanich L, Swartz P, Swart D, Taverner T, Taylor A, Teuchert N, Turner L, Uys M, van de Venter A, van der Merwe L, van der Schyff S, van Niekerk E, van Rhyn N, van Wyk N, van Zyl F, Venter B, Verster B, Verster J, Visser J, Visser ME, Wasserfall L, Wakelin M, Webber S, Wicomb R, Yeh E. 1. Black RE, Victora CG, Walker SP, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013;382(9890):427-451. https: 10.1016/S0140-6736(13)60937-X 2. Webb P. Nutrition and the Post-2015 Sustainable Development Goals. A Technical Note. Geneva: WHO, 2014. United Nations System Standing Committee on Nutrition. https://www.unscn.org/files/Publications/Briefs_on_Nutrition/Final_ Nutrition%20and_the_SDGs.pdf (accessed 2 December 2016).

3. Ashworth A, Shrimpton R, Jamil K. Growth monitoring and promotion: Review of evidence of impact. Matern Child Nutr 2008;4(Suppl 1):86-117. https://doi.org/10.1111/j.1740-8709.2007.00125.x

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4. National Department of Health. Strategic Plan for Maternal, Neonatal, Child and Women’s Health (MNCWH) and Nutrition in South Africa 2012 – 2016.

Pretoria: NDoH, 2011. https://extranet.who.int/nutrition/gina/sites/default/ files/ZAF%202012%20MNCWHstratplan.pdf (accessed 6 December 2017).

5. Tarwa C, de Villiers FPR. The use of the Road to Health Card in monitoring child health. SA Fam Pract 2007;49(1):15-15d. https://doi.org/10.1080/207862 04.2007.10873497 6. Kitenge G, Govender I. Nurses’ monitoring of the Road to Health Chart at primary healthcare level in Makhado, Limpopo province. S Afr Fam Pract 2013;55(3):275-280. https://doi.org/10.1080/20786204.2013.10874350 7. Department of Health. Western Cape Road to Health Booklet Training Package CD; 2010.

8. De Onis M, Onyango A, Borghi E, Siyam A, Pinol A. WHO Child Growth Standards: Length/Height-for-Age, Weight-for-Age, Weight-for-Length, Weight-for-Height and Body Mass Index-for-Age. Methods and development.

Geneva: WHO, 2016. http://www.who.int/childgrowth/standards/Technical_ report.pdf (accessed March 2016).

9. WHO Expert Committee. Physical Status: The Use and Interpretation of Anthropometry. Geneva: WHO, 1995. http://www.who.int/childgrowth/ publications/physical_status/en/index.html (accessed March 2016).

10. United Nation System. Standing Committee on Nutrition: Task Force on Assessment, Monitoring, and Evaluation. Fact sheets on Food and Nutrition Security Indicators/Measures: Mid-Upper Arm Circumference (MUAC) http:// www.unscn.org/files/Task_Forces/Assessment_Monitoring_and_Evaluation/ MUAC.pdf (accessed March 2016).

11. Coulibaly F. Mothers perception of quality of growth monitoring and promotion programs: A qualitative study in Cote d'Ivoire. Ecol Food Nutr 2002;41(6):475-500.

12. Thandrayen K, Saloojee H. Quality of care offered to children attending primary health care clinics in Johannesburg. SA J Child Health 2010;4(3):73-77.

13. Jonker L, Stellenberg EL. Missed opportunities in child healthcare. Afr J Prim Health Care Fam Med 2014;6(1):1-7. https://doi.org/10.4102/phcfm.v6i1.537 14. Du Plessis LM, Najaar B, Koornhof HE, et al. Evaluation of the implementation of the vitamin A supplementation programme in the Boland/Overberg region of the Western Cape Province. S Afr J Clin Nutr 2007;20(4):126-132.

15. Department of Performance Monitoring and Evaluation. Evaluation of Nutrition Interventions for Children from Conception to Age 5. Department of Health, Department of Social Development & Department of Performance Monitoring and Evaluation. The Presidency, Republic of South Africa, South Africa, Pretoria. 2014. http://www.nutritionsociety.co.za/attachments/ article/76/Summary-Evaluation-of-Nutritional-Interventions-for-Childrenfrom-Conception-to-Age-5-.pdf (accessed March 2016) 16. Cloete I, Daniels L, Jordaan J, Derbyshire C, Volmink L, Schubl C. Knowledge and perceptions of nursing staff on the new Road to Health Booklet growth charts in primary healthcare clinics in the Tygerberg subdistrict of the Cape Town metropole district. S Afr J Clin Nutr 2013;26(3):141-146. https://doi.org /10.1080/16070658.2013.11734458 17. Schoeman SE, Hendricks MK, Hattingh SP, Benadé AJS, Laubscher JA, Dhansay MA. The targeting of nutritionally at-risk children attending a primary health care facility in the Western Cape Province of South Africa.

Publ Health Nutr 2006;9(8),1007-1012. https://doi.org/ 10.1017/PHN2006986 18. Machingaidze S, Wiysonge CS, Hussey GD. Strengthening the Expanded Programme on Immunization in Africa: Looking beyond 2015. PLoS Med 2013;10:e1001405 https://doi.org/10.1371/journal.pmed.1001405 19. Ndirangu J, Bärnighausen T, Tanser F, Tint K, Newell ML. Levels of childhood vaccination coverage and the impact of maternal HIV status on child vaccination status in rural KwaZulu-Natal, South Africa. Trop Med Int Health 2009;14(11):1383-1393. https://doi.org/10.1111/j.1365-3156.2009.02382.x 20. Wiysonge CS, Ngcobo NJ, Jeena PM, et al. Advances in childhood immunisation in South Africa: Where to now? Programme managers’ views and evidence from systematic reviews. BMC Public Health 2012;12(1):578. https://doi. org/10.1186/1471-2458-12-578 21. National Department of Health (NDoH). National vitamin A supplementation policy guidelines for South Africa. Pretoria: NDoH, 2012. http://www.adsa. org.za/Portals/14/Documents/DOH/Vit%20A%20policy%20guidelines%20 OF%20S%20A%20-%20recent_1.pdf (accessed March 2016).

22. Hendricks M, Beardsley J, Bourne L, Mzamo B, Golden B. Are opportunities for vitamin A supplementation being utilised at primary health-care clinics in the Western Cape Province of South Africa? Publ Health Nutr 2007;10(10):10821088. https://doi.org/10.1017/S1368980007699522 23. Stanley CN, Oreh NC, Johnson-Ajinwo RO. Knowledge, attitudes and practices of intermittent deworming in Alakahia community, Rivers State, Nigeria. Int Res J Med Sci 2013;1(7):1-7.

Accepted 12 September 2017.

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RESEARCH

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Placental malaria and neonatal anti-tetanus antibody status: Any association?

M F Bashir,1 MBBS, FWACP (Paed); H A Elechi,2 MBBS, FWACP (Paed); G M Ashir,2 MBBS, FWACP (Paed); A I Rabasa,2 MBBS, FWACP (Paed); A B Musa,3 MSc; R T Akuhwa,2 MBBS FWACP (Paed); A G Farouk,2 MBBS, FMC Paed Department of Paediatrics, Abubakar Tafawa Balewa University Teaching Hospital, Bauchi, Nigeria Department of Paediatrics, College of Medical Sciences, University of Maiduguri, Nigeria 3 Department of Medical Laboratory Science, College of Medical Sciences, University of Maiduguri, Nigeria 1 2

Corresponding author: H A Elechi (h3elechi@unimaid.edu.ng) Background. Neonatal tetanus (NT) has long remained an important cause of neonatal morbidity and mortality in the tropics, where it coexists with a high prevalence of placental malaria. The current strategy for the control of NT involves stimulating the production of a protective level of an anti-tetanus antibody in the mother, through tetanus toxoid immunisation, and transferring it through the placenta to the fetus. Placental malaria is known to alter the morphology and functions of the placenta, but the results of studies on the effect of the transfer of the anti-tetanus antibody, specifically, remain inconclusive.

Objective. To study the influence of placental malaria on the transplacental transfer of anti-tetanus antibodies among mother-infant pairs at the University of Maiduguri Teaching Hospital in north-eastern Nigeria.

Method. Maternal and cord-blood samples were collected from 162 mother-infant pairs, and analysed for anti-tetanus antibody levels using the enzyme-linked immunosorbent assay technique. Placental biopsies were also taken from each mother-infant pair, and placental malaria diagnosed histologically.

Results. A total of 71.6% (n=116) of the 162 mother-infant pairs were positive for placental malaria, out of whom 50.9% (n=59) had chronicactive, 37.9% (n=44) acute and 11.2% (n=13) past placental malaria. In addition, 25.3% (n=41) babies were classified as seronegative for tetanus antibodies, of whom 72.7% (n=32) were delivered to mothers who were positive for placental malaria. A total of 34.5% (n=56) mother-infant pairs had poor placental transfer for tetanus antibodies, as signified by a cord-maternal ratio of <1.0 antibodies; of these, 24.7% (n=40) were positive for placental malaria. There was a statistically significant association between type of placental malaria and serostatus (p=0.0009), and efficiency of placental transfer (p=0.0340). Mothers with chronic-active malaria were 7.4 times more likely to deliver a seronegative infant compared with mothers with acute malaria (p=0.0002; odds ratio (OR) 7.353; 95% confidence interval (CI) 2.327 - 23.234). Similarly, maternal-infant pairs with chronic-active malaria were 2.9 times more likely to have inefficient placental transfer (p=0.0221; OR 2.859; 95% CI 1.200 - 6.859).

Conclusion. Placental malaria has remained a very common medical condition in Maiduguri among pregnant women, and may partly account for the high level of neonatal tetanus prevalent in the area.

S Afr J Child Health 2017;11(4):180-185. DOI:10.7196/SAJCH.2017.v11i4.1327

Globally, neonatal tetanus accounts for 7% of neonatal mortality,[1] but in Nigeria, one of the 27 countries that account for 90% of the global burden of the disease, it accounts for up to 20%.

[1-4] Reports from different centres across the six geopolitical zones of Nigeria revealed very high case-fatality rates, with some approaching 100%.[5-11] Strengthening routine immunisation against tetanus for pregnant mothers using tetanus toxoid (TT) is considered the single most effective strategy, independent of other interventions, in eliminating neonatal tetanus.[12] The effectiveness of this strategy depends on the integrity of the placenta, which is the only medium of exchange between the mother and the fetus.

Placental transfer of the immunoglobulin IgG is a facilitated process that appears to be mediated by a specific fetal Fc receptor on the syncytiotrophoblastic cells.[13] Binding of IgG to this receptor leads to endocytosis, and it is subsequently actively transported across the villous stroma, basement membrane and, finally, through the endothelial cells of the fetal villi vessels.[14] The process becomes more efficient in late gestation; in one study, fetal concentrations of IgG immunoglobulin approximated the maternal levels at 38 weeks’ gestation, and continued to increase until birth, reaching more than twice the maternal levels by delivery.[15] Certain prevailing factors in the tropics, however, have been shown to interfere with the transplacental transfer of IgGs: hypergammaglobulinaemia, 180

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owing to endemic and recurrent infections in the tropics, inversely affects the transfer of specific IgG, owing to the saturation of the Fc receptor;[16] HIV infection has also been shown to impair the ability of the mother to produce and transfer adequate IgGs to her fetus.[17] Placental malaria can produce pathological changes in the placenta, such as thickening of the basement membrane, inflammatory cell infiltrates, villitis and microinfarct owing to clumping of parasitised red blood cells and the occlusion of microvasculatures.[18] These changes could lead to a reduction in blood flow to the intervillous spaces, and alteration in the structure of the placental barrier, thereby impacting negatively on the transplacental transfer of molecules.

In Nigeria, placental malaria remains highly endemic,[19,20] and has been shown to impair the transplacental transfer of maternal IgG needed to fight against common childhood infectious diseases such as tetanus,[21,22] measles[23] and the Epstein-Barr virus.[24] However, there are conflicting reports regarding the effect of placental malaria on the efficiency of the transplacental transfer of the anti-tetanus antibody, and therefore on the cord-blood concentrations. In a malarial area of Papua New Guinea,[21] the cordmaternal ratio (CMR) of the anti-tetanus antibody among pregnant women with heavy placental malarial infections was considerably lower (0.18) than that among women without such infections (0.83).

Approximately 10% of babies born to mothers whose placenta were heavily infected with Plasmodium falciparum failed to acquire

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RESEARCH protective levels of the anti-tetanus antibody, despite adequate maternal antibody concentrations.[21] Additionally, Cumberland et al.[22] reported that in Kenya, maternal and neonatal anti-tetanus antibody serum levels, as well as transplacental transfer, were reduced when women had chronic-active or past placental malaria. By contrast, studies in Malawi[25] and The Gambia[23] did not find any effect of placental malaria on anti-tetanus antibody serum levels or transplacental transfer. However, these conflicting findings could be accounted for by differences in methodology: in the Malawian study,[25] in addition to a smaller sample size, thick and thin films from placental blood smear were used, rather than placental histology, which assessed only the presence or absence of parasites, and therefore excluded past placental malaria, one of the groups with a significant effect on transplacental transfer in the Kenyan study.[22] Furthermore, those with placental malaria in both the Malawian[25] and Gambian[23] studies were not further subclassified into acute and chronic. This may be an important distinction, as demonstrated in the Kenyan study,[22] where acute placental malaria had no significant effect on transplacental transfer of the antibody, in contrast to active chronic and past placental malaria. Therefore, the cases of acute malaria in both studies[23,25] might have influenced the stated results. Similarly, neither of the two studies[23,25] subclassified those with placental malaria based on the degree of parasitisation, which was identified by Brair et al.[21] as an important factor in Papua New Guinea.

These conflicting findings, coupled with the high prevalence of neonatal tetanus and placental malaria in Nigeria, make it imperative to ascertain the effect of the latter on the former if the scourge is to be overcome. Therefore, we aim to determine the effect of placental malaria on cord serum levels of the anti-tetanus antibody, as well as its effect on the transplacental transfer of this antibody.

Methods

Study area

The study was carried out at the labour ward of the University of Maiduguri Teaching Hospital (UMTH), Maiduguri, Borno State, Nigeria. UMTH is a tertiary healthcare centre located in northeastern Nigeria, and a centre of excellence for infectious diseases research and immunology. It also serves as a referral site for the six north-eastern states and the neighbouring countries of Chad, Cameroon and Niger.

Ethical considerations

The protocol of this hospital-based cross-sectional descriptive study was reviewed and approved by the Research and Ethics Review Committee of UMTH (ref. no. ADM/TH.75/Vol.II). Signed or thumb-printed informed consent was obtained from each mother.

Confidentiality was maintained, and mothers were informed of the outcome of the investigations.

Sample size determination

The minimum sample size was determined using Cochran’s sample size formula for categorical data,[26] at an a level of 0.05 and a standard normal deviate of 1.96, corresponding to a 95% confidence interval (CI). The proportion of newborns with protective levels of tetanus IgG antibody (seropositives) was selected using the method from a previous study in Jos by Adabara et al.,[27] at 88%. The sample size for the study, therefore, was 162 mother-infant pairs.

Data collection

Mother-infant pairs were enrolled using the systematic random sampling method; the first of every three mother-infant pairs were selected at the labour ward from the first day of data collection, to ensure an even spread over the period of study. Mothers who had had stillbirths, or had a history of anti-tetanus serum (ATS) administration or blood transfusion within the preceding 4 weeks to 181

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delivery, were excluded. Also excluded were mothers with diabetes mellitus, hypertension, eclampsia or pre-eclampsia, as a result of the known effects of these conditions on placental function.[28] Upon enrolment, a questionnaire on sociodemographic variables was completed for each mother-infant pair. This included biodata, pregnancy and antenatal history and gestational age, as well as indicators of socioeconomic status such as the occupations and educational levels of both parents. A history of TT vaccination during the current pregnancy, verifiable from the patient’s antenatal clinic records, was obtained where possible, including the number of doses and their interval, as well as the number of TT doses received before the index pregnancy. Gestational age at delivery was determined by ultrasound scan, where available, or by date using the last menstrual period, and confirmed by the New Ballard score[29] of the baby after delivery. Socioeconomic status was assigned using Oyedeji’s[30] model.

Birth weight was measured using a digital weighing scale; babies weighing <2.50 kg were classified as low birth weight.[31] All weights were measured to the nearest 0.01 kg.

Sample collection and analysis

Maternal venous blood (2 mL) was collected from a peripheral vein following an aseptic procedure. Additionally, 2 mL of cord blood from the placental end of the cord, after early clamping of the cord, was also collected, and stored in properly labelled sterile plain bottles. Sera were separated after centrifuging these blood samples at 5 000 rpm for 5 minutes. Aliquots of serum samples were stored at –200C until analysis.

The serums from each mother-infant pair were matched, and assayed for tetanus IgG antibodies by the enzyme-linked immunosorbent assay (ELISA) technique (Demeditec Diagnostics, Germany). The optical density was measured at 450 nm (OD450) in an ELISA microplate reader. Standard curves were drawn for each plate, and optical densities of the test-serum dilutions falling within the linear part of the curve were extrapolated. The results were expressed as IU/mL. Antibody levels below 0.1 IU/mL were classified as seronegative, in accordance with World Health Organization (WHO) recommendations. [32] A full-thickness placental biopsy specimen was obtained from a healthy pericentric area, and fixed in 10% neutral buffered formal saline for 24 hours. It was then sent to the histopathology laboratory, where subsequent processing was carried out. Representative samples were taken from fixed placental tissue, and processed using the Shandon automatic tissue-processing machine (Shandon Southern Instruments Ltd., UK) over a period of 24 hours. The tissue was then embedded using paraffin wax, and sections were cut at 4 µm, mounted on a slide, dewaxed using a hot plate and cleaned in xylene, before hydrating in descending grades of ethanol and, finally, washed in water and stained with Giemsa stain (1:10 dilution) for 30 minutes. Finally, under a coverslip, it was examined under a ×40 lens of a 4 × 4 Olympus electric microscope (Olympus Optical Co., Ltd., Japan). The presence of malaria parasites and/or pigment was considered positive for placental malaria. Those classified as positive were further subclassified into acute placental malaria, chronic-active malaria and past malaria, based on the presence of malaria parasites alone, malaria parasites and pigment, and pigment alone, respectively.

Data analysis

Data obtained were entered into a computer that generated a computerised data base. Analysis was done using SPSS version 16.0 (SPSS Inc., USA). Tables were used for data presentation as appropriate. Geometric means and standard deviations (SDs) of antitetanus antibody titres were determined. Frequencies of anti-tetanus antibody serostatus (seropositives and seronegatives) were compared using Fisher’s exact test. A p-value of <0.05 was considered significant.

Results

A total of 162 mother-infant pairs were enrolled. The mean (SD)

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RESEARCH age of the mothers was 27.2 (6.0) years. Most (74.7%; n=121) were multipara, and belonged to the low socioeconomic class, 81.5% (n=132). A total of 85.2 (n=138) mothers had had at least two TT vaccinations during the current pregnancy, and 71.6% (n=116) of them were positive for placental malaria (Table 1). Out of those with placental malaria, 38% (n=44) had acute malaria, 59 (51%) chronic -active malaria while 11% (n=13) had past malaria.

Of the 162 babies enrolled, 51.9% (n=84) were male and 48.1% (n=78) were female, giving a male to female ratio (M:F) of 1.08:1.

A total of 92% (n=149) were term and the remaining 8% (n=13) were preterm. None of the babies was post term. Low birth weight was observed in 9 5.6% (n=9) of babies, while the remaining 94.4% (n=153) were of normal birth weight.

The mean (SD) anti-tetanus antibody titre of the mothers and their babies was 0.160 (0.122) IU/mL and 0.230 (0.170) IU/mL, respectively, giving an overall CMR of 1.437. A total of 76.5% (n=124) of mothers and 74.4% (n=121) of babies were seropositive for tetanus antibodies (titre of â&#x2030;Ľ0.1 IU/mL). There was a strong positive correlation between maternal and cord-blood levels of tetanus antibodies (r=0.668; p<0.001), with a shared variance of 44.6% (Fig. 1). There was a weak but significant negative correlation between maternal anti-tetanus antibody levels and CMRs (r=â&#x20AC;&#x201C;0.158;

p=0.045) with a shared variance of only 2% (Fig. 2).

A total of 25.3% (n=41) of babies were classified as seronegative for tetanus antibodies (titre of <0.1 IU/mL), out of whom 72.7% (n=32) were delivered to mothers who were positive for placental malaria.

Similarly, 34.5% (n=56) mother-infant pairs had poor placental transfer (CMR <1) for tetanus antibodies, out of whom 24.7% (n=40) were positive for placental malaria. However, placental malaria did not show a significant association with either the tetanus serostatus of the babies (p=0.3233) or with the efficiency of placental transfer of tetanus antibodies (p=1.000).

Of the 32 seronegative infants born to placental-malaria positive mothers, 78.1% (n=25) of the mothers had chronic-active malaria, while 12.5% (n=4) and 9.4% (n=3) had acute and past malaria, respectively. Similarly, of the 40 maternal-infant pairs with CMR <1 and placental malaria positive, 67.5% (n=20), 25.0% (n=10) and 7.5% (n=3) had chronic-active, acute and past malaria respectively. There was a statistically significant association between type of placental malaria and serostatus (p=0.0009) and with the efficiency of placental transfer (p=0.0340). Mothers with chronic-active malaria were 7.4 times more likely to deliver a seronegative infant than mothers with acute malaria (odds ratio (OR) 7.353; 95% CI 2.327 - 23.234; p=0.0002) (Table 2) Similarly, maternal-infant pairs with chronic-

Table 1. Sociodemographic and obstetric characteristics of the mothers studied (N=162) Characteristic n (%) Maternal tetanus antibody titre (IU/mL)

Age (years) 14 - 19 20 - 24 25 - 29 >30 Parity Primipara Multipara Socioeconomic status High Middle Low TT vaccination status None 1 >2 Placental malaria status Positive Negative

.800

14 (8.6) 38 (23.5) 54 (33.3) 56 (34.6) 41 (25.3) 121 (74.7) 14 (8.6) 16 (9.9) 13 (81.5) 12 (7.4) 12 (7.4) 138 (85.2)

R2=0.446 .600

.400

.200

.000 .000

116 (71.6) 46 (28.4)

.100

.200

.300

.400

.500

.600

Cord-blood tetanus antibody titre (IU/mL)

TT = tetanus toxoid.

Fig. 1. Pearson correlation between maternal and cord-blood tetanus antibody titres.

Table 2. The effect of various types of placental malaria on newborn anti-tetanus antibody status Placental malaria type

Anti-tetanus antibody status Seronegative (<0.1), n Seropositive (>0.1), n

Chronic-active Acute Past Chronic-active Past Acute

25 4 3 25 3 4

34 40 10 34 10 40

OR

95% CI

p-value*

7.353

2.327 - 23.23

0.0002

0.4050

0.1016 - 1.638

0.2282

3.000

0.5762 - 15.62

0.3325

OR = odds ratio; CI = confidence interval. *Fisherâ&#x20AC;&#x2122;s exact test.

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RESEARCH active malaria were 2.9 times more likely to have inefficient placental transfer (OR 2.859; 95% CI 1.200 - 6.859; p=0.0221) than those with acute malaria (Table 3).

Among the remaining maternal and infant factors studied, only gestational age at birth showed a statistically significant association

.800

with cord-blood serostatus (p=0.004) as well as CMR (p=0.002). The preterms were 5.624 times more likely to be seronegative (OR 5.624; CI 1.961 - 28.41) and 7.464 times more likely to have inefficient transfer of anti-tetanus antibody (OR 7.464; CI 1.724 - 18.35) compared to term neonates.

Logistic regression analysis showed that only an infantâ&#x20AC;&#x2122;s gestational age could significantly predict the anti-tetanus antibody serostatus, even after controlling for all other factors in the model (Table 4).

Maternal tetanus antibody titre (IU/mL)

Discussion R2=0.025

.600

.400

.200

.000 .000

2.00

4.00

6.00

Cord-maternal ratio

Fig. 2. Pearson correlation between maternal anti-tetanus antibody titres and cord-maternal ratios (CMR).

The 71.6% prevalence of placental malaria among the mothers in this study was more than twice that reported by Bako et al.[19] (33.9%) from the same centre. It is also higher than the 57.6% reported by Ibhanesebhor and Okolo[20] in Benin, Nigeria, as well as the 51.1% reported in The Gambia by Okoko et al.[23] However, this higher prevalence observed in this study when compared with these earlier studies may be accounted for by the difference in the criteria used for the diagnosis of placental malaria. While the other studies used only the presence of the malaria parasite as the diagnostic criterion, this study used the malaria parasite and/or malaria pigment, so that past or chronic malaria, which are more likely to be associated with structural and functional changes in placenta than acute malaria, could also be diagnosed.[33] Similarly to earlier studies,[22,27,34] in both mothers and babies, the overall geometric mean titres of anti-tetanus antibodies were within the protective range (>0.1 IU/mL), with a correspondingly high proportion of anti-tetanus antibody seropositivity. Cumberland et al.[22] in 2007 reporting from Kenya found the geometric mean titres of anti-tetanus antibody of both the mothers and their babies to be within the protective range. Similarly, Hood et al.[34] found the geometric mean concentration of anti-tetanus antibodies in Nigerian

Table 3. The effect of various types of placental malaria on efficiency of transplacental transfer (cord-maternal ratio) of antitetanus antibody Efficiency of transplacental transfer Inefficient transfer Efficient transfer Placental malaria type OR 95% CI p-value (<1), n (>1), n Chronic-active Acute Past Chronic-active Past Acute

27 10 3 27 3 10

32 34 10 32 10 34

2.859

1.200 - 6.859

0.0221

0.3556

0.0886 - 1.425

0.2139

1.020

0.2344 - 4.4439

1.000

OR = odds ratio; CI = confidence interval. *Fisherâ&#x20AC;&#x2122;s exact test.

Table 4. Logistic regression analysis results exploring the predictive significance of some maternal and infant factors on cord-blood anti-tetanus antibody serostatus Wald Independent variables Df p-value test Maternal age SES Parity TT vaccination status Placental malaria Birth weight Gestational age Gender Constant

2.050 3.052 0.386 0.141 1.312 0.063 7.859 0.545 0.165

3 2 1 2 1 1 1 1 1

0.562 0.217 0.534 0.932 0.252 0.802 0.005 0.460 0.685

SES = socioeconomic status; Df=degrees of freedom; p significant at <0.05.

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mothers and their infants to be within the protective range. The proportion of seropositive mothers and babies were similarly very high in these studies by Hood et al.,[34] Adabara et al.[27] (both from Nigeria) and Cumberland et al.[22] from Kenya. However, the findings from this study and the earlier ones[22,27,34] may not be a true reflection of the anti-tetanus antibody serostatus in the general population, because women who deliver in hospital are more likely to have received the TT vaccination than women who deliver at home.[35] This is further supported by the higher incidence of neonatal tetanus among homedelivered infants,[36] indicating a lower or non-protective anti-tetanus antibody level. It is known that in Nigeria and other developing countries, the proportion of pregnant women not enrolling for antenatal care has continued to remain high, with an attendant high proportion of home deliveries.[37] The mean CMR found in this study was higher than that in most previous studies, such as in Ibadan, Nigeria,[34] Kenya,[22] Libreville, Gabon,[38] Thailand[39] and India.[40] While it was found to be >1.0 in

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RESEARCH this study, signifying efficient placental transfer, the others reported <1.0, pointing to the earlier held view of poor placental transfer of tetanus antibodies in African mothers. However, a further limitation, apart from the small sample size in the Ibadan study, lay in the fact that most of the studies used an in vitro technique to determine antitetanus antibody levels that measures both IgG and IgM antibodies, resulting in misleadingly high maternal titres, and therefore low CMRs, compared with the standard ELISA (in vivo) used in this study, which measures only IgG. A highly significant positive correlation was observed between the maternal and baby tetanus antibody levels, affirming the direct relationship between the two, with the later dependent on the former.

A similar significant positive correlation was reported by Adabara et al.[27] in Nigeria. However, in our study, a significant but weak negative correlation was found to exist between maternal tetanus antibody levels and CMR, with only about 2% of its variance being attributable to changes in maternal tetanus antibody levels. The reason for the decreasing efficiency of the transplacental transfer of anti-tetanus antibody with increasing maternal levels of the antibody is not clear. It may be that mothers with high tetanus antibody levels might generally be hypergammaglobinaemic. It is known that this condition is associated with reduced placental transfer of tetanus antibodies, as previously reported.[23,41,42] High maternal IgG has been found to be common in Africa.[23,42] This is owing to the fact that the IgG binding site on the FcRn receptor can become saturated. Therefore, the amount of IgG transmitted depends on the number of cell surface receptors, because unbound IgG molecules are digested by lysosomal enzymes inside the vesicles.[43] Michaux et al.[38] reported that total IgG concentrations in cord sera tend to be lower than in the mothers when total IgG levels in maternal serum reached 15 g/L. Similarly to the observations in Malawi by de Moreas-Pinto et al.[25] and Okoko et al.[23] in The Gambia, this study found no significant association between placental malaria and materno-fetal transfer of tetanus antibodies, or cord-blood tetanus antibody levels. However, this finding seems to be the result of the cofounding effects of the various types of placental malaria on one another. This is evident from the significant association, demonstrated in this study, between the types of placental malaria and cord-blood levels (serostatus) of the tetanus antibody, as well as the efficiency of tetanus antibody transfer. As Cumberland et al.[22] also found, chronic-active placental malaria was significantly associated with reduced transplacental transfer and cord-blood levels of tetanus antibody in this study. The reason for the difference between chronic-active malaria and the other types of placental malaria in this study is not clear, but may be the result of differences in the extent and type of changes to the placental membrane. However, in contrast to this study, Cumberland et al.22 also demonstrated that past placental malaria was significantly associated with reduced cord-blood levels, and poor tetanus antibody transfer. The reason for this contrasting finding remains unclear, but this study might not have demonstrated the effect of past placental malaria owing to the small number of mothers involved who had past placental malaria. It could also be that active inflammation and past damage to the placenta act synergistically to cause the observed effect of chronic-active malaria, but neither individually would have had a significant effect on cord-blood levels and the efficiency of tetanus antibody transfer, as in this study.

Conclusion and recommendations

Placental malaria remains a very common medical condition in Maiduguri among pregnant women, and may partly account for the high level of neonatal tetanus prevalent in the area. Prompt treatment of cases of malaria in pregnancy, as well as scaling up of the strategy of intermittent preventive treatment of malaria in pregnancy might go a long way towards reducing the scourge of neonatal tetanus.

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Acknowledgements. We wish to acknowledge Prof. A Mayun and Dr A Bukar, both of the Department of Histopathology, as well Mr D Bukbuk and Mr S Joshua of the Immunology Department, UMTH, for their expert contribution in viewing the slides and running the ELISA. Author contributions. MFB conceived the idea, prepared a proposal for the research and collected and analysed the data. HAE participated in data analysis, and prepared the manuscript for publication. GMA corrected the proposal and manuscript. AIR supervised and made corrections in all stages of the study. ABM preserved and processed the placental tissue for viewing while RTA corrected the proposal for the study. AGF read through and corrected the proposal and manuscript.

Funding. None.

Conflicts of interest. None.

1. Lawan JE, Cousens S, Zupan J. 4 million neonatal deaths: When? Where? Why? Lancet 2005;365(9462):891-900. https://doi.org/10.1016/s0140-6736(05)71048-5 2. United Nations International Children’s Emergency Fund, World Health Organization, United Nations Population Fund. Maternal and Neonatal Tetanus Elimination by 2005: Strategies for Achieving and Maintaining Elimination.

New York: UNICEF, 2000.

3. Babaniyi O, Parakoyi B. Cluster survey for poliomyelitis and neonatal tetanus in Ilorin, Nigeria. Int J Epidemiol 1991;20(2):515-520. https://doi.org/10.1093/ ije/20.2.515 4. Eregie CO. Uvulectomy as an epidemiological factor in neonatal tetanus mortality: Observation from a cluster survey. West Afr J Med 1994;13(1):56-8.

5. World Health Organization. Incidence of neonatal tetanus in Kano State, Nigeria, 2006. Wkly Epidemiol Rec 2006;81(46):433-440.

6. Eregie CO, Ofovwe G. Cluster survey on neonatal mortality in Nigeria: Observation of some clinical aspects. J Trop Pediatr 1993;39(6):372-373.

7. Omoigberale AI, Abiodun PO. Upsurge in neonatal tetanus in Benin City, Nigeria. East Afr Med J 2005;82(2):98-102.

8. Oruamabo RS, Igbagiri FP. Neonatal tetanus in Port Harcourt. Afr J Med Med Sci 1996;25(3):265-268.

9. Asekun-Olarinmoye EO, Lawoyin TO, Onadeko MO. Risk factors associated with neonatal tetanus in Ibadan, Nigeria – a revisit. Afr J Med Med Sci 2003;32(3):275-278.

10. Owa JA, Makinde OO. Neonatal tetanus in babies of women immunized with TT during pregnancy. Trop Doct 1990;20(4):156-157.

11. Osuhor PC. Neonatal tetanus in Zaria, northern Nigeria. Indian J Public Health 1983;27(1):32-37.

12. Gupta SD, Keyl PM. Effectiveness of prenatal TT immunization against neonatal tetanus in a rural area in India. Pediatr Infect Dis J 1998;17(4):316-321.

13. Chucri TM, Monteiro JM, Lima AR, Salvadori MLB, Kfoury JR, Miglino MA. A review of immune transfer by the placenta. J Reprod Immunol 2010;87(12):14-20. https://doi.org/10.1016/j.jri.2010.08.062 14. Blackburn ST. The prenatal period and placental physiology. In: Blackburn S. Maternal, Fetal & Neonatal Physiology: A Clinical Perspective (4th ed.).

Washington: Elselvier, 2013:61-114.

15. Pitcher-Willnot RW, Hindocha P, Wood CBS. The placental transfer of IgG subclasses in human pregnancy. Clin Exp Immunol 1980;41(2):303-308.

16. Gendel D, Richard-Lenoble D, Massamba MB, Picaud A, Francual C, Blot P. Placental transfer of tetanus antibodies and protection of the newborn. J Trop Pediatr 1990;36(6):279-282. https://doi.org/10.1093/tropej/36.6.279 17. Bashir MF, Elechi HA, Ashir MG, et al. Neonatal tetanus immunity in Nigeria: The effect of HIV infection on serum levels and transplacental transfer of antibodies. J Trop Med 2016. https://doi.org/10.1155/2016/7439605 18. Galbraight RM, Fox H, His B, Galbraight GMP, Bray RS, Faulk WP. The materno-fetal relationship in malaria: histological, ultrastructural and immunopathological studies of the placenta. Trans R Soc Trop Med Hyg 1980;74(1):61-72. https://doi.org/10.1016/0035-9203(80)90012-7 19. Bako BG, Audu BM, Geidam AD, Kullima AA, Ashiru GM, Malah GM et al. Prevalence, risk factors and effects of placental malaria in the UMTH, Maiduguri, North-eastern Nigeria: A cross-sectional study. J Obstet Gynaecol 2009;29:(4):307-310. https://doi.org/10.1080/01443610902878783 20. Ibhanesebhor SE, Okolo AA. Placental malaria and pregnancy outcome.

Int J Gynaecol Obstet 1992;37(4):247-252. https://doi.org/10.101600207292(92)90324-C 21. Brair ME, Brabin BJ, Milligan P, Maxwell S, Hart CA. Reduced transfer of tetanus antibodies with placental malaria. Lancet 1994;343(8891):208-209. https://doi.org/10.1016/S0140-6736(94)90991-1 22. Cumberland P, Shulman CE, Maple PAC, et al. Maternal HIV infection and placental malaria reduce transplacental antibody transfer and tetanus antibody levels in newborns in Kenya. J Infect Dis 2007;196(4):550-557. https://doi. org/10.1086/519845 23. Okoko BJ, Wesumperuma LH, Ota MO, et al. Influence of placental malaria infection and maternal hypergammaglobulinaemia on materno-fetal transfer of measles and tetanus antibodies in a rural west African population. J Health Popul Nutr 2001;19(2):59-65. https://doi. org/10.1086/322808

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RESEARCH 24. Ogalla S, Daud II, Asito AS, et al. Reduced transplacental transfer of a subset of Epstein-Barr virus-specific antibodies to neonates of mothers infected with Plasmodium falciparum malaria during pregnancy. Clin Vaccine Immunol 2015;22(11):1197-1205. https://doi.org/10.1128/cvi.00270-15 25. De Moraes-Pinto MI, Verhoeff F, Chimsuku L, et al. Placental antibody transfer: Influence of maternal HIV infection and placental malaria. Arch Dis Child Fetal Neonatal Ed 1998;79(3):202-205.

26. Cochran WG. Sampling Techniques (3rd ed.). New York: John Wiley & Sons, 1977.

27. Adabara NU, Kandakai-Olukemi YT, Enenebeaku MN, Daru PH. Assessment of materno-fetal transfer of antitetanus immunoglobulin G in Jos University Teaching Hospital, Jos. Shiraz E-Med J 2010;11(2):1-8.

28. Vambergue A, Fajardy I. Consequences of gestational and pregestational diabetes on placental function and birth weight. World J Diabetes 2011;2(11):196-203.

29. Ballard JL, Khoury JC, Wedig K, et al. New Ballard Score, expanded to include extremely premature infants. J Pediatr 1991;119(3):417-423. https://doi. org/10.1016/S0022-3476(05)82056-6 30. Oyedeji GA. Socioeconomic and cultural background of hospitalised children in Ilesha. Nig J Paediatr 1985;12(4):111-117.

31. Stoll BJ, Adams-Chapman I. The high-risk infant. In: Kliegman RM, Behrman RE, Jenson HB, Stanton BF, eds. Nelson Textbook of Pediatrics (18th ed.).

Philadelphia: Saunders, 2007:97.

32. World Health Organization. Tetanus Vaccine: WHO Position Paper. Wkly Epidemiol Rec 2006;81(20):198-208.

33. Brabin BJ, Romagosa C, Abdelgalil S, et al. The sick placenta â&#x20AC;&#x201C; the role of malaria.

Placenta 2004;25(5):359-378. https://doi.org/10.1016/j.placenta.2003.10.019 34. Hood N, Chan MC, Maxwell SM, Familusi JB, Hart CA. Placental transfer of tetanus toxoid antibodies in Nigerian mothers. Ann Trop Paediatr 1994;14(3):179-182. https://doi.org/10.1080/02724936.1994.11747714

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35. Cutts FT, Rodrigues LC, Colombo S, Bennett S. Evaluation of factors influencing vaccine uptake in Mozambique. Int J Epidemiol 1989;18(2):427-433. https:// doi.org/10.1093/ije/18.2.427 36. Alhaji MA, Bello MA, Elechi HA, Akuhwa RT, Bukar FL, Ibrahim HA. A review of neonatal tetanus in University of Maiduguri Teaching Hospital, North-eastern Nigeria. Niger Med J 2013;54(6):398-401. https://doi.org/ 10.4103/0300-1652.126294 37. United Nations International Childrenâ&#x20AC;&#x2122;s Emergency Fund. Statistics. In: At a Glance: Nigeria. New York: UNICEF, 2013. http://www.unicef.org/ infobycountry/nigeria_statistics.html (accessed 10 December 2015).

38. Michaux JL, Heremans JF, Hitzig WH. Immunoglobulin levels in cord-blood serum of negroes and caucasians. Trop Geogr Med 1966;18(1):10-14.

39. Sangpetchsong V, Vichaikummart S, Vichitnant A, Podhipak A. Transfer rate of transplacental immunity to tetanus from nonimmunized and immunized mothers. Southeast Asian J Trop Med Public Health 1984;15(3):275-280.

40. Maselle SY. Maternal and fetal tetanus toxoid antibody levels following immunization in pregnancy. J Obstet Gynaecol East Cent Africa 1989;8(1):11-14.

41. Gendrel D, Richard-Lenoble D, Massamba MB, Picaud A, Francoual C, Blot P. Placental transfer of tetanus antibodies and protection of the newborn. J Trop Pediatr 1990;36(6): 279-282. https://doi.org/10.1093/tropej/36.6.279 42. Hartter HK, Oyedele OI, Dietz K, Kreis S, Hoffman JP, Muller CP. Placental transfer and decay of maternally acquired antimeasles antibodies in Nigerian children. Pediatr Infect Dis J 2000;19(7):635-641.

43. Saji F, Koyama M, Matsuzaki N. Human placental Fc receptors. Placenta 1994;15(5):453-466. https://doi.org/10.1016/S0143-4004(05)80415-1

Accepted 12 September 2017.

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This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Predictors of obesity and cardiometabolic disease risk in South African children V K Moselakgomo, PhD; M Van Staden, PhD Department of Physiology and Environmental Health, School of Molecular and Life Sciences, University of Limpopo, Sovenga, South Africa Corresponding author: V K Moselakgomo (violetmoselakgomo@yahoo.com) Background. Obesity is a major public health problem in developed countries, and is also a growing concern in developing nations. This study assessed the predictors of overweight and obesity in South African (SA) children and adolescents, and examined the extent to which these dependent measures correlate with cardiometabolic disease (CMD) risk.

Objectives. To assess the predictors of overweight and obesity in SA children and adolescents.

Methods. A total of 1 361 (boys, n=678; girls, n=683) children aged 9 - 11 (boys, n=455; girls, n=411) and adolescents aged â&#x2030;Ľ12 - 13 (boys, n=288; girls n= 267) participated in the study. The childrenâ&#x20AC;&#x2122;s anthropometric and physiological measurements were taken. Body mass index (BMI) was calculated and used to classify the children as underweight, of normal weight overweight or obese, as well as to screen them for CMD risk.

Results. Findings indicated that 81.2%, 17.4%, 0.9 and 0.5% of the children (<12 years old) were underweight, of normal weight, overweight, and obese, respectively. For adolescents (12 - 13 years old), 63.0%, 32.5%, 3.4% and 1.0% were underweight, of normal weight, overweight and obese, respectively. Provincial analysis of the results showed that the likelihood of a girl in Mpumalanga Province becoming overweight or obese was 0.33 times that of a female child in Limpopo Province.

Conclusion. Periodic assessment of predictors of obesity and CMD disease risk in SA children is necessary. Intervention and prevention strategies are also needed to curb the rising tendency of CMD risk among the youths.

S Afr J Child Health 2017;11(4):186-191. DOI:10.7196/SAJCH.2017.v11i4.1331

Obesity is a major public health problem in developed countries and is fast becoming a growing threat to human health in developing nations.[1] In recent years, it has been established that several chronic diseases of lifestyle (CDLs) typically reported for adults in Western countries, such as diabetes, cardiovascular diseases (CVD) and hypertension, can also be observed in children and are frequently associated with body weight disorders such as underweight, overweight and obesity.[2] The current US statistics published by the National Health and Nutrition Examination Survey (NHANES) reported 21.5% overweight and 10.4% obesity among 2 - 5-year-olds.

[2] In addition, increases in this condition were reported in the same age group in Europe[3] and Australia.[4] However, obesity is not only a problem in developed nations, but is rapidly becoming a public health concern in countries undergoing the nutrition transition, such as Thailand, Chile and South Africa (SA),[5-7] to such an extent that the situation has been declared a global epidemic by the World Health Organization (WHO).[1] The WHO[8] views obesity as an independent risk factor for CVD, which significantly increases the risk of morbidity and mortality.

In Africa, the menace of CVDs has now become a serious health issue. In particular, sub-Saharan Africa has seen a tremendous increase in CVD risk factors, which has caused many deaths in both young and older persons.[9] SA is one of the countries in the sub-Saharan region of Africa undergoing a nutritional transition, in terms of changes in the dietary profile of the human population as a result of a shift from a traditional to a Western diet. Such a transition determines the nutritional status of the overall population.[10-11] Although obesity and CMD seem less life-threatening during childhood, their risk factors are particularly prevalent in the country and are progressing at a rapid pace. The prevalence of obesity and CMD has been partly attributed to the increase in urbanisation, industrialisation and adoption of a Western lifestyle, which negatively affect the quality of lives of many South Africans.[5,12] According to the American Heart Association,[13] CDLs are strongly and closely related to obesity and CMD risks, and 187

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strong evidence exists that elevated cholesterol levels in childhood may play a role in the development of hypertension later in life.[14] In addition, poor dietary intake and physical inactivity,[15-17] along with excessive body fat,[18-20] adversely affect CMD risks. These habits are often established during childhood,[8] thus allowing overweight and obesity to reach epidemic proportions in many countries.

Popkin et al.[21] highlight the high global prevalence of overweight and obesity among children and adolescents, particularly in urban areas and among girls: 9% and 27% in 15 - 17-year-old boys and girls, and 10% and 23% in boys and girls aged 10 - 14 years old, respectively. These trends have been supported by other national and regional studies,[10,11] which also showed an increased prevalence of obesity. In a recent SA survey published by Awotidebe et al.,[22] an indication of 8.7% pre-hypertensive and 4.3% hypertensive children was also reported. The findings of these surveys seem to warn against the potential health crises which could result given the increased incidence of childhood overweight, excessive body fat and abdominal adiposity as they are likely to add to the enormous socioeconomic and public health burden in future. Therefore, these trends should be closely monitored and prioritised in the face of all other health needs in the country.

Despite the fact that research reports overwhelmingly support the association between bodyweight disorders, such as underweight, overweight and obesity, with CMD,[12] regional comparisons among children in the SA context are problematic, in view of the different criteria used to evaluate the anthropometric and CMD variables among the children in the various studies.[22-24] A number of studies have also determined the correlation of different anthropometric indices with obesity and CMD risk factors among children in developed countries.[3,4] The results of such studies have been based on a number of criteria derived from the Childhood Obesity Working Group of the International Obesity Task Force (COWG/ IOTF) age- and sex-specific BMI cut-off point,[25] the Centers for Disease Control and Prevention BMI-dependent cut-off point of the

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RESEARCH upper 5th percentile, developed by Must and Strauss[26] based on the US NHANES and the standards suggested by the WHO/US National Center for Health Statistics. These studies used both percentile norms by age and gender and cut-off points to classify children as underweight, normal, overweight or obese.

Although these references proved to be good indicators of adverse health outcomes in developed countries,[27-29] the trends are, however, difficult to quantify, in view of the existence of a wide variety of definitions of childhood obesity. Moreover, little is known about the health consequences of bodyweight disorders among SA children.

Consequently, studies evaluating associations between health outcomes and bodyweight categories defined by different sets of cutoff points are needed to inform the decision on which method best assesses the risk. Therefore, in this study, the age- and sex-specific BMI cut-off point developed by Cole et al.,[25] for COWG/IOTF was used to assess the risk factors of obesity and CMD in SA children.

The rationale for the use of IOTF classification is that it has been, firstly, recommended internationally as a screening rather than a diagnostic tool for paediatric obesity. Secondly, the IOTF criteria correlate with total body fat and CMD risk factors. Thirdly, the definition is less haphazard and more internationally acceptable than others, and should encourage direct comparison of trends in childhood obesity worldwide. Nevertheless, definitions of the interaction effects for phenotypes related to obesity and CMD are important because they have the potential to screen and identify children at risk, detect early development of complications and recognise those that are likely to be resistant to health-related interventions.

Therefore, the objectives of this study were to assess the predictors of overweight and obesity in SA children and adolescents, and examine the extent to which these dependent measures correlate with CMD risk.

various parts of the provinces. Demographic data, which included age, gender and ethnicity, were obtained from participants, as these were regarded as correlates of obesity, normal weight, overweight and underweight among the children. For convenience and ease of data interpretation, the participants were categorised as children (ages 9 - 11 years) and adolescents (ages ≥12 - 13 years).

Methods

Defining weight categories

Ethical considerations

The Health Sciences Research Ethics Committee of the Faculty of Health Sciences, North-West University, SA (Ethics Ref. no. NWU00088-12-S1) granted ethics approval for the research to be carried out. Before data collection, permission to conduct the study was granted by the provincial heads of the education departments and the district managers for the Department of Basic Education in Limpopo and Mpumalanga provinces. Information leaflets and informed consent forms were administered to the head teachers, pupils and their parents or guardians, who gave permission for the study to be conducted. The research complied with the Health Professions Council of SA’s General Ethical Guidelines for Health Researchers.[30]

Sampling

The study was conducted using a cross-sectional design, in which data were collected on body composition and blood pressure among targeted samples of primary-school children in the Limpopo and Mpumalanga provinces of SA. These provinces, which share a common boundary, are relatively under-resourced compared with the other provinces in the country, and the majority of the people belong to the lower socioeconomic brackets. The study sample comprised 1 361 participants (678 boys and 683 girls, aged 9 - 13 years) who were selected from rural primary schools located in the two provinces.

To select the samples, schools in each province were numbered serially based on an alphabetical listing. Subsequently, eight schools were randomly selected from each province. Class registers were used to draw targeted groups of children whose ages could be verified. Children who were reportedly ill and/or were outside of the age limits set for the study were excluded. Overall, participants were randomly selected from 16 rural primary schools located in 188

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Anthropometric measurements

Height and weight were measured using the protocol of the International Society for the Advancement of Kinanthropometry.[31] Body composition indices of BMI (weight/height2) were derived. BMI was used to classify the children into the following weight categories: underweight, normal weight, overweight or obese for age and gender.

Based on the BMI classification, COWG/IOTF’s age- and sex-specific BMI cut-off point, developed by Cole et al.,[25] was applied in order to evaluate the children at risk of obesity and CMD. The results were then compared with available normative data.

Blood pressure measurements

Blood pressure (BP) was measured using an electronic BP monitor (Omron HEM-705 CP devices (Omron Corporation, Japan). The standardised guidelines of the National Heart, Lung, and Blood Institute’s National High Blood Pressure Education Program (NHLBI/NHBPEP) were applied for the assessment of BP among the children.[32] Elevated BP was defined as the mean systolic and the diastolic BP above the 95th percentile for age and gender, after adjusting for weight and height.[32] Based on these guidelines, the first and third readings of the BP monitor were taken as systolic and diastolic BP (SBP and DBP), respectively. The averages of the two BP measurements were used to examine the existence of the incidence of hypertension associated with obesity and CMD risks among SA children.

BMI was determined by dividing the participants’ weight (kg) by the square of their height (m); BMI defined as kg/m2 offers a reasonable measure of fatness in children. The IOTF cut-off points are widely accepted, and have been used as the global standard for age- and gender-specific norms of BMI classifications to categorise overweight and obesity in youths aged 2 - 18 years old.[25,26] In this study, the BMI cut-off point was used as a determinant of overweight and obesity among children and adolescents aged 9 - 13 years.

Pilot study

A pilot study was conducted before the actual data collection, to ascertain the logistical and technical procedures for taking the measurements. This was preceded by an intensive training workshop conducted by two experts in kinanthropometry, who have many years of experience and have published extensively in the area of body composition and childhood and adolescent physiology. The objectives of the workshop and pilot study were to ensure that the field workers could competently undertake the anthropometric and physiological measurements.

Statistical analysis

Mean and standard deviation were calculated for body weight, height, BMI, SBP and DBP for all age and gender categories.

Differences in these measurements were evaluated for boys and girls using independent variables. In order to compare differences in the prevalence of overweight and obesity and, consequently, hypertension among the children, a series of inferential statistics were computed. Bivariate analysis was conducted to examine if significant relationships existed between BMI and CMD risk factors.

Binary logistic regression analysis was performed to determine the variables which predicted the children’s age-related BMI categories.

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0.185 0.001 0.000 0.000 0.000 0.081 –1.33 3.40 5.63 4.87 3.91 1.75 12.4 (0.48) 147.8 (8.70) 42.0 (9.96) 19.2 (4.25) 116.3 (14.6) 78.7 (12.2) 116 (50.9) 95 (41.6) 13 (5.7) 4 (1.8) 228 (100)

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BMI = body mass index; BP = blood pressure; mmHg = millimetres of mercury.

10.1 (0.78) 138.4 (48.4) 31.9 (7.48) 16.9 (2.74) 112.4 (12.8) 78.0 (12.9) 355 (78) 94 (20.7) 5 (1.1) 1 (0.2) 455 (100)

10.2 (0.78) 137.7 (59.3) 31.1 (8.23) 20.6 (7.61) 109.4 (13.2) 76.8 (13.3) 348 (84.7) 57 (13.9) 3 (0.7) 3 (0.7) 411(100)

–1.04 0.17 1.42 –1.03 3.38 1.36 -

0.300 0.869 0.156 0.301 0.001 0.176 Age (years) Height (cm) Body mass (kg) BMI (kg/m2) Systolic BP (mmHg) Diastolic BP (mmHg) Underweight, n (%) Normal, n (%) Overweight, n (%) Obese, n (%) Overall, n (%)

Adolescents (n=495) Girls (n=267) t-value Boys (n=228) Table 2. Anthropometric characteristics and weight status (mean (SD)) of participants (N=1 361) Children (n=866) Variable Boys (n=455) Girls (n=411) t-value p-value

153 144 12

171 172 11

SD = standard deviation; BMI = body mass index; p = p-value; kg = kilograms; kg/m2 = kilograms per square meter; SBP = systolic blood pressure; DBP = diastolic blood pressure; mmHg = millimetres of mercury. *Statistically significant (p≤0.05).

0.001*

0.604

0.004* 145 170 10

12.4 (0.49) 145.2 (8.92) 37.4 (7.94) 17.6 (2.45) 111.4 (13.1) 76.7 (13.5) 196 (73.4) 66 (24.7) 4 (1.5) 1 (0.4) 267 (100)

p-value

0.551

0.787

0.002*

0.470

80.8 (14.5) 74.9 (12.9) 76.1 (12.3) 76.5 (13.6) 79.3 (14.9) 79.3 (12.6) 75.8 (11.5) 77.4 (12.1) 79.9 (14.7) 77.3 (12.9) 76.0 (11.9) 76.9 (12.9) 0.003*

105.9 (11.7) 109.3 (12.6) 111.3 (13.9) 110.5 (13.7) 111.3 (13.4) 113.3 (11.9) 112.1 (13.1) 116.4 (15.2) 108.8 (12.9) 0.939 111.4 (12.4) 0.051 111.7 (13.5) 0.002* 113.3 (14.8) 0.617

16.0 (1.7) 17.0 (3.3) 17.2 (4.7) 17.2 (2.5) 15.9 (1.9) 17.1 (2.3) 17.4 (3.3) 18.6 (4.4) 15.9 (1.8) 0.446 17.0 (2.8) 0.001* 17.3 (4.0) <0.001* 17.9 (3.6) 0.977

130.4 (6.4) 134.5 (6.2) 138.1 (5.8) 142.2 (8.0) 130.7 (7.2) 135.3 (6.8) 140.5 (7.2) 145.7 (8.2) 130.6 (6.9) 0.959 134.9 (6.5) <0.001* 139.3 (6.6) <0.001* 143.9 (8.2) 0.670

27.4 (4.7) 31.1 (6.2) 33.0 (10.2) 35.2 (7.7) 27.5 (5.4) 31.5 (6.3) 34.9 (8.1) 39.6 (9.3) 27.4 (5.1) 31.3 (6.3) 34.0 (9.3) 37.3 (8.8) 95 113

Girls 189

9

DBP (mmHg), mean (SD) All Boys Girls SBP (mmHg), mean (SD) p All Boys Girls p p

The children’s physical characteristics according to age categories and gender are provided in Table 1. The results showed that there were significant agerelated differences between boys and girls in terms of body mass, height, BMI, SBP, and DBP. For instance, boys had a significantly higher mean body weight at ages 11, 12 and 13 years compared with the girls. Age-related significant differences were also observed for height in boys at ages 11, 12 and 13 years (p<0.05). Mean BMI values were significantly higher in boys at ages 12 and 13 years compared with the girls of the same age groups (p<0.05). A significantly higher mean SBP was found in boys at ages 9, 10 and 12 years than in girls of the same ages. The mean DBPs for boys were significantly higher than those of girls at ages 10 and 13 years (p<0.05). Comparisons of the boys’ and girls’ data for body mass, height and BMI at ages 9 and 10 yielded no significant differences.

Anthropometric characteristics and prevalence rates of overweight and obesity in the boys and girls are presented in Table 2. In the younger age group, participants differed only in SBP (p=0.001), with the boys having higher mean values. Of the total number of children, 81.2% were underweight, 17.4% had normal BMI, 0.9% were overweight, and 0.5% obese. In the adolescent group, participants differed substantially in four variables (height, p=0.001; body mass, p<0.001; BMI, p<0.001; and SBP, p<0.001). BMI was normal in 32.5% of the adolescents, whereas 3.4% were overweight and 1.0% obese. In both groups, the prevalence of overweight was higher among boys for both children and adolescents than among the girls, whereas the obesity prevalence rate was higher among girls, for children, and among adolescent boys (p<0.05). When overweight and obesity were combined (Table 3), the prevalence rate was lower (1.4%) in the children than adolescents (4.4%). The overall rate of overweight and obesity combined was 2.5% in the whole group of subjects.

Table 4 details the mean BMI and prevalence rates of overweight and obesity, stratified by age and sex, based on the IOTF criteria. The average BMI

BMI (kg/m2), mean (SD) All Boys Girls

Results

Table 1. Physical characteristics according to age groups and gender Age, Body mass (kg), Height (cm), (years) n n mean (SD) p mean (SD) Boys Girls All Boys Girls All Boys

All data analyses were performed with the Statistical Package for the Social Sciences (SPSS) version 24.0 (IBM Corp., USA). For all statistical analyses the level of significance was set at p≤0.05.

p

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RESEARCH Table 3. Prevalence of overweight and obesity combined among participants (N=1 361) Group n Overweight, n (%) Obese, n (%)

Total, n (%)

Children Adolescents Total

12 (1.4) 22 (4.4) 34 (2.5)

866 495 1 361

8 (0.9) 17 (3.4) 25 (1.8)

4 (0.5) 5 (1.0) 9 (0.7)

Table 4. Prevalence of overweight and obesity stratified by age and sex using the IOTF criteria Boys (n=683) Girls (n=678) BMI, BMI, mean (SD) Overweight, % Obese, % n mean (SD) Overweight, % Age (years) n 9 113 15.9 (1.96) 0.0 0.0 95 16.0 (1.76) 0.0 10 170 17.1 (2.36) 1.2 0.0 145 17.2 (2.98) 0.7 11 172 17.6 (3.13) 1.7 0.6 171 17.3 (4.72) 1.2 Total children 455 16.8 (2.48) 1.1 0.2 411 16.8 (3.15) 0.7 12 144 18.7 (4.41) 4.2 2.1 153 17.3 (2.59) 2.0 13 84 20.0 (3.84) 8.3 1.2 114 18.0 (2.21) 0.9 Total adolescents 228 19.4 (4.13) 5.7 1.8 267 17.7 (2.40) 1.5

Obese, % 0.0 0.7 1.2 0.7 0.7 0.0 0.4

IOTF = International Obesity Task Force; BMI = body mass index; SD = standard deviation.

Table 5. Prevalence of overweight and obesity stratified by sex and province using the IOTF criteria Boys (n=683) Girls (n= 678) BMI, Provinces n mean (SD) Overweight, % Obese, % n BMI, mean (SD) Overweight, % Children Limpopo 158 16.5 (2.43) 0.3 136 16.3 (1.93) 0.0 Mpumalanga 125 16.8 (2.04) 0.8 0.0 104 17.3 (3.25) 1.0 Adolescents Limpopo 191 18.2 (3.81) 2.2 0.5 223 17.5 (4.40) 1.0 Mpumalanga 209 18.7 (3.94) 1.4 0.7 215 17.4 (2.26) 0.5

Obese, % 0.0 0.4 0.5 0.2

IOTF = International Obesity Task Force; BMI = body mass index; SD = standard deviation.

Table 6. Correlation matrix showing relationship between BMI and risks factors of CMD variables (N=1 361) Variables Age Body mass Height BMI SBP Age Body mass Height BMI SBP DBP

Coefficient (r) Coefficient (r) Sig. (2-tailed) Coefficient (r) Sig. (2-tailed) Coefficient (r) Sig. (2-tailed) (r) Coefficient (r) Sig. (2-tailed) Coefficient (r) Sig. (2-tailed)

1 0.501* 0.000 0.129* 0.000 –0.022 0.418 0.113* 0.000 –0.029 0.286

DBP

1 0.202* 0.000 0.026 0.341 0.290* 0.000 0.133* 0.000

1 –0.091* 0.001 0.037 0.176 0.065† 0.016

1 0.018 0.516 0.074* 0.007

1 0.440* 0.000

1

BMI = body mass index; CMD = cardiometabolic disease; SBP = systolic blood pressure; DBP = diastolic blood pressure. *Significant at 0.01. † Significant at 0.05.

for boys generally increased with age, from 9 to 10 years and 11 to 13 years, but the trend among the girls was inconsistent, especially for those who were 11 - 13 years old. However, among the adolescent girls, the BMI scores at ages 11 and 12 years remained stable, and thereafter increased at age 13 years. The prevalence of overweight and obesity tended to be higher among adolescent boys and girls (aged 12 - 13 years) than among the children (9 -11 years).

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The prevalence of overweight and obesity stratified by sex and province is presented in Table 5.

The results showed that male children living in Limpopo had a lower prevalence of overweight (0.3%), and were not obese (0.0%), compared with those from Mpumalanga Province.

However, none of the male participants were obese. Female children living in Mpumalanga Province had higher prevalence rates of

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RESEARCH Table 7. The odds of becoming overweight in female children according to age and province (n=411) Variables OR 95% CI p-value Province Limpopo 1 0.06 - 1.82 0.201 Mpumalanga 0.33 Age 2.88 0.69 - 11.9 0.144 OR = odds ratio; CI = confidence interval .

overweight (1.0%) and obesity (0.4%) than their counterparts in Limpopo Province. In the adolescent group, boys in Limpopo Province had a higher percentage of overweight (2.2%) than their contemporaries in Mpumalanga Province, with a 1.4% overweight prevalence rate. Furthermore, boys from Mpumalanga Province had a higher prevalence of obesity (0.7%) compared with their peers from Limpopo Province (0.5%). However, girls from Limpopo demonstrated a higher prevalence of overweight (1.0%) and obesity (0.5%) than their peers from Mpumalanga. The results also showed a statistically significant relationship between age and body mass (r=0.501; p=0.000), height (r=0.129; p=0.000), and SBP (r=0.113; p=0.000) of the participants in the combined group of children and adolescents. BMI correlated significantly with height (r=–0.091; p=0.001) and DBP (r=0.074; p=0.007). Height was also found to be significantly positively correlated with DBP (r=0.065; p=0.016), while SBP (r=0.018; p=0.516) and age (r=–0.022; p=0.418) yielded nonsignificant correlations with BMI (Table 6).

Analysis of the influence of age, gender and province on overweight and obesity among female children revealed that the regression model was not significant (α2(2, N=411)=–14.742; p=0.201) (Table 7). The model explained between 1.1% and 7.5% of the variation in weight status, and correctly classified 58.2% of the cases. Furthermore, age did not make a significant contribution to the model, with an odds ratio of 2.88, suggesting that the likelihood of being overweight decreases by a factor of 2.9 with a unit increase in age among the children and adolescents. The results by province indicated that the likelihood of a girl from Mpumalanga becoming overweight or obese was 0.33 times higher than that of a girl in Limpopo.

Discussion

This study assessed the risk factors for obesity and CMD among 1 361 primary school children (boys, n=678; girls, n=683) aged 9 - 13 years in the Mpumalanga and Limpopo provinces of SA. Using the IOTF norms, we observed the prevalence of overweight and obesity by gender and age among the children. Furthermore, bivariate correlations between BMI and the risk factors for CMD were observed. The study of bodyweight disorders using the IOTF’s BMI criteria is of potential interest from a public-health standpoint. The use of age- and gender-related BMI centiles for assessing bodyweight disorders in SA youngsters could provide a window of opportunity to observe levels of overweight or underweight, which can be used as a tool to recognise such disorders, so that interventions to prevent health complications can be made.

However, during the quest to determine the right definition of overweight and obesity, to avoid overestimation, overweight and obesity in youth continue to rise globally.[35] The findings from our study revealed that underweight was most prevalent among the participants. The present findings corroborate those of Goon et al.,[33] who reported a higher prevalence of underweight than overweight and obesity in Nigerian children and adolescents. Despite the prevalence of underweight found in this study, the fact of overweight and obesity still needs to be recognised as a potential public-health concern.

Studies have established that the prevalence of overweight and obesity is no longer limited to technologically advanced countries, 191

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but is currently a rising public health problem in emerging economies.[33,34] As stated by Reddy et al.,[35] one out of five children in SA is either overweight or obese. Findings from this present study showed that the prevalence of overweight and obesity combined for boys and girls in the younger age category were 1.1% and 1.2%, respectively.

The equivalent rates for adolescent boys and girls were 8.0% and 1.9%, respectively. In younger age groups, the rates were higher in girls, while among adolescents, higher prevalence rates were noted among the boys. This contradicts the results of a study by Musa et al.,[34] which found a high prevalence of combined overweight and obesity of 19.7% and 23.2% for 9 - 11-year-old Nigerian children.

In our study, it was observed that the rate of combined overweight and obesity was higher for adolescent boys than girls. This finding was surprising, in that girls usually have a higher propensity to be overweight and obese than boys of a similar age group.[27-29] Overweight and obesity were more common in adolescents than in children in the present study. These findings contradict those of Schnohr et al.,[36] which showed a higher prevalence of overweight and obesity in children than in adolescents.

Both male and female children in Mpumalanga province exhibited a higher prevalence of overweight and obesity than those from Limpopo province. From a public health perspective, the epidemic of overweight and obesity could have damaging consequences, resulting in poor health outcomes as a result of its association with CMD risk.

Furthermore, both overweight and obesity might have destructive consequences for the growth and motor development of children.[37] Studies have also indicated that overweight and obesity could have deleterious outcomes if left without any preventive intervention, as the youngsters in these studies were in developmental stages.[33-35] The results of this study underscore the significance of adopting a healthy lifestyle at an early developmental stage.[38] Although our study focused mainly on overweight and obesity, the existence of underweight conditions in this cohort of children and adolescents should not be ignored. Some of the reasons stated in previous studies as possible causes of underweight in developing countries were poverty levels, low socioeconomic backgrounds, environmental factors, poor nutritional intake and food practices and parents’ ignorance of this,[33-35] and of the dangers of a sedentary lifestyle or the influence of genetic endowment.[33-35] As many children from public primary schools in our study were from low socioeconomic backgrounds, they probably had limited access to daily balanced diets.

Limitations

The findings of this study should be interpreted in light of a number of limitations. Firstly, BMI is only a surrogate measure of body composition, and cannot reliably distinguish between fat-free mass and adipose tissue. Secondly, since our study was carried out in only two provinces of SA, the present findings cannot be generalised to the entire country, because of its demographic and racial diversity.

Thirdly, hereditary endowment may also partly account for the observed outcomes, but this aspect was beyond the scope of the study. Lastly, children’s socioeconomic background and nutrition were not assessed in the present study, but these may give a proper indication of their lifestyles, and further elucidate the results.

Conclusion

The occurrence of overweight and obesity in a combined sample of SA children was lower than the rate observed for adolescent boys and girls. Overall, children from Mpumalanga Province exhibited a higher incidence of overweight and obesity than those from Limpopo Province. Owing to the increasing prevalence of overweight and obesity in these children and adolescents, urgent preventive interventions that target high-risk behaviours in early life should be implemented in primary and secondary schools, thereby creating

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RESEARCH awareness of the consequences of bodyweight disorders, especially in low socioeconomic groups.

Acknowledgements. The authors are thankful to the provincial Departments of Basic Education of Limpopo and Mpumalanga provinces, the Department of Education District Offices, school authorities, teachers, parents and the children who participated in the study, for their co-operation. Sincere gratitude goes to the University of Limpopo students’ research team for their assistance in data collection. The authors express their profound appreciation to the Physical Activity, Sport and Recreation School for Biokinetics, Recreation and Sports Science, North-West University, as well as the Department of Sport, Rehabilitation and Dental Sciences, Tshwane University of Technology, for facilitating the logistics of the study.

Author contributions. VKM developed the concepts, collected data, performed the data cleaning, analysis and interpretation, and drafted the manuscript. MvS technically reviewed the manuscript.

Funding. This material is based upon work supported financially by the National Research Foundation (NRF) of SA. Conflicts of interest. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors, and therefore the NRF does not accept any liability in this regard.

1. World Health Organization. Global Strategy on Diet, Physical Activity and Health: Childhood Overweight and Obesity. Geneva: WHO, 2011. http://www.who.int/ dietphysicalactivity/childhood/en/ (accessed 8 February 2012) 2. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007-2008. JAMA 2010;303(3):242-249. https://doi.org/10.1001/jama.2009.2012 3. Del-Rio-Navarro BE, Velazquez-Monroy O, Lara-Esqueda A, et al. Obesity and metabolic risks in children. Arch Med Res 2008;39(2):215-221. https://doi. org/10.1016/j.arcmed.2007.07.008 4. Wake M, Hardy P, Canterford L, Sawyer M, Carlin JB. Overweight, obesity and girth of Australian preschoolers: Prevalence and socioeconomic correlates. Int J Obes 2007;31(7):1044-1051. https://doi.org/10.1038/ sj.ijo.0803503 5. Rossouw HA, Grant CC, Viljoen M. Overweight and obesity in children and adolescents: The South African problem. S Afr J Sci 2012;108(5-6):31-37. https:// doi.org/10.4102/sajs.v108i5/6.907 6. Toriola AL, Moselakgomo VK, Shaw BS, Goon DT. Overweight, obesity and underweight in rural black South African children. S Afr J Clin Nutr 2012;25(2):5761. https://doi.org/10.1080/16070658.2012.11734406 7. Singh R. Childhood obesity: An epidemic in waiting? Int J Med Public Health 2013;3(1):2-7. https://doi.org/10.4103/2230-8598.109298 8. World Health Organization. Obesity and overweight: Diet and physical activity.

Geneva: WHO, 2010. http://www.who.int/dietphysicalactivity/childhoo/en/ (accessed 20 November 2010).

9. Ramoshaba N, Monyeki K, Hay L. Components of height and blood pressure among Ellisras rural children: Ellisras longitudinal study. Int J Environ Res Public Health 2016;13(9):856. https://doi.org/10.3390/ijerph13090856 10. Kimani-Murage EW. Exploring the paradox: Double burden of malnutrition in rural South Africa. Glob Health Act 2013;6(0):1924-1929. https://doi.org/10.3402/ gha.v6i0.19249 11. Tathiah N, Moodley I, Mubaiwa V, Denny L, Taylor M. South Africa’s nutritional transition: Overweight, obesity, underweight and stunting in female primary school learners in rural KwaZulu-Natal, South Africa. A Afr Med J 2013;103(10):718723. https://doi.org/10.7196/samj.6922 12. Kimani-Murage EW, Kahn K, Pettifor JM, et al. The prevalence of stunting, overweight and obesity, and metabolic disease risk in rural South African children. BMC Public Health 2010;10(1):158. https://doi. org/10.1186/1471-2458-10-158 13. American Heart Association. Cardiovascular Disease Statistics. Dallas: AHA, 2010. http//www.circ.ahajournals.org (accessed 4 November 2016).

14. Shields M, Tremblay MS. Canadian childhood obesity estimates based on World Health Organization, International Obesity Task Force and Centers for Disease Control and Prevention cut-off points. Int J Pediatr Obes 2010;5(2):265-273. https:// doi.org/10.3109/17477160903268282 15. Foo LH. Influence of body composition, muscle strength, diet and physical activity and total body and forearm bone mass in Chinese adolescents girls. Brit J Nutr 2007;98(6):1281-1287. https://doi.org/10.1017/ s0007114507787421

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16. Ford C, Ward D, White M. Television viewing associated with adverse dietary outcomes in children ages 2 - 6. Obes Rev 2012;13(12):1139-1147. https://doi. org/10.1111/j.1467-789x.2012.01028.x 17. Ferreira FS. Relationship between physical fitness and nutritional status in Portuguese sample of school adolescents. J Obes Weight Loss Ther 2013;3(5):36. https://doi.org/10.4172/2165-7904.1000190 18. Lee DC, Artero EG, Sui X, Blair SN. Review: Mortality trends in the general population: The importance of cardiorespiratory fitness. J Psychopharmacol 2010;24(Suppl 4):S27-S35. https://doi. org/10.1177/1359786810382057 19. Amusa LO, Goon DT, Amey AK, Toriola AL. Health-related physical fitness and associations with anthropometric measurements in 7 - 15 year old school children. J Pediatr 2011;86(6):497-502.

20. Goon DT, Toriola AL, Shaw BS, Akinyemi O. Can waist circumference be estimated from BMI in Nigerian children? Gazz Med Ital 2011;170(4):225-228.

21. Popkin BM, Adair LS, Ng SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutri Rev 2012;70(1):3-21. https://doi. org/10.1111/j.1753-4887.2011.00456.x 22. Awotidebe A, Monyeki MA, Moss SJ, Strydom GL, Amstrong M, Kemper HCG. Relationship of adiposity and cardiorespiratory fitness with resting blood pressure of South African adolescents: The PAHL Study. J Hum Hyper 2016;30(4):245-251. https://doi.org/10.1038/jhh.2015.81 23. Wakabayashi I. Age-dependent influence of gender on the association between obesity and a cluster of cardiometabolic risk factors. Gender Med 2012;9(4):267-277.

24. Goon DT, Toriola AL, Shaw BS, Amusa LO, Musa DI. Sex differences in anthropometric characteristics of Nigerian school children aged 9 - 2 years. Afr J Phys Health Educ Recr Dance 2008;14(2):130-142. https://doi.org/10.4314/ ajpherd.v14i2.24798 25. Cole TJ, Flegal KM, Nicholls D, Jackson AA. Body mass index cut-offs to define thinness in children and adolescents: International survey. BMJ 2007; 335(7612):194. https://doi.org/10.1136/bmj.39238.399444.55 26. Must A, Strauss RS. Risks and consequences of childhood and adolescent obesity. Int J Obes Relat Metabol Disord 2000;23(Suppl 2):S2-S11. https://doi. org/10.1038/sj/ijo/0800852 27. Hajian-Tilaki K, Heidari B. A comparison between International Obesity Task Force and Center for Disease Control references in assessment of overweight and obesity among adolescents in Babol, northern Iran. Int J Prev Med 2013;4(2):226-231.

28. Valerio G, Maffeis C, Balsamo A. Severe obesity and cardiometabolic risk in children: Comparison from two international classification systems. PloS One 2013;8(12):e83793. https://doi.org/10.1371/journal.pone.0083793 29. Edginton CR, Chin M, Amusa LO, Toriola AL. Health and physical education: A new global statement of consensus – perspectives from South Africa. Afr J Phys Health Educ Recr Dance 2012;18(2):434-441.

30. Edeling HJ, Mabuya NB, Engelbrecht P, Rosman KD, Birrel DA. HPCSA Serious Injury Narrative Test Guideline. S Afr MedJ 2013;103(10):763-766. https://doi. org/10.7196/SAMJ.7118 31. The International Society for the Advancement of Kinanthropometry.

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Glasgow: ISAK, 2006.

32. Cooper CB. Blood pressure measurement, hypertension and endurance exercise. ACSM Health Fit, 2000;4:32-33.

33. Goon DT, Toriola AL, Shaw BS. Screening for body weight disorders in Nigerian children using contrasting definitions. Obes Rev 2010;11(7):508-515. https://doi.org/10.1111/j.1467-789x.2009.00682.x 34. Musa DI, Toriola AL, Monyeki MA, Lawal B. Prevalence of childhood and adolescent overweight and obesity in Benue State (Nigeria). Trop Medicine Int Health 2012;17(11):1369-1375. https://doi.org/10.1111/j.13653156.2012.03083.x 35. Reddy SP, Resnicow K, James S. Rapid increase in overweight and obesity among South African adolescents: Comparison of data from the South African National Youth Risk Behaviour Survey in 2002 and 2008. Am J Pub Health 2012;102(2):262-268. https://doi.org/10.2105/ajph.2011.300222 36. Schnohr C, Sørensen TI, Niclasen BVL. Changes since 1980 in body mass index and the prevalence of overweight among inschooling children in Nuuk, Greenland. Int J Circumpolar Health 2005;64(2):157-162. https://doi. org/10.3402/ijch.v64i2.17968 37. Malina RM, Bouchard C, Bar-Or O. Growth, Maturation and Physical Activity (2nd ed.). Champaign, Illinois: Human Kinetics, 2004.

38. Koning M, Hoekstra T, de Jong E, Visscher TLS, Seidell JC, Renders CM. Identifying developmental trajectories of body mass index in childhood using latent class growth (mixture) modelling: Associations with dietary, sedentary and physical activity behaviours: A longitudinal study. BMC Public Health 2016;16(4):1128-1134. https://doi.org/10.1186/s12889-016-3757-7 Accepted 3 May 2017.

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This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Community feedback on the JustMilk Nipple Shield Delivery System in the Vhembe District of Limpopo Province, South Africa A D Flynn,1 BS; R L Scheuerle,1,2 PhD; G Galgon,1 PhD; S E Gerrard,1,2 PhD; V O Netshandama,3 PhD JustMilk 501(c)(3) non-profit, Temecula, California, USA Department of Chemical Engineering and Biotechnology, Faculty of Engineering, University of Cambridge, UK 3 Department of Community Engagement, Faculty of School of Health Sciences, University of Venda, Thohoyandou, Limpopo, South Africa 1 2

Corresponding author: A Flynn (Aspen.Flynn@justmilk.org) Background. Infant medication administration is a major public-health challenge, especially in rural or low-resource areas. The JustMilk Nipple Shield Delivery System (NSDS) is a novel method of infant medication delivery designed to address some of these challenges.

Objective. To explore the acceptability of the JustMilk NSDS in selected communities in the Vhembe District of Limpopo, South Africa.

Methods. Data were collected through 39 semi-structured interviews and in five small groups (a total of 44 interviewees) with infant caretakers and health workers in the Vhembe District. Interviews were transcribed and coded into themes, which were verified by an independent coder.

Results. Four themes arose around the acceptability of the JustMilk NSDS: input on device design; perceived benefits of the device; perceived barriers to community acceptance; and suggested device applications. Participants expressed positivity about the NSDS concept.

The potential for increased dosing accuracy was stated as the main positive attribute of the NSDS. Potential stigma was noted, and the need for an education programme on the device was discussed. No major community barriers to NSDS use were noted. Acetaminophen and deworming agents were suggested as potential applications for the device.

Conclusion. Participants were enthusiastic about the potential benefits of the NSDS, and were interested in using the device to deliver medication to infants. Design suggestions, especially to combat the potential stigma of device use, will be thoroughly considered by the researchers. This study was a positive step forward in developing the NSDS as a novel method of medication delivery to breastfeeding infants, particularly in rural or low-resource areas.

S Afr J Child Health 2017;11(4):193-197. DOI:10.7196/SAJCH.2017.v11i4.1340

The purpose of this study was to identify factors that might influence the user-acceptability of the JustMilk Nipple Shield Delivery System (NSDS), a novel platform for delivering drugs and nutrients to breastfeeding infants, in the Vhembe District of Limpopo, South Africa (SA). Paediatric medication delivery is a major public-health challenge. Most medications are designed for adults, often resulting in a lack of both dosage-appropriate formulations for infants, and suitable methods for delivering infant medications.[1] The most common infant drug-delivery devices are measuring spoons, dosing cups and oral syringes, all of which deliver liquid formulations and can lead to dosing errors.[1,2] Additionally, they have the following problems: cold chain and refrigerated storage requirements; unpalatability; and the potential presence of harmful excipients.[3] Alternatively, solid dispersible tablets must be dissolved in potable water in a clean container before being administered as above.[4] The development of safe, effective and affordable paediatric drug delivery devices is crucial to alleviate these problems.[1,5] The JustMilk NSDS combines a modified nipple-shield with a dosage form such as a rapidly disintegrating tablet, and is currently in preclinical studies.[6-9] To use the NSDS, a mother places it over her breast, and as she breastfeeds, milk passes through the device, causing the active pharmaceutical ingredients (APIs) to be released directly from the tablet into the breast milk, which passes to the infant. The tablet is predosed with the infant medication and is designed to be rapidly delivered during feeding to minimise dosing concerns. Since the device utilises human milk as the tabletâ&#x20AC;&#x2122;s dissolving agent, potable

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water is not required to dissolve the tablet. The solid dispersible tablet may have a longer shelf life than liquid medication.

Limpopo is the northern-most province in SA, and has a population of 5.4 million. It is the most rural SA province, with 87% of the population considered rural, compared with the national average of 43%.[10] In this area, with limited access to health clinics, which often use liquid formulations, the long shelflife of a dry NSDS tablet insert could be beneficial.[11] The generally higher range of temperature stability with tablets (compared with liquids) could also be of use during the areaâ&#x20AC;&#x2122;s exceptionally hot and rainy summer seasons. In addition, intermittent electricity in the region may compromise refrigeration options for liquid formulations.[12] Limited access to potable water suggests that the potentially disposable nature of the device might be useful, as there would be no need to hygienically clean the device for reuse.[13,14] Breastfeeding is extremely common in the Vhembe district, as is the early introduction of mixed feeding.[15]

Methods

Study setting

This study was conducted in the Mutale and Thulamela municipalities of the Vhembe district of Limpopo, SA. Table 1 lists the specific characteristics of each of these municipalities.[16,17] Interviews with infant caretakers (ICs) and health workers (HWs) were conducted at four rural government clinics and in five communities. The clinics were Thondo Tshivhase Clinic, Rambuda Clinic, Mutale Health

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RESEARCH Centre and the University of Venda Campus Clinic. The communities were Tshilamba, Tshishivhe, Pile, Tshapasha and Tzhagwa.

Participant recruitment

Participants were recruited through purposive sampling. A key informant helped identify participants using her knowledge as a local community resident, and as a past fieldworker for the Malnutrition and Enteric Diseases (MAL-ED) study.[18] Eligibility criteria centred on identifying with at least one of the following categories: (i) IC of a child â&#x2030;¤5 years; or (ii) HW employed at a local clinic. A total of 35 ICs (30 mothers and 5 women elders) and 9 HWs participated in the study, resulting in 44 total participants (Table 2). ICs and HWs agreed to participate via informed verbal consent before interviews. Only those who agreed to participate contributed to the findings of the study.

Ethical considerations

Ethical approval was granted by the University of Venda (ref. no.

CE/14/01/1605), the Vhembe District Municipality Department of Health and Social Development (ref. no. 10/1/1) and the Limpopo Department of Health (ref. no. 4/2/2).

Data collection

Data collection occurred over 9 months in 2014, through 39 semistructured interviews with 44 total participants. Five interviews were conducted in small groups and 34 interviews were one-onone. Participants were asked open-ended questions relating to the potential acceptability of the NSDS. Topics included technology specifications, such as preferred device material, texture, shape, size and colour; the design of the tablet insert; packaging; acceptability within Venda culture and breastfeeding practices; possible stigma associated with device use; and potential applications of the technology.

Table 1. Characteristics of the study municipalities Feature Tribal/traditional area, % Mean household size Female-headed household, % Highest education level, % No schooling Some primary Completed primary Some secondary Completed secondary Higher education Not applicable Unemployment rate, % Flush toilet connected to sewerage, % Piped water inside dwelling, % Electricity for lighting, %

Data analysis

This study used grounded theory to collect and analyse data.[19] Interviews were transcribed and coded into themes and subcategories, which were verified through an independent coder. Handwritten notes were coded in a similar fashion. The data analysis was modelled on Teschâ&#x20AC;&#x2122;s methods of qualitative data analysis.[20] Member checking was completed with selected participants at a later date, as an added measure of ensuring data saturation.

Results

Four main themes emerged surrounding community acceptability of the JustMilk NSDS: input on device design; perceived benefits of the device; perceived barriers to community acceptance; and suggested device applications.

Device design

Mutale 96.8 3.8 54.8

Thulamela 85.4 3.9 54.4

2.2 45.5 7.0 36.7 6.8 1.1 0.7 48.8 3.8 5.8 83.3

2.3 42.7 6.4 36.0 9.6 1.9 1.1 43.8 10.7 15.2 87.2

Table 2. Participant information (N=44) Feature

Mothers

Participants, n Mean age, years Age range, years Mean no. of children No. of children range

30 27.9 19 - 45 1.6 1-4

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Participants were shown a video simulation of the NSDS. To assess shape preferences, mothers were shown the NSDS prototypes as well as three other shapes of commercially available conventional nipple shields. To assess device material preferences, participants were presented with conventional nipple shields of varying thicknesses.

To assess device colour preferences, two colours of NSDS prototypes, transparent and yellow (dyed with local materials), were shown as examples, and participants were informed that the device could be any colour. Tablet insert colour preferences were assessed by presenting NSDS prototypes each containing a single model tablet of a particular colour: white, yellow, green, blue or black.

Interviews with ICs were conducted at the homes of participants in the local Tshivenda language with a translator, or in English.

All interviews with HWs were conducted at local health clinics, in English. Transcription and coding of the semi-structured interviews began during data collection. Participant recruitment and subsequent interviews were concluded when it was determined that data saturation was reached.

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Device material A disposable, one-time-use device was preferred by a majority of participants. The main reasons for this were stated as ease of use and increased hygiene. Mothers considered that sterilising the device after every use might be inconvenient, time consuming, and difficult.

Some HWs and ICs noted cost and environmental impact as concerns with a disposable device, but these were secondary to prioritising hygienic medication-delivery practices. A concern over sufficient access to clean water was also brought up as a barrier to proper cleaning of the device.

Some ICs initially indicated a preference for a reusable device, expressing doubt that government clinics would be able to maintain a stock of the devices. However, after probing, it was revealed that these participants had a stronger preference for a disposable device for the same reasons as cited above.

A minority of participants, primarily ICs, strongly preferred a reusable device. One mother stated that a reusable NSDS would be more convenient because she would not need to travel to the clinic as frequently to acquire more devices. One grandmother

Infant caretakers (ICs) Grandmothers/elders 5 62 - 84 -

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Health workers (HWs) 9 46.4 24 - 60 -

RESEARCH noted that washing the device after each use would be similar to the current common practice of washing a spoon used to deliver infant medication, and liked this familiarity of practice.

Participants with either preference (disposable or reusable) expressed concern that a small child may find a used NSDS that had been improperly disposed of and play with it, causing disease in the child.

Most participants emphasised that the NSDS device should feel as similar to a breast as possible, while also maintaining a durable feel to ensure that it will not disintegrate or fall apart during use. ICs often preferred a material that they described as soft, but not too thin.

Device shape, size and colour The circular shape of the original NSDS prototype was preferred over alternative models with a reduced surface area (designed to increase skin-to-skin contact while breastfeeding). ICs, mothers in particular, expressed concern that an NSDS with a reduced surface area would fall off the breast during use. Many participants indicated a need for varying sizes of NSDS devices, stating that nipples are often different sizes, and the size of the current NSDS prototype would not fit all women’s nipples. Most participants preferred a transparent device, the major reason being that it would clearly show dirt on the device, allowing a mother to know if it was contaminated. A few mothers preferred a transparent device specifically because it would enable them to observe the medication dissolving and entering the infant’s mouth. One mother preferred a transparent device because she believed it to be the most discreet.

No participants preferred the yellow NSDS prototype to the transparent prototype. Some mothers did not have a strong preference between the two examples. Some mothers suggested making the device brown in colour to more accurately match skin tone, with a few stating that an infant might ‘run away’ or ‘be scared’ of a colour that did not match the breast. When probed about additional NSDS colours, most participants re-emphasised their original colour preference.

Tablet colour Most participants preferred a white tablet. Their reasons for this included that white was closest to the transparent colour of the sample prototypes, and white is the standard colour for many current medications in tablet form. Some ICs and HWs suggested coloured tablets resembling sweets to encourage the infant to come to the breast.

Packaging Participants were evenly split between preferring the pill prepackaged within the NSDS or requiring that an IC insert the tablet at home immediately before medication delivery. ICs who preferred receiving an NSDS with the pill already inside primarily cited hygiene as the reason for this preference, as it would require less direct handling of the device.

Some ICs specifically expressed a concern that mothers might not wash their hands before inserting the tablet, with one mother warning that this could ‘make a sickness to the child’. Some mothers also expressed

a fear that they might drop the tablet on the ground as they try to insert it into the NSDS. Convenience was also cited as a reason for this preference, but was not as heavily emphasised as hygiene.

Participants who preferred the notion of the mother or another IC inserting the tablet at home immediately prior to medication delivery often did not have a specific reason for this preference.

Some mothers, however, expressed concern that they might receive an NSDS with the incorrect medication if they did not put it in themselves.

In the case of a disposable device, most mothers preferred that the device come prepackaged with the tablet insert already loaded inside. A small portion of ICs preferred a device, either disposable or reusable, where they would place the tablet in themselves because it would make them feel more personally empowered and capable in ensuring the health of their infant.

Both ICs and HWs preferred that instructions for the device include a verbal explanation in the clinic, accompanied by a demonstration by the nurse. One mother also suggested that written instructions be included as a method to remind mothers how to use the device when they are at home (Table 3).

Perceived benefits of NSDS

All participants were enthusiastic about the NSDS, and most preferred the concept to current methods of infant medication delivery.

Accuracy of dosing The most popular aspect of the NSDS was that the medication is predosed, eliminating the need to manually measure medication.

Many infant medications in the Vhembe district are administered as syrups or liquid suspensions, and delivered with a measuring spoon provided by the clinic or with a household teaspoon, and these two instruments often differ in size. Additionally, most mothers mentioned challenges in ensuring that the infant swallows the full dose, stating that the medication often runs down the side of the infant’s mouth during administration. Participants often mentioned that they were unsure if the baby was receiving the proper dose. These concerns included both under-dosing and over-dosing.

Ease of delivery Participants often stated that using the NSDS might increase the willingness of the infant to swallow medication. Many participants noted that infants do not like the taste of medication and do not want to swallow it. Several ICs mentioned squeezing the infant’s mouth during administration to facilitate the process. The word ‘force’ came up several times when participants described their experiences in administering infant medication.

Breastfeeding practices Some participants brought up the fact that the NSDS could be easily incorporated into existing breastfeeding practices. A few participants

Table 3. Interview quotes on NSDS design Sub-theme Material Colour Packaging

Quote ‘If it’s disposable … it’s going to be very clean. I think it’s a good thing.’

‘I want to use it and throw it away. Because if I supposed to clean it, I will forget.’

‘People cannot see while I am using this one [transparent device].’

‘Maybe they just made a mistake and put the wrong medicine. Then myself I take that medication and give it to my child, my child then get ill. The nurse is gone; I’m left alone with my child being ill.’

‘Even though they come together with the pills inside, myself I would take it out for me to learn to get experience of putting the pills myself.’

‘Okay, they can tell me there at the pharmacy. When I get [to] the road, I’ve got some other problem, then I forget. So on the paper is easy. When I get there at home, I will read it.’

NSDS = JustMilk Nipple Shield Delivery System; IC = infant caretaker; HW = health worker.

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Participant, age IC: Grandmother, 65 IC: Mother, 45 IC: Mother, 29 IC: Mother, 22 IC: Mother, 30 IC: Mother, 21

RESEARCH mentioned that use of the device would encourage breastfeeding in the community. One mother mentioned that HWs especially recommend breastfeeding when an infant is ill, and explained that this device could act as a tool to encourage breastfeeding in the community (Table 4).

Perceived barriers to community acceptance of NSDS

A concern noted by many participants was that the device can only be used by mother-infant dyads who are currently breastfeeding, and would not be effective in delivering medication to toddlers. An additional need to address medication administration for this age group was expressed. It was also noted that some mothers work or go to school during the day and therefore would not always be present in the home to deliver medication through breastfeeding. Some ICs stated that without proper education, other community members might think that a mother using the device has HIV, or that she has a condition that does not allow her to breastfeed normally or come into contact with her baby.

Many participants emphasised the idea that they would not associate any stigma with the device if they had prior knowledge about the device’s function. Participants were highly encouraging about educating all members of the community on the purpose of the device. When probed on how they would feel if they saw someone else using the NSDS, participants mostly expressed thoughts of curiosity (Table 5).

Potential applications of NSDS

The most common tablet insert suggestion from ICs was acetaminophen, given for common infant illnesses such as colds,

coughs and fevers. This is currently delivered to infants as a syrup using a medication spoon. HWs often suggested the deworming medication albendazole, since it is only provided to government clinics as solid tablets, and requires crushing and mixing in potable water before delivery as a liquid. Antibiotics were also suggested, as participants noted that the forms they currently used were oral suspensions requiring refrigeration that last for only up to 7 days.

Discussion

All participant preferences for NSDS design, including disposability, a soft yet durable material, transparent colour and white API tablet will be carefully considered in future iterations of the NSDS design.

The reasoning behind preferring a disposable or reusable NSDS highlights a strong community value of hygiene in the Vhembe district. Current limited access to infant medication-delivery devices, such as medicine spoons, seemed to occasionally sway an IC to favour a reusable device, for fear that the NSDS might also have a limited availability, especially if distributed by the government Department of Health. This mistrust of government health services seemed to be a factor in many responses, and should be thoroughly considered in the implementation of NSDS use.

An interest, particularly from mothers, in learning how to insert the tablet and to watch the medication dissolve, suggests that mothers greatly value a sense of ownership towards the health of their infant. Further community input on how to incorporate the concept of ownership into every step of NSDS use should be considered. It was clear that some participants did not trust the government clinic to insert the correct medication into the NSDS. Additional research into trust between patients and government

Table 4. Interview quotes on perceived benefits of NSDS Subtheme Preference over current medication delivery methods Dosing accuracy

Ease of delivery Incorporating device into breastfeeding practices

Quote ‘Ah, it is good. Not going to suffer to give medicine by using the spoon.’

IC, age (years) Grandmother, 84

‘This is a perfect device because there is no way I can give overdose. I … am quite certain that I have given the right amount at the right time because if it comes already packaged, I just take one and give. So this is good.’

‘It is good because I give one dose. I might overdose with teaspoon, but this has the whole dose.’

‘The child cannot refuse to drink the medicine. She will always be drinking all the medicine.’

‘Even us who force the babies, there is no need to force now.’

‘It’s not like forcing the child, like squeezing. For this she will be breastfeeding, getting the medicine together.’

‘Yeah it would influence us to give us our babies the breast rather than the bottle.’

Grandmother, 84 Mother, 34 Mother, 37 Mother, 42 Mother, 30 Mother, 38

NSDS = JustMilk Nipple Shield Delivery System ; IC = infant caretaker; HW = health worker.

Table 5. Interview quotes on perceived barriers to acceptance of NSDS Subtheme Social stigma Education programme

Perception of others using the device

Quote ‘To me, there is not [a] problem, but I don’t know about others because what will they think? … If I have this one, some people maybe they don’t know about it. They will think I have HIV.’ ‘There is a need for … eh, education about the device. Because if in a household the mother just starts putting the shield and starts breastfeeding and has not explained that it is for administration of medication, people in the household, the in-laws would think oh, this mother has a really devastating disease … that she is afraid to pass to the … kid. Yeah. So, that part is very important that it’s communicated … before using it.’

‘Yeah, people … they won’t know about it. So you have to tell them, show them, so that they can understand what is this.’

‘I would have no problem because I will know that the mother is giving the child medicine.’

‘I would ask the mother what are you doing with that, with that thing? And the mother will tell me, I’m giving the medicine to the child.’

NSDS = JustMilk Nipple Shield Delivery System ; IC = infant caretaker; HW = health worker.

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IC, age (years) Mother, 20 Grandmother, 65

Mother, 21 Mother, 38 Grandmother, 84

RESEARCH health services is recommended. As the literacy level of ICs can be limited, NSDS instructions should include a visual component, such as drawings or diagrams.

Comments suggesting that NSDS use could have a significant impact on improving dosing accuracy, and might increase the willingness of a child to swallow medication, will be considered in future clinical research.

A community education programme may be necessary to address the hygienic use of the NSDS and to reduce potential social stigma, especially in association with HIV. Efforts will also be made to make the device as discreet as possible, allowing mothers to feel comfortable using it in a variety of social situations. A breastfeeding education programme may also complement NSDS use.

The shared responsibility of infant care within the household may present a barrier to NSDS use, as only the mother can deliver the medication with this system.

APIs suggested by participants will be thoroughly considered.

Specific emphasis will be placed on community preference, current infant-health needs in the region, and the feasibility of formulating the APIs into solid dispersible tablets.

The findings from these selected communities may be transferable to similar communities.

Study limitations

Back-and-forth translation from Tshivenda to English occurred during interviews with participants who only spoke Tshivenda. The interviews were transcribed and coded in English, based on these translations. While the translator was fluent in both languages, some nuances of the responses may have been lost or misunderstood during data analysis. However, the researchers are confident that all data acquired were valid, and data saturation was reached.

Interview conditions were not standardised, as they occurred within the various selected communities at participant homes and clinic offices. However, this interview environment was more familiar to participants, and therefore most likely encouraged accurate and thoughtful responses.

Despite these limitations, the researchers are confident that the information gathered is truthful and represents the full range of participant responses.

Conclusion

A qualitative research study was conducted in selected communities in the Vhembe district of Limpopo, SA, to assess the acceptability of the JustMilk Nipple Shield Delivery System (NSDS), a novel infant drug- and nutrient-delivery device. Data were collected through semi-structured interviews with 35 ICs and 9 HWs. A diversity of opinion was expressed within these interviews, which led to several suggestions on NSDS design and implementation. Four main themes arose addressing community acceptability of the JustMilk NSDS: input on device design; perceived benefits of the device; perceived barriers to community acceptance; and suggested device applications.

Participants had an overall positive reaction to the JustMilk NSDS, and did not cite any major cultural factors that would negatively affect community acceptance. Participants felt positive toward the current design and gave related suggestions, including that it more closely resemble the appearance and texture of a human breast. The most attractive features of the device appeared to be the potential for increased dosing accuracy compared with existing methods, and the possibility that infants will accept medication with greater ease.

Participants also emphasised the potential to incorporate NSDS use into current breastfeeding practices. An education programme to accompany device use was stated to be very important, to inform

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community members about hygiene practices surrounding device use, and to decrease any potential stigma. The NSDS and an associated education programme could provide an opportunity to encourage breastfeeding throughout the Venda community.

This study is a promising step in the design and implementation of the JustMilk NSDS. All suggestions by community members will be thoroughly considered, alongside feasibility of manufacturing.

Additional acceptability studies will be planned to inform future device iterations. Clinical studies will also be necessary to understand additional aspects of device acceptability by mother-infant dyads, and to ensure that the device does not pose any unforeseen hazard to the mother or child.

Acknowledgements. The researchers thank the translation services and community knowledge of Jeanet Rabambukwa, logistical support from the MAL-ED study at the University of Venda, logistical support from Queen Makwela and Sean O’Malley, and mentorship from Prof. Nuriye Hodoglugil and Prof. Ndola Prata at the University of California, Berkeley School of Public Health. We are grateful to Rebecca Smith for assistance in editing the manuscript.

Author contributions. ADF designed and implemented this research, conducted the majority of participant interviews and performed data analysis and manuscript preparation. RLS conducted interviews and provided substantial contribution to study design and manuscript preparation. GG was critical in revising the content of the work for publication. SEG contributed to study design and manuscript review.

VON provided substantial guidance on every step of study design, implementation, data analysis, and manuscript preparation.

Funding. This project receives funding from the Saving Lives at Birth: A Grand Challenge for Development programme, a joint effort by the US Agency for International Development (USAID), Grand Challenges Canada, the government of Norway, the Bill & Melinda Gates Foundation and the UK’s Department for International Development (DFID).

Additional thanks are given to the Gates Cambridge Trust for funding researcher Rebekah Scheuerle.

Conflicts of interest. ADF, RLS, GG and SEG were board members of JustMilk at the time of data collection. SEG and GG are listed inventors on US patent number 8357117, and ADF, RLS, GG and SEG are listed inventors on provisional US patent numbers 62/307,375; 62/337,805; and 62/424,006, all pertaining to the NSDS. 1. Walsh J, Bickmann D, Breitkreutz J, Chariot-Goulet M. Delivery devices for the administration of paediatric formulations: Overview of current practice, challenges and recent developments. Int J Pharm 2011;415(1-2):221-231. https://doi.org/10.1016/j.ijpharm.2011.05.048 2. Sobhani P, Christopherson J, Ambrose PJ, Corelli RL. Accuracy of oral liquid measuring devices: Comparison of dosing cup and oral dosing syringe. Ann Pharmacother 2008;42(1):46-52. https://doi.org/10.1345/aph.1K420 3. Tuleu C, Breitkreutz J. Educational Paper: Formulation-related issues in pediatric clinical pharmacology. Eur J Pediatr 2013;172(6):717-720. https://doi. org/10.1007/s00431-012-1872-8 4. United Nations Children’s Fund. Dispersible Tablets. New York: UNICEF, 2010. http://www.unicef.org/supply/index_53571.html 5. World Health Organization. WHO Drug Information 26(1). Geneva: WHO, 2012.

6. Sokal DC, Gerrard SE, Kneen E, Hubbard R, Galgon G, Banda T. Device and method for delivering an agent into breast milk while breastfeeding. US Patent no. US8357117 B2, 2009.

7. Gerrard SE, Baniecki ML, Sokal DC, et al. A nipple shield delivery system for oral drug delivery to breastfeeding infants: Microbicide delivery to inactivate HIV. Int J Pharm 2012;434(1-2):224-234. https://doi.org/10.1016/j. ijpharm.2012.05.035 8. Gerrard SE, Orlu-Gul M, Tuleu C, Slater NKH. Modelling the physiological factors that affect drug delivery from a nipple shield delivery system to breastfeeding infants. J Pharm Sci 2013;102(10):3773-3783.

9. Scheuerle RL, Gerrard SE, Kendall RA, Tuleu C, Slater NKH, Mahbubani KT. Characterising the disintegration properties of tablets in opaque media using texture analysis. Int J Pharm 2015;486(1-2):136-143. https://doi.org/10.1016/j. ijpharm.2015.03.023 10. Bessong PO, Nyathi E, Mahopo TC, Netshandama V. Development of the Dzimauli community in Vhembe District, Limpopo Province of South Africa, for the MAL-ED cohort study. Clin Infect Dis 2014;59(Suppl 4):S317-S24.

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RESEARCH https://doi.org/10.1093/cid/ciu418 11. United Nations Childrenâ&#x20AC;&#x2122;s Fund. Improving Newborn Care in South Africa: Lessons Learned from Limpopo Initiative for Newborn Care (LINC).New York: UNICEF, 2011. http://www.unicef.org/southafrica/SAF_resources_ newborncare.pdf 12. Van Schalkwyk A. A case study of non-payment for municipal services in the Vhembe District Municipality. Mediterr J Soc Sci 2012;3(12):90-105. https:// doi.org/10.5901/mjss.2012.v3n12p90 13. Rietveld LC, Haarhoff J, Jagals P. A tool for technical assessment of rural water supply systems in South Africa. Phys Chem Earth 2009;34(1-2):43-49. https:// doi.org/10.1016/j.pce.2007.12.001 14. Majuru B, Jagals P, Hunter PR. Assessing rural small community water supply in Limpopo, South Africa: Water service benchmarks and reliability. Sci Total Environ 2012;435-436:479-486. https://doi.org/10.1016/j.scitotenv.2012.07.024 15. Mushaphi L, Mbhenyane X, Khoza L, Amey A. Infant feeding practices of mothers and nutritional status of infants in Vhembe District in the Limpopo Province. S Afr J Clin Nutr 2008;21(2):36-41. http://www.ajol.info/index.php/ sajcn/article/view/34789 16. Statistics South Africa (SSA). Thulamela. Cape Town: SSA, 2011. http://www.

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statssa.gov.za/?page_id=993&id=thulamela-municipality (accessed 28 June 2017).

17. Statistics South Africa. Mutale. Cape Town: StatsSA, 2011. http://www.statssa. gov.za/?page_id=993&id=mutale-municipality (accessed 28 June 2017).

18. The MAL_ED Network Investigators. The MAL-ED study: A multinational and multidisciplinary approach to understand the relationship between enteric pathogens, malnutrition, gut physiology, physical growth, cognitive development, and immune responses in infants and children up to 2 years of age in resource-poor environments. Clin Infect Dis 2014;59(Suppl 4):S193-S206. https://doi.org/10.1093/cid/ciu653 19. Strauss A, Corbin J. Grounded theory research: Procedures, canons, and evaluative critieria. Qual Sociol 1990;13(1):3-21. https://doi.org/10.1007/ BF00988593 20. Tesch R. Qualitative Research: Analysis Types and Software Tools. New York: Taylor & Francis, 1990.

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CASE REPORT

This open-access article is distributed under Creative Commons licence CC-BY-NC 4.0.

Diandric triploidy in a liveborn infant with 3-4 syndactyly and a neural tube defect C E Spencer,1 MB ChB, DCH, FCMG, MMed (Med Genet); B Mofokeng,1 MB ChB; A Turner,1 MSc (Med) (Hum Genet); F Nakwa,2 MB BCh, FCPaeds, MMed (Paeds), Cert (Neonatol), Cert (Paed Neurol); A Krause,1 MB BCh, PhD Division of Human Genetics, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand and National Health Laboratory Service, Johannesburg, South Africa 2 Department of Paediatrics, Division of Neonatology, Chris Hani Baragwanath Academic Hospital, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa 1

Corresponding author: C E Spencer (careni.spencer@nhls.ac.za) Triploidy is a chromosomal abnormality caused by an additional set of haploid chromosomes. It is a common cause of early first-trimester miscarriages. Only very rarely are babies with triploidy born alive and even more rarely do they survive beyond the first few days of life. We present here a case of a term baby with confirmed paternal (diandric) triploidy and some unusual features, who survived for 50 days, and review the literature on those who survived.

S Afr J Child Health 2017;11(4):198-200. DOI:10.7196/SAJCH.2017.v11i4.1420

Triploidy is a chromosomal abnormality caused by an additional haploid set of chromosomes. It has been reported to occur in 1 to 3% of all conceptuses with most of these resulting in spontaneous miscarriage at an early gestation.[1] Only 1 in 10 000 fetuses with triploidy will survive to term, with only 1 in 1 200 of these surviving after birth.[2] The literature reports on only a small number of longterm surviving infants,[1] which is defined as those surviving >45 days.[2] Triploidy can occur due to maternal (digynic) or paternal (diandric) additional haploid chromosomes and, depending on the parent of origin, the phenotype can be predicted to some degree.

Potential karyotype complements are 69XXX, 69XXY or 69XYY. This report presents a case of paternal (diandric) triploidy with structural abnormalities, minimal dysmorphic features and long survival of 50 days.

Case report

A 4-day-old male was referred to the Division of Human Genetics, National Health Laboratory Service and the University of the Witwatersrand for a clinical genetic assessment, as he had multiple congenital abnormalities and the diagnosis was uncertain. Ethics approval for publication was obtained from the University of the Witwatersrand Human Research ethics committee (ref. no.

M1604107).

The patient was the only child to his non-consanguineous parents.

He had three maternal half-siblings, the eldest of whom has an intellectual disability and a clubfoot of unknown cause. There is no further family history of physical disability, neural tube defects or miscarriages.

The baby was born after an uneventful pregnancy, during which his 37-year-old G4P4 HIV-positive mother took antiretroviral medication, smoked six cigarettes per day and received adequate dosing of penicillin for a positive rapid plasma reagin (RPR) result. She attended regular antenatal clinics but no ultrasound investigations were conducted during the pregnancy. The baby was born at the local clinic at 39 weeks’ gestation by normal vertex delivery. His birth parameters were as follows: weight 1 670 g (Z-score <–3); length 35 cm (Z-score <–3); and head circumference 30 cm (Z-score <–3). He had severe and asymmetric intrauterine growth restriction. His Apgar scores were good but he was transferred to 198

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the academic referral hospital after birth as congenital abnormalities were noted and respiratory distress was present. Upon admission, his mild respiratory distress was presumed to be due to a congenital pneumonia and he was initiated on antibiotics.

On examination, he was noted to have a square head with a prominent forehead, prominent eyes and down-slanted palpebral fissures. He had mild facial asymmetry. His lips were thin with a smooth philtrum and his mouth was small with down-turned corners. He had bilateral 3-4 complete cutaneous syndactyly of his hands (Fig. 1). A lumbosacral myelomeningocele was present and there was no spontaneous movement of his lower limbs.

Investigations revealed normal kidneys on ultrasound and also a normal cranial ultrasound. His cardiac echogram showed a ventriculoseptal defect (VSD), atrioseptal defect (ASD) and a patent ductus arteriosus (PDA), with severe tricuspid regurgitation (TR) and a dilated right heart.

A quantitative fluorescent polymerase chain reaction (QF-PCR) (Elucigene QST*Rplusv2, United Kingdom) for aneuploidy demonstrated likely triploidy, which was confirmed by a karyotype demonstrating 69XXY in 11 out of 11 counted cells. The same QF-PCR investigation was used to determine the parent of origin of the additional haploid chromosome complement. Only maternal DNA was available and thus some markers were not informative. Of

Fig. 1. 3-4 cutaneous syndactyly of the infant’s right hand is demonstrated.

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CASE REPORT the 19 markers tested 11 were informative and confirmed that the additional haploid complement was not maternal in origin, leading us to conclude that this baby in fact had paternal (diandric) triploidy.

Three of the informative markers showed a single paternal allele of increased peak area ratio and 6 had two distinct paternal alleles.

The parents were counselled regarding the diagnosis and the poor prognosis. Management options were discussed with them and a decision was made not to offer extraordinary lifesaving measures in the event of a cardiac or respiratory arrest. The baby received orogastric feeds, antibiotics and dressings for his large myelomeningocele. He was also later treated for cardiac failure.

At about 3 weeks of age his condition was stable and a decision was made to close his myelomeningocele in order to facilitate the mother’s wish to care for him at home. This surgery was delayed owing to a confirmed Acinetobacter baumanii meningitis. His condition deteriorated and he was transferred to NICU for nasal continuous positive airway pressure and treatment of his infection.

He passed away in the NICU at 50 days of age owing to sepsis.

Discussion

Table 1. Summary of the long-surviving cases (>45 days) of triploidy reported in the literature and the origin of the additional haploid chromosome complement Survival

Parental origin

Karyotype

Fryns et al.

60 d

Mat

69,XXX

Cassidy et al.[9]

160 d

ND

69,XXX

Schrocksnadel et al.

7m

ND

69,XXX

Faix et al.[11]

127 d

ND

69,XXX

Strobel et al.

>5.5 m

ND

69,XXX

Arvidsson et al.[13]

27 w

Mat

69,XXY

312 d

Mat

69,XXY

10.5 w

Pat

69,XXX

Hasegawa et al.

46 d

Mat

69,XXX

Iliopoulos et al. [2]

164 d

Mat

69,XXX

Takabachi et al.

221 d

Mat

69,XXX

Present case

50 d

Pat

69,XXY

Study [8]

[10]

[12]

Sherard et al.

[14]

Niemann-Seyde et al.[15] [7]

[1]

Triploidy is a major cause of miscarriages.[3] Three different mechanisms can lead to triploidy: (i) a non-disjunction event in meiosis 1 or 2 of spermatogenesis; (ii) non-disjunction in meiosis 1 or 2 of oogenesis; and (iii) dispermy. Dispermy is considered to be the most common cause of triploidy.[4] Two different phenotypes are recognised based on whether the additional set of chromosomes is maternal (digynic) or paternal (diandric) in nature. Type 1 is diandric and recognised by a large, cystic placenta with a well-formed fetus and a normal or microcephalic head. Type 2 is digynic with a small non-cystic placenta and a growth-retarded fetus with relative macrocephaly.[4] In more recent larger studies this phenotypic distinction between maternal and paternal triploidy has been challenged.[5] Aside from the features defining type 1 and type 2 triploidy, the literature describes a multitude of other malformations. These include facial dysmorphism, central nervous system abnormalities in 50% of cases, cardiac defects in 31% of cases on second-trimester ultrasound, limb abnormalities and genito-urinary and gastrointestinal defects.[6] Type 1 fetuses are reported to be more likely to miscarry early in pregnancy, whereas type 2 cases often survive until later in the pregnancy and are more likely to live beyond birth.[7] In our case, the placenta was not available for examination and therefore we cannot comment on its features.

An investigation of the markers in the baby and the mother in this case showed that the infant had diandric triploidy and, for 6 of the 9 informative markers, two different alleles of paternal origin were identified. Thus, the mechanism causing triploidy was more likely to have been either dispermy or a non-disjunction event in meiosis 1 and very unlikely to have been due to an event in meiosis 2. Triploidy owing to a non-disjunction event in meiosis 2 will have a preponderance of similar-sized alleles, as two similar sister chromatids separate during this process. The determination that this baby had diandric triploidy was unexpected in view of the fact that the traditional clinical phenotype of a severely growthrestricted baby was compatible with a type 2 triploidy and also that the baby survived beyond birth, which is more common in digynic triploidy cases.[4] Subsequent literature suggests that this needs further investigation with larger sample sizes, and that the parent of origin cannot be used to provide a prognosis for the pregnancy or postnatal survival.[3] In our case, the infant presented with severe and asymmetric growth restriction, cardiac lesions and minimal dysmorphic features.

It was, however, the combination of the 3-4 syndactyly in a growthrestricted infant with a neural tube defect that prompted the consideration of triploidy as the diagnosis. Syndactyly of the third 199

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d = days; Mat = maternal; ND = not determined; m = months; w = weeks; Pat = paternal.

and fourth digits is an uncommon abnormality and only associated with a limited number of genetic syndromes. This case report highlights the need to consider triploidy in live-born infants with 3-4 cutaneous finger syndactyly.

Live birth is exceedingly rare in cases of triploidy. This male infant survived 50 days, which is considered a ῾long survival᾽ in the literature. Since 1977 there have only been 11 published reports of babies with triploidy living beyond 45 days.[1] Since this baby survived for 50 days, he represents the 12th case reported in the literature who survived beyond 45 days (Table 1). Infants affected with triploidy usually succumb to respiratory problems or pneumonia. It has been proposed that survival has improved owing to successful treatment of infections. The association between digynic triploidy and an increased chance of survival is perhaps now even less clear than previously thought, as this case represents a second example of diandric triploidy with long survival compared with 6 cases with digynic triploidy.

Despite the fact that some infants with triploidy live longer, their outcome is still extremely poor. The longest surviving child was only 10.5 months old and had severe neurological and developmental impairment.[14] Because of the poor outcomes, extreme measures to prolong life are not usually considered. The management should however be discussed in a multidisciplinary setting and in conjunction with the parents in order to respect their views and decisions.

Conclusion

This case report describes a term, severely growth-retarded infant with minimal facial dysmorphism, cutaneous 3-4 syndactyly, cardiac defects and a neural tube defect. He was confirmed to have triploidy that was likely diandric in origin. This case history illustrates that although most cases of triploidy end in miscarriage, live birth is possible. The diagnosis should be considered in growthrestricted babies with cutaneous 3-4 syndactyly and other suggestive features. There are only a handful of reported cases of triploidy in which infants survived beyond 45 days – our case was the 12th such description. With this report we add to the literature describing the clinical features of those babies with triploidy surviving more than 45 days and also question whether parental origin of the triploidy can reliably be used to predict likelihood of survival.

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CASE REPORT Acknowledgement. The authors wish to thank the family described in this case report for their permission to use this information.

Author contribution. All authors were involved in the management of this patient. CS drafted the initial manuscript and BM, FN, AT and AK reviewed and edited it.

Funding. None.

Conflict of interest. None.

1. Takabachi N, Nishimaki S, Omae M, et al. Long-term survival in a 69,XXX triploid premature infant. Am J of Med Genet A 2008;146A(12):1618-1621. https://doi.org/10/1002/amjg.a.32352 2. Iliopoulos D, Vassiliou G, Sekerli E, et al. Long survival in a 69,XXX triploid infant in Greece. Genet Mol Res 2005;4(4):755-759.

3. Baumer A, Balmer D, Binkert F, Schinzel A. Parental origin and mechanisms of formation of triploidy: A study of 25 cases. Eur J Hum Genet 2000;8(12):911917. https://doi.org/10.1038/sj.ejhg.5200572 4. McFadden DE, Kalousek DK. Two different phenotypes of fetuses with chromosomal triploidy: correlation with parental origin of the extra haploid set.

Am J Med Genet 1991;38(4):535-538. https://doi.org/10.1002/ajmg.1320380407 5. Joergensen MW, Niemann I, Rasmussen AA, et al. Triploid pregnancies: genetic and clinical features of 158 cases. Am J Obstet Gynecol 2014;211(4):370 e1-19. https://doi.org/10.1016/j.ajog.2014.03.039 6. Chen CP, Chern SR, Tsai FJ, Hsu CY, Ko K, Wang W. Prenatal diagnosis and molecular analysis of triploidy in a fetus with intrauterine growth restriction, relative macrocephaly and holoprosencephaly. Taiwan J Obstet Gynecol 2009;48(3):323-326. http://doi.org/10.1016/S1028-4559(09)60318-1

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7. Hasegawa T, Harada N, Ikeda K, et al. Digynic triploid infant surviving for 46 days. Am J Med Genet 1999;87(4):306-310. https://doi.org/10.1002/(sici)10968628(19991203)87:4%3C306::aid-ajmg5%3E3.0.co;2-6 8. Fryns JP, van de Kerckhove A, Goddeeris P, van den Berghe H. Unusually long survival in a case of full triploidy of maternal origin. Hum Genet 1977;38(2):147155. https://doi.org/10.1007/bf00527396 9. Cassidy SB, Whitworth T, Sanders D, Lorber CA, Engel E. Five month extrauterine survival in a female triploid (69,XXX) child. Ann Genet 1977;20(4):277-279.

10. Schrocksnadel H, Guggenbichler P, Rhomberg K, Berger H. Complete triploidy (69,XXX) surviving until the age of 7 months. Wien Klin Wochenschr 1982;94(12):309-315.

11. Faix RG, Barr M, Jr., Waterson JR. Triploidy: Case report of a live-born male and an ethical dilemma. Pediatrics 1984;74(2):296-299.

12. Strobel SL, Brandt JT. Abnormal hematologic features in a live-born female infant with triploidy. Arch Pathol Lab Med 1985;109(8):775-777.

13. Arvidsson CG, Hamberg H, Johnsson H, Myrdal U, Anneren G, Brun A. A boy with complete triploidy and unusually long survival. Acta Paediatr Scand 1986;75(3):507-510.

14. Sherard J, Bean C, Bove B, et al. Long survival in a 69,XXY triploid male. Am J Med Genet 1986;25(2):307-312. http://doi.org/10.1002/ajmg.1320250216 15. Niemann-Seyde SC, Rehder H, Zoll B. A case of full triploidy (69,XXX) of paternal origin with unusually long survival time. Clin Genet 1993;43(2):79-82. https://doi.org/10.1111/j.1399-0004.1993.tb04432.x

Accepted 31 July 2017.

DECEMBER 2017 Vol. 11 No. 4

CPD December 2017 The CPD programme for SAJCH is administered by Medical Practice Consulting.

CPD questionnaires must be completed online at www.mpconsulting.co.za

True (T) or false (F): Regarding HIV and viral lower respiratory tract infection (LRTI) in children admitted to the intensive care unit (ICU) 1. HIV-positive children who are admitted with viral LRTI have a higher in-hospital mortality compared with those who are HIVnegative.

2. Respiratory syncytial virus is the most common viral cause for admission to the ICU in children with LRTI. 3. In children who are admitted with viral LRTI, adenovirus infection is more common in HIV-positive than HIV-negative children.

Regarding infant hearing screening 4. Hearing loss is estimated to be present in 3 - 6/1 000 neonates in South Africa.

5. Targeted neonatal hearing screening is the policy in most developed countries.

Regarding the Road-to-Health booklet (RtHB) promotion messages 6. The RtHB is an assessment and monitoring tool for child health.

7. Only 15% of infants <6 months of age were being exclusively breastfed.

8. Two-thirds of caregivers stated that they had read the health promotion messages in the RtHB. Regarding culture-positive infections in a neonatal unit 9. Late-onset sepsis (LOS) is defined as sepsis occurring after 48 hours of life.

10. The vast majority of cases of sepsis were classified as LOS.

Regarding the RtHB 11.

The majority of healthcare workers knew how to diagnose stunting.

12. Few caregivers knew the timing of the deworming programme.

Regarding placental malaria and materno-fetal tetanus antibodies 13. Nigeria has one of the highest rates of neonatal tetanus in the world.

14. Chronic placental malaria is associated with an increased risk of babies being born seronegative for tetanus antibodies in cord blood.

Regarding obesity and cardiometabolic risk in SA children 15. Globally, 27% of urban boys (15 - 17 years of age) were overweight or obese.

16.

In assessing the prevalence of hypertension in children, the reference norms take into consideration age, sex, height and weight.

Regarding a nipple shield medication delivery system 17. The JustMilk device uses rapidly dispersible tablets to provide the medication.

18. Caregivers were not concerned about the device being functional for breastfeeding infants only.

Regarding triploidy in a live-born infant 19. Triploidy is mainly associated with third-trimester stillbirths.

20. Diandric triploidy refers to the additional haploid chromosomes being paternal in origin.

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