Prevalence and Transmission Routes of
H. pylori
Nayoung Kim
Abstract
To establish health policies for the prevention of Helicobacter pylori (H. pylori)-related diseases, observation of prevalence trends and confrmation of risk factors for H. pylori infection are important. New infections of H. pylori have been falling due to improved sanitation and better living conditions over the decades. However, its prevalence has been reported to be still higher than 50% in 2013 in Africa, Central/South America, some areas of Asia, and South/East Europe and at least twofold higher in countries with high gastric cancer (GC) incidence. In South Korea where the incidence of GC is still the highest in the world, the prevalence of H. pylori decreased to 41.5% in 2016–2017. In contrast, in Northern Europe and North America, about one-third of adults are infected. However, even in these countries, H. pylori remains highly prevalent among the immigrants coming from countries with a high prevalence of H. pylori. The lower prevalence of infection in children aged around 5–10% even in the presence of high prevalence in adults suggests a
N. Kim (*)
Department of Internal Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Gyeonggi-do, South Korea
e-mail: nakim49@snu.ac.kr; nayoungkim49@empas.com
further decline of H. pylori prevalence in the coming decades. Low socioeconomic conditions in childhood are the most important risk factors for H. pylori infection. Although the way of transmission is still unclear, interpersonal transmission appears to be the main route, especially, in the developed countries.
Keywords
Helicobacter pylori · Prevalence
Transmission · Epidemiology
1.1 Introduction
The prevalence of Helicobacter pylori (H. pylori), a cause of peptic ulcer disease, gastric adenocarcinoma, and low-grade gastric mucosaassociated lymphoid tissue (MALT) lymphoma [1], has been falling due to improved sanitation and better living conditions over the decades in most countries [2–4]. The changing epidemiology of the bacterium has been associated with a decline in the peptic ulcer disease and gastric cancer (GC) [5] but it could increase gastroesophageal refux disease and asthma, which are related to acid or immunity [6, 7]. There are many studies regarding the prevalence and risk factors of H. pylori infection, and older age was commonly considered as the main risk factor [4, 8, 9]. Adults have a continuous risk of H. pylori infection, resulting in increased seroprevalence during
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023
N. Kim (ed.), Helicobacter pylori, https://doi.org/10.1007/978-981-97-0013-4_1
lifetime as a function of age [10]. However, this does not mean that young people have a higher seroprevalence when they get older, as cross-sectional presentation does not necessarily give an accurate picture of lifetime trends. To compensate for this, there have been precious studies on lifetime trends for H. pylori seroprevalence [8, 9, 11, 12]. In this chapter, the epidemiology and risk factors of H. pylori will be summarized over the decades depending on adults and children. In addition, the transmission route will be presented according to developed and developing countries.
1.2 Prevalence of H. pylori
This chapter has received much help from two review articles, which have been published in 2014 [13, 14]. Eusebi et al. [14] have searched PubMed up to September 2013, and Peleteiro et al. [13] made a search from Medline and PubMed databases for the period of April 2013–March 2014, in which results have been well introduced in this review. In addition, I tried to update the prevalence of H. pylori, which has been published in PubMed until now. The characteristics of the populations and tests in the publications were rather variable. That is, the clinical setting such as socioeconomic status was different. The assessment of H. pylori status was done mainly through enzyme-linked immunosorbent assay (ELISA) tests to determine IgG antibody titers in serum, but few studies used urine, saliva, or urea breath test (UBT) and joint information of blood and biopsy specimens. Thus, the results of the prevalence rate of H. pylori in one country in a similar period could be at a wide range sometimes. As age is a very critical factor for the prevalence of H. pylori, the prevalence results are shown separately for adults and children in this chapter.
1.2.1 Prevalence of H. pylori in the Adults
The prevalence of H. pylori increased overall with age, decreasing in the older age groups such
as those over 60 or 70 years old in some countries (Chile [15], Ecuador [16], Japan [17], Mexico [18], Latvia [19], and South Korea [9, 20]). In the late 1990s/early 2010s, the prevalence estimates were generally higher among countries in Central/South America and Asia [13], which decreased in the late 2010s in most of these countries.
1.2.1.1 Asia Pacifc Area
As the GC incidence is highest in Korea, Japan, and China, the trend of prevalence of H. pylori in these countries was compared. All of these countries showed a decrease in the prevalence of H. pylori, but the details were slightly different. That is, the prevalence of H. pylori was 71.4% in China (35–64 years, 1989) [21], which decreased in 2000 (Table 1.1). That is, a total of 5417 healthy individuals aged between 30 and 69 years from areas of high incidence of GC in China were tested with 13C-UBT, and the prevalence of H. pylori infection was 63.4% in the 2014 report [30]. When two Chinese prevalence studies using UBT or serum IgG antibody were compared by age, the 2004–2005 Jiangsu study [28] showed a higher rate than the 2003 Beijing study [29] regardless of age. Another study included 51,299 subjects aged ≥18 years who underwent health checkups between April 2013 and June 2016 in urban city of China using H. pylori urease-IgG antibodies [31].The overall H. pylori prevalence was found to be 31.9%, with the highest prevalence in the 1950–1959 birth cohort [31] (Fig. 1.1a). Similarly, Japan showed an H. pylori prevalence rate of 70.0% among 40–79 years old in 1988–1990 [53] and 75.0% among 40–69 years old in 1990–1992 [54]. However, three subsequent Japanese prevalence studies of H. pylori (using urine antibody or serum IgG antibody) in 1992 [83], 2002–2006 [17], and 2007–2011 [84] showed a defnite decrease in prevalence rate as time regardless of age (Fig. 1.1c). In South Korea, the decrease of seroprevalence was signifcant across all age groups and in most areas of the country, especially in the age below 40 years old (Fig. 1.1b), which refects the changes from developing to developed country. That is, in a large cross-sectional nationwide multicenter
N. Kim
Table 1.1 Prevalence of H. pylori infection reported in adults
Country Year reference Setting Number
Argentina 2000 [22] B 754 (261 children and 493 adults)
Australia 2008 [23] B 2413
IgG
Serum IgG (ELISA) 15.4
2011 [24] A 1400 Serum IgG (ELISA) 15.5
Bhutan 2013 [25] A 372 Histology and RUT 73.4
2014 [26] A 244 Serum IgG (ELISA) 86
Canada 2013 [27] A 203
Gastric biopsy tested positive for the bacterium 37.9
Chile 2007 [15] A 3619 Serum IgG (ELISA) Crude 73.0/ Adjusted 73.4
China 2008 [21] A 8280 H. pylori antibody in urine (ELISA) 71.4
2008 [28] A 1371 13C expired air (UBT) and Serum IgG (ELISA) 62 2009 [29] A 1232
[30] A 5417
[31] A 51,299
Cyprus 2013 [32] A 103
Gastric biopsy, PCR (primers for urea) 39.8
Czech Republic 2006 [33] B 2509 (1234 men and 1275 women) 13C expired air (UBT) 41.7
2012 [34] B 1837 (857 men and 969 women) 13C expired air (UBT) 23.5
Ethiopia 2013 [35] A 1388
Finland 1999 [36] A 173
2001 [37] A 730 (1983)
Anti-H. pylori antibodies of all isotypes (IgG, IgM, IgA) 65.7
Serum IgG (EIA) 61.0
Serum IgG (EIA)
(1983) 618 (1995) 13.1 (1995)
2006 [38] A 336
2009 [39] A 958
France 1999 [40] A 1597
Germany 1999 [41] A 1834
2005 [42] A 6545
Iceland 2005 [43] A 96 (only women)
India 2013 [44] A 530
Serum IgG (not further specifed) 65.0 (1977–1980) 59.0 (1997–1998)
Serum IgG (EIA) 31.0 (1983) 21.0 (1989) 24.0 (1995) 19.0 (2001)
IgG in saliva (ELISA) 25.4
Serum IgG (ELISA) 39.3
Serum IgG (ELISA) 40.7
Serum IgG (ELISA) 33.0
Histology and RUT 58
2013 [45] A 530 Histology and RUT 62
Indonesia 2015 [46] A 267
Culture, histology, and RUT 22.1
2016 [47] A 193 (47 men and 146 women) 13C-UBT 15
Iran 2014 [48] B 8459 (3575 men and 4172 women)
Serum IgG (ELISA) and stool antigen 30.6–82
2016 [49] A Meta-analysis Meta-analysis (heterogenous) 62
Israel 2000 [50] A 144
Serum IgG (ELISA) 46.5 (continued)
Table 1.1 (continued)
Country Year reference Setting Number
Italy (Sardinia) 2015 [51] A 11,202 (4160 men and 7042 women)
Diagnostic method
Histology, RUT, or 13C expired air (UBT) 43.8
Japan 2005 [52] A 350 Serology 19.7
2005 [53] A 633 (349 men and 284 women) H. pylori antibody in serum (not further specifed) 70.0
2006 [54] A 511 (342 men and 169 women)
2007 [55] B 4136
Kazakhstan 2013 [56] A 835
Latvia 2012 [19] A 3564 (1218 men and 2346 women)
Lebanon 2012 [57] A 308 (144 men and 164 women)
Malaysia 2016 [58] A 275 (202 men and 153 women)
Mexico 1998 [18] B 11,605
Serum IgG (ELISA) 75.0
Serum IgG (ELISA) 54.7–67.5
Serum IgG (ELISA) 76.5
Serum IgG (ELISA) 79.2
Serum IgG (ELISA) 52.0
Serum IgG (ELISA) 44.7
Serum IgG (ELISA) 66.0 2013 [59] A 343 Serum IgG (ELISA) 52.2
Morocco 2013 [60] A 429 Histology, RUT, culture 75.5
New Zealand 2014 [23] 11–85 (A) 4463
Nigeria 2013 [61] A 125
IgG (ELISA) / histology 93.6/80.0
Oman 2013 [ 62] A 133 (100 men and 33 women) Serum IgM, IgG, and IgA (ELISA) 69.5
Portugal 2013 [63] A 2067
Republic of San Marino 1995 [64] A 2237 (1048 men and 1189 women)
Serum IgG (ELISA) 84.2
IgG (ELISA) 51.0
Saudi Arabia 2013 [65] A 456 Serum IgG (ELISA) 28.3
Singapore 2002 [66] A 261 (130 men and 131 women) Serum IgG (ELISA) 50.2
South Korea 2001 [67] A 3394 Serum IgG (ELISA) 66.9
2005 [68] A 344 (228 men and 116 women) Serum IgG (ELISA) 80.8
2007 [20] A 15,916 (8616 men and 7300 women)
2008 [69] A 25,536
2013 [8] A 10,796 (6085 men and 4711 women)
2018 [9] A 16,885 (8950 men and 7935 women)
Sweden 2003 [70] A 3502
2004 [71] A 499 (414 men and 85 women)
2011 [72] A 117
Serum IgG (ELISA) 56.0
Serum IgG (not further specifed) 59.2 Urease enzyme in biopsies (RUT)
H. pylori presence in histological examination
Serum IgG (ELISA and EIA) 54.4
Serum IgG (ELISA and EIA) 43.9
Serum IgG (ELISA) 18.0
Serum IgG (ELISA) 40.0
Serum IgG (ELISA) 35.0
2016 [73] A 388 (186 men and 202 women) EIA 15.8
Table 1.1 (continued)
Country Year reference Setting
The Netherlands
2013 [74] A 1550
2013 [75] A 6837
Taiwan 2003 [76] B 924
Turkey 2003 [77] A 675/260/148a
H. pylori antibody, and CagA antigen
Serum IgG and CagA antibodies 46
Serum IgG (ELISA) 16.7
IgG (ELISA) 13.1/30.4/44.5
2013 [78] A 4622 13C expired air (UBT) 82.5
The United Kingdom 2002 [79] B 10,118
The United States 2000 [80] A 7465 (3717 men and 3748 women)
IgG (ELISA) 13.4
IgG (ELISA) 32.5
2005 [81] B 7462 Serum IgG (ELISA) 27.1
2015 [82] A 1200
or histopathology 28.9
A adults, B both children and adults, EIA enzyme immunoassay, ELISA enzyme-linked immunosorbent assay, RUT rapid urease test, PCR polymerase chain reaction, UBT urea breath test
a Three subgroups were recruited encompassing 675 Germans (402 men, 273 women), 260 Turkish people born and raised in Germany (145 men, 115 women), and 148 Turkish people living in Turkey (91 men, 57 women)
study, more than 10,796 asymptomatic subjects without a history of H. pylori eradication were enrolled in the adult age group greater than and equal to 16 years in 2011; its prevalence was 54.4% [8]. In addition, it further decreased to 43.9% among 16,885 asymptomatic subjects without a history of H. pylori eradication in the adult age group greater than and equal to 16 years in 2016–2017 [9] (Fig. 1.1b). This result was signifcantly lower than that reported in the same country by similar surveys performed in 1993–1999 [68], 1998 [67], 2005 [20], and 2006 [69] where the prevalence of H. pylori was 80.8% [68], 66.9% [67], 59.6% [20], 59.2% [69], and 54.4% [8] respectively (Table 1.1), in the age of greater than and equal to 16 years [8]. This decreasing trend could be explained by cohort analysis [8] instead of continuous new infections over the age. All younger birth cohorts had a lower seroprevalence of H. pylori than older birth cohorts at the same age, and a decreased seroprevalence within the same birth cohorts was also accounted for in this phenomenon [8] (Fig. 1.2). The signifcant difference of H. pylori prevalence between male and female was the same until 2016–2017 [9]. The prevalence in Singapore was already not so high in 1998, at 50.2% (55–69 years) [66] (Table 1.1). In India, the preva-
lence of infection ranged from 58 to 62% in subjects with dyspeptic symptoms [44, 45], and in Kazakhstan, the prevalence of H. pylori was 76.5% among symptomatic and asymptomatic cases [56]. Similarly, in Bhutan, the infection was present in 73.4% of cases, although it was lower in the capital city, Thimphu, than in the rural areas, mainly related to sanitary conditions [25]. An even higher prevalence rate of 86% was reported from another study in the same country [26] (Table 1.1). In contrast, H. pylori prevalence in Indonesia is relatively low. One study showed that, in 193 subjects from a low-income community in Northern Jakarta, it was only 15% [47]. Similarly, another Indonesian study showed that in the 267 patients in Java, Papua, Sulawesi, Borneo, and Sumatra Islands, the overall prevalence was 22.1% [46] (Table 1.1). Orang Asli tribes in peninsula Malaysia H. pylori prevalence was 44.7% (115/275) [58] (Table 1.1).
In Oman, one of the Eastern Mediterranean regions, H. pylori prevalence was reported to be 69.5% among 15- to 50-year-olds by serology [62]. Similarly, in a population-based crosssectional survey in Turkey, a weighted overall prevalence of infection was 82.5% among more than 4600 subjects [78] (Table 1.1). Interestingly, the prevalence was lowest among individuals liv1 Prevalence and Transmission Routes
Fig. 1.1 Comparison of prevalence rate of H. pylori infection among China, Korea, and Japan. (a) Birth year and the H. pylori prevalence in China. Males: χ2 = 222.232, p-value for trends = 0.000; females: χ2 = 266.960, p-value for trends = 0.000; total: χ2 = 482.885, p-value for trends = 0.000 (Adapted from Yu et al. [31]) (b)
ing in the southern part of Turkey who usually have a citrus fruit-rich diet, as this is the major citrus fruit-growing area [78]. In the Eshraghian review article regarding H. pylori prevalence in ten studies from Iran, the overall prevalence of H. pylori infection ranged from 30.6 to 82% irrespective of time and age group [48]. In 2016,
Seroprevalence in asymptomatic subjects without a history of H. pylori eradication in 1998 [67], 2005 [20], 2011 [8], and 2016–2017 [9] in Korea. (c) Prevalence (using urine antibody or serum IgG antibody) of H. pylori in 1992 [83], 2002–2006 [17], and 2007–2011 in Japan [84]
there was a meta-analysis using 21 studies, and the H. pylori prevalence was 62%. In addition, the prevalence of H. pylori infection from the Eastern Mediterranean region (fve studies from the Kingdom of Saudi Arabia, four studies from Egypt, two studies from the United Arab Emirates, and one study from Libya, Tunisia, and
Fig. 1.2 Seroprevalence of H. pylori infection in asymptomatic subjects without a history of H. pylori eradication in birth cohort by age in Korea. Each line connects the values for the same cohort group in different age groups. For example, the frst line shows the seroprevalence of H. pylori in a birth cohort in 1972–1977 for ages 22–39 years, and the second line shows the seroprevalence of H. pylori in a birth cohort in 1966–1971 for ages 28–45 years. All younger birth cohorts at the same age have a lower seroprevalence of H. pylori than older birth cohorts (Adapted from Lim et al. [8])
Lebanon) ranged from 22 to 87.6% [48] (Table 1.1). In the case of Israel, the prevalence rate was 46.5% (mean age 18.7 years, 1986–1995) [50]. This wide variation in Middle Asia is probably related to the various age groups and methodology of H. pylori tests. In Australia, two seroprevalence rate studies performed in 2002 for 1–59 years old [23] and during 2002–2005 [24] showed 15.4% and 15.5%, respectively (Table 1.1). In the case of New Zealand where several ethnic groups live, H. pylori prevalence was highest among Pacifc people (ranging from 39 to 83%) followed by Maori (18–57%) and then European (7–35%) [85] (Table 1.1). The absolute ethnic differences in seroprevalence are decreased in subsequent cohorts, but the relative ethnic differences increased [85].
1.2.1.2 Europe
In Europe, the prevalence of H. pylori seems to be lower in Northern countries than in Southern and Eastern countries [14]. In the Netherlands, a randomly selected sample of 1550 blood donors from four different regions was tested for the presence of antibodies against H. pylori and the
CagA antigen [74]. This study where only native Dutch subjects were evaluated excluding nonEuropean immigrants reported a 31.7% prevalence of H. pylori infection (Table 1.1), with 28% of H. pylori-positive subjects carrying a CagApositive strain [74]. The seroprevalence of H. pylori declined from 48% in subjects born between 1935 and 1946 to 16% in those born between 1977 and 1987, as a likely consequence of a birth cohort effect. Moreover, the proportion of CagA-positive subjects decreased from 38% to 14% in the same age cohorts. Additionally, from the Netherlands, a population-based prospective study of a cohort of more than 6500 pregnant women was published [75]. This study found that the prevalence of H. pylori in Dutch women was 24%. In contrast, the prevalence of H. pylori in non-Dutch women was much higher, 64% [75]. Moreover, in the latter group, infected subjects born abroad (frst-generation immigrants) had a higher risk of H. pylori infection than secondgeneration immigrants [75].
In Sweden, the prevalence of H. pylori was 18.0% (17–79 years, 1995) [70], 40.0% (51–79 years, 1995–1997) [71], and 35.0% (16–40 years, 1968–2001) [72]. In addition, the
prevalence of positive H. pylori serology (EIA) decreased from 37.9% (1989) to 15.8% in Sweden [73] (Table 1.1). In Iceland, H. pylori prevalence was 33% (mean age, 27 years women; 1975–1997) [43]. When the seroprevalence was compared among randomly selected 25- to 50-year-old people from Estonia, Iceland, and Sweden, it was found to be 69%, 36%, and 11%, respectively [86]. In Finland, the proportion of pregnant women infected declined to nearly half between 1983 (30.1%) and 1995 (13.1%) [37] and between 1983 (30.1%) and 2001 (19.3%) [39] (Table 1.1). H. pylori prevalence in adults who took part in a large population-based health survey was 65.0% (1977–1980) and 59.0% (1997–1980) [38]. In addition, H. pylori prevalence in the aged people who were older than 100 years was 61.0% (mean age, 101 years and 1 month; 1991) [36].
In the Czech Republic, between 2001 and 2011, the prevalence decreased from 41.7% [33] to 23.5% [34] (Table 1.1). In the case of the United Kingdom, it was 13.4% (1–84 years, 1986–1996), lower than the other countries because the children were included [87]. In France, H. pylori prevalence in adults was 25.4% by ELISA method IgG in saliva between 1995 and 1997 [40] (Table 1.1). Similarly, the prevalence rate was 23% in Hungary (19–23 years, 1999–2000) [88] and 39.8% in Cyprus (2013) [32] (Table 1.1). In Germany, H. pylori prevalence in adults was 39.3% (18–89 years, 1987–1988) [41] and 40.7% (18–79 years, 1997–1999) [42] by ELISA tests to determine IgG antibody titers in serum (Table 1.1). In Italy, a dramatic decrease in the prevalence of infection occurred over the 19-year observation period due to the improvement in socioeconomic conditions in dyspeptic Sardinian patients from 1995 to 2013 [51]. The overall prevalence of H. pylori infection in Sardinians was 43.8% (M: 46.6% vs. F: 42.0%; p = 0.0001) [51] and 51% in San Marino (20–79 years, 1990–1991) [64] (Table 1.1). In contrast, a higher prevalence of H. pylori was reported in Portugal, where the prevalence of H. pylori infection was 84.2%, with 61.7% of strains also positive for CagA [63] (Table 1.1). In addition, based on the proportion of included subjects, the incidence rate of infec-
tion was 3.6/100 person-years, showing that Portuguese rates of H. pylori infection remain very high in Europe [63]. Similarly, Latvia also showed a higher prevalence, 79.2% in the age group of 17–99 (n = 3564) [19].
1.2.1.3 North America
In the United States, H. pylori prevalence in adults yielded small declines between 1988 and 1991 (32.7%) [80] and 1999–2000 (27.1%) [81]. In the cross-sectional study from a Veteran’s Affairs Center in the United States among patients aged 40–80 years old, the overall prevalence was 28.9%, but ethnicity was the most important factor [82] (Table 1.1). That is, H. pylori was highest among black males aged 50–59 (53.3%), followed by Hispanic males aged 60–69 (48.1%), and lowest in non-Hispanic white males aged 40–49 (8.2%) [82]. In a Canadian study where the presence of H. pylori infection was evaluated in 203 aboriginal patients with dyspepsia referred for gastroscopy, H. pylori infection was reported by histology in 37.9% of patients [27] (Table 1.1).
1.2.1.4 Latin America
In the late 1990s/early 2000s, the prevalence estimates were generally higher among countries in Central/South America (around 20 years, ranging from 30% in Argentina [22] to 70% in Mexico [18]; around 60 years, ranging from 70% in Chile [15] to 90% in Mexico [18]) (Table 1.1). However, in 2013, a study from Mexico showed a seroprevalence rate of 52.2% among 343 pregnant women living in rural areas in Mexico [59], which is a decreased rate than the previous high seroprevalence rate in this area [18] (Table 1.1). Similarly in Ecuador, a cross-sectional seroprevalence study during 2001–2002 showed a 63.1% seroprevalence rate [16], which is rather a decreased rate than the previous reports from Latin America (Table 1.1).
1.2.1.5 Africa
New data from African countries have been summarized in the same review article [14] (Table 1.1). Studies from Morocco and Ethiopia reported a prevalence of H. pylori infection of
75.5% [60] and 65.7% [35], respectively. Both studies also found a signifcant increase with age [35, 60], probably due to the birth cohort effect. A survey from patients with dyspepsia in Nigeria reported higher values: the prevalence was 80% when tested with histology and was even higher, reaching 93.6%, when serology was applied [61]. In the case of Lebanon, the seroprevalence study performed during 2008–2009 (n = 308, greater than and equal to 18 years old) showed a rate of 52.0%, which is a quite decreased rate [57] (Table 1.1).
1.2.1.6
Summary
In most countries, recent surveys yielded lower prevalence estimates in the developing countries. However, H. pylori prevalence in adults in Africa, Central/South America, Asia, and South/East Europe was still higher than 50%, and it is related to the birth cohort effect. In the developed countries, only small variations were observed, and H. pylori prevalence in adults still showed a low rate, 20–40%, but the proportion of immigrants from the high-prevalence countries affected the H. pylori prevalence in adults, suggesting that
ethnicity became a strong predictor for H. pylori in the developed countries [13, 14].
1.2.2
Prevalence of H. pylori in Children
H. pylori infection occurs mainly during childhood, especially under the age of 5 years [52, 89, 90], and H. pylori prevalence in adulthood depends on infection in childhood [11]. It is important to determine the status of the current H. pylori infection in children including prevalence, incidence, and origin of infection because such evidence can be used to expect the incidences of H. pylori-related diseases in the future and can also be incorporated into a prevention strategy for GC [13]. Recently, the H. pylori prevalence in children quickly decreased in China.
1.2.2.1 Asia
The nationwide report performed in 1998 in South Korea shows the distribution of seroprevalence according to age as Figs. 1.3 and 1.4 [67].
Fig. 1.3 Seroprevalence of H. pylori infection according to age. The seroprevalence was increased with age and was highest in people in their 40s (78.5%). The characteristic feature of our study was that the infection rate was
steeply increased in three age groups (10–12 years, 16–19 years, and people in their 20s). M months, yr years (Modifed from Kim et al. [67])
Fig. 1.4 Seroprevalence of H. pylori infection according to gender in children and adults. In adults, a signifcant difference was observed between genders.
*p < 0.05. yr years (Modifed from Kim et al. [67])
The seropositivity of infants from birth to 6 months was 24.4% and decreased to 6% in the group aged 1–3 years, suggesting the transfer of the mother’s H. pylori IgG into the fetal blood [67]. The prevalence of H. pylori infection was increased progressively and steeply with advanced age (p < 0.05) from 6% in the 1- to 3-year-old group to 78.5% in the 40- to 49-yearold group. A characteristic feature of this study was that the seroprevalence increased abruptly in 10–12 years, resulting in the overall seroprevalence of H. pylori infection among children below 16 years old, 17.2% [67] (Table 1.2). In China, a total of 1634 children and adolescents with upper gastrointestinal (GI) symptoms, who underwent gastroscopy with gastric biopsies, were evaluated for the presence of H. pylori infection [93]. The histological examination of gastric biopsies showed a 32.1% prevalence of H. pylori infection [93]. Recently, decreasing trends have been seen in China where, in Hangzhou [94], the positivity rates were 14.8%, 20.2%, and 25.8% in 3–6, 7–11, and 12–17 years age groups, respectively, with the overall prevalence decreasing from 21.6 to 17.2% between 2007 and 2014. In contrast, H. pylori prevalence in Japanese children during 2010–2011 was approximately 1.8% [99], which is much lower than that reported
in Japanese adults. In detail, H. pylori prevalence was 1.9% among 689 children aged 0–8 years in 2010 and 1.8% among 835 children aged 0–11 in 2011 [99]. No feco-conversion was observed in 430 children aged 0–8 years (170 were aged 0–4 years) who provided follow-up stool samples after 1 year [99]. In contrast, another study in a small town in Japan showed that H. pylori prevalence in children was 12.1% [98] (Table 1.2), suggesting again that different environments affect the seroprevalence in one country. Recently, the trend has been similar in Japan. That is, one study from a high GC incidence area found only 85 of 1765 (4.8%) students aged 13–15 years to be positive [100], and in another, the prevalence in school children aged 12–15 years was 3.1% [101] (Table 1.2).
In the case of Iran, a higher rate of seroprevalence in children was reported, 50.5%, with 61.7% of children positive for CagA [97] (Table 1.2). In Iceland overall, 3.4% (7/205) of the children were infected with H. pylori [96] (Table 1.2). In Latvia on the other hand, there has been no evidence of a fall in prevalence in children over the last 10 years [102]. Furthermore, the prevalence of H. pylori was high, 87.7%, and it increased with population density or employee density in Vietnam [107] (Table 1.2).
Table 1.2 Prevalence of H. pylori infection in children
Country
Belgium 2013 [91] 12–25
Brazil 2014 [92] 2–19
China 2014 [93] 1–18
[94] 3–17
Ecuador 2004 [16] 6 months–16
Germany 2003 [95] 7–20
Iceland 2017 [96] 7–9
Iran 2013 [97] 1–15
2016 [49] Children
Ireland 2005 [89] 24–48 months
[90] 0–12 months
[98] 1–18
2014 [99] 0–8/0–11
(389 boys and 449 girls)
[102]
2003 [104]
[105]
The United States 1996 [106] 6–19
Vietnam 2016 [107] 6–15
(1326 boys and 1255 girls)
(730 boys and 730 girls)
EIA enzyme immunoassay, ELISA enzyme-linked immunosorbent assay, RUT rapid urease test, PCR polymerase chain reaction, HpSA H. pylori stool antigen, UBT urea breath test
1.2.2.2 Europe
In Belgium, a study carried out on children and young adults reported a prevalence of infection of 11%, ranging from 3.2% in Belgian-born children to 60% in children born of foreign parents coming from countries with a high prevalence of H. pylori infection [91]. Similarly, the seroprevalence of German children in Germany was 13.1%, but that of Turkish children in Germany and Turkish children in Turkey was 30.4% and 44.5%, respectively [77], suggesting that seroprevalence could be different depending on race and socioeconomic status. Similarly, 7- to 9-yearold German children showed 9.4% of H. pylori prevalence by UBT [95], but a subgroup analysis showed that German children prevalence was 7.1% and that of the immigrant children was 28.2% [95] (Table 1.2). In contrast, Bastos et al. reported a very high prevalence of infection in Portuguese children [103], similar to the high 1 Prevalence and Transmission Routes of
prevalence in adults [63]. Among 13-year-old students from Porto, the prevalence was 66.2% (Table 1.2). More than half of the negative subjects were again tested after a median follow-up of 37 months, revealing an incidence rate of 4.1/100 person-years [103].
1.2.2.3
North America
In the United States, H. pylori prevalence in children and adolescents was 24.8% (6–19 years, 1988–1991) [106] (Table 1.2).
1.2.2.4
Latin America
In Brazil, Pacheco et al. compared several diagnostic tests and reported a high prevalence of 41.1% in subjects aged 2.1–19 years old [92] (Table 1.2).
1.2.2.5
Summary
H. pylori prevalence in children is very variable in the world, suggesting that still active H. pylori infection occurs in childhood in some countries.
1.3 Risk Factors of H. pylori Infection
There have been many studies regarding the risk factors of H. pylori. The most frequent independent risk factors for H. pylori infection were living in rural areas, poor sanitation, overcrowding, lower educational level, and low socioeconomic status [67]. In terms of gender, most studies reported no signifcant difference in H. pylori infection between men and women, both in adults [25, 26, 35, 45, 60, 74] and in children [67, 91, 103]. However, in South Korea, gender showed no difference in H. pylori prevalence among children, but the male gender became a risk factor in adults aged 13 years and over [8, 20, 67] (Table 1.3). In contrast, women showed higher H. pylori prevalence in Iran [48], suggesting that somehow intimate personal relationships could be related to H. pylori transmission. In terms of age, H. pylori seroprevalence became defnitely higher in the adults than in the children recently [99]. However, no signifcant association was found between infection and age in the adult pop-
Table 1.3 Multivariate analysis of risk factors for H. pylori infection in three nationwide epidemiologic studies in South Korea
Children (1–15 years)
2001
[65]
Age
Geographic areas
Drinking water (tap or well water)
Adults (≥16 years)
Age
Geographic areas
Sex (male)
Low mother’s education Crowding in childhood
Family income per month
2007
[20]
2013
[8]
2016–2017
[9]
Low economic status in childhood
Age
Geographic areas
Sex (male)
Medium or low monthly income
Medium education than high
Age
Geographic area
Sex (male)
Medium or low monthly income
Medium education than high cholesterol (240 ≥ mg/dL)
Age
Geographic area
Sex (male)
Medium monthly income vs. high (more than US $ 10,000 per month)
Medium education level vs. high (university graduates or graduates of postgraduate course
ulation [26, 44, 45, 75]. Instead, the age-specifc gradient in H. pylori prevalence reported by some studies seems to be related to a birth cohort effect [8, 35, 60, 74, 93]. Several socioeconomic factors have been associated with H. pylori infection [14]. In particular, subjects with a low socioeconomic status, which has been measured as a low family income, had a higher likelihood of carrying H. pylori infection [30, 75], especially in the childhood [65] (Table 1.3). Furthermore, an inverse association between educational level and H. pylori infection was found in the majority
1 Prevalence and Transmission Routes of H. pylori
of the studies [8, 20, 60, 63, 78]; except for two cases [30, 48], individuals with lower educational levels had a higher risk than those with higher education [14]. The same association concerning the parents’ education was also found in studies on children [91, 103], especially the mother’s education [65] (Table 1.3). Moreover, several factors related to residence have been found to be associated with the infection [14]. Indeed, living in a rural area [20, 25] and in crowded homes [26, 65, 103], and having contaminated sources of drinking water [65, 78] were risk factors for H. pylori infection (Table 1.3). Among the main lifestyle habits, smoking and alcohol consumption showed discordant results [14]. Although in most studies, there was no signifcant association with H. pylori infection [8, 20, 30, 60, 65, 75], some authors reported that regular smokers in Turkey [78] and in Saudi Arabia [108] and drinkers in Saudi Arabia [108] were at higher risk [14]. In contrast, in one study, regular alcohol drinking was a protective factor for H. pylori infection in Turkey [78]. The main subpopulations in Malaysia are Malays, Chinese, and Indians who have a H. pylori prevalence of 16.4%, 48.1%, and 61.8%, respectively. However, three Aboriginal tribes (the Orang Asli) comprise 1% of the Malaysian population and are divided into three separate tribes (the Negrito, Senoi, and ProtoMalay) and live in seven isolated settlements. A total of 275 subjects were studied, 115 (44.7%) were H. pylori positive, the highest seroprevalence being among Negrito (65.7%), and prevalence appeared to be related to age, gender, tribe, and house materials [58].
1.4 Transmission of H. pylori
It has now been established that H. pylori is mainly transmitted through person-to-person, especially in the childhood and intrafamilial transmission [55, 109–112]. However, it is not clear how the bacteria are transmitted from person to person and why the colonization does not occur in some persons, but it persists forever in others. The main route of transmission is regarded through oral–oral, fecal–oral, or gastric–oral. As
the route of transmission could be different depending on developing or developed countries because the exposed age, race, and socioeconomic status are variable in these countries [105], the transmission of H. pylori was summarized in two conditions of the developing and developed countries in this chapter.
1.4.1 Transmission of H. pylori in the Developing Countries
In the past, fecal–oral transmission was regarded as the main route in the developing countries. That is, environmental transmission, such as drinking contaminated water, could play a major role. However, as more evidence came out, fecal–oral transmission became a minor route although it remains a possible route. In addition, the transmission of H. pylori was found to be different from hepatitis A viral infection [76, 104, 113]. Instead, parental transmission has been frequently reported. Didelot et al. sequenced the genomes of 97 H. pylori isolates from 52 members of two families living in rural conditions in South Africa [79]. Transmission events were more frequent between close relatives and between individuals living in the same house. Turkish report has shown a close relationship of colonized H. pylori between the dental plaque and gastric epithelium [77]. In addition, further evidence came from Brazil that an H. pyloriinfected mother was a strong and independent risk factor (odds ratio 22.7; 95% confdence interval, 2.31–223.21) [114]. Taken together, oral–oral transmission became a more important transmission route of H. pylori infection even in developing countries. This could be related to the characteristics of H. pylori, which need good conditions such as humidity and anaerobic conditions with warmth.
1.4.2 Transmission of H. pylori in the Developed Countries
In developed countries, parental transmission has been frequently reported [99], but the transmis-
sion route is not so simple because of the immigrants from countries with a high prevalence of H. pylori. For instance, the seroprevalence of German children in Germany was 13.1%, but that of Turkish children in Germany was 30.4%, and Turkish in Turkey was 44.5% [77], suggesting that seroprevalence could be different depending on race and socioeconomic status. Similarly, among 7- to 9-year-old Germans, H. pylori prevalence was 9.4% by UBT, but a subgroup analysis showed that prevalence in German children was 7.1% and that of the immigrants’ children was 28.2% [95]. In this study, the number of family members was found to be a risk factor, and the prevalence rate was high when a family member had GI symptoms [95]. The intrafamilial transmission became strong from much evidence in the developed countries. One study that performed fngerprinting showed that among 35 families, the strain of 29 families (81%) was the same [111]. In addition, the concordance between mother and children was 56% (10 among 18 families), but none between father and children, and 22% between husband and wife, suggesting that a close relationship increases the possibility of transmission [111]. Osaki et al. performed a multilocus sequence typing DNA analysis using the stools of parents belonging to three families with a child positive for H. pylori infection [115]. The study showed an intrafamilial transmission in all selected families, with a motherto-child transmission in at least two families. Similarly, Urita et al. investigated the intrafamilial transmission of H. pylori infection by testing 838 children and their family members from a small town in Japan [98]. The H. pylori prevalence in children was 12.1%, and most risk factors were the siblings, mother, and grandmother, but the father and grandfather were not a risk factor [98]. Indeed, it seems that mothers transmit the infection through mouth secretions, using common spoons, or tasting the child’s food [14]. Grandmothers might take care of their grandchildren when mothers are at work increasing the risk of transmission. A similar report has come out from Ireland that children could be infected when the mother or siblings had H. pylori infection [89]. Taken together, H. pylori
infection in the developed countries could have characteristics of developing countries due to the immigrants from countries with a high prevalence of H. pylori. However, the oral–oral especially mother-to-child transmission is the main route.
1.5 Conclusion
Data from recent studies show that the prevalence of H. pylori infection is still high in most countries worldwide. However, the decrease is very prominent when the countries are in the transition from developing to developed countries such as South Korea and urban areas of China. H. pylori seems to be less frequent in Northern European and North American populations; however, about one-third of the adults seem to still be infected. Even in these countries, H. pylori remains highly prevalent in immigrants coming from countries with a high prevalence of H. pylori. The most frequent independent risk factors for H. pylori infection were living in rural areas, poor sanitation, overcrowding, lower educational level, and low socioeconomic status. Parent-to-child infection is thought to be the main infection route of infrequent infection for children. The lower prevalence of infection in the younger generations suggests a further decline in H. pylori prevalence in the community over the coming decades.
References
1. Egan BJ, Holmes K, O’Connor HJ, O’Morain CA. Helicobacter pylori gastritis, the unifying concept for gastric diseases. Helicobacter. 2007;12 (Suppl 2):39–44.
2. Parsonnet J. The incidence of Helicobacter pylori infection. Aliment Pharmacol Ther. 1995;9 (Suppl 2):45–51.
3. Roosendaal R, Kuipers EJ, Buitenwerf J, van Uffelen C, Meuwissen SG, van Kamp GJ, et al. Helicobacter pylori and the birth cohort effect: evidence of a continuous decrease of infection rates in childhood. Am J Gastroenterol. 1997;92:1480–2.
4. Burucoa C, Axon A. Epidemiology of Helicobacter pylori infection. Helicobacter. 2017;22 (Suppl 1):e12403.
5. Fuccio L, Eusebi LH, Bazzoli F. Gastric cancer, Helicobacter pylori infection and other risk factors. World J Gastrointest Oncol. 2010;2:342–7.
6. Sonnenberg A. Review article: historic changes of Helicobacter pylori-associated diseases. Aliment Pharmacol Ther. 2013;38:329–42.
7. Lim JH, Kim N, Lim SH, Kwon JW, Shin CM, Chang YS, et al. Inverse relationship between Helicobacter pylori infection and asthma among adults younger than 40 years: a cross-sectional study. Medicine (Baltimore). 2016;95:e2609.
8. Lim SH, Kwon JW, Kim N, Kim GH, Kang JM, Park MJ, et al. Prevalence and risk factors of Helicobacter pylori infection in Korea: nationwide multicenter study over 13 years. BMC Gastroenterol. 2013;13:104.
9. Lim SH, Kim N, Kwon JW, Kim SE, Baik GH, Lee JY, et al. Trends in the seroprevalence of Helicobacter pylori infection and its putative eradication rate over 18 years in Korea: a crosssectional nationwide multicenter study. PLoS One. 2018;13:e0204762.
10. Veldhuyzen van Zanten SJ, Pollak PT, Best LM, Bezanson GS, Marrie T. Increasing prevalence of Helicobacter pylori infection with age: continuous risk of infection in adults rather than cohort effect. J Infect Dis. 1994;169:434–7.
11. Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA. The cohort effect and Helicobacter pylori. J Infect Dis. 1993;168:219–21.
12. Kosunen TU, Aromaa A, Knekt P, Salomaa A, Rautelin H, Lohi P, et al. Helicobacter antibodies in 1973 and 1994 in the adult population of Vammala, Finland. Epidemiol Infect. 1997;119:29–34.
13. Peleteiro B, Bastos A, Ferro A, Lunet N. Prevalence of Helicobacter pylori infection worldwide: a systematic review of studies with national coverage. Dig Dis Sci. 2014;59:1698–709.
14. Eusebi LH, Zagari RM, Bazzoli F. Epidemiology of Helicobacter pylori infection. Helicobacter. 2014;19 (Suppl 1):1–5.
15. Ferreccio C, Rollán A, Harris PR, Serrano C, Gederlini A, Margozzini P, et al. Gastric cancer is related to early Helicobacter pylori infection in a high-prevalence country. Cancer Epidemiol Biomarkers Prev. 2007;16:662–7.
16. Gómez NA, Salvador A, Vargas PE, Zapatier JA, Alvarez J. Seroprevalence of Helicobacter pylori among the child population of Ecuador. Rev Gastroenterol Peru. 2004;24:230–3.
17. Shiota S, Murakami K, Fujioka T, Yamaoka Y. Population-based strategies for Helicobacter pylori-associated disease management: a Japanese perspective. Expert Rev Gastroenterol Hepatol. 2010;4:149–56.
18. Torres J, Leal-Herrera Y, Perez-Perez G, Gomez A, Camorlinga-Ponce M, Cedillo-Rivera R, et al. A community-based seroepidemiologic study of Helicobacter pylori infection in Mexico. J Infect Dis. 1998;178:1089–94.
19. Leja M, Cine E, Rudzite D, Vilkoite I, Huttunen T, Daugule I, et al. Prevalence of Helicobacter pylori infection and atrophic gastritis in Latvia. Eur J Gastroenterol Hepatol. 2012;24:1410–7.
20. Yim JY, Kim N, Choi SH, Kim YS, Cho KR, Kim SS, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter. 2007;12:333–40.
21. Wang X, Terry P, Yan H. Stomach cancer in 67 Chinese counties: evidence of interaction between salt consumption and Helicobacter pylori infection. Asia Pac J Clin Nutr. 2008;17:644–50.
22. Olmos JA, Rios H, Higa R. Prevalence of Helicobacter pylori infection in Argentina: results of a nationwide epidemiologic study. Argentinean HP Epidemiologic Study Group. J Clin Gastroenterol. 2000;31:33–7.
23. Moujaber T, MacIntyre CR, Backhouse J, Gidding H, Quinn H, Gilbert GL. The seroepidemiology of Helicobacter pylori infection in Australia. Int J Infect Dis. 2008;12:500–4.
24. Pandeya N, Whiteman DC, Australian Cancer Study. Prevalence and determinants of Helicobacter pylori sero-positivity in the Australian adult community. J Gastroenterol Hepatol. 2011;26:1283–9.
25. Vilaichone RK, Mahachai V, Shiota S, Uchida T, Ratanachu-ek T, Tshering L, et al. Extremely high prevalence of Helicobacter pylori infection in Bhutan. World J Gastroenterol. 2013;19:2806–10.
26. Dorji D, Dendup T, Malaty HM, Wangchuk K, Yangzom D, Richter JM. Epidemiology of Helicobacter pylori in Bhutan: the role of environment and geographic location. Helicobacter. 2014;19:69–73.
27. Sethi A, Chaudhuri M, Kelly L, Hopman W. Prevalence of Helicobacter pylori in a frst nations population in northwestern Ontario. Can Fam Physician. 2013;59:e182–7.
28. Shi R, Xu S, Zhang H, Ding Y, Sun G, Huang X, et al. Prevalence and risk factors for Helicobacter pylori infection in Chinese populations. Helicobacter. 2008;13:157–65.
29. Cheng H, Hu FL, Zhang L, Yang G, Ma J, Hu J, et al. Prevalence of Helicobacter pylori infection and identifcation of risk factors in rural and urban Beijing, China. Helicobacter. 2009;14:128–33.
30. Zhu Y, Zhou X, Wu J, Su J, Zhang G. Risk factors and prevalence of Helicobacter pylori infection in persistent high incidence area of gastric carcinoma in Yangzhong city. Gastroenterol Res Pract. 2014;2014:481365.
31. Yu X, Yang X, Yang T, Dong Q, Wang L, Feng L. Decreasing prevalence of Helicobacter pylori according to birth cohorts in urban China. Turk J Gastroenterol. 2017;28:94–7.
32. Krashias G, Bashiardes S, Potamitou A, Potamitis GS, Christodoulou C. Prevalence of Helicobacter pylori cagA and vacA genes in Cypriot patients. J Infect Dev Ctries. 2013;7:642–50.
33. Bures J, Kopácová M, Koupil I, Vorísek V, Rejchrt S, Beránek M, et al. Epidemiology of Helicobacter 1
pylori infection in the Czech Republic. Helicobacter. 2006;11:56–65.
34. Bures J, Kopáčová M, Koupil I, Seifert B, Skodová Fendrichová M, et al. Signifcant decrease in prevalence of Helicobacter pylori in the Czech Republic. World J Gastroenterol. 2012;18:4412–8.
35. Mathewos B, Moges B, Dagnew M. Seroprevalence and trend of Helicobacter pylori infection in Gondar University Hospital among dyspeptic patients, Gondar, North West Ethiopia. BMC Res Notes. 2013;6:346.
36. Rehnberg-Laiho L, Louhija J, Rautelin H, Jusufovic J, Tilvis R, Miettinen A, et al. Helicobacter antibodies in Finnish centenarians. J Gerontol A Biol Sci Med Sci. 1999;54:M400–3.
37. Rehnberg-Laiho L, Rautelin H, Koskela P, Sarna S, Pukkala E, Aromaa A, et al. Decreasing prevalence of Helicobacter antibodies in Finland, with reference to the decreasing incidence of gastric cancer. Epidemiol Infect. 2001;126:37–42.
38. Salomaa-Räsänen A, Kosunen TU, Karjalainen J, Aromaa A, Knekt P, Sarna S, et al. IgA antibodies in persisting Helicobacter pylori infection in Finnish adults. Clin Microbiol Infect. 2006;12:236–40.
39. Seiskari T, Viskari H, Kaila M, Haapala AM, Koskela P, Hyöty H. Time trends in allergic sensitisation and Helicobacter pylori prevalence in Finnish pregnant women. Int Arch Allergy Immunol. 2009;150:83–8.
40. Broutet N, Sarasqueta AM, Cantet F, Lethuaire D, Mégraud F. Is there a link between the variation in gastric cancer mortality and differences in Helicobacter pylori prevalence in different regions of France? Gastroenterol Clin Biol. 1999;23:754–60.
41. Brenner H, Berg G, Frohlich M, Boeing H, Koenig W. Chronic infection with Helicobacter pylori does not provoke major systemic infammation in healthy adults: results from a large population-based study. Atherosclerosis. 1999;147:399–403.
42. Kuepper-Nybelen J, Thefeld W, Rothenbacher D, Brenner H. Patterns of alcohol consumption and Helicobacter pylori infection: results of a population-based study from Germany among 6545 adults. Aliment Pharmacol Ther. 2005;21:57–64.
43. Lehtinen M, Ogmundsdottir HM, Bloigu A, Hakulinen T, Hemminki E, Gudnadottir M, et al. Associations between three types of maternal bacterial infection and risk of leukemia in the offspring. Am J Epidemiol. 2005;162:662–7.
44. Sodhi JS, Javid G, Zargar SA, Tufail S, Shah A, Khan BA, et al. Prevalence of Helicobacter pylori infection and the effect of its eradication on symptoms of functional dyspepsia in Kashmir, India. J Gastroenterol Hepatol. 2013;28:808–13.
45. Adlekha S, Chadha T, Krishnan P, Sumangala B. Prevalence of Helicobacter pylori infection among patients undergoing upper gastrointestinal endoscopy in a medical college hospital in Kerala, India. Ann Med Health Sci Res. 2013;3:559–63.
46. Syam AF, Miftahussurur M, Makmun D, Nusi IA, Zain LH, Zulkhairi, Akil F, et al. Risk factors and prevalence of Helicobacter pylori in fve largest islands of Indonesia: a preliminary study. PLoS One. 2015;10:e0140186.
47. Goto Y, Syam AF, Darnindro N, Hapsari FPC. Risk factors for and prevalence of Helicobacter pylori infection among healthy inhabitants in northern Jakarta, Indonesia. Asian Pac J Cancer Prev. 2016;17:4469–75.
48. Eshraghian A. Epidemiology of Helicobacter pylori infection among the healthy population in Iran and countries of the Eastern Mediterranean Region: a systematic review of prevalence and risk factors. World J Gastroenterol. 2014;20:17618–25.
49. Moosazadeh M, Lankarani KB, Afshari M. Metaanalysis of the prevalence of Helicobacter pylori infection among children and adults of Iran. Int J Prev Med. 2016;7:48.
50. Gdalevich M, Cohen D, Ashkenazi I, Mimouni D, Shpilberg O, Kark JD. Helicobacter pylori infection and subsequent peptic duodenal disease among young adults. Int J Epidemiol. 2000;29:592–5.
51. Dore MP, Marras G, Rocchi C, Soro S, Loria MF, Bassotti G, et al. Changing prevalence of Helicobacter pylori infection and peptic ulcer among dyspeptic Sardinian patients. Intern Emerg Med. 2015;10:787–94.
52. Konno M, Fujii N, Yokota S, Sato K, Takahashi M, Sato K, et al. Five-year follow-up study of motherto-child transmission of Helicobacter pylori infection detected by a random amplifed polymorphic DNA fngerprinting method. J Clin Microbiol. 2005;43:2246–50.
53. Kikuchi S, Yagyu K, Obata Y, Yingsong L, Yatsuya H, Hoshiyama Y, et al. Serum pepsinogen values and Helicobacter pylori status among control subjects of a nested case-control study in the JACC study. J Epidemiol. 2005;15 (Suppl 2):S126–33.
54. Sasazuki S, Inoue M, Iwasaki M, Otani T, Yamamoto S, Ikeda S, et al. Effect of Helicobacter pylori infection combined with cagA and pepsinogen status on gastric cancer development among Japanese men and women: a nested case-control study. Cancer Epidemiol Biomarkers Prev. 2006;15:1341–7.
55. Raymond J, Thiberg JM, Chevalier C, Kalach N, Bergeret M, Labigne A, et al. Genetic and transmission analysis of Helicobacter pylori strains within a family. Emerg Infect Dis. 2004;10:1816–21.
56. Benberin V, Bektayeva R, Karabayeva R, Lebedev A, Akemeyeva K, Paloheimo L, et al. Prevalence of H. pylori infection and atrophic gastritis among symptomatic and dyspeptic adults in Kazakhstan. A hospital-based screening study using a panel of serum biomarkers. Anticancer Res. 2013;33:4595–602.
57. Naja F, Nasreddine L, Hwalla N, Moghames P, Shoaib H, Fatfat M, et al. Association of H. pylori infection with insulin resistance and metabolic
N. Kim
syndrome among Lebanese adults. Helicobacter. 2012;17:444–51.
58. Thevakumar K, Chandren JR, Perez-Perez GI, Chua EG, Teh LK, Salleh MZ, et al. Assessment of risk and sero-prevalence of Helicobacter pylori colonization among remote Orang Asli tribes in peninsula Malaysia. PLoS One. 2016;11:e0159830.
59. Alvarado-Esquivel C. Seroepidemiology of Helicobacter pylori infection in pregnant women in rural Durango. Int J Biomed Sci. 2013;9:224–9.
60. Benajah DA, Lahbabi M, Alaoui S, El Rhazi K, El Abkari M, Nejjari C, et al. Prevalence of Helicobacter pylori and its recurrence after successful eradication in a developing nation (Morocco). Clin Res Hepatol Gastroenterol. 2013;37:519–26.
61. Olokoba AB, Gashau W, Bwala S, Adamu A, Salawu FK. Helicobacter pylori infection in Nigerians with dyspepsia. Ghana Med J. 2013;47:79–81.
62. Al-Balushi MS, Al-Busaidi JZ, Al-Daihani MS, Shafeeq MO, Hasson SS. Sero-prevalence of Helicobacter pylori infection among asymptomatic healthy Omani blood donors. Asia Pac J Trop Dis. 2013;3:146–9.
63. Bastos J, Peleteiro B, Barros R, Alves L, Severo M, de Fátima PM, et al. Sociodemographic determinants of prevalence and incidence of Helicobacter pylori infection in Portuguese adults. Helicobacter. 2013;18:413–22.
64. Gasbarrini G, Pretolani S, Bonvicini F, Gatto MR, Tonelli E, Mégraud F, et al. A population based study of Helicobacter pylori infection in a European country: the San Marino study. Relations with gastrointestinal diseases. Gut. 1995;36:838–44.
65. Kim N, Kim JG, Kim JH, Kim HY, Kim SW, Kim JJ, et al. Risk factors of Helicobacter pylori infection in asymptomatic Korean population. Korean J Med. 2000;59:376–87.
66. Chua TS, Fock KM, Chan YH, Dhamodaran S, Sim CS, Ng TM, et al. Seroreactivity to 19.5-kDa antigen in combination with absence of seroreactivity to 35-kDa antigen is associated with an increased risk of gastric adenocarcinoma. Helicobacter. 2002;7:257–64.
67. Kim JH, Kim HY, Kim NY, Kim SW, Kim JG, Kim JJ, et al. Seroepidemiological study of Helicobacter pylori infection in asymptomatic people in South Korea. J Gastroenterol Hepatol. 2001;16:969–75.
68. Shin A, Shin HR, Kang D, Park SK, Kim CS, Yoo KY. A nested case-control study of the association of Helicobacter pylori infection with gastric adenocarcinoma in Korea. Br J Cancer. 2005;92:1273–5.
69. Kim N, Lee SW, Cho SI, Park CG, Yang CH, Kim HS, et al. The prevalence of and risk factors for erosive oesophagitis and non-erosive refux disease: a nationwide multicentre prospective study in Korea. Aliment Pharmacol Ther. 2008;27:173–85.
70. Sörberg M, Nyrén O, Granström M. Unexpected decrease with age of Helicobacter pylori serop-
revalence among Swedish blood donors. J Clin Microbiol. 2003;41:4038–42.
71. Ye W, Held M, Lagergren J, Engstrand L, Blot WJ, McLaughlin JK, et al. Helicobacter pylori infection and gastric atrophy: risk of adenocarcinoma and squamous-cell carcinoma of the esophagus and adenocarcinoma of the gastric cardia. J Natl Cancer Inst. 2004;96:388–96.
72. Persson C, Jia Y, Pettersson H, Dillner J, Nyrén O, Ye W. H. pylori seropositivity before age 40 and subsequent risk of stomach cancer: a glimpse of the true relationship? PLoS One. 2011;6:e17404.
73. Agréus L, Hellström PL, Talley NJ, Wallner B, Forsberg A, Vieth M, et al. A towards a healthy stomach? Helicobacter pylori prevalence has dramatically decreased over 23 years in adults in a Swedish community. United European Gastroenterol J. 2016;4:686–96.
74. van Blankenstein M, van Vuuren AJ, Looman CW, Ouwendijk M, Kuipers EJ. The prevalence of Helicobacter pylori infection in the Netherlands. Scand J Gastroenterol. 2013;48:794–800.
75. den Hollander WJ, Holster IL, den Hoed CM, van Deurzen F, van Vuuren AJ, Jaddoe VW, et al. Ethnicity is a strong predictor for Helicobacter pylori infection in young women in a multiethnic European city. J Gastroenterol Hepatol. 2013;28:1705–11.
76. Maherzi A, Bouaziz Abed A, Fendri C, Oubich F, Koubaa C, Fauchere JL, et al. Helicobacter pylori infection: prospective study for asymptomatic Tunisian children. Arch Pediatr. 2003;10:204–7.
77. Porsch-Ozcürümez M, Doppl W, Hardt PD, SchnellKretschmer H, Tuncay M, Akinci A, et al. Impact of migration on Helicobacter pylori seroprevalence in the offspring of Turkish immigrants in Germany. Turk J Pediatr. 2003;45:203–8.
78. Ozaydin N, Turkyilmaz SA, Cali S. Prevalence and risk factors of Helicobacter pylori in Turkey: a nationally-representative, cross-sectional, screening with the 13C-Urea breath test. BMC Public Health. 2013;13:1215.
79. Didelot X, Nell S, Yang I, Woltemate S, van der Merwe S, Suerbaum S. Genomic evolution and transmission of Helicobacter pylori in two South African families. Proc Natl Acad Sci U S A. 2013;110:13880–5.
80. Everhart JE, Kruszon-Moran D, Perez-Perez GI, Tralka TS, McQuillan G. Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis. 2000;181:1359–63.
81. Cardenas VM, Mulla ZD, Ortiz M, Graham DY. Iron defciency and Helicobacter pylori infection in the United States. Am J Epidemiol. 2006;163:127–34.
82. Nguyen T, Ramsey D, Graham D, Shaib Y, Shiota S, Velez M, et al. The prevalence of Helicobacter pylori 1
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In the States of Maine and Massachusetts, this species is best known by the name of “Butter-boat-billed Coot.” The gunners of Long Island and New Jersey call it the Black Sea Duck. It is often seen along the coast of South Carolina, where my friend J B Has met with it. The Surf Duck is a powerful swimmer and an expert diver. It is frequently observed fishing at the depth of several fathoms, and it floats buoyantly among the surf or the raging billows, where it seems as unconcerned as if it were on the most tranquil waters. It rises on wing, however, with considerable difficulty, and in this respect resembles the Velvet Duck; but when once fairly under way, it flies with rapidity and to a great distance, passing close to the water during heavy gales, but at the height of forty or fifty yards in calm and pleasant weather. It is an uncommonly shy bird, and therefore difficult to be obtained, unless shot at while on wing, or
when asleep, and as it were at anchor on our bays, or near the shore, for it dives as suddenly as the Velvet and Scoter Ducks, eluding even the best percussion-locked guns. The female, which was killed as she flew off from the nest, uttered a rough uncouth guttural cry, somewhat resembling that of the Goosander on similar occasions; and I have never heard any other sound from either sex.
The migration of the Surf Ducks eastward from our Southern coast, begins at a very early season, as in the beginning of March none are to be seen in the New Orleans markets. When I was at Eastport in Maine, on the 7th of May 1833, they were all proceeding eastward. How far up the St Lawrence they advance in winter I have not learned, but they must give a decided preference to the waters of that noble stream, if I may judge by the vast numbers which I saw apparently coming from them as we approached the Labrador coast. I have never seen this species on any fresh-water lake or river, in any part of the interior, and therefore consider it as truly a marine duck.
During their stay with us, they are always seen in considerable numbers together, and, unless perhaps during the breeding season, they seem to be gregarious; for even during their travels northward they always move in large and compact bodies. When I was at Newfoundland, I was assured that they breed there in considerable numbers on the lakes of the interior. My friend Professor M , of Pictou, however informs me that none are seen in Nova Scotia in summer. A gentleman of Boston, with whom I once crossed the Atlantic, assured me that the species is extremely abundant on the northern shores of the Pacific Ocean, and about the mouth of Mackenzie’s River. Doctor T mentions it as being also found on the Columbia. It appears that a single specimen of the Surf Duck has been procured on the shores of Great Britain; and this has induced the ornithologists of that country to introduce it as a constituent of its Fauna.
In all the individuals which I have examined, I have found the stomach to contain fish of different kinds, several species of shellfish, and quantities of gravel and sand, some of the fragments being of large size. Their flesh is tough, rank, and fishy, so as to be scarcely fit for food.
In the young males, in the month of September, the whole upper plumage is mottled with darkish-brown and greyish-white, the latter colour margining most of the feathers. The neck has a considerable extent of dull greyish-white, spread over two or three inches, and approaching toward the cheeks and throat. This colour disappears about the beginning of January, when they become of a more uniform dark tint, the upper part of the head brownish-black, without any white spot; there is a patch of brownish-white at the base of the upper mandible on each side; another of an oblong form over the ear, and on the nape are elongated greyish-white marks; the bill and feet dusky green, the iris brown.
A , Linn Syst Nat vol i p 201 Lath Ind Ornith vol ii p. 847.
B or S D , Wils Amer Ornith vol viii p 49, pl 67, fig 2
F , Ch. Bonaparte, Synopsis of Birds of the United States, p. 389.
O , Richards and Swains Faun Bor Amer vol ii p 449.
B or S D , Nuttall, Manual, vol ii p 416
Adult Male. Plate CCCXVII. Fig. 1.
Bill about the length of the head, very broad, as deep as broad at the base, depressed towards the end, which is rounded. Upper mandible with the dorsal outline convex and descending, before the nostrils concave, on the unguis convex and declinate; the ridge broad and
convex at the base; the sides at the base erect, bulging, and very broad, towards the end convex, the edges soft, with about 30 internal lamellæ, for two-thirds from the base they are nearly parallel and straight, but towards the end ascending, the unguis very large, somewhat triangular and rounded. Lower mandible flattened, with the angle long and rather narrow, the dorsal line slightly convex, the edges with about 35 lamellæ. Nostrils submedial, elliptical, large, pervious, near the ridge.
Head large, oblong, flattened above. Eyes of moderate size. Neck short and thick. Body large and much depressed. Feet short, placed rather far behind; tarsus very short, compressed, having anteriorly in its whole length a series of small scutella, and above the outer toe a partial series, the rest covered with reticular angular scales. Hind toe small, with a free membrane beneath; anterior toes nearly double the length of the tarsus, connected by reticulated membranes having a sinus on their free margins, the inner with a lobed marginal membrane, the outer with a thick margin, the third and fourth about equal and longest. Claws small, that of the first toe very small and curved, of the middle toe largest, with a dilated inner edge, of the rest slender, all rather obtuse.
Plumage soft, dense, blended, and glossy. Feathers on the head and neck of a velvety texture. Wings rather short, narrow, and pointed; primary quills curved, strong, tapering, and pointed, the first longest, the second little shorter, the rest rapidly graduated; secondaries broad and rounded, the inner elongated and tapering. Tail very short, narrow, wedge-shaped, of fourteen stiff, narrow, pointed feathers.
Upper mandible with a nearly square black patch at the base, margined with orange, unless in front, where there is a patch of bluish-white extending to near the nostrils, prominent part over the nostrils deep reddish-orange, becoming lighter towards the unguis, and shaded into rich yellow towards the margins; the unguis dingy greyish-yellow; lower mandible flesh-coloured, unguis darker. Iris
bright yellowish-white. Tarsi and toes orange-red, the webs dusky tinged with green; claws black. The plumage is of a deep black, glossed with blue. On the top of the head, between the eyes, is a roundish patch of white, and on the nape a larger patch of an elongated form.
Length to end of tail 20 inches, to end of wings 18, to end of claws 22; extent of wings 33 1/2; bill from the angle in front 1 1/2; from the prominence at the base 2 1/2; along the edge of lower mandible 2 5/12; wing from flexure 9 3/4; tail 3 3/4; tarsus 1 7/12; first toe and claw 11/12; outer toe, and claw 2 1/4; middle, toe and claw, 1/2/12 longer. Weight 2 lb. 7 oz.
Adult Female. Plate CCCXVII. Fig. 2.
Bill greenish-black; iris as in the male; feet yellowish-orange, webs greyish-dusky, claws black. The general colour of the plumage is brownish-black; darker on the top of the head, the back, wings, and tail; on the breast and sides the feathers edged with dull greyishwhite.
Length to end of tail 19 inches, to end of wings 15 3/4, to end of claws 18; extent of wings 31 1/2; wing from flexure 8 3/4; tarsus 1 5/8; middle toe 2 3/4, hind toe 9/12. Weight 2 lb. 2 oz.
In an adult Male, the tongue is 1 inch 9 twelfths long, has numerous conical papillæ at the base, is deeply grooved along the middle, has two lateral series of bristles, and terminates in a thin rounded lobe, 2 twelfths long. On the middle line of the upper mandible are about ten short conical papillæ, and on each of its margins about 35 lamellæ; on the lower an equal number. The heart is 1 inch 8 twelfths long, 1 inch 2 twelfths broad. The œsophagus, 8 1/2 inches long, is wide, its diameter at the upper part being 1 inch, towards the middle of the
neck 1 inch and a quarter. The proventriculus is 1 1/2 inch long; its glandules cylindrical, 1 1/2 twelfths in length, and, as in all other ducks, arranged so as to form a complete belt. The stomach is a powerful gizzard of a roundish form, 1 inch 10 twelfths long, 1 inch 10 twelfths broad, its lateral muscles very large, the right 10 twelfths thick, the left 9 twelfths. In the stomach were various small bivalve shells and much gravel. The cuticular lining longitudinally rugous; the grinding plates 3/4 inch in diameter. The intestine, 5 feet 7 inches in length, has an average diameter of 6 twelfths. The rectum is 7 1/2 inches long, 8 twelfths in diameter. Of the cœca one is 3 inches 4 twelfths long, cylindrical, obtuse, 2 1/2 twelfths in diameter, the other 4 1/2 inches long.
The aperture of the glottis is 8 twelfths long, with numerous minute papillæ behind. The trachea presents the same structure as that of the Velvet Duck. Its upper rings, to the number of 9, are very narrow, and continuous with a large bony expansion, 7 twelfths long, and 8 twelfths broad. Beyond this part its diameter is 5 twelfths, gradually diminishes to 3 twelfths about the middle, then enlarges to 5 twelfths. In this part the number of rings is 78. Then comes a roundish or transversely elliptical enlargement, 1 inch 2 twelfths in breadth, 9 twelfths in length, convex before, slightly concave behind, and composed of about 12 united rings. The trachea then contracts to 4 twelfths and presently enlarges to form the inferior larynx, which is large, ossified, but symmetrical. In this space there are 6 distinct rings, and 10 united. The entire length of the trachea is 7 1/2 inches, its rings are all osseous and strong. The contractor muscles are very strong, pass along the sides of the lower dilatation, on which are given off the cleido-tracheals, then continue to the commencement of the inferior larynx, where the sterno-tracheals come off. The bronchial half-rings 25, unossified.
The cavity of the nose is very large, being 2 inches long, 1/2 inch in diameter at the lower part, continued narrow in front over the dilatation causing the external protuberance of the base of the bill. The olfactory nerves are of moderate size; the maxillary branches of the fifth pair very large.
AMERICAN AVOSET.
R A , G .
PLATE CCCXVIII. A M , Y W .
The fact of this curious bird’s breeding in the interior of our country accidentally became known to me in June 1814. I was at the time travelling on horseback from Henderson to Vincennes in the State of Indiana. As I approached a large shallow pond in the neighbourhood of the latter town, I was struck by the sight of several Avosets hovering over the margins and islets of the pond, and although it was late, and I was both fatigued and hungry, I could not resist the temptation of endeavouring to find the cause of their being so far from the sea. Leaving my horse at liberty, I walked toward the pond, when, on being at once assailed by four of the birds, I felt confident that they had nests, and that their mates were either sitting or tending their young. The pond, which was about two hundred yards in length, and half as wide, was surrounded by tall bulrushes extending to some distance from the margin. Near its centre were several islets, eight or ten yards in length, and disposed in a line. Having made my way through the rushes, I found the water only a few inches deep; but the mud reached above my knees, as I carefully advanced towards the nearest island. The four birds kept up a constant noise, remained on wing, and at times dived through the air until close to me, evincing their displeasure at my intrusion. My desire to shoot them however was restrained by my anxiety to
study their habits as closely as possible; and as soon as I had searched the different inlets, and found three nests with eggs, and a female with her brood, I returned to my horse, and proceeded to Vincennes, about two miles distant. Next morning at sunrise I was snugly concealed amongst the rushes, with a fair view of the whole pond. In about an hour the male birds ceased to fly over me, and betook themselves to their ordinary occupations, when I noted the following particulars.
On alighting, whether on the water or on the ground, the American Avoset keeps its wings raised until it has fairly settled. If in the water, it stands a few minutes balancing its head and neck, somewhat in the manner of the Tell-tale Godwit. After this it stalks about searching for food, or runs after it, sometimes swimming for a yard or so while passing from one shallow to another, or wading up to its body, with the wings partially raised. Sometimes they would enter among the rushes, and disappear for several minutes. They kept apart, but crossed each other’s path in hundreds of ways, all perfectly silent, and without shewing the least symptom of enmity towards each other, although whenever a Sandpiper came near, they would instantly give chase to it. On several occasions, when I purposely sent forth a loud shrill whistle without stirring, they would suddenly cease from their rambling, raise up their body and neck, emit each two or three notes, and remain several minutes on the alert, after which they would fly to their nests, and then return. They search for food precisely in the manner of the Roseate Spoonbill, moving their heads to and fro sideways, while their bill is passing through the soft mud; and in many instances, when the water was deeper, they would immerse their whole head and a portion of the neck, as the Spoonbill and Red-breasted Snipe are wont to do. When, on the contrary, they pursued aquatic insects, such as swim on the surface, they ran after them, and on getting up to them, suddenly seized them by thrusting the lower mandible beneath them, while the other was raised a good
way above the surface, much in the manner of the Black Shearwater, which however performs this act on wing. They were also expert at catching flying insects, after which they ran with partially expanded wings.
I watched them as they were thus engaged about an hour, when they all flew to the islets where the females were, emitting louder notes than usual. The different pairs seemed to congratulate each other, using various curious gestures; and presently those which had been sitting left the task to their mates and betook themselves to the water, when they washed, shook their wings and tail, as if either heated or tormented by insects, and then proceeded to search for food in the manner above described. Now, Reader, wait a few moments until I eat my humble breakfast.
About eleven o’clock the heat had become intense, and the Avosets gave up their search, each retiring to a different part of the pond, where, after pluming themselves, they drew their heads close to their shoulders, and remained perfectly still, as if asleep, for about an hour, when they shook themselves simultaneously, took to wing, and rising to the height of thirty or forty yards, flew off towards the waters of the Wabash River.
I was now desirous of seeing one of the sitting birds on its nest, and leaving my hiding place, slowly, and as silently as possible, proceeded toward the nearest islet on which I knew a nest to be, having the evening before, to mark the precise spot, broken some of the weeds, which were now withered by the heat of the sun. You, good Reader, will not, I am sure, think me prolix; but as some less considerate persons may allege that I am tediously so, I must tell them here that no student of Nature ever was, or ever can be, too particular while thus marking the precise situation of a bird’s nest. Indeed, I myself have lost many nests by being less attentive. After this short but valuable lecture, you and I will do our best to approach the sitting bird unseen by it. Although a person can advance but
slowly when wading through mud and water knee-deep, it does not take much time to get over forty or fifty yards, and thus I was soon on the small island where the Avoset was comfortably seated on her nest. Softly and on all four I crawled toward the spot, panting with heat and anxiety. Now, Reader, I am actually within three feet of the unheeding creature, peeping at her through the tall grasses. Lovely bird! how innocent, how unsuspecting, and yet how near to thine enemy, albeit he be an admirer of thy race! There she sits on her eggs, her head almost mournfully sunk among the plumage, and her eyes, unanimated by the sight of her mate, half closed, as if she dreamed of future scenes. Her legs are bent beneath her in the usual manner. I have seen this, and I am content. Now she observes me, poor thing, and off she scrambles,—running, tumbling, and at last rising on wing, emitting her clicking notes of grief and anxiety, which none but an inconsiderate or callous-hearted person could hear without sympathizing with her.
The alarm is sounded, the disturbed bird is floundering hither and thither over the pool, now lying on the surface as if ready to die, now limping to induce me to pursue her and abandon her eggs. Alas, poor bird! Until that day I was not aware that gregarious birds, on emitting cries of alarm, after having been scared from their nest, could induce other incubating individuals to leave their eggs also, and join in attempting to save the colony. But so it was with the Avosets, and the other two sitters immediately rose on wing and flew directly at me, while the one with the four younglings betook herself to the water, and waded quickly off, followed by her brood, which paddled along swimming, to my astonishment, as well as ducklings of the same size.
How far such cries as those of the Avoset may be heard by birds of the same species I cannot tell; but this I know, that the individuals which had gone toward the Wabash reappeared in a few minutes after I had disturbed the first bird, and hovered over me. But now,
having, as I thought, obtained all desirable knowledge of these birds, I shot down five of them, among which I unfortunately found three females.
The nests were placed among the tallest grasses, and were entirely composed of the same materials, but dried, and apparently of a former year’s growth. There was not a twig of any kind about them. The inner nest was about five inches in diameter, and lined with fine prairie grass, different from that found on the islets of the pond, and about two inches in depth, over a bed having a thickness of an inch and a half. The islets did not seem to be liable to inundation, and none of the nests exhibited any appearance of having been increased in elevation since the commencement of incubation, as was the case with those described by W . Like those of most waders, the eggs were four in number, and placed with the small ends together. They measured two inches in length, one inch and three-eighths in their greatest breadth, and were, exactly as W tells us, “of a dull olive colour, marked with large irregular blotches of black, and with others of a fainter tint.” To this I have to add, that they are pear-shaped and smooth. As to the time of hatching, I know nothing.
Having made my notes, and picked up the dead birds, I carefully waded through the rushes three times around the whole pond, but, being without my dog, failed in discovering the young brood or their mother. I visited the place twice the following day, again waded round the pond, and searched all the islets, but without success: not a single Avoset was to be seen; and I am persuaded that the mother of the four younglings had removed them elsewhere.
Since that time my opportunities of meeting with the American Avoset have been few. On the 7th of November 1819, while searching for rare birds a few miles from New Orleans, I shot one which I found by itself on the margin of Bayou St John. It was a young male, of which I merely took the measurements and
description. It was very thin, and had probably been unable to proceed farther south. Its stomach contained only two small freshwater snails and a bit of stone. In May 1829, I saw three of these birds at Great Egg Harbour, but found no nests, although those of the Long-legged Avoset of W were not uncommon. My friend J B considers them as rare in South Carolina, where, however, he has occasionally seen some on the gravelly shores of the sea islands.
On the 16th of April 1837, my good friend Captain N C , of the United States Revenue Cutter the Campbell, on board of which I then was, shot three individuals of this species on an immense sand-bar, intersected by pools, about twelve miles from Derniere Island on the Gulf of Mexico, and brought them to me in perfect order. They were larger, and perhaps handsomer, than any that I have seen; and had been killed out of a flock of five while feeding. He saw several large flocks on the same grounds, and assured me that the only note they emitted was a single whistle. He also observed their manner of feeding, which he represented as similar to that described above.
My friend T N says in a note, that he “found this species breeding on the islands of shallow ponds throughout the Rocky Mountains about midsummer. They exhibited great fear and clamour at the approach of the party, but no nests were found, they being then under march.” Dr R states, that it is abundant on the Saskatchewan Plains, where it frequents shallow lakes, and feeds on insects and small fresh water crustacea.
The flight of the American Avoset resembles that of the Himantopus nigricollis. Both these birds pass through the air as if bent on removing to a great distance, much in the manner of the Tell-tale Godwit, or with an easy, rather swift and continued flight, the legs and neck fully extended. When plunging towards an intruder, it at times comes downwards, and passes by you, with the speed of an
arrow from a bow, but usually in moving off again, it suffers its legs to hang considerably. I have never seen one of them exhibit the bending and tremulous motions of the legs spoken of by writers, even when raised suddenly from the nest; and I think that I am equally safe in saying, that the bill has never been drawn from a fresh specimen, or before it has undergone a curvature, which it does not shew when the bird is alive. The notes of this bird resemble the syllable click, sometimes repeated in a very hurried manner, especially under alarm.
R A , Lath Ind Ornith vol ii p 787 Ch Bonaparte, Synopsis of Birds of United States, p 394
A A , R A , Wils. Amer. Ornith. vol. vii. p 126, pl 63, fig 2
R A , Richards. and Swains., Fauna Bor.-Amer. vol. ii. p. 375.
A A , Nuttall, Manual, vol ii p 74
Adult Male. Plate CCCXVIII. Fig. 1.
Bill more than twice the length of the head, very slender, much depressed, tapering to a point, and slightly recurved. Upper mandible, with the dorsal line straight for half its length, then a little curved upwards, and at the tip slightly decurved, the ridge broad and flattened, the edges rather thick, the nasal groove rather long and very narrow. Nostrils linear, basal, pervious. Lower mandible with the angle long and very narrow, the dorsal line slightly curved upwards, the point very slender, extremely thin and a little curved upwards.
Head small, rounded above, rather compressed. Neck long. Body compact, ovate. Legs very long, slender; tibia elongated, bare for half its length, and reticulated; tarsus very long, compressed, reticulated with hexagonal scales; toes rather short, the first extremely small; outer toe a little longer than inner; the anterior toes
connected by webs of which the anterior margin is deeply concave, the lateral toes thickly margined. Claws very small, compressed, rather blunt.
Plumage soft and blended. Wings long, of moderate breadth, pointed; primaries straightish, tapering, the first longest, the rest rapidly graduated; secondaries broad, incurved, the outer rounded, the rest becoming pointed, the inner elongated and tapering. Tail short, even, of twelve rather narrow, rounded feathers.
Bill black. Iris bright carmine. Feet light blue, webs flesh-coloured towards their edges, claws black. Head, neck, and fore part of breast, reddish-buff, the parts around the base of the bill and the eye, nearly white. The back is white; but on its fore part is a longitudinal band of brownish-black elongated feathers on each side, and the inner scapulars are of the same colour, the outer and the anterior edge of the wing being white. The wing brownish-black, with a broad band of white formed by the tips of the secondary coverts, four of the inner secondaries, and the basal part, with the inner webs and outer edges of the rest. The under parts white, excepting some of the primary quills and some of their coverts, which are greyishbrown.
Length to end of tail 18 inches, to end of wings 18 1/2, to end of claws 23 1/2 extent of wings 30 5/8; wing from flexure 9 1/2; tail 3 1/2; bill along the ridge 3 3/4; bare part of the tibia 2 3/12; tarsus 3 5/8; hind toe and claw 3/12; middle toe and claw 1 10/12; breadth of foot extended 2 5/8. Weight 16 3/4 oz.
The Female is similar to the male, but somewhat smaller. Young in winter. Plate CCCXVIII. Fig. 2.
The young in winter is similar to the adult, but with the head and neck white, the dark colours of a browner tint.
Length to end of tail 18 inches, to end of wings 18 1/2; extent of wings 30 1/2. Weight 13 oz.
In structure the Avosets are similar to the Numenii and Totani. In an adult female the tongue is very short in proportion to the length of the bill, being only 1 3/4 inch long, slightly emarginate at the base with a few conical papillæ, slender, tapering to a point, horny on the back, and flattened above. On the palate are two longitudinal series of blunt papillæ. The posterior aperture of the nares is linear, 10 twelfths long, papillate on the edges. The œsophagus is 7 inches and 9 twelfths long, inclines to the right side, and when the neck is bent becomes posterior at the middle, as in the Herons and other long-necked birds; its diameter 5 twelfths at the upper part, dilated to 8 twelfths previous to its entrance into the thorax. The proventriculus is 1 inch long and 7 twelfths in diameter; its glandules cylindrical, 1 twelfth long. The stomach is a gizzard of moderate strength, oblong, 1 1/2 inch in length, 10 twelfths in breadth, its right lateral muscle 4 twelfths thick. Its contents were remains of small shells. Its inner membrane of moderate thickness, hard, longitudinally rugous, and deeply tinged with red. The intestine is 3 feet long, and 4 twelfths in diameter; the rectum 2 inches long; of the cœca one is 2 3/4 inches long, the other 2 1/4, their diameter 2 twelfths.
In another individual the intestine is 3 feet 9 inches long; one of the cœca 2 3/4 inches, the other 3; the stomach 1 1/2 by 1 1/12. Its contents small shell-fish and fragments of quartz.
The trachea is 6 1/2 inches long; its rings extremely thin and unossified, 140 in number, its diameter 3 1/4 twelfths, nearly uniform throughout, but rather narrower in the middle. The lateral muscles are very thin. The bronchi are short, of about 10 rings.
