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RELATIONSHIP OF GROWTH RATE AND ANTHROPOMETRIC MEASUREMENTS WITH MENARCHE IN A LONGITUDINAL STUDY Maria Aparecida Zanetti Passos 1 | Mauro Fisberg 1 | Roberta de Lucena Ferretti 1 | Gérson Luiz Moraes Ferrari 1,2 | Isa de Pádua Cintra Sampaio 1 1
Setor de Medicina do Adolescente (Centro de Atendimento e Apoio ao Adolescente – CAAA) do Departamento de Pediatria da Universidade Federal de São Paulo – UNIFESP/EPM Cotia – São Paulo – 06716260 - Brasil. 2 Centro de Estudos do Laboratório de Aptidão Física de São Caetano do Sul –CELAFISCS Cotia – São Paulo – 06716260 - Brasil. ABSTRACT The objective of this longitudinal study was to analyze the relationship of growth rate and anthropometric measurements with menarche. A total of 301 girls were divided into three groups: G1 (before menarche), G2 (menarche ≤4 months before or after data collection), and G3 (menarche >4 months before or after data collection). Height, body weight, and body mass index (BMI) were collected and their relationships with the following variables were analyzed: age, waist and hip circumferences (WC and HC), percentage of body fat (%BF), sexual maturation, and menarche date. At baseline, 31.2% of the girls were in Tanner stage M2 (61.4% had already menstruated). At the end of the study, 40.5% of the girls were in Tanner stage M4, and 89.4% had already menstruated. The mean age at menarche was 11.8 years, and 23.8% and 11.1% of the sample were overweight and obese, respectively. The mean height and body weight at baseline and end of study were 152.2 vs 158.9 cm, and 47.3 vs 54.7 Kg, respectively. G1 (23.2%) and G2 (23.4%) had similar mean %BF. G1 presented the greatest anthropometric changes, especially in WC (4.9 cm) and HC (6.3 cm). Girls in the pubertal stages M1 to M3 had the highest growth rates. This study stresses the importance of monitoring adolescents continuously to promote a healthy body weight and optimal timing of pubertal events. Keywords: Menarche, Height, Adolescents.
Introduction Height gain during adolescence can be assessed by monitoring growth during puberty. Such growth is defined as the pubertal growth spurt. It consists of a phase of accelerated height gain, a growth rate peak in girls of approximately 8 to 9 centimeters per year, followed by growth rate deceleration. Adolescents gain 20% of their final height and 50% of their final weight, but weight gain occurs roughly six months after the peak growth rate, which coincides with menarche. This is due to a relationship between skeletal maturation and menarche, in different systems, during puberty. The greatest characteristic of this phase is the great variability of its onset and related events, which are not only related to the pubertal growth spurt but also to sexual maturation1-5. Although menarche is a late phenomenon in the pubertal process, some parents only realize at this time that their daughters are no longer children. On this occasion, concerned with the girl’s final height, parents tend to ask about their daughter’s growth potential6. Tanner7 states that height gain is pretty much the same regardless of age at menarche, but Diez et al.6 found a negative and moderate correlation between growth rate and age at menarche. According to Castilhos et al., shorter girls at menarche grow more after it, in an attempt to catch up with their growth potential8, because when they mature earlier, they do not only grow more, but do so for longer, until they reach their final height9. In other words, girls with delayed maturation have a shorter growth spurt than girls who mature earlier. To compensate, they gain some centimeters before the growth spurt, and after the growth spurt they continue growing for a
longer period8. Regarding the nutritional status of these girls, studies have found that the mean age at menarche is lower in overweight and obese adolescents10-12. Hence, the understanding of this phenomenon requires a longitudinal study to analyze how growth rate and anthropometric measurements relate to menarche.
Material and Methods Study population and school sampling The study students were part of the population-based study “Evolução da estatura de adolescentes e sua relação com indicadores nutricionais: Um estudo longitudinal” (Height changes in adolescents and its relationship with nutritional indicators: a longitudinal study). The study used a non-probabilistic, intentional, convenience sample because the Teaching Department of the City of São Paulo requested that these girls be located near the adolescent care sector to minimize transportation problems if they needed specific care from our team. The sample included three public schools (one in the Southern region, one downtown, and one in the Western region) after the principal authorized the study, which was conducted from 2010 to 2013. The participants should be aged 10 to 15 years and could not be participating in a weight loss program, have chronic or mental diseases, be taking pharmaceuticals that affect body composition, be pregnant, or be breastfeeding. The longitudinal study selected 837 male and female adolescents enrolled in grades five through eight after parental or guardian consent. However, 280 adolescents were lost because of incomplete data (they participated only in two
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data collection visits and chose to drop out of the study, moved to another state, or changed schools). The final sample consisted of 557 adolescents who attended all data collection visits during the three-year study. Since this study aimed to assess menarche, only girls were included, specifically 301 girls aged 10 to 15 years. This study complied with the ethical principles for human research established by resolution CNS 196/96 and approved by the Research Ethics Committee of the Graduate and Research Council of the Federal University of São Paulo under protocol number Nº0803/09.
Anthropometric variables The anthropometric data were collected at 12-month intervals during three consecutive years, either in the first or second semester of each year. The measurements were supervised by a professor and two graduate students, who were responsible for training the data collection team. The team consisted of dietitians (students of an adolescent-specialization class), trained to note the measurements in the three study occasions in separate forms so that they could not see the previous measurements, thereby avoiding memory bias. Height (m) was measured by a stadiometer of the brand Seca mounted to the wall at a right angle to the floor, as recommended by Jelliffe13. Body mass (Kg) was measured by a portable digital scale of the brand Seca, with capacity of 150kg. The adolescents, wearing light clothes, were asked to stand erect and barefoot on the scale platform, with the arms hanging by the sides13,14. Body mass index (BMI, kg/m2) was calculated, and the BMI-for-age z-score was classified as recommended by the World Health Organization (WHO) as follows: (Z-score < -2 = underweight; -2 ≤ Z-score ≤ + 1 = normal weight; +1 < z-score ≤ +2 = overweight; +2 > z-score = obesity)15. Waist circumference (WC) was measured by an inelastic tape measure of the brand Seca at the midpoint between the lowest costal margin and the iliac crest16. Hip circumference (HC) was measured at the highest circumference of the gluteal region by the same tape measure16. The waist-to-hip ratio (WHR) was given by the equation: WHR = waist circumference (cm) / hip circumference (cm)17. Body fat was determined by measuring the triceps and subscapular skinfold thicknesses three consecutive times using the standard technique and a scientific caliper of the brand Cescorf, which has an accuracy of 0.1 mm. The percentage of body fat (%BF) was given by the equations of Slaughter et al.18 and classified as recommended by Lohman19. Growth rate (GR) was verified as follows: first, the GR between each assessment was calculated (first to second, and second to third); then the general GR was calculated using these two measurements. GR in centimeters per year was given by calculating the difference in height between the assessments and dividing the difference by the interval between assessments in years.
Sexual maturation and age at menarche Sexual maturation was determined by asking the girls to assess the development of their breasts (M1, M2, M3, M4, M5) using the criteria established by Tanner20 and validated for our
environment by Matsudo & Matsudo21. Adolescents in M1 were grouped as prepubertal, those in M2 to M4, as pubertal, and those in M5, as postpubertal. The adolescents were asked about the occurrence of menarche (yes or no), and those who answered yes were asked about the menarche date (recall method) to assess the interval between menarche and data collection. The girls were then classified as follows: G1 – no menarche; G2 – menarche ≤ four months before or after data collection; and G3 – menarche > four months before or after data collection. Age at menarche was classified as follows:
Lower age limit (<9.57 years): Mean – 2 SD = 11.71 – 2 x 1.07 = 9.57
Upper age limit (>13.85 years): Mean + 2 SD = 11.71 + 2 x 1.07 = 13.85
Appropriate age at menarche in this study: Between ages 9.57 and 13.85 years
Adolescent sample selection The sample size was based on the statistic of a sample population of adolescents respecting the same study inclusion and exclusion criteria, same city, and same coordinators in both projects22-26. The mean height and standard deviation were 156.64 ± 9.68 cm. Thus, a statistical error of approximately 2.0% was used to calculate sample size, which resulted in N=541 subjects, but this study would enroll only girls. This sample size enables accurate statistical analyses, guaranteed by the central limit theorem and law of large numbers27.
Statistical analysis The absolute frequency (n) and percentage (%) of the categorical variables (sex, sexual maturation, menarche, and nutritional status) and the mean, standard deviation, median, minimum, maximum, and quartile of the numerical variables (height, body mass, BMI, WC, HC, WHR, and age) were tabulated to describe the sample’s profile according to the study variables. The chi-square test or Fisher’s exact test (for expected values smaller than 5) compared the categorical variables between groups. The Mann-Whitney test and the Kruskal-Wallis test compared the numerical variables between two and three groups, respectively, since the variables were not normally distributed. The McNemar, Bowker, Friedman, and Wilcoxon tests compared the variables between the three assessments. The Pearson’s or Spearman’s correlation coefficients were also calculated for the quantitative variables28. Repeated measures analysis of variance (repeated measures ANOVA) compared the longitudinal measurements between the three assessments and between groups, the Tukey test compared the groups in each assessment, and profile analysis analyzed the parameters between assessments in each group. Since the variables did not have a normal distribution, they were rank transformed for the analyses29. The data were treated by the software SAS (Statistical Analysis System, version 9.3) using a significance level of 5% (p<0.05)28,30.
Results
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A total of 301 girls aged 10 to 15 years were divided into three groups and followed for three years. The groups were G1 (n=33 girls without menarche during the study period); G2 (n=88 girls who had menarche ≤ four months before or after data collection); and G3 (n=180 girls who had menarche > four months before or after data collection). The study collected anthropometric measurements (height, weight, WC, and HC) and calculated the BMI and WHR by age, sexual maturation, and age at menarche.
A 1982 study called “Pelotas Birth Cohort” analyzed a subsample of individuals and found an association between rapid growth and overweight/obesity in adolescence 33. This finding could partly explain the mechanism that associates rapid growth and age at menarche.
At baseline, 31.23% of the sample self-reported being in Tanner stage M2 based on their breast development; 38.13% were 10 to 11 years old; 30.90% were 12 years old; and 30.8% were 13 to 15 years old; 7.31% were prepubertal; 82.73% were pubertal; and 9.97% were postpubertal; and 61.4% had already menstruated. At the end of the study, 40.53% were in M4; 41.87% were 11 to 13 years old; 33.22% were 14 years old; 24.91% were 15 to 17 years old; 0.33% were prepubertal; 72.43% were pubertal; 27.24 were postpubertal; and 89.4% had already menstruated.
Developed and developing countries found a trend towards lower age at menarche secondary to better quality of life and nutrition35,36.
The mean age at menarche was 11.79 (1.12) years, 12.31% of the girls did not have menarche during the study period, 86.19% had menarche before age 13.85 years, and 1.49% had menarche after age 13.85% years.
In this study the mean age at menarche was 11.71 (0.97) years, which is within the age range 10-13 years but lower than the means found for Bangladesh (15.8), Congo (13.83), Ghana (13.98), Tanzania (15.21), Senegal (16.1), United States (12.8), Greece (12), and Italy (12.2)41.
Most girls (62.23%) were normal weight, 23.80% were overweight, and 11.07% were obese. Of the 10% who did not menstruate during the study, 61.62% were normal weight, 12.12% were overweight, and 24.24% were obese. In G1 63.64%, 12.12%, and 15.15% of the girls were normal weight, overweight, and obese, respectively. In G2 63.64%, 25%, and 7.95% of the girls were normal weight, overweight, and obese, respectively. In G3 59.44%, 26.11%, and 10% of the girls were normal weight, overweight, and obese, respectively. The mean values of the anthropometric variables of G1 differed significantly from those of G2 and G3 during the study period. G2 and G3 variables did not differ significantly. Growth rate and weight gain were positively correlated with age at menarche (r=0.37351; p<0.0001) and (r=0.21597; p<0.0004), respectively.
Discussion The objective of this longitudinal study was to assess the relationship of growth rate and anthropometric measurements with menarche. As expected, the height, weight, and BMI of the study sample increased between baseline and end of study. BMI increased by 1.3 units, demonstrating that the girls gained more weight than height. The growth rate of the girls did not differ markedly between study years (3.8 cm in the first year, 3.5 cm in the second year, and 3.7 cm in the third year, Table 1), indicating that the group as a whole presented homogeneous growth rate during the study period. WC increased by a mean of 1.5 cm, while HC increased by a mean of 5.1 cm during the study three years. The prevalence of excess weight (overweight and obesity) in the study adolescents was very high (34.87%), but when they were divided into three groups, G1 had a very high prevalence of obesity (15.15%) compared with G2 (7.95%) and G3 (10%), which may stem from a possible increase in body fat in preparation for menarche31,32.
These girls tend to have more body fat, and a relationship between more body fat and the risk of early menarche has been reported34. According to Dunger et al.34, high leptin after rapid weight gain during childhood can trigger early puberty.
Proper age at menarche of the study sample ranged from 9.57 to 13.85 years; only 2.61% and 0.75% of the girls had the menarche before age 9.57 years and after age 13.85 years, respectively. Lower age at menarche has been identified as a risk factor for depression in adolescence37, insulin resistance38, breast cancer39, obesity, and metabolic diseases40.
The initiation and progression of puberty can be affected by the environment and by the data collection procedures used by different studies, which may affect result interpretation and comparison, requiring careful analyses. Nonetheless, studies have found a trend towards lower age at menarche in the last 20 years, especially in the United States42 and Asia43,44, and this trend may be associated with higher obesity rates in girls45,46. Within the study groups, all anthropometric variables differed significantly between the three assessments, demonstrating the influence of sexual maturation on body structures (Table 2). Data from a representative sample of North-American children and adolescents aged 8 to 14 years who participated in the Third National Health and Nutrition Examination Survey (NHANES III) conducted between 1988 and 1994 found that early sexual maturation was positively associated with the risk of overweight (OR=1.59 [1.05 – 2.42]) and obesity (OR=1.96 [1.11 – 3.47]) in girls47,48. Portuguese adolescents aged 10 to 15 years who matured early were two times more likely to be overweight than those who did not mature early49. African-American girls who matured early were 3.6 times more likely to become overweight than those who matured in the normal age range or late50. A longitudinal study of 1605 Norwegian adolescents found that the combination of central adiposity and early sexual maturation increased girls’ risk of overweight at the end of adolescence51. The study girls who had not yet menstruated at baseline had a mean age of 10.85 years, and at the end of the study, a mean age of 12.63 years. As mentioned earlier, 12.31% of the adolescents had not menstruated during the study period, and since age at menarche ranged from 10 to 13 years, they were very close to the upper age limit for menarche in this study. Other variables
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that indicate proper physiological conditions for menarche will be discussed next. Although the mechanisms involved in the association between obesity and age at menarche are not well known, endocrine factors may affect the rates of sexual maturation rate and fat gain52. According to Firsch & McArthur53, girls need to reach a minimum weight of 47.8 Kg to menstruate, and more importantly, they should have a percentage of body fat of at least 23.7%. In the third assessment, the group G1 had a mean percentage of body fat of 23.19%, which was very similar to the 23.36% found for G2 at baseline. Although this value is very close to that suggested by Firsch & McArthur53, it was slightly lower for our population, which may indicate that 23.4% of body fat based on skinfold thicknesses is adequate for menarche. In the third assessment, group G1 had a mean weight of 45.87 kg, which is 2 kg less than the weight suggested by Firsch & McArthur53. On the other hand, G2 had a much higher mean weight at baseline (54.14 kg) than that suggested by those authors. Therefore, although the percentage of body fat was slightly smaller, higher body weight could also promote menarche. Em relação ao peso das adolescentes dos grupos G1 e G2, verificou-se que houve um ganho de peso entre a primeira e última avaliação de 8,06 Kg no grupo G1 e de 11,3 Kg no G3, valores superiores aos encontrados em outros estudos31,54,55. Regarding the weight of the adolescents in groups G1 and G2, the group G1 gained 8.06 Kg between the first and last assessment, and group G3, 11.3 Kg, which are higher than the weight gains reported by other studies31,54,55. Group G1 experienced the greatest anthropometric changes between baseline and the last assessment, especially in WC (4.91cm) and HC (6.28 cm) (Table 3). In our understanding these circumferences increase considerably during puberty but not so much after menarche. Increases in these anthropometric measurements may be a predictor of menarche, because this was exactly the group that had not menstruated during the study. It is during puberty that the hormonal changes responsible for the appearance of secondary characters and physical changes occur. Chronological age alone cannot predict an adolescent’s degree of pubertal development, as pubertal development is influenced by intrinsic and environmental factors. Therefore, early or late pubertal development may change growth rate and body composition56.
followed by 23.5% in the second tertile and 13% in the third tertile. Although this analysis took into account sexual maturation at baseline, these results were expected, demonstrating that girls in Tanner stages M1, M2, and M3 are closer to the growth spurt phase, and hence have higher growth rates than girls in Tanner stages M4 and M5, which occur after the growth spurt. It is possible that some girls remained in the same pubertal stage during the study, but these results clearly represent what was expected according to the literature47-49,51. Longitudinal studies are very important for monitoring body changes, especially during adolescence. This study followed a representative sample of girls aged 10 to 15 years at baseline and verified the relationship between menarche and anthropometric variables. The occurrence of menarche in the study population is associated with a %BF of roughly 23.4%, and higher weight may be positively associated with menarche when the percentage of fat is slightly below expected. WC and HC were the anthropometric variables that increased significantly before menarche, and the mean age at menarche was 11.71 years. As expected, girls in the first stages of sexual maturation (M1 to M3) presented higher growth rates, and adolescents who had had menstruation for longer periods presented smaller changes in their anthropometric variables, including height gain. In this sense we reinforce the importance of a multidisciplinary team to continuously monitor adolescents in order to promote proper nutritional status and the occurrence of pubertal events within the optimal age range.
Conclusion This longitudinal study verified the growth rate of adolescents by age, stages of adolescence, and sexual maturation, important variables for the nutritional status classification of this population. The greatest future perspective is to continue the study trying to eliminate all possible sources of bias in order to obtain increasingly better and more accurate results, which allows the scientific community to reproduce the data and especially, use the data in clinical practice, improving the quality of care and research for this population group.
Conflicts of interest The authors have no conflicts of interest.
Acknowledgments
Groups G1 and G2 grew basically twice as much as group G3, demonstrating that they were closer to the growth spurt period.
The authors thank the Pediatrics Department of the Federal University of São Paulo and the study participants, parents, guardians, teachers, and coordinators of the municipal schools of the city of São Paulo.
The group that had not menstruated (G1) had lower anthropometric means during the study period than the other groups (G2 and G3) (Table 4). G2 and G3 had similar height, although weight was a bit lower in G2, so G3 had slightly higher BMI. The group G3 also had higher WC, HC, and %BF.
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Table 5 shows GR by tertiles. GR in the highest tertile was 25.90 cm, followed by 8.53 cm in the second tertile and 3.66 cm in the first tertile. A total of 87% of the girls in Tanner stages M1 to M3 were in the third GR tertile, followed by 76.5% in the second tertile and 44.5% in the first tertile. On the other hand, 55.6% of the girls in M4 and M5 were in the first tertile,
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Research Paper
E-ISSN NO : 2455-295X | VOLUME : 2 | ISSUE : 12 | DEC 2016
Table 1 – Baseline and final (1 and 3) means, standard deviations, first and third quartiles, and medians of the anthropometric variables, age at menarche, and growth rate [initial (1), intermediate (2), and final (3)]. Coleta 1 Idade 3 1 Estatura 3 1 Peso 3 1 Variáveis IMC 3 Antropo 1 métricas CC 3 1 CQ 3 1 RCQ 3 1 Velocidade de 2 Crescimento 3 Idade Menarca
Média 11,90 13,80 152,20 158,90 47,30 54,70 20,20 21,50 68,90 70,40 85,00 90,10 0,80 0,70 3,80 3,50 3,70 11,71
DP 1,06 1,10 7,90 6,10 11,90 11,80 4,30 4,30 10,10 10,10 11,20 10,40 0,10 3,10 3,40 2,60 1,00
Q1 Mediana 11,10 12,00 12,90 13,80 147,40 153,10 155,30 159,00 39,00 46,00 46,60 53,30 17,00 19,60 18,30 20,80 61,10 68,50 63,00 69,00 78,00 84,40 84,00 89,00 0,70 0,80 0,50 0,70 1,10 3,30 1,20 2,50 1,60 3,20 10,90 11,80
Q3 12,70 14,50 157,30 162,50 54,20 61,00 22,80 23,60 75,10 75,60 93,00 96,50 0,80 0,80 5,90 4,80 5,30 12,40
Table 4: Comparison of the means and standard deviations of the anthropometric variables of the three groups during the study period. Variables
G1
G2
G3
p-value1
Age (years)
11.78 (0.53) †
12.70 (0.92)
13.27 (1.04)
0.037
Height (cm)
148.54 (7.67) *†
156.29 (6.48)
156.85 (6.09)
0.002
BM (kg)
41.47 (4.68) *†
50.43 (10.83)
53.58 (11.67)
0.003
BMI (kg/m2)
18.64 (4.68) *†
20.51 (3.83)
21.69 (4.48)
0.031
WC (cm)
63.78 (11.16) *†
68.72 (9.55)
70.59 (9.84)
0.012
HC (cm)
76.74 (10.85) *†
86.38 (8.86)
89.00 (10.13)
0.004
WHR
0.83 (0.14) *†
0.78 (0.06)
0.79 (0.28)
0.029
%BF
22.10 (9.81) *†
24.71 (7.43)
25.94 (7.48)
0.005
G1: no menarche; G2: menarche ≤ four months before or after data collection; G3: menarche > four months before or after data collection; BM: body mass; BMI: body mass index; WC: waist circumference; HC: hip circumference; WHR: waist-to-hip ratio; %BF: percentage of body fat. 1: repeated measures analysis of variance; 2: Tukey’s multiple comparison test; p<0.05: * to compare G1 and G2; p<0.05: † to compare G1 and G3; p<0,05: # to compare G2 and G3.
Table 5 – Frequency of Tanner breast stage at baseline by growth rate in tertiles.
1st GR tertile Value = 3.66 Table 3: Baseline and final anthropometric variables. Variables
G1
G2
G3
Height (cm)
10.55
9.80
5.46
BM (Kg)
8.63
8.06
6.85
2
BMI (kg/m )
1.64
1.34
1.19
WC (cm)
4.91
1.29
0.94
HC (cm)
6.28
3.07
2.38
WHR
0.01
-0.02
-0.02
%BF
3.83
2.66
3.34
G1: no menarche; G2: menarche ≤ months before or after data collection; G3: menarche > four months before or after data collection; BM: body mass; BMI: body mass index; WC: waist circumference; HC: hip circumference; WHR: waist-to-hip ratio; %BF: percentage of body fat.
2nd GR tertile Value = 8.53
3rd GR tertile
Total
Value = 25.90
M1(%)
1 (1%)
5 (4.9%)
16 (16%)
M2(%)
6 (6.1%)
36 (35.3%)
52 (52%)
M3(%)
37 (37.4%)
37 (36.3%)
19 (19%)
M4(%)
35 (35.4%)
20 (19.6%)
7 (7%)
M5(%)
20 (20.2%)
4 (3.9%)
6 (6%)
Total
99 (100%)
102 (100%)
100 (100%)
Mean age (years)
12.83 (0.87)
11.93 (0.86)
11.21 (0.75)
22 (7.3%) 94 (31.2%) 93 (30.9%) 62 (20.6%) 30 (10%) 301 (100%)
GR: growth rate. Chi-square for categorical data: p<0.001; One-way analysis of variance to compare age means: p<0.001. Difference between all groups with p<0.001.
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