Annals of Human Biology
ISSN: 0301-4460 (Print) 1464-5033 (Online) Journal homepage: http://www.tandfonline.com/loi/iahb20
Secular trends of growth and pubertal maturation of school children in Southern Thailand Somchit Jaruratanasirikul & Hutcha Sriplung To cite this article: Somchit Jaruratanasirikul & Hutcha Sriplung (2015) Secular trends of growth and pubertal maturation of school children in Southern Thailand, Annals of Human Biology, 42:5, 447-454, DOI: 10.3109/03014460.2014.955057 To link to this article: http://dx.doi.org/10.3109/03014460.2014.955057
Published online: 18 Sep 2014.
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Date: 05 November 2015, At: 19:48
http://informahealthcare.com/ahb ISSN: 0301-4460 (print), 1464-5033 (electronic) Ann Hum Biol, 2015; 42(5): 447–454 ! 2014 Informa UK Ltd. DOI: 10.3109/03014460.2014.955057
RESEARCH PAPER
Secular trends of growth and pubertal maturation of school children in Southern Thailand Somchit Jaruratanasirikul1 and Hutcha Sriplung2 Department of Pediatrics and 2Epidemiology Unit, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, Thailand
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Abstract
Keywords
Background: In Thailand, studies of growth date back to 1975, but there have been no studies examining any trends in increasing/decreasing growth. Aim: To determine if there have been any secular trends of increasing/decreasing growth and/ or ages at puberty in Thai children. Methods: In 2012, a cross-sectional study of growth was conducted in 3460 children. The median heights and weights and the ages of pubertal maturation were compared with previous studies. Correlations between the secular trends and the health statistics indicators were calculated. Results: From 1975–2012, the median final height of boys and girls had increased by 1.32 and 0.86 cm/decade and weight by 2.49 and 1.76 kg/decade, respectively. In girls, the age at thelarche and menarche had declined by 0.39 and 0.12 years/decade, respectively. In boys, the age at testicular enlargement Tanner II had declined by 0.15 years/decade. Increased physical growth was positively correlated to life expectancy, per capita income and prevalence of overweight/obesity was negatively correlated to prevalence of malnutrition and under-five mortality rate. Conclusion: The positive secular trend towards an increase in growth and a decline in the age at onset of puberty of Thai children is correlated with improvements in overall living conditions in Thailand.
Growth, puberty, secular trend
Introduction Physical growth and pubertal maturation are influenced by several factors including genetic factors (ethnicity, genes controlling bone growth and hormonal regulation) and environmental factors (socioeconomic circumstances, psychosocial situation and nutritional status) and have been widely used as indicators for health status and socioeconomic conditions. Tanner (1999), one of the pioneers of auxology, stated that growth is ‘‘a mirror of conditions of society’’. The concept of ‘‘secular trend’’ for growth and pubertal maturation of the children in a population describes the changes in physical development from one generation to the next. The secular trends of growth and the ages at puberty can be positive (increased growth and earlier age at puberty compared to children of the same age of earlier generations), stable or negative. Studies worldwide have demonstrated a sensitivity of these secular trends to changes in living standards (socio-economic and socio-hygienic conditions) both over time and between different social groups (Hauspie
Correspondence: Somchit Jaruratanasirikul, Department of Pediatrics, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, 90110, Thailand. Tel: 66-074-429618. Fax: 66-074-429618. E-mail: [email protected]
History Received 20 October 2013 Revised 11 July 2014 Accepted 4 August 2014 Published online 18 September 2014
et al., 1997). Several studies from both European and Asian countries have shown a secular trend towards an increase in physical growth and a decline in the median age of pubertal development in both boys and girls. In Thailand, we now have available six studies of physical growth with the age at puberty dating back to 1975: 1975 (Chavalittamrong & Vathakanon, 1978), 1984 (Khanjanasthiti et al., 1987), 1986 (Chavalittamrong & Tantiwongse, 1987), 1994 (Jaruratanasirikul et al., 1996), 1996 (Nutrition Division, Ministry of Public Health, Thailand, 1999) and 2012 (Jaruratanasirikul et al., 2014a,b). It was our purpose with this study to assess changes in physical growth and age at puberty in Thai children and to determine whether there has been a positive, stable or negative secular trend during the last 37 years by comparing our new data with data from the previous studies examining growth and ages at puberty in Thailand. The objective was to assess whether, if a positive secular trend was found, there was any correlation between this trend and the relevant health statistics indicators of the Thai population during this time period of 37 years.
Methods A cross-sectional study was conducted from June 2011 to March 2012 in nine primary and secondary schools in
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Hat Yai municipality, the largest urban centre in southern Thailand, which were randomly selected by probability proportional to size sampling (from a total of 29 schools). Children, boys and girls, aged 6–20 years were asked to participate. A general physical examination including a pubertal assessment was performed in all participants, following the same protocol as in earlier related studies (Jaruratanasirikul et al., 2014a,b). In brief, standing height was measured using a portable stadiometer and weight with a digital electronic scale. Heights and weights of the children were calculated into seven standard percentile lines: 3rd, 10th, 25th, 50th, 75th, 90th and 97th. In the girls, breast development and pubic hair development were assessed by a female paediatric endocrinologist and, in the boys, testicular enlargement and pubic hair development were assessed by one of the two male paediatricians who had been specially trained in pubertal assessment by a paediatric endocrinologist. Testicular enlargement was assessed by the palpation method using a Prader orchidometer. The pubertal stages in boys and girls were graded from 1–5 according to the methods of Marshall and Tanner (1969). The exact age at the time of examination was calculated in years using the child’s birth certificate. For each age group, the proportions of boys and girls with each Tanner stage of testicular or breast enlargement and pubic hair development and the proportion of girls who had passed menarche were calculated. Health statistics indicators Three main sources of health statistics indicators of Thailand dating back to 1990 were searched: (1) the Statistical Forecasting Bureau, National Statistical Office, Ministry of Information and Communication Technology, Thailand, (2) the Bureau of Policy and Strategy, Office of the Permanent Secretary, Ministry of Public Health, Thailand and (3) the Health Information System Development Office (HISO), a health information and statistical website which collects health and related information from various sources. National health statistics were searched mainly for maternal and child health indicators such as maternal mortality rate, infant mortality rate, under-five mortality rate, life expectancy, per capita income, prevalence of underweight and overweight/obesity in pre-school children and quality of drinking water and adequate sanitation facilities in rural areas. Statistical analyses Height and weight at the median (or the 50th percentile) at each age group were compared with the median heights and weights of the five previous studies on physical growth (Chavalittamrong & Vathakanon, 1978; Chavalittamrong & Tantiwongse, 1987; Jaruratanasirikul et al., 1996; Khanjanasthiti et al., 1987; Nutrition Division, Ministry of Public Health, Thailand, 1999). The median ages of girls at thelarche (breast Tanner II), pubarche (pubic hair Tanner II), menarche and ages of boys at testicular enlargement 4 mL and pubarche were compared with previous studies on age at pubertal maturation of Thai children (Jaruratanasirikul & Lebel, 1995; Khanjanasthiti et al., 1972, 1987; Mahachoklertwattana et al., 2002, 2010). ANOVA was used to compare the median height and weight in each age group
Ann Hum Biol, 2015; 42(5): 447–454
among the studies of growth in Thai children including the current study and the median ages of thelarche, pubarche, menarche and testicular enlargement of children among the studies of the age at puberty in Thai girls and boys. The Spearman rank test was used to identify correlations between these trends and the health statistics indicators of the Thai population during the study time period of 37 years. All statistical analyses were performed using R program (R Foundation, Austria available from http://www.r-project. org/foundation/main.html). Ethical considerations The protocol for this study was approved by the Institutional Review Board and the Ethics Committee of the Faculty of Medicine, Prince of Songkla University. Written informed consent and assent was obtained from all participants and their parents.
Results Three thousand four hundred and sixty healthy schoolchildren (2140 girls and 1320 boys), aged 6–20 years, participated in the current study. For physical growth measurements, we found that the median weight and height of both boys and girls in our current study were greater than those in the same ages of the previous five studies of growth in Thai children (Figures 1 and 2). The final heights as defined by a height gain of less than 1.0 cm per year were 170.3 cm in boys (3.3 cm greater than the 167.0 cm final height of boys in 1994 in Hat Yai municipality) and 157.3 cm in girls (2.3 cm greater than the 155.0 cm final height of girls in 1994) and were attained at ages 17 and 13 years, respectively, both 1 year earlier than the ages of 18 and 14 years in the studies of 1975 and 1994 (Table 1). The median weights of boys and girls at the time of attaining their final heights in this study were 59.6 and 52.0 kg, respectively, which were 9.2 and 6.5 kg, respectively, greater than the median weights of Thai boys and girls in the 1975 study. Comparing these two studies of growth of Thai children 37 years apart, we found a definite secular trend towards the upward displacement of growth curves of both weight and height of Thai children in all age groups. Additionally, a trend towards a decline in the age at the time of peak velocity of the median height was found in our study from 13–14 years in 1975–1994 to 12–13 years in 1999–2012 in boys and from 11–12 years in 1975–1994 to 10–11 years in 1999–2012 in girls (Figure 3) and the age at attaining final height in both boys and girls. The median final heights of Thai boys and girls were calculated to have increased at rates of 1.32 and 0.86 cm/decade, respectively, and the median weights at the time of attaining final heights increased by 2.49 and 1.76 kg/decade, respectively, whereas the age at attaining final height decreased at a rate of 0.03 year/decade in both boys and girls. However, using ANOVA for statistical comparison among the six studies, the changes in median heights and weights were not statistically significant in any age group due to the overlapping of the 95% confidence intervals of the median weights and heights in each study. For the ages of pubertal development which were calculated by probit analysis, we found that, in boys, the
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Figure 1. Growth of Thai boys, age 6–18 years, from 1975–2012. (a) Height, (b) Weight.
median ages of having testicular enlargement and pubic hair Tanner stage II were 10.6 and 12.0 years, respectively, and in girls, the median ages of having breast and pubic hair development Tanner stage II were 9.6 and 11.0, respectively, and the age at menarche 12.2 years. Compared to the earlier study of the median age at puberty in boys, the age at testicular enlargement Tanner II declined from 10.8 years in 1999 to 10.6 years in 2012, a time interval of 13 years, giving a rate of decline of 0.15 years/decade, and the age at pubarche from 13.7 years in 1984 to 12.0 years in 2012, an interval of 28 years, giving a rate of decline of 0.61 years/decade. In girls, the median age at thelarche declined from 10.7 to 9.6 and the median age at pubarche from 12.4 to 11.0 years in an interval of 28 years, giving a rate of decline of 0.39 and 0.50 years/decade. The age at menarche declined from 12.7 years in 1972 to 12.2 years in 2012, a 40-year period with a rate of decline of 0.12 years/ decade.
Health statistics indicators of Thailand dating back to 1990 are shown in Table 2. Generally, there are improvements in socioeconomic and living conditions as shown by the increased life expectancy, per capita income, percentages of potable drinking water and adequate sanitation facilities in rural areas and the increasing prevalence of overweight/ obesity in pre-school children and decreased maternal mortality rate, infant mortality rate, under-five mortality rate and decreasing prevalence of underweight pre-school children. Since some of the health statistics indicators of the Thai population and the growth parameters during the study time period of 37 years were from sporadic surveys and some were from regular surveys at intervals, those indicators were modelled to inter/extrapolate values for missing years by log-linear, log-quadratic, log-cubic or S-curve functions according to the nature of those indicators. For example, height at any age of boys and girls fitted very well with an S-shape function, i.e. height of boys at age 10 years, with the
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Figure 2. Growth of Thai girls, age 6–18 years, from 1975–2012. (a) Height, (b) Weight.
Table 1. Median ages at puberty, median final heights and weights of Thai schoolchildren in previous studies compared to the current study. Boys
Year of study 1972 1975 1984 1984# 1994 1999 1999# 2012 Secular trend/decade
Girls
Age at testicular volume 4 mL (yr)
Age at pubarche (yr)
Age at final height (yr)
Final height (cm)
— — — — — — 10.8 10.6 0.15 yr
— — — 13.7 — — 12.4 12.0 0.61 yr
— 18 17 18 18 17 — 17 0.03 yr
— 165.1 165.7 170.0 167.0 169.6 — 170.3 +1.32 cm
Weight at final height (kg) — 50.4 53.8 55.5 56.8 57.6 59.6 +2.49 kg
Age at thelarche (yr)
Age at pubarche (yr)
Age at menarche (yr)
— — — 10.7 9.9 — 9.4 9.6 0.39 yr
— — — 12.4 — — 11.1 11.0 0.50 yr
12.7 — — — 12.4 — 12.1 12.2 0.12 yr
Age at final height (yr)
Final height (cm)
Weight at final height (kg)
— 16 17 15 16 16
— 154.1 154.9 156.0 155.0 156.9
— 45.5 48.0 51.0 50.0 49.0
15 0.03 yr
157.3 +0.86 cm
52.0 +1.76 kg
Sources of data: 1972: Khanjanasthiti et al. (1972); 1975: Chavalittamrong and Vathakanon (1978); 1984: Chavalittamrong and Tantiwongse (1987); 1984#: Khanjanasthiti et al. (1987); 1994: Jaruratanasirikul & Lebel (1995) and Jaruratanasirikul et al. (1996); 1999: Nutrition Division, Ministry of Public Health, Thailand (1999); 1999#: Mahachoklertwattana et al. (2002, 2010); 2012: Jaruratanasirikul et al. (2014a,b).
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Figure 3. Velocity of the median heights, boys (a) and girls (b), age 6–18 years, from 1975–2012.
Table 2. Thailand health statistics indicators during 1991–2011 and the correlation with growth of Thai children (shown as r and p values). Year Health statistics
1990
1995
2000
2005
2011
Life expectancy, (years) Male Female Per capita income, overall of Thailand (Baht/month) Per capita income, Songkhla (Baht/month) Qualified drinking water in rural areas (%) Adequate sanitation facilities in rural areas (%) Prevalence of obesity, age 6–14 years (%) Crude birth rate (per 1000 live births) Maternal mortality rate (per 100 000 live births) Infant 51 year mortality rate (per 1000 live births) Under-five mortality rate (per 1000 live births) Prevalence of malnutrition, pre-school children (%)
67.7 72.4 ND ND ND 73.84 ND 17.0 19.4 7.6 12.8 ND
69.9 74.9 8 262 11 565 28–51 96.14 5.6 16.2 15.6 7.2 11.6 15
69.9 77.6 12 150 13 505 27–49 95.05 6.7–7.9 12.5 13.2 6.2 11.9 12
69.9 77.6 14 963 15 481 40–80 99.1 ND 13.0 12.2 7.6 10.8 14
71.9 78.8 20 904 27 365 68–90 99.5 8.5–9.7 12.1 10.2 7.1 9.8 9
r
p Value 50.001
0.96 0.98 0.91 0.91 0.94 0.95 0.95 0.86 0.69 0.62 0.97 0.97
50.001 50.001 50.001 50.001 50.001 50.01 50.001 0.021 50.001 50.01
ND, No data. Source of data: (1) National Statistical Office, Ministry of Information and Communication Technology, Thailand, (2) Bureau of Policy and Strategy, Office of Permanent Secretary, Ministry of Public Health, Thailand, (3) The Health Information System Development Office (HISO).
lower limit of 130 cm in 1975 and the upper limit of 135.2 cm in 2011 (Figure 4), while a log-linear model was selected for percentages of obesity and a log-cubic analysis fit well with maternal mortality statistics. In testing correlations of height
with health statistics indicators, predicted height, not the true values of height in only 6 years, was used in all models. The method of inter/extrapolation of health indicators gave some degree of model over-fitting with the predicted height, since
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Figure 4. Height prediction model and actual height from surveys.
many additional points were generated on both sides of the statistical models; thus, both actual measurements of the health indicators and the inter/extrapolated values were used to find the correlations with the predicted height. Using the Spearman rank test, increased physical growth, as determined by height and weight, was positively correlated to life expectancy, per capita income, percentages of drinking water and sanitation facilities and prevalence of overweight/ obesity in young children and was negatively correlated to prevalence of malnutrition, crude birth rate, maternal mortality rate, neonatal mortality rate and under-five mortality rate, with statistical significance (Table 2).
Discussion The results of our study showed positive secular trends in growth increments for both weight and height in all age groups of both boys and girls from 1975–2012, a time interval of 37 years, and a secular trend towards a decline in the median age at pubertal maturation of girls from 1984–2012 and the age at puberty of boys from 1999–2012. The median final height of the Thai children in our study increased at a rate of 1.32 cm/decade in boys and 0.86 cm/decade in girls and the age of peak velocity of the median height and the age at attaining final height declined with a rate of 0.03 years/ decade in both boys and girls. The median age at testicular enlargement Tanner 2 in boys declined at a rate of 0.15 years/ decade and the age at pubarche 0.61 years/decade. In girls, the ages at thelarche, pubarche and menarche declined at rates of 0.39, 0.50 and 0.12 years/decade, respectively.
A ‘‘secular trend’’ is a quantitative change or trend in a series of data points increasing or decreasing over a period of time which can be calculated by linear interpolation between the two end-points of the time interval. Studies of secular trends in the physical growth of children usually cover a series of data points with at least 10 years between the first and last points (Danker-Hopfe & Roczen, 2000). Secular changes in growth and the age at pubertal maturation in children are considered to be indicators of changes in the socioeconomic, nutritional and health status of a population over a period of time (Hauspie et al., 1997). In many developed countries in Europe, such trends have been observed for over a century now; for example, between 1880–1980, an increased physical growth of 1.5 cm/decade during childhood and an increased final height of 1–2 cm/decade in adulthood attained at an earlier age demonstrated this positive trend (Danker-Hopfe & Roczen, 2000; Gohlke & Woelfle, 2009; Hauspie et al., 1997; Malina, 1990). In Japan, long-perspective studies covering a 100-year period have shown that Japanese children had overall height and weight increments of 1.0–2.0 cm/decade and 0.4–1.7 kg/decade in boys and 1.1–1.9 cm and 0.4–1.5 kg/ decade in girls, respectively (Kagawa et al., 2011). Additionally, the age at peak height velocity of the Japanese children declined to an age of 10–11 years in girls and 11–12 years in boys (Kagawa et al., 2011; Zheng et al., 2013). China, another Asian country that has had rapid growth in socioeconomic and nutritional status over recent decades, reported a secular trend towards increasing final height in girls from 158.2 cm in 1979 to 159.5 cm in 2004, a rate of 0.53 cm/
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decade (Ma et al., 2009; Zhen-Wang & Cheng-Ye, 2005) and from 169.2 cm in 1979 to 172.0 cm in 2004 in boys, a rate of 1.08 cm/decade (Ma et al., 2011; Zhen-Wang & Cheng-Ye, 2005). More recently, during 1990–2010, earlier ages of peak velocity of median height at ages 10–11 years in girls and 11–12 years in boys have been reported in many Asian countries including China (Ma et al., 2009, 2011; Zhen-Wang & Cheng-Ye, 2005), Korea (Huen et al., 1997; Karlberg, 2002), Hong Kong (Huen et al., 1997; Karlberg, 2002) and our present study from Thailand. The age at menarche, the definite time of full pubertal maturation of the hypothalamic-pituitary-ovary axis in girls, is the most widely used indicator of sexual maturation and for which we have some of the oldest records in both European and Asian countries. With almost no exceptions, these data have shown marked trends towards a younger age at menarche over the last 150 years. In European countries, the decline in age at menarche has been shown to have fallen from 16–17 years in the mid-19th century to 12–13 years in 2000 (Sørensen et al., 2012; Toppari & Juul, 2010) or 0.35 years/ decade (Gohlke & Woelfle, 2009; Malina, 1990). The effect of nutritional status on the timing of the age at menarche has been shown by worldwide events during which most people suffered nutritional deprivation, such as the period of World War II, when many women born between 1920–1934 in European countries such as France, Germany and the Netherlands and Asian countries such as Japan, Korea and China showed a sharp increase in the median age at menarche (Kwang et al., 2003; Onland-Moret et al., 2005). After World War II and the increasingly improving ability of most people to manage a decent diet, the age at menarche in young women began to steadily decline in many European and Asian countries at the rate of 3.6 months/decade (Ong et al., 2006; Sørensen et al., 2012; Toppari & Juul, 2010). The positive secular trend in growth increment and the decline in age at pubertal maturation in Thai children found in our study over the time interval of 37 years can be explained by significant improvements in socioeconomic markers and overall living conditions and health status in Thailand during the period 1990–2011. This is shown in selected health statistics indicators related to growth such as a decreased prevalence of malnutrition in young children and an increased prevalence of overweight/obesity (Aekplakorn & Mo-suwan, 2009; Chavasit et al., 2013; Winichagoon, 2013), decreased mortality rates of infants and children under 5 years, a longer overall life expectancy and the establishment of improved environmental indicators such as improved availability of potable drinking water and adequate sanitation facilities during this 30–40-year period (Table 2) (Bureau of Policy and Strategy, Office of the Permanent Secretary, Ministry of Public Health, Thailand, 2011; Statistical Forecasting Bureau, National Statistical Office, Ministry of Information and Communication Technology, Thailand, 2012; Health Information System Development Office, 2013). The positive secular trends in growth and the age at puberty of Thai children we found were significantly correlated with the health statistics indicators that have been improving during this 30-year time interval. Although there have been only six data sets of growth (height and weight) during the 30-year interval and there is some inconsistency of years in the
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surveys of health indicators, the correlation between growth and health indicators can be calculated by the statistical calculation methods by inter/extrapolation of both the growth data and the indicators based on the actual data set. Our previous study in 2011–2012 also found that girls who were overweight-for-age had ages of thelarche and menarche significantly younger than in normal and underweight-for-age girls (Jaruratanasirikul et al., 2014a), but this relationship between an earlier age at puberty and being overweight was not found in boys (Jaruratanasirikul et al., 2014b). During the last decade, many studies have shown a positive association between body fat and earlier age of onset of puberty, mostly in girls (Ahmed et al., 2009; Walvoord, 2010). Endocrine disrupters, a class of chemicals that interfere with steroid hormone production and activity by a variety of actions and disruptions at different times of exposure during the intrauterine or early childhood period, have been identified as a major factor responsible for the earlier timing of pubertal onset (Buck Louis et al., 2008; Frye et al., 2012; Toppari & Juul, 2010). Nutritional status, either over or under recommended levels, in early childhood has been suggested as one of the potential endocrine disrupters associated with the timing of pubertal development. To test this hypothesis, welldesigned longitudinal studies with data collection of genetic, lifestyle and environmental exposure factors are needed to identify factors related to the secular trend of somatic growth and the timing of puberty in young girls, which are very difficult to determine at the population level.
Conclusion Our current study confirms the existence of a secular trend towards an increase in physical growth and an earlier age of pubertal maturation of Thai children, both boys and girls. The positive secular trend towards an increase in growth and a decline in the age at onset of puberty of Thai children is correlated with improvements in overall living conditions in Thailand.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Grant support: Research Funding Unit, Faculty of Medicine, Prince of Songkla University. Ethical approval: Ethics Committee, Faculty of Medicine, Prince of Songkla University.
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Ma H-M, Du M-L, Luo X-P, Chen S-K, Liu L, Chen R-M, Zhu C, et al, on behalf of the Pubertal Study Group of the Society of Pediatric Endocrinology and Genetic Disease, Chinese Medical Association. 2009. Onset of breast and pubic hair development and menses in urban Chinese girls. Pediatrics 124:e269–e277. Mahachoklertwattana P, Suthutvoravut U, Charoenkiatkul S, Chongviriyaphan N, Rojroonwasinkul N, Thakkinstian A, Rajatanavin R. 2002. Earlier onset of pubertal maturation in Thai girls. J Med Assoc Thai 85(Suppl 4):s1127–s1134. Mahachoklertwattana P, Suthutvoravut U, Poomthavorn P, Charoenkiatkul S, Udomsubpayakul U, Rajatanavin R. 2010. Sexual maturation in Thai boys. J Pediatr Endocrinol Metab 23:65–71. Malina RM. 1990. Research on secular trends in auxology. Anthropologischer Anzeiger 48:209–227. Marshall WA, Tanner JM. 1969. Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–295. Nutrition Division, Ministry of Public Health, Thailand. 1999. National growth references for children under 20 years of age. Ong KK, Ahmed ML, Dunger DB. 2006. Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend. Mol Cell Endocrinol 254–255:8–12. Onland-Moret NC, Peeters PH, van Gills CH, Clavel-Chapelon F, Key T, Tjonneland A, Trichopoulou A, et al. 2005. Age at menarche in relation to adult height: an EPIC study. Am J Epidemiol 162:623–632. Sørensen K, Mouritsen A, Aksglaede L, Hagen CP, Mogensen SS, Juul A. 2012. Recent secular trends in pubertal timing: implications for evaluation and diagnosis of precocious puberty. Horm Res Paediatr 77:137–145. Statistical Forecasting Bureau, National Statistical Office, Ministry of Information and Communication Technology, Thailand. 2012. Key Statistics of Thailand 2012. Available online at: http://service. nso.go.th/nso/nsopublish/pubs/pubsfiles/Key55_T.pdf (accessed September 14, 2013). Tanner JM. 1999. Growth as a mirror of conditions in society. In: Lindgren GW, editor. Growth as a mirror of conditions in society. Stockholm: Stockholm Institute of Education Press. p 9–48. Toppari J, Juul A. 2010. Trends in puberty timing in humans and environmental modifiers. Mol Cell Endocrinol 324:39–44. Walvoord EC. 2010. The timing of puberty: is it changing? Does it matter? J Adolesc Health 47:433–439. Winichagoon P. 2013. Thailand nutrition in transition: situation and challenges of maternal and child nutrition. Asia Pac J Clin Nutr 32: 6–15. Zheng W, Suzuki K, Yokomichi H, Sato M, Yamagat Z. 2013. Multilevel longitudinal analysis of sex differences in height gain and growth rate changes in Japanese school-aged children. J Epidemiol 23:275–279. Zhen-Wang B, Cheng-Ye J. 2005. Secular growth changes in body height and weight in children and adolescents in Shandong, China between 1939 and 2000. Ann Hum Biol 32:650–665.
ISSN: 0301-4460 (Print) 1464-5033 (Online) Journal homepage: http://www.tandfonline.com/loi/iahb20
Secular trends of growth and pubertal maturation of school children in Southern Thailand Somchit Jaruratanasirikul & Hutcha Sriplung To cite this article: Somchit Jaruratanasirikul & Hutcha Sriplung (2015) Secular trends of growth and pubertal maturation of school children in Southern Thailand, Annals of Human Biology, 42:5, 447-454, DOI: 10.3109/03014460.2014.955057 To link to this article: http://dx.doi.org/10.3109/03014460.2014.955057
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Date: 05 November 2015, At: 19:48
http://informahealthcare.com/ahb ISSN: 0301-4460 (print), 1464-5033 (electronic) Ann Hum Biol, 2015; 42(5): 447–454 ! 2014 Informa UK Ltd. DOI: 10.3109/03014460.2014.955057
RESEARCH PAPER
Secular trends of growth and pubertal maturation of school children in Southern Thailand Somchit Jaruratanasirikul1 and Hutcha Sriplung2 Department of Pediatrics and 2Epidemiology Unit, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, Thailand
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Abstract
Keywords
Background: In Thailand, studies of growth date back to 1975, but there have been no studies examining any trends in increasing/decreasing growth. Aim: To determine if there have been any secular trends of increasing/decreasing growth and/ or ages at puberty in Thai children. Methods: In 2012, a cross-sectional study of growth was conducted in 3460 children. The median heights and weights and the ages of pubertal maturation were compared with previous studies. Correlations between the secular trends and the health statistics indicators were calculated. Results: From 1975–2012, the median final height of boys and girls had increased by 1.32 and 0.86 cm/decade and weight by 2.49 and 1.76 kg/decade, respectively. In girls, the age at thelarche and menarche had declined by 0.39 and 0.12 years/decade, respectively. In boys, the age at testicular enlargement Tanner II had declined by 0.15 years/decade. Increased physical growth was positively correlated to life expectancy, per capita income and prevalence of overweight/obesity was negatively correlated to prevalence of malnutrition and under-five mortality rate. Conclusion: The positive secular trend towards an increase in growth and a decline in the age at onset of puberty of Thai children is correlated with improvements in overall living conditions in Thailand.
Growth, puberty, secular trend
Introduction Physical growth and pubertal maturation are influenced by several factors including genetic factors (ethnicity, genes controlling bone growth and hormonal regulation) and environmental factors (socioeconomic circumstances, psychosocial situation and nutritional status) and have been widely used as indicators for health status and socioeconomic conditions. Tanner (1999), one of the pioneers of auxology, stated that growth is ‘‘a mirror of conditions of society’’. The concept of ‘‘secular trend’’ for growth and pubertal maturation of the children in a population describes the changes in physical development from one generation to the next. The secular trends of growth and the ages at puberty can be positive (increased growth and earlier age at puberty compared to children of the same age of earlier generations), stable or negative. Studies worldwide have demonstrated a sensitivity of these secular trends to changes in living standards (socio-economic and socio-hygienic conditions) both over time and between different social groups (Hauspie
Correspondence: Somchit Jaruratanasirikul, Department of Pediatrics, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, 90110, Thailand. Tel: 66-074-429618. Fax: 66-074-429618. E-mail: [email protected]
History Received 20 October 2013 Revised 11 July 2014 Accepted 4 August 2014 Published online 18 September 2014
et al., 1997). Several studies from both European and Asian countries have shown a secular trend towards an increase in physical growth and a decline in the median age of pubertal development in both boys and girls. In Thailand, we now have available six studies of physical growth with the age at puberty dating back to 1975: 1975 (Chavalittamrong & Vathakanon, 1978), 1984 (Khanjanasthiti et al., 1987), 1986 (Chavalittamrong & Tantiwongse, 1987), 1994 (Jaruratanasirikul et al., 1996), 1996 (Nutrition Division, Ministry of Public Health, Thailand, 1999) and 2012 (Jaruratanasirikul et al., 2014a,b). It was our purpose with this study to assess changes in physical growth and age at puberty in Thai children and to determine whether there has been a positive, stable or negative secular trend during the last 37 years by comparing our new data with data from the previous studies examining growth and ages at puberty in Thailand. The objective was to assess whether, if a positive secular trend was found, there was any correlation between this trend and the relevant health statistics indicators of the Thai population during this time period of 37 years.
Methods A cross-sectional study was conducted from June 2011 to March 2012 in nine primary and secondary schools in
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Hat Yai municipality, the largest urban centre in southern Thailand, which were randomly selected by probability proportional to size sampling (from a total of 29 schools). Children, boys and girls, aged 6–20 years were asked to participate. A general physical examination including a pubertal assessment was performed in all participants, following the same protocol as in earlier related studies (Jaruratanasirikul et al., 2014a,b). In brief, standing height was measured using a portable stadiometer and weight with a digital electronic scale. Heights and weights of the children were calculated into seven standard percentile lines: 3rd, 10th, 25th, 50th, 75th, 90th and 97th. In the girls, breast development and pubic hair development were assessed by a female paediatric endocrinologist and, in the boys, testicular enlargement and pubic hair development were assessed by one of the two male paediatricians who had been specially trained in pubertal assessment by a paediatric endocrinologist. Testicular enlargement was assessed by the palpation method using a Prader orchidometer. The pubertal stages in boys and girls were graded from 1–5 according to the methods of Marshall and Tanner (1969). The exact age at the time of examination was calculated in years using the child’s birth certificate. For each age group, the proportions of boys and girls with each Tanner stage of testicular or breast enlargement and pubic hair development and the proportion of girls who had passed menarche were calculated. Health statistics indicators Three main sources of health statistics indicators of Thailand dating back to 1990 were searched: (1) the Statistical Forecasting Bureau, National Statistical Office, Ministry of Information and Communication Technology, Thailand, (2) the Bureau of Policy and Strategy, Office of the Permanent Secretary, Ministry of Public Health, Thailand and (3) the Health Information System Development Office (HISO), a health information and statistical website which collects health and related information from various sources. National health statistics were searched mainly for maternal and child health indicators such as maternal mortality rate, infant mortality rate, under-five mortality rate, life expectancy, per capita income, prevalence of underweight and overweight/obesity in pre-school children and quality of drinking water and adequate sanitation facilities in rural areas. Statistical analyses Height and weight at the median (or the 50th percentile) at each age group were compared with the median heights and weights of the five previous studies on physical growth (Chavalittamrong & Vathakanon, 1978; Chavalittamrong & Tantiwongse, 1987; Jaruratanasirikul et al., 1996; Khanjanasthiti et al., 1987; Nutrition Division, Ministry of Public Health, Thailand, 1999). The median ages of girls at thelarche (breast Tanner II), pubarche (pubic hair Tanner II), menarche and ages of boys at testicular enlargement 4 mL and pubarche were compared with previous studies on age at pubertal maturation of Thai children (Jaruratanasirikul & Lebel, 1995; Khanjanasthiti et al., 1972, 1987; Mahachoklertwattana et al., 2002, 2010). ANOVA was used to compare the median height and weight in each age group
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among the studies of growth in Thai children including the current study and the median ages of thelarche, pubarche, menarche and testicular enlargement of children among the studies of the age at puberty in Thai girls and boys. The Spearman rank test was used to identify correlations between these trends and the health statistics indicators of the Thai population during the study time period of 37 years. All statistical analyses were performed using R program (R Foundation, Austria available from http://www.r-project. org/foundation/main.html). Ethical considerations The protocol for this study was approved by the Institutional Review Board and the Ethics Committee of the Faculty of Medicine, Prince of Songkla University. Written informed consent and assent was obtained from all participants and their parents.
Results Three thousand four hundred and sixty healthy schoolchildren (2140 girls and 1320 boys), aged 6–20 years, participated in the current study. For physical growth measurements, we found that the median weight and height of both boys and girls in our current study were greater than those in the same ages of the previous five studies of growth in Thai children (Figures 1 and 2). The final heights as defined by a height gain of less than 1.0 cm per year were 170.3 cm in boys (3.3 cm greater than the 167.0 cm final height of boys in 1994 in Hat Yai municipality) and 157.3 cm in girls (2.3 cm greater than the 155.0 cm final height of girls in 1994) and were attained at ages 17 and 13 years, respectively, both 1 year earlier than the ages of 18 and 14 years in the studies of 1975 and 1994 (Table 1). The median weights of boys and girls at the time of attaining their final heights in this study were 59.6 and 52.0 kg, respectively, which were 9.2 and 6.5 kg, respectively, greater than the median weights of Thai boys and girls in the 1975 study. Comparing these two studies of growth of Thai children 37 years apart, we found a definite secular trend towards the upward displacement of growth curves of both weight and height of Thai children in all age groups. Additionally, a trend towards a decline in the age at the time of peak velocity of the median height was found in our study from 13–14 years in 1975–1994 to 12–13 years in 1999–2012 in boys and from 11–12 years in 1975–1994 to 10–11 years in 1999–2012 in girls (Figure 3) and the age at attaining final height in both boys and girls. The median final heights of Thai boys and girls were calculated to have increased at rates of 1.32 and 0.86 cm/decade, respectively, and the median weights at the time of attaining final heights increased by 2.49 and 1.76 kg/decade, respectively, whereas the age at attaining final height decreased at a rate of 0.03 year/decade in both boys and girls. However, using ANOVA for statistical comparison among the six studies, the changes in median heights and weights were not statistically significant in any age group due to the overlapping of the 95% confidence intervals of the median weights and heights in each study. For the ages of pubertal development which were calculated by probit analysis, we found that, in boys, the
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Figure 1. Growth of Thai boys, age 6–18 years, from 1975–2012. (a) Height, (b) Weight.
median ages of having testicular enlargement and pubic hair Tanner stage II were 10.6 and 12.0 years, respectively, and in girls, the median ages of having breast and pubic hair development Tanner stage II were 9.6 and 11.0, respectively, and the age at menarche 12.2 years. Compared to the earlier study of the median age at puberty in boys, the age at testicular enlargement Tanner II declined from 10.8 years in 1999 to 10.6 years in 2012, a time interval of 13 years, giving a rate of decline of 0.15 years/decade, and the age at pubarche from 13.7 years in 1984 to 12.0 years in 2012, an interval of 28 years, giving a rate of decline of 0.61 years/decade. In girls, the median age at thelarche declined from 10.7 to 9.6 and the median age at pubarche from 12.4 to 11.0 years in an interval of 28 years, giving a rate of decline of 0.39 and 0.50 years/decade. The age at menarche declined from 12.7 years in 1972 to 12.2 years in 2012, a 40-year period with a rate of decline of 0.12 years/ decade.
Health statistics indicators of Thailand dating back to 1990 are shown in Table 2. Generally, there are improvements in socioeconomic and living conditions as shown by the increased life expectancy, per capita income, percentages of potable drinking water and adequate sanitation facilities in rural areas and the increasing prevalence of overweight/ obesity in pre-school children and decreased maternal mortality rate, infant mortality rate, under-five mortality rate and decreasing prevalence of underweight pre-school children. Since some of the health statistics indicators of the Thai population and the growth parameters during the study time period of 37 years were from sporadic surveys and some were from regular surveys at intervals, those indicators were modelled to inter/extrapolate values for missing years by log-linear, log-quadratic, log-cubic or S-curve functions according to the nature of those indicators. For example, height at any age of boys and girls fitted very well with an S-shape function, i.e. height of boys at age 10 years, with the
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Figure 2. Growth of Thai girls, age 6–18 years, from 1975–2012. (a) Height, (b) Weight.
Table 1. Median ages at puberty, median final heights and weights of Thai schoolchildren in previous studies compared to the current study. Boys
Year of study 1972 1975 1984 1984# 1994 1999 1999# 2012 Secular trend/decade
Girls
Age at testicular volume 4 mL (yr)
Age at pubarche (yr)
Age at final height (yr)
Final height (cm)
— — — — — — 10.8 10.6 0.15 yr
— — — 13.7 — — 12.4 12.0 0.61 yr
— 18 17 18 18 17 — 17 0.03 yr
— 165.1 165.7 170.0 167.0 169.6 — 170.3 +1.32 cm
Weight at final height (kg) — 50.4 53.8 55.5 56.8 57.6 59.6 +2.49 kg
Age at thelarche (yr)
Age at pubarche (yr)
Age at menarche (yr)
— — — 10.7 9.9 — 9.4 9.6 0.39 yr
— — — 12.4 — — 11.1 11.0 0.50 yr
12.7 — — — 12.4 — 12.1 12.2 0.12 yr
Age at final height (yr)
Final height (cm)
Weight at final height (kg)
— 16 17 15 16 16
— 154.1 154.9 156.0 155.0 156.9
— 45.5 48.0 51.0 50.0 49.0
15 0.03 yr
157.3 +0.86 cm
52.0 +1.76 kg
Sources of data: 1972: Khanjanasthiti et al. (1972); 1975: Chavalittamrong and Vathakanon (1978); 1984: Chavalittamrong and Tantiwongse (1987); 1984#: Khanjanasthiti et al. (1987); 1994: Jaruratanasirikul & Lebel (1995) and Jaruratanasirikul et al. (1996); 1999: Nutrition Division, Ministry of Public Health, Thailand (1999); 1999#: Mahachoklertwattana et al. (2002, 2010); 2012: Jaruratanasirikul et al. (2014a,b).
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Figure 3. Velocity of the median heights, boys (a) and girls (b), age 6–18 years, from 1975–2012.
Table 2. Thailand health statistics indicators during 1991–2011 and the correlation with growth of Thai children (shown as r and p values). Year Health statistics
1990
1995
2000
2005
2011
Life expectancy, (years) Male Female Per capita income, overall of Thailand (Baht/month) Per capita income, Songkhla (Baht/month) Qualified drinking water in rural areas (%) Adequate sanitation facilities in rural areas (%) Prevalence of obesity, age 6–14 years (%) Crude birth rate (per 1000 live births) Maternal mortality rate (per 100 000 live births) Infant 51 year mortality rate (per 1000 live births) Under-five mortality rate (per 1000 live births) Prevalence of malnutrition, pre-school children (%)
67.7 72.4 ND ND ND 73.84 ND 17.0 19.4 7.6 12.8 ND
69.9 74.9 8 262 11 565 28–51 96.14 5.6 16.2 15.6 7.2 11.6 15
69.9 77.6 12 150 13 505 27–49 95.05 6.7–7.9 12.5 13.2 6.2 11.9 12
69.9 77.6 14 963 15 481 40–80 99.1 ND 13.0 12.2 7.6 10.8 14
71.9 78.8 20 904 27 365 68–90 99.5 8.5–9.7 12.1 10.2 7.1 9.8 9
r
p Value 50.001
0.96 0.98 0.91 0.91 0.94 0.95 0.95 0.86 0.69 0.62 0.97 0.97
50.001 50.001 50.001 50.001 50.001 50.01 50.001 0.021 50.001 50.01
ND, No data. Source of data: (1) National Statistical Office, Ministry of Information and Communication Technology, Thailand, (2) Bureau of Policy and Strategy, Office of Permanent Secretary, Ministry of Public Health, Thailand, (3) The Health Information System Development Office (HISO).
lower limit of 130 cm in 1975 and the upper limit of 135.2 cm in 2011 (Figure 4), while a log-linear model was selected for percentages of obesity and a log-cubic analysis fit well with maternal mortality statistics. In testing correlations of height
with health statistics indicators, predicted height, not the true values of height in only 6 years, was used in all models. The method of inter/extrapolation of health indicators gave some degree of model over-fitting with the predicted height, since
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Figure 4. Height prediction model and actual height from surveys.
many additional points were generated on both sides of the statistical models; thus, both actual measurements of the health indicators and the inter/extrapolated values were used to find the correlations with the predicted height. Using the Spearman rank test, increased physical growth, as determined by height and weight, was positively correlated to life expectancy, per capita income, percentages of drinking water and sanitation facilities and prevalence of overweight/ obesity in young children and was negatively correlated to prevalence of malnutrition, crude birth rate, maternal mortality rate, neonatal mortality rate and under-five mortality rate, with statistical significance (Table 2).
Discussion The results of our study showed positive secular trends in growth increments for both weight and height in all age groups of both boys and girls from 1975–2012, a time interval of 37 years, and a secular trend towards a decline in the median age at pubertal maturation of girls from 1984–2012 and the age at puberty of boys from 1999–2012. The median final height of the Thai children in our study increased at a rate of 1.32 cm/decade in boys and 0.86 cm/decade in girls and the age of peak velocity of the median height and the age at attaining final height declined with a rate of 0.03 years/ decade in both boys and girls. The median age at testicular enlargement Tanner 2 in boys declined at a rate of 0.15 years/ decade and the age at pubarche 0.61 years/decade. In girls, the ages at thelarche, pubarche and menarche declined at rates of 0.39, 0.50 and 0.12 years/decade, respectively.
A ‘‘secular trend’’ is a quantitative change or trend in a series of data points increasing or decreasing over a period of time which can be calculated by linear interpolation between the two end-points of the time interval. Studies of secular trends in the physical growth of children usually cover a series of data points with at least 10 years between the first and last points (Danker-Hopfe & Roczen, 2000). Secular changes in growth and the age at pubertal maturation in children are considered to be indicators of changes in the socioeconomic, nutritional and health status of a population over a period of time (Hauspie et al., 1997). In many developed countries in Europe, such trends have been observed for over a century now; for example, between 1880–1980, an increased physical growth of 1.5 cm/decade during childhood and an increased final height of 1–2 cm/decade in adulthood attained at an earlier age demonstrated this positive trend (Danker-Hopfe & Roczen, 2000; Gohlke & Woelfle, 2009; Hauspie et al., 1997; Malina, 1990). In Japan, long-perspective studies covering a 100-year period have shown that Japanese children had overall height and weight increments of 1.0–2.0 cm/decade and 0.4–1.7 kg/decade in boys and 1.1–1.9 cm and 0.4–1.5 kg/ decade in girls, respectively (Kagawa et al., 2011). Additionally, the age at peak height velocity of the Japanese children declined to an age of 10–11 years in girls and 11–12 years in boys (Kagawa et al., 2011; Zheng et al., 2013). China, another Asian country that has had rapid growth in socioeconomic and nutritional status over recent decades, reported a secular trend towards increasing final height in girls from 158.2 cm in 1979 to 159.5 cm in 2004, a rate of 0.53 cm/
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decade (Ma et al., 2009; Zhen-Wang & Cheng-Ye, 2005) and from 169.2 cm in 1979 to 172.0 cm in 2004 in boys, a rate of 1.08 cm/decade (Ma et al., 2011; Zhen-Wang & Cheng-Ye, 2005). More recently, during 1990–2010, earlier ages of peak velocity of median height at ages 10–11 years in girls and 11–12 years in boys have been reported in many Asian countries including China (Ma et al., 2009, 2011; Zhen-Wang & Cheng-Ye, 2005), Korea (Huen et al., 1997; Karlberg, 2002), Hong Kong (Huen et al., 1997; Karlberg, 2002) and our present study from Thailand. The age at menarche, the definite time of full pubertal maturation of the hypothalamic-pituitary-ovary axis in girls, is the most widely used indicator of sexual maturation and for which we have some of the oldest records in both European and Asian countries. With almost no exceptions, these data have shown marked trends towards a younger age at menarche over the last 150 years. In European countries, the decline in age at menarche has been shown to have fallen from 16–17 years in the mid-19th century to 12–13 years in 2000 (Sørensen et al., 2012; Toppari & Juul, 2010) or 0.35 years/ decade (Gohlke & Woelfle, 2009; Malina, 1990). The effect of nutritional status on the timing of the age at menarche has been shown by worldwide events during which most people suffered nutritional deprivation, such as the period of World War II, when many women born between 1920–1934 in European countries such as France, Germany and the Netherlands and Asian countries such as Japan, Korea and China showed a sharp increase in the median age at menarche (Kwang et al., 2003; Onland-Moret et al., 2005). After World War II and the increasingly improving ability of most people to manage a decent diet, the age at menarche in young women began to steadily decline in many European and Asian countries at the rate of 3.6 months/decade (Ong et al., 2006; Sørensen et al., 2012; Toppari & Juul, 2010). The positive secular trend in growth increment and the decline in age at pubertal maturation in Thai children found in our study over the time interval of 37 years can be explained by significant improvements in socioeconomic markers and overall living conditions and health status in Thailand during the period 1990–2011. This is shown in selected health statistics indicators related to growth such as a decreased prevalence of malnutrition in young children and an increased prevalence of overweight/obesity (Aekplakorn & Mo-suwan, 2009; Chavasit et al., 2013; Winichagoon, 2013), decreased mortality rates of infants and children under 5 years, a longer overall life expectancy and the establishment of improved environmental indicators such as improved availability of potable drinking water and adequate sanitation facilities during this 30–40-year period (Table 2) (Bureau of Policy and Strategy, Office of the Permanent Secretary, Ministry of Public Health, Thailand, 2011; Statistical Forecasting Bureau, National Statistical Office, Ministry of Information and Communication Technology, Thailand, 2012; Health Information System Development Office, 2013). The positive secular trends in growth and the age at puberty of Thai children we found were significantly correlated with the health statistics indicators that have been improving during this 30-year time interval. Although there have been only six data sets of growth (height and weight) during the 30-year interval and there is some inconsistency of years in the
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surveys of health indicators, the correlation between growth and health indicators can be calculated by the statistical calculation methods by inter/extrapolation of both the growth data and the indicators based on the actual data set. Our previous study in 2011–2012 also found that girls who were overweight-for-age had ages of thelarche and menarche significantly younger than in normal and underweight-for-age girls (Jaruratanasirikul et al., 2014a), but this relationship between an earlier age at puberty and being overweight was not found in boys (Jaruratanasirikul et al., 2014b). During the last decade, many studies have shown a positive association between body fat and earlier age of onset of puberty, mostly in girls (Ahmed et al., 2009; Walvoord, 2010). Endocrine disrupters, a class of chemicals that interfere with steroid hormone production and activity by a variety of actions and disruptions at different times of exposure during the intrauterine or early childhood period, have been identified as a major factor responsible for the earlier timing of pubertal onset (Buck Louis et al., 2008; Frye et al., 2012; Toppari & Juul, 2010). Nutritional status, either over or under recommended levels, in early childhood has been suggested as one of the potential endocrine disrupters associated with the timing of pubertal development. To test this hypothesis, welldesigned longitudinal studies with data collection of genetic, lifestyle and environmental exposure factors are needed to identify factors related to the secular trend of somatic growth and the timing of puberty in young girls, which are very difficult to determine at the population level.
Conclusion Our current study confirms the existence of a secular trend towards an increase in physical growth and an earlier age of pubertal maturation of Thai children, both boys and girls. The positive secular trend towards an increase in growth and a decline in the age at onset of puberty of Thai children is correlated with improvements in overall living conditions in Thailand.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Grant support: Research Funding Unit, Faculty of Medicine, Prince of Songkla University. Ethical approval: Ethics Committee, Faculty of Medicine, Prince of Songkla University.
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