SHORT AND FAT?
Association between stunting and body
composition in 10‐year‐old children in rural
Bangladesh
08
Fall
SUPERVISORS• Lars-Åke Persson - International Maternal and Child Heatlh,
Department of Womens and Childrens’s Health, Uppsala University
PERNILLA SVEFORS
CONTENTS
1. POPULÄRVETENSKAPLIG SAMMANFATTNING ... 3
2. PREFACE ... 4
3.ABSTRACT ... 5
4. ABBREVIATIONS ... 6
5. BACKGROUND ... 7
5.1 DOHAD ... 75.2 THE “THIN FAT BABY” ... 7
5.3 STUNTING AND BODY COMPOSITION ... 8
1. POPULÄRVETENSKAPLIG SAMMANFATTNING
Förekomsten av kroniska sjukdomar, så kallade ”non‐communicable diseases” (NCDs) så som hjärtkärlsjukdomar och typ 2 diabetes ökar explosionsartad i låg och medelinkomstländer. Enligt Världshälsoorganisationen (WHO) sker 80% av alla dödsfall orsakade av NCDs i dessa länder. Samtidigt är undernäring och infektionssjukdomar fortfarande ett stort problem, något som leder till en dubbel sjukdomsbörda. Under de senaste åren har forskning tytt på att undernäring under foster och spädbarnstiden kan leda till ökad risk att utveckla NCDs som vuxen. Om mamman är undernärd under fostertiden kan detta alltså ge ökad risk för barnet att utveckla till exempel diabetes som vuxen. Detta kallas ” Developmental Origins of Health and Disease” hypotesen, DOHaD. Om detta stämmer betyder det att man kan bekämpa epidemin av typ 2 diabetes och hjärtkärlsjukdomar som idag hotar låg och medelinkomst länder genom att förebygga undernäring i tidig ålder.
Den vanligaste typen av undernäring i världen i dag är hämning av längdtillväxten hos barn, så kallad ”stunting”. För att ytterligare undersöka sambandet mellan undernäring och utveckling av kroniska sjukdomar har vi analyserat kroppskonstitution hos tillväxthämmade barn (stunted) och normallånga barn (non stunted) för att se om tillväxthämmade barn har en större tendens att ackumulera fett, något som skulle kunna leda till en ökad risk för fetma och kroniska sjukdomar i vuxenlivet. Vi mätte olika kroppsmått, så som längd, vikt, omfångsmått och tjocklek på hudveck hos tioåriga barn på landsbygden i låginkomstlandet Bangladesh. Vi använde oss även av så kallad bioimpedans‐mätning för att uppskatta mängden fett och fettfri massa hos barnen.
2. PREFACE
During January and February I spent six weeks in Bangladesh taking part in the data collection of the MINIMat trial. The MINIMAt trial is a randomized trial focused on prenatal food and micronutrient supplementation to pregnant women and is a collaboration between Uppsala University and ICDDR,B, International center for diarrheal disease research, Bangladesh, the leading research institute in Bangladesh. During my stay I visited the field site in Matlab, a rural sub‐district approximately 90 km south east of Dhaka, and accompanied the health care workers in their home and clinic visits collecting data. ICDDR,B has been active in the area since the 1960s and besides being a research center now also runs a hospital that provides healthcare to the region. Being set in a rural environment it is impressive to witness the remarkable research and health care infrastructure that is in place, providing a platform for research and researchers from all over the globe and disciplines. The table underneath describes characteristics of Bangladesh compared to Sweden.
WHO statistics Sweden Bangladesh
Total population 9,380,000 148,692,000
Gross national income per capita
(PPP international $) 39,730 1,810 Life expectancy at birth m/f
(years) 79/83 64/66
Probability of dying under five
(per 1 000 live births) 3 46 Probability of dying between 15
and 60 years m/f (per 1 000 population)
74/47 246/222
Total expenditure on health per capita (Intl $, 2010)
3,757 57
Total expenditure on health as % of GDP (2010)
3.ABSTRACT
Background – Research over the last decades indicates that undernutrition during early development influences later changes in metabolism, growth and body composition. Objective- To analyze body composition in non‐stunted and stunted children in a low‐income setting at the age of 10 years. Design – Cross sectional study in rural Bangladesh Subjects- A total of 694 children, 357 girls and 337 boys participating in the ten‐ year follow up of the MINIMat trial.
Measurements – Anthropometric measurements including, height, weight, mid‐ upper arm, head, waist, abdominal and hip circumferences and triplicate skinfolds at four sites. Bioelectrical impedance measuring fat mass percentage (BF), fat mass (FM), fat free mass (FFM) and total body water (TBW).
4. ABBREVIATIONS
• ICDDR,B – International center for diarrheal disease research, Bangladesh
• BMI- Body mass index • HAZ- Height for age Z-score • WAZ – Weight for age Z-score • BF – Body fat percentage • FM – Fat mass
• FFM – Fat free mass • TBW – Total body water • WHR – Waist -hip ratio • SSF - Subscapular skinfold • TSF - Triceps skinfold
• SSF/TSF – Subscapular skinfold -triceps skinfold ratio • SD - Standard deviation
• C.I – Confidence interval
Skinfolds – measure amount of subcutaneous fat
5. BACKGROUND
5.1 DOHaD At the moment low and middle‐income countries are observing an epidemic of non‐ communicable diseases (NCDs) such as diabetes and cardiovascular diseases (CVD). According to WHO, 80% of deaths due to NCDs happen in low‐income countries 1 . At the same time undernutrition and infectious diseases continue to be a problem in most of these countries leading to a so‐called double burden of diseases and an economic challenge for countries with limited healthcare resources. 2. Research overthe last decades indicates that undernutrition during critical periods of early development influences changes in metabolism, growth and body composition 3 and
that fetal growth restriction and low weight gain in infancy are associated with increased risk of adult cardiovascular disease, type 2 diabetes and metabolic syndrome 4. On the basis of these observations the Developmental Origins of Health
and Disease (DOHaD) hypothesis has been developed, suggesting that unbalanced nutrition in utero and infancy leads to a higher risk for developing NCDs as adults 5.
The presence of undernutrition combined with the rapid nutrition transition that takes place in low‐income countries (with increasing access to Westernized diets and less physical activity) may be a reason for increases in childhood adiposity and the rising prevalence of NCDs 3
5.2 THE “THIN FAT BABY”
During the last two decades there has been a rapid increase in prevalence of diabetes in the South Asian region, now reaching epidemic proportions. The prevalence of diabetes is estimated to increase with 151% between the years of 2000 to 20306. At the same time the region struggles with undernutrition and has the highest number of stunted children in the world, 93 million 7.
South Asians are known to have an increased risk of developing diabetes compared to other ethnic groups 8 and India is today the country with the biggest
number of diabetic patients in the world. 9. The Indian population is more insulin‐
than members of other populations of comparable BMI 10. Recent studies have shown that this phenotype is present also at birth. Yanik et al. showed that babies born small have small abdominal viscera and low muscle mass but preserved body fat, the so‐called “thin‐fat” baby. Indian babies are small compared to UK babies and abdominal viscera and muscle suffer most while subscapular fat is the most preserved11. There is also evidence that the “thin‐fat” phenotype persists
throughout childhood and pre‐puberty 12. This indicates that the body composition
seen in adult Indians could be a result of metabolic and structural changes caused by fetal undernutrition.
5.3 STUNTING AND BODY COMPOSITION
Currently stunting is the most dominant form of undernutrition and more common than underweight and wasting in low‐income countries. Stunting is defined as a height more than two standard deviations under the WHO growth standards. In 2010 the prevalence of stunted children <5 years was 38,5% in Africa, 27,6% in Asia and 13,5% in Latin‐America, Asia being home to over 100 million stunted children. The process of becoming stunted starts in utero and early life, the main causes being intrauterine growth restriction, frequent infections and inadequate nutrition to support rapid growth 7. The Maternal and Child Undernutrition Study Group determined that stunting is linked to impaired cognitive development, school achievement, economic productivity in adulthood and maternal reproductive outcomes 13. Lately the association between stunting and the implications on body composition later in life has started to be explored. A study based on national representative surveys in Russia, South Africa, Guatemala, China and Brazil described that stunted children have a higher risk of developing obesity than non‐ stunted children 14. Hoffman et al measured energy expenditure and fat distribution
in children in low‐income areas in Sao‐Paolo, Brazil and showed that stunted children exhibit a lower fat oxidation, indicating a higher susceptibility to accumulate body fat 15, as well as a higher percentage of abdominal fat compared to
those with normal stature 16. Moreover, Martins et al. demonstrated that stunted
body mass than non‐stunted 17. In addition reports from a large cohort in Guatemala has described a positive association between childhood stunting and increased abdominal fat in adulthood 18. However the evidence is still inconclusive. A
prospective cohort study of 116 children between 7 and 11 years in Kingston, Jamaica, reported that early childhood stunting resulted in low body mass index and total body fat but increased subscapular, triceps skinfold (SSF/TSF) ratio, indicating a more central pattern of body fat distribution compared to non‐stunted children 19.
However a similar South African study using DXA to determine body composition was unable to find an association between early stunting and later tendency to accumulate central body fat in urban, pre‐pubertal children. 20.
5.4 MINIMat
The Maternal and Infant Nutrition Interventions in Matlab (MINIMat) trial is a factorial randomized trial focused on early prenatal food and micronutrient supplementation to pregnant women and the effect on the children's future health, carried out in rural Bangladesh. Previous reports have demonstrated that early invitation (immediately after ascertainment of pregnancy) to prenatal food supplementation can reduce stunting in boys 21. These findings indicate programming effects by prenatal nutrition interventions. This student paper analyzes the association between stunting and body composition in the MINIMat cohort. Finding an association between stunting and adiposity, one of the strongest risk factors for metabolic diseases, would give further evidence to the association between undernutrition and body composition and contribute to the conclusion that prevention of type 2 diabetes and other NCDs must “begin in utero and continue throughout childhood and the course of life” 22.
5.5 AIM
6. METHODS
6.1 PARTICIPANTS
The MINIMat trial has been carried out in Matlab, a rural sub‐district 57 km south‐ east of the capital, Dhaka. In the area the population receives health services from the International Center for Diarrheal Disease Research, Bangladesh (ICDDR,B). A Health and Demographic Surveillance System has been in place since mid‐1960s, covering a population of about 220 000 in more than 140 villages with monthly updates of demographic and selected health information.
This study is based on the 10‐year follow up off the cohort of women and their children that participated in the MINIMat trial 2001 – 2004 (and the follow‐up at 2 and 4,5 years of age). 1590 children born between April 2002 and November 2003 will participate in the 10‐year follow up. Data collection was initiated in early May 2012 when the children started to reach 10 years. This student paper will present data collected from children born between April and December 2002 (n=697) 6.2 MEASUREMENTS The data collection was initiated by a home visit, collecting informed consent and interviewing the mother and child regarding socioeconomic status (SES). Trained personnel with at least ten years of education performed the interview, using structured questionnaires that included both pre‐coded and open‐ended questions. Information collected included family wealth, household structure, age of mother, parental education, employment and food security.
measurements of skinfold thickness of biceps, triceps, sub‐scapular and supra‐iliac were carried out using a Holtain caliper to the nearest 0,2mm. The same study nurse performed all measurements of skinfold thickness and circumferences in the same order on the left side of the body. The proportion of fat free mass (FFM) and fat mass (FM) was assed by bioelectrical impedance using Tanita TBF‐300MA Body Composition Analyzer. Height, sex and age were entered manually while weight was recorded automatically adjusting for weight of clothes in all subjects, children being barefoot wearing light clothes. Weighing equipment was calibrated daily with standard weights. The Tanita software uses in‐built prediction equations to estimate FM and FFM. These built‐in prediction equations are based on Caucasian populations of age 7 and older. In a validation study conducted in the Matlab population, the equations were found to be inaccurate. Therefore an equation previously derived in this population using oxide dilution as a reference method was used to predict FFM 23.
6.3 ETHICS
Informed consent was obtained from parents of participating children. Both the ethical review committee at ICDDR,B and the research ethics committee at Uppsala University approved the trial and the follow‐up.
6.4 STATISTICAL ANALYSIS
7. RESULTS
694 mothers and children were visited and measured between May and December 2012 (Table 1). The population of participating children comprised of an almost equal proportion of girls and boys, (51,4%, 48,6%). Their mean age was 10.04 years, mean height 129.1 cm, HAZ – 1.39 and mean weight 23.9 kg. The mean height of the mothers was 151.2 cm, equivalent to adult women in India and more than 16 cm below standard height of women in Sweden 26,27 Among the mothers 80.6 % had previously gone to school with a mean of 6.2 years and 95.2 % of the children were going to school at the time of the home visit. The mothers of the stunted children turned out to have fewer years of education and lower socioeconomic status than mothers of the non‐stunted children (P<0.001). The socioeconomic characteristics of the mothers and sex of the participating children are described in table 1. Table 1 Characteristics of study participants, stratified for stunted, height (<2 SD score), or not. Variables Total n=694 Non stunted n=490 Stunted n=204 Girls 357 241 116 Boys 337 249 88 Wealth score 2.99 (1.42) 3.11 (1.41) 2.72 (1.40) Mothers education (years) 6.15 (2.98) 6.38 (3.08) 5.52 (2.59) The prevalence of stunting (< ‐ 2 S.D) in the study population was 29.4% (206/694) and mild stunting (>‐2 ‐<‐1) 38.8% (269/694). The prevalence of stunting among girls was somewhat higher, 32.5 % compared to boys 26.1 %. The distribution of the severity of stunting is shown in table 2.
Table 2 Distribution of severity of stunting . Means (SD) Variables Total n=694 n=357 Girls n=337 Boys Severe (<-3 HAZ) 38 (5.5%) 24 (6.7%) 14 (4.2%) Moderate (>-3 <-2) 166 (23.9) 92 (25.8) 74 (22.0%) Mild ( > -2 < -1) 269 (38.8%) 127 (35.6%) 142 (42.1%) No (> -1) 221 (31.8%) 114 (31.9) 107 (31.8%) There were significant differences in body composition between the sexes and the stunted and non‐ stunted children. Girls proved to have more subcutaneous fat, higher percentage fat mass (BF), fat mass (FM) and lower waist hip ratio (WHR) and subscapular triceps skinfold ratio (SSF/TSF) compared to the boys (p<0.001). This was observed in stunted as well as non‐stunted groups. The stunted children were smaller than the non‐stunted children in all measurements including BMI, circumferences and skinfolds (all P<0.001). They also displayed lower average percentage of BF and FM, assessed by BIA (both P<0.001). The anthropometrics of the participants are described in table 3 and 4.
Table 3 Age and body composition in non‐stunted and stunted girls and boys means (SD)
Variables Girls Boys
Non stunted
n=241 Stunted n=116 n=357Total Non stuntedn=249 Stuntedn=88 n=337Total
Table 4 Body composition in non‐stunted and stunted girls and boys means (SD)
Variables Girls Boys
Non stunted
n=241 Stunted n=116 n=357Total Non stuntedn=249 Stuntedn=88 n=337Total
BF % 17.4 (3.19) 14.8 (2.82) 16.6 (3.32) 14.0 (3.12) 10.4 (2.55) 13.0 (3.34) FM 4.6 (1.71) 3.1 (0.86) 4.1 (1.66) 3.6 (1.39) 2.1 (0.68) 3.2 (1.40) FFM 21.1 (2.95) 17.5 (1.40) 20.0 (3.09) 21.4 (2.49) 17.9 (1.41) 20.5 (2.75) MUAC 18.3 (1.94) 16.7 (1.33) 17.7 (1.87) 17.8 (1.78) 16.3 (1.19) 17.4 (1.76) Waist 53.8 (4.73) 50.5 (3.25) 52.7 (4.57) 54.5 (4.14) 51.2 (2.58) 53.6 (4.05) Abdominal 55.5 (5.28) 51.8 (3.42) 53.3 (5.05) 55.7 (4.49) 52.0 (2.71) 54.7 (4.40) Hip 65.2 (5.10) 60.1 (3.40) 63.5 (5.20) 63.6 (4.25) 58.0 (3.19) 62.1 (4.68) W/H ratio 0.83 (0.04) 0.84 (0.04) 0.83 (0.04) 0.86 (0.04) 0.88 (0.04) 0.86 (0.04) Biceps 5.0 (1.76) 4.5 (1.27) 4.9 (1.63) 4.2 (1.27) 3.8 (0.93) 4.1 (1.20) Triceps 9.4 (2.95) 8.5 (2.17) 9.1 (2.76) 7.6 (2.37) 6.7 (1.66) 7.3 (2.24) Subscapular 6.1 (2.00) 5.4 (1.33) 5.9 (1.83) 5.2 (1.51) 4.5 (0.75) 5.0 (1.38) Suprailiac 7.1 (3.13) 6.2 (2.21) 6.8 (2.89) 5.8 (2.31) 4.7 (1.21) 5.5 (2.11) SSF/TSF ratio 0.66 (0.14) 0.65 (0.10) 0.66 (0.13) 0.70 (0.12) 0.69 (0.11) 0.70 (0.12)
Table 5 Anthropometric z‐scores for non‐stunted and stunted girls and boys means (SD)
Variables Girls Boys
Non stunted
n=241 Stunted n=116 n=357Total Non stuntedn=249 Stunted n=88 n=337Total
ZBM% 0.69 (0.84) 0-.02 (0.75) 0.48 (0.88) -0.25 (0.82) -1.16 (0.87) -0.48 (0.88) ZFM 0.58 (1.06) -0.37 (0.54) 0.29 (1.03) -0.07 (0.87) -0.97 (0.43) -0.29 (0.87) ZFFM 0.29 (1.01) -0.97 (0.48) -0.09 (1.05) 0.39 (0.85) -0.83 (0.48) 0.09 (0.94) ZMUAC 0.32 (1.06) -0.430.(73) 0.08 (1.02) 0.12 (0.97) -0.66 (0.85) -0.08 (0.96) ZWaist -1.58 (1.09) -0.60 (0.75) -0.10 (1.05) 0.30 (0.95) -0.45 (0.59) 0.10 (0.93) ZAbdominal -1.56 (1.11) -0.56 (0.72) -0.04 (1.06) 0.25 (0.95) -0.52 (0.57) 0.05 (0.93) ZHip -1.270 (1.02) -0.56 (0.68) 0.14 (1.04) 0.15 (0.85) -0.96 (0.63) -0.14 (0.94) ZBiceps -1.25 (1.18) 0.01 (0.85) 0.25 (1.10) -0.19 (0.85) -0.45 (0.63) -0.26 (0.81) ZTriceps -1.22 (1.11) 0.09 (0.82) 0.32 (1.04) -0.24 (0.89) -0.59 (0.62) -0.33 (0.84) ZSubscapular -0.97(1.18) 0.00 (0.79) 0.26 (1.08) -0.16 (0.89) -0.57 (0.45) -0.27 (0.82) ZSuprailiac -1.101.19) 0.01 (0.84) 0.24 (1.10) -0.15 (0.88) -0.53 (0.46) -0.25 (0.81) Skinfolds -1.00 (1.08) 0.03 (0.73) 0.26 (0.99) -0.19 (0.82) -0.54 (0.48) -0.28 (0.78) The SSF/TSF ratio was significantly lower among stunted girls (P<0.05) but not among boys. However the waist to hip ratio was significantly higher among both stunted girls and boys. The more severely stunted the child was the higher mean WHR was found (P<0.001). This is presented in table 6. Table 6 Waist‐Hip ratio in relation to degree of stunting or non‐stunting (means, 95% CI)
Height group Girls Boys
Figure 1
Anthropometric z-scores for non-stunted and stunted girls
Figure 2
8. DISCUSSION
In this study we have analyzed body composition in non‐stunted and stunted 10‐ year‐old girls and boys in rural Bangladesh. We found that the stunted children were smaller in all measurements but had higher WHR and that it, among the girls, existed a pattern with relatively preserved subcutaneous fat and a bigger deficit in lean body mass.
Being implemented in an excellent research infrastructure the MINIMat trial has many pre‐requisites to obtain high quality data. Experienced study nurses who have received repeated training and are supervised by senior medical doctors are responsible for data collection. Only one team performs the measurements and the equipment is frequently standardized. The trial is conducted in rural Bangladesh in a typical low socioeconomic setting where undernutrition in early life is widespread and the prevalence of chronic diseases such as diabetes in adult life is increasing. This makes the results relevant for other areas in Bangladesh, neighboring countries in South Asia as well as for other low‐income countries with a rapid nutrition and demographic transition. Previous reports that stunting is associated with overweight 14 was not true for our study population. On the contrary the stunted children in our cohort turned out to be smaller in all measurements compared to the non‐stunted children and boys as well as girls had substantial deficits in lean body mass. However the stunted girls had significantly preserved subcutaneous fat compared to their non‐stunted counterparts. This is in accordance with the findings of the Indian Pune study where small Indian babies exhibited preserved body fat and low muscle mass, the so called “thin fat baby” 11. Hoffman 15 described that stunted children have a lower rate of
fat oxidation, favoring accumulation of body fat. To spare body fat, despite low energy intake, but reduce linear growth may be a way for the body to secure energy for the high metabolic demands of a growing brain 28. However, if the tendency to
another eventual factor promoting future obesity and insulin resistance due to decreased capacity of physical labor seen in stunted adults 2.
WHR has conventionally been used to assess amount of central fat and metabolic risk. In our study population the stunted children had a significantly higher WHR ratio then the non‐stunted group. However, previous research has described that WHR is a poor indicator for the amount of central fat 29–32. Waist
circumference has in these studies been shown to be superior to identify children with high central fat mass. In our study population the children have waist circumference in the 3rd to10 th percentile compared to reference values for
children in their own age from Pakistan 33. According to this the waist‐hip ratio in
this case does not represent a high amount of fat. Nevertheless, it could convey something about the localization of fat. The high WHR in stunted individuals would then point towards a more central fat distribution, supporting the theory of the association between undernutrition and metabolic risk. However, another way of interpreting the high WHR in the stunted group is that it represents a higher grade of immaturity, as younger children have higher WHR 33. Whether the WHR represents a higher metabolic risk in stunted children or not is hard to conclude form this study. One‐way of gaining more information is already planned: comparing the anthropometric findings with the children’s metabolic markers.
The body composition between girls and boys differed significantly in our study population. Boys had a more centralized pattern of subcutaneous fat with a higher WHR and SSF/TSF ratio and girls more subcutaneous fat. In addition the stunted group had different patterns of smallness. As mentioned before the stunted girls presented a body composition with significantly spared subcutaneous fat. The stunted boys on the other hand showed no tendency to spare body fat compared to non‐stunted but had a bigger deficit in lean body mass. These gender disparities may represent differences in puberty development as well as differences in body composition that seem to be present between the sexes in all stages of life 34–36. However, it might also reflect biological differences in how females and males react to stunting. Martins 17, found that stunted boys showed a bigger increase in body fat
Resent research indicates that the process of stunting is initiated already in utero 37. The MINIMat trial has focused on prenatal food intervention to pregnant women and has previously reported effects of the interventions on stunting. Longitudinal analyses of the development of the MINIMat cohort will evaluate the effects of birth weight, food intervention and stunting on future body composition and health and give further information on the association between undernutrition and risk of chronic disease.
8.1 SUMMARY
