Body Composition Assessment in Infancy and Early Childhood: Comparison of Anthropometry with Dual-Energy X-Ray Absorptiometry in Low-Income Group Children from India

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BODY COMPOSITION ORIGINAL ARTICLE Body composition assessment in infancy and early childhood: comparison of anthropometry with dual-energy X-ray absorptiometry in low-income group children from India

B Kulkarni, RS Mamidi, N Balakrishna and KV Radhakrishna

BACKGROUND/OBJECTIVE: Anthropometry is a simple, inexpensive method of body composition assessment, but its validity has not been examined adequately in young children. The study therefore compared the body composition estimates using anthropometry with those using dual-energy X-ray absorptiometry (DXA) in infants and young children. METHODS: Body composition estimates using anthropometry and DXA were assessed and compared at 6, 12 and 18 months in a cohort of 137 infants enrolled at birth. RESULTS: Fat mass (FM) and body fat percent (%BF) estimates by anthropometry were lower than those using DXA. Mean differences (DXA − skinfold thickness) in FM, fat free mass (FFM) and %BF were highest at 6 months (350 g, − 226 g and 4%, respectively); the differences reduced with increase in age and were lowest at 18 months (46 g, 56 g and 0%, respectively). Bland–Altman analyses showed good agreement between the FM, FFM and %BF estimates by the two methods only at 18 months. Accretion of FM and FFM during follow-up, estimated by the two methods, was signiﬁcantly different, with agreement between the methods seen only for increment in FFM from 6 to 12 months. CONCLUSIONS: Substantial differences were found in the body composition estimates by anthropometry compared with DXA and also in the longitudinally assessed tissue accretion patterns by the two methods. As the body composition patterns may be inﬂuenced by the method used for body composition assessment, results of studies assessing body composition by anthropometry during infancy should be interpreted with caution. European Journal of Clinical Nutrition (2014) 68, 658–663; doi:10.1038/ejcn.2014.37; published online 19 March 2014

INTRODUCTION air displacement plethysmography are expensive and not suitable 10 Although periodic measurement of weight during childhood is for use in community-based studies in developing countries. important for growth monitoring, it cannot differentiate between Anthropometry using the skinfold thickness (SFT) measurements the accretion of fat mass (FM) and fat free mass (FFM) during is a valuable technique in these settings, which has been validated 11–13 growth. Examination of body composition in childhood and in adults, indicating reasonable precision and accuracy. changes in tissue accretion during growth is important to monitor However, some researchers have argued that skinfold measure- the optimal growth of FM and FFM compartments. Body ments are difﬁcult to perform in infants and are associated with 14 composition in childhood tracks to adulthood and a body operator-related imprecision. composition with a higher FM and lower FFM is known to be Only a few studies have validated anthropometric assessment of associated with a higher risk of metabolic syndrome and body composition against a reference method in infants and young 15,16 cardiovascular disease in adults.1–3 Muscle mass, a major children. Majority of these were carried out in developed component of FFM, is an important determinant of physical work countries. Similar evidence based on studies carried out in the capacity and has a protective role in chronic degenerative community settings of developing countries is not available. diseases such as osteoporosis.4,5 We therefore compared the body composition estimates by Epidemiologic studies have shown that poor growth during anthropometry with those measured using DXA, which has been early life followed by rapid weight gain in later life is associated shown to measure FM and FFM with high precision in pediatric 17 with an increased risk of obesity and adult onset chronic diseases population. like diabetes and cardiovascular disease.6–8 This could be partly explained by the body composition changes as the growth in MATERIALS AND METHODS initial 2 years of life is related to FFM, whereas growth during later childhood is related to FM in adulthood.9 Understanding the This study was conducted according to the guidelines laid down in the patterns of accretion of FFM and FM during childhood growth Declaration of Helsinki Principles and all procedures involving human subjects were approved by the Institutional Ethics Committee of National may help us devise strategies to promote optimal growth. Institute of Nutrition (Hyderabad, India). Written informed consent was There is a paucity of data on body composition of infants as obtained from mothers of infants who were enrolled in the study. simple, inexpensive, safe and reliable methods are not readily The study included infants who were prospectively followed up from available. Precise methods for body composition assessment such birth along with their mothers who participated in a study assessing the as isotope dilution, dual-energy X-ray absorptiometry (DXA) and effect of calcium-rich food supplementation on the bone density changes

Clinical Division, National Institute of Nutrition, Hyderabad, India. Correspondence: Dr B Kulkarni, Clinical Division, National Institute of Nutrition, Jamai Osmania PO, Hyderabad 500007, India. E-mail: [email protected] Received 28 September 2013; revised 31 January 2014; accepted 5 February 2014; published online 19 March 2014 Body composition assessment in infants B Kulkarni et al 659 during lactation. The study was carried out during the period 2007–2011 in FFM, TM and body fat percent (%BF) were calculated at 6, 12 and 18 months. an urban slum in Hyderabad, India and the mothers and their infants were Differences (DXA − skinfold method) in increments of FM, FFM, TM and %BF enrolled soon after delivery. In case of some children, enrollment was during the two consecutive follow-ups, that is, baseline to 6, 6–12 and 12–18 delayed till 2 months after delivery because of local customs. A total of 137 months were also calculated. Pearson's correlation coefﬁcients were infants were enrolled at baseline and follow-up measurements were calculated to assess the relationship between the FM, FFM, TM and %BF carried out at 6, 12 and 18 months. A written informed consent was estimates by the two methods at all follow-ups and for all increments. obtained from the mothers before the start of the study. A pretested Bland–Altman analysis was used to examine the agreement between the questionnaire was administered to the mothers to record the birth two methods.23 A test was considered signiﬁcant when P-value was o0.05. history as well as breast feeding and complementary feeding practices.

Body composition assessment RESULTS Body composition was assessed by two methods: by DXA at baseline and All the infants belonged to the low socioeconomic group. Most at 6, 12 and 18 months and by anthropometry at 6, 12 and 18 months. (74%) of the mothers were home makers and 64% of fathers were Anthropometric measurements included weight and length along with skilled laborers. The infants were born at term and their mean (s.d.) crown rump length and the length measurements of the upper arm and age at baseline measurement was 33 (8) days. Mean birth weight of lower arm. In addition, circumferences of head, chest, mid-arm, mid-thigh the babies (based on hospital records) was 2.8 kg and 32% of the and mid-calf were measured along with SFT measurements at triceps and babies were born with low birth weight (o2.5 kg). About 60% of subscapular region. All the measurements were carried out by two trained fi field investigators. Weight was measured to the nearest 1 g using a digital the babies were exclusively breast fed for the rst 6 months and SECA weighing scale (Seca, Hamburg, Germany). Length was measured to rest of them were given animal milk and water along with breast the nearest 0.1 cm using an infantometer scale made in-house at our milk. Data on 137 children (48% boys) were available for analysis. institute, which has been validated and used in previous studies at our center.18 Lengths of the upper and lower arm along with the circumferences were measured to the nearest 0.1 cm using a non-stretchable measuring Comparison of body composition estimates by two methods tape. SFT was measured to the nearest 0.1 mm using Harpenden Calipers during follow-up (British Indicators, Burgess Hill, UK). Training sessions for the field Table 1 shows mean values of FM, FFM, TM and %BF by investigators were repeated every 6 months and regular assessment of anthropometry and DXA at baseline (only DXA) and at three intra- and interindividual variation in anthropometric measurements was follow-ups. The estimates by DXA are useful in understanding the carried out for quality control. Estimates of FM and FFM from the above patterns of tissue growth during infancy and early childhood. anthropometric indices were calculated using the method described by There were no sex-related differences in the FM and %BF either at Dauncey et al.19 The method assumes the body to be a sphere (head) and various hollow cylinders (the trunk and the limbs). The estimate of FM is baseline or at any of the follow-ups, but boys had higher FFM and calculated from the volume of the fat component of these cylinders by using TM than girls at all the time points (based on the DXA triceps and subscapular SFT. We chose Dauncey’s method over the other estimates—data not shown) similar to the previously reported 24 commonly used method described by Weststrate and Deurenberg20 because studies. Anthropometric method underestimated FM and %BF at in an earlier study in young children carried out at our institute (unpublished), 6 and 12 months. The difference in the estimates was higher at Dauncey’s method showed better agreement with DXA than the Westrate 6 months and reduced at 12 and 18 months. At 18 months, and Deurenberg method. A number of studies have used Dauncey’s method estimates of %BF (19%) by the two methods were similar and the 21,22 to estimate the body composition of infants based on anthropometry. differences in the FM and FFM estimates were small and Weight was considered to be equivalent of total mass (TM) measured statistically not significant. Bivariate analysis showed significant using DXA. o All the children had their body composition assessed by DXA (QDR correlation between the methods (P 0.001) for all body Discovery, Hologic, Waltham, MA, USA), which was operated in a single- composition indices and at all follow-ups (Table 2). Strength of beam mode. Quality control scans were performed daily using a association varied greatly and was lowest for %BF at 6 months manufacturer-supplied phantom. All the scans were performed in supine (r = 0.536) and highest for TM at 6 months of age (r = 0.981). position when the infant was asleep. The scans were analyzed using infant Agreement between the two methods for FM, %BF and FFM whole-body software. DXA and anthropometric measurements were assessed using the Bland–Altman method was good only at carried out on the same day. However, in case of a few children, it was 18 months, with significant differences in the estimates by the two not possible to complete the scan on the same day and the scan was methods seen at earlier follow-ups (Table 2 and Figures 1a–c). either postponed to the next day or abandoned if the mother could not return for the measurements on the following day. Comparison of increments in body composition indices by two Statistical analysis methods during follow-up All the analyses were carried out using Statistical Package for Table 3 shows the increments in body composition indices by the Social Sciences for Windows (SPSS version 17; IBM, Chicago, IL, USA). two methods at successive follow-ups in the first 18 months of life. For continuous variables, mean and s.d. was calculated. For categorical Increments in FM from 6 to 12 months and 12 to 18 months, variables, frequencies were calculated. Mean differences (DXA − SFT) in FM, estimated by DXA, were negative, indicating reduction in FM at

Table 1. Body composition indices of children assessed longitudinally during ﬁrst 18 months of life using DXA and anthropometry

Age (months) DXA Anthropometry

Na FM (g) FFM (g) TM (g) %BF N FM (g) FFM (g) TMb(g) %BF

Baseline 0.6 (0.5) 130 584 (257) 3291 (330) 3875 (517) 15 (5) 137 NA NA 3730 (730) NA F-up 1 6.3 (0.8) 124 1980 (608) 5112 (559) 7091 (820) 28 (7) 126 1628 (471) 5330 (600) 6959 (826) 23 (5) F-up 2 12.0 (0.8) 113 1848 (557) 6319 (617) 8167 (881) 22 (5) 114 1675 (501) 6474 (816) 8135 (1045) 20 (5) F-up 3 18.2 (1.2) 97 1789 (622) 7273 (648) 9062 (953) 19 (5) 96 1745 (547) 7238 (862) 8974 (1013) 19 (5) All 8.6 (6.6) 464 1517 (785) 5348 (1582) 6864 (2139) 21 (7) 473 1463 (566) 5250 (1844) 6711 (2229) 22 (6) Abbreviations: %BF, body fat percent; DXA, dual-energy X-ray absorptiometry; FM, fat mass; FFM, fat free mass; F-up, follow-up; NA, data not available; s.d., standard deviation; TM, total mass. aSample size. bBody weight was considered as total mass in case of anthropometry. All the values are presented as mean (s.d.).

© 2014 Macmillan Publishers Limited European Journal of Clinical Nutrition (2014) 658 – 663 Body composition assessment in infants B Kulkarni et al 660 these time points, whereas those measured with anthropometry 8 7 were positive, indicating accretion of FM at these follow-ups 17 − − −

11 (NS) (Table 4). Increments in FFM at different follow-up periods

− measured with DXA were higher than those measured with anthropometry. Bivariate analysis showed a modest correlation between the increments in the FM, TM and %BF at different follow-ups measured by the two methods, but there was no 795 11 268 15 202 16 460 signiﬁcant relation between the increments in FFM by the two − − − − 999 (NS) 12 methods. The overall agreement between the two methods for − estimation of FM, %BF and FFM increments at different follow-ups using the Bland– Altman analysis was poor except for the increments in FFM between 6 and 12 months. The increments in TM (from 1 to 6 months and 12 to 18 months) measured by the

cant; TM, total mass or body weight; s.d, ﬁ ﬁ Altman analysis two methods were not signi cantly different, indicating a good – 1150 860 1446 1047 1114 451 agreement (Table 4). − − − 1321 (NS) 995 − DISCUSSION

e; NS, not signi The present study, which compared the body composition estimates in young children by anthropometry and DXA, showed 916 1274 664 1130 474 663 a good agreement between the methods only for the estimates at − − − 893 (NS) 1433 18 months of age. Agreement between the methods during − infancy was poor. The increments in fat and FFM measured by the two methods during follow-up did not show good agreement UL LL UL LL UL LL UL LL between the methods. The ﬁndings suggest that the results of the prospective studies assessing the body composition changes 0.01) 1012 0.01) 986 0.01) 1042 during growth may be inﬂuenced by the method used for body o o o composition assessment. Only a few studies, mainly from the developed countries, comparing the body composition estimates by anthropometry with a precise reference method in infants and young children have been reported till date.16,25,26 To our knowledge, such a 0.01) 0.245 ( 0.01) 0.486 ( 0.01) 0.500 ( 0.01) 0.536 (0.01) 1174 0.001) NAstudy has not 801 yet been reported from a developing country. o o o o o A recent study from Australia compared the FFM and %BF estimates by anthropometry with the air displacement plethysmo-

value) graphy in 77 infants at birth, 6.5 weeks, 3 months and (P- 4.5 months.15 There was a poor correlation between the body b 0.01) 0.985 ( 0.01) 0.898 ( 0.01) 0.869 ( 0.01) 0.981 ( composition estimates by the two methods and anthropometry o o o o –

Altman analysis in children followed up from birth to 18 months of life underestimated %BF by 2.4 8.9 percentage points. Similarly, in – our study, anthropometry underestimated %BF at 6 months of age by about 4%, but the limits of agreement were wide. In the Australian study, the estimation of FFM and %BF from anthropometric measurements was carried out using Salughter’s equation, 0.01) 0.948 ( 0.01) 0.609 ( 0.01) 0.630 ( 0.01) 0.710 ( which was developed in prepubescent children.27 On the other o o o o hand, our study used Dauncey’s equation that was developed in cient. ﬁ newborns. The Australian study did not carry out the follow-up measurements beyond 4.5 months and therefore direct comparison of the results of the two studies is not possible. However, the 1 (8) 0.794 ( pattern of improvement in the agreement between the methods − with increase in age that was observed in our study was not seen Correlation coef

b in the Australian study. Two other studies in infants from the United Kingdom and Sweden have also reported a poor correlation between the estimates of %BF by anthropometry and those based on isotope dilution technique.25,26 However,

anthropometry, bivariate analysis and Bland none of these studies had body composition estimates measured Sample size. − anthropometry BIivariate analysis Bland a Mean (s.d.) R

− beyond 6 months. Only one study from Germany has compared 158 (644) 24 (512) 2 (5) 0.678 ( 226 (444) 124 (163) 4 (6) 0.736 ( anthropometry with DXA for body composition assessment in − − DXA infancy.16 In this study, which included 104 term and preterm babies followed up at 0, 2 and 4 months of age, a total of 185 data points (measures at all follow-ups pooled together) were analyzed

FM (g) FFM (g) TM (g) %BF FM (g) FFM (g) TM (g)for agreement %BF in FM FM (g) and %BF FFM (g) estimations TM (g) by the two %BF methods.

a Although the body fat measurements by the two methods were N closely correlated, anthropometry systematically underestimated body fat compared with DXA, which was also seen in our study. Mean differences in DXA It is well known that body composition patterns during early life predict future disease risk. However, only a few studies have documented accretion of fat and lean mass during infancy.28–30 All 460 48 (482) 62 (606) 108 (376) 18 Months 96 46 (470) 56 (689) 100 (448) 0 (6) 0.683 ( 12 Months 112 189 (426) 6 Months 124 350 (412) 1 Month 130 NA NA 170 (315) NA NA NA 0.805 ( Table 2. Abbreviations: %BF, body fat percent; DXA, dual-energy X-ray absorptiometry; FM, fat mass; FFM, fat free mass; LL, lower limit; NA, data not availabl standard deviation; UL, upper limit. The present study therefore makes a valuable contribution to the

Figure 1. (a)Bland–Altman plot for comparing %BF measured by SFT with DXA at 6 months. The dashed red line represents the line of best fit from linear regression. (b)Bland–Altman plot for comparing %BF measured by SFT with DXA at 12 months. The dashed red line represents the line of best fit from linear regression. (c)Bland–Altman plot for comparing %BF measured by SFT with DXA at 18 months. The dashed red line represents the line of best fit from linear regression. The full colour version of this figure is available at European Journal of Clinical Nutrition online.

Table 3. Increment in FM, FFM, TM and %BF from birth to 18 months of life using DXA and anthropometry

Increment (DXA) Increment (anthropometry)

Na FM (g) FFM (g) TM (g) %BF N FM (g) FFM (g) TM (g) %BF

Mean (s.d.) Mean (s.d.)

1–6 Months 115 1392 (584) 1794 (497) 3186 (722) 13 (7) 126 NA NA 3216 (867) NA 6–12 Months 110 − 160 (406) 1261 (494) 1101 (472) − 6 (5) 114 49 (403) 1159 (617) 1205 (660) − 3 (5) 12–18 Months 91 − 92 (478) 955 (477) 863 (484) − 3 (5) 94 86 (523) 691 (832) 769 (807) − 1 (6) Abbreviations: %BF, body fat percent; DXA, dual-energy X-ray absorptiometry; FM, fat mass; FFM, fat free mass; NA, data not available; TM, total mass or body weight; s.d., standard deviation. aSample size. understanding of fat and lean mass accretion patterns during Another reason for the higher difference in the estimates at an infancy. An important ﬁnding of the present study is that the earlier age could be related to the errors due to practical differences in body composition estimates between the two difﬁculties in holding the very small skinfolds by investigators, methods reduced with increasing age with good agreement which may reduce later with the growth of the child. Although we between the methods seen at 18 months. The predictive do not have data beyond 18 months, the trend in the agreement equations using the subcutaneous measures of body fat, that is, between the methods observed in this cohort suggests that SFT to estimate the total body fat assume a constant ratio anthropometry may be a more reliable technique for body between internal and subcutaneous fat at a given level of fatness. composition assessment beyond infancy. On the other hand, DXA measures total body fat that includes An important aspect of body composition measurements in both subcutaneous and internal FM.31 The rapid changes in the young children is the change in FM, FFM and %BF over a period of proportion of subcutaneous fat to the total body fat during early time, which is important in longitudinal studies (observational as childhood may partly explain the age-related differences in the well as intervention studies) to assess growth or to assess the agreement between the two methods seen in our study.32 effect of interventions on body composition of young children

© 2014 Macmillan Publishers Limited European Journal of Clinical Nutrition (2014) 658 – 663 Body composition assessment in infants B Kulkarni et al 662 over a period of time. We therefore compared the increments in body composition indices using anthropometry and DXA at 15 9

14 10 successive follow-ups. The correlation between the methods was − − modest for all the indices and Bland–Altman analysis did not show agreement between the methods except a good agreement for increment in FFM from 6 to 12 months. This ﬁnding has important

1217 implications for longitudinal studies assessing the tissue accretion − 786 (NS) NA NA 1346 (NS)

− patterns. It indicates that the estimates of tissue growth in these − studies may be inﬂuenced by the method used for body composition assessment, although it is commonly assumed that the error with a particular method is similar at different time points. cant; TM, total mass or body weight; Altman analysis ﬁ The major strength of the study is the prospective design, – 1532 1549 which allowed comparison of increments in the FM and FFM by − 1360 (NS) 1003

− the two methods during early childhood. The other strengths include a relatively larger number of study participants who were followed up for 18 months unlike the previous studies where the

e; NS, not signi follow-up was limited to early infancy. In addition, the study included a comprehensive assessment of all body composition 1174 2095 1105 1546 indices unlike majority of the earlier studies that have limited their − − analysis to FM. The study also has a number of limitations that need to be acknowledged. The most important limitation is the use of DXA as a reference method, as DXA is known to have its own limitations.33 It has been argued that DXA may not be 0.001) 800 0.001) 717 considered as a 'gold standard' technique for the assessment of o o body composition.34 However, the accuracy of DXA for body composition assessment has been demonstrated in the piglet model.35 In addition, DXA has been shown to have good reliability for body composition assessment in newborns36 and it is one of the methods recommended by International Atomic Energy 0.001) 0.366 ( 0.001) 0.199 ( 0.001) NA NA NA NA NAAgency 684 for body composition assessment during infancy.37 o o o Moreover, the estimates of %BF and the pattern of age-related changes in the FM, FFM and %BF using DXA in our study were

-value) UL LL ULsimilar LL to the UL values LL estimated UL LL by multicomponent models in P Altman analysis in children followed up from birth till 18 months of life ( 38,39 –

b reference children. Another limitation was the inability to compare the estimates of body composition by the two methods at 1 month (baseline) because the data based on anthropometric measurements were not available at 1 month. In conclusion, signiﬁcant differences were observed in the body composition estimates by anthropometry compared with DXA 0.001) 145 (0.17) 0.498 ( 0.001) 0.175 (0.07) 0.575 ( during infancy, but there was good agreement between the o o methods at 18 months of age. The ﬁndings suggest that the results of the studies assessing body composition by anthro-

cient. pometry during infancy need to be interpreted with caution. The ﬁ reliability of anthropometry appears to be better beyond 1 year of age. Moreover, it is important to understand that the results of the 2 (6) 0.507 ( 3 (6) 0.362 ( ﬂ − − prospective studies may be in uenced by the method used for body composition assessment. Correlation coef b anthropometry ), bivariate analysis and Bland

51 (367) NA NA NA 0.862 ( CONFLICT OF INTEREST 107 (555) − − − ﬂ

anthropometry) Bivariate analysisThe authors declare no con ict Bland of interest. − Sample size. Mean (s.d.) R a ACKNOWLEDGEMENTS The study was sponsored by Department of Biotechnology, Government of India. We thank Dr B Sesikeran, Director, National Institute of Nutrition, Hyderabad, India for the support to carry out this work. We are grateful to our ﬁeld staff led by Chenna Increment (DXA

FM FFM TM %BF FMKrishna FFM Reddy TM and RS Venkateswar %BF Rao for FM their help in conducting FFM the study TM and %BF 187 (494) 281 (907) 101 (724) 194 (456) 93 (727) K Usha Rani for her help with the DXA measurements. We are grateful to the study − − women and their children who participated in this study. a N

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