PEDIATRIC HIGHLIGHT

High prevalence of insulin resistance in postpubertalAsian Indian children is associated with adverse truncalbody fat patterning, abdominal adiposity and excessbody fat

A Misra1*, NK Vikram1, S Arya1, RM Pandey2, V Dhingra1, A Chatterjee3, M Dwivedi4, R Sharma3,K Luthra4, R Guleria1 and KK Talwar5

1Department of Medicine, All India Institute of Medical Sciences, New Delhi, India; 2Department of Biostatistics, All IndiaInstitute of Medical Sciences, New Delhi, India; 3Department of Dietetics, All India Institute of Medical Sciences, New Delhi,India; 4Department of Biochemistry, All India Institute of Medical Sciences, New Delhi, India; and 5Department ofCardiology, All India Institute of Medical Sciences, New Delhi, India

OBJECTIVE: The objectives were to study the relationships of insulin resistance with generalized and abdominal obesity, andbody fat patterning in urban postpubertal Asian Indian children.DESIGN: Cross-sectional, population-based epidemiological study.SUBJECTS: In all, 250 (155 males and 95 females) healthy urban postpubertal children.MEASUREMENTS: Anthropometric profile, percentage of body fat (%BF), fasting serum insulin, and lipoprotein profile.RESULTS: Fasting insulin correlated significantly with body mass index (BMI), %BF, waist circumference (WC), central andperipheral skinfold thicknesses and sum of four skinfold thicknesses (

P4SF) in both sexes, and with systolic blood pressure and

waist–to hip circumference ratio (W–HR) in males only. Consistent increase in fasting insulin was noted with increasing values ofcentral skinfold thickness at each tertile of peripheral skinfold thickness, WC, and %BF. Central skinfold thickness correlated withfasting insulin even after adjusting for WC, W–HR, and %BF. The odds ratios (OR) (95% CI) of hyperinsulinemia (fasting insulinconcentrations in the highest quartile) were 4.7 (2.4–9.4) in overweight subjects, 8 (4.1–15.5) with high %BF, 6.4 (3.2–12.9)with high WC, 3.7 (1.9–7.3) with high W–HR, 6.8 (3.3–13.9) with high triceps skinfold thickness, 8 (4.1–15.7) with highsubscapular skinfold thickness, and 10.1 (5–20.5) with high

P4SF. In step-wise multiple logistic regression analysis, %BF [OR

(95% CI): 3.2 (1.4–7.8)] and ?4SF [OR (95% CI): 4.5 (1.8–11.3)] were independent predictors of hyperinsulinemia, similar toinsulin resistance assessed by HOMA (homeostatic model of assessment) in the study.CONCLUSION: A high prevalence of insulin resistance in postpubertal urban Asian Indian children was associated with excessbody fat, abdominal adiposity, and excess truncal subcutaneous fat. Primary prevention strategies for coronary heart disease anddiabetes mellitus in Asian Indians should focus on the abnormal body composition profile in childhood.

International Journal of Obesity (2004) 28, 1217–1226. doi:10.1038/sj.ijo.0802704

Published online 17 August 2004

Keywords: insulin resistance; Asian Indians; obesity; postpubertal children; truncal skinfolds

IntroductionThe prevalence of insulin resistance and diabetes mellitus is

particularly high in adult Asian Indians.1,2 These metabolic

factors are forerunners of the accelerated and severe athero-

sclerosis seen in Asian Indians in all geographic regions.3

While the determinants of insulin resistance and the

metabolic syndrome in adult Asian Indians continue to be

debated, generalized and regional obesity have been shown

to be important predictors.1,2

Studies in several ethnic groups show that metabolic

abnormalities associated with insulin resistance manifest

during childhood and adolescence.4–7 In particular, over-

weight and obese children and adolescents,8,9 and thoseReceived 23 October 2003; revised 4 February 2004; accepted 14 March

2004; published online 17 August 2004

*Correspondence: Dr A Misra, Department of Medicine, All India Institute

of Medical Sciences, New Delhi 110029, India.

E-mail: anoopmisra@metabolicresearchindia.com

Conflict of Interest: None

International Journal of Obesity (2004) 28, 1217–1226& 2004 Nature Publishing Group All rights reserved 0307-0565/04 $30.00

www.nature.com/ijo

having truncal obesity,10 are at a substantially increased risk

for the development of multiple cardiovascular risk factors.

Insulin resistance as estimated by the hyperinsulinemic–

euglycemic clamp technique11 and by surrogate markers12

has been reported in children and adolescents. Further,

fasting hyperinsulinemia in early life predicted the develop-

ment of dyslipidemia5 and cardiovascular risk13 in adult-

hood.

Whereas high prevalence rates of hyperinsulinemia,

insulin resistance and the metabolic syndrome have been

documented in adult Asian Indians, only three investigators

have studied children, adolescents, and young adults.14–16

These studies have dealt with limited numbers of offspring of

migrant Asians who are generally more affluent, and have an

acculturated diet and lifestyle as compared to those living in

India. A population-based study of insulin resistance,

anthropometric, and cardiovascular risk factor profile in

postpubertal Asian Indian children has not been carried out.

Such a study is important since clues for the development of

high cardiovascular risk and type II diabetes mellitus in adult

Asian Indians may manifest at a young age, reflected by the

increasing prevalence of overweight and obesity among

urban adolescents.17 The findings of such a study would also

be important to the children of a rapidly growing population

of migrant Asian Indians settled in the USA, Canada, the UK,

and other countries.

We hypothesized that urban postpubertal Asian Indian

children are insulin resistant and manifest other features of

the metabolic syndrome. The insulin resistance in these

children is related to excess body fat and to regional excess of

fat. The present study aimed to examine the relationship of

surrogate markers of insulin resistance with the measures of

generalized and regional obesity, anthropometric profile,

and serum lipoproteins in urban postpubertal children in

north India.

Materials and methodsStudy design and sampling method

The data of the subjects included in this study were taken

randomly from a large ongoing Epidemiological Study of

Adolescents and Young adults (ESAY study) comprising

postpubertal children and young adults 14–25 y of age from

schools and colleges located in southwest New Delhi. The

details of the sampling methods have been reported earlier.18

The multistage cluster sampling, based on the modified

World Health Organization Expanded Program of Immuni-

zation Sampling Plan,19 was adapted for collecting an

appropriately representative sample from high schools and

colleges in the ESAY study. Out of the target sample of 4000

subjects for the ESAY study, a total of 1795 subjects had been

recruited till May 2003. A total of 250 subjects (155 males

and 95 females) 14–18 y of age were recruited from the

database of ESAY study for the current investigation.

Approval for conducting the study was obtained from the

Director of Education, Ministry of Education, Government

of New Delhi. The study was initiated in August 2000 after

approval from the institutional ethics committee. A written

informed consent was obtained from subjects Z18 years of

age. For subjects o18 years of age, written informed consent

was obtained from their parents.

Clinical profile and measurements

A brief clinical history, demographic, anthropometric, and

clinical profiles were recorded. The same physician recorded

the anthropometric measurements according to the meth-

ods described earlier.20 Briefly, height (to the nearest 0.5 cm),

weight (to the nearest 0.1 kg), waist and hip circumferences,

and skinfold thickness measurements at four sites (biceps,

triceps, subscapular, and suprailiac) were obtained. Body

mass index (BMI), waist-to-hip circumference ratio (W–HR),

central skinfold thickness (sum of subscapular and suprailiac

skinfold thicknesses), peripheral skinfold thickness (sum of

biceps and triceps skinfold thicknesses), sum of four skinfold

thickness (P

4SF), and central:peripheral skinfolds ratio (C:P

ratio) were calculated. The reproducibility of the skinfold

thickness measurement was assessed for all individual

skinfolds and the coefficient of variation for the measure-

ment error was estimated as o10%.

A four-point bioelectrical impedance apparatus (Tanita

TBF 300, TANITA Corp., Tokyo, Japan), validated for Asian

children and adolescents,21 was used to measure the

percentage of body fat (%BF), according to a standard

procedure described earlier.18

Blood pressure was measured by a standard mercury

sphygmomanometer (Industrial Electronic and Allied Pro-

ducts, Pune, India), after the subject had rested for 5 min in

the sitting position, using the appropriate cuff size and phase

5 Korotkoff sounds were taken for diastolic blood pressure

categorization. In case of an abnormal blood pressure

recording, another reading was obtained after 5 min rest

and the mean of the two values was taken for the final

record. The same physician measured the blood pressure

using the same instrument for all the subjects and the

instrument was periodically validated against a Hawksley

Random Zero Sphygmomanometer (Hawksley, Lancing,

Sussex, UK).

Metabolic parameters

Venous blood samples were drawn after a 12-h overnight fast

and transported immediately to the laboratory where the

serum from blood samples was separated in cold centrifuge

(Plasto Crafts, Mumbai, India) at 2000 rpm for 10 min and

stored in a deep freezer at �201C. Fasting blood glucose

(FBG), total cholesterol (TC), serum triacylglycerol (TG), and

HDL concentrations were estimated the same day in the

Metabolic Research Laboratory using the respective reagent

kits (Randox Laboratory, San Francisco, CA, USA) on a

semiautomated analyzer (das srl, palombaraSabina, Italy).

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

The value of LDL was calculated according to Freidewald’s

equation if serum TG concentrations were o400 mg/dL.22

Serum insulin assay

Serum insulin was determined using a commercially avail-

able radioimmunoassay kit (Medicorp, Montreal, Canada).

The principle of this assay was based on competitive binding

of labeled and unlabeled insulin to the binding sites of anti-

insulin antibodies immobilized on inner wall of the tube.

The radioactivity of iodinated insulin bound to the anti-

insulin antibodies on solid phase was measured using a

gamma counter (Stratec Biomedical Systems, pfrozheim,

Germany). The intra- and interassay percentage coefficient

variables were 2.6% and 3%, respectively.

Definitions

Since cutoffs to define normal values of anthropometric and

metabolic parameters were not available for the Asian Indian

children in the age group of 14–18 y, the percentile data

analyzed from the ESAY study cohort (n¼1795) were used as

the reference. Overweight was defined as BMI 485th

percentile (Table 1). Values 485th percentile were used as

cutoffs for defining high values of %BF, waist circumference

(WC), W–HR, triceps and subscapular skinfold thickness, andP

4SF (Table 1). For lipoproteins, except HDL, cutoff values

495th percentiles of the reference population were used to

define hypercholesterolemia and high concentrations of TG

and LDL (Table 1).18 Low concentrations of HDL were

defined as values less than 5th percentile of the reference

population.18 Hypertension was defined as persistent eleva-

tion of systolic blood pressure (SBP) 4130 mmHg and/or

diastolic blood pressure (DBP) 484 mmHg (495th percen-

tile) and those on treatment with antihypertensive medica-

tion. The criteria defined by American Diabetic Association

were used to diagnose impaired fasting glucose (FBG Z6.1

and o7.0 mmol/l) and diabetes (FBG Z7.0 mmol/l).23 Smok-

ing was defined as any amount of current cigarette smoking,

irrespective of the frequency; the prevalence was 3.2% in

males, whereas none of the females smoked.

Insulin resistance was measured by two surrogate mea-

sures: fasting hyperinsulinemia and homeostasis model

assessment (HOMA).24 Subjects were categorized according

to quartiles of fasting insulin concentrations (mU/ml) as

follows: malesFquartile 1: r11.5, quartile 2: 11.6–14.2,

quartile 3: 14.3–18.7, and quartile 4: 418.7; femalesFquar-

tile 1: r15.8, quartile 2: 15.9–18.4, quartile 3: 18.5–23.7, and

quartile 4: 423.7. Fasting insulin concentrations in the first

three quartiles were defined as normal (normoinsulinemia),

whereas insulin concentrations in the fourth quartile were

defined as high (hyperinsulinemia). The value of HOMA was

calculated by the following equation:24

(fasting insulin (mU/ml)� fasting glucose (mmol/l))/22.5

The value of HOMA denoting various degrees of insulin

resistance was termed as HOMA-IR.

Statistical analysis

The data were entered in an Excel spreadsheet (Microsoft

Corp, Washington, USA). The distributions of anthropo-

metric and biochemical parameters were confirmed for

approximate normality. We used mean and standard devia-

tions to summarize the variables. The differences in anthro-

pometric parameters in males and females were compared

using the Z-test. As fasting insulin concentrations were

nonnormally distributed, log transformation was carried out

to calculate partial correlations among fasting insulin

concentrations and various factors, adjusting for age. One-

way analysis of variance (ANOVA) followed by Bonferroni

post hoc test, if required, was used to compare mean values of

various clinical, anthropometric, and biochemical para-

meters across quartiles of fasting insulin and HOMA-IR.

Fasting insulin concentrations was categorized as binary

outcome variable (hyperinsulinemia or normoinsuline-

mia). The analysis for risk factors was performed in three

Table 1 Definitions and prevalence of abnormal values of anthropometric and biochemical parameters

Males Females

Variables Definitiona % prevalence Definitiona % prevalence Overall % prevalence

BMI (kg/m2) 423.0 16.7 423.0 21 18.3

Percentage of body fat 428.5 24.7 434.0 16.8 23.3

Waist circumference (cm) 479.0 17.3 476.0 16.8 17.1

Waist-to-hip circumference ratio 40.86 14.1 40.84 17.9 15.5

Triceps skinfold thickness (mm) 419.7 19.2 421.0 12.6 16.7

Subscapular skinfold thickness (mm) 421.7 22.4 425.0 17.9 20.7

Sum of four skinfolds (mm) 471.0 21.8 486.7 14.7 19.1

Total cholesterol (mmol/l) 44.36 13.6 44.67 12.6 13.2

Serum triacylglycerol (mmol/l) 41.33 14.8 41.33 17.9 16.0

LDL (mmol/l) 42.78 14.2 42.94 13.7 14.0

HDL (mmol/l) o0.98 9.0 o0.98 11.6 10.0

aAbnormal values defined as values 485th percentile for anthropometric parameters, 495th percentile for total cholesterol, triacylglycerol, and LDL, and o5th

percentile for HDL.

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

stages: first, the associations of hyperinsulinemia and high

HOMA-IR with various measures of obesity were assessed

using the Pearson’s w2 test. Subsequently, binary logistic

regression analysis was used to quantify the strength of the

association (odds ratios (OR) and 95% CI) of anthropometric

parameters and various measures of obesity with hyperinsu-

linemia and high HOMA-IR. Finally, factors showing statis-

tically significant association with the outcome variable were

simultaneously considered in the multivariate logistic re-

gression model to determine the independent risk factors of

hyperinsulinemia and high HOMA-IR. STATA 8.0, Inter-

cooled version statistical software25 was used for the

statistical analysis. In this study, statistical significance was

considered at a P-value of o0.05.

ResultsDemographic and anthropometric profiles

Elevated blood pressure was recorded in 4. 4% subjects (4.5%

males and 4.2% females). The mean values of BMI and WC

were comparable among males and females, but males had

higher W–HR as compared to females. Females had higher

mean values of all individual skinfolds thickness, central

skinfolds, peripheral skinfolds, C:P ratio,P

4SF, and %BF as

compared to males (Table 2). Overweight was observed in

18.3% and high values of %BF in 23.3% subjects (Table 1).

Biochemical parameters

None of the subjects had impaired fasting glucose or

diabetes. The mean values of all the lipid parameters, except

TG, were significantlly higher in females than in males

(Table 2). For both males and females, the mean values of

lipoproteins were not statistically different between normal

weight and overweight subjects except higher levels of HDL

in normal weight females (1.3770.27 mmol/l) as compared

to overweight females (1.2170.27 mmol/l, P¼0.02). No

significant difference in the prevalence of any variable of

dyslipidemia was observed between normal weight and

overweight subjects.

Fasting insulin concentrations and HOMA-IR values

Females had higher mean fasting insulin concentrations and

HOMA-IR values as compared to males (Table 2). The mean

fasting insulin concentrations were higher in overweight

subjects (22.577.0 mU/ml) and in subjects with high %BF

(22.577.2 mU/ml) as compared to normal weight subjects

(16.375.7 mU/ml, Po0.001) and subjects with normal %BF

(16.075.4 mU/ml, Po0.001). Similarly, mean fasting insulin

concentrations were higher in subjects with high values of

triceps skinfold thickness,P

4SF, WC, and W–HR as

compared to subjects with lower values of these parameters

(Po0.001 for all variables). The pattern of distribution of

HOMA-IR values was similar to that of fasting insulin

concentrations.

With increasing quartiles of fasting insulin, a significant

increasing trend in BMI, %BF, thickness of all individual

skinfolds, central and peripheral skinfold thicknesses, andP

4SF was observed in both sexes, whereas a significant

increasing trend in SBP, WC, W–HR, and C:P ratio was

observed only in males (Table 3). Among hyperinsulinemic

males, the mean values of triceps skinfold thickness

(20.6 mm) represented the 88th percentile and subscapular

skinfold thickness (25.4 mm) 89th percentile, in hyperinsu-

linemic females, triceps skinfold thickness (18.5 mm) repre-

sented the 73rd percentile and subscapular skinfold

thickness (21 mm) 74th percentile in reference to percentile

data of skinfold thickness from the ESAY study cohort. No

significant trend was observed with any of the lipoproteins

in either males or females. Finally, the distribution of various

anthropometric and biochemical parameters across quartiles

of HOMA-IR was similar to that observed across quartiles of

fasting insulin.

In males, the prevalence of fasting hyperinsulinemia was

significantly higher in those with high values of BMI, %BF,

WC, W–HR, and triceps and subscapular skinfold thicknesses

(Figure 1a), and in females, it was significantly higher in

subjects with high values of %BF, triceps and subscapular

skinfold thicknesses, andP

4SF (Figure 1b) as compared to

those with normal values of these variables.

Table 2 Anthropometric and biochemical parametersa

Variables

Males

(n¼155)

Females

(n¼95) P-value

Age (y) 16.2 (1.2) 17.2 (1.2) o0.001

Systolic blood pressure (mmHg) 115.9 (9.5) 111.4 (9.3) o0.001

Diastolic blood pressure (mmHg) 76.1 (6.6) 76.4 (6.9) NS

Anthropometric parameters

BMI (kg/m2) 20.3 (3.8) 19.9 (3.6) NS

%BF 24.0 (8.4) 26.5 (8.9) 0.02

Waist circumference (cm) 71.3 (9.6) 69.4 (8.8) NS

Waist-to-hip circumference ratio 0.83 (0.05) 0.79 (0.07) o0.001

Skinfold thickness (mm)

Biceps 6.7 (4.1) 8.7 (3.8) o0.001

Triceps 13.8 (7.0) 16.0 (4.6) o0.01

Subscapular 15.7 (9.8) 17.6 (7.4) NS

Suprailiac 15.2 (9.9) 22.4 (8.0) o0.001

Central skinfolds 31.0 (19.2) 40.0 (14.6) o0.001

Peripheral skinfolds 20.5 (10.8) 24.8 (7.8) o0.001

Central: peripheral skinfolds ratio 1.49 (0.35) 1.64 (0.41) 0.003

Sum of four skinfolds (P

4SF) 51.4 (29.5) 64.8 (21.1) o0.001

Biochemical parameters

Fasting blood glucose (mmol/l) 5.04 (0.54) 4.86 (0.44) 0.01

Glycosylated hemoglobin (g %) 5.5 (0.5) 5.5 (0.6) NS

Total cholesterol (mmol/l) 3.69 (0.63) 4.06 (0.52) o0.001

Serum triacylglycerol (mmol/l) 1.01 (0.39) 1.02 (0.35) NS

HDL (mmol/l) 1.20 (0.19) 1.34 (0.28) o0.01

LDL (mmol/l) 2.01 (0.68) 2.26 (0.59) o0.01

Fasting serum insulin (mU/ml) 16.0 (5.7) 19.8 (6.7) o0.01

HOMA-IR 3.6 (1.4) 4.3 (1.6) o0.01

aMean (s.d.). NS, not significant; HOMA-IR, values of insulin resistance were

calculated by homeostasis model of assessment. Higher values denote

increasing magnitude of insulin resistance.

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

Correlations of fasting insulin and HOMA-IR

Correlations of HOMA-IR with anthropometric parameters

were almost identical to those observed with fasting insulin

concentrations, hence only the latter are reported. For both

sexes, fasting insulin concentrations correlated significantly

with BMI, %BF, WC, individual skinfold thickness, central

and peripheral skinfold thickness, andP

4SF; correlations

being stronger in males (Table 4). Significant correlations of

fasting insulin concentrations with SBP, W–HR, and C:P ratio

were observed in males only (Table 4). No significant

correlation between fasting insulin concentrations and any

of the lipid parameters was observed in either sex. Among

the skinfolds, triceps and suprailiac skinfold thickness was

more strongly correlated with fasting insulin concentrations.

Central and peripheral skinfold thickness correlated more

strongly with fasting insulin concentrations as compared

to WC, W–HR, and C:P ratio. The correlation of central

skinfold thickness with fasting insulin remained significant

after adjusting for peripheral skinfold thickness (males:

r¼0.22, P¼0.007), WC (males: r¼0.34, Po0.001), W–HR

(males: r¼0.63, Po0.001; females: r¼ 0.30, P¼0.003), and

%BF (males: r¼0.42. Po0.001). On the other hand, after

Table 3 Distribution of anthropometric and biochemical parametersa across quartiles (Q) of fasting serum insulin concentrations

Fasting serum insulin quartiles (mU/ml) One-way ANOVA

Variable Q1 Q2 Q3 Q4 F-value P-value

Males (n¼155)

SBP (mmHg) 111.2 (10.6) 113.3 (7.8) 118.4 (7.2)b 120.5 (8.9)c,d 9.4 o0.001

DBP (mmHg) 74 (6.8) 75.9 (5.1) 77.3 (5.9) 77.3 (8.0) 2.3 NS

BMI (kg/m2) 17.7 (2.1) 18.4 (2.2) 21.3 (3.0)b,e 23.9 (3.8)c,d,f 38.8 o0.001

%BF 19.1 (5.5) 19.5 (4.9) 25.9 (7.6)b,e 32.1 (7.7)c,d,f 33.8 o0.001

WC (cm) 64.7 (4.7) 66.2 (5.6) 73.5 (7.4)b,e 80.7 (10.0)c,d,f 40.8 o0.001

W–HR 0.81 (0.06) 0.80 (0.03) 0.83 (0.04) 0.86 (0.06)c,d 11.3 o0.001

Skinfold thickness

Biceps 4.4 (1.4) 4.8 (1.9) 7.2 (3.4)b,e 10.4 (5.3)c,d,f 26.2 o0.001

Triceps 9.1 (3.1) 9.9 (3.6) 15.6 (5.2)b,e 20.6 (7.7)c,d,f 40.8 o0.001

Subscapular 9.4 (2.6) 10.6 (3.8) 17.6 (7.5)b,e 25.4 (12.0)c,d,f 38.2 o0.001

Suprailiac 9.0 (3.7) 9.8 (5.1) 16.3 (8.0)b,e 25.8 (10.5)c,d,f 43.8 o0.001

Centralg 18.4 (5.7) 20.4 (8.0) 33.9 (148)b,e 51.2 (22.0)c,d,f 44.6 o0.001

Peripheralh 13.5 (4.2) 14.7 (5.0) 22.7 (8.1)b,e 30.9 (12.8)c,d,f 37.5 o0.001

C:P ratio 1.40 (0.30) 1.41(0.35) 1.49 (0.33) 1.66 (0.66)c,d,f 5.1 0.002P

4SF 31.9 (9.3) 35.1 (12.3) 56.6 (22.2)b,e 82.1 (33.9)c,d,f 44.7 o0.001

FBG (mmol/l) 5.02 (0.53) 5.1 (0.49) 4.97 (0.61) 5.02 (0.57) 0.4 NS

TC (mmol/l) 3.66 (0.6) 3.82 (0.75) 3.62 (0.58) 3.67 (0.57) 0.8 NS

TG (mmol/l) 0.93 (0.35) 0.99 (0.43) 1.05 (0.36) 1.08 (0.42) 1.1 NS

HDL (mmol/l) 1.21 (0.22) 1.16 (0.21) 1.25 (0.17) 1.21 (0.18) 1.5 NS

LDL (mmol/l) 2.01 (0.67) 2.13 (0.84) 1.89 (0.62) 1.97 (0.62) 1.5 NS

Females (n¼95)

SBP (mmHg) 108.9 (11.5) 112.8 (8.3) 110.0 (8.7) 113.8 (7.9) 1.5 NS

DBP (mmHg) 72.6 (8.6) 76.0 (5.6) 73.7 (7.0) 75.6 (6.0) 1.3 NS

BMI (kg/m2) 18.1 (2.5) 19.4 (2.9) 20.0 (3.2) 22.2 (4.5)c 5.9 o0.001

%BF 22.1 (6.4) 25.6 (8.1) 26.7 (7.6) 31.9 (10.6)c 5.6 0.001

WC (cm) 66.3 (8.7) 69.6 (7.9) 69.6 (7.1) 72.0 (10.7) 1.7 NS

W–HR 0.79 (0.06) 0.80 (0.06) 0.79 (0.06) 0.77 (0.07) 0.5 NS

Skinfold thickness

Biceps 7.7 (3.0) 8.2 (3.6) 8.1 (3.0) 11.1 (4.8)c 4.2 0.007

Triceps 14.1 (4.5) 15.2 (3.5) 16.3 (4.1) 18.5 (5.1)c 4.3 0.006

Subscapular 14.4 (5.6) 17.6 (8.2) 17.5 (6.7) 21.0 (7.9)c 3.3 0.02

Suprailiac 19.5 (5.9) 20.8 (8.7) 22.1 (6.5) 27.6 (8.7)c,d 5.2 0.002

Centralg 33.9 (10.6) 38.4 (16.2) 39.6 (12.3) 48.6 (15.4)c 4.7 0.004

Peripheralh 21.8 (6.8) 23.5 (6.6) 24.3 (6.5) 29.6 (9.4)c 4.8 0.003

C:P ratio 1.59 (0.38) 1.61 (0.39) 1.64 (0.40) 1.70 (0.50) 0.3 NSP

4SF 55.7 (16.1) 61.9 (22.0) 63.9 (17.3) 78.2 (22.7)c 5.4 0.001

FBG (mmol/l) 4.81 (0.43) 4.84 (0.5) 4.92 (0.38) 4.91 (0.5) 0.3 NS

TC (mmol/l) 4.05 (0.59) 4.05 (0.4) 4.05 (0.66) 4.07 (0.42) 0.01 NS

TG (mmol/l) 0.96 (0.32) 1.02 (0.31) 0.93 (0.35) 1.19 (0.38) 2.8 NS

HDL (mmol/l) 1.3 (0.23) 1.22 (0.32) 1.44 (0.31) 1.38 (0.20) 3.0 NS

LDL (mmol/l) 2.31 (0.64) 2.39 (0.53) 2.18 (0.68) 2.14 (0.47) 0.9 NS

aMean (s.d.). Q1 males r11.5, femalesr15.8; Q2 males 11.6–14.2, females 15.9–18.4; Q3 males 14.3–18.7, females 18.5–23.7; Q4 males Z18.8, femalesZ23.8.bQ1 vs Q3. cQ1 vs Q4. dQ2 vs Q4. eQ2 vs Q3. fQ3 vs Q4. gSum of subscapular and suprailiac skinfolds thickness. hSum of biceps and triceps skinfolds thickness. SBP,

systolic blood pressure; DBP, diastolic blood pressure; BMI, body mass index; %BF, percentage of body fat; WC, waist circumference; W–HR, waist-to-hip

circumference ratio; C:P ratio, central-to-peripheral skinfold thickness ratio; S4SF, sum of four skinfolds thickness; FBG, fasting blood glucose; TC, total cholesterol;

TG, triacylglycerol; NS¼not significant.

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

adjusting for central skinfold thickness, the correlations of

peripheral skinfold thickness, WC, W–HR with fasting

insulin became nonsignificant in both sexes, whereas the

correlation of %BF with fasting insulin remained significant

only in females (r¼0.25, P¼0.01). The correlation of C:P

ratio with fasting insulin remained significant after adjusting

for peripheral skinfold thickness in males (r¼0.22,

P¼0.007), whereas it became nonsignificant after adjusting

for central skinfold thickness.

Keeping the value of peripheral skinfold thickness con-

stant, increasing central skinfold thickness was associated

with a consistent increase in fasting insulin concentrations

(Figure 2). On the other hand, keeping the central skinfold

thickness value constant, no such consistent relationship of

fasting insulin concentration was observed with increasing

peripheral skinfold thickness. Similarly, at each tertile of %BF

and WC, increasing value of central skinfold thickness was

associated with a consistent increase in fasting insulin

concentrations. On keeping the central skinfold thickness

constant, no consistent increase in fasting insulin concen-

tration was observed with increasing %BF and WC.

The OR for fasting hyperinsulinemia in subjects with high

values of various anthropometric parameters and measures

of obesity were calculated including gender in the regression

equation (Table 5). High values of BMI, %BF, WC, W–HR,

triceps and subscapular skinfold thickness, andP

4SF were

observed more frequently in subjects with hyperinsulinemia

than those with normoinsulinemia (Table 5). The odds of

hyperinsulinemia in subjects with high BMI were 4.7 times,

high %BF 8 times, high WC 6.4 times, high W–HR 3.7 times,

high triceps skinfold 6.8 times, high subscapular skinfold

thickness eight times, and highP

4SF 10.1 times as

Figure 1 Prevalence of high values of anthropometric parameters and other

measures of obesity (all variables485th percentile) among males (a) and

females (b) with normoinsulinemia and hyperinsulinemia. ‘Hyperinsulinemia’

was defined as fasting serum insulin concentrations in the fourth quartile (in

males418.7 mU/ml and in females 423.7 mU/ml). BMI, body mass index;

%BF, percentage of body fat; WC, waist circumference; W–HR, waist-to-hip

circumference ratio; TR, triceps skinfold thickness; SS, subscapular skinfold

thickness;P

4SF, sum of four skinfold thicknesses. The values of all

anthropometric and obesity measures were considered high when 485th

percentile of the reference population.

Table 4 Partial correlation coefficients adjusted for age

Fasting serum insulin HOMA-IR

Variable(s) Males Females Males Females

Systolic blood pressure 0.30a 0.07 0.26b 0.08

BMI (kg/m2) 0.62a 0.39a 0.56a 0.39a

%BF 0.62a 0.38a 0.58a 0.36a

WC (cm) 0.63a 0.25c 0.58a 0.28b

W–HR 0.38a 0.01 0.38a 0.008

Skinfold thickness

Biceps 0.61a 0.25c 0.61a 0.28b

Triceps 0.69a 0.30b 0.67a 0.28b

Subscapular 0.65a 0.25c 0.64a 0.23c

Suprailiac 0.68a 0.30b 0.66a 0.31b

Central 0.68a 0.29b 0.66a 0.28b

Peripheral 0.67a 0.30b 0.66a 0.30b

C:P ratio 0.24b 0.05 0.22b 0.05P

4SF 0.69a 0.31b 0.68a 0.31b

aPo0.001; bPo0.01; cPo0.05; BMI, Body mass index; %BF, Percentage of

body fat; WC, Waist circumference; W–HR, waist-to-hip circumference ratio;

central skinfold thickness, sum of subscapular and suprailiac skinfolds

thickness; peripheral skinfold thickness, sum of biceps and triceps skinfolds

thickness; C:P ratio, ratio of central-to-peripheral skinfolds thickness; S4SF,

sum of four skinfolds thickness; HOMA-IR, value of insulin resistance as

calculated by homeostasis model of assessment.

Figure 2 Distribution of mean levels of fasting serum insulin (mU/ml) by

tertiles of central (sum of subscapular and suprailiac skinfolds) and peripheral

(sum of biceps and triceps skinfolds) skinfold thicknesses. Central skinfold

thickness tertiles (mm): tertile 1, upto 23.7; tertile 2, 23.8–38.7; tertile 3,

438.7. Peripheral skinfold thickness tertiles (mm): tertile 1, upto 17; tertile 2,

17.1–24.7; tertile 3, 424.7.

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

compared to those with normal values of these variables,

respectively. Finally, when all the anthropometric para-

meters were considered together in stepwise multiple

regression analysis, %BF (OR (95% CI): 3.2 (1.4–7.8);

P¼0.008) andP

4SF (OR (95% CI): 4.5 (1.8–11.3);

P¼0.001) were independent predictors of hyperinsulinemia

(Table 5). The odds of high HOMA-IR in subjects with high

values of various measures of obesity were similar to those

observed for fasting hyperinsulinemia.

DiscussionThis is the first study to examine comprehensively the

relationships of fasting insulin concentrations and HOMA-IR

with anthropometric parameters, body fat and its patterning,

and serum lipoproteins in urban postpubertal Asian Indian

children using proper sampling methodology. Important

observations included a high prevalence of insulin resistance

in postpubertal children that correlated with overweight,

abdominal obesity, high subcutaneous truncal adiposity, and

excess body fat. In contrast to earlier data,11 no relationship

with FBG and lipid parameters was observed across quartiles

of fasting insulin.

Three earlier studies showed higher fasting insulin con-

centrations and HOMA-IR values in South Asians or Asian

Indians as compared to other ethnic groups,14–16 but did not

assess their relationships with peripheral and truncal

subcutaneous fat, abdominal adiposity, and body fat, and

included either a small number of prepubertal children or

young adults. Whincup et al14 studied surrogate markers of

insulin resistance in an unspecified number of Asian Indian

children among 40 South Asian prepubertal children (9–11 y

age) in a population-based study. South Asian children in

this study had ancestral origins from several south Asian

countries (Bangladesh, Pakistan, Sri Lanka, Nepal, etc) and

might have a different cardiovascular risk factor profile than

Asian Indians.26 Dickinson et al15 studied 10 lean young

adult Asian Indian volunteers using the hyperinsulinemic–

euglycemic clamp and the study of Walker et al16 did not

have complete data. Studies in India, which have shown

relationship of insulin resistance syndrome with low birth

weight, were carried out in prepubertal children and were

hospital based.27

Compared to the historical data of Black and White

children of similar age groups, Asian Indian children in the

present study had thicker central skinfolds despite having

lower BMI and WC (Table 6). Further, increasing tertiles of

truncal skinfold thickness were associated with higher

fasting insulin concentrations at any tertile of peripheral

skinfold thickness, %BF, and WC in the current study.

Truncal skinfold thickness independently predicts cardio-

vascular risk28 and type II diabetes mellitus29 in adults, and

correlates closely to postglucose load hyperinsulinemia in

children.9 A few investigators have shown that adult South

Asian and Asian Indians of both sexes have thicker truncal

skinfolds than Caucasians.30,31 Interestingly, as compared to

Caucasians, greater truncal skinfold thickness in adult Asian

Table 5 OR (95% CI) of hyperinsulinemia as binary outcome variable with various anthropometric parameters and measures of obesity as predictors

Variables Hyperinsulinemia,a n (%) Normoinsulinemia, n (%) w2, P-value Unadjusted OR (95% CI) Adjusted OR (95% CI)

Gender

Males 39 (62.9) 117 (61.9) 0.88 1 FFemales 23 (37.1) 72 (38.1) o0.01 0.95 (0.5–1.7)

BMI (kg/m2)

Normal 38 (61.3) 167 (88.4) 22.8, 1 FHighb 24 (38.7) 22 (11.6) o0.01 4.7 (2.4–9.4)c

% BF

Normal 27 (45) 164 (86.8) 44.5, 1 1

Highb 33 (55) 25 (13.2) o0.01 8.0 (4.1–15.5)c 3.2 (1.4–7.8)d

WC (cm)

Normal 37 (59.7) 171 (90.5) 31.1, 1 FHighb 25 (40.3) 18 (9.5) o0.01 6.4 (3.2–12.9)c

W–HR

Normal 41 (66.1) 166 (87.8) 15.2, 1 FHighb 21 (33.9) 23 (12.2) o0.01 3.7 (1.9–7.3)c

Triceps skinfold thickness

Normal 37 (59.7) 172 (91) 32.9, 1 FHighb 25 (40.3) 17 (9) o0.01 6.8 (3.3–13.9)c

Subscapular skinfold thickness

Normal 31 (50) 168 (88.9) 43.0, 1 FHighb 31 (50) 21 (11.1) o0.01 8.0 (4.1–15.7)c

Sum of four skinfolds (S4SF)

Normal 31 (50) 172 (91) 50.7, 1 1

Highb 31 (50) 17 (9) o0.01 10.1 (5–20.5)c 4.5 (1.8–11.3)d

BMI, Body mass index; %BF, Percentage of body fat; WC, Waist circumference; W-HR, Waist-to-hip circumference ratio. aHyperinsulinemia, fasting serum insulin

levels (in mU/ml) Z18.8 in males and Z23 in females. bHigh values of measures of obesity were defined as values 485th percentile for each variable. cPo0.01.dPo0.001.

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

Indians was associated with a higher magnitude of hyper-

insulinemia at similar values of BMI and %BF, and lower

WC.31 Further, despite having a lower body weight and

triceps skinfold thickness, Asian Indian neonates had

preserved subscapular skinfolds and higher insulin concen-

trations as compared to Caucasian neonates.32

It appears that excess truncal subcutaneous adipose tissue

is an important determinant of insulin resistance in adult

Asian Indians and, in this study, we found similar observa-

tions in postpubertal children. It is known that subcuta-

neous adipose tissue is closely correlated to insulin resistance

in adults,33 and some investigators believe that this correla-

tion is stronger than that of intra-abdominal fat.33 Specifi-

cally, similar to our data, sum of three central skinfold

thicknesses showed close correlation with 1-h insulin

response independent of the peripheral skinfolds in Black

and White children and adolescents.10

Among hyperinsulinemic postpubertal children, we re-

corded the prevalence of overweight as defined by BMI and

excess %BF to be B39 and 55%, respectively. These data are

consistent with our previous study, which showed high %BF

at a normal range of BMI in urban adult Asian Indians,20,34

which is associated with insulin resistance,35 dyslipidemia,

and type II diabetes mellitus.36 Although no similar data are

available for Asian Indian children, we have recently

reported high C-reactive protein concentrations in 13% of

adolescents and young adults (age range: 14–24 y) from the

same cohort of the ESAY study.18 In conjunction with the

data of the current study, we now have evidence of

substantial prevalence of subclinical inflammation

(B22%)18 and hyperinsulinemia (B59%) in overweight

urban postpubertal Asian Indian children and young adults,

portending a high risk of glucose intolerance and coronary

heart disease later in life.

Interethnic differences in the surrogate measures of

abdominal obesity are highlighted in Table 6. The mean

height of Asian Indian children in the present study was

significantly lower as compared to Black and White chil-

dren.37 Interestingly, Asian Indian children had a lesser WC

as compared to Black and White children37,38 of comparable

age, but the W–HR was higher. The latter could be due to less

fat-free mass of the lower limbs of Asian Indians, resulting in

lower value of hip circumference. Lower realized height of

Asian Indians may cause lesser length and fat-free mass of

lower extremities. Importantly, both WC and W–HR did not

independently predict hyperinsulinemia in the presence of

%BF andP

4SF. These findings are intriguing given the

previous data showing a close pathophysiological relation-

ship of abdominal adiposity with insulin resistance in Asians

Indians.1,39 However, we used surrogate measures of abdom-

inal obesity and did not estimate the intra-abdominal fat.

Further, a different relationship of insulin resistance and

abdominal obesity may exist in adults and the elderly

compared to postpubertal children. Finally, children who

have a low birth weight and remain lighter in childhood may

manifest abdominal obesity only during the adulthood.40

Although we did not address this hypothesis, it is likely that

many children in our study had low birth weight since it is

observed in B1/3rd urban children in India.27

We did not attempt to analyze the lifestyle profile as a

possible determinant of the observed anthropometry and

insulin resistance in the present study. However, we recently

reported nearly 2/3rd of 659 subjects of ESAY study to be

sedentary in a preliminary communication,41 which may be

responsible for some of the adverse anthropometric and

metabolic variables in the present study. An imbalanced

dietary profile, including high saturated fat and low

dietary fiber intake, has also been recorded in the ESAY

study cohort42 and may constitute other potential determi-

nants for the adverse anthropometric and metabolic data

shown by us.

These data suggest that the important proatherogenic

determinants for coronary heart disease in Asian Indians

are already manifesting in postpubertal children. Cogni-

zance should be taken of these important observations

for the formulation of primary prevention policies for

coronary heart disease and type II diabetes mellitus for

Asian Indians

Table 6 Comparisons of anthropometry and body fat patterning of postpubertal children of three ethnic groups

Malesa Femalesa

Variables White children Black children Asian Indians (n¼155) White children Black children Asian Indians (n¼95)

Height (cm) 168713.0b 170710.0c 16576.4d,e 16178.0f 16277.0g 15576.0d,e

BMI (kg/m2) 22.274.2h 22.674.2i 20.373.8d,e 22.374.5j 23.976.2k 19.973.6d,e

WC (cm) 78.0713.0b 79.0711.0c 71.379.6e 77.0714.0f 77.0713.0g 69.478.8d,e

W–HR 0.8170.05b 0.8170.05c 0.8370.05d,e 0.7770.06f 0.7670.05g 0.7970.07e

Skinfold thickness (mm)

Triceps 10.476.5h 11.777.9i 13.877.0d,e 15.077.4j 17.378.9k 16.074.6

Subscapular 11.077.5h 12.277.9i 15.779.8d,e 14.478.0j 17.779.8k 17.677.4d

Suprailiac 12710b 13.077.0c 15.279.9 18.0710.0f 19.0711.0g 22.478.0d,e

BMI, Body mass index; WC, Waist circumference; W-HR, Waist-to-hip circumference ratio. aFor White and Black children, data from Mensah et al (mean age:

15.372.3 y, 37) and Park et al (age range: 13–17 y, 38), respectively, for Asian Indian children: present study (age range: 14–18 y). bn¼43. cn¼74. dP o0.05 White

vs Asian Indian children. eP o0.05 Black vs Asian Indian children. fn¼ 38. gn¼70. hn¼384. in¼ 174. jn¼431. kn¼ 253. All data in mean7s.d.

Insulin resistance in postpubertal Asian Indian childrenA Misra et al

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International Journal of Obesity

Acknowledgements

The study was funded by a grant from the Department of

Science and Technology, Ministry of Science and Technol-

ogy, Government of India, New Delhi. The authors are

thankful to Ministry of Education, Government of New

Delhi for their assistance in conducting the study. Mr

Ramesh Giri assisted in anthropometry and body fat

measurement, Mr Inder Taneja, Mr Gian Chand, and Mrs

Alice Jacob performed biochemical investigations and in-

sulin assay, and Mr RL Taneja supervised the quality control

of biochemical tests. The cooperation of the children who

took part in the study, and the help extended by the

principals, teachers, and staff of the various schools and

colleges where the study was conducted is greatly appre-

ciated.

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