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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2005-1253
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The Journal of Clinical Endocrinology & Metabolism Vol. 91, No. 1 93-97
Copyright © 2006 by The Endocrine Society

Ethnicity Modifies the Effect of Obesity on Insulin Resistance in Pregnancy: A Comparison of Asian, South Asian, and Caucasian Women

Ravi Retnakaran, Anthony J. G. Hanley, Philip W. Connelly, Mathew Sermer and Bernard Zinman

Division of Endocrinology (R.R., A.J.G.H., B.Z.) and Department of Laboratory Medicine and Pathobiology (P.W.C.), University of Toronto, Toronto, Ontario, Canada M5G 1L5; and Leadership Sinai Centre for Diabetes (R.R., A.J.G.H., B.Z.) and Division of Obstetrics and Gynecology (M.S.), Mount Sinai Hospital, Toronto, Ontario, Canada M5G 1X5

Address all correspondence and requests for reprints to: Dr. Bernard Zinman, Leadership Sinai Centre for Diabetes, Mount Sinai Hospital, Lebovic Building, Room L5-024, 600 University Avenue, Toronto, Ontario, Canada M5G 1X5. E-mail: zinman{at}mshri.on.ca


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Women of Asian and South Asian descent are at increased risk of developing gestational diabetes mellitus compared with Caucasians, despite lower body mass index (BMI). Nevertheless, there has been limited study of insulin action during pregnancy in these ethnic groups.

Objective: The objective of the study was to compare insulin sensitivity in pregnancy in Asian, South Asian, and Caucasian subjects and to determine whether the impact of obesity on insulin action is modified by ethnicity.

Design and Participants: A cross-sectional study was performed in outpatients undergoing oral glucose tolerance testing in late pregnancy. Participants were stratified into three groups: 1) Caucasian (n = 116); 2) South Asian (n = 31); and 3) Asian (n = 28).

Main Outcome Measure: Insulin sensitivity was measured using the oral glucose tolerance test (ISOGTT) index of M. Matsuda and R. DeFronzo, previously validated in pregnancy.

Results: There were no significant ethnic differences in insulin sensitivity despite variation in prepregnancy BMI (Caucasians, 25.2 kg/m2; South Asians, 23.3 kg/m2; Asians, 21.4 kg/m2; overall P = 0.0001). On multiple linear regression analysis, the strongest independent determinants of ISOGTT were gestational diabetes mellitus (t = –5.71; P < 0.0001) and BMI (t = –5.43; P < 0.0001). Importantly, both Asian (t = –2.87; P = 0.0047) and South Asian (t = –2.46; P = 0.015) ethnicity also emerged as negative, independent determinants of ISOGTT. Furthermore, Asian ethnicity significantly modified the association of prepregnancy BMI with ISOGTT (interaction term, t = –2.29; P = 0.0231)

Conclusions: Asian and South Asian ethnicity are both independently associated with increased insulin resistance in late pregnancy. Prepregnancy BMI has a much greater effect on insulin resistance in pregnancy in Asian women than in Caucasians. Ethnicity thus emerges as a factor that modulates the effect of obesity on insulin resistance in pregnancy.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
GESTATIONAL DIABETES MELLITUS (GDM), like type 2 diabetes (type 2 DM), is characterized by metabolic defects of insulin resistance and relative insufficiency of insulin secretion. As with type 2 DM, ethnicity-associated factors may play a role in the development of GDM (1). Indeed, women belonging to certain ethnic groups, such as Asians and South Asians, exhibit an increased risk of developing GDM (1). Despite this risk differential, however, there has been limited study of ethnic differences in insulin dynamics during pregnancy (2, 3). In a cross-sectional study in late pregnancy, Gunton et al. (4) reported that Asian women develop GDM at lower body mass index (BMI) than Caucasians but found no differences in insulin resistance and pancreatic ß-cell function between the two ethnic groups. Given the differences in BMI, this study raises the possibility that the effect of obesity on insulin action may vary between these ethnic groups. Indeed, ethnic heterogeneity in the impact of obesity on insulin resistance has been reported previously in nonpregnant African-American, Hispanic, and Caucasian subjects (5). Thus, we hypothesized that Asian and South Asian women may exhibit differences in the effect of body habitus on insulin action in pregnancy compared with Caucasians. In a cross-sectional study in late pregnancy, we sought to evaluate ethnic differences in insulin resistance and secretion and determine whether the impact of obesity on insulin dynamics is modified by ethnicity.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
The study design and methods have been fully described previously (6, 7, 8). The study protocol was approved by the Mount Sinai Hospital Research Ethics Board, and all subjects gave written informed consent. In brief, participants in the study consisted of 180 healthy pregnant women attending ambulatory obstetrics clinics, who had been referred for a 3-h, 100-g oral glucose tolerance test (OGTT) after an abnormal result on a screening 50 g glucose challenge test (plasma glucose ≥ 7.8 mmol/liter at 1 h post challenge). Demographic and historical data were collected by an interviewer-administered questionnaire at the time of the OGTT, as described previously (6). South Asian participants were defined as having ancestry from India, Pakistan, Sri Lanka, and Bangladesh. Asian participants were defined as having ancestry from other countries in East and Southeast Asia, including China, Japan, Korea, Vietnam, and the Philippines. Five subjects were classified as neither Caucasian, Asian, nor South Asian and were not included in the current analysis. The OGTT allowed for classification of participants into three glucose tolerance groups: 1) GDM, 2) impaired glucose tolerance (IGT), and 3) normal glucose tolerance, based on National Diabetes Data Group criteria (9), as described in a previous report (6).

Biochemistry

Venous blood samples for measurement of insulin, proinsulin, and C-peptide were drawn at fasting and hourly during the OGTT. Specific insulin was measured with the Roche Elecsys 1010 immunoassay analyzer and the electrochemiluminescence immunoassay kit. This assay exhibits 0.05% cross-reactivity to intact human proinsulin and the primary circulating split form (Des 31, 32). C-peptide was measured using chemiluminescent enzyme immunoassay (Immulite 2000; Diagnostic Products, Los Angeles, CA). This assay has cross-reactivity of 0% for insulin and 17% for proinsulin (at 10 ng/ml). Proinsulin was measured by RIA (catalog no. HPI-15K; Linco Research, St. Charles, MO). This assay shows less than 0.1% cross-reactivity to both human insulin and C-peptide, respectively. Plasma adiponectin concentration was measured at 3 h post challenge [adiponectin level is not affected by food intake (ref.10)] by RIA (Linco Research) with a coefficient of variation of 9.3%.

Statistical indices

The fasting C-peptide/insulin (C/I) ratio was calculated as a measure of hepatic insulin extraction (C/I decreases as hepatic insulin extraction decreases) (11). The fasting proinsulin/C-peptide (PI/C) ratio was calculated as a measure of relative proinsulin secretion [hyperproinsulinemia has been associated with ß-cell dysfunction (Ref.12)]. Stimulated indices for glucose and insulin were determined as the area under the curve (AUC) for these measures during the OGTT using the trapezoidal rule.

The ISOGTT insulin sensitivity model of Matsuda and DeFronzo (13) is defined by the following formula: 10,000/square root[Gluc0 x Ins0 x mean Gluc x mean Ins], where Ins0 and Gluc0 represent plasma insulin and glucose values, respectively, at time 0 during the OGTT. Mean glucose and mean insulin were calculated from measurements at baseline and 60, 120, and 180 min during the OGTT. In a validation study in pregnant patients, the ISOGTT index showed better correlation with insulin sensitivity derived using the euglycemic-hyperinsulinemic clamp technique than did either the quantitative insulin sensitivity check index model or the homeostasis model of assessment for insulin resistance (HOMA-IR) (14).

Statistical analysis

All analyses were conducted using the Statistical Analysis System (SAS version 8.02; SAS Institute, Cary, NC). P < 0.05 was considered statistically significant. Means and SDs or proportions were determined by ethnicity, and ANOVA and {chi}2 tests were used to assess univariate differences between continuous and categorical variables, respectively (Table 1Go). The distributions of fasting proinsulin, fasting PI/C, fasting C/I, fasting insulin, AUCinsulin, and ISOGTT were skewed, and thus medians and interquartile ranges were presented for these variables in Table 1Go. The natural logarithmic transformations of these skewed variables were used in univariate and multivariate analyses. Multiple linear regression analysis of dependent-variable logarithmically transformed ISOGTT was performed with covariates age, weeks gestation, parity, prepregnancy BMI, weight gain in pregnancy, glucose intolerance (GDM and IGT), ethnicity, previous history of GDM, and family history of type 2 DM (Table 2Go). Ethnicity was coded using Caucasians as the reference group. Interaction terms of prepregnancy BMI with 1) Asian ethnicity and 2) South Asian ethnicity, respectively, were tested in separate analyses using the full multiple linear regression model. Within each ethnic group, Spearman’s univariate correlations, with partial adjustment for AUCglucose, were assessed between 1) prepregnancy BMI and 2) ISOGTT and fasting C/I, respectively.


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  		TABLE 1. Demographic, clinical, and metabolic data by ethnic group

 

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  		TABLE 2. Multivariate analysis of dependent-variable log ISOGTT

 

   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The study population consisted of 116 Caucasian subjects, 31 participants of South Asian descent, and 28 women of Asian heritage. As reported previously, there were no significant differences between the three ethnic groups with respect to mean age, weeks gestation, weight gain during pregnancy, parity, personal history of previous GDM, and family history of type 2 DM/GDM (Table 1Go and Ref.15). Prepregnancy BMI was highest in the Caucasian women (25.2 kg/m2), followed in turn by the South Asian subjects (23.3 kg/m2), and Asian women (21.4 kg/m2), respectively (overall P = 0.0001). Whereas glucose tolerance status was not significantly different between the three ethnic groups, AUCglucose (a continuous measure of glucose tolerance) was significantly higher in South Asians compared with either Asians (pairwise P = 0.0226) or Caucasians (pairwise P = 0.0451). Nevertheless, there were no significant differences between the groups with respect to unadjusted measures of insulin secretion (fasting C-peptide, proinsulin, and PI/C), hepatic insulin extraction (fasting C/I), and insulin sensitivity (fasting insulin, AUCinsulin, and ISOGTT).

To determine whether ethnicity was independently associated with insulin sensitivity, multiple linear regression analysis was performed with dependent-variable logarithmically transformed ISOGTT (Table 2Go). A model fully adjusted for age, weeks gestation, parity, prepregnancy BMI, weight gain in pregnancy, glucose intolerance, ethnicity, previous history of GDM, and family history of diabetes reconciled 34.5% of the variance in ISOGTT. The strongest independent (and negative) determinants of ISOGTT were GDM and prepregnancy BMI. Importantly, however, both Asian and South Asian ethnicity also emerged as negative, independent determinants of ISOGTT, consistent with greater insulin resistance in these two ethnic groups (compared with the Caucasian subjects). Furthermore, in separate models testing for effect modification, the interaction term between ethnicity and prepregnancy BMI was statistically significant in Asian participants (interaction term, t = –2.29; P = 0.0231) and of borderline significance in South Asian women (interaction term, t = 1.74; P = 0.0832).

Given these interactions, we sought to elucidate the manner in which ethnicity affected the relationship between obesity and insulin action. On Spearman’s univariate correlation analysis, with adjustment for AUCglucose, prepregnancy BMI was strongly and inversely associated with ISOGTT in Asian women (r = –0.52; P = 0.0054). This relationship was less strong in Caucasians (r = –0.38; P < 0.0001) and was not apparent in South Asian women (r = –0.07; P value was not significant). Similarly, BMI was inversely and significantly associated with fasting C/I (i.e. hepatic insulin extraction) in Asian subjects (r = –0.43; P = 0.0253). This association was much weaker and at borderline significance in Caucasians (r = –0.16; P = 0.0917) and was again not present in South Asians (r = –0.04; P value was not significant).

The impact of ethnicity on the relationship between prepregnancy maternal obesity and insulin sensitivity in late pregnancy is readily appreciated when plotting ISOGTT vs. BMI for each ethnic group (Fig. 1Go, A–C). Increasing prepregnancy BMI was associated with a significantly greater decline in insulin sensitivity in Asian women than in Caucasian women (as evidenced by the nonoverlapping 95% confidence intervals (CIs) of the slopes shown in Fig. 1Go, A and B). Furthermore, at any BMI greater than approximately 17 kg/m2, insulin sensitivity was lower in Asian women than in Caucasian subjects. Comparing these two ethnic groups, it is apparent that insulin sensitivity in an Asian woman with prepregnancy BMI of 23 kg/m2 was comparable with that of a Caucasian woman of BMI 30 kg/m2. Finally, this analysis shows the relatively modest effect of BMI on insulin sensitivity in South Asian women [slope of –0.04; 95% CI of (–0.15, 0.08)] (Fig. 1CGo), in contrast to their Asian and Caucasian counterparts.



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  		FIG. 1. Plot of ISOGTT vs. prepregnancy BMI in Caucasians (A), Asians (B), and South Asians (C).

 
We have previously demonstrated strikingly reduced serum levels of the insulin-sensitizing protein adiponectin in South Asian women in pregnancy compared with their Caucasian and Asian counterparts (15). In the current analysis, the addition of adiponectin as a covariate in the multivariate regression analysis of ISOGTT identifies the same independent determinants as in Table 2Go, with the sole exception that South Asian ethnicity is replaced by adiponectin concentration in the model (GDM, t = –4.67, P < 0.0001; IGT, t = –2.34, P = 0.0208; prepregnancy BMI, t = –4.63, P < 0.0001; weight gain in pregnancy, t = –2.87, P = 0.0047; Asian, t = –2.23, P = 0.0274; adiponectin, t = 3.47, P = 0.0007). Thus, hypoadiponectinemia potentially contributes to the increased insulin resistance observed in South Asian women in pregnancy.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
In this report, we demonstrate that Asian and South Asian ethnicity are independently associated with increased insulin resistance in late pregnancy compared with Caucasian heritage. Furthermore, prepregnancy BMI has a far greater effect on insulin resistance in pregnancy in Asian women compared with Caucasians and has a relatively modest effect in this regard in South Asian women. Thus, ethnicity emerges as a factor that modulates the impact of obesity on insulin resistance in pregnancy in these three ethnic groups.

In the nonpregnant state, numerous investigators have previously demonstrated increased insulin resistance in South Asians, possibly related to enhanced accumulation of visceral fat, compared with Caucasians (16, 17, 18, 19). Similarly, in recent years, a growing body of literature has also linked Asian ethnicity with reduced insulin sensitivity (20, 21, 22, 23). It has not been known, however, whether these ethnic differences persist in late pregnancy, a physiologic state typically characterized by severe insulin resistance. Nevertheless, this question is particularly relevant in the context of the increased prevalence of GDM in Asian and South Asian women (1), a phenomenon whose basis remains unclear. Previously, Gunton et al. (4) studied insulin dynamics in 223 pregnant women undergoing OGTT after an abnormal glucose challenge test and found that mean insulin resistance, measured by HOMA-IR, did not differ between Asian and Caucasian subjects. The current report extends this previous work by using the ISOGTT index [demonstrated previously to exhibit better correlation with clamp-derived insulin sensitivity than the HOMA-IR model in pregnant subjects (Ref.14)] to compare insulin sensitivity between Caucasian, Asian, and South Asian women. Importantly, this analysis demonstrates that both Asian and South Asian ethnicity are independently associated with increased insulin resistance in pregnancy. Accordingly, ethnic differences in insulin resistance may contribute to the increased prevalence of GDM in Asian and South Asian women.

In the current report, as one would expect, higher prepregnancy BMI was generally associated with greater insulin resistance in late pregnancy, although the strength of this association was not uniform across the three ethnic groups. Indeed, the identification of interaction between ethnic background and prepregnancy BMI as an independent determinant of insulin sensitivity suggests that ethnicity-associated factors modify the effect of obesity on insulin resistance in pregnancy. This finding is consistent with a previous finding of ethnicity as a modifier of the relationship between waist circumference and fasting insulin in nonpregnant Asian and Caucasian women (23). Similarly, using data from the Third National Health and Nutrition Examination Survey, Palaniappan et al. (5) found that the effect of BMI on insulin sensitivity varied by ethnicity when comparing Hispanic, African-American, and Caucasian subjects. These ethnic groups also exhibit differences in the associations of BMI with diabetes and hypertension, respectively (24, 25). The current study thus extends this concept of ethnic heterogeneity in an obesity-associated complication to Asian and South Asian women in pregnancy, two patient populations facing an increased risk of GDM.

The current findings may hold clinical relevance with respect to the modification of diabetogenic risk in pregnancy. Although maternal obesity is a well-recognized risk factor for the development of GDM, this risk may be particularly profound in Asian women, even at relatively low BMI. Accordingly, two key implications follow. First, it may be especially important for Asian women to enter pregnancy at ideal body weight to ameliorate the risk of GDM. Second, these data further emphasize the crucial need for ethnicity-specific thresholds for overweight and obesity (i.e. to determine said ideal body weight). The development of such standards could allow for early identification and evaluation of minority women at particular risk of developing GDM.

In contrast to the findings in Asian women, increased BMI had a relatively modest effect on insulin resistance in the South Asian participants. One explanation for this observation is that South Asians exhibit increased visceral obesity compared with other ethnic groups at similar BMI (18). Thus, in South Asians, BMI may not adequately reflect the deleterious metabolic effects of increased visceral adiposity, such as greater insulin resistance. A mediator of potential significance in this context is adiponectin, an insulin-sensitizing, adipocyte-derived cytokine that circulates at serum concentration inversely proportional to both intraabdominal fat and insulin resistance (26). As noted earlier, we have reported previously strikingly reduced serum levels of adiponectin in South Asian women in pregnancy compared with Caucasian and Asian counterparts (15). Furthermore, in the current analysis, the inclusion of adiponectin as a covariate in the multivariate regression analysis of ISOGTT leads to the replacement of South Asian ethnicity by adiponectin in the final model. These findings suggest that hypoadiponectinemia likely contributes to the increased insulin resistance observed in South Asian women in pregnancy.

The cross-sectional nature of this study precludes definitive comment on causal relationships between factors of interest. Nevertheless, the associations described herein are consistent with our current understanding of the interrelationships between ethnicity, obesity, and insulin resistance. Another limitation of the current study is that the method of assessment of insulin sensitivity is based on posthepatic insulin levels. As such, the current findings could potentially be due, at least in part, to ethnic differences in hepatic insulin extraction and its relationship to BMI. A third limitation is the inability to adjust for differences in body fat distribution, an issue that is likely of particular relevance in South Asians. Indeed, ethnicity-associated differences in visceral obesity could underlie the varying relationships between BMI and insulin resistance. Additional study in this regard is warranted.

In summary, Asian and South Asian ethnicity are both independently associated with increased insulin resistance in late pregnancy. Prepregnancy BMI has a much greater effect on insulin resistance in pregnancy in Asian women than in Caucasians and has a relatively modest impact in this regard in South Asian women. Thus, ethnicity emerges as a factor that modulates the effect of obesity on insulin resistance in pregnancy.


   Acknowledgments
 
We thank Nuryt Gioulos, Azar Azad, and the Mount Sinai Hospital Department of Pathology and Laboratory Medicine, Nancy Hutton, and Mount Sinai Hospital Patient Care Services.


   Footnotes
 
This study was supported by an operating grant from the Canadian Institutes of Health Research. R.R. is supported by a Canadian Institutes of Health Research Fellowship. A.J.G.H. is supported by a Canadian Diabetes Association Scholarship and a University of Toronto Banting and Best Diabetes Centre New Investigator Award. B.Z. holds the Sam and Judy Pencer Family Chair in Diabetes Research at Mount Sinai Hospital and the University of Toronto.

First Published Online October 25, 2005

Abbreviations: AUC, Area under the curve; BMI, body mass index; C/I, fasting C-peptide/insulin ratio; CI, confidence interval; GDM, gestational diabetes mellitus; HOMA-IR, homeostasis model of assessment for insulin resistance; IGT, impaired glucose tolerance; OGTT, oral glucose tolerance test; PI/C, fasting proinsulin/C-peptide; type 2 DM, type 2 diabetes mellitus.

Received June 6, 2005.

Accepted October 13, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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