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The Journal of Clinical Endocrinology & Metabolism Vol. 82, No. 2 383-387
Copyright © 1997 by The Endocrine Society

Pediatric Endocrinology

Glucose Metabolism in Identical Twins Discordant for Obesity. The Critical Role of Visceral Fat1

Tapani Rönnemaa, Markku Koskenvuo, Jukka Marniemi, Terhi Koivunen, Antti Sajantila, Aila Rissanen, Merja Kaitsaari, Claude Bouchard and Jaakko Kaprio

Departments of Medicine (T.R.), Public Health (Ma.K.), and Diagnostic Radiology (T.K.), University of Turku, FIN-20520 Turku, Finland; Research and Development Centre (J.M., Me.K.), Social Insurance Institution, FIN-20720, Turku, Finland; Department of Human Molecular Genetics (A.J.), National Public Health Institute and Department of Forensic Medicine, University of Helsinki, FIN-00300 Helsinki, Finland; Department of Psychiatry, Helsinki University Central Hospital (A.R.), FIN-00180 Helsinki, Finland; Physical Activity Sciences Laboratory (C.B.), Laval University, Quebec G1K 7PH, Canada; and Department of Public Health (J.K.), University of Helsinki, FIN-00014 Helsinki, Finland

Address all correspondence and requests for reprints to: Dr. Tapani Rönnemaa, Department of Medicine, University of Turku, FIN-20520 Turku, Finland.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Obesity, especially intraabdominally deposited fatness, is associated with reduced insulin sensitivity. However, it is not well established whether this association is confounded by genetic factors. We studied 23 monozygous twin pairs (14 female, 9 male), 33–59 yr old, who had, on the average, 18 kg intrapair difference in body weight. A 75-g oral glucose tolerance test with glucose and insulin measurements at 30-min intervals was performed, and fat distribution was determined with magnetic resonance imaging. The pairs were divided into two groups by the gender-specific median of the abdominal visceral fat area (AVF) in the obese co-twins. In the high-AVF pairs, the mean area under curve (AUC) for glucose (mmol x min/L) was 758 vs. 968 (P = 0.001), AUC for insulin (mU x min/L) was 4320 vs. 8741 (P = 0.001), and insulin sensitivity index (mg x L x L/mmol x mU x min) was 71.5 vs. 45.9 (P < 0.001) in the lean and obese co-twins, respectively. In the low AVF pairs, the mean AUC for glucose was 669 vs. 706 (not significant), AUC for insulin was 3323 vs. 4241 (not significant), and the sensitivity index was 85.2 vs. 73.7 (P = 0.04) in the lean and obese co-twins, respectively. In subjects who are genetically identical but who are discordant for body mass, only those who differ most in visceral fat level are characterized by major alterations in insulin sensitivity and glucose tolerance.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
IT IS WELL established that obesity is an independent risk factor for noninsulin-dependent diabetes mellitus (1). Several studies in the 1980’s suggested that distribution of body fat was an important determinant of the disturbing effect of obesity on glucose metabolism (2, 3, 4). It was shown that accumulation of intraabdominal fat was associated with reduced insulin sensitivity. However, some recent studies have proposed that sc fat accumulation (5), especially truncal sc fat (6), may be as harmful as, or even more disadvantageous for glucose metabolism, than intraabdominal fat deposition.

When comparing the glucose metabolism in unrelated obese and nonobese subjects, as has been the case in previous studies, differences in the genetic background of the subjects were not taken into account. However, genetic factors may be of importance, as approximately 50% of the variation in body fat distribution is genetically determined (7). One strategy to assess the independent impact of obesity on glucose metabolism without the confounding effects of genetic factors is to examine identical twins who are discordant for obesity. Therefore, we compared glucose metabolism in 23 identical nondiabetic twin pairs who had, on the average, a 7-kg/m2 difference in body mass index (BMI). Special attention was paid to the distribution of body fat, as determined by magnetic resonance imaging.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

The Finnish Twin Cohort includes all pairs (4307 monozygous, 9581 like-sexed dizygous pairs) of adult Finnish twins born before 1958 and alive in 1975 (8). Based on a postal questionnaire sent to the twins in 1990, identical twin pairs born between 1932 and 1957 and discordant for obesity were identified. Discordance for obesity was defined as a BMI difference of at least 4 kg/m2 and, in addition, the BMI of the obese co-twin had to be more than 27 kg/m2, and the BMI of the lean co-twin had to be less than 25 kg/m2. Subjects with a history of thyroid disorders, psychiatric diseases, diabetes, major musculoskeletal problems, and other diseases, or taking medications (e.g. diuretics or ß-blockers) possibly affecting glucose metabolism were excluded. All eligible twin pairs, based on a response letter, were invited to take part in the present study in 1992, provided that they still fulfilled the criteria. A total of 28 twin pairs were examined.

The physical examination revealed that two of the pairs had a BMI difference less than 3 kg/m2, and they were excluded. Three pairs had a BMI difference between 3 and 4 kg/m2, and they were included in the final study population. The obese co-twin of one pair was found to have previously undiagnosed overt diabetes mellitus, and this pair was excluded.

Zygosity of the twin pairs was originally based on a validated self-administered questionnaire (9). The monozygosity of the pairs of the present study was confirmed by dermatomatoglyphic analysis of fingertip prints (10, 11) by a highly experienced expert. All except six pairs were confirmed to be monozygotic. DNA samples of the six pairs with uncertain zygosity were typed for markers at six different polymorphic gene loci (DIS80, APOB, D17S30, COL2A1, VWA, and HUMTH). Four of the pairs were found to be monozygotic, and the two other pairs were dizygotic; these two pairs were excluded.

Thus, the final study sample consisted of 23 nondiabetic identical twin pairs (14 female, 9 male) with more than 3 kg/m2 difference in BMI and having no diseases or medications possibly affecting the results.

Methods

Glucose metabolism was assessed in a 2-h glucose (75 g) tolerance test with glucose and insulin measurements at 0, 30, 60, 90, and 120 min. Serum glucose was measured by the glucose dehydrogenase method (Merck Diagnostica, Darmstadt, Germany). Plasma insulin was measured by RIA (Pharmacia Diagnostics, Uppsala, Sweden). The antiserum of this kit is specific for insulin and does not cross-react with proinsulin or C-peptide (cross-reactivities < 0.1%). An insulin sensitivity index was calculated according to the formula of Cederholm and Wibell (12). Serum free fatty acids (FFAs) were measured enzymatically after an overnight fast using acyl-CoA synthetase, acyl CoA oxidase, and peroxidase (Wako Chemicals, Neuss, Germany). Smoking was defined as regular smoking at the time of examination.

Percentage of body fat was determined using the so-called four-component method. The method is based on the division of body mass into four components with different densities: fat tissue 0.9007 g/cm3), water (0.994 g/cm3), minerals (3.042 g/cm3), and proteins (1.34 g/cm3). Water mass was estimated by bioelectric impedance method (BIA-101A/S, RJL System Inc., Clemens, MI). Mineral mass was estimated by dual-energy x-ray absorptiometry (Norland XR26, Norland Corporation, Fort Atkinson, WI). The density of the whole body was estimated by underwater weighing corrected for information on body water and mineral mass. The proportion of fat tissue was calculated from the density of the whole body according to the formula of Siri (13).

The distribution of body fat was measured by magnetic resonance imaging (MRI) (14). Imaging was performed at 0.1 tesla (Mega4R, Instrumentarium Co., Imaging Division, Helsinki, Finland). Axial and sagittal localizers were used to obtain a transaxial T1-weighted image (relaxation time/echo time = 155/20, slice thickness 10 mm) at the level of the fourth lumbar vertebra. Visceral and sc fat areas were measured. MRI was not performed in three pairs, either because of claustrophobia or because of temporary malfunctioning of the MRI equipment. These three pairs were excluded from analyses concerning body fat distribution.

A paired t test was used to compare means and the McNemar’s test to compare the proportions of obese and lean co-twins. Pearson correlation coefficients were calculated to quantify the association between intrapair differences in adiposity or its distribution and intrapair differences in variables of glucose metabolism. Multiple regression analyses were performed to analyze the independent contributions of visceral fat and body fat percentage to glucose metabolism. All statistical analyses were performed using Statistical Analysis System (SAS) statistical programs.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The average difference in weight between the obese and lean co-twins was 16 kg among males and 19 kg among females (Table 1Go). In both genders, the abdominal visceral fat (AVF) area was twice as large in the obese co-twins as in the lean co-twins. The difference in sc fat area between obese and lean co-twins was greater among female than male pairs. Fasting serum glucose, area under curve (AUC) for glucose, fasting insulin, and AUC for insulin were significantly greater in obese co-twins compared with lean co-twins. Accordingly, the insulin sensitivity index was lower in the obese co-twins. Intrapair differences in indices of glucose metabolism were somewhat greater among males compared with females. Serum FFA concentrations were similar in obese and lean co-twins.


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  		Table 1. Characteristics and glucose metabolism of the co-twins (mean ± SE)

 
To characterize the specific impact of fat distribution on glucose metabolism, the twin pairs were divided according to the median value of AVF area of the obese co-twins (Fig. 1Go). Gender-specific median values were used for males and females, and results from both genders were combined. In both subgroups of AVF, the abdominal sc fat area was almost twice as large in the obese co-twins as in the nonobese co-twins. The intrapair differences in fasting glucose and insulin, AUC for glucose, and AUC for insulin, as well as the insulin sensitivity index between the obese and nonobese co-twins, were statistically highly significant among the high-AVF area pairs. In contrast, the corresponding intrapair differences were small or nonsignificant among the pairs with low AVF fat area. The proportion of smokers and serum FFA concentrations did not differ between obese and lean co-twins in either subgroup of AVF. When a division of twin pairs was made by the median value of waist to hip ratio of the obese co-twins, the results were essentially similar (data not shown) compared with results obtained using division of the pairs by AVF.



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  		Figure 1. Glucose metabolism in twins stratified by gender-specific median value of abdominal visceral fat (AVF) area in the obese co-twin. Columns represent mean values, genders are combined. Pair t test was used except for smoking McNemar’s test. High AVF, above median; low AVF, below median value. In the high-AVF pairs, mean BMI was 30.2 and 22.5 kg/m2 (P < 0.001), mean abdominal subcutaneous fat (ASF) area was 276 and 141 cm2 (P < 0.001), mean AVF area was 127 and 49 cm2 (P < 0.001), and number of smokers was 2/10 and 5/10 (P not significant) in the obese and lean co-twins, respectively. In the low AVF pairs, mean BMI was 27.9 and 23.2 kg/m2 (P < 0.001), mean ASF area was 280 and 184 cm2 (P < 0.001), mean AVF area was 58 and 32 cm2 (P = 0.001), and number of smokers was 4/10 and 5/10 (P not significant) in the obese and lean co-twins, respectively.

 
When the twin pairs were divided according to the gender-specific median value of abdominal sc fat (ASF) area in the obese co-twins, the intrapair differences in glucose metabolism were similar among high- and low-ASF subgroups. For example, AUC of insulin was 6369 ± 1136 and 4022 ± 519 mU x min/L (P = 0.019) in obese and lean co-twins of the high-ASF subgroup, and 6592 ± 1108 and 3620 ± 340 mU x min/L (P = 0.022) in obese and lean co-twins of the low ASF subgroup, respectively.

To quantify the relationship between adiposity or its distribution with glucose metabolism, we correlated intrapair differences in adiposity variables to indicators of insulin sensitivity (Table 2Go, Fig. 2Go). Intrapair differences in BMI and percentage of body fat did not show any significant correlation to the metabolic variables. Intrapair differences in AVF area were those most significantly correlated to intrapair differences in glucose and insulin AUCs and to intrapair difference in insulin sensitivity index. In contrast, intra-pair differences in sc fat area showed no correlation to intrapair differences in indices of glucose metabolism. In multiple regression analyses, the association between intrapair differences in AVF area and differences in glucose metabolism remained significant when adjustment was made for differences in body fat percentage (Table 3Go). The whole model explained 31–50% of the variation in intrapair differences in glucose metabolism.


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  		Table 2. Pearson correlation coefficients between intrapair differences in glucose metabolism and intrapair differences in indices of obesity and its distribution. Genders are combined

 


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  		Figure 2. Correlation between intrapair differences (obese vs. nonobese) in abdominal visceral fat (AVF) area and intrapair differences in AUC for glucose and insulin during an oral glucose tolerance test. Genders are combined.

 

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  		Table 3. Multiple regression analyses on the association between intrapair differences in glucose metabolism and intrapair differences in AVF area and percentage of body fat

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Our results show that in identical twins discordant for obesity, the obese co-twins exhibit disturbed glucose metabolism compared with the leaner co-twins. However, despite a similar difference in BMI in subgroups of identical twins stratified according to indicators of body fat distribution, a clear-cut difference in insulin sensitivity between the obese and lean co-twins was observed only in the subgroup with a large amount of AVF. Accordingly, the intrapair difference in insulin sensitivity was inversely correlated to visceral fat but not with sc fat or overall adiposity. Our results are thus in accordance with earlier findings in study cohorts of subjects not related by nascency, showing the importance of visceral fat deposition in disturbed glucose metabolism (2, 4, 15, 16) but are in contrast to the results of a recent study in which the amount of truncal sc fat showed the strongest inverse correlation to insulin sensitivity (6). In the latter study, the population was racially heterogeneous. In our study, all subjects were Caucasians, and because obese and lean individuals were genetically identical, the association between visceral fat and insulin resistance is entirely a consequence of adipose mass differences, i.e. the degree of visceral obesity, and is not confounded by genetic influences.

Discordance for obesity in identical twins is a rare phenomenon. We found only 50 out of approximately 1500 twin pairs fulfilling our discordance criterion. Therefore, an important question is whether all twin pairs studied were really monozygous. We paid special attention to this by performing fingertip print analyses in all pairs and an analysis of alleles at six marker loci in those pairs in whom the identity could not be fully confirmed by fingertip print characteristics. Therefore, it is highly unlikely that any of the pairs studied would have been dizygous. Of course, we cannot exclude the possibility that postconception tissue-selective mutation potentially affecting adipose tissue could have occurred in some of the pairs.

To study glucose metabolism, we performed an oral glucose tolerance test with samples collected every 30 min for glucose and insulin measurements. As indicators of insulin sensitivity, we used fasting insulin, insulin area, and a sensitivity index calculated according to Cederholm & Wibell (12). Although we did not directly measure insulin sensitivity by the hyperinsulinemic-euglycemic clamp technique (17), our indicators, even fasting insulin, are well correlated with clamp results in nondiabetic subjects (18). Moreover, all indicators of insulin sensitivity in the present study exhibit consistent relationships with body fat and its distribution. We used MRI at the level of the fourth lumbar vertebra to assess body fat distribution. Results obtained with MRI correlate strongly with those obtained with computed tomography, and the reproducibility of the MRI method is good (19).

Although visceral fat accumulation itself seems to be responsible for the low insulin sensitivity in subjects with this type of obesity, other environmental factors could act as confounders. For example, smoking is related to insulin resistance (20), and it may also favor upper body fat accumulation (21). In our study, the proportion of smokers did not differ significantly between obese and nonobese co-twins when analyzed as whole groups or as subgroups with either visceral or sc fat accumulation. In fact, the number of smokers tended to be somewhat higher among lean co-twins, suggesting that the results were not confounded by smoking.

Regarding the mechanism by which visceral fat may result in reduced insulin sensitivity, it has been proposed that increased flux of FFAs from intraabdominal fat stores to the liver and systemic circulation leads to a higher preponderance of tissues to fat use instead of glucose as fuel (22, 23). We did not measure FFA kinetics, but similar FFA levels in obese and lean co-twins, independent of fat distribution, suggest that if the flux of FFAs from visceral fat is increased, it is likely compensated by their increased use (24).

We conclude that when genetic factors are controlled for, subjects prone to AVF accumulation are more susceptible to experiencing reduced insulin sensitivity, whereas subjects with a tendency to ASF deposition exhibit only modest or no disturbances in glucose metabolism.


   Acknowledgments
 
We thank Professor Terry E. Reed, Indiana University School of Medicine, for analyzing the fingertip prints.


   Footnotes
 
1 This study was supported in part by a grant from the Academy of Finland. Back

Received June 20, 1996.

Revised October 25, 1996.

Accepted October 31, 1996.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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