Elsevier

Metabolism

Volume 61, Issue 2, February 2012, Pages 262-272
Metabolism

Clinical Science
Improvement in insulin sensitivity following a 1-year lifestyle intervention program in viscerally obese men: contribution of abdominal adiposity

https://doi.org/10.1016/j.metabol.2011.06.024Get rights and content

Abstract

The objectives of the study were to quantify the effect of a 1-year healthy eating–physical activity/exercise lifestyle modification program on insulin sensitivity in viscerally obese men classified according to their glucose tolerance status and to evaluate the respective contributions of changes in body fat distribution vs changes in cardiorespiratory fitness (CRF) to the improvements in indices of plasma glucose/insulin homeostasis. Abdominally obese, dyslipidemic men (waist circumference ≥90 cm, triglycerides ≥1.69 mmol/L, and/or high-density lipoprotein cholesterol <1.03 mmol/L) were recruited. The 1-year intervention/evaluation was completed by 104 men. Body weight, composition, and fat distribution were assessed by dual-energy x-ray absorptiometry/computed tomography. Cardiorespiratory fitness and cardiometabolic risk profile were measured. After 1 year, insulin sensitivity improved in association with decreases in both visceral (VAT) and subcutaneous adiposity (SAT) as well as with the improvement in CRF, regardless of baseline glucose tolerance. Further analyses were performed according to changes in glucose tolerance status: improvement (group I, n = 39), no change (group N, n = 50), or worsening (group W, n = 15) after 1 year. Groups I and N improved their insulin sensitivity and their CRF, whereas group W did not, while losing less VAT than groups I and N. Multiple regressions showed that reduction in VAT was associated with an improvement in homeostasis model assessment of insulin resistance, whereas reduction in SAT was rather associated with improvement of the insulin sensitivity index of Matsuda. Changes in CRF were not independently associated with changes in indices of plasma glucose/insulin homeostasis. A 1-year lifestyle intervention improved plasma glucose/insulin homeostasis in viscerally obese men, including those with normal glucose tolerance status at baseline. Changes in SAT and VAT but not in CRF appeared to mediate these improvements.

Introduction

Abdominal obesity, characterized by excess visceral adipose tissue (VAT) and ectopic fat deposition, has been associated with a cluster of atherogenic and diabetogenic abnormalities [1]. However, pharmacological approaches to target VAT accumulation are virtually nonexistent since the withdrawal of some of the few available antiobesity drugs [2], [3]. Several lifestyle intervention studies using exercise as the treatment modality have shown its ability to mobilize VAT and improve the cardiometabolic risk (CMR) profile, even in the absence of weight loss [4], [5]. In the well-known Diabetes Prevention Study (DPS) [6] and Diabetes Prevention Program (DPP) [7], a 58% reduction in the incidence of type 2 diabetes mellitus (T2D) was reported in patients with glucose intolerance following a lifestyle modification program focusing on healthy eating and increased physical activity. However, only few studies have addressed the question of whether it has beneficial effects on indices of plasma glucose/insulin homeostasis specifically among men selected on the basis of their excess visceral adiposity who were further classified on the basis of their glucose tolerance [7], [8], [9]. For instance, a recent study has shown that the reduction in T2D's incidence related to physical activity was heterogeneous depending upon the glucose tolerance status of participants assessed at baseline [9].

The present study was designed as a body composition/adipose tissue distribution lifestyle intervention to examine how a healthy eating, physical activity/exercise program could improve the CMR profile of a group of viscerally obese men with the atherogenic dyslipidemia of insulin resistance. Participants did not have T2D; and the study included subjects with both normal and impaired glucose tolerance, aiming at specifically targeting excess visceral adiposity rather than metabolic disturbances. Key inclusion criteria were the presence of abdominal obesity and the high triglyceride/low high-density lipoprotein (HDL) cholesterol atherogenic dyslipidemia that is a lipid phenotype associated with excess VAT [10]. The primary end point of the intervention was visceral adiposity measured by computed tomography. We put forward the hypothesis that a 1-year lifestyle modification program integrating healthy eating habits combined with an increase in physical activity and endurance exercise could lead to improvements in insulin sensitivity, irrespective of patients' glucose tolerance status. We also examined whether changes in body fat distribution vs changes in cardiorespiratory fitness (CRF) would contribute to the improvements in indices of plasma glucose/insulin homeostasis.

Section snippets

Study design

One hundred forty-four men, between the ages of 30 and 65 years and presenting with abdominal obesity (waist circumference ≥90 cm), triglyceride levels of at least 1.69 mmol/L, and/or HDL cholesterol less than 1.03 mmol/L, were recruited by solicitation in the media to participate to a 3-year lifestyle modification program (the “SYNERGIE” study, to emphasize the synergism between healthy eating and increased physical activity/exercise). Men with T2D, with body mass index (BMI) values less than

Results

From the 144 men who were initially involved in the study, 35 men dropped out during the first year, whereas 5 men did not have complete OGTT data. The men who completed the 1-year intervention/evaluation presented slightly higher BMI (31.2 ± 3.1 vs 30.1 ± 2.8 for the men who completed the 1-year intervention/evaluation vs the men who did not, respectively; P = .04), higher fasting insulin (173 ± 74 vs 141 ± 78, respectively; P = .03), higher HOMA-IR (6.47 ± 2.95 vs 5.10 ± 2.77, respectively; P

Discussion

The present study is not a randomized trial to quantify the effects of a lifestyle modification program on the CMR profile. Indeed, whether a lifestyle modification program can improve the CMR profile has already been very well documented [6], [7], [29], [30], [31], [32]. Instead, the present study was designed to test whether a 1-year healthy eating–physical activity/exercise program would change the insulin sensitivity of viscerally obese dyslipidemic men, regardless of their glucose

Conclusion

The present 1-year healthy eating–physical activity/exercise intervention program substantially improved indices of plasma glucose/insulin homeostasis in viscerally obese dyslipidemic men, regardless of their glucose tolerance status at baseline. As a consequence, the majority of participants improved or stabilized their glucose tolerance status over the 1-year intervention. However, lack of CRF improvement and limited losses in VAT and SAT defined a subgroup of subjects who failed to improve

Funding source

This study was supported by the Canadian Institutes of Health Research.

Conflict of Interest

No conflict of interest.

Acknowledgment

Dr Borel is a postdoctoral fellow supported by a fellowship from Agiràdom (Meylan, France) and the Rhône-Alpes region (France). Dr Nazare is a postdoctoral fellow supported by a fellowship from “Fondation Bullukian” and “Institut Appert.” Jessica Smith is a post-doctoral fellow supported by a fellowship from the International Chair on Cardiometabolic Risk. Dr Paul Poirier is a senior clinical researcher of the Fonds de recherche en santé du Québec.

References (49)

  • W.C. Knowler et al.

    Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin

    N Engl J Med

    (2002)
  • S. Schafer et al.

    Lifestyle intervention in individuals with normal versus impaired glucose tolerance

    Eur J Clin Invest

    (2007)
  • S. Engberg et al.

    Differential relationship between physical activity and progression to diabetes by glucose tolerance status: the Inter99 Study

    Diabetologia

    (2010)
  • I. Lemieux et al.

    Hypertriglyceridemic waist: a marker of the atherogenic metabolic triad (hyperinsulinemia; hyperapolipoprotein B; small, dense LDL) in men?

    Circulation

    (2000)
  • The Airlie (VA) Consensus Conference: Standardization of Anthropometric Measurements. Lohman T, Roche A, Martorel R,...
  • K. van der Kooy et al.

    Techniques for the measurement of visceral fat: a practical guide

    Int J Obes Relat Metab Disord

    (1993)
  • M. Ferland et al.

    Assessment of adipose tissue distribution by computed axial tomography in obese women: association with body density and anthropometric measurements

    Br J Nutr

    (1989)
  • J.P. Despres et al.

    Effect of rimonabant on the high-triglyceride/low–HDL-cholesterol dyslipidemia, intraabdominal adiposity, and liver fat: the ADAGIO-Lipids trial

    Arterioscler Thromb Vasc Biol

    (2009)
  • A. Pare et al.

    Is the relationship between adipose tissue and waist girth altered by weight loss in obese men?

    Obes Res

    (2001)
  • American College of Sports Medicine

    ACSM's guidelines for exercise testing and prescription

    (1995)
  • R. Richterich et al.

    [Determination of plasma glucose by hexokinase-glucose-6-phosphate dehydrogenase method]

    Schweiz Med Wochenschr

    (1971)
  • B. Desbuquois et al.

    Use of polyethylene glycol to separate free and antibody-bound peptide hormones in radioimmunoassays

    J Clin Endocrinol Metab

    (1971)
  • L.G. Heding

    Radioimmunological determination of human C-peptide in serum

    Diabetologia

    (1975)
  • D.M. Nathan et al.

    Impaired fasting glucose and impaired glucose tolerance: implications for care

    Diabetes Care

    (2007)
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    Authors contribution: Anne-Laure Borel: data analysis, data interpretation and manuscript writing. Julie-Anne Nazare: data interpretation and critical revision. Jessica Smith: data interpretation and critical revision. Natalie Alméras: design conception, conduct of the study, and critical revision. Angelo Tremblay: design conception and critical revision. Jean Bergeron: design conception and critical revision. Paul Poirier: design conception and critical revision. Jean-Pierre Després: design conception, conduct of the study, data interpretation, critical revision.

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