Journal of Physiology and Biochemistry

, Volume 74, Issue 4, pp 591–601 | Cite as

The relationship between adiposopathy and glucose-insulin homeostasis is not affected by moderate-intensity aerobic training in healthy women with obesity

  • Andrée-Anne Clément
  • Eléonor Riesco
  • Sébastien Tessier
  • Michel Lacaille
  • Francine Pérusse
  • Mélanie Coté
  • Jean-Pierre Després
  • John Weisnagel
  • Jean Doré
  • Denis R. Joanisse
  • Pascale MauriègeEmail author
Original Article


The contribution of adiposopathy to glucose-insulin homeostasis remains unclear. This longitudinal study examined the potential relationship between the adiponectin/leptin ratio (A/L, a marker of adiposopathy) and insulin resistance (IR: homeostasis model assessment (HOMA)), insulin sensitivity (IS: Matsuda), and insulin response to an oral glucose tolerance test before and after a 16-week walking program, in 29 physically inactive pre- and postmenopausal women with obesity (BMI, 29–35 kg/m2; age, 47–54 years). Anthropometry, body composition, VO2max, and fasting lipid-lipoprotein and inflammatory profiles were assessed. A/L was unchanged after training (p = 0.15), despite decreased leptin levels (p < 0.05). While the Matsuda index tended to increase (p = 0.07), HOMA decreased (p < 0.05) and fasting insulin was reduced (p < 0.01) but insulin area under the curve (AUC) remained unchanged (p = 0.18) after training. Body fatness and VO2max were improved (p < 0.05) while triacylglycerols increased and HDL-CHOL levels decreased after training (p < 0.05). At baseline, A/L was positively associated with VO2max, HDL-CHOL levels, and Matsuda (0.37 < ρ < 0.56; p < 0.05) but negatively with body fatness, HOMA, insulin AUC, IL-6, and hs-CRP levels (− 0.41 < ρ < − 0.66; p < 0.05). After training, associations with fitness, HOMA, and inflammation were lost. Multiple regression analysis revealed A/L as an independent predictor of IR and IS, before training (partial R2 = 0.10 and 0.22), although A/L did not predict the insulin AUC pre- or post-intervention. A significant correlation was found between training-induced changes to A/L and IS (r = 0.38; p < 0.05) but not with IR or insulin AUC. Although changes in the A/L ratio could not explain improvements to glucose-insulin homeostasis indices following training, a relationship with insulin sensitivity was revealed in healthy women with obesity.


Adiponectin Leptin Insulin sensitivity Brisk walking Menopausal status 



The cooperation of the participants who participated to this walking program is greatly appreciated.

Thanks to Alexandra Andersen, Denise Christen, Katie Lacasse, Geneviève Ouellet, Renaud Turcotte-Sabourin, Guillaume Salamin, and Jean Tremblay for their very helpful assistance in the supervision of walking sessions as well as to Caroline Brière, dietetic technician, for her dedicated work on the 3-day dietary records. Special thanks to Valérie-Ève Julien, Marie-Christine Dubé, and Marie Tremblay for their precious help and implication in OGTT.

Funding information

This study was supported by the operating grant # MOP-77572 obtained from the Canadian Institutes of Health Research (PM) and from the Fondation du Centre de Recherche de l’Institut Universitaire de Cardiologie et Pneumologie de Québec (DRJ).

Compliance with ethical standards

The experimental design was approved by the Laval University Ethics Committee on Human Research for Medical Sciences, and all participants provided written informed consent.

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. 1.
    Bastien M, Poirier P, Lemieux I, Despres JP (2014) Overview of epidemiology and contribution of obesity to cardiovascular disease. Prog Cardiovasc Dis 56:369–381. CrossRefGoogle Scholar
  2. 2.
    Bays H (2014) Central obesity as a clinical marker of adiposopathy; increased visceral adiposity as a surrogate marker for global fat dysfunction. Curr Opin Endocrinol Diabetes Obes 21:345–351. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Bays HE, Gonzalez-Campoy JM, Henry RR, Bergman DA, Kitabchi AE, Schorr AB, Rodbard HW, Adiposopathy Working G (2008) Is adiposopathy (sick fat) an endocrine disease? Int J Clin Pract 62:1474–1483. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Chagas EFB, Bonfim MR, Turi BC, Brondino NCM, Monteiro HL (2017) Effect of moderate-intensity exercise on inflammatory markers among postmenopausal women. J Phys Act Health 14:479–485. CrossRefPubMedGoogle Scholar
  5. 5.
    Christiansen T, Paulsen SK, Bruun JM, Pedersen SB, Richelsen B (2010) Exercise training versus diet-induced weight-loss on metabolic risk factors and inflammatory markers in obese subjects: a 12-week randomized intervention study. Am J Physiol Endocrinol Metab 298:E824–E831. CrossRefPubMedGoogle Scholar
  6. 6.
    Clément AA, Joanisse DR, Mauriège P (2017) The metabolically healthy obese phenotype: a temporary state? Obésité (in press. CrossRefGoogle Scholar
  7. 7.
    Collaboration NCDRF (2016) Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet 387:1377–1396. CrossRefGoogle Scholar
  8. 8.
    Despres JP (2012) Body fat distribution and risk of cardiovascular disease: an update. Circulation 126:1301–1313. CrossRefPubMedGoogle Scholar
  9. 9.
    Di Blasio A, Izzicupo P, D'Angelo E, Melanzi S, Bucci I, Gallina S, Di Baldassarre A, Napolitano G (2014) Effects of patterns of walking training on metabolic health of untrained postmenopausal women. J Aging Phys Act 22:482–489. CrossRefPubMedGoogle Scholar
  10. 10.
    Di Blasio A, Ripari P, Bucci I, Di Donato F, Izzicupo P, D'Angelo E, Di Nenno B, Taglieri M, Napolitano G (2012) Walking training in postmenopause: effects on both spontaneous physical activity and training-induced body adaptations. Menopause 19:23–32. CrossRefPubMedGoogle Scholar
  11. 11.
    Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502PubMedPubMedCentralGoogle Scholar
  12. 12.
    Gerosa-Neto J, Antunes BM, Campos EZ, Rodrigues J, Ferrari GD, Rosa Neto JC, Bueno CRJ, Lira FS (2016) Impact of long-term high-intensity interval and moderate-intensity continuous training on subclinical inflammation in overweight/obese adults. J Exerc Rehabil 12:575–580. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Golbidi S, Laher I (2014) Exercise induced adipokine changes and the metabolic syndrome. J Diabetes Res 2014:1–16. CrossRefGoogle Scholar
  14. 14.
    Gondim OS, de Camargo VT, Gutierrez FA, Martins PF, Passos ME, Momesso CM, Santos VC, Gorjao R, Pithon-Curi TC, Cury-Boaventura MF (2015) Benefits of regular exercise on inflammatory and cardiovascular risk markers in normal weight, overweight and obese adults. PLoS One 10:e0140596. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ha CH, Swearingin B, Jeon YK, Lee M (2014) Effects of combined exercise on HOMA-IR, HOMA β-cell and atherogenic index in Korean obese female. Sport Sci Health 11:49–55. CrossRefGoogle Scholar
  16. 16.
    Hong HR, Jeong JO, Kong JY, Lee SH, Yang SH, Ha CD, Kang HS (2014) Effect of walking exercise on abdominal fat, insulin resistance and serum cytokines in obese women. J Exerc Nutr Biochem 18:277–285. CrossRefGoogle Scholar
  17. 17.
    Huth C, Dubois MJ, Marette A, Tremblay A, Weisnagel SJ, Lacaille M, Mauriege P, Joanisse DR (2015) Irisin is more strongly predicted by muscle oxidative potential than adiposity in non-diabetic men. J Physiol Biochem 71:559–568. CrossRefPubMedGoogle Scholar
  18. 18.
    Huth C, Pigeon E, Riou ME, St-Onge J, Arguin H, Couillard E, Dubois MJ, Marette A, Tremblay A, Weisnagel SJ, Lacaille M, Mauriege P, Joanisse DR (2016) Fitness, adiposopathy, and adiposity are independent predictors of insulin sensitivity in middle-aged men without diabetes. J Physiol Biochem 72:435–444. CrossRefPubMedGoogle Scholar
  19. 19.
    Inoue M, Maehata E, Yano M, Taniyama M, Suzuki S (2005) Correlation between the adiponectin-leptin ratio and parameters of insulin resistance in patients with type 2 diabetes. Metabolism 54:281–286. CrossRefPubMedGoogle Scholar
  20. 20.
    Inoue M, Yano M, Yamakado M, Maehata E, Suzuki S (2006) Relationship between the adiponectin-leptin ratio and parameters of insulin resistance in subjects without hyperglycemia. Metabolism 55:1248–1254. CrossRefPubMedGoogle Scholar
  21. 21.
    Jung CH, Rhee EJ, Choi JH, Bae JC, Yoo SH, Kim WJ, Park CY, Mok JO, Kim CH, Lee WY, Oh KW, Park SW, Kim SW (2010) The relationship of adiponectin/leptin ratio with homeostasis model assessment insulin resistance index and metabolic syndrome in apparently healthy Korean male adults. Korean Diabetes J 34:237–243. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Karvonen MJ, Kentala E, Mustala O (1957) The effects of training on heart rate; a longitudinal study. Ann Med Exp Biol Fenn 35:307–315PubMedGoogle Scholar
  23. 23.
    Laukkanen R, Oja P, Pasanen M, Vuori I (1992) Validity of a two kilometre walking test for estimating maximal aerobic power in overweight adults. Int J Obes Relat Metab Disord 16:263–268PubMedGoogle Scholar
  24. 24.
    Lee MJ, Wu Y, Fried SK (2013) Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Asp Med 34:1–11. CrossRefGoogle Scholar
  25. 25.
    Lemoine S, Rossell N, Drapeau V, Poulain M, Garnier S, Sanguignol F, Mauriege P (2007) Effect of weight reduction on quality of life and eating behaviors in obese women. Menopause 14:432–440. CrossRefPubMedGoogle Scholar
  26. 26.
    Madsen EL, Rissanen A, Bruun JM, Skogstrand K, Tonstad S, Hougaard DM, Richelsen B (2008) Weight loss larger than 10% is needed for general improvement of levels of circulating adiponectin and markers of inflammation in obese subjects: a 3-year weight loss study. Eur J Endocrinol 158:179–187. CrossRefPubMedGoogle Scholar
  27. 27.
    Matsuda M, DeFronzo RA (1999) Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 22:1462–1470CrossRefGoogle Scholar
  28. 28.
    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRefGoogle Scholar
  29. 29.
    Mauriege P, Imbeault P, Doucet E, Lacaille M, Langin D, Almeras N, Despres JP, Tremblay A (2013) Weight loss and regain in obese individuals: a link with adipose tissue metabolism indices? J Physiol Biochem 69:497–505. CrossRefPubMedGoogle Scholar
  30. 30.
    Mauriege P, Joanisse DR, CasparBauguil S, Cartier A, Lemieux I, Bergeron J, Biron S, Marceau P, Richard D (2015) Gene expression of different adipose tissues of severely obese women with or without a dysmetabolic profile. J Physiol Biochem 71:719–732. CrossRefPubMedGoogle Scholar
  31. 31.
    Mauriège P, Karelis A, Rabasa-Lhoret R, Deshaies Y, Joanisse D (2016) Is adiposopathy a valuable marker to discriminate individuals with metabolically healthy obesity (MHO) and those with metabolically abnormal obesity (MAO)? Abstract, 13th French-Spanish Meeting of the Consortium Trans-Pyrénéen Obésité-Diabète (CTPIOD), Toulouse, France, June 2016Google Scholar
  32. 32.
    Mauriege P, Prud’homme D, Marcotte M, Yoshioka M, Tremblay A, Després J (1997) Regional differences in adipose tissue metabolism between sedentary and endurance-trained women. Am J Phys 273:E497–E506Google Scholar
  33. 33.
    Moreno-Indias I, Tinahones FJ (2015) Impaired adipose tissue expandability and lipogenic capacities as ones of the main causes of metabolic disorders. J Diabetes Res 2015:1–12. CrossRefGoogle Scholar
  34. 34.
    Nelson ME, Rejeski WJ, Blair SN, Duncan PW, Judge JO, King AC, Macera CA, Castaneda-Sceppa C, American College of Sports M, American Heart A (2007) Physical activity and public health in older adults: recommendation from the American College of Sports Medicine and the American Heart Association. Circulation 116:1094–1105. CrossRefPubMedGoogle Scholar
  35. 35.
    Prud’homme D, Despres JP, Landry JF, Moorjani S, Lupien PJ, Tremblay A, Nadeau A, Bouchard C (1994) Systolic blood pressure during submaximal exercise: an important correlate of cardiovascular disease risk factors in normotensive obese women. Metabolism 43:18–23CrossRefGoogle Scholar
  36. 36.
    Riesco E, Tessier S, Lacaille M, Perusse F, Cote M, Despres JP, Bergeron J, Weisnagel JS, Dore J, Mauriege P (2013) Impact of a moderate-intensity walking program on cardiometabolic risk markers in overweight to obese women: is there any influence of menopause? Menopause 20:185–193. CrossRefPubMedGoogle Scholar
  37. 37.
    Soules MR, Sherman S, Parrott E, Rebar R, Santoro N, Utian W, Woods N (2001) Executive summary: stages of reproductive aging workshop (STRAW). Climacteric 4:267–272CrossRefGoogle Scholar
  38. 38.
    St-Pierre AC, Cantin B, Dagenais GR, Mauriege P, Despres JP, Lamarche B (2004) The triglyceride/high-density lipoprotein cholesterol ratio, the small dense low-density lipoprotein phenotype, and ischemic heart disease risk. Metab Syndr Relat Disord 2:57–64. CrossRefPubMedGoogle Scholar
  39. 39.
    Tchernof A, Despres JP (2013) Pathophysiology of human visceral obesity: an update. Physiol Rev 93:359–404. CrossRefPubMedGoogle Scholar
  40. 40.
    Tremblay A, Sévigny J, Leblanc C, Bouchard C (1983) The reproducibility of a three-day dietary record. Nutr J 3:819–830Google Scholar
  41. 41.
    van Gemert WA, May AM, Schuit AJ, Oosterhof BY, Peeters PH, Monninkhof EM (2016) Effect of weight loss with or without exercise on inflammatory markers and adipokines in postmenopausal women: the SHAPE-2 trial, a randomized controlled trial. Cancer Epidemiol Biomark Prev 25:799–806. CrossRefGoogle Scholar
  42. 42.
    Vega GL, Grundy SM (2013) Metabolic risk susceptibility in men is partially related to adiponectin/leptin ratio. J Obes 2013:1–9. CrossRefGoogle Scholar
  43. 43.
    Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27:1487–1495CrossRefGoogle Scholar

Copyright information

© University of Navarra 2018

Authors and Affiliations

  • Andrée-Anne Clément
    • 1
    • 2
  • Eléonor Riesco
    • 3
  • Sébastien Tessier
    • 4
  • Michel Lacaille
    • 1
    • 2
  • Francine Pérusse
    • 1
    • 2
  • Mélanie Coté
    • 2
  • Jean-Pierre Després
    • 1
    • 2
  • John Weisnagel
    • 5
    • 6
  • Jean Doré
    • 1
  • Denis R. Joanisse
    • 1
    • 2
  • Pascale Mauriège
    • 1
    • 2
    Email author
  1. 1.Department of Kinesiology, Faculty of MedicineLaval UniversityQuébecCanada
  2. 2.Québec Heart and Lung University Research CentreQuébecCanada
  3. 3.Faculty of Physical Activity Sciences, University of Sherbrooke, and Research Centre on AgingCIUSSS de l’Estrie – CHUSSherbrookeCanada
  4. 4.Institut National de Santé PubliqueQuébecCanada
  5. 5.Lipid Research CentreCentre Hospitalier de l’Université Laval (CHUL)QuébecCanada
  6. 6.Diabetes Research UnitCentre Hospitalier de l’Université Laval (CHUL)QuébecCanada

Personalised recommendations