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Comparison of the effect of ‘metabolically healthy but obese’ and ‘metabolically abnormal but not obese’ phenotypes on development of diabetes and cardiovascular disease in Chinese

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Abstract

The present study was designed to determine the prevalence of ‘metabolically healthy but obese’ (MHO) and ‘metabolically abnormal but not obese’ (MANO) phenotypes in Chinese population, and to investigate the association of these two phenotypes with the risk of diabetes and cardiovascular disease (CVD). A total of 2,764 subjects aged 30–90 were followed up over a mean period of 43.80 ± 11.25 months. The metabolic syndrome was defined according to the joint committee for developing Chinese guidelines on prevention and treatment of dyslipidemia in adults. Subjects with body fat percentage (BF %) >25 % for men or BF % >35 % for women were defined as being obese. The proportion of MHO and MANO phenotypes were 22.9, 7.6 % in men, and 26.2, 6.0 % in women, respectively. The MANO phenotype was associated with increased risk for diabetes both in men [hazard ratios (HR): 4.44 (1.21–16.26)] and women [HR: 8.68 (2.87–24.96)] after adjustment of age, serum total cholesterol (TC), triglycerides (TG), and family history of diabetes. This association held for CVD in women [HR: 2.87 (1.44–5.73)], but not in men after adjustment of age, serum TC, TG, and family history of CVD. No association was observed between the MHO phenotype and incident diabetes or CVD. MHO and MANO phenotypes are common in Chinese population. Metabolic risk factors appeared to play a more important role in the development of diabetes and CVD than body fat alone.

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References

  1. S. Frood, L.M. Johnston, C.L. Matteson, D.T. Finegood, Obesity, Complexity, and the Role of the Health System. Curr. Obes. Rep. 2, 320–326 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  2. G. Reaven, F. Abbasi, T. McLaughlin, Obesity, insulin resistance, and cardiovascular disease. Recent Prog. Horm. Res. 59, 207–223 (2004)

    Article  CAS  PubMed  Google Scholar 

  3. E. Bonora, The metabolic syndrome and cardiovascular disease. Ann. Med. 38, 64–80 (2006)

    Article  CAS  PubMed  Google Scholar 

  4. N. Stefan, H.U. Haring, F.B. Hu, M.B. Schulze, Metabolically healthy obesity: epidemiology, mechanisms, and clinical implications. Lancet Diabetes Endocrinol. 1, 152–162 (2013)

    Article  PubMed  Google Scholar 

  5. F. Conus, R. Rabasa-Lhoret, F. Peronnet, Characteristics of metabolically obese normal-weight (MONW) subjects. Appl. Physiol. Nutr. Metab. 32, 4–12 (2007)

    Article  PubMed  Google Scholar 

  6. A.D. Karelis, M. Brochu, R. Rabasa-Lhoret, Can we identify metabolically healthy but obese individuals (MHO)? Diabetes Metab. 30, 569–572 (2004)

    Article  CAS  PubMed  Google Scholar 

  7. G.V. Denis, M.S. Obin, ‘Metabolically healthy obesity’: origins and implications. Mol. Aspects Med. 34, 59–70 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. M. Bluher, The distinction of metabolically ‘healthy’ from ‘unhealthy’ obese individuals. Curr. Opin. Lipidol. 21, 38–43 (2010)

    Article  PubMed  Google Scholar 

  9. C. Voulgari, N. Tentolouris, P. Dilaveris, D. Tousoulis, N. Katsilambros, C. Stefanadis, Increased heart failure risk in normal-weight people with metabolic syndrome compared with metabolically healthy obese individuals. J. Am. Coll. Cardiol. 58, 1343–1350 (2011)

    Article  CAS  PubMed  Google Scholar 

  10. S.H. Lee, H.S. Ha, Y.J. Park, J.H. Lee, H.W. Yim, K.H. Yoon, M.I. Kang, W.C. Lee, H.Y. Son, Y.M. Park, H.S. Kwon, Identifying metabolically obese but normal-weight (MONW) individuals in a nondiabetic Korean population: the Chungju Metabolic disease Cohort (CMC) study. Clin. Endocrinol. (Oxf) 75, 475–481 (2011)

    Article  Google Scholar 

  11. J.B. Meigs, P.W. Wilson, C.S. Fox, R.S. Vasan, D.M. Nathan, L.M. Sullivan, R.B. D’Agostino, Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J. Clin. Endocrinol. Metab. 91, 2906–2912 (2006)

    Article  CAS  PubMed  Google Scholar 

  12. S. Camastra, E. Bonora, S. Del Prato, K. Rett, M. Weck, E. Ferrannini, Effect of obesity and insulin resistance on resting and glucose-induced thermogenesis in man. EGIR (European Group for the Study of Insulin Resistance). Int. J. Obes. Relat. Metab. Disord. 23, 1307–1313 (1999)

    Article  CAS  PubMed  Google Scholar 

  13. E. Bonora, S. Kiechl, J. Willeit, F. Oberhollenzer, G. Egger, G. Targher, M. Alberiche, R.C. Bonadonna, M. Muggeo, Prevalence of insulin resistance in metabolic disorders: the Bruneck Study. Diabetes 47, 1643–1649 (1998)

    Article  CAS  PubMed  Google Scholar 

  14. N. Ruderman, D. Chisholm, X. Pi-Sunyer, S. Schneider, The metabolically obese, normal-weight individual revisited. Diabetes 47, 699–713 (1998)

    Article  CAS  PubMed  Google Scholar 

  15. R.V. Dvorak, W.F. DeNino, P.A. Ades, E.T. Poehlman, Phenotypic characteristics associated with insulin resistance in metabolically obese but normal-weight young women. Diabetes 48, 2210–2214 (1999)

    Article  CAS  PubMed  Google Scholar 

  16. F. Conus, D.B. Allison, R. Rabasa-Lhoret, M. St-Onge, D.H. St-Pierre, A. Tremblay-Lebeau, E.T. Poehlman, Metabolic and behavioral characteristics of metabolically obese but normal-weight women. J. Clin. Endocrinol. Metab. 89, 5013–5020 (2004)

    Article  CAS  PubMed  Google Scholar 

  17. W.H.O. Expert, Consultation, Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363, 157–163 (2004)

    Article  Google Scholar 

  18. R.C. Ma, J.C. Chan, Type 2 diabetes in East Asians: similarities and differences with populations in Europe and the United States. Ann. N. Y. Acad. Sci. 1281, 64–91 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  19. L.L. Roberson, E.C. Aneni, W. Maziak, A. Agatston, T. Feldman, M. Rouseff, T. Tran, M.J. Blaha, R.D. Santos, A. Sposito, M.H. Al-Mallah, R. Blankstein, M.J. Budoff, K. Nasir, Beyond BMI: The “Metabolically healthy obese” phenotype and its association with clinical/subclinical cardiovascular disease and all-cause mortality – a systematic review. BMC Public Health 14, 14 (2014)

    Article  PubMed Central  PubMed  Google Scholar 

  20. W.P. Jia, C. Pang, L. Chen, Y.Q. Bao, J.X. Lu, H.J. Lu, J.L. Tang, Y.M. Wu, Y.H. Zuo, S.Y. Jiang, K.S. Xiang, Epidemiological characteristics of diabetes mellitus and impaired glucose regulation in a Chinese adult population: the Shanghai Diabetes Studies, a cross-sectional 3-year follow-up study in Shanghai urban communities. Diabetologia 50, 286–292 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. C. Wang, X.H. Hou, M.L. Zhang, Y.Q. Bao, Y.H. Zou, W.H. Zhong, K.S. Xiang, W.P. Jia, Comparison of body mass index with body fat percentage in the evaluation of obesity in Chinese. Biomed. Environ. Sci. 23, 173–179 (2010)

    Article  PubMed  Google Scholar 

  22. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419 (1985)

    Article  CAS  PubMed  Google Scholar 

  23. W. Jia, H. Wu, Y. Bao, C. Wang, J. Lu, J. Zhu, K. Xiang, Association of serum retinol-binding protein 4 and visceral adiposity in Chinese subjects with and without type 2 diabetes. J. Clin. Endocrinol. Metab. 92, 3224–3229 (2007)

    Article  CAS  PubMed  Google Scholar 

  24. M. Matsuda, R.A. DeFronzo, Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 22, 1462–1470 (1999)

    Article  CAS  PubMed  Google Scholar 

  25. C. Wang, X. Hou, Y. Bao, J. Pan, Y. Zuo, W. Zhong, W. Jia, K. Xiang, The metabolic syndrome increased risk of cardiovascular events in Chinese–a community based study. Int. J. Cardiol. 139, 159–165 (2010)

    Article  PubMed  Google Scholar 

  26. L. Li, C. Wang, Y. Bao, L. Peng, H. Gu, W. Jia, Optimal body fat percentage cut-offs for obesity in Chinese adults. Clin. Exp. Pharmacol. Physiol. 39, 393–398 (2013)

    Article  Google Scholar 

  27. Y. Bao, J. Lu, C. Wang, M. Yang, H. Li, X. Zhang, J. Zhu, H. Lu, W. Jia, K. Xiang, Optimal waist circumference cutoffs for abdominal obesity in Chinese. Atherosclerosis 201, 378–384 (2008)

    Article  CAS  PubMed  Google Scholar 

  28. K.G. Alberti, P.Z. Zimmet, Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 15, 539–553 (1998)

    Article  CAS  PubMed  Google Scholar 

  29. M.A. Foulkes, P.A. Wolf, T.R. Price, J.P. Mohr, D.B. Hier, The Stroke Data Bank: design, methods, and baseline characteristics. Stroke 19, 547–554 (1988)

    Article  CAS  PubMed  Google Scholar 

  30. H. Tunstall-Pedoe, K. Kuulasmaa, P. Amouyel, D. Arveiler, A.M. Rajakangas, A. Pajak, Myocardial infarction and coronary deaths in the World Health Organization MONICA Project. Registration procedures, event rates, and case-fatality rates in 38 populations from 21 countries in four continents. Circulation 90, 583–612 (1994)

    Article  CAS  PubMed  Google Scholar 

  31. F. Soriguer, C. Gutierrez-Repiso, E. Rubio-Martin, E. Garcia-Fuentes, M.C. Almaraz, N. Colomo, I. Esteva de Antonio, M.S. de Adana, F.J. Chaves, S. Morcillo, S. Valdés, G. Rojo-Martínez, Metabolically healthy but obese, a matter of time? Findings from the prospective Pizarra study. J. Clin. Endocrinol. Metab. 98, 2318–2325 (2013)

    Article  CAS  PubMed  Google Scholar 

  32. Z. Pataky, E. Bobbioni-Harsch, A. Golay, Open questions about metabolically normal obesity. Int. J. Obes. (Lond) 34(Suppl 2), S18–23 (2010)

    Article  Google Scholar 

  33. B.J. Kwon, D.W. Kim, S.H. Her, D.B. Kim, S.W. Jang, E.J. Cho, S.H. Ihm, H.Y. Kim, H.J. Youn, K.B. Seung, J.H. Kim, T.H. Rho, Metabolically obese status with normal weight is associated with both the prevalence and severity of angiographic coronary artery disease. Metabolism 62, 952–960 (2013)

    Article  CAS  PubMed  Google Scholar 

  34. C.M. Phillips, C. Dillon, J.M. Harrington, V.J. McCarthy, P.M. Kearney, A.P. Fitzgerald, I.J. Perry, Defining metabolically healthy obesity: role of dietary and lifestyle factors. PLoS ONE 8, e76188 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. A.D. Karelis, D.H. St-Pierre, F. Conus, R. Rabasa-Lhoret, E.T. Poehlman, Metabolic and body composition factors in subgroups of obesity: what do we know? J. Clin. Endocrinol. Metab. 89, 2569–2575 (2004)

    Article  CAS  PubMed  Google Scholar 

  36. M.P. St-Onge, I. Janssen, S.B. Heymsfield, Metabolic syndrome in normal-weight Americans: new definition of the metabolically obese, normal-weight individual. Diabetes Care 27, 2222–2228 (2004)

    Article  PubMed  Google Scholar 

  37. G. Iacobellis, M.C. Ribaudo, A. Zappaterreno, C.V. Iannucci, F. Leonetti, Prevalence of uncomplicated obesity in an Italian obese population. Obes. Res. 13, 1116–1122 (2005)

    Article  PubMed  Google Scholar 

  38. M. Hamer, E. Stamatakis, Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality. J. Clin. Endocrinol. Metab. 97, 2482–2488 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. W.P. Jia, C. Wang, S. Jiang, J.M. Pan, Characteristics of obesity and its related disorders in China. Biomed. Environ. Sci. 23, 4–11 (2010)

    Article  CAS  PubMed  Google Scholar 

  40. K.M. Choi, H.J. Cho, H.Y. Choi, S.J. Yang, H.J. Yoo, J.A. Seo, S.G. Kim, S.H. Baik, D.S. Choi, N.H. Kim, Higher mortality in metabolically obese normal-weight people than in metabolically healthy obese subjects in elderly Koreans. Clin. Endocrinol. (Oxf) 79, 364–370 (2013)

    Article  Google Scholar 

  41. A.D. Karelis, M. Faraj, J.P. Bastard, D.H. St-Pierre, M. Brochu, D. Prud’homme, R. Rabasa-Lhoret, The metabolically healthy but obese individual presents a favorable inflammation profile. J. Clin. Endocrinol. Metab. 90, 4145–4150 (2005)

    Article  CAS  PubMed  Google Scholar 

  42. S.L. Appleton, C.J. Seaborn, R. Visvanathan, C.L. Hill, T.K. Gill, A.W. Taylor, R.J. Adams, North West Adelaide Health Study, Team, Diabetes and cardiovascular disease outcomes in the metabolically healthy obese phenotype: a cohort study. Diabetes Care 36, 2388–2394 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  43. T. McLaughlin, G. Allison, F. Abbasi, C. Lamendola, G. Reaven, Prevalence of insulin resistance and associated cardiovascular disease risk factors among normal weight, overweight, and obese individuals. Metabolism 53, 495–499 (2004)

    Article  CAS  PubMed  Google Scholar 

  44. Y. Shimamoto, M. Mizukoshi, A. Kuroi, T. Imanishi, T. Takeshita, M. Terada, T. Akasaka, Is visceral fat really a coronary risk factor? A multi-detector computed tomography study. Int. Heart J. 54, 273–278 (2013)

    Article  PubMed  Google Scholar 

  45. Y. Wang, E.B. Rimm, M.J. Stampfer, W.C. Willett, F.B. Hu, Comparison of abdominal adiposity and overall obesity in predicting risk of type 2 diabetes among men. Am. J. Clin. Nutr. 81, 555–563 (2005)

    CAS  PubMed  Google Scholar 

  46. N. Stefan, K. Kantartzis, J. Machann, F. Schick, C. Thamer, K. Rittig, B. Balletshofer, F. Machicao, A. Fritsche, H.U. Haring, Identification and characterization of metabolically benign obesity in humans. Arch. Intern. Med. 168, 1609–1616 (2008)

    Article  PubMed  Google Scholar 

  47. N. Stefan, H.U. Haring, The role of hepatokines in metabolism. Nat. Rev. Endocrinol. 9, 144–152 (2013)

    Article  CAS  PubMed  Google Scholar 

  48. K.J. Hunt, R.G. Resendez, K. Williams, S.M. Haffner, M.P. Stern, San Antonio Heart Study, National Cholesterol Education Program versus World Health Organization metabolic syndrome in relation to all-cause and cardiovascular mortality in the San Antonio Heart Study. Circulation 110, 1251–1257 (2004)

    Article  PubMed  Google Scholar 

  49. G.N. Thomas, C.M. Schooling, S.M. McGhee, S.Y. Ho, B.M. Cheung, N.M. Wat, E.D. Janus, K.S. Lam, T.H. Lam, Hong Kong Cardiovascular Risk Factor Prevalence Study Steering Committee, Metabolic syndrome increases all-cause and vascular mortality: the Hong Kong Cardiovascular Risk Factor Study. Clin. Endocrinol. (Oxf) 66, 666–671 (2007)

    Article  Google Scholar 

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Acknowledgments

This work was supported by Drug Innovation Program of National Science and Technology Project (No. 2011ZX09307-001-02) and the Public Health Key Disciplines of Shanghai (No. 12GWZX0104).

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Correspondence to Chen Wang.

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Deng Luo and Fang Liu are contributed equally to this work.

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Luo, D., Liu, F., Li, X. et al. Comparison of the effect of ‘metabolically healthy but obese’ and ‘metabolically abnormal but not obese’ phenotypes on development of diabetes and cardiovascular disease in Chinese. Endocrine 49, 130–138 (2015). https://doi.org/10.1007/s12020-014-0444-2

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