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Lipid accumulation product and visceral adiposity index are effective markers for identifying the metabolically obese normal-weight phenotype

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Abstract

Aim

Studies have identified the metabolically obese normal-weight (MONW) phenotype, which carries increased risk of diabetes and cardiovascular disease. We aimed to investigate the ability of lipid accumulation product (LAP) and visceral adiposity index (VAI), two markers of visceral obesity, to identify the MONW phenotype.

Methods

Normal-weight participants [body mass index (BMI) being of 18.5–23 kg/m2] (n = 3,552; 46.9 % men) in the 2009 nationwide China Health and Nutrition Survey were included in our analysis. Four different criteria that have been published were used to define the MONW phenotype. LAP and VAI were calculated according to published formula.

Results

Receiver operating characteristic (ROC) curve analysis revealed that, regardless of the definition used to define MONW phenotype, both LAP [area under the ROC curve (AUC) ranging from 0.606 to 0.807 depending on the criteria used for MONW phenotype] and VAI (AUC ranging from 0.611 to 0.835 depending on the criteria used for MONW phenotype) outperformed anthropometric parameters including BMI, waist circumference, waist-to-hip ratio, and waist-to-height ratio for identifying MONW phenotype. Both LAP and VAI were strongly related to the MONW phenotype, irrespective of the criteria used to define the MONW phenotype. The associations between the 4th quartile of LAP and the MONW phenotype or between the 4th quartile of VAI and the MONW phenotype were consistently seen in various subgroups.

Conclusion

Our study demonstrates that both LAP and VAI are effective markers for identifying the Chinese adults with MONW phenotype.

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References

  1. Karelis AD, St-Pierre DH, Conus F, Rabasa-Lhoret R, Poehlman ET (2004) Metabolic and body composition factors in subgroups of obesity: what do we know? J Clin Endocrinol Metab 89:2569–2575

    Article  CAS  PubMed  Google Scholar 

  2. Wildman RP, Muntner P, Reynolds K, McGinn AP, Rajpathak S, Wylie-Rosett J, Sowers MR (2008) The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999–2004). Arch Intern Med 168:1617–1624

    Article  PubMed  Google Scholar 

  3. Pajunen P, Kotronen A, Korpi-Hyovalti E, Keinanen-Kiukaanniemi S, Oksa H, Niskanen L, Saaristo T, Saltevo JT, Sundvall J, Vanhala M, Uusitupa M, Peltonen M (2011) Metabolically healthy and unhealthy obesity phenotypes in the general population: the FIN-D2D Survey. BMC Public Health 11:754

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Kuk JL, Ardern CI (2009) Are metabolically normal but obese individuals at lower risk for all-cause mortality? Diabetes Care 32:2297–2299

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  7. Conus F, Allison DB, Rabasa-Lhoret R, St-Onge M, St-Pierre DH, Tremblay-Lebeau A, Poehlman ET (2004) Metabolic and behavioral characteristics of metabolically obese but normal-weight women. J Clin Endocrinol Metab 89:5013–5020

    Article  CAS  PubMed  Google Scholar 

  8. Nazare JA, Smith JD, Borel AL, Haffner SM, Balkau B, Ross R, Massien C, Almeras N, Despres JP (2012) Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the international study of prediction of intra-abdominal adiposity and its relationship with cardiometabolic risk/intra-abdominal adiposity. Am J Clin Nutr 96:714–726

    Article  CAS  PubMed  Google Scholar 

  9. Kahn HS (2005) The “lipid accumulation product” performs better than the body mass index for recognizing cardiovascular risk: a population-based comparison. BMC Cardiovasc Disord 5:26

    Article  PubMed Central  PubMed  Google Scholar 

  10. Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, Galluzzo A (2010) Visceral adiposity index: a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care 33:920–922

    Article  PubMed Central  PubMed  Google Scholar 

  11. Popkin BM, Du S, Zhai F, Zhang B (2010) Cohort profile: The China Health and Nutrition Survey—monitoring and understanding socio-economic and health change in China, 1989–2011. Int J Epidemiol 39:1435–1440

    Article  PubMed Central  PubMed  Google Scholar 

  12. WHO Expert Consultation (2004) Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363:157–163

  13. Karelis AD, Rabasa-Lhoret R (2008) Inclusion of C-reactive protein in the identification of metabolically healthy but obese (MHO) individuals. Diabetes Metab 34:183–184

    Article  CAS  PubMed  Google Scholar 

  14. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive summary of the third report of The National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 285:2486–2497

  15. Meigs JB, Wilson PW, Fox CS, Vasan RS, Nathan DM, Sullivan LM, D’Agostino RB (2006) Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab 91:2906–2912

    Article  CAS  PubMed  Google Scholar 

  16. Gordon-Larsen P, Adair LS, Meigs JB, Mayer-Davis E, Herring A, Yan SK, Zhang B, Du S, Popkin BM (2013) Discordant risk: overweight and cardiometabolic risk in Chinese adults. Obesity 21:E166–E174

    Article  CAS  PubMed  Google Scholar 

  17. Arnlov J, Ingelsson E, Sundstrom J, Lind L (2010) Impact of body mass index and the metabolic syndrome on the risk of cardiovascular disease and death in middle-aged men. Circulation 121:230–236

    Article  PubMed  Google Scholar 

  18. Bays HE (2011) Adiposopathy is “sick fat” a cardiovascular disease? J Am Coll Cardiol 57:2461–2473

    Article  CAS  PubMed  Google Scholar 

  19. Gallagher D, Visser M, Sepulveda D, Pierson RN, Harris T, Heymsfield SB (1996) How useful is body mass index for comparison of body fatness across age, sex, and ethnic groups? Am J Epidemiol 143:228–239

    Article  CAS  PubMed  Google Scholar 

  20. Roubenoff R (2004) Sarcopenic obesity: the confluence of two epidemics. Obes Res 12:887–888

    Article  PubMed  Google Scholar 

  21. Hill JO, Sidney S, Lewis CE, Tolan K, Scherzinger AL, Stamm ER (1999) Racial differences in amounts of visceral adipose tissue in young adults: the CARDIA (Coronary Artery Risk Development in Young Adults) study. Am J Clin Nutr 69:381–387

    CAS  PubMed  Google Scholar 

  22. Harris TB, Visser M, Everhart J, Cauley J, Tylavsky F, Fuerst T, Zamboni M, Taaffe D, Resnick HE, Scherzinger A, Nevitt M (2000) Waist circumference and sagittal diameter reflect total body fat better than visceral fat in older men and women: the health, aging and body composition study. Ann NY Acad Sci 904:462–473

    Article  CAS  PubMed  Google Scholar 

  23. Lemieux I, Pascot A, Couillard C, Lamarche B, Tchernof A, Almeras N, Bergeron J, Gaudet D, Tremblay G, Prud’homme D, Nadeau A, Despres JP (2000) Hypertriglyceridemic waist: a marker of the atherogenic metabolic triad (hyperinsulinemia; hyperapolipoprotein B; small, dense LDL) in men? Circulation 102:179–184

    Article  CAS  PubMed  Google Scholar 

  24. Tanko LB, Bagger YZ, Qin G, Alexandersen P, Larsen PJ, Christiansen C (2005) Enlarged waist combined with elevated triglycerides is a strong predictor of accelerated atherogenesis and related cardiovascular mortality in postmenopausal women. Circulation 111:1883–1890

    Article  CAS  PubMed  Google Scholar 

  25. Sam S, Haffner S, Davidson MH, D’Agostino RB Sr, Feinstein S, Kondos G, Perez A, Mazzone T (2009) Hypertriglyceridemic waist phenotype predicts increased visceral fat in subjects with type 2 diabetes. Diabetes Care 32:1916–1920

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Taverna MJ, Martinez-Larrad MT, Frechtel GD, Serrano-Rios M (2011) Lipid accumulation product: a powerful marker of metabolic syndrome in healthy population. Eur J Endocrinol 164:559–567

    Article  CAS  PubMed  Google Scholar 

  27. Ioachimescu AG, Brennan DM, Hoar BM, Hoogwerf BJ (2010) The lipid accumulation product and all-cause mortality in patients at high cardiovascular risk: a PreCIS database study. Obesity (Silver Spring) 18:1836–1844

    Article  CAS  Google Scholar 

  28. Wehr E, Pilz S, Boehm BO, Marz W, Obermayer-Pietsch B (2011) The lipid accumulation product is associated with increased mortality in normal weight postmenopausal women. Obesity (Silver Spring) 19:1873–1880

    Article  CAS  Google Scholar 

  29. Zhang X, Shu XO, Li H, Yang G, Xiang YB, Cai Q, Ji BT, Gao YT, Zheng W (2013) Visceral adiposity and risk of coronary heart disease in relatively lean Chinese adults. Int J Cardiol 168:2141–2145

    Article  PubMed Central  PubMed  Google Scholar 

  30. Mangge H, Zelzer S, Puerstner P, Schnedl WJ, Reeves G, Postolache TT, Weghuber D (2013) Uric acid best predicts metabolically unhealthy obesity with increased cardiovascular risk in youth and adults. Obesity (Silver Spring) 21:E71–E77

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the China Health and Nutrition Survey, supported by the NIH (R01-HD30880, DK056350, and R01-HD38700), and the National Institute of Nutrition and Food Safety, China Center for Disease Control and Prevention, Carolina Population Center, the University of North Carolina at Chapel Hill and the Fogarty International Center for providing the data used here. We also thank the China-Japan Friendship Hospital and Ministry of Health for support for CHNS 2009 survey.

Conflict of interest

Tingting Du, Xuefeng Yu, Jianhua Zhang, and Xingxing Sun declare that they have no conflict of interest.

Ethical standard

The study was approved by the institutional review committees of the University of North Carolina at Chapel Hill, the National Institute of Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, and the China-Japan Friendship Hospital, Ministry of Health.

Human and Animal Rights disclosure

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2008.

Informed consent

Informed consent was obtained from all patients for being included in the study.

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Authors and Affiliations

  1. Department of Endocrinology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Tingting Du, Xuefeng Yu & Jianhua Zhang

  2. Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Xingxing Sun

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  1. Tingting Du
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  2. Xuefeng Yu
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Correspondence to Jianhua Zhang or Xingxing Sun.

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Du, T., Yu, X., Zhang, J. et al. Lipid accumulation product and visceral adiposity index are effective markers for identifying the metabolically obese normal-weight phenotype. Acta Diabetol 52, 855–863 (2015). https://doi.org/10.1007/s00592-015-0715-2

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  • DOI: https://doi.org/10.1007/s00592-015-0715-2

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