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Metabolic Features of Individuals with Obesity Referred for Bariatric and Metabolic Surgery: a Cohort Study

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A Correction to this article was published on 18 May 2020

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Abstract

Background

The concept of metabolic obesity phenotypes has been proposed, but its relevance to metabolic features is unclear.

Purpose

To determine a new definition of metabolic obesity phenotype, investigate the characteristics of expressing clustered normal and abnormal metabolic parameters, and analyze factors associated with metabolic abnormalities.

Materials and Methods

Characteristics of 600 patients were analyzed. The definition of metabolic obesity phenotype includes elevated blood pressure, glucose, lipid, and uric acid levels and abnormal lipoprotein levels. Independent sample t test and a general linear model with repeated measures were applied to investigate the differences in metabolic parameters.

Results

A total of 108 (18.0%) participants were obese yet metabolically healthy, whereas 492 (82.0%) were obese and metabolically unhealthy. Body weight at baseline was significantly higher in metabolically unhealthy phenotype (P < 0.001). For non-phasic oral glucose tolerance test (OGTT) curve shape, 100% glucose, 100% C-peptide, and 95.8% insulin curves were found in the metabolically unhealthy group. Men had an increased risk for elevated lipid level than women (OR = 1.83, 1.21–2.77). Individuals with class II/III obesity had an increased risk for elevated blood pressure, glucose, and UA levels than did those with class I obesity (OR = 2.22, 1.43–3.44; OR = 1.73, 1.11–2.68; OR = 3.61, 2.29–5.69, respectively).

Conclusions

Approximately one-fifth of individuals with obesity had a metabolically healthy phenotype, and nearly one-third of individuals with class III obesity had this phenotype. Non-phasic OGTT curve shape is a meaningful predictive factor of metabolically unhealthy phenotype before bariatric surgery. Male sex and class II/III obesity are risk factors associated with specific metabolic abnormalities.

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Change history

  • 18 May 2020

    In the original articles there are data errors in some of the Figure 2 tables. The corrected Figure 2 tables follow.

References

  1. Collaboration, N.C.D.R.F. 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. 2016;387(10026):1377–96.

    Article  Google Scholar 

  2. Bray GA, Heisel WE, Afshin A, et al. The science of obesity management: an Endocrine Society scientific statement. Endocr Rev. 2018;39(2):79–132.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Arterburn D, Courcoulas A. Bariatric surgery for obesity and metabolic conditions in adults. BMJ. 2014;349:g3961.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Christ JP, Falcone T. Bariatric surgery improves Hyperandrogenism, menstrual irregularities, and metabolic dysfunction among women with polycystic ovary syndrome (PCOS). Obes Surg. 2018;28:2171–7.

    Article  PubMed  Google Scholar 

  5. Sung H, et al. Global patterns in excess body weight and the associated cancer burden.CA Cancer J Clin, 2018.

  6. Garvey WT et al. American association of clinical endocrinologists and american college of endocrinology position statement on the 2014 advanced framework for a new diagnosis of obesity as a chronic disease. Endocr Pract. 2014;20(9):977–89.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Garvey WT, Mechanick JI, Brett EM, et al. American Association of Clinical Endocrinologists and American College of endocrinology comprehensive clinical practice guidelines for medical Care of Patients with obesity. Endocr Pract. 2016;22(Suppl 3):1–203.

    Article  PubMed  Google Scholar 

  8. Roberson LL, Aneni EC, Maziak W, et al. Beyond BMI: the "metabolically healthy obese" phenotype & its association with clinical/subclinical cardiovascular disease and all-cause mortality -- a systematic review. BMC Public Health. 2014;14:14.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wildman RP, Muntner P, Reynolds K, et al. 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. 2008;168(15):1617–24.

    Article  PubMed  Google Scholar 

  10. Appleton SL, Seaborn CJ, Visvanathan R, et al. Diabetes and cardiovascular disease outcomes in the metabolically healthy obese phenotype: a cohort study. Diabetes Care. 2013;36(8):2388–94.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kramer CK, Zinman B, Retnakaran R. Are metabolically healthy overweight and obesity benign conditions?: a systematic review and meta-analysis. Ann Intern Med. 2013;159(11):758–69.

    Article  PubMed  Google Scholar 

  12. Mathew H, Farr OM, Mantzoros CS. Metabolic health and weight: understanding metabolically unhealthy normal weight or metabolically healthy obese patients. Metabolism. 2016;65(1):73–80.

    Article  CAS  PubMed  Google Scholar 

  13. Lotta LA, Abbasi A, Sharp SJ, et al. Definitions of metabolic health and risk of future type 2 diabetes in BMI categories: asystematic review and network meta-analysis. Diabetes Care. 2015;38(11):2177–87.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Karelis AD, Rabasa-Lhoret R. Inclusion of C-reactive protein in the identification of metabolically healthy but obese (MHO) individuals. Diabetes Metab. 2008;34(2):183–4.

    Article  CAS  PubMed  Google Scholar 

  15. Stefan N, Häring HU, Hu FB, et al. Metabolically healthy obesity: epidemiology, mechanisms, and clinical implications. Lancet Diabetes Endocrinol. 2013;1(2):152–62.

    Article  PubMed  Google Scholar 

  16. Stefan N, Haring HU, Schulze MB. Metabolically healthy obesity: the low-hanging fruit in obesity treatment? Lancet Diabetes Endocrinol. 2018;6(3):249–58.

    Article  PubMed  Google Scholar 

  17. Hinnouho GM, Czernichow S, Dugravot A, et al. Metabolically healthy obesity and the risk of cardiovascular disease and type 2 diabetes: the Whitehall II cohort study. Eur Heart J. 2015;36(9):551–9.

    Article  PubMed  Google Scholar 

  18. Heianza Y, Arase Y, Tsuji H, et al. Metabolically healthy obesity, presence or absence of fatty liver, and risk of type 2 diabetes in Japanese individuals: Toranomon hospital health management center study 20 (TOPICS 20). J Clin Endocrinol Metab. 2014;99(8):2952–60.

    Article  CAS  PubMed  Google Scholar 

  19. Heianza Y, Kato K, Kodama S, et al. Stability and changes in metabolically healthy overweight or obesity and risk of future diabetes: Niigata wellness study. Obesity (Silver Spring). 2014;22(11):2420–5.

    Article  Google Scholar 

  20. Jung CH et al. Association of metabolically healthy obesity with subclinical coronary atherosclerosis in a Korean population. Obesity (Silver Spring). 2014;22(12):2613–20.

    Google Scholar 

  21. Twig G, Afek A, Derazne E, et al. Diabetes risk among overweight and obese metabolically healthy young adults. Diabetes Care. 2014;37(11):2989–95.

    Article  CAS  PubMed  Google Scholar 

  22. Meigs JB, Wilson PWF, Fox CS, et al. Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab. 2006;91(8):2906–12.

    Article  CAS  PubMed  Google Scholar 

  23. Arnlov J, Sundstrom J, Ingelsson E, et al. Impact of BMI and the metabolic syndrome on the risk of diabetes in middle-aged men. Diabetes Care. 2011;34(1):61–5.

    Article  PubMed  CAS  Google Scholar 

  24. Bo S, Musso G, Gambino R, et al. Prognostic implications for insulin-sensitive and insulin-resistant normal-weight and obese individuals from a population-based cohort. Am J Clin Nutr. 2012;96(5):962–9.

    Article  CAS  PubMed  Google Scholar 

  25. Soriguer F, Gutiérrez-Repiso C, Rubio-Martín E, et al. Metabolically healthy but obese, a matter of time? Findings from the prospective Pizarra study. J Clin Endocrinol Metab. 2013;98(6):2318–25.

    Article  CAS  PubMed  Google Scholar 

  26. Aung K, Lorenzo C, Hinojosa MA, et al. Risk of developing diabetes and cardiovascular disease in metabolically unhealthy normal-weight and metabolically healthy obese individuals. J Clin Endocrinol Metab. 2014;99(2):462–8.

    Article  CAS  PubMed  Google Scholar 

  27. Bell JA, Kivimaki M, Hamer M. Metabolically healthy obesity and risk of incident type 2 diabetes: a meta-analysis of prospective cohort studies. Obes Rev. 2014;15(6):504–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hamer M, Stamatakis E. Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality. J Clin Endocrinol Metab. 2012;97(7):2482–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Consultation, W.H.O.E. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363(9403):157–63.

    Article  Google Scholar 

  30. Williams B et al. ESC/ESH guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension: the task force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension. J Hypertens. 2018;36(10):1953–2041.

    Article  CAS  PubMed  Google Scholar 

  31. Expert Committee on the, D. and M. Classification of Diabetes. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 2003;26(Suppl 1):S5–20.

    Google Scholar 

  32. Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.

    Article  CAS  Google Scholar 

  33. Phillips DI et al. Understanding oral glucose tolerance: comparison of glucose or insulin measurements during the oral glucose tolerance test with specific measurements of insulin resistance and insulin secretion. Diabet Med. 1994;11(3):286–92.

    Article  CAS  PubMed  Google Scholar 

  34. Tschritter O, Fritsche A, Shirkavand F, et al. Assessing the shape of the glucose curve during an oral glucose tolerance test. Diabetes Care. 2003;26(4):1026–33.

    Article  CAS  PubMed  Google Scholar 

  35. Kanauchi M, Kimura K, Kanauchi K, et al. Beta-cell function and insulin sensitivity contribute to the shape of plasma glucose curve during an oral glucose tolerance test in non-diabetic individuals. Int J Clin Pract. 2005;59(4):427–32.

    Article  CAS  PubMed  Google Scholar 

  36. Abdul-Ghani MA, Lyssenko V, Tuomi T, et al. The shape of plasma glucose concentration curve during OGTT predicts future risk of type 2 diabetes. Diabetes Metab Res Rev. 2010;26(4):280–6.

    Article  CAS  PubMed  Google Scholar 

  37. Trujillo-Arriaga HM, Roman-Ramos R. Fitting and evaluating the glucose curve during a quasi continuous sampled oral glucose tolerance test. Comput Biol Med. 2008;38(2):185–95.

    Article  CAS  PubMed  Google Scholar 

  38. Tura A, Morbiducci U, Sbrignadello S, et al. Shape of glucose, insulin, C-peptide curves during a 3-h oral glucose tolerance test: any relationship with the degree of glucose tolerance? Am J Physiol Regul Integr Comp Physiol. 2011;300(4):R941–8.

    Article  CAS  PubMed  Google Scholar 

  39. Stone NJ et al. ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association task force on practice guidelines. J Am Coll Cardiol. 2013;63(25 Pt B):2889–934.

    PubMed  Google Scholar 

  40. Garvey WT et al. American association of clinical endocrinologists and american college of endocrinology consensus conference on obesity: building an evidence base for comprehensive action. Endocr Pract. 2014;20(9):956–76.

    Article  PubMed  Google Scholar 

  41. Elahi D. In praise of the hyperglycemic clamp. A method for assessment of beta-cell sensitivity and insulin resistance. Diabetes Care. 1996;19(3):278–86.

    Article  CAS  PubMed  Google Scholar 

  42. Pacini G, Mari A. Methods for clinical assessment of insulin sensitivity and beta-cell function. Best Pract Res Clin Endocrinol Metab. 2003;17(3):305–22.

    Article  CAS  PubMed  Google Scholar 

  43. Kim JY, Coletta DK, Mandarino LJ, et al. Glucose response curve and type 2 diabetes risk in Latino adolescents. Diabetes Care. 2012;35(9):1925–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to thank all of the involved study investigators, staffs, clinicians, nurses, and technicians for dedicating their time and skills to the completion of this study.

Funding

This study was supported by National Key Technologies R&D Program (Grant No. 2015BAI13B09), Research Foundation of Beijing Friendship Hospital, Capital Medical University (Grant No. yyqdkt 2017-31), Wu Jieping Medical Foundation (Grant No. 320.2710.1813), and Beijing Municipal Administration of Hospitals Incubating Program (Grant No. PX2018001).

Author information

Author notes

  1. Mengyi Li and Yang Liu contributed equally to this work.

Authors and Affiliations

  1. Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, No.95 Yong-an Road, Xi-Cheng District, Beijing, 100050, China

    Mengyi Li, Yang Liu, Lan Jin, Lixue Wang, Kaixin Zhao, Meng Zhang, Wei Xu, Peng Zhang & Zhongtao Zhang

  2. National Clinical Research Center for Digestive Diseases, Beijing Friendship Hospital, Capital Medical University, No.95 Yong-an Road, Xi-Cheng District, Beijing, 100050, China

    Na Zeng

  3. Department of Radiology, Beijing Friendship Hospital, Capital Medical University, No.95 Yong-an Road, Xi-Cheng District, Beijing, 100050, China

    Han Lv

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  1. Mengyi Li
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Correspondence to Zhongtao Zhang.

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Statement of Informed Consent

Informed consent was obtained from all individual participants included in this study.

Statement of Human and Animal Rights

This study was performed in accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committees of Beijing Friendship Hospital, Capital Medical University.

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Li, M., Liu, Y., Jin, L. et al. Metabolic Features of Individuals with Obesity Referred for Bariatric and Metabolic Surgery: a Cohort Study. OBES SURG 29, 3966–3977 (2019). https://doi.org/10.1007/s11695-019-04067-0

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