DOI: https://doi.org/10.22263/2312-4156.2023.3.19
V.M. Bondarenko1, S.I. Pimanov1, E.V. Makarenko1, E.F. Bondarenko2
Metabolically healthy obesity: epidemiology, criteria and pathogenetic mechanisms
1Vitebsk State Order of Peoples’ Friendship Medical University, Vitebsk, Republic of Belarus
2Vitebsk Regional Clinical Hospital, Vitebsk, Republic of Belarus
Vestnik VGMU. 2023;22(3):19-28.
Abstract.
Obesity is a significant medical and social problem. The negative impact of obesity on the life expectancy and working capacity of overweight patients has been convincingly proved. This negative impact is due to the high risk of occurrence of comorbid pathology, which includes cardiovascular diseases, type 2 diabetes, osteoarthritis, gout, and some types of cancer. At the same time, considerable differences were found in the individual risk of developing concomitant diseases, which cannot be explained only by the degree of obesity. Clinical observations made it possible to identify a group of subjects with metabolically healthy obesity (MHO), who differ from metabolically unhealthy patients in the absence of cardiometabolic risk factors and a more favorable prognosis. Data on the prevalence of MHO vary significantly due to the lack of uniform criteria. The carried out literature review indicates that MHO is more common in women than in men, mainly in younger people, physically active, with a lower content of visceral adipose tissue.
Keywords: metabolically healthy obesity, metabolically unhealthy obesity, cardiovascular diseases, diabetes mellitus, cardiometabolic risk, visceral adipose tissue.
References
1. Phillips CM. Metabolically healthy obesity across the life course: epidemiology, determinants, and implications. Ann N Y Acad Sci. 2017 Mar;1391(1):85-100. doi: http://dx.doi.org/10.1111/nyas.13230
2. Neeland IJ, Ross R, Després J-P, Matsuzawa Y, Yamashita S, Shai I, et al. Visceral and ectopic fat, atherosclerosis, and cardiometabolic disease: a position statement. Lancet Diabetes Endocrinol. 2019 Sep;7(9):715-25. doi: http://dx.doi.org/10.1016/S2213-8587(19)30084-1
3. Bray GA, Kim KK, Wilding JPH. Obesity: a chronic relapsing progressive disease process. A position statement of the World Obesity Federation. Obes Rev. 2017 Jul;18(7):715-23. doi: http://dx.doi.org/10.1111/obr.12551
4. Blüher M. Metabolically Healthy Obesity. Endocr Rev. 2020 May;41(3):bnaa004. doi: http://dx.doi.org/10.1210/endrev/bnaa004
5. Iacobini C, Pugliese G, Fantauzzi CB, Federici M, Menini S. Metabolically healthy versus metabolically unhealthy obesity. Metabolism. 2019 Mar;92:51-60. doi: http://dx.doi.org/10.1016/j.metabol.2018.11.009
6. Gažarová M, Galšneiderová M, Mečiarová L. Obesity diagnosis and mortality risk based on a body shape index (ABSI) and other indices and anthropometric parameters in university students. Rocz Panstw Zakl Hig. 2019;70(3):267-75. doi: http://dx.doi.org/10.32394/rpzh.2019.0077
7. Cornier M-A, Després J-P, Davis N, Grossniklaus DA, Klein S, Lamarche B, et al. Assessing adiposity: a scientific statement from the American Heart Association. Circulation. 2011 Nov;124(18):1996-2019. doi: http://dx.doi.org/10.1161/CIR.0b013e318233bc6a
8. Berker D, Koparal S, Işik S, Paşaoğlu L, Aydin Y, Erol K, et al. Compatibility of different methods for the measurement of visceral fat in different body mass index strata. Diagn Interv Radiol. 2010 Jun;16(2):99-105. doi: http://dx.doi.org/10.4261/1305-3825.DIR.2749-09.1
9. Stefan N, Häring H-U, Hu FB, Schulze MB. Metabolically healthy obesity: epidemiology, mechanisms, and clinical implications. Lancet Diabetes Endocrinol. 2013 Oct;1(2):152-62. doi: http://dx.doi.org/10.1016/S2213-8587(13)70062-7
10. Goyal A, Nimmakayala KR, Zonszein J. Is there a paradox in obesity? Cardiol Rev. 2014 Jul-Aug;22(4):163-70. doi: http://dx.doi.org/10.1097/CRD.0000000000000004
11. Kivimäki M, Strandberg T, Pentti J, Nyberg ST, Frank P, Jokela M, et al. Body-mass index and risk of obesity-related complex multimorbidity: an observational multicohort study. Lancet Diabetes Endocrinol. 2022 Apr;10(4):253-63. doi: http://dx.doi.org/10.1016/S2213-8587(22)00033-X
12. Whitlock G, Lewington S, Sherliker P, Clarke R, Emberson J, Halsey J, et al. Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet. 2009 Mar;373(9669):1083-96. doi: http://dx.doi.org/10.1016/S0140-6736(09)60318-4
13. Okorodudu DO, Jumean MF, Montori VM, Romero-Corral A, Somers VK, Erwin PJ, et al. Diagnostic performance of body mass index to identify obesity as defined by body adiposity: a systematic review and meta-analysis. Int J Obes (Lond). 2010 May;34(5):791-9. doi: http://dx.doi.org/10.1038/ijo.2010.5
14. Hankinson AL, Daviglus ML, Van Horn L, Chan Q, Brown I, Holmes E, et al. Diet composition and activity level of at risk and metabolically healthy obese American adults. Obesity (Silver Spring). 2013 Mar;21(3):637-43. doi: http://dx.doi.org/10.1002/oby.20257
15. Piché M-E, Poirier P, Lemieux I, Després J-P. Overview of Epidemiology and Contribution of Obesity and Body Fat Distribution to Cardiovascular Disease: An Update. Prog Cardiovasc Dis. 2018 Jul-Aug;61(2):103-113. doi: http://dx.doi.org/10.1016/j.pcad.2018.06.004
16. Wildman RP, Muntner P, Reynolds K, McGinn AP, Rajpathak S, Wylie-Rosett J, 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 Aug;168(15):1617-24. doi: http://dx.doi.org/10.1001/archinte.168.15.1617
17. Caleyachetty R, Thomas GN, Toulis KA, Mohammed N, Gokhale KM, Balachandran K, et al. Metabolically Healthy Obese and Incident Cardiovascular Disease Events Among 3.5 Million Men and Women. J Am Coll Cardiol. 2017 Sep;70(12):1429-37. doi: http://dx.doi.org/10.1016/j.jacc.2017.07.763
18. Smith GI, Mittendorfer B, Klein S. Metabolically healthy obesity: facts and fantasies. Clin Invest. 2019 Oct;129(10):3978-89. doi: http://dx.doi.org/10.1172/JCI129186
19. Rey-López JP, de Rezende LF, Pastor-Valero M, Tess BH. The prevalence of metabolically healthy obesity: a systematic review and critical evaluation of the definitions used. Obes Rev. 2014 Oct;15(10):781-90. doi: http://dx.doi.org/10.1111/obr.12198
20. Karelis AD, Rabasa-Lhoret R. Inclusion of C-reactive protein in the identification of metabolically healthy but obese (MHO) individuals. Diabetes Metab. 2008 Apr;34(2):183-4. doi: http://dx.doi.org/10.1016/j.diabet.2007.11.004
21. Lavie CJ, Laddu D, Arena R, Ortega FB, Alpert MA, Kushner RF. Healthy Weight and Obesity Prevention: JACC Health Promotion Series. J Am Coll Cardiol. 2018 Sep;72(13):1506-31. doi: http://dx.doi.org/10.1016/j.jacc.2018.08.1037
22. van Vliet-Ostaptchouk JV, Nuotio M-L, Slagter SN, Doiron D, Fischer K, Foco L, et al. The prevalence of metabolic syndrome and metabolically healthy obesity in Europe: a collaborative analysis of ten large cohort studies. BMC Endocr Disord. 2014 Feb;14:9. doi: http://dx.doi.org/10.1186/1472-6823-14-9
23. Wang B, Zhuang R, Luo X, Yin L, Pang C, Feng T, et al. Prevalence of Metabolically Healthy Obese and Metabolically Obese but Normal Weight in Adults Worldwide: A Meta-Analysis. Horm Metab Res. 2015 Oct;47(11):839-45. doi: http://dx.doi.org/10.1055/s-0035-1559767
24. Velho S, Paccaud F, Waeber G, Vollenweider P, Marques-Vidal P. Metabolically healthy obesity: different prevalences using different criteria. Eur J Clin Nutr. 2010 Oct;64(10):1043-51. doi: http://dx.doi.org/10.1038/ejcn.2010.114
25. Slagter SN, Corpeleijn E, van der Klauw MM, Sijtsma A, Swart-Busscher LG, Perenboom CWM, et al. Dietary patterns and physical activity in the metabolically (un)healthy obese: the Dutch Lifelines cohort study. Nutr J. 2018 Feb;17(1):18. doi: http://dx.doi.org/10.1186/s12937-018-0319-0
26. Lin H, Zhang L, Zheng R, Zheng Y. The prevalence, metabolic risk and effects of lifestyle intervention for metabolically healthy obesity: a systematic review and meta-analysis: A PRISMA-compliant article. Medicine (Baltimore). 2017 Nov;96(47):e8838. doi: http://dx.doi.org/10.1097/MD.0000000000008838
27. Molli AEI, Steinhardt AP, López AP, González CD, Vilariño J, Frechtel GD, et al. Metabolically healthy obese individuals present similar chronic inflammation level but less insulin-resistance than obese individuals with metabolic syndrome. PLoS One. 2017 Dec;12(12):e0190528. doi: http://dx.doi.org/10.1371/journal.pone.0190528
28. Gómez-Ambrosi J, Silva C, Galofré JC, Escalada J, Santos S, Gil MJ, Valentí V, et al. Body adiposity and type 2 diabetes: increased risk with a high body fat percentage even having a normal BMI. Obesity (Silver Spring). 2011 Jul;19(7):1439-44. doi: http://dx.doi.org/10.1038/oby.2011.36
29. Bays HE. Adiposopathy is "sick fat" a cardiovascular disease? J Am Coll Cardiol. 2011 Jun;57(25):2461-73. doi: http://dx.doi.org/10.1016/j.jacc.2011.02.038
30. Schleinitz D, Böttcher Y, Blüher M, Kovacs P. The genetics of fat distribution. Diabetologia. 2014 Jul;57(7):1276-86. doi: http://dx.doi.org/10.1007/s00125-014-3214-z
31. Shulman GI. Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease. N Engl J Med. 2014 Sep;371(12):1131-41. doi: http://dx.doi.org/10.1056/NEJMra1011035
32. Abraham TM, Pedley A, Massaro JM, Hoffmann U, Fox CS. Association between visceral and subcutaneous adipose depots and incident cardiovascular disease risk factors. Circulation. 2015 Oct;132(17):1639-47. doi: http://dx.doi.org/10.1161/CIRCULATIONAHA.114.015000
33. von Krüchten R, Lorbeer R, Müller-Peltzer K, Rospleszcz S, Storz C, Askani E, et al. Association between Adipose Tissue Depots and Dyslipidemia: The KORA-MRI Population-Based Study. Nutrients. 2022 Feb;14(4):797. doi: http://dx.doi.org/10.3390/nu14040797
34. Bondarenko VM, Pimanov SI, Makarenko EV. Ultrasound diagnosis of local fat depots in patients with arterial hypertension and coronary heart disease. Vestn VGMU. 2019;18(5):84-98. (In Russ.) doi: http://dx.doi.org/https://doi.org/10.22263/2312-4156.2019.5.84
35. Pimanov S, Bondarenko V, Makarenko E. Visceral fat in different locations assessed by ultrasound: Correlation with computed tomography and cut-off values in patients with metabolic syndrome. Clin Obes. 2020 Dec;10(6):e12404. doi: http://dx.doi.org/10.1111/cob.12404
36. McMorrow AM, Connaughton RM, Lithander FE, Roche HM. Adipose tissue dysregulation and metabolic consequences in childhood and adolescent obesity: potential impact of dietary fat quality. Proc Nutr Soc. 2015 Feb;74(1):67-82. doi: http://dx.doi.org/10.1017/S002966511400158X
37. Klöting N, Fasshauer M, Dietrich A, Kovacs P, Schön MR, Kern M, et al. Insulin-sensitive obesity. Am J Physiol Endocrinol Metab. 2010 Sep;299(3):E506-15. doi: http://dx.doi.org/10.1152/ajpendo.00586.2009
Information about authors:
V.M. Bondarenko – Candidate of Medical Sciences, associate professor of the Chair of Hospital Surgery with the course of the Faculty for Advanced Training & Retraining, Vitebsk State Order of Peoples’ Friendship Medical University,
e-mail: Этот адрес электронной почты защищён от спам-ботов. У вас должен быть включен JavaScript для просмотра. – Vladimir M. Bondarenko;
S.I. Pimanov – Doctor of Medical Sciences, professor, head of the Chair of Internal Diseases & Ultrasound Diagnostics of the Faculty for Advanced Training & Retraining, Vitebsk State Order of Peoples’ Friendship Medical University;
E.V. Makarenko – Doctor of Medical Sciences, professor of the Chair of Internal Diseases & Ultrasound Diagnostics of the Faculty for Advanced Training & Retraining, Vitebsk State Order of Peoples’ Friendship Medical University;
E.F. Bondarenko – anesthesiologist-resuscitator, Vitebsk Regional Clinical Hospital.
