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Published in: BMC Public Health 1/2014

Open Access 01-12-2014 | Research article

Beyond BMI: The “Metabolically healthy obese” phenotype & its association with clinical/subclinical cardiovascular disease and all-cause mortality -- a systematic review

Authors: Lara L Roberson, Ehimen C Aneni, Wasim Maziak, Arthur Agatston, Theodore Feldman, Maribeth Rouseff, Thinh Tran, Michael J Blaha, Raul D Santos, Andrei Sposito, Mouaz H Al-Mallah, Ron Blankstein, Matthew J Budoff, Khurram Nasir

Published in: BMC Public Health | Issue 1/2014

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Abstract

Background

A subgroup has emerged within the obese that do not display the typical metabolic disorders associated with obesity and are hypothesized to have lower risk of complications. The purpose of this review was to analyze the literature which has examined the burden of cardiovascular disease (CVD) and all-cause mortality in the metabolically healthy obese (MHO) population.

Methods

Pubmed, Cochrane Library, and Web of Science were searched from their inception until December 2012. Studies were included which clearly defined the MHO group (using either insulin sensitivity and/or components of metabolic syndrome AND obesity) and its association with either all cause mortality, CVD mortality, incident CVD, and/or subclinical CVD.

Results

A total of 20 studies were identified; 15 cohort and 5 cross-sectional. Eight studies used the NCEP Adult Treatment Panel III definition of metabolic syndrome to define “metabolically healthy”, while another nine used insulin resistance. Seven studies assessed all-cause mortality, seven assessed CVD mortality, and nine assessed incident CVD. MHO was found to be significantly associated with all-cause mortality in two studies (30%), CVD mortality in one study (14%), and incident CVD in three studies (33%). Of the six studies which examined subclinical disease, four (67%) showed significantly higher mean common carotid artery intima media thickness (CCA-IMT), coronary artery calcium (CAC), or other subclinical CVD markers in the MHO as compared to their MHNW counterparts.

Conclusions

MHO is an important, emerging phenotype with a CVD risk between healthy, normal weight and unhealthy, obese individuals. Successful work towards a universally accepted definition of MHO would improve (and simplify) future studies and aid inter-study comparisons. Usefulness of a definition inclusive of insulin sensitivity and stricter criteria for metabolic syndrome components as well as the potential addition of markers of fatty liver and inflammation should be explored. Clinicians should be hesitant to reassure patients that the metabolically benign phenotype is safe, as increased risk cardiovascular disease and death have been shown.
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Literature
2.
go back to reference Ogden CL, Carroll MD, Kit BK, Flegal KM: Prevalence of obesity in the United States, 2009–2010. NCHS data brief. 2012, 82: 1-8.PubMed Ogden CL, Carroll MD, Kit BK, Flegal KM: Prevalence of obesity in the United States, 2009–2010. NCHS data brief. 2012, 82: 1-8.PubMed
3.
go back to reference Solomon CG, Manson JE: Obesity and mortality: a review of the epidemiologic data. Am J Clin Nutr. 1997, 66 (4 Suppl): 1044S-1050S.PubMed Solomon CG, Manson JE: Obesity and mortality: a review of the epidemiologic data. Am J Clin Nutr. 1997, 66 (4 Suppl): 1044S-1050S.PubMed
4.
go back to reference Flegal KM, Kit BK, Orpana H, Graubard BI: Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA. 2013, 309 (1): 71-82. 10.1001/jama.2012.113905.CrossRefPubMedPubMedCentral Flegal KM, Kit BK, Orpana H, Graubard BI: Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA. 2013, 309 (1): 71-82. 10.1001/jama.2012.113905.CrossRefPubMedPubMedCentral
5.
go back to reference Finkelstein EA, Trogdon JG, Cohen JW, Dietz W: Annual medical spending attributable to obesity: payer-and service-specific estimates. Health Aff (Millwood). 2009, 28 (5): w822-w831. 10.1377/hlthaff.28.5.w822.CrossRef Finkelstein EA, Trogdon JG, Cohen JW, Dietz W: Annual medical spending attributable to obesity: payer-and service-specific estimates. Health Aff (Millwood). 2009, 28 (5): w822-w831. 10.1377/hlthaff.28.5.w822.CrossRef
6.
go back to reference Bluher M: The distinction of metabolically 'healthy' from 'unhealthy' obese individuals. Curr Opin Lipidol. 2010, 21 (1): 38-43. 10.1097/MOL.0b013e3283346ccc.CrossRefPubMed Bluher M: The distinction of metabolically 'healthy' from 'unhealthy' obese individuals. Curr Opin Lipidol. 2010, 21 (1): 38-43. 10.1097/MOL.0b013e3283346ccc.CrossRefPubMed
7.
go back to reference Karelis AD: To be obese–does it matter if you are metabolically healthy?. Nat Rev Endocrinol. 2011, 7 (12): 699-700. 10.1038/nrendo.2011.181.CrossRefPubMed Karelis AD: To be obese–does it matter if you are metabolically healthy?. Nat Rev Endocrinol. 2011, 7 (12): 699-700. 10.1038/nrendo.2011.181.CrossRefPubMed
8.
go back to reference 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): 1617-1624. 10.1001/archinte.168.15.1617.CrossRefPubMed 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): 1617-1624. 10.1001/archinte.168.15.1617.CrossRefPubMed
9.
go back to reference Arnlov J, Ingelsson E, Sundstrom J, Lind L: Impact of body mass index and the metabolic syndrome on the risk of cardiovascular disease and death in middle-aged men. Circulation. 2010, 121 (2): 230-236. 10.1161/CIRCULATIONAHA.109.887521.CrossRefPubMed Arnlov J, Ingelsson E, Sundstrom J, Lind L: Impact of body mass index and the metabolic syndrome on the risk of cardiovascular disease and death in middle-aged men. Circulation. 2010, 121 (2): 230-236. 10.1161/CIRCULATIONAHA.109.887521.CrossRefPubMed
10.
go back to reference Calori G, Lattuada G, Piemonti L, Garancini MP, Ragogna F, Villa M, Mannino S, Crosignani P, Bosi E, Luzi L, et al: Prevalence, metabolic features, and prognosis of metabolically healthy obese Italian individuals: the Cremona Study. Diabetes Care. 2011, 34 (1): 210-215. 10.2337/dc10-0665.CrossRefPubMed Calori G, Lattuada G, Piemonti L, Garancini MP, Ragogna F, Villa M, Mannino S, Crosignani P, Bosi E, Luzi L, et al: Prevalence, metabolic features, and prognosis of metabolically healthy obese Italian individuals: the Cremona Study. Diabetes Care. 2011, 34 (1): 210-215. 10.2337/dc10-0665.CrossRefPubMed
11.
go back to reference Hamer M, Stamatakis E: Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality. J Clin Endocrinol Metab. 2012, 97 (7): 2482-2488. 10.1210/jc.2011-3475.CrossRefPubMedPubMedCentral Hamer M, Stamatakis E: Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality. J Clin Endocrinol Metab. 2012, 97 (7): 2482-2488. 10.1210/jc.2011-3475.CrossRefPubMedPubMedCentral
12.
go back to reference Hosseinpanah F, Barzin M, Sheikholeslami F, Azizi F: Effect of different obesity phenotypes on cardiovascular events in Tehran Lipid and Glucose Study (TLGS). Am J Cardiol. 2011, 107 (3): 412-416. 10.1016/j.amjcard.2010.09.034.CrossRefPubMed Hosseinpanah F, Barzin M, Sheikholeslami F, Azizi F: Effect of different obesity phenotypes on cardiovascular events in Tehran Lipid and Glucose Study (TLGS). Am J Cardiol. 2011, 107 (3): 412-416. 10.1016/j.amjcard.2010.09.034.CrossRefPubMed
13.
go back to reference Kuk JL, Ardern CI: Are metabolically normal but obese individuals at lower risk for all-cause mortality?. Diabetes Care. 2009, 32 (12): 2297-2299. 10.2337/dc09-0574.CrossRefPubMedPubMedCentral Kuk JL, Ardern CI: Are metabolically normal but obese individuals at lower risk for all-cause mortality?. Diabetes Care. 2009, 32 (12): 2297-2299. 10.2337/dc09-0574.CrossRefPubMedPubMedCentral
14.
go back to reference Meigs JB, Wilson PW, Fox CS, Vasan RS, Nathan DM, Sullivan LM, D'Agostino RB: Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab. 2006, 91 (8): 2906-2912. 10.1210/jc.2006-0594.CrossRefPubMed Meigs JB, Wilson PW, Fox CS, Vasan RS, Nathan DM, Sullivan LM, D'Agostino RB: Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab. 2006, 91 (8): 2906-2912. 10.1210/jc.2006-0594.CrossRefPubMed
15.
go back to reference Ogorodnikova AD, Kim M, McGinn AP, Muntner P, Khan U, Wildman RP: Incident cardiovascular disease events in metabolically benign obese individuals. Obesity (Silver Spring). 2012, 20 (3): 651-659. 10.1038/oby.2011.243.CrossRef Ogorodnikova AD, Kim M, McGinn AP, Muntner P, Khan U, Wildman RP: Incident cardiovascular disease events in metabolically benign obese individuals. Obesity (Silver Spring). 2012, 20 (3): 651-659. 10.1038/oby.2011.243.CrossRef
16.
go back to reference Ortega FB, Lee DC, Katzmarzyk PT, Ruiz JR, Sui X, Church TS, Blair SN: The intriguing metabolically healthy but obese phenotype: cardiovascular prognosis and role of fitness. Eur Heart J. 2013, 34 (5): 389-397. 10.1093/eurheartj/ehs174.CrossRefPubMed Ortega FB, Lee DC, Katzmarzyk PT, Ruiz JR, Sui X, Church TS, Blair SN: The intriguing metabolically healthy but obese phenotype: cardiovascular prognosis and role of fitness. Eur Heart J. 2013, 34 (5): 389-397. 10.1093/eurheartj/ehs174.CrossRefPubMed
17.
go back to reference St-Pierre AC, Cantin B, Mauriege P, Bergeron J, Dagenais GR, Despres JP, Lamarche B: Insulin resistance syndrome, body mass index and the risk of ischemic heart disease. CMAJ. 2005, 172 (10): 1301-1305. 10.1503/cmaj.1040834.CrossRefPubMedPubMedCentral St-Pierre AC, Cantin B, Mauriege P, Bergeron J, Dagenais GR, Despres JP, Lamarche B: Insulin resistance syndrome, body mass index and the risk of ischemic heart disease. CMAJ. 2005, 172 (10): 1301-1305. 10.1503/cmaj.1040834.CrossRefPubMedPubMedCentral
18.
go back to reference Voulgari C, Tentolouris N, Dilaveris P, Tousoulis D, Katsilambros N, Stefanadis C: Increased heart failure risk in normal-weight people with metabolic syndrome compared with metabolically healthy obese individuals. J Am Coll Cardiol. 2011, 58 (13): 1343-1350. 10.1016/j.jacc.2011.04.047.CrossRefPubMed Voulgari C, Tentolouris N, Dilaveris P, Tousoulis D, Katsilambros N, Stefanadis C: Increased heart failure risk in normal-weight people with metabolic syndrome compared with metabolically healthy obese individuals. J Am Coll Cardiol. 2011, 58 (13): 1343-1350. 10.1016/j.jacc.2011.04.047.CrossRefPubMed
19.
go back to reference Katzmarzyk PT, Church TS, Janssen I, Ross R, Blair SN: Metabolic syndrome, obesity, and mortality: impact of cardiorespiratory fitness. Diabetes Care. 2005, 28 (2): 391-397. 10.2337/diacare.28.2.391.CrossRefPubMed Katzmarzyk PT, Church TS, Janssen I, Ross R, Blair SN: Metabolic syndrome, obesity, and mortality: impact of cardiorespiratory fitness. Diabetes Care. 2005, 28 (2): 391-397. 10.2337/diacare.28.2.391.CrossRefPubMed
20.
go back to reference Daly CA, Hildebrandt P, Bertrand M, Ferrari R, Remme W, Simoons M, Fox KM: Adverse prognosis associated with the metabolic syndrome in established coronary artery disease: data from the EUROPA trial. Heart. 2007, 93 (11): 1406-1411. 10.1136/hrt.2006.113084.CrossRefPubMedPubMedCentral Daly CA, Hildebrandt P, Bertrand M, Ferrari R, Remme W, Simoons M, Fox KM: Adverse prognosis associated with the metabolic syndrome in established coronary artery disease: data from the EUROPA trial. Heart. 2007, 93 (11): 1406-1411. 10.1136/hrt.2006.113084.CrossRefPubMedPubMedCentral
21.
go back to reference Song Y, Manson JE, Meigs JB, Ridker PM, Buring JE, Liu S: Comparison of usefulness of body mass index versus metabolic risk factors in predicting 10-year risk of cardiovascular events in women. Am J Cardiol. 2007, 100 (11): 1654-1658. 10.1016/j.amjcard.2007.06.073.CrossRefPubMedPubMedCentral Song Y, Manson JE, Meigs JB, Ridker PM, Buring JE, Liu S: Comparison of usefulness of body mass index versus metabolic risk factors in predicting 10-year risk of cardiovascular events in women. Am J Cardiol. 2007, 100 (11): 1654-1658. 10.1016/j.amjcard.2007.06.073.CrossRefPubMedPubMedCentral
22.
go back to reference Bo S, Musso G, Gambino R, Villois P, Gentile L, Durazzo M, Cavallo-Perin P, Cassader M: 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): 962-969. 10.3945/ajcn.112.040006.CrossRefPubMed Bo S, Musso G, Gambino R, Villois P, Gentile L, Durazzo M, Cavallo-Perin P, Cassader M: 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): 962-969. 10.3945/ajcn.112.040006.CrossRefPubMed
23.
go back to reference Bobbioni-Harsch E, Pataky Z, Makoundou V, Laville M, Disse E, Anderwald C, Konrad T, Golay A: From metabolic normality to cardiometabolic risk factors in subjects with obesity. Obesity (Silver Spring). 2012, 20 (10): 2063-2069. 10.1038/oby.2012.69.CrossRef Bobbioni-Harsch E, Pataky Z, Makoundou V, Laville M, Disse E, Anderwald C, Konrad T, Golay A: From metabolic normality to cardiometabolic risk factors in subjects with obesity. Obesity (Silver Spring). 2012, 20 (10): 2063-2069. 10.1038/oby.2012.69.CrossRef
24.
go back to reference Alam I, Ng TP, Larbi A: Does inflammation determine whether obesity is metabolically healthy or unhealthy?. Aging Perspect Mediat Inflamm. 2012, 2012: 14- Alam I, Ng TP, Larbi A: Does inflammation determine whether obesity is metabolically healthy or unhealthy?. Aging Perspect Mediat Inflamm. 2012, 2012: 14-
25.
go back to reference Marini MA, Succurro E, Frontoni S, Hribal ML, Andreozzi F, Lauro R, Perticone F, Sesti G: Metabolically healthy but obese women have an intermediate cardiovascular risk profile between healthy nonobese women and obese insulin-resistant women. Diabetes Care. 2007, 30 (8): 2145-2147. 10.2337/dc07-0419.CrossRefPubMed Marini MA, Succurro E, Frontoni S, Hribal ML, Andreozzi F, Lauro R, Perticone F, Sesti G: Metabolically healthy but obese women have an intermediate cardiovascular risk profile between healthy nonobese women and obese insulin-resistant women. Diabetes Care. 2007, 30 (8): 2145-2147. 10.2337/dc07-0419.CrossRefPubMed
26.
go back to reference Stefan N, Kantartzis K, Machann J, Schick F, Thamer C, Rittig K, Balletshofer B, Machicao F, Fritsche A, Haring HU: Identification and characterization of metabolically benign obesity in humans. Arch Intern Med. 2008, 168 (15): 1609-1616. 10.1001/archinte.168.15.1609.CrossRefPubMed Stefan N, Kantartzis K, Machann J, Schick F, Thamer C, Rittig K, Balletshofer B, Machicao F, Fritsche A, Haring HU: Identification and characterization of metabolically benign obesity in humans. Arch Intern Med. 2008, 168 (15): 1609-1616. 10.1001/archinte.168.15.1609.CrossRefPubMed
27.
go back to reference Khan UI, Wang D, Thurston RC, Sowers M, Sutton-Tyrrell K, Matthews KA, Barinas-Mitchell E, Wildman RP: Burden of subclinical cardiovascular disease in "metabolically benign" and "at-risk" overweight and obese women: the Study of Women's Health Across the Nation (SWAN). Atherosclerosis. 2011, 217 (1): 179-186. 10.1016/j.atherosclerosis.2011.01.007.CrossRefPubMedPubMedCentral Khan UI, Wang D, Thurston RC, Sowers M, Sutton-Tyrrell K, Matthews KA, Barinas-Mitchell E, Wildman RP: Burden of subclinical cardiovascular disease in "metabolically benign" and "at-risk" overweight and obese women: the Study of Women's Health Across the Nation (SWAN). Atherosclerosis. 2011, 217 (1): 179-186. 10.1016/j.atherosclerosis.2011.01.007.CrossRefPubMedPubMedCentral
28.
go back to reference Park J, Kim SH, Cho GY, Baik I, Kim NH, Lim HE, Kim EJ, Park CG, Lim SY, Kim YH, et al: Obesity phenotype and cardiovascular changes. J Hypertens. 2011, 29 (9): 1765-1772. 10.1097/HJH.0b013e32834a50f3.CrossRefPubMed Park J, Kim SH, Cho GY, Baik I, Kim NH, Lim HE, Kim EJ, Park CG, Lim SY, Kim YH, et al: Obesity phenotype and cardiovascular changes. J Hypertens. 2011, 29 (9): 1765-1772. 10.1097/HJH.0b013e32834a50f3.CrossRefPubMed
29.
go back to reference Irace C, Scavelli F, Carallo C, Serra R, Cortese C, Gnasso A: Body mass index, metabolic syndrome and carotid atherosclerosis. Coron Artery Dis. 2009, 20 (2): 94-99. 10.1097/MCA.0b013e3283219e76.CrossRefPubMed Irace C, Scavelli F, Carallo C, Serra R, Cortese C, Gnasso A: Body mass index, metabolic syndrome and carotid atherosclerosis. Coron Artery Dis. 2009, 20 (2): 94-99. 10.1097/MCA.0b013e3283219e76.CrossRefPubMed
30.
go back to reference Sims EA: Are there persons who are obese, but metabolically healthy?. Metabolism. 2001, 50 (12): 1499-1504. 10.1053/meta.2001.27213.CrossRefPubMed Sims EA: Are there persons who are obese, but metabolically healthy?. Metabolism. 2001, 50 (12): 1499-1504. 10.1053/meta.2001.27213.CrossRefPubMed
31.
go back to reference Lebovitz HE, Banerji MA: Point: visceral adiposity is causally related to insulin resistance. Diabetes Care. 2005, 28 (9): 2322-2325. 10.2337/diacare.28.9.2322.CrossRefPubMed Lebovitz HE, Banerji MA: Point: visceral adiposity is causally related to insulin resistance. Diabetes Care. 2005, 28 (9): 2322-2325. 10.2337/diacare.28.9.2322.CrossRefPubMed
33.
go back to reference Muniyappa R, Lee S, Chen H, Quon MJ: Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am J Physiol Endocrinol Metab. 2008, 294 (1): E15-E26.CrossRefPubMed Muniyappa R, Lee S, Chen H, Quon MJ: Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am J Physiol Endocrinol Metab. 2008, 294 (1): E15-E26.CrossRefPubMed
34.
go back to reference Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J, Feve B: Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw. 2006, 17 (1): 4-12.PubMed Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J, Feve B: Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw. 2006, 17 (1): 4-12.PubMed
35.
go back to reference Nordestgaard BG, Zacho J: Lipids, atherosclerosis and CVD risk: is CRP an innocent bystander?. Nutr Metab Cardiovasc Dis. 2009, 19 (8): 521-524. 10.1016/j.numecd.2009.07.005.CrossRefPubMed Nordestgaard BG, Zacho J: Lipids, atherosclerosis and CVD risk: is CRP an innocent bystander?. Nutr Metab Cardiovasc Dis. 2009, 19 (8): 521-524. 10.1016/j.numecd.2009.07.005.CrossRefPubMed
36.
go back to reference Moore JB: Non-alcoholic fatty liver disease: the hepatic consequence of obesity and the metabolic syndrome. Proc Nutr Soc. 2010, 69 (2): 211-220. 10.1017/S0029665110000030.CrossRefPubMed Moore JB: Non-alcoholic fatty liver disease: the hepatic consequence of obesity and the metabolic syndrome. Proc Nutr Soc. 2010, 69 (2): 211-220. 10.1017/S0029665110000030.CrossRefPubMed
37.
go back to reference Targher G, Day CP, Bonora E: Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010, 363 (14): 1341-1350. 10.1056/NEJMra0912063.CrossRefPubMed Targher G, Day CP, Bonora E: Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010, 363 (14): 1341-1350. 10.1056/NEJMra0912063.CrossRefPubMed
38.
go back to reference Messier V, Karelis AD, Robillard ME, Bellefeuille P, Brochu M, Lavoie JM, Rabasa-Lhoret R: Metabolically healthy but obese individuals: relationship with hepatic enzymes. Metabolism. 2010, 59 (1): 20-24. 10.1016/j.metabol.2009.06.020.CrossRefPubMed Messier V, Karelis AD, Robillard ME, Bellefeuille P, Brochu M, Lavoie JM, Rabasa-Lhoret R: Metabolically healthy but obese individuals: relationship with hepatic enzymes. Metabolism. 2010, 59 (1): 20-24. 10.1016/j.metabol.2009.06.020.CrossRefPubMed
39.
go back to reference Soverini V, Moscatiello S, Villanova N, Ragni E, Di Domizio S, Marchesini G: Metabolic syndrome and insulin resistance in subjects with morbid obesity. Obes Surg. 2010, 20 (3): 295-301. 10.1007/s11695-009-9999-z.CrossRefPubMed Soverini V, Moscatiello S, Villanova N, Ragni E, Di Domizio S, Marchesini G: Metabolic syndrome and insulin resistance in subjects with morbid obesity. Obes Surg. 2010, 20 (3): 295-301. 10.1007/s11695-009-9999-z.CrossRefPubMed
40.
go back to reference Romero CX, Romero TE, Shlay JC, Ogden LG, Dabelea D: Changing trends in the prevalence and disparities of obesity and other cardiovascular disease risk factors in three racial/ethnic groups of USA adults. Adv Prev Med. 2012, 2012: 172423-CrossRefPubMedPubMedCentral Romero CX, Romero TE, Shlay JC, Ogden LG, Dabelea D: Changing trends in the prevalence and disparities of obesity and other cardiovascular disease risk factors in three racial/ethnic groups of USA adults. Adv Prev Med. 2012, 2012: 172423-CrossRefPubMedPubMedCentral
41.
go back to reference Mensah GA, Mokdad AH, Ford ES, Greenlund KJ, Croft JB: State of disparities in cardiovascular health in the United States. Circulation. 2005, 111 (10): 1233-1241. 10.1161/01.CIR.0000158136.76824.04.CrossRefPubMed Mensah GA, Mokdad AH, Ford ES, Greenlund KJ, Croft JB: State of disparities in cardiovascular health in the United States. Circulation. 2005, 111 (10): 1233-1241. 10.1161/01.CIR.0000158136.76824.04.CrossRefPubMed
42.
go back to reference Hankinson AL, Daviglus ML, Van Horn L, Chan Q, Brown I, Holmes E, Elliott P, Stamler J: Diet composition and activity level of at risk and metabolically healthy obese American adults. Obesity (Silver Spring). 2012, 21 (3): 637-643.CrossRef Hankinson AL, Daviglus ML, Van Horn L, Chan Q, Brown I, Holmes E, Elliott P, Stamler J: Diet composition and activity level of at risk and metabolically healthy obese American adults. Obesity (Silver Spring). 2012, 21 (3): 637-643.CrossRef
43.
go back to reference Gill JM, Malkova D: Physical activity, fitness and cardiovascular disease risk in adults: interactions with insulin resistance and obesity. Clin Sci (Lond). 2006, 110 (4): 409-425. 10.1042/CS20050207.CrossRef Gill JM, Malkova D: Physical activity, fitness and cardiovascular disease risk in adults: interactions with insulin resistance and obesity. Clin Sci (Lond). 2006, 110 (4): 409-425. 10.1042/CS20050207.CrossRef
44.
go back to reference Wilmot EG, Edwardson CL, Achana FA, Davies MJ, Gorely T, Gray LJ, Khunti K, Yates T, Biddle SJ: Sedentary time in adults and the association with diabetes, cardiovascular disease and death: systematic review and meta-analysis. Diabetologia. 2012, 55 (11): 2895-2905. 10.1007/s00125-012-2677-z.CrossRefPubMed Wilmot EG, Edwardson CL, Achana FA, Davies MJ, Gorely T, Gray LJ, Khunti K, Yates T, Biddle SJ: Sedentary time in adults and the association with diabetes, cardiovascular disease and death: systematic review and meta-analysis. Diabetologia. 2012, 55 (11): 2895-2905. 10.1007/s00125-012-2677-z.CrossRefPubMed
45.
go back to reference Nesto RW: Obesity: a major component of the metabolic syndrome. Texas Heart Institute journal / from the Texas Heart Institute of St Luke's Episcopal Hospital, Texas Children's Hospital. 2005, 32 (3): 387-389. Nesto RW: Obesity: a major component of the metabolic syndrome. Texas Heart Institute journal / from the Texas Heart Institute of St Luke's Episcopal Hospital, Texas Children's Hospital. 2005, 32 (3): 387-389.
46.
go back to reference Wang F, Deeney JT, Denis GV: Brd2 Gene disruption causes "metabolically healthy" obesity: epigenetic and chromatin-based mechanisms that uncouple obesity from type 2 diabetes. Vitam Horm. 2013, 91: 49-75.CrossRefPubMedPubMedCentral Wang F, Deeney JT, Denis GV: Brd2 Gene disruption causes "metabolically healthy" obesity: epigenetic and chromatin-based mechanisms that uncouple obesity from type 2 diabetes. Vitam Horm. 2013, 91: 49-75.CrossRefPubMedPubMedCentral
47.
go back to reference Speakman JR: Obesity: the integrated roles of environment and genetics. J Nutr. 2004, 134 (8 Suppl): 2090S-2105S.PubMed Speakman JR: Obesity: the integrated roles of environment and genetics. J Nutr. 2004, 134 (8 Suppl): 2090S-2105S.PubMed
Metadata
Title
Beyond BMI: The “Metabolically healthy obese” phenotype & its association with clinical/subclinical cardiovascular disease and all-cause mortality -- a systematic review
Authors
Lara L Roberson
Ehimen C Aneni
Wasim Maziak
Arthur Agatston
Theodore Feldman
Maribeth Rouseff
Thinh Tran
Michael J Blaha
Raul D Santos
Andrei Sposito
Mouaz H Al-Mallah
Ron Blankstein
Matthew J Budoff
Khurram Nasir
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2014
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/1471-2458-14-14

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