542
Views
14
CrossRef citations to date
0
Altmetric
Review Article

High prevalence of cardiovascular disease in South Asians: Central role for brown adipose tissue?

, , , , , , & show all
Pages 150-157 | Received 23 Jul 2014, Accepted 09 Dec 2014, Published online: 08 May 2015

References

  • Forouhi N, Sattar N, Tillin T, et al. Do known risk factors explain the higher coronary heart disease mortality in South Asians compared with European men? Prospective follow-up of the Southall and Brent studies, UK. Diabetologia 2006;49:2580–8
  • Srinath R, Shah B, Varghese C, Ramadoss A. Responding to the threat of chronic diseases in India. Lancet 2005;366:1744–9
  • Turin TC, Shahana N, Wangchuk LZ, et al. Burden of cardio- and cerebro-vascular disease and the conventional risk factors in South Asian population. Global Health 2005;8:121–30
  • Anand SS, Yusuf S, Vuksan V, et al. Differences in risk factors, atherosclerosis and cardiovascular disease between ethnic groups in Canada: the study of health assessment and risk in ethnic groups (SHARE). Lancet 2000;356:279–84
  • Joshi P, Islam S, Pais P, et al. Risk factors for early myocardial infarction in South Asians compared with individuals in other countries. J Am Med Assoc 2007;297:286–94
  • McKeigue PM, Ferrie JE, Pierpoint T, Marmot MG. Association of early-onset coronary heart disease in South Asian men with glucose intolerance and hyperinsulinemia. Circulation 1993;87:152–61
  • McKeigue PM, Shah B, Marmot MG. Relation of central obesity and insulin resistance with high diabetes prevalence and cardiovascular risk in South Asians. Lancet 1991;337:382–6
  • Gupta R, Gupta R, Agrawal A, et al. Migrating husbands and changing cardiovascular risk factors in the wife: a cross sectional study in Asian Indian women. J Epidemiol Community Health 2012;66:881–9
  • Dodani S, Dong L. Acculturation, coronary artery disease and carotid intima media thickness in South Asian immigrants – unique population with increased risk. Ethn Dis 2011;21:314–21
  • Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 2003;23:168–75
  • Steinberg D. Atherogenesis in perspective: hypercholesterolemia and inflammation as partners in crime. Nat Med 2002;8:1211–17
  • Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006;6:508–19
  • Barter PJ, Baker PW, Rye KA. Effect of high-density lipoproteins on the expression of adhesion molecules in endothelial cells. Curr Opin Lipidol 2002;13:285–8
  • Navab M, Ananthramaiah GM, Reddy ST, et al. The double jeopardy of HDL. Ann Med 2005;37:173–8
  • von Eckardstein A, Hersberger M, Rohrer L. Current understanding of the metabolism and biological actions of HDL. Curr Opin Clin Nutr Metab Care 2005;8:147–52
  • Navab M, Hama SY, Cooke CJ, et al. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: step 1. J Lipid Res 2000;41:1481–94
  • Sugatani J, Miwa M, Komiyama Y, Ito S. High-density lipoprotein inhibits the synthesis of platelet-activating factor in human vascular endothelial cells. J Lipid Mediat Cell Signal 1996;13:73–88
  • Annema W, von Eckardstein A. High-density lipoproteins. Circ J 2013;77:2432–48
  • National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). 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) final report. Circulation 2002;106:3143–421
  • Haffner SM, Lehto S, Ronnemaa T, et al. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998;339:229–34
  • Lee CD, Folsom AR, Pankow JS, Brancati FL. Cardiovascular events in diabetic and nondiabetic adults with or without history of myocardial infarction. Circulation 2004;109:855–60
  • Malmberg K, Yusuf S, Gerstein HC, et al. Impact of diabetes on long-term prognosis in patients with unstable angina and non-Q-wave myocardial infarction: results of the OASIS (Organization to Assess Strategies for Ischemic Syndromes) Registry. Circulation 2000;102:1014–19
  • Bloomgarden ZT. Inflammation, atherosclerosis, and aspects of insulin action. Diabetes Care 2005;28:2312–19
  • Yoneshiro T, Aita S, Matsushita M, et al. Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity (Silver Spring) 2011;19:13–16
  • Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009;360:1509–17
  • van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009;360:1500–8
  • Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med 2009;360:1518–25
  • Enerback S. Human brown adipose tissue. Cell Metab 2010;11:248–52
  • Connolly E, Morrisey RD, Carnie JA. The effect of interscapular brown adipose tissue removal on body-weight and cold response in the mouse. Br J Nutr 1982;47:653–8
  • Dulloo AG, Miller DS. Energy balance following sympathetic denervation of brown adipose tissue. Can J Physiol Pharmacol 1984;62:235–40
  • Tziomalos K, Weerasinghe CN, Mikhailidis DP, Seifalian AM. Vascular risk factors in South Asians. Int J Cardiol 2008;128:5–16
  • Chambers JC, Eda S, Bassett P, et al. C-reactive protein, insulin resistance, central obesity, and coronary heart disease risk in Indian Asians from the United Kingdom compared with European whites. Circulation 2001;104:145–50
  • Razak F, Anand SS, Shannon H, et al. Defining obesity cut points in a multiethnic population. Circulation 2007;115:2111–18
  • Ajjan R, Carter AM, Somani R, et al. Ethnic differences in cardiovascular risk factors in healthy Caucasian and South Asian individuals with the metabolic syndrome. J Thromb Haemost 2007;5:754–60
  • Boon MR, Karamali NS, de Groot CJ, et al. E-selectin is elevated in cord blood of South Asian neonates compared with Caucasian neonates. J Pediatr 2012;160:844–8
  • Chandalia M, Abate N, Garg A, et al. Relationship between generalized and upper body obesity to insulin resistance in Asian Indian men. J Clin Endocrinol Metab 1999;84:2329–35
  • Ehtisham S, Crabtree N, Clark P, et al. Ethnic differences in insulin resistance and body composition in United Kingdom adolescents. J Clin Endocrinol Metab 2005;90:3963–9
  • McKeigue PM, Marmot MG, Syndercombe Court YD, et al. Diabetes, hyperinsulinaemia, and coronary risk factors in Bangladeshis in east London. Br Heart J 1988;60:390–6
  • Raji A, Gerhard-Herman MD, Warren M, et al. Insulin resistance and vascular dysfunction in nondiabetic Asian Indians. J Clin Endocrinol Metab 2004;89:3965–72
  • Assmann G, Schulte H, von Eckardstein A, Huang Y. High-density lipoprotein cholesterol as a predictor of coronary heart disease risk. The PROCAM experience and pathophysiological implications for reverse cholesterol transport. Atherosclerosis 1996;124:S11–S20
  • Barter P, Gotto AM, LaRosa JC, et al. HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events. N Engl J Med 2007;357:1301–10
  • Di Angelantonio E, Sarwar N, Perry P, et al. Major lipids, apolipoproteins, and risk of vascular disease. JAMA 2009;302:1993–2000
  • Gordon DJ, Rifkind BM. High-density lipoprotein – the clinical implications of recent studies. N Engl J Med 1989;321:1311–16
  • Sharrett AR, Ballantyne CM, Coady SA, et al. Coronary heart disease prediction from lipoprotein cholesterol levels, triglycerides, lipoprotein(a), apolipoproteins A-I and B, and HDL density subfractions: The Atherosclerosis Risk in Communities (ARIC) Study. Circulation 2001;104:1108–13
  • Wilson PW, Abbott RD, Castelli WP. High density lipoprotein cholesterol and mortality. The Framingham Heart Study. Arteriosclerosis 1988;8:737–41
  • Anand SS, Enas EA, Pogue J, et al. Elevated lipoprotein(a) levels in South Asians in North America. Metabolism 1998;47:182–4
  • Enas EA, Chacko V, Senthilkumar A, et al. Elevated lipoprotein(a) – a genetic risk factor for premature vascular disease in people with and without standard risk factors: a review. Dis Mon 2006;52:5–50
  • Enas EA, Chacko V, Pazhoor SG, et al. Dyslipidemia in South Asian patients. Curr Atheroscler Rep 2007;9:367–74
  • Dube JB, Boffa MB, Hegele RA, Koschinsky ML. Lipoprotein(a): more interesting than ever after 50 years. Curr Opin Lipidol 2012;23:133–40
  • Lear SA, Humphries KH, Kohli S, Birmingham CL. The use of BMI and waist circumference as surrogates of body fat differs by ethnicity. Obesity (Silver Spring) 2007;15:2817–24
  • Raji A, Seely EW, Arky RA, Simonson DC. Body fat distribution and insulin resistance in healthy Asian Indians and Caucasians. J Clin Endocrinol Metab 2001;86:5366–71
  • Chandalia M, Lin P, Seenivasan T, et al. Insulin resistance and body fat distribution in South Asian men compared to Caucasian men. PLoS One 2007;2:e812
  • Petersen KF, Dufour S, Feng J, et al. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Natl Acad Sci USA 2006;103:18273–7
  • Anand SS, Tarnopolsky MA, Rashid S, et al. Adipocyte hypertrophy, fatty liver and metabolic risk factors in South Asians: the Molecular Study of Health and Risk in Ethnic Groups (mol-SHARE). PLoS One 2011;6:e22112
  • Ndumele CE, Nasir K, Conceicao RD, et al. Hepatic steatosis, obesity, and the metabolic syndrome are independently and additively associated with increased systemic inflammation. Arterioscler Thromb Vasc Biol 2011;31:1927–32
  • Targher G, Bertolini L, Padovani R, et al. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 2007;30:1212–18
  • Bajaj S, Nigam P, Luthra A, et al. A case–control study on insulin resistance, metabolic co-variates & prediction score in non-alcoholic fatty liver disease. Indian J Med Res 2009;129:285–92
  • Mukhopadhyay B, Forouhi NG, Fisher BM, et al. A comparison of glycaemic and metabolic control over time among South Asian and European patients with Type 2 diabetes: results from follow-up in a routine diabetes clinic. Diabet Med 2006;23:94–8
  • Chandie Shaw PK, Vandenbroucke JP, Tjandra YI, et al. Increased end-stage diabetic nephropathy in Indo-Asian immigrants living in the Netherlands. Diabetologia 2002;45:337–41
  • Hall LM, Moran CN, Milne GR, et al. Fat oxidation, fitness and skeletal muscle expression of oxidative/lipid metabolism genes in South Asians: implications for insulin resistance? PLoS One 2010;5:e14197
  • Bakker LE, Boon MR, van der Linden RA, et al. Brown adipose tissue volume in healthy lean south Asian adults compared with white Caucasians: a prospective, case-controlled observational study. Lancet Diabetes Endocrinol 2014;2:210–17
  • Tseng YH, Kokkotou E, Schulz TJ, et al. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 2008;454:1000–4
  • Nisoli E, Clementi E, Paolucci C, et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003;299:896–9
  • Cubbon RM, Murgatroyd SR, Ferguson C, et al. Human exercise-induced circulating progenitor cell mobilization is nitric oxide-dependent and is blunted in South Asian men. Arterioscler Thromb Vasc Biol 2010;30:878–84
  • van Diepen JA, Berbee JF, Havekes LM, Rensen PC. Interactions between inflammation and lipid metabolism: relevance for efficacy of anti-inflammatory drugs in the treatment of atherosclerosis. Atherosclerosis 2013;228:306–15
  • Lau DC, Dhillon B, Yan H, et al. Adipokines: molecular links between obesity and atheroslcerosis. Am J Physiol Heart Circ Physiol 2005;288:H2031–41
  • Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003;111:1805–12
  • Madjid M, Willerson JT. Inflammatory markers in coronary heart disease. Br Med Bull 2011;100:23–38
  • Kissebah AH. Intra-abdominal fat: is it a major factor in developing diabetes and coronary artery disease? Diabetes Res Clin Pract 1996;30:25–30
  • Peters MJ, Ghouri N, McKeigue P, et al. Circulating IL-6 concentrations and associated anthropometric and metabolic parameters in South Asian men and women in comparison to European whites. Cytokine 2013;61:29–32
  • Lear SA, Chockalingam A, Kohli S, et al. Elevation in cardiovascular disease risk in South Asians is mediated by differences in visceral adipose tissue. Obesity (Silver Spring) 2012;20:1293–300
  • Nisoli E, Briscini L, Giordano A, et al. Tumor necrosis factor alpha mediates apoptosis of brown adipocytes and defective brown adipocyte function in obesity. Proc Natl Acad Sci USA 2000;97:8033–8
  • Corsetti JP, Gansevoort RT, Sparks CE, Dullaart RP. Inflammation reduces HDL protection against primary cardiac risk. Eur J Clin Invest 2010;40:483–9
  • deGoma EM, deGoma RL, Rader DJ. Beyond high-density lipoprotein cholesterol levels evaluating high-density lipoprotein function as influenced by novel therapeutic approaches. J Am Coll Cardiol 2008;51:2199–211
  • Sharma M. Combination therapy for dyslipidemia. Curr Opin Cardiol 2011;26:420–3
  • Schwartz GG, Olsson AG, Abt M, et al. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N Engl J Med 2012;367:2089–99
  • Ansell BJ, Navab M, Hama S, et al. Inflammatory/antiinflammatory properties of high-density lipoprotein distinguish patients from control subjects better than high-density lipoprotein cholesterol levels and are favorably affected by simvastatin treatment. Circulation 2003;108:2751–6
  • Navab M, Hama SY, Hough GP, et al. A cell-free assay for detecting HDL that is dysfunctional in preventing the formation of or inactivating oxidized phospholipids. J Lipid Res 2001;42:1308–17
  • Roberts CK, Ng C, Hama S, et al. Effect of a short-term diet and exercise intervention on inflammatory/anti-inflammatory properties of HDL in overweight/obese men with cardiovascular risk factors. J Appl Physiol 2006;101:1727–32
  • Van Lenten BJ, Hama SY, de Beer FC, et al. Anti-inflammatory HDL becomes pro-inflammatory during the acute phase response. Loss of protective effect of HDL against LDL oxidation in aortic wall cell cocultures. J Clin Invest 1995;96:2758–67
  • Dodani S, Kaur R, Reddy S, et al. Can dysfunctional HDL explain high coronary artery disease risk in South Asians? Int J Cardiol 2008;129:125–32
  • Celermajer DS, Sorensen KE, Gooch VM, et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992;340:1111–15
  • Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 2000;101:1899–906
  • Neunteufl T, Katzenschlager R, Hassan A, et al. Systemic endothelial dysfunction is related to the extent and severity of coronary artery disease. Atherosclerosis 1997;129:111–18
  • Jin RC, Loscalzo J. Vascular nitric oxide: formation and function. J Blood Med 2010;2010:147–62
  • Kawashima S. The two faces of endothelial nitric oxide synthase in the pathophysiology of atherosclerosis. Endothelium 2004;11:99–107
  • Cersosimo E, DeFronzo RA. Insulin resistance and endothelial dysfunction: the road map to cardiovascular diseases. Diabetes Metab Res Rev 2006;22:423–36
  • Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 2006;113:1888–904
  • Murphy C, Kanaganayagam GS, Jiang B, et al. Vascular dysfunction and reduced circulating endothelial progenitor cells in young healthy UK South Asian men. Arterioscler Thromb Vasc Biol 2007;27:936–42
  • Chambers JC, McGregor A, Jean-Marie J, Kooner JS. Abnormalities of vascular endothelial function may contribute to increased coronary heart disease risk in UK Indian Asians. Heart 1999;81:501–4
  • Nofer JR, van der Giet M, Tolle M, et al. HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J Clin Invest 2004;113:569–81
  • Aicher A, Zeiher AM, Dimmeler S. Mobilizing endothelial progenitor cells. Hypertension 2005;45:321–5
  • Griese DP, Ehsan A, Melo LG, et al. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: implications for cell-based vascular therapy. Circulation 2003;108:2710–15
  • Peichev M, Naiyer AJ, Pereira D, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000;95:952–8
  • Hill JM, Zalos G, Halcox JP, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003;348:593–600
  • Vasa M, Fichtlscherer S, Aicher A, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 2001;89:E1–E7
  • Berbée JFP, Boon MR, Khedoe PPSJ, et al. Central role for brown adipose tissue in dyslipidemia and atherosclerosis development. Nat Commun 2015, accepted
  • van der Lans AA, Hoeks J, Brans B, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 2013;123:3395–403
  • Yoneshiro T, Aita S, Matsushita M, et al. Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest 2013;123:3404–8
  • Geerling JJ, Boon MR, van der Zon GC, et al. Metformin lowers plasma triglycerides by promoting VLDL-triglyceride clearance by brown adipose tissue in mice. Diabetes 2014;63:880–91

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.