Advertisement

Lipids in South Asians: Epidemiology and Management

  • Minhal Makshood
  • Wendy S. PostEmail author
  • Alka M. Kanaya
Lipids (E. Michos, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Lipids

Abstract

Purpose of Review

This review focuses on lipoprotein abnormalities in South Asians (SA) and addresses risk stratification and management strategies to lower atherosclerotic cardiovascular disease (ASCVD) in this high-risk population.

Recent Findings

South Asians (SAs) are the fastest growing ethnic group in the United States (U.S) and have an increased risk of premature coronary artery disease (CAD). While the etiology may be multifactorial, lipoprotein abnormalities play a key role. SAs have lower low-density lipoprotein cholesterol (LDL-C) compared with Whites and at any given LDL-C level, SA ethnicity poses a higher risk of myocardial infarction (MI) and coronary artery disease (CAD) compared with other non-Asian groups. SAs have lower high-density lipoprotein cholesterol (HDL-C) with smaller particle sizes of HDL-C compared with Whites. SAs also have higher triglycerides than Whites which is strongly related to the high prevalence of metabolic syndrome in SAs. Lipoprotein a (Lp(a)) levels are also higher in SAs compared with many other ethnic groups. This unique lipoprotein profile plays a vital role in the elevated ASCVD risk in SAs. Studies evaluating dietary patterns of SAs in the U.S show high consumption of carbohydrates and saturated fats.

Summary

SAs have a high-risk lipoprotein profile compared with other ethnicities. Lipid abnormalities play a central role in the pathogenesis of CAD in SAs. More studies are needed to understand the true impact of the various lipoproteins and their contribution to increasing ASCVD in SAs. Aggressive lowering of LDL-C in high-risk groups using medications, such as statins, and lifestyle modification including dietary changes is essential in overall CAD risk reduction.

Keywords

Lipids South Asians Dyslipidemia MASALA Low-density lipoprotein High-density lipoprotein 

Abbreviations

ACC/AHA

American College of Cardiology/American Heart Association

ACCORD

Action to Control Cardiovascular Risk in Diabetes

AMI

Acute myocardial infarction

ASCVD

Atherosclerotic cardiovascular disease

CAC

Coronary artery calcium

CAD

Coronary artery disease

CCA-IMT

Carotid artery–intima media thickness

CETP

Cholesteryl ester transfer protein

CVD

Coronary vascular disease

FIELD

Fenofibrate Intervention and Event Lowering in Diabetes

FOURIER

Further Cardiovascular Outcomes Research with PCSK9 Inhibition in Subjects with Elevated Risk

HDL-C

High-density lipoprotein cholesterol

ICA-IMT

Internal carotid artery intima-media thickness

IMPROVE-IT

Improved Reduction of Outcomes: Vytorin Efficacy International Trial

LDL-C

Low-density lipoprotein cholesterol

Lp(a)

Lipoprotein a

MASALA

The Mediators of Atherosclerosis in South Asians Living in America

MESA

Multi-Ethnic Study of Atherosclerosis

MS

Metabolic syndrome

PCE

Pooled cohort equation

PCSK-9

Proprotein convertase subtilisin/kexin type 9

SAs

South Asians

VLDL-C

Very low-density lipoprotein cholesterol

Notes

Compliance with Ethical Standards

Conflict of Interest

Minhal Makshood, Wendy Post, and Alka Kanaya declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. 1.
    American Community survey. B02015 ACS Asian alone by selected groups 2017 [cited 2017].Google Scholar
  2. 2.
    Enas EA, Garg A, Davidson MA, Nair VM, Huet BA, Yusuf S. Coronary heart disease and its risk factors in first-generation immigrant Asian Indians to the United States of America. Indian Heart J. 1996;48(4):343–53.PubMedGoogle Scholar
  3. 3.
    Talegawkar SA, Jin Y, Kandula NR, Kanaya AM. Cardiovascular health metrics among south Asian adults in the United States: prevalence and associations with subclinical atherosclerosis. Prev Med. 2017;96:79–84.PubMedGoogle Scholar
  4. 4.
    Kanaya AM, Vittinghoff E, Lin F, Kandula NR, Herrington D, Liu K, et al. Incidence and progression of coronary artery calcium in south Asians compared with 4 race/ethnic groups. J Am Heart Assoc. 2019;8(2):e011053.Google Scholar
  5. 5.
    Yusuf S, Hawken S, Ôunpuu S, Dans T, Avezum A, Lanas F, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet. 2004;364(9438):937–52.Google Scholar
  6. 6.
    Joshi P, Islam S, Pais P, Reddy S, Dorairaj P, Kazmi K, et al. Risk factors for early myocardial infarction in South Asians compared with individuals in other countries. Jama. 2007;297(3):286–94.PubMedGoogle Scholar
  7. 7.
    Enas, E.A. and J. Mehta, Malignant coronary artery disease in young Asian Indians: thoughts on pathogenesis, prevention, and therapy. Coronary Artery Disease in Asian Indians (CADI) Study. Clin Cardiol, 1995. 18(3): p. 131–135.Google Scholar
  8. 8.
    Enas EA. Coronary artery disease epidemic in Indians: a cause for alarm and call for action. J Indian Med Assoc. 2000;98(11):694–5 697-702.PubMedGoogle Scholar
  9. 9.
    Ahmed ST, Rehman H, Akeroyd JM, Alam M, Shah T, Kalra A, et al. Premature coronary heart disease in South Asians: burden and determinants. Curr Atheroscler Rep. 2018;20(1):6.PubMedGoogle Scholar
  10. 10.
    Bhupathiraju SN, Guasch-Ferré M, Gadgil MD, Newgard CB, Bain JR, Muehlbauer MJ, et al. Dietary patterns among Asian Indians living in the United States have distinct metabolomic profiles that are associated with cardiometabolic risk. J Nutr. 2018;148(7):1150–9.Google Scholar
  11. 11.
    Talegawkar SA, Kandula NR, Gadgil MD, Desai D, Kanaya AM. Dietary intakes among South Asian adults differ by length of residence in the USA. Public Health Nutr. 2016;19(2):348–55.PubMedGoogle Scholar
  12. 12.
    Gadgil MD, Anderson CAM, Kandula NR, Kanaya AM. Dietary patterns are associated with metabolic risk factors in South Asians living in the United States. J Nutr. 2015;145(6):1211–7.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Shah AD, Vittinghoff E, Kandula NR, Srivastava S, Kanaya AM. Correlates of prediabetes and type II diabetes in US South Asians: findings from the Mediators of Atherosclerosis in South Asians Living in America (MASALA) study. Ann Epidemiol. 2015;25(2):77–83.PubMedGoogle Scholar
  14. 14.
    Kandula NR, Kanaya AM, Liu K, Lee JY, Herrington D, Hulley SB, et al. Association of 10-year and lifetime predicted cardiovascular disease risk with subclinical atherosclerosis in South Asians: findings from the Mediators of Atherosclerosis in South Asians Living in America (MASALA) study. J Am Heart Assoc. 2014;3(5):e001117.Google Scholar
  15. 15.
    Karthikeyan G, Teo KK, Islam S, McQueen MJ, Pais P, Wang X, et al. Lipid profile, plasma apolipoproteins, and risk of a first myocardial infarction among Asians: an analysis from the INTERHEART Study. J Am Coll Cardiol. 2009;53(3):244–53.PubMedGoogle Scholar
  16. 16.
    Kalhan R, Puthawala K, Agarwal S, Amini SB, Kalhan SC. Altered lipid profile, leptin, insulin, and anthropometry in offspring of South Asian immigrants in the United States. Metabolism. 2001;50(10):1197–202.PubMedGoogle Scholar
  17. 17.
    Anand SS, Yusuf S, Vuksan V, Devanesen S, Montague P, Kelemen L, et al. The Study of Health Assessment and Risk in Ethnic groups (SHARE): rationale and design. The SHARE Investigators. Can J Cardiol. 1998;14(11):1349–57.Google Scholar
  18. 18.
    Hastings KG, Jose PO, Kapphahn KI, Frank ATH, Goldstein BA, Thompson CA, et al. Leading causes of death among Asian American subgroups (2003-2011). PLoS One. 2015;10(4):e0124341.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Barzi F, Patel A, Woodward M, Lawes CM, Ohkubo T, Gu D, et al. A comparison of lipid variables as predictors of cardiovascular disease in the Asia Pacific region. Ann Epidemiol. 2005;15(5):405–13.Google Scholar
  20. 20.
    Thomas I, Gupta S, Sempos C, Cooper R. Serum lipids of Indian physicians living in the U.S. compared to U.S.-born physicians. Atherosclerosis. 1986;61(2):99–106.PubMedGoogle Scholar
  21. 21.
    Krishnaswami S, Prasad NK, Jose VJ. A study of lipid levels in Indian patients with coronary arterial disease. Int J Cardiol. 1989;24(3):337–45.PubMedGoogle Scholar
  22. 22.
    St-Pierre AC, Cantin B, Dagenais GR, Mauriège P, Bernard PM, Després JP, et al. Low-density lipoprotein subfractions and the long-term risk of ischemic heart disease in men: 13-year follow-up data from the Quebec Cardiovascular Study. Arterioscler Thromb Vasc Biol. 2005;25(3):553–9.PubMedGoogle Scholar
  23. 23.
    Kulkarni KR, Markovitz JH, Nanda NC, Segrest JP. Increased prevalence of smaller and denser LDL particles in Asian Indians. Arterioscler Thromb Vasc Biol. 1999;19(11):2749–55.PubMedGoogle Scholar
  24. 24.
    Palaniappan LP, Kwan AC, Abbasi F, Lamendola C, McLaughlin TL, Reaven GM. Lipoprotein abnormalities are associated with insulin resistance in South Asian Indian women. Metabolism. 2007;56(7):899–904.PubMedGoogle Scholar
  25. 25.
    Dodani S. Excess coronary artery disease risk in South Asian immigrants: can dysfunctional high-density lipoprotein explain increased risk? Vasc Health Risk Manag. 2008;4(5):953–61.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Ehtisham S, Crabtree N, Clark P, Shaw N, Barrett T. Ethnic differences in insulin resistance and body composition in United Kingdom adolescents. J Clin Endocrinol Metab. 2005;90(7):3963–9.PubMedGoogle Scholar
  27. 27.
    Bakker LEH, Boon MR, Annema W, Dikkers A, van Eyk HJ, Verhoeven A, et al. HDL functionality in South Asians as compared to white Caucasians. Nutr Metab Cardiovasc Dis. 2016;26(8):697–705.PubMedGoogle Scholar
  28. 28.
    Chow CK, McQuillan B, Raju PK, Iyengar S, Raju R, Harmer JA, et al. Greater adverse effects of cholesterol and diabetes on carotid intima-media thickness in South Asian Indians: comparison of risk factor-IMT associations in two population-based surveys. Atherosclerosis. 2008;199(1):116–22.PubMedGoogle Scholar
  29. 29.
    Dodani S, Dong L, Guirgis FW, Reddy ST. Carotid intima media thickness and low high-density lipoprotein (HDL) in South Asian immigrants: could dysfunctional HDL be the missing link? Arch Med Sci. 2014;10(5):870–9.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Bhalodkar NC, Blum S, Rana T, Bhalodkar A, Kitchappa R, Kim KS, et al. Comparison of levels of large and small high-density lipoprotein cholesterol in Asian Indian men compared with Caucasian men in the Framingham Offspring Study. Am J Cardiol. 2004;94(12):1561–3.PubMedGoogle Scholar
  31. 31.
    Forouhi NG, Sattar N, Tillin T, McKeigue PM, Chaturvedi N. Do known risk factors explain the higher coronary heart disease mortality in south Asian compared with European men? Prospective follow-up of the Southall and Brent studies, UK. Diabetologia. 2006;49(11):2580–8.PubMedGoogle Scholar
  32. 32.
    Dodani S, Henkhaus R, Wick J, Vacek J, Gupta K, Dong L, et al. Metabolic syndrome in South Asian immigrants: more than low HDL requiring aggressive management. Lipids Health Dis. 2011;10:45–5.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Superko HR, Enas EA, Kotha P, Bhat NK, Garrett B. High-density lipoprotein subclass distribution in individuals of Asian Indian descent: the National Asian Indian Heart Disease Project. Prev Cardiol. 2005;8(2):81–6.PubMedGoogle Scholar
  34. 34.
    Misra A, Khurana L. Obesity-related non-communicable diseases: South Asians vs White Caucasians. Int J Obes. 2011;35(2):167–87.Google Scholar
  35. 35.
    Ajjan R, Carter AM, Somani R, Kain K, Grant PL. Ethnic differences in cardiovascular risk factors in healthy Caucasian and South Asian individuals with the metabolic syndrome. J Thromb Haemost. 2007;5(4):754–60.PubMedGoogle Scholar
  36. 36.
    Petersen KF, Dufour S, Feng J, Befroy D, Dziura J, Man CD, et al. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Natl Acad Sci U S A. 2006;103(48):18273–7.Google Scholar
  37. 37.
    Shah AD, Kandula NR, Lin F, Allison MA, Carr J, Herrington D, et al. Less favorable body composition and adipokines in South Asians compared with other US ethnic groups: results from the MASALA and MESA studies. Int J Obes. 2016;40(4):639–45.PubMedGoogle Scholar
  38. 38.
    Frank AT, Zhao B, Jose PO, Azar KM, Fortmann SP, Palaniappan NP. Racial/ethnic differences in dyslipidemia patterns. Circulation. 2014;129(5):570–9.PubMedGoogle Scholar
  39. 39.
    Sandhofer A, Kaser S, Ritsch A, Laimer M, Engl J, Paulweber B, et al. Cholesteryl ester transfer protein in metabolic syndrome. Obesity (Silver Spring). 2006;14(5):812–8.PubMedGoogle Scholar
  40. 40.
    Rashid S, Sniderman A, Melone M, Brown PE, Otvos JD, Mente A, et al. Elevated cholesteryl ester transfer protein (CETP) activity, a major determinant of the atherogenic dyslipidemia, and atherosclerotic cardiovascular disease in South Asians. Eur J Prev Cardiol. 2015;22(4):468–77.PubMedGoogle Scholar
  41. 41.
    Clarke R, Peden JF, Hopewell JC, Kyriakou T, Goel A, Heath SC, et al. Genetic variants associated with Lp(a) lipoprotein level and coronary disease. N Engl J Med. 2009;361(26):2518–28.PubMedGoogle Scholar
  42. 42.
    Erqou S, Kaptoge S, Perry PL, Di Angelanonio E, Thompson A, White IR, et al. Lipoprotein(a) concentration and the risk of coronary heart disease, stroke, and nonvascular mortality. Jama. 2009;302(4):412–23.Google Scholar
  43. 43.
    Kamstrup PR, Typjaerg-Hansen A, Steffenson R, Nordestgaard BG. Genetically elevated lipoprotein(a) and increased risk of myocardial infarction. Jama. 2009;301(22):2331–9.PubMedGoogle Scholar
  44. 44.
    Gambhir JK, Kaur H, Gambhir DS, Prabhu KM. Lipoprotein(a) as an independent risk factor for coronary artery disease in patients below 40 years of age. Indian Heart J. 2000;52(4):411–5.PubMedGoogle Scholar
  45. 45.
    Anand SS, Enas EA, Pogue J, Haffner S, Pearson T, Yusuf S. Elevated lipoprotein(a) levels in South Asians in North America. Metabolism. 1998;47(2):182–4.PubMedGoogle Scholar
  46. 46.
    Banerjee D, Wong EC, Shin J, Fortmann SP, Palaniappan L. Racial and ethnic variation in lipoprotein (a) levels among Asian Indian and Chinese patients. J Lipids. 2011;2011:291954.Google Scholar
  47. 47.
    Palaniappan L, Anthony MN, Mahesh C, Elliott M, Killeen A, Giacherio D, et al. Cardiovascular risk factors in ethnic minority women aged < or =30 years. Am J Cardiol. 2002;89(5):524–9.Google Scholar
  48. 48.
    Velmurugan K, Deepa R, Ravikumar R, Lawrence JB, Anshoo H, Senthilvelmurugan M, et al. Relationship of lipoprotein(a) with intimal medial thickness of the carotid artery in type 2 diabetic patients in south India. Diabet Med. 2003;20(6):455–61.PubMedGoogle Scholar
  49. 49.
    Isser HS, Puri VK, Narain VS, Saran RK, Dwivedi SK, Singh S. Lipoprotein (a) and lipid levels in young patients with myocardial infarction and their first-degree relatives. Indian Heart J. 2001;53(4):463–6.PubMedGoogle Scholar
  50. 50.
    Pare G, Caku A, McQueen M, Anand SS, Enas E, Clarke R, et al. Lipoprotein(a) levels and the risk of myocardial infarction among seven ethnic groups. Circulation. 2019;139:1472–82.PubMedGoogle Scholar
  51. 51.
    Kanaya AM, Kandula N, Herrington D, Budoff MJ, Hulley S, Vittinghoff E, et al. Mediators of Atherosclerosis in South Asians Living in America (MASALA) study: objectives, methods, and cohort description. Clin Cardiol. 2013;36(12):713–20.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Olson JL, Bild DE, Kronmal RA, Burke GL. Legacy of MESA. Glob Heart. 2016;11(3):269–74.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Huffman MD, Kandula NR, Baldridge AS, Tsai MI, Prabhakaran D, Kanaya AM. Evaluating the potential association between lipoprotein(a) and atherosclerosis (from the mediators of atherosclerosis among South Asians living in America cohort). Am J Cardiol. 2018.Google Scholar
  54. 54.
    Saleheen D, Zaidi M, Rasheed A, Ahmad U, Hakeem A, Murtaza M, et al. The Pakistan Risk of Myocardial Infarction Study: a resource for the study of genetic, lifestyle and other determinants of myocardial infarction in South Asia. Eur J Epidemiol. 2009;24(6):329–38.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Jin Y, Kanaya AM, Kandula NR, Rodriguez LA, Talegawkar SA. Vegetarian diets are associated with selected cardiometabolic risk factors among middle-older aged South Asians in the United States. J Nutr. 2018;148(12):1954–60.PubMedGoogle Scholar
  56. 56.
    Wilson PWF, Polonsky TS, Miedema MD, Khera A, Kosinski AS, Kuvin JT. Systematic review for the 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA guideline on the management of blood cholesterol: a report of the American College of Cardiology/American Heart Association Task Force on clinical practice guidelines. J Am Coll Cardiol. 2018.Google Scholar
  57. 57.
    Hajra A, Li Y, Siu S, Udaltsova N, Armstrong MA, Friedman GD, et al. Risk of coronary disease in the South Asian American population. J Am Coll Cardiol. 2013;62(7):644–5.PubMedGoogle Scholar
  58. 58.
    Al Rifai M, Cainzos-Achirica M, Kanaya AM, Kandula NR, Dardardi Z, Joshi PH et al. Discordance between 10-year cardiovascular risk estimates using the ACC/AHA 2013 estimator and coronary artery calcium in individuals from 5 racial/ethnic groups: comparing MASALA and MESA. Atherosclerosis. 2018.Google Scholar
  59. 59.
    Mahmood SS, Levy D, Vasan RS, Wang TJ. The Framingham Heart Study and the epidemiology of cardiovascular disease: a historical perspective. Lancet. 2014;383(9921):999–1008.PubMedGoogle Scholar
  60. 60.
    Bansal M, Kasliwal RR, Trehan N. Comparative accuracy of different risk scores in assessing cardiovascular risk in Indians: a study in patients with first myocardial infarction. Indian Heart J. 2014;66(6):580–6.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Gadgil MD, Anderson CAM, Kandula NR, Kanaya AM. Dietary patterns in Asian Indians in the United States: an analysis of the metabolic syndrome and atherosclerosis in South Asians living in America study. J Acad Nutr Diet. 2014;114(2):238–43.PubMedGoogle Scholar
  62. 62.
    Backes AC, Abbasi F, Lamendola C, McLaughlin TL, Reaven G, Palaniappan LP. Clinical experience with a relatively low carbohydrate, calorie-restricted diet improves insulin sensitivity and associated metabolic abnormalities in overweight, insulin resistant South Asian Indian women. Asia Pac J Clin Nutr. 2008;17(4):669–71.Google Scholar
  63. 63.
    Islam NS, Zanowiak JM, Wyatt LC, Kavathe R, Singh H, Kwon SC, et al. Diabetes prevention in the New York City Sikh Asian Indian community: a pilot study. Int J Environ Res Public Health. 2014;11(5):5462–86.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Mukherjea A, Underwood KC, Stewart AL, Ivey SL, Kanaya AM. Asian Indian views on diet and health in the United States: importance of understanding cultural and social factors to address disparities. Fam Community Health. 2013;36(4):311–23.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Kanaya AM, Kandula NR, Ewing SK, Herrington D, Liu K, Blaha MJ, et al. Comparing coronary artery calcium among U.S. South Asians with four racial/ethnic groups: the MASALA and MESA studies. Atherosclerosis. 2014;234(1):102–7.Google Scholar
  66. 66.
    Chandra KS, Bansal M, Nair T, Iyenger SS, Gupta R, Manchanda SC, et al. Consensus statement on management of dyslipidemia in Indian subjects. Indian Heart J. 2014;66(Suppl 3):S1–51.Google Scholar
  67. 67.
    Gupta M, Braga MFB, Teoh H, Tsigoulis M, Verma S. Statin effects on LDL and HDL cholesterol in South Asian and white populations. J Clin Pharmacol. 2009;49(7):831–7.PubMedGoogle Scholar
  68. 68.
    Yusuf S, Bosch J, Dagenais G, Zhu J, Xavier D, Liu L, et al. Cholesterol lowering in intermediate-risk persons without cardiovascular disease. N Engl J Med. 2016;374(21):2021–31.Google Scholar
  69. 69.
    Deedwania PC, Gupta M, Stein M, Ycas J, Gold A, IRIS Study Group. Comparison of rosuvastatin versus atorvastatin in South-Asian patients at risk of coronary heart disease (from the IRIS Trial). Am J Cardiol. 2007;99(11):1538–43.PubMedGoogle Scholar
  70. 70.
    Gupta M, Martineau P, Tran T, Despres JP, Gaw A, de Teresa E, et al. Low-density lipoprotein cholesterol and high-sensitivity C-reactive protein lowering with atorvastatin in patients of South Asian compared with European origin: insights from the Achieve Cholesterol Targets Fast with Atorvastatin Stratified Titration (ACTFAST) study. J Clin Pharmacol. 2012;52(6):850–8.PubMedGoogle Scholar
  71. 71.
    Lee E, Ryan S, Birmingham B, Zalikowski J, March R, Ambrose H, et al. Rosuvastatin pharmacokinetics and pharmacogenetics in white and Asian subjects residing in the same environment. Clin Pharmacol Ther. 2005;78(4):330–41.Google Scholar
  72. 72.
    Mahadevan L, Yesudas A, Sajesh PK, Revu S, Kumar P, Santhosh D, et al. Prevalence of genetic variants associated with cardiovascular disease risk and drug response in the Southern Indian population of Kerala. Indian J Hum Genet. 2014;20(2):175–84.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Menon AS, Singh Y, Kotwal N, Girish R. Statins: cholesterol guidelines and Indian perspective. Indian J Endocr Metab. 2015;19(5):546–53.Google Scholar
  74. 74.
    Sabatine MS, Giugliano RP, Keech AC, Honarpour N, Wiviott SD, Murphy SA, et al. Evolocumab and clinical outcomes in patients with cardiovascular disease 2017. 376(18): p. 1713–1722.Google Scholar
  75. 75.
    Jia L, Betters JL, Yu L. Niemann-pick C1-like 1 (NPC1L1) protein in intestinal and hepatic cholesterol transport. Annu Rev Physiol. 2011;73:239–59.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Stitziel NO, Won HH, Morrison AC, Peloso GM, Do R, Lange LA, et al. Inactivating mutations in NPC1L1 and protection from coronary heart disease. N Engl J Med. 2014;371(22):2072–82.Google Scholar
  77. 77.
    Madan M, Vira T, Rampakakis E, Gupta A, Khithani A, Balleza L, et al. A randomized trial assessing the effectiveness of ezetimibe in South Asian Canadians with coronary artery disease or diabetes: the INFINITY study. Adv Prev Med. 2012;2012:103728.Google Scholar
  78. 78.
    Giugliano RP, Cannon CP, Blazing MA, Nicolau JC, Corbalán R, Špinar J, et al. Benefit of adding ezetimibe to statin therapy on cardiovascular outcomes and safety in patients with versus without diabetes mellitus: results from IMPROVE-IT (improved reduction of outcomes: vytorin efficacy international trial). Circulation. 2018;137(15):1571–82.PubMedGoogle Scholar
  79. 79.
    Keech A, Simes RJ, Barter P, Best J, Scott R, Taskinen MR, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet. 2005;366(9500):1849–61.Google Scholar
  80. 80.
    Ginsberg HN, Elam MB, Lovato LC, Crouse JR 3rd, Leiter LA, Linz P. Effects of combination lipid therapy in type 2 diabetes mellitus. New England Journal of Medicine, 2010. 362(17): p. 1563–1574.Google Scholar
  81. 81.
    Maki KC. The ODYSSEY Outcomes trial: clinical implications and exploration of the limits of what can be achieved through lipid lowering. J Clin Lipidol. 2018;12(5):1102–5.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Minhal Makshood
    • 1
  • Wendy S. Post
    • 2
    Email author
  • Alka M. Kanaya
    • 3
  1. 1.Johns Hopkins UniversityBaltimoreUSA
  2. 2.Johns Hopkins UniversityBaltimoreUSA
  3. 3.University of California. San FranciscoSan FranciscoUSA

Personalised recommendations