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HIV and Cardiovascular Disease: Update on Clinical Events, Special Populations, and Novel Biomarkers

  • Complications of Antiretroviral Therapy (GA McComsey, Section Editor)
  • Published:
Current HIV/AIDS Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The objective of this review is to provide an update on the link between HIV infection and cardiovascular disease (CVD). We will focus our review mainly on literature describing clinical CVD events and understudied topics of importance.

Recent Findings

Heart failure, peripheral artery disease, and stroke are CVD modalities deserving more attention in the context of HIV infection in the highly active antiretroviral therapy era. Incidence data on clinical CVD from HIV populations in low- and middle-income countries are limited. Multisubstance use is common in HIV, but understudied as a moderator or mediator of the association between HIV and CVD. CVD risk assessment in HIV remains challenging, but new research into novel biomarkers may provide further insights. There is also a need for inclusion of non-biologic factors in our attempts to understand, quantify, and predict CVD risk among PLWHA.

Summary

Significant attention has been paid to generating and testing hypotheses to understand the mechanisms of myocardial infarction in HIV. Similar attention is deserving for heart failure, PAD, stroke, and cardiovascular disease risk in resource-limited settings and among substance users with HIV.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Stein JH, Currier JS, Hsue PY. Arterial disease in patients with human immunodeficiency virus infection: what has imaging taught us? JACC Cardiovasc Imaging. 2014;7(5):515–25.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sun D, Wu Y, Yuan Y, Wang Y, Liu W, Yang J. Is the atherosclerotic process accentuated under conditions of HIV infection, antiretroviral therapy, and protease inhibitor exposure? Meta-analysis of the markers of arterial structure and function. Atherosclerosis. 2015;242(1):109–16.

    Article  PubMed  CAS  Google Scholar 

  3. Kearns A, Gordon J, Burdo TH, Qin X. HIV-1-associated atherosclerosis: Unraveling the Missing Link. J Am Coll Cardiol. 2017;69(25):3084–98.

    Article  PubMed  PubMed Central  Google Scholar 

  4. D’Ascenzo F, Cerrato E, Calcagno A, Grossomarra W, Ballocca F, Omede P, et al. High prevalence at computed coronary tomography of non-calcified plaques in asymptomatic HIV patients treated with HAART: a meta-analysis. Atherosclerosis. 2015;240(1):197–204.

    Article  PubMed  CAS  Google Scholar 

  5. Dorjee K, Baxi SM, Reingold AL, Hubbard A. Risk of cardiovascular events from current, recent, and cumulative exposure to abacavir among persons living with HIV who were receiving antiretroviral therapy in the United States: a cohort study. BMC Infect Dis. 2017;17(1):708.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sabin CA, Reiss P, Ryom L, Phillips AN, Weber R, Law M, et al. Is there continued evidence for an association between abacavir usage and myocardial infarction risk in individuals with HIV? A cohort collaboration. BMC Med. 2016;14:61.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Pugliese A, Isnardi D, Saini A, Scarabelli T, Raddino R, Torre D. Impact of highly active antiretroviral therapy in HIV-positive patients with cardiac involvement. J Inf Secur. 2000;40(3):282–4.

    CAS  Google Scholar 

  8. Lumsden RH, Bloomfield GS. The causes of HIV-associated cardiomyopathy: a tale of two worlds. Biomed Res Int 2016; 2016:8196560, 1, 9.

  9. • Freiberg MS, Chang CH, Skanderson M, Patterson OV, DuVall SL, Brandt CA, et al. Association between HIV infection and the risk of heart failure with reduced ejection fraction and preserved ejection fraction in the antiretroviral therapy era: results from the veterans aging cohort study. JAMA Cardiol. 2017;2(5):536–46. Documents independent association of HIV infection with incident heart failure (including type heart failure) in the combination ART era using a behaviorally and demographically similar comparator group of uninfected people.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Al-Kindi SG, ElAmm C, Ginwalla M, Mehanna E, Zacharias M, Benatti R, et al. Heart failure in patients with human immunodeficiency virus infection: epidemiology and management disparities. Int J Cardiol. 2016;218:43–6.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Steverson AB, Pawlowski AE, Schneider D, Nannapaneni P, Sanders JM, Achenbach CJ, et al. Clinical characteristics of HIV-infected patients with adjudicated heart failure. Eur J Prev Cardiol. 2017;24(16):1746–58.

    Article  PubMed  PubMed Central  Google Scholar 

  12. So-Armah KA, Lim JK, Lo Re V, Tate JP, Chung-Chou HC, Butt AA, et al. FIB-4 stage of liver fibrosis predicts incident heart failure among HIV infected and uninfected patients. Hepatology. 2017;66:1286–95.

    Article  PubMed  CAS  Google Scholar 

  13. White JR, Chang CC, So-Armah KA, Stewart JC, Gupta SK, Butt AA, et al. Depression and human immunodeficiency virus infection are risk factors for incident heart failure among veterans: veterans aging cohort study. Circulation. 2015;132(17):1630–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Schwarze-Zander C, Pabst S, Hammerstingl C, Ohlig J, Wasmuth JC, Boesecke C, et al. Pulmonary hypertension in HIV infection: a prospective echocardiographic study. HIV Med. 2015;16(9):578–82.

    Article  PubMed  CAS  Google Scholar 

  15. Brittain EL, Duncan MS, Chang J, Patterson OV, DuVall SL, Brandt CA, et al. Increased echocardiographic pulmonary pressure in HIV-infected and uninfected individuals in the veterans aging cohort study. Am J Respir Crit Care Med. 2017

  16. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med. 2006;355(3):251–9.

    Article  PubMed  CAS  Google Scholar 

  17. Lourenco AP, Leite-Moreira AF, Balligand JL, Bauersachs J, Dawson D, de Boer RA, et al. An integrative translational approach to study heart failure with preserved ejection fraction: a position paper from the Working Group on Myocardial Function of the European Society of Cardiology. Eur J Heart Fail. 2017;

  18. Pitt B, Pfeffer MA, Assmann SF, Boineau R, Anand IS, Claggett B, et al. Spironolactone for heart failure with preserved ejection fraction. N Engl J Med. 2014;370(15):1383–92.

    Article  PubMed  CAS  Google Scholar 

  19. Edelman EJ, Gordon KS, Glover J, McNicholl IR, Fiellin DA, Justice AC. The next therapeutic challenge in HIV: polypharmacy. Drugs Aging. 2013;30(8):613–28.

    Article  PubMed  PubMed Central  Google Scholar 

  20. High KP, Brennan-Ing M, Clifford DB, Cohen MH, Currier J, Deeks SG, et al. HIV and aging: state of knowledge and areas of critical need for research. A report to the NIH Office of AIDS Research by the HIV and Aging Working Group. J Acquir Immune Defic Syndr. 2012;60(Suppl 1):S1–18.

    Article  PubMed  CAS  Google Scholar 

  21. Smilowitz NR, Gupta N, Guo Y, Coppola JT, Bangalore S. Influence of human immunodeficiency virus seropositive status on the in-hospital management and outcomes of patients presenting with acute myocardial infarction. J Invasive Cardiol. 2016;28(10):403–9.

    PubMed  Google Scholar 

  22. Singh V, Mendirichaga R, Savani GT, Rodriguez AP, Dabas N, Munagala A, et al. Coronary revascularization for acute myocardial infarction in the HIV population. J Interv Cardiol. 2017;30(5):405–14.

    Article  PubMed  Google Scholar 

  23. Uriel N, Nahumi N, Colombo PC, Yuzefpolskaya M, Restaino SW, Han J, et al. Advanced heart failure in patients infected with human immunodeficiency virus: is there equal access to care? J Heart Lung Transplant. 2014;33(9):924–30.

    Article  PubMed  Google Scholar 

  24. Fowkes FG, Rudan D, Rudan I, Aboyans V, Denenberg JO, McDermott MM, et al. Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis. Lancet. 2013;382(9901):1329–40.

    Article  PubMed  Google Scholar 

  25. McDermott MM. Lower extremity manifestations of peripheral artery disease: the pathophysiologic and functional implications of leg ischemia. Circ Res. 2015;116(9):1540–50.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Criqui MH, Aboyans V. Epidemiology of peripheral artery disease. Circ Res. 2015;116(9):1509–26.

    Article  PubMed  CAS  Google Scholar 

  27. Knudsen A, Malmberg CA, Kjaer A, Lebech AM. Low prevalence of peripheral arterial disease in a cross-sectional study of Danish HIV-infected patients. Infect Dis (Lond). 2015;47(11):776–82.

    Article  Google Scholar 

  28. Qaqa AY, DeBari VA, Isbitan A, Mohammad N, Sison R, Slim J, et al. The role of postexercise measurements in the diagnosis of peripheral arterial disease in HIV-infected patients. Angiology. 2011;62(1):10–4.

    Article  PubMed  Google Scholar 

  29. Sharma A, Holman S, Pitts R, Minkoff HL, Dehovitz JA, Lazar J. Peripheral arterial disease in HIV-infected and uninfected women. HIV Med. 2007;8(8):555–60.

    Article  PubMed  CAS  Google Scholar 

  30. Qaqa AY, Debari VA, El-Kersh K, Sison R, Isbitan A, Mohammad N, et al. Epidemiologic aspects of abnormal ankle brachial index in the HIV infected population. Int Angiol. 2012;31(3):227–33.

    PubMed  CAS  Google Scholar 

  31. Johns K, Saeedi R, Mancini GB, Bondy G. Ankle brachial index screening for occult vascular disease is not useful in HIV-positive patients. AIDS Res Hum Retrovir. 2010;26(9):955–9.

    Article  PubMed  Google Scholar 

  32. Bernal E, Masia M, Padilla S, Hernandez I, Gutierrez F. Low prevalence of peripheral arterial disease in HIV-infected patients with multiple cardiovascular risk factors. J Acquir Immune Defic Syndr. 2008;47(1):126–7.

    Article  PubMed  Google Scholar 

  33. Olalla J, Salas D, Del Arco A, De la Torre J, Prada J, Machin-Hamalainen S, et al. Ankle-branch index and HIV: the role of antiretrovirals. HIV Med. 2009;10(1):1–5.

    Article  PubMed  CAS  Google Scholar 

  34. Kwiatkowska W, Knysz B, Arczynska K, Drelichowska J, Czarnecki M, Gasiorowski J, et al. Peripheral arterial disease and ankle-brachial index abnormalites in young and middle-aged HIV-positive patients in lower Silesia, Poland. PLoS One. 2014;9(12):e113857.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Periard D, Cavassini M, Taffe P, Chevalley M, Senn L, Chapuis-Taillard C, et al. High prevalence of peripheral arterial disease in HIV-infected persons. Clin Infect Dis. 2008;46(5):761–7.

    Article  PubMed  Google Scholar 

  36. Gutierrez F, Bernal E, Masia M. Considerations on ankle-brachial index interpretation in HIV-1 infected patients. HIV Med 2009; 10(6):395; author reply 395-396.

  37. Palacios R, Alonso I, Hidalgo A, Aguilar I, Sanchez MA, Valdivielso P, et al. Peripheral arterial disease in HIV patients older than 50 years of age. AIDS Res Hum Retrovir. 2008;24(8):1043–6.

    Article  PubMed  Google Scholar 

  38. Ye Y, Zeng Y, Li X, Zhang S, Fang Q, Luo L, et al. HIV infection: an independent risk factor of peripheral arterial disease. J Acquir Immune Defic Syndr. 2010;53(2):276–8.

    Article  PubMed  Google Scholar 

  39. Bali V, Yermilov I, Coutts K, Legorreta AP. Novel screening metric for the identification of at-risk peripheral artery disease patients using administrative claims data. Vasc Med. 2016;21(1):33–40.

    Article  PubMed  CAS  Google Scholar 

  40. • Gutierrez J, Albuquerque ALA, Falzon L. HIV infection as vascular risk: a systematic review of the literature and meta-analysis. PLoS One. 2017;12(5):e0176686. Provides recent global estimates of rates/risk for multiple CVD etiologies from larger longitudinal studies.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Yen YF, Chen M, Jen I, Lan YC, Chuang PH, Liu YL, et al. Association of HIV and opportunistic infections with incident stroke: a nationwide population-based cohort study in Taiwan. J Acquir Immune Defic Syndr. 2017;74(2):117–25.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Sico JJ, Chang CC, So-Armah K, Justice AC, Hylek E, Skanderson M, et al. HIV status and the risk of ischemic stroke among men. Neurology. 2015;84(19):1933–40.

    Article  PubMed  PubMed Central  Google Scholar 

  43. • Marcus JL, Leyden WA, Chao CR, Chow FC, Horberg MA, Hurley LB, et al. HIV infection and incidence of ischemic stroke. AIDS. 2014;28(13):1911–9. Provides important data on secular trends in stroke incidence rates showing differences differ by HIV status and age group.

    Article  PubMed  CAS  Google Scholar 

  44. Okeke NL, Hicks CB, McKellar MS, Fowler VG Jr, Federspiel JJ. History of AIDS in HIV-infected patients is associated with higher in-hospital mortality following admission for acute myocardial infarction and stroke. J Infect Dis. 2016;213(12):1955–61.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Chow FC, Bacchetti P, Kim AS, Price RW, Hsue PY. Effect of CD4+ cell count and viral suppression on risk of ischemic stroke in HIV infection. AIDS. 2014;28(17):2573–7.

    Article  PubMed  Google Scholar 

  46. Chow FC, Price RW, Hsue PY, Kim AS. Greater risk of stroke of undetermined etiology in a contemporary HIV-infected cohort compared with uninfected individuals. J Stroke Cerebrovasc Dis: Off J Natl Stroke Assoc. 2017;26(5):1154–60.

    Article  Google Scholar 

  47. Benjamin LA, Allain TJ, Mzinganjira H, Connor MD, Smith C, Lucas S, et al. The role of human immunodeficiency virus-associated vasculopathy in the etiology of stroke. J Infect Dis. 2017;216(5):545–53.

    Article  PubMed  PubMed Central  Google Scholar 

  48. • Bertrand L, Dygert L, Toborek M. Antiretroviral treatment with Efavirenz disrupts the blood-brain barrier integrity and increases stroke severity. Sci Rep. 2016;6:39738. Pre-clinical study that can and should complement existing exiting work on effects of HIV infection on gastrointestinal barrier function.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12(12):1365–71.

    Article  PubMed  CAS  Google Scholar 

  50. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105(9):1135–43.

    Article  PubMed  CAS  Google Scholar 

  51. • Klein DB, Leyden WA, Xu L, Chao CR, Horberg MA, Towner WJ, et al. Declining relative risk for myocardial infarction among HIV-positive compared with HIV-negative individuals with access to care. Clin Infect Dis. 2015;60(8):1278–80. Provides important data on secular trends in myocardial infarction incidence rates showing differences differ by HIV status.

    Article  PubMed  Google Scholar 

  52. • Althoff KN, McGinnis KA, Wyatt CM, Freiberg MS, Gilbert C, Oursler KK, et al. Comparison of risk and age at diagnosis of myocardial infarction, end-stage renal disease, and non-AIDS-defining cancer in HIV-infected versus uninfected adults. Clin Infect Dis. 2015;60(4):627–38. Provides data to test a frequently repeated theory that HIV accelerates aging and thus diseases common with aging like myocardial infarction.

    Article  PubMed  Google Scholar 

  53. • Crane HM, Paramsothy P, Drozd DR, Nance RM, Delaney JA, Heckbert SR, et al. Types of myocardial infarction among human immunodeficiency virus-infected individuals in the United States. JAMA Cardiol. 2017;2(3):260–7. Provides increased specificity for describing the association between HIV status and myocardial infarction by differentiating types of myocardial infaraction.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Drozd DR, Kitahata MM, Althoff KN, Zhang J, Gange SJ, Napravnik S, et al. Increased risk of myocardial infarction in HIV-infected individuals in North America compared with the general population. J Acquir Immune Defic Syndr. 2017;75(5):568–76.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  55. Rasmussen LD, Helleberg M, May MT, Afzal S, Kronborg G, Larsen CS, et al. Myocardial infarction among Danish HIV-infected individuals: population-attributable fractions associated with smoking. Clin Infect Dis. 2015;60(9):1415–23.

    PubMed  Google Scholar 

  56. Freiberg MS, Chang CC, Kuller LH, Skanderson M, Lowy E, Kraemer KL, et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern Med. 2013;173(8):614–22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. • Paisible AL, Chang CC, So-Armah KA, Butt AA, Leaf DA, Budoff M, et al. HIV infection, cardiovascular disease risk factor profile, and risk for acute myocardial infarction. J Acquir Immune Defic Syndr. 2015;68(2):209–16. Provides data enabling comparison of contribution of HIV status versus traditional cardiovascular disease risk factors to absolute cardiovascular disease risk while also demonstrating that even with control of cardiovascular disease risk factors, relative risk of myocardial infarction remains elevated in PLWHA compared to uninfected people.

    Article  PubMed  Google Scholar 

  58. Echeverria P, Domingo P, Llibre JM, Gutierrez M, Mateo G, Puig J, et al. Prevalence of ischemic heart disease and management of coronary risk in daily clinical practice: results from a Mediterranean cohort of HIV-infected patients. Biomed Res Int. 2014;2014:823058.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Hatleberg CI, Ryom L, El-Sadr W, Smith C, Weber R, Reiss P, et al. Improvements over time in short-term mortality following myocardial infarction in HIV-positive individuals. AIDS. 2016;30(10):1583–96.

    Article  PubMed  CAS  Google Scholar 

  60. D’Ascenzo F, Cerrato E, Appleton D, Moretti C, Calcagno A, Abouzaki N, et al. Prognostic indicators for recurrent thrombotic events in HIV-infected patients with acute coronary syndromes: use of registry data from 12 sites in Europe, South Africa and the United States. Thromb Res. 2014;134(3):558–64.

    Article  PubMed  CAS  Google Scholar 

  61. Carballo D, Delhumeau C, Carballo S, Bahler C, Radovanovic D, Hirschel B, et al. Increased mortality after a first myocardial infarction in human immunodeficiency virus-infected patients; a nested cohort study. AIDS Res Ther. 2015;12:4.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ladapo JA, Richards AK, DeWitt CM, Harawa NT, Shoptaw S, Cunningham WE, et al. Disparities in the quality of cardiovascular care between HIV-infected versus HIV-uninfected adults in the United States: a cross-sectional study. J Am Heart Assoc. 2017;6(11):e007107.

    Article  PubMed  PubMed Central  Google Scholar 

  63. O’Dwyer EJ, Bhamra-Ariza P, Rao S, Emmanuel S, Carr A, Holloway CJ. Lower coronary plaque burden in patients with HIV presenting with acute coronary syndrome. Open Heart. 2016;3(2):e000511.

    Article  PubMed  PubMed Central  Google Scholar 

  64. • Feinstein MJ, Mitter SS, Yadlapati A, Achenbach CJ, Palella FJ Jr, Gonzalez PE, et al. HIV-related myocardial vulnerability to infarction and coronary artery disease. J Am Coll Cardiol. 2016;68(18):2026–7. Though a small pilot study, provides interesting mechanistic insight into why prognosis after a myocardial infarction may be worse among PLWHA compared to uninfected people.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Tseng ZH, Secemsky EA, Dowdy D, Vittinghoff E, Moyers B, Wong JK, et al. Sudden cardiac death in patients with human immunodeficiency virus infection. J Am Coll Cardiol. 2012;59(21):1891–6.

    Article  PubMed  PubMed Central  Google Scholar 

  66. • Temu TM, Kirui N, Wanjalla C, Ndungu AM, Kamano JH, Inui TS, et al. Cardiovascular health knowledge and preventive practices in people living with HIV in Kenya. BMC Infect Dis. 2015;15:421. Provides data indicating cardiovascular disease risk knowledge and prioritization among PLWHA is low in Kenya, an example of a setting with high HIV prevalence, high cardiovascular disease risk factor prevalence, and constrained resources to tackle a double burden of HIV and CVD simultaneously.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rodriguez-Arboli E, Mwamelo K, Kalinjuma AV, Furrer H, Hatz C, Tanner M, et al. Incidence and risk factors for hypertension among HIV patients in rural Tanzania—a prospective cohort study. PLoS One. 2017;12(3):e0172089.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Naidu S, Ponnampalvanar S, Kamaruzzaman SB, Kamarulzaman A. Prevalence of metabolic syndrome among people living with HIV in developing countries: a systematic review. AIDS Patient Care STDs. 2017;31(1):1–13.

    Article  PubMed  Google Scholar 

  69. Divala OH, Amberbir A, Ismail Z, Beyene T, Garone D, Pfaff C, et al. The burden of hypertension, diabetes mellitus, and cardiovascular risk factors among adult Malawians in HIV care: consequences for integrated services. BMC Public Health. 2016;16(1):1243.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Angkurawaranon C, Nitsch D, Larke N, Rehman AM, Smeeth L, Addo J. Ecological study of HIV infection and hypertension in sub-Saharan Africa: is there a double burden of disease? PLoS One. 2016;11(11):e0166375.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Kwarisiima D, Balzer L, Heller D, Kotwani P, Chamie G, Clark T, et al. Population-based assessment of hypertension epidemiology and risk factors among HIV-positive and general populations in rural Uganda. PLoS One. 2016;11(5):e0156309.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Kingery JR, Alfred Y, Smart LR, Nash E, Todd J, Naguib MR, et al. Short-term and long-term cardiovascular risk, metabolic syndrome and HIV in Tanzania. Heart. 2016;102(15):1200–5.

    Article  PubMed  Google Scholar 

  73. Dimala CA, Atashili J, Mbuagbaw JC, Wilfred A, Monekosso GL. Prevalence of hypertension in HIV/AIDS patients on highly active antiretroviral therapy (HAART) compared with HAART-naive patients at the Limbe regional hospital, Cameroon. PLoS One. 2016;11(2):e0148100.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Naanyu V, Vedanthan R, Kamano JH, Rotich JK, Lagat KK, Kiptoo P, et al. Barriers influencing linkage to hypertension care in Kenya: qualitative analysis from the LARK hypertension study. J Gen Intern Med. 2016;31(3):304–14.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Mashinya F, Alberts M, Van Geertruyden JP, Colebunders R. Assessment of cardiovascular risk factors in people with HIV infection treated with ART in rural South Africa: a cross sectional study. AIDS Res Ther. 2015;12:42.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Muyanja D, Muzoora C, Muyingo A, Muyindike W, Siedner MJ. High prevalence of metabolic syndrome and cardiovascular disease risk among people with HIV on stable ART in southwestern Uganda. AIDS Patient Care STDs. 2016;30(1):4–10.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Eholie SP, Lacombe K, Krain A, Diallo Z, Ouiminga M, Campa P, et al. Metabolic disorders and cardiovascular risk in treatment-naive HIV-infected patients of sub-saharan origin starting antiretrovirals: impact of westernized lifestyle. AIDS Res Hum Retrovir. 2015;31(4):384–92.

    Article  PubMed  CAS  Google Scholar 

  78. Sander LD, Newell K, Ssebbowa P, Serwadda D, Quinn TC, Gray RH, et al. Hypertension, cardiovascular risk factors and antihypertensive medication utilisation among HIV-infected individuals in Rakai, Uganda. Tropical Med Int Health. 2015;20(3):391–6.

    Article  Google Scholar 

  79. Osegbe ID, Soriyan OO, Ogbenna AA, Okpara HC, Azinge EC. Risk factors and assessment for cardiovascular disease among HIV-positive patients attending a Nigerian tertiary hospital. Pan Afr Med J. 2016;23:206.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Menanga AP, Ngomseu CK, Jingi AM, Mfangam BM, Noubiap JJ, Gweth MN, et al. Patterns of cardiovascular disease in a group of HIV-infected adults in Yaounde, Cameroon. Cardiovasc Diagn Ther. 2015;5(6):420–7.

    PubMed  PubMed Central  Google Scholar 

  81. Botha S, Fourie CM, van Rooyen JM, Kruger A, Schutte AE. Cardiometabolic changes in treated versus never treated HIV-infected black South Africans: the PURE study. Heart Lung Circ. 2014;23(2):119–26.

    Article  PubMed  Google Scholar 

  82. Shaffer D, Hughes MD, Sawe F, Bao Y, Moses A, Hogg E, et al. Cardiovascular disease risk factors in HIV-infected women after initiation of lopinavir/ritonavir- and nevirapine-based antiretroviral therapy in sub-Saharan Africa: A5208 (OCTANE). J Acquir Immune Defic Syndr. 2014;66(2):155–63.

    PubMed  PubMed Central  CAS  Google Scholar 

  83. Feinstein MJ, Kim JH, Bibangambah P, Sentongo R, Martin JN, Tsai AC, et al. Ideal cardiovascular health and carotid atherosclerosis in a mixed cohort of HIV-infected and uninfected Ugandans. AIDS Res Hum Retrovir. 2017;33(1):49–56.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Siedner MJ, Kim JH, Nakku RS, Hemphill L, Triant VA, Haberer JE, et al. HIV infection and arterial stiffness among older-adults taking antiretroviral therapy in rural Uganda. AIDS. 2016;30(4):667–70.

    Article  PubMed  CAS  Google Scholar 

  85. Ssinabulya I, Kayima J, Longenecker C, Luwedde M, Semitala F, Kambugu A, et al. Subclinical atherosclerosis among HIV-infected adults attending HIV/AIDS care at two large ambulatory HIV clinics in Uganda. PLoS One. 2014;9(2):e89537.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Schoffelen AF, de Groot E, Tempelman HA, Visseren FL, Hoepelman AI, Barth RE. Carotid intima media thickness in mainly female HIV-infected subjects in rural South Africa: association with cardiovascular but not HIV-related factors. Clin Infect Dis. 2015;61(10):1606–14.

    Article  PubMed  CAS  Google Scholar 

  87. •• Vos A, Tempelman H, Deville W, Barth R, Wensing A, Kretzschmar M, et al. HIV and risk of cardiovascular disease in sub-Saharan Africa: rationale and design of the Ndlovu Cohort Study. Eur J Prev Cardiol. 2017;24(10):1043–50. Will provide much needed prospective, longitudinal cardiovascular disease incidence data in regions of the world with some of the highest HIV burden.

    Article  PubMed  Google Scholar 

  88. •• Strijdom H, De Boever P, Walzl G, Essop MF, Nawrot TS, Webster I, et al. Cardiovascular risk and endothelial function in people living with HIV/AIDS: design of the multi-site, longitudinal EndoAfrica study in the Western Cape Province of South Africa. BMC Infect Dis. 2017;17(1):41. Will provide much needed prospective, longitudinal cardiovascular disease incidence data in regions of the world with some of the highest HIV burden.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Soliman EZ, Sharma S, Arasteh K, Wohl D, Achhra A, Tambussi G, et al. Baseline cardiovascular risk in the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) trial. HIV Med. 2015;16 Suppl 1:46–54.

    Article  PubMed  CAS  Google Scholar 

  90. Hu XF, Young K, Chan HM. Estimating cardiovascular disease incidence from prevalence: a spreadsheet based model. BMC Med Res Methodol. 2017;17(1):9.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Benjamin LA, Corbett EL, Connor MD, Mzinganjira H, Kampondeni S, Choko A, et al. HIV, antiretroviral treatment, hypertension, and stroke in Malawian adults: a case-control study. Neurology. 2016;86(4):324–33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. • Lagat DK, DeLong AK, Wellenius GA, Carter EJ, Bloomfield GS, Velazquez EJ, et al. Factors associated with isolated right heart failure in women: a pilot study from western Kenya. Glob Heart. 2014;9(2):249–54. Identifies and highlights important cardiovascular disease risk factors that do not typically get factored into conceptual models of HIV-related cardiovascular disease risk.

    Article  PubMed  Google Scholar 

  93. Arodiwe I, Ikefuna A, Obidike E, Arodiwe E, Anisuba B, Ibeziako N, et al. Left ventricular systolic function in Nigerian children infected with HIV/AIDS: a cross-sectional study. Cardiovasc J Afr. 2016;27(1):25–9.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Namuyonga J, Lubega S, Musiime V, Lwabi P, Lubega I. Cardiac dysfunction among Ugandan HIV-infected children on antiretroviral therapy. Pediatr Infect Dis J. 2016;35(3):e85–8.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Bigna JJ, Nansseu JR, Um LN, Noumegni SR, Sime PS, Aminde LN, et al. Prevalence and incidence of pulmonary hypertension among HIV-infected people in Africa: a systematic review and meta-analysis. BMJ Open. 2016;6(8):e011921.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Kelly SG, Plankey M, Post WS, Li X, Stall R, Jacobson LP, et al. Associations between tobacco, alcohol, and drug use with coronary artery plaque among HIV-infected and uninfected men in the multicenter AIDS cohort study. PLoS One. 2016;11(1):e0147822.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Green TC, Kershaw T, Lin H, Heimer R, Goulet JL, Kraemer KL, et al. Patterns of drug use and abuse among aging adults with and without HIV: a latent class analysis of a US veteran cohort. Drug Alcohol Depend. 2010;110(3):208–20.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Kelso NE, Sheps DS, Cook RL. The association between alcohol use and cardiovascular disease among people living with HIV: a systematic review. Am J Drug Alcohol Abuse. 2015;41(6):479–88.

    PubMed  PubMed Central  Google Scholar 

  99. Kelso-Chichetto NE, Plankey M, Sheps DS, Abraham AG, Chen X, Shoptaw S, et al. The impact of long-term moderate and heavy alcohol consumption on incident atherosclerosis among persons living with HIV. Drug Alcohol Depend. 2017;181:235–41.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  100. Lorenz DR, Dutta A, Mukerji SS, Holman A, Uno H, Gabuzda D. Marijuana use impacts midlife cardiovascular events in HIV-infected men. Clin Infect Dis. 2017;65(4):626–35.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Lucas GM, Atta MG, Fine DM, McFall AM, Estrella MM, Zook K, et al. HIV, cocaine use, and hepatitis C virus: a triad of nontraditional risk factors for subclinical cardiovascular disease. Arterioscler Thromb Vasc Biol. 2016;36(10):2100–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Lesko CR, Moore RD, Tong W, Lau B. Association of injection drug use with incidence of HIV-associated non-AIDS-related morbidity by age, 1995-2014. AIDS. 2016;30(9):1447–55.

    Article  PubMed  Google Scholar 

  103. Pinto Neto L, Dias FR, Bressan FF, Santos CRO. Comparison of the ACC/AHA and Framingham algorithms to assess cardiovascular risk in HIV-infected patients. Braz J Infect Dis. 2017;21(6):577–80.

    Article  PubMed  Google Scholar 

  104. De Socio GV, Pucci G, Baldelli F, Schillaci G. Observed versus predicted cardiovascular events and all-cause death in HIV infection: a longitudinal cohort study. BMC Infect Dis 2017; 17(1):414.

  105. • Feinstein MJ, Nance RM, Drozd DR, Ning H, Delaney JA, Heckbert SR, et al. Assessing and refining myocardial infarction risk estimation among patients with human immunodeficiency virus: a study by the centers for AIDS research network of integrated clinical systems. JAMA Cardiol. 2017;2(2):155–62. Results of this study raises the question of whether we should be looking beyond HIV viremia, CD4 cell count, antiretroviral therapy and traditional cardiovascular disease risk factors in tailoring cardiovascular disease risk prediction for PLWHA.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Thompson-Paul AM, Lichtenstein KA, Armon C, Palella FJ Jr, Skarbinski J, Chmiel JS, et al. Cardiovascular disease risk prediction in the HIV outpatient study. Clin Infect Dis. 2016;63(11):1508–16.

    Article  PubMed  Google Scholar 

  107. Raggi P, De Francesco D, Manicardi M, Zona S, Bellasi A, Stentarelli C, et al. Prediction of hard cardiovascular events in HIV patients. J Antimicrob Chemother. 2016;71(12):3515–8.

    Article  PubMed  CAS  Google Scholar 

  108. Salinas JL, Rentsch C, Marconi VC, Tate J, Budoff M, Butt AA, et al. Baseline, time-updated, and cumulative HIV care metrics for predicting acute myocardial infarction and all-cause mortality. Clin Infect Dis. 2016;63(11):1423–30.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Herrera S, Guelar A, Sorli L, Vila J, Molas E, Grau M, et al. The Framingham function overestimates the risk of ischemic heart disease in HIV-infected patients from Barcelona. HIV Clin Trials. 2016;17(4):131–9.

    Article  PubMed  Google Scholar 

  110. Krikke M, Hoogeveen RC, Hoepelman AI, Visseren FL, Arends JE. Cardiovascular risk prediction in HIV-infected patients: comparing the Framingham, atherosclerotic cardiovascular disease risk score (ASCVD), Systematic Coronary Risk Evaluation for the Netherlands (SCORE-NL) and Data Collection on Adverse Events of Anti-HIV Drugs (D:A:D) risk prediction models. HIV Med. 2016;17(4):289–97.

    Article  PubMed  CAS  Google Scholar 

  111. Chew KW, Bhattacharya D, McGinnis KA, Horwich TB, Tseng CH, Currier JS, et al. Short communication: coronary heart disease risk by Framingham risk score in hepatitis C and HIV/hepatitis C-coinfected persons. AIDS Res Hum Retrovir. 2015;31(7):718–22.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Markowicz S, Delforge M, Necsoi C, De Wit S. Cardiovascular risk evaluation of HIV-positive patients in a case-control study: comparison of the D:A:D and Framingham equations. J Int AIDS Soc 2014; 17(4 Suppl 3):19515.

  113. • Friis-Moller N, Ryom L, Smith C, Weber R, Reiss P, Dabis F, et al. An updated prediction model of the global risk of cardiovascular disease in HIV-positive persons: the Data-collection on Adverse Effects of Anti-HIV Drugs (D:A:D) study. Eur J Prev Cardiol. 2016;23(2):214–23. Provides an update on a cardiovascular disease risk prediction model built using data from PLWHA.

    Article  PubMed  Google Scholar 

  114. Haissman JM, Knudsen A, Hoel H, Kjaer A, Kristoffersen US, Berge RK, et al. Microbiota-dependent marker TMAO is elevated in silent ischemia but is not associated with first-time myocardial infarction in HIV infection. J Acquir Immune Defic Syndr. 2016;71(2):130–6.

    Article  PubMed  CAS  Google Scholar 

  115. Srinivasa S, Fitch KV, Lo J, Kadar H, Knight R, Wong K, et al. Plaque burden in HIV-infected patients is associated with serum intestinal microbiota-generated trimethylamine. AIDS. 2015;29(4):443–52.

    Article  PubMed  CAS  Google Scholar 

  116. Al-Kindi SG, Kim CH, Morris SR, Freeman ML, Funderburg NT, Rodriguez B, et al. Brief report: elevated red cell distribution width identifies elevated cardiovascular disease risk in patients with HIV infection. J Acquir Immune Defic Syndr. 2017;74(3):298–302.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Haissman JM, Haugaard AK, Knudsen A, Kristoffersen US, Seljeflot I, Pedersen KK, et al. Marker of endothelial dysfunction asymmetric dimethylarginine is elevated in HIV infection but not associated with subclinical atherosclerosis. J Acquir Immune Defic Syndr. 2016;73(5):507–13.

    Article  PubMed  CAS  Google Scholar 

  118. Zanni MV, Toribio M, Wilks MQ, Lu MT, Burdo TH, Walker J, et al. Application of a novel CD206+ macrophage-specific arterial imaging strategy in HIV-infected individuals. J Infect Dis. 2017;215(8):1264–9.

    Article  PubMed  PubMed Central  Google Scholar 

  119. Knudsen A, Hag AM, Loft A, von Benzon E, Keller SH, Moller HJ, et al. HIV infection and arterial inflammation assessed by (18)F-fluorodeoxyglucose (FDG) positron emission tomography (PET): a prospective cross-sectional study. J Nucl Cardiol. 2015;22(2):372–80.

    Article  PubMed  Google Scholar 

  120. • Rasheed S, Hashim R, Yan JS. Possible biomarkers for the early detection of HIV-associated heart diseases: a proteomics and bioinformatics prediction. Comput Struct Biotechnol J. 2015;13:145–52. Provides an example of how proteomics and bioinformatics can be used to provide new insights into how HIV contributes to cardiovascular disease risk.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Yong YK, Shankar EM, Westhorpe CL, Maisa A, Spelman T, Kamarulzaman A, et al. Genetic polymorphisms in the CD14 gene are associated with monocyte activation and carotid intima-media thickness in HIV-infected patients on antiretroviral therapy. Medicine (Baltimore). 2016;95(31):e4477.

    Article  CAS  Google Scholar 

  122. Shendre A, Irvin MR, Aouizerat BE, Wiener HW, Vazquez AI, Anastos K, et al. RYR3 gene variants in subclinical atherosclerosis among HIV-infected women in the Women’s Interagency HIV Study (WIHS). Atherosclerosis. 2014;233(2):666–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. El-Far M, Tremblay CL. Gut microbial diversity in HIV infection post combined antiretroviral therapy: a key target for prevention of cardiovascular disease. Curr Opin HIV AIDS. 2017;

  124. Dirajlal-Fargo S, Sattar A, Kulkarni M, Funderburg N, McComsey GA. Soluble TWEAK may predict carotid atherosclerosis in treated HIV infection. HIV Clin Trials. 2017;18(4):156–63.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  125. Vos AG, Idris NS, Barth RE, Klipstein-Grobusch K, Grobbee DE. Pro-inflammatory markers in relation to cardiovascular disease in HIV infection. A systematic review. PLoS One. 2016;11(1):e0147484.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Vos AG, Hulzebosch A, Grobbee DE, Barth RE, Klipstein-Grobusch K. Association between immune markers and surrogate markers of cardiovascular disease in HIV positive patients: a systematic review. PLoS One. 2017;12(1):e0169986.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Secemsky EA, Scherzer R, Nitta E, Wu AH, Lange DC, Deeks SG, et al. Novel biomarkers of cardiac stress, cardiovascular dysfunction, and outcomes in HIV-infected individuals. JACC Heart Fail. 2015;3(8):591–9.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Rasmussen LJ, Knudsen A, Katzenstein TL, Gerstoft J, Obel N, Jorgensen NR, et al. Soluble urokinase plasminogen activator receptor (suPAR) is a novel, independent predictive marker of myocardial infarction in HIV-1-infected patients: a nested case-control study. HIV Med. 2016;17(5):350–7.

    Article  PubMed  CAS  Google Scholar 

  129. Bellasi A, Raggi P, Rossi R, Rochira V, Stentarelli C, Zona S, et al. Intact parathyroid hormone levels are associated with increased carotid intima media thickness in HIV infected patients. Atherosclerosis. 2014;237(2):618–22.

    Article  PubMed  CAS  Google Scholar 

  130. Knudsen A, Katzenstein TL, Benfield T, Jorgensen NR, Kronborg G, Gerstoft J, et al. Plasma plasminogen activator inhibitor-1 predicts myocardial infarction in HIV-1-infected individuals. AIDS. 2014;28(8):1171–9.

    Article  PubMed  CAS  Google Scholar 

  131. Smith JM, Flexner C. The challenge of polypharmacy in an aging population and implications for future antiretroviral therapy development. AIDS. 2017;31(Suppl 2):S173–84.

    Article  PubMed  Google Scholar 

  132. So-Armah K, Freiberg MS. Cardiovascular disease risk in an aging HIV population: not just a question of biology. Curr Opin HIV AIDS. 2014;9(4):346–54.

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Kaku So-Armah.

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Both authors received NIH grants.

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This article is part of the Topical Collection on Complications of Antiretroviral Therapy

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Methods

We searched PubMed for relevant papers in English published between January 01, 2014 and October 31, 2017. For peripheral artery disease, we relaxed the time requirement given the dearth of available studies.

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So-Armah, K., Freiberg, M.S. HIV and Cardiovascular Disease: Update on Clinical Events, Special Populations, and Novel Biomarkers. Curr HIV/AIDS Rep 15, 233–244 (2018). https://doi.org/10.1007/s11904-018-0400-5

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