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ARTICLE |

Cardiac Morbidity and Related Mortality in Children With HIV Infection FREE

Lynn M. Luginbuhl, MD; E. John Orav, PhD; Kenneth McIntosh, MD; Steven E. Lipshultz, MD
[+] Author Affiliations

Reprint requests to Department of Cardiology, Children's Hospital, 300 Longwood Ave, Boston, MA 02115 (Dr Lipshultz).


JAMA. 1993;269(22):2869-2875. doi:10.1001/jama.1993.03500220055026
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Published online

Objective.  —Dysrhythmias, hemodynamic instability, congestive heart failure, and sudden death are serious complications of human immunodeficiency virus (HIV) infection that, to our knowledge, have not been studied systematically. We sought to determine the cumulative incidence and clinical predictors of these adverse events in a cohort of HIV-infected children.

Design.  —Historical cohort study.

Setting.  —University-affiliated, primary and tertiary care pediatric hospital and ambulatory care center.

Participants.  —Eighty-one HIV-infected children who had one or more cardiac evaluations between 1984 and 1991 form the study cohort. The initial cardiac evaluation occurred at a median age of 1.5 years, and children were followed up to a median age of 3.6 years.

Main Outcome Measures.  —Mortality (related to cardiac dysfunction as well as noncardiac causes), tachycardia, bradycardia, hypertension, hypotension, marked sinus arrhythmia, cardiac arrest, and chronic congestive heart failure.

Results.  —Hemodynamic abnormalities and dysrhythmias occurred frequently. Eight unexpected cardiorespiratory arrests occurred in seven children (9%). Chronic congestive heart failure was noted in 10% of patients. Thirty children died, 10 with significant cardiac dysfunction. As HIV-infected children progressed from acquired immunodeficiency syndrome (AIDS)—related complex to AIDS, significant cardiac problems were more likely to occur. Both nonneurologic AIDS and encephalopathy were strongly associated with most severe cardiac outcomes. However, encephalopathy was the strongest correlate of cardiorespiratory arrest (P=.002). Epstein-Barr virus coinfection was the strongest correlate of chronic congestive heart failure (P<.001).

Conclusions.  —Cardiac morbidity and mortality are more common with advanced HIV infection. The presence of encephalopathy or Epstein-Barr virus coinfection identifies HIV-infected children at especially high risk for adverse cardiac outcomes.(JAMA. 1993;269:2869-2875)

REFERENCES

Lipshultz SE, Chanock S, Sanders SP, Colan SD, McIntosh K.  Cardiovascular manifestations of human immunodeficiency virus infection in infants and children. Am J Cardiol . 1989;;63:1489-1497.
Craddock C, Pasvol G, Bull R, Protheroe A, Hopkin A, Horkin J.  Cardiorespiratory arrest and autonomic neuropathy in AIDS. Lancet . 1987;;2:16-18.
Brady MT, Reiner CB, Singley C, Roberts WH, Sneddon JM.  Unexpected death in an infant with AIDS: disseminated cytomegalovirus infection with pancarditis. Pediatr Pathol . 1988;;8:205-214.
Kovacs A, Hinton D, Wong W, Rasheed S, Ono J, Hofman F.  HIV infection of myocytes and sudden death in pediatric AIDS. Pediatr Res . 1992;;31: 167A. Abstract 986.
Lipshultz SE, Luginbuhl L, Saul JP, McIntosh K.  Dysrhythmias, unexpected arrest, and sudden death in pediatric HIV infection. Circulation . 1991;; 84:II-660. Abstract.
Anderson DW, Virmani R.  Emerging patterns of heart disease in human immunodeficiency virus infection. Hum Pathol . 1991;;21:253-259.
Anderson DW, Virmani R, Reilly JM, et al.  Prevalent myocarditis at necropsy in the acquired immunodeficiency syndrome. J Am Coll Cardiol . 1988;; 11:792-799.
Reilly JM, Cunnion RE, Anderson DW, et al.  Frequency of myocarditis, left ventricular dysfunction, and ventricular tachycardia in the acquired immune deficiency syndrome. Am J Cardiol . 1988;; 62:789-793.
Bharati S, Joshi VV, Connor EM, Oleske JM, Lev M.  Conduction system in children with acquired immunodeficiency syndrome. Chest . 1989;; 96:406-413.
Simpson DM, Wolfe DE.  Neuromuscular complications of HIV infection and its treatment. AIDS . 1991;;5:917-926.
Freeman R, Roberts MS, Friedman LS, Broadbridge C.  Autonomic function and human immunodeficiency virus infection. Neurology . 1990;;40: 575-580.
Ruttimann S, Hilti P, Spinas GA, Dubach UC.  High frequency of human immunodeficiency virus— associated autonomic neuropathy and more severe involvement in advanced stages of human immunodeficiency virus disease. Arch Intern Med . 1991;; 151:2441-2443.
Welby SB, Rogerson SJ, Beeching NJ.  Autonomic neuropathy is common in human immunodeficiency virus infection. J Infect . 1991;;23:123-128.
Villa A, Foresti V.  Autonomic nervous system dysfunction associated with HIV infection in intravenous heroin users. AIDS . 1992;;6:85-89.
Scott G, Piaggesi A, Ewing DJ.  Sequential autonomic function tests in HIV infection. AIDS . 1990;; 4:1279-1281.
Cohen J, Laudenslager M.  Autonomic nervous system dysfunction in human immunodeficiency virus. Neurology . 1989;;8:111-112.
Lipshultz SE, Sanders SP, Colan SD, McIntosh K.  Enhanced left ventricular function in pediatric human immunodeficiency virus infection. Pediatr Res . 1989;;25:183A. Abstract.
Centers for Disease Control and Prevention.  Classification system for human immunodeficiency virus (HIV) infection in children under 13 years of age. MMWR Morb Mortal Wkly Rep . 1987;;36:225-236.
Colan SD, Borow KM, Neumann A.  Left ventricular end-systolic wall stress-velocity of fiber shortening relation: a load-independent index of myocardial contractility. J Am Coll Cardiol . 1984;; 4:715-724.
Lipshultz SE, Orav EJ, Sanders SP, Hale AR, McIntosh K, Colan SD.  Cardiac structure and function in children with human immunodeficiency virus infection treated with zidovudine. N Engl J Med . 1992;;327:1260-1265.
Colan SD, Parness IA, Spevak PJ, Sanders SP.  Developmental modulation of myocardial mechanics: age- and growth-related alterations in afterload and contractility. J Am Coll Cardiol . 1992;:19:619-629.
Davignon A, Rautaharju P, Boisselle E, Soumis F, Megelas M, Choquette A.  Normal ECG standards for infants and children. Pediatr Cardiol . 1980;;1:123-131.
Garson A Jr. The Electrocardiogram in Infants and Children: A Systematic Approach . Philadelphia, Pa: Lea and Febiger; 1983;.
Lennette ET.  Epstein-Barr virus.  In: Lennette EH, Holonen P, Murphy FA, eds. Laboratory Diagnosis of Infectious Diseases: Principles and Practice . New York, NY: Springer-Verlag; 1988;;2:230-246.
Fleischer G, Henle W, Henle G, et al.  Primary infection with Epstein-Barr virus in infants in the United States: clinical and serologic observations. J Infect Dis . 1979;;139:553-558.
Cappel R, De Cuyper F, De Braekeleer J.  Rapid detection of IgG and IgM antibodies for cytomegalovirus by the enzyme-linked immunosorbent assay (ELISA). Arch Virol . 1978;;58:253-258.
Gleaves CA, Smith TF, Shuster EA, Pearson GR.  Rapid detection of cytomegalovirus in MRC-5 cells inoculated with urine specimens by using low-speed centrifugation and monoclonal antibody to an early antigen. J Clin Microbiol . 1984;;19:917-919.
Task Force on Blood Pressure Control in Children.  Report of the second Task Force on Blood Pressure Control in Children, 1987. Pediatrics . 1987;; 79:1-25.
Villa A, Cruccu V, Foresti V, Guareschi G, Tronci M, Confalonieri F.  HIV-related functional involvement of autonomic nervous system. Acta Neurol . 1990;;12:14-18.
Joshi VV, Gadol C, Connor E, Oleske JM, Mendelson J, Marin-Garcia J.  Dilated cardiomyopathy in children with acquired immunodeficiency syndrome: a pathologic study of five cases. Hum Pathol . 1988;;19:69-73.
Stewart JM, Kaul A, Gromisch DS, Reyes E, Woolf PK, Gowitz MH.  Symptomatic cardiac dysfunction in children with human immunodeficiency virus infection. Am Heart J . 1989;;117:140-144.
Kaul S, Fishbein MC, Siegel RJ.  Cardiac manifestations of acquired immune deficiency syndrome: a 1991 update. Am Heart J . 1991;;122:535-544.
Acierno LJ.  Cardiac complications in acquired immunodeficiency syndrome (AIDS): a review. J Am Coll Cardiol . 1989;;13:1144-1154.
Kelly JW, Dooley DP, Lattuada CP, Smith CE.  A severe, unusual reaction to trimethoprim-sulfamethoxazole in patients infected with human immunodeficiency virus. Clin Infect Dis . 1992;;14:1034-1039.
Cohen AJ, Weiser B, Afzal Q, Fuhrer J.  Ventricular tachycardia in two patients with AIDS receiving gancyclovir (DHPG). AIDS . 1990;;4:807-809.
Stein KM, Haronian H, Mensah GA, Acosta A, Jacobs J, Kligfield P.  Ventricular tachycardia and torsades de pointes complicating pentamidine therapy of Pneumocystis carinii pneumonia in the acquired immunodeficiency syndrome. Am J Cardiol . 1990;;66:888-889.
Wharton JM, Demopulos PA, Goldschlager N.  Torsades de pointes during administration of pentamidine isethionate. Am J Med . 1987;;83:571-576.
Tyson AA, Hackshaq BT, Kutcher MA.  Acute Epstein-Barr virus myocarditis simulating myocardial infarction with cardiogenic shock. South Med J . 1989;:82:1184-1187.
Miller R, Ward C, Amsterdam E, Mason DT, Zelis R.  Focal mononucleosis myocarditis simulating myocardial infarction. Chest . 1973;;63:102-105.
Butler T, Pastore J, Simon G, et al.  Infectious mononucleosis myocarditis. J Infect . 1981;;3:172-175.
Fish M, Barton H.  Heart involvement in infectious mononucleosis. Arch Intern Med . 1958;;101: 636-644.
Frishman W, Kraus ME, Zabkar J, Brooks V, Alonso D, Dixon LM.  Infectious mononucleosis and fatal myocarditis. Chest . 1977;;72:535-538.
Moiseev VS, Ogurtsov PP, Traianova TG, et al.  The viral and immunological characteristics of cardiomyopathies and myocarditis. Ter Arkh . 1990;;62: 77-82.
Webster BH.  Cardiac complications of infectious mononucleosis: a review of the literature and report of 5 cases. Am J Med Sci . 1957;;234: 62-70.
Ogurtsov PP, Stepina VN, Rukosuev VS, Nanaev AK.  Epstein-Barr virus infection and congestive cardiomyopathy (serologic and immunomorphologic aspects). Biull-Vsesoiuznogo-Kardiol-Nauchn-Tsentra-AMN-SSSR . 1988;;11:18-22.
Jacob AJ, Boon NA.  HIV cardiomyopathy: a dark cloud with a silver lining? Br Heart J . 1991;; 66:1-2.
Cotton P.  AIDS giving rise to cardiac problems. JAMA . 1990;;263:2149.
Lewis WL, Grody WW.  AIDS and the heart: review and consideration of pathogenic mechanisms. Cardiovasc Pathol . 1992;;1:53-64.
Kaplan LD, McGrath MS.  AIDS-associated non-Hodgkin's lymphoma. AIDS Updates . 1991;;4:1-11.
Andiman WA, Eastman R, Martin K, et al.  Opportunistic lymphoproliferations associated with Epstein-Barr viral DNA in infants and children with AIDS. Lancet . 1985;;2:1390-1393.
Goldblum N, Daefler S, Llana T, Ablashi D, Josephs S, Salahuddin Z.  Susceptibility to HIV-1 infection of a human B-lymphoblastoid cell line, DG75, transfected with subgenomic DNA fragments of Epstein-Barr virus. Dev Biol Stand . 1990;;72:309-313.
Laurence J, Astrin SM.  Human immunodeficiency virus induction of malignant transformation in human B lymphocytes. Proc Natl Acad Sci U S A . 1991;;88:7635-7639.
Mallon J, Borkowski J, Albin R, Pepitoni S, Schwartz J, Kieff E.  The Epstein-Barr virus BZLF1 gene product activates the human immunodeficiency virus type 1 5' long terminal repeat. J Virol . 1990;;64:6282-6285.
Calabrese LH, Proffitt MR, Yen-Lieberman B, Hobbs RE, Ratliff NB.  Congestive cardiomyopathy and illness related to the acquired immunodeficiency syndrome (AIDS) associated with isolation of retrovirus from myocardium. Ann Intern Med . 1987;;107:691-692.
Flomenbaum M, Soeiro R, Udem S, Kress Y, Factor S.  Proliferative membranopathy and human immunodeficiency virus in AIDS hearts. J Acquir Immune Defic Syndr . 1989;;2:129-135.
Lipshultz SE, Fox CH, Perez-Atayde AR, et al.  Identification of human immunodeficiency virus-1 RNA and DNA in the heart of a child with cardiovascular abnormalities and congenital acquired immune deficiency syndrome. Am J Cardiol . 1990;; 66:246-250.
Grody WW, Cheng L, Lewis W.  Infection of the heart by the human immunodeficiency virus. Am J Cardiol . 1990;;66:203-206.
Cenacchi G, Re MC, Furlini G, et al.  Human immunodeficiency virus type 1 antigen detection in endomyocardial biopsy: an immunomorphological study. Microbiologica . 1990;;13:145-9.
Wu AY-Y, Forouhar F, Cartun RW, et al.  Identification of human immunodeficiency virus in the heart of a patient with acquired immunodeficiency syndrome. Mod Pathol . 1990;;3:625-630.
Wu TC, Pizzorno MC, Hayward GS, et al.  In situ detection of human cytomegalovirus immediateearly gene transcripts within cardiac myocytes of patients with HIV-associated cardiomyopathy. AIDS . 1992;;6:777-785.
Hsia J, Adams S, Mohanty N, Ross A.  Human immunodeficiency virus-related heart disease during 560 patient-years of follow-up. Circulation . 1992;; 86:I-795. Abstract.
De Castro S, d'Amati G, Gallo P, et al.  Frequency and significance of acute global left ventricular dysfunction (LVD) in human immunodeficiency virus (HIV) infection. J Am Coll Cardiol . 1993;;21:280A. Abstract.
Kavanaugh-McHugh AL, Hutton N, Holt E, Modlin JF, Livingston R, Ruff AJ.  Echocardiographic abnormalities in pediatric HIV infection: prevalence and serial changes. Pediatr Res . 1992;;31: 166A. Abstract.
Stein KM, Fenton C, Lehany AM, Okin PM, Kligfield P.  Incidence of QT interval prolongation during pentamidine therapy of Pneumocystis carinii pneumonia. Am J Cardiol . 1991;;68:1091-1094.

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

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Lipshultz SE, Chanock S, Sanders SP, Colan SD, McIntosh K.  Cardiovascular manifestations of human immunodeficiency virus infection in infants and children. Am J Cardiol . 1989;;63:1489-1497.
Craddock C, Pasvol G, Bull R, Protheroe A, Hopkin A, Horkin J.  Cardiorespiratory arrest and autonomic neuropathy in AIDS. Lancet . 1987;;2:16-18.
Brady MT, Reiner CB, Singley C, Roberts WH, Sneddon JM.  Unexpected death in an infant with AIDS: disseminated cytomegalovirus infection with pancarditis. Pediatr Pathol . 1988;;8:205-214.
Kovacs A, Hinton D, Wong W, Rasheed S, Ono J, Hofman F.  HIV infection of myocytes and sudden death in pediatric AIDS. Pediatr Res . 1992;;31: 167A. Abstract 986.
Lipshultz SE, Luginbuhl L, Saul JP, McIntosh K.  Dysrhythmias, unexpected arrest, and sudden death in pediatric HIV infection. Circulation . 1991;; 84:II-660. Abstract.
Anderson DW, Virmani R.  Emerging patterns of heart disease in human immunodeficiency virus infection. Hum Pathol . 1991;;21:253-259.
Anderson DW, Virmani R, Reilly JM, et al.  Prevalent myocarditis at necropsy in the acquired immunodeficiency syndrome. J Am Coll Cardiol . 1988;; 11:792-799.
Reilly JM, Cunnion RE, Anderson DW, et al.  Frequency of myocarditis, left ventricular dysfunction, and ventricular tachycardia in the acquired immune deficiency syndrome. Am J Cardiol . 1988;; 62:789-793.
Bharati S, Joshi VV, Connor EM, Oleske JM, Lev M.  Conduction system in children with acquired immunodeficiency syndrome. Chest . 1989;; 96:406-413.
Simpson DM, Wolfe DE.  Neuromuscular complications of HIV infection and its treatment. AIDS . 1991;;5:917-926.
Freeman R, Roberts MS, Friedman LS, Broadbridge C.  Autonomic function and human immunodeficiency virus infection. Neurology . 1990;;40: 575-580.
Ruttimann S, Hilti P, Spinas GA, Dubach UC.  High frequency of human immunodeficiency virus— associated autonomic neuropathy and more severe involvement in advanced stages of human immunodeficiency virus disease. Arch Intern Med . 1991;; 151:2441-2443.
Welby SB, Rogerson SJ, Beeching NJ.  Autonomic neuropathy is common in human immunodeficiency virus infection. J Infect . 1991;;23:123-128.
Villa A, Foresti V.  Autonomic nervous system dysfunction associated with HIV infection in intravenous heroin users. AIDS . 1992;;6:85-89.
Scott G, Piaggesi A, Ewing DJ.  Sequential autonomic function tests in HIV infection. AIDS . 1990;; 4:1279-1281.
Cohen J, Laudenslager M.  Autonomic nervous system dysfunction in human immunodeficiency virus. Neurology . 1989;;8:111-112.
Lipshultz SE, Sanders SP, Colan SD, McIntosh K.  Enhanced left ventricular function in pediatric human immunodeficiency virus infection. Pediatr Res . 1989;;25:183A. Abstract.
Centers for Disease Control and Prevention.  Classification system for human immunodeficiency virus (HIV) infection in children under 13 years of age. MMWR Morb Mortal Wkly Rep . 1987;;36:225-236.
Colan SD, Borow KM, Neumann A.  Left ventricular end-systolic wall stress-velocity of fiber shortening relation: a load-independent index of myocardial contractility. J Am Coll Cardiol . 1984;; 4:715-724.
Lipshultz SE, Orav EJ, Sanders SP, Hale AR, McIntosh K, Colan SD.  Cardiac structure and function in children with human immunodeficiency virus infection treated with zidovudine. N Engl J Med . 1992;;327:1260-1265.
Colan SD, Parness IA, Spevak PJ, Sanders SP.  Developmental modulation of myocardial mechanics: age- and growth-related alterations in afterload and contractility. J Am Coll Cardiol . 1992;:19:619-629.
Davignon A, Rautaharju P, Boisselle E, Soumis F, Megelas M, Choquette A.  Normal ECG standards for infants and children. Pediatr Cardiol . 1980;;1:123-131.
Garson A Jr. The Electrocardiogram in Infants and Children: A Systematic Approach . Philadelphia, Pa: Lea and Febiger; 1983;.
Lennette ET.  Epstein-Barr virus.  In: Lennette EH, Holonen P, Murphy FA, eds. Laboratory Diagnosis of Infectious Diseases: Principles and Practice . New York, NY: Springer-Verlag; 1988;;2:230-246.
Fleischer G, Henle W, Henle G, et al.  Primary infection with Epstein-Barr virus in infants in the United States: clinical and serologic observations. J Infect Dis . 1979;;139:553-558.
Cappel R, De Cuyper F, De Braekeleer J.  Rapid detection of IgG and IgM antibodies for cytomegalovirus by the enzyme-linked immunosorbent assay (ELISA). Arch Virol . 1978;;58:253-258.
Gleaves CA, Smith TF, Shuster EA, Pearson GR.  Rapid detection of cytomegalovirus in MRC-5 cells inoculated with urine specimens by using low-speed centrifugation and monoclonal antibody to an early antigen. J Clin Microbiol . 1984;;19:917-919.
Task Force on Blood Pressure Control in Children.  Report of the second Task Force on Blood Pressure Control in Children, 1987. Pediatrics . 1987;; 79:1-25.
Villa A, Cruccu V, Foresti V, Guareschi G, Tronci M, Confalonieri F.  HIV-related functional involvement of autonomic nervous system. Acta Neurol . 1990;;12:14-18.
Joshi VV, Gadol C, Connor E, Oleske JM, Mendelson J, Marin-Garcia J.  Dilated cardiomyopathy in children with acquired immunodeficiency syndrome: a pathologic study of five cases. Hum Pathol . 1988;;19:69-73.
Stewart JM, Kaul A, Gromisch DS, Reyes E, Woolf PK, Gowitz MH.  Symptomatic cardiac dysfunction in children with human immunodeficiency virus infection. Am Heart J . 1989;;117:140-144.
Kaul S, Fishbein MC, Siegel RJ.  Cardiac manifestations of acquired immune deficiency syndrome: a 1991 update. Am Heart J . 1991;;122:535-544.
Acierno LJ.  Cardiac complications in acquired immunodeficiency syndrome (AIDS): a review. J Am Coll Cardiol . 1989;;13:1144-1154.
Kelly JW, Dooley DP, Lattuada CP, Smith CE.  A severe, unusual reaction to trimethoprim-sulfamethoxazole in patients infected with human immunodeficiency virus. Clin Infect Dis . 1992;;14:1034-1039.
Cohen AJ, Weiser B, Afzal Q, Fuhrer J.  Ventricular tachycardia in two patients with AIDS receiving gancyclovir (DHPG). AIDS . 1990;;4:807-809.
Stein KM, Haronian H, Mensah GA, Acosta A, Jacobs J, Kligfield P.  Ventricular tachycardia and torsades de pointes complicating pentamidine therapy of Pneumocystis carinii pneumonia in the acquired immunodeficiency syndrome. Am J Cardiol . 1990;;66:888-889.
Wharton JM, Demopulos PA, Goldschlager N.  Torsades de pointes during administration of pentamidine isethionate. Am J Med . 1987;;83:571-576.
Tyson AA, Hackshaq BT, Kutcher MA.  Acute Epstein-Barr virus myocarditis simulating myocardial infarction with cardiogenic shock. South Med J . 1989;:82:1184-1187.
Miller R, Ward C, Amsterdam E, Mason DT, Zelis R.  Focal mononucleosis myocarditis simulating myocardial infarction. Chest . 1973;;63:102-105.
Butler T, Pastore J, Simon G, et al.  Infectious mononucleosis myocarditis. J Infect . 1981;;3:172-175.
Fish M, Barton H.  Heart involvement in infectious mononucleosis. Arch Intern Med . 1958;;101: 636-644.
Frishman W, Kraus ME, Zabkar J, Brooks V, Alonso D, Dixon LM.  Infectious mononucleosis and fatal myocarditis. Chest . 1977;;72:535-538.
Moiseev VS, Ogurtsov PP, Traianova TG, et al.  The viral and immunological characteristics of cardiomyopathies and myocarditis. Ter Arkh . 1990;;62: 77-82.
Webster BH.  Cardiac complications of infectious mononucleosis: a review of the literature and report of 5 cases. Am J Med Sci . 1957;;234: 62-70.
Ogurtsov PP, Stepina VN, Rukosuev VS, Nanaev AK.  Epstein-Barr virus infection and congestive cardiomyopathy (serologic and immunomorphologic aspects). Biull-Vsesoiuznogo-Kardiol-Nauchn-Tsentra-AMN-SSSR . 1988;;11:18-22.
Jacob AJ, Boon NA.  HIV cardiomyopathy: a dark cloud with a silver lining? Br Heart J . 1991;; 66:1-2.
Cotton P.  AIDS giving rise to cardiac problems. JAMA . 1990;;263:2149.
Lewis WL, Grody WW.  AIDS and the heart: review and consideration of pathogenic mechanisms. Cardiovasc Pathol . 1992;;1:53-64.
Kaplan LD, McGrath MS.  AIDS-associated non-Hodgkin's lymphoma. AIDS Updates . 1991;;4:1-11.
Andiman WA, Eastman R, Martin K, et al.  Opportunistic lymphoproliferations associated with Epstein-Barr viral DNA in infants and children with AIDS. Lancet . 1985;;2:1390-1393.
Goldblum N, Daefler S, Llana T, Ablashi D, Josephs S, Salahuddin Z.  Susceptibility to HIV-1 infection of a human B-lymphoblastoid cell line, DG75, transfected with subgenomic DNA fragments of Epstein-Barr virus. Dev Biol Stand . 1990;;72:309-313.
Laurence J, Astrin SM.  Human immunodeficiency virus induction of malignant transformation in human B lymphocytes. Proc Natl Acad Sci U S A . 1991;;88:7635-7639.
Mallon J, Borkowski J, Albin R, Pepitoni S, Schwartz J, Kieff E.  The Epstein-Barr virus BZLF1 gene product activates the human immunodeficiency virus type 1 5' long terminal repeat. J Virol . 1990;;64:6282-6285.
Calabrese LH, Proffitt MR, Yen-Lieberman B, Hobbs RE, Ratliff NB.  Congestive cardiomyopathy and illness related to the acquired immunodeficiency syndrome (AIDS) associated with isolation of retrovirus from myocardium. Ann Intern Med . 1987;;107:691-692.
Flomenbaum M, Soeiro R, Udem S, Kress Y, Factor S.  Proliferative membranopathy and human immunodeficiency virus in AIDS hearts. J Acquir Immune Defic Syndr . 1989;;2:129-135.
Lipshultz SE, Fox CH, Perez-Atayde AR, et al.  Identification of human immunodeficiency virus-1 RNA and DNA in the heart of a child with cardiovascular abnormalities and congenital acquired immune deficiency syndrome. Am J Cardiol . 1990;; 66:246-250.
Grody WW, Cheng L, Lewis W.  Infection of the heart by the human immunodeficiency virus. Am J Cardiol . 1990;;66:203-206.
Cenacchi G, Re MC, Furlini G, et al.  Human immunodeficiency virus type 1 antigen detection in endomyocardial biopsy: an immunomorphological study. Microbiologica . 1990;;13:145-9.
Wu AY-Y, Forouhar F, Cartun RW, et al.  Identification of human immunodeficiency virus in the heart of a patient with acquired immunodeficiency syndrome. Mod Pathol . 1990;;3:625-630.
Wu TC, Pizzorno MC, Hayward GS, et al.  In situ detection of human cytomegalovirus immediateearly gene transcripts within cardiac myocytes of patients with HIV-associated cardiomyopathy. AIDS . 1992;;6:777-785.
Hsia J, Adams S, Mohanty N, Ross A.  Human immunodeficiency virus-related heart disease during 560 patient-years of follow-up. Circulation . 1992;; 86:I-795. Abstract.
De Castro S, d'Amati G, Gallo P, et al.  Frequency and significance of acute global left ventricular dysfunction (LVD) in human immunodeficiency virus (HIV) infection. J Am Coll Cardiol . 1993;;21:280A. Abstract.
Kavanaugh-McHugh AL, Hutton N, Holt E, Modlin JF, Livingston R, Ruff AJ.  Echocardiographic abnormalities in pediatric HIV infection: prevalence and serial changes. Pediatr Res . 1992;;31: 166A. Abstract.
Stein KM, Fenton C, Lehany AM, Okin PM, Kligfield P.  Incidence of QT interval prolongation during pentamidine therapy of Pneumocystis carinii pneumonia. Am J Cardiol . 1991;;68:1091-1094.
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