HIV-Related Cardiac Complications: CT and MRI Findings

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1 Cardiopulmonary Imaging Pictorial Essay Nakazono et al. CT and MRI of HIV-Related Cardiac Complications Cardiopulmonary Imaging Pictorial Essay Downloaded from by on 02/06/18 from IP address Copyright RRS. For personal use only; all rights reserved Takahiko Nakazono 1,2 Jean Jeudy 1 Charles S. White 1 Nakazono T, Jeudy J, White CS Keywords: IDS, IDS complications, cardiovascular disease, CT, HIV, MRI DOI: /JR Received December 28, 2010; accepted after revision ugust 2, Department of Diagnostic Radiology and Nuclear Medicine, University of Maryland School of Medicine, altimore, MD. 2 Present ddress: Department of Radiology, Saga Social Insurance Hospital, Hyogominami 3-8-1, Saga City, Saga , Japan. ddress correspondence to T. Nakazono (nakazot@hotmail.co.jp). JR 2012; 198: X/12/ merican Roentgen Ray Society HIV-Related Cardiac Complications: CT and MRI Findings OJECTIVE. Cardiovascular complications in patients with HIV infection include myocardial, endocardial, pericardial, and vascular diseases. The complications are caused by the HIV infection itself, opportunistic infections, HIV-related tumors, and the side effects of highly active antiretroviral therapy. The article reviews the CT and MRI findings suggestive of HIV-related cardiovascular diseases. CONCLUSION. The cardiovascular complications of HIV infection frequently overlap, making the diagnosis difficult. CT and MRI are useful for the noninvasive evaluation of these complications. I n 2009, approximately 33.3 million people globally were living with HIV infection, 2.6 million people were newly infected with HIV, and 1.8 million people died of IDS [1]. Since the advent of highly active antiretroviral therapy (HRT) in 1996, HIV-related mortality has decreased drastically. However, because HIV-infected patients are living longer, cardiovascular complications have become more frequent and a major problem in many patients [2]. Complications may include myocardial, endocardial, pericardial, and vascular diseases that are caused by the HIV infection itself, opportunistic infections, HIV-related tumors, and the side effects of HRT. lthough echocardiography is a standard tool for the evaluation of cardiac diseases, CT and MRI are increasingly used to provide additional information. This article reviews the clinical features and CT and MRI findings of HIV-related cardiovascular complications. Dilated Cardiomyopathy Dilated cardiomyopathy occurs in HIVinfected patients with a prevalence of 8 30% [3]. The cause is unclear, but it may be the result of myocardial invasion by the HIV infection itself, opportunistic infections, an autoimmune response, drug-related cardiac toxicity, nutritional deficiencies, endothelial dysfunction, autonomic dysfunction, or prolonged immunosuppression [2]. This complication usually occurs in patients with advanced immunosuppression and low CD4 lymphocyte counts [4]. Isolated left or right cardiac dysfunction may occur. On CT and MRI, dilatation of cardiac chambers (Figs. 1 3, 4, and S4 [Figs. S4, S5C, S6C, and S8 can be seen in the JR electronic supplement to this article, available at and presents more detail than the figures printed here.]) is present, occasionally with left ventricular wall thinning (Fig. 2) or thickening (Fig. 3). Cine MRI is useful for the evaluation of cardiac function and shows diffuse hypokinesis of the cardiac walls, as shown in Figure S4. Right cardiac dysfunction may cause dilatation of the superior vena cava (Fig. 2), inferior vena cava (Figs. 1C, 1D, and 3), hepatic veins (Fig. 1D), and coronary sinus (Fig. 1C). Pericardial effusion (Figs. 3, 4, and S4), pleural effusions (Figs. 2, 4, and S4), and pulmonary edema (Fig. 2) are seen in patients with severe heart failure. Myocarditis The incidence of myocarditis is reported to be 6 52% in HIV-infected patients [4]. No specific pathogen is found in more than 80% of the affected patients, but lymphocytic myocarditis is present in approximately half of the cases at autopsy [4]. The common pathogens of infectious myocarditis include Toxoplasma gondii, Mycobacterium tuberculosis, and Cryptococcus neoformans [5]. MRI is useful for the evaluation of myocarditis. Myocardial edema shows high signal intensity on T2-weighted and STIR MR images 364 JR:198, February 2012

2 CT and MRI of HIV-Related Cardiac Complications Downloaded from by on 02/06/18 from IP address Copyright RRS. For personal use only; all rights reserved (Fig. 5). Late gadolinium-enhanced MR images typically show linear or nodular enhancement with a nonsegmental distribution predominantly in intramural or subepicardial regions (Fig. 5), which may reflect both inflammation in the early stage and fibrosis in the late stage of myocarditis [6]. Cine MRI, shows motion abnormalities of the involved cardiac walls (Fig. S5C [available at Coronary rtery Disease oth the prevalence of coronary artery disease (CD) and mortality associated with it appear to be increased among HIV-infected patients [2]. lthough the mechanism is still unclear, HIV is believed to accelerate atherosclerosis [2]. CD is also caused by metabolic abnormalities such as lipodystrophy, hyperlipidemia, and hyperglycemia caused by protease inhibitors in HRT [2] (Figs. 6, 6, and 7). HRT is independently associated with a 26% relative increase in the rate of myocardial infarction per year of exposure [7]. ECG-gated MDCT angiography has high spatial and temporal resolution and is especially useful for the diagnosis of CD (Fig. 6). Perfusion MRI can detect ischemia as a perfusion defect in the myocardium, and myocardial infarction shows subendocardial or transmural enhancement on late gadolinium-enhanced MR images. Cine MRI shows abnormal wall motion with ischemia. Endocarditis The prevalence of endocarditis in autopsy studies of patients with IDS has been reported to be 10 17% [3]. lthough any cardiac valve can be involved, the most common location is the tricuspid valve [3]. Infective endocarditis usually occurs in patients using illicit IV drugs. Staphylococcus aureus (75%) and Streptococcus viridians (20%) are the most common causative organisms [8]. ECG-gated CT and MRI show a vegetation as an oscillating mass adjacent to the involved cardiac valve (Figs. 6, and S6C [available at or as irregular thickening of the valve (Fig. 7). In leftsided endocarditis, the most serious complications are cerebral and myocardial emboli. Right-sided endocarditis causes septic emboli, abscess, and infarction in the lung. Cardiac valvular insufficiency may develop in association with endocarditis [9], and cine MRI can detect the regurgitant jet (Figs. 8 and S8 [available at Pericardial Effusion and Pericarditis Pericardial effusion is the most common (5 46%) cardiovascular complication of HIV infection and may be caused by infection or HIV-related tumors [3]. The presence of a pericardial effusion is an independent predictor of mortality and poor prognosis [2]. Serous pericardial effusion is most common and shows low attenuation on CT images (Fig. 3), low signal intensity on T1-weighted MR images, and high signal intensity on T2-weighted MR images (Fig. 4). Sanguineous or purulent effusion may increase attenuation on CT images and signal intensity on T1-weighted MR images. In pericarditis, thickening of the pericardium may be seen. Cardiac Involvement of HIV-Related Tumors Various malignancies are associated with HIV infection, but cardiac involvement by these tumors is rare. Kaposi sarcoma is a lowgrade malignancy that derives from mesenchymal cells or endothelial cells and is the most common HIV-related tumor. The epicardium and pericardium are most frequently involved by Kaposi sarcoma [9]. Lymphoma is the second most common tumor involving the heart in HIV-infected patients. The majority of the lesions are high-grade - cell tumors such as large cell immunoblastic or urkitt lymphomas [3] (Fig. 9). The right atrium is most commonly involved by malignant lymphomas [9]. Pericardial effusion (Fig. 9) and pericardial involvement (Fig. 10) are common in malignant lymphomas. Myocardial involvement in HIV-related tumors shows single or multiple ill-defined lesions with low attenuation on contrastenhanced CT images (Figs. 9 and 9) and high signal intensity on T2-weighted and STIR MR images (Fig. 9C) corresponding to the myocardium. The lesions show heterogeneous enhancement on late gadoliniumenhanced MR images [3]. Tumor necrosis is rare in malignant lymphoma [3]. Pulmonary rterial Hypertension The incidence of pulmonary arterial hypertension (PH) in HIV-infected patients is several thousand times greater than that in the general population [2]. lthough the cause is unclear, PH is caused by only HIV infection in most cases and may be caused by secondary pulmonary fibrosis resulting from recurrent pulmonary infection and IV drug abuse in others [10] (Figs. 1 and 2). The histopathologic findings of HIV-related PH are similar to those of primary PH, and the most common finding is plexogenic pulmonary arteriopathy [10]. The prognosis of patients with this complication is poor because of right heart dysfunction [2]. The imaging findings of HIV-related PH are similar to those observed in primary PH. They include enlargement of the pulmonary artery trunk and central pulmonary arteries (Figs. 1 and 2), tapering of peripheral vessels, and right atrial and ventricular dilatation (Figs. 1 and 2). Vasculitis, neurysm, and ortic Dissection oth infective and noninfective vasculitides rarely occur in association with HIV infection. Various types of noninfective vasculitis that involve small, medium, and large vessels are found in these patients [11]. Infective arteritis or aortitis is rare, but mycotic aneurysms may develop, especially in IV drug users. The causative agents include Salmonella species, M. tuberculosis, S. aureus, and Treponema pallidum [3, 12] (Fig. 11). In addition, HIV infection and long-term HRT can accelerate atherosclerosis in patients [13]. Vasculitides and atherosclerosis can cause aneurysms (Fig. 11), aortic dissection (Fig. 11), and arterial occlusive disease. neurysms may be single or multiple and may affect vessels such as the aorta or the common carotid, common iliac, femoral, or popliteal arteries [3]. Cerebral vasculopathy with aneurysms is a rare but severe complication in HIV-infected patients. This condition produces diffuse dilatation of the major arteries of the circle of Willis and occurs predominantly in young adults who present with strokes or other brain involvement and sometimes in patients who present with pseudodementia or confusion [11]. The underlying pathogenesis of this complication is unknown and both HIV and varicella-zoster virus have been implicated [11]. Thromboembolism Patients with HIV infection tend to develop coagulation abnormalities that cause both arterial and venous thromboses. The incidence of thromboembolic events in HIVinfected patients is reported to be %; the incidence is higher in patients with IDS, opportunistic infections, and malignancy and in those receiving HRT [14] (Fig. 12). Deep vein thrombosis in the lower extremities and pulmonary embolism (Fig. 12) are common [3]. JR:198, February

3 Nakazono et al. Downloaded from by on 02/06/18 from IP address Copyright RRS. For personal use only; all rights reserved Clinical Roles of CT and MRI in the Diagnosis of HIV-Related Cardiovascular Complications Cardiovascular complications in HIV-infected patients include various diseases that frequently overlap or that may coexist. Integrating information regarding clinical findings, medical history, laboratory data including CD4 lymphocyte counts, and imaging findings is important in arriving at an accurate diagnosis. HIV-infected patients with low CD4 lymphocyte counts are reported to have a high risk of dilated cardiomyopathy, endocarditis, myocarditis, pericardial effusion, pericarditis, and HIV-related tumors [3]. Echocardiography is a standard tool for the evaluation and follow-up of cardiac abnormalities and function in HIV-infected patients. If echocardiography is not diagnostic, CT and MRI are helpful for further assessment of cardiovascular complications. HRT has decreased opportunistic infections and cardiomyopathy and has improved mortality dramatically in HIV-infected patients. However, HRT causes side effects such as lipodystrophy, hyperlipidemia, and hyperglycemia and increases the risk of atherosclerosis, CD, myocardial infarction, and thromboembolism in patients with HIV [3]. ECG-gated CT angiography has a high accuracy in the diagnosis of CD. Triple-rule-out CT can simultaneously evaluate for CD, aortic dissection, and pulmonary embolism [15] and may be useful for the assessment of HIV-infected patients with acute chest pain. oth acute myocarditis and myocardial infarction may occur in HIVinfected patients with chest pain, elevated cardiac enzyme levels, and ECG changes. Clinical differentiation between the two entities is difficult but is crucial for optimal clinical management. Late gadolinium-enhanced MR images are helpful for the distinction between myocarditis and myocardial infarction [16]. Conclusion Cardiovascular complications in HIVinfected patients include various diseases and can be life-threatening. CT and MRI are useful for the noninvasive evaluation of these complications. References 1. World Health Organization Website. Global summary of the IDS epidemic: hiv/data/2009_global_summary.png. ccessed December 28, Ho JE, Hsue PY. Cardiovascular manifestations of HIV infection. Heart 2009; 95: Restrepo CS, Diethelm L, Lemos J, et al. Cardiovascular complications of human immunodeficiency virus infection. RadioGraphics 2006; 26: Sani MU. Myocardial disease in human immunodeficiency virus (HIV) infection: a review. Wien Klin Wochenschr 2008; 120: nderson DW, Virmani R, Reilly JM, et al. Prevalent myocarditis at necropsy in the acquired immunodeficiency syndrome. J m Coll Cardiol 1988; 11: Raj V, Joshi S, Pennell DJ. Images in cardiovascular medicine: cardiac magnetic resonance of acute myocarditis in an human immunodeficiency virus patient presenting with acute chest pain syndrome. Circulation 2010; 121: Friis-Møller N, Weber R, Reiss P, et al.; DD Study Group. Cardiovascular disease risk factors in HIV patients: association with antiretroviral therapy results from the DD study. IDS 2003; 17: Nahass RG, Weinstein MP, artels J, Gocke DJ. Infective endocarditis in intravenous drug users: a comparison of human immunodeficiency virus type 1-negative and -positive patients. J Infect Dis 1990; 162: d mati G, di Gioia CR, Gallo P. Pathological findings of HIV-associated cardiovascular disease. nn N Y cad Sci 2001; 946: Mehta NJ, Khan I, Mehta RN, Sepkowitz D. HIV-related pulmonary hypertension: analytic review of 131 cases. Chest 2000; 118: Guillevin L. Vasculitides in the context of HIV infection. IDS 2008; 22(suppl 3):S27 S Olmos JM, Fernández-yala M, Gutierrez J, Val JF, González-Marcias J. Superior vena cava syndrome secondary to syphilitic aneurysm of the ascending aorta in a human immunodeficiency virus infected patient. Clin Infect Dis 1998; 27: Mirza H, Patel P, Suresh K, Krukenkamp I, Lawson WE. HIV disease and an atherosclerotic ascending aortic aneurysm. Rev Cardiovasc Med 2004; 5: Shen YM, Frenkel EP. Thrombosis and a hypercoagulable state in HIV-infected patients. Clin ppl Thromb Hemost 2004; 10: Halpern EJ. Triple-rule-out CT angiography for evaluation of acute chest pain and possible acute coronary syndrome. Radiology 2009; 252: Laissy JP, Hyafil F, Feldman LJ, et al. Differentiating acute myocardial infarction from myocarditis: diagnostic value of early- and delayedperfusion cardiac MR imaging. Radiology 2005; 237: Fig year-old woman with HIV infection, dilated cardiomyopathy, and pulmonary arterial hypertension who had history of IV drug abuse. D, xial contrast-enhanced CT images show dilatation of cardiac chambers, pulmonary arteries, inferior vena cava (IVC), hepatic veins, and coronary sinus (arrow, C). Reflux of contrast medium into IVC and hepatic veins (arrowheads, D) is seen in D. C D 366 JR:198, February 2012

4 CT and MRI of HIV-Related Cardiac Complications Downloaded from by on 02/06/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-old woman with HIV infection and dilated cardiomyopathy. and, xial contrast-enhanced CT images show dilatation of predominantly right cardiac chambers and inferior vena cava (arrow, ), thickening of left ventricular wall, and marked pericardial effusion. Pneumonia is seen in left lower lobe. Fig year-old woman with HIV infection, dilated cardiomyopathy (left ventricular ejection fraction = 25%), and pulmonary arterial hypertension who had history of IV drug abuse and highly active antiretroviral therapy. and, xial contrast-enhanced CT images show dilatation of cardiac chambers with thinning of left ventricular wall and enlargement of pulmonary artery and superior vena cava. ilateral pleural effusions and pulmonary edema are also seen. Fig year-old woman with HIV infection and dilated cardiomyopathy (left ventricular ejection fraction = 15%)., Cine MR image (four-chamber view) obtained in diastole shows dilatation of cardiac chambers, pericardial effusion, and bilateral pleural effusions. Figure S4, cine MRI, can be seen in the JR electronic supplement to this article, available at and presents more detail than the image printed here. Fig year-old man with HIV infection and myocarditis., Short axis STIR MR image shows areas with slightly increased signal intensity (arrows) in myocardium of anterior and inferior walls of left ventricle., Short axis late gadolinium-enhanced MR image shows subepicardial enhancement in inferoseptal wall (arrow). See Figure S5C, cine MRI, which is available at JR:198, February

5 Nakazono et al. Downloaded from by on 02/06/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-old woman with HIV infection, endocarditis, and coronary artery disease who had history of highly active antiretroviral therapy., xial contrast-enhanced CT image shows calcified plaques (arrows) in ascending aorta and left anterior descending artery., Multiplanar image (four-chamber view) shows nodular thickening (arrows) of mitral valve. Thickening is caused by vegetation. Fig year-old man with HIV infection, endocarditis, and coronary artery disease who had history of IV drug abuse and highly active antiretroviral therapy., Coronal multiplanar reformatted contrastenhanced CT image shows vegetation (arrow) adjacent to aortic valve and calcified plaques (arrowhead) in left anterior descending artery (LD)., Curved planar reformatted image shows calcified coronary plaques (arrow) and 70% stenosis of LD. See Figure S6C, cine CT, which is available at www. ajronline.org. Fig year-old man with HIV infection, endocarditis, and mitral regurgitation., Cine MR image obtained during systole shows regurgitant jet (arrow) through mitral valve extending toward left atrium. See cine MRI, Figure S8, which is available at Fig year-old woman with HIV infection and cardiac involvement of malignant lymphoma (urkitt lymphoma). and, xial contrast-enhanced CT images show multiple low-attenuation lesions (arrows), which reflect myocardial involvement of malignant lymphoma in left ventricular wall, and pericardial effusion. C, Short axis STIR MR image shows ill-defined high-signal-intensity lesion (arrow) in anterior wall of left ventricle. C 368 JR:198, February 2012

6 CT and MRI of HIV-Related Cardiac Complications Downloaded from by on 02/06/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-old man with HIV infection, syphilitic aortic aneurysm, and aortic dissection. xial contrast-enhanced CT image shows dilatation of ascending aorta, intimal flap (arrow) in descending aorta, and bilateral pleural effusions. FOR YOUR INFORMTION Fig year-old man with HIV infection and pericardial involvement of non Hodgkin lymphoma. and, xial contrast-enhanced CT image () and coronal maximum-intensity-projection image () show irregular pericardial thickening (arrows), which reflects involvement of malignant lymphoma. Multiple enlarged axillary lymph nodes (arrowheads, ) are seen in. Fig year-old woman with HIV infection, dilated cardiomyopathy, deep vein thrombosis, and pulmonary embolism who had history of highly active antiretroviral therapy. and, Coronal maximum-intensity-projection contrast-enhanced CT images show dilatation of cardiac chambers and filling defects (arrows, ) in both pulmonary arteries. Multiple wedge-shaped lesions (arrowheads) consistent with pulmonary infarctions are seen in both peripheral lungs. data supplement for this article can be viewed in the online version of the article at: JR:198, February