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Stroke Caused by Human Immunodeficiency Virus–Associated Intracranial Large-Vessel Aneurysmal Vasculopathy FREE

Brent Tipping, MBChB; Linda de Villiers, MBChB; Sally Candy, MBChB; Helen Wainwright, MBChB
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Copyright 2006 American Medical Association. All Rights Reserved. Applicable FARS/DFARS Restrictions Apply to Government Use.

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Arch Neurol. 2006;63(11):1640-1642. doi:10.1001/archneur.63.11.1640
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Background  Intracranial aneurysms related to human immunodeficiency virus (HIV) infection have been well described in pediatric patients but not in adults.

Objective  To describe a case of intracranial large-vessel aneurysmal vasculopathy causing stroke in a 27-year-old HIV-infected woman.

Design  Comparison of clinical and histological data with previously published cases.

Setting  A referral hospital stroke unit.

Patient  A 27-year-old HIV-infected woman presenting with stroke; neuroimaging demonstrated fusiform aneurysmal dilation of the left internal carotid and the left middle cerebral artery and its branches.

Results  Autopsy showed degeneration of the elastic lamina, myxoid degeneration, and medial atrophy, causing consequent ectasia of the involved intracranial vessels.

Conclusion  Aneurysmal dilation of the intracranial arteries occurs in HIV-infected adults, but the pathogenic role of HIV remains unknown.

Figures in this Article

Human immunodeficiency virus (HIV) infection is associated with vascular disease and an increased incidence of stroke in adults.1 In addition, childhood HIV–associated intracranial aneurysmal vasculopathy has been described.2 16 This report describes an adult HIV-infected woman who had a cerebral infarct caused by aneurysmal dilatation of the arteries in the circle of Willis. To the best of our knowledge, this is the first description of HIV-associated intracranial aneurysmal vasculopathy in an adult with postmortem histopathology.

A 27-year-old woman with World Health Organization stage IV HIV infection17 and a CD4 count of 14 cells/μL presented with a right hemiparesis. Computed tomography with intravenous contrast (Figure 1A) showed an infarct of the left basal ganglia and fusiform dilation of the left middle and anterior cerebral arteries, as well as the distal basilar artery (Figure 1B). The extracranial carotid and vertebral arteries appeared normal on computed tomography angiography. Cerebrospinal fluid analysis showed a protein level of 1.0 g/L; cerebrospinal fluid glucose level of 41 mg/dL (2.3 mmol/L); blood glucose level of 72 mg/dL (4.0 mmol/L); 7 lymphocytes per cubic millimeter; 3 polymorphs per cubic millimeter; negative cryptococcal latex antigen fixation; negative rapid plasma reagin; and negative culture for bacteria, fungi, and tuberculosis.

Place holder to copy figure label and caption
Figure 1.

A, Contrast-enhanced computed tomography (CT) scan and 3-dimensional reconstruction (B) of the CT angiogram showing fusiform dilation of the left internal carotid artery, left anterior cerebral, and left middle cerebral artery (long arrows), as well as dilation of the tip of the basilar artery (short arrows).

Grahic Jump Location

The patient died of bacterial pneumonia 25 days after her initial presentation.

Cranial autopsy examination showed fusiform dilation of the left internal carotid, and of the left middle cerebral artery and branches (Figure 2). Thrombus was present in the left middle cerebral artery, including the anterior branch. Histological examination of the left internal carotid and middle cerebral arteries showed luminal thrombosis, concentric intimal fibrosis with hyalinization, atrophic media, and fragmentation and thinning of the elastic lamina. Neutrophils were present on the luminal surface related to the thrombus (Figure 3). Arteries on the nonsymptomatic right side had thickened internal elastic lamina with fragmentation and focal intimal proliferation with calcification. The media was preserved. Alcian blue staining of vessels on the right as well as severely affected vessels on the left showed deposition of mucopolysaccharides in the intima and media of the arteries with splaying of the myocytes (Figure 4). No microorganisms or cytopathic changes were observed and immunoperoxidase stains showed moderate numbers of CD68 + macrophages and some CD3 + lymphocytes. Human immunodeficiency virus p24 antigen staining of the vessel sections was negative. Sections of the left caudate infarct showed liquefactive necrosis and perivascular chronic inflammation.

Place holder to copy figure label and caption
Figure 2.

Fusiform dilation of the left internal carotid and the left middle cerebral arteries and its branches (arrows).

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Place holder to copy figure label and caption
Figure 3.

Microscopic examination of left internal carotid artery with intimal hyperplasia, luminal neutrophilic infiltrate, fibrosis, and thickened, beaded internal elastic lamina (arrow) with fragmentation (hematoxylin-eosin, original magnification ×100).

Grahic Jump Location
Place holder to copy figure label and caption
Figure 4.

Microscopic examination of mucopolysaccharide deposition in the intima and media (arrow) with splaying of smooth muscle cells, medial atrophy, and fragmentation of the elastic lamina (Alcian blue, original magnification ×100).

Grahic Jump Location

Fusiform dilation of intracranial arteries has been described in HIV-positive children (32 cases)2 16 and in only 2 studies of HIV-positive adults (5 cases).18 19 Clinical manifestations varied from cerebral infarcts (14 children), transient ischemic attacks (2 adults), intracranial hemorrhages (5 children), subarachnoid hemorrhage (3 adults), seizures (3 children), and movement disorders (3 children). One study reports an incidence of fusiform intracranial artery dilation of 1.9% in 426 HIV-positive children.4

The pathogenesis of intracranial aneurysms in HIV infection is postulated to be caused by immune activation in response to transendothelial migration of HIV strains with tropism for cerebral mononuclear cells,9 and an alteration of dynamic vascular responsiveness to pulsatile blood flow regulated by alterations in circulating cytokines and growth factors leading to vascular remodelling.20 Opportunistic infections associated with HIV that are known to involve vessels—such as varicella-zoster virus, herpes simplex virus, cytomegalovirus, Epstein-Barr virus, Treponema pallidum, Candida albicans, Cryptococcus neoformans, and Mycobacterium tuberculosis—may contribute to the production of these cytokines and growth factors.1 Repeated infections may contribute to an increase in elastases, leading to the fragmentation and thinning of the internal elastic lamina, an early histological finding in the development of fusiform aneurysms.6 ,15 Although it was absent in our patient, HIV glycoprotein 41 has been demonstrated in mononuclear cells within the intima of aneurysmal intracranial arteries in 1 case.12 Extracranial aneurysms in HIV-positive patients are due to vasculitis of the vasa vasora, which are absent in the intracranial arteries, implying that the pathogenesis is different.21

The survival of patients with aneurysmal HIV-associated vasculopathy prior to the availability of highly active antiretroviral therapy was less than 1 year.5 7 ,12 ,15 16 Stabilization of intracranial aneurysms has been reported in 3 patients after 4 months of highly active antiretroviral therapy,9 ,17 and in 1 case of resolution after 15 months of highly active antiretroviral therapy.3 It remains to be seen whether highly active antiretroviral therapy will arrest progression or promote resolution of intracranial aneurysms in adults, thereby confirming the role of HIV in the pathogenesis of intracranial arterial aneurysm formation.

Correspondence: Brent Tipping, MBChB, Institute of Ageing in Africa, Division of Geriatric Medicine, University of Cape Town, L51, Old Main Bldg, Groote Schuur Hospital, Observatory, 7925 Cape Town, South Africa (btipping@mweb.co.za).

Accepted for Publication: May 22, 2006.

Author Contributions:Study concept and design: Tipping and de Villiers. Acquisition of data: Tipping, Candy, and Wainwright. Analysis and interpretation of data: Tipping and Candy. Drafting of the manuscript: Tipping, de Villiers, Candy, and Wainwright. Critical revision of the manuscript for important intellectual content: de Villiers and Candy. Administrative, technical, and material support: Tipping. Study supervision: de Villiers and Candy. Microscopy: Wainwright.

Financial Disclosure: None reported.

Connor  MD, Lammie  GA, Bell  JE, Warlow  CP, Simmonds  P, Brettle  RD. Cerebral infarction in adult AIDS patients: observations from the Edinburgh HIV autopsy cohort. Stroke 2000;312117- 2126
PubMed
Dubrovsky  T, Curless  R, Scott  G.  et al.  Cerebral aneurysmal arteriopathy in childhood AIDS. Neurology 1998;51560- 565
PubMed
Martinez-Longoria  CA, Morales-Aguirre  JJ, Villalobos-Acosta  CP, Gomez-Barreto  D, Cashat-Cruz  M. Occurrence of intracerebral aneurysm in an HIV-infected child: a case report. Pediatr Neurol 2004;31130- 132
PubMed
Patsalides  AD, Wood  LV, Atac  GK, Sandifer  E, Butman  JA, Patronas  NJ. Cerebrovascular disease in HIV-infected pediatric patients: neuroimaging findings. AJR Am J Roentgenol 2002;179999- 1003
PubMed
Philippet  P, Blanche  S, Sebag  G, Rodesch  G, Griscelli  C, Tardieu  M. Stroke and cerebral infarcts in children infected with human immunodeficiency virus. Arch Pediatr Adolesc Med 1994;148965- 970
PubMed
Shah  SS, Zimmerman  RA, Rorke  LB, Vezina  LG. Cerebrovascular complications of HIV in children. AJNR Am J Neuroradiol 1996;171913- 1917
PubMed
Park  YD, Belman  AL, Kim  TS.  et al.  Stroke in pediatric acquired immunodeficiency syndrome. Ann Neurol 1990;28303- 311
PubMed
Husson  RN, Saini  R, Lewis  LL, Butler  KM, Patronas  N, Pizzo  PA. Cerebral artery aneurysms in children infected with human immunodeficiency virus. J Pediatr 1992;121927- 930
PubMed
Mazzoni  P, Chiriboga  CA, Millar  WS, Rogers  A. Intracerebral aneurysms in human immunodeficiency virus infection: case report and literature review. Pediatr Neurol 2000;23252- 255
PubMed
Fulmer  BB, Dillard  SC, Musulman  EM, Palmer  CA, Oakes  J. Two cases of cerebral aneurysms in HIV+ children. Pediatr Neurosurg 1998;2831- 34
PubMed
Visrutaratna  P, Oranratanachai  K. HIV encephalopathy and cerebral aneurysmal arteriopathy. Singapore Med J 2002;43377- 380
PubMed
Kure  K, Park  YD, Kim  TS.  et al.  Immunohistochemical localization of an HIV epitope in cerebral aneurysmal arteriopathy in pediatric acquired immunodeficiency syndrome (AIDS). Pediatr Pathol 1989;9655- 667
PubMed
Carvalho Neto  AD, Bruck  I, Coelho  LO.  et al.  Cerebral arterial aneurysm in a child with acquired immunodeficiency syndrome: case report. Arq Neuropsiquiatr 2001;59444- 448
PubMed
Bonkowsky  JL, Christenson  JC, Nixon  GW, Pavia  AT. Cerebral aneurysms in a child with acquired immune deficiency syndrome during rapid immune reconstitution. J Child Neurol 2002;17457- 460
PubMed
Bulsara  KR, Raja  A, Owen  J. HIV and cerebral aneurysms. Neurosurg Rev 2005;2892- 95
PubMed
Nunes  ML, Pinho  AP, Sfoggia  A. Cerebral aneurysmal dilatation in an infant with perinatally acquired HIV infection and HSV encephalitis. Arq Neuropsiquiatr 2001;59116- 118
PubMed
World Health Organization,  Interim proposal for a WHO Staging System for HIV infection and disease. Weekly Epidemiological Record 1990;65221- 224
Berkefeld  J, Enzensberger  W, Lanfermann  H. MRI in human immunodeficiency virus-associated cerebral vasculitis. Neuroradiology 2000;42526- 528
PubMed
Taylor  A, LeFeuvre  D, Levy  A, Candy  S. Arterial dissection and subarachnoid haemorrhage in human immunodeficiency virus–infected patients: a report of three cases. Intervent Neuroradiol 2004;10137- 144
Krizanac-Bengez  L, Mayberg  MR, Janigro  D. The cerebral vasculature as a therapeutic target for neurological disorders and the role of shear stress in vascular homeostatis and pathophysiology. Neurol Res 2004;26846- 853
PubMed
Chetty  R, Batitang  S, Nair  R. Large artery vasculopathy in HIV-positive patients: another vasculitic enigma. Hum Pathol 2000;31374- 379
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

A, Contrast-enhanced computed tomography (CT) scan and 3-dimensional reconstruction (B) of the CT angiogram showing fusiform dilation of the left internal carotid artery, left anterior cerebral, and left middle cerebral artery (long arrows), as well as dilation of the tip of the basilar artery (short arrows).

Grahic Jump Location
Place holder to copy figure label and caption
Figure 2.

Fusiform dilation of the left internal carotid and the left middle cerebral arteries and its branches (arrows).

Grahic Jump Location
Place holder to copy figure label and caption
Figure 3.

Microscopic examination of left internal carotid artery with intimal hyperplasia, luminal neutrophilic infiltrate, fibrosis, and thickened, beaded internal elastic lamina (arrow) with fragmentation (hematoxylin-eosin, original magnification ×100).

Grahic Jump Location
Place holder to copy figure label and caption
Figure 4.

Microscopic examination of mucopolysaccharide deposition in the intima and media (arrow) with splaying of smooth muscle cells, medial atrophy, and fragmentation of the elastic lamina (Alcian blue, original magnification ×100).

Grahic Jump Location

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Connor  MD, Lammie  GA, Bell  JE, Warlow  CP, Simmonds  P, Brettle  RD. Cerebral infarction in adult AIDS patients: observations from the Edinburgh HIV autopsy cohort. Stroke 2000;312117- 2126
PubMed
Dubrovsky  T, Curless  R, Scott  G.  et al.  Cerebral aneurysmal arteriopathy in childhood AIDS. Neurology 1998;51560- 565
PubMed
Martinez-Longoria  CA, Morales-Aguirre  JJ, Villalobos-Acosta  CP, Gomez-Barreto  D, Cashat-Cruz  M. Occurrence of intracerebral aneurysm in an HIV-infected child: a case report. Pediatr Neurol 2004;31130- 132
PubMed
Patsalides  AD, Wood  LV, Atac  GK, Sandifer  E, Butman  JA, Patronas  NJ. Cerebrovascular disease in HIV-infected pediatric patients: neuroimaging findings. AJR Am J Roentgenol 2002;179999- 1003
PubMed
Philippet  P, Blanche  S, Sebag  G, Rodesch  G, Griscelli  C, Tardieu  M. Stroke and cerebral infarcts in children infected with human immunodeficiency virus. Arch Pediatr Adolesc Med 1994;148965- 970
PubMed
Shah  SS, Zimmerman  RA, Rorke  LB, Vezina  LG. Cerebrovascular complications of HIV in children. AJNR Am J Neuroradiol 1996;171913- 1917
PubMed
Park  YD, Belman  AL, Kim  TS.  et al.  Stroke in pediatric acquired immunodeficiency syndrome. Ann Neurol 1990;28303- 311
PubMed
Husson  RN, Saini  R, Lewis  LL, Butler  KM, Patronas  N, Pizzo  PA. Cerebral artery aneurysms in children infected with human immunodeficiency virus. J Pediatr 1992;121927- 930
PubMed
Mazzoni  P, Chiriboga  CA, Millar  WS, Rogers  A. Intracerebral aneurysms in human immunodeficiency virus infection: case report and literature review. Pediatr Neurol 2000;23252- 255
PubMed
Fulmer  BB, Dillard  SC, Musulman  EM, Palmer  CA, Oakes  J. Two cases of cerebral aneurysms in HIV+ children. Pediatr Neurosurg 1998;2831- 34
PubMed
Visrutaratna  P, Oranratanachai  K. HIV encephalopathy and cerebral aneurysmal arteriopathy. Singapore Med J 2002;43377- 380
PubMed
Kure  K, Park  YD, Kim  TS.  et al.  Immunohistochemical localization of an HIV epitope in cerebral aneurysmal arteriopathy in pediatric acquired immunodeficiency syndrome (AIDS). Pediatr Pathol 1989;9655- 667
PubMed
Carvalho Neto  AD, Bruck  I, Coelho  LO.  et al.  Cerebral arterial aneurysm in a child with acquired immunodeficiency syndrome: case report. Arq Neuropsiquiatr 2001;59444- 448
PubMed
Bonkowsky  JL, Christenson  JC, Nixon  GW, Pavia  AT. Cerebral aneurysms in a child with acquired immune deficiency syndrome during rapid immune reconstitution. J Child Neurol 2002;17457- 460
PubMed
Bulsara  KR, Raja  A, Owen  J. HIV and cerebral aneurysms. Neurosurg Rev 2005;2892- 95
PubMed
Nunes  ML, Pinho  AP, Sfoggia  A. Cerebral aneurysmal dilatation in an infant with perinatally acquired HIV infection and HSV encephalitis. Arq Neuropsiquiatr 2001;59116- 118
PubMed
World Health Organization,  Interim proposal for a WHO Staging System for HIV infection and disease. Weekly Epidemiological Record 1990;65221- 224
Berkefeld  J, Enzensberger  W, Lanfermann  H. MRI in human immunodeficiency virus-associated cerebral vasculitis. Neuroradiology 2000;42526- 528
PubMed
Taylor  A, LeFeuvre  D, Levy  A, Candy  S. Arterial dissection and subarachnoid haemorrhage in human immunodeficiency virus–infected patients: a report of three cases. Intervent Neuroradiol 2004;10137- 144
Krizanac-Bengez  L, Mayberg  MR, Janigro  D. The cerebral vasculature as a therapeutic target for neurological disorders and the role of shear stress in vascular homeostatis and pathophysiology. Neurol Res 2004;26846- 853
PubMed
Chetty  R, Batitang  S, Nair  R. Large artery vasculopathy in HIV-positive patients: another vasculitic enigma. Hum Pathol 2000;31374- 379
PubMed

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