Virus vasculopathy and stroke: An under-recognized cause and treatment target

Infectious Disorders - Drug Targets

Volumn 10, Issue 2, 2010, Pages 105-111

  Nagel, M A ^a   Mahalingam, R ^a   Cohrs, R J ^a   Gilden, D ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

CMV; HIV; Virus vasculopathy; VZV

Indexed keywords

ACETYLSALICYLIC ACID; ACICLOVIR; ANTIVIRUS AGENT; GANCICLOVIR; IMMUNOGLOBULIN G ANTIBODY; PREDNISONE; VALACICLOVIR;

ARTERY DISSECTION; ARTICLE; BLEEDING; BRAIN HEMORRHAGE; CEREBROSPINAL FLUID; CHICKENPOX; CLINICAL FEATURE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DIABETES MELLITUS; DRUG TARGETING; HERPES ZOSTER; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERTENSION; INFECTION; NONHUMAN; PATHOGENESIS; PRIMARY INFECTION; STROKE; TRANSIENT ISCHEMIC ATTACK; VARICELLA ZOSTER VIRUS;

EID: 77958076261     PISSN: 18715265     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152610790963537     Document Type: Article

References (81)

1. Lloyd-Jones, D.; Adams, R.; Carnethon, M.; De Simone, G.; Ferguson, T.B.; Flegal, K.; Ford, E.; Furie, K.; Go, A.; Greenlund, K.; Haase, N.; Hailpern, S.; Ho, M.; Howard, V.; Kissela, B.; Kittner, S.; Lackland, D.; Lisabeth, L.; Marelli, A.; McDermott, M.; Meigs, J.; Mozaffarian, D.; Nichol, G.; O'Donnell, C.; Roger, V.; Rosamond, W.; Sacco, R.; Sorlie, P.; Stafford, R.; Steinberger, J.; Thom, T.; Wasserthiel-Smoller, S.; Wong, N.; Wylie-Rosett, J.; Hong, Y.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics - 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation, 2009, 119, 480-486.
2. Gilden, D.H.; Kleinschmidt-DeMasters, B.K.; Wellish, M.; Hedley-Whyte, E.T.; Rentier, B.; Mahalingam, R. Varicella zoster virus, a cause of waxing and waning vasculitis: The New England Journal of Medicine case 5-1995 revisited. Neurology, 1996, 47, 1441-1446.
3. Hyman, R.W.; Ecker, J.R.; Tenser, R.B. Varicella-zoster virus RNA in human trigeminal ganglia. Lancet, 1983, 2, 814-816.
4. Gilden, D.H.; Vafai, A.; Shtram, Y.; Becker, Y.; Devlin, M.; Wellish, M. Varicella-zoster virus DNA in human sensory ganglia. Nature, 1983, 306, 478-480.
5. Gilden, D.H.; Rozenman, Y.; Murray, R.; Devlin, M.; Vafai, A. Detection of varicella-zoster virus nucleic-acid in neurons of normal human thoracic ganglia. Ann. Neurol., 1987, 22, 377-380.
6. Gilden, D.H.; Gesser, R.; Smith, J.; Wellish, M.; LaGuardia, J.J.; Cohrs, R.J.; Mahalingam. R. Presence of VZV and HSV-1 DNA in human nodose and celiac ganglia. Virus Genes, 2001, 23, 145-147.
7. Mahalingam, R.; Wellish, M.; Wolf, W.; Dueland, A.N.; Cohrs, R.; Vafai, A.; Gilden, D.H. Latent varicella zoster virus DNA in human trigeminal and thoracic ganglia. N. Engl. J. Med., 1990, 323, 627-631.
8. LaGuardia, J.J.; Cohrs, R.J.; Gilden, D.H. Prevalence of varicellazoster virus DNA in dissociated human trigeminal ganglion neurons and non-neuronal cells. J. Virol., 1999, 73, 8571-8577.
9. Miller, A.E. Selective decline in cellular immune-response to varicella-zoster in the elderly. Neurology, 1980, 30, 582-587.
10. Berger, R.; Florent, G.; Just, M. Decrease of the lymphoproliferative response to varicella-zoster virus-antigen in the aged. Infect. Immun., 1981, 32, 24-27.
11. Hayward, A.R.; Herberger, M. Lymphocyte-responses to varicella zoster virus in the eldery. J. Clin. Immunol., 1987, 7, 174-178.
12. Hayward, A.; Levin, M.; Wolf, W.; Angelova, G.; Gilden, D. Varicella-zoster virus specific immunity after herpes zoster. J. Infect. Dis., 1991, 163, 873-875.
13. Holland, G.N. The progressive outer retinal necrosis syndrome. Int. Ophthalmol., 1994, 18, 163-165.
14. Gilden, D.H.; Beinlich, B.R.; Rubinstien, E.M.; Stommel, E.; Swenson, R.; Rubinstein, D.; Mahalingam, R. Varicella-zoster virus myelitis: an expanding spectrum. Neurology, 1994, 44, 1818-1823.
15. Nagel, M.A.; Cohrs, R.J.; Mahalingam, R.; Wellish, M.C.; Forghani, F.; Schiller, A.; Safdieh, J.E.; Kamenkovich, E.; Ostrow, L.W.; Levy, M.; Greenberg, B.; Russman, A.N.; Katzan, I.; Gardner, C.J.; Häusler, M.; Nau, R.; Saraya, T.; Wada, H.; Goto, H.; de Martino, M.; Ueno, M.; Brown, W.D.; Terborg, C.; Gilden, D.H. The varicella zoster virus vasculopathies: clinical, CSF, imaging and virological features. Neurology, 2008, 70, 853-860.
16. Gilden, D.H.; Dueland, A.N.; Cohrs, R.; Martin, J.R.; Kleinschmidt-DeMasters, B.K.; Mahalingam, R. Preherpetic neuralgia. Neurology, 1991, 41, 1215-1218.
17. Gilden, D.H.; Wright, R.R.; Schneck, S.A.; Gwaltney Jr., J.M.; Mahalingam, R. Zoster sine herpete, a clinical variant. Ann. Neurol., 1994, 35, 530-533.
18. Askalan, R.; Laughlin, S.; Mayank, S.; Chan, A.; MacGregor, D.; Andrew, M.; Curtis, R.; Meaney, B.; deVeber, G. Chickenpox and stroke in childhood: a study of frequency and causation. Stroke, 2001, 32, 1257-1262.
19. Amlie-Lefond, C.; Bernard, T.J.; Sébire, G.; Friedman, N.R.; Heyer, G.L.; Lerner, N.B.; DeVeber, G.; Fullerton, H.J.; International Pediatric Stroke Study Group. Predictors of cerebral arteriopathy in children with arterial ischemic stroke: results of the International Pediatric Stroke Study. Circulation, 2009, 119, 1417-1423.
20. Braun, K.P.; Bulder, M.M.; Chabrier, S.; Kirkham, F.J.; Ulterwaal, C.S.; Tardieu, M.; Sébire, G. The course and outcome of unilateral intracranial arteriopathy in 79 children with ischaemic stroke. Brain, 2009, 132, 544-557.
21. Petito, C.K.; Cho, E.S.; Lemann, W.; Navia, B.A.; Price, R.W. Neuropathology of acquired immunodeficiency syndrome (AIDS): an autopsy review. J. Neuropathol. Exp. Neurol., 1986, 45, 635-646.
22. Gray, F.; Mohr, M.; Rozenberg, F.; Bélec, L.; Lescs, M.C.; Dournon, E.; Sinclair, E.; Scaravilli, F. Varicella-zoster virus encephalitis in acquired immunodeficiency syndrome: report of four cases. Neuropathol. Appl. Neurobiol., 1992, 18, 502-514.
23. Gray, F.; Bélec, L.; Lescs, M.C.; Chrétien, F.; Ciardi, A.; Hassine, D.; Flament-Saillour, M.; de Truchis, P.; Clair, B.; Scaravilli, F. Varicella-zoster virus infection of the central nervous system in the acquired immune deficiency syndrome. Brain, 1994, 117, 987-999.
24. Ryder, J.W.; Croen, K.; Kleinschmidt-DeMasters, B.K.; Ostrove, J.M.; Straus, S.E.; Cohn, D.L. Progressive encephalitis three months after resolution of cutaneous zoster in a patient with AIDS. Ann. Neurol., 1986, 19, 182-188.
25. Morgello, S.; Block, G.A.; Price, R.W.; Petito, C.K. Varicellazoster virus leukoencephalitis and cerebral vasculopathy. Arch. Pathol. Lab. Med., 1988, 112, 173-177.
26. Reshef, E.; Greenberg, S.B.; Jankovic, J. Herpes zoster ophthalmicus followed by contralateral hemiparesis: report of two cases adn review of literature. J. Neurol. Neurosurg. Psychiatry, 1985, 48, 122-127.
27. Hall, S.; Carlin, L.; Roach, E.S.; McLean Jr., W.T. Herpes zoster and central retinal artery occlusion. Ann. Neurol., 1983, 13, 217-218.
28. Gilden, D.H.; Lipton, H.L.; Wolf, J.S.; Akenbrandt, W.; Smith, J.E.; Mahalingam, R.; Forghani, B. Two patients with unusual forms of varicella-zoster virus vasculopathy. N. Engl. J. Med., 2002, 347, 1500-1503.
29. Gilden, D.H.; Mahalingam, R.; Cohrs, R.J.; Kleinschmidt-DeMasters, B.K., Forghani, B. The protean manifestations of varicella-zoster virus vasculopathy. J. Neurovirol., 2002, 8, 75-79.
30. Russman, A.N.; Lederman, R.J.; Calabrese, L.H.; Embi, P.J.; Forghani, B.; Gilden, D.H. Multifocal varicella-zoster virus vasculopathy without rash. Arch. Neurol., 2003, 60, 1607-1609.
31. Burgoon, M.P.; Hammack, B.N.; Owens, G.P.; Maybach, A.L.; Eikelenboom, M.J.; Gilden, D.H. Oligoclonal immunoglobulins in cerebrospinal fluid during varicella zoster virus (VZV) vasculopathy are directed against VZV. Ann. Neurol., 2003, 54, 459-563.
32. Nagel, M.A.; Forghani, B.; Mahalingam, R.; Wellish, M.C.; Cohrs, R.J.; Russman, A. N.; Katzan, I.; Lin, R.; Gardner, C.J.; Gilden, D.H. The value of detecting anti-VZV antibody in CSF to diagnose VZV vasculopathy. Neurology, 2007, 68, 1069-1073.
33. Mayberg, M.; Langer, R.S.; Zervas, N.T.; Moskowitz, M.A. Perivascular meningeal projections from cat trigeminal ganglia: possible pathway for vascular headaches in man. Science, 1981, 213, 228-230.
34. Mayberg, M.R.; Zervas, N.T.; Moskowitz, M.A. Trigeminal projections to supratentorial pial and dural blood vessels in cats demonstrated by horseradish peroxidase histochemistry. J. Comp. Neurol., 1984, 223, 46-56.
35. Saito, K.; Moskowitz, M.A. Contributions from the upper cervical dorsal roots and trigeminal ganglia to the feline circle of Willis. Stroke, 1989, 20, 524-526.
36. Linnemann Jr., C.C.; Alvira, M.M. Pathogenesis of varicella-zoster angiitis in the CNS. Arch. Neurol., 1980, 37, 239-240.
37. Doyle, P.W.; Gibson, G.; Dolman, C.L. Herpes zoster ophthalmicus with contralateral hemiplegia: identification of cause. Ann. Neurol., 1983, 14, 84-85.
38. Eidelberg, D.; Sotrel, A.; Horoupian, D.S.; Neumann, P.E.; Pumarola-Sune, T.; Price, R.W. Thrombotic cerebral vasculopathy associated with herpes zoster. Ann. Neurol., 1986, 19, 7-14.
39. Amlie-Lefond, C.; Kleinschmidt-DeMasters, B.K.; Mahalingam, R.; Davis, L.E.; Gilden, D.H. The vasculopathy of varicella-zoster virus encephalitis. Ann. Neurol., 1995, 37, 784-790.
40. Melanson, M.; Chalk, C.; Georgevich, L.; Fett, K., Lapierre, Y.; Duong, H.; Richardson, J.; Marineau, C.; Rouleau, G.A. Varicellazoster virus DNA in CSF and arteries in delayed contralateral hemiplegia: evidence for viral invasion of cerebral arteries. Neurology, 1996, 47, 569-570.
41. Kleinschmidt-DeMasters, B.K.; Mahalingam, R.; Shimek, C.; Marcoux, H.L.; Wellish, M.; Tyler, K.L.; Gilden, D.H. Profound cerebrospinal fluid pleocytosis and Froin's Syndrome secondary to widespread necrotizing vasculitis in an HIV-positive patient with varicella zoster virus encephalomyelitis. J. Neurol. Sci., 1998, 159, 213-218.
42. Gilden, D.; Cohrs, R.J.; Mahalingam, R.; Nagel, M.A. Varicella zoster virus vasculopathies: diverse clinical manifestations, laboratory features, pathogenesis, and treatment. Lancet Neurol., 2009, 8, 731-740.
43. Manco-Johnson, M.J.; Nuss, R.; Key, N.; Moertel, C.; Jacobson, L.; Meech, S.; Weinberg, A.; Lefkowitz, J. Lupus anticoagulant and protein S deficiency in children with postvaricella purpura fulminans or thrombosis. J. Pediatr., 1996, 128, 319-323.
44. Josephson, C.; Nuss, R.; Jacobson, L.; Hacker, M.R.; Murphy, J.; Weinberg, A.; Manco-Johnson, M.J. The varicella-autoantibody syndrome. Pediatr. Res., 2001, 50, 345-352.
45. Kurugöl, Z.; Vardar, F.; Ozkinay, F.; Kavakli, K.; Cetinkaya, B.; Ozkinay, C. Lupus anticoagulant and protein S deficiency in a child who developed disseminated intravascular coagulation in association with varicella. Turk. J. Pediatr., 2001, 43, 139-142.
46. Regnault, V.; Boehlen, F.; Ozsahin, H.; Wahl, D.; de Grott, P.G.; Lecompte, T.; de Moerloose, P. Anti-protein S antibodies following a varicella infection: detection, characterization and influence on thrombin generation. J. Thromb. Haemost., 2005, 3, 1243-1249.
47. Massano, J.; Ferreira, D.; Toledo, T.; Mansilha, A.; Azevedo, E.; Carvalho, M. Stroke and multiple peripheral thrombotic events in an adult with varicella. Eur. J. Neurol., 2008, 15, e90-1.
48. Reeves, M.; Sinclair, J. Aspects of human cytomegalovirus latency and reactivation. Curr. Top. Microbiol. Immunol., 2008, 325, 297-313.
49. Weill, D. Role of cytomegalovirus in cardiac allograft vasculopathy. Transpl. Infect. Dis., 2001, 2 (Suppl. 3), 44-48.
50. Potena, L.; Valantine, H.A. Cytomegalovirus-associated allograft rejection in heart transplant patients. Curr. Opin. Infect. Dis., 2007, 20, 425-31.
51. Melnick, J.L.; Petrie, B.L.; Dreesman, G.R.; Burek, J.; McCollum, C.H.; DeBakey, M.E. Cytomegalovirus antigen within human arterial smooth muscle cells. Lancet, 1983, 2, 644-647.
52. Adam, E.; Melnick, J.L.; Probtsfield, J.L.; Petrie, B.L.; Burek, J.; Bailey, K.R.; McCollum, C.H.; DeBakey, M.E. High levels of cytomegalovirus antibody in patients requiring vascular surgery for atherosclerosis. Lancet, 1987, 2, 291-293.
53. Hendrix, M.G.; Salimans, M.M.; van Boven, C.P.; Bruggeman, C.A. High prevalence of latently present cytomegalovirus in arterial walls of patients suffering from grade III atherosclerosis. Am. J. Pathol., 1990, 136, 23-28.
54. Burns, L.J.; Pooley, J.C.; Walsh, D.J.; Vercellotti, G.M.; Weber, M.L.; Kovacs, A. Intercellular adhesion molecule-1 expression in endothelial cells is activated by cytomegalovirus immediate early proteins. Transplantation, 1999, 67, 137-144.
55. Dengler, T.J.; Raftery, M.J.; Werle, M.; Zimmermann, R.; Schonrich, G. Cytomegalovirus infection of vascular cells induces expression of pro-inflammatory adhesion molecules by paracrine action of secreted interleukin-1beta. Transplantation, 2000, 69, 1160-1168.
56. Qiu, H.; Straat, K.; Rahbar, A.; Wan, M.; Soderberg-Naucler, C.;Haeggstrom, J.Z. Human CMV infection induces 5-lipoxygenase expression and leukotriene B4 production in vascular smooth muscle cells. J. Exp. Med., 2008, 205, 19-24.
57. Espinola-Klein, C.; Rupprecht, H.J.; Blankenberg, S.; Bickel, C.; Kopp, H.; Rippin, G.; Hafner, G.; Pfeifer, U.; Meyer, J. Are morphological or functional changes in the carotid artery wall associated with Chlamydia pneumoniae, Helicobacter pylori, cytomegalovirus, or herpes simplex virus infection? Stroke, 2000, 31, 2127-2133.
58. Ridker, P.M.; Hennekens, C.H.; Stampfer, M.J.; Wang, F. Prospective study of herpes simplex virus, cytomegalovirus, and the risk of future myocardial infarction and stroke. Circulation, 1998, 98, 2796-2799.
59. Voisard, R.; Krugers, T.; Reinhardt, B.; Vaida, B.; Baur, R.; Herter, T.; Luske, A.; Weckermann, D.; Weingartner, K.; Rossler, W.; Hombach, V.; Mertens, T. HCMV-infection in a human arterial organ culture model: effects on cell proliferation and neointimal hyperplasia. BMC Microbiol., 2007, 7, 68.
60. Reinhardt, B.; Vaida, B.; Voisard, R.; Keller, L.; Breul, J.; Metzger, H.; Herter, T.; Baur, R.; Lüske, A.; Mertens, T. Human cytomegalovirus infection in human renal arteries in vitro. J. Virol. Methods, 2003, 109, 1-9.
61. Connor, M.D.; Lammie, G.A.; Bell, J.E.; Warlow, C.P.; Simmonds, P.; Brettle, R.D. Cerebral infarction in adult AIDS patients: observations from the Edinburgh HIV Autopsy Cohort. Stroke, 2000, 31, 2117-2126.
62. Cole, J.W.; Pinto, A.N.; Hebel, J.R.; Buchholz, D.W.; Earley, C.J.; Johnson, C.J.; Macko, R.F.; Price, T.R.; Sloan, M.A.; Stern, B.J.; Wityk, R.J.; Wozniak, M.A.; Kittner, S.J. Acquired immunodeficiency syndrome and the risk of stroke. Stroke, 2004, 35, 51-56.
63. Tipping, B.; de Villiers, L.; Wainwright, H.; Candy, S.; Bryer, A. Stroke in patients with human immunodeficiency virus infection. J. Neurol. Neurosurg. Psychiatry, 2007, 78, 1320-1324.
64. Park, Y.D.; Belman, A.L.; Kim, T.S.; Kure, K.; Llena, J.F.; Lantos, G.; Bernstein, L.; Dickson, D.W. Stroke in pediatric acquired immunodeficiency syndrome. Ann. Neurol., 1990, 28, 303-311.
65. Leeuwis, J.W.; Wolfs, T.F.W.; Braun, K.P.J. A child with HIVassociated transient cerebral arteriopathy. AIDS, 2007, 21, 1383-1393.
66. Bhagavati, S.; Choi, J. Rapidly progressive cerebrovascular stenosis and recurrent strokes followed by improvement in HIV vasculopathy. Cerebrovasc. Dis., 2008, 26, 449-452.
67. Cutfield, N.J.; Steele, H.; Wilhelm, T.; Weatherall, M.W. Successful treatment of HIV associated cerebral vasculopathy with HAART. J. Neurol. Neurosurg. Psychiatry, 2009, 80, 936-937.
68. Modi, G.; Ranchod, K.; Modi, M.; Mochan, A. Human immunodeficiency virus associated intracranial aneurysms: report of three adult patients with an overview of the literature. J. Neurol. Neurosurg. Psychiatry, 2008, 79, 44-46.
69. Kure, K.; Park, Y.D.; Kim, T.S.; Lyman, W.D.; Lantos, G.; Lee, S.; Cho, S.; Belman, A.L.; Weidenheim, K.M.; Dickson, D.W. Immunohistochemical localization of an HIV epitope in cerebral aneurysmal arteriopathy in pediatric acquired immunodeficiency syndrome (AIDS). Pediatr. Pathol., 1989, 9, 655-667.
70. Tipping, B.; de Villiers, L.; Candy, S.; Wainwright, H. Stroke caused by human immunodeficiency virus-associated intracranial large-vessel aneurismal vasculopathy. Arch. Neurol., 2006, 63, 1640-1642.
71. Gilden, D.H.; Nagel, M. Stroke caused by human immunodeficiency virus-associated vasculopathy. Arch. Neurol., 2007, 64, 763.
72. Kossorotoff, M.; Touze, E.; Godon-Hardy, S.; Serre, I.; Mateus, C.; Mas, J.L.; Zuber, M. Cerebral vasculopathy with aneurysm formation in HIV-infected young adults. Neurology, 2006, 66, 1121-1122.
73. Gilden, D.H.; Nagel, M.A. Cerebral vasculopathy with aneurysm formation in HIV-infected young adults. Neurology, 2006, 67, 2089.
74. Henry, K.; Melroe, H.; Huebsch, J.; Hermundson, J.; Levine, C.; Swensen, L.; Daley, J. Severe premature coronary artery disease with protease inhibitors. Lancet, 1998, 351,1328.
75. Hsue, P.Y.; Giri, K.; Erickson, S.; MacGregor, J.S.; Younes, N.; Shergill, A.; Waters, D.D. Clinical features of acute coronary syndromes in patients with human immunodeficiency virus infection. Circulation, 2004, 109, 316-319.
76. Bobryshev, Y.V. Identification of HIV-1 in the aortic wall of AIDS patients. Atherosclerosis, 2000, 152, 529-530.
77. Goldberg, S.H.; van der, M.P.; Hesselgesser, J.; Jaffer, S.; Kolson, D.L.; Albright, A.V.; Gonzalez-Scarano, F.; Lavi, E. CXCR3 expression in human central nervous system diseases. Neuropathol. Appl. Neurobiol., 2001, 27, 127-138.
78. Eugenin, E.A.; Morgello, S.; Klotman, M.E.; Mosoian, A.; Lento, P.A.; Berman, J.W.; Schecter, A.D. Human immunodeficiency virus (HIV) infects human arterial smooth muscle cells in vivo and in vitro: implications for the pathogenesis of HIV-mediated vascular disease. Am. J. Pathol., 2008, 172, 1100-1111.
79. Barbaro, G.; Barbarini, G.; Pellicelli, AM. HIV-associated coronary arteritis in a patient with fatal myocardial infarction. N. Engl. J. Med., 2001, 344, 1799-1800.
80. Tinkle, B.T.; Ngo, L.; Luciw, P.A.; Maciag, T.; Jay, G. Human immunodeficiency virus-associated vasculopathy in transgenic mice. J. Virol., 1997, 71, 4809-4814.
81. Mujawar, Z.; Rose, H.; Morrow, M.P.; Pushkarsky, T.; Dubrovsky, L.; Mukhamedova, N.; Fu, Y.; Dart, A.; Orenstein, J.M.; Bobryshev, Y.V.; Bukrinsky, M.; Sviridov, D. Human immunodeficiency virus impairs reverse cholesterol transport from macrophages. PLoS Biol., 2006, 4, e365.