Progressive multifocal leukoencephalopathy and JC Virus-related disease in modern neurology practice

Multiple Sclerosis and Related Disorders

Volumn 3, Issue 4, 2014, Pages 419-430

  Carruthers, Robert L ^a,b   Berger, Joseph ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

JCV; JCV serology; Multiple sclerosis; Natalizumab; PML IRIS; Progressive multifocal leukoencephalopathy

Indexed keywords

FINGOLIMOD; FUMARIC ACID DIMETHYL ESTER; MIRTAZAPINE; NATALIZUMAB; RITUXIMAB; STEROID;

CD4 CD8 RATIO; CLINICAL FEATURE; DIAGNOSTIC IMAGING; DIFFERENTIAL DIAGNOSIS; DISEASE ASSOCIATION; DNA VIRUS INFECTION; DRUG EFFICACY; DRUG MONITORING; DRUG SAFETY; HIGH RISK PATIENT; HUMAN; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNOADSORPTION; IMMUNOSURVEILLANCE; INCIDENCE; INFECTION PREVENTION; INFECTION RISK; JC VIRUS INFECTION; LYMPHOCYTOPENIA; MEDICAL PRACTICE; MULTIPLE SCLEROSIS; NEUROTROPISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PLASMAPHERESIS; PROGNOSIS; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; RELAPSE; REVIEW; RISK ASSESSMENT; VIRUS PATHOGENESIS; VIRUS REPLICATION;

EID: 84902458735     PISSN: 22110348     EISSN: 22110356     Source Type: Journal    
DOI: 10.1016/j.msard.2014.01.005     Document Type: Review

References (93)

1. A. Antinori, A. Cingolani, P. Lorenzini, M.L. Giancola, I. Uccella, and S. Bossolasco et al. Clinical epidemiology and survival of progressive multifocal leukoencephalopathy in the era of highly active antiretroviral therapy: data from the Italian Registry Investigative Neuro AIDS (IRINA) J Neurovirol 9 Suppl 1 2003 S47 S53
2. C. Antoniol, S. Jilek, M. Schluep, N. Mercier, M. Canales, and G. Le Goff et al. Impairment of JCV-specific T-cell response by corticotherapy: effect on PML-IRIS management? Neurology 79 2012 2258 2264
3. I. Ayzenberg, C. Lukas, N. Trampe, R. Gold, and K. Hellwig Value of MRI as a surrogate marker for PML in natalizumab long-term therapy J Neurol 259 2012 1732 1733
4. A. dArminio Monforte, P. Cinque, A. Mocroft, F.D. Goebel, F. Antunes, and C. Katlama et al. Changing incidence of central nervous system diseases in the EuroSIDA cohort Ann Neurol 55 2004 320 328
5. J. Berenguer, P. Miralles, J. Arrizabalaga, E. Ribera, F. Dronda, and J. Baraia-Etxaburu et al. Clinical course and prognostic factors of progressive multifocal leukoencephalopathy in patients treated with highly active antiretroviral therapy Clin Infect Dis 36 2003 1047 1052
6. J.R. Berger Steroids for PML-IRIS. A double-edged sword? Neurology 2009
7. J.R. Berger, A.J. Aksamit, D.B. Clifford, L. Davis, I.J. Koralnik, and J.J. Sejvar et al. PML diagnostic criteria: consensus statement from the AAN neuroinfectious disease section Neurology 80 2013 1430 1438
8. J.R. Berger, S.A. Houff, J.A. Gurwell, N. Vega, C.S. Miller, and R.J. Danaher JC virus antibody status underestimates infection rates Ann Neurol 2013 10.1002/ana.23893
9. J.R. Berger, L. Pall, D. Lanska, and M. Whiteman Progressive multifocal leukoencephalopathy in patients with HIV infection J Neurovirol 4 1998 59 68
10. F. Bernal-Cano, J.T. Joseph, and I.J. Koralnik Spinal cord lesions of progressive multifocal leukoencephalopathy in an acquired immunodeficiency syndrome patient J Neurovirol 13 2007 474 476
11. BiogenIdec PML incidence in patients receiving Tysabri (natalizumab) Med Inf: Biogen I 2013 (December)
12. N.F. Blair, B.J. Brew, and J.P. Halpern Natalizumab-associated PML entified in the presymptomatic phase using MRI surveillance Neurology 78 2012 507 508
13. M. Blinkenberg, F. Sellebjerg, A.M. Leffers, C.G. Madsen, and P.S. Sorensen Clinically silent PML and prolonged immune reconstitution inflammatory syndrome in a patient with multiple sclerosis treated with natalizumab Mult Scler 19 2013 1226 1229
14. G. Bloomgren, S. Richman, C. Hotermans, M. Subramanyam, S. Goelz, and A. Natarajan et al. Risk of natalizumab-associated progressive multifocal leukoencephalopathy N Engl J Med 366 2012 1870 1880
15. A.L. Boster, J.A. Nicholas, I. Topalli, Y.Y. Kisanuki, W. Pei, and B. Morgan-Followell et al. Lessons learned from fatal progressive multifocal leukoencephalopathy in a patient with multiple sclerosis treated with natalizumab JAMA Neurol 70 2013 398 402
16. B.R. Brooks, and D.L. Walker Progressive multifocal leukoencephalopathy Neurol Clin 2 1984 299 313
17. R.L. Carruthers, T. Chitnis, and B.C. Healy Modeling probability of additional cases of natalizumab-associated JCV sero-negative progressive multifocal leukoencephalopathy Mult Scler 2013
18. D. Cettomai, and J.C. McArthur Mirtazapine use in human immunodeficiency virus-infected patients with progressive multifocal leukoencephalopathy Arch Neurol 66 2009 255 258
19. H. Chang, M. Wang, R.T. Tsai, H.S. Lin, J.S. Huan, and W.C. Wang et al. High incidence of JC viruria in JC-seropositive older individuals J Neurovirol 8 2002 447 451
20. Y. Chen, E. Bord, T. Tompkins, J. Miller, C.S. Tan, and R.P. Kinkel et al. Asymptomatic reactivation of JC virus in patients treated with natalizumab N Engl J Med 361 2009 1067 1074
21. P.U. Chikezie, and A.L. Greenberg Idiopathic CD4+ T lymphocytopenia presenting as progressive multifocal leukoencephalopathy: case report Clin Infect Dis 24 1997 526 527
22. P. Cinque, C. Pierotti, M.G. Vigano, A. Bestetti, C. Fausti, and D. Bertelli et al. The good and evil of HAART in HIV-related progressive multifocal leukoencephalopathy J Neurovirol 7 2001 358 363
23. D.B. Clifford, B. Ances, C. Costello, S. Rosen-Schmidt, M. Andersson, and D. Parks et al. Rituximab-associated progressive multifocal leukoencephalopathy in rheumatoid arthritis Arch Neurol 68 2011 1156 1164
24. D.B. Clifford, A. De Luca, D.M. Simpson, G. Arendt, G. Giovannoni, and A. Nath Natalizumab-associated progressive multifocal leukoencephalopathy in patients with multiple sclerosis: lessons from 28 cases Lancet Neurol 9 2010 438 446
25. D.B. Clifford, A. Nath, P. Cinque, B.J. Brew, R. Zivadinov, and L. Gorelik et al. A study of mefloquine treatment for progressive multifocal leukoencephalopathy: results and exploration of predictors of PML outcomes J Neurovirol 19 2013 351 358
26. M. del Pilar Martin, P.D. Cravens, R. Winger, E.M. Frohman, M.K. Racke, and T.N. Eagar et al. Decrease in the numbers of dendritic cells and CD4+ T cells in cerebral perivascular spaces due to natalizumab Arch Neurol 65 2008 1596 1603
27. S. Delbue, F.R. Guerini, R. Mancuso, D. Caputo, R. Mazziotti, and M. Saresella et al. JC virus viremia in interferon-beta -treated and untreated Italian multiple sclerosis patients and healthy controls J Neurovirol 13 2007 73 77
28. M. Delgado-Alvarado, M.J. Sedano, V. Gonzalez-Quintanilla, E.M. de Lucas, J.M. Polo, and J. Berciano Progressive multifocal leukoencephalopathy and idiopathic CD4 lymphocytopenia J Neurol Sci 327 2013 75 79
29. E.A. Engels, D.E. Rollison, P. Hartge, D. Baris, J.R. Cerhan, and R.K. Severson et al. Antibodies to JC and BK viruses among persons with non-Hodgkin lymphoma Int J Cancer 117 2005 1013 1019
30. U. Ermis, J. Weis, and J.B. Schulz PML in a patient treated with fumaric acid N Engl J Med 368 2013 1657 1658
31. FDA.gov. FDA Drug Safety Communication: FDA investigating rare brain infection in patient taking Gilenya (fingolimod).
32. A.J. Fine, A. Sorbello, C. Kortepeter, and L. Scarazzini Progressive multifocal leukoencephalopathy after natalizumab discontinuation Ann Neurol 2013
33. J. Gasnault, M. Kahraman, M.G. de Goer de Herve, D. Durali, J.F. Delfraissy, and Y. Taoufik Critical role of JC virus-specific CD4 T-cell responses in preventing progressive multifocal leukoencephalopathy AIDS 17 2003 1443 1449
34. S. Gheuens, D.R. Smith, X. Wang, D.C. Alsop, R.E. Lenkinski, and I.J. Koralnik Simultaneous PML-IRIS after discontinuation of natalizumab in a patient with MS Neurology 78 2012 1390 1393
35. L. Gorelik, M. Lerner, S. Bixler, M. Crossman, B. Schlain, and K. Simon et al. Anti-JC virus antibodies: implications for PML risk stratification Ann Neurol 68 2010 295 303
36. S. Haider, D. Nafziger, J.A. Gutierrez, I. Brar, N. Mateo, and J. Fogle Progressive multifocal leukoencephalopathy and idiopathic CD4+lymphocytopenia: a case report and review of reported cases Clin Infect Dis 31 2000 E20 E22
37. H. Hendel-Chavez, M.G. de Goer de Herve, C. Giannesini, A.A. Mazet, C. Papeix, and C. Louapre et al. Immunological hallmarks of JC virus replication in multiple sclerosis patients on long-term natalizumab therapy J Virol 87 2013 6055 6059
38. E. Iacobaeus, C. Ryschkewitsch, M. Gravell, M. Khademi, E. Wallstrom, and T. Olsson et al. Analysis of cerebrospinal fluid and cerebrospinal fluid cells from patients with multiple sclerosis for detection of JC virus DNA Mult Scler 15 2009 28 35
39. T. Iwase, K. Ojika, E. Katada, S. Mitake, H. Nakazawa, and N. Matsukawa et al. An unusual course of progressive multifocal leukoencephalopathy in a patient with idiopathic CD4+ T lymphocytopenia J Neurol Neurosurg Psychiatry 64 1998 788 791
40. P.N. Jensen, and E.O. Major A classification scheme for human polyomavirus JCV variants based on the nucleotide sequence of the noncoding regulatory region J Neurovirol 7 2001 280 287
41. B.O. Khatri, S. Man, G. Giovannoni, A.P. Koo, J.C. Lee, and B. Tucky et al. Effect of plasma exchange in accelerating natalizumab clearance and restoring leukocyte function Neurology 72 2009 402 409
42. M.N. Khoury, M.A. Mittleman, and I.J. Koralnik ABO blood groups and risk for progressive multifocal leukoencephalopathy JAMA Neurol 70 2013 1331 1332
43. B.K. Kleinschmidt-DeMasters, and K.L. Tyler Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis N Engl J Med 353 2005 369 374
44. I.J. Koralnik, R.A. Du Pasquier, and N.L. Letvin JC virus-specific cytotoxic T lymphocytes in individuals with progressive multifocal leukoencephalopathy J Virol 75 2001 3483 3487
45. I.J. Koralnik, C. Wuthrich, X. Dang, M. Rottnek, A. Gurtman, and D. Simpson et al. JC virus granule cell neuronopathy: A novel clinical syndrome distinct from progressive multifocal leukoencephalopathy Ann Neurol 57 2005 576 580
46. J. Kuhle, R. Gosert, R. Buhler, T. Derfuss, R. Sutter, and O. Yaldizli et al. Management and outcome of CSF-JC virus PCR-negative PML in a natalizumab treated MS patient Neurology 2011 (TBA:TBA)
47. A. Langer-Gould, S.W. Atlas, A.J. Green, A.W. Bollen, and D. Pelletier Progressive multifocal leukoencephalopathy in a patient treated with natalizumab N Engl J Med 353 2005 375 381
48. H. Linda, and A. von Heijne Presymptomatic diagnosis with MRI and adequate treatment ameliorate the outcome after natalizumab-associated progressive multifocal leukoencephalopathy Front Neurol 4 2013 11
49. H. Linda, A. von Heijne, E.O. Major, C. Ryschkewitsch, J. Berg, and T. Olsson et al. Progressive multifocal leukoencephalopathy after natalizumab monotherapy N Engl J Med 361 2009 1081 1087
50. P.D. Ling, J.A. Lednicky, W.A. Keitel, D.G. Poston, Z.S. White, and R. Peng et al. The dynamics of herpesvirus and polyomavirus reactivation and shedding in healthy adults: a 14-month longitudinal study J Infect Dis 187 2003 1571 1580
51. E.O. Major, E. Frohman, and D. Douek JC viremia in natalizumab-treated patients with multiple sclerosis N Engl J Med 368 2013 2240 2241
52. R.B. Markowitz, H.C. Thompson, J.F. Mueller, J.A. Cohen, and W.S. Dynan Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects J Infect Dis 167 1993 13 20
53. G. Martin-Blondel, J. Bauer, V. Cuvinciuc, E. Uro-Coste, A. Debard, and P. Massip et al. In situ evidence of JC virus control by CD8+ T cells in PML-IRIS during HIV infection Neurology 81 2013 964 970
54. F.J. Mateen, R. Muralidharan, M. Carone, D. van de Beek, D.M. Harrison, and A.J. Aksamit et al. Progressive multifocal leukoencephalopathy in transplant recipients Ann Neurol 70 2011 305 322
55. A. Matos, V. Duque, S. Beato, J.P. da Silva, E. Major, and A. Melico-Silvestre Characterization of JC human polyomavirus infection in a Portuguese population J Med Virol. 82 2010 494 504
56. M.E. Mazda, J.R. Brosch, A.L. Wiens, J.M. Bonnin, A.P. Kamer, and D.H. Mattson et al. A case of natalizumab-associated progressive multifocal leukoencephalopathy with repeated negative CSF JCV testing Int J Neurosci 123 2013 353 357
57. I. Metz, E.W. Radue, A. Oterino, T. Kumpfel, H. Wiendl, and S. Schippling et al. Pathology of immune reconstitution inflammatory syndrome in multiple sclerosis with natalizumab-associated progressive multifocal leukoencephalopathy Acta Neuropathol 123 2012 235 245
58. N. Mikael Cohen, Elisabeth Maillart, Caroline Papeix, Sandra Vukusic, David Brassat, and Jerome De Seze et al. A French observational study about switching from natalizumab to fingolimod in multiple sclerosis 2013 American Academy of Neurology San Diego, California
59. E.S. Molloy, and L.H. Calabrese Progressive multifocal leukoencephalopathy: a national estimate of frequency in systemic lupus erythematosus and other rheumatic diseases Arthritis. Rheum. 60 2009 3761 3765
60. P.W. OConnor, A. Goodman, L. Kappos, F.D. Lublin, D.H. Miller, and C. Polman et al. Disease activity return during natalizumab treatment interruption in patients with multiple sclerosis Neurology 76 2011 1858 1865
61. T. Olsson, A. Achiron, L. Alfredsson, T. Berger, D. Brassat, and A. Chan et al. Anti-JC virus antibody prevalence in a multinational multiple sclerosis cohort Mult Scler 19 2013 1533 1538
62. K. Owczarczyk, R. Hilker, A. Brunn, M. Hallek, and A. Rubbert Progressive multifocal leucoencephalopathy in a patient with sarcoidosis - successful treatment with cidofovir and mirtazapine Rheumatology (Oxford) 46 2007 888 890
63. E. Palazzo, and S.A. Yahia Progressive multifocal leukoencephalopathy in autoimmune diseases Joint Bone Spine 79 2012 351 355
64. R. Phan-Ba, E. Lommers, L. Tshibanda, P. Calay, B. Dubois, and G. Moonen et al. MRI preclinical detection and asymptomatic course of a progressive multifocal leucoencephalopathy (PML) under natalizumab therapy J Neurol Neurosurg Psychiatry 83 2012 224 226
65. R. Planas, I. Jelcic, S. Schippling, R. Martin, and M. Sospedra Natalizumab treatment perturbs memory- and marginal zone-like B-cell homing in secondary lymphoid organs in multiple sclerosis Eur J Immunol 42 2012 790 798
66. S.M. Plavina T, G. Bloomgren, S. Richman, A. Pace, S. Lee, and B. Schlain et al. Anti-JCV antibody index further defines PML risk in natalizumab-treated MS patients 2013 CMSC Orlando Florida
67. V. Puri, N. Chaudhry, P. Gulati, N. Patel, M. Tatke, and S. Sinha Progressive multifocal leukoencephalopathy in a patient with idiopathic CD4+T lymphocytopenia Neurol India 58 2010 118 121
68. A. Rossi, S. Delbue, R. Mazziotti, M. Valli, E. Borghi, and R. Mancuso et al. Presence, quantitation and characterization of JC virus in the urine of Italian immunocompetent subjects J Med Virol 79 2007 408 412
69. R.A. Rudick, P.W. OConnor, C.H. Polman, A.D. Goodman, S.S. Ray, and N.M. Griffith et al. Assessment of JC virus DNA in blood and urine from natalizumab-treated patients Ann Neurol 68 2010 304 310
70. C.F. Ryschkewitsch, P.N. Jensen, M.C. Monaco, and E.O. Major JC virus persistence following progressive multifocal leukoencephalopathy in multiple sclerosis patients treated with natalizumab Ann Neurol 68 2010 384 391
71. S. Schippling, C. Kempf, F. Buchele, I. Jelcic, O. Bozinov, and A. Bont et al. JC virus granule cell neuronopathy and GCN-IRIS under natalizumab treatment Ann Neurol 74 2013 622 626
72. N. Schwab, T. Schneider-Hohendorf, V. Posevitz, J. Breuer, K. Gobel, and S. Windhagen et al. L-Selectin is a possible biomarker for individual PML risk in natalizumab-treated MS patients Neurology 81 2013 865 871
73. D. Stefoski, and R. Balabanov Novel interventions with favorable resolution of natalizumab-indeced progressive multifocal leukoencephalopathy (PML) 2012 ECTRIMS, Lyons France
74. O. Stuve, C.M. Marra, A. Bar-Or, M. Niino, P.D. Cravens, and S. Cepok et al. Altered CD4+/CD8+ T-cell ratios in cerebrospinal fluid of natalizumab-treated patients with multiple sclerosis Arch Neurol 63 2006 1383 1387
75. C.S. Tan, B.J. Dezube, P. Bhargava, P. Autissier, C. Wuthrich, and J. Miller et al. Detection of JC virus DNA and proteins in the bone marrow of HIV-positive and HIV-negative patients: implications for viral latency and neurotropic transformation J Infect Dis 199 2009 881 888
76. C.S. Tan, L.C. Ellis, C. Wuthrich, L. Ngo, T.A. Broge Jr., and J. Saint-Aubyn et al. JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy J Virol 84 2010 9200 9209
77. C.S. Tan, and I.J. Koralnik Progressive multifocal leukoencephalopathy and other disorders caused by JC virus: clinical features and pathogenesis Lancet Neurol 9 2010 425 437
78. I.L. Tan, J.C. McArthur, D.B. Clifford, E.O. Major, and A. Nath Immune reconstitution inflammatory syndrome in natalizumab-associated PML Neurology 77 2011 1061 1067
79. K. Tan, R. Roda, L. Ostrow, J. McArthur, and A. Nath PML-IRIS in patients with HIV infection. Clinical manifestations and treatment with steroids Neurology 2009
80. C. Tortorella, V. Direnzo, M. DOnghia, and M. Trojano Brainstem PML lesion mimicking MS plaque in a natalizumab-treated MS patient Neurology 81 2013 1470 1471
81. Tuan Dong-Si, Gary Bloomgren, Madé Wenten, Jeffrey Philip, and James McIninch Shoibal Datta et al. Natalizumab-associated progressive multifocal leukoencephalopathy (PML) in multiple sclerosis patients: survival and functional outcome when asymptomatic at diagnosis 2013 American Academy of Neurology San Diego, CA
82. C. Tur, M. Tintore, A. Vidal-Jordana, J. Castillo, I. Galan, and J. Rio et al. Natalizumab discontinuation after PML risk stratification: outcome from a shared and informed decision Mult Scler 18 2012 1193 1196
83. Tysabri (natalizumab) prescribing information. Biogen Idec. Cambridge, MA; 2004.
84. G. Van Assche, M. Van Ranst, R. Sciot, B. Dubois, S. Vermeire, and M. Noman et al. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohns disease N Engl J Med 353 2005 362 368
85. B.W. van Oosten, J. Killestein, F. Barkhof, C.H. Polman, and M.P. Wattjes PML in a patient treated with dimethyl fumarate from a compounding pharmacy N Engl J Med 368 2013 1658 1659
86. J.A. van Rossum, A. Vennegoor, L. Balk, B.M. Uitdehaag, C.H. Polman, and J. Killestein Safety, anxiety and natalizumab continuation in JC virus-seropositive MS patients Mult Scler 2013
87. P. Vermersch, L. Kappos, R. Gold, J.F. Foley, T. Olsson, and D. Cadavid et al. Clinical outcomes of natalizumab-associated progressive multifocal leukoencephalopathy Neurology 76 2011 1697 1704
88. R.P. Viscidi, N. Khanna, C.S. Tan, X. Li, L. Jacobson, and D.B. Clifford et al. JC virus antibody and viremia as predictors of progressive multifocal leukoencephalopathy in human immunodeficiency virus-1-infected individuals Clin Infect Dis 53 2011 711 715
89. C. Warnke, A.K. Mausberg, M. Stettner, T. Dehmel, L. Nekrich, and G. Meyer Zu Horste et al. Natalizumab affects the T-cell receptor repertoire in patients with multiple sclerosis Neurology 81 2013 1400 1408
90. W. Wenning, A. Haghikia, J. Laubenberger, D.B. Clifford, P.F. Behrens, and A. Chan et al. Treatment of progressive multifocal leukoencephalopathy associated with natalizumab N Engl J Med 361 2009 1075 1080
91. C. Wuthrich, X. Dang, S. Westmoreland, J. McKay, A. Maheshwari, and M.P. Anderson et al. Fulminant JC virus encephalopathy with productive infection of cortical pyramidal neurons Ann Neurol 65 2009 742 748
92. C. Wuthrich, B.F. Popescu, S. Gheuens, M. Marvi, R. Ziman, and S.P. Denq et al. Natalizumab-associated progressive multifocal leukoencephalopathy in a patient with multiple sclerosis: a postmortem study J Neuropathol Exp Neurol 72 2013 1043 1051
93. T.A. Yousry, D. Pelletier, D. Cadavid, A. Gass, N.D. Richert, and E.W. Radue et al. Magnetic resonance imaging pattern in natalizumab-associated progressive multifocal leukoencephalopathy Ann Neurol 72 2012 779 787