Neurological approaches for investigating West Nile virus disease and its treatment in rodents

Antiviral Research

Volumn 100, Issue 2, 2013, Pages 535-545

  Morrey, John D ^a   Siddharthan, Venkatraman ^a   Wang, Hong ^a  

^a UTAH STATE UNIVERSITY   (United States)

Author keywords

Autonomic; Electromyography; Optogenetic; Plethysmography; Spinal cord; West Nile virus

Indexed keywords

3,4 DIAMINOPYRIDINE; ACETYLCYSTEINE; ALPHA TOCOPHEROL; AZATHIOPRINE; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; DEXTROMETHORPHAN; GABAPENTIN; LAMOTRIGINE; PENICILLAMINE; RILUZOLE; SELEGILINE; TACRINE; THREONINE; TOPIRAMATE; VERAPAMIL; XALIPRODEN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AUTONOMIC NERVOUS SYSTEM; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; ELECTROMYOGRAPHY; HAMSTER; HEART RATE VARIABILITY; MAZE TEST; MEMORY; MOTONEURON; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PHOTOACTIVATION; PLETHYSMOGRAPHY; PRIORITY JOURNAL; RESPIRATORY FUNCTION; REVIEW; RODENT; SPATIAL MEMORY; SPINAL CORD; WEST NILE FEVER; WEST NILE FLAVIVIRUS; ANIMAL; AUTONOMIC; DISEASE MODEL; ELECTROPHYSIOLOGY; HUMAN; NEUROLOGIC EXAMINATION; OPTOGENETIC; PATHOLOGY; VIROLOGY;

ANIMALIA; CRICETINAE; MUS; RODENTIA; WEST NILE VIRUS;

AUTONOMIC; ELECTROMYOGRAPHY; OPTOGENETIC; PLETHYSMOGRAPHY; SPINAL CORD; WEST NILE VIRUS;

ANIMALS; CRICETINAE; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; MICE; NEUROLOGIC EXAMINATION; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84885495196     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.09.010     Document Type: Review

References (93)

1. F. Abroug, L. Ouanes-Besbes, I. Ouanes, N. Nciri, F. Dachraoui, and F. Najjar Adrenal insufficiency in severe West Nile virus infection Intens. Care Med. 32 2006 1636 1639
2. D.P. Agamanolis, M.J. Leslie, E.A. Caveny, J. Guarner, W.J. Shieh, and S.R. Zaki Neuropathological findings in West Nile virus encephalitis: a case report Ann. Neurol. 54 2003 547 551
3. M. Ali, Y. Safriel, J. Sohi, A. Llave, and S. Weathers West Nile virus infection: MR imaging findings in the nervous system AJNR Am. J. Neuroradiol. 26 2005 289 297
4. D.S. Asnis, R. Conetta, A.A. Teixeira, G. Waldman, and B.A. Sampson The West Nile virus outbreak of 1999 in New York: the Flushing Hospital experience Clin. Infect. Dis. 30 2000 413 418
5. A. Bagic, E.A. Boudreau, J. Greenfield, and S. Sato Electro-clinical evolution of refractory non-convulsive status epilepticus caused by West Nile virus encephalitis Epilept. Disord. 9 2007 98 103
6. D. Ben-Nathan, G.J.M. Maestroni, S. Lustig, and A. Conti Protective effects of melatonin in mice infected with encephalitis viruses Arch. Virol. 140 1995 223 230
7. D. Ben-Nathan, I. Huitinga, S. Lustig, N. van Rooijen, and D. Kobiler West Nile virus neuroinvasion and encephalitis induced by macrophage depletion in mice Arch. Virol. 141 1996 459 469
8. A.D. Betensley, S.H. Jaffery, H. Collins, N. Sripathi, and F. Alabi Bilateral diaphragmatic paralysis and related respiratory complications in a patient with West Nile virus infection Thorax 59 2004 268 269
9. A.V. Bode, J.J. Sejvar, W.J. Pape, G.L. Campbell, and A.A. Marfin West Nile virus disease: a descriptive study of 228 patients hospitalized in a 4-county region of Colorado in 2003 Clin. Infect. Dis. 42 2006 1234 1240
10. C.M. Bosanko, J. Gilroy, A.M. Wang, W. Sanders, M. Dulai, J. Wilson, and K. Blum West nile virus encephalitis involving the substantia nigra: neuroimaging and pathologic findings with literature review Arch. Neurol. 60 2003 1448 1452
11. J.P. Bouffard, M.A. Riudavets, R. Holman, and E.J. Rushing Neuropathology of the brain and spinal cord in human West Nile virus infection Clin. Neuropathol. 23 2004 59 61
12. E.J. Buenz, M. Rodriguez, and C.L. Howe Disrupted spatial memory is a consequence of picornavirus infection Neurobiol. Dis. 24 2006 266 273
13. M.P. Busch, S.H. Kleinman, L.H. Tobler, H.T. Kamel, P.J. Norris, I. Walsh, J.L. Matud, H.E. Prince, R.S. Lanciotti, D.J. Wright, J.M. Linnen, and S. Caglioti Virus and antibody dynamics in acute West Nile virus infection J. Infect. Dis. 198 2008 984 993
14. S.N. Byrne, G.M. Halliday, L.J. Johnston, and N.J. King Interleukin-1beta but not tumor necrosis factor is involved in West Nile virus-induced Langerhans cell migration from the skin in C57BL/6 mice J. Invest. Dermatol. 117 2001 702 709
15. D.L. Camenga, N. Nathanson, and G.A. Cole Cyclophosphamide-potentiated West Nile viral encephalitis: relative influence of cellular and humoral factors J. Infect. Dis. 130 1974 634 641
16. N.J. Cao, C. Ranganathan, W.J. Kupsky, and J. Li Recovery and prognosticators of paralysis in West Nile virus infection J. Neurol. Sci. 236 2005 73 80
17. P.J. Carson, P. Konewko, K.S. Wold, P. Mariani, S. Goli, P. Bergloff, and R.D. Crosby Long-term clinical and neuropsychological outcomes of West Nile virus infection Clin. Infect. Dis. 43 2006 723 730
18. J.B. Chapa, J.T. Ahn, L.M. DiGiovanni, and M.A. Ismail West Nile virus encephalitis during pregnancy Obstet. Gynecol. 102 2003 229 231
19. Y. Chudasama, and T.W. Robbins Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans Biol. Psychol. 73 2006 19 38
20. R.L. Cook, X. Xu, E.J. Yablonsky, N. Sakata, J.H. Tripp, R. Hess, P. Piazza, and C.R. Rinaldo Demographic and clinical factors associated with persistent symptoms after West Nile virus infection Am. J. Trop. Med. Hyg. 83 2010 1133 1136
21. J. Dai, P. Wang, F. Bai, T. Town, and E. Fikrig Icam-1 participates in the entry of west Nile virus into the central nervous system J. Virol. 82 2008 4164 4168
22. J.W. Dalley, R.N. Cardinal, and T.W. Robbins Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates Neurosci. Biobehav. Rev. 28 2004 771 784
23. M. Dantes, and A. McComas The extent and time course of motoneuron involvement in amyotrophic lateral sclerosis Muscle Nerve 14 1991 416 421
24. L.E. Davis, R. DeBiasi, D.E. Goade, K.Y. Haaland, J.A. Harrington, J.B. Harnar, S.A. Pergam, M.K. King, B.K. DeMasters, and K.L. Tyler West Nile virus neuroinvasive disease Ann. Neurol. 60 2006 286 300
25. M.S. Diamond, B. Shrestha, A. Marri, D. Mahan, and M. Engle B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus J. Virol. 77 2003 2578 2586
26. M.S. Diamond, E.M. Sitati, L.D. Friend, S. Higgs, B. Shrestha, and M. Engle A critical role for induced IgM in the protection against West Nile virus infection J. Exp. Med. 198 2003 1853 1862
27. S.I. Doron, J.F. Dashe, L.S. Adelman, W.F. Brown, B.G. Werner, and S. Hadley Histopathologically proven poliomyelitis with quadriplegia and loss of brainstem function due to West Nile virus infection Clin. Infect. Dis. 37 2003 e74 77
28. J.D. Fratkin, A.A. Leis, D.S. Stokic, S.A. Slavinski, and R.W. Geiss Spinal cord neuropathology in human West Nile virus infection Arch. Pathol. Lab. Med. 128 2004 533 537
29. E. Gelpi, M. Preusser, F. Garzuly, H. Holzmann, F.X. Heinz, and H. Budka Visualization of Central European tick-borne encephalitis infection in fatal human cases J. Neuropathol. Exp. Neurol. 64 2005 506 512
30. S.E. Gibbs, A.E. Ellis, D.G. Mead, A.B. Allison, J.K. Moulton, E.W. Howerth, and D.E. Stallknecht West Nile virus detection in the organs of naturally infected blue jays (Cyanocitta cristata) J. Wildl. Dis. 41 2005 354 362
31. K.B. Gibney, R.S. Lanciotti, J.J. Sejvar, C.T. Nugent, J.M. Linnen, M.J. Delorey, J.A. Lehman, E.N. Boswell, J.E. Staples, and M. Fischer West Nile virus RNA not detected in urine of 40 people tested 6 years after acute West Nile virus disease J. Infect. Dis. 203 2011 344 347
32. K. Gottfried, R. Quinn, and T. Jones Clinical description and follow-up investigation of human West Nile virus cases South Med. J. 98 2005 603 606
33. P. Grossman, and E.W. Taylor Toward understanding respiratory sinus arrhythmia: relations to cardiac vagal tone, evolution and biobehavioral functions Biol. Psychol. 74 2007 263 285
34. E.B. Hayes, J.J. Sejvar, S.R. Zaki, R.S. Lanciotti, A.V. Bode, and G.L. Campbell Virology, pathology, and clinical manifestations of West Nile virus disease Emerg. Infect. Dis. 11 2005 1174 1179
35. Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology Eur. Heart J. 17 1996 354 381
36. E.A. Hunsperger, and J.T. Roehrig Temporal analyses of the neuropathogenesis of a West Nile virus infection in mice J. Neurovirol. 12 2006 129 139
37. E.A. Hunsperger, and J.T. Roehrig Nocodazole delays viral entry into the brain following footpad inoculation with West Nile virus in mice J. Neurovirol. 15 2009 211 218
38. L.E. Jeha, C.A. Sila, R.J. Lederman, R.A. Prayson, C.M. Isada, and S.M. Gordon West Nile virus infection: a new acute paralytic illness Neurology 61 2003 55 59
39. R.T. Johnson The pathogenesis of acute viral encephalitis and postinfectious encephalomyelitis J. Infect. Dis. 155 1987 359 364
40. L.J. Johnston, G.M. Halliday, and N.J. King Langerhans cells migrate to local lymph nodes following cutaneous infection with an arbovirus J. Invest. Dermatol. 114 2000 560 568
41. M. Khairallah, S. Ben Yahia, A. Ladjimi, H. Zeghidi, F. Ben Romdhane, L. Besbes, S. Zaouali, and R. Messaoud Chorioretinal involvement in patients with West Nile virus infection Ophthalmology 111 2004 2065 2070
42. Laboratory-acquired West Nile virus infections - United States MMWR Morb. Mortal Wkly. Rep. 51 2002 1133 1135
43. A.A. Leis, and D.S. Stokic Neuromuscular manifestations of human West Nile virus infection Curr. Treat. Options Neurol. 7 2005 15 22
44. P. Leyssen, R. Croes, P. Rau, S. Heiland, E. Verbeken, R. Sciot, J. Paeshuyse, N. Charlier, E. De Clercq, U. Meyding-Lamade, and J. Neyts Acute encephalitis, a poliomyelitis-like syndrome and neurological sequelae in a hamster model for flavivirus infections Brain Pathol. 13 2003 279 290
45. J. Li, J.A. Loeb, M.E. Shy, A.K. Shah, A.C. Tselis, W.J. Kupski, and R.A. Lewis Asymmetric flaccid paralysis: a neuromuscular presentation of West Nile virus infection Ann. Neurol. 53 2003 703 710
46. C.A. Lichtensteiger, K. Heinz-Taheny, T.S. Osborne, R.J. Novak, B.A. Lewis, and M.L. Firth West Nile virus encephalitis and myocarditis in wolf and dog Emerg. Infect. Dis. 9 2003 1303 1306
47. N.P. Lindsey, J.E. Staples, J.A. Lehman, and M. Fischer Surveillance for human West Nile virus disease - United States, 1999-2008 MMWR Surveill. Summ. 59 2010 1 17
48. A. Macedo de Oliveira, B.D. Beecham, S.P. Montgomery, R.S. Lanciotti, J.M. Linnen, C. Giachetti, L.A. Pietrelli, S.L. Stramer, and T.J. Safranek West Nile virus blood transfusion-related infection despite nucleic acid testing Transfusion 44 2004 1695 1699
49. J.M. Mazurek, K. Winpisinger, B.J. Mattson, R. Duffy, and R.L. Moolenaar The epidemiology and early clinical features of West Nile virus infection Am. J. Emerg. Med. 23 2005 536 543
50. T.D. Moon, A. Nadimpalli, E.B. Martin, M.A. Ortiz, and R.B. Van Dyke Balance and gait abnormalities of a child with West Nile virus infection Pediatr. Infect. Dis. J. 24 2005 568 570
51. J.D. Morrey, C.W. Day, J.G. Julander, L.M. Blatt, D.F. Smee, and R.W. Sidwell Effect of interferon-alpha and interferon-inducers on West Nile virus in mouse and hamster animal models Antivir. Chem. Chemother. 15 2004 101 109
52. J.D. Morrey, C.W. Day, J.G. Julander, A.L. Olsen, R.W. Sidwell, C.D. Cheney, and L.M. Blatt Modeling hamsters for evaluating West Nile virus therapies Antiviral Res. 63 2004 41 50
53. J.D. Morrey, V. Siddharthan, A.L. Olsen, H. Wang, J.G. Julander, J.O. Hall, H. Li, J.L. Nordstrom, S. Koenig, S. Johnson, and M.S. Diamond Defining limits of treatment with humanized neutralizing monoclonal antibody for West Nile virus neurological infection in a hamster model Antimicrob. Agents Chemother. 51 2007 2396 2402
54. J.D. Morrey, A.L. Olsen, V. Siddharthan, N.E. Motter, H. Wang, B.S. Taro, D. Chen, D. Ruffner, and J.O. Hall Increased blood-brain barrier permeability is not a primary determinant for lethality of West Nile virus infection in rodents J. Gen. Virol. 89 2008 467 473
55. J.D. Morrey, V. Siddharthan, H. Wang, J.O. Hall, R.T. Skirpstunas, A.L. Olsen, J.L. Nordstrom, S. Koenig, S. Johnson, and M.S. Diamond West Nile virus-induced acute flaccid paralysis is prevented by monoclonal antibody treatment when administered after infection of spinal cord neurons J. Neurovirol. 14 2008 152 163
56. J.D. Morrey, B.S. Taro, V. Siddharthan, H. Wang, D.F. Smee, A.J. Christensen, and Y. Furuta Efficacy of orally administered T-705 pyrazine analog on lethal West Nile virus infection in rodents Antiviral Res. 80 2008 377 379
57. J.D. Morrey, V. Siddharthan, H. Wang, J.O. Hall, N.E. Motter, R.D. Skinner, and R.T. Skirpstunas Neurological suppression of diaphragm electromyographs in hamsters infected with West Nile virus J. Neurovirol. 16 2010 3129 3198
58. J.D. Morrey, V. Siddharthan, H. Wang, and J.O. Hall Respiratory insufficiency correlated strongly with mortality of rodents infected with West Nile virus PLoS ONE 7 2012 e38672
59. K.E. Morrison Therapies in amyotrophic lateral sclerosis-beyond riluzole Curr. Opin. Pharmacol. 2 2002 302 309
60. K. Murray, C. Walker, E. Herrington, J.A. Lewis, J. McCormick, D.W. Beasley, R.B. Tesh, and S. Fisher-Hoch Persistent infection with West Nile virus years after initial infection J. Infect. Dis. 201 2010 2 4
61. S. Ohka, and A. Nomoto Recent insights into poliovirus pathogenesis Trends Microbiol. 9 2001 501 506
62. T. Oliphant, M. Engle, G.E. Nybakken, C. Doane, S. Johnson, L. Huang, S. Gorlatov, E. Mehlhop, A. Marri, K.M. Chung, G.D. Ebel, L.D. Kramer, D.H. Fremont, and M.S. Diamond Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus Nat. Med. 11 2005 522 530
63. B.I. Omalu, A.A. Shakir, G. Wang, W.I. Lipkin, and C.A. Wiley Fatal fulminant pan-meningo-polioencephalitis due to West Nile virus Brain Pathol. 13 2003 465 472
64. L.R. Petersen, and A.A. Marfin West Nile virus: a primer for the clinician Ann. Intern. Med. 137 2002 173 179
65. K.A. Petropoulou, S.M. Gordon, R.A. Prayson, and P.M. Ruggierri West Nile virus meningoencephalitis: MR imaging findings AJNR Am. J. Neuroradiol. 26 2005 1986 1995
66. O. Rashidipour, and K.M. Chan Motor unit number estimation in neuromuscular disease Canad. J. Neurol. Sci. 35 2008 153 159
67. S.A. Rubin, T.A. Yednock, and K.M. Carbone In vivo treatment with anti-alpha4 integrin suppresses clinical and pathological evidence of Borna disease virus infection J. Neuroimmunol. 84 1998 158 163
68. M. Saad, S. Youssef, D. Kirschke, M. Shubair, D. Haddadin, J. Myers, and J. Moorman Acute flaccid paralysis: the spectrum of a newly recognized complication of West Nile virus infection J. Infect. 51 2005 120 127
69. B.A. Sampson, C. Ambrosi, A. Charlot, K. Reiber, J.F. Veress, and V. Armbrustmacher The pathology of human West Nile Virus infection Hum. Pathol. 31 2000 527 531
70. M.A. Samuel, H. Wang, V. Siddharthan, J.D. Morrey, and M.S. Diamond Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis Proc. Natl. Acad. Sci. U.S.A. 104 2007 17140 17145
71. J.J. Sejvar The long-term outcomes of human West Nile virus infection Clin. Infect. Dis. 44 2007 1617 1624
72. J.J. Sejvar, M.B. Haddad, B.C. Tierney, G.L. Campbell, A.A. Marfin, J.A. Van Gerpen, A. Fleischauer, A.A. Leis, D.S. Stokic, and L.R. Petersen Neurologic manifestations and outcome of West Nile virus infection JAMA 290 2003 511 515
73. J.J. Sejvar, A.A. Leis, D.S. Stokic, J.A. Van Gerpen, A.A. Marfin, R. Webb, M.B. Haddad, B.C. Tierney, S.A. Slavinski, J.L. Polk, V. Dostrow, M. Winkelmann, and L.R. Petersen Acute flaccid paralysis and West Nile virus infection Emerg. Infect. Dis. 9 2003 788 793
74. J.J. Sejvar, A.V. Bode, A.A. Marfin, G.L. Campbell, D. Ewing, M. Mazowiecki, P.V. Pavot, J. Schmitt, J. Pape, B.J. Biggerstaff, and L.R. Petersen West Nile virus-associated flaccid paralysis Emerg. Infect. Dis. 11 2005 1021 1027
75. J.J. Sejvar, A.V. Bode, A.A. Marfin, G.L. Campbell, J. Pape, B.J. Biggerstaff, and L.R. Petersen West Nile Virus-associated flaccid paralysis outcome Emerg. Infect. Dis. 12 2006 514 516
76. J.J. Sejvar, A.T. Curns, L. Welburg, J.F. Jones, L.M. Lundgren, L. Capuron, J. Pape, W.C. Reeves, and G.L. Campbel Neurocognitive and functional outcomes in persons recovering from West Nile virus illness J. Neuropsychol. 2 2008 477 499
77. J.M. Shefner, M.E. Cudkowicz, and R.H. Brown Jr. Comparison of incremental with multipoint MUNE methods in transgenic ALS mice Muscle Nerve 25 2002 39 42
78. J.M. Shefner, M. Cudkowicz, and R.H. Brown Jr. Motor unit number estimation predicts disease onset and survival in a transgenic mouse model of amyotrophic lateral sclerosis Muscle Nerve 34 2006 603 607
79. A.I. Shpall, A. Varpetian, and D.A. Ginsberg Urinary retention in a patient with West Nile virus Urology 61 2003 1259
80. V. Siddharthan, H. Wang, N.E. Motter, J.O. Hall, R.D. Skinner, R.T. Skirpstunas, and J.D. Morrey Persistent West Nile virus associated with a neurological sequela in hamsters identified by motor unit number estimation J. Virol. 83 2009 4251 4261
81. C.A. Smeraski, V. Siddharthan, and J.D. Morrey Treatment of spatial memory impairment in hamsters infected with West Nile virus using a humanized monoclonal antibody MGAWN1 Antiviral Res. 91 2011 43 49
82. K.E. Steele, M.J. Linn, R.J. Schoepp, N. Komar, T.W. Geisbert, R.M. Manduca, P.P. Calle, B.L. Raphael, T.L. Clippinger, T. Larsen, J. Smith, R.S. Lanciotti, N.A. Panella, and T.S. McNamara Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York Vet. Pathol. 37 2000 208 224
83. C.R. Sunico, G. Dominguez, J.M. Garcia-Verdugo, R. Osta, F. Montero, and B. Moreno-Lopez Reduction in the motoneuron inhibitory/excitatory synaptic ratio in an early-symptomatic mouse model of amyotrophic lateral sclerosis Brain Pathol. 21 2011 1 15
84. R.B. Tesh, M. Siirin, H. Guzman, A.P. Travassos da Rosa, X. Wu, T. Duan, H. Lei, M.R. Nunes, and S.Y. Xiao Persistent West Nile virus infection in the golden hamster: studies on its mechanism and possible implications for other flavivirus infections J. Infect. Dis. 192 2005 287 295
85. J.H. Tonry, S.Y. Xiao, M. Siirin, H. Chen, A.P. da Rosa, and R.B. Tesh Persistent shedding of West Nile virus in urine of experimentally infected hamsters Am. J. Trop. Med. Hyg. 72 2005 320 324
86. S. Verma, Y. Lo, M. Chapagain, S. Lum, M. Kumar, U. Gurjav, H. Luo, A. Nakatsuka, and V.R. Nerurkar West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: transmigration across the in vitro blood-brain barrier Virology 385 2009 425 433
87. T. Wang, T. Town, L. Alexopoulou, J.F. Anderson, E. Fikrig, and R.A. Flavell Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis Nat. Med. 10 2004 1366 1373
88. H. Wang, V. Siddharthan, J.O. Hall, and J.D. Morrey Autonomic nervous dysfunction in hamsters infected with West Nile virus PLoS One 6 2011 e19575
89. Wang, H., Siddharthan, V., Hall, J.O., Morrey, J.D., 2013a. Autonomic deficit not cause of death in West Nile virus neurological disease. Clin. Autonom. Res., (Accepted for publication)
90. H. Wang, V. Siddharthan, K.K. Kesler, J.O. Hall, N.E. Motter, J.G. Julander, and J.D. Morrey Fatal neurological respiratory insufficiency common among viral encephalitides J. Infect. Dis. 208 2013 573 583
91. D. Weiss, D. Carr, J. Kellachan, C. Tan, M. Phillips, E. Bresnitz, and M. Layton Clinical findings of West Nile virus infection in hospitalized patients, New York and New Jersey, 2000 Emerg. Infect. Dis. 7 2001 654 658
92. S.Y. Xiao, H. Guzman, H. Zhang, A.P. Travassos da Rosa, and R.B. Tesh West Nile virus infection in the golden hamster (Mesocricetus auratus): a model for West Nile encephalitis Emerg. Infect. Dis. 7 2001 714 721
93. Z. Xu, R. Waeckerlin, M.D. Urbanowski, G. van Marle, and T.C. Hobman West Nile virus infection causes endocytosis of a specific subset of tight junction membrane proteins PLoS One 7 2012 e37886