Neurological sequelae resulting from encephalitic alphavirus infection

Frontiers in Microbiology

Volumn 7, Issue JUN, 2016, Pages

  Ronca, Shannon E ^a,b   Dineley, Kelly T ^b   Paessler, Slobodan ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Alphavirus; Behavior; Sequelae; VEEV; WEEV

Indexed keywords

ALPHAVIRUS INFECTION; ARBOVIRUS; ARTHRALGIA; AUTONOMIC NERVOUS SYSTEM; EASTERN EQUINE ENCEPHALITIS VIRUS; ENCEPHALITIS; ENDEMIC DISEASE; FUNCTIONAL NEUROIMAGING; HEALTH CARE COST; HEARING IMPAIRMENT; HEMIPLEGIA; HUMAN; INTELLECTUAL IMPAIRMENT; LUNG ALVEOLUS HYPOVENTILATION; MEDICAL TECHNOLOGY; MENTAL INSTABILITY; MOSQUITO BITE; MOTONEURON; MULTIPLE ORGAN FAILURE; NEUROSCIENCE; NONHUMAN; PATHOGENESIS; PREPULSE INHIBITION; REVIEW; RNA VIRUS; SEIZURE; SLEEP DISORDERED BREATHING; STARTLE REFLEX; TOGAVIRIDAE; VENEZUELAN EQUINE ENCEPHALITIS; WESTERN EQUINE ENCEPHALITIS VIRUS; WESTERN HEMISPHERE;

EID: 84979995601     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00959     Document Type: Review

References (91)

1. Ahmari, S. E., Risbrough, V. B., Geyer, M. A., and Simpson, H. B. (2012). Impaired sensorimotor gating in unmedicated adults with obsessive-compulsive disorder. Neuropsychopharmacology 37, 1216-1223. doi: 10.1038/npp.2011.308.
2. Alevizatos, A. C., McKinney, R. W., and Feigin, R. D. (1967). Live, attenuated Venezuelan equine encephalomyelitis virus vaccine. I. Clinical effects in man. Am. J. Trop. Med. Hyg. 16, 762-768.
3. Anukumar, B., Thekkekara, R. J., and Tandale, B. V. (2016). Outcomes of West Nile encephalitis patients after one year of West Nile encephalitis outbreak in Kerala, India: a follow-up study. J. Med. Virol. doi: 10.1002/jmv.24545 [Epub ahead of print].
4. Asnis, D. S., Conetta, R., Teixeira, A. A., Waldman, G., and Sampson, B. A. (2000). The west nile virus outbreak of 1999 in New York: the Flushing Hospital experience. Clin. Infect. Dis. 30, 413-418. doi: 10.1086/313737.
5. Barrett, S. L., Kelly, C., Watson, D. R., Bell, R., and King, D. J. (2005). Normal levels of prepulse inhibition in the euthymic phase of bipolar disorder. Psychol. Med. 35, 1737-1746. doi: 10.1017/S0033291705005702.
6. Bhavana, K., Tyagi, I., and Kapila, R. K. (2008). Chikungunya virus induced sudden sensorineural hearing loss. Int. J. Pediatr. Otorhinolaryngol. 72, 257-259. doi: 10.1016/j.ijporl.2007.09.022.
7. Boere, W. A., Harmsen, T., Vinje, J., Benaissa-Trouw, B. J., Kraaijeveld, C. A., and Snippe, H. (1984). Identification of distinct antigenic determinants on Semliki Forest virus by using monoclonal antibodies with different antiviral activities. J. Virol. 52, 575-582.
8. Bowen, G. S., Fashinell, T. R., Dean, P. B., and Gregg, M. B. (1976). Clinical aspects of human Venezuelan equine encephalitis in Texas. Bull. Pan Am. Health Organ. 10, 46-57.
9. Braff, D., Stone, C., Callaway, E., Geyer, M., Glick, I., and Bali, L. (1978). Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15, 339-343. doi: 10.1111/j.1469-8986.1978.tb01390.x.
10. Braff, D. L. (1992). Reply to cognitive therapy and schizophrenia. Schizophr. Bull. 18, 37-38. doi: 10.1093/schbul/18.1.37.
11. Braff, D. L., Geyer, M. A., Light, G. A., Sprock, J., Perry, W., Cadenhead, K. S., et al. (2001). Impact of prepulse characteristics on the detection of sensorimotor gating deficits in schizophrenia. Schizophr. Res. 49, 171-178. doi: 10.1016/S0920-9964(00)00139-0.
12. Burton, J. M., Kern, R. Z., Halliday, W., Mikulis, D., Brunton, J., Fearon, M., et al. (2004). Neurological manifestations of West Nile virus infection. Can. J. Neurol. Sci. 31, 185-193. doi: 10.1017/S0317167100053828.
13. Calisher, C. H., Sasso, D. R., and Sather, G. E. (1973). Possible evidence for interference with Venezuelan equine encephalitis virus vaccination of equines by pre-existing antibody to Eastern or Western Equine encephalitis virus, or both. Appl. Microbiol. 26, 485-488.
14. Calisher, C. H., Shope, R. E., Brandt, W., Casals, J., Karabatsos, N., Murphy, F. A., et al. (1980). Proposed antigenic classification of registered arboviruses I. Togaviridae Alphavirus. Intervirology 14, 229-232. doi: 10.1159/000149190.
15. Carrara, A. S., Gonzales, G., Ferro, C., Tamayo, M., Aronson, J., Paessler, S., et al. (2005). Venezuelan equine encephalitis virus infection of spiny rats. Emerg. Infect. Dis. 11, 663-669. doi: 10.3201/eid1105.041251.
16. Carrera, J. P., Forrester, N., Wang, E., Vittor, A. Y., Haddow, A. D., Lopez-Verges, S., et al. (2013). Eastern equine encephalitis in Latin America. N. Engl. J. Med. 369, 732-744. doi: 10.1056/NEJMoa1212628.
17. Carroll, C. A., Vohs, J. L., O'Donnell, B. F., Shekhar, A., and Hetrick, W. P. (2007). Sensorimotor gating in manic and mixed episode bipolar disorder. Bipolar Disord. 9, 221-229. doi: 10.1111/j.1399-5618.2007.00415.x.
18. Casetta, I., Ciorba, A., Cesnik, E., Trevisi, P., Tugnoli, V., and Bovo, R. (2011). West Nile virus neuroinvasive disease presenting with acute flaccid paralysis and bilateral sensorineural hearing loss. J. Neurol. 258, 1880-1881. doi: 10.1007/s00415-011-6011-3.
19. Castellanos, F. X., Fine, E. J., Kaysen, D., Marsh, W. L., Rapoport, J. L., and Hallett, M. (1996). Sensorimotor gating in boys with Tourette's syndrome and ADHD: preliminary results. Biol. Psychiatry 39, 33-41. doi: 10.1016/0006-3223(95)00101-8.
20. CDC (2010). Arboviral Encephalitis Cases Reported in Humans by Virus, United States, 1964-2010. Available at: http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm-content_area.
21. CDC (2012). West nile virus disease and other arboviral diseases, United States, 2011. MMWR Morb. Mortal. Wkly. Rep. 61, 510-514.
22. CDC (2013). West nile virus disease and other arboviral diseases, United States, 2011. MMWR Morb. Mortal. Wkly. Rep. 62, 513-517.
23. Chauhan, P. S., Misra, U. K., Kalita, J., Chandravanshi, L. P., and Khanna, V. K. (2016). Memory and learning seems to be related to cholinergic dysfunction in the JE rat model. Physiol. Behav. 156, 148-155. doi: 10.1016/j.physbeh.2016.01.006.
24. Chusri, S., Siripaitoon, P., Hirunpat, S., and Silpapojakul, K. (2011). Case reports of neuro-Chikungunya in southern Thailand. Am. J. Trop. Med. Hyg. 85, 386-389. doi: 10.4269/ajtmh.2011.10-0725.
25. Cohn, J. E., and Kuida, H. (1962). Primary alveolar hypoventilation associated with Western equine encephalitis. Ann. Intern. Med. 56, 633-644. doi: 10.7326/0003-4819-56-4-633.
26. Crawley, J. N. (2007). What's Wrong with My Mouse: Behavioral Phenotyping of Transgenic and Knockout Mice. Hoboken, NJ: John Wiley & Sons, Inc.
27. Das, S., and Basu, A. (2008). Japanese encephalitis virus infects neural progenitor cells and decreases their proliferation. J. Neurochem. 106, 1624-1636. doi: 10.1111/j.1471-4159.2008.05511.x.
28. Davis, M., Gendelman, D. S., Tischler, M. D., and Gendelman, P. M. (1982a). A primary acoustic startle circuit: lesion and stimulation studies. J. Neurosci. 2, 791-805.
29. Davis, M., Parisi, T., Gendelman, D. S., Tischler, M., and Kehne, J. H. (1982b). Habituation and sensitization of startle reflexes elicited electrically from the brainstem. Science 218, 688-690. doi: 10.1126/science.7134967.
30. Deaton, A. V., Craft, S., and Skenazy, J. (1986). Enduring psychiatric and neuropsychologic sequelae in the post-encephalitis patient. Int. J. Psychiatry Med. 16, 275-280. doi: 10.2190/RV2Q-UKFW-UY9L-5D8H.
31. Earnest, M. P., Goolishian, H. A., Calverley, J. R., Hayes, R. O., and Hill, H. R. (1971). Neurologic, intellectual, and psychologic sequelae following western encephalitis. A follow-up study of 35 cases. Neurology 21, 969-974. doi: 10.1212/WNL.21.9.969.
32. Fendt, M., Li, L., and Yeomans, J. S. (2001). Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology (Berl.) 156, 216-224. doi: 10.1007/s002130100794.
33. Finley, K. H., and Chapman, W. M. (1953). The 1952 outbreak of encephalitis in California; long term neurologic and psychiatric studies of sequelae. Calif. Med. 79, 94-96.
34. Forrester, N. L., Kenney, J. L., Deardorff, E., Wang, E., and Weaver, S. C. (2008). Western Equine Encephalitis submergence: lack of evidence for a decline in virus virulence. Virology 380, 170-172. doi: 10.1016/j.virol.2008.08.012.
35. Forrester, N. L., Palacios, G., Tesh, R. B., Savji, N., Guzman, H., Sherman, M., et al. (2012). Genome-scale phylogeny of the alphavirus genus suggests a marine origin. J. Virol. 86, 2729-2738. doi: 10.1128/JVI.05591-11.
36. Fulton, J. S., and Burton, A. N. (1953). After effects of western equine encephalomyelitis infection in man. Can. Med. Assoc. J. 69, 268-272.
37. Gottfried, K., Quinn, R., and Jones, T. (2005). Clinical description and follow-up investigation of human West Nile virus cases. South Med. J. 98, 603-606. doi: 10.1097/01.SMJ.0000155633.43244.AC.
38. Greiser-Wilke, I., Moenning, V., Kaaden, O. R., and Figueiredo, L. T. (1989). Most alphaviruses share a conserved epitopic region on their nucleocapsid protein. J. Gen. Virol. 70(Pt 3), 743-748. doi: 10.1099/0022-1317-70-3-743.
39. Griffin, D. E. (2007). "Alphaviruses," in Fields Virology, eds D. L. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, et al. (Philadelphia, PA: Lippincott Williams & Wilkins), 1001-1067.
40. Grillon, C., Ameli, R., Charney, D. S., Krystal, J., and Braff, D. (1992). Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol. Psychiatry 32, 939-943. doi: 10.1016/0006-3223(92)90183-Z.
41. Hanson, R. P. (1957). An epizootic of equine encephalomyelitis that occurred in Massachusetts in 1831. Am. J. Trop. Med. Hyg. 6, 858-862.
42. Hart, J. Jr., Tillman, G., Kraut, M. A., Chiang, H. S., Strain, J. F., Li, Y., et al. (2014). West Nile virus neuroinvasive disease: neurological manifestations and prospective longitudinal outcomes. BMC Infect. Dis. 14:248. doi: 10.1186/1471-2334-14-248.
43. Hasbun, R., Garcia, M. N., Kellaway, J., Baker, L., Salazar, L., Woods, S. P., et al. (2016). West nile virus retinopathy and associations with long term neurological and neurocognitive sequelae. PLoS ONE 11:e0148898. doi: 10.1371/journal.pone.0148898.
44. Herzon, H., Shelton, J. T., and Bruyn, H. B. (1957). Sequelae of western equine and other arthropod-borne encephalitides. Neurology 7, 535-548. doi: 10.1212/WNL.7.8.535.
45. Hossain, M. J., Gurley, E. S., Montgomery, S., Petersen, L., Sejvar, J., Fischer, M., et al. (2010). Hospital-based surveillance for Japanese encephalitis at four sites in Bangladesh, 2003-2005. Am. J. Trop. Med. Hyg. 82, 344-349. doi: 10.4269/ajtmh.2010.09-0125.
46. Kakoti, G., Dutta, P., Ram Das, B., Borah, J., and Mahanta, J. (2013). Clinical profile and outcome of Japanese encephalitis in children admitted with acute encephalitis syndrome. Biomed Res. Int. 2013, 152656. doi: 10.1155/2013/152656.
47. Kesler, R. A. (1933). Mosquitoes as vectors of the virus of equine encephalomyelitis. J. Am. Vet. Med. Assoc. 82, 767-771.
48. Klee, A. L., Maidin, B., Edwin, B., Poshni, I., Mostashari, F., Fine, A., et al. (2004). Long-term prognosis for clinical West Nile virus infection. Emerg. Infect. Dis. 10, 1405-1411. doi: 10.3201/eid1008.030879.
49. Koch, M. (1999). The neurobiology of startle. Prog. Neurobiol. 59, 107-128. doi: 10.1016/S0301-0082(98)00098-7.
50. Koch, M., and Schnitzler, H. U. (1997). The acoustic startle response in rats-circuits mediating evocation, inhibition and potentiation. Behav. Brain Res. 89, 35-49. doi: 10.1016/S0166-4328(97)02296-1.
51. Kohl, S., Heekeren, K., Klosterkotter, J., and Kuhn, J. (2013). Prepulse inhibition in psychiatric disorders-apart from schizophrenia. J. Psychiatr. Res. 47, 445-452. doi: 10.1016/j.jpsychires.2012.11.018.
52. Kubes, V., and Rios, F. A. (1939). The causative agent of infectious equine encephalomyelitis in Venezuela. Science 90, 20-21. doi: 10.1126/science.90.2323.20.
53. Kumar, V., Abbas, A. K., Fausto, N., and Aster, J. C. (2010). Pathologic Basis of Disease. Philadelphia, PA: Saunders, Elsevier Inc.
54. Kumari, V., Soni, W., and Sharma, T. (1999). Normalization of information processing deficits in schizophrenia with clozapine. Am. J. Psychiatry 156, 1046-1051.
55. LaBeaud, A. D., Lisgaris, M. V., King, C. H., and Mandalakas, A. M. (2006). Pediatric West Nile virus infection: neurologic disease presentations during the 2002 epidemic in Cuyahoga County, Ohio. Pediatr. Infect. Dis. J. 25, 751-753. doi: 10.1097/01.inf.0000227830.73271.65.
56. Madden, K. (2003). West Nile virus infection and its neurological manifestations. Clin. Med. Res. 1, 145-150. doi: 10.3121/cmr.1.2.145.
57. McBride, W., Gill, K. R., and Wiviott, L. (2006). West Nile Virus infection with hearing loss. J. Infect. 53, e203-e205. doi: 10.1016/j.jinf.2006.01.017.
58. McKinney, R. W., Berge, T. O., Sawyer, W. D., Tigertt, W. D., and Crozier, D. (1963). Use of an attenuated strain of Venezuelan equine encephalomyelitis virus for immunization in man. Am. J. Trop. Med. Hyg. 12, 597-603.
59. Meyer, K. F., Haring, C. M., and Howitt, B. (1931). The etiology of epizootic encephalomyelitis of horses in the San Joaquin valley, 1930. Science 74, 227-228. doi: 10.1126/science.74.1913.227.
60. Morjaria, S., Arguello, E., Taur, Y., Sepkowitz, K., Hatzoglou, V., Nemade, A., et al. (2015). West Nile virus central nervous system infection in patients treated with rituximab: implications for diagnosis and prognosis, with a review of literature. Open Forum Infect. Dis. 2:ofv136. doi: 10.1093/ofid/ofv136.
61. Mulder, D. W., Parrott, M., and Thaler, M. (1951). Sequelae of western equine encephalitis. Neurology 1, 318-327. doi: 10.1212/WNL.1.7-8.318.
62. Murray, K. O., Garcia, M. N., Rahbar, M. H., Martinez, D., Khuwaja, S. A., Arafat, R. R., et al. (2014). Survival analysis, long-term outcomes, and percentage of recovery up to 8 years post-infection among the Houston West Nile virus cohort. PLoS ONE 9:e102953. doi: 10.1371/journal.pone.0102953.
63. Nalca, A., Fellows, P. F., and Whitehouse, C. A. (2003). Vaccines and animal models for arboviral encephalitides. Antiviral Res. 60, 153-174. doi: 10.1016/j.antiviral.2003.08.001.
64. Paessler, S., Aguilar, P., Anishchenko, M., Wang, H. Q., Aronson, J., Campbell, G., et al. (2004). The hamster as an animal model for eastern equine encephalitis-and its use in studies of virus entrance into the brain. J. Infect. Dis. 189, 2072-2076. doi: 10.1086/383246.
65. Paessler, S., Ni, H., Petrakova, O., Fayzulin, R. Z., Yun, N., Anishchenko, M., et al. (2006). Replication and clearance of Venezuelan equine encephalitis virus from the brains of animals vaccinated with chimeric SIN/VEE viruses. J. Virol. 80, 2784-2796. doi: 10.1128/JVI.80.6.2784-2796.2006.
66. Paessler, S., Yun, N. E., Judy, B. M., Dziuba, N., Zacks, M. A., Grund, A. H., et al. (2007). Alpha-beta T cells provide protection against lethal encephalitis in the murine model of VEEV infection. Virology 367, 307-323. doi: 10.1016/j.virol.2007.05.041.
67. Palmer, R. J., and Finley, K. H. (1956). Sequelae of encephalitis; report of a study after the California epidemic. Calif. Med. 84, 98-100.
68. Patel, H., Sander, B., and Nelder, M. P. (2015). Long-term sequelae of West Nile virus-related illness: a systematic review. Lancet Infect. Dis. 15, 951-959. doi: 10.1016/S1473-3099(15)00134-6.
69. Pearce, B. D., Hubbard, S., Rivera, H. N., Wilkins, P. P., Fisch, M. C., Hopkins, M. H., et al. (2013). Toxoplasma gondii exposure affects neural processing speed as measured by acoustic startle latency in schizophrenia and controls. Schizophr. Res. 150, 258-261. doi: 10.1016/j.schres.2013.07.028.
70. Rampal, Sharda, M., and Meena, H. (2007). Neurological complications in Chikungunya fever. J. Assoc. Physicians India 55, 765-769.
71. Reddy, A. J., Woods, C. W., and Welty-Wolf, K. E. (2008). Eastern equine encephalitis leading to multi-organ failure and sepsis. J. Clin. Virol. 42, 418-421. doi: 10.1016/j.jcv.2008.03.008.
72. Rich, B. A., Vinton, D., Grillon, C., Bhangoo, R. K., and Leibenluft, E. (2005). An investigation of prepulse inhibition in pediatric bipolar disorder. Bipolar Disord. 7, 198-203. doi: 10.1111/j.1399-5618.2005.00183.x.
73. Rivas, F., Diaz, L. A., Cardenas, V. M., Daza, E., Bruzon, L., Alcala, A., et al. (1997). Epidemic Venezuelan equine encephalitis in La Guajira, Colombia, 1995. J. Infect. Dis. 175, 828-832.
74. Rogers, D. C., Fisher, E. M. C., Brown, S. D. M., Peters, J., Hunter, A. J., and Martin, J. E. (1997). Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm. Genome 8, 711-713. doi: 10.1007/s003359900551.
75. Silverman, M. A., Misasi, J., Smole, S., Feldman, H. A., Cohen, A. B., Santagata, S., et al. (2013). Eastern equine encephalitis in children, Massachusetts and New Hampshire, USA, 1970-2010. Emerg. Infect. Dis. 19, 194-201. doi: 10.3201/eid1902.120039.
76. Steele, K. E., and Twenhafel, N. A. (2010). REVIEW PAPER: pathology of animal models of alphavirus encephalitis. Vet. Pathol. 47, 790-805. doi: 10.1177/0300985810372508.
77. Suarez, O. M., and Bergold, G. H. (1968). Investigations of an outbreak of Venezuelan equine encephalitis in towns of eastern Venezuela. Am. J. Trop. Med. Hyg. 17, 875-880.
78. Swerdlow, N. R., Braff, D. L., and Geyer, M. A. (1999). Cross-species studies of sensorimotor gating of the startle reflex. Ann. N. Y. Acad. Sci. 877, 202-216. doi: 10.1111/j.1749-6632.1999.tb09269.x.
79. Swerdlow, N. R., Geyer, M. A., and Braff, D. L. (2001). Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl.) 156, 194-215. doi: 10.1007/s002130100799.
80. Taylor, K., Borisevich, V., Kolokoltsova, O., Smith, J., Smith, J., Estes, M., et al. (2011). Identification of novel immune factors regulating outcome to viral encephalitis. J. Immun. 186(Supp. 1), 170.12.
81. Taylor, K., Kolokoltsova, O., Patterson, M., Poussard, A., Smith, J., Estes, D. M., et al. (2012). Natural killer cell mediated pathogenesis determines outcome of central nervous system infection with Venezuelan equine encephalitis virus in C3H/HeN mice. Vaccine 30, 4095-4105. doi: 10.1016/j.vaccine.2012.03.076.
82. Tenbroeck, C., and Merrill, M. H. (1933). A serological difference between eastern and western equine encephalomyelitis virus. Proc. Soc. Exp. Biol. Med. 31, 217-220. doi: 10.3181/00379727-31-7066C.
83. Tigertt, W. D., Berge, T. O., and Downs, W. G. (1962). Studies on the virus of Venezuelan equine encephalomyelitis in Trinidad, W.I. II. Serological status of human beings, 1954-1958. Am. J. Trop. Med. Hyg. 11, 835-840.
84. Villari, P., Spielman, A., Komar, N., McDowell, M., and Timperi, R. J. (1995). The economic burden imposed by a residual case of eastern encephalitis. Am. J. Trop. Med. Hyg. 52, 8-13.
85. Voss, K., Amaya, M., Mueller, C., Roberts, B., Kehn-Hall, K., Bailey, C., et al. (2014). Inhibition of host extracellular signal-regulated kinase (ERK) activation decreases new world alphavirus multiplication in infected cells. Virology 46, 490-503. doi: 10.1016/j.virol.2014.09.005.
86. Weatherhead, J. E., Miller, V. E., Garcia, M. N., Hasbun, R., Salazar, L., Dimachkie, M. M., et al. (2015). Long-term neurological outcomes in West Nile virus-infected patients: an observational study. Am. J. Trop. Med. Hyg. 92, 1006-1012. doi: 10.4269/ajtmh.14-0616.
87. Weike, A. I., Bauer, U., and Hamm, A. O. (2000). Effective neuroleptic medication removes prepulse inhibition deficits in schizophrenia patients. Biol. Psychiatry 47, 61-70. doi: 10.1016/S0006-3223(99)00229-2.
88. White, D. P., Miller, F., and Erickson, R. W. (1983). Sleep apnea and nocturnal hypoventilation after western equine encephalitis. Am. Rev. Respir. Dis. 127, 132-133. doi: 10.1164/arrd.1983.127.1.132.
89. Winkelmann, E. R., Luo, H., and Wang, T. (2016). West nile virus infection in the central nervous system. F1000Res. 5(F1000 Faculty Rev):105. doi: 10.12688/f1000research.7404.1.
90. Yin, Z., Wang, X., Li, L., Li, H., Zhang, X., Li, J., et al. (2015). Neurological sequelae of hospitalized Japanese encephalitis cases in Gansu province, China. Am. J. Trop. Med. Hyg. 92, 1125-1129. doi: 10.4269/ajtmh.14-0148.
91. Zacks, M. A., and Paessler, S. (2010). Encephalitic alphaviruses. Vet. Microbiol. 140, 281-286. doi: 10.1016/j.vetmic.2009.08.023.