CHRONIC ST. LOUIS ENCEPHALITIS VIRUS INFECTION IN THE GOLDEN HAMSTER (MESOCRICETUS AURATUS)

MARINA T. SIIRIN Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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TAO DUAN Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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HAO LEI Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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HILDA GUZMAN Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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AMELIA P. A. TRAVASSOS DA ROSA Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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DOUGLAS M. WATTS Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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SHU-YUAN XIAO Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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ROBERT B. TESH Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas

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To further study the phenomenon of flavivirus persistent infection, golden hamsters (Mesocricetus auratus) were inoculated intraperitoneally with a low pathogenicity strain of St. Louis encephalitis virus (SLEV). After inoculation, the animals remained asymptomatic and developed high levels of specific neutralizing antibodies in their sera. However, about one half of the hamsters continued to shed infectious SLEV in their urine for prolonged periods of time. By co-cultivation, SLEV was recovered from selected tissues (kidney, lung, and brain) of some of the animals for up to 185 days after initial infection. Although no specific histopathologic changes were observed in these tissues, SLEV antigen was shown by immunohistochemistry in the interstitium and tubular epithelium of the renal cortex and in a few large neurons of the cerebral cortex. Seventeen SLEV isolates from urine and tissues of the chronically infected hamsters were sequenced. In comparison with the infecting parent SLEV strain, two common mutations and amino acid substitutions were observed in all of the hamster isolates. The findings of this study were very similar to previous descriptions of chronic West Nile, Modoc, and tick-borne encephalitis virus infections in mammals, and they re-emphasize the potential importance of persistent flavivirus infection in vertebrates.

Author Notes

Reprint requests: Robert B. Tesh, Department of Pathology, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555-0609. E-mail: rtesh@utmb.edu.
  • 1

    Monath TP, 1980. Epidemiology. Monath TP, ed. St. Louis Encephalitis. Washington, DC: American Public Health Association, 239–312.

    • PubMed
    • Export Citation
  • 2

    Reisen WK, 2003. Epidemiology of St. Louis encephalitis virus. Adv Virus Res 61 :139–183.

  • 3

    Thiel HJ, Collett MS, Gould EA, Heinz FX, Houghton M, Myers G, Purcell RH, Rice CM, 2005. Family Flaviviridae. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, eds. Virus Taxonomy: Classification and Nomenclature of Viruses. Eight Report of the International Committee on the Taxonomy of Viruses. San Diego: Elsevier Academic Press, 981–998.

    • PubMed
    • Export Citation
  • 4

    Endy TP, Nisalak A, 2002. Japanese encephalitis virus: ecology and epidemiology. Cur Topics Microbiol Immunol 267 :11–48.

  • 5

    Komar N, 2003. West Nile virus: epidemiology and ecology in North American. Adv Virus Res 61 :185–234.

  • 6

    Murgue B, Zeller H, Deubel V, 2002. The ecology and epidemiology of West Nile virus in Africa, Europe and Asia. Cur Topics Microbiol Immunol 267 :195–221.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Marshall ID, 1988. Murray Valley and Kunjin encephalitis. Monath TP, ed. The Arboviruses: Epidemiology and Ecology. Vol. 3. Boca Raton: CRC Press, 151–189.

    • PubMed
    • Export Citation
  • 8

    Brinker KR, Monath TP, 1980. The acute disease. Monath TP, ed. St. Louis Encephalitis. Washington, DC: American Public Health Association, 503–534.

    • PubMed
    • Export Citation
  • 9

    Sejvar JJ, Bode AV, Curiel M, Marfin AA, 2004. Post-infectious encephalomyelitis associated with St. Louis encephalitis virus infection. Neurology 63 :1719–1721.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Quick DT, Thompson JM, Bond JO, 1965. The 1962 epidemic of St. Louis encephalitis in Florida. IV. Clinical features of cases in the Tampa Bay area. Am J Epidemiol 81 :415–427.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Luby JP, Murphy FK, Gilliam JN, Kang CY, Frank R, 1980. Antigenuria in St. Louis encephalitis. Am J Trop Med Hyg 29 :265–268.

  • 12

    Tesh RB, Siirin M, Guzman H, Travassos da Rosa APA, Wu X, Duan T, Lei H, Nunes MR, Xiao SY, 2005. Persistent West Nile virus infection in the golden hamster: Studies on its mechanism and possible implications for other flavivirus infections. J Infect Dis 192 :287–295.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Tonry JH, Xiao SY, Siirin M, Chen H, Travassos da Rosa APA, Tesh RB, 2005. Persistent shedding of West Nile virus in urine of experimentally infected hamsters. Am J Trop Med Hyg 72 :320–324.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Tonry JH, Brown CB, Cropp CB, Co JK, Bennett SN, Nerukar VR, Kuberski T, Gubler DJ, 2005. West Nile virus detection in urine. Emerg Infect Dis 11 :1294–1296.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Causey OR, Shope RE, Theiler M, 1964. Isolation of St. Louis encephalitis virus from arthropods in Para, Brazil. Am J Trop Med Hyg 13 :449.

  • 16

    Beaty BJ, Calisher CH, Shope RE, 1945. Arboviruses. Lennette EH, Lennette DA, Lennette ET, eds. Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections. Seventh edition. Washington, DC: American Public Health Association, 189–212.

    • PubMed
    • Export Citation
  • 17

    Xiao SY, Guzman H, Zhang H, Travassos da Rosa APA, Tesh RB, 2001. West Nile virus infection in the golden hamster (Mesocricetus auratus): A model for West Nile encephalitis. Emerg Infect Dis 7 :714–721.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Xiao SY, Zhang H, Guzman H, Tesh RB, 2001. Experimental yellow fever virus infection in the golden hamster (Mesocricetus auratus). 2. Pathology. J Infect Dis 183 :1437–1444.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Kramer LD, Chandler LJ, 2001. Phylogenetic analysis of the envelope gene of St. Louis encephalitis virus. Arch Virol 146 :2341–2355.

  • 20

    Ding X, Wu X, Duan T, Siirin M, Guzman H, Yang Z, Tesh RB, Xiao SY, 2005. Nucleotide and amino acid changes in West Nile virus strains exhibiting renal tropism in hamsters. Am J Trop Med Hyg 73 :803–807.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Percy DH, Barthold SW, 2001. Pathology of Laboratory Rodents and Rabbits. Second edition. Ames: Iowa State Press.

    • PubMed
    • Export Citation
  • 22

    Van Marck EAE, Jacob W, Deelder AM, Gigase PLJ, 1978. Spontaneous glomerular basement membrane changes in the golden Syrian hamster (Mesocricetus auratus): A light and electron microscope study. Lab Anim 12 :207–211.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Bhardwaj S, Holbrook M, Shope RE, Barrett ADT, Watowich CJ, 2001. Biophysical characterization and vector-specific antagonist activity of Domain III of the tick-borne flavivirus envelope protein. J Virol 75 :4002–4007.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Roehrig JT, 2003. Antigenic structure of flavivirus proteins. Adv Virus Res 59 :141–175.

  • 25

    Reisen WK, Chiles RE, Martinez VM, Fang Y, Green EN, 2003. Experimental infection of California birds with western equine encephalomyelitis and St. Louis encephalitis viruses. J Med Entomol 40 :968–982.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Monath TP, Croop CB, Bowen GS, Kemp GE, Mitchell CJ, Gardner JJ, 1980. Variation in virulence for mice and rhesus monkeys among St. Louis encephalitis strains of different origins. Am J Trop Med Hyg 29 :948–962.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Tesh RB, Travassos da Rosa APA, Guzman H, Araujo TP, Xiao SY, 2002. Immunization with heterologous flaviviruses protective against fatal West Nile encephalitis. Emerg Infect Dis 8 :245–251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Slavin HB, 1943. Persistence of the virus of St. Louis encephalitis in the central nervous system of mice for over five months. J Bacteriol 46 :113–116.

  • 29

    Pogodina VV, Frolova MP, Malenko GV, Fokina GI, Koreshkova GV, Kiseleva LL, Bochkova NG, Ralph NM, 1983. Study on West Nile virus persistence in monkeys. Arch Virol 75 :71–86.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Mathur A, Arora KL, Rawat S, Chaturvedi UC, 1986. Persistence, latency and reactivation of Japanese encephalitis in mice. J Gen Virol 67 :381–385.

  • 31

    Sharms S, Mathur A, Prakash V, Kulshreshtha R, Kumar R, Chaturvedi UC, 1991. Japanese encephalitis virus latency in peripheral blood lymphocytes and recurrence of infection in children. Clin Exp Immunol 85 :85–89.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Ravi V, Desai AS, Shenoy PK, Satishchandra P, Chandramuki A, Gouri-Devi M, 1993. Persistence of Japanese encephalitis virus in the human nervous system. J Med Virol 40 :326–329.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Pogodina VV, Frolova MP, Malenko GV, Fokina GI, Levina LS, Mamonenko LL, Koreshkova GV, Ralf NM, 1981. Persistence of tick-borne encephalitis virus in monkeys. 1. Features of experimental infection. Acta Virol 25 :337–343.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Gritsun TS, Frolova TV, Zhankov AI, Armesto M, Turner SL, Frolova MP, Pogodina VV, Lashkevich VA, Gould EA, 2003. Characterization of a Siberian virus isolated from a patient with progressive chronic tick-borne encephalitis. J Virol 77 :25–36.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Johnson HN, 1970. Long-term persistence of Modoc virus in hamster kidney cells: in vivo and in vitro demonstration. Am J Trop Med Hyg 19: 537–539.

  • 36

    Davis JW, Hardy JL, 1974. Characterization of persistent Modoc viral infection in Syrian hamsters. Infect Immun 10 :328–334.

  • 37

    Davis JW, Hardy JL, Reeves WC, 1974. Modoc viral infections in the deer mouse Peromyscus maniculatus. Infect Immun 10 :1362–1369.

  • 38

    Constatine DG, Woodall DF, 1964. Latent infection of Rio Bravo virus in salivary glands of bats. Public Health Rep 79 :1033–1039.

  • 39

    Kharitonova NN, Leonov YA, 1985. Omsk Hemorrhagic Fever: Ecology of the Agent and Epizootiology (in Russian). New Delhi: Amerind.

    • PubMed
    • Export Citation
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