• 1

    Moore J, 2002. Parasites and the Behavior of Animals. Oxford: Oxford University Press.

  • 2

    Combes C, 2001. Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago: University of Chicago Press.

  • 3

    Klein SL, 2003. Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79: 441–449.

    • Search Google Scholar
    • Export Citation
  • 4

    Plyusnin A, Morzunov SP, 2001. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 256: 47–75.

    • Search Google Scholar
    • Export Citation
  • 5

    Schmaljohn CS, Hjelle B, 1997. Hantaviruses: a global disease problem. Emerg Infect Dis 3 :95–104.

  • 6

    Dohmae K, Okabe M, Nishimune Y, 1994. Experimental transmission of hantavirus infection in laboratory rats. J Infect Dis 170: 1589–1592.

    • Search Google Scholar
    • Export Citation
  • 7

    Glass GE, Childs JE, Korch GW, LeDuc JW, 1988. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus).Epidemiol Infect 101: 459–472.

    • Search Google Scholar
    • Export Citation
  • 8

    Lee PW, Yanagihara R, Gibbs CJ, Gajdusek DC, 1986. Pathogenesis of experimental Hantaan virus infection in laboratory rats. Arch Virol 88: 57–66.

    • Search Google Scholar
    • Export Citation
  • 9

    Nuzum EO, Rossi CA, Stephenson EH, LeDuc JW, 1988. Aerosol transmission of Hantaan and related viruses to laboratory rats. Am J Trop Med Hyg 38: 636–640.

    • Search Google Scholar
    • Export Citation
  • 10

    Bernshtein AD, Apekina NS, Mikhailova TV, Myasnikov YA, Khlyap LA, Korotkov YS, Gavrilovskaya IN, 1999. Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrionomys glareolus).Arch Virol 144: 2415–2428.

    • Search Google Scholar
    • Export Citation
  • 11

    Glass GE, Livingstone W, Mills JN, Hlady G, Fine JB, Biggler W, Coke T, Frazier D, Atherley S, Rollin PE, Ksiazek TG, Peters CJ, Childs JE, 1998. Black creek canal virus infection in Sigmodon hispidus in southern Florida. Am J Trop Med Hyg 59: 699–703.

    • Search Google Scholar
    • Export Citation
  • 12

    Childs JE, Ksiazek TG, Spiropoulou CF, Krebs JW, Morzunov S, Maupin GO, Gage KL, Rollin PE, Sarisky J, Enscore RE, Frey JK, Peters CJ, Nichol ST, 1994. Serologic and genetic identification of Peromyscus maniculatus as the primary reservoir for a new hantavirus in the southwest United States. J Infect Dis 169: 1271–1280.

    • Search Google Scholar
    • Export Citation
  • 13

    Mills JN, Ksiazek TG, Ellis BA, Rollin PE, Nichol ST, Yates TL, Gannon WL, Levy CE, Engelthaler DM, Davis T, Tanda DT, Frampton JW, Nichols CR, Peters CJ, Childs JE, 1997. Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am J Trop Med Hyg 56: 273–284.

    • Search Google Scholar
    • Export Citation
  • 14

    Weigler BJ, Ksiazek TG, Vandenbergh JG, Levin M, Sullivan WT, 1996. Serological evidence for zoonotic hantaviruses in North Carolina rodents. J Wildl Dis 32: 354–357.

    • Search Google Scholar
    • Export Citation
  • 15

    Bennett SG, Webb JP Jr, Madon MB, Childs JE, Ksiazek TG, Torrez-Martinez M, Hjelle B, 1999. Hantavirus (Bunyaviridae) infections in rodents from Orange and San Diego counties, California. Am J Trop Med Hyg 60: 75–84.

    • Search Google Scholar
    • Export Citation
  • 16

    Root JJ, Calisher CH, Beaty BJ, 1999. Relationships of deer mouse movement, vegetative structure, and prevalence of infection with Sin Nombre virus. J Wildl Dis 35: 311–318.

    • Search Google Scholar
    • Export Citation
  • 17

    Klein SL, Zink MC, Glass GE, 2003. Seoul virus infection increases aggressive behaviour in male Norway rats. Anim Behav (in press).

  • 18

    Escutenaire S, Chalon P, de Jaegere F, Karelle-Bui L, Mees G, Brochier B, Rozenfeld F, Pastore P-P, 2002. Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus).Emerg Infect Dis 8: 930–936.

    • Search Google Scholar
    • Export Citation
  • 19

    Meyer BJ, Schmaljohn CS, 2000. Persistent hantavirus infections: characteristics and mechanisms. Trends Microbiol 8: 61–67.

  • 20

    Klein SL, Bird BH, Glass GE, 2000. Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J Virol 74: 8213–8217.

    • Search Google Scholar
    • Export Citation
  • 21

    Klein SL, Bird BH, Glass GE, 2001. Sex differences in immune responses and viral shedding following Seoul virus infection in Norway rats. Am J Trop Med Hyg 65: 57–63.

    • Search Google Scholar
    • Export Citation
  • 22

    Klein SL, Marson AL, Scott AL, Ketner G, Glass GE, 2002. Neonatal sex steroids affect responses to Seoul virus infection in male, but not female, Norway rats. Brain Behav Immun 16: 736–746.

    • Search Google Scholar
    • Export Citation
  • 23

    Hutchinson KL, Rollin PE, Shieh WJ, Zaki S, Greer PW, Peters CJ, 2000. Transmission of Black Creek Canal virus between Cotton rats. J Med Virol 60: 70–76.

    • Search Google Scholar
    • Export Citation
  • 24

    Botten J, Mirowsky K, Kusewitt D, Bharadwaj M, Yee J, Ricci R, Feddersen RM, Hjelle B, 2000. Experimental infection model for Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus).Proc Natl Acad Sci USA 97: 10578–10583.

    • Search Google Scholar
    • Export Citation
  • 25

    Kariwa H, Kamimura M, Arikawa J, Yoshimatsu K, Takashima I, Hashimoto N, 1995. Characterization of the mode of Hantaan virus infection in adult mice using a nested reverse transcriptase polymerase chain reaction: transient virus replication in adult mice. Microbiol Immunol 39: 35–41.

    • Search Google Scholar
    • Export Citation
  • 26

    Kawamura K, Zhang XK, Arikawa J, Takashima I, Dempo K, Hashimoto N, 1991. Susceptibility of laboratory and wild rodents to Rattus or Aopdemus-type hantaviruses. Acta Virol 35: 54–63.

    • Search Google Scholar
    • Export Citation
  • 27

    Klein SL, Bird BH, Nelson RJ, Glass GE, 2002. Environmental and physiological factors associated with Seoul virus infection among urban populations of Norway rats. J Mammal 83: 478–488.

    • Search Google Scholar
    • Export Citation
  • 28

    Davis DE, 1953. The characteristics of rat populations. Q Rev Biol 28: 373–401.

  • 29

    Bodner L, Baum BJ, 1985. Characteristics of stimulated parotid gland secretion in the aging rat. Mech Ageing Dev 31: 337–342.

  • 30

    Arthur RR, Lofts RS, Gomez J, Glass GE, LeDuc JW, Childs JE, 1992. Grouping of hantaviruses by small (S) genome segment polymerase chain reaction and amplification of viral RNA from wild-caught rats. Am J Trop Med Hyg 47: 210–224.

    • Search Google Scholar
    • Export Citation
  • 31

    Ruo SL, Sanchez A, Elliott LH, Brammer LS, McCormick JB, Fisher-Hoch SP, 1991. Monoclonal antibodies to three strains of hantaviruses: Hantaan, R22, Puumala. Arch Virol 199: 1–11.

    • Search Google Scholar
    • Export Citation
  • 32

    Moshkin M, Gerlinskaya L, Morozova O, Bakhvalova V, Evsikov V, 2002. Behavior, chemosignals, and endocrine function in male mice infected with tick-borne encephalitis virus. Psychoneuroendocrinology 27: 603–608.

    • Search Google Scholar
    • Export Citation
  • 33

    Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ, 1993. Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav Brain Res 58: 113–121.

    • Search Google Scholar
    • Export Citation
  • 34

    Romero LM, Ramenofsky M, Wingfield JC, 1997. Season and migration alters the corticosterone response to capture and handling in an Artic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelii).Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 116: 171–177.

    • Search Google Scholar
    • Export Citation
  • 35

    Borucki MK, Boone JD, Rowe JE, Bohlman MC, Kuhn EA, DeBaca R, St. Jeor SC, 2000. Role of maternal antibody in natural infection of Peromyscus maniculatus with Sin Nombre virus. J Virol 74: 2426–2429.

    • Search Google Scholar
    • Export Citation
  • 36

    Dohmae K, Koshimizu U, Nishimune Y, 1993. In utero and mammary transfer of hantavirus antibody from dams to infant rats. Lab Anim Sci 43 :557–561.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

WOUNDING: THE PRIMARY MODE OF SEOUL VIRUS TRANSMISSION AMONG MALE NORWAY RATS

View More View Less
  • 1 The W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; Department of Comparative Medicine, The Johns Hopkins School of Medicine, Baltimore, Maryland

In rodent populations, males are more likely to be infected with hantaviruses and to engage in aggression than are females. To assess the relationship between aggression and Seoul virus infection, Norway rats were trapped in Baltimore, Maryland and wounding, infection status, and steroid hormone concentrations were examined. Older males and males with high-grade wounds were more likely to have IgG antibody to Seoul, to shed virus in saliva, urine, and feces, and to have viral RNA in organs than either juveniles or adult males with less severe wounds. In contrast, neither age nor wounding predicted virus shedding among females. Although viral antigen was not identified in the brain, viral protein was detected in the gonads and adrenal glands of adult males. Males with more severe wounds had higher testosterone concentrations than males with no or low-grade wounds. Because wounding, testosterone, and virus shedding are associated among males, aggression may be the primary mode of Seoul virus transmission among male, but not female, Norway rats.

Save