Pteropid Bats are Confirmed as the Reservoir Hosts of Henipaviruses: A Comprehensive Experimental Study of Virus Transmission (original) (raw)

Print ISSN:

0002-9637

Online ISSN:

1476-1645

• Introduction
• Materials and Methods
  • Animals.
  • Viral inoculum.
  • Experimental infections.
  • Serology.
  • HeV and NiV genome Taqman polymerase chain reaction assays.
  • Virus isolation.
  • Histopathologic and immunohistochemical methods.
• Results
  • Animals.
  • Clinical observations.
  • Detection of henipavirus genome.
  • Virus isolation.
  • Postmortem.
  • Histopathology and immunohistochemistry.
  • Serology.
• Discussion

ProCite

RefWorks

Reference Manager

• 1. Young PL, Halpin K, Selleck PW, Field H, Gravel JL, Kelly MA, Mackenzie JS, 1996. Serologic evidence for the presence in Pteropus bats of a paramyxovirus related to equine morbillivirus. Emerg Infect Dis 2: 239–240.
  • PubMed
    YoungPLHalpinKSelleckPWFieldHGravelJLKellyMAMackenzieJS, 1996. Serologic evidence for the presence in Pteropus bats of a paramyxovirus related to equine morbillivirus. Emerg Infect Dis 2: 239–240.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halpin K, Young P, Field H, Mackenzie J, 2000. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81: 1927–1932.
  • PubMed
    HalpinKYoungPFieldHMackenzieJ, 2000. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81: 1927–1932.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Johara M, Field H, Rashdi A, Morrissy C, van der Heide B, Rota P, Adzhar A, White J, Daniels P, Jamaluddin A, Ksiazek T, 2001. Nipah virus infection in bats (order Chiroptera) in Peninsular Malaysia. Emerg Infect Dis 7: 439–441.
  • PubMed
    JoharaMFieldHRashdiAMorrissyCvan der HeideBRotaPAdzharAWhiteJDanielsPJamaluddinAKsiazekT, 2001. Nipah virus infection in bats (order Chiroptera) in Peninsular Malaysia. Emerg Infect Dis 7: 439–441.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chua KB, Koh CL, Hooi PS, Wee KF, Khong JH, Chua BH, Chan YP, Lim ME, Lam SK, 2002. Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4: 145–151.
  • PubMed
    ChuaKBKohCLHooiPSWeeKFKhongJHChuaBHChanYPLimMELamSK, 2002. Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4: 145–151.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Rahman SA, Hassan SS, Olival KJ, Mohamed M, Chang LY, Hassan L, Saad NM, Shohaimi SA, Mamat ZC, Naim MS, Epstein JH, Suri AS, Field HE, Daszak P; , 2010. Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerg Infect Dis 16: 1990–1993.
  • PubMed
    RahmanSAHassanSSOlivalKJMohamedMChangLYHassanLSaadNMShohaimiSAMamatZCNaimMSEpsteinJHSuriASFieldHEDaszakP; Henipavirus Ecology Research Group, 2010. Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerg Infect Dis 16: 1990–1993.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Reynes JM, Counor D, Ong S, Faure C, Seng V, Molia S, Walston J, Georges-Courbot MC, Deubel V, Sarthou JL, 2010. Nipah virus in Lyle's flying foxes, Cambodia. Emerg Infect Dis 11: 1042–1047.
  • PubMed
    ReynesJMCounorDOngSFaureCSengVMoliaSWalstonJGeorges-CourbotMCDeubelVSarthouJL, 2010. Nipah virus in Lyle's flying foxes, Cambodia. Emerg Infect Dis 11: 1042–1047.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Mungall BA, Middleton D, Crameri G, Bingham J, Halpin K, Russell G, Green D, McEachern J, Pritchard I, Eaton BT, Wang LF, Bossart KN, Broder CC, 2006. Feline model of acute Nipah virus infection and protection with a soluble glycoprotein-based subunit vaccine. J Virol 80: 12293–12302.
  • PubMed
    MungallBAMiddletonDCrameriGBinghamJHalpinKRussellGGreenDMcEachernJPritchardIEatonBTWangLFBossartKNBroderCC, 2006. Feline model of acute Nipah virus infection and protection with a soluble glycoprotein-based subunit vaccine. J Virol 80: 12293–12302.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Mungall BA, Schopman NC, Lambeth L, Doran TJ, 2008. Inhibition of Henipavirus infection by RNA interference. Antiviral Res 80: 324–331.
  • PubMed
    MungallBASchopmanNCLambethLDoranTJ, 2008. Inhibition of Henipavirus infection by RNA interference. Antiviral Res 80: 324–331.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Middleton DJ, Westbury HA, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Hyatt AD, 2002. Experimental Nipah virus infection in pigs and cats. J Comp Pathol 126: 124–136.
  • PubMed
    MiddletonDJWestburyHAMorrissyCJvan der HeideBMRussellGMBraunMAHyattAD, 2002. Experimental Nipah virus infection in pigs and cats. J Comp Pathol 126: 124–136.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Middleton DJ, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Westbury HA, Halpin K, Daniels PW, 2007. Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136: 266–272.
  • PubMed
    MiddletonDJMorrissyCJvan der HeideBMRussellGMBraunMAWestburyHAHalpinKDanielsPW, 2007. Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136: 266–272.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. van den Hurk AF, Smith CS, Field HE, Smith IL, Northill JA, Taylor CT, Jansen CC, Smith GA, Mackenzie JS, 2009. Transmission of Japanese encephalitis virus from the black flying fox, Pteropus alecto, to Culex annulirostris mosquitoes, despite the absence of detectable viremia. Am J Trop Med Hyg 81: 457–462.
  • PubMed
    van den HurkAFSmithCSFieldHESmithILNorthillJATaylorCTJansenCCSmithGAMackenzieJS, 2009. Transmission of Japanese encephalitis virus from the black flying fox, Pteropus alecto, to Culex annulirostris mosquitoes, despite the absence of detectable viremia. Am J Trop Med Hyg 81: 457–462.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Williamson M, Hooper P, Selleck P, Westbury H, Slocombe R, 1999. Experimental Hendra virus infection in pregnant guinea-pigs and fruit bats (Pteropus poliocephalus). J Comp Pathol 122: 201–207.
  • PubMed
    WilliamsonMHooperPSelleckPWestburyHSlocombeR, 1999. Experimental Hendra virus infection in pregnant guinea-pigs and fruit bats (Pteropus poliocephalus). J Comp Pathol 122: 201–207.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, Daszak P, 2011. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus species). Proceedings of the Royal Society B.
  • PubMed
    PlowrightRKFoleyPFieldHEDobsonAPFoleyJEEbyPDaszakP, 2011. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus species). Proceedings of the Royal Society B. DOI:10.1098/rspb.2011.0522
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Williamson M, Hooper P, Selleck P, Gleeson L, Daniels P, Westbury H, Murray K, 1998. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Aust Vet J 76: 813–818.
  • PubMed
    WilliamsonMHooperPSelleckPGleesonLDanielsPWestburyHMurrayK, 1998. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Aust Vet J 76: 813–818.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Leonard LL, Allen R, Sulkin SE, 1968. Bat immunoglobulins formed in response to experimental japanese B encephalitis (JBE) virus infection. J Immunol 101: 1168–1175.
  • PubMed
    LeonardLLAllenRSulkinSE, 1968. Bat immunoglobulins formed in response to experimental japanese B encephalitis (JBE) virus infection. J Immunol 101: 1168–1175.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chakravarty AK, Sarkar SK, 1994. Immunofluorescence analysis of immunoglobulin bearing lymphocytes in the Indian fruit bat: Pteropus giganteus. Lymphology 27: 97–104.
  • PubMed
    ChakravartyAKSarkarSK, 1994. Immunofluorescence analysis of immunoglobulin bearing lymphocytes in the Indian fruit bat: Pteropus giganteus. Lymphology 27: 97–104.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chakraborty AK, Chakravarty AK, 1984. Antibody-mediated immune response in the bat, Pteropus giganteus. Dev Comp Immunol 8: 415–423.
  • PubMed
    ChakrabortyAKChakravartyAK, 1984. Antibody-mediated immune response in the bat, Pteropus giganteus. Dev Comp Immunol 8: 415–423.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE, 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc R Soc Lond B Biol Sci 275: 861–869.
  • PubMed
    PlowrightRKFieldHESmithCDivljanAPalmerCTaborGDaszakPFoleyJE, 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc R Soc Lond B Biol Sci 275: 861–869.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halpin K, Hyatt AD, Plowright RK, Epstein JH, Daszak P, Field HE, Wang L, Daniels PW, , 2007. Emerging viruses: coming in on a wrinkled wing and a prayer. Clin Infect Dis 44: 711–717.
  • PubMed
    HalpinKHyattADPlowrightRKEpsteinJHDaszakPFieldHEWangLDanielsPW, Henipavirus Ecology Research Group, 2007. Emerging viruses: coming in on a wrinkled wing and a prayer. Clin Infect Dis 44: 711–717.
    )| false
  • Search Google Scholar
  • Export Citation
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Peter Daszak and the Henipavirus Ecology Research Group

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• Abstract/Excerpt
• Author Notes

Bats of the genus Pteropus have been identified as the reservoir hosts for the henipaviruses Hendra virus (HeV) and Nipah virus (NiV). The aim of these studies was to assess likely mechanisms for henipaviruses transmission from bats. In a series of experiments, Pteropus bats from Malaysia and Australia were inoculated with NiV and HeV, respectively, by natural routes of infection. Despite an intensive sampling strategy, no NiV was recovered from the Malaysian bats and HeV was reisolated from only one Australian bat; no disease was seen. These experiments suggest that opportunities for henipavirus transmission may be limited; therefore, the probability of a spillover event is low. For spillover to occur, a range of conditions and events must coincide. An alternate assessment framework is required if we are to fully understand how this reservoir host maintains and transmits not only these but all viruses with which it has been associated.

Author Notes

*Address correspondence to Alex D. Hyatt, Australian Animal Health Laboratory, Private Bag 24, Geelong, Victoria Australia 3220. E-mail: alex.hyatt@csiro.au

Financial support: This work was supported by a National Institutes of Health/National Science Foundation “Ecology of Infectious Diseases” award (R01-TW05869) from the John E. Fogarty International Center.

Authors' addresses: Kim Halpin, Life Technologies, Singapore, E-mail: kim.halpin@lifetech.com. Alex D. Hyatt, Deborah Middleton, and John Bingham, Australian Animal Health Laboratory, Geelong, Australia, E-mails: alex.hyatt@csiro.au, deborah.middleton@csiro.au, and john.bingham@csiro.au. Rhys Fogarty, Flinders University, Flinders Medical Centre Bedford Park, Australia, E-mail: rhys.fogarty@flinders.edu.au. Jonathan H. Epstein, Tom Hughes, Peter Daszak, and the Henipavirus Ecology Research Group, EcoHealth Alliance, New York, NY, E-mails: epstein@ecohealthalliance.org, Tom.hughes@ecohealthalliance.org, and daszak@ecohealthalliance.org. Sohayati Abdul Rahman, Veterinary Research Institute, Jalan Sultan Azlan Shah 31400 Ipoh, Malaysia, E-mail: sohayati@jphvri.po.my. Craig Smith and Hume E. Field, Biosecurity Queensland, Department of Employment, Economic Development and Innovation, Animal Research Institute, Yeerongpilly, Australia, E-mails: craig.smith@deedi.qld.gov.au and hume.field@deedi.qld.gov.au.

Copyright:

©The American Society of Tropical Medicine and Hygiene 2011

Received:

12 Oct 2010

|

Accepted:

26 May 2011

|

Published Online:

01 Nov 2011

Print ISSN:

0002-9637

Online ISSN:

1476-1645

• Introduction
• Materials and Methods
  • Animals.
  • Viral inoculum.
  • Experimental infections.
  • Serology.
  • HeV and NiV genome Taqman polymerase chain reaction assays.
  • Virus isolation.
  • Histopathologic and immunohistochemical methods.
• Results
  • Animals.
  • Clinical observations.
  • Detection of henipavirus genome.
  • Virus isolation.
  • Postmortem.
  • Histopathology and immunohistochemistry.
  • Serology.
• Discussion

ProCite

RefWorks

Reference Manager

• 1. Young PL, Halpin K, Selleck PW, Field H, Gravel JL, Kelly MA, Mackenzie JS, 1996. Serologic evidence for the presence in Pteropus bats of a paramyxovirus related to equine morbillivirus. Emerg Infect Dis 2: 239–240.
  • PubMed
    YoungPLHalpinKSelleckPWFieldHGravelJLKellyMAMackenzieJS, 1996. Serologic evidence for the presence in Pteropus bats of a paramyxovirus related to equine morbillivirus. Emerg Infect Dis 2: 239–240.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halpin K, Young P, Field H, Mackenzie J, 2000. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81: 1927–1932.
  • PubMed
    HalpinKYoungPFieldHMackenzieJ, 2000. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81: 1927–1932.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Johara M, Field H, Rashdi A, Morrissy C, van der Heide B, Rota P, Adzhar A, White J, Daniels P, Jamaluddin A, Ksiazek T, 2001. Nipah virus infection in bats (order Chiroptera) in Peninsular Malaysia. Emerg Infect Dis 7: 439–441.
  • PubMed
    JoharaMFieldHRashdiAMorrissyCvan der HeideBRotaPAdzharAWhiteJDanielsPJamaluddinAKsiazekT, 2001. Nipah virus infection in bats (order Chiroptera) in Peninsular Malaysia. Emerg Infect Dis 7: 439–441.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chua KB, Koh CL, Hooi PS, Wee KF, Khong JH, Chua BH, Chan YP, Lim ME, Lam SK, 2002. Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4: 145–151.
  • PubMed
    ChuaKBKohCLHooiPSWeeKFKhongJHChuaBHChanYPLimMELamSK, 2002. Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4: 145–151.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Rahman SA, Hassan SS, Olival KJ, Mohamed M, Chang LY, Hassan L, Saad NM, Shohaimi SA, Mamat ZC, Naim MS, Epstein JH, Suri AS, Field HE, Daszak P; , 2010. Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerg Infect Dis 16: 1990–1993.
  • PubMed
    RahmanSAHassanSSOlivalKJMohamedMChangLYHassanLSaadNMShohaimiSAMamatZCNaimMSEpsteinJHSuriASFieldHEDaszakP; Henipavirus Ecology Research Group, 2010. Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerg Infect Dis 16: 1990–1993.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Reynes JM, Counor D, Ong S, Faure C, Seng V, Molia S, Walston J, Georges-Courbot MC, Deubel V, Sarthou JL, 2010. Nipah virus in Lyle's flying foxes, Cambodia. Emerg Infect Dis 11: 1042–1047.
  • PubMed
    ReynesJMCounorDOngSFaureCSengVMoliaSWalstonJGeorges-CourbotMCDeubelVSarthouJL, 2010. Nipah virus in Lyle's flying foxes, Cambodia. Emerg Infect Dis 11: 1042–1047.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Mungall BA, Middleton D, Crameri G, Bingham J, Halpin K, Russell G, Green D, McEachern J, Pritchard I, Eaton BT, Wang LF, Bossart KN, Broder CC, 2006. Feline model of acute Nipah virus infection and protection with a soluble glycoprotein-based subunit vaccine. J Virol 80: 12293–12302.
  • PubMed
    MungallBAMiddletonDCrameriGBinghamJHalpinKRussellGGreenDMcEachernJPritchardIEatonBTWangLFBossartKNBroderCC, 2006. Feline model of acute Nipah virus infection and protection with a soluble glycoprotein-based subunit vaccine. J Virol 80: 12293–12302.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Mungall BA, Schopman NC, Lambeth L, Doran TJ, 2008. Inhibition of Henipavirus infection by RNA interference. Antiviral Res 80: 324–331.
  • PubMed
    MungallBASchopmanNCLambethLDoranTJ, 2008. Inhibition of Henipavirus infection by RNA interference. Antiviral Res 80: 324–331.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Middleton DJ, Westbury HA, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Hyatt AD, 2002. Experimental Nipah virus infection in pigs and cats. J Comp Pathol 126: 124–136.
  • PubMed
    MiddletonDJWestburyHAMorrissyCJvan der HeideBMRussellGMBraunMAHyattAD, 2002. Experimental Nipah virus infection in pigs and cats. J Comp Pathol 126: 124–136.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Middleton DJ, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Westbury HA, Halpin K, Daniels PW, 2007. Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136: 266–272.
  • PubMed
    MiddletonDJMorrissyCJvan der HeideBMRussellGMBraunMAWestburyHAHalpinKDanielsPW, 2007. Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136: 266–272.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. van den Hurk AF, Smith CS, Field HE, Smith IL, Northill JA, Taylor CT, Jansen CC, Smith GA, Mackenzie JS, 2009. Transmission of Japanese encephalitis virus from the black flying fox, Pteropus alecto, to Culex annulirostris mosquitoes, despite the absence of detectable viremia. Am J Trop Med Hyg 81: 457–462.
  • PubMed
    van den HurkAFSmithCSFieldHESmithILNorthillJATaylorCTJansenCCSmithGAMackenzieJS, 2009. Transmission of Japanese encephalitis virus from the black flying fox, Pteropus alecto, to Culex annulirostris mosquitoes, despite the absence of detectable viremia. Am J Trop Med Hyg 81: 457–462.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Williamson M, Hooper P, Selleck P, Westbury H, Slocombe R, 1999. Experimental Hendra virus infection in pregnant guinea-pigs and fruit bats (Pteropus poliocephalus). J Comp Pathol 122: 201–207.
  • PubMed
    WilliamsonMHooperPSelleckPWestburyHSlocombeR, 1999. Experimental Hendra virus infection in pregnant guinea-pigs and fruit bats (Pteropus poliocephalus). J Comp Pathol 122: 201–207.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, Daszak P, 2011. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus species). Proceedings of the Royal Society B.
  • PubMed
    PlowrightRKFoleyPFieldHEDobsonAPFoleyJEEbyPDaszakP, 2011. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus species). Proceedings of the Royal Society B. DOI:10.1098/rspb.2011.0522
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Williamson M, Hooper P, Selleck P, Gleeson L, Daniels P, Westbury H, Murray K, 1998. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Aust Vet J 76: 813–818.
  • PubMed
    WilliamsonMHooperPSelleckPGleesonLDanielsPWestburyHMurrayK, 1998. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Aust Vet J 76: 813–818.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Leonard LL, Allen R, Sulkin SE, 1968. Bat immunoglobulins formed in response to experimental japanese B encephalitis (JBE) virus infection. J Immunol 101: 1168–1175.
  • PubMed
    LeonardLLAllenRSulkinSE, 1968. Bat immunoglobulins formed in response to experimental japanese B encephalitis (JBE) virus infection. J Immunol 101: 1168–1175.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chakravarty AK, Sarkar SK, 1994. Immunofluorescence analysis of immunoglobulin bearing lymphocytes in the Indian fruit bat: Pteropus giganteus. Lymphology 27: 97–104.
  • PubMed
    ChakravartyAKSarkarSK, 1994. Immunofluorescence analysis of immunoglobulin bearing lymphocytes in the Indian fruit bat: Pteropus giganteus. Lymphology 27: 97–104.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Chakraborty AK, Chakravarty AK, 1984. Antibody-mediated immune response in the bat, Pteropus giganteus. Dev Comp Immunol 8: 415–423.
  • PubMed
    ChakrabortyAKChakravartyAK, 1984. Antibody-mediated immune response in the bat, Pteropus giganteus. Dev Comp Immunol 8: 415–423.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE, 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc R Soc Lond B Biol Sci 275: 861–869.
  • PubMed
    PlowrightRKFieldHESmithCDivljanAPalmerCTaborGDaszakPFoleyJE, 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc R Soc Lond B Biol Sci 275: 861–869.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Halpin K, Hyatt AD, Plowright RK, Epstein JH, Daszak P, Field HE, Wang L, Daniels PW, , 2007. Emerging viruses: coming in on a wrinkled wing and a prayer. Clin Infect Dis 44: 711–717.
  • PubMed
    HalpinKHyattADPlowrightRKEpsteinJHDaszakPFieldHEWangLDanielsPW, Henipavirus Ecology Research Group, 2007. Emerging viruses: coming in on a wrinkled wing and a prayer. Clin Infect Dis 44: 711–717.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Dorland WAN, 1994. Dorland's Illustrated Medical Dictionary. London: W.B. Saunders.
  • PubMed
    DorlandWAN, 1994. Dorland's Illustrated Medical Dictionary. London: W.B. Saunders.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Henderson IF, Henderson WD, 1989. Henderson's Dictionary of Biological Terms. London: Longman Scientific & Technical.
  • PubMed
    HendersonIFHendersonWD, 1989. Henderson's Dictionary of Biological Terms. London: Longman Scientific & Technical.
    )| false
  • Search Google Scholar
  • Export Citation
• 1. Swinton J, Harwood J, Grenfell BT, Gilligan CA, 1998. Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations. J Anim Ecol 67: 54–68.
  • PubMed
    SwintonJHarwoodJGrenfellBTGilliganCA, 1998. Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations. J Anim Ecol 67: 54–68.
    )| false
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