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Published in: EcoHealth 3/2017

01-09-2017 | Original Contribution

Arenavirus Dynamics in Experimentally and Naturally Infected Rodents

Authors: Joachim Mariën, Benny Borremans, Sophie Gryseels, Bram Vanden Broecke, Beate Becker-Ziaja, Rhodes Makundi, Apia Massawe, Jonas Reijniers, Herwig Leirs

Published in: EcoHealth | Issue 3/2017

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Abstract

Infectious diseases of wildlife are typically studied using data on antibody and pathogen levels. In order to interpret these data, it is necessary to know the course of antibodies and pathogen levels after infection. Such data are typically collected using experimental infection studies in which host individuals are inoculated in the laboratory and sampled over an extended period, but because laboratory conditions are controlled and much less variable than natural conditions, the immune response and pathogen dynamics may differ. Here, we compared Morogoro arenavirus infection patterns between naturally and experimentally infected multimammate mice (Mastomys natalensis). Longitudinal samples were collected during three months of bi-weekly trapping in Morogoro, Tanzania, and antibody titer and viral RNA presence were determined. The time of infection was estimated from these data using a recently developed Bayesian approach, which allowed us to assess whether the natural temporal patterns match the previously observed patterns in the laboratory. A good match was found for 52% of naturally infected individuals, while most of the mismatches can be explained by the presence of chronically infected individuals (35%), maternal antibodies (10%), and an antibody detection limit (25%). These results suggest that while laboratory data are useful for interpreting field samples, there can still be differences due to conditions that were not tested in the laboratory.
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Literature
go back to reference Asano BMS, Ahmed R (1996) CD8 T cell memory in B cell-deficient mice. Journal of Experimental Medicine 183:2165–2174CrossRefPubMed Asano BMS, Ahmed R (1996) CD8 T cell memory in B cell-deficient mice. Journal of Experimental Medicine 183:2165–2174CrossRefPubMed
go back to reference Bagamian KH, Towner JS, Kuenzi AJ, et al. (2012) Transmission ecology of Sin Nombre hantavirus in naturally infected North American deermouse populations in outdoor enclosures. PLoS One 7:1–10. doi:10.1371/journal.pone.0047731 Bagamian KH, Towner JS, Kuenzi AJ, et al. (2012) Transmission ecology of Sin Nombre hantavirus in naturally infected North American deermouse populations in outdoor enclosures. PLoS One 7:1–10. doi:10.​1371/​journal.​pone.​0047731
go back to reference Borremans B, Leirs H, Gryseels S, et al. (2011) Presence of Mopeia virus, an African arenavirus, related to biotope and individual rodent host characteristics: implications for virus transmission. Vector-Borne and Zoonotic Diseases 11:1125–1131. doi:10.1089/vbz.2010.0010 CrossRefPubMed Borremans B, Leirs H, Gryseels S, et al. (2011) Presence of Mopeia virus, an African arenavirus, related to biotope and individual rodent host characteristics: implications for virus transmission. Vector-Borne and Zoonotic Diseases 11:1125–1131. doi:10.​1089/​vbz.​2010.​0010 CrossRefPubMed
go back to reference Borremans B (2014). Ammonium improves elution of fixed dried blood spots without affecting immunofluorescence assay quality. Tropical Medicine and International Health 22:533–543 Borremans B (2014). Ammonium improves elution of fixed dried blood spots without affecting immunofluorescence assay quality. Tropical Medicine and International Health 22:533–543
go back to reference Borremans B, Vossen R, Becker-ziaja B, et al. (2015a) Shedding dynamics of Morogoro virus, an African arenavirus closely related to Lassa virus, in its natural reservoir host Mastomys natalensis. Scientific Reports 5:10445CrossRefPubMedPubMedCentral Borremans B, Vossen R, Becker-ziaja B, et al. (2015a) Shedding dynamics of Morogoro virus, an African arenavirus closely related to Lassa virus, in its natural reservoir host Mastomys natalensis. Scientific Reports 5:10445CrossRefPubMedPubMedCentral
go back to reference Borremans B, Sluydts V, Makundi RH, Leirs H (2015b) Evaluation of short-, mid-and long-term effects of toe clipping on a wild rodent. Wildlife Research 42:143–148CrossRef Borremans B, Sluydts V, Makundi RH, Leirs H (2015b) Evaluation of short-, mid-and long-term effects of toe clipping on a wild rodent. Wildlife Research 42:143–148CrossRef
go back to reference Buchmeier MJ, Welsh RM, Dutko Ambao FJ (1978) The virology and immunobiology of lymphocytic choriomeningitis virus infection. Advances in Immunology 30:275–331CrossRef Buchmeier MJ, Welsh RM, Dutko Ambao FJ (1978) The virology and immunobiology of lymphocytic choriomeningitis virus infection. Advances in Immunology 30:275–331CrossRef
go back to reference Burnet FM, Fenner F (1949) The Production of Antibodies, 2nd ed., Melbourne, Australia: Macmillan Magazines Ltd Burnet FM, Fenner F (1949) The Production of Antibodies, 2nd ed., Melbourne, Australia: Macmillan Magazines Ltd
go back to reference Carrat F, Vergu E, Ferguson NM, et al. (2008) Time lines of infection and disease in human influenza: a review of volunteer challenge studies. American Journal of Epidemiology 167:775–785. doi:10.1093/aje/kwm375 CrossRefPubMed Carrat F, Vergu E, Ferguson NM, et al. (2008) Time lines of infection and disease in human influenza: a review of volunteer challenge studies. American Journal of Epidemiology 167:775–785. doi:10.​1093/​aje/​kwm375 CrossRefPubMed
go back to reference Chantrey, J. (1999) The epidemiology of cowpox in its reservoir hosts (Doctoral dissertation, University of Liverpool) Chantrey, J. (1999) The epidemiology of cowpox in its reservoir hosts (Doctoral dissertation, University of Liverpool)
go back to reference Franca R, Poulson J, Brown EW, Howerth RD, Berghaus D, Carter DES (2012) Effect of different routes of inoculation on infectivity and viral shedding of LPAI viruses in mallards research note. Avian Diseases 56:981–985CrossRefPubMed Franca R, Poulson J, Brown EW, Howerth RD, Berghaus D, Carter DES (2012) Effect of different routes of inoculation on infectivity and viral shedding of LPAI viruses in mallards research note. Avian Diseases 56:981–985CrossRefPubMed
go back to reference Fulhorst CF, Ksiazek TG, Peters CJ, Tesh RB (1999) Experimental infection of the cane mouse Zygodontomys brevicauda (family Muridae) with guanarito virus (Arenaviridae), the etiologic agent of Venezuelan hemorrhagic fever. Journal of Infectious Diseases 180:966–969CrossRefPubMed Fulhorst CF, Ksiazek TG, Peters CJ, Tesh RB (1999) Experimental infection of the cane mouse Zygodontomys brevicauda (family Muridae) with guanarito virus (Arenaviridae), the etiologic agent of Venezuelan hemorrhagic fever. Journal of Infectious Diseases 180:966–969CrossRefPubMed
go back to reference Fulhorst CF, Milazzo ML, Bradley RD, Peppers LL (2001) Experimental infection of Neotoma albigula (Muridae) with Whitewater Arroyo virus (Arenaviridae). American Journal of Tropical Medicine and Hygeine 65:147–151CrossRef Fulhorst CF, Milazzo ML, Bradley RD, Peppers LL (2001) Experimental infection of Neotoma albigula (Muridae) with Whitewater Arroyo virus (Arenaviridae). American Journal of Tropical Medicine and Hygeine 65:147–151CrossRef
go back to reference Fulhorst CF, Milazzo ML, Duno G, Salas RA (2002) Experimental infection of the Sigmodon alstoni cotton rat with Caño Delgadito virus, a South American hantavirus. American Journal of Tropical Medicine and Hygeine 67:107–111CrossRef Fulhorst CF, Milazzo ML, Duno G, Salas RA (2002) Experimental infection of the Sigmodon alstoni cotton rat with Caño Delgadito virus, a South American hantavirus. American Journal of Tropical Medicine and Hygeine 67:107–111CrossRef
go back to reference Glass GE, Childs JE, Leduc JW, et al. (1990) Determining matrilines by antibody-response to exotic antigens. Journal of Mammalogy 71:129–138CrossRef Glass GE, Childs JE, Leduc JW, et al. (1990) Determining matrilines by antibody-response to exotic antigens. Journal of Mammalogy 71:129–138CrossRef
go back to reference Kallio ER, Begon M, Henttonen H, et al. (2010) Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proceedings of the Royal Society of London B: Biological Sciences 277:3783–3791. doi:10.1098/rspb.2010.1022 CrossRef Kallio ER, Begon M, Henttonen H, et al. (2010) Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proceedings of the Royal Society of London B: Biological Sciences 277:3783–3791. doi:10.​1098/​rspb.​2010.​1022 CrossRef
go back to reference Kallio ER, Poikonen A, Vaheri A, et al. (2006) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proceedings of the Royal Society of London B: Biological Sciences 273:2771–2776. doi:10.1098/rspb.2006.3645 CrossRef Kallio ER, Poikonen A, Vaheri A, et al. (2006) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proceedings of the Royal Society of London B: Biological Sciences 273:2771–2776. doi:10.​1098/​rspb.​2006.​3645 CrossRef
go back to reference Leirs H (1994) Population ecology of Mastomys natalensis (Smith, 1834). Implications for rodent control in Africa. Brussels (Doctoral dissertation, University of Antwerp). Leirs H (1994) Population ecology of Mastomys natalensis (Smith, 1834). Implications for rodent control in Africa. Brussels (Doctoral dissertation, University of Antwerp).
go back to reference Lukashevich IS, Maryankova R, Vladyko AS, et al. (1999) Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. Journal of Medical Virology 59:552–560.CrossRefPubMedPubMedCentral Lukashevich IS, Maryankova R, Vladyko AS, et al. (1999) Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. Journal of Medical Virology 59:552–560.CrossRefPubMedPubMedCentral
go back to reference Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 363:321–339. doi:10.1098/rstb.2007.2142 CrossRefPubMed Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 363:321–339. doi:10.​1098/​rstb.​2007.​2142 CrossRefPubMed
go back to reference Matloubian M, Concepcion RJ, Ahmed R (1994) CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. Journal of Virology 68:8056–8063.PubMedPubMedCentral Matloubian M, Concepcion RJ, Ahmed R (1994) CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. Journal of Virology 68:8056–8063.PubMedPubMedCentral
go back to reference Murphy FA, Winn WC, Walker DH, Flemister MR, Whitfield SG (1976) Early lymphoreticular viral tropism and antigen persistence Tamiami virus infection in the cotton rat. Laboratory Investigation 34:125–140PubMed Murphy FA, Winn WC, Walker DH, Flemister MR, Whitfield SG (1976) Early lymphoreticular viral tropism and antigen persistence Tamiami virus infection in the cotton rat. Laboratory Investigation 34:125–140PubMed
go back to reference Oldstone MBA (2002) Biology and Pathogenesis of Lymphocytic Choriomeningitis Virus Infection. Springer-Verlag, Berlin HeidelbergCrossRef Oldstone MBA (2002) Biology and Pathogenesis of Lymphocytic Choriomeningitis Virus Infection. Springer-Verlag, Berlin HeidelbergCrossRef
go back to reference Oldstone MB, Dixon FJ (1967) Lymphocytic choriomeningitis: production of antibody by “tolerant” infected mice. Science 80:1193–1195.CrossRef Oldstone MB, Dixon FJ (1967) Lymphocytic choriomeningitis: production of antibody by “tolerant” infected mice. Science 80:1193–1195.CrossRef
go back to reference Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildlife Monographs 3–97. doi:10.2307/3830560 Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildlife Monographs 3–97. doi:10.​2307/​3830560
go back to reference Samiel MD, Takekawa JY, Baranyuk VV, Orthmeyer DL (1999) Effects of avian cholera on survival of Lesser Snow Geese Anser caerulescens: an experimental approach. Bird Study 46:S239–S247. doi:10.1080/00063659909477250 CrossRef Samiel MD, Takekawa JY, Baranyuk VV, Orthmeyer DL (1999) Effects of avian cholera on survival of Lesser Snow Geese Anser caerulescens: an experimental approach. Bird Study 46:S239–S247. doi:10.​1080/​0006365990947725​0 CrossRef
go back to reference Telfer S, Bennett M, Bown K, et al. (2002) The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71:558–568CrossRef Telfer S, Bennett M, Bown K, et al. (2002) The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71:558–568CrossRef
go back to reference Tersago K, Crespin L, Verhagen R, Leirs H (2012) Impact of Puumala virus infection on maturation and survival in bank voles: capture-mark-recapture analysis. Journal of Wildlife Diseases 48:148–156CrossRefPubMed Tersago K, Crespin L, Verhagen R, Leirs H (2012) Impact of Puumala virus infection on maturation and survival in bank voles: capture-mark-recapture analysis. Journal of Wildlife Diseases 48:148–156CrossRefPubMed
go back to reference Vitullo A, Hodara V, Merani MS (1987) Effect of persistent infection with Junin virus on growth and reproduction of its natural reservoir, Calomys musculinus. American Journal of Tropical Medicine and Hygeine 37:663–669CrossRef Vitullo A, Hodara V, Merani MS (1987) Effect of persistent infection with Junin virus on growth and reproduction of its natural reservoir, Calomys musculinus. American Journal of Tropical Medicine and Hygeine 37:663–669CrossRef
go back to reference Voutilainen L, Kallio ER, Niemimaa J, et al. (2016) Temporal dynamics of Puumala hantavirus infection in cyclic populations of bank voles. Scientific Reports 6:1–14. doi:10.1038/srep21323 CrossRef Voutilainen L, Kallio ER, Niemimaa J, et al. (2016) Temporal dynamics of Puumala hantavirus infection in cyclic populations of bank voles. Scientific Reports 6:1–14. doi:10.​1038/​srep21323 CrossRef
go back to reference Walker DH, Wulff H, Lange J V, Murphy FA (1975) Comparative pathology of Lassa virus infection in monkeys, guinea-pigs, and Mastomys natalensis. Bulletin of the World Health Organization 52:523–534PubMedPubMedCentral Walker DH, Wulff H, Lange J V, Murphy FA (1975) Comparative pathology of Lassa virus infection in monkeys, guinea-pigs, and Mastomys natalensis. Bulletin of the World Health Organization 52:523–534PubMedPubMedCentral
go back to reference Webb P, Justines G, Johnson K (1975) Infection of wild and laboratory animals with Machupo and Latino viruses. Bulletin of the World Health Organization 52:493–499PubMedPubMedCentral Webb P, Justines G, Johnson K (1975) Infection of wild and laboratory animals with Machupo and Latino viruses. Bulletin of the World Health Organization 52:493–499PubMedPubMedCentral
go back to reference Weigand H, Hotchin J (1961) Studies of lymphocytic choriomeningitis in mice. Journal of Immunology 86:401. Weigand H, Hotchin J (1961) Studies of lymphocytic choriomeningitis in mice. Journal of Immunology 86:401.
go back to reference Wulff H, McIntosh BM, Hamner DB, Johnson KM (1977) Isolation of an arenavirus closely related to Lassa virus from Mastomys natalensis in south-east Africa. Bulletin of the World Health Organization 55:441–444PubMedPubMedCentral Wulff H, McIntosh BM, Hamner DB, Johnson KM (1977) Isolation of an arenavirus closely related to Lassa virus from Mastomys natalensis in south-east Africa. Bulletin of the World Health Organization 55:441–444PubMedPubMedCentral
go back to reference Yanagihara R, Amyx HL, Gajdusek DC (1985) Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). Journal of Virology 55:34–38PubMedPubMedCentral Yanagihara R, Amyx HL, Gajdusek DC (1985) Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). Journal of Virology 55:34–38PubMedPubMedCentral
Metadata
Title
Arenavirus Dynamics in Experimentally and Naturally Infected Rodents
Authors
Joachim Mariën
Benny Borremans
Sophie Gryseels
Bram Vanden Broecke
Beate Becker-Ziaja
Rhodes Makundi
Apia Massawe
Jonas Reijniers
Herwig Leirs
Publication date
01-09-2017
Publisher
Springer US
Published in
EcoHealth / Issue 3/2017
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1256-7

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