, Volume 10, Issue 3, pp 298–313 | Cite as

Deciphering Serology to Understand the Ecology of Infectious Diseases in Wildlife

  • Amy T. GilbertEmail author
  • A. R. Fooks
  • D. T. S. Hayman
  • D. L. Horton
  • T. Müller
  • R. Plowright
  • A. J. Peel
  • R. Bowen
  • J. L. N. Wood
  • J. Mills
  • A. A. Cunningham
  • C. E. Rupprecht


The ecology of infectious disease in wildlife has become a pivotal theme in animal and public health. Studies of infectious disease ecology rely on robust surveillance of pathogens in reservoir hosts, often based on serology, which is the detection of specific antibodies in the blood and is used to infer infection history. However, serological data can be inaccurate for inference to infection history for a variety of reasons. Two major aspects in any serological test can substantially impact results and interpretation of antibody prevalence data: cross-reactivity and cut-off thresholds used to discriminate positive and negative reactions. Given the ubiquitous use of serology as a tool for surveillance and epidemiological modeling of wildlife diseases, it is imperative to consider the strengths and limitations of serological test methodologies and interpretation of results, particularly when using data that may affect management and policy for the prevention and control of infectious diseases in wildlife. Greater consideration of population age structure and cohort representation, serological test suitability and standardized sample collection protocols can ensure that reliable data are obtained for downstream modeling applications to characterize, and evaluate interventions for, wildlife disease systems.


antibody prevalence epidemiological models immunity surveillance wildlife disease 



The authors thank the working group of Research and Policy for Infectious Disease Dynamics program of the Science and Technology Directorate, Department of Homeland Security and the Rabies program at CDC-Atlanta, specifically Richard Franka and Michael Niezgoda, for insightful discussions of serologic testing and interpretation. AG was supported by an Oak Ridge Institute for Science and Education (ORISE) fellowship. DTSH acknowledges support from the David H. Smith Fellowship in Conservation Research and the Wellcome Trust. AAC was supported by a Royal Society Wolfson Research Merit award. ARF and DLH are supported by the UK Department for Environment, Food and Rural Affairs (DEFRA) projects SV3500 and SV3034. JLNW was supported by the Alborada Trust. The findings and conclusions in this report are those of the authors only, and do not necessarily reflect the views of their institutions.


  1. Aleman N, Quiroga MI, Lopez-Pena M, Vazquez S, Guerrero FH, and Nieto JM (2001). Induction and inhibition of apoptosis by pseudorabies virus in the trigeminal ganglion during acute infection of swine. Journal of Virology 75:469-479.PubMedCrossRefGoogle Scholar
  2. Alexander KA, and Appel MJ (1994). African wild dogs (Lycaon pictus) endangered by a canine distemper epizootic among domestic dogs near the Masai Mara National Reserve, Kenya. Journal of Wildlife Diseases 30:481-485.PubMedCrossRefGoogle Scholar
  3. Alexeyev OA, Ahlm C, Elgh F, Aava B, Palo T, Settergren B, et al. (1998). A minority of seropositive wild bank voles (Clethrionomys glareolus) show evidence of current Puumala virus infection. Epidemiology and Infection 121:419-425.PubMedCrossRefGoogle Scholar
  4. Anderson RM, and May RM (1979). Population biology of infectious diseases: Part I. Nature 280:361-367.PubMedCrossRefGoogle Scholar
  5. Anderson RM, and May RM (1986). The invasion, persistence and spread of infectious diseases within animal and plant communities. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 314:533-570.CrossRefGoogle Scholar
  6. Aubert MF (1992). Practical significance of rabies antibodies in cats and dogs. Revue Scientifique et Technique (International Office of Epizootics) 11:735-760.Google Scholar
  7. Baer GM, and Bales GL (1967). Experimental rabies infection in the Mexican freetail bat. Journal of Infectious Diseases 117:82-90.PubMedCrossRefGoogle Scholar
  8. Baldwin CL, and Roop RM (2002). Brucella infections and immunity. Pages 255-279 in L. J. Paradise, H. Friedman, and M. Bendinelli, editors. Opportunistic Intracellular Bacteria and Immunity Kluwer Academic Press, New YorkGoogle Scholar
  9. Boulinier T, and Staszewski V (2008). Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology & Evolution 23:282-288.CrossRefGoogle Scholar
  10. Bouma HR, Carey HV, and Kroese FG (2010). Hibernation: the immune system at rest? Journal of Leukocyte Biology 88:619-624.PubMedCrossRefGoogle Scholar
  11. Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, et al. (1989a). Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. Journal of General Virology 70:37-43.PubMedCrossRefGoogle Scholar
  12. Calisher CH, Karabatsos N, Zeller H, Digoutte JP, Tesh RB, Shope RE, et al. (1989b). Antigenic relationships among rhabdoviruses from vertebrates and hematophagous arthropods. Intervirology 30:241-257.PubMedGoogle Scholar
  13. Chambers MA, Pressling WA, Cheeseman CL, Clifton-Hadley RS, and Hewinson RG (2002). Value of existing serological tests for identifying badgers that shed Mycobacterium bovis. Veterinary Microbiology 86:183-189.PubMedCrossRefGoogle Scholar
  14. Chambers MA, Rogers F, Delahay RJ, Lesellier S, Ashford R, Dalley D, et al. (2011). Bacillus Calmette-Guerin vaccination reduces the severity and progression of tuberculosis in badgers. Proceedings of the Royal Society. B, Biological sciences 278:1913-1920.PubMedCrossRefGoogle Scholar
  15. Childs JE, Richt JA, and Mackenzie JS (2007). Conceptualizing and partitioning the emergence process of zoonotic viruses from wildlife to humans. Current Topics in Microbiology & Immunology 315:1-31.Google Scholar
  16. Cleaveland S, Appel MGJ, Chalmers WSK, Chillingworth C, Kaare M, and Dye C (2000). Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Veterinary Microbiology 72:217-227.PubMedCrossRefGoogle Scholar
  17. Cleaveland S, Barrat J, Barrat MJ, Selve M, Kaare M, and Esterhuysen J (1999). A rabies serosurvey of domestic dogs in rural Tanzania: results of a rapid fluorescent focus inhibition test (RFFIT) and a liquid-phase blocking ELISA used in parallel. Epidemiology and Infection 123:157-164.PubMedCrossRefGoogle Scholar
  18. Constantine DG, Tierkel ES, Kleckner MD, and Hawkins DM (1968). Rabies in New Mexico cavern bats. Public Health Reports 83:303-316.PubMedCrossRefGoogle Scholar
  19. Cross PC, Edwards WH, Scurlock BM, Maichak EJ, and Rogerson JD (2007). Effects of management and climate on elk brucellosis in the Greater Yellowstone Ecosystem. Ecological Applications 17:957-964.PubMedCrossRefGoogle Scholar
  20. Daszak P, Cunningham AA, and Hyatt AD (2000). Emerging infectious diseases of wildlife– threats to biodiversity and human health. Science 287:443-449.PubMedCrossRefGoogle Scholar
  21. Deem SL, Spelman LH, Yates RA, and Montali RJ (2000). Canine distemper in terrestrial carnivores: a review. Journal of Zoo and Wildlife Medicine 31:441-451.PubMedGoogle Scholar
  22. Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P, Binger T, et al. (2012). Bats host major mammalian paramyxoviruses. Nat Commun 3:796.PubMedCrossRefGoogle Scholar
  23. Evans AS (1976). Causation and disease: the Henle-Koch postulates revisited. The Yale Journal of Biology and Medicine 49:175-195.PubMedGoogle Scholar
  24. Faber M, Pulmanausahakul R, Hodawadekar SS, Spitsin S, McGettigan JP, Schnell MJ, et al. (2002). Overexpression of the rabies virus glycoprotein results in enhancement of apoptosis and antiviral immune response. Journal of Virology 76:3374–3381.PubMedCrossRefGoogle Scholar
  25. Farrington CP, Kanaan MN, and Gay NJ (2001). Estimation of the basic reproduction number for infectious diseases from age-stratified serological survey data. Journal of the Royal Statistical Society Series C-Applied Statistics 50:251-283.CrossRefGoogle Scholar
  26. Fooks AR (2007). Rabies - the need for a ‘one medicine’ approach. The Veterinary Record 161:289-290.PubMedCrossRefGoogle Scholar
  27. Fouchet D, Marchandeau S, Bahi-Jaber N, and Pontier D (2007). The role of maternal antibodies in the emergence of severe disease as a result of fragmentation. Journal of the Royal Society Interface 4:479-489.CrossRefGoogle Scholar
  28. George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, et al. (2011). Host and viral ecology determine bat rabies seasonality and maintenance. Proceedings Of The National Academy Of Sciences Of The United States Of America 108:10208-10213.PubMedCrossRefGoogle Scholar
  29. Graham AL, Cattadori IM, Lloyd-Smith JO, Ferrari MJ, and Bjornstad ON (2007). Transmission consequences of coinfection: cytokines writ large? Trends Parasitol 23:284-291.PubMedCrossRefGoogle Scholar
  30. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, and Nussey DH (2010). Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662-665.PubMedCrossRefGoogle Scholar
  31. Greenwald R, Esfandiari J, Lesellier S, Houghton R, Pollock J, Aagaard C, et al. (2003). Improved serodetection of Mycobacterium bovis infection in badgers (Meles meles) using multiantigen test formats. Diagnostic Microbiology and Infectious Disease 46:197-203.PubMedCrossRefGoogle Scholar
  32. Halpin K, Hyatt AD, Fogarty R, Middleton D, Bingham J, Epstein JH, et al. (2011). Pteropid bats are confirmed as the reservoir hosts of henipaviruses: a comprehensive experimental study of virus transmission. American Journal of Tropical Medicine and Hygiene 85:946-951.PubMedCrossRefGoogle Scholar
  33. Hampson K, Dushoff J, Cleaveland S, Haydon DT, Kaare M, Packer C, et al. (2009). Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biology 7:e53.PubMedCrossRefGoogle Scholar
  34. Hawley DM, and Altizer SM (2011). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25:48-60.CrossRefGoogle Scholar
  35. Haydon DT, Cleaveland S, Taylor LH, and Laurenson MK (2002). Identifying reservoirs of infection: A conceptual and practical challenge. Emerging Infectious Diseases 8:1468-1473.PubMedCrossRefGoogle Scholar
  36. Haydon DT, Randall DA, Matthews L, Knobel DL, Tallents LA, Gravenor MB, et al. (2006). Low-coverage vaccination strategies for the conservation of endangered species. Nature 443:692-695.PubMedCrossRefGoogle Scholar
  37. Hayman DT, Fooks AR, Rowcliffe JM, McCrea R, Restif O, Baker KS, et al. (2012) Endemic Lagos bat virus infection in Eidolon helvum. Epidemiology and Infection 140(12):2163–2171. doi: 10.1017/S0950268812000167
  38. Hazel SM, Bennett M, Chantrey J, Bown K, Cavanagh R, Jones TR, et al. (2000). A longitudinal study of an endemic disease in its wildlife reservoir: cowpox and wild rodents. Epidemiology and Infection 124:551-562.PubMedCrossRefGoogle Scholar
  39. Heisey DM, Joly DO, and Messier F (2006). The fitting of general force-of-infection models to wildlife disease prevalence data. Ecology 87:2356-2365.PubMedCrossRefGoogle Scholar
  40. Heisey DM, Osnas EE, Cross PC, Joly DO, Langenberg JA, and Miller MW (2010). Linking process to pattern: estimating spatiotemporal dynamics of a wildlife epidemic from cross-sectional data. Ecological Monographs 80:221-240.CrossRefGoogle Scholar
  41. Hirota J, Nishi H, Matsuda H, Tsunemitsu H, and Shimiz S (2010). Cross-reactivity of Japanese encephalitis virus-vaccinated horse sera in serodiagnosis of West Nile virus. The Journal of Veterinary Medical Science 72:369-372.PubMedCrossRefGoogle Scholar
  42. Horowitz A, Behrens RH, Okell L, Fooks AR, and Riley EM (2010). NK cells as effectors of acquired immune responses: effector CD4 + T cell-dependent activation of NK cells following vaccination. Journal of Immunology 185:2808-2818.CrossRefGoogle Scholar
  43. Horton DL, McElhinney LM, Marston DA, Wood JL, Russell CA, Lewis N, et al. (2010). Quantifying antigenic relationships among the lyssaviruses. Journal of Virology 84:11841-11848.PubMedCrossRefGoogle Scholar
  44. Kaden V, Kramer M, Kern B, Hlinak A, Mewes L, Hanel A, et al. (2006). Diagnostic procedures after completion of oral immunisation against classical swine fever in wild boar. Revue Scientifique et Technique (International Office of Epizootics) 25:989-997.Google Scholar
  45. Kallio ER, Begon M, Henttonen H, Koskela E, Mappes T, Vaheri A, et al. (2010). Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proceedings of the Royal Society of London. Series B, Biological sciences 277:3783-3791.CrossRefGoogle Scholar
  46. Kaplan B, Kahn LH, and Monath TP (2009). ‘One health - one medicine’: linking human, animal and environmental health. Veterinaria Italiana 45:1-195.Google Scholar
  47. Knobel DL, Fooks AR, Brookes SM, Randall DA, Williams SD, Argaw K, et al. (2008). Trapping and vaccination of endangered Ethiopian wolves to control an outbreak of rabies. Journal of Applied Ecology 45:109-116.CrossRefGoogle Scholar
  48. Kuzmin IV, Franka R, and Rupprecht CE (2008). Experimental infection of big brown bats (Eptesicus fuscus) with West Caucasian bat virus (WCBV). Developments in Biologicals 131:327-337.PubMedGoogle Scholar
  49. Kuzmin IV, Turmelle AS, Agwanda B, Markotter W, Niezgoda M, Breiman RF, et al. (2011). Commerson’s leaf-nosed bat (Hipposideros commersoni) is the likely reservoir of Shimoni bat virus. Vector Borne and Zoonotic Diseases 11:1465-1470.PubMedCrossRefGoogle Scholar
  50. Lachish S, Gopalaswamy AM, Knowles SCL, and Sheldon BC (2012). Site-occupancy modelling as a novel framework for assessing test sensitivity and estimating wildlife disease prevalence from imperfect diagnostic tests. Methods in Ecology and Evolution 3:339-348.CrossRefGoogle Scholar
  51. Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, et al. (1999). Origin of the West Nile Virus Responsible for an Outbreak of Encephalitis in the Northeastern United States. Science 286:2333-2337.PubMedCrossRefGoogle Scholar
  52. Lembo T, Hampson K, Auty H, Beesley CA, Bessell P, Packer C, et al. (2011). Serologic surveillance of anthrax in the Serengeti ecosystem, Tanzania, 1996-2009. Emerging Infectious Diseases 17:387-394.PubMedCrossRefGoogle Scholar
  53. Mansfield KL, Horton DL, Johnson N, Li L, Barrett AD, Smith DJ, et al. (2011). Flavivirus-induced antibody cross-reactivity. Journal of General Virology 92:2821-2829.PubMedCrossRefGoogle Scholar
  54. Middleton DJ, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Westbury HA, et al. (2007). Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). Journal of Comparative Pathology 136:266-272.PubMedCrossRefGoogle Scholar
  55. Moore SM, Wilkerson MJ, Davis RD, Wyatt CR, and Briggs DJ (2006). Detection of cellular immunity to rabies antigens in human vaccinees. Journal of Clinical Immunology 26:533-545.PubMedCrossRefGoogle Scholar
  56. Muller T, Selhorst T, Schuster P, Vos A, Wenzel U, and Neubert A (2002). Kinetics of maternal immunity against rabies in fox cubs (Vulpes vulpes). BMC Infect Dis 2:10.PubMedCrossRefGoogle Scholar
  57. Muller T, Teuffert J, Staubach C, Selhorst T, and Depner KR (2005). Long-term studies on maternal immunity for Aujeszky’s disease and classical swine fever in wild boar piglets. Journal of Veterinary Medicine. B, Infectious diseases and veterinary public health 52:432-436.PubMedCrossRefGoogle Scholar
  58. Muller TF, Schuster P, Vos AC, Selhorst T, Wenzel UD, and Neubert AM (2001). Effect of maternal immunity on the immune response to oral vaccination against rabies in young foxes. American Journal of Veterinary Research 62:1154-1158.PubMedCrossRefGoogle Scholar
  59. Mumford J (2000). Collaborative study for the establishment of three European Pharmacopoeia biological reference preparations for equine influenza horse antiserum. PHARMEUROPA Special Issue, Bio 2000-1, 5–21.Google Scholar
  60. OIE (2010) Principles and methods of validation of diagnostic assays for infectious diseases, pp 1–18 in OIE Terrestrial Manual.Google Scholar
  61. Pannwitz G, Freuling C, Denzin N, Schaarschmidt U, Nieper H, Hlinak A, et al. (2011) A long-term serological survey on Aujeszky's disease virus infections in wild boar in East Germany. Epidemiology and Infection 140(2):348-358. doi: 10.1017/S0950268811000033 PubMedCrossRefGoogle Scholar
  62. Peel AJ, Baker KS, Crameri G, Barr JA, Hayman DTS, Wright E, et al. (2012). Henipavirus neutralising antibodies in an isolated island population of African fruit bats. PloS ONE 7:e30346.PubMedCrossRefGoogle Scholar
  63. Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, et al. (2008). Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proceedings of the Royal Society of London. Series B, Biological sciences 275:861-869.CrossRefGoogle Scholar
  64. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, et al. (2011). Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proceedings of the Royal Society of London. Series B, Biological sciences 278:3703-3712.CrossRefGoogle Scholar
  65. Raberg L, Graham AL, and Read AF (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 364:37-49.PubMedCrossRefGoogle Scholar
  66. Restif O, Hayman DTS, Pulliam J, Plowright R, George D, Luis A, et al. (2012) Model-guided fieldwork: practical guidelines for multidisciplinary research on wildlife ecological and epidemiological dynamics. Ecology Letters 15(10):1083-1094. doi: 10.1111/j.1461-0248.2012.01836.x PubMedCrossRefGoogle Scholar
  67. Robardet E, Picard-Meyer E, Andrieu S, Servat A, and Cliquet F (2011). International interlaboratory trials on rabies diagnosis: an overview of results and variation in reference diagnosis techniques (fluorescent antibody test, rabies tissue culture infection test, mouse inoculation test) and molecular biology techniques. Journal of Virological Methods 177:15-25.PubMedCrossRefGoogle Scholar
  68. Rupprecht CE, Barrett J, Briggs D, Cliquet F, Fooks AR, Lumlertdacha B, et al. (2008). Can rabies be eradicated? Developments in Biologicals 131:95-121.PubMedGoogle Scholar
  69. Shankar V, Bowen RA, Davis AD, Rupprecht CE, and O’Shea T J (2004). Rabies in a captive colony of big brown bats (Eptesicus fuscus). Journal of Wildlife Diseases 40:403-413.PubMedCrossRefGoogle Scholar
  70. Sidwa TJ, Wilson PJ, Moore GM, Oertli EH, Hicks BN, Rohde RE, et al. (2005). Evaluation of oral rabies vaccination programs for control of rabies epizootics in coyotes and gray foxes: 1995-2003. Journal of the American Veterinary Medical Association 227:785-792.PubMedCrossRefGoogle Scholar
  71. Siegrist CA (2003). Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21:3406-3412.PubMedCrossRefGoogle Scholar
  72. Steece R, and Altenbach JS (1989). Prevalence of rabies specific antibodies in the Mexican free-tailed bat at Lava Cave, New Mexico. Journal of Wildlife Diseases 25:490-496.PubMedCrossRefGoogle Scholar
  73. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, and Rupprecht CE (2010). Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science 329:676-679.PubMedCrossRefGoogle Scholar
  74. Swanepoel R, Smit SB, Rollin PE, Formenty P, Leman PA, Kemp A, et al. (2007). Studies of reservoir hosts for Marburg virus. Emerging Infectious Diseases 13:1847-1851.PubMedCrossRefGoogle Scholar
  75. Taylor LH, Latham SM, and Woolhouse MEJ (2001). Risk factors for human disease emergence. Philosophical Transactions of the Royal Society B-Biological Sciences 356:983-989.CrossRefGoogle Scholar
  76. Temperton NJ, Chan PK, Simmons G, Zambon MC, Tedder RS, Takeuchi Y, et al. (2005). Longitudinally profiling neutralizing antibody response to SARS coronavirus with pseudotypes. Emerging Infectious Diseases 11:411-416.PubMedCrossRefGoogle Scholar
  77. Troyer JL, Pecon-Slattery J, Roelke ME, Johnson W, VandeWoude S, Vazquez-Salat N, et al. (2005). Seroprevalence and genomic divergence of circulating strains of feline immunodeficiency virus among Felidae and Hyaenidae species. Journal of Virology 79:8282-8294.PubMedCrossRefGoogle Scholar
  78. Turmelle AS, Allen LC, Jackson FR, Kunz TH, Rupprecht C, and McCracken GF (2010a). Ecology of rabies virus exposure in colonies of Brazilian free-tailed bats (Tadarida brasiliensis) at natural and man-made roosts in Texas. Vector Borne and Zoonotic Diseases 10:165-175.PubMedCrossRefGoogle Scholar
  79. Turmelle AS, Jackson FR, Green D, McCracken GF, and Rupprecht CE (2010b). Host immunity to repeated rabies virus infection in big brown bats. Journal of General Virology 91:2360–2366.PubMedCrossRefGoogle Scholar
  80. Vos A (2003). Oral vaccination against rabies and the behavioural ecology of the red fox (Vulpes vulpes). Journal of Veterinary Medicine. B, Infectious diseases and veterinary public health 50:477-483.PubMedCrossRefGoogle Scholar
  81. Wang ZW, Sarmento L, Wang Y, Li XQ, Dhingra V, Tseggai T, et al. (2005). Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. Journal of Virology 79:12554–12565.PubMedCrossRefGoogle Scholar
  82. Weyer J, Kuzmin IV, Rupprecht CE, and Nel LH (2008). Cross-protective and cross-reactive immune responses to recombinant vaccinia viruses expressing full-length lyssavirus glycoprotein genes. Epidemiology and Infection 136:670-678.PubMedCrossRefGoogle Scholar
  83. WHO (1999) 1999: St. Louis encephalitis in the United States of America.
  84. Wittmann G, and Rziha HG (1989). Aujeszky’s disease (pseudorabies) in pigs. Pages 230-325 in G. Wittmann, editor. Herpesvirus diseases of cattle, horses and pigs. Kluwer Academic Publishers, Boston.CrossRefGoogle Scholar
  85. Wood JM, Gaines-Das RE, Taylor J, and Chakraverty P (1994). Comparison of influenza serological techniques by international collaborative study. Vaccine 12:167-174.PubMedCrossRefGoogle Scholar
  86. Woolhouse ME, Howey R, Gaunt E, Reilly L, Chase-Topping M, and Savill N (2008). Temporal trends in the discovery of human viruses. Proceedings of the Royal Society B-Biological Sciences 275:2111-2115.CrossRefGoogle Scholar
  87. Wright E, Temperton NJ, Marston DA, McElhinney LM, Fooks AR, and Weiss RA (2008). Investigating antibody neutralization of lyssaviruses using lentiviral pseudotypes: a cross-species comparison. Journal of General Virology 89:2204-2213.PubMedCrossRefGoogle Scholar
  88. Xiang ZQ, and Ertl HC (1992). Transfer of maternal antibodies results in inhibition of specific immune responses in the offspring. Virus Research 24:297-314.PubMedCrossRefGoogle Scholar
  89. Zinsstag J, Schelling E, Bonfoh B, Fooks AR, Kasymbekov J, Waltner-Toews D, et al. (2009). Towards a ‘One Health’ research and application tool box. Veterinaria Italiana 45:121-133.PubMedGoogle Scholar
  90. Zinsstag J, Schelling E, Waltner-Toews D, and Tanner M (2011). From “one medicine” to “one health” and systemic approaches to health and well-being. Prev Vet Med 101:148-156.PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health (outside the USA) 2013

Authors and Affiliations

  • Amy T. Gilbert
    • 1
    • 11
    Email author
  • A. R. Fooks
    • 2
    • 3
  • D. T. S. Hayman
    • 2
    • 4
    • 5
    • 6
  • D. L. Horton
    • 2
  • T. Müller
    • 7
  • R. Plowright
    • 8
  • A. J. Peel
    • 4
    • 5
  • R. Bowen
    • 9
  • J. L. N. Wood
    • 4
  • J. Mills
    • 10
  • A. A. Cunningham
    • 5
  • C. E. Rupprecht
    • 1
    • 12
  1. 1.National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and PreventionAtlantaUSA
  2. 2.Wildlife Zoonoses and Vector-Borne Disease GroupAnimal Health and Veterinary Laboratories AgencySurreyUK
  3. 3.The National Consortium for Zoonosis ResearchUniversity of LiverpoolNestonUK
  4. 4.Disease Dynamics Unit, Department of Veterinary MedicineUniversity of CambridgeCambridgeUK
  5. 5.Institute of ZoologyZoological Society of LondonLondonUK
  6. 6.Department of BiologyColorado State UniversityCOUSA
  7. 7.Friedrich-Loeffler-InstitutFederal Research Institute for Animal HealthWusterhausenGermany
  8. 8.Center for Infectious Disease DynamicsThe Pennsylvania State UniversityUniversity ParkUSA
  9. 9.Department of Biomedical SciencesColorado State UniversityCOUSA
  10. 10.Population Biology, Ecology, and Evolution ProgramEmory UniversityAtlantaUSA
  11. 11.United States Department of AgricultureNational Wildlife Research CenterFort CollinsUSA
  12. 12.Global Alliance for Rabies ControlManhattanUSA

Personalised recommendations