Viral antibody dynamics in a chiropteran host

Journal of Animal Ecology

Volumn 83, Issue 2, 2014, Pages 415-428

  Baker, Kate S ^a,b,i   Suu Ire, Richard ^c   Barr, Jennifer ^d   Hayman, David T S ^e   Broder, Christopher C ^f   Horton, Daniel L ^g   Durrant, Christopher ^b   Murcia, Pablo R ^h   Cunningham, Andrew A ^b   Wood, James L N ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF ZOOLOGY   (United Kingdom)

^c FORESTRY COMMISSION   (Ghana)

^d CSIRO   (Australia)

^e Veterinary Dentistry and Oral Surgery   (United States)

^f UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^g VETERINARY LABORATORIES AGENCY   (United Kingdom)

^h UNIVERSITY OF GLASGOW   (United Kingdom)

ⁱ WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Hendra virus; Immune response; Infection persistence; Luminex; Maternal immunity; Nipah virus; Paramyxoviruses; Serology; Zoonosis

Indexed keywords

VIRUS ANTIBODY;

ANIMAL; BAT; BLOOD; FEMALE; GHANA; HENIPAVIRUS; HENIPAVIRUS INFECTION; IMMUNOLOGY; LACTATION; LONGITUDINAL STUDY; MALE; PREGNANCY; SEASON; VETERINARY; VIROLOGY;

ANIMALS; ANTIBODIES, VIRAL; CHIROPTERA; FEMALE; GHANA; HENIPAVIRUS; HENIPAVIRUS INFECTIONS; LACTATION; LONGITUDINAL STUDIES; MALE; PREGNANCY; SEASONS;

EID: 84894286492     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12153     Document Type: Article

References (74)

1. Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. & Rohani, P. (2006) Seasonality and the dynamics of infectious diseases. Ecology Letters, 9, 467-484.
2. Amman, B.R., Carroll, S.A., Reed, Z.D., Sealy, T.K., Balinandi, S., Swanepoel, R. et al. (2012) Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathogens, 8, e1002877.
3. Badrane, H. & Tordo, N. (2001) Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders. Journal of Virology, 75, 8096-8104.
4. Baker, M.L., Schountz, T. & Wang, L.F. (2013) Antiviral immune responses of bats: a review. Zoonoses and Public Health, 60, 104-116.
5. Baker, K.S., Todd, S., Marsh, G., Fernandez-Loras, A., Suu-Ire, R., Wood, J.L. et al. (2012a) Co-circulation of diverse paramyxoviruses in an urban African fruit bat population. Journal of General Virology, 93, 850-856.
6. Baker, K.S., Todd, S., Marsh, G.A., Crameri, G., Barr, J., Kamins, A.O. et al. (2012b) Novel potentially-zoonotic paramyxoviruses from the African straw-colored fruit bat, Eidolon helvum. Journal of Virology. 2013; 87:1348-1358.
7. Baker, K.S., Leggett, R.M., Bexfield, N.H., Alston, M., Daly, G., Todd, S. et al. (2013) Metagenomic study of the viruses of African straw-coloured fruit bats: detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology, 441, 95-106.
8. Bossart, K.N., Crameri, G.S., Dimitrov, A.S., Mungall, B.A., Feng, Y.R., Patch, J.R. et al. (2005) Receptor binding, fusion inhibition and induction of cross-reactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus. Journal of Virology, 79, 6690-6702.
9. Bossart, K.N., McEachern, J.A., Hickey, A.C., Choudhry, V., Dimitrov, D.S., Eaton, B.T. et al. (2007) Neutralization assays for differential Henipavirus serology using Bio-Plex protein array systems. Journal of Virological Methods, 142, 29-40.
10. Boue, A., Nicolas, A. & Montagnon, B. (1971) Reinfection with rubella in pregnant women. Lancet, 1, 1251-1253.
11. Bratsch, S., Wertz, N., Chaloner, K., Kunz, T.H. & Butler, J.E. (2011) The little brown bat, M. lucifugus, displays a highly diverse V H, D H and J H repertoire but little evidence of somatic hypermutation. Developmental and Comparative Immunology, 35, 421-430.
12. Breed, A.C., Yu, M., Barr, J.A., Crameri, G., Thalmann, C.M. & Fa Wang, L. (2010) Prevalence of henipavirus and rubulavirus antibodies in pteropid bats, Papua New Guinea. Emerging Infectious Diseases, 16, 1997-1999.
13. Breed, A.C., Breed, M.F., Meers, J. & Field, H.E. (2011) Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus)-implications for disease risk management. PLoS ONE, 6, e28816.
14. Breed, A.C., Meers, J., Sendow, I., Bossart, K.N., Barr, J.A., Smith, I. et al. (2013) The distribution of henipaviruses in Southeast Asia and Australasia: is Wallace's line a barrier to Nipah virus? PLoS ONE, 8, e61316.
15. Calisher, C.H., Childs, J.E., Field, H.E., Holmes, K.V. & Schountz, T. (2006) Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews, 19, 531-545.
16. Christe, P., Arlettaz, R. & Vogel, P. (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of ins bat host (Myotis myotis). Ecology Letters, 3, 207-212.
17. Chua, K.B., Bellini, W.J., Rota, P.A., Harcourt, B.H., Tamin, A., Lam Sai Kit, K. et al. (2000) Nipah virus: a recently emergent deadly paramyxovirus. Science, 288, 1432-1435.
18. Drexler, J.F., Corman, V.M., Gloza-Rausch, F., Seebens, A., Annan, A., Ipsen, A. et al. (2009) Henipavirus RNA in African bats. PLoS ONE, 4, e6367.
19. Drexler, J.F., Corman, V.M., Gloza-Rausch, F., Muller, M.A. & Drosten, C. (2012a) Amplification of emerging RNA viruses associated with formation and parturition in a bat maternity roost. EcoHealth, 000, 223.
20. Drexler, J.F., Corman, V.M., Muller, M.A., Maganga, G.D., Vallo, P., Binger, T. et al. (2012b) Bats host major mammalian paramyxoviruses. Nature Communications, 3, 796.
21. Epstein, J.H., Baker, M.L., Zambrana-Torrelio, C., Middleton, D., Barr, J.A., Dubovi, E. et al. (2013) Duration of Maternal Antibodies against Canine Distemper Virus and Hendra Virus in Pteropid Bats. PLoS ONE, 8, e67584.
22. Field, H.E. (2005) The Ecology of Hendra Virus and Australian Bat Lyssavirus. Doctoral dissertation. University of Queensland, Australia.
23. Field, H., Crameri, G., Kung, N.Y. & Wang, L.F. (2012) Ecological aspects of hendra virus. Current topics in Microbiology and Immunology, 359, 11-23.
24. George, D.B., Webb, C.T., Farnsworth, M.L., O'Shea, T.J., Bowen, R.A., Smith, D.L. et al. (2011) Host and viral ecology determine bat rabies seasonality and maintenance. Proceedings of the National Academy Science USA, 108, 10208-10213.
25. Gloza-Rausch, F., Ipsen, A., Seebens, A., Gottsche, M., Panning, M., Felix Drexler, J. et al. (2008) Detection and prevalence patterns of group I coronaviruses in bats, northern Germany. Emerging Infectious Diseases, 14, 626-631.
26. Grotjan, H.E. & Keel, B.A. (1996) Immunoassay, 1st edn. Academic Press, Inc. Waltham, Massachusetts, USA.
27. Halpin, K., Young, P.L., Field, H.E. & MacKenzie, J.S. (2000) Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. Journal of General Virology, 81, 1927-1932.
28. Halpin, K., Hyatt, A.D., Fogarty, R., Middleton, D., Bingham, J., Epstein, J.H. 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.
29. Hayman, D.T., Suu-Ire, R., Breed, A.C., McEachern, J.A., Wang, L., Wood, J.L. et al. (2008) Evidence of henipavirus infection in West African fruit bats. PLoS ONE, 3, e2739.
30. Hayman, D.T., Fooks, A.R., Rowcliffe, J.M., McCrea, R., Restif, O., Baker, K.S. et al. (2012a) Endemic Lagos bat virus infection in Eidolon helvum. Epidemiology and Infection, 1-9; 140: 2163-2171.
31. Hayman, D.T.S., McCrea, R., Restif, O., Suu-Ire, R., Fooks, A.R., Wood, J.L.N. et al. (2012b) Demography of straw-colored fruit bats in Ghana. Journal of Mammalogy.; 93: 1393-1404.
32. Healy, M.J. (1972) Statistical analysis of radioimmunoassay data. The Biochemical Journal, 130, 207-210.
33. Hosseini, P.R., Dhondt, A.A. & Dobson, A. (2004) Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches. Proceedings of the Royal Society. B, Biological sciences, 271, 2569-2577.
34. Iehle, C., Razafitrimo, G., Razainirina, J., Andriaholinirina, N., Goodman, S.M., Faure, C. et al. (2007) Henipavirus and Tioman virus antibodies in Pteropodid Bats, Madagascar. Emerging Infectious Diseases, 13; 13: 159-61.
35. Kallio, E.R., Poikonen, A., Vaheri, A., Vapalahti, O., Henttonen, H., Koskela, E. et al. (2006) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proceedings of the Royal Society. B, Biological sciences, 273, 2771-2776.
36. Kallio, E.R., 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. B, Biological sciences, 277, 3783-3791.
37. Lefvert, A. (1998) Maternal Antibodies. Encyclopedia of Immunology (ed. P.J. Delves ), pp. 1671-1677. Elsevier Ltd, New York, NY, USA
38. Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J.H. et al. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science, 310, 676-679.
39. Li, Y., Wang, J., Hickey, A.C., Zhang, Y., Wu, Y., Zhang, H. et al. (2008) Antibodies to Nipah or Nipah-like Viruses in Bats, China. Emerging Infectious Diseases, 14, 1974-1976.
40. Lo, M.K., Lowe, L., Hummel, K.B., Sazzad, H.M., Gurley, E.S., Hossain, M.J. et al. (2012) Characterization of Nipah virus from outbreaks in Bangladesh, 2008-2010. Emerging Infectious Diseases, 18, 248-255.
41. Luby, S.P., Hossain, M.J., Gurley, E.S., Ahmed, B.N., Banu, S., Khan, S.U. et al. (2009) Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001-2007. Emerging Infectious Diseases, 15, 1229-1235.
42. Luis, A.D., Hayman, D.T., O'Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R. et al. (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?. Proceedings Biological sciences/The Royal Society, 280, 20122753.
43. Marsh, G.A., de Jong, C., Barr, J.A., Tachedjian, M., Smith, C., Middleton, D. et al. (2012) Cedar virus: a novel henipavirus isolated from Australian bats. PLoS Pathogens, 8, e1002836.
44. McFarlane, R., Becker, N. & Field, H. (2011) Investigation of the climatic and environmental context of Hendra virus spillover events 1994-2010. PLoS ONE, 6, e28374.
45. Middleton, D.J., Morrissy, C.J., van der Heide, B.M., Russell, G.M., Braun, M.A., Westbury, H.A. et al. (2007) Experimental Nipah virus infection in Pteropid bats (Pteropus poliocephalus). Journal of Comparative Pathology, 136, 266-272.
46. Motulsky, H. & Christopoulos, A. (2004) Fitting Models to Biological Data Using Linear and Nonlinear Regression: A Practical Guide to Curve Fitting, 1st edn. Oxford University Press, New York.
47. Muller, M.A., Ulrich, R.G., Reusken, C., Drexler, J.F., Lattwein, E., Biesold, S.E. et al. (2012) Antibody Prevalence Study for Human Pathogenic Viruses in Bats and Rodents. Ecohealth, Kunming, China.
48. Murray, P.K., Selleck, P.W., Hooper, P.T., Hyatt, A.D., Gould, A.R., Gleeson, L.J. et al. (1995) A Morbillivirus that caused fatal disease in horses and humans. Science, 268, 94-97.
49. Mutere, F.A. (1968) Breeding cycles in tropical bats in Uganda. Journal of Animal Ecology, 37, 8-9.
50. Peel, A.J. (2012) The epidemiology of Lagos bat virus and henipaviruses in straw coloured fruit bats (Eidolon helvum), using population genetics to infer population connectivity. Doctorate of Philosophy, University of Cambridge.
51. Peel, A.J., Baker, K.S., Crameri, G., Barr, J.A., Hayman, D.T., Wright, E. et al. (2012) Henipavirus neutralising antibodies in an isolated island population of african fruit bats. PLoS ONE, 7, e30346.
52. Peel, A.J., McKinley, T.J., Baker, K.S., Barr, J.A., Crameri, G., Hayman, D.T. et al. (2013) Use of cross-reactive serological assays for detecting novel pathogens in wildlife: assessing an appropriate cutoff for henipavirus assays in African bats. Journal of Virological Methods, 193, 295-303.
53. Plowright, R.K., Field, H.E., 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. B, Biological sciences, 275, 861-869.
54. Plowright, R.K., Foley, P., Field, H.E., Dobson, A.P., Foley, J.E., 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. B, Biological sciences, 278, 3703-3712.
55. Pomeroy, L.W., Bjornstad, O.N. & Holmes, E.C. (2008) The evolutionary and epidemiological dynamics of the paramyxoviridae. Journal of Molecular Evolution, 66, 98-106.
56. Potgieter, L.N. (1995) Immunology of bovine viral diarrhea virus. The Veterinary clinics of North America Food Animal Practice, 11, 501-520.
57. Rahman, S.A., Hassan, S.S., Olival, K.J., Mohamed, M., Chang, L.Y., Hassan, L. et al. (2010) Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerging Infectious Diseases, 16, 1990-1993.
58. Reynes, J.M., Counor, D., Ong, S., Faure, C., Seng, V., Molia, S. et al. (2005) Nipah virus in Lyle's flying foxes, Cambodia. Emerging Infectious Diseases, 11, 1042-1047.
59. Rivera-Benitez, J.F., Martinez-Bautista, R., Perez-Torres, A., Garcia-Contreras Adel, C., Reyes-Leyva, J., Hernandez, J. et al. (2013) Persistence of porcine rubulavirus in experimentally infected boars. Veterinary Microbiology, 162, 491-498.
60. Rogers, R.J., Douglas, I.C., Baldock, F.C., Glanville, R.J., Seppanen, K.T., Gleeson, L.J. et al. (1996) Investigation of a second focus of Equine Morbillivirus infection in coastal Queensland. Australian Veterinary Journal, 74, 243-244.
61. Roulin, A. & Heeb, P. (1999) The immunological function of allosuckling. Ecology Letters, 2, 319-324.
62. R-team, R.D.C.T. (2006) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
63. Sendow, I., Field, H.E., Curran, J., Darminto, Morrissy, C.J., Meehan, G. et al. (2006) Henipavirus in Pteropus Vampyrus bats, Indonesia. Emerging Infectious Diseases, 12, 711-712.
64. Sohayati, A.R., Hassan, L., Sharifah, S.H., Lazarus, K., Zaini, C.M., Epstein, J.H. et al. (2011) Evidence for Nipah virus recrudescence and serological patterns of captive Pteropus vampyrus. Epidemiology and Infection, 139, 1570-1579.
65. Tan, C.T., Goh, K.J., Wong, K.T., Sarji, S.A., Chua, K.B., Chew, N.K. et al. (2002) Relapsed and late-onset Nipah encephalitis. Annals of Neurology, 51, 703-708.
66. Thrusfield, M. (2005) Veterinary Epidemiology, 3rd edn. Blackwell Publishing, Oxford, UK.
67. Towner, J.S., Amman, B.R., Sealy, T.K., Carroll, S.A., Comer, J.A., Kemp, A. et al. (2009) Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathogens, 5, e1000536.
68. Wacharapluesadee, S., Lumlertdacha, B., Boongird, K., Wanghongsa, S., Chanhome, L., Rollin, P. et al. (2005) Bat Nipah virus, Thailand. Emerging Infectious Diseases, 11, 1949-1951.
69. Wacharapluesadee, S., Boongird, K., Wanghongsa, S., Ratanasetyuth, N., Supavonwong, P., Saengsen, D. et al. (2009) A Longitudinal study of the prevalence of Nipah virus in Pteropus lylei Bats in Thailand: evidence for seasonal preference in disease transmission. Vector Borne and Zoonotic Diseases.; 10: 183-90.
70. Weinberg, E.D. (1984) Pregnancy-associated depression of cell-mediated immunity. Reviews of Infectious Diseases, 6, 814-831.
71. Williamson, M.M., Hooper, P.T., Selleck, P.W., Gleeson, L.J., Daniels, P.W., Westbury, H.A. et al. (1998) Transmission studies of Hendra virus (Equine Morbillivirus) in fruit bats, horses and cats. Australian Veterinary Journal, 76, 813-818.
72. Williamson, M.M., Hooper, P.T., Selleck, P.W., Westbury, H.A. & Slocombe, R.F. (1999) Experimental Hendra virus infection in pregnant guinea-pigs and fruit bats (Pteropus poliocephalus). Journal of Comparative Pathology, 122, 201-207.
73. Wilson, E.B. (1927) Probable inference, the law of succession, and statistical inference. Journal of the American Statistical Association, 22, 209-212.
74. Zhu, Z., Bossart, K.N., Bishop, K.A., Crameri, G., Dimitrov, A.S., McEachern, J.A. et al. (2008) Exceptionally potent cross-reactive neutralization of Nipah and Hendra viruses by a human monoclonal antibody. Journal of Infectious Diseases, 197, 846-853.