Biannual birth pulses allow filoviruses to persist in bat populations

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1803, 2015, Pages

  Hayman, David T S ^a  

^a MASSEY UNIVERSITY   (New Zealand)

Author keywords

Bats; Critical community size; Ebola; Filovirus; Marburg; Seasonality

Indexed keywords

BAT; COLONY; DISEASE TRANSMISSION; HOST-PATHOGEN INTERACTION; MORTALITY; PROBABILITY; PUBLIC HEALTH; SEASONALITY; VIRAL DISEASE;

EBOLA VIRUS; MARBURGVIRUS; ROUSETTUS AEGYPTIACUS;

EID: 84922573233     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.2591     Document Type: Article

References (67)

1. Kermack WO, McKendrick AG. 1927 Contribution to the mathematical theory of epidemics.Proc. R. Soc. Lond. A 115, 700-721. (doi:10.1098/rspa.1927.0118)
2. Kermack WO, McKendrick AG. 1932 Contributions to the mathematical theory of epidemics II—The problem of endemicity. Proc. R. Soc. Lond. A 138, 55-83. (doi:10.1098/rspa.1932.0171)
3. Kermack WO, McKendrick AG. 1933 Contributions to the mathematical theory of epidemics III—Further studies of this problem of endemicity. Proc. R. Soc. Lond. A 141, 94-122. (doi:10.1098/rspa.1933.0106)
4. Bartlett MS. 1957 Mealses periodicity and community size. J. R. Stat. Soc. A 120, 48–70. (doi:10.2307/2342553)
5. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008 Global trends in emerging infectious diseases. Nature 451, 990-993. (doi:10.1038/nature06536)
6. Luis AD et al. 2013 A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. R. Soc. B 280, 20122753. (doi:10.1098/rspb.2012.2753)
7. World Health Organization. 2014 Situation reports: Ebola response roadmap. See http://apps.who.int/iris/bitstream/10665/136508/1/roadmapsitrep 15Oct2014.pdf?ua=1.
8. Brauburger K, Hume AJ, Muhlberger E, Olejnik J. 2012 Forty-five years of Marburg virus research.Viruses Basel 4, 1878-1927. (doi:10.3390/v4101878)
9. Bausch DG et al. 2003 Risk factors for Marburg hemorrhagic fever, Democratic Republic of the Congo. Emerg. Infect. Dis 9, 1531-1537. (doi:10.3201/eid0912.030355)
10. Swanepoel R, Leman PA, Burt FJ, Zachariades NA, Braack LE, Ksiazek TG, Rollin PE, Zaki SR, Peters CJ. 1996 Experimental inoculation of plants and animals with Ebola virus. Emerg. Infect. Dis. 2, 321-325. (doi:10.3201/eid0204.960407)
11. Leroy EM et al. 2005 Fruit bats as reservoirs of Ebola virus. Nature 438, 575-576. (doi:10.1038/438575a)
12. Olival KJ, Hayman DT. 2014 Filoviruses in bats: current knowledge and future directions. Viruses 6, 1759-1788. (doi:10.3390/v6041759)
13. Paweska JT, Jansen van Vuren P, Masumu J, Leman PA, Grobbelaar AA, Birkhead M, Clift S, Swanepoel R, Kemp A. 2012 Virological and serological findings in Rousettus aegyptiacus experimentally inoculated with vero cells-adapted hogan strain of Marburg virus. PLoS ONE 7, e45479. (doi:10.1371/journal.pone.0045479)
14. Taniguchi S et al. 2011 Reston Ebolavirus antibodies in bats, the Philippines. Emerg. Infect. Dis. 17, 1559-1560. (doi:10.3201/eid1708.101693)
15. Olival KJ et al. 2013 Ebola virus antibodies in fruit bats, Bangladesh. Emerg. Infect. Dis. 19, 270–273. (doi:10.3201/eid1902.120524)
16. Yuan JF, Zhang YJ, Li JL, Zhang YZ, Wang LF, Shi ZL. 2012 Serological evidence of ebolavirus infection in bats, China. Virol. J. 9, 236. (doi:10.1186/1743-422x-9-236)
17. Negredo A et al. 2011 Discovery of an Ebolavirus-like Filovirus in Europe. PLoS Pathog. 7, e1002304. (doi:10.1371/journal.ppat.1002304)
18. Hayman DT, Bowen RA, Cryan PM, McCracken GF, O’Shea TJ, Peel AJ, Gilbert A, Webb CT, Wood JL. 2013 Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses Public Health 60, 2-21. (doi:10.1111/zph.12000)
19. Barcley RMR, Harder LD. 2003 Life histories of bats: life in the slow lane. In Bat ecology (eds TH Kunz, MB Fenton), pp. 209–256. Chicago, IL: The University of Chicago Press.
20. Kallio ER, Begon M, Henttonen H, Koskela E, Mappes T, Vaheri A, Vapalahti O. 2010 Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proc. R. Soc. B 277, 3783-3791. (doi:10.1098/rspb.2010.1022)
21. Garnier R, Ramos R, Staszewski V, Militao T, Lobato E, Gonzalez-Solis J, Boulinier T. 2012 Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology. Proc. R. Soc. B 279, 2033-2041. (doi:10.1098/rspb.2011.2277)
22. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. 2006 Seasonality and the dynamics of infectious diseases. Ecol. Lett. 9, 467-484. (doi:10.1111/j.1461-0248.2005.00879.x)
23. Peel AJ, Pulliam JRC, Luis AD, Plowright RK, O’Shea TJ, Hayman DTS, Wood JLN, Webb CT, Restif O. 2014 The effect of seasonal birth pulses on pathogen persistence in wild mammal populations.Proc. R. Soc. B 281, 20132962. (doi:10.1098/rspb.2013.2962)
24. Amman BR et al. 2012 Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathog. 8, e1002877. (doi:10.1371/journal.ppat.1002877)
25. Mondul AM, Krebs JW, Childs JE. 2003 Trends in national surveillance for rabies among bats in the United States (1993–2000). J. Am. Vet. Med. Assoc. 222, 633-639. (doi:10.2460/javma.2003.222.633)
26. Drexler JF, Corman VM, Wegner T, Tateno AF, Zerbinati RM, Gloza-Rausch F, Seebens A, Muller MA, Drosten C. 2011 Amplification of emerging viruses in a bat colony. Emerg. Infect. Dis. 17, 449-456. (doi:10.3201/eid1703.100526)
27. Patyk K, Turmelle A, Blanton JD, Rupprecht CE. 2012 Trends in national surveillance data for bat rabies in the United States: 2001–2009. Vector Borne Zoonotic Dis. 12, 666-673. (doi:10.1089/vbz.2011.0839)
28. Anderson RM, May RM. 1979 Population biology of infectious diseases: part I. Nature 280, 361–367. (doi:10.1038/280361a0)
29. George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, Stanley TR, Ellison LE, Rupprecht CE. 2011 Host and viral ecology determine bat rabies seasonality and maintenance. Proc. Natl Acad. Sci. USA 108, 10208–10213. (doi:10.1073/pnas.1010875108)
30. Restif O et al. 2012 Model-guided fieldwork: practical guidelines for multidisciplinary research on wildlife ecological and epidemiological dynamics. Ecol. Lett. 15, 1083-1094. (doi:10.1111/j.1461-0248.2012.01836.x)
31. Lekone PE, Finkenstadt BF. 2006 Statistical inference in a stochastic epidemic SEIR model with control intervention: Ebola as a case study. Biometrics 62, 1170-1177. (doi:10.1111/j.1541-0420.2006.00609.x)
32. Legrand J, Grais RF, Boelle PY, Valleron AJ, Flahault A. 2007 Understanding the dynamics of Ebola epidemics. Epidemiol. Infect. 135, 610–621. (doi:10.1017/S0950268806007217)
33. Chowell G, Hengartner NW, Castillo-Chavez C, Fenimore PW, Hyman JM. 2004 The basic reproductive number of Ebola and the effects of public health measures: the cases of Congo and Uganda. J. Theor. Biol. 229, 119-126. (doi:10.1016/j.jtbi.2004.03.006)
34. Hayman DTS, Emmerich P, Yu M, Wang LF, Suu-Ire R, Fooks AR, Cunningham AA, Wood JLN. 2010 Long-term survival of an urban fruit bat seropositive for Ebola and Lagos bat viruses. PLoS ONE 5, e11978. (doi:10.1371/journal.pone.0011978)
35. Hayman DTS, McCrea R, Restif O, Suu-Ire R, Fooks AR, Wood JLN, Cunningham AA, Rowcliffe JM. 2012 Demography of straw-colored fruit bats in Ghana. J. Mammal. 93, 1393-1404. (doi:10.1644/11-MAMM-A-270.1)
36. Begon M, Bennett M, Bowers RG, French NP, Hazel SM, Turner J. 2002 A clarification of transmission terms in host–microparasite models: numbers, densities and areas. Epidemiol. Infect. 129, 147-153. (doi:10.1017/S0950268802007148)
37. Mutere FA. 1967 The breeding biology of equatorial vertebrates; reproduction in the fruit bat Eidolon helvum, at latitude 08200N. J. Zool. 153, 153–161. (doi:10.1111/j.1469-7998.1967.tb04058.x)
38. King AA, Ionides EL, Breto CM, Ellner S, Kendall B. 2009 pomp: statistical inference for partially observed Markov processes. See http://pomp.r-forge.r-rproject.org.
39. R Development Core Team. 2012 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
40. Nelder JA, Mead R. 1965 A simplex algorithm for function minimization. Comput. J. 7, 308–313. (doi:10.1093/comjnl/7.4.308)
41. Hayman DT et al. 2012 Endemic Lagos bat virus infection in Eidolon helvum. Epidemiol. Infect. 140, 2163-2171. (doi:10.1017/S0950268812000167)
42. Towner JS et al. 2007 Marburg virus infection detected in a common African bat. PLoS ONE 2, e764. (doi:10.1371/journal.pone.0000764)
43. Cox DR, Oakes D. 1984 Analysis of survival data. London, UK: Chapman and Hall.
44. Collett D. 1994 Modelling survival data in medical research. London, UK: Chapman and Hall.
45. Hens N, Shkedy Z, Aerts M, Faes C, Van Damme P, Beutels P. 2012 Modeling infectious disease parameters based on serological and social contact data. New York, NY: Springer.
46. Blower SM, Dowlatabadi H. 1994 Sensitivity and uncertainty analysis of complex-models of disease transmission—an HIV model, as an example. Int Stat. Rev. 62, 229-243. (doi:10.2307/1403510)
47. Carnell R. 2009 lhs: Latin hypercube samples. R package version 0.10. http://CRAN.R-project.org/ package=lhs.
48. Hayman DT, Suu-Ire R, Breed AC, McEachern JA, Wang L, Wood JL, Cunningham AA. 2008 Evidence of henipavirus infection in West African fruit bats. PLoS ONE 3, e2739. (doi:10.1371/journal.pone.0002739)
49. Hayman DT, Yu M, Crameri G, Wang LF, Suu-Ire R, Wood JL, Cunningham AA. 2012 Ebola virus antibodies in fruit bats, Ghana, West Africa. Emerg. Infect. Dis. 18, 1207-1209. (doi:10.3201/eid1807.111654)
50. Towner JS et al. 2009 Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 5, e1000536. (doi:10.1371/journal.ppat.1000536)
51. Wacharapluesadee S, Boongird K, Wanghongsa S, Ratanasetyuth N, Supavonwong P, Saengsen D, Gongal GN, Hemachudha T. 2010 A longitudinal study of the prevalence of Nipah virus in Pteropus lylei bats in Thailand: evidence for seasonal preference in disease transmission. Vector Borne Zoonotic Dis. 10, 183-190. (doi:10.1089/vbz.2008.0105)
52. 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 spp.). Proc. R. Soc. B 278, 3703–3712. (doi:10.1098/rspb.2011.0522)
53. Albarino CG, Uebelhoer LS, Vincent JP, Khristova ML, Chakrabarti AK, McElroy A, Nichol ST, Towner JS. 2013 Development of a reverse genetics system to generate recombinant Marburg virus derived from a bat isolate. Virology 446, 230-237. (doi:10.1016/j.virol.2013.07.038)
54. Towner JS. 2013 Bats as reservoirs of filoviruses (data from recent challenges). Bat Res. News 54, Abstracts of papers presented at the 16th International Bat Research Conference and the 43rd Annual Meeting of the North American Society for Bat Research, San Jose, Costa Rica, pp. 71–226.
55. Hadjisterkotis E. 2006 The destruction and conservation of the Egyptian Fruit bat Rousettus aegyptiacus in Cyprus: a historic review. Eur. J. Wildl. Res. 52, 282-287. (doi:10.1007/s10344-006-0041-7)
56. Chen JP, Rossiter SJ, Flanders JR, Sun YH, Hua PY, Miller-Butterworth C, Liu XS, Rajan KE, Zhang SY. 2010 Contrasting genetic structure in two co-distributed species of Old World fruit bat. PLoS ONE 5, e13903. (doi:10.1371/journal.pone.0013903)
57. Epstein JH et al. 2009 Pteropus vampyrus, a hunted migratory species with a multinational home-range and a need for regional management. J. Appl. Ecol. 46, 991-1002. (doi:10.1111/j.1365-2664.2009.01699.x)
58. Olival KJ. 2008 Population genetic structure and phylogeography of Southeast Asian flying foxes: implications for conservation and disease ecology. New York, NY: Columbia University.
59. Rahman SA et al. 2010 Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerg. Infect. Dis. 16, 1990–1993. (doi:10.3201/eid1612.091790)
60. Olival KJ, Dick CW, Simmons NB, Morales JC, Melnick DJ, Dittmar K, Perkins SL, Daszak P, Desalle R. 2013 Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia. Parasites Vectors 6, 231. (doi:10.1186/1756-3305-6-231)
61. Peel AJ et al. 2013 Continent-wide panmixia of an African fruit bat facilitates transmission of potentially zoonotic viruses. Nat. Commun. 4, 2770. (doi:10.1038/ncomms3770)
62. Gilbert AT et al. 2013 Deciphering serology to understand the ecology of infectious diseases in wildlife. EcoHealth 10, 298-313. (doi:10.1007/s10393-013-0856-0)
63. World Health Organization. 2014 Ebola Haemorrhagic Fever, Guinea (Situation as of 27 March 2014). See http://www.afro.who.int/en/clusters-a-programmes/dpc/epidemic-a-pandemic-alert-and-response/outbreak-news/4069-ebola-haemorrhagic-fever-guinea-27-march-2014.html.
64. World Health Organization. 2014 Ebola virus disease outbreak—Democratic Republic of the Congo— update 10 September 2014. See http://www.afro.who.int/en/clusters-a-programmes/dpc/epidemic-a-pandemic-alert-and-response/outbreak-news/4272-ebola-virus-disease-outbreak-drc-10-september-2014.html.
65. World Health Organization. 2014 Marburg virus disease—Uganda. See http://www.afro.who.int/en/clusters-a-programmes/dpc/epidemic-a-pandemic-alert-and-response/outbreak-news/4272-ebola-virus-disease-outbreak-drc-10-september-2014.html.
66. Pybus OG, Fraser C, Rambaut A. 2013 Evolutionary epidemiology: preparing for an age of genomic plenty. Phil. Trans. R. Soc. B 368, 20120193. (doi:10.1098/rstb.2012.0193)
67. Wood JL et al. 2012 A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study. Phil. Trans. R. Soc. B 367, 2881-2892. (doi:10.1098/rstb.2012.0228)