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. 2007;315:363–387. doi: 10.1007/978-3-540-70962-6_15

Ebolavirus and Other Filoviruses

E Leroy §, J P Gonzalez §, X Pourrut §
Editors: James E Childs5, John S Mackenzie6, Jürgen A Richt7
PMCID: PMC7121322  PMID: 17848072

Abstract

Since Ebola fever emerged in Central Africa in 1976, a number of studies have been undertaken to investigate its natural history and to characterize its transmission from a hypothetical reservoir host(s) to humans. This research has comprised investigations on a variety of animals and their characterization as intermediate, incidental, amplifying, reservoir, or vector hosts. A viral transmission chain was recently unveiled after a long absence of epidemic Ebola fever. Animal trapping missions were carried out in the Central African rain forest in an area where several epidemics and epizootics had occurred between 2001 and 2005. Among the various animals captured and analyzed, three species of fruit bats (suborder Megachiroptera) were found asymptomatically and naturally infected with Ebola virus: Hypsignathus monstrosus (hammer-headed fruit beats), Epomops franqueti (singing fruit bats), and Myonycteris torquata (little collared fruit bats).

Keywords: Reservoir Host, Nipah Virus, Secondary Host, Marburg Virus, Incidental Host

Contributor Information

James E. Childs, Email: Jamesechilds@comcast.net

John S. Mackenzie, Email: J.Mackenzie@curtin.edu.au

Jürgen A. Richt, Email: juergen.richt@ars.usda.gov

J. P. Gonzalez, Email: frjpg@mahidol.ac.th

References

  1. Allela L, Boury O, Pouillot R, Delicat A, Yaba P, Kumulungui B, Rouquet P, Gonzalez JP, Leroy EM. Ebola virus antibody prevalence in dogs and human risk. Emerg Infect Dis. 2005;11:385–390. doi: 10.3201/eid1103.040981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amengual B, Whitby JE, King A, Cobo JS, Bourhy H. Evolution of European bat lyssaviruses. J Gen Virol. 1997;78:2319–2328. doi: 10.1099/0022-1317-78-9-2319. [DOI] [PubMed] [Google Scholar]
  3. Arata AA, Johnson B. Approaches towards studies on potential reservoirs of viral haemorrhagic fever in southern Sudan. In: Pattyn SR, editor. Ebola virus haemorrhagic fever. Amsterdam: Elsevier/Netherland biomedical; 1977. pp. 191–202. [Google Scholar]
  4. Badrane H, Tordo N. Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders. J Virol. 2001;75:8096–8104. doi: 10.1128/JVI.75.17.8096-8104.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bausch DG, Borchert M, Grein T, Roth C, Swanepoel R, Libande ML, Talarmin A, Bertherat E, Muyembe-Tamfum JJ, Tugume B, Colebunders R, Konde KM, Pirad P, Olinda LL, Rodier GR, Campbell P, Tomori O, Ksiazek TG, Rollin PE. Risk factors for Marburg hemorrhagic fever Democratic Republic of the Congo. Emerg Infect Dis. 2003;9:1531–1537. doi: 10.3201/eid0912.030355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bergmans W. Taxonomy and biogeography of African fruit bats (Mammalia Megachiroptera) Beaufortia. 1989;39:89–152. [Google Scholar]
  7. Bertherat E, Talarmin A, Zeller H. La République Démocratique du Congo: Entre guerre civile et Virus de Marburg. Le Comité de Cooridantion Scienctifique et Technique International pour l’épideemie de Durba. Med Tropic. 1999;59:201–204. [PubMed] [Google Scholar]
  8. Breman JG, Johnson KM, van der Groen G, Robbins CB, Szczeniowski MV, Ruti K, Webb PA, Meier F, Heymann DL. A search for Ebola virus in animals in the Democratic Republic of the Congo and Cameroon: ecologic, virologic, and serologic surveys, 1979–1980. J Infect Dis. 1999;179:S139–S147. doi: 10.1086/514278. [DOI] [PubMed] [Google Scholar]
  9. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev. 2006;19:531–545. doi: 10.1128/CMR.00017-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Centers for Disease Control Ebola-Reston virus infection among quarantined nonhuman primates–Texas, 1996. Morb Mortal Wkly Rep. 1996;45:314–316. [PubMed] [Google Scholar]
  11. Constantine DG, Tierkel ES, Kleckner MD, Hawkins DM. Rabies in New Mexico cavern bats. Pub Health Rep. 1968;83:303–316. [PMC free article] [PubMed] [Google Scholar]
  12. Feldmann H, Wahl-Jensen V, Jones SM, Stroher U. Ebola virus ecology: a continuing mystery. Trends Microbiol. 2004;12:433–437. doi: 10.1016/j.tim.2004.08.009. [DOI] [PubMed] [Google Scholar]
  13. Formenty P, Boesch C, Wyers M, Steiner C, Donati F, Dind F, Walker F, Le Guenno B. Ebola virus outbreak among wild chimpanzees living in a rain forest of Cote d’Ivoire. J Infect Dis. 1999;179:120–126. doi: 10.1086/514296. [DOI] [PubMed] [Google Scholar]
  14. Geisbert TW, Jahrling PB, Hanes MA, Zack PM. Association of Ebola-related Reston virus particles and antigen with tissue lesions of monkeys imported to the United States. J Comp Pathol. 1992;106:137–152. doi: 10.1016/0021-9975(92)90043-T. [DOI] [PubMed] [Google Scholar]
  15. Gonzalez JP, McCormick JB, Saluzzo JF, Georges AJ. Les fièvres hémorragiques africaines d’origine virale en République Centrafricaine. Cah ORSTOM Ser Ent Méd Parasit. 1983;XXI:119–130. [Google Scholar]
  16. Gonzalez JP, Herbreteau V, Morvan J, Leroy EM. Ebola virus circulation in Africa: a balance between clinical expression and epidemiological silence. Bull Soc Pathol Exot. 2005;98:210–217. [PubMed] [Google Scholar]
  17. Halpin K, Young PL, Field HE, Mackenzie JS. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol. 2000;81:1927–1932. doi: 10.1099/0022-1317-81-8-1927. [DOI] [PubMed] [Google Scholar]
  18. Heymann DL, Weisfeld JS, Webb PA, Johnson KM, Cairns T, Berquist H. Ebola hemorrhagic fever: Tandala 1977–1978. J Infect Dis. 1980;142:372–376. doi: 10.1093/infdis/142.3.372. [DOI] [PubMed] [Google Scholar]
  19. Hill JE, Smith JD. Bats: a natural history. Austin: University of Texas Press; 1984. [Google Scholar]
  20. Huijbregts B, De Wachter P, Ndong Obiang S, Akou Ella M. Ebola and the decline of gorilla Gorilla gorilla and chimpanzee Pan troglodytes populations in Minkebe forest, north-eastern Gabon. Oryx. 2003;37:437–443. doi: 10.1017/S0030605303000802. [DOI] [Google Scholar]
  21. Jahrling PB, Geisbert TW, Jaax NK, Hanes MA, Ksiazek TG, Peters CJ. Experimental infection of cynomolgus macaques with Ebola-Reston filoviruses from the 1989–1990 US epizootic. Arch Virol Suppl. 1996;11:115–134. doi: 10.1007/978-3-7091-7482-1_11. [DOI] [PubMed] [Google Scholar]
  22. Johnson KM. Ebola haemorrhagic fever in Zaire (1976) World Health Organ. 1976;56:271–293. [PMC free article] [PubMed] [Google Scholar]
  23. Kiley MP, Bowen ET, Eddy GA, Isaacson M, Johnson KM, McCormick JB, Murphy FA, Pattyn SR, Peters D, Prozesky OW, Regnery RL, Simpson DI, Slenczka W, Sureau P, van der Groen G, Webb PA, Wulff H. Filoviridae: a taxonomic home for Marburg and Ebola viruses? Intervirology. 1982;18:24–32. doi: 10.1159/000149300. [DOI] [PubMed] [Google Scholar]
  24. Kuzmin IV, Orciari LA, Arai YT, Smith JS, Hanlon CA, Kameoka Y, Rupprecht CE. Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P, G gene sequences. Virus Res. 2003;97:65–79. doi: 10.1016/S0168-1702(03)00217-X. [DOI] [PubMed] [Google Scholar]
  25. Kuzmin IV, Hughes GJ, Botvinkin AD, Orciari LA, Rupprecht CE. Phylogenetic relationships of Irkut and West Caucasian bat viruses within the Lyssavirus genus and suggested quantitative criteria based on the N gene sequence for lyssavirus genotype definition. Virus Res. 2005;111:28–43. doi: 10.1016/j.virusres.2005.03.008. [DOI] [PubMed] [Google Scholar]
  26. Langevin P, Barclay RMR. Hypsignathus monstrosus. Mammal Species. 1990;357:1–4. doi: 10.2307/3504110. [DOI] [Google Scholar]
  27. Leirs H, Mills JN, Krebs JW, Childs JE, Akaibe D, Woollen N, Ludwig G, Peters CJ, Ksiazek TG. Search for the Ebola virus reservoir in Kikwit Democratic Republic of the Congo: reflections on a vertebrate collection. J Infect Dis. 1999;179:S155–S163. doi: 10.1086/514299. [DOI] [PubMed] [Google Scholar]
  28. Leroy EM, Rouquet P, Formenty P, Souquiere S, Kilbourne A, Froment JM, Bermejo M, Smit S, Karesh W, Swanepoel R, Zaki SR, Rollin PE. Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science. 2004;303:387–390. doi: 10.1126/science.1092528. [DOI] [PubMed] [Google Scholar]
  29. Leroy EM, Telfer P, Kumulungui B, Yaba P, Rouquet P, Roques P, Gonzalez JP, Ksiazek TG, Rollin PE, Nerrienet E. A serological survey of Ebola virus infection in central African nonhuman primates. J Infect Dis. 2004;190:1895–1899. doi: 10.1086/425421. [DOI] [PubMed] [Google Scholar]
  30. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Delicat A, Paweska JT, Gonzalez JP, Swanepoel R. Fruit bats as reservoirs of Ebola virus. Nature. 2005;438:575–576. doi: 10.1038/438575a. [DOI] [PubMed] [Google Scholar]
  31. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310(5748):676–679. doi: 10.1126/science.1118391. [DOI] [PubMed] [Google Scholar]
  32. Mackenzie JS. Emerging zoonotic encephalitis viruses: lessons from Southeast Asia and Oceania. J Neurovirol. 2005;1:434–440. doi: 10.1080/13550280591002487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Martini GA, Siegert R. Marburg virus disease. Berlin Heidelberg New York: Springer; 1971. p. 131. [Google Scholar]
  34. Miranda ME, Ksiazek TG, Retuya TJ, Khan AS, Sanchez A, Fulhorst CF, Rollin PE, Calaor AB, Manalo DL, Roces MC, Dayrit MM, Peters CJ. Epidemiology of Ebola (subtype Reston) virus in the Philippines, 1996. J Infect Dis. 1999;179:115–119. doi: 10.1086/514314. [DOI] [PubMed] [Google Scholar]
  35. Monath TP. Ecology of Marburg and Ebola viruses: speculations and directions for the future research. J Infect Dis. 1999;179:S127–S138. doi: 10.1086/514281. [DOI] [PubMed] [Google Scholar]
  36. Morvan JM, Deubel V, Gounon P, Nakoune E, Barriere P, Murri S, Perpete O, Selekon B, Coudrier D, Gautier-Hion A, Colyn M, Volehkov V. Identification of Ebola virus sequences present as RNA or DNA in organs of terrestrial small mammals of the Central African Republic. Microbes Infect. 1999;1:1193–1201. doi: 10.1016/S1286-4579(99)00242-7. [DOI] [PubMed] [Google Scholar]
  37. Morvan JM, Nakoune E, Deubel V, Colyn M. Forest ecosystems and Ebola virus. B Soc Pathol Exot. 2000;93:172–175. [PubMed] [Google Scholar]
  38. Pinzon JE, Wilson JM, Tucker CJ, Arthur R, Jahrling PB, Formenty P. Trigger events: enviroclimatic coupling of Ebola hemorrhagic fever outbreaks. Am J Trop Med Hyg. 2004;71:664–674. [PubMed] [Google Scholar]
  39. Pourrut X, Kumulungui B, Wittmann T, Moussavou G, Delicat A, Yaba P, Nkoghe D, Gonzalez JP, Leroy EM. The natural History of Ebola virus in Africa. Microbes Infect. 2005;7:1005–1014. doi: 10.1016/j.micinf.2005.04.006. [DOI] [PubMed] [Google Scholar]
  40. Reiter P, Turell M, Coleman R, Miller B, Maupin G, Liz J, Kuehne A, Barth J, Geisbert J, Dohm D, Glick J, Pecor J, Robbins R, Jahrling P, Peters C, Ksiazek T. Field investigations of an outbreak of Ebola hemorrhagic fever Kikwit Democratic Republic of the Congo, 1995: arthropod studies. J Infect Dis. 1999;179:S148–S154. doi: 10.1086/514304. [DOI] [PubMed] [Google Scholar]
  41. Rollin PE, Williams RJ, Bressler DS, Pearson S, Cottingham M, Pucak G, Sanchez A, Trappier SG, Peters RL, Greer PW, Zaki S, Demarcus T, Hendricks K, Kelley M, Simpson D, Geisbert TW, Jahrling PB, Peters CJ, Ksiazek TG. Ebola (subtype Reston) virus among quarantined nonhuman primates recently imported from the Philippines to the United States. J Infect Dis. 1999;179:108–114. doi: 10.1086/514303. [DOI] [PubMed] [Google Scholar]
  42. Shaman J, Day JF, Stieglitz M. Drought-induced amplification of Saint Louis encephalitis virus Florida. Emerg Infect Dis. 2002;8:575–580. doi: 10.3201/eid0801.010049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sulkin SE, Allen R (1974) Virus infections in bats. In: Melnick JL (ed) Monographs in Virolology 8. Karger, Basel. [PubMed]
  44. Swanepoel R, Leman PA, Burt FJ. Experimental inoculation of plants and animals with Ebola virus. Emerg Infect Dis. 1996;2:321–325. doi: 10.3201/eid0204.960407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Walsh PD, Abernethy KA, Bermejo M, Beyers R, De Wachter P, Akou ME, Huijbregts B, Mambounga DI, Toham AK, Kilbourn AM, Lahm SA, Latour S, Maisels F, Mbina C, Mihindou Y, Obiang SN, Effa EN, Starkey MP, Telfer P, Thibault M, Tutin CE, White LJ, Wilkie DS. Catastrophic ape decline in western equatorial Africa. Nature. 2003;422:611–614. doi: 10.1038/nature01566. [DOI] [PubMed] [Google Scholar]
  46. Walsh PD, Biek R, Real LA. Wave-like spread of Ebola Zaire. PLoS Biol. 2005;3:e371. doi: 10.1371/journal.pbio.0030371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Yob JM, Field H, Rashdi AM, Morrissy C, van der Heide B, Rota P, bin Adzhar A, White J, Daniels P, Jamaluddin A, Ksiazek T. Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerg Infect Dis. 2001;7:439–441. doi: 10.3201/eid0703.010312. [DOI] [PMC free article] [PubMed] [Google Scholar]

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