Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 24, Number 12—December 2018

Survey of Ebola Viruses in Frugivorous and Insectivorous Bats in Guinea, Cameroon, and the Democratic Republic of the Congo, 2015–2017

Helene M. De Nys1, Placide Mbala Kingebeni1, Alpha K. Keita1, Christelle Butel, Guillaume Thaurignac, Christian-Julian Villabona-Arenas, Thomas Lemarcis, Mare Geraerts, Nicole Vidal, Amandine Esteban, Mathieu Bourgarel, François Roger, Fabian Leendertz, Ramadan Diallo, Simon-Pierre Ndimbo-Kumugo, Justus Nsio-Mbeta, Nikki Tagg, Lamine Koivogui, Abdoulaye Toure, Eric Delaporte, Steve Ahuka-Mundeke, Jean-Jacques Muyembe Tamfum, Eitel Mpoudi-Ngole, Ahidjo Ayouba2, and Martine Peeters2Comments to Author 

Author affiliations: TransVIHMI of Institut de Recherche pour le Développement, Institut National de la Santé et de la Recherche Médicale and University of Montpellier, Montpellier, France (H.M. De Nys, P. Mbala Kingebeni, A.K. Keita, C. Butel, G. Thaurignac, C.-J. Villabona-Arenas, T. Lemarcis, M. Geraerts, N. Vidal, A. Esteban, A. Toure, E. Delaporte, A. Ayouba, M. Peeters); National Institute of Biomedical Research, Kinshasa, Democratic Republic of the Congo (P. Mbala Kingebeni, S.-P. Ndimbo-Kumugo, S. Ahuka-Mundeke, J.-J. Muyembe Tamfum); Cliniques Universitaires de Kinshasa, Kinshasa (P. Mbala Kingebeni, S. Ahuka-Mundeke, J.-J. Muyembe Tamfum); Centre de Recherche et de Formation en Infectiologie de Guinée, Conakry, Guinea (A.K. Keita, A. Toure); ASTRE of Centre de coopération internationale en recherche agronomique pour le développement, Institut national de la Recherche Agronomique and Univerisity of Montpellier, Montpellier (M. Bourgarel, F. Roger); Robert Koch-Institute, Berlin, Germany (F. Leendertz); Ministère de l’Elevage et des Productions Animales, Conakry (R. Diallo); Direction de Lutte contre la Maladie, Kinshasa (J. Nsio-Mbeta); Royal Zoological Society of Antwerp, Antwerp, Belgium (N. Tagg); Université de Conakry, Conakry (L. Koivogui); Institut National de Sante Publique, Conakry (A. Toure); Institut de Recherches Médicales et d’Études des Plantes Médicinales, Yaoundé, Cameroon (E. Mpoudi-Ngole); Cameroon Institut de Recherche pout le Développement, Yaoundé (E. Mpoudi-Ngole)

Main Article

Table 5

Zaire Ebola virus antibodies in insectivorous bats from our research, Guinea, Cameroon, and the DRC, 2015–2017, and other published studies*

Family Species Country Year of study (reference) Test No. tested No. (%) positive† Total, no. positive/tested (%)†
Emballonuridae Coleura afra Cameroon 2015–2017‡ Luminex 5 0–0 (0–0) 0/14 (0)

Saccolaimus peli
1979–1980 (26)
0 (0)

Hipposideridae Hipposideros sp. DRC 2015–2017‡ Luminex 157 0–0 (0–0) 0/1,395 (0)
Hipposideros sp. Cameroon 2015–2017‡ Luminex 837 0–0 (0–0)
Hipposideros sp. DRC 1979–1980 (26) IFA 69 0 (0)
Hipposideros sp. Guinea 2015–2017‡ Luminex 288 0–0 (0–0)

Hipposideros sp.
2014 (11)
0 (0)

Miniopteridae Miniopterus sp. Guinea 2015–2017‡ Luminex 27 0–0 (0–0) 0/234 (0)
Miniopterus sp. DRC 2015–2017‡ Luminex 205 0–0 (0–0)

M. minor
1995 (27)
0 (0)

Molossidae Chaerephon sp. Guinea 2015–2017‡ Luminex 44 0–0 (0–0) 0/401 (0)
C. pumilus Guinea 2014 (11) ELISA 1 0 (0)
C. ansorgei DRC 1995 (27) ELISA 120 0 (0)
C. major DRC 1979–1980 (26) IFA 26 0 (0)

C. pumilus
1995 (27)
0 (0)

Mops sp. Guinea 2015–2017‡ Luminex 230 0–0 (0–0) 4–9/705 (0.6–1.3)
Mops sp. Cameroon 2015–2017‡ Luminex 264 1–6 (0.4–2.3)
Mops sp. DRC 1979–1980 (26) IFA 158 0 (0)
Mops sp. DRC 1995 (27) ELISA 28 0 (0)
Mops condylurus Gabon 2003–2008 (13) ELISA 24 3 (12.5)
M. condylurus Guinea 2014 (11) ELISA 1 0 (0)

Myopterus whitleyi
1995 (27)
0 (0)

Nycteridae Nycteris sp. Guinea 2015–2017‡ Luminex 15 0–0 (0–0) 0/43 (0)
Nycteris sp. Guinea 2014 (11) ELISA 6 0 (0)
Nycteris sp. Cameroon 2015–2017‡ Luminex 7 0–0 (0–0)
Nycteris sp. DRC 1979–1980 (26) IFA 14 0 (0)

Nycteris hispida
1995 (27)
0 (0)

Rhinolophidae Rhinolophus sp. Guinea 2015–2017‡ Luminex 26 0–0 (0–0) 0/86 (0)
Rhinolophus sp. DRC 2015–2017‡ Luminex 6 0–0 (0–0)

Rhinolophus sp.
0–0 (0–0)

Vespertilionidae Glauconycteris variegata Cameroon 2015–2017‡ Luminex 3 0–0 (0–0) 0/143 (0)
Chalinolobus sp. DRC 1979–1980 (26) IFA 15 0 (0)
Eptesicus sp. DRC 1979–1980 (26) IFA 22 0 (0)
Eptesicus tenuipinnis DRC 1995 (27) ELISA 1 0 (0)
Kerivoula sp. Guinea 2014 (11) ELISA 1 0 (0)
Kerivoula sp. Cameroon 2015–2017‡ Luminex 1 0–0 (0–0)
Myotis bocagii Cameroon 2015–2017‡ Luminex 3 0–0 (0–0)
M. bocagii DRC 1995 (27) ELISA 22 0 (0)
M. bocagii DRC 1979–1980 (26) IFA 17 0 (0)
Neoromicia sp. Cameroon 2015–2017‡ Luminex 5 0–0 (0–0)
Pipistrellus nanus DRC 1995 (27) ELISA 2 0 (0)
Scotophilus nux Cameroon 2015–2017‡ Luminex 6 0–0 (0–0)
Scotophilus leucogaster Guinea 2015–2017‡ Luminex 15 0–0 (0–0)
Scotophilus nigrita Guinea 2015–2017‡ Luminex 1 0–0 (0–0)
Scotophilus dinganii DRC 1995 (27) ELISA 19 0 (0)

Scotophilus sp.
1979–1980 (26)
0 (0)

Total 4–9/3,023 (0.13–0.30)

*DRC, the Democratic Republic of the Congo; IFA, immunofluorescence assay.
†For data from cited studies, the number of positive samples reported in the original study is indicated. For our results, we show the range in the number of samples simultaneously reactive with glycoprotein and nucleoprotein of Zaire Ebola virus on the basis of 4 different statistical methods used to determine cutoff values.
‡This study.

Main Article

  1. Mylne  A, Brady  OJ, Huang  Z, Pigott  DM, Golding  N, Kraemer  MU, et al. A comprehensive database of the geographic spread of past human Ebola outbreaks. Sci Data. 2014;1:140042. DOIPubMedGoogle Scholar
  2. Baize  S, Pannetier  D, Oestereich  L, Rieger  T, Koivogui  L, Magassouba  N, et al. Emergence of Zaire Ebola virus disease in Guinea. N Engl J Med. 2014;371:141825. DOIPubMedGoogle Scholar
  3. Maganga  GD, Kapetshi  J, Berthet  N, Kebela Ilunga  B, Kabange  F, Mbala Kingebeni  P, et al. Ebola virus disease in the Democratic Republic of Congo. N Engl J Med. 2014;371:208391. DOIPubMedGoogle Scholar
  4. World Health Organization. Ebola outbreak Democratic Republic of the Congo 2017. 2017 Jul 2 [cited 2018 May 3].
  5. Pigott  DM, Millear  AI, Earl  L, Morozoff  C, Han  BA, Shearer  FM, et al. Updates to the zoonotic niche map of Ebola virus disease in Africa. eLife. 2016;5:e16412. DOIPubMedGoogle Scholar
  6. Leroy  EM, Kumulungui  B, Pourrut  X, Rouquet  P, Hassanin  A, Yaba  P, et al. Fruit bats as reservoirs of Ebola virus. Nature. 2005;438:5756. DOIPubMedGoogle Scholar
  7. Leendertz  SA, Gogarten  JF, Düx  A, Calvignac-Spencer  S, Leendertz  FH. Assessing the evidence supporting fruit bats as the primary reservoirs for Ebola viruses. EcoHealth. 2016;13:1825. DOIPubMedGoogle Scholar
  8. Kamins  AO, Rowcliffe  JM, Ntiamoa-Baidu  Y, Cunningham  AA, Wood  JL, Restif  O. Characteristics and risk perceptions of Ghanaians potentially exposed to bat-borne zoonoses through bushmeat. EcoHealth. 2015;12:10420. DOIPubMedGoogle Scholar
  9. Gonzalez  JP, Pourrut  X, Leroy  E. Ebolavirus and other filoviruses. Curr Top Microbiol Immunol. 2007;315:36387. DOIPubMedGoogle Scholar
  10. Leroy  EM, Epelboin  A, Mondonge  V, Pourrut  X, Gonzalez  JP, Muyembe-Tamfum  JJ, et al. Human Ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo, 2007. Vector Borne Zoonotic Dis. 2009;9:7238. DOIPubMedGoogle Scholar
  11. Marí Saéz  A, Weiss  S, Nowak  K, Lapeyre  V, Zimmermann  F, Düx  A, et al. Investigating the zoonotic origin of the West African Ebola epidemic. EMBO Mol Med. 2015;7:1723. DOIPubMedGoogle Scholar
  12. Pourrut  X, Délicat  A, Rollin  PE, Ksiazek  TG, Gonzalez  JP, Leroy  EM. Spatial and temporal patterns of Zaire ebolavirus antibody prevalence in the possible reservoir bat species. J Infect Dis. 2007;196(Suppl 2):S17683. DOIPubMedGoogle Scholar
  13. Pourrut  X, Souris  M, Towner  JS, Rollin  PE, Nichol  ST, Gonzalez  JP, et al. Large serological survey showing cocirculation of Ebola and Marburg viruses in Gabonese bat populations, and a high seroprevalence of both viruses in Rousettus aegyptiacus. BMC Infect Dis. 2009;9:159. DOIPubMedGoogle Scholar
  14. Hayman  DT, Emmerich  P, Yu  M, Wang  LF, Suu-Ire  R, Fooks  AR, et al. Long-term survival of an urban fruit bat seropositive for Ebola and Lagos bat viruses. PLoS One. 2010;5:e11978. DOIPubMedGoogle Scholar
  15. Hayman  DT, Yu  M, Crameri  G, Wang  LF, Suu-Ire  R, Wood  JL, et al. Ebola virus antibodies in fruit bats, Ghana, West Africa. Emerg Infect Dis. 2012;18:12079. DOIPubMedGoogle Scholar
  16. Ogawa  H, Miyamoto  H, Nakayama  E, Yoshida  R, Nakamura  I, Sawa  H, et al. Seroepidemiological prevalence of multiple species of filoviruses in fruit bats (Eidolon helvum) migrating in Africa. J Infect Dis. 2015;212(Suppl 2):S1018. DOIPubMedGoogle Scholar
  17. Towner  JS, Pourrut  X, Albariño  CG, Nkogue  CN, Bird  BH, Grard  G, et al. Marburg virus infection detected in a common African bat. PLoS One. 2007;2:e764. DOIPubMedGoogle Scholar
  18. Towner  JS, Amman  BR, Sealy  TK, Carroll  SA, Comer  JA, Kemp  A, et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 2009;5:e1000536. DOIPubMedGoogle Scholar
  19. Kuzmin  IV, Niezgoda  M, Franka  R, Agwanda  B, Markotter  W, Breiman  RF, et al. Marburg virus in fruit bat, Kenya. Emerg Infect Dis. 2010;16:3524. DOIPubMedGoogle Scholar
  20. Swanepoel  R, Smit  SB, Rollin  PE, Formenty  P, Leman  PA, Kemp  A, et al.; International Scientific and Technical Committee for Marburg Hemorrhagic Fever Control in the Democratic Republic of Congo. Studies of reservoir hosts for Marburg virus. Emerg Infect Dis. 2007;13:184751. DOIPubMedGoogle Scholar
  21. Negredo  A, Palacios  G, Vázquez-Morón  S, González  F, Dopazo  H, Molero  F, et al. Discovery of an ebolavirus-like filovirus in europe. PLoS Pathog. 2011;7:e1002304. DOIPubMedGoogle Scholar
  22. Yang  XL, Zhang  YZ, Jiang  RD, Guo  H, Zhang  W, Li  B, et al. Genetically diverse filoviruses in Rousettus and Eonycteris spp. bats, China, 2009 and 2015. Emerg Infect Dis. 2017;23:4826. DOIPubMedGoogle Scholar
  23. World Health Organization. Ebola situation report - 30 March 2016. 2016 [cited 2018 May 3].
  24. Dudas  G, Carvalho  LM, Bedford  T, Tatem  AJ, Baele  G, Faria  NR, et al. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature. 2017;544:30915. DOIPubMedGoogle Scholar
  25. Pigott  DM, Deshpande  A, Letourneau  I, Morozoff  C, Reiner  RC Jr, Kraemer  MUG, et al. Local, national, and regional viral haemorrhagic fever pandemic potential in Africa: a multistage analysis. Lancet. 2017;390:266272. DOIPubMedGoogle Scholar
  26. Breman  JG, Johnson  KM, van der Groen  G, Robbins  CB, Szczeniowski  MV, Ruti  K, et al.; Ebola Virus Study Teams. 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(Suppl 1):S13947. DOIPubMedGoogle Scholar
  27. Leirs  H, Mills  JN, Krebs  JW, Childs  JE, Akaibe  D, Woollen  N, et al. Search for the Ebola virus reservoir in Kikwit, Democratic Republic of the Congo: reflections on a vertebrate collection. J Infect Dis. 1999;179(Suppl 1):S15563. DOIPubMedGoogle Scholar
  28. Ayouba  A, Touré  A, Butel  C, Keita  AK, Binetruy  F, Sow  MS, et al. Development of a sensitive and specific serological assay based on luminex technology for detection of antibodies to Zaire Ebola virus. J Clin Microbiol. 2016;55:16576. DOIPubMedGoogle Scholar
  29. Peel  AJ, McKinley  TJ, Baker  KS, Barr  JA, Crameri  G, Hayman  DT, et al. Use of cross-reactive serological assays for detecting novel pathogens in wildlife: assessing an appropriate cutoff for henipavirus assays in African bats. J Virol Methods. 2013;193:295303. DOIPubMedGoogle Scholar
  30. Gilbert  AT, Fooks  AR, Hayman  DT, Horton  DL, Müller  T, Plowright  R, et al. Deciphering serology to understand the ecology of infectious diseases in wildlife. EcoHealth. 2013;10:298313. DOIPubMedGoogle Scholar
  31. Lardeux  F, Torrico  G, Aliaga  C. Calculation of the ELISA’s cut-off based on the change-point analysis method for detection of Trypanosoma cruzi infection in Bolivian dogs in the absence of controls. Mem Inst Oswaldo Cruz. 2016;111:5014. DOIPubMedGoogle Scholar
  32. Killick  R, Eckley  IA. changepoint: an R package for changepoint analysis. J Stat Softw. 2014;58:119. DOIGoogle Scholar
  33. Hinkley  DV. Inference about the change-point in a sequence of random variables. Biometrika. 1970;57:117. DOIGoogle Scholar
  34. Laing  ED, Mendenhall  IH, Linster  M, Low  DHW, Chen  Y, Yan  L, et al. Serologic evidence of fruit bat exposure to filoviruses, Singapore, 2011–2016. Emerg Infect Dis. 2018;24:1147. DOIPubMedGoogle Scholar
  35. Cullen  AC, Frey  HC. Probabilistic techniques in exposure assessment. New York: Plenum Press; 1999. p. 81–159.
  36. Delignette-Muller  ML, Dutang  C. fitdistrplus: an R package for fitting distributions. J Stat Softw. 2015;64:134. DOIGoogle Scholar
  37. Monleau  M, Montavon  C, Laurent  C, Segondy  M, Montes  B, Delaporte  E, et al. Evaluation of different RNA extraction methods and storage conditions of dried plasma or blood spots for human immunodeficiency virus type 1 RNA quantification and PCR amplification for drug resistance testing. J Clin Microbiol. 2009;47:110718. DOIPubMedGoogle Scholar
  38. Guichet  E, Serrano  L, Laurent  C, Eymard-Duvernay  S, Kuaban  C, Vidal  L, et al. Comparison of different nucleic acid preparation methods to improve specific HIV-1 RNA isolation for viral load testing on dried blood spots. J Virol Methods. 2018;251:759. DOIPubMedGoogle Scholar
  39. Irwin  DM, Kocher  TD, Wilson  AC. Evolution of the cytochrome b gene of mammals. J Mol Evol. 1991;32:12844. DOIPubMedGoogle Scholar
  40. Kocher  TD, Thomas  WK, Meyer  A, Edwards  SV, Pääbo  S, Villablanca  FX, et al. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989;86:6196200. DOIPubMedGoogle Scholar
  41. He  B, Feng  Y, Zhang  H, Xu  L, Yang  W, Zhang  Y, et al. Filovirus RNA in fruit bats, China. Emerg Infect Dis. 2015;21:16757. DOIPubMedGoogle Scholar
  42. Han  BA, Schmidt  JP, Alexander  LW, Bowden  SE, Hayman  DT, Drake  JM. Undiscovered bat hosts of filoviruses. PLoS Negl Trop Dis. 2016;10:e0004815. DOIPubMedGoogle Scholar
  43. Rimoin  AW, Lu  K, Bramble  MS, Steffen  I, Doshi  RH, Hoff  NA, et al. Ebola virus neutralizing antibodies detectable in survivors of theYambuku, Zaire outbreak 40 years after infection. J Infect Dis. 2018;217:22331. DOIPubMedGoogle Scholar
  44. Paweska  JT, Storm  N, Grobbelaar  AA, Markotter  W, Kemp  A, Jansen van Vuren  P. Experimental inoculation of Egyptian fruit bats (Rousettus aegyptiacus) with Ebola virus. Viruses. 2016;8:29. DOIPubMedGoogle Scholar
  45. Amman  BR, Jones  ME, Sealy  TK, Uebelhoer  LS, Schuh  AJ, Bird  BH, et al. Oral shedding of Marburg virus in experimentally infected Egyptian fruit bats (Rousettus aegyptiacus). J Wildl Dis. 2015;51:11324. DOIPubMedGoogle Scholar
  46. Schuh  AJ, Amman  BR, Jones  ME, Sealy  TK, Uebelhoer  LS, Spengler  JR, et al. Modelling filovirus maintenance in nature by experimental transmission of Marburg virus between Egyptian rousette bats. Nat Commun. 2017;8:14446. DOIPubMedGoogle Scholar
  47. Jones  ME, Schuh  AJ, Amman  BR, Sealy  TK, Zaki  SR, Nichol  ST, et al. Experimental inoculation of Egyptian rousette bats (Rousettus aegyptiacus) with viruses of the Ebolavirus and Marburgvirus genera. Viruses. 2015;7:342042. DOIPubMedGoogle Scholar
  48. Swanepoel  R, Leman  PA, Burt  FJ, Zachariades  NA, Braack  LE, Ksiazek  TG, et al. Experimental inoculation of plants and animals with Ebola virus. Emerg Infect Dis. 1996;2:3215. DOIPubMedGoogle Scholar
  49. Storm  N, Jansen Van Vuren  P, Markotter  W, Paweska  JT. Antibody responses to Marburg virus in Egyptian rousette bats and their role in protection against infection. Viruses. 2018;10:73. DOIPubMedGoogle Scholar

Main Article

1These first authors contributed equally to this article.

2These senior authors contributed equally to this article.

Page created: November 20, 2018
Page updated: November 20, 2018
Page reviewed: November 20, 2018
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.