Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection

Brian R. Amman, Serena A. Carroll, Zachary D. Reed, Tara K. Sealy, Stephen Balinandi, Robert Swanepoel, Alan Kemp, Bobbie Rae Erickson, James A. Comer, Shelley Campbell, Deborah L. Cannon, Marina L. Khristova, Patrick Atimnedi, Christopher D. Paddock, Rebekah J. Kent Crockett, Timothy D. Flietstra, Kelly L. Warfield, Robert Unfer, Edward Katongole-Mbidde, Robert Downing & 6 others Jordan W. Tappero, Sherif R. Zaki, Pierre E. Rollin, Thomas Ksiazek, Stuart T. Nichol, Jonathan S. Towner

Research output: Contribution to journalArticle

145 Citations (Scopus)

Abstract

Marburg virus (family Filoviridae) causes sporadic outbreaks of severe hemorrhagic disease in sub-Saharan Africa. Bats have been implicated as likely natural reservoir hosts based most recently on an investigation of cases among miners infected in 2007 at the Kitaka mine, Uganda, which contained a large population of Marburg virus-infected Rousettus aegyptiacus fruit bats. Described here is an ecologic investigation of Python Cave, Uganda, where an American and a Dutch tourist acquired Marburg virus infection in December 2007 and July 2008. More than 40,000 R. aegyptiacus were found in the cave and were the sole bat species present. Between August 2008 and November 2009, 1,622 bats were captured and tested for Marburg virus. Q-RT-PCR analysis of bat liver/spleen tissues indicated ~2.5% of the bats were actively infected, seven of which yielded Marburg virus isolates. Moreover, Q-RT-PCR-positive lung, kidney, colon and reproductive tissues were found, consistent with potential for oral, urine, fecal or sexual transmission. The combined data for R. aegyptiacus tested from Python Cave and Kitaka mine indicate low level horizontal transmission throughout the year. However, Q-RT-PCR data show distinct pulses of virus infection in older juvenile bats (~six months of age) that temporarily coincide with the peak twice-yearly birthing seasons. Retrospective analysis of historical human infections suspected to have been the result of discrete spillover events directly from nature found 83% (54/65) events occurred during these seasonal pulses in virus circulation, perhaps demonstrating periods of increased risk of human infection. The discovery of two tags at Python Cave from bats marked at Kitaka mine, together with the close genetic linkages evident between viruses detected in geographically distant locations, are consistent with R. aegyptiacus bats existing as a large meta-population with associated virus circulation over broad geographic ranges. These findings provide a basis for developing Marburg hemorrhagic fever risk reduction strategies.

Original languageEnglish (US)
Article numbere1002877
JournalPLoS Pathogens
Volume8
Issue number10
DOIs
StatePublished - Oct 2012

Fingerprint

Marburgvirus
Infection
Boidae
Uganda
Virus Diseases
Polymerase Chain Reaction
Filoviridae
Marburg Virus Disease
Viruses
Satellite Viruses
Genetic Linkage
Africa South of the Sahara
Risk Reduction Behavior
Population
Disease Outbreaks
Fruit
Colon

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

Cite this

Amman, B. R., Carroll, S. A., Reed, Z. D., Sealy, T. K., Balinandi, S., Swanepoel, R., ... Towner, J. S. (2012). Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection. PLoS Pathogens, 8(10), [e1002877]. https://doi.org/10.1371/journal.ppat.1002877

Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection. / Amman, Brian R.; Carroll, Serena A.; Reed, Zachary D.; Sealy, Tara K.; Balinandi, Stephen; Swanepoel, Robert; Kemp, Alan; Erickson, Bobbie Rae; Comer, James A.; Campbell, Shelley; Cannon, Deborah L.; Khristova, Marina L.; Atimnedi, Patrick; Paddock, Christopher D.; Kent Crockett, Rebekah J.; Flietstra, Timothy D.; Warfield, Kelly L.; Unfer, Robert; Katongole-Mbidde, Edward; Downing, Robert; Tappero, Jordan W.; Zaki, Sherif R.; Rollin, Pierre E.; Ksiazek, Thomas; Nichol, Stuart T.; Towner, Jonathan S.

In: PLoS Pathogens, Vol. 8, No. 10, e1002877, 10.2012.

Research output: Contribution to journalArticle

Amman, BR, Carroll, SA, Reed, ZD, Sealy, TK, Balinandi, S, Swanepoel, R, Kemp, A, Erickson, BR, Comer, JA, Campbell, S, Cannon, DL, Khristova, ML, Atimnedi, P, Paddock, CD, Kent Crockett, RJ, Flietstra, TD, Warfield, KL, Unfer, R, Katongole-Mbidde, E, Downing, R, Tappero, JW, Zaki, SR, Rollin, PE, Ksiazek, T, Nichol, ST & Towner, JS 2012, 'Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection', PLoS Pathogens, vol. 8, no. 10, e1002877. https://doi.org/10.1371/journal.ppat.1002877
Amman, Brian R. ; Carroll, Serena A. ; Reed, Zachary D. ; Sealy, Tara K. ; Balinandi, Stephen ; Swanepoel, Robert ; Kemp, Alan ; Erickson, Bobbie Rae ; Comer, James A. ; Campbell, Shelley ; Cannon, Deborah L. ; Khristova, Marina L. ; Atimnedi, Patrick ; Paddock, Christopher D. ; Kent Crockett, Rebekah J. ; Flietstra, Timothy D. ; Warfield, Kelly L. ; Unfer, Robert ; Katongole-Mbidde, Edward ; Downing, Robert ; Tappero, Jordan W. ; Zaki, Sherif R. ; Rollin, Pierre E. ; Ksiazek, Thomas ; Nichol, Stuart T. ; Towner, Jonathan S. / Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection. In: PLoS Pathogens. 2012 ; Vol. 8, No. 10.
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abstract = "Marburg virus (family Filoviridae) causes sporadic outbreaks of severe hemorrhagic disease in sub-Saharan Africa. Bats have been implicated as likely natural reservoir hosts based most recently on an investigation of cases among miners infected in 2007 at the Kitaka mine, Uganda, which contained a large population of Marburg virus-infected Rousettus aegyptiacus fruit bats. Described here is an ecologic investigation of Python Cave, Uganda, where an American and a Dutch tourist acquired Marburg virus infection in December 2007 and July 2008. More than 40,000 R. aegyptiacus were found in the cave and were the sole bat species present. Between August 2008 and November 2009, 1,622 bats were captured and tested for Marburg virus. Q-RT-PCR analysis of bat liver/spleen tissues indicated ~2.5{\%} of the bats were actively infected, seven of which yielded Marburg virus isolates. Moreover, Q-RT-PCR-positive lung, kidney, colon and reproductive tissues were found, consistent with potential for oral, urine, fecal or sexual transmission. The combined data for R. aegyptiacus tested from Python Cave and Kitaka mine indicate low level horizontal transmission throughout the year. However, Q-RT-PCR data show distinct pulses of virus infection in older juvenile bats (~six months of age) that temporarily coincide with the peak twice-yearly birthing seasons. Retrospective analysis of historical human infections suspected to have been the result of discrete spillover events directly from nature found 83{\%} (54/65) events occurred during these seasonal pulses in virus circulation, perhaps demonstrating periods of increased risk of human infection. The discovery of two tags at Python Cave from bats marked at Kitaka mine, together with the close genetic linkages evident between viruses detected in geographically distant locations, are consistent with R. aegyptiacus bats existing as a large meta-population with associated virus circulation over broad geographic ranges. These findings provide a basis for developing Marburg hemorrhagic fever risk reduction strategies.",
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AU - Warfield, Kelly L.

AU - Unfer, Robert

AU - Katongole-Mbidde, Edward

AU - Downing, Robert

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