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PLoS Pathogens. Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection
[Source: PLoS Pathogens, full text: (LINK). Abstract, edited.]
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Seasonal Pulses of Marburg Virus Circulation in Juvenile Rousettus aegyptiacus Bats Coincide with Periods of Increased Risk of Human Infection
Brian R. Amman<SUP>1</SUP>, Serena A. Carroll<SUP>1</SUP>, Zachary D. Reed<SUP>1</SUP>, Tara K. Sealy<SUP>1</SUP>, Stephen Balinandi<SUP>1</SUP>, Robert Swanepoel<SUP>2</SUP><SUP>?a</SUP>, Alan Kemp<SUP>2</SUP>, Bobbie Rae Erickson<SUP>1</SUP>, James A. Comer<SUP>1</SUP>, Shelley Campbell<SUP>1</SUP>, Deborah L. Cannon<SUP>1</SUP>, Marina L. Khristova<SUP>3</SUP>, Patrick Atimnedi<SUP>4</SUP>, Christopher D. Paddock<SUP>5</SUP>, Rebekah J. Kent Crockett<SUP>6</SUP>, Timothy D. Flietstra<SUP>1</SUP>, Kelly L. Warfield<SUP>7</SUP>, Robert Unfer<SUP>7</SUP>, Edward Katongole-Mbidde<SUP>8</SUP>, Robert Downing<SUP>9</SUP>, Jordan W. Tappero<SUP>9</SUP>, Sherif R. Zaki<SUP>5</SUP>, Pierre E. Rollin<SUP>1</SUP>, Thomas G. Ksiazek<SUP>1</SUP><SUP>?b</SUP>, Stuart T. Nichol<SUP>1</SUP>, Jonathan S. Towner<SUP>1</SUP><SUP>*</SUP>
<SUP></SUP>
1 Viral Special Pathogens Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 2 National Institute of Communicable Diseases, Special Pathogens Unit, Johannesburg, South Africa, 3 Biotechnology Core Facility Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 4 Uganda Wildlife Authority, Kampala, Republic of Uganda, 5 Infectious Disease Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 6 Division of Vector-borne Diseases, Arbovirus Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 7 Integrated BioTherapeutics, Gaithersburg, Maryland, United States of America, 8 Uganda Virus Research Institute, Entebbe, Republic of Uganda, 9 Global AIDS Program, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
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.
Author Summary
Marburg virus, like its close relative Ebola virus, can cause large outbreaks of hemorrhagic fever with case fatalities nearing 90%. For decades the identity of the natural reservoir was unknown. However, in 2007 Marburg viruses were isolated directly from Egyptian fruit bats (Rousettus aegyptiacus) that inhabited a Ugandan gold mine where miners were previously infected. Soon after, two tourists became infected with Marburg virus after visiting nearby Python Cave, a popular attraction in Queen Elizabeth National Park, Uganda. This cave also contained R. aegyptiacus bats (~40,000 animals). These events prompted a long-term investigation of Python Cave to determine if, 1) R. aegyptiacus in the cave carried infectious Marburg virus genetically similar to that found in the tourists, and 2) what ecological factors might influence virus spillover to humans. In the study, we found that, 1) approximately 2.5% of the bat colony is actively infected at any one time and that virus isolates from bats are genetically similar to those from infected tourists, and 2) specific age groups of bats (juveniles~six months of age) are particularly likely to be infected at specific times of the year that roughly coincide with historical dates of Marburg virus spillover into humans.
Citation: Amman BR, Carroll SA, Reed ZD, Sealy TK, Balinandi S, 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(10): e1002877. doi:10.1371/journal.ppat.1002877
Editor: Yoshihiro Kawaoka, University of Wisconsin-Madison, United States of America
Received: April 19, 2012; Accepted: July 5, 2012; Published: October 4, 2012
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: Funding was received from the Department of Health and Human Services. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
Competing interests: The authors have declared that no competing interests exist.
* E-mail: jit8@cdc.gov
?a Current address: Zoonoses Research Unit, Department of Medical Virology, University of Pretoria, Pretoria, South Africa
?b Current address: Galveston National Lab, Department of Pathology, University of Texas Medical Branch, Galveston, Texas, United States of America
-Brian R. Amman<SUP>1</SUP>, Serena A. Carroll<SUP>1</SUP>, Zachary D. Reed<SUP>1</SUP>, Tara K. Sealy<SUP>1</SUP>, Stephen Balinandi<SUP>1</SUP>, Robert Swanepoel<SUP>2</SUP><SUP>?a</SUP>, Alan Kemp<SUP>2</SUP>, Bobbie Rae Erickson<SUP>1</SUP>, James A. Comer<SUP>1</SUP>, Shelley Campbell<SUP>1</SUP>, Deborah L. Cannon<SUP>1</SUP>, Marina L. Khristova<SUP>3</SUP>, Patrick Atimnedi<SUP>4</SUP>, Christopher D. Paddock<SUP>5</SUP>, Rebekah J. Kent Crockett<SUP>6</SUP>, Timothy D. Flietstra<SUP>1</SUP>, Kelly L. Warfield<SUP>7</SUP>, Robert Unfer<SUP>7</SUP>, Edward Katongole-Mbidde<SUP>8</SUP>, Robert Downing<SUP>9</SUP>, Jordan W. Tappero<SUP>9</SUP>, Sherif R. Zaki<SUP>5</SUP>, Pierre E. Rollin<SUP>1</SUP>, Thomas G. Ksiazek<SUP>1</SUP><SUP>?b</SUP>, Stuart T. Nichol<SUP>1</SUP>, Jonathan S. Towner<SUP>1</SUP><SUP>*</SUP>
<SUP></SUP>
1 Viral Special Pathogens Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 2 National Institute of Communicable Diseases, Special Pathogens Unit, Johannesburg, South Africa, 3 Biotechnology Core Facility Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 4 Uganda Wildlife Authority, Kampala, Republic of Uganda, 5 Infectious Disease Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 6 Division of Vector-borne Diseases, Arbovirus Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 7 Integrated BioTherapeutics, Gaithersburg, Maryland, United States of America, 8 Uganda Virus Research Institute, Entebbe, Republic of Uganda, 9 Global AIDS Program, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
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.
Author Summary
Marburg virus, like its close relative Ebola virus, can cause large outbreaks of hemorrhagic fever with case fatalities nearing 90%. For decades the identity of the natural reservoir was unknown. However, in 2007 Marburg viruses were isolated directly from Egyptian fruit bats (Rousettus aegyptiacus) that inhabited a Ugandan gold mine where miners were previously infected. Soon after, two tourists became infected with Marburg virus after visiting nearby Python Cave, a popular attraction in Queen Elizabeth National Park, Uganda. This cave also contained R. aegyptiacus bats (~40,000 animals). These events prompted a long-term investigation of Python Cave to determine if, 1) R. aegyptiacus in the cave carried infectious Marburg virus genetically similar to that found in the tourists, and 2) what ecological factors might influence virus spillover to humans. In the study, we found that, 1) approximately 2.5% of the bat colony is actively infected at any one time and that virus isolates from bats are genetically similar to those from infected tourists, and 2) specific age groups of bats (juveniles~six months of age) are particularly likely to be infected at specific times of the year that roughly coincide with historical dates of Marburg virus spillover into humans.
Citation: Amman BR, Carroll SA, Reed ZD, Sealy TK, Balinandi S, 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(10): e1002877. doi:10.1371/journal.ppat.1002877
Editor: Yoshihiro Kawaoka, University of Wisconsin-Madison, United States of America
Received: April 19, 2012; Accepted: July 5, 2012; Published: October 4, 2012
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: Funding was received from the Department of Health and Human Services. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
Competing interests: The authors have declared that no competing interests exist.
* E-mail: jit8@cdc.gov
?a Current address: Zoonoses Research Unit, Department of Medical Virology, University of Pretoria, Pretoria, South Africa
?b Current address: Galveston National Lab, Department of Pathology, University of Texas Medical Branch, Galveston, Texas, United States of America
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