CoChat
Sign Up
Cited by 453Viral Infections and Outbreaks ResearchViral Infections and VectorsVirology and Viral Diseases

The DOI matches its Crossref record; 31 of the 32 references it cites were found in a registry or an index.

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

Open access
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 G., Nichol, Stuart T., Towner, Jonathan S.·2012·PLoS Pathogens
DOI 10.1371/journal.ppat.1002877PMC PMC3464226
Open this paper in CoChat — free accountOpen PDF

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.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.ppat.1002877

Cites

31 of 31 references verified0 citation errors · 0 not checkable

Statistics

Figures

Figure 1 Bayesian phylogeny of full length Marburg genome. Phylogenetic results from a Bayesian analysis on full-length Marburg virus genome sequences from 12 Marburg bat isolates, 3 recent Ugandan human isolates from the two Kitaka miners (01Uga 2007, 02Uga 2007), and the Dutch tourist (01Uga/Net 2008), as well as 45 historical isolates (Table S2 for GenBank accession numbers). Posterior probabilities above .50 are shown above the appropriate nodes. Marburg virus sequences from human cases from Kitaka mine (Uganda 2007) in are in orange, sequences from human cases from Python Cave (2008 Uganda) are in blue, sequences from Kitaka Mine bats are in red, and sequences from Python Cave bats are in green.
Figure 1 Bayesian phylogeny of full length Marburg genome. Phylogenetic results from a Bayesian analysis on full-length Marburg virus genome sequences from 12 Marburg bat isolates, 3 recent Ugandan human isolates from the two Kitaka miners (01Uga 2007, 02Uga 2007), and the Dutch tourist (01Uga/Net 2008), as well as 45 historical isolates (Table S2 for GenBank accession numbers). Posterior probabilities above .50 are shown above the appropriate nodes. Marburg virus sequences from human cases from Kitaka mine (Uganda 2007) in are in orange, sequences from human cases from Python Cave (2008 Uganda) are in blue, sequences from Kitaka Mine bats are in red, and sequences from Python Cave bats are in green.CC0 · PubMed Central
Figure 2 Bayesian phylogeny of Marburg NP and VP35 genes. Phylogenetic results from a Bayesian analysis on concatenated NP and VP35 sequence fragments obtained from bat specimens, historical isolates (45), and the recent Ugandan human samples (01Uga 2007, 02Uga 2007, 01Uga/Net 2008) as well as the American tourist (01Uga/USA 2007), for which there was no isolate, only partial Marburg virus sequence (Table S2 for GenBank accession numbers). Sequences 846QBat_Uga_2009, 849QBat_Uga_2009, 1079QBat_Uga_2009, 1261QBat_Uga_2009, 1328QBat_Uga_2009, and 1511QBat_Uga_2009 represent NP only. Posterior probabilities above .50 are shown above the appropriate nodes. Marburg virus sequences from human cases from Kitaka mine (Uganda 2007) in are in orange, sequences from human cases from Python Cave (2008 Uganda) are in blue, sequences from Kitaka Mine bats are in red, and sequences from Python Cave bats are in green.
Figure 2 Bayesian phylogeny of Marburg NP and VP35 genes. Phylogenetic results from a Bayesian analysis on concatenated NP and VP35 sequence fragments obtained from bat specimens, historical isolates (45), and the recent Ugandan human samples (01Uga 2007, 02Uga 2007, 01Uga/Net 2008) as well as the American tourist (01Uga/USA 2007), for which there was no isolate, only partial Marburg virus sequence (Table S2 for GenBank accession numbers). Sequences 846QBat_Uga_2009, 849QBat_Uga_2009, 1079QBat_Uga_2009, 1261QBat_Uga_2009, 1328QBat_Uga_2009, and 1511QBat_Uga_2009 represent NP only. Posterior probabilities above .50 are shown above the appropriate nodes. Marburg virus sequences from human cases from Kitaka mine (Uganda 2007) in are in orange, sequences from human cases from Python Cave (2008 Uganda) are in blue, sequences from Kitaka Mine bats are in red, and sequences from Python Cave bats are in green.CC0 · PubMed Central
Figure 3 Percent active infection among older and younger juvenile bats and adults. (A) Histogram showing the percent of juvenile bats from Kitaka Mine and Python Cave actively infected (Q-RT-PCR+) with Marburg virus during breeding and birthing seasons. (B) Histogram of the percent of adult bats from Kitaka Mine and Python Cave actively infected (Q-RT-PCR+) with Marburg virus during breeding and birthing seasons.
Figure 3 Percent active infection among older and younger juvenile bats and adults. (A) Histogram showing the percent of juvenile bats from Kitaka Mine and Python Cave actively infected (Q-RT-PCR+) with Marburg virus during breeding and birthing seasons. (B) Histogram of the percent of adult bats from Kitaka Mine and Python Cave actively infected (Q-RT-PCR+) with Marburg virus during breeding and birthing seasons.CC0 · PubMed Central
Figure 4 Increases in seasonal risk to human health. Historical spillover events (colored circles on X axis) compared to predicted seasonal levels of PCR+ juveniles (sinusoidal curve). The amplitude of the curve is based on average PCR+ juveniles experimentally determined during birthing (12.4%) and breeding (2.7%) seasons. Large light green vertical rectangles represent the proposed approximate three month seasons of increased risk based on the average level of juvenile infected bats at peak times of encompassing birthing (February and August) and breeding (May and November). Large gray arrows depict the twice yearly influx of newly autonomous juvenile bats born in the prior birthing season. The influx begins at the approximate time of the juvenile's independence from their mothers.
Figure 4 Increases in seasonal risk to human health. Historical spillover events (colored circles on X axis) compared to predicted seasonal levels of PCR+ juveniles (sinusoidal curve). The amplitude of the curve is based on average PCR+ juveniles experimentally determined during birthing (12.4%) and breeding (2.7%) seasons. Large light green vertical rectangles represent the proposed approximate three month seasons of increased risk based on the average level of juvenile infected bats at peak times of encompassing birthing (February and August) and breeding (May and November). Large gray arrows depict the twice yearly influx of newly autonomous juvenile bats born in the prior birthing season. The influx begins at the approximate time of the juvenile's independence from their mothers.CC0 · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 4

  1. [3]Wilson, D E. and Reeder, D M. (2005) Mammal species of the world. Baltimore: Johns Hopkins University Press. 2142 p.
  2. [16]Zaki SR, Shieh WJ, Greer PW, Goldsmith CS, Ferebee T, et al (1999) A novel immunohistochemical assay for the detection of Ebola virus in skin: implications for diagnosis, spread, and surveillance of Ebola hemorrhagic fever. Commission de Lutte contre les Epidemies a Kikwit. J Infect Dis 179 Suppl 1: S36– S47. 9988163
  3. [17]Martini GA, Schmidt HA (1968) [Spermatogenic transmission of the “Marburg virus”. (Causes of “Marburg simian disease”)]. Klin Wochenschr 46: 398– 400. 4971902
  4. [23]Towner JS, Amman BR, Nichol ST (2011) Significant zoonotic diseases identified in bats: Filoviruses. In: Investigating the Role of Bats in Emerging Zoonoses. Newman SH, Field HE, de Jong CE, Epstein JH, editors. Rome: Food and Agriculture Organisation of the United Nations. pp. 123–135.

Cited by

Sorted by citations

See all 453

Related

See all

Metadata

Authors
Amman, B. R., Carroll, S. A., Reed, Z. D., Sealy, T. K., Balinandi, S., Swanepoel, R., Kemp, A., Erickson, B. R., Comer, J. A., Campbell, S., Cannon, D. L., Khristova, M. L., Atimnedi, P., Paddock, C. D., Kent Crockett, R. J., Flietstra, T. D., Warfield, K. L., Unfer, R., Katongole-Mbidde, E., Downing, R., Tappero, J. W., Zaki, S. R., Rollin, P. E., Ksiazek, T. G., Nichol, S. T., & Towner, J. S.
Affiliations
  • Centers for Disease Control and Prevention (US)
  • National Institute for Communicable Diseases (ZA)
  • Uganda Wildlife Authority (UG)
  • Integrated BioTherapeutics (United States) (US)
Corresponding author
Towner, Jonathan S.
ORCID
Venue
PLoS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2012-10-04
Volume
8
Issue
10
Pages
e1002877
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
DOI
10.1371/journal.ppat.1002877
PMC
PMC3464226
OpenAlex
W2131851182
Cited by
453
References
32
Citations by year
2026: 36 · 2025: 41 · 2024: 34 · 2023: 46 · 2022: 40 · 2021: 25 · 2020: 36 · 2019: 36 · 2018: 34 · 2017: 32 · 2016: 31 · 2015: 31 · 2014: 17 · 2013: 11 · 2012: 3
FWCI
13.75
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Pathogens (publishedVersion, public-domain)
  • Europe PMC (PubMed Central) (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • UpSpace Institutional Repository (University of Pretoria) (submittedVersion, cc-by)
Funders
  • U.S. Department of Health and Human Services
  • Centers for Disease Control and Prevention
Topics
  • Health Sciences › Medicine › Infectious Diseases › Viral Infections and Outbreaks Research
  • Health Sciences › Medicine › Infectious Diseases › Viral Infections and Vectors
  • Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
Keywords
Marburg virus, Rousettus aegyptiacus, Pteropodidae, bat reservoir hosts, juvenile bats, Marburg hemorrhagic fever, horizontal transmission, metapopulation, risk mitigation strategies
MeSH terms
Animals, Base Sequence, Chiroptera, Disease Reservoirs, Female, Humans, Male, Marburg Virus Disease, Nuclear Proteins, Phylogeny, Retrospective Studies, RNA, Viral, Seasons, Uganda, Sequence Analysis, RNA, Marburgvirus, Viral Regulatory and Accessory Proteins, Caves

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review