Suspected Exposure to Filoviruses Among People Contacting Wildlife in Southwestern Uganda.

Tierra Smiley Evans¹ Leonard Tutaryebwa² Kirsten V Gilardi¹ Peter A Barry³ Andrea Marzi⁴ Meghan Eberhardt³ Benard Ssebide⁵ Michael R Cranfield⁵ Obed Mugisha² Emmanuel Mugisha² Scott Kellermann⁶ Jonna A K Mazet¹ Christine K Johnson¹

Affiliations 6 institutions

One Health Institute, School of Veterinary Medicine.
Bwindi Community Hospital, Buhoma, Uganda.
Center for Comparative Medicine, Department of Pathology and Laboratory Medicine, University of California, Davis.
Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana.
Gorilla Doctors, Mountain Gorilla Veterinary Project, Inc., Kampala, Uganda.
University of San Francisco, California.

PMID29924324 DOI10.1093/infdis/jiy251 Year2018 Journal The Journal of infectious diseases J Infect Dis Languageeng Statusppublish

Abstract

Human and filovirus host interactions remain poorly understood in areas where Ebola hemorrhagic fever outbreaks are likely to occur. In the Bwindi region of Uganda, a hot spot of mammalian biodiversity in Africa, human livelihoods are intimately connected with wildlife, creating potential for exposure to filoviruses. We tested samples from 331 febrile patients presenting to healthcare facilities near Bwindi Impenetrable Forest, Uganda, by polymerase chain reaction (PCR) analysis and Western blot, using recombinant glycoprotein antigens for Ebola virus (EBOV), Sudan virus (SUDV), Bundibugyo virus (BDBV), and Marburg virus. Behavioral data on contact with wildlife were collected to examine risk factors for filovirus seropositivity. All patients were negative for active filovirus infection, by PCR analysis. However, patients were seroreactive to SUDV (4.7%), EBOV (5.3%), and BDBV (8.9%), indicating previous exposure. Touching duikers was the most significant risk factor associated with EBOV seropositivity, while hunting primates and touching and/or eating cane rats were significant risk factors for SUDV seropositivity. People in southwestern Uganda have suspected previous exposure to filoviruses, particularly those with a history of wildlife contact. Circulation of filoviruses in wild animals and subsequent spillover into humans could be more common than previously reported.

Supporting text Virus Host Location

Adolescent 34 Adult 71 Aged 31 Animals 1948 Animals, Wild 187 Antigens, Viral 49 Child 42 Child, Preschool 37 Female 289 Filoviridae 9 Filoviridae Infections 5 Glycoproteins 23 Humans 1440 Infant 26 Infant, Newborn 4 Male 224 Middle Aged 60 Uganda 10 Young Adult 26

Evidence records

8 total

Zoonotic Surveillance

8 records · 3 evidence types

Evidence type Viral Detection

1 records

OVE3022 Viral Detection

Key finding

PCR testing of 331 febrile patients near Bwindi Impenetrable Forest, Uganda showed no active infection with Ebola virus, Sudan virus, Bundibugyo virus, or Marburg virus.

Virus

Host

Location

Supporting text

We tested samples from 331 febrile patients presenting to healthcare facilities near Bwindi Impenetrable Forest, Uganda, by polymerase chain reaction (PCR) analysis and Western blot, using recombinant glycoprotein antigens for Ebola virus (EBOV), Sudan virus (SUDV), Bundibugyo virus (BDBV), and Marburg virus. All patients were negative for active filovirus infection, by PCR analysis.

Method: polymerase chain reaction (PCR) analysis
Sample type: human samples
Geographic raw: Bwindi Impenetrable Forest, Uganda

Evidence type Serological Evidence

4 records

OVE3023 Serological Evidence

Key finding

Febrile patients in the Bwindi region of Uganda showed 4.7% seroreactivity to Sudan virus, indicating prior exposure rather than active infection.

Virus

Host

Location

Supporting text

Patients were seroreactive to SUDV (4.7%), indicating previous exposure.

Method: Western blot using recombinant glycoprotein antigens
Sample type: serum samples

OVE3024 Serological Evidence

Key finding

Febrile patients in the Bwindi region of Uganda showed 5.3% seroreactivity to Ebola virus, consistent with previous exposure.

Virus

Host

Location

Supporting text

Patients were seroreactive to EBOV (5.3%), indicating previous exposure.

Method: Western blot using recombinant glycoprotein antigens
Sample type: serum samples

OVE3025 Serological Evidence

Key finding

Febrile patients in the Bwindi region of Uganda showed 8.9% seroreactivity to Bundibugyo virus, suggesting previous exposure.

Virus

Host

Location

Supporting text

Patients were seroreactive to BDBV (8.9%), indicating previous exposure.

Method: Western blot using recombinant glycoprotein antigens
Sample type: serum samples

OVE3029 Serological Evidence

Key finding

Serological reactivity among people contacting wildlife in southwestern Uganda indicates animal-to-human spillover exposure to multiple filoviruses.

Virus

Host

Location

Supporting text

People in southwestern Uganda have suspected previous exposure to filoviruses, particularly those with a history of wildlife contact. Circulation of filoviruses in wild animals and subsequent spillover into humans could be more common than previously reported.

Method: PCR analysis | Western blot | recombinant glycoprotein antigen assay | behavioral risk factor survey

Evidence type Reservoir Ecology

3 records

OVE3026 Reservoir Ecology

Key finding

Touching duikers in the Bwindi region of Uganda was significantly associated with human Ebola virus seropositivity.

Virus

Host

Location

Supporting text

In the Bwindi region of Uganda, a hot spot of mammalian biodiversity in Africa, human livelihoods are intimately connected with wildlife, creating potential for exposure to filoviruses. Touching duikers was the most significant risk factor associated with EBOV seropositivity.

Method: behavioral risk factor analysis | serological testing (Western blot using recombinant glycoprotein antigens)
Sample type: human sera
Geographic raw: Bwindi region of Uganda
Country inferred: UGA

OVE3027 Reservoir Ecology

Key finding

Hunting primates in the Bwindi region of Uganda was significantly associated with human Sudan virus seropositivity.

Virus

Host

Location

Supporting text

In the Bwindi region of Uganda, a hot spot of mammalian biodiversity in Africa, human livelihoods are intimately connected with wildlife, creating potential for exposure to filoviruses. Hunting primates was a significant risk factor for SUDV seropositivity.

Method: behavioral risk factor analysis | serological testing (Western blot using recombinant glycoprotein antigens)
Sample type: human sera
Geographic raw: Bwindi region of Uganda
Country inferred: UGA

OVE3028 Reservoir Ecology

Key finding

Touching or eating cane rats in the Bwindi region of Uganda was significantly associated with human Sudan virus seropositivity.

Virus

Host

Location

Supporting text

In the Bwindi region of Uganda, a hot spot of mammalian biodiversity in Africa, human livelihoods are intimately connected with wildlife, creating potential for exposure to filoviruses. Touching and/or eating cane rats were significant risk factors for SUDV seropositivity.

Method: behavioral risk factor analysis | serological testing (Western blot using recombinant glycoprotein antigens)
Sample type: human sera
Geographic raw: Bwindi region of Uganda
Country inferred: UGA

References

48 references

Reference network

Force-directed citation graph. OmniVira-indexed references are prioritized and recursively expanded up to three steps.

46 nodes · 48 links

Drag nodes to explore citation neighborhoods


-	2014 Ebola outbreak in West Africa	Centers for Disease Control. 2014 Ebola	2017
PMID 23327370	Ebola virus outbreaks in Africa: past and present. Onderstepoort J Vet Res 2012; 79:451	Muyembe-Tamfum	2012
PMID 25786916	Seroepidemiological prevalence of multiple species of filoviruses in fruit bats ( Eidolon helvum ) migrating in Africa	Ogawa	2015
PMID 19649327	Isolation of genetically diverse Marburg viruses from Egyptian fruit bats	Towner	2009
PMID 16319873	Fruit bats as reservoirs of Ebola virus	Leroy	2005
PMID 16943403	; International Scientific and Technical Committee for Marburg Hemorrhagic Fever Control in the Democratic Republic of the Congo Marburg hemorrhagic fever associated with multiple genetic lineages of virus	Bausch	2006
PMID 21987753	Outbreak of marburg hemorrhagic fever among miners in Kamwenge and Ibanda districts, Uganda, 2007	Adjemian	2011
PMID 19323614	Human Ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo, 2007. Vector Borne Zoonotic Dis 2009; 9:723–8	Leroy	2009
PMID 23711383	Genomic analysis of filoviruses associated with four viral hemorrhagic fever outbreaks in Uganda and the Democratic Republic of the Congo in 2012. Virology 2013; 442:97–100	Albarino	2013
PMID 18258034	; International Scientific and Technical Committee for Marburg Hemorrhagic Fever Control in the Democratic Republic of Congo Studies of reservoir hosts for Marburg virus	Swanepoel	2007
PMID 7746057	Isolation and partial characterisation of a new strain of Ebola virus	Le Guenno	1995
PMID 9988167	Ebola hemorrhagic fever outbreaks in Gabon, 1994–1997: Epidemiologic and health control issues	Georges	1999
PMID 14726594	Multiple Ebola virus transmission events and rapid decline of central African wildlife	Leroy	2004
PMID 9988175	Ebola virus outbreak among wild chimpanzees living in a rain forest of Cote d’Ivoire	Formenty	1999
-	Ebola and the decline of gorilla ( Gorilla gorilla ) and chimpanzee ( Pan troglodytes ) populations in Minkebe Forest, north-eastern Gabon. Oryx 2003; 37:437–43	Huijbregts	2003
-	Ebola in great apes—current knowledge, possibilities for vaccination, and implications for conservation and human health. Mammal Review 2017; 47:98–111	Leendertz	2017
PMID 17010400	Morbidity and mortality of wild animals in relation to outbreaks of Ebola haemorrhagic fever in Gabon, 1994–2003. Trans R Soc Trop Med Hyg 2007; 101:64–78	Lahm	2007
PMID 10580275	Identification of Ebola virus sequences present as RNA or DNA in organs of terrestrial small mammals of the Central African Republic. Microbes Infect 1999; 1:1193–201	Morvan	1999
PMID 19590002	Discovery of swine as a host for the Reston ebolavirus	Barrette	2009
PMID 15757552	Ebola virus antibody prevalence in dogs and human risk	Allela	2005
PMID 15752448	Wild animal mortality monitoring and human Ebola outbreaks, Gabon and Republic of Congo, 2001–2003	Rouquet	2005
PMID 10717539	Ebola and Marburg virus antibody prevalence in selected populations of the Central African Republic. Microbes Infect 2000; 2:39–44	Gonzalez	2000
PMID 9988172	Prevalence of IgG antibodies to Ebola virus in individuals during an Ebola outbreak, Democratic Republic of the Congo, 1995	Busico	1999
-	Primates of western Uganda	Newton-Fisher	2010
PMID 17079496	Rapid molecular strategy for filovirus detection and characterization	Zhai	2007
PMID 27455307	Inactivation of RNA viruses by gamma irradiation: a study on mitigating factors	Hume	2016
PMID 21987751	Management of accidental exposure to Ebola virus in the biosafety level 4 laboratory, Hamburg, Germany	Gunther	2011
PMID 21987745	Single immunization with a monovalent vesicular stomatitis virus-based vaccine protects nonhuman primates against heterologous challenge with Bundibugyo ebolavirus	Falzarano	2011
-	Applied logistic regression. New York: John Wiley and Sons, 2013	Hosmer	2013
PMID 24914678	ForceAtlas2, a continuous graph layout algorithm for handy network visualization designed for the Gephi software	Jacomy	2014
PMID 22931687	Reemerging Sudan Ebola virus disease in Uganda, 2011	Shoemaker	2012
PMID 12460399	An outbreak of Ebola in Uganda. Trop Med Int Health 2002; 7:1068–75	Okware	2002
-	The reemergence of Ebola hemorrhagic fever, Democratic Republic of the Congo, 1995	Khan	1999
PMID 19751577	Response to imported case of Marburg hemorrhagic fever, the Netherland	Timen	2009
PMID 20019654	Imported case of Marburg hemorrhagic fever - Colorado, 2008	Centers for Disease Control and Preventi	2009
PMID 1579085	Evidence for occurrence of filovirus antibodies in humans and imported monkeys: do subclinical filovirus infections occur worldwide?Med Microbiol Immunol 1992; 181:43–55	Becker	1992
PMID 10881895	Human asymptomatic Ebola infection and strong inflammatory response	Leroy	2000
PMID 27846221	Minimally symptomatic infection in an Ebola ‘hotspot’: a cross-sectional serosurvey	Richardson	2016
PMID 20161740	High prevalence of both humoral and cellular immunity to Zaire ebolavirus among rural populations in Gabon	Becquart	2010
PMID 9988162	Clinical, virologic, and immunologic follow-up of convalescent Ebola hemorrhagic fever patients and their household contacts, Kikwit, Democratic Republic of the Congo. Commission de Lutte contre les Epidemies a Kikwit	Rowe	1999
PMID 23343532	Ebola virus antibodies in fruit bats, bangladesh	Olival	2013
PMID 8622982	The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing	Sanchez	1996
PMID 20861331	Enzyme-linked immunosorbent assay for detection of filovirus species-specific antibodies. Clin Vaccine Immunol 2010; 17:1723–8	Nakayama	2010
PMID 23711383	Genomic analysis of filoviruses associated with four viral hemorrhagic fever outbreaks in Uganda and the Democratic Republic of the Congo in 2012. Virol 2013; 442:97–100	Albarino	2013
PMID 19751577	Response to imported case of Marburg hemorrhagic fever, the Netherland	Timen	2009
PMID 20019654	Imported case of Marburg hemorrhagic fever - Colorado, 2008	Centers for Disease Control and Preventi	2009
PMID 14720391	Risk factors for Marburg hemorrhagic fever, Democratic Republic of the Congo	Bausch	2003
PMID 16775337	Marburgvirus genomics and association with a large hemorrhagic fever outbreak in Angola	Towner	2006