Pathogenesis of bat rabies in a natural reservoir: Comparative susceptibility of the straw-colored fruit bat (Eidolon helvum) to three strains of Lagos bat virus

Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human rabies acquired from bats calls for a better understanding of lyssavirus infections in their natural hosts. So far, there is no experimental...

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Veröffentlicht in:	PLoS neglected tropical diseases Jg. 12; H. 3; S. e0006311
Hauptverfasser:	Suu-Ire, Richard, Begeman, Lineke, Banyard, Ashley C., Breed, Andrew C., Drosten, Christian, Eggerbauer, Elisa, Freuling, Conrad M., Gibson, Louise, Goharriz, Hooman, Horton, Daniel L., Jennings, Daisy, Kuzmin, Ivan V., Marston, Denise, Ntiamoa-Baidu, Yaa, Riesle Sbarbaro, Silke, Selden, David, Wise, Emma L., Kuiken, Thijs, Fooks, Anthony R., Müller, Thomas, Wood, James L. N., Cunningham, Andrew A.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Public Library of Science 01.03.2018 Public Library of Science (PLoS)
Schlagworte:	Analysis Antigens Bats Biology Biology and Life Sciences Brain Brain research Chiroptera Disease DNA Eidolon helvum Endemic species Excretion Fruits Funding Infections Inoculation Medicine and Health Sciences Meningoencephalitis Mephitidae Methods Microbiological strains Nucleotide sequence Oral cavity Pathogenesis Pathology PCR Physiological aspects Rabies Reservoirs (Water) Risk factors RNA-directed DNA polymerase Strains Strains (organisms) Straw Straw colored fruit bat Supervision Tissue Tissues Transmission Tropical diseases Vectors (Biology) Veterinary medicine Virology Viruses Zoology Zoonoses Netherlands Ghana United Kingdom > UK Nigeria Senegal Germany
ISSN:	1935-2735, 1935-2727, 1935-2735
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Abstract	Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human rabies acquired from bats calls for a better understanding of lyssavirus infections in their natural hosts. So far, there is no experimental model that mimics natural lyssavirus infection in the reservoir bat species. Lagos bat virus is a lyssavirus that is endemic in straw-colored fruit bats (Eidolon helvum) in Africa. Here we compared the susceptibility of these bats to three strains of Lagos bat virus (from Senegal, Nigeria, and Ghana) by intracranial inoculation. To allow comparison between strains, we ensured the same titer of virus was inoculated in the same location of the brain of each bat. All bats (n = 3 per strain) were infected, and developed neurological signs, and fatal meningoencephalitis with lyssavirus antigen expression in neurons. There were three main differences among the groups. First, time to death was substantially shorter in the Senegal and Ghana groups (4 to 6 days) than in the Nigeria group (8 days). Second, each virus strain produced a distinct clinical syndrome. Third, the spread of virus to peripheral tissues, tested by hemi-nested reverse transcriptase PCR, was frequent (3 of 3 bats) and widespread (8 to 10 tissues positive of 11 tissues examined) in the Ghana group, was frequent and less widespread in the Senegal group (3/3 bats, 3 to 6 tissues positive), and was rare and restricted in the Nigeria group (1/3 bats, 2 tissues positive). Centrifugal spread of virus from brain to tissue of excretion in the oral cavity is required to enable lyssavirus transmission. Therefore, the Senegal and Ghana strains seem most suitable for further pathogenesis, and for transmission, studies in the straw-colored fruit bat.
AbstractList	Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human rabies acquired from bats calls for a better understanding of lyssavirus infections in their natural hosts. So far, there is no experimental model that mimics natural lyssavirus infection in the reservoir bat species. Lagos bat virus is a lyssavirus that is endemic in straw-colored fruit bats (Eidolon helvum) in Africa. Here we compared the susceptibility of these bats to three strains of Lagos bat virus (from Senegal, Nigeria, and Ghana) by intracranial inoculation. To allow comparison between strains, we ensured the same titer of virus was inoculated in the same location of the brain of each bat. All bats (n = 3 per strain) were infected, and developed neurological signs, and fatal meningoencephalitis with lyssavirus antigen expression in neurons. There were three main differences among the groups. First, time to death was substantially shorter in the Senegal and Ghana groups (4 to 6 days) than in the Nigeria group (8 days). Second, each virus strain produced a distinct clinical syndrome. Third, the spread of virus to peripheral tissues, tested by hemi-nested reverse transcriptase PCR, was frequent (3 of 3 bats) and widespread (8 to 10 tissues positive of 11 tissues examined) in the Ghana group, was frequent and less widespread in the Senegal group (3/3 bats, 3 to 6 tissues positive), and was rare and restricted in the Nigeria group (1/3 bats, 2 tissues positive). Centrifugal spread of virus from brain to tissue of excretion in the oral cavity is required to enable lyssavirus transmission. Therefore, the Senegal and Ghana strains seem most suitable for further pathogenesis, and for transmission, studies in the straw-colored fruit bat. Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human rabies acquired from bats calls for a better understanding of lyssavirus infections in their natural hosts. So far, there is no experimental model that mimics natural lyssavirus infection in the reservoir bat species. Lagos bat virus is a lyssavirus that is endemic in straw-colored fruit bats (Eidolon helvum) in Africa. Here we compared the susceptibility of these bats to three strains of Lagos bat virus (from Senegal, Nigeria, and Ghana) by intracranial inoculation. To allow comparison between strains, we ensured the same titer of virus was inoculated in the same location of the brain of each bat. All bats (n = 3 per strain) were infected, and developed neurological signs, and fatal meningoencephalitis with lyssavirus antigen expression in neurons. There were three main differences among the groups. First, time to death was substantially shorter in the Senegal and Ghana groups (4 to 6 days) than in the Nigeria group (8 days). Second, each virus strain produced a distinct clinical syndrome. Third, the spread of virus to peripheral tissues, tested by hemi-nested reverse transcriptase PCR, was frequent (3 of 3 bats) and widespread (8 to 10 tissues positive of 11 tissues examined) in the Ghana group, was frequent and less widespread in the Senegal group (3/3 bats, 3 to 6 tissues positive), and was rare and restricted in the Nigeria group (1/3 bats, 2 tissues positive). Centrifugal spread of virus from brain to tissue of excretion in the oral cavity is required to enable lyssavirus transmission. Therefore, the Senegal and Ghana strains seem most suitable for further pathogenesis, and for transmission, studies in the straw-colored fruit bat.Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human rabies acquired from bats calls for a better understanding of lyssavirus infections in their natural hosts. So far, there is no experimental model that mimics natural lyssavirus infection in the reservoir bat species. Lagos bat virus is a lyssavirus that is endemic in straw-colored fruit bats (Eidolon helvum) in Africa. Here we compared the susceptibility of these bats to three strains of Lagos bat virus (from Senegal, Nigeria, and Ghana) by intracranial inoculation. To allow comparison between strains, we ensured the same titer of virus was inoculated in the same location of the brain of each bat. All bats (n = 3 per strain) were infected, and developed neurological signs, and fatal meningoencephalitis with lyssavirus antigen expression in neurons. There were three main differences among the groups. First, time to death was substantially shorter in the Senegal and Ghana groups (4 to 6 days) than in the Nigeria group (8 days). Second, each virus strain produced a distinct clinical syndrome. Third, the spread of virus to peripheral tissues, tested by hemi-nested reverse transcriptase PCR, was frequent (3 of 3 bats) and widespread (8 to 10 tissues positive of 11 tissues examined) in the Ghana group, was frequent and less widespread in the Senegal group (3/3 bats, 3 to 6 tissues positive), and was rare and restricted in the Nigeria group (1/3 bats, 2 tissues positive). Centrifugal spread of virus from brain to tissue of excretion in the oral cavity is required to enable lyssavirus transmission. Therefore, the Senegal and Ghana strains seem most suitable for further pathogenesis, and for transmission, studies in the straw-colored fruit bat. Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human rabies acquired from bats calls for a better understanding of lyssavirus infections in their natural hosts. So far, there is no experimental model that mimics natural lyssavirus infection in the reservoir bat species. Lagos bat virus is a lyssavirus that is endemic in straw-colored fruit bats (Eidolon helvum) in Africa. Here we compared the susceptibility of these bats to three strains of Lagos bat virus (from Senegal, Nigeria, and Ghana) by intracranial inoculation. To allow comparison between strains, we ensured the same titer of virus was inoculated in the same location of the brain of each bat. All bats (n = 3 per strain) were infected, and developed neurological signs, and fatal meningoencephalitis with lyssavirus antigen expression in neurons. There were three main differences among the groups. First, time to death was substantially shorter in the Senegal and Ghana groups (4 to 6 days) than in the Nigeria group (8 days). Second, each virus strain produced a distinct clinical syndrome. Third, the spread of virus to peripheral tissues, tested by hemi-nested reverse transcriptase PCR, was frequent (3 of 3 bats) and widespread (8 to 10 tissues positive of 11 tissues examined) in the Ghana group, was frequent and less widespread in the Senegal group (3/3 bats, 3 to 6 tissues positive), and was rare and restricted in the Nigeria group (1/3 bats, 2 tissues positive). Centrifugal spread of virus from brain to tissue of excretion in the oral cavity is required to enable lyssavirus transmission. Therefore, the Senegal and Ghana strains seem most suitable for further pathogenesis, and for transmission, studies in the straw-colored fruit bat. Rabies is a neurologic disease that causes severe suffering and is almost always fatal. The disease is caused by infection with a virus of the genus Lyssavirus, of which 16 species are known. These viruses replicate in neurons, are excreted in the mouth, and are transmitted by bites. Dogs are the most important source of rabies for humans, but recently there is a relative increase in people contracting the disease from bats. To better understand the development of human rabies caused by these bat-acquired viruses, we need to study this disease in its bat host under controlled circumstances. To do so, we chose a naturally occurring lyssavirus–host combination: Lagos bat virus in straw-colored fruit bats. We compared three available strains of Lagos bat virus (all isolated from brains of this bat species) for their ability to mimic a natural infection. We used intracranial inoculation to ensure infection of the brain. All three strains infected brain neurons, resulting in fatal neurologic disease, however only two of the strains showed the ability to reach the site of excretion—the mouth—and were considered a suitable virus to use for further studies of this disease in bats.
Audience	Academic
Author	Kuzmin, Ivan V. Drosten, Christian Kuiken, Thijs Müller, Thomas Banyard, Ashley C. Freuling, Conrad M. Jennings, Daisy Riesle Sbarbaro, Silke Suu-Ire, Richard Cunningham, Andrew A. Eggerbauer, Elisa Wood, James L. N. Horton, Daniel L. Gibson, Louise Wise, Emma L. Breed, Andrew C. Fooks, Anthony R. Goharriz, Hooman Marston, Denise Begeman, Lineke Ntiamoa-Baidu, Yaa Selden, David
AuthorAffiliation	7 Institute of Virology, Medical University of Berlin, Berlin, Germany 8 Institute of Molecular Virology and Cell Biology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Greifswald, Island of Riems, Germany 9 School of Veterinary Medicine, University of Surrey, Guildford, United Kingdom 3 Veterinary Services Department, Ministry of Food and Agriculture, Accra, Ghana 10 Department of Pathology, University of Texas Medical Branch, Galveston, Texas, United States of America 1 Institute of Zoology, Zoological Society of London, London, United Kingdom 6 Wildlife Zoonoses and Vector Borne Disease Research Group, Animal and Plant Health Agency, Addlestone, United Kingdom 11 Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom 4 Wildlife Division of the Forestry Commission, Accra, Ghana 5 Department of Viroscience, Erasmus University Medical Centre, Rotterdam, The Netherlands 2 Department of Animal Biology and Conservation Science, University
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29505617$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	COPYRIGHT 2018 Public Library of Science 2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: ) to three strains of Lagos bat virus. PLoS Negl Trop Dis 12(3): e0006311. https://doi.org/10.1371/journal.pntd.0006311 2018 Suu-Ire et al 2018 Suu-Ire et al 2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: ) to three strains of Lagos bat virus. PLoS Negl Trop Dis 12(3): e0006311. https://doi.org/10.1371/journal.pntd.0006311
Copyright_xml	– notice: COPYRIGHT 2018 Public Library of Science – notice: 2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: ) to three strains of Lagos bat virus. PLoS Negl Trop Dis 12(3): e0006311. https://doi.org/10.1371/journal.pntd.0006311 – notice: 2018 Suu-Ire et al 2018 Suu-Ire et al – notice: 2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: ) to three strains of Lagos bat virus. PLoS Negl Trop Dis 12(3): e0006311. https://doi.org/10.1371/journal.pntd.0006311
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Notes	new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 RSI and LB are joint first authors of this work. The authors have declared that no competing interests exist.
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Snippet	Rabies is a fatal neurologic disease caused by lyssavirus infection. People are infected through contact with infected animals. The relative increase of human...
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SubjectTerms	Analysis Antigens Bats Biology Biology and Life Sciences Brain Brain research Chiroptera Disease DNA Eidolon helvum Endemic species Excretion Fruits Funding Infections Inoculation Medicine and Health Sciences Meningoencephalitis Mephitidae Methods Microbiological strains Nucleotide sequence Oral cavity Pathogenesis Pathology PCR Physiological aspects Rabies Reservoirs (Water) Risk factors RNA-directed DNA polymerase Strains Strains (organisms) Straw Straw colored fruit bat Supervision Tissue Tissues Transmission Tropical diseases Vectors (Biology) Veterinary medicine Virology Viruses Zoology Zoonoses
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Title	Pathogenesis of bat rabies in a natural reservoir: Comparative susceptibility of the straw-colored fruit bat (Eidolon helvum) to three strains of Lagos bat virus
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