Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques
ABSTRACT Simian hemorrhagic fever (SHF) is a highly lethal disease in captive macaques. Three distinct arteriviruses are known etiological agents of past SHF epizootics, but only one, simian hemorrhagic fever virus (SHFV), has been isolated in cell culture. The natural reservoir(s) of the three viru...
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American Society for Microbiology
2016
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oai:doaj.org-article:a904addf906743f29017beb908b6e0782021-11-15T15:49:39ZDivergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques10.1128/mBio.02009-152150-7511https://doaj.org/article/a904addf906743f29017beb908b6e0782016-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02009-15https://doaj.org/toc/2150-7511ABSTRACT Simian hemorrhagic fever (SHF) is a highly lethal disease in captive macaques. Three distinct arteriviruses are known etiological agents of past SHF epizootics, but only one, simian hemorrhagic fever virus (SHFV), has been isolated in cell culture. The natural reservoir(s) of the three viruses have yet to be identified, but African nonhuman primates are suspected. Eleven additional divergent simian arteriviruses have been detected recently in diverse and apparently healthy African cercopithecid monkeys. Here, we report the successful isolation in MARC-145 cell culture of one of these viruses, Kibale red colobus virus 1 (KRCV-1), from serum of a naturally infected red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) sampled in Kibale National Park, Uganda. Intramuscular (i.m.) injection of KRCV-1 into four cynomolgus macaques (Macaca fascicularis) resulted in a self-limiting nonlethal disease characterized by depressive behavioral changes, disturbance in coagulation parameters, and liver enzyme elevations. In contrast, i.m. injection of SHFV resulted in typical lethal SHF characterized by mild fever, lethargy, lymphoid depletion, lymphoid and hepatocellular necrosis, low platelet counts, increased liver enzyme concentrations, coagulation abnormalities, and increasing viral loads. As hypothesized based on the genetic and presumed antigenic distance between KRCV-1 and SHFV, all four macaques that had survived KRCV-1 injection died of SHF after subsequent SHFV injection, indicating a lack of protective heterotypic immunity. Our data indicate that SHF is a disease of macaques that in all likelihood can be caused by a number of distinct simian arteriviruses, although with different severity depending on the specific arterivirus involved. Consequently, we recommend that current screening procedures for SHFV in primate-holding facilities be modified to detect all known simian arteriviruses. IMPORTANCE Outbreaks of simian hemorrhagic fever (SHF) have devastated captive Asian macaque colonies in the past. SHF is caused by at least three viruses of the family Arteriviridae: simian hemorrhagic fever virus (SHFV), simian hemorrhagic encephalitis virus (SHEV), and Pebjah virus (PBJV). Nine additional distant relatives of these three viruses were recently discovered in apparently healthy African nonhuman primates. We hypothesized that all simian arteriviruses are potential causes of SHF. To test this hypothesis, we inoculated cynomolgus macaques with a highly divergent simian arterivirus (Kibale red colobus virus 1 [KRCV-1]) from a wild Ugandan red colobus. Despite being only distantly related to red colobuses, all of the macaques developed disease. In contrast to SHFV-infected animals, KRCV-1-infected animals survived after a mild disease presentation. Our study advances the understanding of an important primate disease. Furthermore, our data indicate a need to include the full diversity of simian arteriviruses in nonhuman primate SHF screening assays.Victoria Wahl-JensenJoshua C. JohnsonMichael LauckJason T. WeinfurterLouise H. MonclaAndrea M. WeilerOlivia CharlierOscar RojasRussell ByrumDan R. RaglandLouis HuzellaErika ZommerMelanie CohenJohn G. BernbaumYíngyún CaìHannah B. SanfordSteven MazurReed F. JohnsonJing QinGustavo F. PalaciosAdam L. BaileyPeter B. JahrlingTony L. GoldbergDavid H. O’ConnorThomas C. FriedrichJens H. KuhnAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 1 (2016) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Microbiology QR1-502 |
| spellingShingle |
Microbiology QR1-502 Victoria Wahl-Jensen Joshua C. Johnson Michael Lauck Jason T. Weinfurter Louise H. Moncla Andrea M. Weiler Olivia Charlier Oscar Rojas Russell Byrum Dan R. Ragland Louis Huzella Erika Zommer Melanie Cohen John G. Bernbaum Yíngyún Caì Hannah B. Sanford Steven Mazur Reed F. Johnson Jing Qin Gustavo F. Palacios Adam L. Bailey Peter B. Jahrling Tony L. Goldberg David H. O’Connor Thomas C. Friedrich Jens H. Kuhn Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques |
| description |
ABSTRACT Simian hemorrhagic fever (SHF) is a highly lethal disease in captive macaques. Three distinct arteriviruses are known etiological agents of past SHF epizootics, but only one, simian hemorrhagic fever virus (SHFV), has been isolated in cell culture. The natural reservoir(s) of the three viruses have yet to be identified, but African nonhuman primates are suspected. Eleven additional divergent simian arteriviruses have been detected recently in diverse and apparently healthy African cercopithecid monkeys. Here, we report the successful isolation in MARC-145 cell culture of one of these viruses, Kibale red colobus virus 1 (KRCV-1), from serum of a naturally infected red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) sampled in Kibale National Park, Uganda. Intramuscular (i.m.) injection of KRCV-1 into four cynomolgus macaques (Macaca fascicularis) resulted in a self-limiting nonlethal disease characterized by depressive behavioral changes, disturbance in coagulation parameters, and liver enzyme elevations. In contrast, i.m. injection of SHFV resulted in typical lethal SHF characterized by mild fever, lethargy, lymphoid depletion, lymphoid and hepatocellular necrosis, low platelet counts, increased liver enzyme concentrations, coagulation abnormalities, and increasing viral loads. As hypothesized based on the genetic and presumed antigenic distance between KRCV-1 and SHFV, all four macaques that had survived KRCV-1 injection died of SHF after subsequent SHFV injection, indicating a lack of protective heterotypic immunity. Our data indicate that SHF is a disease of macaques that in all likelihood can be caused by a number of distinct simian arteriviruses, although with different severity depending on the specific arterivirus involved. Consequently, we recommend that current screening procedures for SHFV in primate-holding facilities be modified to detect all known simian arteriviruses. IMPORTANCE Outbreaks of simian hemorrhagic fever (SHF) have devastated captive Asian macaque colonies in the past. SHF is caused by at least three viruses of the family Arteriviridae: simian hemorrhagic fever virus (SHFV), simian hemorrhagic encephalitis virus (SHEV), and Pebjah virus (PBJV). Nine additional distant relatives of these three viruses were recently discovered in apparently healthy African nonhuman primates. We hypothesized that all simian arteriviruses are potential causes of SHF. To test this hypothesis, we inoculated cynomolgus macaques with a highly divergent simian arterivirus (Kibale red colobus virus 1 [KRCV-1]) from a wild Ugandan red colobus. Despite being only distantly related to red colobuses, all of the macaques developed disease. In contrast to SHFV-infected animals, KRCV-1-infected animals survived after a mild disease presentation. Our study advances the understanding of an important primate disease. Furthermore, our data indicate a need to include the full diversity of simian arteriviruses in nonhuman primate SHF screening assays. |
| format |
article |
| author |
Victoria Wahl-Jensen Joshua C. Johnson Michael Lauck Jason T. Weinfurter Louise H. Moncla Andrea M. Weiler Olivia Charlier Oscar Rojas Russell Byrum Dan R. Ragland Louis Huzella Erika Zommer Melanie Cohen John G. Bernbaum Yíngyún Caì Hannah B. Sanford Steven Mazur Reed F. Johnson Jing Qin Gustavo F. Palacios Adam L. Bailey Peter B. Jahrling Tony L. Goldberg David H. O’Connor Thomas C. Friedrich Jens H. Kuhn |
| author_facet |
Victoria Wahl-Jensen Joshua C. Johnson Michael Lauck Jason T. Weinfurter Louise H. Moncla Andrea M. Weiler Olivia Charlier Oscar Rojas Russell Byrum Dan R. Ragland Louis Huzella Erika Zommer Melanie Cohen John G. Bernbaum Yíngyún Caì Hannah B. Sanford Steven Mazur Reed F. Johnson Jing Qin Gustavo F. Palacios Adam L. Bailey Peter B. Jahrling Tony L. Goldberg David H. O’Connor Thomas C. Friedrich Jens H. Kuhn |
| author_sort |
Victoria Wahl-Jensen |
| title |
Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques |
| title_short |
Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques |
| title_full |
Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques |
| title_fullStr |
Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques |
| title_full_unstemmed |
Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques |
| title_sort |
divergent simian arteriviruses cause simian hemorrhagic fever of differing severities in macaques |
| publisher |
American Society for Microbiology |
| publishDate |
2016 |
| url |
https://doaj.org/article/a904addf906743f29017beb908b6e078 |
| work_keys_str_mv |
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