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Zoonosis Update the Arenaviruses

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0915ZU.qxp 8/29/2005 2:58 PM Page 904 Zoonosis Update The arenaviruses Michele T. Jay, DVM, MPVM, DACVPM; Carol Glaser, DVM, MD; Charles F. Fulhorst, DVM, DrPH he virus family Arenaviridae is a diverse group of of 2 single-stranded RNA molecules designated L TRNA viruses and includes the etiologic agents of (large) and S (small). The S segment encodes gene several emerging zoonoses that are characterized by sequences for 2 structural proteins: the nucleocapsid high case-fatality rates. Murid rodents (rats and mice) protein and the envelope glycoprotein precursor, which are the principal reservoirs of the arenaviruses for is posttranslationally cleaved into the GP-1 and GP-2 which natural host relationships have been studied subunits. Notably, partial sequence analysis of the extensively. Six arenaviruses are known to cause nucleocapsid protein has been extensively used to study human disease: Guanarito virus (causes Venezuelan the evolution and genetic diversity of the Arenaviridae. hemorrhagic fever), Junin virus (Argentine hemorrhag- The Arenaviridae has only 1 unique genus, ic fever), lymphocytic choriomeningitis virus (lym- Arenavirus, which currently includes 22 species phocytic choriomeningitis), Lassa virus (Lassa fever), (Appendix).1,2 Many novel arenaviruses have been Machupo virus (Bolivian hemorrhagic fever), and Sabiá reported in the literature3–7 over the last decade, espe- virus (human disease [not yet named]). cially in the Americas, but the natural history and clin- The purpose of this article is to review the major ical importance of most of these viruses remain features of the zoonotic arenaviruses, which are impor- unclear. The family comprises 2 serocomplexes: the tant for several reasons: the viruses cause severe disease lymphocytic choriomeningitis-Lassa (Old World) com- in humans in the geographic regions where the viruses plex and the Tacaribe (New World) complex. Members are endemic, infections may be diagnosed in humans of the former are associated with the subfamily outside of areas in which the viruses are endemic as a Murinae (Old World rats and mice), whereas members result of travel or exposure in research settings, labora- of the latter are associated with the subfamily tory and pet animals (mice and hamsters) and wild- Sigmodontinae (New World rats and mice). caught rodents may harbor arenaviruses and pose a risk Undoubtedly, the number of recognized arenaviruses to their handlers, legal or illegal importation of wild will continue to increase as more potential rodent- rodents for the pet trade could result in introduction of virus relationships are examined. arenaviruses into locations in which the viruses are not The lymphocytic choriomeningitis-Lassa complex endemic, and arenaviruses are classified as Category A is grouped into 2 monophyletic lineages that appear to bioterrorism pathogens by the CDC because of the correlate with monophyletic genera within the rodent extremely serious consequences to public health associ- subfamily Murinae.8 The South American members of ated with their use in a terrorist attack. the Tacaribe complex are classified into 3 distinct lin- eages (designated A, B, and C), and in some instances, Taxonomy and Classification the lineages appear to correlate with monophyletic genera within the rodent subfamily Sigmodontinae.8–10 Arenavirus particles are spherical to pleomorphic 11,12 and approximately 50 to 300 nm in diameter. Virions Results of recent phylogenetic studies by Charrel et possess a lipid-containing envelope that is covered with al indicate that the North American arenaviruses (Bear distinct, spikelike projections distributed evenly over Canyon, Tamiami, and Whitewater Arroyo) comprise a the surface. Host-cell ribosomes are accumulated in fourth lineage in the Tacaribe complex and are the variable numbers within the envelope. In fact, the name product of recombination between 2 South American “arena” originates from the Latin word for sandy arenaviruses, one from lineage A and one from lineage (arenosus), which describes the granular appearance of B. All of the pathogenic viruses in the Tacaribe com- these host-cell ribosomes when viewed by use of an plex are classified in lineage B (Guanarito, Junin, electron microscope.1 The Arenaviridae genome consists Machupo, and Sabiá viruses), perhaps suggesting an as yet unrecognized genetic factor that is causally associ- From the California Department of Health Services, Division of ated with the pathogenic phenotype of the New World Communicable Disease Control, 1616 Capitol Ave, Sacramento, CA arenaviruses.10 95899-7413 (Jay); the California Department of Health Services, Findings of phylogenetic studies have also sug- Division of Communicable Disease Control, 805 Marina Bay Pkwy, gested that there is an ancient evolutionary relation- Richmond, CA 94804 (Glaser); and the Department of Pathology, University of Texas Medical Branch, Galveston, TX 77555-0144 ship between the arenaviruses and their specific rodent (Fulhorst). Dr Jay’s present address is Western Institute for Food hosts. The Muridae-Arenaviridae relationship may be Safety and Security, University of California, Davis, CA 95616. an example of host-virus codivergence, at least in some Address correspondence to Dr. Jay instances in which the phylogeny of the virus species 904 Vet Med Today: Zoonosis Update JAVMA, Vol 227, No. 6, September 15, 2005 0915ZU.qxp 8/29/2005 2:58 PM Page 905 appears to match the phylogeny of its specific rodent Although much has been learned about the epi- host.8–10 Although intriguing, the codivergence model demiologic and ecologic characteristics of the arena- for rodent and arenavirus evolution is difficult to viruses since the discovery of lymphocytic chorio- prove, especially because the taxonomy of the Muridae meningitis virus more than 70 years ago, there are still remains controversial. Interestingly, a similar phyloge- many gaps in our understanding of this complex group netic relationship has been observed between murid of viruses. Arenaviruses and their associated human rodent reservoirs and hantaviruses, another emerging diseases are difficult to study for several reasons. First, group of rodent-borne RNA viruses; many epidemio- surveillance systems for arenaviral infections in human logic and ecologic parallels exist between these other- and rodent populations are poor or nonexistent in the wise unrelated rodent-borne viruses.13,14 countries where these viruses are endemic. Second, Partial sequence analysis (primarily based on the population-based, longitudinal studies are challenging nucleocapsid protein) has revealed a remarkable genet- to conduct because most of these viruses circulate in ic diversity within the genus as a whole and among dif- remote and sometimes inaccessible locations of devel- ferent strains of those arenaviruses that have been stud- oping countries; investigations are hampered by the ied in detail. For example, Lassa virus strains vary as lack of roads and other infrastructure and by political much as 27% at the nucleotide level and 15% at the unrest, among other factors. For this reason, there is a amino acid level.15 Genetic diversity among strains may bias toward collecting data from outbreaks or conduct- also vary by host and geographic location. Results of a ing studies in areas in which the disease is hyperen- study16 of Guanarito virus isolates collected from west- demic. Third, safe handling of these viruses requires ern Venezuela identified higher sequence variation high-level containment facilities (biosafety level 4 for among strains isolated from rodents, compared with the hemorrhagic fever viruses). Serologic surveys are human isolates. In the southwestern United States, commonly performed in lieu of studies that involve findings of sequence analyses of Whitewater Arroyo handling live virus, but the results from such investi- virus strains isolated from wood rats have suggested gations can be difficult to interpret because testing that this species varies genetically by geographic loca- methods vary widely between laboratories. Finally, tion.17,18 In addition, considerable genetic diversity has interpretation of epidemiologic data is further compli- been found among Whitewater Arroyo virus strains that cated by an incomplete understanding of the genetic have been isolated from different species of wood rat diversity of the genus and strain differences within the (Neotoma spp). Whether some of these isolates repre- individual species, circulation of different arenaviral sent novel arenaviral species remains to be elucidated. species and coinfections in the same geographic region, and the fact that the taxonomy of many of the Epidemiology and Ecology rodent reservoirs is in flux. Each arenaviral species is usually associated with a Despite these limitations, some generalizations single rodent species or closely related species. All of can be made about the epidemiology of the arenavirus- the arenaviruses that cause disease are rodent-borne es. The geographic distribution of each arenavirus sub- (the reservoir of Sabiá virus is unknown, but presumed sumes the geographic range of its principal host. In the to be a South American rodent). Therefore, the epi- Americas, the distribution of the arenaviruses identi- demiologic and ecologic characteristics of these viruses fied to date has been assessed (Figure 1). The disease depend primarily on rodent-host population dynamics patterns in human populations range from hyper- and human behavior that increases the likelihood of
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