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      Transmission cycles, host range, evolution and emergence of arboviral disease

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          Key Points

          • Many recent viral pandemics have been attributed to the ability of some RNA viruses, for example HIV, dengue virus and possibly the severe acute respiratory syndrome (SARS) coronavirus, to change their host range to include humans. The authors discuss the mechanisms of host-range alteration used by a selection of viruses, including Venezuelan equine and Japanese encephalitis viruses (VEEV and JEV, respectively), dengue virus and West Nile virus (WNV).

          • Venezuelan equine encephalitis (VEE) was first recognized as a disease of horses, donkeys and mules in northern South America during the mid 1930s, but there has been renewed interest in this virus because of its potential as a biological weapon. Molecular analysis of epidemic strains — which exploit horses for amplification — and comparison with strains that do not cause epidemic disease, have shown that a few amino-acid mutations can affect host-range alteration. Changes on the surface of the VEE virion seem to be important for these host range changes.

          • JEV causes epidemics of encephalitis in India, Korea, China, South-East Asia and Indonesia. The disease affects children, and is associated with a mortality rate of greater than 20%. However, unlike VEEV, there is no evidence that JEV undergoes mutation and selection to replicate in different hosts. Pigs amplify transmission in peridomestic settings, and migratory birds have a role in dispersion of JEV. Although different genotypes have been isolated, their relevance to pathology and host range is unclear.

          • WNV is now endemic in the United States after first emerging in New York in 1999. WNV has a very broad host range. Forty-nine species of mosquitoes and ticks, and 225 species of birds are susceptible to infection. Other hosts include horses, cattle, llamas, alligators, cats, dogs, wolves and sheep. Transmission of WNV among these species has not been reported. Although humans are probably dead-end hosts, infection with WNV can cause severe disease.

          • Dengue viruses are very important human arboviral pathogens and use humans as reservoir hosts. Aedes aegypti and Aedes albopictus mosquitoes are the most common vectors in urban settings. It is thought that the human epidemic form of dengue virus evolved in the last 2000 years, and genetic analysis indicates that mutations have resulted in adaptation to the urban mosquito host. However, links between mutations and human pathogenicity have not been established.

          • Finally, the authors discuss how host-range changes can be studied experimentally. Cell-culture model systems can be used to find mutations that correlate with virus fitness and adaptation in different host strains. Viruses that replicate in useful laboratory animal models can also be studied in whole animal hosts.

          Abstract

          Many pandemics have been attributed to the ability of some RNA viruses to change their host range to include humans. Here, we review the mechanisms of disease emergence that are related to the host-range specificity of selected mosquito-borne alphaviruses and flaviviruses. We discuss viruses of medical importance, including Venezuelan equine and Japanese encephalitis viruses, dengue viruses and West Nile viruses.

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          Most cited references69

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          Characterization of a novel coronavirus associated with severe acute respiratory syndrome.

          P Rota (2003)
          In March 2003, a novel coronavirus (SARS-CoV) was discovered in association with cases of severe acute respiratory syndrome (SARS). The sequence of the complete genome of SARS-CoV was determined, and the initial characterization of the viral genome is presented in this report. The genome of SARS-CoV is 29,727 nucleotides in length and has 11 open reading frames, and its genome organization is similar to that of other coronaviruses. Phylogenetic analyses and sequence comparisons showed that SARS-CoV is not closely related to any of the previously characterized coronaviruses.
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            Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China.

            Y Guan (2003)
            A novel coronavirus (SCoV) is the etiological agent of severe acute respiratory syndrome (SARS). SCoV-like viruses were isolated from Himalayan palm civets found in a live-animal market in Guangdong, China. Evidence of virus infection was also detected in other animals (including a raccoon dog, Nyctereutes procyonoides) and in humans working at the same market. All the animal isolates retain a 29-nucleotide sequence that is not found in most human isolates. The detection of SCoV-like viruses in small, live wild mammals in a retail market indicates a route of interspecies transmission, although the natural reservoir is not known.
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              Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States.

              In late summer 1999, an outbreak of human encephalitis occurred in the northeastern United States that was concurrent with extensive mortality in crows (Corvus species) as well as the deaths of several exotic birds at a zoological park in the same area. Complete genome sequencing of a flavivirus isolated from the brain of a dead Chilean flamingo (Phoenicopterus chilensis), together with partial sequence analysis of envelope glycoprotein (E-glycoprotein) genes amplified from several other species including mosquitoes and two fatal human cases, revealed that West Nile (WN) virus circulated in natural transmission cycles and was responsible for the human disease. Antigenic mapping with E-glycoprotein-specific monoclonal antibodies and E-glycoprotein phylogenetic analysis confirmed these viruses as WN. This North American WN virus was most closely related to a WN virus isolated from a dead goose in Israel in 1998.
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                Author and article information

                Contributors
                sweaver@utmb.edu
                Journal
                Nat Rev Microbiol
                Nat. Rev. Microbiol
                Nature Reviews. Microbiology
                Nature Publishing Group UK (London )
                1740-1526
                1740-1534
                2004
                : 2
                : 10
                : 789-801
                Affiliations
                [1 ]GRID grid.176731.5, ISNI 0000 0001 1547 9964, Department of Pathology, , Microbiology and Immunology, Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, ; Galveston, 77555-0609 Texas USA
                [2 ]GRID grid.176731.5, ISNI 0000 0001 1547 9964, Department of Pathology, , Microbiology and Immunology, Center for Tropical Diseases, University of Texas Medical Branch, ; Galveston, 77555-0609 Texas USA
                Article
                BFnrmicro1006
                10.1038/nrmicro1006
                7097645
                15378043
                b7598af1-f49f-49a4-9913-b453f0e2a3bf
                © Nature Publishing Group 2004

                This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

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                © Springer Nature Limited 2004

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