Chapter 55 : Alphaviruses

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The alphaviruses are principally mosquito-borne, positive-strand RNA viruses in the family that exhibit a broad range of pathogenicity in humans and animals (1, 2). Members of the genus are distributed worldwide in diverse ecological niches, where they are usually maintained in cycles between mosquitoes and birds or mammals. While human infections generally are incidental to the transmission cycles, in some instances human-mosquito-human cycles can maintain transmission and lead to large outbreaks and epidemics. Among the 24 alphaviruses listed in Table 1, 16 have been associated with human illness. Clinically, these manifest most commonly as polyarthralgia, often accompanied by fever and/or rash, or as central nervous system (CNS) infections. In addition to the alphaviruses circulating between mosquitoes and vertebrate hosts, a single example of an alphavirus, restricted to mosquitoes, has recently been described, Eilat virus (EILV) (3), and there are two known aquatic species, southern elephant seal virus (SESV) and salmon pancreatic disease virus (SPDV), that are likely to have lice as vectors (4, 5). This chapter reviews general aspects of the virology, pathogenesis, laboratory diagnosis, and prevention of the alphavirus infections, followed by more detailed discussion of those that cause human disease.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 1

Phylogenetic tree of the alphavirus species and selected variants based on the structural protein (E2, 6K, E1) amino acid sequences constructed using Bayesian methods and midpoint rooting. Terminal nodes are labeled by virus species, subtype, or variant, in parentheses. The dashed line indicates the point at which ancestors of Sindbis and Madariaga viruses recombined to form the recombinant WEEV group. All posterior probabilities were 1 except nodes with a symbol had posterior probabilities less than 0.9 and nodes with a had no posterior support. Adapted from reference with permission.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 2

Ross River virus (RRV): (Left) Cryoelectron microscopic image reconstruction of RRV showing the flower-like envelope protein spikes, virion membrane, and nucleocapsid core. (Right) Relationships of spike and capsid proteins and virion RNA. Courtesy of R. J. Kuhn.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 3

Schematic diagram of alphavirus genome [positive (+) sense RNA with poly(A) (A) tail and 5′ terminal cap (CAP); viral complementary RNA (vcRNA) of negative (-) sense; and subgenomic mRNA of positive sense]. Viral nonstructural proteins are translated from the 5′ two-thirds region of the genome, yielding polyprotein intermediates and nonstructural proteins nsP1 to nsP4. RNA is replicated into negative-sense RNA templates and transcribed into 26S subgenomic RNA. Cotranslational processing of the subgenomic mRNA yields the three principal structural proteins: capsid and envelope glycoproteins (E1 and E2). ORF, open reading frame; nt, nucleotide.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 4

Replication of alphaviruses. After binding to the cell membrane (step 1), virions are taken up in endocytic vesicles (steps 2 and 3). The virion and vesicular membranes fuse, releasing the nucleocapsid (step 4). The viral nucleocapsid binds to a ribosome (step 5) and is uncoated, freeing viral RNA (step 6) from the individual capsid (gray dots). Positive-sense viral RNA (heavy line) is replicated (step 7), producing complementary negative-sense RNA (gray line) (step 8), which, in turn, is transcribed to full-length genomic positive-sense RNA (step 9) or subgenomic RNA (step 10). Nonstructural proteins (nsp) are translated from genomic RNA. Subgenomic RNA is translated to produce capsid proteins (black dots) and envelope proteins, which are modified before insertion into the cell membrane (gray bars) (step 11). Genomic RNA is packaged with capsid proteins into nucleocapsid cores (step 12); capsid and E2 proteins associate (step 13) prior to viral budding (step 14).

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 5

Reported cases of EEE among humans in the United States, 2004 to 2013. The reported incidence is highest in Florida, where equine cases are reported perennially from the northeastern coast and throughout the peninsula. Relatively constant inland foci of transmission have been identified in upstate New York, southwestern Michigan, northeastern Indiana, and southcentral Georgia. In Massachusetts, human cases have been reported almost entirely from the eastern counties and, in New Jersey, from the southern counties. Reprinted from the CDC at http://www.cdc.gov/easternequineencephalitis/tech/epi/html.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 7

Reported cases of EEE by month, United States, 2003–2015. Data from reference .

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 6

Schematic diagram of the EEE transmission cycle; solid lines show known portions, and broken lines show speculative portions. The principal enzootic mosquito vector, transmits the virus among birds and occasionally initiates an outbreak among pheasants or other captive birds. Various other species bridge the enzootic cycle to infect humans and horses, which are dead-end hosts; the principal species include found in salt marsh coastal habitat; associated with open meadows and flooded ground pools; associated with woodland pools; and found in open freshwater swamps with emerging vegetation. The viral overwintering mechanism is unknown but potentially includes vertically infected mosquitoes, persistently infected birds, and other vertebrates.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 8

Geographic distribution of VEE epizootics and sylvatic viral subtypes.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 9

Life cycles of Venezuelan equine encephalitis virus. (A) Sylvatic VEEVs circulate continuously in silent tropical and subtropical foci among () mosquitoes and small mammals or aquatic birds. Humans (e.g., soldiers on jungle bivouacs) are infected when they chance upon transmission foci. Bridging vectors (e.g., ) that feed on viremic vertebrates in a sylvatic focus can carry the virus to nearby areas of human activity. (B) In contrast to the continuous cycling of sylvatic VEEV subtypes, epizootic VEEV had never been isolated until recently, except during periodic outbreaks. Once introduced, epizootic viruses are rapidly amplified among equines (horses and burros). Equines develop high viremia levels, so various mosquito species can function as biological vectors (only some important species are shown), and other biting insects, such as blackflies, can spread the virus mechanically. Humans develop illness with high viremia levels but probably have an insignificant role, if any, in viral amplification. Transmission declines as susceptible equines are exhausted by natural infection or immunization. It is speculated that epizootic IC viruses arise by mutation from sylvatic ID viruses; the subpopulation circulates in a sylvatic cycle and under appropriate conditions is amplified, leading to epizootic and epidemic spread.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 10

Origin, spread, and distribution of chikungunya virus and its vectors showing the African origins of enzootic chikungunya virus strains and the patterns of emergence and spread of the Asian lineage and Indian Ocean lineage (IOL) of the virus and the distributions of and . ECSA denotes eastern, central, and southern African. Reprinted from reference with permission.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 11

Small papular lesions seen in Sindbis (Ockelbo) fever. Courtesy of B. Niklasson.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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Image of FIGURE 12

Notifications and notification rates of RRV infections, Australia, 2005–2006, by Statistical Division of residence. Reprinted from reference with permission.

Citation: Smith D, Mackenzie J, Frolov I, Weaver S. 2017. Alphaviruses, p 1347-1379. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch55
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