Table

California Serogroup (Bunyavirus, Bunyaviridae): Classification, Mosquito Associations, Vertebrate Hosts, and Geographic Distribution of Virus Types and Subtypes

Virus type and subtype

Variety

Vector associations

Vertebrate associations

Geographic distribution

California encephalitis California encephalitis

Inkoo La Crosse

San Angelo Tahyna

Melao

Trivittatus Guaroa

La Crosse Snowshoe hare

Tahyna Lumbo Melao Jamestown Canyon"

South River Keystone

Serra do Navio

Ocblerotatus melanimon

Ochlerotatus dorsalis Ocblerotatus and Aedes spp. Ochlerotatus triseriatus Ochlerotatus stimulans group Ochlerotatus canadensis Culiseta inornata Aedes, Anopheles, Psorophora? Ae. vexans, Cs. annulata Ae. pembaensis?

Ochlerotatus scapularis? Cs. inornata

Ochlerotatus communis group Ochlerotatus provocans Ochlerotatus abserratus Ochlerotatus intrudens Ochlerotatus stimulans group Anopheles spp. (same as Jamestown Canyon virus?) Ochlerotatus atlanticus,

Ochlerotatus tormentor Ochlerotatus fulvus Ochlerotatus trivittatus Anopheles spp.

Lagomorphs

Lagomorphs? Sciurid rodents, foxes Lagomorphs

Unknown

Lagomorphs

Unknown

Unknown

Deer

United States (western, southwestern) Finland

United States (eastern) United States (northern), Canada

United States (southwestern) Europe, Tajikistan, Azerbaijan East Africa

Trinidad, Brazil, Panama United States, Canada

Deer?

Lagomorphs, Cotton rats

Unknown

Lagomorphs

Unknown

United States (northeastern) United States (coastal, eastern)

Brazil (Amapa state) United States Panama, Colombia, Brazil

'Jerry Slough virus is a strain of Jamestown Canyon virus in the western United States.

1943. It was isolated from Ochlerotatus melanimon and Cx. tarsalis at that place and time. Extensive studies of the mosquito and vertebrate-host relationships of this virus in California have shown that Oc. melanimon and Oc. dorsalis are the principal vectors and that the virus is transmitted transovarially by these species. Serologic surveys have implicated jackrabbits, cottontail rabbits, California ground squirrels, and kangaroo rats as vertebrate hosts. The virus also has been isolated in New Mexico, Utah, and Texas. However, since the time of original discovery, CE virus only rarely has been associated with human disease.

La Crosse (LAC) virus This is the most important human pathogen in the California serogroup, causing an acute, febrile illness in children. Most cases are subclinical or mild, but some progress to severe encephalitis and, rarely, death. In 1964, LAC virus was isolated from preserved brain tissue of a child who had died of encephalitis in 1960 in the vicinity of La Crosse, Wisconsin (USA). The virus currently is distributed in the eastern United States, including the midwestern states bordering the Great Lakes, east to New York and Pennsylvania, south to West Virginia and North Carolina, and west to Texas. However, most human cases occur in West Virginia, Wisconsin, Illinois, Indiana, and Ohio.

The disease tends to be highly focal within its known range, such that particular regions or towns are known to be endemic. Prevalence varies regionally. In the United States, there were 2245 cases of La Crosse encephalitis reported to the Centers for Disease Control and Prevention from 1964 to 1995, with an average of 70 per year (range, 29—160). In Ohio, where cases are particularly well documented, there was an average of 26 cases per year between 1963 and 1995. La Crosse encephalitis probably is underreported to public health agencies.

The principal vector of LAC virus is the eastern tree hole mosquito, Ochlerotatus triseriatus. The virus is transmitted both horizontally, to sciurid rodents, particularly chipmunks and squirrels, and vertically, from female mosquitoes to their progeny. The discovery of transovar-ial transmission of LAC virus was one of the first documentations of this phenomenon in mosquitoes and revealed an overwintering mechanism for LAC virus. It also demonstrated that vertebrate reservoirs were not always essential to the persistence of mosquito-borne viruses in nature and that the mosquito itself could be a reservoir host. Thus an infected female is able to transmit the virus at its first blood feeding without previously having taken an infectious blood meal. Another important new finding was that Ae. triseriatus males, infected transovar-ially, transferred LAC virus to females via mating (i.e., venereal transmission).

Epidemiologic investigations of cases of encephalitis or aseptic meningitis of unknown origin often reveal La Crosse encephalitis in areas where previously it was unknown. Such investigations almost always reveal populations of Ochlerotatus triseriatus in the immediate vicinity where infection was thought to occur, such as backyards or wooded areas where children play. Water-filled artificial containers, particularly discarded tires, have become important habitats for Oc. triseriatus larvae and provide a link between the sylvan La Crosse cycle and humans. In Ohio and New York State, LAC virus also has been isolated repeatedly from Ochlerotatus canadensis; however, the role of this mosquito as a vector to humans and its role in an enzootic cycle are not well understood.

Snowshoe hare (SSH) virus This pathogen is closely related to La Crosse virus, but its ecology is very different. It originally was isolated from the blood of a snow-shoe hare in Montana in 1958. Lagomorphs (hares and rabbits) are the enzootic vertebrate hosts. SSH virus is distributed in the northern parts of the United States and in Canada, where it has been isolated from a variety of Ochlerotatus species and from Culiseta inornata. Even though SSH virus is very similar antigenically to La Crosse virus, human disease rarely has been documented except in Ontario, Quebec, and Nova Scotia (Canada), where 10 cases of an encephalitis-like illness have been attributed to SSH virus.

Keystone (KEY) virus This virus is a subtype in the Melao virus complex, first isolated in 1964 from a collection of blood-fed Ochlerotatus atlanticus and Oc. tormentor in Florida. It is not considered to be a human pathogen. It occurs along the eastern seaboard of the United States, where it has been isolated from Oc. atlanticus, Oc. tormentor, Oc. infirmatus, and other mosquitoes. Transovarial transmission of the virus has been demonstrated for Oc. atlanticus in the field. Gray squirrels and cottontail rabbits in northern coastal areas, and cottontail rabbits and cotton rats in Florida and Texas, have been identified as vertebrate hosts.

Trivittatus (TVT) virus This virus was first isolated from Ochlerotatus trivittatus in North Dakota in 1948. It also has been isolated from other mosquitoes, including Oc. infirmatus in the southeastern United States, where Oc. trivittatus is absent. Transovarial transmission has been demonstrated in the latter species. Trivittatus virus shows a widespread distribution in the eastern half of the United States. Cottontail rabbits are vertebrate hosts.

Jamestown Canyon (JC) virus This is another subtype in the Melao virus complex. It was originally isolated from Culiseta inornata in Colorado in 1961. Since that time it has been isolated in both Canada and the United States from Ochlerotatus, Culiseta, and Anopheles species in regions from Alaska east to Ontario and New England, south to Maryland, and in western and southwestern states, including California. The principal vectors are Ochlerotatus species with univoltine life cycles (i.e., snowpool and spring species). An antigenic variant known only from California is Jerry Slough virus, which is transmitted by Cs. inornata. In the eastern United States, a variety or strain of JC subtype is South River virus. Transovarial transmission of JC virus has been demonstrated in some mosquito species. Its vertebrate hosts are large wild ungulates, especially deer. JC virus has been associated with encephalitis-type illness in humans in Ontario, New York, and Michigan.

Tahyna (TAH) virus This is a subtype of the CE virus complex, distributed widely in Europe and parts of western Asia. It has been associated with human febrile and central nervous system illnesses in France, the former Czechoslovakia, and Tajikistan. Foci are now known from Finland south to Tajildstan. Although the prevalence of infection in humans is poorly* known, serosurveys in the Rhine River valley of Germany documented antibody to TAH virus in up to 23% of humans living in the area. In the former Czechoslovakia, TAH virus was implicated in 1% of febrile illnesses of children in an endemic area and in 20% of central nervous system illnesses. This virus was first isolated from Ae. vexans and Ochlerotatus caspius in Slovakia in 1958. The mosquito vectors are Ae. vexans, Oc. caspius, and Cs. annulata. Hares and pigs are vertebrate reservoir hosts. Lumbo virus is a variety of TAH and occurs in parts of Africa.

Rift Valley fever (RVF) virus This pathogen (Fig. 12.20) is classified with viruses in the genus Phlebovirus in the Bunyaviridae (Meegan and Bailey, 1988). It is distributed in eastern Africa north to Egypt, and in parts of West Africa, where it has been associated with large outbreaks of acute illness in livestock (see Veterinary Importance, below). Humans may become infected by mosquito bite or, more commonly, by contact with virus-contaminated blood or through inhalation of virus in aerosols during slaughter of livestock. Humans rarely die of infection but develop an illness including fever, headache, myalgia, retinitis, and, in rare cases, liver involvement. Large epizootics and epidemics have occurred in South Africa (1950-1951,1953), Zimbabwe (19681969), Egypt (1977-1978, 1993), Mauritania (1987), and Kenya and Somalia (1997-1998). These outbreaks generally involved thousands to hundreds of thousands of cases in livestock. The epidemic in Egypt in 1977—1978

FIGURE 12.29 Geographic distribution of human malaria. (Reconstructed from World Health Organization, Vector Biology and Control Division, 1989, and other sources.)

The literature on human malaria and its vectors is voluminous. A comprehensive source is Gilles and Warrell (1994). Other sources include Boyd (1949), Macdonald (1957), Molineaux and Gramiccia (1980), Wernsdorfer and McGregor (1988), and Strickland (1991).

Plasmodium Life Cycle

The complex life cycle of Plasmodium species involves both sexual and asexual reproduction. The sexual phase (gametogony) begins in the blood of the human host and is completed within the lumen of the midgut of the mosquito. The first phase of asexual reproduction (sporo-gony) occurs on the outer wall of the midgut. The second phase of asexual reproduction occurs first in the liver and later in the blood of the human host. The process in both sites is termed schizogony or merogony. Sporogony is often referred to as the exogenous phase of malaria parasite development, because it occurs outside of the human host. Conversely, merogony is often referred to as the endogenous phase of development within the human host. These two developmental phases are depicted in Fig. 12.30 and discussed in more detail below.

An Anopheles female becomes infected with malarial parasites when she ingests blood containing red blood cells that are infected with gametocytes, specifically the sexual microgametocyte and macrogametocyte stages of the parasite. A microgametocyte bursts from its host red blood cell within the blood meal in the midgut lumen of the mosquito, where it extends four to eight flagella-like forms called microgametes in a process termed exflagellation. A macrogametocyte sheds the erythrocytic membrane and transforms into a single mature macrogamete. One microgamete locates and fertilizes a macrogamete, forming a diploid zygote. The zygote transforms into a motile ookinete. The ookinete passes through the per-itrophic membrane, then through the midgut epithelial cell membrane, and forms an oocyst between the midgut epithelial cells and the basement membrane of the epithelium. A single, malaria-infected Anopheles may have few to hundreds of oocysts, depending on the original number of gametocyte-infected red blood cells in the blood meal and on the number of macrogametocytes that become fertilized. During sporogony, the encysted parasite becomes haploid again and undergoes multiple mitoses until the oocyst contains thousands of motile sporo-zoites. The oocyst bursts, releasing sporozoites, which make their way to the salivary glands and penetrate the secretory cells. The sporozoites accumulate within these cells, with some also passing into the salivary ducts. The mosquito then is infective. The sporozoites enter a human host when the mosquito probes and the salivary gland

Ring-form trophozoite

Merozoites

Penetrate red blood cell

'Immature meront

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