West Nile fever-a reemerging mosquito-borne viral disease in Europe.
The 1996-97 outbreak of West Nile fever in and near Bucharest, Romania, with more than 500 clinical cases and a case-fatality rate approaching 10% (1-3), was the largest outbreak of arboviral illness in Europe since the Ockelbo-Pogosta-Karelian fever epidemic caused by Sindbis virus in northern Europe in the 1980s. This latest outbreak reaffirmed that mosquito-borne viral diseases may occur on a mass scale, even in temperate climates.
West Nile virus is a member of the Japanese encephalitis antigenic complex of the genus Flavivirus, family Flaviviridae (4). All known members of this complex (Alfuy, Japanese encephalitis, Kokobera, Koutango, Kunjin, Murray Valley encephalitis, St. Louis encephalitis, Stratford, Usutu, and West Nile viruses) are transmissible by mosquitoes and many of them can cause febrile, sometimes fatal, illnesses in humans.
West Nile virus was first isolated from the blood of a febrile woman in the West Nile district of Uganda in 1937 (5) and was subsequently isolated from patients, birds, and mosquitoes in Egypt in the early 1950s (6-7). The virus was soon recognized as the most widespread of the flaviviruses, with geographic distribution including Africa and Eurasia. Outside Europe (Figure), the virus has been reported from Algeria, Asian Russia, Azerbaijan, Botswana, Central African Republic, Cote d'Ivoire, Cyprus, Democratic Republic of Congo (former Zaire), Egypt, Ethiopia, India, Israel, Kazakhstan, Madagascar, Morocco, Mozambique, Nigeria, Pakistan, Senegal, South Africa, Tajikistan, Turkmenia, Uganda, and Uzbekistan. Furthermore, West Nile virus antibodies have been detected in human sera from Armenia, Borneo, China, Georgia, Iraq, Kenya, Lebanon, Malaysia, the Philippines, Sri Lanka, Sudan, Syria, Thailand, Tunisia, and Turkey (8-10). Kunjin virus is closely related to West Nile virus (11,12), representing a counterpart or subtype for Australia and Southeast Asia; some West Nile virus seroreactions in Southeast Asia may, in fact, represent antibodies to Kunjin virus.
West Nile Virus Ecology
Mosquitoes, largely bird-feeding species, are the principal vectors of West Nile virus. The virus has been isolated from 43 mosquito species, predominantly of the genus Culex (Table 1). In Africa and the Middle East, the main vector is Cx. univittatus (although Cx. poicilipes, Cx. neavei, Cx. decens, Aedes albocephalus, or Mimomyia spp. play an important role in certain areas). In Europe, the principal vectors are Cx. pipiens, Cx. modestus, and Coquillettidia richiardii, and in Asia, Cx. quinquefasciatus, Cx. tritaeniorhynchus, and Cx. vishnui predominate. Successful experimental transmission of the virus has been described in Culiseta longiareolata, Cx. bitaeniorhynchus, and Ae. albopictus (8,13). Transovarial transmission of the virus has been demonstrated in Cx. tritaeniorhynchus, Ae. aegypti, and Ae. albopictus, though at low rates.
Table 1. Isolations of West Nile virus from hematophagous arthropods (7-10)
Species No. Countries Mosquitoes Culex antennatus(a) 6 Egypt, Madagascar decens group 8 Madagascar ethiopicus 1 Ethiopia guiarti 1 Cote d"Ivoire modestus 3 France, Russia neavei 4 Senegal, South Africa nigripes 1 Central African Republic perexiguus 1 Israel perfuscus group 3 Central African Republic, Senegal pipiens(a) 7 South Africa, Egypt, Israel, Romania, Czechland, Bulgaria(b) poicilipes 29 Senegal pruina 1 Central African Republic quinquefasciatus(a) 7 India, Pakistan, Madagascar scottii 1 Madagascar theileri(a) 4 South Africa tritaeniorhynchus(a) 3 Pakistan, India, Madagascar univittatus(a) 51 Egypt, Israel, South Africa, Madagascar vishnui(a) group 6 India, Pakistan weschei 1 Central African Republic sp. 3 Egypt, Algeria, Central African Republic Coquillettidia metallica 1 Uganda microannulata 1 South Africa richiardii 5 South Russia, Bulgaria(b) Mansonia uniformis 1 Ethiopia Aedes aegypti(a) 1 Madagascar africanus 1 Central African Republic albocephalus 35 Madagascar albothorax 1 Kenya cantans 7 Slovakia, Ukraine, Bulgaria(b) caspius(a) 1 Ukraine circumluteolus 2 South Africa, Madagascar excrucians 1 Ukraine juppi+caballus 1 South Africa madagascarensis 1 Madagascar vexans 3 Senegal, Russia Anopheles brunnipes 1 Madagascar coustani 1 Israel maculipalpis 1 Madagascar maculipennis 3 Portugal, Ukraine subpictus 1 India sp. 1 Madagascar Mimomyia hispida 8 Senegal lacustris 4 Senegal splendens 6 Senegal sp. 2 Senegal Aedeomyia africana 1 Senegal Soft ticks Argas hermanni(a) 3 Egypt Ornithodoros capensis(a) 5 Azerbaijan Hard ticks Hyalomma marginatum 5 Astrakhan, Azerbaijan detritum 1 Turkmenistan Rhipicephalus turanicus 1 Azerbaijan muhsamae 1 Central African Republic Amblyomma variegatum 1 Central African Republic Dermacentor marginatus(a) 1 Moldavia
(a) Experimental transmission of the virus also demonstrated.
(b) Detected in mosquitoes by immunofluorescence assay.
Virus isolations have occasionally been reported from other hematophagous arthropods (e.g., bird-feeding argasid [soft] or amblyommine [hard] ticks) (Table 1), and experimental transmission has been observed in Ornithodoros savignyi, O. moubata, O. maritimus, O. erraticus, Rhipicephalus sanguineus, R. rossicus, Dermacentor reticulatus, and Haemaphysalis leachii (8,13).
Wild birds are the principal hosts of West Nile virus. The virus has been isolated from a number of wetland and terrestrial avian species in diverse areas (7-10,14-16). High, long-term viremia, sufficient to infect vector mosquitoes, has been observed in infected birds (7,17,18). The virus persists in the organs of inoculated ducks and pigeons for 20 to 100 days (18). Migratory birds are therefore instrumental in the introduction of the virus to temperate areas of Eurasia during spring migrations (12,14-16,19).
Rarely, West Nile virus has been isolated from mammals (Arvicanthis niloticus, Apodemus flavicollis, Clethrionomys glareolus, sentinel mice and hamsters, Lepus europaeus, Rousettus leschenaulti, camels, cattle, horses, dogs, Galago senegalensis, humans) in enzootic foci (8-10). Mammals are less important than birds in maintaining transmission cycles of the virus in ecosystems. Only horses and lemurs (20) have moderate viremia and seem to support West Nile virus circulation locally. Frogs (Rana ridibunda) also can harbor the virus, and their donor ability for Cx. pipiens has been confirmed (21).
Although Palearctic natural foci of West Nile virus infections are mainly situated in wetland ecosystems (river deltas or flood plains) and are characterized by the bird-mosquito cycle, argasid and amblyommine ticks may serve as substitute vectors and form a bird-tick cycle in certain dry and warm habitats lacking mosquitoes. Even a frog-mosquito cycle (21) may function under certain circumstances.
In Europe, West Nile virus circulation is confined to two basic types of cycles and ecosystems: rural (sylvatic) cycle (wild, usually wetland birds and ornithophilic mosquitoes) and urban cycle (synanthropic or domestic birds and mosquitoes feeding on both birds and humans, mainly Cx. pipiens/molestus). The principal cycle is rural, but the urban cycle predominated in Bucharest during the 1996-97 outbreak (2,3). Circulation of West Nile fever in Europe is similar to that of St. Louis encephalitis in North America, where the rural cycle of exoanthropic birds--Cx, tarsalis alternates with the urban cycle of synanthropic birds--Cx, pipiens/ quinquefasciatus.
West Nile Fever in Humans and Other Vertebrates
West Nile fever in humans usually is a febrile, influenzalike illness, characterized by an abrupt onset (incubation period is 3 to 6 days) of moderate to high fever (3 to 5 days, infrequently biphasic, sometimes with chills), headache (often frontal), sore throat, backache, myalgia, arthralgia, fatigue, conjunctivitis, retrobulbar pain, maculopapular or roseolar rash (in approximately half the cases, spreading from the trunk to the extremities and head), lymphadenopathy, anorexia, nausea, abdominal pain, diarrhea, and respiratory symptoms (9). Occasionally ([is less than] 15% of cases), acute aseptic meningitis or encephalitis (associated with neck stiffness, vomiting, confusion, disturbed consciousness, somnolence, tremor of extremities, abnormal reflexes, convulsions, pareses, and coma), anterior myelitis, hepatosplenomegaly, hepatitis, pancreatitis, and myocarditis occur. Laboratory findings involve a slightly increased sedimentation rate and a mild leukocytosis; cerebrospinal fluid in patients with central nervous system involvement is clear, with moderate pleocytosis and elevated protein. The virus can be recovered from the blood for up to 10 days in immunocompetent febrile patients, as late as 22 to 28 days after infection in immunocompromised patients; peak viremia occurs 4 to 8 days postinfection. Recovery is complete (less rapid in adults than in children, often accompanied by long-term myalgias and weakness), and permanent sequelae have not been reported. Most fatal cases have been recorded in patients older than 50 years. Many of the West Nile fever symptoms have been reproduced in volunteers with underlying neoplastic disease who had been inoculated with virus to achieve pyrexia and oncolysis (22).
Hundreds of West Nile fever cases have been described in Israel and South Africa. The largest African epidemic, with approximately 3,000 clinical cases, occurred in an arid region of the Cape Province after heavy rains in 1974 (23). An outbreak with approximately 50 patients, eight of whom died, was described in Algeria in 1994 (1). Other cases or outbreaks have been observed in Azerbaijan, Central African Republic, Democratic Republic of Congo (former Zaire), Egypt, Ethiopia, India, Madagascar, Nigeria, Pakistan, Senegal, Sudan, and in a few European countries.
Equine disease, called Near Eastern equine encephalitis in Egypt and lourdige in France, was observed and experimentally reproduced as fever and diffuse encephalomyelitis with a moderate to high fatality rate in Egypt (24), France (c. 50 cases in 1962-65) (25), Italy (14 cases in 1998, six died or were euthanised) (R. Lelli, G. Ferrari, pers. comm.), Portugal (26) and Morocco (42 of 94 affected horses died) (27). In the 1960s, the biphasic, encephalomyelitic form, which causes staggering gait and weakness to paralysis of the hind legs, was apparent among infected semiferal horses in Camargue (25).
Inoculation of sheep with West Nile virus results in fever, abortion in pregnant ewes, and rare encephalitis, in contrast to the asymptomatic infection seen in pigs and dogs (9,28). Rabbits, adult albino rats, and guinea pigs are resistant to West Nile virus infection, but laboratory mice and Syrian hamsters are markedly susceptible; they often become ill with fatal encephalitis, even when inoculated peripherally (8). Adult rodents stressed or immunosuppressed by cold, isolation, cyclophosphamide, corticosterone, or bacterial endotoxin contract fatal encephalitis, even when an attenuated viral strain is given (29). Inoculation of rhesus and bonnet monkeys (but not cynomolgus monkeys or chimpanzees) causes fever, ataxia, and prostration with occasional encephalitis, tremor of extremities, pareses, or paralysis. Infection may be fatal or cause long-term virus persistence in survivors (5,6,30).
Birds usually do not show any symptoms when infected with West Nile virus. However, natural disease due to the virus has been observed in a pigeon in Egypt (7), and inoculation of certain avian species (e.g., pigeons, chickens, ducks, gulls, and corvids) causes occasional encephalitis and death or long-term virus persistence (7,10,17,18). Chick embryos may be killed by the virus (8).
West Nile Virus and Fever in Europe
In Europe, the presence of West Nile virus was indicated in 1958, when two Albanians had specific West Nile virus antibodies (31). The first European isolations of the virus were recorded in 1963 from patients and mosquitoes in the Rhone Delta (32) and from patients and Hyalomma marginatum ticks in the Volga Delta (33,34). West Nile virus was subsequently isolated in Portugal (35), Slovakia (36), Moldavia (37), Ukraine (38), Hungary (39), Romania (2), Czechland (40), and Italy (V. Deubel, G. Ferrari, pers. comm.).
The incidence of West Nile fever in Europe is largely unknown. In the 1960s, cases were observed in southern France (25), southern Russia (41), Spain (26), southwestern Romania (42), in the 1970s, 1980s, and 1990s in Belarus (43), western Ukraine (44), southeastern Romania (1,2), and Czechland (45). West Nile fever in Europe occurs during the period of maximum annual activity of mosquito vectors (July to September) (Table 2).
Table 2. West Nile Virus in Europe, 1960-1998 Country Year Species infected Portugal, southern 1967-1970 Cattle, sheep Horses Humans Mosquitoes (1 isolate) Wild birds Spain, northern 1979 Rodents Northwestern 1960s Humans Donana National Park Humans Ebro Delta 1979 Epidemic of influenza-like illness France, southern 1962 Humans, 10 severe cases (2 isolates) Horses, 50 encephalomyelitis cases (1 isolate) Camargue 1962-1965 Mosquitoes (2 isolates) Wild birds 1975-1980 Humans Horses Corsica 1965 Humans Italy, Tuscany 1998 Horses, 14 cases, 2 fatal (1 isolate) Northeastern 1967-1969 Migrating birds Humans Northwestern Humans Central Humans Domestic mammals Rodents Chickens Southern Humans Goats 1981 Rodents Former Yugoslavia Serbia Humans Croatia Humans Montenegro Humans Bosnia, Kosovo Humans Albania 1958 Humans Domestic animals Greece 1970-1978 Humans Domestic animals Rabbits Birds Bulgaria 1960-1970 Humans Eastern Wetland birds Domestic animals 1978 Mosquitoes (virus detected) Romania Bucharest, SE lowlands 1996 Humans, 453 clin. cases, 9% fatality rate (1 isolate) 1997 Human, 14 cases, 2 fatal Domestic & wild mammals Dogs Wild birds 1966-70 Mosquitoes (1 isolate) Banat (SW) Humans (cases) Southern 1980-1995 Humans Hungary 1970s Rodents (2 isolates) Cattle Humans Slovakia 1972 Mosquitoes (1 isolate) 1970-1973 Migrating birds (4 isolates) Game animals Cattle, dogs Sheep Pigeons Humans Austria 1964-1977 Wetland passerines Reptiles Wild mammals Domestic animals Humans Czechland 1978 Domestic animals Southern Bohemia 1978 Hares Southern Moravia 1980s Game animals 1985 Wetland birds 1990 Cormorants 1997 Mosquitoes (1 isolate) Humans (5 cases) Poland near Warsaw 1996 Sparrows Belarus 1977 Humans (cases in Brest area) 1972-1973 Wild birds Ukraine Southern, western Birds (7 isolates), mosquitoes (3 isolates) Southern 1970s Human cases (4 isolates) Western 1985 Humans 38 cases, encephalitis in 16 Moldavia 1970s Ticks, mosquitoes (several isolates) Humans Russia, Volga Delta 1963-1968 Humans (>10 cases, 3 isolates) Ticks (4 isolates) Water birds (2 isolates) Mosquitoes (2 isolates) Country Species infected HI(a) (%) Portugal, southern Cattle, sheep 15 Horses 29 Humans 3 Mosquitoes (1 isolate) Wild birds 5 Spain, northern Rodents 3 Northwestern Humans 17 Donana National Park Humans + Ebro Delta Epidemic of influenza-like 8-30 illness France, southern Humans, 10 severe cases (2 19 isolates) Horses, 50 encephalomyelitis 9 cases (1 isolate) Camargue Mosquitoes (2 isolates) Wild birds 6 Humans 5 Horses 2 Corsica Humans 30 Italy, Tuscany Horses, 14 cases, 2 fatal (1 isolate) Northeastern Migrating birds 10 Humans 5 Northwestern Humans 23 Central Humans 2-8 Domestic mammals 8 Rodents 8 Chickens 20 Southern Humans 2-5 Goats 2-13 Rodents 1 Former Yugoslavia Serbia Humans 1-8 Croatia Humans 1-3 Montenegro Humans 1 Bosnia, Kosovo Humans 1 Albania Humans Domestic animals Greece Humans 1-27 Domestic animals 7 Rabbits 4 Birds 22 Bulgaria Humans 3 Eastern Wetland birds 2 Domestic animals 1 Mosquitoes (virus detected) Romania Bucharest, SE lowlands Humans, 453 clin. cases, 9% 17 fatality rate (1 isolate) Human, 14 cases, 2 fatal Domestic & wild mammals 2-23 Dogs 19-45 Wild birds 22 Mosquitoes (1 isolate) Banat (SW) Humans (cases) 17 Southern Humans 2-12 Hungary Rodents (2 isolates) Cattle 4-9 Humans 4-6 Slovakia Mosquitoes (1 isolate) Migrating birds (4 isolates) Game animals Cattle, dogs 8 Sheep 1 Pigeons 5 Humans 1-4 Austria Wetland passerines 1-3 Reptiles Wild mammals Domestic animals 7-33 Humans 1-6 Czechland Domestic animals 2 Southern Bohemia Hares 5 Southern Moravia Game animals 8 Wetland birds 4-10 Cormorants 10 Mosquitoes (1 isolate) Humans (5 cases) Poland near Warsaw Sparrows 3-12 Belarus Humans (cases in Brest area) 1 Wild birds 3 Ukraine Southern, western Birds (7 isolates), mosquitoes (3 isolates) Southern Human cases (4 isolates) Western Humans 38 cases, encephalitis in 16 Moldavia Ticks, mosquitoes (several isolates) Humans 3 Russia, Volga Delta Humans (>10 cases, 3 7-31 isolates) Ticks (4 isolates) Water birds (2 isolates) 4-59 Mosquitoes (2 isolates) Neutra- Country Species infected lization (%) Portugal, southern Cattle, sheep Horses Humans Mosquitoes (1 isolate) Wild birds Spain, northern Rodents Northwestern Humans 17 Donana National Park Humans Ebro Delta Epidemic of influenza-like illness France, southern Humans, 10 severe cases (2 isolates) Horses, 50 encephalomyelitis 30 cases (1 isolate) Camargue Mosquitoes (2 isolates) Wild birds Humans Horses Corsica Humans 55 Italy, Tuscany Horses, 14 cases, 2 fatal 40 (1 isolate) Northeastern Migrating birds Humans Northwestern Humans Central Humans Domestic mammals Rodents Chickens Southern Humans Goats Rodents Former Yugoslavia Serbia Humans Croatia Humans Montenegro Humans Bosnia, Kosovo Humans Albania Humans 2 Domestic animals Greece Humans 1 Domestic animals Rabbits Birds Bulgaria Humans Eastern Wetland birds 10 Domestic animals Mosquitoes (virus detected) Romania Bucharest, SE lowlands Humans, 453 clin. cases, 9% fatality rate (1 isolate) Human, 14 cases, 2 fatal Domestic & wild mammals Dogs Wild birds Mosquitoes (1 isolate) Banat (SW) Humans (cases) Southern Humans Hungary Rodents (2 isolates) Cattle Humans Slovakia Mosquitoes (1 isolate) Migrating birds (4 isolates) 1-13 Game animals 1-8 Cattle, dogs Sheep Pigeons Humans Austria Wetland passerines Reptiles Wild mammals Domestic animals Humans Czechland Domestic animals Southern Bohemia Hares Southern Moravia Game animals Wetland birds Cormorants Mosquitoes (1 isolate) Humans (5 cases) 2 Poland near Warsaw Sparrows Belarus Humans (cases in Brest area) Wild birds Ukraine Southern, western Birds (7 isolates), mosquitoes (3 isolates) Southern Human cases (4 isolates) Western Humans 38 cases, encephalitis in 16 Moldavia Ticks, mosquitoes (several isolates) Humans Russia, Volga Delta Humans (>10 cases, 3 isolates) Ticks (4 isolates) Water birds (2 isolates) 2-11 Mosquitoes (2 isolates) Country Species infected Ref. Portugal, southern Cattle, sheep 26, 35 Horses Humans Mosquitoes (1 isolate) Wild birds Spain, northern Rodents Northwestern Humans 26 Donana National Park Humans Ebro Delta Epidemic of influenza-like illness France, southern Humans, 10 severe cases (2 25,32,46 isolates) Horses, 50 encephalomyelitis cases (1 isolate) Camargue Mosquitoes (2 isolates) Wild birds Humans Horses Corsica Humans Italy, Tuscany Horses, 14 cases, 2 fatal 47 (1 isolate) Northeastern Migrating birds Humans (b) Northwestern Humans Central Humans Domestic mammals Rodents Chickens Southern Humans Goats Rodents Former Yugoslavia Serbia Humans 48 Croatia Humans Montenegro Humans Bosnia, Kosovo Humans Albania Humans 31,49 Domestic animals Greece Humans 50.51 Domestic animals Rabbits Birds Bulgaria Humans 52,53 Eastern Wetland birds Domestic animals Mosquitoes (virus detected) Romania 1-3,42 54,55 Bucharest, SE lowlands Humans, 453 clin. cases, 9% fatality rate (1 isolate) Human, 14 cases, 2 fatal Domestic & wild mammals (c) Dogs Wild birds Mosquitoes (1 isolate) Banat (SW) Humans (cases) Southern Humans Hungary Rodents (2 isolates) 39,56 Cattle Humans Slovakia Mosquitoes (1 isolate) 16, 36, 57-60 Migrating birds (4 isolates) Game animals Cattle, dogs Sheep Pigeons Humans Austria Wetland passerines 61,62 Reptiles Wild mammals Domestic animals Humans Czechland Domestic animals 40,45, 63-67 Southern Bohemia Hares Southern Moravia Game animals Wetland birds Cormorants Mosquitoes (1 isolate) Humans (5 cases) Poland near Warsaw Sparrows 68 Belarus Humans (cases in Brest area) 43 Wild birds Ukraine 34,44,69 Southern, western Birds (7 isolates), mosquitoes (3 isolates) Southern Human cases (4 isolates) Western Humans 38 cases, encephalitis in 16 Moldavia Ticks, mosquitoes (several 37, 70 isolates) Humans Russia, 33,344,155 Volga Delta Humans (>10 cases, 3 isolates) Ticks (4 isolates) Water birds (2 isolates) Mosquitoes (2 isolates)
(a) Hemagglutination inhibition.
(b) Q. Ferrari, R. Lelli, pets. comm.
(c) C. Ceianu, pers. comm.
West Nile virus can cause sporadic human cases, clusters, or outbreaks of West Nile fever, even in temperate Europe. Environmental factors, including human activities that enhance vector population densities (irrigation, heavy rains followed by floods, higher than usual temperatures, and formation of ecologic niches enabling the mass breeding of mosquitoes) allow the reemergence of this mosquito-borne disease. For instance, global warming scenarios hypothesize warmer, more humid weather that may produce an increase in the distribution and abundance of mosquito vectors (71). Surveillance for West Nile fever (monitoring population densities and infection rates of principal vectors, serosurveys on vertebrates and exposed human groups, and routine diagnosis of human infections) should therefore be carried out in affected areas.
The mechanism of West Nile virus persistence in disease-endemic foci of temperate Europe presents a challenge for further research. General hypotheses of how an arbovirus could overwinter under adverse climatic conditions have already been postulated (72). The virus could persist in hibernating female Culex spp.; transovarially infected Culex spp. progeny; or chronically infected vertebrate hosts, perhaps birds or frogs. Alternatively, the virus may be reintroduced by chronically infected migratory birds from tropical or subtropical foci at irregular intervals. These issues have to be addressed, because present data substantiate all particular mechanisms and their combinations. For instance, the hibernating vector idea has been supported by a few field and experimental data on female Cx. univittatus (7,73). On the other hand, if the reintroduction scheme is correct, a greatly increased activity of West Nile virus in Africa should be followed by an epidemic occurrence of West Nile fever in Europe in the next few years.
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Zdenek Hubalek and Jiri Halouzka are scientists at the Academy of Sciences of the Czech Republic. They are interested in the ecology of arthropodborne human pathogenic viruses and bacteria.
Address for correspondence: Z. Hubalek, Institute of Vertebrate Biology, Academy of Sciences, Klasterni 2, CZ-69142 Valtice, Czech Republic; fax: 420-627-352-387; e-mail: email@example.com.
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|Publication:||Emerging Infectious Diseases|
|Date:||Sep 1, 1999|
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