Rev. sci. tech. Off. int. Epiz., 2004, 23 (2), 535-555

Epidemiological processes involved in the emergence of vector-borne diseases: West Nile fever, Rift Valley fever, Japanese encephalitis and Crimean-Congo haemorrhagic fever

V. Chevalier, S. de la Rocque, T. Baldet, L. Vial & F. Roger

Centre de coopération internationale en recherche agronomique pour le développement (CIRAD), Campus International de Baillarguet, 34398 Montpellier Cedex 5, France

Summary Over the past few decades, the geographical distribution of arthropod-borne zoonoses has dramatically expanded. The influence of human-induced or ecological changes on the risk of disease outbreaks is undeniable. However, few hypotheses have been proposed which address the re-emergence of these diseases, the spread of these viruses to previously uninfected areas and their establishment therein. Host and vector movements play an important role in the dissemination of pathogens, and the ability of these diseases to colonise previously uninfected areas may be explained by the diversity of hosts and vectors, the presence of favourable ecological conditions, and the successful adaptations of vectors or pathogens to new ecosystems. The objective of this paper is to describe the epidemiological processes of the vector-borne diseases Rift Valley fever, West Nile fever, Japanese encephalitis and Crimean-Congo haemorrhagic fever.

Keywords Crimean-Congo haemorrhagic fever – Dissemination – Diversity – Emerging disease – Epidemiological process – Japanese encephalitis – Rift Valley fever – Vector – West Nile fever. Introduction

Over the past few decades, significant changes in the distribution and vector-host contact, long distance distribution and intensity of major vector-borne zoonotic transportation of arboviruses has also been described. It diseases have been recorded. While some of these diseases has recently been observed that once arboviruses reach have been described in endemic areas, little is known previously uninfected areas they may have the capacity to about the epidemiological processes involved in the settle and spread. In light of these observations, re-emergence of zoonotic arboviruses or the spread of epidemiologists have undertaken investigations to these viruses to previously uninfected areas. This lack of determine why these recent changes in distribution are knowledge combined with an absence of specific taking place now, what the influencing factors are, and for treatments and, in some cases, the lack of a vaccine (there how long such changes will continue to occur. is no vaccine for West Nile fever or Crimean-Congo haemorrhagic fever, and vaccines against Rift Valley fever The aim of this paper is to present a study of the may cause females to abort) may explain the difficulties epidemiological processes involved in the transmission of affected countries have in forecasting outbreaks and vector-borne zoonotic diseases using, as models, four controlling the diseases. current emerging arboviruses: Rift Valley fever (RVF), West Nile fever (WNF), Japanese encephalitis (JE) and Crimean- Many vector-borne zoonotic diseases have a complex Congo haemorrhagic fever (CCHF). The first part of the epidemiology. Although transmission is strongly linked to study will describe the influence of ecological and human- local ecological parameters, i.e. vector dynamics, host induced changes on the occurrence of outbreaks in 536 Rev. sci. tech. Off. int. Epiz., 23 (2)

endemic areas. Mechanisms involved in long distance virus – WNV has recently reached North America and is rapidly dissemination and factors influencing the ability of a spreading across the continent. disease to survive and colonize previously uninfected areas will then be examined. The final section will review the factors and processes that determine the evolution of Japanese encephalitis arthropod-borne diseases in areas where the virus was not Japanese encephalitis virus, belonging to the genus previously present. As stated above, four current emerging Flavivirus (family Flaviviridae), is considered to be the most arboviruses will be used as examples throughout this common cause of encephalitis worldwide. The first severe paper; these diseases are briefly described below. outbreak of disease was reported in Japan in 1924, followed by a series of outbreaks occurring between 1931 and 1948 (128, 149) (Fig. 1). The virus is now endemic Rift Valley fever throughout much of Southeast Asia (93) and is responsible Rift Valley fever virus, belonging to the genus Phlebovirus for over 50,000 clinical cases annually. Symptoms range (family Bunyaviridae), can be transmitted to humans and from a mild fever to acute meningomyeloencephalitis, with other ruminants by several arthropods, although permanent neurological damage reported in 50% of mosquitoes of the genera Aedes and Culex are considered to recovered cases (137). Fatality rates are high (reaching up be the most common vectors of the disease. Human to 25%) in young children (13). The virus is maintained in infections may also result from contact with the tissues and a zoonotic cycle via the transmission between rice field- body fluids of infected ruminants during slaughter or the breeding mosquitoes (mainly from the genus Culex), abortus of infected animals. The disease, which is often domestic pigs and/or water birds, and humans (as clinically inapparent or mild in adult sheep or cattle, may incidental hosts). Although JE continues to spread in Asia, cause abortion in pregnant adults and death in young vaccination campaigns coupled with an improvement in animals. Infections in humans are characterised by a severe living conditions have significantly reduced the impact of influenza-like syndrome, although some patients can the disease in Japan. develop complications during the later stages of the disease, i.e. encephalitis, retinitis or fatal haemorrhagic fever (161). Restrictions on the trade of domestic animals Crimean-Congo haemorrhagic fever and animal products from infected areas can have severe Crimean-Congo haemorrhagic fever virus, belonging to the economic impacts. Rift Valley fever is endemic in many genus Nairovirus (family Bunyaviridae), is a tick-borne African countries and has recently spread to Saudi Arabia zoonosis that is a public health concern in many regions of and Yemen (3, 132). the world including Africa, the Middle East, southern and eastern Europe, and western Asia. Clinical disease in humans is initially manifested as an acute febrile illness West Nile fever followed by a fatal haemorrhagic syndrome with mortality West Nile fever virus, belonging to the genus Flavivirus rates of up to 50% (141). The virus is transmitted to (family Flaviviridae), is categorized, along with Japanese reservoir mammals and humans through the bite of hard encephalitis virus (JEV), Saint Louis encephalitis virus ticks (mainly of the genus Hyalomma). Humans may also (SLEV), and Murray Valley encephalitis virus, as part of the become infected through direct contact with blood or JEV complex (54, 136). The basic transmission cycle tissues of infected humans or livestock (139). The highly involves wild and domestic birds that act as the main hosts pathogenic nature of the virus occasionally results in and mosquitoes (mainly from the genus Culex) that act as serious nosocomial outbreaks (111). Since the first vectors. In favourable ecological conditions the basic cycle outbreak of CCHF described in Europe in 1945 (56), may be amplified by transmission of the virus to humans several subsequent outbreaks have been reported and horses, both of which act as dead-end hosts (12). Most worldwide in newly discovered foci as well as in foci where infections in humans and horses are asymptomatic or the virus has been previously recognized (165). cause non-specific mild febrile signs; however, potentially fatal cases of meningitis or encephalitis may develop, with mortality rates reported of between 26% to 43% in humans and 9% to 16% in horses. Epidemiological processes in

The natural history of WNF varies considerably between endemic areas regions and continents. For example: In endemic areas, the epidemiology of the aforementioned – the virus is widespread and endemic in Africa and Asia diseases is characterised by the immunological background – in Europe, waves of outbreaks have occurred over the and density of vertebrate hosts, vector abundance, and the past two decades local environment. The temporal expression of these Rev. sci. tech. Off. int. Epiz., 23 (2) 537

1924 1994

1954 2003

diseases is based on a natural rhythm balanced by host immunity and vector population dynamics. External events, such as unusual rainfalls or human induced changes, may affect this balance and lead to outbreaks.

Impacts of biological factors Rift Valley fever virus has been recorded across the continent of Africa (including Madagascar) with recent spread into Saudi Arabia. The virus is capable of inhabiting a variety of different bioclimatic conditions including wet and tropical areas, e.g. the Gambia (146), hot and arid 1984 areas, e.g. Yemen (3) or Chad (119), and irrigated regions, e.g. the Senegal River valley (66, 67, 77) and the Nile Delta (57, 130). Fig. 1 The spread of Japanese encephalitis in Asia and in Australia The presence of vectors and their population dynamics are (1924-2003) strongly linked to land cover patterns. For example, the Source: WHO website 2003 annual rainfall at Lake Nasser in Egypt is very low, http:// www.who.int/ith/chapter05-m07-japencepha/html (128, 149) resulting in minimal amplification of the mosquito 538 Rev. sci. tech. Off. int. Epiz., 23 (2)

population. However, high densities of Culex spp. of RVF was recorded in the Ferlo sahelian area, north of (consisting of 93% of Cx. pipiens and 4.5% Cx. univittatus) Senegal, during the 2003 rainy season, which was marked were observed during outbreaks of RVF in this area in by a significant reduction in the average rainfall 1977 and 1978, and were believed to be associated with (Chevalier et al., in preparation). local irrigation practices. Evidence supporting Cx. pipiens as the main vector in these outbreaks included: In West Africa, where climatic factors have not been implicated in outbreaks of RVF, other factors, such as herd – the bioecology of Cx. pipens (population dynamics, immunity, may be important determinants in the temporal biting activity and host preference) pattern of disease outbreaks. A cyclical pattern of disease – a decrease in the number of RVF human cases emergence, with virus circulation recorded every five to six corresponding with a decrease in the Cx. pipiens years during the past 20 years, has been observed in population, occurring at the beginning of the cold season northern Senegal and southern Mauritania (Mauritania 1987 [68], Mauritania and Senegal – isolation of the virus from non blood-fed field 1993 [167], Mauritania 1998 [106]). More recently, in specimens (57, 97, 130). 2002-2003, RVF led to severe animal losses in Mauritania, Senegal, the Gambia and Mali (146). A similar periodicity Conversely, a variety of mosquito species, some of which has also been observed in Egypt. The interepizootic period had previously been confirmed experimentally as vectors coincides with the time when the herds are renewed (145). for RVF (i.e. Cx. pipiens, Ae. caspius and Cx. perexiguus) Following an outbreak, it has been demonstrated that herd (151), were associated with an outbreak of disease in the immunity may reach 80% (146) with a subsequent same region in 1993 (4). decrease in immunity occurring over the following years. If additional exposure does not occur, the herd immunity Vector presence and population dynamics are also strongly will decrease over subsequent years resulting in an linked to climatic factors. In East Africa, the occurrence of increasing susceptibility of the herds once again. outbreaks has been clearly correlated to unusually heavy rainfall associated with El Niño (31, 32, 83, 138), such as How the virus is able to survive the interepizootic period the December 1997 outbreak in Kenya which occurred remains unclear. In wet or irrigated areas, low level virus following a rainfall of 60 to 100 times the average level. circulation may persist all year round as a result of The outbreak then rapidly spread to Somalia and Tanzania permanent Culex populations. In more arid areas, such as resulting in an estimated 89,000 human cases (124). The Ferlo, it has been proven that the virus is capable of primary vectors involved in this outbreak were floodwater circulating at a low level without the appearance of clinical mosquitoes belonging to the Aedes genus, signs during the rainy season (167). In the dry season, (i.e. Ae. cumminsii, Ae. circumluteolus, Ae. mcintoshi), with there are no vectors, which means that there is no Cx. zombaensis acting as secondary vectors. Hypotheses mosquito transmission during this season. There are regarding the processes involved in the transmission of several different hypotheses as to how the virus is RVF within the breeding habitats (referred to in Kenya as maintained during the dry season, as follows: dambos) of these mosquitoes have been derived through studies of mosquito ecology (82). As shown by – the presence of reservoir animals such as rodents, i.e. Ae. mcintoshi, female mosquitoes of the floodwater antibodies to RVF have been detected in the African grass Aedes spp. transmit the virus to their descendents by rat (Arvicanthis niloticus) and the Guinea multimammate vertical transmission (82). The eggs are laid in the wet soil mouse (Mastomys erythroleucus) in Senegal (44), while the of temporary ponds where they are capable of surviving for Namaqua rock rat (Aethomys namaquensis) is believed to be several years once the soil dries (110, 148). Subsequent a reservoir of RVF in South Africa (114) flooding of these areas results in a mass hatching of – vertical transmission by floodwater Aedes spp., as mosquito eggs (51, 102), some of which are infective, described previously. which then leads to a new outbreak of disease. To a lesser extent, the transmission cycle also involves Culex mosquitoes; however, they require a semi-permanent body of water to persist (7). Human-induced risk parameters History provides numerous examples of the potential The correlation between outbreaks of RVF and periods of impact of human induced changes on vector- heavy rainfall observed in East Africa is not relevant to borne diseases. West Africa. For instance, outbreaks of RVF were observed during the drought periods of 1982 to 1985 in Mauritania Crimean-Congo haemorrhagic fever (125) and 1987 in Senegal (107), while outbreaks in the Senegalian cities of Matam and Podor in 2002 (146) During World War Two enemy occupation of Crimea occurred during a dry season. Likewise, a high incidence (autonomous republic of the Ukraine) (1941-1944), Rev. sci. tech. Off. int. Epiz., 23 (2) 539

traditional agriculture activities and the hunting of Climatic conditions also have an effect on disease European hares, an important amplifying host of CCHF, emergence. Dry and hot climatic conditions (129) will were disrupted resulting in a marked increase in hare and increase the concentration of organic materials in standing tick (Hyalomma marginatum) population densities. water, while variations in temperature are known to Reoccupation of this area in 1944 by Russian troops, which influence vector capacities (29, 35, 69). In Romania, it is had not been previously exposed to the disease, resulted in likely that the combination of these factors induced the the first recorded outbreak of CCHF in Crimea. The urban outbreak of 1996 in the city of Bucharest (129). This outbreak stopped when elevated rainfalls led to high tick correlation between poor urban infrastructure, drought mortality, and traditional hunting and agricultural induced vector amplification and WNV outbreaks is practices were reinitiated. reminiscent of some SLEV epidemics that have occurred in the United States of America (USA) (53, 131). West Nile Nine years later a new outbreak took place in Astrakhan virus and SLEV (both of which are included in the JEV Oblast (southern Russia) where vertebrate host and tick serocomplex) have a strong antigenic and genetic vector populations were normally regulated by seasonal relatedness and many epidemiological similarities. inundations of the Volga River. In the early 1950s, however, the river flow was regulated in order to develop On the other hand, changes in human demographics may new agricultural areas. The tick population consequently sometimes have a positive impact. In Asia, for instance, the exploded leading to the first appearance of CCHF in demographic explosion in the 1980s promoted the Astrakhan in 1953 (56). development of rice cultivation and pig breeding (138, 149) (as previously mentioned, rice fields are good mosquito breeding sites and pigs are amplifying hosts of Rift Valley fever JE), consequently, the number of amplifying hosts Human development activities have also been implicated in dramatically increased, provoking the geographical spread outbreaks of arboviruses, such as RVF. The flooding of the of JE. Alternatively, in Japan and Taiwan, the demographic Aswan dam in Egypt in 1971, and the subsequent irrigation explosion was coupled with an increase in urbanisation, an of vast areas used for cultivation provided local mosquitoes improvement in living conditions, the shrinkage of rice with ideal breeding habitats and resulted in high numbers of fields, the implementation of vaccination campaigns and Culex mosquitoes during the following summer. In addition, the intensification and relocation of pig farms far from increases in grassy areas attracted breeders from foreign residential areas. In Japan and Taiwan, the incidence rate of regions leading to a very high density of ruminants in the confirmed cases has dropped dramatically in the last region. Ruminants from infected southern areas may have 20 years, with fewer than 100 cases reported per year in introduced the virus into this new favourable ecosystem. Japan (118, 164). Unfortunately this is not the case in the This combination of events led to the first reported outbreak People’s Republic of China, where traditional pig breeding in this region in 1977 to 1978 (57, 130). At present this area remains predominant and residential areas are located is still considered endemic, with outbreaks or evidence of close to the pig flocks. Consequently, despite large circulating virus recorded in 1993 (4), 1997 (1) and 2003 vaccination campaigns, JE continues to spread, leading to (163). A similar sequence of events was associated with the more than 10,000 cases each year (118). building of the Diama dam in the western African countries of Senegal and Mauritania, although, in this case, the virus was believed to have been present prior to the construction of the dam (125, 167). Changes in disease distribution during the last few decades West Nile fever, Saint Louis encephalitis virus and Japanese encephalitis virus Significant changes in the distribution of arboviruses have been observed recently. In this review, three major Changing human demographics, resulting in an mechanisms by which arboviruses and their vectors are intensification of urbanisation and increasing levels of disseminated will be discussed. poverty, have also been associated with an increased risk of some arbovirus outbreaks (e.g. WNV and SLEV). For the past four decades WNV circulation has been recorded in Virus dissemination associated with domestic Romania and Russia, particularly during the hot summer animal movements months (58, 113). In Bucharest, deteriorated urban and suburban conditions combined with flooding of the During the last few decades the distribution of RVF has basements of many structures, has favoured a high density expanded from the southeastern to the northern countries of Cx. pipiens mosquitoes in human settlements and of Africa. The first major outbreak of RVF was recorded domestic bird breeding grounds. close to Lake Naivasha in Kenya in 1930-1931 (99). Up 540 Rev. sci. tech. Off. int. Epiz., 23 (2)

until 1977, the disease seemed to be limited to southern suggesting that the disease spread from Africa to Africa with infections reported in northeastern South Saudi Arabia via the introduction of viraemic animals (124, Africa in 1950 (103), Namibia in 1955 (100) and South 134). The trade of infected sheep and camels between Africa in 1952-1953, 1955-1959, 1969-1971, Sudan and Egypt was believed to be responsible for the 1974-1976, 1981 and 1999 (6, 88, 89, 91, 140, 142). 1977 RVF outbreak near Lake Nasser in Egypt, an area After 1977, the disease spread to the northern and western known to be involved in the trade of sheep and camels countries of Africa, causing severe human cases and with northern Sudan (1). Outbreaks of disease had substantial livestock losses, i.e. Egypt in been reported in irrigated regions of Sudan since 1977-1978 (57, 130) and the Senegal River valley 1971. The detection of antibodies to RVF in samples (southern Mauritania and northern Senegal) in 1987-1988 collected from camels crossing the border from Sudan into (66, 67, 77). A severe outbreak was recorded in Kenya, Egypt lends further support to this hypothesis (96). Tanzania and Somalia in 1997-1998 (162). In The presence of mosquito vectors (Cx. pipiens, 2000 the disease spread to the Arabic peninsula and Cx. univittatus and Cx. antennatus) in northern Egypt caused the death of 224 people (3, 132) (Fig. 2). (the Nile Delta region) (143) further contributed to the spread of RVF and resulted in a substantial number of The dissemination of RVF virus has, in many cases, been human deaths (598 deaths out of a total of attributed to livestock movements. In Saudi Arabia 200,000 human cases) and severe livestock losses (20, 21) six strains of RVF isolated from mosquitoes in the (80, 95). In Senegal, the Ferlo region is a common Jizan region were shown to be very genetically similar to gathering area for nomadic herds from infected those isolated from the 1997-1998 outbreak in Kenya, neighbouring regions (Senegal River valley, Oriental

1977-1978 1997-1998 2000 1982-1985, 1987-1988, Egypt Saudi Arabia 1993, 1998, 2002-2003 Mauritania 2004 2000 1987-1988, 1993, 2002-2003 Chad Yemen Senegal

2002-2003 The Gambia 1997-1998 Somalia 1930, 1997-1998 Kenya

1997-1998 Tanzania

1979 Madagascar 1955 Namibia

1950-1953, 1955-1959, 1969-1971, 1974-1976, 1981, 1999 South Africa

0 1000 2000 Km.

Fig. 2 Rift Valley fever outbreaks in the world since 1930 In bold, outbreaks in the last five years Rev. sci. tech. Off. int. Epiz., 23 (2) 541

Senegal, Mali, Mauritania and the Gambia). Because of the Phylogenetic analyses indicating a high degree of genetic availability of water and grass in this region, livestock relatedness between strains isolated from the departure owners and their herds regularly settle in this area at the and arrival sites of various migratory routes, have provided beginning of the rainy season. Recent studies have shown additional support for the theory that migratory birds are regular and intensive virus circulation in this area vectors of WNV: (Chevalier, in preparation). – there are few differences between strains circulating thousands of kilometres apart (e.g. Senegal ArD93548/93 Virus dissemination associated with wild bird and Kenya KN3829/98 or Kenya and Italy PaAr981/98) (14) movements – more than 99% of virus RNA nucleotides isolated in Europe and in Africa are similar, regardless of whether the During the last few years, a number of significant strains are isolated from the same or different vectors (i.e. outbreaks of WNV infection in humans and horses have Cx. univittatus in Kenya and Cx. neavei in Senegal) (123) been observed, i.e. Algeria in 1994 (81), Romania in 1996 (129), Morocco in 1996 (2, 109), Italy in 1998 (5), – in September and October 1998 in Eilat (Israel), WNV Russia in 1999 (113), Israel in 2000 (136, 160) and France was isolated from a flock of young white storks that had in 2000 (37). Unexpectedly, WNV was identified for the migrated, for the first time, from Europe to Israel. Some of first time in New York City in 1999 (19), where it resulted these storks also had WNV antibodies. Strains of WNV in 62 human cases, of which seven died (22). In 2003, the isolated during a 1998 outbreak in Israeli geese showed a epidemic was still not under control and USA authorities high degree of genetic relatedness to the strain isolated reported a total of 9,122 human cases (including from the European storks, suggesting that the virus may 30% encephalitis and/or meningitis, 2% of which have originated in eastern Europe. were fatal [26]) across 44 states and six Canadian provinces. A high degree of genetic similarity (>99.8%) Ecological parameters may also have an impact on the was shown between the USA virus strains and those spread of WNV by migratory birds. It is well established isolated from the 1998 outbreak in Israel (79), suggesting that migratory pathways are similar from year to year. that the virus may have been introduced to North America However, parameters such as the date of migration, the from this part of the world (18). duration of the journey, the abundance and diversity of species, the age distribution of the flock, and A common hypothesis is that the virus was introduced the destination may vary: through the importation of infected exotic birds. In the – according to the availability of nesting areas and palearctic and oriental temperate areas, WNF outbreaks are human-induced environmental change generally known to occur: – as a result of climatic conditions during the migration – in the spring, after the introduction of the virus by which may reduce the survival rate of birds migrating birds arriving from southern enzootic tropical areas Furthermore, the stress induced by the migration – in or close to wetland areas where the birds establish (i.e. some birds may lose 50% of their weight during the their nesting sites (61, 143). migration) can have severe physiological consequences which may impact the duration and level of viraemia (8). The long distance transportation of WNF has been attributed to the migration of infected birds from endemic areas. Millions of birds are known to migrate from Africa to Virus dissemination with or through vectors southern Europe annually (11), and although the viraemia in birds is usually short lived, some of the migratory birds Prior to 1995, the recorded geographical distribution of JEV are capable of reaching their European summer nesting infection extended from as far west as Pakistan to as far east sites within the span of a few days (11). Antibodies to as Japan, and as far north as maritime Russia to as far south WNV have been detected in the blood of many migratory as Bali (13, 149). However, in April 1995 an outbreak of birds in Eurasia (59). Similarly, migratory birds have been JE occurred in the Torres Strait, Australia, and resulted in implicated in the spread of genetically related strains of three clinical cases, two of which were fatal. Seroconversion WNV throughout the Western Hemisphere (16, 86, 116). in pigs and humans was reported on Badu Island and other Alternatively, a role for blood feeding ectoparasites of birds surrounding islands in the Torres Strait (47). The main in the transmission of WNV has been suspected. Support vectors incriminated in the spread of the disease were the for this hypothesis comes from the observation that the Culex annulirostris Skuse and mosquitoes of the Culex sitiens principal vectors from which WNV have been isolated are group (64, 120). The emergence of JE in Australia was mainly ornithophilic mosquitoes (Cx. univittatus in the unexpected because the closest area where it had been Middle East and Cx. pipiens in Europe) (59, 61, 79, 143). previously described was in Bali, Indonesia (3,000 km west 542 Rev. sci. tech. Off. int. Epiz., 23 (2)

of the Torres Strait), and the nearest site where it had been isolated was Flores, Indonesia (2,200 km west of the Torres Colonisation of areas previously Strait) (92). In 1998 another case of JEV occurred on Badu Island with widespread seroconversion reported in sentinel unaffected by disease pigs. JEV was widespread on Badu Island and was recorded Upon reaching an area previously unaffected by disease, for the first time in mainland Australia on Cape York favourable conditions may promote the amplification and Peninsula (48). spread of a virus within the novel environment. However, the epidemiological processes in the new environment (i.e. Nucleotide sequence analyses have indicated that the virus local vectors and hosts) may differ from those described in was probably introduced from Indonesia to Papua New areas endemic for the particular virus. Guinea (PNG) (63), and then from PNG to Australia (64, 120). There is serological evidence that JEV has been present in PNG since at least 1989 (62). Indications of gene flow between populations of Cx. annulirostris in PNG, Rift Valley fever the Torres Strait and Cape York has provided evidence of As previously described, RVF is capable of colonising virus dispersal between these areas, while entomological several different bioclimatic areas. The virus has been studies demonstrating the long distance transport of isolated from 16 arthropod species (twelve of which are Cx. annulirostris by high altitude winds have suggested a suspected or confirmed RVF vectors), representing five mechanism for the spread of the virus (74, 121). Although genera (99) (Table I) (34, 42, 57, 71, 72, 75, 82, 85, 90, waterbirds or frugivorous bats could have introduced JEV 98, 130, 151, 167). The extensive distribution of the virus into Australia (65), the most likely hypothesis is that the can be explained by the large number and diversity of virus was periodically transmitted by wind-blown potential vectors. mosquitoes (Fig. 3) (47, 48, 121). Similar epidemiological processes may be associated Unlike JEV, vector-borne dispersion of WNF and RVF is with outbreaks of RVF in different countries. For example, unlikely over long distances because WNF and RVF vectors in Saudi Arabia the transmission dynamics of RVF were (most commonly mosquitoes of the order Diptera, family similar to those observed in the Horn of Africa. Namely, Culicidae) have a short active flight capacity (1-2 km) and a heavier than usual rainfalls, leading to the flooding of large bioecology that does not involve wind-borne dispersion. areas of crops, resulted in the mass hatching of Aedes eggs. Long-distance wind-blown dispersion has been described for Aedes vexans was thought to be the main vector in the vectors from other families of the order Diptera, e.g. transmission of the disease, while Cx. tritaeniorhynchus was bluetongue disease (BT), a non zoonotic arthropod-borne believed to have acted as a secondary vector (72, 101). disease that is disseminated by Culicoides biting midges When the rainfall stopped, the Aedes population (Diptera: Ceratopagonidae). Bluetongue virus was spread decreased, however, the number of Culex remained high from Sardinia to Corsica by Culicoides imicola (33) and from and continued to transmit the virus. Because RVF had not Indonesia to northern Australia by exotic Culicoides (38). existed previously in Saudi Arabia (72), the host

Papua New Guinea

Torres Strait Australia

0 100 200 Km.

Cape York

Fig. 3 Wind-borne dissemination of Japanese encephalitis by mosquitoes from Papua New Guinea to Australia Rev. sci. tech. Off. int. Epiz., 23 (2) 543

Table I Table II Potential vectors of Rift Valley fever West Nile virus infected arthropods identified in field studies (55) Countries Species References Mosquitoes Ticks Egypt Culex pipiens (59, 98, 131) Saudi Arabia Cx. tritaeniorhynchus (73) Aedes richardii Deinocerites Amblyomma Senegal Aedes vexans (43, 168) aegypti Culex cancer variegatum Egypt Ae. caspius (152) africanus antennatus Mimomya Argas Senegal Ae. ochraceus (43, 168) albocephalus decens group hispida hermanni Senegal Cx. poicilipes (35) albopictus erraticus lacustris Dermacentor Senegal Ae. dalzieli (43, 99) albothorax ethiopicus splendens marginatus Kenya Ae. cumminsii (83, 94) cinereus guiarti Ochlerotatus Hyalomma Kenya Ae. furcifer (83, 94) circumluteolus modestus atlanticus detritum Kenya Ae. mcintoshi (83, 94) juppi + caballus neavi atropalpus marginatum Kenya Cx. zombaensis (86) madagascarensis nigripalpus canadensis Ornithodoros Kenya Ma. africana (86) vexans nigripes cantans capensis South Africa Cx. zombaensis (70) Aedomya perexiguus cantator Rhipicephalus South Africa Ae. unidentatus (70) africana perfuscus group caspius muhsamae South Africa Ae. circumluteolus (76) Anopheles pipiens excrucians turicanus South Africa Ae. dentatus (70) atropos poicilipes japonicus barberi pruina sollicitans brunnipes quinquesfasciatus taeniorhynchus population was naive, which resulted in a particularly coustani restuans triseriatus severe outbreak (3, 132). crucians?bradleyi salinarius trivittatus maculipalpis scottii tormentor West Nile fever maculipennis tarsalis signifera punctipennis territans Psorophora West Nile fever appears to be ubiquitous, affecting rural, quadrimaculatus theileri ciliata e.g. South Africa (70) and urban areas, e.g. New York and subpictus tritaeniorhynchus columbiae Bucharest, as well as a variety of climatic zones including walkeri univittatus ferox arid areas, e.g. Algeria and Morocco, temperate areas, Coquillettidia vishnui group Uranotaenia e.g. Romania (cool) and Italy and France (warm), and metallica weschei sapphirina tropical and subtropical areas, e.g. Guadeloupe (115) and Florida (Fig. 4). Several arthropod species have been microannulata Culiseta described as potential WNV vectors (55) (Table II). perturbans inornata

In Europe, the virus has been isolated from eight mosquito the widespread distribution and ability of WNV to exist in and two hard tick species (9, 15, 28, 40, 49, 50, 60, 78, a variety of ecosystems. 87, 129, 150, 160), while in Senegal no less than 83 virus strains have been isolated from 12 arthropod species (147). In 2000, horses infected with WNV were detected in The virus has been isolated from two additional species of periurban areas (27) in the south of France mosquitoes in South Africa (70). More recently, 15 species (Camargue region). West Nile virus was believed to have of insects in the USA have been identified as suspected or been introduced into the wetland areas of France where confirmed vectors of WNV (43, 152, 160). migratory birds nested and mosquito densities were high. A cycle of low level transmission between wild aquatic Regarding the host population, WNV has been isolated birds and marsh mosquitoes (i.e. Cx. modestus) was from a large number of vertebrates, primarily of the avian suspected in the maintenance of the virus in wet land species. In Europe, infection has been detected in at least areas. Sedentary domestic birds, such as sparrows, may 21 wild aquatic and terrestrial bird species (58); ten of have contributed to the spread of WNV to periurban and which were capable of producing subsequent experimental urban areas where other vector species (i.e. Cx. pipiens) infection in European mosquitoes (59). In South Africa, were capable of transmitting the disease (27). 30 avian species have been identified as hosts of WNV (70), while in the USA, WNV infection has been In North America the epidemiological picture is, however, documented in 138 different species of birds (25). The completely different. Since being detected for the first time great diversity of potential hosts and vectors may explain in New York in the summer of 1999 (19), the virus has 544 Rev. sci. tech. Off. int. Epiz., 23 (2)

0 1000 2000 Km.

Fig. 4 West Nile virus circulation in the world since 1960 rapidly spread. There were 62 cases in six counties in able to feed on both humans and birds, thereby facilitating 1999, 21 cases in ten counties in 2000 (94) and 66 cases transmission of the virus to humans. ‘Associated with a in 359 counties (27 states) in 2001 (24). In 2002, more highly susceptible avian population and a high human than 4,000 human cases were recorded and the virus was density, this bridge-vector might have lead to the explosion detected along the Atlantic coast from Maine to Florida, of the disease in the USA’ (41). Except for a few reports in inland to eastern North Dakota, and in Canada (18). the south of Europe, this hybrid species has not been detected in European countries The extensive spread of WNV throughout North America was first attributed to the infection of an immunologically – Saint Louis encephalitis virus is widespread in the USA naive population with a particularly virulent viral strain. (52) and has close antigenic relatedness to WNV. Initially, However, phylogenetic analyses revealed that the strain American authorities had hoped that antibodies produced isolated from the 1999 New York outbreak was the same as in response to SLEV would cross-react with WNV and that responsible for the Bucharest and Volgograd outbreaks reduce the impact of the disease (58, 145). Unfortunately, and had a strong similarity to the Israeli strain (113). this existing cross-immunity did not prevent WNV dissemination These different epidemics also had several epidemiological – WNV was probably imported from the USA to the Neo- components in common. For example, urban areas were tropics and Central America (previously WNV-free areas) by highly infected, Cx. pipiens was identified as the main migrating birds without causing large numbers of equine vector, nervous signs were reported in a large number of cases or significant avian mortality (10, 23, 36, 76, 116). human cases and mortality rates for human infections were high (19, 22, 113, 129, 150, 157, 159). However, despite these similarities, the European outbreaks were sporadic Japanese encephalitis and located in areas near wetlands or river deltas (104), while in North America, the virus spread rapidly across the Vector and host diversity can also often explain the USA and into adjacent countries. Likewise, a high extensive distribution of JE (126, 127). However, despite mortality rate in wild and domestic avifauna was recorded the Australian mainland having the mosquito vectors in America, but not in Europe (24, 37, 129). The reasons (Cx. annulirostris and Cx. gelidus) and vertebrate hosts (feral for these differences are still not clear and the results of and domestic pigs and wild birds) suitable for the recent studies confirm the complex epidemiology of WNV: establishment of JE (30, 92), several studies have demonstrated a failure of the virus to become endemic in – Fonseca et al. showed that in northeastern USA a large this area (154, 156). This failure has been attributed to proportion of Cx. pipiens were actually a hybrid species several factors, such as: Rev. sci. tech. Off. int. Epiz., 23 (2) 545

– the presence of dead-end hosts, such as wallabies and (133). The wide geographic distribution of each of these tick cattle (73, 92) species can be attributed to: – the co-circulation of flaviviruses which are genetically – the ecological adaptability of the tick species similar to JEV and provide cross-protection to infection with JEV (92) – the dissemination of ticks that are in the immature – the long distances between pig breeding farms and stages of development through the movement of local birds residential areas (unlike the Torres Strait where the close – the ability of adult ticks to parasitise numerous proximity of pig breeding farms and residential areas may domestic animals (56). have contributed to the outbreaks in this area) (48, 155, 156). The number of potential hosts for CCHF is high and reflects the diverse feeding preferences of the immature Variations in the transmission of JEV, based on and adult tick vectors. Antibodies against CCHF virus have observations from several study sites in India, were been detected in domestic and wild animals including attributed to differences in the availability of pigs and hares, hedgehogs, rodents, chiropters, and large mammals alternative hosts (117). such as giraffes and rhinoceroses. On each continent dozens of bird species serve as hosts to the nine or ten Crimean-Congo haemorrhagic fever species of ticks which feed on birds during their immature stages of development. Despite the observation that the Crimean-Congo haemorrhagic fever virus is present in over level of viraemia in birds is usually low to unnoticeable, it 30 countries which are situated in a range of ecologically has been shown that the virus can be replicated and diverse regions (Fig 5). The virus has been isolated from transmitted by infected birds (166), suggesting that the 28 species and sub-species of hard ticks, comprising seven role of birds in the epidemiology of the virus is two-fold genera, each of which may contribute differently to the (i.e. transportation of infected ticks and local/long distance transmission, amplification and maintenance of the virus dissemination of the virus by infected birds).

Countries at risk

0 1500 3000 Km. Countries in which CCHF virus has been isolated

Fig. 5 Countries in which Crimean-Congo haemorrhagic fever virus has been isolated and countries at risk of infection Source: WHO website http://www.who.int/csr/disease/crimean_congoHF/en/ 546 Rev. sci. tech. Off. int. Epiz., 23 (2)

Lastly, the virus may be maintained in tick populations continents, such as North America where authorities have during inter-epizootic periods through several demonstrated that the main Culicidae species are potential mechanisms, such as trans-stadial and trans-ovarial RVF vectors (128). transmission, sexual transmission and the co-feeding of ticks aggregated on the same host (17, 45, 84). West Nile fever The epidemiology of WNF varies between continents. Tropical endemic regions are likely to be protected by Discussion and future strong host immunity; however, Africa and Asia must not be considered out of danger, as perturbations in the fragile expectations equilibrium between host susceptibility, vector challenge and the virus may result in disease outbreaks. The impact The transmission of arthropod-borne zoonoses is only of WNV in the USA emphasises the importance of partially described for endemic areas and largely recognising the devastating potential of diseases which are undocumented in areas that have recently become often considered to be of minor importance. In addition, infected. Hypotheses on the epidemiological processes of the incredible expansion of WNF in the USA has proven four current emerging arboviruses, i.e. RVF, WNV, JEV and that even the most industrialised countries in the world are CCHF virus, with particular emphasis on the impact of at risk when a new pathogen is introduced. Whether WNV ecological and human-induced environmental changes on in the USA will achieve an ecological equilibrium vector abundance and/or distribution and vectorial resembling that of SLEV is unknown. In Europe, it is not capacity (VC), have been summarised in this paper. known whether the outbreaks of WNV in the 1990s were Due to the long distance transport of these viruses by due to new epidemiological processes or part of normal vectors and hosts, entire countries or even continents may long term cycles. It is assumed that the virus can persist remain uninfected. Interestingly, the number of potential silently for long periods of time within the European vectors for RVF or WNF is higher than for other ecosystems. West Nile virus circulation has been regularly arboviruses, which may explain the ability of these viruses recorded in various eastern European countries. to colonise new areas. Immediate establishment of a virus in a novel ecosystem may occur under favourable Japanese encephalitis conditions, e.g. RVF in Saudia Arabia, while in other ecosystems new transmission cycles may develop involving Several of the epidemiological features of Japanese local hosts or vectors, e.g. Camargue, France. encephalitis remain unknown, such as: – the overwintering mechanism Rift Valley fever – the genetic variability of the virus – the potential role of vectors such as Cx. quinquefasciatus, In view of the changes in distribution of RVF that have whose breeding sites include the waste-waters of taken place over the last few decades, it can be assumed both urban environments and industrialised swine- that the northernmost territories of Africa and the breeding areas. Middle East are threatened by the disease. Its major vectors are already present in the Maghreb (i.e. a region located in Due to the diversity of breeding sites utilised by the northern part of the continent of Africa that includes Cx. quinquefasciatus, potential exists for this species to Morocco, Tunisia, Algeria, Libya and Mauritania) where become a bridge-vector between swine production areas host densities are high and transboundary animal and urban areas. movements are intense, especially before the Aïd-el-Kebir period (i.e. an Islamic religious holiday celebrated with the The geographical distribution of JE is continuing to sacrificing of a sheep). The evolution (i.e. whether or not expand, promoted by a number of factors that include: the disease will become endemic) of the RVF outbreak that – favourable ecological conditions (i.e. the cultivation of occurred in Saudi Arabia in 2000, is still uncertain. vast rice fields) Furthermore, the risk for neighbouring countries (Jordan, Iraq, etc.) needs to be evaluated. Such risk management is – significant vector populations (i.e. Cx. tritaeniorhynchus) a high priority considering the direct and indirect in countries such as Pakistan, Afghanistan and Iran economic impacts (i.e. the cost of trade bans between the – the widespread presence of the main avian host of JE, Horn of Africa and the Arabic Peninsula has been the heron Nycticorax nyctycorax. Nycticorax nyctycorax can estimated to be between US$50 and US$75 million per be found from Japan to the Middle East, in northern Africa, year), and the dramatic social consequences for local and even on the American continent, where rice is widely people, associated with a disease outbreak (108). Rift cultivated and several species of potential mosquito vectors Valley fever may also be a potential threat to other are present (118). Rev. sci. tech. Off. int. Epiz., 23 (2) 547

Crimean-Congo haemorrhagic fever animals originated. While routes taken by migrating birds are well-known, nothing is known about the ability of the Africa swine fever virus was first introduced from Africa into associated pathogens to reach and colonise new areas. the Americas in the 1960s and 1970s. Although this virus is not zoonotic, this event demonstrates that tick-borne viruses Lastly, genetic evolution of viruses or vectors is may jump between continents, suggesting that CCHF may uncontrolled and unpredictable. Modelling techniques continue to spread and colonise new areas (105). Several have proposed several possible patterns for the co- reported nosocomial outbreaks (i.e. Dubai 1979, South evolution of viruses and hosts. However, although Africa 1984, Pakistan 2002, Mauritania 2003) attest to the mathematical approaches can provide some constructive highly contagious nature of the CCHF virus, making it results, they are often insufficient in predicting outcomes probably one of the most dangerous viruses to manipulate because viral emergence and host interactions are (56, 128, 153) and one of the research priorities for the next stochastic and dependent on both the hosts’ genetics and few decades. external conditions.

Given the lack of disease knowledge, the ability of pathogens to move across boundaries and the absence of Conclusion available vaccines such as in the case of RVF, WNV and The reasons for the recent and dramatic emergence and CCHF, the control of these diseases may not be possible in re-emergence of arboviral diseases are multifactorial and the future. only partly understood. Several factors are involved in the recent changes in the distribution of arthropod-borne Therefore, more parameters will need to be added to the diseases. Demographic and social changes, such as poverty models in order to optimise the prediction and control of or uncontrolled urbanisation, will probably be some of the emerging zoonoses. The most pressing needs are: most important challenges in the control of arboviruses over the next few decades. Massive cities in the tropics, – to further understand the epidemiological mechanisms with their lack of sanitary measures, serve as incubators for that allow interepizootic persistence emerging zoonoses and represent one of the greatest risk – to understand the role of amplifying hosts in the spread factors in the transmission of zoonotic diseases in the next of diseases century (105). – to identify the key environmental factors involved in Climatic factors are also of great importance in the outbreaks transmission of vector-borne zoonotic diseases. The four – to implement a large scale monitoring system. disease examples discussed in this paper demonstrate how some elements of the disease transmission cycle, notably The rapid distribution of information and an improved the vector population dynamics, are affected by climatic coordination between countries will be essential to monitor parameters. The ‘basic reproduction number’ and its these diseases. Moreover, in the field of zoonoses, related concept, VC, can be used to simulate the surveillance and research on human and animal health transmission risk and provide a relative indicator of the should go hand in hand. The concept of ‘one medicine’ impact of different climatic scenarios on the proposed by Calvin Schwabe (112) needs to be developed transmissibility of vector-borne diseases. Vectorial capacity and applied. To summarise, there is an urgent need to is determined by the complex interactions between hosts, implement a global information and monitoring network vectors, pathogens and environmental factors (39). Several that would supply models with field data, allow scientists bio-climatic models are currently being implemented, and authorities to assess the risk of disease outbreaks in time some of which have already proved useful in predicting and space, and strengthen the surveillance of emerging outbreak occurrences. However, although helpful in our zoonotic diseases (risk-based surveillance). Most understanding of transmission dynamics, and useful as a importantly, a fully integrated approach is essential in order tool in specific situations, some authors (123) believe that to adequately control emerging infectious diseases (46). the existing models have a limited value for assessing the impact of long-term climate changes on disease transmission.

Nevertheless, because outbreaks may occur in the absence of climatic events, other parameters must also be considered. Transboundary animal movements play a key role in the long distance dissemination of pathogens. Some of these movements are illegal and usually little is known about the serological status of the countries from which the 548 Rev. sci. tech. Off. int. Epiz., 23 (2)

Les processus épidémiologiques dans l’émergence de maladies à transmission vectorielle (fièvre West Nile, fièvre de la Vallée du Rift, encéphalite japonaise et fièvre hémorragique de Crimée-Congo)

V. Chevalier, S. de la Rocque, T. Baldet, L. Vial & F. Roger

Résumé Durant les dernières décennies, la distribution géographique des maladies à transmission vectorielle s’est considérablement étendue. Si l’influence des changements anthropogènes ou écologiques sur les risques d’épidémie est indubitable, plusieurs hypothèses ont été émises pour tenter d’expliquer la réémergence de ces maladies ainsi que l’établissement et la propagation de ces virus dans des zones autrefois épargnées. Les déplacements de l’hôte et du vecteur jouent un rôle important dans la dissémination des agents pathogènes. La capacité de ces maladies à coloniser des zones non contaminées peut s’expliquer par la diversité des hôtes et des vecteurs, l’existence de conditions écologiques favorables et la faculté d’adaptation des vecteurs et des agents pathogènes aux nouveaux écosystèmes. Cet article a pour objet de décrire les processus épidémiologiques intervenant dans l’émergence ou la réémergence des maladies à transmission vectorielle, à savoir la fièvre de la Vallée du Rift, la fièvre West Nile, l’encéphalite japonaise et la fièvre hémorragique de Crimée-Congo.

Mots-clés Dissémination – Diversité – Encéphalite japonaise – Fièvre de la Vallée du Rift – Fièvre West Nile – Fièvre hémorragique de Crimée-Congo – Maladie émergente – Processus épidémiologique – Vecteur. Rev. sci. tech. Off. int. Epiz., 23 (2) 549

Procesos epidemiológicos que intervienen en la aparición de enfermedades transmitidas por vectores: fiebre West Nile, fiebre del Valle del Rift, encefalitis japonesa y fiebre hemorrágica de Crimea-Congo

V. Chevalier, S. de la Rocque, T. Baldet, L. Vial & F. Roger

Resumen De unos decenios a esta parte, el número de zoonosis transmitidas por artrópodos ha crecido espectacularmente. Los cambios antropogénicos o ecológicos tienen una influencia innegable en el riesgo de brote. Sin embargo, se han formulado pocas hipótesis para explicar el resurgimiento de dichas enfermedades, la propagación de los virus a zonas previamente libres de ellos y su asentamiento en esas zonas. Los desplazamientos de los anfitriones y vectores influyen sobremanera en la propagación de un patógeno, y tal vez la capacidad de esas enfermedades para colonizar áreas hasta entonces indemnes se explique por la diversidad de anfitriones y vectores, la presencia de condiciones ecológicas favorables y la eficaz adaptación de los vectores o patógenos a nuevos ecosistemas. El autor describe los procesos epidemiológicos de una serie de enfermedades transmitidas por vectores: la fiebre del Valle del Rift, la fiebre West Nile, la encefalitis japonesa y la fiebre hemorrágica de Crimea-Congo.

Palabras clave Diseminación – Diversidad – Encefalitis japonesa – Enfermedad emergente – Fiebre hemorrágica de Crimea-Congo – Fiebre del Valle del Rift – Fiebre West Nile – Proceso epidemiológico – Vector.

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