African Horse Sickness: Transmission and Epidemiology Ps Mellor

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African horse sickness: transmission and epidemiology Ps Mellor

To cite this version:

Ps Mellor. African horse sickness: transmission and epidemiology. Veterinary Research, BioMed Central, 1993, 24 (2), pp.199-212. hal-00902118

HAL Id: hal-00902118 https://hal.archives-ouvertes.fr/hal-00902118 Submitted on 1 Jan 1993

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African horse sickness: transmission and epidemiology

PS Mellor

Institute for Animal Health, Pirbright Laboratory, Ash Road, Pirbright, Woking, Surrey, UK

(Received 29 June 1992; accepted 27 August 1992)

Summary ― African horse sickness (AHS) virus causes a non-contagious, infectious, arthropod- borne disease of equines and occasionally of dogs. The virus is widely distributed across sub- Saharan African where it is transmitted between susceptible vertebrate hosts by the vectors. These are usually considered to be species of Culicoides biting midges but mosquitoes and/or ticks may also be involved to a greater or lesser extent. Periodically the virus makes excursions beyond its sub-Saharan enzootic zones but until recently does not appear to have been able to maintain itself outside these areas for more than 2-3 consecutive years at most. This is probably due to a number of factors including the apparent absence of a long term vertebrate reservoir, the prevalence and seasonal incidence of the vectors and the efficiency of control measures (vaccination and vector abatement). The recent AHS epizootics in Iberia and N Africa spanning as they do, 5 or more yr, seem to have established a new pattern in AHS virus persistence. This is probably linked to the continuous presence of adult C imicola in the area. Culicoides imicola is basically an Afro-Asiatic insect and prefers warm climates. Therefore its continuous adult presence in parts of Iberia and N Africa may be due to some recent moderations of the climate in these areas.

African horse sickness / transmission / epidemiology

Résumé ― La peste équine : transmission et épidémiologie. Le virus de la peste équine provo- que chez les équins et occasionnellement chez le chien, une maladie infectieuse non contagieuse, transmise par des arthropodes. Ce virus est largement réparti au Sud du Sahara où il est transmis aux hôtes vertébrés sensibles par des vecteurs. On a l’habitude de considérer que ceux-ci sont des moucherons piqueurs (Culicoides) mais des moustiques et/ou des tiques peuvent être également impliqués dans une plus ou moins grande mesure. Périodiquement, le virus fait des apparitions au- delà des zones enzootiques sub-sahariennes mais pendant longtemps il n’a pas réussi à se mainte- nir en dehors de ces zones pendant plus de 2-3 ans consécutifs. Ce fait est probablement dû à de nombreux facteurs mais en particulier à l’absence apparente d’un réservoir de vertébrés de longue durée chez les vertébrés, à la prévalence et à l’incidence saisonnière des vecteurs et à l’efficacité des mesures de contrôles (vaccination et réduction des vecteurs). Les épizooties récentes de peste équine dans la péninsule ibérique et en Afrique du Nord, qui se sont étendues sur 5 ans ou plus, semblent avoir établi un nouveau modèle de persistence du virus. Ceci est probablement dû à la présence permanente d’adultes de C imicola dans cette zone. C imicola est un insecte localisé es- sentiellement en Afrique et en Asie et qui préfère les climats chauds. La présence permanente d’adultes dans certaines parties de la péninsule ibérique et en Afrique du Nord pourrait s’expliquer par une modification récente du climat dans ces régions. peste équine / transmission / épidémiologie INTRODUCTION which occurred in 1327 (Mouie. 1896). However despite this early record the virus group appears to have originated in Africa African horse sickness (AHS) virus is a and was first as a distinct dis- double stranded RNA virus which causes recognised ease entity there subsequent to the intro- a non-contagious, infectious, arthropod- duction of breeds of borne disease of equines. The disease is highly susceptible characterised by clinical signs which de- equine during the exploration of Central Af- rica. The earliest account comes from East velop as a result of the impaired function In of the circulatory and respiratory systems Central Africa in 1569 (Theal, 1899). southern Africa the disease has been rec- giving rise to serous effusions and hae- since the of the morrhage in various organs and tissues ognised occupation Cape (Howell, 1963). The extent and severity of of Good Hope by the Dutch East India at the of the l8th cen- the clinical signs caused by AHS virus are Company beginning frequently used to classify the disease into tury when large numbers of deaths occurred in horses 4 distinct forms. In increasing order of se- imported (Henning, 1956). verity these are horse sickness fever, the However, it was not until 1900 that subacute or cardiac form, the cardio- M’Fadyean using samples of infected pulmonary or mixed form and the peracute horse blood showed that the agent of or pulmonary form. Comprehensive ac- horse sickness fever was able to pass counts of the clinical signs, pathogenesis through bacterial filters and concluded that and pathology caused in equines by AHS it was an &dquo;ultravisible&dquo; virus. Theiler in a se- virus have been published by Rafyi (1961), ries of experiments covering several years Howell (1963), Erasmus (1973), Mircham- (1908, 1915 and 1921) then recognised sy and Hazrati (1973) and Lubroth (1988). that AHS virus existed as a number of anti- AHS virus exists as a number of distinct genically distinct strains but not until 1962 serotypes and to date 9 have been inter- were the 2 most recent internationally ac- nationally recognised. Animals recovering cepted serotypes (8 and 9) identified and from an infection with any one of these characterised (Howell, 1962). The isolation serotypes develop a solid immunity to it of an additional strain of AHS virus in Ken- but may continue to be susceptible to het- ya (G-75), that apparently is not neutral- erologous serotypes (Anonymous, 1978). ised by antisera to any of the 9 recognised Since under natural conditions AHS vi- serotypes, suggests that a further serotype rus is transmitted between its vertebrate should now be added to the internationally hosts virtually exclusively by the bites of recognised list (Davies and Lund, 1974; various species of haematophagous ar- Davies, 1976). thropods its distribution is limited to those geographical areas where competent vectors are present and to those times of the GEOGRAPHICAL DISTRIBUTION year when conditions are favourable for AND OCCURRENCE vector activity. AHS virus is widely distributed across sub- Saharan Africa and is enzootic in a band HISTORY stretching from Senegal and Gambia in the west to Ethiopia and Somalia in the east Probably the first historical reference to (Howell, 1963). It also occurs as far south AHS concerns an epizootic in the Yemen as S Africa and may extend at times to Egypt in the north. The Sahara desert, Africa and appeared in southern Morocco, however, provides an effective geographi- rapidly extending into Algeria and Tunisia cal barrier which usually, though not invari- and eventualy crossing the Straits of Gi- ably, prevents incursions into North and braltar into southern Spain in October NW Africa from the infected areas further 1966 (Rabah, 1966; Diaz Montilla and south. Panos Marti, 1967, 1968; Mornet et al, Until relatively recently AHS virus was 1967; Sers, 1967; Laaberki, 1969). The ep- believed to be confined to Africa with the izootic once more was caused by AHS virus 9 Montilla and Panos exception of occasional excursions across serotype (Diaz the Red Sea into SW Arabia (Rafyi, 1961; Marti, 1968). Pilo-Moron et al (1969) re- Mirchamsy and Hazrati, 1973). However, garded the appearance of AHS in N Africa in the summer of 1959 the situation as being due to the movement of nomads changed. Horse sickness fever appeared and their animals, particularly donkeys first in Saudi Arabia and the southern re- across the Sahara from Central Africa gions of Iran, and then spread northwards, where AHS virus serotype 9 was apparently eastwards and westwards to involve Af- enzootic (Maurice and Provost, 1967). The ghanistan and Pakistan by the autumn of 1965-1966 epizootic succeeded in &dquo;over- 1959. During the spring and summer of the wintering&dquo; once in N Africa but the northern following year the disease continued to extension into southern Spain was eliminat- spread, particularly along the courses of ed within 3 wk apparently through a vigor- the great rivers which formed the major ous vaccination and slaughter policy (Diaz trade routes, its progress being facilitated Montilla and Panos Marti, 1968). by the movements of nomadic tribesmen Subsequent to 1966 AHS virus appar- and their animals (Howell, 1960). Syria, ently remained quiescent in sub-Saharan Lebanon, Jordon, Iraq, Turkey, Cyprus and Africa for over 20 yrs. However, in 1987 an extensive tracts of India were rapidly in- outbreak of AHS due to serotype 4 was volved all within the next 6 months (How- confirmed in the provinces of Madrid, Tole- ell, 1960, 1965; Rafyi, 1961; Gorhe et al, do and Avila in Central Spain (Lubroth, 1965; Mirchamsy and Hazrati, 1973). How- 1988). The origin of the outbreak is be- ever, by the end of 1961 in the face of a lieved to have been the importation of 10 massive vaccination campaign and the zebra from Namibia, 5 of which were taken deaths of over 300 000 equines the dis- to a Safari Park (El Rincon) 50 km SW of ease in Asia apparently came to a halt (An- Madrid. This safari park subsequently be- war and Qureshi, 1972). This was probably came the site of the first 27 cases of AHS due to a combination of factors including in Spain the first signs being detected on adverse climatic conditions, vector abate- July 22nd and 23rd some 26 d after the ar- ment campaigns, vaccination and the virtu- rival of the zebra (Lubroth, 1988; Mellor et al depopulation of susceptible equines al, 1990b). The epizootic continued for 3-4 over much of the area. The virus responsi- months in central Spain, the last officially ble for the epizootic was identified retro- recorded death being in mid-October 1987 spectively, from isolations made in Paki- by which time 146 equines had died and India and several Middle Eastern stan, over 38 000 had been vaccinated (Anony- as AHS virus 9 countries, serotype (How- mous, 1987; Diaz Yubero, 1987). Unfortu- ell, 1962; Shah, 1964; Rabah, 1966; Sers, nately in October 1988 almost a year after 1967; Mornet et al, 1967). the last reported death, a recrudescence of In 1965 AHS again spread beyond its AHS due to serotype 4 was confirmed in traditional enzootic zones in sub-Saharan the south of Spain at Sotogrande in Cadiz. Later the same month the disease spread theatre it is worthwhile recording that for into the neighbouring Province of Malaga. the first time since 1959 AHS has also Official records indicate that 156 equines been reported in Saudi Arabia, where AHS died either directly or indirectly due to virus serotype 9 was isolated from clinical AHS, the last reported death being in early cases in the SW, Abha Region in 1989 December (Rodriguez et al, 1989). Then at (Mellor et al, 1990a). Further information the end of July in 1989 AHS once more concerning the extent of this outbreak is broke out at Sotogrande, the disease be- apparently not available. ing confirmed by laboratory findings in early August (Anonymous, 1989a). In rapid succession cases also occurred in the TRANSMISSION provinces of Huelva, Cordoba and Seville in Andalucia, and in Extramadura. Badajoz AHS virus had long been thought to be This time the disease did not at inter- stop transmitted by biting arthropods and suspi- national boundaries and during September cion has at one time or another fallen on a into the southern 2 spread Portuguese wide variety of species and genera. As provinces of Baixo Alentejo and the Al- early as 1903, Pitchford-Watkins and and then in October cases also oc- gave, Theiler suggested that Anopheles mosqui- curred in and Larache in Tetouan, Tanger toes could be involved. In 1912 Schuberg It Morocco (Anonymous, 1989b, 1990a). and Kuhn showed that Stomoxys calci- has been estimated that some altogether trans is capable of transmitting the virus 2 000 equines died in these 3 countries mechanically (ie without replication of the during 1989 (Mellor, 1991). In September virus in the vector). However, the impor- 1990 for the 4th successive AHS due year tance of this method of transmission was to 4 was confirmed in serotype Spain (Mal- later discounted because S calcitrans is a and caused the deaths of a further 66 aga) daytime feeder and it was found that con- the last case equines, positive being diag- fining horses in mosquito proof stables at nosed in November (Anonymous, 1990b). night protected them against the disease In Morocco in 1990 AHS was detected in 6 (Theiler, 1915). Williams (1913) in the ab- Provinces with the loss of some 555 sence of other haematophagous insects however the virus did not equines, appar- during outbreak of AHS in the Sudan con- recrudesce in ently Portugal (Anonymous, sidered Lyperosia minuta to be a likely In 1991 remained free 1992). Portugal vector. Van Saceghem (1918) suspected from the disease and Spain also reported ticks and Tabanids, and Carpano (1931) no cases but the virus continued its pro- suggested Anopheles, Aedes, Phleboto- Morocco some gression through involving mus and Simulium as possible carriers. 20 provinces and extending for the first However, Nieschulz et al (1934) and Nies- time south of the Atlas mountains (Anony- chulz and Du Toit (1937) after a careful mous, 1992). At the time of writing in early study of the mosquito fauna at Onderste- 1992 it remains to be seen whether further poort (S Africa) concluded that mosquitos recrudescences of AHS will occur either in are not vectors of horse sickness. These Morocco or in neighbouring Maghreb coun- workers did record the survival of AHS vi- tries in view of the oc- though widespread rus in some mosquitoes for up to 27 d but currence of the disease 1991 this during despite numerous attempts they were nev- would seem to be not unlikely. er able to transmit the virus by mosquito Separate from the incursion of AHS vi- bite. Then in 1944 came something of a rus serotype 4 into the Mediterranean breakthrough when Du Toit showed that wild caught Culicoides species were infect- infected with the ’released virus’ which ed with AHS virus and later in 1945 (quot- they were subsequently able to transmit to ed in Wetzel et al, 1970) he succeeded in susceptible hosts. ’Showering’ is a phe- transmitting the virus by Culicoides bite nomenon described by Luedke et al (1977) from an infected to a susceptible horse 122 and Jones et al (1981) whereby the bites d after the insects infecting blood meal. of a vector species of Culicoides (C varii- This was the first definitive demonstration pennis) were purported to stimulate re- of the biological transmission of AHS virus lease of bluetongue (BT) virus from an by any species of arthropod. Since that unknown, extra-vascular depot into the time AHS virus has been regarded by most blood stream of a bull ’latently’ infected workers primarily as a Culicoides-borne vi- with the virus. Presumably it is envisaged rus. However, the situation is far from be- that such a mechanism would be triggered ing clear-cut and in more recent times a by factor(s) in the saliva of the vectors, variety of reports have been published possibly in association with a degree of dealing with mosquitoes and ticks, in addi- host stress. However, considerable doubt tion to Culicoides, as potential or actual has recently been cast upon the validity of vectors of AHS virus. this earlier work and the whole BT virus showering phenomenon (Osburn, 1988; Walton, 1991 ). In the light of this it might Mosquitoes be prudent to critically re-evaluate the apparent existence of a similar mechanism in with AHS virus. Ozawa and Nakata (1965) and Ozawa et dogs &dquo;latently&dquo;infected al (1966a, b, 1970) recorded the success- ful transmission of AHS virus to horses via the bites of artificially infected Anopheles Ticks stephensi, Culex pipiens and Aedes aegypti. These authors found that virus repli- Salama et al (1979, 1980) isolated AHS virus 9 from 17% of 2 089 field cated only in a limited number of mosqui- serotype of dromadarii collect- toes allowed to engorge upon viraemic samples Hyalomma ed in it is not clear blood but transmission was demonstrated Egypt. Unfortunately from their work whether the viruses isolat- when refeeding these individuals at periods of between 15 and 22 d post infection ed originated from the tissues of the ticks or whether were (dpi). The maximum titres of virus recov- themselves, they present in the lumen, as a result of a re- ered from infected mosquitoes were never merely gut cent viraemic blood meal. Nevertheless significantly higher than the amounts in- the same authors also the gested but an eclipse phase apparently oc- reported presence of in curred just subsequent to infection and vi- AHS viruses newly emerged (ie adult ticks and succeeded in rus was recovered for up to 35 dpi. unfed) they Hussein (1982) and Abdallah (1983) also transmitting the virus via tick bite to camels and to horses. Infected ticks were considered the mosquito, C pipiens to be a reported biological vector of AHS virus, and follow- to retain virus for up to 10 wk post infection and trans-stadial but not transovarial trans- ing on from their work El-Husseini et al mission was recorded and (1986) reported that C pipiens was also (Dardiri Brown, able to induce &dquo;showering&dquo; of AHS virus 1989). from the spleens of latently infected dogs. Awad et al (1981) also suceeded in Subsequent batches of mosquitoes feed- transmitting AHS virus, serotype 9, from in- ing upon the same dogs thereby became fected to susceptible horses via the bites of adult H dromadarii. Clean ticks then be- persistently infected. Additional increases came persistently infected by feeding upon in virus titre failed to produce any change the viraemic horse. Trans-stadial transmis- in infection rate indicating that at an infect- sion from larvae to nymphs and from ing titre of 10s,0 logloMID50/0.02 ml the in- nymphs to adults was demonstrated but fection rate (IR) is equal to the susceptibil- once again transovarial transmission was ity rate (SR) (Mellor, 1990). No C not recorded. variipennis were persistently infected with AHS virus when the virus titre of the infect- Further studies in Egypt, by Salama et at (reported in Dardiri and Salama, 1988; ing blood meal was equal to or less than 104 ml. It is that Dardiri and Brown, 1989) showed that the iogioM!D5o/0.02 likely the failure of Kitaoka to record AHS brown dog tick Rhipicephalus sanguineus (1966) virus in was due. sanguineus is able to transmit AHS virus replication C puncticollis to his selection of a that is experimentally from infected dogs and species prob- to oral infection with the horses to healthy dogs and horses. Trans- ably insusceptible virus re- stadial transmission occurred from larvae (Mellor et al, 1981 The negative sults of Wetzel et al (1970) who were deal- to nymphs and from nymphs to adult but with an transovarial transmission was absent. ing apparently susceptible species of Culicoides may have been due to the low infecting titres of virus used in their ex- around Culicoides periments (ie, lo2-8MID50/0.03 ml) as compared to the minimum titres of 10’’o-1045M!Dg/0.02 ml found necessary Subsequent to Du Toit’s original work with by Mellor et al (1975). S African Culicoides in 1944 and 1945 no In 1985, Erasmus (personal communi- studies involving AHS virus and Culicoides cation; cited in Venter et al, 1991) reported species seem to have been published until the isolation of AHS virus serotypes 2, 4 the reports of Kitaoka (1966) using and 7 from field collected non-blood- C puncticollis and Wetzel et at (1970) us- engorged C imicola in S Africa and Black- ing C pallidipennis (= imicola). Both of burn et al (1985) also isolated AHS virus these studies failed to demonstrate either serotype 4 from non-blood-engorged C imi- AHS virus replication in Culicoides or cola in Zimbabwe. Apparently over the transmission by them. However, Boorman years numerous isolations of AHS virus et at (1975) and Mellor et at (1975) using have been made from wild-caught C imico- colonized C variipennis finally confirmed la in S Africa but none have been made Du Toit’s original work and demonstrated from other species of Culicoides or from for the first time that AHS virus is able to non-blood-engorged mosquitoes (Eras- replicate (by a factor of up to 10 000-fold) mus, personal communication, 1988). after oral ingestion by a species of Culi- However, recently Mellor et al (1990b) coides. These authors also showed that have reported several isolations of AHS vi- transmission could occur after 7-10 d in- rus serotype 4 from non-blood-engorged, cubation at 26 °C. Mellor et at (1975) fur- wild-caught Culicoides during the 1988 epi- ther showed that the infection rates of C zootic in Spain. While 4 of these isolations variipennis increased in a linear relation- were from C imicola 2 were from mixed ship with the titre of virus in the blood pools of Culicoides consisting mainly of C meal, to reach a peak at =05 10 loglo pulicaris and C obsoletus but excluding C (mouse infective dose) MID501°.02 ml imicola. The 2 isolations from ’other’ spe- when =35% of engorging midges were cies of Culicoides originated from insect catches in which C imicola were also mid-gut. The virus attaches to the luminal present, but on testing these proved to be surface of the mid-gut cells, infects these negative for AHS virus. There is therefore cells and replicates in them. Progeny virus clearly no possibility of AHS virus from in- is then released through the basement fected C imicola ’contaminating’ speci- lamina into the haemocoel from where the mens of other Culicoides species in the secondary target cells or organs, including same insect catch and consequently these the salivary glands, are infected. Subse- 2 isolations must be considered as being quent to virus replication in the salivary valid. The final AHS virus isolation from in- glands transmission may take place. Indi- sects reported by Mellor et al (1990b) vidual vectors once persistently infected came from a pool of blood-engorged mos- usually remain so for life. However, it quitoes. Its significance is therefore difficult should be remembered that not all female to interpret since the presence of virus insects within a vector species are neces- may merely reflect a recent viraemic blood sarily susceptible to infection with a partic- meal. However, the fact that mosquitoes ular arbovirus, or if infected are competent are clearly able to acquire AHS virus from to transmit that virus. A series of barriers or viraemic hosts in this way means that they constraints exists within certain individuals are potentially capable of transmitting it, ei- of a vector species which either prevent vi- ther biologically as Ozawa et al (1966a, b, rus infection or else restrict it in such a way 1970) suggested or possibly even mechan- as to prevent transmission. These refracto- ically. ry and susceptible traits within a vector are under control but the Futher studies dealing with detailed as- species genetic which are pects of the virogenesis of AHS virus in mechanisms by they expressed are as understood Culicoides are seemingly not yet available. yet poorly (Mellor, However, it is of relevance to note that 1990). those species of Culicoides which are either proven or suspect vectors of AHS vi- EPIDEMIOLOGICAL CONSIDERATIONS rus (C imicola, C variipennis, C obsoletus, C pulicaris) have also been implicated in the transmission of the related BT viruses Apart from the ingestion of virus contami- (Mellor et al, 1990b). In other words these nated meat by dogs (Van Rensburg et al, 2 virus groups have several vector species 1981; Hess, 1988) AHS virus is transmit- of Culicoides in common. Therefore it is ted in nature between its vertebrate hosts logical to suppose that many of the princi- virtually exclusively by the bites of certain ples expounded in the recent review by species of haematophagous anthropods. Mellor (1990) which deals with the replica- Its geographical distribution and seasonal tion of BT virus in Culicoides will find equal incidence is therefore limited not only by application to the replication of AHS virus the requirement for susceptible vertebrate in Culicoides. While it would be inappropri- hosts but also by the necessity for compe- ate to reiterate the detailed conclusions of tent arthropod vectors. In most circum- the BT paper here, the general cycle of stances it is the arthropod vector which is events that any arbovirus, including AHS the controlling factor. This is evidenced by virus, must follow through a competent in- the observations of most workers in the sect vector may be summarised as follows. field, who have shown that temperature Virus is ingested as part of a blood meal and moisture are the main factors deter- from a viraemic host and is deposited in mining the incidence of AHS (and the prev- the lumen of the hind part of the vector’s alence of the vectors) and that the disease disappears abruptly after the first frosts, tute an overwintering mechanism for BT vi- despite the continuing presence of large rus, particularly in those parts of its range numbers of susceptible vertebrate hosts where adverse climatic conditions curtail (Hess, 1988). Therefore since throughout vector activity for up to 2-3 months of the recorded history AHS has made periodic year. excursions its enzootic zones in beyond AHS virus conversely causes a much sub-Saharan Africa it follows that compe- briefer viraemia in its vertebrate hosts. tent vectors must also be anthropod This ranges from a maximum of 27 d in ze- present at least at certain times or sea- bra down to 18 d in the horse, although it sons in these epizootic areas. Indeed, both species it is usually much less (Eras- Sellers et al (1977) and Sellers (1980) mus et al, 1978; personal communication, have amassed a considerable amount of 1988). The duration of viraemia in donkeys convincing circumstancial evidence to sug- and mules has apparently not been deter- gest that the emergence of AHS from its mined with any degree of certainty but it enzootic zones may frequently be due to seems to be somewhat longer than in long range dispersal flights by infected horses, though less than in zebra (Eras- vectors travelling with the prevailing winds. mus, personal communication, 1988) while These authors infer flight ranges of up to in dogs it is usually considered to be transi- 700 km and consider that wind borne tory (Anonymous, 1978). Therefore in the infected vectors were the most likely absence of a long-term vertebrate reser- cause of the spread of AHS from Morocco voir and of transovarial transmission to Spain in 1966, from Turkey to Cyprus in through the vector, AHS virus will presum- 1969, and from Senegal to the Cape ably only be able to survive via continuous Verde Islands in 1943. However, until the and uninterrupted cycles of transmission recent series of epizootics in Spain, Portu- between its vertebrate and invertebrate gal and Morocco (1987-1991) AHS virus hosts, with no ’vector-free’ period being has apparently been unable to persist for greater than the maximum duration of vi- more than 2-3 consecutive years at most, raemia. In much of sub-Saharan Africa the beyond its traditional enzootic zones (Raf- climatic conditions are suitable for continu- yi, 1961; Gorhe et al, 1965; Bourdin, 1973; ous vector activity throughout the year. Un- Mirchamsy and Hazrati, 1973). At first der such conditions cycling of virus be- sight the reasons for this are difficult to tween vertebrate and invertebrate hosts determine, particularly in view of the fact will proceed without interruption and also that the related BT virus group, which util- without the need for an &dquo;unidentified verte- ises smilar vectors, has succeeded admir- brate reservoir&dquo;. Further north and south, ably in establishing itself apparently per- climatic conditions are likely to be less con- manently, across Asia, Australia and the ducive to continuous vector activity and an Americas (Mellor, 1990). However BT vi- annual ’vector-free’ period will occur. This rus has 2 major advantages. It infects ru- period will tend to occupy an increasing minants which are generally far more abun- portion of the year as distance from the dant than are equines and the viraemia it equator increases. When the length of the causes in some ruminant species, particu- vector-free period exceeds the duration of larly cattle, can be as long as 70-100 d viraemia in the local susceptible vertebrate (Nevill, 1971; Osburn et al, 1983). In the population AHS virus will be unable to per- absence of a true carrier animal or of sist and should it occur at all, will only do transovarial transmission in the vector this so in epizootic form. Such epizootics are extended period of viraemia could consti- likely to be a regular or annual event when the ’vector-free’ period is relatively short weather conditions, moving north in favour- and when AHS virus enzootic zones are able years and retreating south again dur- adjacent, but will be sporadic or occasional ing adverse conditions. At the moment we if the ’vector-free’ period is lengthy and have very little idea of the amplitude and should AHS virus enzootic zones be re- frequency of these variations or of the pre- mote. This latter is the situation which until cise environmental conditions that control recently seemed to apply to southern Eu- them (Mellor, 1987). However, in the con- rope and N Africa. However, the 1987- text of AHS virus persistence it is now 1991 epizootics in the area patently do not known that there are areas of southern fit into this pattern and the persistence of Spain and southern Portugal where C imi- AHS virus in the western Mediterranean cola is present in the adult phase through- region for 5 consecutive yr (at least) is an out the year (Mellor and Boned, 1989; un- unprecedented situation (Mellor, 1991).). published data; Capela, 1992; personal The question is therefore, how has the vi- communication). Bearing in mind the ap- rus managed to establish itself in this area parent absence of a long-term vertebrate and in the face of a concerted vaccination reservoir (at least in Europe), it is this ’all and vector abatement campaign (Diaz Yu- the year round’ presence of adult C imicola bero, 1987; Anonymous, 1987, 1992; Lu- due possibly to some recent moderation of broth, 1988). the climate, which has facilitated the over- It is clear that the transmission of AHS wintering of AHS virus in southern Spain virus in Iberia (and Morocco) is closely and/or Morocco from 1987-1991. Similarly the of the virus to overwinter in the linked with the presence of C imicola, the inability only confirmed field vector (Erasmus, Madrid-Toledo area of Spain, following its 1987, personal communication). Culi- original introduction in 1987, was due to coides imicola is an insect which is basical- the fact that adult C imicola disappear off the around the end of November in ly an Afro-Asian species and it is present wing throughout Africa (Walker and Davis, this area and do not reappear until the fol- and un- 1971; Wirth and Dyce, 1985) and as far lowing April (Mellor Boned, 1989; in central east as Laos (Howarth, 1985). It was only published data). Consequently C imicola is either not or as recently as 1982 that C imicola was first Spain present recorded in Europe, from Cordoba in else is only present as larvae for 3-4 southern Spain (Mellor et al, 1983) and not months of the year, far too long for AHS vi- until 1984 that it was first identified in Por- rus to persist in vertebrates alone. tugal (Mellor et al, 1985). Since that time The last officially reported equine death we have learned that it is widely distributed in central Spain during 1987 occurred in in Iberia ranging as far north at least as mid-October (Diaz Yubero, 1987) while the Madrid and Toledo in Spain (Mellor and first clinical cases in southern Spain in Boned 1988, unpublished observations) 1988 were not detected until early Octo- and Vila Real (41°30’N) in northern Portu- ber, almost 12 months later (Mellor et al, gal (Capela and Caeiro, 1991). It is likely 1990b). The long ’apparent’, inter-epizootic that in common with most other species of silence plus the considerable distance of Culicoides the distribution of C imicola is > 500 km between the 1987 and 1988 out- dependent upon a series of environmental break areas gave rise to a number of theo- factors including topography, temperature, ries regarding their separate origin. These availability of vertebrate hosts and availa- have included the transport of infected bility of suitable breeding sites. Further- equines and the flight of infected vectors more, its range will vary with the prevailing both from N Africa during 1988, and vaccine reversion. None of these theories are tend to peak at that time of the year, a situ- likely. Unlike 1966 when there was an epi- ation which also applies in Spain and Por- zootic of AHS virus serotype 9 centred in tugal (Mellor and Boned, 1988; unpub- N Africa, which may well have given rise to lished data; Capela, 1991; personal the Spanish outbreak of the same sero- communication). This being so the most type in that year (Sellers et al, 1977), in likely explanation for the observed inci- 1987 and 1988 there was no evidence at dence of AHS in southern Spain is that all of AHS anywhere across N Africa. Vac- even during the inter-epizootic periods, the cine reversion is equally unlikely in view of virus continued to circulate between sus- the time period of > 9 months between the ceptible equines and insect vectors but at end of vaccination in 1987 and the out- a very low level due to reduced vector pop- break in 1988. Also the S African vaccines ulation densities and activity rates. In such used in Spain have apparently never been a situation any infections at all in horses known to revert to virulence (Erasmus, would possibly still have been detected by personal communication, 1988). the authorities but the infection of a small All of the recent series of AHS epizoo- number of donkeys or mules, which both tics in Spain, Portugal and Morocco tend to present a less dramatic clinical pic- (1987-1991) have been due to AHS virus ture, might have escaped notice. The in- serotype 4 (Lubroth, 1988; Mellor et al, creased life span of the adult vectors dur- 1990b; Hooghuis, personal communica- ing the cooler times of the year, coupled tion, 1991; Anonymous, 1992). This is with a longer period of viraemia in donkeys serotype which has never previously been and mules, would also tend to reduce the recorded outside sub-Saharan Africa and number of transmissions necessary to at no time during the course of these epi- maintain the virus. zootics has there been any other evidence Although C imicola has long been the to suggest that AHS virus type 4 is spread- only confirmed (Culicoides) field vector of ing out of its enzootic zones (Mellor, AHS virus, isolations of this virus have now 1991 It therefore seems reasonably cer- been made in Spain from mixed pools of tain that there was only one introduction of non-engorged Culicoides consisting almost AHS virus type 4 into the western Mediter- entirely of C obsoletus and C pulicaris but ranean area and that was into central excluding C imicola (Mellor et al, 1990). in 1987. Since that Spain time the virus The range of C obsoletus and C pulicaris has persisted, overwintering 4 times in the extends much further north than that of process. C imicola and these species are probably The long periods of apparent quies- among the commonest Culicoides in north- cence between the annual disease epi- ern Europe. Intuitively one feels that if ei- sodes that were seen in Spain from 1987 ther or both of them have been involved in to 1990, are a feature that is reasonably AHS virus transmission in Spain then they common to several Culicoides-transmitted are likely to have been of much less impor- Orbiviruses in the Northern Hemisphere. tance than C imicola. However, this as- Epizootic haemorrhagic disease of deer vi- sessment is based upon the absence of rus and BT virus may both cause annual any other records linking C obsoletus and bouts of disease in the late summer and C pulicaris with AHS. Since AHS only rare- autumn (Inaba, 1975; Yonguc et al, 1982; ly extends as far north as Spain (and Por- Osburn et al, 1983; Anonymous, 1991).). tugal), it may be that the paucity of evi- This is related to the population densities dence linking these 2 species with this of the vector species of Culicoides which virus have more to do with a lack of oppor- tunity than with vector incompetence. Fur- REFERENCES thermore, it is well documented that differ- ent of a vector of Culi- populations species Abdallah SK (1983) Further studies on the trans- coides can vary widely in their ability to mission of African horse sickness. PhD the- transmit a particular virus (Jones and Fos- sis, Cairo University, Egypt ter, 1978; Jennings and Mellor, 1987), Anonymous (1978) African Horse Sickness. Ref- therefore some European populations of C erence Manual, Foreign Animal Diseases obsoletus and C pulicaris may prove to be Courses. Plum Island Animal Diseases Cen- 1-11I more efficient AHS virus vectors than pop- tre, 3rd edn, ulations of the same species further south. Anonymous (1987) Status of African horse sickness Bull Off Int 99, 46-48 It is also the case that species of Culi- (AHS). Epizoot coides which are competent to transmit Anonymous (1989a) African horse sickness epizoot. Bull Off Int 496 AHS virus are, as has been mentioned Epizoot 101, earlier in this paper, also able to transmit Anonymous (1989b) African horse sickness. the closely related BT viruses. If these 2 vi- Bull Off Int Epizoot 101, 550 rus groups do usually share common vec- Anonymous (1990a) Peste equina. In: Informe de la Comision de la Fievre Aftosa Otras tors then it may be of importance to note y 58th General Session, Off Int that both C and C obsoletus have Epizootios. Epi- pulicaris zoot, Paris, 14-18 May, 9-133 been implicated as potential vectors of BT Anonymous (1990b) Informe Sobre la Aparicion virus and Pitzolis, 1979; (Mellor Jennings de un Broté de Peste Equina en Malaga. and It is that the Mellor, 1988). possible Subdireccion Gen San Anim, Min Ag Pesca y northerly extension in the range of AHS vi- Alim, Spain rus to include SW Europe may have Anonymous (1991) Haemorrhagic Disease of brought the virus into contact with new, White-Tailed Deer: Information Brochure. SE previously unsuspected vectors which, Co-Op Wildlife Dis Study, Coll Vet Med Univ without the vigorous control programmes Georgia, GA, USA implemented by the Spanish and Portu- Anonymous (1992) La Peste Equine au Maroc. 1990 et 1991. Données guese Veterinary Authorities, could have Epizooties de 1989, Epidemiologiques et Stratdgie de Lutte. Roy- precipitated even further northwards aume Maroc Min Agric R6forme Agraire, Mo- of the disease. It is of spread clearly impor- rocco, April 60 pp tance that the competence of all potential Anwar M, Qureshi MAA (1972) Control and vector species of Culicoides in areas con- eradication of African horse sickness in Paki- sidered to be vulnerable to AHS virus in- stan. In: CENTO Semin Control and Eradica- cursion should be elucidated, so that risk tion Viral Diseases, Turkey, 110-1122 can be assessed, and if necessary effec- Awad FI, Amin MM, Salama SA, Khide S (1981) tive control measures devised and imple- The role played by Hyalomma dromedarii in mented in advance of possible disease the transmission of African horse sickness in outbreaks. Egypt. Bull Anim Hlth Prod Afr 29, 337-340 Blackburn NK, Searle L, Phelps RJ (1985) Virus- es isolated from Culicoides (Dipt Cerat) at the research farm Ma- ACKNOWLEDGMENTS caught veterinary zowe, Zimbabwe. J Entomol Soc S Afr 48, 331-336 This paper was conceived and produced during Boorman J, Mellor PS, Penn M, Jennings M the tenure of an EC project entitled ’African (1975) The growth of African horse sickness horse sickness virus in Europe’, (Contract No virus in embryonated hen eggs and the trans- 8001-CT91-0211). The author gratefully ac- mission of virus by Culicoides varripennis. knowledges the financial support. Coq (Dipt Cerat). Arch Virol47, 343-349 Bourdin P (1973) Ecology of African horse sick- Hess WR (1988) African horse sickness. In.! The ness. In: Proc 3rd Int Conf Equine Inf Dis. Arboviruses, Epidemiology and Ecology (Mo- Paris, 1972, 12-30 nath TP, ed) CRC Press Inc, Boca Raton, 1-18 Carpano M (1931) African horse sickness as FL, vol 2, observed particularly in Egypt and Eritrea. Howarth FG (1985) Biosystematics of the Culi- Min Agric Tech Sci Serv Bull Cairo 115, 1-411 coides of Laos (Dipt Cerat). Int J Entomol 27, Dardiri AH, Salama SA (1988) African horse 1-96 sickness: an overview. Equine Vet Sci 8, 46- Howell PG (1960) The 1960 epizootic of African 49 horse sickness in the Middle East and SW Dardiri AH, Brown CC (1989) African horse sick- Asia. J S Afr Vet Med Assoc 31, 329-334 ness update. In: llth Int Symp Wld Assoc Howell PG (1962) The isolation and identifica- Vet Micro Imm Spec Inf Dis (WAVMI). Peru- tion of further antigenic types of African horse gia, Italy, October 2-6, 287-289 sickness virus. Onderstepoort J Vet Res 29, Davies FG (1976) AHS vaccine. Vet Rec 98, 36 139-149 Davies FG, Lund LJ (1974) The application of Howell PG (1963) 2. African horse sickness. In: fluorescent antibody techniques to the virus Emerging Diseases of Animals. Food and of African horse sickness. Res Vet Sci 17, Agric Org, Rome, No 61, 73-108 128-130 Hussein RES (1982) African horse sickness, dif- Diaz Montilla R, Panos Marti P (1967) Epizooto- ferent methods of prevention and control. PhD logia de la peste equina en Espana. Bull Off Thesis, Zagazig Univ, Egypt Int Epizoot 68, 705-7144 Inaba Y (1975) lbaraki disease and its relation- Diaz Montilla R, Panos Marti P (1968) La peste ship to bluetongue. Aust Vet J 51, 178-185 equina. Bull Off Int Epizoot70, 647-662 Jennings DM, Mellor PS (1987) Variations in the Diaz Yubero MA (1987) Situacion de la Peste responses of Culicoides variipennis (Dipt Ce- to oral infection with Equina en Espana. Epizootiological Inf No rat) bluetongue virus. ESP, 87/6/145 Arch Virol95, 177-182 Du Toit RM (1944) The transmission of blue- Jennings DM, Mellor PS (1988) The vector po- tongue and horse sickness by Culicoides. tential of British Culicoides species for blue- Onderstepoort J Vet Sci 19, 7-166 tongue virus. Vet Microbiol 17, 1-100 El-Husseini MM, Salama SA, Abdallah SK, Jones RH, Foster NM (1978) Heterogeneity of Abou Bakr HE, Hassanein MM (1986) Role Culicoides variipennis to oral infection with of Culex pipiens L in recovering latent Afri- bluetongue virus. Am J Trop Med Hyg 27, 178-183 can horse sickness virus from dogs. J Egypt Soc Parasitol 16, 249-258 Jones RH, Luedke AJ, Walton TE, Metcalf HE Erasmus BJ (1973) The pathogenesis of African (1981) Bluetongue in the United States, an horse sickness. In: Proc 3rd Int Conf Equine entomological perspective towards control. InfDis. Paris, 1972, 1-111 World Anim Rev 38, 2-8 Erasmus BJ, Young E, Pieterse LM, Boshoff ST Kitaoka S (1966) Report to the Government of (1978) The susceptibility of zebra and ele- Iran on Vector Problems of Biting Midges, phants to African horse sickness virus. In: Culicoides, in Connection with African Horse June-lOth Equine Infectious Diseases (Bryans JT, ger- Sickness (11 th Dec, 1966). pp 8 ber H, eds) Vet Publ, NJ, 4th edn, 409-4133 Laaberki A (1969) Evolution d’une epizootic de Gorhe DS, Khot JB, Paranjpe VL, Manjrekar SL Peste equine Africaine au maroc. Bull Off Int 821-936 (1965) Observations on the outbreak of Epizoot 71, South African horse sickness in India during Lubroth J (1988) African horse sickness and the 1960-1961. Bombay Vet Coll Mag 1964- epizootic in Spain 1987. Equine Pract 10, 26- 1965, 5-155 33 Henning MW (1956) Animal Diseases in South Luedke AJ, Jones RH, Walton TE (1977) Over- Africa. Central News Agency Ltd, South Afri- wintering mechanism for bluetongue virus. ca, 3rd edn, 785-808 Biological recovery of latent virus from a bovine by the bites of Culicoides variipennis. Mornet P, Toma B, Sers JL (1967) Une nouvelle Am J Trop Med Hyg 26, 313-325 maladie rbput6e 16galement contagieuse : la Maurice Y, Provost A (1967) La peste equine a peste equine. Rech Med Vét Ec Alfort 143, 119-139 type 9 en Afrique Centrale, enqu6te s6rolo- gique. Rev Elev Med Vét Pays Trop 20, 21- Moul6 L (1896) Histoire de la Medecine Vétéri- 25 naire. Maulde, Paris, p 38 Mellor PS, Boorman J, Jennings M (1975) The Nevill EM (1971) Cattle and Culicoides biting multiplication of African horse sickness virus midges as possible overwintering hosts of in two species of Culicoides (Dipt Cerat). bluetongue virus. Onderstepoort J Vet Res Arch Virol 47, 351-356 38, 65-72 Mellor PS, Pitzolis G (1979) Observations on Nieschulz 0, Du Toit RM (1937) Investigations breeding sites and light-trap collections of into the transmission of horse sickness at Culicoides during an outbreak of bluetongue Onderstepoort during the season 1932-1933. in Cyprus. Bull Entomol Res 69, 229-234 Onderstepoort J Vet Sci Anim Ind 8, 213-269 Mellor PS, Jennings M, Braverman Y, Boorman Nieschulz 0, Bedford GAH, Du Toit RM (1934) J (1981) Infection of Israeli Culicoides with Results of a mosquito survey at Onderste- African horse sickness, bluetongue and Aka- poort during the summer 1931-1932 in con- bane viruses. Acta Virol25, 401-407 nection with the transmission of horse sick- Mellor PS, Boorman JPT, Wilkinson PJ, Marti- ness. Onderstepoort J Vet Sci Anim Ind 3, nez-Gomez F (1983) Potential vectors of 275-335 bluetongue and African horse sickness virus- Osburn BI (1988) The persistence and survival es in Spain. Vet Rec 112, 229-230 of bluetongue virus. In: Seminars on Blue- Mellor PS, Jennings DM, Wilkinson PJ, Boor- tongue. Ottawa, Jan 20, 40-49 man JPT (1985) Culicoides imicola: blue- Osburn BI, MacLachlan NJ, Anderson GA, Scott tongue vector in Spain and Portugal. Vet Rec JL (1983) A review of bovine bluetongue. Bo- 116, 589-590 vine Proc 15, 23-28 Mellor PS (1987) Factors limiting the natural Ozawa Y, Nakata G (1965) Experimental trans- spread of bluetongue virus in Europe. In: mission of African horse sickness by means Bluetongue in the Mediterranean Region of mosquitoes. Am J Vet Res 26, 744-748 WP, CEC Publ, DG No Eur (Taylor ed) Agric, Ozawa Y, Nakata G, Shad-del F, Navai S 102 37 EN Lux, 69-74 (1966a) Transmission of African horse sick- Mellor PS (1990) The replication of bluetongue ness by a species of mosquito Aedes aegypti virus in Culicoides vectors. Curr Top Microbi- Linnaeus. Am J Vet Res 27, 695-697 ol lmmunol 162, 143-161 Ozawa Y, Nakata G, Shad-del F (1966b) Experi- Mellor PS, Hamblin C, Graham SD (1990a) The mental transmission of African horse sick- occurrence of African horse sickness in Sau- ness by means of mosquitoes. Arch Inst Razi di Arabia. Vet Rec 127, 41-42 18, 119-125 Mellor PS, Boned J, Hamblin C, Graham S Ozawa Y, Shad-del F, Nakata G, Navai S (1990b) Isolations of African horse sickness (1970) Transmission of African horse sick- virus from vector insects made the during ness by means of mosquito bites and replica- 1988 epizootic in Spain. Epidemiol Infect tion of the virus in Aedes aegypti. Arch Inst 105, 447-454 Razi 22, 113-122 Mellor PS (1991) African horse sickness in Eu- Pilo-Moron E, Vincent J, Ait-Mesbah 0, Forth- In: Proc Soc Vet Prev Med rope. Mtg Epidem omme G (1969) Origine de la peste equine Univ 17-19 (Thrusfield MV, ed) Lond, April en Afrique du Nord; r6sultats d’une enqu6te 1991, 27-32 sur les anes de Sahara Aig6rien. Arch Inst M’Fadyean J (1900) African horse sickness. Pasteur (Algeria) 47, 105-1188 J Comp Pathol 13, 1-20 Pitchford-Watkins N, Theiler A (1903) Investiga- Mirchamsy H, Hazrati A (1973) A review on ae- tions into the nature and causes of horse tiology and pathogeny of African horse sick- sickness. Agric J Cape Good Hope 23, 15- ness. Arch Inst Razi 25, 23-46 156 Rabah M (1966) La peste equine au Maroc. Theiler A (1915) The problem of horse sickness. These doct vet, Lyon, France In: Rept 15th Ann Mtg Sth Afr Assoc Adv Sci. Rafyi A (1961) Horse sickness. Bull Off Int Epi- pp 65-83 zoot 56, 216-250 Theiler A (1921) African horse sickness (Pestis Rodriguez M, Castano M, Garcia I (1989) Peste equorum). 5th Afr Dept Ag Sci Bull No 199 equina Africana en Espana: focos de 1987, Van Rensburg LBJ, De Clerk J, Groenewald 1988 et 1989. In: Proc 3rd Jornada T6cnicas HB, Botha WS (1981) An outbreak of African Sobre et Caballo Expoaviga. 89, 25-30 horse sickness in dogs. JS Afr Vet Assoc 52, Salama SA, El-Husseini MM, Abdalla SK (1979) 323-325 Isolations and identification of African horse Van Saceghem R (1918) La peste du cheval ou sickness virus in camel tick Hyalomma drom- horse sickness au Congo Belge. Bull Soc adarii. In: 3rd Ann Rep US AHS Project Cai- Pathol Exot 11, 423-432 ro. 55-69 Venter GJ, Hill E, Pajor ITP, Nevill EM (1991) Salama SA, El-Husseini MM, Abdalla SK (1980) The use of a membrane feeding technique to Isolations and identification of African horse determine the infection rate of Culicoides imi- sickness virus in camel tick. In: 4th Ann Rep cola (Dipt Cerat) for two bluetongue sero- US AHS Project Cairo. 91-98 types in South Africa. Onderstepoort J Vet Schuberg A, Kuhn P (1912) Ober die ubertra- Res 58, 5-9 gung von krankheiten durch einheimische Walker A; Davies FG (1971) A preliminary sur- stechende insekten. Arb Gesundh-Amt (8erl) vey of the epidemiology of bluetongue in 40, 209-234 Kenya. J Hyg (Camb) 69, 47-611 Sellers RF (1980) Weather, host and vector - Walton TE (1991) Verbal statement. In: 2nd Int their interplay in the spread of insect-borne Symp Bluetongue, African Horse Sickness animal virus diseases. J Hyg (Camb) 85, 65- and Related Orbiviruses. Paris, 17-21 June 102 1991 Sellers RF, Pedgley DE, Tucker MR (1977) Wetzel H, Nevill EM, Erasmus BJ (1970) Stud- Possible spread of African horse sickness on ies on the transmission of African horse sick- the wind. J Hyg (Camb) 79, 279-298 ness. OnderstepoortJ Vet Res 37, 165-168 Sers JL La en (1967) peste equine Alg6rie. Williams AJ (1913) Notes on an outbreak of These doct France vet, Maisons-Alfort, horse sickness connected with the presence Shah KV (1964) Investigation of African horse of a Lyperosia as a possible transmitter. Vet sickness in India. Indian J Vet Sci 34, 1-144 J 69, 382-386 Theal GM (1899) Records of South-Eastern Af- Wirth WW, Dyce AL (1985) The taxonomic stat- rica Collected in Various Libraries and Ar- us of the Culicoides vectors of bluetongue vi- chive Departments in Europe. Gov of Cape rus. In: Bluetongue and Related Orbiviruses Colony, vol 3, p 224 (Barber TL, Jochim MM, eds) AR Liss, NY, Theiler A (1908) The immunisation of mules 151-164 with polyvalent serum and virus. In: Trans- Yonguc AD, Taylor WP, Csontos L, Worrall E vaal Dept Agric Rept Govt Vet Bacteriol (1982) Bluetongue in Western Turkey. Vet 1906-1907. pp 192-2133 Rec 111, 144-146