Artykuł przeglądowy Review
Bluetongue virus (BTV) and epizootic hemorrhagic disease virus (EHDV) are separate but closely related species within the genus Orbivirus and the family
Reoviridae (18, 19). These two viruses are genetically
distinct and do not cross-react serologically. Both vi-ruses are transmitted by the Culicoides biting midge (Diptera, Ceratopogonidae), with different midge species having different levels of competence for the onward transmission of each virus (7). Until now, 27 serotypes of BTV (BTV 1 to BTV 27) and 10 serotypes of EHDV (EHDV 1-8, EHDV-318 and Ibaraki virus) have been serologically identified (3, 22, 45). Genetic diversity within BTV and EHDV species occurs as a consequence of both genetic drift and genetic shift. Genetic shift occurs as a consequence of reassort-ment of viral genome segreassort-ments during co-infections of either animals or insect vectors with more than one virus serotype or strain, whereas genetic drift occurs as a consequence of polymerase “infidelity” during
replication of the virus leading to a viral quasispecies with subsequent founder effect of specific genetic variants in either Culicoides midges or animal hosts (25). BTV is more important economically because it is infectious for domestic and wild ruminant species, EHDV is most significant as a pathogen of ruminant wildlife, notably white-tailed deer (Odocoileus
vir-ginianus). Both viruses causes similar clinical signs
including high fever, hyperaemia in nasal and oral mucosa, lethargy, oedema, ulcerations of the dental pad, haemorrhaging of the heart, lungs, major blood vessels and other tissues (17, 19).
Bluetongue (BT) is an infectious but non-contagious, viral disease of ruminants, mainly sheep and less fre-quently of cattle, goats, buffalo, deer, dromedaries, and antelopes. BT has a significant economic impact, mainly due to the disease effect on animals (morbidity, mortality, reproductive failure, reduction in milk yields and weight gain) and, most of all, to the disruption of
Recent changes in the global distribution
of arboviral infections in ruminants
WIESŁAW NIEDBALSKI, ANDRZEJ FITZNER
Department of Foot and Mouth Disease, National Veterinary Research Institute, Wodna 7, 98-220 Zduńska Wola, Poland
Received 20.08.2019 Accepted 17.09.2019
Niedbalski W., Fitzner A.
Recent changes in the global distribution of arboviral infections in ruminants
Summary
The aim of this paper is to present the recent changes in the global distribution of bluetongue (BT) and epizootic hemorrhagic disease (EHD) in the world. Both of these arboviral infections are widespread in the territory of many continents. BT is currently endemic in many tropical, sub-tropical and temperate regions of the world (Africa, southern Asia, Australia, the Middle East, and the Americas), between latitudes 50°N and 35°S, during times of the year that are optimal for vector activity. In Europe, BTV serotypes 1, 2, 4, 8 and 16 are currently circulating in many regions of continent. The range of EHDV lies approximately between latitudes 35°S and 49°N. EHDV infection of wild and domestic ruminants has been reported in the America, Africa, Asia, Australia, the Middle East as well as some islands of the Indian Ocean. Recently it has also been recorded in cattle in countries surrounding the Mediterranean Basin including: Israel, Turkey, and northern African countries such as Morocco, Algeria and Tunisia. So far there has been no report of EHDV being present in Europe, but there has been only limited surveillance for subclinical infections in wild cervids. The global range of BT and EHD and their aetiological agents have changed remarkably in recent years, most notably with the incursion to Europe of multiple virus serotypes. The enormous genetic diversity of these orbiviruses can lead to the emergence of viruses with unique biological properties, such as a capacity for horizontal and vertical transmission. Reassortment of the genes of invasive orbiviruses with those viruses already present in environment has facilitated the successful introduction and spread of novel reassortant progeny between episystems.
international trade of animals and animal products (29). BT is currently endemic in many tropical, sub-tropical and temperate regions of the world (Africa, southern Asia, Australia, the Middle East, and the Americas), between latitudes 50°N and 35°S, during times of the year that are optimal for vector activity (40). BT is widespread throughout Central and South American and the Caribbean, but with little or no clinical signs. In South America, BTV-4 and BTV-12 have been isolated from Brazil and Argentina, while there is serological evidence for the presence of BTV serotypes 4, 6, 12, 14, 17, 19 and 20 (42). Serological surveys and virus isolations through Central America and the Caribbean have identified the presence of BTV serotypes 1, 3, 4, 6, 8, 10-14 and 17. Since 1999 the incursion of multiple novel BTV serotypes into the south-eastern USA from the adjacent Caribbean episystem was found (18, 33). In Canada, BTV serotypes 2, 10, 11, 13 and 17 are listed as immediately notifiable (http://www. inspection.gc.ca/animals/terrestrial-animals/diseases/ immediately-notifiable/eng). In Australia, BTV-20 was isolated in 1970s from Culicoides midges in the northern territory of this continent. Seven more BTV serotypes: 1, 3, 9, 15, 16, 21 and 23 were sub-sequently identified by 1986 (15). It was shown that many Australian BTV strains have limited virulence or are non-virulent (6). In 2017 BTV infection was extended into Victoria state, which is farther south than the virus’ traditional distribution on that continent. Recently, identification and genomic characterization of the first isolate of BTV-5 from Australia has been de-scribed (41). On the Asian continent, across Indonesia, Malaysia, China and Japan, there is evidence for BTV serotypes 1-4, 7, 9, 11-13, 15, 16, 20, 21 and 23 with an unconfirmed report of BTV-17 from China. BTV serotypes 1, 3, 9, 16 and 23 seem to be widely spread throughout these countries. BTV-2 appears to be absent in the south and east regions of Asia, and BTV sero-types 8 and 18 (present in India) had not yet spread as far as Southeast Asia (6). On the Indian subcontinent, BT has been identified since 1963 in many areas of India and by 2009 evidence for the presence of twenty-one of the twenty four known BTV serotypes had been found in India. While BTV is now considered endemic in India and Pakistan, there are few reports from other countries in this region (27). The first report of BTV infection in the Republic of Korea appeared in 2015; BTV-1 was isolated in blood samples collected from abattoirs throughout the country and complete coding sequence of the segment 2 gene was presented (35).
Historically, Europe has experienced only sporadic incursions of BT, involving a single virus serotype on each occasion (20). However, since 1998 BTV spread northwards into the Mediterranean Basin, where five BTV serotypes (1, 2, 3, 8, 15) have been identified (21). Afterwards, between 1998 and 2005, BTV en-tered Europe from at least two origins and spread up
to 800 km further north in Europe than ever before. It has been suggested that this spread has been driven by the recent changes in European climate, which have allowed increased virus persistence during winter, the northward expansion of C. Imicola and, beyond this vector’s range, transmission by indigenous European
Culicoides species, thereby expanding the risk of
transmission over larger geographical regions (28). In August 2006, for the first time, BTV passed the latitude 50°N and the disease caused by BTV serotype 8 occurred in the Netherlands, Belgium, Germany, France and Luxembourg. The sequence analysis of the BTV-8 genome suggested a close similarity to BTV strain of this serotype previously isolated from sub-Saharan Africa (16). However, the implementation of BT compulsory vaccination programmes in Europe in spring 2008 resulted in eradication of disease caused by BTV-8 in 2011.
After a four year break, in August 2015, BTV-8 re-emerged in Europe, in central France and subsequently spread throughout the entire country (31). How BTV-8 persisted in areas that were thought to have been free of virus transmission remains unknown, although it has been recently reported that low-level circulation of BTV-8 occurred in France prior to the detection in 2015 (5). However, there were observations suggested that changes had occurred in the epidemiology of the re-emerging strain of BTV-8. Whereas the 2007-2009 BTV-8 strain caused widespread clinical signs in cattle and sheep, the re-emerging BTV-6 strain caused only mild clinical signs. Moreover, evidence of reduced viremia, pathogenicity and vector competence in re-emerging BTV-8 strain in sheep have been proved (8). In addition, the rate of spread of the virus in France appeared slower than BTV-8 from the previous epizoo- tics. The high degree of amino acid similarity between the 2007 and 2015 BTV-8 strains confirms the hypoth-esis that this is not a new introduction of BTV-8 (31). The total number of BTV outbreaks in France since 2015 has been estimated at 4015: there have been 143, 1294, 1925 and 653 BT outbreaks in 2015, 2016, 2017 and up to 23 September 2018, respectively (https://ec.europa.eu/food?sites/food/files/animals/ docs/ad_adns_outbreaks-per disease.pdf). Then, on 23 October 2017, a BTV-8 outbreak was confirmed in cattle in Basel-Landschaft canton in the northwest of Switzerland, returning, similarly in cattle, in September 2018 (https://healthmap.org/promed/p/105). The cases in cattle were reportedly subclinical, detected within the framework of an active surveillance program. Moreover, four BTV-8 outbreaks were recorded in sheep, with the first starting on 12 October 2018, fol-lowed by three additional on sheep farm, starting on 16, 31 October and 7 November 2018. Differently from the outbreaks in cattle, the disease cases in sheep were identified by clinical signs, which were confirmed by laboratory diagnostics. In total, as of 1 February 2019,
79 outbreaks caused by BTV serotype 8 were reported in Switzerland. On 12 December 2018, the German authorities con-firmed a case of BTV-8 in cattle in the district of Rastatt in Baden-Württemberg, Germany. This was the first case of BT in Germany since November 2009, and as of 25 May 2019, 57 outbreaks of BTV-8 have now been re-ported in Germany (Baden-Württemberg, Saarland and Rhineland-Palatinate Landers). The majority of these are in the south-western part of the country close to the borders with France and Switzerland. (https:// www.agriculture.gov.ie/
bluetongue/). In addition, the outbreak of BTV-8 was detected on the 14 February 2019 in cattle holding in the Luxembourg region of southern Belgium, and as of 11 March 2019 four BTV-8 outbreaks have been reported (http://www.gov.uk/government/publications/ bluetongue-virus-in-europe).
In France, apart from outbreaks of BTV-8, disease caused by BTV serotype 4 has been detected in 2016 in Corsica and in November 2017 in mainland France, adjacent to the Swiss border (30). The results of phylo-genetic analysis and epidemiological data suggest that BTV-4 has been introduced to mainland France from Corsica or Italy where BTV-4 outbreaks have been reported in summer and autumn 2016. This was the first report of the introduction of BTV-4 in mainland France. This genetically distinct reassortant strain of BTV-4 was identified in 2014 in the Balkan countries (Croatia, Greece, Bulgaria, Romania, Slovenia), dur-ing 2014-2016 in the mainland Italy and in the years 2016-2017 in Sardinia. In 2014 BTV-4 outbreaks were also reported in Spain and Portugal. In addition to BT outbreaks caused by serotypes 8 and 4, BTV-1, 2 and 16 are present in parts of the Mediterranean Basin. BTV-1 is circulating in France (Corsica), Italy, Spain and Portugal. BTV serotype 16 has been con-firmed in September 2017 in Greece and at present is circulating on the Greek islands of Samos, Lesvos and Dodecanese. The list of BT restriction zones in Europe as of 27 March 2019 is as follows (Fig. 1): Zone Y – BTV-8 and 4, France: mainland territories of country, Zone I – BTV-1 and 4, Italy, Croatia: the island of Lastovo in Split-Dalmatia county, Spain:
the autonomous community of Andalucia (provinces Cadiz, Cordoba, Huelva, Jaen, Malaga and Sevilla, Granada), autonomous community of Castilla-La Mancha (Ciudad Real province), autonomous com-munity of Extremadura (Badajoz province), Portugal: the entire continental territory of the country, Zone H – BTV serotype not specified, Malta: the whole territory, Zone T – BTV-1, 2, 4, 8 and 16, France: department de Haute-Corse, department de Corse-du-Sud, Zone X – BTV-4 and 16, Greece: the islands of Dodekanisa and Samos, Zone A3 – BTV-4, Greece: the entire territory of Greece except for the regional units of Cyclades islands and the island of Chios, Bulgaria: the whole territory, Romania: the whole territory, Hungary: the whole territory, Croatia: the whole territory, Spain: in the autonomous community of Castilla-La Mancha (Ciudad Real, Toledo and Albacete provinces), in the autonomous community of Castilla y Leon (Avila prov-ince), the autonomous community of Extramadura, Slovenia: the whole territory, Italy, Zone A4 – BTV-1, 4, 8, 16, Greece: the island Lesbos, Zone A5 – BTV-1, 3, 4, Italy: Sicilia and Sardegna, Zone A6 – BTV-1, 4, 16, Italy: Crotone and Reggio de Calabria, – Zone A7 – BTV-4, 16 and 8, Cyprus: the whole territory, Zone A8 – BTV-16, Greece: the islands of Kos, Ikaria, Samos, Dodekanis and Lesvos, Zone F – BTV-8, Belgium: the entire territory, Switzerland: the entire territory, Germany: Baden-Württemberg, Saarland, Rhineland-Palatinate Landers (administrative divisions of Hessen, North Rhine-Westphalia, and Bavaria).
Epizootic hemorrhagic disease (EHD) is an acute, infectious and fatal viral disease of ruminants (20).
Fig. 1. Bluetongue-restricted zones in Europe as of 27 March 2019 (http://ec.europa.eu/food/ animal/diseases/controlmeasures/bt_restrictionzones-map.jpg)
EHD epidemics resulted in significant economic losses from decreased productivity, including reduced milk yield. EHDV affects a wide range of susceptible animals starting from domestic ruminants to wild ruminants including cer-vids, especially white-tailed deer (Odocoileus
virginia-nus) in North America. The
morbidity and mortality due to EHD in wildlife is difficult to determine. The estimated number of affected animals and populations in at risk areas suggests an infection rate of 29% and mortality rate of 20% in white-tailed deer (10). These cervids are the most severely affected by the disease while the survival rate
is much higher in mule deer (Odocoileus hemionus), black-tailed deer (Odocoileus hemionus
columbia-nus) and pronghorn antelope (43). The distribution of
EHD depends on the distribution and abundance of the biting midge Culicoides variipennis, the level of existing immunity in deer, and the genetic varia-tions in susceptibility (10). EHD was first described in 1955 in a New Jersey outbreak characterized by high mortality in tailed deer (19). Outbreaks in white-tailed deer are seasonal, occurring from mid-summer to late autumn and appear to occur every 2 to 3 years in endemic areas, and every 8 to 10 years in epidemic areas (24). According to reported cases, the range of EHDV lies approximately between latitudes 35°S and 49°N (34). EHDV infection of wild and domestic ruminants has been reported in the Americas, Africa, Asia, Australia, the Middle East and some islands of the Indian Ocean (Fig. 2). So far there has been no report of EHDV being present in Europe, but there has been only limited surveillance for subclinical infec-tions in wild cervids. Recently EHD has been recorded in cattle in countries surrounding the Mediterranean Basin, including Israel, Turkey and northern African countries such as Morocco, Algeria and Tunisia (7, 12, 13, 32). Very little is known about the distribution of EHDV in other regions of Africa apart from the fact that EHDV-3 (now reclassified as EHDV-1) and EHDV-4 were isolated in Nigeria in the late 1960s and EHDV-4 and EHDV-6 in cattle in Sudan in 1982 and EHDV (serotype unknown) in South Africa during 1995-1997 (32). EHDV serotypes 1, 2, 5, 6, 7 and 8 are known to occur in Australia (19). On the Asian continent, the occurrence of EHDV was first recorded in 1959 in Japan with the name of Ibaraki disease and has become epidemic with a record death of over 56 000 death cases
(14). The virus genome was detected from diseased and asymptomatic cattle by RT-PCR. The disease occurred in Japan was characterized by fever, anorexia and dif-ficulty in swallowing, which may lead to dehydration and emaciation with aspiration pneumonia constituting the major cause of death in affected animals. Oedema, haemorrhages, erosions, and ulcerations may be seen in the mouth, on the lips, and around the coronets. The animals may be stiff and lame and the skin may be thickened and oedematous. Abortions, foetal malfor-mations and stillbirth have also been reported in the 1997 EHD epidemics in Japan (26).
There has been a wide distribution of EHD among the different regions of USA, while the frequency and severity occur infrequently in larger outbreaks result-ing in higher mortality in the northern USA. Likewise a higher survival rate with less severity can be noted in southern regions of the country (10). North American isolates of EHDV are able to cause viremia in cattle and in sheep, usually without inducing clinical disease, calves inoculated with EHDV-2 became infected, as evidenced by development of viremia and serocon-version. However, the virus did not cause detectable clinical disease, clinopathologic abnormalities, or gross lesions (1). Historically only EHDV-1 and 2 have been reported in North America. EHDV-1 (New Jersey strain) and EHDV-2 (Alberta strain) were first isolated in USA in a large scale mortality of white-tailed deer. In 2006, a non-EHDV-1 or -2 virus was recovered from moribund or dead white-tailed deer in Indiana and Illinois. This virus was later typed as EHDV-6 by serological and genetic testing (2). EHDV-6 was originally described from Australia and is an emerging pathogen of cattle in Morocco, Algeria and Turkey. EHDV-6 was also recovered from Kansas and
Texas in 2008 and become endemic. Subsequently, ad-ditional isolations of EHDV-6 from white-tailed deer in Missouri in 2007, Kansas and Texas in 2008 and Missouri and Michigan in 2009, suggesting that the virus has overwintered and may be endemic in a geo-graphically widespread region of the USA (2). How this newly identified virus type has spread in the USA is difficult to determine. It is possible that the virus has been present for some time since genetic characteriza-tion indicated that this virus is a reassortant. Recently, EHDV-1 and 6 are endemic throughout the USA in both wild and domestic ruminants, while EHDV-2 is primarily endemic in south-eastern USA (24) and is the most commonly detected EHDV serotype infecting white-tailed deer in the USA (38). Although EHDV-1, 2 and 6 are endemic in various areas of North America, South America and the Caribbean basin, no clini-cal outbreaks in cattle had been reported until 2013, when EHD was reported in cattle from Illinois (USA) following an outbreak in deer in the same location in 2012 (37). The absence of clinical signs in relation to antibody prevalence could not be explained by poor detection and several factors may contribute to the ob-served enzootic stability: innate host resistance, mater-nal antibody transfer, vector species composition and seasonality (36). Similar findings of serologic detec-tion of EHDV-1 and 2 were reported in Mule deer and Pronghorn antelope in Arizona, and in sentinel cattle in Texas (9). A phylogenetic analysis of the EHDV-2 strains based on samples collected throughout the eastern USA over three decades revealed that closely related genotypes were widely distributed in time and space (23). Additional analysis of these data indicated that in outbreaks within the same year, genetic and spatial distances are positively correlated and that the virus is evolving at a rate similar to that seen in other vector-borne viruses (4). The fact that evidence for a demographic expansion of the virus was not apparent from the genetic data suggest that EHDV-2 dynamics are limited by factors other than deer host density. The abundance of competent vectors, for example, may have a much more pronounced effect on virus popu-lation sizes (4). In addition, phylogenetic analysis of the outer capsid serotype-specific protein from USA field strains of EHDV-2 indicated regionalized genetic types, suggesting limited movement of virus popula-tion across the country.
Before 2000 only sporadic reports on the presence of EHDV in the Mediterranean Basin were available. In 2004, an outbreak caused by EHDV-6 was reported in Morocco and the same EHDV serotype was respon-sible for another outbreak in the same country two years later. In the same year, EHDV-6 caused disease outbreaks in Algeria and Tunisia and one year later in Turkey (39). In 2006, the clinical cases of EHD were also described in cattle in Israel; however, the disease was caused by EHDV serotype 7 (44). The
first cases were observed in the region bordering Jordan, where suspect clinical cases of EHDV were also found. Within-herd morbidity ranged from 5 to 80% in infected dairy herds, with variable involvement of replacement heifers; the case-fatality was less than 1%. The duration of the disease in individual animals was reported to range between 3 and 30 days. There were no reports of a distinctive disease syndrome in sheep or goats in these areas. Affected cows showed a 10 to 20% reduction in milk production and loss of appetite, followed by clinical signs similar to caused by Ibaraki virus. The losses due to abortion, infertil-ity problems and inferior milk qualinfertil-ity were noted as a result of disease (44). Summarizing, in 2006-2007, disease outbreaks caused by EHDV infection have been reported in Algeria, Tunisia, Morocco, Israel and Turkey. Two different virus serotypes were involved: EHDV-6 and 7. Both isolates were pathogenic and capable of causing EHD in cattle. The possible origin of both EHDV strains is unclear. In the late 1980s EHDV-6 was identified in Sudan, Bahrain and Oman, and it is likely that this EHDV serotype has remained in the region until the recent outbreaks. Conversely the only place where the presence of EHDV-7 has been evidenced other than Israel is Australia. In September 2015, a large outbreak of EHD was identified in an Israeli dairy and beef farm. According to the sequence and phylogenetic analysis of the VP2 gene, the 2015 Israeli EHD outbreak was caused by EHDV-6, which was found not only in cattle with clinical symptoms of disease, but also in aborted foetuses (12). Even though the origin of the EHDV serotypes which af-fected the African and Asian Mediterranean countries remains unclear, it is important to notice that there is an alarming similarity between the EHDV scenario and that of BTV which took place at the end of the 1990s. During that period some BTV serotypes that initially circulated in Algeria, Tunisia, Turkey and Israel were able to cross the Mediterranean Sea and invade south-ern Europe through westsouth-ern, eastsouth-ern and southsouth-ern corridors.
To conclude, the global distribution of bluetongue (BT) and epizootic hemorrhagic disease (EHD) in the world have changed remarkably in recent years, most notably with the incursion to Europe of multiple BTV serotypes. The unexpected emergence of BT or EHD provides an uniquely sobering and unambigu-ous reminder of the potential consequences of climate change on the distribution and severity of vector-borne diseases. The enormous genetic diversity of these orbiviruses can lead to the emergence of viruses with unique biological properties, such as capacity for hori-zontal and vertical transmission. Reassortment of the genes of invasive orbiviruses with those viruses already present in environment has facilitated the successful introduction and spread of novel reassortant progeny between episystems.
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Corresponding author: Dr hab. Wiesław Niedbalski, assoc. prof., Wodna 7, 98-220 Zduńska Wola, Poland; e-mail: wieslaw.niedbalski@piwzp.pl
