Scientific Opinion on the Role of Tick Vectors in the Epidemiology of Crimean-Congo Hemorrhagic Fever and African Swine Fever in Eurasia

The report provides an update on the role of the tick vectors in the epidemiology of African swine fever (ASF) and Crimean and Congo haemorrhagic fever (CCHF) in Eurasia, specifically to review of the geographical distribution of the relevant ticks with presentation of maps of their occurrence in Europe and Mediterranean basin; a description of the factors that define the relevant tick population dynamics and identify possible high risk areas in the EU; an update on the role of tick vectors associated with CCHF and ASF in Eurasia; and reviews available methods for the control of the relevant tick vectors. Data were collected through systematic literature review in a database from which maps of geographic distribution of ticks, CCHF virus and ASF virus were issued. The main vectors for CCHF are Hyalomma spp, Increase in the number of fragmented areas and the degradation of agricultural lands to bush lands are the two main factors in the creation of new foci of CCHF in endemic areas. Movement of livestock and wildlife species, which may carry infected ticks, contributes to the spread of the infection. The Middle East and Balkan countries are the most likely sources of introduction of CCHFV into other European countries. All the Ornithodoros species investigated so far can become infective with ASF virus and are perhaps biological vectors. These ticks are important in maintaining the local foci of the ASFV, but do not play an active role in the geographical spread of the virus. Wild boars have never been found infested by Ornithodoros spp. because wild boars normally do not rest inside protected burrows, but above the ground. There is no single ideal solution to the control of ticks relevant for CCHF or ASF. The integrated control approach is probably the most effective.

© European Food Safety Authority, 2010

Introduction

The recent developments in the EU, especially the risk of introduction of African swine fever virus (ASF) from the East European countries and the Caucasus; and the threat that would represent the spread of the Crimean-Congo hemorrhagic fever virus (CCHF) in Europe; elicited a self-mandate of the EFSA’s Panel of the Animal Health and Animal Welfare on the role of tick vectors associated with Crimean-Congo hemorrhagic fever and African swine fever in Eurasia. The occurrence of other tick-borne animal diseases and zoonoses in the EU was also considered as part of this mandate. The terms of reference of the self-mandate were:

• Provide an update on the role of the tick vectors in the epidemiology of ASF and CCHF in Eurasia, more in particular:
  • provide a review of the geographical distribution of the relevant ticks and produce maps of Eurasia displaying their occurrences;
  • review surveillance data to provide estimates of the relevant tick abundance and disease incidence in Eurasia;
  • describe the factors that define the relevant tick population dynamics and identify possible high risk areas in the EU for introduction considering the biological and ecological characteristics of the ticks and their ability to adapt to new areas;
  • provide an update on the role of the relevant vectors in the transmission and the maintenance of ASF and CCHF in Eurasia;
  • review available methods for the control of the relevant tick vectors.

• Provide a general overview of the geographic distribution of ticks which have proven involvement in the transmission of animal diseases and zoonoses in Eurasia.

The mandate resulted in two scientific reports: this one on ”The role of ticks in the epidemiology of CCHF and ASF in Eurasia” (addressing the first point); and another on “The geographic distribution of tick-borne infections and their vectors in Europe and the other regions of the Mediterranean basin”, covering the second point.

The methodology

Part of the presented information derived from findings of two previous scientific reports (CFP/EFSA/AHAW/2007/02 and CFP/EFSA/AHAW/2008/04) obtained in accordance with Article 36 of Regulation (EC) No 178/ 2002[1] . The section on ASF was elaborated in parallel with EFSA scientific opinion on African swine fever (EFSA Journal 2010; 8(3); 1556). In addition, a systematic literature review was performed in order to gather data on tick and tick-borne pathogens distribution. The review included searching in the databases integrated in ISI web of knowledge and Pubmed for the scientific papers published during the last 10 years. The ad hoc experts, also, contributed with relevant scientific papers regardless of the timeframe, which were also submitted to the same procedure of systematic literature review. Historical data on ticks’ distribution (approximately from year 1970 to 2000) was obtained from the integrated consortium of ticks and tick-borne diseases (European project, ICTTD3). All these data were stored in a database that allowed the creation of distribution maps either for ticks or for tick-borne pathogens. The maps have the limitation of representing only what was found through the systematic literature review process or in the ITTCD3 database.

The results for CCHF

Relevant tick species were identified and their role in transmission of the viruses is discussed. The main vectors are Hyalomma spp. but at local level Dermacentor spp. and Rhipicephalus spp. have proven capacity of maintaining the CCHFV through their life cycle and transmit it to the vertebrates. However the role of I. ricinus (the most widely distributed tick in Europe) in the transmission of CCHFV has not been ascertained. Several studies indicate that argasid (soft) ticks are not competent CCHFV vectors.

Maps are provided describing the geographic distribution of the ticks involved in the epidemiology of CCHF, as well as the distribution of CCHFV. It is unknown so far the reason for the limited geographical spread of CCHF cases to countries in the South East of Europe and Middle East, although the tick vectors of CCHFV (Hyalomma marginatum, Dermacentor marginatus, Rhipicephalus bursa) are much wider spread in Europe.

Surveillance data are scattered and inconsistent in terms of diagnostic capability and host species including humans. Data on tick abundance is lacking, specifically for Hy. marginatum. Infection can be monitored in ticks using various methods of collection. Movement of livestock and wildlife species, which may carry infected ticks, contributes to the spread of the infection. Migratory birds may not be sufficient to establish new foci of infection. The absence of clinical signs and the lack of reliable diagnostic tests to detect the infection in mammals and birds make the confirmation of the infection in animals difficult. This report has not considered the movement of viraemic domestic or wild animals as a source of spread infection because it is out of the remit of the mandate.

Disease ecology, including its vectors, was described. Mammals such as rodents, hedgehogs, hares, are considered the principle reservoirs of CCHFV. Ungulates are important hosts for adult tick vector species. Vireamic periods, however, in ruminants appear to be short which may reduce the transmission of this virus to other hosts. In the tick populations the infection is maintained by transstadial and transovarial transmissions. Co-feeding transmission has not been proven in a natural setting. Increase in the number of fragmented areas and the degradation of agricultural lands to bush lands are the two main factors in the creation of new foci of CCHF in endemic areas. A complex chain of interactive factors exists that makes causes for changes in the infection level often difficult to assess. Climate change is only one of the factors associated with the spread of the infection. High risk areas were identified according to scientific evidence, specifically related to the vector ecology. The Middle East and Balkan countries are the most likely sources of introduction of CCHFV into other European countries. There are existing risk models for other tick-borne diseases, such as tick-borne relapsing fever (TBRF), and ASF. These two models serve the purpose of identifying gaps in knowledge and data that can be applied for CCHF risk modelling.

Measures of control of the relevant ticks were presented with scientific evidence of their efficiency. There is no single ideal solution to the control of ticks. The integrated control approach is probably the most effective.

The results for ASF

Relevant tick species were identified. Of all the invertebrates tested up to the present only the soft ticks of the genus Ornithodoros are susceptible to ASFV infection either naturally or experimentally. Other soft ticks remain untested under laboratory conditions. Hard ticks or other blood feeding invertebrates have not been shown to be a vector of ASFV. All the Ornithodoros species (O. erraticus, O. moubata /porcinus, O. coreaceus. O. turicata, O. puertoricensis, O. parkeri and O. savignyi) investigated so far can become infective and are perhaps biological vectors of ASF. Of these species, some are found only in Afrotropical and Neotropical regions. Only the O. erraticus complex is found in the European, trans-Caucasus countries (TCC) and Russian Federation territories.

Maps are provided describing the geographic distribution of the ticks involved in the epidemiology of ASF, as well as the distribution of ASFV.

To our knowledge there is no systematic monitoring of the occurrence of Ornithodoros ticks in EU.

The ecology of the disease was revised. The O. erraticus complex, because of its long life (up to 15 years) and strong resistance to starvation and persistence of infection for up to 5 years, is important in maintaining the local foci of the ASFV (and lead to endemicity in a region). However, they do not play an active role in the geographical spread of the virus. Ornithodoros ticks feed mainly on animal species living in burrows, such as rodents and reptiles. Pigs are mostly accidental hosts, from which the ticks can be infected. The epidemiological role played by soft ticks becomes important where pigs are managed under traditional systems, including old shelters/sties with crevices. Wild boars have never been found infested by Ornithodoros spp. because wild boars normally do not rest inside protected burrows, but above the ground. Due to the limited available data on associated factors with the distribution of soft ticks, prediction of their potential distribution is difficult to construct. EFSA scientific opinion on African swine fever (EFSA Journal 2010; 8(3); 1556) elaborates on the risk of introduction of ASFV in the EU.

Measures of control of the relevant ticks were discussed. Eradication of O. erraticus from the old pig sties is invariably unsuccessful. The use of acaricides on pigs and their habitat can reduce the level of infestation in the premises but does not avoid the pigs of becoming infected by ASF virus if they are bitten by a virus infective tick.

Recommendations

CCHF

The current database on ticks’ distribution should be maintained. Scientific information can be included in the database only if the following items are clearly specified: the scientific names of the organisms studied (vectors or pathogens), origin of samples (vegetation, host), type of samples (blood, serum, organs, etc), geo-reference of the sample, diagnostic tools used to identify the ticks, date, and history of the samples if applicable (imported host or vectors, travel history).

There is a need for a standard case definition of CCHFV infection in vertebrates and arthropods. It is essential to notify the presence of vectors during outbreaks and the disease notification should include the possible involvement of vectors.

Mapping of endemic areas and assessment of future risk areas are necessary for appropriate surveillance and control of CCHF. Vector collection with reliable identification methods and tools (morphological keys and DNA-based tick species identification) should be available in all countries where CCHFV occur or can be expected to emerge in the near future.

The presence of CCHFV in a geographic area can be monitored by PCR on ticks collected on the animals and in the environment (questing ticks)
Frequent serosurveys of grazing animals, including livestock and wildlife, in CCHFV free areas neighbouring or bordering known high risk areas (i.e. the southern Balkans and Turkey) is another approach for determining recent introduction of the virus. A prerequisite for such approaches, however, would be the development of reliable and specific diagnostic assays to detect antibodies in a range of host species.

A risk model for the introduction and spread of CCHFV, including gaps in existing knowledge, should be considered regarding the available similar models such as ASF and TBRF. Pathways other than tick transmission for the introduction and spread of infection should be considered in this risk model.

To prevent virus infection to humans by ticks, general guidelines on personal protection should be available to the general public in affected countries.

Integrated tick control measures should be developed at international level.

Acaricides should be used in accordance with the best practice that minimise the development of resistance by the tick species.

ASF

The ASF recommendations are in agreement to those presented in EFSA scientific opinion on African swine fever (EFSA, 2010)

Recommendations for research

CCHF

The role of other tick species, specifically I. ricinus, in the transmission of CCHFV should be investigated under natural conditions.

The role of European wild life, especially wild ungulates, in the spread of CCHFV needs to be investigated.

The necessary biotic and abiotic conditions for the maintenance of CCHFV in nature require further investigation.

In order to understand the epidemiology, further knowledge on the pathogenesis and distribution of the virus in mammalian hosts should be obtained

ASF

Different Ornithodoros spp. may play various roles in the epidemiology of ASF. It would need further investigations

CCHF, ASF, vector, Hyalomma, Ornithodoros, tick-borne disease, Europe