Determination of the role of hard (Ixodid) ticks in the transmission of lumpy skin disease virus in cattle

Lead Research Organisation: The Pirbright Institute
Department Name: UNLISTED

Abstract

Lumpy skin disease (LSD) is an economically important viral infection of cattle occurring in most African countries and in the Middle East. It may cause significant economical losses to the farmers due to decrease in milk yield, abortions, infertility problems in males and females, and a loss in body weight and the value of hide. In endemic countries the loss of production, the costs of control and eradication programmes and, restriction or ban on the international trade of live animals or animal products following an outbreak are substantial. In general, poxviruses have been shown to enter the host through the skin or respiratory tract. Direct contact between infected and susceptible animals is considered to be a relatively inefficient route of the transmission of lumpy skin disease virus (LSDV). The virus is secreted in saliva, ocular and nasal discharges, and semen of the infected animals and therefore contaminated food or water and artificial insemination may serve as a source of infection. The occurrence of the disease is closely connected to warm and wet weather conditions and the abundance of insects. However, little is known about the importance of the different insect vectors in the transmission of LSDV during natural outbreaks. So far, no studies on the potential role of hard ticks in the transmission of LSDV have been carried out. In late 2008 a pilot study on the potential role of hard ticks in the transmission of LSDV was undertaken by the Capripoxvirus Reference Laboratory, IAH, UK and the Department of Veterinary Tropical Diseases, University of Pretoria, South Africa. LSD viral antigen was demonstrated in mouthparts, salivary glands and gut of three tick species, commonly found in Africa, post-feeding on the skin lesions of experimentally infected cattle. The viral antigen was also demonstrated in skin biopsies collected from the feeding sites of the infected ticks on non-infected recipient animals. In addition, viral DNA was demonstrated in eggs laid by female ticks previously fed on the skin lesions of infected cattle. Although these findings do not prove that the virus found in the ticks was still infective, it suggests that the mechanical, transstadial and transovarial transmission of LSDV may occur and further investigations are required. The aim of this study is to investigate the transmission of LSDV by three African ticks species. Laboratory-bred larvae, nymphs and adult ticks will be placed to feed on the skin of cattle experimentally infected with LSDV. Post-feeding partially engorged adult males and females or larvae hatched from eggs laid by females previously fed on LSD skin lesions will be placed to feed on the skin of non-infected animals. Nymphs will be allowed to develop to adults and then the unengorged adults will be transferred to feed on the skin of noninfected animals. The recipient animals will be closely monitored for clinical signs of LSD, samples will be collected at different intervals to detect viraemia, seroconversion and the presence of live virus in the skin of the non-infected animals. Detailed studies will be carried out on the persistence of the virus in different cell types of larvae, nymphs and adult ticks. Also, the effect of the severity of the infection in the host and of the environmental variables (temperature and humidity) on the transmission of LSDV by tick vectors and on viral multiplication rates and dissemination in ticks will be studied. The impact of the study will include the improved control of the LSD and therefore the improved welfare of the farming communities, families, nutritional and education status of the children in endemic countries. In addition, it will affect governmental policies on the international trade of live ruminants and on the potential spread of the disease caused by climate-change and an increase in abundance of tick populations.

Technical Summary

Lumpy skin disease (LSD) is an economically devastating poxviral infection of cattle in Africa and the Middle East. The virus is secreted in saliva, ocular and nasal discharge and semen of infected animals but direct contact is considered to be a relatively ineffective route of transmission. The occurrence of disease outbreaks has been connected to wet and warm weather conditions, and to the abundance of insect populations. However, little is known of the importance of insects as field vectors of the disease and no studies have been undertaken on the role of hard ticks in the transmission of the disease. The aim of the proposed research is to investigate the transmission of lumpy skin disease virus (LSDV) between cattle by different life stages of A. hebraeum, R. appendiculatus and B. decoloratus ticks. All of these ticks are common in Africa. Laboratory-bred larvae, nymphs and adults will be placed to feed on the skin of the cattle experimentally infected with LSDV. Post-feeding the partially engorged adult R. appendiculatus and A. hebraeum males, and larvae hatched from eggs laid by females, previously fed on the skin lesions of cattle with LSD, will be transferred to feed on the skin of non-infected recipient animals. Infected A. hebraeum and R. appendiculatus nymphs will be allowed to moult to adults and then transferred to feed on the skin of non-infected cattle. The recipient animals will be monitored for clinical signs of LSD. Samples will be collected at regular intervals to detect viraemia and seroconversion, and live virus in the skin of the previously non-infected animals. Also, the survival mechanisms of the virus during the moulting of the ticks and the influence of ambient temperature on virogenesis in nymphal stages of ticks and the possible presence of live virus or viral antigen in tick salivary glands, the cells of the midgut and eggs will be investigated.

Planned Impact

No previous studies on the transmission of LSDV by hard ticks have been undertaken. This study will provide fundamental data on the transmission of LSDV and it will significantly improve the understanding of the epidemiology of LSD. The insect vector has been demonstrated to be able to transmit the virus but the importance of this phenomenon in field conditions is not fully understood. In case LSDV is transmitted by hard tick vector, further investigation on the potential reservoir for the virus between outbreaks such as wild ruminants infested by the same tick species as cattle will be undertaken. Due to the close relatedness of the members of the Capripoxvirus genus hard ticks may transmitt sheep pox and goat pox viruses as well. Therefore further studies are required in order to investigate the transmission of sheep pox and goat pox virus by hard tick vectors. In addition to northern Africa sheep and goat pox is endemic also in the Middle East, Indian subcontinent and in most Asian countries which make the potential impact of this study substantial. The other poxviruses of veterinary importance, such as camel pox and ORF will benefit on the data obtained from this study. Camel pox virus belongs to the genus Orthopoxvirus within the Poxviridae family. The clinical signs and the epidemiology of camel pox are very similar to Capripox virus infections. Wernery et al. (1997) were able to isolate camel pox virus on cell cultures and the virus was also detected by electron microscopy in samples obtained from camel ticks (Hyalomma dromedarii) collected from infected camels. Previously several poxviruses have been showed to be transmitted by insect vectors but this study on hard tick vector is novel. The impact of this study for the community can be divided into three components, namely impact to the farming community, to the work of field veterinarians and the preventative health care of the cattle and to the work of governmental veterinary authorities. The impact of this study for the livelihood of poor farmers, small holders and the cattle farming industry as a whole is significant. If the ticks will be shown to be able to transmit the disease the eradication and control measures of the disease can be targeted to improve tick treatment of cattle in addition to other control measures. Fields veterinarians in Africa and in the Middle East should be aware of the potential role of ticks in the transmission of LSDV between cattle. This study will have direct effect on tick treatment policy recommended by the veterinary authorities. Governmental veterinary authorities responsible for the export and import policy for live domestic and wild ruminants should be informed on the potential role of hard tick vector in the transmission of LSDV. Scientists working with the tick research and vector-borne viruses will obtain fundamental data from this study. African swine fever virus (ASFV) is the other large, enveloped virus, in which the genome consists of a single molecule of linear double-stranded DNA. Both LSDV and ASFV replicate in the cytoplasm of the cells. In addition to the oronasal route of transmission, ASFV is transmitted by soft ticks of the Ornithodoros genus. The virus replicates in ticks and transstadial, transovarial and sexual transmission have been demonstrated in these ticks. The transmission of ASFV by soft tick vector has previously been studied in detail but since LSDV and ASFV share common features this study may provide new data for ASF as well. Female students will be encouraged to participate in the project. In addition to the tick expertise, the PhD project will provide the student with skills to perform the diagnostic tests for the detection of LSD antigen and antibodies. In countries where LSD is endemic, a rapid laboratory confirmation or tentative diagnosis of the disease is crucial for the swift implementation of the effective control measures which in turn may prevent the further spread of the diseas

Publications

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Abutarbush SM (2016) Adverse Reactions to Field Vaccination Against Lumpy Skin Disease in Jordan. in Transboundary and emerging diseases

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Lubinga J.C. (2012) Vector potential of Amblyomma hebraeum in the transmission of lumpy skin disease virus in Parasitological Society of South Africa, Bloemfontein, South Africa, October 1-3rd

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Lubinga J.C. (2012) Detection of lumpy skin disease virus in saliva of Amblyomma hebraeum and Rhipicephalus appendiculatus ticks post-feeding on experimentally infected cattle in Faculty Day, Faculty of Veterinary Science, University of Pretoria, South Africa, September 10th

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Tuppurainen E.S.M. (2012) Capripoxviruses - General overview in Sample Management -training course for 120 Ugandan goverment field veterinarians, Entebbe, Uganda September 3rd -6th

 
Description 1. Mechanical transmission of lumpy skin disease virus from the experimentally infected to naive animal was demonstrated via the mouthparts of Rhipicephalus appendicultaus male ticks
2. After feeding on infected cattle Boophilus decoloratus females were able to pass the virus via their eggs to subsequent larvae. When these larvae were transferred to feed on naive animal it became viraemic and developed skin lesions from which viral DNA was detected using a PCR method
3. Viraemic animals without skin lesions were able to transmit the virus between infected and naive cattle via tick vectors
4. Using PCR and virus isolation, the presence of the virus has been detected in experimentally-induced saliva samples collected from A. hebraeum and R. appendiculatus males after feeding on LSDV-infected cattle
5. Evidence of vertical transmission of the virus by R. appendiculatus was obtained
6. The presence of the virus was also demonstrated using immunohistochemical staining in various tick organs including midgut, salivary glands, ovaries, testes, and fat body, demonstrating that the virus was able to pass from the midgut into the haemocoel
Exploitation Route The role of ticks in transmission of LSDV should be taken into consideration in control and eradication of LSDV in infected countries and when requirements are set for the importation of live cattle from affected countries
Sectors Agriculture, Food and Drink

 
Description This study has a significant impact on better understanding of the epidemiology and transmission of lumpy skin disease affecting the control and eradication measures of the disease. In addition, the data on the role of tick vectors for LSDV have been used to suggest new recommendations set for the international trade of live cattle from infected countries given by the OIE Manual Code. Cattle in Africa are kept not only for the production of milk and meat or draft power; the socioeconomic impact of LSD for the wellbeing of poor rural communities is therefore substantial due to the total loss of production of infected animals. The control of LSDV in endemic countries is therefore of paramount importance.
First Year Of Impact 2013
Sector Agriculture, Food and Drink
Impact Types Economic,Policy & public services

 
Description OIE recommendations for the importation of live ruminants from countries concidered infected with lumpy skin disease
Policy Influence Type Participation in advisory committee
Impact The OIE Terrestrial Code Commission was provided with a recommendation that acaricide treatment of cattle should be added to the conditions set for the importation of live domestic or wild ruminants from countries concidered infected with lumpy skin disease
 
Description Provision of monoclonal antibody for lumpy skin disease virus 
Organisation National Centre for Foreign Animal Diseases (NCFAD)
Country Canada 
Sector Public 
PI Contribution Monoclonal antibody is required for immunohistochemical staining of the samples obtained from the experiment
Start Year 2010
 
Description collaboration with the Department of Veterinary Tropical Diseases (DVTD), University of Pretoria, South Africa 
Organisation University of Pretoria
Department Department of Veterinary Tropical Diseases
Country South Africa 
Sector Academic/University 
PI Contribution The PhD student at the DVTD investigates the presence of live LSDV or viral antigen using PCR, virus isolation, electron microscopy or immunoperoxidase staining in saliva and salivary glands and/or gut cells and eggs of ticks. The influence of ambient temperature on virogenesis in nymphal stages of A. hebraeum and R. appendiculatus, which may elucidate an overwintering mechanism of the virus is included into his PhD project.
Start Year 2010
 
Description Detection of lumpy skin disease virus in saliva of Amblyomma hebraeum and Rhipicephalus appendiculatus ticks post feeding on experimentally infected cattle 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research or patient groups
Results and Impact Oral presentation given by PhD student Jimmy Lubinga, Faculty Day, Faculty of Veterinary Science, University of Pretoria, South Africa, 10.09.2012 Oral presentation given by PhD student Jimmy Lubinga at the Faculty Day of the Veterinary Faculty, University of Pretoria Scientific data obtained from this study disseminated

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description Determination of the role of ixodid (hard) ticks in the transmission of lumpy skin disease virus 
Form Of Engagement Activity Scientific meeting (conference/symposium etc.)
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Participants in your research or patient groups
Results and Impact Presentation in the 30th World Veterinary Congress, Cape Town, South Africa, 10-14th October 2012 http://www.worldvetcongress2011.com

no actual impacts realised to date
Year(s) Of Engagement Activity 2011
URL http://www.worldvetcongress2011.com
 
Description Lecture: Tick vectors for lumpy skin disease virus 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach local
Primary Audience Postgraduate students
Results and Impact A lecture on the role of hard ticks in the transmission of LSDV were given at the University of Surrey, Faculty of Health and Medical Sciences/ Department of Microbial & Cellular Sciences, MSc course in Veterinary Microbiology (Module 5: Transmission and control of infectious diseases of animals (Vectors)) Power Point presentation

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description Lumpy skin disease - emerging threat to the Middle East and Europe 
Form Of Engagement Activity Scientific meeting (conference/symposium etc.)
Part Of Official Scheme? Yes
Geographic Reach international
Primary Audience Participants in your research or patient groups
Results and Impact Presentation on given by Eeva Tuppurainen in the World Organization for Animal Health (OIE) Subregional workshop on Lumpy skin disease and other vector-borne diseases, 28th Feb 2013, Larnaca Cyprus. The transmission of the virus by tick vectors was included into the presentation.
Research data on tick vectors for LSDV obtained from this project was disseminated in the meeting. Participants: chief veterinary authorities from Israel, Palestine, Egypt, Lebanon, Syria, Jordan, Cyprus and Iraq. Due to the potential contamination of the environment by LSDV infected tick eggs or larvae the importance of regular vaccination campaigns and acaricide treatment of cattle was emphasized.


Recommedations were given for the control and eradication measures for the lumpy skin disease in the Middle East region. The importance of acaricide treatment of cattle and regular vaccination campaigns was emphasized due to the transmission of the virus by tick and insect vectors

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
Description Poster: Mechanical and transstadial transmission of lumpy skin disease virus by Rhipicephalus appendiculatus and Amblyomma hebraeum ticks 
Form Of Engagement Activity Scientific meeting (conference/symposium etc.)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research or patient groups
Results and Impact Poster to be presented at the IX International Congress of Veterinary Virology, 4 - 7 September, Madrid. Spain Scientific data obtained from this study disseminated

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description Presentation at 30th World Veterinary Congress, Oct 2011, Cape Town 
Form Of Engagement Activity Scientific meeting (conference/symposium etc.)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Participants in your research or patient groups
Results and Impact Title of the presentation "Determination of the role of ixodid (hard) ticks in the transmission of lumpy skin disease virus" Leaflet, website

no actual impacts realised to date
Year(s) Of Engagement Activity 2011
 
Description University lecture entitled "The role of tick vectors in the transmission of lumpy skin disease virus" 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact University of Surrey, Faculty of Health and Medical Science, Department of Microbiological and Cellular Sciences, MSc course in Veterinary Microbiology, Module 5: Transmission and control of infectious diseases (vectors) Power Point presentation

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description Vector potential of Amblyomma hebraeum in the transmission of lumpy skin disease virus 
Form Of Engagement Activity Scientific meeting (conference/symposium etc.)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Oral presentation given by PhD student JL in Annual Congress of the Parasitological Society of Southern Africa, 1-3 Oct 2012, Bloemfontein, South Africa Oral presentation given by PhD student Jimmy Lubinga given to scientists working on parasitology in southern Africa Scientific data obtained from this study disseminated

no actual impacts realised to date
Year(s) Of Engagement Activity 2012