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Experimental evidence of mechanical lumpy skin disease virus transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies.

ABSTRACT: Lumpy skin disease (LSD) is a devastating disease of cattle characterized by fever, nodules on the skin, lymphadenopathy and milk drop. Several haematophagous arthropod species like dipterans and ticks are suspected to play a role in the transmission of LSDV. Few conclusive data are however available on the importance of biting flies and horseflies as potential vectors in LSDV transmission. Therefore an in vivo transmission study was carried out to investigate possible LSDV transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies from experimentally infected viraemic donor bulls to acceptor bulls. LSDV transmission by Stomoxys calcitrans was evidenced in 3 independent experiments, LSDV transmission by Haematopota spp. was shown in one experiment. Evidence of LSD was supported by induction of nodules and virus detection in the blood of acceptor animals. Our results are supportive for a mechanical transmission of the virus by these vectors.

SUBMITTER: Sohier C

PROVIDER: S-EPMC6934832 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Experimental evidence of mechanical lumpy skin disease virus transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies.

Sohier C C Haegeman A A Mostin L L De Leeuw I I Campe W Van WV De Vleeschauwer A A Tuppurainen E S M ESM van den Berg T T De Regge N N De Clercq K K

Scientific reports 20191227 1

Lumpy skin disease (LSD) is a devastating disease of cattle characterized by fever, nodules on the skin, lymphadenopathy and milk drop. Several haematophagous arthropod species like dipterans and ticks are suspected to play a role in the transmission of LSDV. Few conclusive data are however available on the importance of biting flies and horseflies as potential vectors in LSDV transmission. Therefore an in vivo transmission study was carried out to investigate possible LSDV transmission by Stomo ...[more]

PMID: 31882819

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Project description:BACKGROUND:From a veterinary-medical point of view, the stable fly, Stomoxys calcitrans, is perhaps the economically most important blood-sucking muscoid fly species (Diptera: Muscidae), owing to its worldwide occurrence, frequently high local abundance, direct harm caused to livestock, pet animals and humans, as well as its vector role. Considering the latter in the context of protozoan parasites, the stable fly is a mechanical vector of trypanosomes and Besnoitia besnoiti. However, its role as a vector of piroplasms appears to be seldom studied, despite old data suggesting mechanical transmission of babesiae by dipteran flies. METHODS:In this study 395 stable flies (and one Haematobia stimulans) were collected at a cattle farm with known history of bovine theileriosis, and at further nine, randomly chosen locations in Hungary. These flies were separated according to sex (30 of them also cut into two parts: the head with mouthparts and the thorax-abdomen), followed by individual DNA extraction, then screening for piroplasms by PCR and sequencing. RESULTS:In stable flies, Theileria orientalis and T. capreoli were identified at the cattle farm and T. equi was identified in three other locations. At the cattle farm, significantly more male stable flies carried piroplasm DNA than females. There was no significant difference between the ratio of PCR-positive flies between the stable (void of cattle for at least two hours) and the pen on the pasture with cattle at the time of sampling. Among dissected flies (29 S. calcitrans and 1 H. stimulans), exclusively the thoracic-abdominal parts were PCR-positive, whereas the head and mouthparts remained negative. CONCLUSIONS:Theileria DNA is detectable in stable flies, in the case of T. orientalis at least for two hours after blood-feeding, and in the case of T. capreoli also in the absence of infected hosts (i.e. roe deer). Male flies rather than females, and thoracic-abdominal (most likely crop) contents rather than mouthparts may pose a risk of mechanical transmission. These data suggest that it is worth to study further the vector role of stable flies in the epidemiology of theilerioses, in which not the immediate, but rather the delayed type transmission seems possible.

Project description:The transmission of "lumpy skin disease virus" (LSDV) has prompted intensive research efforts due to the rapid spread and high impact of the disease in recent years, especially in Eastern Europe and Balkan countries. In this study, we experimentally evaluate the vaccine-derived virulent recombinant LSDV strain (Saratov/2017) and provide solid evidence on the capacity of the virus for transmission in a vector-proof environment. In the 60-day long experiment, we used inoculated bulls (IN group) and two groups of in-contact animals (C1 and C2), with the former (C1) being in contact with the inoculated animals at the onset of the trial and the latter (C2) being introduced at day 33 of the experiment. The infection in both groups of contact animals was confirmed clinically, serologically and virologically, and viremia was demonstrated in blood, nasal and ocular excretions, using molecular tools. Further studies into LSDV biology are a priority to gain insights into whether the hypothesized indirect contact mode evidenced in this study is a de novo-created feature, absent from both parental stains of the novel (recombinant) LSDV isolate used, or whether it was dormant, but then unlocked by the process of genetic recombination. Author summary: In global terms, LSD has been termed a "neglected disease" due to its historic natural occurrence of being restricted to Africa and, occasionally, Israel. However, after its slow spread throughout the Middle East, the disease is now experiencing a resurgence of research interest following a recent and rapid spread into more northern latitudes. Given the dearth of solid findings on potential transmission mechanisms, no efficient or reliable control program currently exists, which does not involve the use of live attenuated vaccines or stamping out policies - both of which are controversial for implementation in non-endemic regions or countries. The vector-borne mode is the only working concept currently available, but with scarce evidence to support the aggressive spread northwards - except for human-assisted spread, including legal or illegal animal transportation. The emergence of outbreaks is not consistently linked to weather conditions, with the potential for new outbreaks to occur and spread rapidly. Here, for the first time, we provide evidence for indirect contact-mode transmission for a naturally-occurring recombinant LSDV isolated from the field. In an insect-proof facility, we obtained solid evidence that the novel LSDV strain can pass to in-contact animals. Given the recombinant nature of the virus utilised, its genetic background relating to the observed transmission pattern within the study needs to be delineated.

Dataset Information

Experimental evidence of mechanical lumpy skin disease virus transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies.

Publications

Experimental evidence of mechanical lumpy skin disease virus transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies.

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