Potential mechanical transmission of Lumpy skin disease virus (LSDV) by the stable fly (Stomoxys calcitrans) through regurgitation and defecation

ABSTRACT Lumpy skin disease virus (LSDV) is a vector-transmitted poxvirus that causes disease in cattle. Vector species involved in LSDV transmission and their ability to acquire and transmit the virus are poorly characterized. Using a highly representative bovine experimental model of lumpy skin disease, we fed four model vector species (Aedes aegypti, Culex quinquefasciatus, Stomoxys calcitrans, and Culicoides nubeculosus) on LSDV-inoculated cattle in order to examine their acquisition and retention of LSDV. Subclinical disease was a more common outcome than clinical disease in the inoculated cattle. Importantly, the probability of vectors acquiring LSDV from a subclinical animal (0.006) was very low compared with that from a clinical animal (0.23), meaning an insect feeding on a subclinical animal was 97% less likely to acquire LSDV than one feeding on a clinical animal. All four potential vector species studied acquired LSDV from the host at a similar rate, but Aedes aegypti and Stomoxys calcitrans retained the virus for a longer time, up to 8 days. There was no evidence of virus replication in the vector, consistent with mechanical rather than biological transmission. The parameters obtained in this study were combined with data from studies of LSDV transmission and vector life history parameters to determine the basic reproduction number of LSDV in cattle mediated by each of the model species. This reproduction number was highest for Stomoxys calcitrans (19.1), followed by C. nubeculosus (7.1) and Ae. aegypti (2.4), indicating that these three species are potentially efficient transmitters of LSDV; this information can be used to inform LSD control programs. IMPORTANCE Lumpy skin disease virus (LSDV) causes a severe systemic disease characterized by cutaneous nodules in cattle. LSDV is a rapidly emerging pathogen, having spread since 2012 into Europe and Russia and across Asia. The vector-borne nature of LSDV transmission is believed to have promoted this rapid geographic spread of the virus; however, a lack of quantitative evidence about LSDV transmission has hampered effective control of the disease during the current epidemic. Our research shows subclinical cattle play little part in virus transmission relative to clinical cattle and reveals a low probability of virus acquisition by insects at the preclinical stage. We have also calculated the reproductive number of different insect species, therefore identifying efficient transmitters of LSDV. This information is of utmost importance, as it will help to define epidemiological control measures during LSDV epidemics and of particular consequence in resource-poor regions where LSD vaccination may be less than adequate.

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Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera: Culicidae)

Epidemiology and Infection ◽

10.1017/s0950268801005179 ◽

2001 ◽

Vol 126 (2) ◽

pp. 317-321 ◽

Cited By ~ 120

Author(s):

C. M. CHIHOTA ◽

L. F. RENNIE ◽

R. P. KITCHING ◽

P. S. MELLOR

Keyword(s):

Aedes Aegypti ◽

Disease Virus ◽

Skin Disease ◽

Mosquito Species ◽

Clinical Disease ◽

Mechanical Transmission ◽

Infected Cattle ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus

Aedes aegypti female mosquitoes are capable of the mechanical transmission of lumpy skin disease virus (LSDV) from infected to susceptible cattle. Mosquitoes that had fed upon lesions of LSDV-infected cattle were able to transmit virus to susceptible cattle over a period of 2–6 days post-infective feeding. Virus was isolated from the recipient animals in 5 out of 7 cases. The clinical disease recorded in the animals exposed to infected mosquitoes was generally of a mild nature, with only one case being moderate. LSDV has long been suspected to be insect transmitted, but these findings are the first to demonstrate this unequivocally, and they suggest that mosquito species are competent vectors.

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Mechanical Transmission of Lumpy Skin Disease Virus by Stomoxys spp. (Stomoxys calsitrans, Stomoxys sitiens, Stomoxys indica), Diptera: Muscidae

Animals ◽

10.3390/ani10030477 ◽

2020 ◽

Vol 10 (3) ◽

pp. 477

Author(s):

Arman Issimov ◽

Lespek Kutumbetov ◽

Mukhit B. Orynbayev ◽

Berik Khairullin ◽

Balzhan Myrzakhmetova ◽

...

Keyword(s):

Disease Virus ◽

Skin Disease ◽

Clinical Signs ◽

Severe Case ◽

Mechanical Transmission ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus ◽

First Time

Samples collected for PCR from recipient animals tested positive in 5 out of 6 cases, while the virus was isolated from 4 of 6 animals. The clinical signs exhibited by recipient animals were mostly moderate in nature with only one severe case. To our knowledge, this is the first time that transmission of LSDV by three Stomoxys species has been demonstrated, and their role as mechanical vectors of LSDV is indicated.

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Evidence of Transstadial and Mechanical Transmission of Lumpy Skin Disease Virus byAmblyomma hebraeumTicks

Transboundary and Emerging Diseases ◽

10.1111/tbed.12102 ◽

2013 ◽

Vol 62 (2) ◽

pp. 174-182 ◽

Cited By ~ 29

Author(s):

J. C. Lubinga ◽

E. S. M. Tuppurainen ◽

R. Mahlare ◽

J. A. W. Coetzer ◽

W. H. Stoltsz ◽

...

Keyword(s):

Disease Virus ◽

Skin Disease ◽

Mechanical Transmission ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus

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Quantifying and modelling the acquisition and retention of lumpy skin disease virus by haematophagus insects reveals clinically but not subclinically-affected cattle are promoters of viral transmission and key targets for control of disease outbreaks

10.1101/2020.06.18.154252 ◽

2020 ◽

Author(s):

Beatriz Sanz-Bernardo ◽

Ismar R. Haga ◽

Najith Wijesiriwardana ◽

Sanjay Basu ◽

Will Larner ◽

...

Keyword(s):

Aedes Aegypti ◽

Disease Virus ◽

Skin Disease ◽

Control Measures ◽

Stomoxys Calcitrans ◽

Effective Control ◽

Vector Species ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus

AbstractLumpy skin disease virus (LSDV), a poxvirus that causes severe disease in cattle, has in the last few years rapidly extended its distribution from Africa and the Middle East into Europe, Russia, and across Asia. LSDV is believed to be primarily spread mechanically by blood-feeding arthropods, however the exact mode of arthropod transmission, the relative ability of different arthropod species to acquire and retain the virus, as well as their comparative importance for LSDV transmission, remain poorly characterised. Since the vector-borne nature of LSDV transmission is believed to have enabled the rapid geographic expansion of this virus, the lack of quantitative evidence on LSDV transmission has impeded effective control of the disease during the current epidemic. Obtaining high quality data on virus transmission by arthropods is challenging, and practical limitations often result in inadequate arthropod numbers or model hosts, limiting the transferability of experimental findings to the natural transmission scenario.We have addressed these limitations in this study. Using a highly representative bovine experimental model of lumpy skin disease we allowed four representative vector species (Aedes aegypti, Culex quinquefasciatus, Stomoxys calcitrans and Culicoides nubeculosus) to blood-feed on LSDV-inoculated cattle in order to examine the acquisition and retention of LSDV by these species in unprecedented detail. We found the probability of LSDV transmission from clinical cattle to vector correlated with disease severity. Subclinical disease was more common than clinical disease in the inoculated cattle, however the probability of vectors acquiring LSDV from subclinical animals was very low.All four potential vector species studied had a similar rate of acquisition of LSDV after feeding on the host, but Aedes aegypti and Stomoxys calcitrans retained the virus for a longer time, up to 8 days. There was no evidence of virus replication in the vector, consistent with mechanical rather than biological transmission. The parameters obtained in the in-vivo transmission experiments subsequently enabled enhanced modelling approaches to determine the basic reproduction number of LSDV in cattle mediated by each of the insect species. This was highest for Stomoxys calcitrans (19.1), C. nubeculosus (7.4), and Ae. aegypti (2.4), surprisingly indicating these three species are all potentially efficient transmitters of LSDV. These results reveal that currently applied LSDV control measures such as stamping out of all cattle on affected premises or insect control measures targeting single species need to be urgently reconsidered. Overall our studies have highlighted that the combination of highly relevant in-vivo experiments and mathematical modelling can be directly applied to devise evidence-based proportionate and targeted control programmes.

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Retention of lumpy skin disease virus in Stomoxys spp (Stomoxys calcitrans, Stomoxys sitiens, Stomoxys indica) following intrathoracic inoculation, Diptera: Muscidae

PLoS ONE ◽

10.1371/journal.pone.0238210 ◽

2021 ◽

Vol 16 (2) ◽

pp. e0238210

Author(s):

Arman Issimov ◽

David B. Taylor ◽

Malik Shalmenov ◽

Birzhan Nurgaliyev ◽

Izimgali Zhubantayev ◽

...

Keyword(s):

Disease Virus ◽

Skin Disease ◽

Virus Isolation ◽

Emerging Disease ◽

Stomoxys Calcitrans ◽

Post Inoculation ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus ◽

Means Of Transmission ◽

Intrathoracic Inoculation

Lumpy skin disease (LSD) is an emerging disease of cattle in Kazakhstan and the means of transmission remains uncertain. In the current study, retention of Lumpy Skin Disease Virus (LSDV) by three Stomoxys species following intrathoracic inoculation was demonstrated under laboratory conditions. A virulent LSDV strain was injected into the thorax of flies to bypass the midgut barrier. The fate of the pathogen in the hemolymph of the flies was examined using PCR and virus isolation tests. LSDV was isolated from all three Stomoxys species up to 24h post inoculation while virus DNA was detectable up to 7d post inoculation.

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Using the basic reproduction number to assess the risk of transmission of lumpy skin disease virus by biting insects

10.1101/602292 ◽

2019 ◽

Author(s):

Simon Gubbins

Keyword(s):

Disease Virus ◽

Basic Reproduction Number ◽

Skin Disease ◽

Reproduction Number ◽

Sensitivity Analyses ◽

Published Data ◽

Mechanical Transmission ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus ◽

The Basic Reproduction Number

SummaryIn recent years, lumpy skin disease virus (LSDV) has emerged as a major threat to cattle outside Africa, where it is endemic. Although evidence suggests that LSDV is transmitted by the bites of blood sucking arthropods, few studies have assessed the risk of transmission posed by particular vector species. Here this risk is assessed by calculating the basic reproduction number (R0) for transmission of LSDV by five species of biting insect: the stable fly, Stomoxys calcitrans, the biting midge, Culicoides nubeculosus, and three mosquito species, Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. Parameters relating to mechanical transmission of LSDV were estimated using new analyses of previously-published data from transmission experiments, while vector life history parameters were derived from the published literature. Uncertainty and sensitivity analyses were used to compute R0 for each species and to identify those parameters which influence its magnitude. Results suggest that S. calcitrans is likely to be the most efficient at transmitting LSDV, with Ae. aegypti also an efficient vector. By contrast, C. nubeculosus, An. stephensi, and Cx. quinquefasciatus are likely to be inefficient vectors of LSDV. However, there is considerable uncertainty associated with the estimates of R0, reflecting uncertainty in most of the constituent parameters. Sensitivity analysis suggests that future experimental work should focus on estimating the probability of transmission from insect to bovine and on the virus inactivation rate in insects.

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Attempted mechanical transmission of lumpy skin disease virus by biting insects

Medical and Veterinary Entomology ◽

10.1046/j.1365-2915.2003.00445.x ◽

2003 ◽

Vol 17 (3) ◽

pp. 294-300 ◽

Cited By ~ 63

Author(s):

C. M. Chihota ◽

L. F. Rennie ◽

R. P. Kitching ◽

P. S. Mellor

Keyword(s):

Disease Virus ◽

Skin Disease ◽

Mechanical Transmission ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus

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Mechanical transmission of lumpy skin disease virus by Rhipicephalus appendiculatus male ticks

Epidemiology and Infection ◽

10.1017/s0950268812000805 ◽

2012 ◽

Vol 141 (2) ◽

pp. 425-430 ◽

Cited By ~ 50

Author(s):

E. S. M. TUPPURAINEN ◽

J. C. LUBINGA ◽

W. H. STOLTSZ ◽

M. TROSKIE ◽

S. T. CARPENTER ◽

...

Keyword(s):

Disease Virus ◽

Skin Disease ◽

Clinical Signs ◽

Viral Disease ◽

Rhipicephalus Appendiculatus ◽

Mechanical Transmission ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus ◽

Feeding Site ◽

Source Of Infection

SUMMARYLumpy skin disease (LSD) is an economically important, acute or sub-acute, viral disease of cattle that occurs across Africa and in the Middle East. The aim of this study was to investigate if lumpy skin disease virus (LSDV) can be transmitted mechanically by African brown ear ticks (Rhipicephalus appendiculatus Neum.). Laboratory-bred R. appendiculatus males were fed on experimentally infected viraemic ‘donor’ cattle. Partially fed male ticks were then transferred to feed on an uninfected ‘recipient’ cow. The recipient animal became viraemic, showed mild clinical signs of LSD and seroconverted. Additionally, R. appendiculatus males were found to transmit LSDV through feeding on skin lacking visible lesions, demonstrating that viraemic animals without lesions at the feeding site of ticks may be a source of infection. This is the first time that transmission of poxviruses by a tick species has been demonstrated and the importance of this mode of transmission in the spread of LSDV in endemic settings is discussed.

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Comparative Evaluation of Lumpy Skin Disease Virus-Based Live Attenuated Vaccines

Vaccines ◽

10.3390/vaccines9050473 ◽

2021 ◽

Vol 9 (5) ◽

pp. 473

Author(s):

Andy Haegeman ◽

Ilse De Leeuw ◽

Laurent Mostin ◽

Willem Van Campe ◽

Laetitia Aerts ◽

...

Keyword(s):

Disease Virus ◽

Skin Disease ◽

Vaccination Campaign ◽

Ease Of Use ◽

Vaccine Failure ◽

Lumpy Skin Disease ◽

Lumpy Skin Disease Virus ◽

The Balkans ◽

The Past ◽

Preventative Strategy

Vaccines form the cornerstone of any control, eradication and preventative strategy and this is no different for lumpy skin disease. However, the usefulness of a vaccine is determined by a multiplicity of factors which include stability, efficiency, safety and ease of use, to name a few. Although the vaccination campaign in the Balkans against lumpy skin disease virus (LSDV) was successful and has been implemented with success in the past in other countries, data of vaccine failure have also been reported. It was therefore the purpose of this study to compare five homologous live attenuated LSDV vaccines (LSDV LAV) in a standardized setting. All five LSDV LAVs studied were able to protect against a challenge with virulent LSDV. Aside from small differences in serological responses, important differences were seen in side effects such as a local reaction and a Neethling response upon vaccination between the analyzed vaccines. These observations can have important implications in the applicability in the field for some of these LSDV LAVs.

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