An expert opinion assessment of blood-feeding arthropods based on their capacity to transmit African swine fever virus in Metropolitan France.
Ornithodoros
Tabanidae
African swine fever (ASF)
Stomoxys flies
arthropods
blood-feeding vector
culicoides
fleas
hard ticks
lice
mosquitoes
pig
sand flies
soft ticks
vectorial capacity
vectorial competence
virus
wild boar
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
May 2021
May 2021
Historique:
revised:
29
07
2020
received:
07
04
2020
accepted:
29
07
2020
pubmed:
5
8
2020
medline:
16
6
2021
entrez:
5
8
2020
Statut:
ppublish
Résumé
To deal with the limited literature data on the vectorial capacity of blood-feeding arthropods (BFAs) and their role in the transmission of African swine fever virus (ASFV) in Metropolitan France, a dedicated working group of the French Agency for Food, Environmental and Occupational Health & Safety performed an expert knowledge elicitation. In total, 15 different BFAs were selected as potential vectors by the ad hoc working group involved. Ten criteria were considered to define the vectorial capacity: vectorial competence, current abundance, expected temporal abundance, spatial distribution, longevity, biting rate, active dispersal capacity, trophic preferences for Suidae, probability of contact with domestic pigs and probability of contact with wild boar. Fourteen experts participated to the elicitation. For each BFA, experts proposed a score (between 0 and 3) for each of the above criteria with an index of uncertainty (between 1 and 4). Overall, all experts gave a weight for all criteria (by distributing 100 marbles). A global weighted sum of score per BFA was calculated permitting to rank the different BFAs in decreasing order. Finally, a regression tree analysis was used to group those BFAs with comparable likelihood to play a role in ASF transmission. Out of the ten considered criteria, the experts indicated vectorial competence, abundance and biting rate as the most important criteria. In the context of Metropolitan France, the stable fly (Stomoxys calcitrans) was ranked as the most probable BFA to be a vector of ASFV, followed by lice (Haematopinus suis), mosquitoes (Aedes, Culex and Anopheles), Culicoides and Tabanidea. Since scientific knowledge on their vectorial competence for ASF is scarce and associated uncertainty on expert elicitation moderate to high, more studies are however requested to investigate the potential vector role of these BFAs could have in ASFV spread, starting with Stomoxys calcitrans.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1190-1204Informations de copyright
© 2020 Wiley-VCH GmbH.
Références
Bailey, D. L., Whitfield, T. L., & Smittle, B. J. (1973). Flight and dispersal of the stable fly. Journal of Economic Entomology, 66(2), 410-411. https://doi.org/10.1093/jee/66.2.410
Baldacchino, F., Desquesnes, M., Mihok, S., Foil, L. D., Duvallet, G., & Jittapalapong, S. (2014). Tabanids: Neglected subjects of research, but important vectors of disease agents!. Infection, Genetics and Evolution, 28, 596-615. https://doi.org/10.1016/j.meegid.2014.03.029
Bartsch, S., Bauer, B., Wiemann, A., Clausen, P. H., & Steuber, S. (2009). Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasitology Research, 105(2), 373-380. https://doi.org/10.1007/s00436-009-1408-y
Breiman, L., Friedman, J. H., Olshen, R. A., & Stone, C. J. (Eds.) (1984). Classification and regression trees. Pacific Grove (CA): Chapman and Hall Publisher.
Chenais, E., Ståhl, K., Guberti, V., & Depner, K. (2018). Identification of wild boar-habitat epidemiologic cycle in African swine fever epizootic. Emerging Infectious Diseases, 24(4), 810-812. https://doi.org/10.3201/eid2404.172127
Cooksey, L. M., & Wright, R. E. (1987). Flight range and dispersal activity of the host-seeking horse fly, Tabanus abactor (Diptera: Tabanidae), in North Central Oklahoma. Environmental Entomology, 16, 211-217. https://doi.org/10.1093/ee/16.1.211
Costard, S., Mur, L., Lubroth, J., Sanchez-Vizcaino, J. M., & Pfeiffer, D. U. (2013). Epidemiology of African swine fever virus. Virus Research, 173(1), 191-197. https://doi.org/10.1016/j.virusres.2012.10.030
EFSA (2010). Scientific opinion on the role of tick vectors in the epidemiology of crimean-congo hemorrhagic fever and African swine fever in Eurasia. Parma, Italy: European Food Safety Authority (EFSA).
EFSA (2018). Epidemiological analyses of African swine fever in the European Union. Parma, Italy: European Food Safety Authority (EFSA). (November 2017 until November 2018).
Estrada-Peña, A., Gray, J. S., Kahl, O., Lane, R. S., & Nijhof, A. M. (2013). Research on the ecology of ticks and tick-borne pathogens-methodological principles and caveats. Frontiers in Cellular and Infection Microbiology, 3, 29. https://doi.org/10.3389/fcimb.2013.00029
Fasina, F. O., Lazarus, D. D., Spencer, B. T., Makinde, A. A., & Bastos, A. D. (2012). Cost implications of African swine fever in smallholder farrow-to-finish units: Economic benefits of disease prevention through biosecurity. Transboundary and Emerging Diseases, 59(3), 244-255. https://doi.org/10.1111/j.1865-1682.2011.01261.x
Fischer, O., Mátlová, L., Dvorská, L., Svástová, P., Bartl, J., Melichárek, I., … Pavlík, I. (2001). Diptera as vectors of mycobacterial infections in cattle and pigs. Medical and Veterinary Entomology, 15(2), 208-211. https://doi.org/10.1046/j.1365-2915.2001.00292.x
Foil, L. D., & Hogsette, J. A. (1994). Biology and control of tabanids, stable flies and horn flies. Revue Scientifique Et Technique (International Office of Epizootics), 13, 1125-1158. https://doi.org/10.20506/rst.13.4.821
Galindo, I., & Alonso, C. (2017). African swine fever virus: A review. Viruses, 9(5), E103. https://doi.org/10.3390/v9050103
Garigliany, M., Desmecht, D., Tignon, M., Cassart, D., Lesenfant, C., Paternostre, J., … Linden, A. (2019). Phylogeographic analysis of African swine fever virus, Western Europe, 2018. Emerging Infectious Diseases, 25(1), 184-186. https://doi.org/10.3201/eid2501.181535
Golnar, A. J., Martin, E., Wormington, J. D., Kading, R. C., Teel, P. D., Hamer, S. A., & Hamer, G. L. (2019). Reviewing the potential vectors and hosts of African swine fever virus transmission in the United States. Vector-Borne and Zoonotic Diseases, 19(7), 512-524. https://doi.org/10.1089/vbz.2018.2387
Gore, S. M. (1987). Biostatistics and the Medical Research Council. MRC News, 35, 19-20.
Gubbins, S., Carpenter, S., Baylis, M., Wood, J. L., & Mellor, P. S. (2008). Assessing the risk of bluetongue to UK livestock: Uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number. Journal of the Royal Society, Interface, 5(20), 363-371. https://doi.org/10.1098/rsif.2007.1110
Guinat, C., Gogin, A., Blome, S., Keil, G., Pollin, R., Pfeiffer, D. U., & Dixon, L. (2016). Transmission routes of African swine fever virus to domestic pigs: Current knowledge and future research directions. The Veterinary Record, 178(11), 262-267. https://doi.org/10.1136/vr.103593
Halasa, T., Bøtner, A., Mortensen, S., Christensen, H., Toft, N., & Boklund, A. (2016). Simulating the epidemiological and economic effects of an African swine fever epidemic in industrialized swine populations. Veterinary Microbiology, 193, 7-16. https://doi.org/10.1016/j.vetmic.2016.08.004
Hameed, M., Liu, K., Anwar, M. N., Wahaab, A., Li, C., Di, D., … Ma, Z. (2019). A viral metagenomic analysis reveals rich viral abundance and diversity in mosquitoes from pig farms. Transboundary and Emerging Diseases, https://doi.org/10.1111/tbed.13355
Herm, R., Tummeleht, L., Jürison, M., Vilem, A., & Viltrop, A. (2020). Trace amounts of African swine fever virus DNA detected in insects collected from an infected pig farm in Estonia. Veterinary Medicine and Science, 6(1), 100-104. https://doi.org/10.1002/vms3.200.
Hogsette, J., & Ruff, J. P. (1985). Stable fly (Diptera: Muscidae) migration in Northwest Florida. Environmental Entomology, 14(2), 170-175. https://doi.org/10.1093/ee/14.2.170
Humblet, M. F., Vandeputte, S., Albert, A., Gosset, C., Kirschvink, N., Haubruge, E., & Saegerman, C. (2012). Multidisciplinary and evidence-based method for prioritizing diseases of food-producing animals and zoonoses. Emerging Infectious Diseases, 18(4), https://doi.org/10.3201/eid1804.111151.
Kirkeby, C., Bodker, R., Stockmarr, A., Lind, P., & Heegaard, P. M. (2013). Quantifying dispersal of European culicoides (Diptera: Ceratopogonidae) vectors between farms using a novel mark-release-recapture technique. PLoS One, 8(4), e61269. https://doi.org/10.1371/journal.pone.0061269
Krinsky, W. L. (1976). Animal disease agents transmitted by horse flies and deer flies (Diptera: Tabanidae). Journal of Medical Entomology, 13, 225-275. https://doi.org/10.1093/jmedent/13.3.225
LaDeau, S. L., Allan, B. F., Leisnham, P. T., & Levy, M. Z. (2015). The ecological foundations of transmission potential and vector-borne disease in urban landscapes. Functional Ecology, 29, 889-901. https://doi.org/10.1111/1365-2435.12487
Lempereur, L., Sohier, C., Smeets, F., Maréchal, F., Berkvens, D., Madder, M., … Losson, B. (2018). Dispersal capacity of Haematopota spp. and Stomoxys calcitrans using a mark-release-recapture approach in Belgium. Medical and Veterinary Entomology, 32(3), 298-303. https://doi.org/10.1111/mve.12297
McGarry, J. W., & Baker, A. S. (1997). Observations on the mite fauna associated with adult Stomoxys calcitrans in the U.K. Medical and Veterinary Entomology, 11(2), 159-164. https://doi.org/10.1111/j.1365-2915.1997.tb00307.x
Mellor, P. S., Kitching, R. P., & Wilkinson, P. J. (1987). Mechanical transmission of capripox virus and African swine fever virus by Stomoxys calcitrans. Research in Veterinary Science, 43(1), 109-112. https://doi.org/10.1016/S0034-5288(18)30753-7
Middlekauff, W. W., & Lane, R. S. (1980). Adult and immature Tabanidae (Diptera) of California. Bulletin of the California Insect Survey, 22, 1-99.
Mulumba-Mfumu, L. K., Saegerman, C., Dixon, L. K., Madimba, K. C., Kazadi, E., Mukalakata, N. T., … Penrith, M. L. (2019). African swine fever: Update on Eastern, Central and Southern Africa. Transboundary and Emerging Diseases, 66(4), 1462-1480. https://doi.org/10.1111/tbed.13187
Nash, T. A. M. (1944). A low density of tsetse flies associated with a high incidence of sleeping sickness. Bulletin of Entomological Research, 35(1), 51. https://doi.org/10.1017/S0007485300005630
Niederwerder, M. C., Stoian, A. M. M., Rowland, R. R. R., Dritz, S. S., Petrovan, V., Constance, L. A., … Hefley, T. J. (2019). Infectious dose of African swine fever virus when consumed naturally in liquid or feed. Emerging Infectious Diseases, 25(5), 891-897. https://doi.org/10.3201/eid2505.181495
Oke, P. O., Oke, B. E., & Adejinmi, J. O. (2017). Swine farm infestation with Culicoides species (biting midges) in Zaria, Nigeria. Sokoto Journal of Veterinary Sciences, 15(2), 66-69. https://doi.org/10.4314/sokjvs.v15i2.10
Olesen, A. S., Hansen, M. F., Rasmussen, T. B., Belsham, G. J., Bødker, R., & Bøtner, A. (2018). Survival and localization of African swine fever virus in stable flies (Stomoxys calcitrans) after feeding on viremic blood using a membrane feeder. Veterinary Microbiology, 222, 25-29. https://doi.org/10.1016/j.vetmic.2018.06.010
Olesen, A. S., Lohse, L., Hansen, M. F., Boklund, A., Halasa, T., Belsham, G. J., … Bødker, R. (2018). Infection of pigs with African swine fever virus via ingestion of stable flies (Stomoxys calcitrans). Transboundary and Emerging Diseases, 65(5), 1152-1157. https://doi.org/10.1111/tbed.12918
Pautienius, A., Grigas, J., Pileviciene, S., Zagrabskaite, R., Buitkuviene, J., Pridotkas, G., … Stankevicius, A. (2018). Prevalence and spatiotemporal distribution of African swine fever in Lithuania, 2014-2017. Virology Journal, 15(1), 177. https://doi.org/10.1186/s12985-018-1090-8
Pereira de Oliveira, R., Hutet, E., Paboeuf, F., Duhayon, M., Boinas, F., Perez de Leon, A., … Le Potier, M. F. (2019). Comparative vector competence of the Afrotropical soft tick Ornithodoros moubata and Palearctic species, O. erraticus and O. verrucosus, for African swine fever virus strains circulating in Eurasia. PLoS One, 14(11), e0225657. https://doi.org/10.1371/journal.pone.0225657
Perie, P., Chermette, R., Millemann, Y., & Zientara, S. (2005). Culicoides, hematophagous Diptera vectors of Bluetongue disease. Bulletin De L'académie Vétérinaire De France, 158(3), 213-224. https://doi.org/10.4267/2042/47770
Petit, K., Dunoyer, C., Fischer, C., Hars, J., Baubet, E., López-Olvera, J. R., … Saegerman, C. (2020). Assessment of the impact of forestry and leisure activities on wild boar spatial disturbance with a potential application to ASF risk of spread. Transboundary and Emerging Diseases, 67(3), 1164-1176. https://doi.org/10.1111/tbed.13447.
Petrasiunas, A., Bernotiene, R., & Turcinaviciene, J. (2018). Catches of blood-feeding flies with NZI traps in African Swine Fever affected areas of Lithuania. Bulletin of the Lithuanian Entomological Society, 2(30), 112-118.
Pietschmann, J., Mur, L., Blome, S., Beer, M., Pérez-Sánchez, R., Oleaga, A., & Sánchez-Vizcaíno, J. M. (2016). African swine fever virus transmission cycles in Central Europe: Evaluation of wild boar-soft tick contacts through detection of antibodies against Ornithodoros erraticus saliva antigen. BMC Veterinary Research, 12, 1. https://doi.org/10.1186/s12917-015-0629-9
Plateforme ESA (2019). Bulletin hebdomadaire de veille santé animale du 17/12/2019. Accessed at 22 December 2019, URL: https://www.plateforme-esa.fr/bulletin-hebdomadaire-de-veille-sante-animale-du-17-12-2019
Podgorski, T., & Smietanka, K. (2018). Do wild boar movements drive the spread of African swine fever? Transboundary and Emerging Diseases, 65(6), 1588-1596. https://doi.org/10.1111/tbed.12910
Price, D. A., & Hardy, W. T. (1954). Isolation of the bluetongue virus from Texas sheep-Culicoides shown to be a vector. Journal of the American Veterinary Medical Association, 124(925), 255-258.
Rasmussen, L. D., Kristensen, B., Kirkeby, C., Rasmussen, T. B., Belsham, G. J., Bødker, R., & Bøtner, A. (2012). Culicoids as vectors of Schmallenberg virus. Emerging Infectious Diseases, 18(7), 1204-1206. https://doi.org/10.3201/eid1807.120385
Rodhain, F. (1985). Arbovirus-vector relations. Bulletin De La Societe De Pathologie Exotique Et De Ses Filiales, 78(5), 763-768.
Rodhain, F. (1991). Le fonctionnement des systèmes virus-vecteurs. Annales De La Société Belge De Médecine Tropicale, 71(1), 189-199.
Rowlands, R. J., Michaud, V., Heath, L., Hutchings, G., Oura, C., Vosloo, W., … Dixon, L. K. (2008). African swine fever virus isolate, Georgia, 2007. Emerging Infectious Diseases, 14(12), 1870-1874. https://doi.org/10.3201/eid1412.080591
Saegerman, C. (2018). Découverte inattendue de la peste porcine africaine en Belgique. Epidémiologie Et Santé Animale, 73, 147-164.
Saegerman, C., Berkvens, D., & Mellor, P. S. (2008). Bluetongue epidemiology in the European Union. Emerging Infectious Diseases, 14(4), 539-544. https://doi.org/10.3201/eid1404.071441
Saegerman, C., Porter, S. R., & Humblet, M. F. (2011). The use of modelling to evaluate and adapt strategies for animal disease control. Revue Scientifique Et Technique, 30(2), 555-569. https://doi.org/10.20506/rst.30.2.2048
Sanchez-Botija, C., & Badiola, C. (1966). Presencie of the African swine pest virus in Haematopinus suis. Bulletin-Office International Des Epizooties, 66(1), 699-705.
Sanchez-Botija, C.(1963). Reservorios del virus de la peste porcina Africana. Investigacion del virus la P.P.A en los artropodos mediante la prueba de la hemoadsorcion. Bulletin-Office International Des Epizooties, 60, 895-899.
Sánchez-Vizcaíno, J. M., Mur, L., & Martínez-López, B. (2013). African swine fever (ASF): Five years around Europe. Veterinary Microbiology, 165(1-2), 45-50. https://doi.org/10.1016/j.vetmic.2012.11.030
Schulz, K., Conraths, F. J., Blome, S., Staubach, C., & Sauter-Louis, C. (2019). African swine fever: Fast and furious or slow and steady? Viruse, 11(9), E866. https://doi.org/10.3390/v11090866
Zimmer, J. Y., Haubruge, E., Francis, F., Bortels, J., Joie, E., Simonon, G., … Kirschvink, N. (2008). Distribution of potential bluetongue vectors on Belgium farms. The Veterinary Record, 162(21), 700. https://doi.org/10.1136/vr.162.21.700