Potential routes for indirect transmission of African swine fever virus into domestic pig herds.
African swine fever virus
contaminated materials
domestic pig herds
indirect virus transmission
insects
pig meat
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Jul 2020
Jul 2020
Historique:
received:
07
01
2020
revised:
18
02
2020
accepted:
05
03
2020
pubmed:
10
3
2020
medline:
20
11
2020
entrez:
10
3
2020
Statut:
ppublish
Résumé
Following its introduction into Georgia in 2007, African swine fever virus (ASFV) has become widespread on the European continent and in Asia. In many cases, the exact route of introduction into domestic pig herds cannot be determined, but most introductions are attributed to indirect virus transmission. In this review, we describe knowledge gained about different matrices that may allow introduction of the virus into pig herds. These matrices include uncooked pig meat, processed pig-derived products, feed, matrices contaminated with the virus and blood-feeding invertebrates. Knowledge gaps still exist, and both field studies and laboratory research are needed to enhance understanding of the risks for ASFV introductions, especially via virus-contaminated materials, including bedding and feed, and via blood-feeding, flying insects. Knowledge obtained from such studies can be applied to epidemiological risk assessments for the different transmission routes. Such assessments can be utilized to help predict the most effective biosecurity and control strategies.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1472-1484Subventions
Organisme : University of Copenhagen
Organisme : Statens Serum Institut
Informations de copyright
© 2020 Blackwell Verlag GmbH.
Références
Alonso, C., Borca, M., Dixon, L., Revilla, Y., Rodriguez, F., & Escribano, J. M. (2018). ICTV virus taxonomy profile: Asfarviridae. Journal of General Virology, 99(5), 613-614. https://doi.org/10.1099/jgv.0.001049
Beltrán-Alcrudo, D., Lubroth, J., Depner, K., & De La Rocque, S. (2008). EMPRES watch. African swine fever in the Caucasus. Retrieved from: http://www.fao.org/docs/eims/upload/242232/ew_caucasus_apr08.pdf Accessed October 23 2019.
Boinas, F., Ribeiro, R., Madeira, S., Palma, M., de Carvalho, I. L., Núncio, S., & Wilson, A. J. (2014). The medical and veterinary role of Ornithodoros erraticus complex ticks (Acari: Ixodida) on the Iberian Peninsula. Journal of Vector Ecology, 39, 238-248. https://doi.org/10.1111/jvec.12098
Carlson, J., Zani, L., Henke, J., Leidenberger, S., Nurmoja, I., Tummeleht, L., …Blome, S. (2017). Soil as a vector for African swine fever virus in wild boar populations. 11th EPIZONE Annual Meeting, 19-21st of September 2017, Paris. EPIZONE abstract book, C35. Retrieved from: https://www.epizone-eu.net/upload_mm/4/9/b/12b5ead2-581f-4ab8-8b4f-fd0b587dce65_EPIZONE2017%20Abstract%20book.pdf Accessed November 12 2019.
Chenais, E., Depner, K., Guberti, V., Dietze, K., Viltrop, A., & Ståhl, K. (2019). Epidemiological considerations on African swine fever in Europe 2014-2018. Porcine Health Management, 5, 1-10. https://doi.org/10.1186/s40813-018-0109-2
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, 810-821. https://doi.org/10.3201/eid2404.172127
Costard, S., Mur, L., Lubroth, J., Sánchez-Vizcaíno, J. M., & Pfeiffer, D. U. (2013). Epidemiology of African swine fever virus. Virus Research, 173, 191-197. https://doi.org/10.1016/j.virusres.2012.10.030
Costard, S., Wieland, B., de Glanville, W., Jori, F., Rowlands, R., Vosloo, W., … Dixon, L. K. (2009). African swine fever: How can global spread be prevented? Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 2683-2696. https://doi.org/10.1098/rstb.2009.0098
Davies, K., Goatley, L. C., Guinat, C., Netherton, C. L., Gubbins, S., Dixon, L. K., & Reis, A. L. (2017). Survival of African swine fever virus in excretions from pigs experimentally infected with the Georgia 2007/1 isolate. Transboundary and Emerging Diseases, 64, 425-431. https://doi.org/10.1111/tbed.12381.
de Carvalho Ferreira, H. C., Weesendorp, E., Quak, S., Stegeman, J. A., & Loeffen, W. L. A. (2013). Quantification of airborne African swine fever virus after experimental infection. Veterinary Microbiology, 165, 243-251. https://doi.org/10.1016/j.vetmic.2013.03.007
de Carvalho Ferreira, H. C., Zúquete, S. T., Wijnveld, M., Weesendorp, E., Jongejan, F., Stegeman, A., & Loeffen, W. L. A. (2014). No evidence of African swine fever virus replication in hard ticks. Ticks and Tick-Borne Diseases, 5, 582-589. https://doi.org/10.1016/j.ttbdis.2013.12.012
Dee, S. A., Bauermann, F. V., Niederwerder, M. C., Singrey, A., Clement, T., de Lima, M., … Diel, D. G. (2018). Survival of viral pathogens in animal feed ingredients under transboundary shipping models. PLoS ONE, 13, e0194509. https://doi.org/10.1371/journal.pone.0194509
Diaz, A. V., Netherton, C. L., Dixon, L. K., & Wilson, A. J. (2012). African swine fever virus strain Georgia 2007/1 in Ornithodoros erraticus ticks. Emerging Infectious Diseases, 18, 1026-1028. https://doi.org/10.3201/eid1806.111728
Donaldson, A. I., & Ferris, N. P. (1976). The survival of some air-borne animal viruses in relation to relative humidity. Veterinary Microbiology, 1, 413-420. https://doi.org/10.1016/0378-1135(76)90056-0
Eble, P. L., Hagenaars, T. J., Weesendorp, E., Quak, S., Moonen-Leusen, H. W., & Loeffen, W. L. A. (2019). Transmission of African Swine Fever Virus via carrier (survivor) pigs does occur. Veterinary Microbiology, 237, 108345. https://doi.org/10.1016/j.vetmic.2019.06.018
EC (2014) African swine fever in Lithuania. SCoFcAH 21st of August 2014, State Food and Veterinary Service, Lithuania. Retrieved from: https://ec.europa.eu/food/sites/food/files/animals/docs/reg-com_ahw_20140821_pres_asf_lithuania.pdf. Accessed October 22, 2019.
ECDC (2019). Ornithodoros - current known distribution: January 2019. European Centre for Disease Prevention and Control. Retrieved from: https://www.ecdc.europa.eu/en/publications-data/ornithodoros-current-known-distribution-january-2019 Accessed October 22 2019.
EFSA (2017). Cortiñas Abrahantes, J., Gogin, A., Richardson, J., & Gervelmeyer, A. Scientific report on epidemiological analyses on African swine fever in the Baltic countries and Poland. EFSA Journal, 15 (4732), 1-73.
EFSA, Boklund, A., Cay, B., Depner, K., Földi, Z., Guberti, V., … Gortázar, C. (2018). Scientific report on the epidemiological analyses of African swine fever in the European Union, (2017 until November 2018). EFSA Journal, 16(5494), 1-106.
EFSA Panel on Animal Health and Welfare (2010). Scientific Opinion on the role of tick vectors in the epidemiology of Crimean Congo hemorrhagic fever and African swine fever in Eurasia. EFSA Journal, 8(1703), 1-156.
EFSA Panel on Animal Health and Welfare (2014). Scientific Opinion on African swine fever. EFSA Journal, 12(3628), 1-77.
EFSA Panel on Animal Health and Welfare (2015). Scientific Opinion on African swine fever. EFSA Journal, 13(4163), 1-92.
Estrada-Peña, A., Mihalca, A. D., & Petney, T. (Eds.), (2017). Ticks of Europe and North Africa - A guide to species identification, 1st. ed. Springer.
FAO (2019). Agriculture and Consumer Protection Department, Animal Production and Health. ASF Situation in Asia Update. http://www.fao.org/ag/againfo/programmes/en/empres/ASF/situation_update.html Accessed January 3, 2020.
Forth, J. H., Amendt, J., Blome, S., Depner, K., & Kampen, H. (2018). Evaluation of blowfly larvae (Diptera: Calliphoridae) as possible reservoirs and mechanical vectors of African swine fever virus. Transboundary and Emerging Diseases, 65, 210-213. https://doi.org/10.1111/tbed.12688
Gallardo, C., Soler, A., Nieto, R., Cano, C., Pelayo, V., Sanchez, M. A., … Arias, M. (2017). Experimental infection of domestic pigs with African swine fever virus Lithuania 2014 genotype II field isolate. Transboundary and Emerging Diseases, 64(1), 300-304. https://doi.org/10.1111/tbed.12346
Gogin, A., Gerasimov, V., Malogolovkin, A., & Kolbasov, D. (2013). African swine fever in the North Caucasus region and the Russian Federation in years 2007-2012. Virus Research, 173, 198-203. https://doi.org/10.1016/j.virusres.2012.12.007
Greig, A., & Plowright, W. (1970). The excretion of two virulent strains of African swine fever virus by domestic pigs. Journal of Hygiene, 68, 673-682. https://doi.org/10.1017/S0022172400042613
Guinat, C., Reis, A. L., Netherton, C. L., Goatley, L., Pfeiffer, D. U., & Dixon, L. (2014). Dynamics of African swine fever virus shedding and excretion in domestic pigs infected by intramuscular inoculation and contact transmission. Veterinary Research, 45, 93-101. https://doi.org/10.1186/s13567-014-0093-8
Haas, B., Ahl, R., Böhm, R., & Strauch, D. (1995). Inactivation of viruses in liquid manure. Revue Scientifique Et Technique-Office International Des Epizooties, 14, 435-445. https://doi.org/10.20506/rst.14.2.844
Herm, R., Tummeleht, L., Jürison, M., Vilem, A., & Viltrop, A. (2019). Trace amounts of African swine fever virus DNA detected in insects collected from an infected pig farm in Estonia. Veterinary Medicine and Science, 6, 100-104. https://doi:10.1002/vms3.200
Jelsma, T., Wijnker, J. J., Smid, B., Verheij, E., van der Poel, W. H. M., & Wisselink, H. J. (2019). Salt inactivation of classical swine fever virus and African swine fever virus in porcine intestines confirms the existing in vitro casings model. Veterinary Microbiology, 238, 1-9. https://doi.org/10.1016/j.vetmic.2019.108424
Karalyan, Z., Avetisyan, A., Avagyan, H., Ghazaryan, H., Vardanyan, T., Manukyan, A., … Voskanyan, H. (2019). Presence and survival of African swine fever virus in leeches. Veterinary Microbiology, 237, 1-8. https://doi.org/10.1016/j.vetmic.2019.108421
Kim, H.-J., Lee, M.-J., Lee, S.-K., Kim, D.-Y., Seo, S.-J., Kang, H.-E., & Nam, H.-M. (2019). African swine fever virus in pork brought into South Korea by travelers from China, August 2018. Emerging Infectious Diseases, 25, 1231-1233. https://doi.org/10.3201/eid2506.181684
Krug, P. W., Davis, T., O’Brien, C., LaRocco, M., & Rodriguez, L. L. (2018). Disinfection of transboundary animal disease viruses on surfaces used in pork packing plants. Veterinary Microbiology, 219, 219-225. https://doi.org/10.1016/j.vetmic.2018.04.029
Linden, A., Licoppe, A., Volpe, R., Paternostre, J., Lesenfants, C., Cassart, D., … Cay, A. B. (2019). Summer 2018: African swine fever virus hits north-western Europe. Transboundary and Emerging Diseases, 66, 54-55. https://doi.org/10.1111/tbed.13047
Mazur-Panasiuk, N., Bruczyńska, M., Walczak, M., Juszkiewicz, M., & Woźniakowski, G. (2019). African swine fever and hard ticks - the potential mechanical vector in virus transmission between wild boars? 13th EPIZONE Annual Meeting, 26-28st of August 2019, Berlin. EPIZONE abstract book, Poster 26. Retrieved from: https://www.epizone-eu.net/upload_mm/8/0/7/1231c415-35fd-4f91-9298-5916d96ce5a4_Abstractband_EPIZONE_final_2.pdf Accessed October 22 2019.
McKercher, P. D., Hess, W. R., & Hamdy, F. (1978). Residual viruses in pork products. Applied and Environmental Microbiology, 35, 142-145.
McKercher, P. D., Yedloutschnig, R. J., Callis, J. J., Murphy, R., Panina, G. F., Civardi, A., … Scatozza, F. (1987). Survival of viruses in "Prosciutto di Parma" (Parma ham). Canadian Institute of Food Science and Technology Journal, 20, 267-272. https://doi.org/10.1016/S0315-5463(87)71198-5
Mebus, C., Arias, M., Pineda, J. M., Tapiador, J., House, C., & Sánchez-Vizcaíno, J. M. (1997). Survival of several swine viruses in different Spanish dry cured meat products. Food Chemistry, 59, 555-559. https://doi.org/10.1016/S0308-8146(97)00006-X
Mebus, C. A., House, C., Gonzalvo, F. R., Pineda, J. M., Tapiador, J., Pire, J. J., … Sanchez-Vizcaino, J. M. (1993). Survival of foot-and mouth disease, African swine fever, and hog cholera viruses in Spanish serrano cured hams and Iberian cured hams, shoulders and loins. Food Microbiology, 10, 133-143. https://doi.org/10.1006/fmic.1993.1014
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, 109-112.
Montgomery, E. (1921). On a form of swine fever occurring in British East Africa (Kenya colony). Journal of Comparative Pathology and Therapeutics, 34, 159-191. https://doi.org/10.1016/S0368-1742(21)80031-4
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, 891-897. https://doi.org/10.3201/eid2505.181495
Nurmoja, I., Mõtus, K., Kristian, M., Niine, T., Schulz, K., Depner, K., & Viltrop, A. (2018). Epidemiological analysis of the 2015-2017 African swine fever outbreaks in Estonia. Preventive Veterinary Medicine [published online ahead of print], S0167-5877(18)30361-1. https://doi.org/10.1016/j.prevetmed.2018.10.001
OIE WAHIS Interface (2020). http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/Immsummary. Accessed January 3 2020.
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., Boklund, A., Halasa, T., Belsham, G. J., Rasmussen, T. B., & Bøtner, A. (2018). Short time window for transmissibility of African swine fever virus from a contaminated environment. Transboundary and Emerging Diseases, 65, 1024-1032. https://doi.org/10.1111/tbed.12837
Olesen, A. S., Lohse, L., Boklund, A., Halasa, T., Gallardo, C., Pejsak, Z., … Bøtner, A. (2017). Transmission of African swine fever virus from infected pigs by direct contact and aerosol routes. Veterinary Microbiology, 211, 92-102. https://doi.org/10.1016/j.vetmic.2017.10.004
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, 1152-1157. https://doi.org/10.1111/tbed.12918
Oļševskis, E., Guberti, V., Seržants, M., Westergaard, J., Gallardo, C., Rodze, I., & Depner, K. (2016). African swine fever virus introduction into the EU in 2014: Experience of Latvia. Research in Veterinary Science, 105, 28-30. https://doi.org/10.1016/j.rvsc.2016.01.006
Penrith, M.-L., & Vosloo, W. (2009). Review of African swine fever: Transmission, spread and control. Journal of the South African Veterinary Association, 80, 58-62.
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, e0225657. https://doi.org/10.1371/journal.pone.0225657
Petrini, S., Feliziani, F., Casciari, C., Giammarioli, M., Torresi, C., & Mario De Mia, G. (2019). Survival of African swine fever virus (ASFV) in various traditional Italian dry-cured meat products. Preventive Veterinary Medicine, 162, 126-130. https://doi.org/10.1016/j.prevetmed.2018.11.013
Plowright, W., & Parker, J. (1967). The stability of African swine fever virus with particular reference to heat and pH inactivation. Archiv Für Die Gesamte Virusforschung, 21, 383-402. https://doi.org/10.1007/bf01241738
Sindryakova, I. P., Morgunov, Y. P., Chichikin, A. Y., Gazaev, I. K., Kudryashov, D. A., & Tsybanov, S. Z. (2016). The influence of temperature on the Russian isolate of African swine fever virus in pork products and feed with extrapolation to natural conditions. Agricultural Biology, 51, 467-474. https://doi.org/10.15389/agrobiology.2016.4.467eng
Stoian, A. M. M., Zimmerman, J., Ji, J., Hefley, T. J., Dee, S., Diel, D. G., … Niederwerder, M. C. (2019). Half-Life of African swine fever virus in shipped feed. Emerging Infectious Diseases, 25, 2261-2263. https://doi.org/10.3201/eid2512.191002
Turner, C., & Williams, S. M. (1999). Laboratory-scale inactivation of African swine fever virus and swine vesicular disease virus in pig slurry. Journal of Applied Microbiology, 87, 148-157. https://doi.org/10.1046/j.1365-2672.1999.00802.x
Turner, C., Williams, S. M., Burton, C. H., Cumby, T. R., Wilkinson, P. J., & Farrent, J. W. (1999). Pilot scale thermal treatment of pig slurry for the inactivation of animal virus pathogens. Journal of Environmental Science and Health Part B, 34, 989-1007. https://doi.org/10.1080/03601239909373241
Turner, C., Williams, S. M., Burton, C. H., Farrent, J. W., & Wilkinson, P. J. (1998). Laboratory scale inactivation of pig viruses in pig slurry and design of a pilot plant for thermal inactivation. Water Science and Technology, 38, 79-86. https://doi.org/10.1016/S0273-1223(98)00500-9
Wang, T., Sun, Y., & Qiu, H.-J. (2018). African swine fever: An unprecedented disaster and challenge to China. Infectious Diseases of Poverty, 7, 1-5. https://doi.org/10.1186/s40249-018-0495-3
Wang, W.-H., Lin, C.-Y., Ishcol, M. R. C., Urbina, A. N., Assavalapsakul, W., Thitithanyanont, A., … Wang, S.-F. (2019). Detection of African swine fever virus in pork products brought to Taiwan by travellers. Emerging Microbes & Infections, 8, 1000-1002. https://doi.org/10.1080/22221751.2019.1636615
Wilkinson, P. J., & Donaldson, A. I. (1977). Transmission studies with African swine fever virus. The early distribution of virus in pigs infected by airborne virus. Journal of Comparative Pathology, 87, 497-501. https://doi.org/10.1016/0021-9975(77)90038-x
Zani, L., Dietze, K., Dimova, Z., Forth, J. H., Denev, D., Depner, K., & Alexandrov, T. (2019). African swine fever in a Bulgarian backyard farm- a case report. Veterinary Sciences, 6, 1-9. https://doi.org/10.3390/vetsci6040094