INTRODUCTION: African swine fever (ASF) is a notifiable disease of swine that impacts global pork trade and food security. In several countries across the globe, the disease persists in wild boar (WB) populations sympatric to domestic pig (DP) operations, with continued detections in both sectors. While there is evidence of spillover and spillback between the sectors, the frequency of occurrence and relative importance of different risk factors for transmission at the wildlife-livestock interface remain unclear. METHODS: To address this gap, we leveraged ASF surveillance data from WB and DP across Eastern Poland from 2014-2019 in an analysis that quantified the relative importance of different risk factors for explaining variation in each of the ASF surveillance data from WB and DP. RESULTS: ASF prevalence exhibited different seasonal trends across the sectors: apparent prevalence was much higher in summer (84% of detections) in DP, but more consistent throughout the year in WB (highest in winter with 45%, lowest in summer at 15%). Only 21.8% of DP-positive surveillance data included surveillance in WB nearby (within 5 km of the grid cell within the last 4 weeks), while 41.9% of WB-positive surveillance samples included any DP surveillance samples nearby. Thus, the surveillance design afforded twice as much opportunity to find DP-positive samples in the recent vicinity of WB-positive samples compared to the opposite, yet the rate of positive WB samples in the recent vicinity of a positive DP sample was 48 times as likely than the rate of positive DP samples in the recent vicinity of a positive WB sample. Our machine learning analyses found that positive samples in WB were predicted by WB-related risk factors, but not to DP-related risk factors. In contrast, WB risk factors were important for predicting detections in DP on a few spatial and temporal scales of data aggregation. DISCUSSION: Our results highlight that spillover from WB to DP might be more frequent than the reverse, but that the structure of current surveillance systems challenge quantification of spillover frequency and risk factors. Our results emphasize the importance of, and provide guidance for, improving cross-sector surveillance designs.

Department of Game Management and Wildlife Biology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czechia

Department of Swine Diseases National Veterinary Research Institute Puławy Poland

Mammal Research Institute Polish Academy of Sciences Białowieża Poland

National Wildlife Research Center USDA APHIS Wildlife Services Fort Collins CO United States

Zobrazit více v PubMed

Taylor LH, Latham SM, Woolhouse MEJ. Risk factors for human disease emergence. Philos T R Soc B. (2001) 356:983–9. 10.1098/rstb.2001.0888 PubMed DOI PMC

Mason-D'Croz D, Bogard JR, Herrero M, Robinson S, Sulser TB, Wiebe K, et al. . Modelling the global economic consequences of a major African swine fever outbreak in China. Nat Food. (2020) 1:221–8. 10.1038/s43016-020-0057-2 PubMed DOI PMC

Luskin MS, Meijaard E, Surya S, Sheherazade, Walzer C, Linkie M. African Swine Fever threatens Southeast Asia's 11 endemic wild pig species. Conserv Lett. (2021) 14:e12784. 10.1111/conl.12784 DOI

Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI, Graham AL, et al. . Pathways to zoonotic spillover. Nat Rev Microbiol. (2017) 15:502–10. 10.1038/nrmicro.2017.45 PubMed DOI PMC

Sokolow SH, Nova N, Pepin KM, Peel AJ, Pulliam JRC, Manlove K, et al. . Ecological interventions to prevent and manage zoonotic pathogen spillover. Philos Trans R Soc Lond B Biol Sci. (2019) 374:20180342. 10.1098/rstb.2018.0342 PubMed DOI PMC

Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JRC, Dobson AP, et al. . Epidemic dynamics at the human-animal interface. Science. (2009) 326:1362–7. 10.1126/science.1177345 PubMed DOI PMC

Cross PC, Prosser DJ, Ramey AM, Hanks EM, Pepin KM. Confronting models with data: the challenges of estimating disease spillover. Philos Trans R Soc Lond B Biol Sci. (2019) 374:20180435. 10.1098/rstb.2018.0435 PubMed DOI PMC

Chenais E, Stahl K, Guberti V, Depner K. Identification of wild boar-habitat epidemiologic cycle in african swine fever epizootic. Emerg Infect Dis. (2018) 24:810–2. 10.3201/eid2404.172127 PubMed DOI PMC

Pepin KM, Miller RS, Wilber MQ. A framework for surveillance of emerging pathogens at the human-animal interface: pigs and coronaviruses as a case study. Prev Vet Med. (2021) 188:105281. 10.1016/j.prevetmed.2021.105281 PubMed DOI PMC

Rhyan JC, Spraker TR. Emergence of diseases from wildlife reservoirs. Vet Pathol. (2010) 47:34–9. 10.1177/0300985809354466 PubMed DOI

Pepin KM, Golnar A, Podgorski T. Social structure defines spatial transmission of African swine fever in wild boar. J R Soc Interface. (2021) 18:20200761. 10.1098/rsif.2020.0761 PubMed DOI PMC

Guinat C, Gogin A, Blome S, Keil G, Pollin R, Pfeiffer DU, et al. . Transmission routes of African swine fever virus to domestic pigs: current knowledge and future research directions. Vet Rec. (2016) 178:262–7. 10.1136/vr.103593 PubMed DOI PMC

Bergmann H, Dups-Bergmann J, Schulz K, Probst C, Zani L, Fischer M, et al. . Identification of risk factors for african swine fever: a systematic review. Viruses-Basel. (2022) 14:2107. 10.3390/v14102107 PubMed DOI PMC

Boinas FS, Wilson AJ, Hutchings GH, Martins C, Dixon LJ. The persistence of African swine fever virus in field-infected Ornithodoros erraticus during the ASF endemic period in Portugal. PLoS ONE. (2011) 6:e20383. 10.1371/journal.pone.0020383 PubMed DOI PMC

Iglesias I, Rodriguez A, Feliziani F, Rolesu S, De la Torre A. Spatio-temporal analysis of African swine fever in sardinia (2012-2014): trends in domestic pigs and wild boar. Transbound Emerg Dis. (2017) 64:656–62. 10.1111/tbed.12408 PubMed DOI

Rolesu S, Mandas D, Loi F, Oggiano A, Dei Giudici S, Franzoni G, et al. . African swine fever in smallholder sardinian farms: last 10 years of network transmission reconstruction and analysis. Front Vet Sci. (2021) 8:692448. 10.3389/fvets.2021.692448 PubMed DOI PMC

Fasina FO, Agbaje M, Ajani FL, Talabi OA, Lazarus DD, Gallardo C, et al. . Risk factors for farm-level African swine fever infection in major pig-producing areas in Nigeria, 1997-2011. Prev Vet Med. (2012) 107:65–75. 10.1016/j.prevetmed.2012.05.011 PubMed DOI

Boklund A, Dhollander S, Chesnoiu Vasile T, Abrahantes JC, Botner A, Gogin A, et al. . Risk factors for African swine fever incursion in Romanian domestic farms during 2019. Sci Rep. (2020) 10:10215. 10.1038/s41598-020-66381-3 PubMed DOI PMC

Gulenkin VM, Korennoy FI, Karaulov AK, Dudnikov SA. Cartographical analysis of African swine fever outbreaks in the territory of the Russian Federation and computer modeling of the basic reproduction ratio. Prev Vet Med. (2011) 102:167–74. 10.1016/j.prevetmed.2011.07.004 PubMed DOI

Vergne T, Gogin A, Pfeiffer DU. Statistical exploration of local transmission routes for african swine fever in pigs in the russian federation, 2007-2014. Transbound Emerg Dis. (2017) 64:504–12. 10.1111/tbed.12391 PubMed DOI

Jiang D, Ma T, Hao MM, Ding FY, Sun K, Wang Q, et al. . Quantifying risk factors and potential geographic extent of African swine fever across the world. PLoS ONE. (2022) 17:e0267128. 10.1371/journal.pone.0267128 PubMed DOI PMC

Sánchez-Vizcaino JM, Mur L, Gomez-Villamandos JC, Carrasco L. An update on the epidemiology and pathology of African swine fever. J Comp Pathol. (2015) 152:9–21. 10.1016/j.jcpa.2014.09.003 PubMed DOI

Chenais E, Depner K, Guberti V, Dietze K, Viltrop A, Stahl K. Epidemiological considerations on African swine fever in Europe 2014-2018. Porcine Health Manag. (2019) 5:6. 10.1186/s40813-018-0109-2 PubMed DOI PMC

EFSA, Banos JV, Boklund A, Gogin A, Gortazar C, Guberti V, et al. . Epidemiological analyses of African swine fever in the European Union: (September 2020 to August 2021). EFSA J. (2022) 20:e07290. 10.2903/j.efsa.2022.7290 PubMed DOI PMC

EFSA, Boklund A, Cay B, Depner K, Foldi Z, Guberti V, et al. . Epidemiological analyses of African swine fever in the European Union (November 2017 until November 2018). EFSA J. (2018) 16:e05494. 10.2903/j.efsa.2018.5494 PubMed DOI PMC

Pepin KM, Golnar AJ, Abdo Z, Podgorski T. Ecological drivers of African swine fever virus persistence in wild boar populations: insight for control. Ecol Evol. (2020) 10:2846–59. 10.1002/ece3.6100 PubMed DOI PMC

Podgórski T, Borowik T, Lyjak M, Wozniakowski G. Spatial epidemiology of African swine fever: Host, landscape and anthropogenic drivers of disease occurrence in wild boar. Prev Vet Med. (2020) 177:104691. 10.1016/j.prevetmed.2019.104691 PubMed DOI

Bosch J, Iglesias I, Munoz MJ, de la Torre A. A cartographic tool for managing african swine fever in eurasia: mapping wild boar distribution based on the quality of available habitats. Transbound Emerg Dis. (2017) 64:1720–33. 10.1111/tbed.12559 PubMed DOI

Gervasi V, Guberti V. African swine fever endemic persistence in wild boar populations: Key mechanisms explored through modelling. Transbound Emerg Dis. (2021) 68:2812–25. 10.1111/tbed.14194 PubMed DOI PMC

Nurmoja I, Schulz K, Staubach C, Sauter-Louis C, Depner K, Conraths FJ, et al. . Development of African swine fever epidemic among wild boar in Estonia - two different areas in the epidemiological focus. Sci Rep UK. (2017) 7:12562. 10.1038/s41598-017-12952-w PubMed DOI PMC

O'Neill X, White A, Ruiz-Fons F, Gortazar C. Modelling the transmission and persistence of African swine fever in wild boar in contrasting European scenarios. Sci Rep UK. (2020) 10:5895. 10.1038/s41598-020-62736-y PubMed DOI PMC

Iglesias I, Munoz MJ, Montes F, Perez A, Gogin A, Kolbasov D, et al. . Reproductive ratio for the local spread of African swine fever in wild boars in the Russian federation. Transbound Emerg Dis. (2016) 63:e237–e45. 10.1111/tbed.12337 PubMed DOI

Loi F, Di Sabatino D, Baldi I, Rolesu S, Gervasi V, Guberti V, et al. . Estimation of R(0) for the spread of the first ASF epidemic in italy from fresh carcasses. Viruses. (2022) 14:2240. 10.3390/v14102240 PubMed DOI PMC

Marcon A, Linden A, Satran P, Gervasi V, Licoppe A, Guberti V. R(0) Estimation for the African swine fever epidemics in wild boar of Czech Republic and Belgium. Vet Sci. (2019) 7:E2. 10.3390/vetsci7010002 PubMed DOI PMC

Mazur-Panasiuk N, Wozniakowski G, Niemczuk K. The first complete genomic sequences of African swine fever virus isolated in Poland. Sci Rep. (2019) 9:4556. 10.1038/s41598-018-36823-0 PubMed DOI PMC

Denstedt E, Porco A, Hwang J, Nga NTT, Ngoc PTB, Chea S, et al. . Detection of African swine fever virus in free-ranging wild boar in Southeast Asia. Transbound Emerg Dis. (2021) 68:2669–75. 10.1111/tbed.13964 PubMed DOI PMC

Bellini S, Casadei G, De Lorenzi G, Tamba M. A review of risk factors of African swine fever incursion in pig farming within the European union scenario. Pathogens. (2021) 10:84. 10.3390/pathogens10010084 PubMed DOI PMC

Mur L, Sanchez-Vizcaino JM, Fernandez-Carrion E, Jurado C, Rolesu S, Feliziani F, et al. . Understanding African swine fever infection dynamics in sardinia using a spatially explicit transmission model in domestic pig farms. Transbound Emerg Dis. (2018) 65:123–34. 10.1111/tbed.12636 PubMed DOI

Nurmoja I, Motus K, Kristian M, Niine T, Schulz K, Depner K, et al. . Epidemiological analysis of the 2015-2017 African swine fever outbreaks in Estonia. Prev Vet Med. (2020) 181:104556. 10.1016/j.prevetmed.2018.10.001 PubMed DOI

Lange M, Siemen H, Blome S, Thulke H-H. Analysis of spatiotemporal patterns of African swine fever cases in Russian wild boar does not reveal an endemic situation. Prev Vet Med. (2014) 117:317–25. 10.1016/j.prevetmed.2014.08.012 PubMed DOI

Frant MP, Gal-Cison A, Bocian L, Zietek-Barszcz A, Niemczuk K, Wozniakowski G, et al. . African swine fever in wild boar (Poland 2020): passive and active surveillance analysis and further perspectives. Pathogens. (2021) 10:1219. 10.3390/pathogens10091219 PubMed DOI PMC

Wozniakowski G, Pejsak Z, Jablonski A. Emergence of African Swine fever in Poland (2014-2021). Successes and failures in disease eradication. Agriculture. (2021) 11:738. 10.3390/agriculture11080738 DOI

Gilbert M, Cinardi G, Da Re D, Wint WGR, Wisser D, Robinson TP. Global Pigs Distribution in 2015 (5 Minutes of Arc). Cambridge, MA: Harvard Dataverse, V1; (2022).

Gilbert M, Nicolas G, Cinardi G, Van Boeckel TP, Vanwambeke SO, Wint GRW, et al. . Global distribution data for cattle, buffaloes, horses, sheep, goats, pigs, chickens and ducks in 2010. Sci Data. (2018) 5:180227. 10.1038/sdata.2018.227 PubMed DOI PMC

Podgórski T, Apollonio M, Keuling O. Contact rates in wild boar populations: Implications for disease transmission. J Wildlife Manage. (2018) 82:1210–8. 10.1002/jwmg.21480 DOI

Podgórski T, Pepin K, Radko A, Podbielska A, Lyjak M, Wozniakowski G, et al. . How do genetic relatedness and spatial proximity shape African swine fever infections in wild boar? Transbound Emerg Dis. (2022) 69:2656–66. 10.1111/tbed.14418 PubMed DOI

Sauter-Louis C, Conraths FJ, Probst C, Blohm U, Schulz K, Sehl J, et al. . African Swine fever in wild boar in Europe-a review. Viruses. (2021) 13:1717. 10.3390/v13091717 PubMed DOI PMC

Hayes BH, Andraud M, Salazar LG, Rose N, Vergne T. Mechanistic modelling of African swine fever: a systematic review. Prev Vet Med. (2021) 191:105358. 10.1016/j.prevetmed.2021.105358 PubMed DOI

Kosowska A, Barasona JA, Barroso-Arévalo S, Leon LB, Cadenas-Fernández E, Sánchez-Vizcaíno JM. Low transmission risk of African swine fever virus between wild boar infected by an attenuated isolate and susceptible domestic pigs. Front Vet Sci. (2022) 9:844209. 10.3389/fvets.2023.1177246 PubMed DOI PMC

Sanchez-Cordon PJ, Nunez A, Neimanis A, Wikstrom-Lassa E, Montoya M, Crooke H, et al. . African swine fever: disease dynamics in wild boar experimentally infected with ASFV isolates belonging to genotype I and II. Viruses. (2019) 11:852. 10.3390/v11090852 PubMed DOI PMC

Jori F, Petit G, Civil N, Decors A, Charrier F, Casabianca F, et al. . A questionnaire survey for the assessment of wild-domestic pig interactions in a context oedema disease outbreaks among wild boars (Sus scrofa) in South-Eastern France. Transbound Emerg Dis. (2022) 69:4009–15. 10.1111/tbed.14704 PubMed DOI PMC

Clontz LM, Yang AN, Chinn SM, Pepin KM, VerCauteren KC, Wittemyer G, et al. . Role of social structure in establishment of an invasive large mammal after translocation. Pest Manag Sci. (2023) 12:3819–29. 10.1002/ps.7567 PubMed DOI

Scillitani L, Monaco A, Toso S. Do intensive drive hunts affect wild boar (Sus scrofa) spatial behaviour in Italy? Some evidences and management implications. Eur J Wildlife Res. (2010) 56:307–18. 10.1007/s10344-009-0314-z DOI

Thurfjell H, Spong G, Ericsson G. Effects of hunting on wild boar Sus scrofa behaviour. Wildlife Biol. (2013) 19:87–93. 10.2981/12-027 DOI

Cadenas-Fernandez E, Sanchez-Vizcaino JM, Pintore A, Denurra D, Cherchi M, Jurado C, et al. . Free-ranging pig and wild boar interactions in an endemic area of african swine fever. Front Vet Sci. (2019) 6:376. 10.3389/fvets.2019.00376 PubMed DOI PMC

EFSA, Stahl K, Boklund A, Podgorski T, Vergne T, Abrahantes JC, et al. . Epidemiological analysis of African swine fever in the European Union during 2022. EFSA J. (2023) 21:8016. 10.2903/j.efsa.2023.8016 PubMed DOI PMC

Morelle K, Podgorski T, Prevot C, Keuling O, Lehaire F, Lejeune P. Towards understanding wild boar Sus scrofa movement: a synthetic movement ecology approach. Mammal Rev. (2015) 45:15–29. 10.1111/mam.12028 DOI