Recommendations and Technical Specifications for Sustainable Surveillance of Zoonotic Pathogens Where Wildlife is Implicated

EFSA Supporting PublicationsVolume 20, Issue 1 7812E External scientific reportOpen Access Recommendations and technical specifications for sustainable surveillance of zoonotic pathogens where wildlife is implicated ENETWILD-consortium, Corresponding Author ENETWILD-consortium [email protected] ENETWILD Consortium www.enetwild.comCorrespondence [email protected]Search for more papers by this authorDolores Gavier-Widen, Dolores Gavier-WidenSearch for more papers by this authorEzio Ferroglio, Ezio FerroglioSearch for more papers by this authorGraham Smith, Graham SmithSearch for more papers by this authorCatarina Gonçalves, Catarina GonçalvesSearch for more papers by this authorRachele Vada, Rachele VadaSearch for more papers by this authorStefania Zanet, Stefania ZanetSearch for more papers by this authorFriederike Gethöffer, Friederike GethöfferSearch for more papers by this authorOliver Keuling, Oliver KeulingSearch for more papers by this authorChristoph Staubach, Christoph StaubachSearch for more papers by this authorCarola Sauter-Louis, Carola Sauter-LouisSearch for more papers by this authorJose Antonio Blanco, Jose Antonio BlancoSearch for more papers by this authorIsabel G Fernández de Mera, Isabel G Fernández de MeraSearch for more papers by this authorTomasz Podgorski, Tomasz PodgorskiSearch for more papers by this authorMagdalena Larska, Magdalena LarskaSearch for more papers by this authorCeline Richomme, Celine RichommeSearch for more papers by this authorSascha Knauf, Sascha KnaufSearch for more papers by this authorJolianne M. Rijks, Jolianne M. RijksSearch for more papers by this authorAzahara Gómez, Azahara GómezSearch for more papers by this authorPaulo C Alves, Paulo C AlvesSearch for more papers by this authorNuno Santos, Nuno SantosSearch for more papers by this authorJoao Queirós, Joao QueirósSearch for more papers by this authorJohanna Dups-Bergmann, Johanna Dups-BergmannSearch for more papers by this authorAleksija Neimanis, Aleksija NeimanisSearch for more papers by this authorJoaquín Vicente, Joaquín VicenteSearch for more papers by this author ENETWILD-consortium, Corresponding Author ENETWILD-consortium [email protected] ENETWILD Consortium www.enetwild.comCorrespondence [email protected]Search for more papers by this authorDolores Gavier-Widen, Dolores Gavier-WidenSearch for more papers by this authorEzio Ferroglio, Ezio FerroglioSearch for more papers by this authorGraham Smith, Graham SmithSearch for more papers by this authorCatarina Gonçalves, Catarina GonçalvesSearch for more papers by this authorRachele Vada, Rachele VadaSearch for more papers by this authorStefania Zanet, Stefania ZanetSearch for more papers by this authorFriederike Gethöffer, Friederike GethöfferSearch for more papers by this authorOliver Keuling, Oliver KeulingSearch for more papers by this authorChristoph Staubach, Christoph StaubachSearch for more papers by this authorCarola Sauter-Louis, Carola Sauter-LouisSearch for more papers by this authorJose Antonio Blanco, Jose Antonio BlancoSearch for more papers by this authorIsabel G Fernández de Mera, Isabel G Fernández de MeraSearch for more papers by this authorTomasz Podgorski, Tomasz PodgorskiSearch for more papers by this authorMagdalena Larska, Magdalena LarskaSearch for more papers by this authorCeline Richomme, Celine RichommeSearch for more papers by this authorSascha Knauf, Sascha KnaufSearch for more papers by this authorJolianne M. Rijks, Jolianne M. RijksSearch for more papers by this authorAzahara Gómez, Azahara GómezSearch for more papers by this authorPaulo C Alves, Paulo C AlvesSearch for more papers by this authorNuno Santos, Nuno SantosSearch for more papers by this authorJoao Queirós, Joao QueirósSearch for more papers by this authorJohanna Dups-Bergmann, Johanna Dups-BergmannSearch for more papers by this authorAleksija Neimanis, Aleksija NeimanisSearch for more papers by this authorJoaquín Vicente, Joaquín VicenteSearch for more papers by this author First published: 12 January 2023 https://doi.org/10.2903/sp.efsa.2023.EN-7812Citations: 1 Question number EFSA-Q-2023-00009 AboutPDF ToolsExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract A science-based participatory process guided by EFSA identified 10 priority zoonotic pathogens for future One Health surveillance in Europe: highly pathogenic avian influenza, swine influenza, West Nile disease, tick-borne-encephalitis, echinococcosis, Crimean Congo Haemorrhagic Fever, hepatitis E, Lyme disease, Q-fever, Rift Valley fever. The main aim of this report is to formulate recommendations and technical specifications for sustainable coordinated One health surveillance for early detection of these zoonotic pathogens where wildlife is implicated. For this purpose: (i) first, we reviewed the cornerstones of integrated wildlife monitoring that are applicable to zoonotic disease surveillance in wildlife under OH surveillance in the EU; (ii) we analysed the characteristics of the main wildlife groups and the selected pathogens relevant to surveillance aimed at early detection, and integrated with other health compartments; (iii) we proposed general recommendations for the first steps of sustainable wildlife zoonotic disease surveillance in the EU, and (iv) specific recommendations of surveillance aimed at risk based early detection of pathogens in the main wild species groups. We finally proposed (iv) a framework for integrating animal disease surveillance components (wildlife, domestic, environment) for early detection under OH approach. References Abeykoon Mudiyanselage HA, Clark NJ, Soares Magalhaes RJ. 2021. Coxiella burnetii in the environment: A systematic review and critical appraisal of sampling methods. Zoonoses Public Health 68: 165- 181. Artois M, Bengis R, Delahay R, Duchêne M, Duff P, Ferroglio E, Gortázar C, Hutchings M, Kock R, Leighton T, Mörner T, Smith GC. 2009. Wildlife disease surveillance and monitoring. In: R Delahay, G Smith, M Hutchings (eds) Management of disease in wild mammals. Springer, New York, p 284. Baker L, Matthiopoulos J, Müller T, Freuling C, Hampson K. 2020. Local rabies transmission and regional spatial coupling in European foxes. PLoS ONE 15(5): e0220592. Barasona JA, Vicente J, Díez-Delgado I, Aznar J, Gortázar C, Torres MJ. 2017. Environmental Presence of Mycobacterium tuberculosis Complex in Aggregation Points at the Wildlife/Livestock Interface. Transbound Emerg Dis. 64, 1148- 1158. Barroso P, Acevedo P, Vicente J. 2021. The importance of long-term studies on wildlife diseases and their interfaces with humans and domestic animals: A review. Transbound Emerg Dis. 68, 1895- 1909. Battisti E, Zanet S, Khalili S, Trisciuoglio A, Hertel B, Ferroglio E. 2020. Molecular survey on vector-borne pathogens in alpine wild carnivorans. Front Vet Sci. 2020; 7: 1. Belsare AV, Gompper ME, Keller B, Sumners J, Hansen L, Millspaugh JJ. 2020. An agent-based framework for improving wildlife disease surveillance: A case study of chronic wasting disease in Missouri white-tailed deer. Ecol Modell 417:108919. Benestad SL, Mitchell G, Simmons, 2016. First case of chronic wasting disease in Europe in a Norwegian free-ranging reindeer. Vet Res 47, 88. Bodewes R, Bestebroer TM, van der Vries E, Verhagen JH, Herfst S, Koopmans MP, Fouchier RAM, Pfankuche VM, Wohlsein P, Siebert U, Baumgärtner W, Osterhaus AD. 2015. Avian influenza A(H10N7) virus-associated mass deaths among harbor seals. Emerg Infect Dis 21, 720- 722. Bonardi S, Filipello V, Pavoni E, Carta V, Bolzoni L, Corradi M, Gilioli S, Losio MN. 2020. Geographical restriction of Hepatitis E virus circulation in wild boars (Sus scrofa) in Emilia-Romagna region, Northern Italy. Ital J Food Saf. 6, 8463. Bourgarel M, Pfukenyi DM, Boué V, Talignani L, Chiweshe N, Diop F, Caron A, Matope G, Missé D, Liégeois F. 2018. Circulation of Alphacoronavirus, Betacoronavirus and Paramyxovirus in Hipposideros bat species in Zimbabwe. Infect. Genet. Evol. 58, 253- 257. Brock M. 2015. Putting bambi in the firing line: applying moral philosophy to environmental and economic attitudes to deer culling. School of Economics, University of East Anglia, Norwich, United Kingdom. Cardoso B, García-Bocanegra I, Acevedo P, Cáceres G, Alves PC, Gortázar C. 2022. Stepping up from wildlife disease surveillance to integrated wildlife monitoring in Europe. Res Vet Sci. 144, 149- 156. Carpio AJ, Apollonio M, Acevedo P. 2021. Wild ungulate overabundance in Europe: contexts, causes, monitoring and management recommendations. Mammal Review 51, 95- 108. Chapron G, Kaczensky P, Linnell JD., Von Arx M, Huber D, André, López-Bao JV, Boitani L. 2014. Recovery of large carnivores in Europe's modern human-dominated landscapes. Science, 346 (6216), pp. 1517- 1519. Donald PF, Green RE, Heath MF. 2001. Agricultural intensification and the collapse of Europe's farmland bird populations. Proceedings of the Royal Society B: Biological Sciences 268, 25- 29. EFSA (European Food Safety Authority), Aznar I, Baldinelli F, Papanikolaou A, Stoicescu A and Van der Stede Y. 2021. Annual Report on surveillance for avian influenza in poultry and wild birds in Member States of the European Union in 2020. EFSA Journal 2022; 20(9): 7754. ENETWILD-consortium, Fernandez-Lopez J, Acevedo P, Blanco-Aguiar JA, Vicente J. 2020. Analysis of wild boar-domestic pig interface in Europe: preliminary analysis. EFSA supporting publication 2020:EN-1834. 45 pp. ENETWILD-consortium, Illanas S, Acevedo P, Apollonio M, Blanco-Aguiar JA, Brivio F, Croft S, Cretois B, Fernández-López J, Ferroglio E, Keuling O, Linnell JDC, Plis K, Podgórski T, Scandura M, Smith GC, Soriguer RC, Vada R, Zanet S and Vicente J. 2021. Analysis of wild ungulate-livestock interface in Europe: preliminary results. EFSA supporting publication 2021:EN-7038. ENETWILD-consortium, Illanas S, Croft S, Smith GC, López-Padilla S, Vicente J, Blanco-Aguiar JA, Scandura M, Apollonio M, Ferroglio E, Zanet S, Vada R, Keuling O, Plis K, Podgorski T, Brivio F, Fernández-López J, Ruiz C, Soriguer RC, Acevedo P. 2022. New models for wild ungulates occurrence and hunting yield abundance at European scale. EFSA supporting publication 2022:EN-7631. ENETWILD-consortium, Alves PC, Gavier-Widen D, Ferroglio E, Queirós J, Rafael M, Santos N, Silva T, Gonçalves C, Vada R, Zanet S, Smith G, Gethöffer F, Keuling O, Staubach C, Sauter-Louis C, Blanco JA, Podgorski T, Larska M, Richomme C, Knauf S, Rijks JM, Pasetto C, Benatti F, Poncina M, Gómez A, Dups-Bergmann J, Neimanis A, Vicente J, 2022. Literature review on the main existing structures and systematic/academic initiatives for surveillance in the EU for zoonoses in the environment and the methods for surveillance of pathogens in the environment. EFSA supporting publication 2022:EN-7792.115 pp 111. ENETWILD-consortium, Ferroglio E, Gavier-Widen D, Gonçalves C, Vada R, Zanet S, Smith G, Gethöffer F, Keuling O, Staubach C, Sauter-Louis C, Blanco JA, Podgorski T, Magdalena Larska M, Richomme C, Knauf S, Jolianne M, Rijks JM, Gómez A, Alves PC, Queirós J, Rafael M, Santos N, Silva T, Dups-Bergmann J, Neimanis A, Vicente J, 2022. Describing and mapping of the main existing structures and systematic initiatives and academic activities for surveillance in the EU for zoonoses (transboundary, emerging and re-emerging) in domestic animals and wildlife. EFSA supporting publication 2022:EN-7795. 116pp. ENETWILD-consortium, Klaas M, Sebastian M, Ferroglio E, Goncalves C, Vada R, Vicente J, Zanet S, Gavier-Widén D, Vicente J. 2022. A review of endangered wildlife hosts in Europe for selected pathogens to be targeted by One Health surveillance. EFSA Supporting publication 2022:EN-7766. 12 pp. Farrell MJ, Davies TJ. 2019. Disease mortality in domesticated animals is predicted by host evolutionary relationships. Proc. Natl. Acad. Sci. USA 116, 7911– 7915 Fernández-López J, Blanco-Aguiar JA Vicente J, Acevedo P. 2022. Can we model distribution of population abundance from wildlife–vehicles collision data? Ecography 2022: e06113. Ferroglio E, Mignone W, Saracco M. 2002. Prevalence of seroreactors to Leishmania infantum in the canine population of North-West Italy. Parassitologia 44(Suppl. 1), 68. Fuchs R, Herold M, Verburg PH, Clevers, JGPW, Eberle J. 2015. Gross changes in reconstructions of historic land cover/use for Europe between 1900 and 2010. Global Change Biology 21, 299- 313. Galan M, Pagès M, Cosson JF. 2012. Next-Generation Sequencing for Rodent Barcoding: Species Identification from Fresh, Degraded and Environmental Samples. PLoS ONE 7(11): e48374 Gortázar C, Acevedo P, Ruiz-Fons, Vicente J. 2006. Disease risks and overabundance of game species. Eur J Wildl Res 52, 81- 87. Gortázar C, Azlan Che Amat, Daniel J. O'Brien. 2015. Open questions and recent advances in the control of a multi-host infectious disease: animal tuberculosis. Mammal Review 45, 160- 175. Gortázar C, Ruiz-Fons JF, Höfle U. 2016. Infections shared with wildlife: an updated perspective. European Journal of Wildlife Research 62, 511– 525. Grilo C, Koroleva E, Andrášik R, Bíl M, González-Suárez M. 2020. Roadkill risk and population vulnerability in European birds and mammals. Frontiers in Ecology and the Environment 18, 323- 328. Guth S, Mollentze N, Renault K, Streicker DG, Visher E, Boots M, Brook CE. 2022. Bats host the most virulent-but not the most dangerous-zoonotic viruses. Proc Natl Acad Sci USA 5, 119(14): e2113628119. Guth S, Visher E, Boots M, Brook, CE. 2019. Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal-human interface. Philos. Trans. R. Soc. Lond. B Biol. Sci. 374, 20190296. Hayman DT, Bowen RA, Cryan PM, McCracken GF, O'Shea TJ, Peel AJ, Gilbert A, Webb CT, Wood JL. 2013. Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses Public Health 60, 2- 21 Herrero-Cófreces S, Mougeot F, Lambin X, Luque-Larena JJ. 2021. Linking Zoonosis Emergence to Farmland Invasion by Fluctuating Herbivores: Common Vole Populations and Tularemia Outbreaks in NW Spain. Front Vet Sci. 12, 8:698454. Hudson PJ, Dobson AP, Lafferty KD. 2006. Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 21, 381– 385. Hood G, Roche X, Brioudes A, von Dobschuetz S, Fasina FO, Kalpravidh W, Makonnen Y, Lubroth J, Sims L. 2021. A literature review of the use of environmental sampling in the surveillance of avian influenza viruses. Transbound Emerg Dis. 68, 110- 126. Jiménez M, González E, Martín-Martín I, Hernández S, Molina R. 2014. Could wild rabbits (Oryctolagus cuniculus) be reservoirs for Leishmania infantum in the focus of Madrid, Spain? Veterinary Parasitology 202, 296- 300. Johnson PTJ, Preston DL, Hoverman JT, Richgels KLD. 2013. Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230– 234. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature 451, 990- 993. Kaplan, JO, Krumhardt, KM, Zimmermann N. 2009. The prehistoric and preindustrial deforestation of Europe. Quaternary Science Reviews 28, 3016- 3034. Krog JS, Hansen MS, Holm E, Hjulsager CK, Chriél M, Pedersen K, Andresen LO, Abildstrøm M, Jensen TH, Larsen LE. 2015. Influenza A(H10N7) virus in dead harbor seals, Denmark. Emerg Infect Dis J 21, 684. Kropil R, Smolko P, Garaj P 2015. Home range and migration patterns of male red deer Cervus elaphus in Western Carpathians. Eur J Wildl Res 61, 63– 72. Kuiken T, Leighton FA, Fouchier RAM, LeDuc JW, Peiris JSM, Schudel A, Stohr K, Osterhaus ADME. 2005. Public health - Pathogen surveillance in animals. Science 309, 1680- 1681 Lipkin WI. 2013. The changing face of pathogen discovery and surveillance. Nat Rev Microbiol. 11, 133- 141. Longdon JD, Hadfield CL, Webster DJ, Obbard FM. 2011. Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathog. 7, e1002260. Martínez-Jauregui M, Delibes-Mateos M, Arroyo B, Soliño M. Addressing social attitudes toward lethal control of wildlife in national parks. Conserv Biol. 2020 34: 868- 878. Massei G, Kindberg J, Licoppe A, Gačić D, Šprem N, Kamler J, Baubet E, Hohmann U, Monaco A, Ozoliņš J, Cellina S, Podgórski T, Fonseca C, Markov N, Pokorny B, Rosell C, Náhlik A. 2015. Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Management Science 71, 492- 500. McFarlane R, Sleigh A, McMichael T. 2012. Synanthropy of wild mammals as a determinant of emerging infectious diseases in the Asian-Australasian region. Ecohealth 9, 24– 35. Meier R, Ryser-Degiorgis M. 2018. Wild boar and infectious diseases: evaluation of the current risk to human and domestic animal health in Switzerland: A review. Schweiz Arch Tierheilkd. 160, 443- 460. Mick V, Le Carrou G, Corde Y, Game Y, Jay M, Garin-Bastuji B. 2014. Brucella melitensis in France: Persistence in Wildlife and Probable Spillover from Alpine Ibex to Domestic Animals. PLoS One 9(4): e94168. Milner JM, Bonenfant C, Mysterud A, Gaillard JM, Csányi S, Stenseth N. Chr. 2006. Temporal and spatial development of red deer harvesting in Europe: Biological and cultural factors. Journal of Applied Ecology 43, 721- 734. Mörner T, Obendorf DL, Artois M, Woodford MH. 2002. Surveillance and monitoring of wildlife diseases. Rev Sci Tech. 21, 67- 76. Nichols JD, Williams BK. Monitoring for conservation. 2006. Trends Ecol Evol 21, 668- 673. Putman R, Apollonio M. 2010. Behaviour and Management of European Ungulates. Whittles Publishing Rivero-Juarez A, Frias M, Martinez-Peinado A, Risalde MA, Rodriguez-Cano D, Camacho A, García-Bocanegra I, Cuenca-Lopez F, Gomez-Villamandos JC, Rivero A. 2017. Familial Hepatitis E outbreak linked to wild boar meat consumption. Zoonoses Public Health 64, 561- 565. Ruiz-Fons F, Segalés J, Gortázar C. 2008. A review of viral diseases of the European wild boar: effects of population dynamics and reservoir role. Vet J. 176, 158- 169. Ryser-Degiorgis MP. 2013. Wildlife health investigations: needs, challenges and recommendations. BMC Vet Res 9, 223. Salkeld D, Padgett KA, Jones JH. 2013. Meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission isidiosyncratic. Ecol. Lett. 16, 679- 686. Sánchez M, Valcárcel F, González J, González MG, Martín-Hernández R, Tercero JM, González-Jara P, Olmeda AS. 2022. Seasonality of Coxiella burnetii among Wild Rabbits (Oryctolagus cuniculus) and the Hyalomma lusitanicum (Acari: Ixodidae) in a Meso-Mediterranean Ecosystem. Pathogens 11, 36. Vikøren T, Våge J, Madslien KI, Røed KH, Rolandsen CM, Tran L, Hopp P, Veiberg V, Heum M, Moldal T, Neves CGd, Handeland K, Ytrehus B, Kolbjørnsen Ø, Wisløff H, Terland R, Saure B, Dessen KM, Svendsen SG, Nordvik BS, Benestad SL 2019. First Detection of Chronic Wasting Disease in a Wild Red Deer (Cervus elaphus) in Europe. Journal of Wildlife Diseases 55, 970- 972. Walton L, Marion G, Davidson RS, White PCL, Smith LA, Gavier-Widen D, Yon L, Hannant D, Hutchings MR. 2016. The ecology of wildlife disease surveillance: demographic and prevalence fluctuations undermine surveillance. Journal of Applied Ecology 53, 1460 - 1469. Wobeser G. 1994. Investigation and management of disease in wild animals. Plenum. New York. World Organisation for Animal Health (OIE). 2014. Guidelines for Terrestrial Animal Health Surveillance (GTAHS). World Organisation for Animal Health (OIE). 2015. Training manual on surveillance and international reporting of diseases in wild animals (Focal Point Manual). 2nd OIE Training Workshop for Focal Points on Wildlife. Yoccoz NG, Nichols JD, Boulinier T. 2001. Monitoring of biological diversity in space and time. Trends in Ecology and Evolution 16, 446- 453. Zanet S, Battisti E, Pepe, Ciuca L, Colombo L, Trisciuoglio A, Ferroglio E, Cringoli G, Rinaldi L, Maurelli MP. 2020. Tick-borne pathogens in Ixodidae ticks collected from privately-owned dogs in Italy: a country-wide molecular survey. BMC Vet es 16, 46. Zohari S, Neimanis A, Härkönen T, Moraeus C, Valarcher J. 2014. Avian influenza A(H10N7) virus involvement in mass mortality of harbour seals (Phoca vitulina) in Sweden, March through October 2014. Euro Surveill 19, 20967. Citing Literature Volume20, Issue1January 20237812E ReferencesRelatedInformation