Terrestrial rabies control in the European Union: Historical achievements and challenges ahead

Veterinary Journal

Volumn 203, Issue 1, 2015, Pages 10-17

  Müller, Thomas ^a   Freuling, Conrad Martin ^a   Wysocki, Patrick ^a   Roumiantzeff, Micha ^b   Freney, Jean ^c   Mettenleiter, Thomas Christoph ^a   Vos, Adriaan ^d  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b Fondation Mérieux Applied Research   (France)

^c HOSPICES CIVILS DE LYON   (France)

^d IDT Biologika GmbH   (Germany)

Author keywords

Europe; Oral rabies vaccination; Rabies; Red fox; Wildlife reservoirs

Indexed keywords

RABIES VACCINE;

BAT; CANIS AUREUS; DISEASE CARRIER; DOG; EPIZOOTIOLOGY; EUROPEAN UNION; FUNDING; GEOGRAPHIC DISTRIBUTION; HEALTH CARE DISPARITY; HERPESTES AUROPUNCTATUS; HISTORY OF MEDICINE; INFECTION CONTROL; MONGOOSE; NONHUMAN; PET ANIMAL; POPULATION MIGRATION; RABIES; REVIEW; SPECIES DISTRIBUTION; VACCINATION; VULPES VULPES; WILDLIFE; WOLF; ANIMAL; EUROPE; VETERINARY;

ANIMALIA; VULPES; VULPES VULPES;

ANIMALS; DISEASE RESERVOIRS; EUROPE; EUROPEAN UNION; RABIES;

EID: 84921651313     PISSN: 10900233     EISSN: 15322971     Source Type: Journal    
DOI: 10.1016/j.tvjl.2014.10.026     Document Type: Review

References (88)

1. Arechiga Ceballos N., Moron S.V., Berciano J.M., Nicolas O., Lopez C.A., Juste J., Nevado C.R., Setien A.A., Echevarria J.E. Novel lyssavirus in bat, Spain. Emerging Infectious Diseases 2013, 19:793-795.
2. Arnold J., Humer A., Heltai M., Murariu D., Spassov N., Hacklander K. Current status and distribution of golden jackals Canis aureus in Europe. Mammal Review 2012, 42:1-11.
3. Aubert M. Epidemiology of fox rabies. Wildlife Rabies Control 1992, 9-18. Wells Medical, Kent, UK. K. Bögel, F.X. Meslin, M. Kaplan (Eds.).
4. Badrane H., Bahloul C., Perrin P., Tordo N. Evidence of two lyssavirus phylogroups with distinct pathogenicity and immunogenicity. Journal of Virology 2001, 75:3268-3276.
5. Baer G.M., Abelseth M.K., Debbie J.G. Oral vaccination of foxes against rabies. American Journal of Epidemiology 1971, 93:487-490.
6. Balmori A., Carbonell R. Expansion and distribution of the Egyptian mongoose (Herpestes ichneumon) in the Iberian Peninsula. Galemys 2012, 24:83-85.
7. Banyard A.C., Hayman D., Johnson N., McElhinney L., Fooks A.R. Bats and lyssaviruses. Advances in Virus Research 2011, 79:239-289.
8. Banyard A.C., Hayman D., Freuling C.M., Müller T., Fooks A.R., Johnson N. Bat rabies. Rabies: Scientific Basis of the Disease and Its Management 2013, 215-265. Academic Press, New York, USA. A.C. Jackson (Ed.).
9. Barun A., Budinski I., Simberloff D. A ticking time-bomb? The small Indian mongoose in Europe. Aliens 2008, 26:14-16.
10. Barun A., Simberloff D., Budinski I. Impact of the small Indian mongoose on native amphibians and reptiles of the Adriatic islands, Croatia. Animal Conservation 2010, 13:549-555.
11. Beltran-Beck B., Garcia F.J., Gortazar C. Raccoons in Europe: Disease hazards due to the establishment of an invasive species. European Journal of Wildlife Research 2012, 58:5-15.
12. Blancou J. Rabies in Europe and the Mediterranean Basin: From antiquity to the 19th century. Historical Perspective of Rabies in Europe and the Mediterranean Basin 2004, 15-23. World Organization for Animal Health (Office International des Épizooties, OIE), Paris, France. A.A. King, A.R. Fooks, M. Aubert (Eds.).
13. Blanton J.D., Palmer D., Rupprecht C.E. Rabies surveillance in the United States during 2009. Journal of the American Veterinary Medical Association 2010, 237:646-657.
14. Botvinkin A.D., Selnikova O.P., Antonova L.A., Moiseeva A.B., Nesterenko E.Y. Human rabies case caused from a bat bite in Ukraine. Rabies Bulletin Europe 2005, 29:5-7.
15. Brookes S.M., Parsons G., Johnson N., McElhinney L.M., Fooks A.R. Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses. Vaccine 2005, 23:4101-4109.
16. Brookes S.M., Healy D.M., Fooks A.R. Ability of rabies vaccine strains to elicit cross-neutralising antibodies. Developments in Biologicals 2006, 125:185-193.
17. Cirovic D., Rakovic M., Milenkovic M., Paunovic M. Small Indian mongoose Herpestes auropunctatus (Herpestidae, Carnivora): An invasive species in Montenegro. Biological Invasions 2011, 13:393-399.
18. Cliquet F., Aubert M. Elimination of terrestrial rabies in Eastern European countries. Developments in Biologicals 2004, 119:185-204.
19. Cliquet F., Picard-Meyer E., Barrat J., Brookes S.M., Healy D.M., Wasniewski M., Litaize E., Biarnais M., Johnson L., Fooks A.R. Experimental infection of foxes with European bat lyssaviruses type-1 and 2. BMC Veterinary Research 2009, 5:19.
20. Cliquet F., Picard-Meyer E., Robardet E. Rabies in Europe: What are the risks?. Expert Review of Anti-infective Therapy 2014, 12:905-908.
21. Dacheux L., Larrous F., Mailles A., Boisseleau D., Delmas O., Biron C., Bourchier C., Ilari F., Lefranc T., Raffi F., et al. European bat lyssavirus transmission among cats, Europe. Emerging Infectious Diseases 2009, 15:280-284.
22. Daoust P.Y., Wandeler A.I., Casey G.A. Cluster of rabies cases of probable bat origin among red foxes in Prince Edward Island, Canada. Journal of Wildlife Diseases 1996, 32:403-406.
23. Demetriou P., Moynagh J. The European Union strategy for external cooperation with neighbouring countries on rabies control. Rabies Bulletin Europe 2011, 35:5-7.
24. Dietzgen R.G., Calisher C.H., Kurath G., Kuzmin I.V., Rodriguez L.L., Stone D.M. Family rhabdoviridae. Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses 2012, 686-714. Elsevier, San Diego, USA. A.M.Q. King, M.J. Adams, E.B. Carstens, E.J. Lefkowitz (Eds.).
25. Dunlop R.H., Williams D.J. Veterinary Medicine: An Illustrated History 1996, 1-13. Mosby, St Louis, USA.
26. European Food Safety Authority (EFSA) Assessment of the risk of rabies introduction into the UK, Ireland, Sweden, Malta, as a consequence of abandoning the serological test measuring protective antibodies to rabies. EFSA Journal 2006, 436:1-54.
27. European Union (EU) Commission implementing decision of 30 November 2012 approving annual and multiannual programmes and the financial contribution from the Union for the eradication, control and monitoring of certain animal diseases and zoonoses presented by the Member States for 2013 (notified under document C(2012) 8682) (2012/761/EU). Official Journal of the European Union 2012, 55:83-93. L336.
28. European Union (EU) Information and Notices. Official Journal of the European Union 2013, 56:1-24. C288.
29. Everard C.O., Everard J.D. Mongoose rabies in the Caribbean. Annals of the New York Academy of Sciences 1992, 653:356-366.
30. Fevre E.M., Bronsvoort B.M., Hamilton K.A., Cleaveland S. Animal movements and the spread of infectious diseases. Trends in Microbiology 2006, 14:125-131.
31. Fooks A.R., McElhinney L.M., Pounder D.J., Finnegan C.J., Mansfield K., Johnson N., Brookes S.M., Parsons G., White K., McIntyre P.G., et al. Isolation of a European bat lyssavirus type 2a from a fatal human case of rabies encephalitis. Journal of Medical Virology 2003, 71:281-289.
32. Fooks A.R., Roberts D.H., Lynch M., Hersteinsson P., Runolfsson H. Rabies in the United Kingdom, Ireland and Iceland. Historical Perspective of Rabies in Europe and the Mediterranean Basin 2004, 25-32. World Organization for Animal Health (Office International des Épizooties, OIE), Paris, France. A.A. King, A.R. Fooks, M. Aubert (Eds.).
33. Fooks A.R., Banyard A.C., Horton D.L., Johnson N., McElhinney L.M., Jackson A.C. Current status of rabies and prospects for elimination. Lancet 2014, 10.1016/S0140-6736(13)62707-5.
34. Freuling C., Müller T. Oral rabies vaccination (ORV) campaigns in jeopardy!?. Rabies Bulletin Europe 2009, 33:7-8.
35. Freuling C., Selhorst T., Bätza H.J., Müller T. The financial challenge of keeping a large region rabies-free - The EU example. Developments in Biologicals 2008, 131:273-282.
36. Freuling C., Hampson K., Selhorst T., Schröder R., Meslin F.X., Mettenleiter T.C., Müller T. The elimination of fox rabies from Europe: Determinants of success and lessons for the future. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2013, 368:20120142.
37. Freuling C., Vos A., Johnson N., Mühle R.U., Müller T. Rabies: Animal reservoirs of an ancient disease. The Role of Animals in Emerging Viral Diseases 2013, 63-87. Academic Press, San Diego, USA. N. Johnson (Ed.).
38. Freuling C.M., Beer M., Conraths F.J., Finke S., Hoffmann B., Keller B., Kliemt J., Mettenleiter T.C., Muhlbach E., Teifke J.P., et al. Novel lyssavirus in Natterer's Bat, Germany. Emerging Infectious Diseases 2011, 17:1519-1522.
39. Gautret P., Ribadeau-Dumas F., Parola P., Brouqui P., Bourhy H. Risk for rabies importation from North Africa. Emerging Infectious Diseases 2011, 17:2187-2193.
40. Goddard A.D., Donaldson N.M., Horton D.L., Kosmider R., Kelly L.A., Sayers A.R., Breed A.C., Freuling C.M., Muller T., Shaw S.E., et al. A quantitative release assessment for the noncommercial movement of companion animals: Risk of rabies reintroduction to the United Kingdom. Risk Analysis 2012, 32:1769-1783.
41. Johnson N., Dicker A., Mork T., Marston D.A., Fooks A.R., Tryland M., Fuglei E., Müller T. Phylogenetic comparison of rabies viruses from disease outbreaks on the Svalbard Islands. Vector Borne and Zoonotic Diseases 2007, 7:457-460.
42. Johnson N., Freuling C., Horton D., Müller T., Fooks A.R. Imported rabies, European Union and Switzerland, 2001-2010. Emerging Infectious Diseases 2011, 17:753-754.
43. Kauhala K., Kowalczyk R. Invasion of the raccoon dog Nyctereutes procyonoides in Europe: History of colonization, features behind its success, and threats to native fauna. Current Zoology 2011, 57:584-598.
44. Kirandjiski T., Mrenoski S., Celms I., Mitrov D., Dzadzovski I., Cvetkovikj I., Krstevski K., Picard-Meyer E., Viviani P., Malinovski D., et al. First reported cases of rabies in the Republic of Macedonia. Veterinary Record 2012, 170:312.
45. Kuzmin I.V., Botvinkin A.D., McElhinney L.M., Smith J.S., Orciari L.A., Hughes G.J., Fooks A.R., Rupprecht C.E. Molecular epidemiology of terrestrial rabies in the former Soviet Union. Journal of Wildlife Diseases 2004, 40:617-631.
46. Lapiz S., Miranda M., Garcia R., Daguro L., Paman M., Madrinan F., Rances P., Briggs D. Implementation of an intersectoral program to eliminate human and canine rabies: The Bohol Rabies Prevention and Elimination Project. PLoS Neglected Tropical Diseases 2012, 6:e1891.
47. Leslie M.J., Messenger S., Rohde R.E., Smith J., Cheshier R., Hanlon C., Rupprecht C.E. Bat-associated rabies virus in skunks. Emerging Infectious Diseases 2006, 12:1274-1277.
48. Linnell J.D.C., Andersen R., Andersone Z., Balciauskas L., Blanco J.C., Boitani L., Brainerd S., Breitenmoser U., Kojola I., Liberg O., et al. The fear of wolves: A review of wolf attacks on humans. Norsk Institutt for Naturforskning (NINA) Oppdragsmelding 2002, 731:1-65. accessed 9 October 2014. http://www.wwf.de/fileadmin/fm-wwf/Publikationen-PDF/2002.Review.wolf.attacks.pdf.
49. Lojkic I., Galic M., Cac Z., Jelic I., Bedekovic T., Lojkic M., Cvetnic Z. Bites of a rabid wolf in 67-old man in north-eastern part of Croatia. Rabies Bulletin Europe 2009, 33:5-7.
50. Lumio J., Hillbom M., Roine R., Ketonen L., Haltia M., Valle M., Neuvonen E., Lähdewirta J. Human rabies of bat origin in Europe. Lancet 1986, 327:378.
51. Malerczyk C., Selhorst T., Tordo N., Moore S.A., Müller T. Antibodies induced by vaccination with purified chick embryo cell culture vaccine (PCECV) cross-neutralize non-classical bat lyssavirus strains. Vaccine 2009, 27:5320-5325.
52. Michler F.-U. Der Waschbär. Neubürger auf dem Vormarsch 2007, 36-59. Deutscher Landwirtschaftsverlag (DLV), München, Germany.
53. Mishaeva N., Votyakov V., Velhin S., Nekhai M., Titov L. Complex rabies post-exposure prophylactic treatment after severe wolf bites in Belarus. Rabies Bulletin Europe 2007, 31:6-10.
54. Moriceau J.M. Histoire du Méchant Loup. 3000 Attaques sur l'Homme en France, Xe-XXe Siècle 2008, Fayardm, Paris, France, 623 pp. Second Ed.
55. Möckel R. Ein goldschakal (Canis aureus) in Südbrandenburg - Erstnachweis für Deutschland. Säugetierkundliche Informationen 2000, 4:477-481.
56. Müller T., Cox J., Peter W., Schäfer R., Johnson N., McElhinney L.M., Geue J.L., Tjornehoj K., Fooks A.R. Spill-over of European bat lyssavirus type 1 into a stone marten (Martes foina) in Germany. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 2004, 51:49-54.
57. Müller T., Selhorst T., Burow J., Schameitat A., Vos A. Cross reactive antigenicity in orally vaccinated foxes and raccoon dogs against European bat lyssavirus type 1 and 2. Developments in Biologicals 2006, 125:195-204.
58. Müller T., Demetriou P., Moynagh J., Cliquet F., Fooks A.R., Conraths F.J., Mettenleiter T.C., Freuling C.M. Rabies Elimination in Europe - A Success Story. Rabies Control - Towards Sustainable Prevention at the Source. Compendium of the OIE Global Conference on Rabies Control, Incheon-Seoul, Republic of Korea, 7-9 September 2011 2012, 31-43. OIE, Paris, France.
59. Nadin-Davis S.A., Torres G., Ribas M.L., Guzman M., De La Paz R.C., Morales M., Wandeler A.I. A molecular epidemiological study of rabies in Cuba. Epidemiology and Infection 2006, 134:1313-1324.
60. Nel L.H., Scott T.P., Wright N., Mollentze N., Markotter W., Sabeta C.T., le Roux K. Rabies and Rabies Control in African Regions. Rabies Control - Towards Sustainable Prevention at the Source, Compendium of the OIE Global Conference on Rabies Control, Incheon-Seoul, Republic of Korea, 7-9 September 2011 2012, 51-58. OIE, Paris, France.
61. Nolden T., Banyard A.C., Finke S., Fooks A.R., Hanke D., Höper D., Horton D., Mettenleiter T.C., Müller T., Teifke J.P., et al. Comparative studies on genetic, antigenic and pathogenic characteristics of Bokeloh bat lyssavirus. Journal of General Virology 2014, 95:1647-1653.
62. Nowak E. Verbreitungs-und bestandsentwicklung des marderhundes Nyctereutes procyonoides (Gray,1834) in Europa. Zeitschrift für Jagdwissenschaft 1984, 30:137-154.
63. Ramnial V., Kosmider R., Aylan O., Freuling C., Müller T., Fooks A.R. Quantitative risk assessment to compare the risk of rabies entering the UK from Turkey via quarantine, the Pet Travel Scheme and the EU Pet Movement Policy. Epidemiology and Infection 2010, 138:1114-1125.
64. Rosatte R.C., Donovan D., Allan M., Bruce L., Buchanan T., Sobey K., Stevenson B., Gibson M., MacDonald T., Whalen M., et al. The control of raccoon rabies in Ontario Canada: Proactive and reactive tactics, 1994-2007. Journal of Wildlife Diseases 2009, 45:772-784.
65. Roumiantzeff M., Freney J., Tordo N. Le Rage et le loup: Histoire et actualité Européenne. Vivre Avec le Loup? Trois Mille ans de Conflit 2014, 239-259. Tallandier, Paris, France. J.-M. Moriceau (Ed.).
66. Rupprecht C.E., Barrett J., Briggs D., Cliquet F., Fooks A.R., Lumlertdacha B., Meslin F.X., Müller T., Nel L.H., Schneider C., et al. Can rabies be eradicated?. Developments in Biologicals 2008, 131:95-121.
67. Schatz J., Fooks A.R., McElhinney L., Horton D., Echevarria J., Vazquez-Moron S., Kooi E.A., Rasmussen T.B., Müller T., Freuling C.M. Bat rabies surveillance in Europe. Zoonoses and Public Health 2013, 60:22-34.
68. Selimov M.A., Tatarov A.G., Botvinkin A.D., Klueva E.V., Kulikova L.G., Khismatullina N.A. Rabies-related Yuli virus; identification with a panel of monoclonal antibodies. Acta Virologica 1989, 33:542-546.
69. Seroka D. Rabies in Poland 1940-1977. Weekly Epidemiological Record 1979, 13:99-100.
70. Shwiff S., Hampson K., Anderson A. Potential economic benefits of eliminating canine rabies. Antiviral Research 2013, 98:352-356.
71. Sihvonen L. Documenting freedom from disease and re-establishing a free status after a breakdown. Rabies. Acta Veterinaria Scandinavica Supplement 2001, 94:89-91.
72. Steck F., Wandeler A., Bichsel P., Capt S., Hafliger U., Schneider L. Oral immunization of foxes against rabies. Laboratory and field studies. Comparative Immunology, Microbiology and Infectious Diseases 1982, 5:165-171.
73. Steck F., Wandeler A.I., Bichsel P., Capt S., Schneider L.G. Oral immunisation of foxes against rabies - A field study. Zentralblatt für Veterinärmedizin. Reihe B 1982, 29:372-396.
74. Tasioudi K.E., Iliadou P., Agianniotaki E.I., Robardet E., Liandris E., Doudounakis S., Tzani M., Tsaroucha P., Picard-Meyer E., Cliquet F., et al. Recurrence of animal rabies, Greece, 2012. Emerging Infectious Diseases 2014, 20:326-328.
75. Tietjen S., Kaufhold B., Müller T., Freuling C.M. Case report: Illegal puppy trade and transport, Germany. Rabies Bulletin Europe 2011, 35:8-10.
76. Tjornehoj K., Fooks A.R., Agerholm J.S., Ronsholt L. Natural and experimental infection of sheep with European bat lyssavirus type-1 of Danish bat origin. Journal of Comparative Pathology 2006, 134:190-201.
77. Tsiodras S., Dougas G., Baka A., Billinis C., Doudounakis S., Balaska A., Georgakopoulou T., Rigakos G., Kontos V., Tasioudi K.E., et al. Re-emergence of animal rabies in northern Greece and subsequent human exposure, October 2012-March 2013. Eurosurveillance 2013, 18:20474.
78. Tvrtkovic N., Krystufek B. Small Indian mongoose Herpestes auropunctatus (Hodgson, 1836) on the Adriatic Islands of Yugoslavia. Bonner Zoologische Beiträge 1990, 41:3-8.
79. Vigilato M.A.N., Clavijo A., Knobl T., Silva H.M.T., Cosivi O., Schneider M.C., Leanes L.F., Belotto A.J., Espinal M.A. Progress towards eliminating canine rabies: Policies and perspectives from Latin America and the Caribbean. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2013, 368:20120143.
80. Vos A., Müller T., Neubert L., Zurbriggen A., Botteron C., Pöhle D., Schoon H., Haas L., Jackson A.C. Rabies in red foxes (Vulpes vulpes) experimentally infected with European bat lyssavirus type 1. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 2004, 51:327-332.
81. Vos A., Ortmann S., Kretzschmar A.S., Köhnemann B., Michler F. The raccoon (Procyon lotor) as potential rabies reservoir species in Germany: A risk assessment. Berliner und Münchener Tierärztliche Wochenschrift 2012, 125:228-235.
82. Vos A., Kretzschmar A., Ortmann S., Lojkic I., Habla C., Müller T., Kaiser C., Hundt B., Schuster P. Oral vaccination of captive small Indian mongoose (Herpestes auropunctatus) against rabies. Journal of Wildlife Diseases 2013, 49:1033-1036.
83. Vos A., Nolden T., Habla C., Finke S., Freuling C.M., Teifke J.P., Müller T. Raccoons (Procyon lotor) in Germany as potential reservoir species for lyssaviruses. European Journal of Wildlife Research 2013, 59:637-643.
84. Wandeler A. Oral immunization of wildlife. The Natural History of Rabies 1991, 485-503. Academic Press, New York, USA. Second Ed. G.M. Baer (Ed.).
85. Wandeler A. Epidemiology and ecology of fox rabies in Europe. Historical Perspective of Rabies in Europe and the Mediterranean Basin 2004, 201-214. World Organization for Animal Health (Office International des Épizooties, OIE), Paris, France. A.A. King, A.R. Fooks, M. Aubert (Eds.).
86. World Health Organization (WHO) WHO expert consultation on rabies: Second report. WHO Technical Report Series 2013, 982:1-139.
87. Yakobson B., Goga I., Freuling C.M., Fooks A.R., Gjinovci V., Hulaj B., Horton D., Johnson N., Muhaxhirif J., Recica I., et al. Implementation and monitoring of oral rabies vaccination of foxes in Kosovo between 2010 and 2013 - An international and intersectorial effort. International Journal of Medical Microbiology 2014, 304:902-910. 10.1016/j.ijmm.2014.07.009.
88. Yakobson B.A., King R., Amir S., Devers N., Sheichat N., Rutenberg D., Mildenberg Z., David D. Rabies vaccination programme for red foxes (Vulpes vulpes) and golden jackals (Canis aureus) in Israel (1999-2004). Developments in Biologicals 2006, 125:133-140.