Welfare biology research: vaccination of animals in the wild

19 Dec 2018

Vaccination as a potential large-scale strategy to improve the welfare state of wild animals is one of the many topics that could be researched in welfare biology.

Below is a project draft to illustrate the kind of research that scientists could develop in relation to vaccination, regarded as a potential method to improve the quality of life of wild animals. This research project idea is designed with a broad scope and may be divided into many specific research projects. Thus, it includes a series of research questions which can become separate projects, as well as a list of possible species worth considering, and a compilation of relevant publications.

We hope to inspire researchers interested in wild animal vaccination to design their own research projects adapted to their particular circumstances. The results could be relevant to improve our understanding of wild animal suffering and the ways to reduce it.

Project idea: effects of oral rabies vaccination programs on the welfare of animals in the wild

With the goal of eliminating rabies, a lethal zoonotic viral disease, many countries have developed public health campaigns to prevent rabies in humans, domesticated animals (including cows, cats, and dogs) and wild animals (bats and terrestrial carnivores). The control of wildlife rabies had focused traditionally on reducing host populations, through hunting or poisoning animals belonging to target species, such as bats, foxes, coyotes, and raccoons. (Lethal methods have also been used to control rabies in stray dog and cat populations.) This strategy can be challenged for being morally objectionable and has been proven to be ineffective in controlling the disease,[1] whereas mass vaccination is often promoted as an effective strategy.[2]

Oral rabies vaccination programs targeting wild terrestrial animals have been carried out since the 1980s in Europe and North America and have shown a high degree of success in eliminating the disease on wildlife reserves. During the last three decades, large-scale oral vaccination programs have freed large portions of Europe and North America from terrestrial wildlife rabies,[3] and become known as the most effective method to control the disease.

Rabies is a recognized zoonotic disease that has threatened human and animal lives since ancient times and has become an important public health issue for many countries and international organizations such as World Health Organization (WHO)[4] and World Organization for Animal Health (OIE).[5] Rabies control programs through oral vaccination are often implemented for protecting human health, preventing economic losses,[6] and in some cases for conservation purposes (e.g. African wild dog,[7]Ethiopian wolf[8]). Since national and international policies for rabies control require precise evaluation of their programs, a large amount of papers have been published assessing the efficacy of oral vaccination campaigns in controlling the disease[9] as well as their economic viability.[10] A few studies have evaluated the impacts of such programs on the ecology of animal populations.[11] Yet, assessments of the effects of oral rabies vaccination on the well-being of animals seem to be lacking, despite its being regarded as an animal-welfare friendly method itself. The great amount of data already published may give us some insights into how vaccinations impact the welfare of wild animals if they are analyzed from an approach that focuses on the welfare of animals.

Purpose

Assess the effects of oral rabies vaccination programs on the welfare of wild animal populations.

Key questions

  • How much suffering is caused by rabies in the targeted area before and after vaccinations?
  • How many animal lives are saved by oral rabies vaccination campaigns?
  • What are the side-effects of vaccines on the health state of targeted animals?
  • What are the effects of oral rabies vaccinations on the health state of non-targeted wild animals?
  • What are the long-term welfare effects of eliminating rabies from an ecosystem?

Species worth considering

Red fox (Vulpes vulpes)

Gray fox (Urocyon cineroargenteus)

Coyote (Canis latrans)

Raccoon (Procyon lotor)

Striped skunk (Mephitis mephitis)

Raccoon dog (Nyctereutes procyonoides)

African wild dog (Lycaon pictus)

Expected impacts

  • This project would be an attempt to approach interventions on wild animals from a perspective focused on the welfare of the animals.
  • The results of this project would give us insights into the benefits and harms of oral vaccination campaigns for wild animals.
  • It would promote further research on the welfare effects of vaccination campaigns against other diseases endured by wild animals.

Further readings

Brochier, B.; Deschamps, P.; Costy, F.; Hallet, L.; Leuris, J.; Villers, M.; Péharpré, D.; Mosselmans, F.; Beier, R.; Lecomte, L.; Mullier, P.; Roland, H.; Bauduin, B.; Kervyn, T.; Renders, C.; Escutenaire, S. & Pastoret, P.P. (2001) “Elimination de la rage en Belgique par la vaccination du renard roux (Vulpes vulpes )“, Annales de Médecine vétérinaire, 145, pp. 293-305.

Carey, A. B. (1982) “The ecology of red foxes, gray foxes, and rabies in the eastern United States”, Wildlife Society Bulletin, 20, pp. 18-26.

EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare). (2015) “Scientific opinion – Update on oral vaccination of foxes and raccoon dogs against rabies”, EFSA Journal, 13 (7), 70 pp.

Gremillion-Smith, C. & Woolf, A. (1988) “Epizootiology of skunk rabies in North America”, Journal of Wildlife Diseases, 24 (4), pp. 620-626.

Hadidian, J.; Jenkins, S.R.; Johnston, D. H.; Savarie, P. J.; Nettles, V. F.; Manski, D. & Baer, G. M. (1989) “Acceptance of simulated oral rabies vaccine baits by urban raccoons”, Journal of Wildlife Diseases, 25, pp. 1-9.

Jackson, H. C. & Schneider, L. G. (1984) “Rabies in the Federal Republic of Germany, 1950–1981: The influence of landscape”, Bulletin of the World Health Organization, 62, pp. 99-106.

Johnston, D. H. & Beauregard, M. (1969) “Rabies epidemiology in Ontario”, Bulletin of the Wildlife Disease Association5, pp. 357–370.

Randall, D. A.; Marino, J.; Haydon, D. T.; Sillero-Zubiri, C.; Knobel, D. L.; Tallents, L. A.; Macdonald, D. W. & Laurenson, M. K. (2006) “An integrated disease management strategy for the control of rabies in Ethiopian wolves”, Biological Conservation, 131 (2), pp. 151-162.

Real, L. A.; Russel, C.; Waller, L.; Smith, D. & Childs, J. (2005) “Spatial Dynamics and Molecular Ecology of North American Rabies”, Journal of Heredity, 96 (3), pp. 253-260.

Root, J. J.; Puskas, R. B.; Fischer, J. W.; Swope, C. B.; Neubaum, M. A.; Reeder, S. A. & Piaggio, A. J. (2009) “Landscape genetics of raccoons (Procyon lotor) associated with ridges and valleys of Pennsylvania: implications for oral rabies vaccination programs”, Vector Borne Zoonotic Dis. 9 (6), pp. 583-588.

Rosatte, R.C. (1988) “Rabies in Canada: History, Epidemiology and Control”, Can Vet J, 29, pp. 362-365.

Steck, F. & Wandeler, A. I. (1980) “The epidemiology of fox rabies in Europe”, Epidemiologic Reviews, 2, pp. 71–96.

Sterner, R. T. & Smith, G. C. (2006) “Modelling wildlife rabies: Transmission, economics, and conservation”, Biological Conservation, 131 (2), pp. 163-179

Tabel, H.; Corner, A. H.; Webster, W. A. & Casey, C. A. (1974) “History and epizootiology of rabies in Canada”, The Canadian Veterinary Journal, 15, pp. 217–281.

Torrence, M. E.; Jenkins, S. R. & Glickman, T. (1992) “Epidemiology of racoon rabies in Virginia, 1984 to 1989”, Journal of Wildlife Diseases, 28 (3), pp. 369-376.

Wandeler, A. I.; Capt, S.; Kappeler, A. & Hauser, R. (1988). “Oral immunization of wildlife against rabies: concept and first field experiments”, Reviews of Infectious Diseases, 10 (4), pp. S649-53.

Wasniewski, M.; Almeida, I.; Baur, A.; Bedekovic, T.; Boncea, D.; Chaves, L. B.; David, D.; De Benedictis, P.; Dobrostana, M.; Giraud, P.; Hostnik, P.; Jaceviciene, I.; Kenklies, S.; König, M.; Mähar, K.; Mojzis, M.; Moore, S.; Mrenoski, S.; Müller, T.; Ngoepe, E.; Nishimura, M.; Nokireki, T.; Pejovic, N.; Smreczak, M.; Strandbygaard, B.; Wodak, E. & Cliquet, F. (2016) “First international collaborative study to evaluate rabies antibody detection method for use in monitoring the effectiveness of oral vaccination programmes in fox and raccoon dog in Europe”, Journal of Virological Methods, 238, pp. 77-85.

Wilhelm, U. & Schneider, L. G. (1990) “Oral immunization of foxes against rabies: practical experiences of a field trial in the Federal Republic of Germany”, Bulletin of the World Health Organization, 68, pp. 87-92.

Yakobson, B.; Goga, I.; Freuling, C. M.; Fooks, A. R.; Gjinovci, V.; Hulaj, B.; Horton, D.; Johnson, N.; Muhaxhiri, J.; Recica, I.; David, D.; O’Flaherty, R.; Taylor, N.; Wilsmore, T. & Müller, T. (2014) “Implementation and monitoring of oral rabies vaccination of foxes in Kosovo between 2010 and 2013—An international and intersectoral effort”, International Journal of Medical Microbiology, 304 (7), pp. 902-910.

Zienius, D.; Sereika, V. & Lelešius, R. (2007) “Rabies occurrence in red fox and raccoon dog population in Lithuania”, Etologija, 53, pp. 59-64.

Notes

[1] Curk, A. & Carpenter, T. E. (1994) “Efficacy of the first oral vaccination against fox rabies in Slovenia”, Rev. sci. tech. Off. int. Epiz.; 13 (3), pp. 763-775.

Müller, W. W. (1997) “Where do we stand with oral vaccination of foxes against rabies in Europe?” Archives of Virology Supplementum, 13, pp. 83–94.

[2] Mass vaccination has also been proven to be less expensive than lethal methods: Aubert, M. F. A. (1999) “Costs and benefits of rabies control in wildlife in France”, Rev. Sci. Tech. Off. Int. Epiz., 18, pp. 533-543.

[3] Freuling, C. M.; Hampson, K.; Selhorst, T.; Schröder, R.; Meslin, F. X.; Mettenleiter, T. C. & Müller, T. (2013) “The elimination of fox rabies from Europe: determinants of success and lessons for the future”, Philosophical Transactions of the Royal Society B: Biological Sciences, 368.

Have, P.; Aubert, M.; Breitenmoser, U.; Brochier, B.; Cliquet, F. & Müller, T. (2002) The oral vaccination of foxes against rabies. Report of the Scientific Committee on Animal Health and Animal Welfare. European Commission. Health & Consumer Protection Directorate-General.

MacInnes, C. D.; Smith, S. M.; Tinline, R. R.; Ayers, N. R.; Bachmann, P.; Ball, D. G. A.; Calder, L. A.; Crosgrey, S. J.; Fielding, C.; Hauschildt, P.; Honig, J. M.; Johnston, D. H.; Lawson, K. F.; Nunan, C. P.; Pedde, M. A.; Pond, B.; Stewart, R. B. & Voigt, D. R. (2001) “Elimination of rabies from red foxes in eastern Ontario”, Journal of Wildlife Diseases, 37, pp. 119–132.

Müller, T.; Freuling, C. M.; Wysocki, P.; Roumiantzeff, M.; Freney, J.; Mettenleiter, T. C. & Vose, A. (2015a) “Terrestrial rabies control in the European Union: Historical achievements and challenges ahead”, The Veterinary Journal, 203, pp. 10-17.

Müller, T. F.; Schröder, R.; Wysocki, P.; Mettenleiter, T. C. & Freuling, C. M. (2015b). “Spatio-temporal Use of Oral Rabies Vaccines in Fox Rabies Elimination Programmes in Europe”, PLoS Negl Trop Dis.; 9 (8), e0003953.

Slate, D.; Algeo, T. P.; Nelson, K. M.; Chipman, R. B.; Donovan, D.; Blanton, J. D.; Niezgoda, M.; Rupprecht, C. E. (2009) “Oral Rabies Vaccination in North America: Opportunities, Complexities, and Challenges”, PLOS Neglected Tropical Diseases, 3(12), e549.

Vitasek, J. (2004) “A review of rabies elimination in Europe”, Vet. Med. -Czech, 49(5), pp. 171-185.

[4] World Health Organization (WHO) webpage on rabies: http://www.who.int/rabies/en/

[5] World Health Organization for Animal Health (OIE) webpage on rabies: http://www.oie.int/en/animal-health-in-the-world/rabies-portal/what-is-rabies/

[6] Wandeler, A. I. (2000) “Oral immunization against rabies: afterthoughts and foresight”, Schweiz. Arch. Tierheilkd, 142, pp. 455–462.

[7] Knobel, D. L.; Du Toit, J. T. & Bingham, J. (2002) “Development of a bait and baiting system for delivery of oral rabies vaccine to free-ranging African wild dogs (Lycaon pictus)”, Journal of Wildlife Diseases, 38, pp. 352–362.

Vial, F.; Haydon, D. T.; Cleaveland, S. & Rasmussen, G. (2006). “Development of vaccination strategies for the management of rabies in African wild dogs”, Biological Conservation, 131 (2), pp. 180-192.

[8] Randall, D.A.; Marino, J.; Haydon, D.T.; Sillero-Zubiri, C.; Knobel, D.L.; Tallents, L.A.; Macdonald, D.W. & Laurenson, M.K. (2006) “An integrated disease management strategy for the control of rabies in Ethiopian wolves”, Biological Conservation, 131 (2), pp. 151-162.

[9] For example:

Boulanger, J. R.; Bigler, L. L.; Curtis, P. D. & Lein, D. H. (2008) “Evaluation of an oral vaccination program to control raccoon rabies in a suburbanized landscape” Human-Wildlife Conflicts, 2 (2), 212-224.

Brochier, B.; Thomas, I.; Iokem, A.; Ginter, A.; Kalpers, J.; Paquot, A.; Costy, F. & Pastoret, P. P. (1988) “A field trial in Belgium to control fox rabies by oral immunisation”, The Veterinary Record, 123 (24), pp. 618-621.

Curk, A. & Carpenter, T.E. (1994) “Efficacy of the first oral vaccination against fox rabies in Slovenia”, Rev. sci. tech. Off. int. Epiz. 13 (3), pp. 763-775.

Fearneyhough, M. G.; Wilson, P. J.; Clark, K. A.; Smith, D. R.; Johnston, D. H.; Hicks, B. N. & Moore, G. M. (1998) “Results of an oral rabies vaccination program for coyotes”, J. Am. Vet. Med. Assoc., 212, pp. 498–502.

Freuling, C. M.; Hampson, K.; Selhorst, T.; Schröder, R.; Meslin, F. X.; Mettenleiter, T. C.; & Müller, T. (2013) “The elimination of fox rabies from Europe: determinants of success and lessons for the future”, Philosophical Transactions of the Royal Society B: Biological Sciences, 368.

Hostnik, P.; Toplak. I.; Barlič-Maganja, D.; Grom, J. & Bidovec, A. (2006). “Control of Rabies in Slovenia”, Journal of Wildlife Diseases, 42 (2), pp. 459-465.

Müller, T.; Bätza, H. J.; Freuling, C.; Kliemt, A.; Kliemt, J.; Heuser, R.; Schlüter, H.; Selhorst, T.; Vos, A. & Mettenleiter, T.C. (2012) “Elimination of terrestrial rabies in Germany using oral vaccination of foxes”, Berl Münch Tierärztl Wochenschr, 125, pp. 117–190.

Müller, T.; Freuling, C. M.; Wysocki, P.; Roumiantzeff, M.; Freney, J.; Mettenleiter, T. C. & Vose, A. (2015a) “Terrestrial rabies control in the European Union: Historical achievements and challenges ahead”, The Veterinary Journal, 203, pp. 10-17.

Müller, T. F.; Schröder, R.; Wysocki, P.; Mettenleiter, T. C. & Freuling, C. M. (2015b). “Spatio-temporal Use of Oral Rabies Vaccines in Fox Rabies Elimination Programmes in Europe”, PLoS Negl Trop Dis.; 9 (8), e0003953.

Nelson, K. (ed). (2006). Cooperative rabies management program: National Report 2006, United States Department of Agriculture, Animal and Plant Health Inspection Service.

Niin, E.; Laine, M.; Guiot, A. L.; Demerson, J. M. & Cliquet, F. (2008) “Rabies in Estonia: Situation before and after the first campaigns of oral vaccination of wildlife with SAG2 vaccine bait”, Vaccine, 26, pp. 29-30.

Nyberg, M.; Kulonen, K.; Neuvonen, E.; Ek-Kommonen, C.; Nuorgam, M. & Westerling, B. (1992) “An Epidemic of sylvatic rabies in Finland – descriptive epidemiology and results of oral vaccination”, Acta Vet Scand, 33, pp. 43-57.

Olson, C. A.; Mitchell, K. D. & Werner, P. A. (2000) “Bait ingestion by free-ranging raccoons and non-target species in an oral rabies vaccine field trial in Florida”, Journal of Wildlife Diseases, 36, pp. 734-743.

Papatheodorou, D. P.; Tasioudi, K. E.; Korou, L. M.; Georgiou, V.; Iliadou, P.; Markantonatos, G.; Kirtzalidou, A.; Tzani, M.; Chondrokouki, E. & Mangana-Vougiouka, O. (2018) “First four Oral Rabies Vaccination campaigns of the red foxes in Greece: Evaluating factors and assessment”, Veterinary Microbiology, 216, pp. 107-118.

Robbins, A. H.; Borden, M. D.; Windmiller, B. S.; Niezgoda, M.; Marcus, L. C.; O’Brien, S. M.; Kreindel, S. M.; Mcguill, M. W.; Demaria, J. A.; Rupprecht, C. E. & Rowell, S. (1998) “Prevention of the spread of rabies to wildlife by oral vaccination of raccoons in Massachusetts”, J. Am. Vet. Med. Assoc., 213, pp. 1407–1412.

Rosatte, R. C.; Power, M. J.; MacInnes, C. D. & Campbell, J. B. (1992) “Trap-vaccinate-release and oral vaccination for rabies control in urban skunks, raccoons and foxes”, Journal of Wildlife Diseases, 28 (4), pp. 562-571.

Sidwa, T. J.; Wilson, P. J.; Moore, G. M.; Oertli, E. H.; Hicks, B. N.; Rohde, R. E. & Johnston, D. H. (2005) “Evaluation of oral rabies vaccination programs for control of rabies epizootics in coyotes and gray foxes: 1995–2003”, Journal of the American Veterinary Medical Association, 227 (5), pp. 785-792.

Slate, D.; Rupprecht, C. E.; Rooney, J. A.; Donovan, D.; Lein, D. H. & Chipman, R. B. (2005) “Status of oral rabies vaccination in wild carnivores in the United States”, Virus Research, 111, pp. 68–76.

Stohr, K. & Meslin, F. M. (1996) “Progress and setbacks in the oral immunization of foxes against rabies in Europe”, Vet Record, 139, pp. 32–35.

Suppo, C.; Naulin, J.; Langlais, M. & Artois, M. (2000) “A modelling approach to vaccination and contraception programmes for rabies control in fox populations”, Proc. R. Soc. Lond. B, 267, pp. 1575-1582.

Tischendorf, L.; Thulke, H. H.; Staubach, C.; Müller, M. S.; Jelsch, F.; Goretzki, J.; Selhorst, T.; Müller, T.; Schlüter, H. & Wissel, C. (1998) “Chance and risk of controlling rabies in large-scale and long-term immunized fox populations”, Proceedings of the Royal Society B, 265, pp. 839–846.

Vitasek, J. (2004) “A review of rabies elimination in Europe”, Vet. Med. -Czech, 49 (5), pp. 171-185.

Wasniewski, M.; Almeida, I.; Baur, A.; Bedekovic, T.; Boncea, D.; Chaves, L. B.; David, D.; De Benedictis, P.; Dobrostana, M.; Giraud, P.; Hostnik, P.; Jaceviciene, I.; Kenklies, S.; König, M.; Mähar, K.; Mojzis, M.; Moore, S.; Mrenoski, S.; Müller, T.; Ngoepe, E.; Nishimura, M.; Nokireki, T.; Pejovic, N.; Smreczak, M.; Strandbygaard, B.; Wodak, E. & Cliquet, F. (2016) “First international collaborative study to evaluate rabies antibody detection method for use in monitoring the effectiveness of oral vaccination programmes in fox and raccoon dog in Europe”, Journal of Virological Methods, 238, pp. 77-85.

Wilhelm, U. & Schneider, L.G. (1990) “Oral immunization of foxes against rabies: practical experiences of a field trial in the Federal Republic of Germany”, Bulletin of the World Health Organization, 68, pp. 87-92.

Yakobson, B.; Goga, I.; Freuling, C.M.; Fooks, A.R.; Gjinovci, V.; Hulaj, B.; Horton, D.; Johnson, N.; Muhaxhiri, J.; Recica, I.; David, D.; O’Flaherty, R.; Taylor, N.; Wilsmore, T. & Müller, T. (2014) “Implementation and monitoring of oral rabies vaccination of foxes in Kosovo between 2010 and 2013—An international and intersectoral effort”, International Journal of Medical Microbiology, 304 (7), pp. 902-910.

[10] For example: Aubert, M. F. A. (1999) “Costs and benefits of rabies control in wildlife in France”, Rev. Sci. Tech. Off. Int. Epiz., 18, pp. 533-543.

[11]  Chautan, M.; Pontier, D. & Artois, M. (2000) “Role of rabies in recent demographic changes in red fox populations in Europe”, Mammalia, 64, pp. 391-410.

Vos, A.C. (1995) “Population dynamics of the red fox (Vulpes vulpes) after the disappearance of rabies in county Garmisch-Partenkirchen, Germany, 1987-1992”, Annales Zoologici Fennici, 32, pp. 93-97.