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Volume 26, Number 12—December 2020
Online Report

Role of Oral Rabies Vaccines in the Elimination of Dog-Mediated Human Rabies Deaths

Ryan M. WallaceComments to Author , Florence Cliquet, Christine Fehlner-Gardiner, Anthony R. Fooks, Claude T. Sabeta, Alvaro Aguilar Setién, Changchun Tu, Vlad Vuta, Boris Yakobson, Dong-Kun Yang, Gideon Brückner, Conrad M. Freuling, Lea Knopf, Artem Metlin, Patricia Pozzetti, Pebi Purwo Suseno, Sean V. Shadomy, Gregorio Torres, Marco Antonio Natal Vigilato, Bernadette Abela-Ridder, and Thomas Müller
Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA (R.M. Wallace, S.V. Shadomy); Agency for Food, Environmental, and Occupational Health and Safety, Malzéville, France (F. Cliquet); Canadian Food Inspection Agency, Ottawa, Ontario, Canada (C. Fehlner-Gardiner); Animal and Plant Health Agency, Weybridge, UK (A.R. Fooks); Onderstepoort Veterinary Institute, Pretoria, South Africa (C.T. Sabeta); Unidad de Investigación Médica en Inmunología, Coordinación de Investigación en Salud, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico (A.A. Setién); Academy of Agricultural Sciences, Changchun, China (C. Tu); Institute for Diagnosis and Animal Health, Faculty of Veterinary Medicine, Bucharest, Romania (V. Vuta); Kimron Veterinary Institute, Beit Dagan, Israel (B. Yakobson); Animal and Plant Quarantine Agency, Gimcheong-si, South Korea (D.-K. Yang); World Organisation for Animal Health, Paris, France (G. Brückner, P. Pozzetti, G. Torres); Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany (C.M. Freuling, T. Müller); World Health Organization, Geneva, Switzerland (L. Knopf, B. Abela-Ridder); Federal Centre for Animal Health, Vladimir, Russia (A. Metlin); Ministry of Agriculture, Jakarta, Indonesia (P. Purwo Suseno); Food and Agriculture Organization of the United Nations, Rome, Italy (S.V. Shadomy); Pan American Health Organization, Rio de Janeiro, Brazil (M.A.N. Vigilato)

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Table 1

Examples from the published literature of vaccination campaigns that have met or failed to meet vaccination targets

Successful vaccination programs
Unsuccessful vaccination programs
Country Vaccination coverage, % Reference Country Vaccination coverage, % Reference
Zambia 80 (29) Chad 19 (30)
Mexico >90 (31) Chad 24 (32)
Chad 74 (30) Kenya 29 (33)
Thailand 70 (34) Nigeria 17 (35)
Bolivia 85 (36) South Africa 56 (37)
Tanzania 68 (38) Tanzania 9 (38)

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References
  1. World Health Organization. Ten years in public health, 2007–2017. Geneva: The Organization; 2017.
  2. World Health Organization. Global programme to eliminate lymphatic filariasis: progress report, 2016. Wkly Epidemiol Rec. 2017;92:594607.PubMedGoogle Scholar
  3. Greene  SA, Ahmed  J, Datta  SD, Burns  CC, Quddus  A, Vertefeuille  JF, et al. Progress toward polio eradication—worldwide, January 2017–March 2019. MMWR Morb Mortal Wkly Rep. 2019;68:45862. DOIPubMedGoogle Scholar
  4. The Lancet. Guinea worm disease eradication: a moving target. Lancet. 2019;393:1261. DOIPubMedGoogle Scholar
  5. Njeumi  F, Taylor  W, Diallo  A, Miyagishima  K, Pastoret  PP, Vallat  B, et al. The long journey: a brief review of the eradication of rinderpest. Rev Sci Tech. 2012;31:72946. DOIPubMedGoogle Scholar
  6. Lambo  TA. Eradication of smallpox. N Engl J Med. 1981;305:224. DOIPubMedGoogle Scholar
  7. Minghui  R, Stone  M, Semedo  MH, Nel  L. New global strategic plan to eliminate dog-mediated rabies by 2030. Lancet Glob Health. 2018;6:e8289. DOIPubMedGoogle Scholar
  8. Wallace  RM, Undurraga  EA, Blanton  JD, Cleaton  J, Franka  R. Elimination of dog-mediated human rabies deaths by 2030: needs assessment and alternatives for progress based on dog vaccination. Front Vet Sci. 2017;4:9. DOIPubMedGoogle Scholar
  9. World Health Organization. Zero by 30: the global strategic plan to prevent human deaths from dog-transmitted rabies by 2030—executive summary. 2018 [cited 2018 Jun 20]. http://www.oie.int/fileadmin/Home/eng/Media_Center/docs/pdf/Rabies_portal/EN_executiveSummary.pdf
  10. World Health Organization. WHO expert consultation on rabies: third report. World Health Organ Tech Rep Ser. 2018;1012:195 [cited 2019 Dec 10]. https://apps.who.int/iris/handle/10665/272364
  11. Rupprecht  CE, Barrett  J, Briggs  D, Cliquet  F, Fooks  AR, Lumlertdacha  B, et al. Can rabies be eradicated? Dev Biol (Basel). 2008;131:95121.PubMedGoogle Scholar
  12. Fooks  AR, Banyard  AC, Horton  DL, Johnson  N, McElhinney  LM, Jackson  AC. Current status of rabies and prospects for elimination. Lancet. 2014;384:138999. DOIPubMedGoogle Scholar
  13. World Health Organization. WHO expert consultation on rabies: second report. World Health Organ Tech Rep Ser. 2013;982:1139.PubMedGoogle Scholar
  14. Hampson  K, Coudeville  L, Lembo  T, Sambo  M, Kieffer  A, Attlan  M, et al.; Global Alliance for Rabies Control Partners for Rabies Prevention. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis. 2015;9:e0003709. DOIPubMedGoogle Scholar
  15. Shwiff  SA, Elser  JL, Ernst  KH, Shwiff  SS, Anderson  AM. Cost-benefit analysis of controlling rabies: placing economics at the heart of rabies control to focus political will. Rev Sci Tech. 2018;37:6819. DOIPubMedGoogle Scholar
  16. Müller  T, Demetriou  P, Moynagh  J, Cliquet  F, Fooks  AR, Conraths  FJ, et al. Rabies elimination in Europe—a success story. In: Fooks AR, Müller T, editors. Rabies control—towards sustainable prevention at the source: compendium of the OIE Global Conference on Rabies Control, Incheon-Seoul, South Korea, 7–9 Sep 2011. Paris: World Organization for Animal Health; 2012. p. 31–44.
  17. Velasco-Villa  A, Escobar  LE, Sanchez  A, Shi  M, Streicker  DG, Gallardo-Romero  NF, et al. Successful strategies implemented towards the elimination of canine rabies in the Western Hemisphere. Antiviral Res. 2017;143:112. DOIPubMedGoogle Scholar
  18. Clavijo  A, Del Rio Vilas  VJ, Mayen  FL, Yadon  ZE, Beloto  AJ, Vigilato  MA, et al. Gains and future road map for the elimination of dog-transmitted rabies in the Americas. Am J Trop Med Hyg. 2013;89:10402. DOIPubMedGoogle Scholar
  19. Vigilato  MA, Clavijo  A, Knobl  T, Silva  HM, Cosivi  O, Schneider  MC, et al. Progress towards eliminating canine rabies: policies and perspectives from Latin America and the Caribbean. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120143. DOIPubMedGoogle Scholar
  20. Lapiz  SM, Miranda  ME, Garcia  RG, Daguro  LI, Paman  MD, Madrinan  FP, et al. Implementation of an intersectoral program to eliminate human and canine rabies: the Bohol Rabies Prevention and Elimination Project. PLoS Negl Trop Dis. 2012;6:e1891. DOIPubMedGoogle Scholar
  21. Kayali  U, Mindekem  R, Hutton  G, Ndoutamia  AG, Zinsstag  J. Cost-description of a pilot parenteral vaccination campaign against rabies in dogs in N’Djaména, Chad. Trop Med Int Health. 2006;11:105865. DOIPubMedGoogle Scholar
  22. World Health Organization. Mexico is free from human rabies transmitted by dogs. 2019 [cited 2019 Dec 28]. https://www.who.int/news/item/21-12-2019-mexico-is-free-from-human-rabies-transmitted-by-dogs
  23. Knobel  DL, Cleaveland  S, Coleman  PG, Fèvre  EM, Meltzer  MI, Miranda  ME, et al. Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ. 2005;83:3608.PubMedGoogle Scholar
  24. Freuling  CM, Hampson  K, Selhorst  T, Schröder  R, Meslin  FX, Mettenleiter  TC, et al. The elimination of fox rabies from Europe: determinants of success and lessons for the future. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120142. DOIPubMedGoogle Scholar
  25. MacInnes  CD, Smith  SM, Tinline  RR, Ayers  NR, Bachmann  P, Ball  DG, et al. Elimination of rabies from red foxes in eastern Ontario. J Wildl Dis. 2001;37:11932. DOIPubMedGoogle Scholar
  26. Slate  D, Algeo  TP, Nelson  KM, Chipman  RB, Donovan  D, Blanton  JD, et al. Oral rabies vaccination in north america: opportunities, complexities, and challenges. PLoS Negl Trop Dis. 2009;3:e549. DOIPubMedGoogle Scholar
  27. Robardet  E, Bosnjak  D, Englund  L, Demetriou  P, Martín  PR, Cliquet  F. Zero endemic cases of wildlife rabies (classical rabies virus, RABV) in the European Union by 2020: an achievable goal. Trop Med Infect Dis. 2019;4:124. DOIPubMedGoogle Scholar
  28. Cliquet  F, Guiot  AL, Aubert  M, Robardet  E, Rupprecht  CE, Meslin  FX. Oral vaccination of dogs: a well-studied and undervalued tool for achieving human and dog rabies elimination. Vet Res (Faisalabad). 2018;49:61. DOIPubMedGoogle Scholar
  29. De Balogh  KK, Wandeler  AI, Meslin  FX. A dog ecology study in an urban and a semi-rural area of Zambia. Onderstepoort J Vet Res. 1993;60:43743.PubMedGoogle Scholar
  30. Kayali  U, Mindekem  R, Yémadji  N, Vounatsou  P, Kaninga  Y, Ndoutamia  AG, et al. Coverage of pilot parenteral vaccination campaign against canine rabies in N’Djaména, Chad. Bull World Health Organ. 2003;81:73944.PubMedGoogle Scholar
  31. Vigilato  MA, Clavijo  A, Knobl  T, Silva  HM, Cosivi  O, Schneider  MC, et al. Progress towards eliminating canine rabies: policies and perspectives from Latin America and the Caribbean. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120143. DOIPubMedGoogle Scholar
  32. Durr  S, Mindekem  R, Kaninga  Y, Doumagoum Moto  D, Meltzer  MI, Vounatsou  P, et al. Effectiveness of dog rabies vaccination programmes: comparison of owner-charged and free vaccination campaigns. Epidemiol Infect. 2009;137:155867. DOIPubMedGoogle Scholar
  33. Kitala  P, McDermott  J, Kyule  M, Gathuma  J, Perry  B, Wandeler  A. Dog ecology and demography information to support the planning of rabies control in Machakos District, Kenya. Acta Trop. 2001;78:21730. DOIPubMedGoogle Scholar
  34. Kongkaew  W, Coleman  P, Pfeiffer  DU, Antarasena  C, Thiptara  A. Vaccination coverage and epidemiological parameters of the owned-dog population in Thungsong District, Thailand. Prev Vet Med. 2004;65:10515. DOIPubMedGoogle Scholar
  35. Dzikwi  AA, Ibrahim  AS, Umoh  JU. Knowledge, attitude and practice about rabies among children receiving formal and informal education in Samaru, Zaria, Nigeria. Glob J Health Sci. 2012;4:1329. DOIPubMedGoogle Scholar
  36. Suzuki  K, Pereira  JA, Frías  LA, López  R, Mutinelli  LE, Pons  ER. Rabies-vaccination coverage and profiles of the owned-dog population in Santa Cruz de la Sierra, Bolivia. Zoonoses Public Health. 2008;55:17783. DOIPubMedGoogle Scholar
  37. van Sittert  SJ, Raath  J, Akol  GW, Miyen  JM, Mlahlwa  B, Sabeta  CT. Rabies in the Eastern Cape Province of South Africa—where are we going wrong? J S Afr Vet Assoc. 2010;81:20715. DOIPubMedGoogle Scholar
  38. Cleaveland  S, Kaare  M, Tiringa  P, Mlengeya  T, Barrat  J. A dog rabies vaccination campaign in rural Africa: impact on the incidence of dog rabies and human dog-bite injuries. Vaccine. 2003;21:196573. DOIPubMedGoogle Scholar
  39. Lembo  T, Hampson  K, Kaare  MT, Ernest  E, Knobel  D, Kazwala  RR, et al. The feasibility of canine rabies elimination in Africa: dispelling doubts with data. PLoS Negl Trop Dis. 2010;4:e626. DOIPubMedGoogle Scholar
  40. Adrien  J, Georges  Y, Augustin  PD, Monroe  B, Gibson  AD, Fenelon  N, et al.; Haiti-Rabies Field Response Team. A multipartner response to prevent a binational rabies outbreak—Anse-à-Pitre, Haiti, 2019. MMWR Morb Mortal Wkly Rep. 2019;68:7079. DOIPubMedGoogle Scholar
  41. Gibson  AD, Ohal  P, Shervell  K, Handel  IG, Bronsvoort  BM, Mellanby  RJ, et al. Vaccinate-assess-move method of mass canine rabies vaccination utilising mobile technology data collection in Ranchi, India. BMC Infect Dis. 2015;15:589. DOIPubMedGoogle Scholar
  42. Gibson  AD, Yale  G, Vos  A, Corfmat  J, Airikkala-Otter  I, King  A, et al. Oral bait handout as a method to access roaming dogs for rabies vaccination in Goa, India: A proof of principle study. Vaccine X. 2019;1:100015. DOIPubMedGoogle Scholar
  43. Purwo Suseno  P, Rysava  K, Brum  E, De Balogh  K, Ketut Diarmita  I, Fakhri Husein  W, et al. Lessons for rabies control and elimination programmes: a decade of One Health experience from Bali, Indonesia. Rev Sci Tech. 2019;38:21324. DOIPubMedGoogle Scholar
  44. Gibson  AD, Wallace  RM, Rahman  A, Bharti  OK, Isloor  S, Lohr  F, et al. Reviewing solutions of scale for canine rabies elimination in India. Trop Med Infect Dis. 2020;5:47. DOIPubMedGoogle Scholar
  45. Smith  TG, Millien  M, Vos  A, Fracciterne  FA, Crowdis  K, Chirodea  C, et al. Evaluation of immune responses in dogs to oral rabies vaccine under field conditions. Vaccine. 2019;37:47439.PubMedGoogle Scholar
  46. Wallace  RM, Undurraga  EA, Gibson  A, Boone  J, Pieracci  EG, Gamble  L, et al. Estimating the effectiveness of vaccine programs in dog populations. Epidemiol Infect. 2019;147:e247.PubMedGoogle Scholar
  47. Ben Youssef  S, Matter  HC, Schumacher  CL, Kharmachi  H, Jemli  J, Mrabet  L, et al. Field evaluation of a dog owner, participation-based, bait delivery system for the oral immunization of dogs against rabies in Tunisia. Am J Trop Med Hyg. 1998;58:83545.PubMedGoogle Scholar
  48. Matter  HC, Kharmachi  H, Haddad  N, Ben Youssef  S, Sghaier  C, Ben Khelifa  R, et al. Test of three bait types for oral immunization of dogs against rabies in Tunisia. Am J Trop Med Hyg. 1995;52:48995.PubMedGoogle Scholar
  49. World Health Organization. Report of WHO consultation on oral immunization of dogs against rabies. Geneva: The Organization; 1988 [cited 2019 Dec 10]. https://apps.who.int/iris/handle/10665/58694
  50. World Health Organization. Report of WHO consultation on requirements and criteria for field trials on oral rabies vaccination of dogs and wild carnivores. Geneva: The Organization; 1989 [cited 2019 Dec 10]. https://apps.who.int/iris/handle/10665/58394
  51. World Health Organization. Oral vaccination of dogs against rabies—guidance for research on oral rabies vaccines and field application of oral vaccination of dogs against rabies. Geneva, The Organization; 2007 [cited 2019 Dec 10]. https://apps.who.int/iris/handle/10665/331036
  52. World Organization for Animal Health. Rabies (infection with rabies virus and other lyssaviruses) [chapter 3.1.17]. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Meslin F-X, editor. Paris: World Organization for Animal Health; 2018. p. 35 [cited 2019 Dec 10]. https://apps.who.int/iris/handle/10665/331036
  53. Cliquet  F, Guiot  AL, Aubert  M, Robardet  E, Rupprecht  CE, Meslin  FX. Correction to: Oral vaccination of dogs: a well-studied and undervalued tool for achieving human and dog rabies elimination. Vet Res. 2018;49:84.PubMedGoogle Scholar
  54. Fu  R, Altamirano  J, Sarnquist  CC, Maldonado  YA, Andrews  JR. Assessing the risk of vaccine-derived outbreaks after reintroduction of oral poliovirus vaccine in postcessation settings. Clin Infect Dis. 2018;67(suppl_1):S26–34.
  55. Medaglia  ML, Pessoa  LC, Sales  ER, Freitas  TR, Damaso  CR. Spread of cantagalo virus to northern Brazil. Emerg Infect Dis. 2009;15:11423.PubMedGoogle Scholar
  56. Rupprecht  CE, Blass  L, Smith  K, Orciari  LA, Niezgoda  M, Whitfield  SG, et al. Human infection due to recombinant vaccinia-rabies glycoprotein virus. N Engl J Med. 2001;345:5826. DOIPubMedGoogle Scholar
  57. Centers for Disease Control and Prevention (CDC). Human vaccinia infection after contact with a raccoon rabies vaccine bait - Pennsylvania, 2009. MMWR Morb Mortal Wkly Rep. 2009;58:12047.PubMedGoogle Scholar
  58. Müller  T, Bätza  HJ, Beckert  A, Bunzenthal  C, Cox  JH, Freuling  CM, et al. Analysis of vaccine-virus-associated rabies cases in red foxes (Vulpes vulpes) after oral rabies vaccination campaigns in Germany and Austria. Arch Virol. 2009;154:108191. DOIPubMedGoogle Scholar
  59. Hostnik  P, Picard-Meyer  E, Rihtarič  D, Toplak  I, Cliquet  F. Vaccine-induced rabies in a red fox (Vulpes vulpes): isolation of vaccine virus in brain tissue and salivary glands. J Wildl Dis. 2014;50:397401. DOIPubMedGoogle Scholar
  60. Vuta  V, Picard-Meyer  E, Robardet  E, Barboi  G, Motiu  R, Barbuceanu  F, et al. Vaccine-induced rabies case in a cow (Bos taurus): Molecular characterisation of vaccine strain in brain tissue. Vaccine. 2016;34:50215. DOIPubMedGoogle Scholar
  61. Wandeler  AI, Capt  S, Kappeler  A, Hauser  R. Oral immunization of wildlife against rabies: concept and first field experiments. Rev Infect Dis. 1988;10(Suppl 4):S64953. DOIPubMedGoogle Scholar
  62. Fehlner-Gardiner  C, Nadin-Davis  S, Armstrong  J, Muldoon  F, Bachmann  P, Wandeler  A. Era vaccine-derived cases of rabies in wildlife and domestic animals in Ontario, Canada, 1989-2004. J Wildl Dis. 2008;44:7185. DOIPubMedGoogle Scholar
  63. Pfaff  F, Müller  T, Freuling  CM, Fehlner-Gardiner  C, Nadin-Davis  S, Robardet  E, et al. In-depth genome analyses of viruses from vaccine-derived rabies cases and corresponding live-attenuated oral rabies vaccines. Vaccine. 2019;37:475865. DOIPubMedGoogle Scholar
  64. Electronic Code of Federal Regulations. Title 9, subchapter E, part 113. Standard requirements, subjgrp 74: live virus vaccines. 2007 [cited 2019 Dec 10]. https://www.ecfr.gov/cgi-bin/text-idx?tpl=/ecfrbrowse/Title09/9cfrv1_02.tpl
  65. European Directorate for the Quality of Medicines. Rabies vaccine (live, oral) for foxes and raccoon dogs. Strasbourg (France): European Council; 2014. p. 1011–2.
  66. Head  JR, Vos  A, Blanton  J, Müller  T, Chipman  R, Pieracci  EG, et al. Environmental distribution of certain modified live-virus vaccines with a high safety profile presents a low-risk, high-reward to control zoonotic diseases. Sci Rep. 2019;9:6783. DOIPubMedGoogle Scholar
  67. Dellepiane  N, Wood  D. Twenty-five years of the WHO vaccines prequalification programme (1987-2012): lessons learned and future perspectives. Vaccine. 2015;33:5261. DOIPubMedGoogle Scholar
  68. Gibson  AD, Mazeri  S, Yale  G, Desai  S, Naik  V, Corfmat  J, et al. Development of a non-meat-based, mass producible and effective bait for oral vaccination of dogs against rabies in Goa State, India. Trop Med Infect Dis. 2019;4:118. DOIPubMedGoogle Scholar
  69. World Organization for Animal Health. OIE policy paper on vaccine banks. Paris: World Organization for Animal Health; 2018. p. 16 [cited 2019 Dec 10]. https://www.oie.int/fileadmin/Home/eng/Links/docs/pdf/Policy-Paper-VB-final-EN_Oct-2018_01.pdf
  70. Mace  J, Renaudin  S, Dieuzy-Labaye  I, Dehove  A. Vaccine banks for controlling dog-mediated rabies. Rev Sci Tech. 2018;37:5118. DOIPubMedGoogle Scholar
  71. Jeon  S, Cleaton  J, Meltzer  MI, Kahn  EB, Pieracci  EG, Blanton  JD, et al. Determining the post-elimination level of vaccination needed to prevent re-establishment of dog rabies. PLoS Negl Trop Dis. 2019;13:e0007869. DOIPubMedGoogle Scholar
  72. Anderson  A, Kotzé  J, Shwiff  SA, Hatch  B, Slootmaker  C, Conan  A, et al. A bioeconomic model for the optimization of local canine rabies control. PLoS Negl Trop Dis. 2019;13:e0007377. DOIPubMedGoogle Scholar
  73. Borse  RH, Atkins  CY, Gambhir  M, Undurraga  EA, Blanton  JD, Kahn  EB, et al. Cost-effectiveness of dog rabies vaccination programs in East Africa. PLoS Negl Trop Dis. 2018;12:e0006490. DOIPubMedGoogle Scholar
  74. Darkaoui  S, Cliquet  F, Wasniewski  M, Robardet  E, Aboulfidaa  N, Bouslikhane  M, et al. A century spent combating rabies in Morocco (1911–2015): how much longer? Front Vet Sci. 2017;4:78. DOIPubMedGoogle Scholar

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Page updated: November 19, 2020
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