Achieving Population-Level Immunity to Rabies in Free-Roaming Dogs in Africa and Asia

PLoS Neglected Tropical Diseases

Volumn 8, Issue 11, 2014, Pages

  Morters, Michelle K ^a   McKinley, Trevelyan J ^a   Horton, Daniel L ^b,c   Cleaveland, Sarah ^d   Schoeman, Johan P ^e   Restif, Olivier ^a   Whay, Helen R ^f   Goddard, Amelia ^e   Fooks, Anthony R ^b,g   Damriyasa, I Made ^h   Wood, James L N ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY OF PRETORIA   (South Africa)

^f UNIVERSITY OF BRISTOL   (United Kingdom)

^g UNIVERSITY OF LIVERPOOL   (United Kingdom)

^h UDAYANA UNIVERSITY   (Indonesia)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM HYDROXIDE; NEUTRALIZING ANTIBODY; RABIES VACCINE; RABIES VIRUS GLYCOPROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS ANTIBODY;

ANCYLOSTOMA; ANIMAL EXPERIMENT; ARTICLE; BLOOD CELL COUNT; BLOOD SAMPLING; COHORT ANALYSIS; CONTROLLED STUDY; DEMODEX CANIS; DERMATITIS; DOG; FEMALE; GENDER; GEOMETRIC MEAN TITRE; HEALTH STATUS; IMMUNITY; IMMUNOLOGICAL PARAMETERS; LACTATION; LONGITUDINAL STUDY; LYSSAVIRUS; MALE; MORTALITY; NONHUMAN; RABIES; SYMPTOM; VACCINATION; VIRUS NEUTRALIZATION; ANIMAL; BIOLOGICAL MODEL; BLOOD; DOG DISEASES; IMMUNOLOGY; INDONESIA; MASS IMMUNIZATION; RABIES VIRUS; SEROCONVERSION; SOUTH AFRICA; VETERINARY;

ANIMALS; ANTIBODIES, VIRAL; COHORT STUDIES; DOG DISEASES; DOGS; FEMALE; INDONESIA; LONGITUDINAL STUDIES; MALE; MASS VACCINATION; MODELS, BIOLOGICAL; RABIES; RABIES VACCINES; RABIES VIRUS; SEROCONVERSION; SOUTH AFRICA; VACCINATION;

EID: 84920391955     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003160     Document Type: Article

References (86)

1. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, et al. (2005) Re-evaluating the burden of rabies in Africa and Asia. Bulletin of the World Health Organization 83: 360–368.
2. Ezeokoli CD, Umoh JU, (1987) Epidemiology of rabies in northern Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 81: 268–272.
3. Butler JRA, Bingham J, (2000) Demography and dog-human relationships of the dog population in Zimbabwean communal lands. The Veterinary Record 147: 442–446.
4. Kitala PM, McDermott JJ, Coleman PG, Dye C, (2002) Comparison of vaccination strategies for the control of dog rabies in Machakos District, Kenya. Epidemiology and Infection 129: 215–222.
5. Kayali U, Mindekem R, Yemadji N, Oussiguere A, Naissengar S, et al. (2003) Incidence of canine rabies in N'Djamena, Chad. Preventive Veterinary Medicine 61: 227–233.
6. Windiyaningsih C, Wilde H, Meslin F-X, Suroso T, Widarso HS, (2004) The rabies epidemic on Flores Island, Indonesia (1998–2003). Journal of the Medical Association of Thailand 87: 1389–1393.
7. Kasempimolporn S, Jitapunkul S, Sitprija V, (2008) Moving towards the elimination of rabies in Thailand. Journal of the Medical Association of Thailand 91: 433–437.
8. Reece JF, Chawla SK, (2006) Control of rabies in Jaipur, India, by the sterilisation and vaccination of neighbourhood dogs. The Veterinary Record 159: 379–383.
9. Gsell A, Knobel DL, Cleaveland S, Kazwala RR, Vounatsou P, et al. (2012) Domestic dog demographic structure and dynamics relevant to rabies control in urban areas in Africa: the case of Iringa, Tanzania. BMC Veterinary Research 8: 1–10.
10. Estrada R, Vos A, De Leon R, Mueller T, (2001) Field trial with oral vaccination of dogs against rabies in the Philippines. BMC Infectious Diseases 1: 1–7.
11. Lembo T, Hampson K, Kaare MT, Ernest E, Knobel D, et al. (2010) The feasibility of canine rabies elimination in Africa: dispelling doubts with data. PLoS Neglected Tropical Diseases 4: 1–9.
12. Knobel DL, Lembo T, Morters M, Townsend SE, Cleaveland S, et al. (2013) Dog rabies and its control. In: Jackson AC, editor. Rabies: scientific basis of the disease and its management, 3rd edition. United States: Elsevier. pp. 591–615.
13. Cleaveland S, Kaare M, Tiringa P, Mlengeya T, Barrat J, (2003) A dog rabies vaccination campaign in rural Africa: impact on the incidence of dog rabies and human dog-bite injuries. Vaccine 21: 1965–1973.
14. Cleaveland S, Kaare M, Knobel D, Laurenson MK, (2006) Canine vaccination - providing broder benefits for disease control. Veterinary Microbiology 117: 43–50.
15. Schneider MC, Belotto A, Ade MP, Correa E, Tamayo H, et al. (2005) Epidemiological situation of human rabies in Latin America in 2004. Epidemiological Bulletin/Pan-American Health Organization 26: 2–4.
16. WHO (2013) World Health Organization Expert Consultation on Rabies Second Report. Geneva: World Health Organization.
17. Council of Europe (2008) European pharmacopoeia Rabies vaccine (inactivated) for veterinary use. France: Council of Europe.
18. Jackson AC (2013) Rabies: Scientific basis of the disease and its management; Jackson AC, editor. San Diego, United States: Academic Press.
19. Morters MK, McKinley TJ, Restif O, Conlan AJK, Cleaveland S, et al. (2014) The demography of free-roaming dog populations and applications to disease and population control. Journal of Applied Ecology 51: 1096–1106.
20. Mitmoonpitak C, Tepsumethanon V, Wilde H, (1998) Rabies in Thailand. Epidemiology and Infection 120: 165–169.
21. Roitt I, Brostoff J, Male D (2001) Immunology 6th Edition. United Kingdom: Mosby.
22. Dionigi R, Zonta A, Dominioni L, Gnes F, Ballabio A, (1977) The effects of total parenteral nutrition on immunodepression due to malnutrition. Annals of Surgery 185: 467–474.
23. MSD (2013) Nobivac rabies data sheet. MSD Animal Health, United Kingdom. United Kingdom.
24. Hampson K, Dushoff J, Cleaveland S, Haydon DT, Kaare M, et al. (2009) Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biology 7(3): 462–471.
25. Johnson N, Cunningham AF, Fooks AR, (2010) The immune response to rabies virus infection and vaccination. Vaccine 28: 3896–3901.
26. Moore SM, Hanlon CA, (2010) Rabies-specific antibodies: measuring surrogates of protection against a fatal disease. PLoS Neglected Tropical Diseases 4: 1–7.
27. Siegrist C-A (2008) Vaccine immunology. In: Plotkin S, Orenstein W, Offit P, editors. Vaccines. United States: Suanders. pp. 17–36.
28. Corradi A, Ferrari L, Borghetti P, (2007) Parameters for evaluating the cell-mediated immune response during viral infection: diagnostic and prognostic applications. Veterinary Research Communications 31: 103–107.
29. Arya SC, Agarawal N, (2006) Immunogenicity of newly introduced Vero cell rabies vaccine. Vaccine 24: 847–848.
30. Thraenhart O, Kreuzfelder E, Hillebrandt M, Marcus I, Ramakrishnan K, et al. (1994) Long-term humoral and cellular immunity after vaccination with cell-culture rabies vaccine in man. Clinical Immunology and Immunopathology 71: 287–292.
31. Sikes RK, Peacock GV, Acha P, Arko RJ, Dierks R, (1971) Rabies vaccines: duration-of-immunity study in dogs. Journal of the American Veterinary Medical Association 159: 1491–1499.
32. Lodmell DL, Ewalt LC, Parnell MJ, Rupprecht CE, Hanlon CA, (2006) One-time intradermal DNA vaccination in ear pinnae one year prior to infection protects dogs against rabies virus. Vaccine 24: 412–416.
33. Brown AL, Merry D, L, Beckenhauer WH, (1973) Modified live-virus rabies vaccine produced from Flury high egg-passage virus grown on an established canine-kideny cell line: three-year duration of immunity study in dogs. American Journal of Veterinary Research 34: 1427–1432.
34. Bahloul C, Taieb D, Diouani MF, Ahmed SBH, Chtourou Y, et al. (2006) Field trials of a very potent rabies DNA vaccine which induced long lasting virus neutralizing antibodies and protection in dogs in experimental conditions. Vaccine 24: 1063–1072.
35. Hu RL, Fooks AR, Zhang SF, Liu Y, Zhang F, (2008) Inferior rabies vaccine quality and low immunization coverage in dogs (Canis familiaris) in China. Epidemiology and Infection 136: 1556–1563.
36. Minke JM, Bouvet J, Cliquet F, Wasniewski M, Guiot AL, et al. (2009) Comparison of antibody responses after vaccination with two inactivated rabies vaccines. Veterinary Microbiology 133: 283–286.
37. Aubert MFA, (1992) Practical significance of rabies antibodies in cats and dogs. Revue Scientifique et Technique-Office International 11: 735–760.
38. Bunn TO, Ridpath HD, Beard PD (1984) The relationship between rabies antibody titres in dogs and cats and protection from challenge. Georgia, USA: Centres for Disease Control.
39. Sharpee RL, Nelson LD, Beckenhauer WH (1985) Inactivated tissue culture rabies vaccine with three years immunogenicity in dogs and cats; Kuwert E, Merieux C, Koprowski H, Bogel K, editors. Berlin: Springer-Verlag. 262–269 p.
40. Precausta P, Soulebot JP, Chappius G, Brun A, Bugand M, et al. (1985) NIL2 cell inactivated tissue culture vaccine against rabies - immunization of carnivores; Kuwert E, Merieux C, Koprowski H, Bogel K, editors. Berlin: Springer-Verlag. 227–240 p.
41. Bunn TO (1991) Canine and feline vaccines, past and present. In: Baer GM, editor. The natural history of rabies. United States: CRC Press. pp. 415–425.
42. Cliquet F, Aubert M, Sagne L, (1998) Development of a fluorescent antibody virus neutralisation test (FAVN test) for the quantificaiton of rabies-neutralising antibody. Journal of Immunological Methods 212: 79–87.
43. Ondrejkova A, Suli J, Ondrejka R, Benisek Z, Franka R, et al. (2002) Comparison of the detection and quantification of rabies antibodies in canine sera. Veterinarni Medicina 47: 218–221.
44. Sharpee RL, Nelson LD, Beckenhauer WH (1985) Inactivated tissue culture rabies vaccine with three years immunogenicity in dogs and cats; Kuwert E, Merieux C, Koprowski H, Bogel K, editors. Berlin: Springer-Verlag.
45. Kennedy I (1998) Quarantine and rabies: a reappraisal. Report by the advisory group on quarantine to the Rt Hon Nick Brown MP, Minister of Agriculture, Fisheries and Food. London.
46. CDC (2008) Centers for Disease Control and Prevention: Recommendations of the Advisory Committee on Immunization Practices (ACIP). United States. 1–36 p.
47. Moore SE, Goldblatt D, Bates CJ, Prentice AM, (2003) Impact of nutritional status on antibody responses to different vaccines in undernourished Gambian children. Acta Paediatrica 92: 170–176.
48. Tepsumethanon W, Polsuwan C, Lumlertdaecha B, Khawplod P, Hemachudha T, et al. (1991) Immune response to rabies vaccine in Thai dogs: a preliminary report. Vaccine 9: 627–630.
49. Berndtsson LT, Nyman A-KJ, Rivera E, Klingeborn B, (2011) Factors associated with the success of rabies vaccination of dogs in Sweden. Acta Veterinaria Scandinavica 53: 1–7.
50. Cliquet F, Verdier Y, Sagne L, Aubert M, Schereffer JL, et al. (2003) Neutralising antibody titration in 25,000 sera of dogs and cats vaccinated against rabies in France, in the framework of the new regulations that offer an alternative to quarantine. Revue Scientifique et Technique-Office International 22: 857–866.
51. Jakel V, Konig M, Cussler K, Hanschmann K, Thiel H-J (2008) Factors influencing the antibody response to vaccination against rabies. Scientific & Technical Department of the OIE. 431–437 p.
52. Sage G, Khawplod P, Wilde H, Lobaugh C, Hemachudha T, et al. (1993) Immune response to rabies vaccine in Alaskan dogs: failure to achieve a consistently protective antibody response. Transactions of the Royal Society of Tropical Medicine and Hygiene 87: 593–595.
53. Sihvonen L, Kulonen K, Neuvonen E, Pekkanen K, (1996) Rabies antibodies in vaccinated dogs. Acta Veterinaria Scandinavica 36: 87–91.
54. Wilde H, Chutivongse S, Tepsumethanon W, Choomkasien P, (1991) Rabies in Thailand. Reviews of Infectious Diseases 13: 644–652.
55. Chomel B, Chappuis G, Bullon F, Cardenas E, David de Beublain T, et al. (1987) Serological results of a dog vaccination campaign against rabies in Peru. Revue Scientifique et Technique-Office International 6: 97–113.
56. Tizard I, Ni Y, (1998) Use of serological testing to assess immune status of companion animals. Journal of the American Veterinary Medical Association 213: 54–60.
57. Weiss DJ, Wardrop JK (2010) Schalm's veterinary hematology 6th edition; Weiss DJ, Wardrop JK, editors. United States: Wiley Blackwell.
58. Phillips TR, Jensen JL, Rubino MJ, Yang WC, Schultz R, (1989) Effects of vaccines on the canine immune system. Canadian Journal of Veterinary Research 53: 154–160.
59. Miyamoto T, Taura Y, Une S, Yoshitake M, Nakama S, et al. (1992) Changes in blastogenic responses of lymphocytes and delayed type hypersensivity responses after vaccination in dogs. Journal of Veterinary Medical Science 54: 945–950.
60. Strasser A, May B, Teltscher A, Wistrela E, Niedermuller H, (2003) Immune modulation following immunization with polyvalent vaccines in dogs. Veterinary Immunology and Immunopathology 94: 113–121.
61. Baron RB, (1986) Malnutrition in hospitalized patients - diagnosis and treatment. Western Journal of Medicine 144: 63–67.
62. Morters MK, Bharadwaj S, Cleaveland S, Whay HR, Damriyasa IM, et al. (2014) Participatory methods for the assessment of the ownership status of free-roaming dogs in Bali, Indonesia, for disease control and animal welfare. Preventive Veterinary Medicine 116: 203–208.
63. Merial (2013) Rabisin rabies data sheet. United Kingdom.
64. Kennedy LJ, Lunt M, Barnes A, McElhinney L, Fooks AR, et al. (2007) Factors influencing the antibody response of dogs vacccinated against rabies. Vaccine 25: 8500–8507.
65. Miller WH, Griffin CE, Campbell KL (2013) Muller & Kirk's Small Animal Dermatology 7th Edition. St. Louis, United States: Elsevier.
66. Guaguere E, Prelaud P, Craig M (2008) A practical guide to canine dermatology. Italy: Merial.
67. Mansfield KL, Burr PD, Snodgrass DR, Sayers R, Fooks AR, (2004) Factors affecting the serological response of dogs and cats to rabies vaccination. The Veterinary Record 154: 423–426.
68. WHO (1996) Laboratory techniques in rabies, 4th edition. World Health Organization, Geneva.
69. Horton DL, McElhinney LM, Marston DA, Wood JLN, Russell CA, et al. (2010) Quantifying antigenic relationships among the Lyssaviruses. Journal of Virology 84: 11841–11848.
70. Soulsby EJL (1982) Helminths, arthropods and protozoa of domestic animals, 7th edition. United States: Bailliere Tindall.
71. Pinheiro J, Bates D, DebRoy S, Deepayan S, Team RDC (2013) nlme: Linear and nonlinear mixed effects models. R package version 3.1-109 ed.
72. R Core Team (2013) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
73. Venables WN, Ripley BD (2002) Modern applied statistics with S. United States: Springer.
74. Caughley G (1977) Analysis of vertebrate populations. United States: The Blackburn Press.
75. Pianka ER (1999) Vital statistics of populations; Cummings B, editor. United States.
76. Thoresen SI, Tverdal A, Havre G, Morberg H, (1995) Effects of storage time and freezing temperature on clinical chemical parameters from canine serum and heparinzed plasma. Veterinary Clinical Pathology 24: 129–133.
77. Reynolds B, Taillade B, Medaille C, Palenche F, Trumel C, et al. (2006) Effect of repeated freeze-thaw cycles on routine plasma biochemical constituents in canine plasma. Veterinary Clinical Pathology 35: 339–340.
78. Gilbert A, Fooks AR, Hayman DTS, Horton DL, Muller T, et al. (2013) Deciphering serology to further understand the ecology of infectious diseases in wildlife. Ecohealth 10: 298–313.
79. Minnaar WN, Krecke RC, (2001) Helminths in dogs belonging to people in a resource-limited urban community in Gauteng, South Africa. Onderstepoort Journal of Veterinary Research 68: 111–117.
80. Minnaar WN, Krecke RC, Rajput JI, (1999) Helminth parasites of dogs from two resource-limited communities in South Africa. Journal of the South African Veterinary Association 70: 92–94.
81. Lloyd S, Amerasinghe PH, Soulsby EJL, (1983) Periparturient immunosupression in the bitch and its influence on infection with Toxocara canis. Journal of Small Animal Practice 24: 237–247.
82. Lloyd S, (1983) Effects of pregnancy and lactation upon infection. Veterinary Immunology and Immunopathology 4.
83. Putra AAG, Hampson K, Girardi J, Hiby E, Knobel D, et al. (2013) Responses to a rabies epidemic, Bali, Indonesia, 2008–2011. Emerging Infectious Diseases 19: 648–651.
84. Kaare M, Lembo T, Hampson K, Ernest E, Estes A, et al. (2009) Rabies control in rural Africa: evaluating strategies for effective domestic dog vaccination. Vaccine 27: 152–160.
85. Bogel K, Joshi DD, (1990) Accessibility of dog populations for rabies control in Kathmandu, Nepal. Bulletin of the World Health Organization 68: 611–617.
86. Durr S, Mindekem R, Kaninga Y, Moto DD, Meltzer MI, et al. (2009) Effectiveness of dog rabies vaccination programmes: comparison of owner-charged and free vaccination campaigns. Epidemiology and Infection 137: 1558–1567.