Rabies and rabies-related viruses: A modern perspective on an ancient disease

OIE Revue Scientifique et Technique

Volumn 23, Issue 2, 2004, Pages 625-642

  Cliquet, F ^a   Picard Meyer, E ^a  

^a WORLD HEALTH ORGANIZATION   (Switzerland)

Author keywords

Bat rabies; Bats; Epidemiology; Lyssavirus; Rabies; Terrestrial rabies

Indexed keywords

ANIMALIA; LYSSAVIRUS; RABIES VIRUS;

EID: 13244288753     PISSN: 02531933     EISSN: None     Source Type: Journal    
DOI: 10.20506/rst.23.2.1514     Document Type: Review

References (100)

1. Advisory Committee on Immunization Practices (ACIP) (1999). - Human rabies prevention - United States, 1999. Recommendations of the ACIP. MMWR Recomm. Rep., 48 (RR-1), 1-21.
2. Allworth A., Murray K. & Morgan K. (1996). - A human case of encephalitis due to a lyssavirus recently identified in fruit bats. Communic. Dis. Intell., 20 (24), 504.
3. Amengual B., Whitby J.E., King A., Cobo J.S. & Bourhy H. (1997). - Evolution of European bat lyssaviruses. J. gen. Virol., 78 (9), 2319-2328.
4. Anon. (1997). - Australian bat lyssavirus, information for medical practitioners. In Recommendations of the Lyssavirus Expert Group Meeting, 11 November 1996, Communicable Diseases Network, Australia, New Zealand. Medicine Australia, the Online Journal of Medicine. Website: http://medicineau.net.au/ clinical/internalmedicine/internal med1502.html (accessed on 25 August 2004).
5. Anon. (2003). - Rabies cases per country and administrative units, 4th quarter 2003. Rabies Bull. Eur., 27 (4), 1-27.
6. Arai Y.T., Kuzmin I.V., Kameoka Y. & Botvinkin A.D. (2003). - New lyssavirus genotype from the lesser mouse-eared bat (Myotis blythi), Kyrghyzstan. Emerg. infect. Dis., 9 (3), 333-337.
7. Arguin P.M., Murray-Lillibridge K., Miranda M.E.G., Smith J.S., Calaor A.B. & Rupprecht C.E. (2002). - Serologic evidence of Lyssavirus infections among bats, the Philippines. Emerg. infect. Dis., 8 (3), 258-262.
8. Atanasiu P., Perrin P., Favre S., Chevallier G. & Tsiang H. (1974). - Immunofluorescence and immunoperoxydase in the diagnosis of rabies. In Viral immunodiagnosis (E. Kurstak & R. Morisset, eds). Academic Press Inc., New York, 141-155.
9. Aubert M. (1992). - Epidemiology of fox rabies. In Wildlife rabies control (K. Bögel, F.-X. Meslin & M. Kaplan, eds). Wells Medical Ltd, Tunbridge Wells, 9-18.
10. Aubert M. (1999). - Costs and benefits of rabies control in wildlife in France. In The economics of animal disease control (B.D. Perry, ed.). Rev. sci. tech. Off. int. Epiz., 18 (2), 533-543.
11. Aubert M., Cliquet F. & Hammami S. (2000). - De la vaccination orale du renard contre la rage à l'élimination de la rage canine. Bull. Soc. Vêt. Prat. Fr., 84 (1), 17-28.
12. Badrane H., Bahloul C., Perrin P. & Tordo N. (2001). - Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J. Virol., 75 (7), 3268-3276.
13. Barrat J., Barrat M.J., Müller T. & Cliquet F. (2003). - European interlaboratory FAT comparison test 2001. Rabies Bull. Eur., 27 (1), 7-12.
14. Belotto A.J. (2001). - Vaccination against dog rabies in urban centres of Latin America: experience in Brazil and Mexico. In Rabies control in Asia (B. Dodet, F.-X. Meslin & E. Heseltine, eds). John Libbey Eurotext, Paris, 73-76.
15. Belotto A.J., Leanes L.F., Schneider M.C., Correa E. & Tamayo H. (2003). - Rabies in South America: regional program for the elimination of rabies in the Americas. In Rabies in the Americas. Proc. XIV International conference on rabies in the Americas, 19-24 October, Philadelphia, Pennsylvania, 47 pp.
16. Bingham J. (2001). - Rabies in Flores, Indonesia: comparisons and contrasts to rabies control in Africa. In Proc. VI Southern and Eastern African Rabies Group (SEARG) meeting, 18-21 June, Lilongwe, Malawi. Editions Fondation Mérieux, Lyons, 127-130.
17. Bingham J., Schumacher C.L., Hill F.W.G. & Aubert A. (1999). - Efficacy of SAG-2 oral rabies vaccine in two species of jackal (Canis adustus and Canis mesomelas). Vaccine, 17 (6), 551-558.
18. Black E.M., McElhinney L.M., Lowings J.P., Smith J., Johnstone P. & Heaton P.R. (2000). - Molecular methods to distinguish between classical rabies and the rabies-related European bat lyssaviruses. J. virol. Meth., 87 (1/2), 123-131.
19. Blancou J. (1988). - Epizootiology of rabies: Eurasia and Africa. In Rabies (J.B. Campbell & K.M. Charlton, eds). Kluwer Academic Publishers, Boston, 243-265.
20. Botvinkin A.D., Poleschuk E.M., Kuzmin I.V., Borisova T.I., Gazaryan S.V., Yager P. & Rupprecht C.E. (2003). - Novel lyssaviruses isolated from bats in Russia. Emerg. infect. Dis., 9 (12), 1623-1625.
21. Boué F. (2002). - Biological regulation of dog populations, a key to reduce canine rabies. In Proc. XIII International meeting on research advances and rabies control in the Americas, 3-8 November, Oaxaca, Mexico, 61 pp.
22. Bourhy H., Rollin P.E., Vincent J. & Sureau P. (1989). - Comparative field evaluation of the fluorescent-antibody test, virus isolation from tissue culture, and enzyme immunodiagnosis for rapid laboratory diagnosis of rabies. J. clin. Microbiol., 27 (3), 519-523.
23. Bourhy H., Kissi B., Lafon M., Sacramento D. & Tordo N. (1992). - Antigenic and molecular characterization of bat rabies virus in Europe. J. clin. Microbiol., 30 (9), 2419-2426.
24. Bourhy H., Kissi B. & Tordo N. (1993). - Molecular diversity of the Lyssavirus genus. Virology, 194 (1), 70-81.
25. Brass D. (1994). - Rabies in bats: natural history and public health implications. Livia Press, Ridgefield, 335 pp.
26. Bruyère-Masson V., Barrat J., Cliquet F., Rotivel Y., Bourhy H., Brie P., Melik N., Gibon C. & Alvado-Brette B. (2001). - A puppy illegally imported from Morocco brings rabies to France. Rabies Bull. Eur., 25 (3), 12-13.
27. Cleaveland S. (1998). - The growing problem of rabies in Africa. In Proc. Royal Society of Tropical Medicine and Hygiene meeting at Manson House, London, 20 March 1997. Epidemiology and control of rabies. Trans. roy. Soc. trop. Med. Hyg., 92 (2), 131-134.
28. Cleaveland S., Fèvre E.M., Kaare M. & Coleman P.G. (2002). - Estimating human rabies mortality in the United Republic of Tanzania from dog bite injuries. Bull. WHO, 80 (4), 304-310.
29. 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 (17/18), 1965-1973.
30. Cliquet F., Lowings F., Barrat J. & Bruyère V. (1999). - A case of rabies diagnosed in France from an imported African bat. In Rabies in the Americas. Proc. X International rabies in the Americas conference, 14-19 November, San Diego, 72 pp.
31. Cliquet F., Seghaier C., Blasco E., Barrat J., Brochier B., Hammami S., Pastoret P.-P. & Aubert M. (2001). - Immunizing young dogs against rabies during mass vaccination may be a challenge. In Rabies control in Asia (B. Dodet, F.-X. Meslin & E. Heseltine, eds). John Libbey Eurotext, Paris, 126-136.
32. Coleman P.G., Fèvre E.M. & Cleaveland S. (2004). - Estimating the public health impact of rabies. Emerg. infect. Dis., 10(1), 140-142.
33. David D., Yakobson B., Rotenberg D., Dveres N., Davidson I. & Stram Y. (2002). - Rabies virus detection by RT-PCR in decomposed naturally infected brains. Vet. Microbiol., 87 (2), 111-118.
34. De Mattos C.A., Favi M., Yung Y., Pavletic C. & de Mattos C.C. (2000). - Bat rabies in urban centers in Chile. J. Wildl Dis., 36 (2), 231-240.
35. Dean D.J. & Abelseth M.K. (1973). - The fluorescent antibody test. In Laboratory techniques in rabies, 3rd Ed. (M.M. Kaplan & H. Koprowski, eds). World Health Organization (WHO) Monograph Series No. 23. WHO, Geneva, 73-84.
36. Direction de l'épidémiologie et de lutte contre les maladies (2003). - Lutte contre la rage chez l'homme. Guide des professionnels de la santé. Ministry of Health, Kingdom of Morocco, Rabat, 72 pp.
37. Dodet B., Meslin F.-X. & Aubert M. (2001). - Executive summary. In Rabies control in Asia (B. Dodet, F.-X. Meslin & E. Heseltine, eds). John Libbey Eurotext, Paris, 191-196.
38. Favi M., de Mattos C.A., Yung V., Chala E., Lopez L.R. & de Mattos C.C. (2002). - First case of human rabies in Chile caused by an insectivorous bat virus variant. Emerg. infect. Dis., 8(1), 79-81.
39. Field H., McCall B. & Barrett J. (1999). - Australian bat lyssavirus infection in a captive juvenile black flying fox. Emerg. infect. Dis., 5 (3), 438-440.
40. Fooks A.R., Brookes S.M., Johnson N., McElhinney L.M. & Hutson A.M. (2003). - European bat lyssaviruses: an emerging zoonosis. Epidemiol. Infect., 131 (3), 1029-1039.
41. Fraser G.C., Hooper P.T., Lunt R.A., Gould A.R., Gleeson L.J., Hyatt A.D., Russell G.M. & Kattenbelt J.A. (1996). - Encephalitis caused by a lyssavirus in fruit bats in Australia. Emerg. infect. Dis., 2 (4), 327-331.
42. Gould A.R., Hyatt A.D., Lunt R.A., Kattenbelt J.A., Hengstberger S. & Blacksell S.D. (1998). - Characterisation of a novel lyssavirus isolated from Pteropid bats in Australia. Virus Res., 54 (2), 165-187.
43. Gould A.R., Kattenbelt J.A., Gumley S.G. & Lunt R.A. (2002). - Characterisation of an Australian bat lyssavirus variant isolated from an insectivorous bat. Virus Res., 89 (1), 1-28.
44. Guyatt K.J., Twin J., Davis F., Holmes E.C., Smith G.A., Smith I.L., Mackenzie J.S. & Young P.L. (2003). - A molecular epidemiological study of Australian bat lyssavirus. J. gen. Virol., 84 (2), 485-496.
45. Hanlon C.A., Kuzmin I., Blanton J., Manangan J., Murphy S.M. & Rupprecht C.E. (2003). - Efficacy of rabies biologics against newly described Lyssaviruses. In Rabies in the Americas. Proc. XIV International conference on rabies in the Americas, 19-24 October, Philadelphia, 55-56.
46. Hanna J.N., Carney I.K., Smith G.A., Tannenberg A.E., Deverill J.E., Botha J.A., Serafin I.L., Harrower B.J., Fitzpatrick P.F. & Searle J.W. (2000). - Australian bat lyssavirus infection: a second human case, with a long incubation period. Med. J. Aust., 172 (12), 597-599.
47. Heaton P.R., Johnstone P., McElhinney L.M., Cowley R., O'Sullivan E. & Whitby J.E. (1997). - Heminested PCR assay for detection of six genotypes of rabies and rabies-related viruses. J. clin. Microbiol., 35 (11), 2762-2766.
48. Hooper P.T., Lunt R.A., Gould A.R., Samaratunga H., Hyatt A.D., Gleeson L.J., Rodwell B.J., Rupprecht C.E., Smith J.S. & Murray P.K. (1997). - A new lyssavirus - the first endemic rabies-related virus recognized in Australia. Bull. Inst. Pasteur, 95 (4), 209-218.
49. Hughes G.J., Smith J.S., Hanlon C.A. & Rupprecht C.E. (2004). - Evaluation of a TaqMan PCR assay to detect rabies virus RNA: influence of sequence variation and application to quantification of viral loads. J. clin. Microbiol., 42 (1), 299-306.
50. Johnson N., Black C., Smith J., Un H., McElhinney L.M., Aylan O. & Fooks A.R. (2003). - Rabies emergence among foxes in Turkey. J. Wildl. Dis., 39 (2), 262-270.
51. Johnson N., Selden D., Parsons G., Healy D., Brookes S.M., McElhinney L.M., Hutson A.M. & Fooks A.R. (2003). - Isolation of a European bat lyssavirus type 2 from a Daubenton's bat in the United Kingdom. Vet. Rec., 152 (13), 383-387.
52. Kamoltham T., Singhsa J., Promsaranee U., Sonthon P., Mathean P. & Thinyounyong W. (2003). - Elimination of human rabies in a canine endemic province in Thailand: five-year programme. Bull. WHO, 81 (5), 375-381.
53. Kamolvarin N., Tirawatnpong T., Rattanasiwamoke R., Tirawatnpong S., Panpanich T. & Hemachudha T. (1993). - Diagnosis of rabies by polymerase chain reaction with nested primers. J. infect. Dis., 167 (1), 207-210.
54. Kaplan M.M., Cohen D., Koprowski H., Dean D. & Ferrigan L. (1962).-Studies on the local treatment of wounds for the prevention of rabies. Bull WHO, 26, 765-775.
55. 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). J. Wildl. Dis., 38 (2), 352-362.
56. Koprowski H. (1973). - The mouse inoculation test. In Laboratory techniques in rabies, 3rd Ed. (M.M. Kaplan & H. Koprowski, eds). World Health Organization (WHO) Monograph Series No. 23. WHO, Geneva, 85-93.
57. Krebs J.W., Noll H.R., Rupprecht C.E. & Childs J.E. (2002). - Rabies surveillance in the United States during 2001. JAVMA, 221 (12), 1690-1701.
58. Kuzmin I.V. (2002). - Bat lyssaviruses in Central Asia: new evidence for genus diversity and potential significance for public health. In Proc. XIII International meeting on research advances and rabies control in the Americas, 3-8 November, Oaxaca, Mexico, 61 pp.
59. Kuzmin I.V., Orciari L.A., Arai Y.T., Smith J.S., Hanlon C.A., Kameoka Y. & Rupprecht C.E. (2003). - Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P and G gene sequences. Virus Res., 97 (2), 65-79.
60. Lang J., Hoa D.Q., Gioi N.V., Vien N.C., Nguyen C.V., Rouyrre N. & Forrat R. (1999). - Immunogenicity and safety of low-dose intradermal rabies vaccination given during an Expanded Programme on Immunization session in Viet Nam: results of a comparative randomized trial. Trans. roy. Soc. trop. Med. Hyg., 93 (2), 208-213.
61. Leney J. (2001). - Responsible dog ownership: an adapted concept for dog population management in Asian countries. In Rabies control in Asia (B. Dodet, F.-X. Meslin & E. Heseltine, eds). John Libbey Eurotext, London, 137-141.
62. McColl K.A., Chamberlain T., Lunt R., Newberry K. & Westbury H.A. (2001). - Studies with Australian bat lyssavirus in flying foxes, and domestic cats and dogs. In Proc. VI Southern and Eastern African Rabies Group (SEARG) meeting, 18-21 June, Lilongwe, Malawi. Editions Fondation Mérieux, Lyons, 101-104.
63. McElhinney L.M., Sawyer J., Finnegan C.J., Smith J. & Fooks A.R. (2002). - Use of rapid real-time PCR for the detection of rabies virus. In Rapid cycle real-time PCR: methods and applications (U. Reischl, C. Wittwer & F. Cockerill, eds). Springer Verlag, Berlin, 235-240.
64. McQuiston J.H., Yager P.A., Smith J.S. & Rupprecht C.E. (2001). - Epidemiologic characteristics of rabies virus variants in dogs and cats in the United States, 1999. JAVMA, 218(12), 1939-1942.
65. Martínez-Burnes J., López A., Medellín J., Haines D., Loza E. & Martínez M. (1997). - An outbreak of vampire battransmitted rabies in cattle in northeastern Mexico. Can. vet. J., 38 (3), 175-177.
66. Meslin F.-X. (2003). - The challenge to provide affordable rabies post-exposure treatment. Vaccine, 21 (27-30), 4122-4123.
67. Meslin F.-X., Stöhr K. & Heymann D. (2000). - Public health implications of emerging zoonoses. In An update on zoonoses (P.-P. Pastoret, ed.). Rev. sci. tech. Off. int. Epiz., 19 (1), 310-317.
68. Messenger S.L., Rupprecht CE. & Smith J.S. (2003). - Bats, emerging virus infections, and the rabies paradigm. In Bat ecology (T.H. Kunz & M.B. Fenton, eds). University of Chicago Press, Chicago, 622-667.
69. Müller T., Cox J., Peter W., Schäfer R., Bodamer P., Wulle U., Burow J. & Müller W. (2001). - Infection of a stone marten with European Bat Lyssa Virus (EBL1). Rabies Bull. Eur., 25 (3), 9-11.
70. Nadin-Davis S.A. (1998). - Polymerase chain reaction protocols for rabies virus discrimination. J. virol. Meth., 75 (1), 1-8.
71. Nadin-Davis S.A., Sheen M. & Wandeler A.I. (2003). - Use of discriminatory probes for strain typing of formalin-fixed, rabies virus-infected tissues by in situ hybridization. J. clin. Microbiol., 41 (9), 4343-4352.
72. Nel L.H., Thomson G.R. & von Teichman B.F. (1993). - Molecular epidemiology of rabies virus in South Africa. Onderstepoort J. vet. Res., 60 (4), 301-306.
73. Perera M.A., Harischandra P.A., Wimalaratne O. & Damboragama S.N. (2000). - Feasibility of canine oral rabies vaccination in Sri Lanka - a preliminary report. Ceylon med. J., 45 (2), 61-64.
74. Perrin P., Gontier C., Lecocq E. & Bourhy H. (1992). - A modified rapid enzyme immunoassay for the detection of rabies and rabies-related viruses: RREID-lyssa. Biologicals, 20 (1), 51-58.
75. Persing D.H., Smith T.F., Tenover F.C. & White T.J. (1993). - Diagnostic molecular biology: principles and applications. American Society for Microbiology, Washington, DC, 641 pp.
76. Picard-Meyer E., Bruyère V., Barrat J., Tissot E., Barrat M.J. & Cliquet F. (2004). - Development of a hemi-nested RT-PCR method for the specific determination of European Bat Lyssavirus 1: comparison with other rabies diagnostic methods. Vaccine, 22 (15/16), 1921-1929.
77. Puanghat A. (2001). - Human rabies in Thailand. Rabies in humans in India. In Rabies control in Asia (B. Dodet, F.-X. Meslin & E. Heseltine, eds). John Libbey Eurotext, Paris, 252-253.
78. Ronsholt L. (2002). - A new case of european bat lyssavirus (EBL) infection in Danish sheep. Rabies Bull. Eur., 26 (2), 15.
79. Rupprecht C.E., Hanlon C.A. & Hemachudha T. (2002). - Rabies re-examined. Lancet infect. Dis., 2 (6), 327-343.
80. Sacramento D., Bourhy H. & Tordo N. (1991). - PCR technique as an alternative method for diagnosis and molecular epidemiology of rabies virus. Molec. cell. Probes, 5 (3), 229-240.
81. Seghaier C., Cliquet F., Hammami S., Aouina T., Tlatli A. & Aubert M. (1999). - Rabies mass vaccination campaigns in Tunisia: are vaccinated dogs correctly immunized? Am. J. trop. Med. Hyg., 61 (6), 879-884.
82. Serra-Cobo J., Amengual B., Abellán C. & Bourhy H. (2002). - European bat Lyssavirus infection in Spanish bat populations. Emerg. infect. Dis., 8 (4), 413-420.
83. Servat A. & Cliquet F. (2001). - Rabies proficiency tests to appraise laboratories for approval to perform rabies serological tests. In Proc. XII International Meeting on advances in rabies research and control in the Americas, 12-16 November, Peterborough, Canada. Ontario Ministry of Natural Resources, 43-44.
84. Shope R.E., Murphy F.A., Harrison A.K., Causey O.R., Kemp G.E., Simpson D.I. & Moore D.L. (1970). - Two African viruses serologically and morphologically related to rabies virus. J. Virol., 6 (5), 690-692.
85. Smith J.S. (1996). - New aspects of rabies with emphasis on epidemiology, diagnosis, and prevention of the disease in the United States. Clin. Microbiol. Rev., 9 (2), 166-176.
86. Smith J.S. & Baer G.M. (1988). - Epizootiology of rabies: the Americas. In Rabies (J.B. Campbell & K.M. Charlton, eds). Kluwer Academic Publishers, Boston, 267-299.
87. Smith J.R., Rohde R., Mayes B., Parmely C. & Leslie L.M. (2001). - Molecular evidence for sustained transmission of a bat variant of rabies virus in skunks in Arizona. Paper presented at 12th International Meeting on advances in rabies research and control in the Americas, 12-16 November, Peterborough, Canada, 47.
88. Steck F. & Wandeler A. (1980). - The epidemiology of fox rabies in Europe. Epidemiol. Rev., 2, 71-96.
89. Sugiyama M., Ito N. & Minamoto N. (2003). - Isothermal amplification of rabies virus gene. J. vet. med. Sci., 65 (10), 1063-1068.
90. Swanepoel R., Barnard B.J.H., Meredith C.D., Bishop G.C., Bruckner G.K., Foggin C.M. & Hubschle O.J.B. (1993). - Rabies in southern Africa. Onderstepoort J. vet. Res., 60 (4), 325-346.
91. Tidemann C.R., Vardon M.J., Nelson J.E., Speare R. & Gleeson L.J. (1997). - Health and conservation implications of Australian bat Lyssavirus. Aust. Zool., 30, 369-376.
92. Uhaa I.J., Dato V.M., Sorhage F.E., Beckley J.W., Roscoe D.E., Gorsky R.D. & Fishbein D.B. (1992). - Benefits and costs of using an orally absorbed vaccine to control rabies in raccoons. JAVMA, 201 (12), 1873-1882.
93. Warner C.K., Zaki S.R., Shieh W.J., Whitfield S.G., Smith J.S., Orciari L.A., Shaddock J.H., Niezgoda M., Wright C.W., Goldsmith C.S., Sanderlin D.W., Yager P.A. & Rupprecht C.E. (1999). - Laboratory investigation of human deaths from vampire bat rabies in Peru. Am. J. trop. Med. Hyg., 60 (3), 502-507.
94. Wiktor T.J. & Koprowski H. (1978). - Monoclonal antibodies against rabies virus produced by somatic cell hybridization: detection of antigenic variants. Proc. natl Acad. Sci. USA, 75 (8), 3938-3942.
95. World Health Organization (WHO) (1992). - WHO Expert Committee on Rabies: eighth report. WHO Technical Report Series No. 824. World Health Organization, Geneva, 84 pp.
96. World Health Organization (WHO) (1990-1999). - World survey of rabies, Nos 26-35 for the years 1990-1999. WHO, Geneva.
97. World Health Organization (WHO) (2001). - Strategies for the control and elimination of rabies in Asia. Report of a WHO interregional consultation. Report of the workshop on rabies control in Asian countries, 17-21 July, Geneva. WHO, Geneva, 32 pp.
98. World Health Organization (WHO) (2004). - Dog rabies control activities currently implemented. Website: http://www.who.int/rabies/animal/ rabies_control_activities_morinfo/en/ (accessed on 8 November 2004).
99. World Society for the Protection of Animals (WSPA) (1994). - Stray dog control. WSPA, London, 49 pp.
100. Yongxin Y. & Qing T. (2001). - Rabies and rabies control in China. In Rabies control in Asia (B. Dodet, F.-X. Meslin & E. Heseltine, eds). John Libbey Eurotext, Paris, 210-211.