Abstract
Lyssaviruses continue to evolve and pose threats to humans, domestic animals, and wildlife. As a fatal disease of zoonotic importance, rabies is fortunately preventable, thanks to the advent of potent biologics. Pioneering works done during the last two centuries act as cornerstone of research making rabies diagnosis, prevention, control, and selective elimination possible. The field has benefited immensely from the tremendous scientific advancement during the last three decades in virology, molecular biology, vaccinology, and delivery systems. Vaccines have evolved from the first generation of crude nerve tissue-based products to recombinant vaccines. Cell culture-based inactivated rabies vaccines for intramuscular (IM) and intradermal (ID) use in humans continue to play a pivotal role when it comes to rabies prophylaxis. Parenteral and oral vaccinations prove time and again promising tools for rabies control in domestic animals and wildlife. Improvements likely to cause paradigm shift include products based on virus-like particles, obviating the need for a high containment facility; sparing usage of antigens using new adjuvants; delivery using novel systems; and direct inoculation of potent vaccines without the need of rabies immune globulin (RIG).
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References
Patel MR, Emerman M, Malik HS. Paleovirology—ghosts and gifts of viruses past. Curr Opin Virol. 2011;1:304–9.
Katzourakis A. Paleovirology: inferring viral evolution from host genome sequence data. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120493.
Aiewsakun P, Katzourakis A. Endogenous viruses: connecting recent and ancient viral evolution. Virology. 2015;479–480:26–37.
Metegnier G, Becking T, Chebbi MA, Giraud I, Moumen B, Schaack S, et al. Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups. Mob DNA. 2015;6:16.
Rupprecht C, Kuzmin I, Meslin F. Lyssaviruses and rabies: current conundrums, concerns, contradictions and controversies. F1000Res. 2017 Feb 23;6:184.
Hayman DT, Fooks AR, Marston DA, Garcia-R JC. The global phylogeography of lyssaviruses—challenging the ‘Out of Africa’ hypothesis. PLoS Negl Trop Dis. 2016;10:e0005266.
Remlinger P. Le passage du virus rabique à travers les filtres. Ann Inst Pasteur. 1903;17:834–49.
Negri A. Contributoallo studio dell’eziologiadellarabbia. Boll Soc Med-Chir Pavia. 1903;2:88–115.
Fermi C. Immunisierung der muridenmitWut. Zeitschriftfür Hygiene und Infektionskrankheiten. 1908;58:233–76.
Webster LT, Dawson JR. Early diagnosis of rabies by mouse inoculation. Measurement of humoral immunity to rabies by mouse protection test. Proc Soc Exper Biol Med. 1935;32:570–3.
Habel K. Evaluation of a mouse test for the standardization of the immunizing power of antirabies vaccines. Pub Health Rep. 1940;55:1473–87.
Reagan RL, Brueckner AL. Electron micrographs of Negri bodies found in rabies. J Infect Dis. 1950;87:213–6.
Fuenzalida E, Palacios R. An improved method for preparation of rabies vaccine. Bol Inst bact Chile. 1955;8:3–10.
Kissling RE. Growth of rabies virus in non-nervous tissue culture. Proc Soc Exp Biol Med. 1958;98:223–5.
Goldwasser RA, Kissling RE. Fluorescent antibody staining of street and fixed rabies virus antigens. Proc Soc Exp Biol Med. 1958;98:219–23.
Dietzschold B, Cox JH, Schneider G. Structure and function of rabies virus glycoprotein. Dev Biol Stand. 1978;40:45–55.
Wiktor TJ, Koprowski H. Monoclonal antibodies against rabies virus produced by somatic cell hybridization: detection of antigenic variants. Proc Natl Acad Sci U S A. 1978;75:3938–42.
Yelverton E, Norton S, Obijeski JF, Goeddel DV. Rabies virus glycoprotein analogs: biosynthesis in Escherichia coli. Science. 1983;219:614–20.
Sacramento D, Bourhy H, Tordo N. PCR technique as an alternative method for diagnosis and molecular epidemiology of rabies virus. Mol Cell Probes. 1991;5:229–40.
Smith JS, Orciari LA, Yager PA, Seidel HD, Warner CK. Epidemiologic and historical relationships among 87 rabies virus isolates as determined by limited sequence analysis. J Infect Dis. 1992;166:296–307.
Conzelmann KK, Meyers G. Genetic engineering of animal RNA viruses. Trends Microbiol. 1996;4:386–93.
Rosner F. Rabies in the Talmud. Med Hist. 1974;18:198–200.
Wilkinson L. The development of the virus concept as reflected in corpora of studies on individual pathogens. 4. Rabies—two millennia of ideas and conjecture on the aetiology of a virus disease. Med Hist. 1977;21:15–31.
Carter KC. Nineteenth-century treatments for rabies as reported in the Lancet. Med Hist. 1982;26:67–78.
Jackson AC. Rabies: Scientific basis of the disease and its management. 3rd ed. Jackson AC, editor. Oxford: Academic; 2013.
Dalfardi B, Esnaashary MH, Yarmohammadi H. Rabies in medieval Persian literature—the Canon of Avicenna (980–1037 AD). Infect Dis Poverty. 2014;3:7.
Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, et al. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis. 2015;9:e0003709.
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;83:360–8.
Crowcroft NS, Thampi N. The prevention and management of rabies. Br Med J. 2015;350:g7827.
Manning SE, Rupprecht CE, Fishbein D, Hanlon CA, Lumlertdacha B, Guerra M, et al. Human rabies prevention-United States, 2008: recommendations of the Advisory Committee on Immunization Practices. MMWR Recomm Rep. 2008;57:1–28.
Rupprecht CE, Briggs D, Brown CM, Franka R, Katz SL, Kerr HD, et al. Use of a reduced (4-dose) vaccine schedule for postexposure prophylaxis to prevent human rabies: recommendations of the advisory committee on immunization practices. MMWR Recomm Rep. 2010;59:1–9.
Dodet B, Durrheim DN, Rees H. Rabies: underused vaccines, unnecessary deaths. Vaccine. 2014;32:2017–9.
Semple D. On the nature of rabies and antirabic treatment. Br Med J. 1919;2:333–6.
Hemachudha T, Griffin DE, Chen WW, Johnson RT. Immunologic studies of rabies vaccination-induced Guillain-Barré syndrome. Neurology. 1988;38:375–8.
Arya SC. Transmissible spongiform encephalopathies and sheep-brain derived rabies vaccines. Biologicals. 1994;22:73.
Fuenzalida E, Palacios R, Borgono JM. Antirabies antibody response in man to vaccine made from infected suckling—mouse brains. Bull World Health Organ. 1964;30:431–6.
Peck FB Jr, Powell HM. Culbertson CG. A new antirabies vaccine for human use; clinical and laboratory results using rabies vaccine made form embryonated duck eggs. J Lab Clin Med. 1955;45:679–83.
Sumbali Gand Mehrotra RS. Cultivation of animal viruses. In: Principles of microbiology. New Delhi: Tata McGraw-Hill; 2009. p. 213.
WHO Expert committee on Rabies. Seventh report, WHO technical report series 709. Geneva: WHO; 1984. p. 1–104.
Montomoli E, Khadang B, Piccirella S, Trombetta C, Mennitto E, Manini I, et al. Cell culture-derived influenza vaccines from Vero cells: a new horizon for vaccine production. Expert Rev Vaccines. 2012;11:587–94.
Glück R, Matthieu JM, Wegmann A, Méan F. Absence of myelin basic protein in an improved purified duck embryo rabies vaccine. Neurochem Pathol. 1986;4:69–75.
Mahendra BJ, Madhusudana SN, Sampath G, Datta SS, Ashawathnarayana DH, Venkatesh GM, et al. Immunogenicity, safety and tolerance of a purified duck embryo vaccine (PDEV VAXIRAB) for rabies post-exposure prophylaxis: results of a multicentric study in India. Hum Vaccines. 2010;6:721–4.
Jordan I, Sandig V. Matrix and backstage: cellular substrates for viral vaccines. Viruses. 2014;6:1672–700.
Brookes SM, Parsons G, Johnson N, McElhinney LM, Fooks AR. Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses. Vaccine. 2005;23:4101–9.
Rupprecht CE, Hanlon CA, Hemachudha T. Rabies reexamined. Lancet Infect Dis. 2002;2:327–43.
Hernandez R, Sinodis C, Brown DT. Growth and maintenance of chick embryo fibroblasts (CEF). Curr Protoc Microbiol. 2010;17:A4I.1–8.
Kraus B, Von Fricks S, Feigl S, Koch SM, Fleischanderl D, Terler K, et al. Avian cell line—Technology for large scale vaccine production. BMC Proc. 2011;5:52.
Barrett PN, Mundt W, Kistner O, Howard MK. Vero cell platform in vaccine production: moving towards cell culture-based viral vaccines. Expert Rev Vaccines. 2009;8:607–18.
Enserink M. Influenza. Crisis underscores fragility of vaccine production system. Science. 2004;306:385.
Uscher-Pines L, Barnett DJ, Sapsin JW, Bishai DM, Balicer RD. A systematic analysis of influenza vaccine shortage policies. Pub Health. 2008;122:183–91.
Barth R, Franke V. Purified chick-embryo cell vaccine for humans. In: Meslin FX, Kaplan MM, Koprowski H, editors. Laboratory techniques in rabies. 4th ed. Geneva: WHO; 1996. p. 290–4.
Barth R, Gruschkau H, Jaeger O, Milcke L, Weinmann E. Purified chick embryo cell (PCEC) rabies vaccine for human use. Laboratory data. Behring Inst Mitt. 1984;76:142–54.
Vodopija I, Ljubicic M, Baklaic Z. Antibody response to PCEC rabies vaccine following abbreviated (3 dose) immunization schedules. In: Vodopija I, Nicholson KG, Smerdel S, Bijok U, editors. Improvements in rabies post-exposure treatment. Zagreb: Zagreb Institute of Public Health; 1985. p. 175–7.
Vodopija I, Sureau P, Lafon M, Baklaic Z, Ljubicic M, Svjetlicic M, et al. An evaluation of second generation tissue culture rabies vaccines for use in man: a four-vaccine comparative immunogenicity study using a pre-exposure vaccination schedule and an abbreviated 2-1-1 postexposure schedule. Vaccine. 1986;40:245–8.
Dreesen DW, Fishbein DB, Kemp DT, Brown J. Two-year comparative trial on the immunogenicity and adverse effects of purified chick embryo cell rabies vaccine for pre-exposure immunization. Vaccine. 1989;7:397–400.
Briggs DJ, Dreesen DW, Nicolay U, Chin JE, Davis R, Gordon C, et al. Purified Chick Embryo Cell Culture Rabies Vaccine: interchangeability with Human Diploid Cell Culture Rabies Vaccine and comparison of one versus two-dose post-exposure booster regimen for previously immunized persons. Vaccine. 2000;19:1055–60.
Finke S, Karger A, Freuling C, Müller T. Assessment of inactivated human rabies vaccines: biochemical characterization and genetic identification of virus strains. Vaccine. 2012;30:3603–9.
Giesen A, Gniel G, Malerczyk C. 30 years of rabies vaccination with Rabipur: a summary of clinical data and global experience. Expert Rev Vaccines. 2015;14:351–67.
Ma B, He LF, Zhang YL, Chen M, Wang LL, Yang HW, et al. Characteristics and viral propagation properties of a new diploid cell line, Walwax-2, and its suitability as a candidate cell substrate for vaccine production. Hum Vaccines Immunother. 2015;11:998–1009.
Jacobs JP, Jones CM, Baille JP. Characteristics of a human diploid cell designated MRC-5. Nature. 1970;227:168–70.
Hayflick L. History of cell substrates used for human biologicals. Dev Biol Stand. 1989;70:11–26.
Kissling RE, Reese DR. Anti-rabies vaccine of tissue culture origin. J Immunol. 1963;91:362–8.
Wiktor TJ, Fernandes MV, Koprowski H. Cultivation of rabies virus in human diploid cell strain WI-38. J Immunol. 1964;93:353–66.
Nicholson KG. Rabies vaccines. In: Zuckerman AJ, editor. Recent developments in prophylactic immunization, vol. 12. Lankaster: Kluwer; 1989. p. 114–54.
Guo SH, Tao H, Ying ZF. Study on safety and immunogenicity of oral poliomyelitis attenuated live vaccine (human diploid cell). Zhongguo Yi Miao He Mian Yi. 2010;16:193–6.
Wiktor TJ, Koprowski H. Successful immunization of primates with rabies vaccine prepared in human diploid cell strain WI-38. Proc Soc Exp Biol Med. 1965;118:1069–73.
Wiktor TJ, Plotkin SA, Grella DW. Human cell culture rabies vaccine. Antibody response in man. JAMA. 1973;224:1170–1.
Kuwert EK, Marcus I, Werner J, Scheiermann N, Höher PG, Thraenhart O, et al. Post-exposure use of human diploid cell culture rabies vaccine. Dev Biol Stand. 1976;37:273–86.
Bahmanyar M, Fayaz A, Nour-Salehi S, Mohammadi M, Koprowski H. Successful protection of humans exposed to rabies infection. Postexposure treatment with the new human diploid cell rabies vaccine and antirabies serum. JAMA. 1976;236:2751–4.
Plotkin SA, Wiktor TJ, Koprowski H, Rosanoff EI, Tint H. Immunization schedules for the new human diploid cell vaccine against rabies. Am J Epidemiol. 1976;103:75–80.
Wiktor TJ, Plotkin SA, Koprowski H. Development and clinical trials of the new human rabies vaccine of tissue culture (human diploid cell) origin. Dev Biol Stand. 1978;40:3–9.
Plotkin SA, Wiktor T. Vaccination of children with human cell culture rabies vaccine. Pediatrics. 1979;63:219–21.
Cox JH, Schneider LG. Prophylactic immunization of humans against rabies by intradermal inoculation of human diploid cell culture vaccine. J Clin Microbiol. 1976;3:96–101.
Cox JH, Klietmann W, Schneider LG. Human rabies immunoprophylaxis using HDC (MRC-5) vaccine. Dev Biol Stand. 1978;40:105–8.
Klietmann W, Domres B, Cox JH. Rabies post-exposure treatment and side-effects in man using HDC (MRC 5) vaccine. Dev Biol Stand. 1978;40:109–13.
Kuwert EK, Thraenhart O, Marcus I, Werner J, Atanasiu P, Bahmanyar M, et al. Comparative study on antibody determination by different methods in sera of persons vaccinated with HDCS rabies vaccine. Dev Biol Stand. 1978;40:221–9.
Nicholson KG, Turner GS. Studies with human diploid cell strain rabies vaccine and human antirabies immunoglobulin in man. Dev Biol Stand. 1978;40:115–20.
Hicks DJ, Fooks AR, Johnson N. Developments in rabies vaccines. Clin Exp Immunol. 2012;169:199–204.
Fayaz A, Simani S, Janani A, Farahtaj F, Biglari P, Howeizi N, et al. Antibody persistence, 32 years after post-exposure prophylaxis with human diploid cell rabies vaccine (HDCV). Vaccine. 2011;29:3742–5.
Horaud F. Absence of viral sequences in the WHO-Vero Cell Bank. A collaborative study. Dev Biol Stand. 1992;76:43–6.
Levenbook IS, Petricciani JC, Elisberg BL. Tumorigenicity of Vero cells. J Biol Stand. 1984;12:391–8.
Furesz J, Fanok A, Contreras G, Becker B. Tumorigenicity testing of various cell substrates for production of biologicals. Dev Biol Stand. 1989;70:233–43.
Vincent-Falquet JC, Peyron L, Souvras M, Moulin JC, Tektoff J, Patet J. Qualification of working cell banks for the Vero cell line to produce licensed human vaccines. Dev Biol Stand. 1989;70:153–6.
Osada N, Kohara A, Yamaji T, Hirayama N, Kasai F, Sekizuka T, et al. The genome landscape of the African green monkey kidney-derived vero cell line. DNA Res. 2014;21:673–83.
Ohara H. Cytogenetic examination of VERO cells derived from the present stock. In: Simizu B, Terasima T, editors. VERO cells: origin, properties and biomedical applications. Chiba: Department of Microbiology School of Medicine Chiba University; 1988. p. 36–8.
Toovey S. Preventing rabies with the Verorab vaccine: 1985–2005 Twenty years of clinical experience. Travel Med Infect Dis. 2007;5:327–48.
WHO expert consultation on rabies. First report 931, WHO technical report series 13-7-2005. Geneva: WHO; 2005. p. 1–121.
Sabchareon A, Chantavanich P, Pasuralertsakul S, Pojjaroen-Anant C, Prarinyanupharb V, Attanath P, et al. Persistence of antibodies in children after intradermal or intramuscular administration of preexposure primary and booster immunizations with purified Vero cell rabies vaccine. Pediatr Infect Dis J. 1998;17:1001–7.
Strady A, Lang J, Lienard M, Blondeau C, Jaussaud R, Plotkin SA. Antibody persistence following preexposure regimens of cell-culture rabies vaccines: 10-year follow-up and proposal for a new booster policy. J Infect Dis. 1998;177:1290–5.
Lang J, Cetre JC, Picot N, Lanta M, Briantais P, Vital S, et al. Immunogenicity and safety in adults of a new chromatographically purified Vero-cell rabies vaccine (CPRV): a randomized, double-blind trial with purified Vero-cell rabies vaccine (PVRV). Biologicals. 1998;26:299–308.
Rourou S, Ben Ayed Y, Trabelsi K, Majoul S, Kallel H. An animal component free medium that promotes the growth of various animal cell lines for the production of viral vaccines. Vaccine. 2014;32:2767–9.
Li R, Huang L, Li J, Mo Z, He B, Wang Y, et al. A next-generation, serum-free, highly purified Vero cell rabies vaccine is safe and as immunogenic as the reference vaccine Verorab® when administered according to a post-exposure regimen in healthy children and adults in China. Vaccine. 2013;31:5940–7.
Jackson AC, editor. Rabies. 3rd ed. New York: Academic; 2013.
Rupprecht CE, Plotkin SA. Rabies vaccines. In: Plotkin SA, Orenstein WA, Offit PA, editors. Vaccines. 6th ed. Philadelphia: Elsevier Saunders; 2013. p. 636–68.
WHO expert consultation on rabies. First report 982, WHO technical report series, Second report. Geneva: WHO; 2013. p. 1–139.
WHO. Rabies vaccines: WHO position paper. Wkly Epidemiol Rec. 2010;32:309–20.
Höper D, Freuling CM, Müller T, Hanke D, von Messling V, Duchowc K, et al. High definition viral vaccine strain identity and stability testing using full-genome population data—the next generation of vaccine quality control. Vaccine. 2015;33:5829–37.
Shi LT, Yu YX, Liu JH, Tang JR, Wu XH, Cao SC, et al. Analysis of full-length gene sequence of a rabies vaccine strain CTN-1 for human use in China. Chinese J Virol. 2010;26:195–201.
Rupprecht CE, Barrett J, Briggs D, Cliquet F, Fooks AR, Lumlertdacha B, et al. Can rabies be eradicated? Dev Biol (Basel). 2008;131:95–121.
Aubrit F, Perugi F, Leon A, Guehenneux F, Champion-Arnaud P, Lahmar M, et al. Cell substrates for the production of viral vaccines. Vaccine. 2015;33:5905–12.
Altaras NE, Aunins JG, Evans RK, Kamen A, Konz JO, Wolf J. Production and formulation of adenovirus vectors. Biochem Eng Biotechnol. 2005;199:193–260.
Nestola P, Peixoto C, Silva RR, Alves PM, Mota JP, Carrondo MJ. Improved virus purification processes for vaccines and gene therapy. Biotechnol Bioeng. 2015;112:843–57.
Andreadis ST, Roth CM, Le Doux JM, Morgan JR, Yarmush ML. Large-scale processing of recombinant retroviruses for gene therapy. Biotechnol Prog. 1999;15:1–11.
Braas G, Searle PF, Slater NK, Lyddiatt A. Strategies for the isolation and purification of retroviral vectors for gene therapy. Bioseparation. 1996;6:211–28.
Kulkarni PS, Sahai A, Gunale B, Dhere RM. Development of a new purified vero cell rabies vaccine (Rabivax-S) at the Serum Institute of India Pvt Ltd. Expert Rev Vaccines. 2017;16:303–11.
Kumru OS, Joshi SB, Smith DE, Middaugh CR, Prusik T, Volkin DB. Vaccine instability in the cold chain: mechanisms, analysis and formulation strategies. Biologicals. 2014;45:237–59.
Verma R, Khanna P, Prinja S, Rajput M. Intra-dermal administration of rabies vaccines in developing countries: at an affordable cost. Hum Vaccin. 2011;7:792–4.
Fooks AR, Banyard AC, Horton DL, Johnson N, McElhinney LM, Jackson AC. Current status of rabies and prospects for elimination. Lancet. 2014;384:1389–99.
Fooks AR, Brookes SM, Johnson N, McElhinney LM, Hutson AM. European bat lyssaviruses: an emerging zoonosis. Epidemiol Infect. 2003;131:1029–39.
Hanna JN, Carney IK, Smith GA, Tannenberg AE, Deverill JE, Botha JA, et al. Australian bat lyssavirus infection: a second human case, with a long incubation period. Med J Aust. 2000;172:597–9.
vanThiel P-PAM, de Bie RM, Eftimov F, Tepaske R, Zaaijer HL, et al. Fatal human rabies due to Duvenhage virus from a bat in Kenya: failure of treatment with coma-induction, ketamine, and antiviral drugs. PLoS Negl Trop Dis. 2009;3:e428.
Leonova GN, Belikov S, Kondratov IG, Krylova NV, Pavlenko EV, Romanova EV, et al. A fatal case of bat lyssavirus infection in Primorye Territory of the Russian Far East. Rabies Bull Europe. 2009;33:5–8.
Familusi JB, Osunkoya BO, Moore DL, Kemp GE. Fabiyi A. A fatal human infection with Mokola virus. Am J Trop Med Hyg. 1972;21:959–63.
Johnson N, Vos A, Freuling C, Tordo N, Fooks AR, Muller T. Human rabies due to lyssavirus infection of bat origin. Vet Microbiol. 2010;142:151–9.
Bourhy H, Kissi B, Lafon M, Sacramento D, Tordo N. Antigenic and molecular characterization of bat rabies virus in Europe. J Clin Microbiol. 1992;30:2419–26.
Larghi OP. Diaz AM. Cross protection of mice against different rabies virus isolates. ZentralblBakteriolMikrobiolHyg A. 1985;259:268–74.
Fooks A. The challenge of new and emerging lyssaviruses. Expert Rev Vaccines. 2004;3:333–6.
Nel LH. Vaccines for lyssaviruses other than rabies. Expert Rev Vaccines. 2005;4:533–40.
Malerczyk C, Freuling C, Gniel D, Giesen A, Selhorst T, Müller T. Cross-neutralization of antibodies induced by vaccination with Purified Chick Embryo Cell Vaccine (PCECV) against different Lyssavirus species. Hum Vaccin Immunother. 2014;10:2799–804.
Evans JS, Horton DL, Easton AJ, Fooks AR, Banyard AC. Rabies virus vaccines: is there a need for a pan-lyssavirus vaccine? Vaccine. 2012;30:7447–54.
Chabaud-Riou M, Moreno N, Guinchard F, Nicolai MC, Niogret-Siohan E, Seve N, et al. G-protein based ELISA as a potency test for rabies vaccines. Biologicals. 2017;46:124–9.
Servat A, Kempff S, Brogat V, Litaize E, Schereffer JL, Cliquet F. A step forward in the quality control testing of inactivated rabies vaccines—extensive evaluation of European vaccines by using alternative methods to the in vivo potency tests. Altern Lab Anim. 2015;43:19–27.
Hattwick MA, Rubin RH, Music S, Sikes RK, Smith JS, Gregg MB. Postexposure rabies prophylaxis with human rabies immune globulin. JAMA. 1974;227:407–10.
Dietzschold B. Antibody-mediated clearance of viruses from the mammalian central nervous system. Trends Microbiol. 1993;1:63–6.
World Health Organization. Rabies. Fact sheet. http://www.who.int/mediacentre/factsheets/fs099/en/. Accessed 29 Oct 2017.
Sadeghi M, Moallem SA, Yousefi-Abdolmaleki E, Montazeri M. The rabies early death phenomenon: a report of ineffective administration of rabies vaccine during symptomatic disease. Indian J Crit Care Med. 2015;19:422–4.
Morimoto K, Khawplod P, Sato Y, Virojanapirom P, Hemachudha T. Rabies vaccination at a virus-inoculated site as an alternative option to rabies immunoglobulin. Arch Virol. 2016;161:2537–41.
Casadevall A. Passive antibody administration (immediate immunity) as a specific defence against biological weapons. Emerg Infect Dis. 2002;8:833–41.
Joob S. Rabies vaccination in special scenarios: a review. Adv Trop Med Pub Health Int. 2013;3:1–4.
Thisyakorn U, Pancharoen C, Wilde H. Immunologic and virologic evaluation of HIV-1 infected children after rabies vaccination. Vaccine. 2001;19(11–12):1534–7.
Pancharoen C, Thisyakorn U, Tantawichien T, Jaijaroensup W, Khawplod P, Wilde H. Failure of pre- and postexposure rabies vaccinations in a child infected with HIV. Scand J Infect Dis. 2001;33:390–1.
Sudarshan MK, Madhusudana SN, Mahendra BJ. Post-exposure prophylaxis with purified vero cell rabies vaccine during pregnancy-safety and immunogenicity. J Commun Dis. 1999;31:229–36.
Moore SE, Goldblatt D, Bates CJ, Prentice AM. Impact of nutritional status on antibody responses to different vaccines in undernourished Gambian children. Acta Paediatr. 2003;92:170–6.
Sampath G, Reddy SV, Rao ML, Rao YU, Palaniappan C. An immunogenicity study of a newly introduced purified Vero cell rabies vaccine (Abhayrab) manufactured in India. Vaccine. 2005;23:897–900.
Korver K, Boeschoten EW, Krediet RT, van Steenis G, Schellekens PT. Dose-response effects in immunizations with keyhole limpet haemocyanin and rabies vaccine: shift in some immunodeficiency states. Clin Exp Immunol. 1987;70:328–35.
Chung EH. Vaccine allergies. Clin Exp Vaccine Res. 2014;3:50–7.
Wood RA, Berger M, Dreskin SC, Setse R, Engler RJ, Dekker CL, et al. An algorithm for treatment of patients with hypersensitivity reactions after vaccines. Pediatrics. 2008;122:e771–7.
Wiedermann-Schmidt U, Maurer W. Hilfs- und Zusatzstoffe von ImpfstoffenMedizinischeRelevanz. Wiener KlinischeWochenschrift. 2005;117:510.
Abbas AK, Lichtman AH, Pober J. Disease caused by immune response: hypersensitivity and autoimmunity. In: Cellular and molecular immunology. Philadelphia: Saunders; 2000. p. 404–15.
Plotkin SA, Orenstein WA, Offit PA. Rabies vaccines. In: Vaccines. 5th ed. Philadelphia: Elsevier, Saunders; 2008. p. 687–714.
World Health Organisation. Recommendations for inactivated rabies vaccine for human use produced in cell substrates and embryonated eggs. Expert Consultation on Rabies World Health Organ Tech Rep Ser. Geneva: World Health Organisation; 2007. p. 83–132.
European Medicines Agency. Guidelines on the warning on transmissible agents in summary of product characteristics (SmPCs) and package leaflets for plasma-derived medicinal products. London: European Medicine Agency; 2011.
World Health Organisation. Requirements for the use of animal cells as in vitro substrates for the production of biologicals. Expert Consultation on Rabies World Health Organ Tech Rep Ser. Geneva: World Health Organisation; 1998. p. 19–56.
Mark C. Large variations in the ovalbumin content in six European influenza vaccines. Pharm Sci Notes. 2006;2006:27–9.
Anderson MC, Baer H, Frazier DJ, Quinnan GV. The role of specific IgE and betapropiolactone in reactions resulting from booster doses of human diploid cell rabies vaccine. J Allergy Clin Immunol. 1987;80:861–8.
Swanson MC, Rosanoff E, Gurwith M, et al. IgE and IgG antibodies to- propiolactone and human serum albumin associated with urticarial reactions to rabies vaccine. J Infect Dis. 1987;155:909–13.
Fishbein DB, Yenne KM, Dreesen DW, Teplis CF, Mehta N, Briggs DJ. Risk factors for systemic hypersensitivity reactions after booster vaccinations with human diploid cell rabies vaccine: a nationwide prospective study. Vaccine. 1993;11:1390–4.
Dreesen DW, Bernard KW, Parker RA, Deutsch AJ, Brown J. Immune complex-like disease in 23 persons following a booster dose of rabies human diploid cell vaccine. Vaccine. 1986;4:45–9.
Marth E, Kleinhappl B. Albumin is a necessary stabilizer of TBE-vaccine to avoid fever in children after vaccination. Vaccine. 2001;20:532–7.
Arora A, Moeller L, Froeschle J. Safety and immunogenicity of a new chromatographically purified rabies vaccine in comparison to the human diploid cell vaccine. J Travel Med. 2004;11:195–9.
Briggs DJ, Dreesen DW, Morgan P, Chin JE, Seedle CD, Cryz L, et al. Safety and immunogenicity of Lyssavac Berna human diploid cell rabies vaccine in healthy adults. Vaccine. 1996;14:1361–5.
Fishbein DB, Dreesen DW, Holmes DF, Pacer RE, Ley AB, Yager PA, et al. Human diploid cell rabies vaccine purified by zonal centrifugation: a controlled study of antibody response and side effects following primary and booster pre-exposure immunizations. Vaccine. 1989;7:437–42.
Dobardzic A, Izurieta H, Woo EJ, Iskander J, Shadomy S, Rupprecht C, et al. Safety review of the purified chick embryo cell rabies vaccine: data from the Vaccine Adverse Event Reporting System (VAERS), 1997–2005. Vaccine. 2007;25:4244–51.
Moylett EH, Hanson IC. Mechanistic actions of the risks and adverse events associated with vaccine administration. J Allergy Clin Immunol. 2004;114:1010–20.
Sakaguchi M, Nakayama T, Inouye S. Food allergy to gelatin in children with systemic immediate-type reactions, including anaphylaxis, to vaccines. J Allergy Clin Immunol. 1996;98:1058–61.
Gupta M, Sindher S, Saltzman R, Heimall J. Evaluation and safe administration of rabies vaccine to a child presumably allergic to the gelatin content of the PCECV RabAvert. J Allergy Clin Immunol Pract. 2014;3:281–2.
Chernin LR, Swender D, Hostoffer RW. Cracking the shell on egg-hypersensitive patients and egg containing vaccines. J Am Osteopath Assoc. 2011;111:S5–7.
Peng J, Lu S, Zhu Z, Zhang M, Hu Q, Fang Y. Safety comparison of four types of rabies vaccines in patients with WHO category II animal exposure an observation based on different age groups. Medicine. 2016;95:47–51.
Gallegos Gallegos RM, Espinosa Larios EL, Ramos RamÃrez L, KretschmerSchmid R, Aguilar Setién A. Rabies veterinary virus vaccine produced in BHK-21 cells grown on microcarriers in a bioreactor. Arch Med Res. 1995;26:59–63.
Rajendran R, Lingala R, Vuppu S, Bandi BO, Manickam E, Macherla SR, et al. Assessment of packed bed bioreactor systems in the production of viral vaccines. AMB Express. 2014;4:25.
Mendonça RZ, Ioshimoto LM, Mendonça RM, De-Franco M, Valentini EJ, Beçak W, et al. Preparation of human rabies vaccine in VERO cell culture using a microcarrier system. Braz J Med Biol Res. 1993;26:1305–17.
Kallel H, Rourou S, Majoul S, Loukil H. A novel process for the production of a veterinary rabies vaccine in BHK-21 cells grown on microcarriers in a 20-l bioreactor. Appl Microbiol Biotechnol. 2003;61:441–6.
Moro PL, Woo EJ, Paul W, Lewis P, Petersen BW, Cano M. Post-Marketing Surveillance of Human Rabies Diploid Cell Vaccine (Imovax) in the Vaccine Adverse Event Reporting System (VAERS) in the United States, 1990–2015. PLoS Negl Trop Dis. 2016;10:e0004846.
Ramezankhani R, Shirzadi MS, Ramezankhani A, Mozafary JP. A comparative study on the adverse reactions of purified chick embryo cell vaccine (PCECV) and purified vero cell rabies vaccine (PVRV). Arch Iran Med. 2016;19:502–7.
Baer GM. Oral rabies vaccination: an overview. Rev Infect Dis. 1988;10:S644–8.
Nyberg M, Kulonen K, Neuvonen E, Ek-Kommonen C, Nuorgam M, Westerling B. An epidemic of sylvatic rabies in Finland—descriptive epidemiology and results of oral vaccination. Acta Vet Scand. 1992;33:43–57.
Faber M, Li J, Kean RB, Hooper DC, Alugupalli KR, Dietzschold B. Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc Natl Acad Sci U S A. 2009;106:11300–5.
Steck F, Wandeler A, Bichsel P, Capt S, Hafliger U, Schneider L. Oral immunization of foxes against rabies. Laboratory and field studies. Comp Immunol Microbiol Infect Dis. 1982;5:165–71.
Rupprecht CE, Wiktor TJ, Johnston DH, Hamir AN, Dietzschold B, Wunner WH, et al. Oral immunization and protection of raccoons (Procyon lotor) with a vaccinia-rabies glycoprotein recombinant virus vaccine. Proc Natl Acad Sci U S A Biol Sci. 1986;83:7947–50.
Rupprecht CE, Dietzschold B, Cox JH, Schneider LG. Oral vaccination of raccoons (procyon-lotor) with an attenuated (Sad-B19) rabies virus-vaccine. J Wildl Dis. 1989;25:548–54.
Meehan SK. Rabies epizootic in coyotes combated with oral vaccination program. J Am Vet Med Assoc. 1995;206:1097–9.
Fearneyhough MG, Wilson PJ, Clark KA, Smith DR, Johnston DH, Bradley N, et al. Results of an oral rabies vaccination program for coyotes. J Am Vet Med Assoc. 1998;212(4):498–502.
Rosatte RC, Power MJ, MacInnes CD, Campbell JB. Trap-vaccinate-release and oral vaccination for rabies control in urban skunks, raccoons and foxes. J Wildl Dis. 1992;28:562–71.
Blanton JD, Meadows A, Murphy S, Manangan JS, Hanlon CA, Faber ML, et al. Vaccination of small asian mongoose (herpestesjavanicus) against rabies. J Wildl Dis. 2006;42:663–6.
Vos A, Kretzschmar A, Ortmann S, Lojkic I, Habla C, Muller T, et al. Oral vaccination of captive small Indian mongoose (Herpestes auropunctatus) against rabies. J Wildl Dis. 2013;49:1033–6.
Haddad N, Khelifa RB, Matter H, Kharmachi H, Aubert MFA, Wandeler A, et al. Assay of oral vaccination of dogs against rabies in Tunisia with the vaccinal strain Sad(Bern). Vaccine. 1994;12:307–9.
Aylan O, Vos A. Efficacy studies with SAD B19 in Turkish dogs. J ETLIK Veterin Microbiol. 1998;9:93–102.
Rupprecht CE, Hanlon CA, Blanton JD, Manangan JS, Morrill P, Murphy S, et al. Oral vaccination of dogs with recombinant rabies virus vaccines. Virus Res. 2005;111:101–5.
Cliquet F, Aubert M. Elimination of terrestrial rabies in Western European countries. Dev Biol (Basel). 2004;119:185–204.
Cliquet F, Picard-Meyer E, Robardet E. Rabies in Europe: what are the risks? Expert Rev Anti Infect Ther. 2014;12:905–8.
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.
Borg, T. Commission implementing decision of 29 November 2013 approving annual and mutiannual 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 2014 and the following years. Off J Eur Union. 2013:101–10.
Fry T, Van Dalen K, Hurley J, Nash P. Mucosal adjuvants to improve wildlife rabies vaccination. J Wildl Dis. 2012;48:1042–6.
Sillero-Zubiri C, Marino J, Gordon CH, Bedin E, Hussein A, Regassa F, et al. Feasibility and efficacy of oral rabies vaccine SAG2 in endangered Ethiopian wolves. Vaccine. 2016;34:4792–8.
Brown LJ, Rosatte RC, Fehlner-Gardiner C, Ellison JA, Jackson FR, Bachmann P, et al. Oral vaccination and protection of striped skunks (Mephitis mephitis) against rabies using ONRAB(R). Vaccine. 2014;32:3675–9.
McCoy K, Tatsis N, Korioth-Schmitz B, Lasaro MO, Hensley SE, Lin SW, et al. Effect of preexisting immunity to adenovirus human serotype 5 antigens on the immune responses of nonhuman primates to vaccine regimens based on human- or chimpanzee-derived adenovirus vectors. J Virol. 2007;81:6594–604.
Choi J, Yang DK, Kim HH, Jo HY, Choi SS, Kim JT, et al. Application of recombinant adenoviruses expressing glycoprotein or nucleoprotein of rabies virus to Korean raccoon dogs. Clin Exp Vaccine Res. 2015;4:189–94.
Cliquet F, Picard-Meyer E, Mojzis M, Dirbakova Z, Muizniece Z, Jaceviciene I, et al. In-depth characterization of live vaccines used in Europe for oral rabies vaccination of wildlife. PLOS One. 2015;10:e01041537.
Coleman PG, Dye C. Immunization coverage required to prevent outbreaks of dog rabies. Vaccine. 1996;14:185–6.
Zinsstag J, Dürr S, Penny MA, Mindekem R, Roth F, Menendez Gonzalez S, et al. Transmission dynamics and economics of rabies control in dogs and humans in an African city. Proc Natl Acad Sci U S A. 2009;106:14996–5001.
Davlin SL, Vonville HM. Canine rabies vaccination and domestic dog population characteristics in the developing world: a systematic review. Vaccine. 2012;30:3492–502.
Darkaoui S, Boué F, Demerson JM, FassiFihri O, Yahia KI, Cliquet F. First trials of oral vaccination with rabies SAG2 dog baits in Morocco. Clin Exp Vaccine Res. 2014;3:220–6.
Zhou M, Wang L, Zhou S, Wang Z, Ruan J, Tang L, et al. Recombinant rabies virus expressing dog GM-CSF is an efficacious oral rabies vaccines for dogs. Oncotarget. 2016;6:38504–16.
Yang DK, Kim HH, Choi SS, Lee SH, Cho IS. A recombinant rabies virus (ERAGS) for use in a bait vaccine for swine. Clin Exp Vaccine Res. 2016;5:169–74.
Schnell MJ, Mebatsion T, Conzelmann KK. Infectious rabies viruses from cloned cDNA. EMBO J. 1994;13:4195–203.
Cliquet F, Freuling C, Smreczak M, van der Poel WHM, Horton D, Fooks AR, et al. Development of harmonised schemes for monitoring and reporting of rabies in animals in the European Union. EFSA Sci Rep. 2010:60.
OIE. Rabies. In: Manual of diagnostic tests and vaccines for terrestrial animals (mammals, birds and bees), Online Version. OIE; 2013.
Cliquet F, Sagné L, Schereffer JL, Aubert MF. ELISA test for rabies antibody titration in orally vaccinated foxes sampled in the fields. Vaccine. 2000;18:3272–9.
Yakobson B, Goga I, Freuling CM, Fooks AR, Gjinovci V, Hulaj B, et al. Implementation and monitoring of oral rabies vaccination of foxes in Kosovo between 2010 and 2013-an international and intersectorial effort. Int J Med Microbiol. 2014;304:902–10.
Zienius D, Pridotkas G, Jaceviciene I, Ruzauskas M. The field efficiency of oral rabies vaccination in the Lithuanian red fox population from 2006 to 2013. Vet Med. 2014;59:299–306.
Bedekovic T, Simic I, Kresic N, Lojkic I, Mihaljevic Z, Sucec I, et al. Evaluation of ELISA for the detection of rabies virus antibodies from the thoracic liquid and muscle extract samples in the monitoring of fox oral vaccination campaigns. BMC Vet Res. 2016;12:76–82.
Bedekovic T, Lemo N, Lojkic I, Mihaljevic Z, Jungic A, Cvetnic Z, et al. Modification of the fluorescent antibody virus neutralisation test-elimination of the cytotoxic effect for the detection of rabies virus neutralising antibodies. J Virol Methods. 2013;189:204–8.
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Nagarajan, T., Rupprecht, C.E. (2020). History of Rabies and Rabies Vaccines. In: Ertl, H. (eds) Rabies and Rabies Vaccines. Springer, Cham. https://doi.org/10.1007/978-3-030-21084-7_2
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