Rabies vaccines: where do we stand, where are we heading?

References

• Fishbein DB , Robinson LE . Rabies. N Engl J Med 1993;329(22):1632-8
   PubMed Web of Science ®Google Scholar
• Francki RIB , Fauquet CM , Knudson DL , Brown F . Classification and nomenclature of viruses: fifth report of international committee on taxonomy of viruses. Arch Virol. 1991. 2(Suppl):1-450
   Google Scholar
• WHO Expert Consultation on Rabies. Second Report. WHO Technical Report Series 982. World Health Organization; Geneva, Switzerland: 2013
   Google Scholar
• Fooks AR , Banyard AC , Horton DL , et al. Current status of rabies and prospects for elimination. Lancet 2014. [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Consales CA , Bolzan VL . Rabies review: immunopathology, clinical aspects and treatment. J. Venom. Anim. Toxins Incl. Trop. Dis 2007;13(1):5-38
   Google Scholar
• Menezes R . Rabies in India. CMAJ 2008;178(5):564-6
   PubMed Web of Science ®Google Scholar
• WHO . Information sheet. Observed rate of vaccine reactions. Rabies vaccine. World Health Organization; Geneva, Switzerland: 2012
   Google Scholar
• McGettigan JP . Experimental rabies vaccines for humans. Expert Rev Vaccines 2010;9(10):1177-86
   PubMed Web of Science ®Google Scholar
• Wunner WH , Larson JK , Dietzschold B , Smith CL . The molecular biology of rabies viruses. Rev Infect Dis 1988;10(Suppl 4):S771-84
   PubMedGoogle Scholar
• Mebatsion T , Weiland F , Conzelmann KK . Matrix protein of rabies virus is responsible for the assembly and budding of bullet-shaped particles and interacts with the transmembrane spike glycoprotein G. J Virol 1999;73(1):242-50
   PubMed Web of Science ®Google Scholar
• Cox JH , Dietzschold B , Schneider LG . Rabies virus glycoprotein. II. Biological and serological characterization. Infect Immun 1977;16(3):754-9
   PubMed Web of Science ®Google Scholar
• Macfarlan RI , Dietzschold B , Koprowski H . Stimulation of cytotoxic T-lymphocyte responses by rabies virus glycoprotein and identification of an immunodominant domain. Mol Immunol 1986;23(7):733-41
   PubMed Web of Science ®Google Scholar
• Celis E , Karr RW , Dietzschold B , et al. Genetic restriction and fine specificity of human T cell clones reactive with rabies virus. J Immunol 1988;141(8):2721-8
   PubMed Web of Science ®Google Scholar
• Hoff G , M S. Rabies and Animal Bite investigation. Missouri Health Department, Kansas City, Kansas. 2005
   Google Scholar
• Blanton JD , Palmer D , Rupprecht CE . Rabies surveillance in the United States during 2009. J Am Vet Med Assoc 2010;237(6):646-57
   PubMed Web of Science ®Google Scholar
• Epidemiology and burden of disease. Available from: http://www.who.int/rabies/epidemiology/en/
   Google Scholar
• Rupprecht CE . Use of a Reduced (4-Dose) Vaccine Schedule for Postexposure Prophylaxis to Prevent Human Rabies Recommendations of the Advisory Committee on Immunization Practices. MMWR 2010;59(RR02):1-9
   PubMedGoogle Scholar
• Current WHO guide for rabies pre and post-exposure treatment in humans. Available from: www.who.int/rabies/en/WHO_guide_rabies_pre_post_exp_treat_humans.pdf
   Google Scholar
• Warrell MJ , Riddell A , Yu L-M , et al. A simplified 4-site economical intradermal post-exposure rabies vaccine regimen: a randomised controlled comparison with standard methods. PLoS Negl Trop Dis 2008;2(4):e224
   PubMed Web of Science ®Google Scholar
• WHO . Available from: www.who.int/wer(Weekly Epidemiological record, no. 32, 6 august 2010)
   Google Scholar
• Gogtay N , Thatte U , Kshirsagar N , et al. Safety and pharmacokinetics of a human monoclonal antibody to rabies virus: a randomized, dose-escalation phase 1 study in adults. Vaccine 2012;30(50):7315-20
   PubMed Web of Science ®Google Scholar
• Bakker ABH , Python C , Kissling CJ , et al. First administration to humans of a monoclonal antibody cocktail against rabies virus: safety, tolerability, and neutralizing activity. Vaccine 2008;26(47):5922-7
   PubMed Web of Science ®Google Scholar
• Randomized Phase II Trial on Safety and Neutralizing Activity of CL184 and Rabies Vaccine Versus Human Rabies Immune Globulin (HRIG) and Rabies Vaccine in Children and Adolescents. Available from: http://clinicaltrials.gov/show/NCT00708084
   Google Scholar
• A Randomized Phase II Trial to Compare the Safety and Neutralizing Activity of CL184 in Combination With Rabies Vaccine vs. HRIG or Placebo in Combination With Rabies Vaccine in Healthy Adult Subjects. Available from: http://clinicaltrials.gov/show/NCT00656097
   Google Scholar
• Rabies Virus Neutralizing Activity and Safety of CL184, a Monoclonal Antibody Cocktail, in Simulated Rabies Post-Exposure Prophylaxis in Healthy Adults. Available from: http://clinicaltrials.gov/show/NCT01228383
   Google Scholar
• Nath A , Tyler KL . Novel approaches and challenges to treatment of central nervous system viral infections. Ann Neurol 2013;74(3):412-22
   PubMed Web of Science ®Google Scholar
• Zhang J , Ruan X , Zan J , et al. Efficient generation of monoclonal antibodies against major structural proteins of rabies virus with suckling mouse brain antigen. Monoclon. Antib. Immunodiagn. Immunother 2014;33(2):94-100
   PubMedGoogle Scholar
• Yang L , Cen J , Xue Q , et al. Identification of rabies virus mimotopes screened from a phage display peptide library with purified dog anti-rabies virus serum IgG. Virus Res 2013;174(1-2):47-51
   PubMed Web of Science ®Google Scholar
• Turki I , Hammami A , Kharmachi H , Mousli M . Engineering of a recombinant trivalent single-chain variable fragment antibody directed against rabies virus glycoprotein G with improved neutralizing potency. Mol Immunol 2014;57(2):66-73
   PubMed Web of Science ®Google Scholar
• Lee J-H , Park D-Y , Lee K-J , et al. Intracellular reprogramming of expression, glycosylation, and function of a plant-derived antiviral therapeutic monoclonal antibody. PLoS One 2013;8(8):e68772
   PubMed Web of Science ®Google Scholar
• Both L , van Dolleweerd C , Wright E , et al. Production, characterization, and antigen specificity of recombinant 62-71-3, a candidate monoclonal antibody for rabies prophylaxis in humans. FASEB J 2013;27(5):2055-65
   PubMed Web of Science ®Google Scholar
• Chakrabarti P . “Living versus dead”: the Pasteurian paradigm and imperial vaccine research. Bull Hist Med 2010;84(3):387-423
   PubMed Web of Science ®Google Scholar
• Biswas S , Reddy GS , Srinivasan VA , Rangarajan PN . Preexposure efficacy of a novel combination DNA and inactivated rabies virus vaccine. Hum Gene Ther 2001;12(15):1917-22
   PubMed Web of Science ®Google Scholar
• Mahendra BJ , Madhusudana SN , Sampath G , 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 Vaccin 2010;6(9):721-4
   Web of Science ®Google Scholar
• Dietzschold B , Hooper DC . Human diploid cell culture rabies vaccine (HDCV) and purified chick embryo cell culture rabies vaccine (PCECV) both confer protective immunity against infection with the silver-haired bat rabies virus strain (SHBRV). Vaccine 1998;16(17):1656-9
   PubMed Web of Science ®Google Scholar
• Jaiiaroensup W , Lang J , Thipkong P , et al. Safety and efficacy of purified Vero cell rabies vaccine given intramuscularly and intradermally. (Results of a prospective randomized trial). Vaccine 1998;16(16):1559-62
   PubMed Web of Science ®Google Scholar
• Estrada R , Vos A , Rc de L . Acceptability of local made baits for oral vaccination of dogs against rabies in the Philippines. BMC Infect Dis 2001;1:19
   PubMed Web of Science ®Google Scholar
• Esh JB , Cunningham JG , Wiktor TJ . Vaccine-induced rabies in four cats. J Am Vet Med Assoc 1982;180(11):1336-9
   PubMed Web of Science ®Google Scholar
• Faber M , Faber M-L , Papaneri A , et al. A single amino acid change in rabies virus glycoprotein increases virus spread and enhances virus pathogenicity. J Virol 2005;79(22):14141-8
   PubMed Web of Science ®Google Scholar
• Strady C , Andreoletti L , Baumard S , et al. Immunogenicity and booster efficacy of pre-exposure rabies vaccination. Trans R Soc Trop Med Hyg 2009;103(11):1159-64
   PubMed Web of Science ®Google Scholar
• Prevec L , Campbell JB , Christie BS , et al. A recombinant human adenovirus vaccine against rabies. J Infect Dis 1990;161(1):27-30
   PubMed Web of Science ®Google Scholar
• Yarosh OK , Wandeler AI , Graham FL , et al. Human adenovirus type 5 vectors expressing rabies glycoprotein. Vaccine 1996;14(13):1257-64
   PubMed Web of Science ®Google Scholar
• Shen CF , Lanthier S , Jacob D , et al. Process optimization and scale-up for production of rabies vaccine live adenovirus vector (AdRG1.3). Vaccine 2012;30(2):300-6
   PubMed Web of Science ®Google Scholar
• Cenna J , Hunter M , Tan GS , et al. Replication-deficient rabies virus-based vaccines are safe and immunogenic in mice and nonhuman primates. J Infect Dis 2009;200(8):1251-60
   PubMed Web of Science ®Google Scholar
• Dorfmeier CL , Lytle AG , Dunkel AL , et al. Protective vaccine-induced CD4(+) T cell-independent B cell responses against rabies infection. J Virol 2012;86(21):11533-40
   PubMed Web of Science ®Google Scholar
• Dorfmeier CL , Shen S , Tzvetkov EP , McGettigan JP . Reinvestigating the role of IgM in rabies virus postexposure vaccination. J Virol 2013;87(16):9217-22
   PubMed Web of Science ®Google Scholar
• Chen Z , Zhou M , Gao X , et al. A novel rabies vaccine based on a recombinant parainfluenza virus 5 expressing rabies virus glycoprotein. J Virol 2013;87(6):2986-93
   PubMed Web of Science ®Google Scholar
• Faber M , Li J , Kean RB , et al. Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc Natl Acad Sci USA 2009;106(27):11300-5
   PubMed Web of Science ®Google Scholar
• Schutsky K , Curtis D , Bongiorno EK , et al. Intramuscular inoculation of mice with the live-attenuated recombinant rabies virus TriGAS results in a transient infection of the draining lymph nodes and a robust, long-lasting protective immune response against rabies. J Virol 2013;87(3):1834-41
   PubMed Web of Science ®Google Scholar
• Koraka P , Bosch B-J , Cox M , et al. A recombinant rabies vaccine expressing the trimeric form of the glycoprotein confers enhanced immunogenicity and protection in outbred mice. Vaccine 2014;32(36):4644-50
   PubMed Web of Science ®Google Scholar
• Wang X , Feng N , Ge J , et al. Recombinant canine distemper virus serves as bivalent live vaccine against rabies and canine distemper. Vaccine 2012;30(34):5067-72
   PubMed Web of Science ®Google Scholar
• Wu Q , Yu F , Xu J , et al. Rabies-virus-glycoprotein-pseudotyped recombinant baculovirus vaccine confers complete protection against lethal rabies virus challenge in a mouse model. Vet Microbiol 2014;171(1-2):93-101
   PubMed Web of Science ®Google Scholar
• MERCK MANUALS . Available from: www.merckmanuals.com/vet/pharmacology/vaccines_and_immunotherapy/active_immunization.html
   Google Scholar
• Saxena M , Van TTH , Baird FJ , et al. Pre-existing immunity against vaccine vectors-friend or foe? Microbiology 2013;159(Pt 1):1-11
   PubMed Web of Science ®Google Scholar
• Daniell H . Production of biopharmaceuticals and vaccines in plants via the chloroplast genome. Biotechnol J 2006;1(10):1071-9
   PubMedGoogle Scholar
• McGarvey PB , Hammond J , Dienelt MM , et al. Expression of the rabies virus glycoprotein in transgenic tomatoes. Biotechnology 1995;13(13):1484-7
   PubMed Web of Science ®Google Scholar
• Yusibov V , Hooper DC , Spitsin S V , et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 2002;20(25-26):3155-64
   PubMed Web of Science ®Google Scholar
• Ashraf S , Singh PK , Yadav DK , et al. High level expression of surface glycoprotein of rabies virus in tobacco leaves and its immunoprotective activity in mice. J. Biotechnol 2005 119(1):1-14
   PubMed Web of Science ®Google Scholar
• Loza-Rubio E , Rojas E , Gómez L , et al. Development of an edible rabies vaccine in maize using the Vnukovo strain. Dev. Biol 2008;131:477-82
   Google Scholar
• Desmézières E , Jacob Y , Saron MF , et al. Lyssavirus glycoproteins expressing immunologically potent foreign B cell and cytotoxic T lymphocyte epitopes as prototypes for multivalent vaccines. J Gen Virol 1999;80(Pt 9):2343-51
   PubMedGoogle Scholar
• Da Cruz FW , McBride AJ , Conceição FR , et al. Expression of the B-cell and T-cell epitopes of the rabies virus nucleoprotein in Mycobacterium bovis BCG and induction of an humoral response in mice. Vaccine 2001;20(5-6):731-6
   PubMed Web of Science ®Google Scholar
• Mansfield KL , Johnson N , Fooks AR . Identification of a conserved linear epitope at the N terminus of the rabies virus glycoprotein. J Gen Virol 2004;85(Pt 11):3279-83
   PubMedGoogle Scholar
• Xiang ZQ , Spitalnik S , Tran M , et al. Vaccination with a plasmid vector carrying the rabies virus glycoprotein gene induces protective immunity against rabies virus. Virology 1994;199(1):132-40
   PubMed Web of Science ®Google Scholar
• Perrin P , Jacob Y , Aguilar-Sétien A , et al. Immunization of dogs with a DNA vaccine induces protection against rabies virus. Vaccine 1999;18(5-6):479-86
   PubMed Web of Science ®Google Scholar
• Lodmell DL , Ray NB , Parnell MJ , et al. DNA immunization protects nonhuman primates against rabies virus. Nat Med 1998;4(8):949-52
   PubMed Web of Science ®Google Scholar
• Margalith M , Vilalta A . Sustained protective rabies neutralizing antibody titers after administration of cationic lipid-formulated pDNA vaccine. Genet Vaccines Ther 2006;4:2
   PubMedGoogle Scholar
• Lodmell DL , Ray NB , Ulrich JT , Ewalt LC . DNA vaccination of mice against rabies virus: effects of the route of vaccination and the adjuvant monophosphoryl lipid A (MPL). Vaccine 2000;18(11-12):1059-66
   PubMed Web of Science ®Google Scholar
• Pinto AR , Reyes-Sandoval A , Ertl HCJ . Chemokines and TRANCE as genetic adjuvants for a DNA vaccine to rabies virus. Cell Immunol 2003;224(2):106-13
   PubMed Web of Science ®Google Scholar
• Lodmell DL , Ray NB , Ewalt LC . Gene gun particle-mediated vaccination with plasmid DNA confers protective immunity against rabies virus infection. Vaccine 1998;16(2-3):115-18
   PubMed Web of Science ®Google Scholar
• Lodmell DL , Ewalt LC . Rabies vaccination: comparison of neutralizing antibody responses after priming and boosting with different combinations of DNA, inactivated virus, or recombinant vaccinia virus vaccines. Vaccine 2000;18(22):2394-8
   PubMed Web of Science ®Google Scholar
• Lodmell DL , Parnell MJ , Bailey JR , et al. Rabies DNA vaccination of non-human primates: post-exposure studies using gene gun methodology that accelerates induction of neutralizing antibody and enhances neutralizing antibody titers. Vaccine 2002;20(17-18):2221-8
   PubMed Web of Science ®Google Scholar
• Osorio JE , Tomlinson CC , Frank RS , et al. Immunization of dogs and cats with a DNA vaccine against rabies virus. Vaccine 1999;17(9-10):1109-16
   PubMed Web of Science ®Google Scholar
• Kaur M , Rai A , Bhatnagar R . Rabies DNA vaccine: no impact of MHC class I and class II targeting sequences on immune response and protection against lethal challenge. Vaccine 2009;27(15):2128-37
   PubMed Web of Science ®Google Scholar
• Kaur M , Saxena A , Rai A , Bhatnagar R . Rabies DNA vaccine encoding lysosome-targeted glycoprotein supplemented with Emulsigen-D confers complete protection in preexposure and postexposure studies in BALB/c mice. FASEB J 2010;24(1):173-83
   PubMed Web of Science ®Google Scholar
• Tao L , Ge J , Wang X , et al. Generation of a recombinant rabies Flury LEP virus carrying an additional G gene creates an improved seed virus for inactivated vaccine production. Virol J 2011;8:454
   PubMed Web of Science ®Google Scholar
• Liu X , Yang Y , Sun Z , et al. A recombinant rabies virus encoding two copies of the glycoprotein gene confers protection in dogs against a virulent challenge. PLoS One 2014;9(2):e87105
   PubMed Web of Science ®Google Scholar
• Wenqiang J , Yin X , Lan X , et al. Development of a reverse genetics system for the aG strain of rabies virus in China. Arch Virol 2014;159(5):1033-8
   PubMed Web of Science ®Google Scholar
• Norton JE , Lytle AG , Shen S , et al. ICAM-1-based rabies virus vaccine shows increased infection and activation of primary murine B cells in vitro and enhanced antibody titers in-vivo. PLoS One 2014;9(1):e87098
   PubMed Web of Science ®Google Scholar
• Fenje P , Pinteric L . Potentiation of tissue culture rabies vaccine by adjuvants. Am J Public Health Nations Health 1966;56(12):2106-13
   PubMedGoogle Scholar
• Ullas PT , Madhusudana SN , Desai A , et al. Enhancement of immunogenicity and efficacy of a plasmid DNA rabies vaccine by nanoformulation with a fourth-generation amine-terminated poly(ether imine) dendrimer. Int J Nanomedicine 2014;9:627-34
   PubMed Web of Science ®Google Scholar
• Gupta PK , Sonwane AA , Singh NK , et al. Intracerebral delivery of small interfering RNAs (siRNAs) using adenoviral vector protects mice against lethal peripheral rabies challenge. Virus Res 2012;163(1):11-18
   PubMed Web of Science ®Google Scholar
• Wiktor TJ , Macfarlan RI , Reagan KJ , et al. Protection from rabies by a vaccinia virus recombinant containing the rabies virus glycoprotein gene. Proc Natl Acad Sci USA 1984;81(22):7194-8
   PubMed Web of Science ®Google Scholar
• Cadoz M , Strady A , Meignier B , et al. Immunisation with canarypox virus expressing rabies glycoprotein. Lancet 1992;339(8807):1429-32
   PubMed Web of Science ®Google Scholar
• Cliquet F , Gurbuxani JP , Pradhan HK , et al. The safety and efficacy of the oral rabies vaccine SAG2 in Indian stray dogs. Vaccine 2007;25(17):3409-18
   PubMed Web of Science ®Google Scholar
• Blancou J , Artois M , Brochier B , et al. Safety and efficacy of an antirabies vaccine consisting of recombinant vaccinia-rabies virus administered orally to the fox, dog and cat. Ann Rech Vet 1989;20(2):195-204
   PubMedGoogle Scholar
• World Health Organization . Sustaining the drive to overcome the global impact of neglected tropical diseases. Second WHO report on neglected tropical diseases. WHO, Geneva, Switzerland; 2013
   Google Scholar
• Cleaveland S , Fèvre EM , Kaare M , Coleman PG . Estimating human rabies mortality in the United Republic of Tanzania from dog bite injuries. Bull World Health Organ 2002;80(4):304-10
   PubMed Web of Science ®Google Scholar
• Hampson K , Dobson A , Kaare M , et al. Rabies exposures, post-exposure prophylaxis and deaths in a region of endemic canine rabies. PLoS Negl Trop. Dis 2008;2(11):e339
   PubMed Web of Science ®Google Scholar
• Mallewa M , Fooks AR , Banda D , et al. Rabies encephalitis in malaria-endemic area, Malawi, Africa. Emerg Infect Dis 2007;13(1):136-9
   PubMed Web of Science ®Google Scholar
• Schneider MC , Romijn PC , Uieda W , et al. Rabies transmitted by vampire bats to humans: an emerging zoonotic disease in Latin America? Rev Panam Salud Publica 2009;25(3):260-9
   PubMed Web of Science ®Google Scholar
• Israsena N , Mahavihakanont A , Hemachudha T . Rabies virus infection and microRNAs. Adv Virus Res 2011;79:329-44
   PubMed Web of Science ®Google Scholar
• Müller T , Dietzschold B , Ertl H , et al. Development of a mouse monoclonal antibody cocktail for post-exposure rabies prophylaxis in humans. PLoS Negl Trop Dis 2009;3(11):e542
   PubMed Web of Science ®Google Scholar
• WHO . Rabies. Available from: http://www.who.int/biologicals/vaccines/rabies/en/
   Google Scholar
• Lin F , Zeng F , Lu L , et al. The primary hamster kidney cell rabies vaccine: adaptation of viral strain, production of vaccine, and pre- and postexposure treatment. J Infect Dis 1983;147(3):467-73
   PubMed Web of Science ®Google Scholar
• Pichon S , Guinet-Morlot F , Minutello M , et al. A serum-free, purified vero cell rabies vaccine is safe and as immunogenic as the reference vaccine Verorab for pre-exposure use in healthy adults: results from a randomized controlled phase-II trial. Vaccine 2013;31(18):2295-301
   PubMed Web of Science ®Google Scholar
• Lang J , Cetre JC , Picot N , 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(4):299-308
   PubMed Web of Science ®Google Scholar
• Kulkarni PS , Sapru A , D’costa PM , et al. Safety and immunogenicity of a new purified vero cell rabies vaccine (PVRV) administered by intramuscular and intradermal routes in healthy volunteers. Vaccine 2013;31(24):2719-22
   PubMed Web of Science ®Google Scholar
• Clinical trial for rabies monoclonal antibody. Available from: www.eurekalert.org/pub_releases/2012-08/uomm-ctf080712.php
   Google Scholar
• An Open-label, Single-Arm Study to Evaluate the Safety and Rabies Virus Antibody Titers of Intramuscularly Administered Rabies Immune Globulin (Human). Available from: http://clinicaltrials.gov/show/NCT02139657
   Google Scholar
• Study of Purified Vero Rabies Vaccine and Rabies Human Diploid Cell Vaccine in a Simulated Rabies Post-exposure Regimen. Available from: http://clinicaltrials.gov/ct2/show/NCT01877395?term=rabies&rank=1
   Google Scholar
• Study of the Purified Vero Rabies Vaccine - Serum Free in Comparison With the Reference Purified Vero Rabies Vaccine. Available from: http://clinicaltrials.gov/ct2/show/NCT01339312?term=rabies&rank=4
   Google Scholar
• Safety and Immunogenicity of Two Intradermal Rabies Vaccine Regimens Administered With and Without Human Rabies Immunoglobulin in Subjects ≥ 1 Years of Age. Available from: http://clinicaltrials.gov/ct2/show/NCT02177032?term=rabies&rank=8
   Google Scholar
• A Randomized Phase II Trial to Compare the Safety and Neutralizing Activity of CL184 in Combination With Rabies Vaccine vs. HRIG or Placebo in Combination With Rabies Vaccine in Healthy Adult Subjects. Available from: http://clinicaltrials.gov/ct2/show/NCT00656097?term=rabies&rank=13
   Google Scholar
• Phase II/III Study of the Safety and Effectiveness of HRIG With Co-administration of Active Rabies Vaccine in Healthy Subjects (KAMRAB-003). Available from: http://clinicaltrials.gov/ct2/show/NCT02040090?term=rabies&rank=20
   Google Scholar