Volume 6, Issue 4 (10-2018)                   JoMMID 2018, 6(4): 77-86 | Back to browse issues page

XML Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Golahdooz M, Eybpoosh S, Bashar R, Taherizadeh M, Pourhossein B, Shirzadi M, et al . Comparison of Immune Responses following Intradermal and Intramuscular Rabies Vaccination Methods. JoMMID. 2018; 6 (4) :77-86
URL: http://jommid.pasteur.ac.ir/article-1-165-en.html
Department of Virology, Pasteur Institute of Iran, Tehran, Iran
Abstract:   (1515 Views)
Rabies is a zoonotic viral disease. The causative agent is a negative-sense RNA genome virus of the genus Lyssavirus (Family: Rhabdoviridae). The disease, commonly transmitted by rabid dogs, is the cause of mortality of over 59000 humans worldwide annually. This disease can be prevented before the development of symptoms through proper vaccination even after exposure. Hence, improvement of the vaccination schedule in the countries where rabies is endemic is essential. In addition to the type of vaccine, injection routes also contribute to enhanced immune responses and increased potency of the vaccines. The vaccines approved by the World Health Organization (WHO) include cell culture and embryonated egg-based rabies vaccines (CCEEVs). In order to develop a vaccine against rabies, it is necessary to use an appropriate delivery system to promote a proper antigen-specific immune response. Different routes of injection such as intradermal (ID), intramuscular (IM) or subcutaneous (SC) are practiced, with controversies over their suitability. In this article, we discuss the immunological aspects of rabies vaccination by comparing ID and IM delivery systems.
Full-Text [PDF 574 kb]   (460 Downloads)    
Type of Study: Review article |
Received: 2018/06/10 | Accepted: 2019/06/19 | Published: 2019/07/3

1. Madhusudana SN, Subha S, Thankappan U, Ashwin YB. Evaluation of a direct rapid immunohistochemical test (dRIT) for rapid diagnosis of rabies in animals and humans. Virologica Sinica. 2012; 27 (5): 299-302. [DOI:10.1007/s12250-012-3265-6]
2. Wilde H, Hemachudha T, Jackson AC. management of human rabies. Trans R Soc Trop Med Hyg. 2008; 102 (10): 979-82. [DOI:10.1016/j.trstmh.2008.04.008]
3. Dietzschold B, Faber M, Schnell MJ. New approaches to the prevention and eradication of rabies. Expert Rev Vaccines. 2003; 2 (3): 399-406. [DOI:10.1586/14760584.2.3.399]
4. Parmar D, Vora D, Rathod P, Narlawar U. Epidemiological profile of animal bite cases attending Anti rabies clinic and pre-treatment practices adopted by them following animal bite: A cross-sectional study. Int J Med Health Res. 2016; 2 (4): 11-3.
5. Sridhar N, Kiran BS, Rudrapal M. Management, Post-exposure Prophylaxis and Treatment of Dog Bites and Rabies Cases in a Tertiary Care Hospital. Biosci Biotech Res Asia. 2013; 10 (1):361-364 [DOI:10.13005/bbra/1135]
6. Wieten R, Tawil S, Van Vugt M, Goorhuis A, Grobusch M. Risk of rabies exposure among travellers. Neth J Med. 2015; 73: 219-26.
7. Fisher CR, Streicker DG, Schnell MJ. The spread and evolution of rabies virus: conquering new frontiers. Nat Rev Microbiol. 2018. [DOI:10.1038/nrmicro.2018.11]
8. Srithayakumar V, Sribalachandran H, Rosatte R, Nadin-Davis SA, Kyle CJ. Innate immune responses in raccoons after raccoon rabies virus infection. J Gen Virol. 2014; 95 (1): 16-25. [DOI:10.1099/vir.0.053942-0]
9. Fazeli M, Golahdouz M, Bashar R, Arab Baferani M, Doosti Irani A, Pourhossein B, et al. Design and Validation of a Persian Knowledge, Attitude, and Practice Questionnaire for Rabies (PKAP-Rabies) in the General Population of Iran. J Med Microbiol Infect Dis. 2018; 6 (2): 67-71. [DOI:10.29252/JoMMID.]
10. Organization WH. WHO expert consultation on rabies: third report. 2018.
11. Liu Y, Zhang H-P, Zhang S-F, Wang J-X, Zhou H-N, Zhang F, et al. Rabies outbreaks and vaccination in domestic camels and cattle in northwest China. PLoS Negl Trop Dis. 2016; 10 (9): e0004890. [DOI:10.1371/journal.pntd.0004890]
12. Sultanov AA, Abdrakhmanov SK, Abdybekova AM, Karatayev BS, Torgerson PR. Rabies in Kazakhstan. PLoS Negl Trop Dis. 2016; 10 (8): e0004889. [DOI:10.1371/journal.pntd.0004889]
13. Coetzer A, Kidane A, Bekele M, Hundera A, Pieracci E, Shiferaw M, et al. The SARE tool for rabies control: Current experience in Ethiopia. Antiviral Res. 2016; 135: 74-80. [DOI:10.1016/j.antiviral.2016.09.011]
14. Ponsich A, Goutard F, Sorn S, Tarantola A. A prospective study on the incidence of dog bites and management in a rural Cambodian, rabies-endemic setting. Acta tropica. 2016; 160: 62-7. [DOI:10.1016/j.actatropica.2016.04.015]
15. Dehghani R, Sharif A, Madani M, Kashani HH, Sharif MR. Factors influencing animal bites in Iran: a descriptive study. Osong Public Health Res Perspect. 2016; 7 (4): 273-7. [DOI:10.1016/j.phrp.2016.06.004]
16. Shirzadi MR. 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 (7): 502.
17. Elser JL, Bigler LL, Anderson AM, Maki JL, Lein DH, Shwiff SA. The economics of a successful raccoon rabies elimination program on Long Island, New York. PLoS Negl Trop Dis. 2016; 10 (12): e0005062. [DOI:10.1371/journal.pntd.0005062]
18. Hampson K, Dushoff J, Bingham J, Brückner G, Ali Y, Dobson A. Synchronous cycles of domestic dog rabies in sub-Saharan Africa and the impact of control efforts. P Natl Acad Sci. 2007; 104 (18): 7717-22. [DOI:10.1073/pnas.0609122104]
19. Fu Z. The rabies situation in Far East Asia. Dev Biol. 2008; 131: 55-61.
20. Picot V, Rasuli A, Abella-Rider A, Saadatian-Elahi M, Aikimbayev A, Barkia A, et al. The Middle East and Eastern Europe rabies Expert Bureau (MEEREB) third meeting: Lyon-France (7-8 April, 2015). J Infect Public Health. 2017; 10 (6): 695-701. [DOI:10.1016/j.jiph.2017.03.005]
21. Organization WH. WHO expert consultation on rabies: second report: World Health Organization; 2013.
22. Nandi S, Kumar M. Development in immunoprophylaxis against rabies for animals and humans. Avicenna J Med Biotechnol. 2010; 2 (1): 3.
23. Favi M, Yung V, Roos O, Rodriguez L, Trujillo R, Acevedo A. Immune response of suckling mouse brain (CRL) rabies vaccine and tissue culture rabies vaccine (Verorab) in pre-exposure prophylaxis in humans. Revista medica de Chile. 2004; 132 (1): 41-6. [DOI:10.4067/S0034-98872004000100006]
24. Kulkarni PS, Sapru A, D'costa PM, Pandit A, Madhusudana SN, Yajaman AB, 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. [DOI:10.1016/j.vaccine.2013.03.050]
25. Malerczyk C, Briggs DJ, Dreesen DW, Banzhoff A. Duration of immunity: an anamnestic response 14 years after rabies vaccination with purified chick embryo cell rabies vaccine. J Travel Med. 2007; 14 (1): 63-4. [DOI:10.1111/j.1708-8305.2006.00097.x]
26. Andersson C. Production and delivery of recombinant subunit vaccines: Bioteknologi; 2000.
27. Galvez-Romero G, Salas-Rojas M, Pompa-Mera EN, Chávez-Rueda K, Aguilar-Setién Á. Addition of C3d-P28 adjuvant to a rabies DNA vaccine encoding the G5 linear epitope enhances the humoral immune response and confers protection. Vaccine. 2018; 36 (2): 292-8. [DOI:10.1016/j.vaccine.2017.11.047]
28. Dietzschold B, Wang H, Rupprecht CE, Celis E, Tollis M, Ertl H, et al. Induction of protective immunity against rabies by immunization with rabies virus ribonucleoprotein. Proc Natl Acad Sci. 1987; 84 (24): 9165-9. [DOI:10.1073/pnas.84.24.9165]
29. Baer GM. The natural history of rabies: CRC press; 1991.
30. Smreczak M, Zmudzinski J. Rabies control in wildlife with oral vaccination in Poland. Bulletin-Veterinary Institute in Pulawy. 2005; 49 (3): 255.
31. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science. 2003; 300 (5625): 1524-5. [DOI:10.1126/science.1085536]
32. Wang ZW, Sarmento L, Wang Y, Li X-q, Dhingra V, Tseggai T, et al. Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol. 2005; 79 (19): 12554-65. [DOI:10.1128/JVI.79.19.12554-12565.2005]
33. Carty M, Reinert L, Paludan SR, Bowie AG. Innate antiviral signalling in the central nervous system. Trends Immunol. 2014; 35 (2): 79-87. [DOI:10.1016/j.it.2013.10.012]
34. Johnson N, Cunningham AF, Fooks AR. The immune response to rabies virus infection and vaccination. Vaccine. 2010; 28: 3896-901. [DOI:10.1016/j.vaccine.2010.03.039]
35. Nair S, Diamond MS. Innate immune interactions within the central nervous system modulate pathogenesis of viral infections. Curr Opin Immunol. 2015; 36: 47-53. [DOI:10.1016/j.coi.2015.06.011]
36. Cuervo AM, Bergamini E, Brunk UT, Dröge W, Ffrench M, Terman A. Autophagy and aging: the importance of maintaining" clean" cells. Autophagy. 2005; 1 (3): 131-40. [DOI:10.4161/auto.1.3.2017]
37. Reinke SN, Resch L, Maingat F, Branton W, Jackson AC, Holt R, et al. Metagenomic and metabolomic characterization of rabies encephalitis: new insights into the treatment of an ancient disease. J Infect Dis. 2012; 207 (9): 1451-6. [DOI:10.1093/infdis/jis479]
38. Johnson N, Cunningham AF. Interplay between rabies virus and the mammalian immune system. World J Clin Infect Dis. 2015; 5 (4): 67-76. [DOI:10.5495/wjcid.v5.i4.67]
39. Dietzschold B, Kao M, Zheng YM, et al. Delineation of putative mechanisms involved in antibody-mediated clearance of rabies virus from the central nervous system. Proc Natl Acad Sci. 1992; 89: 7252-6. [DOI:10.1073/pnas.89.15.7252]
40. Rouse BT, Sehrawat S. Immunity and immunopathology to viruses: what decides the outcome? Nat Rev Immunol. 2010; 10 (7): 514. [DOI:10.1038/nri2802]
41. mondiale de la Santé O, Organization WH. Weekly Epidemiological Record, 2018, vol. 93, 16 [Full issue]. Weekly Epidemiological Record= Relevé épidémiologique hebdomadaire. 2018; 93 (16): 201-20.
42. Khawplod P, Wilde H, Yenmuang W, Benjavongkulchai M, Chomchey P. Immune response to tissue culture rabies vaccine in subjects who had previous postexposure treatment with Semple or suckling mouse brain vaccine. Vaccine. 1996; 14 (16): 1549-52. [DOI:10.1016/S0264-410X(96)00090-4]
43. Berndtsson LT, Nyman A-KJ, Rivera E, Klingeborn B. Factors associated with the success of rabies vaccination of dogs in Sweden. Acta Vet Scand. 2011; 53 (1): 22. [DOI:10.1186/1751-0147-53-22]
44. Rodrigues F, Mandke V, Roumiantzeff M, Rao CM, Mehta J, Pavri K, et al. Persistence of rabies antibody 5 years after pre-exposure prophylaxis with human diploid cell antirabies vaccine and antibody response to a single booster dose. Epidemiol Infect. 1987; 99 (1): 91-5. [DOI:10.1017/S0950268800066899]
45. Tollis M, Dietschold B, Volia CB, Koprowski H. Immunization of monkeys with rabies ribonucleoprotein (RNP) confers protective immunity against rabies. Vaccine. 1991; 9 (2): 134-6. [DOI:10.1016/0264-410X(91)90270-G]
46. Lodmell DL, Ray NB, Parnell MJ, Ewalt LC, Hanlon CA, Shaddock JH, et al. DNA immunization protects nonhuman primates against rabies virus. Nat Med. 1998; 4 (8): 949-52. [DOI:10.1038/nm0898-949]
47. 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. [DOI:10.1016/S0264-410X(00)00005-0]
48. Lodmell DL, Parnell MJ, Weyhrich JT, Ewalt LC. Canine rabies DNA vaccination: a single-dose intradermal injection into ear pinnae elicits elevated and persistent levels of neutralizing antibody. Vaccine. 2003; 21 (25-26): 3998-4002. [DOI:10.1016/S0264-410X(03)00297-4]
49. Morris J, Crowcroft N. Pre-exposure rabies booster vaccinations: a literature review. Dev Biol. 2006; 125: 205-15.
50. Suwansrinon K, Wilde H, Benjavongkulchai M, Banjongkasaena U, Lertjarutorn S, Boonchang S, et al. Survival of neutralizing antibody in previously rabies vaccinated subjects: a prospective study showing long lasting immunity. Vaccine. 2006; 24 (18): 3878-80. [DOI:10.1016/j.vaccine.2006.02.027]
51. Lodmell DL, Ewalt LC, Parnell MJ, Rupprecht CE, Hanlon CA. One-time intradermal DNA vaccination in ear pinnae one year prior to infection protects dogs against rabies virus. Vaccine. 2006; 24 (4): 412-6. [DOI:10.1016/j.vaccine.2005.08.003]
52. Lim PL, Barkham TM. Serologic response to rabies pre-exposure vaccination in persons with potential occupational exposure in Singapore. Int J Infect Dis. 2010; 14 (6): e511-e3. [DOI:10.1016/j.ijid.2009.08.008]
53. 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 (21): 3742-5. [DOI:10.1016/j.vaccine.2011.03.048]
54. Schneider L, Cox J, Müller W, Hohnsbeen K-P. Current oral rabies vaccination in Europe: an interim balance. J Infect Dis.
55. Madhusudana SN, Mani RS. Intradermal vaccination for rabies prophylaxis: conceptualization, evolution, present status and future. Expert Rev Vaccines. 2014; 13 (5): 641-55. [DOI:10.1586/14760584.2014.901893]
56. Khawplod P, Wilde H, Chomchey P, Benjavongkulchai M, Yenmuang W, Chaiyabutr N, et al. What is an acceptable delay in rabies immune globulin administration when vaccine alone had been given previously?, Vaccine. 1996; 14 (5): 389-91. [DOI:10.1016/0264-410X(95)00213-K]
57. Mondiale de la Santé O, Organization WH. Rabies vaccines: WHO position paper-April 2018-Vaccins antirabiques: Note de synthèse de l'OMS-avril 2018. Weekly Epidemiological Record= Relevé épidémiologique hebdomadaire. 2018; 93 (16): 201-19.
58. Ravish HS, Srikanth J, Ashwath Narayana DH, Annadani R, Vijayashankar V, Undi M. Pre-exposure prophylaxis against rabies in children: safety of purified chick embryo cell rabies vaccine (Vaxirab N) when administered by intradermal route. Hum Vaccin Immunother. 2013; 9 (9): 1910-3. [DOI:10.4161/hv.25203]
59. Madhusudana S, Anand NP, Shamsundar R. Economical multi-site intradermal regimen with purified chick embryo cell vaccine (Rabipur) prevents rabies in people bitten by confirmed rabid animals. Int J Infect Dis. 2002; 6 (3): 210-4. [DOI:10.1016/S1201-9712(02)90113-X]
60. Jaiiaroensup W, Lang J, Thipkong P, Wimalaratne O, Samranwataya P, Saikasem A, 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. [DOI:10.1016/S0264-410X(98)00045-0]
61. Shin J-H, Sakoda Y, Yano S, Ochiai K, Kida H, Umemura T. Effective prevention against rabies by intracerebral immunization in mice. J Vet Med Sci. 2009; 71 (10): 1331-6. [DOI:10.1292/jvms.001331]
62. Mills DJ, Lau CL, Fearnley EJ, Weinstein P. The Immunogenicity of a Modified Intradermal Pre‐exposure Rabies Vaccination Schedule-A Case Series of 420 Travelers. J Travel Med. 2011; 18 (5): 327-32. [DOI:10.1111/j.1708-8305.2011.00540.x]
63. Sudarshan M, Madhusudana S, Mahendra B, Narayana DA, Giri MA, Muhamuda K, et al. Boosting effect of purified chick embryo cell rabies vaccine using the intradermal route in persons previously immunized by the intramuscular route or vice versa. Natl Med J India. 2006; 19 (4): 192.
64. Sunden Y, Yano S, Ishida S, Ochiai K, Umemura T. Intracerebral vaccination suppresses the spread of rabies virus in the mouse brain. Microbes Infect. 2010; 12 (14-15): 1163-9. [DOI:10.1016/j.micinf.2010.08.002]
65. Yoneda A, TuchiYA K, TAKAshimA Y, ArAKAwA T, Tsuji N, Hayashi Y, et al. Protection of mice from rabies by intranasal immunization with inactivated rabies virus. Exp Anim. 2008; 57 (1): 1-9. [DOI:10.1538/expanim.57.1]
66. Yu P, Huang Y, Zhang Y, Tang Q, Liang G. Production and evaluation of a chromatographically purified Vero cell rabies vaccine (PVRV) in China using microcarrier technology. Hu Vacc Immunotherap. 2012; 8 (9): 1230-5. [DOI:10.4161/hv.20985]
67. Liniger M, Zuniga A, Naim HY. Use of viral vectors for the development of vaccines. Expert Rev Vaccines. 2007; 6 (2): 255-66. [DOI:10.1586/14760584.6.2.255]
68. Cook IF. Evidence based route of administration of vaccines. Hum Vaccine. 2008; 4 (1): 67-73. [DOI:10.4161/hv.4.1.4747]
69. Hanna Jr M, Congdon C, Wust CJ. Effect of antigen dose on lymphatic tissue germinal center changes. Proc Soc Exp Biol Med. 1966; 121 (1): 286-90. [DOI:10.3181/00379727-121-30760]
70. Yao C, Kaplan DH. Langerhans cells transfer targeted antigen to dermal DC and acquire MHC-II in vivo. J Invest Dermatol. 2018. [DOI:10.1016/j.jid.2018.02.005]
71. Liard C, Munier S, Joulin-Giet A, Bonduelle O, Hadam S, Duffy D, et al. Intradermal immunization triggers epidermal Langerhans cell mobilization required for CD8 T-cell immune responses. J Invest Dermatol. 2012; 132 (3): 615-25. [DOI:10.1038/jid.2011.346]
72. Malissen B, Tamoutounour S, Henri S. The origins and functions of dendritic cells and macrophages in the skin. Nat Rev Immunol. 2014; 14 (6): 417. [DOI:10.1038/nri3683]
73. Engelke L, Winter G, Hook S, Engert J. Recent insights into cutaneous immunization: how to vaccinate via the skin. Vaccine. 2015; 33 (37): 4663-74. [DOI:10.1016/j.vaccine.2015.05.012]
74. Teunissen M, Haniffa M, Collin M. Insight into the immunobiology of human skin and functional specialization of skin dendritic cell subsets to innovate intradermal vaccination design. Intradermal Immunization: Springer; 2011. 25-76. [DOI:10.1007/82_2011_169]
75. Levin C, Bonduelle O, Nuttens C, Primard C, Verrier B, Boissonnas A, et al. Critical role for skin-derived migratory DCs and Langerhans cells in TFH and GC responses after intradermal immunization. J Invest Dermatol. 2017; 137 (9): 1905-13. [DOI:10.1016/j.jid.2017.04.016]
76. Schmitt D. Cutaneous immune system. Comptes Rendus des Seances de la Société de Biologie et de ses Filiales. 1994; 188 (3): 207-21.

Add your comments about this article : Your username or Email:

Send email to the article author

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.