The Development of Polio Vaccines: the Current Update (Review)
The dramatic history of the development and use of polio vaccines reflects the evolution of vaccine preparations under the influence of changing epidemiological conditions and socio-economic factors.
The invention of two polio vaccines — the inactivated Salk vaccine and the live oral vaccine from Sabin strains, each with its own advantages and disadvantages — is on the list of the most significant medical achievements of the XX century. Over the past 50 years, these vaccines were used in various modalities, schemes, and combinations. As a result, poliomyelitis has been completely eradicated in almost all countries of the world. The sustained WHO-led efforts toward full eradication of the disease are expected to result in complete cessation of the virus circulation. In this case, the poliovirus, like the smallpox virus, will remain only in laboratories. However, it would be unreasonable to stop the vaccination even after the pathogen circulation has been stopped like it was in the case with the elimination of smallpox virus. Unlike the smallpox vaccination, vaccines against poliomyelitis will not lose their relevance in the near future because these two viruses significantly differ from each other in terms of biological and epidemiological characteristics.
- Underwood M. A treatise on the diseases of children with general directions for the management of infants from the birth. London: J. Mathews; 1789.
- Badham J. Paralysis in childhood: four remarkable cases of suddenly induced paralysis in the extremities, occurring in children, without any apparent cerebral or cerebro-spinal lesion. London Med Gazzette 1834; 17: 215.
- Heine J. Beobachtungen über Lähmungszustände der unteren Extremitäten und deren Behandlung. Stuttgart: Köhler; 1840.
- Cornil V. Paralysie infantile; cancer les seins; autopsie; altérations de la moelle épinière, des nerfs et des muscles; géneéralisation du cancer. C R Soc Biol (Paris) 1863; 5: 187.
- Jacobi M. Pathogeny of infantile paralysis. Am J Obstet 1875; 7: 1.
- Putnam J.J., Taylor E.W. Is acute poliomyelitis unusually prevalent this season. Bost Med Surg J 1893; 129(21): 509–510, https://doi.org/10.1056/nejm189311231292103.
- Flexner S., Clark P.F. A note on the mode of infection in epidemic poliomyelitis. Proc Soc Exp Biol Med 1912; 10: 1–10.
- Frost W.H. Epidemiologic studies of acute anterior poliomyelitis. Hyg Lab Bull 1913; 90.
- Chumakov M.P., Voroshilova M.K., Drozdov S.G., Dzagurov S.G., Lashkevich V.A., Mironova L.L., Ralph N.M., Gagarina A.V., Ashmarina E.E., Shirman G.A., Fleer G.P., Tolskaya E.A., Sokolova I.S., Elbert L.B., Sinyak K.M. Some results of the work on mass immunization in the Soviet Union with live poliovirus vaccine prepared from Sabin strains. Bull World Health Organ 1961; 25(1): 79–91.
- Flexner S., Lewis P.A. The transmission of acute poliomyelitis to monkeys. JAMA 1909; 53(20): 1639, https://doi.org/10.1001/jama.1909.92550200027002g.
- Flexner S., Lewis P.A. Experimental poliomyelitis in monkeys. Seventh note: active immunization and passive serum protection. JAMA 1910; 54(22): 1780, https://doi.org/10.1001/jama.1910.92550480001001i.
- Bodian D., Morgan I.V., Howe H.A. Differentiation of types of poliomyelitis viruses: III. The grouping of fourteen strains into three basic immunological types. Am J Hyg 1949; 49(2): 234–245, https://doi.org/10.1093/oxfordjournals.aje.a119273.
- Burnet F.M., Macnamara J. Immunological differences between strains of poliomyelitic virus. Br J Exp Pathol 1931; 12(2): 57–61.
- Kessel J.F., Pait C.F. Differentiation of three groups of poliomyelitis virus. Proc Soc Exp Biol Med 1949; 70(2): 315–316, https://doi.org/10.3181/00379727-70-16911.
- Pallansch M.A., Oberste M.S., Whitton J.L. Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In: Knipe D.M., Howley P.M. (editors). Fields virology. Vol. 1. Philadelphia: Lippincott Williams and Wilkins; 2013; p. 490–530.
- Racaniello V.R. Picornaviridae: the viruses and their replication. In: Knipe D.M., Howley P.M. (editors). Fields virology. Vol. 1. Philadelphia: Lippincott Williams and Wilkins; 2013; p. 453–489.
- Herold J., Andino R. Poliovirus RNA replication requires genome circularization through a protein–protein bridge. Mol Cell 2001; 7(3): 581–591, https://doi.org/10.1016/s1097-2765(01)00205-2.
- Rossmann M.G., He Y., Kuhn R.J. Picornavirus–receptor interactions. Trends Microbiol 2002; 10(7): 324–331, https://doi.org/10.1016/s0966-842x(02)02383-1.
- Stanway G. Structure, function and evolution of picornavirus. J Gen Virol 1990; 71(Pt 11): 2483–2501, https://doi.org/10.1099/0022-1317-71-11-2483.
- Chang T.W., Weinstein L., Macmahon E. Paralytic poliomyelitis in a child with hypogammaglobulinemia: probable implication of type 1 vaccin strain. Pediatrics 1966; 37: 630–636.
- Feigin R.D., Guggenheim M.A., Johnson S.D. Vaccine-related paralytic poliomyelitis in an immunodeficient child. J Pediatr 1971; 79(4): 642–647, https://doi.org/10.1016/s0022-3476(71)80313-x.
- Wright P.F., Hatch M.H., Kasselberg A.G., Lowry S.P., Wadlington W.B., Karzon D.T. Vaccine-associated poliomyelitis in a child with sex-linked agammaglobulinemica. J Pediatr 1977; 91(3): 408–412, https://doi.org/10.1016/s0022-3476(77)81309-7.
- Nottay B.K., Kew O.M., Hatch M.H., Heyward J.T., Obijeski J.F. Molecular variation of type 1 vaccine-related and wild polioviruses during replication in humans. Virology 1981; 108(2): 405–423, https://doi.org/10.1016/0042-6822(81)90448-7.
- Alexander L.N., Seward J.F., Santibanez T.A., Pallansch M.A., Kew O.M., Prevots D.R., Strebel P.M., Cono J., Wharton M., Orenstein W.A., Sutter R.W. Vaccine policy changes and epidemiology of poliomyelitis in the United States. JAMA 2004; 292(14): 1696–1701, https://doi.org/10.1001/jama.292.14.1696.
- Ishmukhametov A.A., Ivanova O.E., Chernyavskaya O.P. Poliomielit. V kn.: Rukovodstvo po epidemiologii infektsionnykh bolezney. T. 1 [Infectious disease epidemiology guide. Vol. 1]. Pod red. Briko N.I. [Briko N.I. (editor)]. Moscow; 2018; p. 313–324.
- MU 3.1.1.2130-06. Enterovirusnye zabolevaniya: klinika, laboratornaya diagnostika, epidemiologiya, profilaktika [MU 3.1.1.2130-06. Enteroviral diseases: clinic, laboratory diagnostics, epidemiology, prevention]. Moscow; 2006.
- Leshchinskaya E.V., Latysheva I.N. Klinika, diagnostika i lechenie ostrogo poliomielita [Clinic, diagnosis, and treatment of acute poliomyelitis]. Moscow; 1998.
- Chumakov M.P., Prisman I.M., Zatsepin T.S. Poliomielit, detskiy spinnomozgovoy paralich [Poliomyelitis, childhood cerebrospinal paralysis]. Moscow: Medgiz; 1953.
- World Health Organization. Polio laboratory manual. Geneva: WHO; 2004.
- World Health Organization. Manual for the virological investigation of polio. Geneva: WHO; 1997.
- World Health Organization. Rukovodstvo po provedeniyu dopolnitel’nykh meropriyatiy, napravlennykh na likvidatsiyu poliomielita [Guidelines for additional activities aimed at eradicating poliomyelitis]. Geneva: WHO; 1997.
- Prikaz Ministerstva zdravookhraneniya RF ot 21 marta 2014 g. No.125n “Ob utverzhdenii natsional’nogo kalendarya profilakticheskikh privivok i kalendarya profilakticheskikh privivok po epidemicheskim pokazaniyam” [Order of the Ministry of Health of the Russian Federation dated March 21, 2014 No.125n “On approval of the national calendar of preventive vaccinations and the calendar of preventive vaccinations according to epidemic indications”].
- Kramer S.D., Aycock W.L., Solomon C.I., Thenebe C.L. Convalescent serum therapy in preparalytic poliomyelitis. N Engl J Med 1932; 206(9): 432–435, https://doi.org/10.1056/nejm193203032060902.
- Brodie M. Active immunization in monkeys against poliomyelitis with germicidally inactivated virus. Science 1934; 79(2061): 594–595, https://doi.org/10.1126/science.79.2061.594.
- Enders J.F., Weller T.H., Robbins F.C. Cultivation of the Lansing strain of poliomyelitis virus in cultures of various human embryonic tissues. Science 1949; 109(2822): 85–87, https://doi.org/10.1126/science.109.2822.85.
- Hammon W.M., Coriell L.L., Stokes J. Jr. Evaluation of Red Cross gamma globulin as a prophylactic agent for poliomyelitis. 2. Conduct and early follow-up of 1952 Texas and Iowa-Nebraska studies. J Am Med Assoc 1952; 150(8): 750–756, https://doi.org/10.1001/jama.1952.03680080012002.
- Salk J.E., Bennet B.L., Lewis L.J., Ward E.N., Youngner J.S. Studies in human subjects on active immunization against poliomyelitis. JAMA 1953; 151(13): 1081–1098, https://doi.org/10.1001/jama.1953.13.1081.
- Lashkevich V.A. History of development of the live poliomyelitis vaccine from Sabin attenuated strains in 1959 and idea of poliomyelitis eradication. Voprosy virusologii 2013; 58(1): 4–10.
- Koprowski H., Jervis G.A., Norton T.W. Immune responses in human volunteers upon oral administration of a rodent-adapted strain of poliomyelitis virus. Am J Hyg 1952; 55(1): 108–126, https://doi.org/10.1093/oxfordjournals.aje.a119499.
- Koprowski H. Immunization against poliomyelitis with living attenuated virus. Am J Trop Med Hyg 1956; 5(3): 440–452, https://doi.org/10.4269/ajtmh.1956.5.440.
- Sabin A.B., Boulgar L.R. History of Sabin attenuated poliovirus oral live vaccine strains. J Biol Stand 1973; 1(2): 115–118, https://doi.org/10.1016/0092-1157(73)90048-6.
- Chumakov M.P., Voroshilova M.K., Vasil’eva K.A., et al. Preliminary report on massive immunization of the population with a live oral polio vaccine from attenuated Sabin virus. Voprosy virusologii 1959; 5: 520–533.
- Nathanson N., Langmuir A.D. The Cutter incident. Poliomyelitis following formaldehyde-inactivated poliovirus vaccination in the United States during the Spring of 1955: II. Relationship of poliomyelitis to Cutter vaccine. Am J Epidemiol 1995; 142(2): 109–148, https://doi.org/10.1093/oxfordjournals.aje.a117611.
- Zhivaya vaktsina protiv poliomielita [Live polio vaccine]. Pod red. Smorodintseva A.A. [Smorodintsev A.A. (editor)]. Leningrad; 1960.
- Bartoshevich E.N., Tsuker M.B., Leshchinskaya E.V., Sokolova I.S., Martynenko I.N., Andreeva L.S., Ashmarina E.E. Polio-like paralytic diseases in children vaccinated with the Sabin live vaccine. Vestnik AMN SSSR 1963; 6: 16–21.
- Kew O., Morris-Glasgow V., Landaverde M., Burns C., Shaw J., Garib Z., André J., Blackman E., Freeman C.J., Jorba J., Sutter R., Tambini G., Venczel L., Pedreira C., Laender F., Shimizu H., Yoneyama T., Miyamura T., van Der Avoort H., Oberste M.S., Kilpatrick D., Cochi S., Pallansch M., de Quadros C. Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 2002; 296(5566): 356–359, https://doi.org/10.1126/science.1068284.
- Kew O.M., Wright P.F., Agol V.I., Delpeyroux F., Shimizu H., Nathanson N., Pallansch M.A. Circulating vaccine-derived polioviruses: current state of knowledge. Bull World Health Organ 2004; 82(1): 16–23.
- Centers for Disease Control and Prevention. Update on vaccine-derived polioviruses — worldwide, April 2011–June 2012. MMWR Morb Mortal Wkly Rep 2012; 61: 741–746.
- Lopez C., Biggar W.D., Park B.H., Good R.A. Nonparalytic poliovirus infections in patients with severe combined immunodeficiency disease. J Pediatr 1974; 84(4): 497–502, https://doi.org/10.1016/s0022-3476(74)80667-0.
- Davis L.E., Bodian D., Price D., Butler I.J., Vickers J.H. Chronic progressive poliomyelitis secondary to vaccination of an immunodeficient child. N Engl J Med 1977; 297(5): 241–245, https://doi.org/10.1056/nejm197708042970503.
- Martín J., Odoom K., Tuite G., Dunn G., Hopewell N., Cooper G., Fitzharris C., Butler K., Hall W.W., Minor P.D. Long-term excretion of vaccinederived poliovirus by a healthy child. J Virol 2004; 78(24): 13839–13847, https://doi.org/10.1128/jvi.78.24.13839-13847.2004.
- van Wezel A.L., van Steenis G., van der Marel P., Osterhaus A.D. Inactivated poliovirus vaccine: current production methods and new developments. Rev Infect Dis 1984; 6(Suppl 2): S335–S340, https://doi.org/10.1093/clinids/6.supplement_2.s335.
- Ehrenfeld E., Modlin J., Chumakov K. Future of polio vaccines. Expert Rev Vaccines 2009; 8(7): 899–905, https://doi.org/10.1586/erv.09.49.
- Doi Y., Abe S., Yamamoto H., Horie H., Ohyama H., Satoh K., Tano Y., Ota Y., Miyazawa M., Wakabayashi K., Hashizume S. Progress with inactivated poliovirus vaccines derived from the Sabin strains. Dev Biol (Basel) 2001; 105: 163–169.
- Dragunsky E.M., Ivanov A.P., Wells V.R., Ivshina A.V., Rezapkin G.V., Abe S., Potapova S.G., Enterline J.C., Hashizume S., Chumakov K.M. Evaluation of immunogenicity and protective properties of inactivated poliovirus vaccines: a new surrogate method for predicting vaccine efficacy. J Infect Dis 2004; 190(8): 1404–1412, https://doi.org/10.1086/424524.
- Dragunsky E.M., Ivanov A.P., Abe S., Potapova S.G., Enterline J.C., Hashizume S., Chumakov K.M. Further development of a new transgenic mouse test for the evaluation of the immunogenicity and protective properties of inactivated poliovirus vaccine. J Infect Dis 2006; 194(6): 804–807, https://doi.org/10.1086/506949.
- Tano Y., Shimizu H., Martin J., Nishimura Y., Simizu B., Miyamura T. Antigenic characterization of a formalin-inactivated poliovirus vaccine derived from live-attenuated Sabin strains. Vaccine 2007; 25(41): 7041–7046, https://doi.org/10.1016/j.vaccine.2007.07.060.
- Shimizu H. Poliovirus vaccine. Uirusu 2012; 62(1): 57–65, https://doi.org/10.2222/jsv.62.57.
- Verdijk P., Rots N.Y., Bakker W.A. Clinical development of a novel inactivated poliomyelitis vaccine based on attenuated Sabin poliovirus strains. Expert Rev Vaccines 2011; 10(5): 635–644, https://doi.org/10.1586/erv.11.51.
- Ivanov A.P., Klebleeva T.D., Ivanova O.E., Ipatova E.G., Gmyl L.V., Ishmuhametov A.A. Experimental approaches to the development of inactivated poliovirus vaccine based on sabin strains. Ehpidemiologiya i vaktsinoprofilaktika 2016; 15(4): 59–64, https://doi.org/10.31631/2073-3046-2016-15-4-59-64.
- Guest S., Pilipenko E., Sharma K., Chumakov K., Roos R.P. Molecular mechanisms of attenuation of the Sabin strain of poliovirus type 3. J Virol 2004; 78(20): 11097–11107, https://doi.org/10.1128/jvi.78.20.11097-11107.2004.
- Kauder S.E., Racaniello V.R. Poliovirus tropism and attenuation are determined after internal ribosome entry. J Clin Invest 2004; 113(12): 1743–1753, https://doi.org/10.1172/jci200421323.
- Gromeier M., Alexander L., Wimmer E. Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc Natl Acad Sci U S A 1996; 93(6): 2370–2375, https://doi.org/10.1073/pnas.93.6.2370.
- Chumakov K., Dragunsky E., Ivshina A., Enterline J., Wells V., Nomura T., Gromeier M., Wimmer E. Inactivated vaccines based on alternatives to wild-type seed virus. Dev Biol (Basel) 2001; 105: 171–177.
- Dobrikova E.Y., Goetz C., Walters R.W., Lawson S.K., Peggins J.O., Muszynski K., Ruppel S., Poole K., Giardina S.L., Vela E.M., Estep J.E., Gromeier M. Attenuation of neurovirulence, biodistribution, and shedding of a poliovirus: rhinovirus chimera after intrathalamic inoculation in Macaca fascicularis. J Virol 2012; 86(5): 2750–2759, https://doi.org/10.1128/jvi.06427-11.
- Macadam A.J., Ferguson G., Stone D.M., Meredith J., Almond J.W., Minor P.D. Live-attenuated strains of improved genetic stability. Dev Biol (Basel) 2001; 105: 179–187.
- Macadam A.J., Ferguson G., Stone D.M., Meredith J., Knowlson S., Auda G., Almond J.W., Minor P.D. Rational design of genetically stable, live-attenuated poliovirus vaccines of all three serotypes: relevance to poliomyelitis eradication. J Virol 2006; 80(17): 8653–8663, https://doi.org/10.1128/jvi.00370-06.
- Rowe A., Burlison J., Macadam A.J., Minor P.D. Functional formation of domain V of the poliovirus noncoding region: significance of unpaired bases. Virology 2001; 289(1): 45–53, https://doi.org/10.1006/viro.2001.1111.
- Toyoda H., Yin J., Mueller S., Wimmer E., Cello J. Oncolytic treatment and cure of neuroblastoma by a novel attenuated poliovirus in a novel poliovirus-susceptible animal model. Cancer Res 2007; 67(6): 2857–2864, https://doi.org/10.1158/0008-5472.can-06-3713.
- Pfeiffer J.K., Kirkegaard K. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc Natl Acad Sci U S A 2003; 100(12): 7289–7294, https://doi.org/10.1073/pnas.1232294100.
- Vignuzzi M., Stone J.K., Arnold J.J., Cameron C.E., Andino R. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 2006; 439(7074): 344–348, https://doi.org/10.1038/nature04388.
- Vignuzzi M., Wendt E., Andino R. Engineering attenuated virus vaccines by controlling replication fidelity. Nat Med 2008; 14(2): 154–161, https://doi.org/10.1038/nm1726.
- Burns C.C., Shaw J., Campagnoli R., Jorba J., Vincent A., Quay J., Kew O. Modulation of poliovirus replicative fitness in HeLa cells by deoptimization of synonymous codon usage in the capsid region. J Virol 2006; 80(7): 3259–3272, https://doi.org/10.1128/jvi.80.7.3259-3272.2006.
- Gutman G.A., Hatfield G.W. Nonrandom utilization of codon pairs in Escherichia coli. Proc Natl Acad Sci U S A 1989; 86(10): 3699–3703, https://doi.org/10.1073/pnas.86.10.3699.
- Coleman J.R., Papamichail D., Skiena S., Futcher B., Wimmer E., Mueller S. Virus attenuation by genome-scale changes in codon pair bias. Science 2008; 320(5884): 1784–1787, https://doi.org/10.1126/science.1155761.
- Burns C.C., Campagnoli R., Shaw J., Vincent A., Jorba J., Kew O. Genetic inactivation of poliovirus infectivity by increasing the frequencies of CpG and UpA dinucleotides within and across synonymous capsid region codons. J Virol 2009; 83(19): 9957–9969, https://doi.org/10.1128/jvi.00508-09.
- Mueller S., Coleman J.R., Papamichail D., Ward C.B., Nimnual A., Futcher B., Skiena S., Wimmer E. Live attenuated influenza virus vaccines by computer-aided rational design. Nat Biotechnol 2010; 28(7): 723–726, https://doi.org/10.1038/nbt.1636.
- Cooper P.D. Genetics of picornaviruses. In: Fraenkel-Conrat H., Wagner R. (editors). Regulation and genetics. Comprehensive virology. Vol 9. Springer US; 1997; p. 133–207, https://doi.org/10.1007/978-1-4684-2718-9_4.
- Furlone M., Guillot S., Otelea D., Balanant J., Candrea A., Crainic R. Polioviruses with natural recombinant genomes isolated from vaccine-associated poliomyelitis. Virology 1993; 196(1): 199–208, https://doi.org/10.1006/viro.1993.1468.
- Agol V.I. Recombination and other genomic rearrangements in picornaviruses. Seminars in Virology 1997; 8(2): 77–84, https://doi.org/10.1006/smvy.1997.0112.
- Combelas N., Holmblat B., Joffret M.L., Colbère-Garapin F., Delpeyroux F. Recombination between poliovirus and coxsackie A viruses of species C: a model of viral genetic plasticity and emergence. Viruses 2011; 3(8): 1460–1484, https://doi.org/10.3390/v3081460.
- Runckel C., Westesson O., Andino R., DeRisi J.L. Identification and manipulation of the molecular determinants influencing poliovirus recombination. PLoS Pathog 2013; 9(2): e1003164, https://doi.org/10.1371/journal.ppat.1003164.
- Porta C., Kotecha A., Burman A., Jackson T., Ren J., Loureiro S., Jones I.M., Fry E.E., Stuart D.I., Charleston B. Rational engineering of recombinant picornavirus capsids to produce safe, protective vaccine antigen. PLoS Pathog 2013; 9(3): e1003255, https://doi.org/10.1371/journal.ppat.1003255.
- Sanders B.P., Edo-Matas D., Custers J.H., Koldijk M.H., Klaren V., Turk M., Luitjens A., Bakker W.A., Uytdehaag F., Goudsmit J., Lewis J.A., Schuitemaker H. PER.C6(®) cells as a serum-free suspension cell platform for the production of high titer poliovirus: a potential low cost of goods option for world supply of inactivated poliovirus vaccine. Vaccine 2013; 31(5): 850–856, https://doi.org/10.1016/j.vaccine.2012.10.070.
- Verdijk P., Rots N.Y., van Oijen M.G., Oberste M.S., Boog C.J., Okayasu H., Sutter R.W., Bakker W.A. Safety and immunogenicity of inactivated poliovirus vaccine based on Sabin strains with and without aluminum hydroxide: a phase I trial in healthy adults. Vaccine 2013; 31(47): 5531–5536, https://doi.org/10.1016/j.vaccine.2013.09.021.
- Westdijk J., Koedam P., Barro M., Steil B.P., Collin N., Vedvick T.S., Bakker W.A., van der Ley P., Kersten G. Antigen sparing with adjuvanted inactivated polio vaccine based on Sabin strains. Vaccine 2013; 31(9): 1298–1304, https://doi.org/10.1016/j.vaccine.2012.12.076.
- Baldwin S.L., Fox C.B., Pallansch M.A., Coler R.N., Reed S.G., Friede M. Increased potency of an inactivated trivalent polio vaccine with oil-in-water emulsions. Vaccine 2011; 29(4): 644–649, https://doi.org/10.1016/j.vaccine.2010.11.043.
- Ivanov A.P., Dragunsky E.M., Chumakov K.M. 1,25-dihydroxyvitamin d3 enhances systemic and mucosal immune responses to inactivated poliovirus vaccine in mice. J Infect Dis 2006; 193(4): 598–600, https://doi.org/10.1086/499970.
- Resik S., Tejeda A., Lago P.M., Diaz M., Carmenates A., Sarmiento L., Alemañi N., Galindo B., Burton A., Friede M., Landaverde M., Sutter R.W. Randomized controlled clinical trial of fractional doses of inactivated poliovirus vaccine administered intradermally by needle-free device in Cuba. J Infect Dis 2010; 201(9): 1344–1352, https://doi.org/10.1086/651611.
- Cadorna-Carlos J., Vidor E., Bonnet M.C. Randomized controlled study of fractional doses of inactivated poliovirus vaccine administered intradermally with a needle in the Philippines. Int J Infect Dis 2012; 16(2): e110–e116, https://doi.org/10.1016/j.ijid.2011.10.002.
- Nelson K.S., Janssen J.M., Troy S.B., Maldonado Y. Intradermal fractional dose inactivated polio vaccine: a review of the literature. Vaccine 2012; 30(2): 121–125, https://doi.org/10.1016/j.vaccine.2011.11.018.
- Soonawala D., Verdijk P., Wijmenga-Monsuur A.J., Boog C.J., Koedam P., Visser L.G., Rots N.Y. Intradermal fractional booster dose of inactivated poliomyelitis vaccine with a jet injector in healthy adults. Vaccine 2013; 31(36): 3688–3694, https://doi.org/10.1016/j.vaccine.2013.05.104.
- Resik S., Tejeda A., Sutter R.W., Diaz M., Sarmiento L., Alemañi N., Garcia G., Fonseca M., Hung L.H., Kahn A.L., Burton A., Landaverde J.M., Aylward R.B. Priming after a fractional dose of inactivated poliovirus vaccine. N Engl J Med 2013; 368(5): 416–424, https://doi.org/10.1056/nejmoa1202541.
- Hiraishi Y., Nandakumar S., Choi S.O., Lee J.W., Kim Y.C., Posey J.E., Sable S.B., Prausnitz M.R. Bacillus Calmette-Guérin vaccination using a microneedle patch. Vaccine 2011; 29(14): 2626–2636, https://doi.org/10.1016/j.vaccine.2011.01.042.
- del Pilar Martin M., Weldon W.C., Zarnitsyn V.G., Koutsonanos D.G., Akbari H., Skountzou I., Jacob J., Prausnitz M.R., Compans R.W. Local response to microneedle-based influenza immunization in the skin. MBio 2012; 3(2): e00012-12, https://doi.org/10.1128/mbio.00012-12.
- Kim Y.C., Song J.M., Lipatov A.S., Choi S.O., Lee J.W., Donis R.O., Compans R.W., Kang S.M., Prausnitz M.R. Increased immunogenicity of avian influenza DNA vaccine delivered to the skin using a microneedle patch. Eur J Pharm Biopharm 2012 Jun; 81(2): 239–247, https://doi.org/10.1016/j.ejpb.2012.03.010.
- Edens C., Collins M.L., Ayers J., Rota P.A., Prausnitz M.R. Measles vaccination using a microneedle patch. Vaccine 2013; 31(34): 3403–3409, https://doi.org/10.1016/j.vaccine.2012.09.062.