Vaccine Strategies

David J. Rowlands; Philip D. Minor

doi:10.1128/9781555816698.ch27

Chapter 27 : Vaccine Strategies

Authors: David J. Rowlands¹, Philip D. Minor²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Institute for Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom; 2: Division of Virology, National Institute for Biological Standards and Control, South Mimms, Potters Bar, Hertfordshire EN6 3QG, United Kingdom

Content Type: Monograph

Publication Year: 2010

Category: Viruses and Viral Pathogenesis

Book DOI: 10.1128/9781555816698

Chapter DOI: 10.1128/9781555816698.ch27

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Vaccine Strategies, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555816698/9781555816032_Chap27-1.gif /docserver/preview/fulltext/10.1128/9781555816698/9781555816032_Chap27-2.gif

Abstract:

Vaccination is one of the most cost-effective methods to control and prevent infectious diseases and has had a major impact on human and animal health over the last century. Commercial vaccines have been developed for just three picornavirus-associated diseases. Two are human afflictions, poliomyelitis and hepatitis A, and the third is foot-and-mouth disease (FMD), a major disease of domestic livestock. The antigenic material for use in vaccines is subject to rigorous regulatory controls to minimize unwanted side effects. All current picornavirus vaccines are produced in tissue culture under tightly controlled conditions. The presence of multiple serotypes is obviously a complicating issue for the development and deployment of vaccines. In the early development of FMD vaccines, formaldehyde was used to chemically inactivate the virus. However, the inactivation kinetics in the relatively crude virus suspensions used for vaccine production are not linear, and a small persistent fraction of infectious virus may be detected even after prolonged inactivation times, as was also seen in some early polio vaccines. The culture of hepatitis A virus in vitro proved difficult, and much of the early work that led to the eventual development of a vaccine relied on human volunteer studies or work in New World primates or chimpanzees. Quantitative improvements would be expected to reduce the frequency at which booster immunizations are required and, qualitatively, broadening of the immune response to include cell-mediated responses and secretory immunity is desirable.

Citation: Rowlands D, Minor P. 2010. Vaccine Strategies, p 431-447. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch27

Highlighted Text: Show | Hide

Full text loading...

References

/content/book/10.1128/9781555816698.ch27

1. Abrams, C. C.,, A. M. King, and, G. J. Belsham. 1995. Assembly of foot-and-mouth disease virus empty capsids synthesized by a vaccinia virus expression system. J. Gen. Virol. 76: 3089– 3098.

2. Ahrl, R.,, B. Haas,, R. J. Lorenz, and, G. Wittmann. 1990. Alternative potency test of FMD vaccines and results of comparative antibody assays in different cell systems and ELISA, p. 51–60. Report of the Session of the Research Group of the Standing Technical Committee of the European Commission for the Control of Foot-and-Mouth Disease, Lindholm, Denmark.

3. Almeida, M. R.,, E. Rieder,, J. Chinsangaram,, G. Ward,, C. Beard,, M. J. Grubman, and, P. W. Mason. 1998. Construction and evaluation of an attenuated vaccine for foot-and-mouth disease: difficulty adapting the leader proteinase-deleted strategy to the serotype O1 virus. Virus Res. 55: 49– 60.

4. Ansardi, D. C.,, D. C. Porter, and, C. D. Morrow. 1993. Complementation of a poliovirus defective genome by a recombinant vaccinia virus which provides poliovirus P1 capsid precursor in trans. J. Virol. 67: 3684– 3690.

5. Backues, K. A.,, M. Hill,, A. C. Palmenberg,, C. Miller,, K. F. Soike, and, R. Aguilar. 1999. Genetically engineered Mengo virus vaccination of multiple captive wildlife species. J. Wildl. Dis. 35: 384– 387.

6. Barteling, S. J. 2004. Modern inactivated foot-and mouth disease (FMD) vaccines: historical background and key elements in production and use, p. 305–333. In F. Sobrino and, E. Domingo (ed.), Foot-and-Mouth Disease: Current Perspectives. Horizon Bioscience, Wymondham, England.

7. Bedson, S. P.,, H. B. Maitland, and, Y. M. Burbury. 1927. 2nd report, Foot-and-Mouth Disease Research Committee. HMSO, London, England.

8. Belin, M. 1927. Premiere tentative de vaccination antiaph-teuse realisee a l’aide des complexes vaccino-aphteux. C. R. Soc. Biol. Paris 96: 116.

9. Benkirane, N.,, G. Guichard,, J. P. Briand,, S. Muller,, F. Brown, and, M. H. Van Regenmortel. 1996. Mimicry of viral epitopes with retro-i nverso peptides of increased stability. Dev. Biol. Stand. 87: 283– 291.

10. Bittle, J. L.,, R. A. Houghten,, H. Alexander,, T. M. Shinnick,, J. G. Sutcliffe,, R. A. Lerner,, D. J. Rowlands, and, F. Brown. 1982. Protection against foot-and-mouth disease by immunization with a chemically synthesized peptide predicted from the viral nucleotide sequence. Nature 298: 30– 33.

11. Black, L., and, T. W. Pay. 1975. The evaluation of hypersensi-tivity tests in cattle after foot-and-mouth disease vaccination. J. Hyg. (London) 74: 169– 181.

12. Broekhuijsen, M. P.,, J. M. van Rijn,, A. J. Blom,, P. H. Pouwels,, B. E. Enger-Valk,, F. Brown, and, M. J. Francis. 1987. Fusion proteins with multiple copies of the major antigenic determinant of foot-and-mouth disease virus protect both the natural host and laboratory animals. J. Gen. Virol. 68: 3137– 3143.

13. Brooksby, J. B. 1958. The virus of foot-and-mouth disease. Adv. Virus Res. 5: 1– 37.

14. Brooksby, J. B., and, J. Rogers. 1957. Methods used in typing the virus of foot-and-mouth disease at Pirbright, 1950-1955, p. 31–34. Methods of Typing and Cultivation of Foot-and-Mouth Disease Virus. Project 208. Organisation for European Economic Cooperation, Paris, France.

15. Brown, C. C.,, J. Chinsangaram, and, M. J. Grubman. 2000. Type I interferon production in cattle infected with 2 strains of foot-and-mouth disease virus, as determined by in situ hybridization. Can. J. Vet. Res. 64: 130– 133.

16. Burns, C. C.,, J. Shaw,, R. Campagnoli,, J. Jorba,, A. Vincent,, J. Quay, and, O. Kew. 2006. Modulation of poliovirus replicative fitness in HeLa cells by deoptimization of synonymous codon usage in the capsid region. J. Virol. 80: 3259– 3272.

17. Cao, Y.,, Z. Lu,, J. Sun,, X. Bai,, P. Sun,, H. Bao,, Y. Chen,, J. Guo,, D. Li,, X. Liu, and, Z. Liu. 2009. Synthesis of empty capsid-like particles of Asia I foot-and-mouth disease virus in insect cells and their immunogenicity in guinea pigs. Vet. Microbiol. 137: 10– 17.

18. Capstick, P. B.,, R. C. Telling,, W. G. Chapman, and, D. L. Stewart. 1962. Growth of a cloned strain of hamster kidney cells in suspended cultures and their susceptibility to the virus of foot-and-mouth disease. Nature 195: 1163– 1164.

19. Chen, H. F.,, M. H. Chang,, B. L. Chiang, and, S. T. Jeng. 2006. Oral immunization of mice using transgenic tomato fruit expressing VP1 protein from enterovirus 71. Vaccine 24: 2944– 2951.

20. Chung, Y. C.,, M. S. Ho,, J. C. Wu,, W. J. Chen,, J. H. Huang,, S. T. Chou, and, Y. C. Hu. 2008. Immunization with viruslike particles of enterovirus 71 elicits potent immune responses and protects mice against lethal challenge. Vaccine 26: 1855– 1862.

21. Clarke, B. E.,, S. E. Newton,, A. R. Carroll,, M. J. Francis,, G. Appleyard,, A. D. Syred,, P. E. Highfield,, D. J. Rowlands, and, F. Brown. 1987. Improved immunogenicity of a peptide epitope after fusion to hepatitis B core protein. Nature 330: 381– 384.

22. Cox, J. H.,, J. Ivanyi,, D. B. Young,, J. R. Lamb,, A. D. Syred, and, M. J. Francis. 1988. Orientation of epitopes influences the immunogenicity of synthetic peptide dimers. Eur. J. Immunol. 18: 2015– 2019.

23. Cunliffe, H. R. 1973. Inactivation of foot-and-mouth disease virus with ethylenimine. Appl. Microbiol. 26: 747– 750.

24. Cutrone, R.,, J. Lednicky,, G. Dunn,, P. Rizzo,, M. Bocchetta,, K. Chumakov,, P. Minor, and, M. Carbone. 2005. Some oral polio-virus vaccines were contaminated with infectious SV40 after 1961. Cancer Res. 65: 10273– 10279.

25. de Avila Botton, S.,, M. C. Brum,, E. Bautista,, M. Koster,, R. Weiblen,, W. T. Golde, and, M. J. Grubman. 2006. Immunopo-tentiation of a foot-and-mouth disease virus subunit vaccine by interferon alpha. Vaccine 24: 3446– 3456.

26. DiMarchi, R.,, G. Brooke,, C. Gale,, V. Cracknell,, T. Doel, and, N. Mowat. 1986. Protection of cattle against foot-and-mouth disease by a synthetic peptide. Science 232: 639– 641.

27. Doel, T. R. 2003. FMD vaccines. Virus Res. 91: 81– 99.

28. Doel, T. R., and, P. J. Baccarini. 1981. Thermal stability of foot-and-mouth disease virus. Arch. Virol. 70: 21– 32.

29. Dougherty, R. H., and, J. V. Fahy. 2009. Acute exacerbations of asthma: epidemiology, biology and the exacerbation-prone phenotype. Clin. Exp. Allergy 39: 193– 202.

30. Du, Y.,, P. Jiang,, Y. Li,, H. He,, W. Jiang,, X. Wang, and, W. Hong. 2007. Immune responses of two recombinant adenoviruses expressing VP1 antigens of FMDV fused with porcine gran-ulocyte macrophage colony-stimulating factor. Vaccine 25: 8209– 8219.

31. Du, Y.,, Y. Li,, H. He,, J. Qi,, W. Jiang,, X. Wang,, B. Tang,, J. Cao, and, P. Jiang. 2008. Enhanced immunogenicity of multiple-epitopes of foot-and-mouth disease virus fused with porcine interferon alpha in mice and protective efficacy in guinea pigs and swine. J. Virol. Methods 149: 144– 152.

32. Duke, G. M.,, J. E. Osorio, and, A. C. Palmenberg. 1990. Attenuation of Mengo virus through genetic engineering of the 5′ noncoding poly(C) tract. Nature 343: 474– 476.

33. Elmishad, A. G.,, M. Bocchetta,, H. I. Pass, and, M. Carbone. 2006. Polio vaccines, SV40 and human tumours, an update on false positive and false negative results. Dev. Biol. (Basel) 123: 109– 117.

34. Flehmig, B.,, A. Haage, and, M. Pfister. 1986. Immunogenicity of a hepatitis A virus vaccine. J. Med. Virol. 22: 7– 16.

35. Foo, D. G.,, S. Alonso,, M. C. Phoon,, N. P. Ramachandran,, V. T. Chow, and, C. L. Poh. 2007. Identification of neutralizing linear epitopes from the VP1 capsid protein of enterovirus 71 using synthetic peptides. Virus Res. 125: 61– 68.

36. Fowler, V. L.,, N. J. Knowles,, D. J. Paton, and, P. V. Barnett. 2010. Marker vaccine potential of a foot-and mouth disease virus with a partial VP1 G-H loop deletion. Vaccine 38: 3428– 3434.

37. Fowler, V. L.,, D. J. Paton,, E. Rieder, and, P. V. Barnett. 2008. Chimeric foot-and-mouth disease viruses: evaluation of their efficacy as potential marker vaccines in cattle. Vaccine 26: 1982– 1989.

38. Francis, M. J.,, G. Z. Hastings,, A. L. Brown,, K. G. Grace,, D. J. Rowlands,, F. Brown, and, B. E. Clarke. 1990. Immunological properties of hepatitis B core antigen fusion proteins. Proc. Natl. Acad. Sci. USA 87: 2545– 2549.

39. Francis, M. J.,, G. Z. Hastings,, F. Brown,, J. McDermed,, Y. A. Lu, and, J. P. Tam. 1991. Immunological evaluation of the multiple antigen peptide (MAP) system using the major immuno-genic site of foot-and-mouth disease virus. Immunology 73: 249– 254.

40. Francis, M. J.,, G. Z. Hastings,, A. D. Syred,, B. McGinn,, F. Brown, and, D. J. Rowlands. 1987. Non-responsiveness to a foot-and-mouth disease virus peptide overcome by addition of foreign helper T-cell determinants. Nature 330: 168– 170.

41. Frenkel, H. S. 1947. La culture du virus de la fievre aphteuse sur l’epithelium de la langue des bovides. Bull. Off. Int. Epi-zoot. 28: 155– 162. (In French.)

42. Galloway, I. A.,, W. M. Henderson, and, J. B. Brooksby. 1948. Strains of the virus of foot-and-mouth disease recovered from outbreaks in Mexico. Proc. Soc. Exp. Biol. Med. 69: 57– 63.

43. Gellis, S. S.,, J. Stokes,, G. M. Brother,, W. M. Hall,, H. R. Gilmore,, E. Beyer, and, R. A. Morissey. 1945. The use of human immune serum globulin (gamma globulin) in infectious (epidemic) hepatitis in the Mediterranean theatre of operations. JAMA 128: 1062– 1063.

44. Grubman, M. J. 2005. Development of novel strategies to control foot-and-mouth disease: marker vaccines and antivirals. Biologicals 33: 227– 234.

45. Grubman, M. J., and, J. Chinsangaram. 2000. Foot-and-mouth disease virus: the role of the leader proteinase in viral pathogenesis. Recent Res. Dev. Virol. 2: 123– 134.

46. Grubman, M. J.,, D. O. Morgan,, J. Kendall, and, B. Baxt. 1985. Capsid intermediates assembled in a foot-and-mouth disease virus genome RNA-programmed cell-free translation system and in infected cells. J. Virol. 56: 120– 126.

47. Gust, I. D. 1988. Prevention and control of hepatitis A, p. 7780. In A. J. Zuckerman (ed.), Viral Hepatitis and Liver Disease. Alan R. Liss, Inc., New York, NY.

48. Hammon, W. D.,, L. L. Corielli,, P. F. Wehrle, and, J. Stokes. 1953. Evaluation of Red Cross gammaglobulin as a prophylactic agent for poliomyelitis. 4:Final report of results based on clinical diagnosis. JAMA 151: 1272– 1285.

49. He, Y.,, P. Qian,, K. Zhang,, Q. Yao,, D. Wang,, Z. Xu,, B. Wu,, M. Jin,, S. Xiao, and, H. Chen. 2008. Construction and immune response characterization of a recombinant pseudorabies virus co-expressing capsid precursor protein (P1) and a multiepi-tope peptide of foot-and-mouth disease virus in swine. Virus Genes 36: 393– 400.

50. Heikkinen, T., and, A. Jarvinen. 2003. The common cold. Lancet 361: 51– 59.

51. Hohlich, B. J.,, K. H. Wiesmuller,, B. Haas,, W. Gerner,, R. Correa,, H. R. Hehnen,, T. Schlapp,, E. Pfaff, and, A. Saalmuller. 2003. Induction of an antigen-specific immune response and partial protection of cattle against challenge infection with foot-and-mouth disease virus (FMDV) after lipopeptide vaccination with FMDV-specific B-cell epitopes. J. Gen. Virol. 84: 3315– 3324.

52. Karron, R. A.,, R. J. Daemer,, J. R. Ticehurst,, K. Mihalik,, H. Popper,, S. M. Feinstone, and, R. H. Purcell. 1988. Evaluation of attenuation of cell culture adapted hepatitis A virus in nonhu-man primates, p. 74–76. In A. J. Zuckerman (ed.), Viral Hepatitis and Liver Disease. Alan R. Liss, Inc., New York, NY.

53. Katpally, U.,, T. M. Fu,, D. C. Freed,, D. R. Casimiro, and, T. J. Smith. 2009. Antibodies to the buried N terminus of rhinovirus VP4 exhibit cross-serotypic neutralization. J. Virol. 83: 7040– 7048.

54. Kew, O.,, V. Morris-Glasgow,, M. Landaverde,, C. Burns,, J. Shaw,, Z. Garib,, J. Andre,, E. Blackman,, C. J. Freeman,, J. Jorba,, R. Sutter,, G. Tambini,, L. Venczel,, C. Pedreira,, F. Laender,, H. Shimizu,, T. Yoneyama,, T. Miyamura,, H. van Der Avoort,, M. S. Oberste,, D. Kilpatrick,, S. Cochi,, M. Pallansch, and, C. de Quadros. 2002. Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 296: 356– 359.

55. King, A. M.,, B. O. Underwood,, D. McCahon,, J. W. Newman, and, F. Brown. 1981. Biochemical identification of viruses causing the 1981 outbreaks of foot and mouth disease in the UK. Nature 293: 479– 480.

56. Kitching, P.,, J. Hammond,, M. Jeggo,, B. Charleston,, D. Paton,, L. Rodriguez, and, R. Heckert. 2007. Global FMD control: is it an option? Vaccine 25: 5660– 5664.

57. Laporte, J., and, G. Lenoir. 1973. Structural proteins of foot-and-mouth disease virus. J. Gen. Virol. 20: 161– 168.

58. Lewis, J. K.,, B. Bothner,, T. J. Smith, and, G. Siuzdak. 1998. Antiviral agent blocks breathing of the common cold virus. Proc. Natl. Acad. Sci. USA 95: 6774– 6778.

59. Lewis, S. A.,, D. O. Morgan, and, M. J. Grubman. 1991. Expression, processing, and assembly of foot-and-mouth disease virus capsid structures in heterologous systems: induction of a neutralizing antibody response in guinea pigs. J. Virol. 65: 6572– 6580.

60. Li, C. P., and, M. Schaffer. 1953. Adaptation of type 1 poliomyelitis virus to mice. Proc. Soc. Exp. Biol. Med. 82: 477– 481.

61. Li, Q.,, A. G. Yafal,, Y. M. Lee,, J. Hogle, and, M. Chow. 1994. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J. Virol. 68: 3965– 3970.

62. Li, Y.,, C. M. Stirling,, M. S. Denyer,, P. Hamblin,, G. Hutchings,, H. H. Takamatsu, and, P. V. Barnett. 2008. Dramatic improvement in FMD DNA vaccine efficacy and cross-serotype antibody induction in pigs following a protein boost. Vaccine 26: 2647– 2656.

63. Li, Z.,, Y. Yi,, X. Yin,, Z. Zhang, and, J. Liu. 2008. Expression of foot-and-mouth disease virus capsid proteins in silkworm-baculovirus expression system and its utilization as a subunit vaccine. PLoS One 3: e2273.

64. Loeffler, F., and, P. Frosch. 1897. Summarischer Bericht uber die Ergbnisse der Untersuchungen der Kommission zur Er-forschung der Maul-und Klauenseuche bei dem Institut fur In-fektionskrankheiten in Berlin. Zentralbl. Bakteriol. Parasitol. Infekt. 22: 257– 259. (In German.)

65. Macadam, A. J.,, G. Ferguson,, D. M. Stone,, J. Meredith,, S. Knowlson,, G. Auda,, J. W. Almond, and, P. D. Minor. 2006. Rational design of genetically stable, live-attenuated poliovirus vaccines of all three serotypes: relevance to poliomyelitis eradication. J. Virol. 80: 8653– 8663.

66. Mason, P. W.,, J. Chinsangaram,, M. P. Moraes,, G. A. Mayr, and, M. J. Grubman. 2003. Engineering better vaccines for foot- and-mouth disease. Dev. Biol. (Basel) 114: 79– 88.

67. Mason, P. W.,, M. J. Grubman, and, B. Baxt. 2003. Molecular basis of pathogenesis of FMDV. Virus Res. 91: 9– 32.

68. Mason, P. W.,, M. E. Piccone,, T. S. McKenna,, J. Chinsangaram, and, M. J. Grubman. 1997. Evaluation of a live-attenuated foot-and-mouth disease virus as a vaccine candidate. Virology 227: 96– 102.

69. Mateo, R.,, E. Luna,, V. Rincon, and, M. G. Mateu. 2008. Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J. Virol. 82: 12232– 12240.

70. Minor, P. D.,, A. John,, M. Ferguson, and, J. P. Icenogle. 1986. Antigenic and molecular evolution of the vaccine strain of type 3 poliovirus during the period of excretion by a primary vac-cinee. J. Gen. Virol. 67: 693– 706.

71. Moraes, M. P.,, T. de Los Santos,, M. Koster,, T. Turecek,, H. Wang,, V. G. Andreyev, and, M. J. Grubman. 2007. Enhanced antiviral activity against foot-and-mouth disease virus by a combination of type I and II porcine interferons. J. Virol. 81: 7124– 7135.

72. Mowat, G. N., and, W. G. Chapman. 1962. Growth of foot- and-mouth disease virus in a fibroblastic cell line derived from hamster kidneys. Nature 194: 253– 255.

73. Mowat, G. N.,, R. C. Masters, and, M. J. Prince. 1973. Enhancement of immunizing potency of a foot-and-mouth disease vaccine for cattle by treatment of the antigen with formaldehyde. Arch. Gesamte Virusforsch. 41: 365– 370.

74. Mueller, S.,, D. Papamichail,, J. R. Coleman,, S. Skiena, and, E. Wimmer. 2006. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J. Virol. 80: 9687– 9696.

75. Mulcahy, G.,, C. Gale,, P. Robertson,, S. Iyisan,, R. D. DiMarchi, and, T. R. Doel. 1990. Isotype responses of infected, virus-vaccinated and peptide-vaccinated cattle to foot-and-mouth disease virus. Vaccine 8: 249– 256.

76. Nathanson, N., and, A. D. Langmuir. 1963. The Cutter Incident. Poliomyelitis following formaldehyde-inactivated poliovirus vaccination in the United States during the spring of 1955. I. Background. Am. J. Hyg. 78: 16– 28.

77. Nkowane, B. M.,, S. G. Wassilak,, W. A. Orenstein,, K. J. Bart,, L. B. Schonberger,, A. R. Hinman, and, O. M. Kew. 1987. Vaccine-associated paralytic poliomyelitis. United States: 1973 through 1984. JAMA 257: 1335– 1340.

78. Offit, P. A. 2005. The Cutter Incident. Yale University Press, New Haven, CT.

79. Parida, S. 2009. Vaccination against foot-and-mouth disease virus: strategies and effectiveness. Expert Rev. Vaccines 8: 347– 365.

80. Pena, L.,, M. P. Moraes,, M. Koster,, T. Burrage,, J. M. Pacheco,, F. D. Segundo, and, M. J. Grubman. 2008. Delivery of a foot-and-mouth disease virus empty capsid subunit antigen with nonstructural protein 2B improves protection of swine. Vaccine 26: 5689– 5699.

81. Pfaff, E.,, M. Mussgay,, H. O. Bohm,, G. E. Schulz, and, H. Schaller. 1982. Antibodies against a preselected peptide recognize and neutralize foot and mouth disease virus. EMBO J. 1: 869– 874.

82. Piccone, M. E.,, E. Rieder,, P. W. Mason, and, M. J. Grubman. 1995. The foot-and-mouth disease virus leader proteinase gene is not required for viral replication. J. Virol. 69: 5376– 5382.

83. Provost, P. J., and, M. R. Hilleman. 1979. Propagation of human hepatitis A virus in cell culture in vitro. Proc. Soc. Exp. Biol. Med. 160: 213– 221.

84. Provost, P. J.,, J. V. Hughes,, W. J. Miller,, P. A. Giesa,, F. S. Banker, and, E. A. Emini. 1986. An inactivated hepatitis A viral vaccine of cell culture origin. J. Med. Virol. 19: 23– 31.

85. Ren, X. G.,, F. Xue,, Y. M. Zhu,, G. Z. Tong,, Y. H. Wang,, J. K. Feng,, H. F. Shi, and, Y. R. Gao. 2009. Construction of a recombinant BHV-1 expressing the VP1 gene of foot and mouth disease virus and its immunogenicity in a rabbit model. Bio-technol. Lett. 31: 1159– 1165.

86. Rennels, M. B.,, R. L. Ward,, M. E. Mack, and, E. T. Zito. 1996. Concurrent oral poliovirus and rhesus-human reassortant rotavirus vaccination: effects on immune responses to both vaccines and on efficacy of rotavirus vaccines. The US Rotavirus Vaccine Efficacy Group. J. Infect. Dis. 173: 306– 313.

87. Rodriguez, L. L.,, J. Barrera,, E. Kramer,, J. Lubroth,, F. Brown, and, W. T. Golde. 2003. A synthetic peptide containing the consensus sequence of the G-H loop region of foot-and-mouth disease virus type-O VP1 and a promiscuous T-helper epitope induces peptide-specific antibodies but fails to protect cattle against viral challenge. Vaccine 21: 3751– 3756.

88. Rodriguez Pulido, M.,, F. Sobrino,, B. Borrego, and, M. Saiz. 2009. Attenuated foot-and-mouth disease virus RNA carrying a deletion in the 3′ noncoding region can elicit immunity in swine. J. Virol. 83: 3475– 3485.

89. Rombaut, B., and, J. P. Jore. 1997. Immunogenic, non-infectious polio subviral particles synthesized in Saccharo-myces cerevisiae. J. Gen. Virol. 78: 1829– 1832.

90. Roosien, J.,, G. J. Belsham,, M. D. Ryan,, A. M. King, and, J. M. Vlak. 1990. Synthesis of foot-and-mouth disease virus capsid proteins in insect cells using baculovirus expression vectors. J. Gen. Virol. 71: 1703– 1711.

91. Rosenbusch, C. T.,, A. Decamps, and, N. Gelormini. 1948. In-tradermal foot-and-mouth disease vaccine: results obtained from the first million head of cattle vaccinated. J. Am. Vet. Med. Assoc. 112: 45– 47.

92. Rowlands, D. J.,, D. V. Sangar, and, F. Brown. 1975. A comparative chemical and serological study of the full and empty particles of foot-and mouth disease virus. J. Gen. Virol. 26: 227– 238.

93. Ryman, K. D.,, W. B. Klimstra,, K. B. Nguyen,, C. A. Biron, and, R. E. Johnston. 2000. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J. Virol. 74: 3366– 3378.

94. Sabin, A. B. 1956. Present status of attenuated live-virus poliomyelitis vaccine. JAMA 162: 1589– 1596.

95. Sabin, A. B., and, L. Boulger. 1973. History of Sabin attenuated poliovirus oral live vaccine strains. J. Biol. Stand. 1: 115– 118.

96. Sabin, A. B.,, W. A. Henessen, and, J. Winsner. 1954. Studies of variants of poliomyelitis virus. 1. Experimental segregation and properties of avirulent varients of three immunogenic types. J. Exp. Med. 99: 551– 576.

97. Salt, J. S.,, P. V. Barnett,, P. Dani, and, L. Williams. 1998. Emergency vaccination of pigs against foot-and-mouth disease: protection against disease and reduction in contact transmission. Vaccine 16: 746– 754.

98. Shi, X. J.,, B. Wang, and, M. Wang. 2007. Immune enhancing effects of recombinant bovine IL-18 on foot-and-mouth disease vaccination in mice model. Vaccine 25: 1257– 1264.

99. Skinner, H. H. 1951. Propagation of strains of foot-and-mouth disease virus in unweaned white mice. Proc. R. Soc. Med. 44: 1041– 1044.

100. Spratt, B. 2007. Independent review of the safety of UK facilities handling foot-and-mouth disease. http://www.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/fmd/documents/spratt_final.pdf.

101. Steward, M. W.,, C. M. Stanley,, R. Dimarchi,, G. Mulcahy, and, T. R. Doel. 1991. High-affinity antibody induced by immunization with a synthetic peptide is associated with protection of cattle against foot-and-mouth disease. Immunology 72: 99– 103.

102. Stokes, J., and, J. R. Neefe. 1945. The prevention and attenuation of infectious hepatitis by gammaglobulin. JAMA 127: 144– 145.

103. Strohmaier, K.,, R. Franze, and, K. H. Adam. 1982. Location and characterization of the antigenic portion of the FMDV immunizing protein. J. Gen. Virol. 59: 295– 306.

104. Su, C.,, X. Duan,, X. Wang,, C. Wang,, R. Cao,, B. Zhou, and, P. Chen. 2007. Heterologous expression of FMDV im-munodominant epitopes and HSP70 in P. pastoris and the subsequent immune response in mice. Vet. Microbiol. 124: 256– 263.

105. Taboga, O.,, C. Tami,, E. Carrillo,, J. I. Nunez,, A. Rodriguez,, J. C. Saiz,, E. Blanco,, M. L. Valero,, X. Roig,, J. A. Camarero,, D. Andreu,, M. G. Mateu,, E. Giralt,, E. Domingo,, F. Sobrino, and, E. L. Palma. 1997. A large-scale evaluation of peptide vaccines against foot-and-mouth disease: lack of solid protection in cattle and isolation of escape mutants. J. Virol. 71: 2606– 2614.

106. Telling, R. C., and, R. Elsworth. 1965. Submerged culture of hamster kidney cells in a stainless steel vessel. Biotechnol. Bioeng. 7: 417– 434.

107. Ubertini, B.,, L. Nardelli,, A. Dal Prato,, G. P. Panina, and, A. Santero. 1963. Large scale cultivation of foot-and-mouth disease virus on calf kidney cell monolayers in rolling bottles. Zentralbl. Vet. Med. B 10: 93.

108. Urakawa, T.,, M. Ferguson,, P. D. Minor,, J. Cooper,, M. Sullivan,, J. W. Almond, and, D. H. Bishop. 1989. Synthesis of im-munogenic, but non-infectious, poliovirus particles in insect cells by a baculovirus expression vector. J. Gen. Virol. 70: 1453– 1463.

109. Vallee, H., and, H. Carre. 1922. Sur la pluralite des virus aph-teux. C. R. Acad. Sci. Paris 174: 1498– 1500.

110. Vallee, H.,, H. Carre, and, P. Rinjard. 1925. On immunisation against foot-and-mouth disease. Rech. Med. Vet. 101: 297– 299.

111. van Wezel, A. L.,, G. van Steenis,, P. van der Marel, and, A. D. Osterhaus. 1984. Inactivated poliovirus vaccine: current production methods and new developments. Rev. Infect. Dis. 6 (Suppl. 2): S335– S340.

112. Vignuzzi, M.,, J. K. Stone,, J. J. Arnold,, C. E. Cameron, and, R. Andino. 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439: 344– 348.

113. Villen, J.,, E. Borras,, W. M. Schaaper,, R. H. Meloen,, M. Davila,, E. Domingo,, E. Giralt, and, D. Andreu. 2002. Functional mimicry of a discontinuous antigenic site by a designed synthetic peptide. Chembiochem 3: 175– 182.

114. Waldmann, O.,, K. Kobe, and, G. Pyl. 1937. Die Aktive Im-munisierung des Rindes gegan Maul-und Klauenseuche mit-tels Formolimpfstoff. Zentralbl. Bakteriol. Parasitol. Infekt. 138: 401– 412. (In German.)

115. Waldmann, O., and, J. Pape. 1920. Die Kuenstliche Uebertragung der Maul-und Klauenseuche das Meerschweinchen. Berl. Tierarztl. Wochenschr. 36: 519– 520. (In German.)

116. Waldmann, O., and, K. Trautwein. 1926. Experimentelle Untersuchungen uber die Pluralitat des Maul-und Klauen-seuchevirus. Berl. Tierarztl. Wochenschr. 42: 569– 571. (In German.)

117. Wang, C. Y.,, T. Y. Chang,, A. M. Walfield,, J. Ye,, M. Shen,, S. P. Chen,, M. C. Li,, Y. L. Lin,, M. H. Jong,, P. C. Yang,, N. Chyr,, E. Kramer, and, F. Brown. 2002. Effective synthetic peptide vaccine for foot-and-mouth disease in swine. Vaccine 20: 2603– 2610.

118. Wang, D. M.,, J. B. Zhu,, M. Peng, and, P. Zhou. 2008. Induction of a protective antibody response to FMDV in mice following oral immunization with transgenic Stylosanthes spp. as a feedstuff additive. Transgenic Res. 17: 1163– 1170.

119. Wang, J. L.,, M. Q. Liu,, J. Han,, W. Z. Chen,, W. Cong,, G. Cheng,, Y. H. Gao,, Y. G. Lu,, J. L. Chen,, X. P. Zuo,, W. Y. Yan, and, Z. X. Zheng. 2007. A peptide of foot-and-mouth disease virus serotype Asia 1 generating a neutralizing antibody response, and an immunostimulatory peptide. Vet. Micro- biol. 125: 224– 231.

120. Wu, C. N.,, Y. C. Lin,, C. Fann,, N. S. Liao,, S. R. Shih, and, M. S. Ho. 2001. Protection against lethal enterovirus 71 infection in newborn mice by passive immunization with subunit VP1 vaccines and inactivated virus. Vaccine 20: 895– 904.

121. Wu, Q.,, M. P. Moraes, and, M. J. Grubman. 2003. Recombinant adenovirus co-expressing capsid proteins of two serotypes of foot-and-mouth disease virus (FMDV): in vitro characterization and induction of neutralizing antibodies against FMDV in swine. Virus Res. 93: 211– 219.

122. Yang, C. D.,, J. T. Liao,, C. Y. Lai,, M. H. Jong,, C. M. Liang,, Y. L. Lin,, N. S. Lin,, Y. H. Hsu, and, S. M. Liang. 2007. Induction of protective immunity in swine by recombinant bamboo mosaic virus expressing foot-and-mouth disease virus epitopes. BMC Biotechnol. 7: 62.