The compatibility of inactivated-enterovirus 71 vaccination with coxsackievirus A16 and poliovirus immunizations in humans and animals

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 11, 2015, Pages 2723-2733

  Mao, Qunying ^a   Wang, Yiping ^a   Shao, Jie ^a   Ying, Zhifang ^a   Gao, Fan ^a   Yao, Xin ^a   Li, Changgui ^a   Ye, Qiang ^a   Xu, Miao ^a   Li, Rongcheng ^b   Zhu, Fengcai ^c   Liang, Zhenglun ^a  

^a NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

^b Guangxi Zhuang Autonomous Region Center for Disease Control and Prevention   (China)

^c JIANGSU PROVINCIAL CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Coxsackievirus A16 (CA16); Enterovirus 71 (EV71); Foot, and mouth disease (HFMD); Hand; Neutralizing antibody (NTAb); Poliovirus; Vaccine

Indexed keywords

INACTIVATED EV71; INACTIVATED VACCINE; INACTIVATED VIRUS VACCINE; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; PLACEBO; VIRUS ANTIBODY; VIRUS VACCINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; COXSACKIEVIRUS A16; CYTOPATHOGENIC EFFECT; ENTEROVIRUS 71; FEMALE; GENOTYPE; HAND FOOT AND MOUTH DISEASE; HUMAN; IMMUNIZATION; MOUSE; NEUROLOGICAL COMPLICATION; NONHUMAN; PATHOGENESIS; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PHASE 3 CLINICAL TRIAL; POLIOMYELITIS VIRUS; RHABDOMYOSARCOMA CELL; SEROCONVERSION; VACCINATION; VACCINATION REACTION; ADOLESCENT; ADULT; ANIMAL; BLOOD; CHILD; CLINICAL TRIAL; ENTEROVIRUS; ENTEROVIRUS A; HAND, FOOT AND MOUTH DISEASE; IMMUNOLOGY; INFANT; MALE; MIDDLE AGED; POLIOMYELITIS; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CHILD; CHILD, PRESCHOOL; ENTEROVIRUS; ENTEROVIRUS A, HUMAN; FEMALE; HAND, FOOT AND MOUTH DISEASE; HUMANS; IMMUNIZATION SCHEDULE; INFANT; MALE; MICE; MIDDLE AGED; PLACEBOS; POLIOMYELITIS; POLIOVIRUS; VACCINES, INACTIVATED; VIRAL VACCINES; YOUNG ADULT;

EID: 84983486003     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1011975     Document Type: Article

References (56)

1. Abu Bakar S, Chan YF, Lam SK. Outbreaks of enterovirus 71 infection. N Engl J Med 2000; 342:355-6; PMID:10660400; http://dx.doi.org/10.1056/NEJM200002033420513
2. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 2010; 10(11):778-90; PMID:20961813; http://dx.doi.org/10.1016/S1473-3099(10)70194-8
3. Ooi MH, Wong SC, Lewth waite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 2010; 9:1097-105; PMID:20965438; http://dx.doi.org/10.1016/S1474-4422(10)70209-X
4. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shih SR. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N Engl J Med 1999; 341:929-35; PMID:10498487; http://dx.doi.org/10.1056/NEJM199909233411301
5. McMinn P, Lindsay K, Perera D, Chan HM, Chan KP, Cardosa MJ. Phylogenetic analysis of enterovirus 71 strains isolated during linked epidemics in Malaysia, Singapore, and Western Australia. J Virol 2001; 75:7732-8; PMID:11462047; http://dx.doi.org/10.1128/JVI.75.16.7732-7738.2001
6. Lee MS, Chang LY. Development of enterovirus 71 vaccines. Expert Rev Vaccines 2010; 9:149-56; PMID:20109026; http://dx.doi.org/10.1586/erv.09.152
7. Tan X, Huang X, Zhu S, Chen H, Yu Q, Wang H, Huo X, Zhou J, Wu Y, Yan D, et al. The persistent circulation of enterovirus 71 in People’s Republic of China: causing emerging nationwide epidemics since 2008. PLoS One 2011; 6(9):e25662; PMID:21980521; http://dx.doi.org/10.1371/journal.pone.0025662
8. Li YP, Liang ZL, Gao Q, Huang LR, Mao QY, Wen SQ, Liu Y, Yin WD, Li RC, Wang JZ. Safety and immunogenicity of a novel human Enterovirus 71 (EV71) vaccine: a randomized, placebo-controlled, double-blind, Phase I clinical trial. Vaccine 2012; 30 (22):3295-303; PMID:22426327; http://dx.doi.org/10.1016/j.vaccine.2012.03.010
9. Li YP, Liang ZL, Xia JL, Wu JY, Wang L, Song LF, Mao QY, Wen SQ, Huang RG, Hu YS, et al. Immunogenicity, safety, and immune persistence of a novel inactivated human enterovirus 71 vaccine: a phase II, Randomized, double-blind, placebo-controlled Trial. J Infect Dis 2014; 209(1):46-55; http://dx.doi.org/10.1093/infdis/jit429
10. Zhu F, Xu W, Xia J, Liang Z, Liu Y, Zhang X, Tan X, Wang L, Mao Q, Wu J, et al. Efficacy, safety, and immunogenicity of an enterovirus 71 vaccine in China. N Engl J Med 2014; 370(9):818-28; http://dx.doi.org/10.1056/NEJMoa1304923
11. Zhu FC, Wang JZ, Li XL, Liang ZL, Ge HM, Meng FY, Mao QY, Zhang YT, Zhang ZY, Ji H, et al. Reactogenicity and immunogenicity of an enterovirus 71 vaccine in chinese healthy children and infants. Pediatr Infect Dis J 2012; 31 (11):1158-65; PMID:22926209; http://dx.doi.org/10.1097/INF.0b013e31826eba74
12. Zhu FC, Liang ZL, Li XL, Ge HM, Meng FY, Mao QY, Zhang YT, Hu YM, Zhang ZY, Li JX, et al. Immunogenicity and safety of an enterovirus 71 vaccine in healthy Chinese children and infants: a randomised, double-blind, placebo-controlled phase 2 clinical trial. Lancet 2013; 381(9871):1037-45.
13. Zhu FC, Meng FY, Li JX, Li XL, Mao QY, Tao H, Zhang YT, Yao X, Chu K, Chen QH, et al. Efficacy, safety, and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in China: a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 2013; 381(9882):2024-32; http://dx.doi.org/10.1016/S0140-6736(13)61049-1
14. Liu L, Zhang Y, Wang J, Zhao H, Jiang L, Che Y, Shi H, Li R, Mo Z, Huang T, et al. Study of the integrated immune response induced by an inactivated EV71 vaccine. PLoS One 2013; 8(1): e54451
15. Li R, Liu L, Mo Z, Wang X, Xia J, Liang Z, Zhang Y, Li Y, Mao Q, Wang J, et al. An inactivated enterovirus 71 vaccine in healthy children. N Engl J Med 2014; 370(9):829-37; http://dx.doi.org/10.1056/NEJMoa1303224
16. Van Regenmortel MHV, Fauquet CM, Bishop DHL, Carsten EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, et al. (Eds.), Virus Taxonomy. Classification and Nomenclature of Viruses. Seventh Report of the ICTV. New York: Academic Press, 2000:657-73.
17. Juhela S, Hyoty H, Lonnrot M, Roivainen M, Simell O, Ilonen J.1998. Enterovirus infections and enterovirus specific T-cell responses ininfancy. J Med Virol 54:226-32; PMID:9515773; http://dx.doi.org/10.1002/(SICI)1096-9071(199803)54:3%3c226::AID-JMV14%3e3.0.CO;2-F
18. Liu W, Wu S, Xiong Y, Li T, Wen Z, Yan M, Qin K, Liu Y, Wu J. Co-circulation and genomic recombination of coxsackievirus A16 and enterovirus 71 during a large outbreak of hand, foot, and mouth disease in Central China. PLoS One 2014; 9(4):e96051; PMID:24776922; http://dx.doi.org/10.1371/journal.pone.0096051
19. Li L, He Y, Yang H, Zhu J, Xu X, Dong J, Zhu Y, Jin Q. Genetic characteristics of human enterovirus 71 and coxsackievirus A16 circulating from 1999 to 2004 in Shenzhen, People’s Republic of China. J Clin Microbiol 2005; 43:3835-9; PMID:16081920; http://dx.doi.org/10.1128/JCM.43.8.3835-3839.2005
20. Oberste MS, Maher K, Kilpatrick DR, Pallansch MA. Molecular evolution 432 of the human enteroviruses: correlation of serotype with VP1 sequence and 433 application to picornavirus classification. J Virol 1999; 73:1941-8; PMID:9971773
21. Yao X, Mao QY, He P, Zhou C, Zhu XF, Zhang W, Lu FM, Liang ZL, Li FX, Wang JZ. Genetic characteristics of coxsakievirus A16 complete genome isolated in Beijing, 2008. 2010, 31(12):1437-38.
22. World heaith organization. WHO recommendations for routine immunization–summary tables. http://www.who.int/immunization/policy/immunization_schedules/en/
23. Cello J, Strannegård O, Svennerholm B. A study of the cellular immune response to enteroviruses in humans: identification of cross-reactive T cell epitopes on the structural proteins of enteroviruses. J Gen Virol 1996; 77:2097-108; PMID:8811009; http://dx.doi.org/10.1099/0022-1317-77-9-2097
24. Samuelson A, Forsgren M, Johansson B, Wahren B, Sällberg M. Molecular basis for serological cross-reactivity between enteroviruses. Clin Diagn Lab Immunol 1994; 1:336-41; PMID:7496972
25. Lin Y, Wen K, Pan Y, Wang Y, Che X, Wang B. Crossreactivity of anti-EV71 IgM and neutralizing antibody in series sera of patients infected with Enterovirus 71 and Coxsackievirus A 16. J Immunoassay Immunochem 2011; 32(3):233-43; PMID:21574094; http://dx.doi.org/10.1080/15321819.2011.559297
26. Chou AH, Liu CC, Chang JY, Jiang R, Hsieh YC, Tsao A, Wu CL, Huang JL, Fung CP, Hsieh SM, et al. Formalin-inactivated EV71 vaccine candidate induced cross-neutralizing antibody against subgenotypes B1, B4, B5 and C4A in adult volunteers. PLoS One 2013; 8(11):e79783. e Collection 2013; http://dx.doi.org/10.1371/journal.pone.0079783
27. Leng Q, Yang C, Zhu K, Deng C, Zhu L, Wan J. Preexisting heterologous immunity to poliovirus vaccination may mitigate severity of hand, food and mouth disease caused by EV71. BMC Proceedings 2011; 5 (Suppl 1):P27; http://dx.doi.org/10.1186/1753-6561-5-s1-p27
28. Hovi T, Roivainen M. Peptide antisera targeted to a conserved sequence in poliovirus capsid VP1 cross-react widely with members of the genus Enterovirus. JClin-Microbiol 1993; 31(5):1083-7.
29. Tan S, Tan X, Sun X, Lu G, Chen CC, Yan J, Liu J, Xu W, Gao GF. VP2 dominated CD4C T cell responses against enterovirus 71 and cross-reactivity against coxsackievirus A16 and polioviruses in a healthy population. J Immunol 2013; 191(4):1637-47; http://dx.doi.org/10.4049/jimmunol.1301439
30. Wu TC, Wang YF, Lee YP, Wang JR, Liu CC, Wang SM, Lei HY, Su IJ, Yu CK. Immunity to avirulent enterovirus 71 and coxsackie A16 virus protects against enterovirus 71 infection in mice. J Virol 2007; 81(19):10310-5. Epub 2007 Jul 11; http://dx.doi.org/10.1128/JVI.00372-07
31. Lin Y, Wen K, Pan Y, Wang Y, Che X, Wang B. Crossreactivity of anti-EV71 IgM and neutralizing antibody in series sera of patients infected with Enterovirus 71 and Coxsackievirus A 16. J Immunoassay Immunochem 2011; 32(3):233-43; PMID:21574094; http://dx.doi.org/10.1080/15321819.2011.559297
32. Zhang HM, Li CR, Liu YJ, Liu WL, Fu D, Xu LM, Xie JJ, Tan Y, Wang H, Chen XC, et al. To investigate pathogen of hand, foot and mouth disease in Shenzhen in 2008. Chin J Exp Clin Virol 2009; 23:334-6; PMID:20387478
33. Pan H, Zhu YF, Qi X, Zhang YJ, Li L, Deng F, Wu B, Wang SJ, Zhu FC, Wang H. Analysis on the epidemiological and genetic characteristics of enterovirustype 71 and Coxsackie A16 virus infection in Jiangsu, China. Zhonghua Liu Xing Bing XueZaZhi 2009; 30:339-43; PMID:19731523
34. Ferson MJ, Bell SM. Outbreak of CoxsackievirusA16 hand, foot, and mouth disease in a child day care center. Am J Public Health 1991; 81:1675-6; PMID:1746672; http://dx.doi.org/10.2105/AJPH.81.12.1675
35. Bendig JW, Fleming DM. Epidemiological, virological, and clinical features of an epidemic of hand, foot, and mouth disease in England and Wales. Commun Dis Rep CDR Rev 1996; 6:R81-6; PMID:8664928
36. Chang LY. Enterovirus 71 in Taiwan. Pediatr Neonatol 2008; 49:103-12; PMID:19054914; http://dx.doi.org/10.1016/S1875-9572(08)60023-6
37. Ang LW, Koh BK, Chan KP, Chua LT, James L, Goh KT. Epidemiology and control of hand, foot and mouth disease in Singapore, 2001-2007. Ann Acad Med Singapore 2009; 38:106-12; PMID:19271036
38. Zhu J, Luo Z, Wang J, Xu Z, Chen H, Fan D, Gao N, Ping G, Zhou Z, Zhang Y, et al. Phylogenetic analysis of Enterovirus 71 circulating in Beijing, China from 2007 to 2009. PLoS One 2013; 8:e56318; PMID:23418551; http://dx.doi.org/10.1371/journal.pone.0056318
39. Wang J, Qi S, Zhang X, Zhang Y, Liu L, Che Y, He Z, Zhao Y, Lu S, Yu W, Li Q. Coxsackievirus A 16 infection does not interfere with the specific immune response induced by an enterovirus 71 inactivated vaccine in rhesus monkeys. Vaccine 2014; 32 (35):4436-42. doi: 10.1016/j.vaccine.2014.06.062.
40. Arita I, Nakane M, Fenner F. Public health. Is polio eradication realistic? Science 2006; 312(5775):852-4; http://dx.doi.org/10.1126/science.1124959
41. World Health Organization. 2012, Posting date. Polio case count. http://apps.who.int/immunization_monitoring/en/diseases/poliomyelitis/afpextract.cfm
42. Luo HM, Zhang Y, Wang XQ, Yu WZ, Wen N, Yan DM, Wang HQ, Wushouer F, Wang HB, Xu AQ, et al. Identification and control of a poliomyelitis outbreak in Xinjiang, China. N Engl J Med 2013; 369(21):1981-90; http://dx.doi.org/10.1056/NEJMoa1303368
43. Deng C, Yang C, Wan J, Zhu L, Leng Q. Irregular poliovirus vaccination correlates to pulmonary edema of hand, foot, and mouth disease. Clin Vaccine Immunol 2011; 18(9): 1589-90. Epub 2011 Jul 13; http://dx.doi.org/10.1128/CVI.05132-11
44. Aylward B, Tangermann R. The global polio eradication initiative: lessons learned and prospects for success. Vaccine 2011; 29: Suppl 4:D80-D85; http://dx.doi.org/10.1016/j.vaccine.2011.10.005
45. Minor PD, Ferguson M, Evans DM, Almond JW, Icenogle JP. Antigenic structure of polioviruses of serotypes 1, 2 and 3. J Gen Virol 1986; 67(Pt 7):1283-91; PMID:2425046; http://dx.doi.org/10.1099/0022-1317-67-7-1283
46. Emini EA, Jameson BA, Lewis AJ, Larsen GR, Wimmer E. Polio virus neutralization epitopes: analysis and localization with neutralizing monoclonal antibodies. J Virol 1982; 43(3):997-1005.
47. Lentz KN, Smith AD, Geisler SC, Cox S, Buontempo P, Skelton A, DeMartino J, Rozhon E, Schwartz J, Girijavallabhan V, et al. Structure of poliovirus type 2 Lansing complexed with antiviral agent SCH48973: comparison of the structural and biological properties of three poliovirus serotypes. Structure 1997; 5(7):961-78; PMID:9261087; http://dx.doi.org/10.1016/S0969-2126(97)00249-9
48. Page GS, Mosser AG, Hogle JM, Filman DJ, Rueckert RR, Chow M. Three-dimensional structure of poliovirus serotype 1 neutralizing determinants. J Virol 1988; 62(5):1781-94; PMID:2451757
49. Foo DG, Alonso S, Phoon MC, Ramachandran NP, Chow VT, Poh CL. Identification of neutralizing linear epitopes from the VP1 capsid protein of Enterovirus 71 using synthetic peptides. Virus Res 2007; 125(1):61-8; PMID:17222936; http://dx.doi.org/10.1016/j.virusres.2006.12.005
50. Lee H, Cifuente JO, Ashley RE, Conway JF, Makhov AM, Tano Y, Shimizu H, Nishimura Y, Hafenstein S. A strain-specific epitope of Enterovirus 71 identified by cryoEM of the complex with Fab from neutralizing antibody. J Virol 2013; 87(21):11363-70; PMID:23946455; http://dx.doi.org/10.1128/JVI.01926-13
51. Liu CC, Chou AH, Lien SP, Lin HY, Liu SJ, Chang JY, Guo MS, Chow YH, Yang WS, Chang KH, et al. Identification and characterization of a cross-neutralization epitope of Enterovirus71. Vaccine 2011; 29(26):4362-72; http://dx.doi.org/10.1016/j.vaccine.2011.04.010
52. Lim XF, Jia Q, Khong WX, Yan B, Premanand B, Alonso S, Chow VT, Kwang J. Characterization of an isotype-dependent monoclonal antibody against linear neutralizing epitope effective for prophylaxis of enterovirus 71 infection. PLoS One 2012; 7(1):e29751. Epub 2012 Jan 18; PMID:22279543; http://dx.doi.org/10.1371/journal.pone.0029751
53. Kirk K, Poh CL, Fecondo J, Pourianfar H, Shaw J, Grollo L. Cross-reactive neutralizing antibody epitopes against Enterovirus 71 identified by an in silicoapproach. Vaccine 2012; 30(Nov (49)):7105-10; PMID:23022400; http://dx.doi.org/10.1016/j.vaccine.2012.09.030
54. Shi J, Huang X, Liu Q, Huang Z. Identification of conserved neutralizing linear epitopes within the VP1 protein of coxsackievirus A16. Vaccine 2013; 31 (17):2130-6; http://dx.doi.org/10.1016/j.vaccine.2013.02.051
55. Liang Z, Mao Q, Gao Q, Li X, Dong C, Yu X, Yao X, Li F, Yin W, Li Q, et al. Establishing China’s national standards of antigen content and neutralizing antibody responses for evaluation of enterovirus 71 (EV71) vaccines. Vaccine 2011; 29: 9668-74; PMID:22015395; http://dx.doi.org/10.1016/j.vaccine.2011.10.018
56. WHO Department of Immunization, Vaccines and Biologicals. Polio laboratory manual. 4th ed. Geneva: World Health Organization, 2004. (WHO/IVB/04.10.).