Seroprevalence of enterovirus 71 antibody among children in China: A systematic review and meta-analysis

Pediatric Infectious Disease Journal

Volumn 34, Issue 12, 2015, Pages 1399-1406

  Yang, Bingyi ^a   Wu, Peng ^a   Wu, Joseph T ^a   Lau, Eric H Y ^a   Leung, Gabriel M ^a   Yu, Hongjie ^b   Cowling, Benjamin J ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

children; enterovirus; meta analysis; seroprevalence

Indexed keywords

ENTEROVIRUS 71 ANTIBODY; MATERNAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS VACCINE;

ANTIBODY DETECTION; BLOOD SAMPLING; CHILD; CHINA; ENTEROVIRUS 71; ENTEROVIRUS INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GEOGRAPHY; HAND FOOT AND MOUTH DISEASE; HUMAN; IMMUNITY; INFECTION RISK; META ANALYSIS; NEWBORN; PHYSICAL EXAMINATION; PRIORITY JOURNAL; REVIEW; SEROPREVALENCE; SYSTEMATIC REVIEW; ADOLESCENT; ENTEROVIRUS A; HAND, FOOT AND MOUTH DISEASE; INFANT; PRESCHOOL CHILD;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; CHINA; ENTEROVIRUS A, HUMAN; HAND, FOOT AND MOUTH DISEASE; HUMANS; INFANT; INFANT, NEWBORN; SEROEPIDEMIOLOGIC STUDIES;

EID: 84944350840     PISSN: 08913668     EISSN: 15320987     Source Type: Journal    
DOI: 10.1097/INF.0000000000000900     Document Type: Review

References (84)

1. Lee MS, Lin TY, Chiang PS, An investigation of epidemic enterovirus 71 infection in Taiwan, 2008: clinical, virologic, and serologic features. Pediatr Infect Dis J 2010 29 1030 1034
2. Chan LG, Parashar UD, Lye MS, Deaths of children during an outbreak of hand, foot, and mouth disease in sarawak, malaysia: clinical and pathological characteristics of the disease. For the Outbreak Study Group. Clin Infect Dis 2000 31 678 683
3. Shimizu H, Utama A, Yoshii K, Enterovirus 71 from fatal and nonfatal cases of hand, foot and mouth disease epidemics in Malaysia, Japan and Taiwan in 1997-1998. Jpn J Infect Dis 1999 52 12 15
4. Wu Y, Yeo A, Phoon MC, The largest outbreak of hand; foot and mouth disease in Singapore in 2008: the role of enterovirus 71 and coxsackievirus A strains. Int J Infect Dis 2010 14 e1076 e1081
5. Ishimaru Y, Nakano S, Yamaoka K, Outbreaks of hand, foot, and mouth disease by enterovirus 71. High incidence of complication disorders of central nervous system. Arch Dis Child 1980 55 583 588
6. Solomon T, Lewthwaite P, Perera D, Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 2010 10 778 790
7. Xing W, Liao Q, Viboud C, Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis 2014 14 308 318
8. Cardosa MJ, Krishnan S, Tio PH, Isolation of subgenus B adenovirus during a fatal outbreak of enterovirus 71-Associated hand, foot, and mouth disease in Sibu, Sarawak. Lancet 1999 354 987 991
9. Hsueh C, Jung SM, Shih SR, Acute encephalomyelitis during an outbreak of enterovirus type 71 infection in Taiwan: report of an autopsy case with pathologic, immunofluorescence, and molecular studies. Mod Pathol 2000 13 1200 1205
10. National notifiable disease situation in 2014. Available at: http://www.nhfpc.gov.cn. Accessed May 9 2015
11. Li L, Yin H, An Z, Considerations for developing an immunization strategy with enterovirus 71 vaccine. Vaccine 2015 33 1107 1112
12. Chong P, Liu CC, Chow YH, Review of enterovirus 71 vaccines. Clin Infect Dis 2015 60 797 803
13. Zhu FC, Meng FY, Li JX, 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 2024 2032
14. Li R, Liu L, Mo Z, An inactivated enterovirus 71 vaccine in healthy children. N Engl J Med 2014 370 829 837
15. Zhu F, Xu W, Xia J, Efficacy, safety, and immunogenicity of an enterovirus 71 vaccine in China. N Engl J Med 2014 370 818 828
16. Huang XY, Liu GH, Chen HM, [Seroepidemiological study of enterovirus 71 in Henan province]. Zhongguo Bing Yuan Sheng Wu Xue Za Zhi 2010 5 617 639
17. Xu MH, [Pathogen Composition Causing Hand Foot and Mouth Disease (HFMD) and Seroepidemiology of Enterovirus 71 Infection in Shanghai, China] 2012 Shanghai: Fudan University
18. Wilson EB, Probable inference, the law of succession, and statistical inference. J Am Stat Assoc 1927 22 209 212
19. Newcombe RG, Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 1998 17 857 872
20. Shamseer L, Moher D, Clarke M, PRISMA-P Group Preferred reporting items for systematic review and meta-Analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 2015 349 g7647
21. Egger M, Smith GD, Bias in location and selection of studies. BMJ 1998 316 61 66
22. Hedges LV, Vevea JL, Fixed-And random-effects models in meta-Analysis. Psycholog Methods 1998 3 486 504
23. Higgins JP, Thompson SG, Deeks JJ, Measuring inconsistency in meta-Analyses. BMJ 2003 327 557 560
24. Cochran WG, The combination of estimates from different experiments. Biometrics 1954 10 101 129
25. Viechtbauer W, Conducting meta-Analyses in R with the meta for package. J Stat Software 2010 36 1 48
26. Zhu FC, Liang ZL, Meng FY, Retrospective study of the incidence of HFMD and seroepidemiology of antibodies against EV71 and CoxA16 in prenatal women and their infants. PLoS One 2012 7 e37206
27. Guo XB, Zhu SL, Wang DY, [Seroepidemiology investigation of HEV71 in healthy children of 1-6 years old in three counties of China in 2005]. Zhongguo Yi Miao He Mian Yi 2009 15 141 144
28. Xu WG, Wang YL, [Seroepidemiological study of Enterovirus 71 infection in children aged 1 through 6 years in Changzhou in 2006]. Shi Yong Yu Fang Yi Xue 2013 20 179 180
29. Mao QY, Yang ZW, Yu X, [Epidemic tendency of neutralizing antibody against Enterovirus 71 and Coxsackievirus A 16 in infants in rural area of Kaifeng City, Henan Province, China]. Zhongguo Sheng Wu Zhi Pin Xue Za Zhi 2009 22 911 922
30. Zhou SL, Li LL, He YQ, [Serological epidemiology investigation of Enterovirus type 71 infection in Shenzhen]. Re Dai Yi Xue Za Zhi 2007 7 66 67
31. Deng HL, Ma SW, Mi B, [Survey on Enterovirus subclinical infection of healthy children in Xi'an]. Yi Xue Lin Chuang Yan Jiu 2012 29 204 208
32. Mao QY, Liao XY, Yu X, Dynamic change of mother-source neutralizing antibodies against enterovirus 71 and coxsackievirus A16 in infants. Chin Med J (Engl) 2010 123 1679 1684
33. Ni H, Yi B, Yin J, Epidemiological and etiological characteristics of hand, foot, and mouth disease in Ningbo, China, 2008-2011. J Clin Virol 2012 54 342 348
34. Zhu FC, Liang ZL, Li XL, 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 1037 1045
35. Yu H, Wang M, Chang H, Prevalence of antibodies against enterovirus 71 in children from Lu'an City in Central China. Jpn J Infect Dis 2011 64 528 532
36. Zhu FC, Wang JZ, Li XL, Reactogenicity and immunogenicity of an enterovirus 71 vaccine in Chinese healthy children and infants. Pediatr Infect Dis J 2012 31 1158 1165
37. Zhu Z, Zhu S, Guo X, Retrospective seroepidemiology indicated that human enterovirus 71 and coxsackievirus A16 circulated wildly in central and southern China before large-scale outbreaks from 2008. Virol J 2010 7 300
38. Li YP, Liang ZL, Gao Q, Safety and immunogenicity of a novel human Enterovirus 71 (EV71) vaccine: a randomized, placebo-controlled, double-blind, Phase I clinical trial. Vaccine 2012 30 3295 3303
39. Zeng M, El Khatib NF, Tu S, Seroepidemiology of Enterovirus 71 infection prior to the 2011 season in children in Shanghai. J Clin Virol 2012 53 285 289
40. Li W, Yi L, Su J, Seroepidemiology of human enterovirus71 and coxsackievirusA16 among children in Guangdong province, China. BMC Infect Dis 2013 13 322
41. Ji H, Li L, Liu Y, Seroepidemiology of human enterovirus71 and coxsackievirusA16 in Jiangsu province, China. Virol J 2012 9 248
42. Li W, Yi L, Su J, Seroprevalence of human enterovirus 71 and coxsackievirus A16 in Guangdong, China, in pre-And post-2010 HFMD epidemic period. PLoS One 2013 8 e80515
43. Bai YS, Yang AN, Zhang J, [Survey on prevalence of EV71 and ECHO infection among population received physical examination in Yinchuan City]. Ningxia Yi Ke Da Xue Xue Bao 2012 34 453 455
44. Ding Q, Zhu FC, Li L, [Serum epidemiology survey of HEV 71 among children in Ganyu County]. Jiangsu Yu Fang Yi Xue 2011 22 4 6
45. Hou HB, Zhou HT, Zeng HS, [IgG antibody levels in healthy people of Futian District of Shenzhen City]. Zhi Ye Yu Jian Kang 2012 28 3107 3108
46. Liu FR, Liu Q, Li G, [Seroepidemiology study on EV71 infection among healthy children in Longgang District, Shenzhen City]. Hua Nan Yu Fang Yi Xue 2013 39 40 46
47. Liao YH, Chen QJ, Liao LH, [Seroepidemiology study on Enterovirus 71 in Longyan City]. Hai Xia Yu Fang Yi Xue Za Zhi 2012 18 28 30
48. Zhang DX, Yang F, Wang B, [Subclinical infection of hand-foot-mouth disease in Shenzhen City]. Zhongguo Re Dai Yi Xue 2011 11 1332 1333
49. Zhu W, Ju LW, Jiang LF, [Serum levels of antibody against enterovirus 71 in healthy children at Shanghai in 2011]. Zhonghua Chuan Ran Bing Za Zhi 2013 31 650 653
50. Li JM, Xu YJ, Wang QY, [Investigation of enterovirus 71 antibody levels among children in the Longgang District, City of Shenzhen]. Zhongguo Bing Yuan Sheng Wu Xue Za Zhi 2012 7 924 926
51. Li JM, Zhang Y, Gao L, [Seroepidemiology investigation of neutralizing antibody against enterovirus 71 among healthy people in Tianjin]. Zhonghua Liu Xing Bing Xue Za Zhi 2011 32 568 570
52. Yang XH, Yan YS, [Cause of HFMD epidemic caused by HEV71 in Fujian Province: seroepidemiology and molecular epidemiology of HEV71]. 10th Conference on Epidemiology in Eastern China, Hefei, China. In
53. Xiong Y, Gong T, Shi Y, [Seroepidemiology investigation on HEV71 in the population in Nanchang in early 2010]. Xian Dai Yu Fang Yi Xue 2013 40 7 10
54. Cai MS, Ren Y, [Investigation on HFMD recessive infection in healthy population in some community of Shenzhen in 2012]. Zhongguo Wei Sheng Jian Yan 2013 23 2355 2357
55. Zhao SC, Zhang SJ, Yue JN, [Seroepidemiologic investigation of HEV71 among children in Xining city]. Zhongguo Gong Gong Wei Sheng 2011 27 361 362
56. Kuang L, Wang CB, Liang ZF, [Investigation on enterovirus 71 antibody levels among children in Guangzhou area]. Zhongguo Xun Zheng Er Ke Za Zhi 2011 6 211 214
57. Guo RL, Deng J, Li Yx, [Serum epidemiological study of HFMD in Handan, 2009]. Zhongguo Bing Yuan Sheng Wu Xue Za Zhi 2011 6 848 850
58. Chen XL, Wen SQ, Wei D, [Survey on level of antibody against EV71 and Cox A 16 among children aged 0 to 15 in Mengshan County]. Yi Yao Qian Yan 2012 2 115 116
59. Chen XQ, Zhang ZY, Pang HY, [Monitoring and analysis of the levels of neutralizing antibody against enterovirus 71 in individuals under the age of 15 in Donghai County]. Xian Dai Yu Fang Yi Xue 2013 40 3875 3877
60. Lin XW, Xie RN, Zeng C, [Investigation of Human Enterovirus 71 infection among clinical cases and healthy people in Chaoshan District]. Yi Xue Jian Yan Yu Lin Chuang 2007 18 66 67
61. Chen RL, Pan RY, Lai ZF, [The microneutralization assay for the detection of neutralizing antibodies against EV71 and CV A 16 among healthy population]. Zhongguo Yu Fang Yi Xue Za Zhi 2013 14 362 365
62. Hu YM, Wang X, Wang JZ, Immunogenicity, safety, and lot consistency of a novel inactivated enterovirus 71 vaccine in Chinese children aged 6 to 59 months. Clin Vaccine Immunol 2013 20 1805 1811
63. Li ZF, Liu TX, Yang GP, [Seroepidemiological investigation on enterovirus 71 among children in Lipu County, Guangxi in 2010]. Ying Yong Yu Fang Yi Xue 2013 19 281 283
64. Ooi EE, Phoon MC, Ishak B, Seroepidemiology of human enterovirus 71, Singapore. Emerg Infect Dis 2002 8 995 997
65. Tran CB, Nguyen HT, Phan HT, The seroprevalence and seroincidence of enterovirus71 infection in infants and children in Ho Chi Minh City, Viet Nam. PLoS One 2011 6 e21116
66. Linsuwanon P, Puenpa J, Huang SW, Epidemiology and seroepidemiology of human enterovirus 71 among Thai populations. J Biomed Sci 2014 21 16
67. Luo ST, Chiang PS, Chao AS, Enterovirus 71 maternal antibodies in infants, Taiwan. Emerg Infect Dis 2009 15 581 584
68. Ang LW, Phoon MC, Wu Y, The changing seroepidemiology of enterovirus 71 infection among children and adolescents in Singapore. BMC Infect Dis 2011 11 270
69. Diedrich S, Weinbrecht A, Schreier E, Seroprevalence and molecular epidemiology of enterovirus 71 in Germany. Arch Virol 2009 154 1139 1142
70. Rabenau HF, Richter M, Doerr HW, Hand, foot and mouth disease: seroprevalence of Coxsackie A16 and Enterovirus 71 in Germany. Med Microbiol Immunol 2010 199 45 51
71. Chang LY, King CC, Hsu KH, Risk factors of enterovirus 71 infection and associated hand, foot, and mouth disease/herpangina in children during an epidemic in Taiwan. Pediatrics 2002 109 e88
72. Lu CY, Lee CY, Kao CL, Incidence and case-fatality rates resulting from the 1998 enterovirus 71 outbreak in Taiwan. J Med Virol 2002 67 217 223
73. Akhmadishina LV, Eremeeva TP, Trotsenko OE, Seroepidemiology and molecular epidemiology of enterovirus 71 in Russia. PLoS One 2014 9 e97404
74. Zhang Y, Tan XJ, Wang HY, An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J Clin Virol 2009 44 262 267
75. Zhang Y, Zhu Z, Yang W, An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J 2010 7 94
76. Hu M, Li Z, Wang J, Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS One 2012 7 e38978
77. Feng H, Duan G, Zhang R, Time series analysis of hand-foot-mouth disease hospitalization in Zhengzhou: establishment of forecasting models using climate variables as predictors. PLoS One 2014 9 e87916
78. Deng T, Huang Y, Yu S, Spatial-Temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong Province, China. PLoS One 2013 8 e56943
79. Mao LX, Wu B, Bao WX, Epidemiology of hand, foot, and mouth disease and genotype characterization of Enterovirus 71 in Jiangsu, China. J Clin Virol 2010 49 100 104
80. Pan Z, Trikalinos TA, Kavvoura FK, Local literature bias in genetic epidemiology: an empirical evaluation of the Chinese literature. PLoS Med 2005 2 e334
81. Xu F, Yan Q, Wang H, Performance of detecting IgM antibodies against enterovirus 71 for early diagnosis. PLoS One 2010 5 e11388
82. Wendelboe AM, Van Rie A, Salmaso S, Duration of immunity against pertussis after natural infection or vaccination. Pediatr Infect Dis J 2005 24 S58 S61
83. Waaijenborg S, Hahné SJ, Mollema L, Waning of maternal antibodies against measles, mumps, rubella, and varicella in communities with contrasting vaccination coverage. J Infect Dis 2013 208 10 16
84. Leuridan E, Hens N, Hutse V, Early waning of maternal measles antibodies in era of measles elimination: longitudinal study. BMJ 2010 340 c1626