Epidemiological Characteristics of Hand, Foot and Mouth Disease Reinfection in Guangzhou, Southern China from 2012 to 2017
-
Xuan Zhong
,
Hui Wang
,
Chun Chen
,
Xiaoni Zou
,
Tiegang Li
Abstract
Background: Hand, foot and mouth disease (HFMD) reinfection is common because of the limited cross-protection from infections of different enterovirus. We aimed to investigate the epidemiological characteristics and its influential factors of HFMD reinfection in Guangzhou, China.
Methods: Data on HFMD patients aged ≤5 yr from 2012 to 2017 were extracted from surveillance system. Influential factors of reinfection were assessed using the logistic regression model.
Results: Of 369,054 HFMD patients, 11,321 patients (3.07%) were classified as reinfection. The reinfection rate in male was higher than in female (χ2=60.11, P<0.001). The reinfection rate in patients ≤1 yr was 3.86%, which showed a downward trend with age (Z=37.37, Ptrend<0.001). The highest reinfection rate was observed in the scattered children (3.38%), followed by nursery care children and others (χ2=514.75, P<0.001). Besides, higher risk of reinfection was detected among those who were male, lower age group, rural residence and other enteroviruses infection compared with their respective counterparts. Seasonality was illustrated according to the number of reinfections peaked from April to July. Time intervals curves revealed the number of reinfections gradually increased after 13 months from the initial infection.
Conclusion: Male ≤4 yr, living rural area, especially those lived scattered and infected with other enteroviruses were more likely to be reinfection.
1. Guerra AM, Waseem M (2019). Hand Foot and Mouth Disease. In: StatPearls. edn. Treasure Island (FL).
2. Li XW, Ni X, Qian SY, et al (2018). Chinese guidelines for the diagnosis and treat-ment of hand, foot and mouth disease (2018 edition). World J Pediatr, 14(5):437-447.
3. Koh WM, Bogich T, Siegel K, et al (2016). The Epidemiology of Hand, Foot and Mouth Disease in Asia: A Systematic Re-view and Analysis. Pediatr Infect Dis J, 35(10):e285-300.
4. Liu SL, Pan H, Liu P, et al (2015). Compara-tive epidemiology and virology of fatal and nonfatal cases of hand, foot and mouth disease in mainland China from 2008 to 2014. Rev Med Virol, 25(2):115-128.
5. Deng T, Huang Y, Yu S, et al (2013). Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the dis-trict level in Guangdong Province, China. PLoS One, 8(2):e56943.
6. Wang J, Hu T, Sun D, et al (2017). Epidemi-ological characteristics of hand, foot, and mouth disease in Shandong, China, 2009-2016. Sci Rep, 7(1):8900.
7. Li T, Yang Z, Di B, et al (2014). Hand-foot-and-mouth disease and weather factors in Guangzhou, southern China. Epidemiol Infect, 142(8):1741-1750.
8. Xiao X, Gasparrini A, Huang J, et al (2017). The exposure-response relationship be-tween temperature and childhood hand, foot and mouth disease: A multicity study from mainland China. Environ Int, 100:102-109.
9. Mao QY, Wang Y, Bian L, et al (2016). EV71 vaccine, a new tool to control out-breaks of hand, foot and mouth disease (HFMD). Expert Rev Vaccines, 15(5):599-606.
10. Zhu FC, Meng FY, Li JX, et al (2013). Effi-cacy, safety, and immunology of an inac-tivated alum-adjuvant enterovirus 71 vac-cine in children in China: a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet, 381(9882):2024-2032.
11. Li R, Liu L, Mo Z, et al (2014). An inactivat-ed enterovirus 71 vaccine in healthy chil-dren. N Engl J Med, 370(9):829-837.
12. Huang J, Liao Q, Ooi MH, et al (2018). Epi-demiology of Recurrent Hand, Foot and Mouth Disease, China, 2008-2015. Emerg Infect Dis, 24(3):432-442.
13. Dang LX, Wang C, Bao WB, et al (2018). A Meta-analysis of recurrent infections prevalence of hand-foot-and-mouth dis-ease among children in China. Chin J Sch Health, 39(3):411-414.
14. Chen GP, Wu JB, Wang JJ, et al (2016). Ep-idemiological characteristics and influen-tial factors of hand, foot and mouth dis-ease (HFMD) reinfection in children in Anhui province. Epidemiol Infect, 144(1):153-160.
15. Xie Z, Wang L, Yan Y, et al (2014). [A co-hort study on the characteristics of the recurrent epidemics on hand, foot and mouth disease, in Fujian province]. Zhong-hua Liu Xing Bing Xue Za Zhi, 35(10):1109-1114.
16. Xing W, Liao Q, Viboud C, et al (2014). Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis, 14(4):308-318.
17. The Chinese Ministry of Health (2010). The Guidelines for The Prevention and Con-trol of HFMD (2009 edition). Chinese Prac-tical Journal of Rural Doctor, 16: 125-127.
18. Peng Y, Yu B, Kong DG, et al (2018). Rein-fection hazard of hand-foot-mouth dis-ease in Wuhan, China, using Cox-proportional hazard model. Epidemiol In-fect, 146(10):1337-1342.
19. Xiao-Hong J, Qian LI (2017). Characteristic analysis of the repeated infection cases with hand-footand-mouth disease (HFMD) in Chaoyang District of Beijing City between 2008 and 2014. Modern Pre-ventive Medicine.
20. Shi C, Liu J, Shi P, et al (2018). Epidemio-logical characteristics and influential fac-tors of hand, foot, and mouth disease re-infection in Wuxi, China, 2008-2016. BMC Infect Dis, 18(1):472.
21. Zhou ZM, Xu Y, Hu CS, et al (2017). Epi-demiological Features of Hand, Foot and Mouth Disease during the Period of 2008-14 in Wenzhou, China. J Trop Pedi-atr, 63(3):182-188.
22. Zhu G, Xiao J, Zhang B, et al (2018). The spatiotemporal transmission of dengue and its driving mechanism: A case study on the 2014 dengue outbreak in Guang-dong, China. Sci Total Environ, 622-623:252-259.
23. Xu B, Tian H, Sabel CE, et al (2019). Im-pacts of Road Traffic Network and Soci-oeconomic Factors on the Diffusion of 2009 Pandemic Influenza A (H1N1) in Mainland China. Int J Environ Res Public Health, 16(7):1223.
24. Land area and population density in various districts of Guangzhou (2017). http://www.gzstats.gov.cn/gzstats/gzsq/201701/1036f733bf244636b9b62af6f9a504f1.shtml
25. Xie YH, Chongsuvivatwong V, Tan Y, et al (2015). Important roles of public play-grounds in the transmission of hand, foot, and mouth disease. Epidemiol Infect, 143(7):1432-1441.
26. Tian H, Zhang Y, Sun Q, et al (2014). Preva-lence of multiple enteroviruses associated with hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China: outbreaks of coxsackieviruses a10 and b3. PLoS One, 9(1):e84233.
27. Luo L, Xing W, Liao Q, et al (2015). [Re-search progress on seroepidemiological study of enterovirus 71 and cox-sackievirus A16 infection among chil-dren]. Zhonghua Yu Fang Yi Xue Za Zhi, 49(2):184-188.
28. Zhang D, Chen Y, Chen X, et al (2017). Enterovirus 71 Neutralizing Antibodies Seroepidemiological Research among Children in Guangzhou, China between 2014 and 2015: A Cross-Sectional Study. Int J Environ Res Public Health, 14(3):319.
29. Zhang D, Li Z, Zhang W, et al (2016). Hand-Washing: The Main Strategy for Avoiding Hand, Foot and Mouth Dis-ease. Int J Environ Res Public Health, 13(6):610.
30. Zhao D, Wang L, Cheng J, et al (2017). Im-pact of weather factors on hand, foot and mouth disease, and its role in short-term incidence trend forecast in Huainan City, Anhui Province. Int J Biometeorol, 61(3):453-461.
31. Zhang Q, Zhou M, Yang Y, et al (2019). Short-term effects of extreme meteoro-logical factors on childhood hand, foot, and mouth disease reinfection in Hefei, China: A distributed lag non-linear analy-sis. Sci Total Environ, 653:839-848.
32. Solomon T, Lewthwaite P, Perera D, et al (2010). Virology, epidemiology, patho-genesis, and control of enterovirus 71. Lancet Infect Dis, 10(11):778-790.
33. Yang Y, You E, Wu J, et al (2018). Effects of relative humidity on childhood hand, foot, and mouth disease reinfection in Hefei, China. Sci Total Environ, 630:820-826.
34. Cheng Q, Bai L, Zhang Y, et al (2018). Am-bient temperature, humidity and hand, foot, and mouth disease: A systematic re-view and meta-analysis. Sci Total Environ, 625:828-836.
35. Eames KT (2014). The influence of school holiday timing on epidemic impact. Epi-demiol Infect, 142(9):1963-1971.
36. Li JX, Song YF, Wang L, et al (2016). Two-year efficacy and immunogenicity of Si-novac Enterovirus 71 vaccine against hand, foot and mouth disease in chil-dren. Expert Rev Vaccines, 15(1):129-137.
37. Takahashi S, Liao Q, Van Boeckel TP, et al (2016). Hand, Foot, and Mouth Disease in China: Modeling Epidemic Dynamics of Enterovirus Serotypes and Implica-tions for Vaccination. PLoS Med, 13(2):e1001958.
38. Zhang Y, Tan X, Cui A, et al (2013). Com-plete genome analysis of the C4 sub-genotype strains of enterovirus 71: pre-dominant recombination C4 viruses per-sistently circulating in China for 14 years. PLoS One, 8(2):e56341.
39. Huang ML, Chiang PS, Chia MY, et al (2013). Cross-reactive neutralizing anti-body responses to enterovirus 71 infec-tions in young children: implications for vaccine development. PLoS Negl Trop Dis, 7(2):e2067.
40. Blomqvist S, Klemola P, Kaijalainen S, et al (2010). Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. J Clin Virol, 48(1):49-54.
41. Mirand A, Henquell C, Archimbaud C, et al (2012). Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infec-tions in 2010, France: a large citywide, prospective observational study. Clin Mi-crobiol Infect, 18(5):E110-118.
2. Li XW, Ni X, Qian SY, et al (2018). Chinese guidelines for the diagnosis and treat-ment of hand, foot and mouth disease (2018 edition). World J Pediatr, 14(5):437-447.
3. Koh WM, Bogich T, Siegel K, et al (2016). The Epidemiology of Hand, Foot and Mouth Disease in Asia: A Systematic Re-view and Analysis. Pediatr Infect Dis J, 35(10):e285-300.
4. Liu SL, Pan H, Liu P, et al (2015). Compara-tive epidemiology and virology of fatal and nonfatal cases of hand, foot and mouth disease in mainland China from 2008 to 2014. Rev Med Virol, 25(2):115-128.
5. Deng T, Huang Y, Yu S, et al (2013). Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the dis-trict level in Guangdong Province, China. PLoS One, 8(2):e56943.
6. Wang J, Hu T, Sun D, et al (2017). Epidemi-ological characteristics of hand, foot, and mouth disease in Shandong, China, 2009-2016. Sci Rep, 7(1):8900.
7. Li T, Yang Z, Di B, et al (2014). Hand-foot-and-mouth disease and weather factors in Guangzhou, southern China. Epidemiol Infect, 142(8):1741-1750.
8. Xiao X, Gasparrini A, Huang J, et al (2017). The exposure-response relationship be-tween temperature and childhood hand, foot and mouth disease: A multicity study from mainland China. Environ Int, 100:102-109.
9. Mao QY, Wang Y, Bian L, et al (2016). EV71 vaccine, a new tool to control out-breaks of hand, foot and mouth disease (HFMD). Expert Rev Vaccines, 15(5):599-606.
10. Zhu FC, Meng FY, Li JX, et al (2013). Effi-cacy, safety, and immunology of an inac-tivated alum-adjuvant enterovirus 71 vac-cine in children in China: a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet, 381(9882):2024-2032.
11. Li R, Liu L, Mo Z, et al (2014). An inactivat-ed enterovirus 71 vaccine in healthy chil-dren. N Engl J Med, 370(9):829-837.
12. Huang J, Liao Q, Ooi MH, et al (2018). Epi-demiology of Recurrent Hand, Foot and Mouth Disease, China, 2008-2015. Emerg Infect Dis, 24(3):432-442.
13. Dang LX, Wang C, Bao WB, et al (2018). A Meta-analysis of recurrent infections prevalence of hand-foot-and-mouth dis-ease among children in China. Chin J Sch Health, 39(3):411-414.
14. Chen GP, Wu JB, Wang JJ, et al (2016). Ep-idemiological characteristics and influen-tial factors of hand, foot and mouth dis-ease (HFMD) reinfection in children in Anhui province. Epidemiol Infect, 144(1):153-160.
15. Xie Z, Wang L, Yan Y, et al (2014). [A co-hort study on the characteristics of the recurrent epidemics on hand, foot and mouth disease, in Fujian province]. Zhong-hua Liu Xing Bing Xue Za Zhi, 35(10):1109-1114.
16. Xing W, Liao Q, Viboud C, et al (2014). Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis, 14(4):308-318.
17. The Chinese Ministry of Health (2010). The Guidelines for The Prevention and Con-trol of HFMD (2009 edition). Chinese Prac-tical Journal of Rural Doctor, 16: 125-127.
18. Peng Y, Yu B, Kong DG, et al (2018). Rein-fection hazard of hand-foot-mouth dis-ease in Wuhan, China, using Cox-proportional hazard model. Epidemiol In-fect, 146(10):1337-1342.
19. Xiao-Hong J, Qian LI (2017). Characteristic analysis of the repeated infection cases with hand-footand-mouth disease (HFMD) in Chaoyang District of Beijing City between 2008 and 2014. Modern Pre-ventive Medicine.
20. Shi C, Liu J, Shi P, et al (2018). Epidemio-logical characteristics and influential fac-tors of hand, foot, and mouth disease re-infection in Wuxi, China, 2008-2016. BMC Infect Dis, 18(1):472.
21. Zhou ZM, Xu Y, Hu CS, et al (2017). Epi-demiological Features of Hand, Foot and Mouth Disease during the Period of 2008-14 in Wenzhou, China. J Trop Pedi-atr, 63(3):182-188.
22. Zhu G, Xiao J, Zhang B, et al (2018). The spatiotemporal transmission of dengue and its driving mechanism: A case study on the 2014 dengue outbreak in Guang-dong, China. Sci Total Environ, 622-623:252-259.
23. Xu B, Tian H, Sabel CE, et al (2019). Im-pacts of Road Traffic Network and Soci-oeconomic Factors on the Diffusion of 2009 Pandemic Influenza A (H1N1) in Mainland China. Int J Environ Res Public Health, 16(7):1223.
24. Land area and population density in various districts of Guangzhou (2017). http://www.gzstats.gov.cn/gzstats/gzsq/201701/1036f733bf244636b9b62af6f9a504f1.shtml
25. Xie YH, Chongsuvivatwong V, Tan Y, et al (2015). Important roles of public play-grounds in the transmission of hand, foot, and mouth disease. Epidemiol Infect, 143(7):1432-1441.
26. Tian H, Zhang Y, Sun Q, et al (2014). Preva-lence of multiple enteroviruses associated with hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China: outbreaks of coxsackieviruses a10 and b3. PLoS One, 9(1):e84233.
27. Luo L, Xing W, Liao Q, et al (2015). [Re-search progress on seroepidemiological study of enterovirus 71 and cox-sackievirus A16 infection among chil-dren]. Zhonghua Yu Fang Yi Xue Za Zhi, 49(2):184-188.
28. Zhang D, Chen Y, Chen X, et al (2017). Enterovirus 71 Neutralizing Antibodies Seroepidemiological Research among Children in Guangzhou, China between 2014 and 2015: A Cross-Sectional Study. Int J Environ Res Public Health, 14(3):319.
29. Zhang D, Li Z, Zhang W, et al (2016). Hand-Washing: The Main Strategy for Avoiding Hand, Foot and Mouth Dis-ease. Int J Environ Res Public Health, 13(6):610.
30. Zhao D, Wang L, Cheng J, et al (2017). Im-pact of weather factors on hand, foot and mouth disease, and its role in short-term incidence trend forecast in Huainan City, Anhui Province. Int J Biometeorol, 61(3):453-461.
31. Zhang Q, Zhou M, Yang Y, et al (2019). Short-term effects of extreme meteoro-logical factors on childhood hand, foot, and mouth disease reinfection in Hefei, China: A distributed lag non-linear analy-sis. Sci Total Environ, 653:839-848.
32. Solomon T, Lewthwaite P, Perera D, et al (2010). Virology, epidemiology, patho-genesis, and control of enterovirus 71. Lancet Infect Dis, 10(11):778-790.
33. Yang Y, You E, Wu J, et al (2018). Effects of relative humidity on childhood hand, foot, and mouth disease reinfection in Hefei, China. Sci Total Environ, 630:820-826.
34. Cheng Q, Bai L, Zhang Y, et al (2018). Am-bient temperature, humidity and hand, foot, and mouth disease: A systematic re-view and meta-analysis. Sci Total Environ, 625:828-836.
35. Eames KT (2014). The influence of school holiday timing on epidemic impact. Epi-demiol Infect, 142(9):1963-1971.
36. Li JX, Song YF, Wang L, et al (2016). Two-year efficacy and immunogenicity of Si-novac Enterovirus 71 vaccine against hand, foot and mouth disease in chil-dren. Expert Rev Vaccines, 15(1):129-137.
37. Takahashi S, Liao Q, Van Boeckel TP, et al (2016). Hand, Foot, and Mouth Disease in China: Modeling Epidemic Dynamics of Enterovirus Serotypes and Implica-tions for Vaccination. PLoS Med, 13(2):e1001958.
38. Zhang Y, Tan X, Cui A, et al (2013). Com-plete genome analysis of the C4 sub-genotype strains of enterovirus 71: pre-dominant recombination C4 viruses per-sistently circulating in China for 14 years. PLoS One, 8(2):e56341.
39. Huang ML, Chiang PS, Chia MY, et al (2013). Cross-reactive neutralizing anti-body responses to enterovirus 71 infec-tions in young children: implications for vaccine development. PLoS Negl Trop Dis, 7(2):e2067.
40. Blomqvist S, Klemola P, Kaijalainen S, et al (2010). Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. J Clin Virol, 48(1):49-54.
41. Mirand A, Henquell C, Archimbaud C, et al (2012). Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infec-tions in 2010, France: a large citywide, prospective observational study. Clin Mi-crobiol Infect, 18(5):E110-118.
| Files | ||
| Issue | Vol 51 No 9 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v51i9.10563 | |
| Keywords | ||
| Hand foot and mouth disease Enterovirus Reinfection Epidemiology | ||
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How to Cite
1.
Zhong X, Wang H, Chen C, Zou X, Li T. Epidemiological Characteristics of Hand, Foot and Mouth Disease Reinfection in Guangzhou, Southern China from 2012 to 2017. Iran J Public Health. 2022;51(9):2078-2088.
