First seroepidemiological investigation of human enterovirus 71 in Iran
-
Mahsa Javadi
,
Ahmad Nejati
,
Maryam Yousefi
,
Mahmood Mahmoodi
,
Zabihollah Shoja
,
Shohreh Shahmahmoodi
Abstract
Background and Objectives: Human Enterovirus 71 (EV-A71) is the causative agent for many dermal to neurological diseases especially polio-like paralysis outbreaks around the world. This study, the first of this kind in Iran, aimed to find neutralizing antibodies against EV-A71 in serum of healthy individuals in different age groups based on neutralization test (NT).
Materials and Methods: In this cross-sectional study, 547 serum samples were collected from healthy individuals who were referring for routine checkup tests (aged from under 6 months to over 31 years old) to Imam-Khomeini Hospital in Tehran during January-December 2015. Serum samples were examined by NT in cell culture to detect neutralizing antibodies against EV-A71. In the next step, some of the positive samples were subjected to complete titration to determine the exact titer of anti-EV-A71 antibodies.
Results: Of 547 samples, 310 (56.7%) were positive for EV-A71 neutralizing antibody. The presence of the antibody increased with age (p<0.001), and there was a significant statistical relationship between sex and the presence of antibody (p=0.009).
Conclusion: Our results demonstrated an apparent but limited circulation of EV-A71 in our society. After the worldwide eradication of poliovirus, EV-A71 which can cause polio-likes syndrome, might be the new challenge for our health care system as regard more in depth research is however needed.
1. Yip CC, Lau SK, Woo PC, Yuen KY. Human enterovirus 71 epidemics: what's next? Emerg Health Threats J 2013; 6:19780.
2. Ryu WS, Kang B, Hong J, Hwang S, Kim J, Cheon DS. Clinical and etiological characteristics of enterovirus 71-related diseases during a recent 2-year period in Korea. J Clin Microbiol 2010; 48:2490-2494.
3. Knipe DM, Howley P (2013). Fields Virology. 6th ed. Wolters Kluwer Health/Lippincott Williams & Wilkins (LWW). Philadelphia.
4. Sabanathan S, Tan le V, Thwaites L, Wills B, Qui PT, Rogier van Doorn H. Enterovirus 71 related severe hand, foot and mouth disease outbreaks in South-East Asia: current situation and ongoing challenges. J Epidemiol Community Health 2014; 68:500-502.
5. Yi EJ, Shin YJ, Kim JH, Kim TG, Chang SY. Enterovirus 71 infection and vaccines. Clin Exp Vaccine Res 2017; 6:4-14.
6. van der Sanden S, Koopmans M, Uslu G, van der Avoort H; Dutch working group for clinical virology. epidemiology of enterovirus 71 in the Netherlands, 1963 to 2008. J Clin Microbiol 2009; 47:2826-2833.
7. Li HG, Lao Q. The pulmonary complications associated with EV71-infected hand–foot–mouth disease. Radiol Infect Dis 2017; 4:137-142.
8. Eggertson L. Infectious disease experts monitor outbreaks of enterovirus 71 in Asia. CMAJ 2012; 184(15):E781-782.
9. Chang PC, Chen SC, Chen KT. The current status of the disease caused by enterovirus 71 infections: epidemiology, pathogenesis, molecular epidemiology, and vaccine development. Int J Environ Res Public Health 2016; 13:890.
10. Chen M, Ju Y, Chen M, Xie Z, Zhou K, Tan Y, Mo J. Epidemiological and genetic characteristics of EV71 in hand, foot, and mouth disease in Guangxi, southern China, from 2010 to 2015. PLoS One 2017; 12(12):e0188640.
11. Kim HJ, Hyeon JY, Hwang S, Lee YP, Lee SW, Yoo JS, et al. Epidemiology and virologic investigation of human enterovirus 71 infection in the Republic of Korea from 2007 to 2012: a nationwide cross-sectional study. BMC Infect Dis 2016; 16:425.
12. Tan CY, Gonfrier G, Ninove L, Zandotti C, Dubot-Pérès A, de Lamballerie X, et al. Screening and detection of human enterovirus 71 infection by a real‐time RT‐PCR assay in Marseille, France, 2009–2011. Clin Microbiol Infect 2012; 18(4):E77-E80.
13. Rahimi P, Mahdian Naser H, Sohrabi A. The association of non-polio enteroviruses with aseptic meningitis in children in Iran. J Med Microbiol Infect Dis 2014; 2:56-60.
14. Rahimi P, Roohandeh A, Sohrabi A, Mostafavi E, Bahram Ali G. Impact of human enterovirus 71 genotypes in meningoencephalitis in Iran. Jundishapur J Microbiol 2015; 8(12):e27113.
15. Roohandeh A, Rahimi P, Sohrabi A, Mobasheri M, Azadmanesh K, Shahosseini Z, et al. Frequency of human enterovirus 71 in children under 8 years old with aseptic menengitis in Tehran. Clin Lab 2013; 59:915-920.
16. Shahmahmoodi S, Mehrabi Z, Eshraghian MR, Azad TM, Tabatabaie H, Yousefi M, et al. First detection of enterovirus 71 from an acute flaccid paralysis case with residual paralysis in Iran. J Clin Virol 2008; 42:409-411.
17. Chang LY, King CC, Hsu KH, Ning HC, Tsao KC, Li CC, et al. Risk factors of enterovirus 71 infection and associated hand, foot, and mouth disease/herpangina in children during an epidemic in Taiwan. Pediatrics 2002; 109(6):e88-e88.
18. Akya A, Elahi A, Moghoofei M, Chegenelorestani R, Nejati A, Babaei F. Enterovirus detection in patients suspected aseptic meningitis by RT-PCR in Kermanshah, Iran. J Kerman Univ Med Sci 2018; 25:18-26.
19. Wang JX, Zhu SL, Wang J, Lin Y, Pei YW, Sun DP, et al. Seroprevalence of enterovirus A71 and coxsackievirus A16 in healthy people in Shandong province, China. PLoS One 2016; 11(9):e0162373.
20. Yang C, Deng C, Wan J, Zhu L, Leng Q. Neutralizing antibody response in the patients with hand, foot and mouth disease to enterovirus 71 and its clinical implications. Virol J 2011; 8:306.
21. Zhu R, Cheng T, Yin Z, Liu D, Xu L, Li Y, et al. Serological survey of neutralizing antibodies to eight major enteroviruses among healthy population. Emerg Microbes Infect 2018; 7:2.
22. van der Sanden S, van Eek J, Martin DP, van der Avoort H, Vennema H, Koopmans M. Prediction of protection against Asian enterovirus 71 outbreak strains by cross-neutralizing capacity of serum from Dutch donors, the Netherlands. Emerg Infect Dis 2016; 22:1562-1569.
23. Mizuta K, Aoki Y, Suto A, Ootani K, Katsushima N, Itagaki T, et al. Cross-antigenicity among EV71 strains from different genogroups isolated in Yamagata, Japan, between 1990 and 2007. Vaccine 2009; 27:3153-3158.
24. World Health Organization. (2004). Polio laboratory manual, 4th ed. World Health Organization. Geneva, Switzerland: WHO Document Production Services.
25. Yousefi M, Nejati A, Zahraei SM, Mahmoudi S, Parhizgari N, Farsani SMJ, et al. Enteroviruses and adenoviruses in stool specimens of paralytic children-can they be the cause of paralysis? Iran J Microbiol 2018; 10:194-201.
26. Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 2010; 9:1097-1105.
27. Rasti M, Rastegarvand N, Makvandi M, Teimoori A, Azaran A. Co-circulation of echovirus 6 and 30 with coxsackievirus A6 among children with hand, foot, and mouth disease in Ahvaz, Southwest Iran. Arch Clin Infect Dis 2019; 14(3):e83522.
28. Lerdsamran H, Prasertsopon J, Mungaomklang A, Klinmalai C, Noisumdaeng P, Sangsiriwut K, et al. Seroprevalence of antibodies to enterovirus 71 and coxsackievirus A16 among people of various age groups in a northeast province of Thailand. Virol J 2018; 15:158.
29. Liu B, Luo L, Yan S, Wen T, Bai W, Li H, et al. Clinical features for mild hand, foot and mouth disease in China. PLoS One 2015; 10(8):e0135503.
30. Martínez-López N, Muñoz-Almagro C, Launes C, Navascués A, Imaz-Pérez M, Reina J, et al. Surveillance for enteroviruses associated with hand, foot, and mouth disease, and other mucocutaneous symptoms in spain, 2006–2020. Viruses 2021; 13:781.
31. Song C, Li Y, Zhou Y, Liang L, Turtle L, Wang F, et al. Enterovirus genomic load and disease severity among children hospitalised with hand, foot and mouth disease. EBioMedicine 2020; 62:103078.
32. Luo ST, Chiang PS, Chao AS, Liou GY, Lin R, Lin TY, et al. Enterovirus 71 maternal antibodies in infants, Taiwan. Emerg Infect Dis 2009; 15:581.
2. Ryu WS, Kang B, Hong J, Hwang S, Kim J, Cheon DS. Clinical and etiological characteristics of enterovirus 71-related diseases during a recent 2-year period in Korea. J Clin Microbiol 2010; 48:2490-2494.
3. Knipe DM, Howley P (2013). Fields Virology. 6th ed. Wolters Kluwer Health/Lippincott Williams & Wilkins (LWW). Philadelphia.
4. Sabanathan S, Tan le V, Thwaites L, Wills B, Qui PT, Rogier van Doorn H. Enterovirus 71 related severe hand, foot and mouth disease outbreaks in South-East Asia: current situation and ongoing challenges. J Epidemiol Community Health 2014; 68:500-502.
5. Yi EJ, Shin YJ, Kim JH, Kim TG, Chang SY. Enterovirus 71 infection and vaccines. Clin Exp Vaccine Res 2017; 6:4-14.
6. van der Sanden S, Koopmans M, Uslu G, van der Avoort H; Dutch working group for clinical virology. epidemiology of enterovirus 71 in the Netherlands, 1963 to 2008. J Clin Microbiol 2009; 47:2826-2833.
7. Li HG, Lao Q. The pulmonary complications associated with EV71-infected hand–foot–mouth disease. Radiol Infect Dis 2017; 4:137-142.
8. Eggertson L. Infectious disease experts monitor outbreaks of enterovirus 71 in Asia. CMAJ 2012; 184(15):E781-782.
9. Chang PC, Chen SC, Chen KT. The current status of the disease caused by enterovirus 71 infections: epidemiology, pathogenesis, molecular epidemiology, and vaccine development. Int J Environ Res Public Health 2016; 13:890.
10. Chen M, Ju Y, Chen M, Xie Z, Zhou K, Tan Y, Mo J. Epidemiological and genetic characteristics of EV71 in hand, foot, and mouth disease in Guangxi, southern China, from 2010 to 2015. PLoS One 2017; 12(12):e0188640.
11. Kim HJ, Hyeon JY, Hwang S, Lee YP, Lee SW, Yoo JS, et al. Epidemiology and virologic investigation of human enterovirus 71 infection in the Republic of Korea from 2007 to 2012: a nationwide cross-sectional study. BMC Infect Dis 2016; 16:425.
12. Tan CY, Gonfrier G, Ninove L, Zandotti C, Dubot-Pérès A, de Lamballerie X, et al. Screening and detection of human enterovirus 71 infection by a real‐time RT‐PCR assay in Marseille, France, 2009–2011. Clin Microbiol Infect 2012; 18(4):E77-E80.
13. Rahimi P, Mahdian Naser H, Sohrabi A. The association of non-polio enteroviruses with aseptic meningitis in children in Iran. J Med Microbiol Infect Dis 2014; 2:56-60.
14. Rahimi P, Roohandeh A, Sohrabi A, Mostafavi E, Bahram Ali G. Impact of human enterovirus 71 genotypes in meningoencephalitis in Iran. Jundishapur J Microbiol 2015; 8(12):e27113.
15. Roohandeh A, Rahimi P, Sohrabi A, Mobasheri M, Azadmanesh K, Shahosseini Z, et al. Frequency of human enterovirus 71 in children under 8 years old with aseptic menengitis in Tehran. Clin Lab 2013; 59:915-920.
16. Shahmahmoodi S, Mehrabi Z, Eshraghian MR, Azad TM, Tabatabaie H, Yousefi M, et al. First detection of enterovirus 71 from an acute flaccid paralysis case with residual paralysis in Iran. J Clin Virol 2008; 42:409-411.
17. Chang LY, King CC, Hsu KH, Ning HC, Tsao KC, Li CC, et al. Risk factors of enterovirus 71 infection and associated hand, foot, and mouth disease/herpangina in children during an epidemic in Taiwan. Pediatrics 2002; 109(6):e88-e88.
18. Akya A, Elahi A, Moghoofei M, Chegenelorestani R, Nejati A, Babaei F. Enterovirus detection in patients suspected aseptic meningitis by RT-PCR in Kermanshah, Iran. J Kerman Univ Med Sci 2018; 25:18-26.
19. Wang JX, Zhu SL, Wang J, Lin Y, Pei YW, Sun DP, et al. Seroprevalence of enterovirus A71 and coxsackievirus A16 in healthy people in Shandong province, China. PLoS One 2016; 11(9):e0162373.
20. Yang C, Deng C, Wan J, Zhu L, Leng Q. Neutralizing antibody response in the patients with hand, foot and mouth disease to enterovirus 71 and its clinical implications. Virol J 2011; 8:306.
21. Zhu R, Cheng T, Yin Z, Liu D, Xu L, Li Y, et al. Serological survey of neutralizing antibodies to eight major enteroviruses among healthy population. Emerg Microbes Infect 2018; 7:2.
22. van der Sanden S, van Eek J, Martin DP, van der Avoort H, Vennema H, Koopmans M. Prediction of protection against Asian enterovirus 71 outbreak strains by cross-neutralizing capacity of serum from Dutch donors, the Netherlands. Emerg Infect Dis 2016; 22:1562-1569.
23. Mizuta K, Aoki Y, Suto A, Ootani K, Katsushima N, Itagaki T, et al. Cross-antigenicity among EV71 strains from different genogroups isolated in Yamagata, Japan, between 1990 and 2007. Vaccine 2009; 27:3153-3158.
24. World Health Organization. (2004). Polio laboratory manual, 4th ed. World Health Organization. Geneva, Switzerland: WHO Document Production Services.
25. Yousefi M, Nejati A, Zahraei SM, Mahmoudi S, Parhizgari N, Farsani SMJ, et al. Enteroviruses and adenoviruses in stool specimens of paralytic children-can they be the cause of paralysis? Iran J Microbiol 2018; 10:194-201.
26. Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 2010; 9:1097-1105.
27. Rasti M, Rastegarvand N, Makvandi M, Teimoori A, Azaran A. Co-circulation of echovirus 6 and 30 with coxsackievirus A6 among children with hand, foot, and mouth disease in Ahvaz, Southwest Iran. Arch Clin Infect Dis 2019; 14(3):e83522.
28. Lerdsamran H, Prasertsopon J, Mungaomklang A, Klinmalai C, Noisumdaeng P, Sangsiriwut K, et al. Seroprevalence of antibodies to enterovirus 71 and coxsackievirus A16 among people of various age groups in a northeast province of Thailand. Virol J 2018; 15:158.
29. Liu B, Luo L, Yan S, Wen T, Bai W, Li H, et al. Clinical features for mild hand, foot and mouth disease in China. PLoS One 2015; 10(8):e0135503.
30. Martínez-López N, Muñoz-Almagro C, Launes C, Navascués A, Imaz-Pérez M, Reina J, et al. Surveillance for enteroviruses associated with hand, foot, and mouth disease, and other mucocutaneous symptoms in spain, 2006–2020. Viruses 2021; 13:781.
31. Song C, Li Y, Zhou Y, Liang L, Turtle L, Wang F, et al. Enterovirus genomic load and disease severity among children hospitalised with hand, foot and mouth disease. EBioMedicine 2020; 62:103078.
32. Luo ST, Chiang PS, Chao AS, Liou GY, Lin R, Lin TY, et al. Enterovirus 71 maternal antibodies in infants, Taiwan. Emerg Infect Dis 2009; 15:581.
| Files | ||
| Issue | Vol 13 No 4 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i4.6975 | |
| Keywords | ||
| Iran; Human enterovirus 71; Seroepidemiological investigation; Neutralization test | ||
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How to Cite
1.
Javadi M, Nejati A, Yousefi M, Mahmoodi M, Shoja Z, Shahmahmoodi S. First seroepidemiological investigation of human enterovirus 71 in Iran. Iran J Microbiol. 2021;13(4):502-508.
