Global epidemiology of Enterovirus 71

Future Virology

Volumn 4, Issue 5, 2009, Pages 501-510

  Tong, C Y William ^a,b   Bible, Jon M ^c  

^a ST THOMAS HOSPITAL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GSTS Pathology   (United Kingdom)

Author keywords

Encephalitis; Enterovirus 71; Epidemiology; Genogroups; Hand, foot and mouth disease; Host factors; Meningitis

Indexed keywords

ASIA; BRAIN STEM; CELLULAR IMMUNITY; CEREBROSPINAL FLUID ANALYSIS; COXSACKIE VIRUS A; DISEASE ASSOCIATION; DISEASE SEVERITY; DISEASE SURVEILLANCE; EARLY DIAGNOSIS; ENCEPHALITIS; ENTEROVIRUS 71; ENVIRONMENTAL FACTOR; EPIDEMIC; FLACCID PARALYSIS; GENETIC VARIABILITY; HAND FOOT AND MOUTH DISEASE; HERD IMMUNITY; HUMORAL IMMUNITY; INFECTION CONTROL; MOLECULAR EVOLUTION; NEUROLOGICAL COMPLICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PUBLIC HEALTH; REVIEW; UNINDEXED SEQUENCE; VIRAL GENETICS; VIRUS INFECTION;

HUMAN ENTEROVIRUS 71;

EID: 73849109440     PISSN: 17460794     EISSN: None     Source Type: Journal    
DOI: 10.2217/fvl.09.25     Document Type: Review

References (55)

1. Schmidt NJ, Lennette EH, Ho HH: An apparently new enterovirus isolated from patients with disease of the central nervous system. J. Infect. Dis. 129, 304-309 (1974).
2. Oberste MS, Penaranda S, Maher K, Pallansch MA: Complete genome sequences of all members of the species Human enterovirus A. J. Gen. Virol. 85, 1597-1607 (2004).
3. Witso E, Palacios G, Ronningen KS et al.: Asymptomatic circulation of HEV71 in Norway. Virus Res. 123, 19-29 (2007).
4. Chen KT, Chang HL, Wang ST, Cheng YT, Yang JY: Epidemiologic features of hand-foot-mouth disease and herpangina caused by Enterovirus 71 in Taiwan, 1998-2005. Pediatrics 120, e244-e252 (2007).
5. Chan KP, Goh KT, Chong CY, Teo ES, Lau G, Ling AE: Epidemic hand, foot and mouth disease caused by human Enterovirus 71, Singapore. Emerg. Infect. Dis. 9, 78-85 (2003).
6. Wong KT, Munisamy B, Ong KC et al.: The distribution of inflammation and virus in human Enterovirus 71 encephalomyelitis suggests possible viral spread by neural pathways. J. Neuropathol. Exp. Neurol. 67, 162-169 (2008).
7. Ishimaru Y, Nakano S, Yamaoka K, Takami S: Outbreaks of hand, foot, and mouth disease by Enterovirus 71. High incidence of complication disorders of central nervous system. Arch. Dis. Child. 55, 583-588 (1980).
8. Chumakov M, Voroshilova M, Shindarov L et al.: Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch. Virol. 60, 329-340 (1979).
9. Nagy G, Takatsy S, Kukan E, Mihaly I, Domok I: Virological diagnosis of enterovirus type 71 infections: experiences gained during an epidemic of acute CNS diseases in Hungary in 1978. Arch. Virol. 71, 217-227 (1982).
10. Chan LG, Parashar UD, Lye MS et al.: 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. 31, 678-683 (2000).
11. Ho M, Chen ER, Hsu KH et al.: An epidemic of Enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med. 341, 929-935 (1999).
12. Cardosa MJ, Perera D, Brown BA et al.: Molecular epidemiology of human Enterovirus 71 strains and recent outbreaks in the Asia-Pacific region: comparative analysis of the VP1 and VP4 genes. Emerg. Infect. Dis. 9, 461-468 (2003). ■■ Molecular epidemiology of Enterovirus 71 (EV71) in the Asia-Pacific region from 1997 to 2002.
13. Chua KB, Chua BH, Lee CS et al.: Genetic diversity of Enterovirus 71 isolated from cases of hand, foot and mouth disease in the 1997, 2000 and 2005 outbreaks, Peninsular Malaysia. Malays. J. Pathol. 29, 69-78 (2007).
14. AbuBakar S, Sam IC, Yusof J et al.: Enterovirus 71 outbreak, Brunei. Emerg. Infect. Dis. 15, 79-82 (2009). ■■ Report of an outbreak in Brunei in 2006 due to EV71 genogroup B5. Previous outbreaks in Sarawak in 1997, 2000 and 2003 were due to B3, B4 and B5, respectively. An ancestor of B5 is probably a Singaporean strain from 2000. A total of 1681 cases were reported, with three deaths.
15. Podin Y, Gias EL, Ong F et al.: Sentinel surveillance for human Enterovirus 71 in Sarawak, Malaysia: lessons from the first 7 years. BMC Public Health 6, 180 (2006). ■■ Successful sentinel program in Sarawak after the 1997 outbreak. EV71 outbreaks were occurring every 3 years since 1997. However, genogroup C1 virus behaved like other enterovirus species A viruses and occurred annually.
16. Chen SC, Chang HL, Yan TR, Cheng YT, Chen KT: An eight-year study of epidemiologic features of Enterovirus 71 infection in Taiwan. Am. J. Trop. Med. Hyg. 77, 188-191 (2007).
17. Li L, He Y, Yang H et al.: Genetic characteristics of human Enterovirus 71 and coxsackievirus A16 circulating from 1999 to 2004 in Shenzhen, People's Republic of China. J. Clin. Microbiol. 43, 3835-3839 (2005). ■ A total of 147 samples were collected over 6 years in Shenzhen, China (1999-2004). Of these, 13% were EV71 positive and 28% had Coxsackie A virus (CAV)16.
18. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA: Enterovirus surveillance - United States, 1970-2005. MMWR Surveill. Summ. 55, 1-20 (2006).
19. Kung SH, Wang SF, Huang CW, Hsu CC, Liu HF, Yang JY: Genetic and antigenic analyses of Enterovirus 71 isolates in Taiwan during 1998-2005. Clin. Microbiol. Infect. 13, 782-787 (2007). ■ Evolution of EV71 genogroups within Taiwan, based on viral capsid protein 1 sequencing: 1998 C2, 1999-2003 B4, 2004-2005 C4.
20. Huang YP, Lin TL, Kuo CY et al.: The circulation of subgenogroups B5 and C5 of Enterovirus 71 in Taiwan from 2006 to 2007. Virus Res. 137, 206-212 (2008).
21. Bible JM, Iturriza-Gomara M, Megson B et al.: Molecular epidemiology of human Enterovirus 71 in the United Kingdom from 1998 to 2006. J. Clin. Microbiol. 46, 3192-3200 (2008). ■■ Molecular epidemiology of EV71 in the UK over a 9-year period. Cases were found almost every year, exclusively genogroup C, with C1 more than C2. Clusters corresponded to years and evidence of predated sequences elsewhere is suggestive of an introduction of new strains from time to time.
22. Perez-Velez CM, Anderson MS, Robinson CC et al.: Outbreak of neurologic enterovirus type 71 disease: a diagnostic challenge. Clin. Infect. Dis. 45, 950-957 (2007). ■■ Outbreak of EV71 in Denver, USA from 2003-2005. A total of 16 cases were identified, 56% of whom were less than 6 months old. Only 31.2% detected EV71 in cerebrospinal fluid. Respiratory samples and lower gastrointestinal samples had a higher diagnostic yield.
23. Lin KH, Hwang KP, Ke GM et al.: Evolution of EV71 genogroup in Taiwan from 1998 to 2005: an emerging of subgenogroup C4 of EV71. J. Med. Virol. 78, 254-262 (2006). ■ Report of identification of EV71 genogroup C4 from Taiwan in 2004, which was phylogenetically closer to genotype C4 viruses isolated from China in 1998 and 2000-2004 than those from Japan in 2003-2004.
24. Huemer HP, Ortner B, Huang CW et al.: Isolating Asian Enterovirus 71 subgenogroup C4 in two Austrian clinical samples from 2004. Euro. Surveill. 13, 28 (2008). ■ EV71 genogroup C4 was isolated in an Austrian acute flaccid paralysis surveillance program, suggesting international transmission of EV71.
25. Zhang Y, Tan XJ, Wang HY et al.: An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human Enterovirus 71 in Shandong, China. J. Clin. Virol. 44, 262-272 (2009). ■■ Most recent hand, foot and mouth disease outbreak report from China prior to 2008. A total of 1149 cases were reported in the Shandong province of China, of which 83.9% were confirmed as EV71, 14.9% Coxsackie A virus 16 and one case of Coxsackie B virus 2. Overall mortality was 0.26%. Three lineages were described. Genogroup C4b was the same strain as the one circulating in China from 1998 to 2004. This was replaced by genogroup C4a, which circulated between 2003 and 2008 and was the cause of the outbreak in China in 2008.
26. Qiu J: Enterovirus 71 infection: a new threat to global public health? Lancet Neurol. 7, 868-869 (2008).
27. Hosoya M, Kawasaki Y, Sato M et al.: Genetic diversity of Enterovirus 71 associated with hand, foot and mouth disease epidemics in Japan from 1983 to 2003. Pediatr. Infect. Dis. J. 25, 691-694 (2006).
28. Sanders SA, Herrero LJ, McPhie K et al.: Molecular epidemiology of Enterovirus 71 over two decades in an Australian urban community. Arch. Virol. 151, 1003-1013 (2006). ■ Australian EV71 was mainly genogroup C1 with a recent switch in 2000 and 2001 to genogroup B4. C1 was found in 1980-1990s in Sydney, which was also circulating in the USA in 1987-1995 and the Asia-Pacific region in 1997-2001. Genogroup C2 first appeared in 1995 and then emerged again in 1998. Genogroup B4 appeared between 2000 and 2001.
29. Huang SC, Hsu YW, Wang HC et al.: Appearance of intratypic recombination of Enterovirus 71 in Taiwan from 2002 to 2005. Virus Res. 131, 250-259 (2008).
30. Yoke-Fun C, AbuBakar S: Phylogenetic evidence for inter-typic recombination in the emergence of human Enterovirus 71 subgenotypes. BMC Microbiol. 6, 74 (2006).
31. Siafakas N, Papaventsis D, Levidiotou-Stefanou S, Vamvakopoulos NC, Markoulatos P: Classification and structure of echovirus 5′-UTR sequences. Virus Genes 31, 293-306 (2005). ■ Two genetic clusters of 5′ UTR among enteroviruses - polio-like or nonpolio-like. It was suggested that enteroviruses could freely recombine their 5′UTR region, resulting in covariance - evolutionary pressure favoring structural conservation.
32. Shahmahmoodi S, Mehrabi Z, Eshraghian MR et al.: First detection of Enterovirus 71 from an acute flaccid paralysis case with residual paralysis in Iran. J. Clin. Virol. 42, 409-411 (2008).
33. Castro CM, Cruz AC, Silva EE, Gomes Mde L: Molecular and seroepidemiologic studies of Enterovirus 71 infection in the State of Para, Brazil. Rev. Inst. Med. Trop. Sao Paulo 47, 65-71 (2005).
34. Chakraborty R, Iturriza-Gomara M, Musoke R, Palakudy T, D'Agostino A, Gray J: An epidemic of Enterovirus 71 infection among HIV-1-infected orphans in Nairobi. AIDS 18, 1968-1970 (2004).
35. Mizuta K, Abiko C, Murata T et al.: Frequent importation of Enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J. Clin. Microbiol. 43, 6171-6175 (2005). ■■ Evolution of EV71 genogroups in Yamagata prefecture, Japan, from 1999 to 2003, changing successively from genogroups C2 to B4 to C4 and then B5. Authors attributed the appearance of new strains to importation.
36. Ortner B, Huang CW, Schmid D et al.: Epidemiology of enterovirus types causing neurological disease in Austria 1999-2007: detection of clusters of echovirus 30 and Enterovirus 71 and analysis of prevalent genotypes. J. Med. Virol. 81, 317-324 (2009).
37. Ooi MH, Wong SC, Podin Y et al.: Human Enterovirus 71 disease in Sarawak, Malaysia: a prospective clinical, virological, and molecular epidemiological study. Clin. Infect. Dis. 44, 646-656 (2007). ■■ Prospective study of EV71 in Malaysia from 2000 to 2004. Genogroup B4 was less likely to be associated with CNS complications compared with other genotypes, especially genogroup C1. Genogroup B5 was newly emerged in 2003, and more likely to be part of a family cluster.
38. Cardosa MJ, Krishnan S, Tio PH et al.: Isolation of subgenus B adenovirus during a fatal outbreak of enterovirus 71-associated hand, foot, and mouth disease in Sibu, Sarawak. Lancet 354, 987-991 (1999).
39. Yang TT, Huang LM, Lu CY et al.: Clinical features and factors of unfavorable outcomes for non-polio enterovirus infection of the central nervous system in northern Taiwan, 1994-2003. J. Microbiol. Immunol. Infect. 38, 417-424 (2005).
40. 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 38, 106-112 (2009). ■■ Detailed description of hand, foot and mouth disease outbreaks in Singapore with analysis of risk factors and discussion of public health intervention strategies.
41. Ooi EE, Phoon MC, Ishak B, Chan SH: Seroepidemiology of human Enterovirus 71, Singapore. Emerg. Infect. Dis. 8, 995-997 (2002).
42. Tai WC, Hsieh HJ, Wu MT: Hand, foot and mouth disease in a healthy adult caused by intrafamilial transmission of Enterovirus 71. Br. J. Dermatol. 160, 890-892 (2009).
43. Hamaguchi T, Fujisawa H, Sakai K et al.: Acute encephalitis caused by intrafamilial transmission of Enterovirus 71 in adult. Emerg. Infect. Dis. 14, 828-830 (2008).
44. Ooi MH, Wong SC, Mohan A et al.: Identification and validation of clinical predictors for the risk of neurological involvement in children with hand, foot, and mouth disease in Sarawak. BMC Infect. Dis. 9, 3 (2009). ■■ Three clinical predictors: fever for 3 days or more, 38.5°C or more and lethargy, predicted cerebrospinal fluid pleocytosis. Patients with CNS complication were more likely to be male and Chinese.
45. Chang LY, Chang IS, Chen WJ et al.: HLA-A33 is associated with susceptibility to Enterovirus 71 infection. Pediatrics 122, 1271-1276 (2008).
46. Chang LY, Hsiung CA, Lu CY et al.: Status of cellular rather than humoral immunity is correlated with clinical outcome of Enterovirus 71. Pediatr. Res. 466-471 (2006).
47. Yang KD, Yang MY, Li CC et al.: Altered cellular but not humoral reactions in children with complicated Enterovirus 71 infections in Taiwan. J. Infect. Dis. 183, 850-856 (2001).
48. Ho HY, Cheng ML, Weng SF et al.: Glucose-6-phosphate dehydrogenase deficiency enhances Enterovirus 71 infection. J. Gen. Virol. 89, 2080-2089 (2008).
49. Hsu BM, Chen CH, Wan MT: Genetic diversity of epidemic Enterovirus 71 strains recovered from clinical and environmental samples in Taiwan. Virus Res. 126, 69-75 (2007).
50. Kung CM, King CC, Lee CN, Huang LM, Lee PI, Kao CL: Differences in replication capacity between Enterovirus 71 isolates obtained from patients with encephalitis and those obtained from patients with herpangina in Taiwan. J. Med. Virol. 79, 60-68 (2007).
51. Hagiwara A, Tagaya I, Yoneyama T: Epidemic of hand, foot and mouth disease associated with Enterovirus 71 infection. Intervirology 9, 60-63 (1978).
52. Samuda GM, Chang WK, Yeung CY, Tang PS: Monoplegia caused by Enterovirus 71: an outbreak in Hong Kong. Pediatr. Infect. Dis. J. 6, 206-208 (1987).
53. Bible JM, Pantelidis P, Chan KS, Tong CYW: Genetic evolution of Enterovirus 71: epidemiological and pathological implications. Rev. Med. Virol. 17, 371-379 (2007).
54. International Society for Infectious Diseases - ProMED-mail: a global electronic reporting system for outbreaks of emerging infectious diseases and toxins. www.promedmail.org/ ■■ Extremely useful resources for emerging infectious diseases. Reports very often appear as an outbreak is developing. Most of the recent data on Figure 1 in this paper were collected from ProMED-mail archives.
55. National Center for Biotechnology Information www.ncbi.nlm.nih.gov/