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Molecular Epidemiology of Human Enterovirus 71 Strains and Recent

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Molecular Epidemiology of Human Enterovirus 71 Strains and Recent RESEARCH Molecular Epidemiology of Human Enterovirus 71 Strains and Recent Outbreaks in the Asia-Pacific Region: Comparative Analysis of the VP1 and VP4 Genes Mary Jane Cardosa,* David Perera,* Betty A. Brown,† Doosung Cheon,‡ Hung Ming Chan,* Kwai Peng Chan,§ Haewol Cho,‡ and Peter McMinn¶ This study provides a comprehensive overview of the high mortality in Taiwan in 1998 and 2000 (10,11), have raised molecular epidemiology of human enterovirus 71 (HEV71) in considerable public concern about the virulence of this virus the Asia-Pacific region from 1997 through 2002. Phylogenetic and the disease syndromes most recently attributed to it analysis of the VP4 and VP1 genes of recent HEV71 strains (12–14). indicates that several genogroups of the virus have been circu- Several groups have attempted to describe the molecular lating in the Asia-Pacific region since 1997. The first of these recent outbreaks, described in Sarawak (Malaysian Borneo) in epidemiology of HEV71 in the Asia-Pacific region, and the 1997, was caused by genogroup B3. This outbreak was fol- phylogenetic relationships of recent HEV71 strains to earlier lowed by large outbreaks in Taiwan in 1998, caused by strains from Asia and other parts of the world have been genogroup C2, and in Perth (Western Australia) in 1999, where described (15–19). In the past 4 years, nine publications have viruses belonging to genogroups B3 and C2 cocirculated. presented comparative analyses of HEV71 strains based on Singapore, Taiwan, and Sarawak had HEV71 epidemics in several genome regions (Table 1). Taken together, more than 2000, caused predominantly by viruses belonging to genogroup 250 HEV71 strains isolated from the region between 1997 and B4; however, large numbers of fatalities were observed only in 2002 have been analyzed by different groups. However, gain- Taiwan. HEV71 was identified during an epidemic of hand, foot ing a comprehensive insight into the phylogenetic relationships and mouth disease in Korea; that epidemic was found to be due to viruses constituting a new genogroup, C3. between all these HEV71 strains has been difficult because of the lack of a standardized methodology. The strategies used by each of these groups are summarized in Table 1. uman enterovirus 71 (HEV71) was first isolated in 1969 We sequenced the complete VP1 gene of 66 HEV71 isolates H(1) and is most often associated with outbreaks of the mild from Singapore, Sarawak (Malaysian Borneo), and Perth, childhood exanthem, hand, foot and mouth disease (HFMD) Western Australia, from 1997 to early 2001 (22) and deter- (2). HEV71 is closely related to coxsackie virus A16 (CA16), mined that these recent strains were from the genogroups B and the other major causative agent of HFMD, but unlike CA16, C, based on the nomenclature of Brown et al. (21). In Sarawak HEV71 is also associated with cases of acute neurologic dis- in 1997, isolates from fatal and nonfatal cases all belonged to ease including poliomyelitis-like paralysis, encephalitis, and genogroup B, in a previously undescribed cluster that we have aseptic meningitis (3,4). Although HEV71 outbreaks associat- named B3 (22). Viruses belonging to genogroup B3 were also ed with small numbers of cases of severe neurologic disease isolated in Singapore in 1998, and B3 was the genogroup most were reported in the 1980s in Australia (5), Asia (6), and the commonly identified for viruses isolated in Perth during 1999. United States (4), mortality associated with such outbreaks was However, HEV71 strains isolated from children with severe low, unlike earlier outbreaks in Bulgaria in 1975 (7) and neurologic disease during the Perth epidemic belonged to Hungary in 1978 (8). Twenty years later in 1997, deaths asso- genogroup C2 (22). Another previously undescribed genogroup ciated with epidemics of HEV71-associated HFMD in B cluster (B4) was identified in Singapore in 1997 and contin- Sarawak, Malaysia (9), followed closely by outbreaks with ued to circulate there in 2000 (23) through 2002. Viruses from genogroup B4 were also identified as the primary cause of a *Universiti Malaysia Sarawak, Sarawak, Malaysia; †Centers for large HFMD outbreak in Sarawak in 2000. Disease Control and Prevention, Atlanta, Georgia, USA; ‡National As several regions of the HEV71 genome have been used in Institute of Health, Seoul, Korea; §Singapore General Hospital, Singapore; and ¶Telethon Institute for Child Health Research, Perth, phylogenetic studies, including the VP1 (21,22) and VP4 Western Australia, Australia (15,19) genes and the 5′ untranslated region (5′ UTR) (16,20), Emerging Infectious Diseases • Vol. 9, No. 4, April 2003 461 RESEARCH Table 1. Summary of recent studies of human enterovirus 71 (HEV71) phylogeny No. of nucleotides Reference Gene/ regiona sequenced No. of new strains (source, time) AbuBakar et al., 1999 (20) 5′ UTR 440 13 (Malaysia, 1997) Brown et al., 1999 (21) VP1 891 113 (several countries, 1970–1998) Shimizu et al., 1999 (15) VP4/VP2 420 29 (Malaysia and Japan, 1997; Taiwan, 1998; 5 others (Bulgaria, Hungary, Japan, Taiwan, USA), 1973–1980) Wang et al., 2000 (16) 5′ UTR 681 36 (Taiwan, 1998) Shih et al., 2000 (17) VP1 >500 16 (Taiwan, 1998) Singh et al., 2000 (18) VP1 341 20 (Singapore, Japan, and Peninsular Malaysia, 1997–1998) Chu et al., 2001 (19) VP4 207 20 (Taiwan, 1998); 3 (Taiwan, 1986) McMinn et al., 2001 (22) VP1 891 66 (Sarawak, Singapore, and Perth, 1997–2001) Wang et al., 2002 (11) 5′ UTR VP1 648 841 26, 3, and 19 strains (Taiwan, 1998, 1999, and 2000) were sequenced in the 5′ UTR; 12, 2, and 19 strains (same 3 years) were sequenced in VP1 aUTR, untranslated region. undertaking a comprehensive analysis of the molecular epi- for both strands by using the ABI377 automated DNA demiology of recent HEV71 activity in the Asia-Pacific region sequencer (Applied Biosystems). has not been possible. To overcome this deficiency, we present here a comprehensive phylogenetic analysis of recent HEV71 HEV71 Sequence Data Obtained from GenBank strains, accomplished by examining both the VP1 and VP4 The VP4 gene sequences of another 78 HEV71 strains genes. obtained from GenBank (Appendix Table 2, online only) were included in this analysis, allowing the generation of dendro- Materials and Methods grams containing 128 HEV71 strains isolated from 1970 to 2002. These strains were isolated in the United States, Japan, Viruses Taiwan, Malaysia, Singapore, China, Bulgaria, Hungary, and All viruses used in this study were propagated in rhab- the United Kingdom. In addition, 33 complete and 9 near-com- domyosarcoma cells before extraction of RNA. Thirty-nine plete VP1 gene sequences of HEV71 strains retrieved from representative HEV71 isolates from recent years in Sarawak, GenBank and used in this study are listed in Appendix Table 2, Singapore, Perth, and Korea, as well as 16 strains isolated in online only. the United States from1972 to 1995, were propagated in rhab- domyosarcoma cells and subjected to nucleotide sequence Phylogenetic Analysis analysis (see below). These strains were used to generate 12 Alignment of the VP1 and VP4 gene sequences was under- new VP1 gene sequences and 55 new VP4 gene sequences taken by using the ClustalW program (25). Dendrograms were (Appendix Table 1, online only). constructed by using the neighbor-joining method with PHYLIP, version 3.5 (26) and drawn using TreeView (27). Reverse Transcriptase–Polymerase Bootstrap analysis with 1,000 pseudoreplicates was performed Chain Reaction (RT-PCR) by using the program Seqboot (28). The CA16 strain G10 (29) RNA was extracted from infected rhabdomyosarcoma cell was used as an outgroup for phylogenetic analysis of the VP4 supernatants by using the High Pure viral nucleic acid kit sequence data, and the HEV71 prototype strain BrCr-CA-70 (Roche Diagnostics GmbH, Mannheim, Germany). RT-PCR (30) was used as an outgroup for analysis of the VP1 sequence was performed as described (22), except that the annealing data. Historically Brown and co-workers (21) described temperature for amplification of the VP4 gene was 50°C. genogroups as lineages of HEV71 distinguished by differing at Primer pairs 159/162 and 161/NP1A (24) were used for VP1 least 15% in the VP1 gene. In this study we maintained the amplification of nucleotides (nt) 2385 to 2850 relative to BrCr; genogroups originally described and designated subgeno- for VP4 amplification, the primers VP2-REV (5′ TTCCAAT- groups to aid in discussing evolving progeny viruses. ACCACCCCTTGGATGA 3′) and EVP-2 (19) were used to amplify nt 449 to 1192 relative to BrCr. Results Nucleotide Sequence Analysis Overview of HEV71 Phylogeny PCR products were purified from gels with the QIAquick Figure 1 presents an overview of the VP4-based phyloge- gel extraction kit (QIAGEN Inc, Valencia, CA). Cycle sequenc- netic tree, generated by including representative members of ing was achieved with the primers 159/162 and 161/NP1A for each of the genogroups A, B, and C. While there are a few out- VP1 and EVP-4 (15) and VP2-REV for VP4 by using the Big liers, this comprehensive VP4-based dendrogram accurately Dye Terminator Cycle Sequencing kit version 2.0 (Applied reproduces the genogroup clusters B1, B2, B3, B4, C1, and C2 Biosystems, Foster City, CA). All sequences were determined (21,22) supported by the bootstrap values indicated. However, 462 Emerging Infectious Diseases • Vol. 9, No. 4, April 2003 RESEARCH strains in our collection from two of the more recently described genogroups B3 and C3 showed very high similarity to each other within the genogroup (>98% and 99% identity, respectively), while those within the B1 and C1 genogroups showed the widest divergence. The phylogenetic relationships between the consensus sequences of the different genogroups based on VP4 analysis are shown as an unrooted tree (Figure 2). This cladogram clearly illustrates that the C genogroup viruses are more divergent than the B genogroup viruses; how- ever, because we might not have strains that are evenly distrib- uted temporally and geographically, we were unable to deter- mine if this difference in divergence means that genogroup B viruses have evolved more recently than the genogroup C viruses.
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