| | Genetic distribution of group A human rotavirus types isolated in Gyunggi province of Korea, 1999–2002Received 17 April 2006; received in revised form 6 October 2006; accepted 10 October 2006. published online 24 November 2006. Abstract BackgroundHuman rotavirus genotypes G1–G4 and G9 are the major etiological agents of infantile gastroenteritis. G1 was the most prevalent in Korea during the 10-year period prior to 1997. However, between 1998 and 1999, G4 was the predominant type in Korea, as it was in other Asian countries. ObjectivesThe circulating pattern and genetic variability of group A human rotavirus in Gyunggi, Korea, 1999–2002, were examined in 189 stool specimens. Study designStool samples were collected from children with diarrhea, and group A human rotavirus type was determined using multiplex RT-PCR in those specimens found to be positive for rotavirus by ELISA. Each genotype was sequenced, and phylogenetic analysis was performed on the sequences. ResultWe found significant variability from year to year in the prevalence of different G and P types of rotavirus. We also found relatively high prevalence rates for types normally considered to be uncommon. Furthermore, we found that the most prevalent combination of G and P types changed from year to year. Although the combination of G and P types changed every year, the sequence of G genotypes showed a high level of similarity (>97%) compared to those of strains from other Asian countries. ConclusionWe report the types of rotavirus circulating in Gyunggi province, Korea from 1999 to 2002. This information on rotavirus diversity has important implications for rotavirus vaccine efficacy and future vaccine development. 1. Introduction  Human rotaviruses (HRV) are major causes of enteric disease in infants and young children. It is estimated that rotaviruses cause approximately 600,000 deaths annually worldwide and that in developing countries 1205 children die daily from rotavirus disease (Estes, 2001, Parashar et al., 2003, Parashar and Glass, 2006). Rotavirus, which is a genus belonging to the Reoviridae family, has a genome of 11 segments of double-stranded RNA (dsRNA) surrounded by a triple-layered capsid consisting of a core, inner capsid, and outer capsid layer. The outer capsid is composed of two viral structural proteins, VP7 and VP4, which induce the production of neutralizing antibodies and define virus G (VP7) or P (VP4) serotype specificity (Estes, 1996, Estes, 2001). Fifteen G genotypes and 26 P genotypes have been described (Varshney et al., 2002, Rahman et al., 2005a, Santos and Hoshino, 2005, Martella et al., 2006, Samajdar et al., 2006). Globally, there are five combinations of G and P genotypes which are most common. These are P[8] with G1, G3, G4 and G9, and P[4] with G2 (Santos and Hoshino, 2005, Castello et al., 2006). Among the G genotypes, G1 was the most common in Korea in the 10-year period before 1997 (Kim et al., 1990, Kim et al., 1992, Kim et al., 1999), but G4 predominated between 1998 and 1999 (Kim et al., 1999). This predominance is found in other Asian countries such as Taiwan, Thailand, and Japan (Maneekarn and Ushijima, 2000, Tsai et al., 2000, Zhou et al., 2000). In this study, we examined the distribution of the G and P types of HRV strains infecting children in Gyunggi province, which contains 25% of the population of Korea, and corroborate reports that there is significant variance in the types of HRV strains that are present in Korea from year to year. 2. Materials and methods 2.1. Sample collection One hundred eighty-nine stool specimens were obtained from children less than 5 years old who were treated for acute diarrhea at Korea University Ansan Hospital (Ansan, Gyunggi, Korea) or at Park's Pediatrics (Ilsan, Gyunggi, Korea) between December 1999 and January 2002. HRV in stool specimens was detected by Rotatek® ELISA (Korea Green Cross Corporation). 2.2. Extraction of dsRNA and RT-PCR HRV double-stranded RNA (dsRNA) was extracted using a QIAamp Viral RNA kit (Qiagen GmbH, Hilden, Germany) in accordance with the manufacturer's instructions. The dsRNA samples were subjected to semi-nested multiplex RT-PCR using conserved and type specific primers (VP7-G1, G2, G3, G4, G8 and G9, and VP4-P[4], P[6], P[8], P[9] and P[10]) (Gentsch et al., 1992, Taniguchi et al., 1992, Das et al., 1994, Gouvea et al., 1994b, Wu et al., 1994). Amplicons were purified using a QIAquick PCR purification kit (Qiagen GmbH, Hilden, Germany) and sequenced automatically using the ABI PRISM™ 377 automated DNA sequencer (Perkin-Elmer, Cetus, CT, USA). 2.3. Phylogenetic analysis of nucleotide and amino acid sequences Partial VP7 nucleotide and amino acid sequences were analyzed using the Clustal W program (Thompson et al., 1994). A mid-pointed phylogenetic tree was constructed using the maximum parsimony method with PAUP 4.0b (Sinauer Associates Inc., MA, USA). 3. Results 3.1. Determination of G genotypes and P genotypes HRV was detected in 115 of 189 (60.8%) stool samples by ELISA. G and P genotypes were detected by multiplex PCR in 105 (91.3%) and 96 (83.5%) of these samples, respectively. Overall, among G genotypes (Fig. 1), G2 (51.3%) was the most dominant, followed by G1 (28.6%), G4 (8.7%), G3 (0.9%), and mixed types (1.8%). Ten specimens (8.7%) could not be typed and G9 was not detected. In the winter of 1999–2000, G2 was by far the most prevalent type at 62.2%, followed by G1 at 19.5%, and G4 at 11%. There was a reversal between the prevalence of G1 and G2 types for the following winter (2000–2001), when type frequencies were G1 (76.5%), G2 (17.6%), and G4 (5.9%). The pattern of prevailing types changed again the next winter (2001–2002). At this time, the dominant type had shifted back from G1 (25%) to G2 (31.1%), followed by G3 (6.3%), and mixed types G1/G2 (6.3%), G1/G3 (6.3%). Overall the following P types (Fig. 2) were found: P[4] (49.6%), P[6] (14.8%), P[8] (16.5%) and, mixed type (2.6%). For nineteen samples (16.5%) the type could not be determined. In each year of the study, the P types also changed significantly. For the winter season of 1999-2000, P[4] was the dominant type, at 63.4%. Only P[8] (64.8%) and P[4] (17.6%) were detected during the next winter (2000–2001), along with the remainder being untypeable. A dramatic shift in prevailing types was again detected the next winter season (2001–2002), when P[6] was the most prevalent at 68.7% and 18.8% of samples contained P[4]/P[6] mixed types. 3.2. Correlation of G and P types For the winter season of 1999–2000, G2P[4] (52.4%) was the dominant combination of genotypes. Other combinations detected were G1P[8] (7.3%), G1P[6] (3.7%), G4P[6] (3.7%), G4P[4] (2.4%), G4P[8] (2.4%) and G1P[4] (1.2%) (Fig. 3). Twenty-two samples (26.8%) were identified for one type (G or P), but were untypeable for the other type. The dominant HRV G–P combination types were different the next winter. G1P[8] (58.9%) prevailed during the 2000–2001 winter season, followed by G2P[4] (17.6%) and G4P[8] (6.0%). Some samples (17.6%) were found to be G1 type, but were untypeable for P type. G2P[6] (25%) was the dominant type for the winter of 2001–2002. Over the same period, the following other combinations were found: G1P[6] (12.5%), G1P[4] (6.3%), G2P[4] (6.3%) and G3P[6] (6.3%). Interestingly, the P[6] type was 87.5% of identified genotypes. The P[6] isolates showed various combination types, G1P[6], G2P[6], G3P[6], G4P[6]. Three samples showed G and P mixed infections, G1P[4]/P[6] (6.3%), G1/G2P[4]P[6] (6.3%) and G1/G3P[4]P[6] (6.3%). Four samples (25%) were identified for only P[6](Table 1). | | |  | Season G type/[P] type | % (n) | |
|---|
| | December1999–February 2000 (n =82) | December 2000–February 2001 (n=17) | December 2001–February 2002 (n=16) | Total (n=115) | |
|---|
| G1/P[4] | 1.2 (1) | 0 (0) | 6.3 (1) | 1.7 (2) | | | G1/P[6] | 3.7 (3) | 0 (0) | 12.5 (2) | 4.3 (5) | | | G1/P[8] | 7.3 (6) | 58.8 (10) | 0 (0) | 13.9 (16) | | | G1/– | 7.3 (6) | 17.6 (3) | 0 (0) | 7.8 (9) | | | G2/P[4] | 52.4 (43) | 17.6 (3) | 6.3 (1) | 40.9 (47) | | | G2/P[6] | 0 (0) | 0 (0) | 25 (4) | 3.5 (4) | | | G2/– | 9.8 (8) | 0 (0) | 0 (0) | 7.0 (8) | | | G3/P[6] | 0 (0) | 0 (0) | 6.3 (1) | 0.8 (1) | | | G4/P[4] | 2.4 (2) | 0 (0) | 0 (0) | 1.7 (2) | | | G4/P[6] | 3.7 (3) | 0 (0) | 0 (0) | 2.6 (3) | | | G4/P[8] | 2.4 (2) | 6.0 (1) | 0 (0) | 2.6 (3) | | | G4/– | 2.4 (2) | 0 (0) | 0 (0) | 1.7 (2) | | | G1/P[4]P[6] | 0 (0) | 0 (0) | 6.3 (1) | 0.8 (1) | | | G1G2/P[4]P[6] | 0 (0) | 0 (0) | 6.3 (1) | 0.8 (1) | | | G1G3/P[4]P[6] | 0 (0) | 0 (0) | 6.3 (1) | 0.8 (1) | | | –/P[4] | 7.3 (6) | 0 (0) | 0 (0) | 5.2 (6) | | | –/P[6] | 0 (0) | 0 (0) | 25 (4) | 3.5 (4) | | | | | | Total | (82) | (17) | (16) | (115) | | | | |
3.3. Partial sequence analysis of VP7 To determine the extent of genetic drift within a genotype, we determined the VP7 nucleotide sequences for the G1, G2 and G4 isolates over the study period. We found that G1 isolates maintained a similarity of 97% between 1999 and 2001, while both G2 and G4 isolates maintained a similarity of 98% over this period. Therefore, although the frequencies of the types in the population, and the G and P combinations were changing dramatically, the genetic sequences were comparatively unchanged. All G1 strains isolated in 2000 and 2001 were G1P[8], but the two strains isolated in 2002, from samples KUM02001 and KUM02011 were G1P[4] and G1P[6], respectively. The strain isolated from sample KUM02001 showed 97.1–97.5% similarity with other strains, but that from KUM02011 showed 97.1–99.6% similarity with other strains regardless of year. All G2 strains isolated in 2000 and 2001 were G2P[4], and were highly similar (>99.2%). Strains from KUM00013 isolated in 2000, and KUM01024 isolated in 2001 were 100% identical, and the G2P[6] isolates, KUM02005 and KUM02019, from 2002 had a similarity of 99.7%. However, the strain isolated from sample KUM02005 had a lower similarity (98.6–99.1%) with strains isolated in other seasons. G4 was divided into G4P[6], and G4P[8], but their sequence homology was high (98.5–99.8%), irrespective of type or year. To investigate the genetic relationships between strains, partial nucleotide sequences (nt 29–1035) of VP7 and the full length of its amino acid (326 aa) were analyzed. G1 was closely related to TF14 (Taiwan) and 97'SH19 (China) (98%). In the case of G2, KUM00085 isolated in 2000 was closely related to KO-2 (99%) originating in Japan, with KUM02005 (99%) and KUM02019 (98%) isolated in 2002, and with Sc27 (99%) from India. G4 was closely related to strains isolated in Japan, Hochi and Odelia (97%), but KUM02013 showed low similarity with Kagawa82 (74.2%). Overall, Korean rotaviruses isolated from 1999 to 2002 were similar to strains isolated from other Asian countries (Fig. 4). 4. Discussion Knowledge about the prevalence of different HRV strains in different places and their variations over time can guide intervention strategies with vaccines. Studies in many countries indicate that serotype G1 was the most prevalent and that serotypes G2–G4, and G9 were evenly distributed (Jain et al., 2001, Hoshino et al., 2005). In Korea, G1 was the major genotype until 1997 (Kim et al., 1990, Kim, 1992, Kim, 1993), but this shifted to G4 from 1998 to 2000 (Seo and Sim, 2000, Song et al., 2003). In this study, serotype G2 (51.3%) was predominant and serotypes G1, G4 and G3 followed at 28.6%, 8.7%, and 0.9%, respectively, similar to other reports for the same period (Kim et al., 2002, So et al., 2004). Although G9 was reported continuously in several Asian countries, such as Japan and Thailand (Unicomb et al., 1999, Bon et al., 2000, Cubitt et al., 2000, Maneekarn and Ushijima, 2000, Palombo et al., 2000, Ramachandran et al., 2000, Zhou et al., 2000, Cunliffe et al., 2001, Iturriza-Gomara et al., 2001), it was not detected among our samples. Two G9 genotypes were reported in 2001 (Kim et al., 2005) and in 2004 we also detected G9 genotype in Gyunggi (S.S. Moon, unpublished data). According to worldwide reports, the most common G and P combinations are G1P[8], G3P[8], G4P[8] and G2P[4] (Chatterjee et al., 1996, Leite et al., 1996, Griffin et al., 2000). Uncommon G types and P types in G and P combinations have been recently detected in Korea as well in various other countries. In this study, common types (G1P[8], G2P[4] and G4P[8]) were isolated from 62.1% and 82.4% of samples in 2000 and 2001, respectively. However, the frequency of common types dropped to only 6.3% between December 2001 to February 2002, and various uncommon genotype combinations, including G2P[6], G1P[6], G3P[6] and G4P[6], were detected. These types have been reported in older infants and children with acute gastroenteritis in Brazil and India (Timenetsky Mdo et al., 1994, Steele et al., 1995, Leite et al., 1996, Ramachandran et al., 1996, Adah et al., 1997a, Linhares et al., 2002). Moreover, the P[6] type has broad regional distribution, as have G5 and G8 (Santos and Hoshino, 2005, Santos et al., 2005). P[6] types bearing G1–G4 may be a cause of acute gastroenteritis in Korea. During the winter season in 2001–2002, co-infections accounted for 2.4% of all positive samples (G1P[4]/P[6], G1G2P[4]P[6] and G1,G3P[4]P[6]). These results are indicative of reassortment events involving independent segregation of VP7 and VP4 genes (Iturriza-Gomara et al., 2002). In addition, we found a prevalence of specimens untypeable for either G or P type (but still detectable by HRV-ELISA) of 25%. In other Asian countries, the presence of untypeable samples have prevalence rates from 2% in Taiwan (Tsai et al., 2000) to 56.7% in Japan (Zhou et al., 2000). This may be caused by accumulation of point mutations in VP7 and VP4 genes (Adah et al., 1997b, Desselberger et al., 2001, Santos et al., 2003, Iturriza-Gomara et al., 2004, Rahman et al., 2005b) or by the presence of what are believed to be uncommon serotypes such as G5, G8, G10 and G12 (Taniguchi et al., 1990, Gouvea et al., 1994a, Gouvea et al., 1994c, Leite et al., 1996, Santos et al., 1998, Cunliffe et al., 2000, Griffin et al., 2002, Pongsuwanna et al., 2002). VP7 nucleotide sequences of HRV in our study had high homologies (>97%) with those of Japan, China and India, but they had lower homology with those of USA and Australia (94%). A live attenuated vaccine based on G1P[8] human strain, Rotarix™, has shown efficacy against HRV gastroenteritis caused by G1, G3, G4 and G9 with P[8], and G2P[4] (Bernstein et al., 1999, De Vos et al., 2004, Vesikari et al., 2004, Phua et al., 2005, Glass et al., 2006, Ruiz-Palacios et al., 2006, Vesikari et al., 2006). A high level of protection was reported against G1, G3, G4 and G9 with P[8], but lower efficacy was reported against G2P[4] (Salinas et al., 2005, Ruiz-Palacios et al., 2006, Vesikari et al., 2006). In this study, G2P[4] strain and P[6] were detected with a high frequency of 40.9% and 14.8%, consistent with other results from the same period (Min et al., 2004). The two main outcomes of this study are our corroboration of previous reports of high variability in the prevalence of different HRV types from year to year, and our finding of a very high prevalence of the G2 strain in Korea over the study period. 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a Department of Microbiology, College of Medicine, Korea University, Seoul 136-705, Korea b Institute for Viral Diseases, Medical Science Research Center, Korea University, Seoul, Korea c The Bank for the Pathogenic Virus, Korea University, Seoul, Korea d Central Research Institute, GreenCross Vaccine Corporation, Member of the Rhein Biotech Group, Yongin, Korea e Department of Pediatric, Korea University Ansan Hospital, Ansan, Gyunggi province, Korea  Corresponding author at: Department of Microbiology, College of Medicine, Korea University, Seoul 136-705, Korea. Tel.: +82 2 920 6168; fax: +82 2 923 3645.
PII: S1386-6532(06)00378-7 doi:10.1016/j.jcv.2006.10.004 © 2006 Elsevier B.V. All rights reserved. | |
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