For best viewing of the website please use Mozilla Firefox or Google Chrome.
Citation: Ting Zhang, Jing Li, Yong-Zhong Jiang, Jun-Qiang Xu, Xu-Hua Guan, Li-Qiang Wang, Jie Chen, Yi Liang. Genotype distribution and evolutionary analysis of rotavirus associated with acute diarrhea outpatients in Hubei, China, 2013–2016 [J].VIROLOGICA SINICA, 2022, 37(4) : 503-512.  http://dx.doi.org/10.1016/j.virs.2022.05.005

Genotype distribution and evolutionary analysis of rotavirus associated with acute diarrhea outpatients in Hubei, China, 2013–2016

  • Corresponding author: Yi Liang, liangyi@whu.edu.cn
  • Received Date: 26 March 2021
    Accepted Date: 17 May 2022
    Available online: 26 May 2022
  • Group A human rotaviruses (RVAs) annually cause the deaths of 215,000 infants and young children. To understand the epidemiological characteristics and genetic evolution of RVAs, we performed sentinel surveillance on RVA prevalence in a rotavirus-surveillance network in Hubei, China. From 2013 to 2016, a total of 2007 fecal samples from hospital outpatients with acute gastroenteritis were collected from four cities of Hubei Province. Of the 2007 samples, 153 (7.62%) were identified positive for RVA by real-time RT-PCR. RVA infection in Hubei mainly occurred in autumn and winter. The highest detection rate of RVA infection was in 1–2 years old of outpatients (16.97%). No significant difference of RVA positive rate was observed between females and males. We performed a phylogenetic analysis of the G/P genotypes based on the partial VP7/VP4 gene sequences of RVAs. G9P[8] was the most predominant strain in all four years but the prevalence of G2P[4] genotype increased rapidly since 2014. We reconstructed the evolutionary time scale of RVAs in Hubei, and found that the evolutionary rates of the G9, G2, P[8], and P[4] genotypes of RVA were 1.069×10-3, 1.029×10-3, 1.283×10-3 and 1.172×10-3 nucleotide substitutions/site/year, respectively. Importantly, using a molecular clock model, we showed that most G9, G2, P[8], and P[4] genotype strains dated from the recent ancestor in 2005, 2005, 1993, and 2013, respectively. The finding of the distribution of RVAs in infants and young children in Hubei Province will contribute to the understanding of the epidemiological characteristics and genetic evolution of RVAs in China.

  • 加载中
  • 10.1016j.virs.2022.05.005-ESM1.xlsx
    10.1016j.virs.2022.05.005-ESM2.xlsx
    10.1016j.virs.2022.05.005-ESM3.pdf
    1. Agbemabiese, C.A., Nakagomi, T., Doan, Y.H., Do, L.P., Damanka, S., Armah, G.E., Nakagomi, O., 2016. Genomic constellation and evolution of Ghanaian G2P[4] rotavirus strains from a global perspective. Infect. Genet. Evol. 45, 122–131.

    2. Akran, V., Peenze, I., Akoua-Koffi, C., Kette, H., de Beer, M.C., Dosso, M., Steele, A.D., 2010. Molecular characterization and genotyping of human rotavirus strains in Abidjan, Cote d'Ivoire. J. Infect. Dis. 202, S220–S224.

    3. Aminu, M., Page, N.A., Ahmad, A.A., Umoh, J.U., Dewar, J., Steelem, A.D., 2010. Diversity of rotavirus VP7 and VP4 genotypes in Northwestern Nigeria. J. Infect. Dis. 202, S198–S204.

    4. Arista, S., Giammanco, G.M., De Grazia, S., Ramirez, S., Lo Biundo, C., Colomba, C., Cascio, A., Martella, V., 2006. Heterogeneity and temporal dynamics of evolution of G1 human rotaviruses in a settled population. J. Virol. 80, 10724–10733.

    5. Chandran, A., Fitzwater, S., Zhen, A., Santosham, M., 2010. Prevention of rotavirus gastroenteritis in infants and children: rotavirus vaccine safety, efficacy, and potential impact of vaccines. Biologics 4, 213–229.

    6. Charles, M.D., Holman, R.C., Curns, A.T., Parashar, U.D., Glass, R.I., Bresee, J.S., 2006. Hospitalizations associated with rotavirus gastroenteritis in the United States, 1993-2002. Pediatr. Infect. Dis. J. 25, 489–493.

    7. Cunliffe, N.A., Kilgore, P.E., Bresee, J.S., Steele, A.D., Luo, N., Hart, C.A., Glass, R.I., 1998. Epidemiology of rotavirus diarrhoea in Africa: a review to assess the need for rotavirus immunization. Bull. World Health Organ. 76, 525–537.

    8. da Silva Soares, L., de Fátima Dos Santos Guerra, S., do Socorro Lima de Oliveira, A., da Silva Dos Santos, F., de Fátima Costa de Menezes, E.M., Mascarenhas, J.D., Linhares, A.C., 2014. Diversity of rotavirus strains circulating in Northern Brazil after introduction of a rotavirus vaccine: high prevalence of G3P[6] genotype. J. Med. Virol. 86, 1065–1072.

    9. Dian, Z., Fan, M., Wang, B., Feng, Y., Ji, H., Dong, S., Zhang, A.M., Liu, L., Niu, H., Xia, X., 2017. The prevalence and genotype distribution of rotavirus A infection among children with acute gastroenteritis in Kunming, China. Arch. Virol. 162, 281–285.

    10. Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973.

    11. Duan, Z.J., Liu, N., Yang, S.H., Zhang, J., Sun, L.W., Tang, J.Y., Jin, Y., Du, Z.Q., Xu, J., Wu, Q.B., Tong, Z.L., Gong, S.T., Qian, Y., Ma, J.M., Liao, X.C., Widdowson, M.A., Jiang, B., Fang, Z.Y., 2009. Hospital-based surveillance of rotavirus diarrhea in the People's Republic of China, August 2003-July 2007. J. Infect. Dis. 200, S167–S173.

    12. Duffy, S., Shackelton, L.A., Holmes, E.C., 2008. Rates of evolutionary change in viruses:patterns and determinants. Nat. Rev. Genet. 9, 267–276.

    13. Durmaz, R., Kalaycioqlu, A.T., Acar, S., Bakkaloglu, Z., Karagoz, A., Korukluoglu, G., Ertek, M., Torunoglu, M.A., Turkish Rotavirus Surveillance Network, 2014. Prevalence of rotavirus genotypes in children younger than 5 years of age before the introduction of a universal rotavirus vaccination program: report of rotavirus surveillance in Turkey. PLoS One 9, e113674.

    14. Fu, C., He, Q., Xu, J., Xie, H., Ding, P., Hu, W., Dong, Z., Liu, X., Wang, M., 2012. Effectiveness of the Lanzhou lamb rotavirus vaccine against gastroenteritis among children. Vaccine 31, 154–158.

    15. Fang, Z.Y., Wang, B., Kilgore, P.E., Bresee, J.S., Zhang, L.J., Sun, L.W., Du, Z.Q., Tang, J.Y., Hou, A.C., Shen, H., Song, X.B., Nyambat, B., Hummelman, E., Xu, Z.Y., Glass, R.I., 2005. Sentinel hospital surveillance for rotavirus diarrhea in the People's Republic of China, August 2001-July 2003. J. Infect. Dis. 192, S94–S99.

    16. Gauchan, P., Nakagomi, T., Sherchand, J.B., Yokoo, M., Pandey, B.D., Cunliffe, N.A., Nakagomi, O., 2013. Continued circulation of G12P[6] rotaviruses over 28 months in Nepal: successive replacement of predominant strains. Trop. Med. Health 41, 7–12.

    17. Glass, R.I., Parashar, U.D., Bresee, J.S., Turcios, R., Fischer, T.K., Widdowson, M.A., Jiang, B., Gentsch, J.R., 2006. Rotavirus vaccines: current prospects and future challenges. Lancet 368, 323–332.

    18. Hacimustafaoǧlu, M., Celebi, S., Aǧin, M., Ozkaya, G., 2011. Rotavirus epidemiology of children in Bursa, Turkey: a multi-centered hospital-based descriptive study. Turk. J. Pediatr. 53, 604–613.

    19. Hull, J.J., Teel, E.N., Kerin, T.K., Freeman, M.M., Esona, M.D., Gentsch, J.R., Cortese, M.M., Parashar, U.D., Glass, R.I., Bowen, M.D., National Rotavirus Strain Surveillance System, 2011. United States rotavirus strain surveillance from 2005 to 2008: genotype prevalence before and after vaccine introduction. Pediatr. Infect. Dis. J. 30, S42–S47.

    20. Iturriza-Gomara, M., Dallman, T., Bányai, K., Böttiger, B., Buesa, J., Diedrich, S., Fiore, L., Johansen, K., Koopmans, M., Korsun, N., Koukou, D., Kroneman, A., Lászlo, B., Lappalainen, M.,, Maunula, L., Marques, A.M., Matthijnssens, J., Midgley, S., Mladenova, Z., Nawaz, S., Poljsak-Prijatelj, M., Pothier, P., Ruggeri, F.M., Sanchez Fauquier, A., Steyer, A., Sidaraviciute-Ivaskeviciene, I., Syriopoulou, V., Tran, A.N., Usonis, V., VAN Ranst, M., De Rougemont, A., Gray, J., 2011. Rotavirus genotypes cocirculating in Europe between 2006 and 2009 as determined by EuroRotaNet, a panEuropean collaborative strain surveillance network. Epidemiol. Infect. 139, 895–909.

    21. Iturriza-Gómara, M., Kang, G., Gray, J., 2004. Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J. Clin. Virol. 31, 259–265.

    22. Jin, Y., Cheng, W.X., Yang, X.M., Jin, M., Zhang, Q., Xu, Z.Q., Yu, J.M., Zhu, L., Yang, S.H., Liu, N., Cui, S.X., Fang, Z.Y., Duan, Z.J., 2009. Viral agents associated with acute gastroenteritis in children hospitalized with diarrhea in Lanzhou, China. J. Clin. Virol. 44, 238–241.

    23. Jin, Y., Ye, X.H., Fang, Z.Y., Li, Y.N., Yang, X.M., Dong, Q.L., Huang, X., 2008. Molecular epidemic features and variation of rotavirus among children with diarrhea in Lanzhou, China, 2001-2006. World J. Pediatr. 4, 197–201.

    24. Kiseleva, V., Faizuloev, E., Meskina, E., Marova, A., Oksanich, A., Samartseva, T., Bakhtoyarov, G., Bochkareva, N., Filatov, N., Linok, A., Ammour, Y., Zverev, V., 2018. Molecular-genetic characterization of human rotavirus a strains circulating in Moscow, Russia (2009-2014). Virol. Sin. 33, 304–313.

    25. László, B., Kónya, J., Danár, E., Deák, J., Farkas, A., Gray, J., Grósz, G., Iturriza-Gomara, M., Jakab, F., Juhász, Á., Kisfali, P., Kovács, J., Lengyel, G., Martella, V., Melegh, B., Mészáros, J., Molnár, P., Nyúl, Z., Papp, H., Pátri, L., Puskás, E., Sántha, I., Schneider, F., Szomor, K., Toth, A., Tóth, E., Szücs, G., Bányai, K., 2012. Surveillance of human rotaviruses in 2007-2011, Hungary: exploring the genetic relatedness between vaccine and field strains. J. Clin. Virol. 55, 140–146.

    26. Leshem, E., Lopman, B., Glass, R., Gentsch, J., Bányai, K., Parashar, U., Patel, M., 2014. Distribution of rotavirus strains and strain-specific effectiveness of the rotavirus vaccine after its introduction: a systematic review and meta-analysis. Lancet Infect. Dis. 14, 847–856.

    27. Li, J., Zhang, Y., Yang, Y., Liang, Z., Tian, Y., Liu, B., Gao, Z., Jia, L., Chen, L., Wang, Q., 2019. Effectiveness of Lanzhou lamb rotavirus vaccine in preventing gastroenteritis among children younger than 5 years of age. Vaccine 37, 3611–3616.

    28. Li, Y., Wang, S.M., Zhen, S.S., Chen, Y., Deng, W., Kilgore, P.E., Wang, X.Y., 2014. Diversity of rotavirus strains causing diarrhea in < 5 years old Chinese children: a systematic review. PLoS One 9, e84699.

    29. Matthijnssens, J., Ciarlet, M., McDonald, S.M., Attoui, H., Bányai, K., Brister, J.R., Buesa, J., Esona, M.D., Estes, M.K., Gentsch, J.R., Iturriza-Gómara, M., Johne, R., Kirkwood, C.D., Martella, V., Mertens, P.P., Nakagomi, O., Parreño, V., Rahman, M., Ruggeri, F.M., Saif, L.J., Santos, N., Steyer, A., Taniguchi, K., Patton, J.T., Desselberger, U., Van Ranst, M., 2011. Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification working group (RCWG). Arch. Virol. 156, 1397–1413.

    30. Matthijnssens, J., Heylen, E., Zeller, M., Rahman, M., Lemey, P., Van Ranst, M., 2010. Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol. Biol. Evol. 27, 2431–2436.

    31. Mijatovic-Rustempasic, S., Tam, K.I., Kerin, T.K., Lewis, J.M., Gautam, R., Quaye, O., Gentsch, J.R., Bowen, M.D., 2013. Sensitive and specific quantitative detection of rotavirus A by one-step real-time reverse transcription-PCR assay without antecedent double-stranded-RNA denaturation. J. Clin. Microbiol. 51, 3047–3054.

    32. Nelson, E.A.S., Bresee, J.S., Parashar, U.D., Widdowson, M.A., Glass, R.I., Asian Rotavirus Surveillance Network, 2008. Rotavirus epidemiology: the Asian rotavirus surveillance network. Vaccine 26, 3192–3196.

    33. Oluwatoyin Japhet, M., Adeyemi Adesina, O., Famurewa, O., Svensson, L., Nordgren, J., 2012. Molecular epidemiology of rotavirus and norovirus in Ile-Ife, Nigeria: high prevalence of G12P[8] rotavirus strains and detection of a rare norovirus genotype. J. Med. Virol. 84, 1489–1496.

    34. Pietsch, C., Petersen, L., Patzer, L., Liebert, U.G., 2009. Molecular characteristics of German G8P[4] rotavirus strain GER1H-09 suggest that a genotyping and subclassification update is required for G8. J. Clin. Microbiol. 47, 3569–3576.

    35. Posada, D., 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256.

    36. Pukuta, E.S., Esona, M.D., Nkongolo, A., Seheri, M., Makasi, M., Nyembwe, M., Mondonge, V., Dahl, B.A., Mphahlele, M.J., Cavallaro, K., Gentsch, J., Bowen, M.D., Waku-Kouomou, D., Muyembe, J.J., SURVAC Working Group, 2014. Molecular surveillance of rotavirus infection in the democratic republic of the Congo August 2009 to june 2012. Pediatr. Infect. Dis. J. 33, 355–359.

    37. Rambaut, A., Lam, T.T., Carvalho, L.M., Pybus, O.G., 2016. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2, vew007.

    38. Santos, N., Hoshino, Y., 2005. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev. Med. Virol. 15, 29–56.

    39. Simmonds, M.K., Armah, G., Asmah, R., Banerjee, I., Damanka, S., Esona, M., Gentsch, J.R., Gray, J.J., Kirkwood, C., Page, N., Iturriza-Gomara, M., 2008. Newóligonucleotide primers for P-typing of rotavirus strains: strategies for typing previously untypeable strains. J. Clin. Virol. 42, 368–373.

    40. Stupka, J.A., Degiuseppe, J.I., Parra, G.I., Argentinean National Rotavirus Surveillance Network, 2012. Increased frequency of rotavirus G3P[8] and G12P[8] in Argentina during 2008-2009: whole-genome characterization of emerging G12P[8] strains. J. Clin. Virol. 54, 162–167.

    41. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.

    42. Tate, J.E., Burton, A.H., Boschi-Pinto, C., Parashar, U.D., World Health OrganizationCoordinated Global Rotavirus Surveillance Network, 2016. Global, regional, and national estimates of rotavirus mortality in children < 5 Years of age, 2000-2013. Clin. Infect. Dis. 62, S96–S105.

    43. Todd, S., Page, N.A., Duncan Steele, A., Peenze, I., Cunliffe, N.A., 2010. Rotavirus strain types circulating in Africa: review of studies published during 1997-2006. J. Infect. Dis. 202, S34–S42.

    44. Wang, Y.H., Kobayashi, N., Zhou, D.J., Yang, Z.Q., Zhou, X., Peng, J.S., Zhu, Z.R., Zhao, D.F., Liu, M.Q., Gong, J., 2007. Molecular epidemiologic analysis of group A rotaviruses in adults and children with diarrhea in Wuhan city, China, 2000-2006. Arch. Virol. 152, 669–685.

    45. Wang, Y.H., Kobayashi, N., Zhou, X., Nagashima, S., Zhu, Z.R., Peng, J.S., Liu, M.Q., Hu, Q., Zhou, D.J., Watanabe, S., Ishino, M., 2009. Phylogenetic analysis of rotaviruses with predominant G3 and emerging G9 genotypes from adults and children in Wuhan, China. J. Med. Virol. 81, 382–389.

    46. Wang, Y.H., Pang, B.B., Ghosh, S., Zhou, X., Shintani, T., Urushibar, N., Song, Y.W., He, M.Y., Liu, M.Q., Tang, W.F., Peng, J.S., Hu, Q., Zhou, D.J., Kobayashi, N., 2014. Molecular epidemiology and genetic evolution of the whole genome of G3P [8] human rotavirus in Wuhan, China, from 2000 through 2013. PLoS One 9, e88850.

    47. Wang, Y.H., Zhou, X., Ghosh, S., Zhou, D.J., Pang, B.B., Peng, J.S., Hu, Q., Kobayashi, N., 2011. Prevalence of human rotavirus genotypes in during 2008-2011: changing trend of predominant genotypes and emergence of strains with the P[8]b subtype of the VP4 gene. Arch. Virol. 156, 2221–2231.

    48. Weinberg, G.A., Payne, D.C., Teel, E.N., Mijatovic-Rustempasic, S., Bowen, M.D., Wikswo, M., Gentsch, J.R., Parashar, U.D., 2012. First reports of human rotavirus G8P[4] gastroenteritis in the United States. J. Clin. Microbiol. 50, 1118–1121.

    49. Wu, D., Yen, C., Yin, Z.D., Li, Y.X., Liu, N., Liu, Y.M., Wang, H.Q., Cui, F.Q., Gregory, C.J., Tate, J.E., Parashar, U.D., Yin, D.P., Li, L., 2016. The public health burden of rotavirus disease in children younger than five years and considerations for rotavirus vaccine introduction in China. Pediatr. Infect. Dis. J. 35, e392–e398.

    50. Xiao, N., Wu, J., Zhou, Y., Sun, M., Li, H., 2014. Epidemiological and clinical studies of rotavirus-induced diarrhea in China from 1994-2013. Hum. Vaccines Immunother. 10, 3672–3680.

    51. Yu, J., Lai, S., Geng, Q., Ye, C., Zhang, Z., Zheng, Y., Wang, L., Duan, Z., Zhang, J., Wu, S., Parashar, U., Yang, W., Liao, Q., Li, Z., 2019. Prevalence of rotavirus and rapid changes in circulating rotavirus strains among children with acute diarrhea in China, 2009-2015. J. Infect. 78, 66–74.

    52. Zhao, L., Shi, X., Meng, D., Guo, J., Li, Y., Liang, L., Guo, X., Tao, R., Zhang, X., Gao, R., Gao, L., Wang, J., 2021. Prevalence and genotype distribution of group A rotavirus circulating in Shanxi Province, China during 2015-2019. BMC Infect. Dis. 21, 94.

    53. Zhang, J., Liu, H., Jia, L., Payne, D.C., Hall, A.J., Xu, Z., Gao, Z., Chang, Z., Jiang, B., Parashar, U.D., Meng, L., Yu, H., Duan, Z., 2015. Active, population-based surveillance for rotavirus gastroenteritis in Chinese children: Beijing Municipality and Gansu Province, China. Pediatr. Infect. Dis. J. 34, 40–46.

    54. Zhang, S., Yin, J., Yang, J., Tian, L., Li, D., Zhang, Q., Chen, J., Xu, W., Zhou, X., 2017. Epidemiology and genetic diversity of group A rotavirus in acute diarrhea patients in pre-vaccination era in southwest China. J. Med. Virol. 89, 71–78.

  • 加载中

Article Metrics

Article views(412) PDF downloads(8) Cited by()

Related
Proportional views
    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Genotype distribution and evolutionary analysis of rotavirus associated with acute diarrhea outpatients in Hubei, China, 2013–2016

      Corresponding author: Yi Liang, liangyi@whu.edu.cn
    • a Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, 430072, China;

    Abstract: Group A human rotaviruses (RVAs) annually cause the deaths of 215,000 infants and young children. To understand the epidemiological characteristics and genetic evolution of RVAs, we performed sentinel surveillance on RVA prevalence in a rotavirus-surveillance network in Hubei, China. From 2013 to 2016, a total of 2007 fecal samples from hospital outpatients with acute gastroenteritis were collected from four cities of Hubei Province. Of the 2007 samples, 153 (7.62%) were identified positive for RVA by real-time RT-PCR. RVA infection in Hubei mainly occurred in autumn and winter. The highest detection rate of RVA infection was in 1–2 years old of outpatients (16.97%). No significant difference of RVA positive rate was observed between females and males. We performed a phylogenetic analysis of the G/P genotypes based on the partial VP7/VP4 gene sequences of RVAs. G9P[8] was the most predominant strain in all four years but the prevalence of G2P[4] genotype increased rapidly since 2014. We reconstructed the evolutionary time scale of RVAs in Hubei, and found that the evolutionary rates of the G9, G2, P[8], and P[4] genotypes of RVA were 1.069×10-3, 1.029×10-3, 1.283×10-3 and 1.172×10-3 nucleotide substitutions/site/year, respectively. Importantly, using a molecular clock model, we showed that most G9, G2, P[8], and P[4] genotype strains dated from the recent ancestor in 2005, 2005, 1993, and 2013, respectively. The finding of the distribution of RVAs in infants and young children in Hubei Province will contribute to the understanding of the epidemiological characteristics and genetic evolution of RVAs in China.

    Reference (54) Relative (20)

    目录

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return