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Published in: Archives of Virology 5/2015

01-05-2015 | Original Article

Molecular characterization and multiple infections of rotavirus, norovirus, sapovirus, astrovirus and adenovirus in outpatients with sporadic gastroenteritis in Shanghai, China, 2010–2011

Authors: Lijuan Lu, Ran Jia, Huaqing Zhong, Menghua Xu, Liyun Su, Lingfeng Cao, Zuoquan Dong, Niuniu Dong, Jin Xu

Published in: Archives of Virology | Issue 5/2015

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Abstract

Rotavirus (RV), norovirus (NoV), sapovirus (SaV), human astrovirus (HAstV) and human adenovirus (HAdV) are significant because they are the most common pathogens that cause diarrhea in young children. The aim of this study was to investigate the genetic characteristics and compare the roles of these five viruses in outpatient children with diarrhea in Shanghai. A total of 436 fecal samples were collected from pediatric patients with acute gastroenteritis from January 2010 to December 2011. The selected samples were subjected to reverse transcription PCR (RT-PCR) or PCR to detect and genotype RV, NoV, SaV, HAstV and HAdV. RV (43.3 %, 189/436) was the most prevalent virus, followed by NoV (28.9 %, 126/436), HAdV (7.1 %, 31/436). HAstV (1.8 %, 8/436) and SaV (0.5 %, 2/436). The percentage of multiple infection cases was 14.9 % (65/436), and RV + NoV was the predominant mixed infection. The RV genotype combinations of P[8]G3 (52/189, 27.5 %), P[8]G1 (51/189, 26.9 %) and P[8]G9 (48/189, 25.4 %) occurred most frequently. The predominant NoV genotype was GII.4 (73.0 %, 92/126), and the majority of GII.4 clustered as GII.4-2006b (65.2 %, 60/92). Two of the SaV cases were identified as GI.2 and GII.1. All HAstV-positive samples belonged to HAstV-1. The predominant HAdV type was HAdV-41 (45.2 %, 14/31). This study clearly shows the diversity of the viral causative agents of acute gastroenteritis in outpatient children in Shanghai, which will provide baseline information for future vaccination strategies and development in this area.
Literature
2.
go back to reference Moreno-Espinosa S, Farkas T, Jiang X (2004) Human caliciviruses and pediatric gastroenteritis. Semin Pediatr Infect Dis 15:237–245CrossRefPubMed Moreno-Espinosa S, Farkas T, Jiang X (2004) Human caliciviruses and pediatric gastroenteritis. Semin Pediatr Infect Dis 15:237–245CrossRefPubMed
3.
go back to reference Ramani S, Kang G (2009) Viruses causing childhood diarrhoea in the developing world. Curr Opin Infect Dis 22:477–482CrossRefPubMed Ramani S, Kang G (2009) Viruses causing childhood diarrhoea in the developing world. Curr Opin Infect Dis 22:477–482CrossRefPubMed
4.
go back to reference Anderson EJ (2010) Prevention and treatment of viral diarrhea in pediatrics. Expert Rev Anti Infect Ther 8:205–217CrossRefPubMed Anderson EJ (2010) Prevention and treatment of viral diarrhea in pediatrics. Expert Rev Anti Infect Ther 8:205–217CrossRefPubMed
5.
go back to reference Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, Steele D, Birmingham M, Glass RI (2009) Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200(Suppl 1):S9–S15CrossRefPubMed Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, Steele D, Birmingham M, Glass RI (2009) Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200(Suppl 1):S9–S15CrossRefPubMed
6.
go back to reference Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14:1224–1231CrossRefPubMedCentralPubMed Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14:1224–1231CrossRefPubMedCentralPubMed
7.
go back to reference Pang XL, Joensuu J, Vesikari T (1999) Human calicivirus-associated sporadic gastroenteritis in Finnish children less than two years of age followed prospectively during a rotavirus vaccine trial. Pediatr Infect Dis 18:420–426CrossRef Pang XL, Joensuu J, Vesikari T (1999) Human calicivirus-associated sporadic gastroenteritis in Finnish children less than two years of age followed prospectively during a rotavirus vaccine trial. Pediatr Infect Dis 18:420–426CrossRef
8.
go back to reference Rockx B, De Wit M, Vennema H, Vinjé J, De Bruin E, Van Duynhoven Y, Koopmans M (2002) Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis 35:246–253CrossRefPubMed Rockx B, De Wit M, Vennema H, Vinjé J, De Bruin E, Van Duynhoven Y, Koopmans M (2002) Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis 35:246–253CrossRefPubMed
9.
go back to reference Moyo SJ, Hanevik K, Blomberg B, Kommedal O, Nordbø SA, Maselle S, Langeland N (2014) Prevalence and molecular characterisation of human adenovirus in diarrhoeic children in Tanzania; a case control study. BMC Infect Dis 14:666CrossRefPubMedCentralPubMed Moyo SJ, Hanevik K, Blomberg B, Kommedal O, Nordbø SA, Maselle S, Langeland N (2014) Prevalence and molecular characterisation of human adenovirus in diarrhoeic children in Tanzania; a case control study. BMC Infect Dis 14:666CrossRefPubMedCentralPubMed
10.
go back to reference Jin Y, Cheng WX, Yang XM, Jin M, Zhang Q, Xu ZQ, Yu JM, Zhu L, Yang SH, Liu N, Cui SX, Fang ZY, Duan ZJ (2009) Viral agents associated with acute gastroenteritis in children hospitalized with diarrhea in Lanzhou, China. J Clin Virol 44:238–241CrossRefPubMed Jin Y, Cheng WX, Yang XM, Jin M, Zhang Q, Xu ZQ, Yu JM, Zhu L, Yang SH, Liu N, Cui SX, Fang ZY, Duan ZJ (2009) Viral agents associated with acute gastroenteritis in children hospitalized with diarrhea in Lanzhou, China. J Clin Virol 44:238–241CrossRefPubMed
11.
go back to reference Nguyen TA, Yagyu F, Okame M, Phan TG, Trinh QD, Yan H, Hoang KT, Cao AT, Le Hoang P, Okitsu S, Ushijima H (2007) Diversity of viruses associated with acute gastroenteritis in children hospitalized with diarrhea in Ho Chi Minh City, Vietnam. J Med Virol 79:582–590CrossRefPubMed Nguyen TA, Yagyu F, Okame M, Phan TG, Trinh QD, Yan H, Hoang KT, Cao AT, Le Hoang P, Okitsu S, Ushijima H (2007) Diversity of viruses associated with acute gastroenteritis in children hospitalized with diarrhea in Ho Chi Minh City, Vietnam. J Med Virol 79:582–590CrossRefPubMed
12.
go back to reference Ouyang Y, Ma H, Jin M, Wang X, Wang J, Xu L, Lin S, Shen Z, Chen Z, Qiu Z, Gao Z, Peng L, Li J (2012) Etiology and epidemiology of viral diarrhea in children under the age of five hospitalized in Tianjin, China. Arch Virol 157:881–887CrossRefPubMed Ouyang Y, Ma H, Jin M, Wang X, Wang J, Xu L, Lin S, Shen Z, Chen Z, Qiu Z, Gao Z, Peng L, Li J (2012) Etiology and epidemiology of viral diarrhea in children under the age of five hospitalized in Tianjin, China. Arch Virol 157:881–887CrossRefPubMed
13.
go back to reference Shimizu H, Phan TG, Nishimura S, Okitsu S, Maneekarn N, Ushijima H (2007) An outbreak of adenovirus serotype 41 infection in infants and children with acute gastroenteritis in Maizuru City, Japan. Infect Genet Evol 7:279–284CrossRefPubMed Shimizu H, Phan TG, Nishimura S, Okitsu S, Maneekarn N, Ushijima H (2007) An outbreak of adenovirus serotype 41 infection in infants and children with acute gastroenteritis in Maizuru City, Japan. Infect Genet Evol 7:279–284CrossRefPubMed
14.
go back to reference Akihara S, Phan TG, Nguyen TA, Hansman G, Okitsu S, Ushijima H (2005) Existence of multiple outbreaks of viral gastroenteritis among infants in a day care center in Japan. Arch Virol 150:2061–2075CrossRefPubMed Akihara S, Phan TG, Nguyen TA, Hansman G, Okitsu S, Ushijima H (2005) Existence of multiple outbreaks of viral gastroenteritis among infants in a day care center in Japan. Arch Virol 150:2061–2075CrossRefPubMed
15.
go back to reference Utagawa ET, Nishizawa S, Sekine S, Hayashi Y, Ishihara Y, Oishi I, Iwasaki A, Yamashita I, Miyamura K, Yamazaki S (1994) Astrovirus as a cause of gastroenteritis in Japan. J Clin Microbiol 32:1841–1845PubMedCentralPubMed Utagawa ET, Nishizawa S, Sekine S, Hayashi Y, Ishihara Y, Oishi I, Iwasaki A, Yamashita I, Miyamura K, Yamazaki S (1994) Astrovirus as a cause of gastroenteritis in Japan. J Clin Microbiol 32:1841–1845PubMedCentralPubMed
16.
go back to reference Nguyen TA, Hoang L, le Pham D, Hoang KT, Mizuguchi M, Okitsu S, Ushijima H (2008) Identification of human astrovirus infections among children with acute gastroenteritis in the Southern Part of Vietnam during 2005–2006. J Med Virol 80:298–305CrossRefPubMed Nguyen TA, Hoang L, le Pham D, Hoang KT, Mizuguchi M, Okitsu S, Ushijima H (2008) Identification of human astrovirus infections among children with acute gastroenteritis in the Southern Part of Vietnam during 2005–2006. J Med Virol 80:298–305CrossRefPubMed
17.
go back to reference Rodriguez-Baez N, O’Brien R, Qiu SQ, Bass DM (2002) Astrovirus, adenovirus, and rotavirus in hospitalized children: prevalence and association with gastroenteritis. J Pediatr Gastroenterol Nutr 35:64–68CrossRefPubMed Rodriguez-Baez N, O’Brien R, Qiu SQ, Bass DM (2002) Astrovirus, adenovirus, and rotavirus in hospitalized children: prevalence and association with gastroenteritis. J Pediatr Gastroenterol Nutr 35:64–68CrossRefPubMed
18.
go back to reference Phan TG, Okame M, Nguyen TA, Maneekarn N, Nishio O, Okitsu S, Ushijima H (2004) Human astrovirus, norovirus (GI, GII), and sapovirus infections in Pakistani children with diarrhea. J Med Virol 73:256–261CrossRefPubMed Phan TG, Okame M, Nguyen TA, Maneekarn N, Nishio O, Okitsu S, Ushijima H (2004) Human astrovirus, norovirus (GI, GII), and sapovirus infections in Pakistani children with diarrhea. J Med Virol 73:256–261CrossRefPubMed
19.
go back to reference Lu L, Zhong H, Xu M, Su L, Cao L, Dong N, Xu J (2014) Molecular epidemiology of human calicivirus infections in children with acute diarrhea in Shanghai: a retrospective comparison between inpatients and outpatients treated between 2006 and 2011. Arch Virol 159:1613–1621CrossRefPubMed Lu L, Zhong H, Xu M, Su L, Cao L, Dong N, Xu J (2014) Molecular epidemiology of human calicivirus infections in children with acute diarrhea in Shanghai: a retrospective comparison between inpatients and outpatients treated between 2006 and 2011. Arch Virol 159:1613–1621CrossRefPubMed
20.
go back to reference Lu L, Zhong H, Su L, Cao L, Xu M, Xu J (2013) Epidemical characteries of group A Rotavirus genotypes in children hospitalized with diarrhea in Shanghai, during 2008–2011. Chin J Evid Based Pediatr 8:98–104 Lu L, Zhong H, Su L, Cao L, Xu M, Xu J (2013) Epidemical characteries of group A Rotavirus genotypes in children hospitalized with diarrhea in Shanghai, during 2008–2011. Chin J Evid Based Pediatr 8:98–104
21.
go back to reference Lu L, Xu J, Zhong H, Su L, Cao L, Xu M (2012) Molecular epidemiology study on group A rotavirus in hospitalized children with diarrhea in Shanghai during 2006–2008. Chin Infect Dis 30:90–94 Lu L, Xu J, Zhong H, Su L, Cao L, Xu M (2012) Molecular epidemiology study on group A rotavirus in hospitalized children with diarrhea in Shanghai during 2006–2008. Chin Infect Dis 30:90–94
22.
go back to reference Xu J, Yang Y, Sun J, Ding Y, Su L, Fang Z, Glass RI (2009) Molecular epidemiology of rotavirus infections among children hospitalized for acute gastroenteritis in Shanghai, China, 2001 through 2005. J Clin Virol 44:58–61CrossRefPubMed Xu J, Yang Y, Sun J, Ding Y, Su L, Fang Z, Glass RI (2009) Molecular epidemiology of rotavirus infections among children hospitalized for acute gastroenteritis in Shanghai, China, 2001 through 2005. J Clin Virol 44:58–61CrossRefPubMed
23.
go back to reference Noel JS, Lee TW, Kurtz JB, Glass RI, Monroe SS (1995) Typing of human astroviruses from clinical isolates by enzyme immunoassay and nucleotide sequencing. J Clin Microbiol 33:797–801PubMedCentralPubMed Noel JS, Lee TW, Kurtz JB, Glass RI, Monroe SS (1995) Typing of human astroviruses from clinical isolates by enzyme immunoassay and nucleotide sequencing. J Clin Microbiol 33:797–801PubMedCentralPubMed
24.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedCentralPubMed Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedCentralPubMed
25.
go back to reference Kawai K, O’Brien MA, Goveia MG, Mast TC, El Khoury AC (2012) Burden of rotavirus gastroenteritis and distribution of rotavirus strains in Asia: a systematic review. Vaccine 30:1244–1254CrossRefPubMed Kawai K, O’Brien MA, Goveia MG, Mast TC, El Khoury AC (2012) Burden of rotavirus gastroenteritis and distribution of rotavirus strains in Asia: a systematic review. Vaccine 30:1244–1254CrossRefPubMed
26.
go back to reference Phan TG, Nishimura S, Okame M, Nguyen TA, Khamrin P, Okitsu S, Maneekarn N, Ushijima H (2004) Virus diversity and an outbreak of group C rotavirus among infants and children with diarrhea in Maizuru city, Japan during 2002–2003. J Med Virol 74:173–179CrossRefPubMed Phan TG, Nishimura S, Okame M, Nguyen TA, Khamrin P, Okitsu S, Maneekarn N, Ushijima H (2004) Virus diversity and an outbreak of group C rotavirus among infants and children with diarrhea in Maizuru city, Japan during 2002–2003. J Med Virol 74:173–179CrossRefPubMed
27.
go back to reference Benhafid M, Elomari N, Elqazoui M, Meryem AI, Rguig A, Filali-Maltouf A, Elaouad R (2013) Diversity of rotavirus strains circulating in children under 5 years of age admitted to hospital for acute gastroenteritis in Morocco, June 2006 to May 2009. J Med Virol 85:354–362CrossRefPubMed Benhafid M, Elomari N, Elqazoui M, Meryem AI, Rguig A, Filali-Maltouf A, Elaouad R (2013) Diversity of rotavirus strains circulating in children under 5 years of age admitted to hospital for acute gastroenteritis in Morocco, June 2006 to May 2009. J Med Virol 85:354–362CrossRefPubMed
28.
go back to reference Maiklang O, Vutithanachot V, Vutithanachot C, Hacharoen P, Chieochansin T, Poovorawan Y (2012) Prevalence of group A genotype human rotavirus among children with diarrhea in Thailand, 2009–2011. Southeast Asian J Trop Med Public Health 43:904–916PubMed Maiklang O, Vutithanachot V, Vutithanachot C, Hacharoen P, Chieochansin T, Poovorawan Y (2012) Prevalence of group A genotype human rotavirus among children with diarrhea in Thailand, 2009–2011. Southeast Asian J Trop Med Public Health 43:904–916PubMed
29.
go back to reference Sánchez-Fauquier A, Montero V, Colomina J, González-Galán V, Aznar J, Aisa ML, Gutierrez C, Sainz de Baranda C, Wilhelmi I (2011) Global study of viral diarrhea in hospitalized children in Spain: results of structural surveillance of viral gastroenteritis net work (VIGESS-net) 2006–2008. J Clin Virol 52:353–358CrossRefPubMed Sánchez-Fauquier A, Montero V, Colomina J, González-Galán V, Aznar J, Aisa ML, Gutierrez C, Sainz de Baranda C, Wilhelmi I (2011) Global study of viral diarrhea in hospitalized children in Spain: results of structural surveillance of viral gastroenteritis net work (VIGESS-net) 2006–2008. J Clin Virol 52:353–358CrossRefPubMed
30.
go back to reference Chen Y, Li Z, Han D, Cui D, Chen X, Zheng S, Yu F, Liu J, Lai S, Yan Y, Lin Z, Shi Z, Wu T, Li L, Yang W (2013) Viral agents associated with acute diarrhea among outpatient children in southeastern China. Pediatr Infect Dis J 32:e285–e290CrossRefPubMed Chen Y, Li Z, Han D, Cui D, Chen X, Zheng S, Yu F, Liu J, Lai S, Yan Y, Lin Z, Shi Z, Wu T, Li L, Yang W (2013) Viral agents associated with acute diarrhea among outpatient children in southeastern China. Pediatr Infect Dis J 32:e285–e290CrossRefPubMed
31.
go back to reference Harada S, Okada M, Yahiro S, Nishimura K, Matsuo S, Miyasaka J, Nakashima R, Shimada Y, Ueno T, Ikezawa S, Shinozaki K, Katayama K, Wakita T, Takeda N, Oka T (2009) Surveillance of pathogens in outpatients with gastroenteritis and characterization of sapovirus strains between 2002 and 2007 in Kumamoto Prefecture, Japan. J Med Virol 81:1117–1127CrossRefPubMed Harada S, Okada M, Yahiro S, Nishimura K, Matsuo S, Miyasaka J, Nakashima R, Shimada Y, Ueno T, Ikezawa S, Shinozaki K, Katayama K, Wakita T, Takeda N, Oka T (2009) Surveillance of pathogens in outpatients with gastroenteritis and characterization of sapovirus strains between 2002 and 2007 in Kumamoto Prefecture, Japan. J Med Virol 81:1117–1127CrossRefPubMed
32.
go back to reference Román E, Wilhelmi I, Colomina J, Villar J, Cilleruelo ML, Nebreda V, Del Alamo M, Sánchez-Fauquier A (2003) Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children. J Med Microbiol 52:435–440CrossRefPubMed Román E, Wilhelmi I, Colomina J, Villar J, Cilleruelo ML, Nebreda V, Del Alamo M, Sánchez-Fauquier A (2003) Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children. J Med Microbiol 52:435–440CrossRefPubMed
33.
go back to reference Klein EJ, Boster DR, Stapp JR, Wells JG, Qin X, Clausen CR, Swerdlow DL, Braden CR, Tarr PI (2006) Diarrhea etiology in a Children’s Hospital Emergency Department: a prospective cohort study. Clin Infect Dis 43:807–813CrossRefPubMed Klein EJ, Boster DR, Stapp JR, Wells JG, Qin X, Clausen CR, Swerdlow DL, Braden CR, Tarr PI (2006) Diarrhea etiology in a Children’s Hospital Emergency Department: a prospective cohort study. Clin Infect Dis 43:807–813CrossRefPubMed
34.
go back to reference Nakanishi K, Tsugawa T, Honma S, Nakata S, Tatsumi M, Yoto Y, Tsutsumi H (2009) Detection of enteric viruses in rectal swabs from children with acute gastroenteritis attending the pediatric outpatient clinics in Sapporo, Japan. J Clin Virol 46:94–97CrossRefPubMed Nakanishi K, Tsugawa T, Honma S, Nakata S, Tatsumi M, Yoto Y, Tsutsumi H (2009) Detection of enteric viruses in rectal swabs from children with acute gastroenteritis attending the pediatric outpatient clinics in Sapporo, Japan. J Clin Virol 46:94–97CrossRefPubMed
35.
go back to reference Ferreira MS, Xavier Mda P, Tinga AC, Rose TL, Fumian TM, Fialho AM, de Assis RM, Carvalho Costa FA, de Oliveira SA, Leite JP, Miagostovich MP (2012) Assessment of gastroenteric viruses frequency in a children’ day care center in Rio De Janeiro, Brazil: a fifteen year study (1994–2008). PloS One 7:e33754CrossRefPubMedCentralPubMed Ferreira MS, Xavier Mda P, Tinga AC, Rose TL, Fumian TM, Fialho AM, de Assis RM, Carvalho Costa FA, de Oliveira SA, Leite JP, Miagostovich MP (2012) Assessment of gastroenteric viruses frequency in a children’ day care center in Rio De Janeiro, Brazil: a fifteen year study (1994–2008). PloS One 7:e33754CrossRefPubMedCentralPubMed
36.
go back to reference Wiegering V, Kaiser J, Tappe D, Weissbrich B, Morbach H, Girschick HJ (2011) Gastroenteritis in childhood: a retrospective study of 650 hospitalized pediatric patients. Int J Infect Dis 15:e401–e407CrossRefPubMed Wiegering V, Kaiser J, Tappe D, Weissbrich B, Morbach H, Girschick HJ (2011) Gastroenteritis in childhood: a retrospective study of 650 hospitalized pediatric patients. Int J Infect Dis 15:e401–e407CrossRefPubMed
37.
go back to reference Rasanen S, Lappalainen S, Salminen M, Huhti L, Vesikari T (2011) Noroviruses in children seen in a hospital for acute gastroenteritis in Finland. Eur J Pediatr 170:1413–1418CrossRefPubMedCentralPubMed Rasanen S, Lappalainen S, Salminen M, Huhti L, Vesikari T (2011) Noroviruses in children seen in a hospital for acute gastroenteritis in Finland. Eur J Pediatr 170:1413–1418CrossRefPubMedCentralPubMed
38.
go back to reference Gonzalez-Galan V, Sánchez-Fauqier A, Obando I, Montero V, Fernandez M, Torres MJ, Neth O, Aznar-Martin J (2011) High prevalence of community-acquired norovirus gastroenteritis among hospitalized children: a prospective study. Clin Microbiol Infect 17:1895–1899CrossRefPubMed Gonzalez-Galan V, Sánchez-Fauqier A, Obando I, Montero V, Fernandez M, Torres MJ, Neth O, Aznar-Martin J (2011) High prevalence of community-acquired norovirus gastroenteritis among hospitalized children: a prospective study. Clin Microbiol Infect 17:1895–1899CrossRefPubMed
39.
go back to reference Zeng M, Xu X, Zhu C, Chen J, Zhu Q, Lin S, Jie Y, Shu X (2012) Clinical and molecular epidemiology of norovirus infection in childhood diarrhea in China. J Med Virol 84:145–151CrossRefPubMed Zeng M, Xu X, Zhu C, Chen J, Zhu Q, Lin S, Jie Y, Shu X (2012) Clinical and molecular epidemiology of norovirus infection in childhood diarrhea in China. J Med Virol 84:145–151CrossRefPubMed
40.
go back to reference Gao ZY, Huang F, Dou XF, Li J, Yan HQ, Wu XN, Jia L, Wang QY (2010) Study on the etiology of human caliciviruses in Beijing. Chin J Dis Control Prev 16:309–312 Gao ZY, Huang F, Dou XF, Li J, Yan HQ, Wu XN, Jia L, Wang QY (2010) Study on the etiology of human caliciviruses in Beijing. Chin J Dis Control Prev 16:309–312
41.
go back to reference Chan-It W, Thongprachum A, Khamrin P, Kobayashi M, Okitsu S, Mizuguchi M, Ushijima H (2012) Emergence of a new norovirus GII.6 variant in Japan, 2008–2009. J Med Virol 84:1089–1096CrossRefPubMed Chan-It W, Thongprachum A, Khamrin P, Kobayashi M, Okitsu S, Mizuguchi M, Ushijima H (2012) Emergence of a new norovirus GII.6 variant in Japan, 2008–2009. J Med Virol 84:1089–1096CrossRefPubMed
42.
go back to reference Ji J, Zhang Z, Liu G, Liu X, Gao Z, Li X (2012) Surveillance of rotavirus and human calicivirus gastroenteritis in pediatric diarrheal patients in enteric clinics in Beijing. Chin J Health Lab Technol 22:843–846 Ji J, Zhang Z, Liu G, Liu X, Gao Z, Li X (2012) Surveillance of rotavirus and human calicivirus gastroenteritis in pediatric diarrheal patients in enteric clinics in Beijing. Chin J Health Lab Technol 22:843–846
43.
go back to reference Dey SK, Shimizu H, Phan TG, Hayakawa Y, Islam A, Salim AF, Khan AR, Mizuguchi M, Okitsu S, Ushijima H (2009) Molecular epidemiology of adenovirus infection among infants and children with acute gastroenteritis in Dhaka City, Bangladesh. Infect Genet Evol 9:518–522CrossRefPubMed Dey SK, Shimizu H, Phan TG, Hayakawa Y, Islam A, Salim AF, Khan AR, Mizuguchi M, Okitsu S, Ushijima H (2009) Molecular epidemiology of adenovirus infection among infants and children with acute gastroenteritis in Dhaka City, Bangladesh. Infect Genet Evol 9:518–522CrossRefPubMed
44.
go back to reference Chhabra P, Samoilovich E, Yermalovich M, Chernyshova L, Gheorghita S, Cojocaru R, Shugayev N, Sahakyan G, Lashkarashvili M, Chubinidze M, Zakhashvili K, Videbaek D, Wasley A, Vinjé J (2014) Viral gastroenteritis in rotavirus negative hospitalized children <5 years of age from the independent states of the former Soviet Union. Infect Genet Evol 28:283–288CrossRefPubMed Chhabra P, Samoilovich E, Yermalovich M, Chernyshova L, Gheorghita S, Cojocaru R, Shugayev N, Sahakyan G, Lashkarashvili M, Chubinidze M, Zakhashvili K, Videbaek D, Wasley A, Vinjé J (2014) Viral gastroenteritis in rotavirus negative hospitalized children <5 years of age from the independent states of the former Soviet Union. Infect Genet Evol 28:283–288CrossRefPubMed
45.
go back to reference Soli KW, Maure T, Kas MP, Bande G, Bebes S, Luang-Suarkia D, Siba PM, Morita A, Umezaki M, Greenhill AR, Horwood PF (2014) Detection of enteric viral and bacterial pathogens associated with paediatric diarrhoea in Goroka, Papua New Guinea. Int J Infect Dis 27:54–58CrossRefPubMed Soli KW, Maure T, Kas MP, Bande G, Bebes S, Luang-Suarkia D, Siba PM, Morita A, Umezaki M, Greenhill AR, Horwood PF (2014) Detection of enteric viral and bacterial pathogens associated with paediatric diarrhoea in Goroka, Papua New Guinea. Int J Infect Dis 27:54–58CrossRefPubMed
46.
go back to reference Guo L, Xu X, Song J, Wang W, Wang J, Hung T (2010) Molecular characterization of astrovirus infection in children with diarrhea in Beijing, 2005–2007. J Med Virol 82:415–423CrossRefPubMed Guo L, Xu X, Song J, Wang W, Wang J, Hung T (2010) Molecular characterization of astrovirus infection in children with diarrhea in Beijing, 2005–2007. J Med Virol 82:415–423CrossRefPubMed
47.
go back to reference Wang F, Wang YH, Peng JS, Zhou X, Tang L, Kobayashi N, Hu Q, Zhou DJ, Huang HJ, Liu MQ (2011) Genetic characterization of Human astrovirus infection in Wuhan, People’s Republic of China, 2007–2008. Can J Microbiol 57:964–968CrossRefPubMed Wang F, Wang YH, Peng JS, Zhou X, Tang L, Kobayashi N, Hu Q, Zhou DJ, Huang HJ, Liu MQ (2011) Genetic characterization of Human astrovirus infection in Wuhan, People’s Republic of China, 2007–2008. Can J Microbiol 57:964–968CrossRefPubMed
48.
go back to reference Sdiri-Loulizi K, Gharbi-Khélifi H, de Rougemont A, Chouchane S, Sakly N, Ambert-Balay K, Hassine M, Guédiche MN, Aouni M, Pothier P (2008) Acute infantile gastroenteritis associated with human enteric viruses in Tunisia. J Clin Microbiol 46:1349–1355CrossRefPubMedCentralPubMed Sdiri-Loulizi K, Gharbi-Khélifi H, de Rougemont A, Chouchane S, Sakly N, Ambert-Balay K, Hassine M, Guédiche MN, Aouni M, Pothier P (2008) Acute infantile gastroenteritis associated with human enteric viruses in Tunisia. J Clin Microbiol 46:1349–1355CrossRefPubMedCentralPubMed
49.
go back to reference Tran A, Talmud D, Lejeune B, Jovenin N, Renois F, Payan C, Leveque N, Andreoletti L (2010) Prevalence of rotavirus, adenovirus, norovirus, and astrovirus infections and coinfections among hospitalized children in northern France. J Clin Microbiol 48:1943–1946CrossRefPubMedCentralPubMed Tran A, Talmud D, Lejeune B, Jovenin N, Renois F, Payan C, Leveque N, Andreoletti L (2010) Prevalence of rotavirus, adenovirus, norovirus, and astrovirus infections and coinfections among hospitalized children in northern France. J Clin Microbiol 48:1943–1946CrossRefPubMedCentralPubMed
50.
go back to reference Ferreira CE, Raboni SM, Pereira LA, Nogueira MB, Vidal LR, Almeida SM (2012) Viral acute gastroenteritis: clinical and epidemiological features of co-infected patients. Braz J Infect Dis 16:267–272CrossRefPubMed Ferreira CE, Raboni SM, Pereira LA, Nogueira MB, Vidal LR, Almeida SM (2012) Viral acute gastroenteritis: clinical and epidemiological features of co-infected patients. Braz J Infect Dis 16:267–272CrossRefPubMed
51.
go back to reference Marie-Cardine A, Gourlain K, Mouterde O, Castignolles N, Hellot MF, Mallet E, Buffet-Janvresse C (2002) Epidemiology of acute viral gastroenteritis in children hospitalized in Rouen, France. Clin Infect Dis 34:1170–1178CrossRefPubMed Marie-Cardine A, Gourlain K, Mouterde O, Castignolles N, Hellot MF, Mallet E, Buffet-Janvresse C (2002) Epidemiology of acute viral gastroenteritis in children hospitalized in Rouen, France. Clin Infect Dis 34:1170–1178CrossRefPubMed
52.
go back to reference Herrmann JE, Taylor DN, Echeverria P, Blacklow NR (1991) Astroviruses as a cause of gastroenteritis in children. N Engl J Med 324:1757–1760CrossRefPubMed Herrmann JE, Taylor DN, Echeverria P, Blacklow NR (1991) Astroviruses as a cause of gastroenteritis in children. N Engl J Med 324:1757–1760CrossRefPubMed
53.
54.
go back to reference Cheng WX, Ye XH, Yang XM, Li YN, Jin M, Jin Y, Duan ZJ (2010) Epidemiological study of human calicivirus infection in children with gastroenteritis in Lanzhou from 2001 to 2007. Arch Virol 155:553–555CrossRefPubMed Cheng WX, Ye XH, Yang XM, Li YN, Jin M, Jin Y, Duan ZJ (2010) Epidemiological study of human calicivirus infection in children with gastroenteritis in Lanzhou from 2001 to 2007. Arch Virol 155:553–555CrossRefPubMed
55.
go back to reference Tu ET, Bull RA, Greening GE, Hewitt J, Lyon MJ, Marshall JA, McIver CJ, Rawlinson WD, White PA (2008) Epidemics of gastroenteritis during 2006 were associated with the spread of norovirus GII.4 variants 2006a and 2006b. Clin Infect Dis 46:413–420CrossRefPubMed Tu ET, Bull RA, Greening GE, Hewitt J, Lyon MJ, Marshall JA, McIver CJ, Rawlinson WD, White PA (2008) Epidemics of gastroenteritis during 2006 were associated with the spread of norovirus GII.4 variants 2006a and 2006b. Clin Infect Dis 46:413–420CrossRefPubMed
56.
go back to reference Jin M, Xie HP, Duan ZJ, Liu N, Zhang Q, Wu BS, Li HY, Cheng WX, Yang SH, Yu JM, Xu ZQ, Cui SX, Zhu L, Tan M, Jiang X, Fang ZY (2008) Emergence of the GII4/2006b variant and recombinant noroviruses in China. J Med Virol 80:1997–2004CrossRefPubMed Jin M, Xie HP, Duan ZJ, Liu N, Zhang Q, Wu BS, Li HY, Cheng WX, Yang SH, Yu JM, Xu ZQ, Cui SX, Zhu L, Tan M, Jiang X, Fang ZY (2008) Emergence of the GII4/2006b variant and recombinant noroviruses in China. J Med Virol 80:1997–2004CrossRefPubMed
57.
go back to reference Xu J, Yang Y, Sun J, Ding Y (2009) Molecular epidemiology of norovirus infection among children with acute gastroenteritis in Shanghai, China, 2001–2005. J Med Virol 81:1826–1830CrossRefPubMed Xu J, Yang Y, Sun J, Ding Y (2009) Molecular epidemiology of norovirus infection among children with acute gastroenteritis in Shanghai, China, 2001–2005. J Med Virol 81:1826–1830CrossRefPubMed
58.
go back to reference Medici MC, Tummolo F, Albonetti V, Abelli LA, Chezzi C, Calderaro A (2012) Molecular detection and epidemiology of astrovirus, bocavirus, and sapovirus in Italian children admitted to hospital with acute gastroenteritis, 2008–2009. J Med Virol 84:643–650CrossRefPubMed Medici MC, Tummolo F, Albonetti V, Abelli LA, Chezzi C, Calderaro A (2012) Molecular detection and epidemiology of astrovirus, bocavirus, and sapovirus in Italian children admitted to hospital with acute gastroenteritis, 2008–2009. J Med Virol 84:643–650CrossRefPubMed
59.
go back to reference Sdiri-Loulizi K, Hassine M, Gharbi-Khelifi H, Aouni Z, Chouchane S, Sakly N, Neji-Guédiche M, Pothier P, Ambert-Balay K, Aouni M (2011) Molecular detection of genogroup I sapovirus in Tunisian children suffering from acute gastroenteritis. Virus Genes 43:6–12CrossRefPubMed Sdiri-Loulizi K, Hassine M, Gharbi-Khelifi H, Aouni Z, Chouchane S, Sakly N, Neji-Guédiche M, Pothier P, Ambert-Balay K, Aouni M (2011) Molecular detection of genogroup I sapovirus in Tunisian children suffering from acute gastroenteritis. Virus Genes 43:6–12CrossRefPubMed
60.
go back to reference Jeong AY, Jeong HS, Jo MY, Jung SY, Lee MS, Lee JS, Jee YM, Kim JH, Cheon DS (2011) Molecular epidemiology and genetic diversity of human astrovirus in South Korea from 2002 to 2007. Clin Microbiol Infect 17:404–408CrossRefPubMed Jeong AY, Jeong HS, Jo MY, Jung SY, Lee MS, Lee JS, Jee YM, Kim JH, Cheon DS (2011) Molecular epidemiology and genetic diversity of human astrovirus in South Korea from 2002 to 2007. Clin Microbiol Infect 17:404–408CrossRefPubMed
61.
go back to reference Naficy AB, Rao MR, Holmes JL, Abu-Elyazeed R, Savarino SJ, Wierzba TF, Frenck RW, Monroe SS, Glass RI, Clemens JD (2000) Astrovirus diarrhea in Egyptian children. J Infect Dis 182:685–690CrossRefPubMed Naficy AB, Rao MR, Holmes JL, Abu-Elyazeed R, Savarino SJ, Wierzba TF, Frenck RW, Monroe SS, Glass RI, Clemens JD (2000) Astrovirus diarrhea in Egyptian children. J Infect Dis 182:685–690CrossRefPubMed
62.
go back to reference Li L, Phan TG, Nguyen TA, Kim KS, Seo JK, Shimizu H, Suzuki E, Okitsu S, Ushijima H (2005) Molecular epidemiology of adenovirus infection among pediatric population with diarrhea in Asia. Microbiol Immunol 49:121–128CrossRefPubMed Li L, Phan TG, Nguyen TA, Kim KS, Seo JK, Shimizu H, Suzuki E, Okitsu S, Ushijima H (2005) Molecular epidemiology of adenovirus infection among pediatric population with diarrhea in Asia. Microbiol Immunol 49:121–128CrossRefPubMed
63.
go back to reference Uhnoo I, Wadell G, Svensson L, Johansson ME (1984) Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children. J Clin Microbiol 20:365–372PubMedCentralPubMed Uhnoo I, Wadell G, Svensson L, Johansson ME (1984) Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children. J Clin Microbiol 20:365–372PubMedCentralPubMed
64.
go back to reference Soares CC, Volotao EM, Albuquerque MC, Albuquerque MCM, da Silva FM, de Carvalho TRB, Nozawa CM, Linhares RE, Santos N (2002) Prevalence of enteric adenoviruses among children with diarrhea in four Brazilian cities. J Clin Virol 23:171–177CrossRefPubMed Soares CC, Volotao EM, Albuquerque MC, Albuquerque MCM, da Silva FM, de Carvalho TRB, Nozawa CM, Linhares RE, Santos N (2002) Prevalence of enteric adenoviruses among children with diarrhea in four Brazilian cities. J Clin Virol 23:171–177CrossRefPubMed
65.
go back to reference Saderi H, Roustai MH, Sabahi F, Sadeghizadeh M, Owlia P, De Jong JC (2002) Incidence of enteric adenovirus gastroenteritis in Iranian children. J Clin Virol 24:1–5CrossRefPubMed Saderi H, Roustai MH, Sabahi F, Sadeghizadeh M, Owlia P, De Jong JC (2002) Incidence of enteric adenovirus gastroenteritis in Iranian children. J Clin Virol 24:1–5CrossRefPubMed
66.
go back to reference Faden H, Wilby M, Hainer ZD, Rush-Wilson K, Ramani R, Lamson D, Boromisa R (2011) Pediatric adenovirus infection: relationship of clinical spectrum, seasonal distribution, and serotype. Clin Pediatr (Phila) 50:483–487CrossRef Faden H, Wilby M, Hainer ZD, Rush-Wilson K, Ramani R, Lamson D, Boromisa R (2011) Pediatric adenovirus infection: relationship of clinical spectrum, seasonal distribution, and serotype. Clin Pediatr (Phila) 50:483–487CrossRef
67.
68.
go back to reference Silva PA, Stark K, Mockenhaupt FP, Reither K, Weitzel T, Ignatius R, Saad E, Seidu-Korkor A, Bienzle U, Schreier E (2008) Molecular characterization of enteric viral agents from children in northern region of Ghana. J Med Virol 80:1790–1798CrossRefPubMed Silva PA, Stark K, Mockenhaupt FP, Reither K, Weitzel T, Ignatius R, Saad E, Seidu-Korkor A, Bienzle U, Schreier E (2008) Molecular characterization of enteric viral agents from children in northern region of Ghana. J Med Virol 80:1790–1798CrossRefPubMed
Metadata
Title
Molecular characterization and multiple infections of rotavirus, norovirus, sapovirus, astrovirus and adenovirus in outpatients with sporadic gastroenteritis in Shanghai, China, 2010–2011
Authors
Lijuan Lu
Ran Jia
Huaqing Zhong
Menghua Xu
Liyun Su
Lingfeng Cao
Zuoquan Dong
Niuniu Dong
Jin Xu
Publication date
01-05-2015
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 5/2015
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-015-2387-1

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