Arch Virol DOI 10.1007/s00705-015-2387-1

ORIGINAL ARTICLE

Molecular characterization and multiple infections of rotavirus, norovirus, sapovirus, astrovirus and adenovirus in outpatients with sporadic gastroenteritis in Shanghai, China, 2010–2011 Lijuan Lu • Ran Jia • Huaqing Zhong • Menghua Xu • Liyun Su • Lingfeng Cao Zuoquan Dong • Niuniu Dong • Jin Xu



Received: 24 November 2014 / Accepted: 27 February 2015 Ó Springer-Verlag Wien 2015

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

L. Lu and R. Jia contribute equally to this manuscript. L. Lu  R. Jia  H. Zhong  M. Xu  L. Su  L. Cao  Z. Dong  N. Dong  J. Xu (&) Department of Clinical Laboratory, Children’s Hospital of Fudan University, 399 Wanyuan Road, Shanghai 201102, China e-mail: [email protected]

information for future vaccination strategies and development in this area.

Introduction Acute diarrhea in children is a global public health problem and a major cause of death in children in developing areas. At least 120 types of pathogens can cause diarrhea, and more than 50 % of infant diarrhea cases are caused by viruses, predominantly rotavirus, norovirus, sapovirus, human astrovirus and adenovirus [1–4]. Rotavirus (RV) is one of the most important viruses, and it causes a large proportion of acute gastroenteritis cases in infants and young children worldwide. In China, RV was responsible for approximately 10–50 deaths per 100,000 children less than 5 years of age [5]. Norovirus (NoV) and sapovirus (SaV) belong to the human calicivirus (HuCV) family; however, these viruses are genetically diverse and exhibit different pathogenicity. NoV is the second-most frequent etiological agent of acute gastroenteritis in young children. In developing countries, NoV has been estimated to cause up to 200,000 deaths each year in children \5 years of age [6]. The detection rate of SaV is typically much lower than that of NoV, and SaV appears to produce symptoms milder than those of NoV. In addition, SaV can cause viral gastroenteritis in sporadic cases as well as outbreaks of diarrhea in all age groups [2, 7, 8]. Human adenovirus (HAdV) is associated with a longer duration of watery diarrhea than other causes of diarrhea, and an increased number of patients present with vomiting compared with patients with RV infections. HAdV has also been implicated in acute respiratory and urinary tract infection, besides gastrointestinal infection. To date, 60

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HAdV serotypes have been identified, of which only genotypes 40, 41, and rarely 38 have been found to be associated with acute gastroenteritis [9]. HAdV typically accounts for 0.4 % to 17.6 % of acute gastroenteritis in children, and the detection rate is higher in developing countries than in developed countries [10–14]. The severity of human astrovirus (HAstV) diarrhea is much less than that observed with RV because of the shorter duration of vomiting and diarrhea, and its prevalence rate in sporadic cases varies from 3.2 % to 14 % in different regions [10, 12, 14–18]. In previous studies, our workgroup had collected and analyzed specimens from hospitalized children with acute diarrhea in Shanghai from 2010 to 2011 and summarized the epidemiological and clinical data for RV and NoV infections [19–21]. However, detailed data on the prevalence rates of RV, NoV, SaV, HAstV and HAdV in outpatient children with acute diarrhea in this area have not been reported. The aim of this study was to describe the genetic characteristics and to compare the importance of these five viruses in outpatient children with acute diarrhea in Shanghai from 2010 to 2011. These findings will provide baseline information for future vaccination strategies and development in Shanghai.

Material and methods Stool collection A total of 436 samples were randomly collected by the systematic sampling method from 25,112 pediatric patients (B5 years) who were admitted to the outpatient department with a clinical diagnosis of acute gastroenteritis in Children’s Hospital of Fudan University during the period from January 2010 to December 2011. This hospital is a public and tertiary general specialist children’s hospital in Shanghai, China. Among the enrolled patients, 3.4 % of children were divided into high-income groups, 60.8 % of children were divided into middle-income groups and 35.8 % of children belonged to low-income groups. The criteria for acute gastroenteritis were defined as C3 instances of loose stool or looser-than-normal stool within a 24-hour period combined with significant changes to the fecal exterior, including watery or thin paste texture and the presence of mucous; the definition excluded the presence of pus or blood, regardless of the fever conditions. The fecal specimens were collected during a clinical visit till further processed and frozen at -70 °C after routine laboratory detection. All samples were from different patients. Because the stool specimens were collected during the normal course of patient care, informed consent from

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each patient was not required, but the whole study proposal has been reviewed by the Institutional Review Board in our hospital. Viral RNA/DNA extraction Nucleic acids were extracted from 10 % fecal suspensions in 0.9 % physiological saline using a TIANamp Virus DNA/RNA Kit (Tiangen Biotech, Beijing, China) according to the manufacturer’s instructions. The extracted viral RNA/DNA was dissolved in 40 lL of nuclease-free water and stored at -70 °C until analysis. Detection and genotyping of group A rotavirus All of the samples were subjected to G and P genotyping using one-step reverse transcription PCR (RT-PCR) and semi-nested PCR with type-specific primers, as described previously [22] (Table 1). Detection of NoV, SaV, HAstV and HAdV The presence of NoV and SaV was confirmed by RT-PCR amplification of a 331-bp or 319-bp fragment, respectively, of the RdRp gene, as reported previously [19]. HAdV was analyzed by PCR amplification of a 482-bp fragment located in the hexon gene, using the primers Ad1 and Ad2 as described previously [10]. The HAstV strains were confirmed by RT-PCR by amplifying a partial region of ORF2 as previously described, to generate a product with a predicted size of 449-bp [23] (Table 1). Molecular characterization of NoV-, SaV-, HAstVand HAdV-positive samples All of the positive amplification products were purified and sequenced using first-generation sequencing technologies and the same primers that were used for their amplification (Sunny Biotechnology Co., Ltd.). The sequence alignments and molecular characterization were conducted using the Kimura 2-parameter method as a model of nucleotide substitution, and the phylogenetic trees were generated by MEGA version 5.05 [24] using the neighbor-joining method with 1,000 bootstrap replicates of the sequence alignment datasets.

Results Detection of viral agents in outpatients with diarrhea Among the 436 stool specimens collected from the outpatients (age B5 years) presenting with diarrhea from 2010

Viruses causing gastroenteritis in children in China Table 1 Primers used for detection of RV, HuCV (NoV and SaV), HAdV and HAstV

Virus RV

HuCV

HAdV HuCV: 331 bp for NoV, 319 bp for SaV; (?): forward primer; (-): reverse primer

HAstV

Primer

Genotype

Sequence (50 –30 )

PCR product (bp)

9Con1

G (?)

TAGCTCCTTTTAATGTATGG

9Con2

G (-)

GTATAAAAATACTTGCCACCA

905

9T1

G1 (-)

TCTTGTCAAAGCAAATAATG

159

9T2

G2 (-)

GTTAGAAATGATTGTCCACT

245

9T3

G3 (-)

GTCCAGTTGCAGTGTTAGC

467

9T4

G4 (-)

GGGTCGATGGAAAATTCT

404

9T9B

G9 (-)

TATAAAGTCCATTGCAC

111

4Con2

P (-)

ATTTCGGACCATTTATAACC

4Con3

P (?)

TGGCTTCGCCATTTTATAGACA

877

1T1

P[8] (-)

TCTACTTGGATAACGTGC

346

2T1

P[4] (-)

CTATTGTTAGAGGTTAGAGTC

484

3T1

P[6] (-)

TGTTGATTAGTTGGATTCAA

268

4T1

P[9] (-)

TGAGACATGCAATTGGAC

392

5T1

P[10] (-)

ATCATAGTTAGTAGTCGG

584

289H 289I

(-) (-)

TGACGATTTCATCATCACCATA TGACGATTTCATCATCCCCGTA

290H

(?)

GATTACTCCAGGTGGGACTCCAC

290I

(?)

GATTACTCCAGGTGGGACTCAAC

290J

(?)

GATTACTCCAGGTGGGATTCAAC

290K

(?)

GATTACTCCAGGTGGGATTCCAC

Ad1

(?)

TTCCCCATGGCICAYAACAC

Ad2

(-)

CCCTGGTAKCCRATRTTGTA

Mon269

(?)

CAACTCAGGAAACAGGGTGT

Mon270

(-)

TCAGATGCATTGTCATTGGT

to 2011, 66.7 % (291/436) of patients contained at least one of the five viruses tested. Among those specimens, RV was the most common virus and was identified in 43.3 % (189/436), whereas NoV was found in 28.9 % (126/436), and HAdV, HAstV and SaV were detected in 7.1 % (31/ 436), 1.8 % (8/436) and 0.5 % (2/436) of samples, respectively. Of the 436 stool specimens, single infections were detected in 226 (51.8 %) of the 436 specimens, whereas mixed virus infections were detected in 65 (14.9 %) of the same specimens (Fig. 1A and B). RV was the most common virus in single infections (58.0 % of 226), followed by NoV (31.0 % of 226). The most frequent multiple viruses infections were RV and NoV (76.9 % of 65), NoV and HAdV (9.2 % of 65) and RV and HAdV (7.7 % of 65) (Fig. 1C and D). RV and HuCV infections were identified throughout the year. Peaks of RV infection occurred in October (70.0 %) and November (66.7 %) while the peaks for HuCV infection were in June (60.0 %) and September (66.7 %). The highest rates of HAdV infection were in February, March and May (16.7 %, 16.7 % and 13.3 %), respectively. The majority (10.0 %) of the HAstV infections were detected in

331/319 482 449

September, but no seasonal pattern could be determined, as only eight samples were positive for this virus (Fig. 2). Molecular characterization of RV-positive samples Among the RV-positive patients, the most prevalent G type during the study period was G1 (31.2 %, 59/189), which was followed by G3 (28.6 %, 54/189) and G9 (27.0 %, 51/189). P[8] (91.0 %, 172/189) was the most predominant P genotype, followed by P[4] (5.3 %, 10/189). When the G and P types were combined, P[8]G3, P[8]G1 and P[8]G9 were predominant and accounted for 27.5 % (52/189), 26.9 % (51/189) and 25.4 % (48/189) of RV-positive cases, respectively (Table 2). Molecular characterization of NoV-, SaV-, HAstVand HAdV-positive samples All of the NoV strains belonged to the GII genogroup, and the majority clustered with GII.4 (73.0 %, 92/126), followed by GII.b (15.9 %, 20/126) and GII.12 (9.5 %, 12/126). NoV GII.7 (0.8 %, 1/126) and GII.2 (0.8 %, 1/126) were also identified (Fig. 3). The two SaV-positive

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L. Lu et al. Fig. 1 Distribution of RV, NoV, SaV, HAdV and HAstV in 291 positive stool samples out of a total of 436 from outpatient children in Shanghai during 2010 to 2011. (A–B) Detection rate (%) of each virus in single (n = 226) and mixed (n = 65) infections. (C–D) Distribution (%) of single (n = 226) and mixed (n = 65) infections

(16.1 %, 5/31). Additionally, HAdV-12 (2 cases), HAdV-2 (1 case), HAdV-5 (1 case) and HAdV-19 (1 case) were identified (Fig. 6).

Discussion

Fig. 2 Seasonality of RV, HuCV, HAdV and HAstV infections in outpatient children\5 years of age in Shanghai during 2010 and 2011

samples were sequenced and classified as genotypes GI.1 and GII.2 (Fig. 4). Phylogenetic analysis based on RdRp nucleotide sequences demonstrated that all of the eight HAstVs could be classified as HAstV1 (Fig. 5). The sequence identities of the positive HAdV samples were confirmed by sequence analysis. HAdV-41 (45.2 %, 14/31) was the most common viral agent of gastroenteritis in children, followed by type 3 (22.6 %, 7/31) and type 40

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Few studies have been performed to determine the prevalence of RV, NoV, SaV, HAstV and HAdV in outpatient children with acute diarrhea in Shanghai. In this study, these viral pathogens were identified in 66.7 % of specimens. With respect to pathogen distribution, our results are consistent with those of previous studies in which RV was found to be the most frequently detected viral causative agent for gastroenteritis in children, followed by NoV, HAdV, HAstV and SaV [4, 10, 11]. Of these five viruses, RV accounted for 43.3 % of the cases, and this result was similar to the results of most studies at home and abroad (32.2–44.5 %) [25–29]; however, this prevalence was higher than that reported in some areas of southeastern China, Japan, Spain and Washington, D.C. (USA)

Viruses causing gastroenteritis in children in China Table 2 Distribution of combinations of G and P types among RVpositive specimens collected from outpatients at Children’s Hospital, Fudan University, Shanghai, China, from 2010 to 2011 P type/G type

2010–2011 %

Total

P[8]G1

26.9 %

P[8]G2

1.1 %

2

P[8]G3

27.5 %

52

P[8]G9

25.4 %

48

P[8]Gm

10.1 %

19

P[4]G1

2.1 %

4

P[4]G2

1.6 %

3

P[4]G3

1.1 %

2

P[4]Gm

0.5 %

1

P[10]G9

1.1 %

2

PmG1

1.6 %

3

PmG3

0.5 %

1

PmG9

0.5 %

1

100.0 %

189

Total

51

Gm mixed genotype, Pm mixed P genotype

(11.6–25.5 %) [30–34]. NoV was the second-most significant etiological agent (28.9 %) in outpatient children with diarrhea, which is consistent with the results from studies in China and other areas (26.0–36.0 %) [35–40]. Researchers in Japan have demonstrated that NoV is the most predominant pathogen, with a detection rate as high as 50.0 % in children with diarrhea [31, 41]. These data suggest that NoV has played an increasingly significant role in worldwide cases of sporadic diarrhea in infants and young children. The seasonal distribution of each of those viruses was distinct. RV was the most frequently detected virus in children with diarrhea from 2010 to 2011 in Shanghai; however, the detection rate of NoV infections in outpatients was unexpectedly and remarkably higher than that of RV in June (60.0 % vs. 43.3 %) and September (66.7 % vs. 56.7 %). A similar phenomenon in peak months was observed in outpatients in Beijing [42]. In our study, we observed high prevalence of HAdV in February, March and May, which was similar to the results of a study conducted in Bangladesh, but different from what was observed in Tanzania [9, 43]. Because of the limited numbers, no seasonal pattern could be concluded based on the prevalence of HAstV in this study, which is consistent with a study in the independent states of the former Soviet Union [44]. The positivity rate for HAdV (7.1 %) in this study was higher than that in other areas such as southeastern China, Japan, Spain and the USA (2.7–4.8 %) but lower than that in Goroka, Papua New Guinea (11.6 %) [9, 30–34, 41, 44,

45]. The difference in the pathogen detection rates may be partly explained by the different primer sets used. In our experimental design, the primers used to test HAdV could detect HAdV A-F, including 51 serotypes, whereas other studies have typically monitored only HAdV-40 and HAdV-41. The 1.8 % incidence of diarrhea caused by HAstV in our study is similar to that observed in outpatients in other areas (1.1 %–6.5 %) [30, 32–34, 41] but obviously lower than that observed in Beijing (7.8 %) and Wuhan (13.6 %), China, which suggests that HAstV played a subordinate causative role in outpatient children with diarrhea in Shanghai [46, 47]. The comprehensive detection of the five viruses showed that there was a high percentage (14.9 %) of co-infection in this study among the positive samples, and all of these combinations involved two infectious agents. The results obtained from this study were consistent with those of previous studies, which have reported worldwide occurrence rates of viral co-infections ranging from 1.6 % to 19 % [3, 12, 18, 48–51]. As in previous studies [49, 51– 53], RV ? NoV appeared to be the most frequent mixed infection, followed by NoV ? HAdV. RV was the viral agent most frequently implicated in co-infections in this study, confirming the importance of RV as the major pathogen of pediatric diarrhea in Shanghai. Both domestically and abroad, few studies have investigated the presence of the G and P RV genotypes in outpatients. Our previous study of hospitalized children showed that the most frequently observed G genotype from 2010 to 2011 was G3, followed by G9 [20]. Genotype G9 was detected in only one out of 363 RV-positive samples between 2001 and 2005 [22]. This finding indicates that G9 has only recently developed into a common genotype and may become the predominant G genotype in outpatient and hospitalized children with acute diarrhea in Shanghai. Therefore, additional surveillance of active strains is required to monitor the varying pattern of the G genotype. Consistent with the frequency of combinations worldwide, the predominant combinations in this study were G3P[8] (27.5 %), G1P[8] (26.9 %) and G9P[8] (25.4 %). In previous studies conducted in hospitalized children in Shanghai from 2001 to 2011, G3P[8] was the most common combination; however, a significant decrease in the prevalence of this strain has occurred since 2008, whereas the occurrence of G9P[8] increased, and it became the leading genotype in 2011 [20–22]. The variability of RV genotypes has been reported and appears to be dependent on the continent and source of the specimens (hospitalized children and outpatients), which confirms the spatial and temporal variations and evolution of RV strains. A total of 128 HuCV strains (126 NoVs and 2 SaVs) were detected in this study. These data correlate with previous studies that showed higher proportions of NoV

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Fig. 3 Phylogenetic tree of NoV strains from NoV-positive children with sporadic gastroenteritis treated as outpatients at Children’s Hospital, Fudan University, Shanghai, China, from 2010–2011. The

tree was generated using to the neighbor-joining method and based on partial sequences of the RdRp gene (319 bp). Black dots indicate the reference strains

and lower proportions of SaV [2, 54]. GII.4 was characterized as the predominant strain, which is consistent with other studies of pediatric diarrhea [25, 35, 41]. Although GII.4 NoV variants emerge consecutively worldwide every 2–3 years, the GII.4-2006b variant has remained dominant, as reported in other studies in recent years [12, 39, 55]. The GII.b strain was the subordinate variant in outpatients, with 18 cases occurring in 2011 and 2 cases occurring in 2010,

and this finding was the first epidemiological report of the GII.b strain in China [39, 56, 57]. However, the GII.3 strain, which was identified as the second-most prevalent genotype in hospitalized children in Shanghai prior to 2006, was not detected [57]. A novel finding in this study was that SaV infection was confirmed with a detection rate of 0.5 % for the first time in Shanghai. This result is consistent with previous reports on

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Viruses causing gastroenteritis in children in China

Fig. 4 Phylogenetic dendrogram of the nucleotide sequences of the SaV isolates collected from outpatient children with acute diarrhea at Children’s Hospital, Fudan University, Shanghai, China, from 2010 to 2011. The dendrogram was generated using the neighbor-joining method based on a 331-bp sequence of the RdRp gene. Black dots indicate the reference strains

SaV epidemiology in areas in the world in which its prevalence has been shown to range from 0.3 % to 9.3 % [54, 58, 59]. Of the reported cases of SaV, one SaV belongs to GI.2 and the other belongs to GII.1. Because SaV was not found in the children hospitalized for diarrhea in the same period in Shanghai, this result was similar to reports

from Japan and Tunisia, where SaV was only identified in outpatient children [57, 59]. The epidemiological data on HAstV as a causative agent of gastroenteritis in Shanghai are rather limited. HAstV-1 was the predominant and only serotype found in this study, which is consistent with reports from most parts of the world [9, 12, 16–18]. However, in addition to HAstV-1, other minor genotypes were found in other regions. HAstV-3 infection has previously been identified in Wuhan and Beijing, China [40, 47]. In South Korea and Egypt, diverse genotypes of HAstV have been reported, including HAstV-1, HAstV-2, HAstV-3, HAstV-4, HAstV-5, HAstV6 and HAstV-8 [60, 61]. This article provides the first description of the molecular epidemiology of HAdV in outpatients in Shanghai. The enteric adenoviruses (HAdV-41 and HAdV-40) were found to constitute 61.3 % of the HAdV-positive cases. The molecular characterization of the enteric adenovirus strains showed a clear predominance of HAdV-41 (45.2 %) while the incidence of HAdV-40 (16.1 %) was lower, which is consistent with numerous studies in various parts of the world [11, 12, 62, 63]. However, HAdV-40 and HAdV-41 infections were reported to occur at equal frequency in diarrhea children in some areas [44, 64, 65].

Fig. 5 Phylogenetic tree of HAstV nucleotide sequences. The neighbor-joining phylogenetic tree is based on the nucleotide sequences of the capsid region of the HAstV genome. Black dots indicate the reference strains

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L. Lu et al. Fig. 6 Phylogenetic analysis of HAdV strains from outpatient children based on the partial nucleotide sequence (482 bp) of the hexon gene of HAdV. Black dots indicate the reference strains

Some studies have reported that antigenic drift of HAdV41 has led to an increase in HAdV-41 prevalence and a decrease in HAdV-40 [9, 13]. HAdV-3 has been shown to cause keratoconjunctivitis; however, HAdV-3 (22.6 %) was the secondary genotype in our study (HAdV-40 was previously secondary at 16.1 %) and occurred most frequently in February and March. Additionally, HAdV-3 has also been detected in a child with diarrhea in New York [66]. These data suggest that different HAdV genotypes could trigger similar symptoms in children; however, further research is required. Consistent with studies in Lanzhou and Tianjin in China, Japan and Ghana [9, 12, 62, 67, 68], we found that other types of HAdV were detected less frequently in children presenting with diarrhea, including HAdV-12, HAdV-2, HAdV-5 and HAdV-19. This phenomenon indicates that other ‘‘nonenterovirus’’ pathogens are significant in children with diarrhea, which requires additional attention from physicians. In summary, this study clearly shows the diversity of the viral causative agents of acute gastroenteritis in outpatient children in Shanghai. These data will provide baseline information for future vaccination strategies and development in this area.

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Acknowledgment This work was supported by the Program of the National Natural Science Foundation of China (NSFC81273204).

References 1. Kapikian AZ (1993) Viral gastroenteritis. JAMA 269:627–630 2. Moreno-Espinosa S, Farkas T, Jiang X (2004) Human caliciviruses and pediatric gastroenteritis. Semin Pediatr Infect Dis 15:237–245 3. Ramani S, Kang G (2009) Viruses causing childhood diarrhoea in the developing world. Curr Opin Infect Dis 22:477–482 4. Anderson EJ (2010) Prevention and treatment of viral diarrhea in pediatrics. Expert Rev Anti Infect Ther 8:205–217 5. 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–S15 6. 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 14:1224–1231 7. 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 18:420–426 8. Rockx B, De Wit M, Vennema H, Vinje´ J, De Bruin E, Van Duynhoven Y, Koopmans M (2002) Natural history of human

Viruses causing gastroenteritis in children in China

9.

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

23.

24.

calicivirus infection: a prospective cohort study. Clin Infect Dis 35:246–253 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 14:666 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 44:238–241 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 79:582–590 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 157:881–887 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 7:279–284 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 150:2061–2075 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 32:1841–1845 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 80:298–305 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 35:64–68 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 73:256–261 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 159:1613–1621 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, 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 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 44:58–61 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 33:797–801 Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using

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26.

27.

28.

29.

30.

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32.

33.

34.

35.

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37.

38.

39.

maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 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 30:1244–1254 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 74:173–179 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 85:354–362 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 43:904–916 Sa´nchez-Fauquier A, Montero V, Colomina J, Gonza´lez-Gala´n 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 52:353–358 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–e290 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 81:1117–1127 Roma´n E, Wilhelmi I, Colomina J, Villar J, Cilleruelo ML, Nebreda V, Del Alamo M, Sa´nchez-Fauquier A (2003) Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children. J Med Microbiol 52:435–440 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 43:807–813 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 46:94–97 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:e33754 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–e407 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 170:1413–1418 Gonzalez-Galan V, Sa´nchez-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 17:1895–1899 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 84:145–151

123

L. Lu et al. 40. 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. 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 84:1089–1096 42. 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. 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 9:518–522 44. 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, Vinje´ 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 28:283–288 45. 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 27:54–58 46. 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 82:415–423 47. 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 57:964–968 48. Sdiri-Loulizi K, Gharbi-Khe´lifi H, de Rougemont A, Chouchane S, Sakly N, Ambert-Balay K, Hassine M, Gue´diche MN, Aouni M, Pothier P (2008) Acute infantile gastroenteritis associated with human enteric viruses in Tunisia. J Clin Microbiol 46:1349–1355 49. 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 48:1943–1946 50. 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 16:267–272 51. 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 34:1170–1178 52. Herrmann JE, Taylor DN, Echeverria P, Blacklow NR (1991) Astroviruses as a cause of gastroenteritis in children. N Engl J Med 324:1757–1760 53. Walter JE, Mitchell DK (2003) Astrovirus infection in children. Curr Opin Infect Dis 16:247–253 54. Cheng WX, Ye XH, Yang XM, Li YN, Jin M, Jin Y, Duan ZJ (2010) Epidemiological study of human calicivirus infection in

123

55.

56.

57.

58.

59.

60.

61.

62.

63.

64.

65.

66.

67.

68.

children with gastroenteritis in Lanzhou from 2001 to 2007. Arch Virol 155:553–555 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 46:413–420 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 80:1997–2004 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 81:1826–1830 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 84:643–650 Sdiri-Loulizi K, Hassine M, Gharbi-Khelifi H, Aouni Z, Chouchane S, Sakly N, Neji-Gue´diche M, Pothier P, Ambert-Balay K, Aouni M (2011) Molecular detection of genogroup I sapovirus in Tunisian children suffering from acute gastroenteritis. Virus Genes 43:6–12 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 17:404–408 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 182:685–690 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 49:121–128 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 20:365–372 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 23:171–177 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 24:1–5 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) 50:483–487 Kim M, Lim MY, Ko G (2010) Enhancement of enteric adenovirus cultivation by viral transactivator proteins. Appl Environ Microbiol 76:2509–2516 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 80:1790–1798

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

Rotavirus (RV), norovirus (NoV), sapovirus (SaV), human astrovirus (HAstV) and human adenovirus (HAdV) are significant because they are the most commo...
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