Review

Comprehensive Review of Human Sapoviruses

Tomoichiro Oka, Qiuhong Wang, Kazuhiko Katayama, Linda J. Saif
DOI: 10.1128/CMR.00011-14

SUMMARY

Sapoviruses cause acute gastroenteritis in humans and animals. They belong to the genus Sapovirus within the family Caliciviridae. They infect and cause disease in humans of all ages, in both sporadic cases and outbreaks. The clinical symptoms of sapovirus gastroenteritis are indistinguishable from those caused by noroviruses, so laboratory diagnosis is essential to identify the pathogen. Sapoviruses are highly diverse genetically and antigenically. Currently, reverse transcription-PCR (RT-PCR) assays are widely used for sapovirus detection from clinical specimens due to their high sensitivity and broad reactivity as well as the lack of sensitive assays for antigen detection or cell culture systems for the detection of infectious viruses. Sapoviruses were first discovered in 1976 by electron microscopy in diarrheic samples of humans. To date, sapoviruses have also been detected from several animals: pigs, mink, dogs, sea lions, and bats. In this review, we focus on genomic and antigenic features, molecular typing/classification, detection methods, and clinical and epidemiological profiles of human sapoviruses.

INTRODUCTION

Sapoviruses cause acute gastroenteritis in humans and animals. They belong to the genus Sapovirus within the family Caliciviridae. Sapovirus infections are a public health problem because they cause acute gastroenteritis in people of all ages in both outbreaks and sporadic cases worldwide. Outbreaks often occur in semiclosed settings. Outbreaks caused by foodborne transmission of sapovirus have also been reported. In this comprehensive review, we focus mainly on human sapoviruses.

HISTORY

Sapovirus particles are small (about 30 to 38 nm in diameter) and icosahedral and have cup-shaped depressions on the surface, which is a typical calicivirus morphology (Fig. 1) (1). Sapovirus particles were first detected in human diarrheic stool samples in 1976 in the United Kingdom using electron microscopy (EM) (2), and the virus was soon recognized as a new gastroenteritis pathogen (3 – 11). However, the prototype strain of the Sapovirus genus was from another outbreak in Sapporo, Japan, in 1982 (strain Hu/SaV/Sapporo/1982/JPN), because it has been studied extensively for sapovirus virological and genetic characteristics (10, 12 – 14).

FIG 1
FIG 1

Transmission electron micrographs of sapovirus and norovirus particles from clinical samples. Scale bars indicate 100 nm. (Courtesy of Yasutaka Yamashita, Ehime Prefectural Institute of Public Health and Environmental Science, Japan.)

TAXONOMY

Sapoviruses were previously called “typical human caliciviruses” or “Sapporo-like viruses.” In 2002, The International Committee on the Taxonomy of Viruses assigned these viruses to the species Sapporo virus, genus Sapovirus, in the family Caliciviridae (15). Currently, the family Caliciviridae consists of five established genera, Sapovirus, Norovirus, Lagovirus, Vesivirus, and Nebovirus (http://www.ictvonline.org/virusTaxonomy.asp), whereas five new genera (Bavovirus, Nacovirus, Recovirus, Valovirus, and Secalivirus) have been proposed (16 – 20).

CELL CULTURE AND ANIMAL INFECTION TRIALS

Attempts to grow human sapoviruses in cell cultures (2, 4, 5, 9, 21 – 24), have been reported, and two studies describe the propagation of sapoviruses in green monkey kidney cells (23) or primary human embryo kidney cells in the presence of trypsin and actinomycin D (Table 1) (24); however, no confirmed reproduction of these data is available. Currently, only a few porcine sapovirus strains have been grown successfully in primary porcine kidney cells or a porcine kidney cell line (i.e., LLC-PK1) in the presence of porcine intestinal contents or bile acids (Table 1) (25 – 28). Bile acids likely support porcine sapovirus replication via escape from endosomes during the virus entry step (29). Also, a cellular cyclic AMP (cAMP) signaling pathway induced by intestinal contents or bile acids likely causes downregulation of innate immunity (25, 30). An infection trial of human sapoviruses in mice did not succeed (5). Currently, only the specific porcine sapovirus (Cowden strain) has been studied for its pathogenesis in gnotobiotic pigs (31 – 33).

View this table:
TABLE 1

Cell culture trials for human and animal sapoviruses

PHYSICAL CHARACTERISTICS AND STABILITY

Sapovirus is a nonenveloped virus, and the virus has a buoyant density of 1.36 to 1.41 g/cm3 (5, 22, 34, 35). The stability of porcine sapovirus under physicochemical treatment is as follows: (i) stable at pH 3.0 to 8.0 at room temperature for 1 h, (ii) sensitive to ethanol treatment (60% and 70%) at room temperature for 30 s, (iii) inactivated by 200 mg/liter (or ppm) sodium hypochlorite at room temperature for 30 min, and (iv) inactivated by heating at 56°C for 2 h (36).

GENOMIC ORGANIZATION

The sapovirus genome has a positive-sense, single-stranded RNA genome, which is approximately 7.1 to 7.7 kb in size and has a 3′-end poly(A) tail. The sapovirus genome contains two open reading frames (ORFs) (Fig. 2). ORF1 encodes a large polyprotein containing the nonstructural proteins followed by the major capsid protein, VP1 (Fig. 2). ORF2 is predicted to encode the minor structural protein VP2 (Fig. 2) (28, 37). A similar genomic organization (i.e., two ORFs, with the first ORF encoding the nonstructural proteins and VP1) is found in other calicivirus genera, such as Lagovirus, Nebovirus, and the newly proposed genera Valovirus, Bavovirus, and Nacovirus (17, 19, 20, 38, 39). The genomic organization of Norovirus, Vesivirus, and Recovirus differs from that of Sapovirus: ORF1 encodes nonstructural proteins, and ORF2 and ORF3 encode structural proteins VP1 and VP2, respectively (18, 37, 40). A third ORF (ORF3) has been predicted in several human (12, 41 – 47) and bat (48) sapovirus strains; however, its function is unknown.

FIG 2
FIG 2

Diagram of sapovirus genomic organization and the RT-PCR target regions for human sapoviruses based on the GI.1 Manchester strain (GenBank accession no. X86560). A schematic diagram of the sapovirus genomic organization, including the putative subgenomic transcript, two common open reading frames (ORF1 and ORF2), the predicted viral nonstructural proteins (NS1, NS2, NS3 [NTPase], NS4, NS5 [VPg], and NS6-NS7 [protease–RNA-dependent RNA polymerase {RdRp}]), and structural proteins VP1 and VP2 is shown. The putative cleavage sites in the ORF polyprotein and their predicted sizes are indicated, according to previous reports (37, 41, 42, 49 – 51, 55, 272). Typical amino acid motifs for NS3 (GAPGIGKT), NS5 (KGKTK and DDEYDE), NS6 (GDCG), NS7 (WKGL, KDEL, DYSKWDST, GLPSG, and YGDD) and VP1 (PPG and GWS) are also shown. An overview of the RT-PCR target regions (RdRp region, RdRp-VP1 junction region, and VP1 region) is shown, and the detailed primer information is summarized in Tables 2 to 4. The putative first amino acids of VP1 from subgenomic transcript “MEG” and the cleavage site of this motif (ME/G; the slash indicates the cleavage site) from the ORF1 polyprotein are also shown with their nucleotide positions. The putative NS7 (RdRp) region and the cleavage site between RdRp and VP1 are based on previous reports (50, 52, 55, 58). The proposed subdomains in the sapovirus VP1 from the subgenomic transcript (N-terminal variable region [NVR] [1 to 43]), N-terminal region [N] [44 to 285]), central variable region [CVR] [286 to 441]), and C-terminal region [C] [442 to 561]) (47) are also indicated.

The ORF1-encoded polyprotein is expressed and processed into at least six nonstructural (NS) proteins (NS1, NS2, NS3, NS4, NS5, and NS6-NS7) and a structural protein (VP1) by virus-encoded protease (Fig. 2) (49 – 54). In vitro studies failed to show cleavage of the NS6-NS7 protein by the viral protease (28, 49, 50, 52, 55, 56), although both the NS6 and NS7 proteins can carry out their respective functions (proteolytic and polymerase) when expressed individually in vitro (56 – 58). The NS6-NS7 protein was also detected in porcine sapovirus-infected cells (28). Similar to the case for sapoviruses, vesivirus also produces the NS6-NS7 protein (fused protease-polymerase) (52, 53, 59 – 61), whereas noroviruses and lagoviruses produce an individual protease and polymerase, NS6 and NS7, respectively (51, 53, 62 – 67). The biological functions of the other sapovirus NS proteins have not been experimentally determined; however, NS3 and NS5 have a typical calicivirus NTPase motif (GAPGIGKT) and VPg motifs (KGKTK and DDEYDE), respectively (Fig. 2) (37, 49, 68, 69). VPg is linked to the 5′ end of the viral RNA and is critical for calicivirus genome replication, transcription, and translation (37, 70).

VP1, an approximately 60-kDa protein, is a major component of the complete virus (34, 35). Two mechanisms can be considered in the production of sapovirus VP1. One is that VP1 is cleaved from the ORF1-encoded polyprotein, and the other is that VP1 is translated from a subgenomic RNA (from the 3′-coterminal RNA corresponding to VP1 to the genome end region) (Fig. 2) (71, 72). A subgenomic RNA was confirmed for the sapovirus Cowden strain during replication (25). The VP2 protein has not yet been identified in sapovirus virions; however, the expression of this protein was detected in the in vitro translation products of a porcine sapovirus full-length genomic cDNA construct and from porcine sapovirus-infected cells (28). VP2 is predicted to be a strong basic protein and is identified as an interior component of the norovirus particles (73).

The expression of VP1 in insect or mammalian cells resulted in spontaneously assembled virus-like particles (VLPs) (12, 71, 72, 74 – 81). The sapovirus VLPs are morphologically and antigenically indistinguishable from those of the native sapovirus virions found in clinical specimens (12, 74). Digitized electron cryomicrographs of the human sapovirus VLPs revealed that the icosahedral capsid is formed from 180 molecules of VP1, the same as in norovirus (76). Sapovirus VP1 could be separated into several domains: the N-terminal variable region (NVR), N-terminal region (N), central variable region (CVR), and C-terminal region (C) (Fig. 2) (47). The conserved amino acid motif “GWS” was found in the predicted N and CVR junction (Fig. 2). The “G” in this motif is strictly conserved among caliciviruses (76). Norovirus VP1 has also been separated into several domains, the N-terminal domain, shell domain, and protruding (P) domain, which is further divided into P1 and P2 subdomains (76, 82, 83). The sapovirus VP1 CVR region likely corresponds to the highly variable P2 domain of norovirus VP1 (47, 76).

GENOMIC SEQUENCE AND ANTIGENICITY

The first complete genome of a sapovirus was determined for the Manchester strain detected in the United Kingdom in 1993 (Hu/Manchester/93/UK; GenBank accession no. X86560) (41, 42), which is closely related genetically to the prototype Sapporo strain (14). Thus far, 26 (21 from humans and five from animals [porcine and bat]) complete sapovirus genomes are available in GenBank (as of 1 September 2013). The VP1-encoding region is the most diverse region in the genome (84 – 86), and sapoviruses are divided into multiple genogroups based on complete VP1 sequences. Five genogroups (GI to GV) are recognized (46, 87), and nine additional genogroups (GVI to GXIV) were recently proposed (88). To date, human sapoviruses have been classified into four genogroups (GI, GII, GIV, and GV).

Distinct antigenicity among sapovirus strains has been demonstrated by using clinical specimens (9, 43, 89 – 91), recombinant VP1 proteins (77, 92), or virus-like particles (VLPs) (74, 77, 80, 81, 93). Antigenicity differs among GI, GII, GIV, and GV strains (93, 94) and is also distinct among different genotypes within GI and GII (80, 81, 94). These experimental results also support that VP1 determines sapovirus antigenicity. The antigenic differences between human and animal sapoviruses have not yet been determined.

MOLECULAR CHARACTERIZATION

Genogroups and GenotypesThe partial RNA-dependent RNA polymerase (RdRp) or partial VP1 region (Fig. 2) or both of these regions can be used to partially characterize detected sapoviruses, as well as to investigate the similarity of the detected sapovirus for epidemiological surveys. In contrast, the RdRp-VP1 junction region (Fig. 2) is too short for such sequence analysis.

For genetic classification of sapoviruses, VP1 sequences are widely used, because this region is more diverse than the RdRp region (45, 46) and the VP1 sequence correlates with virus phenotype (i.e., antigenicity) (43, 74, 77, 80, 81, 92 – 95). The International Calicivirus Conference Committee proposed that at least the entire VP1 region sequence is necessary to designate new genogroups or genotypes. We recently established a human sapovirus classification scheme based on the complete VP1 nucleotide sequences (87). In this review, we include newly available sapovirus strains and updated sapovirus genotype numbering along with our previous analytical methods and criteria (87). The frequency histogram with pairwise distance values of 59 representative complete capsid nucleotide sequences of GI, GII, GIII, GIV, and GV sapoviruses resulted in three clearly distinct and nonoverlapping peaks (0 to 0.159, 0.198 to 0.471, and 0.522 to 0.807) (Fig. 3A). These three peaks can be considered to represent the strain, genotype, and genogroup, respectively, as previously described (87). The mean values ± 3 standard deviations (SD) for the pairwise distance peaks were 0 to 0.151, 0.170 to 0.416, and 0.489 to 0.801, respectively (Fig. 3A), and the cutoff values for the genotype and genogroup clusters were designated ≤0.169 and ≤0.488, respectively. Based on the criteria, human sapovirus GI and GII were each subdivided into seven genotypes (GI.1 to GI.7 and GII.1 to GII.7). GIV was placed into a single genotype (GIV.1), and GV was subdivided into two genotypes (GV.1 and GV.2) (Fig. 4). GV also includes sapoviruses detected from pigs (GV.3) and sea lions (GV.4). As summarized in Fig. 4, genotype numbering based on the entire VP1 sequences is inconsistent among research groups for GI.5, GI.6, and GII.2 to GII.5 (46, 47, 87, 96). The phylogenetic tree pattern based on the 59 complete VP1 amino acid sequences is similar to that based on the nucleotide sequences (data not shown); however, the pairwise distance histogram showed only two major peaks (0 to 0.480 and 0.652 to 1.115), and we cannot define the genotype range statistically (Fig. 3B). This differs from the case for noroviruses, because genotypes could be defined statistically by both VP1 nucleotide and amino acid sequences (97).

FIG 3
FIG 3

Pairwise distance distribution histograms of 59 representative sapovirus complete VP1 sequences. The vertical dashed lines indicate the cutoff limits for genogrouping and/or genotyping. (A) Limits based on nucleotide sequences, with three peaks (0 to 0.159, 0.198 to 0.471, and 0.522 to 0.807) corresponding to the strain, genotype, and genogroup range, respectively. The mean values ± 3 SD for the pairwise distance peaks were 0 to 0.151, 0.170 to 0.416, and 0.489 to 0.801, and the cutoff values for the genotype and genogroup clusters were designated ≤0.169 and ≤0.488, respectively. (B) Limits based on amino acid sequences, with two major peaks (0 to 0.480 and 0.652 to 1.115) corresponding to the strain and genogroup range, respectively.

FIG 4
FIG 4

Genogroup and genotypes of GI, GII, GIII, GIV, and GV sapovirus strains based on complete VP1 nucleotide sequences. The phylogenetic tree is based on the complete VP1 nucleotide sequences (approximately 1,690 nt) of a total of 59 sapovirus strains (representing 58 sapovirus strains corresponding to all genotypes within GI, GII, GIV, and GV and one porcine strain representing GIII). The phylogenetic tree was constructed by the neighbor-joining method with 1,000 bootstrap replications using NJPlot software (http://pbil.univ-lyon1.fr/software/njplot.html) (273). The numbers on each branch indicate the bootstrap values of ≥950. The scale represents the nucleotide substitutions per site. Each sapovirus strain is indicated as genogroup/genotype-GenBank accession number-strain name (i.e., GI.1-U65427-Sapporo). Genotyping numbers are updated based on a recent classification scheme (87). Genotyping numbers from three other reports (46, 47, 96) are summarized for comparison.

Evolution and Emergence of Predominant Sapovirus StrainsGenogroup and genotype analysis is important to characterize the currently circulating sapoviruses in the population. Emergence of genetically similar sapoviruses in multiple countries in Europe (98) and dynamic changes of genogroups and genotypes in different years among gastroenteritis patients in the same geographical area in Japan have been reported (99 – 101). Interestingly, GIV.1 strains were detected predominantly in Japan, Canada, the United States, and Europe around 2007 (98, 101 – 104). The dynamic change of the detected sapovirus genogroups in 2007 was also identified by national surveillance through regional diagnostic labs network in Japan (http://www.nih.go.jp/niid/en/iasr-table/2784-iasrtve.html; see “IASR Tables Virus” “By Season” “Gastrointestinal Pathogens” “PDF”). This is a distinct trend compared to noroviruses, in which a specific genogroup and genotype (i.e., genogroup II and genotype 4 [GII.4]) have been predominant in the past decade in Japan (http://www.nih.go.jp/niid/en/iasr-table/2784-iasrtve.html) and in multiple other countries (105 – 108). In the case of norovirus GII.4, time-ordered genetic and antigenic change of VP1 was identified (109, 110). Recent studies from Europe reported similar time-ordered genetic change in the VP1 region of the sapovirus GI.2 strains (98), as reported for norovirus GII.4 strains (111 – 115).

Due to the inconsistent genotype numbering systems used by different research groups for GI.5, GI.6, and GII.2 to GII.5 (46, 47, 87, 96) (Fig. 4), it is important to indicate which numbering system was used for genotyping, and a harmonized genotype numbering system will facilitate comparison and exchange of information from sapovirus surveillance at national and international levels.

Recombinant StrainsSapoviruses with inconsistent grouping between the nonstructural protein-encoding region (including the RdRp region) and the VP1 encoding region have been designated “recombinant” or “chimeric” strains. Both intra- and intergenogroup recombinant strains have been reported (Fig. 5). All reported intergenogroup recombinant strains were GIV (based on VP1 sequence), whereas they were clustered together with GII strains in the RdRp region (46, 85, 102, 116, 117). Intragenogroup recombinant strains within GI (118 – 120), GII (84, 121, 122), and GIII (123) have been identified.

FIG 5
FIG 5

Comparative phylogenetic analysis of sapoviruses based on complete RdRp and VP1 nucleotide sequences. Phylogenetic trees of 27 sapovirus strains (10 GI, 5 GII, 5 GIV, and 6 GV strains and 1 representative GIII strain) whose sequences covering the putative complete RdRp to the end of VP1 had been available at GenBank (www.ncbi.nlm.nih.gov/) by 1 September 2013 are shown. The trees on the left and right are based on the nucleotide sequences of the putative complete RdRp region (approximately 1,570 nt) and the entire VP1 region (approximately 1,690 nt), respectively. The phylogenetic trees were constructed by the neighbor-joining method with 1,000 bootstrap replications using NJPlot software. The numbers on each branch indicate the bootstrap values of ≥950. The scale represents the nucleotide substitutions per site. The sapovirus strains showing inconsistent clustering patterns on the two trees are indicated within dashed boxes.

Recently, a norovirus classification scheme has been reported (97). The authors used nucleotide sequences of nearly complete RdRp (1,300 nucleotides [nt]) and both amino acid and nucleotide sequences of VP1 for classification (97). Although sapovirus RdRp (NS7) is fused with protease (NS6) (Fig. 2), we defined the putative complete RdRp-encoding region (1,566 nt) for sapoviruses (Fig. 2) based on our previous in vitro studies (52, 58). Among GI, GII, GIV, and GV sapoviruses, the nucleotide sequences spanning the putative complete RdRp- and VP1-encoding regions (Fig. 2) of 26 strains (10 GI, 5 GII, 5 GIV, and 6 GV based on VP1) were available in GenBank as of 1 September 2013. All of these strains and a representative GIII Cowden strain of pig origin were used for phylogenetic analysis based on the RdRp and VP1 regions. We found conserved amino acid motif “WKGL” (Fig. 2) at amino acid positions 12 to 15 in the putative compete RdRp (NS7) region among these sapovirus strains. As shown in Fig. 5, several strains clustered differently on the phylogenetic trees based on RdRp- and VP1-encoding regions. For example, based on the RdRp region, GII and GIV strains are not well separated, as discussed previously (85). The GII.2 Mc10 and GII.3 C12 strains also cluster together in the RdRp region and were previously reported as intragenogroup recombinant strains (84). The GV.4 strain clustered together with other GV strains (GV.1, GV.2, and GV.3) in the VP1 region, but it is separated from other GV strains in the RdRp region. However, the RdRp sequence-based classification is less reliable due to the fewer available sequences compared to the complete VP1 sequences. Further accumulation of sufficient sequence data spanning the complete or sufficient length of the RdRp- to the VP1-encoding regions for all the genogroups and genotypes are critical to provide a better understanding of “recombinant” or “chimeric” strains and to establish a reliable classification scheme for the sapovirus RdRp region in the future, because the putative complete RdRp sequence data for GI.3, GI.4, GI.6, GI.7, GII.4, GII.5, and GII.7 sapoviruses are not yet available (Fig. 5). In addition, it is also critical to amplify a single PCR fragment covering the partial RdRp- and VP1-encoding region for recombination analysis to avoid the possibility of coinfection of different genogroups and/or genotypes of sapovirus strains, as discussed previously (124).

LABORATORY DIAGNOSIS

Virus Particle DetectionSapoviruses are morphologically distinguishable from other gastroenteritis pathogens (e.g., norovirus, rotavirus, astrovirus, or adenovirus) by their typical “Star of David” surface morphology under the electron microscope (1, 33, 90, 125) (Fig. 1). However, this has low sensitivity compared to nucleic acid detection methods (116, 126 – 128, 130, 131).

Antigen Detection MethodsEnzyme-linked immunosorbent assays (ELISAs) have been developed for the detection of human sapovirus antigens (91, 93, 132, 190) and have been used for the detection of sapoviruses from clinical samples (43, 91, 132 – 135, 190). However, these assays are not widely used for diagnosis due to the difficulty in detection of antigenically diverse sapovirus strains, low sensitivity compared to nucleic acid detection methods (43, 91, 93), and current lack of commercial availability. The development of a broadly reactive ELISA or immunochromatography system for the detection of sapovirus antigens depends on the combination of a panel of genogroup/genotype-specific antisera and/or using broadly reactive monoclonal antibodies. These approaches may be feasible, because a common epitope(s) likely exists among GI, GII, GIV, and GV sapovirus strains (94). Broadly reactive norovirus-specific monoclonal antibodies that recognize VP1s of different genogroups of noroviruses were also reported (136 – 140).

Nucleic Acid Detection MethodsReverse transcription-PCR (RT-PCR), especially real-time RT-PCR, has become a major and routine method for sapovirus detection from clinical specimens (i.e., feces), because of its specificity, sensitivity, and broad reactivity. Numerous primers have been designed for the detection of human sapoviruses (Tables 2 to 4). These primers are designed to amplify the partial RdRp (44, 46, 141 – 144, 146 – 153), RdRp-VP1 junction (86, 154 – 162), or partial VP1 (126, 152, 163 – 166) region (Fig. 2). Due to the high genetic diversity of sapoviruses, most of the assays include multiple or degenerate primers (Tables 2 to 4). The primers targeting the conserved motifs of the RdRp region (e.g., p290 and p289 [Table 2]) also amplify other human gastroenteritis viruses (norovirus, rotavirus, and astrovirus) (144, 167, 168). Numerous primers with distinct names are quite similar, especially for RdRp-VP1 junction-targeting primer sets (Table 3).

View this table:
TABLE 2

Primer combinations targeting the RdRp region for human sapovirus detection

View this table:
TABLE 3

Primer and probe combinations targeting the RdRp-VP1 junction region for human sapovirus detection

View this table:
TABLE 4

Primer and probe combinations targeting the VP1 region for human sapovirus detection

Multiplex RT-PCR or PCR assays, whose products were differentiated by agarose gel electrophoresis (101, 159, 163, 169), real-time RT-PCR or PCR (156, 158, 162, 170), and a microsphere-based fluorescent PCR product detection assay (e.g., Luminex technology) (160, 166), have been reported for the detection of human sapoviruses together with other gastroenteritis viruses. Although these assays aimed for simultaneous detection of multiple viruses, it is unclear whether these assays can detect all genogroups of human sapoviruses.

Sapoviruses were also detected by specific primer-independent techniques (i.e., the metagenomic sequence approach) from untreated sewage (16), sewage sludge (171), and feces from California sea lions (172), dogs (173), and humans. These approaches are not widely used for diagnosis but may be applicable for routine clinical diagnosis in the future, when the cost of such assays and data analysis is comparable to that of traditional assays.

Selection of Detection MethodsThe nucleic acid detection method is more sensitive than EM (116, 126 – 128, 130, 131) or ELISA (91). Different detection rates among different PCR assays using the same panel of specimens (clinical specimens, environmental water, and shellfish) were reported (99 – 101, 174 – 177). Assays targeting the RdRp-VP1 junction region have the highest detection rate and can be used as the first choice for sapovirus screening from clinical specimens (101, 174). The VP1-targeting RT-PCR is preferred because the products can be sequenced for reliable genotyping (99 – 101). Similar results were reported for environmental water samples (i.e., river water) (175). RdRp-VP1 junction-targeting real-time RT-PCR was also used for the detection of sapoviruses from shellfish (178, 179): however, the nested RT-PCR targeting the partial VP1 region is superior to the real-time RT-PCR and single-round RT-PCR because of the low level of viral RNA in shellfish compared to clinical specimens (177, 178). Currently, limited primer sets (47, 86, 100, 165, 175, 180) have demonstrated the ability to detect all genogroups of human sapoviruses.

Full-Genome Sequencing ApproachesFull genomic sequence analysis is still not practical for routine diagnosis. A long single-round or nested RT-PCR to amplify a 2- to 2.5-kb PCR fragment to determine the complete VP1 sequences of various sapovirus strains from clinical specimens is feasible by using forward primers targeting the RdRp and/or RdRp-VP1 junction region (Tables 2 to 4) and a reverse primer hybridized to the 3′-end poly(A) tail (Fig. 2) (46, 47, 87, 130, 174, 181, 182). In contrast, the amplification of the 5′-end 5- to 5.5-kb fragment corresponding to the beginning of the genome to the VP1 upstream region is variable because of the lack of universal primers. As a new technology, the specific primer-independent metagenomic sequencing approach (i.e., next-generation sequencing techniques) can be used to determine the nearly complete genome sequences (lacking the 5′ end or both the 5′ and 3′ ends) from fecal specimens (172, 173). 5′ rapid amplification of cDNA ends (RACE) techniques (14, 41, 42) are still necessary to determine 5′ ends to obtain the complete sapovirus genomic sequences.

CLINICAL AND EPIDEMIOLOGICAL OBSERVATIONS

Symptoms and Severity of DiseaseBased on the epidemiological data from patients with sapovirus gastroenteritis, the incubation period ranges from less than 1 day to 4 days (5, 8, 44, 130, 135, 178, 183, 184). Major clinical symptoms include diarrhea and vomiting; however, additional constitutional symptoms (i.e., nausea, stomach/abdominal cramps, chills, headache, myalgia, or malaise) are also frequently reported. Similar to the case for norovirus illness, fever is a rare clinical symptom. Diarrhea usually resolves within 1 week (4, 5, 7 – 9, 44, 104, 117, 127, 135, 183, 185 – 189); however, individuals showing symptoms for a longer time (i.e., from over a week to up to 20 days) were also reported (9, 21, 127, 186, 188, 267). In general, the severity of sapovirus gastroenteritis is milder than that for rotavirus and norovirus (Table 5) (185, 186, 191). Gastroenteritis symptoms are usually self-limiting, and patients usually recover within a couple of days; however, the symptoms, severity, and duration of disease are dependent on the individual, and sapovirus infection sometimes leads to hospitalization (22, 152, 167, 193 – 209). Mortality is rare, but it was reported from outbreaks that occurred in a long-term-care facility for the elderly (104). Human noroviruses are associated with more serious clinical complications in susceptible groups (i.e., premature neonates and immunocompromised patients) (210 – 212). No such information is available for human sapoviruses, and this requires investigation in the future.

View this table:
TABLE 5

Reported clinical severity scores for sapovirus-, norovirus-, and rotavirus-associated gastroenteritis

Subclinical (asymptomatic) sapovirus infection was also detected (4, 6, 21, 134, 135, 213 – 216). Quantitative PCR analysis revealed that asymptomatic individuals also shed sapovirus in the feces at levels comparable to those shed by individuals with gastroenteritis (182, 183).

Shedding Levels and Patterns in FecesSapovirus shedding in feces may continue after symptoms disappear (1 to 4 weeks after onset of illness) (6, 22, 174, 191). Sapovirus shedding levels in clinical stool specimens range from 1.32 × 105 to 1.05 × 1011 genomic copies/gram of stool (80, 99, 101, 116, 117, 127 – 130, 174, 178, 181 – 183). Sapovirus RNA shedding levels in feces gradually decreased after onset of illness (174). During the prolonged excretion period (i.e., 25 days and 28 days after onset of illness) in some individuals in an outbreak, both synonymous and nonsynonymous nucleotide substitutions in the VP1-encoding region have been identified (174), and this is a possible mechanism for the generation of new variants of sapovirus in vivo. Similar to the case for noroviruses, sapoviruses were also detected from an immunocompromised patient who showed prolonged diarrhea (147 days) (217), although further studies with quantitative analysis are necessary.

Sporadic CasesSapoviruses are detected worldwide (i.e., in more than 35 countries), and more than 100 papers have described sapovirus detection from clinical specimens. Among them, 13 studies detected more than 30 sapovirus strains from patients with sporadic gastroenteritis (Table 6) (89, 99, 101, 102, 126, 131, 132, 165, 185, 191, 215, 216, 218 – 226). Although different methods (electron microscopy, ELISA, and PCR assays with different primer sets) were used in these studies, the sapovirus positive rates ranged from 2.2% to 12.7%. Eight studies also detected other gastroenteritis pathogens, and sapoviruses ranked second to fourth as the major viral pathogens among patients with sporadic gastroenteritis (Table 6). Similar to the case for noroviruses (101, 131, 185, 198), sapoviruses were detected mainly in the cold season among patients with sporadic gastroenteritis (89, 99 – 101, 131, 198, 225 – 227), although different seasonal peaks among years have also been reported (132, 185). Sapovirus illnesses occur more frequently in younger children than in older children and adults (131, 191, 216).

View this table:
TABLE 6

Sapovirus positive rates in gastroenteritis patients from 13 studies that detected more than 30 strains during the study period

OutbreaksAlthough the reported outbreak numbers are less for sapoviruses than for noroviruses (145, 228 – 230), sapovirus gastroenteritis outbreaks occur throughout the year in all ages of people in various settings, such as child day care centers, kindergartens, schools, colleges, hospitals, nursing homes, restaurants, hotels, wedding halls, and ships (3 – 7, 9, 80, 98, 103, 104, 116, 117, 127, 129, 130, 145, 174, 181, 182, 186, 188, 189, 228, 231 – 237). Suspected foodborne sapovirus outbreaks have also been reported (44, 145, 178, 230, 232, 238). The largest foodborne sapovirus outbreak (n = 665) has been reported in Japan in 2010 (183). An epidemiological investigation pointed to contaminated box lunches which were prepared by food handlers who were shedding sapovirus.

Data from four studies suggest that sapovirus caused 1.3 to 8.0% of the gastroenteritis outbreaks (Table 7) (98, 145, 228, 230), and data from the other three studies reported that sapovirus was detected in 5.9 to 22.6% of outbreak samples that tested negative for norovirus or both norovirus and pathogenic bacteria (103, 104, 234) (Table 7).

View this table:
TABLE 7

Sapovirus positive rates in gastroenteritis outbreaks

Coinfections of sapoviruses and multiple enteric viruses (e.g., noroviruses, rotaviruses, astroviruses, adenoviruses, enteroviruses, kobuviruses, etc.) have also been reported among acute gastroenteritis outbreaks (10, 178, 230, 231, 235 – 237, 239). Coinfections with different sapovirus strains (i.e., different genogroups/genotypes) were also identified from oyster/clam-associated gastroenteritis outbreaks (178, 236).

Sapoviruses in Seafood, Environmental Water, and AnimalsSapoviruses genetically indistinguishable (i.e., similar or identical based on partial virus genome sequences) from those detected in human clinical specimens have also been detected from shellfish (oysters and clams) (177, 178, 240, 241) and environmental water samples (river water and wastewater) (16, 171, 175, 176, 180, 241 – 246). These sapoviruses were likely viruses of human fecal origin that were discharged into environmental waters and accumulated in shellfish (i.e., oysters or clams). As evidence, sapoviruses were detected more frequently with higher viral RNA levels from environmental water samples (i.e., sewage and river water) in the cold season (175, 176, 180, 243, 247, 248), when the number of patients with sapovirus-associated sporadic gastroenteritis increased (89, 99 – 101, 131, 198, 225 – 227). In addition, similar sapovirus strains were detected from gastroenteritis patients, wastewater, and oysters, which were collected from geographically related areas in the same season (241). In contrast, sapoviruses genetically indistinguishable from those detected in human clinical specimens have not been discovered in other animals (i.e., swine, mink, bats, dogs, and sea lions) (48, 88, 123, 172, 173, 249 – 253). Based on complete VP1 sequences, GV.3 porcine sapoviruses are closest to human strains; however, they can be clearly separated into a different genotype (Fig. 4). These results suggest the existence of interspecies barriers among human and animal sapoviruses, although further epidemiological studies for other animals and experimental infection studies using human sapoviruses in various animals are necessary. Sapovirus contamination levels were ∼1.6 × 104 copies/g of digestive tissue in various types of shellfish (oyster, cockle, and smooth clam) (179), up to 1.3 × 105 copies/liter in wastewater treatment plant influent (248), and ∼1.3 × 109 copies/liter in untreated wastewater (247).

Transmission Route and Host SusceptibilityTransmission of sapovirus is through the fecal-oral route. Sapoviruses can be transmitted from person to person via contact with sapovirus-positive feces, vomitus, or sapovirus-contaminated materials/surfaces or via contaminated food and drinking water (44, 104, 129, 130, 145, 178, 182, 183, 231, 232, 236 – 239). These transmission routes are similar to those for norovirus (254), and sapovirus may also have a low infectious dose similar to that of norovirus (i.e., 1,015 to 2,800 genomic copies) (255, 256); however, similar volunteer studies are necessary to confirm this speculation for sapoviruses. No host genetic factors for susceptibility or resistance to human sapovirus infection and disease have been identified. Susceptibility to human sapoviruses is not associated with histo-blood group antigen (HBGA) phenotypes (214). In vitro data also support no binding of sapovirus to HBGAs (257, 258). This differs from the case for the prototype norovirus (Norwalk virus): certain HBGA phenotypes (e.g., nonsecretor) of an individual are clearly related to resistance to virus infection (259, 260). Other different genogroups/genotypes of norovirus strains can also bind to HBGAs (113, 261 – 263) but lack a clear relatedness between the HBGA phenotypes and resistance to infection (264 – 266). Sialic acids have recently been reported as binding factors for porcine sapovirus (258).

ImmunityThe serological responses to sapovirus infection were demonstrated by immune electron microscopy, ELISA, or radioimmunoassay using paired sera (i.e., acute- and convalescent-phase sera) with purified virus from clinical specimens (3, 4, 7, 22, 90, 190, 267, 268). The seroprevalence studies of human sapoviruses using purified virus or recombinant capsid proteins demonstrated a gradually increasing seroprevalence rate with age, and it reached a high level (>90%) in school-age children, and remained high (80 to 100%) in sera or pooled immunoglobulin collected from adults (92, 132, 190, 269 – 271). These results suggest that sapovirus infection is common during early childhood.

Protective immunity/resistance mechanisms to sapovirus infection at the putative primary infection site (e.g., intestinal lumen) remain to be clarified, but the presence of preexisting serum antibodies to sapoviruses was associated with reduced frequencies of sapovirus infection and illness, at least for antibodies to antigenically homologous sapoviruses (267). A similar phenomenon was also observed in gastroenteritis outbreaks that occurred in mother and baby units (7). Adults who had serum antibodies to antigenically indistinguishable human sapoviruses did not show any clinical symptoms on reinfection (7). Symptomatic reinfections with a different genogroup/genotype of sapovirus were recently reported in a study from Japan (99).

CONCLUSIONS AND FUTURE DIRECTIONS

Recent epidemiological studies with improved diagnostic assays have highlighted the impact of sapovirus-associated gastroenteritis. Genetically highly diverse sapovirus strains were identified through epidemiological surveillance studies. Continuous surveillance with a broadly reactive detection system(s) and molecular characterization will permit the identification of changes in major strains as well as the emergence of new strains and an understanding of the evolution of sapoviruses among humans and animals. However, in contrast to the significant improvement in sapovirus detection methods, the basic understanding of infection/replication sites, pathological changes in infected persons, immunological responses and protective immunity to sapovirus infections in humans, infectious dose, and stability in the environment remain unknown. To date, no vaccines or antiviral drugs are available for the control and prevention of human sapovirus infections. The mechanisms of virus binding and entry into target cells and viral RNA replication and translation are undefined, partially due to the lack of a cell culture system. Extensive studies of human sapoviruses in clinical cases, the use of the cell culture-adapted porcine sapovirus strain as a model, and establishment of a human sapovirus cell culture system will improve our knowledge of sapoviruses and may lead to more targeted control measures for prevention of sapovirus gastroenteritis in the future.

ACKNOWLEDGMENTS

We thank Yasutaka Yamashita, who kindly provided transmission EM pictures for human sapovirus and norovirus, and Kelly A. Scheuer and Susan Sommer-Wagner for their editing of the manuscript.

REFERENCES

  1. 1.↵
    2. Madeley CR
    . 1979. Comparison of the features of astroviruses and caliciviruses seen in samples of feces by electron microscopy. J Infect Dis 139:519–523. doi:10.1093/infdis/139.5.519.
    OpenUrlCrossRefPubMed
  2. 2.↵
    2. Madeley CR ,
    3. Cosgrove BP
    . 1976. Caliciviruses in man. Lancet i:199–200. (Letter.) doi:10.1016/S0140-6736(76)91309-X.
    OpenUrlCrossRef
  3. 3.↵
    2. McSwiggan DA ,
    3. Cubitt D ,
    4. Moore W
    . 1978. Calicivirus associated with winter vomiting disease. Lancet i:1215. doi:10.1016/S0140-6736(78)91012-7.
    OpenUrlCrossRef
  4. 4.↵
    2. Chiba S ,
    3. Sakuma Y ,
    4. Kogasaka R ,
    5. Akihara M ,
    6. Horino K ,
    7. Nakao T ,
    8. Fukui S
    . 1979. An outbreak of gastroenteritis associated with calicivirus in an infant home. J Med Virol 4:249–254. doi:10.1002/jmv.1890040402.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    2. Cubitt WD ,
    3. McSwiggan DA ,
    4. Moore W
    . 1979. Winter vomiting disease caused by calicivirus. J Clin Pathol 32:786–793. doi:10.1136/jcp.32.8.786.
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    2. Chiba S ,
    3. Sakuma Y ,
    4. Kogasaka R ,
    5. Akihara M ,
    6. Terashima H ,
    7. Horino K ,
    8. Nakao T
    . 1980. Fecal shedding of virus in relation to the days of illness in infantile gastroenteritis due to calicivirus. J Infect Dis 142:247–249. doi:10.1093/infdis/142.2.247.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    2. Cubitt WD ,
    3. McSwiggan DA ,
    4. Arstall S
    . 1980. An outbreak of calicivirus infection in a mother and baby unit. J Clin Pathol 33:1095–1098. doi:10.1136/jcp.33.11.1095.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    2. Humphrey TJ ,
    3. Cruickshank JG ,
    4. Cubitt WD
    . 1984. An outbreak of calicivirus associated gastroenteritis in an elderly persons home. A possible zoonosis? J Hyg (Lond) 93:293–299. doi:10.1017/S0022172400064822.
    OpenUrlCrossRefPubMed
  9. 9.↵
    2. Cubitt WD ,
    3. Pead PJ ,
    4. Saeed AA
    . 1981. A new serotype of calicivirus associated with an outbreak of gastroenteritis in a residential home for the elderly. J Clin Pathol 34:924–926. doi:10.1136/jcp.34.8.924.
    OpenUrlAbstract/FREE Full Text
  10. 10.↵
    2. Nakata S ,
    3. Honma S ,
    4. Numata KK ,
    5. Kogawa K ,
    6. Ukae S ,
    7. Morita Y ,
    8. Adachi N ,
    9. Chiba S
    . 2000. Members of the family caliciviridae (Norwalk virus and Sapporo virus) are the most prevalent cause of gastroenteritis outbreaks among infants in Japan. J Infect Dis 181:2029–2032. doi:10.1086/315500.
    OpenUrlCrossRefPubMedWeb of Science
  11. 11.↵
    2. Chiba S ,
    3. Nakata S ,
    4. Numata-Kinoshita K ,
    5. Honma S
    . 2000. Sapporo virus: history and recent findings. J Infect Dis 181(Suppl 2):S303–S308. doi:10.1086/315574.
    OpenUrlCrossRefPubMed
  12. 12.↵
    2. Numata K ,
    3. Hardy ME ,
    4. Nakata S ,
    5. Chiba S ,
    6. Estes MK
    . 1997. Molecular characterization of morphologically typical human calicivirus Sapporo. Arch Virol 142:1537–1552. doi:10.1007/s007050050178.
    OpenUrlCrossRefPubMedWeb of Science
  13. 13.↵
    2. Matson DO ,
    3. Zhong WM ,
    4. Nakata S ,
    5. Numata K ,
    6. Jiang X ,
    7. Pickering LK ,
    8. Chiba S ,
    9. Estes MK
    . 1995. Molecular characterization of a human calicivirus with sequence relationships closer to animal caliciviruses than other known human caliciviruses. J Med Virol 45:215–222. doi:10.1002/jmv.1890450218.
    OpenUrlCrossRefPubMedWeb of Science
  14. 14.↵
    2. Nakanishi K ,
    3. Tatsumi M ,
    4. Kinoshita-Numata K ,
    5. Tsugawa T ,
    6. Nakata S ,
    7. Tsutsumi H
    . 2011. Full sequence analysis of the original Sapporo virus. Microbiol Immunol 55:657–660. doi:10.1111/j.1348-0421.2011.00358.x.
    OpenUrlCrossRefPubMed
  15. 15.↵
    2. Mayo MA
    . 2002. A summary of taxonomic changes recently approved by ICTV. Arch Virol 147:1655–1663. doi:10.1007/s007050200039.
    OpenUrlCrossRefPubMedWeb of Science
  16. 16.↵
    2. Ng TF ,
    3. Marine R ,
    4. Wang C ,
    5. Simmonds P ,
    6. Kapusinszky B ,
    7. Bodhidatta L ,
    8. Oderinde BS ,
    9. Wommack KE ,
    10. Delwart E
    . 2012. High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J Virol 86:12161–12175. doi:10.1128/JVI.00869-12.
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    2. Wolf S ,
    3. Reetz J ,
    4. Hoffmann K ,
    5. Grundel A ,
    6. Schwarz BA ,
    7. Hanel I ,
    8. Otto PH
    . 2012. Discovery and genetic characterization of novel caliciviruses in German and Dutch poultry. Arch Virol 157:1499–1507. doi:10.1007/s00705-012-1326-7.
    OpenUrlCrossRefPubMed
  18. 18.↵
    2. Farkas T ,
    3. Sestak K ,
    4. Wei C ,
    5. Jiang X
    . 2008. Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J Virol 82:5408–5416. doi:10.1128/JVI.00070-08.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    2. L'Homme Y ,
    3. Sansregret R ,
    4. Plante-Fortier E ,
    5. Lamontagne AM ,
    6. Ouardani M ,
    7. Lacroix G ,
    8. Simard C
    . 2009. Genomic characterization of swine caliciviruses representing a new genus of Caliciviridae. Virus Genes 39:66–75. doi:10.1007/s11262-009-0360-3.
    OpenUrlCrossRefPubMed
  20. 20.↵
    2. Wolf S ,
    3. Reetz J ,
    4. Otto P
    . 2011. Genetic characterization of a novel calicivirus from a chicken. Arch Virol 156:1143–1150. doi:10.1007/s00705-011-0964-5.
    OpenUrlCrossRefPubMed
  21. 21.↵
    2. Spratt HC ,
    3. Marks MI ,
    4. Gomersall M ,
    5. Gill P ,
    6. Pai CH
    . 1978. Nosocomial infantile gastroenteritis associated with minirotavirus and calicivirus. J Pediatr 93:922–926. doi:10.1016/S0022-3476(78)81212-8.
    OpenUrlCrossRefPubMedWeb of Science
  22. 22.↵
    2. Suzuki H ,
    3. Konno T ,
    4. Kutsuzawa T ,
    5. Imai A ,
    6. Tazawa F ,
    7. Ishida N ,
    8. Katsushima N ,
    9. Sakamoto M
    . 1979. The occurrence of calicivirus in infants with acute gastroenteritis. J Med Virol 4:321–326. doi:10.1002/jmv.1890040410.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    2. Kjeldsberg E
    . 1977. Small spherical viruses in faeces from gastroenteritis patients. Acta Pathol Microbiol Scand B 85B:351–354.
    OpenUrl
  24. 24.↵
    2. Cubitt WD ,
    3. Barrett AD
    . 1984. Propagation of human candidate calicivirus in cell culture. J Gen Virol 65:1123–1126. doi:10.1099/0022-1317-65-6-1123.
    OpenUrlCrossRefPubMed
  25. 25.↵
    2. Chang KO ,
    3. Sosnovtsev SV ,
    4. Belliot G ,
    5. Kim Y ,
    6. Saif LJ ,
    7. Green KY
    . 2004. Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc Natl Acad Sci U S A 101:8733–8738. doi:10.1073/pnas.0401126101.
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    2. Flynn WT ,
    3. Saif LJ
    . 1988. Serial propagation of porcine enteric calicivirus-like virus in primary porcine kidney cell cultures. J Clin Microbiol 26:206–212.
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    2. Parwani AV ,
    3. Flynn WT ,
    4. Gadfield KL ,
    5. Saif LJ
    . 1991. Serial propagation of porcine enteric calicivirus in a continuous cell line. Effect of medium supplementation with intestinal contents or enzymes. Arch Virol 120:115–122. doi:10.1007/BF01310954.
    OpenUrlCrossRefPubMedWeb of Science
  28. 28.↵
    2. Chang KO ,
    3. Sosnovtsev SS ,
    4. Belliot G ,
    5. Wang Q ,
    6. Saif LJ ,
    7. Green KY
    . 2005. Reverse genetics system for porcine enteric calicivirus, a prototype sapovirus in the Caliciviridae. J Virol 79:1409–1416. doi:10.1128/JVI.79.3.1409-1416.2005.
    OpenUrlAbstract/FREE Full Text
  29. 29.↵
    2. Shivanna V ,
    3. Kim Y ,
    4. Chang KO
    . 2014. The crucial role of bile acids in the entry of porcine enteric calicivirus. Virology 456:268–278. doi:10.1016/j.virol.2014.04.002.
    OpenUrlCrossRefPubMed
  30. 30.↵
    2. Chang KO ,
    3. Kim Y ,
    4. Green KY ,
    5. Saif LJ
    . 2002. Cell-culture propagation of porcine enteric calicivirus mediated by intestinal contents is dependent on the cyclic AMP signaling pathway. Virology 304:302–310. doi:10.1006/viro.2002.1665.
    OpenUrlCrossRefPubMedWeb of Science
  31. 31.↵
    2. Flynn WT ,
    3. Saif LJ ,
    4. Moorhead PD
    . 1988. Pathogenesis of porcine enteric calicivirus-like virus in four-day-old gnotobiotic pigs. Am J Vet Res 49:819–825.
    OpenUrlPubMedWeb of Science
  32. 32.↵
    2. Guo M ,
    3. Hayes J ,
    4. Cho KO ,
    5. Parwani AV ,
    6. Lucas LM ,
    7. Saif LJ
    . 2001. Comparative pathogenesis of tissue culture-adapted and wild-type Cowden porcine enteric calicivirus (PEC) in gnotobiotic pigs and induction of diarrhea by intravenous inoculation of wild-type PEC. J Virol 75:9239–9251. doi:10.1128/JVI.75.19.9239-9251.2001.
    OpenUrlAbstract/FREE Full Text
  33. 33.↵
    2. Saif LJ ,
    3. Bohl EH ,
    4. Theil KW ,
    5. Cross RF ,
    6. House JA
    . 1980. Rotavirus-like, calicivirus-like, and 23-nm virus-like particles associated with diarrhea in young pigs. J Clin Microbiol 12:105–111.
    OpenUrlAbstract/FREE Full Text
  34. 34.↵
    2. Terashima H ,
    3. Chiba S ,
    4. Sakuma Y ,
    5. Kogasaka R ,
    6. Nakata S ,
    7. Minami R ,
    8. Horino K ,
    9. Nakao T
    . 1983. The polypeptide of a human calicivirus. Arch Virol 78:1–7. doi:10.1007/BF01310853.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.↵
    2. Parwani AV ,
    3. Saif LJ ,
    4. Kang SY
    . 1990. Biochemical characterization of porcine enteric calicivirus: analysis of structural and nonstructural viral proteins. Arch Virol 112:41–53. doi:10.1007/BF01348984.
    OpenUrlCrossRefPubMedWeb of Science
  36. 36.↵
    2. Wang Q ,
    3. Zhang Z ,
    4. Saif LJ
    . 2012. Stability of and attachment to lettuce by a culturable porcine sapovirus surrogate for human caliciviruses. Appl Environ Microbiol 78:3932–3940. doi:10.1128/AEM.06600-11.
    OpenUrlAbstract/FREE Full Text
  37. 37.↵
    2. Green KY
    . 2007. Caliciviridae: the noroviruses: specific virus families, p 949–979. In Knipe DM , Howley PM , Griffin DE , Lamb RA , Martin MA , Roizman B , Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
  38. 38.↵
    2. Smiley JR ,
    3. Chang KO ,
    4. Hayes J ,
    5. Vinje J ,
    6. Saif LJ
    . 2002. Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. J Virol 76:10089–10098. doi:10.1128/JVI.76.20.10089-10098.2002.
    OpenUrlAbstract/FREE Full Text
  39. 39.↵
    2. Meyers G ,
    3. Wirblich C ,
    4. Thiel HJ
    . 1991. Rabbit hemorrhagic disease virus—molecular cloning and nucleotide sequencing of a calicivirus genome. Virology 184:664–676. doi:10.1016/0042-6822(91)90436-F.
    OpenUrlCrossRefPubMedWeb of Science
  40. 40.↵
    2. Clarke IN ,
    3. Lambden PR
    . 2000. Organization and expression of calicivirus genes. J Infect Dis 181(Suppl)2:S309–S316. doi:10.1086/315575.
    OpenUrlCrossRefPubMed
  41. 41.↵
    2. Liu BL ,
    3. Clarke IN ,
    4. Caul EO ,
    5. Lambden PR
    . 1995. Human enteric caliciviruses have a unique genome structure and are distinct from the Norwalk-like viruses. Arch Virol 140:1345–1356. doi:10.1007/BF01322662.
    OpenUrlCrossRefPubMedWeb of Science
  42. 42.↵
    2. Liu B ,
    3. Clarke IN ,
    4. Caul EO ,
    5. Lambden PR
    . 1997. The genomic 5′ terminus of Manchester calicivirus. Virus Genes 15:25–28. doi:10.1023/A:1007946628253.
    OpenUrlCrossRefPubMedWeb of Science
  43. 43.↵
    2. Jiang X ,
    3. Cubitt WD ,
    4. Berke T ,
    5. Zhong W ,
    6. Dai X ,
    7. Nakata S ,
    8. Pickering LK ,
    9. Matson DO
    . 1997. Sapporo-like human caliciviruses are genetically and antigenically diverse. Arch Virol 142:1813–1827. doi:10.1007/s007050050199.
    OpenUrlCrossRefPubMedWeb of Science
  44. 44.↵
    2. Noel JS ,
    3. Liu BL ,
    4. Humphrey CD ,
    5. Rodriguez EM ,
    6. Lambden PR ,
    7. Clarke IN ,
    8. Dwyer DM ,
    9. Ando T ,
    10. Glass RI ,
    11. Monroe SS
    . 1997. Parkville virus: a novel genetic variant of human calicivirus in the Sapporo virus clade, associated with an outbreak of gastroenteritis in adults. J Med Virol 52:173–178. doi:10.1002/(SICI)1096-9071(199706)52:2<173::AID-JMV10>3.0.CO;2-M.
    OpenUrlCrossRefPubMedWeb of Science
  45. 45.↵
    2. Schuffenecker I ,
    3. Ando T ,
    4. Thouvenot D ,
    5. Lina B ,
    6. Aymard M
    . 2001. Genetic classification of “Sapporo-like viruses.” Arch Virol 146:2115–2132. doi:10.1007/s007050170024.
    OpenUrlCrossRefPubMedWeb of Science
  46. 46.↵
    2. Farkas T ,
    3. Zhong WM ,
    4. Jing Y ,
    5. Huang PW ,
    6. Espinosa SM ,
    7. Martinez N ,
    8. Morrow AL ,
    9. Ruiz-Palacios GM ,
    10. Pickering LK ,
    11. Jiang X
    . 2004. Genetic diversity among sapoviruses. Arch Virol 149:1309–1323. doi:10.1007/s00705-004-0296-9.
    OpenUrlCrossRefPubMedWeb of Science
  47. 47.↵
    2. Okada M ,
    3. Yamashita Y ,
    4. Oseto M ,
    5. Ogawa T ,
    6. Kaiho I ,
    7. Shinozaki K
    . 2006. Genetic variability in the sapovirus capsid protein. Virus Genes 33:157–161. doi:10.1007/s11262-005-0051-7.
    OpenUrlCrossRefPubMed
  48. 48.↵
    2. Tse H ,
    3. Chan WM ,
    4. Li KS ,
    5. Lau SK ,
    6. Woo PC ,
    7. Yuen KY
    . 2012. Discovery and genomic characterization of a novel bat sapovirus with unusual genomic features and phylogenetic position. PLoS One 7:e34987. doi:10.1371/journal.pone.0034987.
    OpenUrlCrossRefPubMed
  49. 49.↵
    2. Oka T ,
    3. Katayama K ,
    4. Ogawa S ,
    5. Hansman GS ,
    6. Kageyama T ,
    7. Ushijima H ,
    8. Miyamura T ,
    9. Takeda N
    . 2005. Proteolytic processing of sapovirus ORF1 polyprotein. J Virol 79:7283–7290. doi:10.1128/JVI.79.12.7283-7290.2005.
    OpenUrlAbstract/FREE Full Text
  50. 50.↵
    2. Oka T ,
    3. Yamamoto M ,
    4. Katayama K ,
    5. Hansman GS ,
    6. Ogawa S ,
    7. Miyamura T ,
    8. Takeda N
    . 2006. Identification of the cleavage sites of sapovirus open reading frame 1 polyprotein. J Gen Virol 87:3329–3338. doi:10.1099/vir.0.81799-0.
    OpenUrlCrossRefPubMed
  51. 51.↵
    2. Oka T ,
    3. Yokoyama M ,
    4. Katayama K ,
    5. Tsunemitsu H ,
    6. Yamamoto M ,
    7. Miyashita K ,
    8. Ogawa S ,
    9. Motomura K ,
    10. Mori H ,
    11. Nakamura H ,
    12. Wakita T ,
    13. Takeda N ,
    14. Sato H
    . 2009. Structural and biological constraints on diversity of regions immediately upstream of cleavage sites in calicivirus precursor proteins. Virology 394:119–129. doi:10.1016/j.virol.2009.08.018.
    OpenUrlCrossRefPubMed
  52. 52.↵
    2. Oka T ,
    3. Yamamoto M ,
    4. Yokoyama M ,
    5. Ogawa S ,
    6. Hansman GS ,
    7. Katayama K ,
    8. Miyashita K ,
    9. Takagi H ,
    10. Tohya Y ,
    11. Sato H ,
    12. Takeda N
    . 2007. Highly conserved configuration of catalytic amino acid residues among calicivirus-encoded proteases. J Virol 81:6798–6806. doi:10.1128/JVI.02840-06.
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    2. Oka T ,
    3. Murakami K ,
    4. Wakita T ,
    5. Katayama K
    . 2011. Comparative site-directed mutagenesis in the catalytic amino acid triad in calicivirus proteases. Microbiol Immunol 55:108–114. doi:10.1111/j.1348-0421.2010.00295.x.
    OpenUrlCrossRefPubMed
  54. 54.↵
    2. Yokoyama M ,
    3. Oka T ,
    4. Kojima H ,
    5. Nagano T ,
    6. Okabe T ,
    7. Katayama K ,
    8. Wakita T ,
    9. Kanda T ,
    10. Sato H
    . 2012. Structural basis for specific recognition of substrates by sapovirus protease. Front Microbiol 3:312. doi:10.3389/fmicb.2012.00312.
    OpenUrlCrossRefPubMed
  55. 55.↵
    2. Oka T ,
    3. Katayama K ,
    4. Ogawa S ,
    5. Hansman GS ,
    6. Kageyama T ,
    7. Miyamura T ,
    8. Takeda N
    . 2005. Cleavage activity of the sapovirus 3C-like protease in Escherichia coli. Arch Virol 150:2539–2548. doi:10.1007/s00705-005-0591-0.
    OpenUrlCrossRefPubMed
  56. 56.↵
    2. Robel I ,
    3. Gebhardt J ,
    4. Mesters JR ,
    5. Gorbalenya A ,
    6. Coutard B ,
    7. Canard B ,
    8. Hilgenfeld R ,
    9. Rohayem J
    . 2008. Functional characterization of the cleavage specificity of the sapovirus chymotrypsin-like protease. J Virol 82:8085–8093. doi:10.1128/JVI.00693-08.
    OpenUrlAbstract/FREE Full Text
  57. 57.↵
    2. Fullerton SW ,
    3. Blaschke M ,
    4. Coutard B ,
    5. Gebhardt J ,
    6. Gorbalenya A ,
    7. Canard B ,
    8. Tucker PA ,
    9. Rohayem J
    . 2007. Structural and functional characterization of sapovirus RNA-dependent RNA polymerase. J Virol 81:1858–1871. doi:10.1128/JVI.01462-06.
    OpenUrlAbstract/FREE Full Text
  58. 58.↵
    2. Bull RA ,
    3. Hyde J ,
    4. Mackenzie JM ,
    5. Hansman GS ,
    6. Oka T ,
    7. Takeda N ,
    8. White PA
    . 2011. Comparison of the replication properties of murine and human calicivirus RNA-dependent RNA polymerases. Virus Genes 42:16–27. doi:10.1007/s11262-010-0535-y.
    OpenUrlCrossRefPubMed
  59. 59.↵
    2. Green KY ,
    3. Mory A ,
    4. Fogg MH ,
    5. Weisberg A ,
    6. Belliot G ,
    7. Wagner M ,
    8. Mitra T ,
    9. Ehrenfeld E ,
    10. Cameron CE ,
    11. Sosnovtsev SV
    . 2002. Isolation of enzymatically active replication complexes from feline calicivirus-infected cells. J Virol 76:8582–8595. doi:10.1128/JVI.76.17.8582-8595.2002.
    OpenUrlAbstract/FREE Full Text
  60. 60.↵
    2. Sosnovtsev SV ,
    3. Garfield M ,
    4. Green KY
    . 2002. Processing map and essential cleavage sites of the nonstructural polyprotein encoded by ORF1 of the feline calicivirus genome. J Virol 76:7060–7072. doi:10.1128/JVI.76.14.7060-7072.2002.
    OpenUrlAbstract/FREE Full Text
  61. 61.↵
    2. Oehmig A ,
    3. Buttner M ,
    4. Weiland F ,
    5. Werz W ,
    6. Bergemann K ,
    7. Pfaff E
    . 2003. Identification of a calicivirus isolate of unknown origin. J Gen Virol 84:2837–2845. doi:10.1099/vir.0.19042-0.
    OpenUrlCrossRefPubMed
  62. 62.↵
    2. Konig M ,
    3. Thiel HJ ,
    4. Meyers G
    . 1998. Detection of viral proteins after infection of cultured hepatocytes with rabbit hemorrhagic disease virus. J Virol 72:4492–4497.
    OpenUrlAbstract/FREE Full Text
  63. 63.↵
    2. Belliot G ,
    3. Sosnovtsev SV ,
    4. Mitra T ,
    5. Hammer C ,
    6. Garfield M ,
    7. Green KY
    . 2003. In vitro proteolytic processing of the MD145 norovirus ORF1 nonstructural polyprotein yields stable precursors and products similar to those detected in calicivirus-infected cells. J Virol 77:10957–10974. doi:10.1128/JVI.77.20.10957-10974.2003.
    OpenUrlAbstract/FREE Full Text
  64. 64.↵
    2. Chang KO ,
    3. Sosnovtsev SV ,
    4. Belliot G ,
    5. King AD ,
    6. Green KY
    . 2006. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 353:463–473. doi:10.1016/j.virol.2006.06.006.
    OpenUrlCrossRefPubMedWeb of Science
  65. 65.↵
    2. Sosnovtsev SV ,
    3. Belliot G ,
    4. Chang KO ,
    5. Prikhodko VG ,
    6. Thackray LB ,
    7. Wobus CE ,
    8. Karst SM ,
    9. Virgin HW ,
    10. Green KY
    . 2006. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells. J Virol 80:7816–7831. doi:10.1128/JVI.00532-06.
    OpenUrlAbstract/FREE Full Text
  66. 66.↵
    2. Katayama K ,
    3. Hansman GS ,
    4. Oka T ,
    5. Ogawa S ,
    6. Takeda N
    . 2006. Investigation of norovirus replication in a human cell line. Arch Virol 151:1291–1308. doi:10.1007/s00705-005-0720-9.
    OpenUrlCrossRefPubMedWeb of Science
  67. 67.↵
    2. Meyers G ,
    3. Wirblich C ,
    4. Thiel HJ ,
    5. Thumfart JO
    . 2000. Rabbit hemorrhagic disease virus: genome organization and polyprotein processing of a calicivirus studied after transient expression of cDNA constructs. Virology 276:349–363. doi:10.1006/viro.2000.0545.
    OpenUrlCrossRefPubMed
  68. 68.↵
    2. Pfister T ,
    3. Wimmer E
    . 2001. Polypeptide p41 of a Norwalk-like virus is a nucleic acid-independent nucleoside triphosphatase. J Virol 75:1611–1619. doi:10.1128/JVI.75.4.1611-1619.2001.
    OpenUrlAbstract/FREE Full Text
  69. 69.↵
    2. Marin MS ,
    3. Casais R ,
    4. Alonso JM ,
    5. Parra F
    . 2000. ATP binding and ATPase activities associated with recombinant rabbit hemorrhagic disease virus 2C-like polypeptide. J Virol 74:10846–10851. doi:10.1128/JVI.74.22.10846-10851.2000.
    OpenUrlAbstract/FREE Full Text
  70. 70.↵
    2. Leen EN ,
    3. Kwok KY ,
    4. Birtley JR ,
    5. Simpson PJ ,
    6. Subba-Reddy CV ,
    7. Chaudhry Y ,
    8. Sosnovtsev SV ,
    9. Green KY ,
    10. Prater SN ,
    11. Tong M ,
    12. Young JC ,
    13. Chung LM ,
    14. Marchant J ,
    15. Roberts LO ,
    16. Kao CC ,
    17. Matthews S ,
    18. Goodfellow IG ,
    19. Curry S
    . 2013. Structures of the compact helical core domains of feline calicivirus and murine norovirus VPg proteins. J Virol 87:5318–5330. doi:10.1128/JVI.03151-12.
    OpenUrlAbstract/FREE Full Text
  71. 71.↵
    2. Oka T ,
    3. Yamamoto M ,
    4. Miyashita K ,
    5. Ogawa S ,
    6. Katayama K ,
    7. Wakita T ,
    8. Takeda N
    . 2009. Self-assembly of sapovirus recombinant virus-like particles from polyprotein in mammalian cells. Microbiol Immunol 53:49–52. doi:10.1111/j.1348-0421.2008.00086.x.
    OpenUrlCrossRefPubMed
  72. 72.↵
    2. Hansman GS ,
    3. Oka T ,
    4. Takeda N
    . 2008. Sapovirus-like particles derived from polyprotein. Virus Res 137:261–265. doi:10.1016/j.virusres.2008.07.002.
    OpenUrlCrossRefPubMed
  73. 73.↵
    2. Vongpunsawad S ,
    3. Venkataram Prasad BV ,
    4. Estes MK
    . 2013. Norwalk virus minor capsid protein VP2 associates within the VP1 shell domain. J Virol 87:4818–4825. doi:10.1128/JVI.03508-12.
    OpenUrlAbstract/FREE Full Text
  74. 74.↵
    2. Jiang X ,
    3. Zhong W ,
    4. Kaplan M ,
    5. Pickering LK ,
    6. Matson DO
    . 1999. Expression and characterization of Sapporo-like human calicivirus capsid proteins in baculovirus. J Virol Methods 78:81–91. doi:10.1016/S0166-0934(98)00169-4.
    OpenUrlCrossRefPubMedWeb of Science
  75. 75.↵
    2. Guo M ,
    3. Qian Y ,
    4. Chang KO ,
    5. Saif LJ
    . 2001. Expression and self-assembly in baculovirus of porcine enteric calicivirus capsids into virus-like particles and their use in an enzyme-linked immunosorbent assay for antibody detection in swine. J Clin Microbiol 39:1487–1493. doi:10.1128/JCM.39.4.1487-1493.2001.
    OpenUrlAbstract/FREE Full Text
  76. 76.↵
    2. Chen R ,
    3. Neill JD ,
    4. Noel JS ,
    5. Hutson AM ,
    6. Glass RI ,
    7. Estes MK ,
    8. Prasad BV
    . 2004. Inter- and intragenus structural variations in caliciviruses and their functional implications. J Virol 78:6469–6479. doi:10.1128/JVI.78.12.6469-6479.2004.
    OpenUrlAbstract/FREE Full Text
  77. 77.↵
    2. Hansman GS ,
    3. Natori K ,
    4. Oka T ,
    5. Ogawa S ,
    6. Tanaka K ,
    7. Nagata N ,
    8. Ushijima H ,
    9. Takeda N ,
    10. Katayama K
    . 2005. Cross-reactivity among sapovirus recombinant capsid proteins. Arch Virol 150:21–36. doi:10.1007/s00705-004-0406-8.
    OpenUrlCrossRefPubMed
  78. 78.↵
    2. Hansman GS ,
    3. Oka T ,
    4. Katayama K ,
    5. Takeda N
    . 2006. Enhancement of sapovirus recombinant capsid protein expression in insect cells. FEBS Lett 580:4047–4050. doi:10.1016/j.febslet.2006.06.040.
    OpenUrlCrossRefPubMed
  79. 79.↵
    2. Oka T ,
    3. Hansman GS ,
    4. Katayama K ,
    5. Ogawa S ,
    6. Nagata N ,
    7. Miyamura T ,
    8. Takeda N
    . 2006. Expression of sapovirus virus-like particles in mammalian cells. Arch Virol 151:399–404. doi:10.1007/s00705-005-0613-y.
    OpenUrlCrossRefPubMed
  80. 80.↵
    2. Hansman GS ,
    3. Saito H ,
    4. Shibata C ,
    5. Ishizuka S ,
    6. Oseto M ,
    7. Oka T ,
    8. Takeda N
    . 2007. Outbreak of gastroenteritis due to sapovirus. J Clin Microbiol 45:1347–1349. doi:10.1128/JCM.01854-06.
    OpenUrlAbstract/FREE Full Text
  81. 81.↵
    2. Oka T ,
    3. Miyashita K ,
    4. Katayama K ,
    5. Wakita T ,
    6. Takeda N
    . 2009. Distinct genotype and antigenicity among genogroup II sapoviruses. Microbiol Immunol 53:417–420. doi:10.1111/j.1348-0421.2009.00133.x.
    OpenUrlCrossRefPubMed
  82. 82.↵
    2. Prasad BV ,
    3. Hardy ME ,
    4. Dokland T ,
    5. Bella J ,
    6. Rossmann MG ,
    7. Estes MK
    . 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286:287–290. doi:10.1126/science.286.5438.287.
    OpenUrlAbstract/FREE Full Text
  83. 83.↵
    2. Hardy ME
    . 2005. Norovirus protein structure and function. FEMS Microbiol Lett 253:1–8. doi:10.1016/j.femsle.2005.08.031.
    OpenUrlCrossRefPubMed
  84. 84.↵
    2. Katayama K ,
    3. Miyoshi T ,
    4. Uchino K ,
    5. Oka T ,
    6. Tanaka T ,
    7. Takeda N ,
    8. Hansman GS
    . 2004. Novel recombinant sapovirus. Emerg Infect Dis 10:1874–1876. doi:10.3201/eid1010.040395.
    OpenUrlCrossRefPubMedWeb of Science
  85. 85.↵
    2. Hansman GS ,
    3. Takeda N ,
    4. Oka T ,
    5. Oseto M ,
    6. Hedlund KO ,
    7. Katayama K
    . 2005. Intergenogroup recombination in sapoviruses. Emerg Infect Dis 11:1916–1920. doi:10.3201/eid1112.050722.
    OpenUrlCrossRefPubMedWeb of Science
  86. 86.↵
    2. Oka T ,
    3. Katayama K ,
    4. Hansman GS ,
    5. Kageyama T ,
    6. Ogawa S ,
    7. Wu FT ,
    8. White PA ,
    9. Takeda N
    . 2006. Detection of human sapovirus by real-time reverse transcription-polymerase chain reaction. J Med Virol 78:1347–1353. doi:10.1002/jmv.20699.
    OpenUrlCrossRefPubMedWeb of Science
  87. 87.↵
    2. Oka T ,
    3. Mori K ,
    4. Iritani N ,
    5. Harada S ,
    6. Ueki Y ,
    7. Iizuka S ,
    8. Mise K ,
    9. Murakami K ,
    10. Wakita T ,
    11. Katayama K
    . 2012. Human sapovirus classification based on complete capsid nucleotide sequences. Arch Virol 157:349–352. doi:10.1007/s00705-011-1161-2.
    OpenUrlCrossRefPubMed
  88. 88.↵
    2. Scheuer KA ,
    3. Oka T ,
    4. Hoet AE ,
    5. Gebreyes WA ,
    6. Molla BZ ,
    7. Saif LJ ,
    8. Wang Q
    . 2013. Prevalence of porcine noroviruses, molecular characterization of emerging porcine sapoviruses from finisher swine in the United States, and unified classification scheme for sapoviruses. J Clin Microbiol 51:2344–2353. doi:10.1128/JCM.00865-13.
    OpenUrlAbstract/FREE Full Text
  89. 89.↵
    2. Cubitt WD ,
    3. McSwiggan DA
    . 1981. Calicivirus gastroenteritis in North West London. Lancet ii:975–977. doi:10.1016/S0140-6736(81)91167-3.
    OpenUrlCrossRef
  90. 90.↵
    2. Cubitt WD ,
    3. Blacklow NR ,
    4. Herrmann JE ,
    5. Nowak NA ,
    6. Nakata S ,
    7. Chiba S
    . 1987. Antigenic relationships between human caliciviruses and Norwalk virus. J Infect Dis 156:806–814. doi:10.1093/infdis/156.5.806.
    OpenUrlCrossRefPubMedWeb of Science
  91. 91.↵
    2. Hansman GS ,
    3. Guntapong R ,
    4. Pongsuwanna Y ,
    5. Natori K ,
    6. Katayama K ,
    7. Takeda N
    . 2006. Development of an antigen ELISA to detect sapovirus in clinical stool specimens. Arch Virol 151:551–561. doi:10.1007/s00705-005-0630-x.
    OpenUrlCrossRefPubMed
  92. 92.↵
    2. Farkas T ,
    3. Deng X ,
    4. Ruiz-Palacios G ,
    5. Morrow A ,
    6. Jiang X
    . 2006. Development of an enzyme immunoassay for detection of sapovirus-specific antibodies and its application in a study of seroprevalence in children. J Clin Microbiol 44:3674–3679. doi:10.1128/JCM.01087-06.
    OpenUrlAbstract/FREE Full Text
  93. 93.↵
    2. Hansman GS ,
    3. Oka T ,
    4. Sakon N ,
    5. Takeda N
    . 2007. Antigenic diversity of human sapoviruses. Emerg Infect Dis 13:1519–1525. doi:10.3201/eid1310.070402.
    OpenUrlCrossRefPubMed
  94. 94.↵
    2. Kitamoto N ,
    3. Oka T ,
    4. Katayama K ,
    5. Li TC ,
    6. Takeda N ,
    7. Kato Y ,
    8. Miyoshi T ,
    9. Tanaka T
    . 2012. Novel monoclonal antibodies broadly reactive to human recombinant sapovirus-like particles. Microbiol Immunol 56:760–770. doi:10.1111/j.1348-0421.2012.00499.x.
    OpenUrlCrossRefPubMed
  95. 95.↵
    2. Hansman GS ,
    3. Natori K ,
    4. Ushijima H ,
    5. Katayama K ,
    6. Takeda N
    . 2005. Characterization of polyclonal antibodies raised against sapovirus genogroup five virus-like particles. Arch Virol 150:1433–1437. doi:10.1007/s00705-005-0506-0.
    OpenUrlCrossRefPubMed
  96. 96.↵
    2. Hansman GS ,
    3. Oka T ,
    4. Katayama K ,
    5. Takeda N
    . 2007. Human sapoviruses: genetic diversity, recombination, and classification. Rev Med Virol 17:133–141. doi:10.1002/rmv.533. (Erratum, 17:2364, doi:10.1002/rmv.552.)
    OpenUrlCrossRefPubMedWeb of Science
  97. 97.↵
    2. Kroneman A ,
    3. Vega E ,
    4. Vennema H ,
    5. Vinje J ,
    6. White PA ,
    7. Hansman G ,
    8. Green K ,
    9. Martella V ,
    10. Katayama K ,
    11. Koopmans M
    . 2013. Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 158:2059–2068. doi:10.1007/s00705-013-1708-5.
    OpenUrlCrossRefPubMed
  98. 98.↵
    2. Svraka S ,
    3. Vennema H ,
    4. van der Veer B ,
    5. Hedlund KO ,
    6. Thorhagen M ,
    7. Siebenga J ,
    8. Duizer E ,
    9. Koopmans M
    . 2010. Epidemiology and genotype analysis of emerging sapovirus-associated infections across Europe. J Clin Microbiol 48:2191–2198. doi:10.1128/JCM.02427-09.
    OpenUrlAbstract/FREE Full Text
  99. 99.↵
    2. Harada S ,
    3. Oka T ,
    4. Tokuoka E ,
    5. Kiyota N ,
    6. Nishimura K ,
    7. Shimada Y ,
    8. Ueno T ,
    9. Ikezawa S ,
    10. Wakita T ,
    11. Wang Q ,
    12. Saif LJ ,
    13. Katayama K
    . 2012. A confirmation of sapovirus re-infection gastroenteritis cases with different genogroups and genetic shifts in the evolving sapovirus genotypes, 2002-2011. Arch Virol 157:1999–2003. doi:10.1007/s00705-012-1387-7. (Erratum, 158:2641–2642, 2013, doi:10.1007/s00705-013-1757-9.)
    OpenUrlCrossRefPubMed
  100. 100.↵
    2. Harada S ,
    3. Tokuoka E ,
    4. Kiyota N ,
    5. Katayama K ,
    6. Oka T
    . 2013. Phylogenetic analysis of the nonstructural and structural protein encoding region sequences, indicating successive appearance of genomically diverse sapovirus strains from gastroenteritis patients. Jpn J Infect Dis 66:454–457.
    OpenUrlCrossRefPubMed
  101. 101.↵
    2. Harada S ,
    3. Okada M ,
    4. Yahiro S ,
    5. Nishimura K ,
    6. Matsuo S ,
    7. Miyasaka J ,
    8. Nakashima R ,
    9. Shimada Y ,
    10. Ueno T ,
    11. Ikezawa S ,
    12. Shinozaki K ,
    13. Katayama K ,
    14. Wakita T ,
    15. Takeda N ,
    16. 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. doi:10.1002/jmv.21454. (Erratum, 85:1685–1686, 2013, doi:10.1002/jmv.23677.)
    OpenUrlCrossRef
  102. 102.↵
    2. Chanit W ,
    3. Thongprachum A ,
    4. Khamrin P ,
    5. Okitsu S ,
    6. Mizuguchi M ,
    7. Ushijima H
    . 2009. Intergenogroup recombinant sapovirus in Japan, 2007–2008. Emerg Infect Dis 15:1084–1087. doi:10.3201/eid1507.090153.
    OpenUrlCrossRefPubMed
  103. 103.↵
    2. Pang XL ,
    3. Lee BE ,
    4. Tyrrell GJ ,
    5. Preiksaitis JK
    . 2009. Epidemiology and genotype analysis of sapovirus associated with gastroenteritis outbreaks in Alberta, Canada: 2004-2007. J Infect Dis 199:547–551. doi:10.1086/596210.
    OpenUrlCrossRefPubMed
  104. 104.↵
    2. Lee LE ,
    3. Cebelinski EA ,
    4. Fuller C ,
    5. Keene WE ,
    6. Smith K ,
    7. Vinje J ,
    8. Besser JM
    . 2012. Sapovirus outbreaks in long-term care facilities, Oregon and Minnesota, USA, 2002-2009. Emerg Infect Dis 18:873–876. doi:10.3201/eid1805.111843.
    OpenUrlCrossRefPubMed
  105. 105.↵
    2. Siebenga JJ ,
    3. Vennema H ,
    4. Duizer E ,
    5. Koopmans MP
    . 2007. Gastroenteritis caused by norovirus GGII.4, The Netherlands, 1994-2005. Emerg Infect Dis 13:144–146. doi:10.3201/eid1301.060800.
    OpenUrlCrossRefPubMedWeb of Science
  106. 106.↵
    2. Glass RI ,
    3. Parashar UD ,
    4. Estes MK
    . 2009. Norovirus gastroenteritis. N Engl J Med 361:1776–1785. doi:10.1056/NEJMra0804575.
    OpenUrlCrossRefPubMedWeb of Science
  107. 107.↵
    2. Siebenga JJ ,
    3. Vennema H ,
    4. Zheng DP ,
    5. Vinje J ,
    6. Lee BE ,
    7. Pang XL ,
    8. Ho EC ,
    9. Lim W ,
    10. Choudekar A ,
    11. Broor S ,
    12. Halperin T ,
    13. Rasool NB ,
    14. Hewitt J ,
    15. Greening GE ,
    16. Jin M ,
    17. Duan ZJ ,
    18. Lucero Y ,
    19. O'Ryan M ,
    20. Hoehne M ,
    21. Schreier E ,
    22. Ratcliff RM ,
    23. White PA ,
    24. Iritani N ,
    25. Reuter G ,
    26. Koopmans M
    . 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J Infect Dis 200:802–812. doi:10.1086/605127.
    OpenUrlCrossRefPubMedWeb of Science
  108. 108.↵
    2. Vega E ,
    3. Barclay L ,
    4. Gregoricus N ,
    5. Shirley SH ,
    6. Lee D ,
    7. Vinje J
    . 2014. Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J Clin Microbiol 52:147–155. doi:10.1128/JCM.02680-13.
    OpenUrlAbstract/FREE Full Text
  109. 109.↵
    2. Lindesmith LC ,
    3. Beltramello M ,
    4. Donaldson EF ,
    5. Corti D ,
    6. Swanstrom J ,
    7. Debbink K ,
    8. Lanzavecchia A ,
    9. Baric RS
    . 2012. Immunogenetic mechanisms driving norovirus GII. 4 antigenic variation. PLoS Pathog 8:e1002705. doi:10.1371/journal.ppat.1002705.
    OpenUrlCrossRefPubMed
  110. 110.↵
    2. Lindesmith LC ,
    3. Donaldson EF ,
    4. Baric RS
    . 2011. Norovirus GII.4 strain antigenic variation. J Virol 85:231–242. doi:10.1128/JVI.01364-10.
    OpenUrlAbstract/FREE Full Text
  111. 111.↵
    2. Siebenga JJ ,
    3. Vennema H ,
    4. Renckens B ,
    5. de Bruin E ,
    6. van der Veer B ,
    7. Siezen RJ ,
    8. Koopmans M
    . 2007. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol 81:9932–9941. doi:10.1128/JVI.00674-07.
    OpenUrlAbstract/FREE Full Text
  112. 112.↵
    2. Motomura K ,
    3. Oka T ,
    4. Yokoyama M ,
    5. Nakamura H ,
    6. Mori H ,
    7. Ode H ,
    8. Hansman GS ,
    9. Katayama K ,
    10. Kanda T ,
    11. Tanaka T ,
    12. Takeda N ,
    13. Sato H
    . 2008. Identification of monomorphic and divergent haplotypes in the 2006-2007 norovirus GII/4 epidemic population by genomewide tracing of evolutionary history. J Virol 82:11247–11262. doi:10.1128/JVI.00897-08.
    OpenUrlAbstract/FREE Full Text
  113. 113.↵
    2. Bok K ,
    3. Abente EJ ,
    4. Realpe-Quintero M ,
    5. Mitra T ,
    6. Sosnovtsev SV ,
    7. Kapikian AZ ,
    8. Green KY
    . 2009. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J Virol 83:11890–11901. doi:10.1128/JVI.00864-09.
    OpenUrlAbstract/FREE Full Text
  114. 114.↵
    2. Motomura K ,
    3. Yokoyama M ,
    4. Ode H ,
    5. Nakamura H ,
    6. Mori H ,
    7. Kanda T ,
    8. Oka T ,
    9. Katayama K ,
    10. Noda M ,
    11. Tanaka T ,
    12. Takeda N ,
    13. Sato H
    . 2010. Divergent evolution of norovirus GII/4 by genome recombination from May 2006 to February 2009 in Japan. J Virol 84:8085–8097. doi:10.1128/JVI.02125-09.
    OpenUrlAbstract/FREE Full Text
  115. 115.↵
    2. van Beek J ,
    3. Ambert-Balay K ,
    4. Botteldoorn N ,
    5. Eden JS ,
    6. Fonager J ,
    7. Hewitt J ,
    8. Iritani N ,
    9. Kroneman A ,
    10. Vennema H ,
    11. Vinje J ,
    12. White PA ,
    13. Koopmans M
    . 2013. Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Euro Surveill 18(1):pii=20345. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20345 .
  116. 116.↵
    2. Hansman GS ,
    3. Ishida S ,
    4. Yoshizumi S ,
    5. Miyoshi M ,
    6. Ikeda T ,
    7. Oka T ,
    8. Takeda N
    . 2007. Recombinant sapovirus gastroenteritis, Japan. Emerg Infect Dis 13:786–788. doi:10.3201/eid1305.070049.
    OpenUrlCrossRefPubMed
  117. 117.↵
    2. Mikula C ,
    3. Springer B ,
    4. Reichart S ,
    5. Bierbacher K ,
    6. Lichtenschopf A ,
    7. Hoehne M
    . 2010. Sapovirus in adults in rehabilitation center, upper Austria. Emerg Infect Dis 16:1186–1187. doi:10.3201/eid1607.091789.
    OpenUrlCrossRefPubMed
  118. 118.↵
    2. Phan TG ,
    3. Okitsu S ,
    4. Muller WE ,
    5. Kohno H ,
    6. Ushijima H
    . 2006. Novel recombinant sapovirus, Japan. Emerg Infect Dis 12:865–867. doi:10.3201/eid1205.051608.
    OpenUrlCrossRefPubMedWeb of Science
  119. 119.↵
    2. Phan TG ,
    3. Trinh QD ,
    4. Yagyu F ,
    5. Sugita K ,
    6. Okitsu S ,
    7. Muller WE ,
    8. Ushijima H
    . 2006. Outbreak of sapovirus infection among infants and children with acute gastroenteritis in Osaka City, Japan during 2004-2005. J Med Virol 78:839–846. doi:10.1002/jmv.20632.
    OpenUrlCrossRefPubMedWeb of Science
  120. 120.↵
    2. Dey SK ,
    3. Mizuguchi M ,
    4. Okitsu S ,
    5. Ushijima H
    . 2011. Novel recombinant sapovirus in Bangladesh. Clin Lab 57:91–94.
    OpenUrlPubMed
  121. 121.↵
    2. Hansman GS ,
    3. Takeda N ,
    4. Katayama K ,
    5. Tu ET ,
    6. McIver CJ ,
    7. Rawlinson WD ,
    8. White PA
    . 2006. Genetic diversity of sapovirus in children, Australia. Emerg Infect Dis 12:141–143. doi:10.3201/eid1201.050846.
    OpenUrlCrossRefPubMed
  122. 122.↵
    2. Nguyen TA ,
    3. Hoang L ,
    4. Pham le D ,
    5. Hoang KT ,
    6. Okitsu S ,
    7. Mizuguchi M ,
    8. Ushijima H
    . 2008. Norovirus and sapovirus infections among children with acute gastroenteritis in Ho Chi Minh City during 2005-2006. J Trop Pediatr 54:102–113. doi:10.1093/tropej/fmm096.
    OpenUrlCrossRefPubMed
  123. 123.↵
    2. Wang QH ,
    3. Han MG ,
    4. Funk JA ,
    5. Bowman G ,
    6. Janies DA ,
    7. Saif LJ
    . 2005. Genetic diversity and recombination of porcine sapoviruses. J Clin Microbiol 43:5963–5972. doi:10.1128/JCM.43.12.5963-5972.2005.
    OpenUrlAbstract/FREE Full Text
  124. 124.↵
    2. Gallimore CI ,
    3. Iturriza-Gomara M ,
    4. Lewis D ,
    5. Cubitt D ,
    6. Cotterill H ,
    7. Gray JJ
    . 2006. Characterization of sapoviruses collected in the United Kingdom from 1989 to 2004. J Med Virol 78:673–682. doi:10.1002/jmv.20592.
    OpenUrlCrossRefPubMedWeb of Science
  125. 125.↵
    2. Roingeard P
    . 2008. Viral detection by electron microscopy: past, present and future. Biol Cell 100:491–501. doi:10.1042/BC20070173.
    OpenUrlCrossRefPubMedWeb of Science
  126. 126.↵
    2. Okada M ,
    3. Shinozaki K ,
    4. Ogawa T ,
    5. Kaiho I
    . 2002. Molecular epidemiology and phylogenetic analysis of Sapporo-like viruses. Arch Virol 147:1445–1451. doi:10.1007/s00705-002-0821-7.
    OpenUrlCrossRefPubMed
  127. 127.↵
    2. Wu FT ,
    3. Oka T ,
    4. Takeda N ,
    5. Katayama K ,
    6. Hansman GS ,
    7. Muo CH ,
    8. Liang SY ,
    9. Hung CH ,
    10. Dah-Shyong Jiang D ,
    11. Hsin Chang J ,
    12. Yang JY ,
    13. Wu HS ,
    14. Yang CF
    . 2008. Acute gastroenteritis caused by GI/2 sapovirus, Taiwan, 2007. Emerg Infect Dis 14:1169–1171. doi:10.3201/eid1407.071531.
    OpenUrlCrossRefPubMed
  128. 128.↵
    2. Ootsuka Y ,
    3. Yamashita Y ,
    4. Ichikawa T ,
    5. Kondo R ,
    6. Oseto M ,
    7. Katayama K ,
    8. Takeda N ,
    9. Oka T
    . 2009. Molecular characterization of sapoviruses detected in sporadic gastroenteritis cases in 2007 in Ehime Prefecture, Japan. Jpn J Infect Dis 62:246–248.
    OpenUrlPubMed
  129. 129.↵
    2. Miyoshi M ,
    3. Yoshizumi S ,
    4. Kanda N ,
    5. Karino T ,
    6. Nagano H ,
    7. Kudo S ,
    8. Okano M ,
    9. Ishida S
    . 2010. Different genotypic sapoviruses detected in two simultaneous outbreaks of gastroenteritis among schoolchildren in the same school district in Hokkaido, Japan. Jpn J Infect Dis 63:75–78.
    OpenUrlPubMed
  130. 130.↵
    2. Yamashita Y ,
    3. Ootsuka Y ,
    4. Kondo R ,
    5. Oseto M ,
    6. Doi M ,
    7. Miyamoto T ,
    8. Ueda T ,
    9. Kondo H ,
    10. Tanaka T ,
    11. Wakita T ,
    12. Katayama K ,
    13. Takeda N ,
    14. Oka T
    . 2010. Molecular characterization of Sapovirus detected in a gastroenteritis outbreak at a wedding hall. J Med Virol 82:720–726. doi:10.1002/jmv.21646.
    OpenUrlCrossRefPubMed
  131. 131.↵
    2. Pang XL ,
    3. Preiksaitis JK ,
    4. Lee BE
    . 2014. Enhanced enteric virus detection in sporadic gastroenteritis using a multi-target real-time PCR panel: a one-year study. J Med Virol 86:1594–1601. doi:10.1002/jmv.23851.
    OpenUrlCrossRefPubMed
  132. 132.↵
    2. Nakata S ,
    3. Honma S ,
    4. Numata K ,
    5. Kogawa K ,
    6. Ukae S ,
    7. Adachi N ,
    8. Jiang X ,
    9. Estes MK ,
    10. Gatheru Z ,
    11. Tukei PM ,
    12. Chiba S
    . 1998. Prevalence of human calicivirus infections in Kenya as determined by enzyme immunoassays for three genogroups of the virus. J Clin Microbiol 36:3160–3163.
    OpenUrlAbstract/FREE Full Text
  133. 133.↵
    2. Matson DO ,
    3. Estes MK ,
    4. Glass RI ,
    5. Bartlett AV ,
    6. Penaranda M ,
    7. Calomeni E ,
    8. Tanaka T ,
    9. Nakata S ,
    10. Chiba S
    . 1989. Human calicivirus-associated diarrhea in children attending day care centers. J Infect Dis 159:71–78. doi:10.1093/infdis/159.1.71.
    OpenUrlCrossRefPubMedWeb of Science
  134. 134.↵
    2. Matson DO ,
    3. Estes MK ,
    4. Tanaka T ,
    5. Bartlett AV ,
    6. Pickering LK
    . 1990. Asymptomatic human calicivirus infection in a day care center. Pediatr Infect Dis J 9:190–196. doi:10.1097/00006454-199003000-00009.
    OpenUrlCrossRefPubMedWeb of Science
  135. 135.↵
    2. Grohmann G ,
    3. Glass RI ,
    4. Gold J ,
    5. James M ,
    6. Edwards P ,
    7. Borg T ,
    8. Stine SE ,
    9. Goldsmith C ,
    10. Monroe SS
    . 1991. Outbreak of human calicivirus gastroenteritis in a day-care center in Sydney, Australia. J Clin Microbiol 29:544–550.
    OpenUrlAbstract/FREE Full Text
  136. 136.↵
    2. Kitamoto N ,
    3. Tanaka T ,
    4. Natori K ,
    5. Takeda N ,
    6. Nakata S ,
    7. Jiang X ,
    8. Estes MK
    . 2002. Cross-reactivity among several recombinant calicivirus virus-like particles (VLPs) with monoclonal antibodies obtained from mice immunized orally with one type of VLP. J Clin Microbiol 40:2459–2465. doi:10.1128/JCM.40.7.2459-2465.2002.
    OpenUrlAbstract/FREE Full Text
  137. 137.↵
    2. Parker TD ,
    3. Kitamoto N ,
    4. Tanaka T ,
    5. Hutson AM ,
    6. Estes MK
    . 2005. Identification of genogroup I and genogroup II broadly reactive epitopes on the norovirus capsid. J Virol 79:7402–7409. doi:10.1128/JVI.79.12.7402-7409.2005.
    OpenUrlAbstract/FREE Full Text
  138. 138.↵
    2. Yoda T ,
    3. Suzuki Y ,
    4. Terano Y ,
    5. Yamazaki K ,
    6. Sakon N ,
    7. Kuzuguchi T ,
    8. Oda H ,
    9. Tsukamoto T
    . 2003. Precise characterization of norovirus (Norwalk-like virus)-specific monoclonal antibodies with broad reactivity. J Clin Microbiol 41:2367–2371. doi:10.1128/JCM.41.6.2367-2371.2003.
    OpenUrlAbstract/FREE Full Text
  139. 139.↵
    2. Shiota T ,
    3. Okame M ,
    4. Takanashi S ,
    5. Khamrin P ,
    6. Takagi M ,
    7. Satou K ,
    8. Masuoka Y ,
    9. Yagyu F ,
    10. Shimizu Y ,
    11. Kohno H ,
    12. Mizuguchi M ,
    13. Okitsu S ,
    14. Ushijima H
    . 2007. Characterization of a broadly reactive monoclonal antibody against norovirus genogroups I and II: recognition of a novel conformational epitope. J Virol 81:12298–12306. doi:10.1128/JVI.00891-07.
    OpenUrlAbstract/FREE Full Text
  140. 140.↵
    2. Parra GI ,
    3. Azure J ,
    4. Fischer R ,
    5. Bok K ,
    6. Sandoval-Jaime C ,
    7. Sosnovtsev SV ,
    8. Sander P ,
    9. Green KY
    . 2013. Identification of a broadly cross-reactive epitope in the inner shell of the norovirus capsid. PLoS One 8:e67592. doi:10.1371/journal.pone.0067592.
    OpenUrlCrossRefPubMed
  141. 141.↵
    2. Berke T ,
    3. Golding B ,
    4. Jiang X ,
    5. Cubitt DW ,
    6. Wolfaardt M ,
    7. Smith AW ,
    8. Matson DO
    . 1997. Phylogenetic analysis of the caliciviruses. J Med Virol 52:419–424. doi:10.1002/(SICI)1096-9071(199708)52:4<419::AID-JMV13>3.0.CO;2-B.
    OpenUrlCrossRefPubMedWeb of Science
  142. 142.↵
    2. Wolfaardt M ,
    3. Taylor MB ,
    4. Booysen HF ,
    5. Engelbrecht L ,
    6. Grabow WO ,
    7. Jiang X
    . 1997. Incidence of human calicivirus and rotavirus infection in patients with gastroenteritis in South Africa. J Med Virol 51:290–296. doi:10.1002/(SICI)1096-9071(199704)51:4<290::AID-JMV6>3.0.CO;2-0.
    OpenUrlCrossRefPubMedWeb of Science
  143. 143.↵
    2. Wright PJ ,
    3. Gunesekere IC ,
    4. Doultree JC ,
    5. Marshall JA
    . 1998. Small round-structured (Norwalk-like) viruses and classical human caliciviruses in southeastern Australia, 1980-1996. J Med Virol 55:312–320. doi:10.1002/(SICI)1096-9071(199808)55:4<312::AID-JMV10>3.0.CO;2-G.
    OpenUrlCrossRefPubMedWeb of Science
  144. 144.↵
    2. Jiang X ,
    3. Huang PW ,
    4. Zhong WM ,
    5. Farkas T ,
    6. Cubitt DW ,
    7. Matson DO
    . 1999. Design and evaluation of a primer pair that detects both Norwalk- and Sapporo-like caliciviruses by RT-PCR. J Virol Methods 83:145–154. doi:10.1016/S0166-0934(99)00114-7.
    OpenUrlCrossRefPubMedWeb of Science
  145. 145.↵
    2. Hedlund KO ,
    3. Rubilar-Abreu E ,
    4. Svensson L
    . 2000. Epidemiology of calicivirus infections in Sweden, 1994-1998. J Infect Dis 181(Suppl 2):S275–S280. doi:10.1086/315585.
    OpenUrlCrossRefPubMed
  146. 146.↵
    2. Honma S ,
    3. Nakata S ,
    4. Kinoshita-Numata K ,
    5. Kogawa K ,
    6. Chiba S
    . 2000. Evaluation of nine sets of PCR primers in the RNA dependent RNA polymerase region for detection and differentiation of members of the family Caliciviridae, Norwalk virus and Sapporo virus. Microbiol Immunol 44:411–419. doi:10.1111/j.1348-0421.2000.tb02515.x.
    OpenUrlCrossRefPubMedWeb of Science
  147. 147.↵
    2. Vinje J ,
    3. Deijl H ,
    4. van der Heide R ,
    5. Lewis D ,
    6. Hedlund KO ,
    7. Svensson L ,
    8. Koopmans MP
    . 2000. Molecular detection and epidemiology of Sapporo-like viruses. J Clin Microbiol 38:530–536.
    OpenUrlAbstract/FREE Full Text
  148. 148.↵
    2. Honma S ,
    3. Nakata S ,
    4. Sakai Y ,
    5. Tatsumi M ,
    6. Numata-Kinoshita K ,
    7. Chiba S
    . 2001. Sensitive detection and differentiation of Sapporo virus, a member of the family Caliciviridae, by standard and booster nested polymerase chain reaction. J Med Virol 65:413–417. doi:10.1002/jmv.2050.
    OpenUrlCrossRefPubMed
  149. 149.↵
    2. Martinez N ,
    3. Espul C ,
    4. Cuello H ,
    5. Zhong W ,
    6. Jiang X ,
    7. Matson DO ,
    8. Berke T
    . 2002. Sequence diversity of human caliciviruses recovered from children with diarrhea in Mendoza, Argentina, 1995-1998. J Med Virol 67:289–298. doi:10.1002/jmv.2220.
    OpenUrlCrossRefPubMedWeb of Science
  150. 150.↵
    2. Ratcliff RM ,
    3. Doherty JC ,
    4. Higgins GD
    . 2002. Sensitive detection of RNA viruses associated with gastroenteritis by a hanging-drop single-tube nested reverse transcription-PCR method. J Clin Microbiol 40:4091–4099. doi:10.1128/JCM.40.11.4091-4099.2002.
    OpenUrlAbstract/FREE Full Text
  151. 151.↵
    2. Bon F ,
    3. Giraudon H ,
    4. Sancey C ,
    5. Barranger C ,
    6. Joannes M ,
    7. Pothier P ,
    8. Kohli E
    . 2004. Development and evaluation of a new commercial test allowing the simultaneous detection of noroviruses and sapoviruses by reverse transcription-PCR and microplate hybridization. J Clin Microbiol 42:2218–2220. doi:10.1128/JCM.42.5.2218-2220.2004.
    OpenUrlAbstract/FREE Full Text
  152. 152.↵
    2. Monica B ,
    3. Ramani S ,
    4. Banerjee I ,
    5. Primrose B ,
    6. Iturriza-Gomara M ,
    7. Gallimore CI ,
    8. Brown DW ,
    9. Fathima M ,
    10. Moses PD ,
    11. Gray JJ ,
    12. Kang G
    . 2007. Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J Med Virol 79:544–551. doi:10.1002/jmv.20862.
    OpenUrlCrossRefPubMedWeb of Science
  153. 153.↵
    2. Rachakonda G ,
    3. Choudekar A ,
    4. Parveen S ,
    5. Bhatnagar S ,
    6. Patwari A ,
    7. Broor S
    . 2008. Genetic diversity of noroviruses and sapoviruses in children with acute sporadic gastroenteritis in New Delhi, India. J Clin Virol 43:42–48. doi:10.1016/j.jcv.2008.05.006.
    OpenUrlCrossRefPubMedWeb of Science
  154. 154.↵
    2. Chan MC ,
    3. Sung JJ ,
    4. Lam RK ,
    5. Chan PK ,
    6. Lai RW ,
    7. Leung WK
    . 2006. Sapovirus detection by quantitative real-time RT-PCR in clinical stool specimens. J Virol Methods 134:146–153. doi:10.1016/j.jviromet.2005.12.013.
    OpenUrlCrossRefPubMed
  155. 155.↵
    2. Logan C ,
    3. O'Leary JJ ,
    4. O'Sullivan N
    . 2007. Real-time reverse transcription PCR detection of norovirus, sapovirus and astrovirus as causative agents of acute viral gastroenteritis. J Virol Methods 146:36–44. doi:10.1016/j.jviromet.2007.05.031.
    OpenUrlCrossRefPubMed
  156. 156.↵
    2. Svraka S ,
    3. van der Veer B ,
    4. Duizer E ,
    5. Dekkers J ,
    6. Koopmans M ,
    7. Vennema H
    . 2009. Novel approach for detection of enteric viruses to enable syndrome surveillance of acute viral gastroenteritis. J Clin Microbiol 47:1674–1679. doi:10.1128/JCM.00307-09.
    OpenUrlAbstract/FREE Full Text
  157. 157.↵
    2. van Maarseveen NM ,
    3. Wessels E ,
    4. de Brouwer CS ,
    5. Vossen AC ,
    6. Claas EC
    . 2010. Diagnosis of viral gastroenteritis by simultaneous detection of adenovirus group F, astrovirus, rotavirus group A, norovirus genogroups I and II, and sapovirus in two internally controlled multiplex real-time PCR assays. J Clin Virol 49:205–210. doi:10.1016/j.jcv.2010.07.019.
    OpenUrlCrossRefPubMed
  158. 158.↵
    2. Gustavsson L ,
    3. Westin J ,
    4. Andersson LM ,
    5. Lindh M
    . 2011. Rectal swabs can be used for diagnosis of viral gastroenteritis with a multiple real-time PCR assay. J Clin Virol 51:279–282. doi:10.1016/j.jcv.2011.05.025.
    OpenUrlCrossRefPubMed
  159. 159.↵
    2. Khamrin P ,
    3. Okame M ,
    4. Thongprachum A ,
    5. Nantachit N ,
    6. Nishimura S ,
    7. Okitsu S ,
    8. Maneekarn N ,
    9. Ushijima H
    . 2011. A single-tube multiplex PCR for rapid detection in feces of 10 viruses causing diarrhea. J Virol Methods 173:390–393. doi:10.1016/j.jviromet.2011.02.012.
    OpenUrlCrossRefPubMed
  160. 160.↵
    2. Liu J ,
    3. Kibiki G ,
    4. Maro V ,
    5. Maro A ,
    6. Kumburu H ,
    7. Swai N ,
    8. Taniuchi M ,
    9. Gratz J ,
    10. Toney D ,
    11. Kang G ,
    12. Houpt E
    . 2011. Multiplex reverse transcription PCR Luminex assay for detection and quantitation of viral agents of gastroenteritis. J Clin Virol 50:308–313. doi:10.1016/j.jcv.2010.12.009.
    OpenUrlCrossRefPubMed
  161. 161.↵
    2. Liu J ,
    3. Gratz J ,
    4. Amour C ,
    5. Kibiki G ,
    6. Becker S ,
    7. Janaki L ,
    8. Verweij JJ ,
    9. Taniuchi M ,
    10. Sobuz SU ,
    11. Haque R ,
    12. Haverstick DM ,
    13. Houpt ER
    . 2013. A laboratory-developed TaqMan Array Card for simultaneous detection of 19 enteropathogens. J Clin Microbiol 51:472–480. doi:10.1128/JCM.02658-12.
    OpenUrlAbstract/FREE Full Text
  162. 162.↵
    2. Jiang Y ,
    3. Fang L ,
    4. Shi X ,
    5. Zhang H ,
    6. Li Y ,
    7. Lin Y ,
    8. Qiu Y ,
    9. Chen Q ,
    10. Li H ,
    11. Zhou L ,
    12. Hu Q
    . 2014. Simultaneous detection of five enteric viruses associated with gastroenteritis by use of a PCR assay: a single real-time multiplex reaction and its clinical application. J Clin Microbiol 52:1266–1268. doi:10.1128/JCM.00245-14.
    OpenUrlAbstract/FREE Full Text
  163. 163.↵
    2. Yan H ,
    3. Yagyu F ,
    4. Okitsu S ,
    5. Nishio O ,
    6. Ushijima H
    . 2003. Detection of norovirus (GI, GII), sapovirus and astrovirus in fecal samples using reverse transcription single-round multiplex PCR. J Virol Methods 114:37–44. doi:10.1016/j.jviromet.2003.08.009.
    OpenUrlCrossRefPubMedWeb of Science
  164. 164.↵
    2. Gunson RN ,
    3. Collins TC ,
    4. Carman WF
    . 2006. The real-time detection of sapovirus. J Clin Virol 35:321–322. doi:10.1016/j.jcv.2005.11.001.
    OpenUrlCrossRefPubMed
  165. 165.↵
    2. Okada M ,
    3. Yamashita Y ,
    4. Oseto M ,
    5. Shinozaki K
    . 2006. The detection of human sapoviruses with universal and genogroup-specific primers. Arch Virol 151:2503–2509. doi:10.1007/s00705-006-0820-1.
    OpenUrlCrossRefPubMedWeb of Science
  166. 166.↵
    2. Liu Y ,
    3. Xu ZQ ,
    4. Zhang Q ,
    5. Jin M ,
    6. Yu JM ,
    7. Li JS ,
    8. Liu N ,
    9. Cui SX ,
    10. Kong XY ,
    11. Wang H ,
    12. Li HY ,
    13. Cheng WX ,
    14. Duan ZJ
    . 2012. Simultaneous detection of seven enteric viruses associated with acute gastroenteritis by a multiplexed Luminex-based assay. J Clin Microbiol 50:2384–2389. doi:10.1128/JCM.06790-11.
    OpenUrlAbstract/FREE Full Text
  167. 167.↵
    2. Zintz C ,
    3. Bok K ,
    4. Parada E ,
    5. Barnes-Eley M ,
    6. Berke T ,
    7. Staat MA ,
    8. Azimi P ,
    9. Jiang X ,
    10. Matson DO
    . 2005. Prevalence and genetic characterization of caliciviruses among children hospitalized for acute gastroenteritis in the United States. Infect Genet Evol 5:281–290. doi:10.1016/j.meegid.2004.06.010.
    OpenUrlCrossRefPubMed
  168. 168.↵
    2. Ludert JE ,
    3. Alcala AC ,
    4. Liprandi F
    . 2004. Primer pair p289-p290, designed to detect both noroviruses and sapoviruses by reverse transcription-PCR, also detects rotaviruses by cross-reactivity. J Clin Microbiol 42:835–836. doi:10.1128/JCM.42.2.835-836.2004.
    OpenUrlAbstract/FREE Full Text
  169. 169.↵
    2. Shigemoto N ,
    3. Fukuda S ,
    4. Tanizawa Y ,
    5. Kuwayama M ,
    6. Ohara S ,
    7. Seno M
    . 2011. Detection of norovirus, sapovirus, and human astrovirus in fecal specimens using a multiplex reverse transcription-PCR with fluorescent dye-labeled primers. Microbiol Immunol 55:369–372. doi:10.1111/j.1348-0421.2011.00325.x.
    OpenUrlCrossRefPubMed
  170. 170.↵
    2. Niwa S ,
    3. Tsukagoshi H ,
    4. Ishioka T ,
    5. Sasaki Y ,
    6. Yoshizumi M ,
    7. Morita Y ,
    8. Kimura H ,
    9. Kozawa K
    . 2014. Triplex real-time PCR assay for detection and quantification of norovirus (GI and GII) and sapovirus. Microbiol Immunol 58:68–71. doi:10.1111/1348-0421.12107.
    OpenUrlCrossRefPubMed
  171. 171.↵
    2. Bibby K ,
    3. Peccia J
    . 2013. Identification of viral pathogen diversity in sewage sludge by metagenome analysis. Environ Sci Technol 47:1945–1951. doi:10.1021/es305181x.
    OpenUrlCrossRefPubMedWeb of Science
  172. 172.↵
    2. Li L ,
    3. Shan T ,
    4. Wang C ,
    5. Cote C ,
    6. Kolman J ,
    7. Onions D ,
    8. Gulland FM ,
    9. Delwart E
    . 2011. The fecal viral flora of California sea lions. J Virol 85:9909–9917. doi:10.1128/JVI.05026-11.
    OpenUrlAbstract/FREE Full Text
  173. 173.↵
    2. Li L ,
    3. Pesavento PA ,
    4. Shan T ,
    5. Leutenegger CM ,
    6. Wang C ,
    7. Delwart E
    . 2011. Viruses in diarrhoeic dogs include novel kobuviruses and sapoviruses. J Gen Virol 92:2534–2541. doi:10.1099/vir.0.034611-0.
    OpenUrlCrossRefPubMedWeb of Science
  174. 174.↵
    2. Iwakiri A ,
    3. Ganmyo H ,
    4. Yamamoto S ,
    5. Otao K ,
    6. Mikasa M ,
    7. Kizoe S ,
    8. Katayama K ,
    9. Wakita T ,
    10. Takeda N ,
    11. Oka T
    . 2009. Quantitative analysis of fecal sapovirus shedding: identification of nucleotide substitutions in the capsid protein during prolonged excretion. Arch Virol 154:689–693. doi:10.1007/s00705-009-0358-0.
    OpenUrlCrossRefPubMed
  175. 175.↵
    2. Kitajima M ,
    3. Oka T ,
    4. Haramoto E ,
    5. Katayama H ,
    6. Takeda N ,
    7. Katayama K ,
    8. Ohgaki S
    . 2010. Detection and genetic analysis of human sapoviruses in river water in Japan. Appl Environ Microbiol 76:2461–2467. doi:10.1128/AEM.02739-09.
    OpenUrlAbstract/FREE Full Text
  176. 176.↵
    2. Kitajima M ,
    3. Haramoto E ,
    4. Phanuwan C ,
    5. Katayama H
    . 2011. Genotype distribution of human sapoviruses in wastewater in Japan. Appl Environ Microbiol 77:4226–4229. doi:10.1128/AEM.00088-11.
    OpenUrlAbstract/FREE Full Text
  177. 177.↵
    2. Iizuka S ,
    3. Takai-Todaka R ,
    4. Ohshiro H ,
    5. Kitajima M ,
    6. Wang Q ,
    7. Saif LJ ,
    8. Wakita T ,
    9. Noda M ,
    10. Katayama K ,
    11. Oka T
    . 2013. Detection of multiple human sapoviruses from imported frozen individual clams. Food Environ Virol 5:119–125. doi:10.1007/s12560-013-9109-1.
    OpenUrlCrossRefPubMed
  178. 178.↵
    2. Iizuka S ,
    3. Oka T ,
    4. Tabara K ,
    5. Omura T ,
    6. Katayama K ,
    7. Takeda N ,
    8. Noda M
    . 2010. Detection of sapoviruses and noroviruses in an outbreak of gastroenteritis linked genetically to shellfish. J Med Virol 82:1247–1254. doi:10.1002/jmv.21791.
    OpenUrlCrossRefPubMed
  179. 179.↵
    2. Benabbes L ,
    3. Ollivier J ,
    4. Schaeffer J ,
    5. Parnaudeau S ,
    6. Rhaissi H ,
    7. Nourlil J ,
    8. Le Guyader FS
    . 2013. Norovirus and other human enteric viruses in moroccan shellfish. Food Environ Virol 5:35–40. doi:10.1007/s12560-012-9095-8.
    OpenUrlCrossRefPubMed
  180. 180.↵
    2. Sano D ,
    3. Perez-Sautu U ,
    4. Guix S ,
    5. Pinto RM ,
    6. Miura T ,
    7. Okabe S ,
    8. Bosch A
    . 2011. Quantification and genotyping of human sapoviruses in the Llobregat river catchment, Spain. Appl Environ Microbiol 77:1111–1114. doi:10.1128/AEM.01721-10.
    OpenUrlAbstract/FREE Full Text
  181. 181.↵
    2. Ishida S ,
    3. Yoshizumi S ,
    4. Miyoshi M ,
    5. Ikeda T ,
    6. Okui T ,
    7. Katayama K ,
    8. Takeda N ,
    9. Oka T
    . 2008. Characterization of sapoviruses detected in Hokkaido, Japan. Jpn J Infect Dis 61:504–506.
    OpenUrlPubMed
  182. 182.↵
    2. Yoshida T ,
    3. Kasuo S ,
    4. Azegami Y ,
    5. Uchiyama Y ,
    6. Satsumabayashi K ,
    7. Shiraishi T ,
    8. Katayama K ,
    9. Wakita T ,
    10. Takeda N ,
    11. Oka T
    . 2009. Characterization of sapoviruses detected in gastroenteritis outbreaks and identification of asymptomatic adults with high viral load. J Clin Virol 45:67–71. doi:10.1016/j.jcv.2009.03.003.
    OpenUrlCrossRefPubMed
  183. 183.↵
    2. Kobayashi S ,
    3. Fujiwara N ,
    4. Yasui Y ,
    5. Yamashita T ,
    6. Hiramatsu R ,
    7. Minagawa H
    . 2012. A foodborne outbreak of sapovirus linked to catered box lunches in Japan. Arch Virol 157:1995–1997. doi:10.1007/s00705-012-1394-8.
    OpenUrlCrossRefPubMed
  184. 184.↵
    2. Lee RM ,
    3. Lessler J ,
    4. Lee RA ,
    5. Rudolph KE ,
    6. Reich NG ,
    7. Perl TM ,
    8. Cummings DA
    . 2013. Incubation periods of viral gastroenteritis: a systematic review. BMC Infect Dis 13:446. doi:10.1186/1471-2334-13-446.
    OpenUrlCrossRefPubMed
  185. 185.↵
    2. Pang XL ,
    3. Honma S ,
    4. Nakata S ,
    5. Vesikari T
    . 2000. Human caliciviruses in acute gastroenteritis of young children in the community. J Infect Dis 181(Suppl 2):S288–S294. doi:10.1086/315590.
    OpenUrlCrossRefPubMedWeb of Science
  186. 186.↵
    2. Sakai Y ,
    3. Nakata S ,
    4. Honma S ,
    5. Tatsumi M ,
    6. Numata-Kinoshita K ,
    7. Chiba S
    . 2001. Clinical severity of Norwalk virus and Sapporo virus gastroenteritis in children in Hokkaido, Japan. Pediatr Infect Dis J 20:849–853. doi:10.1097/00006454-200109000-00005.
    OpenUrlCrossRefPubMedWeb of Science
  187. 187.↵
    2. Akihara S ,
    3. Phan TG ,
    4. Nguyen TA ,
    5. Hansman G ,
    6. Okitsu S ,
    7. Ushijima H
    . 2005. Existence of multiple outbreaks of viral gastroenteritis among infants in a day care center in Japan. Arch Virol 150:2061–2075. doi:10.1007/s00705-005-0540-y.
    OpenUrlCrossRefPubMedWeb of Science
  188. 188.↵
    2. Johansson PJ ,
    3. Bergentoft K ,
    4. Larsson PA ,
    5. Magnusson G ,
    6. Widell A ,
    7. Thorhagen M ,
    8. Hedlund KO
    . 2005. A nosocomial sapovirus-associated outbreak of gastroenteritis in adults. Scand J Infect Dis 37:200–204. doi:10.1080/00365540410020974.
    OpenUrlCrossRefPubMedWeb of Science
  189. 189.↵
    2. Yan H ,
    3. Abe T ,
    4. Phan TG ,
    5. Nguyen TA ,
    6. Iso T ,
    7. Ikezawa Y ,
    8. Ishii K ,
    9. Okitsu S ,
    10. Ushijima H
    . 2005. Outbreak of acute gastroenteritis associated with group A rotavirus and genogroup I sapovirus among adults in a mental health care facility in Japan. J Med Virol 75:475–481. doi:10.1002/jmv.20292.
    OpenUrlCrossRefPubMedWeb of Science
  190. 190.↵
    2. Nakata S ,
    3. Estes MK ,
    4. Chiba S
    . 1988. Detection of human calicivirus antigen and antibody by enzyme-linked immunosorbent assays. J Clin Microbiol 26:2001–2005.
    OpenUrlAbstract/FREE Full Text
  191. 191.↵
    2. Rockx B ,
    3. De Wit M ,
    4. Vennema H ,
    5. Vinje J ,
    6. De Bruin E ,
    7. Van Duynhoven Y ,
    8. Koopmans M
    . 2002. Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis 35:246–253. doi:10.1086/341408.
    OpenUrlCrossRefPubMedWeb of Science
  192. 192.
    2. Ruuska T ,
    3. Vesikari T
    . 1990. Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand J Infect Dis 22:259–267. doi:10.3109/00365549009027046.
    OpenUrlCrossRefPubMedWeb of Science
  193. 193.↵
    2. Kirkwood CD ,
    3. Bishop RF
    . 2001. Molecular detection of human calicivirus in young children hospitalized with acute gastroenteritis in Melbourne, Australia, during 1999. J Clin Microbiol 39:2722–2724. doi:10.1128/JCM.39.7.2722-2724.2001.
    OpenUrlAbstract/FREE Full Text
  194. 194.↵
    2. Dove W ,
    3. Cunliffe NA ,
    4. Gondwe JS ,
    5. Broadhead RL ,
    6. Molyneux ME ,
    7. Nakagomi O ,
    8. Hart CA
    . 2005. Detection and characterization of human caliciviruses in hospitalized children with acute gastroenteritis in Blantyre, Malawi. J Med Virol 77:522–527. doi:10.1002/jmv.20488.
    OpenUrlCrossRefPubMedWeb of Science
  195. 195.↵
    2. Guntapong R ,
    3. Hansman GS ,
    4. Oka T ,
    5. Ogawa S ,
    6. Kageyama T ,
    7. Pongsuwanna Y ,
    8. Katayama K
    . 2004. Norovirus and sapovirus infections in Thailand. Jpn J Infect Dis 57:276–278.
    OpenUrlPubMed
  196. 196.↵
    2. Hansman GS ,
    3. Katayama K ,
    4. Maneekarn N ,
    5. Peerakome S ,
    6. Khamrin P ,
    7. Tonusin S ,
    8. Okitsu S ,
    9. Nishio O ,
    10. Takeda N ,
    11. Ushijima H
    . 2004. Genetic diversity of norovirus and sapovirus in hospitalized infants with sporadic cases of acute gastroenteritis in Chiang Mai, Thailand. J Clin Microbiol 42:1305–1307. doi:10.1128/JCM.42.3.1305-1307.2004.
    OpenUrlAbstract/FREE Full Text
  197. 197.↵
    2. Kirkwood CD ,
    3. Clark R ,
    4. Bogdanovic-Sakran N ,
    5. Bishop RF
    . 2005. A 5-year study of the prevalence and genetic diversity of human caliciviruses associated with sporadic cases of acute gastroenteritis in young children admitted to hospital in Melbourne, Australia (1998-2002). J Med Virol 77:96–101. doi:10.1002/jmv.20419.
    OpenUrlCrossRefPubMed
  198. 198.↵
    2. Phan TG ,
    3. Okame M ,
    4. Nguyen TA ,
    5. Maneekarn N ,
    6. Nishio O ,
    7. Okitsu S ,
    8. Ushijima H
    . 2004. Human astrovirus, norovirus (GI, GII), and sapovirus infections in Pakistani children with diarrhea. J Med Virol 73:256–261. doi:10.1002/jmv.20084.
    OpenUrlCrossRefPubMedWeb of Science
  199. 199.↵
    2. Khamrin P ,
    3. Maneekarn N ,
    4. Peerakome S ,
    5. Tonusin S ,
    6. Malasao R ,
    7. Mizuguchi M ,
    8. Okitsu S ,
    9. Ushijima H
    . 2007. Genetic diversity of noroviruses and sapoviruses in children hospitalized with acute gastroenteritis in Chiang Mai, Thailand. J Med Virol 79:1921–1926. doi:10.1002/jmv.21004.
    OpenUrlCrossRefPubMed
  200. 200.↵
    2. Nguyen TA ,
    3. Yagyu F ,
    4. Okame M ,
    5. Phan TG ,
    6. Trinh QD ,
    7. Yan H ,
    8. Hoang KT ,
    9. Cao AT ,
    10. Le Hoang P ,
    11. Okitsu S ,
    12. 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. doi:10.1002/jmv.20857.
    OpenUrlCrossRefPubMedWeb of Science
  201. 201.↵
    2. Phan TG ,
    3. Okame M ,
    4. Nguyen TA ,
    5. Nishio O ,
    6. Okitsu S ,
    7. Ushijima H
    . 2005. Genetic diversity of sapovirus in fecal specimens from infants and children with acute gastroenteritis in Pakistan. Arch Virol 150:371–377. doi:10.1007/s00705-004-0401-0.
    OpenUrlCrossRefPubMedWeb of Science
  202. 202.↵
    2. Gutierrez-Escolano AL ,
    3. Velazquez FR ,
    4. Escobar-Herrera J ,
    5. Lopez Saucedo C ,
    6. Torres J ,
    7. Estrada-Garcia T
    . 2010. Human caliciviruses detected in Mexican children admitted to hospital during 1998-2000, with severe acute gastroenteritis not due to other enteropathogens. J Med Virol 82:632–637. doi:10.1002/jmv.21743.
    OpenUrlCrossRefPubMed
  203. 203.↵
    2. Jin Y ,
    3. Cheng WX ,
    4. Yang XM ,
    5. Jin M ,
    6. Zhang Q ,
    7. Xu ZQ ,
    8. Yu JM ,
    9. Zhu L ,
    10. Yang SH ,
    11. Liu N ,
    12. Cui SX ,
    13. Fang ZY ,
    14. Duan ZJ
    . 2009. Viral agents associated with acute gastroenteritis in children hospitalized with diarrhea in Lanzhou, China. J Clin Virol 44:238–241. doi:10.1016/j.jcv.2008.12.010.
    OpenUrlCrossRefPubMedWeb of Science
  204. 204.↵
    2. Li CS ,
    3. Chan PK ,
    4. Tang JW
    . 2009. Prevalence of diarrhea viruses in hospitalized children in Hong Kong in 2008. J Med Virol 81:1903–1911. doi:10.1002/jmv.21611.
    OpenUrlCrossRefPubMed
  205. 205.↵
    2. Lorrot M ,
    3. Bon F ,
    4. El Hajje MJ ,
    5. Aho S ,
    6. Wolfer M ,
    7. Giraudon H ,
    8. Kaplon J ,
    9. Marc E ,
    10. Raymond J ,
    11. Lebon P ,
    12. Pothier P ,
    13. Gendrel D
    . 2011. Epidemiology and clinical features of gastroenteritis in hospitalised children: prospective survey during a 2-year period in a Parisian hospital, France. Eur J Clin Microbiol Infect Dis 30:361–368. doi:10.1007/s10096-010-1094-9.
    OpenUrlCrossRefPubMed
  206. 206.↵
    2. Medici MC ,
    3. Tummolo F ,
    4. Albonetti V ,
    5. Abelli LA ,
    6. Chezzi C ,
    7. 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. doi:10.1002/jmv.23231.
    OpenUrlCrossRefPubMed
  207. 207.↵
    2. Rimoldi SG ,
    3. Stefani F ,
    4. Pagani C ,
    5. Chenal LL ,
    6. Zanchetta N ,
    7. Di Bartolo I ,
    8. Lombardi A ,
    9. Ruggeri FM ,
    10. Di Lillo D ,
    11. Zuccotti GV ,
    12. Gismondo MR
    . 2011. Epidemiological and clinical characteristics of pediatric gastroenteritis associated with new viral agents. Arch Virol 156:1583–1589. doi:10.1007/s00705-011-1037-5.
    OpenUrlCrossRefPubMed
  208. 208.↵
    2. Trang NV ,
    3. Luan le T ,
    4. Kim-Anh le T ,
    5. Hau VT ,
    6. Nhung le TH ,
    7. Phasuk P ,
    8. Setrabutr O ,
    9. Shirley H ,
    10. Vinje J ,
    11. Anh DD ,
    12. Mason CJ
    . 2012. Detection and molecular characterization of noroviruses and sapoviruses in children admitted to hospital with acute gastroenteritis in Vietnam. J Med Virol 84:290–297. doi:10.1002/jmv.23185.
    OpenUrlCrossRefPubMed
  209. 209.↵
    2. Park S ,
    3. Oh S ,
    4. Cho S ,
    5. Lee J ,
    6. Ryu S ,
    7. Song M ,
    8. Jung H ,
    9. Park G ,
    10. Choi S ,
    11. Chae Y ,
    12. Kim H
    . 2012. Genetic characterization of sapovirus detected in hospitalized children with acute gastroenteritis in Korea. Clin Lab 58:1219–1224. doi:10.7754/Clin.Lab.2012.120118.
    OpenUrlCrossRefPubMed
  210. 210.↵
    2. Bok K ,
    3. Green KY
    . 2012. Norovirus gastroenteritis in immunocompromised patients. N Engl J Med 367:2126–2132. doi:10.1056/NEJMra1207742.
    OpenUrlCrossRefPubMedWeb of Science
  211. 211.↵
    2. Frange P ,
    3. Touzot F ,
    4. Debre M ,
    5. Heritier S ,
    6. Leruez-Ville M ,
    7. Cros G ,
    8. Rouzioux C ,
    9. Blanche S ,
    10. Fischer A ,
    11. Avettand-Fenoel V
    . 2012. Prevalence and clinical impact of norovirus fecal shedding in children with inherited immune deficiencies. J Infect Dis 206:1269–1274. doi:10.1093/infdis/jis498.
    OpenUrlCrossRefPubMed
  212. 212.↵
    2. Naing Z ,
    3. Rayner B ,
    4. Killikulangara A ,
    5. Vunnam K ,
    6. Leach S ,
    7. McIver CJ ,
    8. Scott GM ,
    9. Craig ME ,
    10. Lui K ,
    11. Rawlinson WD
    . 2013. Prevalence of viruses in stool of premature neonates at a neonatal intensive care unit. J Paediatr Child Health 49:E221–E226. doi:10.1111/jpc.12113.
    OpenUrlCrossRefPubMed
  213. 213.↵
    2. Akihara S ,
    3. Phan TG ,
    4. Nguyen TA ,
    5. Yagyu F ,
    6. Okitsu S ,
    7. Muller WE ,
    8. Ushijima H
    . 2005. Identification of sapovirus infection among Japanese infants in a day care center. J Med Virol 77:595–601. doi:10.1002/jmv.20497.
    OpenUrlCrossRefPubMed
  214. 214.↵
    2. Bucardo F ,
    3. Carlsson B ,
    4. Nordgren J ,
    5. Larson G ,
    6. Blandon P ,
    7. Vilchez S ,
    8. Svensson L
    . 2012. Susceptibility of children to sapovirus infections, Nicaragua, 2005-2006. Emerg Infect Dis 18:1875–1878. doi:10.3201/eid1811.111581.
    OpenUrlCrossRefPubMed
  215. 215.↵
    2. Chhabra P ,
    3. Payne DC ,
    4. Szilagyi PG ,
    5. Edwards KM ,
    6. Staat MA ,
    7. Shirley SH ,
    8. Wikswo M ,
    9. Nix WA ,
    10. Lu X ,
    11. Parashar UD ,
    12. Vinje J
    . 2013. Etiology of viral gastroenteritis in children <5 years of age in the United States, 2008-2009. J Infect Dis 208:790–800. doi:10.1093/infdis/jit254.
    OpenUrlCrossRefPubMed
  216. 216.↵
    2. de Wit MA ,
    3. Koopmans MP ,
    4. Kortbeek LM ,
    5. Wannet WJ ,
    6. Vinje J ,
    7. van Leusden F ,
    8. Bartelds AI ,
    9. van Duynhoven YT
    . 2001. Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. Am J Epidemiol 154:666–674. doi:10.1093/aje/154.7.666.
    OpenUrlCrossRefPubMedWeb of Science
  217. 217.↵
    2. Roos-Weil D ,
    3. Ambert-Balay K ,
    4. Lanternier F ,
    5. Mamzer-Bruneel MF ,
    6. Nochy D ,
    7. Pothier P ,
    8. Avettand-Fenoel V ,
    9. Anglicheau D ,
    10. Snanoudj R ,
    11. Bererhi L ,
    12. Thervet E ,
    13. Lecuit M ,
    14. Legendre C ,
    15. Lortholary O ,
    16. Zuber J
    . 2011. Impact of norovirus/sapovirus-related diarrhea in renal transplant recipients hospitalized for diarrhea. Transplantation 92:61–69. doi:10.1097/TP.0b013e31821c9392.
    OpenUrlCrossRefPubMedWeb of Science
  218. 218.↵
    2. Amar CF ,
    3. East CL ,
    4. Gray J ,
    5. Iturriza-Gomara M ,
    6. Maclure EA ,
    7. McLauchlin J
    . 2007. Detection by PCR of eight groups of enteric pathogens in 4,627 faecal samples: re-examination of the English case-control Infectious Intestinal Disease Study (1993-1996). Eur J Clin Microbiol Infect Dis 26:311–323. doi:10.1007/s10096-007-0290-8.
    OpenUrlCrossRefPubMedWeb of Science
  219. 219.↵
    2. Iturriza-Gomara M ,
    3. Elliot AJ ,
    4. Dockery C ,
    5. Fleming DM ,
    6. Gray JJ
    . 2009. Structured surveillance of infectious intestinal disease in pre-school children in the community: ‘The Nappy Study.’ Epidemiol Infect 137:922–931. doi:10.1017/S0950268808001556.
    OpenUrlCrossRefPubMed
  220. 220.↵
    2. Phan TG ,
    3. Nguyen TA ,
    4. Nishimura S ,
    5. Nishimura T ,
    6. Yamamoto A ,
    7. Okitsu S ,
    8. Ushijima H
    . 2005. Etiologic agents of acute gastroenteritis among Japanese infants and children: virus diversity and genetic analysis of sapovirus. Arch Virol 150:1415–1424. doi:10.1007/s00705-005-0514-0.
    OpenUrlCrossRefPubMed
  221. 221.↵
    2. Phan TG ,
    3. Khamrin P ,
    4. Quang TD ,
    5. Dey SK ,
    6. Takanashi S ,
    7. Okitsu S ,
    8. Maneekarn N ,
    9. Ushijima H
    . 2007. Emergence of intragenotype recombinant sapovirus in Japan. Infect Genet Evol 7:542–546. doi:10.1016/j.meegid.2007.02.004.
    OpenUrlCrossRefPubMedWeb of Science
  222. 222.↵
    2. Phan TG ,
    3. Trinh QD ,
    4. Yagyu F ,
    5. Okitsu S ,
    6. Ushijima H
    . 2007. Emergence of rare sapovirus genotype among infants and children with acute gastroenteritis in Japan. Eur J Clin Microbiol Infect Dis 26:21–27. doi:10.1007/s10096-006-0235-7.
    OpenUrlCrossRefPubMedWeb of Science
  223. 223.↵
    2. Chan-it W ,
    3. Thongprachum A ,
    4. Okitsu S ,
    5. Mizuguchi M ,
    6. Ushijima H
    . 2010. Epidemiology and molecular characterization of sapovirus and astrovirus in Japan, 2008-2009. Jpn J Infect Dis 63:302–303.
    OpenUrlPubMed
  224. 224.↵
    2. Dey SK ,
    3. Phan GT ,
    4. Nishimura S ,
    5. Mizuguchi M ,
    6. Okitsu S ,
    7. Ushijima H
    . 2010. Molecular and epidemiological trend of sapovirus, and astrovirus infection in Japan. J Trop Pediatr 56:205–207. doi:10.1093/tropej/fmp082.
    OpenUrlCrossRefPubMed
  225. 225.↵
    2. Johnsen CK ,
    3. Midgley S ,
    4. Bottiger B
    . 2009. Genetic diversity of sapovirus infections in Danish children 2005-2007. J Clin Virol 46:265–269. doi:10.1016/j.jcv.2009.07.008.
    OpenUrlCrossRefPubMed
  226. 226.↵
    2. Tam CC ,
    3. O'Brien SJ ,
    4. Tompkins DS ,
    5. Bolton FJ ,
    6. Berry L ,
    7. Dodds J ,
    8. Choudhury D ,
    9. Halstead F ,
    10. Iturriza-Gomara M ,
    11. Mather K ,
    12. Rait G ,
    13. Ridge A ,
    14. Rodrigues LC ,
    15. Wain J ,
    16. Wood B ,
    17. Gray JJ
    . 2012. Changes in causes of acute gastroenteritis in the United Kingdom over 15 years: microbiologic findings from 2 prospective, population-based studies of infectious intestinal disease. Clin Infect Dis 54:1275–1286. doi:10.1093/cid/cis028.
    OpenUrlCrossRefPubMed
  227. 227.↵
    2. Dey SK ,
    3. Phathammavong O ,
    4. Nguyen TD ,
    5. Thongprachum A ,
    6. Chan-It W ,
    7. Okitsu S ,
    8. Mizuguchi M ,
    9. Ushijima H
    . 2012. Seasonal pattern and genotype distribution of sapovirus infection in Japan, 2003-2009. Epidemiol Infect 140:74–77. doi:10.1017/S0950268811000240.
    OpenUrlCrossRefPubMed
  228. 228.↵
    2. Blanton LH ,
    3. Adams SM ,
    4. Beard RS ,
    5. Wei G ,
    6. Bulens SN ,
    7. Widdowson MA ,
    8. Glass RI ,
    9. Monroe SS
    . 2006. Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004. J Infect Dis 193:413–421. doi:10.1086/499315.
    OpenUrlCrossRefPubMedWeb of Science
  229. 229.↵
    2. Hall AJ ,
    3. Wikswo ME ,
    4. Manikonda K ,
    5. Roberts VA ,
    6. Yoder JS ,
    7. Gould LH
    . 2013. Acute gastroenteritis surveillance through the National Outbreak Reporting System, United States. Emerg Infect Dis 19:1305–1309. doi:10.3201/eid1908.130482.
    OpenUrlCrossRefPubMed
  230. 230.↵
    2. Iritani N ,
    3. Kaida A ,
    4. Abe N ,
    5. Kubo H ,
    6. Sekiguchi JI ,
    7. Yamamoto SP ,
    8. Goto K ,
    9. Tanaka T ,
    10. Noda M
    . 2014. Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka City, Japan. J Med Virol 86:2019–2025. doi:10.1002/jmv.23883.
    OpenUrlCrossRefPubMed
  231. 231.↵
    2. Bon F ,
    3. Ambert-Balay K ,
    4. Giraudon H ,
    5. Kaplon J ,
    6. Le Guyader S ,
    7. Pommepuy M ,
    8. Gallay A ,
    9. Vaillant V ,
    10. de Valk H ,
    11. Chikhi-Brachet R ,
    12. Flahaut A ,