Systematic review and meta-analysis of enteric virus shedding in human excretions

Gang Zheng; Elana MG Chan; Alexandria B Boehm

doi:10.1016/j.ebiom.2025.105878

. 2025 Aug 5;119:105878. doi: 10.1016/j.ebiom.2025.105878

Systematic review and meta-analysis of enteric virus shedding in human excretions

Gang Zheng ¹, Elana MG Chan ¹, Alexandria B Boehm ^1,^∗

PMCID: PMC12789771 PMID: 40768836

Summary

Background

Wastewater-based epidemiology can inform the understanding of infectious disease occurrence in communities. Quantitative information on shedding of pathogen biomarkers in excretions that enter wastewater is needed to link measurements of pathogen biomarkers to rates of disease occurrence.

Methods

We compile, summarise, and compare data on shedding of human norovirus, rotavirus, hepatitis A virus, and adenovirus group F in stool, vomit, urine, saliva, mucus, and sputum using a systematic review and meta-analysis approach.

Findings

We provide summaries of measured concentrations of the viruses across excretions where data exist. We provide longitudinal shedding profiles in terms of concentrations and positivity rates. Duration of shedding and day of peak shedding are also provided.

Interpretation

There are limited data available for excretions other than stool, and limited data available for adenovirus group F. The aggregated data provided herein can serve as model inputs to translate wastewater enteric virus biomarker concentrations to disease occurrence rates. The study highlights data gaps and research needs.

Funding

This study was funded by a gift from the Sergey Brin Family Foundation to ABB.

Keywords: Norovirus, Adenovirus, Rotavirus, Hepatitis A virus, Stool, Saliva, Vomitus, Human excretions, Shedding

Research in context.

Evidence before this study

Wastewater-based epidemiology is a valuable tool for monitoring infectious diseases at the community level. Previous research has demonstrated the presence of enteric viruses in wastewater and shown a link between measurements of pathogen biomarkers to rates of disease occurrence. However, the interpretation of wastewater viral concentrations for public health applications remains challenging due to the lack of well-characterised viral shedding profiles. To address this gap, we conducted a comprehensive literature review research in late 2023 using Web of Science, PubMed, and Scopus using keywords: stool, vomit, saliva, urine, mucus, and sputum, and norovirus, rotavirus, hepatitis A virus, and adenovirus group F. Studies meeting inclusion criteria were evaluated for methodological data quality and risk of selective reporting bias, and subsequently, data were extracted. Our search identified over 100 studies reporting viral concentrations, and longitudinal concentration and presence/absence data across different viruses and excretions. Existing literature lacks a comprehensive compilation and quantitative modelling of enteric virus shedding data for these viruses and excretions.

Added value of this study

This study systematically characterises enteric virus shedding in infected patients using a systematic review and meta-analysis approach. We identified variations in the shedding concentrations, day of peak shedding, and shedding duration between different excretions and viruses. This study provides statistical models of shedding profiles to describe the temporal variation in enteric viruses positivity/concentration in excretions. The summarised shedding profiles and parameters provided in this study can inform and improve mass-balance and physical models aimed at estimating disease incidence from wastewater virus biomarker concentrations, although further validation is necessary.

Implications of all the available evidence

This review and meta-analysis provides quantitative shedding profiles and key parameters for modelling infection occurrence from wastewater measurements. Our findings highlight substantial gaps in the literature, particularly the limited data on enteric virus shedding in excretions other than stool. Addressing these gaps will require expanded shedding studies across underrepresented excretions and adherence to standardised reporting framework.

Introduction

Globally, diarrhoeal disease is a leading cause of child mortality and morbidity, causing approximately 1.7 billion cases of child diarrhoea with over 400,000 deaths for children under 5 years old every year.¹ Among the most common causes of diarrhoeal diseases are infections caused by enteric viruses, including norovirus, rotavirus, and adenovirus group F.² While hepatitis A virus infections cause acute hepatitis, it can also present with gastrointestinal symptoms and transmitted via the fecal-oral route.³ Despite their importance, there are limited data on the prevalence and incidence of enteric viral infections, limiting prevention efforts and response activities, and a thorough understanding of disease epidemiology.⁴

Wastewater-based epidemiology (WBE) has emerged as a tool to help better understand community health. WBE monitors pathogen biomarkers in wastewater to track infectious disease circulation in a community. Recent studies have shown enteric virus and HAV concentrations in wastewater are positively associated with traditional measures of disease occurrence.5, 6, 7 However, there has been limited success in translating virus biomarker concentrations in wastewater to the number of infections in a community. Mechanistic, process-based modelling studies have illustrated that information on biomarker shedding into wastewater via excretions is critical to do so.8, 9, 10, 11, 12 The goal of this study is to characterise enteric virus and HAV shedding in infected patients using a systematic review and meta-analysis approach for this application. The compiled data can be used as input parameters to models to estimate infection occurrence in communities from wastewater measurements of pathogen biomarkers, and to inform knowledge gaps and future research needs on viral shedding.

Methods

Ethics

This is a systematic literature review and meta-analysis with no human subjects, so no ethical approval was needed for this work.

Search strategy and selection criteria

We reviewed the literature to report shedding of human norovirus (NoV), rotavirus (RV), hepatitis A virus (HAV), and enteric adenovirus group F (AdV) in stool, vomit, urine, saliva, mucus, and sputum. These viruses were chosen because we and others have previously measured them in wastewater and found that their concentrations there are associated with traditional disease metrics.13, 14, 15 The selected excretions were included as they enter domestic sewage.¹⁶^,¹⁷ There are other excretions that may be important that we do not consider (e.g., blood, skin sloughing). The systematic review and meta-analysis were pre-registered,¹⁸ and followed the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines.¹⁹

We conducted searches for peer reviewed papers using three databases using search fields as provided in Fig. 1. The applied search terms included enteric virus and excretion names (Supplementary Table S1). The exact date the search was completed is provided in Appendix (p 6).

Identified papers were imported into Covidence (https://www.covidence.org) and duplicates removed. The title and abstract of each paper were reviewed for relevance by one reviewer, and 10% of papers deemed irrelevant were reviewed independently by a second reviewer to confirm the decision making process. If papers seemed to be potentially relevant, they were advanced to full-text review. During full-text review, papers that met the following seven inclusion criteria were retained: (1) published in a peer-reviewed journal; (2) written in English; (3) contained primary data (e.g., not a review); (4) contained original data not generated by a model, estimation, or from another study; (5) contained human shedding data; (6) contained extractable shedding data, defined as concentration or longitudinal presence of the virus in an excretion; wash and swab samples were deemed valid for assessing the presence of the virus in corresponding excretions (e.g., throat swab for saliva, rectal swab for stool); and (7) contained shedding data from individuals without documented chronic infections, immunocompromised health conditions, or co-infection with multiple enteric virus. A second reviewer participated in the full-text review reviewing approximately 10% papers.

We extracted relevant information from each paper: (1) virus and excretion; (2) study type (cross-sectional or longitudinal and challenge/feeding study, natural infection, or vaccination); (3) concentrations or presence of viruses in excretion and the time at which the sample was collected (if provided), and reported units of concentration (if provided); (4) sample size; (5) virus detection method; (6) patient age and symptomatic status; (7) data measurement quality metrics (Supplementary Table S2). In some papers, data were presented in the form of summary statistics without individual-level data. The type of summary statistic was recorded with all related descriptive statistics including the number of individual data used to calculate the summary statistics. For papers presenting shedding data in graphical format, WebPlotDigitizer (https://plotdigitizer.com) was used for data extraction. All extracted data are available from the Stanford Digital Repository (https://doi.org/10.25740/cs445xw7641). Data from 15% of the papers were extracted by a second researcher to ensure that data extraction methods were correct and no errors were made.

Included papers were evaluated according to six quality control criteria (Supplementary Table S2) and each assigned a quality score (QS) between 0 and 6. The paper was categorised as low confidence if QS < 2, moderate confidence if 2 ≤ QS < 4, and high confidence if 4 ≤ QS ≥ 6. Data from papers with QS < 2 were excluded.

Data analysis

The goals of the meta-analysis were to (1) describe observed enteric virus concentrations in excretions and (2) generate longitudinal enteric virus shedding time series in excretions both in terms of concentrations and detection positivity rates. Secondary outcomes included the duration of shedding, timing of peak shedding of viruses, and peak virus concentration (Appendix pp 3,5) in each excretion.

Concentrations of viruses

All reported, measured concentrations of each virus in each excretion were combined, regardless of study design. Assumptions used to do so are outlined in the Appendix (p 2). The resultant data were not normally distributed (Shapiro–Wilk, p < 0.05), so Kruskal–Wallis tests were used to test for differences across viruses and excretions using adjusted p = 0.025 to account for multiple comparisons (Appendix p 3). Dunn post-hoc test with a Bonferoni correction was applied as needed.

Longitudinal concentration data

Longitudinal data includes the time when the excretion was obtained during the course of infection. They were categorised into two distinct groups: those reporting as a function of days after symptom (DAS) onset and days after infection (DAI). Studies reporting as a function of DAS were generally those of natural infection, while those reporting relative to DAI were generally feeding/challenge studies including vaccination studies. In compiling longitudinal data, several assumptions were made, as outlined in the Appendix (pp 2–3). Nonlinear regression models with logistic function and gamma function were used to characterise shedding profiles (Supplementary Table S3). The logistic function was defined as $\log_{10} (c o n c + 1) = A {(1 + \exp (B \times (t - C)))}^{- 1}$ and the gamma function was $\log_{10} (c o n c + 1) = A t^{B} \exp (- C t)$ where conc is concentration, t is time, and A, B, and C are fitting parameters. Functions were fit using nonlinear least squares (NLS) optimisation via the nlsLM function from the minpack.lm package in R (4.4.0). Longitudinal concentration datasets with smaller than 5 discrete days of data were excluded from plotting and shedding profile modelling, as we deemed this number of data points insufficient.

The timing of peak viral shedding was defined as the time at which the highest viral concentration occurred during the shedding process (Appendix p 2). Aggregated peak shedding days were not normally distributed (Shapiro–Wilk, p < 0.05), so we used Kruskal–Wallis to compare across viruses and excretions using p = 0.05 as only one set of comparisons was possible due to data limitations.

Longitudinal presence data

Longitudinal presence data are observations regarding the presence or absence of viruses in excretions over time. Longitudinal concentration studies were incorporated into the longitudinal presence data. Longitudinal presence data were categorised as relative to DAS or DAI, with several additional assumptions in the Appendix (pp 2–3) regardless of study design.

We described virus presence at each available time point using positivity rates: $P o s i t i v i t y r a t e (t i m e) = \frac{Σ p o s i t i v e s a m p l e s}{Σ t o t a l s a m p l e s}$ . For time points where the number of data points was less than 5, the positivity rate was not calculated, as we deemed that such a small sample size would provide a positivity rate with too much uncertainty. Logistic models and gamma models were used to characterise shedding profiles. The logistic and gamma models are defined as above, except on the left hand side of the equation is positivity rate. Datasets with smaller than 5 discrete days of data were excluded for plotting and shedding profile modelling.

The duration of viral shedding, defined as the time interval between day 0 to the last positive sample, was determined from longitudinal presence data (Appendix p 3). The aggregated duration variable was not normal (Shapiro–Wilk, p < 0.05), so Kruskal–Wallis test was used to evaluate differences in the shedding duration across different viruses. The Dunn post-hoc test with a Bonferoni correction was also used.

Heterogeneity across studies for concentration data was quantified using Cochran’s Q test and the I² statistic for each virus–excretion pair. Between study heterogeneity for longitudinal concentration data was evaluated using a nonlinear mixed effect model with the nlme function in R. For each model parameter, the I² statistic was calculated using the standard deviation and residual, representing the variability across studies.

Publication bias was assessed through funnel plot and Begg’s rank correlation test to examine small-study effects. Because the outcomes of this study are from single-group studies without a comparative group and defined effect size (odd ratio or risk ratio), standard publication bias assessments are not directly applicable. Instead, we evaluated whether smaller studies tended to report disproportionately high proportions of positive results, which may indicate a small-study effect. Additional details are in the Appendix (pp 3–4). All the data processing, compiling and analysis were performed in R (4.4.0).

Role of funder

The funder of the study had no role in study design, data collection, data analysis, data interpretation, or the writing of the report. The corresponding author had full access to all data in the study and final responsibility for the decision to submit this systematic review and meta-analysis for publication.

Results

Systematic review

A total of 5002, 6442, 2922 and 902 papers for NoV, RV, HAV, and AdV respectively, were identified from the three databases after dereplication. Following the screening process, 65 papers on NoV, 41 on RV, 27 on HAV, and 6 on AdV (130 papers total) qualified for data extraction (Fig. 1). This total includes two additional papers that were brought to our attention during peer review and met the inclusion criteria but were not captured through the original screening process. Out of the 130 papers, 72% (n = 93) reported sampling methodologies, 100% (n = 130) reported sample detection methods, 62% (n = 80) reported a detection threshold, 25% (n = 32) reported use of controls, 23% (n = 30) reported use of analytical replicates, and 55% (n = 71) reported sample preservation and processing methods (Supplementary Table S4). Four papers (1 NoV, 2 RV, 1 HAV) were categorised as low confidence and excluded leaving 126 included papers (Appendix p 4).

The total number of data points for each virus in each excretion varied between 0 and 6820 (Supplementary Table S5). The largest number of data points were available for stool (n = 18,381), with comparatively fewer data points (n < 250) available for other excretions. A larger number of data points were available for NoV (n = 6558) and RV (n = 9666) compared to HAV (n = 2500) and AdV (n = 218). A summary of the study types and measurement approaches used are in the Appendix (pp 4–5).

Norovirus

NoV concentrations were reported in stool (43 papers),20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40^,41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62 vomit (2 papers),⁵⁴^,⁶¹ and saliva (1 paper).⁶³ Median NoV concentration in these excretions was 7.9 log₁₀ copies per gram stool (interquartile range (IQR) = 6.2–9.1; n = 2888), 4.6 log₁₀ copies per millilitre vomit (IQR = 4.3–5.6; n = 54), and 3.2 log₁₀ copies per millilitre saliva (IQR = 2.6–3.5; n = 8) (Fig. 2). No data were found on NoV concentration in urine, mucus, and sputum.

Fig. 2 — Concentration of various enteric viruses in different excretions: a) stool, b) saliva, and c) vomit. Individual concentration data points are represented as grey circles. Data points exceeding 15 log₁₀ genome copies (gc) per g/mL excretion are not shown in this figure. The lower and upper edges of the boxes correspond to the 25th and 75th percentiles, respectively, while the centre line represents the median. Whiskers extend to the smallest and largest values within 1.5 times the IQR. Abbreviations: NoV = norovirus, RV = rotavirus, HAV = hepatitis A virus, AdV = adenovirus group F.

Longitudinal NoV concentrations were measured in stool relative to DAS (9 papers)²³^,²⁴^,³⁰^,³⁵^,³⁸^,⁴⁵^,⁴⁸^,⁵⁰^,⁵⁹ and relative to DAI (4 papers),²⁹^,⁴⁴^,⁵⁴^,⁶⁴ in saliva relative to DAS (1 paper),⁶³ and in vomit relative to DAI (1 paper).⁵⁴ No longitudinal concentration data were available for other excretions. We applied regression models to the profiles for stool and saliva with respect to DAS and DAI (Fig. 3, Supplementary Table S6). Vomit was not modelled or plotted due to the limited number of discrete days (<5 discrete days). Median peak NoV shedding in stool occurred 4.0 DAS (IQR = 2.0–7.0; n = 46) and 4.0 DAI (IQR = 3.0–5.0; n = 65). The median peak NoV shedding day was 1.0 DAI (IQR = 1.0–1.0; n = 12) in vomit (Fig. 4).

Fig. 3 — Longitudinal concentration profiles of available data on enteric virus shedding in excretions. Only data on NoV, RV, and HAV are available for stool, and only NoV is available in saliva. No other viruses or excretions had sufficient data for plotting. Profiles are plotted as a function of days after symptom onset or days after infection, depending on data availability. Concentrations are expressed log₁₀ genome copies (gc) per g (stool) or mL (saliva); all values were measured by quantitative PCR methods. Grey circles are all raw data extracted from papers on concentrations as a function of time. Blue line is the modelled concentration profile. Model parameters are in Supplementary Table S6. Abbreviations: NoV = norovirus, RV = rotavirus, HAV = hepatitis A virus, AdV = adenovirus group F.

Fig. 4 — Peak day of shedding and duration of shedding in units of days for different enteric viruses in (a–c) Peak day of shedding in stool and vomit, measured relative to days after symptom onset or infection. (d–g) Duration of shedding in stool, saliva, and vomit, relative to days after symptom onset or infection. Grey circles represent individual data points. The lower and upper edges of the boxes correspond to the 25th and 75th percentiles, respectively, while the centre line represents the median. Whiskers extend to the smallest and largest values within 1.5 times the IQR. Abbreviations: NoV = norovirus, RV = rotavirus, HAV = hepatitis A virus, AdV = adenovirus group F.

Longitudinal NoV presence data was provided in stool relative to DAS (24 papers)²³^,²⁴^,³⁰^,³⁵^,³⁸^,⁴⁵^,⁴⁸^,⁵⁰^,⁵⁹^,65, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79 and DAI (8 papers),²⁹^,⁴⁴^,⁵⁴^,⁶²^,⁶⁴^,80, 81, 82 in saliva relative to DAS (3 papers),⁶³^,⁷⁸^,⁸³ and in vomit relative to DAS (3 papers)⁶⁷^,⁷⁶^,⁷⁸ and DAI (2 papers).⁵⁴^,⁸⁴ We modelled the profiles for stool and saliva (Fig. 5, Supplementary Table S6). Vomit was not modelled or plotted due to insufficient data (<5 discrete days). Median NoV shedding duration in stool was 11.5 DAS (IQR = 6.0–22.0; n = 80) and 14.0 DAI (IQR = 9.0–27.0; n = 49). Median NoV shedding duration in vomit was 1.0 DAI (n = 1). Median shedding duration for NoV in saliva was 13.0 DAS (IQR = 11.5–13.0; n = 6) (Fig. 4). No studies provided longitudinal presence data on NoV in urine, mucus, or sputum.

Fig. 5 — Longitudinal positivity rate profiles of available data on enteric virus shedding in excretions. Only data on NoV, RV, and HAV are available for stool, and only NoV is available in saliva. No other viruses or excretions had sufficient data for plotting. Profiles are plotted as a function of days after symptom onset or days after infection, depending on data availability. Grey circles represent combined positivity rates calculated for each day as a function of time. Blue line is the modelled positivity rate profile. Model parameters are in Supplementary Table S6. Abbreviations: NoV = norovirus, RV = rotavirus, HAV = hepatitis A virus, AdV = adenovirus group F.

Rotavirus

Sixteen papers presented data on RV concentration in stool.²¹^,³⁴^,⁴⁵^,⁴⁹^,⁵⁵^,85, 86, 87, 88, 89, 90, 91, 92, 93, 94, 95 Median RV concentration in stool was 6.5 log₁₀ copies per gram (IQR = 5.1–7.7; n = 1391) (Fig. 2). No paper reported concentration data in other excretions.

Longitudinal RV concentration data in stool was measured as a function of DAS (1 paper)⁴⁵ and DAI (5 papers).⁸⁵^,⁸⁷^,⁸⁸^,⁹¹^,⁹⁴ Profiles and their models (Supplementary Table S6) are provided in Fig. 3. Median peak day of RV shedding in stool occurred 3.0 DAI (IQR = 1.0–7.0; n = 99) (Fig. 4).

Longitudinal RV presence data was provided in stool as a function of DAS (11 papers)⁴⁵^,96, 97, 98, 99, 100, 101, 102, 103, 104, 105 and DAI (19 papers)⁸⁵^,⁸⁷^,⁸⁸^,⁹⁴^,106, 107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117, 118, 119, 120 and in saliva as a function of DAS (1 papers).¹⁰¹ Regression models were applied to the stool profiles (Fig. 5, Supplementary Table S6). Saliva data were not modelled or plotted because data were only available for a limited number (<5) days. Median RV shedding duration in stool was 8.0 DAS (IQR = 6.0–14.8; n = 48) and 5.0 DAI (IQR = 2.5–10.0; n = 75) (Fig. 4). While none of the studies investigated RV shedding in excretions beyond stool and saliva, a limited number of reports (which did not fit our inclusion criteria) noted the detection of RV RNA in other excretions, such as vomit,¹²¹^,¹²² urine,¹²³^,¹²⁴ and nasal secretions.125, 126, 127

Hepatitis A virus

HAV concentration data were provided in stool (7 papers)²¹^,128, 129, 130, 131, 132, 133 and saliva (4 papers).134, 135, 136, 137 Median HAV concentration was 4.8 log₁₀ copies per gram stool (IQR = 3.7–6.1; n = 150) and 3.2 log₁₀ copies per millilitre saliva (IQR = 3.2–3.6; n = 69) (Fig. 2). No data were identified regarding HAV concentration in other excretions.

Longitudinal concentration data were reported for HAV shedding in stool measured as a function of DAS (2 papers), and the profile was modelled (Fig. 3, Supplementary Table S6).¹²⁹^,¹³³ One paper reported data in saliva as a function of DAS.¹³⁵ Median peak day of HAV shedding in stool was 18.0 DAS (IQR = 16.0–25.5; n = 3) (Fig. 4).

Longitudinal HAV presence data for stool was provided as a function of DAS (14 papers)¹²⁹^,¹³³^,138, 139, 140, 141, 142, 143, 144, 145, 146, 147, 148, 149 and DAI (4 papers),149, 150, 151, 152 and in saliva as a function of DAS (2 papers).¹³⁵^,¹⁴⁶ These data were modelled (Fig. 5, Supplementary Table S6). Median HAV shedding duration in stool was 9.5 DAS (IQR = 5.8–18.0; n = 18) and 35.0 DAI (IQR = 34.0–41.0; n = 5) (Fig. 4). Although no studies included in the analysis reported HAV shedding in excretions other than stool and saliva, one study (not meeting our inclusion criteria) documented HAV RNA presence in urine.¹⁵³

Adenovirus group F

Six papers provided concentration data on AdV in stool.⁴⁹^,⁸⁶^,154, 155, 156, 157 Median AdV concentration in stool was 8.5 log₁₀ copies per gram (IQR = 6.2–11.2; n = 216) (Fig. 2). Concentration data were not available for other excretions.

One paper reported longitudinal AdV concentration data in stool as a function of DAS.¹⁵⁴ For longitudinal presence data, 1 study provided data for stool as a function of DAS.¹⁵⁴ As both the longitudinal concentration and presence data had a limited number of discrete days (<5 discrete days), they were not plotted or modelled. While no studies investigated AdV shedding in excretions other than stool, there were reports (not meeting our inclusion criteria) documenting the AdV presence in saliva,¹⁵⁸ and urine.¹⁵⁹^,¹⁶⁰

Meta-analysis

We compared concentration across excretion types for each virus. Median NoV concentration was highest in stool followed by vomit and saliva (Fig. 2). NoV concentrations were significantly different across excretion types (Kruskal–Wallis test, p < 0.0001). Post hoc tests indicated significant differences in concentrations between stool and saliva, and stool and vomit (both p < 0.0001). Median HAV concentration was significantly higher in stool compared to saliva (Fig. 2, p < 0.0001). No statistical test was conducted to compare virus concentrations of RV and AdV across different excretions as concentration data for these viruses were only available for stool.

We compared concentrations across viruses for each excretion type. In stool, median AdV concentration was highest, followed by NoV, RV, and HAV (Fig. 2); concentrations were different (p < 0.0001). Post hoc analysis indicated statistically significant differences between all pairs of viruses (all p < 0.001). There was no difference in concentrations of NoV and HAV measured in saliva (p = 0.48). Statistical comparisons for other excretions were not conducted due to lack of data.

We compared peak day across excretions for each virus. For data reported relative to DAI, the median peak shedding day of NoV occurred 3.0 days earlier in vomit than in stool, and the difference in peak day was statistically significant (p < 0.0001). It was not possible to compare the peak shedding day for other viruses due to insufficient (n < 2) or lack of data.

We compared peak day across viruses for each excretion. For data reported relative to DAS, the median peak day of shedding for NoV was earlier for HAV (p = 0.0044). For data reported relative to DAI, median peak shedding day in stool occurred earlier for RV (3.0 days) than NoV (4.0 days); differences were not statistically significant (p = 0.16). Data were unavailable for other comparisons.

We compared shedding duration across excretions for each virus. For data reported as a function of DAS, the median duration of shedding for NoV was longer in saliva (13 days), than stool (11.5 days) (Fig. 4), and the difference was not statistically different (p = 0.95). Other comparisons were not possible due to lack of data.

We compared shedding duration across viruses for each excretion. The median duration of shedding in stool relative to DAS was longest for NoV (11.5 days) followed by HAV (9.5 days), and RV (8.0 days) (Fig. 4); durations were not significantly different (p = 0.68). For data reported relative to DAI, median shedding duration in stool was longest for HAV (35.0 days) followed by NoV (14.0 days) and RV (5.0 days) (Fig. 4); the durations were significantly different (p < 0.0001). Post hoc tests showed statistically significant differences between NoV and HAV (p = 0.032), NoV and RV (p < 0.0001) and RV and HAV (p < 0.0001). Other comparisons were not possible owing to lack of data.

Between study heterogeneity was found among concentration data from most virus–excretion pairs, with I² statistics ranging from 0% to 97.5% (Supplementary Table S7 and Appendix p 5). The I² for longitudinal concentration data ranged from 0% to 65.7% (Supplementary Table S8 and Appendix p 5). Between study heterogeneity was not found for parameters across most virus–excretion profiles, except for parameter A for RV measured in stool relative to DAI, which showed an I² of 65.7%.

Publication bias

Funnel plots were used to assess the presence of small-study effects for all included papers and each virus subgroup (Supplementary Fig. S3). Although visual inspection of plots showed some asymmetry, Begg’s rank correlation did not detect statistically significant asymmetry (p = 0.71) nor for any virus subgroup (Appendix p 5), indicating limited evidence of publication bias.

Discussion

There are limited cross sectional and longitudinal data on enteric virus and HAV shedding in excretions we considered in this study. AdV data were most limited while NoV data were most available. Stool concentrations were available for each virus while we found very limited to no concentrations in saliva, sputum, urine, mucus, and vomit. Additional research is needed to measure viral concentrations in these excretions to inform interpretation of their concentrations in wastewater for WBE applications.

Only HAV and NoV concentrations in excretions other than stool were available in the literature. For NoV, concentrations tended to be highest in stool compared to other excretions (vomit and saliva). On a per mass basis, stool tended to have 1000 times higher NoV concentrations than other excretions. In contrast, HAV concentrations in stool and saliva tended to be similar. The flux of stool (mass per day) into wastewater is expected to be higher than that of vomitus or saliva on an individual basis which might suggest that of these three excretions,¹⁶¹ stool is the main excretion contributing NoV and HAV to wastewater. A mechanistic modelling study, like that of Chen and Bibby,¹⁶¹ could assess the relative importance of different excretions in contribution biomarkers to wastewater; however, such an analysis is beyond the scope of the current study.

We previously conducted a review of respiratory virus shedding in excretions that contribute to wastewater.¹⁶² In that study, we also identified a lack of quantitative data, with the most available for influenza. In contrast to the findings here for NoV, where stool had higher concentrations than saliva by three orders of magnitude, influenza concentrations were higher in saliva compared to stool by two to three orders of magnitude. This is perhaps not unexpected as NoV infects the gastrointestinal tract and influenza primarily the respiratory tract. Interestingly, concentrations of NoV in wastewater tend to be much higher than concentrations of influenza.⁷^,¹⁶³

Median shedding durations varied between 8 and 13 DAS or 1 and 35 DAI depending on virus and excretion. HAV tended to have the longest shedding duration (35 DAI) among all the viruses. This prolonged shedding may be attributable to the unique pathogenesis of HAV (liver as main site of infection).³ Shedding duration defines the length of time an infected individual may contribute biomarkers to wastewater via a specific excretion and therefore the duration that a biomarker of disease may be detected in wastewater. For example, the long duration of shedding of HAV may suggest that detection of HAV in wastewater could indicate the presence of convalescing individuals in a sewershed rather than acutely ill individuals.

In our study, we chose to not combine data measured as a function of DAS and DAI as the time period between infection and symptom onset (incubation time) can be highly uncertain and vary among individuals.¹⁶⁴ By subtracting median shedding duration for the same virus and excretion measured as a function of DAS and DAI, we can estimate incubation time. This was only possible using stool for NoV, HAV, and RV, and we calculated incubation time to be 2.5, 25.5, and −3 days, respectively. The value for RV is unrealistic and a result of uncertainty in the parameters. However, these values generally agree with studies that state incubation times for RV and NoV are short (less than 48 h),¹⁶⁵^,¹⁶⁶ while incubation time for HAV is long (15–50 days).¹⁶⁷ In our review of the literature, we also found longitudinal data measured as a function of days after detection. Given the uncertainties associated with interpreting this measure of time, we omitted such data from our analysis.

The longitudinal data provided in this paper can be used to model the prevalence, reproductive numbers, and incidence forecasts of different diseases.168, 169, 170 Similarly, concentration data can be used to inform estimates of the number of infected individuals contributing biomarkers to wastewater.⁹^,171, 172, 173 Aside from using these data to improve interpretation of biomarker concentrations in wastewater, the concentration data summarised herein may also be useful for microbial risk assessments where hazard identification and characterisation is the first step.¹⁷⁴^,¹⁷⁵

It is important to note that many of the papers we included in this study were lacking in one or more quality control metrics. In particular, many studies omitted data on laboratory methods including the use of positive and negative controls and replication and study detection limits. Such information is essential when reporting on measurements of viruses and we recommend that future work in this area use accepted data reporting guidelines such as the Minimum Information for Publication of Quantitative Real-Time PCR Experiments (MIQE) or the Environmental Microbiology Minimum Information (EMMI) guidelines for PCR measurements.¹⁷⁶^,¹⁷⁷ We found that some studies reported pseudo virus concentrations by reporting Cq values from quantitative PCR machines. Without detailed information on standard curves and other methodological details, these values have limited external validity and therefore could not be used to inform our analysis of concentrations in excretions. We urge laboratories to report quantitative data according to the MIQE or EMMI guidelines so that they are externally valid.¹⁷⁶^,¹⁷⁷

There are several limitations associated with this work. First, it is important to note that there were different and limited data available across viruses and excretions which may lead to biases in our analyses that compare such measurements. Some studies reported paired data, and we did not omit those from our meta-analysis, doing so yielded the same results as including them (Appendix p 5). Second, we did not consider the role of dose in affecting shedding in studies that were viral feeding and challenge studies. Third, we combined data from studies conducted using different measurement methods for the analyses. Fourth, we did not differentiate between studies conducted using vaccines; for example, much of the RV longitudinal studies focused on post-vaccination shedding in stool. Fifth, the data reported herein likely under-represent shedding from asymptomatic natural infections, which would not be captured by the study designs implemented by researchers. We recommend future studies that target this population, as their contributions to wastewater may be important, and lack of knowledge about them may bias interpretation of wastewater concentration of biomarkers. Finally, we did not attempt to examine variation in shedding between different populations (i.e., adults versus children). All data available from this review are available for other researchers should they desire to conduct further analyses to account for some of these limitations. Future work is recommended to systematically compile and analyse shedding data for other important enteric viruses such as hepatitis E virus, astrovirus, and enteroviruses. The compiled data offer valuable insights that can inform and improve initial modelling efforts for infection rate estimation using wastewater-based epidemiology, pending further validation.

Contributors

GZ contributed to the conceptualism of the study, data curation, formal analysis, methodology, visualisation, writing the original draft, and reviewing subsequent drafts. EMGC contributed to the methodology, data curation, and reviewing subsequent drafts. ABB contributed to the conceptualism of the study, methodology, project administration, visualisation, writing the original draft, reviewing subsequent drafts, supervision, and funding acquisition. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication. All authors verified the underlying data of the study.

Data sharing statement

Compiled data are immediately available publicly at the Stanford Digital Repository (https://doi.org/10.25740/cs445xw7641). Details regarding functions used in R are provided in the text and so no data analysis code is provided.

Declaration of interests

AB has received funding from the Sergey Brin Family Foundation for this work, as well as funding from the Sloan Foundation and the National Science Foundation for related work. Additionally, AB has served on a wastewater-based epidemiology advisory committee for the California Water Boards. All other authors declare no competing interests.

Acknowledgements

This study was supported by a gift from the Sergey Brin Family Foundation to ABB. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, and approval of the manuscript; and decision to submit the manuscript for publication.

Footnotes

^{Appendix A}

Supplementary data related to this article can be found at https://doi.org/10.1016/j.ebiom.2025.105878.

Appendix A. Supplementary data

Supplementary Figs. S1–S3 and Tables S1–S9

mmc1.pdf^{(639.1KB, pdf)}

References

1.WHO Diarrhoeal disease. https://www.who.int/news-room/fact-sheets/detail/diarrhoeal-disease
2.Greening G.E., Cannon J.L. In: Viruses in foods. Goyal S.M., Cannon J.L., editors. Springer International Publishing; Cham: 2016. Human and animal viruses in food (including taxonomy of enteric viruses) pp. 5–57. [Google Scholar]
3.WHO Hepatitis A. https://www.who.int/news-room/fact-sheets/detail/hepatitis-a
4.Thielman N.M., Guerrant R.L. Acute infectious diarrhea. N Engl J Med. 2004;350:38–47. doi: 10.1056/NEJMcp031534. [DOI] [PubMed] [Google Scholar]
5.Kazama S., Miura T., Masago Y., et al. Environmental surveillance of norovirus genogroups I and II for sensitive detection of epidemic variants. Appl Environ Microbiol. 2017;83:e03406–e03416. doi: 10.1128/AEM.03406-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
6.Wang H., Churqui M.P., Tunovic T., et al. Measures against COVID-19 affected the spread of human enteric viruses in a Swedish community, as found when monitoring wastewater. Sci Total Environ. 2023;895 doi: 10.1016/j.scitotenv.2023.165012. [DOI] [PMC free article] [PubMed] [Google Scholar]
7.Boehm A.B., Wolfe M.K., White B.J., et al. Human norovirus (HuNoV) GII RNA in wastewater solids at 145 United States wastewater treatment plants: comparison to positivity rates of clinical specimens and modeled estimates of HuNoV GII shedders. J Expo Sci Environ Epidemiol. 2024;34:440–447. doi: 10.1038/s41370-023-00592-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
8.Silverman A.I., Boehm A.B. Systematic review and meta-analysis of the persistence of enveloped viruses in environmental waters and wastewater in the absence of disinfectants. Environ Sci Technol. 2021;55:14480–14493. doi: 10.1021/acs.est.1c03977. [DOI] [PubMed] [Google Scholar]
9.Soller J., Jennings W., Schoen M., et al. Modeling infection from SARS-CoV-2 wastewater concentrations: promise, limitations, and future directions. J Water Health. 2022;20:1197–1211. doi: 10.2166/wh.2022.094. [DOI] [PMC free article] [PubMed] [Google Scholar]
10.Wu F., Xiao A., Zhang J., et al. SARS-CoV-2 titers in wastewater foreshadow dynamics and clinical presentation of new COVID-19 cases. medRxiv. 2020 doi: 10.1101/2020.06.15.20117747. [DOI] [PMC free article] [PubMed] [Google Scholar]
11.Zhu Y., Oishi W., Maruo C., et al. Early warning of COVID-19 via wastewater-based epidemiology: potential and bottlenecks. Sci Total Environ. 2021;767 doi: 10.1016/j.scitotenv.2021.145124. [DOI] [PMC free article] [PubMed] [Google Scholar]
12.Phan T., Brozak S., Pell B., et al. Making waves: integrating wastewater surveillance with dynamic modeling to track and predict viral outbreaks. Water Res. 2023;243 doi: 10.1016/j.watres.2023.120372. [DOI] [PubMed] [Google Scholar]
13.Yu A.T., Burnor E., Rabe A., et al. Wastewater surveillance for norovirus, California, USA. Emerg Infect Dis. 2024;30:2438. doi: 10.3201/eid3011.241001. [DOI] [PMC free article] [PubMed] [Google Scholar]
14.Fantilli A., Cola G.D., Castro G., et al. Hepatitis A virus monitoring in wastewater: a complementary tool to clinical surveillance. Water Res. 2023;241 doi: 10.1016/j.watres.2023.120102. [DOI] [PubMed] [Google Scholar]
15.Boehm A.B., Shelden B., Duong D., Banaei N., White B.J., Wolfe M.K. A retrospective longitudinal study of adenovirus group F, norovirus GI and GII, rotavirus, and enterovirus nucleic acids in wastewater solids at two wastewater treatment plants: solid-liquid partitioning and relation to clinical testing data. mSphere. 2024;9 doi: 10.1128/msphere.00736-23. [DOI] [PMC free article] [PubMed] [Google Scholar]
16.Crank K., Chen W., Bivins A., Lowry S., Bibby K. Contribution of SARS-CoV-2 RNA shedding routes to RNA loads in wastewater. Sci Total Environ. 2022;806 doi: 10.1016/j.scitotenv.2021.150376. [DOI] [PMC free article] [PubMed] [Google Scholar]
17.Ghosh S., Kumar M., Santiana M., et al. Enteric viruses replicate in salivary glands and infect through saliva. Nature. 2022;607:345–350. doi: 10.1038/s41586-022-04895-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
18.Zheng G., Boehm AB. Systematic review and meta-analysis of enteric virus shedding in human excretions. OSF; 2024. http://osf.io/ecb8f [DOI] [PubMed] [Google Scholar]
19.Page M.J., McKenzie J.E., Bossuyt P.M., et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372 doi: 10.1136/bmj.n71. [DOI] [PMC free article] [PubMed] [Google Scholar]
20.Lai C.-C., Wang Y.-H., Wu C.-Y., Hung C.-H., Jiang D.D.-S., Wu F.-T. A norovirus outbreak in a nursing home: norovirus shedding time associated with age. J Clin Virol. 2013;56:96–101. doi: 10.1016/j.jcv.2012.10.011. [DOI] [PubMed] [Google Scholar]
21.Coudray-Meunier C., Fraisse A., Martin-Latil S., Delannoy S., Fach P., Perelle S. A novel high-throughput method for molecular detection of human pathogenic viruses using a nanofluidic real-time PCR system. PLoS One. 2016;11 doi: 10.1371/journal.pone.0147832. [DOI] [PMC free article] [PubMed] [Google Scholar]
22.Bucardo F., Nordgren J., Carlsson B., et al. Asymptomatic norovirus infections in Nicaraguan children and its association with viral properties and histo-Blood group antigens. Pediatr Infect Dis J. 2010;29:934. doi: 10.1097/INF.0b013e3181ed9f2f. [DOI] [PubMed] [Google Scholar]
23.Takanashi S., Wang Q., Chen N., et al. Characterization of emerging GII.g/GII.12 noroviruses from a gastroenteritis outbreak in the United States in 2010. J Clin Microbiol. 2020;49:3234–3244. doi: 10.1128/JCM.00305-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
24.Lee C.-C., Chiu C.-H., Lee H.-Y., Tsai C.-N., Chen C.-L., Chen S.-Y. Clinical and virological characteristics of viral shedding in children with norovirus gastroenteritis. J Microbiol Immunol Infect. 2022;55:1188–1194. doi: 10.1016/j.jmii.2021.10.006. [DOI] [PubMed] [Google Scholar]
25.Shigemoto N., Tanizawa Y., Matsuo T., et al. Clinical evaluation of a bioluminescent enzyme immunoassay for detecting norovirus in fecal specimens from patients with acute gastroenteritis. J Med Virol. 2014;86:1219–1225. doi: 10.1002/jmv.23765. [DOI] [PubMed] [Google Scholar]
26.Höhne M., Schreier E. Detection and characterization of norovirus outbreaks in Germany: application of a one-tube RT-PCR using a fluorogenic real-time detection system. J Med Virol. 2004;72:312–319. doi: 10.1002/jmv.10573. [DOI] [PubMed] [Google Scholar]
27.Scipioni A., Bourgot I., Mauroy A., et al. Detection and quantification of human and bovine noroviruses by a TaqMan RT-PCR assay with a control for inhibition. Mol Cell Probes. 2008;22:215–222. doi: 10.1016/j.mcp.2008.02.003. [DOI] [PubMed] [Google Scholar]
28.Nishimura N., Nakayama H., Yoshizumi S., et al. Detection of noroviruses in fecal specimens by direct RT-PCR without RNA purification. J Virol Methods. 2010;163:282–286. doi: 10.1016/j.jviromet.2009.10.011. [DOI] [PubMed] [Google Scholar]
29.Kirby A.e., Shi J., Montes J., Lichtenstein M., Moe C l. Disease course and viral shedding in experimental Norwalk virus and snow Mountain virus infection. J Med Virol. 2014;86:2055–2064. doi: 10.1002/jmv.23905. [DOI] [PubMed] [Google Scholar]
30.Aoki Y., Suto A., Mizuta K., Ahiko T., Osaka K., Matsuzaki Y. Duration of norovirus excretion and the longitudinal course of viral load in norovirus-infected elderly patients. J Hosp Infect. 2010;75:42–46. doi: 10.1016/j.jhin.2009.12.016. [DOI] [PubMed] [Google Scholar]
31.Costantini V.P., Cooper E.M., Hardaker H.L., et al. Epidemiologic, virologic, and host genetic factors of norovirus outbreaks in long-term care facilities. Clin Infect Dis Off Publ Infect Dis Soc Am. 2015;62:1. doi: 10.1093/cid/civ747. [DOI] [PMC free article] [PubMed] [Google Scholar]
32.Pang X., Lee B., Chui L., Preiksaitis J.K., Monroe S.S. Evaluation and validation of real-time reverse transcription-pcr assay using the LightCycler system for detection and quantitation of norovirus. J Clin Microbiol. 2004;42:4679–4685. doi: 10.1128/JCM.42.10.4679-4685.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
33.Théry L., Bidalot M., Pothier P., Ambert-Balay K. Evaluation of immunochromatographic tests for the rapid detection of the emerging GII.17 norovirus in stool samples, January 2016. Eurosurveillance. 2016;21 doi: 10.2807/1560-7917.ES.2016.21.4.30115. [DOI] [PubMed] [Google Scholar]
34.Pratte-Santos R., Miagostovich M.P., Fumian T.M., et al. High prevalence of enteric viruses associated with acute gastroenteritis in pediatric patients in a low-income area in vitória, Southeastern Brazil. J Med Virol. 2019;91:744–750. doi: 10.1002/jmv.25392. [DOI] [PubMed] [Google Scholar]
35.Miyoshi T., Uchino K., Yoshida H., et al. Long-term viral shedding and viral genome mutation in norovirus infection. J Med Virol. 2015;87:1872–1880. doi: 10.1002/jmv.24242. [DOI] [PubMed] [Google Scholar]
36.Kumthip K., Khamrin P., Ushijima H., Maneekarn N. Molecular detection and characterization of norovirus in asymptomatic food handlers in Chiang Mai, Thailand. Infect Genet Evol. 2021;89 doi: 10.1016/j.meegid.2021.104725. [DOI] [PubMed] [Google Scholar]
37.Henke-Gendo C., Harste G., Juergens-Saathoff B., Mattner F., Deppe H., Heim A. New real-time PCR detects prolonged norovirus excretion in highly immunosuppressed patients and children. J Clin Microbiol. 2009;47:2855–2862. doi: 10.1128/JCM.00448-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
38.Tu E.T.-V., Bull R.A., Kim M.-J., et al. Norovirus excretion in an aged-care setting. J Clin Microbiol. 2008;46:2119. doi: 10.1128/JCM.02198-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
39.Rajko-Nenow P., Keaveney S., Flannery J., McIntyre A., Doré W. Norovirus genotypes implicated in two oyster-related illness outbreaks in Ireland. Epidemiol Infect. 2013;142:2096. doi: 10.1017/S0950268813003014. [DOI] [PMC free article] [PubMed] [Google Scholar]
40.Dábilla N., Nunes Vieira Almeida T., Carvalho Rebouças Oliveira A., et al. Norovirus in feces and nasopharyngeal swab of children with and without acute gastroenteritis symptoms: first report of GI.5 in Brazil and GI.3 in nasopharyngeal swab. J Clin Virol Off Publ Pan Am Soc Clin Virol. 2017;87:60–66. doi: 10.1016/j.jcv.2016.12.009. [DOI] [PubMed] [Google Scholar]
41.Munir N., Liu P., Gastañaduy P., Montes J., Shane A., Moe C. Norovirus infection in immunocompromised children and children with hospital-acquired acute gastroenteritis. J Med Virol. 2014;86:1203–1209. doi: 10.1002/jmv.23774. [DOI] [PubMed] [Google Scholar]
42.Ozawa K., Oka T., Takeda N., Hansman G.S. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J Clin Microbiol. 2007;45:3996–4005. doi: 10.1128/JCM.01516-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
43.Reymão T.K.A., Fumian T.M., Justino M.C.A., et al. Norovirus RNA in serum associated with increased fecal viral load in children: detection, quantification and molecular analysis. PLoS One. 2018;13 doi: 10.1371/journal.pone.0199763. [DOI] [PMC free article] [PubMed] [Google Scholar]
44.Atmar R.L., Opekun A.R., Gilger M.A., et al. Norwalk virus shedding after experimental human infection. Emerg Infect Dis. 2008;14(10):1553–1557. doi: 10.3201/eid1410.080117. [DOI] [PMC free article] [PubMed] [Google Scholar]
45.Gutierrez M.B., de Figueiredo M.R., Fialho A.M., Cantelli C.P., Miagostovich M.P., Fumian T.M. Nosocomial acute gastroenteritis outbreak caused by an equine-like G3P[8] DS-1-like rotavirus and GII.4 Sydney[P16] norovirus at a pediatric hospital in Rio de Janeiro, Brazil, 2019. Hum Vaccines Immunother. 2021;17:4654–4660. doi: 10.1080/21645515.2021.1963169. [DOI] [PMC free article] [PubMed] [Google Scholar]
46.La Rosa G., Pourshaban M., Iaconelli M., Muscillo M. Quantification of norovirus genogroups I and II in environmental and clinical samples using TaqMan real-time RT-PCR. Food Environ Virol. 2009;1:15–22. [Google Scholar]
47.Fumian T.M., Justino M.C.A., Mascarenhas J.D.P., et al. Quantitative and molecular analysis of noroviruses RNA in blood from children hospitalized for acute gastroenteritis in Belém, Brazil. J Clin Virol. 2013;58:31–35. doi: 10.1016/j.jcv.2013.06.043. [DOI] [PubMed] [Google Scholar]
48.Teunis P.F.M., Sukhrie F.H.A., Vennema H., Bogerman J., Beersma M.F.C., Koopmans M.P.G. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol Infect. 2015;143:1710–1717. doi: 10.1017/S095026881400274X. [DOI] [PMC free article] [PubMed] [Google Scholar]
49.Qiu Y., Freedman S.B., Williamson-Urquhart S., et al. Significantly longer shedding of norovirus compared to rotavirus and adenovirus in children with acute gastroenteritis. Viruses. 2023;15 doi: 10.3390/v15071541. [DOI] [PMC free article] [PubMed] [Google Scholar]
50.Obara M., Hasegawa S., Iwai M., et al. Single base substitutions in the capsid region of the norovirus genome during viral shedding in cases of infection in areas where norovirus infection is endemic. J Clin Microbiol. 2008;46:3397–3403. doi: 10.1128/JCM.01932-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
51.Fioretti J.M., Fumian T.M., Rocha M.S., et al. Surveillance of Noroviruses in Rio De Janeiro, Brazil: occurrence of New GIV Genotype in Clinical and Wastewater Samples. Food Environ Virol. 2018;10:1–6. doi: 10.1007/s12560-017-9308-2. [DOI] [PubMed] [Google Scholar]
52.Miyoshi M., Yoshizumi S., Ishida S., et al. Usefulness of the rapid determination system of viral genome sequences in human stool specimens. J Virol Methods. 2012;179:256–260. doi: 10.1016/j.jviromet.2011.11.013. [DOI] [PubMed] [Google Scholar]
53.Sarmento S.K., de Andrade J.D.S.R., Miagostovich M.P., Fumian T.M. Virological and epidemiological features of norovirus infections in Brazil, 2017–2018. Viruses. 2021;13 doi: 10.3390/v13091724. [DOI] [PMC free article] [PubMed] [Google Scholar]
54.Kirby A.E., Streby A., Moe C.L. Vomiting as a symptom and transmission risk in norovirus illness: evidence from human challenge studies. PLoS One. 2016;11 doi: 10.1371/journal.pone.0143759. [DOI] [PMC free article] [PubMed] [Google Scholar]
55.Fumian T.M., Leite J.P.G., Rocha M.S., et al. Performance of a one-step quantitative duplex RT-PCR for detection of rotavirus A and noroviruses GII during two periods of high viral circulation. J Virol Methods. 2016;228:123–129. doi: 10.1016/j.jviromet.2015.11.008. [DOI] [PubMed] [Google Scholar]
56.Ushijima H., Thongprachum A., Khamrin P., et al. Evaluation of immunochromatographic tests and a new enzyme immunoassay for detection of a novel GII.17 norovirus in stool samples. Jpn J Infect Dis. 2017;70:326–328. doi: 10.7883/yoken.JJID.2016.413. [DOI] [PubMed] [Google Scholar]
57.Huynen P., Mauroy A., Martin C., et al. Molecular epidemiology of norovirus infections in symptomatic and asymptomatic children from bobo dioulasso, Burkina Faso. J Clin Virol. 2013;58:515–521. doi: 10.1016/j.jcv.2013.08.013. [DOI] [PubMed] [Google Scholar]
58.González G.G., Liprandi F., Ludert J.E. Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol. 2011;83:1972–1982. doi: 10.1002/jmv.22185. [DOI] [PubMed] [Google Scholar]
59.Pombubpa K., Kittigul L. Assessment of a rapid immunochromatographic test for the diagnosis of norovirus gastroenteritis. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2012;31:2379–2383. doi: 10.1007/s10096-012-1579-9. [DOI] [PubMed] [Google Scholar]
60.Sakamaki N., Ohiro Y., Ito M., et al. Bioluminescent enzyme immunoassay for the detection of norovirus capsid antigen. Clin Vaccine Immunol. 2012;19:1949–1954. doi: 10.1128/CVI.00427-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
61.Atmar R.L., Opekun A.R., Gilger M.A., et al. Determination of the 50% human infectious dose for norwalk virus. J Infect Dis. 2014;209:1016–1022. doi: 10.1093/infdis/jit620. [DOI] [PMC free article] [PubMed] [Google Scholar]
62.Rouphael N., Beck A., Kirby A.E., et al. Dose-response of a Norovirus GII.2 controlled human challenge model inoculum. J Infect Dis. 2022;226:1771–1780. doi: 10.1093/infdis/jiac045. [DOI] [PMC free article] [PubMed] [Google Scholar]
63.Anfruns-Estrada E., Sabrià A., Fuentes C., et al. Detection of norovirus in saliva samples from acute gastroenteritis cases and asymptomatic subjects: association with age and higher shedding in stool. Viruses. 2020;12:1369. doi: 10.3390/v12121369. [DOI] [PMC free article] [PubMed] [Google Scholar]
64.Newman K.L., Moe C.L., Kirby A.E., Flanders W.D., Parkos C.A., Leon J.S. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol. 2016;184:347–357. doi: 10.1111/cei.12772. [DOI] [PMC free article] [PubMed] [Google Scholar]
65.Lee N., Chan M.C.W., Wong B., et al. Fecal viral concentration and diarrhea in Norovirus gastroenteritis. Emerg Infect Dis. 2007;13(9):1399–1401. doi: 10.3201/eid1309.061535. [DOI] [PMC free article] [PubMed] [Google Scholar]
66.Chiba S., Sakuma Y., Kogasaka R., et al. Fecal shedding of virus in relation to the days of illness in infantile gastroenteritis due to calicivirus. J Infect Dis. 1980;142:247–249. doi: 10.1093/infdis/142.2.247. [DOI] [PubMed] [Google Scholar]
67.Cheng H.-Y., Hung M.-N., Chen W.-C., et al. Ice-associated norovirus outbreak predominantly caused by GII.17 in Taiwan, 2015. BMC Public Health. 2017;17:870. doi: 10.1186/s12889-017-4869-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
68.Verhoef L., Boxman I.L., Duizer E., et al. Multiple exposures during a norovirus outbreak on a river-cruise sailing through Europe, 2006. Euro Surveill. 2008;13 [PubMed] [Google Scholar]
69.Rockx B., de Wit M., Vennema H., et al. Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis. 2002;35:246–253. doi: 10.1086/341408. [DOI] [PubMed] [Google Scholar]
70.Jacqueline C., Del Valle Arrojo M., Bellver Moreira P., et al. 3[P12] outbreak associated with the drinking water supply in a rural area in Galicia, Spain, 2021. Microbiol Spectr. 2022;10 doi: 10.1128/spectrum.01048-22. [DOI] [PMC free article] [PubMed] [Google Scholar]
71.Phumpholsup T., Theamboonlers A., Wanlapakorn N., et al. Norovirus outbreak at a daycare center in BANGKOK, 2014. Southeast Asian J Trop Med Public Health. 2015;46:616–623. [PubMed] [Google Scholar]
72.Hedlund K.-O., Bennet R., Eriksson M., Ehrnst A. Norwalk-like virus as a cause of diarrhea in a pediatric hospital. Clin Microbiol Infect. 1998;4:417–421. [Google Scholar]
73.Struve J., Bennet R., Ehrnst A., et al. Nosocomial calicivirus gastroenteritis in a pediatric hospital. Pediatr Infect Dis J. 1994;13:882–885. doi: 10.1097/00006454-199410000-00007. [DOI] [PubMed] [Google Scholar]
74.Haruki K., Seto Y., Murakami T., Kimura T. Pattern of shedding of small, round-structured virus particles in stools of patients of outbreaks of food-poisoning from raw oysters. Microbiol Immunol. 1991;35:83–86. doi: 10.1111/j.1348-0421.1991.tb01536.x. [DOI] [PubMed] [Google Scholar]
75.Thornhill T.S., Kalica A.R., Wyatt R.G., Kapikian A.Z., Chanock R.M. Pattern of shedding of the norwalk particle in stools during experimentally induced gastroenteritis in volunteers as determined by immune electron microscopy. J Infect Dis. 1975;132:28–34. doi: 10.1093/infdis/132.1.28. [DOI] [PubMed] [Google Scholar]
76.Prystajecky N., Brinkman F.S., Auk B., Isaac-Renton J.L., Tang P. Personalized genetic testing and norovirus susceptibility. Can J Infect Dis Med Microbiol. 2014;25:222. doi: 10.1155/2014/708579. [DOI] [PMC free article] [PubMed] [Google Scholar]
77.Murata T., Katsushima N., Mizuta K., Muraki Y., Hongo S., Matsuzaki Y. Prolonged norovirus shedding in infants <or=6 months of age with gastroenteritis. Pediatr Infect Dis J. 2007;26:46–49. doi: 10.1097/01.inf.0000247102.04997.e0. [DOI] [PubMed] [Google Scholar]
78.Green J., Wright P.A., Gallimore C.I., Mitchell O., Morgan-Capner P., Brown D.W. The role of environmental contamination with small round structured viruses in a hospital outbreak investigated by reverse-transcriptase polymerase chain reaction assay. J Hosp Infect. 1998;39:39–45. doi: 10.1016/s0195-6701(98)90241-9. [DOI] [PubMed] [Google Scholar]
79.Cheng H.-Y., Lee C.-C., Chang Y.-C., et al. Viral shedding in gastroenteritis in children caused by variants and novel recombinant norovirus infections. Medicine (Baltimore) 2021;100 doi: 10.1097/MD.0000000000025123. [DOI] [PMC free article] [PubMed] [Google Scholar]
80.Gary G.W., Kaplan J.E., Stine S.E., Anderson L.J. Detection of Norwalk virus antibodies and antigen with a biotin-avidin immunoassay. J Clin Microbiol. 1985;22:274–278. doi: 10.1128/jcm.22.2.274-278.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
81.Treanor J.J., Madore H.P., Dolin R. Development of an enzyme immunoassay for the Hawaii agent of viral gastroenteritis. J Virol Methods. 1988;22:207–214. doi: 10.1016/0166-0934(88)90103-6. [DOI] [PubMed] [Google Scholar]
82.Graham D.Y., Jiang X., Tanaka T., Opekun A.R., Madore H.P., Estes M.K. Norwalk virus infection of volunteers: new insights based on improved assays. J Infect Dis. 1994;170:34–43. doi: 10.1093/infdis/170.1.34. [DOI] [PubMed] [Google Scholar]
83.Kirby A., Dove W., Ashton L., Hopkins M., Cunliffe N.A. Detection of norovirus in mouthwash samples from patients with acute gastroenteritis. J Clin Virol. 2010;48:285–287. doi: 10.1016/j.jcv.2010.05.009. [DOI] [PubMed] [Google Scholar]
84.Greenberg H.B., Wyatt R.G., Kapikian A.Z. Norwalk virus in vomitus. Lancet Lond Engl. 1979;1:55. doi: 10.1016/s0140-6736(79)90508-7. [DOI] [PubMed] [Google Scholar]
85.Chilengi R., Simuyandi M., Chibuye M., et al. A pilot study on use of live attenuated rotavirus vaccine (RotarixTM) as an infection challenge model. Vaccine. 2020;38:7357–7362. doi: 10.1016/j.vaccine.2020.09.023. [DOI] [PubMed] [Google Scholar]
86.Freedman S.B., Xie J., Nettel-Aguirre A., et al. A randomized trial evaluating virus-specific effects of a combination probiotic in children with acute gastroenteritis. Nat Commun. 2020;11:2533. doi: 10.1038/s41467-020-16308-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
87.Yen C., Jakob K., Esona M.D., et al. Detection of fecal shedding of rotavirus vaccine in infants following their first dose of pentavalent rotavirus vaccine. Vaccine. 2011;29:4151–4155. doi: 10.1016/j.vaccine.2011.03.074. [DOI] [PMC free article] [PubMed] [Google Scholar]
88.Jacobsen S., Niendorf S., Lorenz R., Bock C.-T., Mas Marques A. Differentiation between wild-type group A rotaviruses and vaccine strains in cases of suspected horizontal transmission and adverse events following vaccination. Viruses. 2022;14 doi: 10.3390/v14081670. [DOI] [PMC free article] [PubMed] [Google Scholar]
89.Stals F., Walther F.J., Bruggeman C.A. Faecal and pharyngeal shedding of rotavirus and rotavirus IgA in children with diarrhoea. J Med Virol. 1984;14:333–339. doi: 10.1002/jmv.1890140406. [DOI] [PubMed] [Google Scholar]
90.Nordgren J., Bucardo F., Svensson L., Lindgren P.-E. Novel light-upon-extension real-time PCR assay for simultaneous detection, quantification, and genogrouping of group A rotavirus. J Clin Microbiol. 2010;48:1859–1865. doi: 10.1128/JCM.02288-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
91.Li J.-S., Cao B., Gao H.-C., et al. Faecal shedding of rotavirus vaccine in Chinese children after vaccination with lanzhou lamb rotavirus vaccine. Sci Rep. 2018;8:1001. doi: 10.1038/s41598-018-19469-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
92.Ray P., Fenaux M., Sharma S., et al. Quantitative evaluation of rotaviral antigenemia in children with acute rotaviral diarrhea. J Infect Dis. 2006;194:588–593. doi: 10.1086/505878. [DOI] [PubMed] [Google Scholar]
93.Gutierrez M.B., Fialho A.M., Maranhão A.G., et al. Rotavirus A in Brazil: molecular epidemiology and surveillance during 2018-2019. Pathog Basel Switz. 2020;9 doi: 10.3390/pathogens9070515. [DOI] [PMC free article] [PubMed] [Google Scholar]
94.Cowley D., Boniface K., Bogdanovic-Sakran N., Kirkwood C.D., Bines J.E. Rotavirus shedding following administration of RV3-BB human neonatal rotavirus vaccine. Hum Vaccines Immunother. 2017;13:1908–1915. doi: 10.1080/21645515.2017.1323591. [DOI] [PMC free article] [PubMed] [Google Scholar]
95.Chrystie I.L., Totterdell B.M., Banatvala J.E. Asymptomatic endemic rotavirus infections in the newborn. Lancet Lond Engl. 1978;1:1176–1178. doi: 10.1016/S0140-6736(78)90967-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
96.Pickering L.K., Bartlett A.V., III, Reves R.R., Morrow A. Asymptomatic excretion of rotavirus before and after rotavirus diarrhea in children in day care centers. J Pediatr. 1988;112:361–365. doi: 10.1016/s0022-3476(88)80313-5. [DOI] [PubMed] [Google Scholar]
97.Clark H.F., Dolan K.T., Horton-Slight P., Palmer J., Plotkin S.A. Diverse serologic response to rotavirus infection of infants in a single epidemic. Pediatr Infect Dis. 1985;4:626–631. doi: 10.1097/00006454-198511000-00006. [DOI] [PubMed] [Google Scholar]
98.Richardson S., Grimwood K., Gorrell R., Palombo E., Barnes G., Bishop R. Extended excretion of rotavirus after severe diarrhoea in young children. Lancet Lond Engl. 1998;351:1844–1848. doi: 10.1016/S0140-6736(97)11257-0. [DOI] [PubMed] [Google Scholar]
99.Guarino A., Canani R.B., Russo S., et al. Oral immunoglobulins for treatment of acute rotaviral gastroenteritis. Pediatrics. 1994;93:12–16. [PubMed] [Google Scholar]
100.Vesikari T., Sarkkinen H.K., Mäki M. Quantitative aspects of rotavirus excretion in childhood diarrhoea. Acta Paediatr Scand. 1981;70:717–721. doi: 10.1111/j.1651-2227.1981.tb05774.x. [DOI] [PubMed] [Google Scholar]
101.Zheng B.J., Chang R.X., Ma G.Z., et al. Rotavirus infection of the oropharynx and respiratory tract in young children. J Med Virol. 1991;34:29–37. doi: 10.1002/jmv.1890340106. [DOI] [PubMed] [Google Scholar]
102.von Bonsdorff C.H., Hovi T., Mäkelä P., Mörttinen A. Rotavirus infections in adults in association with acute gastroenteritis. J Med Virol. 1978;2:21–28. doi: 10.1002/jmv.1890020105. [DOI] [PubMed] [Google Scholar]
103.Mukhopadhya I., Sarkar R., Menon V.K., et al. Rotavirus shedding in symptomatic and asymptomatic children using reverse transcription-quantitative PCR. J Med Virol. 2013;85:1661–1668. doi: 10.1002/jmv.23641. [DOI] [PMC free article] [PubMed] [Google Scholar]
104.Chiappini E., Azzari C., Moriondo M., Galli L., de Martino M. Viraemia is a common finding in immunocompetent children with rotavirus infection. J Med Virol. 2005;76:265–267. doi: 10.1002/jmv.20351. [DOI] [PubMed] [Google Scholar]
105.Argüelles M.H., Villegas G.A., Castello A., et al. VP7 and VP4 genotyping of human group A rotavirus in Buenos Aires, Argentina. J Clin Microbiol. 2000;38:252–259. doi: 10.1128/jcm.38.1.252-259.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
106.Vesikari T., Kapikian A.Z., Delem A., Zissis G. A comparative trial of rhesus monkey (RRV-1) and bovine (RIT 4237) oral rotavirus vaccines in young children. J Infect Dis. 1986;153:832–839. doi: 10.1093/infdis/153.5.832. [DOI] [PubMed] [Google Scholar]
107.Dang D.A., Nguyen V.T., Vu D.T., et al. A dose-escalation safety and immunogenicity study of a new live attenuated human rotavirus vaccine (Rotavin-M1) in Vietnamese children. Vaccine. 2012;30(Suppl 1):A114–A121. doi: 10.1016/j.vaccine.2011.07.118. [DOI] [PubMed] [Google Scholar]
108.Phua K.B., Quak S.H., Lee B.W., et al. Evaluation of RIX4414, a live, attenuated rotavirus vaccine, in a randomized, double-blind, placebo-controlled phase 2 trial involving 2464 Singaporean infants. J Infect Dis. 2005;192(Suppl 1):S6–S16. doi: 10.1086/431511. [DOI] [PubMed] [Google Scholar]
109.Rivera L., Peña L.M., Stainier I., et al. Horizontal transmission of a human rotavirus vaccine strain--a randomized, placebo-controlled study in twins. Vaccine. 2011;29:9508–9513. doi: 10.1016/j.vaccine.2011.10.015. [DOI] [PubMed] [Google Scholar]
110.Ward R.L., Bernstein D.I., Young E.C., Sherwood J.R., Knowlton D.R., Schiff G.M. Human rotavirus studies in volunteers: determination of infectious dose and serological response to infection. J Infect Dis. 1986;154:871–880. doi: 10.1093/infdis/154.5.871. [DOI] [PubMed] [Google Scholar]
111.Donato C.M., Ch’ng L.S., Boniface K.F., et al. Identification of strains of RotaTeq rotavirus vaccine in infants with gastroenteritis following routine vaccination. J Infect Dis. 2012;206:377–383. doi: 10.1093/infdis/jis361. [DOI] [PubMed] [Google Scholar]
112.Bennett A., Pollock L., Jere K.C., et al. Infrequent transmission of monovalent human rotavirus vaccine virus to household contacts of vaccinated infants in Malawi. J Infect Dis. 2019;219:1730–1734. doi: 10.1093/infdis/jiz002. [DOI] [PMC free article] [PubMed] [Google Scholar]
113.Magwira C.A., Kgosana L.P., Esona M.D., Seheri M.L. Low fecal rotavirus vaccine virus shedding is significantly associated with non-secretor histo-blood group antigen phenotype among infants in northern Pretoria, South Africa. Vaccine. 2020;38:8260–8263. doi: 10.1016/j.vaccine.2020.11.025. [DOI] [PubMed] [Google Scholar]
114.Flores J., Daoud G., Daoud N., et al. Reactogenicity and antigenicity of rhesus rotavirus vaccine (MMU-18006) in newborn infants in Venezuela. Pediatr Infect Dis J. 1988;7:776–780. doi: 10.1097/00006454-198811000-00006. [DOI] [PubMed] [Google Scholar]
115.Cantelli C.P., Velloso A.J., de Assis R.M.S., et al. Rotavirus A shedding and HBGA host genetic susceptibility in a birth community-cohort, Rio de Janeiro, Brazil, 2014-2018. Sci Rep. 2020;10:6965. doi: 10.1038/s41598-020-64025-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
116.Smith C.K., McNeal M.M., Meyer N.R., Haase S., Dekker C.L. Rotavirus shedding in premature infants following first immunization. Vaccine. 2011;29:8141–8146. doi: 10.1016/j.vaccine.2011.08.028. [DOI] [PubMed] [Google Scholar]
117.Hiramatsu H., Suzuki R., Nagatani A., et al. Rotavirus vaccination can be performed without viral dissemination in the neonatal intensive care unit. J Infect Dis. 2018;217:589–596. doi: 10.1093/infdis/jix590. [DOI] [PubMed] [Google Scholar]
118.Miura H., Kawamura Y., Sugata K., et al. Rotavirus vaccine strain transmission by vaccinated infants in the foster home. J Med Virol. 2017;89:79–84. doi: 10.1002/jmv.24613. [DOI] [PubMed] [Google Scholar]
119.Mijatovic-Rustempasic S., Immergluck L.C., Parker T.C., et al. Shedding of porcine circovirus type 1 DNA and rotavirus RNA by infants vaccinated with rotarix®. Hum Vaccines Immunother. 2017;13:928–935. doi: 10.1080/21645515.2016.1255388. [DOI] [PMC free article] [PubMed] [Google Scholar]
120.Anderson E.L., Belshe R.B., Bartram J., Crookshanks-Newman F., Chanock R.M., Kapikian A.Z. Evaluation of rhesus rotavirus vaccine (MMU 18006) in infants and young children. J Infect Dis. 1986;153:823–831. doi: 10.1093/infdis/153.5.823. [DOI] [PubMed] [Google Scholar]
121.Tort L.F.L., Victoria M., Lizasoain A.A., et al. Molecular epidemiology of group A rotavirus among children admitted to hospital in Salto, Uruguay, 2011-2012: first detection of the emerging genotype G12. J Med Virol. 2015;87:754–763. doi: 10.1002/jmv.24123. [DOI] [PubMed] [Google Scholar]
122.Cotterill H., Curry A., Riordan T. Rotavirus in vomit. J Infect. 1988;16:206–207. doi: 10.1016/s0163-4453(88)94297-1. [DOI] [PubMed] [Google Scholar]
123.Borade A., Bais A.S., Bapat V., Dhongade R. Characteristics of rotavirus gastroenteritis in hospitalized children in Pune. Indian J Med Sci. 2010;64:210–218. [PubMed] [Google Scholar]
124.Yokoyama T., Sugimoto N., Taniguchi K., et al. Molecular and immunohistochemical detection of rotavirus in urinary sediment cells of children with rotavirus gastroenteritis. Clin Microbiol Infect. 2011;17:1190–1193. doi: 10.1111/j.1469-0691.2011.03522.x. [DOI] [PubMed] [Google Scholar]
125.Santosham M., Yolken R.H., Quiroz E., et al. Detection of rotavirus in respiratory secretions of children with pneumonia. J Pediatr. 1983;103:583–585. doi: 10.1016/s0022-3476(83)80591-5. [DOI] [PubMed] [Google Scholar]
126.Satter S.M., Katz E., Hossain M.E., et al. Detection of rotavirus in respiratory specimens from Bangladeshi children aged <2 years hospitalized for acute gastroenteritis. J Infect Dis. 2024;229:457–461. doi: 10.1093/infdis/jiad333. [DOI] [PubMed] [Google Scholar]
127.Martin Perceval L., Scherdel P., Jarry B., de Visme S., Levieux K., Gras-Le Guen C. Sudden unexpected death in infancy: current practices in virological investigations and documentation in the French registry. J Pediatr. 2023;257 doi: 10.1016/j.jpeds.2023.01.003. [DOI] [PubMed] [Google Scholar]
128.Kiyohara T., Ouchi Y., Hasegawa Y., et al. An in-house-anti-hepatitis A virus (HAV)-specific immunoglobulin M capture enzyme-linked immunosorbent assay: evaluation and application to an HAV outbreak. J Med Virol. 2009;81:1513–1516. doi: 10.1002/jmv.21578. [DOI] [PubMed] [Google Scholar]
129.Tjon G.M.S., Coutinho R.A., van den Hoek A., et al. High and persistent excretion of hepatitis A virus in immunocompetent patients. J Med Virol. 2006;78:1398–1405. doi: 10.1002/jmv.20711. [DOI] [PubMed] [Google Scholar]
130.Arankalle V.A., Sarada Devi K.L., Lole K.S., Shenoy K.T., Verma V., Haneephabi M. Molecular characterization of hepatitis A virus from a large outbreak from Kerala, India. Indian J Med Res. 2006;123:760–769. [PubMed] [Google Scholar]
131.Hundekar S., Thorat N., Gurav Y., Lole K. Viral excretion and antibody titers in children infected with hepatitis A virus from an orphanage in Western India. J Clin Virol. 2015;73:27–31. doi: 10.1016/j.jcv.2015.10.012. [DOI] [PubMed] [Google Scholar]
132.Costafreda M.I., Bosch A., Pintó R.M. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Appl Environ Microbiol. 2006;72:3846–3855. doi: 10.1128/AEM.02660-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
133.Kamel A.H., Ali M.A., El-Nady H.G., et al. Presence of enteric hepatitis viruses in the sewage and population of Greater Cairo. Clin Microbiol Infect. 2011;17:1182–1185. doi: 10.1111/j.1469-0691.2011.03461.x. [DOI] [PubMed] [Google Scholar]
134.Amado L.A., Villar L.M., de Paula V.S., Gaspar A.M.C. Comparison between serum and saliva for the detection of hepatitis A virus RNA. J Virol Methods. 2008;148:74–80. doi: 10.1016/j.jviromet.2007.10.020. [DOI] [PubMed] [Google Scholar]
135.Mackiewicz V., Dussaix E., Petitcorps M.-F.L., Roque-Afonso A.M. Detection of Hepatitis A virus RNA in saliva. J Clin Microbiol. 2004;42:4329. doi: 10.1128/JCM.42.9.4329-4331.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
136.Amado L.A., Villar L.M., de Paula V.S., Pinto M.A., Gaspar A.M.C. Exposure to multiple subgenotypes of hepatitis A virus during an outbreak using matched serum and saliva specimens. J Med Virol. 2011;83:768–775. doi: 10.1002/jmv.22045. [DOI] [PubMed] [Google Scholar]
137.Amado Leon L.A., de Almeida A.J., de Paula V.S., et al. Longitudinal study of hepatitis A infection by saliva sampling: the kinetics of HAV markers in saliva revealed the application of saliva tests for hepatitis A study. PLoS One. 2015;10 doi: 10.1371/journal.pone.0145454. [DOI] [PMC free article] [PubMed] [Google Scholar]
138.Locarnini S.A., Gust I.D., Ferris A.A., Stott A.C., Wong M.L. A prospective study of acute viral hepatitis with particular reference to hepatitis A. Bull World Health Organ. 1976;54:199. [PMC free article] [PubMed] [Google Scholar]
139.Chitambar S.D., Fadnis R.S., Joshi M.S., Habbu A., Bhatia S.G. Case report: hepatitis A preceding Guillain-Barré syndrome. J Med Virol. 2006;78:1011–1014. doi: 10.1002/jmv.20656. [DOI] [PubMed] [Google Scholar]
140.Coulepis A.G., Locarnini S.A., Lehmann N.I., Gust I.D. Detection of hepatitis A virus in the feces of patients with naturally acquired infections. J Infect Dis. 1980;141:151–156. doi: 10.1093/infdis/141.2.151. [DOI] [PubMed] [Google Scholar]
141.Coutinho R.A., Duermeyer W., van der Veen J. Epidemiology of hepatitis A in Amsterdam, October 1978--December 1979. J Virol Methods. 1980;2:47–55. doi: 10.1016/0166-0934(80)90038-5. [DOI] [PubMed] [Google Scholar]
142.Tassopoulos N.C., Papaevangelou G.J., Ticehurst J.R., Purcell R.H. Fecal excretion of Greek strains of hepatitis A virus in patients with hepatitis A and in experimentally infected chimpanzees. J Infect Dis. 1986;154:231–237. doi: 10.1093/infdis/154.2.231. [DOI] [PubMed] [Google Scholar]
143.Coursaget P., Maupas P., Hibon P., Lesage G., Hubert M. Hepatitis A diagnosis in man: radioimmunoassay for hepatitis A antigen detection in faeces. J Med Virol. 1980;6:53–60. doi: 10.1002/jmv.1890060108. [DOI] [PubMed] [Google Scholar]
144.Normann A., Pfisterer-Hunt M., Schade S., et al. Molecular epidemiology of an outbreak of hepatitis A in Italy. J Med Virol. 1995;47:467–471. doi: 10.1002/jmv.1890470429. [DOI] [PubMed] [Google Scholar]
145.Bruisten S.M., van Steenbergen J.E., Pijl A.S., Niesters H.G., van Doornum G.J., Coutinho R.A. Molecular epidemiology of hepatitis A virus in Amsterdam, the Netherlands. J Med Virol. 2001;63:88–95. [PubMed] [Google Scholar]
146.Selander B., Bläckberg J., Widell A., Johansson P.J.H. No evidence of intrauterine transmission of hepatitis A virus from a mother to a premature infant. Acta Paediatr Oslo Nor. 1992 2009;98:1603–1606. doi: 10.1111/j.1651-2227.2009.01402.x. [DOI] [PubMed] [Google Scholar]
147.Yotsuyanagi H., Koike K., Yasuda K., et al. Prolonged fecal excretion of hepatitis A virus in adult patients with hepatitis A as determined by polymerase chain reaction. Hepatology. 1996;24:10–13. doi: 10.1053/jhep.1996.v24.pm0008707246. [DOI] [PubMed] [Google Scholar]
148.Frösner G.G., Overby L.R., Flehmig B., et al. Seroepidemiological investigation of patients and family contacts in an epidemic of hepatitis A. J Med Virol. 1977;1:163–173. doi: 10.1002/jmv.1890010303. [DOI] [PubMed] [Google Scholar]
149.Dienstag J.L., Feinstone S.M., Kapikian A.Z., Purcell R.H. Faecal shedding of hepatitis-A antigen. Lancet. 1975;1:765–767. doi: 10.1016/s0140-6736(75)92434-4. [DOI] [PubMed] [Google Scholar]
150.Ma F., Yang J., Kang G., et al. Comparison of the safety and immunogenicity of live attenuated and inactivated hepatitis A vaccine in healthy Chinese children aged 18 months to 16 years: results from a randomized, parallel controlled, phase IV study. Clin Microbiol Infect. 2016;22:811.e9–811.e15. doi: 10.1016/j.cmi.2016.06.004. [DOI] [PubMed] [Google Scholar]
151.Wang X., Pan Y., Chen J., et al. The excretion rate and stability of HAAg in human fecal samples after live attenuated hepatitis A vaccination. J Med Virol. 2020;92:3312–3318. doi: 10.1002/jmv.25747. [DOI] [PubMed] [Google Scholar]
152.Stapleton J.T., Lange D.K., LeDuc J.W., Binn L.N., Jansen R.W., Lemon S.M. The role of secretory immunity in hepatitis A virus infection. J Infect Dis. 1991;163:7–11. doi: 10.1093/infdis/163.1.7. [DOI] [PubMed] [Google Scholar]
153.Joshi M.S., Bhalla S., Kalrao V.R., Dhongade R.K., Chitambar S.D. Exploring the concurrent presence of hepatitis A virus genome in serum, stool, saliva, and urine samples of hepatitis A patients. Diagn Microbiol Infect Dis. 2014;78:379–382. doi: 10.1016/j.diagmicrobio.2013.12.013. [DOI] [PubMed] [Google Scholar]
154.Portes S.A.R., Volotão E.D.M., Rocha M.S., et al. A non-enteric adenovirus A12 gastroenteritis outbreak in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 2016;111:403–406. doi: 10.1590/0074-02760160030. [DOI] [PMC free article] [PubMed] [Google Scholar]
155.do Nascimento L.G., Fialho A.M., de Andrade J.D.S.R., de Assis R.M.S., Fumian T.M. Human enteric adenovirus F40/41 as a major cause of acute gastroenteritis in children in Brazil, 2018 to 2020. Sci Rep. 2022;12 doi: 10.1038/s41598-022-15413-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
156.Allayeh A.K., Al-Daim S.A., Ahmed N., El-Gayar M., Mostafa A. Isolation and genotyping of adenoviruses from wastewater and diarrheal samples in Egypt from 2016 to 2020. Viruses. 2022;14 doi: 10.3390/v14102192. [DOI] [PMC free article] [PubMed] [Google Scholar]
157.Elmahdy E.M., Ahmed N.I., Shaheen M.N.F., Mohamed E.-C.B., Loutfy S.A. Molecular detection of human adenovirus in urban wastewater in Egypt and among children suffering from acute gastroenteritis. J Water Health. 2019;17:287–294. doi: 10.2166/wh.2019.303. [DOI] [PubMed] [Google Scholar]
158.Zhuo R., Parsons B.D., Lee B.E., et al. Identification of enteric viruses in oral swabs from children with acute gastroenteritis. J Mol Diagn. 2018;20:56–62. doi: 10.1016/j.jmoldx.2017.09.003. [DOI] [PubMed] [Google Scholar]
159.Fall A., Campodónico V.L., Howard C., et al. Dissemination and genome characterization of a human adenovirus F41 in a patient with B-Cell lymphoma. Virol J. 2023;20:141. doi: 10.1186/s12985-023-02101-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
160.McFarlane E.S., Goldbloom A.L., Embil J.A. Prolonged excretion of an identical cytomegalovirus strain by two siblings and the intermittent isolation of an adenovirus from the urine of one of them. J Med Virol. 1987;23:283–287. doi: 10.1002/jmv.1890230311. [DOI] [PubMed] [Google Scholar]
161.Chen W., Bibby K. A model-based framework to assess the feasibility of monitoring zika virus with wastewater-based epidemiology. ACS EST Water. 2023;3:1071–1081. [Google Scholar]
162.Lowry S.A., Wolfe M.K., Boehm A.B. Respiratory virus concentrations in human excretions that contribute to wastewater: a systematic review and meta-analysis. J Water Health. 2023;21:831–848. doi: 10.2166/wh.2023.057. [DOI] [PubMed] [Google Scholar]
163.Schoen M.E., Bidwell A.L., Wolfe M.K., Boehm A.B. United States influenza 2022–2023 season characteristics as inferred from wastewater solids, influenza hospitalization, and syndromic data. Environ Sci Technol. 2023;57:20542–20550. doi: 10.1021/acs.est.3c07526. [DOI] [PMC free article] [PubMed] [Google Scholar]
164.Lee R.M., Lessler J., Lee R.A., et al. Incubation periods of viral gastroenteritis: a systematic review. BMC Infect Dis. 2013;13:446. doi: 10.1186/1471-2334-13-446. [DOI] [PMC free article] [PubMed] [Google Scholar]
165.CDC . Epidemiology and Prevention of Vaccine-Preventable Diseases. 2024. Chapter 19: rotavirus.https://www.cdc.gov/pinkbook/hcp/table-of-contents/chapter-19-rotavirus.html published online Sept 30. [Google Scholar]
166.Health D of P. California department of public health. https://www.cdph.ca.gov/Programs/CID/DCDC
167.CDC . Epidemiology and Prevention of Vaccine-Preventable Diseases. 2024. Chapter 9: hepatitis A.https://www.cdc.gov/pinkbook/hcp/table-of-contents/chapter-9-hepatitis-a.html published online Sept 30. [Google Scholar]
168.Huisman J.S., Scire J., Caduff L., et al. Wastewater-based estimation of the effective reproductive number of SARS-CoV-2. Environ Health Perspect. 2022;130 doi: 10.1289/EHP10050. [DOI] [PMC free article] [PubMed] [Google Scholar]
169.Nourbakhsh S., Fazil A., Li M., et al. A wastewater-based epidemic model for SARS-CoV-2 with application to three Canadian cities. Epidemics. 2022;39 doi: 10.1016/j.epidem.2022.100560. [DOI] [PMC free article] [PubMed] [Google Scholar]
170.Mohring J., Leithäuser N., Wlazło J., et al. Estimating the COVID-19 prevalence from wastewater. Sci Rep. 2024;14 doi: 10.1038/s41598-024-64864-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
171.McManus O., Christiansen L.E., Nauta M., et al. Predicting COVID-19 incidence using wastewater surveillance data, Denmark, October 2021–June 2022. Emerg Infect Dis. 2023;29 doi: 10.3201/eid2908.221634. [DOI] [PMC free article] [PubMed] [Google Scholar]
172.Staff G.B. Global Biodefense. 2020. Sewage surveillance: watching wastewater for SARS-CoV-2.https://globalbiodefense.com/2020/08/31/sewage-surveillance-watching-wastewater-for-sars-cov-2/ published online Aug 31. [Google Scholar]
173.Chan E.M.G., Bidwell A., Li Z., Tilmans S., Boehm A.B. Public health policy impact evaluation: a potential use case for longitudinal monitoring of viruses in wastewater at small geographic scales. PLoS Water. 2024;3 [Google Scholar]
174.Haas C.N., Rose J.B., Gerba C.P. 2nd ed. Wiley; Hoboken: 2014. Quantitative microbial risk assessment. [DOI] [Google Scholar]
175.Carducci A., Donzelli G., Cioni L., Federigi I., Lombardi R., Verani M. Quantitative microbial risk assessment for workers exposed to bioaerosol in wastewater treatment plants aimed at the choice and setup of safety measures. Int J Environ Res Public Health. 2018;15:1490. doi: 10.3390/ijerph15071490. [DOI] [PMC free article] [PubMed] [Google Scholar]
176.Bustin S.A., Benes V., Garson J.A., et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55:611–622. doi: 10.1373/clinchem.2008.112797. [DOI] [PubMed] [Google Scholar]
177.Borchardt M.A., Boehm A.B., Salit M.L., Spencer S.K., Wigginton K.R., Noble R.T. The environmental microbiology minimum information (EMMI) guidelines: qPCR and dPCR quality and reporting for environmental microbiology. Environ Sci Technol. 2021;55:10210–10223. doi: 10.1021/acs.est.1c01767. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Figs. S1–S3 and Tables S1–S9

mmc1.pdf^{(639.1KB, pdf)}

[bib1] 1.WHO Diarrhoeal disease. https://www.who.int/news-room/fact-sheets/detail/diarrhoeal-disease

[bib2] 2.Greening G.E., Cannon J.L. In: Viruses in foods. Goyal S.M., Cannon J.L., editors. Springer International Publishing; Cham: 2016. Human and animal viruses in food (including taxonomy of enteric viruses) pp. 5–57. [Google Scholar]

[bib3] 3.WHO Hepatitis A. https://www.who.int/news-room/fact-sheets/detail/hepatitis-a

[bib4] 4.Thielman N.M., Guerrant R.L. Acute infectious diarrhea. N Engl J Med. 2004;350:38–47. doi: 10.1056/NEJMcp031534. [DOI] [PubMed] [Google Scholar]

[bib5] 5.Kazama S., Miura T., Masago Y., et al. Environmental surveillance of norovirus genogroups I and II for sensitive detection of epidemic variants. Appl Environ Microbiol. 2017;83:e03406–e03416. doi: 10.1128/AEM.03406-16. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib6] 6.Wang H., Churqui M.P., Tunovic T., et al. Measures against COVID-19 affected the spread of human enteric viruses in a Swedish community, as found when monitoring wastewater. Sci Total Environ. 2023;895 doi: 10.1016/j.scitotenv.2023.165012. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib7] 7.Boehm A.B., Wolfe M.K., White B.J., et al. Human norovirus (HuNoV) GII RNA in wastewater solids at 145 United States wastewater treatment plants: comparison to positivity rates of clinical specimens and modeled estimates of HuNoV GII shedders. J Expo Sci Environ Epidemiol. 2024;34:440–447. doi: 10.1038/s41370-023-00592-4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib8] 8.Silverman A.I., Boehm A.B. Systematic review and meta-analysis of the persistence of enveloped viruses in environmental waters and wastewater in the absence of disinfectants. Environ Sci Technol. 2021;55:14480–14493. doi: 10.1021/acs.est.1c03977. [DOI] [PubMed] [Google Scholar]

[bib9] 9.Soller J., Jennings W., Schoen M., et al. Modeling infection from SARS-CoV-2 wastewater concentrations: promise, limitations, and future directions. J Water Health. 2022;20:1197–1211. doi: 10.2166/wh.2022.094. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib10] 10.Wu F., Xiao A., Zhang J., et al. SARS-CoV-2 titers in wastewater foreshadow dynamics and clinical presentation of new COVID-19 cases. medRxiv. 2020 doi: 10.1101/2020.06.15.20117747. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib11] 11.Zhu Y., Oishi W., Maruo C., et al. Early warning of COVID-19 via wastewater-based epidemiology: potential and bottlenecks. Sci Total Environ. 2021;767 doi: 10.1016/j.scitotenv.2021.145124. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib12] 12.Phan T., Brozak S., Pell B., et al. Making waves: integrating wastewater surveillance with dynamic modeling to track and predict viral outbreaks. Water Res. 2023;243 doi: 10.1016/j.watres.2023.120372. [DOI] [PubMed] [Google Scholar]

[bib13] 13.Yu A.T., Burnor E., Rabe A., et al. Wastewater surveillance for norovirus, California, USA. Emerg Infect Dis. 2024;30:2438. doi: 10.3201/eid3011.241001. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib14] 14.Fantilli A., Cola G.D., Castro G., et al. Hepatitis A virus monitoring in wastewater: a complementary tool to clinical surveillance. Water Res. 2023;241 doi: 10.1016/j.watres.2023.120102. [DOI] [PubMed] [Google Scholar]

[bib15] 15.Boehm A.B., Shelden B., Duong D., Banaei N., White B.J., Wolfe M.K. A retrospective longitudinal study of adenovirus group F, norovirus GI and GII, rotavirus, and enterovirus nucleic acids in wastewater solids at two wastewater treatment plants: solid-liquid partitioning and relation to clinical testing data. mSphere. 2024;9 doi: 10.1128/msphere.00736-23. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib16] 16.Crank K., Chen W., Bivins A., Lowry S., Bibby K. Contribution of SARS-CoV-2 RNA shedding routes to RNA loads in wastewater. Sci Total Environ. 2022;806 doi: 10.1016/j.scitotenv.2021.150376. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib17] 17.Ghosh S., Kumar M., Santiana M., et al. Enteric viruses replicate in salivary glands and infect through saliva. Nature. 2022;607:345–350. doi: 10.1038/s41586-022-04895-8. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib18] 18.Zheng G., Boehm AB. Systematic review and meta-analysis of enteric virus shedding in human excretions. OSF; 2024. http://osf.io/ecb8f [DOI] [PubMed] [Google Scholar]

[bib19] 19.Page M.J., McKenzie J.E., Bossuyt P.M., et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372 doi: 10.1136/bmj.n71. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib20] 20.Lai C.-C., Wang Y.-H., Wu C.-Y., Hung C.-H., Jiang D.D.-S., Wu F.-T. A norovirus outbreak in a nursing home: norovirus shedding time associated with age. J Clin Virol. 2013;56:96–101. doi: 10.1016/j.jcv.2012.10.011. [DOI] [PubMed] [Google Scholar]

[bib21] 21.Coudray-Meunier C., Fraisse A., Martin-Latil S., Delannoy S., Fach P., Perelle S. A novel high-throughput method for molecular detection of human pathogenic viruses using a nanofluidic real-time PCR system. PLoS One. 2016;11 doi: 10.1371/journal.pone.0147832. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib22] 22.Bucardo F., Nordgren J., Carlsson B., et al. Asymptomatic norovirus infections in Nicaraguan children and its association with viral properties and histo-Blood group antigens. Pediatr Infect Dis J. 2010;29:934. doi: 10.1097/INF.0b013e3181ed9f2f. [DOI] [PubMed] [Google Scholar]

[bib23] 23.Takanashi S., Wang Q., Chen N., et al. Characterization of emerging GII.g/GII.12 noroviruses from a gastroenteritis outbreak in the United States in 2010. J Clin Microbiol. 2020;49:3234–3244. doi: 10.1128/JCM.00305-11. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib24] 24.Lee C.-C., Chiu C.-H., Lee H.-Y., Tsai C.-N., Chen C.-L., Chen S.-Y. Clinical and virological characteristics of viral shedding in children with norovirus gastroenteritis. J Microbiol Immunol Infect. 2022;55:1188–1194. doi: 10.1016/j.jmii.2021.10.006. [DOI] [PubMed] [Google Scholar]

[bib25] 25.Shigemoto N., Tanizawa Y., Matsuo T., et al. Clinical evaluation of a bioluminescent enzyme immunoassay for detecting norovirus in fecal specimens from patients with acute gastroenteritis. J Med Virol. 2014;86:1219–1225. doi: 10.1002/jmv.23765. [DOI] [PubMed] [Google Scholar]

[bib26] 26.Höhne M., Schreier E. Detection and characterization of norovirus outbreaks in Germany: application of a one-tube RT-PCR using a fluorogenic real-time detection system. J Med Virol. 2004;72:312–319. doi: 10.1002/jmv.10573. [DOI] [PubMed] [Google Scholar]

[bib27] 27.Scipioni A., Bourgot I., Mauroy A., et al. Detection and quantification of human and bovine noroviruses by a TaqMan RT-PCR assay with a control for inhibition. Mol Cell Probes. 2008;22:215–222. doi: 10.1016/j.mcp.2008.02.003. [DOI] [PubMed] [Google Scholar]

[bib28] 28.Nishimura N., Nakayama H., Yoshizumi S., et al. Detection of noroviruses in fecal specimens by direct RT-PCR without RNA purification. J Virol Methods. 2010;163:282–286. doi: 10.1016/j.jviromet.2009.10.011. [DOI] [PubMed] [Google Scholar]

[bib29] 29.Kirby A.e., Shi J., Montes J., Lichtenstein M., Moe C l. Disease course and viral shedding in experimental Norwalk virus and snow Mountain virus infection. J Med Virol. 2014;86:2055–2064. doi: 10.1002/jmv.23905. [DOI] [PubMed] [Google Scholar]

[bib30] 30.Aoki Y., Suto A., Mizuta K., Ahiko T., Osaka K., Matsuzaki Y. Duration of norovirus excretion and the longitudinal course of viral load in norovirus-infected elderly patients. J Hosp Infect. 2010;75:42–46. doi: 10.1016/j.jhin.2009.12.016. [DOI] [PubMed] [Google Scholar]

[bib31] 31.Costantini V.P., Cooper E.M., Hardaker H.L., et al. Epidemiologic, virologic, and host genetic factors of norovirus outbreaks in long-term care facilities. Clin Infect Dis Off Publ Infect Dis Soc Am. 2015;62:1. doi: 10.1093/cid/civ747. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib32] 32.Pang X., Lee B., Chui L., Preiksaitis J.K., Monroe S.S. Evaluation and validation of real-time reverse transcription-pcr assay using the LightCycler system for detection and quantitation of norovirus. J Clin Microbiol. 2004;42:4679–4685. doi: 10.1128/JCM.42.10.4679-4685.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib33] 33.Théry L., Bidalot M., Pothier P., Ambert-Balay K. Evaluation of immunochromatographic tests for the rapid detection of the emerging GII.17 norovirus in stool samples, January 2016. Eurosurveillance. 2016;21 doi: 10.2807/1560-7917.ES.2016.21.4.30115. [DOI] [PubMed] [Google Scholar]

[bib34] 34.Pratte-Santos R., Miagostovich M.P., Fumian T.M., et al. High prevalence of enteric viruses associated with acute gastroenteritis in pediatric patients in a low-income area in vitória, Southeastern Brazil. J Med Virol. 2019;91:744–750. doi: 10.1002/jmv.25392. [DOI] [PubMed] [Google Scholar]

[bib35] 35.Miyoshi T., Uchino K., Yoshida H., et al. Long-term viral shedding and viral genome mutation in norovirus infection. J Med Virol. 2015;87:1872–1880. doi: 10.1002/jmv.24242. [DOI] [PubMed] [Google Scholar]

[bib36] 36.Kumthip K., Khamrin P., Ushijima H., Maneekarn N. Molecular detection and characterization of norovirus in asymptomatic food handlers in Chiang Mai, Thailand. Infect Genet Evol. 2021;89 doi: 10.1016/j.meegid.2021.104725. [DOI] [PubMed] [Google Scholar]

[bib37] 37.Henke-Gendo C., Harste G., Juergens-Saathoff B., Mattner F., Deppe H., Heim A. New real-time PCR detects prolonged norovirus excretion in highly immunosuppressed patients and children. J Clin Microbiol. 2009;47:2855–2862. doi: 10.1128/JCM.00448-09. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib38] 38.Tu E.T.-V., Bull R.A., Kim M.-J., et al. Norovirus excretion in an aged-care setting. J Clin Microbiol. 2008;46:2119. doi: 10.1128/JCM.02198-07. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib39] 39.Rajko-Nenow P., Keaveney S., Flannery J., McIntyre A., Doré W. Norovirus genotypes implicated in two oyster-related illness outbreaks in Ireland. Epidemiol Infect. 2013;142:2096. doi: 10.1017/S0950268813003014. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib40] 40.Dábilla N., Nunes Vieira Almeida T., Carvalho Rebouças Oliveira A., et al. Norovirus in feces and nasopharyngeal swab of children with and without acute gastroenteritis symptoms: first report of GI.5 in Brazil and GI.3 in nasopharyngeal swab. J Clin Virol Off Publ Pan Am Soc Clin Virol. 2017;87:60–66. doi: 10.1016/j.jcv.2016.12.009. [DOI] [PubMed] [Google Scholar]

[bib41] 41.Munir N., Liu P., Gastañaduy P., Montes J., Shane A., Moe C. Norovirus infection in immunocompromised children and children with hospital-acquired acute gastroenteritis. J Med Virol. 2014;86:1203–1209. doi: 10.1002/jmv.23774. [DOI] [PubMed] [Google Scholar]

[bib42] 42.Ozawa K., Oka T., Takeda N., Hansman G.S. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J Clin Microbiol. 2007;45:3996–4005. doi: 10.1128/JCM.01516-07. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib43] 43.Reymão T.K.A., Fumian T.M., Justino M.C.A., et al. Norovirus RNA in serum associated with increased fecal viral load in children: detection, quantification and molecular analysis. PLoS One. 2018;13 doi: 10.1371/journal.pone.0199763. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib44] 44.Atmar R.L., Opekun A.R., Gilger M.A., et al. Norwalk virus shedding after experimental human infection. Emerg Infect Dis. 2008;14(10):1553–1557. doi: 10.3201/eid1410.080117. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib45] 45.Gutierrez M.B., de Figueiredo M.R., Fialho A.M., Cantelli C.P., Miagostovich M.P., Fumian T.M. Nosocomial acute gastroenteritis outbreak caused by an equine-like G3P[8] DS-1-like rotavirus and GII.4 Sydney[P16] norovirus at a pediatric hospital in Rio de Janeiro, Brazil, 2019. Hum Vaccines Immunother. 2021;17:4654–4660. doi: 10.1080/21645515.2021.1963169. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib46] 46.La Rosa G., Pourshaban M., Iaconelli M., Muscillo M. Quantification of norovirus genogroups I and II in environmental and clinical samples using TaqMan real-time RT-PCR. Food Environ Virol. 2009;1:15–22. [Google Scholar]

[bib47] 47.Fumian T.M., Justino M.C.A., Mascarenhas J.D.P., et al. Quantitative and molecular analysis of noroviruses RNA in blood from children hospitalized for acute gastroenteritis in Belém, Brazil. J Clin Virol. 2013;58:31–35. doi: 10.1016/j.jcv.2013.06.043. [DOI] [PubMed] [Google Scholar]

[bib48] 48.Teunis P.F.M., Sukhrie F.H.A., Vennema H., Bogerman J., Beersma M.F.C., Koopmans M.P.G. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol Infect. 2015;143:1710–1717. doi: 10.1017/S095026881400274X. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib49] 49.Qiu Y., Freedman S.B., Williamson-Urquhart S., et al. Significantly longer shedding of norovirus compared to rotavirus and adenovirus in children with acute gastroenteritis. Viruses. 2023;15 doi: 10.3390/v15071541. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib50] 50.Obara M., Hasegawa S., Iwai M., et al. Single base substitutions in the capsid region of the norovirus genome during viral shedding in cases of infection in areas where norovirus infection is endemic. J Clin Microbiol. 2008;46:3397–3403. doi: 10.1128/JCM.01932-07. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib51] 51.Fioretti J.M., Fumian T.M., Rocha M.S., et al. Surveillance of Noroviruses in Rio De Janeiro, Brazil: occurrence of New GIV Genotype in Clinical and Wastewater Samples. Food Environ Virol. 2018;10:1–6. doi: 10.1007/s12560-017-9308-2. [DOI] [PubMed] [Google Scholar]

[bib52] 52.Miyoshi M., Yoshizumi S., Ishida S., et al. Usefulness of the rapid determination system of viral genome sequences in human stool specimens. J Virol Methods. 2012;179:256–260. doi: 10.1016/j.jviromet.2011.11.013. [DOI] [PubMed] [Google Scholar]

[bib53] 53.Sarmento S.K., de Andrade J.D.S.R., Miagostovich M.P., Fumian T.M. Virological and epidemiological features of norovirus infections in Brazil, 2017–2018. Viruses. 2021;13 doi: 10.3390/v13091724. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib54] 54.Kirby A.E., Streby A., Moe C.L. Vomiting as a symptom and transmission risk in norovirus illness: evidence from human challenge studies. PLoS One. 2016;11 doi: 10.1371/journal.pone.0143759. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib55] 55.Fumian T.M., Leite J.P.G., Rocha M.S., et al. Performance of a one-step quantitative duplex RT-PCR for detection of rotavirus A and noroviruses GII during two periods of high viral circulation. J Virol Methods. 2016;228:123–129. doi: 10.1016/j.jviromet.2015.11.008. [DOI] [PubMed] [Google Scholar]

[bib56] 56.Ushijima H., Thongprachum A., Khamrin P., et al. Evaluation of immunochromatographic tests and a new enzyme immunoassay for detection of a novel GII.17 norovirus in stool samples. Jpn J Infect Dis. 2017;70:326–328. doi: 10.7883/yoken.JJID.2016.413. [DOI] [PubMed] [Google Scholar]

[bib57] 57.Huynen P., Mauroy A., Martin C., et al. Molecular epidemiology of norovirus infections in symptomatic and asymptomatic children from bobo dioulasso, Burkina Faso. J Clin Virol. 2013;58:515–521. doi: 10.1016/j.jcv.2013.08.013. [DOI] [PubMed] [Google Scholar]

[bib58] 58.González G.G., Liprandi F., Ludert J.E. Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol. 2011;83:1972–1982. doi: 10.1002/jmv.22185. [DOI] [PubMed] [Google Scholar]

[bib59] 59.Pombubpa K., Kittigul L. Assessment of a rapid immunochromatographic test for the diagnosis of norovirus gastroenteritis. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2012;31:2379–2383. doi: 10.1007/s10096-012-1579-9. [DOI] [PubMed] [Google Scholar]

[bib60] 60.Sakamaki N., Ohiro Y., Ito M., et al. Bioluminescent enzyme immunoassay for the detection of norovirus capsid antigen. Clin Vaccine Immunol. 2012;19:1949–1954. doi: 10.1128/CVI.00427-12. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib61] 61.Atmar R.L., Opekun A.R., Gilger M.A., et al. Determination of the 50% human infectious dose for norwalk virus. J Infect Dis. 2014;209:1016–1022. doi: 10.1093/infdis/jit620. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib62] 62.Rouphael N., Beck A., Kirby A.E., et al. Dose-response of a Norovirus GII.2 controlled human challenge model inoculum. J Infect Dis. 2022;226:1771–1780. doi: 10.1093/infdis/jiac045. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib63] 63.Anfruns-Estrada E., Sabrià A., Fuentes C., et al. Detection of norovirus in saliva samples from acute gastroenteritis cases and asymptomatic subjects: association with age and higher shedding in stool. Viruses. 2020;12:1369. doi: 10.3390/v12121369. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib64] 64.Newman K.L., Moe C.L., Kirby A.E., Flanders W.D., Parkos C.A., Leon J.S. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol. 2016;184:347–357. doi: 10.1111/cei.12772. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib65] 65.Lee N., Chan M.C.W., Wong B., et al. Fecal viral concentration and diarrhea in Norovirus gastroenteritis. Emerg Infect Dis. 2007;13(9):1399–1401. doi: 10.3201/eid1309.061535. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib66] 66.Chiba S., Sakuma Y., Kogasaka R., et al. Fecal shedding of virus in relation to the days of illness in infantile gastroenteritis due to calicivirus. J Infect Dis. 1980;142:247–249. doi: 10.1093/infdis/142.2.247. [DOI] [PubMed] [Google Scholar]

[bib67] 67.Cheng H.-Y., Hung M.-N., Chen W.-C., et al. Ice-associated norovirus outbreak predominantly caused by GII.17 in Taiwan, 2015. BMC Public Health. 2017;17:870. doi: 10.1186/s12889-017-4869-4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib68] 68.Verhoef L., Boxman I.L., Duizer E., et al. Multiple exposures during a norovirus outbreak on a river-cruise sailing through Europe, 2006. Euro Surveill. 2008;13 [PubMed] [Google Scholar]

[bib69] 69.Rockx B., de Wit M., Vennema H., et al. Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis. 2002;35:246–253. doi: 10.1086/341408. [DOI] [PubMed] [Google Scholar]

[bib70] 70.Jacqueline C., Del Valle Arrojo M., Bellver Moreira P., et al. 3[P12] outbreak associated with the drinking water supply in a rural area in Galicia, Spain, 2021. Microbiol Spectr. 2022;10 doi: 10.1128/spectrum.01048-22. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib71] 71.Phumpholsup T., Theamboonlers A., Wanlapakorn N., et al. Norovirus outbreak at a daycare center in BANGKOK, 2014. Southeast Asian J Trop Med Public Health. 2015;46:616–623. [PubMed] [Google Scholar]

[bib72] 72.Hedlund K.-O., Bennet R., Eriksson M., Ehrnst A. Norwalk-like virus as a cause of diarrhea in a pediatric hospital. Clin Microbiol Infect. 1998;4:417–421. [Google Scholar]

[bib73] 73.Struve J., Bennet R., Ehrnst A., et al. Nosocomial calicivirus gastroenteritis in a pediatric hospital. Pediatr Infect Dis J. 1994;13:882–885. doi: 10.1097/00006454-199410000-00007. [DOI] [PubMed] [Google Scholar]

[bib74] 74.Haruki K., Seto Y., Murakami T., Kimura T. Pattern of shedding of small, round-structured virus particles in stools of patients of outbreaks of food-poisoning from raw oysters. Microbiol Immunol. 1991;35:83–86. doi: 10.1111/j.1348-0421.1991.tb01536.x. [DOI] [PubMed] [Google Scholar]

[bib75] 75.Thornhill T.S., Kalica A.R., Wyatt R.G., Kapikian A.Z., Chanock R.M. Pattern of shedding of the norwalk particle in stools during experimentally induced gastroenteritis in volunteers as determined by immune electron microscopy. J Infect Dis. 1975;132:28–34. doi: 10.1093/infdis/132.1.28. [DOI] [PubMed] [Google Scholar]

[bib76] 76.Prystajecky N., Brinkman F.S., Auk B., Isaac-Renton J.L., Tang P. Personalized genetic testing and norovirus susceptibility. Can J Infect Dis Med Microbiol. 2014;25:222. doi: 10.1155/2014/708579. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib77] 77.Murata T., Katsushima N., Mizuta K., Muraki Y., Hongo S., Matsuzaki Y. Prolonged norovirus shedding in infants <or=6 months of age with gastroenteritis. Pediatr Infect Dis J. 2007;26:46–49. doi: 10.1097/01.inf.0000247102.04997.e0. [DOI] [PubMed] [Google Scholar]

[bib78] 78.Green J., Wright P.A., Gallimore C.I., Mitchell O., Morgan-Capner P., Brown D.W. The role of environmental contamination with small round structured viruses in a hospital outbreak investigated by reverse-transcriptase polymerase chain reaction assay. J Hosp Infect. 1998;39:39–45. doi: 10.1016/s0195-6701(98)90241-9. [DOI] [PubMed] [Google Scholar]

[bib79] 79.Cheng H.-Y., Lee C.-C., Chang Y.-C., et al. Viral shedding in gastroenteritis in children caused by variants and novel recombinant norovirus infections. Medicine (Baltimore) 2021;100 doi: 10.1097/MD.0000000000025123. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib80] 80.Gary G.W., Kaplan J.E., Stine S.E., Anderson L.J. Detection of Norwalk virus antibodies and antigen with a biotin-avidin immunoassay. J Clin Microbiol. 1985;22:274–278. doi: 10.1128/jcm.22.2.274-278.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib81] 81.Treanor J.J., Madore H.P., Dolin R. Development of an enzyme immunoassay for the Hawaii agent of viral gastroenteritis. J Virol Methods. 1988;22:207–214. doi: 10.1016/0166-0934(88)90103-6. [DOI] [PubMed] [Google Scholar]

[bib82] 82.Graham D.Y., Jiang X., Tanaka T., Opekun A.R., Madore H.P., Estes M.K. Norwalk virus infection of volunteers: new insights based on improved assays. J Infect Dis. 1994;170:34–43. doi: 10.1093/infdis/170.1.34. [DOI] [PubMed] [Google Scholar]

[bib83] 83.Kirby A., Dove W., Ashton L., Hopkins M., Cunliffe N.A. Detection of norovirus in mouthwash samples from patients with acute gastroenteritis. J Clin Virol. 2010;48:285–287. doi: 10.1016/j.jcv.2010.05.009. [DOI] [PubMed] [Google Scholar]

[bib84] 84.Greenberg H.B., Wyatt R.G., Kapikian A.Z. Norwalk virus in vomitus. Lancet Lond Engl. 1979;1:55. doi: 10.1016/s0140-6736(79)90508-7. [DOI] [PubMed] [Google Scholar]

[bib85] 85.Chilengi R., Simuyandi M., Chibuye M., et al. A pilot study on use of live attenuated rotavirus vaccine (RotarixTM) as an infection challenge model. Vaccine. 2020;38:7357–7362. doi: 10.1016/j.vaccine.2020.09.023. [DOI] [PubMed] [Google Scholar]

[bib86] 86.Freedman S.B., Xie J., Nettel-Aguirre A., et al. A randomized trial evaluating virus-specific effects of a combination probiotic in children with acute gastroenteritis. Nat Commun. 2020;11:2533. doi: 10.1038/s41467-020-16308-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib87] 87.Yen C., Jakob K., Esona M.D., et al. Detection of fecal shedding of rotavirus vaccine in infants following their first dose of pentavalent rotavirus vaccine. Vaccine. 2011;29:4151–4155. doi: 10.1016/j.vaccine.2011.03.074. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib88] 88.Jacobsen S., Niendorf S., Lorenz R., Bock C.-T., Mas Marques A. Differentiation between wild-type group A rotaviruses and vaccine strains in cases of suspected horizontal transmission and adverse events following vaccination. Viruses. 2022;14 doi: 10.3390/v14081670. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib89] 89.Stals F., Walther F.J., Bruggeman C.A. Faecal and pharyngeal shedding of rotavirus and rotavirus IgA in children with diarrhoea. J Med Virol. 1984;14:333–339. doi: 10.1002/jmv.1890140406. [DOI] [PubMed] [Google Scholar]

[bib90] 90.Nordgren J., Bucardo F., Svensson L., Lindgren P.-E. Novel light-upon-extension real-time PCR assay for simultaneous detection, quantification, and genogrouping of group A rotavirus. J Clin Microbiol. 2010;48:1859–1865. doi: 10.1128/JCM.02288-09. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib91] 91.Li J.-S., Cao B., Gao H.-C., et al. Faecal shedding of rotavirus vaccine in Chinese children after vaccination with lanzhou lamb rotavirus vaccine. Sci Rep. 2018;8:1001. doi: 10.1038/s41598-018-19469-w. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib92] 92.Ray P., Fenaux M., Sharma S., et al. Quantitative evaluation of rotaviral antigenemia in children with acute rotaviral diarrhea. J Infect Dis. 2006;194:588–593. doi: 10.1086/505878. [DOI] [PubMed] [Google Scholar]

[bib93] 93.Gutierrez M.B., Fialho A.M., Maranhão A.G., et al. Rotavirus A in Brazil: molecular epidemiology and surveillance during 2018-2019. Pathog Basel Switz. 2020;9 doi: 10.3390/pathogens9070515. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib94] 94.Cowley D., Boniface K., Bogdanovic-Sakran N., Kirkwood C.D., Bines J.E. Rotavirus shedding following administration of RV3-BB human neonatal rotavirus vaccine. Hum Vaccines Immunother. 2017;13:1908–1915. doi: 10.1080/21645515.2017.1323591. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib95] 95.Chrystie I.L., Totterdell B.M., Banatvala J.E. Asymptomatic endemic rotavirus infections in the newborn. Lancet Lond Engl. 1978;1:1176–1178. doi: 10.1016/S0140-6736(78)90967-4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib96] 96.Pickering L.K., Bartlett A.V., III, Reves R.R., Morrow A. Asymptomatic excretion of rotavirus before and after rotavirus diarrhea in children in day care centers. J Pediatr. 1988;112:361–365. doi: 10.1016/s0022-3476(88)80313-5. [DOI] [PubMed] [Google Scholar]

[bib97] 97.Clark H.F., Dolan K.T., Horton-Slight P., Palmer J., Plotkin S.A. Diverse serologic response to rotavirus infection of infants in a single epidemic. Pediatr Infect Dis. 1985;4:626–631. doi: 10.1097/00006454-198511000-00006. [DOI] [PubMed] [Google Scholar]

[bib98] 98.Richardson S., Grimwood K., Gorrell R., Palombo E., Barnes G., Bishop R. Extended excretion of rotavirus after severe diarrhoea in young children. Lancet Lond Engl. 1998;351:1844–1848. doi: 10.1016/S0140-6736(97)11257-0. [DOI] [PubMed] [Google Scholar]

[bib99] 99.Guarino A., Canani R.B., Russo S., et al. Oral immunoglobulins for treatment of acute rotaviral gastroenteritis. Pediatrics. 1994;93:12–16. [PubMed] [Google Scholar]

[bib100] 100.Vesikari T., Sarkkinen H.K., Mäki M. Quantitative aspects of rotavirus excretion in childhood diarrhoea. Acta Paediatr Scand. 1981;70:717–721. doi: 10.1111/j.1651-2227.1981.tb05774.x. [DOI] [PubMed] [Google Scholar]

[bib101] 101.Zheng B.J., Chang R.X., Ma G.Z., et al. Rotavirus infection of the oropharynx and respiratory tract in young children. J Med Virol. 1991;34:29–37. doi: 10.1002/jmv.1890340106. [DOI] [PubMed] [Google Scholar]

[bib102] 102.von Bonsdorff C.H., Hovi T., Mäkelä P., Mörttinen A. Rotavirus infections in adults in association with acute gastroenteritis. J Med Virol. 1978;2:21–28. doi: 10.1002/jmv.1890020105. [DOI] [PubMed] [Google Scholar]

[bib103] 103.Mukhopadhya I., Sarkar R., Menon V.K., et al. Rotavirus shedding in symptomatic and asymptomatic children using reverse transcription-quantitative PCR. J Med Virol. 2013;85:1661–1668. doi: 10.1002/jmv.23641. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib104] 104.Chiappini E., Azzari C., Moriondo M., Galli L., de Martino M. Viraemia is a common finding in immunocompetent children with rotavirus infection. J Med Virol. 2005;76:265–267. doi: 10.1002/jmv.20351. [DOI] [PubMed] [Google Scholar]

[bib105] 105.Argüelles M.H., Villegas G.A., Castello A., et al. VP7 and VP4 genotyping of human group A rotavirus in Buenos Aires, Argentina. J Clin Microbiol. 2000;38:252–259. doi: 10.1128/jcm.38.1.252-259.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib106] 106.Vesikari T., Kapikian A.Z., Delem A., Zissis G. A comparative trial of rhesus monkey (RRV-1) and bovine (RIT 4237) oral rotavirus vaccines in young children. J Infect Dis. 1986;153:832–839. doi: 10.1093/infdis/153.5.832. [DOI] [PubMed] [Google Scholar]

[bib107] 107.Dang D.A., Nguyen V.T., Vu D.T., et al. A dose-escalation safety and immunogenicity study of a new live attenuated human rotavirus vaccine (Rotavin-M1) in Vietnamese children. Vaccine. 2012;30(Suppl 1):A114–A121. doi: 10.1016/j.vaccine.2011.07.118. [DOI] [PubMed] [Google Scholar]

[bib108] 108.Phua K.B., Quak S.H., Lee B.W., et al. Evaluation of RIX4414, a live, attenuated rotavirus vaccine, in a randomized, double-blind, placebo-controlled phase 2 trial involving 2464 Singaporean infants. J Infect Dis. 2005;192(Suppl 1):S6–S16. doi: 10.1086/431511. [DOI] [PubMed] [Google Scholar]

[bib109] 109.Rivera L., Peña L.M., Stainier I., et al. Horizontal transmission of a human rotavirus vaccine strain--a randomized, placebo-controlled study in twins. Vaccine. 2011;29:9508–9513. doi: 10.1016/j.vaccine.2011.10.015. [DOI] [PubMed] [Google Scholar]

[bib110] 110.Ward R.L., Bernstein D.I., Young E.C., Sherwood J.R., Knowlton D.R., Schiff G.M. Human rotavirus studies in volunteers: determination of infectious dose and serological response to infection. J Infect Dis. 1986;154:871–880. doi: 10.1093/infdis/154.5.871. [DOI] [PubMed] [Google Scholar]

[bib111] 111.Donato C.M., Ch’ng L.S., Boniface K.F., et al. Identification of strains of RotaTeq rotavirus vaccine in infants with gastroenteritis following routine vaccination. J Infect Dis. 2012;206:377–383. doi: 10.1093/infdis/jis361. [DOI] [PubMed] [Google Scholar]

[bib112] 112.Bennett A., Pollock L., Jere K.C., et al. Infrequent transmission of monovalent human rotavirus vaccine virus to household contacts of vaccinated infants in Malawi. J Infect Dis. 2019;219:1730–1734. doi: 10.1093/infdis/jiz002. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib113] 113.Magwira C.A., Kgosana L.P., Esona M.D., Seheri M.L. Low fecal rotavirus vaccine virus shedding is significantly associated with non-secretor histo-blood group antigen phenotype among infants in northern Pretoria, South Africa. Vaccine. 2020;38:8260–8263. doi: 10.1016/j.vaccine.2020.11.025. [DOI] [PubMed] [Google Scholar]

[bib114] 114.Flores J., Daoud G., Daoud N., et al. Reactogenicity and antigenicity of rhesus rotavirus vaccine (MMU-18006) in newborn infants in Venezuela. Pediatr Infect Dis J. 1988;7:776–780. doi: 10.1097/00006454-198811000-00006. [DOI] [PubMed] [Google Scholar]

[bib115] 115.Cantelli C.P., Velloso A.J., de Assis R.M.S., et al. Rotavirus A shedding and HBGA host genetic susceptibility in a birth community-cohort, Rio de Janeiro, Brazil, 2014-2018. Sci Rep. 2020;10:6965. doi: 10.1038/s41598-020-64025-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib116] 116.Smith C.K., McNeal M.M., Meyer N.R., Haase S., Dekker C.L. Rotavirus shedding in premature infants following first immunization. Vaccine. 2011;29:8141–8146. doi: 10.1016/j.vaccine.2011.08.028. [DOI] [PubMed] [Google Scholar]

[bib117] 117.Hiramatsu H., Suzuki R., Nagatani A., et al. Rotavirus vaccination can be performed without viral dissemination in the neonatal intensive care unit. J Infect Dis. 2018;217:589–596. doi: 10.1093/infdis/jix590. [DOI] [PubMed] [Google Scholar]

[bib118] 118.Miura H., Kawamura Y., Sugata K., et al. Rotavirus vaccine strain transmission by vaccinated infants in the foster home. J Med Virol. 2017;89:79–84. doi: 10.1002/jmv.24613. [DOI] [PubMed] [Google Scholar]

[bib119] 119.Mijatovic-Rustempasic S., Immergluck L.C., Parker T.C., et al. Shedding of porcine circovirus type 1 DNA and rotavirus RNA by infants vaccinated with rotarix®. Hum Vaccines Immunother. 2017;13:928–935. doi: 10.1080/21645515.2016.1255388. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib120] 120.Anderson E.L., Belshe R.B., Bartram J., Crookshanks-Newman F., Chanock R.M., Kapikian A.Z. Evaluation of rhesus rotavirus vaccine (MMU 18006) in infants and young children. J Infect Dis. 1986;153:823–831. doi: 10.1093/infdis/153.5.823. [DOI] [PubMed] [Google Scholar]

[bib121] 121.Tort L.F.L., Victoria M., Lizasoain A.A., et al. Molecular epidemiology of group A rotavirus among children admitted to hospital in Salto, Uruguay, 2011-2012: first detection of the emerging genotype G12. J Med Virol. 2015;87:754–763. doi: 10.1002/jmv.24123. [DOI] [PubMed] [Google Scholar]

[bib122] 122.Cotterill H., Curry A., Riordan T. Rotavirus in vomit. J Infect. 1988;16:206–207. doi: 10.1016/s0163-4453(88)94297-1. [DOI] [PubMed] [Google Scholar]

[bib123] 123.Borade A., Bais A.S., Bapat V., Dhongade R. Characteristics of rotavirus gastroenteritis in hospitalized children in Pune. Indian J Med Sci. 2010;64:210–218. [PubMed] [Google Scholar]

[bib124] 124.Yokoyama T., Sugimoto N., Taniguchi K., et al. Molecular and immunohistochemical detection of rotavirus in urinary sediment cells of children with rotavirus gastroenteritis. Clin Microbiol Infect. 2011;17:1190–1193. doi: 10.1111/j.1469-0691.2011.03522.x. [DOI] [PubMed] [Google Scholar]

[bib125] 125.Santosham M., Yolken R.H., Quiroz E., et al. Detection of rotavirus in respiratory secretions of children with pneumonia. J Pediatr. 1983;103:583–585. doi: 10.1016/s0022-3476(83)80591-5. [DOI] [PubMed] [Google Scholar]

[bib126] 126.Satter S.M., Katz E., Hossain M.E., et al. Detection of rotavirus in respiratory specimens from Bangladeshi children aged <2 years hospitalized for acute gastroenteritis. J Infect Dis. 2024;229:457–461. doi: 10.1093/infdis/jiad333. [DOI] [PubMed] [Google Scholar]

[bib127] 127.Martin Perceval L., Scherdel P., Jarry B., de Visme S., Levieux K., Gras-Le Guen C. Sudden unexpected death in infancy: current practices in virological investigations and documentation in the French registry. J Pediatr. 2023;257 doi: 10.1016/j.jpeds.2023.01.003. [DOI] [PubMed] [Google Scholar]

[bib128] 128.Kiyohara T., Ouchi Y., Hasegawa Y., et al. An in-house-anti-hepatitis A virus (HAV)-specific immunoglobulin M capture enzyme-linked immunosorbent assay: evaluation and application to an HAV outbreak. J Med Virol. 2009;81:1513–1516. doi: 10.1002/jmv.21578. [DOI] [PubMed] [Google Scholar]

[bib129] 129.Tjon G.M.S., Coutinho R.A., van den Hoek A., et al. High and persistent excretion of hepatitis A virus in immunocompetent patients. J Med Virol. 2006;78:1398–1405. doi: 10.1002/jmv.20711. [DOI] [PubMed] [Google Scholar]

[bib130] 130.Arankalle V.A., Sarada Devi K.L., Lole K.S., Shenoy K.T., Verma V., Haneephabi M. Molecular characterization of hepatitis A virus from a large outbreak from Kerala, India. Indian J Med Res. 2006;123:760–769. [PubMed] [Google Scholar]

[bib131] 131.Hundekar S., Thorat N., Gurav Y., Lole K. Viral excretion and antibody titers in children infected with hepatitis A virus from an orphanage in Western India. J Clin Virol. 2015;73:27–31. doi: 10.1016/j.jcv.2015.10.012. [DOI] [PubMed] [Google Scholar]

[bib132] 132.Costafreda M.I., Bosch A., Pintó R.M. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Appl Environ Microbiol. 2006;72:3846–3855. doi: 10.1128/AEM.02660-05. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib133] 133.Kamel A.H., Ali M.A., El-Nady H.G., et al. Presence of enteric hepatitis viruses in the sewage and population of Greater Cairo. Clin Microbiol Infect. 2011;17:1182–1185. doi: 10.1111/j.1469-0691.2011.03461.x. [DOI] [PubMed] [Google Scholar]

[bib134] 134.Amado L.A., Villar L.M., de Paula V.S., Gaspar A.M.C. Comparison between serum and saliva for the detection of hepatitis A virus RNA. J Virol Methods. 2008;148:74–80. doi: 10.1016/j.jviromet.2007.10.020. [DOI] [PubMed] [Google Scholar]

[bib135] 135.Mackiewicz V., Dussaix E., Petitcorps M.-F.L., Roque-Afonso A.M. Detection of Hepatitis A virus RNA in saliva. J Clin Microbiol. 2004;42:4329. doi: 10.1128/JCM.42.9.4329-4331.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib136] 136.Amado L.A., Villar L.M., de Paula V.S., Pinto M.A., Gaspar A.M.C. Exposure to multiple subgenotypes of hepatitis A virus during an outbreak using matched serum and saliva specimens. J Med Virol. 2011;83:768–775. doi: 10.1002/jmv.22045. [DOI] [PubMed] [Google Scholar]

[bib137] 137.Amado Leon L.A., de Almeida A.J., de Paula V.S., et al. Longitudinal study of hepatitis A infection by saliva sampling: the kinetics of HAV markers in saliva revealed the application of saliva tests for hepatitis A study. PLoS One. 2015;10 doi: 10.1371/journal.pone.0145454. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib138] 138.Locarnini S.A., Gust I.D., Ferris A.A., Stott A.C., Wong M.L. A prospective study of acute viral hepatitis with particular reference to hepatitis A. Bull World Health Organ. 1976;54:199. [PMC free article] [PubMed] [Google Scholar]

[bib139] 139.Chitambar S.D., Fadnis R.S., Joshi M.S., Habbu A., Bhatia S.G. Case report: hepatitis A preceding Guillain-Barré syndrome. J Med Virol. 2006;78:1011–1014. doi: 10.1002/jmv.20656. [DOI] [PubMed] [Google Scholar]

[bib140] 140.Coulepis A.G., Locarnini S.A., Lehmann N.I., Gust I.D. Detection of hepatitis A virus in the feces of patients with naturally acquired infections. J Infect Dis. 1980;141:151–156. doi: 10.1093/infdis/141.2.151. [DOI] [PubMed] [Google Scholar]

[bib141] 141.Coutinho R.A., Duermeyer W., van der Veen J. Epidemiology of hepatitis A in Amsterdam, October 1978--December 1979. J Virol Methods. 1980;2:47–55. doi: 10.1016/0166-0934(80)90038-5. [DOI] [PubMed] [Google Scholar]

[bib142] 142.Tassopoulos N.C., Papaevangelou G.J., Ticehurst J.R., Purcell R.H. Fecal excretion of Greek strains of hepatitis A virus in patients with hepatitis A and in experimentally infected chimpanzees. J Infect Dis. 1986;154:231–237. doi: 10.1093/infdis/154.2.231. [DOI] [PubMed] [Google Scholar]

[bib143] 143.Coursaget P., Maupas P., Hibon P., Lesage G., Hubert M. Hepatitis A diagnosis in man: radioimmunoassay for hepatitis A antigen detection in faeces. J Med Virol. 1980;6:53–60. doi: 10.1002/jmv.1890060108. [DOI] [PubMed] [Google Scholar]

[bib144] 144.Normann A., Pfisterer-Hunt M., Schade S., et al. Molecular epidemiology of an outbreak of hepatitis A in Italy. J Med Virol. 1995;47:467–471. doi: 10.1002/jmv.1890470429. [DOI] [PubMed] [Google Scholar]

[bib145] 145.Bruisten S.M., van Steenbergen J.E., Pijl A.S., Niesters H.G., van Doornum G.J., Coutinho R.A. Molecular epidemiology of hepatitis A virus in Amsterdam, the Netherlands. J Med Virol. 2001;63:88–95. [PubMed] [Google Scholar]

[bib146] 146.Selander B., Bläckberg J., Widell A., Johansson P.J.H. No evidence of intrauterine transmission of hepatitis A virus from a mother to a premature infant. Acta Paediatr Oslo Nor. 1992 2009;98:1603–1606. doi: 10.1111/j.1651-2227.2009.01402.x. [DOI] [PubMed] [Google Scholar]

[bib147] 147.Yotsuyanagi H., Koike K., Yasuda K., et al. Prolonged fecal excretion of hepatitis A virus in adult patients with hepatitis A as determined by polymerase chain reaction. Hepatology. 1996;24:10–13. doi: 10.1053/jhep.1996.v24.pm0008707246. [DOI] [PubMed] [Google Scholar]

[bib148] 148.Frösner G.G., Overby L.R., Flehmig B., et al. Seroepidemiological investigation of patients and family contacts in an epidemic of hepatitis A. J Med Virol. 1977;1:163–173. doi: 10.1002/jmv.1890010303. [DOI] [PubMed] [Google Scholar]

[bib149] 149.Dienstag J.L., Feinstone S.M., Kapikian A.Z., Purcell R.H. Faecal shedding of hepatitis-A antigen. Lancet. 1975;1:765–767. doi: 10.1016/s0140-6736(75)92434-4. [DOI] [PubMed] [Google Scholar]

[bib150] 150.Ma F., Yang J., Kang G., et al. Comparison of the safety and immunogenicity of live attenuated and inactivated hepatitis A vaccine in healthy Chinese children aged 18 months to 16 years: results from a randomized, parallel controlled, phase IV study. Clin Microbiol Infect. 2016;22:811.e9–811.e15. doi: 10.1016/j.cmi.2016.06.004. [DOI] [PubMed] [Google Scholar]

[bib151] 151.Wang X., Pan Y., Chen J., et al. The excretion rate and stability of HAAg in human fecal samples after live attenuated hepatitis A vaccination. J Med Virol. 2020;92:3312–3318. doi: 10.1002/jmv.25747. [DOI] [PubMed] [Google Scholar]

[bib152] 152.Stapleton J.T., Lange D.K., LeDuc J.W., Binn L.N., Jansen R.W., Lemon S.M. The role of secretory immunity in hepatitis A virus infection. J Infect Dis. 1991;163:7–11. doi: 10.1093/infdis/163.1.7. [DOI] [PubMed] [Google Scholar]

[bib153] 153.Joshi M.S., Bhalla S., Kalrao V.R., Dhongade R.K., Chitambar S.D. Exploring the concurrent presence of hepatitis A virus genome in serum, stool, saliva, and urine samples of hepatitis A patients. Diagn Microbiol Infect Dis. 2014;78:379–382. doi: 10.1016/j.diagmicrobio.2013.12.013. [DOI] [PubMed] [Google Scholar]

[bib154] 154.Portes S.A.R., Volotão E.D.M., Rocha M.S., et al. A non-enteric adenovirus A12 gastroenteritis outbreak in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 2016;111:403–406. doi: 10.1590/0074-02760160030. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib155] 155.do Nascimento L.G., Fialho A.M., de Andrade J.D.S.R., de Assis R.M.S., Fumian T.M. Human enteric adenovirus F40/41 as a major cause of acute gastroenteritis in children in Brazil, 2018 to 2020. Sci Rep. 2022;12 doi: 10.1038/s41598-022-15413-1. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib156] 156.Allayeh A.K., Al-Daim S.A., Ahmed N., El-Gayar M., Mostafa A. Isolation and genotyping of adenoviruses from wastewater and diarrheal samples in Egypt from 2016 to 2020. Viruses. 2022;14 doi: 10.3390/v14102192. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib157] 157.Elmahdy E.M., Ahmed N.I., Shaheen M.N.F., Mohamed E.-C.B., Loutfy S.A. Molecular detection of human adenovirus in urban wastewater in Egypt and among children suffering from acute gastroenteritis. J Water Health. 2019;17:287–294. doi: 10.2166/wh.2019.303. [DOI] [PubMed] [Google Scholar]

[bib158] 158.Zhuo R., Parsons B.D., Lee B.E., et al. Identification of enteric viruses in oral swabs from children with acute gastroenteritis. J Mol Diagn. 2018;20:56–62. doi: 10.1016/j.jmoldx.2017.09.003. [DOI] [PubMed] [Google Scholar]

[bib159] 159.Fall A., Campodónico V.L., Howard C., et al. Dissemination and genome characterization of a human adenovirus F41 in a patient with B-Cell lymphoma. Virol J. 2023;20:141. doi: 10.1186/s12985-023-02101-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib160] 160.McFarlane E.S., Goldbloom A.L., Embil J.A. Prolonged excretion of an identical cytomegalovirus strain by two siblings and the intermittent isolation of an adenovirus from the urine of one of them. J Med Virol. 1987;23:283–287. doi: 10.1002/jmv.1890230311. [DOI] [PubMed] [Google Scholar]

[bib161] 161.Chen W., Bibby K. A model-based framework to assess the feasibility of monitoring zika virus with wastewater-based epidemiology. ACS EST Water. 2023;3:1071–1081. [Google Scholar]

[bib162] 162.Lowry S.A., Wolfe M.K., Boehm A.B. Respiratory virus concentrations in human excretions that contribute to wastewater: a systematic review and meta-analysis. J Water Health. 2023;21:831–848. doi: 10.2166/wh.2023.057. [DOI] [PubMed] [Google Scholar]

[bib163] 163.Schoen M.E., Bidwell A.L., Wolfe M.K., Boehm A.B. United States influenza 2022–2023 season characteristics as inferred from wastewater solids, influenza hospitalization, and syndromic data. Environ Sci Technol. 2023;57:20542–20550. doi: 10.1021/acs.est.3c07526. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib164] 164.Lee R.M., Lessler J., Lee R.A., et al. Incubation periods of viral gastroenteritis: a systematic review. BMC Infect Dis. 2013;13:446. doi: 10.1186/1471-2334-13-446. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib165] 165.CDC . Epidemiology and Prevention of Vaccine-Preventable Diseases. 2024. Chapter 19: rotavirus.https://www.cdc.gov/pinkbook/hcp/table-of-contents/chapter-19-rotavirus.html published online Sept 30. [Google Scholar]

[bib166] 166.Health D of P. California department of public health. https://www.cdph.ca.gov/Programs/CID/DCDC

[bib167] 167.CDC . Epidemiology and Prevention of Vaccine-Preventable Diseases. 2024. Chapter 9: hepatitis A.https://www.cdc.gov/pinkbook/hcp/table-of-contents/chapter-9-hepatitis-a.html published online Sept 30. [Google Scholar]

[bib168] 168.Huisman J.S., Scire J., Caduff L., et al. Wastewater-based estimation of the effective reproductive number of SARS-CoV-2. Environ Health Perspect. 2022;130 doi: 10.1289/EHP10050. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib169] 169.Nourbakhsh S., Fazil A., Li M., et al. A wastewater-based epidemic model for SARS-CoV-2 with application to three Canadian cities. Epidemics. 2022;39 doi: 10.1016/j.epidem.2022.100560. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib170] 170.Mohring J., Leithäuser N., Wlazło J., et al. Estimating the COVID-19 prevalence from wastewater. Sci Rep. 2024;14 doi: 10.1038/s41598-024-64864-1. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib171] 171.McManus O., Christiansen L.E., Nauta M., et al. Predicting COVID-19 incidence using wastewater surveillance data, Denmark, October 2021–June 2022. Emerg Infect Dis. 2023;29 doi: 10.3201/eid2908.221634. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib172] 172.Staff G.B. Global Biodefense. 2020. Sewage surveillance: watching wastewater for SARS-CoV-2.https://globalbiodefense.com/2020/08/31/sewage-surveillance-watching-wastewater-for-sars-cov-2/ published online Aug 31. [Google Scholar]

[bib173] 173.Chan E.M.G., Bidwell A., Li Z., Tilmans S., Boehm A.B. Public health policy impact evaluation: a potential use case for longitudinal monitoring of viruses in wastewater at small geographic scales. PLoS Water. 2024;3 [Google Scholar]

[bib174] 174.Haas C.N., Rose J.B., Gerba C.P. 2nd ed. Wiley; Hoboken: 2014. Quantitative microbial risk assessment. [DOI] [Google Scholar]

[bib175] 175.Carducci A., Donzelli G., Cioni L., Federigi I., Lombardi R., Verani M. Quantitative microbial risk assessment for workers exposed to bioaerosol in wastewater treatment plants aimed at the choice and setup of safety measures. Int J Environ Res Public Health. 2018;15:1490. doi: 10.3390/ijerph15071490. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib176] 176.Bustin S.A., Benes V., Garson J.A., et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55:611–622. doi: 10.1373/clinchem.2008.112797. [DOI] [PubMed] [Google Scholar]

[bib177] 177.Borchardt M.A., Boehm A.B., Salit M.L., Spencer S.K., Wigginton K.R., Noble R.T. The environmental microbiology minimum information (EMMI) guidelines: qPCR and dPCR quality and reporting for environmental microbiology. Environ Sci Technol. 2021;55:10210–10223. doi: 10.1021/acs.est.1c01767. [DOI] [PubMed] [Google Scholar]

PERMALINK

Systematic review and meta-analysis of enteric virus shedding in human excretions

Gang Zheng

Elana MG Chan

Alexandria B Boehm

Summary

Background

Methods

Findings

Interpretation

Funding

Research in context.

Evidence before this study

Added value of this study

Implications of all the available evidence

Introduction

Methods

Ethics

Search strategy and selection criteria

Fig. 1.

Data analysis

Concentrations of viruses

Longitudinal concentration data

Longitudinal presence data

Role of funder

Results

Systematic review

Norovirus

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Rotavirus

Hepatitis A virus

Adenovirus group F

Meta-analysis

Publication bias

Discussion

Contributors

Data sharing statement

Declaration of interests

Acknowledgements

Footnotes

Appendix A. Supplementary data

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases