Meta-Analysis of the Reduction of Norovirus and Male-Specific Coliphage Concentrations in Wastewater Treatment Plants

Pouillot, Régis; Doren, Jane M. Van; Woods, Jacquelina; Plante, Daniel; Smith, Mark W.; Goblick, Gregory N.; Roberts, Christopher; Locas, Annie; Hajen, Walter; Stobo, Jeffrey; White, John Kerr; Holtzman, Jennifer; Buenaventura, Enrico; Burkhardt, William; Catford, Angela; Edwards, Robyn; DePaola, Angelo; Calci, Kevin R.

doi:10.1128/aem.00509-15

Cited by 63 publications

(74 citation statements)

References 56 publications

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“…The concentration of NoV GII in the influent was higher than that of GI, which is in accordance with previous reports and epidemiological trends in the United States and globally (3,8,(35)(36)(37)(38). Epidemiological data in the United States and worldwide have shown that NoV outbreaks peak in the colder winter months, with 55% of the cases in the United States occurring in December to February (35,39), and is in agreement with our observation of high NoV GII densities (5.6 log 10 GC/100 ml) in the influent in November to March and with previous reports (3, 37, 40, 41).…”

Section: Discussionsupporting

confidence: 81%

“…These findings indicate that virus removal was impacted negatively by the initial viral loads and positively by the environmental temperature. Virus removal fluctuated over time and was in accordance with previous studies (6,36,37,49). Compared with NoV GII strains, the GI strains seemed to be approximately 4.8 times more resistant to the two-stage wastewater treatment.…”

Section: Figsupporting

confidence: 72%

“…A recent study estimated that the 50% human infectious dose (HID50) of NoV is similar to that of other RNA viruses and ranges between 3.01 and 3.45 log 10 virions (43). Regarding high densities of NoV GI and GII observed in the effluent discharged into the river water, we can imply that the exposure of drinking water, irrigation water, shellfish harvesting, or recreational waters with sewage-contaminated surface waters can pose a potential health risk to humans (37,38,42,44). The health risk can be higher during the aftermath of a heavy rain or system failure that causes overflow of raw or partially treated wastewater into the environment (45).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, MSC removal seemed to have the potential to indicate the efficiency of secondary treatment on removing NoV GII in WWTP. Recently, MSC (along with E. coli) has been suggested as a good indicator of virus removal across conventional secondary disinfection processes (9,37). Assuming a comparable abundance and survival of NoV and MSC, we could conclude that at least a portion of NoV GII strains detected in the effluent maintained their infectivity due to simultaneous detection of viable MSC plaques and NoV GII viral genomes, as suggested by Hewitt et al (8), who reported the parallel occurrence of cultivable enteric viruses and PCR concentrations.…”

Section: Figmentioning

confidence: 99%

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Pathogenic Enteric Viruses and Microbial Indicators during Secondary Treatment of Municipal Wastewater

Montazeri

Goettert

Achberger

et al. 2015

Appl Environ Microbiol

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c Pathogenic enteric viruses are responsible for a wide range of infections in humans, with diverse symptoms. Raw and partially treated wastewaters are major sources of environmental contamination with enteric viruses. We monitored a municipal secondary wastewater treatment plant (New Orleans, LA) on a monthly basis for norovirus (NoV) GI and GII and enterovirus serotypes using multiplex reverse transcription-quantitative PCR (RT-qPCR) and microbial indicators of fecal contamination using standard plating methods. Densities of indicator bacteria (enterococci, fecal coliforms, and Escherichia coli) did not show monthly or seasonal patterns. Norovirus GII was more abundant than GI and, along with enterovirus serotypes, increased in influent during fall and spring. The highest NoV GI density in influent was in the fall, reaching an average of 4.0 log 10 genomic copies/100 ml. Norovirus GI removal (0.95 log 10 ) was lower than that for GII, enterovirus serotypes, and male-specific coliphages (1.48 log 10 ) or for indicator bacteria (4.36 log 10 ), suggesting higher resistance of viruses to treatment. Male-specific coliphages correlated with NoV GII densities in influent and effluent (r ‫؍‬ 0.48 and 0.76, respectively) and monthly removal, indicating that male-specific coliphages can be more reliable than indicator bacteria to monitor norovirus GII load and microbial removal. Dominant norovirus genotypes were classified into three GI genotypes (GI.1, GI.3, and GI.4) and four GII genotypes (GII.3, GII.4, GII.13, and GII.21), dominated by GI.1 and GII.4 strains. Some of the seasonal and temporal patterns we observed in the pathogenic enteric viruses were different from those of epidemiological observations. E nteric viruses are responsible for a wide range of infections in humans with diverse symptoms. Infected individuals shed millions of virus particles in their feces or body fluids, which eventually enter sewage systems. Enteric viruses may naturally occur in aquatic environments as well, but human activities, in particular, sewage discharge, is the primary source of environmental contaminants (1-3). Among the pathogenic enteric viruses, norovirus (NoV), enterovirus (EV), adenovirus, astrovirus, and rotavirus have been found frequently in municipal wastewaters worldwide (1, 4-6). Several gastroenteritis outbreaks have been linked directly or indirectly to human exposure of raw or partially treated sewage-contaminated water or foods (2).Municipal wastewaters usually undergo a secondary treatment before being discharged into the environment. The process involves a mechanical treatment for removing solids followed by biological and chemical treatments, nutrient removal, and discharge (7). Primary-treated (physically processed) wastewater or the effluent water that does not undergo a disinfection process may still harbor infectious enteric viruses, similar to the raw sewage (4, 8). To protect water quality and public safety, fecal coliforms and Escherichia coli have been used to monitor fecal pollution in wastewater dis...

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Section: Discussionsupporting

confidence: 81%

Section: Figsupporting

confidence: 72%

Section: Discussionmentioning

confidence: 99%

Section: Figmentioning

confidence: 99%

See 2 more Smart Citations

Pathogenic Enteric Viruses and Microbial Indicators during Secondary Treatment of Municipal Wastewater

Montazeri

Goettert

Achberger

et al. 2015

Appl Environ Microbiol

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“…; Pouillot et al . ). This is because they have several characteristics in common with enteric viruses.…”

Section: Introductionmentioning

confidence: 97%

The application of phage-based faecal pollution markers to predict the concentration of adenoviruses in mussels (Mytilus edulis) and their overlying waters

et al. 2016

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Aim This study set out to determine whether phage‐based indicators may provide a ‘low‐tech’ alternative to existing approaches that might help maintain the microbial safety of shellfish and their overlying waters. Methods and Results Mussels and their overlying waters were collected biweekly from an estuary in southeast England over a 2‐year period (May 2013–April 2015) (n = 48). Levels of bacterial indicators were determined using membrane filtration and most probable number methods and those of bacteriophages were determined by direct plaque assay. The detection of adenovirus was determined using real‐time polymerase chain reaction. The results revealed that somatic coliphages demonstrated the most significant correlations with AdV F and G in mussels (ρ = 0·55) and overlying waters (ρ = 0·66), followed by GB124 phages (ρ = 0·43) while Escherichia coli showed no correlation with AdV F and G in mussels. Conclusion This study demonstrates that the use of somatic coliphages and GB124 phages may provide a better indication of the risk of adenovirus contamination of mussels and their overlying waters than existing bacterial indicators. Significance and Impact of the Study Phage‐based detection may be particularly advantageous in low‐resource settings where viral infectious disease presents a significant burden to human health.

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Evaluating the fate of bacterial indicators, viral indicators, and viruses in water resource recovery facilities

Worley-Morse

Mann

Khunjar

et al. 2019

Water Environment Research

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A year‐long sampling campaign at nine water resource recovery facilities (WRRFs) was conducted to assess the treatability and fate of bacterial indicators, viral indicators, and viruses. Influent concentrations of viral indicators (male‐specific and somatic coliphages) and bacterial indicators (Escherichia coli and enterococci) remained relatively constant, typically varying by one order of magnitude over the course of the year. Annual average bacterial indicator reduction ranged from 4.0 to 6.7 logs, and annual average viral indicator reduction ranged from 1.6 to 5.4 logs. Bacterial and viral indicator reduction depended on the WRRF's treatment processes, and bacterial indicator reduction was greater than viral indicator reduction for many processes. Viral reduction (adenovirus 41, norovirus GI, and norovirus GII) was more similar to viral indicator reduction than bacterial indicator reduction. Overall, this work suggests that viral indicator reduction in WRRFs is variable and depends on specific unit processes. Moreover, for the same unit treatment process, viral indicator reduction and bacterial indicator reduction can vary.Practitioner points A year‐long sampling campaign was conducted at nine water resource recovery facilities (WRRFs).The treatability and fate of bacterial indicators, viral indicators, and viruses were assessed.Viral indicator reduction in WRRFs is variable and depends on specific unit processes.For the same unit treatment process, viral indicator reduction and bacterial indicator reduction can vary.

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Meta-Analysis of the Reduction of Norovirus and Male-Specific Coliphage Concentrations in Wastewater Treatment Plants

Cited by 63 publications

References 56 publications

Pathogenic Enteric Viruses and Microbial Indicators during Secondary Treatment of Municipal Wastewater

Pathogenic Enteric Viruses and Microbial Indicators during Secondary Treatment of Municipal Wastewater

The application of phage-based faecal pollution markers to predict the concentration of adenoviruses in mussels (Mytilus edulis) and their overlying waters

Evaluating the fate of bacterial indicators, viral indicators, and viruses in water resource recovery facilities

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