Bioaccumulation and persistence of faecal bacterial and viral indicators in Mytilus edulis and Crassostrea gigas

Olalemi, Adewale; Baker‐Austin, Craig; Ebdon, James; Taylor, Huw

doi:10.1016/j.ijheh.2016.06.002

Cited by 26 publications

(25 citation statements)

References 22 publications

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“…In this study, the decreased kinetics of GI and GII NoV (genomes) and FRNAPH (infectious particles and genomes) in oysters under different purification conditions were established. When focusing only on purification conditions applied to oysters coming from polluted areas, many studies have shown not only the incidence of physicochemical conditions (i.e., water temperature, salinity, and dissolved oxygen) on shellfish physiology but also the effect of the initial microorganism load (i.e., natural or artificial contamination) (10,(35)(36)(37). For these reasons, we decided to work with naturally NoV-contaminated oysters that were also positive for FRNAPH, because of the high correlation previously demonstrated (25).…”

Section: Discussionmentioning

confidence: 99%

F-Specific RNA Bacteriophages Model the Behavior of Human Noroviruses during Purification of Oysters: the Main Mechanism Is Probably Inactivation Rather than Release

Leduc

Leclerc

Challant

et al. 2020

Appl Environ Microbiol

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Noroviruses (NoV) are responsible for many shellfish outbreaks. Purification processes may be applied to oysters before marketing to decrease potential fecal pollution. This step is rapidly highly effective in reducing Escherichia coli; nevertheless, the elimination of virus genomes has been described to be much slower. It is therefore important to identify (i) the purification conditions that optimize virus removal and (ii) the mechanism involved. To this end, the effects of oyster stress, nutrients, and the presence of a potential competitor to NoV adhesion during purification were investigated using naturally contaminated oysters. Concentrations of NoV (genomes) and of the viral indicator F-specific RNA bacteriophage (FRNAPH; genomes and infectious particles) were regularly monitored. No significant differences were observed under the test conditions. The decrease kinetics of both virus genomes were similar, again showing the potential of FRNAPH as an indicator of NoV behavior during purification. The T90 (time to reduce 90% of the initial titer) values were 47.8 days for the genogroup I NoV genome, 26.7 days for the genogroup II NoV genome, and 43.9 days for the FRNAPH-II genome. Conversely, monitoring of the viral genomes could not be used to determine the behavior of infectious viruses because the T90 values were more than two times lower for infectious FRNAPH (20.6 days) compared to their genomes (43.9 days). Finally, this study highlighted that viruses are primarily inactivated in oysters rather than released in the water during purification processes. IMPORTANCE This study provides new data about the behavior of viruses in oysters under purification processes and about their elimination mechanism. First, a high correlation has been observed between F-specific RNA bacteriophages of subgroup II (FRNAPH-II) and norovirus (NoV) in oysters impacted by fecal contamination when both are detected using molecular approaches. Second, when using reverse transcription-quantitative PCR and culture to detect FRNAPH-II genomes and infectious FRNAPH in oysters, respectively, it appears that genome detection provides limited information about the presence of infectious particles. The comparison of both genomes and infectious particles highlights that the main mechanism of virus elimination in oysters is inactivation. Finally, this study shows that none of the conditions tested modify virus removal.

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Section: Discussionmentioning

confidence: 99%

F-Specific RNA Bacteriophages Model the Behavior of Human Noroviruses during Purification of Oysters: the Main Mechanism Is Probably Inactivation Rather than Release

Leduc

Leclerc

Challant

et al. 2020

Appl Environ Microbiol

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show abstract

“…When the focus was only on the depuration conditions applied to oysters coming from polluted areas, many studies have shown not only the impact of the physicochemical conditions (i.e., water temperature, salinity, dissolved oxygen) and shellfish physiology but also the impact of the initial microorganism load (i.e., natural or artificial contamination) (59)(60)(61)(62). For these reasons, we decided to work with oysters that were naturally contaminated with NoV and that were also positive for FRNAPH because of the high correlation of the presence of the two viruses discussed above.…”

Section: Discussionmentioning

confidence: 99%

F-Specific RNA Bacteriophages, Especially Members of Subgroup II, Should Be Reconsidered as Good Indicators of Viral Pollution of Oysters

Hartard

Leclerc

Rivet

et al. 2018

Appl Environ Microbiol

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Norovirus (NoV) is the leading cause of gastroenteritis outbreaks linked to oyster consumption. In this study, we investigated the potential of F-specific RNA bacteriophages (FRNAPH) as indicators of viral contamination in oysters by focusing especially on FRNAPH subgroup II (FRNAPH-II). These viral indicators have been neglected because their behavior is sometimes different from that of NoV in shellfish, especially during the depuration processes usually performed before marketing. However, a significant bias needs to be taken into account. This bias is that, in the absence of routine culture methods, NoV is targeted by genome detection, while the presence of FRNAPH is usually investigated by isolation of infectious particles. In this study, by targeting both viruses using genome detection, a significant correlation between the presence of FRNAPH-II and that of NoV in shellfish collected from various European harvesting areas impacted by fecal pollution was observed. Moreover, during their depuration, while the long period of persistence of NoV was confirmed, a similar or even longer period of persistence of the FRNAPH-II genome, which was over 30 days, was observed. Such a striking genome persistence calls into question the relevance of molecular methods for assessing viral hazards. Targeting the same virus (i.e., FRNAPH-II) by culture and genome detection in specimens from harvesting areas as well as during depuration, we concluded that the presence of genomes in shellfish does not provide any information on the presence of the corresponding infectious particles. In view of these results, infectious FRNAPH detection should be reconsidered as a valuable indicator in oysters, and its potential for use in assessing viral hazard needs to be investigated. This work brings new data about the behavior of viruses in shellfish, as well as about the relevance of molecular methods for their detection and evaluation of the viral hazard. First, a strong correlation between the presence of F-specific RNA bacteriophages of subgroup II (FRNAPH-II) and that of norovirus (NoV) in shellfish impacted by fecal contamination has been observed when both viruses are detected using molecular approaches. Second, when reverse transcription-PCR and culture are used to detect FRNAPH-II in shellfish, it appears that the genomes of the viruses present a longer period of persistence than infectious virus, and thus, virus genome detection fails to give information about the concomitant presence of infectious viruses. Finally, this study shows that FRNAPH persist at least as long as NoV does. These data are major arguments to reconsider the potential of FRNAPH as indicators of shellfish viral quality.

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“…This may be the result of differences in the physiology of the shellfish or the pathogen, the rate of metabolism in the shellfish, the duration of exposure of the shellfish to the pathogen or its source, the exposure dose and other factors, such as salinity and temperature, which all serve to influence filtration rates within the shellfish (Olalemi et al . ).…”

Section: Discussionmentioning

confidence: 97%

“…This work is applicable to other types of shellfish species, although different shellfish species may demonstrate varying abilities to bioaccumulate microbial indicators or pathogens. This may be the result of differences in the physiology of the shellfish or the pathogen, the rate of metabolism in the shellfish, the duration of exposure of the shellfish to the pathogen or its source, the exposure dose and other factors, such as salinity and temperature, which all serve to influence filtration rates within the shellfish (Olalemi et al 2016).…”

Section: Discussionmentioning

confidence: 99%

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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Bioaccumulation and persistence of faecal bacterial and viral indicators in Mytilus edulis and Crassostrea gigas

Cited by 26 publications

References 22 publications

F-Specific RNA Bacteriophages Model the Behavior of Human Noroviruses during Purification of Oysters: the Main Mechanism Is Probably Inactivation Rather than Release

F-Specific RNA Bacteriophages Model the Behavior of Human Noroviruses during Purification of Oysters: the Main Mechanism Is Probably Inactivation Rather than Release

F-Specific RNA Bacteriophages, Especially Members of Subgroup II, Should Be Reconsidered as Good Indicators of Viral Pollution of Oysters

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

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