Oysters and norovirus: something special?

Shellfish can be a vector for human pathogens. Despite regulation based on enteric bacteria, shellfish are still implicated in viral outbreaks. Oysters are the most common shellfish associated with outbreaks, and noroviruses, which cause acute gastroenteritis, are the most frequently identified pathogen in these outbreaks. Analysis of shellfish-related outbreak data worldwide shows an unexpected high proportion of genogroup I strains. Recent studies performed in vitro, in vivo and in the environment indicate that oysters are not just a passive filter, but can selectively accumulate norovirus strains based on virus carbohydrate ligands shared with humans. These observations may help explain the GI/GII bias observed in shellfish-related outbreaks compared to other outbreaks.

Strain-dependent norovirus bioaccumulation in oysters.

Noroviruses (NoVs) are the main agents of gastroenteritis in humans and the primary pathogens of shellfish-related outbreaks. Some NoV strains bind to shellfish tissues by using carbohydrate structures similar to their human ligands, leading to the hypothesis that such ligands may influence bioaccumulation. This study compares the bioaccumulation efficiencies and tissue distributions in oysters (Crassostrea gigas) of three strains from the two principal human norovirus genogroups. Clear differences between strains were observed. The GI.1 strain was the most efficiently concentrated strain. Bioaccumulation specifically occurred in digestive tissues in a dose-dependent manner, and its efficiency paralleled ligand expression, which was highest during the cold months. In comparison, the GII.4 strain was very poorly bioaccumulated and was recovered in almost all tissues without seasonal influence. The GII.3 strain presented an intermediate behavior, without seasonal effect and with less bioaccumulation efficiency than that of the GI.1 strain during the cold months. In addition, the GII.3 strain was transiently concentrated in gills and mantle before being almost specifically accumulated in digestive tissues. Carbohydrate ligand specificities of the strains at least partly explain the strain-dependent bioaccumulation characteristics. In particular, binding to the digestive-tube-specific ligand should contribute to bioaccumulation, whereas we hypothesize that binding to the sialic acid-containing ligand present in all tissues would contribute to retain virus particles in the gills or mantle and lead to rapid destruction.

[Norovirus and oysters: from the land to the sea!] / Norovirus et huîtres : de la terre à la mer !

Human fecal wastes contain a large variety of viruses that can enter the environment through discharge of waste materials from infected individuals. Despite this high diversity introduced into the environment by human fecal pollution, noroviruses have been recognized as the primary cause of disease in association with consumption of contaminated shellfish. To explain bivalve mollusk contamination, several factors including human epidemiology, virus persistence through sewage treatment plant and shellfish uptake may be suggested. Considering different outbreaks described in the literature, the most common route for transmission is accidental contamination after heavy rainfall, when extra loads cause an overflow and release of untreated sewage into the aquatic environment. Outbreak analysis also demonstrates the impact on shellfish consumption of some viral strain transmission and thus their impact on molecular epidemiology, especially for norovirus. To limit shellfish contamination and thus to protect the consumer, the most desirable and effective option is to reduce the viral input.

Bovine norovirus: carbohydrate ligand, environmental contamination, and potential cross-species transmission via oysters.

Noroviruses (NoV) are major agents of acute gastroenteritis in humans and the primary pathogens of shellfish-related outbreaks. Previous studies showed that some human strains bind to oyster tissues through carbohydrate ligands that are similar to their human receptors. Thus, based on presentation of shared norovirus carbohydrate ligands, oysters could selectively concentrate animal strains with increased ability to overcome species barriers. In comparison with human GI and GII strains, bovine GIII NoV strains, although frequently detected in bovine feces and waters of two estuaries of Brittany, were seldom detected in oysters grown in these estuaries. Characterization of the carbohydrate ligand from a new GIII strain indicated recognition of the alpha-galactosidase (α-Gal) epitope not expressed by humans, similar to the GIII.2 Newbury2 strain. This ligand was not detectable on oyster tissues, suggesting that oysters may not be able to accumulate substantial amounts of GIII strains due to the lack of shared carbohydrate ligand and that they should be unable to contribute to select GIII strains with an increased ability to recognize humans.

Distribution in tissue and seasonal variation of norovirus genogroup I and II ligands in oysters.

Bivalve molluscan shellfish, such as oysters, filter large volumes of water as part of their feeding activities and are able to accumulate and concentrate different types of pathogens, particularly noroviruses, from fecal human pollution. Based on our previous observation of a specific binding of the Norwalk strain (prototype norovirus genogroup I) to the oyster digestive tract through an A-like carbohydrate structure indistinguishable from human blood group A antigen and on the large diversity between strains in terms of carbohydrate-binding specificities, we evaluated the different ligands implicated in attachment to oysters tissues of strains representative of two main genogroups of human norovirus. The GI.1 and GII.4 strains differed in that the latter recognized a sialic acid-containing ligand, present in all tissues, in addition to the A-like ligand of the digestive tract shared with the GI.1 strain. Furthermore, bioaccumulation experiments using wild-type or mutant GI.1 Viruslike particles showed accumulation in hemocytes largely, but not exclusively, based on interaction with the A-like ligand. Moreover, a seasonal effect on the expression of these ligands was detected, most visibly for the GI.1 strain, with a peak in late winter and spring, a period when GI strains are regularly involved in oyster-related outbreaks. These observations may explain some of the distinct epidemiological features of strains from different genogroups.