[en] Sea products are consumed worldwide. Seafood, especially shellfish, is consumed crude or not well cooked therefore they are risky for the development of foodborne diseases. Moreover, these animals filter water and concentrate the microorganisms and the toxins. Risks are multiple : bacteria (Clostridium, Vibrio), viruses (norovirus, hepatitis A) and the biotoxins (paralytic, neurotoxic, diarrhoeic and amnesic) produced by phytoplankton. The European regulation 91/492/EC indicates the microbiological and toxicological criteria for the sale of the shellfish. Nevertheless, in the absence of good diagnosis methods, the viruses were omitted in this regulation. But it is a major cause of toxi-infection due to shellfish consumption. The large number of outbreaks worldwide due to the ingestion of seafood indicates that these ones must be carefully controlled. Therefore, we need powerful diagnosis tools. The aim of this review is to describe the major biological risks (bacteria, viruses, biotoxins) for the human health linked to the consumption of sea food. [fr] Les produits de la mer sont des denrées alimentaires consommées dans le monde entier. Les
fruits de mer et en particulier les mollusques bivalves sont consommés crus ou peu cuits, il en résulte que
ce sont des aliments à risque du point de vue des toxi-infections alimentaires. De plus, ces animaux filtrent
l’eau et concentrent les microorganismes et les toxines. Les risques sont multiples : bactéries (Clostridium,
Vibrio), virus (norovirus, hépatite A) et les biotoxines (paralysante, neurotoxique, diarrhéique, amnésiante)
produites par le phytoplancton. La norme européenne 91/492/EC fixe les critères microbiologiques et toxicologiques
pour la mise en vente de ces produits. Cependant, faute de méthodes diagnostiques fiables, les
virus ont été omis de cette directive. Or, il s’agit d’une cause majeure de toxi-infection due à l’ingestion de
ce type de produits. Le nombre important de foyers épidémiques dans le monde, dus à la consommation
de « fruits de mer» indique que ceux-ci doivent faire l’objet d’une surveillance toute particulière. Mais pour
cela, il faut disposer d’outils diagnostiques performants.
Le but de cette revue est de décrire les principaux dangers biologiques pour la santé humaine (bactéries,
virus, biotoxines) liés à la consommation de fruits de mer.
Disciplines :
Food science
Author, co-author :
China, Bernard; Université de Liège - ULiège - ULG > Sciences des Denrées alimentaires > Microbiologie des Denrées alimentaires
de Schaetzen, Marie-Athénaïs ; Université de Liège - ULiège > Département de sciences des denrées alimentaires > Microbiologie des Denrées alimentaires
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires > Microbiologie des denrées alimentaires
Language :
French
Title :
Shellfish, a dangerous food?
Alternative titles :
[fr] Les mollusques bivalves des aliments dangereux ?
ASSOCIATION FRANCAISE DE NORMALISATION. Norme française NF V 08-060, microbiologie des aliments, dénombrement des coliformes thermotolérants par comptage des colonies obtenues à 44°C. In: Association Française de Normalisation (Ed.), microbiologie alimentaire, Tome 2: méthodes de routine et évaluation d'une méthode alternative. Association Française de Normalisation: Paris, 2002, 155-164.
ARAUJO R. M., PUIG A., LASOBRAS J., LUCENA F., JOFRE J. Phages of enteric bacteria in fresh water with different levels of faecal pollution. J. Appl. Microbiol., 1997, 82, 281-6
AUSTRALIA NEW ZEALAND FOOD AUTHORITY. Shellfish toxins in food. A toxicological review and risk assesment. Technical report series n°14. ANZFA: Canberra, Australie, 2001, 21 p.
BAG P.K., NANDI S., BHACRA R. K., RAMAMURTHY T., BHATTACHARYA S. K., NISHIBUCHI M; HAMABATA T., YAMASAKI S., TAEKEDA Y., NAIR G. B. Clonal diversity among recently emerged strains of Vibrio parahaemolyticus 03:K6 associated with pandemic spread. J. Clin. Microbiol., 1999, 37, 2354-2357.
BRITISH BROADCAST CORPORATION. Vomiting bug cases at record high. BBC news, [en ligne] (3 January 2003). http://news.bbc.co.uk/2/hi/health/2625509.stm Consulté le 17/11/03.
BRYNESTAD S., GRANUM PE. Clostridium perfringens and foodborne infections. Int., J. Food Microbiol., 2002, 74, 195-202.
CANARD B., COLE S.T. Genome organization of the anaerobic pathogen Clostridium perfringens. Proc. Natl. Acad. Sci. USA, 1989, 86, 6676-6680
CENTERS FOR DISEASE CONTROL AND PREVENTION. Vibrio vulnificus infections associated with eating raw oysters-Los Angeles, 1996. MMWR, 1996, 45, 621-624
CHOWDHURY N. R., CHAKRABORTY S ; RAMA-MURTHY T., NISHIBUCHI M., YAMASAKI S., TAKEDA Y., NAIR G. B. Molecular evidence of clonal Vibrio parahaemolyticus pandemic strains. Emerg. Infect. Dis., 2000, 6, 631-636.
COMMUNAUTE EUROPEENNE. Directive du conseil fixant les règles sanitaires régissant la production et la mise sur le marché de mollusques bivalves vivants (91/492/CEE). J. Off. Comm. Europ., 1991, L268, 1-17.
COMMUNAUTE EUROPEENNE. 1999/313/CE: décision du conseil; du 29 avril 1999, relative aux laboratoires de référence pour le contrôle des contaminations bactériologiques et virales des mollusques bivalves. J. Off. Comm. Europ., 1999, L120, 40-41.
CORNILLOT E., SAINT-JOANIS B., DAUBE G., KATAYAMA S.-I., GRANUM P.E., CANARD B., COLE S.T. The enterotoxin gene (cpe) of Clostridium perfringens can be chromosomal or plasmid-borne. Mol. Microbiol., 1995, 15, 639-647
DE SCHRIJVER K., MAES I., DE MAN L., MICHELET J. Une épidé mie d'intoxications diarrhéiques dues aux fruits de mer à Anvers, Belgique. Eurosurveillance, 2002, 7, 139-141.
DEVI S. J., HAYAT U., FRASCH C. E., KREGER A. S., MORRIS J.G. JR. Capsular polysaccharide-protein conjugate vaccines of carbotype 1 Vibrio vulnificus: construction, immunogenicity, and protective efficacy in a murine model. Infect Immun., 1995, 63, 2906-2911
ELLIOT E. L., KVENBERG, J.E. Risk assessement used to evaluate the US position on Listeria monocytogenes in seafood. Internat. J. Food Microbiol., 2000, 62, 253-260.
GALLACHER, S., SMITH E.A. Bacteria and Paralytic Sheelfish toxins. Protist, 1999, 150, 245-255.
GANTZER C., MAUL A., AUDIC J. M., SCHWARTZBROD L. Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages, and Bacteroides fragilis phages in treated wastewater. Appl. Environ. Microbiol., 1998, 64, 4307-12.
GLASS R.I., NOEL J., ANDO T., FANKHAUSER R., BELLIOT G., MOUNTS A., PARASHAR U. D., BRESEE J.S., MONROE S.S. The epidemiology of enteric caliciviruses from humans: a reassessment using new diagnostics. J. Infect. Dis., 2000, 181, S254-261.
GRABOW W.O.K, NEUBRECH T.E., HOLTZHAUSEN C.S. JOFRE J. Bacteroides fragilis and Escherichia coli bacteriophages : excretion by humans and animals. Wat. Sc. Technol., 1995, 31, 223-230.
HACKNEY C. R., DICHARRY A. Seafood borne bacterial pathogens of marine origin. Food Technol., 1988, 42, 104-109.
HAEGHEBAERT S., POPOFF M. R., CARLIER J. P., PAVILLON G., DELAROCQUE-ASTAGNEAU E. Caractéristiques épidémiologiques du botulisme humain en France 1991-2000. [en ligne] (2003) Adresse URL: http://www.invs.sante.fr/publications/2003/snmi/SNMI-G-p 123-196.pdf Consulté le 17/11/03
HATHEWAY C. L. Botulism : the present status of the disease. Curr. Top. Microbiol. Immunol., 1995, 195, 55-75.
HAVELAAR A. H., HOGEBOOM W. M. A method for the enumeration of male-specific bacteriophages in sewage. J. Appl. Bacteriol., 1984, 56, 439-47.
HAVELAAR A. H., HOGEBOOM W. M. Factors affecting the enumeration of coliphages in sewage and sewage-polluted waters. Ant. Van Leeuw., 1983, 49, 387-397.
HLADY W.G., MULLEN R. C., HOPKIN R. S. Vibrio vulnificus from raw oysters. Leading cause of reported deaths from foodborne illness in Florida. J. Flo. Med. Assoc., 1993, 80, 536-538.
HOLMES M.J., TEO S. L. M. Toxic marine dinoflagellates in singapore waters that cause seefood poisonings. Clin. Exp. Pharmacol. Physiol., 2002, 29, 829-836.
HONDA T., IIDA T. The pathogenivity of Vibrio parahaemolyticus and the role of the thermostable direct hemolysin and related hemolysin. Rev. Med. Microbiol., 1993, 4, 106-113.
HONDA T., NI Y. X., MIWATANI T. Purification and characterization of a hemolysin produced by a clinical isolate of Kanagawa phenomenon-negative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. Infect. Immun., 1988, 56, 961-965.
HYYTIÄ-TREES, E. Prevalence, molecular epidemiology and growth of Clostridium botulinum type E in fish and fishery products. (PhD thesis). University of Helsinki: Helsinki, 1999, 73 p.
INTERNATIONAL COMMISSION ON MICROBIOLOGICAL SPECIFICATIONS FOR FOOD. Fish and fish products. In: Bloom, R. (Ed.), microorganisms in foods, 6, microbial ecology of food commodities. Aspen Publication: Gaithersburg, 2000, 131-187.
IGUCHI T, KONDO S, HISATSUNE K. Vibrio parahaemolyticus O serotypes from O1 to O13 all produce R-type lipopolysaccharide: SDS-PAGE and compositional sugar analysis. FEMS Microbiol. Lett., 1995, 130, 287-292
INTERNATIONAL ORGANIZATION FOR STANDARDIZATION. Qualité de l'eau: détection et dénombrement des bactériophages Partie 1: dénombrement des bactériophages ARN F spécifiques. ISO 1075-1., ISO, Genève, Suisse, 1995, 1-12
INTERNATIONAL ORGANIZATION FOR STANDARDIZATION. Qualité de l'eau: détection et dénombrement des bactériophages Partie 2: énumeration des coliphages somatiques. ISO 1075-2, ISO, Genève, Suisse, 1996, 1-15.
INTERNATIONAL ORGANIZATION FOR STANDARDIZATION. Qualité de l'eau: détection et dénombrement des bactériophages - Partie 4: dénombrement des bactériophages infectant Bacteroides fragilis, ISO 10705-4, ISO, Genève, Suisse, 2001, 1-20
JACKSON J. K., MURPHREE R. L., TAMPLIN M. L. Evidence that mortality from Vibrio vulnificus infection results from single strains among heterogeneous populations in shellfish. J Clin Microbiol., 1997, 35, 2098-2101
JOSEPH S. W., COLWELL R. R., KAPER J. B. Vibrio parahaemolyticus and related halophilic Vibrios. Crit. Rev. Microbiol., 1982, 10, 77-124.
KATAYAMA S., DUPUY B., DAUBE G., CHINA B., COLE S.T. Genome mapping of Clostridium perfringens strains with I-CeuI shows many virulence genes to be plasmid-borne. Mol. Gen. Genet., 1996, 251, 720-726.
KINGSLEY D. H., RICHARDS G. P. Persistence of hepatitis A virus in oysters. J. Food Prot., 2003, 66, 331-334.
KOOPMANS M., von BONSDORFF C.H., VINJE J., DE MEDICI D., MONROE S. Foodborne viruses. FEMS Microbiol. Rev., 2002, 26, 187-205.
LABBE R.G. Clostridium perfringens. In: Lind, B., Baird-Parker, T., Gould, G. (eds), The microbiological safety and quality of food. Asppen Publishers: Gaithersburg, 2000, 1110-1135.
LECLERC H., EDBERG S., PIERZO V., DELATTRE J.M. Bacteriophages as indicators of enteric viruses and public health risk in groundwaters. J. Appl. Microbiol., 2000, 88, 5-21.
LEE C. Y., PANICKER G., BEJ A. K. Detection of pathogenic bacteria in shellfish using multiplex PCR followed by CovaLink NH microwell plate sandwich hybridization. J. Microbiol. Meth., 2003, 53, 199-209
LEMOINE T., GERMANETTO P., GIRAUD P. Toxi-infection alimentaire collective a Vibrio parahaemolyticus. [en ligne] (26/04/1999) Adresse URL: http://www.invs.sante.fr/beh/1999/9910 Consulté le 21/11/03
LOPALCO P.L., MALFAIT P., SALMASO S., GERMINARIO C., QUARTO M., BARBUTIL S. Une épidémie d'hépatite A persistante en Italie dans les Pouilles, 1996: suivi épidémiologique. Eurosurveillance, 1997, 2, 31-33.
LUIZZI G. D., SALLABANDA A., DIBRA A., KACARRICY E., SHAPO L. Choléra dans la région méditeranéenne : une épidémie en Albanie. Eurosurveillance, 1995, 0, 1-2.
MATSUMOTO C., OKUDA J., ISHIBASHI M., IWANAGA M., GARG P., RAMMAMURTHY T., WONG H. C., DEPAOLA A., KIM Y. B., ALBERT M. J., NISHIBUCHI M. Pandemic sread of an 03 :K6 clone of Vibrio parahaemolyticus and emerge of related strains evidenced by arbitrariky primed PCR and toxRS sequences analyses. J. Clin. Microbiol., 2000, 38, 578-585.
MIYOSHI S., OH E. G., HIRATA K., SHINODA S. Exocellular toxic factors produced by Vibrio vulnificus. J. Toxicol.-Toxin Rev., 1993, 12, 253-288.
MUNIAIN-MUJIKA I., CALVO M., LUCENA F., GIRONES R. Comparative analysis of viral pathogens and potential indicators in shellfish. Intern. J. Food Microbiol., 2003, 83, 75-85.
NISHIBUCHI M, KAPER J. B. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infect. Immun., 1995, 63, 2093-9.
OKUDA J., ISHIBASHI M., HAYAKAWA E., NISHINO T., TAKEDA Y., MUKHOPADHYAY A. K., GARG S., BHATTACHARYA SK, NAIR GB, NISHIBUCHI M. Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J. Clin. Microbiol., 1997, 35, 3150-3155.
OKUJO N., AKIYAMA T., MIYOSHI S., SHINODA S., YAMAMOTO S. Involvement of vulnibactin and exocellular protease in utilization of transferrin- and lactoferrinbound iron by Vibrio vulnificus. Microbiol Immunol., 1996, 40, 595-598
OLIVER J.D., KAPER J. B. Vibrio species. In: Doyle M. P., Beucat L. R., Montville, T.J. (Eds.), Food microbiology. ASM Press: Washington, 1997, 228-264.
PETERSON K. M., MEKALANOS J. J. Characterization of the Vibrio cholerae toxR regulon: identification of novel genes involved in intestinal colonization. Infect. Immun., 1988, 56, 288-289.
PETERSON K.M. Molecular pathogenesis of Vibrio Infections. In: Cary J.W., Linz J.E., Bhatnagar D. (Eds), Microbial foodborne diseases, mechanisms of pathogenesis and toxin synthesis. Technomic publishing Co: Lancaster, 2000, 157-185.
PETIT L., GIBERT M., POPOFF M. R. Clostridium perfringens: toxinotype and genotype. Trends Microbiol., 1999, 7, 104-110.
POTASMAN I., PAZ A., ODEH M. Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis., 2002, 35, 921-928.
QUILLIAM M. A. Phycotoxins. J. AOAC Int., 1999, 82, 773-81
RAIMONDI F., KAO J. P., KAPER J. B., GUANDALINI S., FASANO A. Calcium-dependent intestinal chloride secretion by Vibrio parahaemolyticus thermostable direct hemolysin in a rabbit model. Gastroenteroogy., 1995, 109, 381-386
RAIMONDI F., KAO J.P.Y., FIORENTINI C., FABBRI A., DONELLI G., GASPARINI N., RUBINO A., FASANO A. Enterotoxicity and cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin in in vitro systems. Infect. Immun., 2000, 68, 3180-3185.
ROBINSON E., WILES K.G., SCHWARZ J. R. Vibrio vulnificus infections: Texas 2000. Dis. Prevent. News, 2000, 60, 1-4.
ROCOURT, J., JACQUET CH., REILLY, A. Epidemiology of human listeriosis and seafoods. Int. J. Food Microbiol., 2000, 62, 197-209.
RONVEAUX O., VOS D., BOSMAN A., BRANDWIJK K., VINJE K., KOOPMANS M., REINTJES R. Epidémie de gastroentérite à virus de Norwalk-like dans un hôpital de long et moyen séjour à Rotterdam. Eurosureillance., 2000, 5, 54-57.
SANCHEZ, G., PINTO, R. M., VANACLOCHA, H., BOSCH, A. Molecular characterization of hepatitis A virus isolates from a transcontiental shellfish-borne outbreak. J. Clin. Microbiol., 2002, 40, 4148-4155.
SANTE CANADA. Direction générale de la population et de la santé publique. Fiche technique santé-sécurité- matière infectieuse, fiche n°75, le virus de l'Hépatite A. [en ligne] (2001). Adresse URL: http://www.hc-sc.gc.ca/pphb-dgspsp/msds-ftss/ msds75e.html Consulté le 17/11/03.
SCIPIONI A., DAUBE G., THIRY E. La contamination de l'eau et des aliments par les virus pathogènes pour l'homme. Ann. Méd. Vét., 2000, 144, 207-211.
SMITH DEWAAL C., BARLOW K, ALDERTON L., JACOBSON M. F. Outbreak alert!: Center for Sciences in Public Interest (CSPI): Washington, 2001, 48 p.
SUMMER J., ROSS T. A semi-quantitative seafood safety risk assessement. Int. J. Food Microbiol., 2002, 77, 55-59.
TARTERA C., LUCENA F., JOFRE J. Human origin of Bacteroides fragilis bacteriophages present in the environment. Appl. Environ. Microbiol., 1989, 55, 2696-2701.
TRUCKSIS M., GALEN J. E., MICHALSKI J., FASANO A., KAPER J. B. Accessory cholera enterotoxin (Ace), the third toxin of a Vibrio cholerae virulence cassette. Proc. Natl. Acad. Sci. USA, 1993, 90, 5267-5271.
WALDOR M.K., MEKALANOS J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Nature, 1996, 272, 1910-1914.
WERKER D. H., KING A. S., KELLY M. T., MATHESON T. Le choléra en Colombie britannique. RMTC, 1996, 22, 75-78
WONG H. C., LIN C. H. Evaluation of typing of Vibrio parahaemolyticus by three PCR methods using specific primers. J. Clin. Microbiol., 2001, 39, 4233-4240.
WORM H. C., Van Der POEL W. H. M., BRANDSTATTER G. Hepatitis E: an overview. Microb. Infect., 2002, 4, 657-666.
