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Applied and Environmental Microbiology, March 2003, p. 1556-1563, Vol. 69, No. 3
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.3.1556-1563.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Evaluation of Potential Indicators of Viral Contamination in Shellfish and Their Applicability to Diverse Geographical Areas

M. Formiga-Cruz,1 A. K. Allard,2 A.-C. Conden-Hansson,2 K. Henshilwood,3 B. E. Hernroth,4 J. Jofre,1 D. N. Lees,3 F. Lucena,1 M. Papapetropoulou,5 R. E. Rangdale,3 A. Tsibouxi,5 A. Vantarakis,5 and R. Girones1*

Biology School, University of Barcelona, Barcelona, Spain,1 Umeå University Hospital, Umeå,2 Kristinebergs Marine Research Station, Fiskebäckskil, Sweden,4 Centre for Environment, Fisheries and Aquaculture Science, Weymouth, United Kingdom,3 School of Medicine, University of Patras, Patras, Greece5

Received 5 July 2002/ Accepted 14 November 2002

The distribution of the concentration of potential indicators of fecal viral pollution in shellfish was analyzed under diverse conditions over 18 months in diverse geographical areas. These microorganisms have been evaluated in relation to contamination by human viral pathogens detected in parallel in the analyzed shellfish samples. Thus, significant shellfish-growing areas from diverse countries in the north and south of Europe (Greece, Spain, Sweden, and the United Kingdom) were defined and studied by analyzing different physicochemical parameters in the water and the levels of Escherichia coli, F-specific RNA bacteriophages, and phages infecting Bacteroides fragilis strain RYC2056 in the shellfish produced, before and after depuration treatments. A total of 475 shellfish samples were studied, and the results were statistically analyzed. According to statistical analysis, the presence of human viruses seems to be related to the presence of all potential indicators in the heavily contaminated areas, where E. coli would probably be suitable as a fecal indicator. The F-RNA phages, which are present in higher numbers in Northern Europe, seem to be significantly related to the presence of viral contamination in shellfish, with a very weak predictive value for hepatitis A virus, human adenovirus, and enterovirus and a stronger one for Norwalk-like virus. However, it is important to note that shellfish produced in A or clean B areas can sporadically contain human viruses even in the absence of E. coli or F-RNA phages. The data presented here will be useful in defining microbiological parameters for improving the sanitary control of shellfish consumed raw or barely cooked.


* Corresponding author. Mailing address: Biology School, University of Barcelona, Av. Diagonal, 645, 08028-Barcelona, Spain. Phone: 34-93-402-14-83. Fax: 34-93-411-05-92. E-mail: rosina{at}bio.ub.es.


Applied and Environmental Microbiology, March 2003, p. 1556-1563, Vol. 69, No. 3
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.3.1556-1563.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.




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