Prevalence, Molecular Identification, and Risk Factors for Cryptosporidium Infection in Edible Marine Fish: A Survey Across Sea Areas Surrounding France

Type Article
Date 2019-05
Language English
Author(s) Certad Gabriela1, 2, Follet Jérôme3, 4, Gantois Nausicaa1, Hammouma-Ghelboun Ourida3, Guyot Karine1, Benamrouz-Vanneste Sadia1, 5, Fréalle Emilie1, Seesao Yuwalee1, Delaire Baptiste6, Creusy Colette6, Even Gaël7, 8, Verrez-Bagnis VeroniqueORCID9, Ryan Una10, Gay Mélanie11, Aliouat-Denis Cécile1, Viscogliosi Eric1
Affiliation(s) 1 : CNRS, Inserm, CHU Lille, U1019 – UMR 8204 – CIIL – Centre d’Infection et d’Immunité de Lille, Institut Pasteur de Lille, Université de Lille, Lille, France
2 : Délégation à la Recherche Clinique et à l’innovation, Groupement des Hôpitaux de l’Institut Catholique de Lille, Lille, France
3 : ISA-YNCREA Hauts-de-France, Lille, France
4 : CNRS, ISEN, UMR 8520 – IEMN, Université de Lille, Lille, France
5 : Laboratoire Ecologie et Biodiversité, Faculté de Gestion Economie et Sciences, Institut Catholique de Lille, Lille, France
6 : Service d’Anatomie et de Cytologie Pathologiques, Groupement des Hôpitaux de l’Institut Catholique de Lille, Lille, France
7 : Gènes Diffusion, Douai, France
8 : PEGASE-Biosciences, Institut Pasteur de Lille, Lille, France
9 : Ifremer, Laboratoire Ecosystèmes Microbiens et Molécules Marines pour les Biotechnologies, Nantes, France
10 : Centre for Sustainable Aquatic Ecosystems, College of Science, Health, Engineering and Education, Murdoch University, Perth, WA, Australia
11 : Laboratory for Food Safety, French Agency for Food, Environmental and Occupational Health and Safety (ANSES), Boulogne-sur-mer, France
Source Frontiers In Microbiology (1664-302X) (Frontiers Media SA), 2019-05 , Vol. 10 , N. 1037 , P. 15p.
DOI 10.3389/fmicb.2019.01037
WOS© Times Cited 23
Keyword(s) Cryptosporidium, edible marine fish, 18S rRNA gene, gp60, molecular epidemiology, phylogeny, novel genotypes, European seas

Cryptosporidium, a zoonotic pathogen, is able to infect a wide range of hosts including wild and domestic animals, and humans. Although it is well known that some parasites are both fish pathogens and recognized agents of zoonosis with a public health impact, little information is available concerning the prevalence of Cryptosporidium in wild aquatic environments. To evaluate the prevalence of Cryptosporidium spp. in commercially important edible marine fish in different European seas (English channel, North sea, Bay of Biscay, Celtic sea and Mediterranean sea), 1,853 specimens were collected as part of two surveys. Nested PCR followed by sequence analysis at the 18S rRNA gene locus was used to identify Cryptosporidium spp. The overall prevalence of Cryptosporidium spp. in sampled fish reached 2.3% (35 out of 1,508) in a first campaign and 3.2% (11 out of 345) in a second campaign. Sequence and phylogenetic analysis of positive samples identified Cryptosporidium parvum (n = 10) and seven genotypes which exhibited between 7.3 and 10.1% genetic distance from C. molnari, with the exception of one genotype which exhibited only 0.5–0.7% genetic distance from C. molnari. Among 31 analyzed fish species, 11 (35.5%) were identified as potential hosts for Cryptosporidium. A higher prevalence of Cryptosporidium spp. was observed in larger fish, in fish collected during the spring-summer period, and in those caught in the North East Atlantic. Pollachius virens (saithe) was the most frequently Cryptosporidium positive species. In fish infected by other parasites, the risk of being Cryptosporidium positive increased 10-fold (OR: 9.95, CI: 2.32–40.01.04, P = 0.0002). Four gp60 subtypes were detected among the C. parvum positive samples: IIaA13G1R1, IIaA15G2R1, IIaA17G2R1, and IIaA18G3R1. These C. parvum subtypes have been previously detected in terrestrial mammals and may constitute an additional source of infection for other animals and in particular for humans. Microscopical examination of histological sections confirmed the presence of round bodies suggestive of the development of C. parvum within digestive glands. We report herein the first epidemiological and molecular data concerning the detection of Cryptosporidium in edible marine fish in European seas surrounding France broadening its host range and uncovering potential novel infection routes.

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FIGURE S1 | Hierarchical cluster analysis was used to define variables (R stats package). Five groups were defined ranging from 1-smallest fishes to 5-largest fishes. 124 KB Open access
FIGURE S2 | The number of base substitutions per site from between sequences are shown. Analyses were conducted using the Tamura 3-parameter model. The analysis involved 29 nucleotide sequences. ... 133 KB Open access
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Certad Gabriela, Follet Jérôme, Gantois Nausicaa, Hammouma-Ghelboun Ourida, Guyot Karine, Benamrouz-Vanneste Sadia, Fréalle Emilie, Seesao Yuwalee, Delaire Baptiste, Creusy Colette, Even Gaël, Verrez-Bagnis Veronique, Ryan Una, Gay Mélanie, Aliouat-Denis Cécile, Viscogliosi Eric (2019). Prevalence, Molecular Identification, and Risk Factors for Cryptosporidium Infection in Edible Marine Fish: A Survey Across Sea Areas Surrounding France. Frontiers In Microbiology, 10(1037), 15p. Publisher's official version : , Open Access version :