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      Detection of Echinococcus multilocularis and other foodborne parasites in fox, cat and dog faeces collected in kitchen gardens in a highly endemic area for alveolar echinococcosis Translated title: Détection d’ Echinococcus multilocularis et autres parasites transmissibles par l’alimentation dans des fèces de renards, chats et chiens récoltées dans des jardins potagers situés en aire de haute endémie d’échinococcose alvéolaire

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          Echinococcus multilocularis, Toxoplasma gondii and Toxocara spp. are foodborne parasites whose eggs or oocysts are spread in the environment via canid or felid faeces. They can cause infections in humans following the raw consumption of contaminated fruit or vegetables. In this study, their occurrence was investigated by quantitative polymerase chain reaction (qPCR) in 254 carnivore faeces deposited in 94 kitchen gardens of northeastern France that were sampled between two and six times from October 2011 to April 2013. Less than 25% of the sampled kitchen gardens contained more than 75% of the collected faeces. Of the 219 faeces that could be attributed to an emitter, cat accounted for 58%, fox for 32% and dog for 10%. Echinococcus multilocularis was detected in 35%, 11% and 7% of fox, dog and cat faeces, respectively, and Toxocara spp. in 33%, 12% and 5.5% of cat, fox and dog faeces, respectively. Toxoplasma gondii was detected in 2/125 cat faeces and 2/21 dog faeces. The 34 faeces that tested positive for E. multilocularis were found in only 19 out of the 94 sampled kitchen gardens, and the 40 faeces that tested positive for Toxocara spp. were found in 28 of them. Consequently, some kitchen gardens appeared particularly at risk of human exposure to foodborne parasites, including E. multilocularis responsible for alveolar echinococcosis (AE), which is a serious zoonosis. In endemic areas, kitchen garden owners should be informed about the zoonotic risk linked to carnivore faeces deposits and encouraged to set up preventive measures.

          Translated abstract

          Echinococcus multilocularis, Toxoplasma gondii et Toxocara spp. sont des parasites transmissibles par l’alimentation dont les œufs ou oocystes sont répandus dans l’environnement avec les fèces de canidés ou félidés. Ils peuvent être responsables d’infections humaines suite à la consommation crue de fruits et légumes contaminés. Leur présence a été recherchée par qPCR dans 254 fèces de carnivores déposées dans 94 potagers du nord-est de la France, échantillonnés deux à six fois entre octobre 2011 et avril 2013. Moins de 25 % de ces potagers contenaient plus de 75 % des fèces collectées. Parmi les 219 fèces pour lesquelles l’émetteur a pu être identifié, 58 % étaient de chat, 32 % de renard et 10 % de chien. Echinococcus multilocularis a été détecté dans 35 %, 11 % et 7 % des fèces de renard, chien et chat respectivement et Toxocara spp. dans 33 %, 12 % et 5.5 % des fèces de chat, renard et chien, respectivement. Toxoplasma gondii a été détecté dans 2/125 fèces de chat et 2/21 fèces de chien. Les 34 fèces testées positives pour E. multilocularis ont été trouvées dans seulement 19 des 94 potagers échantillonnés et les 40 fèces testées positives pour Toxocara spp. dans 28 d’entre eux. En conséquence, certains potagers apparaissent particulièrement à risque d’exposition humaine aux parasites transmissibles par l’alimentation et, notamment, à E. multilocularis responsable de l’échinococcose alvéolaire qui est une grave zoonose. En zone d’endémie, les propriétaires de potagers devraient être informés du risque zoonotique lié au dépôt de fèces de carnivores et encouragés à prendre des mesures de prévention.

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          Most cited references 51

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          Emerging food-borne parasites.

           P DORNY,  N Praet,  N Deckers (2009)
          Parasitic food-borne diseases are generally underrecognised, however they are becoming more common. Globalization of the food supply, increased international travel, increase of the population of highly susceptible persons, change in culinary habits, but also improved diagnostic tools and communication are some factors associated with the increased diagnosis of food-borne parasitic diseases worldwide. This paper reviews the most important emerging food-borne parasites, with emphasis on transmission routes. In a first part, waterborne parasites transmitted by contaminated food such as Cyclospora cayetanensis, Cryptosporidium and Giardia are discussed. Also human fasciolosis, of which the importance has only been recognised in the last decades, with total numbers of reported cases increasing from less than 3000 to 17 million, is looked at. Furthermore, fasciolopsiosis, an intestinal trematode of humans and pigs belongs to the waterborne parasites as well. A few parasites that may be transmitted through faecal contamination of foods and that have received renewed attention, such as Toxoplasma gondii, or that are (re-)emerging, such as Trypanosoma cruzi and Echinococcus spp., are briefly reviewed. In a second part, meat-borne parasite infections are reviewed. Humans get infected by eating raw or undercooked meat infected with cyst stages of these parasites. Meat inspection is the principal method applied in the control of Taenia spp. and Trichinella spp. However, it is often not very sensitive, frequently not practised, and not done for T. gondii and Sarcocystis spp. Meat of reptiles, amphibians and fish can be infected with a variety of parasites, including trematodes (Opisthorchis spp., Clonorchis sinensis, minute intestinal flukes), cestodes (Diphyllobothrium spp., Spirometra), nematodes (Gnathostoma, spp., anisakine parasites), and pentastomids that can cause zoonotic infections in humans when consumed raw or not properly cooked. Another important zoonotic food-borne trematode is the lungfluke (Paragonimus spp.). Traditionally, these parasitic zoonoses are most common in Asia because of the particular food practices and the importance of aquaculture. However, some of these parasites may emerge in other continents through aquaculture and improved transportation and distribution systems. Because of inadequate systems for routine diagnosis and monitoring or reporting for many of the zoonotic parasites, the incidence of human disease and parasite occurrence in food is underestimated. Of particular concern in industrialised countries are the highly resistant waterborne protozoal infections as well as the increased travel and immigration, which increase the exposure to exotic diseases. The increased demand for animal proteins in developing countries will lead to an intensification of the production systems in which the risk of zoonotic infections needs to be assessed. Overall, there is an urgent need for better monitoring and control of food-borne parasites using new technologies.
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            Emerging parasite zoonoses associated with water and food.

            The environmental route of transmission is important for many protozoan and helminth parasites, with water, soil and food being particularly significant. Both the potential for producing large numbers of transmissive stages and their environmental robustness, being able to survive in moist microclimates for prolonged periods of time, pose a persistent threat to public and veterinary health. The increased demands on natural resources increase the likelihood of encountering environments and produce contaminated with parasites. For waterborne diseases, the protozoa, Cryptosporidium, Giardia and Toxoplasma, are the most significant causes, yet, with the exception of Toxoplasma, the contribution of zoonotic transmission remains unclear due to the absence of 'standardised' methods. The microsporidia have been documented in one waterborne outbreak, but the role of animals as the cause of contamination was not elucidated. In foods, surface contamination is associated with the faecal-oral pathogens, and some data are available to indicate that animal wastes remain an important source of contamination (e.g. cattle faeces and apple cider outbreaks), however, further work should focus on examining the source of contamination on fruit and vegetables. Increasing recognition of the burden of human fascioliasis has occurred; it is now recognised as an emerging zoonosis by the WHO. Toxoplasma, Trichinella and Taenia spp. remain important meatborne parasites, however, others, including Pleistophora-like microsporidians may be acquired from raw or lightly cooked fish or crustaceans. With increased international travel, the public health importance of the foodborne trematodiases must also be realised. Global sourcing of food, coupled with changing consumer vogues, including the consumption of raw vegetables and undercooking to retain the natural taste and preserve heat-labile nutrients, can increase the risk of foodborne transmission. A greater awareness of parasite contamination of our environment and its impact on health has precipitated the development of better detection methods. Robust, efficient detection, viability and typing methods are required to assess risks and to further epidemiological understanding.
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              Comparison of two DNA targets for the diagnosis of Toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes

              Background Toxoplasmosis is an infectious disease caused by the parasitic protozoan Toxoplasma gondii. It is endemic worldwide and, depending on the geographic location, 15 to 85% of the human population are asymptomatically infected. Routine diagnosis is based on serology. The parasite has emerged as a major opportunistic pathogen for immunocompromised patients, in whom it can cause life-threatening disease. Moreover, when a pregnant woman develops a primary Toxoplasma gondii infection, the parasite may be transmitted to the fetus and cause serious damnage. For these two subpopulations, a rapid and accurate diagnosis is required to initiate treatment. Serological diagnosis of active infection is unreliable because reactivation is not always accompanied by changes in antibody levels, and the presence of IgM does not necessarily indicate recent infection. Application of quantitative PCR has evolved as a sensitive, specific, and rapid method for the detection of Toxoplasma gondii DNA in amniotic fluid, blood, tissue samples, and cerebrospinal fluid. Methods Two separate, real-time fluorescence PCR assays were designed and evaluated with clinical samples. The first, targeting the 35-fold repeated B1 gene, and a second, targeting a newly described multicopy genomic fragment of Toxoplasma gondii. Amplicons of different intragenic copies were analyzed for sequence heterogeneity. Results Comparative LightCycler experiments were conducted with a dilution series of Toxoplasma gondii genomic DNA, 5 reference strains, and 51 Toxoplasma gondii-positive amniotic fluid samples revealing a 10 to 100-fold higher sensitivity for the PCR assay targeting the newly described 529-bp repeat element of Toxoplasma gondii. Conclusion We have developed a quantitative LightCycler PCR protocol which offer rapid cycling with real-time, sequence-specific detection of amplicons. Results of quantitative PCR demonstrate that the 529-bp repeat element is repeated more than 300-fold in the genome of Toxoplasma gondii. Since individual intragenic copies of the target are conserved on sequence level, the high copy number leads to an ultimate level of analytical sensitivity in routine practice. This newly described 529-bp repeat element should be preferred to less repeated or more divergent target sequences in order to improve the sensitivity of PCR tests for the diagnosis of toxoplasmosis.

                Author and article information

                EDP Sciences
                26 July 2017
                : 24
                : ( publisher-idID: parasite/2017/01 )
                [1 ] University of Reims Champagne-Ardenne, SFR Cap Santé, EA 3800 PROTAL 51092 Reims cedex France
                [2 ] University of Reims Champagne-Ardenne, CERFE 08240 Boult-aux-Bois France
                [3 ] French Institute for Fighting Zoonoses (ELIZ), Domaine de Pixéricourt 54220 Malzéville France
                [4 ] University Hospital of Reims, Department of Parasitology-Mycology 51092 Reims cedex France
                [5 ] University of Bourgogne Franche-Comté, Laboratory of Chrono-environment, UMR UFC/CNRS 6249 affi. INRA 25030 Besançon France
                [6 ] University Hospital of Besançon, Department of Parasitology-Mycology 25030 Besançon France
                Author notes
                parasite170062 10.1051/parasite/2017031
                © M.-L. Poulle et al., published by EDP Sciences, 2017

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 2, Tables: 3, Equations: 0, References: 55, Pages: 11
                Research Article


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