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      Identifying drivers of fox and cat faecal deposits in kitchen gardens in order to evaluate measures for reducing contamination of fresh fruit and vegetables

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          Abstract

          Preventing foodborne pathogen contamination of raw fruit and vegetables in the field is critically important for public health. Specifically, it involves preventing faecal deposit by wildlife or domestic animals in fields of crops and kitchen gardens. The present study aims to identify the drivers of fox, dog and cat faecal deposits in kitchen gardens in order to mitigate the risk of contamination of raw produce with parasites shed in carnivore faeces. The focus was on Echinococcus multilocularis, ranked highest in the importance of foodborne parasites in Europe, but attention was also paid to other parasites of major concern - Toxoplasma gondii and Toxocara spp. During the winters of 2014 to 2016, faecal samples were collected from 192 kitchen gardens located in north-eastern France. From these samples, 77% contained scat of carnivores. Molecular analyses revealed that 59% of the 1016 faeces collected were from cats, 31% from foxes, and 10% from dogs. The ease of accessibility to kitchen gardens, the presence of food in the vicinity, and the composition of the surrounding vegetation were used to explain the distribution of fox and cat faeces. Generalized Linear Mixed Effects modelling showed that: i) fencing was not efficient in reducing cat faecal deposits, but drastically decreases those of foxes; ii) the abundance of Microtus sp. indicates a reason for the presence of both fox and cat faecal deposits, iii) the abundance of Arvicola terrestris, the proximity of fruit trees or farms and the predominance of forest and grassland around the village are all drivers of fox faecal deposits. These results point to the importance of fencing around kitchen gardens located in E. multilocularis endemic areas, particularly those surrounded by forest and grassland or close to fruit trees or farms.

          Highlights

          • 192 kitchen gardens sampled 6 times over 2 winters, 1016 carnivore faeces collected.

          • Fencing, food and vegetation cover tested as explanatory factors for faeces location.

          • Numerous cat faeces, even in enclosed gardens. Microtus sp. drives their deposit.

          • Garden accessibility, food and vegetation cover drive the faecal deposits of foxes.

          • Fencing off kitchen gardens should be encouraged in E. multilocularis endemic areas.

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          Most cited references52

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          Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern.

          Echinococcosis in humans is a zoonotic infection caused by larval stages (metacestodes) of cestode species of the genus Echinococcus. Cystic echinococcosis (CE) is caused by Echinococcus granulosus, alveolar echinococcosis (AE) is caused by E. multilocularis, and polycystic forms are caused by either E. vogeli or E. oligarthrus. In untreated cases, AE has a high mortality rate. Although control is essentially feasible, CE remains a considerable health problem in many regions of the northern and southern hemispheres. AE is restricted to the northern hemisphere regions of North America and Eurasia. Recent studies have shown that E. multilocularis, the causative agent of AE, is more widely distributed than previously thought. There are also some hints of an increasing significance of polycystic forms of the disease, which are restricted to Central and South America. Various aspects of human echinococcosis are discussed in this review, including data on the infectivity of genetic variants of E. granulosus to humans, the increasing invasion of cities in Europe and Japan by red foxes, the main definitive hosts of E. multilocularis, and the first demonstration of urban cycles of the parasite. Examples of emergence or reemergence of CE are presented, and the question of potential spreading of E. multilocularis is critically assessed. Furthermore, information is presented on new and improved tools for diagnosing the infection in final hosts (dogs, foxes, and cats) by coproantigen or DNA detection and the application of molecular techniques to epidemiological studies. In the clinical field, the available methods for diagnosing human CE and AE are described and the treatment options are summarized. The development of new chemotherapeutic options for all forms of human echinococcosis remains an urgent requirement. A new option for the control of E. granulosus in the intermediate host population (mainly sheep and cattle) is vaccination. Attempts are made to reduce the prevalence of E. multilocualaris in fox populations by regular baiting with an anthelmintic (praziquantel). Recent data have shown that this control option may be used in restricted areas, for example in cities, with the aim of reducing the infection risk for humans.
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            Toxoplasmosis - a waterborne zoonosis.

            J Dubey (2004)
            Humans become infected with Toxoplasma gondii mainly by ingesting uncooked meat containing viable tissue cysts or by ingesting food or water contaminated with oocysts from the feces of infected cats. Circumstantial evidence suggests that oocyst-induced infections in humans are clinically more severe than tissue cyst-acquired infections. Until recently, water-borne transmission of T. gondii was considered uncommon but a large human outbreak linked to contamination of a municipal water reservoir in Canada by wild felids and the widespread infection by marine mammals in the USA provide reasons to question this view. The present paper reviews information on the biology of oocyst-induced infections of T. gondii in humans and animals and examines possible importance of transmission by water.
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              Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review

              Foodborne illness resulting from the consumption of contaminated fresh produce is a common phenomenon and has severe effects on human health together with severe economic and social impacts. The implications of foodborne diseases associated with fresh produce have urged research into the numerous ways and mechanisms through which pathogens may gain access to produce, thereby compromising microbiological safety. This review provides a background on the various sources and pathways through which pathogenic bacteria contaminate fresh produce; the survival and proliferation of pathogens on fresh produce while growing and potential methods to reduce microbial contamination before harvest. Some of the established bacterial contamination sources include contaminated manure, irrigation water, soil, livestock/ wildlife, and numerous factors influence the incidence, fate, transport, survival and proliferation of pathogens in the wide variety of sources where they are found. Once pathogenic bacteria have been introduced into the growing environment, they can colonize and persist on fresh produce using a variety of mechanisms. Overall, microbiological hazards are significant; therefore, ways to reduce sources of contamination and a deeper understanding of pathogen survival and growth on fresh produce in the field are required to reduce risk to human health and the associated economic consequences.
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                Author and article information

                Contributors
                Journal
                Food Waterborne Parasitol
                Food Waterborne Parasitol
                Food and Waterborne Parasitology
                Elsevier
                2405-6766
                29 December 2018
                March 2019
                29 December 2018
                : 14
                : e00034
                Affiliations
                [a ]University of Reims Champagne-Ardenne, SFR Cap Santé, EA 7510 ESCAPE, 51092 Reims cedex, France
                [b ]University of Reims Champagne-Ardenne, CERFE, 08240 Boult-aux-Bois, France
                [c ]French Establishment for Fighting Zoonoses (ELIZ), Domaine de Pixérécourt, 54220 Malzéville, France
                [d ]EcoDataDesign, 25000 Besançon, France
                [e ]ANSES, Nancy Laboratory for Rabies and Wildlife, National Reference Laboratory for Echinococcus spp., Wildlife Eco-epidemiology and Surveillance Unit, 54220 Malzéville, France
                [f ]CROC, Carnivore Research and Observation Center, 57590 Lucy, France
                [g ]University Hospital of Reims, Department of Parasitology-Mycology, National Reference Center for Toxoplasma, 51092 Reims cedex, France
                Author notes
                [* ]Corresponding author at: University of Reims Champagne-Ardenne, SFR Cap Santé, EA 7510 ESCAPE, 51092 Reims cedex, France. matthieu.Bastien@ 123456e-l-i-z.com
                Article
                S2405-6766(18)30024-6 e00034
                10.1016/j.fawpar.2018.e00034
                7034018
                32095604
                11eafb4d-6bf2-47aa-97fb-d650e2179d69
                © 2019 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 17 August 2018
                : 22 December 2018
                : 28 December 2018
                Categories
                Article

                environmental contamination,foodborne parasites,echinococcus multilocularis,toxoplasma gondii,toxocara sp.

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