Folia Parasitologica 65:002 (2018) | DOI: 10.14411/fp.2018.002
High density of fox and cat faeces in kitchen gardens and resulting rodent exposure to Echinococcus multilocularis and Toxoplasma gondii
- 1 University of Reims Champagne-Ardenne, EA 3800 PROTAL, SFR Cap Santé, Reims cedex, France;
- 2 University of Reims Champagne-Ardenne, CERFE, Boult-aux-Bois, France;
- 3 French Establishment for Fighting Zoonoses (ELIZ), Domaine de Pixerécourt, Malzéville, France;
- 4 EcoDataDesign, France;
- 5 ANSES, Nancy Laboratory for Rabies and Wildlife, National Reference Laboratory for Echinococcus spp., Wildlife Eco-epidemiology and Surveillance Unit, Malzéville, France;
- 6 Research and Observation Centre on Carnivores (CROC), Lucy, France;
- 7 University Hospital of Reims, Department of Parasitology-Mycology, National Reference Centre on Toxoplasma, Reims cedex, France
The faeces of the red fox, Vulpes vulpes (Linnaeus), and the domestic cat, Felis catus (Linnaeus), can be responsible for spreading eggs of Echinococcus multilocularis Leuckart, 1863 and oocysts of Toxoplasma gondii (Nicolle et Manceaux, 1908) into the environment. The accidental ingestion of these eggs or oocysts, through consumption of raw fruits or vegetables grown in or in contact with contaminated soil, can lead to alveolar echinococcosis (AE) or toxoplasmosis in humans. The present study provides a quantitative assessment of the faecal deposition by foxes and cats in kitchen gardens where fruits and vegetables are grown and its consequences for zoonosis transmission. The density of definitive host faeces is considered as one of the main factors in infection risk for intermediate hosts. The density of fox and cat faeces, as well as the prevalence of both AE and toxoplasmosis in rodent populations (contaminated by ingestion of eggs or oocysts), were compared within and outside kitchen gardens. Our results showed that the mean density of fox faeces did not significantly differ between kitchen gardens and habitat edges (0.29 ± 0.04 faeces/m2 vs 0.22 ± 0.02 faeces/m2), the latter being known as an area of high fox faeceal densities. The density of cat faeces was significantly higher within the kitchen garden than outside (0.86 ± 0.22 faeces/m2 vs 0.04 ± 0.02 faeces/m2). The sampled kitchen gardens might therefore be considered as possible hotspots for both fox and cat defecation. Of the 130 rodents trapped, 14% were infected by at least one species of fox or cat intestinal parasite. These rodents were significantly more often infected when they were exposed to a kitchen garden. These results suggest that the deposit of fox and cat faeces in kitchen gardens would significantly impact the risk of human exposure to E. multilocularis and T. gondii. and should be prevented using effective means.
Keywords: rodent prevalence, food-borne agents, fox faeces density, cat faeces density, parasite transmission risk
Received: January 18, 2017; Accepted: December 23, 2017; Published online: March 8, 2018 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Afonso E., Lemoine M., Poulle M.-L., Ravat M.-C., Romand S., Thulliez P., Villena I., Aubert D., Rabilloud M., Riche B., Gilot-Fromont E. 2008: Spatial distribution of soil contamination by Toxoplasma gondii in relation to cat defecation behaviour in an urban area. Int. J. Parasitol. 38: 1017-1023.
Go to original source...
Go to PubMed... - Agresti A., Coull B.A. 1998: Approximate is better than "exact" for interval estimation of binomial proportions. Am. Stat. 52: 119-126.
Go to original source... - Bivand R., Keitt T., Rowlingson B. 2014: rgdal: Bindings for the geospatial data abstraction library. R package version 1.2-16, https://CRAN.R-project.org/package=rgdal, 11/2017.
- Blaszkowska J., Kurnatowski P., Damiecka P. 2011: Contamination of the soil by eggs of geohelminths in rural areas of Lodz district (Poland). Helminthologia 48: 67-76.
Go to original source... - Briner T., Nentwig W., Airoldi J.-P. 2005: Habitat quality of wildflower strips for common voles (Microtus arvalis) and its relevance for agriculture. Agric, Ecosyst. Environ. 105: 173-179.
Go to original source... - Cook A.J.C., Gilbert R.E., Buffolano W., Zufferey J., Pe- tersen E., Jenum P.A., Foulon W., Semprini A.E., Dunn D.T., Congenital E.R.N. 2000: Sources of Toxoplasma in- fection in pregnant women: European multicentre case-control study. Br. Med. J. 321: 142-147.
Go to original source...
Go to PubMed... - Deplazes P., Hegglin D., Gloor S., Romig T. 2004: Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol. 20: 77-84.
Go to original source...
Go to PubMed... - Dubey J.P., Desmonts G. 1987: Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet. J. 19: 337-339.
Go to original source...
Go to PubMed... - Dubie T., Tere G. 2014: Toxoplasmosis: epidemiology with the emphasis of its public health importance. MRJMMS 2: 97-108.
- Eckert J., Deplazes P. 2004: Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing con- cern. Clin. Microbiol. Rev. 17: 107-135.
Go to original source...
Go to PubMed... - Eckert J., Deplazes P., Kern P. 2011: Alveolar echinococcosis (Echinococcus multilocularis) and Neotropical forms of echino- coccosis (Echinococcus vogeli and Echinococcus oligarthrus). In: S.R. Palmer, L. Soulsby, P. Torgerson and D.W.G. Brown (Eds.), Oxford Textbook of Zoonoses Biology, Clinical Practice, and Public Health Control. Oxford University Press, Oxford, pp. 669-699.
Go to original source... - Federer K., Armua-Fernandez M.T., Hoby S., Wenker C., Deplazes P. 2015: In vivo viability of Echinococcus multiloc- ularis eggs in a rodent model after different thermo-treatments. Exp. Parasitol. 154: 14-19.
Go to original source...
Go to PubMed... - Finerman R., Sackett R. 2003: Using home gardens to decipher health and healing in the Andes. Med. Anthropol. Q. 17: 459-482.
Go to original source...
Go to PubMed... - Forin-Wiart M.-A. 2014: Identification des facteurs de variation de la prédation exercée par les chats domestiques (Felis silvestris catus) en milieu rural. PhD thesis, Reims Champagne Ardenne University, Reims, 268 pp.
- Forin-Wiart M.-A., Gotteland C., Gilot-Fromont E., Poulle M.-L. 2014: Assessing the homogeneity of individual scat detection probability using the bait-marking method on a monitored free-ranging carnivore population. Eur.J. Wildl. Res. 60: 665-672.
Go to original source... - Führer H.-P., Schneider R., Walochnik J., Auer H. 2010: Extraintestinal helminths of the common vole (Microtus arva- lis) and the water vole (Arvicola terrestris) in western Austria (Vorarlberg). Parasitol. Res. 106: 1001-1004.
Go to original source...
Go to PubMed... - Gilot-Fromont E., Lélu M., Dardé M.-L., Richomme C., Aubert D., Afonso E., Mercier A., Gotteland C., Villena I. 2012: The life cycle of Toxoplasma gondii in the natural environment. In: O. Djurkovi Djakovi (Ed.), Toxoplasmosis - Recent Advances. InTech: 3-36, Available from: https://www.intechopen.com/books/toxoplasmosis-recent-advances/the-life-cycle-of-toxoplasma-gondii-in-the-natural-environment
Go to original source... - Giraudoux P., Craig P.S., Delattre P., Bao G., Bartholo- mot B., Harraga S., Quéré J.-P., Raoul F., Wang Y., Shi D., Vuitton D.A. 2003: Interactions between landscape chang- es and host communities can regulate Echinococcus multilocu- laris transmission. Parasitology 127: S121-S131.
Go to original source...
Go to PubMed... - Giraudoux P., Delattre P., Takahashi K., Raoul F., Quéré J.P., Craig P., Vuitton D., Pawlowski Z. 2002: Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale ap- proaches? In: Proceedings of the NATO Advanced Research Workshop on Cestode Zoonoses: Echinococcosis and Cysticercosis: An Emergent and Global Problem, Poznañ, Poland, 10-13 September 2000. IOS Press, pp. 251-266.
- Giraudoux P., Pradier B., Delattre P., Deblay S., Salvi D., Defaut R. 1995: Estimation of water vole abundance by using surface indices. Acta Theriol. 40: 77-96.
Go to original source... - Goszczyñski J. 1990: Scent marking by red foxes in Central Poland during the winter season. Acta Theriol. 35: 7-16.
Go to original source... - Gotteland C. 2013: Dynamique spatio-temporelle de la contamination environnementale par Toxoplasma gondii. PhD thesis, Reims Champagne Ardenne University, Reims, 245 pp.
- Gotteland C., Chaval Y., Villena I., Galan M., Geers R., Aubert D., Poulle M.-L., Charbonnel N., Gilot-From- ont E. 2014: Species or local environment, what determines the infection of rodents by Toxoplasma gondii? Parasitology 141: 259-268.
Go to original source...
Go to PubMed... - Guislain M.-H., Raoul F., Giraudoux P., Terrier M.-E., Froment G., Ferte H., Poulle M.-L. 2008: Ecological and biological factors involved in the transmission of Echinococcus multilocularis in the French Ardennes. J. Helminthol. 82: 143-151.
Go to original source...
Go to PubMed... - Guislain M.-H., Raoul F., Poulle M.L., Giraudoux P. 2007: Fox faeces and vole distribution on a local range: ecological data in a parasitological perspective for Echinococcus multilocularis. Parasite 14: 299-308.
Go to original source...
Go to PubMed... - Hofer S., Gloor S., Müller U., Mathis A., Hegglin D., Deplazes P. 2000: High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zürich, Switzerland. Parasitology 120: 135-142.
Go to original source...
Go to PubMed... - Janko C., Schröder W., Linke S., König A. 2012: Space use and resting site selection of red foxes (Vulpes vulpes) living near villages and small towns in southern Germany. Acta Theriol. 57: 245-250.
Go to original source... - Kapel C.M.O., Torgerson P.R., Thompson R.C.A., Deplazes P. 2006: Reproductive potential of in experimentally infected foxes, dogs, raccoon dogs and cats. Int. J. Parasitol. 36: 79-86.
Go to original source...
Go to PubMed... - Kern P., Ammon A., Kron M., Sinn G., Sander S., Peters- en L.R., Gaus W., Kern P. 2004: Risk factors for alveolar echinococcosis in humans. Emerg. Infect. Dis. 12: 2088-2093.
- Knapp J., Millon L., Mouzon L., Umhang G., Raoul F., Ali Z.S., Combes B., Comte S., Gbaguidi-Haore H., Gre- nouillet F., Giraudoux P. 2014: Real time PCR to detect the environmental faecal contamination by Echinococcus multiloc- ularis from red fox stools. Vet. Parasitol. 201: 40-47.
Go to original source...
Go to PubMed... - Knapp J., Combes B., Umhang G., Aknouche S., Millon L. 2016a: Could the domestic cat play a significant role in the trans- mission of Echinococcus multilocularis? A study based on qPCR analysis of cat feces in a rural area in France. Parasite 23: 42.
Go to original source...
Go to PubMed... - Knapp J., Umhang G., Poulle M.-L., Millon L. 2016b: De- velopment of a Real-Time PCR for a sensitive one-step coprodi- agnosis allowing both the identification of carnivore feces and the detection of Toxocara spp. and Echinococcus multilocularis. App. Environ. Microbiol. 82: 2950-2958.
Go to original source...
Go to PubMed... - Kozakiewicz M., Kozakiewicz A., £ukowski A., Gortat T. 1993: Use of space by bank voles (Clethrionomys glareolus) in a Polish farm landscape. Landsc. Ecol. 8: 19-24.
Go to original source... - Lass A., Pietkiewicz H., Szostakowska B., Myjak P. 2012: The first detection of Toxoplasma gondii DNA in environmental fruits and vegetables samples. Eur. J. Clinical Microbiol. Infect. Dis. 31: 1101-1108.
Go to original source... - Lass A., Szostakowska B., Myjak P., Korzeniewski K. 2015: The first detection of Echinococcus multilocularis DNA in envi- ronmental fruit, vegetable, and mushroom samples using nested PCR. Parasitol. Res. 114: 4023-4029.
Go to original source...
Go to PubMed... - Lélu M. 2010: Etude d'un parasite à cycle complexe, Toxoplasma gondii: variabilité du cycle de transmission et dynamique de la phase environnementale. PhD thesis, Reims Champagne Ardenne University, Reims, 209 pp.
- Lélu M., Gilot-Fromont E., Aubert D., Richaume A., Afonso E., Dupuis E., Gotteland C., Marnef F., Poulle M.-L., Dumètre A., Thulliez P., Dardé M.-L., Villena I. 2011: Development of a sensitive method for Toxoplasma gondii oo- cyst extraction in soil. Vet. Parasitol. 183: 59-67.
Go to original source...
Go to PubMed... - Lélu M., Villena I., Darde M.-L., Aubert D., Geers R., Du- puis E., Marnef F., Poulle M.-L., Gotteland C., Dume- tre A., Gilot-Fromont E. 2012: Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. App. Environ. Microbiol. 78: 5127-5132.
Go to original source... - Litt J.S., Soobader M.-J., Turbin M.S., Hale J.W., Buchenau M., Marshall J.A. 2011: The influence of social involvement, neighborhood aesthetics, and community garden participation on fruit and vegetable consumption. Am. J. Public Health. 101: 1466-1473.
Go to original source...
Go to PubMed... - Marchesi P., Blant M., Capt S. (Eds.) 2008: Faune-Helvetica. Mammifères de Suisse - Clé de Détermination. CSCF & SSBF, Neuchâtel, 294 pp.
- Marsh R. 1998: Building on traditional gardening to improve household food security. Food Nutr. Agric. 22: 4-14.
- Piarroux M., Piarroux R., Knapp J., Bardonnet K., Du- mortier J., Watelet J., Gerard A., Beytout J., Abergel A., Bresson-Hadni S., Gaudart J., for the FrancEchino Surveillance Network 2013: Populations at risk for alveolar echinococcosis, France. Emerg. Infect. Dis. 19: 721-728.
Go to original source...
Go to PubMed... - Pleydell D.R.J., Raoul F., Tourneux F., Danson F.M., Gra- ham A.J., Craig P.S., Giraudoux P. 2004: Modelling the spatial distribution of Echinococcus multilocularis infection in foxes. Acta Trop. 91: 253-265.
Go to original source...
Go to PubMed... - Pusenius J., Viitala J. 1993: Varying spacing behaviour of breed- ing field voles, Microtus agrestis. Ann. Zool. Fenn. 30: 143-152.
- Quintaine T. 2010: Ecologie de la transmission d'Echinococcus multilocularis: Identification des milieux propices et modélisation de l'effet du comportement de l'hôte définitif, Vulpes vulpes. PhD thesis, Franche-Comté University, Besançon, 146 pp.
- R Core Team 2015: R: A language and environment for statisti- cal computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
- Reperant L.A., Hegglin D., Tanner I., Fischer C., Deplazes P. 2009: Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 136: 329-337.
Go to original source...
Go to PubMed... - Reyes-García V., Aceituno L., Vila S., Calvet-Mir L., Garnatje T., Jesch A., Lastra J.J., Parada M., Rigat M., Vallès J., Pardo-De-Santayana M. 2012: Home gardens in three mountain regions of the Iberian Peninsula: description, motivation for gardening, and gross financial benefits. J. Sustain. Agr. 36: 249-270.
Go to original source... - Robardet E., Giraudoux P., Caillot C., Augot D., Boue F., Barrat J. 2011: Fox defecation behaviour in relation to spatial distribution of voles in an urbanised area: an increasing risk of transmission of Echinococcus multilocularis? Int. J. Parasitol. 41: 145-154.
Go to original source...
Go to PubMed... - Robert-Gangneux F., Aubert D., Villena I. 2015: Toxoplas- mosis: a widespread zoonosis diversely affecting humans and animals. In: A. Sing (Ed.), Zoonoses - Infections Affecting Hu- mans and Animals: Focus on Public Health Aspects. Springer, Dordrecht, pp. 355-376.
Go to original source... - Simon J.A., Kurdzielewicz S., Jeanniot E., Dupuis E., Marnef M., Aubert D., Villena I., Poulle M.-L. 2017: Spatial distribution of soil contaminated with Toxoplasma gon- dii oocysts in relation to the distribution and use of domestic cat defecation sites on dairy farms. Int. J. Parasitol. 47: 357-367.
Go to original source...
Go to PubMed... - Spitz F., Le Louarn H., Poulet A., Dassonville R. 1974: Standardisation des piégeages en ligne pour quelques espèces de rongeurs. Rev. Ecol. (Terre & Vie) 28: 564-578.
Go to original source... - Stoddart D.M. 1970: Individual range, dispersion and dispersal in a population of water voles (Arvicola terrestris (L.)). J. Animal. Ecol. 39: 403-425.
Go to original source... - Tenter A.M., Heckeroth A.R., Weiss L.M. 2000: Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30: 1217-1258.
Go to original source...
Go to PubMed... - Trachsel D., Deplazes P., Mathis A. 2007: Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134: 911-920.
Go to original source...
Go to PubMed... - Umhang G., Forin-Wiart M.-A., Hormaz V., Caillot C., Boucher J.-M., Poulle M.-L., Franck B. 2015: Echino- coccus multilocularis detection in the intestines and feces of free-ranging domestic cats (Felis s. catus) and European wild- cats (Felis s. silvestris) from northeastern France. Vet. Parasitol. 214: 75-79.
Go to original source...
Go to PubMed... - Veit P., Bilger B., Schad V., Schäfer J., Frank W., Lucius R. 1995: Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110: 79-86.
Go to original source...
Go to PubMed... - Vukicevic-radic O., Matic R., Kataranovski D., Stamenk- ovic S. 2006: Spatial organization and home range of Apodemus flavicollis and A. agrarius on Mt. Avala, Serbia. Acta Zool. Academ. Sci. Hung. 52: 81-96.


