Soil contamination with canine intestinal parasites eggs in the parks and shelter dogs from Bucharest area

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1 Available online at ScienceDirect Agriculture and Agricultural Science Procedia 6 ( 2015 ) ST26733, International Conference "Agriculture for Life, Life for Agriculture" Soil contamination with canine intestinal parasites eggs in the parks and shelter dogs from Bucharest area Poliana Tudor Faculty of Veterinary Medicine, 105 Splaiul Independentei, Bucharest, Romania Abstract Soil-transmitted helminthes infections are caused by different species of parasitic worms. They are transmitted by eggs or larvae present in dog faeces, which contaminate the soil. The presence of infective parasitic elements in the environment represents an important way of transmission of intestinally nematodes from dog to human and other animals. They can become infected by accidental ingestion of the infective elements or cutaneous contact with contaminated soil. The aim of this study was to determine the possibility of contamination with canine intestinal worms of the soil from different parks in Bucharest and a dog s shelter outside of town. A total of 45 soil samples were collected from 4 dog playpens (from which 3 fenced and 1 unfenced), 4 playgrounds and one shelter dogs. Helminthes eggs were found in % of the soil samples. Positive samples for at least one parasite have found in 1 (the unfenced once), 4 playpens, 3/4 playground and 1/1 shelter dogs. The most frequently parasites species found in the examinated soil samples were Toxocara spp. (17.17%), followed by Trichuris spp. (8.88%), Strongyloides spp. and Toxascaris spp., each one with 4.44 %. 8.88% had only one kind of eggs, and two parasites mixt were found in %. This study has shown that Toxocara spp. were the main species of canine intestinally parasites in the soil samples, representing a major zoonotic risk for human The Authors. Published by by Elsevier B.V. This is an open access article under the CC BY-NC-ND license ( Peer-review under responsibility of the University of Agronomic Sciences and Veterinary Medicine Bucharest. Peer-review under responsibility of the University of Agronomic Sciences and Veterinary Medicine Bucharest Keywords: canine, helminths eggs, soil samples Corresponding author: Tel address: polianatudor@yahoo.com The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license ( Peer-review under responsibility of the University of Agronomic Sciences and Veterinary Medicine Bucharest doi: /j.aaspro

2 388 Poliana Tudor / Agriculture and Agricultural Science Procedia 6 ( 2015 ) Introduction Soil is an important route of transmission of a large number of pathogens, to both animals and humans. The main source of soil contamination with parasites is represented by infected animals and/or infected humans which can spread a large number of infected elements (eggs, larvae) in the environment through their faeces (Traversa et al., 2014). The eggs/ larvae of many nematodes are highly resistant. They can survive in the environment for a long period of time (months, years) (Mitrea, 2011). Animals and humans are contaminated by accidental ingestion of the infected elements or by cutaneous contact with the contaminated soil. The concentration of pets in urban areas associated with a growing number of stray animals contributes to soil contamination in public places and spreading geoheminth infections (Cassenote et al., 2011). Soil-transmitted helminth (STH) infections are caused by different species of parasite worms, including roundworms (i.e. Toxocara spp.; Ascaris spp.), hookworms (i.e. Ancylostoma spp.), and whipworms (i.e. Trichuris spp.) (Traversa et al., 2014). Human infections with canine intestinal worms are among the most common zoonotic infections, Pullan et al. (2014) estimates worldwide by 2010, over 1.45 billion people were infected with at least one species of intestinal nematodes, most of the cases being concentrated in underdeveloped areas. Numerous studies conducted on soil samples in different parts of the world have demonstrated broad environmental contamination, especially in public places, such as parks and playgrounds for children (Habluetzel et al., 2003; Avcioglu and Burgu, 2008; Bojar and K ape, 2012; Stoj evi et al., 2012; Sprenger et al., 2013; Maraghi et al., 2014; Otero et al., 2014). Worldwide, the rate of soil contamination varies greatly, running the intervention of a wide range of factors. Previous studies carried out on soil samples have discovered mostly Toxocara canis, T. cati, Trichuris vulpis, Ancylostoma spp, eggs (Blaszkowska et al., 2013; Bojar and K ape, 2012) and also cysts of Giardia spp. cysts and Cryptosporidium spp. oocysts (Tavalla et al., 2012; Stoj evi et al. 2010). The aim of this study was to determine the posibility of contamination with canine intestinal worms of the soil from different parks in Bucharest and a dog s shelter outside of town. 2. Research Methods For the presented study were elected 2 types of places in Bucharest represented by pens for dogs (of which 3 fenced and 1 unfenced) and playgrounds for children (4 unfenced) near blocks. Moreover soil samples were harvested from a dogs shelter outside of town. From September to November 2014 the 5 soil samples taken at a distance of 10 m apart, were harvested from each place, for a total of 45 samples. For each place were collected 30 g soils, placed in labeled plastic bags and transported to the laboratory. To isolate the parasite eggs, soil samples were processed by previously described method by Dunsmore et al. (1984) and Mandarino-Pereira et al. (2010) with some modifications. Briefly, we have used for flotation supersaturated solution of NaCl. Eggs were identified based on morphological characters (Mitrea, 2011). No attempt was made to differentiate between T. canis eggs and T. cati. 3. Results and Discussion Out of the 45 soil samples examined 10 (22.22%) were positive. Of the 40 samples collected from public places, only 5 samples (12.50%) were positive for at least one parasite. In contrast, all 5 samples collected from dog shelters were positive. Thus, of the 9 places chosen for examination, eggs of parasites were isolated in 5 (55.55%) of them, as follows: 1 (the unfenced) / 4 pens for dogs, playgrounds for children ¾ and 1/1 shelter for dogs. Microscopic examination allowed the identification of eggs of Toxocara spp. in 17.77% samples, Trichuris spp. in 8.88% samples, Ancylostoma spp., respectively Toxascaris spp. in 4.44% for each sample. 8.88% of samples contained one type eggs, and combinations of two parasites were found in 13.33% samples. Stray dogs are still representing an unsolved problem in Romania including in Bucharest. These dogs do not receive antiparasitic treatments and can be a reservoir for zoonotic potential parasites such as Toxocara spp. With their faeces they also eliminate eggs/ larvae of helminths making a contribution for environmental contamination. The canine faeces in the environment are representing an important source of pathogens for pets, but also for the community at large (Traversa et al., 2014). The present study aimed the possibility of helminth eggs soil contamination with zoonotic risk.

3 Poliana Tudor / Agriculture and Agricultural Science Procedia 6 (2015) Studies on soil contamination with helminth eggs were made worldwide and contamination rate varied greatly. In Poland, ranged between 7.9% and 10.6% (Blaszkowska et al., 2013) and 18.6% (Bojar and Káapeü, 2012) respectively. In Italy was 24% (Habluetzel et al., 2003), 63.3% in Portugal (Otero et al., 2014), 79.2% in Slovakia (Rudohradská et al., 2011), in India between 4.75% (Thomas and Jeyathilakan, 2014) and 12.84% (Sudhakar et al., 2013), 31% in the Philippines (Paller and de Chavez, 2014), and 79.3% in Iran (Tavalla et al., 2012). In Brazil, several studies were conducted, and the values of soil contamination rate was 22.4% (Mandarino-Pereira et al., 2010), 30.2% (Cassenote et al., 2011), 36% (Sprenger et al., 2014), 44% (de Moura et al., 2013) and 78.6% (Marchioro et al., 2013). In our study the rate of soil contamination was 22.22%. However, this value was influenced by the fact that all soil samples collected from dog shelters were positive. The amount of soil contamination rate in public places (pens for dogs and playgrounds for children) was 12.5% (5/40). The differences between the results of earlier studies may be attributed to a wide range of factors, such as climatic conditions, the population of dogs, soil type, number and volume of samples tested, the season in which sampling was performed, the mode of storage of samples, and the methods used (Mizgajska, 2001; Santarém et al., 2009). In our study parasite eggs were identified in almost all places that were not fenced and also in dog shelters. Fenced places specially arranged for dogs recreation were free of helminth eggs, this means that the animals which had access here received antiparasitic medication. Moreover, in this places have access only dogs with their owners. Interestingly, in a dog pen, two samples were positive. The explanation is that although the place was initially arranged for recreation of dogs subsequently the fence was broken and the access of stray dogs was free, suggesting a potential route of contamination of that place. Avcioglu and Balkaya (2011), in a study conducted in Erzurum, Turkey, found that fenced parks were free of nematode eggs. In our study in one of the playgrounds for children all samples were negative even though the place was not fenced. Probably the stray dogs in that area were captured and taken to dog shelters with the posibility of being given for adoption. Fig. 1. Toxocara spp egg from soil samples (x100) Toxocara spp. eggs (Fig. 1) were most frequently found in this study, similar to previous reports which estimated that over 90% of the investigated areas in the world were contaminated with T. canis (Kirchheimer and Jacobs, 2008). The value obtained by us was smaller than the ones reported in Iran (22.2% - Zibaei et al., 2010; 29,2% - Maraghi et al., 2014) and England (17,8% - 30% - Kirchheimer and Jacobs, 2008), but higher that those reported in Brazil (8.0% - Mandarino-Pereira et al., 2010), Turkey (15,6% - Aydenizoz et al., 2006) and Poland (16.6% - Bojar and Káapeü, 2012). de Maura et al. (2013) analyzing the frequency of helminths in public markets in Pelotas, Brazil, found that the rate of soil contamination with Toxocara spp. eggs was 8.8%. The diferences can be atributed in general to the previous mentioned factors. Thus, the analysis of Stojþeviü et al. (2010) showed different values of the rate of soil contamination with eggs of Toxocara spp. according to the season, 15.5% in June 389

4 390 Poliana Tudor / Agriculture and Agricultural Science Procedia 6 ( 2015 ) respectively 23.3% in December. Differences in the rate of soil contamination with Toxocara spp. eggs were found depending on the season by Avcioglu and Burgu (2008) in Turkey and by Stoj evi et al. (2010) in Croatia, respectively Habluetzel et al. (2003) in Italy. As mentioned above the present study did not differentiate between T. canis eggs and T. cati, all were considered as T. canis eggs. Taking into account the extremely high prolificacy of female T. canis, which gives up to eggs/day, and the fact that an animal can be parasitized by 1 to 1000 worms, suggests that the environment may be contaminated every day by millions of eggs (Barriga, 1988). After reaching the ground, T. canis eggs can survive for long periods (several years)(lloyd, 1993), and under favorable conditions of temperature and humidity, can become infested, representing a risk of contamination to other animals, but also humans and in particular for children, producing toxocariasis. Toxocariasis is a public health problem, it is transmitted to humans by ingestion of eggs from contaminated soil (sapro-zoonosis) on unwashed hands (disease dirty hands ) or by eating raw vegetables (Wolfe and Wright, 2003). Our study showed that Trichuri spp. was the second parasite prevalence detected in soil samples, being present in both dog shelters and in public places. Similar results were published by Bojar and K ape (2012) who conducted an investigation of soil contamination with geohelminth eggs in recreational areas in the region of Lublin, Poland. Similarly, Mandarino-Pereira et al. (2010) monitoring the prevalence of parasites in soils from public markets in Seropédica, Brazil, identified Trichuris spp. eggs in 8.0% of samples. Stojcev et al. (2010) conducted a survey on soil and sand in the region of Pula, Croatia, and have found that eggs of Trichuris spp. were in 10.0% of samples. The Trichuris genus includes nematodes that affect pets, rent animals and humans. The dog is parasited with T. vulpis, a nematode that is ubiquitous in the large intestine and gives eggs which can survive in the soil even in difficult environmental conditions (Traversa et al., 2014). Called the whipworm due to its appearance, with long and thin front and thicker back ( whip handle ), T. vulpis is important for both physicians and veterinarians, although its zoonotic potential has not been yet elucidated (Traversa, 2011). Soil contamination with Ancylostoma spp and Toxascaris spp eggs was lower in our study, similar to those reported by Stojcevic et al. (2010). In contrast, studies in Brazil showed higher values of 6.9% (Cassenote et al., 2011), 13.5% (de Mauro et al., 2013), 14.5% (Sprenger et al., 2014), and 20% (Mandarino-Pereira et al., 2010) for Ancylostoma spp. Evaluation of soil contamination with canine intestinal parasites eggs are an important tool in assessing to which risks are people exposed. The main source of soil contamination is the faeces from infected animals. As such, deworming animals is the best way to prevent spreading the parasites. Therefore a better informing and education of dog owners about the necesity of periodic deworming is needed to reduce the potential risks of parasitic zoonoses. 4. Conclusions The results of this study indicated that soil contamination rate was high, and the eggs of Toxocara spp had the highest prevalence. These results require periodical studies on the rate of soil contamination with helminth eggs and surveillance of disease risk in humans. Acknowledgements This study was published during the project POSDRU/89/1.5/S/ References Avcioglu, H., Burgu, A., Prevalence of Toxocara ova in soil samples from public parks in Ankara Turkey. Vector-Borne and Zoonotic Diseases, 8 (3): Avcioglu, H., Balkaya, I., The relationship of public park accessibility to dogs to the presence of Toxocara species ova in the soil. Vector- Borne and Zoonotic Diseases, 11 (2): Aydenizöz Ozkayhan, M., Soil contamination with ascarid eggs in playground in Kirikkale, Turkey. J. Helminthol., 80 (1): Barriga, O., A critical look at the importance, prevalence and control of toxocariasis and the possibilities of immunological control. Veterinary Parasitology, 29 (1-2):

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