Soil and sand contamination with canine intestinal parasite eggs as a risk factor for human health in public parks in Niš (Serbia)

More than 2 billion people worldwide are exposed to a risk for geohelminth infections. Regarding geographical distribution and clinical relevance, the most common canine helminths are Toxocara canis, Ancylostomatidae, and Trichuris vulpis, but the significance of these pathogens has been often underestimated by both veterinary and human medical professionals, as well as the general public (Traversa et al., 2014).

Human contact with the soil is one of the possible ways of spreading the canine intestinal parasites. These pathogens reach the soil via canine and human feces and can survive in this environment for a long period, making it a potential reservoir of infection (Tudor, 2015). The developing forms of geohelminths can survive the longest and enter the organism of susceptible individuals via skin or wounds in the visible mucosa (Ancylostoma caninum, Uncinaria stenocephala, Strongyloides stercoralis), causing a cutaneous larva migrans (Heukelbach & Feldmeier, 2008; Jaleta et al., 2017), or by ingestion (T. canis), when a visceral or ocular larva migrans is formed, which may persist in human tissues even for as long as several years (Aydenizöz-Özkayhana et al., 2008; Overgaauw & van Knapen, 2013). The infections such as these are mainly sporadic, but in extraordinary situations (natural disasters and wars), they can also occur in epidemic scales (Tudor, 2015).

According to the information from the available literature, different degrees of soil contamination with helminth eggs and larvae from canine feces have been established. In Poland, the percentage was between 7.9 % and 10.6 % (Blaszkovska et al., 2012) and 18.6 % (Bojar & Kłapeć, 2012); in Italy, 24 % (Habluetzel et al., 2003); in Portugal, 63.3 % (Otero et al., 2014); in Slovakia, 79.2 % (Rudohradska et al., 2011); in India, 12.84 % (Sudhakar et al., 2013); in Spain, 71.33 % (Martínez-Moreno et al., 2007); and in Romania, 22.22 % (Tudor, 2015).

The studies performed in public parks in several Serbian cities, such as Belgrade (Pavlović et al., 2015), Požarevac, Kostolac (Pavlović et al., 2015) and Kruševac (Raičević & Pavlović, 2019), have demonstrated a degree of contamination of urban green spaces, soil, and sand ponds in day-care facilities for pre-school children with zoonotic protozoa, nematodes, and cestodes.

This paper aimed to establish the degree of soil contamination and sand with zoonotic parasites from the canine feces and the degree of risk they could pose for human health in public places and playgrounds in the city of Niš.

Not applicable.

In the examined soil and sand samples, seven endoparasites were identified: protozoa from the Cystoisospora genus (Fig. 1A), nematodes (Toxocara canis – Fig. 1B, Toxascaris leonina – Fig. 1C, Trichuris vulpis – Fig. 1D, ancylostomatidae – Fig. 1E) and a trematode Alaria alata (Fig. 1F).

Figure 1

Each of the 4 methods of parasitological diagnostics applied was used according to the degree of sensitivity of the selected method for the appropriate type of parasite elements, as expected in the samples of the test material.

The study was performed in dry and humid periods in the spring season of 2019, investigating the prevalence of intestinal helminths eggs and protozoan oocysts in the samples of soil and sand from public parks and playgrounds for children in the city of Niš. The eggs of T. canis were diagnosed with the highest prevalence (16 – 22 % in the soil; 26 % in the sand), which agreed with other authors’ findings, demonstrating the prevalence of this ascarid at 15.6 % in the playgrounds in Turkey (Aydenizoz, 2006) and 15.5 % – 23.3 % in the playgrounds in Croatia (Stojčević et al., 2010). The literature data suggest that depending on the climate and geographical location, the level of contamination varies among different countries and within individual countries, where it is determined by the action of local geoclimatic factors. Accordingly, the contamination of public parks in Italy with eggs of T. canis was 63.6 % (Giacometti et al., 2000), in Slovakia 61.3 % (Rudohradská et al., 2011), in Serbia (Kruševac) 50.1 % (Raičević & Pavlović, 2019), while in Spain over 67 % of parks and 1.24 % of soil samples were contaminated (Ruiz et al., 2001).

The results of this study agree with the data about soil contamination with T. canis eggs obtained by the authors from the Czech Republic 5.0 to 20.4 % (Dubná et al., 2007), Croatia – 15.5 do 23.3 % (Stojčević et al., 2010), Spain – 16.4 % (Dado et al., 2012), Poland – 16.6 % (Bojar & Káapeü, 2012), Romania – 17.17 % (Tudor, 2015) and Greece – 17.2 % (Papavasilopoulos et al., 2018).

The degree of contamination of sand samples with the ascarid T. canis, as was found in the study, is following the authors’ findings from Slovakia – 6.8 to 27.0 % (Ondriska et al., 2013), markedly higher than that from the Czech Republic – 11.9 % (Dubná et al., 2007), Slovakia – 11.8 % (Papajová et al., 2014) and slightly higher than the degree of contamination established in India – 17.64 % (Sudhakar et al., 2013).

The contamination with ancylostomatids eggs was diagnosed in 8 – 12 % of soil samples and 8 % of sand samples, while the presence of T. vulpis eggs was established in 4 – 6 % of soil samples and 4 % of sand samples. The studies from Croatia report a higher degree of contamination of soil and sand samples from the playgrounds in Pula with T. vulpis eggs – 10 – 17.7 % (Stojčević et al., 2010).

A statistically significant difference in the degree of contamination with A. alata eggs was found between sand (16 %) and soil samples (2 %). In the samples of soil from Park 1, the eggs of this trematode were not found. The reason might have been a dry period of sampling (May) since a higher degree of contamination and a greater number of identified species are always reported in humid periods of the year (Nurdian, 2004). An increased number of soil samples positive for the presence of ascarids and ancylostomatids, as well as sand samples for the presence of A. alata, can be explained by favorable climatic conditions, with moderate temperatures, appropriate soil humidity and adequate environmental conditions in general. During the spring months, the eggs accumulated and concentrated in the soil, and due to low precipitation, they were not washed down to deeper layers of soil. The analysis of soil sections revealed that most of the eggs were situated at the depth of 0 – 4 cm (Storey & Phillips, 1985). Since they are not situated on the surface, the eggs are probably protected from the action of direct sunlight and decay.

Such a long survival of ascarid eggs can be explained by the fact that these are most resilient helminth eggs, able to preserve their vitality for up to several years. On the other hand, protozoan cysts and oocysts have a reduced ability to survive in the natural environment (the cysts of Giardia spp. are less resilient than Cryptosporidium spp. oocysts). This fact may partly explain the absence of these protozoa in our study, in contrast to other authors’ findings (Martínez-Moreno et al., 2007; Dado et al., 2012; Pavlović et al., 2015).

A difference was established in the number of positive soil (13) and sand samples (20). The sand was sampled only from the „free“ part of Čair park (50 samples), since in other parks of interest for the study there were no sandpits.

Since the texture and humidity of samples have an impact on the length of survival of parasite eggs in the external environment, it should be emphasized that the samples of soil and sand in our study were almost identical as to their humidity. The reason is the vicinity of the Nišava river and its tributary Gabrovačka river, i.e. the fact that sand has an increased capacity to hold moisture. Nišava flows past the Parks 1 and 3 (from which exclusively soil was sampled), while the Park 2 is located further in the city core (the only park with free sand for sampling). In the Park 2, a higher degree of sand contamination (40 %) was found compared to soil contamination (38 %), which agreed with the results reported by Bojar and Kłapeć (2012), who detected the highest degree of contamination of sand (40 %) on the lake beaches in southeastern Poland. The authors stressed that in these places there was an increased chance for contamination of recreational areas with eggs of intestinal parasites from wild animals. The results are supported by the fact that in Poland and other European countries the phenomenon of synanthropization of wild animals, especially red foxes and feral pigs, has been observed, which opens new, additional opportunities for soil and sand pollution in public places in urban areas.

Most parasite eggs (especially embryonated ones) were found in the samples from shadowy places (under the trees or small shrubs). The reason is the ability of soil to hold humidity in such places and protection from direct sunlight, which significantly prolongs egg viability. The finding is also directly correlated with the behavior of dogs and their choice of spots for defecation (Rubel & Wisniveskyy, 2005).

In our study, 5 – 20g of soil and 5 – 20g of sand were examined for each of these methods. The amount of sample tested was dependent on the method used. According to literature data from Mandarino-Pereira et al. (2010) tested soil samples (25g) using a modified centrifugal-flotation technique with NaNO3 (Dunsmore et al. 1984) and an adaptation of Rugai’s et al. method (Carvalho et al., 2005) is a spontaneous sedimentation method. This method checks 100g of soil and can be done the granulometric analyses of the samples were done and the soil classified into sand, silt, and clay according to their composition (Embrapa, 1997).

According to Kazacos (1983), the ability to diagnose parasitic elements in soil samples increases when a larger amount of soil (30g) is used for analysis. These authors claim that 30g of soil is the maximum amount of soil that can be effectively cultivated. In our study, the maximum amount of soil/sand sampled was 20g for technical reasons. Our experience shows that a larger amount of the sample leads to the formation of a dense suspension with the formation of air bubbles, which make it difficult to microscopically examine the preparations and to diagnose parasitic elements.

The experience of other authors shows that sedimentation techniques are more practical and economical than flotation for soil and sand examination, but leave more impurity particles in the supernatant, which may interfere with the detection of the parasite by microscopy (Carvalho et al., 2005). Therefore, the flotation method with a saturated ZnSO4 solution is always recommended as an alternative. The flotation technique requires the use of a solution of appropriate specific gravity, which makes this technique more expensive than sedimentation (Dunsmore et al., 1984).

The diagnosed canine intestinal parasites from the soil and sand present an important potential serious human health hazard, especially for the children aged 3 – 5 years. Supporting this notion are the diagnosed cases of parasitic zoonoses in Serbia (Gvozdenović et al., 2012; Mijatović et al., 2015; Miladinović Tasić et al., 2017; Perić et al., 2017), and that is the reason why a synchronized cooperation of professionals in the fields of both veterinary and human medicine is mandatory.

In conclusion, in the areas of public parks in the city of Niš, we established contamination with endoparasites of 38 – 46 % of soil samples and 40 % of sand samples. In the samples of soil, the contamination with T. canis ascarid (a low and medium degree) and ancylostomatids (a low and medium degree) was predominant, while in the samples of sand different degrees of contamination were present with T. canis and A. alata. Such a finding suggests a serious risk for human health since the above geohelminths are the etiological agents of visceral, ocular and cutaneous larva migrans syndrome, as well as of human larval alariosis. The finding of A. alata trematode in the samples of soil (2 %) and sand (16 %) indicates a significant circulation of stray dogs in the areas of public parks in the city of Niš. For owned dogs and people, they represent a reservoir of zoonotic parasites found in the soil and sand in the studied public spaces.

The resolution of this significant public health problem is therefore necessary through the Suggestion of measures, involving: a) control of parasite transmission in the environment, b) guidelines/information for dog owners for the prevention, maintenance of health, and spread of zoonotic diseases, and c) education of medical and veterinary professionals, pet owners and the general public.