The Relationship of Public Park Accessibility to Dogs to the Presence of Toxocara Species Ova in the Soil

Abstract

This survey was conducted to determine prevalence of Toxocara spp. ova in public parks in Erzurum, Turkey. A total of 214 soil samples were collected from July 2007 to June 2008 in 36 public parks, of which 28 were unfenced and 8 were fenced. Prevalence of Toxocara spp. was 64.28% in unfenced public parks, while no contamination was observed fenced public parks (p < 0.001). Average number of Toxocara spp. ova was 1.43 per 50 g sand ranging from 1 to 7. Moreover, soils from unfenced public parks were contaminated with Taeniid spp. ova (3.12%). In conclusion, public parks and/or playgrounds should be fenced to prevent fecal contamination, suggesting that a more frequent surveillance should be performed and preventive measures should be taken and enforced by local governments to reduce likelihood of zoonoses in children.

Introduction

T he increasing popularity of pet animals, particularly dogs and cats, has been associated with widespread contamination of the soil with infective ova and larvae. In addition to pica, children's play habits and their attraction to pets put them at higher risk for infection than adults (Schantz and Glickman 1978). There are several intestinal parasites that dogs can transmit to humans. Toxocara spp. and Echinococcus spp. are transmitted from dogs to humans, resulting in occurrence of visceral larva migrans and hydatidosis in humans, respectively. Toxocara ova gain infection capability within 2–4 weeks after being excreted via feces (Glickman and Shofer 1987).

Public parks can be contaminated via defecation by stray dogs and cats or infected pet animals. Because of ingesting sand and petting infected animals, children are prone to these zoonoses in public parks contaminated with helminth ova. Moreover, Toxocara spp. ova are extremely resistant to environmental conditions (Glickman and Shofer 1987), which may make contamination for long term. Public park contamination and human health have been focus of numerous epidemiological surveys. As quoted by Avcioglu and Burgu (2008) worldwide prevalence of Toxocara spp. ova in public parks was estimated to be 9.75%, 6.73%, 28.31%, 11.57%, 0.55%, 14.03%, and 11.87% in North America, Latin America, Europe, Asia, Middle East, Australia, and Turkey, respectively. The objective of this survey was to determine if fenced and unfenced public parks in Erzurum, Turkey, were contaminated with Toxocara ova.

Materials and Methods

Sample collection and process

Erzurum (39°52′N, 41°17′E) is the largest city in eastern Turkey. There are 500,000 inhabitants and 36 public parks in the city center. A total of 54 soil samples from fenced public parks (n = 8) and 160 soil samples from unfenced public parks (n = 28) were examined from July 2007 to June 2008 for egg contamination. In each public park, a 1-m² area was lined for every 5-m² plot. Finally, about 250–300 g soil sample was taken at 10 cm depth at the center of isolated area.

After homogenization of all soil samples from each park, 50 g representative soil sample was mixed with distilled water and 1 mL Tween 40. The remaining sample was discarded. Mixture was vortexed and then filtered through a 250-μm filter. An aliquot of 28 mL was added with 20 mL distilled water and centrifuged at 4000 g for 3 min. This process was repeated three times. Final sediment was transferred to a centrifuge tube and 12 mL saturated NaCl solution (density of 1.18; 360 g NaCl per liter water) was added for flotation (Kazacos 1983). Then the material was centrifuged again for 10 min. Samples were analyzed under light microscopy for egg identification and count per 50 g soil samples. Additionally, fecal samples (n = 34) were collected from stray dogs around the park areas to assess if they were positive for helminth ova after floating them with Fülleborn solution (Kassai 1999).

Data analysis

Egg counts by public parks and soil samples were evaluated using descriptive statistics (SPSS Version 10.0.1, 1999; SPSS, Chicago, IL). Chi-square test was employed to determine differences between fenced and unfenced public parks in prevalence of contamination, and statistical significance was declared to be p < 0.05. Fecal examination results were descriptively reported.

Results

Overall prevalence of Toxocara spp. ova was 18 (50.0%) and 30 (14.01%) in public parks and soil samples of these parks, respectively. In unfenced public parks and sand samples, prevalence of Toxocara spp. was 64.28% (18/28) and 18.75% (30/160), respectively. However, no contamination was observed in 54 soil samples collected from fenced public parks (p < 0.001; Table 1). Although emphasizing on Toxocara spp., ova of Toxascaris leonina and Taeniid spp. were also identified in unfenced public parks. Prevalence of T. leonina and Taeniid spp. was 1.25% and 3.12%, respectively (Table 1).

Table 1.

Public Park Contamination Rate and Toxocara Species Ova Prevalence in Soil Samples

Parks	Toxocara spp.
Unfenced parks (n = 28)	18
Fenced parks (n = 8)	0
p-Value	<0.001

Soils	Toxocara spp.	Taenia spp.
n = 160	30	7
n = 54	0	0
p-Value	<0.0001	<0.0001

The number of Toxocara spp. ova among contaminated samples was 43, and the average of number of ova per 50 g sample was 1.43, ranging from 1 to 7. There were two T. leonina and eight Taeniid spp. ova in these samples. The mean egg number of these genera was 1 (1) and 1.6 (1–3), respectively. The recovered species from fecal samples were Toxocara canis, T. leonina, Taeniid spp., Trichuris spp., and their prevalence are summarized in Table 2.

Table 2.

Fecal Flotation Results of Stray Dogs

			Stray dogs around the park areas
			Sex		Age (year)
Species	np/n	p	♂	♀	<1	>1
Toxocara canis	12/34	35.29	8	4	7	5
Toxascaris leonina	7/34	20.58	6	1	3	4
Taenia spp.	2/34	5.88	2	—	—	2
Trichuris spp.	1/34	2.94	1	—	—	1

np, number positive; n, number examined; p, prevalence (positive %).

Discussion

Toxocariasis is an important zoonosis. The worldwide prevalence of Toxocara spp. ova in public parks in large cities is 15.90% (Avcioglu and Burgu 2008). In a similar survey conducted in Ankara (Avcioglu and Burgu 2008), it was shown that 45% of the public parks were contaminated and the prevalence of Toxocara spp. ova in soils of these parks was 15.05%. Prevalence of Toxocara spp. in this survey (14.01%) was within that reported continental averages, but is greater than the average reported in Turkey (Avcioglu and Burgu 2008). Differences could be related broadly to sample size, laboratory method, animal population, socioeconomic status, and climatological variables in the region as well as city regulations and enforcements. Moreover, enforcement of hygiene in park, use of antiparasitic drugs, and obedience training as well as application of stool collection in special containers by owner, management of stray dogs and cats, and workshops on public awareness by municipal government can also contribute to the prevalence.

Previous studies ascertain the importance of this surveillance because of its relation to public health. For example, visceral larva migrans seroprevalance among children in Turkey was reported to be ranging from 12.95% to 75% (Kuman and Altıntaş 1984, Doğan et al. 2007). Prevalence of Toxocana cati and T. canis was reported to be 0.32%–59.4% (Burgu et al. 1980, Ayçiçek et al. 1998) in Turkey. Moreover, a report released by the Ministry of Health between 1984 and 1994 revealed that the number of cystic and alveolar echinococcosis was 27,267 and 118, respectively (Altintaş 2003). In addition, alveolar echinococcosis was reported in humans several times in Erzurum (Polat et al. 2002, Gündoğdu et al. 2005). Ova of Taenia spp. and Echinococcus spp. are seldom differentiated based on morphology and the methods we used. Contamination rate of 3.12% with Taeniid spp. ova in this survey could be misleading, because they could be Echinococcus spp. ova defecated by stray dogs. Besides, prevalence of fecal samples from stray dog around the park areas in this study was T. canis 35.29%, T. leonina 20.58%, Taeniid spp. 5.88%, and Trichuris spp. 2.94% (Table 2). These results show that contamination of parks and infection in dogs have a close relationship with each other.

Although various methods had been examined to prevent sandpit contamination by Toxocara spp. ova in Japan (Uga and Kataoka 1995, Abe and Yasukawa 1997), no effective methods were established until now, partly because of the cost and various reasons. Uga and Kataoka (1995) worked on the efficiency of fence construction around sandpits in Hyogo city and detected Toxocara spp. ova at 9 weeks after sand replacement. Abe and Yasukawa (1997) stated that the number of ova recovered from sandpits following fence construction decreased but it was not sufficient to prevent contamination. Contamination of fenced sandpits might be due to the following: users, especially children, often left the gate open, owners of pets play inside fenced areas with their children and dogs, and the gate was not designed to close automatically with a spring. In this study, prevalence of Toxocara spp. ova in unfenced public parks was 64.28% (18/28), whereas no contamination was observed in eight fenced public parks (p < 0.001). Stray dogs are more likely to contaminate public parks than are owned dogs being deliberately exercised there, because they are likely to be carrying higher worm burdens because of infrequent antihelminthic application. In addition, improvement of fence design coupled with education of sandpit users is necessary to prevent contamination of Toxocara spp. ova following fence construction.

In this study, average egg number was greater than that reported by Childs (1985) and Toparlak et al. (2002) and lower than that reported by Düwell (1984), Abo-Shehada (1989), Mahdi and Ali (1993), Güçlü and Aydenizöz (1998), Oge and Oge (2000), Ruiz de Ybáňez et al. (2001), and Dubna et al. (2007). In the literature, the average egg number was the highest (16.7, with range of 2–64) and lowest (0.44, with range of 1–6) in the studies of Ruiz de Ybáňez et al. (2001) and Toparlak et al. (2002), respectively. Being low number does not necessarily disregard the risk for toxocarosis. Exposure to even low numbers of ova in children may cause ocular larva migrans (Glickman et al. 1979).

In conclusion, public parks in Erzurum were examined with respect to prevalence of Toxocara spp. ova and their accessibility. Contamination rate with Toxocara spp. ova was 50.0% in public parks in the city. Prevalence of Toxocara spp. in unfenced public parks was 64.28% (18/28), whereas no contamination was observed in eight fenced public parks. Risks to human health can be more effectively and more practically reduced by educating the owners about pet animal health (i.e., effective deworming) and by encouraging compliance with existing laws requiring the removal of feces from public places. Parks should be fenced to prevent fecal contamination by dogs and cats. Public awareness should be notified, a more frequent surveillance should be performed, and preventive measures should be taken and enforced by local governments to reduce likelihood of zoonoses in children.

Footnotes

Acknowledgment

This study was supported by the Research Project of the Atatürk University, Erzurum, Turkey (project no. 2007-187).

Disclosure Statement

No competing financial interests exist.

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