INTRODUCTION

Animals represent a way of life for much of the world, so the closeness between people and pets has created a special relationship known as the human-animal bond. Dogs provide benefits such as emotional development, socialization and physical well-being (^{Paul et al., 2010}). Around the world the number of urban households that maintain "domestic dogs" has increased and this trend increases the frequency of human-animal companion contact (^{Bwalya et al., 2011}).

It is known that dogs can be reservoirs of intestinal nematodes with zoonotic potential (^{Moskvina y Ermolenko, 2016}; ^{Medina-Pinto et al., 2018}), such as, Taenia spp. (^{Beiromvand et al., 2018}), Dipylidium caninum, Ancylostoma spp., Giardia spp., Cryptosporidium sp. (^{Soriano et al., 2010}) or Toxocara canis (^{Chen et al., 2018}). These represent a potential public health risk, with a significant socio-economic impact, particularly in impoverished communities (^{Chen et al., 2018}) and in children; since they have more direct and indirect contact with dogs, compared to adults (^{Xhaxhiu et al., 2011}).

In the Mexican Republic, specifically in Mexico City, Toxocara canis and Ancylostoma caninum have been as the most frequent parasites reported, in dog feces (^{Eguia-Aguilar et al., 2005}). Other studies conducted in Chiapas states (^{Martínez-Barbosa et al., 2008}) y Yucatán, México (^{Medina-Pinto et al., 2018}) (^{Martínez-Barbosa et al., 2008}) and Yucatán, México (^{Medina-Pinto et al., 2018}) position Toxocara canis and Ancylostoma caninum among the most frequent parasites in dog feces, which roam the parks and streets of these towns. On the other hand, ^{Vélez-Hernández et al. (2014)} also mentions Dipylidium caninum as a parasite of high prevalence in feces, collected from the soil, from wandering and owner dogs from Puerto Escondido, Oaxaca, Mexico. All these pathogens can be in the human environment found, such as water, soil, food, parks and contamination by dog feces, which represents a high risk for people (^{Romero et al., 2015}). However, in the municipality of Tulancingo de Bravo, Hidalgo, no studies have been in this regard, conducted.

The objective of this study was to determine the prevalence of gastrointestinal helminths in dogs from the Health Services in Tulancingo, Hidalgo and their possible relationship as zoonosis.

MATERIAL AND METHODS

Place of study

The investigation was during the months of January to July 2012 conducted, with samples obtained from dogs slaughtered in the Health Jurisdiction No. 2 of the Health Services of Hidalgo State, located in Tulancingo de Bravo municipality, Hidalgo, Mexico. The region is geographically located between parallels 20° 03' and 20° 13' of North Latitude; the meridians 98° 14’ and 98° 31’ west longitude, and an altitude between 2200 and 2700 m a.s.l. It has a climate ranging from semi-dry temperate subhumid with rains in summer, too mild subhumid with rains in summer (^{INEGI, 2009}).

Sample size

The sample size was determined based on the proportion of positive animals to parasites (P=0.5), assuming maximum variability; with a reliability of 0.95 and an estimation error of less than 0.1. The result was to take 96 samples; however, it was to 100 samples adjusted, because Sanitary Jurisdiction No. 2 performs the sacrifice of dogs only once a week, so samples of 5 dogs were taken per week for 20 weeks. Samples from partial digestive tracts were obtained using systematic sampling with random start (^{Martínez, 2010}).

Collection and analysis of samples

After the slaughtering of the animals, the esophagus, stomach and small intestine were obtained. Each gastrointestinal tract (TGI) was in relation to the age and sex of each dog, classified. Age classification was performed by teething, in two categories; young animals up to 12 months of age and adult animals older than 12 months. Subsequently, the TGI were placed in plastic trays and were taken to the Parasitology Research Laboratory of the Academic Area of Veterinary Medicine and Zootechnics, Institute of Agricultural Sciences, Autonomous University of Hidalgo State. All the TGI were dissected longitudinally to collect the intestinal content, subsequently this content was examined in a dark-bottomed tray to highlight the parasites. The helminths were washed in physiological saline solution (SSF) and identified by their morphological characteristics, using a stereoscopic microscope (UPSEHKRAFT brand), with 10x and 40x objectives and an optical microscope (IROSCOPE brand, model WB-3) with the objective 10x (^{MAFF, 1986}).

Data analysis

Sample data were analyzed at a 95% confidence interval (CI) (^{Martínez, 2010}), using the chi-square test (Fisher's exact), to compare the prevalence of the various parasites according to the classes of dogs, forming groups according to age and sex.

RESULTS

Prevalence of helminths in dogs

From the 100 samples processed, 84% (95% CI: 75.57-89.90), were positive for some helminth. Six different species of helminths were found (Table 1), the most prevalent were Toxocara canis (53%; 95% CI: 42.28-62.48) and Ancylostoma caninum (50%; 95% CI: 40.38-59.61); those with the lowest prevalence were Uncinaria stenocephala (10%; 95% CI: 5.52-17.43) and Spirocerca lupi (1%; 95% CI: 0.17-5.44).

Prevalence of helminths in relation to the sex and age of dogs

In the prevalence of helminths by sex, 68 digestive tracts were female, of which 88.23% were positive for some helminth and 32 digestive tracts were male, with 75% positive for some parasite (Table 2) (P> 0.05). The prevalence of Dipylidium caninum was 47.06% in females and 25.02% in males (P <0.02).

On the other hand, for the prevalence of helminths in relation to the age of the animals, was obtained that 88.88% of young dogs and 80% of animals older than one year of age were positive for some helminth (P> 0.05). In addition, the prevalence of Toxocara canis was 71.11% in young animals and 38.18% in adult animals (P <0.02). On the other hand, the prevalence of Taenia spp was 4.44% and 25.45%, for young and adult dogs, respectively (P <0.05). Finally, in relation to Uncinaria stenocephala the prevalence was 2.22 and 16.36 for young and adult dogs, respectively (P <0.05).

DISCUSSION

The prevalence of helminths in the present study (84%) is similar to studies conducted in dogs in Mexico; Querétaro with 78.60% (^{Fernández y Cantó, 2002}) and 72.8% (^{Canto et al., 2011}), Mexico City with 85% (^{Eguia-Aguilar et al., 2005}); as well as in other regions of the world such as Zambia with 78.3% and sub-Saharan Africa with 71% (^{Chidumayo, 2018}). The high prevalence of parasites could be, because the samples examined belonged to dogs without owners, or that they came from canine rabies control centers; in whose cases they are not subject to deworming programs. However, in Zambia, ^{Bwalya et al. (2011)} also reported a high prevalence of helminths in dogs with owners (78.3%).

These authors point out that it is an important finding, since it emphasizes that there is no care for pets with respect to helminth control through regular deworming. ^{Romero et al. (2015)} and ^{Idika et al. (2017)}, presented parasite prevalence of 13.10% and 51.7%, respectively. This low prevalence could be because of the processed samples came from dogs with owners, which are regularly subject to control and prevention treatments for parasitic diseases. On the other hand, ^{Trasviña-Muñoz et al. (2017)}, reported a general prevalence of 21.5%. These researchers mention that the low prevalence could be due to the climate of the place of study, where they have temperatures that vary from 36 °C to 50 °C, with low humidity, which can delay or even suppress the development of parasite eggs.

The helminths found according to the order of prevalence were Toxocara canis, Ancylostoma caninum, Dipylidium caninum, Taenia spp, Uncicaria stenocephala and Spirocerca lupi, which generally coincides with the findings of ^{Fernández y Cantó (2002)} and ^{Eguia-Aguilar et al. (2005)}. Dogs are the main transmitters of toxocariasis to men especially in developing countries, where most have access to public parks and playgrounds, which serve as the main source of soil contamination and represent a great risk of human exposure to Toxocara eggs (^{Chen et al., 2018}). Similarly, the larvae of Toxocara canis can pass through the feces of infected animals, and humans can become infected with these larvae when they work with soil or play in contaminated areas. This infection seems to be more prevalent in children and in socioeconomically disadvantaged populations, due to inconsistent hygiene practices (^{Chen et al., 2018}).

In the present investigation, a high prevalence was found for Ancylostoma caninum, which is important since the presence of Ancylostoma larvae or hookworm in dog feces can infect humans, which impacts on public health. Ancylostoma larvae can penetrate the skin when walking barefoot in a contaminated soil, and although they cannot reproduce in the human body, they produce red papular lesions that move under the skin as the larvae migrate. Clinically it manifests itself by severe itching, especially at night (^{O'Neil, 2018}).

Dipylidium caninum was the most prevalent cestode of the present study, which is consistent with the high prevalence reported in studies conducted in Querétaro, Mexico (^{Canto et al., 2011}) and Mexico City, Mexico (^{Eguia-Aguilar et al., 2005}). This prevalence could be due to the increase in stray dogs that do not receive any type of antiparasitic treatment, and consequently, they are with fleas and lice frequently infested, which can be intermediaries of Dipylidium caninum. When the canine host ingests infected adult fleas, the cystecercoid is released in the stomach, subsequently settling in the small intestine of its definitive host (^{Beugnet et al., 2018}; ^{Labuschagne et al., 2018}); however, fleas can occasionally infect humans, especially children living with pets, who do not have veterinary control for ectoparasites (^{Neira et al., 2008}; ^{Ayala et al., 2012}).

The second cestode found in the present investigation was Taenia spp., with a prevalence of 16%; which is less than 25.7% reported in feces collected from dogs from rural areas of Khuzestan, province of Iran (^{Beiromvand et al., 2018}). The importance of Taenia spp., is that the domestic dog can be a definitive host when acquiring the infection, by consuming the carcasses removed from infected herbivorous domestic animals; mainly sheep carcasses (^{Beiromvand et al., 2018}). The sheep, the cattle (^{Alemu et al., 2015}) and less commonly the human being, can be intermediate hosts, after the ingestion of eggs of these parasites (^{Sonmez et al., 2017}).

The general prevalence of helminths was similar among young and adult animals. However, young dogs had a higher prevalence of Toxocara canis; This may be because the most important form of Toxocara canis infection in dogs is the prenatal transmission of larvae; also known as transplacental or intrauterine transmission (^{Schnieder et al., 2011}), where female dogs that harbor somatic larvae can infect up to 100% of newborn puppies (^{Gawor et al., 2015}). A higher prevalence was also found in adult animals for Uncinaria stenocephala. This parasite is one of the agents related to cutaneous parasitosis in humans, known as a completely as cutaneous migrans larva. This zoonosis occurs especially in areas where there are dogs and cats without owners, as well as in sandy and humid soils, such as beaches and recreational parks (^{Plascencia et al., 2013}); This explains the relatively low prevalence of this nematode in the present investigation.

The prevalence of Taenia spp was higher in adult animals; ^{Fernández y Cantó (2002)} reported contrary data. The highest prevalence in adult animals of the present study may be because adult animals may acquire the infection by consuming the infected animal carcasses (^{Beiromvand et al., 2018}).

The results of prevalence of helminths by sex of dogs show no difference; however, the prevalence of Dipylidium caninum was higher in females than in males; Similar data were reported by (^{Chávez et al., 2012}), who mentions that females are more prone to Dipylidium caninum. In this sense, ^{Hernández et al. (2007)}, mention that the general prevalence of Dipylidium caninum is higher during the coldest time of the year. It is probably because stray dogs usually congregate in greater numbers, to seek refuge from colder temperatures; which facilitates the propagation of vectors, by increasing promiscuity among them and consequently the chances of infection with Dipylidium caninum are increased.

The present study was carried out during the period of greatest reproductive activity in the dog, which runs from March to July (^{Choy y Echevarría, 2005}), so it is possible that in our case, the females had a higher prevalence of Dipylidium caninum, due to the contact they have with parasitized male flea dogs.

CONCLUSIONS

High prevalence of gastrointestinal helminths of dogs from the Health Services of Tulancingo de Bravo, Hidalgo, Mexico was observed; which demonstrates the public health risk that mean dogs without owners that roam the streets. Some of the parasites found have a high risk of zoonosis, so it is necessary to implement awareness campaigns for the general population, about the responsible possession of companion animals, such as dogs.