nueva página del texto (beta)
Inglés (pdf)
Artículo en XML
Referencias del artículo
Traducción automática
Enviar artículo por email
Citado por SciELO 
Similares en
SciELO 
Permalink
Introduction
Companion animals have been shown to play an important role in the mental and physical health of their owners (Esch & Petersen, 2013). These companion animals are the primary hosts of many endoparasites and ectoparasites, some parasites are hosted exclusively by dogs, others can be associated with livestock, and at the same time they can easily infect humans, so they are of veterinary and also human medical importance (Dantas-Torres & Otranto, 2014). Therefore, the transmission of zoonotic parasitic diseases is an emerging public health problem that requires the "One Health" approach (Fletcher et al., 2012; Lorenzo-Rebenaque et al., 2023). Globally, dogs are the most common companion animal with close contact with humans (Safarov et al., 2022), but this coexistence has allowed many parasites of veterinary interest to affect the human population due to their zoonotic potential (Amissah-Reynolds et al., 2016).
In Mexico, there are approximately 19.5 million dogs, 70 % of which live in street conditions. This population of unowned dogs is due to the usual practice of owners who allow their dogs to reproduce indiscriminately, abandoned by their owners, or offspring from unsterilized abandoned females (Alvarez, 2018). This reflects the inadequate or lack of animal protection measures that prevent the reproduction of dogs, such as permanent sterilization campaigns (Mota-Rojas et al., 2021; Cortez-Aguirre et al., 2018). The overpopulation of dogs in the streets of developing countries harms human health and safety due to physical attacks and intimidation of humans, they also pose a major risk to animal welfare (Lyons et al., 2022), as well as facilitate the transmission of zoonotic diseases (Kisiel et al., 2016), which ultimately represents a public health problem, especially due to the danger associated with the excretion of feces into the environment, which serves as an important focus of infection for humans (Lorenzo-Rebenaque et al., 2023), mainly affecting children in contact with puppies and outdoor playgrounds (Biu et al., 2012). In several cities in México, the presence of parasites in the feces of wandering dogs has been recognized, among which the most common are Ancylostoma caninum, Toxocara canis and Dipylidium caninum (De la Rosa-Arana & Tapia-Romero, 2018; Martínez-Barbosa et al., 2008; Medina-Pinto et al., 2018; Olave-Leyva et al., 2019; Vélez-Hernández et al., 2014), some of these helminth parasites are zoonotic and can be transmitted directly from these animals to the human environment without the involvement of vectors or intermediate hosts (Deplazes et al., 2011), causing diseases in humans such as visceral larva migrans caused by Toxocara canis and cutaneous larva migrans caused by Ancylostoma spp. (Idika et al., 2017). Therefore, this study aimed to investigate the prevalence of gastrointestinal parasites in dog feces and their zoonotic significance in the region of Tulancingo, Hidalgo, México.
Material and Methods
Study area
The research was conducted with samples obtained from dogs captured by the Sanitary Jurisdiction No. 2 of the Health Services of Hidalgo, located in the municipality of Tulancingo de Bravo, Hidalgo, Mexico. The study was conducted from January to June 2012. The region is located at 20° 03' 20° 13' N; 98° 14' 98° 31' W and an altitude between 2200 and 2700 masl (INEGI, 2009). The climate is semi-dry temperate (49.0 %), sub-humid temperate with summer rains, medium humidity (34.0 %), and sub-humid temperate with summer rains, higher humidity (17.0 %). It has an average annual temperature of 14 °C and rainfall ranging between 500 and 553 mm per year (SIIEH, 2011).
Sample size determination
The sample size was determined based on the proportion of parasite-positive animals (p = 0.5), assuming maximum variability, with a reliability of 0.95 and an estimation error of less than 0.1; obtaining a sample size of 96, however, 105 were collected in case of missing data, 5 dogs were sampled per week for 21 weeks, using systematic sampling with random start (Martinez, 2010).
Sample collection and analysis
All samples were collected in the morning and directly from the rectum after the sacrifice of the animals. Samples were classified based on the age and sex of the dogs. Age was determined by dentition, in two groups, young dogs up to 12 months and adult dogs older than 12 months. Approximately 5 g of feces were obtained per individual, each sample was placed in an individual plastic bag, identified, and preserved at 4° C in a portable thermos to be transported to the Laboratorio de Investigación en Parasitología of the Academic Area of Medicina Veterinaria y Zootecnia, Instituto de Ciencias Agrícolas, Universidad Autónoma del Estado de Hidalgo, for analysis. Thereafter, all samples were examined by the qualitative Flotation technique (Bowman, 2014), in NaCl-saturated solution, to detect helminth eggs and protozoan oocysts. To detect Taenia eggs and Dipylidium caninum ovigerous sacs, the Graham technique (Bowman, 2014) was performed, for which a cellulose acetate adhesive tape was placed on the anal folds of the animals. Each sample was identified and placed on a slide for analysis under a compound microscope (Zeigen brand) with 10x and 40x objectives in search of parasite eggs. The modified Ziehl-Neelsen technique was also used for the observation of Cryptosporidium spp. oocysts (Arrington, 1992).
Data were analyzed by 95 % confidence intervals (CI) (Martinez, 2010), using the chi-squared test (Fisher's exact) to determine associations between the prevalence of parasites according to the age and sex of the dogs.
Results and Discussion
The general prevalence of endoparasites in dogs
From 105 samples processed, 95.23 % were positive for parasites, identifying 8 different species of parasites, the most prevalent were Ancylostoma caninum (72.38 %, 95 % CI: 63.15-80.02) and Toxocara canis (49.52 %, 95 % CI: 40.11-58.93), the lowest prevalence were Taenia spp (1.91 %, 95 % CI: 0.52-6.68) Trichuris vulpis (0.95%, 95 % CI: 0.17-5.19) (Table 1).
Table 1 The general prevalence of gastrointestinal parasites in dog feces, Tulancingo Hidalgo, Mexico.
| Parasite by species | Positive samples (%) | CI (95%) |
|---|---|---|
| Ancylostoma caninum | 76 (72.38) | 63.15-80.02 |
| Toxocara canis | 52 (49.52) | 40.11-58.93 |
| Cryptosporidium spp | 22 (36.07) | 25.17-48.61 |
| Cystoisospora | 8 (7.62) | 3.91-14.31 |
| Uncinaria stenocephala | 8 (7.62) | 3.91-14.32 |
| Dipylidium caninum | 5 (4.76) | 2.05-10.67 |
| Taenia spp | 2 (1.91) | 0.52-6.68 |
| Trichuris vulpis | 1 (0.95) | 0.17-5.19 |
Prevalence of endoparasites by type of infection
The prevalence of endoparasites by type of infection is shown in Table 2. Multiple infection (51.5 %) was more common than single infection (43.8 %). The percentage of dogs with multiple infections of 2 and 3 parasites was 36.19 % and 12.38 %, respectively. It was observed that Toxocara canis and Ancylostoma caninum were the most prevalent parasites (17.14 %) in the association of the 2 parasites and Toxocara canis, Ancylostoma caninum, and Cryptosporidium spp were the most prevalent (17.14) in the association of 3 parasites.
Table 2 Prevalence of gastrointestinal parasites by type of infection in dog feces from the study area.
| Type of infection | Number of samples (%) | Main associated parasites (%) |
|---|---|---|
| Simple | 46 (43.80) | Ancylostoma caninum (30.47) |
| Multiple Two parasites Three parasites Four parasites Five parasites | 54 (51.5) | -- |
| 38 (36.19) | Toxocara canis-Ancylostoma caninum (17.14) | |
| 13 (12.38) | Toxocara canis-Ancylostoma caninum-Cryptosporidium spp (5.71) | |
| 2 (1.98) | -- | |
| 1 (0.95) | -- | |
| No parasite | 5 (4.76) | -- |
Prevalence of endoparasites in relation to gender and age of dogs.
No differences were observed in the prevalence of the different parasite species between females and males (p > 0.05; Table 3). In the case of prevalence with age, 42.86 % and 6.67 % of the samples from young and adult dogs were positive for Toxocara canis, respectively (p < 0.01).
The overall prevalence of gastrointestinal parasites, 95.23 %, of the present study, is similar to the reported 8 5% of parasitosis in unowned dogs in Mexico City (Eguía-Aguilar et al., 2005), the lower prevalence in unowned dogs, has been reported in the Mexicali Valley, Mexico (Trasviña-Muñoz et al., 2020), as well as around the world, such as Morocco 58 % (Idrissi et al., 2022), Ghana 66.7 % (Amissah-Reynolds et al., 2016), and Japan 39.2 % (Kimura et al., 2013). The high prevalence of endoparasites in this study is partly due to the lack of veterinary management as these are unowned animals. In addition to environmental factors, specific to the site such as relative humidity, ambient temperature, and bioclimatic factors that favor or diminish the development and transmission of gastrointestinal parasitosis (Biu et al., 2012; Trasviña-Muñoz et al., 2020). However, high prevalence rates are also found in owned dogs, which may be due to a lack of knowledge of zoonotic parasites by dog owners, lack of veterinary services in the study area, low level of hygiene by dog owners, and generally poor socio-economic conditions prevailing in the study area (Idrissi et al., 2022; Moro & Abah, 2019). Regardless of the conditions in which dogs are found, high prevalence rates represent a serious threat to public health, especially in socioeconomically disadvantaged communities, although, countries such as Spain have presented an overall prevalence of parasites of 65.8 % (Sánchez-Theven et al., 2019), United States with 20.7 % (Stafford et al., 2020) and Italy with prevalence to helminths of 29. 1 % (Scaramozzino et al., 2018), which denotes the indisputable problem in both street animals and owned dogs, representing a public health risk worldwide.
Among the parasites with the highest prevalence in this study were Ancylostoma caninum and Toxocara canis. These parasites are the main etiological agents causing parasitic zoonoses worldwide, mainly affecting children and adolescents, especially in impoverished communities (Chen et al., 2018). In countries such as Nigeria, high incidences have also been reported for these parasites ranging from 33.6 to 51.9 % and 20 to 27.3 %, respectively (Biu et al., 2012; et al., 2017). Also, Lorenzo-Rebenaque et al. (2023) reported a Spain prevalence of 3.0 % and 17 % for Ancylostoma caninum and Toxocara canis, respectively. Regardless of such reported prevalence percentages, the presence of cutaneous larva migrans in the feces of dogs infected with the Ancylostoma parasite, may infect humans if larvae penetrate the skin when walking barefoot on contaminated soil (Idika et al., 2017), although other parts of the body that are exposed can be affected by this parasite (Pereda et al., 2016). Ancylostoma caninum is of special interest among zoonotic parasitosis since it is one of the most commonly found parasitic species in the feces of free-roaming dogs (Lyons et al., 2022). This pathogen has been found in common environments for humans, such as water, soil, food, and parks, and contamination with dog feces, representing a high risk for the population (Romero et al., 2015).
Moreover, toxocariasis in dogs is one of the most common zoonotic parasitosis in both urban and rural areas and it is known that rural dwellers have low awareness of the potential threat of zoonotic parasites (Gawor et al., 2015), this becomes of greater importance in developing countries where unowned dogs can spread Toxocara eggs in the environment such as public parks and playgrounds, serving as the main source of soil contamination, increasing the risk of human exposure to infectious eggs (Chen et al., 2018). The clinical manifestations caused by toxocariasis in humans are visceral (visceral larva migrans), ocular (ocular larva migrans), neurotoxocariasis and common toxocariasis. Toxocara canis is one of the most widespread public health and economically important zoonotic parasites shared by humans and dogs (Macpherson, 2013).
On the other hand, multiple infection was more common than single infection, contrary data were reported by (Amissah-Reynolds et al., 2016) who report a prevalence of 42.2 % in single infection and 10.4 % in multiple infection, and mentioned that the interaction between parasite species depends more on the parasite load than on the presence of other parasite species alone (Ugbomoiko et al., 2008). In general, there was no statistical difference between single and multiple infections, nor between the main associated parasites. In this sense, it is mentioned that the mere fact of presenting a high prevalence of multiple infections represents an important role in the epidemiology of parasitic diseases because it reveals the proportion of dogs that require combined pharmacological treatment (Fontanarrosa et al., 2006), which in the case of Tulancingo, Hidalgo was more than 50 % of the animals.
Prevalence of endoparasites between females and males showed no differences, however, the prevalence of Toxocara canis was higher for young dogs compared to adult dogs, since this parasite is vertically transmitted through pregnant bitches that harbor somatic larvae infecting up to 100 % of their puppies by transplacental route, trans mammary (lactogenic) or horizontally through ingestion of embryonated eggs from the environment or ingestion of larvae through vertebrate and/or invertebrate paratenic hosts (Schnieder et al., 2011; Macpherson, 2013; Gawor et al., 2015).
Table 3 Prevalence of gastrointestinal parasites in relation to the sex and age of the dogs in the study area.
| Variable | Females (%) | Males (%) | Young (%) | Adults (%) |
|---|---|---|---|---|
| Positive samples/processed samples Percentage (95 % CI) | 65/69 94.20 (88.68-99.72) | 34/36 94.44 (86.95-101.92) | 52/54 96.29 (91.25-101.33) | 47/51 92.15 (84.77-99.53) |
| Ancylostoma caninum | 51 (48.57) | 25 (23.81) | 39 (37.14) | 37 (35.24) |
| Toxocara canis | 35 (33.33) | 17 (16.19) | 45 (42.86)a | 7 (6.67)b |
| Cryptosporidium spp | 15 (24.59) | 7 (11.48) | 15 (24.59) | 7 (11.48) |
| Cystoisospora | 4 (3.81) | 4 (3.81) | 5 (4.76) | 3 (2.86) |
| Uncinaria stenocephala | 7 (6.67) | 1 (0.95) | 6 (5.71) | 2 (1.90) |
| Dipylidium caninum | 3 (2.86) | 2 (1.90) | 3 (2.86) | 2 (1.90) |
| Taenia spp | 1 (0.95) | 1 (0.95) | 0 (0) | 2 (1.90) |
| Trichuris vulpis | 1 (0.95) | 0 (0) | 1 (0.95) | 0 (0) |
ab Different letters, between females and males or between young and adults, indicate a difference (p < 0.01).
Conclusions
As in other parts of the country and the world, in Tulancingo Hidalgo, Mexico, a high prevalence of gastrointestinal parasites was observed, among which there are species with zoonotic importance, which represents a public health problem mainly affecting children. Therefore, necessary to develop functional public policies focused on "One Health" for developing countries, especially in marginalized areas, in addition to raising public awareness about the presence of unowned dogs roaming free and serving as vectors of diseases that affect humans.
