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Abanico veterinario
versión On-line ISSN 2448-6132versión impresa ISSN 2007-428X
Abanico vet vol.11 Tepic ene./dic. 2021 Epub 04-Abr-2022
https://doi.org/10.21929/abavet2021.39
Original Article
Prevalence of parasites in dog´s feces of Gomez Palacio, Durango, Mexico
1Laboratorio de Bioindicadores. Centro de Investigación y Jardín Etnobiológico, Universidad Autónoma de Coahuila, Dr. Francisco González 37, Viesca, Coahuila, México. CP. 27480.
2Facultad de Ciencias Biológicas, Universidad Juárez del Estado de Durango, Av. Universidad S/N, Fraccionamiento Filadelfia, Gómez Palacio, Durango, México. C.P. 35010.
3Laboratorio de Parasitología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Carretera a Xmatkuil Km. 15.5, Yucatán, México. C.P. 97000.
The aim of the present study was to estimate the prevalence of parasites and identify the ones with the zoonotic potential present in the feces of household’s dogs and stray dogs in Gomez Palacio, Durango, Mexico. Fifty fecal samples from household dogs and 50 fecal samples from stray dogs were collected and analyzed by sucrose flotation and McMaster techniques. The statistical analyzes showed a significant difference between households and stray dogs (p= 0.021). The highest prevalence was obtained by stray dogs with 22% (11/50), while household’s dogs got a majority of 6% (3/50). The parasites of morphologically identified household dogs corresponded to Cystoisospora canis (6%) and Trichuris vulpis (4%), while in stray dogs parasites corresponded to Ancylostoma spp. (12%), Cystoisospora canis (10%), Toxocara spp. (4%), Trichuris vulpis (4%), and Taenia spp. (2%). The Chi-square (X2) analysis showed that the prevalence of parasites in stray dogs according to age presented a significant difference (p= 0.002); 100% of the puppies were parasitized. In Gomez Palacio, parasites with zoonotic potential are present in the feces of households and stray dogs, representing a risk of infection for the human population.
Keywords: stray dogs; household dogs; zoonosis; parasitism; public health
El objetivo del presente estudio fue estimar la prevalencia e identificar los parásitos con potencial zoonótico presentes en las heces fecales de perros domiciliarios y callejeros de Gómez Palacio, Durango, México. Se colectaron 50 muestras de heces fecales de perros domiciliarios, así como 50 muestras de heces fecales de perros callejeros. Las muestras se analizaron mediante las técnicas de flotación por sacarosa y de McMaster. Los análisis estadísticos mostraron diferencia significativa entre las prevalencias de perros domiciliarios y callejeros (p= 0.021). La mayor prevalencia la obtuvieron los perros callejeros con 22% (11/50), mientras que los perros domiciliarios obtuvieron una prevalencia del 6% (3/50). Los parásitos de perros domiciliarios identificados morfológicamente correspondieron a Cystoisospora canis (6%) y Trichuris vulpis (4%), mientras que los parásitos de perros callejeros correspondieron a Ancylostoma spp. (12%), Cystoisospora canis (10%), Toxocara spp. (4%), Trichuris vulpis (4%) y Taenia spp. (2%). El análisis de Chi-cuadrada (X2) mostró que la prevalencia de parásitos en perros callejeros presentó diferencia significativa entre edades (p= 0.002), el 100% de los cachorros resultó parasitado. En Gómez Palacio se encuentran parásitos con potencial zoonótico presentes en las heces de perros domiciliarios y callejeros lo que representa un riesgo de infección para la población humana.
Palabras clave: perros callejeros; perros domiciliarios; zoonosis; parasitismo; salud pública
INTRODUCTION
The dog (Canis lupus familiaris) has been in close contact with humans since its domestication process. It currently plays an important role in our lives, since it is not only a companion animal, but also helps us in different activities, performing rescues, serving as a guide for blind people, participating in the detection of drugs and explosives (Macpherson et al., 2013) and even the influence of dogs is used in the treatment of patients with pathological shyness, emotional disorders, lack of sociability and autism (Zapata et al., 2015). This close interaction between humans and dogs has resulted in the possible acquisition of zoonotic diseases (Macpherson et al., 2013).
Dogs are related to 60 zoonoses, among which those of parasitic origin stand out (Hernández et al., 2019). Through feces, dogs can transmit zoonotic diseases to humans (Johnson et al., 2015) when the latter have contact with contaminated food, objects, water, air or soil (Desachy, 2016). Different studies conducted in Mexico and worldwide show that the parasite genera with the highest prevalence are Toxocara spp. and Ancylostoma spp. (Rodríguez-Vivas et al., 2001; Romero-Núñez et al., 2011; Solarte-Paredes et al., 2013; Kaminsky et al., 2014; Vega et al., 2014; González et al. 2015; Huerto et al., 2015; Delgado-Fernández, 2017; Peña et al., 2017; Plúas-Hurtado & Sánchez- Hernández, 2021). In turn, the most reported zoonotic parasite species are Ancylostoma caninum and Toxocara canis (Encalada-Mena et al., 2011; Vélez-Hernández et al., 2014; Idika et al., 2017; Sarmiento-Rubiano et al., 2018; Lara-Reyes et al., 2019; Olave-Leyva et al., 2019; Silva et al., 2020). Other parasites reported in dogs in Latin America are Ascaris lumbricoides (Acosta-Jurado et al., 2017), Cystoisospora spp. (Gorman et al., 2006), Dypylidium caninum (López et al., 2006; Cisneros et al., 2020), Echinococcus granulosus (Chuiquisana et al., 2014), Spirocerca lupi (Rodríguez-Vivas et al., 2019), Strongyloides spp. (Llanos et al., 2010; Diaz-Anaya et al., 2015) and Taenia spp. (Fernández-Campos & Cantó-Alarcón, 2002; Luzio et al., 2017), among others.
Canine fecal waste represents an important public health problem, due to the risk of transmission of zoonotic risk parasites; since not only people who have pets are exposed to contracting a disease, but all people are. In Mexico City, it is estimated that at least five tons of feces from stray dogs end up being sprayed daily in the environment, as well as from dogs of irresponsible owners (Zúñiga-Carraco & Caro-Lozano, 2020), who do not have the culture or precaution to pick up their biological waste.
The purpose of this research was to estimate the prevalence of parasites present in the feces of household and stray dogs in Gómez Palacio, Durango, Mexico, through a descriptive epidemiological study; as well as to identify those with zoonotic potential.
MATERIAL AND METHODS
Study site
The study was conducted in the municipality of Gómez Palacio, Durango, Mexico, which is located at coordinates 25°32'8.16" and 25°53'16.8" North Latitude and 103°41'24" and 103° 19'8.4" West Longitude, altitude between 1100 and 1800 m a.s.l. It has an average temperature range of 18-22°C and an annual rainfall of 100-400 mm; it has a very dry semi-warm climate (BS0hw), with rainfall in summer (INEGI, 2010).
Collection and analysis of fecal samples
Fifty fecal samples were collected from household dogs. Contact with dog owners was made at a Veterinary Clinic in Gómez Palacio municipality, Durango; as well as at the Faculty of Biological Sciences of the Universidad Juárez del Estado de Durango (UJED) during the months of August to November 2016. A fecal sample was taken in plastic jars given to the owners that were asked for fresh samples and the upper portion to avoid contamination with soil and to be transported in coolers at a temperature of approximately 4°C for later analysis. A survey was made to each owner to find out the sex, age, health, grooming and data about the nutrition, condition and general health of their pets. Prior to the survey, owners were asked for their consent and the data obtained were handled confidentially.
A collection of 50 fecal samples from stray dogs was also performed in five neighborhoods (Carlos Herrera, 5 de mayo, La Feria subdivisions, Hamburgo and Benito Juárez) of Gómez Palacio, Durango, during the months of August to October 2017. Samples were taken in plastic jars with 5% formalin, waited for dogs to defecate in the streets, proceeded to take the sample from the top and then transported to the Faculty of Biological Sciences of the UJED to perform the corresponding analyses. Age classification was done by dentition in three categories: puppies (under 6 months of age), young (6 months to 2 years of age) and adults (older than 2 years of age) (Malloy & Embil, 1978). The sucrose flotation method was used to analyze the fecal samples (Dryden et al., 2005) and the McMaster technique was used to quantify the parasite load (Cruz-Reyes et al., 2001). A total of 100 fecal samples were analyzed. This number was chosen based on the literature and because there are no official publications on the number of stray dogs in Gómez Palacio, Durango.
Data analysis
The Test of Independence (Contingency Tables 2x2 and rxc) with significance level of p<0.05 was used in the PASW Statistics 18 program.
RESULTS
Prevalence of parasites in household and stray dogs
This study showed that, in the Gómez Palacio city, Durango, Cystoisospora canis was the most prevalent parasite in household dogs, followed by Trichuris vulpis. In stray dogs, Ancylostoma spp. was the most prevalent parasite, followed by Cystosospora canis, Toxocara spp, Trichuris vulpis and finally Taenia spp. Only one parasite with zoonotic potential was found in household dogs: Trichuris vulpis, while four parasites with zoonotic potential were found in stray dogs: Ancylostoma spp, Taenia spp, Toxocara spp. and Trichuris vulpis. Table 1 shows the frequency and prevalence of each.
Table 1 Frequency and prevalence of parasite eggs and oocysts found in feces of household and stray dogs in Gómez Palacio city, Durango
HOUSEHOLD DOGS | ||
---|---|---|
Parasite | Frequency | Prevalence |
Cystoisospora canis | 3 | 6.00 |
Trichuris vulpis | 2 | 4.00 |
STRAY DOGS | ||
Parasite | Frequency | Prevalence |
Ancylostoma spp. | 6 | 12.00 |
Cystoisospora canis | 5 | 10.00 |
Taenia spp. | 1 | 2.00 |
Toxocara spp. | 2 | 4.00 |
Trichuris vulpis | 2 | 4.00 |
Prevalence in household and stray dogs based on sex and age
Regarding prevalence by age in household dogs, the highest prevalence was obtained in dogs under 6 months of age (12.5%) and according to sex, males obtained a prevalence (8.33%). In stray dogs, the highest prevalence was obtained in dogs under 6 months of age (100%) and according to sex, very similar results were obtained for females (25%) and males (20.5%) (Table 2).
Table 2 Prevalence in household and stray dogs in Gómez Palacio, Durango, according to sex and age variables
HOUSEHOLD DOGS | |||
---|---|---|---|
Variable | Total | Positive to parasites | Prevalence |
Age | |||
< 6 months | 8 | 1 | 12.50 |
6 months to 2 years | 14 | 0 | 0.00 |
> 2 years | 28 | 2 | 7.14 |
Sex | |||
Females | 26 | 1 | 3.84 |
Males | 24 | 2 | 8.33 |
STRAY DOGS | |||
Variable | Total | Positive to parasites | Prevalence |
Age | |||
< 6 months | 3 | 3 | 100.00 |
6 months to 2 years | 2 | 1 | 50.00 |
> 2 years | 45 | 7 | 15.55 |
Sex | |||
Female | 16 | 4 | 25.00 |
Males | 34 | 7 | 20.50 |
Prevalence of parasites in feces of stray dogs by neighborhood
In stray dogs, neighborhoods with the highest prevalence of parasites in feces were La Feria subdivisions and 5 de mayo, with 30% and 28.57%, respectively (Table 3). In La Feria subdivisions, Toxocara spp. and Taenia spp. parasites were found, which have zoonotic potential; in addition to being the neighborhood with the highest prevalence of intestinal parasites; while in 5 de mayo neighborhood the greatest variability of parasites was found, with Cystoisospora canis, Ancylostoma spp. In the Hamburgo neighborhood, only the parasite Ancylostoma spp. was found, and finally, in the Carlos Herrera neighborhood, Cystoisospora canis and Trichuris vulpis were found.
Table 3 Prevalence of parasites in stray dogs by sampling site.
Neighborhood | Total n= 50 | Parasite-positive samples | Prevalence |
---|---|---|---|
Carlos Herrera | n= 11 | 2 | 18.18 |
5 de mayo | n= 14 | 4 | 28.57 |
La Feria Fraccionamiento | n= 10 | 3 | 30.00 |
Hamburgo | n= 10 | 2 | 20.00 |
Benito Juárez | n= 5 | 0 | 0 |
**Prevalence was obtained taking into account parasite positive samples and the total number of samples per neighborhood.
In the case of household dogs, the Hamburgo neighborhood had the highest prevalence of parasites in feces with 25% and only Cystoisospora canis was found; while in the La Feria neighborhood with 11.11% and Miravalle with 10% prevalence, the same parasite (Trichuris vulpis), which has zoonotic potential, was found.
A significant difference was found between the prevalence of parasites in the feces of household dogs and stray dogs (p=0.021). Six percent of the household dogs were parasitized, while 22% of the stray dogs were parasitized.
Regarding the prevalence of household and stray dogs by sex, no significant differences were found (p>0.05).
When analyzing the parasitic infection prevalence in household dogs by age class, no significant differences were found (p=0.459); however, in stray dogs significant differences were found (p=0.002), 100% of puppies were parasitized, 50% of juveniles and 15.6% of adults.
DISCUSSION
The prevalence of parasites in feces found in this study for household dogs (6%) differs from that found by Ruvalcaba et al. (2012) in Zacatecas and by Rodríguez-Vivas et al. (2011) in Yucatán (94.7% and 80%, respectively). These differences could be due to the fact that the study conducted in Zacatecas covered the four seasons of the year and different diagnostic techniques were used; in addition to the fact that both investigations were conducted in rural areas, where there is a lesser culture of disease prevention in animals and dogs generally have access to the street and coexist with stray dogs and other animals; in contrast to the present work in which the dogs are from an urban area and have more limited access to public areas. Regarding the prevalence of parasites for stray dogs (22%) is similar to results found by Trasviña-Muñoz et al. (2017) in Baja California Norte and García-Hinojosa et al. (2018) in Chihuahua (21.5% and 25% respectively), this could be because their studies conducted in urban areas where there is more prevention in the care of pets, and differs from that reported by Alvarado-Esquivel et al. (2015) in Veracruz (98%). These differences could be due to the fact that the study site was a dog shelter, where there is greater spread of parasites due to proximity, cleanliness, nutritional conditions, among other factors.
With respect to the prevalence based on sex and age in stray and household dogs, the highest prevalence in both cases was in dogs under 6 months of age (100% and 12.5% respectively) and according to sex, females had a higher prevalence of stray dogs with 25% and in the case of house dogs, males had the highest prevalence with 8.33%. It differs to Rodríguez-Vivas et al. (2011), Ruvalcaba et al. (2012), Alvarado- Esquivel et al. (2015), Trasviña-Muñoz et al. (2017) and García- Hinojosa et al. (2018), because none evaluated prevalence based on sex and age but very similar to what was obtained by Plúas- Hurtado & Sánchez- Hernández, (2021) who obtained prevalences of 46.9 % of parasitosis in dogs aged 0-24 months. This could be due to the fact that puppy dogs are more susceptible to parasites due to feeding problems, developing immune system, among others.
Cystoisospora canis was the most prevalent parasite in domiciliary dogs (6%), and was also found in stray dogs (10%) in the present work, which differs from Sierra-Cifuentes et al. (2015) in Colombia where a prevalence of 4.4% was obtained for this parasite; this may be because the study was conducted in a canine welfare center where its inhabitants at some period of the year have a preventive antiparasitic control that could have avoided the presence and parasite spread.
Another parasite found in household and stray dogs was Trichuris vulpis, with a prevalence of 4% in this work, which differs from that mentioned by Torres-Chablé et al. (2015), in Tabasco (0.3%) with household dogs; while Medina-Pinto et al. (2018) in Yucatán and Vélez-Hernández et al. (2014) in Oaxaca (1% and 1.1%, respectively) in stray dogs: on the other hand, high prevalences are reported by Rodríguez-Vivas et al. (2011) in Yucatán (25.4%) with household dogs and Alvarado-Esquivel et al. (2015) in Veracruz (18.8%) with stray dogs. In the case of the low prevalences reported in Yucatán and Oaxaca, it should be noted that both works were carried out in areas with the presence of domiciliary dogs, which could explain the low values reported; however, in the case of Oaxaca, high values were presented in the general prevalence and in the other parasites found. This could be explained because the prepatency period of Trichuris vulpis is relatively long, approximately three months; in addition, egg shedding is not constant (Birchard et al., 2006), so it is recommended to repeat the analysis of several different stool samples (Galán et al., 2019). This could also explain the low prevalences reported in Tabasco and in the present study.
Regarding the high prevalences reported in Yucatan and Veracruz, authors mention that both studies were conducted in rural areas, which could influence the results; in addition to other factors such as humidity and temperature that could have favored egg development at the time of the study. In house dogs in Italy, La Torre et al. (2018) reported similar results to the present work (5.5%); while in stray dogs, Sierra-Cifuentes et al. (2015) reported higher results (16.2%) in Colombia. Human infections with Trichuris spp. are usually accidental by ingesting embryonated eggs in contaminated food and water or by geophagy (Rodríguez-Vivas et al., 2001).
On the other hand, the most prevalent parasite in stray dogs was Ancylostoma spp. (12%), which is very similar to other works in some Mexican states, where this parasite has also been reported as the most prevalent, as in Medina-Pinto et al. (2018) in Yucatan (10%), but lower than that reported by Alvarado-Esquivel et al. (2015) in Veracruz (88.1%). The difference found could be attributed to the fact that in the research conducted in Veracruz, most of the dogs were of rural origin; while in the study conducted in Yucatan dogs corresponded to urban origin. Prevalences ranging from 0.8% to 62.5% are reported in other countries (Johnson et al., 2015; Sierra-Cifuentes et al., 2015; Idika et al., 2017; Kidima, 2019; Silva et al. 2020; Sulieman et al. 2020).
Statistical analyses showed significant difference between the frequencies of domiciliary and stray dogs parasitized (p=0.021). Household dogs showed a prevalence of 6%, while stray dogs showed a prevalence of 22%. In a study conducted in Medina-Pinto et al. (2017) found that feces collected in parks where stray dogs were observed were more likely (p=0.046), to be positive for parasite eggs than in parks where owned dogs were observed. These differences may be due to the fact that stray dogs do not have preventive health management and that they have free access to areas where there are high rates of parasite egg and larval contamination, which can cause infections and re-infections. To determine these factors more precisely, it is proposed that risk factor analyses be carried out in future studies.
The parasite Toxocara spp. was found in stray dogs with a prevalence of 4% in this work, similar to some works in Mexico where it has been reported in prevalence ranges from 0.23% to 59.6% (Ruvalcaba et al., 2012; Torres-Chablé et al., 2015; Hernández et al., 2019). In Africa, Johnson et al. (2015), have reported it with a prevalence of 5.8% for domiciliary dogs, while in Portugal Silva et al. (2020) reported it with a prevalence of 29% for stray dogs. The low prevalence in household dogs may be due to the fact that their owners comply with the responsibility of supplying dewormers to their pets, and in the case of stray dogs the prevalences tend to be higher, due to several environmental and anthropic factors to which they are exposed and that propitiate unfavorable environments for the reproduction and propagation of parasites.
Taenia spp. was found with a prevalence of 2% for stray dogs in this work, similar to that reported in our country by Trasviña-Muñoz et al. (2017) in Baja California Norte, where they reported prevalences of 3.9%; while in Hidalgo, Olave-Leyva et al. (2019), report it with prevalences of 16%. These differences may be due to the high temperatures and low humidity that occur in Baja California Norte, compared to Hidalgo, factors that intervene with the presence and development of this parasite. In Oklahoma it has been reported with a percentage of 0.47% (Nagamori et al., 2020) in household dogs, while in stray dogs in Colombia and Sudan prevalences of 4.4% and 6.7% are reported, respectively (Sierra-Cifuentes et al., 2015; Sulieman et al., 2020).This could be due to the fact that in the areas of Colombia and Sudan where the studies were conducted there was a high presence and spread of the parasite; in addition to the fact that perhaps the canine hosts reviewed were susceptible to infection. In other studies that have been conducted in the world, this parasite has not been reported (Johnson et al., 2015; Idika et al., 2017; La Torre et al., 2018; Kidima, 2019; Silva et al., 2020), this may be due to the techniques that were used to rescue the parasites from feces, also due to the different environmental, geographical and sanitary conditions, among others.
The results obtained in the present work coincide with those reported by Idika et al. (2017) in Nigeria, where no significant difference was found between frequency and sex of dogs (p > 0.05), but by age group, which coincides in this work for stray dogs (p=0.002), where the highest percentages of parasites were obtained in dogs younger than 6 months of age. In Mexico there are similar reports, where Encalada-Mena et al. (2011) in Campeche, Rodríguez-Vivas et al. (2011) in Yucatán and Olave-Leyva et al. (2019) in Hidalgo report that the age factor had significant difference with respect to the prevalence of parasites; these studies report the highest prevalences of parasites in the younger age categories. This could be because younger dogs are more susceptible to parasitic infections from before birth.
In four of the five neighborhoods sampled, parasites were found that may present a zoonotic risk for the people living in them. These colonies have semi-urban areas where dogs find food, water and territory, i.e., favorable conditions for their survival. These places are generally used as garbage dumps and sanitary conditions are inefficient; therefore, dogs and humans are exposed to high levels of contamination with intestinal parasites.
The low prevalences reported in the present study for both household and stray dogs may be due to the environmental conditions of Gómez Palacio city, Durango, since it is a desert area that records maximum temperatures from April to September with a range of 41- 44°C (Servicio Meteorológico Nacional, 2020). This factor could prevent the development of parasites in certain seasons of the year, although there are many factors that can influence; for example, the sensitivity and specificity of the flotation techniques used to concentrate parasite eggs, the methodology used, the sample size, the amount of larval eggs ingested by the dogs, the biological cycles of the parasites and, although the eggs can survive in the environment, if favorable environmental conditions are not present, infective larvae do not develop and therefore, the prevalences decrease.
CONCLUSIONS
The parasites found in feces of household and stray dogs were: Ancylostoma spp, Taenia spp, Toxocara spp, Trichuris vulpis and Cystoisospora canis; the first four of which are zoonotic in nature, posing a risk to public health in Gómez Palacio municipality, Durango. A significant difference was found between prevalences of intestinal parasites for household and stray dogs. Stray dogs had a higher prevalence than household ones. In stray dogs, a significant difference was found in relation to age class; all puppies were parasitized. No significant difference was found between parasitism and sex of stray and house dogs.
It is suggested to continue with more extensive studies on the prevalence of parasites in feces of household animals in urban areas, both in those animals with owners and those in street conditions.
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Received: June 01, 2021; Accepted: October 03, 2021