Parasitic profile of traction equids in the semi-arid climate of Paraíba State , Northeastern , Brazil

The objective of this study was to determine the parasitological profiles of traction equids from the semi-arid climate of Paraíba (PB) State. We analyzed 96 equids that performed traction work, with no defined breed, males and females, and all older than 24 months. Among the analyzed animals, 51% were donkeys, 41.7% mules, and 7.3% horses. Fecal material and blood were collected for parasitological examination and to determine the packed cell volume (PCV), respectively. The samples were sent to the Veterinary Parasitology Laboratory, Veterinary Hospital IFPB, Sousa-PB campus, and epidemiological questionnaires were provided to the owners. It was observed that 83.3% of equids tested positive for gastrointestinal parasites. Strongylidae was the most prevalent parasite (83.3%), followed by Giardia sp. (5.3%), and Eimeria sp. (2.1%). The mean eggs per gram (EPG) value of the fecal samples was 1143. Fecal analysis revealed that 78.9% of the larvae were from “small strongyles”. The presence of ectoparasites was not observed in the studied animals. The answers to our questionnaire revealed that 69.8% of the animals had never been dewormed and that the remaining 31.2% had only been dewormed once. We concluded that the prevalence of gastrointestinal parasites among traction equids in the municipality of Sousa-PB is high.

The most prevalent ectoparasites in equids include the ticks Amblyomma cajennense, Anocentor nitens, and Rhipicephalus (Boophilus) microplus.Tick infestation causes economic loss due to decreasing animal productivity and the expense associated with the use of tick preventives (PRATA et al., 1996).
There are no reports that describe the main parasites of traction horses, donkeys, and mules in the municipality of Sousa-PB.Therefore, the objective of this study was to identify the main parasites in working equids in the municipality of Sousa, arid midland of Paraíba.
This study was performed in the municipality of Sousa, Paraíba.The laboratory analyses were performed at the Veterinary Parasitology Laboratory (LPV), Veterinary Hospital, Federal Institute of Education Science and Technology of Paraíba (IFPB), Sousa-PB campus.
The number of animals required for analysis was calculated using an expected prevalence of 50% for gastrointestinal helminths, gastrointestinal protozoa, and ectoparasites since there are no previous reports detailing the prevalence of these parasites in equids in the semi-arid region of Paraíba.A minimum confidence level of 95% was also considered assuming a statistical error of 10% (THRUSFIELD, 1995).
For the identification of helminths and protozoa in the equids, fecal samples were collected as advised by Gordon & Whitlock (1939).Fecal analysis was performed in accordance with the study by Roberts & O'Sullivan (1950), and the eggs per gram of feces (EPG) were calculated for each parasitic helminth.Centrifugation in Sucrose Solution (CFSS), the method developed by Tobie et al. (1938), was used to isolate protozoal cysts and oocysts as well as low-density eggs.For the quantification and identification of the larvae isolated in the fecal examinations, the method of Bevilaqua et al. (1993) was followed.To identify ectoparasites, inspection of the entire body of the animal was performed.For the determination of the PCV using the microhematocrit method (FERREIRA et al., 1978), blood samples were collected by jugular venipuncture into a tube containing EDTA anticoagulant (10%) and then sent to LPV.
An epidemiological questionnaire was provided to the owners of the traction equids, in which the cleanliness and nutrition of the animals were addressed.The following information was requested: owner's and animal's signalment, management of the animal (nutrition and sanitation), and health history of the animal.
The data were analyzed using the chi-square test, followed by the Fisher's exact test at a 5% level of significance (SERRA-FREIRE, 2002).
It was observed that 83.3% (80/96) of the traction equids had positive fecal parasitological examinations.Piccoli et al. (2015) also detected a high prevalence of parasitic infection (82%) among traction horses in Porto Alegre, Rio Grande do Sul. Ferraro et al. (2008) likewise identified a parasitological prevalence of 88% among traction horses in Curitiba, Paraná.
There was no statistically significant difference (p ≥ 0.05) in the prevalence of gastrointestinal parasites among the species evaluated (Table 1).
In the present work 5.3%(5/96) of the animals were positive for Giardia sp. and 2.1% (2/96) were positive for Eimeria sp.A similar prevalence for the genus Giardia (4%, 6/150) was found by Nasciutti et al. (2013) in a slaughterhouse in the city of Araguari, Minas Gerais.
An association was observed between Strongylidae and the protozoa Giardia sp. in 8.2% (4/49) of the donkeys.Among the mules, 5% (2/40) were positive for the protozoa Eimeria sp. in combination with Strongylidae.Among the horses, 14.3% (1/7) had an association between Strongylidae and Giardia sp.In a study performed by Souza et al. (2009) on horses in Rio de Janeiro-RJ, an association was detected between Giardia sp. and Eimeria sp.This differed from the present study, in which no animal showed infection with more than one genus of protozoa.
It was observed that 85.7% of the male equids and 80% of the females were infected with gastrointestinal parasites.However, only among the horses was the difference between the sexes statistically significant (p ≤ 0.05) (Table 2).However, low sampling of male horses may have interfered with the results and promoted this difference.
The mean (±SD) EPG of the traction equids was 1143(±1853).The donkeys possessed a statistically lower mean EPG (p ≤ 0.05) as compared to the other species at 807 (± 770), whereas the mule EPG average was 1571 (± 2682) and the horses was 1050 (± 800).On classifying by category, 35% (34/96) of the animals were classified as having low-level infection (<500), 28% (27/96) as medium (500-1000), and 37% (35/96) as high (>1000).The donkeys possessed the highest percentage of positive fecal examinations but the lowest level of parasitic disease, confirming the resistance of the species.Chitra et al. (2011) stated that, although donkeys are also known in India for their robustness, they are the species most vulnerable to parasitic infection.
Only among the horses did the prevalence of infection differ significantly (p ≤ 0.05) between the females and the males.In general for the traction equids, there was no statistically significant difference (p ≥ 0.05) in EPG between the sexes (Table 3).Similar results  2008) when evaluating traction animals from Curitiba-Paraná, where the mean EPG for males was 1,492 and that for females was 1,322.Mules aged ≥ 12 years had significantly higher EPG (p ≤ 0.05) as compared to mules in other age groups and to other species of the same age group (Table 4).It was also observed that animals ≥ 12 years of age were more vulnerable (p ≤ 0.05) to high levels of parasitism.This finding was also made by Ferraro et al. (2008) who observed an average EPG of 1438 (high level) in adult and geriatric animals.It has been shown that as they increase in age, equids develop a resistance where they may develop severe infections while remaining asymptomatic (BOWMAN, 2014).Thus, equids of advanced age become sources of infection for younger animals.
No statistically significant difference was observed (p ≥ 0.05) when the EPG levels were evaluated in association with the PCV (Figure 1).When evaluating gastrointestinal parasitism and hematology in horses and donkeys in São Luís, Maranhão, Ferreira et al. (2014) observed that the degree of parasitism was not responsible for the hematological alterations.
In the fecal examinations, it was found that 78.9% of the larvae were small strongyles or cyathostomes, followed by 7.1% Strongylus equinus, 3% Strongylus edentatus, 6% Strongylus vulgaris, and 5% Trichostrongylus axei (Figure 2).It was observed that among the horses, S. vulgaris was present with the highest prevalence (12.8%).Similar results were obtained by Ferraro et al. (2008), with an average prevalence of 88% for the cyathostomes and 12% for S. vulgaris.Although a thorough visual inspection was performed on all animals, the presence of ectoparasites was not observed.Perhaps the rusticity of these animals, coupled with the absence of a defined breed and the high temperatures present throughout the year, does not favor ectoparasite infestation.Rego et al. (2009) also did not identify ectoparasites in 166 equines used for work and sport in Curitiba, Paraná.According to Chagas et al. (2001), high temperatures do not provide an ideal environment for the breeding and survival of engorged female ticks, and at 20 °C the females are not very mobile.In Sousa-PB, the average annual temperature is 27 °C, and the average daytime temperature exceeds 35 °C.By contrast, in Curitiba-PR, the average annual temperature does not exceed 17.5 °C (IBGE, 2010).
In the epidemiological questionnaire, 63.5% (61/96) of the owners replied that they possessed other equids in addition to the evaluated animal, and 60.4% (58/96) of the equids were maintained in direct contact with other species of animals.These included canines, felines, poultry, cattle, sheep, goats, and pigs.
Regarding the use of dewormers, 69.8% (67/96) of the equids had never been dewormed and the remaining 31.2% (29/96) had only been dewormed once.Of the dewormers used, the only compound cited was ivermectin.The most commonly used formulation was paste (51.7%, 15/29), followed by injectable (48.3%, 14/29).The limited use of dewormers may explain the high parasite burden found in this study, where it was observed that 65% (62/96) of the animals possessed EPG > 500 (medium to high).
None of the equids evaluated had been vaccinated.Furthermore, the term "vaccinated" was frequently confused with "dewormed", which denotes a low level of knowledge regarding animal health management possessed by the owners.
With regard to nutrition, 59.5% (57/96) of the equids in this study were fed a combination of grass and corn, 37.5% (36/96) were pasture-fed only, and 3% (3/96) were provided a mixture of pasture and a commercial ration.It is well known that little attention is paid to the quality of the food provided to traction equids.This may be one of the factors contributing to the high prevalence of parasitism observed in the present study.It has been proven that a well-balanced diet can improve the immune response of the host, and therefore limit the development of parasitic infections.
Inadequate nutrition and sanitation was observed in a study by Herd (1990).According to the investigators in that study, forced labor, malnutrition, and stress were associated with parasitism, and severely impaired the health of the equids, even leading to death.However, despite being used all day for work under adverse environmental conditions, the traction equids in this study were resistant to parasitic disease.No affliction was reported that required removal of any of the equids from work.
We concluded that the prevalence of gastrointestinal parasites in traction equids in the municipality of Sousa-PB is high.However, no animal presented parasitic disease.Ectoparasites were not founded on the animals in this study.Increased awareness is required for owners to improve the cleanliness of these animals.

Figure 1 .
Figure 1.Packed cell volume (PCV) in relationship to the eggs per gram (EPG) levels among traction equids in Sousa, Paraíba, Brazil.

Table 1 .
Number of infected animals and prevalence (%) of helminths and protozoa among traction equids in Sousa, Paraíba, Brazil.
were found by Ferraro et al. (

Table 4 .
Relationship between mean EPG (± SD) and the equid age range.

Table 2 .
Prevalence of helminths and protozoa among traction equids, according to sex, in Sousa, Paraíba, Brazil.

Table 3 .
Mean and standard deviation of eggs per gram (EPG) in male and female traction equids in Sousa, Paraíba, Brazil.