The total prevalence of enteric parasites in the fecal sample showed 115 positive cases, where helminths were 81 (62.7%) and protozoa were 34 (26.3%) out of 129 examined dogs (Fig 2). Infection rates were high in the fecal samples collected from dogs in area 2, the percentages of helminths and protozoa were (27.1%), (10.07%) respectively followed by area (3) (20.1%), (9.3%) and finally area (1) (15.5%), (6.9%) in Taif region, the difference was statistically significant (p=<0.0001). The prevalence of mixed infection of enteric helminthic and protozoa in fecal samples of stray dogs in three areas was higher than single infection (Table 1, 2 and 3).
Regarding infection with helminths eggs recovered from fecal sample examination from single or mixed form,
Echinococcus granulosus,
Toxocara canis,
Trichuris vulpis were of high infection rate (15.5%), (10.07%), (10.07%) followed by
Ascaris lumbercoides (7.7%), then
Toxocara leonine (6.9%), while both
Ancylostoma caninum and
Ancylostoma braziliense are of the same percentage (6.2%). Concerning single and mixed protozoa infection,
Giardia was of a high prevalence (16.2%) followed by
Cryptosporidium (8.5%) and finally
Entamoeba histolytica (1.5%) in fecal samples of stray dogs (Fig 3).
The total prevalence of helminths eggs by three different mount preparations showed
Toxocara canis and
Toxocara leonine eggs were (10.07%), (6.9%) respectively confirmed by the trichrome stain. At the same time, the percentage with the saline-based wet mount was (6.9%), (5.4%) and (8.5%), (6.2%) by the iodine-based wet mount. The prevalence of
Trichuris vulpis was (10.07%) confirmed by trichrome wet mount, while the percentage (6.9%) by saline wet method and wet iodine mount preparation.
Echinoccous granulose prevalence was (15.5%) detected by trichrome wet mount and (11.6%) by saline wet method and (13.1%) by iodine wet mount. The prevalence of
Ancylostom caninum and
Ancylostoma braziliense was (6.2%) detected by saline wet mount preparation, and trichrome wet mount prevalence with iodine wet mount was (4.6%) and (3.8%), respectively. A prevalence of (7.7%) for
Ascaris lumbricoides was detected by trichrome mount wet, while prevalence with both saline wet and iodine wet mounts was (5.4%) (Table 4).
Protozoa recovered from the fecal samples and the total prevalence of
Cryptosporidium species was (8.5%) detected by Kinyoun’s acid-fast stain, while the prevalence with saline wet mount and iodine were (7.7%), (6.9%) respectively. The prevalence of
Giardia was (16.2%) confirmed with iodine wet mount method while, with saline wet mount and Kinyoun’s acid-fast were (12.4%), (13.9%).
Entamoeba histolytica incidence was (1.5%) confirmed with iodine wet mount method and Kinyoun’s acid-fast while, with saline wet mount was (0.8%) (Fig 4).
As per our knowledge, this is the first study addressing mixed infections between dogs and humans in Saudi Arabia. Public health authorities and research bodies all over the world are especially and highly interested in the intestinal parasites found in dogs. This huge attention was taken because dogs are reservoirs for these zoonotic parasites, carry and transmit them
(Gracenea et al., 2009). Our study showed a total prevalence (115 out of 129 cases) for enteric parasites in the fecal samples, where it was for helminths 81 (62.7%) and for protozoa 34 (26.3%). This result was recorded for the first time in Taif, KSA. As stray dogs have free access to potentially infectious; synchronized with the lack of anti-parasitic treatments, dogs are heavily parasitized animals. Humans in Taif are at high risk for being subjected to different gastrointestinal parasites of zoonotic potential, which can be spread easily via stray dogs, a fact that is relevant to what is aforementioned. Similar results were reordered in other countries in the world, such as in the Philippines and Canada
(Villeneuve et al., 2015; Urgel et al., 2019).
Infection rates in fecal samples collected from three different areas in Taif showed higher rates of infection with helminths and protozoa in the area (2) (27.1%), (10.07%) followed by area (3) (20.1%), (9.3%) and finally area (1) (15.5%), (6.9%), respectively. The difference was statistically significant (p=<0.001). A possible explanation for these findings is that areas (2 and 3) are characterized by dogs living in close contact with livestock besides the presence of animal slaughterhouses. These animal species are intermediary hosts essentially required for many parasites to complete their life cycle
(Weese et al., 2011). Prevalence of intestinal parasites (helminths and protozoa) in the fecal samples of dogs in three areas showed a higher rate of mixed infection rather than of mono-infection. This is attributed to the fact that the presence of one parasite species may lessen the immunity of the dogs with higher parasite intensity, which in turn enhances the presence of the other parasitic species, causing these mixed infection cases
(Fontanarrosa et al., 2006). The present study showed types of helminth and protozoan species like those reported in earlier surveys of dogs (
De Alwis, 2000).
It was found, after observing various helminths eggs by different mounting techniques, that
E. granulosus,
T. canis, and
T. vulpis were the helminths in single and mixed infection and resembled high rates of infection (15.5%), (10.07%) and (10.07%), respectively followed by
A. lumbercoides (7.7%), then
T. leonine (6.9%), while both
A. caninum and
A. braziliense are of the same percentage (6.2%). These results were confirmed with the trichrome wet mount method. The trichrome stain has been considered as a helpful stain in the detection of helminths ova
(Wood et al., 1982; Hale et al., 1996). They described the appearance of the most common helminth ova that was easily detected using the trichrome stain than other mount preparation.
In the present work, we found
E. granulosus prevalence was high in the areas 2 and 3 (40%) in either single infection or mixed infection with
T. canis and
T. leonine. This finding is particularly important because there are many large feedlots for cattle, sheep, goats and camels in areas 2 and 3. These animals are of high infection risk by contamination of food or water supplies with eggs carried by dogs, which could result in the spread of this zoonotic infection to local stray dogs. Consequently, human and animal infection with an intermediate stage (hydatid cyst) may arise in KSA
(Deplazes et al., 2011; Shalaby et al., 2011).
T. canis prevalence in the current study was (10.07%). It has been documented that
T. canis ova were very resistant to extreme weather conditions and chemical agents (
Torres-Chablé et al., 2015;
Regidor-Cerrillo et al., 2020). Also, it is well known that routes of infection of
T. canis include oral, transmammary, and transplacental and that it can be transmitted by paratenic hosts, which let the parasite everlasting in our ecosystem
(Corrales et al., 1999). T. leonine percentage was (6.9%), the latter one of the more frequent parasites detected in shelter dogs in several countries
(Villeneuve et al., 2015). The region is a shared habitat with dogs; this interaction may explain the presence of
T. leonina in stray dogs
(Beiromvand et al., 2013).
The prevalence of
T. vulpis was (10.07%). The zoonotic potential of
T. vulpis was supported by
Dunn et al., (2002), who recorded human infection with this worm due to close contact with dogs.
Trichuris spp. is considered to be soil-transmitted helminths
(Liberato et al., 2018). The prevalence of
A. caninum and
A. braziliense was (6.2%) in this study. Transmission of this parasite can occur through penetration of skin at hair follicles or sweat glands or through direct ingestion of
A. caninum (
Wojnarowicz and Smith, 2007;
Scaramozzino et al., 2018). However, recorded mixed infection with
A. braziliense and
T. vulpis similar result by
Villeneuve et al., (2015) has reported a strong positive association between
Ancylostoma sp. and
T. vulpis in North America. The
A. lumbricoides has a prevalence of (7.7%), where the present study suggested that dogs could act as reservoir hosts of
A. lumbricoides and environmental contaminators that increase the risk of infection in humans
(Zaman et al., 2018).
Concerning single and mixed protozoa infection,
Giardia was of high prevalence (16.2%), followed by
Cryptosporidium (8.5%) and finally
E. histolytica (1.5%) in fecal samples of dogs. Protozoa appeared to have less shrinkage and a more distinct internal structure with the saline concentration than other mount preparations
(Zaman et al., 2018). The present work recorded that the prevalence of
Giardia was (16.2%), which was confirmed by the iodine wet mount method, where internal structures of trophozoites, cysts were stained well by iodine, the method that made their recognition and identification easier in the specimens.
Cryptosporidium species was (8.5%) detected by Kinyoun’s acid-fast stain
(Elsafi et al., 2014). Those protozoa represent zoonotic risk factors for man, the zoonotic potentiality supported by (
Robertson and Thompson, 2002;
Stafford et al., 2020). Finally, the higher prevalence of
Giardia sp. and
Cryptosporidium sp. in stray dogs may be due to dogs drinking water from small rivers and lakes that are frequently more contaminated with parasites
(Frizzo et al., 2016).
