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Research Article
 

Role of Pet Dogs in Transmitting Zoonotic Intestinal Parasites in Egypt



M.A. Ibrahim, K.A. Gihan, S.M. Aboelhadid and M.M. Abdel-Rahim
 
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ABSTRACT

Objective: The objective of this study was to determine the prevalence of zoonotic intestinal parasites in pet dogs and their owners in Cairo and Giza Governorates, Egypt. Methodology: A total of 395 fecal samples collected from pet dogs beside 145 stool samples from humans were subjected to macroscopic and microscopic examination using different flotation and sedimentation techniques. Results: The overall prevalence of enteric parasites in the examined dogs was 25.6%. Higher prevalence was shown in police dogs (43.3%) followed by pet shop dogs (30.8%) and finally in household dogs (13.8%). Cryptosporidium was the most frequent parasite detected in the examined dogs (10.1%) and humans (10.3%), whereas Giardia was the lowest one (0.5 and 2.8% respectively). In addition, Entamoeba histolytica/Entamoeba dispar were found at a rate of 5.6% (dogs) and 7.6% (humans). Trichuris vulpis, Toxascaris leonina and Toxocara canis were identified only from the examined dogs at a rate of 3.3, 5.8 and 0.3% respectively. Young age (<6 months), female sex, local breed, undercooked feeding, outdoor housing and irregular de-worming were significantly associated with increased prevalence of the identified parasites in dogs. Regarding humans, the highest prevalence of enteric parasites was found in the age group between 5-10 years old (60%). Gender did not affect the risk of an infection in the study population. Conclusion: In conclusion, parasitological results in this study clearly highlight the significant role of pet dogs as a host for several species of enteric parasites; therefore preventive measures should be taken to avoid the environmental contamination and infection of both man and animals.

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  How to cite this article:

M.A. Ibrahim, K.A. Gihan, S.M. Aboelhadid and M.M. Abdel-Rahim, 2016. Role of Pet Dogs in Transmitting Zoonotic Intestinal Parasites in Egypt. Asian Journal of Animal and Veterinary Advances, 11: 341-349.

DOI: 10.3923/ajava.2016.341.349

URL: https://scialert.net/abstract/?doi=ajava.2016.341.349

INTRODUCTION

Pet animals, particularly dogs are important companions in many households worldwide; participating to the physical, social and emotional development and the well-being of their owners1. However, in spite of the worthy benefits to the society, companion dogs remain a major threat to public health, with dogs harboring several pathogens that can be spread to humans2. As communities become more urban, the presence of pets within houses has increased in popularity3. Since pet dogs share the same environment with humans and due to their close association with their owners, they play a significant role in the zoonotic transmission routes of the pathogens. Of the zoonotic pathogens acquired from dogs, gastrointestinal parasites are of particular concern as they can cause considerable burdens in humans4. As regards zoonotic parasites, Toxocara canis, Ancylostoma caninum, Echinococcus granulosus, Dipylidium caninum, Entameba histolytica, Giardia spp. and Cryptosporidium spp., represent the most popular enteric parasites reported in humans5-7. Zoonotic transmission of these parasites occurs either directly by direct contact with infected animal or indirectly by contact with animal feces and contaminated food and water8. With the increasing number of pet dogs in the last decades there is more contact between dogs and people, together with a low level of hygienic conditions and lack of sufficient veterinary attention and zoonotic disease awareness compound the risk of transmission of zoonotic gastrointestinal parasites to humans5. Nevertheless, only few data are available on the occurrence of intestinal parasites in companion dogs in Egypt. Current information on regional prevalence rates is essential for the development and modification of control measures in animal and public health. The main objective of this study was to determine the prevalence of zoonotic enteric parasites in pet dogs and their human contacts in Cairo and Giza Governorates, Egypt.

MATERIALS AND METHODS

Sampling: A total of 395 fecal samples from pet dogs beside 145 stool samples from humans were collected from Cairo and Giza Governorates, Egypt during the period from July, 2014 to October, 2015.

Dog samples: Fecal samples were collected from household dogs (n = 210) that underwent clinical examination in different veterinary clinics, pet shop dogs (n = 65), beside 120 police dogs obtained from Department of Training Security and Guard Dogs, Police Academy, Cairo. From each dog a fecal sample was collected immediately after defecation and put in a plastic bag then transported to Laboratory of Parasitology Department, Faculty of Veterinary Medicine, Beni-Suef University for parasitological examination. Formalin (10%) was used as preservative for the samples. A questionnaire was used to record the general characteristics of the dogs, including age, gender, breed, type of food eaten, housing condition, presence or absence of diarrhea and history of anthelmintic usage.

Human samples: Stool samples were obtained from both dog owners (n = 100) and pet shop workers (n = 45). Of the sampled individuals, 113 were males and 32 were females. Data concerning age, gender, residence and gastrointestinal complains were recorded using a questionnaire for each person. Each sample was labeled and sent to the laboratory for further parasitological examination.

Laboratory procedures
Macroscopic examination: Feces were stored at 4°C and examined within 48 h. All fecal samples were examined by naked eye for demonstration of adult nematodes and proglottides of tapeworms.

Microscopic examination: Each sample was subjected for examination by centrifugal fecal floatation technique using different solutions (saturated salt solution, zinc sulphate and Sheather’s solution) according to Zajac and Conboy9. Furthermore, formol ether sedimentation technique10 was applied for each sample. Lugol’s iodine solution was used to facilitate identification of protozoal cysts and trophozoites. Also, Modified Ziehl-Neelsen (MZN) stain was used to detect Cryptosporidium spp., oocyst in the examined samples11. Parasite eggs, oocysts and cysts were identified under light microscope based on color, shape and contents according to the key given by Soulsby12.

RESULTS

Prevalence of enteric parasites in the examined dogs: The overall prevalence of enteric parasites in the examined pet dogs was 25.6%, with the police dogs showed the highest prevalence (43.3%) followed by pet shop dogs (30.8%) and finally household dogs (13.8%) (Table 1). The recovered helminths eggs were found belonging to Trichuris vulpis (3.3%), Toxascaris leonina (5.8%) and Toxocara canis (0.3%), whereas the detected protozoa were Cryptosporidium spp. (10.1%), Giardia spp. (0.5%) and Entamoeba histolytica/Entamoeba dispar (5.6%).

Table 1: Prevalence of enteric parasites in the examined dogs

Table 2:Risk factors associated with enteric parasites prevalence in the examined dogs (n = 395)

Risk factors associated with enteric parasites prevalence in the examined dogs: Analysis of the risk factors associated with increased prevalence of enteric parasites in the examined dogs revealed that puppies under 6 months of age showed the highest enteric parasite prevalence (64.3%) compared with the other age groups. Concerning the gender, it was found that females has a higher infection rate (29%) compared with males (22.3%). Local breeds exhibited a higher prevalence (36.7%) than exotic ones (24.7%). Also the parasite prevalence was higher in diarrheic dogs (57.1%) than non-diarrheic ones (22.5%). In addition, undercooked feeding, outdoor housing and irregular de-worming were found to be attributed to high prevalence of endoparasites in the examined dogs (Table 2).

Prevalence and risk factors associated with zoonotic enteric parasites in the examined humans: Out of 145 humans, 30 (20.7%) were found positive for enteric parasites (Table 3). The isolated parasites were found belonging to species of Cryptosporidium (10.1%), Giardia (2.8%) and Entamoeba hystolytica/Entamoeba dispar (7.6%). Children in the age group between 5-10 years old showed the highest prevalence of endoparasites. The parasite prevalence in pet shop workers was higher than in households, 27.3 and 16.7% respectively. The study also indicated that males were nearly equal females in the prevalence of enteric parasites (20.4 vs. 21.9%). Finally, individuals with gastrointestinal complains exhibited higher prevalence than those without gastrointestinal complains; 13.3 and 7.6% respectively.

DISCUSSION

The coproscopical examination revealed that the overall prevalence of enteric parasites in the examined pet dogs was 25.6%, a result which is supported by the finding of Ahmed et al.13 who reported that 18.3% of the examined house and police dogs in Alexandria, Egypt were harbored enteric parasites. Similar result (26.9%) was obtained by Gracenea et al.14 in the examined dogs in Spain. Contrary to this finding Fok et al.15 reported that the total infection rate in owned dogs in northern and eastern region of Hungary was 57.8%. Also, Villeneuve et al.16 found that the gastrointestinal parasites infection rate in the examined dogs was 33.9%. Worldwide, it has been found that the prevalence of intestinal parasites in dog range from 16.5% (Canada) to 90% (Sri Lanka)6,17. It can vary widely, based in part on geographical location, host individual features, management, sampling protocols, demographic factors, anthelmintic usage and diagnostic techniques18. Further, canine helminths are susceptible to the effects of environmental condition and to climate change due to their developmental stages and their survival periods in the environment19,20.

Trichuris vulpis represented 2.5% of recovered parasites which is nearly similar to that (2%) reported by Sarvi et al.21. However, a higher prevalence (18.8%) was reported by Alvarado-Esquive et al.22 in shelter dogs in Veracruz, Mexico. The zoonotic potential of T. vulpis was supported by Dunn et al.23 who recorded a case of human infection with this worm in a woman with duodenal ulcer disease, chronic diarrhea and close contact with dogs.

Table 3: Prevalence and risk factors associated with zoonotic enteric parasites in the examined humans (n = 145)

Also, Marquez-Navarro et al.24 reported a case of child infection with rhinitis due to T. vulpis. However, clear data still need to be provided to definitively add Trichuris vulpis to the causes of human intestinal infections25.

Toxascaris leonina was detected at a rate of 5.8% which is higher than that (3%) reported by Villeneuve et al.16. Contrary to this finding, a higher percentage (13%) was recorded by Kim and Huh26. Also, Beiromvand et al.27 found Toxascaris leonina to be the most frequent ascarid identified in dog feces while Mateus et al.28 found it to be the least frequent. It seems that Toxascaris leonina does not display zoonotic potential. However, a case of osteomyositis with cutaneous abscesses containing worms identified as Toxascaris leonina has been described in the 1960's in the former USSR29 and also another case of ocular infection by a suspected Toxascaris spp., larva has been described from Africa30.

Even though high prevalence of T. canis in dogs in several countries allover the world, this nematode parasite was detected in only one sample (0.3%) that obtained from a pet shop dog. However, Ahmed et al.13 detected T. canis in both police and house dogs at a rate 0.8 and 5% respectively, whereas Sarvi et al.21 detected T. canis in domestic dogs in Iran at a rate of 27%. Infection of human by Toxocara spp., has worldwide distribution and appears in variable frequencies, depending on local factors such as close contact with soil contaminated by dog31 or dog hair32. The zoonotic ability of Toxocara spp., has been established and it is well known that pet ascarids cause human infections globally as demonstrated by several surveys carried out in all corners of the World10,33.

As regards Cryptosporidium spp., they were detected at a rate of 10.1% in the examined dogs. Nearly similar result (7.8%) was recorded by Ngui et al.34 in rural dogs in Malaysia, whereas lower percentages (3%) and (3.3%) have been reported by Villeneuve et al.16 and Giangaspero et al.35 in Canada and Italy respectively. Regarding humans, Cryptosporidium oocysts were detected a rate of 10.3%; with children of 5-10 years old were more affected (40%). This is in agreement with many studies carried out in individuals of various ages in several areas of Egypt that denote the prevalence of cryptosporidiosis in humans varied36 between 0 and 47%. Also, Mukhopadhyay et al.37 reported a high prevalence of cryptosporidiosis in young children, especially those aged less than 2 years. The zoonotic potential of Cryptosporidium has been proved by Sargent et al.38 who denoted that dogs act as a potential source of zoonotic cryptosporidiosis. Several reports indicated that Cryptosporidium canis is present in human patients in the United Kingdom, Kenya, Peru, Thailand and the United States39,40. Although, a recent study suggested that cryptosporidiosis from pet dogs poses only a minimal zoonotic risk, the possible public-health implications of C. canis cannot be ignored41. Even though a small number of humans are infected with C. canis, recent findings of concurrent C. hominis infection in C. canis infected persons suggest that many of the C. canis infections in humans may be due to anthroponotic rather than zoonotic transmission42.

The results of the present study showed that Giardia was less frequent (0.5%) than Cryptosporidium in the examined dogs. Contrary to this result43 found that Giardia was the most frequent among intestinal protozoa whereas Cryptosporidium was less common in the canine fecal samples. Also in a study conducted in Australia, Giardia was found to be the most prevalent parasite in healthy pet dogs (9.4%) whereas Cryptosporidium was detected at much lower rate44 (0.6%). In Portugal, Neves et al.45 reported the prevalence of Giardia spp., in 7.4% of apparently healthy dogs and in 15.5% of those suffered from gastrointestinal disease. Besides, Alvarado-Esquive et al.22 identified Giardia spp., in dogs at much higher levels (45.5%). Recent surveys of gastrointestinal parasites of dogs have demonstrated high levels (prevalence of 7.2-22.1%) of Giardia in stray as well as domestic dogs in both developing and developed countries17,46. Concerning humans, Giardia spp., were detected at a rate of 2.8% (Table 3). In developing countries, Giardia prevalence in humans fell47-52 into the range of 8-30%. On the other hand, lower prevalence rates were reported in Germany53 (1.5%), Italy54 (0.4-6.2%), United Kingdom55 (1.3%) and United States56 (1.4%). Several studies denoted that dogs can harbor zoonotic assemblage (Assemblage A) of Giardia57,58. Also, the presence of genetically similar isolates in humans and dogs from different geographical locations worldwide has provided circumstantial evidence in support of Giardia (G. duodenalis) being zoonotic59,60. However, the facility of genotyping Giardia is not readily available to veterinarians in practice; consequently all positives should be assumed zoonotic. Therefore, treatment is necessary regardless of whether the animals asymptomatic, given the zoonotic potential of this parasite and because they are a source of infection for other animals61.

Entamoeba histolytica/Entamoeba dispar were detected in the examined dogs at a rate of 5.6% while in humans the prevalence was 7.6%. Because it is impossible to differentiate pathogenic E. histolytica from non-pathogenic Entamoeba dispar, using light microscopy62, all cysts morphologically consistent with E. histolytica were referred to as E. histolytica/Entamoeba dispar to reflect this uncertainty. In a study carried out in Alexandria Governorate, Egypt, E. histolytica/Entamoeba dispar was recovered in a rate of 18.3% from the examined dogs13. Also, Alam et al.63 in Lahore, Pakistan, isolated E. histolytica like cyst from housed and clinically diseased dogs in a percentage of 15.6 and 95%, respectively. They added that dogs play an important role in the epidemiology of Entamoeba infection in endemic areas. Human amoebiasis was reported at a higher rate (14.4%) in Beni-Suef Governorate, Egypt from diarrheic and/or dysenteric patients64. Also, in a study by Aza et al.65 in Malaysia, amoebiasis was reported in humans at prevalence of 21.0%. On the other hand, Al-Harthi and Jamjoom66 reported 2.6% prevalence of E. histolytica infection in Makah, Saudi Arabia. Accuratestrain-specific diagnosis of E. histolytica would help in the generation of accurate epidemiological data for a better estimate of the burden of amoebiasis on the health of the world67. The just presence of Entamoeba cysts in feces of humans is of low significance, as the Pan American Health Organization does not recommend treatment to asymptomatic individuals presenting cysts of Entamoeba histolytica/Entamoeba dispar in stools without the specific identification of E. histolytica68. It is worth mentioning that close contact with pet dogs was associated with an increased risk of contracting Entamoeba, this might be due to that cysts of Entamoeba are deposited on the surface (fur) of the animals during close contact with humans and then later transmitted to a next person69. Finally, the presence of enteric parasites in the studied population demonstrates that the poor hygienic conditions, important risk factor of fecal-oral transmission, were not improved in the community.

Generally the lower prevalence of enteric parasites (especially helminths) in household dogs (13.8%) as compared to both police (43.3%) and pet shop (30.8%) dogs reported in this study might be attributed to the regular deworming of pet dogs using (pyrantal, febental and praziquental) and to the general hygienic measures applicable to the household dogs. Also, it might reflect the highest risk of parasitic infections and consequently environmental contamination and transmission of enteric parasites through the fecal-oral route more frequently in outdoor dogs70.

It is worth mentioning that all the estimated parasites either helminths or protozoa have a direct life cycle. The animals investigated were housed under captivity so the chances for harboring cestodes or trematodes, which require an intermediate host were limited. In spite of hygienic measures, regular deworming and high quality of feeding, a range of different parasites were reported in this work. The relative high prevalence of intestinal parasites recorded reflects that even with relatively high level of care, companion dogs may act as a potential source for environmental contamination with such parasites and the potentiality of other animals as well as humans to be infected.

Analysis of risk factors associated with parasitic infection revealed that puppies under 6 months of age showed the highest enteric parasite prevalence (64.3%) compared with the other age groups. Abere et al.71 reported that the overall prevalence of parasites was significantly higher in young dogs (<1 year) than adults. This was partially due to parasite specific immunity usually acquired with age or probably as a consequence of single or repeated exposures72. However, it is nowadays established that patent intestinal infections occur in dogs of all ages73.

Concerning the gender, it was found that females has a higher infection rate (29%) compared with males (22.3%) which in accordance with Davoust et al.74 in Nigeria who concluded that female dogs were more liable to contract intestinal nematodes than males. In contrast Getahun and Addis75 reported that the prevalence rate of enteric parasites was higher in male than female dogs (79.2 vs. 76.8%). However, Alvarado-Esquive22 found that the overall prevalence of parasitic infections in dogs did not vary with sex.

Local breeds of dogs were found to harbor more enteric parasites (36.7%) than exotic breeds (24.7%). In accordance with this finding, Getahun and Addis75 reported that the exotic breeds were more likely to contract infection. On the other hand Swai et al.76 in Tanzania and Shukllari et al.77 in Albania documented that breed was not a risk factor for parasitic infection in dogs and all breeds have equal opportunity to contract the infection if exposed to the same source. The association of enteric parasite infection with local breeds is probably due to differences in healthcare received, in comparison with pure breeds, where pure breed dogs generally receive better care, including deworming and access to clean food and water78.

Dogs kept outdoor (police and pet shop dogs) exhibited a higher prevalence of enteric parasites (38.9%) compared with those kept as households (13.8%). This is in accordance with Katagiri and Oliveira-Sequeira18 and Zanzani et al.78 who found that cohabitation with other dogs is one of the most important risk factors associated to endoparasitism. This might be attributed to that the presence of multiple dogs outdoor makes them more susceptible to infection with more environmental contamination.

Irregular deworming was found to be a contributing factor in the increasing prevalence of parasitic infection in dogs as 49 (56.4%) out of 156 dogs irregularly receiving anthelmintic drugs were harbored enteric parasite compared to 22 (8.6%) out of 255 dogs receiving anthelmintic regularly. While the increased awareness and controlling of dog parasites reduce the likelihood of environmental contamination and zoonotic transmission, irregular deworming without targeting of particular parasite were considered to be of less affectivity and increasing the drug resistance79. It is worth mentioning that a treatment frequency of at least 4 times per year or even a monthly treatment, are general recommendations according to different scenarios, e.g., real zoonotic risks, presence of children in the pet owners family, pregnancy of bitch and housing conditions80.

CONCLUSION

On conclusion, parasitological results in this study clearly highlight the significant role of pet dogs as a host for several species of enteric parasites; therefore preventive measures should be taken to avoid the environmental contamination and infection of both man and animals.

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