4.1. Risk of Infection by Group
The prevalence of parasites found in dog fecal samples in Portugal and in other countries are presented in Table 5
Prevalence of parasites found in dog fecal samples in Portugal and in other countries.
Prevalence of parasites found in dog fecal samples in Portugal and in other countries.
|Authors||Country||N||Dog Sample Origin||Overall Prevalence|
|Tarsitano et al. ||Italy||152||Environmental||8.5%|
|Rinaldi et al.  ||Italy||415||Environmental||16.9%|
|Dubná et al. ||Czech Republic||3780||Environmental + Shelter Dogs||17.6%|
|Martínez-Carrasco et al.  ||Spain||275||Dogs presented to veterinary clinics + Shelter Dogs + Stray Dogs||25.0%|
|Papazahariadou et al.  ||Greece||281||Farm Dogs + Hunting Dogs||26.0%|
|Gracenea et al.  ||Spain||505||Shelter Dogs||26.9%|
|Soriano et al. ||Argentina||1944||Environmental||37.9%|
|Szabová et al. ||Slovak Republic||752||Environmental + Owned Dogs + Shelter Dogs||45.7%|
|Balassiano et al.  ||Brazil||500||Dogs presented to veterinary clinics||46.4%|
|Fontanarrosa et al.  ||Argentina||2193||Owned Dogs||52.4%|
|Okoye et al. ||Nigeria||413||Stray Dogs||52.6%|
|Benito et al. ||Spain||1040||Shelter Dogs||53.6%|
|Katagiri and Oliveira-Sequeira ||Brazil||254||Owned Dogs||54.3%|
|Beiromvand et al. ||Iran||77||Owned Dogs + Stray Dogs||66.0%|
|Bajer et al. ||Poland||108||Sled Dogs||68.0%|
|Ugbomoiko et al. ||Nigeria||396||Owned Dogs||68.4%|
|Martínez-Moreno et al. ||Spain||1800||Shelter Dogs||71.3%|
|Gingrich et al. ||Galapagos Island||97||Owned Dogs||71.4%|
|Eguía-Aguilar et al. ||México||120||Stray Dogs||85.0%|
|Mandarino-Pereira et al. ||Brazil||81||Environmental||92.6%|
|Crespo and Jorge ||Portugal||576||Environmental||17.9%|
|Cruz et al. ||Portugal||49||Environmental||18.4%|
|Neves et al. ||Portugal||368||Dogs presented to veterinary clinics||20.6%|
|Mateus et al. ||Portugal||100||Shelter Dogs||41.0%|
|Crespo et al. ||Portugal||548||Environmental||50.0%|
|Cardoso et al. ||Portugal||301||Farm Dogs||58.8%|
The diversity of results obtained from different studies highlights the importance of promoting research at the local level to plan control strategies [7
]. The differences reflected in Table 5
may be partially explained by the origin of the dog samples. Animals placed in shelters are dewormed by veterinarians [41
], but the high densities observed frequently in shelters may contribute to the propagation of these parasites [42
]. There is also a wide disparity with regard to the sampling collection methods (many of the studies included in Table 5
involved collection of samples per rectum
or in necropsy), the number of samples collected and the coprological method used, making it difficult to compare results. There is no unique technique capable to do the parasitological diagnosis of all kinds of parasitic species that may be present in feces [43
]. Although compared to post-mortem
fecal examination fecal flotation is less sensitive in the detection of parasites [21
], faecal flotation is considered a very valuable method for the assessment of the majority of dog parasites [45
]. The frequency found in the positive samples is high, and the risk of parasitism and occurrence of multiple infections is higher in hunting dogs. This highlights the need of health education in a specific target group: hunters and their families.
A much lower parasite prevalence in hunting dog samples than in the present study has been previously reported [22
]. Hunting dogs are at the highest risk of worm infections and are therefore responsible for most environmental contamination and human disease [46
]. Helminth zoonoses transmitted among dogs, wildlife, and people have been discussed by Jenkins et al.
]. In Portugal the impact of wildlife on public health is unknown [17
], however, zoonotic helminths in wild carnivores fecal samples have been found in footpaths of a protected area in Ponte de Lima, where people, domestic and wild animals coexist [48
Access to soil, the hygiene of the environment, illness, the owners’ level of education, and veterinary care, are all associated with intestinal parasite infections in dogs [25
]. Concerning the farm and hunting dogs that were sampled, no clinical signs were observed, this is in agreement with Neves et al.
]. In a study about dog owners’ awareness conducted in this municipality it was concluded that the practices used to deworm dogs, if any, were not correct, and few owners referred fecal elimination after deworming [49
], which is in agreement with other surveys [6
]. Szabová et al.
] found that the environmental samples had the lowest prevalence recorded. In our study, some of the environmental samples were not as fresh as those from the farm or hunting dogs, so it was somehow expected to find lower parasite prevalence in these samples. On the other hand, supposing that environmental samples correspond to stray dogs, these usually do not undergo deworming, and therefore they are possible carriers of many parasites [32
]. Our results could be explained by our environmental samples in fact not being from homeless dogs, but from owned dogs that have free outside access, as Ponte de Lima is mainly a rural municipality.
4.2. Diversity of Parasites Found and Individual Prevalence
In the examined samples, seven parasitic species were isolated. A similar number has been recorded in other studies [17
], although several refer a higher [1
] or lower [26
] number of parasitic species. In addition to the number of parasitic species, there is a great variability in isolated species and specific prevalence which indicates the necessity of being cautious when extrapolating conclusions from data from one location to another.
There is also variety concerning the most prevalent intestinal parasite found in different studies: Ancylostomatidae or Ancylostoma caninum
spp. or Toxocara canis
], Isospora canis
] and Cryptosporidium
]. Once again this discrepancy may be due to most of the variables previously mentioned, namely the different methodologies used.
A Pareto analysis showed that most of the parasitic forms were Ancylostomatidae and Trichuris
spp. Interestingly Rubel et al.
] reported that the highest prevalence of eggs of both these parasite was detected in areas with lower socio-economic level, and Szabová et al.
] pointed to the contamination of the environment in which animals move.
For Papazahariadou et al.
], Ancylostomatidae were more frequent in farm dogs rather than hunting dogs, unlike in our study.This may be associated, in our study, with the local habit of keeping hunting dogs in kennels where they defecate, maintaining a highly infective habitat [11
]. Dogs are hosts to hookworms that may cause zoonotic diseases, most notably cutaneous larva migrans
spp. were the most frequent intestinal parasites found in hunting dogs. Most of the other studies have reported a much lower prevalence [1
]. The eggs may remain viable and infective in the environment for years, leading to high infection rates in dogs [57
]. Humans can be infected by Trichuris vulpis
some cases have already been reported [58
eggs were more commonly found in farm dogs. According to Cardoso et al.
], the domestic slaughtering of pigs and small ruminants showed a statistical association with Toxocara
infections, and this practice is usual in farm dog owners in this municipality. Human infection is caused by direct contact with contaminated soil or dog hair [59
]. Visceral larva migrans
, ocular larva migrans
], and severe diseases affecting the central nervous system and/or the eye can occur [61
]. We found infective Toxocara
spp. eggs in a few environmental samples. In most rural and urban resource-limited communities, children are considered the highest risk group [12
], however in farms, adults and children are equally susceptible to soil-transmitted infections [62
]. Very high Toxocara canis
seroprevalence has been found in farmers, veterinarians, slaughterhouse staff and hunters [63
]. Health education to raise public awareness is therefore strongly encouraged [26
is an ascarid less frequent than others, as our and other studies confirm [20
]. In contrast, Beiromvand et al.
] found it to be the most frequent. Dipylidium caninum
has been usually considered the most frequent Cestoda in dogs [27
], as reported in our study. Humans can become infected and very young children are the ones most often affected [64
]. Symptoms are usually absent, although abdominal discomfort, diarrhea and pruritus may be present [65
The detection of Taeniidae eggs in fecal samples by routine microscopy suffers from low sensitivity [6
]. A cross-sectional survey in Germany and other European countries have detected these eggs only in 0.25% of the samples [66
]. In Portugal, owning cattle was found to be a significant risk factor for Taenia
spp. presence in dogs [17
] however, in our study, the higher prevalence of positive samples was not in farm dogs, but in hunting dogs. The coat of the foxes can be contaminated with Taeniidae eggs [67
], so hunters—human and dog—can be directly exposed to these immediately infective eggs [6
spp. eggs are morphologically indistinguishable from Taenia
spp. Echinococcosis is one of the five most important zoonoses in the Mediterranean region [68
], nonetheless, it remains a neglected zoonosis [69
]. Despite the low sensitivity of fecal based methods to Echinococcus granulosus
egg detection, it is revelant for public health to remark the absence of these parasites in our study.
Unlike in some studies [25
], helminth eggs were more commonly identified than protozoan. The trend of reducing helminthic and increasing protozoan infection has been attributed to the knowledge of dog owners about potential zoonotic transmission of these agents and how to control them [70
]. These facts stand in contrast with the results of our study, in this may be explained by limited awareness in Ponte de Lima. Although the methods used are not appropriate for protozoan diagnosis we did find Isospora
spp. and these parasites were more prevalent in hunting dog samples.
Undoubtedly, the present study revealed poor hygiene conditions and animal housing, similarly to Cardoso et al.
]. Furthermore, a wide diversity of zoonotic parasites has been detected, and well distributed throughout the municipality.
4.5. “One Health” Approach Is Required
A close collaboration between veterinary and public health professionals in a “One Health” approach is required [5
]. In Portugal, veterinary practitioners acting as information sources about zoonoses transmitted by canids are needed, but there are basic priorities that should be considered first. So far, data is limited to only a few urban areas and no information is available for large territories of the country with more suitable socioeconomic and environmental conditions for parasitic transmission. Multidisciplinary approaches will lead to a more complete understanding of the actual epidemiological situation in the country. Few studies have been undertaken to determine the prevalence of these organisms and/or their associated diseases in people from the same community. Many physicians are not knowledgeable about these infections [73
], and they feel that a collaborative relationship with a veterinarian who possesses specialty training in zoonoses would be valuable to their practice [74
]. Several studies have shown that physicians delegate to veterinarians the responsibility to do health education of communities concerning zoonoses [46
], and suggest that veterinarians should be involved not only in controlling zoonotic disease in animals, but also in providing information for patients and physicians [75
]. Nonetheless, communication among veterinarians, physicians, and dogs owners or human patients seems to be insufficient [76
]. Although changing in human behavior is an extremely difficult challenge [46
], this is essential for the success of the control and prevention of these diseases. Effective campaigns and education programs could be instituted to prevent of zoonotic infections associated with household pets and address issues surrounding poorly prepared or cooked food [76