The identified parasites in the current study, with an overall prevalence of 83.02%, are presented in Table 1. The prevalence of 52.83% for Joyeuxiella spp. in stray cats of the present study seems to be remarkably higher than the earlier studies (Shiraz, Iran, 34.3% [13]; Mashhad, Iran, 7.6% [7]; and Egypt, 14.5% [14]). With a few exceptions, the prevalence rates of 67.1% in Dubai, UAE [15], 76% in Majorca Island, Spain [16], and 85% in Kashan, Iran [17] were mentioned in a review article conducted by Schuster [18].
According to the histopathological findings, the penetration of the adult worm into the intestinal mucosa caused intestinal damage and enteritis. The lesions associated with Joyeuxiella spp. might result in clinical manifestations of diarrhea in cats, which would propagate the parasite and the parasite eggs that perpetuate the transmission cycle. Joyeuxiella spp. may make cats more susceptible to secondary parasitizations, most likely due to adverse effects on the host that have been established through histopathological analysis. Along with the 38.68% prevalence of simultaneous infections with multiple parasites, it is interesting to note that almost 70% of the cats harboring T. taeniaeformis (21.70%) were also infected with Joyeuxiella species. It might suggest that these two cestodes have a shared intermediate host. Along with common wall gecko (Tarentola mauritanica), lizards, snakes, and amphibians can all harbor cysticercoids of Joyeuxiella spp. and T. taeniaeformis [16]. Therefore, it is crucial to consider coinfection with these two parasites. Additionally, some cases of Toxocara spp. (6 out of 16 positive cases) were simultaneously infected with Joyeuxiella spp., which might lead to the spread of eggs of this zoonotic parasite due to the resultant diarrhea.
The prevalence rate of T. taeniformis in the present study (21.70%) was higher than that found in Thailand (Bangkok, 0.07%; [19]), Portugal (Lisbon, 3.1%; [20]), Egypt (Beni-Suef, 9.6%; [14]), Iran (Mashhad, 9.6%; [7]), Shiraz, Iran (12%; [13]), and Iran (Kashan, 15%; [17]), and it was comparable to that reported in Egypt (Nile Delta, 22%; [21]). However, it has been reported to be lower than that which has been documented in India (Aizawl, 70.4%; [22]) and Qatar (Doha, 75.8%; [23]).
D. caninum was encountered with a modest prevalence (1.89%) compared to other studies. For instance, it has been found in 23%, 68.1%, 62.9%, and 40.7% of stray cats that were necropsied in the studies performed in Mashhad, Iran [7], Kashan, Iran [17], Egypt [14], and India [22], respectively. Although D. caninum infection is almost asymptomatic and is low pathogenic in cats, it should be treated properly, mainly because of its zoonotic potential [6, 23].
The most frequent nematode found in the stray cats of the current study was Physaloptera spp. (23.59%), while it has been previously reported to be 3.8% in Mashhad, Iran [7]. Higher prevalence rates of Physaloptera spp. infection have been reported in Kashan, Iran (39.8%) and Shiraz, Iran (44.6%) [17 and 13, respectively], and other countries such as Aizawl, India (44.4%) [22]. Physaloptera species are occasionally responsible for intermittent vomiting. Although they appear ascarids, they typically attach to the proximal duodenal mucosa by their anterior hooks [7].
After Physaloptera spp., T. cati was found to be the most prevalent nematode in the current study (15.09%). This infection rate of toxocariasis was more prevalent compared to that in Qatar [0.8%; 23], Brazil [2.2%; 25], Thailand [3.5%; 19], and Egypt [9%; 21]. Nonetheless, it was comparatively lower in comparison with the prevalence encountered in Iraq [25.58%; 26], Germany [27.1%; 27], Spain (35%; 16], Argentina [35.7%; 28], Portugal [38.3%; 20], and India [59.3%; 22]. The highest (86.3%) and lowest (8%) prevalence rates of T. cati in Iran have been previously reported by Yakhchali et al. [Ahar Municipality, Northwestern Iran; 29] and Esmaeilzadeh et al. [Zanjan, north-west of Iran; 30], respectively. Comparison of the present study with the earlier investigations highlighted that the difference in prevalence of the identified parasite species is possibly a result of regional, environmental, or climatic variations [21].
Another nematode, Rictularia spp., was found in the current study with a lower prevalence (1.89%) compared to the estimated prevalence of 52.2% in Kashan, Iran [17]. Limited information is available regarding the prevalence rate of this parasite in Iran [17].
The only protozoa found in this study, Isospora spp., had a low prevalence of 6.60% based on the analysis of fresh fecal samples. Additionally, C. felis, which is thought to be the most prevalent external parasite infesting cats [7, 29], was the only species of ectoparasites of the stray cats in the present study. This blood-sucking mite can lead to allergic dermatological reactions and dermatitis [7]. In accordance with Zibaei et al. [Shiraz, Iran; 13] and Borji et al. [Mashhad, Iran; 7], no ticks or fleas were discovered on the examined stray cats.
Among the detected parasites, T. cati (15.09%) is the most important one and is directly related to the sanitation measures in the study area. Several studies have been carried out to continuously monitor the prevalence rate of toxocariasis in stray cat populations in Shiraz. According to Mikaeili et al. [31], the rate of T. cati infection in stray cats was 26.7%, whereas it has been reported to be 3.9% in stray dogs of Shiraz, Iran [32]. According to Szwabe and Blaszkowska [33], stray cats are a more critical reservoir for the parasites than dogs.
A straightforward comparison of the studies clarifies that toxocariasis has dropped from 52.8% in 2001 [34] and 42.6% in 2007 [7] to 26.7% in 2013 [31], and also 15.09% in the present study. Although the changes are on a downward trend, the parasitic infections with this zoonotic nematode have continued to be relatively prevalent in stray cats of this area for the last 7–8 years. Therefore, increasing public awareness regarding feline zoonotic parasites, especially among locals, and improving sanitary standards and therapeutic and preventive protocols are crucial to reduce and minimize this zoonotic disease. Given the growing population of stray dogs and cats, human beings are at risk of being infected by accidental ingestion of embryonated eggs of Toxocara spp. through contact with contaminated hair of the infected cats, soil, water, salads, or raw vegetables [7, 29, 35].
The contamination rate of Toxocara spp. eggs has been reported 16% in 150 soil samples collected from public parks in Shiraz, southern Iran, by nested PCR [36]. Besides, as a source of viable and embryonated eggs, contact with contaminated cats’ or dogs’ hair sources is another risk factor [35, 37, 38]. Human beings can acquire the infection by ingesting nematode eggs from contaminated sources, and only a few nematode larvae can cause the syndrome of visceral larva migrans (VLM), ocular larva migrans (OLM), or neuro-toxocariasis [35]. Given that stray cats do not receive the same level of anthelmintic treatment as owed ones, they face severe parasitic infections and release the eggs into the environment.
It has been reported that each female worm lays a total of approximately 50,000 up to 200,000 eggs per day. A volunteer in 1959 was given orally approximately 100 embryonated eggs of T. canis in normal saline [39]. His blood eosinophil level increased from 5–26% on day 13 and 62% on day 30 post-infection. The eosinophilic level remained at 48% after 4.5 months of the ingestion. Therefore, it seems that each cat can infect a significant fraction of the population when there is a high prevalence of infection [34].
Additionally, cats habitually bury their feces, which may increase the chance that the T. cati eggs remain more vital and easily spread in the environment [22]. Moreover, the climate might facilitate the survival of the parasites and their eggs [22]. According to a recent systematic review undertaken by Abbaszadeh Afshar et al. [40], the seroprevalence of human toxocariasis has been reported to be 0.84-29% in various geographic locations of Iran and 2.4–92.8% in other countries throughout the world [40].
The high prevalence of Toxocara species in cats and dogs of Shiraz suggests that both urban and rural populations are likely to be affected by toxocariasis. In a study performed on 519 schoolchildren from Shiraz, southern Iran, the prevalence of Toxocara serum-positive samples was 25.60% [34]. Because toxocarid eggs are more likely to be encountered in rural areas, this percentage was higher among children who live there. On the other hand, geographic location, parents with low education, financial hardship, poor hygiene, and contact with infected cats as well as exposure to contaminated soil, have all been found and proposed as risk factors and have a strong correlation with seropositivity [32, 41]. Rural residency, exposure to cats and dogs, pica, and thumb sucking have all predisposed children to ingesting large numbers of Toxocara eggs from contaminated soils [41].
In the present survey, females were more frequently infected with parasites than males, but the difference was insignificant. In line with our study, earlier studies from various regions of Iran found no appreciable variation in terms of the prevalence of parasitic infections between males and females [7, 17, 29]. However, it has been reported earlier that females seem to have a higher prevalence of parasites due to their higher susceptibility to the stress associated with their reproduction behavior [16].
Age has been implicated as a significant risk factor for parasitic infections in the case of cat populations, with cats less than six months old being more susceptible to infection than the older ones [17]. However, our study revealed a higher prevalence of the parasites in cats older than one year compared to the younger ones, which is contrary to the conclusions drawn from other studies [7, 13, 19, 34]. These controversial findings could be attributed to the accessibility of infected foods for various age groups, genetics, or level of immunity against the helminth infection in the examined cats, in addition to the variations in sample sizes and the frequency of the cats in different age groups.
In conclusion, the high prevalence of parasitic infections, particularly T. cati, in stray cats in this study is a warning sign, especially for school children and the younger children playing in the parks, who are seriously at risk. If all preventive and therapeutic measures are not taken, the infection could spread widely; the prevalence rate may drastically increase, and inflict serious diseases. Therefore, it is crucial to inform and educate the public regarding the hazards and zoonotic aspects of zoonotic parasitic infections, particularly those caused by Toxocara species. It is important to remember that stray animals, including dogs and cats, are difficult to control. Nevertheless, the first step is to reduce the chance of becoming infected, limiting the risk of the disease spreading. In the next steps, local authorities should plan effective measures and strategies to control the population of homeless cats, including building new shelters with appropriate veterinary care, mass sterilization of cats, stricter enforcement of pet ownership laws, educating owners, and making people more responsible for these abandoned animals.