This study estimated the prevalence of major digestive and respiratory helminths in client-owned dogs and cats in France and explored associations between parasitic infestation and qualitative factors. The results indicate that Toxocara cati in cats, and T. canis and Uncinaria stenocephala in dogs, were the most common helminths detected in the faecal samples, whereas whipworms (Trichuris vulpis) in dogs, tapeworms (Dipylidium caninum and Taeniidae), and lungworms (Angiostrongylus vasorum, Aelurostrongylus abstrusus) were less commonly found. Significant correlations were observed between infection and the following criteria: age and deworming habits for dogs and cats, reproductive status, food type, presence of other animals in the house, and living environment/lifestyle for cats, and living environment, dog’s activity and time spent outside off-leash for dogs.
Estimated parasite prevalence
Previous epidemiological surveys performed in France on the prevalence of internal parasites in pets showed contrasting results. Comparing these studies is difficult due to their different designs, methods used for detecting parasites, animal populations, geographical location, environment, age distribution and season [7, 8, 15, 16].
In the present study, 15.2% of the dogs and 14.6% of the cats were infected by at least one of the targeted parasites, which is below the prevalence rates of the last national report from 1997 (21.6% in dogs and 17.3% in cats) . In both studies, the prevalence of infection in animals <1 year-old was relatively similar for dogs, but lower for cats in the present study compared to results obtained in 1997 (27.7% vs 24.7% in dogs and 31.7% vs 23.5% in cats, in 1997 and in the present study, respectively). Ascarids (Toxocara canis and T. cati) were the most frequent helminths (8.5% in dogs and 11.3% in cats) with prevalence rates similar to previous studies (5.4 ─ 23% for T. canis and 2.9% ─ 14.2% for T. cati [8, 15, 17]. We didn’t detect Toxascaris leonina in dogs and only at a very low prevalence in cats (0.2%) as in previous French reports, with usual findings of less than 1% of positive animals [6, 7, 18]. In the present study, hookworms were identified in dogs (A. caninum and U. stenocephala; 1.7% and 4.3%, respectively), but not in cats (A. tubaeforme). These results were within the range of prevalence rates for these parasite species (0.5–3.4% for A. caninum and 2.1–17.2% for U. stenocephala) published in other studies conducted in France [15, 18–20]. Trichuris vulpis was detected in only 2.7% of the dogs in our study whereas prevalence rates in another survey in France reached 19% . This difference may be due to the fact that we only enrolled client-owned dogs while in the previous surveys animals living in groups were included and also to differences of sensitivity of coproscopical methods. Prevalence rates for tapeworms based on coproscopy, generally do not exceed 3% in France [6, 7]. We detected tapeworms (D. caninum and Taeniidae) more frequently in cats (1.9% and 1.2%, respectively) than in dogs (D. caninum only [0.5%]). However, these prevalence of tapeworms might be underestimated, especially due to the intermittent rectal excretion of gravid segments.
Cardio-respiratory nematodes were rarely detected in the faeces of dogs and cats (0.5% for the French heartworm Angiostrongylus vasorum and 0.7% for Aelurostrongylus abstrusus). This prevalence of Angiostrongylus vasorum is lower than in previous studies in France [1.14-1.25%; 17,21,22] and in countries bordering France [e.g., 0.5 - 3.1%; ,23–25] in healthy client-owned dogs, with differences according to the detection method used (antigen detection, antibody detection and/or coproscopical analyses). In France, the cat lungworm, Aelurostrongylus abstrusus, is considered sporadic. However in recent years, the distribution of this parasite seems to be spreading in several countries, with prevalence rates up to 20% in enzootic areas [6, 26, 27]. In our study, the other metastrongyloid, Troglostrongylus spp., responsible for severe respiratory disease in cats, was not detected whereas it has been recently reported in Southern Europe [28–30].
Younger age is associated with a higher risk of internal parasitism, as observed in our study and previous studies [31, 32]. Certain modes of transmission (e.g., trans-placental and/or trans-mammary contamination) that are exclusive to the newly whelped or neonates and the limited immunity to parasites in young pets explain the higher prevalence of T. canis or T. cati in young individuals [6, 8].
Living environment and lifestyle are also major factors influencing parasite risk for both dogs and cats. A positive correlation between parasite prevalence and rural areas has been described for T. cati, Ancylostoma spp., and lungworms in cats  and T. canis in dogs . The higher parasite prevalence in cats with outdoor access was previously reported for T. cati and Ae. abstrusus [6, 32, 33].
We observed that outdoor access, rural areas, time off-leash, and hunting/herding for dogs are the main factors increasing the risk of parasite risk, with odds-ratio up to 5.34. All these living conditions are associated with outdoor access of animals with no or limited control of animal activities from the owner when outdoors, and outdoor areas are typically larger and vegetated. In addition, wildlife is more abundant and diverse in rural and natural areas. All these factors are expected to increase the probability of encountering infective parasite stages by dogs and cats, either on the ground or in intermediate/paratenic hosts (e.g., snails, birds, rodents).
Cats living with several other pets were significantly more infected than cats living alone or with few animals and a similar trend was observed for dogs in our study. In a previous study, cats living with one or two other cats were not significantly more infected than cats living alone, but for higher densities of cat populations (more than 3 other cats in the house), the risk for Toxocara infestation was significantly more important . The higher prevalence observed can be due to a higher risk of contamination due to the higher number of animals in a limited environment, to a higher probability to hunt and eat prey, and also, perhaps to a lower interest or financial support for veterinary care by owners of several animals.
The food type was associated with parasite prevalence in cats in univariate analyses, with a higher prevalence in cats not fed exclusively with commercial diets. The lowest prevalence was observed in cats exclusively fed commercial diets, and prevalence increases with the partial or full replacement of commercial diets. Parasite prevalence exceeded 30% in cats exclusively fed with homemade food and raw meat. While such a factor was not relevant in a previous study , it might partly be explained by the presence of infective parasite stages in raw or undercooked meat.
Intact cats more frequently harboured parasites in their feces than spayed/neutered cats in our study. Such findings can result from lower roaming activities in neutered/spayed cats compared to intact cats, decreasing potential risk of exposure to parasites , even if some authors didn’t observe any difference in activity level according to the reproductive status [36, 37]. In addition, intact cats are probably less medicalized than neutered/spayed cats and, therefore, deworming is probably less frequent (never dewormed cats >6 months of age: 35.9% (n = 37/103) and 16.8% (n=44/262) of intact and neutered, respectively; P < 0.001).
Guidelines for the control and treatment of parasites in pet animals are proposed by the European Scientific Councel Companion Animal Parasite (ESCCAP) . For instance, puppies should be treated with appropriate anthelminthics against roundworms from the age of 2 weeks, then every 14 days up to 2 weeks after weaning because of milk transmission, and then monthly up to 6 months of age. The schedule should be similar in cats, except that because prenatal infection does not occur in kittens, fortnightly treatment can begin at 3 weeks of age . Then, the different risk factors are described to help veterinarians propose a customized deworming program to pet owners.
Although the majority of pet owners give anthelminthic drugs, our results show that most of them do not follow the ESCCAP recommendations . Thirty-two percent and 23.8% of all dogs and cats, respectively, had not been dewormed within the 12 previous months. The proportion of never dewormed animals was the highest in animals less than 6 months of age (≤6 months vs. >6 months of age: 70.7% (n=41/58) vs. 22.2% (n = 81/365) for cats; 31.8% (n = 27/85) vs. 7.5% (n = 23/306) for dogs). However, young animals were often only a few months old when recruited into the study, when they were presented to the clinic for vaccines, and their owner(s) did not have any recommendation from a vet before study recruitment. This can explain the low frequency of previously dewormed animals in the young animal group. The generally advocated four-times-a-year deworming advice was poorly applied as only 38.9% (n=37/95) and 24.1% (n=81/208) of dogs and cats, respectively, older than 2 years with outdoor access receive ≥ 3 deworming treatments per year. Moreover, as suggested by the results of recent studies [39, 40], a significant percentage of dogs or cats could “benefit” from more frequent treatment (or fecal analyses) as suggested by ESCCAP .
The results obtained in this study show that animals receiving no anthelmintic treatment were significantly more infected by helminths than animals receiving 1-2 treatments/year. Surprisingly, parasite prevalence was similar in animals never dewormed and animals dewormed ≥3 times per year. These unexpected observations that have also been reported in previous studies  may be partially explained by possible reinfestations from a contaminated environment, possible reactivations of Toxacara spp. larvae encysted , coprophagy in dogs leading to false positive faecal samples. The significant effects of deworming frequency on parasite prevalence in univariate tests but not in multivariate analyses suggests statistical biases. Confounding effects with age cannot be excluded as young pets where often never dewormed at the first visit to the vet but dewormed monthly prior to the following examination.