The aim of the present study was to estimate the current prevalence of major digestive and respiratory helminths in client-owned dogs and cats in France and to explore associations between parasitic infestation and qualitative factors. The results indicate that Toxocara cati in cats and Toxocara canis and U. stenocephala in dogs were the most common helminths detected in the faecal samples, whereas whipworms (Trichuris vulpis), Strongyloïdes stercoralis, Eucoleus spp./Capillaria spp., the French heartworm Angiostrongylus vasorum, the lungworms Aelurostrongylus abstrusus and Crenosoma vulpis, and tapeworms (D. caninum and Taeniidae) 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.
The detection of endoparasites was based on standardized coprological analyses performed by trained people in expert centers. The techniques and protocols used in each laboratory were in accordance with standard guidelines and routinely conducted for parasitological diagnosis. However, coproscopical analyses have a low sensitivity for some parasites and, consequently, some limitations of the methodology and analysis may have resulted in underestimation of the reported prevalence ; these include:
Some parasites may have not been detected because they were still immature (sample collected during the pre-patent period, before the development of mature adults) or because the shedding of eggs or tapeworm segments in the faeces was intermittent for some parasites. In this study, faecal samples were collected at a single time-point for each animal in order to avoid onerous practical constraints for the owners and to limit the risk of reduced participation. To limit biases associated with intermittent shedding of propagules and improve detection probability, faecal sampling could have been performed on 3 consecutive days [6, 16].
Faecal samples collected in the private clinics were shipped at ambient temperature within 48 h, and analysed within 5 days after collection (stored at 4 °C). During shipment, some worm eggs may have hatched and, consequently, may be not detected in the fecal float, resulting in a false negative result.
Many different procedures and techniques are used, each with their own advantages and limitations. The methods most frequently used to recover parasite eggs are flotation techniques that rely on the differences in the specific gravity of the egg(s), fecal debris and flotation solution. The specific gravity of most parasite eggs is between 1.05 and 1.23 . The saturated sodium chloride (NaCl; specific gravity: 1.20) used in this study is effective for recovering Toxocara canis, A. caninum and Trichuris vulpis eggs. For all three of these parasites, while an additional centrifugation step should have isolated a significantly higher fecal counts compared with the simple fecal flotation method, the specific gravity of the selected flotation solution and the absence of centrifugation do not seem to affect the number of infections detected [18, 19]. Incorporating other diagnostics strategies, including detection of fecal antigen for nematodes, would certainly have helped to improve diagnostic sensitivity in our study .
The diagnosis of larvae from cardio-pulmonary nematodes (e.g. Angiostrongylus vasorum and Aelurostrongylus abstrusus) can be based on several techniques, including Baermann/McKenna coproscopy, serological test detecting circulating antigens, enzyme-linked immunosorbent assays (ELISAs) for antibody detection and quantitative PCR test on bronchoalveolar lavage material. Studies comparing serological tests and the coproscopical technique of Baermann have shown that coproscopy remains a very useful tool for the diagnosis of both A. vasorum and A. abstrusus [21, 22]. In this study, the McKenna technique was used because it is easier to use and more sensitive than the Baermann method .
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 varying designs, methods used for detecting parasites, animal populations, geographical location, environment, age distribution and seasons of sample collection [7, 8, 23, 24].
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 reported in the last national survey report from 1997 (21.6% in dogs and 17.3% in cats) . In both studies, the prevalence of infection in animals aged < 1 year 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 frequently found helminths (8.5% in dogs and 11.3% in cats), with prevalence rates similar to those reported in previous studies (5.4–23% for T. canis and 2.9–14.2% for T. cati [8, 23, 25]). Toxascaris leonina was not detected in dogs and only detected at a very low prevalence in cats (0.2%), similar to previous French reports, with the usual findings of < 1% of positive animals [6, 7, 26]. In the present study, hookworms were identified in dogs (Ancylostoma caninum and U. stenocephala, 1.7% and 4.3%, respectively), but not in cats (Ancylostoma tubaeforme). These results were within the range of prevalence rates previously reported for these parasite species (0.5–3.4% for A. caninum and 2.1–17.2% for U. stenocephala) in other studies conducted in France [23, 27]. Trichuris vulpis was detected in 2.7% of the dogs in our study, whereas prevalence rates in another survey in France reached 19% . This difference may be due to only client-owned dogs being enrolled in the present study, while previous surveys included animals living in groups. The sensitivity of coproscopical methods between surveys may also have resulted in significantly different findings. 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 prevalences of tapeworms might be commonly underestimated, especially due to the intermittent rectal excretion of gravid segments.
In the present study, cardio-respiratory nematodes were rarely detected in the faeces of dogs and cats (0.5% for the French heartworm Angiostrongylus vasorum, 0.2% for Crenosoma vulpis and 0.7% for Aelurostrongylus abstrusus). This prevalence of A. vasorum is lower than that reported in previous studies in France (1.1–1.3%) [25, 28] and in countries bordering France (e.g. 0.5–3.1%) [29,30,31] in healthy client-owned dogs, with differences accounted for according to the detection method used (antigen detection, antibody detection and/or coproscopical analyses). In France, the cat lungworm, A. abstrusus, is considered to be 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, 32, 33]. In our study, the other metastrongyloid, Troglostrongylus spp., which is responsible for severe respiratory disease in cats, was not detected whereas it has been recently reported in southern Europe [34,35,36].
Younger age is associated with a higher risk of internal parasitism, as observed in our study and in previous studies [37, 38]. Certain modes of transmission (e.g. trans-placental and/or trans-mammary contamination) that are exclusive to 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 A. abstrusus [6, 38, 39].
We observed that outdoor access, rural areas, hunting/herding and time off-leash for dogs are the main factors increasing the risk of parasite risk. All of 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 of 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 (> 3 other cats in the household), the risk for Toxocara infestation was significantly higher . This higher observed prevalence 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 the 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 the prevalence was found to increase with the partial or full replacement of commercial diets with alternative food. Parasite prevalence exceeded 30% in cats exclusively fed 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 faeces than spayed/neutered cats in our study. Such findings may result from lower roaming activities in neutered/spayed cats compared to intact cats, decreasing the potential risk of exposure to parasites , even if some authors of previous studies did not observe any difference in activity level according to reproductive status [42, 43]. In addition, intact cats are probably less medicalized than neutered/spayed cats and, therefore, deworming probably occurs less frequently (never dewormed cats aged > 6 months: 35.9% (n = 37/103) in intact cats and 16.8% (n = 44/262) in neutered cats, respectively; P < 0.001).
Guidelines for the control and treatment of parasites in pet animals have been proposed by the European Scientific Councel Companion Animal Parasites (ESCCAP) . These guidelines include the recommendation that 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 and, therefore treatment every 2 weeks can begin at 3 weeks of age . The guidelines also describe the various risk factors to help veterinarians propose a customized deworming program to pet owners.
Although the majority of pet owners give their pets anthelminthic drugs, our results show that most owners do not follow the ESCCAP recommendations . Of the animals included in the present study, 32% of dogs and 23.8% of cats had not been dewormed within the 12 previous months. The proportion of animals never dewormed was the highest in animals aged < 6 months (≤ 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) had not received 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 implemented as only 38.9% (n = 37/95) and 24.1% (n = 81/208) of dogs and cats, respectively, aged > 2 years with outdoor access received ≥ 3 deworming treatments per year. Moreover, as suggested by the results of recent studies [45, 46], a significant percentage of dogs or cats could “benefit” from more frequent treatment or faecal analyses, as suggested by ESCCAP .
The results obtained in this study show that faecal samples from animals never dewormed /dewormed > 1 year ago were positive for helminths significantly more often than samples from animals dewormed within 365 days of study participation. Surprisingly, parasite prevalence was the lowest in animals dewormed 6–12 months previously. This unexpected observation along with the absence of significant influence of the time since last deworming in multivariate analyses suggest statistical biases. We cannot exclude confounding effects with age and parasitic risk, such as: (i) young pets were often never dewormed prior to the first visit to the veterinarian and enrolment in the study, but were then dewormed monthly prior to the subsequent examination; (ii) young pets have a higher prevalence of parasites and are more frequently dewormed than adult animals; and (iii) deworming frequency in pets aged > 6 months is prescribed according to parasitic risk, leading to low frequency of deworming in pets at low risk.