The present study is the first large-scale effort to determine the prevalence of intestinal parasites in dogs visiting dog parks throughout the USA. In 2019, the 100 largest USA cities contained a total of 810 dedicated dog parks . Testing of samples collected from 288 parks in 30 of these cities allowed us to document parasites in over 20% of dogs and 85% of parks. The prevalence of parasite infection in dogs in the present study is higher than that seen in pet dogs with fecal samples submitted from veterinary practices to national diagnostic laboratories (12.5%), but lower than that reported from stray dogs upon arrival at municipal shelters (36%). The differences in findings between the pet dog survey and this study may be due to CAI detecting some infections missed by CF, the only method used in the earlier survey, and to the fact that while dogs attending dog parks receive attention from their owners, not all benefit from routine veterinary care [2, 5].
Giardia was the most commonly identified intestinal parasite, both in the present study (13.0%) and in an earlier national report of parasites in pet dogs (4.0%) . In contrast, Giardia was only rarely detected (0.6%) in a national survey of shelter dogs in which samples were examined by sugar CF, presumably due to the lower sensitivity of this method for recovering the fragile cysts [5, 12]. Infections with Giardia are often subclinical, and cysts or trophozoites are shed intermittently from infected dogs, limiting the diagnostic sensitivity of CF as a stand-alone method. This may have been one factor behind the much higher rate of detection of Giardia infection by CAI than by CF, as would the fragility of Giardia cysts, leading to their degeneration between collection of fresh samples and CF testing at the laboratory. By combining CAI with CF, the present study may better estimate the true prevalence of infection. An earlier report using a similar strategy (CF + CAI) found a Giardia prevalence of 15.6% among dogs presenting to clinics with diarrhea or vomiting . Dogs in shelters, breeding facilities and kennels are more likely to be infected with Giardia, and an increased prevalence among dogs that visit dog parks, compared with those not visiting dog parks, has been reported .
Nematodes were also commonly detected, identified in 10% of the samples tested. As in other studies using CF alone, the hookworm A. caninum and whipworm T. vulpis, which present a risk to canine health throughout all life stages of a dog, were the most common intestinal nematodes identified [14, 25, 26]. The results may underestimate the prevalence of T. vulpis and T. canis, as samples were collected during July and August, a time when infections with these nematodes may be at their lowest prevalence . Surprisingly, passive flotation remains the most commonly used technique in clinical practice despite multiple studies demonstrating that it fails to detect many infections when compared to CF [12,13,14,15]. Combining CAI for nematode antigens with CF in the present study resulted in detection of nearly 80% (78.4%) more nematode infections than CF alone, likely due to the CAI detecting non-patent infections [16, 17]. Detection of parasite ova by CF in instances when CAI was negative could be due to coprophagia or predation, resulting in a positive CF in the absence of infection. In this study, 37 (1.2%) samples tested positive for Eimeria spp., supporting the role coprophagy may have played in the discordant results. Another factor could be that a low intensity infection may not produce sufficient antigen, leading to a negative CAI even though some ova were being shed [14, 17]. These findings reinforce the previously demonstrated complementary value of combining CAI with CF to enhance intestinal nematode detection .
Cestodes or trematodes were only rarely detected in the present study, even though recent studies in the USA have shown that the prevalence of infection with common tapeworms (e.g. Dipylidium caninum, Taenia spp.) is greater than that of nematodes in some populations of dogs and cats [14, 29]. Because eggs of cestodes common in dogs are shed in proglottids, and because most cestode and trematode eggs are heavy, recovery by CF is poor . Using a higher specific gravity sugar solution for CF in part addresses this limitation, enhancing recovery of taeniid eggs, but sensitivity remains very low for identifying Dipylidium caninum infection [14, 30], and CAI is not yet commercially available for canine cestodes or trematodes. Eggs of Spirometra sp. or Alaria sp., less common cestodes and trematodes of dogs, respectively, are occasionally detected on CF. In the present study, Spirometra sp. eggs were identified in two dogs and Alaria sp. eggs in one dog.
As with earlier national reports, although parasites are found in every region, the present study indicates that the highest prevalence of nematode intestinal parasite infection, and in particular A. caninum infection, occurs in the Southeast [2, 5]. This factor, together with the very high prevalence of heartworm infection in the southeastern USA, likely explains the common owner-reported use of HWCM in this region. Other canine surveys from the region support that hookworm and whipworm are very common, identifying A. caninum in as many as 48% of shelter dogs and 17% of samples from dog parks, and T. vulpis in up to 39% of shelter dogs and 8.5% of samples from dog parks [14, 26, 31, 32].
In the present study, more than 15% of dogs visiting dog parks in the Southeast, and 4 to 5.3% of those in the Midwest and Northeast, were infected with hookworm, a finding that is particularly concerning given the recent reports of multiple drug-resistant hookworms in pet dogs, including Greyhounds [33,34,35]. Although we do not know the resistance status, six of the 12 Greyhounds sampled from dog parks in the present study were positive for hookworm, and five of those six were reported by the owner to be on a HWCM at the time they were sampled, compared to 57.7% of non-Greyhound, hookworm positive dogs that were reportedly receiving a HWCM (data not shown). Hundreds of thousands of stray and rescue dogs, including retired Greyhounds, are commonly relocated from the southern USA to other regions, a practice that can facilitate movement of parasites, including resistant parasites [7, 36, 37].
Intestinal nematodes, particularly A. caninum and T. vulpis, but not all intestinal parasites (e.g. Giardia, Cystoisospora spp.), were less commonly detected in samples from dogs reportedly receiving HWCM in the present study, providing evidence that implementing broad-spectrum parasite control measures reduces infections and limits environmental contamination with eggs. This finding has long been suspected and is supported by other regional surveys [26, 38]. However, hookworm, whipworm, or ascarid infections were still detected in some dogs reportedly receiving HWCM in the present study, perhaps due to the earlier detection afforded by antigen testing, the short (2‒3 weeks) prepatent period of hookworm, and the fact that not all HWCMs are effective against whipworm or other intestinal nematodes [16, 17, 28, 39]. For example, injectable products are not effective against either whipworm or ascarids, and are not FDA-label approved for efficacy against new hookworm infections beyond the time of initial administration [40, 41]. Products containing ivermectin/pyrantel are effective against A. caninum, Ancylostoma braziliense and U. stenocephala, but are not effective against whipworms . Those containing milbemycin oxime are effective against whipworms, ascarids and the common hookworm, A. caninum, but not against its relatively scarce and less pathogenic relative, U. stenocephala . Topically applied moxidectin is indicated to treat and control T. vulpis, A. caninum, U. stenocephala and ascarids . The hookworm efficacy of all these treatments is based on having demonstrated efficacy prior to reports suggesting the incipient emergence of multi-drug resistant A. caninum [33, 35]. Detection of nematode infections and other parasites in dogs reported to be receiving HWCMs in the present study indicates that regular testing is warranted for all dogs even when these medications are used.
Interestingly, a majority (68.8%) of owners in the present study reported current use of a HWCM, similar to other recent papers surveying dog owners in Oklahoma and Florida [26, 45]. This high owner-reported prevalence of use contrasts with other data indicating that, even in areas where heartworm infection is common, only a minority of pet dogs receive a HWCM [46, 47]. Factors that may bias owner-reported use of HWCM include forgetfulness, guilt about not following veterinary recommendations, and confusion about a given product’s efficacy for heartworm versus external parasites. Additionally, the study was conducted in the summer months, when mosquitoes are most active, a timing that may have resulted in a higher proportion of owners reporting current use of HWCM. Routine use of HWCM is critically important because many of the products can limit environmental contamination with zoonotic parasites like A. caninum and T. canis which cause cutaneous larva migrans and toxocariasis, respectively. Other strategies such as reducing the number of stray or free-roaming animals, prompt removal of all pet feces, wearing shoes to avoid skin contact with contaminated soil, hand-washing after handling feces or soil, and avoiding geophagy in children can also reduce infection risk .