High Prevalence of Covert Infection With Gastrointestinal Helminths in Cats
Fecal flotation is routinely used to identify feline helminth infections in clinical practice, but it is known to have limitations of sensitivity, particularly for cestodes. To determine the prevalence of helminths in a contemporary population of cats and evaluate the ability of fecal flotation to detect these infections, helminths were recovered from intestinal tracts removed from 116 adult cats humanely euthanized by an animal control shelter in northeastern Oklahoma. Results were compared to those of fecal flotation performed using both passive and centrifugal techniques. Helminths were identified in 78/116 (67.2%) cats, including Toxocara cati (48/116; 41.4%), Ancylostoma tubaeforme (8/116; 6.9%), Dipylidium caninum (40/116; 34.5%), and Taenia taeniaeformis (30/116; 25.9%). Cats with T. cati were significantly more likely to harbor T. taeniaeformis (P = .001) than cats without ascarids. Centrifugal fecal flotation with sugar solution identified 37/48 (77.1%) T. cati infections, 8/30 (26.7%) T. taeniaeformis infections, and no D. caninum infections. Proglottids were detected on external examination in 19.0% (12/63) of cats with cestodes. Cestodes were present in over half of the cats examined in this study, but the majority of these infections were not evident by the detection of external proglottids or recovery of characteristic stages on fecal flotation.
Introduction
Helminth infections are common in cats, but fecal flotation underestimates their prevalence, and contemporary surveys documenting the presence of helminths by the most accurate method, direct recovery at necropsy examination, are lacking. Historic necropsy surveys report 46.2 to 55.7% of cats harbor T. cati, 22 to 33% are infected with Taenia spp., and 10 to 13% have Dipylidium caninum.1,2 However, when surveys are conducted by fecal flotation alone, prevalence drops to 21 to 36.2% for T. cati, 3.9 to 5.3% for Taenia spp., and 0.1 to 1.1% for D. caninum. 1,3 Evaluating animals by fecal flotation alone underestimates the prevalence of cestode infections for two reasons: (1) cestode eggs are shed in packets rather than evenly distributed in the fecal mass; and (2) the eggs are dense and, thus, less likely to float in the specific gravity of standard flotation solutions.4,5 Nonetheless, some surveys conducted by fecal float alone detected cestodes in fecal samples from up to 5.7% of pet cats tested, suggesting a high prevalence of infection.6 More recent surveys, however, have failed to document a significant number of cestode infections in pet cats by fecal flotation despite the fact that clients commonly report finding proglottids to veterinarians.7,8
Cats acquire infection with gastrointestinal helminths via ingestion of immature stages, often through predation. For example, infection with T. cati may occur by predation of paratenic hosts harboring larvae in their tissues, although direct ingestion of infective eggs from a contaminated environment is also a potential route of infection. Ancylostoma tubaeforme is transmitted by ingestion of larvae, either directly or in paratenic host tissues, or, rarely, through skin penetration. Cestodes require an intermediate host. Cats become infected with D. caninum upon ingestion of cysticercoids within fleas during grooming, whereas infection with Taenia taeniaeformis occurs following ingestion of strobilocerci when preying on infected rodent intermediate hosts.9,10
Toxocara cati infections are associated with ill-thrift, abdominal distension, and diarrhea in cats, and create a zoonotic risk.11,12 Cats that ingest larvated eggs develop pulmonary lesions, including eosinophilic endarteritis and medial hypertrophy of the pulmonary arterioles, as larvae migrate through the lungs, although the clinical significance of these changes is not well understood.13,14 Feline infection with A. tubaeforme has been associated with blood loss, anemia, diarrhea, and weight loss.15 In contrast, most adult cestode infections are considered nonpathogenic in cats, although the aesthetic concerns associated with these infections, particularly the presence of motile proglottids in the home environment, may cause emotional distress to the client.9 Dipylidium caninum is potentially zoonotic, with infection usually occurring in children following ingestion of an infected flea.16 Human infection with both adult and larval T. taeniaeformis has also been reported.17,18 Some cestodes, such as Spirometra sp., are known to induce gastrointestinal illness in cats, and the literature contains occasional reports of clinical disease in cats associated with Taenia sp.19,20
To determine the degree to which currently available and widely used fecal diagnostic assays may fail to identify helminth infections in cats, we evaluated randomly selected cats from an animal shelter in northeastern Oklahoma for helminth infections and compared the results of diagnostic testing to documented presence of infection by direct examination at necropsy.
Materials and Methods
Sample Collection
All data were collected via examination of carcasses from adult cats euthanized as part of standard operating procedure at an animal shelter in northeastern Oklahoma over a 12 mo period from 2010 to 2011. All cats included in this study were slated for euthanasia according to standard shelter protocols prior to inclusion of carcasses for examination in the study, and the study's objectives and design were approved by shelter administration. Post-mortem physical examination was performed on each carcass, and estimated age, sex, neuter status, and body condition score recorded. An external parasite examination was performed via use of thumb counts as previously described.21 Fleas collected were placed in 70% ethanol for later identification by comparison to standard keys and proglottids were placed on slides for microscopic examination and identification by embryo morphology.22,23 The entire gastrointestinal tract was collected and examined grossly from the gastroesophageal sphincter to the distal colon. All gastrointestinal helminths present were collected and either fixed in 10% formalin or rinsed in phosphate-buffered saline and placed in Beltsville fixative for later identification.24 All fecal material in the colon was collected for flotation analysis. Sections of the right caudal lung lobe of each cat and intestinal sections from a subset of cats (n = 20) were placed in 10% buffered formalin for histologic examination.
Identification and Enumeration of Helminths
Helminths were examined microscopically, identified using standard keys, and enumerated.25,26 Because cestodes break during handling, only individual scolices were included in the enumeration.
Fecal Flotation
Replicate fecal samples (4 g) from each cat were examined for helminth eggs/embryos by both passive flotation using sodium nitrate solutiona in a commercial kit according to manufacturer's instructions and by centrifugation as previously described.23 Briefly, for passive flotation, feces were mixed with a commercial sodium nitrate solution, allowed to sit for 15 min, and then a coverslip used to transfer the surface of the flotation to a slide for examination. For centrifugal flotation, feces were mixed with Sheather's sugar solution in a small disposable cup, the mixture strained using a 3-in2 gauze into a second cup, the fecal suspension transferred to a 15 mL centrifuge tube creating a slight positive meniscus, and a cover slip placed on top. The tubes were spun at 500 G for 10 min, the coverslip was removed, and it was placed on a slide for examination. For both methods, the entire area under the coverslip was systematically examined with a standard compound microscope using the 10x objective (100x magnification), and all parasite stages present recorded.
Histologic Examination of Tissues
Formalin-fixed sections of right caudal lung lobe from each cat and intestinal sections from a subset of cats (n = 20) were processed through graded alcohols and xylene and then embedded in paraffin. Four micrometer sections were stained with hematoxylin and eosin and examined microscopically. Sections were examined by a pathologist blind to the infection status of each cat. For lung sections, the degree of medial hypertrophy of the pulmonary vessels, which is associated with nematode migration in the lungs, was ranked (0 to 3) as absent, mild, moderate, or severe.
Data Analysis
Infection with each helminth species identified was compared to age, sex, neuter status, body condition score, proglottid recovery on external examination (if appropriate), presence of flea infestation, presence of other helminths, and presence of lung lesions using Chi-square tests with significance assigned at P < .05. Intensity of infection with T. taeniaeformis was compared to egg recovery on fecal flotation using a Mann-Whitney rank sum test with significance assigned at P < .05.27
Results
Cats (n = 116; 57 male and 59 female) included in this study were estimated by dentition and physical examination to be from 1–12 yr of age (mean = 2.7 yr) with an average body condition score of 4.7/9. The majority (78.4%) of cats were intact. Evidence of flea infestation was identified on 85/116 cats (73.3%); all fleas recovered were Ctenocephalides felis.
Helminths were identified in 78/116 (67.2%) cats (Table 1), including Toxocara cati (41.4%), Ancylostoma tubaeforme (6.9%), Dipylidium caninum (34.5%), and Taenia taeniaeformis (25.9%). A triradiate specimen of T. taeniaeformis with a scolex bearing a single rostellum and six suckers was recovered from one cat. Intensity of infection ranged from a single adult T. taeniaeformis or D. caninum to as many as 56 T. taeniaeformis and 63 D. caninum (Table 1). Seven cats harbored both D. caninum and T. taeniaeformis, and a single tetrathyridia of Mesocestoides sp. was recovered from one cat (Table 1). Gross lesions coincident with the presence of cestodes, including gross distension of the small intestine, thickening of the intestinal wall, mucosal hemorrhage, and/or ulceration, were identified in some cats with high numbers of either T. taeniaeformis or D. caninum. In a subset of cats (n = 20) from which intestinal sections were examined, histologic lesions suggestive of parasitic enteritis (i.e., significant eosinophils) were not consistently identified in cats with cestodes.
Passive and centrifugal fecal flotation identified 68.8 and 77.1% (33/48 and 37/48) T. cati infections, respectively. Passive and centrifugal fecal flotation identified 2/8 (25%) and 8/8 (100%) A. tubaeforme infections, respectively. Examination for proglottids identified 12/63 (19.0%) cestode infections. Passive and centrifugal fecal flotation using sugar solution identified 3/63 (4.8%) and 8/63 (12.7%) cestode infections, respectively, all of which were consistent with Taenia spp. (Table 2). No D. caninum infections were identified by either fecal flotation method in these cats.
The prevalence of helminths did not vary with age (χ2 = 1.02, df = 1, P = .31), sex (χ2 = 0.83, df = 1, P = .36), neuter status (χ2 = 1.36, df = 1, P = .24), or body condition score (χ2 = <0.001, df = 1, P = .99). Although the median intensity of infection was higher in cats identified as infected with T. taeniaeformis on fecal float (median of 11.0 cestodes) than in cats in which infections were not identified by fecal float (median of 3.0 cestodes), the difference was not significant (T = 163,5, df = 2, P = .07).
The majority of cats with D. caninum had evidence of flea infestation (82.5%). However, the prevalence of C. felis infestation in cats with D. caninum (82.5%) was not significantly greater than that in cats without D. caninum (17.5%; χ2 = 2.65, df = 1, P = .10); seven cats without evidence of fleas on external examination had D. caninum (Table 2). Taenia taeniaeformis was significantly more common in cats infected with Toxocara cati (66.7%; χ2 = 10.67, df = 1, P = .001). The presence of T. cati did not vary with the presence of D. caninum (52.5%; χ2 = 3.11, df = 1, P = .077). Lung lesions characteristic of nematode migration with severity scores of 1–3 were identified in 50/116 (43.1%) cats, but the presence of these lesions did not vary with the presence of T. cati in the small intestine at the time of examination (χ2 = .77, df = 1, P = .37).
Discussion
Over two-thirds of the cats examined in this study harbored helminths. Toxocara cati was the most common helminth found and was present in greater than 40% of the cats examined. While most (77%) of these T. cati infections would have been detected by centrifugal fecal flotation, infections in 11 of the cats would not have been identified clinically, presumably because worms were too immature or too few to allow for detection of eggs. Lesions typically associated with nematode migration in the lungs were also common in the cats in the present study, but were not significantly associated with the presence of ascarids in the small intestine at the time of examination. Infection with Dirofiliaria immitis or Aelurostrongylus abstrusus, which can cause similar lung lesions, was not detected in any cat by antigen testing, necropsy examination of the pulmonary arteries, or histologic examination of lung tissues (data not shown). Cats with lung lesions but no evidence of corresponding nematode infection may have cleared the parasites prior to examination. However, infection of cats through predation, which allows ingestion of larvae in paratenic hosts, does not result in lung migration of T. cati.10,28 We suspect that many of the cats in the present study were infected with T. cati via predation and, therefore, did not have associated lung lesions, a conclusion supported by the fact that T. cati infection and T. taeniaeformis infection, which requires predation, were associated.
In addition, over half the cats examined had cestodes, with D. caninum the most common species found, followed closely by T. taeniaeformis. This high prevalence is consistent with other reported surveys. Indeed, D. caninum is considered the most common tapeworm of cats throughout much of the world and surveys place D. caninum prevalence in adult cats between 10 and 24%.28–31 Prevalence of T. taeniaeformis in previous studies is similarly high, including in cats from the United States (33%) and Belgium (28%).1,32 Our prevalences for D. caninum and Taenia sp. in the present study are high (34.5 and 25.9%, respectively), a finding that may be due to the nature of the study population.
Surveys in the United States conducted by fecal examination by flotation or for evidence of proglottids reveal a lower cestode prevalence of 1.1 to 4%, a difference that is due to the poor sensitivity of these techniques.3,33,34 For the majority of infected cats in the present study, the cestode infections were not identified by any ante mortem technique used (Table 2). The limitations of available diagnostic tests for cestode infection are well recognized, but the data in the present study reveal the extent to which these limitations can influence reaching an accurate diagnosis in an individual cat.1,9 Although owned cats presenting to a veterinarian may have a lower average risk of infection, these same limitations in diagnostic sensitivity would be expected. Proglottid identification or the recovery of embryos on fecal flotation positively identified infection in 18 of 63 (28.6%) cats with tapeworms in the present study, but had we relied on these techniques alone, the majority of infected cats examined would have remained undiagnosed and, unless treated with a broad spectrum anthelmintic containing praziquantel, would have gone untreated for cestode infection.
Adult cestodes are usually considered to be of low pathogenic potential and thought to cause little, if any, clinical disease in companion animals.27 However, there are case reports of intestinal obstruction due to Taenia spp. in both cats and people, and D. caninum has been associated with seizures and other neurologic signs.20,35,36,37 In other host species, such as horses with Anoplocephala perfoliata, case-controlled studies in recent years have revealed a link between the presence of adult cestodes and clinically significant intestinal disease.38,39 Surprisingly, cats in the present study were found to have gross intestinal lesions at necropsy apparently coincident with the presence of cestodes that included distension of the small intestine, thickening of the wall, hemorrhage, and ulceration. The presence of multiple attachment sites in the mucosa of the small intestine of cats harboring a single worm suggests adult T. taeniaeformis may occasionally detach and reattach.28 Although consistent histological changes were not identified in the subset of cats from which tissues were examined, these observations suggest that the dogma that tapeworm infections do not cause significant pathology should perhaps be revisited through careful experimental study. Disease would likely occur more commonly with high numbers of cestodes. A total of five cats in the present study had over 35 adult T. taeniaeformis, and the cestode mass in one cat, an approximately 1 yr old intact female, weighed 34.4 g, or 1.5% of the cat's body weight (data not shown). Intestinal obstruction has been reported in a cat with >30 T. taeniaeformis recovered surgically.20
Because D. caninum is transmitted primarily by Ctenocephalides felis, we expected to see an association between flea infestation and presence of this cestode, but we did not (P = .103). The high prevalence of cats with evidence of active flea infestation (73.3%), as indicated by presence of fleas, flea dirt, or significant alopecia characteristic of flea allergy, may have masked our ability to detect any association. Of 40 cats with D. caninum, 33 (82.5%) had evidence of flea infestation, compared to 68.4% (52/76) of the cats that did not have D. caninum. Moreover, a total of seven cats without any evidence of fleas at the time of examination were infected with D. caninum, suggesting the infestation had resolved prior to examination, was not detected on examination, or that the cats were infected through another route, such as ingestion of prey species infested with C. felis or other arthropods infected with D. caninum cysticercoids. Larvae of other fleas (C. canis, Pulex irritans) and the biting louse (Trichodectes canis) are potential intermediate hosts of D. caninum.28 Data from the present study suggest that absence of fleas at a single examination should not be interpreted as precluding the presence of D. caninum.
Conclusion
The data from the present study demonstrate that ascarids and cestodes remain common parasites of cats. Unfortunately, currently available diagnostic tests are unlikely to reveal all of these infections in practice. Performing multiple fecal flotation assays on an individual cat may improve sensitivity of this assay for ascarids, but would not be expected to improve detection of cestodes. Time spent outdoors and access to prey species increase the risk of infection with both ascarids and taeniid tapeworms and may also increase the risk of flea infestation, which can lead to infection with D.caninum. Feline ascarids can cause gastrointestinal disease and lung lesions in cats and pose a zoonotic risk. While the clinical significance of cestodes to the health of a cat, if any, remains unclear, infected cats provide a reservoir of infection in the environment that supports the maintenance of these low-risk zoonoses. In addition, motile proglottids emerging in and around the cat may cause psychological distress to clients, threatening the human–animal bond. Until better methods for identifying helminths become available, veterinarians should consider the potential for infection in cats, particularly cestodes in cats with outdoor access or a past or current history of flea infestation, and treat with appropriate compounds when historical information suggests infection is likely.
Contributor Notes
