Abstract
Over a 3.5-year period, fecal samples from 1322 cats from two shelters and affiliated foster homes in upstate New York were processed for parasite detection by both 1.18 spg zinc sulfate and 1.3 spg sugar double centrifugal flotation. In 50.9% of the samples at least one parasite was detected. Overall, 18 different parasites ranging in prevalence from 0.2% to 21% were recovered. The most prevalent parasites of foster and shelter cats in this study were Cystoisospora species and Toxocara cati (21% prevalence, each). In order of percentage of positive samples, other findings were: Giardia species (8.9%), Aelurostrongylus abstrusus (6.2%), taeniid eggs (3.9%), Cryptosporidium species (3.8%), Aonchotheca species (3.7%), Eucoleus species (2.3%), Ancylostoma species (2.2%), Cheyletiella species (2.0%), Dipylidium caninum (1.1%), Otodectes species, Toxoplasma-like oocysts and Sarcocystis species (0.8% each), Demodex and Spirometra species (0.4% each), and Alaria species and Felicola subrostratus (0.2% each).
Over a 3.5-year period (August 2006–January 2010), a total of 1629 feline fecal samples from two shelters and affiliated foster homes in Cortland and Tompkins counties in the state of New York were submitted as teaching material for parasite detection to the Community Practice Service (CPS) clinical rotation. Third and fourth year veterinary students at Cornell University's Veterinary College processed these samples as part of a clinical diagnostic parasitology course. These samples corresponded to 1322 individual cats. Of these, 307 samples represented resubmissions, ie, for these cats more than one fecal sample was examined. Shelters housed 1272 of these cats, while the remaining 50 were in foster care. No information on source of cat prior to arrival, age, gender, housing (ie, whether singly or in groups), history of parasite control products used (if any), length animals had been in custody, or signs of disease, is submitted along with the fecal samples, but both apparently-healthy and ill cats can shed parasites in their feces. 1,2 Collected samples were stored at 4°C and processed within 5 days of collection. All samples were processed by both 1.18 spg zinc sulfate and 1.3 spg sugar double centrifugal flotation. 3 Slides were examined under 100× or 400× magnification using bright field microscopy. Parasites were identified based on morphology alone, thus, in many instances identification beyond the genus level may not always be accurate. All samples were processed under the supervision of the principal author; all samples were examined by the principal author.
In just over half the samples (50.9%) at least one parasite was detected. Eighteen different parasites ranging in prevalence from 0.2 to 21% were noted (Table 1). The most prevalent parasites of foster and shelter cats in this study were Cystoisospora species and Toxocara cati (each had a prevalence of 21%). This trend seems to be consistent with the findings of other surveys (Table 1). 4–23 As individual Cystoisospora species are not always recorded on our forms, and mixed infections of Cystoisospora species are often present, these infections are grouped in our data. Giardia species cysts were detected in 8.9% of all fecal samples. The cat lungworm, Aelurostrongylus abstrusus, was present in 6.2% of samples examined. When taken together, the next most prevalent parasites were the capillarids (2.3% of samples contained Eucoleus species and 3.7% contained Aonchotheca species; mixed infections are common); Eucoleus aerophilus can cause coughing and wheezing due to bronchiolar disease and Aonchotheca putorii has been reported as a cause of gastritis in cats in Europe. 24 The remaining parasites were each found in less than 4% of samples: taeniids (3.9%), Cryptosporidium species (3.8%), Ancylostoma species (2.2%), Cheyletiella species (2.0%), Dipylidium caninum (1.1%), Otodectes species, Toxoplasma gondii, and Sarcocystis species (0.8% each), Demodex and Spirometra species (0.4% each), and Alaria species and Felicola subrostratus (0.2% each). Oocysts of size and shape consistent with T gondii were recorded as ‘T gondii’, although by microscopic examination alone, they cannot be differentiated from Hammondia or Besnotia species. While the techniques used in this study cannot determine Giardia species assemblages or Cryptosporidium species, the authors believe Giardia intestinalis assemblage F and Cryptosporidium felis are most likely; neither of which are considered to be a major source of zoonotic infections. 25–27
Table 1.
Region | Year | N | Source of animals | Percent parasite prevalence (%) | Notes | Method (spg of solution, if given) | Reference | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Cystoisospora species | Cryptosporidium species | Giardia species | Sarcocystis species | Toxoplasma species-like | Aelurostrongylus species | Toxascaris leonina | Toxocara cati | Hookworms | ‘Capillarids’ | Ollulanus tricuspis | Dipylidium species | Taeniids | Alaria species | |||||||
Northeast | ||||||||||||||||||||
NY | 2006–2009 | 1322 | (SH)(F) | 21.0 | 3.8 | 8.9 | 0.8 | 0.8 | 6.2 | — | 21.0 | 2.2 | 3.7 Ap 2.3 Ea | — | 1.1 | 3.9 | 0.2 | Spirometra also detected (0.4%) | ZS (1.18) and S (1.3); CF | Present study |
NY | 2001 | 263 | (SH)(O), <1 year old | — | 3.8 | 7.2 | — | 1.1 | — | — | 32.7 | — | — | — | — | — | — | ZS (1.18) and S (1.3); CF | Spain 2001 4 | |
NY | 1971 | 132 | (SH) | — | — | — | — | — | — | — | 75.0 | — | — | — | — | 13.0 | — | Necropsy | Styles 1971 5 | |
PA | 2009 | 1566 | (H) | 37.0 Cf; 1.2 Cr | — | 2.3 | — | — | — | 0.1 | 7.5 | 0.5 | — | 0.1 | 0.8 | 0.3 | — | Proglottids, ZS (?); CF; sometimes EAS | Gates and Nolan 2009 6 | |
CT | 2003 | 450 | (ST)(O) | — | — | — | — | 0.7 | 0.2 | — | 39.8 | 0.4 | — | — | 4.7 | — | — | Ovassay; ZS; SF | Rembiesa 2003 7 | |
NJ | 1970 | 757 | (ST) | 36.0 | — | 2.5 | — | — | * | — | * | * | *Ea | * | * | * | * | (*) other recovered nematodes and trematodes | ZS (1.2) SF, PAF sedimentation; necropsy | Burrows 1970 8 |
NJ | 1967 | 1480 | (ST) | — | — | — | — | — | 1.1 | — | 36.2 | 34.2 | 9.0 | 0.2 | 0.1 | 5.3 | — | Trichuris 0.2% | ZS (1.2); F | Lillis 1967 9 |
NJ | 1955 | 300 | (ST) | — | — | — | — | — | — | 10.0 | 42.0 | 19.0 | — | — | 32.3 | 14.3 | — | Necropsy; NaCl (1.25); CF | Mann 1955 10 | |
NJ | 1952 | 100 | (V) | 7.0* | — | — | — | — | — | 5.0 | 50.0 | 17.0 | — | — | 19.0 | 8.0 | — | *‘Coccidia’ | Necropsy; NaCl (1.25) CF | Mann 1952 11 |
Midwest | ||||||||||||||||||||
IA | 1983* | 60 | (SH)(O) | — | — | — | — | — | — | — | — | — | 18.3 A.p | — | — | — | — | * Aonchotheca survey | Necropsy | Greeve 1983 12 |
IA | 1978 | 11,995 | (O) | — | — | — | — | — | — | * | * | 1.7 | — | — | — | — | — | (*) 3.2% ‘Ascarids’ | ‘Fecal examination’ | Lightner 1978 13 |
IL | 1977 | 217 | (R)(SH)(O) | 23.0 Cf; 24.0 Cr | — | — | — | 1.0 | — | 32.0 | 6.0 | 9.0 | 4.0 | — | — | — | — | S (?); F | Guterbock 1977 14 | |
IL | 1948 | 51 | (SH) | — | — | — | — | — | — | — | 37.3 | 5.9 | — | — | 39.2 | 3.9 | — | Trichinella 21.6% | Necropsy | Cross 1948 15 |
IL KY | 1971 | 100 | (LD) | — | — | — | — | — | — | 12.0 | 26.0 | 45.0 | — | — | 14.0 | 16.0 | — | Physaloptera species 5%, Amphimerus pseudofelineus 1% | Necropsy | Power 1971 16 |
MI | 1953 | 147 | (UK), 6-12 wks old | 89.0 | — | 5.0 | — | — | — | 1.0 | 67.0 | 8.0 | 1.4 Ea | — | 1.0 | 0.5 | — | Trichomonas 1%; Physaloptera 1% | Necropsy | Hitchcock 1953 17 |
MO | 1978 | 1294 | (O) | 67.0 | — | — | — | — | — | — | — | 6.4 | 2.6* | — | * | * | — | (*) 24.4% ‘Ascarids’; 5.2% ‘tapeworm’. ‘Capillarids’ or Trichuris species | MS (1.25); (unspecified method) | Visco 1978 18 |
OH | 1976 | 1000 | (SH) | 94.0 | — | — | 0.2 | 1.0 | — | — | 25.0 | 9.6 | 1.3 | — | * | * | — | (*) 0.5% ‘tapeworm’ | S (1.15); CF | Christie 1976 19 |
WI | 1980 | 23 | (SH) | — | — | — | — | — | — | 13 | 43.5 | 4.4 | — | — | 21.7 | 21.7 | — | Necropsy | Amin 1980 20 | |
West | ||||||||||||||||||||
CA | 2007 | 344 | (SH) | 52.0 | 4.7 | 9.9 | — | — | — | — | 19.0 | 1.0 | — | — | 2.0 | 2.0 | — | Strongyloides stercoralis 1% | ZS (?); CF; DIF and EIA Cryptosporidium and Giardia | Mekaru 2007 2 |
CO | 2000 | 206 | (SH)(O) | — | 5.4 | 2.4 | — | — | — | — | 3.9 | — | — | — | — | — | — | ZS (?); CF | Hill 2000 1 | |
UT | 1977 | 100 | (ST) | 10.0 | — | — | — | — | — | — | 43.0 | — | — | — | 1.0 | 10.0 | — | Physaloptera species 2% | Necropsy examination; S; F | Sawyer 1977 21 |
South | ||||||||||||||||||||
MS | 2006 | 250 | (SH)(O) | — | — | 13.3 | — | — | — | — | — | — | — | — | — | — | — | * Giardia study | S (1.13); CF and IFA | Vasilopulos 2006 22 |
TN | 1956 | 12 | (SH)(ST) | — | — | — | — | — | — | * | * | 34.0 | — | — | 8.0 | 17.0 | — | (*) 50% ‘Ascarids’ | Necropsy | Ciordia 1956 23 |
(*)=notes in note column (—)=parasite not reported. SH=shelter cats; F=foster cats; H=veterinary hospital patients; ST=stray cats; O=owned cats; R=research cats; V=‘various’; LD=‘local dealer’; U=‘unknown’. Cf=Cystoisospora felis; Cr= Cystoisospora rivolta-like; Ap= Aonchotheca putorii; Ea= Eucoleus aerophilus. ZS=ZnSO4; S=sugar/sucrose; CF=centrifugal flotation; EAS=ethyl acetate sedimentation; SF=standing flotation; PAF=phenol–alcohol–formaldehyde; F=unspecified flotation; MS=MgSO4; DIF=direct immunofluorescence; EIA=enzyme immunoassay; IFA=indirect fluorescent antibody.
Prevalence determination based solely on fecal examination is likely to underestimate the true prevalence of infection in the population. Animals may have non-patent or latent infections that cannot be detected by the methods employed here, or animals may have been treated with anti-parasitic drugs prior to sample submission. In addition, tapeworm infections are more readily diagnosed by observing segments (as was sometimes the case with these samples) rather than by egg recovery in fecal flotation. Likewise, fecal flotation is not the method of choice for detection of fluke infections or ectoparasite infestations. Detection of larvae can be accomplished by the methods used here, as evidenced by the recovery of A abstrusus larvae in 6.2% of samples; however, Baermann sedimentations of all samples may have increased our ability to detect infections with this parasite.
The methods used here are considered by many, including the authors, to be the gold standard for routine fecal diagnostic testing for parasites. 28–31 The results obtained are generally within the range of those previously reported in other surveys (Table 1). There appears to be only one other survey 19 reporting the prevalence of Sarcocystis species in cats; our prevalence was four times greater than that reported by Christie et al. 19 The prevalence of T gondii-like oocysts in fecal samples in our study (0.8%), falls in the range of what is to be expected; it is believed at any point in time only about 1% of cats are shedding oocysts of this type. This is reflected by the data from other surveys as well (Table 1).
With regards to helminth infections, only two other surveys have reported Aelurostrongylus species prevalence in fecal samples 7,9 ; these studies found a prevalence of 0.2% and 1.1%. The 6.2% prevalence found in our survey is quite a bit higher, even though, as mentioned above, this is still expected to be an underestimate of the true prevalence. It may be that the previous studies used standing flotation procedures, which are known to generally have poorer parasite recoveries, 30,31 or the discrepancy may be due to seasonal or geographical differences. Toxascaris leonina was not reported in any of the three surveys conducted in New York State (including this one). The highest prevalence of T cati, hookworms, capillarids, Dipylidium species and taeniids has been reported in surveys that have included necropsy examinations, as would be expected (Table 1). This survey is the only survey reporting the prevalence of Spirometra (0.4%) and Alaria species (0.2%).
Many of the parasites detected in these cats are acquired through predation, (eg, Cystoisospora, Toxoplasma, Toxocara, Ancylostoma, Aelurostrongylus, Taenia species, etc). Cats of any age with access to prey species can be infected, including owned cats that have access to the outdoors and those in homes that have the potential for visits from mice, vole or other transport hosts. The findings of this study support the recommendation that all pets, even those under regular veterinary care, should have at least one annual fecal examination and should be placed on year-round prevention for internal and external parasites.
References
- 1.Hill S.L., Cheney J.M., Taton-Allen G.F., Reif J.S., Bruns C., Lappin M.R. Prevalence of enteric zoonotic organisms in cats, J Am Vet Med Assoc 216, 2000, 687–692. [DOI] [PubMed] [Google Scholar]
- 2.Mekaru S.R., Marks S.L., Felley L.J., Chouicha N., Kass P.H. Comparison of direct immunofluorescence, immunoassays, and fecal flotation for detection of Cryptosporidium spp and Giardia spp in naturally exposed cats in 4 Northern California animal shelters, J Vet Intern Med 21, 2007, 959–965. [DOI] [PubMed] [Google Scholar]
- 3.Bowman D.D. Diagnostic parasitology. Bowman D.D. Georgi's parasitology for veterinarians, 9th edn, 2009, Elsevier: St Louis, 295–371. [Google Scholar]
- 4.Spain C.V., Scarlett J.M., Wade S.E., McDonough P. Prevalence of enteric zoonotic agents in cats less than 1 year old in Central New York State, J Vet Intern Med 15, 2001, 33–38. [DOI] [PubMed] [Google Scholar]
- 5.Styles T.J., Evans D.S. Intestinal parasites of dogs and cats in Schenectady County, NYS J Med 71, 1971, 2755–2757. [PubMed] [Google Scholar]
- 6.Gates M.C., Nolan T.J. Endoparasite prevalence and recurrence across different age groups of dogs and cats, Vet Parasitol 166, 2009, 153–158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Rembiesa C., Richardson D.J. Helminth parasites of the house cat, Felis catus, in Connecticut, USA, Comp Parasitol 70, 2003, 115–119. [Google Scholar]
- 8.Burrows R.B., Hunt G.R. Intestinal protozoan infections in cats, J Am Vet Med Assoc 157, 1970, 2065–2067. [PubMed] [Google Scholar]
- 9.Lillis W.G. Helminth survey of dogs and cats in New Jersey, J Parasitol 53, 1967, 1082–1084. [PubMed] [Google Scholar]
- 10.Mann P.H. Additional information pertaining to the incidence of heartworms and intestinal helminths in stray cats and dogs in Bergen County, northern New Jersey, J Parasitol 41, 1955, 637. [Google Scholar]
- 11.Mann P.H., Fratta I. The incidence of coccidia, heartworms, and intestinal helminths in dogs and cats in northern New Jersey, J Parasitol 38, 1952, 496–497. [Google Scholar]
- 12.Greeve J.H., Kung F.Y. Capillaria putorii in domestic cats in Iowa, J Am Vet Med Assoc 182, 1983, 511–513. [PubMed] [Google Scholar]
- 13.Lightner L., Christensen B.M., Beran G.W. Epidemiologic findings on canine and feline intestinal nematode infections from records of the Iowa State University Veterinary Clinic, J Am Vet Med Assoc 172, 1978, 564–567. [PubMed] [Google Scholar]
- 14.Guterbock W.M., Levine N.D. Coccidia and intestinal nematodes of east central Illinois cats, J Am Vet Med Assoc 170, 1977, 1411–1413. [PubMed] [Google Scholar]
- 15.Cross S.X., Allen R.W. Incidence of intestinal helminths and trichinae in dogs and cats in Chicago, N Am Vet 29, 1948, 27–30. [PubMed] [Google Scholar]
- 16.Power L.A. Helminths of cats from the midwest with a report of Ancylostoma caninum in this host, J Parasitol 57, 1971, 610. [PubMed] [Google Scholar]
- 17.Hitchcock D.J. Incidence of gastro-intestinal parasites in some Michigan kittens, N Am Vet 34, 1953, 428–429. [Google Scholar]
- 18.Visco R.J., Corwin R.M., Selby L.A. Effect of age and sex on the prevalence of intestinal parasitism in cats, J Am Vet Med Assoc 172, 1978, 797–800. [PubMed] [Google Scholar]
- 19.Christie E., Dubey J.P., Pappas P.W. Prevalence of Sarcocystis infection and other intestinal parasitisms in cats from a humane shelter in Ohio, J Am Vet Med Assoc 168, 1976, 421–422. [PubMed] [Google Scholar]
- 20.Amin O.M. Helminth and arthropod parasites of some domestic animals in Wisconsin, T Wisc Acad Sci 68, 1980, 106–110. [Google Scholar]
- 21.Sawyer T.W., Cowgill L.M., Andersen F.L. Helminth parasites of cats and dogs from central Utah, Great Basin Nat 36, 1976, 471–474. [Google Scholar]
- 22.Vasilopulos R.J., Mackin A.J., Rickard L.G., Pharr G.T., Huston C.L. Prevalence and factors associated with fecal shedding of Giardia spp in domestic cats, J Am Anim Hosp Assoc 42, 2006, 424–429. [DOI] [PubMed] [Google Scholar]
- 23.Ciordia H., Jones A.W. The incidence of intestinal helminths in dogs and cats in Knoxville, Tennessee, J Am Vet Med Assoc 128, 1956, 139. [PubMed] [Google Scholar]
- 24.Bowman D.D., Hendrix C.M., Lindsay D.S., Barr S.C. The nematodes, Adenophorea, Feline clinical parasitology, 2002, Iowa State University Press: Ames, IA, 338–354. [Google Scholar]
- 25.Ballweber L.R., Xiao L.H., Bowman D.D., Kahn G., Cama V.A. Giardiasis in dogs and cats: update on epidemiology and public health significance, Trends Parasitol 26, 2010, 180–189. [DOI] [PubMed] [Google Scholar]
- 26.Bowman D.D., Lucio-Forster A. Cryptosporidiosis and giardiasis in dogs and cats: veterinary and public health importance, Exp Parasitol 124, 2010, 121–127. [DOI] [PubMed] [Google Scholar]
- 27.Lucio-Forster A., Griffiths J.K., Cama V.A., Xiao L.H., Bowman D.D. Minimal zoonotic risk of cryptosporidiosis from pet dogs and cats, Trends Parasitol 26, 2010, 174–179. [DOI] [PubMed] [Google Scholar]
- 28.Blagburn B.L., Butler J.M. Optimize intestinal parasite detection with centrifugal fecal flotation, Vet Med 101, 2006, 455–463. [Google Scholar]
- 29.Blagburn B.L. Why fecal centrifugation is better, Vet Med, (Suppl S), 2008, 8–9.
- 30.Dryden M.W., Payne P.A., Ridley R., Smith V. Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts, Vet Ther 6, 2005, 15–28. [PubMed] [Google Scholar]
- 31.Zajac A.M., Johnson J., King S.E. Evaluation of the importance of centrifugation as a component of zinc sulfate fecal flotation examinations, J Am Anim Hosp Assoc 38, 2002, 221–224. [DOI] [PubMed] [Google Scholar]