Prevalence and risk factors for Giardia and coccidia species of pet cats in 2003–2004

Abstract

Prevalence and risk factors for feline coccidia and Giardia species infections were estimated for cats visiting 434 Banfield hospitals in 40 states in 2003–2004. Evaluated were 631,021 cats making 1,456,712 office visits (encounters) and having 211,105 fecal examinations. The overall fecal prevalences of coccidia and Giardia species were 1.4% and 0.58%, respectively. Cats at increased risk of coccidia infection were under 4 years of age, intact, and seen during the summer, fall, and spring months compared to winter. Cats at increased risk of Giardia species infection were under 4 years of age. Those at decreased risk were mixed breed and seen during the summer, fall, and spring. The highest regional risk of coccidia and Giardia species infection was for cats in the East South Central region and Mountain region, respectively, compared to the South Pacific region.

Intestinal protozoal parasites such as Giardia species and coccidians including Isospora species, Toxoplasma gondii, Hammondia species, Besnoitia species, Sarcocystis species, and Cryptosporidium species, may cause clinical and subclinical infection in cats of all ages (Kirkpatrick 1986, Barr and Bowman 1994, Lappin et al 1997, Bowman, 1999). Giardia species infection in cats occurs worldwide with prevalence varying from 1.2% to 14% (Bemrick 1961, Kirkpatrick 1986, Swan and Thompson 1986, Kucharova 1989, Kirkpatrick 1990, Tonks et al 1991). Transmission occurs by the fecal–oral route or through contaminated fomites (Bowman et al 2002). Infection may result in malabsorptive diarrhea, weight loss, and reduced growth rate particularly in kittens (Kirkpatrick 1986, 1990). Transmission of Giardia species between cats and humans remains controversial with reports indicating that genetically identical forms of Giardia species are found in both species (Thompson et al 1988, Warburton et al 1994). By comparison, the clinical presentation of giardiasis in humans ranges from asymptomatic to severe enteritis (Bowman 1999).

Coccidians with zoonotic potential include Toxoplasma gondii and Cryptosporidium parvum. T gondii is found worldwide, infecting essentially all warm-blooded animals that may serve as intermediate or paratenic hosts (Dubey and Lappin 1998, Bowman et al 2002). Cats are the only known definitive host shedding infective oocysts in their feces. Transmission occurs transplacentally and/or by ingestion of oocysts in the feces or bradyzoites in the tissues of paratenic hosts (Dubey and Lappin 1998). Clinical toxoplasmosis in cats may occur in neonates when transplacental infection occurs. Clinical signs in cats are described as pulmonary/pneumonic, neurologic, hepatic, pancreatic, cardiac, and ocular (Dubey and Carpenter 1993). However, most infected cats remain asymptomatic. Human infection with Toxoplasma gondii can cause lymphadenopathy and fever in immunocompetent individuals and encephalitis in immunosuppressed persons (Dubey and Lappin 1998, Bowman 1999). Neonatal infections in humans can result in congenital defects or death of the fetus (Bowman 1999).

Cryptosporidium parvum and C felis have a worldwide distribution with an estimated 15% of cats in the United States demonstrating seropositivity (Lappin et al 1997, McReynolds et al 1999). Transmission occurs through ingestion and infected cats may be asymptomatic or present with persistent, water-losing diarrhea and weight loss (Prestwood 1990, Bowman et al 2002). Cryptosporidium is a zoonosis, but the extent to which infection is passed between cats and humans is unknown (Bowman et al 2002). Infection is diagnosed in 4–7% of humans admitted to hospitals with gastroenteritis and it poses a severe threat to immunocompromised individuals (Barr 1998). Isospora felis and I rivolta are also coccidians with a worldwide distribution. Isospora can cause coccidiosis in cats and results in severe infection in kittens. Older kittens may develop chronic diarrhea, but kittens under 4 weeks of age are more likely to have severe enteritis that may result in death (Bowman 1999, Bowman et al 2002). Cats are infected by the oral route, either by ingestion of oocysts or paratenic hosts (Bowman 1999, Bowman et al 2002). Other coccidians such as Hammondia species, Besnoitia species, and Sarcocystis species are considered non-pathogenic in cats (Bowman 1999).

Previous studies of protozoal parasites of cats in the United States have found a fecal prevalence of Giardia species ranging from 2.4% to 7.3% (Kirkpatrick 1988, Nolan and Smith 1995, Hill et al 2000, Spain et al 2001, Nutter et al 2004), coccidia infection from 2.9% to 6.7% (Visco et al 1978, Kirkpatrick 1988, Nolan and Smith 1995), and Cryptosporidium from 2.4% to 5.4% (Lappin et al 1997, Hill et al 2000, Spain et al 2001, Nutter et al 2004). Cats in these studies were typically from humane societies, a mix of humane societies and private veterinary practices, or veterinary teaching hospitals. Thus the sample of cats used in previous studies may not have been representative of the healthy pet cat population. The purpose of the present study was to evaluate the medical records of pet cats seen at Banfield, The Pet Hospital to estimate the prevalence of parasitism with Giardia species and coccidia, especially Isospora species, among cats receiving primary healthcare. Patient medical records were recorded and stored in a standard electronic format, thus facilitating epidemiologic studies and comparison of results in different geographic areas. The present study also utilized these medical records to identify risk factors for Giardia species and coccidia infections in pet cats.

Materials and Methods

Banfield, The Pet Hospital provided Purdue University School of Veterinary Medicine the electronic medical records for all cats seen at their hospitals throughout the United States from 1 January 2003 to 31 December 2004. The medical records were created using proprietary software (PetWare is the proprietary medical records software of Banfield, the Pet Hospital®, Portland OR), that assigns a unique identification number to each patient and encounter (office visit). Information on age, breed, sex, neuter status, hospital location, date of encounter and fecal examination results was extracted from each record. Information on indoor/outdoor status of the patients was unavailable. Fecal samples were obtained by owner submission or by the veterinarian using a fecal loop when necessary. Data on the percent of owner submission versus collection at the veterinary hospitals were unavailable due to the retrospective nature of the study. All fecal samples from 1 January 2003 to 31 December 2004 were incorporated in the study, including normal or diarrheic stools. Fecal examinations were performed using zinc sulfate solution (OvaSol Zinc Sulfate Heptahydrate Fecal Flotation Medium, Vedco, St. Joseph, MO) and a fecal flotation device (Fecalyzer; EVSCO Pharmaceuticals, Buena, NJ) with trained technicians; direct smears were undertaken in conjunction with flotations when requested by the veterinarian. The exact number of samples tested by zinc flotation alone, direct smear alone, or both methods, is unknown as the retrospective nature of the study allowed only a final fecal diagnosis to be obtained. Additional test methods such as Giardia ELISA tests, Cryptosporidium indirect fluorescent antibody test (IFA) or FA, and toxoplasmosis IgG/IgM, were used less frequently at Banfield hospitals than fecal flotations or smears. Therefore, these test results were not included in the present study.

Fecal test prevalence (% positive) was estimated for Giardia species and coccidia infection using the number of positive fecal tests divided by the total number of tests performed, and the results were expressed as the number of positive fecal tests per 1000 tests. Due to the retrospective nature of the study, a diagnosis of coccidia by fecal examination could have included Toxoplasma gondii, Cryptosporidium species, Isospora species, or any other coccidial intestinal parasite. The patient medical records do not distinguish between these parasites. However, the testing method utilized in this study would have been most effective in recovering Isospora species. Giardia species infection was characterized by genus alone with no attempt to identify the species. Prevalence was determined by age, gender, breed, season, and geographic region. Age categories included kitten (0–<6 months), juvenile (6–<12 months), young adult (12 months–<4 years), adult (4–<10 years), and geriatric (10+ years). Season was categorized as winter (December, January, February), spring (March, April, May), summer (June, July, August), and fall (September, October, November). The United States was divided into 10 regions based on a modification of the system used by the Centers for Disease Control and Prevention (CDC) for reporting of human notifiable diseases (Department of Health and Human Services 2005). Fecal prevalence of Giardia species and coccidia infection was mapped using Arc GIS (ESRI ArcMap 9.0, Environmental Systems Research Institute, Redlands, CA) for each of the following regions: North Atlantic, East North Central, West North Central, Mid Atlantic, South Atlantic, East South Central, West South Central, Mountain, North Pacific, and South Pacific (North Atlantic region=ME, NH, VT, MA, RI, CT, NY, NJ, PA, and DE (26 hospitals); East North Central region=OH, IN, IL, MI, and WI (35 hospitals); West North Central region=MN, IA, MO, ND, SD, NE, and KS (31 hospitals); Mid Atlantic region=DC, MD, VA, WV, and NC (47 hospitals); South Atlantic region=SC, GA, and FL (76 hospitals); East South Central region=KY, TN, AL, and MS (18 hospitals); West South Central region=AR, LA, OK, and TX (65 hospitals); Mountain region=MT, ID, WY, CO, NM, AZ, UT, and NV (56 hospitals); North Pacific region=WA, OR, and AK (21 hospitals); South Pacific region=CA, and HI (59 hospitals)).

Cats with fecal positive and fecal negative test results were compared to determine risk factors for Giardia species and coccidia infection separately using multivariate logistic regression (SAS9 ETL Studio, SAS Institute Inc., Cary, NC). Potential risk factors were age, gender, breed, season, and region. Risk was expressed as an odds ratio (OR) with 95% confidence interval. An OR>1.0 denotes an increased risk and a P value of <0.05 is statistically significant.

Results

Descriptive Findings

A total of 1,456,712 encounters for 631,021 cats were evaluated (Table 1). The mean number of encounters per cat over the 2-year period was 2.31; 56.1% of cats had one encounter, 17.4% had two encounters, 8.7% had three encounters, and 17.8% had four or more encounters. Male cats accounted for 49.9% of encounters and females 49.8%; gender was not specified for 0.3% of encounters. Eighty-four percent of the encounters were made by neutered/spayed cats. Cats recorded as mixed breed (domestic longhair, domestic mediumhair, domestic shorthair, or unknown) comprised the majority of the encounters (84.4%) compared to purebred cats (15.6%) represented by over 40 American and European cat breeds. The frequency of cat encounters by season was greater in the summer and fall compared to the winter and spring. Encounters by hospital region ranged from 36,141 (2.5%) in the East South Central to 285,043 (19.6%) in the South Atlantic.

Table 1.

Frequency of all cat encounters and those with fecal examinations at Banfield hospitals in 2003–2004

		Encounters
All		With fecal tests
N	Total encounters (%)	N	Within category (%)
Age*
Kitten (0–<6 months)	325,557	22.3	66,029	20.3
Juvenile (6–<12 months)	97,127	6.7	14,686	15.1
Young adult (12 months–<4 years)	436,794	30.0	66,945	15.3
Adult (4–<10 years)	385,314	26.5	46,812	12.1
Geriatric (10+ years)	211,793	14.5	16,611	7.8
Gender
Male intact	104,445	7.2	12,461	11.9
Female intact	123,467	8.5	15,723	12.7
Male neutered	621,747	42.7	92,040	14.8
Female spayed	602,151	41.3	90,560	15.0
Unknown	4,902	0.34	321	6.5
Breed
Mixed breed	1,230,170	84.4	182,042	14.8
Purebred	226,542	15.6	29,063	12.8
Season
Summer	413,893	28.4	58,487	14.1
Fall	397,156	27.3	56,453	14.2
Winter	313,681	21.5	46,754	14.9
Spring	331,982	22.8	49,411	14.9
Region
North Atlantic	55,157	3.8	7,298	13.2
East North Central	94,242	6.5	15,026	15.9
West North Central	101,248	7.0	16,766	16.6
Mid Atlantic	158,841	10.9	26,694	16.8
South Atlantic	285,043	19.6	50,405	17.7
East South Central	36,141	2.5	5,984	16.6
West South Central	174,464	12.0	26,254	15.0
Mountain	136,777	9.4	16,576	12.1
North Pacific	158,355	10.9	17,230	10.9
South Pacific	256,440	17.6	28,872	11.3
Total	1,456,712	100	211,105	14.5

^*Age missing for 127 encounters.

A fecal examination was recorded for 211,105 encounters (14.5%). Fecal examinations were undertaken more frequently for kittens, juveniles, and young adults than adult and geriatric cats (Table 1). Spayed females and neutered males were more likely to have a fecal test performed than intact cats. Fecal tests were undertaken more frequently for mixed breed cats compared to purebred cats. The prevalence of fecal examinations by season was evenly distributed, ranging from 14.1% in the summer to 14.9% in the spring. Cats in the North Pacific region were least likely to be tested whereas cats in the South Atlantic region were most likely to be tested.

The percent of positive tests for ova of coccidia infection was 1.4% or 14.2 per 1000 fecal tests while for Giardia species it was 0.58% or 5.8 per 1000 fecal tests (Table 2). Kittens had the greatest prevalence of coccidia and Giardia species shedding. Prevalence decreased as age increased for coccidia and for Giardia species, with the exception of a small increase among geriatric cats. Additional analysis was performed to further estimate the prevalence of these parasites in kittens at 2 week age intervals (Figs 1 and 2). Cats 4–6 weeks of age had the greatest prevalence of coccidia whereas a more even distribution was demonstrated for Giardia species. Intact cats were more likely to be shedding either parasite compared to neutered cats of both sexes. Coccidia prevalence was greater in mixed breed cats compared to Giardia species in purebred cats. Cats shedding coccidia had a greater prevalence in the summer compared to the other seasons while cats shedding Giardia species had a greater prevalence in the fall and winter. Coccidia was most prevalent in the East South Central region and least prevalent in the North Pacific (Fig 3) whereas Giardia species was most prevalent in the Mountain region and least prevalent in the North Atlantic and Mid Atlantic regions (Fig 4).

Table 2.

Prevalence of coccidia and Giardia species positive fecal tests for cats visiting Banfield hospitals in 2003 and 2004

	Fecal tests	Coccidia		Giardia
Positive fecal tests	Positives/1000 fecal tests	Positive fecal tests	Positives/1000 fecal tests
Age*
Kitten	66,029	2,596	39.3	614	9.3
Juvenile	14,686	94	6.4	109	7.4
Young adult	66,945	218	3.3	260	3.9
Adult	46,812	67	1.4	156	3.3
Geriatric	16,611	30	1.8	84	5.1
Gender
Male intact	12,461	637	51.1	148	11.9
Female intact	15,723	642	40.8	160	10.2
Male neutered	92,040	906	9.8	468	5.1
Female spayed	90,560	786	8.7	444	4.9
Breed
Mixed breed	182,042	2,673	14.7	997	5.5
Purebred	29,063	333	11.5	226	7.8
Season
Summer	58,487	1,256	21.5	329	5.6
Fall	56,453	929	16.5	351	6.2
Winter	46,754	323	6.9	288	6.2
Spring	49,411	498	10.1	255	5.2
Region
North Atlantic	7,298	144	19.7	7	1.0
East North Central	15,026	132	8.8	24	1.6
West North Central	16,766	222	13.2	159	9.5
Mid Atlantic	26,694	420	15.7	28	1.0
South Atlantic	50,405	767	15.2	170	3.4
East South Central	5,984	186	31.1	40	6.7
West South Central	26,254	591	22.5	157	6.0
Mountain	16,576	182	11.0	544	32.8
North Pacific	17,230	128	7.4	20	1.2
South Pacific	28,872	234	8.1	74	2.6
Total	211,105	3,006	14.2	1,223	5.8

^*Refer to Table 1 for description of age categories.

Fig 1.

Prevalence (95% CI) of coccidia species positive fecal examinations of cats less than 6 months of age at Banfield hospitals in 2003–2004.

Fig 2.

Prevalence (95% CI) of Giardia species positive fecal examinations of cats less than 6 months of age at Banfield hospitals in 2003–2004.

Fig 3.

Coccidia species positive fecal tests for cats seen at Banfield hospitals in the United States by region, 2003–2004.

Fig 4.

Giardia species positive fecal tests for cats seen at Banfield hospitals in the United States by region, 2003–04.

Analytic Findings

Multivariate logistic regression for coccidia demonstrated a significantly increased risk of infection for cats in the kitten, juvenile, and young adult age groups compared with geriatric cats (Table 3). Intact cats were at increased risk compared to neutered or spayed cats while there was no statistically significant risk associated with breed. Significantly higher risk was associated with the summer, fall, and spring seasons compared with the winter season. There was an increased risk of coccidia for most of the geographic regions compared to the South Pacific region with cats in the East South Central region having four times greater risk of infection; the North Pacific had a decreased risk.

Table 3.

Risk factors for coccidia and Giardia species infection in cats visiting Banfield hospitals in 2003 and 2004

Risk factors	Coccidia		Giardia
OR	95% Confidence interval	OR	95% Confidence interval
Age*
Kitten	55.8	38.9, 79.9	4.97	3.96, 6.26
Juvenile	7.36	4.88, 11.1	2.84	2.14, 3.78
Young adult	3.47	2.37, 5.09	1.53	1.20, 1.96
Adult	1.21	0.79, 1.87	1.03	0.79, 1.34
Geriatric†	1.00	–	1.00	–
Gender
Male intact	1.63	1.47, 1.82	1.21	1.00, 1.47
Female intact	1.51	1.36, 1.68	1.17	0.97, 1.40
Male neutered	1.11	1.01, 1.22	1.02	0.89, 1.16
Female spayed†	1.00	–	1.00	–
Breed
Mixed breed	1.13	1.00, 1.26	0.72	0.62, 0.83
Purebred†	1.00	–	1.00	–
Season
Summer	2.66	2.35, 3.01	0.86	0.73, 1.00
Fall	1.82	1.60, 2.07	0.91	0.77, 1.06
Winter†	1.00	–	1.00	–
Spring	2.09	1.82, 2.41	0.98	0.83, 1.16
Region
North Atlantic	1.86	1.51, 2.30	0.37	0.17, 0.81
East North Central	1.24	1.00, 1.54	0.81	0.51, 1.29
West North Central	2.32	1.93, 2.79	5.33	4.04, 7.03
Mid Atlantic	2.46	2.09, 2.89	0.57	0.37, 0.88
South Atlantic	2.86	2.46, 3.31	2.03	1.54, 2.67
East South Central	4.16	3.43, 5.05	3.30	2.24, 4.85
West South Central	3.36	2.88, 3.91	2.98	2.25, 3.93
Mountain	1.28	1.06, 1.56	13.17	10.31, 16.82
North Pacific	0.96	0.78, 1.20	0.46	0.28, 0.75
South Pacific†	1.00	–	1.00	–

^*Refer to Table 1 for description of age categories.

^†Reference category.

Similar to the findings for coccidia infection, multivariate logistic regression for Giardia species infection indicated an increased risk for kittens, juveniles, and young adults compared to geriatric cats. There was no statistically significant risk associated with sex or neuter status, but there was a decreased risk of infection for mixed breed cats compared with purebred cats. The summer, fall, and spring seasons had a decreased risk of infection compared with the winter season. Cats in the Mountain region had 13 times greater risk of Giardia species infection compared with cats in the South Pacific region.

Discussion

The overall fecal prevalence of Giardia species (0.58%) and coccidia (1.4%) in pet cats visiting Banfield hospitals was lower than previously reported in the veterinary literature for domestic and shelter cats. A study of feral and domestic cats in North Carolina in 2004 found a 6% Giardia species prevalence among feral cats and 5% prevalence among domestic cats (Nutter et al 2004). Another study of cats under 1 year of age in central New York reported a fecal prevalence of Giardia species infection of 7.3% and Cryptosporidium species of 3.8% (Spain et al 2001). Giardia species prevalence was found to be 2.4% in a study of domestic cats and shelter cats in Colorado and 2.4% in a study at the University of Pennsylvania Veterinary Teaching Hospital (Nolan and Smith 1995, Hill et al 2000). The latter study also found coccidia prevalence of 4.2% (Nolan and Smith 1995). Another study from the University of Missouri Veterinary Hospital found a fecal prevalence of 6.7% for coccidia (Visco et al 1978). The fecal prevalence in these published studies was determined using centrifugal flotation techniques with zinc sulfate, sugar, or magnesium sulfate solutions, with the exception of the North Carolina study in which an indirect fluorescent antibody test was used (Visco et al 1978, Nolan and Smith 1995, Hill et al 2000, Spain et al 2001, Nutter et al 2004). Differences in fecal prevalence estimates between the present study and those reported in the literature may be due to differences in the source and geographic location of the cats, the health status of the cats, age variation, as well as differences in the techniques used for a diagnosis. Use of zinc sulfate fecal flotations and direct smears was the sole means of diagnosis in the present study. Zinc sulfate solution is considered superior to sucrose solutions of equal density for flotation of protozoan cysts (Bowman 1999). It will, however, distort protozoan trophozoites. Banfield hospitals generally use fecal flotation alone without centrifugation, lowering the sensitivity of the technique. Direct smears are typically less sensitive than fecal flotations due to the small fecal sample used. However, this method is useful for identifying protozoan trophozoites (Bowman 1999). Underestimates of prevalence could have occurred if the condition of the fecal sample submitted by the owners was not of superior diagnostic quality.

The increased risk of Giardia species and coccidia infections associated with kittens, juveniles, and young adults is consistent with previous reports (Kirkpatrick 1988, Pederson 1991, Hill et al 2000, Spain et al 2001). Infection with either parasite is thought to be more common among younger cats and those housed in catteries (Kirkpatrick 1986, Pederson 1991, Dubey 1993, Barr 1998, Bowman et al 2002). One study undertaken at the University of Pennsylvania Veterinary Teaching Hospital reported a mean age of cats with coccidia infection of 2.7 years and with Giardia species infection of 1 year (Kirkpatrick 1988). A more recent study indicated that the age of cats with Giardia species infection ranged from 10 months to 4 years (Hill et al 2000). It has been suggested that older cats may become refractory to Giardia species infection because of acquired immunity (Kirkpatrick 1986, Dubey 1993, Bowman et al 2002). The present study found that kittens had a 55.8 times greater risk of coccidia infection compared with cats 10 years of age or older. This is consistent with previous reports indicating that neonates and young kittens are more commonly diagnosed with coccidiosis, especially Isospora species (Dubey and Greene 1998, Bowman 1999). A study undertaken at the University of Missouri Veterinary Hospital did not find a significant difference in coccidia infection among cats 0–5 years old (Visco et al 1978). However, in the present study, kittens were compared to geriatric cats (10+ years) whereas the Missouri study used a narrower age range.

The present study found an increased prevalence of Giardia species infection in purebred cats compared with mixed breed cats. Giardia species infection has been implicated as a cause of disease in catteries (Kirkpatrick 1986, Pederson 1991, Dubey 1993, Barr 1998, Bowman et al 2002). Coccidia infection has also been associated with catteries, but the results of the present study revealed no significant difference in risk among purebred and mixed breed cats (Pederson 1991, Dubey and Greene 1998).

The seasonal prevalences of Giardia species and coccidia were not unexpected with a peak in the fall and winter for Giardia species versus the summer for coccidia. These findings are consistent with a study that evaluated the seasonal prevalence of Giardia species and coccidia infections in dogs and another study that measured serum IgG antibodies against Cryptosporidium parvum in cats (Kirkpatrick 1988, Hill et al 2000).

An important finding of the present study is the geographic difference in fecal prevalence of Giardia species and coccidia in cats in the United States with a higher prevalence of coccidia in the south central regions and Giardia species in the Mountain region. To our knowledge, the regional prevalence of protozoal parasitism of cats based on fecal examinations has not been previously studied. Although both parasites have a worldwide distribution, environmental conditions such as humidity and soil type in these regions may influence survival of specific protozoal parasites or provide a more suitable habitat for the prey species or paratenic hosts that are a source of infection to cats such as rodents, reptiles, and birds (Pederson 1991, Bowman et al 2002, Lappin 2005).

Even though this study used more than 211,000 fecal test results over a 2 year period, there were several limitations including an unequal geographic distribution of Banfield hospitals, use of fecal examinations alone to diagnose protozoal infections, and the lack of environmental and management history for individual cats. For example, 10 states did not have Banfield hospitals and were not included in the study. Therefore, results were reported for broader geographic areas. Results of additional detection methods for protozoal infections such as giardia ELISA tests, cryptosporidium IFA or FA, and toxoplasmosis IgG/IgM, were not evaluated in this study due to the low number of tests performed. Had results of these more sensitive tests been included and centrifugation been performed in regards to fecal technique, the prevalence estimates would probably have been higher.

The findings of this study suggest that the prevalence of Giardia species and coccidia is lower than previously reported. Nonetheless, veterinarians should still counsel owners on the risks of humans acquiring protozoal infections from their cat(s), especially in households with young children, pregnant women, or immunocompromised individuals. The Companion Animal Parasite Council (CAPC) recommends that cats less than 1 year of age receive two to four fecal examinations during their first year of life and then one to two times per year thereafter (Companion Animal Parasite Council 2005).