Prevalence of serum antibody titers against feline panleukopenia virus, feline herpesvirus 1, and feline calicivirus in cats entering a Florida animal shelter

Brian A. DiGangi Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Julie K. Levy Maddie's Shelter Medicine Program, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Brenda Griffin Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Susan P. McGorray Department of Biostatistics, College of Medicine, University of Florida, Gainesville, FL 32608.

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Edward J. Dubovi Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, NY 14852.

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Patricia A. Dingman Maddie's Shelter Medicine Program, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Sylvia J. Tucker Maddie's Shelter Medicine Program, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Abstract

Objective—To determine the proportion of cats entering a Florida animal shelter with serum antibody titers against feline panleukopenia virus (FPV), feline herpesvirus 1 (FHV1), and feline calicivirus (FCV) and to identify factors associated with seropositivity.

Design—Cross-sectional study.

Animals—347 cats admitted to a Florida animal shelter.

Procedures—Within 24 hours after admission to the animal shelter, blood samples were collected from all cats ≥ 8 weeks of age. Serum antibody titers against FPV were determined via a hemagglutination inhibition assay, and those against FHV1 and FCV were determined via virus neutralization assays. Age, sex, environment (urban or rural), source (stray or previously owned), evidence of previous caregiving, health status (healthy or not healthy), and outcome (adoption, transfer, return to owner, or euthanasia) were evaluated as potential factors associated with antibody seropositivity.

Results—Of 347 cats, 138 (39.8%), 38 (11.0%), and 127 (36.6%) had antibody titers ≥ 40, ≥ 8, and ≥ 32 (ie, seropositive) against FPV, FHV1, and FCV, respectively. Factors associated with seropositivity included being neutered, age ≥ 6 months, and being relinquished by an owner. On multivariable analysis, health status at shelter admission, environment, vaccination at shelter admission, and outcome were not associated with seropositivity.

Conclusions and Clinical Relevance—Most cats were seronegative for antibodies against FPV, FHV1, and FCV at the time of admission to an animal shelter. These findings supported current guidelines that recommend vaccination of all cats immediately after admission to animal shelters, regardless of the source or physical condition.

Abstract

Objective—To determine the proportion of cats entering a Florida animal shelter with serum antibody titers against feline panleukopenia virus (FPV), feline herpesvirus 1 (FHV1), and feline calicivirus (FCV) and to identify factors associated with seropositivity.

Design—Cross-sectional study.

Animals—347 cats admitted to a Florida animal shelter.

Procedures—Within 24 hours after admission to the animal shelter, blood samples were collected from all cats ≥ 8 weeks of age. Serum antibody titers against FPV were determined via a hemagglutination inhibition assay, and those against FHV1 and FCV were determined via virus neutralization assays. Age, sex, environment (urban or rural), source (stray or previously owned), evidence of previous caregiving, health status (healthy or not healthy), and outcome (adoption, transfer, return to owner, or euthanasia) were evaluated as potential factors associated with antibody seropositivity.

Results—Of 347 cats, 138 (39.8%), 38 (11.0%), and 127 (36.6%) had antibody titers ≥ 40, ≥ 8, and ≥ 32 (ie, seropositive) against FPV, FHV1, and FCV, respectively. Factors associated with seropositivity included being neutered, age ≥ 6 months, and being relinquished by an owner. On multivariable analysis, health status at shelter admission, environment, vaccination at shelter admission, and outcome were not associated with seropositivity.

Conclusions and Clinical Relevance—Most cats were seronegative for antibodies against FPV, FHV1, and FCV at the time of admission to an animal shelter. These findings supported current guidelines that recommend vaccination of all cats immediately after admission to animal shelters, regardless of the source or physical condition.

Feline panleukopenia virus, FHV1, and FCV are widespread in the cat population in the United States,1–4 particularly in unvaccinated free-roaming strays and cats residing in animal shelters.5–8 In contrast to the low incidence or importance of these 3 viruses in privately owned pet cats, FPV, FHV1, and FCV infections are a constant and serious threat to the health and welfare of cats residing in animal shelters and often result in death. Outbreaks of FPV are frequently managed by depopulation, and the longer that a cat spends in a shelter environment, the greater its risk for the development of clinical signs of respiratory tract disease and subsequent euthanasia.7,9–11

Current guidelines recommend the vaccination of all cats ≥ 4 weeks old against FPV, FHV1, and FCV at the time of admission to animal shelters12; however, this practice may be considered cost prohibitive, unsafe, or unnecessary, particularly in shelters where a high proportion of cats are euthanized. Additionally, the proportion of cats entering animal shelters that are already protected (ie, seropositive) against infection (FPV) or disease (FHV1 and FCV) because of prior vaccination or natural exposure, and for which vaccination at shelter admission would not be beneficial, is usually unknown.

Detection of serum antibodies has been used as evidence of previous exposure to infectious agents and duration of immunologic response.2,13 Measurement of serum antibodies against FPV is recommended as a tool for managing disease outbreaks in animal shelters.14 The objective of the study reported here was to determine the prevalence of and factors associated with seropositivity for FPV, FHV1, and FCV antibodies in cats entering animal shelters. This information will provide objective data to support currently recommended vaccination protocols for cats in animal shelters as well as identify factors that may be useful components of a risk assessment for individual cats during a disease outbreak.

Materials and Methods

Animals—Cats admitted to an animal shelter between May 7 and August 15, 2010, were enrolled in the study. Information collected for each cat included date of admission, signalment (age, breed, sex, and neuter status), ZIP code of origin, source (stray, previously owned, or confiscated or left at the shelter night box [other]), evidence of caregiving (relinquished, declawed, neutered, microchipped, collared or tagged, or ear-tipped by a trap-neuter-return program), health status at admission (healthy or not healthy), and outcome (adopted, transferred, euthanized, or reclaimed by owner). If a cat's actual age was unknown, age was estimated as pediatric (< 6 months), adolescent (6 to 11 months), young adult (1 to 5 years), or mature adult (> 5 years). Cats were classified as sexually intact if no evidence of a previous sterilization surgery was detected during physical examination. Address of origin was used to determine whether the community from which the cat originated was primarily urban or rural on the basis of population density, number of residents, housing density, income, and land use as recorded in an online directory.15 Vaccination history for owner-relinquished cats prior to entering the shelter was unknown. Health status of cats was determined on the basis of results of physical examinations performed by a veterinarian or trained technician. Body condition score was evaluated on a 9-point scale, with 1 being emaciated and 9 being obese16; for this study population, BCSs of 4, 5, or 6 were considered ideal. A cat was classified as not healthy if it had clinical signs of illness, an injury, positive results on a retroviral screening (FeLV antigen and FIV antibody) test, or any combination of these factors. A cat that had one of the following physical examination findings in the absence of other abnormalities was considered healthy: fleas, ear mites, mild dental disease, lactation, pregnancy, matted fur, or was underweight or overweight (BCS, 2 to 3 or 7 to 8, respectively). The study protocol was approved by the University of Florida Institutional Animal Care and Use Committee.

Study site—The study was conducted in an open-admission municipal animal shelter in north Florida. In 2009, the population of the county in which the shelter was located was 243,574 people, and 4,030 cats were admitted to the shelter.

Serologic testing—Blood (3 mL) was collected via jugular, cephalic, or femoral venipuncture into serum separator tubes within 24 hours after admission to the shelter. In accordance with shelter policy, cats were vaccinated as soon after admission as possible; therefore, in some instances, cats were vaccinated prior to blood sample collection. Serum was obtained by centrifugation and stored at −20°C until analysis. Serum antibody titers were determined via a hemagglutination inhibition assay for FPV and via virus neutralization assays for FHV1 and FCV at a university-affiliated diagnostic laboratory.a On the basis of a literature review that included independent challenge studies,17 the laboratory at which the assays were conducted recommends assessment for booster vaccination when FPV, FHV1, and FCV antibody titers are < 40, < 8, and < 32, respectively. For the purposes of this study, cats with FPV, FHV1, and FCV antibody titers ≥ 40, ≥ 8, and ≥ 32, respectively, were considered seropositive for the given virus. Cats with FPV, FHV1, and FCV antibody titers < 40, < 8, and < 32, respectively, were considered seronegative for the given virus. All cats were also tested for FeLV antigen and FIV antibodies via a commercially available point-of-care assay.b

Statistical analysis—Prevalence of antibody seropositivity was defined as the number of seropositive cats divided by the number of cats tested for FPV, FHV1, and FCV, respectively. Factors associated with seropositivity were determined via a χ2 test; univariable logistic regression was used to calculate ORs and 95% CIs. All potential factors were entered into a multivariable logistic regression model via stepwise variable selection. Interaction between selected explanatory variables was examined, and Hosmer-Lemeshow tests were used to assess goodness of fit for the models. All analyses were performed with statistical software,c,d and values of P < 0.05 were considered significant for all analyses.

Results

Animals—The demographics of the 347 cats evaluated in the study were summarized (Table 1). Cats categorized as not healthy (n = 65) included the following: 23 cats (1 of which had positive results for FeLV antigen) with signs of an upper respiratory tract infection alone or in combination with other signs of illness or neglect, 4 with diarrhea, 13 (6 of which had positive results for FeLV antigen) with flea infestation in combination with other conditions, and 25 (3 of which had positive results for FeLV antigen, and 1 had positive results for FIV antibodies) with other signs of illness or neglect.

Table 1—

Descriptive analysis for 347 cats admitted to a north Florida animal shelter between May 7 and August 15, 2010.

VariableCategoryNo. (%)
SourceStray234 (67)
Owned95 (27)
Other18 (5)
EnvironmentRural259 (75)
Urban88 (25)
Identification*None321 (93)
Microchip15 (4)
Ear tipped7 (2)
Collar5 (1)
Age< 6 m195 (56)
6–11 m41 (12)
1–5 y97 (28)
> 5 y14 (4)
SexSexually intact male122 (35)
Castrated male27 (8)
Sexually intact female169 (49)
Spayed female29 (8)
BreedDomestic shorthair291 (84)
Domestic longhair47 (14)
Other9 (3)
Health statusHealthy282 (81)
Not healthy65 (19)
BCS1–337 (11)
4–6297 (86)
7–913 (4)
Signs of caregivingNo213 (61)
Yes134 (39)
Vaccinated at admissionNo82 (24)
Yes265 (76)
OutcomeAdopted93 (27)
Transferred46 (13)
Reclaimed by owner6 (2)
Euthanized202 (58)

One cat had an ear tip as well as a microchip and was counted in each category.

Factors associated with seropositivity—Of the 347 cats admitted to the shelter, 138 (39.8%) were seropositive for FPV antibodies (Figure 1). Cats ≥ 1 year old were more likely to be seropositive for FPV antibodies than were cats < 6 months old (P ≤ 0.02), and the odds for cats being seropositive for FPV antibodies increased with age (Table 2). Cats that were neutered, were relinquished by their owners, were from an urban environment, or had signs of previous caregiving were more likely to be seropositive for FPV antibodies than were cats that were not. Cats that were overweight (BCS, 7 to 9) were significantly (P = 0.02) more likely to be seropositive for FPV antibodies than were cats that were underweight (BCS, 1 to 3). Cats vaccinated < 24 hours prior to blood sample collection were less likely to be seropositive for FPV antibodies than were cats that were not vaccinated (P = 0.03), and cats reclaimed by an owner (P < 0.01) or euthanized (P = 0.03) were more likely to be seropositive for FPV antibodies than were cats that were adopted. On multivariable analysis to identify factors significantly associated with cats being seropositive for FPV antibodies, evidence suggested that source, environment of origin, signs of previous caregiving, and vaccination < 24 hours prior to blood sample collection were each significantly associated (ie, collinear) with neuter status; therefore, only one of the collinear terms could be included in the model. The inclusion of neuter status provided the best model fit. Thus, the final multivariable model for FPV seropositivity included only neuter status; neutered cats were significantly (P < 0.01) more likely to be seropositive for FPV antibodies than were sexually intact cats (OR, 4.4; 95% CI, 2.4 to 8.3).

Table 2—

Results of univariable logistic regression analyses of factors associated with cats being seropositive (antibody titer, ≥ 40) for FPV at shelter admission for the cats in Table 1.

VariableCategoryNo. testedNo. seropositivePrevalence (%)OR95% CIP value
Age< 6 m1956633.8ReferentNANA
6–11 m411126.80.70.3–1.60.38
1–5 y975253.62.31.3–3.8< 0.01
> 5 y14964.33.51.0–12.70.02
Neuter statusSexually intact2919934.0ReferentNANA
Neutered563969.64.52.3–8.7< 0.01
SourceStray2348134.6ReferentNANA
Owned954749.51.91.1–3.10.01
Other181055.62.40.8–6.90.07
EnvironmentRural2599235.5ReferentNANA
Urban884652.32.01.2–3.3< 0.01
Health status at admissionHealthy28211239.7ReferentNANA
Not healthy652640.01.00.6–1.80.97
Signs of caregivingNo2136831.9ReferentNANA
Yes1347052.22.31.5–3.7< 0.01
BCS1–3371540.5ReferentNANA
4–629711338.00.90.4–1.90.77
7–9131076.94.91.0–27.30.02
Vaccinated < 24 h after admissionNo824150.0ReferentNANA
Yes2659736.60.60.3–1.00.03
OutcomeAdopted932830.1ReferentNANA
Transferred461634.81.20.6–2.80.58
Reclaimed by owner66100.0< 0.01
Euthanized2028843.61.81.0–3.10.03

NA = Not applicable. — = Not determined.

Figure 1—
Figure 1—

Distribution of serum antibody titers for FPV (A), FHV1 (B), and FCV (C) as determined via a hemagglutination inhibition (FPV) or virus neutralization (FHV1 and FCV) assay performed on blood samples collected within 24 hours after admission for 347 cats that were admitted to a north Florida animal shelter between May 7 and August 15, 2010. The antibody titer thresholds (dashed line) for classifying cats as seropositive were ≥ 40, ≥ 8, and ≥ 32 for FPV, FHV1, and FCV, respectively.

Citation: Journal of the American Veterinary Medical Association 241, 10; 10.2460/javma.241.10.1320

Thirty-eight of 347 (11.0%) cats were seropositive for FHV1 antibodies (Figure 1). Cats ≥ 6 months old were more likely to be seropositive for FHV1 antibodies than were cats < 6 months of age, and the odds for cats being seropositive for FHV1 antibodies increased with age (Table 3). Cats that were neutered (P < 0.01), were relinquished by their owners (P = 0.04), were from an urban environment (P < 0.01), or had signs of previous caregiving (P < 0.01) were more likely to be seropositive for FHV1 antibodies than were cats that were not. Cats that had an ideal BCS (BCS, 4 to 6) were less likely to be seropositive for FHV1 antibodies than were cats that were underweight (BCS, 1 to 3). The final multivariable logistic regression model for FHV1 seropositivity included age and neuter status; the odds of a cat being seropositive for FHV1 antibodies increased with age, and neutered cats were more likely to be seropositive for FHV1 antibodies than were sexually intact cats (Table 4).

Table 3—

Results of univariable logistic regression analyses of factors associated with cats being seropositive (antibody titer, ≥ 8) for FHV1 at shelter admission for the cats in Table 1.

VariableCategoryNo. testedNo. seropositivePrevalence (%)OR95% CIP value
Age< 6 m19510.5ReferentNANA
6–11 m4137.315.31.4–392.90.01
1–5 y972727.874.810.6–1,507.5< 0.01
> 5 y14750.0194.018.9–4,840.6< 0.01
Neuter statusSexually intact291155.2ReferentNANA
Neutered562341.112.85.7–28.9< 0.01
SourceStray234219.0ReferentNANA
Owned951616.82.11.0–4.40.04
Other1815.60.60.0–4.60.62
EnvironmentRural259218.1ReferentNANA
Urban881719.32.71.3–5.7< 0.01
Health status at admissionHealthy282279.6ReferentNANA
Not healthy651116.91.90.8–4.40.08
Signs of caregivingNo213136.1ReferentNANA
Yes1342518.73.51.7–7.6< 0.01
BCS1–3371027.0ReferentNANA
4–6297217.10.20.1–0.5< 0.01
7–913753.83.20.7–14.40.08
Vaccinated < 24 h after admissionNo8278.5ReferentNANA
Yes2653111.71.40.6–3.70.42
OutcomeAdopted931314.0ReferentNANA
Transferred46613.00.90.3–2.90.88
Reclaimed by owner6233.33.10.4–23.00.2
Euthanized202178.40.60.3–1.30.14

See Table 2 for key.

Table 4—

Results for the final multivariable logistic regression model of factors associated with cats being seropositive (antibody titer, ≥ 8) for FHV1 at shelter admission for the cats in Table 1.

VariableCategoryOR95% CI
Age< 6 mReferentNA
6–11 m14.91.5–147.2
1–5 y45.95.8–363.1
> 5 y88.48.5–915.8
Neuter statusSexually intactReferentNA
Neutered2.71.2–6.4

See Table 2 for key.

One hundred twenty-seven of 347 (36.6%) cats were seropositive for FCV antibodies (Figure 1). Cats ≥ 6 months old were more likely to be seropositive for FCV antibodies than were cats < 6 months old (Table 5). Cats that were neutered (P < 0.01), were relinquished by their owners (P < 0.01), were not healthy at shelter admission (P < 0.01), or had signs of previous caregiving (P < 0.01) were more likely to be seropositive for FCV antibodies than were cats that were not. Cats that had an ideal BCS (BCS, 4 to 6) were less likely to be seropositive for FCV antibodies than were cats that were underweight (BCS, 1 to 3). The final multivariable logistic regression model for FCV seropositivity included age and source (Table 6).

Table 5—

Results of univariable logistic regression analyses of factors associated with cats being seropositive (antibody titer, ≥ 32) for FCV at shelter admission for the cats in Table 1.

FactorCategoryNo. testedNo. seropositivePrevalence (%)OR95% CIP value
Age< 6 m1953216.4ReferentNANA
6–11 m412868.311.04.8–25.2< 0.01
1–5 y975657.77.03.9–12.6< 0.01
> 5 y141178.618.74.5–90.0< 0.01
Neuter statusSexually intact2919332.0ReferentNANA
Neutered563460.73.31.8–6.2< 0.01
SourceStray2347632.5ReferentNANA
Owned954850.52.11.3–3.6< 0.01
Other18316.70.40.1–1.60.16
EnvironmentRural2599536.7ReferentNANA
Urban883236.41.00.6–1.70.96
Health status at admissionHealthy2829433.3ReferentNANA
Not healthy653350.82.11.2–3.7< 0.01
Signs of caregivingNo2136329.6ReferentNANA
Yes1346447.82.21.4–3.5< 0.01
BCS1–3372259.5ReferentNANA
4–62979632.30.30.2–0.7< 0.01
7–913969.21.50.3–7.30.53
Vaccinated < 25 h after admissionNo822631.7ReferentNANA
Yes26510138.11.30.8–2.30.29
OutcomeAdopted932931.2ReferentNANA
Transferred461532.61.10.5–2.40.86
Reclaimed by owner6233.31.10.1–7.60.91
Euthanized2028140.11.50.9–2.60.14

See Table 2 for key.

Table 6—

Results for the final multivariable logistic regression model of factors associated with cats being seropositive (antibody titer, ≥ 32) for FCV at shelter admission for the cats in Table 1.

FactorCategoryOR95% CI
Age< 6 mReferentNA
6–11 m11.75.4–25.3
1–5 y6.83.9–11.9
> 5 y16.74.2–66.6
OriginStrayReferentNA
Owned1.781.01–3.13
Other0.290.07–1.17

See Table 2 for key.

Discussion

In the present study, most cats were seronegative for FPV, FHV1, and FCV antibodies at the time they were admitted to the animal shelter. Older cats and cats that had been neutered or were relinquished by an owner were the cats most likely to be seropositive for FPV, FHV1, or FCV antibodies.

Although the present study was conducted at a single Florida animal shelter, the characteristics of this population of shelter cats were similar to those of cats in shelters across the United States.18 A similar studye revealed that 48% of cats admitted to a Wisconsin animal shelter had antibodies against FPV. A study5 that involved predominantly adult, unvaccinated feral cats from the same region as the cats of the present study revealed that 33%, 64%, and 21% of cats had antibodies against FPV, FHV1, and FCV, respectively. Thus, the prevalence of cats with antibodies against FPV in the study reported here was similar to that of unvaccinated feral cats of the other study.5 Conversely, in the study reported here, the prevalence of cats with antibodies against FHV1 was lower and the prevalence of cats with antibodies against FCV was higher, compared with that for unvaccinated feral cats of the other study.5

Analyses of risk factors associated with FPV, FHV1, and FCV infections in cats in animal shelters are lacking, but results of 1 study19 indicate that young kittens are the cats most susceptible to FPV infection and subsequent death. Increased time spent in an animal shelter is associated with an increased risk of developing disease from FHV1 and FCV, especially for kittens.10 Cats with no record of previous vaccination and purebred cats are also at increased risk for developing respiratory tract disease in animal shelters.7,20 Results of the present study support the findings that cats < 6 months of age are more vulnerable to infection with FPV, FHV1, and FCV than are older cats. The increased odds for cats that were neutered or relinquished to the shelter by their owners to be seropositive for antibodies against the evaluated viruses was probably the result of these cats having had previous veterinary care that included vaccination. Despite the fact that multiple cat-related factors were associated with seropositivity for antibodies against FPV, FHV1, and FCV in the present study, it has been suggested that cat-related factors are not as important as facility-related factors (eg, the number of cats admitted, population density, and availability of designated isolation areas for unhealthy cats) for the assessment of the risk for transmission of infectious disease in animal shelters.20,21

Surprisingly, the type of community (rural or urban) from which a cat originated, the health status of a cat at shelter admission, signs of previous caregiving aside from being neutered, and outcome were not associated with seropositivity in the multivariable models. Thus, these factors should not be used to determine an individual cat's need for vaccination at the time of shelter admission or in a risk assessment during a disease outbreak in a shelter. Rather, these findings emphasize the need for all cats to be vaccinated at admission to an animal shelter, regardless of their health status or evidence of previous veterinary care.

Identification and isolation of cats with active disease on the basis of clinical signs of disease or diagnostic test results are the first essential components for controlling a disease outbreak.8,22 During a disease outbreak, the results of antibody titer measurements can be used to classify cats that do not have clinical signs of disease but have been exposed to diseased cats into risk categories so that they can be managed accordingly. This would be especially useful during an FPV outbreak because seropositivity for FPV antibodies is highly predictive of immunity. In contrast, infection with FCV or FHV1 often results in chronic carrier states and the development of partial immunity, which makes antibody titer interpretation less predictive for protection against clinical disease. Caution should be taken whenever antibody titers are used to predict protection against infection (ie, FPV) or disease (ie, FHV1 and FCV) because universal laboratory reference standards for protective antibody titers have not been established and antibody titer thresholds used to classify a cat as seropositive or seronegative are established by the individual laboratory performing the assays. Additionally, different commercial laboratories may use different methods and can report different results when evaluating the same sample, so a single distinct antibody titer threshold at which protection exists cannot be defined. Results of the present study suggested that most cats admitted to animal shelters do not have adequate protection against life-threatening viral infections commonly encountered in those facilities. Vaccination of all cats should occur immediately at or before admission to a high-risk environment such as an animal shelter and should not be withheld from cats with signs of previous veterinary care.

ABBREVIATIONS

BCS

Body condition score

CI

Confidence interval

FCV

Feline calicivirus

FHV1

Feline herpesvirus 1

FPV

Feline panleukopenia virus

a.

Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, NY.

b.

SNAP FIV/FeLV Combo test, IDEXX Laboratories, Westbrook, Me.

c.

Epi Info, version 3.5.1, CDC, Atlanta, Ga.

d.

SAS, version 9.1.3, SAS Institute Inc, Cary, NC.

e.

Newbury SP, Haase C, Larson LJ, et al. A high percentage of feral cats and cats entering a large shelter were found to be susceptible to feline panleukopenia virus (parvovirus) (abstr), in Proceedings. Conf Res Work Anim Dis 2006;93.

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