• View in gallery
    Figure 1—

    Number of cats admitted to SJACC as alive (black bars) or dead (gray bars) from 2006 through 2013.

  • View in gallery
    Figure 2—

    Number of cats admitted to SJACC that were adopted (black bars), euthanized (gray bars), sent to rescue groups (diagonally striped bars), returned to owners (white bars), transferred to another facility or group (hatched bars), or had other outcomes (dotted bars) from 2006 through 2013.

  • View in gallery
    Figure 3—

    Percentage of kittens (< 4 months of age) and adult cats admitted to SJACC before (January 1, 2006, to March 7, 2010) and after (March 8, 2010, to December 31, 2013) initiation of an SNR program by outcome. Cats of unknown age were not included. See Figure 2 for key.

  • View in gallery
    Figure 4—

    Percentage of kittens (< 4 months of age; black bars) and adult cats (gray bars) that were euthanized after admission to SJACC from 2006 through 2013. Cats of unknown age were not included.

  • View in gallery
    Figure 5—

    Percentage of kittens (< 4 months of age) and adult cats admitted to SJACC before (January 1, 2006, to March 7, 2010) and after (March 8, 2010, to December 31, 2013) initiation of an SNR program by outcome. Cats of unknown age were not included. See Figure 4 for remainder of key.

  • View in gallery
    Figure 6—

    Number of cats that were euthanized because of URI (black bars) and number with a diagnosis of or treated for URI (gray bars) after admission to SJACC from 2006 through 2013.

  • View in gallery
    Figure 7—

    Percentage of kittens (< 4 months of age) and adult cats admitted to SJACC before (January 1, 2006, to March 7, 2010) and after (March 8, 2010, to December 31, 2013) initiation of an SNR program by whether they were euthanized because of URI or had a diagnosis of or were treated for URI after admission. Cats of unknown age were not included. See Figure 4 for remainder of key.

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Association between a shelter-neuter-return program and cat health at a large municipal animal shelter

Charlotte H. EdinboroHealth Sciences Practice, Exponent Inc, 149 Commonwealth Dr, Menlo Park, CA 94025

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Heather N. WatsonStatistical and Data Sciences Practice, Exponent Inc, 149 Commonwealth Dr, Menlo Park, CA 94025

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Anne FairbrotherEcoSciences Practice, Exponent Inc, 15375 SE 30th Pl, Ste 250, Bellevue, WA 98007.

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Abstract

OBJECTIVE To determine effects of a shelter-neuter-return (SNR) program on cat admissions and health at a large municipal animal shelter in Northern California.

DESIGN Retrospective cohort study.

ANIMALS 117,383 cats for which data were recorded in the San Jose Animal Care Center database between January 1, 2006, and December 31, 2013.

PROCEDURES Shelter records were analyzed for trends in cat demographic data, shelter intake and outcome types, and prevalence of upper respiratory infection (URI) over the 8-year period and before and after initiation of an SNR program on March 8, 2010.

RESULTS Number of cats admitted to the shelter each year decreased significantly over 8 years; beginning in 2010, duration of stay decreased. Proportion of cats euthanized decreased from 66.6% (28,976/43,517) in the pre-SNR period to 34.9% (11,999/34,380) in the post-SNR period, whereas prevalence of URI increased from 5.5% to 6.8%, and median duration of shelter stay decreased from 6 to 5 days for cats < 4 months of age and from 8 to 6 days for older cats. With implementation of the SNR program and a new treatment policy for cats with URI, more cats received treatment with less medication, yielding cost savings.

CONCLUSIONS AND CLINICAL RELEVANCE Initiation of the SNR program was associated with a decreased number of cats admitted to the shelter and a lower proportion euthanized. With increased resources to care for cats with URI and changes in the URI treatment protocol, fewer cats were euthanized for URI and more cats were treated at lower cost and with a briefer shelter stay.

Abstract

OBJECTIVE To determine effects of a shelter-neuter-return (SNR) program on cat admissions and health at a large municipal animal shelter in Northern California.

DESIGN Retrospective cohort study.

ANIMALS 117,383 cats for which data were recorded in the San Jose Animal Care Center database between January 1, 2006, and December 31, 2013.

PROCEDURES Shelter records were analyzed for trends in cat demographic data, shelter intake and outcome types, and prevalence of upper respiratory infection (URI) over the 8-year period and before and after initiation of an SNR program on March 8, 2010.

RESULTS Number of cats admitted to the shelter each year decreased significantly over 8 years; beginning in 2010, duration of stay decreased. Proportion of cats euthanized decreased from 66.6% (28,976/43,517) in the pre-SNR period to 34.9% (11,999/34,380) in the post-SNR period, whereas prevalence of URI increased from 5.5% to 6.8%, and median duration of shelter stay decreased from 6 to 5 days for cats < 4 months of age and from 8 to 6 days for older cats. With implementation of the SNR program and a new treatment policy for cats with URI, more cats received treatment with less medication, yielding cost savings.

CONCLUSIONS AND CLINICAL RELEVANCE Initiation of the SNR program was associated with a decreased number of cats admitted to the shelter and a lower proportion euthanized. With increased resources to care for cats with URI and changes in the URI treatment protocol, fewer cats were euthanized for URI and more cats were treated at lower cost and with a briefer shelter stay.

Historically, stray cats that entered animal shelters were housed for variable durations, depending on legislative directive and resource availability. Cats considered feral or unsocialized were typically isolated from other animals so their behavior could be observed during the shelter stay. At the end of the shelter stay, cats that were, or appeared to be, feral often were euthanized on that basis. Some otherwise socialized cats that had signs of fear after arrival in this new setting may have consequently appeared feral on the basis of their response to close housing with other cats, novel foods, strange surroundings, potential inability to move beyond a small cage, and other changes in their circumstances. Those cats generally were euthanized as well. Feral cats in shelters were likely to remain there until they were euthanized because of temperaments that would render them unadoptable, their potential to develop URI from the distress associated with close confinement, and limited resources for their care while housed there.1–6

Through the efforts of dedicated caregivers, colonies of feral cats have been established in many locations, generally because of the availability of food and some degree of safety from predators and other threats, including humans and vehicular traffic.7,8 A principle component of feral cat colony management is TNR programs, with the expectation that, over time, the population of feral cats would decrease because of their inability to reproduce.4,6,9–12 Although establishment of managed feral cat colonies has successfully reduced the numbers of free-roaming cats in some areas, such programs require ongoing active commitment by 1 or more caregivers.8

Another strategy to reduce the number of feral cats involves the so-called Feral Freedom concept.13 In this scheme, free-roaming cats are trapped, spayed or neutered, and returned to their sites of capture, with recognition that these cats were living successfully without dedicated caregivers or colonies. Cats in such programs are vaccinated against rabies, are treated for flea infestation, and have microchips implanted for future identification; minor medical procedures are performed at the time of gonadectomy when necessary. Cats that would have been housed in a shelter are instead returned to the streets within a few days after gonadectomy, as close as possible to the sites where they were trapped, to live as before, without contributing to future generations of free-roaming cats. The return of these free-roaming cats to their sites of origin within 3 to 4 days is understood to fill a niche in the suburban or urban environment that would otherwise be filled by nongonadectomized free-roaming cats.

Several large communities and animal control organizations have embraced the Feral Freedom strategy, including the City of San Jose Animal Care and Services.14,15 This municipal department operates SJACC, which adopted a Feral Freedom program on March 8, 2010, initially as a pilot program, in collaboration with Town Cats of Morgan Hill and the Cat Resource Center. Town Cats, a rescue group, provides transportation back to sites where the cats in the program were initially trapped. An analysis of shelter cat admissions between March 2010 and June 2014 revealed a decrease in numbers of kittens and adult cats euthanized, increase in the number of live releases, and decrease in the number of cats euthanized because of URIs.16 A deeper evaluation of the program, now referred to as Shelter-Neuter-Return, was initiated to assess the success of this program and its impact on feline health within the shelter.

The purpose of the study reported here was to determine whether, after the start of the SNR program, fewer cats were admitted to SJACC (alive or dead), fewer cats were euthanized, the proportion of feral cats admitted was lower, and fewer cats in the shelter were identified with URI. We also sought to identify whether the shelter staff adhered to shelter animalcare guidelines17,18 and vaccinated all cats against feline upper respiratory viruses and feline panleukopenia virus (via the FVRCP vaccine) within 24 hours after admission throughout the entire period. A final objective was to determine whether changes in the treatment protocol for URI resulted in financial savings through decreases in the proportion of cats with URI and duration of shelter stay.

Materials and Methods

Cats and data collection

Cat admission reports were provided by SJACC for the years 2006 through 2013. Five types of reports were received as generated by the shelter softwarea and in spreadsheetb format. These files were imported into statistical softwarec,d,e for evaluation. Records included cat demographic data, addresses of the locations where cats were found or addresses given by surrendering owners or reporting parties, date of and cat condition at shelter intake, and date and disposition of outcome. Records also included large text blocks in which treatments, including vaccinations received at admission, were recorded; notations regarding contacts (owners, foster care providers, and rescuers), medical examinations, and other correspondence among personnel; and data concerning geographic information (addresses or street intersections), numbers of cats at various locations, and encounters with animal control officers that did not result in shelter admissions. Duplicate identification numbers and record entries were noted and reconciled through inspection, when possible. Because of incomplete records and other data entry problems, inconsistencies remained in some of the data; therefore, numbers did not always sum to expected total numbers of cats in various categories. Variables with large numbers of categories were reclassified to provide fewer categories.

Additional information provided by SJACC included yearly budgets for shelter operational expenditures, veterinary services, and spay-neuter clinic as well as for personnel and other expenses. In addition, estimates for medication costs and time required for treatment of cats with URI by veterinary staff were provided.

Statistical analysis

Summary statistics were calculated for the total number of cats admitted to SJACC. For further analysis, number of shelter admissions, which sometimes included multiple admissions for the same cat, was included because each admission required use of shelter space, food, staff and volunteer time, and other resources. Data for cats that were not admitted to the shelter were excluded from further analysis.

The search terms FVRCP or vaccine as well as related date information were used to identify in record text fields the first date at which an FVRCP vaccine was administered to cats after admission to decrease clinical signs of URI. The search term URI was used to identify cats for which a diagnosis of URI had been made by a shelter veterinarian or to which treatment for a diagnosed URI had been administered during their shelter stays. When discernible from these entries, first date of URI diagnosis was used to calculate the number of days that each cat had been housed in the shelter before signs of infection appeared. For cats with a URI diagnosis, further analysis included comparison of the duration of stay from admission to diagnosis between the period before March 8, 2010 (ie, the start date for the SNR program; pre-SNR period), and the period after that date (post-SNR period). Comparisons were made between cats with and without URI in the pre- and post-SNR periods for duration of stay until postadmission vaccination as well as overall duration of shelter stay.

The health of cats involved in the SNR program after their initial admission and release was also evaluated, including whether they were received as dead, injured, sick, or a reported nuisance. Inspection of the data revealed that complaints regarding cats or their behavior were indistinguishable from nuisance reports, so the latter term was used. Information for cats that were readmitted to the shelter and reported as nuisances following release was recorded. Free-roaming cats that were discussed with animal control officers but not returned to the shelter were not entered into the database and therefore were not included in this analysis.

Distributions of categorical demographic characteristics were compared between pre- and post-SNR periods by use of the χ2 test and evaluated for temporal trends across the entire study period by use of the Mantel-Haenszel test. Continuous data, such as duration of shelter stay, were tested for normality and compared between periods or over years by use of the Student t test (normally distributed data) or Wilcoxon rank sum or Kruskal-Wallis test (nonnormally distributed data). Temporal trends in cat admissions were evaluated by means of linear regression. Univariate and multivariate logistic regression was used to identify risk factors for URI diagnosis or treatment. A cost analysis for URI treatments over the study period was performed. Values of P < 0.05 were considered significant for all analyses.

Results

All cats

From 2006 through 2013, 117,383 unique cats were brought to SJACC. These included 117,145 unique cats representing a total of 123,773 shelter admissions. Of the total cats brought to the shelter, 42,898 were not admitted and were not included in further analysis because they did not use up shelter resources. These nonadmitted cats included 27,214 cats that had been brought to the spay-neuter clinic, 4,760 that had been brought to vaccination clinics, and 10,924 calls for animal-control assistance or investigations that did not result in admissions. An additional 238 cats were brought to the shelter for health examinations, vaccinations, and deworming medications but were not associated with admissions to the shelter. Because of inconsistencies in the records, several discrepancies existed in data totals and those discrepancies are noticeable in the reported findings.

Of the cats admitted to the shelter, 12,769 (10.9%) unique cats (12,775 admissions [10.3%]) were received as dead and 1,863 (1.6%) were received as owner-requested euthanasia, disposal, or unborn; these cats were removed from descriptive analysis. After additional data review and validation, data on 75,535 unique alive cats (77,897 shelter admissions) were available for further analysis.

The proportion of cats received as dead decreased significantly (P < 0.001) from 2006 through 2013. Similarly, the proportion of dead cats decreased significantly (P < 0.001) after the SNR program started on March 8, 2010 (Figure 1). Before the SNR program began, 7,474 of 50,991 (14.7%) cats were received as dead and 43,517 (85.3%) cats were admitted alive. After the program began, 5,301 of 39,681 (13.4%) cats were received as dead and 34,380 (86.6%) were admitted alive. During the 8-year period, the number of live admissions decreased significantly (P = 0.009; Table 1).

Figure 1—
Figure 1—

Number of cats admitted to SJACC as alive (black bars) or dead (gray bars) from 2006 through 2013.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

Table 1—

Number (%) of cats with various characteristics admitted to SJACC from 2006 through 2013 and before and after initiation of an SNR program on March 8, 2010.

Characteristic2006 (n = 10,732)2007 (n = 10,037)2008 (n = 10,932)2009 (n = 10,982)2010 (n = 9,768)2011 (n = 8,744)2012 (n = 8,213)2013 (n = 8,489)Before SNR program (n = 43,517)After SNR program (n = 34,380)
Age
  Kitten*5,708 (53.2)5,517 (55.0)6,128 (56.1)6,124 (55.8)5,480 (56.1)4,840 (55.4)4,473 (54.5)4,839 (57.0)23,657 (54.4)19,452 (56.6)
  Adult4,234 (39.5)3,972 (39.6)4,209 (38.5)4,250 (38.7)3,736 (38.2)3,319 (38.0)3,165 (38.5)3,054 (36.0)17,233 (39.6)12,706 (36.9)
  Unknown790 (7.4)548 (5.5)595 (5.4)608 (5.5)552 (5.7)585 (6.7)575 (7.0)596 (7.0)2,627 (6.0)2,222 (6.5)
Sex
  Female2,346 (21.9)2,574 (25.6)3,078 (28.2)2,968 (27.0)3,560 (36.4)3,695 (42.3)3,563 (43.4)3,558 (41.9)11,203 (25.7)14, 139 (41.1)
  Male1,783 (16.6)2,096 (20.9)2,349 (21.5)2,410 (21.9)3,358 (34.4)3,498 (40.0)3,312 (40.3)3,494 (41.2)8,884 (20.4)13,416 (39.0)
  Unknown6,603 (61.5)5,367 (53.5)5,505 (50.4)5,604 (51.0)2,850 (29.2)1,551 (17.7)1,338 (16.3)1,437 (16.9)23,430 (53.8)6,825 (19.9)
Neuter status
  Gonadectomized2,387 (22.2)2,496 (24.9)2,941 (26.9)2,872 (26.2)4,499 (46.1)4,869 (55.7)4,828 (58.8)5,158 (60.8)11,009 (25.3)19,041 (55.4)
  Sexually intact or unknown8,345 (77.8)7,541 (75.1)7,991 (73.1)8,110 (73.8)5,269 (53.9)3,875 (44.3)3,385 (41.2)3,331 (39.2)32,508 (74.7)15,339 (44.6)
Breed
  Domestic shorthair9,018 (84.0)8,488 (84.6)8,909 (81.5)8,921 (81.2)7,833 (80.2)7,114 (81.4)6,486 (79.0)6,698 (78.9)35,970 (82.7)27,497 (80.0)
  Domestic medium hair or longhair1,504 (14.0)1,335 (13.3)1,842 (16.8)1,862 (17.0)1,759 (18.0)1,483 (17.0)1,540 (18.8)1,648 (19.4)6,710 (15.4)6,263 (18.2)
  Other210 (2.0)214 (2.1)181 (1.7)199 (1.8)176 (1.8)147 (1.7)187 (2.3)143 (1.7)837 (1.9)620 (1.8)

Proportions changed significantly (P < 0.001; Mantel-Haenszel test) over the study period and differed significantly (P < 0.001; χ2 test) before and after the SNR program began.

Kittens were defined as cats < 4 months old when age was available or as a record entry of kitten or kitten size; adults were defined as ≥ 4 months of age when age was available or as a record entry of adult or adult size.

Cat ages were not uniformly recorded in the shelter database. Cats < 4 months of age when age was available or recorded as kittens or of kitten size were considered kittens; adults were defined as cats ≥ 4 months of age when age was available or recorded as adults or of adult size. Age could not be defined for 6.2% (4,849/77,897) of cats in the 8-year period.

During the 8-year period, the number of live admissions decreased significantly (P = 0.009; Table 1). Significantly more kittens than adults were admitted during each year of the study (P < 0.001); more kittens than adults were admitted to the shelter in both the post-SNR and pre-SNR periods (P < 0.001). After 2010, recording of sex improved, and reproductive status was updated after gonadectomy procedures. It was not possible to compare the sex or reproductive status at shelter admission of 38.8% (30,255/77,897) of cats over the study period; in the pre-SNR period, 53.8% (23,430/43,517) of cats’ sexes were not recorded, compared with 19.9% (6,825/34,380) of cats in the post-SNR period.

Various intake types were similarly distributed over the 8-year period and between pre- and post-SNR periods (Table 2). Most cats were admitted as stray. More than 90% of cats were from the city of San Jose, Calif, regardless of the year. The proportion of euthanized cats decreased from nearly 70% (7,392/10,732) in 2006 to < 30% (2,321/8,489) in 2013 (Figure 2). During this period, the proportion of cats that were adopted increased modestly, from approximately 13% to nearly 17%, and the proportion of transfers to rescue groups increased dramatically, from < 1% to nearly 24%, as expected with the SNR program. These proportional shifts over the 8-year period were evident when distributions were compared for kittens and adults between pre- and post-SNR periods (Figure 3). Median duration of shelter stay was greater for adult cats than for kittens for every year of the study period (Table 3).

Figure 2—
Figure 2—

Number of cats admitted to SJACC that were adopted (black bars), euthanized (gray bars), sent to rescue groups (diagonally striped bars), returned to owners (white bars), transferred to another facility or group (hatched bars), or had other outcomes (dotted bars) from 2006 through 2013.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

Figure 3—
Figure 3—

Percentage of kittens (< 4 months of age) and adult cats admitted to SJACC before (January 1, 2006, to March 7, 2010) and after (March 8, 2010, to December 31, 2013) initiation of an SNR program by outcome. Cats of unknown age were not included. See Figure 2 for key.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

Table 2—

Number (%) of cats admitted to SJACC with various intake classifications and outcomes from 2006 through 2013 and before and after initiation of an SNR program on March 8, 2010.

Characteristic2006 (n = 10,732)2007 (n = 10,037)2008 (n = 10,932)2009 (n = 10,982)2010 (n = 9,768)2011 (n = 8,744)2012 (n = 8,213)2013 (n = 8,489)Before SNR program (n = 43,517)After SNR program (n = 34,380)
Intake type
  Confiscation21 (0.2)21 (0.2)32 (0.3)70 (0.6)29 (0.3)23 (0.3)52 (0.6)14 (0.2)145 (0.3)117 (0.3)
  Foster care108 (1.0)187 (1.9)231 (2.1)144 (1.3)12 (0.1)0 (0.0)0 (0.0)0 (0.0)677 (1.6)5 (0.0)
  Owner surrender388 (3.6)280 (2.8)321 (2.9)409 (3.7)298 (3.1)124 (1.4)330 (4.0)393 (4.6)1,434 (3.3)1,109 (3.2)
  Return to shelter57 (0.5)57 (0.6)37 (0.3)50 (0.5)39 (0.4)50 (0.6)44 (0.5)63 (0.7)212 (0.5)185 (0.5)
  Stray10,149 (94.6)9,491 (94.6)10,311 (94.3)10,309 (93.9)9,371 (95.9)8,528 (97.5)7,767 (94.6)7,962 (93.8)41,039 (94.3)32,849 (95.5)
  Transfer from another facility9 (0.1)1 (0.0)0 (0.0)0 (0.0)19 (0.2)19 (0.2)20 (0.2)57 (0.7)10 (0.0)115 (0.3)
Outcome type*
  Adoption1,372 (12.8)1,137 (11.3)1,187 (10.9)1,292 (11.8)1,376 (14.1)1,293 (14.8)1,222 (14.9)1,422 (16.8)5,126 (11.8)5,175 (15.1)
  Euthanasia7,392 (68.9)6,547 (65.2)7,189 (65.8)7,454 (67.9)4,309 (44.1)3,109 (35.6)2,654 (32.3)2,321 (27.4)28,976 (66.6)11,999 (34.9)
  Rescue1,519 (14.2)1,906 (19.0)2,126 (19.4)1,777 (16.2)2,616 (26.8)1,633 (18.7)1,798 (21.9)2,104 (24.8)7,583 (17.4)7,896 (23.0)
  Return to owner267 (2.5)274 (2.7)273 (2.5)350 (3.2)266 (2.7)188 (2.2)185 (2.3)169 (2.0)1,200 (2.8)772 (2.2)
  Transfer to another facility19 (0.2)8 (0.1)18 (0.2)22 (0.2)1,115 (11.4)2,441 (27.9)2,283 (27.8)2,374 (28.0)67 (0.2)8,213 (23.9)
  Other163 (1.5)165 (1.6)139 (1.3)87 (0.8)86 (0.9)80 (0.9)71 (0.9)92 (1.1)565 (1.3)318 (0.9)

Proportions changed significantly (P < 0.001; Mantel-Haenszel test) over the study period and differed significantly (P < 0.001; χ2 test) before and after the SNR program began.

Outcome type was not recorded for 7 cats.

Rescue included foster care, relocation, and rescue group.

Other included died, missing, requiring euthanasia, temporary, or to be determined.

Table 3—

Duration of stay, number vaccinated, number with a diagnosis of or treated for URI, and intervals from admission to FVRCP vaccination and URI diagnosis for kittens (< 4 months of age) and adult cats admitted to SJACC from 2006 through 2013 and before and after initiation of an SNR program on March 8, 2010.

Characteristic2006 (n = 10,732)2007 (n = 10,037)2008 (n = 10,932)2009 (n = 10,982)2010 (n = 9,768)2011 (n = 8,744)2012 (n = 8,213)2013 (n = 8,489)P value for temporal trendBefore SNR program (n = 43,517)After SNR program (n = 34,380)P value for 2-period comparison
Duration of shelter stay (d)            
  Kitten6 (1–495)7 (1–209)6 (1–129)6 (1–517)5 (1–267)5 (1–450)5 (1–113)5 (1–135)< 0.0016 (1–517)5 (1–450)< 0.001
  Adult8 (1–225)8 (1–335)7 (1–1049)7 (1–653)6 (1–425)6 (1–689)6 (1–217)6 (1–140)< 0.0018 (1–1,049)6 (1–689)< 0.001
  Vaccinated3,7863,7084,0584,1283,6903,2813,2053,269 I5,98613,139< 0.001
Interval from admission to FVRCP vaccination (d)            
  Overall1 (0–52)1 (0–39)2 (0–34)1 (0–48)1 (0–43)1 (0–60)1 (0–59)1 (0–92)< 0.0011 (0–52)1 (0–92)< 0.001
  Kitten1 (0–42)1 (0–39)1 (0–32)1 (0–48)1 (0–43)1 (0–60)1 (0–38)1 (0–68)< 0.0011 (0–48)1 (0–68)< 0.001
  Adult1 (0–52)2 (0–33)2 (0–34)2 (0–29)1 (0–38)1 (0–33)1 (0–59)1 (0–92)< 0.0012 (0–52)1 (0–92)< 0.001
URI diagnosis or treatment            
  Overall354590664734592557716516< 0.0012,3952,328< 0.001
  Kitten42192174259166261349308< 0.001679I, 072< 0.001
  Adult303388467455390277340I97< 0.001I, 6491,1680.27
Interval from admission to URI diagnosis or treatment (d)            
  Kitten5 (3–29)6 (0–138)11 (0–30)13 (0–50)4 (0–54)4 (0–39)3 (0–58)3 (0–93)< 0.0019 (0–138)3 (0–93)< 0.001
  Adult6 (0–17)8 (0–35)15 (0–65)16 (0–69)11 (0–194)12 (0–65)14 (0–67)4 (0–76)< 0.00113 (0–194)11 (0–158)< 0.001

Values for durations and intervals are median (range). Values for URI diagnosis or treatment are number of cats. Cats with missing ages were excluded from the analysis.

Stray cats

Of the 73,888 stray cats admitted to SJACC between 2006 and 2013, 40,078 (54.2%) were euthanized, and a significant (P < 0.001) decrease was evident in proportions of euthanized kittens and adult cats over that 8-year period (Figure 4). In the pre-SNR period, 69.0% (28,334/41,039) of all stray cats were euthanized, and in the post-SNR period, 35.8% (11,744/32,842) were euthanized (Figure 5). The number of stray cats designated at admission as sick or injured and subsequently euthanized was small, compared with the number of clinically and behaviorally normal cats. The proportion of euthanized stray cats that were sick or injured increased after the SNR program began (pre-SNR period, 13.5% [3,828/28,334]; post-SNR period, 42.3% [4,968/11,744]), whereas the proportion of euthanized stray cats designated at admission as feral remained at 2.0% after that point (pre-SNR period, 2.0% [564/28,334]; post-SNR period, 2.0% [239/11,744]). The proportion of euthanized stray cats with specific medical problems in the post-SNR period was more than 3 times as high as in the pre-SNR period (26.3% [3,087/11,744] vs 8.2% [2,327/28,334]). However, the proportion of euthanized stray cats with URI decreased from 10.5% (2,977/28,334) to 3.7% (436/11,744) after the SNR program began. In the pre-SNR period, 17.1% (6,999/41,039) of all stray cats were transferred to rescue organizations, compared with 22.4% (7,344/32,842) in the post-SNR period (P < 0.001). Over the 8-year study period, 11.7% (8,612/73,888) of all stray cats were adopted. In the pre-SNR period, 9.7% (3,981/41,039) of stray cats were adopted, compared with 14.1% (4,631/32,842) in the post-SNR period (P < 0.001).

Figure 4—
Figure 4—

Percentage of kittens (< 4 months of age; black bars) and adult cats (gray bars) that were euthanized after admission to SJACC from 2006 through 2013. Cats of unknown age were not included.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

Figure 5—
Figure 5—

Percentage of kittens (< 4 months of age) and adult cats admitted to SJACC before (January 1, 2006, to March 7, 2010) and after (March 8, 2010, to December 31, 2013) initiation of an SNR program by outcome. Cats of unknown age were not included. See Figure 4 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

SNR cats

The number of stray cats admitted to SJACC as feral ranged between 68 (0.7%) cats in 2007 and 617 (7.9%) cats in 2012. The proportion of feral stray cats admitted before the SNR program began was 1.5% (621/41,039), and that proportion increased 3.5-fold after the program began to 5.3% (1,739/32,849). A total of 8,086 stray cats were transferred to the rescue group Town Cats for return to points of capture or trapping for the SNR program after spending a median of 5 days at SJACC (range, 1 to 118 days); approximately 60% of the cats spent 5 days or less in the shelter. Sixty-eight (0.8%) of the cats transferred to Town Cats had a diagnosis of URI made by a veterinarian or were treated for URI during their shelter stay.

Cats received as nuisances or dead

Over the study period, 65 of 77,897 (0.1%) were reported as being a nuisance; 18 (27.7%) of these were admitted to the shelter before the SNR program began, and 47 (72.3%) were admitted afterward. One kitten and 19 adults of these 47 cats were transferred to Town Cats for the SNR program. Twelve of these 20 (60%) cats were reported as nuisances on their first admission to SJACC. Six (30%) cats were reported as nuisances on their second SJACC admission, and the remaining 2 (10%) were reported as such on their third admission.

Between the pre- and post-SNR periods, a small but significant decrease was evident in the proportion of dead cats received at SJACC. Since the start of the SNR program, 150 participating cats were returned as dead. No information on cause of death was available in the database.

URI

Over the 8-year study period, 62.6% (48,772/77,897) of cats had no FVRCP vaccination date recorded or did not receive FVRCP vaccination. In the pre-SNR period, 63.3% (27,531/43,517) of cats did not have a recorded date of FVRCP vaccination; this was similar in the post-SNR period (61.8%; 21,241/34,380; Table 3). Except for in 2006 and 2008, more kittens than adult cats were euthanized because of clinical signs of URI. Over the 8-year period, 6.2% (4,695/75,535) of all cats representing 6.1% (4,723/77,897) of all shelter admissions received a diagnosis of URI by a shelter veterinarian or were treated for URI during their shelter stays as recorded in the database text fields. Before the SNR program started, 5.5% (2,395/43,517) of cats received a diagnosis of URI or were treated for URI during the stay, compared with 6.8% (2,328/34,380) in the post-SNR period (P < 0.001). Although the number of cats euthanized because of URI decreased over the study period, the number of cats with URI (diagnosis or treatment) did not change significantly (Figures 6 and 7). Over the 8-year study period, of 3,638 cats that were euthanized because of clinical signs of URI, only 591 (16.2%) received a diagnosis of URI or were treated for URI while in the shelter. During that period, 1,004/4,723 (21.3%) cats with URI (diagnosis or treatment) were euthanized. Seventy-one (1.5%) cats with URI became participants in the SNR program. Until 2012, more adults than kittens were identified by veterinary staff as having a URI or described as having been treated for URI (Table 3). In the pre-SNR period, 2.9% (679/23,657) of kittens and 9.6% (1,649/17,233) of adult cats received a URI diagnosis or were treated for URI during their shelter stays, compared with 5.5% (1,072/19,452) of kittens and 9.2% (1,168/12,706) of adult cats in the post-SNR period.

Figure 6—
Figure 6—

Number of cats that were euthanized because of URI (black bars) and number with a diagnosis of or treated for URI (gray bars) after admission to SJACC from 2006 through 2013.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

Figure 7—
Figure 7—

Percentage of kittens (< 4 months of age) and adult cats admitted to SJACC before (January 1, 2006, to March 7, 2010) and after (March 8, 2010, to December 31, 2013) initiation of an SNR program by whether they were euthanized because of URI or had a diagnosis of or were treated for URI after admission. Cats of unknown age were not included. See Figure 4 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.298

Records for 4.5% (3,518/77,897) cats admitted during the 8-year period included the date on which a veterinarian had made the URI diagnosis. Records for an additional 1.6% (1,205) of cats indicated that those cats had been treated for a URI by the end of their shelter stays, but no initial diagnosis or treatment date was recorded. For cats with a date corresponding to the onset of URI signs, the interval from shelter admission until sign onset was significantly (P < 0.001) shorter for kittens than for adult cats throughout the 8-year period, and in both the pre- and post-SNR periods (P < 0.001; Table 3). In addition, median duration of shelter stay was significantly longer in the pre-SNR period than in the post-SNR period for both kittens and cats with URI.

Risk factors for URI

In univariate analysis, every additional day in the shelter increased the risk of URI diagnosis or treatment by 6.5% (OR, 1.065; 95% CI, 1.064 to 1.067; P < 0.001). Kittens were 59% less likely than adults to have been diagnosed with or treated for URI (OR, 0.41; 95% CI, 0.38 to 0.43; P < 0.001). The risk of URI did not differ between female and male cats (P = 0.07). However, the risk of URI was 24% higher in the post-SNR period than in the pre-SNR period (OR, 1.24; 95% CI, 1.17 to 1.32; P < 0.001). Furthermore, the risk of URI was 21-fold greater for cats that received the FVRCP vaccine than for unvaccinated cats (OR, 21.14; 95% CI, 18.98 to 23.55; P < 0.001).

Results of multivariable regression indicated that the risk of URI diagnosis or treatment increased by 5% for each additional day cats stayed in the shelter (OR, 1.048; 95%, CI 1.046 to 1.050; P < 0.001), controlling for other factors. Kittens were 44% less likely than adult cats (OR, 0.56; 95% CI, 0.52 to 0.61; P < 0.001) and female cats were 10% less likely than male cats (OR, 0.90; 95% CI, 0.84 to 0.97; P = 0.006) to have been diagnosed with or treated for URI. Vaccination against FVRCP, compared with lack of vaccination, increased the risk of URI > 8-fold (OR, 8.38; 95% CI, 7.31 to 9.60; P < 0.001). The risk of URI was 10% higher in the post-SNR period than in the pre-SNR period (OR, 1.09; 95% CI, 1.02 to 1.18; P = 0.015). Significant interactions were identified between duration of shelter stay and vaccination and among duration of shelter stay, vaccination, and SNR period (pre- vs post-SNR); interactions between vaccination and SNR period and between duration of shelter stay and SNR period were not significant. When all these interaction terms were included in the multivariable model, the association between SNR period and URI was no longer significant.

Because of the significant interaction terms and because duration of shelter stay differed between FVRCP-vaccinated and unvaccinated cats, which shifted with the start of the SNR program, a stratified analysis was performed on the basis of vaccination status. In the pre-SNR period, the risk of an unvaccinated cat having been diagnosed with or treated for URI increased by 1% for each additional day in the shelter (OR, 1.013; 95% CI, 1.006 to 1.019; P < 0.001), controlling for other factors. Kittens were approximately 50% less likely than adult cats to have been diagnosed with or treated for URI (OR, 0.49; 95% CI, 0.30 to 0.81; P = 0.006). Unvaccinated kittens in the post-SNR period had a 54% increase in the risk of URI diagnosis or treatment, compared with the risk for adult cats (OR, 1.54; 95% CI, 1.15 to 2.07; P = 0.004), controlling for other factors. Each additional day in the shelter increased the risk of URI by 3% (OR, 1.03; 95% CI, 1.02 to 1.04; P < 0.001) for any unvaccinated cat.

Vaccinated kittens before the SNR program were 59% less likely than adult cats to have been diagnosed with or treated for URI (OR, 0.41; 95% CI, 0.36 to 0.46; P < 0.001). Each additional day in the shelter increased the risk of URI by 5% (OR, 1.054; 95% CI, 1.051 to 1.057; P < 0.001) for all vaccinated cats. In the post-SNR period, vaccinated kittens were 30% less likely to be diagnosed with or treated for URI than were adult cats (OR, 0.72; 95% CI, 0.64 to 0.80; P < 0.001), controlling for other factors. Each additional day in the shelter increased the risk of URI by 5% (OR, 1.048; 95% CI, 1.045 to 1.051; P < 0.001) for all vaccinated cats in this period. Female cats were 15% less likely than male cats to have URI (OR, 0.85; 95% CI, 0.76 to 0.94; P = 0.003).

Cost analysis for URI

Prior to 2010, all cats identified as having URI were treated with ophthalmic ointment and orally administered antibiotics and were moved to an isolation ward. None received ophthalmic ointment after 2010, when the cost for that medication became prohibitive; ocular discharge was wiped away as needed. After a change in treatment protocol was initiated in 2011, approximately 10% to 20% of cats with URI were treated by oral administration of antimicrobials, unless they had clinical signs of secondary bacterial infection. The estimated mean amount of time spent by shelter veterinarians in examining cats with URI once those cats had been isolated was between 10 and 20 min/d for the 8-year period. Veterinary technicians spent a total of approximately 1 h/d administering medications to cats in isolation for a URI prior to 2011; after the protocol change, this decreased to approximately 15 min/d.

In the winter, a mean of 2 cats was housed in the isolation ward for URI at any given time each year. Total estimated costs to treat 2 cats in the winter, including estimated costs for orally administered antimicrobials and topically administered ophthalmic ointment, ranged between $45.00 and $57.35/d. On a per-cat basis, individual costs were $0.20 for the antimicrobials, $9.80 for the ophthalmic medication (lasting > 1 day), and $12.50 to $18.68 for veterinary staff. On average, 60 cats were treated for URI in the summer each year. Because veterinary staff costs were based on time spent treating all cats with URI, on a per-cat basis, the cost of medication remained $10, and veterinary staff costs were < $1.00 per day, with resulting total daily costs ranging from $625.00 to $637.35.

Costs decreased considerably when only 10% to 20% of cats with URI received orally administered antimicrobials and no ophthalmic ointment was used. Estimated daily costs to treat 1 of 2 cats in the winter were approximately $0.27 for the antimicrobials and $5.60 to $10.43 for veterinary staff, yielding a total of $11.47 to $21.12/d for 2 cats. Estimated daily costs to treat a cat in the summer were $0.27 for the antimicrobials and < $0.50/d for veterinary staff, so to treat 9 of the 60 cats with URI would result in a total daily cost of $13.63 to $23.28.

Discussion

The present study, involving cat admissions to a large municipal animal shelter over an 8-year period that encompassed the start of an SNR program (March 8, 2010), revealed that fewer cats were admitted (alive or dead) after the program began than were admitted previously. More kittens than adult cats were admitted for each of the 8 years, and implementation of the SNR program had no effect on this finding. A similar admission pattern has been reported for other shelters, including those in Santa Clara and a neighboring county,15 and for some TNR programs, such as at a college campus in Florida.10 In a study19 involving animal shelters in an area previously associated with a large number of cat admissions, admission characteristics were monitored for 2 years after implementation of an intensive public information campaign about an existing TNR program.19 In that targeted area for the specified period, more gonadectomies were performed and fewer cats were impounded or euthanized than in the rest of the county.19 The related public education activities, including encouraging adoptions of socialized cats and enhanced conflict resolution for nuisance cats, were credited with contributing to decreases in shelter admission and euthanasia rates.19

In the present study, more cats were adopted or transferred to rescue organizations from SJACC in 2013 than in 2006, and the proportion of cats that were euthanized decreased from nearly 70% in 2006 to < 30% in 2013. Interestingly, a decrease in the number of cats admitted to other Santa Clara County shelters was also noted during this period, perhaps in response to a municipal spay-neuter voucher program that was in place before the present study began, an increase in public education efforts, or the start of SNR programs at 2 smaller shelters.16 These findings represented a similar improvement in cat population control to that described for Florida,19 only on a larger scale.

The proportion of cats involved in the SNR program in the present study remained fairly stable during the period evaluated. Few cats in the SNR program were returned to the shelter as dead, and even fewer were returned as nuisances. In general, cats deemed as nuisances that were retrapped were released immediately by animal control officers rather than taken back to the shelter, unless there was a concurrent welfare concern, such as illness or malnutrition. Rereleased cats did not enter the shelter system, so their numbers could not be tracked. A valuable next step in evaluating the success of the SNR program would be to monitor the health and welfare of the cats after release.

The proportion of cats admitted to SJACC that were recorded as feral did not decrease after the SNR program began. This classification of cats as feral had been made at admission and was not based on behavioral assessment but rather on their initial appearances, with the purpose of identifying obvious medical concerns for the veterinary department. Starting in 2010, greater attention was paid at intake to the condition of admitted cats, leading to a decrease in the proportion of cats classified as clinically and behaviorally normal and an increase in the proportion classified as feral or having medical or other issues. Classification of cats as unsocialized or feral was not made until after the behavioral assessment, typically after cats had spent 2 days in the shelter. After the SNR program began, 24.6% of stray cats participated in the program, whereas only 5.3% of stray cats were initially characterized as feral on admission. With improved reporting practices by shelter staff members, cats’ conditions on admission have been more appropriately described.

The decrease in cat admissions to SJACC in the present study corresponded to the start of the SNR program. Between 2010 and 2013, the human population in the SJACC service area (ie, Cupertino, Los Gatos, Milpitas, San Jose, and Saratoga, Calif)20 increased by 5.3% and the adjusted total number21,22 of cats admitted to SJACC decreased by 13.1%.23 Although not all cats admitted to SJACC were from this service area, an approximate estimate of per capita adjusted total number of cat admissions decreased from 8.78 admissions/1,000 people to 7.25 admissions/1,000 people, representing a 17.4% decrease. Incorporation of data on the number of cat euthanasias performed in 2010 and 2013 (4,309 and 2,312, respectively) yielded a 49.1% decrease in the number of cats euthanized per 1,000 people, from 3.81 cats/1,000 people to 1.94 cats/1,000 people. Whether this decrease was attributable to the start of the SNR program was unclear because decreases in cat populations were observed for other Santa Clara County shelters and rescue groups during this period as well. After the SNR program began at SJACC, similar programs were initiated at 2 of the other 4 Santa Clara County shelters (one in 2010 and the other in 2013).16

Given the large number of cats admitted to SJACC over the study period (twice as many as those admitted at the other 4 Santa Clara County shelters combined), we believe the decrease in the number of cat admissions at SJACC was the result of its programmatic changes. The explanation for this decrease was probably multifactorial and could have included an improving economy in the area, the changes in SJACC protocols regarding URI treatment and euthanasia, implementation of the SNR program, implementation of other TNR programs, and internal and external factors that were not identified. It is possible that, because efforts were made to educate the general public about the SNR program, some cats that would otherwise have been brought to SJACC were no longer trapped. Other cats in the SJACC service area may have been cared for by active caretakers of feral cat colonies, who may have taken cats to any participating spay-neuter clinic for services, without bringing them to the shelter. The number of stray cats that might have been handled in this manner was not estimated in the present study. Consequently, it may be difficult to discern the true extent to which the number of feral cats in the SJACC service area decreased during the study period.

After the SNR program began in the present study, fewer cats were admitted to the shelter, but the duration of stay did not change because a goal of the program was to return free-roaming cats to their original sites as quickly as possible. Each additional day in the shelter increased the risk of URI diagnosis or treatment by 3% for unvaccinated cats and approximately 5% for vaccinated cats, as reported previously.24 This increased risk for vaccinated cats may appear counterintuitive. However, because cats in the present study were vaccinated several days after admission rather than immediately, they may have had a greater opportunity to become infected with 1 of several upper respiratory pathogens or to develop clinical signs of URI from infections acquired before vaccination. Additionally, cats that were considered unadoptable because of age or medical or behavioral conditions were not vaccinated but rather were euthanized after several days in the shelter; those cats were not treated for URI. Consequently, few unvaccinated cats received a diagnosis of or treatment for URI.

The apparent increase in the risk of URI for vaccinated versus unvaccinated cats should not be interpreted as suggesting that vaccination increased the risk of acquiring URI; instead, the presence of the unvaccinated cats in the shelter for several days likely contributed to the potential pathogen population and not to the count of cats with URI. The finding that, after the SNR program began, female cats were at a lower risk than male cats of having a URI diagnosis or treatment was not expected; examination of the distribution of female and male vaccinated kittens during this period revealed a significant (P = 0.01) difference that likely explained this finding.

Upper respiratory tract infections are among the most common health concerns for cats in animal shelters.25–27 In the present study, patterns of vaccination and treatment for URI were examined because changes in the URI treatment protocol occurred at approximately the same point that the SNR program began. A shift in shelter policy that provided additional resources to treat cats with URI instead of euthanizing them occurred contemporaneously with implementation of the SNR program as well. During the study period, shelter staff did not vaccinate all cats against FVRCP within 24 hours after admission as recommended in published standards of care for animal shelters17 and by the American Association of Feline Practitioners.18 Rather, at SJACC, cats > 4 weeks of age were vaccinated after successful completion of a behavioral assessment.

In cats at SJACC, URI has been controlled through improvements in environmental cleaning protocols, avoidance of moving cats from their cages on a daily basis, and, before 2010, euthanasia of cats with suspected URI. Isolation of cats on the basis of clinical signs was insufficient for control of URI in a study28 involving 4 types of cat housing environments: animal shelters, sanctuaries, foster programs, and TNR programs. Various pathogens were identified in most of those cats, regardless of clinical signs, suggesting that isolation of clinically ill cats alone would not be sufficient to control URI in shelters. Investigators in that study28 recommended that cats be vaccinated before or at admission; however, because many cats in the shelters, sanctuaries, and foster programs had been vaccinated previously, this was identified as only 1 component of a disease control strategy that should also include proper hygiene and reduction in stressful conditions, such as high-density housing.28

The decrease in cat admissions in the post-SNR period in the present study and resultant increase in resource availability may have contributed to the increase in the proportion of cats with URI that were treated rather than euthanized. The proportion of euthanized stray cats identified with URI on admission decreased more than 3-fold after the SNR program began, and more cats received a URI diagnosis or treatment. It is unlikely that the prevalence of URI increased after the SNR program began; rather, it is more likely that the presence of URI was historically underreported when kittens and other stray cats were admitted and then euthanized. The increase in availability of shelter space also made it possible to treat kittens with URI rather than euthanize them. Before the shift in policy, kittens with URI were euthanized, so only adults were in the shelter long enough to develop URI and receive treatment for it. Additionally, veterinary staff had more time available to examine cats with clinical signs sooner after admission and move them to isolation wards sooner for treatment. The overall result was an improvement in the degree of care cats received and a fewer number of cats identified with or treated for URI after admission than the number of cats euthanized for URI.

The cost of medications used to treat URI before 2010 in the present study was similar to a previously reported estimate of $10/d.24 The actual cost of treating cats for URI should include the staff costs, which were available for total cost estimation. With the change in treatment policy, considerably less money was spent on each cat with URI. In addition to cost savings, the policy shift resulted in a change in the amount of time required to handle and treat each cat with URI and the potential negative impact of such handling on each cat and its subsequent behavior when interacting with shelter staff and potential adopters. This protocol change also addressed concerns regarding inappropriate treatment of virally infected cats with antimicrobials, which is a situation that could lead to antimicrobial resistance of bacterial organisms.

Limitations of the study reported here included those inherent in the use of historical records for research purposes. Incomplete or inaccurate information was available for the cats admitted to the shelter, including missing entries for age, sex, and dates of URI treatment. Less than 10% of cats had missing age information, but sex information was missing for approximately half of the cats until reporting improved later in the study period. Because the shelter record-keeping system was not designed for research purposes, dates of URI diagnosis and ages of cats, particularly of kittens, needed to be extrapolated. Of more concern to the URI analysis were the missing dates of FVRCP vaccination for 62.6% of the cats in the shelter, although this was apparently in keeping with the shelter's policy of not vaccinating cats on entry. According to the SJACC operations manager,f the apparent increase in the number of dead cats received by the shelter in 2013 reflected improved record keeping by staff members. Misclassification may have occurred in identifying nuisance SNR cats. Records with missing observations were excluded from the regression models; therefore, an assumption was made that records without missing information were representative of the entire population, which may not have been true. However, there was no reason to believe that cats with missing data would be different from cats with complete data, so any bias introduced by missing data would have been nondifferential.

A strength of the study was that many years of data were available, providing a large sample size. However, even with correction for multiple comparisons, because of the size of the data set, significant associations were likely to have been identified simply by random chance alone. Furthermore, not all homeless cats in the communities served by SJACC were admitted to this particular shelter. People may have chosen not to bring cats to the shelter if they had other options or concerns about the eventual fate of admitted cats. Therefore, the data analysis may have provided an incomplete description of the population served by SJACC.

Critics of SNR programs cite public health concerns regarding human interactions with feral cats, including the potential for transmission of rabies between raccoons and cats.29 However, in California, bats are the primary species that harbor and transmit rabies30 and there was a decrease in the incidence of animal rabies infection from 2001 through 2012.31 Cats in California have not historically posed a rabies threat to the human population and are not required by law to be vaccinated against rabies.32 Nevertheless, because of concerns from the public regarding the potential for rabies transmission by stray cats, the City of San Jose vaccinates SNR cats against rabies.

In conjunction with other changes at SJACC during the study period, the SNR program appeared to have contributed to the significant decrease in cat admissions. Such findings are important for assessing the benefit of similar programs and determining the exact relationship between the program and admission rates.

Acknowledgments

Supported by the Research and Development Department of the American Society for the Prevention of Cruelty to Animals through City of San Jose Animal Care and Services.

The authors thank Gwen Herron-Moon and Rick Nelson for assistance with manuscript preparation.

ABBREVIATIONS

CI

Confidence interval

FVRCP

Feline rhinotracheitis virus, feline calicivirus, and feline panleukopenia virus

SJACC

San Jose Animal Care Center

SNR

Shelter-neuter-return

TNR

Trap-neuter-release

URI

Upper respiratory tract infection

Footnotes

a.

Chameleon/CMS via Crystal Reports (SAP), HLP Inc, Littleton, Colo.

b.

Microsoft Excel, version 14, Microsoft Corp, Redmond, Wash.

c.

SAS, version 9.4, SAS Institute Inc, Cary, NC.

d.

IBM SPSS Statistic, version 20, SPSS Inc, Chicago, Ill.

e.

Epi Info, version 7, CDC, Atlanta, Ga.

f.

Dains S, San Jose Animal Care and Services, San Jose, Calif: Personal communication, 2014.

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Contributor Notes

Address correspondence to Dr. Edinboro (cedinboro@exponent.com).