Although widespread vaccination of pet cats has made FPV infection an uncommon diagnosis at present, animal shelters continue to report large-scale outbreaks of FPV.1–10 Feline panleukopenia virus is a highly contagious parvovirus of cats that is fatal in 50% to 90% of untreated cats and is the most frequent cause of death in cats in animal shelters.11–13 The intensive housing of cats in shelters and durability of the virus contribute to rapid spread of FPV within susceptible cat populations. Outbreaks commonly occur in the summer and fall following a large influx of kittens born in the spring that are admitted to shelters at an age when maternal immunity is waning.10 Kittens are understood to be the most susceptible to FPV infection, but shelter outbreaks may also involve adult cats. Because the incubation period after exposure is 2 to 14 days, apparently healthy cats may leave the shelter for adoption or fostering, only to succumb to infection in their new homes. Institutional responses to outbreaks frequently include temporary closure to new cat admissions or depopulation of entire cat populations, even those without evidence of infection.1–10
The primary route of FPV transmission is fecal-oral contamination. After infection, FPV primarily infects rapidly dividing cells of the bone marrow, lymphoid system, and intestinal mucosa, resulting in severe panleukopenia, vomiting, diarrhea, hypovolemic shock, sepsis, and death. Less commonly, a peracute syndrome occurs in which cats become moribund and die within hours, without manifesting typical gastrointestinal signs. Subclinical disease in partially resistant cats may be accompanied by modest leukopenia in the absence of obvious clinical signs. Kittens infected in utero near term or in the early postnatal period may have viral replication in the granular layer of the cerebellum, causing permanent cerebellar dysfunction and ataxia. Early in utero infection often results in fetal death. High concentrations of FPV may be shed in feces prior to the onset of clinical signs and for several weeks after recovery, although shedding is limited to a 5- to 7-day period in most instances. Feline panleukopenia virus is extremely resistant to inactivation, with most disinfectants other than sodium hypochlorite, potassium peroxymonosulfate, formaldehyde, and glutaraldehyde having little effect on the virus. Infectious viral particles can survive in the environment for longer than 1 year.14–17
Point-of-care fecal antigen test kits are available to confirm parvovirus infection in dogs within a few minutes, allowing rapid identification and isolation of dogs that are shedding parvovirus in feces.18 These canine parvovirus tests also detect FPV antigen in cat feces, although this is not a licensed use and the sensitivity and specificity of these tests in cats have not been reported.19–22 Other laboratory-based diagnostic tests, including virus isolation, PCR assays, and seroconversion, may be more accurate for parvovirus detection, but rapid-assay point-of-care tests are more practical and cost-effective for quick screening of animals in the shelter setting. Thus, although canine parvovirus tests are not validated for use in cats, they are commonly used in this species by shelter veterinarians.
Highly effective inactivated and MLV vaccines are available for immunization against FPV.23–25 Modifiedlive virus vaccines offer rapid-onset protection, which is essential for preventing FPV transmission in shelters. In seronegative cats, primary immunization against FPV with MLV vaccines results in detectable serum antibodies in 5 to 7 days, but confers protection against infection even earlier. In 1 study,26 susceptible kittens could be safely housed in a contaminated environment immediately after vaccination, and full protection against highly virulent challenge was reached by 72 hours after vaccination. In contrast, use of inactivated vaccines results in a slower immune response, often requiring several weeks before protective serum antibody titers are reached.24 Immunization is less effective in kittens with passively acquired maternal antibodies against FPV. Vaccine interference by those antibodies has been detected up to 19 weeks of age.19,27,28
The high number of susceptible cats housed in shelters, durability and high transmission rates of FPV, and high fatality rates among infected cats mandate the use of vigorous preventive measures to protect the health of cats in shelters. Preventive health guidelines for shelters now urge immunization with MLV FPV vaccines immediately upon cats' admission to the shelter.23–25 Vaccination of all cats, regardless of their potential for eventual adoption, is recommended to improve the resistance of the entire shelter population and to reduce environmental contamination by FPV.
Vaccination of all cats and dogs immediately upon admission to a shelter reduces both the number and severity of feline and canine parvovirus outbreaks in shelters.13,23 However, in dogs, it is believed that parvovirus vaccination sometimes results in transient fecal shedding of vaccine antigens that cannot be distinguished from natural infection with diagnostic test kits.18 If this is also true for cats, recently vaccinated cats might have falsepositive test results with fecal parvovirus antigen tests, thus complicating the ability of shelter personnel to test and segregate infected populations. Although this would be true for cats at all types of facilities, it is especially problematic at shelters where large numbers of cats are likely to be both recently vaccinated and manifesting clinical signs such as vomiting and diarrhea, which may or may not be a result of FPV infection.
The purpose of the present study was to determine the frequency and duration of vaccine-induced interference with fecal parvovirus antigen tests in cats by use of 8 commercially available vaccines and 3 canine parvovirus tests.
Materials and Methods
Cats—Eleven SPF queens and their 64 kittens were enrolled in the study. Seven of the queens had previously been vaccinated against FPV and were seropositive for antibodies against FPV. Four of the queens were unvaccinated and were seronegative for anti-FPV antibodies. Because passively acquired anti-FPV antibodies inhibit replication of FPV and subsequent fecal antigen shedding, an effort was made to minimize transfer of maternal FPV antibodies to kittens. To optimize the chance of detecting FPV vaccine–derived antigens in feces, kittens of vaccinated queens were colostrum deprived so that they would have negligible serum titers of anti-FPV antibodies at the time of vaccination. Kittens born to seronegative queens were allowed to nurse normally. Kittens were randomly allocated into 8 groups of 8 kittens each when they were 8 to 10 weeks old such that littermates were distributed among the groups and each group contained 4 males and 4 females. Kittens were housed individually, and staff wore barrier gowns, booties, and gloves beginning the day before vaccination (day −1) to prevent cross-contamination with vaccine viruses. All kittens remained healthy during the study and were seronegative for FeLV antigen and FIV antibodies when tested by means of an ELISA.a The research protocol was approved by the University of Florida Institutional Animal Care and Use Committee and was conducted in facilities accredited by the Association for Assessment and Accreditation of Laboratory Animal Care. Kittens were adopted into private homes at the conclusion of the study.
Vaccination—Eight multivalent vaccines for FPV, feline herpesvirus-1, and feline calicivirus were selected for testing. The vaccines included 5 parenterally administered MLV vaccines, 1 parenterally administered inactivated vaccine, 1 parenterally administered vaccine in which the FPV was inactivated and the herpesvirus-1 and calicivirus were MLVs, and 1 mucosally administered MLV vaccine.b-i Vaccines were administered SC in the left hind limb or intranasally as recommended by the manufacturers.
FPV antibody titers—Blood was collected via jugular venipuncture for determination of anti-FPV antibody titers immediately prior to vaccine administration (day 0) and again 14 days later (day 14). Blood was placed in serum separator tubes, allowed to clot for a minimum of 30 minutes, and centrifuged for 10 minutes. Serum was stored at −20°C pending analysis. End point anti-FPV antibody titers were determined via hemagglutination inhibition by use of 2-fold serum dilutions starting at 1:10.j A titer of 1:40 was considered to be protective against infection.29
Parvovirus antigen testing—Fecal samples were collected once daily from the litter box of each kitten for 15 days beginning immediately prior to administration of the vaccines. If there were no feces in the litter box, samples were collected by use of rectal swabs. Immediately after collection, each fecal sample was tested for parvovirus antigen with each of 3 canine parvovirus point-of-care test kitsk-m according to manufacturers' instructions. Each test kit was also used to test feces from a cat with confirmed FPV infection. Finally, the ability of the test kits to detect the FPV antigen contained in the vaccines was determined by use of swabs soaked in each of the vaccines.
Statistical analysis—The proportions of positive parvovirus antigen test results for each of the 3 test kits, for each individual vaccine, for vaccines grouped by inactivated versus MLV FPV, and for vaccines grouped by parenteral versus mucosal administration were calculated and compared by use of the Fisher exact test. Mean FPV antibody titers for each vaccine group, vaccines grouped by inactivated versus MLV, and vaccines grouped by parenteral versus mucosal administration were calculated and compared by use of the Kruskal-Wallis analysis of variance on ranks test. The magnitudes of FPV antibody titers prior to and 14 days after vaccination were correlated with the occurrence of positive test results and compared with the Spearman rank order test. Values of P < 0.05 were considered significant.
Results
All 3 fecal parvovirus tests yielded strong positive results when feces from a confirmed FPV-infected cat were tested. Results when vaccines were used as the test samples varied. Test 1 yielded positive results with vaccines 1, 2, 3, 6, 7, and 8. Test 2 yielded positive results with vaccines 1, 2, 6, 7, and 8. Test 3 yielded no positive reactions when vaccines were used as test samples.
Fecal parvovirus antigen testing—All kittens had negative results of fecal parvovirus antigen tests prior to vaccination. When all test results were considered, 13 kittens (20%) had at least 1 positive test result (Table 1). Only 1 kitten had positive test results with all 3 tests, and 3 kittens had positive results with 2 of 3 tests. Individual kittens had positive test results on 1 to 8 testing days with occasional negative test days in between the positives. Test 1k yielded a positive result in 1 kitten for 4 consecutive test days (from day 7 through day 10); this kitten had received vaccine 5. Test 2l yielded a positive result in 4 kittens for a total of 8 kitten test days (from day 7 through day 14); positive results occurred in kittens that received vaccines 1, 2, and 5 (2 kittens). Test 3m yielded at least 1 positive test result in 13 kittens for a total of 24 kitten test days (from day 1 through day 14); positive results occurred with each vaccine except vaccine 8. One kitten that received vaccine 1 and was evaluated with test 3 had 8 days of positive test results interspersed with 4 days of negative test results, from day 3 to day 14. The proportion of positive test results was significantly greater for test 3 for both number of kittens (P < 0.02) and number of days with positive test results (P < 0.004), compared with test 1 or test 2. Test 1 and test 2 were not significantly different (P = 0.1). Of the 36 individual positive test results, only 2 (from the same kitten) were subjectively considered to be strongly positive. This occurred with test 3 in a kitten that received vaccine 1 (an inactivated vaccine). There were no significant differences in the proportion of kittens with positive test results between vaccine groups.
Serum antibody responses and results of fecal parvovirus antigen testing in 64 kittens that received 1 of 8 FPV vaccines. Feces were tested with 3 fecal canine parvovirus antigen test kits immediately prior to vaccination and daily for 14 days after vaccination. Serum anti-FPV antibody titers were measured immediately prior to vaccination and 14 days later and are expressed as mean ± SD. Titers ≥ 1:40 were considered protective.
Vaccine Group | Vaccine type | Administration route | FPV antibody titer (pre) | FPV antibody titer (post*) | Percentage protective titers (pre) | Percentage protective titers (post*) | No. kittens (No. kitten test days) with positive results for FPV on fecal tests | ||
---|---|---|---|---|---|---|---|---|---|
Test 1k | Test 2l | Test 3m† | |||||||
1b | IA | SC | 4 ± 5 | 36 ± 28 | 0 | 38 | 0 | 1(1) | 3(10) |
2c | IA | SC | 1 ± 4 | 19 ± 15 | 0 | 25 | 0 | 1(2) | 1(1) |
3d | MLV | SC | 1 ± 4 | 1,760 ± 2,130 | 0 | 75 | 0 | 0 | 2(3) |
4e | MLV | SC | 1 ± 4 | 1,760 ± 1,481 | 0 | 100 | 0 | 0 | 1(1) |
5f | MLV | SC | 4 ± 5 | 1,390 ± 1,733 | 0 | 88 | 1(4) | 2(5) | 3(5) |
6g | MLV | SC | 1 ± 4 | 580 ± 483 | 0 | 88 | 0 | 0 | 1(1) |
7h | MLV | SC | 1 ± 4 | 1,060 ± 807 | 0 | 88 | 0 | 0 | 2(3) |
8i | MLV | IN | 0 ± 0 | 1,040 ± 1,023 | 0 | 75 | 0 | 0 | 0 |
Serum anti-FPV titers and proportion of kittens with protective titers were significantly(P < 0.001) higher 14 days after vaccination in kittens that received MLV vaccines, compared with those in kittens that received IA vaccines. †Proportions of positive test results were significantly(P = 0.02) greater for test 3 than for tests 1 or 2.
IA = Inactivated. IN = Intranasal. Pre = Before vaccination. Post = 14 days after vaccination.
FPV antibody titers—None of the kittens had protective serum antibody titers against FPV prior to vaccination. Eleven kittens (17%) had a low titer of 1:10; these kittens were evenly distributed among the vaccine groups. The remaining kittens were seronegative at the time of vaccination. At 14 days after vaccination, 31% (5/16) of kittens receiving inactivated vaccines had protective titers, whereas 85% (41/48) of kittens receiving MLV vaccines had protective titers (P < 0.001; Table 1). In all 7 of the kittens that failed to develop protective titers after receiving MLV vaccines, test results for serum antibodies were negative both prior to and after vaccination. Mean titers 14 days after vaccination were significantly (P < 0.001) lower in the kittens that received inactivated vaccines (mean ± SD titer, 28 ± 24) than those in kittens that received MLV vaccines (1,265 ± 1,385). The proportion of kittens protected by the mucosally administered MLV vaccine (75% [6/8]) was not significantly different than the proportion of kittens protected by the 5 parenterally administered MLV vaccines (88% [35/40]; P = 0.4). Additionally, mean titers in kittens that received the mucosally administered vaccine (1,040 ± 1,023) were not significantly different than those in kittens that received the parenterally administered MLV vaccines (1,310 ± 1,453; P = 0.7). None of the vaccines induced mean titers consistently higher than those induced by all other vaccines. Response to vaccination as reflected by increase in titer had no effect (P > 0.05) on fecal parvovirus antigen detection.
Discussion
All 3 tests intended for diagnosis of canine parvovirus had strongly positive reactions with feces from a cat with confirmed FPV infection. When these tests were used with feces from recently vaccinated kittens, positive results were occasionally observed, and the frequency of this occurrence varied significantly among the 3 tests. Results were usually weak positives, but 1 kitten had strong positive results with 1 test on 2 of 8 days with positive test results. The reason for the significant differences in the number of positive test results obtained with the 3 different tests is not known, but is likely related to differences in sensitivity (ability of the tests to detect FPV antigens) or specificity (ability of the tests to avoid false-positive results).
A possible explanation for FPV antigen detection in feces after vaccination is replication of live vaccine viruses in lymphoid tissues or intestinal epithelial cells and subsequent shedding of antigens in the feces. However, an unexpected finding was positive antigen test results from 2 of the 3 test brands after administration of inactivated virus vaccines, which do not contain live viruses capable of replication. Although kittens were isolated and barrier procedures were used, it is possible that inadvertent transmission of live vaccine virus occurred, leading to shedding of antigens in kittens in the inactivated virus vaccine group. However, if kittens in the inactivated group were contaminated with MLV vaccine virus, higher serum antibody titers would be expected. The more likely explanation is that falsepositive reactions occurred with 2 of the tests, which could have occurred in both the inactivated and MLV vaccine groups.
There was a marked difference in the immune responses of kittens to inactivated versus MLV vaccines at 2 weeks after vaccination. Although both types of vaccines are capable of inducing solid, long-lasting immunity,29–31 MLV vaccines administered parenterally or mucosally are clearly superior to inactivated vaccines when a rapid protective response is required, as is true in shelters.
Results of the present study in SPF kittens may not be completely representative of cats tested in shelters, where higher or lower rates of vaccine interference with parvovirus testing may be observed. The kittens in this study were selected for their negligible FPV antibody titers. This was intended to give MLV vaccines the maximum opportunity for replication and antigen shedding to determine whether vaccination interferes with testing. In contrast, cats in shelters are admitted with a wide range of naturally occurring serum antibody titers that may interfere with vaccine virus replication, which suggests that the frequency of test interference in shelters may be lower than that observed in this study.28 On the other hand, the stress of a sudden change to unfamiliar and crowded surroundings,32–34 possible preexisting debilitating conditions, and concurrent infections may suppress immune function and allow for enhanced replication of the modified-live (attenuated) vaccine viruses.35–43 Germfree cats have significantly lower rates of clinical disease and microscopic intestinal lesions after experimental FPV infection than SPF cats do.15,16 This is believed to be a result of a slower rate of epithelial cell division in the unstimulated sterile intestines of germfree cats than the rate in the bacteriacolonized intestines of conventional SPF cats. Because FPV preferentially replicates in rapidly dividing cells, concurrent enteric infectious diseases commonly found in cats in shelters may provide increased capacity for FPV vaccine virus replication.30 In this situation, cats in shelters may have higher rates of test interference than the SPF kittens of the present report.
Vaccination of healthy kittens against FPV was associated with positive fecal parvovirus antigen test results, and the frequency of this vaccine interference varied among the 3 tests that were studied. Whenever possible, shelter veterinarians should select vaccines and tests that minimize diagnostic interference after vaccination, in accordance with the principle of differentiating infected from vaccinated animals.44 In addition, positive test results should be interpreted in the context of compatible clinical signs, and confirmatory diagnostic tests should be considered when testing recently vaccinated cats. Although test interference is likely to complicate the identification and control of FPV in shelters, the rate of interference with some tests appears to be low, and most positive test results are subjectively interpreted as weak positives. Despite test interference, the benefit provided by MLV FPV vaccination of all cats upon admission to high-risk environments such as shelters outweighs the negative impact of vaccination on diagnostic test accuracy.
ABBREVIATIONS
FPV | Feline panleukopenia virus |
MLV | Modified-live virus |
SPF | Specific-pathogen–free |
SNAP FIV antibody/FeLV antigen combo test, IDEXX Laboratories, Westbrook, Me.
Fel-O-Vax PCT, Fort Dodge Animal Health, Overland Park, Kan.
FVR C-P, Schering-Plough Animal Health, Omaha, Neb.
Fel-O-Guard Plus 3, Fort Dodge Laboratories Inc, Fort Dodge, Iowa.
Eclipse 3, Schering-Plough Animal Health, Omaha, Neb.
Felocell 3, Pfizer Animal Health, Exton, Pa.
Protex-3, Intervet Inc, Millsboro, Del.
PureVax Feline 3, Merial Inc, Athens, Ga.
Feline UltraNasal FVRCP Vaccine, Heska Corp, Fort Collins, Colo.
Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, NY.
SNAP Parvo, IDEXX Laboratories, Westbrook, Me.
AGEN CPV, AGEN Biomedical Ltd, Brisbane, QLD, Australia.
WITNESS CPV, Synbiotics Corp, San Diego, Calif.
References
- 1
Associated Press. Virus kills hundreds of cats; keeping pets inside can protect them. Detroit Free Press 2004;August 9:5B.
- 2
Beal B. Cats in county at risk from disease outbreak. Red Bluff Daily News 2004;September 29:1B.
- 3
Fiala J. Viral outbreak sweeps Michigan; state confirms FPV. DVM Newsmagazine 2004;September 1:6.
- 4
Mapes LV. Distemper outbreak hits cats: humane society putting cats to death to control disease. The Spokesman Review 1996;August 8:A1.
- 5
Dávila RD. Fatal virus stalking cats, officials warn. Sacramento Bee 2001;January 5:B1.
- 6
Sisson P. Feline virus kills dozens of cats at North County Humane Society. North County Times 2004;September 4:B1.
- 7
Fortems C. Distemper: SPCA forced to put down 60 cats. The Kamloops Daily News 2005;October 27:A4.
- 8
Goldstein S. Virulent virus kills 93 shelter cats. Chicago Tribune 2005;August 25:1.
- 9
Greene L. Fast-acting virus claims cats' lives. St Petersburg Times 2001;June 30:1.
- 10↑
Reif JS. Seasonality, natality and herd immunity in feline panleukopenia. Am J Epidemiol 1976;103:81–87.
- 11
Cave TA, Thompson H, Reid SW, et al. Kitten mortality in the United Kingdom: a retrospective analysis of 274 histopathological examinations (1986 to 2000). Vet Rec 2002;151:497–501.
- 12
Landes C, Kriegleder H, Lengfelder KD. Causes of death and disease in cats based on 1969–1982 autopsy statistics. Tierarztl Prax 1984;12:369–382.
- 13
Whitney WH. Aspects of feline panleukopenia control in a humane facility. Vet Med Small Anim Clin 1973;68:1297–1300.
- 14
Parrish CR. Pathogenesis of feline panleukopenia virus and canine parvovirus. Baillieres Clin Haematol 1995;8:57–71.
- 15
Carlson JH, Scott FW, Duncan JR. Feline panleukopenia. I. Pathogenesis in germfree and specific pathogen-free cats. Vet Pathol 1977;14:79–88.
- 16
Carlson JH, Scott FW. Feline panleukopenia. II. The relationship of intestinal mucosal cell proliferation rates to viral infection and development of lesions. Vet Pathol 1977;14:173–181.
- 17
Carlson JH, Scott FW, Duncan JR. Feline panleukopenia. III. Development of lesions in the lymphoid tissues. Vet Pathol 1978;15:383–392.
- 18↑
McCaw DL, Hoskins JD. Canine viral enteritis. In: Greene CE, ed. Infectious diseases of the dog and cat. 3rd ed. Philadelphia: WB Saunders Co, 2006;63–73.
- 19
Addie DD, Toth S, Thompson H, et al. Detection of feline parvovirus in dying pedigree kittens. Vet Rec 1998;142:353–356.
- 20
Schunck B, Kraft W, Truyen U. A simple touch-down polymerase chain reaction for the detection of canine parvovirus and feline panleukopenia virus in feces. J Virol Methods 1995;55:427–433.
- 21
Esfandiari J, Klingeborn B. A comparative study of a new rapid and one-step test for the detection of parvovirus in faeces from dogs, cats and mink. J Vet Med B Infect Dis Vet Public Health 2000;47:145–153.
- 22
Veijalainen PML, Neuvonen E, Niskanen A, et al. Latex agglutination test for detecting feline panleukopenia virus, canine parvovirus, and parvoviruses of fur animals. J Clin Microbiol 1986;23:556–559.
- 23
Hurley K. Vaccination strategies for cats and dogs in a shelter setting. Maddie's Shelter Medicine Program, College of Veterinary Medicine, University of California-Davis. Available at: www.sheltermedicine.com. Accessed May 9, 2006.
- 24↑
Richards JR, Elston TH, Ford RB, et al. The 2006 American Association of Feline Practitioners feline vaccine advisory panel report. J Am Vet Med Assoc 2006;229:1405–1441.
- 25
Ford RB. Vaccination strategies in the animal shelter environment. In: Miller L, Zawistowski S, eds.Shelter medicine for veterinarians and staff. Ames: Blackwell Publishing, 2004;285–304.
- 26↑
Brun A, Chappuis G, Precausta P, et al. Immunisation against panleucopenia: early development of immunity. Comp Immunol Microbiol Infect Dis 1979;1:335–339.
- 27
Scott FW, Csiza CK, Gillespie JH. Maternally derived immunity to feline panleukopenia. J Am Vet Med Assoc 1970;156:439–453.
- 28↑
Dawson S, Willoughby K, Gaskell RM, et al. A field trial to assess the effect of vaccination against feline herpesvirus, feline calicivirus and feline panleucopenia virus in 6-week-old kittens. J Feline Med Surg 2001;3:17–22.
- 29↑
Mouzin DE, Lorenzen MJ, Haworth JD, et al. Duration of serologic response to three viral antigens in cats. J Am Vet Med Assoc 2004;224:61–66.
- 30↑
Scott FW, Geissinger CM. Long-term immunity in cats vaccinated with an inactivated trivalent vaccine. Am J Vet Res 1999;60:652–658.
- 31
Lappin MR, Andrews J, Simpson D, et al. Use of serologic tests to predict resistance to feline herpesvirus-1, feline calicivirus, and feline parvovirus infection in cats. J Am Vet Med Assoc 2002;220:38–42.
- 32
Kessler MR, Turner DC. Effects of density and cage size on stress in domestic cats (Felis silvestris catus) housed in animal shelters and boarding catteries. Anim Welf 1999;8:259–267.
- 33
Kessler MR, Turner DC. Stress and adaptations of cats (Felis silvestris catus) housed singly, in pairs, and in groups in animal shelters. Anim Welf 1999;8:15–26.
- 34
McCobb EC, Patronek GJ, Marder A, et al. Assessment of stress levels among cats in four animal shelters. J Am Vet Med Assoc 2005;226:548–555.
- 35
Bannasch MJ, Foley JE. Epidemiologic evaluation of multiple respiratory pathogens in cats in animal shelters. J Feline Med Surg 2005;7:109–119.
- 36
Foley JE, Rand C, Bannasch MJ, et al. Molecular epidemiology of feline bordetellosis in two animal shelters in California, USA. Prev Vet Med 2002;54:141–156.
- 37
Cave TA, Golder MC, Simpson J, et al. Risk factors for feline coronavirus seropositivity in cats relinquished to a UK rescue charity. J Feline Med Surg 2004;6:53–58.
- 38
Buonavoglia C, Marsilio F, Tempesta M, et al. Use of a feline panleukopenia modified live virus vaccine in cats in the primary-stage of feline immunodeficiency virus infection. Zentralbl Veterinarmed B 1993;40:343–346.
- 39
Wright JG, Tengelsen LA, Smith KE, et al. Multidrug-resistant Salmonella typhimurium in four animal facilities. Emerg Infect Dis 2005;11:1235–1241.
- 40
Marshall JA, Kennett ML, Rodger SM, et al. Virus and virus-like particles in the faeces of cats with and without diarrhoea. Aust Vet J 1987;64:100–105.
- 41
Hill SL, Cheney JM, Taton-Allen GF, et al. Prevalence of enteric zoonotic organisms in cats. J Am Vet Med Assoc 2000;216:687–692.
- 42
Spain CV, Scarlett JM, Wade SE, et al. Prevalence of enteric zoonotic agents in cats less than 1 year old in central New York State. J Vet Intern Med 2001;15:33–38.
- 43
Pedersen NC, Sato R, Foley JE, et al. Common virus infections in cats, before and after being placed in shelters, with emphasis on feline enteric coronavirus. J Feline Med Surg 2004;6:83–88.
- 44↑
Pasick J. Application of DIVA vaccines and their companion diagnostic tests to foreign animal disease eradication. Anim Health Res Rev 2004;5:257–262.