Effects of anesthesia and surgery on serologic responses to vaccination in kittens

Michael J. Reese Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610.

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Erin V. Patterson Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610.

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Sylvia J. Tucker Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610.

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

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Rolan D. Davis Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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P. Cynda Crawford Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610.

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Julie K. Levy Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610.

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Abstract

Objective—To determine the effects of anesthesia and surgery on serologic responses to vaccination in kittens.

Design—Prospective controlled trial.

Animals—32 specific-pathogen–free kittens.

Procedures—Kittens were assigned to 1 of 4 treatment groups: neutering at 7, 8, or 9 weeks of age or no neutering. All kittens were inoculated with modified-live virus vaccines against feline panleukopenia virus (FPV), feline herpesvirus (FHV), and feline calicivirus (FCV) at 8, 11, and 14 weeks of age and inactivated rabies virus (RV) at 14 weeks of age. Serum antibody titers against FPV, FHV, and FCV were determined at 8, 9, 11, 14, and 17 weeks of age; RV titers were determined at 14 and 17 weeks of age.

Results—Serologic responses of kittens neutered at the time of first vaccination (8 weeks) were not different from those of kittens neutered 1 week before (7 weeks) or 1 week after (9 weeks) first vaccination or from those of kittens that were not neutered. In total, 31%, 0%, 69%, and 9% of kittens failed to develop adequate titers against FPV, FCV, FHV, and RV, respectively, by 17 weeks of age.

Conclusions and Clinical Relevance—Neutering at or near the time of first vaccination with a modified-live virus vaccine did not impair antibody responses in kittens. Many kittens that were last vaccinated at 14 weeks of age had inadequate antibody titers at 17 weeks of age. Kittens may be vaccinated in the perioperative period when necessary, and the primary vaccination series should be extended through at least 16 weeks of age.

Abstract

Objective—To determine the effects of anesthesia and surgery on serologic responses to vaccination in kittens.

Design—Prospective controlled trial.

Animals—32 specific-pathogen–free kittens.

Procedures—Kittens were assigned to 1 of 4 treatment groups: neutering at 7, 8, or 9 weeks of age or no neutering. All kittens were inoculated with modified-live virus vaccines against feline panleukopenia virus (FPV), feline herpesvirus (FHV), and feline calicivirus (FCV) at 8, 11, and 14 weeks of age and inactivated rabies virus (RV) at 14 weeks of age. Serum antibody titers against FPV, FHV, and FCV were determined at 8, 9, 11, 14, and 17 weeks of age; RV titers were determined at 14 and 17 weeks of age.

Results—Serologic responses of kittens neutered at the time of first vaccination (8 weeks) were not different from those of kittens neutered 1 week before (7 weeks) or 1 week after (9 weeks) first vaccination or from those of kittens that were not neutered. In total, 31%, 0%, 69%, and 9% of kittens failed to develop adequate titers against FPV, FCV, FHV, and RV, respectively, by 17 weeks of age.

Conclusions and Clinical Relevance—Neutering at or near the time of first vaccination with a modified-live virus vaccine did not impair antibody responses in kittens. Many kittens that were last vaccinated at 14 weeks of age had inadequate antibody titers at 17 weeks of age. Kittens may be vaccinated in the perioperative period when necessary, and the primary vaccination series should be extended through at least 16 weeks of age.

Cats housed in animal shelters are at risk for becoming infected with FPV, FCV, and FHV because these viruses can persist in the environment and disease transmission rates are typically high in crowded conditions.1–4 Juvenile and debilitated cats are most susceptible to severe life-threatening complications of infection. Vaccination guidelines have been developed to reduce the transmission of highly contagious diseases in animal shelters via increasing individual cat and herd immunity.1 The guidelines recommend implementation of a primary vaccination series consisting of initial vaccination with MLV vaccines against FPV, FCV, and FHV for all cats > 6 weeks of age on the day of admission to a shelter and booster vaccinations every 2 to 3 weeks until cats are 16 weeks of age. Juvenile cats can also be vaccinated against RV, but because rabies is uncommon and requires direct contact for transmission, vaccination may be delayed until the time of adoption.

Because compliance with contracts for postadoption neutering is historically poor, the ideal situation is for cats to be neutered prior to release from shelters.5 In some jurisdictions, neutering of cats before they can be adopted is statutorily required. Consequently, shelters commonly neuter and vaccinate cats within a narrow interval.

To the authors' knowledge, effects of anesthesia and surgery on the immune response of kittens to vaccination are unknown. Some investigators have reported that surgery and anesthesia can suppress innate and acquired immunity, including impairment of leukocyte trafficking, phagocyte function, mitogenesis, natural killer cell activity, Tand B-cell proliferation, and antibody production.6–10 Other investigators have reported that anesthesia and surgery do not impair responses to vaccination.11–13 In 1 study,11 adult feral cats in a trap-neuter-return program had adequate serologic responses to 1 dose of FPV, FHV, FCV, and RV vaccines administered while the cats were anesthetized for neuter surgery. In another study,12 client-owned dogs vaccinated against canine parvovirus and canine distemper virus at time points ranging from 10 days before to 3 days after surgery had increased antibody titers 2 weeks after vaccination. In a third study,13 serologic responses of dogs vaccinated against canine distemper virus at the time of laparotomy were not significantly different from serologic responses of a nonsurgery control group.

Although the practice of simultaneously vaccinating and neutering kittens in shelters is widespread, the impact of this practice on immune responses in kittens has not been elucidated to our knowledge. If surgery suppresses immune responses to vaccination, then kittens in shelters may remain at risk for life-threatening infections. The purpose of the study reported here was to determine whether anesthesia and surgery interfered with serologic responses of kittens vaccinated against FPV, FCV, FHV, and RV.

Materials and Methods

Animals—Specific-pathogen–free queens vaccinated against FPV, FCV, FHV, and RV were bred to give birth to 10 litters of kittens. Thirty-two of these kittens were included in the study. All adult cats and kittens were free of FeLV antigen and FIV antibodies as determined by use of a point-of-care ELISA kit.a Foodb and water were offered free choice throughout the study. Kittens were weaned at 8 weeks of age and placed in group housing. Kittens were identified by use of radio-frequency identification microchips.c At the conclusion of the study, the kittens were adopted. 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 International.

Vaccinations—All kittens were vaccinated at 8, 11, and 14 weeks of age against FPV, FCV, and FHV with a MLV vaccine that also contained inactivated FeLV.d The vaccines were administered SC in the left hind limb, distal to the stifle joint, as recommended by the American Association of Feline Practitioners.1 At 14 weeks of age, an RV vaccinee was administered SC in the right hind limb, distal to the stifle.

Anesthesia and surgery—Kittens were randomly allocated in blocks to 1 of 4 treatment groups by use of a random number table. Each group contained 8 kittens with 4 males and 4 females from different litters. The first group was neutered at 7 weeks of age (1 week prior to first vaccination), the second group was neutered at 8 weeks of age (at the time of first vaccination), the third group was neutered at 9 weeks of age (1 week after first vaccination), and the fourth group was not neutered (control group). Food was withheld from kittens 1 to 4 hours prior to surgery, but access to water was unrestricted.14,15 For each kitten, a preoperative physical examination was performed, and body weight and rectal temperature were recorded. A blood sample was also collected via jugular venipuncture for determination of PCV and blood concentrations of total protein, urea nitrogen, and glucose. Butorphanolf (0.4 mg/kg [0.18 mg/lb], SC) was administered as a preemptive analgesic; a suspension of 75,000 units of penicilling was also administered SC. Anesthesia was induced and maintained with isoflurane (2% to 5%), which was administered via face mask.

Once anesthetized, each kitten was positioned on a blanket containing circulating warm water that was covered with a towel. Surgical sites were clipped and aseptically prepared for surgery. Females were spayed via ventral midline incision; males were castrated via scrotal incision, and the spermatic cords were tied on themselves.15–17 Kittens neutered at 8 weeks were vaccinated at the end of surgery while still anesthetized. Rectal temperatures were measured again as the kittens recovered from anesthesia. Duration of surgery and total duration of anesthesia (defined as the interval between induction of anesthesia by mask and return to sternal recumbency) were measured. Administration of butorphanol was repeated 4 to 6 hours after surgery and again if kittens appeared uncomfortable (eg, decreased activity or hunched appearance). Food was offered within 1 hour after recovery from anesthesia.

Serologic testing—Blood samples (3 to 5 mL) were obtained from kittens via jugular venipuncture at 8, 9, 11, 14, and 17 weeks of age. Blood samples were collected into serum separator tubes, allowed to clot for 30 minutes, and then centrifuged for 20 minutes. Serum was separated and stored at −20°C pending analysis. Serum antibody titers were measured for FPV (hemagglutination inhibition assayh), FCV (virus neutralization assayh), and FHV-1 (virus neutralization assayh). Protective titers established by the laboratory in which assays were conducted were 40, 32, and 16 for FPV, FCV, and FHV, respectively. Serum RV antibody titers were determined at 14 and 17 weeks of age (virus neutralization assay via the rapid fluorescent focus inhibition test).i A titer ≥ 0.5 U/mL is considered adequate for international movement of cats to most rabies-free areas, but true protective titers have not been determined.18 For purposes of statistical analysis, protective titers against FPV, FHV, and FCV and adequate titers against RV were all deemed adequate (vs protective).

Statistical analysis—Mean body weights; PCVs; blood concentrations of total protein, urea nitrogen, and glucose; durations of surgery and anesthesia; and preoperative and postoperative rectal temperatures were compared among treatment groups via the Kruskal-Wallis ANOVA by ranks test. Mean preoperative and postoperative rectal temperatures and durations of surgery and anesthesia for males and females were compared via the Mann-Whitney rank sum test. Mean FPV, FCV, FHV, and RV antibody titers at each time point were compared among treatment groups via the Kruskal-Wallis ANOVA by ranks test. Proportions of kittens with adequate antibody titers against FPV, FHV, FCV, and RV in each treatment group at each time point were compared via the Fisher exact test. Values of P < 0.05 were considered significant.

Results

Treatment groups—Mean preoperative values for PCV and blood concentrations of total protein, urea nitrogen, and glucose were not significantly (all P > 0.1) different among groups of kittens neutered at 7, 8, or 9 weeks of age (Table 1). Body weight increased significantly (P < 0.001) with increasing age for neutered kittens.

Table 1—

Mean ± SD (range) body weight, PCV, and blood concentrations of 3 analytes in specific pathogen-free kittens at the time of neutering at 7, 8, or 9 weeks of age (n = 8 kittens/group).

Age at neutering (wk)Body weight at time of neutering (kg)*PCV (%)Total protein (mg/dL)Urea nitrogen (mg/dL)Glucose (mg/dL)
70.8 ± 0.1 (0.7–1.0)30 ± 2.6 (26–33)4.9 ± 0.5 (4.2–6.0)25 ± 7.1 (15–35)88 ± 24 (50–115)
81.0 ± 0.1 (0.9–1.1)30 ± 2.9 (26–35)4.7 ± 0.7 (4.1–6.2)23 ± 5.6 (20–35)97 ± 13 (81–124)
91.1 ± 0.1 (0.9–1.3)31 ± 2.5 (28–34)4.8 ± 0.2 (4.6–5.0)29 ± 7.8 (20–35)94 ± 9 (83–106)

A signifcant (P < 0.001) increase in body weight was detected in each successive age group.

To convert to pounds, multiply the value by 2.2.

Duration of surgery, total duration of anesthesia, and preoperative and postoperative rectal temperature were not significantly (all P > 0.06) different among the 3 groups of neutered kittens (Table 2). Duration of surgery and total duration of anesthesia were significantly (P < 0.001) longer for females, compared with durations for males. Although preoperative rectal temperatures were not significantly (P = 0.6) different between males and females, females had significantly (P = 0.02) lower postoperative rectal temperatures, presumably because of longer durations of surgery and anesthesia. There were no anesthetic or surgical complications.

Table 2—

Mean ± SD (range) duration of surgery, total duration of anesthesia, and preoperative and postoperative rectal temperatures for male and female specific-pathogen-free kittens neutered at 7, 8, or 9 weeks of age (n = 4 kittens/group).

Age at neutering (wk)Duration of surgery (min)*Duration of anesthesia (min)*Preoperative rectal temperature* (°C)Postoperative rectal temperature* (°C)
Male
71.0 ± 0 (1–1)6.3 ± 0.5 (6–7)38.6 ± 0.2 (38.4–38.8)38.2 ± 0.2 (38.1–38.3)
81.5 ± 0.6 (1–2)6.0 ± 0 (6–6)38.6 ± 0.2 (38.3–38.8)38.1 ± 8.0 (36.9–38.7)
91.0 ± 0 (1–1)5.5 ± 0.6 (5–6)38.9 ± 0.2 (38.6–39.2)38.3 ± 0.6 (37.5–38.6)
Female
710.0 ± 1.8 (8–12)18.5 ± 1.3 (17–20)38.7 ± 0.3 (38.5–39.1)37.7 ± 0.2 (37.5–37.9)
89.3 ± 3.9 (6–15)17.5 ± 3.1 (15–22)38.5 ± 0.3 (38.2–38.8)37.7 ± 0.7 (36.7–38.4)
99.3 ± 1.0 (8–10)17.8 ± 1.0 (17–19)38.8 ± 0.3 (38.4–39)38.0 ± 0.4 (37.4–38.3)

Durations of surgery and anesthesia were significantly (P < 0.001) longer, and postoperative rectal temperatures were significantly (P = 0.02) lower in females, compared with respective values in males, but differences among the groups with respect to these values were not significant.

To convert to degrees Fahrenheit, multiply the value by 9/5 and add 32.

Serum anti-FPV antibody titers—Feline panleukopenia antibody titers were not significantly (all P > 0.6) different among treatment groups at 8, 9, 11, 14, or 17 weeks (Table 3). Thirty-one of 32 (97%) kittens had maternally derived antibodies against FPV at the time of the first vaccination at 8 weeks of age. Only 1 kitten was seronegative. After vaccination at 8, 11, and 14 weeks of age, only 22 (69%) kittens had adequate antibody titers against FPV at 17 weeks of age (Table 4). Adequate titers developed in 21 of 31 (68%) kittens with maternally derived FPV antibodies at the time of the first vaccination and in the kitten that was seronegative at the time of the first vaccination.

Table 3—

Mean ± SD (range) serum antibody titers against FPV, FCV, FHV, and RV in specific-pathogen-free kittens that were neutered at 7, 8, or 9 weeks of age and in unneutered kittens (n = 8 kittens/group).

Age at neutering (wk), by vaccineAge at determination of serum antiviral antibody titer (wk)
89111417
FPV
764 ± 48 (10–160)41 ± 26 (1–80)345 ± 895 (20–2,560)215 ± 443 (0–1,280)368 ± 567 (0–1,280)
868 ± 44 (20–160)43 ± 25 (20–80)110 ± 216 (0–640)45 ± 49 (0–160)305 ± 450 (0–1,280)
949 ± 28 (10–80)31 ± 22 (10–80)108 ± 216 (0–640)419 ± 892 (0–2,560)65 ± 64 (0–160)
No surgery60 ± 51 (0–160)39 ± 29 (0–80)51 ± 26 (10–80)436 ± 560 (10–1,280)208 ± 215 (0–640)
FCV
73 ± 5 (0–12)27 ± 21 (4–64)141 ± 121 (8–384)466 ± 342 (128–1,024)640 ± 368 (128–1,024)
811 ± 15 (0–48)33 ± 28 (6–96)146 ± 156 (32–512)1,184 ± 2,021 (192–6,144)924 ± 1,313 (96–4,096)
93 ± 5 (0–12)23 ± 13 (12–48)212 ± 122 (64–384)560 ± 479 (128–1,024)632 ± 599 (192–2,048)
No surgery4 ± 5 (0–16)32 ± 22 (8–64)126 ± 161 (12–512)336 ± 244 (32–768)448 ± 382 (64–1,024)
FHV
711 ± 16 (0–48)7 ± 8 (0–24)6 ± 7 (0–24)7 ± 6 (0–16)11 ± 5 (4–16)
812 ± 9 (0–24)8 ± 6 (0–16)5 ± 5 (0–16)4 ± 3 (0–8)12 ± 10 (0–32)
96 ± 9 (0–24)3 ± 6 (0–16)3 ± 3 (0–6)3 ± 3 (0–8)8 ± 6 (0–16)
No surgery5 ± 4 (0–12)5 ± 5 (0–12)2 ± 3 (0–8)5 ± 3 (0–8)20 ± 19 (4–48)
RV
7NDNDND0.1 ± 0.1 (0–0.2)46.3 ± 38.3 (0–85.9)
8NDNDND0.2 ± 0.2 (0–0.6)15.2 ± 17.5 (0.2–50.3)
9NDNDND0.1 ± 0.2 (0–0.6)52.9 ± 29.7 (16.0–85.9)
No surgeryNDNDND0.0 ± 0.1 (0–0.2)48.2 ± 35.5 (0–85.9)

Values for antibody titers against FPV, FCV, and FHV are reported as reciprocal dilutions, and titers against RV are reported as units per microliter. Kittens in each group were vaccinated against FPV, FCV, and FHV at 8, 11, and 14 weeks of age and against RV at 14 weeks of age. Blood samples were collected at 8, 9, 11, 14, and 17 weeks of age for determination of serum antibody titers. Antibody titers were not significantly different among the 4 treatment groups.

ND = Not determined.

Table 4—

Proportions of specific-pathogen-free kittens (n = 32) with adequate antibody titers against FPV, FCV, FHV, and RV at various ages; kittens were vaccinated against FPV, FCV, and FHV at 8, 11, and 14 weeks of age and against RV at 14 weeks of age.

AntibodyAge at determination of serum antiviral antibody titer (wk)
89111417
Anti-FPV7556665669
Anti-FCV33894100100
Anti-FHV1996331
Anti-RVNDNDND991

Values reported are percentages. Proportions were not significantly different among kittens that were neutered at 7, 8, or 9 weeks of age and kittens that were not neutered.

See Table 3 for remainder of key.

Serum anti-FCV antibody titers—The 4 treatment groups were not significantly (all P > 0.2) different with respect to FCV antibody titers at 8, 9, 11, 14, or 17 weeks of age (Table 3). Eighteen of 32 (56%) kittens had maternally derived antibodies against FCV at the time of the first vaccination at 8 weeks of age, and 14 were seronegative. By 17 weeks of age, all kittens had adequate antibody titers against FCV (Table 4).

Serum anti-FHV antibody titers—The 4 treatment groups were not significantly (all P > 0.2) different with respect to FHV antibody titers at 8, 9, 11, 14, or 17 weeks of age (Table 3). Twenty-two of 32 (69%) kittens had maternally derived antibodies against FHV at the time of the first vaccination at 8 weeks of age, and 10 were seronegative. After vaccination at 8, 11, and 14 weeks of age, only 10 kittens had adequate antibody titers against FHV at 17 weeks of age (Table 4). Adequate titers developed in 6 of 22 (27%) kittens with maternally derived FHV antibodies at the time of the first vaccination and in 4 of the 10 (40%) kittens that were seronegative at the time of the first vaccination.

Serum anti-RV antibody titers—The 4 treatment groups were not significantly (all P > 0.1) different with respect to antibody titers against RV at 14 or 17 weeks (Table 3). Eight of the 32 (25%) kittens had maternally derived antibodies against RV at the time of the first vaccination at 14 weeks of age, and 24 were seronegative. After vaccination at 14 weeks of age, 29 (91%) kittens had adequate antibody titers against RV at 17 weeks of age (Table 4). Adequate titers developed in 7 of 8 kittens with maternally derived RV antibodies at the time of the first vaccination and in 22 of the 24 (92%) kittens that were seronegative at the time of the first vaccination.

Discussion

Kittens that were neutered a week before, at the time of, or a week after first vaccination developed antibody titers comparable to those of the sexually intact control group. The percentage of kittens that developed adequate antibody titers against FPV, FCV, FHV, and RV by 17 weeks of age was also similar among the 4 treatment groups. This suggests that anesthesia and surgery did not significantly influence the serologic responses of kittens to vaccination in our study, in which kittens were healthy and the duration of surgery and amount of trauma were minimized.

Other studies19–24 have revealed that acute stress may enhance some aspects of immune function, whereas chronic stress is more likely to contribute to immunosuppression. Acute stress promotes innate and adaptive immune responses in rats and mice, including enhanced dendritic cell migration from skin to draining lymph nodes, leukocyte redistribution to the skin, and enhanced T-cell memory.19–24 Removal of kittens from their queens, transportation of kittens to the surgical area, and other factors such as anesthesia, surgical trauma, and postoperative discomfort may act as acute stressors. Enhancement of the immune system attributable to acute stress in the perioperative period may offset any immunosuppressive effects of surgical procedures.

The kittens selected for the controlled trial reported here were born to queens that were seropositive for antibodies against FPV, FCV, FHV, and RV because we believed this scenario simulated one commonly encountered in animal shelters and veterinary practices. Consequently, most kittens had maternally derived antibodies against these viruses at the time of first vaccination. Maternally derived antibodies reportedly persist up to 16 weeks, 14 weeks, and 10 weeks for FPV, FCV, and FHV, respectively, in experimental situations,25–27 but wider variation is likely to exist in nature. In our study, failure of kittens to respond to vaccination was independent of any effect of anesthesia and surgery.

In another study28 in which an MLV vaccine was administered to 8-week-old kittens, 85.4% of seronegative kittens developed adequate titers against FPV by 2 weeks after the first vaccination, but none developed adequate titers against FHV within the same period. This indicates that the kinetics and magnitude of responses to vaccination in cats are not consistent for all viruses, even when the influence of maternally derived immunity is not a factor. Two other studies29,30 revealed that adequate titers against FPV, FCV, and FHV were much more likely to develop in kittens that were seronegative at the time of the first vaccination than in those with maternally derived antibodies. Investigators in 1 study29 speculated that high-titer inactivated vaccines may be more effective in overcoming the influence of maternally derived immunity, compared with the effectiveness of MLV vaccines, but they did not test this hypothesis.

Failure of 3 (9.4%) kittens to develop an adequate response within 3 weeks after the first RV vaccination was consistent with findings of other studies in which investigators evaluated RV vaccination of anesthetized adult cats11 or pet cats vaccinated for purposes of international travel.18 However, in the study reported here, RV titers were measured only once (at 3 weeks after vaccination), and it is unknown whether titers continued to increase after that evaluation. The kittens that failed to develop adequate titers against RV were distributed among 3 treatment groups, including the control group, so surgery did not appear to be a factor in the failure to respond adequately.

Neutering at the time of vaccination did not impair antibody responses in the kittens in our study, but a substantial proportion of kittens that received the final vaccination at 14 weeks of age did not have adequate antibody titers at 17 weeks of age. This suggests that it is appropriate to vaccinate kittens in the perioperative period when necessary and that veterinarians should encourage compliance with new guidelines1 for extending the series of primary vaccinations through at least 16 weeks of age.

ABBREVIATIONS

FCV

Feline calicivirus

FHV

Feline herpesvirus

FPV

Feline panleukopenia virus

MLV

Modified-live virus

RV

Rabies virus

a.

SNAP FIV/FeLV Combo test, IDEXX Laboratories Inc, West-brook, Me.

b.

Iams Kitten Formula, The Iams Co, Dayton, Ohio.

c.

MicroChip identification system, AVID, Folsom, La.

d.

Fel-O-Guard Plus 3 Lv-K, Fort Dodge Animal Health, Fort Dodge, Iowa.

e.

Rabvac 3 TF, Fort Dodge Animal Health, Fort Dodge, Iowa.

f.

Torbugesic, Fort Dodge Animal Health, Fort Dodge, Iowa.

g.

US Vet MicroSuspension II sterile penicillin G procaine, GC Hanford Manufacturing Co, Syracuse, NY.

h.

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

i.

Department of Veterinary Diagnosis, College of Veterinary Medicine, Kansas State University, Manhattan, Kan.

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