Animal Behavior Case of the Month

Lena R. Provoost 1Small Animal Behavior Service, Department of Clinical Sciences and Advanced Medicine, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Statement of the Problem

A cat was evaluated at a small animal behavior service for staring at, chasing, and biting another cat in the same household and periuria for > 1 year.

Signalment

The patient was a 6-year-old 4.9-kg (10.8-lb) neutered male domestic shorthair cat.

History

The patient (cat 1) was adopted from a pet rescue agency at 16 weeks of age and was neutered at that time; it resided with a couple and 3 other adult male cats in a 2-story house with a basement. All cats stayed indoors with free run of the house and were fed together. The most recent addition to the home was a 4-year-old neutered male domestic shorthair cat (cat 2) that was adopted 18 months before the initial behavior consultation. The owners reported that, when introduced to cat 2, cat 1 stared, stiffened, growled, and hissed; had piloerection; and chased the other cat. Over the previous 12 months, coinciding with a move into their current home, the behavior of cat 1 had escalated to swatting, scratching, and biting cat 2 as well as displacing cat 2 from rooms. Generally, cat 1 would lower its head, avert its gaze, and attempt to keep distance from cat 2, but would not completely avoid rooms where cat 2 was present. The owners used verbal reprimands to interrupt chasing and biting. In response, cat 1 would walk away from cat 2 with its ears forward and tail flicking, then back up to a wall and quiver its tail without urinating. These interactions typically occurred twice daily, usually on the first level (floor) of the home. Cat 1 also chased cat 2 out of litter boxes in the basement and guarded access to the second floor of the home by lying at the top of the stairs, and would stare and hiss with its ears forward and chase cat 2 if it passed by.

When cat 2 was first adopted, cat 1 began to back up to walls with a quivering tail, treading its front paws and spraying small amounts of urine. In the current home, this occurred on furniture and walls in the basement. The spraying frequency was intermittent. Months passed without spraying, followed by several weeks of spraying multiple times per day. At the time of the initial behavior consultation, the owners estimated that the patient had sprayed twice daily for the past month. There were 6 litter boxes in the home (2 on the second floor and 4 in the basement); all were large, uncovered, deep, unlined boxes with unscented clumping litter 3 to 5 inches deep. The boxes were scooped daily and washed with soap and water every other week. Cat 1 mostly used the litter boxes on the second floor to defecate and urinate normal volumes. Outside cats were never observed around the home, and the owners were certain that only cat 1 was spraying urine because they had witnessed the behavior. When they observed the cat spraying, they shooed it away from the site and cleaned the area with an enzymatic cleaner.a

Cat 1 frequently paced on the first floor and had spent less time resting near the owners and the other cats over the previous 6 months. This cat routinely hid from visitors and when there were loud noises (eg, during fireworks) or persistent household sounds (eg, from use of a blender or vacuum cleaner). Cat 1 had not shown aggressive behavior toward the owners or the other 2 household cats, and the other cats had not shown aggressive behavior toward cat 1. Cat 1 had affiliative behavior with the other 2 cats; they slept together, allogroomed, and bunted each other. These cats entered the second floor without being stared at or chased by cat 1. Cat 2 also had affiliative behaviors with the other 2 cats; most of its time was spent in the basement, and it would groom itself for approximately 30 seconds after fights with cat 1.

Physical Examination Findings and Laboratory Results

Only cat 1 and the owners were present for the appointment. The patient showed signs of stress, including dilated pupils, vocalization (yowling) on entering the examination room, pacing, increased vigilance, freezing, and frequent self-grooming. A variety of treats and toys were offered but were not approached by the patient; it would orient toward the owners when called by name but continued to pace the room. Results of a physical examination were unremarkable; the penis could not be extruded to check for barbs. Two weeks before the initial behavior consultation, the referring primary care veterinarian (rDVM) had submitted samples for a CBC, serum biochemical analysis including total thyroxine concentration, and urinalysis, with all results within the respective reference ranges; a urine sample submitted for microbial culture had negative results. Because of the biting behavior, screening for FeLV and FIV was recommended, but it was declined because all household cats had tested negative for these viruses at adoption and showed no signs of illness.

Diagnosis

Diagnoses of intercat conflict1–3 with a component of territorial aggression,1,2,4 urine marking secondary to anxiety,5–7 and generalized anxiety disorder8,9 were made. Intercat conflict3 is a term that describes agonistic behavior of one cat toward another within the same household or neighborhood1,3,10 that is often associated with social system destabilization.11 Examples of agonistic behavior that cat 1 showed included staring at, chasing, swatting, scratching, and biting cat 2 as well as displacing cat 2 from rooms and blocking its access to areas in the home. Intercat conflict or aggression stems from many causes, including fear,1,3,5 anxiety,3,5 pain,3 frustration (also reported as redirected aggression),1,3 predatory behavior,3,5 play,3,5 and hyperthyroidism.1 It is proposed that inappropriate social skills are a hallmark of intercat aggression,1 as agonistic behavior is displayed despite lack of provocation.1,2 Generally, cats use increased distance to defuse conflict12 and to avoid escalation of aggression,3 but distance between cats can be difficult to achieve in a multicat household. Intercat conflict was likely triggered by anxiety over the addition of cat 2 causing added pressure on available resources.3,11 Agonistic behavior was associated with access to resources (eg, spaces and litter boxes) in the home despite cat 2's avoidance behavior.1,2 A diagnosis of intercat conflict was also supported by nonelimination marking behavior after fights or negative interactions.1 Guarding of the second floor and defense of cat 1's core area were consistent with territorial aggression.1 Pain and hyperthyroidism were unlikely because physical examination findings were normal and total thyroxine concentration was within the reference range. There was no evidence of redirected aggression or interactions consistent with play. Predatory aggression was also unlikely, as cat 1 consistently vocalized when encountering cat 2.1,3 Some authors consider status-related2 or dominance aggression13 as differential diagnoses for intercat conflict, but this is not widely accepted because the social structure of cats is complex.3,12 Cat 1 had signs of anxiety, including frequent pacing and reduced social interactions with the owners and other household cats. Generalized anxiety disorder was diagnosed because cat 1 had signs of heightened anxiety in the home over the past year and these signs were not solely associated with novel sights, sounds, smells, or social contexts.9 Generalized anxiety most likely contributed to cat 1's reactivity to cat 2.8

House soiling was limited to small volumes of urine on vertical surfaces and posturing consistent with urine marking.14 A distinction was made between toileting in undesired locations (eg, voiding normal urine volumes in such locations, soiling horizontal surfaces, and not using a litter box, with or without attempts to cover the soiled area) and marking behavior (eg, voiding small urine volumes, targeting vertical surfaces, continuing to use a litter box for normal toileting, assuming typical marking posture [backing up to a surface with the tail quivering], and soiling in areas of social importance). Causes of toileting in inappropriate areas (eg, aversions or preferences for a particular litter substrate, litter box style, or litter box location and substrate preferences)1 were not present, as cat 1 consistently used a litter box for defecation and urinating in normal volumes. Urine marking is a normal behavior that provides a visual and chemical message to conspecifics in areas of social significance.11,15 Such marks convey identifying information, and their deteriorating scent over time is a time stamp of the animal's presence that may aid in regulating interactions.15 Aside from being sexually intact,1,11 other causes of urine marking include endocrine disorders1,3,16 and the presence of new, inanimate items in a cat's living space.6

The role of medical conditions in urine spraying is not well understood. Some authors report that endocrine disorders such as hyperthyroidism and conditions that result in increased circulating cortisol or testosterone concentrations can be causes for urine spraying16,17 that resolves after appropriate treatment.18 To the author's knowledge, the only published evidence of this is a clinical report17 of a male cat that was presented for urine spraying and aggressive behavior that resolved after an adrenocortical tumor was diagnosed and removed. In a study19 of 34 cats with urine-spraying behavior, 8 had crystalluria and 7 had urogenital abnormalities that included renal calculi, kidney failure, calculi in the urinary bladder, bacterial urinary tract infection, and cystitis. The effect of these medical conditions on urine spraying was not investigated. A study20 that was performed to investigate potential associations between lower urinary tract disease and urine spraying by gonadectomized cats found no significant differences in urinalysis variables between cats that had urine-marking behavior and a group of control cats without this behavior. Cat 1's urine marking was confined to cat 2's core area (the basement), which reflected anxiety and conflict with cat 26,7 as well as an attempt at emotional stabilization.6,21 It is proposed nonelimination marking, as observed after fights between the 2 cats, infers social status,1 but it may result from a state of high arousal11 and fear associated with verbal reprimands,5,6 supporting the role of anxiety in this behavior. Additionally, urine may be withheld if the mark is not likely to be monitored.1 Hormonal influence on marking was unlikely for the patient of this report because the cat was neutered, although the absence of barbs on the penis was not confirmed. Underlying medical conditions were also considered unlikely on the basis of normal physical examination findings, negative urinalysis and urine culture results, and clinicopathologic data within the respective reference intervals.

Treatment

Chronic anxiety and aggression are welfare concerns for all cats involved in intercat conflict.5,6 Treatment comprised environmental management, behavior modification, and psychopharmaceutical intervention. The owners were advised to avoid punishment, including verbal reprimands, as it can increase the patient's stress and fear.6,9 Punishment does not address the motivation for the patient's behavior and contributes to an already unpredictable and challenging environment, potentially causing the behavior to worsen.9,22 In place of verbal punishment, the owners were advised to redirect the patient by calling its name and providing a cue to perform a behavior incompatible with posturing for urine marking,22 such as hand targeting, and providing a reward for compliance. Environmental management involved avoidance of situations in which cat 1 stared at or chased cat 2 and appropriate litter box maintenance (continuing to scoop litter daily and increasing the frequency of washing the boxes and replacing litter to once weekly).7 Although urine spraying is not associated with litter box hygiene problems, appropriate maintenance may contribute to reduced marking.7,23 The patient was to be segregated to the second floor when not supervised to prevent marking in the basement, and the owners were to monitor its interactions with cat 2.6,7 Urine-marked areas were to be cleaned with another enzymatic cleaner,5,b and a log of occurrences was to be kept.

Alternative forms of marking in socially significant areas were to be encouraged,21 and use of synthetic pheromone products was recommended. The use of synthetic feline F3 facial pheromonec has been reported to promote facial rubbing21 and reduce urine marking,24 and application of synthetic feline interdigital semiochemical pheromoned to scratching posts can help encourage scratching of the treated surface.25 Video recordings of the basement were recommended to determine whether other cats were urine marking. In case of a fight, the owners were instructed not to use their hands or feet to interrupt the behavior but to use a noise other than verbal reprimands and to separate the cats with a towel, blanket, or cushion if needed. The basement was to be cat 2's core area, and the second floor was to be the core area for cat 1; each cat was to be kept out of the other's area with baby gates or closed doors.3 Core areas were to have litter boxes, bedding, elevated resting spaces, hiding boxes, food, water, and toys.3,11 The first floor was to be a shared space, and a diffuser with synthetic feline appeasing pheromonee intended to reduce social tension and conflict between cats was recommended.26 Distribution of resources and management of this space was reviewed.3,6 To address the generalized anxiety of cat 1, background noise to muffle sounds,1 placing the cat in its core area (upstairs) before the arrival of visitors,1 and individual play5 were suggested.

Behavior modification included a targeting cue to redirect the patient's staring. Emergency interruptions (shaking a package of treats, use of a laser pointer, or ringing a bell) were to be associated with high-value treats to redirect either cat's attention.5 Time spent on the first floor was to be alternated between cats, and they were to be gradually reintroduced with desensitization and counterconditioning.4,5 Desensitization and counterconditioning protocols for cats 1 and 2 were to be performed at opposite ends of the living room on the first floor, with each cat attended by an owner who would provide palatable treats that could be quickly eaten. A physical barrier such as an exercise pen was to be placed halfway between the cats' positions to allow the owner working with cat 2 to remove it if cat 1 attempted to chase it. Sessions were to be short, starting with 30 seconds and gradually increased by 1-minute increments as long as cat 1 remained relaxed. Over time, the cats were to be gradually placed closer to each other with the goal of removing the barrier and allowing them to interact once their body language showed no signs of anxiety or agonistic behavior.

Several medications have been shown to effectively treat urine marking, including fluoxetine,27,28 clomipramine,28 buspirone,7,29 and benzodiazepines.30 In 1 study, 17 of 17 cats treated with fluoxetine had a > 90% reduction in the frequency of urine spraying, compared with findings in the week before treatment.27 Other investigations found that efficacies of fluoxetine and clomipramine for reduction in urine-marking behavior appeared to be similar,28 whereas treatment with buspirone resulted in 32 of 62 (52%) cats experiencing a > 75% reduction in the frequency of urine spraying.29 Treatment with buspirone resulted in little or no adverse effects,29 but it can increase behaviors that reflect self-confidence and assertiveness,31,32 which was considered undesirable in this case because the patient had agonistic behavior toward cat 2. Clomipramine, a tricyclic antidepressant, was not initially prescribed because it is reported to have adverse anticholinergic, gastrointestinal, and sedative effects.28,31 Fluoxetine, a selective serotonin (5-hydroxytryptamine) reuptake inhibitor, prevents reuptake of serotonin in synapses, and chronic use reregulates serotonin receptors, increasing postsynaptic flow of serotonin33 to relieve anxiety. The most commonly reported adverse effect of fluoxetine administered to cats is a reduced appetite,27 and therefore, this medication was selected for the patient. Additional adverse effects include sedation, vomiting, diarrhea, restlessness, excitement, seizures, and signs of increased anxiety.34 Fluoxetine was initially prescribed at a dosage lower than the target (0.26 mg/kg [0.12 mg/lb], PO, q 24 h) for 14 days to reduce the potential for adverse effects6,35 and then increased (0.51 mg/kg [0.23 mg/lb], PO, q 24 h).6 The time to effect for fluoxetine is 4 to 6 weeks, and owing to the chronicity of signs of anxiety and stress, an additional, more rapidly acting medication was recommended. Diazepam, a rapid-acting benzodiazepine, has shown efficacy in reducing feline urine spraying30 but is associated with acute hepatic necrosis and liver failure in cats, and it is no longer recommended to treat urine spraying.36 Benzodiazepines may cause paradoxical excitement, and an alternative to diazepam, such as alprazolam or clonazepam, could have been considered, as they have not been associated with acute liver failure in cats; however, to the author's knowledge, no studies have evaluated their efficacy for the treatment of urine spraying.37 Because there is also a risk of human drug misuse, alternatives to benzodiazepines were considered first.9 Gabapentin, an antiepileptic drug, is an α-2-δ ligand that binds to presynaptic voltage-sensitive calcium channels in the amygdala to block release of excitatory neurotransmitters.38 Results of recent studies suggest that gabapentin is effective in reducing stress scores of household cats during transportation and veterinary examination39 and of community cats included in a trap-neuter-return program.40 In cats, the time to effect for gabapentin is 100 minutes, with a half-life of approximately 3 hours after oral administration.41 Also, gabapentin appears to have a synergistic effect when combined with a selective serotonin reuptake inhibitor42 and has been effectively used in an extralabel manner to treat generalized anxiety disorders in people43,44 and pets.31 Therefore, gabapentin was prescribed to provide rapid anxiolysis.31 The initial dosage was 5.1 mg/kg (2.3 mg/lb), PO, every 24 hours for 5 days, followed by 5.1 mg/kg, PO, every 12 hours.35 The initial lower frequency of administration was intended to reduce the anticipated adverse effects of sedation and ataxia39 and encourage owner compliance.45,46 Other reported adverse effects in cats include hypersalivation and vomiting.39 Potential adverse effects, duration to effect, and extralabel use were discussed for all medications prescribed. Potential advantages and disadvantages of the use of synthetic pheromone products were also discussed.

Lastly, the form of medications was reviewed to help ensure compliance and ease of administration. A recent survey of cat owners in Europe46 revealed that registered feline medications and liquid formulations were more palatable to cats than medications formulated for other species and solid formulations (in Europe, veterinary medications are registered and monitored through the European Medicines Agency, similar to the US FDA). Therefore, fluoxetine oral solution was provided as an unflavored (20 mg/5 mL) syrup that was to be mixed in a small amount of canned food or tuna juice. Gabapentin was compoundedf into a small 25-mg catnip-scented tablet to be concealed in a small morsel of food.

Follow-up

At a 1-week follow-up via telephone, the owners reported that administration of the treatments was successful and no adverse effects associated with medications were observed. Environmental enrichment, increased resources, and environmental use of the recommended synthetic pheromones were implemented. During the alternating times on the first floor, the patient had begun urine marking on the closed basement door. To prevent this, the owners had opened the door, allowing the patient access to the basement, where it continued urine marking with the same frequency. Guidelines were reviewed with the owners to keep the patient out of the basement and away from the basement door. When alternating time in shared spaces such as the first floor, the patient was to be actively supervised and redirected away from the basement when needed. It was explained that the patient likely perceived cat 2 as a threat and experienced maladaptive arousal and anxiety when exposed to the presence or scent of that cat, resulting in urine spraying and agonistic behavior. To modify the undesirable behavior associated with such a perception, a strict gradual desensitization and counterconditioning program would have to be followed; otherwise, treatment would likely fail. The owners reported that they understood the treatment plan, but at times the patient wandered off if they turned around for a few seconds. Physical barriers in front of the basement door,6 such as baby gates and flexible gateways, were discussed as a way to prevent the patient from gaining access to the door and entering the basement. The owners reported that the patient's pacing frequency was reduced by approximately 25% and that it had started to rest on the couch near the owners and the other 2 cats more frequently when on the first floor.

One month after the initial behavior consultation, urine marking was markedly decreased to 3 times/wk, occurring when the patient went into the basement unnoticed. The owners indicated that basement door was frequently opened and closed, and it was not always closed properly if they were in a hurry. At this point, the patient readily played with the owners and no longer paced on the first floor. The owners observed the patient rubbing its face on doorways but indicated that it did not use scratch pads once the visual element of the synthetic pheromone was absent, so use of the product was discontinued. Although cat 1 or cat 2 was generally kept confined in a core area in the owners' absence, there continued to be lapses in closing the basement door because of a broken locking mechanism. The planned reintroductions occurred on a nightly basis. During reintroductions, cat 1 continued to stare at cat 2 but ate treats and remained relaxed for up to 10 minutes while cat 2 was present. Approximately once weekly, cat 1 would run toward the physical barrier used to prevent access to cat 2 but was easier to redirect with a target cue. Video recordings of the basement confirmed that cat 1 was the only cat marking in that area when the door was left open. A video recording showed cat 1 urine spraying on the lower stairway when another household cat (not cat 2) was lying across the stairway that led to the first floor. This was interpreted as a sign of the patient's anxiety resulting from the blocked path out of the basement.

At the 2-month follow-up, the owners reported that the patient's urine marking had increased to > 4 times/d for 2 weeks, and new areas were targeted (base of the stairs in basement; a spare bed on second floor when visitors were present). Cats 1 and 2 were in the same room for longer durations of up to 1 hour; staring by cat 1 lasted several minutes and rarely escalated to chasing. The increased marking at the stairs was likely attributable to anxiety associated with a perception of restricted ability to leave the basement; completely excluding the patient from the basement was again emphasized to the clients, and behavior modification to redirect staring was reviewed. Additionally, a pet door with a locking mechanism was recommended to prevent cats other than cat 2 from entering the basement and to help the owners remember to shut the door and lock it from the outside. The increased urine marking likely resulted from a combination of a lack of strict environmental management (keeping the patient out of the basement) and a delayed response to the initial dose of fluoxetine.47 Therefore, a fluoxetine dose increase was warranted, and a recommended increase to 0.81 mg/kg (0.37 mg/lb) was implemented with no adverse effects noted by the owners.

At a 3-month follow-up, urine marking had decreased substantially, with 2 incidences noted in the preceding 6 weeks. The owners indicated they were strictly adhering to the recommendation to keep cats 1 and 2 segregated in core areas during owner absences. Cat 1 chased cat 2 approximately once every 2 weeks during shared time on the first floor but was easier to redirect. At a 6-month follow-up, cats 1 and 2 rested near each other and were observed allogrooming. They were still separated when owners were not home, and a single urine-marking incident had occurred (on an owner's luggage upon return from vacation; it was advised that luggage be quickly placed out of cat 1's reach in this situation). The owners were satisfied with the progress and wished to continue the prescribed medications and use of synthetic pheromone products under the guidance of the rDVM. A follow-up CBC and serum biochemical analysis was recommended, which the owners were to pursue with the rDVM. One year after the initial behavioral consultation, the owners had continued with the patient's treatment plan and were satisfied.

Footnotes

a.

Nature's Miracle Oxy Stain and Odor Remover, Spectrum Brands Inc, Blacksburg, Va.

b.

Anti Icky Poo Odor Remover, Mister Max, Temecula, Calif.

c.

Feliway Original, CEVA Animal Health, Lenexa, Kan.

d.

Feliway Scratch, CEVA Animal Health, Lenexa, Kan.

e.

Feliway Multi-Cat, CEVA Animal Health, Lenexa, Kan.

f.

Wedgewood Pharmacy, Swedesboro, NJ.

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