Animal Behavior Case of the Month

M. Leanne Lilly Behavioral Medicine Service, Department of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210.

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Statement of the Problem

A cat was evaluated because of urination outside the litter box and altercations with another cat living in the same household.

Signalment

The patient was a 7-year-old 4.4-kg (9.7-lb) spayed female domestic shorthair cat.

History

The patient (cat 1) was found at approximately 1 month of age inside the engine compartment of a car and was adopted into a household with 5 people (2 adults and 3 children) and a 2-year-old spayed female cat (cat 2). There were two 2-layered slot systema litter boxes (one in the kitchen and the other in an upstairs bedroom) that contained pelleted litter, and 2 flat litter boxes that contained clay clumping litter were maintained in the basement. All litter boxes were of standard size, scooped a few times per week, changed when they were odorous or seemed full, and cleaned with a bleach solution every 2 to 3 months.

At 2 years of age, cat 1 began depositing small amounts of urine on socially relevant horizontal surfaces (soiled clothing and the tiled foyer entrance through which all human traffic entered between the house and the garage) in response to the presence of visitors, moves, and family trips. Treatment with amoxicillin–clavulanic acidb (dose and route not documented) and buprenorphine hydrochloridec (0.06 mg, oral transmucosally, q 12 h) had been prescribed by the primary care veterinarian without signs of improvement. Amitriptyline hydrochloride (1.04 mg/kg [0.47 mg/lb], PO, q 24 h) administration was initiated and continued for 1 month with no improvement. Following this, the treatment was changed to buprenorphine (0.01 mg/kg [0.005 mg/lb], PO, q 12 h), diazepam (0.52 mg/kg [0.24 mg/lb], PO, q 24 h), and a glucosamine hydrochloride–chondroitin sulfate joint health supplement.d The family moved to a new home, and for 2 months, cat 1 had episodes of hematuria approximately every 2 weeks, each lasting approximately 5 days. At this time, results of urinalysis revealed hematuria with negative urine culture results, and ultrasonographic examination revealed that the bladder wall was thickened. Acepromazine maleate (0.52 mg/kg, PO, q 12 h for 7 days) and fluoxetine hydrochloride (0.52 mg/kg, PO, q 24 h) were prescribed in addition to diazepam and buprenorphine. The client discontinued fluoxetine treatment after 2 months and noted no change in episodes of hematuria during administration of the drug or after its discontinuation. Cat 1 then began to have episodes of urinating small amounts outside of the litter box for several days in a row, roughly 4 to 6 months apart, for several years. Five months prior to the referral examination, following a family trip, this behavior had escalated to weekly urination outside the litter box in socially relevant spaces (the children's hard and soft seating areas). The client reported that cat 1 always squatted while urinating in undesired locations and did not scratch beforehand or attempt to cover the soiled area afterward, but performed both behaviors when urinating in the litter box. The amounts voided were typically small, even with prolonged squatting in and outside of the litter box. The client often raised her voice when she discovered urine in inappropriate locations. Cat 1 had been confined in the bathroom for 3 consecutive months with the box from the bedroom containing pelleted litter; during that time, the client found small amounts of urine on the floor, bathtub, and countertop, and larger amounts of urine in the litter box, but indicated that cat 1 continued to defecate in the litter box throughout all episodes. The family regularly entertained cat 1 with play, even during confinement. At the time of the referral examination, cat 1 was still receiving diazepam, buprenorphine, and the joint health supplement.

Cat 2 had a history of hissing and swatting when cat 1 walked past. The client indicated that cat 1 always attempted to retreat from these threats, engaging in altercations (described as wrestling) with cat 2 only if unable to get away. Over time, the frequency of these altercations increased to daily, although they could be dispersed with loud verbal reprimands. At the time of the referral examination, there had been no altercation in the previous 3 months because of cat 1's confinement. The clients were considering re-homing or euthanizing cat 1.

Physical Examination Findings and Laboratory Results

The patient vocalized but did not exit the carrier during the appointment. A towel treated with a feline synthetic pheromone spraye was placed over the carrier, and the vocalizations quieted. Examination was performed with the cat in its carrier bottom, as it kept 3 of 4 feet in the carrier when gently tilted. Results of the physical examination, including range of motion of the axial skeletal joints, evaluation of muscle mass, and abdominal palpation, were unremarkable other than a full but pliable urinary bladder. At the end of the examination, the cat was gently slid out of the carrier bottom and released to monitor gait, which was deemed normal. Because of the patient's crouching in the carrier, dilated pupils, and disinterest in voluntarily exiting the carrier even with a gentle tilt, a single dose of liquid gabapentinf (9.0 mg/kg [4.1 mg/lb], PO) was dispensed to facilitate handling for venipuncture.1,2 A CBC, serum biochemical analysis (including total thyroxine concentration), and analysis of a urine sample collected by cystocentesis were performed by the primary care veterinarian 3 days after the behavioral consultation. Serum albumin concentration was slightly high (4.1 g/dL; reference range, 2.2 to 4.0 g/dL), but the finding was not considered clinically relevant. No other signs of dehydration were found (BUN concentration, Hct, and PCV were all within the respective reference ranges). Alkaline phosphatase was low (10 U/L; reference range, 14 to 111 U/L), but this was also not clinically concerning.3,4 Urinalysis revealed concentrated urine (specific gravity, 1.049), 3+ hematuria by dipstick with 75 to 100 RBCs/hpf on microscopic examination (with 0 to 3 RBCs/hpf considered normal), 4+ proteinuria by dipstick (> 500 mg/dL), and struvite crystalluria (1 to 5 crystals/hpf). There were no bacteria seen in the sediment on microscopic evaluation. Further evaluation of the urinary system, including radiography and culture of a urine sample, was recommended but declined by the owner.

Diagnosis

Diagnoses of stress-related urine marking and feline idiopathic cystitis (FIC) were made. The small volumes of urine, socially relevant placement, correspondence with stressful events or changes in the household, and lack of digging and covering behaviors outside the litter box were supportive of urine marking, rather than normal urination behaviors or toileting in undesired locations.5–7 Although marking classically involves urine deposition on vertical surfaces, horizontal (squatting) placement is also reported, albeit infrequently.5–7 Hematuria does not rule out urine marking, and this finding was consistent with the concurrent diagnosis of FIC in the cat of the present report.8 Differentiating between urine marking and toileting behavior in inappropriate sites is critical: marking is often attributable to anxiety or environmental or social stressors independent of the litter box.9 Conversely, toileting problems may be associated with a wide array of factors related to the litter box, such as litter or substrate aversion or preferences, hygiene, box location, and issues with access such as having to pass fear-inducing locations or being confronted by other animals (eg, resource guarding by other cats).7,10 Determining which factors are involved necessarily dictates treatment of this condition. Toileting in sites outside the litter box as a result of substrate type, box, or location aversions or preferences was not considered likely, and resource guarding by cat 2 was also not suspected because cat 1 consistently used a litter box for defecation and deposition of large amounts of urine. In addition, cat 1 always covered its feces in the litter box and did not show particular preferences for locations or substrate types (eg, carpet or bedding) other than the soiling of socially relevant locations or items (the entry to the house and children's seats and clothing).7,10

Feline idiopathic cystitis is an inflammation of the bladder for which a definitive cause is unknown. Clinical signs of the disease, including stranguria and hematuria,11,12 are recognized sequelae of stress.13–16 Chronic stress from household changes and threats from cat 2 likely resulted in a recurrent cycle of pain associated with urine marking and toileting7 for cat 1. Recurrent pain has been shown to perpetuate sympathetic activation in cats with FIC17–19,g and in people with interstitial cystitis or female urethral syndrome.20,21 This likely contributed to the persistent FIC signs12 despite the restriction of cat 1 to a single room to avoid agonistic encounters. Additionally, confinement may have also decreased enrichment, potentially contributing to FIC.14

The risk of a urinary tract infection in cat 1 was low, given the findings of concentrated urine, inactive sediment, and no frank bacteriuria and considering that approximately 2% of cats < 10 years of age with periuria are reported to have urinary tract infections identified by culture.8,11,22 Because of this, antimicrobial treatment was neither warranted nor in keeping with good antimicrobial stewardship without a positive urine culture result and susceptibility testing.22 Culture of a urine sample, radiography, ultrasonography, and cystoscopy could have been helpful in definitively ruling out uroliths, infection, and neoplasia.11 Metabolic and endocrine causes (eg, renal disease or diabetes mellitus) were not supported by the results of clinicopathologic testing. Litter box aversion owing to musculoskeletal pain was not suspected because the patient had a normal gait and normal range of limb motion during examination and was reported to have normal ambulation (ie, jumping, running, and playing) at home. However, radiography may have ruled this out more definitively.23,24

Aggression between household cats can arise from a variety of motivations, such as fear, territorial defense, and social status–related aggression.25,26 Cat 1 did not respond aggressively to cat 2, and no aggression diagnoses were made for cat 1; however, frequent aggressive threats from the other cat likely further contributed to cat 1's stress and urine-marking behaviors.5,9

Treatment

A comprehensive plan including medication, environmental enrichment, and reduction of social tension between the cats was implemented. Because a delay in improvement might pose a risk for relinquishment or euthanasia in this situation, the treatment modalities were started simultaneously for urine marking, FIC, and intercat aggression.

Management of FIC focused heavily on environmental changes and enrichment14,18 for resolution and prevention of clinical signs.12 This included daily play sessions, maintenance of vertical resting and hiding spaces, and increased resource opportunities for cat 1 in and out of its confinement area.14 Had daily play sessions been insufficient to meet enrichment needs, food puzzles or food toys could have been used.14,27 Initially, the patient's confinement was maintained because house soiling can substantially damage the human-animal bond.28–30 Previous buprenorphine treatment had been insufficient for presumed pain associated with urination, and gabapentin,f compounded in a flavored liquid at the veterinary medical center pharmacy to allow for accurate dosing, was prescribed instead for management of chronic bladder pain31,32 and relief of anxiety.1,2 The gabapentin dosage was 3.13 mg/kg (1.42 mg/lb), PO, every 12 hours. Gabapentin is a voltage-gated Ca2+ channel (α2-δ subunit) blocker despite being designed as a γ-aminobutyric acid analogue.31 It has no direct effects pertaining to the neurotransmitter γ-aminobutyric acid or its receptors, but has been shown to alleviate signs of osteoarthritis pain33 and anxiety in cats.1,2 Reported adverse effects included sedation and ataxia. Continued buprenorphine use was recommended until hematuria was fully resolved. Benzodiazepines have been used for treatment of cats that are the recipients of aggression from other household cats and for treatment of elimination disorders.34 These drugs have a rapid onset of action.35 However, diazepam had not provided resolution of clinical signs in this patient, and the drug is associated with a risk of hepatic toxicosis in cats36,37; therefore, the dosage was reduced to 0.28 mg/kg (0.13 mg/lb), PO, every 24 hours for 5 days and then stopped. To gain rapid anxiolytic benefits from a benzodiazepine, lorazepam administration was started (0.028 mg/kg [0.13 mg/lb], PO, q 24 h).35,38 Lorazepam was considered safer than other benzodiazepines owing to a lack of active metabolites produced by the liver.35 Extralabel drug use, appetite stimulation, increased risk of sedation in combination with other medications, and risk of disinhibition of aggression were discussed with the client for both medications.26,35 Additionally, lack of long-term studies in cats and the potential for dependence and habituation35 were discussed with the client.

No apparent benefits had been seen when cat 1 was administered fluoxetine or amitriptyline, although the dosages were at the low end of the therapeutic range for both drugs. Previous reports support the utility of fluoxetine for urine marking39 and of amitriptyline for management of idiopathic cystitis40 in cats. Although 1 study41 of cats found that fluoxetine treatment was associated with a > 90% decrease in the rate of periuria in 8 weeks, the client was adamantly uninterested in administering fluoxetine at higher doses. Higher doses of amitriptyline were not considered because of concerns about anticholinergic effects and lower reported efficacy (improvement of signs in 60% of treated cats)42 for treatment of FIC and urine marking, compared with fluoxetine (improvement in 100% of treated cats),41 as well as a previously reported lack of improvement for cystoscopic abnormalities and increased risk for cystic calculi.40,42 Paroxetine and clomipramine were similarly not selected because of the potential for anticholinergic effects to exacerbate stranguria,41,43,44 although several reports39,45 provide evidence that clomipramine can be successfully used to treat urine-marking (spraying) behaviors in cats. Sertraline, an alternate selective serotonin reuptake inhibitor, was considered, especially for a long-lasting option once the imminent threat of euthanasia had passed. Sertraline, like fluoxetine, increases serotonin in the synapse by downregulating presynaptic autoreceptors and lacks anticholinergic adverse effects,43 although it has not undergone placebo-controlled clinical evaluation in cats with periuria. Because of known poor transdermal bioavailability (< 10% to undetectable for behavioral medications studied [buspirone, amitriptyline, and fluoxetine46,47]) and a lack of available studies for other medications, oral administration was chosen for all medications to maximize treatment effects and the chance of a positive outcome. If taking medications proved stressful to the patient, compounding of medications from commercially available products into flavored oral treatments would be most likely to maintain bioavailability and in keeping with AVMA best practices.

A dieth with ingredients that can decrease bladder inflammation and increase water intake48 was suggested as an additional management option.12,20,49 Treatment of soiled spots with an enzymatic cleaner,50 the use of incident logs to record periuria with or without hematuria, and use of the generally preferred clay clumping litter7 instead of pelleted litter in the bathroom litter box were recommended; if litter box use for large amounts of urine and consistent covering of feces had not been reliable across all other treatment attempts and homes, providing a large, open, nonsifting box with clumping clay litter or a litter cafeteria would have been warranted.6

To reduce chronic stress associated with social tension between the cats, complete initial separation (keeping cats in areas separated by a closed door with draft protectors) was also warranted. This allowed for no interactions apart from desensitization and counterconditioning, which is a mainstay of managing intercat aggression.51 A conditioned positive response was to be created first by exposing each cat to the other's scent (a cloth that was rubbed over the other cat) paired with a food reward.26,51 Once cat 1 enthusiastically approached the cloth bearing cat 2's scent, the owners were instructed to rub the cloth linearly along cat 1's body from cheek to rump. The same procedure was to be performed for cat 2 with a cloth bearing the scent of cat 1. Because of cat 1's temporary confinement, this activity replaced passive scent exchange commonly recommended when treating intercat aggression.26,51 Standard desensitization and counterconditioning was recommended, with the owners using baby gates to block the cats’ access to each other during supervised sessions while each cat was provided a favored food; the distance maintained between cats was to be incrementally decreased over time.51,52 The owners were advised to start with the cats as far apart on either side of the barrier as possible given the size of the bathroom (approx 20 feet) and to decrease the distance by < 1-foot increments over several repetitions of this exercise, as long as the cats showed no signs of stress. Once both cats were eating on either side of the barrier, the exercise was to be repeated without a barrier, initially increasing the distance between cats to several feet to prevent altercations, then incrementally decreasing the distance over several repetitions of the exercise.

Both cats were to be trained to use go-to spots on cue with positive reinforcement methods.53 The owners were advised to select a specific location for cat 1 in the bathroom designated for its primary use and to choose any preferred spot away from that room for cat 2. The use of vocal reprimands was discouraged because this could increase fear and anxiety and by extension exacerbate the undesired behaviors for which they were seeking treatment.51,53 Instead, the owners were instructed to use go-to cues as a strategy to disrupt any social tension between the cats.51,52 Potential risks and safety issues related to breaking up altercations, such as avoiding handling highly aroused cats, were also discussed.26,52 Systematic expansion of cat 1's environment by incrementally increasing supervised access to other parts of the house was discussed with the client. Use of a diffuser with synthetic feline-appeasing pheromone54,55 was discussed but declined.

Follow-up

Two weeks after the initial behavioral consultation, the client reported that cat 1's behavior was friendlier after discontinuing diazepam and starting lorazepam treatment. The switch to clumping litter had been made, gabapentin was being administered, and the hematuria had resolved. The client had discontinued buprenorphine per initial instructions. However, urine deposits inside and outside the litter box were small. A week later, the client reported that the previously observed prolonged squatting had ceased and that cat 1 seemed even friendlier. Both cats would eat on opposite sides of the closed bathroom door without overt signs of aggression or stress. Cat 1 was depositing only quarter-sized urine puddles but was consistently using the litter box for urination.

Cat 1 continued to use the litter box exclusively until day 47 after the consultation, when the client was late refilling the cat's medications following a trip; urine deposits with and without hematuria were found outside the litter box. Buprenorphine treatment was reinitiated at the previous dosage until 1 week had passed without visible hematuria. The frequency of lorazepam administration was increased from 24-hour to 12-hour intervals. By day 60, the client was allowing cat 1 out of the bathroom when intending to provide direct supervision; this resulted in hissing from cat 2, but the cats could be separated by use of the go-to cues, and no physical contact ensued. The cats had graduated to eating 12 feet apart without being separated by a barrier during desensitization-and-counterconditioning sessions. Cat 1 had no periuria for multiple weeks, and the client began transitioning the cat to the recommended diet.h

On day 75, cat 1 began howling constantly, which the client described as previously indicating that the cat was “done with confinement.” Cat 1 was let out of confinement for a few hours per day. During this time, vomited food and hair were frequently found throughout the house. The client was counseled on risks associated with vomiting and potential causes, including dietary intolerance from the recent food change. The client elected to give both cats unlimited access to the house, and the family left for a 4-day trip. No incidents of periuria were reported after the trip, but intermittent vomiting persisted. A gastrointestinal evaluation including physical examination, fecal evaluation, and laboratory analyses was recommended to investigate potential parasitic or metabolic causes of vomiting56 but was declined by the client. A diet change was encouraged as well.56

Five months after the initial behavioral consultation, cat 1 had complete access to the house and had no signs of periuria. The owners were feeding a commercially available cat foodi (type and flavor not specified), and vomiting had ceased. Fourteen months after initial consultation, the client sent photos of the cats in social contact (with cat 1's shoulder and chin touching 2's rump), sharing the couch, and sharing a bed. Cat 1 had consistently used the litter box without hematuria for 1 year, and the cats had been altercation-free for 6 months. Lorazepam and gabapentin were still being administered to cat 1 at the same dosages.

Discussion

The clinical and diagnostic approach to urine deposition problems in cats classically involves separating issues of elimination or toileting from marking behaviors.7 Although urine-marking behavior is not typically associated with any lower urinary tract abnormalities,9 the stress-mediated mechanisms for urine marking and sterile hematuria are in no way mutually exclusive.18,g In this case, evaluation and treatment were facilitated by administration of gabapentin, which was custom compounded from a commercially available product by a licensed pharmacy in compliance with state and federal laws. This also formed a mainstay of treatment for presumed bladder discomfort31–33 and potential anxiolysis.1,2 Although ruling out underlying medical conditions is essential when performing any behavioral workup,52 the case described here clearly demonstrated the interplay between a physiologic problem (hematuria) typically associated with inappropriate toileting and a behavioral outcome (marking); both are often influenced by social tensions between cats.

Footnotes

a.

Sifting Cat Litter Pan with Frame, Van Ness Plastic Molding Co Inc, Clifton, NJ.

b.

Clavamox, Zoetis, Parsippany, NJ.

c.

Buprenex, Indivior Inc, North Chesterfield, Va.

d.

Cosequin, Nutramax, Lancaster, SC.

e.

Feliway Classic, Ceva Animal Health Inc, St Louis, Mo.

f.

Compounded from commercially available generic capsules produced by Ascend Laboratories LLC, Parsippany, NJ.

g.

Westropp JL. Evaluation of the effects of stress on the sympathetic nervous system and hypothalamic-pituitary-adrenal axis in cats with feline interstitial cystitis. Doctoral thesis, Department of Veterinary Clinical Sciences, The Ohio State University, Columbus, Ohio, 2005.

h.

c/d Multicare Feline Stress diet, Hill's Science Diet, Topeka, Kan.

i.

Royal Canin, Mars Inc, MacLean, Va.

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