Animal Behavior Case of the Month

Statement of the Problem
A dog was examined because of a 4-month history of excessive salivation and destruction that occurred when the owners were absent.

Signalment
The dog was a 16-month-old castrated male Brittany Spaniel that lived in a suburban home with 2 adults and 2 teenage children.

History
The dog had been obtained from a breeder at 4 months of age. The owners had taken the dog to puppy socialization and obedience classes, but the dog was not crate trained as a puppy and was initially allowed full access to the house when the owners were not home. No problems were identified during the first winter and spring, and during the first summer, the dog was rarely left alone for long periods. When the children returned to school in the fall, however, the dog was left alone during the day several times a week and began chewing the couch and carpeting. For this reason, the owners began putting the dog in a crate when they were away, but they would return to find the dogs chest and the crate floor soaked with saliva.

Blankets or rugs that were next to the crate would be pulled into the crate and shredded, even if the owners were absent for only a short time. The male owner noted that when he shut down his computer before leaving for work, the dog would begin to pant, pace, and follow him closely. No other cues elicited these behaviors. The dog would not eat food left for it until its owners returned and was extremely exuberant when the owners returned from an absence. When the owners were home, the dog followed various family members from room to room and sought their attention frequently by, for example, attempting to climb into their laps or nudging them with its nose. The dog did not chew on household items when the owners were home, bark at people or dogs outside the house, or show fearful responses to noises. One week prior to examination, the dog's regular veterinarian prescribed clomipramine (25 mg, PO, q 24 h). No laboratory testing was performed.

Physical Examination Findings and Laboratory Test Results
Results of a physical examination were unremarkable; the dog weighed f9 kg (42 Ib). To help rule out medical conditions that might have been contributing to the behavior problems and to assess metabolic func-
tion prior to prescribing any medications, a CBC and serum chemistry profile were performed and serum thyroxine concentration was measured as a screening test for thyroid gland disease. Results of all laboratory tests were within reference ranges.

During the initial interview, the dog greeted everyone present and explored the room. The dog frequently sought attention from the female owner, but when the female owner was instructed to avoid interacting with the dog, it quieted after several minutes and lay down. A videotape of the dog in its crate while the owners were gone was reviewed. The dog could stand in its crate, but the crate was too small to allow the dog to raise its head or completely extend its legs when lying on its side. Within minutes after the owners departed, the dog began licking its lips, whining, salivating, and biting at rugs and the crate door with increasing intensity.

Diagnosis
Excessive salivation can result from anticipation of food, anxiety physical abnormalities of the oral cavity, or nausea secondary to metabolic or gastrointestinal tract abnormalities.15 Destruction by chewing or shredding can occur because of separation anxiety, barrier frustration, age-related chewing or play behaviors, or fearful or territorial responses to external stimuli.

Anticipatory salivation was considered unlikely in this dog, despite the presence of food in the crate, because the dog would not eat the food until the owners had returned. Oral cavity abnormalities and nausea were ruled out on the basis of results of the physical examination and laboratory testing. In addition, the excessive salivation occurred only when the dog was in the crate. Age-related chewing and territorial or fearful responses to external stimuli were not observed when the owners were home, decreasing the likelihood that they were responsible for the dog's destructive behavior when left alone. In addition, the problem behaviors occurred every lime the dog was left alone, even for short periods, which suggested that they were not a response to sporadic exposure to external stimuli. Also, the dog received regular training and exercise to provide outlets for age-related play behaviors.

It was considered possible that barrier frustration (ie, resistance to confinement"1) had been contributing to the dog's behavior problems while in the crate, particularly because the crate was small and the dog had not learned to be relaxed in the crate prior to being confined in it for extended periods.' To rule out barrier frustration as a cause of the dog's destructive behavior, it would have been necessary to videotape the dog when left alone out of its crate and to observe the dog when in its crate with the owners present. However,the owners refused to leave the dog alone loose in the house for videotaping and because crate confinement had been the dog's most reliable departure cue for months, it would have been difficult to independently evaluate the dog's response to being put in the crate with the owners present.

Separation anxiety was diagnosed on the basis of the dog's anxious responses to departure cues, anorexia in the owners' absence, and the videotape evidence of behaviors consistent with anxiety (eg, lip licking) and separation distress (eg, excessive salivation, whining, and escape attempts12'6). Barrier frustration remained as a possible contributor to the dog's problem behaviors. Although themselves not diagnostic for separation anxiety,1 additional findings supporting the diagnosis of separation anxiety included the hyper-attachment behaviors of the dog when the owners were home and the overly excited greeting behavior on the owners' return.'1 The problem behavior had developed after several months of constant exposure to family members, which is typical for some dogs with separation anxiety that have learned to depend on their owners' presence for emotional stability.' Intense attachments may be more likely in dogs that have experienced a disrupted home placement,"1 and the dog was obtained at 4 months of age, which may have disrupted primary attachments formed during the socialization period.8

Treatment
The owners were advised to follow a behavior modification plan that incorporated independence training, habituation to predeparture cues, and desen-sitization and counterconditioning to confinement and separation. Antianxiety medications were prescribed to facilitate the behavior modification plan.

To teach the dog to be more independent, the owners were advised to avoid inadvertently reinforcing attention-seeking behaviors. For example, they were instructed to stand up without interacting with the dog if it tried to jump into their laps and to not pet the dog in response to solicitation but to only pet the dog if they had initiated the interaction and the dog had complied with a request. They were also told to close the door behind them if they went briefly into another room. The owners were instructed to ignore the dog for 15 to 30 minutes prior to their departure and after their return. While initially they could let the dog out of its crate when they returned, they were instructed to do so without greeting the dog and to gradually work towards being home for several minutes before releasing the dog from the crate. They were also instructed to teach the dog to obey a ''stay" command by giving praise and food rewards when the dog was relaxed at increasing distances from them.

The owners were instructed to turn the computer on and off frequently when they were home and to leave it running when they were gone. They were asked to watch the dog's reactions to typical predeparture acts, such as putting on their coats or picking up their keys, and if the dog showed any anxious response to these acts, to perform them frequently without subsequently leaving the house. The owners were advised to buy a larger crate for the dog so that the dog could stand with
several inches above its head and could stretch out fully when lying on its side.

They were instructed to frequently ask the dog to go into the crate for treats and, while the dog was eating, to shut the door momentarily and then open the door again, allowing the dog to leave but not interacting with the dog. As the dog became more relaxed with the door shut momentarily, the owners were to gradually extend the time the door was closed until the dog could be left calmly in his crate for 10 to 15 minutes while the owners were home and not leaving. At that time, they were to begin incorporating the departure cues they had been repeating into the routine. When the dog was calm for several sessions, they could begin leaving the home for 1- to 2-minute periods, but were to use a video camera to monitor the dog's reactions and extend the duration of their absences on the basis of calm responses.

A puzzle toy containing high-value food items was to be left for the dog during practice sessions and real departures, both as a way of making the sessions pleasurable for the dog and as an indicator of anxiety (ie, the owners would know that the dog was relaxed if the food was eaten). The owners were advised to also offer the puzzle toy at other quiet times so that the dog learned to use the toy to relax' and so the toy would not become a predictor of the owners' departure.

The tricyclic antidepressant clomipramine was prescribed to facilitate a faster response. Clomipramine is used to treat a variety of anxiety-related behaviors'1 and is approved for the treatment of separation anxiety in dogs. The dosage was increased to 40 mg, PO, twice a day because of a report10 that it is more effective when given at a dosage of 2 mg/kg (0.9 mg/lb), twice a day. Because it may take 2 to 4 weeks for clomipramine to have its greatest effects,""1 the benzodiazepine alprazo-lam was prescribed (0.5 mg, PO, 1 hour prior to the owners' departures) to be administered as needed for immediate anxiolysis. Alprazolam is used for rapid relief of anxiety in people12 and panic or phobias in dogs.Q However, the owners were instructed to not use alprazolam during training sessions because of its potential to decrease learning.g12 A test dose was given when the owners were home to test whether the dog would have a paradoxical response.11

Follow-up
Two weeks after the initial examination, the dog reportedly tolerated the owners closing doors between them and followed the owners less often in the house. However, the degree of salivation and destruction while the dog was alone and in the crate were unchanged. One month after examination, the dog would go into the crate voluntarily to sleep when the owners were home and, during a videotaped episode when the owners were absent, was observed to lie down quietly for much of the taping period. Degree of salivation and destruction were not reported. At that time, the owners had been administering alprazolam 2 to 3 days a week, and its use was discontinued without tapering the dosage.

Three months after examination, the owners reported that the dog continued to do well, but they had not videotaped the dog for several weeks. They were instructed to verify the dog's calm response
by videotape and to then begin reducing the dosage of clomipramine by 25% every 2 weeks. Six months and again 12 months after examination, the dog continued to do well with no medication.

References
1. Overall KL. Fears, anxieties, and stereotypies. In: Clinical behavioral medicine for small animals. St Louis: CV Mosby Co, 1997; 209-250.
2. Simpson BS. Canine separation anxiety. Compend Contin Educ Pi-act Vet 2000;22:328-329.
3. McCrave EA. Diagnostic criteria for separation anxiety in dogs. Vet Clin North Am Small Anim Pract 1991:21:247-255.
4. Lindell EM. Diagnosis and treatment of destructive behavior in dogs. Vet Clin North Am Small Anim Pract 1997:27:533-547.
5. Voith VL, Borchelt PL. Separation anxiety in dogs. In: Voith VL, Borchelt PL, eds. Readings in companion animal behavior. Trenton, NJ: Veterinary Learning Systems, 1996:124-139.
6. Flannigan G, Dodman NH. Risk factors and behaviors associated with separation anxiety in dogs. J Am Vet Med Assoc 2001;219: 460-466.
7. Appleby D, Pluijmakers J. Separation anxiety in dogs: the function of homeostasis in its development and treatment. Vet Clin North Am Small Anim Pract 2003:33:321-345.
8. Serpell J, JagoeJA. Early experience and the development of behaviour. In: Serpell J, ed. The domestic dog: its evolution, behaviour and interactions with people. Cambridge. UK: Cambridge University Press, 1995:79-103.
9. Simpson BS, Papich MG. Pharmacologic management in veterinary behavioral medicine. Vet Clin North Am Small Anim Pract 2003;33:365-404.
10. KingJN, Simpson BS, Overall KL, et al, for the CLOSCA (Clomipramine in Canine Separation Anxiety) Study Group. Treatment of separation anxiety in dogs with clomipramine: results from a prospective, randomized, double-blind, placebo-controlled, parallel-group, multicenter trial. Appf Anim Behav Sci 2000:67: 255-275.
11. Horwitz DE Diagnosis and treatment of canine separation anxiety and the use of clomipramine hydrochloride (Clomicalm). J Am Anim Hasp Assoc 2000;36:107-109.'
12. Stahl SM. Drug treatments for obsessive-compulsive, panic and phobic disorders. In: Essential psycliopharmacology. Cambridge, UK: Cambridge University Press, 2000:354-355.

JAVMA, Vol 229, No. 6, September 15, 2006