Animal Behavior Case of the Month

Christine D. Calder Department of Clinical Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS 39762.

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Statement of the Problem

A dog was evaluated at the behavior service of a veterinary teaching hospital because of lunging, charging, biting, and snapping at visitors in the home and yard.

Signalment

The patient was an otherwise healthy approximately 2-year-old 25.8-kg (57.8-lb) neutered male Labrador Retriever mix.

History

The dog had been acquired by its female owner at approximately 9 months of age from a local shelter. Prior to adoption, the dog and a littermate had been surrendered to the shelter after being found in a closet during a house fire. The dam and a second littermate died in the fire. The current owner volunteered at the shelter and stated that she had adopted this dog because she was concerned that it would be euthanized because of its fears. At the time of the examination, the dog had lived with the current owner for approximately 1 year and 2 months, and the household included 2 spayed female dogs (one 13 years old and the other 7 months old). The patient was reported to have a friendly relationship with both dogs. No other people were living in the house, but the owner had frequent overnight visits from family members and friends. All vaccinations, including vaccination against rabies virus, were current.

Over the past 6 months, the dog's behavior had progressed from running and hiding with ears back, head down, pupils dilated, and tail tucked and avoiding eye contact with unfamiliar people to lunging, snapping, and grabbing of pant legs when visitors moved past or changed from sitting to a standing position. Recently, the dog had snapped at a visiting male family member without breaking the skin when the visitor stood up and walked toward the owner of the dog. Another incident had occurred a few months prior to this, when the dog, which had free access to the front yard at the time, charged the front gate (barking, tail down, and ears back) as it was opened by a female neighbor. The dog charged and jumped on the neighbor and scratched the skin of 1 hand with its teeth. Other than the neighbor, the dog appeared to be less fearful of women, and when the owner's mother visited, the dog would initially hide under the table but would start to follow her around the house after a few hours and solicit petting from her.

Approximately 1 year before the initial consultation at the behavior service, the owner had sent the dog to a boarding and training facility. The dog had been housed on the trainer's farm for a few weeks, but when it was returned home it still had fearful behaviors and had begun showing signs of aggression around food. This latter aggressive behavior had resolved by the time of the examination, and the owner was working with a trainer who used a reward-based approach and also served as a dog walker for the patient.

Physical Examination Findings and Laboratory Results

The dog did not have any obvious physical abnormalities on initial evaluation at the behavior service. It would not take treats and spent most of the consultation curled up behind a table in the corner of the room. The dog remained withdrawn with its ears and the corners of its mouth drawn back, and intermittent panting, dilated pupils, and avoidance of eye contact were observed. A physical examination, serum biochemical analysis, CBC, heartworm antigen test, and measurement of serum total thyroxine concentration had been performed by the referring veterinarian within the previous few weeks with no clinically relevant abnormalities noted. After consultation with the owner and considering the signs of fear shown by the dog, it was decided not to create additional stress by performing another full physical examination and venipuncture.

Diagnosis

Avoidance and aggressively defensive behaviors can be a result of pain, metabolic disorders, or brain lesions.1–12 The unremarkable recent physical examination findings, observations during the consultation, laboratory findings, and the pairing of fearful behavior with a specific stimulus indicated that the dog's clinical signs did not have a primary medical cause. Differential behavioral diagnoses when an aggressive response is displayed toward unfamiliar people include fear-based aggression, territorial aggression, predatory behavior, play aggression, and pain-induced aggression.1–5,8 Play aggression was considered unlikely because the aggressive behaviors included threatening behaviors (growling and lunging) and did not occur in the context of play.1–5 The absence of stalking and chasing behaviors made predatory behavior less likely.1–5 A physical examination and history did not indicate the presence of painful conditions, making pain-induced aggression less likely. The aggressive behavior that was observed when unfamiliar people entered the yard or house could be considered territorial aggression.1,2,4,6 Territorial aggression is often directed at unfamiliar people or dogs (or both) that enter the house or yard, and the display of aggressive behaviors typically does not occur away from the home environment.1,2,4,6,7 The patient's hiding and defensive body language occurred on and off the owner's property and intensified once visitors entered the home, which was more indicative of fear than territorial aggression. However, fear can influence territorial aggression, and in some cases, fear and territorial aggression may be considered the same condition.4,6–8 A diagnosis of fear-based aggression was made.

Fear-based aggression is identified by a display of behavioral clinical signs such as positioning with the ears held back, tail tucked, head down, and pupils dilated; avoiding eye contact; and otherwise exhibiting withdrawn behavior.1,2,5,6 In some cases, barking, growling, lunging, snapping, and biting, motivated by fear, are used to remove a perceived threat.1,2,5,6 Fear and fear-based aggression can occur at any age, and subtle signs of fear can appear in young puppies (< 6 months) and intensify as a dog matures.2,4–6 Some breeds appear to have a predisposition to an abnormal fear response from a young age, which indicates a potential genetic component.13 However, as a puppy, this dog had been found in and was believed to have been living in a closet, and therefore, inadequate socialization during the sensitive socialization development period was likely a contributing factor to the behavioral problems.1,13

Treatment

For environmental management, the owner was instructed to create a safe haven in the house where the dog could be placed to avoid contact with known triggers for its aggressive behavior or where it could retreat on its own.4,6 In this case, the dog's crate was chosen as the safe haven because it had been used in the past and the dog appeared to be comfortable in it. The crate was relocated away from the front entrance of the house to a quieter location, and the owner was instructed to confine the dog to the crate prior to visitors arriving at the house. Food-dispensing toys were to be given to help classically condition a more positive emotional state during confinement and provide species-specific enrichment, therefore reducing stress. Over time, the most frequent visitors and neighbors could be gradually reintroduced to the dog to help create a more positive emotional response toward visitors. In the meantime, neighbors were instructed not to lean over or reach for the dog through the fence, and it was recommended that the owner condition the dog to wearing a basket muzzle.

The owner was instructed not to grab for the dog's collar, as this reduces the ability to choose avoidance and makes barking, growling, and biting more likely.7,14 Positive punishment, including verbal correction, was discouraged because this could lead to increased anxiety, frustration, and aggression.1,4–6,15 Communication through a cue-response-reward system was prescribed to establish consistent and predictable interactions between the dog and owner and to ensure only desired, nonanxious behaviors were rewarded by the owner. The owner was instructed on how to teach focus behaviors with verbal cues to look and touch. These behaviors would teach the dog that making eye contact and physical contact with hands elicit rewards, and then these behaviors could subsequently be used during reintroduction and for response substitution when visitors changed positions or moved around the room.1,2,4,6

The owner was instructed in the use of classic counterconditioning to reduce the dog's reactivity to the sound of the front gate opening. The owner was instructed to stand outside the gate and toss food on the ground as the latch was opened. This was to be repeated 3 to 4 times weekly for 3 to 5 minutes at a time until the dog no longer barked and charged in response to the noise of the latch opening on the front gate.

It was difficult to minimize the dog's exposure to stimuli that induced signs of fear, and its reactions had intensified recently; therefore, psychotropic medications were recommended in addition to behavior modification. At present, there are no medications labeled to treat aggression in dogs. Reduced serotonergic function has been shown to be associated with impaired impulse control and aggressive behavior.4,16,17 Fluoxetine, a selective serotonin reuptake inhibitor (0.4 mg/kg [0.18 mg/lb], PO, q 24 h for 7 days, then increased to 0.8 mg/kg [0.36 mg/lb], PO, q 24 h) was chosen because blockage of serotonin reuptake and downregulation of serotonin receptors has been shown to decrease signs of anxiety and aggression.18 Fluoxetine was chosen instead of a tricyclic antidepressant because it is more selective for serotonin and it has less potential for adverse effects.18 The owner was informed that use of the drug was extralabel and was advised of the potential for adverse effects such as sedation, decrease in appetite, vomiting, diarrhea, tremors, and increased signs of anxiety.18 Since improvement may not be evident for 3 to 4 weeks or longer in response to fluoxetine treatment,18 trazodone (2 mg/kg [0.91 mg/lb], PO, q 12 h) was also prescribed for the first 2 weeks for a more immediate effect.19 Trazodone, a serotonin antagonist and reuptake inhibitor, can have calming and anxiolytic properties and is usually effective within 45 minutes after administration.19–22 The owner was advised that trazodone use in dogs is also extralabel, and adverse effects are uncommon but potentially include mildly soft feces or diarrhea, vomiting, sedation, and increased appetite.19–21 In human males, priapism rarely occurs with trazodone treatment, and although this effect has not been reported for dogs, the drug should be used cautiously for sexually intact males.19

Follow-up

Two months after the initial consultation, electronic communications with the owner revealed that the dog was responding well to the medications with no apparent adverse effects. The owner felt that the dog was more relaxed and less reactive to small changes in the environment, and because of these positive changes, the owner had decided to stop daily administration of trazodone on her own. At the time of communication, the owner's mother was visiting from out of town. The dog had been responding favorably to having an unfamiliar visitor in the home. The dog was being provided with frequent food rewards from the mother, and she was deliberately moving more slowly around the house to prevent triggering a fearful response from the dog. Although the dog would still bark in the morning when the owner's mother first awoke and moved around the house, it then appeared to relax and barked less throughout the day. The dog's crate had been moved to the dining room so that it was away from the front door, and it was then moved into a bedroom at the back of the house during holidays when overnight guests were present in the home. The owner indicated the dog would freely enter its crate without prompting and would relax quickly when visitors arrived. However, 1 week prior to these follow-up communications, the dog had lunged and jumped at the owner's mother while the owner was at work and the dog had appeared to be more agitated in general on that day. The owner called the referring veterinarian, who recommended resuming administration of trazodone (2 mg/kg, PO, q 12 h, for 7 days). The behavior was reported to improve with the treatment.

Four months after the initial behavioral consultation, the dog was brought to the hospital for a recheck evaluation. At this time, the owner was still struggling to gain compliance with simple cues such as sit but planned to increase her efforts in reinforcing these behaviors. The process of conditioning an alternative emotional response to the presence of neighbors and the click of the gate opening was started as previously instructed. The dog would freely approach the fence with friendly body posture in anticipation of treats when the neighbors were in their own yard on the other side of the fence. The dog was doing well with the fluoxetine treatment and appeared less fearful in general. The owner continued to administer trazodone on an as-needed basis for events that were considered more stressful for the dog. The plan was to continue with classic counterconditioning of the response to the gate click and placing the dog in its crate before visitors arrived until the foundation and focus behaviors such as look and touch could be reliably elicited.1,4,6

At a recheck evaluation 6 months after the first visit, the owner reported a new fearful response from the dog to the sound of a clicker that was used for training and to the introduction of certain enrichment devices, such as a muffin tin filled with pieces of food and covered with tennis balls. The dog would bark, back away, or run into the other room when the clicker or muffin tin enrichment device was used. Other environmental noises (eg, storms, cars, alarms, or fireworks) did not appear to cause a similar reaction at that time, but the dog responded to the presence of novel items in the house such as the owner's new coffee pot or a soccer ball by avoiding these items and barking at them. Muffling the clicker with bubble wrap or substituting for the sound by clicking of the tongue or use of a small pinpoint-style flashlight (in a manner used for training dogs with hearing deficits) were suggested as alternatives. Since the previous recheck evaluation, the dog's relationship with the neighbors had improved substantially. The dog was no longer reacting to the opening of the gate and would eagerly take food rewards offered through the fence. It also showed anticipation of food rewards when the neighbors were in their yard and approached the fence with its tail up and wagging and ears and body relaxed. In the examination room at this visit, the dog would not approach staff members but would take food treats tossed near it. The dog had not shown aggression toward visitors since the first recheck evaluation; the fluoxetine treatment was continued at 0.8 mg/kg every 24 hours, but because of the new fearful response to the training clicker, muffin tin, and novel items in the home environment, gabapentin (4 mg/kg [1.8 mg/lb], q 12 h) was additionally prescribed. Gabapentin, considered an anticonvulsant and effective against neuropathic pain, is structurally similar to γ-aminobutyric acid (GABA) but does not appear to have an effect on GABA receptors.5 Although not specifically labeled for treatment of fear and reactivity, gabapentin may have an anxiolytic effect by increasing the amount of GABA in brain cells and, as a result, increasing blood serotonin concentrations.4,5,23 Gabapentin has been administered alone or in combination with a selective serotonin reuptake inhibitor or tricyclic antidepressant to reduce overall reactivity and signs of anxiety with relatively few adverse effects.4,5 Gabapentin was chosen instead of trazodone at this time to reserve trazodone for administration when the dog was exposed to more intense triggers such as unfamiliar visitors or boarding.

In follow-up communications at 8 months after the initial consultation, the dog was doing well. No adverse medication effects were noted, and the dog appeared more relaxed overall. It no longer barked or reacted when the neighbor walked into the backyard and would readily approach the neighbor and solicit petting from her. Ten months after the initial appointment, continued improvement was reported. A friend of the owner had recently visited, and the dog did not bark or lunge at her. The visitor provided food rewards, and the dog started to nudge her leg for more. The friend was then able to walk around in the house, and the dog either followed her or remained in its bed. Neighbors could freely enter the yard and house with little to no reaction from the dog. The gabapentin and fluoxetine treatments were continued, and the trazodone was only given during stressful events such as boarding.

Thirteen months after the initial consult, the dog's behavior continued to improve with no sign of fear or anxiety around neighbors or visitors in the home. At this time, continued treatment with fluoxetine and gabapentin at the same dosages was advised, with trazodone administration at the previous dosage as needed. An annual CBC and serum biochemical analysis were recommended; if the improved behavior continued, reduction of the dosage or possibly discontinuation of the gabapentin, fluoxetine, or both would be recommended in the future.

References

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