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Status-related aggression, resource guarding, and fear-related aggression in 2 female mixed breed dogs
Journal of Veterinary Behavior xxx (2015) 1e7
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Case Report
Status-related aggression, resource guarding, and fear-related aggression in 2 female mixed breed dogs Carlo Siracusa* Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 July 2015 Received in revised form 10 November 2015 Accepted 2 December 2015 Available online xxx
Two household dogs, a 2 year, 8-month-old, spayed female, mixed-breed dog, and a 4 year, 1-month-old, spayed female, mixed-breed dog, presented with a history of aggression toward each other, when in possession of food or other high-value items, and when one approached the other while resting. They responded satisfactorily to treatment with serotonergic drugs, avoidance of provocative situations, and environmental and behavioral modification. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: affective aggression dog intra-specific aggression resource guarding
Presentation KF was a 2.7-year-old, spayed female, 14.5-kg, mixed-breed dog, and LF was a 4-year-old, spayed female, 16.3-kg, mixed-breed dog. KF and LF were presented by their owners for aggression between them when in possession of food or other high-value items, and when LF approached KF while resting. History and presenting signs KF was adopted from the local Society For The Prevention Of Cruelty To Animals at 1.5 years of age, and LF was adopted from a local rescue organization at 1 year of age. They lived with their owners, Ms. F. and Mr. Y., and 2 other dogs in a city apartment with 4 rooms (bedroom, living room, dining room, and kitchen). The other 2 dogs living in the apartment were CF, a 7-year, neutered male, mixed-breed dog obtained at the age of 2 years and JF, a 3-year, spayed female, mixed-breed dog obtained at 6 months. CF and JF did not show aggressive interactions between them or toward KF and LF. Historically, all dogs had free access to all the rooms * Address for reprint requests and correspondence: Carlo Siracusa, Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, 3900 Delancey Street, Philadelphia, PA 19104, Tel: 001 (215)-898-6681; Fax: 001 (215)573-7041. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.jveb.2015.12.001 1558-7878/Ó 2015 Elsevier Inc. All rights reserved.
in the apartment. After KF was acquired, there had not been changes in the household. The dogs were walked on a leash outside 3 times per day. The average length of these walks was about 20 minutes. The owners reported that, although LF had historically growled at the other household dogs around food or other items perceived as highly valuable by her (rawhide, real bones, toys, stolen objects .). KF and the other dogs typically responded by lowering their bodies and moving away and such behavior had not led to fights before the incidents described. The owners also described how KF was often “rough” when playing with the other dogs, jumping on and sometimes mounting them, and attempting to continue the interaction when the other dogs disengaged. This aroused interaction did not escalate into aggression and did not require the intervention of the owners to be interrupted. Starting approximately 4 months before the behavior appointment, KF had been staring, growling at and attempting to bite LF when near food or toys, or when LF approached her while she was resting. The first incident of aggression between KF and LF that led to a bite occurred 1.5 months before presentation. According to the description provided by the owners, KF and LF were under the dining room table, whereas CF and JF were under the chairs occupied by the owners, when a piece of food dropped. KF displayed piloerection and, with ears forward, stared and lunged at LF, biting her face and neck without breaking the skin. Mr. Y. promptly interrupted the aggressive interaction by yelling “no.” He detected
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no serious injuries during a visual inspection of the dogs. CF and JF were alert during the aggressive interaction between KF and LF but remained under their respective chairs. Since this incident, the aggressive behavior had escalated in both frequency and intensity. A second incident occurred 5 weeks before the behavior consultation. LF, CF, and JF were resting on the bed together with the owners. When KF jumped on the bed, LF was startled and stared at her. KF stared back and, a few second later, KF lunged at LF and engaged in a fight. CF and JF jumped off the bed and left the bedroom. KF and LF bit each other several times. The owners separated the 2 dogs by grabbing and pulling on their bodies. During this interaction, KF bit Mr. Y. in his hand without breaking the skin. LF suffered bite punctures on her face, leg, and eyelid. KF had punctures on her leg and face. After separation, KF was confined to her crate in the dining room. A veterinarian was seen to treat the injuries. One final incident occurred a month before the consultation, at dinnertime, in circumstances very similar to the first incident described. Also in this case, KF and LF were under the table, while CF and JF were around the table. The owners were not able to confirm if some food had dropped but described that KF stared at LF and stiffened, and then the 2 dogs lunged at each other, snarling and biting. Mr. Y. grabbed KF by her body and pulled her away, while Ms. F. picked LF up. This intervention of the owners did not interrupt the aggressive behavior of KF, who kept trying to reach LF and bit Mr. Y.’s hand, breaking the skin and causing punctures that did not require hospitalization. Both dogs suffered multiple punctures from bites on their face and body that required veterinary treatment. KF was confined to her crate after this incident. After such incidents, LF showed progressively more fear and wariness around KF. The latter was likely to initiate an aggressive interaction with LF when she was excited, barking, and running around, if off leash, or jumping, if on leash (e.g., before going for a walk). This aggressive display could trigger an aggressive response from LF, if the 2 dogs were in proximity and unrestrained. In an effort to correct KF’s aggression and excitability, the owners had tried verbal and physical corrections (staring at the dog, growling at the dog, rolling the dog on his back and holding down (“alpha rolls”), holding the dog on her side, yelling “no,” leash corrections), with no effect. Since the aggression between KF and LF had developed, KF was kept in a crate in the dining room and LF was kept in the bedroom behind a closed door when not supervised by the owners. KF and LF spent time in these areas also when not confined, and did not show signs of anxiety when confined. CF and JF tended to stay away from KF since her aggressive behavior had escalated. When the owners were at home, all the dogs tended to stay nearby; in particular, KF spent more time in proximity of Mr. Y than the other dogs. Both dogs frequently jumped to seek interaction and contact with the owners. However, according to the owners, the proximity of a dog to one or both owners, or receiving attention from the owners, was not a specific trigger of aggression between KF and LF. Aside from the incidental redirected aggression showed toward Ms. Y. when attempting to separate KF and LF during a fight, the 2 dogs did not show signs of aggression directed to the owners. Before the behavior appointment, KF and LF did not receive formal training classes. The owners had taught them basic verbal cues, such as “sit,” using operant conditioning with intermittent reinforcement. Both dogs responded reliably when not excessively aroused, and did not show aggression over treats used as reinforcement. KF’s and LF’s medical histories were unremarkable. Behavioral, physical, and laboratory evaluation KF and LF were kept on separate leashes during the appointment. Both Ms. F. and Mr. Y. were present, each one holding on one
of the dog’s leash. KF was active and playful, whereas LF was more vigilant, continually monitoring KF. At one point when 2 toys were offered, the dogs stared at each other and then KF barked and lunged at LF. The toys were removed. Physical examination, including a neurologic and orthopedic assessment, complete blood count, serum chemistry, and urinalyses for both dogs were unremarkable (Tables 1-6). No source of pain was found. LF’s laboratory tests showed a mild increase of serum gamma-glutamyl transpeptidase (GGTP) and presence of moderate triple phosphate crystals in the urine. Both findings were considered clinically insignificant because they were not associated with specific clinical signs and/or other hematological or biochemical alterations (Stockham and Scott, 2008a, 2008b). Diagnoses Aggressive interactions between household dogs may be the result of fear, social status conflict, resource guarding, inappropriate social skills, and orthopedic pain or other medical problems. Its progression may be also influenced by the outcome of past aggressive interactions, including the response of the owner (De Keuster and Jung, 2009; Landsberg et al., 2013a; Mertens 2002; Overall 2013a). In KF’s case, aggression was consistent with status-related aggression (i.e., aggression due to social status conflict)dwhich can include resource-guarding behaviordbecause the aggression was associated with control over resources and had progressed from submissive body postures to overtly aggressive over time. Several factors may have contributed to this progression, including KF becoming socially mature, repeated exposure to punishment, and sensitization to contexts in which LF was present (Landsberg et al., 2013a; Mertens 2002; Overall, 2013a). The lack of a clear social hierarchy in group of dogs, together with the potential influence of factors other than social status in the development of aggression between dogs of the same group, has made some authors questioning the appropriateness of “dominance aggression” or “status-related aggression” as diagnostic categories (Bradshaw et al., 2009; De Keuster and Jung, 2009; Miklósi, 2015). Fearrelated aggression was considered as a differential diagnosis for KF. However, it was determined that the primary problem for KF was status-related aggression because of the repeated contexts associated with both resources and excitement, and the absence of posturing consistent with fear (Landsberg et al., 2013a; Mertens 2002; Sherman et al., 1996). The aggression that LF historically showed toward KF was diagnosed as resource guarding, based on the aggressive behavior that she exhibited toward any dog that approached when she had a
Table 1 Complete blood cells count (CBC) of patient KF Test
Reference range
Result
Red blood cells Hemoglobin Hematocrit MCV MCH MCHC Platelet count White blood cells Neutrophils Lymphocytes Monocytes Eosinophils Basophils
4.8-9.3 106/mL 12.1-20.3 g/dL 36%-60% 58-79 fl 19-28 pg 30-38 170-400 103/mL 4.0-15.5 103/mL 2060-10,600 690-4500 0-840 0-1200 0-150
7.07 106/mL 16.1 g/dL 45.7% 65 fl 22.8 pg 35.2 g/dL 383 103/mL 7.8 103/mL 4212 2886 234 390 78
MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration.
C. Siracusa / Journal of Veterinary Behavior xxx (2015) 1e7 Table 2 Serum chemistry panel of patient KF
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Table 4 Complete blood cells count (CBC) of patient LF
Test
Reference range
Result
Test
Reference range
Result
Glucose Urea nitrogen Creatinine Total protein Albumin Total bilirubin Alkaline phosphatase ALT (SGPT) AST (SGOT) Cholesterol Calcium Phosphorus Sodium Potassium Chloride Albumin/globuline ratio BUN/creatinine ratio Globuline Lipase Amylase Triglycerides CPK GGTP Magnesium
70-138 mg/dL 6-25 mg/dL 0.5-1.6 mg/dL 5.0-7.4 g/dL 2.7-4.4 g/dL 0.1-0.3 mg/dL 5-131 U/L 12-118 U/L 15-66 U/L 92-324 mg/dL 8.9-11.4 mg/dL 2.5-6.0 mg/dL 139-154 mEq/L 3.6-5.5 mEq/L 102-120 mEq/L 0.8-2.0 4-27 1.6-3.6 77-695 U/L 290-1125 29-291 mg/dL 59-895 1-12 U/L 1.5-2.5 mEq/L
106 mg/dL 15 mg/dL 1.1 mg/dL 6.1 g/dL 3.4 g/dL 0.2 mg/dL 59 U/L 42 U/L 27 U/L 217 mg/dL 9.8 mg/dL 5.1 mg/dL 146 mEq/L 4.5 mEq/L 109 mEq/L 1.3 14 2.7 201 U/L 551 U/L 65 mg/dL 153 U/L 7 U/L 1.6 mEq/L
Red blood cells Hemoglobin Hematocrit MCV MCH MCHC Platelet count White blood cells Neutrophils Lymphocytes Monocytes Eosinophils Basophils
4.8-9.3 106/mL 12.1-20.3 g/dL 36%-60% 58-79 fl 19-28 pg 30-38 170-400 103/mL 4.0-15.5 103/mL 2060-10,600 690-4500 0-840 0-1200 0-150
7.81 106/mL 17.1 g/dL 49.8% 64 fl 21.9 pg 34.3 g/dL 247 103/mL 9.5 103/mL 5130 3135 190 1045 0
ALT (SGPT), alanine transaminase; AST (SGOT), aspartate transaminase; BUN, blood urea nitrogen; CPK, creatine phosphokinase.
high-value object. Fear-related aggression was also diagnosed based on LF’s increased fearful posturing around KF, particularly when KF was excessively aroused (De Keuster and Jung, 2009; Mertens 2002; Overall 2013a; Sherman et al., 1996). In addition,
Table 3 Urinalysis for KF Test
Reference range
Result
ph Specific gravity Appearance Color Protein Glucose Ketone Bilirubin Blood WBC RBC Bacteria Epithelia Renal epithelial cells Transitional epithelia Triple phosphate crystals Amorphous phosphate Calcium phosphate c. Calcium carbonate c. Ammonium biurate c. Amorphous urate Calcium oxalate crystals Uric acid crystals Mucous Hyaline casts Granular casts RBC casts Waxy casts WBC casts Budging yeast Oval fat body
5.5-7.0 1015-1050 d d d d d d d 0-3 HPF 0-3 HPF None HPF None-few HPF None-rare HPF None-rare HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None-2þ STRANDS/HPF 0-3 LPF None LPF None LPF None None LPF None HPF None HPF
7.0 1036 Clear Yellow Negative Negative Negative Negative Negative 0-3 HPF 0-3 HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None STRANDS/HPF None seen LPF None seen LPF None seen LPF None seen None seen LPF None HPF None HPF
Key: RBC, red blood cells; WBC, white blood cells. HPF, high power field; LPF, low power field.
MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration.
KF behaved socially inappropriately at times (during “rough” interactions) with the other dogs, which may have contributed to LF’s fear (Landsberg et al., 2013a; Reisner, 2002). Although resource guarding may be included in a diagnosis of status-related aggression, LF was not diagnosed with status-related aggression because her conflicts with KF were limited to protection of resources (whereas status-related aggression would include other clinical signs, such as aggression secondary to arousal or excitement, postural provocations, or when maneuvering in small spaces), and because she had consistently shown defensive posturing (Landsberg et al., 2013a; Mertens, 2002; Resiner, 2002). Underlying anxiety in both dogs contributed to their inability to control the intensity of their interaction and aggression when aroused or fearful (Landsberg et al., 2013a; Reisner, 2002). Repeated exposure to aggressive interactions with KF contributed, via a learning process of sensitization, to the increased emotional arousal and aggression observed in LF over time. The owners used punishment when KF was showing aggressive and/or excessively aroused behaviors, further increasing the anxiety experienced by
Table 5 Serum chemistry panel of patient LF Test
Reference range
Result
Glucose Urea nitrogen Creatinine Total protein Albumin Total bilirubin Alkaline phosphatase ALT (SGPT) AST (SGOT) Cholesterol Calcium Phosphorus Sodium Potassium Chloride Albumin/globuline ratio BUN/creatinine ratio Globuline Lipase Amylase Triglycerides CPK GGTP Magnesium
70-138 mg/dL 6-25 mg/dL 0.5-1.6 mg/dL 5.0-7.4 g/dL 2.7-4.4 g/dL 0.1-0.3 mg/dL 5-131 U/L 12-118 U/L 15-66 U/L 92-324 mg/dL 8.9-11.4 mg/dL 2.5-6.0 mg/dL 139-154 mEq/L 3.6-5.5 mEq/L 102-120 mEq/L 0.8-2.0 4-27 1.6-3.6 77-695 U/L 290-1125 29-291 mg/dL 59-895 1-12 U/L 1.5-2.5 mEq/L
105 mg/dL 12 mg/dL 1.2 mg/dL 6.2 g/dL 3.5 g/dL 0.1 mg/dL 28 U/L 27 U/L 23 U/L 213 mg/dL 9.8 mg/dL 3.6 mg/dL 146 mEq/L 4.4 mEq/L 113 mEq/L 1.3 10 2.7 557 U/L 324 U/L 77 mg/dL 89 U/L 15 U/La 1.8 mEq/L
ALT (SGPT), alanine transaminase; AST (SGOT), aspartate transaminase; BUN, blood urea nitrogen; CPK, creatine phosphokinase. a High value.
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Table 6 Urinalysis of patient LF Test
Reference range
Result
ph Specific gravity Appearance Color Protein Glucose Ketone Bilirubin Blood WBC RBC Bacteria Epithelia Renal epithelial cells Transitional epithelia Triple phosphate crystals Amorphous phosphate Calcium phosphate c. Calcium carbonate c. Ammonium biurate c. Amorphous urate Calcium oxalate crystals Uric acid crystals Mucous Hyaline casts Granular casts RBC casts Waxy casts WBC casts Budging yeast Oval fat body
5.5-7.0 1015-1050 d d d d d d d 0-3 HPF 0-3 HPF None HPF None-few HPF None-rare HPF None-rare HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None-2þ STRANDS/HPF 0-3 LPF None LPF None LPF None None LPF None HPF None HPF
7.0 1025 Clear Yellow Negative Negative Negative Negative Negative 0-3 HPF 0-3 HPF None HPF None HPF None HPF None HPF Moderate HPFa None HPF None HPF None HPF None HPF None HPF None HPF None HPF None STRANDS/HPF None seen LPF None seen LPF None seen LPF None seen None seen LPF None HPF None HPF
Key: RBC, red blood cells; WBC, white blood cells. HPF, high power field; LPF, low power field. a High value.
KF and the dogs around her and sensitizing them to each other (Mills 2002). Both dogs showed other anxiety-related behaviors such as inappropriate attention seeking (jumping; Reisner, 2002). However, KF appeared to be more easily aroused than LF, as shown by KF’s inappropriate social skills during play and increased likelihood to attack LF when excited. The unremarkable medical histories, physical exams, and laboratory tests made it unlikely that aggression was associated with medical problems in either dog (De Keuster and Jung, 2009; Landsberg et al., 2013a; Mertens 2002; Overall 2013a). Treatment First, the owners were given safety recommendations, which included avoiding situations that had historically triggered aggression: the dogs were not to rest together on furniture or have high-value objects when together, and would be separated by means of a physical barrier when fed. For safety, the owners were counseled never to use their arms or legs to separate the dogs during a fight, and instead to use loud noises, citronella spray (SprayShield, Premier Pet Products LLC, Midlothian, VA), water, blankets, indoor leads on each dog, or a barrier such as a baby gate if the dogs were fighting (De Keuster and Jung, 2009; Landsberg et al., 2013a; Mertens 2002; Overall, 2013a). The owners were asked to discontinue all positive punishment, including leash corrections, which can increase aggression and reactivity (Herron et al., 2009). Because fights were still possible in spite of the owners’ vigilance, the dogs were to be kept on separate 1.8-2.4 m (6-8 ft) leads, each held by one of the owners without applying active tension on it. For at least 6-8 weeks, they would be separated when unsupervised. A separate “safe haven” was to be established for each dog, to which
they could go spontaneously, or where they could be restricted when necessary. Based on the preference of each dog and on the possible safe interactions among the 4 dogs, it was decided that the crate in the dining room represented a suitable safe haven for KF and the bedroom had to be used for LF. When KF was in fact confined in her crate, the other dogs tended to stay away from it, whereas LF could be safely confined in the bedroom with or without CF and JF. A positive association with the safe haven had to be created via classical conditioning by providing the dog with comfortable bedding and water. Toys and food had to be provided only when the dogs were confined in their respective safe haven, to prevent resource guarding. The safe haven had to be kept at a lowarousal level and free from potential threats to the dogs. White background noise was also considered as an option to decrease arousal (Alworth and Buerkle, 2013; De Keuster and Jung, 2009; Mertens 2002; Overall, 2013a). Second, the owners were taught how to use behavior modification to change the dogs’ behavior. They were advised to use only positive reinforcement or negative punishment (i.e., withdrawal of social attention) when training (Reisner, 2002). The cues “look” (to make eye contact with the owner as needed for redirection of behavior) and “leave it” (to disregard items in front of them) were demonstrated. Other cues included “come,” “go to” a specific place, get “off” furniture when told, and to “drop” items on cue. Such training was intended to enable the owners to redirect and move the dogs without physical contact, and to teach them to increase their distance from furniture and toys, the 2 main contexts in which aggression had occurred (Landsberg et al. 2013a, 2013b; Mills, 2002; Overall, 2013b). Relaxation exercises were also recommended to reinforce calm behavior (Landsberg et al. 2013a; Overall, b). The use of negative punishment was to be limited to attention-seeking behaviors (i.e., KF and LF jumping on the owner to seek contact or interaction). Response substitution through verbal cues (e.g., “touch” the owner’s hand to prevent jumping) and positive reinforcement had to be always preferred. The owners were informed about the potential for negative punishment to generate frustration, increase emotional arousal and, therefore, trigger aggression. They were instructed to discontinue the use of negative punishment if this would have caused frustration and increased arousal. Although behavior training with positive reinforcement had never triggered aggression between KF and LF, the owners were instructed to practice training exercises with each dog separately and to administer only small treats that could be easily swallowed. This safety strategy was implemented to minimize the risk that excessive arousal and resource guarding may trigger aggression during training sessions or use of conditioned responses rewarded with treats. After the initial 6 weeks of avoiding contact and direct interaction between KF and LF, during which there would be opportunity for the behavior modification (and treatment with medication) to be applied, rapprochement of the dogs could be attempted with desensitization and counter-conditioning. The owners were instructed to gradually decrease the distance between the dogs at each step of the protocol, rewarding calm behavior, and to keep the attention of each dog focused on the handler using verbal cues (i.e., “look” and “touch”) and positive reinforcement. The goal was to eventually allow them off-leash in the same area (Overall, 2013a, b). The other household dogs were determined to play no significant role in KF’s and LF’s interactions and therefore were not included in behavior modification. However, the owners were asked to be alert to any excitement or other arousal to which they might be contributing. For a summary of the behavior and environmental modification recommended, see Table 7. Third, serotonergic medication to decrease anxiety, arousal, and impulsivity was prescribed for both dogs. Clomipramine
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Table 7 Behavior and environmental modification recommended for KF and LF First 6-8 weeks: avoidance of contact and interaction After week 6-8: rapprochement
Long-term modification
Confine dogs in respective safe haven when unsupervised Keep dogs on separate 1.8-2.4 m (6-8 ft) leads, each held by one of the owners Keep the attention of each dog focused on the handler using verbal cues (i.e., “look” and “touch”) Gradually decrease the distance between the dogs Reward dogs for calm behavior when together Avoid situations that may triggered aggression Do not allow dogs to rest together on furniture or have high-value objects when together Separated the dogs using a physical barrier when fed Use “look” cue to redirect the dogs’ attention when necessary Use “come,” “go to,” and “off” cues to redirect and move the dogs without physical contact, and to increase their distance from furniture Use “leave it” and “drop it” to increase their distance from high-value items Use “relaxation exercises” to promote calm behavior Use “touch” cue to prevent jumping on owners
hydrochloride (Clomicalm, Novartis Animal Health US, East Hanover, NJ), a tricyclic antidepressant, was prescribed for KF at 20 mg (1.38 mg/kg) by mouth every 12 hours for 7 days (a relatively low dose to minimize side effects), then 40 mg (2.76 mg/kg) by mouth every 12 hours thereafter (Crowell-Davis and Murray, 2006b; Crowell-Davis and Landsberg, 2009; Overall, 1994). Clomipramine was selected for KF, an easily aroused and reactive dog, because it is less likely than fluoxetine to cause increased agitation and activation, and may produce mild, desired sedation (Crowell-Davis and Murray, 2006a; Mills and Simpson, 2002; Overall, 1994). Fluoxetine, with its lower unintended-effect profile, might also have been used to treat KF (Jenike et al., 1990). Fluoxetine hydrochloride (Reconcile, Elanco Animal Health, Greenfield, NJ), a selective serotonin reuptake inhibitor, was prescribed for LF at 8 mg (0.5 mg/kg) by mouth once daily for 7 days, then 16 mg (1 mg/kg) by mouth once daily (Crowell-Davis and Murray, 2006a; Crowell-Davis and Landsberg 2009). Off-label use of both drugs was discussed with the owners, as well as potential undesirable effects including increased aggression (Crowell-Davis and Murray, 2006a, 2006b).
pen had to be used to build a positive association with it via classical conditioning (Landsberg et al., 2013a; Overall, 2013b). At 4 months, the owners reported significant improvement. No fights or major incidents between KF and LF had occurred. LF spent more time in her “safe haven,” by choice, and successfully avoided interacting with KF. There were occasional episodes during which KF “froze” and stared at LF when a high-value item was accidentally accessible. However, KF seemed less reactive and the owners were able to redirect her attention with the “look” cue. The 2 dogs were now usually unrestrained when the owners were home. KF was confined in her crate or exercise pen when the owners were absent and during the owners’ or dogs’ meals. At 6 months, there had been no significant incidents. LF was less fearful around KF, and both dogs were able to occasionally rest on the owners’ bed or couch without showing aggression. When together, KF and LF usually maintained a relaxed body posture, and the owners were able to redirect their attention if alerted by or staring at each other. The owners were reminded of ongoing risks when the dogs shared such resources. In general, LF preferred avoiding interaction with KF and spending time in her safe area. KF was still confined in her crate during meals and when the owners were absent.
Follow-up Weekly follow-up confirmed that the owners were following recommendations. At 8 weeks, the owners reported general improvement. KF was less likely to get excessively aroused (e.g., before going out for a walk) and more appropriate when interacting with CF and JF (i.e., less jumping and mounting, and more likely to stop the interaction when the other dogs disengaged), and no aggressive incidents had occurred. During rapprochement, KF and LF were permitted to sniff each other, on a loose 2.4 m (8 ft) leash, with no signs of aggression. Although KF was generally less anxious and vocal, LF still appeared fearful and occasionally lunged at KF when KF was excited. However, when things were calm, the owners were successful keeping only KF on a leash. Although it had been recommended that both dogs be leashed when together, it was agreed that the owner continue in this way, because LF selfmaintained a safe distance from KF. The owners reported no problems or side effects associated with medication. In response to the owners’ report of ongoing fearful behavior, LF’s fluoxetine dose was increased to 24 mg (1.47 mg/kg) once daily (Crowell-Davis and Murray, 2006a; Crowell-Davis and Landsberg 2009), and the owners were reminded to avoid all potentially fear-inducing situations. They were asked to put LF in the bedroom (her safe haven) whenever KF’s excitement was anticipated, and to use responsesubstitution cues such as “sit” with KF at these times (Landsberg et al., 2013b; Overall, 2013b). An exercise pen was suggested as an alternative to a leash for KF. Relaxation exercises practiced in the
Discussion Two female dogs were presented to our behavior clinic for aggression directed toward each other. Possession of high-value resources (here, food and some toys), excitement, and being approached while resting were identified as triggers for aggression. Physical and laboratory evaluation were unremarkable. The younger dog, KF, was diagnosed with status-related aggression, whereas LF was diagnosed with resource-guarding and fear-related aggression. A multimodal treatment was implemented. The 2 canine patients were considered as components of a single clinical case (the “case” in this article) in which the complex system including the dogs, the owners, and the home environment was approached to treat the aggression between KF and LF. Safety measures were given to minimize the risk of severe aggressive interactions between the 2 dogs, and to prevent physical injuries to the owners attempting to separate the dogs during a fight. Environmental management was used to provide the dogs with safe havens and designated resting areas to increase their individual distance, decrease their threat perception, and increase their control over the environment. Behavior modification, based on both classical and operant conditioning, was recommended to enhance safety and increase the predictability of dog-human and dog-dog interactions. Increased environmental control and predictable interactions are known to reduce stress, fear, anxiety, and
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aggressiveness (Notari, 2009). Pharmacologic treatment with serotonergic medication, clomipramine and fluoxetine, was also implemented. The treatment achieved a notable reduction of the interdog aggression and, 6 months after the initial appointment, the dogs could be together in the same room without restraint or confinement, in absence of high-value items and with the owners present. Several of the characteristics observed in the case reported have been previously reported in cases of interdog aggression. Aggression between household dogs is more frequent among same-sex pairs than among household dogs of opposite sex (Bamberger and Houpt, 2006; Overall, 2013a; Sherman et al., 1996; Wrubel et al., 2011). The aggressor (also defined initiator or instigator, i.e., the first dog that will initiate an aggressive interaction by sending a threatening signal, e.g., staring, growling, snarling, biting .) tends to be younger than the victim and to have arrived in the home more recently in more than 50% of reported cases (Sherman et al., 1996; Wrubel et al., 2011). In the case presented, KF initiated most of the aggressive interactions, particularly when highly aroused, but LF had initially growled at KF when in possession of a high-value item. The triggers for aggression observed in the clinical case presented (i.e., possession of high-value items, excitement, and approaching the dog over a resting spot) are among the most frequently reported triggers for aggression between household dogs (Sherman et al., 1996; Wrubel et al., 2011). A noticeable improvement has been reported for more than half of the cases treated in 2 published studies (Sherman et al., 1996; Wrubel et al., 2011). Sherman et al. (1996) report that 56% of the cases treated for aggression to household dogs could be left together; though, 20% required supervision. In the same study, only 14% of the cases treated were considered completely resolved. The pathogenesis of aggression between household dogs has been historically linked to social conflicts motivated by the need to obtain or defend a higher hierarchical status (Sherman et al., 1996). However, the existence of a clear social hierarchy in groups of domestic dogs is controversial (Boitani et al., 1995; Bonanno and Cafazzo, 2014; Landsberg et al., 2013a; Schilder et al., 2014), and the social structure of canine groups seems to be plastic and adaptable to the local environment (Miklósi, 2015; Overall, 2013a). The social dominance of an individual arises primarily from the deference of other members of the group during an interaction, rather than from the assertive act of the specific dominant individual. Without this, there would be no predictability to social stability and a serious risk of injury to members of the social group (De Keuster and Jung, 2009; Van Der Borg et al., 2015). The role of factors other than dominance, that is, inappropriate social and communication skills, temperamental reactivity and excitability, poor environmental control because of human interference, space distribution and availability, and confinement should be considered in cases of aggression between household dogs (De Keuster and Jung, 2009, Landsberg et al., 2013a). Bradshaw et al. (2009) defines dominance as a property of dyadic relationships (i.e., limited to the interactions between 2 dogs, and not applicable to the complex social structure of a group), and suggests that associative learning and subjective resource value are useful factors to consider when analyzing agonistic behaviors between dogs. These results are confirmed by Cafazzo et al. (2010). Associative learning and resource value can contribute to explain LF’s aggression, which started as resource guarding (subjective resource value) and then generalized following sensitization (associative learning) to KF’s aroused behavior. However, factors like temperamental reactivity, high arousability, and lack of social skills should be also considered to explain KF’s aggressive behavior. Owing to the complex nature of aggression between household dogs, a diagnosis of “intra-specific affective aggression” may be more appropriate, as proposed by De
Keuster and Jung (2009), because this diagnosis is based on the underlying neurophysiology of the aggressive response observed rather than its multiple causes or motivations (Carlson, 2013). The existence of a complex environmental system formed by 6 adult individuals (4 dogs and 2 humans) living in a relatively small city space, with the consequent lack of safe individual spaces, presence of multiple simultaneous social interactions and increased stress contributed to the development of the aggression between KF and LF. The institution of a “safe haven” (the crate and the owners’ bedroom) was in fact recommended to provide the dogs with a protected space in which interactions and arousal are minimized, therefore increasing control over the environment, and decreasing stress and aggression (De Keuster and Jung, 2009; Overall, 2013a). A human analogue safe haven effect had been proved for the presence of the owner during a threatening interaction with a stranger. Owners can provide a buffer against stress in dogs, which can even reduce the effect of a subsequent encounter with the same threatening stimuli later when the owner is not present (Gácsi et al., 2013). However, proximity to and attention from the owner may trigger aggression between dogs in the same household (Wrubel et al., 2011), and the human safe haven effect should be used with caution in such cases. Treatment protocols for aggression between household dogs frequently include behavior modification to support the hierarchical status of the dog whose dominance has been challenged (Sherman et al., 1996; Wrubel et al., 2011). Although the multifactorial nature of this behavior problem previously described raises questions and concerns about such treatment, its effectiveness and appropriateness may in fact ultimately decrease the welfare of the dog chosen as submissive, and pose potential hazards for the people and dogs involved (De Keuster and Jung, 2009; Landsberg et al., 2013a). In the case here reported, we preferred the implementation of a treatment aimed to increase the predictability and control of the environment, increase safety, decrease stress and anxiety, and improve the welfare of our patients, which proved to be a successful strategy. Acknowledgments The idea for the study was conceived and the article was written by Carlo Siracusa. Conflict of interest The author declares no conflict of interest. Ethical considerations The work presented did not need approval because it involved only routine clinical treatment. References Alworth, L.C., Buerkle, S.C., 2013. The effects of music on animal physiology, behavior and welfare. Lab. Anim. 42, 54e61. Bamberger, M., Houpt, K., 2006. Signalment factors, comorbidity, and trends in behavior diagnoses in dogs: 1644 cases (1991-2001). J. Am. Vet. Med. Assoc. 229, 1591e1601. Boitani, L., Francisci, F., Ciucci, P., et al., 1995. Population biology and ecology of feral dogs in central Italy. In: Serpell, J. (Ed.), The Domestic Dog, its Evolution, Behavior and Interactions with People. Cambridge University Press, Cambridge, pp. 217e244. Bonanno, R., Cafazzo, S., 2014. The social organization of a population of freeranging dogs in a suburban area of Rome: A reassessment of the effects of domestication on dogs’ behavior. In: Kaminski, J., Marshall-Pescini, S.M. (Eds.), The Social Dog: Behavior and Cognition. Academic Press, San Diego, pp. 65e104. Bradshaw, J.W.S., Blackwell, E.J., Casey, R.A., 2009. Dominance in domestic dogs useful construct or bad habit? J. Vet. Behav.: Clin. Appl. Res. 4, 135e144.
C. Siracusa / Journal of Veterinary Behavior xxx (2015) 1e7 Cafazzo, S., Valsecchi, P., Bonanni, R., Natoli, E., 2010. Dominance in relation to age, sex, and competitive contexts in a group of free-ranging domestic dogs. Behav. Ecol. 21, 443e455. Carlson, N.R., 2013. Neurophysiology of Behavior, 11th Ed. Person Education, Upper Aaddle River, NJ, pp. 360e392. Crowell-Davis, S.L., Murray, T., 2006a. Selective serotonin reuptake inhibitors. In: Crowell-Davis, S.L., Murray, T. (Eds.), Veterinary Psychopharmacology. Blackwell Publishing, Ames, pp. 80e110. Crowell-Davis, S.L., Murray, T., 2006b. Tricyclic antidepressants. In: CrowellDavis, S.L., Murray, T. (Eds.), Veterinary Psychopharmacology. Blackwell Publishing, Ames, pp. 179e206. Crowell-Davis, S.L., Landsberg, G.M., 2009. In: Horwitz, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine, 2nd Ed. BSAVA, Gloucester, pp. 245e258. De Keuster, T., Jung, H., 2009. Aggression toward familiar people and animals. In: Horwitz, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine, 2nd Ed. BSAVA, Gloucester, pp. 182e210. Gácsi, M., Maros, K., Sernkvist, S., Farago, T., Miklósi, A., 2013. Human analogue safe haven effect of the owner: Behavioural and heart rate response to stressful social stimuli in dogs. PLoS ONE 8, e58475. Herron, M.E., Shofer, F.S., Reisner, I.R., 2009. Survey of the use and outcome of confrontational and non-confrontational training methods in client-owned dogs showing undesired behavior. Appl. Anim. Behav. Sci. 117, 47e54. Jenike, M.A., Baer, L., Greist, J.H., 1990. Clomipramine versus fluoxetine in obsessive compulsive disorder: A retrospective comparison of side effects and efficacy. J. Clin. Psychopharmacol. 10, 122e124. Landsberg, G., Hunthausen, W., Ackerman, L.F., 2013a. Canine aggression. In: Landsberg, G., Hunthausen, W., Ackerman, L.F. (Eds.), Behavior Problems of the Dog and Cat, 3rd Ed. Saunders Elsevier, London, pp. 297e326. Landsberg, G., Hunthausen, W., Ackerman, L.F., 2013b. Treatmentdbehavior modification techniques. In: Landsberg, G., Hunthausen, W., Ackerman, L.F. (Eds.), Behavior Problems of the Dog and Cat, 3rd Ed. Saunders Elsevier, London, pp. 95e112. Mertens, P.A., 2002. Canine aggression. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 195e215. Miklósi, A., 2015. Intra-specific social organization in dogs and related forms. In: Miklósi, A. (Ed.), Dog Behavior, Evolution and Cognition, 2nd Ed. Oxford University Press, Oxford, pp. 172e182.
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Mills, D.S., 2002. Learning, training and behaviour modification techniques. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 37e48. Mills, D.S., Simpson, B.S., 2002. Psychotropic agents. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 237e248. Notari, L., 2009. Stress in veterinary behavioural medicine. In: Horwitz, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine, 2nd Ed. BSAVA, Gloucester, pp. 136e145. Overall, K.L., 1994. Use of clomipramine to treat ritualistic motor behavior in dogs. J. Am. Vet. Med. Assoc 205, 1733e1741. Overall, K.L., 2013a. Abnormal canine behavior and behavioural pathologies involving aggression. In: Overall, K.L. (Ed.), Manual of Clinical Behavior Medicine for Dogs and Cats. Elsevier Mosby, St. Louis, pp. 172e230. Overall, K.L., 2013b. Supplemental materials: client handouts. In: Overall, K.L. (Ed.), Manual of Clinical Behavior Medicine for Dogs and Cats. Elsevier Mosby, St. Louis, pp. 574e796. Reisner, I., 2002. An overview of aggression. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 181e194. Schilder, M.B.H., Vinke, C.M., Van Der Borg, J.A.M., 2014. Dominance in domestic dogs revisited: Useful habit and useful construct? J. Vet. Behav.: Clin. Appl. Res. 9, 184e191. Sherman, C.K., Reisner, I.R., Taliaferro, L.A., et al., 1996. Characteristics, treatment, and outcome of 99 cases of aggression between dogs. Appl. Anim. Behav. Sci. 47, 91e108. Stockham, S.L., Scott, M.A., 2008a. Enzymes. In: Stockham, S.L., Scott, M.A. (Eds.), Fundamentals of Veterinary Clinical Pathology, 2nd Ed. Blackwell Publishing, Ames, pp. 640e674. Stockham, S.L., Scott, M.A., 2008b. Urinary system. In: Stockham, S.L., Scott, M.A. (Eds.), Fundamentals of Veterinary Clinical Pathology, 2nd Ed. Blackwell Publishing, Ames, pp. 415e494. Van der Borg, J.A., Schilder, M.B., Vinke, C.M., de Vries, H., 2015. Dominance in domestic dogs: A quantitative analysis of its behavioural measures. PLoS ONE 10, e0133978. Wrubel, K.M., Moon-Fanelli, A.A., Maranda, L.S., et al., 2011. Interdog household aggression: 38 cases (2006-2007). J. Am. Vet. Med. Assoc. 238, 731e 740.
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Case Report
Status-related aggression, resource guarding, and fear-related aggression in 2 female mixed breed dogs Carlo Siracusa* Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 July 2015 Received in revised form 10 November 2015 Accepted 2 December 2015 Available online xxx
Two household dogs, a 2 year, 8-month-old, spayed female, mixed-breed dog, and a 4 year, 1-month-old, spayed female, mixed-breed dog, presented with a history of aggression toward each other, when in possession of food or other high-value items, and when one approached the other while resting. They responded satisfactorily to treatment with serotonergic drugs, avoidance of provocative situations, and environmental and behavioral modification. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: affective aggression dog intra-specific aggression resource guarding
Presentation KF was a 2.7-year-old, spayed female, 14.5-kg, mixed-breed dog, and LF was a 4-year-old, spayed female, 16.3-kg, mixed-breed dog. KF and LF were presented by their owners for aggression between them when in possession of food or other high-value items, and when LF approached KF while resting. History and presenting signs KF was adopted from the local Society For The Prevention Of Cruelty To Animals at 1.5 years of age, and LF was adopted from a local rescue organization at 1 year of age. They lived with their owners, Ms. F. and Mr. Y., and 2 other dogs in a city apartment with 4 rooms (bedroom, living room, dining room, and kitchen). The other 2 dogs living in the apartment were CF, a 7-year, neutered male, mixed-breed dog obtained at the age of 2 years and JF, a 3-year, spayed female, mixed-breed dog obtained at 6 months. CF and JF did not show aggressive interactions between them or toward KF and LF. Historically, all dogs had free access to all the rooms * Address for reprint requests and correspondence: Carlo Siracusa, Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, 3900 Delancey Street, Philadelphia, PA 19104, Tel: 001 (215)-898-6681; Fax: 001 (215)573-7041. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.jveb.2015.12.001 1558-7878/Ó 2015 Elsevier Inc. All rights reserved.
in the apartment. After KF was acquired, there had not been changes in the household. The dogs were walked on a leash outside 3 times per day. The average length of these walks was about 20 minutes. The owners reported that, although LF had historically growled at the other household dogs around food or other items perceived as highly valuable by her (rawhide, real bones, toys, stolen objects .). KF and the other dogs typically responded by lowering their bodies and moving away and such behavior had not led to fights before the incidents described. The owners also described how KF was often “rough” when playing with the other dogs, jumping on and sometimes mounting them, and attempting to continue the interaction when the other dogs disengaged. This aroused interaction did not escalate into aggression and did not require the intervention of the owners to be interrupted. Starting approximately 4 months before the behavior appointment, KF had been staring, growling at and attempting to bite LF when near food or toys, or when LF approached her while she was resting. The first incident of aggression between KF and LF that led to a bite occurred 1.5 months before presentation. According to the description provided by the owners, KF and LF were under the dining room table, whereas CF and JF were under the chairs occupied by the owners, when a piece of food dropped. KF displayed piloerection and, with ears forward, stared and lunged at LF, biting her face and neck without breaking the skin. Mr. Y. promptly interrupted the aggressive interaction by yelling “no.” He detected
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no serious injuries during a visual inspection of the dogs. CF and JF were alert during the aggressive interaction between KF and LF but remained under their respective chairs. Since this incident, the aggressive behavior had escalated in both frequency and intensity. A second incident occurred 5 weeks before the behavior consultation. LF, CF, and JF were resting on the bed together with the owners. When KF jumped on the bed, LF was startled and stared at her. KF stared back and, a few second later, KF lunged at LF and engaged in a fight. CF and JF jumped off the bed and left the bedroom. KF and LF bit each other several times. The owners separated the 2 dogs by grabbing and pulling on their bodies. During this interaction, KF bit Mr. Y. in his hand without breaking the skin. LF suffered bite punctures on her face, leg, and eyelid. KF had punctures on her leg and face. After separation, KF was confined to her crate in the dining room. A veterinarian was seen to treat the injuries. One final incident occurred a month before the consultation, at dinnertime, in circumstances very similar to the first incident described. Also in this case, KF and LF were under the table, while CF and JF were around the table. The owners were not able to confirm if some food had dropped but described that KF stared at LF and stiffened, and then the 2 dogs lunged at each other, snarling and biting. Mr. Y. grabbed KF by her body and pulled her away, while Ms. F. picked LF up. This intervention of the owners did not interrupt the aggressive behavior of KF, who kept trying to reach LF and bit Mr. Y.’s hand, breaking the skin and causing punctures that did not require hospitalization. Both dogs suffered multiple punctures from bites on their face and body that required veterinary treatment. KF was confined to her crate after this incident. After such incidents, LF showed progressively more fear and wariness around KF. The latter was likely to initiate an aggressive interaction with LF when she was excited, barking, and running around, if off leash, or jumping, if on leash (e.g., before going for a walk). This aggressive display could trigger an aggressive response from LF, if the 2 dogs were in proximity and unrestrained. In an effort to correct KF’s aggression and excitability, the owners had tried verbal and physical corrections (staring at the dog, growling at the dog, rolling the dog on his back and holding down (“alpha rolls”), holding the dog on her side, yelling “no,” leash corrections), with no effect. Since the aggression between KF and LF had developed, KF was kept in a crate in the dining room and LF was kept in the bedroom behind a closed door when not supervised by the owners. KF and LF spent time in these areas also when not confined, and did not show signs of anxiety when confined. CF and JF tended to stay away from KF since her aggressive behavior had escalated. When the owners were at home, all the dogs tended to stay nearby; in particular, KF spent more time in proximity of Mr. Y than the other dogs. Both dogs frequently jumped to seek interaction and contact with the owners. However, according to the owners, the proximity of a dog to one or both owners, or receiving attention from the owners, was not a specific trigger of aggression between KF and LF. Aside from the incidental redirected aggression showed toward Ms. Y. when attempting to separate KF and LF during a fight, the 2 dogs did not show signs of aggression directed to the owners. Before the behavior appointment, KF and LF did not receive formal training classes. The owners had taught them basic verbal cues, such as “sit,” using operant conditioning with intermittent reinforcement. Both dogs responded reliably when not excessively aroused, and did not show aggression over treats used as reinforcement. KF’s and LF’s medical histories were unremarkable. Behavioral, physical, and laboratory evaluation KF and LF were kept on separate leashes during the appointment. Both Ms. F. and Mr. Y. were present, each one holding on one
of the dog’s leash. KF was active and playful, whereas LF was more vigilant, continually monitoring KF. At one point when 2 toys were offered, the dogs stared at each other and then KF barked and lunged at LF. The toys were removed. Physical examination, including a neurologic and orthopedic assessment, complete blood count, serum chemistry, and urinalyses for both dogs were unremarkable (Tables 1-6). No source of pain was found. LF’s laboratory tests showed a mild increase of serum gamma-glutamyl transpeptidase (GGTP) and presence of moderate triple phosphate crystals in the urine. Both findings were considered clinically insignificant because they were not associated with specific clinical signs and/or other hematological or biochemical alterations (Stockham and Scott, 2008a, 2008b). Diagnoses Aggressive interactions between household dogs may be the result of fear, social status conflict, resource guarding, inappropriate social skills, and orthopedic pain or other medical problems. Its progression may be also influenced by the outcome of past aggressive interactions, including the response of the owner (De Keuster and Jung, 2009; Landsberg et al., 2013a; Mertens 2002; Overall 2013a). In KF’s case, aggression was consistent with status-related aggression (i.e., aggression due to social status conflict)dwhich can include resource-guarding behaviordbecause the aggression was associated with control over resources and had progressed from submissive body postures to overtly aggressive over time. Several factors may have contributed to this progression, including KF becoming socially mature, repeated exposure to punishment, and sensitization to contexts in which LF was present (Landsberg et al., 2013a; Mertens 2002; Overall, 2013a). The lack of a clear social hierarchy in group of dogs, together with the potential influence of factors other than social status in the development of aggression between dogs of the same group, has made some authors questioning the appropriateness of “dominance aggression” or “status-related aggression” as diagnostic categories (Bradshaw et al., 2009; De Keuster and Jung, 2009; Miklósi, 2015). Fearrelated aggression was considered as a differential diagnosis for KF. However, it was determined that the primary problem for KF was status-related aggression because of the repeated contexts associated with both resources and excitement, and the absence of posturing consistent with fear (Landsberg et al., 2013a; Mertens 2002; Sherman et al., 1996). The aggression that LF historically showed toward KF was diagnosed as resource guarding, based on the aggressive behavior that she exhibited toward any dog that approached when she had a
Table 1 Complete blood cells count (CBC) of patient KF Test
Reference range
Result
Red blood cells Hemoglobin Hematocrit MCV MCH MCHC Platelet count White blood cells Neutrophils Lymphocytes Monocytes Eosinophils Basophils
4.8-9.3 106/mL 12.1-20.3 g/dL 36%-60% 58-79 fl 19-28 pg 30-38 170-400 103/mL 4.0-15.5 103/mL 2060-10,600 690-4500 0-840 0-1200 0-150
7.07 106/mL 16.1 g/dL 45.7% 65 fl 22.8 pg 35.2 g/dL 383 103/mL 7.8 103/mL 4212 2886 234 390 78
MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration.
C. Siracusa / Journal of Veterinary Behavior xxx (2015) 1e7 Table 2 Serum chemistry panel of patient KF
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Table 4 Complete blood cells count (CBC) of patient LF
Test
Reference range
Result
Test
Reference range
Result
Glucose Urea nitrogen Creatinine Total protein Albumin Total bilirubin Alkaline phosphatase ALT (SGPT) AST (SGOT) Cholesterol Calcium Phosphorus Sodium Potassium Chloride Albumin/globuline ratio BUN/creatinine ratio Globuline Lipase Amylase Triglycerides CPK GGTP Magnesium
70-138 mg/dL 6-25 mg/dL 0.5-1.6 mg/dL 5.0-7.4 g/dL 2.7-4.4 g/dL 0.1-0.3 mg/dL 5-131 U/L 12-118 U/L 15-66 U/L 92-324 mg/dL 8.9-11.4 mg/dL 2.5-6.0 mg/dL 139-154 mEq/L 3.6-5.5 mEq/L 102-120 mEq/L 0.8-2.0 4-27 1.6-3.6 77-695 U/L 290-1125 29-291 mg/dL 59-895 1-12 U/L 1.5-2.5 mEq/L
106 mg/dL 15 mg/dL 1.1 mg/dL 6.1 g/dL 3.4 g/dL 0.2 mg/dL 59 U/L 42 U/L 27 U/L 217 mg/dL 9.8 mg/dL 5.1 mg/dL 146 mEq/L 4.5 mEq/L 109 mEq/L 1.3 14 2.7 201 U/L 551 U/L 65 mg/dL 153 U/L 7 U/L 1.6 mEq/L
Red blood cells Hemoglobin Hematocrit MCV MCH MCHC Platelet count White blood cells Neutrophils Lymphocytes Monocytes Eosinophils Basophils
4.8-9.3 106/mL 12.1-20.3 g/dL 36%-60% 58-79 fl 19-28 pg 30-38 170-400 103/mL 4.0-15.5 103/mL 2060-10,600 690-4500 0-840 0-1200 0-150
7.81 106/mL 17.1 g/dL 49.8% 64 fl 21.9 pg 34.3 g/dL 247 103/mL 9.5 103/mL 5130 3135 190 1045 0
ALT (SGPT), alanine transaminase; AST (SGOT), aspartate transaminase; BUN, blood urea nitrogen; CPK, creatine phosphokinase.
high-value object. Fear-related aggression was also diagnosed based on LF’s increased fearful posturing around KF, particularly when KF was excessively aroused (De Keuster and Jung, 2009; Mertens 2002; Overall 2013a; Sherman et al., 1996). In addition,
Table 3 Urinalysis for KF Test
Reference range
Result
ph Specific gravity Appearance Color Protein Glucose Ketone Bilirubin Blood WBC RBC Bacteria Epithelia Renal epithelial cells Transitional epithelia Triple phosphate crystals Amorphous phosphate Calcium phosphate c. Calcium carbonate c. Ammonium biurate c. Amorphous urate Calcium oxalate crystals Uric acid crystals Mucous Hyaline casts Granular casts RBC casts Waxy casts WBC casts Budging yeast Oval fat body
5.5-7.0 1015-1050 d d d d d d d 0-3 HPF 0-3 HPF None HPF None-few HPF None-rare HPF None-rare HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None-2þ STRANDS/HPF 0-3 LPF None LPF None LPF None None LPF None HPF None HPF
7.0 1036 Clear Yellow Negative Negative Negative Negative Negative 0-3 HPF 0-3 HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None STRANDS/HPF None seen LPF None seen LPF None seen LPF None seen None seen LPF None HPF None HPF
Key: RBC, red blood cells; WBC, white blood cells. HPF, high power field; LPF, low power field.
MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration.
KF behaved socially inappropriately at times (during “rough” interactions) with the other dogs, which may have contributed to LF’s fear (Landsberg et al., 2013a; Reisner, 2002). Although resource guarding may be included in a diagnosis of status-related aggression, LF was not diagnosed with status-related aggression because her conflicts with KF were limited to protection of resources (whereas status-related aggression would include other clinical signs, such as aggression secondary to arousal or excitement, postural provocations, or when maneuvering in small spaces), and because she had consistently shown defensive posturing (Landsberg et al., 2013a; Mertens, 2002; Resiner, 2002). Underlying anxiety in both dogs contributed to their inability to control the intensity of their interaction and aggression when aroused or fearful (Landsberg et al., 2013a; Reisner, 2002). Repeated exposure to aggressive interactions with KF contributed, via a learning process of sensitization, to the increased emotional arousal and aggression observed in LF over time. The owners used punishment when KF was showing aggressive and/or excessively aroused behaviors, further increasing the anxiety experienced by
Table 5 Serum chemistry panel of patient LF Test
Reference range
Result
Glucose Urea nitrogen Creatinine Total protein Albumin Total bilirubin Alkaline phosphatase ALT (SGPT) AST (SGOT) Cholesterol Calcium Phosphorus Sodium Potassium Chloride Albumin/globuline ratio BUN/creatinine ratio Globuline Lipase Amylase Triglycerides CPK GGTP Magnesium
70-138 mg/dL 6-25 mg/dL 0.5-1.6 mg/dL 5.0-7.4 g/dL 2.7-4.4 g/dL 0.1-0.3 mg/dL 5-131 U/L 12-118 U/L 15-66 U/L 92-324 mg/dL 8.9-11.4 mg/dL 2.5-6.0 mg/dL 139-154 mEq/L 3.6-5.5 mEq/L 102-120 mEq/L 0.8-2.0 4-27 1.6-3.6 77-695 U/L 290-1125 29-291 mg/dL 59-895 1-12 U/L 1.5-2.5 mEq/L
105 mg/dL 12 mg/dL 1.2 mg/dL 6.2 g/dL 3.5 g/dL 0.1 mg/dL 28 U/L 27 U/L 23 U/L 213 mg/dL 9.8 mg/dL 3.6 mg/dL 146 mEq/L 4.4 mEq/L 113 mEq/L 1.3 10 2.7 557 U/L 324 U/L 77 mg/dL 89 U/L 15 U/La 1.8 mEq/L
ALT (SGPT), alanine transaminase; AST (SGOT), aspartate transaminase; BUN, blood urea nitrogen; CPK, creatine phosphokinase. a High value.
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C. Siracusa / Journal of Veterinary Behavior xxx (2015) 1e7
Table 6 Urinalysis of patient LF Test
Reference range
Result
ph Specific gravity Appearance Color Protein Glucose Ketone Bilirubin Blood WBC RBC Bacteria Epithelia Renal epithelial cells Transitional epithelia Triple phosphate crystals Amorphous phosphate Calcium phosphate c. Calcium carbonate c. Ammonium biurate c. Amorphous urate Calcium oxalate crystals Uric acid crystals Mucous Hyaline casts Granular casts RBC casts Waxy casts WBC casts Budging yeast Oval fat body
5.5-7.0 1015-1050 d d d d d d d 0-3 HPF 0-3 HPF None HPF None-few HPF None-rare HPF None-rare HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None HPF None-2þ STRANDS/HPF 0-3 LPF None LPF None LPF None None LPF None HPF None HPF
7.0 1025 Clear Yellow Negative Negative Negative Negative Negative 0-3 HPF 0-3 HPF None HPF None HPF None HPF None HPF Moderate HPFa None HPF None HPF None HPF None HPF None HPF None HPF None HPF None STRANDS/HPF None seen LPF None seen LPF None seen LPF None seen None seen LPF None HPF None HPF
Key: RBC, red blood cells; WBC, white blood cells. HPF, high power field; LPF, low power field. a High value.
KF and the dogs around her and sensitizing them to each other (Mills 2002). Both dogs showed other anxiety-related behaviors such as inappropriate attention seeking (jumping; Reisner, 2002). However, KF appeared to be more easily aroused than LF, as shown by KF’s inappropriate social skills during play and increased likelihood to attack LF when excited. The unremarkable medical histories, physical exams, and laboratory tests made it unlikely that aggression was associated with medical problems in either dog (De Keuster and Jung, 2009; Landsberg et al., 2013a; Mertens 2002; Overall 2013a). Treatment First, the owners were given safety recommendations, which included avoiding situations that had historically triggered aggression: the dogs were not to rest together on furniture or have high-value objects when together, and would be separated by means of a physical barrier when fed. For safety, the owners were counseled never to use their arms or legs to separate the dogs during a fight, and instead to use loud noises, citronella spray (SprayShield, Premier Pet Products LLC, Midlothian, VA), water, blankets, indoor leads on each dog, or a barrier such as a baby gate if the dogs were fighting (De Keuster and Jung, 2009; Landsberg et al., 2013a; Mertens 2002; Overall, 2013a). The owners were asked to discontinue all positive punishment, including leash corrections, which can increase aggression and reactivity (Herron et al., 2009). Because fights were still possible in spite of the owners’ vigilance, the dogs were to be kept on separate 1.8-2.4 m (6-8 ft) leads, each held by one of the owners without applying active tension on it. For at least 6-8 weeks, they would be separated when unsupervised. A separate “safe haven” was to be established for each dog, to which
they could go spontaneously, or where they could be restricted when necessary. Based on the preference of each dog and on the possible safe interactions among the 4 dogs, it was decided that the crate in the dining room represented a suitable safe haven for KF and the bedroom had to be used for LF. When KF was in fact confined in her crate, the other dogs tended to stay away from it, whereas LF could be safely confined in the bedroom with or without CF and JF. A positive association with the safe haven had to be created via classical conditioning by providing the dog with comfortable bedding and water. Toys and food had to be provided only when the dogs were confined in their respective safe haven, to prevent resource guarding. The safe haven had to be kept at a lowarousal level and free from potential threats to the dogs. White background noise was also considered as an option to decrease arousal (Alworth and Buerkle, 2013; De Keuster and Jung, 2009; Mertens 2002; Overall, 2013a). Second, the owners were taught how to use behavior modification to change the dogs’ behavior. They were advised to use only positive reinforcement or negative punishment (i.e., withdrawal of social attention) when training (Reisner, 2002). The cues “look” (to make eye contact with the owner as needed for redirection of behavior) and “leave it” (to disregard items in front of them) were demonstrated. Other cues included “come,” “go to” a specific place, get “off” furniture when told, and to “drop” items on cue. Such training was intended to enable the owners to redirect and move the dogs without physical contact, and to teach them to increase their distance from furniture and toys, the 2 main contexts in which aggression had occurred (Landsberg et al. 2013a, 2013b; Mills, 2002; Overall, 2013b). Relaxation exercises were also recommended to reinforce calm behavior (Landsberg et al. 2013a; Overall, b). The use of negative punishment was to be limited to attention-seeking behaviors (i.e., KF and LF jumping on the owner to seek contact or interaction). Response substitution through verbal cues (e.g., “touch” the owner’s hand to prevent jumping) and positive reinforcement had to be always preferred. The owners were informed about the potential for negative punishment to generate frustration, increase emotional arousal and, therefore, trigger aggression. They were instructed to discontinue the use of negative punishment if this would have caused frustration and increased arousal. Although behavior training with positive reinforcement had never triggered aggression between KF and LF, the owners were instructed to practice training exercises with each dog separately and to administer only small treats that could be easily swallowed. This safety strategy was implemented to minimize the risk that excessive arousal and resource guarding may trigger aggression during training sessions or use of conditioned responses rewarded with treats. After the initial 6 weeks of avoiding contact and direct interaction between KF and LF, during which there would be opportunity for the behavior modification (and treatment with medication) to be applied, rapprochement of the dogs could be attempted with desensitization and counter-conditioning. The owners were instructed to gradually decrease the distance between the dogs at each step of the protocol, rewarding calm behavior, and to keep the attention of each dog focused on the handler using verbal cues (i.e., “look” and “touch”) and positive reinforcement. The goal was to eventually allow them off-leash in the same area (Overall, 2013a, b). The other household dogs were determined to play no significant role in KF’s and LF’s interactions and therefore were not included in behavior modification. However, the owners were asked to be alert to any excitement or other arousal to which they might be contributing. For a summary of the behavior and environmental modification recommended, see Table 7. Third, serotonergic medication to decrease anxiety, arousal, and impulsivity was prescribed for both dogs. Clomipramine
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Table 7 Behavior and environmental modification recommended for KF and LF First 6-8 weeks: avoidance of contact and interaction After week 6-8: rapprochement
Long-term modification
Confine dogs in respective safe haven when unsupervised Keep dogs on separate 1.8-2.4 m (6-8 ft) leads, each held by one of the owners Keep the attention of each dog focused on the handler using verbal cues (i.e., “look” and “touch”) Gradually decrease the distance between the dogs Reward dogs for calm behavior when together Avoid situations that may triggered aggression Do not allow dogs to rest together on furniture or have high-value objects when together Separated the dogs using a physical barrier when fed Use “look” cue to redirect the dogs’ attention when necessary Use “come,” “go to,” and “off” cues to redirect and move the dogs without physical contact, and to increase their distance from furniture Use “leave it” and “drop it” to increase their distance from high-value items Use “relaxation exercises” to promote calm behavior Use “touch” cue to prevent jumping on owners
hydrochloride (Clomicalm, Novartis Animal Health US, East Hanover, NJ), a tricyclic antidepressant, was prescribed for KF at 20 mg (1.38 mg/kg) by mouth every 12 hours for 7 days (a relatively low dose to minimize side effects), then 40 mg (2.76 mg/kg) by mouth every 12 hours thereafter (Crowell-Davis and Murray, 2006b; Crowell-Davis and Landsberg, 2009; Overall, 1994). Clomipramine was selected for KF, an easily aroused and reactive dog, because it is less likely than fluoxetine to cause increased agitation and activation, and may produce mild, desired sedation (Crowell-Davis and Murray, 2006a; Mills and Simpson, 2002; Overall, 1994). Fluoxetine, with its lower unintended-effect profile, might also have been used to treat KF (Jenike et al., 1990). Fluoxetine hydrochloride (Reconcile, Elanco Animal Health, Greenfield, NJ), a selective serotonin reuptake inhibitor, was prescribed for LF at 8 mg (0.5 mg/kg) by mouth once daily for 7 days, then 16 mg (1 mg/kg) by mouth once daily (Crowell-Davis and Murray, 2006a; Crowell-Davis and Landsberg 2009). Off-label use of both drugs was discussed with the owners, as well as potential undesirable effects including increased aggression (Crowell-Davis and Murray, 2006a, 2006b).
pen had to be used to build a positive association with it via classical conditioning (Landsberg et al., 2013a; Overall, 2013b). At 4 months, the owners reported significant improvement. No fights or major incidents between KF and LF had occurred. LF spent more time in her “safe haven,” by choice, and successfully avoided interacting with KF. There were occasional episodes during which KF “froze” and stared at LF when a high-value item was accidentally accessible. However, KF seemed less reactive and the owners were able to redirect her attention with the “look” cue. The 2 dogs were now usually unrestrained when the owners were home. KF was confined in her crate or exercise pen when the owners were absent and during the owners’ or dogs’ meals. At 6 months, there had been no significant incidents. LF was less fearful around KF, and both dogs were able to occasionally rest on the owners’ bed or couch without showing aggression. When together, KF and LF usually maintained a relaxed body posture, and the owners were able to redirect their attention if alerted by or staring at each other. The owners were reminded of ongoing risks when the dogs shared such resources. In general, LF preferred avoiding interaction with KF and spending time in her safe area. KF was still confined in her crate during meals and when the owners were absent.
Follow-up Weekly follow-up confirmed that the owners were following recommendations. At 8 weeks, the owners reported general improvement. KF was less likely to get excessively aroused (e.g., before going out for a walk) and more appropriate when interacting with CF and JF (i.e., less jumping and mounting, and more likely to stop the interaction when the other dogs disengaged), and no aggressive incidents had occurred. During rapprochement, KF and LF were permitted to sniff each other, on a loose 2.4 m (8 ft) leash, with no signs of aggression. Although KF was generally less anxious and vocal, LF still appeared fearful and occasionally lunged at KF when KF was excited. However, when things were calm, the owners were successful keeping only KF on a leash. Although it had been recommended that both dogs be leashed when together, it was agreed that the owner continue in this way, because LF selfmaintained a safe distance from KF. The owners reported no problems or side effects associated with medication. In response to the owners’ report of ongoing fearful behavior, LF’s fluoxetine dose was increased to 24 mg (1.47 mg/kg) once daily (Crowell-Davis and Murray, 2006a; Crowell-Davis and Landsberg 2009), and the owners were reminded to avoid all potentially fear-inducing situations. They were asked to put LF in the bedroom (her safe haven) whenever KF’s excitement was anticipated, and to use responsesubstitution cues such as “sit” with KF at these times (Landsberg et al., 2013b; Overall, 2013b). An exercise pen was suggested as an alternative to a leash for KF. Relaxation exercises practiced in the
Discussion Two female dogs were presented to our behavior clinic for aggression directed toward each other. Possession of high-value resources (here, food and some toys), excitement, and being approached while resting were identified as triggers for aggression. Physical and laboratory evaluation were unremarkable. The younger dog, KF, was diagnosed with status-related aggression, whereas LF was diagnosed with resource-guarding and fear-related aggression. A multimodal treatment was implemented. The 2 canine patients were considered as components of a single clinical case (the “case” in this article) in which the complex system including the dogs, the owners, and the home environment was approached to treat the aggression between KF and LF. Safety measures were given to minimize the risk of severe aggressive interactions between the 2 dogs, and to prevent physical injuries to the owners attempting to separate the dogs during a fight. Environmental management was used to provide the dogs with safe havens and designated resting areas to increase their individual distance, decrease their threat perception, and increase their control over the environment. Behavior modification, based on both classical and operant conditioning, was recommended to enhance safety and increase the predictability of dog-human and dog-dog interactions. Increased environmental control and predictable interactions are known to reduce stress, fear, anxiety, and
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aggressiveness (Notari, 2009). Pharmacologic treatment with serotonergic medication, clomipramine and fluoxetine, was also implemented. The treatment achieved a notable reduction of the interdog aggression and, 6 months after the initial appointment, the dogs could be together in the same room without restraint or confinement, in absence of high-value items and with the owners present. Several of the characteristics observed in the case reported have been previously reported in cases of interdog aggression. Aggression between household dogs is more frequent among same-sex pairs than among household dogs of opposite sex (Bamberger and Houpt, 2006; Overall, 2013a; Sherman et al., 1996; Wrubel et al., 2011). The aggressor (also defined initiator or instigator, i.e., the first dog that will initiate an aggressive interaction by sending a threatening signal, e.g., staring, growling, snarling, biting .) tends to be younger than the victim and to have arrived in the home more recently in more than 50% of reported cases (Sherman et al., 1996; Wrubel et al., 2011). In the case presented, KF initiated most of the aggressive interactions, particularly when highly aroused, but LF had initially growled at KF when in possession of a high-value item. The triggers for aggression observed in the clinical case presented (i.e., possession of high-value items, excitement, and approaching the dog over a resting spot) are among the most frequently reported triggers for aggression between household dogs (Sherman et al., 1996; Wrubel et al., 2011). A noticeable improvement has been reported for more than half of the cases treated in 2 published studies (Sherman et al., 1996; Wrubel et al., 2011). Sherman et al. (1996) report that 56% of the cases treated for aggression to household dogs could be left together; though, 20% required supervision. In the same study, only 14% of the cases treated were considered completely resolved. The pathogenesis of aggression between household dogs has been historically linked to social conflicts motivated by the need to obtain or defend a higher hierarchical status (Sherman et al., 1996). However, the existence of a clear social hierarchy in groups of domestic dogs is controversial (Boitani et al., 1995; Bonanno and Cafazzo, 2014; Landsberg et al., 2013a; Schilder et al., 2014), and the social structure of canine groups seems to be plastic and adaptable to the local environment (Miklósi, 2015; Overall, 2013a). The social dominance of an individual arises primarily from the deference of other members of the group during an interaction, rather than from the assertive act of the specific dominant individual. Without this, there would be no predictability to social stability and a serious risk of injury to members of the social group (De Keuster and Jung, 2009; Van Der Borg et al., 2015). The role of factors other than dominance, that is, inappropriate social and communication skills, temperamental reactivity and excitability, poor environmental control because of human interference, space distribution and availability, and confinement should be considered in cases of aggression between household dogs (De Keuster and Jung, 2009, Landsberg et al., 2013a). Bradshaw et al. (2009) defines dominance as a property of dyadic relationships (i.e., limited to the interactions between 2 dogs, and not applicable to the complex social structure of a group), and suggests that associative learning and subjective resource value are useful factors to consider when analyzing agonistic behaviors between dogs. These results are confirmed by Cafazzo et al. (2010). Associative learning and resource value can contribute to explain LF’s aggression, which started as resource guarding (subjective resource value) and then generalized following sensitization (associative learning) to KF’s aroused behavior. However, factors like temperamental reactivity, high arousability, and lack of social skills should be also considered to explain KF’s aggressive behavior. Owing to the complex nature of aggression between household dogs, a diagnosis of “intra-specific affective aggression” may be more appropriate, as proposed by De
Keuster and Jung (2009), because this diagnosis is based on the underlying neurophysiology of the aggressive response observed rather than its multiple causes or motivations (Carlson, 2013). The existence of a complex environmental system formed by 6 adult individuals (4 dogs and 2 humans) living in a relatively small city space, with the consequent lack of safe individual spaces, presence of multiple simultaneous social interactions and increased stress contributed to the development of the aggression between KF and LF. The institution of a “safe haven” (the crate and the owners’ bedroom) was in fact recommended to provide the dogs with a protected space in which interactions and arousal are minimized, therefore increasing control over the environment, and decreasing stress and aggression (De Keuster and Jung, 2009; Overall, 2013a). A human analogue safe haven effect had been proved for the presence of the owner during a threatening interaction with a stranger. Owners can provide a buffer against stress in dogs, which can even reduce the effect of a subsequent encounter with the same threatening stimuli later when the owner is not present (Gácsi et al., 2013). However, proximity to and attention from the owner may trigger aggression between dogs in the same household (Wrubel et al., 2011), and the human safe haven effect should be used with caution in such cases. Treatment protocols for aggression between household dogs frequently include behavior modification to support the hierarchical status of the dog whose dominance has been challenged (Sherman et al., 1996; Wrubel et al., 2011). Although the multifactorial nature of this behavior problem previously described raises questions and concerns about such treatment, its effectiveness and appropriateness may in fact ultimately decrease the welfare of the dog chosen as submissive, and pose potential hazards for the people and dogs involved (De Keuster and Jung, 2009; Landsberg et al., 2013a). In the case here reported, we preferred the implementation of a treatment aimed to increase the predictability and control of the environment, increase safety, decrease stress and anxiety, and improve the welfare of our patients, which proved to be a successful strategy. Acknowledgments The idea for the study was conceived and the article was written by Carlo Siracusa. Conflict of interest The author declares no conflict of interest. Ethical considerations The work presented did not need approval because it involved only routine clinical treatment. References Alworth, L.C., Buerkle, S.C., 2013. The effects of music on animal physiology, behavior and welfare. Lab. Anim. 42, 54e61. Bamberger, M., Houpt, K., 2006. Signalment factors, comorbidity, and trends in behavior diagnoses in dogs: 1644 cases (1991-2001). J. Am. Vet. Med. Assoc. 229, 1591e1601. Boitani, L., Francisci, F., Ciucci, P., et al., 1995. Population biology and ecology of feral dogs in central Italy. In: Serpell, J. (Ed.), The Domestic Dog, its Evolution, Behavior and Interactions with People. Cambridge University Press, Cambridge, pp. 217e244. Bonanno, R., Cafazzo, S., 2014. The social organization of a population of freeranging dogs in a suburban area of Rome: A reassessment of the effects of domestication on dogs’ behavior. In: Kaminski, J., Marshall-Pescini, S.M. (Eds.), The Social Dog: Behavior and Cognition. Academic Press, San Diego, pp. 65e104. Bradshaw, J.W.S., Blackwell, E.J., Casey, R.A., 2009. Dominance in domestic dogs useful construct or bad habit? J. Vet. Behav.: Clin. Appl. Res. 4, 135e144.
C. Siracusa / Journal of Veterinary Behavior xxx (2015) 1e7 Cafazzo, S., Valsecchi, P., Bonanni, R., Natoli, E., 2010. Dominance in relation to age, sex, and competitive contexts in a group of free-ranging domestic dogs. Behav. Ecol. 21, 443e455. Carlson, N.R., 2013. Neurophysiology of Behavior, 11th Ed. Person Education, Upper Aaddle River, NJ, pp. 360e392. Crowell-Davis, S.L., Murray, T., 2006a. Selective serotonin reuptake inhibitors. In: Crowell-Davis, S.L., Murray, T. (Eds.), Veterinary Psychopharmacology. Blackwell Publishing, Ames, pp. 80e110. Crowell-Davis, S.L., Murray, T., 2006b. Tricyclic antidepressants. In: CrowellDavis, S.L., Murray, T. (Eds.), Veterinary Psychopharmacology. Blackwell Publishing, Ames, pp. 179e206. Crowell-Davis, S.L., Landsberg, G.M., 2009. In: Horwitz, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine, 2nd Ed. BSAVA, Gloucester, pp. 245e258. De Keuster, T., Jung, H., 2009. Aggression toward familiar people and animals. In: Horwitz, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine, 2nd Ed. BSAVA, Gloucester, pp. 182e210. Gácsi, M., Maros, K., Sernkvist, S., Farago, T., Miklósi, A., 2013. Human analogue safe haven effect of the owner: Behavioural and heart rate response to stressful social stimuli in dogs. PLoS ONE 8, e58475. Herron, M.E., Shofer, F.S., Reisner, I.R., 2009. Survey of the use and outcome of confrontational and non-confrontational training methods in client-owned dogs showing undesired behavior. Appl. Anim. Behav. Sci. 117, 47e54. Jenike, M.A., Baer, L., Greist, J.H., 1990. Clomipramine versus fluoxetine in obsessive compulsive disorder: A retrospective comparison of side effects and efficacy. J. Clin. Psychopharmacol. 10, 122e124. Landsberg, G., Hunthausen, W., Ackerman, L.F., 2013a. Canine aggression. In: Landsberg, G., Hunthausen, W., Ackerman, L.F. (Eds.), Behavior Problems of the Dog and Cat, 3rd Ed. Saunders Elsevier, London, pp. 297e326. Landsberg, G., Hunthausen, W., Ackerman, L.F., 2013b. Treatmentdbehavior modification techniques. In: Landsberg, G., Hunthausen, W., Ackerman, L.F. (Eds.), Behavior Problems of the Dog and Cat, 3rd Ed. Saunders Elsevier, London, pp. 95e112. Mertens, P.A., 2002. Canine aggression. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 195e215. Miklósi, A., 2015. Intra-specific social organization in dogs and related forms. In: Miklósi, A. (Ed.), Dog Behavior, Evolution and Cognition, 2nd Ed. Oxford University Press, Oxford, pp. 172e182.
7
Mills, D.S., 2002. Learning, training and behaviour modification techniques. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 37e48. Mills, D.S., Simpson, B.S., 2002. Psychotropic agents. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 237e248. Notari, L., 2009. Stress in veterinary behavioural medicine. In: Horwitz, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine, 2nd Ed. BSAVA, Gloucester, pp. 136e145. Overall, K.L., 1994. Use of clomipramine to treat ritualistic motor behavior in dogs. J. Am. Vet. Med. Assoc 205, 1733e1741. Overall, K.L., 2013a. Abnormal canine behavior and behavioural pathologies involving aggression. In: Overall, K.L. (Ed.), Manual of Clinical Behavior Medicine for Dogs and Cats. Elsevier Mosby, St. Louis, pp. 172e230. Overall, K.L., 2013b. Supplemental materials: client handouts. In: Overall, K.L. (Ed.), Manual of Clinical Behavior Medicine for Dogs and Cats. Elsevier Mosby, St. Louis, pp. 574e796. Reisner, I., 2002. An overview of aggression. In: Horwitz, D., Mills, D., Heath, S. (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine. BSAVA, Gloucester, pp. 181e194. Schilder, M.B.H., Vinke, C.M., Van Der Borg, J.A.M., 2014. Dominance in domestic dogs revisited: Useful habit and useful construct? J. Vet. Behav.: Clin. Appl. Res. 9, 184e191. Sherman, C.K., Reisner, I.R., Taliaferro, L.A., et al., 1996. Characteristics, treatment, and outcome of 99 cases of aggression between dogs. Appl. Anim. Behav. Sci. 47, 91e108. Stockham, S.L., Scott, M.A., 2008a. Enzymes. In: Stockham, S.L., Scott, M.A. (Eds.), Fundamentals of Veterinary Clinical Pathology, 2nd Ed. Blackwell Publishing, Ames, pp. 640e674. Stockham, S.L., Scott, M.A., 2008b. Urinary system. In: Stockham, S.L., Scott, M.A. (Eds.), Fundamentals of Veterinary Clinical Pathology, 2nd Ed. Blackwell Publishing, Ames, pp. 415e494. Van der Borg, J.A., Schilder, M.B., Vinke, C.M., de Vries, H., 2015. Dominance in domestic dogs: A quantitative analysis of its behavioural measures. PLoS ONE 10, e0133978. Wrubel, K.M., Moon-Fanelli, A.A., Maranda, L.S., et al., 2011. Interdog household aggression: 38 cases (2006-2007). J. Am. Vet. Med. Assoc. 238, 731e 740.