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2017 Journal of Veterinary Behavior Early Career Scientist Award in Behavioral Medicine
2017 Journal of Veterinary Behavior Early Career Scientist Award in Behavioral Medicine
Canine Research
2017 Journal of Veterinary Behavior Early Career Scientist Award in Behavioral Medicine
a r t i c l e i n f o a b s t r a c t
Article history: The objective of this study was to describe the presence, prevalence, clinical manifestations, and risk
Received 6 May 2017 factors of phantom complex and its effect on the quality of life for dogs that underwent amputation of a
Received in revised form limb. An online questionnaire was developed containing 3 sections with a total of 69 questions. Clinical
18 August 2017
cases were recruited from a web site for 3-legged dog owners. Data were acquired from February to
Accepted 12 September 2017
March 2015. Descriptive statistics and frequency distribution analyses were performed on the collected
Available online 19 September 2017
data. Chi-squared test or Fisher’s exact test were used for assessment of the associations between
categorical variables. One hundred seven questionnaires were completed by owners of dogs with limb
Keywords:
dog
amputation. The most frequent reason for amputation was related to neoplasia (54%). Pain after limb
pain amputation was commonly experienced by dogs, and the time of onset and clinical manifestations of
phantom complex pain after limb amputation were found to resemble those of phantom complex. The duration of pre-
neuropathic pain amputation pain and time between diagnosis and amputation were identified as risk factors for a
quality of life higher frequency of post-amputation pain episodes. This pilot study introduces previously unreported
signs that may be interpreted as expressions of pain in amputee dogs.
Ó 2017 Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.jveb.2017.09.010
1558-7878/Ó 2017 Elsevier Inc. All rights reserved.
M. Menchetti et al. / Journal of Veterinary Behavior 22 (2017) 24e28 25
Galindo-Zamora et al., 2016). However, none of those studies have or partial surgical amputation of 1 limb at least 3 months before,
specifically addressed the occurrence of pain and pain-related be- regardless of the reason for amputation. Based on previous studies
haviors after amputation that could account for PC. Hence, we in humans, this 3-month time frame was considered to be a suffi-
evaluated a client-owned population of dogs with limb amputation cient period to discriminate between the development of post-
through the use of an online survey sought to document the surgical pain only and the occurrence of PC in a nonverbalizing
prevalence of PC by identifying signs and behaviors suggestive of patient.
neuropathic pain, evaluate risk factors associated with PC occur- Skip logic was used in the design of the questionnaire, thereby
rence, and determine the owners’ perceptions of the quality of life allowing participants to skip some questions and be redirected to a
(QoL) of their 3-legged pets. subsequent set of queries based on preceding answers, and it was
not mandatory to answer all questions within a section before
Materials and methods proceeding to the next section. To be included on data analysis, at
least 80% of the questions had to be answered by each participant.
Questionnaire design and description Therefore, we decided to report the results as percentages with
number of respondents in brackets with percentages calculated on
A trial questionnaire was designed based on the experience of the number of respondents per question.
veterinary specialists, published questionnaires for dogs with limb
amputation and/or chronic pain (Withrow and Hirsch 1979; Statistical analysis
Carberry and Harvey 1987; Kirpensteijn et al., 1999; Hielm-
Bjorkmank et al., 2009), and a pediatric model for chronic pain Data analysis was performed using a statistical analysis software
measurement (http://www.deutsches-kinderschmerzzentrum.de/ (PAST 3.x The past of the future, Hammer & Harper, Natural History
fileadmin/media/PDF-Dateien/englisch/parents_initial_3.0.pdf). Museum, University of Oslo, Norway), whereas calculations were
A first draft of the questionnaire was independently evaluated and performed and graphs were constructed using an electronic
approved by 2 veterinary specialists in palliative care, 2 board-certified spreadsheet (Microsoft Excel, Microsoft Corporation, Microsoft
veterinary neurologists, 3 veterinary surgeons, and a 3-legged pet Redmond campus, Redmond, Washington, USA). The distribution of
owner who is the social media manager of a 3-legged dog owner continuous variables was checked using the Shapiro-Wilk test and
online community (http://tripawds.com/). Ethical approval was normal probability plotting. Categorical or ordinal data are
granted by the University of Bologna ethics committee (ID 664/2016). described as percentages of the total respondents to each individual
The questionnaire included 3 sections with a total of 69 questions question. The associations between categorical variables were
(Supporting Information: Table S1). The first section consisted of 33 assessed using the chi-squared test or Fisher’s exact test depending
questions (19 closed-ended, 9 polar, and 5 open-ended questions) on whether the value in one or more of the cells of the contingency
intended to collect factual data regarding the presence and charac- table was 5 or less. The P values 0.05 were considered significant.
terization of factors related to pre-amputation pain. The second
section consisted of 26 questions (19 closed-ended and 7 polar Results
questions) aimed at collecting data regarding pain-related behaviors,
postsurgical complications, therapies, and QoL. The last section Descriptive data
consisted of 10 questions (5 closed-ended and 5 polar) that evaluated
the owner’s satisfaction and the effects of limb amputation in the One hundred seven completed questionnaires were available for
context of social life. data analysis; of these questionnaires, 56% (60/107) referred to 32
Pain was characterized in terms of (1) prevalence, as pain breeds of purebred dogs, with golden retrievers (17%; 10/60) and
observed by the owner before and after amputation; (2) onset, as Labrador retrievers (15%; 9/60) being most highly represented.
the time in which the dogs started showing pain-related behaviors; Mixed-breed dogs accounted for 44% (47/107) of the population.
(3) frequency, as pain recorded episodes (several times daily, Among the dogs, the mean age at the time of the survey was
weekly, monthly or yearly); and (4) type, as pain quality described 7.6 years (median 8 years, range 0.6e16 years). With respect to sex
as persistent, waxing and waning, or sudden and transient (refer- distribution, 56% (60/107) of the dogs were male (70% neutered; 42/
ring to a 7-day pre-amputation, a “typical week” post-amputation, 60) and 44% (47/107) were female (66% spayed; 31/107). At the time
and a “typical month” post-amputation). With “typical week” and of amputation, 39% of the dogs (42/107) were 6-10 years old, 31%
“typical month,” the authors referred to a representative time frame (33/107) were 1-5 years old, 21% (22/107) were 1 year old or less,
of the ordinary pet’s life, of 1 week or month, respectively, during and 9% (10/107) were 11-15 years old. At the time of the study, 79%
the post-amputation phase. (85/107) of the dogs were still alive. Most of the dogs were large
Furthermore, “pain onset before amputation” and “time be- sized, with dogs over 25 kg accounting for 60% (64/107) of the
tween diagnosis and amputation” were defined as the moment in subjects, whereas medium-sized dogs (10-25 kg) accounted for 28%
which dogs started showing signs of pain and the time elapsed (30/104), and small-sized dogs (<10 kg) accounted for 12% (13/104)
between the diagnosis of the underlying disease and amputation. of the canine amputees.
The main reason for amputation was neoplasia (54%; 58/107),
Recruitment of responders followed by trauma (40%; 43/107), limb malformation (3%; 3/107),
and infection (3%; 3/107). In 75% (80/107) of dogs, the entire limb
The questionnaire was administered via an online survey software was amputated, whereas the remaining 25% (27/107) underwent
and questionnaire tool (SurveyMonkey, Online survey services, Palo partial amputation. Of the 107 dogs, 61% (65/107) underwent
Alto, California, USA) from February to March 2015. The study was thoracic and 39% (42/107) underwent pelvic limb amputation
advertised, and the enrollment of the cases was announced on the (Supporting Information: Table S2).
web site and corresponding social media profile of a 3-legged dog
owner community called “Tripawds” (http://tripawds.com), the Pain before and after amputation
members of which were invited to participate in the survey.
The inclusion criteria for participation consisted of being a cur- According to the owners’ perspective, pain was reported in 82%
rent or former owner of a dog that had undergone either complete of dogs before surgery (75/91) and in 85% of dogs after amputation
26 M. Menchetti et al. / Journal of Veterinary Behavior 22 (2017) 24e28
(78/92), regardless the time of surgery, with no significant differ- restless (10/61), 11% chewed the stump (1/9), and 8% scratched the
ence (P ¼ 0.6). stump (1/13) (Supporting Information: Table S4).
Regarding the onset of pain before amputation, 53% (36/68) Furthermore, behavioral changes in terms of aggression and
reported that dogs experienced pain more than 1 month before withdrawal from interactions with humans and animals were
surgery (69% of oncologic patients), whereas the remaining 47% described both before and after the surgery. In particular, in the pre-
(32/68) described pain from 24 hours to 4 weeks before amputation amputation phase, owners described episodes of aggression toward
(Supporting Information: Table S3). humans (10%; 8/83) and animals (18%; 15/83) and the tendency to
Onset of pain before surgery was not associated with the prevent contacts with humans (16%; 13/83) and animals (17%; 14/
development of postsurgical pain (P ¼ 0.09). However, the time 81). The same changes in behavior were reported in the
of pain onset before amputation was significantly associated -amputation phase regarding aggression toward humans and
with the frequency of post-amputation pain, with a significantly animals (8%; 6/79 and 17%; 13/78, respectively) and prevention of
higher frequency of pain episodes reported in dogs that showed human and animal contacts (14%; 11/79 and 21%; 17/82,
an early (more than 1 month) onset of pain before amputation (P respectively), without significant differences between the 2 phases
< 0.01). (P > 0.1).
After the amputation, 79% of owners (51/64) felt that their dogs Environmental and/or physical stress, as judged by the owner,
experiencing pain only in the postsurgical recovery period (from was reported in relation to the onset of pain in 78% of dogs that
24 hours to 4 weeks after amputation). However, 9% (6/64) experienced pain after amputation (46/59). Accessory symptoms
described pain from 1 to 3 months after surgery and 5% (3/64) that could possibly account for pain during the post-amputation
experiencing pain from 3 to 6 months after surgery. Furthermore, period were reported in 26% of the dogs (22/84). In particular,
7% (4/64) described pain episodes in different occasions from the owners described tiredness (16/22), tachypnea (15/22), and irrita-
immediately postsurgical to 6 months after amputation bility (7/22). Moreover, in 18% (4/22), these symptoms appeared at
(Supporting Information: Table S3). least 3 months after amputation (Supporting Information: Table S4).
Regarding the frequency of pre- and post-amputation pain ep-
isodes, no differences were observed (P ¼ 0.4), and dogs experi- Therapies
enced mostly daily episodes of pain before (57%; 38/67) and after
surgery (57%; 36/63) (Supporting Information: Table S3). Of the dogs, 79% (76/96) received medical treatment before the
The type of pain was significantly different in the presurgical amputation. The most frequently administered treatments were
and postsurgical periods (P < 0.01), as owners described pain pain killers (65/96) and anti-inflammatory drugs (48/96)
experienced by their pets 7 days before amputation mostly as (Supporting Information: Table S5). In 46% of the dogs (26/56),
“waxing and waning” in 45% of dogs (29/65) and “persistent” in 40% these treatments were administered for more than 1 month before
(26/65), whereas in a typical month after amputation, they referred surgery. Medical treatments before amputation were not statisti-
to it as “sudden and transient” in 53% (20/38) with none experi- cally associated with the occurrence of pain during the post-
encing persistent pain (Supporting Information: Table S3). amputation period (P ¼ 0.3).
The etiological diagnosis was made between 24 hours and After amputation, treatments were administered to all dogs (91/91)
4 weeks in most dogs (73%; 69/95) and more than 1 month before for which information was available. Before amputation, the most
the surgery in only 27% (26/95). However, no association was frequently administered treatments were pain killers (85/91), followed
observed between length of time from diagnosis to amputation and by antibiotics (63/91) (Supporting Information: Table S5).
the prevalence of pain after amputation (P ¼ 0.6). When specifically asked about administered drugs because of pain
Complications after surgery occurred in 20% (19/95) of the after amputation, the most frequently reported medications were
cases, mostly identified during the first week after surgery (95%; pain killers (55/85), followed by anti-inflammatory drugs (47/85),
17/18). More frequent complications (owners could choose more while specific treatments for neuropathic pain, such as gabapentin,
than 1 answer) were infections (7/17), surgical wound swelling were administered in 22/85 of dogs (Supporting Information:
(6/17), and suture failure (6/17). Furthermore, 6/17 owners Table S5).
identified “pain” as postsurgical complication. No significant
difference in terms of the prevalence of pain after amputation Quality of life
was identified between dogs with and without postsurgical
complications. The degree of adaptation after amputation was described from
“good” to “very good” in 94% of dogs (89/95) and 72% (67/93) were
Manifestations related to the PC able to ambulate within the first week after amputation. Dogs that
exhibited a higher degree of adaptation were associated with a lower
During the first 3-6 months’ post-amputation, owners described probability of experiencing pain during a “typical month” (P ¼ 0.02)
reduced activity levels (67%; 55/82) and overall playfulness (46%; and adapted more quickly (P ¼ 0.005). Regarding the degree of
38/82), a negative emotional state (44%; 35/80), decreased partic- mobility during a “typical week” after the amputation, owners
ipation in family life (31%; 25/81), appetite loss (30%; 25/82), and reported some movement restrictions, as difficulties in jumping
reduced sleep (21%; 17/80). (28%; 24/87) and moving after a major activity (24%; 21/86)
Interactions between the dogs and other animals were also (Supporting Information: Table S6).
impaired in terms of decreased friendliness with family pets (14%;
11/79) and unfamiliar pets (19%; 22/80). Owners’ satisfaction and perspective
Focusing on the presence of possible PC-related behaviors, dogs
exhibited different manifestations of pain or discomfort After the amputation, 59% of owners (46/78) reported an
(Supporting Information: Table S4). In particular, among dogs improvement in the quality of their relationship with their pets,
showing those manifestations in the time frame comprised from and in 75% of cases (62/83), the overall response of the family to the
3 months to more than 1 year after amputation, 35% exhibited amputation was considered to be “very positive.” However, during
muscular twitching in the stump region (23/66), 23% licked the the first month after amputation, 62% of owners (50/81) felt that
stump (10/43), 19% whimpered (10/52), 17% yelped (6/35), 16% were their pet caused conflicts in their work or daily activities, 52%
M. Menchetti et al. / Journal of Veterinary Behavior 22 (2017) 24e28 27
(42/80) expressed a feeling of limited independence, and 46% As previously described (Raske et al., 2015), postsurgical
(37/81) felt that their social life was limited. Nevertheless, 89% of complications occurred in 20% of dogs and the most commonly
the interviewees (70/79) did not regret the decision to have their reported was infection. No relations were found between the
pet undergone amputation, and 92% of the owners (71/77) felt that occurrence of pain after amputation and postoperative complica-
they had been well informed by their veterinarian during the tions. Similarly to other investigations (Kirpensteijn et al., 1999;
decision-making process (Supporting Information: Table S7). Dickerson et al., 2015; Galindo-Zamora et al., 2016), 94% of the
evaluated dogs adapted very well to amputation, regardless of
Discussion which limb (thoracic or pelvic) was amputated or at which level
(complete or partial) the amputation occurred. Interestingly, the
The present investigation represents a preliminary step better and quicker the recovery of dogs, the lower the incidence of
approaching PC in dogs after amputation of a limb. According to our post-amputation pain. This association may suggest that a shorter
survey, 14% of owners felt that their dogs experiencing pain from 1 recovery time might be directly related to either reduced/absent
to 6 months after surgery with and without accompanying pain perception during the postsurgical period and/or the effec-
behavioral changes. Similarly in human amputees, 5%-10% of tiveness of proper pain control.
patients report persistence and worsening of pain beyond the stage In our survey, owners reported behavioral changes both before and
of postsurgical healing, leading to the development of a debilitating after amputation. Similar changes have been previously described in
and neuropathic type of pain (Nikolajsen et al., 1997; Hill, 1999; canine amputation patients, with modifications including aggression
Nikolajsen and Jensen, 2001; Meissner et al., 2015). Taken and anxiety (Kirpensteijn et al., 1999). However, as was reported by
together, these findings suggest that the establishment of neuro- Kirpensteijn (1999), it was not possible to determine the reason for
pathic pain in the residual limb may be delayed for months after these changes in behavior. This common finding could reflect that the
surgical resection and that postoperative care might/should go well presence of pain could be the consequence of a physical limitation or
beyond wound healing. could not be related to the amputation at all.
The type of pain showed a transformation in its pattern The vast majority of interviewees did not regret their decision
changing from a “waxing and waning” and “persistent” before regarding amputation. Within the first month after surgery, owners
amputation to “sudden and transient” after. Such an evolution reported limited independence and conflicts with everyday activ-
might be explained by a first sensitization phase because of the ities. However, these limitations proved to be transient and the
inciting disease, followed by abnormal circuit rearrangement in a pet’s overall QoL was perceived as satisfactory, as previously
manner prone to eliciting bursts of abnormal sensory neuronal described (Withrow and Hirsch, 1979; Carberry and Harvey, 1987;
firing (Dworkin et al., 2003). This observation may support the Kirpensteijn et al., 1999; Dickerson et al., 2015; Galindo-Zamora
hypothesis that this pain is either neuropathic in origin or it has a et al., 2016). These findings might, therefore, be seen as in-
neuropathic component. Investigating neuropathic pain and PC dications of positive outcomes after amputation and support
(comprising PLP) in animals represents a clinical challenge. Veter- amputation during a decision-making process that is emotionally
inary patients cannot verbalize, and some dogs can also have very intense for the owners.
high pain threshold showing any sign of discomfort. Therefore, the This study is the first attempt to describe PC in dogs, so there are
information regarding abnormal painful sensations together with several limitations. Medical records were not available for review,
their quality and intensity can easily be missed despite careful and information on the clinical history was taken as provided by the
monitoring (Mathews, 2008). Accordingly, we focused on mani- owner. An owner’s perception of their dog’s pain manifestations is
festations potentially related to discomfort localized on the stump inherently subjective, involving a level of empathy of the observers,
considering a minimum of 3 months after the amputation. Inter- and may have influenced the results of the questionnaire. We used
estingly, up to one-third of the dogs showed some of those mani- a nonvalidated survey, but given the explorative nature of the
festations from 3 months to 1 year after amputation, suggesting investigation and owners were not asked to measure a specific
again a possible late onset of neuropathic pain. phenomenon, we still consider this as a valid approach. To increase
No difference was observed in the frequency of pain before and the objectiveness of this survey, we tailored questions and their
after surgery. Dogs exhibiting signs of pain several times a day before phrasing using a pediatric model for chronic pain measurement in
amputation were more likely to present a similar frequency of pain which parents are asked to evaluate pain in children, as it may get
after surgery. However, the “frequency of pain episodes” questions closer to this situation between observer and subject observed.
did not further specify a time frame in the post-amputation phase; Furthermore, there are no validated and objective pain scales and
hence, variations through time might have gone undetected. surveys for amputee dogs and/or neuropathic pain in this species.
Previous studies of human patients have suggested that having a
duration of pre-amputation pain that is longer than 1 month may serve
Conclusions
as a risk factor for development of chronic PLP (Jensen et al., 1985;
Nikolajsen et al., 1997; Hanley et al., 2007). Accordingly, dogs experi-
Our pilot study introduces previously unreported signs and be-
encing pain for more than 1 month before amputation were signifi-
haviors that may be interpreted as expressions of pain in amputee
cantly more likely to develop daily episodes of pain after amputation.
dogs. These manifestations may be particularly revealing for those
Several studies have attempted to evaluate the relation between
dogs that experienced post-amputation pain initiating at least 1
the administration of treatment and PLP in human amputees and the
month after surgery. The ability to recognize behavioral signs that
majority has shown that pain control before amputation does not
may indicate the presence of unpleasant sensations related to
prevent the development of PLP (Flor, 2002; Richardson et al., 2007).
neuropathic pain would be of great interest, to prevent and treat it.
Similarly, we did not identify any relationship between the admin-
istration of treatment before amputation and the incidence of post-
amputation pain. Stress during the post-amputation phase seems to Aknowledgments
play a role in the development of pain. A possible relation between
stress and the onset of pain was reported in 78% of patients. This is in The authors sincerely thank Dr. Michael Petty, Rene Agredano
accordance with human studies in which psychological stress rep- and the Tripawd community for their assistance in, support of and
resents a risk factor for PLP occurrence (Richardson et al., 2007). advertisement of this study.
28 M. Menchetti et al. / Journal of Veterinary Behavior 22 (2017) 24e28
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Animals and Directive 2010/63/EU and approved by the “Ethics Kinetic, kinematic, magnetic resonance and owner evaluation of dogs before
and after the amputation of a hind limb. BMC Vet. Res. 12, 20.
Committee” of the Department of Veterinary Medical Sciences of Hanley, M.A., Jensen, M.P., Smith, D.G., Ehde, D.M., Edwards, W.T., Robinson, L.R.,
the University of Bologna (record number 664/2016). 2007. Preamputation pain and acute pain predict chronic pain after lower ex-
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Supplementary data
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