Journal of Veterinary Behavior 22 (2017) 24e28

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Journal of Veterinary Behavior

journal homepage: www.journalvetbehavior.com

Canine Research

2017 Journal of Veterinary Behavior Early Career Scientist Award in Behavioral Medicine

Approaching phantom complex after limb amputation in the canine

species
Marika Menchetti a, *, Gualtiero Gandini a, Antonella Gallucci a, Giorgia Della Rocca b,
Lara Matiasek c, Kaspar Matiasek d, Fabio Gentilini a, Marco Rosati d
a
Department of Veterinary Medical Sciences, University of Bologna, Ozzano dell’Emilia, Bologna, Italy
b
Department of Veterinary Medicine, University of Perugia, Perugia, Italy
c
Neurology Referral Service, Tierklinik Haar, Haar, Germany
d
Section of Clinical and Comparative Neuropathology, Centre for Clinical Veterinary Medicine, Ludwig Maximilians University of Munich, Munich,
Germany

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.

Introduction 2002). PLP has been reported to occur in 60%-80% of patients

The phantom complex (PC) is a multifaceted syndrome that
includes (1) phantom limb sensation, which is defined as any
sensation other than pain perceived as originating from an absent
limb; (2) stump pain (SP) defined as pain localized to the remaining
stump; and (3) phantom limb pain (PLP), which is defined as pain
perceived from the area of the former limb that is not physically
part of the body anymore (Hill, 1999; Faisinger et al., 2000; Flor,
* Address for reprint requests and correspondence: Marika Menchetti, Depart-
ment of Veterinary Medical Sciences, University of Bologna, Ozzano dell’Emilia,
Bologna 40064, Italy. Tel: þ39 0512097318; Fax: þ39 0512097687.
E-mail address: marika.menchetti3@unibo.it (M. Menchetti).
within the first 2 years after amputation and, in up to 10%, may
persist throughout life (Melzack et al., 1971; Nikolajsen et al., 1997;
Probstner et al., 2010).
Clinically, PLP may be confused or overlap with common
postsurgical SP. However, SP usually subsides with healing, whereas
PLP persists in 5%-10% of cases and may worsen over time evolving
into a chronic and neuropathic type of pain (Jensen et al., 1983;
Nikolajsen and Jensen, 2001).
The amputation of a limb is a procedure commonly performed
on small animals. The degree of adaptation, presence of risk factors
associated with a poor quality of life, and owner satisfaction have
been the topics of several veterinary studies during the past years
(Withrow and Hirsch, 1979; Carberry and Harvey, 1987;
Kirpensteijn et al., 1999; Dickerson et al., 2015; Raske et al., 2015;

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