- Email: [email protected]
Approaching phantom complex after limb amputation in the canine species
Accepted Manuscript Approaching phantom complex after limb amputation in the canine species Marika Menchetti, Gualtiero Gandini, Antonella Gallucci, Giorgia Della Rocca, Lara Matiasek, Kaspar Matiasek, Fabio Gentilini, Marco Rosati PII:
S1558-7878(17)30090-4
DOI:
10.1016/j.jveb.2017.09.010
Reference:
JVEB 1085
To appear in:
Journal of Veterinary Behavior
Received Date: 6 May 2017 Revised Date:
18 August 2017
Accepted Date: 12 September 2017
Please cite this article as: Menchetti, M., Gandini, G., Gallucci, A., Della Rocca, G., Matiasek, L., Matiasek, K., Gentilini, F., Rosati, M., Approaching phantom complex after limb amputation in the canine species, Journal of Veterinary Behavior (2017), doi: 10.1016/j.jveb.2017.09.010. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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ACCEPTED MANUSCRIPT 1
Approaching phantom complex after limb amputation in the canine species
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Marika Menchetti a, *, Gualtiero Gandini a, Antonella Gallucci a, Giorgia Della Rocca b, Lara
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Matiasek c, Kaspar Matiasek d, Fabio Gentilini a and Marco Rosati d
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a
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dell’Emilia (BO), Italy
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b
Department of Veterinary Medicine, University of Perugia, 06126 Perugia (PG), Italy
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c
Neurology Referral Service, Tierklinik Haar, 85540 Haar, Germany
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Section of Clinical & Comparative Neuropathology, Ludwig-Maximilians-Universität,
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Munich, Germany
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Department of Veterinary Medical Sciences, University of Bologna, 40064 Ozzano
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E-mail address: [email protected] (M. Menchetti).
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* Corresponding author. Tel.: +39 0512097318
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Abstract
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The objective of this study was to describe the presence, prevalence, clinical manifestations
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and risk factors of phantom complex (PC) and its effect on the quality of life for dogs that
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underwent amputation of a limb. An online questionnaire was developed containing three
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sections with a total of 69 questions. Clinical cases were recruited from a website for three-
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legged dog owners. Data were acquired from February to March 2015. Descriptive statistics
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and frequency distribution analyses were performed on the collected data. Chi-squared test or
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Fisher’s exact test were used for assessment of the associations between categorical variables.
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One hundred and seven questionnaires were completed by owners of dogs with limb
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amputation. The most frequent reason for amputation was related to neoplasia (54%). Pain
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after limb amputation was commonly experienced by dogs and the time of onset and clinical
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manifestations of pain after limb amputation were found to resemble those of PC. The
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duration of pre-amputation pain and time between diagnosis and amputation were identified
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as risk factors for a higher frequency of post-amputation pain episodes. This pilot study
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introduces previously unreported signs that may be interpreted as expressions of pain in
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amputee dogs.
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Keywords: Dog; Pain; Phantom Complex; Neuropathic pain; Quality of life
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Introduction
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The Phantom Complex (PC) is a multifaceted syndrome that includes: 1) Phantom Limb
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Sensation (PLS), which is defined as any sensation other than pain perceived as originating
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from an absent limb; 2) Stump Pain (SP) defined as pain localized to the remaining stump
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and 3) Phantom Limb Pain (PLP), which is defined as pain perceived from the area of the
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former limb that is not physically part of the body anymore (Hill, 1999; Faisinger et al., 2000;
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Flor, 2002). PLP has been reported to occur in 60% to 80% of patients within the first 2 years
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after amputation, and in up to 10% may persist throughout life (Melzack et al., 1971;
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Nikolajsen et al., 1997; Probstner et al., 2010).
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Clinically, PLP may be confused or overlap with common post-surgical SP. However, SP
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usually subsides with healing, whereas PLP persists in 5-10% of cases and may worsen over
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time evolving into a chronic and neuropathic type of pain (Nikolajsen and Jensen, 2001).
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The amputation of a limb is a procedure commonly performed on small animals. The degree
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of adaptation, presence of risk factors associated with a poor quality of life and owner
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satisfaction have been the topic of several veterinary studies during the past years (Withrow
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and Hirsch, 1979; Carberry and Harvey, 1987; Kirpensteijn et al., 1999; Dickerson et al.,
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2015; Raske et al., 2015; Galindo-Zamora et al., 2016). However, none of those studies have
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specifically addressed the occurrence of pain and pain-related behaviors after amputation that
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could account for PC. Hence, we evaluated a client-owned population of dogs with limb
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amputation through the use of an online survey sought to document the prevalence of PC by
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identifying signs and behaviors suggestive of neuropathic pain,evaluaterisk factors associated
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with PC occurrence, and determine the owners’ perceptions of the quality of life (QoL) of
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their three-legged pets.
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Materials and Methods
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Questionnaire design and description
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A trial questionnaire was designed based on the experience of veterinary specialists,
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published questionnaires for dogs with limb amputation and/or chronic pain (Withrow and
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Hirsch 1979; Carberry and Harvey 1987; Kirpensteijn et al., 1999; Hielm-Bjorkmank et al.,
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2009), and a pediatric model for chronic pain measurement (http://www.deutsches-
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kinderschmerzzentrum.de/fileadmin/media/PDF-Dateien/englisch/parents_initial_3.0.pdf).
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A first draft of the questionnaire was independently evaluated and approved by 2 veterinary
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specialist inpalliative care, 2 board certified veterinary neurologists, 3 veterinary surgeons,
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and a three-legged pet owner whois the social media manager of a three-legged dog owner
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online community (http://tripawds.com/). Ethical approval was granted by the University of
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Bologna ethics committee (ID 664/2016).
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The questionnaire included three sections with a total of 69 questions (Supporting
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Information: Table S1). The first section consisted of 33 questions (19 closed-ended, 9 polar,
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and 5 open-ended questions) intended to collect factual data regarding the presence and
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characterization of factors related to pre-amputation pain. The second section consisted of 26
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questions (19 closed-ended and 7 polar questions) aimed at collecting data regarding pain-
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related behaviors, post-surgical complications, therapies and QoL. The last section consisted
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of 10 questions (5 closed-ended and 5 polar) that evaluated the owner’s satisfaction and the
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effects of limb amputation in the context of social life.
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Pain was characterized in terms of 1) prevalence, as pain observed by the owner before and
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after amputation; 2) onset, as the time in which the dogs started showing pain-related
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behaviours; 3) frequency, as pain recorded episodes (several times daily, weekly, monthly or
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yearly) and 4) type, as pain quality described as persistent, waxing and waning or sudden and
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ACCEPTED MANUSCRIPT transient (referring to a 7-days pre-amputation, a “typical week” post-amputation and a
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“typical month” post-amputation). With “typical week” and “typical month”, the authors
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referred to a representative time frame of the ordinary pet´s life, of one week or month
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respectively, during the post-amputation phase.
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Furthermore, pain onset before amputation and time between diagnosis and amputation were
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defined as the moment in which dogs started showing signs of pain and the time elapsed
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between the diagnosis of the underlying disease and amputation.
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Recruitment of responders
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The questionnaire was administered via an online survey software and questionnaire tool
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(SurveyMonkey, Online survey services, Palo Alto, California, United States) from February
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to March 2015. The study was advertised and the enrollment of the cases was announced on
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the website and corresponding social media profile of a three-legged dog owner community
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called “Tripawds” (http://tripawds.com), the members of which were invited to participate in
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the survey.
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The inclusion criteria for participation consisted of being a current or former owner of a dog
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that had undergone either complete or partial surgical amputation of one limb at least three
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months prior, regardless of the reason for amputation. Based on previous studies in humans
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this three-month timeframe was considered to be a sufficient period of time to discriminate
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between the development of post-surgical pain only and/or the occurrence of PC in a non-
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verbalizing patient.
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Skip logic was employed in the design of the questionnaire, thereby allowing participants to
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skip some questions and be redirected to a subsequent set of queries based on preceding
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answers, and it was not mandatory to answer all questions within a section prior to
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proceeding to the next section. To be included on data analysis at least 80% of the questions
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had to be answered by each participant. Therefore, we decided to report the results as
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percentages with number of respondents in brackets with percentages calculated on the
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number of respondents per question.
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Statistical analysis
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Data analysis was performed using a statistical analysis software (PAST 3.x The past of the
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future, Hammer & Harper, Natural History Museum, University of Oslo, Norway), while
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calculations were performed and graphs were constructed using an electronic spreadsheet
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(Microsoft Excel, Microsoft Corporation, Microsoft Redmond campus, Redmond,
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Washington, United States). The distribution of continuous variables was checked using the
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Shapiro-Wilk test and normal probability plotting. Categorical or ordinal data are described
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as percentages of the total respondents to each individual question. The associations between
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categorical variables were assessed using the chi-squared test or Fisher’s exact test depending
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on whether the value in one or more of the cells of the contingency table was five or less. P
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values ≤ 0.05 were considered significant.
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Results
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Descriptive data
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One hundred and seven completed questionnaires were available for data analysis; of these
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questionnaires, 56% (60/107) referred to 32 breeds of purebred dogs, with golden retrievers
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(17%; 10/60) and Labrador retrievers (15%; 9/60) being most highly represented. Mixed
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breed dogs accounted for 44% (47/107) of the population. Among the dogs, the mean age at
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the time of the survey was 7.6 years (median 8 years, range 0.6-16 years). With respect to sex
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ACCEPTED MANUSCRIPT distribution, 56% (60/107) of the dogs were male (70% neutered; 42/60) and 44% (47/107)
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were female (66% spayed; 31/107). At the time of amputation, 39% of the dogs (42/107)
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were 6 to 10 years old, 31% (33/107) were 1 to 5 years old, 21% (22/107) were 1-year-old or
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less and 9% (10/107) were 11 to 15 years old. At the time of the study, 79% (85/107) of the
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dogs were still alive. The majority of the dogs were large-size, with dogs over 25 kg
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accounting for 60% (64/107) of the subjects, while medium size dogs (10-25 kg) accounted
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for 28% (30/104) and small size dogs (<10 kg) for 12% (13/104) of the canine amputees.
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The main reason for amputation was neoplasia (54%; 58/107), followed by trauma (40%;
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43/107), limb malformation (3%; 3/107), and infection (3%; 3/107). In 75% (80/107) of dogs,
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the entire limb was amputated, while the remaining 25% (27/107) underwent partial
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amputation. Of the 107 dogs, 61% (65/107) underwent thoracic and 39% (42/107) underwent
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pelvic limb amputation (Supporting Information: Table S2).
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Pain before and after amputation
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According to the owners’ perspective, pain was reported in 82% of dogs before surgery
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(75/91) and in 85% of dogs after amputation (78/92), regardless the time of surgery, with no
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significant difference (P = 0.6).
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Regarding the onset of pain before amputation, 53% (36/68) reported that dogs experienced
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pain more than one month before surgery (69% of oncologic patients), while the remaining
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47% (32/68) described pain from 24 h to 4 weeks before amputation (Supporting
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Information: Table S3).
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Onset of pain before surgery was not associated with the development of postsurgical pain (P
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= 0.09). However, the time of pain onset before amputation was significantly associated with
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the frequency of post-amputation pain, with a significantly higher frequency of pain episodes
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(P < 0.01).
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After the amputation, 79% of owners (51/64) felt their dogs experiencing pain only in the
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post-surgical recovery period (from 24 hours to 4 weeks after amputation). However, 9%
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(6/64) described pain between 1 to 3 month after surgery and 5% (3/64) experiencing pain
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between 3 to 6 months after surgery. Furthermore, 7% (4/64) described pain episodes in
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different occasions from the immediately post-surgical to 6 months after amputation
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(Supporting Information: Table S3).
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Regarding the frequency of pre- and post-amputation pain episodes, no differences were
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observed (P = 0.4) and dogs experienced mostly daily episodes of pain before (57%; 38/67)
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and after surgery (57%; 36/63) (Supporting Information: Table S3).
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The type of pain was significantly different in the pre- and post-surgical periods (P < 0.01), as
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owners described pain experienced by their pets 7 days prior to amputation mostly as
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“waxing and waning” in 45% of dogs (29/65) and “persistent” in 40% (26/65), whereas in a
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typical month after amputation they referred to it as “sudden and transient” in 53% (20/38)
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with none experiencing persistent pain (Supporting Information: Table S3).
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The etiological diagnosis was made between 24 hours to 4 weeks in the majority of dogs
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(73%; 69/95) and more than 1 month before the surgery in only 27% (26/95). However, no
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association was observed between length of time from diagnosis to amputation and the
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prevalence of pain after amputation (P = 0.6).
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Complications after surgery occurred in 20% (19/95) of the cases, mostly identified during
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the first week after surgery (95%; 17/18). More frequent complications (owners could choose
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more than one answer) were infections (7/17), surgical wound swelling (6/17) and suture
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failure (6/17). Furthermore, 6/17 owners identified “pain” as post-surgical complication. No
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significant difference in terms of the prevalence of pain after amputation was identified
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between dogs with and without post-surgical complications.
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Manifestations related to the PC
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Between the first 3-6 months post-amputation, owners described reduced activity levels
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(67%; 55/82) and overall playfulness (46%; 38/82), a negative emotional state (44%; 35/80),
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decreased participation in family life (31%; 25/81), appetite loss (30%; 25/82), and reduced
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sleep (21%; 17/80).
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Interactions between the dogs and other animals were also impaired in terms of decreased
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friendliness with family pets (14%; 11/79) and unfamiliar pets (19%; 22/80).
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Focusing on the presence of possible PC-related behaviors, dogs exhibited different
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manifestations of pain or discomfort (Supporting Information: Table S4). In particular,
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among dogs showing those manifestations in the timeframe comprised from 3 months to more
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than 1 year after amputation, 35% exhibited muscular twitching in the stump region (23/66),
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23% licked the stump (10/43), 19% whimpered (10/52), 17% yelped (6/35), 16% were
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restless (10/61), 11% chewed the stump (1/9) and 8% scratched the stump (1/13) (Supporting
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Information: Table S4).
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Furthermore, behavioral changes in terms of aggression and withdrawal from interactions
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with humans and animals were described both before and after the surgery. In particular, in
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the pre-amputation phase, owners described episodes of aggression towards humans (10%;
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8/83 ) and animals (18%; 15/83) and the tendency to prevent contacts with humans (16%;
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13/83) and animals (17%; 14/81). The same changes in behaviour were reported in the post-
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amputation phase regarding aggression towards humans and animals (8%; 6/79 and 17%;
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13/78 respectively) and prevention of human and animal contacts (14%; 11/79 and 21%;
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17/82 respectively), without significant differences between the two phases (P > 0.1).
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onset of pain in 78% of dogs that experienced pain after amputation (46/59). Accessory
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symptoms that could possibly account for pain during the post amputation period were
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reported in 26% of the dogs (22/84). In particular, owners described tiredness (16/22),
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tachypnea (15/22) and irritability (7/22). Moreover, in 18% (4/22) these symptoms appeared
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at least 3 months after amputation (Supporting Information: Table S4).
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Therapies
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Of the dogs, 79% (76/96) received medical treatment before the amputation. The most
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frequently administered treatments were pain killers (65/96) and anti-inflammatory drugs
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(48/96) (Supporting Information: Table S5). In 46% of the dogs (26/56) these treatments
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were administered for more than 1 month prior to surgery. Medical treatments before
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amputation were not statistically associated with the occurrence of pain during the post-
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amputation period (P = 0.3).
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After amputation, treatments were administered to all dogs (91/91) for which information
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was available. As before amputation, the most frequently administered treatments were pain
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killers (85/91), followed by antibiotics (63/91) (Supporting Information: Table S5).
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When specifically asked about administered drugs because of pain after amputation, the most
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frequently reported medications were pain killers (55/85), followed by anti-inflammatory
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drugs (47/85), while specific treatments for neuropathic pain, such as gabapentin, were
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administered in 22/85 of dogs (Supporting Information: Table S5).
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Quality of Life
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The degree of adaptation after amputation was described from “good” to “very good” in 94%
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of dogs (89/95) and 72% (67/93) were able to ambulate within the first week after
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ACCEPTED MANUSCRIPT amputation. Dogs that exhibited a higher degree of adaptation were associated with a lower
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probability of experiencing pain during a “typical month” (P = 0.02) and adapted more
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quickly (P = 0.005). Regarding the degree of mobility during a “typical week” after the
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amputation, owners reported some movement restrictions, as difficulties in jumping (28%;
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24/87) and moving after a major activity (24%; 21/86) (Supporting Information: Table S6).
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Owners’ satisfaction and perspective
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After the amputation, 59% of owners (46/78) reported an improvement in the quality of their
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relationship with their pets and in 75% of cases (62/83) the overall response of the family to
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the amputation was considered to be “very positive”. However, during the first month
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following amputation, 62% of owners (50/81) felt that their pet caused conflicts in their work
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or daily activities, 52% (42/80) expressed a feeling of limited independence, and 46% (37/81)
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that their social life was limited. Nevertheless, 89% of the interviewees (70/79) did not regret
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the decision to have their pet undergone amputation, and 92% of the owners (71/77) felt that
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they had been well informed by their veterinarian during the decision-making process
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(Supporting Information: Table S7).
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Discussion
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The present investigation represents a preliminary step approaching phantom complex in
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dogs after amputation of a limb. According to our survey, 14% of owners felt their dogs
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experiencing pain between 1 to 6 months after surgery with and without accompanying
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behavioral changes. Likewise in human amputees, 5-10% of patients report persistence and
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worsening of pain beyond the stage of post-surgical healing, leading to the development of a
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ACCEPTED MANUSCRIPT debilitating and neuropathic type of pain (Nikolajsen et al., 1997; Hill, 1999; Nikolajsen and
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Jensen, 2001; Meissner et al., 2015). Taken together these findings suggest that the
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establishment of neuropathic pain in the residual limb may be delayed for months after
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surgical resection and that post-operative care might/should go well beyond wound healing.
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The type of pain showed a transformation in its pattern changing from a “waxing and
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waning” and “persistent” before amputation to “sudden and transient” after. Such an
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evolution might be explained by a first sensitization phase, because of the inciting disease,
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followed by abnormal circuit re-arrangement in a manner prone to eliciting bursts of
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abnormal sensory neuronal firing (Dworkin et al., 2003). This observation may support the
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hypothesis that this pain is either neuropathic in origin or it has a neuropathic component.
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Investigating neuropathic pain and PC (comprising PLP) in animals represents a clinical
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challenge. Veterinary patients cannot verbalize and some dogs can also have very high pain
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threshold showing any sign of discomfort. Therefore, the information regarding abnormal
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painful sensations together with their quality and intensity can easily be missed despite
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careful monitoring (Mathews, 2008). Accordingly, we focused on manifestations potentially
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related to discomfort localized on the stump considering a minimum of three months after the
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amputation. Interestingly, up to one third of the dogs showed some of those manifestations
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from 3 months to 1 year after amputation, suggesting again a possible late onset of
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neuropathic pain.
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No difference was observed in the frequency of pain before and after surgery. Dogs
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exhibiting signs of pain several times a day prior to amputation were more likely to present a
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similar frequency of pain after surgery. However, the “frequency of pain episodes” questions
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did not further specify a timeframe in the post amputation phase, hence variations through
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time might have gone undetected.
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ACCEPTED MANUSCRIPT Previous studies of human patients have suggested that having a duration of pre-amputation
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pain that is longer than 1 month may serve as a risk factor for development of chronic PLP
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(Jensen et al., 1985; Nikolajsen et al., 1997; Hanley et al., 2007). Accordingly, dogs
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experiencing pain for more than 1 month before amputation were significantly more likely to
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develop daily episodes of pain after amputation.
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Several studies have attempted to evaluate the relation between the administration of
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treatment and PLP in human amputees and the majority has shown that pain control before
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amputation does not prevent the development of PLP (Flor, 2002; Richardson et al., 2007).
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Likewise, we did not identify any relationship between the administration of treatment before
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amputation and the incidence of post-amputation pain. Stress during the post amputation
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phase seems to play a role in the development of pain. A possible relation between stress and
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the onset of pain was reported in 78% of patients. This is in accordance with human studies in
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which psychological stress represents a risk factor for PLP occurrence (Richardson et al.,
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2007).
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As previously described (Raske et al., 2015), post-surgical complications occurred in 20% of
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dogs and the most commonly reported was infection. No relations were found between the
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occurrence of pain after amputation and post-operative complications. Similarly to other
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investigations (Kirpensteijn et al., 1999; Dickerson et al., 2015; Galindo-Zamora et al., 2016),
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94% of the evaluated dogs adapted very well to amputation, regardless of which limb
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(thoracic or pelvic) was amputated or at which level (complete or partial) the amputation
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occurred. Interestingly, the better and quicker the recovery of dogs, the lower the incidence of
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post-amputation pain. This association may suggest that a shorter recovery time might be
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directly related to either reduced/absent pain perception during the post-surgical period
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and/or the effectiveness of proper pain control.
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ACCEPTED MANUSCRIPT In our survey owners reported behavioral changes both before and after amputation. Similar
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changes have been previously described in canine amputation patients, with modifications
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including aggression and anxiety (Kirpensteijn et al., 1999). However, as was reported by
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Kirpensteijn (1999), it was not possible to determine the reason for these changes in behavior.
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This common finding could reflect the presence of pain could be the consequence of a
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physical limitation or could be not related to the amputation at all.
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The vast majority of interviewees did not regret their decision regarding amputation. Within
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the first month post-surgery, owners reported limited independence and conflicts with
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everyday activities. However, these limitations proved to be transient and the pet’s overall
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QoL was perceived as satisfactory, as previously described (Withrow and Hirsch, 1979;
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Carberry and Harvey, 1987; Kirpensteijn et al., 1999; Dickerson et al., 2015; Galindo-
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Zamora et al., 2016). These findings might, therefore, be seen as indications of positive
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outcomes following amputation and support amputation during a decision making process
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that is emotionally intense for the owners.
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This study is the first attempt to describe PC in dogs, so there are several limitations. Medical
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records were not available for review and information on the clinical history was taken as
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provided by the owner. An owner’s perception of their dog’s pain manifestations is inherently
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subjective, involving alevel of empathy of the observers, and may have influenced the results
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of the questionnaire. We used a non-validated survey but given the explorative nature of the
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investigation and owners were not asked to measure a specific phenomenon, we still consider
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this as a valid approach. In order to increase the objectiveness of this survey we tailored
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questions and their phrasing using a pediatric model for chronic pain measurement in which
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parents are asked to evaluate pain in children, as it may get closer to this situation between
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observer and subject observed. Furthermore, there are no validated and objective pain scales
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and surveys for amputee dogs and/or neuropathic pain in this species.
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Conclusions
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Our pilot study introduces previously unreported signs and behaviors that may be interpreted
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as expressions of pain in amputee dogs. These manifestations may be particularly revealing
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for those dogs that experienced post-amputation pain initiating at least one month after
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surgery. The ability to recognize behavioral signs that may indicate the presence of
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unpleasant sensations related to neuropathic pain would be of great interest, in order to
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prevent and treat it.
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Ethical statement
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The work has been reviewed in accordance with the standards recommended by the Guide for
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the Care and Use of Laboratory Animals and Directive 2010/63/EU and approved by the
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“Ethics Committee” of the Department of Veterinary Medical Sciences of the University of
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Bologna (record number 664/2016).
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Authorship
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The idea for the article was conceived by M. Rosati and G. Della Rocca. The experiments
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were designed by M. Rosati, M. Menchetti and A. Gallucci. The experiments were performed
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by M. Menchetti and M. Rosati. The data were analyzed by M. Menchetti and F. Gentilini.
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The article was written by M. Menchetti, M. Rosati, G. Gandini, A, Gallucci, L. Matiasek, K.
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Matiasek.
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Conflict of interest
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The authors disclaim any financial support or relationships that may pose conflict of interest.
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References
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Carberry, C. A., Harvey, H. J., 1987. Owner satisfaction with limb amputation in dogs
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regarding postsurgical adaptation: 64 cases (2005-2012). J. Am. Vet. Med. Assoc.
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Fainsinger, R. L., de Gara, C., Perez, G. A., 2000. Amputation and preventiuon of phantom
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amputation of a hind limb. BMC Vet. Res. 12, 20.
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Hanley, M. A., Jensen, M.P., Smith, D.G., Ehde, D. M., Edwards, W. T., Robinson, L. R.,
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Hielm-Bjorkman, A. K., Rita, H., Tulamo, R. M., 2009. Psychometric testing of the Helsinki
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chronic signs of pain caused by osteoarthritis. Am. J. Vet. Res. 70, 727-734.
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Hill, A., 1999. Phantom limb pain: a review of the literature on attributes and potential mechanisms. J. Pain. Symptom. Manage. 17, 125-142.
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Jensen, T. S., Krebs, B., Nielsen, J., Rasmussen, P., 1985. Immediate and long-term phantom limb pain in amputees: incidence, clinical characteristics and relationship to pre-
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Jensen, T. S., Krebs, B., Nielsen. J., Rasmussen, P., 1983. Phantom limb, phantom pain and
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Kirpensteijn, J., van den Bos, R., Endenburg, N., 1999. Adaptation of dogs to the amputation of a limb and their owners’ satisfaction with the procedure. Vet.Rec. 144, 115-118.
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Mathews, K. A., 2008. Neuropathic pain in dogs and cats: if only they could tell us if they
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hurt. Vet. Clin. North. Am. Small. Anim. Pract. 38. 1365-1414. Meissner, W., Coluzzi, F., Fletcher, D., Huygen, F., Morlion, B., Neugebauer, E., Pérez, A. M., Pergolizzi, J., 2015. Improving the management of post-operative acute pain: priorities
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Melzack, R., 1971. Phantom limb pain: implications for treatment of pathologic pain. Anesthesiology. 35, 409-419
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Nikolajsen, L., Ilkjaer, S., Kroner, K., Christensen, J. H., Jensen, T. S., 1997. The influence
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of preamputation pain on postamputation stump and phantom pain. Pain 72, 393-405.
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Nikolajsen, L., Jensen, T. S., 2001. Phantom limb pain. Br. J. Anaesth. 87, 107-116.
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Probstner, D., Thuler, L. C., Ishikawa, N. M., Alvarenga, R. M., 2010. Phantom limb
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phenomena in cancer amputees. Pain Pract. 10, 249-256.
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Raske, M., McClaran, J.K., Mariano, A., 2015. Short-term wound complications and
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predictive variables for complication after limb amputation in dogs and cats. J. Small.
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Anim. Pract. 56, 247-252. Richardson, C., Glenn, S., Horgan, M., Nurmikko, T., 2007. A prospective study of factors
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associated with the presence of phantom limb pain six months after major lower limb
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amputation in patients with peripheral vascular disease. J. Pain. 8, 793-801.
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Small. Anim. Clin. 74, 332-334.
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Withrow, S. J., Hirsch, V. M., 1979. Owner response to amputation of a pet’s leg. Vet. Med.
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The following supporting information is available for this article:
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Table S1: Final questionnaire showing three sections with a total of 69 questions;
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Table S2: Descriptive data;
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Table S3: Supportive data on pain;
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Table S4: Supportive data on manifestations;
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Table S5: Therapies;
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Table S6: Quality of Life;
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Table S7: Information on owner’s satisfaction and perspective.
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ACCEPTED MANUSCRIPT The presence and prevalence of phantom complex in dogs was investigated
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Previously unreported signs that may be interpreted as expression of pain are discussed
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Duration of pain and time before amputation were associated with pain episodes
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S1558-7878(17)30090-4
DOI:
10.1016/j.jveb.2017.09.010
Reference:
JVEB 1085
To appear in:
Journal of Veterinary Behavior
Received Date: 6 May 2017 Revised Date:
18 August 2017
Accepted Date: 12 September 2017
Please cite this article as: Menchetti, M., Gandini, G., Gallucci, A., Della Rocca, G., Matiasek, L., Matiasek, K., Gentilini, F., Rosati, M., Approaching phantom complex after limb amputation in the canine species, Journal of Veterinary Behavior (2017), doi: 10.1016/j.jveb.2017.09.010. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Approaching phantom complex after limb amputation in the canine species
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Marika Menchetti a, *, Gualtiero Gandini a, Antonella Gallucci a, Giorgia Della Rocca b, Lara
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Matiasek c, Kaspar Matiasek d, Fabio Gentilini a and Marco Rosati d
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a
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dell’Emilia (BO), Italy
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b
Department of Veterinary Medicine, University of Perugia, 06126 Perugia (PG), Italy
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c
Neurology Referral Service, Tierklinik Haar, 85540 Haar, Germany
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d
Section of Clinical & Comparative Neuropathology, Ludwig-Maximilians-Universität,
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Munich, Germany
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Department of Veterinary Medical Sciences, University of Bologna, 40064 Ozzano
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E-mail address: [email protected] (M. Menchetti).
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* Corresponding author. Tel.: +39 0512097318
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Abstract
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The objective of this study was to describe the presence, prevalence, clinical manifestations
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and risk factors of phantom complex (PC) and its effect on the quality of life for dogs that
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underwent amputation of a limb. An online questionnaire was developed containing three
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sections with a total of 69 questions. Clinical cases were recruited from a website for three-
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legged dog owners. Data were acquired from February to March 2015. Descriptive statistics
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and frequency distribution analyses were performed on the collected data. Chi-squared test or
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Fisher’s exact test were used for assessment of the associations between categorical variables.
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One hundred and seven questionnaires were completed by owners of dogs with limb
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amputation. The most frequent reason for amputation was related to neoplasia (54%). Pain
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after limb amputation was commonly experienced by dogs and the time of onset and clinical
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manifestations of pain after limb amputation were found to resemble those of PC. The
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duration of pre-amputation pain and time between diagnosis and amputation were identified
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as risk factors for a higher frequency of post-amputation pain episodes. This pilot study
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introduces previously unreported signs that may be interpreted as expressions of pain in
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amputee dogs.
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Keywords: Dog; Pain; Phantom Complex; Neuropathic pain; Quality of life
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Introduction
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The Phantom Complex (PC) is a multifaceted syndrome that includes: 1) Phantom Limb
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Sensation (PLS), which is defined as any sensation other than pain perceived as originating
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from an absent limb; 2) Stump Pain (SP) defined as pain localized to the remaining stump
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and 3) Phantom Limb Pain (PLP), which is defined as pain perceived from the area of the
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former limb that is not physically part of the body anymore (Hill, 1999; Faisinger et al., 2000;
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Flor, 2002). PLP has been reported to occur in 60% to 80% of patients within the first 2 years
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after amputation, and in up to 10% may persist throughout life (Melzack et al., 1971;
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Nikolajsen et al., 1997; Probstner et al., 2010).
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Clinically, PLP may be confused or overlap with common post-surgical SP. However, SP
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usually subsides with healing, whereas PLP persists in 5-10% of cases and may worsen over
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time evolving into a chronic and neuropathic type of pain (Nikolajsen and Jensen, 2001).
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The amputation of a limb is a procedure commonly performed on small animals. The degree
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of adaptation, presence of risk factors associated with a poor quality of life and owner
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satisfaction have been the topic of several veterinary studies during the past years (Withrow
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and Hirsch, 1979; Carberry and Harvey, 1987; Kirpensteijn et al., 1999; Dickerson et al.,
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2015; Raske et al., 2015; Galindo-Zamora et al., 2016). However, none of those studies have
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specifically addressed the occurrence of pain and pain-related behaviors after amputation that
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could account for PC. Hence, we evaluated a client-owned population of dogs with limb
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amputation through the use of an online survey sought to document the prevalence of PC by
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identifying signs and behaviors suggestive of neuropathic pain,evaluaterisk factors associated
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with PC occurrence, and determine the owners’ perceptions of the quality of life (QoL) of
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their three-legged pets.
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Materials and Methods
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Questionnaire design and description
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A trial questionnaire was designed based on the experience of veterinary specialists,
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published questionnaires for dogs with limb amputation and/or chronic pain (Withrow and
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Hirsch 1979; Carberry and Harvey 1987; Kirpensteijn et al., 1999; Hielm-Bjorkmank et al.,
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2009), and a pediatric model for chronic pain measurement (http://www.deutsches-
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kinderschmerzzentrum.de/fileadmin/media/PDF-Dateien/englisch/parents_initial_3.0.pdf).
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A first draft of the questionnaire was independently evaluated and approved by 2 veterinary
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specialist inpalliative care, 2 board certified veterinary neurologists, 3 veterinary surgeons,
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and a three-legged pet owner whois the social media manager of a three-legged dog owner
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online community (http://tripawds.com/). Ethical approval was granted by the University of
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Bologna ethics committee (ID 664/2016).
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The questionnaire included three sections with a total of 69 questions (Supporting
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Information: Table S1). The first section consisted of 33 questions (19 closed-ended, 9 polar,
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and 5 open-ended questions) intended to collect factual data regarding the presence and
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characterization of factors related to pre-amputation pain. The second section consisted of 26
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questions (19 closed-ended and 7 polar questions) aimed at collecting data regarding pain-
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related behaviors, post-surgical complications, therapies and QoL. The last section consisted
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of 10 questions (5 closed-ended and 5 polar) that evaluated the owner’s satisfaction and the
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effects of limb amputation in the context of social life.
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Pain was characterized in terms of 1) prevalence, as pain observed by the owner before and
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after amputation; 2) onset, as the time in which the dogs started showing pain-related
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behaviours; 3) frequency, as pain recorded episodes (several times daily, weekly, monthly or
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yearly) and 4) type, as pain quality described as persistent, waxing and waning or sudden and
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“typical month” post-amputation). With “typical week” and “typical month”, the authors
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referred to a representative time frame of the ordinary pet´s life, of one week or month
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respectively, during the post-amputation phase.
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Furthermore, pain onset before amputation and time between diagnosis and amputation were
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defined as the moment in which dogs started showing signs of pain and the time elapsed
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between the diagnosis of the underlying disease and amputation.
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Recruitment of responders
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The questionnaire was administered via an online survey software and questionnaire tool
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(SurveyMonkey, Online survey services, Palo Alto, California, United States) from February
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to March 2015. The study was advertised and the enrollment of the cases was announced on
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the website and corresponding social media profile of a three-legged dog owner community
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called “Tripawds” (http://tripawds.com), the members of which were invited to participate in
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the survey.
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The inclusion criteria for participation consisted of being a current or former owner of a dog
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that had undergone either complete or partial surgical amputation of one limb at least three
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months prior, regardless of the reason for amputation. Based on previous studies in humans
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this three-month timeframe was considered to be a sufficient period of time to discriminate
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between the development of post-surgical pain only and/or the occurrence of PC in a non-
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verbalizing patient.
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Skip logic was employed in the design of the questionnaire, thereby allowing participants to
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skip some questions and be redirected to a subsequent set of queries based on preceding
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answers, and it was not mandatory to answer all questions within a section prior to
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proceeding to the next section. To be included on data analysis at least 80% of the questions
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had to be answered by each participant. Therefore, we decided to report the results as
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percentages with number of respondents in brackets with percentages calculated on the
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number of respondents per question.
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Statistical analysis
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Data analysis was performed using a statistical analysis software (PAST 3.x The past of the
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future, Hammer & Harper, Natural History Museum, University of Oslo, Norway), while
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calculations were performed and graphs were constructed using an electronic spreadsheet
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(Microsoft Excel, Microsoft Corporation, Microsoft Redmond campus, Redmond,
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Washington, United States). The distribution of continuous variables was checked using the
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Shapiro-Wilk test and normal probability plotting. Categorical or ordinal data are described
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as percentages of the total respondents to each individual question. The associations between
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categorical variables were assessed using the chi-squared test or Fisher’s exact test depending
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on whether the value in one or more of the cells of the contingency table was five or less. P
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values ≤ 0.05 were considered significant.
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Results
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Descriptive data
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One hundred and seven completed questionnaires were available for data analysis; of these
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questionnaires, 56% (60/107) referred to 32 breeds of purebred dogs, with golden retrievers
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(17%; 10/60) and Labrador retrievers (15%; 9/60) being most highly represented. Mixed
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breed dogs accounted for 44% (47/107) of the population. Among the dogs, the mean age at
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the time of the survey was 7.6 years (median 8 years, range 0.6-16 years). With respect to sex
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were female (66% spayed; 31/107). At the time of amputation, 39% of the dogs (42/107)
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were 6 to 10 years old, 31% (33/107) were 1 to 5 years old, 21% (22/107) were 1-year-old or
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less and 9% (10/107) were 11 to 15 years old. At the time of the study, 79% (85/107) of the
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dogs were still alive. The majority of the dogs were large-size, with dogs over 25 kg
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accounting for 60% (64/107) of the subjects, while medium size dogs (10-25 kg) accounted
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for 28% (30/104) and small size dogs (<10 kg) for 12% (13/104) of the canine amputees.
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The main reason for amputation was neoplasia (54%; 58/107), followed by trauma (40%;
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43/107), limb malformation (3%; 3/107), and infection (3%; 3/107). In 75% (80/107) of dogs,
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the entire limb was amputated, while the remaining 25% (27/107) underwent partial
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amputation. Of the 107 dogs, 61% (65/107) underwent thoracic and 39% (42/107) underwent
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pelvic limb amputation (Supporting Information: Table S2).
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Pain before and after amputation
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According to the owners’ perspective, pain was reported in 82% of dogs before surgery
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(75/91) and in 85% of dogs after amputation (78/92), regardless the time of surgery, with no
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significant difference (P = 0.6).
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Regarding the onset of pain before amputation, 53% (36/68) reported that dogs experienced
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pain more than one month before surgery (69% of oncologic patients), while the remaining
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47% (32/68) described pain from 24 h to 4 weeks before amputation (Supporting
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Information: Table S3).
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Onset of pain before surgery was not associated with the development of postsurgical pain (P
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= 0.09). However, the time of pain onset before amputation was significantly associated with
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the frequency of post-amputation pain, with a significantly higher frequency of pain episodes
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(P < 0.01).
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After the amputation, 79% of owners (51/64) felt their dogs experiencing pain only in the
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post-surgical recovery period (from 24 hours to 4 weeks after amputation). However, 9%
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(6/64) described pain between 1 to 3 month after surgery and 5% (3/64) experiencing pain
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between 3 to 6 months after surgery. Furthermore, 7% (4/64) described pain episodes in
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different occasions from the immediately post-surgical to 6 months after amputation
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(Supporting Information: Table S3).
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Regarding the frequency of pre- and post-amputation pain episodes, no differences were
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observed (P = 0.4) and dogs experienced mostly daily episodes of pain before (57%; 38/67)
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and after surgery (57%; 36/63) (Supporting Information: Table S3).
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The type of pain was significantly different in the pre- and post-surgical periods (P < 0.01), as
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owners described pain experienced by their pets 7 days prior to amputation mostly as
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“waxing and waning” in 45% of dogs (29/65) and “persistent” in 40% (26/65), whereas in a
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typical month after amputation they referred to it as “sudden and transient” in 53% (20/38)
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with none experiencing persistent pain (Supporting Information: Table S3).
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The etiological diagnosis was made between 24 hours to 4 weeks in the majority of dogs
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(73%; 69/95) and more than 1 month before the surgery in only 27% (26/95). However, no
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association was observed between length of time from diagnosis to amputation and the
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prevalence of pain after amputation (P = 0.6).
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Complications after surgery occurred in 20% (19/95) of the cases, mostly identified during
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the first week after surgery (95%; 17/18). More frequent complications (owners could choose
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more than one answer) were infections (7/17), surgical wound swelling (6/17) and suture
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failure (6/17). Furthermore, 6/17 owners identified “pain” as post-surgical complication. No
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significant difference in terms of the prevalence of pain after amputation was identified
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between dogs with and without post-surgical complications.
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Manifestations related to the PC
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Between the first 3-6 months post-amputation, owners described reduced activity levels
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(67%; 55/82) and overall playfulness (46%; 38/82), a negative emotional state (44%; 35/80),
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decreased participation in family life (31%; 25/81), appetite loss (30%; 25/82), and reduced
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sleep (21%; 17/80).
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Interactions between the dogs and other animals were also impaired in terms of decreased
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friendliness with family pets (14%; 11/79) and unfamiliar pets (19%; 22/80).
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Focusing on the presence of possible PC-related behaviors, dogs exhibited different
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manifestations of pain or discomfort (Supporting Information: Table S4). In particular,
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among dogs showing those manifestations in the timeframe comprised from 3 months to more
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than 1 year after amputation, 35% exhibited muscular twitching in the stump region (23/66),
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23% licked the stump (10/43), 19% whimpered (10/52), 17% yelped (6/35), 16% were
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restless (10/61), 11% chewed the stump (1/9) and 8% scratched the stump (1/13) (Supporting
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Information: Table S4).
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Furthermore, behavioral changes in terms of aggression and withdrawal from interactions
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with humans and animals were described both before and after the surgery. In particular, in
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the pre-amputation phase, owners described episodes of aggression towards humans (10%;
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8/83 ) and animals (18%; 15/83) and the tendency to prevent contacts with humans (16%;
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13/83) and animals (17%; 14/81). The same changes in behaviour were reported in the post-
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amputation phase regarding aggression towards humans and animals (8%; 6/79 and 17%;
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13/78 respectively) and prevention of human and animal contacts (14%; 11/79 and 21%;
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17/82 respectively), without significant differences between the two phases (P > 0.1).
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onset of pain in 78% of dogs that experienced pain after amputation (46/59). Accessory
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symptoms that could possibly account for pain during the post amputation period were
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reported in 26% of the dogs (22/84). In particular, owners described tiredness (16/22),
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tachypnea (15/22) and irritability (7/22). Moreover, in 18% (4/22) these symptoms appeared
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at least 3 months after amputation (Supporting Information: Table S4).
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Therapies
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Of the dogs, 79% (76/96) received medical treatment before the amputation. The most
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frequently administered treatments were pain killers (65/96) and anti-inflammatory drugs
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(48/96) (Supporting Information: Table S5). In 46% of the dogs (26/56) these treatments
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were administered for more than 1 month prior to surgery. Medical treatments before
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amputation were not statistically associated with the occurrence of pain during the post-
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amputation period (P = 0.3).
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After amputation, treatments were administered to all dogs (91/91) for which information
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was available. As before amputation, the most frequently administered treatments were pain
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killers (85/91), followed by antibiotics (63/91) (Supporting Information: Table S5).
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When specifically asked about administered drugs because of pain after amputation, the most
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frequently reported medications were pain killers (55/85), followed by anti-inflammatory
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drugs (47/85), while specific treatments for neuropathic pain, such as gabapentin, were
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administered in 22/85 of dogs (Supporting Information: Table S5).
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Quality of Life
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The degree of adaptation after amputation was described from “good” to “very good” in 94%
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of dogs (89/95) and 72% (67/93) were able to ambulate within the first week after
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probability of experiencing pain during a “typical month” (P = 0.02) and adapted more
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quickly (P = 0.005). Regarding the degree of mobility during a “typical week” after the
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amputation, owners reported some movement restrictions, as difficulties in jumping (28%;
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24/87) and moving after a major activity (24%; 21/86) (Supporting Information: Table S6).
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Owners’ satisfaction and perspective
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After the amputation, 59% of owners (46/78) reported an improvement in the quality of their
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relationship with their pets and in 75% of cases (62/83) the overall response of the family to
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the amputation was considered to be “very positive”. However, during the first month
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following amputation, 62% of owners (50/81) felt that their pet caused conflicts in their work
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or daily activities, 52% (42/80) expressed a feeling of limited independence, and 46% (37/81)
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that their social life was limited. Nevertheless, 89% of the interviewees (70/79) did not regret
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the decision to have their pet undergone amputation, and 92% of the owners (71/77) felt that
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they had been well informed by their veterinarian during the decision-making process
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(Supporting Information: Table S7).
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Discussion
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The present investigation represents a preliminary step approaching phantom complex in
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dogs after amputation of a limb. According to our survey, 14% of owners felt their dogs
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experiencing pain between 1 to 6 months after surgery with and without accompanying
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behavioral changes. Likewise in human amputees, 5-10% of patients report persistence and
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worsening of pain beyond the stage of post-surgical healing, leading to the development of a
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Jensen, 2001; Meissner et al., 2015). Taken together these findings suggest that the
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establishment of neuropathic pain in the residual limb may be delayed for months after
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surgical resection and that post-operative care might/should go well beyond wound healing.
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The type of pain showed a transformation in its pattern changing from a “waxing and
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waning” and “persistent” before amputation to “sudden and transient” after. Such an
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evolution might be explained by a first sensitization phase, because of the inciting disease,
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followed by abnormal circuit re-arrangement in a manner prone to eliciting bursts of
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abnormal sensory neuronal firing (Dworkin et al., 2003). This observation may support the
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hypothesis that this pain is either neuropathic in origin or it has a neuropathic component.
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Investigating neuropathic pain and PC (comprising PLP) in animals represents a clinical
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challenge. Veterinary patients cannot verbalize and some dogs can also have very high pain
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threshold showing any sign of discomfort. Therefore, the information regarding abnormal
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painful sensations together with their quality and intensity can easily be missed despite
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careful monitoring (Mathews, 2008). Accordingly, we focused on manifestations potentially
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related to discomfort localized on the stump considering a minimum of three months after the
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amputation. Interestingly, up to one third of the dogs showed some of those manifestations
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from 3 months to 1 year after amputation, suggesting again a possible late onset of
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neuropathic pain.
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No difference was observed in the frequency of pain before and after surgery. Dogs
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exhibiting signs of pain several times a day prior to amputation were more likely to present a
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similar frequency of pain after surgery. However, the “frequency of pain episodes” questions
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did not further specify a timeframe in the post amputation phase, hence variations through
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time might have gone undetected.
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ACCEPTED MANUSCRIPT Previous studies of human patients have suggested that having a duration of pre-amputation
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pain that is longer than 1 month may serve as a risk factor for development of chronic PLP
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(Jensen et al., 1985; Nikolajsen et al., 1997; Hanley et al., 2007). Accordingly, dogs
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experiencing pain for more than 1 month before amputation were significantly more likely to
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develop daily episodes of pain after amputation.
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Several studies have attempted to evaluate the relation between the administration of
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treatment and PLP in human amputees and the majority has shown that pain control before
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amputation does not prevent the development of PLP (Flor, 2002; Richardson et al., 2007).
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Likewise, we did not identify any relationship between the administration of treatment before
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amputation and the incidence of post-amputation pain. Stress during the post amputation
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phase seems to play a role in the development of pain. A possible relation between stress and
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the onset of pain was reported in 78% of patients. This is in accordance with human studies in
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which psychological stress represents a risk factor for PLP occurrence (Richardson et al.,
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2007).
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As previously described (Raske et al., 2015), post-surgical complications occurred in 20% of
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dogs and the most commonly reported was infection. No relations were found between the
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occurrence of pain after amputation and post-operative complications. Similarly to other
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investigations (Kirpensteijn et al., 1999; Dickerson et al., 2015; Galindo-Zamora et al., 2016),
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94% of the evaluated dogs adapted very well to amputation, regardless of which limb
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(thoracic or pelvic) was amputated or at which level (complete or partial) the amputation
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occurred. Interestingly, the better and quicker the recovery of dogs, the lower the incidence of
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post-amputation pain. This association may suggest that a shorter recovery time might be
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directly related to either reduced/absent pain perception during the post-surgical period
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and/or the effectiveness of proper pain control.
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ACCEPTED MANUSCRIPT In our survey owners reported behavioral changes both before and after amputation. Similar
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changes have been previously described in canine amputation patients, with modifications
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including aggression and anxiety (Kirpensteijn et al., 1999). However, as was reported by
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Kirpensteijn (1999), it was not possible to determine the reason for these changes in behavior.
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This common finding could reflect the presence of pain could be the consequence of a
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physical limitation or could be not related to the amputation at all.
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The vast majority of interviewees did not regret their decision regarding amputation. Within
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the first month post-surgery, owners reported limited independence and conflicts with
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everyday activities. However, these limitations proved to be transient and the pet’s overall
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QoL was perceived as satisfactory, as previously described (Withrow and Hirsch, 1979;
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Carberry and Harvey, 1987; Kirpensteijn et al., 1999; Dickerson et al., 2015; Galindo-
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Zamora et al., 2016). These findings might, therefore, be seen as indications of positive
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outcomes following amputation and support amputation during a decision making process
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that is emotionally intense for the owners.
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This study is the first attempt to describe PC in dogs, so there are several limitations. Medical
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records were not available for review and information on the clinical history was taken as
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provided by the owner. An owner’s perception of their dog’s pain manifestations is inherently
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subjective, involving alevel of empathy of the observers, and may have influenced the results
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of the questionnaire. We used a non-validated survey but given the explorative nature of the
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investigation and owners were not asked to measure a specific phenomenon, we still consider
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this as a valid approach. In order to increase the objectiveness of this survey we tailored
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questions and their phrasing using a pediatric model for chronic pain measurement in which
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parents are asked to evaluate pain in children, as it may get closer to this situation between
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observer and subject observed. Furthermore, there are no validated and objective pain scales
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and surveys for amputee dogs and/or neuropathic pain in this species.
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Conclusions
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Our pilot study introduces previously unreported signs and behaviors that may be interpreted
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as expressions of pain in amputee dogs. These manifestations may be particularly revealing
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for those dogs that experienced post-amputation pain initiating at least one month after
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surgery. The ability to recognize behavioral signs that may indicate the presence of
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unpleasant sensations related to neuropathic pain would be of great interest, in order to
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prevent and treat it.
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Ethical statement
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The work has been reviewed in accordance with the standards recommended by the Guide for
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the Care and Use of Laboratory Animals and Directive 2010/63/EU and approved by the
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“Ethics Committee” of the Department of Veterinary Medical Sciences of the University of
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Bologna (record number 664/2016).
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Authorship
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The idea for the article was conceived by M. Rosati and G. Della Rocca. The experiments
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were designed by M. Rosati, M. Menchetti and A. Gallucci. The experiments were performed
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by M. Menchetti and M. Rosati. The data were analyzed by M. Menchetti and F. Gentilini.
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The article was written by M. Menchetti, M. Rosati, G. Gandini, A, Gallucci, L. Matiasek, K.
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Matiasek.
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Conflict of interest
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The authors disclaim any financial support or relationships that may pose conflict of interest.
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ACCEPTED MANUSCRIPT Supporting Information
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The following supporting information is available for this article:
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Table S1: Final questionnaire showing three sections with a total of 69 questions;
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Table S2: Descriptive data;
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Table S3: Supportive data on pain;
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Table S4: Supportive data on manifestations;
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Table S5: Therapies;
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Table S6: Quality of Life;
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Table S7: Information on owner’s satisfaction and perspective.
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ACCEPTED MANUSCRIPT The presence and prevalence of phantom complex in dogs was investigated
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Previously unreported signs that may be interpreted as expression of pain are discussed
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Duration of pain and time before amputation were associated with pain episodes
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