Owner assessment of chronic pain intensity and results of gait analysis of dogs with hip dysplasia treated with acupuncture

Lívia R. Teixeira Department of Anesthesiology, Faculty of Medicine, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Stelio P. L. Luna Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Lídia M. Matsubara Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Maria L. B. Cápua Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Bianca P. C. R. Santos Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Luciane R. Mesquita Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Luis G. Faria Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Felipe S. Agostinho Department of Veterinary Surgery and Anesthesiology, Faculty of Veterinary Medicine and Animal Science, UNESP (Universidade Estadual Paulista), Botucatu, SP 18618970, Brazil.

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Anna Hielm-Björkman Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, 00014 Helsinki, Finland.

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Abstract

OBJECTIVE To evaluate pain intensity and kinetic variables in dogs with hip dysplasia (HD) treated with acupuncture, carprofen, or a placebo.

DESIGN Randomized, controlled clinical study.

ANIMALS 54 HD-affected dogs and 16 healthy dogs.

PROCEDURES Seven HD-affected dogs were removed from the study. Dogs with HD were treated in a blinded manner for 30 days with acupuncture (once weekly for 5 sessions; n = 15), carprofen (4.4 mg/kg [2.0 mg/lb], PO, q 24 h; n = 16), or placebo capsules containing lactose (1 mg/kg [0.45 mg/lb], PO, q 24 h; n = 16). Dogs were evaluated 2 weeks and immediately before (baseline) and 2, 4, and 6 weeks after the onset of treatment. Owners evaluated the dogs' pain intensity with 2 validated questionnaires and a visual analogue scale (VAS) for pain and evaluated degree of lameness with a VAS for locomotion. Kinetics of the hind limbs were also evaluated. Sixteen HD-free dogs were used to assess the evaluation protocol.

RESULTS Owners' assessments revealed that outcomes of the 3 treatments did not differ significantly. The Canine Brief Pain Inventory and VAS pain intensity assessments were decreased from baseline at weeks 4 and 6, respectively, but only in acupuncture-treated dogs. The locomotion VAS values were decreased at week 4 in acupuncture-treated and carprofen-treated dogs. Kinetic evaluation findings did not differ among the groups or over time.

CONCLUSIONS AND CLINICAL RELEVANCE Neither acupuncture nor carprofen was significantly different from placebo. Acupuncture and carprofen reduced the degree of subjectively evaluated lameness, and acupuncture was associated with a decrease in validated chronic pain scores.

Abstract

OBJECTIVE To evaluate pain intensity and kinetic variables in dogs with hip dysplasia (HD) treated with acupuncture, carprofen, or a placebo.

DESIGN Randomized, controlled clinical study.

ANIMALS 54 HD-affected dogs and 16 healthy dogs.

PROCEDURES Seven HD-affected dogs were removed from the study. Dogs with HD were treated in a blinded manner for 30 days with acupuncture (once weekly for 5 sessions; n = 15), carprofen (4.4 mg/kg [2.0 mg/lb], PO, q 24 h; n = 16), or placebo capsules containing lactose (1 mg/kg [0.45 mg/lb], PO, q 24 h; n = 16). Dogs were evaluated 2 weeks and immediately before (baseline) and 2, 4, and 6 weeks after the onset of treatment. Owners evaluated the dogs' pain intensity with 2 validated questionnaires and a visual analogue scale (VAS) for pain and evaluated degree of lameness with a VAS for locomotion. Kinetics of the hind limbs were also evaluated. Sixteen HD-free dogs were used to assess the evaluation protocol.

RESULTS Owners' assessments revealed that outcomes of the 3 treatments did not differ significantly. The Canine Brief Pain Inventory and VAS pain intensity assessments were decreased from baseline at weeks 4 and 6, respectively, but only in acupuncture-treated dogs. The locomotion VAS values were decreased at week 4 in acupuncture-treated and carprofen-treated dogs. Kinetic evaluation findings did not differ among the groups or over time.

CONCLUSIONS AND CLINICAL RELEVANCE Neither acupuncture nor carprofen was significantly different from placebo. Acupuncture and carprofen reduced the degree of subjectively evaluated lameness, and acupuncture was associated with a decrease in validated chronic pain scores.

Hip dysplasia is an abnormal development of the hip joint. The cause of HD is multifactorial. Its progression is individual and difficult to predict, and it often leads to osteoarthritis, which causes signs of pain and crepitus in joints, decreased mobility, and reluctance to exercise. The treatments for HD are conservative therapeutic management when the pain intensity is mild or moderate or surgical interventions when the pain cannot be adequately controlled.1 In the United Kingdom, osteoarthritis is one of the main causes of signs of chronic pain in dogs, and despite the availability of various forms of treatment, there is still a gap in knowledge regarding their safety and efficacy.2 Validated tools such as kinetic evaluations3–5 and owner-completed questionnaires on chronic pain3,6–8 can be used to evaluate the efficacy of these treatments in dogs with HD.

Conservative treatment options include administration of NSAIDs such as carprofen.9–13 However, this drug has adverse effects, particularly in the gastrointestinal tract,14,15 which can preclude extended administration of the treatment.10 In a systematic review16 of 35 research projects and 29 clinical trials in dogs, treatment with NSAIDs caused adverse effects in 35 of the 64 (55%) studies. Considering the limitations of conventional treatments for HD in dogs, it is important to search for new alternatives.7,17

Acupuncture is a nonpharmacological treatment option17 for numerous conditions, including osteoarthritis in humans.18 The contribution of acupuncture to pain control includes muscle relaxation, restoration of blood flow, decrease in joint compression, and improvement in oxygen and nutrient distribution to the affected site, all of which slow disease progression. Additionally, acupuncture reduces local signs of pain and tissue inflammation.19 There are few high-quality veterinary medicine studies that have evaluated the effects of acupuncture in small animals.17 Results of 2 studies20,21 have indicated that gold implanted at acupuncture points significantly reduces pain in dogs with osteoarthritis, but similar results were not obtained in a third study.22 In rats with osteoarthritis, acupuncture reduces the expression of metalloproteinases 1 and 3 and increases expression of tissue inhibitors of metalloproteinase 1 in cartilage, suggesting that the technique also has a chondroprotective effect.23 In humans, both dry-needle acupuncture and electroacupuncture considerably improve pain-related symptoms of osteoarthritis.24 However, the effects of dry-needle acupuncture on reducing the severity of signs of pain and improving lameness of dogs with HD has not yet been evaluated, to our knowledge. The purpose of the study reported here was to evaluate pain intensity and kinetic variables in dogs with HD treated with acupuncture, carprofen, or a placebo. The hypothesis was that both acupuncture and carprofen would reduce signs of pain and lameness and consequently improve symmetry indices derived from kinetic evaluation of the hind limbs of HD-affected dogs.

Materials and Methods

The study was approved by the university's ethics committee on animal use (protocol number 87/2013). The owners were informed of the study and signed a consent form. The sample size was calculated on the basis of data from a previous study,6 where a sample size of 16 dogs/group for a test power of 80% (SD = 40%; P ≤ 0.05) was used to detect differences in assessed variables of at least 30% between groups.

Dogs cared for at the institution's veterinary hospital were considered for inclusion in the study if they had radiographic evidence of unilateral or bilateral HD, signs of pain according to assessments by their owners, and at least 2 clinical signs of the disease (eg, lameness; difficulty lying down, standing up, or going up or down stairs; or reluctance to jump or difficulty jumping). Exclusion criteria included treatment with analgesic or chondroprotective drugs during the preceding 4 weeks or previous hip joint surgery.

All variables evaluated in the study were also assessed once in a group of HD-free dogs (n = 16), which were selected from kennels or belonged to clients interested in HD-free certification for their dog. These dogs did not have any history of signs of pain or any radiographic abnormalities of the hip, stifle, and elbow joints and were used as an HD-free (presumed pain-free) group to assess the experimental protocol and obtain results for a similarly sized group of pain-free dogs with no HD. By inclusion of this group, the intent was to verify that the evaluation tools used under the study conditions were able to distinguish HD-affected dogs from HD-free dogs and therefore also distinguish lame dogs or dogs with signs of pain from pain-free dogs.

Radiographic evaluation

To perform the radiographic examination, HD-affected and HD-free dogs were sedated with morphine sulfatea (0.5 mg/kg [0.23 mg/lb], IM), and anesthesia was induced with propofolb (5 mg/kg [2.27 mg/lb], IV). All dogs underwent radiographic examination (ventrodorsal and lateral imaging) of the hip, stifle, and elbow joints and cervical, thoracic, lumbar, and sacral portions of the vertebral column. A radiologist evaluated the radiographic views for each dog to confirm the presence or absence of HD, determine the degree of HD according to the Orthopedic Foundation for Animals classification scheme,25 and exclude the presence of concomitant orthopedic disease that could influence the evaluations.

Experimental procedures

Fifty-four HD-affected dogs were randomly allocated by use of computer softwarec into 1 of 3 groups that were to be treated with acupuncture (n = 17), carprofend (20), or placebo (17). Acupuncture-treated dogs underwent once-weekly sessions of acupuncture, with a total of 5 sessions within a period of 30 days, without the presence of the owner. For these dogs, acupuncture needles (0.25 × 30 mm) were inserted bilaterally at acupoints KI 3, BL 11, BL 18, BL 23, BL 40, BL 54, LIV 3, GB 29, GB 30, and GB 34 and at the single points GV 2 and Bai hui.26 The acupoints were selected on the basis of their functional effects in traditional Eastern medicine. This type of acupuncture uses only acupuncture needles to stimulate the points and is often referred to as dry-needle acupuncture. Dogs in this group were treated by 2 specialized veterinary acupuncturists (MLBC and BPCRS).

Carprofen-treated dogs received 4.4 mg of carprofen/kg (2.0 mg/lb) orally once daily; this group was a positive control group. Placebo-treated dogs received capsules containing lactose (1 mg/kg [0.45 mg/lb]), which were identical in appearance to the capsules containing carprofen, orally once daily; this group was a negative control group. The day of the first acupuncture session or capsule administration was designated as week 0. To maintain the owners' unawareness of the treatment given to their dog, acupuncture-treated dogs also received capsules containing lactose orally once daily and carprofen- and placebo-treated dogs were brought to the acupuncture clinic once each week for a total of 5 occasions within a period of 30 days. The carprofen- and placebo-treated dogs were handled without the presence of the owner, as if they were receiving acupuncture but no needles were inserted. All of the oral treatments were administered for 30 days. The only individuals involved in the study who were aware of the treatment allocations were the 2 specialized veterinary acupuncturists. They did not participate in the subsequent evaluations.

For ethical reasons, all of the owners were instructed to report deterioration of clinical signs or episodes of signs of pain in their dog. In such instances, the dogs were provided with rescue analgesia (oral administration of 4 mg of tramadol hydrochloride/kg [1.8 mg/lb], q 8 h); this rescue analgesia was given to the dog for as long as the owner considered it necessary. The owners were requested to report if the rescue medication had been used. Data from dogs requiring rescue analgesia were maintained in statistical analyses.

For the HD-affected dogs, 2 pretreatment evaluations were performed at 14 days (week −2) and immediately before the first treatment (week 0 [baseline]) to evaluate whether there would be any significant improvement in the variables of interest in the dogs before the beginning of the study. Treatment-effect evaluations were performed at weeks 2, 4, and 6 after the commencement of treatment. Because all treatments were given within a period of 30 days, the dogs had not received acupuncture, carprofen, or placebo for 2 weeks at the week 6 time point; thus, this final time point served as a short-term follow-up visit at which persistence of possible improvements after the end of the treatment was assessed. The HD-free dogs were evaluated only once at week 0.

At each evaluation, each dog was evaluated by the owner and underwent a kinetic evaluation. Each owner evaluation involved 3 assessment instruments: the CBPI, including total scores and those corresponding to pain severity and pain interference6; the HCPI8; and VASs regarding pain27 and locomotion.7 On the basis of the criterion adopted to consider the relevant differences among the groups and calculate the test's power, improvements for a given dog were considered significant when the scores of the CBPI decreased by 30%.

Lameness was evaluated by kinetic analysis to obtain PVF values and symmetry indices for the PVF and VI values of the hind limbs. A pressure platform system,e which consisted of a series of 4 plates (in total, 1.95 m in length, and 447 mm in width) was used. The system was calibrated according to the manufacturer's specifications. The dogs walked on the platform at constant speed (0.9 to 1.1 m/s). Each dog walked on the platform in the same direction multiple times, starting at 1 end and circling around to walk along the platform again. These rounds of walking were recorded to create a database in a computer with the equipment's software.28,f The dogs walked on the platform repeatedly until 5 valid walks were obtained; a valid walk was when all 4 limbs touched the platform's surface at least 2 times and the dog walked without sudden head movements and without being pulled by the study assistant. To obtain the symmetry indices for the hind limbs, each variable was expressed as a percentage of the difference in values between the 2 hind limbs relative to the mean of the values for the 2 limbs for that same variable.29

The data were subjected to the Shapiro-Wilk normality test. For parametric data, a 1-way ANOVA was performed followed by a Tukey test for between-group comparisons and a repeated-measures ANOVA was performed for within-group comparisons. For the parametric data, the values are reported as the mean and SD. The data that did not follow a normal distribution were subjected to a Kruskal-Wallis test for comparison among groups followed by a Dunn test. A Friedman test was used for within-group comparisons, and a Dunn test was performed to compare the medians. A Pearson test was used to determine correlations between data acquired by use of the assessment instruments and kinetic variables. A χ2 test was used to analyze both the degree of HD and a 30% improvement of the CBPI scores. A significance level of 5% was used in all of the tests. Software30,g was used for the statistical analyses.

Results

Dogs

Of the 54 dogs with HD that commenced the study, 7 were removed before the end of the study. These 7 dogs (2 females and 5 males) included 1 Labrador Retriever, 1 Pitbull, 2 Rottweilers, and 3 mixed breeds; mean ± age was 7.6 ± 3.7 years and mean weight was 30.7 ± 8.7 kg (67.5 ± 19.1 lb). Two dogs (1 from the acupuncture treatment group and 1 from the carprofen treatment group) were removed because the owner administered additional medication without the researchers' consent, 2 dogs (both from the carprofen treatment group) were removed because the owners did not administer all treatments as scheduled, 2 dogs (1 from the acupuncture treatment group and 1 from the carprofen treatment group) were removed because of development of neurologic signs, and 1 dog (originally allocated to the placebo treatment group) was removed because contact with the owner was lost. The data for the dogs that were removed from the study were not included in the statistical analyses. Consequently, analyses included data obtained from 15 acupuncture-treated dogs, 16 carprofen-treated dogs, and 16 placebo-treated dogs. Breed, weight, age, and sex of the remaining 47 dogs and the 16 HD-free dogs were summarized (Table 1). There was no difference in body weight among the groups. The healthy dogs were younger (P = 0.001) than the affected dogs.

Table 1—

Characteristics (breed, mean weight, mean age, and sex) of HD-affected dogs that were evaluated for signs of pain before, during, and after treatment with acupuncture, carprofen, or placebo and HD-free dogs that did not receive any treatment.

 Group
 Acupuncture-treated dogs (n = 15)Carprofen-treated dogs (n = 16)Placebo-treated dogs (n = 16)HD-free dogs (n = 16)
Breed (No. of dogs)Boxer (1)Border Collie (1)Belgian Shepherd (1)Bernese (1)
German Shepherd Dog (3)Belgian Shepherd (1)German Shepherd Dog (6)Border Collie (2) 
Golden Retriever (1)German Shepherd Dog (5)Golden Retriever (1)English Pointer (3) 
Labrador Retriever (3)Great Dane (1)Mixed (5)German Shepherd Dog (1) 
Mixed (5)Kuvacz (1)Poodle (1)Golden Retriever (2) 
Rottweiler (2)Labrador Retriever (1)Rottweiler (2)Labrador Retriever (3) 
 Mixed (3) Maremma Sheepdog (2) 
 Pitbull (2) Mixed (1) 
 Setter (1) Rottweiler (1) 
Mean ± SD weight (kg)34.9 ± 8.235.7 ± 9.030.7 ± 8.329.2 ± 8.6
Mean ± SD age (y)7.2 ± 3.17.8 ± 3.76.6 ± 4.72.9 ± 1.9*
SexFemale (10) Male (5)Female (9) Male (7)Female (9) Male (7)Female (8) Male (8)

Initially, 54 dogs with HD were assigned to 1 of the 3 treatment groups; data from 7 dogs were not used in the analyses (4 dogs from the carprofen-treated group, 2 dogs from the acupuncture-treated group, and 1 dog from the placebo-treated group).

Value for HD-free dogs differs significantly (P = 0.001) from the value for each group of HD-affected dogs.

The degree of HD in the 47 affected dogs included in the study ranged from borderline to severe according to the Orthopedic Foundation for Animals classification (Table 2). There was no significant difference in degree of HD among the 3 groups of HD-affected dogs. The hip joint status of all dogs in the HD-free group was excellent or good according to the Orthopedic Foundation for Animals classification.

Table 2—

Classification of the degree of HD as determined by use of the Orthopedic Foundation for Animals guidelines and HD status (unilateral or bilateral HD) among the dogs in Table 1 that were subsequently treated with acupuncture, carprofen, or placebo.

 Group
VariableAcupuncture-treated dogs (n = 15)Carprofen-treated dogs (n = 16)Placebo-treated dogs (n = 16)P value*
Degree of HD (No. of dogs)
   Fair or borderline2130.461
   Mild3230.973
   Moderate1620.237
   Severe9780.631
HD status (No. of dogs)
   Unilaterally affected
      Right side110NA
      Left side203NA
   Bilaterally affected121513NA

Percentages of dogs in each category were compared across groups; a value of P < 0.05 was considered significant. NA = Not applicable.

Regarding adverse effects, 1 carprofen-treated dog consumed less than normal amounts of food and another carprofen-treated dog vomited (this dog was removed from the study because of incomplete treatment). In both cases, these clinical signs were reported 2 weeks after the beginning of treatment (at week 2) and dogs were treated with omeprazole (1 mg/kg, PO, q 24 h) from week 2 to week 4, accomplishing 2 weeks of treatment. According to the owners, only 2 carprofen-treated dogs required rescue analgesia; treatment with tramadol hydrochloride (4 mg/kg, PO, q 8 h) was given to 1 dog for 6 days between weeks 2 and 4 and to another for 10 days between weeks 0 and 2.

Owner assessments

At baseline (week 0), scores obtained from the HCPI questionnaire, the total score and scores for pain severity and pain interference obtained from the CBPI questionnaire, and the VAS findings for pain and locomotion were significantly (P < 0.001) lower for the HD-free group, compared with data for the other groups (Figures 13). For the HD-affected dogs, there was no difference in the HCPI, CBPI, and VAS data among the 3 treatments at any time point.

Figure 1—
Figure 1—

Mean scores derived by use of the HCPI questionnaire completed by owners of HD-affected dogs 2 weeks before (week −2), immediately before (week 0), and at 2, 4, and 6 weeks after initiation of treatment with acupuncture (diamonds), carprofen (squares), or placebo (triangles) and by owners of HD-free dogs (cross) at week 0 only. Fifty-four HD-affected dogs were initially allocated to receive once-weekly sessions of acupuncture (5 sessions within a 30-day period), 4.4 mg of carprofen/kg orally once daily (2.0 mg of carprofen/lb; positive control group), or placebo capsules containing lactose (1 mg/kg [0.45 mg/lb]) orally once daily (negative control group). Acupuncture-treated dogs also received capsules containing lactose orally once daily and carprofen- and placebo-treated dogs were brought to the acupuncture clinic once each week for a total of 5 occasions within a period of 30 days. All of the oral treatments were administered for 30 days. Data from only 15 acupuncture-treated dogs, 16 carprofen-treated dogs, and 16 placebo-treated dogs were available for analysis. The HD-free dogs (n = 16), were selected from kennels or belonged to clients interested in HD-free certification for their dog. At each time point, each owner evaluation involved 3 assessment instruments: the HCPI; the CBPI, including total scores and those corresponding to pain severity and pain interference; and VASs regarding pain and locomotion. *At this time point, the value for each group of HD-affected dogs differed significantly (P < 0.001) from the value for the HD-free dogs.

Citation: Journal of the American Veterinary Medical Association 249, 9; 10.2460/javma.249.9.1031

Figure 2—
Figure 2—

Median scores for pain severity (A), pain interference (B), and total pain scores (C) derived by use of the CBPI questionnaire completed by owners of the HD-affected and HD-free dogs in Figure 1. For the HD-affected dogs, assessments were made 2 weeks before (week −2), immediately before (week 0), and at 2, 4, and 6 weeks after initiation of treatment with acupuncture (diamonds), carprofen (squares), or placebo (triangles). The HD-free dogs (cross) were assessed only once (week 0). †At this time point, the value for the acupuncture-treated dogs differed significantly from the week −2 or week 0 value or both values. See Figure 1 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 249, 9; 10.2460/javma.249.9.1031

Figure 3—
Figure 3—

Median scores derived by use of a VAS for pain completed by owners of the HD-affected and HD-free dogs in Figure 1. For the HD-affected dogs, assessments were made 2 weeks before (week −2), immediately before (week 0), and at 2, 4, and 6 weeks after initiation of treatment with acupuncture (diamonds), carprofen (squares), or placebo (triangles). The HD-free dogs (cross) were assessed only once (week 0). See Figure 1 and 2 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 249, 9; 10.2460/javma.249.9.1031

Compared with the scores obtained at week −2 and at week 0, the pain severity (P = 0.002) and pain interference (P < 0.001) scores derived from the CBPI questionnaire decreased at weeks 4 and 6, whereas the total score decreased (P < 0.001) only at week 4 in the acupuncture-treated dogs. Improvement of at least 30% from baseline in the CBPI scores was evident in 13 of the 15 acupuncture-treated dogs, 11 of the 16 carprofen-treated dogs, and 7 of the 16 placebo-treated dogs. Improvement of the CBPI scores was significantly (P = 0.034) greater in the acupuncture-treated dogs, compared with findings for the placebo-treated dogs. There was no difference in improvement between the carprofen- and placebo-treated dogs (P = 0.285) or between the acupuncture- and carprofen-treated dogs (P = 0.446).

The VAS for pain revealed that only owners of the acupuncture-treated dogs perceived a reduction (P = 0.008) in their dog's pain intensity at week 6, compared with findings at week −2 (Figure 3). The VAS score for locomotion was lower at week 4 in the acupuncture-treated (P = 0.002) and carprofen-treated (P = 0.024) dogs and at week 6 in the acupuncture-treated dogs (P = 0.002), when compared with the week 0 score. Considering all owner-completed assessment instruments, there were no significant differences between week −2 and week 0.

Gait analysis

In the kinetic evaluations, the PVF values did not differ among the HD-affected dogs and the HD-free dogs at week 0. There was no difference in PVF among the treatments or within treatments at any time interval. The symmetry index for hind limb PVF or VI did not differ among the HD-affected dogs and the HD-free dogs at week 0. There was no difference among or within treatments at any time interval for the symmetry index for hind limb PVF or VI.

Correlation between HCPI, CBPI, and gait analysis data

There was no correlation between the scores obtained from the HCPI questionnaire and the symmetry index for PVF or VI of the hind limbs. Similarly, the total score or pain interference score obtained from the CBPI questionnaire was not correlated with the symmetry index for PVF or VI. The score obtained from the HCPI questionnaire was strongly correlated with the total score (P < 0.001; r = 0.669) and the pain interference score (P < 0.001; r = 0.675) obtained from the CBPI questionnaire.

Discussion

On the basis of the CBPI questionnaire data provided by owners, the comparison of the effects of acupuncture, carprofen, or placebo on pain intensity and lameness in dogs with HD in the present study revealed that only acupuncture alleviated signs of pain at week 4 (ie, after 1 month of treatment), compared with findings before the start of treatment. This improvement also persisted for 2 weeks after cessation of treatment, as indicated by the CBPI data and the VAS score for pain at week 6. Regarding the score for the owner-evaluated VAS for locomotion, lameness was improved at week 4 in both the acupuncture- and carprofen-treated dogs; however, of these 2 treatments, acupuncture had a more long-lasting effect and improvement in lameness was maintained for at least 2 more weeks, as assessed at the follow-up visit at week 6.

Data from dogs that received rescue analgesia were not removed from the analyses in the present study to reduce type 2 error; however, had those data been removed, differences between the carprofen-and acupuncture-treated dogs might have been even more evident because only dogs treated with carprofen received rescue analgesia.

The successful identification of pain events in dogs by use of the 3 assessment instruments used in the present study has been previously reported.3,6–8 When used by the owners of the dogs in the present study, these 3 assessment instruments enabled identification of the expected pain events in the HD-affected dogs. Although data from HCPI and CBPI questionnaires have previously identified positive effects of NSAIDs (ie, by reductions in these pain scores for both thoracic and pelvic limbs) administered to dogs with chronic signs of pain caused by osteoarthritis,3,8,31 the NSAIDs appear to have a smaller effect on lameness, compared with their effect on pain, specifically lameness associated with hip joint diseases. This finding was observed in a previous study32 and has been reinforced by the results of the present study. In contrast, the reduction in the CBPI, VAS for pain, and VAS for locomotion scores over time in the acupuncture-treated dogs appeared to be related to the effect of acupuncture on relieving chronic pain, an effect that persisted 2 weeks after the completion of the acupuncture treatment. To our knowledge, the use of dry needles to alleviate signs of pain and lameness in dogs with HD has not been evaluated. However, results of a study33 in humans indicated that the improvement of the evaluated knee osteoarthritis index persisted for some weeks after cessation of the acupuncture treatment. In a study21 in dogs with HD, gold wire implants placed at acupuncture points around the hip joints improved locomotion and reduced signs of pain, but there was no difference between the treated and the once-needled control groups. In other studies,20,34 gold beads provided pain relief for 2 years after implantation in dogs with HD or hip joint arthritis, and this effect was not observed in dogs treated with a placebo.

The apparent superior analgesic effect of acupuncture observed in the present study could possibly be related to the fact that acupuncture reduces both acute35 and chronic signs of pain.36 The mechanisms related to acupuncture-induced analgesia involve increases in plasma β-endorphin concentration,37 which inhibit presynaptic transmission of pain impulses. Other inhibitory neurotransmitters, such as serotonin,38 are also involved in the pain-alleviating effects of acupuncture. Acupuncture also activates the bulbospinal neurons, resulting in noradrenaline release and activation of α2-adrenoceptors of the dorsal horn of the medulla.39 Given its anti-inflammatory effects and ability to activate immune mechanisms, alleviate physical and emotional stress, accelerate the tissue healing process, and alleviate pain by releasing endorphins and serotonin, acupuncture has an important role in rehabilitating humans with pain.40 In addition to its analgesic effects, acupuncture also facilitates blood clotting41 and acts in the downregulation of metalloproteinase expression, suggesting that it also has a chondroprotective effect.23

In the kinetic evaluation in the present study, variations in the data most likely prevented identification of differences in PVF values between the HD-affected and HD-free dogs, unlike what had been observed in a previous study.42 To minimize this variation, a symmetry index was calculated. The PVF and VI are important variables for identifying lameness43; however, even following analysis of the symmetry indices for each of these variables, there was no significant difference in PVF or VI between the 2 groups. Thus, under the conditions of the study reported here, the kinetic evaluation was not sufficiently effective to identify the dogs with lameness from the HD-free dogs or indicate improvements after treatments. In a previous study,32 kinetic evaluation also did not show an effect of treatments with carprofen or placebo in dogs with osteoarthritis of the hip joint.

The absence of kinetic differences among the treatments in the present study may be related to there being a more pronounced inflammatory process associated with lameness resulting from HD, compared with that associated with lameness resulting from cruciate ligament rupture, for example.44 Moreau et al12 found that NSAID administration was associated with better results in the kinetic analysis of dogs with osteoarthritis of the stifle joint relative to those for dogs with osteoarthritis of the hip joint. This finding may explain why studies that evaluated dogs with osteoarthritis in joints other than the hip joint have usually been able to detect significant improvement with treatment, whereas investigations such as the present study, which specifically evaluated hip joints, did not detect such improvements.12,32,44 Although kinetic evaluations are considered the gold standard in evaluating lameness in dogs with osteoarthritis, it is also known that HD causes complex alterations in gait. These often complicate kinetic evaluations of HD-affected dogs,45 as illustrated by the results of the present study in which no differences in kinetic variables were observed between the HD-affected and HD-free dogs.

Although both the questionnaires for evaluating chronic pain and the kinetic evaluations used in the present study can be useful tools in identifying the efficacy of osteoarthritis treatments, the discrepancy between the CBPI scores and the findings of the kinetic analyses arises because these tools evaluate different aspects of chronic pain. Questionnaires quantify the impact of treatment on a dog's routine activities, whereas kinetic evaluations specifically evaluate lameness.3 Despite the correlation between the HCPI scores and CBPI scores and the similar patterns of scoring over time for the 2 questionnaires, no differences in the HCPI scores for the HD-affected dogs were detected among treatments. This was most likely because of the separation of questions in the CBPI questionnaire into 2 components, which makes identifying the impact of pain on a dog's quality of life easier.

Similar to the CBPI scores, no correlations were observed between the HCPI scores and the findings of the kinetic analysis. In previous studies,3,46 no data obtained with the instruments used to evaluate pain correlated well with data obtained from kinetic evaluations, which was similar to the situation in the present study. In the veterinary medical literature, the only questionnaire that provides data that correlate with findings of kinetic evaluations is the Liverpool Osteoarthritis in Dogs questionnaire,46 which was published after the beginning of the present study.

The study of this report had some limitations, including a heterogeneous sample of dogs. Although there was no difference in age or weight among the 3 groups of HD-affected dogs, there was considerable variation in these variables as well as in body conformation. An analysis of the vertical forces is indicative of limb function, although it is influenced by many factors, such as body weight, conformation, and animal size47 and speed during evaluation,29,48 that latter being the only variable that can be controlled. These limitations were minimized by standardizing the vertical force data with body weight47; however, size of the dogs still generated differences in relative speed.48

Another limitation inherent to any clinical experiment is the variation in the degree of HD among the treatment groups, despite a lack of detectable significant differences. The degree of disease severity hindered some of the dogs from being evaluated while trotting on the gait analyzer because certain dogs could not maintain the trotting speed. Although both walking and trotting are acceptable for evaluating vertical forces,49 the latter is more sensitive and has been shown to have a higher accuracy for evaluation of lameness in dogs.29

In the present study, the kinetic analyses did not differentiate dogs with and without HD and did not therefore differentiate the effects of the treatments. Although improvement was undetectable by means of the kinetic evaluation, the CBPI questionnaire and VAS for pain used to identify signs of pain in this study are well established, and the CBPI is used to assess pain in dogs with osteoarthritis.3,7 By use of these instruments, owners are able to evaluate their dog in its own environment over time.50 Such evaluations are often used in research because they do not require the same amount of time, technical expertise, and equipment as do evaluations performed with gait analyzers, which are typically available only at large research centers. Nevertheless, the fact that, except for the kinetic analysis data, scores were lower for HD-free dogs than for HD-affected dogs demonstrates the ability of the present study assessments to differentiate dogs without HD from dogs with HD.

Although the decreases in scores for the placebo-treated dogs in the present study were not significant, a caregiver placebo effect should always be considered when interpreting owner reports.51 Caregivers may subconsciously believe their dogs improved, thereby lowering their estimates of pain. However, the differences in the percentage of acupuncture- and place-botreated dogs that had a 30% decrease in the CBPI scores indicated that acupuncture was more effective in improving pain scores than was the placebo.

On the basis of the subjective evaluations performed in the present study, acupuncture and carprofen both decreased lameness in dogs with HD, but only acupuncture alleviated HD-related pain. Therefore, acupuncture performed with the protocol and acupoints used in this study appears to be a viable option for improving the quality of life of dogs with HD.

Acknowledgments

This article is part of a thesis submitted to the Graduate Program in Anesthesiology, Faculty of Medicine, UNESP (Universidade Estadual Paulista), Botucatu, Brazil, as a partial requirement for obtaining a doctorate degree.

Supported in part by a research scholarship from CAPES awarded to Dr. Teixeira and by FAPESP (2010/0897-0).

The authors thank Dr. Sheila Canevese Rahal for technical assistance and Agener União for providing the carprofen.

ABBREVIATIONS

CBPI

Canine Brief Pain Inventory

HCPI

Helsinki Chronic Pain Index

HD

Hip dysplasia

PVF

Peak vertical force

VAS

Visual analogue scale

VI

Vertical impulse

Footnotes

a.

Dimorf, Cristália, Itapira, Brazil.

b.

Propovan, Cristália, Itapira, Brazil.

c.

Research Randomizer, version 4.0, Geoffrey C. Urbaniak and Scott Plous, Middletown, Conn. Available at: www.randomizer.org. Accessed Jun 7, 2012.

d.

Carproflan, Agener União/União Química Farmacêutica Nacional, Embu Guaçu, Brazil.

e.

WalkwayTM High Resolution HRV4, Teckscan Onc, South Boston, Mass.

f.

Walkway, version 7.0, Tekscan Inc, South Boston, Mass.

g.

SigmaStat, version 3.1, Systat Software Inc, Point Richmond, Calif.

References

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    • Crossref
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    • Export Citation
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    • Export Citation
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    • Crossref
    • Search Google Scholar
    • Export Citation
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    • Crossref
    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • 28. Tekscan. Walkway user manual, version 7.0 edition. Boston: Tekscan Inc, 1998;243.

  • 29. Voss K, Imhof J, Kaestner S, et al. Force plate gait analysis at the walk and trot in dogs with low-grade hindlimb lameness. Vet Comp Orthopaed 2007; 20: 299304.

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    • Export Citation
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    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Malek S, Sample SJ, Schwartz Z, et al. Effect of analgesic therapy on clinical outcome measures in a randomized controlled trial using client-owned dogs with hip osteoarthritis. BMC Vet Res 2012; 8: 185201.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Berman BM, Singh BB, Lao L, et al. A randomized trial of acupuncture as an adjunctive therapy in osteoarthritis of the knee. Rheumatology 1999; 38: 346354.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Jæger G, Larsen S, Søli N, et al. Two years follow-up study of the pain-relieving effect of gold bead implantation in dogs with hipjoint arthritis. Acta Veterinaria Scandinavica 2007; 49: 17.

    • Search Google Scholar
    • Export Citation
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    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Joaquim JG, Luna SP, Brondani JT, et al. Comparison of decompressive surgery, electroacupuncture, and decompressive surgery followed by electroacupuncture for the treatment of dogs with intervertebral disk disease with longstanding severe neurologic deficits. J Am Vet Med Assoc 2010; 236: 12251229.

    • Crossref
    • Search Google Scholar
    • Export Citation
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  • Figure 1—

    Mean scores derived by use of the HCPI questionnaire completed by owners of HD-affected dogs 2 weeks before (week −2), immediately before (week 0), and at 2, 4, and 6 weeks after initiation of treatment with acupuncture (diamonds), carprofen (squares), or placebo (triangles) and by owners of HD-free dogs (cross) at week 0 only. Fifty-four HD-affected dogs were initially allocated to receive once-weekly sessions of acupuncture (5 sessions within a 30-day period), 4.4 mg of carprofen/kg orally once daily (2.0 mg of carprofen/lb; positive control group), or placebo capsules containing lactose (1 mg/kg [0.45 mg/lb]) orally once daily (negative control group). Acupuncture-treated dogs also received capsules containing lactose orally once daily and carprofen- and placebo-treated dogs were brought to the acupuncture clinic once each week for a total of 5 occasions within a period of 30 days. All of the oral treatments were administered for 30 days. Data from only 15 acupuncture-treated dogs, 16 carprofen-treated dogs, and 16 placebo-treated dogs were available for analysis. The HD-free dogs (n = 16), were selected from kennels or belonged to clients interested in HD-free certification for their dog. At each time point, each owner evaluation involved 3 assessment instruments: the HCPI; the CBPI, including total scores and those corresponding to pain severity and pain interference; and VASs regarding pain and locomotion. *At this time point, the value for each group of HD-affected dogs differed significantly (P < 0.001) from the value for the HD-free dogs.

  • Figure 2—

    Median scores for pain severity (A), pain interference (B), and total pain scores (C) derived by use of the CBPI questionnaire completed by owners of the HD-affected and HD-free dogs in Figure 1. For the HD-affected dogs, assessments were made 2 weeks before (week −2), immediately before (week 0), and at 2, 4, and 6 weeks after initiation of treatment with acupuncture (diamonds), carprofen (squares), or placebo (triangles). The HD-free dogs (cross) were assessed only once (week 0). †At this time point, the value for the acupuncture-treated dogs differed significantly from the week −2 or week 0 value or both values. See Figure 1 for remainder of key.

  • Figure 3—

    Median scores derived by use of a VAS for pain completed by owners of the HD-affected and HD-free dogs in Figure 1. For the HD-affected dogs, assessments were made 2 weeks before (week −2), immediately before (week 0), and at 2, 4, and 6 weeks after initiation of treatment with acupuncture (diamonds), carprofen (squares), or placebo (triangles). The HD-free dogs (cross) were assessed only once (week 0). See Figure 1 and 2 for remainder of key.

  • 1. Davidson JR, Kerwin S. Common orthopedic conditions and their physical rehabilitation. In: Millis DL, Levine D, eds. Canine rehabilitation and physical therapy. 2nd ed. Philadelphia: Elsevier, 2014;543–581.

    • Search Google Scholar
    • Export Citation
  • 2. Bell A, Helm J, Reid J. Veterinarians’ attitudes to chronic pain in dogs. Vet Rec 2014; 175: 428434.

  • 3. Brown DC, Boston RC, Farrar JT. Comparison of force plate gait analysis and owner assessment of pain using the Canine Brief Pain Inventory in dogs with osteoarthritis. J Vet Intern Med 2013; 27: 2230.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Lopez MJ, Quinn MM, Markel MD. Evaluation of gait kinetics in puppies with coxofemoral joint laxity. Am J Vet Res 2006; 67: 236241.

  • 5. Poy NS, DeCamp CE, Bennett RL, et al. Additional kinematic variables to describe differences in the trot between clinically normal dogs and dogs with hip dysplasia. Am J Vet Res 2000; 61: 974978.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Brown DC, Boston RC, Coyne JC, et al. Development and psychometric testing of an instrument designed to measure chronic pain in dogs with osteoarthritis. Am J Vet Res 2007; 68: 631637.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Hielm-Björkman AK, Kuusela E, Liman A, et al. Evaluation of methods for assessment of pain associated with chronic osteoarthritis in dogs. J Am Vet Med Assoc 2003; 222: 15521558.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Hielm-Björkman AK, Rita H, Tulamo R-M. Psychometric testing of the Helsinki Chronic Pain Index by completion of a questionnaire in Finnish by owners of dogs with chronic signs of pain caused by osteoarthritis. Am J Vet Res 2009; 70: 727734.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Edamura K, King JN, Seewald W, et al. Comparison of oral robenacoxib and carprofen for the treatment of osteoarthritis in dogs: a randomized clinical trial. J Vet Med Sci 2012; 74: 11211131.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Mansa S, Palmer E, Grondahl C, et al. Long-term treatment with carprofen of 805 dogs with osteoarthritis. Vet Rec 2007; 160: 427430.

  • 11. Johnston SA, McLaughlin RM, Budsberg SC. Nonsurgical management of osteoarthritis in dogs. Vet Clin North Am Small Anim Pract 2008; 38: 14491470.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Moreau M, Dupuis J, Bonneau NH, et al. Clinical evaluation of a nutraceutical, carprofen and meloxicam for the treatment of dogs with osteoarthritis. Vet Rec 2003; 152: 323329.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Liesegang A, Limacher S, Sobek A. The effect of carprofen on selected markers of bone metabolism in dogs with chronic osteoarthritis. Schweiz Arch Tierheilkd 2007; 149: 353362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Luna SP, Basílio AC, Steagall PV, et al. Evaluation of adverse effects of long-term oral administration of carprofen, etodolac, flunixin meglumine, ketoprofen, and meloxicam in dogs. Am J Vet Res 2007; 68: 258264.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Reymond N, Speranza C, Gruet P, et al. Robenacoxib vs. carprofen for the treatment of canine osteoarthritis; a randomized, noninferiority clinical trial. J Vet Pharmacol Ther 2012; 35: 175183.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Monteiro-Steagall BP, Steagall PVM, Lascelles BDX. Systematic review of nonsteroidal anti-inflammatory drug-induced adverse effects in dogs. J Vet Intern Med 2013; 27: 10111019.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Corti L. Nonpharmaceutical approaches to pain management. Top Companion Anim M 2014; 29: 2428.

  • 18. White A, Foell J. Acupuncture is superior to sham for painful conditions. Evid Based Med 2013; 18:e56.

  • 19. Ma Y-t, Ma M, Cho ZH. Peripheral mechanisms of acupuncture. In: Ma Y-t, Ma M, Cho ZH, eds. Biomedical acupunture for pain management: an integrative appoach. St Louis: Elsevier, 2005;3148.

    • Search Google Scholar
    • Export Citation
  • 20. Jaeger GT, Larsen S, Soli N, et al. Double-blind, placebo-controlled trial of the pain-relieving effects of the implantation of gold beads into dogs with hip dysplasia. Vet Rec 2006; 158: 722726.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Hielm-Björkman A, Raekallio M, Kuusela E, et al. Double-blind evaluation of implants of gold wire at acupuncture points in the dog as a treatment for osteoarthritis induced by hip dysplasia. Vet Rec 2001; 149: 452456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Bolliger C, DeCamp CE, Stajich M, et al. Gait analysis of dogs with hip dysplasia treated with gold bead implantation acupuncture. Vet Comp Orthopaed 2002; 15: 116122.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Bao F, Sun H, Wu ZH, et al. Effect of acupuncture on expression of matrix metalloproteinase and tissue inhibitor in cartilage of rats with knee osteoarthritis. Zhongguo Zhen Jiu 2011; 31: 241246.

    • Search Google Scholar
    • Export Citation
  • 24. Tukmachi E, Jubb R, Dempsey E, et al. The effect of acupuncture on the symptoms of knee osteoarthritis—an open randomised controlled study. Acupunct Med 2004; 22: 1422.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Orthopedic Foundation for Animals. An examination of hip grading. Available at: www.ofa.org/hd_grades.html. Accessed Mar 6, 2012.

  • 26. Chrisman C, Xie H. Canine transpositional acupoints. In: Xie H, Preast V, eds. Xie's veterinary acupuncture. Ames, Iowa: Blackwell Publishing, 2007;129216.

    • Search Google Scholar
    • Export Citation
  • 27. Holton LL, Scott EM, Nolan AM, et al. Comparison of three methods used for assessment of pain in dogs. J Am Vet Med Assoc 1998; 212: 6166.

    • Search Google Scholar
    • Export Citation
  • 28. Tekscan. Walkway user manual, version 7.0 edition. Boston: Tekscan Inc, 1998;243.

  • 29. Voss K, Imhof J, Kaestner S, et al. Force plate gait analysis at the walk and trot in dogs with low-grade hindlimb lameness. Vet Comp Orthopaed 2007; 20: 299304.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Systate Software I. SigmaStat 3.1: user's manual. San Jose, Calif: Systat Software, Inc, 2004.

  • 31. Brown DC, Boston RC, Coyne JC, et al. Ability of the Canine Brief Pain Inventory to detect response to treatment in dogs with osteoarthritis. J Am Vet Med Assoc 2008; 233: 12781283.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Malek S, Sample SJ, Schwartz Z, et al. Effect of analgesic therapy on clinical outcome measures in a randomized controlled trial using client-owned dogs with hip osteoarthritis. BMC Vet Res 2012; 8: 185201.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Berman BM, Singh BB, Lao L, et al. A randomized trial of acupuncture as an adjunctive therapy in osteoarthritis of the knee. Rheumatology 1999; 38: 346354.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Jæger G, Larsen S, Søli N, et al. Two years follow-up study of the pain-relieving effect of gold bead implantation in dogs with hipjoint arthritis. Acta Veterinaria Scandinavica 2007; 49: 17.

    • Search Google Scholar
    • Export Citation
  • 35. Cassu RN, Luna SP, Clark RM, et al. Electroacupuncture analgesia in dogs: is there a difference between uni- and bi-lateral stimulation? Vet Anaesth Analg 2008; 35: 5261.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Joaquim JG, Luna SP, Brondani JT, et al. Comparison of decompressive surgery, electroacupuncture, and decompressive surgery followed by electroacupuncture for the treatment of dogs with intervertebral disk disease with longstanding severe neurologic deficits. J Am Vet Med Assoc 2010; 236: 12251229.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Ahsin S, Saleem S, Bhatti AM, et al. Clinical and endocrinological changes after electro-acupuncture treatment in patients with osteoarthritis of the knee. Pain 2009; 147: 6066.

    • Crossref
    • Search Google Scholar
    • Export Citation
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