Ultrasonography of Osteosarcoma in Dogs
Sonography Atlas of Dogs

Abstract

On each gait analysis session, patients were gently introduced to the gait on the treadmill; on the first day, a speed at which each individual patient walked comfortably on the treadmill was determined; on each subsequent session the patient was evaluated using the same speed, ranging from 0.5 to 0.8 m/s. During each gait analysis session, two to six trials were recorded, each with a duration of approximately 30 s, until at least one valid trial was obtained. A valid trial was defined as 10 consecutive regular steps, in which the dog walked smoothly, without any external forces from the handler being applied, with all paws landing on the appropriate force plate, without overstepping. Video recording was performed, to ensure that the steps were appropriate for analysis.

Both kinetic and kinematic data were simultaneously recorded using commercially available software.¹⁶

Ten consecutive steps were afterwards analyzed for the following kinetic parameters: peak vertical force (PFz), mean vertical force (MFz), and vertical impulse (integral [IFz]). All forces were normalized to the individual body weight of each dog and data were expressed as percentage of body weight (%BW). Mean ± standard deviation (SD) was calculated from 10 valid consecutive steps. Afterwards, load redistribution (LR) was calculated for each forelimb and remaining hind limb, for each measured parameter (PFz, MFz, IFz), using the following equation (according to Steiss et al. [12]): % load bearing = Fz of the limb/total Fz of all limbs*100. Other kinetic parameters were not calculated to avoid overloading this section with too much information. The kinetic data were processed using commercial software¹⁷ and exported to a commercially available spreadsheet.¹⁸

In order to process the kinematic data in Vicon Nexus, all markers were labeled in a trial. Then, 10 valid foot strikes were marked manually to define the gait cycle (stance and swing phases) of each limb. Using a 2-dimensional (2-D) model, projected flexion and extension angles of each remaining joint were calculated: contralateral (with respect to the amputated hind limb) scapulohumeral joint, contralateral cubital joint, contralateral carpal joint, ipsilateral (with respect to the amputated hind limb) scapulohumeral joint, ipsilateral cubital joint, ipsilateral carpal joint, contralateral coxofemoral joint, contralateral femorotibial joint and contralateral tarsal joint. Measured angles are illustrated in Fig. 1. In order to compare the movement pattern of each analyzed joint, the gait cycles were normalized to 100 in all dogs and displayed as percentage of one whole stride. The mean joint angle (±SD) and the range of motion (±SD) of the aforementioned joints were calculated from the mean joint angle progression curves (MJAPC) calculated from the 10 strides per dog. Mean joint angles and range of motion were used since the reader can easily understand their comparison between sessions and to avoid overloading the manuscript with too much data. The kinematic data were processed using commercial software¹⁹ and then exported to a commercially available spreadsheet¹⁸.

Patient 12 presented bilateral hip osteoarthritis; however, it was asymptomatic, and no signs of pain, lameness or difficulty to stand up were detected before or after the amputation. All other patients showed no abnormalities in the physical examination of the remaining limbs. No patient showed abnormalities on the physical examination of the spine throughout the study.

Kinetic and kinematic gait evaluation

The results of the kinetic and kinematic evaluations are presented in Figs. 2, ,3,3, ,44 and and55 and Tables 3 and and4.4. It should be noted that, although nine patients survived until the last examination day, the kinetic and kinematic data were not available from all of them. One animal (Patient 7) refused to walk on the treadmill and others (e.g. Patient 4) walked intermittently in such a way that some trials were not valid for analysis; even though these animals could walk and run perfectly fine on solid ground, they were afraid of walking on the treadmill, apparently due to the movement of the belts. Moreover, although all owners were extremely cooperative, when some of them had the impression that their dog was afraid or tired, they were reluctant to allow their pets to be walked on the treadmill long enough to record valid trials. The number of patients evaluated on each session is also indicated in Tables 3 and 4.

Figure 2: Load redistribution (LR) averages for the a peak (PFz); b mean (MFz); and c integral (IFz) forces. The values in the bars indicate the mean % body weight (BW) loaded by each limb for each calculated parameter

Figure 3: Mean joint angle progression curves of the contralateral (with respect to the amputated hind limb) scapulohumeral joint, cubital joint and carpal joint. Note the similarity of the curves before and after amputation

Figure 4: Mean joint angle progression curves of the ipsilateral (with respect to the amputated hind limb) scapulohumeral joint, cubital joint and carpal joint. Note the similarity of the curves before and after amputation

Figure 5: Mean joint angle progression curves of the contralateral (with respect to the amputated hind limb) coxofemoral joint, femorotibial joint and tarsal joint. Note the similarity of the curves before and after amputation

Table 3: Results of the kinematic analysis. Mean: mean joint angle calculated from the mean joint angle progression curves; SD: Standard deviation; ROM = Range of Motion; p = p value of the Kruskal-Wallis test

Table 4: Owner assessment of patient comfort^a (first part). ^aModified from Hielm-Björkman et al. [13]

Kinetic data showed that 10 days after amputation there was redistribution of the load to all remaining limbs (Fig. 2 and Table 2). The values and pattern of load shifting are represented in Fig. 2. The recorded PFz, MFz and IFz values showed no remarkable changes during the remaining examination time points, indicating that 10 days after the amputation the patient had already reached its new locomotory pattern. This was true for all patients including the lightest (8 kg) and the heaviest (54 kg) ones. There were no statistically-significant differences between sessions (Table 2).

Table 2: Results of the kinetic analysis. p: p value of the Kruskal-Wallis test; PFz: Peak vertical force; MFz: Mean vertical force; IFz: vertical impulse (integral); SD: Standard deviation

With regard to the kinematic gait analysis, even though the patients walked smoothly on the treadmill (Additional file 1: Video 1), there were significant differences between sessions in the means of almost all joint angles (Table 3). It is important to note that there were also marked variations within a patient in the same session (not shown in Table 3). The MJAPC showed a similar pattern between sessions (Figs. 3, ,4 and and5),, but these showed marked individual variations (not shown).

Despite all these different kinematic results, ROMs of all analyzed joints were very similar before and after amputation and remained constant in the subsequent sessions after the amputation, without significant differences between sessions (Table 3).

MR evaluation of the contralateral stifle joint

Postoperative MR examination was possible in eight patients. Although nine patients survived until the end of the study, severe metastatic disease was detected in patient 11 on day 120, and the MR examination was not performed. Postmortem MR examination was not possible in any case, as the owners were very sensitive about their pet’s death, and they elected to dispose the patients’ dead bodies themselves. No changes in the signal intensity of the CrCL, CdCL or the lateral and medial menisci were found, in comparison with the preoperative MR images. No changes in the cartilage surface and no evidence of osteoarthritic changes were found (Fig. 6).

Figure 6: Example of the magnetic resonance examination of the stifle in one patient before (a) and 120 days after the amputation (b). No changes could be detected in the joint 120 days after the procedure

Owner evaluation of patient comfort

The results of the owners’ assessment of patient comfort are presented in Table 4 and show a clear tendency of the patients to improve after amputation. Patient movement after amputation is exemplified with Additional file 2: Video 2. Ten owners answered the final questionnaire (Table 5). This questionnaire revealed a high degree of owner satisfaction with the amputation result.

Table 5: Final owner questionnaire^a (n = 10). ^aAdapted from Carberry and Harvey [4], Withrow and Hirsch [5], von Werthern et al. [6] and Kirpensteijn et al. [7]

Discussion

The main goal of this study was to provide owners and veterinarians with accurate, objective information, not existing previously, about the outcome of the amputated patient (i.e. how the dog adapted to the new locomotory status).

Examination times were chosen using the data of a previous study [7] which indicated that most dogs adapted to the amputation within a month, some within a week, and all within 3 months after surgery. With the last follow-up 120 days after the procedure, a final attempt was made to find any evidence of further gait changes. Since there is the belief that orthopedic disease might occur in the remaining limb after amputation, as a result of a theoretical overload, the contralateral stifle was morphologically assessed using MR images, to evaluate this likelihood. The femorotibial (stifle) joint was chosen, instead of the coxofemoral or tarsal joint, as the former has been extensively investigated, and there is a whole body of literature exemplifying normal and pathologic MR images to compare [14–19].

As expected, a very heterogeneous population was found in this study: different breeds, ages and weights. The main reason for amputating a patient was the presence of a tumor, which agrees with previous studies [6, 7]. The mortality seen in this study was not related the amputation itself.

The kinetic and kinematic analyses revealed that the patients had begun adapting to the new locomotory situation even before the amputation was performed, and that 10 days after the procedure, all major changes had already taken place. It was unfortunate that it was not possible to perform all examinations on all patients. However, exclusively using “good” trials allowed us to obtain reliable results. It should be noted that, even though a valid trial implied that the handler did not exert any external forces, it was not possible to have the animals completely free on the treadmill (see Additional file 1: Video 1). Unfortunately, the willingness to walk or trot or overall activity of the patient were not evaluated in the present study; these factors would have brought additional information about the outcome. It is remarkable that the largest patient (patient 11–54 kg) and the smallest one (patient 10 – 8 kg) adapted equally well. These results agree with the study of Kirpensteijn et al. [7], indicating that, even though subjective, the observations made by the owners of such study were actually very precise. The present study has the advantage of looking at the patients objectively and prospectively, leaving no doubt about the fast adaptation of all animals. The fact that there were no significant changes in the load redistribution after amputation was initially surprising; however, it is easily explainable: all patients were severely lame before the amputation, meaning that the adaptation and compensation to the lack of a hind limb had begun to take place before the amputation was performed. This was even clearer when looking only at those patients which did not load the affected limb at all before surgery. It should also be kept in mind, that the lack of statistically significant changes could have resulted from the low number of dogs included in this study, and therefore in the lack of power of the tests.

The kinematic results (including the statistical analysis) should be interpreted with caution. The fact that significant differences were found in the absolute values of the different joint angles could be explained by the normal variation inherent to motion analysis: marker localization changes lead to changes in joint angles measured. Even though every effort was made to place the markers in the right position, small variations might have occurred, leading to different measurements. However, also huge variations were seen within a session (not shown in Table 3 or Figs. 3, ,44 and and5),5), possibly indicating that the patients adapted to every step they made and in a very irregular manner. Affected balance of the dog during movement and the resulting instability might cause these variations. Another possible explanation is the fact that several gait patterns are possible at a given speed and by a permanent adjustment of the speed of the animal to the treadmill speed [20]. It should also be taken into account that slow speeds were used before the amputation, in order to avoid worsening the pain that patients were already experiencing. After the amputation the animals could have walked on the treadmill more comfortably at faster speeds (personal observations). Even though this might have caused an irregular walking pattern after the procedure, speeds were kept constant to avoid adding a variance factor when measuring the GRF [21]. Finally, the angles measured here can be used to illustrate the movement patterns for the patients in this study, and they cannot be extrapolated to other patient populations. However, our study focuses on determining whether there are variations in the different kinematic parameters before and after amputation in this particular patient population, and that does not seem to be the case.

The similarity in the ROMs before and after surgery is a remarkable finding. The measurement of ROMs seems to be less susceptible to the sources of error commonly found in kinematic studies (misplacement of markers and skin movement), at least in the hind limb [22]. Therefore, the results of the ROMs are more accurate than the absolute measurement of joint angles. That being said, the lack of significant differences between sessions suggests that the patient had also begun to adapt to the new movement situation before amputation, and that this remained stable after the procedure. However, it should also be taken into consideration that joint angular curves in each measurement points are very similar in shape, resulting in stable ROMs; this could also explain why the ROMs showed much less variation than mean joint angles.

The lack of changes in the MR examination of the remaining contralateral stifle after amputation could indicate that an overload in the remaining contralateral hind limb, leading to joint pathology, is not very likely. It was decided to investigate this point, as it is commonly believed by the general public, and even by some veterinarians, that amputating a dog might predispose it to orthopedic abnormalities; the results of our MR (and also our physical examinations) proved otherwise, at least for the stifle. Although 4 months after amputation might possibly be a short time to evaluate joint changes, a previous study describing the experimentally induced rupture of the CrCL in 5 crossbred dogs showed that it is possible to see changes in the cartilage and subchondral bone as early as 4 weeks after the rupture [17]. It is of course difficult to extrapolate such findings to this study, but it could indicate that, if there were ongoing changes in joint morphology, they would be visible 4 months after amputation. Besides, most of our research subjects were oncologic patients, with a (likely) short life span. Measuring cartilage thickness would have been a more accurate method to evaluate subtle joint changes [17]. Unfortunately, this could not be done due to software limitations. In any case, we did not expect to see any changes, as our clinical experience indicates that no changes are seen in the contralateral limb after a hindlimb amputation; nevertheless, it is not known what kind of changes an amputation would cause in patients suffering from degenerative joint disease in the remaining limbs.

With regard to the owner evaluation assessment of the patient after the procedure, the results were as expected: in Table 4, the positive outcome of most patients can be clearly seen. The improvement is especially remarkable in the ability of the dog to lie down and stand up. The lack of improvement or worsening of some parameters for some patients seemed to be related more to the declining general condition of the patient, than to the effects of the amputation itself. The use of an objective tool to measure patient activity, such as an accelerometer, could have provided more accurate information about the outcome and they have been previously used in animals [23]; however, this tool was not available to us.

The responses to the final questionnaire were also as expected: most owners were initially reluctant to have their dogs amputated, but were satisfied with the overall result and the quality of life was considered good; this is in agreement with other studies [4–7]. In the present study, some owners even considered that their pet’s quality of life improved after the amputation, and this might have been related to the removal of the source of pain. The behavioral changes reported by the owners in this study were more small disabilities than behavioral problems. The behavioral problems previously reported [7], such as aggression and anxiety, were not seen in the patients of the present study.

As in previous studies [4, 7], all owners responded that they would have another pet amputated, and none regretted the decision. We believe that an evaluation made by owners whose pets died shortly after the procedure would have been negatively biased and they were not gathered.

The favorable responses of most owners can be explained by the fact that the dogs adapted very soon to their new locomotory situation (kinetic and kinematic analyses) and to the lack of morphologic changes in other joints (as it might be inferred from the lack of morphologic changes in the stifle).

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