Osteosarcoma (OSA) is the most common primary bone tumor in dogs and typically affects middle-age-to-older large- and giant-breed dogs.1 It most commonly arises from the metaphyseal area of appendicular long bones, and the distal radius is most often affected.1 The current standard of care for the management of appendicular OSA is local control and systemic cytotoxic chemotherapy. Arguably, amputation of the affected limb is the most effective means to achieve local control. Patients not amenable to limb amputation due to severe neurological or orthopedic disease, or where amputation is declined by the owners, are considered for alternative local therapies, such as radiation therapy or surgical limb-sparing procedures.
Limb-spare surgery has historically been associated with a very high complication rate, in the 50% to 96% range.2–6 Stereotactic radiation has gained popularity over the last decade, with several studies7–13 demonstrating comparable overall survival to limb amputation, and a risk of pathological fracture, in the 5% to 63% range, which has decreased with improved case selection and technology.11,14–18 Limb-spare surgery for the management of distal radial OSA or other tumor types in dogs has often involved marginal resection of the tumor and reconstruction of the bone column with a plate, filling the defect with a metal endoprosthesis2,4 or cortical bone graft.19–22 A first-generation metal endoprosthesis (Veterinary Orthopedic Implants; VOI) compared favorably in strength in a biomechanical study23 to the use of cortical allografts, with similar outcomes in a prospective clinical study.4 The use of metal endoprostheses is often favored as it precludes the need for bone harvesting or banking requirements, allowing for off-the-shelf implant availability and single-procedure reconstruction. Alternative surgical techniques reported in the veterinary literature include ulnar transposition,24,25 microvascular ulnar autograft,26 lateral manus translation,27 acute limb shortening,28 distraction osteogenesis by bone transport,29,30 and, more recently, 3-D–printed, patient-specific endoprostheses.31–34
A retrospective study2 reporting the clinical outcome in 45 dogs with distal radial OSA treated with either of 2 generations of VOI endoprostheses did not find any significant difference between groups, including the severity, frequency, or time of complications; metastasis-free interval; and overall survival time. The main complications reported in that study included infection (78%), implant related (36%), and local recurrence (24%). Implant-related complications were screw loosening (n = 8) or breakage (n = 3), plate fracture (n = 3), and fracture of the radius (n = 1) or metacarpal bones (n = 1). The second-generation VOI implants, used in this study, include angle-stable 2.7/3.5 18-hole locking plates, available in 2 sizes (11.5- and 16-mm width) and 2 materials (316 L surgical steel and titanium alloy for the 11.5-mm plate width only), and endoprostheses available in 2 lengths (98 and 122 mm). The spacer has been redesigned to be lighter and promote bone ingrowth, and the 11.5-mm plate has 2 combination holes that allow for compression (proximal holes 4 and 5).
Advances in implant technology and materials are happening contemporarily to those on bone regeneration with the development of new compounds and strategies to promote bone healing in the presence of large defects, but that often provides negligible contribution to overall construct strength or stiffness. Opportunities for bone regeneration would exist following distal radial ostectomy if biomechanical stability of the bone column without the use of an endoprosthesis could be demonstrated. The purpose of this study was to assess the biomechanical performance of the second-generation 11.5-mm VOI stainless steel locking limb salvage plate and 122-mm metal endoprosthesis combination used to reconstruct distal radial bone defects in canine cadavers and to compare it to the performance of similar plates without the use of endoprostheses (gap group). Our null hypothesis was that constructs without endoprosthesis would fail at lower loads and have lower stiffness than those reconstructed with an endoprosthesis but would not fail at physiological loads.
Methods
Limb collection
Five paired forelimbs (a total of 10 specimens) were collected from skeletally mature dogs over 20 kg, euthanatized for reasons unrelated to this study, with no historical or gross evidence of skeletal disease. Animal owners signed a consent form upon releasing the cadavers to the anatomical pathology service at Colorado State University, Veterinary Diagnostic Services, allowing their use for research. Alternatively, frozen cadaveric limbs were purchased from Skulls Unlimited International Inc, where providers also signed a disclaimer agreeing to the use of cadavers for research. Orthogonal radiographs of the antebrachia, which included elbow-to-metacarpophalangeal joints, confirmed the absence of skeletal deformity or orthopedic disease and were used to obtain preoperative measurements. Each pair of complete forelimbs was frozen at −80 °C within 24 hours of euthanasia until the time of testing. Limbs were thawed at room temperature for 24 hours before construct preparation.
Construct preparation
Limbs underwent an ex vivo limb-spare procedure with commercially available second-generation surgical stainless steel plates and endoprostheses (11.5-mm double-threaded locking-18-hole plates and radius plate 122-mm long endoprostheses; VOI). The dimensions of the plates used are 290-mm length, 11.5-mm width, and 4-mm thickness. Each pair of limbs was randomly allocated to the plate with (stainless steel with endoprosthesis; SS-E group) and without (stainless steel with a gap; SS-G group) endoprosthesis.
For all limbs, the distal radioulnar segment was resected en bloc, and a 122-mm gap was created. The gap was then filled with an endoprosthesis and stabilized with a limb salvage plate in all groups before the endoprosthesis was removed in the gap groups. Surgical approach, distal radioulnar ostectomy, and reconstruction of the bone column were carried out following standard limb salvage and Association for Osteosynthesis/Association for the Study of Internal Fixation principles and previous descriptions.1,23,35,36 Briefly, a standard dorsal approach to the radius, carpus, and third metacarpal bone was done. The distal radioulnar segment was resected en bloc with an oscillating saw, making sure that a minimum of 40% of radial length and enough bone stock for the placement of all 7 proximal radial screws remained. A 2-mm ostectomy of the proximal radial and ulnar carpal bones was also performed with the oscillating saw in all limbs to provide a flat surface to abut the flared distal end of the endoprosthesis. Dedicated 11.5-mm locking, 18-hole limb salvage plates and 122-mm endoprostheses were secured to the limbs with 5 3.5-mm locking, self-tapping bicortical screws and 2 3.5-mm cortical self-tapping screws in the proximal radius; 2 specialized screws in the endoprosthesis (3.5-mm Kuntz Screws 15 mm; VOI); 1 3.5-mm locking, self-tapping bicortical screw in the radial carpal bone; and 8 2.7-mm locking, self-tapping bicortical screws in the third metacarpal bone. The radial combination plate holes were utilized to compress the metal endoprosthesis against the radius. The plate spanned over 90% of both the radial and third metatarsal bone lengths in all limbs and was applied without prebending. In the gap group, the endoprosthesis was removed after the plate was secured. Postoperative orthogonal view radiographs were taken to confirm appropriate implant placement, and the limbs were frozen at –80 °C until biomechanical testing.
Mechanical testing
Constructs were thawed at room temperature for 24 hours before mechanical testing. Testing was performed as by Liptak et al23 to allow for comparison of the results. Briefly, the humerus was osteotomized 5 cm distal to the humeral head, and soft tissues proximal to the elbow joint were removed. The distal humerus was potted in a custom-designed aluminum fixture using high-strength potting compound (Dynacast; Kindt-Collins) to the level of the distal humeral physis. The potted humerus was attached to the actuator of a materials testing machine (MTS Systems) using a custom fixture. The paw was positioned over the load cell to yield an elbow flexion angle of approximately 125° and a reconstruction offset from the vertical of 10°. To prevent slippage of the paw during axial loading, it was potted in high-strength dental plaster (Resinrock Die Material; Whip Mix; Figure 1)
Limb positioning in the materials testing machine (MTM) before testing. The distal humerus is attached to the actuator of an MTM through a potted fixture at the level of the distal physis. The elbow is flexed at approximately 125°, and the paw is offset 10° from the vertical axis and potted to prevent slippage during axial loading.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.11.0364
Limbs were preconditioned by cyclic axial compression for 30 cycles at 0.25 Hz between 5 and 7 mm of displacement to account for settling of the fixture and viscoelastic artifacts prior to axial compression to failure at 2.5 mm/s. All testing was video recorded to assist in determining the mode of failure. After mechanical testing, orthogonal radiographs of each construct were obtained. Load and displacement data were acquired at 100 Hz during mechanical testing. Load-displacement curves were generated for each specimen tested. Five values were obtained from each load-displacement curve: stiffness (N/mm), yield load (newtons), yield energy absorbed (N/mm), ultimate load (newtons), and ultimate energy absorbed (N/mm). Stiffness was obtained by calculating the slope of the linear region of each curve. Yield strength was defined as the point reaching a 0.2% offset from the linear region of the x-axis. Ultimate load was taken as the maximum force registered during testing or the point on the load-displacement curve immediately preceding the first sudden decrease in load. Yield and ultimate energies were calculated by integrating the polynomial regression curves fitted to each force-displacement curve using Excel (Microsoft Corp) and incorporating the appropriate upper and lower displacement limits. Results were reported as mean ± SD for the SS-E and SS-G groups, respectively (Table 1).
Effect of presence of an endoprosthesis on load and displacement data.
| Yield | Ultimate | ||||
|---|---|---|---|---|---|
| Construct | Stiffness (N/mm) | Load (N) | Energy (N/mm) | Load (N) | Energy (N/mm) |
| SS-E | 360 ± 64 | 644 ± 523 | 1,126 ± 1,695 | 3,385 ± 512 | 39,732 ± 11,679 |
| SS-G | 180 ± 50 | 288 ± 153 | 239 ± 251 | 747 ± 98 | 5,175 ± 878 |
Values reported are mean ± SD.
SS-E = Endoprostheses group. SS-G = Gap group.
Data analysis
An a priori power estimation was completed to ensure adequate samples were tested to detect significant differences in ultimate load outcome using data from similar studies.23,37 A Wilcoxon matched-pairs signed-rank test was performed in this small data set to determine differences in the response variables between groups. The significance level for all statistical analyses was set at P < .05.
Results
Stiffness was 360 ± 64 N/mm and 180 ± 50 N/mm for the SS-E and SS-G groups, respectively (P = .062; Figure 2). Neither group exhibited a discernible yield on the load-deformation curves, and the calculated offset yield load was 644 ± 523 N and 288 ± 153 N (P = .031). Yield energy absorbed was 1,126 ± 1,695 N/mm and 239 ± 251 N/mm (P = .031; Figure 3). Ultimate load was 3,385 ± 512 N and 747 ± 98 N (P = .062). Ultimate energy absorbed was 39,732 ± 11,679 N/mm and 5,175 ± 878 N/mm (P = .031; Figure 4). Yield load, yield energy, and ultimate energy absorbed were significantly different between groups.
Bar graph comparing the stiffness between reconstruction groups and associated P values. SS-E = Endoprostheses group, 360 ± 64 N/mm. SS-G = Gap group, 180 ± 50 N/mm.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.11.0364
Bar graphs comparing yield and ultimate load between reconstruction groups and associated P values. Constructs in the gap group were significantly weaker at yield than constructs in the endoprosthesis group.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.11.0364
Bar graphs comparing yield and ultimate energy absorbed between reconstruction groups and associated P values. Constructs in the gap group absorbed significantly less energy prior to yield and failure than constructs in the endoprosthesis group.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.11.0364
The modes of failure varied between construction types. Constructs in the SS-E group had multiple modes of failure, with humeral fracture at the junction of potting mix and humerus occurring in 2 limbs and sharp bending of the plate at the level of the screw holes closest to the endoprosthesis occurring in 3 constructs, 1 at the level of the seventh carpal screw hole and 2 at the level of the radial carpal screw hole. The biomechanical performance of the limbs that failed by humeral fracture was similar or superior when compared to other samples in the same group and were therefore included in the statistical analyses. All constructs in the SS-G group failed by gradual bending of the plate centered in the midgap area (Figure 5).
Post-testing radiographs showing representative modes of failure of the 2 construct groups, with (A) dorsal sharp bending of a plate at the level of the radiocarpal screw hole in the endoprosthesis construct and (B) dorsal gradual bending of a plate centered at the midpoint of the defect in the gap construct.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.11.0364
Discussion
The aim of this study was to compare the biomechanical properties of a commercially available limb salvage implant, tested under compressive forces in cadaveric models, with and without endoprostheses. The authors hypothesized that if bone reconstructions without endoprostheses were biomechanically sound (ie, would not fail under physiological forces), regenerative strategies could be applied to the distal radial bone defect without the need for additional structural support. In the studied conditions, constructs without endoprosthesis appeared to be weaker than those reconstructed with an endoprosthesis, although stiffness and ultimate load did not reach statistical difference. The authors argue that similar constructs without the use of an endoprosthesis may be unable to resist physiological forces in the clinical setting.
The use of second-generation VOI 11.5-mm stainless steel locking limb salvage plates with 122-mm endoprostheses were selected for this study. The locking compression plate technology works as a locked internal skeletal fixator system that allows for bone stabilization by bridging the fracture site (bridging osteosynthesis).38,39 Unlike the conventional compression plate method, it does not rely on plate-to-bone friction to stabilize the fracture site and can thus potentially decrease damage to the soft tissues and periosteal blood supply. The use of locking compression plates, in combination with a more flexible elastic fixation, may promote callus formation and rapid fracture healing. This technology is often used for complex fractures (ie, multifragmentary or with bone loss) and does not require precise plate contouring. The addition of combination holes on this type of technology allows for the use of the plate as a compression plate or the combination of both techniques depending on the fracture anatomy.38,39 Despite these stated advantages, a retrospective study2 comparing the clinical outcome following limb-sparing surgery using both generations of VOI stainless steel implants for the management of distal radial OSA found no significant differences in the frequency, severity, or timing of surgical complications. The older generation of implants are, however, no longer commercially available, and the use of locking implant technology may still provide some advantages for the implementation of bone regeneration strategies.
Due to the indiscernible yield exhibited by these samples, an offset yield was utilized to reproducibly assess this construct property.40 The yield load, the stress point where deformation of a material becomes permanent and nonreversible, is often poorly defined for high-strength steel due to the gradual onset of nonlinear behavior. An arbitrary offset yield point is often set at 0.2%, stress at which 0.2% of plastic deformation occurs.40 In this study, the yield strength for the endoprosthesis group was significantly higher than for the gap group. Offset yield values for the SS-E group differed markedly with those of a previous similar study23 that used first-generation metal endoprosthesis and where the ulna was also resected (644 ± 523 vs 2,922 ± 563, respectively). Comparisons, however, are not possible due to differences in technology and points of measurement in force-displacement curves.25 Ultimate load in the endoprosthesis group were comparable to results in that same study23 (3,385 ± 512 vs 3,053 ± 528, respectively), whereas constructs in the gap group were weaker and more flexible.
Modes of failure varied between groups and included humeral fracture and plate bending. Humeral fractures were previously reported in a similar study23 and occurred in 2 samples in our endoprosthesis group at forces similar to others in the same group but significantly higher than constructs in the gap group. The methodology used, including the potting technique, may have concentrated stress at the point of fracture, aggravated by the smaller bone size allowed in the inclusion criteria. Bending of the plate occurred in both groups, albeit in different locations. Plates in the endoprosthesis group concentrated stress at the bone-endoprosthesis interface and failed through the closest screw holes, the most distal radial proximally (1 sample), or the radiocarpal distally (2 samples). In the gap group, acting forces and plate bending spread across the gap, causing a broad bend centered in the middle of the gap.
Critical-size bone defects are those that cannot heal spontaneously despite surgical stabilization without further intervention (ie, bone grafting). The size has not been strictly defined and depends on multiple factors related to the bone (relative size of the defect, anatomical location, and presence of circumferential loss), environment (status of the soft tissue envelope and blood supply), and patient (age and presence of comorbidities).41–43 It has been suggested that a defect 2 to 2.5 times greater than the diameter of the affected bone should be considered a critical bone defect unable to heal without appropriate treatment. Radial defects following ostectomy for the management of OSA often fall in this group.44 In humans, the most commonly used strategies to reconstruct large bone defects are distraction osteogenesis and the induced-membrane technique, pioneered by Masquelet and Begue.45 In humans, distraction osteogenesis (ie, segmental transport) remains the gold standard for large bone defects (ie, > 7 cm) and poorly vascularized sites due to the high rate of ultimate success despite the prolonged time of treatment required (months).46 Biologic materials also often considered to promote bone healing include bone marrow aspirates, platelet-rich plasma, and bone morphogenetic proteins despite there currently not being enough evidence to recommend the use of platelet-rich plasma alone or in combination with other bone grafts for bone defect management, and evidence is controversial for the effectiveness of bone morphogenetic proteins-2, with a risk of side effects.47 In humans, sources of osteoprogenitor cells, such as concentrated bone marrow aspirates, are often combined with osteoconductive carriers or scaffolds, such as particulate demineralized bone matrix, collagen sponges, and porous hydroxyapatite ceramics. The most commonly used biomaterials for fracture repair are metals, such as stainless steel and titanium alloys, and polymers, such as polyethene and polyetheretherketone. Metallic biomaterials are still preferred for load-bearing bone applications due to their high mechanical strength and resistance to fracture.48 The authors argue that if constructs without the use of endoprosthesis provided sufficient structural support for use in the limb-spare clinical patient, the use of regenerative strategies that lack biomechanical strength could be considered in those patients.
In this study, however, constructs in the gap group were weaker and more flexible than those reconstructed with an endoprosthesis, and the clinical use of second-generation 11.5-mm VOI plates without a filler for radial surgical limb spare in large- or giant-size dogs is not recommended. Forelimbs of dogs bear about 60% of their bodyweight at walk, with an estimated peak vertical force, or maximum load placed on the ground during the stance phase, of 6.35 N/kg at walk, a force that approximately doubles at trot.49,50 With an estimated median body weight of 25 kg for our test cadavers, a peak vertical force of 159 N at walk and 317 N at trot can be calculated. Mean yield load for the steel gap groups was 288 N, indicating that a trotting gait of these patients would cause cyclic loading of the metal plate, potentially leading to metal fatigue and catastrophic implant failure and excessive motion at the healing site that might inhibit bone healing. Peak vertical force can increase to 42 N/kg when a dog jumps from a height of 94 cm, resulting in a 1,050-N vertical compressive force in a 25-kg dog.51 This value is above the ultimate strength of the stainless steel constructs in the gap group, with ultimate forces prior to failure of 746.8 N. A single jump of a 25-kg patient reconstructed without endoprosthesis could therefore lead to catastrophic failure of the implant. The average weight of patients clinically affected by distal radial OSA, candidates for this type of therapy, is significantly higher.
Some limitations of this study are inherent to the ex vivo cadaveric nature of the study (ie, alteration of tissue characteristics) and the material testing modality (ie, the test performed may not accurately reflect the complexity of the clinical situation). Potting of the paw with plaster may not have allowed for bending of the manus and may have increased the overall stiffness of the construct, which may have affected the results. Freezing of limbs with implants on prior to testing may have led to artefactual screw loosening due to the different response of bone and metal to the freezing and thawing processes. An important limitation in the methodology is the acute compressive testing to failure rather than the more physiological cycling. Preliminary testing in a similar study23 attempted to evaluate the effect of cyclic loading on limbs reconstructed with endoprostheses and cortical allografts through 100,000 cycles at 30% to 100% of body weight. None of the 4 tested constructs failed, and the authors argued that in excess of 1 million cycles would have been more representative of the clinical scenario but could not be considered for logistical and financial reasons. This study did not test the sturdier second-generation 16-mm width, 5-mm thickness, 18-hole, stainless steel locking VOI limb salvage plate, which may be better suited for use without an endoprosthesis, and further studies are required to determine its biomechanical properties in similar conditions. The lack of statistical significance of some of the results may be attributed to the low number of samples (ie, type II error).
In conclusion, the standard-of-care limb salvage plate–endoprosthesis combination utilized for the clinical reconstruction of distal radii affected by OSA was stiffer and stronger than the gap group tested in this biomechanical study. The authors do not recommend the use of second-generation 11.5-mm VOI stainless steel plates without endoprostheses during limb salvage management of distal radial OSA in large- or giant-breed dogs due to the significant risk of implant fatigue and catastrophic implant failure at trot or following a single jump.
Acknowledgments
None reported.
Disclosures
Dr. Wustefeld-Janssens is a member of the AJVR Scientific Review Board, but was not involved in the editorial evaluation of or decision to accept this article for publication.
No AI-assisted technologies were used in the composition of this manuscript.
Funding
Funded by an Internal Pilot Grant from the Colorado State University Animal Cancer Center.
ORCID
J. Aisa https://orcid.org/0000-0003-3880-4875
J. W. Johnson https://orcid.org/0000-0001-7465-3854
B. G. Wustefeld-Janssens https://orcid.org/0000-0001-8458-1735
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