Abstract
The objective of this study was to compare the strength and stiffness of various fixation methods applied to the long bones of the rabbit forelimb. Twenty rabbit radius/ulna and 20 rabbit humeri were randomly assigned to 1 of 4 groups. Control bones remained intact, whereas all others were osteotomized to create fracture models that were fixated with locking plate and locking screws (LP), veterinary cuttable plate (VCP) with cortical screws, or external skeletal fixator constructs (ESF), and tested in 4-point bending until failure. Load/deformation curves were generated for each sample and used to calculate stiffness (slope of the curve) and strength (load to failure). Intact controls had greater strength and stiffness than any fixation techniques in the rabbit radius/ulna and humeri samples. Locking plate and VCP constructs had greater stiffness than ESF when applied to the radius, whereas locking plate constructs were stronger than VCP or ESF when applied to the humerus. Overall, the LP construct had characteristics most closely resembling those of the intact control regarding strength in the humerus. Therefore, fracture fixation with a LP would provide the greatest strength in humeral fracture repairs in the rabbit.
Résumé
Analyse biomécanique de trois techniques de fixation du radius et de l’humérus de lapin. L’objectif de cette étude était de comparer la résistance et la rigidité de différentes méthodes de fixation appliquées aux os longs du membre antérieur du lapin. Vingt radius/cubitus de lapin et 20 humérus de lapin ont été assignés au hasard à un des quatre groupes. Les os témoins sont restés intacts, tandis que tous les autres ont été ostéotomisés pour créer des modèles de fracture qui ont été fixés avec une plaque de verrouillage et des vis de verrouillage (LP), une plaque vétérinaire découpable (VCP) avec des vis corticales ou des constructions de fixateur squelettique externe (ESF), et testés dans une flexion en quatre points jusqu’à la rupture. Des courbes de charge/déformation ont été générées pour chaque échantillon et utilisées pour calculer la rigidité (pente de la courbe) et la résistance (charge à la rupture). Les témoins intacts avaient une résistance et une rigidité supérieures à toutes les techniques de fixation dans les échantillons de radius/cubitus et d’humérus de lapin. Les constructions à plaque de verrouillage et VCP avaient une plus grande rigidité que l’ESF lorsqu’elles étaient appliquées au radius, tandis que les constructions à plaque de verrouillage étaient plus solides que VCP ou ESF lorsqu’elles étaient appliquées à l’humérus. Dans l’ensemble, la construction LP avait des caractéristiques ressemblant le plus à celles du témoin intact en ce qui concerne la force de l’humérus. Par conséquent, la fixation des fractures avec un LP fournirait la plus grande résistance dans les réparations des fractures humérales chez le lapin.
(Traduit par Dr Serge Messier)
Introduction
Domesticated rabbits (Oryctolagus cuniculus) are increasingly popular household pets, ranking as the third most popular companion mammal, just behind cats and dogs (1–3). With an estimated 3 million domesticated rabbits in the US alone, that popularity brings a rise in veterinary visits, ranging from general husbandry to emergency care (2).
Skeletal, particularly long bone fractures, account for more than 50% of reported fractures in rabbits (4). Although fractures in our companion cats and dogs are typically the result of high-impact trauma, e.g., due to vehicles or bite wounds, rabbit long bone fractures are more commonly due to a fall injury, often by jumping out of an owner’s arms (4–6). Rabbits have a smaller bone to body weight ratio than dogs and cats, which may predispose this species to fracture and contribute to the difficulty in their repair (7). In addition, rabbits carry nearly 70% of their body weight in their hind limbs with highly muscled pelvic limbs potentially contributing to the higher prevalence of tibial and femur fracture than forelimb fractures (5,8). Other factors such as a strong startle response and high sensitivity to perceived threats make this species vulnerable to falls, resulting in fractured bones (8,9). Although thoracic limb fractures are less frequent in rabbits, they are more challenging to repair than pelvic limb fractures due to the smaller size and brittle nature of these bones (5,10–13). A successful outcome depends on a stable construct able to withstand high-energy forces, allowing early mobility and return to normal function (5).
Limited information exists on the success and prognosis of long bone fractures in rabbits to guide orthopedic management (5,8,10–16). Traditional repairs of radial and humeral fractures in small animals (cats and dogs) have involved the use of locking plates, dynamic compression plates, and external skeletal fixators (8,10,14–15). However, emergence of smaller orthopedic implants has expanded these traditional methods to smaller companion animals, including rabbits. To the authors’ knowledge, no study exists comparing various plate and external fixation methods to address long bone fractures in the rabbit forelimb.
The objective was to apply 3 fixation methods to the long bones of rabbit forelimbs with osteotomies, to mimic a transverse fracture, and to subject these constructs to biomechanical testing to determine strength and stiffness in 4-point bending testing and to compare these fixation techniques to characteristics of intact bones. It was hypothesized that the locking plate construct most closely approaches the characteristics of intact bones when subjected to 4-point bending.
Materials and methods
Animals
Intact samples (radius/ulna and humerus) were obtained with permission from private owners of rabbits that were treated at the Red Bank Veterinary Hospital in Tinton Falls, New Jersey and were euthanized or died of disease processes unrelated to orthopedic pathology. If orthopedic disease was identified, samples were excluded from study and analysis.
Diagnostic imaging
Diagnostic imaging of harvested bones was performed by means of conventional radiography (Vet-Ray; APX Imaging, Naperville, Illinois, USA). Any samples with radiographic evidence of orthopedic disease were excluded from the study. Radiographic images were used to ensure similar bone size. Any radius with a minimum diaphyseal diameter < 3.8 mm or > 4.0 mm, and any humerus with a minimal diaphyseal diameter < 5.5 mm or > 6.5 mm were excluded.
Sample handling
Immediately following euthanasia, the radius/ulna and humeri samples were harvested. All musculature was stripped from the bones, which were then wrapped in saline-soaked gauze sponges. All samples were stored in a −20°C freezer for preservation until testing. The 20 radius/ulna and 20 bones were randomly assigned using a random number generator into 1 of 4 groups (intact, veterinary cuttable plate fixation, locking plate fixation, or external skeletal fixator fixations).
Surgical fixations were chosen to mirror applications in clinical patients. Immediately prior to surgical fixation, bones were removed from the freezer and allowed to thaw at room temperature for 1 h. All fixation applications were performed at Red Bank Veterinary Hospital. Biomechanical testing occurred immediately after fixation and radiographic evaluation of the samples.
Veterinary cuttable plate (VCP) fixation was performed using a stainless steel 1.5-mm veterinary cuttable plate (DePuy Synthese VET, Johnson-Johnson, New Brunswick, New Jersey, USA) cut to a length of 31 mm (including 6 screw holes). Plates were 0.8-mm thick with a width of 3.8 mm and a hole spacing distance of 5 mm. Screws used were 1.5-mm self-tapping stainless-steel screws with a thread diameter of 1.5 mm, core diameter of 1.1 mm and thread pitch of 0.6 mm (DePuy Synthese VET, Johnson-Johnson). Six screws were placed engaging both cis and trans cortices of the bone using a neutral drill guide, the plate was positioned such that the transverse osteotomy was located between screw numbers 3 and 4. Locking plate (LP) fixation was performed using a 6-hole cuttable titanium locking plate (OsteoCertus, Florida, USA) cut to a length of 33 mm, including 6 screw holes. Plates were 1.6-mm thick with a width of 4.6 mm and a hole spacing distance of 6 mm. Screws used were 1.5-mm self-tapping titanium screws with a thread diameter of 1.5 mm, core diameter of 1.1 mm and thread pitch of 0.55 mm. Six screws were placed engaging both cis and trans cortices of the bone using a neutral drill guide, the plate was positioned such that the transverse osteotomy was located between screw numbers 3 and 4. All plate constructs were applied to the cranial aspect of the radius in the radius/ulna samples or to the medial aspect of the humerus samples with the center of the osteotomy placed in the center of the bone, as measured from proximal to distal.
In the radius/ulna samples, the external skeletal fixator (ESF) apparatus was constructed using 1.5 mm smooth stainless-steel pins (IMEX Veterinary, Longview, Texas, USA) placed in a type 2 configuration. The pins engaged the radius and were placed 5 mm apart. Side bars were constructed medially and laterally with 5-cm moldable casting material cut to a length of 35 mm (Vet-Lite; Veterinary Specialty Products, Florida, USA). The thermoplastic casting material was heated in hot water and rolled to create a cylinder and molded into the pins to create parallel side bars 10 mm from the surface of the bone (Figure 1). In the humerus, the external skeletal fixator apparatus was constructed using 1.5-mm smooth stainless-steel pins in a type 1 configuration. The pins engaged both cis and trans cortices and were placed 5 mm apart. An intramedullary 1.5-mm smooth stainless-steel pin was introduced in a normograde fashion, starting at the greater tubercle and proceeding until the distal aspect of the humerus was engaged. A side bar was constructed on the lateral surface of the bone with 5-cm moldable casting material cut to a length of 100 mm (Vet-Lite; Veterinary Specialty Products). The thermoplastic casting material was heated in hot water and rolled to create a cylinder and molded into the lateral pin and intramedullary pin to create a side bar 10 mm from the surface of the bone. For all external skeletal fixator apparatuses, including radius/ulna and humerus samples, 3 pins were placed proximal, and 3 pins were placed distal to the transverse osteotomy with the osteotomy in the center of the bone, as measured from proximal to distal. All constructs and implants were radiographed using conventional radiography to ensure appropriate placement of implants.
Figure 1.
Example of radius/ulna fixation (left to right) with a type 2 external skeletal fixator, locking plate with locking screws and veterinary cuttable plate with cortical screws. Scale bar = 10 cm.
Destructive 4-point bending
All constructs were subjected to 4-point bending tests until failure. The support span was set at 48 mm and the loading span was set at 4 mm. Displacement was measured using Rubeder electronic vernier calipers IP54 (Quzhou Technology, Quzhou, China). Force was measured with a Mark-10 digital force gauge FM-207 (Mark-10, New York, USA). Constructs were loaded into the device to apply the load in a caudal to cranial direction in the radius/ulna and humerus samples (Figure 2).
Figure 2.
Example of radius/ulna subjected to 4-point bending. Scale bar = 10 cm.
A load was applied constantly until the construct was stable in the device with no displacement prior to the start of each trial. A constant displacement of 1 mm/min was applied until the constructs failed catastrophically, defined as an abrupt loss of fixation due to the bone breaking or implants pulling out of the bone. Measurements were taken every 15 to 30 s to generate the load displacement curve for each sample. The ultimate strength of each construct was defined as the maximum total newton (N) of force immediately prior to catastrophic failure. Stiffness was defined as the mathematical slope calculated from the stress/strain curve within the area of elastic deformation.
Statistical analyses
All results are shown as mean ± standard deviation. A mixed model 1-way analysis of variance (ANOVA) was used to detect differences among the 4 groups. Comparisons were performed to test the underlying hypothesis focusing on the biomechanical differences between intact bone and above-listed fixation techniques (VCP, LP, and ESF), between plate constructs (LP and VCP) and ESF and between plated constructs (LP versus DCP) within the radius/ulna groups and the humerus groups. Data were analyzed using within application statistical calculations (Microsoft Office Excel; Microsoft, Redmond, Washington, USA) and verified using open-source software JASP Team (2021 Version 0.15; https://jasp-stats.org, ©2013–2021 University of Amsterdam, The Netherlands). For all analyses, P < 0.05 was considered significant.
Results
Animals
Five rabbits were excluded based on failure to meet participation criteria. A total of 10 adult rabbits were included in the present study, resulting in 20 radius/ulna and 20 humeri samples. Among the breeds represented were miniature lop (n = 2), unknown (n = 3), Lionhead (n = 1), New Zealand white (n = 1), mini rex (n = 1), Dutch (n = 1), and Holland lop (n = 1). The average age was 4.6 ± 2.5 y with an average total body weight of 2.2 ± 0.5 kg.
Radius/ulna
The average radius/ulna length (mm) was 62.1 mm ± 0.5 mm with an average width of 3.8 mm (Table 1). Load displacement curves were created for all samples (Figure 3). The intact radius/ulna was stronger (158.4 ± 56.8 N) than samples with applied fixation techniques (P, 0.01), including the VCP (58.6 ± 42.7 N), LP (66.6 ± 10.8 N) and ESF (46.5 ± 17.44 N). No difference in strength was identified when ESF was compared to the VCP (P = 0.66), or the LP (P = 0.09). No difference in strength was identified between VCP or LP constructs (P = 0.91; Figure 4).
Table 1.
Animal samples and characteristics of the rabbits and bones. Left and right radius/ulna and humerus measurements were identical in all samples.
| Breed | Body weight (kg) | Age (y) | Radius/ulna length (mm) | Radius/ulna width (mm) | Humerus length (mm) | Humerus width (mm) |
|---|---|---|---|---|---|---|
| Unknown | 2.9 | 4 | 62.5 | 3.8 | 72.7 | 6.0 |
| Lionhead | 2.2 | 9 | 63.5 | 3.8 | 73.5 | 5.6 |
| New Zealand White | 2.9 | 6 | 63.7 | 3.8 | 67.5 | 5.6 |
| Mini Lop | 2.1 | 3 | 60.2 | 3.8 | 63.9 | 6.0 |
| Unknown | 1.4 | 2 | 60.6 | 3.8 | 65.3 | 5.6 |
| Mini Rex | 2.9 | 5 | 60.2 | 3.8 | 67.4 | 6.3 |
| Unknown | 2.2 | 7 | 60.7 | 3.8 | 66.3 | 5.6 |
| Mini Lop | 1.9 | 5 | 64.2 | 3.8 | 71.5 | 6.2 |
| Dutch | 2.0 | 1 | 61.3 | 3.8 | 66.6 | 6.1 |
| Holland Lop | 2.4 | 2 | 63.7 | 3.8 | 71.2 | 5.6 |
Figure 3.
Load/displacement curves of intact (blue), external skeletal fixator (yellow), veterinary cuttable plate (orange), and locking plate fixation (green) in rabbit radius/ulna. Three representative curves were included for each group.
Figure 4.
Average strength measured in newtons (N) of intact (control), veterinary cuttable plate fixation (VCP), locking plate fixation (LP), and external skeletal fixator (ESF) in rabbit radius/ulna. The intact radius/ulna displayed greater strength (N) than all fixation methods including VCP, LP, and ESF, noted by an asterisk (*). No significant difference was determined between fixation methods. Error bars denote standard deviation. Line denotes groups comparisons.
The intact radius/ulna was stiffer (129.4 ± 62.4 N/mm) than samples with applied fixation techniques (P < 0.01), including VCP, LP and ESF (26.5 ± 17.2, 26.3 ± 19.2, and 7.4 ± 4.4 N/mm, respectively). The ESF construct was less stiff than VCP (P < 0.01) and LP (P < 0.01). No difference in stiffness was identified between VCP and LP fixations (P = 0.98; Figure 5). All constructs failed from a longitudinal fracture along the long axis of the bone near the screw-bone or wire-bone interface.
Figure 5.
Average stiffness measured in newtons (N/mm) of displacement of intact (control), veterinary cuttable plate fixation (VCP), locking plate fixation (LP) and external skeletal fixator (ESF) in rabbit radius/ulna. The intact radius/ulna displayed greater stiffness (N/mm) than all fixation methods including VCP, LP, and ESF, noted by an asterisk (*). The plate constructs (VCP and LP) displayed greater stiffness in comparison to the ESF, noted by octothorpe (#). No differences were determined between plate constructs (VCP and LP). Error bars denote standard deviation. Line over bars indicate group comparisons.
Humerus
The average humerus length (mm) was 68.6 mm ± 3.3 mm with an average width of 5.9 mm ± 0.3 mm (Table 1). Load displacement curves were created for all samples (Figure 6). The intact humerus was stronger (230.46 ± 52.48 N) than samples with applied fixation techniques (P < 0.01), including VCP, LP, and ESF (54.66 ± 38.97, 124.14 ± 32.81, and 75.56 ± 21.96 N, respectively). No difference in strength was identified when ESF was compared to the VCP (P = 0.66), although the LP was stronger than the VCP (P = 0.01) or ESF (P = 0.02; Figure 7).
Figure 6.
Load/displacement curves of intact (blue), external skeletal fixator (yellow), veterinary cuttable plate (orange), and locking plate fixation (green) in the rabbit humerus. Three representative curves were included for each group.
Figure 7.
Average strength measured in Newtons (N) of intact (control), veterinary cuttable plate fixation (VCP), locking plate fixation (LP) and external skeletal fixator (ESF) in the rabbit humerus. The intact humerus displayed greater strength (N) than all fixation methods including VCP, LP and ESF, noted by an asterisk (*). The LP displayed greater strength than the VCP, noted by octothorpe (#). Line denotes groups comparisons. Strength (N)
The intact humerus was stiffer (354.52 ± 64.72 N/mm) than samples with applied fixation techniques (P < 0.01), including VCP (33.49 ± 34.96), LP (60.96 ± 39.16), and ESF (15.05 ± 4.14 N/mm). There was no difference among fixation groups (VCP, LP and ESF) with regards to stiffness (P > 0.2; Figure 8).
Figure 8.
Average stiffness measured in newtons (N/mm) of displacement of intact (control) veterinary cuttable plate fixation (VCP), locking plate fixation (LP) and external skeletal fixator (ESF) in the rabbit humerus. The intact humerus displayed greater stiffness (N/mm) than all fixation methods including VCP, LP, and ESF, noted by an asterisk (*). No differences were determined between fixation techniques. Error bars denote standard deviation. Line over bars indicate group comparisons.
All constructs failed from a longitudinal fracture along the axis of the bone near the screw-bone or wire-bone interface.
Discussion
This study mechanically tested 3 fixation techniques on the radius/ulna and humerus of rabbits. In companion rabbit breeds, placement of implants is chosen based on the ability to maximize biomechanical stability as well as ease of surgical approach and accessibility to the bone. In this study, implant placement was chosen to simulate fracture fixation used in clinical cases. A transverse osteotomy was created to mimic a transverse fracture. The locking plate provided the greatest strength in the humerus, but strength did not differ among constructs when applied to the radius/ulna. The locking plate and veterinary cuttable plate constructs were stiffer than the external skeletal fixator constructs in the radius/ulna, but not in the humerus. All constructs failed to reach the strength or stiffness of intact bone. Taken together, we accepted our null hypothesis regarding locking plate fixation of the rabbit humerus but not the rabbit radius/ulna. Further research is warranted to investigate these differences.
Previous studies suggested a locking plate construct to be a better construct in small animals due to its unique locking mechanism between the screw heads and plate holes acting as an internal fixator (17). The use of locking plate over a dynamic compression plate is supported by studies in dogs (18–20) and cats (20). In Watrous et al (21), radial fractures in miniature breed dogs were treated with either 1.5-mm straight or locking plate fixation techniques results, with greater strength for locking plates compared to straight plates. Takizawa et al (14) compared 3 miniature locking plate systems (TITAN LOCK, Fixin micro series, and LCP) in a rabbit radial/ulnar fracture model and reported a greater load carry by the LCP; however, overall, the 3 miniature locking sets provided similar adequate stabilization 4 wk after surgery.
In the present study, the locking plate system had superior strength in the humerus, but not in the radius/ulna. Previous data evaluating bicortical screw placement in rabbits recommended no more than 30% of the diameter of the bone to avoid fissure and/or fracture (22). This was exceeded in this study in the radius, due to use of 1.5-mm screws, and may have contributed to failure to detect significant strength differences among implants in the radius/ulna.
The veterinary cuttable plate and locking plate constructs were stiffer than the external fixator in the radius/ulna, but not in the humerus models. This was most likely due to the difference in the design between the 2 models. In the radius/ulna model, a type 2 fixator was used, with the side bars 10 mm from the surface of the bone. Pins were placed from medial to lateral. A force applied from caudal to cranial would likely be in the direction that the construct was least able to resist the force. In the humerus, a type 1 fixator was used with an intramedullary pin, which was tied into the construct. The addition of the intramedullary pin would significantly resist bending forces, thus increasing the stiffness of the construct. These designs were chosen to mirror what is performed clinically at our institution. It is also possible that differing materials used for connecting bars could have affected overall stiffness and strength of the external fixation techniques.
The load deformation curves in this study were linear with no obvious yield point. This is characteristic of brittle materials which fail before they reach the point of plastic deformation. Rabbit bones are notoriously challenging to repair due to the tendency to fissure during repair (23). This characteristic was evident in our mechanical testing. Evaluation of the constructs, after loading, revealed similar mode of failure regardless of the bone (radius/ulna or humerus) or fixation technique (plate or external fixator). When loads were applied in a caudal-to-cranial direction, the mode of failure consisted of a longitudinal fracture along the long axis of the bone near the screw-bone or wire-bone interface. Minimal deformation of the hardware was seen at the time of failure, suggesting that the brittle rabbit bone at the implant-bone interface was the weakest point of the construct. Perhaps smaller sized implants at the implant-bone interface may provide a stronger repair. In addition, fewer implants spaced further apart may increase the force to failure.
This study compared various implant designs, including different types of metal in the designs. The plates and screws were chosen to be as close to the same size as possible. The stainless-steel plates and screws as well as the pins used for the external fixators were composed of 316L stainless steel, a combination of metals commonly used due to the desirable traits of high strength combined with high corrosion resistance. The titanium implants were constructed of titanium 6–4 alloy, stronger than pure titanium, and also very highly biocompatible. Stainless steel and titanium alloys have different mechanical properties which may have affected the results. Titanium alloys tend to be stronger with more elasticity than stainless-steel. In addition, despite efforts to minimize variability, the plates were slightly different lengths, widths, and heights with slightly different hole spacing, which may have affected the biomechanical results. In addition, this study did not test in compression or torsion, both forces which would be present in clinical cases.
In any given biological environment, a combination of factors, including construct strength and construct stiffness, are required to provide the best microenvironment for bone healing while withstanding the external forces from activity and mobility in the rabbit. These biomechanical data may be used to help determine the optimal repair of factures in clinical situations. The brittle nature of rabbit bones as well as the small size present challenges to any surgical repair. Care should be taken to choose the smallest size implants possible to decrease the potential for propagation of fissures along the bone implant interface as force is applied to the bone. CVJ
Footnotes
Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.
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