Comminuted, nonreconstructable femoral fractures are a frequently encountered and challenging type of fracture in cats. Anatomic reduction requires extensive surgical exposure and manipulation of the fractured bone. Biological internal fixation obviates the need for precise reduction, which shifts the concept from anatomic reduction toward axis restoration and gives priority to biology over mechanics.1–7 Fundamental principles of biological osteosynthesis are based on the need for preservation of blood supply and include minimizing iatrogenic soft tissue disruption,8 use of indirect fracture reduction techniques, application of appropriate stable fixation, and promotion of early return of limb function.9
The goal of attaining the best biological conditions for healing, rather than achieving absolute stability of fixation, is approached by alignment of the main fragments, which provides articular surfaces in a proper 3-D position of angulation, torsion, and length. Basic biological internal fixation techniques are aimed at elastic fixation imitating conditions of spontaneous healing, which includes induction of callus formation.
The method of locked plating has been compared with the use of an angle-stable internal fixator. Locking internal fixators have minimal implant-to-bone contact, which requires less shaping of implants to conform to the bone configuration than the shaping that is required for conventional plates; in addition, locking internal fixators generally are used in a long-span bridging configuration and require low numbers of screws for fixation.1,10
Additional use of an intramedullary pin has been found to be beneficial in facilitating reduction and restoration of alignment, especially in comminuted fractures.11 By reducing plate strain, the intramedullary pin provides a sparing effect on the plate.12 Use of MIPO has gained substantial interest in human trauma surgery, and with the paradigm shift toward biological osteosynthesis, bridge plating techniques are gaining acceptance in veterinary medicine, especially for extremely comminuted fractures.13
Careful handling and preservation of soft tissues around a fracture site are main postulates of biological fracture repair. A plate is inserted through a small incision at 1 end of the fractured bone and maneuvered through a submuscular tunnel along the periosteal surface of the bone. Screws are inserted at each end of the plate, with additional incisions made as needed.14,15 Preservation of a fracture hematoma may contribute to increased callus formation.8,16 Screw placement in relation to the fracture gap may influence plate strain in a buttress plate construct.17 However, there are few recommendations concerning screw position in locked internal fixators for use in veterinary patients. Screw position in relation to the fracture gap and the need for soft tissue dissection near the fracture are important considerations in MIPO.
A locking plate–rod construct with a recently developed locking plate system has been described.18 Stability of this locking plate relies on a fixed-angle construct because screws lock into the plate. Therefore, the use of compressive forces against the periosteum and bone fragments to create stability is not needed. This plate is designed to provide nearly uniform bending strength along the entire plate length, and the cross-section profile of the plate enables more periosteal blood flow than for standard plates. Insertion of standard screws at various angles or locking screws at a fixed angle of 90° is possible because of the geometry of the screw holes. These plates are cuttable and can be bent in both planes.
The purpose of the study reported here was to compare the effect of screw position on biomechanical properties of a combination locking plate–rod construct in a synthetic fracture gap model. We hypothesized that positioning of 1 screw near the fracture gap would lead to increased strength and stiffness of the construct.
Materials and Methods
Sample
Three constructs (2 locking plate–rod constructs and 1 locking plate construct) were tested in a diaphyseal bridge plating configuration by use of bending and torsion. Variables included screw position (near the fracture gap and far from the fracture gap) and insertion of an intramedullary pin (Figures 1 and 2).
Constructs
Implantsa were 11-hole, 8-mm locking plates manufactured from commercially pure grade-4 titanium and the associated locking screws. Plates were 2.5 mm thick and 8 mm wide; holes were at intervals of 9 mm. The 8-mm locking screws were made of TiAl6V4 titanium alloy; screws were self-tapping and had an outer diameter of 3.2 mm, core diameter of 2.4 mm, and thread pitch of 0.64 mm. Intramedullary pins were titanium Kirschner wiresb (1.8 × 150 mm).
Specimens
A cat femoral diaphyseal bone model was chosen for construct evaluation to minimize interspecimen variability. The femoral cortex model was cylinders of beechwood (outer diameter, 10 mm; inner diameter, 6 mm; and wall thickness, 2 mm). Each beechwood cylinder was 75 mm in length, and 50 mm at 1 end was filled with balsa wood, which mimicked cancellous bone. Cylinder dimensions were selected to approximate cat femurs, with an increased cortex thickness to compensate for slightly lower longitudinal modulus and strength of beechwood in comparison to characteristics of cortical bone.19 Two cylinders were aligned in a jig. A 10-mm spacer was placed between the cylinders, and the cylinders were held in position with bone clamps until the appropriate constructs were applied. The spacer was then removed, which resulted in the described plate construct with a 10-mm fracture gap.
For each plate, the central screw hole (hole 6) was placed directly over the fracture gap (Figure 1). The plate then was affixed with 4 self-tapping locking screws on each specimen, with 2 screws placed on each side of the fracture gap. All screws were applied in a monocortical manner and tightened to 1 N•m by use of a torque-limiting screwdriver. To ensure correct function of the locking mechanism, insertion of the screws perpendicular to the long axis of a cylinder was achieved by drilling screw holes by use of a dedicated locking screw sleeve. For construct A (screws far from the fracture gap), screws were placed in holes 1, 2, 10, and 11. For constructs B and C (screws near the fracture gap), screws were placed in holes 1, 5, 7, and 11. A Kirschner wire was inserted into each specimen of constructs A and B; diameter of the Kirschner wire was 30% the diameter of the mimicked medullary canal.
Mechanical testing
Constructs were tested to failure in each loading mode to determine strength and stiffness. Failure was defined as plastic deformation of the plate, which would result in malalignment of the bone in a clinical situation, or breakage of the bone model or plate. Finally, an intact model (solid beechwood rod [160 mm in length and 10 mm in diameter] with no fracture gap and no plate construct) was used to determine a baseline value for strength and stiffness.
Bending of the locking plate–rod and locking plate constructs was conducted on a material testing machine.c All 3 constructs were tested in a single cycle load to failure by use of a crosshead speed of 10 mm/min to the displacement limit of the bending fixture, which was 10 mm; this resulted in a cycle time of ≤ 1 minute. Thirty specimens (10 specimens/construct) were tested. Load was applied by use of 4-point bending to generate a constant bending moment over the entire plate length (Figure 3). The plate was located on the tension side of the bone, which resulted in gap closure. All samples were manually centered in the loading grips. The tested length (length of exposed specimen between loading grips) remained consistent among all specimens, and the tested length (103 mm) represented 64% of the total length of each specimen. The same number of specimens for each construct was tested in torsion. Crosshead speed for torsion tests was 100 mm/min; the pulley radius was 40 mm; thus, there was a torsion rate of 2.5 radians/min. Load-displacement behavior of each specimen was recorded, and slope of the linear region of the curve was defined as stiffness of the construct.
Performance of locking plate–rod and locking plate constructs was described by their bending and torsional yield strength, stiffness, and failure mechanism. Bending stiffness was expressed in terms of flexural rigidity.
Data analysis
Bending moment versus angular deformation curves were recorded for constructs A, B, and C. Yield strength in bending (or torsion) was defined as the bending (or torsion) moment needed to cause offset displacement of 0.2% for the bone plate construct. Construct failure was defined by catastrophic fracture or by a subsidence threshold at the fracture site, whichever occurred first. Subsidence represented a nonrecoverable collapse at the fracture site after load removal and was caused by bending or loosening of a plate. A threshold of 10 mm of crosshead movement in bending tests was deemed indicative of the onset of construct failure in the absence of catastrophic fracture. Values for hollow cylinders with an inner diameter of 6 mm were calculated by use of simple equations listed in a textbook.20
Data were reported as mean ± SD. Statistical analysis was performed with a Wilcoxon test. Primary analysis evaluated the effect of screw placement in a locking plate–rod construct (construct A vs construct B). We hypothesized that positioning the second screw near the fracture gap in each of the fragments would increase strength and stiffness of a construct. A secondary analysis was used to gauge the effect of an intramedullary pin (construct B vs construct C). Values were considered significant at P < 0.05.
Results
Bending
Bending moment at yield point, angle at yield point, and stiffness of each construct were determined (Table 1). Both bending moment and angle at yield point were significantly (P < 0.001) higher for construct A than for construct B. Stiffness was lower, but not significantly so, for construct A than for construct B (Figure 4). Construct C had a significantly (P = 0.002) lower bending moment at yield point and significantly (P < 0.001) lower stiffness than did construct B, but there was no significant difference in angle at yield point between these 2 constructs (Table 2). All plates sustained plastic deformation, but there was no plate breakage.
—Mean ± SD moment at yield, angle at yield, and stiffness of 3 constructs (10 specimens/construct for each testing mode) when tested by loading in bending and in torsion.
Load | Variable | Construct A | Construct B | Construct C |
---|---|---|---|---|
Bending | Moment at yield (N-m) | 3.03 ± 0.27 | 2.17 ± 0.33 | 1.67 ± 0.16 |
Angle at yield (radian) | 0.31 ± 0.02 | 0.21 ± 0.04 | 0.19 ± 0.02 | |
Stiffness (N-m/radian) | 9.92 ± 0.59 | 10.44 ± 0.73 | 8.87 ± 0.52 | |
Torsion | Moment at yield (N-m) | 0.81 ± 0.14 | 0.83 ± 0.14 | 0.79 ± 0.14 |
Angle at yield (radian) | 0.47 ± 0.12 | 0.56 ± 0.30 | 1.08 ± 0.51 | |
Stiffness (N-m/radian) | 1.76 ± 0.28 | 1.79 ± 0.63 | 1.75 ± 0.54 |
Hollow cylinders (outer diameter, 10 mm; inner diameter, 6 mm; and wall thickness, 2 mm) manufactured from beechwood were filled with balsa wood, which mimicked cancellous bone. Four screws were used for each construct. Two screws were inserted in the end holes of each plate (holes 1 and 11). The other 2 screws were inserted in holes 2 and 10 (construct A [far from the fracture gap]) or in holes 5 and 7 (constructs B and C [near the fracture gap]). An intramedullary pin was inserted into constructs A and B.
—Comparison of the difference in results between constructs win Table 1 when tested by loading in bending and in torsion.
Comparison | Load | Variable | Median | 95% CI | P value* |
---|---|---|---|---|---|
A vs B | Bending | Moment at yield (N-m) | 0.86 | 0.57 to 1.16 | < 0.001 |
Angle at yield (radian) | 0.10 | 0.07 to 0.14 | < 0.001 | ||
Stiffness (N-m/radian) | −0.37 | −1.07 to 0.20 | 0.185 | ||
Torsion | Moment at yield (N-m) | −0.04 | −0.18 to 0.12 | 0.570 | |
Angle at yield (radian) | 0.01 | −0.36 to 0.14 | 0.940 | ||
Stiffness (N-m/radian) | −0.10 | −0.54 to 0.60 | 0.734 | ||
B vs C | Bending | Moment at yield (N-m) | −0.51 | −0.78 to −0.25 | 0.002 |
Angle at yield (radian) | −0.02 | −0.05 to 0.02 | 0.424 | ||
Stiffness (N-m/radian) | −1.43 | −1.93 to −1.03 | < 0.001 | ||
Torsion | Moment at yield (N-m) | −0.02 | −0.22 to 0.07 | 0.495 | |
Angle at yield (radian) | 0.44 | 0.10 to 0.87 | 0.016 | ||
Stiffness (N-m/radian) | −0.02 | −0.65 to 0.61 | 0.910 |
< Values were considered significant at P < 0.05.
See Table 1 for remainder of key.
Failure of the plate construct was observed in 1 specimen for construct B as a fracture of the beechwood cylinder. The fracture occurred on the ipsilateral side of the wooden cylinder and started at the screw hole farthest from the fracture gap (Figure 5).
Torsion
There were no significant differences between constructs A and B for any of the 3 torsion variables (Figure 6). However, angle at yield in torsion differed significantly (P = 0.016) between constructs B and C.
Characteristics of a solid beechwood rod
Values were determined for the solid beechwood rod (Table 3).
—Mean ± SD results for a solid beechwood rod (160 mm in length and 10 mm in diameter) when tested by loading in bending and in torsion.
Variable | Bending | Torsion |
---|---|---|
Moment at yield (N-m) | 7.02 ± 2.22 | 1.51 ± 0.23 |
Angle at yield (radian) | 0.14 ± 0.03 | 0.29 ± 0.03 |
Stiffness (N-m/radian) | 52.21 ± 4.39 | 5.22 ± 0.78 |
Discussion
Plate-rod constructions have been successfully used to achieve adequate repositioning and stabilization of comminuted diaphyseal fractures in dogs and cats in a minimally invasive manner.11,12 With respect to the principles of biological osteosynthesis, indirect reduction techniques help minimize manipulation at the fracture site to prevent interference with the vascular supply. In clinical situations, a limited approach to the comminuted fracture zone may simplify insertion of a pin into the distal fragment; repositioning and adequate orientation of the main bone fragments are facilitated under visual control. The primary question of the investigation reported here was whether fixation of a plate to the bone near the fracture site would lead to increased stability of the locking plate–rod construct.
Disadvantages of disturbing the blood supply to a fracture site may be justified by improved stability of the construct as a result of fixation near the fracture. However, if screw insertion adjacent to a fracture lacks mechanical advantages over screw insertion at the plate ends, the decision to make additional incisions for screw placement should be considered with even more caution.
The primary purpose of the study reported here was to determine the effect of screw configuration on strength and stiffness of a locking plate–rod construct in a fracture gap model. The need to investigate an internal fixation system in a cat-sized fracture gap model stemmed from the fact that 8- and 9-mm plates would provide an ideal size for use in most long-bone fractures of cats. The locking plates were manufactured of titanium grade 4, and the screws were made of a titanium alloy,18 which would provide the advantage of materials with increased resistance to implant-related infections.21,22 Another potential benefit of a locked internal fixator would be minimization of the negative effect exerted on the underlying blood supply to the bone because the plate must not be pressed against the cortical bone surface to achieve force transmission.18,23
Yield strength and stiffness of the construct with the second screw placed near the fracture gap (construct B) were not higher in bending or torsion loading than for the construct with the second screw placed at the end of the plate (construct A), which did not support our hypothesis. In fact, contrary to our expectations, the bending moment was significantly higher for construct A than for construct B, whereas no significant differences in torsion were identified between these 2 constructs.
In a previous study,1 the screw was placed farther from the fracture site, which decreased axial stiffness.1 Investigators in another study24 found that the screw location significantly influenced fatigue life of a compression plate bone model construct. Increased tensile strains developing at the end of the screw hole nearest to the fracture gap may lead to plate failure through that screw hole.24
Results of the present study suggested that positioning the second screw nearer the fracture gap did not increase bending or torsional stiffness in the investigated locking plate–rod constructs. Combined with the fact that yield strength for construct A was significantly higher than the yield strength for construct B, the outcome implied that placement of a second locking screw farther from the fracture gap was the preferable choice. This conclusion would be valid as long as the plate is placed on the tension side of the bone, which is a universal principle of internal fixation. Conclusions drawn from the test results would not be true if the constructs were positioned differently. The study was designed to investigate a configuration set up to conform to standard principles of internal fixation. In clinical situations, whereby the plates would need to be placed on the compression side of a long bone, insertion of screws farther apart would definitely provide superior strength and stiffness in bending.
Furthermore, we found that the addition of an intramedullary pin resulted in a significant improvement of the bending strength of the locking plate construct, which is consistent with the findings of another study.11 Adding an intramedullary pin did not significantly affect strength or stiffness in torsion. In addition to a favorable effect on the biomechanical behavior of the locking plate construct, a major clinical advantage of intramedullary pin placement is ease of fracture reduction and limb alignment.11,12
The scenario of a diaphyseal fracture with a comminuted zone and lack of interfragmentary compression in a cat femur was simulated by the gap in the bone model. Relative stability and flexible fixation are required to enable interfragmentary motion and stimulate callus formation,13 which are acknowledged benefits of flexible fixation for promoting bone healing.14 Limited plate-to-bone contact preserves the periosteal blood supply and reduces osteoporosis underneath a plate.16 Low initial stiffness allows fracture-site motion in the early postoperative phase during reduced weight-bearing conditions.
The paradigm shift toward biological osteosynthesis promotes the use of bridge plating techniques for the treatment of nonreconstructable diaphyseal fractures. Bridge plating techniques emphasize biological priorities that rely on more flexible fracture fixation to promote secondary bone healing. With these techniques, relatively long bone plates are affixed with a limited number of screws to the ends of major fracture fragments and act as extramedullary splints.16 An increase in the plate length-to-fracture length ratio can reduce the load acting on the plate. Furthermore, a longer working length of the plate reduces screw loading; thus, fewer screws are needed for load transfer.10 Screw position should be chosen to diminish damage to the bone and to limit the amount of soft tissue dissection required. Previous guidelines of the Arbeitsgemeinschaft Osteosynthese (Association for the Study of Internal Fixation) for a specific screw number or a defined number of cortices engaged in each fragment should no longer be used as the only information concerning plate anchorage in MIPO.25 For simple fractures, it is recommended that screws not be inserted in 3 holes at the fracture zone to increase the system's elasticity and avoid excessive stress on the small part of the implant and possible premature breakage. Because comminuted fractures extend over a large distance, screws are generally spaced farther apart, yet they can still provide adequate stiffness without creating excessive stress on an implant.26
Compliance of a plate-bone construct is increased by increasing the plate working length and limiting the number of screws. The strength of fixation in locking plates is equal to the strength of all screw-bone interfaces, rather than that of a single screw's axial stiffness or pullout resistance.26 A single screw is difficult to pull out, unless several adjacent screws also pull out.
Stability is increased by the locking principle, especially in comminuted or highly unstable fractures. Fixation with 3 monocortical locked screws in a healthy bone is generally thought to be sufficient. There is practically no increase of stability with 4 screws/diaphyseal fragment.24 Use of monocortical screws is mainly indicated in the diaphysis of long bones, whereas bicortical screws should be used in metaphyseal and epiphyseal bone with thin cortices.26 In small bones, screw length must be carefully chosen so that a screw does not touch the transcortex, which may lead to stripping of the thread and loosening of the screw.
During 4-point bending tests in the present study, one of the specimens of construct B failed at both screws of one of the fragments. Locked screws combine to resist pullout,27 which results in typical patterns of failure seen for locking plate constructs: failure occurs at multiple screws concurrently or does not involve any of the screws. By placing the plate on the tension side of the bone, the screw located most distal from the gap fracture would be exposed to the highest stresses caused by bending load.28 This explains the observed initiation of fracture at the distally located screw in the construct B specimen during bending. In all other tests, the jig reached the limit of displacement, and the constructs were far past the yield point without failure of the screw-bone interface.
In vivo physiologic loading in many animal species has been reported.29–32 The universal finding in those studies was that bones under peak physiologic loading have a strain of 2,000 microstrains,32 as measured with strain gauges strategically applied to the surface of bones of numerous animals, which then were stimulated to perform maximum physiologic activity. In laboratory tests, bone can withstand peak tensile strain of approximately 6,000 microstrains. Thus, the single cycle failure of bone under physiologic loading has a safety factor of 3. Average strain for a common activity such as locomotion is 500 microstrains. Therefore, we tested intact beechwood rods (from which the corresponding values for cylinders can easily be calculated; these values for cylinders are generally only marginally lower) to provide a scale on which to place a construct's value. One could anticipate that for constructs stronger than about one-tenth that of intact bone, restriction to only average physiologic activity may provide a sufficient strength margin to allow for timely bone healing. As indicated by results of the present study, the best construct (construct A) was 43% that of an intact beechwood rod in bending and 54% in torsion. Thus, we would expect these constructs to provide a safe margin for strength during the healing period, even if unrestricted activity were allowed.
The present study had some limitations. In vivo factors such as bone resorption leading to screw loosening or callus development leading to plate protection were not addressed in this study. Results of the present study were limited to the use of surrogate specimens. Bone models were used to determine relative differences among constructs. Selection of a bone surrogate material for in vitro studies always results in compromises because there is no available material with the unique structure of bone with its collagen network and mineral matrix that has adequately characterized bone mechanical properties. Strength and stiffness of cortical bone along the longitudinal axis have been reasonably well simulated by fourth-generation glass-epoxy cylinders33,d; however, that material is isotropic, which is a major drawback considering that cortical bone anisotropy has lower stiffness and strength (factor of 3 and 10, respectively) in the transverse plane. A generally accepted range for the longitudinal modulus of elasticity of cortical bone is 15 to 20 GPa; the range for the transverse plane is one-half to one-third of the range for the longitudinal modulus. Tensile strength in tension and compression in the longitudinal direction is in the range of 100 to 200 MPa, whereas it is one-third to one-tenth of that range in the transverse plane.34 The fourth-generation glass-epoxy materiald is a rather new surrogate for bone. Previously, the most commonly used materials were polyoxymethylenee and cotton-reinforced phenolic resin.f Mechanical properties of polyoxymethylene,e with a strength and stiffness of 70 MPa and 3 GPa, respectively, are substantially inferior to those of cortical bone. In addition, polyoxymethylene is isotropic. Cotton-reinforced phenolic resinf is more characteristic of bone, with a typical tensile strength of 70 MPa and modulus of elasticity of 6.5 GPa. However, this material is also isotropic. Beechwood characteristics are within the range of cortical bone, but most importantly, it also has a high level of anisotropy. This anisotropy was a primary factor in the choice of beechwood for the study reported here.
A longitudinal tensile modulus of 14.5 GPa and compression modulus of 12.9 GPa have been reported for beechwood.19 Variability of beechwood with regard to species, origin, and moisture content has been the focus of many studies relevant to its use as a standard material in construction, but cortical bone is greatly influenced by even more factors. Clinical applications must deal with this variability. The key factor in the decision to use beechwood in the present study was that various constructs have been compared in both bending and torsion, and anisotropy could play an important role in how cylinders deform and fail. Thus, balsa wood was chosen as a model for cancellous bone.35–38 Trabecular bone has a broad range of strength and stiffness (strength, 0.03 to 15.6 MPa; modulus of uniaxial stress, 1.1 MPa to 9.8 GPa), and medium-grade balsa wood has mechanical properties within that range.36
Because beechwood and balsa wood are commonly available, inexpensive, and easily machined, we believed that their use in biomechanical experiments, especially those of a comparative nature, was justified, and studies to compare the properties of beechwood with those of cortical bone should be performed by experts in mechanical testing and materials science in better-equipped laboratories. Although cadaveric bone remains the ideal testing material, standardized implant application is complicated by wide interspecimen variation resulting from differences in size, breed, and conformation.
Locking plate constructs were evaluated in a femoral diaphyseal bone model, which accommodated locking screws in a cortical bone surrogate. This will not always be possible in clinical conditions when a plate spans the entire length of a bone, which would thus require placement of the screws in metaphyseal cancellous bone.
Furthermore, the locking plate–rod construct should only be used in adequately sized patients, which will allow monocortical screw insertion without touching an intramedullary pin. In extremely small cats, even the shortest screws can be too long to be inserted without interfering with an intramedullary pin. Pushing the screw tip against the intramedullary pin prevents an efficient locking mechanism and adequate screw purchase and therefore should be avoided. Shorter locking screws than those originally provided are currently available for 8- and 9-mm plates.
In the study reported here, positioning screws close to a fracture gap diminished resistance to bending loads, assuming that the plate was placed on the tension side of the simulated bone. Adding an intramedullary pin to a locking plate led to an increase in bending strength of the construct. Neither screw positioning nor the addition of an intramedullary pin had a significant effect on stiffness or strength in torsion.
Acknowledgments
Supported by Kyon AG.
The authors thank Daniela Hitz for technical assistance and Sabine Schädelin for performing the statistical analysis.
ABBREVIATION
MIPO | Minimally invasive plate osteosynthesis |
Footnotes
Advanced Locking Plate System, provided by Kyon AG, Zurich, Switzerland.
Synthes GmbH, Zuchwil, Switzerland.
Model Z2.5, Zwick/Roell, Ulm, Germany.
Sawbones, Pacific Research Laboratories Inc, Vashon Island, Wash.
Delrin, DuPont, Wilmington, Del.
Tufnol, Bay Plastics Ltd, North Shields, Northumberland, England.
References
1. Stoffel K, Dieter U, Stachowiak G, et al. Biomechanical testing of the LCP—how can stability in locked internal fixators be controlled? Injury 2003; 34 (suppl 2): B11–B19.
2. Palmer RH. Biological osteosynthesis. Vet Clin North Am Small Anim Pract 1999; 29: 1171–1185.
3. Perren SM. Physical and biological aspects of fracture healing with special reference to internal fixation. Clin Orthop 1979; 138: 175–196.
4. Gerber C, Mast JW, Ganz R. Biological internal fixation of fractures. Arch Orthop Trauma Surg 1990; 109: 295–303.
5. Johnson AL, Smith CW, Schaeffer DJ. Fragment reconstruction and bone plate fixation versus bridging plate fixation for treating highly comminuted femoral fractures in dogs: 35 cases (1987–1997). J Am Vet Med Assoc 1998; 213: 1157–1161.
6. Schemitsch EH, Kowalski MJ, Swiontkowski MF, et al. Comparison of the effect of reamed and unreamed locked intramedullary nailing on blood flow in the callus and strength of union following fracture of the sheep tibia. J Orthop Res 1995; 13: 382–389.
7. Hulse D, Ferry K, Fawcett A, et al. Effect of intramedullary pin size on reducing bone plate strain. Vet Comp Orthop Traumatol 2000; 13: 185–190.
8. Mizuno K, Mineo K, Tachibana T, et al. The osteogenetic potential of fracture hematoma. Subperiosteal and intramuscular transplantation of the haematoma. J Bone Joint Surg Br 1990; 72: 822–829.
9. Broos PL, Sermon A. From unstable internal fixation to biological osteosynthesis. A historical overview of operative fracture treatment. Acta Chir Belg 2004; 104: 396–400.
10. Gautier E, Sommer C. Guidelines for the clinical application of the LCP. Injury 2003; 34 (suppl 2): B63–B76.
11. Hulse D, Hyman W, Nori M, et al. Reduction in plate strain by addition of an intramedullary pin. Vet Surg 1997; 26: 451–459.
12. Reems MR, Beale BS, Hulse DA. Use of a plate-rod construct and principles of biological osteosynthesis for repair of diaphyseal fractures in dogs and cats: 47 cases (1994–2001). J Am Vet Med Assoc 2003; 223: 330–335.
13. Bottlang M, Doornink J, Fitzpatrick D, et al. Far cortical locking can reduce stiffness of locked plating constructs while retaining construct strength. J Bone Joint Surg Am 2009; 91: 1985–1994.
14. Guiot LP, Déjardin LM. Prospective evaluation of minimally invasive plate osteosynthesis in 36 nonarticular tibial fractures in dogs and cats. Vet Surg 2011; 40: 171–182.
15. Hudson CC, Pozzi A, Lewis DD. Minimally invasive plate osteosynthesis: applications and techniques in dogs and cats. Vet Comp Orthop Traumatol 2009; 22: 175–182.
16. Perren SM. Evolution of the internal fixation of long bone fractures. The scientific basis of biological internal fixation: choosing a new balance between stability and biology. J Bone Joint Surg Br 2002; 84: 1093–1110.
17. Maxwell M, Horstman CL, Crawford RL, et al. The effects of screw placement on plate strain in 3.5 mm dynamic compression plates and limited-contact dynamic compression plates. Vet Comp Orthop Traumatol 2009; 22: 125–131.
18. Guerrero TG, Kalchofner K, Scherrer N, et al. The advanced locking plate system (ALPS): a retrospective evaluation in 71 small animal patients. Vet Surg 2014; 43: 127–135.
19. Ozyhar T, Hering S, Niemz P. Moisture-dependent orthotropic tension-compression asymmetry of wood. Holzforschung 2013; 67: 395–404.
20. Young WC, Budynas RG. Appendix A. Properties of a plane area. In: Young WC, Budynas RG, eds. Roark's formulas for stress and strain. 7th ed. New York: McGraw-Hill Co, 2001; 799–812.
21. Arens S, Schlegel U, Printzen G, et al. Influence of materials for fixation implants on local infection. An experimental study of steel versus titanium DCP in rabbits. J Bone Joint Surg Br 1996; 78: 647–651.
22. Uhthoff HK, Bardos DI, Liskova-Kiar M. The advantages of titanium alloy over stainless steel plates for the internal fixation of fractures. An experimental study in dogs. J Bone Joint Surg Br 1981; 63-B:427–484.
23. Tepic S, Perren SM. The biomechanics of the PC-Fix internal fixator. Injury 1995; 26 (suppl 2): B5–B10.
24. Hammel SP, Elizabeth Pluhar G, Novo RE, et al. Fatigue analysis of plates used for fracture stabilization in small dogs and cats. Vet Surg 2006; 35: 573–578.
25. Apivatthakakul T, Chiewcharntanakit S. Minimally invasive plate osteosynthesis (MIPO) in the treatment of the femoral shaft fracture where intramedullary nailing is not indicated. Int Orthop 2009; 33: 1119–1126.
26. Cronier P, Pietu G, Dujardin C, et al. The concept of locking plates. Orthop Traumatol Surg Res 2010; 96 (suppl): S17–S36.
27. Cordey J, Borgeaud M, Perren SM. Force transfer between the plate and the bone: relative importance of the bending stiffness of the screws and the friction between plate and bone. Injury 2000; 31 (suppl 3): C21–C28.
28. Egol KA, Kubiak EN, Fulkerson E, et al. Biomechanics of locked plates and screws. J Orthop Trauma 2004; 18: 488–493.
29. Rubin CT, Lanyon LE. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol 1982; 101: 187–211.
30. Carter DR, Smith DJ, Spengler DM, et al. Measurement and analysis of in vivo bone strains on the canine radius and ulna. J Biomech 1980; 13: 27–38.
31. Fritton SP, Kenneth JM, Clinton TR. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech 2000; 33: 317–325.
32. Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J Theor Biol 1984; 107: 321–327.
33. Sawbones. Short-fiber-filled epoxy cylinders. Typical properties. Available at: www.sawbones.com/UserFiles/Docs/biomechanical_catalog.pdf. Accessed April 15, 2015.
34. Wirtz DC, Schiffers N, Pandorf T, et al. Critical evaluation of known bone material properties to realize anisotropic FE-simulation of the proximal femur. J Biomech 2000; 33: 1325–1330.
35. Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech 1987; 20: 1055–1061.
36. Auszac Eco Balsa. Balsa wood properties guide. Available at: www.auszac.com/factsheets.html. Accessed Feb 23, 2014.
37. Da Silva A, Kyriakides S. Compressive response and failure of balsa wood. Int J Solids Struct 2007; 44: 8685–8717.
38. Currey JD. The mechanical properties of bone. Clin Orthop Relat Res 1970; 73: 210–231.