Biomechanical assessment of the effects of vertebral distraction-fusion techniques on the adjacent segment of canine cervical vertebrae

Takaharu Hakozaki Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan.

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Tomu Ichinohe Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan.

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Nobuo Kanno Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan.

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Takuya Yogo Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan.

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Yasuji Harada Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan.

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Tadashi Inaba Department of Mechanical Engineering, Graduate School of Engineering, Mie University, Tsu, Mie 514-8507, Japan.

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Yuichi Kasai Department of Spinal Surgery and Medical Engineering, Graduate School of Medicine, Mie University, Tsu, Mie 514-8507, Japan.

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Yasushi Hara Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan.

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Abstract

OBJECTIVE To assess effects of vertebral distraction-fusion techniques at a treated segment (C5-C6) and an adjacent segment (C4-C5) of canine cervical vertebrae.

SAMPLE Cervical vertebrae harvested from cadavers of 10 skeletally mature Beagles.

PROCEDURES Three models (intact, titanium plate, and polymethylmethacrylate [PM MA]) for stabilization of the caudal region of the cervical vertebrae (C4 through C7) were applied to the C5-C6 vertebral segment sequentially on the same specimens. Biomechanical assessments with flexion-extension, lateral bending, and axial rotational tests were conducted after each procedure. Range of motion (ROM) for a torque load applied with a 6-axis material tester was measured at C4-5 and C5-6 and calculated by use of a 3-D video measurement system.

RESULTS In both the plate and PMMA models, ROM significantly increased at C4-5 and significantly decreased at C5-6, compared with results for the intact model. The ROM at C5-6 was significantly lower for the plate model versus the PMMA model in lateral bending and for the PMMA model versus the plate model in axial rotation. Conversely, ROM at C4-5 was significantly higher in axial rotation for the PMMA model versus the plate model. No significant differences were identified in flexion-extension between the PMMA and plate models at either site.

CONCLUSIONS AND CLINICAL RELEVANCE Results of this study suggested that vertebral distraction and fusion of canine vertebrae can change the mechanical environment at, and may cause disorders in, the adjacent segment. Additionally, findings suggested that effects on the adjacent segment differed on the basis of the fusion method used.

Abstract

OBJECTIVE To assess effects of vertebral distraction-fusion techniques at a treated segment (C5-C6) and an adjacent segment (C4-C5) of canine cervical vertebrae.

SAMPLE Cervical vertebrae harvested from cadavers of 10 skeletally mature Beagles.

PROCEDURES Three models (intact, titanium plate, and polymethylmethacrylate [PM MA]) for stabilization of the caudal region of the cervical vertebrae (C4 through C7) were applied to the C5-C6 vertebral segment sequentially on the same specimens. Biomechanical assessments with flexion-extension, lateral bending, and axial rotational tests were conducted after each procedure. Range of motion (ROM) for a torque load applied with a 6-axis material tester was measured at C4-5 and C5-6 and calculated by use of a 3-D video measurement system.

RESULTS In both the plate and PMMA models, ROM significantly increased at C4-5 and significantly decreased at C5-6, compared with results for the intact model. The ROM at C5-6 was significantly lower for the plate model versus the PMMA model in lateral bending and for the PMMA model versus the plate model in axial rotation. Conversely, ROM at C4-5 was significantly higher in axial rotation for the PMMA model versus the plate model. No significant differences were identified in flexion-extension between the PMMA and plate models at either site.

CONCLUSIONS AND CLINICAL RELEVANCE Results of this study suggested that vertebral distraction and fusion of canine vertebrae can change the mechanical environment at, and may cause disorders in, the adjacent segment. Additionally, findings suggested that effects on the adjacent segment differed on the basis of the fusion method used.

Cervical intervertebral disk herniation and caudal cervical spondylotic myelopathy are commonly diagnosed neurosurgical disorders of the caudal region of the cervical vertebrae of dogs. Clinically, ventral slot decompression or a distraction-fusion method has been used as a treatment for cervical intervertebral disk herniation and caudal cervical spondylotic myelopathy, depending on the nature of the spinal cord compression (dynamic or static) of each patient.1 Although postoperative instability and subluxation are serious complications of ventral slot decompression, these complications are considered preventable by combining ventral slot decompression with a distraction-fusion technique.1,2

Typically, for lesions in the caudal region of the cervical vertebrae in which the slot width after ventral slot decompression is close to 50% of the vertebral body width, use of a distraction-fusion technique should be considered.2 However, use of a distraction-fusion technique can lead to similar lesions in the adjacent intervertebral disk space (so-called domino lesions).3 Clinical signs secondary to domino lesions have been reported for approximately 20% of dogs during the first 6 months to 4 years after surgery.4–7

In a biomechanical evaluation that involved the use of human cervical vertebrae, the intradisk pressures and segmental motion of the adjacent segment increased after use of a distraction-fusion technique.8,9 Additionally, an increase in movement has also been observed radiographically at the proximal and distal intervertebral spaces of the affixed segment in clinical studies.10,11 However, the effect of ventral slot decompression or a distraction-fusion technique on mobility of the adjacent intervertebral spaces has not been sufficiently studied in veterinary medicine.

In particular, with respect to distraction and fusion of the canine cervical vertebrae, various fixation methods that involve use of a metallic implant and PMMA or a plate with a locking system have been reported.12–15 However, only limited information is available on the biomechanics of the fixation method involving a plate with a locking system,16 and no study has yet been conducted to compare effects on the adjacent segments for a plate with a locking system with effects on the adjacent segments for other methods of fixation in dogs.

The purpose of the study reported here was to investigate the effects of a distraction-fusion technique on a treated segment (measured at C5-6) and an adjacent segment (measured at C4-5) of the canine cervical vertebrae. We hypothesized that the fixation strength by use of a plate with a locking system would be higher than that by use of metal implants and PMMA.

Materials and Methods

Sample

Vertebrae (C1 through T3) were harvested from the cadavers of 10 skeletally mature male Beagles. Dogs were 1 to 2 years old and had a mean body weight of 11.2 kg (range, 8.6 to 14.2 kg). They had been used in an undergraduate surgical laboratory and were euthanized by IV administration of pentobarbital at the end of the laboratory. Use of the dogs in the surgical laboratory and the procedures for euthanasia and sample collection were approved by the Animal Care and Use Committee of Nippon Veterinary and Life Science University.

Sample preparation

Computed tomographya and MRIb images of all vertebral specimens were obtained and used to evaluate vertebral morphology and intervertebral disk hydration. Then, 3-D CT reconstruction images were used to exclude vertebrae with fractures or deformities. Sagittal T2-weighted MRI images were used to exclude nucleus pulposus tissues with low signal intensities, as determined by use of the Pfirrmann grading system.17 The caudal region of the cervical vertebrae (C4 through C7) was denuded of all musculature, but the vertebral ligaments and facet joint capsules were allowed to remain intact. Specimens were subsequently wrapped in saline (0.9% NaCl) solution–soaked towels. Specimens were stored at −20°C and thawed for 12 hours at 4°C before testing. The most cranial vertebra (C4) and most caudal vertebrae (C6 and C7) were fixed on a mounting jig by use of dental resin.c To evaluate effects on the adjacent segment after distraction and fusion, 2 intervertebral spaces of the specimen were used: C4-5 for the adjacent segment and C5-6 for the treated segment.

Testing device

A 6-axis material tester was used as the biomechanical testing device (Figure 1).18,19 The testing device was equipped with a 6-axis force sensor at the end point, which allowed detection of forces along the X-, y-, and z-axes and detection of torques around each axis. The device also enabled regulation of the force or torque via feedback of detected values into the control system.

Figure 1—
Figure 1—

Photograph of a 6-axis material tester and a specimen of the cervical vertebrae obtained from a canine cadaver. The most cranial vertebra (C4) and caudal vertebrae (C6 and C7) were fixed on a mounting jig by use of dental resin.

Citation: American Journal of Veterinary Research 77, 11; 10.2460/ajvr.77.11.1194

Testing procedures

Three procedures (models) were applied sequentially on each specimen. The procedures in order of use were untreated (intact model), fixed by use of a titanium plate (plate model), and fixed by use of a metal implant and PMMA (PMMA model). The ROM was tested after each procedure (Figure 2).

Figure 2—
Figure 2—

Photographs of an untreated CS-C6 vertebral segment (intact model; A), the CS-C6 segment stabilized by use of a titanium plate system (plate model; B), and the CS-C6 segment stabilized by use of a metal implant and PMMA (PMMA model; C). The models were applied sequentially (intact model, then the plate model, and finally the PMMA model) to each vertebral specimen.

Citation: American Journal of Veterinary Research 77, 11; 10.2460/ajvr.77.11.1194

No further procedures were performed on the intact model. For the plate model, a commercially available titanium plate systemd was applied for fixation. The plate was 2.0 mm thick and was cut into a 5-hole plate (total length, 40 mm) before application. The screws were 2.4 mm in diameter, with a length of 10 to 14 mm, depending on the size of the specimen. First, a specialized drill sleeve was set in the most cranial screw hole of the plate, which was located on C5. A hole was drilled in both sides of the cortical bone of the vertebral body by use of a drill bit with a diameter of 1.8 mm, and the screws were placed. Subsequently, a screw was installed in the most caudal screw hole of the plate, which was located on C6. The center hole of the plate was left empty, but 2 screws were placed in each of C5 and C6 for bicortical fixation. The screws were placed on the left and right ventral sides of the vertebral body and were used to stabilize the C5-C6 vertebral segment (Figure 3).

Figure 3—
Figure 3—

Representative lateral radiographic views showing fixation of C5-C6 by use of a titanium plate model (A) and a PMMA model (B). For the plate model, 2 plates were placed on the left and right ventral sides of the vertebral body and used to stabilize the CS-C6 vertebral segment. For the PMMA model, 2 anchor screws were placed parallel to each other (one in C5 and the other in C6), with 10 mm of each screw exposed on the ventral side of the vertebral body; screw heads were then completely covered with PMMA, and the C5-C6 vertebral segment was fixed in position.

Citation: American Journal of Veterinary Research 77, 11; 10.2460/ajvr.77.11.1194

For the PMMA model, a metal implant and PMMA were used for fixation. The metal implant comprised a cortical bone screwe (2.7 mm in diameter and 20 mm in length), and the PMMA consisted of 10 g of dental resin.c Two anchor screws were placed parallel to each other (one in C5 and the other in C6), with 10 mm of each screw exposed on the ventral side of the vertebral body. Screw heads were then completely covered with PMMA, and the C5-C6 vertebral segment was fixed in position (Figure 3). For both the PMMA and plate models, the intervertebral disk at the site of fixation was not treated.

Test conditions

Each of the 3 models was subjected to bending and rotational tests, and the maximum ROM under torque load was measured. Conditions of the bending test included 3 degrees of freedom and angular velocity at 0.30°/s. The 3 degrees of freedom condition was defined as the state that restrained translational motion in the X- and y-axes and rotational motion around the z-axis while it allowed rotational motion around the X- and y-axes and translational motion in the z-axis. The angle was defined as the maximum bending angle under a torque load of 1 N•m in the flexion-extension direction or 2 N•m in the left-to-right lateral direction. Conditions of the rotational test included 4 degrees of freedom and an angular velocity at 0.30°/s. The 4 degrees of freedom condition was defined as the rotation around the z-axis under the state that allowed translational motion in the X-, y-, and z-axes while it restrained rotational motion around the X- and y-axes. The angle was defined as the maximum bending angle under a torque load of 5 N•m in both the left and right axial rotation directions. Both the bending and rotational tests were performed 3 times, and only the result of the third repetition of each test was used for analysis.19

3-D video measurement system

For each test, ROMs for the treated segment (C5-C6) and adjacent segment (C4-C5) were calculated by use of a 3-D video measurement system.19 The procedure for analysis by use of the 3-D video measurement system involved placing markers on the jig and specimen. Two video cameras were placed at predetermined positions and used to record the test. Video data were uploaded to a personal computer and converted to a binary code by measurement software.f Relative angles were measured at C4-5 and C5-6 by tracking the markers.

Posttesting assessment

After all tests were completed, CT was performed to assess for bone failure resulting from the mechanical testing and for penetration of the intervertebral disk space during drilling. If either of these conditions were found, data for the specimen were excluded from the analysis.

Statistical analysis

Data were analyzed by use of analytic software.g All continuous data were tested by use of the Shapiro-Wilk test to determine whether they had a normal distribution. An ANOVA followed by the Tukey-Kramer test was used to compare parametric data between the ROMs of each model for the 2 segments. Paired t tests and the Wilcoxon signed rank test were used to compare parametric and nonparametric data, respectively, between the ROMs at C4-5 and C5-6 for the 3 models. For all tests, values of P < 0.05 were considered significant.

Results

Bending test

The ROM of each model and intervertebral space was determined for the bending test (Figure 4). At C4-5, the mean ± SD ROM for flexion and extension was significantly higher for the plate (27.8 ± 5.0°; P = 0.002) and PMMA (25.5 ± 2.1°; P = 0.04) models, compared with the mean for the intact model (19.4 ± 2.3°); values did not differ significantly (P = 0.295) between the plate and PMMA models. At C5-6, mean ± SD ROM for flexion and extension was significantly (P < 0.001) lower for the plate (7.8 ± 1.7°) and PMMA (9.6 ± 1.4°) models, compared with the value for the intact model (22.0 ± 2.3°); values did not differ significantly (P = 0.374) between the plate and PMMA models. There was no significant difference between the ROM at C4-5 and C5-6 for the intact model during flexion and extension.

Figure 4—
Figure 4—

Mean ± SD values of ROM for the intact (black bars), plate (dark gray bars), and PMMA (light gray bars) models described In Figures 2 and 3 for intervertebral spaces for bending in flexion and extension (A), lateral bending in the left and right direction (B), and axial rotation in the left and right direction (C). Values represent results for 6 specimens; C5-C6 Is the treated segment, and C4-CS is the adjacent segment. Notice that the scale on the y-axis differs among panels. *Within a segment, value differs significantly (P < 0.05) from the value for the intact model. †Within a segment, value differs significantly (P < 0.05) from the value for the plate model. ‡Within a model, value differs significantly (P < 0.05) from the value for the C5-6 segment. See Figures 2 and 3 for remainder of key.

Citation: American Journal of Veterinary Research 77, 11; 10.2460/ajvr.77.11.1194

At C4-5, the mean ± SD ROM in the left and right lateral direction was significantly (P < 0.001) higher for the plate (22.9 ± 1.1°) and PMMA (21.6 ± 2.0°) models, compared with the value for the intact model (15.6 ± 2.0°); values did not differ significantly (P = 0.470) between the plate and PMMA models. At C5-6, the mean ± SD ROM in the left and right lateral direction was significantly (P < 0.001) lower for the plate (3.2 ± 1.2°) and PMMA (8.0 ± 2.0°) models, compared with the value for the intact model (14.3 ± 2.8°). Furthermore, the mean ROM for the plate model was significantly (P = 0.004) less than that for the PMMA model. There was no significant difference between the ROM at C4-5 and C5-6 for the intact model during left and right lateral bending.

Rotational test

The ROMs for each model and intervertebral space were determined for the rotational test (Figure 4). At C4-5, the mean ± SD ROM for axial rotation in the left and right lateral direction was significantly (P < 0.001) higher for the plate (9.5 ± 1.4°) and PMMA (12.5 ± 2.4°) models, compared with the value for the intact model (4.2 ± 2.6°). Furthermore, the mean ROM for the PMMA model was significantly (P = 0.030) greater than that for the plate model. At C5-6 for axial rotation in the left and right direction, the mean ± SD ROM was significantly (P < 0.001) lower for the plate (10.0 ± 1.0°) and PMMA (6.8 ± 1.0°) models, compared with the value for the intact model (16.8 ± 2.3°). Furthermore, the mean ROM for the PMMA model was significantly (P = 0.001) less than that for the plate model. For the intact model during axial rotation, C4-5 had a ROM that was significantly (P < 0.001) less than the ROM for C5-6.

Posttesting assessment

All vertebral specimens were assessed by use of CT after testing. None of the specimens had evidence of bone fracture or penetration into the disk space.

Discussion

Results of the study reported here indicated that the ROM of the adjacent segment (C4-C5) of canine cervical vertebrae increased significantly for the PMMA and plate models, compared with that for the intact model. Additionally, results indicated that the ROM of the treated segment (C5-C6) was significantly decreased for both the PMMA and plate models, compared with that for the intact model. This was likely attributable to the fact that the adjacent segment compensated for the ROM lost by fixation of the treated segment. In the present study, the ROM of the adjacent segment (C4-C5) during flexion and extension was increased by 5.3°, which was almost an identical result to that in a previous report.20 On the other hand, reduction of the ROM has also been observed for a method involving use of a locking compression plate as the fixation device.21 Plate fixation in the caudal region of the cervical vertebrae has also been reported for clinical cases.13,14 However, to the authors’ knowledge, no studies have been conducted to evaluate the mobility of the intervertebral portion when 2 plates are placed parallel in the vertebral body, as for the plate model in the present study.

Use of the plate model resulted in a decrease in ROM during flexion and extension as well as during lateral bending and axial rotation. However, in a biomechanical study9 involving disease in an adjacent segment in humans, fixation of C5-C6 with a plate increased intradisk pressure and ROM at C4-5 and C6-7, and investigators suggested the possibility of the involvement of the plate in early disk degeneration was suggested. In the study reported here, results suggested that the increased ROM for the adjacent segment during plate fixation may result in early disk degeneration.

Furthermore, only for the intact model during axial rotation did C4-5 have an ROM that was significantly less than the ROM for C5-6. Investigators in 1 study22 reported that the ROM at C4-5 was 1.1° for left-to-right axial rotation under a torque load of 1 N•m. In another study,23 investigators compared the ROM of the cranial and caudal sites of the cervical vertebrae in dogs and reported that the caudal site had up to 2.6 times as much rotational ability as did the cranial site. In the present study, results suggested that the ROM at C4-5 was less than that at C5-6 and that there was a greater tendency for rotation in the caudal region of the cervical vertebrae than in the cranial region.

Comparison of the results for fixation of C5-C6 in the PMMA and plate models revealed that stronger fixation occurred with the PMMA model during axial rotation and with the plate model during bending. In addition, results indicated that the difference in fixation strength of the treated segment was affecting the ROM of the adjacent segment. These differences were considered to have been caused by the fixation devices of the plate and PMMA models. For the rotational test, the 2 plates placed in the vertebral body were functioning as an independent fixation device for the plate model, but the screws for the PMMA model were placed at the left and right sides of the vertebral body and were cross-linked by PMMA, which created a single fixation device. Therefore, mobility was likely limited with the PMMA model, and accordingly, the ROM was decreased.

Furthermore, the ROM of the PMMA model was possibly influenced by the amount of PMMA used. For a fixation method that involves the use of a metal implant and PMMA, the amount of PMMA that can completely cover the exposed metal implant is assumed to be sufficient.24 However, there has been no report on differences in fixation strength attributable to differences in the amount of PMMA. As a result of standardizing the amount of PMMA to 10 g in the present study, the ROM was reduced. However, whether it was a suitable amount of PMMA for performing the distraction-fusion technique is unknown. A need exists for additional studies in this area.

The present study had some limitations. First, it should be mentioned that all soft tissues had been removed from the specimens used in the study, with only the vertebrae, intervertebral disks, joint capsule, and major ligaments remaining. Moreover, bending and rotational tests were conducted separately. Because these movements occured in complex combinations in the cervical vertebrae of dogs, it was assumed that accurate mobility was not recreated in this study. Second, possible differences in the placement of the metallic implants in the fixation model may have affected fixation strength. Additional studies involving models with different placements of implants are necessary. Third, for the PMMA model of the present study, the screws were placed bicortically, whereas in a clinically affected dog, such placement of screws would carry a risk of spinal cord injury. Finally, the intervertebral disks used in this study were unaltered. Because the goal of distraction-fusion techniques is fusion of the vertebral segments, it is common to perform a treatment on the disk and disk space.4,13,15 Therefore, our findings might differ from clinical results achieved with a vertebral distraction-fusion technique.

To our knowledge, although biomechanical studies involving the use of fixation methods with plates or pins and PMMA have been conducted on the cervical vertebrae of dogs, no reports exist of studies involving comparison of different fixation methods and assessment of the effects on the adjacent segments of the same specimen. In the present study, results suggested that the distraction-fusion technique can change the mechanical environment of the adjacent segment and may cause disease in that segment. Additionally, results suggested that differences in fixation strength of the treated segment affected the ROM of the adjacent segment, which may be important for selecting the appropriate surgical procedure for fusion and for evaluating the effects on the adjacent segment after surgery.

ABBREVIATIONS

PMMA

Polymethylmethacrylate

ROM

Range of motion

Footnotes

a.

Aquilion Prime, Toshiba Medical Systems Corp, Tochigi, Japan.

b.

Signa Excite 3.0-T, GE Healthcare Japan Corp, Tokyo, Japan.

c.

Ostron II, GC Co Ltd, Tokyo, Japan.

d.

MatrixMANDIBLE System, DePuy Synthes Japan VET, Tokyo, Japan.

e.

Cortical bone screw, Mizuho Medical Co Ltd, Tokyo, Japan.

f.

Move-tr/3D, Library Co Ltd, Tokyo, Japan.

g.

SPSS for Windows, version 16.0, SPSS Inc, Chicago, Ill.

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