SPINE Volume 39, Number 8, pp E508-E513 ©2014, Lippincott Williams & Wilkins
CERVICAL SPINE
Morphological Characteristics of Cervical Spine in Patients With Athetoid Cerebral Palsy and the Accuracy of Pedicle Screw Placement So Kato, MD,* Naoki Shoda, MD,* Hirotaka Chikuda, MD, PhD,* Atsushi Seichi, MD,† and Katsushi Takeshita, MD, PhD*
Study Design. A retrospective study. Objective. To investigate the morphology of the cervical spine in patients with athetoid cerebral palsy (CP), and to evaluate its relationship with the breach of cervical pedicle screws. Summary of Background Data. Cervical pedicle screws have been increasingly used in surgery for patients with CP, but screw misplacement is not uncommon. Although the altered morphology of the cervical spine in patients with CP may result in this high breach rate, few studies have examined the cervical pedicle profile. Methods. We retrospectively analyzed 31 patients with cervical myelopathy with CP, as well as 30 patients with cervical spondylotic myelopathy (CSM), who underwent posterior decompression surgery. The pedicle outer diameter, inner diameter, transverse angle and lateral mass deformity were investigated by obtaining preoperative computed tomographic scans. The accuracy of the placement of 56 pedicle screws used in fusion surgery for 12 patients with CP was also analyzed using postoperative computed tomographic scans. Results. The outer diameter of the pedicle in CP was in the range from 3.3 to 9.6 mm, and was larger than that in CSM at all cervical levels except for C7. Pedicle sclerosis was more frequently observed in CP than in CSM (23% vs. 7.3%, P < 0.001). The transverse angle at C3 and C4 was larger, and lateral mass deformity was more frequently observed in CP than in CSM. The critical breach of pedicle screws in CP was found in 29%. A multivariate analysis revealed that pedicle sclerosis was associated with an increased risk of breach (odds ratio: 6.3; 95% confidence interval: 1.03–39.0; P = 0.047). From the *Department of Orthopaedic Surgery, Sensory and Motor System Medicine, Surgical Sciences, Graduate School of Medicine, the University of Tokyo, Tokyo, Japan; and †Department of Orthopaedics, Jichi Medical University, Shimotsuke, Japan. Acknowledgment date: July 31, 2013. Revision date: November 13, 2013. Acceptance date: January 9, 2014. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to So Kato, MD, Department of Orthopaedic Surgery, Sensory and Motor System Medicine, Surgical Sciences, Graduate School of Medicine, the University of Tokyo, 7-3-1 Hongo Bunkyoku, Tokyo 113-8655, Japan; E-mail: [email protected] DOI: 10.1097/BRS.0000000000000234
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Conclusion. The pedicle diameter in patients with CP was relatively large, but pedicle sclerosis, a wide transverse angle and lateral mass deformity were frequently observed. Sclerotic pedicles were associated with a higher risk of critical breach. Key words: morphology, computed tomography, cervical spine, cerebral palsy, degeneration, myelopathy, pedicle screw, accuracy, breach rate, fusion. Level of Evidence: N/A Spine 2014;39:E508–E513
A
thetoid cerebral palsy (CP) is a common movement disorder caused by neonatal hypoxia that damages the basal ganglia, and it is characterized by involuntary movement and posture abnormalities. Patients with CP often show extensive spondylosis of the cervical spine in their early middle age caused by repetitive involuntary movements of the neck. Accelerated degeneration and continuous motion in the cervical spine eventually result in compressive myelopathy, which further complicates the patients’ already compromised neurological function and severely limits their autonomy.1,2 Once myelopathy has developed in patients with CP, it usually progresses with conservative treatment and requires surgical intervention. Although the optimal surgical treatment of cervical myelopathy in patients with CP remains to be established, decompression and fusion are often used to minimize the dynamic factors and prevent further instability of the cervical spine, especially in those with extensive involuntary movements or failed previous decompressive surgery.3–12 Cervical spinal fusion in patients with CP remains a clinical challenge. Instrumentation failure has been common with conventional wire and rod constructs.4,6 Pedicle screws are currently considered to be the most reliable anchor, because they provide stronger fixation than lateral mass screws13,14; however, cervical pedicle screw placement is technically demanding, and also poses a risk of neurovascular damage. Although the use of cervical pedicle screws in patients with CP has been increasingly reported in the literature,11,12,15–19 the results are not necessarily encouraging: a high rate of misplacement has been reported, which is presumably attributable to the
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extensive spondylosis and altered morphology of the spine in these patients.17,18 Although a better understanding of the morphological characteristics of the cervical spine in patients with CP would help surgeons to perform safer and more accurate surgery, no previous study specifically discussed the cervical pedicle profiles in patients with athetoid CP. The objective of this study was to investigate the morphological features of the cervical spine in patients with CP, focusing on the pedicle profiles in comparison with those of patients with cervical spondylotic myelopathy, and its relationship with the breach of pedicle screws.
MATERIALS AND METHODS Study Subjects We retrospectively reviewed our records of the patients with CP who had received posterior decompression surgery for cervical compressive myelopathy due to subaxial lesion between 2001 and 2011. Those with upper cervical lesions alone who underwent O–C2 or C1–C2 decompression and fusion were excluded from the analysis. We have historically used cervical laminoplasty for decompression,20,21 but currently limit its indication to those with minimal instability and mild involuntary movement. In terms of the fixation technique, we have selected posterior pedicle screws for rigid fixation. Pedicle screws of 4.0 mm in diameter were inserted using the guidance of a computed tomographic (CT) navigation system (StealthStation; Medtronic Inc., Minneapolis, MN).22,23 We obtained preoperative CT scans of the cervical spine with a 1.25-mm slice thickness. A surgical plan was devised on the computer work station using reconstructed 2- and 3-dimensional images. Intraoperatively, the reference frame was attached to the relevant spinous process of the vertebra. After matching the intraoperative anatomy and the imaging anatomy, the screw entrance holes were made using an air drill and deepened by a pedicle probe according to the planned screw trajectory under navigation system guidance, and the screws were inserted under fluoroscopy. If the relevant spinous process was not available for the reference frame attachment because of massive deformity or previous splitting by laminoplasty, we attached the reference frame to the adjacent vertebra. The spinal level to be fused was determined by the senior surgeons for each patient.
Imaging Analysis We identified 31 eligible patients with CP, and created reconstructed cross-sectional surfaces at 1-mm intervals from preoperative CT scans using the DICOM viewer (INTAGE Realia Pro; Cybernet Systems Co., Ltd., Tokyo, Japan). On the surfaces that passed the axes of bilateral pedicles, the pedicle outer diameter, inner diameter, and pedicle transverse angle of both pedicles in C3 to C7 were measured (Figure 1). All parameters were measured using the uniformed window level and width that were appropriate for the bony structure analysis (window level: 200, window width: 2000). We checked for the presence Spine
Figure 1. A schematic diagram of the pedicle parameters measured on CT scans (a, outer diameter; b, inner diameter; c, transverse angle). CT indicates computed tomography.
of pedicle sclerosis, which was defined as an inner diameter less than 2.0 mm.16 The pedicle transverse angle was defined as the angle formed by the vertebral midline and the pedicle axis, and we also checked the prevalence of vertebrae with a transverse angle larger than 55.0°.24 The presence of a lateral mass deformity was also investigated, considering that right and left asymmetry can cause a loss of anatomical landmarks that interferes with the estimation of the screw insertion point and angle. We defined a lateral mass with a thickness more than 2.0 mm thicker than the contralateral side as a deformed lateral mass. For comparison, we also obtained preoperative CT scans of 30 patients with cervical spondylotic myelopathy (CSM) without CP who required cervical laminoplasty during the same time period, and investigated the same radiographical parameters mentioned in the earlier text. The postoperative CT scans of the patients with CP who underwent pedicle screw fixation were also analyzed to investigate the accuracy of the pedicle screw placement. The severity of pedicle screw breach was categorized by the Neo grade (grade 0: no deviation, grade 1: deviation less than 2.0 mm, grade 2: deviation more than 2.0 mm, and grade 3: complete deviation).16 Breach grades 2 and 3 were defined as a critical breach.
Statistical Analysis All analyses were carried out using the IBM SPSS Statistics software program version 19 (SPSS, Inc., Somers, NY). For the comparisons of the parameters between the groups, Student t test or Mann-Whitney U test was used for continuous variables, and the χ2 test or Fisher exact test was used for categorical data. The risk factor analysis was conducted by a multivariate logistic regression analysis. For all statistical tests, P < 0.05 was considered to be significant.
RESULTS Sixteen males and 15 females were included in the CP group. Their mean age was 53.7 ± 9.4 years. Among www.spinejournal.com
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them, 19 patients underwent laminoplasty and 12 patients underwent decompression and fusion by posterior pedicle screw fixation. In 8 of these patients, surgery was performed as a revision procedure after laminoplasty. The demographic data of patients with pedicle screw fixation are summarized in Table 1. Twenty males and 10 females were included in the CSM group, and their mean age was 68.5 ± 9.6 years. A summary of all pedicle profile measurements is shown in Table 2.
TABLE 1. The Demographic Data of the
Patients Who Underwent Posterior Decompression and Fusion by Pedicle Screw Fixation
Age Sex
Level
Revision After Laminoplasty
Number of Pedicle Screws Used
1
52
M
C3–C7
+
6
2
59
F
O–C5
+
3
3
41
M
C4–C7
+
8
4
64
F
O–C5
+
3
5
61
F
O–C4
+
2
6
56
M
O–T2
−
5
7
64
F
O–C6
+
2
8
63
M
O–T2
+
6
Pedicle Inner Diameter
9
65
F
O–T2
−
7
The inner diameter in patients with CP were in the range from 0 (no cancellous canal in a pedicle) to 5.8 mm, and it was found to be smaller than that in patients with CSM at all cervical levels. Pedicle sclerosis was more frequently observed in the pedicles of patients with CP than in those of patients with CSM (23% vs. 7.3%, P < 0.001).
10
55
M
O–T2
−
5
11
47
M
O–T3
+
6
12
60
M
O–C5
−
3
Pedicle Outer Diameter The outer diameter in patients with CP was in the range from 3.3 to 9.6 mm, and it was found to be larger than that in patients with CSM at all cervical levels except for C7. A pedicle with an outer diameter narrower than the diameter of the pedicle screw we used (4.0 mm) was found in only 0.6% of the pedicles in patients with CP and in 3.0% of those in patients with CSM (P = 0.03).
Total = 56
TABLE 2. The Measurement of Cervical Pedicle Profiles in Patients With Cerebral Palsy and in Those
With Cervical Spondylotic Myelopathy Outer Diameter (mm)
Level
Transverse Angle (°)
Inner Diameter (mm)
Mean
SD
Range
Mean
SD
Range
Mean
SD
Range
CP
6.5*
0.9
4.8–9.5
2.6*
1.2
0–4.9
50.4*
5.1
36.7–60.5
CSM
5.4
1.0
2.7–8.0
3.0
0.9
0.9–5.1
44.5
6.5
29.6–57.1
CP
6.5*
1.0
3.6–9.5
2.4*
1.3
0–4.8
51.9*
5.7
31.0–63.7
CSM
5.6
0.9
3.3–7.1
3.0
1.0
0–4.8
49.6
6.6
34.1–68.4
CP
6.5*
0.9
3.3–8.6
2.5*
1.4
0–5.1
49.1
5.4
37.9–61.8
CSM
6.0
0.9
3.7–8.0
3.3
1.1
0–5.3
47.9
6.6
32.1–63.1
CP
6.8*
1.0
4.0–9.6
2.8*
1.3
0–5.4
40.7
7.3
24.7–60.9
CSM
6.1
0.9
4.2–7.6
3.4
1.1
0–5.4
42.8
8.1
23.4–58.7
CP
6.9
0.9
4.5–8.9
3.6*
1.3
0–5.8
29.0
6.0
15.5–45.7
CSM
6.9
0.9
5.0–9.1
4.7
0.8
3.2–6.7
27.4
6.3
15.5–44.1
C3
C4
C5
C6
C7
*Statistical significant difference between the CP and CSM groups. SD indicates standard deviation; CP, cerebral palsy; CSM, cervical spondylotic myelopathy.
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CERVICAL SPINE Pedicle Transverse Angle The transverse angle in patients with CP were in the range from 15.5° to 63.7°, and it was found to be larger than that in patients with CSM at C3 and C4. Excluding the C7 level whose mean PTA was notably smaller than the other cervical levels, a PTA wider than 55.0° was observed in 17% of the patients with CP and 11% of the patients with CSM (P = 0.07).
Lateral Mass Deformity A deformity was observed in 14% of the lateral masses of the patients with CP and in 8.7% of those of the patients with CSM (P = 0.03). Its prevalence at each vertebral level was 16% at C3, 15% at C4, 11% at C5, 13% at C6, and 16% at C7 in patients with CP, and 8.3% at C3, 15% at C4, 10% at C5, 5.0% at C6, and 5.0% at C7 in patients with CSM.
Accuracy of Pedicle Screw Placement Among the 56 pedicle screws inserted in patients with CP, 24 screws showed deviation (breach rate: 43%), with a critical breach (i.e., grade 2 or 3) found for 16 screws (29%). However, no clinically serious complication due to neurovascular injury occurred. With regard to the direction of the breach, an outward breach accounted for two-thirds of the overall incidences of breach (16 in 24). The rate of critical breach was higher in cases with revision surgery after laminoplasty (33% vs. 20%, P = 0.29), pedicle sclerosis (67% vs. 24%, P = 0.049), a pedicle transverse angle larger than 55.0° (40% vs. 26%, P = 0.45), and a lateral mass deformity (50% vs. 23%, P = 0.08). A multivariate logistic regression analysis revealed that pedicle sclerosis was associated with an increased risk of critical breach (odds ratio: 6.3; 95% confidence interval: 1.03–39.0; P = 0.047).
Case Presentation (Case 3) We performed posterior decompression and fusion with C4– C7 pedicle screw fixations for cervical myelopathy with CP in a 41-year-old male patient. He had undergone C3–C7 laminoplasty 2 years earlier. No pedicle outer diameter was less than 4.0 mm, but the inner diameters of most of the pedicles at C4 to C6 were less than 2.0 mm, and some of them were associated with a complete loss of the inner cancellous canal. The pedicle transverse angle was wider than 55° in C4 and C5. Lateral masses were deformed by the preoperative osteophyte formation on the right side of C3 to C5. The C5 cross-sectional surface is shown in Figure 2A. Even with very careful insertion
Cervical Spine in Cerebral Palsy • Kato et al
under CT-navigation system guidance, bilateral screw insertions resulted in grade 2 and 3 breaches (Figure 2B).
DISCUSSION There were 2 major findings in this study. First, we evaluated the cervical pedicle profiles in patients with athetoid CP. We found that pedicle outer diameter was larger in patients with CP than in patients with CSM, and that pedicle sclerosis, a wide transverse angle and lateral mass deformity were also more frequently observed. Second, the breach rate of cervical pedicle screws was high in patients with CP, and pedicle sclerosis was associated with an increased risk of screw misplacement. This study first described the morphological characteristics of cervical pedicle in patients with athetoid CP. Harada et al25 reported that the cervical spine in patients with CP is characterized by vertebral body flattening and a narrow sagittal spinal canal diameter. They speculated that the myelopathy in CP occurs on this developmental canal stenosis caused by excessive mechanical stress due to abnormal neck movement, followed by accelerated degenerative changes and instability. In this study, we found that the mean pedicle outer diameter in patients with CP was 6.5 to 6.9 mm, and the outer diameter was larger than that in patients with CSM. The mean outer diameter in patients with CSM was 5.4 to 6.9 mm, and it was similar to the outer diameter measured by CT in Liu et al24 systematic review of Asian subjects (5.3–6.6 mm). Pedicle narrowing was very rare (0.6%) in the patients with CP, whereas 2 previous studies have reported that the percentage of narrow cervical pedicles with a diameter less than that of the pedicle screws was up to 8.5% to 56.3%, depending on the cervical level.26,27 On the contrary, the inner diameter was smaller in patients with CP in our study. Pedicle sclerosis was frequently observed in patients with CP, whereas the other 2 previous studies that measured the inner diameter of cervical pedicles reported that they were in the range from 1.4 to 3.5 mm.28,29 It is not clear whether these morphological characteristics are based on developmental changes or accelerated degeneration. The lumbar pedicle diameter was reported to tend to be greater in male patients with degenerative changes.30 Therefore, we suppose that the cervical pedicle diameter could also become greater in CP, which is associated with massive degeneration. A pedicle transverse angle larger than 55.0° was more frequently observed at C3 to C6 in patients with CP (17%)
Figure 2. An axial CT scan of the C5 vertebra in patient 1 (A, preoperative; B, postoperative). CT indicates computed tomography. Spine
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CERVICAL SPINE than in patients with CSM in this study. The measurement of the pedicle transverse angle has varied among the previous studies, and thus, comparisons among these data need careful interpretation. The transverse angles in this study were somewhat larger than those in previous studies.26,28,29,31 Chazono et al26 considered that the transverse angle is determined by the relative location of the transverse foramen to the spinal canal. According to their theory, the wide transverse angle of cervical vertebrae in patients with CP could be explained by developmental hypoplasia in the sagittal direction. On the contrary, other studies have reported that the pedicle transverse angle did not differ in patients with developmental canal stenosis.32 The canal stenosis in patients with CP might have a different pathophysiological background from the previously reported developmental canal stenosis. The overall breach rate of pedicle screw placement in patients with CP was 43%, and a critical breach occurred in 29% of the screws. A few studies have specifically mentioned the accuracy of pedicle screw placement in patients with CP, and the breach rate was reported to be 18% to 30%.16,17 Nakashima et al18 reported that the breach rate was 2.5-fold higher in patients with CP. These authors mentioned that the loss of anatomical landmarks in a vertebra and the osteosclerotic changes of the pedicle might have led to the high breach rate.33 Our present findings support their hypotheses, in that we found the presence of a lateral mass deformity in many vertebrae, and it was associated with a high breach rate. In addition, pedicle sclerosis was a risk factor for a critical breach. It is risky to advance the probe and screw into the sclerotic pedicles, because it is necessary to put excessively high pressure on them, which can lead to the vertebral rotation so that the insertion could be laterally deviated, and the vertebral artery is more likely to be injured. Indeed, critical breach occurred in 67% of the sclerotic pedicles in this study. In addition, for pedicles with a wide transverse angle, extreme care should be taken because the probe and screw should be aimed in a considerably medial direction against the tension of the surrounding soft tissue. Although CT navigation guidance is an established technique used to facilitate screw placement, with a reported accuracy in the literature ranging from 89% to 100%,34 it is of note that the breach rate in this study was very high even with its assistance. It is possible that the accuracy of the navigation was impaired when the reference frame could not be set on the spinous process of the relevant vertebra. Therefore, we strongly recommend that surgeons pay meticulous attention when inserting the screw into the pedicle in patients with CP because more care is needed compared with patients with nondegenerative changes. Some other intraoperative imaging technologies, including the use of the O-arm, could help to address this issue.35 There are several limitations associated with this study. First, the number of patients with CP included in this study was still limited. Second, we could not examine the relationship between the morphological characteristics and the severity of involuntary movements because the neurological assessment of CP is notoriously difficult. Finally, the accuracy of pedicle screw insertion might have been affected by the E512
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surgeon’s level of proficiency. It might have changed over time due to the learning process given the relatively long period of patient inclusion in this study, although all of the surgical procedures were performed by attending surgeons certified by the Japanese Society for Spine Surgery and Related Research.
CONCLUSION The pedicle outer diameter in patients with CP was relatively large, but pedicle sclerosis, a wide transverse angle and a lateral mass deformity were frequently observed. Pedicle screw placement in a sclerotic pedicle is associated with a high risk of critical breach, and posterior cervical fusion using pedicle screws should always be carefully chosen as a treatment option for the patients with CP, especially when there are massive degenerative changes, after carefully considering their morphological characteristics.
➢ Key Points This retrospective study investigated the morphological characteristics of the cervical spine in patients with athetoid CP in comparison with that in patients with CSM, and its relationship with the breach of cervical pedicle screws. The pedicle outer diameter was larger in patients with CP than in patients with CSM, but pedicle sclerosis, a wide transverse angle and lateral mass deformity were more frequently observed in patients with CP. The breach rate of cervical pedicle screws was high in patients with CP, and pedicle sclerosis was associated with an increased risk of screw misplacement.
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Morphological Characteristics of Cervical Spine in Patients With Athetoid Cerebral Palsy and the Accuracy of Pedicle Screw Placement So Kato, MD,* Naoki Shoda, MD,* Hirotaka Chikuda, MD, PhD,* Atsushi Seichi, MD,† and Katsushi Takeshita, MD, PhD*
Study Design. A retrospective study. Objective. To investigate the morphology of the cervical spine in patients with athetoid cerebral palsy (CP), and to evaluate its relationship with the breach of cervical pedicle screws. Summary of Background Data. Cervical pedicle screws have been increasingly used in surgery for patients with CP, but screw misplacement is not uncommon. Although the altered morphology of the cervical spine in patients with CP may result in this high breach rate, few studies have examined the cervical pedicle profile. Methods. We retrospectively analyzed 31 patients with cervical myelopathy with CP, as well as 30 patients with cervical spondylotic myelopathy (CSM), who underwent posterior decompression surgery. The pedicle outer diameter, inner diameter, transverse angle and lateral mass deformity were investigated by obtaining preoperative computed tomographic scans. The accuracy of the placement of 56 pedicle screws used in fusion surgery for 12 patients with CP was also analyzed using postoperative computed tomographic scans. Results. The outer diameter of the pedicle in CP was in the range from 3.3 to 9.6 mm, and was larger than that in CSM at all cervical levels except for C7. Pedicle sclerosis was more frequently observed in CP than in CSM (23% vs. 7.3%, P < 0.001). The transverse angle at C3 and C4 was larger, and lateral mass deformity was more frequently observed in CP than in CSM. The critical breach of pedicle screws in CP was found in 29%. A multivariate analysis revealed that pedicle sclerosis was associated with an increased risk of breach (odds ratio: 6.3; 95% confidence interval: 1.03–39.0; P = 0.047). From the *Department of Orthopaedic Surgery, Sensory and Motor System Medicine, Surgical Sciences, Graduate School of Medicine, the University of Tokyo, Tokyo, Japan; and †Department of Orthopaedics, Jichi Medical University, Shimotsuke, Japan. Acknowledgment date: July 31, 2013. Revision date: November 13, 2013. Acceptance date: January 9, 2014. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to So Kato, MD, Department of Orthopaedic Surgery, Sensory and Motor System Medicine, Surgical Sciences, Graduate School of Medicine, the University of Tokyo, 7-3-1 Hongo Bunkyoku, Tokyo 113-8655, Japan; E-mail: [email protected] DOI: 10.1097/BRS.0000000000000234
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Conclusion. The pedicle diameter in patients with CP was relatively large, but pedicle sclerosis, a wide transverse angle and lateral mass deformity were frequently observed. Sclerotic pedicles were associated with a higher risk of critical breach. Key words: morphology, computed tomography, cervical spine, cerebral palsy, degeneration, myelopathy, pedicle screw, accuracy, breach rate, fusion. Level of Evidence: N/A Spine 2014;39:E508–E513
A
thetoid cerebral palsy (CP) is a common movement disorder caused by neonatal hypoxia that damages the basal ganglia, and it is characterized by involuntary movement and posture abnormalities. Patients with CP often show extensive spondylosis of the cervical spine in their early middle age caused by repetitive involuntary movements of the neck. Accelerated degeneration and continuous motion in the cervical spine eventually result in compressive myelopathy, which further complicates the patients’ already compromised neurological function and severely limits their autonomy.1,2 Once myelopathy has developed in patients with CP, it usually progresses with conservative treatment and requires surgical intervention. Although the optimal surgical treatment of cervical myelopathy in patients with CP remains to be established, decompression and fusion are often used to minimize the dynamic factors and prevent further instability of the cervical spine, especially in those with extensive involuntary movements or failed previous decompressive surgery.3–12 Cervical spinal fusion in patients with CP remains a clinical challenge. Instrumentation failure has been common with conventional wire and rod constructs.4,6 Pedicle screws are currently considered to be the most reliable anchor, because they provide stronger fixation than lateral mass screws13,14; however, cervical pedicle screw placement is technically demanding, and also poses a risk of neurovascular damage. Although the use of cervical pedicle screws in patients with CP has been increasingly reported in the literature,11,12,15–19 the results are not necessarily encouraging: a high rate of misplacement has been reported, which is presumably attributable to the
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extensive spondylosis and altered morphology of the spine in these patients.17,18 Although a better understanding of the morphological characteristics of the cervical spine in patients with CP would help surgeons to perform safer and more accurate surgery, no previous study specifically discussed the cervical pedicle profiles in patients with athetoid CP. The objective of this study was to investigate the morphological features of the cervical spine in patients with CP, focusing on the pedicle profiles in comparison with those of patients with cervical spondylotic myelopathy, and its relationship with the breach of pedicle screws.
MATERIALS AND METHODS Study Subjects We retrospectively reviewed our records of the patients with CP who had received posterior decompression surgery for cervical compressive myelopathy due to subaxial lesion between 2001 and 2011. Those with upper cervical lesions alone who underwent O–C2 or C1–C2 decompression and fusion were excluded from the analysis. We have historically used cervical laminoplasty for decompression,20,21 but currently limit its indication to those with minimal instability and mild involuntary movement. In terms of the fixation technique, we have selected posterior pedicle screws for rigid fixation. Pedicle screws of 4.0 mm in diameter were inserted using the guidance of a computed tomographic (CT) navigation system (StealthStation; Medtronic Inc., Minneapolis, MN).22,23 We obtained preoperative CT scans of the cervical spine with a 1.25-mm slice thickness. A surgical plan was devised on the computer work station using reconstructed 2- and 3-dimensional images. Intraoperatively, the reference frame was attached to the relevant spinous process of the vertebra. After matching the intraoperative anatomy and the imaging anatomy, the screw entrance holes were made using an air drill and deepened by a pedicle probe according to the planned screw trajectory under navigation system guidance, and the screws were inserted under fluoroscopy. If the relevant spinous process was not available for the reference frame attachment because of massive deformity or previous splitting by laminoplasty, we attached the reference frame to the adjacent vertebra. The spinal level to be fused was determined by the senior surgeons for each patient.
Imaging Analysis We identified 31 eligible patients with CP, and created reconstructed cross-sectional surfaces at 1-mm intervals from preoperative CT scans using the DICOM viewer (INTAGE Realia Pro; Cybernet Systems Co., Ltd., Tokyo, Japan). On the surfaces that passed the axes of bilateral pedicles, the pedicle outer diameter, inner diameter, and pedicle transverse angle of both pedicles in C3 to C7 were measured (Figure 1). All parameters were measured using the uniformed window level and width that were appropriate for the bony structure analysis (window level: 200, window width: 2000). We checked for the presence Spine
Figure 1. A schematic diagram of the pedicle parameters measured on CT scans (a, outer diameter; b, inner diameter; c, transverse angle). CT indicates computed tomography.
of pedicle sclerosis, which was defined as an inner diameter less than 2.0 mm.16 The pedicle transverse angle was defined as the angle formed by the vertebral midline and the pedicle axis, and we also checked the prevalence of vertebrae with a transverse angle larger than 55.0°.24 The presence of a lateral mass deformity was also investigated, considering that right and left asymmetry can cause a loss of anatomical landmarks that interferes with the estimation of the screw insertion point and angle. We defined a lateral mass with a thickness more than 2.0 mm thicker than the contralateral side as a deformed lateral mass. For comparison, we also obtained preoperative CT scans of 30 patients with cervical spondylotic myelopathy (CSM) without CP who required cervical laminoplasty during the same time period, and investigated the same radiographical parameters mentioned in the earlier text. The postoperative CT scans of the patients with CP who underwent pedicle screw fixation were also analyzed to investigate the accuracy of the pedicle screw placement. The severity of pedicle screw breach was categorized by the Neo grade (grade 0: no deviation, grade 1: deviation less than 2.0 mm, grade 2: deviation more than 2.0 mm, and grade 3: complete deviation).16 Breach grades 2 and 3 were defined as a critical breach.
Statistical Analysis All analyses were carried out using the IBM SPSS Statistics software program version 19 (SPSS, Inc., Somers, NY). For the comparisons of the parameters between the groups, Student t test or Mann-Whitney U test was used for continuous variables, and the χ2 test or Fisher exact test was used for categorical data. The risk factor analysis was conducted by a multivariate logistic regression analysis. For all statistical tests, P < 0.05 was considered to be significant.
RESULTS Sixteen males and 15 females were included in the CP group. Their mean age was 53.7 ± 9.4 years. Among www.spinejournal.com
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them, 19 patients underwent laminoplasty and 12 patients underwent decompression and fusion by posterior pedicle screw fixation. In 8 of these patients, surgery was performed as a revision procedure after laminoplasty. The demographic data of patients with pedicle screw fixation are summarized in Table 1. Twenty males and 10 females were included in the CSM group, and their mean age was 68.5 ± 9.6 years. A summary of all pedicle profile measurements is shown in Table 2.
TABLE 1. The Demographic Data of the
Patients Who Underwent Posterior Decompression and Fusion by Pedicle Screw Fixation
Age Sex
Level
Revision After Laminoplasty
Number of Pedicle Screws Used
1
52
M
C3–C7
+
6
2
59
F
O–C5
+
3
3
41
M
C4–C7
+
8
4
64
F
O–C5
+
3
5
61
F
O–C4
+
2
6
56
M
O–T2
−
5
7
64
F
O–C6
+
2
8
63
M
O–T2
+
6
Pedicle Inner Diameter
9
65
F
O–T2
−
7
The inner diameter in patients with CP were in the range from 0 (no cancellous canal in a pedicle) to 5.8 mm, and it was found to be smaller than that in patients with CSM at all cervical levels. Pedicle sclerosis was more frequently observed in the pedicles of patients with CP than in those of patients with CSM (23% vs. 7.3%, P < 0.001).
10
55
M
O–T2
−
5
11
47
M
O–T3
+
6
12
60
M
O–C5
−
3
Pedicle Outer Diameter The outer diameter in patients with CP was in the range from 3.3 to 9.6 mm, and it was found to be larger than that in patients with CSM at all cervical levels except for C7. A pedicle with an outer diameter narrower than the diameter of the pedicle screw we used (4.0 mm) was found in only 0.6% of the pedicles in patients with CP and in 3.0% of those in patients with CSM (P = 0.03).
Total = 56
TABLE 2. The Measurement of Cervical Pedicle Profiles in Patients With Cerebral Palsy and in Those
With Cervical Spondylotic Myelopathy Outer Diameter (mm)
Level
Transverse Angle (°)
Inner Diameter (mm)
Mean
SD
Range
Mean
SD
Range
Mean
SD
Range
CP
6.5*
0.9
4.8–9.5
2.6*
1.2
0–4.9
50.4*
5.1
36.7–60.5
CSM
5.4
1.0
2.7–8.0
3.0
0.9
0.9–5.1
44.5
6.5
29.6–57.1
CP
6.5*
1.0
3.6–9.5
2.4*
1.3
0–4.8
51.9*
5.7
31.0–63.7
CSM
5.6
0.9
3.3–7.1
3.0
1.0
0–4.8
49.6
6.6
34.1–68.4
CP
6.5*
0.9
3.3–8.6
2.5*
1.4
0–5.1
49.1
5.4
37.9–61.8
CSM
6.0
0.9
3.7–8.0
3.3
1.1
0–5.3
47.9
6.6
32.1–63.1
CP
6.8*
1.0
4.0–9.6
2.8*
1.3
0–5.4
40.7
7.3
24.7–60.9
CSM
6.1
0.9
4.2–7.6
3.4
1.1
0–5.4
42.8
8.1
23.4–58.7
CP
6.9
0.9
4.5–8.9
3.6*
1.3
0–5.8
29.0
6.0
15.5–45.7
CSM
6.9
0.9
5.0–9.1
4.7
0.8
3.2–6.7
27.4
6.3
15.5–44.1
C3
C4
C5
C6
C7
*Statistical significant difference between the CP and CSM groups. SD indicates standard deviation; CP, cerebral palsy; CSM, cervical spondylotic myelopathy.
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CERVICAL SPINE Pedicle Transverse Angle The transverse angle in patients with CP were in the range from 15.5° to 63.7°, and it was found to be larger than that in patients with CSM at C3 and C4. Excluding the C7 level whose mean PTA was notably smaller than the other cervical levels, a PTA wider than 55.0° was observed in 17% of the patients with CP and 11% of the patients with CSM (P = 0.07).
Lateral Mass Deformity A deformity was observed in 14% of the lateral masses of the patients with CP and in 8.7% of those of the patients with CSM (P = 0.03). Its prevalence at each vertebral level was 16% at C3, 15% at C4, 11% at C5, 13% at C6, and 16% at C7 in patients with CP, and 8.3% at C3, 15% at C4, 10% at C5, 5.0% at C6, and 5.0% at C7 in patients with CSM.
Accuracy of Pedicle Screw Placement Among the 56 pedicle screws inserted in patients with CP, 24 screws showed deviation (breach rate: 43%), with a critical breach (i.e., grade 2 or 3) found for 16 screws (29%). However, no clinically serious complication due to neurovascular injury occurred. With regard to the direction of the breach, an outward breach accounted for two-thirds of the overall incidences of breach (16 in 24). The rate of critical breach was higher in cases with revision surgery after laminoplasty (33% vs. 20%, P = 0.29), pedicle sclerosis (67% vs. 24%, P = 0.049), a pedicle transverse angle larger than 55.0° (40% vs. 26%, P = 0.45), and a lateral mass deformity (50% vs. 23%, P = 0.08). A multivariate logistic regression analysis revealed that pedicle sclerosis was associated with an increased risk of critical breach (odds ratio: 6.3; 95% confidence interval: 1.03–39.0; P = 0.047).
Case Presentation (Case 3) We performed posterior decompression and fusion with C4– C7 pedicle screw fixations for cervical myelopathy with CP in a 41-year-old male patient. He had undergone C3–C7 laminoplasty 2 years earlier. No pedicle outer diameter was less than 4.0 mm, but the inner diameters of most of the pedicles at C4 to C6 were less than 2.0 mm, and some of them were associated with a complete loss of the inner cancellous canal. The pedicle transverse angle was wider than 55° in C4 and C5. Lateral masses were deformed by the preoperative osteophyte formation on the right side of C3 to C5. The C5 cross-sectional surface is shown in Figure 2A. Even with very careful insertion
Cervical Spine in Cerebral Palsy • Kato et al
under CT-navigation system guidance, bilateral screw insertions resulted in grade 2 and 3 breaches (Figure 2B).
DISCUSSION There were 2 major findings in this study. First, we evaluated the cervical pedicle profiles in patients with athetoid CP. We found that pedicle outer diameter was larger in patients with CP than in patients with CSM, and that pedicle sclerosis, a wide transverse angle and lateral mass deformity were also more frequently observed. Second, the breach rate of cervical pedicle screws was high in patients with CP, and pedicle sclerosis was associated with an increased risk of screw misplacement. This study first described the morphological characteristics of cervical pedicle in patients with athetoid CP. Harada et al25 reported that the cervical spine in patients with CP is characterized by vertebral body flattening and a narrow sagittal spinal canal diameter. They speculated that the myelopathy in CP occurs on this developmental canal stenosis caused by excessive mechanical stress due to abnormal neck movement, followed by accelerated degenerative changes and instability. In this study, we found that the mean pedicle outer diameter in patients with CP was 6.5 to 6.9 mm, and the outer diameter was larger than that in patients with CSM. The mean outer diameter in patients with CSM was 5.4 to 6.9 mm, and it was similar to the outer diameter measured by CT in Liu et al24 systematic review of Asian subjects (5.3–6.6 mm). Pedicle narrowing was very rare (0.6%) in the patients with CP, whereas 2 previous studies have reported that the percentage of narrow cervical pedicles with a diameter less than that of the pedicle screws was up to 8.5% to 56.3%, depending on the cervical level.26,27 On the contrary, the inner diameter was smaller in patients with CP in our study. Pedicle sclerosis was frequently observed in patients with CP, whereas the other 2 previous studies that measured the inner diameter of cervical pedicles reported that they were in the range from 1.4 to 3.5 mm.28,29 It is not clear whether these morphological characteristics are based on developmental changes or accelerated degeneration. The lumbar pedicle diameter was reported to tend to be greater in male patients with degenerative changes.30 Therefore, we suppose that the cervical pedicle diameter could also become greater in CP, which is associated with massive degeneration. A pedicle transverse angle larger than 55.0° was more frequently observed at C3 to C6 in patients with CP (17%)
Figure 2. An axial CT scan of the C5 vertebra in patient 1 (A, preoperative; B, postoperative). CT indicates computed tomography. Spine
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CERVICAL SPINE than in patients with CSM in this study. The measurement of the pedicle transverse angle has varied among the previous studies, and thus, comparisons among these data need careful interpretation. The transverse angles in this study were somewhat larger than those in previous studies.26,28,29,31 Chazono et al26 considered that the transverse angle is determined by the relative location of the transverse foramen to the spinal canal. According to their theory, the wide transverse angle of cervical vertebrae in patients with CP could be explained by developmental hypoplasia in the sagittal direction. On the contrary, other studies have reported that the pedicle transverse angle did not differ in patients with developmental canal stenosis.32 The canal stenosis in patients with CP might have a different pathophysiological background from the previously reported developmental canal stenosis. The overall breach rate of pedicle screw placement in patients with CP was 43%, and a critical breach occurred in 29% of the screws. A few studies have specifically mentioned the accuracy of pedicle screw placement in patients with CP, and the breach rate was reported to be 18% to 30%.16,17 Nakashima et al18 reported that the breach rate was 2.5-fold higher in patients with CP. These authors mentioned that the loss of anatomical landmarks in a vertebra and the osteosclerotic changes of the pedicle might have led to the high breach rate.33 Our present findings support their hypotheses, in that we found the presence of a lateral mass deformity in many vertebrae, and it was associated with a high breach rate. In addition, pedicle sclerosis was a risk factor for a critical breach. It is risky to advance the probe and screw into the sclerotic pedicles, because it is necessary to put excessively high pressure on them, which can lead to the vertebral rotation so that the insertion could be laterally deviated, and the vertebral artery is more likely to be injured. Indeed, critical breach occurred in 67% of the sclerotic pedicles in this study. In addition, for pedicles with a wide transverse angle, extreme care should be taken because the probe and screw should be aimed in a considerably medial direction against the tension of the surrounding soft tissue. Although CT navigation guidance is an established technique used to facilitate screw placement, with a reported accuracy in the literature ranging from 89% to 100%,34 it is of note that the breach rate in this study was very high even with its assistance. It is possible that the accuracy of the navigation was impaired when the reference frame could not be set on the spinous process of the relevant vertebra. Therefore, we strongly recommend that surgeons pay meticulous attention when inserting the screw into the pedicle in patients with CP because more care is needed compared with patients with nondegenerative changes. Some other intraoperative imaging technologies, including the use of the O-arm, could help to address this issue.35 There are several limitations associated with this study. First, the number of patients with CP included in this study was still limited. Second, we could not examine the relationship between the morphological characteristics and the severity of involuntary movements because the neurological assessment of CP is notoriously difficult. Finally, the accuracy of pedicle screw insertion might have been affected by the E512
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surgeon’s level of proficiency. It might have changed over time due to the learning process given the relatively long period of patient inclusion in this study, although all of the surgical procedures were performed by attending surgeons certified by the Japanese Society for Spine Surgery and Related Research.
CONCLUSION The pedicle outer diameter in patients with CP was relatively large, but pedicle sclerosis, a wide transverse angle and a lateral mass deformity were frequently observed. Pedicle screw placement in a sclerotic pedicle is associated with a high risk of critical breach, and posterior cervical fusion using pedicle screws should always be carefully chosen as a treatment option for the patients with CP, especially when there are massive degenerative changes, after carefully considering their morphological characteristics.
➢ Key Points This retrospective study investigated the morphological characteristics of the cervical spine in patients with athetoid CP in comparison with that in patients with CSM, and its relationship with the breach of cervical pedicle screws. The pedicle outer diameter was larger in patients with CP than in patients with CSM, but pedicle sclerosis, a wide transverse angle and lateral mass deformity were more frequently observed in patients with CP. The breach rate of cervical pedicle screws was high in patients with CP, and pedicle sclerosis was associated with an increased risk of screw misplacement.
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