Cervical laminoplasty: evaluation of bone bonding of a high porosity hydroxyapatite spacer
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1 J Neurosurg (Spine 2) 98: , 2003 Cervical laminoplasty: evaluation of bone bonding of a high porosity hydroxyapatite spacer TETSUHIRO IGUCHI, M.D., ARITETSU KANEMURA, M.D., AKIRA KURIHARA, M.D., KOICHI KASAHARA, M.D., SHINICHI YOSHIYA M.D., MINORU DOITA, M.D., AND KOTARO NISHIDA, M.D. Department of Orthopaedic Surgery, Kobe Rosai Hospital; and Department of Orthopaedic Surgery, Kobe Graduate School of Medicine, Kobe, Japan Object. The purpose of this study was to evaluate the usefulness of a high-porosity hydroxyapatite (HA) spacer in cervical laminoplasty. Bone spacer bonding rates, complications associated with the implant, and factors related to bone bonding were examined. Methods. The authors evaluated 33 consecutive patients with cervical myelopathy who underwent high-porosity HA spacer assisted laminoplasty and were followed for at least 1 year (mean 30 months). The results of bone spacer bonding of the 147 implants were evaluated using computerized tomography (CT) scanning. The symptoms significantly improved in 30 patients. No difference in results was detected between patients with cervical spondylosis and those with ossification of posterior longitudinal ligament. Breakage of seven spacers occurred in four patients without causing neck pain or neurological deficits. There were no other HA spacer related complications. The spacers became rigidly bound to bone in 61% of the cases, and bone regrowth developed around the spacer in 91%. The rate of bone spacer bonding increased over time, and the CT-documented attenuation value (Hounsfield unit) of the spacer adjacent to the bone spacer junction in the group in which union occurred was significantly higher than in the nonunion group. Conclusions. High-porosity HA spacer augmented laminoplasty produced good bonding-related results. Bone bonding continued to progress 1 year after surgery, indicating the good osteoconductive capability of high-porosity HA. To avoid breakage of a spacer, a minimum 7-mm distance between spacers is necessary. KEY WORDS cervical spine laminoplasty hydroxyapatite bone bonding I N place of laminectomy, which has often been associated with late-onset neurological deterioration, 5 7 laminoplasty was developed for treatment of patients with cervical myelopathy. Based on the method of widening the spinal canal, this surgery can be divided into two categories: 1) expansive surgery involving the opening of the spinal canal; 2,7 and 2) closed spinal canal involving the placement of spacers such as iliac bone graft, 1,20,23 rib allograft, 1,16 and artificial materials. 4,8,14,17 Both fundamental procedures provide good clinical outcomes; however, symmetrical enlargement with closed spinal canal is considered to be more anatomically and physiologically effective. 2,23 Because of the benefits of no donor site pain, shorter operative time, and decreased blood loss, laminoplasty involving the use of artificial materials such as HA spacers has become remarkably popular. 4,8,14,15,17 The usefulness and safety of HA spacer augmented laminoplasty, however, is still unknown. Although low-porosity HA Abbreviations used in this paper: AP = anteroposterior; CSM = cervical spondylotic myelopathy; CT = computerized tomography; HA = hydroxyapatite; JOA = Japanese Orthopaedic Association; OPLL = ossification of the longitudinal ligament; ROI = region of interest. J. Neurosurg: Spine / Volume 98 / March, 2003 spacer assisted laminoplasty has not been associated with such drawbacks, it is unclear whether a newly enlarged spinal canal can consistently promote rigid bone bonding with low osteogenic activity. 8,14,17 The purpose of this study was to examine the clinical outcome in patients undergoing laminoplasty involving the use of high-porosity HA spacers, which has higher osteoconductive activity, 18,19 and to assess its usefulness for cervical laminoplasty. Clinical Material and Methods Patient Population Between January 1997 and February 2001, 37 consecutive patients in whom no previous spinal surgery had been performed were treated at the lead author s (T.I.) institution. Cervical myelopathy was present in all patients, who underwent double-door laminoplasty involving placement of HA spacers. The HA spacer (Bonfil; Mitsubishi Phama, Co., Osaka, Japan) used in this study was synthesized by sintering at 900 C and was characterized with a 300- m pore size and 60% microporosity. This study includes 33 patients who were followed for a minimum of 1 year including three who underwent concomitant lumbar de- 137
2 T. Iguchi, et al. FIG. 1. Measuring methods of the examined variables. The lordotic angle was determined as the angle (a) between posterior line of C-2 and C-7 in neutral position (Ishihara method). The postoperative AP diameter (b) was the distance between the vertebra and the spacer. The upper interimplant distance (D1) and lower interimplant distance (D2) were measured for each HA implant. The upper intervertebral angle (c) for the C-4 spacer was measured by Lines 1 and 2 and the lower intervertebral angle (d) by Lines 1 and 3. compressive surgery. The diagnoses were CSM in 23 patients and OPLL in 10 patients (27 men, six women; age range years [mean 65.4 years]). All follow-up examinations were conducted at the same institution (mean follow-up period 30 months, range months), and patients were evaluated clinically and radiologically. Surgical Procedure Surgery was performed with the patient in the prone position after induction of general anesthesia. 23 After exposure of the cervical spine, the spinal processes were shortened by up to 15 to 25 mm in length from the base, split, and affixed by nylon sutures with HA spacers. Splitting was performed using a threaded-wire saw 22 in 150 laminae and a 3-mm high-speed burr in 16 laminae. Laminae in the following segments were expanded: C3 7 (29 cases), C3 T1 (two cases), C4 7 (one case), and C4 T1 (one case), and an HA spacer was placed in 159 laminae of the 166 laminae treated. Clinical Evaluation For clinical evaluation, we used the JOA scoring system 20 for cervical myelopathy. Preoperative clinical evaluation data and JOA scores were recorded from the patients charts, and postoperative final scores were determined by one of the authors blinded to the pre- and postoperative clinical course of each patient. The recovery rate was defined according to the following calculation: (postoperative preoperative score) / (17 preoperative score) 100% (the Hirabayashi method 4,23 ). Radiographic Evaluation Six radiographs (AP, lateral [flexion, neutral, and extension], and two oblique), were obtained pre- and postoperatively. Examined variables were lordotic angle in the neutral position 12 AP diameter of the spinal canal, distance between HA implants, number of broken spacers, range of motion, 12,21 and the adjacent intervertebral angles 12 of each spacer examined from C2 3 to C6 7 (Fig. 1). Interspacer distance was considered to be the shortest distance between spacers as demonstrated on lateral neutral x-ray film. Range of motion was determined by calculating the difference of the lordotic angles between extension and flexion x-ray films. Similarly, each superior and inferior intervertebral angle was calculated as a difference of intervertebral angles between extension and flexion. Computerized Tomography Evaluation Helical CT scanning was performed to examine each lamina including the entire spacer; studies were performed using the HiSpeed Advantage scanner (General Electric, Milwaukee, WI) with a 3-mm collimation. Every gantry was placed parallel to each lamina. All scans were examined and photographed at a window level of 100 HU and a width of 1000 HU. The CT scans were evaluated for evidence of implant bone bonding and time-dependent changes of the CT-documented attenuation values within the spacer. A single observer (A.K.) evaluated CT scans of the 147 HA spacers in 30 patients (24 men, six women; mean age 65.5 years) to determine HA spacer bone binding. Bone spacer bonding was classified using the Ichikawa scheme 10 (Fig. 2); Types D and E were identified as union whereas Types C, D, and E were regarded as bone regrowth. The factors influencing bone spacer bonding were examined considering the following variables: age, sex, levels of the inserted spacer, operative time, splitting methods, and the aforementioned radiological factors. For examination of the CT-documented attenuation within the spacer, ROIs were determined in 1-mm-radius circles that were located 2 mm away from each of the six edges in the spacer (Fig. 3). Then, the CT-demonstrated 138 J. Neurosurg: Spine / Volume 98 / March, 2003
3 Hydroxyapatite-induced bone bonding in cervical laminoplasty FIG. 2. Bone-bonding types of the spacer (Ichikawa classification). Type A: Bone resorption occurs around the implant. Type B: A clear space is present between the spacer and the bone without new bone formation. Type C: There is a space between the implant and the bone; however, new laminar bone formation is observed at the inner surface of the spinal canal. Type D: No space at the interface with new bone formation. Type E: Bridging of the new bone at the inner surface of the canal. When the different types were present at both interfaces, a lower degree of classification was applied. attenuation value on 103 scans of the spacers in 21 patients (13 men, eight women; mean age 67.8 years) was measured and assessed in relation to bone bonding. Because a 1.5-mm tunnel penetrated the center of the spacer to allow the passage of strings for fixing the spacer, the CT-evidenced value in the midpart of the spacer was not measured. Statistical Analysis A paired t-test was used for comparison of pre- and postoperative evaluation rates, and a chi-square test was used for examination of data regarding spaces between the HA implants. An unpaired t-test was used for comparison between two groups of variables, and analysis of variance (Fisher protected least significance difference) for comparison among more than three groups. A probability value less than 0.05 was considered significant. Results Surgery-Related Outcome Postoperatively all but three patients improved clinically. In patients who underwent cervical surgery alone improvement in myelopathy (87%), sensory (80%), numbness (77%), and bladder functions (40%) was documented. The mean preoperative JOA score improved from 8.9 to 13.1 at the follow-up examination (p 0.001); overall recovery rate was 50.8%. The mean recovery rate in patients with CSM was 51.2% and that in those with OPLL was 50.4%, indicating no statistical difference. Of the three patients in whom no clinical improvement occurred, one had undergone a concomitant lumbar surgery, and in two T 2 -weighted magnetic resonance imaging revealed local kyphosis with hyperintensity within the spinal cord before surgery and cord atrophy after surgery. J. Neurosurg: Spine / Volume 98 / March, 2003 Radiographic Measurement The mean angle of cervical lordosis was changed little from a preoperative angle of 14.7 to a postoperative angle of 14.9 whereas range of motion decreased remarkably from 36.4 to The decrease in intervertebral angle was greatest at the C3 4 level, while showing no statistical difference between levels, and the increase in AP diameter was significantly greater at C-6 and C-7 (Table 1). The mean interimplant distance between the central spacer and upper spacer was 7 mm and that between the central spacer and lower spacer was 7.1 mm, indicating virtually no difference between them. Breakage of the Spacer The breakage of seven spacers (4.4 %) occurred in four patients (three with CSM and one with OPLL) without causing neck pain or neurological symptoms. One spacer broke at C-3, two at C-4, two at C-5, and two at C-6. Five spacers broke in three patients within 3 months of surgery and two in one patient by the 1-year follow-up examination. Interimplant distances to both upper and lower spacers demonstrated on the immediate postoperative radiographs were not statistically different between the groups in which the implants broke and did not break; however, the distance to the upper spacer was clearly shorter from the central spacer than the distance to the lower spacer in the group of patients in whom spacers broke (Fig. 4 upper). In the group in which the distance to the upper spacer was less than 3 mm (12 spacers), three spacers were found to be broken whereas the other nine were intact. On the other hand, the group in which the distance was greater than 3 mm (107 spacers) between implants three implants broke, whereas 104 were intact; this indicated that a shorter distance between spacers is a statistically significant risk factor for breakage (p = 0.013). Analysis of the same measurement at a lower distance between spacers did not indicate such tendency statistically, and no statistical intergroup difference was observed in intervertebral FIG. 3. Location of each ROI for CT evaluation. Dotted lines indicate a tunnel for passing suture threads. 139
4 T. Iguchi, et al. TABLE 1 Summary of pre- and postoperative intervertebral angle and AP diameter values* Intervertebral Angle AP Diameter Location Preop ( ) Postop ( ) Decrease Rate (%) Preop (mm) Postop (mm) Expansion Rate (%) C C C C C C C C C C *Values presented as the means standard deviations. Significant at p angles between those in whom spacers did and did not break. Bone Spacer Bonding Based on the Ichikawa classification, bone bonding was characterized by Type A for one spacer (0.7%), Type B for 12 (8.2%), Type C for 45 (30.6%), Type D for 81 (55.1%), and Type E for eight (5.4%) (Fig. 4 lower), and thus union occurred in 60.5% and bone regrowth in 91%. The incidence of union (Types D and E) was lower at C-6 and C- 7. Comparison of union (Types D and E) and nonunion (Types A, B, and C) groups indicated that the postoperative period (and hence that for CT examination) in the union group was significantly longer than that in the nonunion group (Fig. 5 upper). A similar tendency was demonstrated in the groups in which bone regrowth occurred (C, D, and E) and did not occur (A and B). At less than 1 year the union rate was 47.4%, whereas at greater than 1 year it was 74.6%; similarly at less than 1 year the bone regrowth rate was 86.8%, whereas at greater than 1 year it was 95.8%. These results indicated that bone bonding depended on postoperative duration and was still ongoing 1 year after surgery. No correlation was demonstrated between the incidence of nonunion and neck symptoms (data not shown). The postoperative AP diameter of the spinal canal alone correlated with bone spacer bonding. Postoperative AP diameters in the union group were significantly smaller than those in the nonunion group, and this relationship was also true in the regrowth and the absent regrowth groups (Fig. 5 lower). Hounsfield Unit Value The CT number of ROI 1 (Fig. 3) showed a significant positive correlation (r = 0.68) with time after surgery (Fig. 6). This finding was true in every ROI (ROI 2, r = 0.64; 3, r = 0.79; 4, r = 0.7; 5, r = 0.69; and 6, r = 0.49). The mean CT values ( standard deviations) of the six measured ROIs at the final evaluation were , , , , , HU, respectively, for ROIs 1, 2, 3, 4, 5, and 6 showing higher density at every area than that of bone ( HU; mean 50 measurements at the pedicles of vertebrae in 10 patients). The CT values determined adjacent to the bone spacer junction (ROIs 1, 2, 5, and 6) were significantly higher than those of areas (ROIs 3 and 4) that were far from the junction (p 0.001); however, no difference was observed between right and left nor between anterior and posterior ROIs. In a comparison between values obtained in the union and the nonunion groups we found significantly higher density in the union group at all ROIs (Fig. 7). FIG. 4. Graphs. Upper: Distances between the central and upper spacers and those between the central and lower spacers. No significant difference was observed between the breakage group and the nonbreakage group; however, the mean space was shorter in the breakage group ( 7 mm). Lower: Bone bonding of the spacer at each level. Distribution of each type according to Ichikawa classification (see upper) is shown. NS = not significant. 140 J. Neurosurg: Spine / Volume 98 / March, 2003
5 Hydroxyapatite-induced bone bonding in cervical laminoplasty FIG. 6. Correlation between the CT-documented Hounsfield unit and postoperative period (days). The CT value showed positive correlation with postoperative period. FIG. 5. Graphs. Upper: Status of bone bonding after surgery. The mean follow-up periods in which CT evaluation was performed were longer in both union and regrowth groups than those in the nonunion and nonregrowth groups. Lower: Anteroposterior diameter and bone bonding. In both union and regrowth groups significantly shorter AP diameters were shown than in the other groups. Discussion Contrary to bioinert alumina ceramics 4 HA has been proven to have good osteoconductivity properties and thus can be regarded as a bioactive ceramic and has been widely used as a bone substitute for large bone defects. 11 Results of HA spacer augmented laminoplasty, in terms of osteoconductivity and bone bonding, have not been reported, and ours is the first study conducted to examine the osteoconductive activity in cervical spine surgery. It is known that the osteoconductivity of synthesized HA differs depending on the sintered temperature, with most remarkable activity being achieved at 700 to 900 C. 18,19 Previous HA spacers used to reconstruct the lamina were sintered at higher temperatures and with a lower microporosity (50 to 300 m pore size, 35 48% porosity sintered with 1150 C; 9,13 and 100 to 500 m pore size, 40% porosity sintered with 1200 C). 14,17 Authors of the preceding clinical studies have reported satisfactory outcomes, and no complications related to the use of HA, although bone spacer bonding data were absent except in one case report in which good bonding was demonstrated 2 years after surgery. 14 In another histological report the authors described the presence of bone bonding in half of the spacer bone interface as well as the presence of fibrous tissue in the other half in the resected three spacers 1 year after index surgery. 13 To secure fixation and to increase the J. Neurosurg: Spine / Volume 98 / March, 2003 bonding rate, a new technique involving fixation of lowporosity spacers with titanium screws has recently been developed. 21 In the present study, a good bone spacer bonding was observed, and the bone regrowth rate was 96%, as evidenced on CT scans. The higher attenuation in the bone union group also demonstrated that the CT-documented Hounsfield unit is a good indicator of bone bonding. The percentage of bone union was lower at the C-6 and C-7 spinal processes, which had significantly greater postoperative AP diameters. In the variables examined in conjunction with bone union, moreover, a postoperative shorter AP diameter alone correlated with good bone bonding. These results indicate that a higher settlement of the HA spacer tends to have lower bone bonding capabilities because it receives less blood from the pedicles after total intraoperative detachment of the muscles. 10 Thus, settlement as low as possible but with enough space to the dura is considered to be necessary. 10 Although breakage of the spacer occurred in small number of patients, it was a major disadvantage. Because no breakage of the previous low-porosity HA spacers was reported, 8,14,17 this defect is considered to be wholly due to high porosity. The breakage related only to the shorter dis- FIG. 7. Comparison of CT-documented value number between the union and the nonunion groups. Density of the spacer in the union group was significantly higher in all ROIs. 141
6 T. Iguchi, et al. tance between spacers and not to other variables. Because a mean distance of more than 7 mm was observed in the nonbreakage group, we have not implanted the spacers at the levels of less than 7 mm in the 11 patients who have undergone laminoplasty since January Consequently there has been no incidence of breakage. The nonspacer-treated lamina in these 11 patients was kept open bilaterally by suturing the bivalve laminae to the muscles at the base of the facet joint. 22 We recommend this supplemental fixation for laminae not supported by spacers. Except for the problem of breakage, good bone bonding was achieved in double-door laminoplasty involving highporosity HA. The authors of a recent study reported that biodegradation occurred in high-porosity synthesized HA, which shares the same characteristics as that used in this study. 3 The use of this type HA, therefore, may induce new bone formation around and within the spacer, resulting in the patient s own bone constructing a new spinal canal. Conclusions In high-porosity HA spacer assisted laminoplasty, rigid bone bonding was observed in 61% and bone regrowth around spacers in 91% of the cases. The process of bone bonding continued more than 1 year after surgery, underscoring the good osteoconductive activity of the spacer. Breakage occurred in 4.4% of 147 spacers. To avoid this complication, a distance of at least 7 mm should be maintained between spacers. As low as possible a settlement of the spacer is considered to be necessary for good implant bone bonding. Acknowledgment The authors thank Dr. Yoshiki Nishida, Department of Radiology, Kobe Rosai Hospital, for his invaluable advice. Disclaimer No funds were received in support of this study. References 1. Edwards CC II, Heller JG, Silcox DH III: T-Saw laminoplasty for the management of cervical spondylotic myelopathy: clinical and radiographic outcome. Spine 25: , Fujimura Y, Nishi Y: Atrophy of the nuchal muscle and change in cervical curvature after expansive open-door laminoplasty. Arch Orthop Trauma Surg 115: , Goto T, Kojima T, Iijima T, et al: Resorption of synthetic porous hydroxyapatite and replacement by newly formed bone. J Orthop Sci 6: , Hase H, Watanabe T, Hirasawa Y, et al: Bilateral open laminoplasty using ceramic laminas for cervical myelopathy. Spine 16: , Heller JG, Edwards CC II, Murakami H, et al: Laminoplasty versus laminectomy and fusion for multilevel cervical myelopathy: an independent matched cohort analysis. Spine 26: , Herkowitz HN: A comparison of anterior cervical fusion, cervical laminectomy, and cervical laminoplasty for the surgical management of multiple level spondylotic radiculopathy. Spine 13: , Hirabayashi K, Watanabe K, Wakano K, et al: Expansive opendoor laminoplasty for cervical spinal stenotic myelopathy. Spine 8: , Hirabayashi S, Kumano K: Contact of hydroxyapatite spacers with split spinous processes in double-door laminoplasty for cervical myelopathy. J Orthop Sci 4: , Hoshi K, Kurokawa T, Nakamura K, et al: Expansive cervical laminoplasties observations on comparative changes in spinous process lengths following longitudinal laminal divisions using autogenous bone or hydroxyapatite spacers. Spinal Cord 34: , Ichikawa S, Iwatani M, Harata S, et al: [Bone ingrowth to the hydroxyapatite spacer after spinous process splitting laminoplasty.] J Japan Spine Res Society 5:215, 1994 (Jpn) 11. Inoue O, Ibaraki K, Shimabukuro H, et al: Packing with highporosity hydroxyapatite cubes alone for the treatment of simple bone cyst. Clin Orthop 293: , Ishihara A: [Roentgenographic studies on the normal pattern of the cervical curvature.] Nippon Seikeigeka Gakkai Zasshi 42: , 1968 (Jpn) 13. Kokubun S, Kashimoto O, Tanaka Y: Histological verification of bone bonding and ingrowth into porous hydroxyapatite spinous process spacer for cervical laminoplasty. Tohoku J Exp Med 173: , Koshu K, Tominaga T, Yoshimoto T: Spinous process-splitting laminoplasty with an extended foraminotomy for cervical myelopathy. Neurosurgery 37: , Koyama T, Handa J: Cervical laminoplasty using apatite beads as implants. Experience in 31 patients with compressive myelopathy due to developmental canal stenosis. Surg Neurol 24: , Lee TT, Manzano GR, Green BA: Modified open-door cervical expansive laminoplasty for spondylotic myelopathy: operative technique, outcome, and predictors for gait improvement. J Neurosurg 86:64 68, Nakano K, Harata S, Suetsuna F, et al: Spinous process-splitting laminoplasty using hydroxyapatite spinous process spacer. Spine 17:S41 S43, Niwa S, Hori M: [Studies in implantation of the synthetic hydroxyapatite.] Rinsho Seikei Geka 21: , 1986 (Jpn) 19. Ono K, Yamamuro T, Nakamura T, et al: Quantitative study on osteoconduction of apatite-wollastonite containing glass ceramic granules, hydroxyapatite granules, and alumina granules. Biomaterials 11: , Seichi A, Takeshita K, Ohishi I, et al: Long-term results of double-door laminoplasty for cervical stenotic myelopathy. Spine 26: , Takayasu M, Takagi T, Nishizawa T, et al: Bilateral open-door cervical expansive laminoplasty with hydroxyapatite spacers and titanium screws. J Neurosurg (Spine 1) 96:22 28, Tanaka J, Seki N, Tokimura F, et al: Operative results of canalexpansive laminoplasty for cervical spondylotic myelopathy in elderly patients. Spine 24: , Tomita K, Kawahara N, Toribatake Y, et al: Expansive midline T-saw laminoplasty (modified spinous process-splitting) for the management of cervical myelopathy. Spine 23:32 37, 1998 Manuscript received June 24, Accepted in final form November 11, Address reprint requests to: Tetsuhiro Iguchi, M.D., Department of Orthopaedic Surgery, Kobe Rosai Hospital, Kagoike- Dori, Chuo-ku, Kobe , Japan. aco66120@par.odn. ne.jp. 142 J. Neurosurg: Spine / Volume 98 / March, 2003
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