JBJS | Article

The Journal of Bone & Joint Surgery, Volume 83, Issue 12

Scientific Article | December 01, 2001

Progression of Ossification of the Posterior Longitudinal Ligament Following en Bloc Cervical Laminoplasty

Yoshiharu Kawaguchi, MD, PhD; Masahiko Kanamori, MD, PhD; Hirokazu Ishihara, MD, PhD; Hiroshi Nakamura, MD, PhD; Kazuhito Sugimori, MD; Haruo Tsuji, MDPhD; Tomoatsu Kimura, MDPhD

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Investigation performed at the Department of Orthopaedic Surgery, Toyama Medical and Pharmaceutical University, Toyama, Japan

Yoshiharu Kawaguchi, MD, PhD
Masahiko Kanamori, MD, PhD
Hirokazu Ishihara, MD, PhD
Hiroshi Nakamura, MD, PhD
Kazuhito Sugimori, MD
Haruo Tsuji, MD, PhD
Tomoatsu Kimura, MD, PhD
Department of Orthopaedic Surgery, Toyama Medical and Pharmaceutical University, 2630 Sugitani, Toyama 930-0194, Japan. E-mail address for Y. Kawaguchi: zenji@ms.toyama-mpu.ac.jp

No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.

The Journal of Bone & Joint Surgery. 2001; 83:1798-1802

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Abstract

Background: Ossification of the posterior longitudinal ligament often causes compressive myelopathy. Ossification is a progressive disease, and it has been reported that the area of ossification increases after decompressive surgery. However, it is uncertain how the progression of ossification affects the long-term outcome after cervical laminoplasty. This study was performed to clarify the relationship between the progression of ossification of the posterior longitudinal ligament and the clinical results following en bloc cervical laminoplasty.

Methods: Forty-five patients who were followed for more than ten years after laminoplasty participated in this study. Radiographs and tomograms of the cervical spine of each patient were made before and after the operation and at the time of the latest follow-up. The extent of ossification in the longitudinal and sagittal axes was evaluated. Neurological function was graded with use of the Japanese Orthopaedic Association scoring system. The relationship between the progression of ossification and the score-based rate of recovery was analyzed.

Results: Thirty-three (73%) of the patients had progression of ossification of the posterior longitudinal ligament after laminoplasty. Progression was frequent in patients with the mixed type of ossification and in those with the continuous type, whereas it was rare in patients with the segmental type. The patients with progression of the ossification were significantly younger than those without progression (p = 0.018). The Japanese Orthopaedic Association score improved rapidly within one year and continued to improve up to five years after surgery. The score tended to decrease thereafter. For thirteen patients, the score had worsened at the time of the latest follow-up. Three patients had neurological deterioration following an increase in the thickness of the ossification.

Conclusions: Progression of ossification of the posterior longitudinal ligament was often observed during the long-term follow-up period after laminoplasty. Young patients with mixed and continuous types of ossification had the greatest risk for progression. Preventive measures, such as the use of a wider laminar opening during the laminoplasty, should be considered for patients who are at risk for progression of ossification.

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Introduction

Cervical laminoplasty is a standard technique for achieving posterior decompression of the spinal cord in patients with multilevel compressive myelopathy. Excellent results following laminoplasty have been reported^1-8. Ossification of the posterior longitudinal ligament is one of the causes of compressive myelopathy⁹. At our hospital, cervical laminoplasty has been indicated for most of the cases of myelopathy due to ossification since 1981. Ossification of the posterior longitudinal ligament is a progressive disease, and it has been reported that the area of ossification increases following decompressive surgery^10-12. However, it is uncertain how the progression of ossification affects the long-term outcome. The purpose of the present study was to clarify the relationship between the progression of ossification and the clinical results following en bloc cervical laminoplasty.

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Fig. 1:: System for classification of ossification of the posterior longitudinal ligament, proposed by the Investigation Committee on the Ossification of the Spinal Ligaments of the Japanese Ministry of Public Health and Welfare. A, continuous type; B, segmental type; C, mixed type; and D, other type.

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Fig. 2-A:: Figs. 2-A, 2-B, and 2-C Case 41. This forty-four-year-old man had the continuous type of ossification from the second through the seventh cervical level. He also had ossification in the thoracic spine and anterior spinal hyperostosis. He had a Japanese Orthopaedic Association score of 6 points preoperatively, and he underwent laminoplasty from the third through the seventh cervical vertebra. Postoperatively, the main symptoms (including spastic gait and clumsiness in both upper extremities) resolved and his score improved to 15 points. Nine years after the procedure, he had numbness in the right arm. Substantial progression of the ossification in the cervical region was observed on radiographs. At the third and fourth cervical levels, anterior compression of the spinal cord due to the progression of the ossification was obvious on magnetic resonance images. Fig. 2-A Preoperative tomogram of the cervical spine. Fig. 2-B Tomogram, made ten years after the laminoplasty, revealing a substantial increase in the thickness of the ossification at the third and fourth cervical levels.

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Fig. 2-B:: Figs. 2-A, 2-B, and 2-C Case 41. This forty-four-year-old man had the continuous type of ossification from the second through the seventh cervical level. He also had ossification in the thoracic spine and anterior spinal hyperostosis. He had a Japanese Orthopaedic Association score of 6 points preoperatively, and he underwent laminoplasty from the third through the seventh cervical vertebra. Postoperatively, the main symptoms (including spastic gait and clumsiness in both upper extremities) resolved and his score improved to 15 points. Nine years after the procedure, he had numbness in the right arm. Substantial progression of the ossification in the cervical region was observed on radiographs. At the third and fourth cervical levels, anterior compression of the spinal cord due to the progression of the ossification was obvious on magnetic resonance images. Fig. 2-A Preoperative tomogram of the cervical spine. Fig. 2-B Tomogram, made ten years after the laminoplasty, revealing a substantial increase in the thickness of the ossification at the third and fourth cervical levels.

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Fig. 2-C:: Postoperative magnetic resonance image showing substantial spinal cord compression due to the ossification.

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TABLE I: Comparison of the Clinical Results Between the Groups with and without Progression of Ossification

*The values are given as the mean and the standard deviation. †JOA = Japanese Orthopaedic Association.

	Progression (N = 33)	No Progression (N = 12)	P Value
Age* (yr)	53.3 8.6	60.2 7.3	0.018
Cervical alignment* (deg)	?1.8 13.9	?1.2 7.8	0.86
Range of motion of the cervical spine* (deg)	?5.2 6.1	?8.5 9.8	0.29
No. of fused laminae*	?3.8 1.2	?3.5 1.6	0.56
Recovery rate based on JOA score*† (%)	57.9 37.2	46.7 40.9	0.39
No. of patients with axial symptoms*	16	4	0.37

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TABLE I: Comparison of the Clinical Results Between the Groups with and without Progression of Ossification

*The values are given as the mean and the standard deviation. †JOA = Japanese Orthopaedic Association.

	Progression (N = 33)	No Progression (N = 12)	P Value
Age* (yr)	53.3 8.6	60.2 7.3	0.018
Cervical alignment* (deg)	?1.8 13.9	?1.2 7.8	0.86
Range of motion of the cervical spine* (deg)	?5.2 6.1	?8.5 9.8	0.29
No. of fused laminae*	?3.8 1.2	?3.5 1.6	0.56
Recovery rate based on JOA score*† (%)	57.9 37.2	46.7 40.9	0.39
No. of patients with axial symptoms*	16	4	0.37

Materials and Methods

Seventy-one patients underwent en bloc cervical laminoplasty between 1982 and 1988 at our hospital for the treatment of cervical myelopathy due to ossification of the posterior longitudinal ligament. Of the seventy-one patients, twenty-two died during the follow-up period. No patient died from complications related to the operation, and there was no obvious relationship between the cause of death and progression of ossification. Forty-nine patients remained for inclusion in this study, and forty-five (92%) of them were followed for a mean of 13.1 years (range, ten to seventeen years); the remaining four patients were lost to follow-up. The follow-up evaluation included physical and radiographic examinations. The physical examination was performed by three senior spinal surgeons (Y.K., M.K., and H.I.). Radiographic findings were assessed by two spinal surgeons (Y.K. and H.N.) and an orthopaedic surgeon (K.S.). There were thirty-two men and thirteen women, with an average age of 55.2 years (range, forty-two to seventy-five years) at the time of the operation.

En bloc laminoplasty, as described by Itoh and Tsuji^2,3,13, was used for decompression of the spinal cord in all of the patients. The details of the operative procedure have been described previously². Decompression of the spinal canal was performed from the third cervical vertebra to the seventh cervical or first thoracic vertebra. The patients were required to stay in bed for the first week after surgery, and thereafter they were allowed to walk while wearing a sternal-occipital-mandibular immobilizer brace. The orthotic device was worn for up to two months after surgery, and the use of a neck collar for one additional month was recommended.

Radiographs of the cervical spine were made for all of the patients before and after the operation and at the latest follow-up examination. Anteroposterior and lateral (neutral and flexion-extension) radiographs were made with a constant distance from the tube to the film and from the spine to the film. A sagittal tomogram of the cervical spine was also made preoperatively and at the time of the latest follow-up. Ossification types were classified as continuous, segmental, mixed, and other according to the criteria proposed by the Investigation Committee on the Ossification of the Spinal Ligaments of the Japanese Ministry of Public Health and Welfare (Fig. 1)⁹. The extent of ossification in the longitudinal axis was evaluated on radiographs, and the anterior-posterior thickness of the area of ossification in the sagittal axis was determined on lateral tomograms. Progression of the ossification was defined as an increase of 2 mm in the longitudinal extent and/or the sagittal thickness. The space available for the spinal cord in the cervical spine was measured as the distance between the posterior aspect of the ossification and the nearest posterior structure on lateral radiographs. Postural alignment of the cervical spine was defined as lordosis or kyphosis on the basis of the angle between lines passing through the inferior margin of the second cervical vertebral body and the inferior margin of the sixth or seventh cervical vertebral body on the lateral neutral radiograph. A lordotic angle was represented as a positive value and a kyphotic angle, as a negative value. In addition, the range of motion of the cervical spine was measured as the change in the angle described above on flexion and extension dynamic radiographs. The number of fused laminae was also determined. Osseous fusion was considered present in the expanded laminae if there was consolidation of the grafted bone on the neutral lateral radiograph or tomogram made at the latest follow-up examination.

Neurological function was graded according to the scale devised by the Japanese Orthopaedic Association¹⁴. The rate of recovery was calculated with use of the following formula: [postoperative score — preoperative score] 100 / [17 (score for full recovery) — preoperative score].

The relationship between the progression of ossification of the posterior longitudinal ligament and the Japanese Orthopaedic Association score-based rate of recovery was analyzed. Furthermore, postoperative axial symptoms such as pain and/or stiffness in the neck or shoulder were also evaluated.

Statistical Analysis

Data are presented as the mean value and the standard deviation. A t test with Welch’s correction was used for statistical analysis of the difference between the mean preoperative and postoperative scores. The same statistical method was used for analysis of the effect of preoperative factors on the postoperative clinical results. The Mann-Whitney test was used for statistical analysis of the difference in the extent of progression among the different types of ossification. A p value of <0.05 was considered significant.

Results

The continuous type of ossification was observed in thirteen patients; the segmental type, in twelve; the mixed type, in eighteen; and the other type, in two. At the time of the latest follow-up, the pattern of ossification had changed from mixed to continuous in ten patients, from segmental to mixed in two patients, from segmental to continuous in one patient, and from other to continuous in one (see Appendix). The mixed type frequently changed (ten of eighteen changed), whereas the segmental type rarely did (three of twelve changed).

Thirty-three (73%) of the forty-five patients had progression of ossification after laminoplasty. The progression occurred in the longitudinal axis in thirty-one patients, and the thickness increased in nineteen. The average extent of progression in the longitudinal axis was 9.0 ± 10.5 mm, and the average increase in thickness was 1.3 ± 1.7 mm. Progression was common in patients with the mixed or continuous type, whereas it was rare in those with the segmental type. The average age of the patients with progression in either dimension was 53.3 ± 8.6 years, whereas the average age of those without progression was 60.2 ± 7.3 years. This difference was significant (p = 0.018). There was no consistent relationship between progression of the ossification and the cervical alignment (p = 0.86), the range of motion of the cervical spine (p = 0.29), or the number of fused laminae (p = 0.56) (Table I).

The Japanese Orthopaedic Association score improved rapidly within one year and continued to improve for up to five years after surgery. The mean score increased from 8.7 points preoperatively to 14.2 points, and the recovery rate was 63.3% at five years postoperatively. After five years, however, the score tended to decrease. Progression of the ossification was not related to the score-based recovery rate (Table I). There were thirteen patients (ten men and three women) whose score had worsened at the time of the latest follow-up. Three patients had neurological deterioration from an increase in the thickness of the ossification (Figs. 2-A, 2-B, and 2-C). The space available for the spinal cord in the patients with neurological deterioration was narrower than the average space in all of the patients throughout the postoperative course. Other causes of worsening of the Japanese Orthopaedic Association score were lumbar spinal stenosis in three patients; cerebral infarction in two patients; and progression of diabetic neuropathy, atherosclerosis and spread of thoracic ossification, and total knee arthroplasty in one patient each. The cause was unknown in one patient.

Preoperative axial symptoms were observed in six patients (13%). The primary symptoms were pain and/or stiffness in the neck or shoulder. The prevalence of postoperative axial symptoms was 44% (twenty patients). However, there was no significant relationship between progression of the ossification and postoperative axial symptoms (p = 0.37) (Table I).

Discussion

Posterior decompression of the spinal canal has been our preferred method for the treatment of neurological deterioration due to ossification of the posterior longitudinal ligament. However, posterior decompression has the disadvantage of leaving ossific lesions in the anterior part of the spinal canal.

There have been few reports concerning the effect of progression of ossification on the outcome of surgical decompression^10-12. Hirabayashi et al. reported that the outcome of patients with progression tended to be worse than that of patients without progression¹⁰. In the present study, although there was no association between progression and the rate of postoperative recovery, three patients had deterioration of postoperative neurological function due to progression after laminoplasty. In all of the patients with deterioration of neurological function, the posterior decompression had resulted in a relatively narrower space available for the spinal cord at surgery and there was an increase in the thickness of the ossification after surgery. An increase in the thickness of the ossification decreases the space available for the spinal cord and might result in stenosis of the spinal canal.

The results of the current study show that young patients with a mixed or continuous type of ossification of the posterior longitudinal ligament have a higher risk for progression of ossification. This finding is in agreement with that of a previous report¹⁵. Increased ossification resulted in worsened neurological function in some patients. Therefore, preventive measures should be considered for patients who are at risk for progression. It has been reported that oral administration of etidronate disodium might be effective in preventing the progression of ossification following surgical decompression in patients with ossification¹⁶. The effects of various doses of etidronate disodium were analyzed, and 1000 mg administered cyclically for two years was found to be effective in preventing the progression. As for surgical treatment, anterior decompression might be indicated in some patients. However, anterior decompression is more difficult to perform than posterior decompression in patients with multilevel spinal cord compression. Yonenobu et al. reported no difference in surgical outcome between a group managed with posterior decompressive surgery and a group managed with anterior decompressive surgery, but surgical complications were more frequent in the latter group¹⁷. Many spinal surgeons agree that anterior decompressive surgery can be performed safely and easily in patients with single or two-level lesions¹⁸. Thus, we believe that laminoplasty offers the best treatment for myelopathy due to multisegmental ossification. In our series, three patients who had neurological deterioration due to an increase in the thickness of the ossification had a decompression that resulted in a narrower space at surgery. In contrast, the patients with a wider laminar opening had no neurological deterioration, although some of them had an increase in the thickness of the ossification. Therefore, a wider opening of the laminae should be considered, especially in patients who have an increased risk for progression of ossification after surgery.

Appendix

A table showing clinical characteristics of all forty-five patients is available with the electronic versions of this article, on our web site at www.jbjs.org (go to the article citation and click on "Supplementary Material") and on our quarterly CD-ROM (call our subscription department, at 781-449-9780, to order the CD-ROM).

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Fig. 2-C:: Postoperative magnetic resonance image showing substantial spinal cord compression due to the ossification.

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TABLE I: Comparison of the Clinical Results Between the Groups with and without Progression of Ossification

*The values are given as the mean and the standard deviation. †JOA = Japanese Orthopaedic Association.

	Progression (N = 33)	No Progression (N = 12)	P Value
Age* (yr)	53.3 8.6	60.2 7.3	0.018
Cervical alignment* (deg)	?1.8 13.9	?1.2 7.8	0.86
Range of motion of the cervical spine* (deg)	?5.2 6.1	?8.5 9.8	0.29
No. of fused laminae*	?3.8 1.2	?3.5 1.6	0.56
Recovery rate based on JOA score*† (%)	57.9 37.2	46.7 40.9	0.39
No. of patients with axial symptoms*	16	4	0.37

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TABLE I: Comparison of the Clinical Results Between the Groups with and without Progression of Ossification

*The values are given as the mean and the standard deviation. †JOA = Japanese Orthopaedic Association.

	Progression (N = 33)	No Progression (N = 12)	P Value
Age* (yr)	53.3 8.6	60.2 7.3	0.018
Cervical alignment* (deg)	?1.8 13.9	?1.2 7.8	0.86
Range of motion of the cervical spine* (deg)	?5.2 6.1	?8.5 9.8	0.29
No. of fused laminae*	?3.8 1.2	?3.5 1.6	0.56
Recovery rate based on JOA score*† (%)	57.9 37.2	46.7 40.9	0.39
No. of patients with axial symptoms*	16	4	0.37