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�:	Abstract
Objective: Expansive laminoplasty has become the gold standard for surgical treatment of cervical multilevel compressive myelopathy. The procedure preserves the motion segment, and it has been believed hitherto that adjacent segment disease would not occur following the procedure. We report the adjacent segment disease following expansive laminoplasty for compressive cervical myelopathy and postulate on the possible pathophysiologic mechanism of the disease.
Methods: We retrospectively reviewed five cases that were considered to have adjacent segment disease following cervical expansive laminoplasty. We evaluated the following: 1) the time period between primary cervical laminoplasty and the additional surgery; 2) the type of primary laminoplasty; 3) the range of bony fusion before the additional surgery; 4) the pathology of the adjacent disease; 5) the methods used for the additional surgery.
Results: The mean time period between the primary cervical laminoplasty and the additional surgery was 12.8 years. The causes of the recurrence or the deterioration of myelopathy were retro-odontoid pseudotumor, atlanto-axial dislocation, and the compressive myelopathy at the cervico-thoracic level. The plain radiographs showed spontaneous long bony fusion with bridging callus at the primary operated site. CT showed that bony fusion was obtained at both interlaminar space and lateral gutter site in all cases except the open-side in the open-door laminoplasty cases. A laminectomy at C1, a partial laminectomy at C2 and a fusion surgery at C0-C2 with bone graft and instrumentation were performed for 1 case, a laminectomy at C1 and a fusion surgery at C1-C2 with transarticular screws were performed for 2 cases, and the additional laminoplasty at T1 and T2 were performed for 2 cases.
Conclusions: We postulated that the spontaneous long bony fusion at the multi-level cervical spine possibly caused continuous mechanical stress at the adjacent level. This could be the pathophysiological mechanism of adjacent segment disease. 
Key Words: laminoplasty; adjacent segment disease; myelopathy, recurrence





Introduction

Expansive laminoplasty for compressive cervical myelopathy was developed by Hirabayashi in 1978 [1,2]. Over the past 30 years the procedure has received a number of modifications; these modifications have resulted in improvements to the procedure [2-19]. Expansive laminoplasty has become the gold standard for surgical treatment of cervical multilevel compressive myelopathy.
The procedure preserves the motion segment, and hitherto it has been believed that adjacent segment disease would not occur following the procedure. A case-series of the adjacent segment disease has never been reported.
The authors of this report experienced five cases of the adjacent segment disease following expansive laminoplasty for compressive cervical myelopathy. Our purpose here is to present these five cases and to postulate on the possible pathophysiologic mechanism of adjacent segment disease.


Materials and Methods

We retrospectively reviewed five cases that were considered to have adjacent segment disease following cervical expansive laminoplasty. These five cases underwent additional surgery (see the Results) between 2010 and 2011 at our institute or our associated hospital. The five consisted of three males and two females. At the time of the additional surgery, their ages ranged from 61 to 84 years (mean age, 74.2 years). The clinical records and the various images were analyzed. We evaluated the following: 1) the time period between primary cervical laminoplasty and the additional surgery; 2) the type of primary laminoplasty; 3) the range of bony fusion before the additional surgery; 4) the pathology of the adjacent disease; 5) the methods used for the additional surgery.





Results

In all five cases the preoperative symptoms improved following the primary cervical expansive laminoplasty. However, more than ten years following the primary surgery the additional surgery was required in all patients because of the recurrence or the deterioration of myelopathy. The time period between the primary cervical laminoplasty and the additional surgery ranged from 11 to 16 years (mean period, 12.8 years). The causes of the recurrence or the deterioration of myelopathy were: 1) Two cases of retro-odontoid pseudotumor; 2) One case of atlanto-axial dislocation; and 3) Two cases of the compressive myelopathy at the levels of C7/T1 and T1/T2. The primary cervical laminoplasties were performed at C3-6, C3-7 and C3-T1 on one, three and one cases respectively. The plain radiographs showed spontaneous long bony fusion with bridging callus at the primary operated site. CT showed that bony fusion was obtained at both the interlaminar space and the lateral gutter in all cases except the open-side in the open-door laminoplasty cases (see the Table). A bony fusion was also present between the autografted bones in the cases in which iliac bone had been used as a spacer between expanded laminas. Two open-door and three French-door laminoplasties had been performed as a primary surgery (see the Table). The bony fusion ranged from C2 to T1 and from C2 to C7 in the upper cervical lesions and cervico-thoracic lesions, respectively. A laminectomy at C1, a partial laminectomy at C2 and a fusion surgery at C0-C2 with bone graft and instrumentation were performed for 1 case, a laminectomy at C1 and a fusion surgery at C1-C2 with transarticular screws were performed for 2 cases, and the additional laminoplasty at T1 and T2 were performed for 2 cases (see the Table).









Case presentation

Case 1

An 81-year-old woman, who had undergone cervical open-door laminoplasty at another university hospital fourteen years previously, consulted our institute because of the deterioration of the spastic quadriparesis. Her previous clumsiness and gait disturbance had been improved by the initial surgery. She now complained of clumsiness in both hands, motor weakness in her upper and lower extremities and gait disturbance. Physical examination revealed deep tendon hyper-reflexia in both arms and legs, positive stretch reflexes such as Hoffmann and Tr�mner reflexes and positive pathological reflex such as Babinski reflex. Her score for cervical myelopathy, according to the criteria proposed by the Japanese Orthopedic Association (JOA score), was 6 out of 17 points (motor: 0/8, sensory: 3/6, bladder and bowel dysfunction: 3/3).
Plain radiograph and CT showed: 1) enlargement of the cervical spinal canal at C3-C7; 2) spontaneous long bony fusion with bridging callus in both the interlaminar space and the hinge-side lateral gutter at C2-T1; and 3) calcified mass lesion behind the dens of the axis. Magnetic resonance imaging (MRI) revealed severe spinal cord compression by retro-odontoid pseudotumor (Figure 1). 
A laminectomy at C1, a partial laminectomy at C2 and a fusion surgery at C0-C2 with bone graft and instrumentation were performed (Figure 2). The tumor tissue, which was partially resected during the surgery, was confirmed by pathological examination as a pseudotumor including granulation tissue with increased capillary vessels, macrophages, lymphocytes and mineral deposition. Her spasticity, motor weakness and gait disturbance gradually improved after surgery. Her JOA score improved to 11 points (motor: 4/8, sensory: 4/6, bladder and bowel dysfunction: 3/3) at 1 month after surgery.






Case 2

A 61-year-old man, who had undergone cervical open-door laminoplasty at another hospital fourteen years previously, was referred to our institute by his family doctor. His previous clumsiness and gait disturbance had been improved by the initial surgery. His chief complaints were the deteriorations of motor weakness in his left leg and gait disturbance. He showed spasticity in his lower extremities. Physical examination revealed the marked limitation of neck range of motion, deep tendon hyperreflexia in both arms and legs, and positivity in Babinski reflex. His JOA score for thoracic myelopathy was 6.5 out of 11 points (motor: 1.5/4, sensory: 2/4, bladder and bowel dysfunction: 3/3).
Plain radiograph and CT showed enlargement of the cervical spinal canal at C3-C7 and spontaneous long bony fusion with bridging callus in both interlaminar space and hinge-side lateral gutter at C2-C7. MRI, myelogram and CT myelogram revealed severe spinal cord compression at C7/T1 and T1/T2 (Figure 3).
An additional French-door laminoplasty, using resected spinous process, was performed at T1 and T2 (Figure 4). His spasticity and gait disturbance were improved and his JOA score for thoracic myelopathy improved to 9 points (motor: 2.5/4, sensory: 3.5/4, bladder and bowel dysfunction: 3/3) one year after surgery.














Discussion

Some previous reports described the recurrence or the late deterioration of myelopathy following expansive laminoplasty for cervical myelopathy. These reports pointed out the decreased sagittal diameter of the spinal canal, progression of the ossification of the posterior longitudinal ligament (OPLL), and the kyphotic change in the alignment of cervical spine as being the causes of the deterioration or recurrence [20-23]. Hitherto it has been believed that adjacent segment disease would not occur following expansive laminoplasty since the procedure preserves the motion segment. As far as we aware this report is the first case-series describing adjacent segment disease following cervical expansive laminoplasty, which explains the recurrence or the late deterioration of myelopathy after cervical laminoplasty.
It is important to note that the cases reviewed in this study are ones that were followed more than 10 years after the initial cervical laminoplasty (mean period, 12.8 years). At the time of the initial surgery, the motion of the operated site was restricted after surgery by bed rest and external fixation (such as a brace) for long periods. The bracing was often enforced for six months. Such restriction was thought to be important to keep the cervical alignment lordosis and protect the spinal cord. However this restriction could lead to spontaneous bony fusion at the interlaminar spaces. Furthermore, we should also consider the consequences of using autograft iliac bone as a spacer and placing chipped bone onto the lateral gutter. These also could facilitate the long bony fusion while they enabled the cervical spine to keep the lordotic alignment and allow a stable reconstruction, which lead to the long-term postoperative satisfactory outcome. Such bony fusion could have sent continuous mechanical stress to the adjacent level, resulting in adjacent segment disease. Could this be the pathophysiological mechanism of an adjacent segment disease as seen in our five cases? (Figure 5) Takagi et al. reported the T1/T2 disc herniation following an en bloc cervical laminoplasty. The report pointed to a similar mechanism [24].
Adjacent segment disease presented in this study consisted of 3 cases of upper cervical lesions and 2 cases of cervico-thoracic lesions. The bony fusion ranged from C2 to T1 and from C2 to C7 in the upper cervical lesions and cervico-thoracic lesions, respectively. In the case of bony fusion ranging from C2 to T1, motion remained only at C1/2. This could be why adjacent segment disease occurred not in cervico-thoracic level but in upper cervical level. Retro-odontoid pseudotumor was reported to occur resulting from the instability at C1/2 [25]. On the other hand, in the case of bony fusion ranging from C2 to C7, mechanical stress seems to focus on the cervico-thoracic level more than the upper cervical level.
Two open-door and three French-door laminoplasties made up the five cases in this study. Spontaneous long bony fusion with bridging callus was observed in both interlaminar space and lateral gutter in all five cases. This indicated that both laminoplasties similarly lead to spontaneous bony fusion between laminas.
We chose the additional French-door laminoplasty for the cervico-thoracic lesion and the posterior decompression and fusion surgery for the upper cervical lesion. These procedures resulted in satisfactory outcomes in all five cases. Retro-odontoid pseudotumor has been reported to disappear by stabilizing C1-2 [25]. That is the reason why we performed only posterior procedure without the resection of the tumor for the retro-odontoid pseudotumor cases.
In recent years, minimally invasive surgical procedures such as skip laminectomy [26,27] and microendoscopic laminotomy [28] have been developed for multilevel cervical compressive myelopathy. These procedures were originally developed to reduce the prevalence of axial pain by preserving the cervical posterior stabilizer. On the other hand, these procedures resulted in good preservation of the motion of cervical spine by minimizing the invasion to the lamina. It has been recently emphasized that neck ROM exercises should be begun as soon as possible after the cervical laminoplasy. The purpose is to avoid the axial pain. However these exercises are also beneficial in preserving the motion of the cervical spine. Thus if such motion-preservation techniques and the method of postoperative ROM exercises become so common, the diseases reviewed in this study will never occur.
When there is deterioration or recurrence of myelopathy long-term after the cervical laminoplasty, adjacent segment disease should be suspected. The cases reviewed in this report draw attention to the importance of long-term follow-up after cervical laminoplasty.




References

1.	Hirabayashi K. Expansive open-door laminoplasty for cervical spondylotic myelopathy [in Japanese]. Shujutsu 1978;32:1159-63.
2. 	 HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/7593114?ordinalpos=192&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVDocSum" Hirabayashi K, Watanabe K, Wakano K, Suzuki N, Satomi K, Ishii Y. Expansive open-door laminoplasty for cervical spinal stenotic myelopashy. Spine 1983;8:693-9.
3. 	Tsuji H. Laminoplasty for patients with compressive myelopathy due to so-called spinal canal stenosis in cervical and thoracic regions. Spine 1982;7:28-34.
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Figure legends

Figure 1. Preoperative imaging studies for Case 1. Plain radiograph showed enlargement of the cervical spinal canal and spontaneous long bony fusion in the posterior column. MRI revealed the severe spinal cord compression by retro-odontoid pseudotumor. CT showed calcified mass lesion behind the dens of axis. a: Lateral view of plain radiograph. b: Sagittal T2-weighted image. c: Axial T2-weighted image. d: Reconstructed CT. e: Conventional CT at C1.

Figure 2. Postoperative imaging studies for Case 1. A laminectomy at C1, a partial laminectomy at C2 and a fusion surgery at C0-C2 with bone graft and instrumentation were performed. The spinal cord was adequately decompressed. a: Lateral view of plain radiograph. b: Axial T2-weighted image.

Figure 3. Preoperative imaging studies for Case 2. Plain radiograph and CT showed enlargement of the cervical spinal canal and spontaneous long bony fusion in the posterior column. MRI and CT myelogram revealed the spinal cord compression at C7/T1 and T1/T2. a: Lateral view of plain radiograph. b: Posterior view of three-dimensionally reconstructed CT. c: Sagittal T2-weighted image. d: Axial T2-weighted image at C7/T1. e: Axial T2-weighted image at T1/T2. f: Reconstructed CT myelogram. g: Conventional CT myelogram at C7/T1. h: Conventional CT myelogram at T1/T2. 

Figure 4. Postoperative imaging studies for Case 2. Additional French-door laminoplasty using resected spinous process was performed at T1 and T2. The spinal cord was adequately decompressed. a: CT at C7/T1. b: CT at T1/T2. c: Sagittal T2-weighted image. d: Axial T2-weighted image at C7/T1. e: Axial T2-weighted image at T1/T2.

Figure 5. Scheme for the possible pathophysiologic mechanism of the adjacent segment diseases following cervical laminoplasty. The possible causes of multi-level spontaneous bony fusion are 1) long-term bed rest and bracing; 2) 	+19����			"	#	$	,	-	K	T	�	�	�	�	�	�������������{k\k{k{Lh�=JhB75�PJnHo(tHh�=Jh_,PJaJnHtHh�=Jh_,PJaJnHo(tHh�=JhB7PJaJnHo(tHh�K�PJaJnHtHh�K�PJaJnHo(tHh�=Jh�+�PJaJnHtHh�=Jh�+�PJaJnHo(tHh�+�PJaJnHo(tHh4R5�PJaJnHo(tH"h�=JhB75�PJaJnHo(tHh�+�5�PJaJnHo(tH	�	�NOPQRS`a�������������������������������$a$gd�g�$��`��a$gd�g�$��`��a$gdB7$
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