An Evidence-Based Stepwise Surgical Approach to Cervical Spondylotic Myelopathy: A Narrative Review of the Current Literature

Accepted Manuscript An Evidence-Based Stepwise Surgical Approach to Cervical Spondylotic Myelopathy: A Narrative Review of the Current Literature Majid Reza Farrokhi, MD, Fariborz Ghaffarpasand, MD, Mehdi Khani, MD, Mehrnaz Gholami, MA PII:

S1878-8750(16)30497-1

DOI:

10.1016/j.wneu.2016.06.109

Reference:

WNEU 4268

To appear in:

World Neurosurgery

Received Date: 2 April 2016 Revised Date:

25 June 2016

Accepted Date: 27 June 2016

Please cite this article as: Farrokhi MR, Ghaffarpasand F, Khani M, Gholami M, An Evidence-Based Stepwise Surgical Approach to Cervical Spondylotic Myelopathy: A Narrative Review of the Current Literature, World Neurosurgery (2016), doi: 10.1016/j.wneu.2016.06.109. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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An Evidence-Based Stepwise Surgical Approach to Cervical Spondylotic Myelopathy: A Narrative Review of the Current Literature

Majid Reza Farrokhi, MD1*, Fariborz Ghaffarpasand, MD1, Mehdi Khani, MD1, Mehrnaz

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Gholami, MA2

Department of Neurosurgery, Shiraz Neuroscience Research Center, Shiraz University of

Shiraz Neuroscience Research Center, Shiraz University of Medical Sciences, Shiraz, Iran.

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Medical Sciences, Shiraz, Iran.

Conflict of Interest: There is no conflict of interest to be declared regarding the manuscript. Source of Funding: This article has no source of funding.

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Short Title: An evidence-based stepwise surgical approach to CSM.

* Corresponding author:

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Majid Reza Farrokhi, MD Professor of Neurosurgery

Shiraz Neuroscience Research Center

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Neurosurgery Department

Shiraz University of Medical Sciences Shiraz, Iran

Address for correspondence: Prof. Majid Reza Farrokhi, Shiraz Neuroscience Research Center, Chamran Hospital, Chamran Boulevard, Shiraz, Iran. PO Box: 7194815644 Tel/ Fax: +9871-36234508 E-mail: [email protected] 1

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An Evidence-Based Stepwise Surgical Approach to Cervical Spondylotic

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Myelopathy: A Narrative Review of the Current Literature

Abstract

Cervical spondylotic myelopathy (CSM) is the most common progressive degenerative disease of the spine in geriatric population. Surgery remains the mainstay of the treatment in

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patients with CSM. The surgical approach should be based on cervical sagittal imbalance. In patients with effective cervical lordosis (fewer than 3 levels of ventral disease), the anterior

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cervical discectomy and fusion (ACDF) or arthroplasty is preferred. Patients with more than 3 levels of compression are generally treated by laminoplasty, especially with preserved lordotic curvature. In patients with straightened spine who have less than 3 involved levels, ACDF with plate is recommended while the patients with more than 3 involved levels with instability should undergo posterior decompression and fusion. In young patients, who have stable cervical spine, laminoplasty is recommended and in old patients with ankylosed spine,

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only laminectomy should be performed. Patients with mild cervical kyphosis (kyphotic angle ≤ 10°) should be managed like patients with straightened spine. However, in severe kyphosis, cervical traction is recommended. If the kyphosis is reducible, further posterior decompression and fusion is adequate. In irreducible patients, if the number of involved levels

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is less than 2 levels, ACDF is adequate, but if it is > 2 levels, anterior cervical corpectomy and fusion should be performed using cervical magnetic resonance imaging for evaluation of

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the patency of subarachnoid space (SAS). In patent SAS, only posterior fusion is adequate while in closed SAS, posterior decompression with posterior fusion is required. These approaches are based on the most recent lines of evidence.

Keywords: Cervical spondylotic myelopathy • Surgery • Conservative care • Stenosis • Stepwise approach • Straightened spine • Cervical kyphosis • Anterior cervical discectomy • Posterior cervical fusion 2

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Context Introduction Epidemiology Pathophysiology and natural course

Cervical sagittal balance and imbalance Approach to patients with normal cervical lordosis Approach to patients with straightened spine Approach to patients with cervical kyphosis

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Complications

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Neurophysiological findings

Summary

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Conclusion References

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Figure Legends

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INTRODUCTION Cervical spondylotic myelopathy (CSM) is the most common progressive degenerative disease of the spine in geriatric population, leading to a high social and economic burden.1-3 The radiologic evidence of CSM is reported in more than 50% of the middle-age patients

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while only 10% of patients suffer from clinical cord or root compression.4 CSM is defined as a part of a spectrum of cervical spine degeneration ranging from neck pain to radiculopathy or myelopathy. CSM is a complex neurosurgical entity which requires various operative and non-operative managements.5-7 Previous systematic review has demonstrated that low levels of evidence support the role of non-operative management in the mild CSM. In those with

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moderate to severe CSM, non-operative management is prohibited7 because this option has been shown to have outcomes inferior to those of surgery.8 Given the unpredictably

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progressive nature of cervical myelopathy, the indications for non-operative management are ostensibly limited.7,8 Based on results from a systematic review, approximately 20% to 60% of patients with symptomatic and radiological features of CSM will deteriorate overtime if not treated surgically.9 Therefore, surgery remains the mainstay of the treatment in patients with CSM. In the past decade, our understanding of the biomechanics of the spine has improved along with advances in spinal instrumentation and this has led to significant

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changes in the surgical management of CSM. Preservation or improvement of neurologic function, correction of sagittal or coronal deformity and maintaining the cervical spine stability are the main aims of the surgical intervention. The choice of surgical intervention in

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CSM mainly depends on clinical condition and the surgeon’s choice. The choice of operative procedure should take into consideration the individual patient's clinical and radiological characteristics, age, co-morbidities, lifestyle (smoking etc.), procedure-specific risks and

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finally, the experience and comfort level of the surgeon with various surgical procedures. Studies, including the AOSpine International multicenter prospective study, have also shown that the majority of the spine surgeons prefer the anterior approach in 51-60% of cases, posterior approach in about 35% and a combined approach in the remaining.10,11 Anterior approach appears to be more suitable when the pathologies of anterior involve only 1 or 2 vertebral body levels, while if more than 2 levels usually proceed using an posterior approach clinically.12 A systematic review of literature demonstrated that, for both effectiveness and safety, there was no clear advantage to either an anterior surgical approach or a posterior surgical approach when treating patients with multilevel CSM, but the overall strength of the 4

ACCEPTED MANUSCRIPT evidence was low.13 There’s no consensus among experts about the best way to perform the surgery to ease CSM. Recently, some researchers are conducting a Patient Centered Outcomes Research Institute (PCORI) study about CSM to find the best surgical method, but their findings have not been published yet.14 Although it is generally agreed that surgical intervention positively impacts the prognosis of CSM, the decision algorithm for the selection

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of the most appropriate surgical technique is complex. Several studies have addressed the issue extensively,6,8,15-17 but none of them provided a stepwise practical approach for surgical management of CSM. The aim of the current review is to provide an evidence-base stepwise

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surgical approach to CSM according to the recent literature.

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EPIDEMIOLOGY

CSM is considered to be the most common degenerative disease of the spinal column in patients older than 55 years.3,4 Age and comorbid conditions, such as hypertension, lung disease, diabetes, and obesity, as predictors of adverse surgical events are also important factors in choosing an appropriate surgical approach.18 In a study conducted by Boakye et al.18, the authors showed that in patients with CSM undergoing anterior cervical discectomy

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and fusion (ACDF), age is the most important indicator of the outcome. It is clearly demonstrated that the degree of cervical lordosis increases by the age and the increase in the lordosis is significantly higher in women compared to men (–25 ± 16 vs. –22 ± 13, respectively).19 Although the disease is common and associated with high socioeconomic

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burden, a recent meta-analysis reported that the literature did not include any article reporting an incidence or prevalence of CSM.1 According to this study, the annual incidence of CSM

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was 1.6 per 100,000 inhabitants based on the number of patients who underwent operation and those who were screened in the outpatient clinics.1 The reported mean age was 62.1 ± 10.6 (range 34.5–80.9) years with a male predominance (52.5%).1 According to some studies, the prevalence of CSM accounts for 10% ~ 15% of cervical spondylosis.20,21 A national cohort study in Taiwan reported that an overall incidence of CSM-related hospitalization is 4.04 per 100,000 person-years.4 Men and older patients had a higher incidence of CSM.4 This study reported that the incidence of spinal cord injury in those with CSM is 12.33 per 1000 person-years4 which is extremely higher when compared to general population (0.13 per 1000 person-years).22 Another recent study in England also reported a male to female ratio of 5

ACCEPTED MANUSCRIPT approximately 2.7:1, with an average age of 63.8 years at the diagnosis. Multi-level disease was seen in the majority of patients, with C5-C6 being the most commonly affected level.3 In Rochester, the average annual age-adjusted incidence rates per 100,000 populations were 83.2 for the total, 107.3 for males and 63.5 for females. The age-specific annual incidence rate per 100,000 populations reached a peak of 202.9 for the age group 50-54 years.23 The prevalence

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of CSM in Italy was also reported to be 3.5 per 1,000 inhabitants which increased to a peak at age 50-59 years, and decreased thereafter. The age-specific prevalence was consistently higher in women contrary to other reports.24

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PATHOPHYSIOLOGY AND NATURAL COURSE

CSM is considered to be the result of both static and dynamic mechanical factors which

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compress the cord resulting in myelopathy.25 Static mechanical factors refer to structural abnormalities and degenerative spondylotic changes of the cervical spinal column such as osteophyte and spur formations, ossification of the posterior longitudinal ligament, ligamentum flavum hypertrophy and kyphosis and subluxation of the cervical spine which result in physical narrowing of the spinal canal or direct compression of the cervical spinal

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cord.17,26,27 Dynamic mechanical factors refer to pathologies associated with cervical motion (flexion and extension). Dynamic factors result from static factors which have previously narrowed the cervical canal. Flexion and extension of the stenotic cervical canal leads to compression of the spinal cord towards the osteophytes and hypertrophied ligamentum

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to myelopathy.

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flavum, respectively.28 These continuous and chronic micro-traumas along with ischemia lead

Although several studies have investigated the natural history of untreated CSM, the subject still remains unclear.9,29-31 A recent meta-analysis of the current literature revealed that 20% to 60% of the patients would deteriorate neurologically over time without surgical intervention (moderate strength of evidence).9 This study also indicated that there is low strength of evidence indicating that the area of circumferential compression is associated with deteriorating neurological symptoms.9 According to the results of several studies which evaluated the outcome of non-operative management of CSM,29-31 it can be concluded that even in patients with mild CSM, surgery should be recommended. Even patients with mild 6

ACCEPTED MANUSCRIPT CSM demonstrate progressive course, especially those who are older than 65 years. This is because chronic compression of the spinal cord results in progressive neural cell loss following apoptosis, neuroinflammation, and vascular disruption.30,32 Those with mild CSM should be consulted regarding the natural course of the disease and surgery should be

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recommended.

NEUROPHYSIOLOGICAL FINDINGS

CSM has a variable course and different possible treatment strategies. In order to choose the

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best treatment strategy, patients with CSM must be evaluated with neuroimaging and neurophysiology.33,34 The neurophysiological evaluation often includes electromyography

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(EMG), electroneurography (ENG), and evoked potentials.33,35 EMG performed with needle electrodes is the oldest method for diagnosing nerve root compression and anterior horn cell syndromes, and is claimed to have no false-positive results.33,36 Sensory evoked potentials (SEPs) by stimulation of tibial nerve and motor evoked potentials (MEPs) from the upper and lower extremities are easy, non-invasive diagnostic tests which are recommended for the differential diagnosis of CSM.33,34,37-40 While SEPs and MEPs are valuable tools in

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documenting the functional involvement of somatosensory and motor pathways in myelopathy,33,36,38,39,41-43 EMG, ENG, and F-wave studies are more useful for evaluation of the peripheral segments of the sensory and motor pathways. The neurophysiological monitoring of SEPs, MEPs and EMG is of great importance to prevent the neurological

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complications during the procedure.44 Baseline and follow-up electrophysiological parameters play an important role for detecting functional abnormalities of the spinal cord

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and may be a useful way to monitor the progression, therefore they can help the decision making process in patients with mild clinical findings and severe radiological findings.33,35,41,45-47 In order to investigate the contribution of various neurophysiological examinations in the diagnosis in cervical spondylosis, Tsiptsios et al.48 examined 70 patients suffering from cervical spondylosis, with peripheral nerve conduction studies, F-wave from the upper limb and EMG from the corresponding muscles, as well as SEPs from upper and lower limbs and separated the patients into four groups who had cervical spondylosis symptoms only, symptoms and signs of spinal root involvement, symptoms and signs of myelopathy, or symptoms and signs of both myelopathy and spinal root involvement. In all 7

ACCEPTED MANUSCRIPT groups of patients SEPs were the most sensitive electrophysiological study.48 SEPs have been also reported to be more sensitive than nerve conduction studies and EMG.49 Lyu et al.37 reported 49% abnormal SEPs for median nerve and 47% for posterior tibial nerve SEPs in CSM patients who had signal changes in the spinal cord with magnetic resonance imaging (MRI). MEPs have been reported to be more sensitive than SEPs in detecting CSM,45 but

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SEP’s are more useful in detecting clinically silent lesions.38,41,50 De Mattei found sensitivity of MEPs in patients with cervical compression myelopathy to be 70% for upper extremity muscles, and 95% for lower extremity muscles.51 Simó et al.41 studied the role of evoked potentials in the diagnosis of CSM in 51 patients with radiological signs of cord compression and they concluded that MEP is more superior to SEP in detecting early stage myelopathy.

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Tanaka et al.52 examined MEPs in patients with clinically relevant cervical myelopathy who underwent decompressive surgery. Patients who presented a central motor latency longer than

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15 ms and/or polyphasic wave pattern of the potential had worse surgical results than the remaining patients. In a cross-sectional observational study, Kalupahana53 studied the changes of neurophysiological parameters in patients with CSM and radiculopathy, with a view of identifying the role of each neurophysiological investigation in the evaluation of these patients and concluded that 1) the study of MEPs of upper limb muscles appears to be a

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useful test for the prediction of the presence of cervical radiculopathy, while median nerve SEPs do not appear to be useful for it; 2) in addition to the well-established abnormalities of central motor conduction times, the duration of MEPs also appear to be of value as an abnormal parameter in the evaluation of cervical myelopathy; and 3) the study of MEPs of

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upper and lower limb muscles appear to be a useful method for the prediction of the presence of cervical myelopathy while the use of posterior tibial SEPs alone seems to be insufficient

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for it. Moreover, Karlikaya et al.34 reported that although MEPs seem to be superior to SEPs in the early stages of myelopathy, certainly combining two methods is the best.

CERVICAL SAGITTAL BALANCE AND IMBALANCE Recently, the role of sagittal balance in cervical spine disorders and on the possible role of imbalance in predicting clinical and functional outcomes has become a focus of attention.54 The spinal column sagittal balance refers to the shape of the spine that encompasses it to keep the standing position with minimal muscular effort.55 Spinal column shape and consequently 8

ACCEPTED MANUSCRIPT the sagittal balance is the result of the balance between the bony structures (vertebras) and the non-bony elements (intervertebral discs, ligaments and fascia). In order to define the intrinsic cervical sagittal balance, a line should be drawn from the dorsocaudal aspect of the C2 vertebral body to the same C7 point to create the associated gray zone. When the shaded gray zone is located posterior to any of the vertebral bodies, it is assumed that the cervical spine

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has effective lordosis. When the posterior-most aspect of the vertebral body is located within the gray zone, we have a straightened cervical spine. Kyphosis is seen when any portion of the vertebral bodies is posterior to the shaded gray area.56 The surgical outcome of the patients with CSM is also dependent on cervical sagittal balance.57,58 A growing body of evidence suggests that there is a strong correlation between the whole and regional spine

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sagittal balance and the quality of life (QOL) and disability in the aging population.59,60 Cervical sagittal plane deformity is mainly due to the secondary etiologies including trauma,

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degenerative spinal disorders, surgical destabilization, spine arthritis (ankylosing spondylitis, rheumatoid arthritis), and malignancies.61,62 Surgical intervention is indicated in those patients with sagittal plane deformities, resulting in neurological deficit, intractable pain and functional disability. The level of compression and the sagittal imbalance are the most important factors in choosing a surgical approach for a patient with CSM. Therefore, the cervical sagittal imbalance should be assessed before any surgical intervention in order to

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obtain favorable outcomes. Naderi et al.56 classified the cervical sagittal imbalance to effective lordosis, straightened spine and kyphotic spine. Tang et al.63 demonstrated that in patients undergoing multilevel posterior cervical fusion for cervical stenosis, myelopathy, and

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kyphosis, the C2-C7 sagittal vertical axis (SVA) and center of gravity of head are important indicators of QOL as well as neck disability index (NDI) after the operation. They demonstrated that a C2-C7 SVA value of approximately 40-mm is required for obtaining

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favorable surgical outcome in posterior cervical fusion.63 However, Villavicencio et al.64 demonstrated that there were no statistically significant differences in clinical outcome scores between the lordotic and parallel graft patient groups, but patients who had maintained or improved segmental sagittal alignment, regardless of graft type, achieved a higher degree of improvement in QOL and NDI scores.64 We herein represent an evidence-based approach to CSM based on the cervical sagittal imbalance (Figure 1). Since there is no clear, straightforward and strong evidence in the literature on stepwise surgical approach to CSM and with regard to increasing old population in the world, the surgical approach to a serious and rather common pathology of the spine make it necessary to suggest a simple, easily 9

ACCEPTED MANUSCRIPT understandable, and applicable algorithm (Figure 1). Although such algorithms can be designed based on the last evidence from retrospective studies reported by expert authors in the literature, it makes no serious bias in such studies and, therefore, it does not make any ambiguity.

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APPROACH TO PATIENTS WITH NORMAL CERVICAL LORDOSIS Special attention should be paid to the sagittal alignment of the cervical spine, i.e. both overall cervical lordosis as well as segmental lordosis at the affected level. In those with sagittal

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alignment of the spinal column, reduction is not necessary for the treatment of CSM and only decompression is required. Therefore, the surgical option depends on several other factors

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such as the number of levels involved, the location of the abnormal compression, the presence of preoperative neck pain and previous operations.6 Current lines of evidence suggest that the surgical approach in those with CSM with effective cervical lordosis is based on the number of involved levels.65-67 In patients with fewer than three levels of ventral disease, the anterior approach is preferred.66-69 Although the surgical approach to CSM treatment has proven to be controversial, anterior decompression and fusion can remove the compressive pathology and

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reconstruct the alignment of the cervical spine, yielding good clinical results. Both ACDF and arthroplasty are the most common surgical procedures of the cervical spine which are indicated in patients with CSM with fewer than 3 involved levels. ACDF preserves the cervical lordosis and corrects and/or prevents the spinal instability. Recently, Zhu et al.69

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demonstrated that ACDF is associated with better cervical range of motion when compared to dynamic cervical implant (DCI) and cervical total disc replacement in patients with CSM with

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fewer than 3 involved levels. In a systematic review, Shamji et al.70 recommended that in limited anterior CSM with normal cervical lordosis, ACDF could be adequate while in more extensive diseases, anterior procedures seem to be inadequate. Increased range of motion of the cervical spine is an important contraindication of the ACDF. Therefore, some authors have tested DCI for treatment of patients with CSM and effective lordosis. In a recent clinical trial, Li et al.67 demonstrated that DCI had comparable results with ACDF. These results were also verified by Fay et al.71. Consequently, DCI also could be used instead of ACDF in these groups of patients. The disadvantages of the anterior approaches include graft complications, need for postoperative bracing, loss of motion, indirect decompression and adjacent segment 10

ACCEPTED MANUSCRIPT degeneration.65 Gum et al.58 showed that in patients undergoing ACDF, postoperative cervical lordosis of at least 6° predicts achievement of minimum clinically important difference for NDI. This indicates that marinating cervical lordosis is important in achieving favorable results after ACDF.

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Patients with more than three levels of compression are generally treated by laminoplasty, especially if cervical lordosis is preserved.72-74 Cervical laminoplasty is a suitable surgical option in many patients with cervical myelopathy caused by multilevel spinal cord compression,75 and numerous studies have documented satisfactory results with this

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method.76-82 This procedure preserves the spinal motility, minimizes the complication of the laminectomy especially postoperative spinal instability and avoids the development of

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postlaminectomy membrane. In laminoplasty, the dura is not exposed and the posterior bony elements are preserved. Thus, concomitant fixation and fusion can be performed.83 In addition, it can be performed in patients with adjacent segment degeneration who undergo multilevel anterior decompression and fusion. In these patients, laminoplasty is not associated with increased degeneration of the adjacent segments while fusion and fixation are not required.84 The presence of cervical kyphosis is the contraindication for laminoplasty. As

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postoperative axial neck pain is common in patients who undergo laminoplasty, the decision to perform laminoplasty in a patient with significant preoperative neck pain should be taken cautiously.6,72 There are some unique complications related to laminoplasty which include postoperative axial neck pain,85 segmental root palsy with an incidence of approximately

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5%,86 closing of the laminar door, and worsening of the cervical alignment.87

APPROACH TO PATIENTS WITH STRAIGHTENED SPINE The cervical spine should normally demonstrate a lordotic curvature so if the cervical spine is straight, it is abnormal. Physiologic cervical lordosis maintains basic biomechanical balance of the cervical spine, through intricate interrelation between physiologic lordosis, anteroposterior intervertebral disc edge space height, and sagittal spatial alignment.88 From a biomechanical point of view, there are many discussions in the literature as to whether the loss of the physiological lordosis could be a possible cause of pain, due to muscular 11

ACCEPTED MANUSCRIPT imbalance or structural overload of the anterior parts of the spine.89,90 The loss or reversal of the normal lordosis has been speculated to cause numerous consequences in health, including decreased vital lung capacity, cervical, interscapular, headache pain and temporomandibular disorders.91,92 Cervical lordosis may play a positive role in cervical spondylosis treatment. The vertebral deformation caused by stress concentration will straighten the cervical curve

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more. With elderly patients, vertebral deformation is the most common reason for sagittal profile change of the cervical spine because of vertebral degeneration.93 In contrast, vertebral degeneration is not so common in young people. Wei et al.88 proposed a finite element analysis of the complete cervical spine with straightened and normal physiological curvature

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by using a specially designed modelling system and their result demonstrated that the active movement range of straightened cervical spine decreases 24–33 %, but stress increases 5–95 %. Also they reported that there was stress concentration at the facet joint cartilage,

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uncovertebral joint and the disk, which implied there might arise abnormal tensions on the hind-brain, cranial nerves, cervical cord, and cervical nerve roots. Wei et al.88 proposed the cervical muscle imbalance could be the main reason for cervical curve straightening.

Loss of normal cervical lordosis which leads to straightened spine along with ossification

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of the posterior longitudinal ligament leads to stenosis of the spinal canal causing cord compression which may contribute to the development of myelopathy,94,95 and in these patients, the spinal cord could be compressed by tethering over the apical vertebra or intervertebral disc or by ossification of the posterior longitudinal ligament.96 One of the

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important pathophysiological mechanisms of CSM in patients with straightened cervical spine is longitudinal distraction causing progressive spinal cord dysfunction.97 It has been

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previously shown in animal studies that artificial distraction of C1 and C7 would result in the disappearance of spinal cord evoked potentials especially at the midcord segment, suggesting that distraction stress in humans is mostly concentrated at the C4 and C5 levels, i.e. where kyphosis and/or local angulatory deformity is frequent.98 Therefore, even when the entire spinal cord is longitudinally distracted, injury of the anterior horn and the pyramidal tracts induced by such mechanical distraction stress will be significant.

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ACCEPTED MANUSCRIPT The number of involved levels is the most important factor in choosing the surgical approach. Multiple case series have reported that a 1 to 3 level ACDF is safe and effective in decompressing ventral pathology.67,99-101 Those with a straightened cervical spine should not generally be considered for extensive posterior decompression. With appropriate placement of the interbody spacer, ACDF adds at least 5 degrees of lordosis per level and thus results in a

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more physiologic lordotic curvature of the cervical spine and potentially restores overall sagittal balance.102 However, applying this procedure to greater than 3 levels can often result in

complications,

including

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extrusion,

subsidence,

fracture,

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pseudoarthrosis.99,100,103,104 ACDF is effective for ventral pathology that is confined to the

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cervical interspaces (i.e., osteophyte/disc complexes). Resection of the osteophyte/disc complex and placement of an interspace graft not only removes the offending ventral pathology, but also can be used to restore lordosis to a straight or kyphotic spine. As ACDF

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cannot be performed in more than 3 level pathologies, other surgical approaches should be undertaken. In those with multilevel CSM who has straightened cervical spine, stability should be evaluated by means of dynamic cervical radiographies. In those with cervical instability, posterior decompression and fusion is the method of choice.105,106 Posterior cervical decompression and fusion is an accepted treatment of CSM and is the procedure of

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choice for the patients with multilevel CSM (Figure 2). Posterior surgical approaches typically involve laminectomy with or without fusion or laminoplasty. These procedures allow for direct decompression of the cervical spine when the causative pathology is located at the posterior aspect of the spinal canal (i.e., hypertrophied ligamentum flavum). Posterior

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approaches also allow indirect decompression of the spinal cord from anterior pathology by enlarging the spinal canal and allowing the cord to migrate away from the offending

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pathology. Posterior approaches offer several advantages compared with anterior cervical approaches for CSM. For example, such procedures may not require fusion of vertebral levels which leads to avoid the cost and potential complications of instrumented fusion and limit adjacent level spondylotic degeneration. In contrast to anterior approaches to the cervical spine, posterior approaches avoid exposure and injury to critical neck structures including the esophagus, recurrent laryngeal nerve, and carotid artery. Furthermore, direct visualization and decompression of nerve roots is possible using posterior approaches. Finally, posterior decompression procedures are particularly appealing in patients with congenitally narrow canals. The primary disadvantages of posterior approaches include the possibility of developing postlaminectomy kyphosis or instability. Furthermore, these approaches do not 13

ACCEPTED MANUSCRIPT typically allow for primary resection of ventral canal pathology such as disc/osteophyte complexes, particularly in association with preexisting kyphotic deformity.18

When dynamic radiographies do not demonstrate the instability of the cervical spine, age is the determining factor for surgical approach. In elder patients with spondylotic spines,

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laminectomy is an appropriate choice. Cervical laminectomy, which permits adequate decompression of the spinal cord, has long been the treatment for multilevel cervical spondylosis. But in younger individuals, laminoplasty is the method of choice. Laminectomy has traditionally been the gold standard for posterior approaches for CSM. This technique has

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been well described in the literature and is considered as a safe surgical procedure. However, the biggest complication after laminectomy is postlaminectomy instability/kyphosis. Multiple

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lamina are resected in patients who undertake aggressive facet resection and these patients are at an increased risk of developing postlaminectomy kyphosis when there is preexisting instability.107 Studies suggest that the risk of postlaminectomy kyphosis in adult patients is between 6% and 52%.108 Resection of the C2 and/or C7 lamina or spinous processes may increase this risk.109,110 This risk could be minimized by instrumented stabilization at the time of initial laminectomy which serves to both stabilize the cervical spine as well as secure the

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spine in an optimal lordotic configuration. There are multiple instrumentation techniques that have been well described in the literature.5,18,105 The goal of instrumentation is to provide temporary structural stabilization to allow solid bone formation. Traditional techniques such as interfacet wiring have been replaced by modern lateral mass and pedicle screw fixation

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systems. These modern fixation systems depend on screws to anchor rods or plates along the lateral masses. The most common technique for placement of lateral mass screw is Magerl

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technique which avoids neurovascular injury.111 In a series of patients with posterior lateral mass instrumentation, Heller et al.112 found that the risk of nerve root injury was less than 1% per screw placed and no patient experienced injury to the vertebral artery or spinal cord.

APPROACH TO PATIENTS WITH CERVICAL KYPHOSIS Cervical kyphosis is a potentially debilitating form of sagittal deformity that poses unique challenges to the treating spinal surgeon.113,114 Cervical kyphotic deformity may lead to CSM due to stenosis of the cervical canal and compression of the cord toward the posterior 14

ACCEPTED MANUSCRIPT longitudinal ligament. The development of kyphotic deformity following decompressive cervical laminectomy is a well-documented iatrogenic cause of sagittal cervical imbalance.115117

Surgery to treat cervical kyphosis is usually a spinal fusion combined with segmental

instrumentation. Surgical correction is the most difficult type of treatment for cervical kyphosis. There are three approaches for cervical kyphosis: the anterior, posterior or

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combined procedures. Surgery to the front of the spine (anterior cervical fusion) is done to relieve the pressure on the spinal cord. The second procedure is done through the back (posterior cervical fusion) to fuse the spine and prevent the kyphosis from returning. Some surgeons prefer the anterior-alone approach because they are familiar with the procedure and it permits both ventral decompression, as the spinal cord compression in cervical kyphosis is

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usually ventral, and the correction of deformity.93,118-122 It is associated with lower rates of morbidity and mortality than the combined approach. Other surgeons prefer the combined

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anterior and posterior approach rather than the anterior procedure alone, as the latter may fail to achieve large correction and is prone to reconstructive failure and loss of correction due to mechanical disadvantages, especially in patients with postlaminectomy kyphosis.123-125 Regarding the importance of neurophysiological monitoring, as it has been discussed before, patients should be neuromonitored throughout the entire operative procedure with transcranial

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motor-evoked potentials, somatosensory-evoked potentials and EMG.

Cervical kyphosis can be categorized as 1 of 2 types of sagittal deformities: flexible versus fixed.125,126 If the kyphosis is flexible, the decision to go ahead with surgery should be based

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upon: the progression of the deformity, the severity of the deformity, and the amount of pain it causes. Flexible cervical kyphosis is posturally reducible with or without gentle traction127

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and therefore commonly treated by reduction and posterior stabilization with fusion to guarantee the stability of the cervical spine.113,114 In this setting, interbody arthrodesis can be used for anterior column load sharing, however, it is not required for deformity correction.126 Alternatively, some authors have reported the use of anterior-only surgery for flexible cervical kyphosis, the reduction being accomplished by anterior column distraction across implants and interbody fusion.93,118,120 In addition, in a case study, Dugoni et al.44 reported that the anterior approach is a good surgical option in flexible cervical kyphosis. However, the posterior approach has been found to be associated with better functional outcome.105 If the fixed deformity is accompanied by neurological problems from pressure on the spinal cord, 15

ACCEPTED MANUSCRIPT surgery becomes more likely. In the treatment of fixed cervical kyphosis, different strategies of correction and stabilization can be entertained with advantages and disadvantages for each. The surgical sequence depends on many factors, including the sites of bony ankylosis, extent of kyphosis, and presence and location of spinal cord compression. If the kyphosis is due to ankylosing spondylitis (AS), the connection between the cervical and thoracic spine is the

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problem area. This type of cervical kyphosis is usually a fixed deformity. In AS the discs between each vertebra of the entire spine calcify and fuse the bones of the spine together. In this situation, osteotomies are required to release the areas of ankylosis, thereby transforming a fixed kyphosis into one that is flexible.114,128 Unlike flexible deformity, preoperative

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cervical halo-traction is of no significant value in cases of fixed deformity. As discussed above, the distinction between flexible and fixed cervical deformities is important in terms of treatment strategy, and in particular, the need for osteotomies to attain correction. This

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procedure involves cutting the front of the spinal column so the surgeon can straighten the spine. The spinal cord is not cut-only the bones of the vertebrae in the front of the spinal column. Importantly, all patients in this series had fixed cervical kyphosis and therefore underwent circumferential osteotomies and stabilization for correction of deformity. Abumi et al.128 treated patients having a fixed kyphosis with a combined anterior and posterior

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procedure; these patients all underwent osteotomies and circumferential spinal fusion. The correction of the kyphosis was achieved in all patients through posterior pedicle screw fixation. In this fixed deformity cohort, mean preoperative kyphosis of +31° was improved to +1° of kyphosis at final follow-up, yielding a final average correction of 30° which provided a

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stronger stabilizing effect and greater pullout strength. In a single institutional experience, O’Shaughnessy et al.125 investigated clinical and radiographic outcomes following the

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surgical treatment of fixed cervical kyphosis with myelopathy and they reported that not only fixed cervical kyphosis with myelopathy can be successfully treated surgically with circumferential osteotomies and instrumented fusion, but also a high percentage of patients achieved an excellent or good clinical outcome and measurable improvement in their symptoms of myelopathy.

The surgical strategy for CSM accompanying local kyphosis remains controversial. Uchida et al.129 reported that the outcomes of anterior decompression/fusion for CSM with local kyphosis with an angle of 10° or more were equivalent to those of laminoplasty alone for the 16

ACCEPTED MANUSCRIPT same pathology at follow-up in their series of 43 patients, and the recovery rates of the Japanese Orthopedic Association score were acceptable in both groups. In their series, the local kyphosis angle of the anterior decompression/fusion group at follow-up was still a mean of 9.2°, so the correction of the local kyphosis would appear to be somewhat mild. Chiba et al.130 reported that several patients obtained an acceptable clinical outcome after laminoplasty

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alone, even in the context of cervical kyphosis, and they speculated that the slack of the spinal cord, especially in patients showing reduction of multilevel disc height, should allow acceptable recovery. On the other hand, several authors have insisted that the outcome of laminoplasty alone for CSM with local kyphosis was not acceptable.131 Baba et al.132 reported that patients with preoperative kyphosis (mean of 11.7°) showed significantly poorer

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neurological improvement. Moreover, Suda et al.131 reported that the outcomes of laminoplasty for CSM accompanying local kyphosis with an angle exceeding 13° (when

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coexisted with myelomalacia) and 5° (without myelomalacia) were poorer than those for CSM without local kyphosis in their multivariate logistic regression analysis.

Based on the experience and evidence provided in the literature, we herein suggest a stepwise surgical approach to CSM with kyphosis deformity. Patients with mild cervical

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kyphosis (kyphotic angle ≤ 10°) should be managed like straightened spine. In patients with mild kyphosis deformity with less than 3 involved levels, ACDF and fusion with plate is recommended. However, the management of CSM with severe cervical kyphosis still remains a dilemma to neurosurgeons. In patients with severe cervical kyphosis, traction is often used

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prior to surgical intervention. If the reduction of kyphosis is significant after 5–7 days of traction, a dorsal strategy that includes fixation and fusion is often used to maintain the

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correction (Figure 3). If there is no reduction of kyphosis after 5–7 days of traction, it is unlikely to achieve success with traction. Traction may also be associated with medical complications, transient neurological deterioration or patient refusal.120 Occasionally, traction is continued into the operating room and used to correct the deformity during the operation. In the anterior procedure, once decompression is completed, the amount of traction is increased to correct the deformity.133 Rhee and Basra134 showed that patients with multilevel disease with neutral cervical alignment or in those with reducible cervical kyphosis, lateral mass fusion is an option as the cervical alignment can be restored prior to securing the instrumentation. In irreducible cervical kyphosis, anterior corpectomy and instrumentation 17

ACCEPTED MANUSCRIPT should be performed to obtain appropriate functional recovery.133,135,136 In patients with less than 2 involved levels, no more imaging and investigations are required. In these patients, ACDF can correct sagittal imbalance about 5° per level so this procedure is associated with favorable outcome and good functional recovery.137 In those with more than 2 involved levels, anterior cervical corpectomy and fusion (ACCF) should be performed using cervical MRI for

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evaluation of the patency of subarachnoid space (SAS) and the cerebrospinal fluid (CSF) flow around the cord. If the magnetic resonance myelogram demonstrates the patent SAS, only posterior cervical fusion can be performed.138 However, in those with closed SAS, posterior decompression and posterior fusion are required to maintain the favorable functional

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recovery.139,140 Posterior cervical fusion may be performed in conjunction with or without a posterior decompression (laminectomy) and/or instrumentation (use of metal screws/rods). Nowadays, metal screws and rods are almost always used, which adds immediate stability and

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increases the fusion rate (percentage of patients where the bone successfully mends together). When Anderson et al. reviewed the treatment of cervical myelopathy, they concluded that posterior cervical decompression with fusion was an acceptable treatment modality.5,141-144 There is a commonly held belief that posterior cervical fusions have a high fusion rate, ranging from 90% to 100%, depending on the fusion criteria utilized.145-154 Higher fusion rates

osteodysplasia.

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COMPLICATIONS

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with posterior cervical fusion may be more appropriate in patients with osteopenia or

As with any surgery, there are risks associated with cervical spine surgery. Possible

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complications can be related to the approach used, the bone graft, healing, or long-term changes. In general, elderly patients, patients who are overweight, smokers, and patients with diabetes or multiple medical problems have higher rates of complications from surgery. However, in a multi-institutional retrospective cohort study conducted by Buerba et al.155, the authors evaluated the effect of obesity on complication rates after posterior cervical fusion in the 30-day postoperative period and their results suggested that high obesity class may not be associated with increased complications after posterior cervical fusion, despite previous study results. Wang et al.156 reported that the risk of complication is highest in patients undergoing a posterior approach or combined anterior posterior procedure and patients with a primary 18

ACCEPTED MANUSCRIPT diagnosis of CSM. Complications related to the correction procedure include implant displacement, graft dislodgment, pseudarthrosis, dysphagia, hoarseness of voice, wound infection, dural tear resulting in CSF leakage, pneumonia, neurological deficits (e.g., quadriparesis, radiculopathy and C5 root palsy) and injury to the vertebral artery. The potential risks and complications of posterior cervical spinal fusion are wound infection,

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degeneration of disk levels above or below surgery level, injury to the vertebral artery, stretch on the nerves from the spinal cord drifting backwards, indirect decompression, late instability or deformity (laminoplasty), inconsistent relief of neck pain (laminoplasty), neurological injuries such as lesions to spinal cord, nerve roots, and dura matter, specific neurological

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injuries such as damages to the greater occipital nerve of Arnold and postoperative C5 palsy, CSF leaks, vascular injuries, and bad positioning which causes increased splenic venous pressure, greater intraoperative bleeding, poor oxygenation of the patient, unfavorable

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position of the head and neck with respect to the trunk, displacement of endotracheal tubes, and ophthalmologic complications. In addition, posterior approach cannot be used for kyphotic spines. Abumi et al.128 utilized posteriorly placed cervical pedicle screw fixation to manage patients with flexible mild degenerative kyphosis. Although they achieved favorable results and no screw-related complications, the risks that were associated with placing the

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cervical pedicle screws limited the use of this strategy. Because anterior approach is performed near to vital anatomic elements, especially when it is necessary to do multilevel corpectomy, intraoperative blood loss, surgical duration, and spinal cord injuries increase. Therefore, overall, posterior cervical fusion is associated with less complication rate

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compared with anterior cervical fusion surgeries.

SUMMARY

The stepwise surgical approach for management of CSM is summarized in Figure 1. The patients with CSM should be managed according to cervical sagittal balance. Accordingly, patients will be divided into cervical lordosis, straightened spine and kyphotic deformity. In those with cervical lordosis, the number of involved levels is the key point in patient selection for surgical intervention. Those with less than 3 involved levels benefit from ACDF or arthroplasty while those with 3 or more involved levels require laminoplasty. In those with straightened spine, number of levels is a determinant factor in choosing the appropriate 19

ACCEPTED MANUSCRIPT surgical approach. The patients with 3 or less involved levels, ACDF with anterior cervical plate is adequate. However, in those with more than 3 involved levels and spine instability, posterior decompression and fusion is required (Figure 2). In those without cervical spine instability, age is a determining factor. In old patients (>65 years) and ankylosed spine, laminectomy is necessary while in youths without ankylosis, laminoplasty is adequate. The

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surgical management of CSM in patients with mild local kyphosis (kyphotic angle ≤ 10°) is the same as patients with straightened spine. However, severe kyphosis requires more complex surgical procedures. Cervical traction in this group of patients would differentiate reducible from irreducible cervical kyphotic deformities. Reducible severe kyphosis is

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successfully treated by posterior decompression and fusion (Figure 3). Irreducible cervical kyphosis with less than 2 involved levels is treated by ACDF, but those with more than 2 involved levels require ACCF and the evaluation of cervical MRI regarding the patency of the

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canal and the characteristics of SAS. In patients with patent SAS, only posterior fusion is adequate while in those with closed SAS, posterior decompression and posterior fusion would be required. As there is no simple and holistic approach, designing such an algorithm can be useful and can form the basis for future studies. This stepwise surgical approach enables the

CONCLUSION

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spine surgeons to choose the appropriate surgical intervention for the appropriate patient.

Surgical management of CSM has evolved significantly during the recent decade. However,

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there is no precise surgical approach or guideline available for CSM. There are many surgical options for CSM, and each patient should have a surgical plan tailored to address each

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individual’s unique clinical circumstance. This paper provides a stepwise evidence-based surgical approach for the management and treatment of patients with CSM. This can help the spine surgeons manage the patients with CSM according to the available evidences in a stepwise approach.

20

ACCEPTED MANUSCRIPT

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FIGURE LEGENDS: Figure 1. Algorithm for surgical treatment of cervical spondylotic myelopathy. Figure 2. (A, B) The preoperative MRI of a 78-year-old man with recent quadriparesis showed severe spinal cord compression. (C, D) Dynamic X-ray showed instability

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(anterolisthesis) at C3-C4 level. (E) CTs did not show ossified posterior longitudinal ligament with mild kyphosis. (F, G, H) Posterior decompression was done by laminectomy of C3 to C7 levels with lateral mass screw fusion from C3 to C6. Spinal cord was

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significantly decompressed and solid fusion was achieved.

Figure 3. (A, B) The initial preoperative MRI of a 73 year-old-man with paraparesis since 9 months showed kyphotic angle at C4–C5 level about 30° degree. (C) Relative alignment after

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7 kg cervical traction was achieved. (D) Posterior decompression and solid lateral mass screw fusion was performed. Spinal cord has been significantly decompressed with good sagittal

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balance. During one year follow-up, the patient was recovered significantly.

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Abbreviations:

CSM: Cervical spondylotic myelopathy ACDF: Anterior cervical discectomy and fusion

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QOL: Quality of life EMG: Electromyography ENG: Electroneurography

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SEPs: Sensory evoked potentials AS: Ankylosing spondylitis

NDI: Neck disability index DCI: Dynamic cervical implant

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SVA: Sagittal vertical axis

ACCF: Anterior cervical corpectomy and fusion

SAS: Subarachnoid space

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CSF: Cerebrospinal fluid

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MRI: Magnetic resonance imaging

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Conflict of Interest

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'Conflicts of interest: none'