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ORIGINAL ARTICLE
Year : 2020  |  Volume : 17  |  Issue : 2  |  Page : 36-42

Strategies in the management of atlantoaxial tuberculosis: Midterm radiological and functional outcomes of seven patients


Division of Orthopaedic Spine Surgery, Institute of Orthopaedics and Traumatology, Madras Medical College, Chennai, Tamil Nadu, India

Date of Submission06-Nov-2020
Date of Acceptance13-Dec-2021
Date of Web Publication08-Mar-2021

Correspondence Address:
Aju Bosco
Division of Orthopaedic Spine Surgery, Institute of Orthopaedics and Traumatology, Madras Medical College, EVR Road, Park Town, Chennai - 600 003, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/joasis.joasis_12_20

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  Abstract 


Keywords: 


How to cite this article:
Uvaraj NR, Bosco A, Vadivelu B. Strategies in the management of atlantoaxial tuberculosis: Midterm radiological and functional outcomes of seven patients. J Orthop Assoc South Indian States 2020;17:36-42

How to cite this URL:
Uvaraj NR, Bosco A, Vadivelu B. Strategies in the management of atlantoaxial tuberculosis: Midterm radiological and functional outcomes of seven patients. J Orthop Assoc South Indian States [serial online] 2020 [cited 2021 Sep 25];17:36-42. Available from: https://www.joasis.org/text.asp?2020/17/2/36/310980




  Introduction Top


Tuberculous involvement of the atlantoaxial (C1-C2) region is rare, accounting for only 0.3%–4.8% of spinal tuberculosis.[1],[2],[3] Early symptoms being nonspecific, delayed identification of this disease is common, which might lead to extensive osseous and soft-tissue destruction, resulting in atlantoaxial instability with or without spinal cord compression at its initial presentation.

Over the years, diverse treatment strategies have been described in the literature, each with its own advantages and disadvantages.[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14] Conservative treatment offers good outcomes in early atlantoaxial tuberculosis with a stable atlantoaxial joint and no neural compression. The treatment of advanced atlantoaxial tuberculosis with the destruction of the C1-C2 articulation with resultant instability and neural compression is conflicting and controversial.[15] Surgical treatment of tuberculosis of the atlantoaxial region is challenging due to the complex anatomy of the region, its critical neurovascular neighborhood, difficulty in accessing the joint, and paucity of cephalad anchor points.

Existing literature is divided between conservative and surgical management. Because of the rarity of this disease, literature is limited by a lack of high-quality studies, leading to a hardly established evidence-based algorithm available to support rationale treatment. We describe a protocol for the management of tuberculosis of the atlantoaxial region and report the midterm clinical, functional, and radiological outcomes of patients treated using our protocol.


  Materials and Methods Top


We did a retrospective review of prospectively collected data of seven consecutive patients with atlantoaxial tuberculosis who were treated at our institution between November 2012 and January 2018. Approval from the Institutional Review Board was obtained.

Data regarding the demographic profile of the patients, including preexisting comorbidities, duration and history of the presenting symptoms, and ambulatory status/disability, were collected. A detailed clinical examination, including the assessment of neurological status was done. Disability due to neck pain was graded using the Neck Disability Index (NDI).[16] In patients presenting with myelopathy, their disability was graded using the Nurick system of grading.[17] Neurological deficits were graded using the American Spinal Injury Association (ASIA) scale.[18]

Laboratory investigations comprising a complete blood count, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), liver function test (LFT), microscopic examination of sputum for acid-fast bacilli (AFB), ELISA for human immunodeficiency virus (HIV), and Mantoux skin test for tubercular protein were done for all patients.

Radiological evaluations, including a plain anteroposterior chest radiograph (to rule out active pulmonary tuberculosis), plain anteroposterior and lateral radiographs of the cervical spine, anteroposterior open mouth and lateral radiographs of the craniovertebral junction (CVJ), magnetic resonance imaging (MRI), and dynamic computerized tomography (CT) scans, were performed for all patients on admission. Radiological grading of the disease severity was done using Lifeso classification.[19]

The diagnosis was established based on the presence of typical clinical and radiological findings and corroborative histopathological and/or bacteriological evidence (polymerase chain reaction [PCR] and culture [BACTEC]) for tuberculosis.

Treatment strategy

Immediate immobilization of the cervical spine in a hard collar was done on admission. A detailed assessment of the extent of osseous and ligamentous destruction of the atlantoaxial region, the presence of instability, neural compression, and the anatomy of the vertebral artery was done before deciding the management strategy. Patients were treated according to the following protocol:

  1. Patients with tuberculosis of the odontoid process alone without radiological evidence of atlantoaxial instability (Lifeso Stage I) and normal neurology are subjected to a transoral core needle biopsy of the odontoid lesion to establish a histopathological and bacteriological diagnosis [Figure 1]. These patients are managed conservatively with immobilization in a halo-vest orthosis
  2. Patients with C1-C2 instability (due to ligamentous disruption) with the preserved architecture of the C1 and C2 vertebrae (Lifeso Stage II) with or without neurological deficit are treated with posterior stabilization and fusion using C1 lateral mass screws and C2 pedicle screws [Figure 2]. Biopsy was obtained from C2 vertebra through transpedicular route for patients who underwent posterior stabilization procedures
  3. Patients with extensive osseous destruction of the atlantoaxial joint complex with resultant instability (Lifeso Stage III), with or without neurological deficit, are treated with posterior stabilization and fusion using an occipitocervical construct with anchorage in C1 and C2 segments where feasible
  4. In patients with predominant involvement of the anterior part of C1-C2 complex with a retropharygeal abscess resulting in dysphagia and dyspnea, surgical drainage of the abscess, is performed through a retropharyngeal approach. If there no clinicoradiological evidence of instability of the C1-C2 articulation or neural compression, no spinal stabilization is warranted
  5. In patients with predominant involvement of the anterior part of the C1-C2 complex with concomitant C1-C2 instability, biopsy, debridement, and anterior instrumented fusion of the C1-C2 joint is done through a sub-mandibular approach [Figure 3].
Figure 1: Showing transoral needle biopsy done using a long needle to procure tissue from the diseased odontoid process for diagnosis

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Figure 2: Plain anteroposterior radiograph of cervical spine (a) in a 55-year old female showing signs of basilar invagination. Plain lateral radiograph (b) of the upper cervical spine showing an anterior subluxation of C1 over C2. Sagittal (c) and coronal (d) computerized tomography scans showing destruction of the C1-C2 joint with evidence of instability. (e) Sagittal T2-weighted magnetic resonance imaging showing the prevertebral abscess anterior to C2, and basilar invagination with compression at the cervicomedullary junction, Postoperative anteroposterior (f) and lateral (g) plain radiographs of the cervical spine at 34 months postsurgery, showing posterior stabilization from C1 to C2. (h) Coronal computerized tomography scan taken at 12 months postsurgery showing complete fusion (yellow arrows) at the C1-C2 joints bilaterally

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Figure 3: (a) Sagittal T2 weighted magnetic resonance imaging showing features of tuberculous spondylitis of C2 with extensive disease of the dens with prevertebral abscess and anterior epidural abscess causing cord compression. Postoperative lateral (b) and anteroposterior (c) radiographs of the cervical spine taken 26 months after surgery showing a stable anterior internal fixation and fusion of the C1-C2 articulation through a submandibular approach

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While doing a posterior stabilization, the cephalad anchorage can be extended to the occiput if the anchorage in C1 was inadequate or not feasible due to extensive destruction. The caudal instrumentation can be extended to one level below if the anchorage in the C2 pedicle was inadequate.

Post-operatively, patients were immobilized in a hard cervical collar for 3 months. All patients received standard anti-tubercular chemotherapy [Intenisve phase(2 months): isoniazid, rifampicin, pyrazinamde, ethambutol and Continuation phase(10 months): isoniazid, rifampicin, ethambutol] with dosages according to body weight. Drugs were administered on a daily basis at home.

Patients were followed up fortnightly for the first 2 months and at 6-week intervals thereafter with ESR, CRP, hemoglobin, LFT, and plain radiographs of the upper cervical spine till completion of treatment. Any derangement in liver function was managed with dose adjustments after consultation with a hepatologist. Response to chemotherapy was determined by clinical signs of well-being, improvement in neurological status, improvement in laboratory parameters (ESR, CRP, hemoglobin), and radiological evidence of healing. The status of bone healing, the integrity of the internal fixation, and progress of fusion at the site of lesion were evaluated on plain radiographs at each follow-up visit. A CT scan of the CVJ was taken at 12 months to assess bone healing and fusion.

After completion of chemotherapy, patients were followed up every 6 months till date for any signs of disease recurrence. Functional outcomes were analyzed using visual analog scale (VAS) and NDI scores at each follow-up visit.


  Results Top


The demographic profile, staging of the disease, details of treatment, and outcomes of patients are given in [Table 1]. The study included seven patients (four females, three males) with atlantoaxial tuberculosis. The mean age at presentation was 41 ± 19.8 (range, 21–70) years. No patient was positive for HIV.
Table 1: Demographic profile, details of treatment and outcomes of patients with atlantoaxial tuberculosis treated using our protocol

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Presenting symptoms and neurology

The mean duration of symptoms at presentation was 3.7 ± 1.1 (range, 2–5) months. The presenting symptoms were neck pain (100%, n = 7), difficulty in neck movement (85.7%, n = 6), neurological deficit (71.4%, n = 5), ataxic gait (42.9%, n = 2), and torticollis (14.3%, n = 1). The mean VAS score and NDI score at presentation were 8.4 ± 0.5 (range, 8–9) and 78.3 ± 8.4% (range, 70% to 96%), respectively. Preoperative ASIA grading of neurological function was ASIA B (n = 1), ASIA C (n = 2), ASIA D (n = 1), and ASIA E (n = 3), [Table 1].

Radiological features

Three patients had evidence of tuberculosis on chest radiographs. The C1-C2 articulation was involved in five patients, while two patients had predominant involvement of the odontoid process (atlantodental articulation). Atlantoaxial instability was evident on plain radiographs and/or CT scans in four patients. MRI showed paravertebral abscess and retropharyngeal abscess formation in all seven patients. Based on Lifeso's radiographic criteria, three patients had stage-I involvement and four patients had stage-III involvement of the atlantoaxial joint.

Laboratory parameters

The ESR and CRP values were elevated in all patients at presentation [Table 1]. Sputum microscopy for AFB was positive in three patients. Tuberculous culture (BACTEC) did not yield growth in any of the samples, and hence, drug sensitivity testing could not be done. However, Gene Xpert (DNA PCR) was positive in four samples, all of which were sensitive to rifampicin. Transoral biopsy yielded a positive histopathological and bacteriological diagnosis in both patients.

Operative parameters

The average operation time for fusion procedures and transoral biopsy/abscess drainage was 190 ± 32.4 (range, 180–240) min and 35 ± 7.1 (range, 30–45) min, respectively. The average intraoperative blood loss for fusion procedures and transoral biopsy/abscess drainage was 562.5 ± 82.0 (range, 500–700) mL and 46.7 ± 7.0 (range, 30–70) mL, respectively.

There were no intra-operative complications.

Follow-up– Analysis of outcomes

The mean follow-up period was 45.3 ± 18.6 (range, 16–65) months. All patients showed a significant improvement in VAS scores for neck pain and NDI scores at final follow-up. The mean VAS and NDI scores at presentation were 8.4 ± 0.5 (range, 8–9) and 78.3 ± 8.4% (range, 70% to 96%), respectively, which reduced to 2.1 ± 0.6 and (1–3) and 10.9 ± 2.8 (range, 6–14) percent, respectively, at a mean of 3 months after initiation of treatment which was maintained till the last follow-up. All patients showed neurological improvement to ASIA E, at final follow-up. None of the patients had neurological deterioration. Following treatment, radiological evidence of healing was seen in all patients at a mean of 8.3 ± 1.0 months (7–10 months). CT evaluation at 1-year post-treatment showed evidence of solid atlantoaxial arthrodesis in four patients and evidence of complete healing of odontoid lesions without any evidence of instability. There was a significant reduction in the mean ESR and CRP values from 57.4 ± 9.7 (range, 46–72) mm/h and 17.4 ± 3.6 (range, 14–25) ng/L, respectively, at presentation to 8 ± 2.6 (range, 4–12) mm/h and 3.4 ± 1.0 (range, 2–5) ng/L, respectively, at final follow-up. One patient (patient No. 2) who had undergone posterior stabilization had unilateral breakage of the C2 pedicle screw. He eventually had good bone healing and fusion without affecting the clinical outcome.

There was no clinical or radiological evidence of disease recurrence till the final follow-up.


  Discussion Top


The pathophysiology and clinical presentation of tuberculosis of the atlantoaxial region are unique due to the complex anatomy of the atlantoaxial segment and its critical neurovascular neighborhood. Early disease with minimal clinical symptoms and an unremarkable neurology (due to the spacious spinal canal in this region) easily goes unnoticed. Patients often present with advanced disease with significant osseoligamentous destruction of the C1-C2 complex with clinical and/or radiological signs of instability, neural compression, and deformity. Conservative treatment offers good outcomes in early atlantoaxial tuberculosis with no clinicoradiological signs of atlantoaxial instability or neural compression. The treatment of advanced atlantoaxial tuberculosis with the destruction of the articulation with resultant instability and neural compression is conflicting and controversial.[15] Surgical treatment of tuberculosis of the atlantoaxial region is challenging due to the complex anatomy of the region, its critical neurovascular neighborhood, difficulty in accessing the joint, and paucity of cephalad anchor points.

Because of the rarity of this disease, literature is limited by a lack of high-quality studies, leading to a hardly established evidence-based algorithm available to support rationale treatment. The available studies in the management of atlantoaxial tuberculosis are mostly retrospective, with few prospective studies.

Over the years, the pendulum of treatment of atlantoaxial tuberculosis has swung between conservative and surgical treatment. There are no set guidelines described for the management of atlantoaxial tuberculosis. A detailed review of the available literature and our own experience has helped us in formulating a treatment strategy for the management of this rare entity.

In the absence of neurological deficit and gross instability, the treatment for the upper cervical spine tuberculosis was plaster immobilization, halo-device fixation, and other conservative approaches. With a better understanding of atlantoaxial regional anatomy, advances in radiological evaluation, and the development of internal fixation devices and spinal surgery techniques, the number of patients with upper cervical spinal tuberculosis receiving surgical treatment has gradually increased.

Tuberculous lesions of the atlantoaxial joint located in the anterior part of the vertebral column were dealt with by anterior surgeries. The anterior surgery has the advantages of better debridement of anteriorly located lesions and direct decompression of the spinal cord. However, reconstruction and fusion for stability after focal debridement are difficult to achieve anteriorly because of the following reasons: (1) the anatomical characteristics of the atlantoaxial joint, (2) damage to the anterior column of the atlantoaxial joint, and (3) lack of a reliable internal fixation method to get a stable anterior reconstruction and stabilization.

Goyal et al. suggested that transarticular screw fixation can be used successfully if the lateral masses are intact and destruction is not severe, thus sparing the movements at the atlantooccipital joint.[20] Chaudhary et al., in their study, observed that CVJ tuberculosis can severely damage the odontoid process, resulting in atlantoaxial dislocation. In these patients, surgery restores and maintains the craniocervical alignment and has a predictable outcome compared with conservative therapy. Pathological odontoid fractures have the potential to go into nonunion. The odontoid process once destroyed completely, is rarely restored after antitubercular therapy.[21]

Qureshi et al. observed that in patients with tuberculosis of CVJ with instability and neurological compromise, who fail to respond to 4–6 weeks of antitubercular chemotherapy with concomitant skull traction should be offered occipitocervical fusion (OCF) with or without posterior decompression. Anterior surgery will be needed only in those few cases who do not improve neurologically after OCF.[1]

Zhang et al. achieved good clinical outcomes with debridement and short segment posteriorly instrumented fusion through a single-stage all-posterior approach. This significantly reduced blood loss and anesthesia time with fewer complications.[22] According to Mandavia et al., a posterior cervical approach may be a safe and effective strategy for patients with cervical TB.[23]

Xing et al. showed good outcomes using an anterior approach for anterior cervical and retropharyngeal debridement combined with posterior occipitocervical fusion for upper cervical tuberculosis.[12] Wang et al. reported favorable outcomes in patients with atlantoaxial tuberculosis who underwent single-stage combined anterior and posterior surgical approach. This method of management facilitates complete debridement, decompression, and a reconstruction of the upper cervical spine.[10]

In this study, a detailed assessment of the extent of osseous and ligamentous destruction of the atlantoaxial region, the presence of instability, neural compression, and the anatomy of the vertebral artery was performed before formulating the management strategy.

Accordingly, posterior stabilization was performed in three patients who had gross atlantoaxial instability with resultant neurological deficit. Short segment fusion with C1 lateral mass and C2 pedicle screws were used in two patients. In one patient, due to extensive destruction of the C2 vertebra resulting in the poor anchorage in the pedicle, the posterior stabilization was extended to the C3 vertebra.

A detailed radiological evaluation is a must in all cases of atlantoaxial tuberculosis mainly to assess the integrity of lateral masses of atlas and pedicles of the axis, the structures which facilitate posterior instrumentation. In the event of destruction of either the lateral masses of the atlas or the pedicles of the axis, there is a need for extending the posterior instrumentation both proximally to the occiput and distally to the subaxial spine.

Patients who presented with the anterior disease only and with no gross atlantoaxial joint instability were subjected to anterior surgical procedures like transoral core needle biopsy (two patients), retropharyngeal abscess drainage (one patient) and anterior stabilization with plates and screws by submandibular approach (one patient).

Transoral core needle biopsy is an ideal method for procuring diseased tissue from lesions of the anterior structures of the atlantoaxial articulation for histopathological examination and GeneXpert study. In this study, two patients with atlantoaxial tuberculosis underwent transoral core needle biopsy to obtain tissue for diagnosis.

Retropharyngeal and submandibular approaches being complex may be indicated when the tuberculous focus is located in the anterior portion of the atlantoaxial complex with intact posterior structures. This approach enables the surgeon to deal with the C1-C2 articulation directly and to perform debridement and instrumented fusion [Figure 2].


  Conclusions Top


Apart from the standard anti-tubercular chemotherapy, which is the cornerstone of the treatment of spinal tuberculosis, there are certain specific considerations for atlantoaxial tuberculosis. Transoral needle biopsy is an ideal option for procuring tissue for diagnosis in patients with anterior lesions of the C1-C2 segment. Transoral decompression with its attendant morbidity may not be indicated in most patients. In patients with extensive bony involvement and in the presence of instability, posterior stabilization may be indicated. The integrity of the lateral masses of C1 and pedicles of C2 vertebra are the determinants for the feasibility of posterior stabilization procedures. In the event of extensive destruction of either C1 or C2 vertebra, there is a need to extend the posterior stabilization construct proximally to the occiput or distally to the subaxial spine. The anterior approaches (lateral retropharyngeal or submandibular) may be required in dealing with lesions located in the anterior part of the atlantoaxial complex.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
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Chadha M, Agarwal A, Singh AP. Craniovertebral tuberculosis: A retrospective review of 13 cases managed conservatively. Spine (Phila Pa 1976) 2007;32:1629-34.  Back to cited text no. 4
    
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Shukla D, Mongia S, Devi BI, Chandramouli BA, Das BS. Management of craniovertebral junction tuberculosis. Surg Neurol 2005;63:101-6.  Back to cited text no. 5
    
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Behari S, Nayak SR, Bhargava V, Banerji D, Chhabra DK, Jain VK, et al. Craniocervical tuberculosis: Protocol of surgical management. Neurosurgery 2003;52:72-80.  Back to cited text no. 8
    
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Arunkumar MJ, Rajshekhar V. Outcome in neurologically impaired patients with craniovertebral junction tuberculosis: Results of combined anteroposterior surgery. J. Neurosurg Spine 2002;97:166-71.  Back to cited text no. 9
    
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Wang B, Shang R, Yang T, Zhang H, Hu H, Hu W, et al. Evaluation of clinical outcomes of one-stage anterior and posterior surgical treatment for atlantoaxial tuberculosis complicated with neurological damage. BMC Musculoskelet Disord 2019;20:148.  Back to cited text no. 10
    
11.
Yadav YR, Madhariya SN, Parihar VS, Namdev H, Bhatele PR. Endoscopic transoral excision of odontoid process in irreducible atlantoaxial dislocation: Our experience of 34 patients. J Neurol Surg A Cent Eur Neurosurg 2013;74:162-7.  Back to cited text no. 11
    
12.
Xing S, Gao Y, Gao K, Zhang G, Yu Z. Anterior cervical retropharyngeal debridement combined with occipital cervical fusion to upper cervical tuberculosis. Spine (Phila Pa 1976) 2016;41:104-10.  Back to cited text no. 12
    
13.
Yin QS, Ai FZ, Zhang K, Mai XH, Xia H, Wu ZH, et al. Transoral atlantoaxial reduction plate internal fixation for the treatment of irreducible atlantoaxial dislocation: A 2-to 4-year follow-up. Orthop Surg 2010;2:149-55.  Back to cited text no. 13
    
14.
Wang C, Yan M, Zhou HT, Wang SL, Dang GT. Open reduction of irreducible atlantoaxial dislocation by transoral anterior atlantoaxial release and posterior internal fixation. Spine (Phila Pa 1976) 2006;31:E306-13.  Back to cited text no. 14
    
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Bao D, Li L, Gong M, Xiang Z. Treatment of atlantoaxial tuberculosis with neurological impairment: A Systematic review. World Neurosurg 2020;135:7-13.  Back to cited text no. 15
    
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Nurick S. The pathogenesis of the spinal cord disorder associated with cervical spondylosis. Brain 1972;95:87-100.  Back to cited text no. 17
    
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ASIA and ISCoS International Standards Committee. The 2019 revision of the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI)-What's new? Spinal Cord 2019;57:815-7.  Back to cited text no. 18
    
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Lifeso R: Atlanto-axial tuberculosis in adults. J Bone Joint Surg Br 1987;69:183-7.  Back to cited text no. 19
    
20.
Goyal T, Tripathy SK, Bahadur R. Tuberculous altantoaxial subluxation: A case report with review of literature. Musculoskelet Surg 2014;98:67-70.  Back to cited text no. 20
    
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Chaudhary K, Potdar P, Bapat M, Rathod A, Laheri V. Structural odontoid lesions in craniovertebral tuberculosis: A review of 15 cases. Spine (Phila Pa 1976) 2012;37:E836-43.  Back to cited text no. 21
    
22.
Zhang HQ, Lin MZ, Guo HB, Ge L, Wu JH, Liu JY, et al. One-stage surgical management for tuberculosis of the upper cervical spine by posterior debridement, short-segment fusion, and posterior instrumentation in children. Eur Spine J 2013;22:72-8.  Back to cited text no. 22
    
23.
Mandavia R, Fox R, Meir A. Atlantoaxial TB with paralysis: Posterior-only cervical approach with good results. JRSM Open 2017;8:2054270417697866.  Back to cited text no. 23
    


    Figures

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