Neurol Med Chir (Tokyo) 45, 512¿518, 2005

Craniovertebral Junction Realignment for the Treatment of Basilar Invagination With : Preliminary Report of 12 Cases

Atul GOEL and Praveen SHARMA

Department of Neurosurgery, King Edward Memorial Hospital and Seth Gordhandas Sunderdas Medical College, Parel, Mumbai, India

Abstract

Twelveselectedpatients,eightmalesandfourfemalesaged14to50years,withsyringomyeliaassoci- ated with congenital craniovertebral bony anomalies including basilar invagination and fixed atlan- toaxial dislocation, and associated Chiari I malformation in eight, were treated by atlantoaxial joint manipulation and restoration of the craniovertebral region alignment between October 2002 and March 2004. Three patients had a history of trauma prior to the onset of symptoms. Spastic quadriparesis and ataxia were the most prominent symptoms. The mean duration of symptoms was 11 months. The atlan- toaxial dislocation and basilar invagination were reduced by manual distraction of the facets of the atlas and axis, stabilization by placement of bone graft and metal spacers within the joint, and direct atlantoaxial fixation using an inter-articular plate and screw method technique. Following surgery all patients showed symptomatic improvement and restoration of craniovertebral alignment during follow up from 3 to 20 months (mean 7 months). Radiological improvement of the syrinx could not be evaluated as stainless steel metal plates, screws, and spacers were used for fixation. Manipulation of the atlantoaxial joints and restoring the anatomical craniovertebral alignments in selected cases of syringomyelia leads to remarkable and sustained clinical recovery, and is probably the optimum surgical treatment.

Key words: atlantoaxial dislocation, basilar invagination, , syringomyelia

Introduction tiary response to reduction in the posterior cranial fossa volume resulting from the primary craniover- The complex of basilar invagination, Chiari I mal- tebral anomaly of basilar invagination and sec- formation, and syringomyelia is relatively common, ondary Chiari I malformation. Accordingly, whereas the association with fixed atlantoaxial posterior fossa bony decompression was recom- dislocationislesscommonbutnotrare.1,4,7,13,15–20) mended for this subgroup of patients. Such cases are generally treated by either anterior The present study included 12 patients with syrin- transoral or posterior bony gomyelia associated with bony abnormalities of the decompression. The indications for opening of the craniovertebral region including `fixed' atlantoaxial dura and manipulation of the arachnoid membrane, dislocation and basilar invagination, and with tonsils, and obex, and draining of the syrinx cavity Chiari I malformation in eight patients. All patients are currently under discussion. No specific fixation were treated by attempted reduction of the atlan- procedure has been recommended for fixed atlan- toaxial dislocation and basilar invagination, and by toaxial dislocation associated with basilar invagina- direct lateral mass plate and screw atlantoaxial tion in the presence of syringomyelia.6) fixation by our reported techniques.5,9,11) No bony or We previously classified cases of syringomyelia dural decompression or neural manipulation of any into three groups and suggested specific treatment kind was performed. protocols on the basis of the possible pathogenetic factors.7,8) We suggested that syringomyelia is a ter- Patients and Methods

Received September 17, 2004; Accepted March 31, Twelve patients with syringomyelia associated with 2005 `fixed' atlantoaxial dislocation and basilar invagina-

512 Craniovertebral Realignment for Syringomyelia 513

Table 1 Principal presenting clinical features

Number of patients Clinical features Preoperative Postoperative

Neck pain 9 recovered in all 9 Torticollis 3 near complete correction of torticollis in all 3 Lower cranial nerve affection 1 improved Weakness all 12 patients improved and were able to walk unaided able to walk unaided 10 needed support to walk 2 Sensations all patients improved; residual affection of kinesthetic normal sensations 3 sensations in 3 patients, residual partial affection of kinesthetic sensations affected 9 spinothalamic sensations in 4 spinothalamic sensations affected 6 Sphincter disturbance 2 recovered

Table 2 Preoperative radiological measurements and changes following surgery

CL (mm) WL (mm) ADI (mm) Omega angle (degrees) Case Age/ Chiari No. Sex Pre Post Dt Pre Post Dt Pre Post Dt Pre Post Alt

122/M15123 6061376708010＋ 2 23/M 8 4 4 5 2 3 18 10 8 40 60 20 － 347/M844 5051257507020＋ 4 48/M 13 4 9 8 0 8 27 6 21 60 85 25 ＋ 5 14/M 9 6 3 15 9 6 20 11 9 60 80 20 － 630/M853 4041394458035－ 7 37/M 10 4 6 8 0 8 13 2 11 75 90 25 ＋ 8 50/F 14 8 6 11 0 11 18 6 12 75 80 5 － 9 35/F 8 3 5 9 2 7 18 5 13 70 80 10 ＋ 10 24/F 12 7 5 10 0 10 13 5 8 75 84 9 ＋ 11 26/M 18 7 11 7 2 5 13 6 7 65 76 11 ＋ 12 32/F 14 8 6 12 2 10 14 6 8 65 80 15 ＋

Values show the distance between the tip of the odontoid process and the anatomical references. Chamberlain's line (CL): This line connects the posterior border of the hard palate to the opisthion. The tip of the odontoid process normally lies below this line.3,7) Wackenheim's line (WL): This line is the clivus baseline extended downwards. Normally, the tip of the odontoid process remains anterior to this line.7,21) Modified omega angle: A line is drawn traversing along the center of base of the axis parallel to the line of the hard palate. The inclination of the tip of the odontoid process to this line is defined as the modified omega angle.7,14) ADI: atlantodental interval, Alt: alteration, Dt: distraction, Pre: preoperative, Post: postoperative. tion were treated between October 2002 and March years (mean 11 months). 2004. Eight patients also had Chiari I malformation. All patients were investigated with magnetic Atlantoaxial dislocation was defined as `fixed' if the resonance imaging, computed tomography, and minimum distance between the tip of the odontoid dynamic radiography. Measurements of structures process and the posterior surface of the anterior based on the radiological studies are shown in arch of the atlas or clivus (in patients with assimilat- Table 2. Measurements were made on all available ed atlas) was more than 4 mm and there was no clear studies and were averaged. Partial or complete radiographic evidence of any reduction of the sub- occipitalization of the atlas was present in eight luxation with extension of the neck. patientsandfusionofC-2andC-3wasobservedin The clinical features of the patients are presented five. Os odontoideum was seen in three patients. in Table 1. Trauma of varying severity was the The surgical techniques employed were described principal precipitating factor in three patients. The previously.5,9–11) Cervical traction is progressively duration of symptoms ranged from 15 days to 5 increased to approximately one-fifth of the total

Neurol Med Chir (Tokyo) 45,October,2005 514 A. Goel et al.

Fig. 1 Case 4. A: Preoperative radiograph of the craniovertebral region with the neck in flexion showing occipitalization of the atlas, fusion of the C-2 and C-3 vertebrae, atlantoaxial dislocation, and basilar invagination. B: Preoperative radiograph of the craniovertebral region with the neck in extension showing persistent atlantoaxial dislocation. C: Preopera-

tive T1-weighted magnetic resonance image showing basilar invagination, fixed atlantoaxial dislocation, Chiari I malformation, and syringomyelia. D: Preoperative computed tomography (CT) scan showing basilar invagination, fixed atlantoaxial dislocation, occipitalization of the atlas, and fusion of the C-2 and C-3 vertebrae. E: Postoperative radiograph with the neck in flexion showing the fixation with plates and screws, and the spacers within the joint cavity. F: Postoperative CT scan showing reduction of the basilar invagination and atlantoaxial dislocation. body weight prior to induction of anesthesia. The joint space. The average spacer measures 10 mm patient is placed prone with the head end of the table in length, 8 mm in breadth, and 4 mm in height. elevated to about 35 degrees. Use of the operating Titanium spacers have multiple small holes to per- microscope facilitates the dissection and screw mit bone fusion and are tapered at one end for easier implantation. The bilateral atlantoaxial facet joints placement in the joint cavity. Multiple bone graft are widely exposed after sectioning of the large C-2 chips are used to fill the distracted joint space ganglion. Exposure of the facet of the atlas was around the spacer. significantly difficult in the present group of Plate and screw fixation of the region is then car- patients because of assimilation of the atlas in most ried out by the interarticular technique.9,11) Atwo- cases and the rostral location of the basilar invagina- holed stainless steel plate measuring 15–20 mm in tion and the atlantoaxial joint. The joint capsule is length and screws of 2.4–2.6 mm diameter and excised and the articular cartilage widely removed 16–22 mm length are used. The screws are passed using the microdrill. The bilateral joints are distract- bilaterally through the holes in the plate into the ed using the intervertebral spreader used in anterior lateral mass of the atlas and axis (Figs. 1 and 2). The cervical disc surgery. The status of the dislocation site and angle of screw implantation is modified to and basilar invagination is evaluated by intraopera- suit the local anatomical situation. The preferred tive radiography. site of screw insertion is at the center of the The distraction of the C-1 and C-2 facets is posterior surface of the lateral mass of the atlas, 1 to maintained by titanium spacers, which are inserted 2 mm above the articular surface, but if there was into the joints (Figs. 1 and 2). The size of the spacers difficulty in exposure due to inadequate space, depends on the space available within the distracted screw insertion is done through the articular sur-

Neurol Med Chir (Tokyo) 45, October, 2005 Craniovertebral Realignment for Syringomyelia 515

Fig. 2 Case 1. A: Preoperative radiograph of the craniovertebral region with the neck in flexion showing occipitalization of the atlas, fusion of the C-2 and C-3 vertebrae, atlantoaxial dislocation, and basilar invagination. B: Preoperative radiograph of the craniovertebral region with the neck in extension showing persistent atlantoaxial dislocation. C: Preopera-

tive T1-weighted magnetic resonance (MR) image showing basilar invagination, fixed atlan- toaxial dislocation, Chiari I malformation, and syringomyelia. D: Preoperative sagittal computed tomography (CT) scan showing dislocation of the facet of the atlas over the facet of the axis. E: Preoperative CT scan showing basilar invagination, fixed atlantoaxial disloca- tion, occipitalization of the atlas, and fusion of the C-2 and C-3 vertebrae. F: Postoperative radiograph with the neck in flexion showing the fixation with plates and screws, and the spacers within the joint cavity. G: Postoperative CT scan showing reduction of the basilar invagination and atlantoaxial dislocation. H: Postoperative sagittal CT scan showing reduction of the atlantoaxial dislocation and realignment of the facets. I: Postoperative coronal CT scan showing the screws in the facets of the atlas and axis and distraction of the joint. face. The preferred site of screw implantation in the screws in both the anterior and posterior cortices is pars of the axis is the medial and superior third. preferable but not mandatory. Additional bone graft Themedialsurfaceoftheparsisidentifiedbefore was placed between the posterior elements of the implantation of the screw. Devices used to cut and C-1-suboccipital bone complex and C-2 after decorti- mold the small metal plates are commercially availa- cation of the host bone area with a burr. ble. The lateral masses of the atlas and axis are firm Postoperatively the traction is discontinued and and cortical in nature, and engagement of the the patient must wear a four-post hard cervical

Neurol Med Chir (Tokyo) 45,October,2005 516 A. Goel et al. collar for 3 months. All activities involving neck distraction, and reduction of basilar invagination.5) movements are restrained during this period. This technique was used to reduce the fixed atlantoaxial dislocation and distraction, and reduce Results the basilar invagination in patients with associated syringomyelia. We consider that the atlantoaxial All patients improved in the symptoms to varying joint in such cases is in an abnormal position as a degrees following surgery and were independent result of congenital abnormality of the bones, and and active in their lives during the follow-up period progressive worsening of the dislocation is probably of3to20months(mean7months)(Table1).There secondary to increasing `slippage' of the atlas over were no intraoperative or postoperative vascular, the axis. The slip of atlas over the axis appears to be neural, or infectious complications. The postopera- accentuated by the event of trauma. A history of tive changes in various radiological parameters are trauma preceding the clinical events, complaints of showninTable2.Noneofthepatientssuffered pain in the neck, and improvement in neurological delayed neurological deficits requiring transoral or symptoms following institution of cervical traction posterior decompression, or any other surgical suggest `vertical' instability of the craniovertebral procedure. No patient needed re-exploration for region. Our experience has shown that the joint in failure of fixation of the implant. Immediate such cases is not `fixed' or `fused' but is mobile and postoperative and follow-up radiography confirmed in some cases is hypermobile, and is probably the fixation and fusion, and reduction of the atlantoaxi- prime cause of the atlantoaxial dislocation and al dislocation and basilar invagination. Bone fusion the basilar invagination. The remarkable clinical was assumed to have occurred if the implant improvement following reduction of the atlantoaxial maintained the distraction, and reduction of the dislocation and basilar invagination indicates that atlantoaxial dislocation and basilar invagination on the complex of atlantoaxial dislocation, basilar dynamic radiography 3 months after surgery. invagination, and syringomyelia is probably sec- Successful and sustained reduction of the atlantoax- ondary to the primary craniovertebral instability. ial dislocation and distraction, and reduction of Opening of the atlantoaxial joint in patients with basilar invagination were observed in all patients. fixed atlantoaxial dislocation, occipitalized atlas, The extent of reduction of the syringomyelia cavity and basilar invagination is technically relatively could not be conclusively demonstrated due to the complex.5,10) The relationship of the vertebral artery type of metal plate and screws used for fixation. All to the atlantoaxial joint complex has to be evaluated patients suffered some degree of sensory loss in the on the basis of preoperative radiological studies.2,12) distribution of the C-2 nerves. Wide removal of the atlantoaxial joint capsule and articular cartilage by drilling and subsequent dis- Discussion traction of the joint by manual manipulation pro- vides a unique opportunity to obtain reduction of Most patients with syringomyelia related to Chiari the basilar invagination and atlantoaxial disloca- malformation but without bony anomaly of the tion. The joints could be maintained in the distract- craniovertebral region have hyporeflexia of the ed and reduced position with the help of bone graft upper extremities and spastic lower extremities. and spacers. The subsequent fixation of the joint Our patients presented with spastic quadriparesis, with interarticular screws and a metal plate pro- suggesting that the symptoms were related to com- vides a biomechanically firm fixation. The fixation pression of the by the invaginated dens was strong enough to sustain the vertical, trans- rather than syringomyelia. Patients with fixed verse, and rotatory strains of the most mobile region atlantoaxial dislocation, basilar invagination, Chiari of the spine. The biomechanical advantage afforded I malformation, and syringomyelia are relatively by our technique is illustrated by our successful fu- younger, with neck pain and far more prominent sion results in the present and previous series.5,9–11) motor symptoms and ataxia than in patients with Following surgery, the alignment of the odontoid similar features without craniovertebral region bony process and the clivus, and the entire craniover- anomaly.7,8) tebral junction became normalized. We could obtain Realignment of the bones in the craniovertebral varying degrees of reduction of the basilar invagina- junction can be attempted in patients with syrin- tion and atlantoaxial dislocation. The atlantoaxial gomyelia associated with `fixed' atlantoaxial disloca- alignments became normal and the tip of the odon- tion, with or without basilar invagination and Chiari toid process receded with respect to Wackenheim's malformation. We recently described a technique clival line21) and Chamberlain's line3) suggesting for reduction of fixed atlantoaxial dislocation and reduction of the basilar invagination and atlantoaxi-

Neurol Med Chir (Tokyo) 45, October, 2005 Craniovertebral Realignment for Syringomyelia 517 al dislocation. The posterior tilt of the odontoid 8) Goel A, Desai KI: Surgery for syringomyelia: An process, as evaluated by the modified omega angle, analysis based on 163 surgical cases. Acta Neurochir was reduced after the surgery.7,14) (Wien) 142: 293–302, 2000 All patients showed sustained neurological 9) Goel A, Desai K, Muzumdar D: Atlantoaxial fixation improvement to various degrees, indicating that the using plate and screw method: A report of 160 treat- ed patients. Neurosurgery 51: 1351–1357, 2002 procedure was effective. The clinical improvement 10) Goel A, Kulkarni AG: Mobile and reducible in the immediate postoperative phase was obviously atlantoaxial dislocation in presence of occipitalized due to decompression of the invaginated brainstem atlas: report on treatment of eight cases by direct as shown by postoperative radiology. Stainless steel lateral mass plate and screw fixation. Spine 29(22): plates, non-locking screws, and custom-made E520–E523, 2004 spacers were used due to the higher costs of branded 11) Goel A, Laheri VK: Plate and screw fixation for material. The effect on syringomyelia could not be atlanto-axial subluxation. Acta Neurochir (Wien) 129: confirmed as the size of the syrinx could not be 47–53, 1994 radiologically evaluated due to the type of metal 12) Gupta S, Goel A: Quantitative anatomy of lateral instruments used. masses of the atlas and axis vertebrae. Neurol India Resection of the C-2 ganglion is necessary to 48: 120–125, 2000 13) Guyotat J, Bret P, Jouanneau E, Ricci AC, Lapras C: achieve the exposure but results in an area of Syringomyelia associated with type I Chiari malfor- numbness along the distribution of the nerve.5,9–11) mation. A 21-year retrospective study on 75 cases However, the area of numbness progressively treated by foramen magnum decompression with a decreases over the years and was not a disabling special emphasis on the value of tonsils resection. feature in any patient. All activities related to neck Acta Neurochir (Wien) 140: 745–754, 1998 movements were restricted for a 3-month period to 14) Klaus E: Rontgendiagnostik der platybasic und provide an opportunity for bone fusion in the joint. basilar Impression. Fortschr Rontgenstr 86: 460–469, Experience with the described technique is limit- 1957 (Ger) ed, but our results suggest that realignment and 15) McRae DL: Bony abnormalities in the region of direct fixation of atlantoaxial joint may be indicated foramen magnum: correlation of anatomic and for selected patients with syringomyelia. The proce- neurologic findings. Acta Radiol 40: 335–354, 1953 dure is technically demanding and requires high 16) Menezes AH: Primary craniovertebral anomalies and hindbrain herniation syndrome (Chiari I): data anatomic accuracy, but the neurological outcome is base analysis. Pediatr Neurosurg 23: 260–269, 1995 extremely gratifying. 17) Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC: Chiari I malforma- References tion redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44: 1) Bindal AK, Dunsker SB, Tew JM Jr: Chiari I malfor- 1005–1017, 1999 mation: classification and management. Neurosur- 18) Pillay PK, Awad IA, Little JR, Hanh JF: Symptomatic gery 37: 1069–1074, 1995 Chiari malformation in adults: a new classification 2) Cacciola F, Phalke U, Goel A: Vertebral artery in based on magnetic resonance imaging with clinical relationship to C1-C2 vertebrae: an anatomical study. and prognostic significance. Neurosurgery 28: Neurol India 52: 178–184, 2004 639–645, 1991 3) Chamberlain WE: Basilar impression (platybasia). A 19) Schijman E, Steinbok P: International survey on the bizarre developmental anomaly of the occipital bone management of Chiari I malformation and syrin- and upper cervical spine with striking and mislead- gomyelia. Childs Nerv Syst 20: 341–348, 2004 ing neurologic manifestations. Yale J Biol Med 11: 20) Stevens JM, Serva WA, Kendall BE, Valentine AR, 487–496, 1939 Ponsford JR: Chiari malformation in adults: relation 4) Chiari H: Ueber Verderbungen des Kleinhirns of morphological aspects to clinical features and infolge von Hydrocephalie des Grossihirns. operative outcome. J Neurol Neurosurg Psychiatry 56: Dwochenschr 17: 1172–1175, 1891 (Ger) 1072–1077, 1993 5) Goel A: Treatment of basilar invagination by 21) Thiebaut F, Wackenheim A, Vrousos C: [New median atlantoaxial joint distraction and direct lateral mass sagittal pneumostratigraphical finding concerning fixation. JNeurosurgSpine1(3): 281–286, 2004 the posterior fossa]. JRadiolElectrolMedNucl42: 6) Goel A, Achawal S: Surgical treatment for Arnold 1–7, 1961 (Fre) Chiari malformation associated with atlantoaxial dislocation. Br J Neurosurg 9: 67–72, 1995 Address reprint requests to:A.Goel,M.D.,Head, 7) Goel A, Bhatjiwale M, Desai K: Basilar invagination: Department of Neurosurgery, King Edward VII a study based on 190 surgically treated cases. J Memorial Hospital, Parel, Mumbai–400012, India. Neurosurg 88: 962–968, 1998 e-mail: atulgoel62＠hotmail.com

Neurol Med Chir (Tokyo) 45,October,2005 518 A. Goel et al.

Commentary ptoms. Based on their present experience, how do they manage in such severe advanced cases? Drs. Goel and Sharma report their surgical experience Also, if they could have followed up the syrinx in twelve patients with compressive brain stem and resolution of their patients with serial MR imaging by high cervical cord lesion secondary to basilar invagi- intraoperative use of instrumentation tools and nation with syringomyelia with mean duration of devices made of titanium instead of steel, they could symptoms being eleven months. Dislocation was have provided high core evidence of improvement by manually reducible in all patients without assistance resumption of craniovertebral stability by satisfactory of skeletal traction and/or further extensive disarticu- alignment. At any rate, the authors are congratulated lation of the facets and joints for realignment under for their excellent surgical outcome and results in this general anesthesia in a prone position. Their series complex of lesions. consists of all selected patients of reducible disloca- Hiromichi HOSODA,M.D. tion. I wonder if they have any experience with Department of Neurosurgery patients other than these twelve patients with Chigasaki Tokushukai Medical Center compressive myelopathy with more advanced ir- Chigasaki, Kanagawa, Japan reducible dislocations and longer duration of sym-

Neurol Med Chir (Tokyo) 45, October, 2005