Basilar invagination: a study based on 190 surgically treated patients

Atul Goel, M.CH.H, Mohinish Bhatjiwale, M.S., M.CH.H, and Ketan Desai, M.S., M.CH.H Department of , King Edward Memorial Hospital and Seth Gordhandas Sunderdas Medical College, Parel, Bombay, India

Object. The authors analyzed the cases of 190 patients with that was diagnosed on the basis of criteria laid down in 1939 by Chamberlain to assess the appropriate surgical procedure. Methods. Depending on the association with , the anomaly of basilar invagination was classified into two groups. Eighty-eight patients who had basilar invagination but no associated Chiari malformation were assigned to Group I; the remainder of the patients, who had both basilar invagination and Chiari malformation, were assigned to Group II. The principal pathological characteristic was observed to be direct compression due to odontoid process indentation in Group I and a reduction in posterior cranial fossa volume in Group II. Conclusions. Despite the anterior concavity of the brainstem in both groups, transoral surgery was the most suitable procedure for those patients in Group I and decompression of the was found to be appropriate for patients in Group II. After surgical decompression, a fixation procedure was found to be necessary in most Group I cases, but only in a small minority of Group II cases. Key Words * basilar invagination * * Chiari malformation * craniovertebral anomaly

Basilar invagination, a primary developmental anomaly,[19,45] has been a subject of clinical interest for some time.[4,5,7,14,20,22,26,28,29,31,32,40,45­47] Lessons learned during the management of 190 cases of basilar invagination are analyzed in this report. CLINICAL MATERIAL AND METHODS Approximately 1800 patients with craniovertebral anomalies were treated in the neurosurgery department at King Edward Memorial Hospital between 1950 and 1996. In the present study 190 cases of patients with basilar invagination who were surgically treated between January 1987 and March 1997 have been reviewed and analyzed. Analysis of cases treated before 1994 was retrospective; analysis of cases treated after that time was prospective. Included in the study were only those patients in whom magnetic resonance (MR) imaging and/or computerized tomography (CT) scanning in addition to conventional radiography was performed. Magnetic resonance imaging was available in 138 cases and CT scanning in 108 cases. In accordance with the criteria for diagnosis of basilar invagination, the tip of the odontoid

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC process was at least 2.5 mm above Chamberlain's line[4] in each case. Depending on the presence or absence of Chiari malformation, the series was divided into two groups. Group I was composed of 88 patients without associated Chiari malformation (Fig. 1); Group II was composed of 102 patients with associated Chiari malformation (Fig. 2). Follow-up review ranged from 2 months to 9 years (average 43 months). Sixteen patients did not report for any follow-up examination after discharge from the hospital and they were evaluated on the basis of their hospital stay. Six patients communicated only through letters informing us of their clinical condition.

Fig. 1. Magnetic resonance image obtained in an 8-year-old boy with Group I basilar invagination.

Fig. 2. Magnetic resonance image obtained in a 34-year-old man with Group II basilar invagination. Extensive syringomyelia is noted. RESULTS

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC The clinical features of the cases are presented in Table 1. Trauma of varying severity was the principle precipitating factor in 48% of the Group I cases. In no case in Group II did trauma play any role in initiating the symptoms. Infections probably precipitated events in four patients in Group I. Of these, one patient had cervical tuberculous lymphadenitis, whereas the other three had chronic respiratory tract infections.

Radiographic Studies Measurements of structures based on radiological studies are shown in Table 2. Measurements were made on all available studies and were averaged. The landmarks used for the measurements of various indices were based on a review of original papers by VanGilder, et al.,[44] and are shown in Fig. 3.

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC Unauthenticated | Downloaded 09/27/21 12:44 PM UTC Fig. 3. Line drawing showing landmarks used for measurements. b = basal line; c = Chamberlain's line; t = tuberculum sellae­torcular herophili line; w = Wackenheim's clival line. The basal angle is the angle between lines b and w. The Klaus height index on plain radiography is the distance from the tip of the odontoid process to line t. On MR imaging, the Klaus height index[22] was measured from the tip of the odontoid process to a line drawn along the tentorium. The omega angle was modified as shown in Fig. 4. The line of the palate was taken as a fixed parameter and a parallel line was drawn from it, passing from the center of the base of the . The angle of the odontoid process was measured on this line. Syringomyelia was present only in Group II; a syrinx was identified in 51 (50%) of these cases. Occipitalization of the atlas was seen in 72 patients (81%) in Group I and 81 patients (79%) in Group II. Fusion of C-2 and C-3 was observed in 49 cases (56%) in Group I and 43 cases (42%) in Group II. Lateral or paramesial compression by the lateral mass of the atlas or the occipital condyle was seen in 21 patients (24%) in Group I and 18 patients (18%) in Group II.

Fig. 4. Line drawing showing the parameters for measurement of the modified omega line.

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC Line A is drawn along the hard palate. Line B is parallel to line A and passes through the center of the base of the axis. Line C extends from the center of the base of the axis along the tip of the odontoid process. The angle between line B and line C is the modified omega angle. Spinal Instability Factor. Instability was defined as the clear radiographic presence of mobile subluxation with flexion resulting in an increase in the atlantodental or clivodental interval, increased compromise of the canal diameter, or reduction in the girth of the brainstem. Spinal instability was seen in three patients (3%) in Group I and one patient (1%) in Group II. Surgical Procedures Before surgery, 82 patients in Group I and 19 patients in Group II were placed in cervical traction. A majority of patients (68 or 82%) in Group I improved clinically following application of traction. The improvement was almost instantaneous in most cases. One patient (5%) in Group II improved as a result of traction. Following traction, the omega angle, Chamberlain's line, atlantodental or clivodental interval, and craniocervical angulation reduced toward normal values in Group I. There was no alteration in these parameters in any patient in Group II.

Table 3 shows the surgical methods and Table 4 provides a summary of the results of those surgeries. In Group II, dorsal foramen magnum bone decompression and duraplasty were performed in 75 patients (74%) in the earlier portion of the series (average duration of follow up 55 months). In most of these cases, the suboccipital bone, the rim of the foramen magnum, and the dura overlying the herniating tonsils were thin. The dura was either left open or a dural homograft was applied. No attempt was made to lyse adhesions around the herniating tonsils or to manipulate the area of the obex. Bone decompression of the foramen magnum alone was performed in 16 patients (16%) treated after 1994 (average follow up 18 months). Simultaneously with the foramen magnum decompression, lateral fixation was performed in eight patients.[16,18] In the 51 patients in whom a syrinx was identified, syringotomy was performed in 38 (75%); this involved insertion of a Silastic draining tube that ran from the syrinx at its maximum dimension to the subarachnoid space. In 13 patients (25%) no direct surgical intervention for the syrinx was undertaken. In the early portion of the series, such an approach was adopted in seven patients in whom the syrinx was relatively small. In the later portion of the series bone decompression of the foramen magnum alone was performed, even in the presence of the syrinx (in six patients).

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC Transoral surgery was performed in 99 patients (Group I, 78 patients [89%]; Group II, 21 patients [21%]) (Table 3). Following transoral surgery, in six cases homologous bone graft was placed between the drilled portion of the vertebral body of the axis and the inferior part of the to assist fusion. In three patients a transoral plate and screw fixation of the clivus to the cervical vertebral body was performed.[17 ] The bone graft was placed underneath the metal plate. These patients were placed in halo fixation following the surgery. Problems of infection and rejection of the metal implant in one case and poor or no visualization of the bone graft on postoperative follow-up imaging in other cases led to the abandonment of anterior fixation. Dorsal fixation (Table 3) was performed in the same surgical session following a transoral surgical procedure in 18 Group I patients. In these cases the indication for immediate fixation was relatively high mobility of the cervical vertebral bodies during drilling. In 39 other Group I patients, fixation was performed as a second-stage surgery. Excessive pain and spasm of the muscles and suboccipital radicular pain formed the primary indication for fixation in these patients. No patient worsened in motor function prior to second-stage fixation. In this group fixation was performed after the initial surgery within 15 days in 16 patients, within 2 months in 11 patients, and between 2 and 6 months in 12 patients. In four additional Group I patients a posterior fixation procedure was performed in an apparently reduced position of the basilar invagination and the atlantoaxial dislocation following cervical traction. However, all four patients needed transoral surgery at a later stage because the reduced position could not be maintained by the implant. In Group II, a posterior fixation procedure was conducted following transoral decompression in the same surgical sitting in one patient. In four patients fixation was performed within 2 weeks after transoral surgery. No patient needed a fixation procedure as a delayed measure. In six Group II patients, no fixation was necessary, even after both anterior and posterior decompressive operations. DISCUSSION Although other subclassifications of basilar invagination have been described,[22,34,37,47] we found division on the basis of presence or absence of Chiari malformation to be appropriate. It divided the

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC anomaly into two discrete types that probably have a common embryological origin,[30] but diverse patterns of clinical presentation, radiological features, and management considerations. Clinical Features and Radiological and Pathological Characteristics On the basis of radiological studies it appeared that in Group I there was invagination of the cervical spine into the base of the . The definition of basilar invagination as being prolapse of the spine into the base of the skull, as suggested by von Torklus,[46] was only appropriate to Group I. In Group II, the clivus was invaginated along with the cervical spine into the posterior cranial fossa. Analysis on the basis of Chamberlain's line[4,13,29,44] and on the distance from the odontoid tip to the pontomedullary junction (Table 2) showed that basilar invagination was much more severe in patients in Group II than in those in Group I. As judged by the atlantodental or clivodental interval, there was an element of "fixed" atlantoaxial dislocation in Group I. The tip of the odontoid process was significantly superior to Wackenheim's clival line in Group I; in Group II it remained below both Wackenheim's clival line and McRae's line[29] of the foramen magnum. On the basis of the Klaus height index,[27,30,39,43] posterior fossa height was only moderately affected or not affected at all in Group I, but was markedly reduced in Group II. The superior position of the odontoid process in patients in Group II was associated with a more horizontal angulation and shortening of the clivus and rostral positioning of the plane of the foramen magnum.[26,43] Platybasia was seen in both groups,[6] but was relatively less frequent and less severe in Group I (Table 2). In Group II, it appears that platybasia was as important as invagination of the odontoid process in causing the anterior concavity of the brainstem and in reducing the volume of the posterior fossa. The anterior concavity of the brainstem formed a pattern of smooth curvature in Group II, whereas the concavity was acute in Group I, the angle being formed by the tip of the odontoid process. The anteroposterior diameter of the foramen magnum was markedly reduced in Group I, whereas it was only marginally reduced, unaffected, or even greater than normal in Group II. Although the brainstem girth was markedly reduced in Group I, it was only marginally affected or unaffected in Group II, indicating thereby that there was no direct brainstem compression as a result of the odontoid process in the latter group. In this study a modified omega angle[22] was used because the line of the hard palate was unaffected by the relative movement of the head and cervical spine during neck movement in these "fixed" craniovertebral anomalies. Facial hypoplasia or hard palatal abnormality was not seen in any case in this series and did not affect the measurements. The reduction in the omega angle in Group I showed that the odontoid process had tilted toward the horizontal plane and was posteriorly angulated in Group I, whereas it was closer to the vertical plane in Group II (Table 2). The association of Chiari malformation, syringomyelia, and basilar invagination has been the subject of various studies.[5,8,10,12,24,31,34] There was Grade I Chiari malformation in all our Group II cases. The presence and extent of the syrinx did not correlate with the severity of basilar invagination and tonsilar herniation.[42] Age and Gender of Patients A significant majority of Group I patients were adolescents (Table 1). Patients in Group II were older at the time of presentation.[10] Male predominance[22,24,29,36,48] was more marked in Group I (72%) than in Group II (54%). Analysis of Symptoms Symptom presentation was relatively acute in patients in Group I, whereas it was longstanding and

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC slowly progressive in patients in Group II (Table 1). Although long term use of the head to carry loads has been recorded as a precipitating factor in some previous studies from India,[1,38] it did not seem significant in this series. In Group I, pyramidal symptoms formed a dominant component. Kinesthetic sensations were also affected in a large majority of cases. In Group II, spinothalamic sensory dysfunction and were equally significant to motor and deep sensory system affection (Table 1). Neck pain and spasms of the muscles of the nape of the neck were frequent findings in Group I. These features suggested strain on the muscles that was secondary to subtle spinal instability in the region. The fact that trauma influenced acute development of symptoms in a large number of Group I cases (48%) also pointed toward an element of spinal instability in the craniovertebral region. Mere physical examination of patients with basilar invagination was of diagnostic value in a majority of cases in both groups (Table 1). The association of platybasia, occipitalization of the atlas, and fusion of in both groups suggests a common origin.[4,19,29,40,45] The analysis of radiological and clinical features suggests that the symptoms and signs in Group I were a result of brainstem compression by the odontoid process, whereas in Group II they were directly related to the crowding of neural structures at the foramen magnum (Table 1). Although the dimensions of the foramen magnum were large and sometimes were even larger than normally found, the volume of its contents and, probably, the longstanding "pulsatile" compression of structures at the foramen magnum resulted in neurological symptoms.[49] Surgical Intervention Clinical and radiological improvement following traction was only obvious in Group I. This suggests that traction assisted in pulling the odontoid process away from the brainstem. This feature also indicates the relative vertical instability of the craniovertebral region in Group I and the stability of the craniovertebral joints in Group II. The surgical treatment of basilar invagination in the presence of Chiari malformation has not been clearly outlined and is confused by the fact that some authors currently recommend anterior surgery, even for this group of patients.[3,7,23,30,41] From the analysis of results shown in Table 4, it appears that patients in Group II benefited from foramen magnum decompression. The procedure resulted in significant amelioration of symptoms and at least an arrest in the progression of the disability. None of the patients in this group had delayed worsening of their neurological condition following a foramen magnum decompression. The suboccipital bone, posterior rim of the foramen magnum, and dura overlying the herniated cerebellar tissue were thin in a significant number of these cases.[14] This was probably related to chronic pressure changes secondary to reduced posterior fossa volume. Dural decompression was performed in the earlier phase of the series. In the later phase, Group II patients were only treated with bone decompression of the foramen magnum and the adjoining suboccipital bone, irrespective of the state of the dura. This policy was based on the understanding that reduction in the volume of the posterior cranial fossa, secondary to abnormal development of bones anterior to the neuraxis, was the primary pathological condition in these cases.[15,26,33,35] The clinical and radiological results in patients who underwent the various treatment modalities were not different, and satisfactory outcome was noted uniformly. Although this experience is limited, we can infer from the results that bone decompression of the foramen magnum alone may be sufficient, even in the presence of syringomyelia.[2,12,21,24,25] Marked clinical worsening was observed in four of 10 Group I patients in whom only a posterior

Unauthenticated | Downloaded 09/27/21 12:44 PM UTC decompression was performed and in three of eight patients in whom a posterior decompression was performed prior to transoral surgery.[9] On the other hand, transoral decompression was an effective and gratifying surgical procedure in 64 (93%) of 69 of these patients. The clinical worsening following transoral surgery in Group II (Table 4) was related to a markedly difficult surgical procedure. This was the result of the high position of the odontoid process and the inability to pull it caudally by cervical traction. Additional removal of the clivus appears to be necessary to achieve complete obliteration of the anterior indentation of the brainstem in these cases. In the earlier portion of this series, transoral bone decompression was performed in 21 Group II patients. Later such a procedure was not preferred because our impression is that the decompressive effect on the neural structures of the posterior fossa and at the level of the foramen magnum is satisfactory following a posterior decompression. The study of pathological characteristics and the analysis of results suggests that anterior transoral decompressive surgery is relevant in Group I and posterior foramen magnum decompression is appropriate in Group II. The necessity for opening the dura after bone decompression of the foramen magnum in Group II needs to be evaluated on the basis of a larger study. Role of Fixation The role of posterior craniovertebral fixation following transoral surgery in patients with basilar invagination has remained controversial.[7,11,20,30] It was observed that the craniovertebral anomaly associated with basilar invagination is of a relatively fixed variety and simultaneous dorsal fixation following a transoral decompression is not mandatory in either group. In Group I, younger patients needed fixation more frequently than older patients.[30] It appears that in Group I, fixation is required but can safely be staged, whereas in Group II it can be avoided. Acknowledgments The authors acknowledge with gratitude the help of Dr. Ravi Ramakant, Head, Department of Radiology, King Edward Memorial Hospital and Seth Gordhandas Sunderdas Medical College, Bombay, India; Dr. Vijay Sheel Kumar, Consultant Neurosurgeon, Apollo Hospital, Delhi, India; and Dr. Naina Goel in the preparation of the manuscript. Dr. Sunil K. Pandya was our principal source of encouragement.

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Manuscript received July 5, 1997. Accepted in final form January 15, 1998. Address reprint requests to: Atul Goel, M.CH.H, Department of Neurosurgery, King Edward Memorial Hospital and Seth Gordhandas Sunderdas Medical College, Parel, Mumbai 400 012, India.

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