Surgical treatment of ventral and ventrolateral intradural extramedullary tumors of craniovertebral and upper-cervical localization

Abstract

Introduction:

Surgical treatment of extramedullary craniovertebral and upper-cervical tumors differs essentially, depending on the peculiarities of their localization.

Materials and methods:

In the Spinal department of the Institute of Neurosurgery during the period from 2000 to 2010 years, 96 patients with ventral and ventrolateral intradural extramedullary craniovertebral tumors and tumors of upper-cervical localization were examined and operated. The patients were distributed as follows: tumors of the craniovertebral localization – neoplasms spreading in rostral direction up to the boundary of the lower third of the clivus, and in caudal direction up to the upper edge body of the axis (C0 – C1): 12patients; tumors at the C1 – C2 level: 28 patients and at 1 – C2 – C3 level: 56 patients. The tumors were also divided as: ventral – 60 patients and ventrolateral – 36 patients.

Conclusion:

Therefore, the adequate choice of a surgical approach firstly depends on the localization of the tumor, its size and the extent to which it has spread. Far-lateral and posterolateral approaches in most cases are the most optimum and the least traumatic in cases of extramedullary ventrolateral tumors of craniovertebral and upper cervical localization. The extreme lateral approach is advisable in cases of large sized ventral craniovertebral tumors.

Introduction

Surgical treatment of extramedullary craniovertebral and upper-cervical tumors differs essentially, depending on the peculiarities of their localization. Surgical removal of the tumors located on the dorsal or dorsolateral surface of the spinal cord is usually performed by posterior midline approach and does not lead to any special disagreement [3], whereas in cases of intradural extramedullary tumors, causing compression of ventrolateral or ventral surface of the spinal cord, surgical treatment becomes much more complicated. In these cases, the choice of surgical approach must depend on tumor localization, level and provide optimum visual control of the tumor, spinal cord, spinal roots and nerves with minimum displacement of spinal cord during surgical manipulations [6].

Materials and Methods

In the Spinal department of the Institute of Neurosurgery during the period from 2000 to 2010 years, 96 patients with ventral and ventrolateral intradural extramedullary craniovertebral tumors and tumors of upper-cervical localization were examined and operated. The patients’ age varied from 30 to 80 years.

According to the level of tumor localization, the patients were distributed as follows: tumors of the craniovertebral localization – neoplasms spreading in rostral direction up to the boundary of the lower third of the clivus, and in caudal direction up to the upper edge body of the axis (C0 – C1) :12 patients; tumors at the C1 – C2 level: 28 patients and at the 1 – C2 – C3 level: 56 patients. The tumors were divided into: ventral – 60; ventrolateral – 36 (Table 1). According to the histology, the tumors were distributed as follows: neurinomas - in 36 patients; meningiomas – in 48 patients; neurofibromas – in 12 patients (Table 2).

Table 1.

Distribution of ventral and ventrolateral tumors depending on the level of localization.

Table 2.

Histology of types of tumors

The tumor's location and size, the degree of spinal cord compression and displacement were determined according to the MRI and CT data. For quantitative estimation of the degree of spinal cord displacement caused by the tumor, we used the scheme of cross-section division of the spinal canal (for example, at C1 level) and its content into 16 sectors, by which the positions of spinal cord in normal state and in case of its displacement by the tumor were estimated (Figure 1). The size of the area cross-section of the spinal cord at C1 level (based on MRT axial sections) is on the average 123 mm²(variation from 84 mm²to 146 mm²); the size of the area cross-section of the dural sac - 321 mm²(variation from 290 mm²to 350 mm²) respectively. The area was calculated by means of the formula of ellipsoid area S =πab, where a, b are small and big radius of the ellipsoid (half of the saggital and frontal dimensions of the spinal cord and dural sac). The ratio of the square spinal cord and dural sac cross-section areas on average is 1 to 3 (1/3). One third is occupied by spinal cord and two-thirds by subarachnoid spaces, filled with liquor. At levels C2 and C3 ratios are similar except for the area of subarachnoid spaces which are less by 20-30 %. Hence, to judge about the degree of spinal cord compression and displacement on the basis of MRI data, we divided our observations into 3 groups: I – tumors with the cross-section area (at level C1) less than the cross-section of the spinal cord – (>1(tumor)+1(spinal cord)/3(dural sac)) – compression is insignificant, practically there is no spinal cord displacement; II – tumors with the cross-section area equal to that of the spinal cord – 1+1/3, compression of the spinal cord is moderate, the spinal cord is displaced by one square, according to the scheme on Figure 1; III – tumors with the area equal to two cross-sections of the spinal cord – (2+1/3), compression is pronounced, liquor spaces on the level of the tumor are absent, the spinal cord is displaced by 2 squares (Figure 1, Table 3).

Figure 1.

Scheme of spinal cord intradural spaces location. A – anterior, AL – anterolateral, LA – lateral anterior, LP – lateral posterior, SA – spinal cord anterior, SP - spinal cord posterior, P – posterior, PL – posterolateral.

Table 3.

Degrees of displacement and compression of spinal cord by the tumor according to MRI data.

Results

Surgical approaches, used on the craniovertebral and upper-cervical levels are divided into: posterior, posterolateral, far-lateral and extreme lateral ones.

The choice of an approach depended on the tumor localization and its size estimated by the scheme as we described above (Figure 1). The posterolateral approach was used to remove tumors of type I, if they occupied sectors A on one side or sectors LA, LP, displaced the spinal cord to sectors LA, LP, PL of the opposite side, occupying sector SA. We used this approach in ‘16 patients (Table 4).

Table 4.

Operative approaches used for ventral and ventrolateral craniovertebral and upper cervical tumors.

The far lateral approach was used in cases when a tumor with a size of types II – III, occupied sectors A on one or two sides, sector SA on one side or sector LA, displacing the spinal cord to the opposite side to sectors P, PL, LP of the opposite side (Figure 2,3). We used this approach in 64 patients (Table 4).

Figure 2.

MRI of III-type ventrolateral tumor at C1 – C2 level.

Figure 3.

Schemes of spinal cord compression and displacement according to axial MRI sections of the tumor at C1 – C2 level. A – Axial MRI at C1 level (spinal cord displaced to LP, PL, P sectors), B – Axial MRI at C2 level (spinal cord displaced to LP, SP sectors).

The extreme-lateral approach was used with the tumors of II – III type size in cases when they occupied sectors A on two sides, in addition, AL, and especially sectors A and SA on two sides, displacing the spinal cord exclusively backwards into sectors P. We used this approach in 16 patients (Table 4).

The level of the tumor's location and extent also played its role in the choice of optimum approach. The extreme-lateral approach was used with the tumor location on levels C0 – C1, C1 – C2. The far-lateral approach was used on all levels C0 – C1, C1 – C2, C2 – C3. The posterolateral approach was used on levels C1 – C2, C2 – C3.

Posterolateral surgical approach included C2 – C3 hemilaminectomy, C2 – C3 medial facetectomy. The vertebral artery and its venous plexus were not allocated and displaced.

With the far lateral approach the “park bench” position was used. A horseshoe-shaped incision began along the midline, 7-8 cm down from the occipital protuberance and went upwards, turning laterally above the occipital protuberance, continued above the upper nuchal line towards the mastoid process (Figure 4). Along the posterior edge of the mastoid, the incision turned downwards and ended 3 cm below the top of the mastoid. We separated muscles together with the skin in a single layer from the occipital bone, spinous process and arches C1 – C4. The flap was turned downwards. The cardinal moment was the identification of the atlas transverse process. The sub-occipital triangle was opened by careful separation of upper and lower oblique muscles from the atlas transverse process. In the depth of the triangle the venous plexus, surrounding the vertebral artery and the artery itself in its position behind the atlas-occipital joint and the upper edge of the C1 arch were found out. The artery was detached by subperiosteal dissection together with the venous plexus. This minimized bleeding. If there was an intracranial spread of the tumor, first we resected the edge of the occipital foramen on one side and widened the zone of resection up to the edge of the sigmoid sinus. Then C1 – C2 hemilaminectomy was performed, and if necessary, C3 was also included. The C1 arch was removed up to the C1 transverse foramen, which was cut open (Figure 5). If it was necessary, the vertebral artery was transposed medially and caudally (medial transposition of the artery), and the remains of the C1 arch were removed up to the C1 lateral mass. Usually, with this approach the condyles of the occipital bone and the C1 lateral masses were uncovered along the back surface, but were not resected. This being done, the dura was incised like a hockey-stick (Figure 6). The spinal cord and lower brain stem, as a rule, transposed dorsally and laterally to the opposite side from the tumor. Initially, we did not try to separate the vessels and nerves, passing along the posterior surface of the tumor. The operative microscope with 8 – 16 magnification was used. First, the area of the posterior surface of the tumor without nerves and vessels was identified. In this area, the tumor was sectioned and the central part was removed stage by stage (by cutting into pieces or by means of cavitron aspirator). Thus, after the tumor debulking, the volume of the tumor reduced and adjacent nerves and vessels were allocated and displaced from the tumor surface. Without spinal cord and lower brain stem traction, the lateral part of the tumor, adjacent to the dura mater, was removed. Then the areas of the tumor, adjacent to the spinal cord and the lover brain stem, were removed (Figure 7).

Figure 4.

Line of skin incision, far-lateral approach.

Figure 5.

The approach stage after performing of osseous resections with far lateral approach. D – dura mater, VA – vertebral artery. The zone of osseous resection is outlined by the arrows.

Figure 6.

The approach stage after dura mater incission. PICA - posterior inferior cerebellar artery, T – the tumor, CN IX – XI the group of lower cranial nerves, C1 – C1 roots, C2 – C2 roots.

Figure 7.

The stage after total removal of the tumor. PICA – posterior inferior cerebellar artery, VD – ventral dura mater, CN IX – XI – the group of lower cranial nerves, C1 – C1 roots, C2 – C2 roots.

In cases of extreme lateral approach the patient laid on the operation table on his side. The incision began 6 cm lower from the top of the mastoid process, continued upwards along the front edge of the sternocleidomastoid muscle, and on the level of the external auditory meatus turned backwards. Sternocleidomastoid muscle was sectioned and drawn forward. The approach was directed strictly to the C1 – C3 side surface and the condyles of the occipital bone. M.m. splenius capitis, semispinalis capitis and longissimus capitis were transposed backwards, the sub-occipital triangle was uncovered. From the front, the jugular vein limited the operative approach. Muscles attached to the C1 transverse process were sectioned. The vertebral artery and vein were uncovered in the groove on the upper surface of the C1 arch close to the area where it goes into the foramen of the C1 transverse process. The C1 – C2 – C3 (depending on tumor localization) hemilaminectomy was performed, the C1 transverse process was resected and its foramen was uncovered. The vertebral artery was transposed backwards. Further, by means of a drill, partial resection of the occipital condyle and of the C1 lateral mass, and, if necessary, medial facetectomy of the C2 – C3 was performed. We have never entirely resected the lateral mass of the C1 vertebra and the occipital condyle. If it was necessary, the lower sectors of the occipital bone up to the posterior edge of the sigmoid sinus were resected. The dura mater was incised linearly. The dentoids were sectioned. The tumor was removed the same way as it was with the far lateral approach. The extreme-lateral approach provided better visualization of the ventral surface of the spinal cord, the lower brain stem, vertebral arteries. Sometimes we converted the far lateral approach into the extreme-lateral one, if during operation it became clear, that the vertebral artery was involved into the meningioma.

With the neurinomas of the C1 root, especially with extravertebral extension, we used the far lateral approach. This approach gave enough space to reach the extravertebral part of the tumor and to visualize the vertebral artery. Removal of the neurinoma began from its medial part and continued towards its lateral part. At first the tumor was debulked and the vertebral artery was allocated, then, the tumor was separated from the dural sac, which was left intact for its further stitching and preventing liquorrhea. If it was impossible to stitch the dural sac, the duroplasty was performed. In case of C2-C3 neurinomas, the dorsolateral approach with hemilaminectomy of C2 and medial facetectomy was done.

In all the 24 patients, the tumors were removed totally (Figures 7, 8, 9, 10). The results of surgical intervention were affected by: the size and the consistency of the tumor, the degree of compression and the direction of spinal cord displacement, the spread of the tumor along the axis (C0, C1, C2, C3), by ventral or ventrolateral location of the tumor and the adequacy of surgical approach. During the surgical intervention in 21 patients, no technical complication and no additional damage to the nerves and vascular structures was observed. In two patients, the tumor removal was complicated because of inadequacy of chosen approach (in one patient instead of the posterolateral the far lateral approach should have been chosen; in one patient excessive traction and partial lesion of the nerves of caudal group were observed). In one patient due to the dense tumor consistency, its separation from the lower brain stem and the spinal cord was traumatic.

Figure 8.

MRI after tumor removal.

Figure 9.

Spiral CT after the tumor removal, the zone of osseous resections is visualized. A – CT plane at C1 level, B – CT plane at C2 level.

Figure 10.

3D reconstruction of the spiral CT (visible osseous resection zone). The zone of C1 hemilaminectomy extended up to the lateral mass of the C1. Arrows indicate lateral mass and foramen in transverse process C1.

For the estimation of the results of surgical treatment, the degree of clinical and functional recovery of the patients was taken into account. Several factors influenced the results of surgical treatment: pre-operative neurological disorders, patients’ age, the degree of compression of spinal cord, the direction of spinal cord displacement (exceptionally dorsal, lateral or dorsolateral), the adequacy of surgical approach and the traumatic effects on the tumor removal, connected with it. There were no deaths in our series. We marked out good, satisfactory and unsatisfactory results. In the patients with “good result” (63% in our study) pain syndrome vanished, capacity for work restored, neurological disturbances regressed (according to Karnofsky performance status, 80 – 100 points) (Table 5). The patients from the “satisfactory result” group (25% in our study) usually had pronounced neurological disturbances before operation due to large sized tumors. In these patients after surgical intervention, capacity for work restored partially, although neurological deficits from light to oderate paresis, sensory disturbances, bladder dysfunctions remained (Karnofsky performance status 60-80). In those patients, who were hospitalized in grave condition and in late terms, “unsatisfactory result” was observed (12% in our study) (Table 5). In these patients, as a rule, surgical intervention resulted in partial neurological symptoms resolution, however, gross neurological disturbances remained (Karnofsky performance status less than 60 points).

Table 5.

The results of surgical treatment depending on the level of tumor localization.

On the whole, with the tumors at C0 – C1 level the results of treatment were worse in comparison with that at C1 – C2 and C3 levels. It was because at C0 – C1 level as a rule, larger tumors were diagnosed.

With ventrally located tumors, the clinical results were worse as compared to that of ventrolateral tumors (Table 6).

Table 6.

The results of surgical treatment depending on the tumor relation to the spinal cord.

Positive results were observed more often with the use of posterolateral and far lateral approaches (Table 7). However, it should be noted that we applied these approaches to ventrolateral tumors, which technically can be removed easily as compared to ventral tumors.

Table 7.

The results of surgical treatment depending on surgical approaches.

Discussion

The compression of spinal cord, roots and vertebral artery on the upper-cervical level presents a complicated problem. Previously it was associated with the necessity of considerable transposition of spinal cord during the operation; very often tumors were not radically removed owing to inadequate surgical approaches, which caused high mortality [4,9].

Among the tumors of craniovertebral and upper cervical localization, meningiomas are prevalent (75%). Their ratio to neurinomas is 3:1. At this level dermoids, teratomas, lipomas, paragangliomas, intradural extraosseous chordomas are rare [4]. In our study, only meningiomas, schwannomas, neurofibromas were found. Spinal neurinomas make up approximately 30% of all primary spinal cord tumors [11]. Hori and others reported that among 45 patients, in 71.1% cases neurinomas grow from sensory roots, in 17.8% - from motor roots and in 11.1% - from both the roots [5,8]. As regards the dura, in 74% cases neurinomas had intradural localization, 23% were intra- extradural and 15% were extradural [7]. George B. and Lot G. reported that neurinomas of the C1 and C2 roots make up 5.3% of neurinomas of all levels of spinal cord and 18% of all neurinomas of cervical spine [3]. The age of the patients with meningiomas varies from 31 to 73, with neurofibromas – from 12 to 57 years. The tumors of craniovertebral and upper cervical localization grow slowly and reach a large size, before diagnosis is made [2].

For the surgical treatment of tumors of craniovertebral and upper cervical region, numerous approaches have been described. They may be conditionally divided into posterior, posterolateral, far lateral and extreme lateral, transcondylar approaches [6]. The anterior transoral approach at this level is fraught with great number of complications such as vertebral artery damage (in case of too lateral allocation and a wide bone window), difficulties in dura suturing, high frequency of liquorrhea and meningitis. The anterolateral approach at C0 – C3 level requires massive osseous resection, considerable transposition of the vertebral artery qith an acute angle of surgical operation. That is why anterior and anterolateral approaches at C0 – C3 level are more acceptable for the removal of extradural tumors of osseous structures and in cases of traumatic lesions [6,13,19].

Previous works prove extremely bad results of the posterior approaches applied to ventral and ventrolateral tumors. Thus, according to Love et al., from 74 operated patients, 34 have died [10]. According to Yasargil M.G. and co-authors, in 1980, the death rate was 13.2%, good results were noted in 69.3%, satisfactory results were seen in 7.9% and bad results in 9.6% of patients [20].

In an attempt to reduce the brain stem and spinal cord trauma during the operation and to improve the vision of the ventrolateral surface of spinal cord and medulla, the lateral approaches were offered. Thus, in 1986 Heros R.C. offered the far lateral approach, which allowed reaching the craniovertebral and upper cervical region laterally and achieving better visibility of the ventrolateral surface of spinal cord and lower brain stem. George B. and co-authors in 1988 used medial transposition of vertebral artery. Transposition of the vertebral artery promoted safe removal of occipital condyles and C1 lateral masses with a drill and provided improvement of field of vision of the lover brain stem and spinal cord ventral surface. Sen C.N., Sekhar L.N. in 1990 offered the transcondylar extreme lateral approach, which allowed to achieve sufficient ventral surface visibility of the medulla and the upper spinal cord (including the ventral surface of the opposite side), to make surgical manipulations aimed at tumor separation much easier, to lessen the traction of nervous structures. These offers have been lately supplemented with several modifications of extreme lateral and far lateral approaches [6,15,18,19].

At present, in common opinion of many authors, the choice of approach should depend on such factors as tumor's location, its histological structure, tumor density, relation of the tumor to the dura and nervous structures and the aim of the surgery (biopsy, decompression or radical removal) [17,18].

The main surgical complications in course of removal of such tumors are connected with trauma of the lower brain stem and the upper spinal cord including disturbances in their blood supply. It generally occurs due to insufficiency of the surgical field of view, firm tumor's consistency or its ossification. Cases of complications connected with the vertebral artery involvement into the tumor and the development of vasospasm after tumor removal are rare. The lesion of the IX-XI nerves may cause intraoperative bradycardia and low arterial pressure, and in the postoperative period – paresis of the vocal cords, cough and deglutition reflexes disorder. Usually these disturbances gradually disappear [13,16,18].

Owing to the introduction of the extreme lateral approaches, it was possible to improve the results of operative treatment essentially. Thus, according to Welling B. and co-authors, among 27 patients with the tumors of craniovertebral localization (18 meningiomas, 3 chordomas, 3 chondrosarcomas, 1 schwannoma, 1 paraganglioma, 1 neuroepithelial cyst), in which the authors applied exclusively extreme lateral transcondylar approach, there were no fatal cases. Transient paresis of vocal cords was noted in 4 patients, in 1 patient – deglutition reflex disorder was seen, in 1 patient- paresis of the hypoglossal nerve was seen and in 3 patients liquorrhea was noted [18]. According to Parlato C. (2003), among 15 patients with craniovertebral and upper cervical tumors (7 meningiomas, 3 epidermoids, 3 C1 neurinomas and 2 neurinomas of the lower IX-XI nerves), in 11 patients the extreme lateral transcondylar approach with partial resection of condyles was used and in 4 patients, the far lateral approach was used. Tumors were removed totally in 11 cases (73.3%) and subtotally – in 4 cases (26.7%). The occipitocervical fusion was not perofrmed [11].

Rhoton AL. prefers the application of extreme lateral approach in cases of large craniovertebral meningiomas [11]. Lot G., George B. reported that the posterolateral approach is preferred in C1 and C2 neurinomas (Lot G., George B.).With neurinomas of ventral localization below C3 level, the anterolateral approach should be preferred [6].

At present, with the craniovertebral tumors, comparatively simple approaches are applied as well as the most complicated ones, requiring massive osseous resections, transposition of vessels, nerves, subsequent careful closure of dura mater [8]. Some authors note that such methods as the extreme lateral transcondylar one with extensive or total removal of condyles are too complicated and by themselves entail a danger of after-effects in the form of bleeding from the vertebral veins, lesions of vertebral arteries, traumatizing of the hypoglossal nerve, destabilization of the craniovertebral junction, ischemia of brain stem. The authors believe that it is necessary to choose the least traumatic approach and in cases where it is possible, to confine to more sparing far lateral approach [1,16].

Boulton M.R., Cusimano reported that with craniovertebral tumors of large size, the removal is more favorable than with small ones. It is explained by the fact that after debulking of large tumours, more space is available for surgical manipulation during the detachment of the tumor capsule remainder from brain stem and dura with minimal displacement of spinal cord, nerves and vessels, as compared to smaller tumors [1,16]. According to our data, it is corroborated only in cases with tumors of soft consistency, the volume of which decreases after the removal of their central part.

Conclusion

Therefore, the adequate choice of a surgical approach first depends on the localization of the tumor, its size and the extent to which it has spread. Far-lateral and posterolateral approaches in most cases are the most optimum and the least traumatic in cases of extramedullary ventrolateral tumors of craniovertebral and upper cervical localization.

The extreme lateral approach is advisable in cases of large sized ventral craniovertebral tumors.

The factors, increasing the risk of unsatisfactory functional outcome of a surgical intervention are dense consistency or ossification of the tumor, its large size and carrying out the operation in the presence of severe neurological disorders.