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연세대학교 의과대학 강남세브란스병원 신경외과학교실 조윤성, 홍창기

Department of Neurosurgery, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea

Yun seong Cho, Chang-Ki Hong

대후두공과 상위경추신경 전방으로의 극외측경과접근법: 수술술기와 36례의 임상분석

J Korean Skull Base Society 14권 1호 : 20~27, 2019

종설1 종설2 원저1

증례1 원저2

증례2 증례3 증례4

Background: Because diseases that are situated anterior to the foramen magnum and the upper cervical spinal canal permit limited access, they are considered some of the most difficult intracranial lesions to surgically treat. The far-lateral transcondylar approach provides such a route. The author has reviewed the technique as well as the surgical results here.

Materials and Methods: During a 16-year period 36 patients underwent surgery in which far-lateral approach were performed. This approach was utilized in patients with aneurysm, schwannoma, meningioma, and chordoma affecting the cervicomedullary junction. Medical records, including imaging studies, descriptions of microsurgical findings were reviewed.

Results: Total tumor resection was achieved in 25 patients, and a subtotal resection was performed in the other 9 patients. In the 2 patients with vertebral artery-posterior inferior cerebellar artery (PICA) aneurysms, 1 underwent clipping, the other underwent trapping and occipital artery-PICA bypass procedure. Postoperative complications included CSF leakage in 4 and temporary lower cranial nerve dysfunction in 10 patients. There was no significant postoperative complication in the remainder of the patients.

Conclusions: Successful surgical management depends on precise understanding of their unique microsurgical anatomy. Sufficient exposure, minimal brain retraction, and preservation of the lower cranial nerves are necessary for a safe surgery.

The far-lateral transcondylar approach to the anterior foramen magnum and upper cervical spinal canal: surgical techniques

and clinical analysis of 36 consecutive patients

논문 접수일 : 2019년 4월 21일 논문 완료일 : 2019년 5월 23일

주소 : Department of Neurosurgery, Gangnam Severance Hospital, Yonsei University College of Medicine, 211 Eonju-ro, Gangnam-gu, Seoul 06273, Korea Tel : +82-2-2019-3391

Fax : +82-2-3461-9229 E-mail : yedamin@yuhs.ac

Chang-Ki Hong

교신저자

far-lateral approach, anterior foramen magnum, craniocervical junction Key Words

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▒ Introduction

Use of the far-lateral transcondylar approach is necessary for resecting a lesion anterior or lateral to the brain stem while minimizing or avoiding brain traction.[8] This technique involves partial removal of the occipital condyle in addition to the conventional lateral suboccipital approach to gain access to the lesion. A lesion located anterior to the upper cervical spinal cord or the medulla requires traction through transposition of the vertebral artery.[8-10] To perform this approach, the occipital condyle and superior articular facet must be partially removed. This approach is essential since it is often the commonly used surgical option for accessing lesions occurring anterior to the foramen magnum. This study reports the surgical methods and outcomes based on the authors’ experience.

▒ Materials and Methods

A total of 36 patients (16 men, 20 women; mean age, 49.3 years; age range, 23-72 years) underwent surgery between March 2002 and September 2018 using the far- lateral transcondylar approach to access lesions that were anterior and lateral to the foramen magnum. This retrospective study involved review of their clinical records and radiological data. Of the 36 patients, 34 had tumor- like lesions and the other two had cerebral aneurysms. The

medial one-third of the occipital condyle was removed in cases of tumor-like lesions, while a smaller amount was removed in the cases of aneurysm. A C1 (atlas) laminectomy was performed only when necessary. Transpositon of vertebral artery is performed to reveal atlanto-occipital joint and occipital condyle only in cases of tumor. None of the cases required post-operative occipitocervical fusion.

The mean follow-up period was 53 months (range, 31-251 months).

▒ Operative Technique

1. Surgical position

The patient’s position during surgery is highly important.

Some positions used in this surgery include the three- quarter oblique position and modified park bench position.

The patient’s neck must be extended to ensure that the surgeon’s hands do not get interrupted by the patient’s shoulders and the movements of an operating microscope are not restrained (Fig. 1). However, excessive cervical extension can increase airway pressure, cause venous congestion in the cerebellum, and even create a highly dangerous situation as the lesion compresses the cervical nerve and brain stem during surgery.[6,7] Therefore, the patient must be put in the same surgical position ahead of the procedure and observed for 20 minutes for any changes in patient’s symptoms or neurological manifestations.

Fig. 1

A B C

Picture depicts the patient in the 3 quarter position. It is much easier to place the patient`s neck flexion with the turned away from the surgeon to obtain appropriate sight and to manipulate microscope.

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2. Surgical procedures

The majority of occipital or cervical skin incision and muscle dissction do not differ from conventional far- lateral approach; however, in the far-lateral transcondylar approach, the occipital muscles have a crucial role as an indicator. Accurate knowledge of their anatomic relationship with the occipital condyle, foramen magnum, hypoglossal canal, jugular tubercle, jugular process, mastoid canal, and facial canal is also essential. To ensure easy identification of

the important nerves and blood vessels, the occipitocervical muscles should be verified and dissected along their plain.

A skin incision reveals the superficial muscles. For confirmation, each muscle has to be dissected as layer by layer fashion; however, from practical point of view, detaching the muscles superior to the suboccipital triangle in one layer may save time. The first layer of muscles exposed through the scalp incision includes the sternocleidomastoid and trapezius; separating the trapezius and splenius capitis

Table 1. A summary of patients’ characteristics Case

no. Sex Age Disease Symptoms and sign Location or origin VA

transposition Complication

1 F 65 Meningioma Neck pain Spinal cord, C1 -

2 F 51 Meningioma Headache, neck pain Cervicomedullary junction +

3 F 59 Meningioma Headache Anterior foramen magnum + Lower CN palsy

4 F 65 Schwannoma Headache -

5 F 44 Meningioma Dysarthria Anterior foramen magnum +

6 F 62 Meningioma Headache Jugular foramen + CSF leakage

7 M 23 Meningioma Dizziness, tinnitus Jugular foramen +

8 F 61 Schwannoma Dizziness +

9 M 50 Meningioma Post neck pain, voice change Clivus +

10 M 56 Schwannoma Headache Petroclival +

11 F 39 Chondrosarcoma Dizziness Petroclival + CSF leakage

12 F 71 Meningioma Headache Petroclival +

13 M 40 Meningioma Gait disturbance Anterior foramen magnum +

14 F 61 Meningioma Facial numbness Anterior foramen magnum +

15 M 44 Chordoma Dysphagia Clivus + Lower CN palsy

16 M 46 Chordoma Hemiparesis Clivus + CSF leakage

17 F 54 Meningioma Quadriparesis, dysphagia Spinal cord, C1 -

18 M 52 PICA aneurysm Consciousness change Cerebello-medullary cistern - 19 M 26 PICA aneurysm Incidental finding Cerebello-medullary cistern -

20 F 67 Meningioma Incidental finding Anterior foramen magnum + Lower CN palsy

21 F 39 Schwannoma Hearing disturbance, dizziness - CSF leakage

22 F 72 Meningioma Headache Anterior foramen magnum + Lower CN palsy

23 F 34 Chordoma Neck pain Clivus +

24 M 37 Chordoma Dysphagia Clivus +

25 F 39 Meningioma Dizziness Anterior foramen magnum +

26 F 54 Meningioma Incidental finding Anterior foramen magnum - Lower CN palsy

27 M 38 Meningioma Headache Cervicomedullary junction +

28 M 33 Schwannoma Neck pain + Lower CN palsy

29 M 62 Meningioma Cognitive dysfunction Anterior foramen magnum + Lower CN palsy

30 F 65 Meningioma Incidental finding Anterior foramen magnum +

31 M 26 Chordoma Dysphagia Clivus + Lower CN palsy

32 M 44 Chordoma Voice change Clivus +

33 F 49 Schwannoma Hearing impairment +

34 F 49 Meningioma Sensory change, hemiparesis Cervicomedullary junction +

35 M 63 Meningioma Incidental finding Anterior foramen magnum + Lower CN palsy

36 M 58 Meningioma Dizziness Anterior foramen magnum + Lower CN palsy

VA: vertebral artery, F: female, M: male, PICA: posterior inferior cerebellar artery, CN: cranial nerve.

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reveals the longissimus capitis medialward (Fig. 2A).

Detaching the longissimus capitis reveals the semispinalis capitis, superior oblique muscle, inferior oblique muscle, and C1 transverse process. Reflecting the semispinalis capitis medially exposes the suboccipital triangle, which consists of the rectus capitis posterior major, superior oblique, and inferior oblique muscles (Fig. 2B). This triangle is covered by a tissue consisting of a fat and fiber mixture;

its bottom comprises the atlanto-occipital membrane and C1 lamina. The vertebral artery and C1 nerve travel inside the suboccipital triangle. To open this triangle, the superior oblique muscle has to be reflected laterally, the rectus capitis posterior major reflected downward and the inferior oblique muscle reflected medially (Fig. 2C,D,E).

Once the suboccipital triangle is open, the venous plexus would appear: it envelops the vertebral artery, stretching along the upper C1 lamina behind the atlanto-occipital joint (Fig. 2F).[3,8] Reflecting the superior oblique muscle

exposes the rectus capitis lateralis, the indicator used to identify the jugular foramen. The jugular process is a part of the occipital bone located lateral to the posterior half of the occipital condyle; it is a crucial structure in the identification of the location of the jugular foramen given that the rectus capitis lateralis is attached to the jugular process located at the posterior tip of the jugular foramen.

The vertebral artery, located at the bottom of the suboccipital triangle, is covered by the semispinalis capitis on the superior side of the triangle. The muscular branches and posterior meningeal arteries arise from the third segment of vertebral artery located between the C1 transverse process and the entrance to the dura mater. The arteries toward the muscles originate from the transverse foramen, spirally envelop the C1 lateral mass, reach the deep muscles, and anastomose with the occipital and deep cervical arteries. These arteries that supply the deep muscles should be cut to transpose the vertebral artery.

Fig. 2 A

E

B

F

C D

Intraoperative photograph. (A) Oblique skin incision. (B) Exposure of the rectus capitis posterior major muscle (RMC), superior oblique muscle (SO), and inferior oblique muscle (IO) forming suboccipital triangle can be obtained. (C) SO is reflected laterally.

(D) RMC is reflected inferiorly. (E) IO is reflected medially. (F) After suboccipital triangle is opened, vertebral artery (VA) and atlas (C1) are exposed.

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Inferomedial transposition of the vertebral artery creates a wider space anterior to the brain stem, thus allowing for access to the lesion without disturbing the lower cranial nerve and enabling safer tumor removal. However, when the upper cervical cord was occupied with the tumor, a sufficient space would be obtained as the tumor being removed, even without traction of the vertebral artery. The posterior meningeal artery originates from the posterior vertebral artery, passes posterior to the lateral mass or superior to the C1 lamina, and penetrates the dura mater

at the foramen magnum region. The posterior meningeal artery should be distinguised from other arteries toward the muscles since it sometimes originates from the posterior spinal artery or, in very rare cases, from the extradural vertebral artery; it also has to be kept in mind during hemostasis in the venous plexus.[3,8]

To transpose the vertebral artery after the occipital craniotomy, the occipital condyle should be identified. And when performing a C1 hemilaminectomy, the transverse foramen also should be opened. The C1 lamina is removed to expose the suboccipital triangle. The vertebral artery is transposed from the C1 transverse foramen to where it penetrates the dura mater. Removal of the posterior part of the transverse foramen and inferomedial transposition of the vertebral artery reveal the atlanto-occipital joint and occipital condyle. The occipital condyle has a downward protrusion along the anterolateral parts of the foramen magnum; the oval-shaped joint is located anteroposterior to the inferolateral side of the condyle. The articular surface of the occipital condyle sits downward and laterally and meets the C1 articular facet that looks upward and medially.

Removal of the hard cortical bone, which covers the occipital condyle, reveals cancellous bones. Drilling deeper from the posterior one-third of the occipital condyle leads one to the cortical bone of the hypoglossal canal. Drilling is continued even further inside to reveal the venous plexus, and the posterior one-third of the occipital condyle is removed to reach the exterior of the intracranial tip of the Fig. 3

Intraoperative photograph demonstrates extradural vertebral artery (VA) which has been transposed posterior and medially.

TF: transverse foramen.

Fig. 4

A B C D

Imaging studies in a 49-year-old woman who had a right hemiparesis and sensory change. Preoperative magnetic resonance image (MRI) shows enhancing mass located at anterior portion of foramen magnum. (A) Axial view and (B) sagittal view. Postoperative MRI confirms total removal of tumor. (C) Axial view and (D) sagittal view.

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hypoglossal nerve. The posterolateral facet of the occipital condyle can be removed without entering the hypoglossal canal that extends anteriorly and laterally.[2,4,8]

An incision into the dura mater is performed from behind the sigmoid sinus along the posterior of the vertebral artery to the upper cervical dura mater. Once the dura mater is opened, the intradural part of the vertebral artery is exposed. Where the vertebral artery penetrates the dura mater, the posterior spinal artery, dentate ligament, C1 nerve, and spinal accessory nerve are tied into a fibrous tunnel with the vertebral artery; careful management is needed not to damage these structures when transposing the vertebral artery.[5-7] Vertebral artery transposition allows tumor excision to be safer avoiding damaging crucial structures by creating a wider space inferior to the lower nerve root (Fig. 3). The dentate ligament is located between the vertebral artery and the C1 nerve to the anterior and the posterior spinal artery and spinal accessory nerve to the posterior; cutting this ligament enables greater exposure of the anterior portion of the cervical cord.[8,11,12].

▒ Results

1. Extent of pre-operative neurological symptoms

Table 1 summarizes the patients’ symptoms, tumor locations, and surgical complications. Headache and neck pain were the most common symptoms, followed by cranial

nerve palsy and movement disorders. The two aneurysm patients presented with subarachnoid hemorrhage.

2. Histology of the tumor and adopted surgical approach A total of 34 cases involved tumors, of which the most common type was meningioma (21 cases), followed by schwannoma (6 cases), chordoma (6 cases), and chondrosarcoma (1 case). Most of meningiomas were located anterior to the foramen magnum, with only two being anterior to the cervical spinal cord (Fig. 4). In two cases, the tumor occurred in the clivus and grew toward the cervical cord. Of the schwannoma cases, one had the tumor originating from the accessory nerve and the remaining five were from the vestibulocochlear nerve. The schwannoma developed from the vestibulocochlear nerve was very large and reached the anterolateral medulla; the far-lateral transcondylar approach was used to remove this tumor since the lateral suboccipital approach was deemed inadequate due to the tumor’s size (Fig. 5).

3. Aneurysm location and surgical method

Both aneurysm cases affected the posterior inferior cerebellar artery (PICA). One case was treated with direct aneurysmal clipping, while the other was treated with occipital artery anastomosis to the PICA, followed by trapping of PICA. In the aneurysm surgery, there was less difficulty in securing the visual field even with less

Table 2. Results of surgery in 34 patients who harbored various tumors

Type of lesion No. of patients Total removal Subtotal removal Follow-up period (months)

Meningioma 21 16 (76.2%) 5 (23.8%) 23.7

Schwannoma 6 5 (83.3%) 1 (16.7%) 14.8

Chordoma 6 4 (66.7%) 2 (33.3%) 32

Chondrosarcoma 1 1 (100.0%) 38

Table 3. Location and treatment of aneurysms in 2 patients who underwent surgery

Case no. Location and shape Treatment

1 VA-PICA, saccular Neck clipping

2 PICA, dissection Trapping with OA-PICA bypass

VA: vertebral artery, PICA: posterior inferior cerebellar artery, OA: occipital artery.

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removing the occipital condyle compared to the tumor removal.

4. Surgical outcomes and complications

All 34 tumor surgery required removal of the posterior one-third of the occipital condyle; of them, vertebral artery transposition was required in 29. The meningioma was totally removed in 16 of 21 cases; the schwannoma was totally removed in 5 of 6 cases; the chordoma was fully removed in 4 of 6 cases; and the chondrosarcoma was treated with subtotal resection (Table 2). Two meningioma and three schwannoma cases, in which the tumor was small and located lateral to the medulla, were treated without vertebral artery traction. Four patients experienced post- operative cerebrospinal fluid (CSF) leaks, of which three were treated with lumbar CSF drainage and the other with a lumboperitoneal shunt to resolve the CSF leakage. Seven of the meningioma and one of the schwannoma patients had dysphagia due to lower cranial nerve palsy, but all recovered after 6 months. The clival meningioma patients also experienced post-operative dysphagia; however, their swallowing functions were not severely impaired despite the incomplete recovery.

All of the cerebral aneurysms were on the anterior medullary segment of the PICA. Direct clipping of the aneurysm resulted in flow arrest of the PICA; fortunately, this did not lead to PICA territory infarction, nor caused

neurological change. The other case of cerebral aneurysm was treated with occipital artery to PICA bypass, followed by aneurysm trapping, and the flow of the PICA was preserved (Table 3).

▒ Discussion

A lesion in the junction from the foramen magnum or the brain stem to the spinal cord eludes sufficient exposure through conventional approaches. Typical examples include meningioma (anterior to the foramen magnum), schwannoma (affecting the upper cervical spinal cord), and chordoma (inferior to the clivus).[8] Past approaches to gain access to these lesions included anterior, such as the transoral and transcervical approaches, and posterior, such as the lateral suboccipital approach. However, anterior approaches cannot provide an adequate access to bilateral lesions; posterolateral approaches often preclude the resection of anterior lesions without traction of the brain stem or spinal cord. Recent years have seen attempts with many modified approaches, but all were involved in the inferior and lateral expansion of a suboccipital craniotomy and the inferomedial transposition of the vertebral artery to approach the lesions from the lateral side.[1,12]

The basic far-lateral transcondylar approach comprises the following three steps: first, muscles are splitted from the posterolateral side of the head and neck margin to Fig. 5

A B Imaging studies in a 49-year-old woman who had a

history of hearing disturbance and tinnitus. (A) Magnetic resonance image (MRI) shows dumbbell-shaped enhancing mass extending to jugular foramen. (B) The patient underwent surgery via far-lateral approach with partial drilling of the occipital condyle. Postoperative MRI confirms completely removed intracranial portion of the tumor and residual tumor with encasement of left cavernous internal carotid artery.

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expose the C1 transverse process and the suboccipital triangle; second, the vertebral artery has to be found in the suboccipital triangle superior to the C1 lamina and between the C1 and C2 (axis) transverse processes; and third, stage is performing a suboccipital craniotomy with a C1 hemilaminectomy.[8-10]

Far lateral transcondylar approach is performed in 34 patients with the tumor located in anterior and lateral to the foramen magnum in our institution. And total removal of tumor was achieved in 21 patients (77.8%). Kratimenos GP & Crockard HA, 1993 perfomed far lateral transcondylar approach in 15 patients with ventrally located tumors of the craniocervical junction, resulting in 12 total removals (80.0%).[6] And S. Balaji Pai et al. 2018 reported that total removal was achieved in 5 out of 6 neoplastic cases (83.3%).

[13] The result of total removal rate in out institution is in accordance with that of other institution’s report.

Furthermore, we provided informations about complications and changes in follow-up studies with this approach which were not in previous reports.

▒ Conclusion

With thorough comprehension of anatomical structures from upper cervical to foramen magnum, far lateral transcondylar approach could provide a safe and wide corridor to the lesions of anterior or anterolateral to the foramen magnum and upper cervical spinal cord. Moreover, an additional condylectomy based on far lateral approach would render the surgery of this challenging location safe and successful.

CONFLICT OF INTEREST

No potential conflict of interest relevant to this article was reported.

REFERENCES

1. Arnold H, Sepehrnia A: Extreme lateral transcondylar approach. J Neurosurg 82:313, 1995 (letter)

2. Babu RP, Sekhar LN, Wright DC: Extreme lateral transcondylar approach:

Technical improvements and lessons learned. J Neurosurg 81:49–59, 1994.

3. Bertalanffy H, Seeger W: The dorsolateral, suboccipital, transcondylar approach to the lower clivus and anterior portion of the craniocervical junction.

Neurosurgery 29:815-821, 1991

4. Hakuba A, Tsujimoto T: Transcondyle approach for foramen magnum meningiomas, in Sekhar LN, Janecka IP (eds): Surgery of Cranial Base Tumors. New York, Raven Press, 1993, pp 671-678

5. Katsuta T, Rhoton AL Jr, Matsushima T: The jugular foramen: Microsurgical anatomy and operative approaches. Neurosurgery 41:149-202, 1997 6. Kratimenos GP, Crockard HA: The far lateral approach for ventrally placed

foramen magnum and upper cervical spine tumors. Br J Neurosurg 7:129- 140, 1993

7. Matsushima T, Ikezaki K, Nagata S, Inoue T, Natori Y, Fukui M, Rhoton AL Jr:

Microsurgical anatomy for lateral approaches to the foramen magnum: With special reference to the far lateral approach and the transcondylar approach, in Nakagawa H (ed): Surgical Anatomy for Microneurosurgery: Anatomy and Approaches to the Craniocervical Junction and Spinal Column [in Japanese].

Tokyo, SciMed, vol VII, 1994, pp 81-89

8. Rhoton AL Jr: The far-lateral approach and its transcondylar, supracondylar, and paracondylar extensions. Neurosurg 47(3) Supplement S195-209, 2000 9. Sen CN, Sekhar LN: An extreme lateral approach to intradural lesions of the

cervical spine and foramen magnum. Neurosurgery 27:197-204, 1990 10. Sen C, Sekhar LN: Extreme lateral transcondylar and transjugular approaches,

in Sekhar LN, Janecka IP (eds): Surgery of Cranial Base Tumors. New York, Raven Press, 1993, pp 389-411

11. Spetzler RF, Grahm TW: The far-lateral approach to the inferior clivus and the upper cervical region: Technical note. BNI Q 6:35-38, 1990

12. Wen HT, Rhoton AL Jr, Katsuta T, de Oliveira E: Microsurgical anatomy of the transcondylar, supracondylar, and paracondylar extensions of the far-lateral approach. J Neurosurg 87:555-585, 1997

13. S. Balaji Pai, G. Raghuram, G. C. Keshav, Elvis Rodrigues : Far-lateral Transcondylar Approach to Anterior Foramen Magnum Lesions - Our Experience. Asian J Neurosurg 13(3): 651-655, 2018

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Table 1. A summary of patients’ characteristics Case
Fig. 2 A E BF C D
Table  1  summarizes  the  patients’ symptoms,  tumor  locations, and surgical complications

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