Journal Pre-proof

Step-by-step dissection of the extreme lateral transodontoid approach to the anterior

craniovertebral junction: surgical anatomy and technical nuances

Irakliy Abramov, MD, PhD, Mohamed A. Labib, MD, CM, David Altshuler, MD, Lena
Mary Houlihan, MD, MCH, PhD, MRCS, Nicolas I. Gonzalez-Romo, MD, Evan Luther,
MD, Michael E. Ivan, MD, Michael T. Lawton, MD, Jacques J. Morcos, MD, Mark C.
Preul, MD
PII: S1878-8750(23)01534-6
DOI: https://doi.org/10.1016/j.wneu.2023.10.132
Reference: WNEU 21363

To appear in: World Neurosurgery

Received Date: 26 July 2023

Revised Date: 25 October 2023
Accepted Date: 26 October 2023

Please cite this article as: Abramov I, Labib MA, Altshuler D, Houlihan LM, Gonzalez-Romo NI, Luther E,
Ivan ME, Lawton MT, Morcos JJ, Preul MC, Step-by-step dissection of the extreme lateral transodontoid
approach to the anterior craniovertebral junction: surgical anatomy and technical nuances, World
Neurosurgery (2023), doi: https://doi.org/10.1016/j.wneu.2023.10.132.

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© 2023 Published by Elsevier Inc.

Credit Author Statement:
Conceptualization: IA, MAL
Data curation: IA, LMH, DA, EL, MEI, MTL, JJM
Formal analysis: IA, MAL
Funding acquisition: MCP
Investigation: IA, MAL
Methodology: IA
Project administration: MCP

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Resources: MCP

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Software: n/a

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Supervision: IA, MCP
Validation: n/a
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Visualization: n/a
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Roles/Writing - original draft: IA

Writing - review & editing: all authors
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Step-by-step dissection of the extreme lateral transodontoid approach to the anterior

craniovertebral junction: surgical anatomy and technical nuances

Irakliy Abramov MD, PhD1

Mohamed A. Labib, MD, CM1

David Altshuler, MD2

Lena Mary Houlihan, MD, MCH, PhD, MRCS1

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Nicolas I. Gonzalez-Romo, MD1

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Evan Luther, MD2

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Michael E. Ivan, MD2
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Michael T. Lawton, MD1
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Jacques J. Morcos, MD2

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Mark C. Preul, MD1

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1
Department of Neurosurgery
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Barrow Neurological Institute

St. Joseph’s Hospital and Medical Center

Phoenix, Arizona

2
Department of Neurosurgery

University of Miami Miller School of Medicine

Miami, Florida
 Correspondence: Mark C. Preul, MD

c/o Neuroscience Publications; Barrow Neurological Institute

St. Joseph’s Hospital and Medical Center

350 W. Thomas Rd.; Phoenix, AZ 85013

Tel: 602.406.3593; Fax: 602.406.4104

E-mail: Neuropub@barrowneuro.org

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DISCLOSURES: The authors have no personal, financial, or institutional interest in any of the

drugs, materials, or devices described in this manuscript.

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FINANCIAL SUPPORT: This study was supported by funds from the Newsome Chair in
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Neurosurgery Research held by Dr. Preul and by the Barrow Neurological Foundation.
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ACKNOWLEDGMENTS: We thank the staff of Neuroscience Publications at Barrow

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Neurological Institute for assistance with manuscript preparation.

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SUBMISSION CATEGORY: Original Article

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 Abramov I et al. 1

Step-by-step dissection of the extreme lateral transodontoid approach to the anterior

craniovertebral junction: surgical anatomy and technical nuances

Irakliy Abramov MD, PhD1

Mohamed A. Labib, MD, CM1

David Altshuler, MD2

f
Lena Mary Houlihan, MD, MCH, PhD, MRCS1

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Nicolas I. Gonzalez-Romo, MD1

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Evan Luther, MD2
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Michael E. Ivan, MD2
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Michael T. Lawton, MD1

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Jacques J. Morcos, MD2

Mark C. Preul, MD1

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1
Department of Neurosurgery

Barrow Neurological Institute

St. Joseph’s Hospital and Medical Center

Phoenix, Arizona

2
Department of Neurosurgery

University of Miami Miller School of Medicine

Miami, Florida
 Abramov I et al. 2

Correspondence: Mark C. Preul, MD

c/o Neuroscience Publications; Barrow Neurological Institute

St. Joseph’s Hospital and Medical Center

350 W. Thomas Rd.; Phoenix, AZ 85013

Tel: 602.406.3593; Fax: 602.406.4104

E-mail: Neuropub@barrowneuro.org

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DISCLOSURES: The authors have no personal, financial, or institutional interest in any of the

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drugs, materials, or devices described in this manuscript.
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FINANCIAL SUPPORT: This study was supported by funds from the Newsome Chair in
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Neurosurgery Research held by Dr. Preul and by the Barrow Neurological Foundation.
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ACKNOWLEDGMENTS: We thank the staff of Neuroscience Publications at Barrow

Neurological Institute for assistance with manuscript preparation.

ur
Jo

SUBMISSION CATEGORY: Original Article

 Abramov I et al. 3

ABSTRACT

Background: Multicompartmental lesions of the anterior craniovertebral junction require

aggressive management. However, the lesions can be difficult to reach, and the surgical

procedure is difficult to understand. The aim of this study was to create a procedural, stepwise

microsurgical educational resource for junior trainees to learn the surgical anatomy of the

extreme lateral transodontoid approach (ELTOA).

Methods: Ten formalin-fixed, latex-injected cadaveric heads were dissected under an operative

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microscope. Dissections were performed under the supervision of a graduated, skull base

fellowship-trained neurosurgeon who has advanced skull base experience. Key steps of the

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procedure were documented with a professional camera and a high-definition video system. A
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relevant clinical case example was reviewed to highlight the principles of the selected approach
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and its application. The clinical case example also describes a rare complication: a
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pseudoaneurysm of the vertebral artery.

Results: Key steps of the ELTOA include patient positioning, skin incision, superficial and deep
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muscle dissection, vertebral artery dissection and transposition, craniotomy, clivus drilling,
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odontoidectomy, and final extra- and intradural exposure.

Conclusions: The ELTOA is a challenging approach, but it allows for significant access to the

anterior craniovertebral junction, which increases the likelihood of gross total lesion resection.

Given the complexity of the approach, substantial training in the dissection laboratory is required

to develop the necessary anatomical knowledge and ultimately to minimize approach-related

morbidity.

RUNNING TITLE: Extreme lateral transodontoid path to CVJ

 Abramov I et al. 4

KEYWORDS: Chordoma; clivus; dissection; far lateral; pseudoaneurysm; skull base; vertebral

artery

ABBREVIATIONS: CN, cranial nerve; CVJ, craniovertebral junction; ELTOA, extreme lateral

transodontoid approach; VA, vertebral artery

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 Abramov I et al. 5

INTRODUCTION

Surgical treatment of lesions involving the anterior craniovertebral junction (CVJ) can be

challenging due to the anatomical complexity of the region. Small unilateral intradural lesions

located at the anterolateral CVJ can be accessed via the far lateral approach.1-4 Extra-intradural

lesions of the anterior CVJ with a predominantly midline location require an endoscopic

endonasal approach.5, 6 Lesions with multicompartmental growth require more aggressive

management that can often be accomplished via the extreme lateral approach when the surgeon

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possesses the requisite intricate anatomical knowledge.7-9

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Different modifications of the extreme lateral approach may be selected, depending on

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the extension of the lesion; these approaches include the transfacetal, transcondylar-
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transtubercular, transjugular, and complete transcondylar approaches.10 Here, we focus on the
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microsurgical anatomy and describe the sequential steps of the extreme lateral transodontoid
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approach (ELTOA), one of the most aggressive variations of the extreme lateral approaches

offering maximal exposure to the anterior CVJ. The ELTOA involves significant tissue
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dissection and bony resection and therefore requires extensive anatomical knowledge of the
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lateral and anterior CVJ landscapes visualized from this perspective. Understanding the complex

relationships of the many vital neural and vascular structures encountered in multiple dissection

planes during this approach is critical to minimizing approach-associated morbidity.

Although other publications have described the technical steps of different extreme

lateral approaches, the surgical procedure remains difficult to understand.7-13 Previous laboratory

investigations partially discuss the steps of the ELTOA and rely mainly on illustrations or

operative videos that may be challenging to interpret without the proper surgical anatomy

background and tend to be more suitable for experienced audiences.8, 10, 11, 13 The aim of this
 Abramov I et al. 6

study is to create a stepwise, procedural, educational resource to teach junior trainees the

challenging surgical anatomy of the ELTOA. We depict the surgical nuances of the ELTOA in

step-by-step, high-quality photographs of intraoperative-oriented cadaveric dissections and

provide a didactic video to enhance the visualization and perspectives of the dissection. In

addition, we provide a clinical case example to highlight and rationalize the core surgical steps.

MATERIAL AND METHODS

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Ten formalin-fixed, latex-injected cadaveric heads were used. Nine sequential unilateral

ELTOAs were completed by a neurosurgeon skilled in neurosurgical anatomy (I.A.) to gain

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essential anatomical knowledge and to develop the expected dissection quality level. The tenth
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ELTOA was completed in a meticulous dissection of the cadaveric specimen to delineate the
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important nuances of the surgical anatomy in the approach and to document the exposure for
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demonstration purposes. Dissections were completed using microsurgical instruments and an

operating microscope (OPMI Pentero, Carl Zeiss Meditec AG, Oberkochen, Germany) under the
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supervision of a graduated, skull base fellowship-trained neurosurgeon who has advanced

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anatomical experience (M.A.L.). Key steps of the procedure were documented with a

professional camera (EOS 5DS R DSLR, Canon Global, Ota City, Tokyo, Japan) with a 50.6-

megapixel sensor and a 100-mm macro lens, as well as a high-definition video system (Zeiss

Trenion 3D HD, Carl Zeiss Meditec AG). A relevant clinical case was also reviewed to highlight

the approach selection and application principles. Institutional review board approval was not

required, as this was a cadaveric laboratory investigation.

 Abramov I et al. 7

RESULTS

Patient Positioning and Perioperative Considerations

After anesthesia induction, the patient is positioned in a park bench position with the

head secured in the 3-pin skull clamp, with the side of the lesion upward (Figure 1A). In

addition, the head is slightly abducted downward and rotated toward the shoulder contralateral to

the side of the lesion, with the mastoid tip at the highest point in the field (Figure 1B-1D).

Intraoperative electrophysiological monitoring is used to assess motor evoked potentials of

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cranial nerves (CNs) VI, VII, and IX to XII.

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Skin Incision and Musculocutaneous Dissection
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Planning the skin incision begins with identifying the relevant surface anatomical
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landmarks, which include the angle of the mandible, the mastoid process, the superior nuchal
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line, and an imaginary line projected from the inion to the C2-C3 vertebrae, approximating the

midline (Figure 2A, Video 1). After the landmarks are identified, the skin is incised in a
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horseshoe fashion, originating several centimeters below the tip of the mastoid process at the
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angle of the mandible. The incision continues in a caudal-cranial direction over the

sternocleidomastoid muscle to the superior nuchal line before turning and extending downward

to the C2-C3 spinal process level.

The skin flap is reflected inferiorly (Figure 2B). Initial soft tissue dissection exposes the

suboccipital region, with the surgeon performing elevation of the superficial muscle layers of the

sternocleidomastoid, splenius, longissimus and semispinalis capitis, and the deep muscle layers

of the superior oblique, inferior oblique, rectus capitis posterior minor and major, and levator

scapulae. First, the insertion of the sternocleidomastoid muscle is detached from the mastoid
 Abramov I et al. 8

process and is retracted anteriorly. Care is taken to identify and preserve CN XI, which runs

below the sternocleidomastoid muscle (Figure 2C). As the dissection progresses, frequent

palpation of the C1 transverse process is recommended to understand the dissection planes. The

underlying superficial muscles and fascial layers are dissected to expose the suboccipital

triangle, which is composed of the rectus capitis posterior major muscle and the superior and

inferior oblique muscles (Figure 2D-F). Dissection of the muscles of the suboccipital triangle is

performed with elevation of the superior and inferior oblique muscles from the C1 transverse

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process and medial reflection of the rectus capitis posterior major muscle (Figures 2G and 2H).

After the suboccipital triangle is dissected, several structures come into view, including the V3

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segment of the vertebral artery (VA) surrounded by the venous plexus, also called the
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“suboccipital cavernous sinus,” the internal jugular vein, and the C2 nerve root and ganglion
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(Figure 2H).14 The insertion of the posterior belly of the digastric muscle is dissected to expose
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the digastric groove. The digastric branch of the facial nerve can be used as a reliable anatomical

landmark to avoid injury to the trunk of CN VII.15 Care is required during the detachment of the
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rectus capitis lateralis muscle. This small muscle can be used as a landmark to avoid damage to
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the internal jugular vein, which exits the jugular foramen just medial to the muscle attachment

(Figure 2J). The VA and the surrounding venous sinus are mobilized in the transverse foramen of

the atlas, and the foramen is opened (Figure 2K) using the micro rongeurs. Once the tributaries

of the suboccipital cavernous sinus are transected, subperiosteal transposition of the VA can be

performed to expose the atlantooccipital joint and C1 lateral mass (Figures 2K and 2L).

The proximal trunks of the extracranial lower CNs can be identified in the carotid sheath

at the skull base according to their usual positions (Figure 3). CN XI is usually found at the

beginning of the musculocutaneous stage. It courses toward the sternocleidomastoid muscle and
 Abramov I et al. 9

can be traced back into the carotid sheath. CN XII can be found before exposure of the

extracranial orifice of the hypoglossal canal and is identified by its relationship with the C1

nerve root, which runs along the carotid sheath, giving a branch to CN XII.16 CN IX is the most

medially located nerve coursing closest to the medial surface of the internal carotid artery. The

remaining trunks in the carotid sheath constitute CN X.

Craniotomy, Clivus Drilling, and Odontoidectomy

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A low retrosigmoid craniotomy is performed to open the foramen magnum (Video 2).

The lower extension of the craniotomy can be determined by the posterior condylar vein, a

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consistent anatomical landmark that guides an effective access to the lateral rim of the foramen
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magnum.17 To prevent injury of the sigmoid sinus during the craniotomy, an imaginary line
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intersecting the digastric point (the most posterior point of the digastric groove) and posterior
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condylar vein can be used to approximate the location of the sigmoid sinus. Drilling anterior to

this line may injure the sigmoid sinus (Figures 4A and 4B).18 The jugular process, a bony
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structure on the posteroinferior surface of the jugular foramen, is resected to expose the inferior-
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posterior surface of the jugular bulb and the transition between the horizontal part of the sigmoid

sinus and the jugular bulb (Figure 4C). Resection of the mastoid tip may be required to enhance

visualization of the sigmoid sinus and jugular bulb.

Access to the extradural aspect of the anterior CVJ is gained after complete resection of

the occipital condyle and C1 lateral mass. The occipital condyle is drilled away, and the

hypoglossal canal is skeletonized (Figures 4D and 4E). Drilling below the hypoglossal canal via

the infrahypoglossal corridor allows extension of the resection to the mid- and lower clivus.19
 Abramov I et al. 10

Additional resection of the ipsilateral regions of the clivus can be achieved via the transjugular

tubercle corridor after the jugular tubercle is resected.19

Next, the C1 lateral mass is carefully drilled away. Care must be taken to avoid damage

to the surrounding critical neurovascular structures. The articulate surface of the ipsilateral

condyle, the odontoid process, and the C1 anterior arch are then exposed (Figures 4F and 4G).

Subsequently, the articulate surface of the ipsilateral occipital condyle is completely resected,

with drilling via the infrahypoglossal corridor exposing the anterior rim of the foramen magnum

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and the lower clivus (Figure 4H).

The odontoid process and anterior arch of C1 are drilled away to create a surgical

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corridor to the contralateral regions of the anterior CVJ. Depending on the extent of the exposure
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required, the entire odontoid process can be exposed and drilled, revealing the contralateral
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atlantooccipital joint and the regions of the lower clivus (Figure 4I). Drilling of the clivus
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progresses mainly through the infrahypoglossal corridor and can be extended to the middle

clivus toward the contralateral paraclival internal carotid artery (Video 2). The transjugular
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tubercle corridor can be used to resect the diseased clivus adjacent to the ipsilateral petroclival
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fissure.

Dural Opening and Surgical Wound Repair

If the lesion extends to the intradural space, the dura is incised to decompress the

brainstem. The ventrolateral brainstem and upper cervical spine can be sufficiently visualized

from the extreme lateral approach, with all the critical vascular structures adequately exposed for

vascular control of potential intraoperative bleeding (Figure 5).

 Abramov I et al. 11

Once the resection is complete, the dura is sutured back into position, and dural defects

are reconstructed with a fascial graft or artificial material. The extradural space is packed with an

autologous fat graft in combination with fibrin glue to achieve a watertight wound closure to

avoid the formation of a potential pseudomeningocele or cerebrospinal fluid leakage. After the

ELTOA, an occipitocervical fusion is required to repair the compromised CVJ stability.

Clinical Case Example

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A 22-year-old woman developed sudden-onset left-sided hearing loss and blurry vision

on both sides. The patient underwent endoscopic endonasal resection of a mass at an outside

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facility shortly after diagnosis. The pathology was consistent with a chordoma, and postoperative
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radiation was recommended. The patient delayed her care for a few months, and new magnetic
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resonance imaging demonstrated recurrence and new growth (Figure 6). The mass extended
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inferiorly into the prevertebral space, with narrowing of the nasopharynx, and into the foramen

magnum, with erosion of the superior aspect of the dens. The patient underwent a planned 2-
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stage repeat endoscopic endonasal resection followed by a left-sided extreme lateral

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transcondylar approach and C1 laminectomy to resect the lesion (Figure 6, Video 3).

Subsequently, she required an occipital bone-to-C3 vertebral fusion. Magnetic resonance

imaging obtained after tumor resection demonstrated significant decompression of the anterior

CVJ, with postoperative changes (Figure 7). Eight days after her discharge from the hospital, the

patient developed an episode of self-limiting oropharyngeal hemorrhage. Vascular imaging

demonstrated a 1.5 × 1.2 × 1.3-cm pseudoaneurysm of the left V3 segment of the vertebral artery

near the area where it had been transposed during the extreme lateral approach (Figure 7E). The

patient underwent sacrifice of the vertebral artery with coil embolization (Figure 7F). With no
 Abramov I et al. 12

new neurological or vascular complications, the patient was discharged home. Adjuvant therapy

with a proton beam radiation, consisting of 33 fractions with 11 fractions boost for a total

planned dose of 59.4 Gy + 19.8 Gy boost, was completed.

DISCUSSION

Evolution of Microsurgical Techniques for Lesions of the Anterolateral Craniovertebral

Junction

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Microsurgery for treating lesions of the anterolateral CVJ has evolved gradually, with

great advancements made by many neurosurgeons from the 1970s through the 1990s. These

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surgeons refined the techniques and expanded the indications for skull base surgery. Among the
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most significant surgical innovations has been the posterolateral retrocondylar approach for
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vertebrobasilar aneurysms, described by Heros20 in 1986. This approach, also regarded as the
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traditional far lateral approach, was later modified by George et al21 in 1988 to include additional

transposition of the vertebral artery, partial mastoidectomy, and exposure of the sigmoid sinus
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for resection of intradural lesions of the anterior foramen magnum.20-22 Sen and Sekhar were the
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first to describe resection of the posteromedial portion of the C1 lateral mass12 as well as partial

and complete condylectomy during the lateral approach to the CVJ junction.23 They named their

approach the “extreme lateral approach,” which was intended to minimize brainstem and

cerebellar retraction during the resection of intra- and extradural lesions.12, 23

Since the original descriptions of a lateral approach to the anterior CVJ, many

microsurgical techniques using different levels of bone drilling have emerged for treating lesions

of the anterolateral CVJ. However, due to the number of authors classifying their approaches

with different terminology, the nomenclature associated with these approaches often overlaps
 Abramov I et al. 13

and has become confusing, with terms such as transcondylar, far lateral transcondylar, far lateral

atlantooccipital transarticular, extreme lateral atlantooccipital transarticular, extreme lateral

transatlas, extreme lateral transtubercular, extreme lateral transodontoid, and extreme far lateral

being used.7, 10, 11, 13, 22, 24 As a result, the far lateral transcondylar approach was occasionally used

to refer to the surgical technique originally described in the extreme lateral approach. The

extreme lateral approach was named using the terms of the anterolateral and transcondylar

approaches.13, 19, 22, 25, 26

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Categorizing the lateral skull base approaches to the anterior CVJ is based on the surgical

trajectory and location of the lesion. The common, broad terms to describe surgical trajectories

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are the anterolateral and posterolateral approaches.27 The main difference between the 2
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techniques is related to the dissection of the musculocutaneous flap. In the posterolateral
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approach, the sternocleidomastoid muscle is reflected anteriorly. In contrast, the anterolateral

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approach requires posterior retraction of the sternocleidomastoid, splenius capitis and

longissimus capitis muscles, with CN XI crossing the surgical field, resulting in a more anterior
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and lateral approach.27 Based on this concept, the traditional far lateral and extreme lateral
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techniques are the posterolateral-based approaches.

From the perspective of lateral skull base approaches, the microsurgical view of the

anterior CVJ is obstructed by bony structures, including the occipital condyle, the C1 lateral

mass, and the odontoid process. Therefore, depending on the extent of the lesion, access to both

the intra- and extradural compartments often necessitates different levels of bone drilling to

achieve the desired exposure. Although both surgical trajectories can expose the odontoid

process with different extents of drilling of the occipital condyle and C1 lateral mass, the

anterolateral approach offers the advantage of being in the anterior angle of attack.13, 27 However,
 Abramov I et al. 14

the diversity of the terminology used to refer to these surgical trajectories makes direct

comparisons of surgical outcomes difficult.

The Extreme Lateral Transodontoid Approach

Access to extradural lesions of the odontoid process and contralateral CVJ was initially

introduced as part of the anterolateral approach.24, 27 Subsequently, Türe and Pamir11 proposed

the extreme lateral transatlas transodontoid approach for extradural lesions, similar to the

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technique described by George and Lot27 and al-Mefty et al24, but through the posterolateral

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trajectory, further modified with additional bone drilling and acknowledged as the ELTOA.

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As described in the current study, the ELTOA involves a great extent of soft-tissue
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dissection and bone drilling. In the demonstrated cadaveric dissection, the muscles were
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dissected in an anatomical layer-by-layer fashion. However, in a clinical setting, a single-layer

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musculocutaneous flap including all superficial muscles is recommended, because it may be

associated with better postoperative healing and fewer wound-site complications.13, 28

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One of the key elements of the ELTOA is the transposition of the V3 segment of the VA.
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Although available techniques allow for safe dissection and mobilization of the vessel, surgeons

must be aware of the intricate anatomical variability of the VA V3 segment in this region.21, 29-31

Bleeding from the muscular branch of the V3 segment of the VA can be confused with bleeding

from the extradural origin of the posterior inferior cerebellar artery, which rarely originates from

the VA.32-34 Another source of bleeding during the transposition of the VA can be related to the

occipital-vertebral anastomosis, which is a common collateral anastomosis between the external

carotid artery and the vertebrobasilar system (Figure 2H).35, 36

 Abramov I et al. 15

Complete condylectomy is performed after transposition of the VA, followed by the

removal of the lateral mass of the atlas, dens, and clivus, providing great exposure of the

extradural anterior CVJ, contralateral atlantooccipital joint, and intradural space, including the

anterolateral medulla and the pons.37 Significant exposure afforded by the ELTOA also

eliminates retraction of the dural sac (containing the caudal medulla and upper spinal cord) at the

level of the CVJ.

Access to the clivus is facilitated with a proper head position. Tilting the head downward

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and rotating it sufficiently to make the mastoid process the highest point in the field are the 2

essential maneuvers in patient positioning that contribute to satisfactory drilling of the lower and

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middle clivus (Figure 1). The downward tilt of the head widens the exposure of the CVJ and the
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clivus, and rotation of the head takes the trajectory to the lower and middle clivus, preventing
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obstruction of the surgical view by the anteriorly located musculocutaneous tissue and internal
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jugular vein (Figures 1 and 4E). The use of an endoscope with angulated lenses can significantly

enhance the resection of an extensive lesion, as it would aid in the drilling of the lower, middle,
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and even upper clivus.38 The only region of the clivus that is difficult to access is adjacent to the
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ipsilateral petroclival fissure.37

The sequela of this approach-associated invasiveness is postoperative CVJ instability,

which is related to the total or near-total removal of the atlantooccipital joint. Depending on the

patient’s perioperative status and postoperative outcome, an occipitocervical fusion can be

performed using unilateral or bilateral fusion plates in a staged operation or during the same

operative session.8, 11, 39

 Abramov I et al. 16

Clinical Application of the Extreme Lateral Transodontoid Approach

When choosing the best possible surgical approach, skull base surgeons should be self-

critical to avoid unnecessary surgical manipulations and to minimize surgery-related

complications. Despite its aggressiveness, the ELTOA in select patients remains unmatched in its

ability to deliver a desired outcome. The ELTOA has been described for the treatment of large,

expansive chordomas; atlantoaxial osteoarthritis; and congenital abnormalities of the

anterolateral CVJ.7, 11, 40 In the clinical case presented here, the histopathological diagnosis was

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consistent with a chordoma. Following the initial surgical intervention, the patient postponed

adjuvant treatment, resulting in tumor recurrence. Chordomas are challenging tumors, with a

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local recurrence rate ranging from 32% to 72% at 5 years, and a prompt staged or combined
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resection is sometimes mandatory to achieve gross total resection.41
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At the readmission of the case described, the lesion predominantly arose in the midline
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with inferior-lateral extension into the prevertebral space and odontoid process. Midline lesions

with a lateral extension or extension beyond the nasopalatine line may be challenging to
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approach from the anterior trajectory via the endoscopic endonasal technique.6, 42 Therefore, the
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ELTOA was selected to complement tumor resection as a second-stage procedure. An

anatomical comparison of the lateral skull base approaches to the endoscopic endonasal

techniques showed that in this patient, the combination of these 2 techniques could compensate

for their inherent limitations.37, 43 Considering the location of the pathologic process, the

significant exposure provided by the ELTOA can be applied for patients with anterior CVJ

lesions extending beyond the midline to the upper cervical spine, and especially for patients with

preexisting CVJ instability, as the pathologic process already invades the atlantooccipital

junction.
 Abramov I et al. 17

However, the advantage of significant exposure of the anterior CVJ is obscured by the

risk of injury to the lower CNs. Although it is transient in most cases, the reported incidence of

the lower CN deficit following the extreme lateral approaches ranges between 17.9% and 50%,

with CN XII being the most commonly injured nerve.40 In rare cases, manipulation of the

extracranial VA can result in pseudoaneurysm formation, which occurred in the presented

clinical case (Figure 7).44, 45 The natural course of such pseudoaneurysms is not well defined, and

the underlying mechanism is due to the penetrating or blunt trauma of the vessel wall during

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surgery.44 The cause of pseudoaneurysm formation in our patient is unclear, as no signs of vessel

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injury occurred intraoperatively. The usual subperiosteal dissection technique of the VA was

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used, which preserves the periosteal sheath protecting the VA, followed by gentle transposition.
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The patient experienced delayed hemorrhage after discharge on postoperative day 8. It can be
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speculated that blunt trauma to the VA, which can appear during the resection of the C1
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transverse process and retraction of the vessel, and subsequent rise in the arterial blood pressure

in the postoperative period, could have contributed to pseudoaneurysm formation and bleeding.
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A systematic review found that of 144 cases of injuries to the VA, 22 resulted in
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pseudoaneurysms; 8 of those were due to blunt trauma.44 Pseudoaneurysm management is based

on lesion size, location, and the dominance of the VA, with endovascular treatment being an

effective treatment method.44, 45

CONCLUSIONS

Judicious use of cranial microsurgical techniques, intimate anatomical knowledge, and

exceptional clinical experience are essential for managing patients with complex skull base

tumors. The ELTOA is a useful approach to the treatment of challenging extradural lesions that
 Abramov I et al. 18

arise at the lower skull base, offering access to the anterior CVJ and increasing the likelihood of

gross total tumor removal. However, given the complexity of the approach, substantial training

in the dissection laboratory is required to develop the necessary anatomical knowledge and

familiarity with the surgical route and to minimize approach-related morbidity.

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 Abramov I et al. 19

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FIGURE LEGENDS

Figure 1. Patient positioning. (A) A roll is placed under the side of the chest contralateral to the

lesion, the contralateral arm is placed on an arm support, and the ipsilateral arm is secured along

the thorax. (B) Exposure of the anterolateral craniovertebral junction (green area) can be

obstructed by the mastoid process in the lateral head position. (C) The surgical corridor can be

widened further by tilting the head downward. (D) Additional head rotation to the contralateral

shoulder affords a better surgical trajectory to the lower and middle clivus, avoiding obstruction

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of the surgical view by the anteriorly located musculocutaneous tissue. Red dashed curved lines

indicate the skin incision. Inset represents the head position. Red arrows indicate the surgical

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corridor. Blue dashed region represents the mastoid process. Blue plane represents the
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musculocutaneous layer at the anterior edge of the surgical opening. Used with permission from
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Barrow Neurological Institute, Phoenix, Arizona.

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Figure 2. Steps of a left-sided extreme lateral transodontoid approach in a cadaveric specimen.

Light blue shading represents the musculocutaneous tissue layer, which is being manipulated or
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dissected. (A) Relevant surface anatomical landmarks for the planning of the skin incision. (B)
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After inferior reflection of the skin flap, the first superficial muscles, the sternocleidomastoid and

splenius, are exposed. Pink shading shows the projection of the mastoid process and C1

transverse process, which should be palpated during dissection. (C) The sternocleidomastoid

muscle is incised and reflected anteriorly. (D) Dissection and retraction of the splenius muscle

from the mastoid process expose the next muscular layers, including the levator scapulae,

longissimus capitis, and semispinalis capitis muscles. (E) After the levator scapulae and

longissimus capitis muscles are dissected, the superior oblique and inferior oblique muscles

come into view. (F) Retraction of the semispinalis capitis muscle exposes the suboccipital
 Abramov I et al. 26

triangle, which comprises the rectus capitis posterior major muscle and superior and inferior

oblique muscles. (G) The insertion of the superior oblique muscle is divided from the transverse

process of the atlas. (H) The suboccipital triangle is completely opened after the inferior oblique

muscles are elevated from the transverse process of the atlas and reflect the rectus capitis major

muscle inferomedially. (I) Detachment of the digastric muscle exposes the internal jugular vein

and the insertion of the rectus capitis lateralis muscle at the jugular process (yellow dashed

outline). The facial nerve can be reliably identified by the digastric branch of the facial nerve

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coursing toward the main trunk. (J) The rostral and caudal attachments of the rectus capitis

lateralis muscle are carefully detached from the jugular process (yellow dashed outline) and C1

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transverse process, respectfully, to expose the most rostral part of the internal jugular vein
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exiting the jugular foramen and lateral condylar vein. (K) The vertebral artery and the
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surrounding venous plexus are identified and mobilized in the transverse foramen of the atlas.
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The transverse foramen of the atlas is opened. Transposition of the vertebral artery (white dashed

outline) can be safely performed medially and inferiorly after transection of the lateral and
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posterior condylar veins (black dashed lines). (L) The vertebral artery is transposed and retracted
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posteriorly to expose the atlantooccipital joint and the C1 lateral mass. The black dashed circle

represents caudal cranial nerves exposed in the exposed carotid sheath. Abbreviations: AM,

angle of the mandible; MP, mastoid process; Sup., superior; SCM, sternocleidomastoid muscle;

Splen. cap. m., splenius capitis muscle; a., artery; Levator scap. m., levator scapulae muscle; CN,

cranial nerve; Inf. oblique m., inferior oblique muscle; Sup. oblique m., superior oblique muscle;

Rectus cap. post. maj., rectus capitis posterior major; IJV, internal jugular vein; Digastric m.,

digastric muscle; Suboc. cav. sinus, suboccipital cavernous sinus; IJV, internal jugular vein; rec.

cap. lat. m., rectus capitis lateralis muscle; PG, parotid gland; L. cond. v., lateral condylar vein;
 Abramov I et al. 27

P. cond. v., posterior condylar vein; VA, vertebral artery; V3, V3 segment of the vertebral artery.

Used with permission from Barrow Neurological Institute, Phoenix, Arizona.

Figure 3. The rostral carotid sheath is exposed at the skull base, and the relationship of the lower

CNs is depicted. CN XII can be identified by the branch of the C1 nerve root running in a close

adjacency to the former. CN IX is usually the most medially located nerve. Abbreviations: CN,

cranial nerve; ICA, internal carotid artery; IJV, internal jugular vein; VA, vertebral artery. Used

with permission from Barrow Neurological Institute, Phoenix, Arizona.

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Figure 4. Continuation of stepwise cadaveric dissection illustrating the left-sided extreme lateral

transodontoid approach. (A) The bony resection stage begins with identifying the C1 lateral

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mass, occipital condyle, jugular process (yellow dashed outlines), and digastric point located on
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the posterior margin of the digastric groove (green dashed outline). A digastric-condylar (red
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dashed) line connecting the digastric point and posterior condylar vein is used to estimate the
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position of the sigmoid sinus and prevent the injury of the latter during retrosigmoid craniotomy.

(B) A low retrosigmoid craniotomy is performed, and the lip of the foramen is unroofed. (C) The
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jugular process is drilled to expose the jugular bulb and its transition with the horizontal part of
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the sigmoid sinus. (D) The hypoglossal canal is skeletonized after drilling of the occipital

condyle. Subsequent access to the mid- and lower clivus can be achieved through 2 surgical

corridors: the infrahypoglossal corridor, limited superiorly by the hypoglossal canal (red arrow),

and the transjugular tubercle corridor, a narrow corridor between the hypoglossal canal and

jugular bulb (yellow arrow). (E) Drilling has progressed via the infrahypoglossal (red arrow) and

transjugular tubercle (yellow arrow) corridors. The jugular tubercle and the lower clivus are

exposed. (F) The C1 lateral mass (green highlight) is drilled through to show the relationship of

the underlying bony structures. The odontoid process is projecting at the deeper dissection level
 Abramov I et al. 28

compared with the articulate surface of the occipital condyle. (G) A lateral view from the

extreme lateral approach. The C1 lateral mass has been completely drilled away, exposing the

articulate surface of the ipsilateral occipital condyle, the upper lateral spinal epidural space

(yellow dashed outline), the anterior arch of the C1 vertebra, and the odontoid process. (H) A

more lateral and caudal cranial view from the extreme lateral approach. After the complete

ipsilateral condylectomy, the extradural aspect of the anterior craniocervical junction is exposed

(yellow and white dashed outline). (I) Surgical view of the extradural anterior craniocervical

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junction after the complete ipsilateral condylectomy and odontoidectomy via the extreme lateral

approach. The contralateral atlantooccipital joint (yellow dashed circle) was exposed after

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resection of the odontoid process. Abbreviations: C1 lat. mass, C1 lateral mass; Occip. cond,
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occipital condyle; Jug. proc., jugular process; Dig. groove, digastric groove; P. cond. v., posterior
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condylar vein; VA, vertebral artery; L. cond. v., lateral condylar vein; ICA, internal carotid
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artery; JT, jugular tubercle; OP, odontoid process; Rec. cap. ant., rectus capitis anterior muscle;

C2 art. surf, C2 articulate surface; For. magnum rim, foramen magnum rim. Used with
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permission from Barrow Neurological Institute, Phoenix, Arizona.

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Figure 5. (A) The intradural view to the surface of the brainstem and surrounding neurovascular

structures after the extreme lateral transodontoid approach with complete condylectomy and

lower and middle clivus drilling. (B) A more caudal cranial view through the approach allows

visualization of the vertebrobasilar junction, contralateral vertebral artery, basilar artery, and

ipsilateral pons. Abbreviations: ICA, internal carotid artery; cAOj, contralateral atlantooccipital

junction; V3, V3 segment of the vertebral artery; V4, V4 segment of the vertebral artery; PICA,

posterior inferior cerebellar artery; Dent. l., dentate ligament; cV4, contralateral V4 segment of
 Abramov I et al. 29

the vertebral artery; BA, basilar artery; AICA, anterior inferior cerebellar artery. Used with

permission from Barrow Neurological Institute, Phoenix, Arizona.

Figure 6. Magnetic resonance imaging demonstrated a homogenous, avidly enhancing chordoma

centered in the left paramedian clivus on T1 axial (A and B) and sagittal (C) planes, measuring

approximately 3.3 x 3.2 x 5.7 cm (ML x AP x CC), with T2 isointensity evident on the coronal

plane (D). The lesion caused a significant mass effect upon the brainstem, displacing it

posteriorly with effacement of the fourth ventricle and without evidence of obstructing

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hydrocephalus. (E) Intraoperative photo of the left-sided extreme lateral transodontoid approach.

A low retrosigmoid craniotomy and transposition of the V3 segment of the vertebral artery are

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completed. (F) The lateral atlantooccipital junction (teal dashed area) is exposed. (G) The left
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hypoglossal canal is skeletonized. The drilling below and above the hypoglossal canal develops
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the infrahypoglossal (red arrow) and transjugular tubercle (yellow arrow) corridors. (H) The C1
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lateral mass and complete condlyectomy have been performed, followed by exposure of the left

hypoglossal nerve in the hypoglossal canal. The lesion is resected via the 2 aforementioned
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surgical corridors (red and yellow arrows), and the nerve is gently retracted caudally or rostrally
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with a dissector. Abbreviations: A, anterior; C, cranial; R, rostral; P, posterior; ML, mediolateral;

AP, anteroposterior; CC, craniocaudal; V3, V3 segment of the vertebral artery; MP, mastoid

process; C1 lat. mass, C1 lateral mass; Occip. cond, occipital condyle; C2 art. surf, C2 articulate

surface. Used with permission from University of Miami Miller School of Medicine, Miami,

Florida.

Figure 7. Magnetic resonance imaging after resection of the patient’s chordoma demonstrated

decompression of the anterior craniovertebral junction and postoperative changes in axial (A),

coronal (B), and sagittal (C) planes. (D) Computed tomography shows occipital bone-to-C3
 Abramov I et al. 30

vertebral fusion. (E) Computed tomography angiography shows a large left vertebral artery

pseudoaneurysm. (F) The left vertebral artery pseudoaneurysm was successfully treated by coil

embolization with no new neurological deficit. Used with permission from University of Miami

Miller School of Medicine, Miami, Florida.

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 Abramov I et al. 31

VIDEO LEGENDS

Video 1. Step-by-step left-sided extreme lateral transodontoid approach in a cadaveric specimen:

musculocutaneous stage. Used with permission from Barrow Neurological Institute, Phoenix,

Arizona.

Video 2. Step-by-step left-sided extreme lateral transodontoid approach in a cadaveric specimen:

craniotomy, clivus drilling, and odontoidectomy. Used with permission from Barrow

Neurological Institute, Phoenix, Arizona.

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Video 3. Clinical case example demonstrating left-sided extreme lateral transodontoid approach

for resection of the chordoma at the anterior craniovertebral junction. Used with permission from

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Barrow Neurological Institute, Phoenix, Arizona.
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ABBREVIATIONS: CN, cranial nerve; CVJ, craniovertebral junction; ELTOA, extreme lateral

transodontoid approach; VA, vertebral artery

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DISCLOSURES: The authors have no personal, financial, or institutional interest in any of the

drugs, materials, or devices described in this manuscript.

FINANCIAL SUPPORT: This study was supported by funds from the Newsome Chair in

Neurosurgery Research held by Dr. Preul and by the Barrow Neurological Foundation.

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