Basilar Invagination (BI)

“Introduction

Ackermann first described basilar invagination (BI) in cretins in 1790. Schuller gave the first radioimaging diagnosis, which Chamberlain and other radiologists later refined.

Basilar invagination is an abnormality at the craniovertebral junction, either congenital (born with) or degenerative (aging/injury), resulting in the odontoid being out of place and protruding into the already limited space of the foramen magnum.

It is commonly associated with conditions such as Chiari malformation, syringomyelia, and Klippel-Feil syndrome. Clinical presentations can range from chronic headaches, limited neck motion, and acute neurologic deterioration. CT and MRI are critical to diagnosing and managing this condition, including operative planning when needed.

Determining the need for operative intervention is controversial in asymptomatic patients, but those at risk of neurologic compromise could require preoperative cervical traction and algorithmic surgical strategies.[1][2][3][4]

Basilar invagination is a condition where the floor of the skull at the foramen magnum has developed in such a way that the superior aspect of the cervical spine is more cephalad (i.e. toward the head) and often posterior and, in effect, has created a narrowing at the foramen magnum opening. This area is at risk of odontoid prolapse along with the decrease in surface area that places the patient at an increased risk for neurologic injury or disruption of cerebrospinal fluid flow. This condition can result from C1-C2 facet instability, congenital osseous defect, or secondary to degenerative processes, as seen in 20% of patients with rheumatoid arthritis.

Epidemiology

BI is the most common form of craniovertebral junction malformation (CVJM).[8][9] A study examining craniovertebral junction (CVJ) anomalies in young adults observed BI to be the most common anomaly (52.3%), followed by atlanto-occipital assimilation (33.3%).[10]

One notable study looking at surgically treated BI patients indicated that a Chiari malformation might correlate to the age at presentation and symptoms. Those with a Chiari malformation usually presented later in the second (20%), third (44%), and fourth (24%) decades of life compared to those without the malformation, usually presenting earlier in the first (15%) and second (58%) decade of life.

Furthermore, those with a Chiari malformation had slower progressing symptoms occurring over a longer time, most commonly weakness (94%), paresthesia (79%), posterior column, and spinothalamic tract disturbance (56%), and ataxia (47%).  Those without the Chiari malformation mainly presented with weakness (100%), neck pain (59%), solely posterior column dysfunction (39%), bowel and bladder disturbance (28%), and paresthesia (25%).

Furthermore, while none of the patients with the Chiari malformation had a history of trauma just before symptomatology, 48% of those without the malformation noted trauma precipitating the symptoms.

Pathophysiology

The most recent theory behind Group A, BI is the atlantoaxial facet joint instability, thereby predisposing to upward migration of the odontoid peg through the foramen magnum resulting in brainstem compression.[11]

BI is the result of the listhesis of C1-C2 facets.[12] “Craniovertebral realignment”  through manipulation, distraction, reduction, and fixation of the atlantoaxial facet joint is, therefore, the principal mandate of surgery in these cohorts.

A developmental anomaly of the bone, as suggested by Virchow and Grawitz, is the pathogenesis for Group B BI. The congenital osseous dysgenesis leads to crowding of the posterior fossa and compression at the foramen magnum.[12]

Secondary natural protective mechanisms after that progress to minimize the stretching of the cord over the indenting odontoid peg by allowing a relatively stretch-free traversal.

History and Physical

There is a wide array of presentations for BI, with many of them directly resulting from the syndrome it may be associated with, such as a Chiari malformation, which is suboccipital at a rate of 33% to 38%.

The degree of cephalad migration of the dens-atlas-clivus weightlifting determines the neurologic sequelae, as this creates significant crowding at the foramen magnum as well as at the medulla oblongata.

Also, this crowding could obstruct cerebrospinal fluid (CSF) flow leading to syringomyelia. In the event of medullary dysfunction, a patient may exhibit ataxia (loss of muscle control in arms and legs), dysmetria (loss of balance and poor coordination of walking, speech, and eye movements), nystagmus (uncontrolled eye movements), dysphagia (swallowing difficulties), or cranial nerve palsies.

Interestingly there have been well-documented associations between exertional cough headaches (almost exclusively at the occipital or suboccipital, not migraine in a pattern) and BI.  In a study of 97 patients evaluated for a cough, exertional, or sexual headaches, advanced imaging noted an intracranial defect in 45% of cases, and up to 80% of the secondary cough headaches were associated with Chiari I.  The authors recommended that every patient with a cough headache have a craniocervical MRI.  In addition to coughing, these headaches can be brought on by laughing, weight lifting, or head postural changes. Other sometimes more apparent findings, while not exclusive to basilar invagination, is a short neck (reported in 78% of cases) and asymmetric face/skull or torticollis (reported in 68% of cases).

One of the frequent causes of the secondary-type basilar impression is rheumatoid arthritis. The basilar impression resulting from rheumatoid arthritis was originally termed “cranial settling” when Mathews and others interpreted odontoid migration to result from cranial descent due to eroded lateral atlantal masses. Approximately 8% of rheumatoid patients demonstrate these changes. These changes may lead to sudden death as a result of instability and require surgical fixation.

The predominant signs and symptoms in patients with BI can be broadly categorized as follows:

Constellation of presenting signs and symptoms include:

Neck pain is the most common (approximately 80%) presenting symptom. Torticollis is observed in around 40% of them.[12] The presentation is comparatively acute in Group A, whereas slowly progressive in Group B patients.[12]

Almost 60% of patients with Type A BI have a history of head injury prior to the onset of their symptoms.[12] Short neck and torticollis are common in Group A basilar invagination. They also have neurological symptoms due to direct compression of the brainstem by the odontoid process. Dysfunctioning medullary structures such as olivary nucleus and nucleus prepositus hypoglossi lead to transsynaptic degeneration, causing disproportionate atrophy of the cerebellar vermis with preserved tonsillar volume.[14] Group B patients have clinical features relating to Central cord syndrome and syringomyelia secondary to crowding of the posterior fossa.[12]

BI can be associated with other concurrent anomalies like:

Telescoping of the spinal segments, in the event of chronic atlantoaxial instability, try to confer natural protection, thereby leading to:

These natural protective sequelae are most often reversible following atlantoaxial stabilization in group A BI and foramen magnum decompression in group B BI.[16]

Evaluation

BI is most often diagnosed pertaining to the following midsagittal craniovertebral parameters:

Chamberlain’s line-running from the posterior aspect of the hard palate and the posterior margin of the foramen magnum

The criteria for diagnosis are the tip of the dens lying >5 mm above Chamberlain’s Line;   >7 mm above McGregor’s Line, or McRae’s line.

Based on Atlantodens interval (ADI):

Recently, BI has been divided into:

Dynamic CT & MRI Imaging

About Dynamic Diagnostic Imaging*

Dynamic CT imaging help assess CVJ instability.[10]

Computed tomography (CT) (*or CBCT) scan details patterns of bony abnormalities, pertinent osseous anatomy, facet angle, and degree of boy destruction. This also helps determine the need for C1–2 osteotomy.[28]

The C2 pedicle in the BI is thinner than the control group.[29] The occipital bone in BI patients is thinner (11 +/- 2.84 mm in the BI group and 17.56 +/- 3.03 mm in the control group).[30] The upper cervical spine is also relatively stiffer in BI patients.[29][31]

Preoperative CT angiography (CTA) is highly recommended to identify any anomalous variations such as “kissing” carotids, high riding vertebral, and an anomalous right vertebral artery (VA) to minimize the risk of intraoperative injury.[32][33][34][35] The separating, fusing, opacifying, and false-coloring-volume rendering (SFOF-VR) technique has been used to identify the course of the VA.[36]

Multi-positional MRI is reliable imaging to evaluate the level of cord compression, T2 signal changes, Chiari malformation, and syringomyelia.[37][28]

Treatment / Management

Evolution of Surgical Strategies

In 1939, Chamberlain first described suboccipital craniectomy, cervical laminectomy, and dural opening to manage BI. However, significant morbidity and mortality were reported following the procedure, especially by Barucha Dastur and Sinh, including the risk of intramedullary hemorrhages.

Sekir advocated the use of traction. For the few patients without any neurological disturbances, clinical and radiological preoperative traction for the progression of the disease has been described as a reasonable alternative to operative stabilization.[38][39] The determination of the approach is usually a result of the reducibility of the BI. Given the importance of reducibility in the surgical approach, preoperative traction is a valuable tool in determining the degree of reducibility and assessment of neurological status.

In a case series of surgically treated patients with BI performed by Goel et al., 82 patients without any associated Chiari malformation were placed in cervical traction, and 82% of these patients noted rapid clinical improvement after the application of traction. Traction can be a useful tool in evaluating the reducibility and predicting intraoperative neurological worsening by surgical position. Headframe reduction technique can be applied in patients with reducible atlantoaxial dislocation (AAD) and BI.[40] Irreducibility is defined as nonalignment of C1–2 during neck extension (determined on lateral x-ray) or after cervical traction.[28]Simple posterior fixation and fusion are adequate for reducible CVJ deformity.

In 1980, Menezes et al. divided craniocervical abnormalities into reducible and irreducible groups. Posterior fixation was recommended for reducible variants. Transoral decompression was followed by posterior occipitocervical fixation for stable ventral lesions, whereas dorsal decompression with or without stabilization was carried out for dorsal pathologies. Transoral surgery, first used by Kanavel, was popularized by Crockard et al.with the application of retractor systems and a microscope for managing the BI. BI is the most common indication for Occipitocervical fixation (OCF).[41] OCF, however, has implant and wound-related complications and significantly restricts head movements as well.[41]

The surgical strategies have slowly evolved from only bone overlay to sublaminar wire fixation and, subsequently, screw plate/rod fixation. From midline fixation strategies, now the notion has shifted to facet fixation, as described by Goel and Laheri.

A reduction via anterior transoral or posterior C1–2 facet distraction is necessary for irreducible deformity.[28]Posterior intra-articular distraction followed by cage implantation and cantilever correction can achieve a complete reduction in most cases.[42] One-stage release, reduction, and fixation through a posterior approach are safe and efficient.[43] A single-stage posterior stand-alone approach is accepted as the first-line treatment.[9] Posterior atlantoaxial facet reduction, fixation, and fusion (AFRF) are also recommended for patients with failed suboccipital bony decompression.[36] If C1–2 facets are fixed, osteotomy may be required.[28] Anterior release reduction and posterior fixation for irreducible BI with AAD, especially in patients with severely deformed bony mass anteriorly compressing the cervicomedullary junction.[28]

Ultimately, the approach should be made on a case-by-case basis after a thorough evaluation of clinical findings and radiographic imagings. There has been a paradigm shift from anterior and combined anterior-posterior approaches to a stand-alone posterior surgical strategy whenever feasible.

The aims of surgical interventions include:

• Foramen magnum decompression,
• Restoring and stabilizing the alignment at the CVJ, and
• Restoring normal cerebrospinal fluid flow dynamics.[9][28]

Traditionally, basilar invagination can be treated with cervical traction and posterior stabilization. However, anterior decompression via a transoral or endonasal approach may be necessary in irreducible cases.[44] Transoral atlantoaxial reduction plate (TARP) fixation, the performance of reduction and decompression, and earlier bone fusion rates of TARP procedure are superior to those of OF.[45] Transoral odontoidectomy as a salvage surgery is safe and effective for inadequate decompression from posterior distraction and fixation.[9][46]

Recently Endoscopic endonasal approach (EAA) has been postulated.[13][47] Compared to the traditional transoral or transpalatal approaches, the EEA approach has the following benefits:

Following EEA for BI, almost 90% of patients have shown neurologic improvement.[13] Image-guided navigation and intraoperative CT can facilitate localization and complete resection of the odontoid process and decompression of the spinal cord.[9]

There is, however, a steep learning curve.[13] Moreover, intraoperative and postoperative CSF leaks have been reported up to 30% and 5%, respectively.[13] A multilayered closure or a mucoperichondrial vascularized flap is preferred to prevent CSF leaks.[13][48]

Limitations of EEA include:

A recent study has validated the role of atlanto-axial facet distraction with fusion posterior only for the group A variant, whereas only suboccipital and foramen magnum decompression without need for duroplasty in the group B variant, even in the presence of syringomyelia.[50]

Posterior C1-C2 distraction and fixation is a safe and effective technique for the treatment of basilar invagination.[21] Restoring the height of the atlantoaxial lateral mass by using an individualized cage and adjusting the posterior occipitocervical angle (ΔPOCA) using cantilever technology is possible.[27] An attempt at C2 nerve root preservation is preferred. [51]The accuracy of freehand pedicle screw placement, measured by the Gertzbein-Robbins scale in BI, has sometimes been reported to be below 25%.[32] Navigation is preferred for complex congenital CVJ malformation to improve the accuracy of instrumentation.[9][52]

The inter-articular cage causes a “folding chair” effect to reduce the dislocation.[27] This cage can also be used as a fulcrum to adjust the occipitocervical angle through the cantilever technique.[27] Appropriate selection of the occipitocervical angle by adjusting the POCA by shaping the rod can be undertaken.[27] CVJ alignment measured by Clivus-canal angle and cervicomedullary angle can help plan the surgical strategy.[28] Head extension maneuver through the occipital screws and rod system for the craniocervical realignment.[28]

Posterior decompression alone, without duroplasty, in type 2 BI releases local compression,  alleviates posterior crowding, and promotes ventricular flows.[14]

A geometric model of the atlantoaxial dislocation and basilar invagination reduction is also developed.[53]

Differential Diagnosis

Platybasia  – an abnormal flattening of the base of the skull was coined by Virchow.

Basilar impression also referred to as atlantoaxial impaction or vertical cranial settling, results from softening of the bone at the skull base secondary to:

It is speculated that the basilar impression is due to recurrent microfractures from repetitive axial loads. Supporting this theory are intraoperative findings of proliferative callus at the base of the skull in patients with osteogenesis imperfect (OI). One study showed that about 25% of such patients had this defect. Even if treated secondary, basilar invagination potentially has devastating sequelae in osteogenesis imperfect patients and other osteochondrodysplasias such as Hajdu-Cheney syndrome.

Prognosis

While surgery can improve some neurological symptoms, complete recovery is not always possible. Residual neurological deficits are common and, in some cases, may be disabling.

Complications

Possible reasons for insufficient decompression include:

The presence of oilisthesis, extreme facet arthropathy, and the contraction of the tissues can hinder the realignment process.[54]

The main limiting variables in reducing AAD in BI are:

Complications of the transoral approach:

Complications of craniovertebral junction fusion surgery:

A few of the common complications of posterior fusion surgery can be:

Pearls and Other Issues

Basilar invagination is infrequently found in isolation and poses significant treatment challenges. Before any treatments specific to the condition, practitioners should screen for other associated anomalies.

Advancements in diagnostic techniques have facilitated the management of this condition. Patients with reducible invaginations potentially can avoid a combined anterior and posterior approach, requiring only posterior decompression and stabilization. The most appropriate surgical approach and fixation choices will likely remain controversial until high-level randomized trials can elucidate the most effective treatment course.

Enhancing Healthcare Team Outcomes

Basilar invagination is a rare neurological disorder that may be found in isolation and poses significant treatment challenges. Because of the complexity of management, it is best managed by an interprofessional team that includes a neurologist, neurosurgeon, ICU nurses, therapists, and a radiologist.

Before any treatments specific to the invagination, practitioners should screen for other associated conditions and try to avoid compromising potential surgical treatment for the invagination. Advancements in diagnostic techniques have assisted with the management of this condition. Patients with reducible invaginations potentially can avoid a combined anterior and posterior approach, requiring only posterior decompression and stabilization. The most appropriate surgical approach and fixation choices will likely remain controversial until high-level randomized trials can elucidate the most effective treatment course.

Irrespective of the type of surgery, some rehabilitation is required in most patients. Besides the physical therapist, the speech and occupational therapist are necessary to regain the function of the muscles.

The social worker should be involved to ensure that the patient’s home environment is safe and support systems are available. A neurology nurse should follow the patient to ensure that the patient is not worsening. Open communication between interprofessional team members is vital to improving outcomes.”