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Management of Tratamento de Invaginação Basilar Andrei Fernandes Joaquim1, MD, PhD.

RESUMO A invaginação basilar (IB) constitui-se de uma anomalia do desenvolvimento da região crânio-cervical que resulta no prolapso da coluna cervical superior na base do crânio, comumente associada com outras anormalidades do neuro-eixo, tais como malformação de Chiari do tipo I e siringomielia. Neste artigo, revisamos os conceitos necessários para entender e tratar os pacientes com IB. O tratamento é discutido com base na classificação proposta por Goel, que divide a IB em dois grupos: grupo A - pacientes com elementos de instabilidade na junção crânio-cervical e grupo B - pacientes com IB secundária à hipoplasia do . O tratamento no grupo A consiste no realinhamento e na estabilização da junção crânio-cervical, muitas vezes através de uma abordagem por via posterior isolada, evitando a morbidade inerente às descompressões por via anterior. No grupo B, a descompressão do forame magno é o tratamento de escolha. As técnicas cirúrgicas a serem utilizadas dependem da anatomia do paciente e da experiência do cirurgião. Resultados cirúrgicos adequados podem ser obtidos com o entendimento dos conceitos e formas de tratamento das diferentes apresentações da IB. Palavras Chave: invaginação basilar, classificação, tratamento.

ABSTRACT Basilar invagination (BI) is a development anomaly of the craniocervical junction that results in a prolapsed of the upper cervical spine into the base, commonly associated to other bone and neural abnormalities, like Chiari I malformation and . In this paper, we review the concepts necessary to understand and treat BI. The most comprehensive and accepted classification system is the proposed by Goel, which divides patients with BI into two groups, as it follows: group A) patients with clear elements of instability; and group B) BI secondary to clivus hypoplasia. Treatment in group A includes craniocervical realignment and stabilization, most of the times using an isolated posterior approach, obviating an unnecessary and morbidity of the anterior decompression. In group B, decompression is the treatment of choice. Surgical techniques should be adequate according to patient’s anatomy and surgeon’s experience. Good surgical results can be obtained with the understanding of the main concepts and treatment options of BI. Keywords: basilar invagination, classification, diagnosis, surgical treatment.

understand and treat BI based on its classification and the Introduction different surgical strategies adopted to treat this challenge and complex anomaly. Basilar invagination (BI) is a radiographic finding that consists in a development anomaly of the craniocervical junction in which the odontoid process is at least 2 mm above Chamberlain’s line (although up to 6.6 mm has been advocated as the normal Material and Methods limit), resulting in a prolapse of the upper cervical spine into the skull base6,10,24. Bone anomalies can cause or be associated A systematic review of the literature using the MedLine with BI. The most commonly findings are clivus hypoplasia, Database (National Library of Medicine), covering the period condyle hypoplasia, anomalies of the atlas formation and from 1980 to 2012, was performed. The search strategy atlanto-occipital assimilation24,25,26. In addition, about 30% of involved the keywords “basilar invagination treatment”. the patients with BI have also neural axis abnormalities, like Inclusion criteria included English language (or translated , syringomyelia and hydrocephalus30. text), diagnosis of basilar invagination, discussion about management and surgical treatment of this entity. No age In this paper, we review the basic concepts necessary to

1Assistant Neurosurgeon – Division, State University of Campinas (UNICAMP), Campinas-SP. Brazil and Centro Infantil Boldrini, Campinas-SP.

Received, Apr 25, 2012. Accepted, Oct 08, 2013 Joaquim AF. - Management of Basilar Invagination J Bras Neurocirurg 24 (1): 53-59, 2013 54

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restrictions were included. All case series, clinical studies and review articles were also included. In addition, a manual search of all referenced articles not found in the search was performed. 315 articles were initially found. Cross references of classic historical articles were also included. We excluded some articles based on repeated information for the purpose of our review. After all abstracts were screened, 31 articles were evaluated and included in our review.

Basic craniocervical craniometry (figure 1) Some basic craniocervical craniometrical concepts are necessary to diagnosis, understand and treat BI. A brief review Figure 1: A – In B, we have the Basion (full arrow) and in O the opisthion (dash arrow). B – The Chamberlain Line, C- The McRae line defining the plane of the of the main craniometrical points is exposed, as it follows: foramen magnum and D- The Wackenheim Clivus Baseline or Basilar line (full line), that forms part of the clivus-canal angle if we add an additional line (dash line) that Basion – it refers to the anterior margin of the foramen passes along the posterior body of the axis. magnum24. Opisthion – it refers to the posterior margin of the foramen Craniocervical junction – anatomic anomalies of clinical magnum24. importance in the treatment of bi McRae line – defines the plan of the foramen magnum. It is Some anatomic development anomalies are associated with BI. formed by a line from the basion to the opisthion. The tip of the The most important are presented below: odontoid process should be fall below this line24. Atlantooccipital Assimilation - assimilation of the atlas is Platybasia – this term refers to a flattening of the skull base. caused by a failure of segmentation between the skull and It can be associated to BI but also may present in isolation23. the first cervical , completely or partially. Although The diagnosis of platybasia is made based on the measurement the Wackenheim clivus baseline may be normal, the clivus- of the Welcher Basal Angle24. This angle is defined by a line canal angle may be decreased. It’s commonly associated with extended from the nasium to the anterior tubercullum sellae fusion of the axis and third cervical vertebra. This association and other from this last to the basion. In normal subjects, it (atlantooccipital assimilation and axis-C3 fusion) is associated 26 should be less than 140o. Patients with increasing in this angle with atlantoaxial subluxation in about 50% of the cases . had the diagnosis of platybasia. Basilar impression – it refers to the acquired form of BI Wackenheim Clivus Baseline or Basilar line – this is a line secondary to softening of the bone and joints at the base of the along the clivus extending inferiorly into the upper cervical skull. The main etiologies include , Paget 24,25 spine canal. It should fall tangent to the posterior aspect disease, infection, tumors, among others . This term was of the tip of the odontoid process. The angle formed by the proposed by Virchow, in 1876, 19 years later of the introduction 27,28 intersection of the line constructed along the posterior surface of the term platybasia . of the axis body and the Wackenhein clivus baseline is called as Basiocciput (clivus) Hypoplasia – represents the hypoplasia of craniovertebral or clivus-canal angle. It normally ranges from the basiocciput that results in shortening of the clivus and BI 150o to 180o, changing about 30o with flexion and extension (violation of the Chamberlain line by the tip of the odontoid), positions24,26,29. Craniocervical kyphosis can be attributed when decreasing the clivus-canal angle and producing cranio-cervical the clivus-canal angle is less than 150o. kyphosis, resulting in deformity at the cervicomedullary junction26. Basion – it refers to the anterior margin of the foramen

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magnum24. Condylar Hypoplasia - The underdevelopment of the occipital CLASSIFICATION OF BI condyles, with a flattened appearance, leads to basilar Goel proposed a classification of BI based on the presence invagination, secondary to violation of the Chamberlain line or absence of clinical and radiological instability12. This and widening of the atlantooccipital joint axis angle. The tip classification is important once it can help surgeons in to of the odontoid process and the lateral masses of the atlas lie decide the best form of surgical treatment: below the McRae line. The lateral mass of the atlas may be fused to the hypoplastic condyles, accentuating the BI and Group A – This group main characteristic is the presence of limiting the movements of the atlantoccipital joint24. a clear instability of the region manifested by the tip of the odontoid process distancing itself from the anterior arch of the Chiari Type I Malformation – a caudal rhombencephalon atlas or the lower end of the clivus. A case example of BI of this abnormality that it is represented by a downward displacement group is presented in Figure 2 and 4. of the cerebellar tonsils and the medial portions of the inferior cerebellar lobes into the cervical spinal canal7,8. Symptoms Diagnostic criteria: are secondary to valve effect by the protruding tonsils at the - atlantoaxial dislocation (generally with C1-2 subluxation) foramen magnum or direct compression of nervous tissue. - tip of the odontoid process protruded into the foramen magnum and above the Chamberlain line, McRae line and CLINICAL AND RADIOLOGICAL EVALUATION Wackenheim’s clival line Patients can present with symptoms of BI at all ages, but most Patients may have also Chiari malformation with tonsilar commonly at the second and third decade of life. Some clinical herniation and syringomyelia. signs can be clearly seen at the first inspection, like torticollis, limited movements, low hairline implantation and short neck. Most of the patients present with neurological deficits, like muscular weakness, gait abnormalities, posterior column and bladder dysfunction, or even low cranial nerves deficits14,23. Sometimes, only neck pain is reported. Symptoms onset can be acute, following a minor trauma, but they are generally chronic and progressive23,30. Radiological evaluation includes Computer Tomography (CT) scan with sagittal and coronal reconstructions to evaluate the bone anatomy and craniocervical Magnetic Resonance Figure 2: Patient with BI of the group A - A – Saggital MRI showing ventral (MR) imaging, to evaluate the neural axis abnormalities, like compression by the tip of the odontoid. B – Sagittal CT scan showing Chiari malformation and the presence of syringomyelia. In the tip of the odontoid above the Chamberlain line and McRae line. C- Sagittal CT scan with an anterior lysthesis of the C1 lateral mass (with an assimilation with some cases, when clear instability cannot be inferred in static the condyle) (full arrow). D- Sagittal CT scan after traction, showing the tip of the radiological exams, at least one dynamic study should be odontoid below the McRae line, decreasing brainstem compression and in E, we can see reduction of the C1-2 lysthesis (full arrow). F- Post operative CT scan after performed in patient evaluation, such as a sagittal flexion and an occipito- C2 fusion and foramen magnum decompression. Note the tip of the extension CT scan or MR at the T2 weighted sequence. odontoid went downward. Patient improve substantially of her symptoms. Surgical treatment is indicated in symptomatic patients once BI is a progressive disease that can lead to severe disability or even death. In asymptomatic patients, close clinical and radiological follow-up is necessary, surgery may be an option in presence of mild symptoms, like cervical pain, or pyramidal signs or presence of syrinx.

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Figure 3: Patient with BI of the group B – note the platybasia (the Welcher Basal Figure 4: Patient with BI of the group A – Sagittal T2 MRI showing compression Angle of 162o (normal 140o) and a clivus-canal angle 103o preoperative (yellow of the brainstem by the dens. Preoperative CT scan showing C1-2 subluxation (B) line). There is a clivus hypoplasia with condyles hypoplasia, as shown in Figure B and the dens protruding into the foramen magnum (C). Note that a posterior fossa (arrow). C – The Sagittal MRI shows brainstem deformation and tonsillar herniation. decompression had been performed previously in another service. Sagittal CT Note that BI of the group B, the tip of the odontoid is below the McRae line (yellow scan after traction and reduction of the C1-2 subluxation and occipito cervical line). D- Sagittal Ct Scan after a posterior foramen magnum decompression and fusion, with the tip of the odontoid moving downward in D, E and F. occipito-C2-3 fixation in extension, increasing the clivus canal angle to 124o . E- Intraoperative picture after instrumentation and F – Post operative CT scan Group B – There is no instability. The alignment of the anterior reconstruction. arch of the atlas, the odontoid process and the inferior aspect SURGICAL TREATMENT of the clivus remains normal. Probably, this condition is secondary to a complete clivus hypoplasia. Platybasia can be Surgical treatment is proposed based on the classification of found in both groups, but it occurs most commonly in group B. BI. Figure 3 shows a case example of a BI in this group. Group A Diagnostic criteria: Realignment of the craniocervical junction results in indirect - atlantoaxial relation is normal, neural decompression19,21. Goel, in 2004, proposed an innovative posterior approach with C1-2 joint distraction and - tip of the odontoid process is above the Chamberlain’s line, direct lateral mass fixation involving placement of spacers - tip of the odontoid is below the Wackenheim’s clival line and in the joints to reduce odontoid migration and reestablish the McRae’s line. craniocervical aligment13. Although technically challenge, The distance between the ponto-medullary junction and the this is the only surgical option that treats C1-2 instability odontoid process is markedly reduced. Posterior cranial fossa directly, being considered the gold standard of treatment in volume can be also markedly reduced in this group. Chiari I patients of group A. This technique requires a long learning malformation is commonly found. curve, with expertise in C1 - C2 fixation using screws, once most of these patients have vertebral artery anomalies and small lateral masses or atlas assimilation. As an alternative, other surgical options can be used. One of these options is preoperative traction and, if reduction is obtained, an occipito- cervical fusion can be performed. Although occipital fixation with screws is preferred, sometimes the is thin, precluding screw insertion. In these cases, wiring techniques are then preferred, even though a less rigid construction is obtained. Jian et al., 2010, published a series of 27 out of 28 patients

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successfully treated with direct intraoperative posterior suboccipital craniectomy, to avoid postoperative cerebellar occipito-C2 pedicle screws reduction with distraction and herniation3,9. However, a large craniectomy has been proposed fixation of BI with atlantoaxial dislocation. After tightening the by others reshaping the small volume of the posterior fossa22. rod in the occipital bone, distraction is performed, moving the Opening of the and coagulation of the tonsils odontoid inferiorly, and then inserting C2 rod holder17. It can even in presence of a syrinx, is controversialy. Many authors be an option in patients whose anatomy precludes C1 screw advocate that these maneuvers lead to an unnecessary risk of insertion or in cases without reduction of C1-2 subluxation complications such as CSF leak, and infection14. with preoperative traction. The potential disadvantages of Others advocate radical tonsil coagulation and duraplasty to this technique, when compared with C1-2 distraction and improve the neural decompression and increase posterior fossa fixation, is that it can leads to craniocervical fixation in flexion volume1,4,15. and an unnecessary occipital fusion in patients without atlas assimilation. Preoperative traction is not helpful in changing craniocervical parameters of patients in this group12,14. This can be explained Nowadays, anterior approaches are rarely used, being indicate by the fact that there is no instability in these patients with only for patients with irreducible ventral compression of the clivus hypoplasia. brainstem. Patients treated in other institutions with previous occipito-cervical fusion without reduction of C1-2 subluxation Failure in obtain clinical improvement after posterior 5,11 may have some benefits from an anterior decompression. A fossa decompression have been reported . Worsening of direct transoral-transpharyngeal approach is the most common craniocervical kyphosis can exacerbate cervicomedullary 16 form of anterior decompression18,20. Endoscopic transnasal, compression over the odontoid . In patients with an o transoral and even transcervical approaches have been also important kyphotic clivus-canal angle (less than 130 ), the proposed, followed by a posterior occipito-cervical fusion brainstem can suffers severe deformative stresses, resulting 16 in selected cases, with or without an additional posterior in clinical deterioration . Once traction is not useful in to decompression2,31. restore craniometrical parameters, these patients may have clinical benefits with craniocervical fusion in mild extension, improving clivus-canal angle in up to 30o to decrease brainstem Summary of treatment in BI - Group A – surgical options deformity and stress16,24.

Treatment of Choice: Summary of treatment in BI - Group B – surgical options 1) C1-2 distraction and manipulation of the joints using spacers. Treatment of Choice: 1) Posterior foramen magnum decompression. Treatment Options: Options: small versus large craniectomy/ duraplasty/ tonsil coagulation 1) Preoperative traction followed by occipito-Cervical fusion if reduction was obtained or; (Preoperative traction is not useful in this group) 2) Direct intraoperative distraction using occipito-C2 pedicle Treatment Option: instrumentation. 1) Craniocervical fusion in mild extension in patients with Anterior approaches: irreducible C1-2 subluxation with ventral clinical deterioration after posterior fossa decompression or compression or previously fixed patients without reduction. severe kyphosis at the craniocervical junction (small clivus- canal angle). Group B Treatment in this group is mainly based on posterior foramen magnum decompression13. Some authors advocate a small

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4 Batzdorf U. Chiari I malformation with syringomyelia. Conclusion Evaluation of surgical therapy by magnetic resonance imaging. J Neurosurg 1988;68(5):726-30. 5 Botelho RV, Neto EB, Patriota GC, Daniel JW, Dumond PAS, Rotta JM. Basilar invagination: craniocervical instability treated Treatment of BI is guided according to the presence (Group A) with cervical traction and occipitocervical fixation Case report. Journal of Neurosurgery Spine 2007;7(4):444-9. or absence (Group B) of C1-2 instability. Surgery can improve 6 Chamberlain WE. Basilar impression (platybasia). Yale J Biol patient symptoms and restore quality of life. Understand the Med 1939; 11(5):487-96. different types of BI, as well as the associated neural axis 7 Chiari H. Über Veränderungen des Kleinhirns infolge von abnormalities are necessary to optimize surgical results. Hydrocephalie des Grosshirns. Dtsch med Wschr 1891;17:1172- Moreover, a correct radiological evaluation of bone and neural 5. anatomy allows surgeons to choose the best surgical technique, 8 Chiari H. Über Veränderungen des Kleinhirns, des und der improving patient outcome. in Folge von congenitaler Hydrocephalie des Grosshirns. Dtsch Akd Wissensch 1895;63:71-125. 9 Duddy MJ, Williams B. Hindbrain migration after decompression for hindbrain : a quantitative assessment using MRI. Brit J Extends from the posterior portion of the hard Neurosurg 1991;5(2):141-52. palate to the opisthion. The odontoid tip should Chamberlain Line be located below this line in normal subjects (or 10 Klaus E. Rontgendiagnostik der platybasic und basilar until 2 mm above it) Impression. Fortschr Rontgenstr 1957; 86:460-9.

Defined by a line extended from the nasium to 11 Grabb PA, Mapstone TB, Oakes, WJ. Ventral Brain Stem the anterior tubercullum sellae and other from Compression in Pediatric and Young Adult Patients with Chiari Welcher Basal Angle this last to the basion. Should be less than 140o. I Malformations. Neurosurgery 1999; 44(3):520-7. Increasing in this angle leads to the diagnosis of 12 Goel A. Basilar invagination, Chiari malformation, platybasia syringomyelia: a review. Neurol India 2009;57(3):235-46. A line from the basion to the opisthion. Defines McRae line 13 Goel A. Treatment of basilar invagination by atlantoaxial joint the plan of the foramen magnum distraction and direct lateral mass fixation. J Neurosurg Spine A line along the clivus that extending it inferiorly 2004;1(3):281-6. Wackenheim Clivus into the upper cervical spine canal. It should be 14 Goel A, Bhatjiwale M, Desai K. Basilar invagination: a study Baseline or Basilar line fall tangent to the posterior aspect of the tip of the based on 190 surgically treated patients. J Neurosurg 1998; odontoid process 88(6):962-8. Angle formed by the intersection of the line 15 Gonçalves da Silva JA, Holanda MMA. Basilar impression, Craniovertebral or constructed along the posterior surface of the Chiari malformation and syringomyelia. A retrospective study clivus-canal angle axis body and the Wackenhein clivus baseline. It of 53 surgically treated patients. Arq Neuropsiquiatr 2003; normally ranges from 150o-180o 61:368-75.

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Corresponding Author

Dr. Andrei F. Joaquim. Disciplina de Neurocirurgia, Universidade Estadual de Campinas, SP. Departamento de Neurologia – Cidade Universitária Zeferino Vaz CEP: 13083-970 Campinas-SP, Brazil Institution: State University of Campinas (UNICAMP), Campinas-SP, Brazil. Consents were obtained from the patient presented in this paper. Financial Disclosure: The authors have no financial interest in this article. E-mail: [email protected]

Joaquim AF. - Management of Basilar Invagination J Bras Neurocirurg 24 (1): 53-59, 2013