Neuroradiology

Radiological Diagnosis of Mass Lesions Within and Adjacent to the Foramen Magnum 1 Joseph A. Marc, M.D., and Mannie M. Schechter, M.D. Masses within or adjacent to the foramen magnum may present difficult clinical problems. They may sometimes be misdiagnosed as degenerative disease of the central nervous system, cervical spondylosis, or even cervical disk disease. In most cases, roentgenography is necessary for proper diagnosis. The anatomy of the region of the foramen magnum is reviewed and 13 cases representing various diseases are presented. Alterations in the regional arterial and venous anatomy are emphasized. INDEX TERMS: Brain, blood supply- Brain Neoplasms, diagnosis· CholesteatomaChordoma- Foramen Magnum· Paget's Disease· Skull Neoplasms Radiology 114:351-365, February 1975

HE DIAGNOSIS

of masses within or adjacent to the

Tforamen magnum often poses a difficult problem for

the physician (36). Disease of the vital structures which pass through this opening can produce a multitude of confusing signs and symptoms. The complex anatomy of this region, the frequently normal cerebrospinal fluid values, and the occasional remissions in the course of the disease add to the clinical perplexity (16). Elusive as these lesions may be, they always lie in a surgically accessible though treacherous area. Moreover, 25-35 % of tumors occurring in this location are benign and thus surgically curable. Unless these entities are kept in mind, one might fail to consider them in the differential diagnosis, causing appropriate treatment to be delayed until permanent damage results. Aring (1) eloquently stated the problem in these words: "To err in the diagnosis of a relievable disorder is a tragedy. A readily missed and usually eminently relievable lesion of the nervous system is one about the junction of the medulla and cervical spinal cord (a junction lesion) . .. As is often the case, the diagnosis will not be made unless it be kept in mind . . . An interesting feature of lesions about the junction of medulla and cervical spinal cord is that one almost invariably is afforded another diagnostic opportunity. In fact, I don't recall an exception. After an erroneous diagnosis, these patients come months or years later with another symptom or two or a change in signs. I believe we have always tumbled to the correct diagnosis eventually, on a second, third, or even a fourth chance. No great credit is due, for the patient would have been spared much illness had we thought of the correct diagnosis sooner."

Precise localization of the lesion, knowledge of the natural history of the disease, and familiarity with the anatomy in this region will help the physician arrive at the correct diagnosis. If the diagnostic modalities are chosen carefully, there is less risk of misdiagnosing a meningioma of the foramen magnum as multiple sclerosis, or of the surgeon exploring the posterior fossa for a suspected tumor being confronted with massive bleeding from an arteriovenous malformation. Anatomical Considerations of the Craniovertebral Junction McRae (31) has described the craniovertebral junction as an area with indefinite boundaries extending from the bones surrounding the foramen magnum down to and including the second cervical vertebra. The foramen magnum may be round or oval and measures about 35 mm in diameter in adults (larger on roentgenograms due to magnification), though its anteromedial aspect is sometimes encroached upon by the occipital condyles. It is seen best in the submentovertex and Towne projections and on submentovertex tomograms. Anomalies of the foramen magnum have been described elsewhere (4, 35). The first and second cervical vertebrae are attached to the occiput by strong ligaments. A thick ligament connects the small tubercles along the medial aspects of the superior facets of the atlas, dividing the vertebral canal into an anterior compartment containing the odontoid process and a posterior compartment containing the spinal cord and its coverings. In about 50 % of normal persons, the tip of the odontoid process is at or below Chamberlain's and

1 From the Department of Radiology, Division of Neuroradiology, Albert Einstein College of Medicine, Bronx, N. Y. (M. M. S., Professor), and the Department of Radiology, Division of Neuroradiology, Emory University and Grady Memorial Hospital, Atlanta, Ga. (J. A. M., Assistant Professor). Presented at the Fifty-ninth Scientific Assembly and Annual Meeting of the Radiological Society of North America, Chicago, III., Nov.

25-30, 1973. This work was supported in part by special fellowship awards 511 NS 2515-02 NSRB and NSO 5290-13 from the National Institute of Neurological Diseases and Stroke, USPHS. sjh

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Diagram of normal anatomy. Lateral view of the craniovertebral junction, showing the pertinent vascular and nervous structures. The vertebral artery (A) enters the foramen magnum and swings forward, joining with the opposite vertebral artery to form the basilar artery (8). The anterior spinal artery (AS) arises from the vertebral artery and runs in the anterior median raphe of the cervical spinal cord, outlining its anterior aspect. The posterior spinal artery (PS), also a branch of the vertebral artery, courses along the posterior aspect of the cervical spinal cord. The posterior spinal venous plexus (VS) is seen more frequently on angiography than the posterior spinal artery. The posterior inferior cerebellar artery (PICA) courses around the medulla oblongata (lateral medullary segment L) to reach the posterior aspect of the medulla (posterior medullary segment p). It then continues posteriorly over the superior aspect of the tonsil (supratonsillar segment oS) and descends behind the tonsil (retrotonsillar segment RJ. The choroidal point (*), at the junction of the posterior medullary and supratonsillar segments, identifies the origin of the choroidal branches of the PICA. The laterally placed hemispheric branch of the PICA (H) may originate from the proximal or distal portion of the PICA. The vermian branch of the PICA ( V) is usually a terminal branch and courses parallel and close to the midline. 1 = atlas; 2 = axis; 0 = odontoid process; 4 = fourth ventricle; 55 = straight sinus.

McGregor's lines; extension of more than half of the odontoid process above either of these lines suggests basilar invagination (31). The digastric line lies 11 ± 4 mm above the midline of the atlanto-occipital joint in normal individuals, at or below it in basilar invagination. Several bony abnormalities may cause the odontoid process to be high in relation to these lines: these include occipitalization of the atlas, platybasia, a high atlas, a short clivus, or a combination of these findings (31). Congenital bony lesions of the craniovertebral junction are usually not seen until adult life, when they may be clinically misdiagnosed as mass lesions or degenerative disease of the central nervous system, cervical

February 1975

spondylosis, or even cervical disk disease. Arnold-Chiari malformations, acquired basilar invagination, multiple sclerosis, hydromyelia, or syringomyelia can also mimic masses in this region. Multiple sclerosis of the spinal cord produces no specific radiological findings. In hydromyelia the "collapsing cord sign" on air myelography might establish the diagnosis, while an enlarged spinal cord shadow would be highly suggestive of syringomyelia in a patient with a typical history and positive findings on physical examination. The upper end of the spinal dura mater and the intracranial dura of the posterior fossa adhere firmly to the margins of the foramen magnum. Thus extradural masses in the cervical region or posterior fossa do not extend beyond these boundaries. The accompanying diagram of normal anatomy illustrates the important neural structures lying within the foramen magnum, including (a) the junction of the medulla oblongata and the spinal cord and their meninges and (b) vascular structures including the two vertebral arteries and their descending spinal arteries. The vertebral arteries enter the foramen magnum and curve forward around the lateral aspects of the medulla oblongata, uniting in front of it to form the basilar artery. The anterior spinal artery (41, 45) is located in the anterior median raphe of the spinal cord and delineates its anterior aspect. Thus angiographic visualization of this vessel permits evaluation of the position of the cord within the spinal canal. The posterior spinal arteries (45) usually form a plexus of anastomotic vessels except for a short distance at their origin, delineating the posterior aspect of the spinal cord. The anterior spinal artery is seen more commonly on angiography than the posterior spinal arteries, while the posterior spinal veins are seen more often than the corresponding arteries. The posterior inferior cerebellar arteries (PICA) arise from the vertebral arteries within the posterior fossa as described by Huang and Wolf (18) and others (13, 30, 48). The posterior medullary, supratonsillar, and tonsillohemispheric segments of the PICA are important landmarks in locating masses of the posterior fossa extending downward into the foramen magnum. Measurements of the choroidal point as described by Huang and Wolf (18), Megret (32), and Belloni and du Boulay (2) help indicate the relative anteroposterior location of a low-lying posterior fossa mass. The meningeal branches of the vertebral arteries play an important role in supplying lesions of the bony and soft-tissue structures outside the arachnoid membrane. We wish to describe 13 patients representing specific pathological and radiological entities. These cases were selected because they illustrate the radioloqical findings found to be most valuable in each condition. Although some of these entities are not ' 'mass' , lesions, they may mimic masses at the craniovertebral junction. In each case the clinical picture is presented briefly, followed by the radiological and surgical or postmortem findings when available. The order of presentation is as follows:

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A. Congenital lesions 1. Arteriovenous malformations 2. Arnold-Chiari malformations B. Acquired lesions 1. Tonsillar herniations 2. Vascular (aneurysms) 3. Neoplastic a. Neoplasms involving the rim of the foramen magnum Meningiomas of the foramen magnum Metastases to the rim of the foramen magnum Chordomas extending to the rim of the foramen magnum b. Tumors of the fourth ventricle Papillomas c. Brainstem gliomas extending into the foramen magnum d. Cerebellar and tonsillar hemangioblastomas e. Masses of the cerebellopontine angle Cholesteatomas 4. Unknown etiology Paget's disease with basilar invagination CASE REPORTS

Arteriovenous Malformations CASE I: A 3%-year-old boy presented with sudden ataxia and a resting tremor of the left arm and leg. Pneumography showed hydrocephalus, and the patient was discharged with a diagnosis of cerebellar degeneration. At the age of 7 he was readmitted with nausea, vomiting, and a hyperextended neck. Examination revealed a stiff neck, severe nystagmus, and ataxia. Lumbar puncture showed bloody cerebrospinal fluid. The basal view of the skull showed enlarged foramina transversaria of C1 (Fig. 1, A). Vertebral angiography disclosed a sizable arteriovenous malformation involving the right cerebellar hemisphere, with large vertebral arteries and dilated sinusoids filling the foramen magnum (Fig. 1, B and D). A review of the pneumogram obtained three years earlier showed that the worm-like vascular structures were identifiable on close examination (Fig. 1, C). Surgery revealed the arteriovenous malformation as well as evidence of previous hemorrhage. Dilated, serpiginous vessels replaced the cerebellar tonsils and filled the foramen magnum.

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ma may trap the unwary into misdiagnosing a tumor on the basis of the pneumogram. In addition, dilated arterial and venous channels protruding through the foramen magnum may mimic cerebellar tonsils on pneumography. Conversely, if no structural displacement is evident it is tempting to diagnose an Arnold-Chiari malformation or degenerative disease of the central nervous system. Delay in establishing the correct diagnosis may result in recurrent bleeding and blockage of the subarachnoid cisterns and the exit foramina of the fourth ventricle, leading to internal hydrocephalus if the patient survives the acute ictus. Arnold-Chiari Malformations CASE II: A 33-year-old man presented with a one-year history of headaches, neck pain, and progressive unsteadiness of gait. Examination showed right hemiparesis, a right Babinski sign, and ataxia. Demyelinating disease of the nervous system was the presumptive diagnosis, though a tumor of the medulla or upper cervical cord and cervical spondylosis were also considered. Films of the cervical spine revealed occipitalization of the body of C1 and fusion of the spinal processes of C1 and C2 with basilar invagination. On cervical myelography, the cerebellar tonsils were seen as a round, bilobate defect at the foramen magnum (Fig. 2, A). Vertebral angiography showed descent of the tonsillohemispheric branch of the PICA, indicating low-lying cerebellar tonsils (Fig. 2, B), but there was no evidence of a mass within the posterior fossa. Angiography excluded the possibility of a neoplasm and confirmed the low position of the tonsils, supporting the diagnosis of an Arnold-Chiari malformation.

COMMENT: Finding a bilobate structure on Pantopaque myelography at the foramen magnum is not reliable evidence of an Arnold-Chiari malformation. Pneumography is perhaps most rewarding, since it may show that the fourth ventricle or part of the cerebellum has extended into the upper cervical region (20-22, 42, 46). However, angiography is advised, since tumors at the level of the foramen magnum may also show a bilobate appearance on Pantopaque myelography. The low position of the tonsillohemispheric branch of the PICA and lack of evidence of a space-occupying lesion should suggest the diagnosis. Tonsillar Herniations

COMMENT: A full-axial view should be obtained routinely in the investigation of lesions around the foramen magnum. The enlarged foramina transversaria suggested vascular pathology in this case. Routine plain films followed by angiography should be the initial investigative procedure in suspected posterior fossa pathology, even if an arteriovenous malformation is not suspected. Air studies may be contraindicated in patients with a bleeding arteriovenous malformation in order to avoid a possible air embolism. When pneumography is the initial investigation of choice, the worm-like appearance of vessels lying within the air-filled subarachnoid spaces may be characteristic enough to permit or at least suggest the diagnosis (37). Only bleeding arteriovenous malformations simulate space-occupying lesions. The mass effect of a hemato-

CASE III: A 5-year-old girl presented with a six-month history of headaches, progressive disturbance of gait, vomiting, and neck stiffness. On examination, bilateral papilledema and left cerebellar signs were noted. Vertebral angiography revealed a large, avascular mass in the left cerebellar hemisphere with evidence of tonsillar herniation, seen as downward extension and stretching of the tonsillar branch of the PICA to the level of C1-C2 (Fig. 3). The tonsillar branch arose from the tonsillohemispheric segment of the PICA at the posterior portion of the superior aspect of the tonsil. The swollen tonsil was outlined anteriorly by the posterior medullary segment, superiorly by the supratonsillar segment of the PICA, and posteriorly by the tonsillar branch.

COMMENT: Herniation of the cerebellar tonsils into and below the foramen magnum commonly accompanies posterior fossa masses. Pneumography or cervical myelography may outline the shadows of the tonsils

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Fig. 1. CASE I. Arteriovenous malformation. A. Plain skull film, basal view, showing the enlarged foramina transversaria (arrows) through which the vertebral arteries course. B. Left vertebral angiogram, lateral view, showing a large arteriovenous malformation partly situated within the foramen magnum (arrows). C. Pneumoencephalogram, reverse Towne view. The worm-like structures outlined by air within the posterior fossa and foramen magnum represent the arteriovenous malformation (arrows). The fourth ventricle is also outlined by air. D. Postoperative right vertebral angiogram, lateral view, showing the markedly dilated vertebral artery.

as masses within or below the foramen magnum. Nonfilling of the ventricles during pneumography is not uncommon in the presence of mass lesions in the posterior fossa, and in such cases angiography may be required to establish the diagnosis. Wickbom and Hanafee have described the tonsils as bilobate smooth intraarachnoidal defects in normal individuals. They become elongated and flattened in persons with an Arnold-Chiari malformation or a slowly growing posterior fossa mass or rounded by a rapidly enlarging neoplasm (47).

However, it has been our experience that the tonsils may take any shape as they herniate through the foramen magnum, regardless of the pathological condition. The cerebellar tonsils may have irregular lower margins without tumor involvement. Vertebral angiography not only helps outline the tonsils as seen through the segments of the PICA (18) but may reveal the pathological process responsible for the herniation. It is necessary to be familiar with the numerous variations in the course of the PICA (18, 30) so as not to confuse a normal varia-

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Fig. 2. CASE II. Arnold-Chiari malformation with basilar invagination. A. Cervical myelogram, postero-anterior view. The low-lying cerebellar tonsils are seen as two rounded structures within the foramen magnum (arrowheads). Note the asymmetry of the tonsils, which could be mistaken for a lobular mass or a tumor infiltrating one of the tonsils. B. Left vertebral arteriogram, lateral view, showing the low position of the tonsillohemispheric branch of the posterior inferior cerebellar artery (arrowheads). As there is no evidence of a space-occupying lesion, an Arnold-Chiari malformation with low-lying tonsils should be suspected.

Fig. 3. CASE III. Left cerebellar cystic astrocytoma with tonsillar herniation. A. Left vertebral angiogram, lateral view. The basilar artery is displaced anteriorly against the clivus (--). The superior cerebellar arteries are elevated (4-). The hemispheric branches of the posterior inferior cerebellar artery are stretched and depressed ( 1). The choroidal point is displaced forward (*). B. Left vertebral angiogram, lateral view. Magnification reveals the posterior medullary segment (-), the supratonsillar segment and the retrotonsillar and tonsillar branches of the posterior inferior cerebellar artery ( ~ ), outlining the herniated, swollen tonsil.

(t ),

tion with tonsillar herniation. Magnification and subtraction techniques will help in most cases. If the tonsillar branch lies below the foramen magnum, tonsillar herniation is definitely present. Stretching of the hemispheric branches of the PICA over the edge of the foramen magnum in the anteroposterior projection, as described by Margolis and Newton (29), is also indicative of tonsillar herniation.

Aneurysms Within the Foramen Magnum CASE IV: A 31-year-old woman with a history of frontal headaches for several years experienced progressive generalized weakness, transient diplopia, and unsteadiness of gait for eight months prior to admission. Examination disclosed left-sided weakness with a left Babinski sign and bloody cerebrospinal fluid. Sagittal tomograms of the skull showed a 2-cm curvilinear calcification within the foramen magnum (Fig. 4, A). Pneumography revealed that the fourth

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Fig. 4. CASE IV. Aneurysm of the left vertebral artery, simulating a mass lesion. A. Sagittal tomogram at the level of the foramen magnum, showing a semicircular calcification which is convex downward (arrows). An aneurysm should be suspected even in the absence of a typical history or signs of subarachnoid hemorrhage. B. Pneumoencephalogram, reverse Towne view, showing upward elevation and tilting of the fourth ventricle by the aneurysm acting as a mass (arrows). The vallecula is displaced toward the left. One should not attempt to remove such a "mass" without first performing angiography. [Reproduced from Rothman at al. (39) and Schechter and de Gutierrez-Mahoney (40) by permission of the authors and publishers] C. Left vertebral angiogram, lateral view. A large fusiform aneurysm of the left vertebral artery at the origin of the PICA is seen, together with marked backward displacement of the distal vertebral artery and the proximal basilar artery, indicating a large space-occupying lesion (larger, in fact, than the visible aneurysmal cavity). At operation, the aneurysm was found to have a sizable intramural thrombus. [Reproduced from Schechter and de Gutlerrez-Mahoney (40) by permission of the author and publisher] D. Photograph of the operative field, showing the aneurysm (*) within the foramen magnum. The lower medulla oblongata and upper cervical spinal cord are displaced laterally (open arrows). The upper cervical nerve roots are stretched (arrowheads). The left cerebellum (0) is retracted superiorly.

ventricle and vallecula were displaced posteriorly and tilted (Fig. 4, B). Althouqh vertebral angiography was performed bilaterally, an aneurysm was seen only on the left side (Fig. 4, C). The degree of vascular and ventricular displacement indicated that the aneurysm was probably much larger than the opacified cavity. At surgery, a 3-cm aneurysm of the vertebral artery was found at the origin of the PICA (Fig. 4, D).

COMMENT: Large aneurysms involving the vertebral arteries or their branches are uncommon. They may be classified as (8) acute, with all of the manifestations of intracranial bleeding, usually followed by sudden death, and (b) chronic, with a prolonged history extending over several months or years. It is the latter group that the

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Fig. 5. CASE V. Meningioma of the foramen magnum. A. Cervical myelogram, oblique view. The column of contrast material is displaced posteriorly (arrows) by an oval extradural lesion. Some contrast material has passed above the lesion, indicating an incomplete block. B. Left vertebral angiogram, lateral view with subtraction. A marked tumor stain is present (*). The anterior spinal artery is displaced posteriorly and attenuated (-). Anterior to the tumor, the anterior meningeal branch of the cervical vertebral artery ( +t- ) is hypertrophied, supplying the tumor.

radiologist is more likely to encounter. Symptoms depend upon the location and size of the aneurysm (10); they include brainstem, cerebellar, or upper cervical cord compression or a combination of these. In less than one-third of patients with a ruptured infratentorial aneurysm, the signs and symptoms suggest the site of the lesion (49); signs of spontaneous subarachnoid hemorrhage are slight and often absent. The clinical picture can be misleading, and the signs and symptoms are usually nonspecific. The cerebrospinal fluid may be clear or xanthochromic. Vertebral angiography is the only definitive diagnostic modality in such cases. The aneurysm may fill from one vertebral artery and not the other, as in the above case. Thus each vertebral artery should be studied separately by angiography. Since the aneurysm may simulate a space-occupying lesion and not be visualized on angiography despite adequate technique, a large, thrombosed aneurysm should be considered when investigating the craniovertebral junction, particularly in a patient with curvilinear calcification and a history of subarachnoid hemorrhage. Meningiomas of the Foramen Magnum CASE V: A 59-year-old woman with a decubitus ulcer and incontinence became progressively weak in all extremities over a fiveyear period. Examination disclosed flat optic disks, a generalized decrease in motor strength, and a sensory level to pin, touch, vibration, and position sense at and below C4. Deep tendon reflexes were 3+ bilaterally, with bilateral Babinski signs. Cerebrospinal fluid protein

ranged between 140 and 500 mgt 100 ml. Pantopaque myelography showed an anterior extradural lesion within and below the foramen magnum, producing an incomplete block (Fig. 5, A). Some Pantopaque passed beyond the obstruction to cap the upper pole of the mass at the rim of the foramen magnum. Vertebral angiography showed that the vertebral, PICA, and basilar arteries were unaffected. The anterior spinal artery showed marked backward displacement and attenuation of its proximal course (Fig. 5, B). The anterior meningeal branch of the vertebral artery supplied a densely stained 3.5-cm oval lesion at the foramen magnum. At surgery, the upper cervical spinal cord was found to be displaced backward and flattened by an anterior meningioma. COMMENT: A total of 2-4 % of all spinal meningiomas occur at the foramen magnum. They are the most common type of extramedullary lesion at this level, twice as common as schwannomas. Most previous reports describe the bizarre clinical patterns associated with benign tumors in the vicinity of the foramen magnum (9, 16, 26, 27, 36), although some workers believe that the clinical syndrome is stereotyped (43). The subarachnoid cisterns in this region allow room for steady growth up to a point, beyond which vital structures are compressed against the bony boundaries (44). In addition, compression of the blood supply to the upper cervical cord and medulla may give rise to peculiar and seemingly unrelated and distant signs. Thus it is not surprising that many such cases were formerly misdiagnosed. The ultimate diagnosis usually rests with the neuroradiologist. Myelography (14, 28) will confirm the presence of an extramedullary lesion, usually situated

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A Fig. 6. CASE VI. Metastatic lesion of the tip of the clivus from a hypernephroma of the kidney. A. Right vertebral angiogram, anteroposterior view with subtraction. The hypertrophied anterior meningeal branch of the right vertebral artery (arrowheads) supplies a densely stained metastatic lesion (*) at the tip of the clivus. [Reproduced from Newton (33) by permission of the author and publisher] B. Lateral view of the right vertebral angiogram, showing the densely stained lesion of the tip of the clivus (*) supplied by the hypertrophied anterior meningeal branch (arrowheads) of the right vertebral artery. One vertebral artery is arched backward by the tumor. The bony landmarks have been retouched for clarification. [Reproduced from Newton (33) by permission of the author and publisher]

anteriolaterally in meningiomas and posterolaterally in schwannomas. Myelography may also reveal coexisting cervical spondylosis, a not uncommon finding. Angiography may reveal a tumor stain supplied by meningeal branches of the vertebral artery (33) and demonstrate the effects of compression on the adjacent spinal arteries, spinal cord, and lower medulla.

Metastases to the Foramen Magnum CASE VI: A 61-year-old man had had a tooth extracted one week before admission. Progressive dysphagia and dysarthria subsequently developed. On examination, the man was chronically ill, with a paralyzed tongue and absent gag reflex. Sagittal midline tomograms of the skull showed destruction of the inferior tip of the clivus. Bilateral vertebral angiography revealed a vascular lesion of the tip of the clivus, supplied by the anterior meningeal branches of both vertebral arteries. The latter vessels were displaced posteriorly behind the vascular mass and within the foramen magnum (Fig. 6). The lesion proved to be a metastatic deposit from a hypernephroma of the kidney. COMMENT:

Metastases to the margins of the fora-

men magnum can be the first manifestation of a distant malignant neoplasm. In this case, the highly vascular nature of the lesion was helpful.

A vascular supply from

meningeal branches of the vertebral arteries indicates dural invasion (33). The destructive bony changes are seen better on sagittal or submentovertex tomograms. Positive- or negative-contrast myelography and pneumography are least informative in such cases.

Chordomas of the Clivus CASE VII: An 8-year-old girl demonstrated slurred speech shortly after tonsillectomy. A month later, her tongue became deviated to the right. Six months later, severe frontal headaches, lethargy, and personality changes became apparent, together with choking attacks on drinking and regurgitation of fluids through the nose. Examination showed nasal speech, nystagmus, insensitive gag reflex, weak palatal movement, and fibrillation of both sides of the tongue. Skull films revealed widened sutures. Pneumography demonstrated backward displacement of the spinal cord and medulla in the region of the foramen magnum, evidenced by posterior displacement of the vallecula and fourth ventricle (Fig. 7, A). Left vertebral angiography showed posterior displacement of the entire basilar artery and the distal vertebral arteries (Fig. 7, B), which were also narrowed due to compression against the posterior lateral lip of the foramen magnum. Surgery revealed a large tumor in front of the bralnstern, stretching the ninth, tenth, and eleventh cranial nerves and extending through the foramen magnum to the lower border of the arch of the atlas and displacing the lower end of the medulla and upper cervical

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Fig. 7. CASE VII. Chordoma of the clivus. A. Pneumoencephalogram, lateral view, showing backward displacement of the fourth ventricle (*) and vallecula (arrowheads). Displacement of the vallecula indicates downward extension of the lesion. [Reproduced from Zingesser and Schechter (50) by permission of the authorand publisher] B. Left vertebral angiogram, lateral projection. The entire basilar and distalvertebral arteries are displaced posteriorly in an arcuate fashion ( - ) and the distalvertebral artery is compressed against the margins of the foramen magnum ( -t+ ). The choroidal point (0) shows backward displacement proportional to that of the vertebral artery, indicating that the lesion is in front of the medulla. [Reproduced from Zingesser and Schechter (50) by permission of the author and publisher]

cord posteriorly. Pathological examination showed that the lesion was a chordoma. COMMENT: Chordomas are invasive, destructive tumors (5) arising from remnants of the notochord, which may persist in the adult anywhere along the clivus or spinal column. Of 46 chordomas of all sites reported by Higinbotham et a/. (3, 15), 36 % occurred at the clivus. Nodular retrosellar calcifications, destruction of the clivus, and a retroclival soft-tissue mass are the most important findings (7). Zingesser and Schechter (50) have demonstrated extension of clivus chordomas upward through the tentorial hiatus. Chordomas can also extend caudad into the foramen magnum, as in the above case, or start at the foramen magnum (34). Marked backward displacement of the distal vertebral artery and its compression against the lip of the foramen magnum, as well as backward displacement of the cervical spinal cord shadow, vallecula, and fourth ventricle, indicate downward extension o.f the tumor. Since chordomas are usually midline lesions, there is no significant lateral displacement.

Tumors of the Fourth Ventricle CASE VIII: A 56-year-old woman had a history of forgetfulness of insidious onset, gradual weakness, and trembling of the hands and legs for two years. Parkinson's disease was diagnosed by her local doctor and treated accordingly. Six months before admission she demonstrated incontinence and a weight loss of 36 kg (80 lb.). On examination she was cachectic and disoriented, with a poor memory, left lower facial weakness, and involvement of the ninthand tenth cranial nerves. Her neck was stiff, and flexion was limited. All extremities demonstrated spasticity, decreased power, and hyperactive reflexes, with bilateral Babinski signs. Vertebral angiography

showed stretching and elongation of the supratonsillar segment of the PICA. Contrary to the classic description of upward elevation of this segment of the artery in masses of the fourth ventricle, it was depressed, even showing a slightdownward convexity (Fig. 8, A and B). This finding, coupled with the roughening and irregularity of the posterior margin of the foramen magnum on plain films, suggested downward extension of the tumor. The patientdied on the ninth hospital day, and autopsy disclosed a large ependymoma filling the fourth ventricle. The lower pole of the tumor was attached to the dura overlying the posterior margin of the foramen magnum (Fig. 8, C). COMMENT: Tumors of the fourth ventricle are the commonest type of posterior fossa neoplasm that may extend into and through the foramen magnum (12). When the tumor is confined to the fourth ventricle, the supratonsillar segment of the PICA is stretched and elevated, showing an upward convexity. However, when the tumor extends downward into the foramen magnum, the PICA curves downward instead, suggesting that the main thrust of the vector of forces is caudad. When the anterior and posterior spinal arteries which demarcate the anteroposterior diameter of the upper cervical cord are displaced anteriorly, they indicate that the tumor has extended into the foramen magnum. The inferior vermian vein and its retrotonsillar tributaries are moved backward, indicating posterior displacement of the inferior vermis, while the veins of the lateral recesses of the fourth ventricle are displaced laterally. Thus the supratonsillar segment of the PICA, the spinal vessels, and the inferior vermian veins are the most useful landmarks (13, 17-19). Although vertebral angiography is usually the neuroradiological procedure of choice, ventriculography with negative and positive contrast media may be

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Fig. 8. CASE VIII. Ependymoma of the fourth ventricle. A. Left vertebral angiogram, lateral projection. The supratonsillar segment of the posterior inferior cerebellar artery is stretched and elongated anteroposteriorly and convex downward (black arrows), while the retrotonsillar segment is displaced backward (white arrow). These findings indicate anteroposterior elongation of the tonsil due to compression and flattening by a centrally placed fourth ventricle mass. The downward convexity of the supratonsillar segment is contrary to the usual upward arching in such cases and reflects the caudad direction of the vector of forces and the caudad extension of the tumor. B. Left vertebral angiogram, anteroposterior projection. The supratonsillar segment of the posterior inferior cerebellar artery is elongated and displaced laterally and downward (arrows). The anterior, lateral, and posterior medullary segments of the posterior inferior cerebellar artery are crowded and displaced downward (arrowheads). C. Postmortem midsagittal section of the brain demonstrates a large mass (*") filling and enlarging the fourth ventricle (arrowheads) and displacing the medulla anteriorly and the cerebellum posteriorly. Note the downward extension of the tumor.

helpful in evaluating problem cases. Among other tumors of the fourth ventricle, papillomas of the choroid plexus, cholesteatomas, and meningiomas produce similar findings. Brainstem Masses CASE IX: A 17-year-old girl demonstrated ataxia, decreased vision, and headaches 18 months prior to admission. Communicating hydrocephalus of unknown etiology was diagnosed at another institution; a shunting procedure was performed, and her vision improved. A year later she became continually drowsy; the shunt was re-

placed, and her level of consciousness improved. She was admitted to our institution 2 years later with increasing ataxia, progressive dysphasia, and visual disturbances. Examination showed pale optic disks and horizontal nystagmus with evidence of multiple bilateral cranial nerve involvement and exaggerated deep tendon reflexes. Left carotid angiography and ventriculography indicated a mass within and adjacent to the third ventricle (Fig. 9, A). Left vertebral angiography showed a large mass involving the brainstem and extending upward to the mesencephalon (Fig. 9, B), anteriorly in front of the pons, and inferiorly into the medulla and upper cervical spinal cord. The inferior extension was indicated by posterior displacement of the choroidal point and the posterior medullary segment of the PICA.

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Fig. 9. CASE IX. Astrocytoma of the bralnstem. A. Left carotid angiogram, lateral view. Pantopaque demonstrates a filling defect within the third ventricle (arrows). The roof of the third ventricle is outlined by the internal cerebral vein (arrowheads). B. Left vertebral angiogram, lateral view. The basilar and distal vertebral arteries are displaced away from the clivus posteriorly (black arrows) by extension of a brainstem astrocytoma extra-axially (paradoxical dislocation). Upward extension into the midbrain and thalamus is indicated by stretching and hypertrophy of the thalamic perforating arteries (white arrow) and by indentation of the Pantopaque within the third ventricle (arrowheads). Downward extension is both exophytic (indicated by backward displacement of the basilar artery and distal vertebral arteries away from the anterior lip of the foramen magnum) (the tip of the clivus), and intra-axial (indicated by a marked increase in the anteroposterior diameter of the medulla oblongata). This is evidenced by the marked oblongation and stretching of the lateral medullary segment of the PICA (white arrows) and the increased distance between the choroidal point (*) and the basilar artery.

Marked stretching, elongation, and lateral displacement of the lateral medullary segment were seen, indicating enlargement of the medulla oblongata. The exophytic portion of the tumor in front of the pons and medulla and behind the clivus extended through the foramen magnum, as indicated by posterior displacement of the distal vertebral and anterior spinal arteries away from the anterior lip of the foramen magnum. Surgery disclosed a large brainstem mass extending superiorly into the mesencephalon and involving the medulla oblongata and upper cervical spinal cord inferiorly and also exophytically in front of the brainstem and upper cervical spinal cord. COMMENT: Brainstem masses may extend in any direction but most commonly grow superiorly toward the thalamus; inferior extension into the foramen magnum is less common than in masses of the fourth ventricle. Marked lateral displacement and elongation of the lateral medullary segment of the PICA indicate an enlarged, infiltrated medulla. If the tumor becomes exophytic in front of the medulla and upper cervical spinal cord, the distal vertebral, proximal basilar, and anterior spinal arteries may be displaced posteriorly. Endocranial drainage of enlarged spinal cord veins (8) would also indicate upper cervical spinal cord extension.

the fourth ventricle (Fig. 10, A); however, the vermian branch of the right PICA was shifted to the left, indicating a mass in the right cerebellar tonsil extending to the midline. Subtraction films showed a densely stained tumor nodule 1 cm in diameter within the foramen magnum (Fig. 10, B). Air ventriculography failed to show the fourth ventricle or aqueduct. A cystic hemangioblastoma with small mural nodules involving the right tonsil, fourth ventricle, and inferior vermis was found at surgery and proved histologically. CASE XI: A 35-year-old man presented with a is-year history of increased numbness in the hands and feet. Myelography revealed an irregular bilobate defect at the foramen magnum, representing a tumor; this was mistaken for the bilobate defect of the normal cerebellar tonsils (Fig. 11, A) and a presumptive diagnosis of multiple sclerosis was made. Two months later, weakness developed in both legs, accompanied by diplopia and lethargy. Examination showed papilledema, left sixth-nerve palsy, and a broad-based ataxic gait. Vertebral angiography disclosed a densely stained midline tumor involving the left cerebellar tonsil and fourth ventricle and extending through the foramen magnum, with its lower pole at the level of the C1 arch (Fig. 11, B and C). The anterior spinal artery was displaced anteriorly against the posterior surfaces of the bodies of C1 and C2 (Fig. 11, C), while the posterior spinal veins were displaced posteriorly against the anterior surfaces of the posterior neural arches of C1 and C2. Surgery revealed a tumor of the inferior vermis and left tonsil, with its lower pole at the level of the first cervical vertebra.

Cerebellar Hemangioblastomas CASE X: A 40-year-old woman presented with a six-month history of increasing occipital headaches of insidious onset as well as blackouts, slurred speech, and unsteady gait for one month. Examination showed papilledema, nystagmus, and ataxia. Bilateral vertebral angiography revealed marked bilateral elevation, stretching, and elongation of the supratonsillar segment of the PICA, more marked on the right, resembling the appearance of this segment in tumors of

COMMENT: Hemangioblastomas may be solid tumors but usually have cystic components. They more commonly affect the lower structures of the posterior cranial fossa and the upper cervical spinal cord. The probable source of such tumors is a vascular analogue developing in or adjacent to the posterior end of the fourth ventricle in utero (23, 24). Angiography is the preferred

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B

Fig. 10.. CASE X. Hemangioblastoma involving the midline structures, including the fourth ventricle. A. Left vertebral angiogram, lateral view. The supratonsillar segments of both posterior inferior cerebellar arteries, filled by reflux into the right vertebral artery, are stretched, elongated, and arched, more marked on the right (arrowheads) than on the left (white arrows). The bulk of the mass is cystic, but a densely stained nodular component (*) is located at the foramen magnum. The hemispheric branch of the posterior inferior cerebellar artery (black arrows) is stretched and displaceddownward below the foramen magnum. B. Left vertebral angiogram, lateral projection. The early venous phase shows the densely stained nodular component of the lesion within and just below the foramen magnum (*). The margins of the foramen magnum have been retouched for clarification. diagnostic procedure in such cases, as it will indicate the location and the nature of the highly vascular lesion. There may also be hypertrophy of the PICA, which is usually the main supply to these tumors. On the lateral projection, the distance between the anterior and posterior spinal arteries may be increased when the upper cervical spinal cord is involved, while the dilated upper cervical venous plexus may be seen draining endocranially. Myelography may be misleading, as the lower pole of the mass could be mistaken for the cerebellar tonsils. Pneumography may indicate the presence of a lesion without defining its nature.

Masses of the Cerebellopontine Angle Extending into the Foramen Magnum CASE XII: A 52-year-old woman presented with inability to walk unaided, decreased hearing on the right side, and a history.of progressive dizziness and nausea for five years and diplopia for one year. Examination showed vertical and horizontal nystagmus, an absent right corneal reflex, anesthesia in the distributionof the first and second trigeminal roots, and a positive left Babinski sign. Tomograms of the temporal bones showed sclerosis of the right petrous portion. Pneumography revealed an elongated soft-tissue mass in the right cerebellopontine angle and within the foramen magnum (Fig. 12, A). Air within the interstices gave the tumor a mottled appearance. Vertebral angiography showed an avascular mass in the right cerebellopontine angle, displacing the basilar and distal vertebral arteries posteriorly. The PICA and the anterior inferior cerebellar artery were displaced posteriorly, with the former depressed and the latter elevated (Fig. 12, B). A cholesteatoma of the cerebellopontine angle extending to the foramen magnum was found at surgery and proved histologically.

compression may be appreciated on angiography. Posterior displacement of the distal vertebral artery, stretching and depression of the PICA, and backward displacement of the anterior spinal artery are helpful signs. Pneumography and tomography should be employed with caution and only if the intracranial pressure is not markedly elevated, since these techniques may cause the tonsils to become impacted in the foramen magnum, already occupied by a tumor.

Paget's Disease with Basilar Invagination CASE XIII: A 56-year-old woman presented with progressive deafness, aphasia, and difficulties in gait of several years duration. Plain films of the skull showed evidence of Paget's disease with basilar invagination (Fig. 13, A), although it was not suspected clinically. Right brachial angiographyshowed marked posterior deviation of the vertebral artery at the foramen magnum, forming a semicircular arc which was convex posteriorly (Fig. 13, B). The basilar artery was markedly attenuated. The external carotid artery branches were hypertrophied, supplying a vascular calvaria. COMMENT: It is well known that basilar invagination is sometimes a complication in Paget's disease of the

COMMENT: When cerebellopontine angle masses extend through the foramen magnum to the upper cervical

skull and that hearing loss and progressive symptoms of brainstem and upper cervical spinal cord compression may be seen as well (35,38). Tonsillar herniation is also known to occur in such cases (6, 11). Plain film findings are diagnostic and will indicate the degree of basilar invagination. If angiography is performed to exclude a cerebellopontine angle mass, vascular changes characteristic of Paget's disease should be recognized, among them narrowing of the basilar artery (11). We wish to emphasize the semicircular appearance and posterior convexity of the distal vertebral artery and the relative

area, the resulting medullary and upper cervical cord

posterior location of the PICA, as these findings may

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Fig. 11. CASE XI. Midline hemanqloblastorna, A. Cervic~1 myelogram', postero-anterior view, showing an irreqular 'bilobate defect at the foramen magnum (arrowheads) representing the tumor. This was mistaken for the cerebellar tonsils. 8. A densely stained hemangioblastoma is situated in the midline, extending to both sides and displacing the left supratonsillar segment laterally (arrowheads). The lower margin of the lesion is within the foramen magnum. C. Left vertebral angiogram, arterial phase. The lateral view shows that the anterior spinal artery is displaced forward against the posterior aspect of the odontoid process (arrows). The tonsillar branch of the posterior inferior cerebellar artery (arrowheads), seen below the foramen magnum, is hypertrophied.

Fig. 12. CASE XII. Cerebellopontine angle mass (cholesteatoma). A. Coronal tomogram taken during pneumoencephalography, showing a large lobulated mass (arrows) in the right cerebellopontine angle. [Reproduced from Long et aJ. (25) by permission of the author and publisher] B. Left vertebral angiogram, lateral view. The anterior inferior cerebellar artery (black arrows) is markedly elevated and displaced posteriorly. The posterior inferior cerebellar artery (white arrows) is markedly depressed and displaced posteriorly. The entire intracranial vertebral and basilar arteries are displaced posteriorly (arrowheads). The degree of arterial displacement indicates the rather extensive superoinferior extension of the mass. The effects of the mass on the distal vertebral, proximal basilar, and posterior inferior cerebellar arteries indicate its extension into the foramen magnum. Although the choroidal point (*) is displaced backward, it maintains its logical relationship to the basilar and vertebral arteries, indicating that the bralnstem is not increased in size but is displaced posteriorly by the mass. The clivus has been retouched for better delineation.

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Fig. 13. CASE XIII. Paget's disease with basilar invagination. A. Plain skull film, lateral view, showing the thickened, dense calvaria. Note the basilar invagination with an inverted, saucer-shaped basal convexity, elevation of the margins of the foramen magnum, and elevation of the petrous pyramids. B. Right brachial angiogram, lateral view. The distal vertebral artery forms a semicircle, open anteriorly (open arrows), around the deformed basal bony structures. The basilar artery filled and emptied quickly (black arrowheads) and is markedly thin in appearance. The choroidal point (*) is displaced posteriorly but maintains its normal relationship to the basilar artery and particularly to the distal vertebral arteries. The tonsillohemispheric branches of the posterior inferior cerebellar artery (white arrows) outline the low position of the cerebellum relative to the brainstem, the result of basilar invagination.

mimic a posterior fossa mass, especially a tumor of the cerebellopontine angle. CONCLUSIONS

It is evident from the above discussion that a wide variety of pathological conditions may occur at the craniovertebral junction. Some may go unrecognized for many years until serious neurological sequelae have developed. Because of the benign nature of many of these lesions, exact localization and early diagnosis are mandatory if treatment is to be beneficial. The proper radiographic approach should begin with plain radiographs of the skull and spine, including tomograms. These may show curvilinear calcification at the foramen magnum or enlargement of the upper cervical foramina transversaria, suggesting an aneurysm or arteriovenous malformation. Paget's disease, metastatic lesions, chordomas, and some cerebellopontine angle masses may produce characteristic radiological changes. Anomalies of the foramen magnum or upper cervical spine (4, 31, 35) should be excluded by plain films and tomograms before searching for a tumor. Vertebral angiography is probably the most useful and safest contrast examination for lesions in this location, although tomography (with or without air studies) and myelography are often helpful as well. The proximal basilar and distal vertebral arteries and their branches, including the PICA, the anterior and posterior spinal arteries, and the meningeal branches of the vertebral arteries, as well as the inferior vermian and anterior and

posterior spinal veins, are the main vascular structures that will help in locating and identifying a lesion. Pneumography, high cervical myelography, and Pantopaque cisternography may show changes indicative! of a lesion within the foramen magnum or extending into it from the posterior fossa, but they will not always revl3al the true nature of the tumor. Pneumography may reveal elevation and backward displacement of the vallecula and fourth ventricle and widening of the upper cervical spinal cord and/or medulla; in addition, in patients with an Arnold-Chiari malformation, pneumography may be more helpful than angiography if the fourth ventricle and the low-lying tonsils are seen within the upper cervical canal. Radiological investigation of the craniovertebral junction requires judicious selection of diagnostic modalities and recognition that one type of study may complement another. Diagnosis of the presence and probable nature of a lesion will be made more frequently and with far greater conviction when one is familiar with the normal and abnormal anatomy of this region. ACKNOWLEDGMENTS: We wish to thank Dr. Thomas H. Newton, University of California, San Francisco, Calif., for permitting us to use CASE VI, and Dr. Octavia Cortez, Director, Department of Radiology, St. Barnabas Hospital, New York, N.Y., for allowing us to use CASE VIII. Department of Radiology Division of Neuroradiology Emory University ao Butler St., S.E. Atlanta, Ga. 30303

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