vertebrobasilar artery in rheumatoid atlantoaxial subluxation · basilar artery insufficiency...

Journal of Neurology, Neurosurgery, and Psychiatry, 1976, 39, 122-128

Vertebrobasilar artery insufficiency in rheumatoidatlantoaxial subluxation

M. W. JONES AND J. C. E. KAUFMANN

From the Department ofPathology (Neuropathology), University Hospital,London, Ontario, Canada

SYNOPSIS Cervical myelopathy has become commonly recognized as a complication of rheumatoidatlantoaxial subluxation. A small group of patients with atlantoaxial subluxation may have inter-mittent symptoms associated with change of head position and which are due to vertebral arterycompression. Two such cases are reported, one with necropsy findings of infarction in the areasupplied by the vertebrobasilar system. The pathogenesis of the symptomatology and infarction isdiscussed.

There are two important neurological syndromesthat can arise from rheumatoid atlantoaxialsubluxation (AAS). One is a compressionmyelopathy (Stevens et al., 1971; Smith et al.,1972) which can uncommonly be complicated byacute compression with tetraplegia or death(Davis and Markley, 1951). The other lesscommon syndrome is that of ischaemicsymptoms related to vertebrobasilar arteryinsufficiency. We have recently encountered twocases of this latter syndrome, one of which cameto postmortem examination. Pathological re-ports are rare but a comparable case was reportedby Webb et al. (1968). This was a 53 year oldfemale with AAS and vertebral artery throm-bosis whose symptoms were intermittent.

CASE 1

Mrs. M.H. is a 45 year old lady with a 15 year historyof seropositive rheumatoid arthritis. Six monthsbefore admission she had one week of confusedamnestic behaviour of uncertain aetiology. Sincethen, she has had repeated bouts of vertigo, asinterpreted by a neurologist, without other symptomsassociated with neck flexion or head rotation. On theday of admission she fell unconscious and hadbilateral clonic movements. In the emergency room

Address for correspondence: Dr J. C. E. Kaufmann, Department ofPathology (Neuropathology), Health Sciences Centre, University ofWestern Ontario, London, Ontario, Canada N6A 3K7.(Accepted 18 September 1975.)

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the aetiology of her semicomatose state was notapparent. Forced flexion of her neck and back inpreparation for a lumbar puncture provoked

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FIG. 1. Case 2. Diagram of infarcted areas in thedistribution of the posterior cerebral artery territoriesas well as scattered inJarcts in cerebellum and brain-stem. Some infarcts were older thani others.

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Vertebrobasilar artery insufficiency in rheumatoid atlantoaxial subluxation

FIG. 2. Case 2. High cervical cord showing areas of infarction affecting grey and white matter (arrows).Luxol-fast blue and cresyl-violet, about x 2.5, enlarged photographically.

opisthotonos. Bilateral carotid angiograms were

normal; however, on retrospect AAS was seen. Thefollowing morning the patient was alert but con-

fused and bilateral vertebral angiograms revealednormal vessels with no signs of impaired flow at theC1-C2 intervertebral space. Ten millimetres of dis-placement between the odontoid process and theanterior arch of Cl vertebra was noted. The patientinadvertently flexed her neck in the recovery room

and again exhibited opisthotonos and lapsed into a

stuporous state from which she awoke throughphases of confusion and hallucination. At allexaminations, her brain-stem reflexes, cranial nerves,

deep tendon reflexes, muscle tone, and plantarreflexes were considered normal. A posterior fusionwas performed wiring Cl to C2 vertebra (Gallitechnique). It was not possible to get close oppositionand there was a 9.5 mm gap from the anterior archof Cl vertebra to the odontoid process. There was an

11 mm canal behind the odontoid process.The patient was seen 19 months postoperatively

and had had no more symptoms of vertigo on neckflexion or rotation.

SUMMARY Her symptoms of vertigo seemed solelyrelated to head flexion or rotation. We are suggestingthat her comatose state and the mental confusion thatfollowed were secondary to vertebral artery narrow-ing from the AAS. The vertebral angiogram wasdone when she was alert and her neck no longermoved enough to impair blood flow. In retrospect,the week of confusion six months before admissionprobably reflected a small stroke in her posteriorcerebral artery territory (Mathew and Meyer, 1974).Tight opposition of Cl vertebra to the odontoidprocess was impossible at surgery. Chun et al. (1974)reported on the presence of a thick pannus ofrheumatoid tissue present between the arch of Clvertebra and the odontoid process acting as a masslesion preventing close opposition. In their case, itwas necessary to remove the abnormal tissue throughan oral approach but in our case this was notnecessary as her symptoms were primarily vascularand not those of a compressive myelopathy.

CASE 2Mr. W.D.M. was a 74 year old man with a 30 year

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M. W. Jones and J. C. E. Kaufmann

history of typical deforming rheumatoid arthritis.Seven months before death he began to complain ofvertigo, as interpreted by a neurologist, whichwould occur with flexion and/or rotation of his headto the right. In addition to vertigo, he would alsodescribe a presyncopal feeling on arising in the morn-ing which would be relieved by lying down. Duringthis time, there were several falls with unconscious-ness lasting for minutes but these could not becharacterized further and were not investigated. Inthe month preceding admission he developed pro-gressive weakness and paraesthesia of all four limbsand by the time of admission was unable to walkbecause of weakness and could no longer do up hisbuttons. He also complained bitterly about a constantsuboccipital head pain.Examination revealed a wasted emaciated man

who had an orthostatic drop in blood pressure from190/110 to 110/80 mmHg. with symptoms of light-headedness. He was certain that this sensation wasdifferent from his vertiginous feeling. He had been onantihypertensive medicine, which was discontinuedon admission. Cranial nerve examination was nor-mal. There was a moderate global weakness withmild flexion contractures of the hips, knees, andelbows. An accurate assessment of muscle tone wasimpossible because of his painful deformed joints.Deep tendon reflexes were reduced in the legs andnormal in the arms; plantar reflexes were equivocal.

Radiography showed anterior subluxation of Cland C2 vertebrae and an upward herniation of theodontoid process through the foramen magnum,giving a picture of pseudobasilar invagination. Onthe 11th hospital day, while upright, the patientsuddenly became unconscious for five minutes. Heawoke and remained restless, confused, and dis-orientated. He now had right lateral gaze nystagmus,

FIG. 3. Case 2. This lateral radiograph of the bilateral extensor plantar reflexes, and inability todissected necropsy specimen shows upward herniation hold his legs up against gravity. He was put inof the odontoid process (arrow) through the foramen traction with skull tongs and his mental state and

magnum above the basi-occiut (curved arrow) better weakness were definitely improving when on thethan films made during life. The posterior part of the 29th hospital day he suddenly became unconsciousspinal column and foramen magnu) have been and was deeply comatose with decerebrate posturing

removed. Note arch of atlas (arrow). and Cheyne-Stokes respirations. His level of con-

sciousness improved over the following days and he

FIG. 4. Case 2. View of the interior ofposterior fossa with dorsum sellae above and confluence of the sinusesbelow. Note the odontoid process of the axis well into the posterior fossa (black arrow) and displaced to theright side. It lies immediately in front of the lower brain-stem and upper spinal cord which are still in situ.(white arrow).FIG. 5. Case 2. Dissected specimen offoramen magnum area viewedfrom behind. The pedicles and laminae ofthe vertebrae have been removed. Note the herniated odontoid process of the axis projecting into the posteriorfossa and the constriction of the right vertebral artery (arrow). An arrow indicates the cut surface of the rim ofthe foramen magnum on each side. The structure above the label is the dural sheath enclosing the spinal cord.

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Vertebrobasilar ar-tery insufficiency in rheumatoid atlantoaxial subluxationz 125

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FIG. 6. Case 2. Left vertebral artery just above themain atheromatous lesion showing lumen occluded bya thrombus undergoing organization and early canali-zation. Verhoeff, x 1.5.

remained in a state of 'coma vigil' until death twoweeks later.Necropsy showed recent infarction symmetrically

in both posterior cerebral artery territories. Inaddition, there were scattered periaqueductal in-farcts throughout the tegmentum of the brain-stem,infarction in the cerebellum bilaterally, and infarc-

A B

tion of the upper cervical cord (Figs 1 and 2). Theodontoid process was displaced to the right and washerniated upwards for a distance of 1 cm throughthe foramen magnum (Figs 3, 4, and 5). As a result,the right vertebral artery was markedly narrowedand constricted in an hourglass fashion between thetip of the odontoid process and the lip of the foramenmagnum. The left vertebral artery was recentlythrombosed in its mid-cervical portion at a site of90%0 atheromatous stenosis (Fig. 6).

Significant general findings in addition to rheuma-toid arthritis were severe bilateral fibrotic lungdisease with silicotic nodules (some showing centralnecrosis), emphysema, nephrosclerosis, right andleft ventricular hypertrophy, and generalized lympha-denopathy.

SUMMARY The suboccipital head pain, muscularweakness, and paraesthesia seem related to themechanical displacement of Cl and C2 vertebrae,causing pressure on the greater occipital nerve andcompression of the cervical cord by the posteriorlydisplaced odontoid process. The clearly isolatedsymptoms of vertigo on head flexion or rotationsuggest brain-stem ischaemia but could alternativelybe explained by odontoid pressure on the medullaoblongata. The history of blackouts, poorly wit-nessed, although likely to be secondary to orthostatichypotension might also reflect intermittent vertebro-basilar artery insufficiency from extrinsic vascularcompression related to AAS. His terminal eventoccurred while in traction on a horizontal Stryker

FIG. 7 Case 2. Diagramillustrating the reduced bloodflow past the atheromatousstenosis on the left side andpast the hourglass constrictionbetween the eccentricallyplaced odontoid process andrim of the foramen magnum onthe right side. A. With thelong axis of the head in ananteroposterior position,without symptoms. B. Vertigooccurred on rotation of thehead to the right side byfurther reducing vertebralbloodflow. C. Thrombosis(lower left) of the left vertebralartery severely reducing flow tobasilar artery. Infarction couldhave been precipitated by

C rotation as in B or could haveoccurred without rotation.OI= reduced flow. El = noflow. *= normal flow.

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Vertebrobasilar artery insufficiency in rheumatoid atlantoaxial subluxation

frame which prevented head flexion but allowed headrotation. Here the pathology would seem to beclearly vascular. The left vertebral artery in theprevious 'stroke-like episode' 30 days earlierprobably thrombosed, giving rise to insufficientbasilar artery blood flow and therefore resulting ininfarction. In the terminal stroke-like episode, theright vertebral artery was probably compressedduring rotational movements further reducing theflow to the basilar artery and leading to an extensionof the infarct (Fig. 7).

DISCUSSION

We feel these two patients with rheumatoidarthritis had paroxysmal symptoms of vertebro-basilar artery insufficiency related to change ofhead position. Both had gross degrees ofinstability and subluxation of their atlantoaxialjoint and, in the second case, there was asignificant degree of upward herniation of theodontoid process into the foramen magnum,pseudobasilar invagination (Martel, 1961).

Review of the literature would suggest thatthe finding of AAS is relatively frequent (Davisand Markley, 1951; Robinson, 1966; Stevenset al., 1971; Smith et al., 1972) but correlatespoorly with neck symptomatology. Smith et al.(1972), in a large series collected over 10 years,found an incidence of 15% in 962 cases andStevens et al. (1971) found an incidence of 25%in 100 successive rheumatoid patients attendingan outpatient clinic. These authors and othershave looked at the frequency of associatedneurological involvement in patients with AAS.Smith et al. (1972) found 13% of those withAAS had evidence of spinal cord or brain-steminvolvement, whereas Stevens et al. (1971)found 'myelopathy' to be present in 66% oftheir patients as judged by a pathological in-crease in deep tendon reflexes. They commentthat limb strength and muscle tone could seldombe tested adequately because of pain or jointdeformity.

Smith et al. (1972) in their paper entitled'Natural history of rheumatoid cervical sub-luxations' found that 10 out of 130 patients withAAS developed neurological involvement overan average follow-up period of seven to eightyears. Of this group, they felt that six developedfeatures compatible with vertebral artery in-volvement but these patients were not studied

by angiograms because the risks were notjustified. Stevens et al. (1971) had one patientwith paroxysmal brain ischaemia on neckflexion. Robinson (1966) reported on 22 patientswith rheumatoid AAS and noted that threepatients had signs of myelopathy. Four otherpatients had symptoms which may be interpretedas ischaemic. Two had what sounded like 'dropattacks' (Sheehan et al., 1960), one had vertigo,nausea, and vomiting associated with rotationof the head, and one had vertigo and blurredvision, also on head rotation.

Crellin et al. (1970) reported on 11 patientswith severe rheumatoid AAS and neurologicalsymptoms who were operated on. Two hadsymptoms of vertebral artery insufficiency,whereas the rest had symptoms of myelopathy.The neurological complications of rheumatoid

AAS usually take the form of a chronic com-pressive myelopathy from a backward slippingof the odontoid process onto the cervical cord.Clinically, these patients will have varyingdegrees of motor weakness, hyperreflexia, andBabinski responses. Sensory signs from this cordlesion are less frequent but patients who do havesymptoms usually describe sensory paraesthesiaon neck flexion. The other neurological syndromewhich we feel these two cases exemplify is that ofbrain-stem ischaemia from vertebral arterycompromise. Admittedly, both had true vertigoon head flexion or rotation which could beinterpreted differently as possibly vestibularend-organ dysfunction; but both had the mechan-ism for impairing vertebral artery flow byincreasing the tortuosity of the vertebral arterywhere it makes a double hairpin turn around thelateral mass of the Cl vertebra and, in effect,causing a dynamic stenosis by attenuating thevessel. Also the second case had severe athero-matous narrowing of his left vertebral artery andan hourglass constriction in the right vertebralartery at the level of the foramen magnum. Hishead on turning to the right would rotate aboutthe odontoid process which would act as afulcrum and therefore pinch off or reducefurther the blood flow through this vessel inview of the abnormal anatomical arrangement(Fig. 7) from the upward herniation of theodontoid process into the foramen magnum.

It has been shown in a cadaver study (Tooleand Tucker, 1960) that physiological changes in

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head position can lead to a reduction in vertebralartery and perhaps carotid blood flow. Similarly,in a human angiographic study (Sheehan et al.,1960) in patients with symptoms of vertebro-basilar artery insufficiency it was also possible toshow a reduced or complete obstruction to bloodflow through the vertebral artery with changes inhead position. The majority of these patientshad together a varying degree of atherosclerosisand cervical spondylosis with osteophytes com-pressing the vertebral artery usually suggestingadditive factors accounting for these symptoms.

The gross dissection was the work of Dr M. J. Ball;Dr Colin Anderson prepared the spinal specimen.

REFERENCES

Chun, C. Kao, Messert, B., Winkler, S. S., and Turner, J. H.(1974). Rheumatoid C1-C2 dislocation: pathogenesis andtreatment reconsidered. Journal of Neurology, Neuro-surgery, and Psychiatry, 37, 1069-1073.

Crellin, R. Q., MacCabe, J. J., and Hamilton, E. B. D. (1970).Severe subluxation of the cervical spine in rheumatoidarthritis. Journal ofBone and Joint Surgery, 52, 244-251.

Davis, F. W., and Markley, H. E. (1951). Rheumatoidarthritis with death from medullary compression. Annalsof Internal Medicine, 35, 451-454.

Martel, W. (1961). The occipito-atlanto-axial joints inrheumatoid arthritis and ankylosing spondylitis. TheAmerican Journal of Roentgenology, 86, 223-240.

Mathew, N. T., and Meyer, J. S. (1974). Pathogenesis andnatural history of transient global amnesia. Stroke, 5,303-311.

Robinson, H. S. (1966). Rheumatoid arthritis-atlanto-axialsubluxation and its clinical presentation. Canadian MedicalAssociation Journal, 94, 470-477.

Sheehan, S., Bauer, R. B., and Meyer, J. S. (1960). Vertebralartery compression in cervical spondylosis. Neurology(Minneap.), 10, 968-985.

Smith, P. H., Benn, R. T., and Sharp, J. (1972). Naturalhistory of rheumatoid cervical luxation. Annals of theRheumatic Diseases, 31, 431-439.

Stevens, J. C., Cartilidge, N. E. F., Saunders, M., Appelby,A., Hall, M., and Shaw, D. A. (1971). Atlanto-axialsubluxation and cervical myelopathy in rheumatoidarthritis. Quarterly Journal of Medicine, 40, 391-408.

Toole, J. B., and Tucker, S. H. (1960). Influence of headposition upon cerebral circulation. Archives of Neurology,2, 616-622.

Webb, F. W S., Hickman, J. A., and Brew, D. St. J. (1968).Death from vertebral artery thrombosis in rheumatoidarthritis. British Medical Journal, 2, 537-538.

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