Anmals ofthe Rheumatic Diseases 1990; 49: 845-850

Surgery of the rheumatoid cervical spine

R A Johnston, I G Kelly

Patients with rheumatoid disease who areadmitted to hospital will often show radiologicalevidence of the disease process in the cervicalspine.' The atlantoaxial level is most commonlyaffected with subaxial levels being less com-monly involved.2 Only a minority of thesepatients will have neurological symptoms of thiscervical disease, however.

Department ofNeurosurgery, SouthernGeneral Hospital,1345 Govan Road,Glasgow G51 4TFR A JohnstonGlasgow RoyalInfirmary, GlasgowG4 OSFI G KellyCorrespondence to:Mr Johnston.

Pathology and patterns of diseaseThe synovitis of rheumatoid disease can affectthe facet joints, the neurocentral joints ofLuschka, and the synovial joint between theodontoid peg and the transverse ligament of theatlas. It causes destruction of intervertebraldiscs and vertebral bodies and leads to liga-mentous laxity.3 These erosive changes can beshown on plain radiographs as abnormal move-

ment of vertebral bodies, and the clinicalexpression of this depends upon the level anddegree of disease. The synovium can give rise toclinical problems in the absence of abnormalmovement by acting as a space occupying lesioncausing root or spinal cord compression. In1951 Davis and Markley recorded cervicalmyelopathy in 16% of their cases who did notshow any cervical subluxation.4At the atlantoaxial level stretching and

destruction of the transverse part of the cruciateligament complex allows the atlas vertebra tomove forward relative to the axis. This results inthe spinal cord being compressed between theposterior arch of the atlas and the odontoid peg.Disease of the synovial joint between theodontoid process and the atlas vertebra causesan expansion of this joint, leading to anteriorcord compression by the mass of pannus. Insome cases the odontoid process is totallyeroded by the inflammatory reaction. Mostcommonly the atlas moves forward relative tothe axis, but rarely the atlas may move poster-iorly if the distal portion of the odontoid processis completely eroded. Occasionally the anteriorsubluxation can become fixed.The lateral masses of the atlas may collapse

secondary to erosive changes in the atlanto-occipital and atlantoaxial synovial joints. Thisleads to vertical subluxation of the odontoidprocess through the foramen magnum. The tipof the odontoid process, which may be expandedby surrounding pannus, is brought into contactwith the cervicomedullary junction.At subaxial levels anterior subluxation occurs

as the result of facet joint disease and is mostcommonly seen at the C5/6 level, which is thelevel of greatest mobility. Any level may beaffected, however, and it is common to see

several levels showing anterior subluxation in astepwise fashion. Subaxial involvement is con-siderably less common than atlantoaxial rheu-matoid disease.A prospective study by Pellicci et al went

some way towards demonstrating the naturalhistory of atlantoaxial and subaxial rheumatoiddisease.5 Over a five year period they found that80% of their patients showed radiological pro-gression while neurological deterioration occur-red in 36%. Cervical pain showed a tendencyto improve and only 13% of the patients whobegan with radiological evidence of diseasecame to surgical treatment. It seems likely thatall seropositive patients will develop radiologicalchanges in the cervical spine with the passage oftime, but neurological deterioration is not in-evitable. There is poor correlation between thedegree of radiological disease of the cervicalspine and the clinical neurological condition.Patients with relatively severe change on radio-graphs may be asymptomatic, and Pelliccireported that 50% of patients in his study whohad severe subluxation were free fromsymptoms.

Vertical subluxation of the odontoid processis recognised as one of the most serious compli-cations of rheumatoid disease and may affect upto 10% of patients who have cervical spinedisease.6 7 Slatis noted progression of thevertical subluxation during a four year period in12 patients who were treated conservatively, butalso observed that the natural history of verticalsubluxation is poorly understood, which makesevaluation of conservative and operative treat-ment difficult.Not all patients with myelopathy show con-

tinued deterioration and some may be managedwithout surgery. Marks and Sharp, however,found that the use of a cervical collar forpatients with a mild or non-progressive myelo-pathy resulted in seven deaths out of 15 patientswithin six months, though not all of thesedeaths were directly attributable to quadri-paresis.8 Patients who underwent surgicalcervical fusion fared better. Further evidence ofthe poor outcome associated with non-operativemanagement of myelopathy was produced byMeijers et al.9

Clinical featuresRheumatoid compression of the spinal cord ornerve roots results in long tract signs and rootpain. The commonest form of root pain iscaused by anterior subluxation of the atlas uponthe axis leading to suboccipital (C2 root) pain.This can be severe and is usually episodic, being

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provoked by sudden movement. It may occur incombination with a myelopathy, but morecommonly occurs in isolation, although it maypredate spinal cord compression. Posteriorcervical pain or pain referred into the trapeziusand interscapular region are not common withrheumatoid disease as they are in spondyliticdegenerative disease.

It can be very difficult to distinguish betweengait disturbance due to joint disease and thatdue to corticospinal tract compression. Spinalcord rheumatoid disease may give the patient asensation of heaviness or fatigability in the legs.Often the patient has had many years of jointdisease and she 'knows her joints', making itpossible to distinguish between walkingproblems associated with joint inflammationand walking problems due to 'something else'.In the presence of cervical spine rheumatoiddisease this 'something else' is spinal cordinvolvement. Hyperreflexia and extensorplantar responses, ifpresent, confirm the clinicalhistory. Paraesthesia, numbness, and brachialgiausually affect the arms, but sometimes thesesymptoms may be due to peripheral neuropathyassociated with rheumatoid disease. The overalldifficulty in diagnosing a myelopathy was notedby Marks and Sharp, who reported a meandelay of 31 weeks between the first neurologicalsymptoms and the diagnosis of spinal corddisease.8

Radiological assessmentLateral projections of the cervical spine per-formed in flexion and extension (figs 1 and 2)are the most common examinations for showingabnormal movement at the C1-2 level. Conven-tional teaching says that a distance of greaterthan 3 mm between the anterior arch of atlasand the front of the odontoid process isabnormal as is a distance of 3-5 mm between the

Figure I Plain radiographofthe cervical spine inextension.

Figure 2 Plain radiograph ofthe cervical spine inflexionshowing atlantoaxial subluxation.

posterior borders of adjacent subaxial vertebrae.This suggests that the available space for thespinal cord at the level concerned may beinsufficient. The state of the odontoid peg andthe lateral processes can be assessed by 'openmouth' views, though disease of the temporo-mandibular joint can make this difficult. Co-existence of vertical subluxation may concealthe amount of anteroposterior movement at theatlantoaxial level because the broader base ofthe odontoid peg comes to lie opposite theanterior arch of the atlas. The amount ofvertical translocation can be calculated byseveral standard radiological measurements.'0

Plain radiographs provide the clinician with aconsiderable amount of information about thedegree of joint disease and bone position, butany conclusions about compression of the spinalcord or medulla are by implication only. Directevidence of spinal cord compression is obtainedwith contrast enhancement or magnetic reson-ance imaging. Myelography has been largelysuperseded by computed tomography myelo-graphy (CTM) and magnetic resonance imaging(MRI). Both CTM and MRI should be carriedout in flexion and extension positions (fig 3).Computed tomography myelography primarilyshows bone tissue with the water soluble contrastsurrounding the spinal cord. Horizontal sectionsthrough the craniocervical junction to the base ofC2 are very helpful in indicating the amount ofanteroposterior movement and also whether anyrotation of the atlas is present. Sagittal imagesneed to be reconstructed from these horizontalsections, whereas MRI is able to provide images

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Surgery ofthe rheumatoid cervical spine

Figure 3 Computed tomography scan shounng cord compression due to rheumatoid disease ofthe periodontoid mynovialjoint.

in almost any plane required, showing thespinal cord, medulla, inflammatory pannus,and fat pads. Magnetic resonance imaging hasbeen shown to be as accurate as CTM inevaluation of most aspects of rheumatoiddisease at the C1-2 level (figs 4 and 5)." 12

Direct imaging of neurological compressionprovides the basis for a fundamental change insurgical decision making. Santavirta et al indi-cated this when referring to myelography andCT, by stating that it is the compression ofneural tissue rather than the size or amplitude ofbony subluxation which is important. 3 Magneticresonance imagmg permits repeat examinationof patients who may be asymptomatic fromtheir cervical disease, without the necessity forintrathecal contrast, and allows evaluation ofthe progression of their disease. The surgeon no

longer has to assume that reduction of bonysubluxation produces relief of neural compres-sion. With good positional imaging reduction of

Figure 4 Magnetic resonance imaging scan (flexion) showing severe cord compresswn due toatlantoaxial subluxation.

compression can be seen to occur (or not) withflexion or extension, and this will influence thetype of surgery to be carried out.

Indications for surgeryThe generally accepted indications for surgicalintervention are neurological deterioration,which is progressive, and cervical/suboccipitalpain which is not controlled by simplemeans.""'6 A more controversial indication isabnormal movement associated with compres-sion indicated by MRI or CTM which isnevertheless asymptomatic. The question ofprophylactic surgery is difficult to answerbecause of insufficient evidence about neuro-logical and radiological progression. The balanceof opinion at present suggests that surgery cansafely be withheld until neurological featuresdevelop, though these can do so within a veryshort space of time. Patients can progress tosevere quadriparesis within a matter of weeksand one of the problems in identifying thisoptimum window for surgical treatment is thewell known difficulty of observing early signs ofmyelopathy by clinical examination. It isprobably impracticable to follow up everypatient with cervical rheumatoid disease byserial MRI examination, though it is by doingjust this that we will be better able to correlateradiological progression and neurologicaldeterioration.

Operative treatmentATLANTOAXIAL DISEASEIn rheumatoid cervical spine disease the mainproblems are abnormal movement of vertebraeand accumulation of inflammatory tissue, bothof which may lead to compression of the spinalcord or nerve roots. It follows that the principlesof surgical treatment are (a) to bring aboutdecompression of the spinal cord or nerve roots,or both, and (b) to restore structural integrityto the vertebral column. For most of the past 25years posterior cervical fusion has been the mostwidely used operative procedure. This wasadvocated and described by Hamblen,"6Newman and Sweetnam,17 and even today it isprobably the most commonly used surgicaltechnique.Ranawat et al found that the results of

posterior surgical intervention were generallydisappointing.'0 Only 42% of their patientsshowed neurological improvement, while 10%showed evidence of continued deterioration.This was set against an early (less than fourmonths) postoperative mortality of 27%, with afurther mortality of 18% up to two years aftersurgery. In the series reported by Zoma et al itwas found that the operative success rate withposterior surgery was only 57%, including somepatients who underwent two procedures. 14Their early postoperative mortality was 8%.Other reports also suggest that posterior surgeryis not the complete answer to operative manage-ment of cervical rheumatoid disease. 18 19 This isnot really surprising considering the varioustypes and combinations of atlantoaxial sublux-ation and subaxial disease which are beingtreated by variations of one operation.

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Figure 5 Magnetic resonance imaging scan (extension) showing that cord compression is stillpresent even though some bony reduction has occurred. Soft tissue compression due to pannus.

The anterior approach to the clivus-atlas-odontoid region was reported early this cen-tury.20 Until fairly recently it was recognised asa hazardous approach both for the surgeon andthe patient because of the risk of meningitis,wound breakdown, cerebrospinal fluid fistula,poor access, and probably also because ofinadequate instrumentation. More recently, theoperation has been revived and modern technicalimprovements have responded to these earlierproblems, making this a safe procedure.21-23Direct decompression of the cervicomedullaryregion by removal of the odontoid process andassociated pannus is a logical approach to ventralcompression of the spinal cord.The re-emergence of transoral approaches to

the odontoid region has added a new dimensionto surgical management of cervical rheumatoiddisease at the atlantoaxial region. In the mostcommon situation where there is anterior sub-luxation of Cl on C2, and with the less commonvertical subluxation, decompression of thespinal cord/medulla can be achieved by remov-ing the odontoid peg and the surroundingpannus. Where there is vertical subluxation it isalso necessary to remove the lower one third ormore of the clivus. The operation is carried outthrough the contaminated field of the mouthand nasopharynx, but local infections are veryuncommon. This may be attributed to the useof prophylactic antibiotics, but perhaps is morelikely to be due to the good healing properties ofthe well vascularised tissues in this region. Avertical incision is made in the posteriorpharyngeal wall through the constrictor musclesand this brings the surgeon almost immediatelyto the anterior arch of atlas. Increased access ina cranial direction is achieved by retraction orsplitting of the soft palate. With advanced casesof vertical subluxation it is necessary to open thehard palate, though the surgeon may use analternative approach through a maxillotomy.The odontoid process, or what remains of it, isremoved completely, making sure that the tip

end is severed from any remaining ligamentousatuchments. It is often possible to observe theremains of the very lax transverse ligament.Pannus is removed as completely as possible tocomplete the decompression down to themembrana tectora.When the anterior decompression has been

achieved it is usual to carry out a posteriorstabilisation procedure under the same anaes-thetic. This makes for a longer operative proce-dure, but the alternative of a two stage proce-dure implies an interim period of cervicaltraction, which will delay recovery and rehabili-tation. The posterior surgical approach entailsexposure of the suboccipital region to the mid orlower cervical level. Exploration of the arch ofCl will confirm any radiological diagnosis ofposterior cord compression and if necessary awide Cl laminectomy is carried out. When thelateral masses are intact the surgeon may choosebetween an occipital/Cl/C2 or a Cl/C2 fixation/fusion procedure. With vertical subluxation thelateral masses of the atlas are eroded and anoccipitocervical procedure is necessary. Anumber of different methods may be used,including a combination of wire, bone graft,and acrylic cement24 (fig 6) or the technique ofsublaminar wiring with a Ransford loop (fig7).24 Both methods are satisfactory and provideimmediate internal stability to the cervicalspine. Both methods entail occipitocervicalfixation/fusion. Use of wire and bone graft alone(fig 8) will necessitate the use of an externalorthosis until bone fusion has occurred. Theadvantage of the former two methods in provid-ing immediate internal stability is that rehabili-tation may begin on recovery from the operation.

The evidence from current publications andfrom our own experience indicates that thiscombined operation is well tolerated by patients,who are often elderly and frail women. Con-sidering the serious nature of the condition, the

Figure 6 Brattstrom occipito-C2fixation andfusion.

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Surgery ofthe rheumatoid ceruical spine

Figure 7 Occipitocerncalfixation by Ransford loop.

Figure 8 CI-2 wiring with bone graft.

general state of health of these patients, and themajor surgical endeavours needed to correct theproblem, there is an acceptably low morbidityand mortality. Hadley reported two deathswithin nine weeks of surgery in 21 patients.23Most of these patients, however, had only theanterior procedure performed. We have founda similar mortality. Complications such as

pharyngeal wound breakdown, cerebrospinalfluid fistula, and infection do occur, but are

uncommon.Neurological improvement was reported in

90% of surviving patients (mixed pathology,including rheumatoid disease) by Hadley,23though little detail of the improvement was

given. In his early series Crockard foundneurological improvement in 15 of 17 patients,and this rate of improvement has been main-tained (personal communication). These very

encouraging results require more detailedneurological verification to establish the trueposition of transoral decompression surgery foratlantoaxial disease.

SUBAXIAL DISEASEThe surgical treatment of subaxial rheumatoiddisease is perhaps less clearly defined. To datethe most common treatment is posteriorfixation/fusion,'0 though this may not actuallyachieve any significant cord decompression.Anterior cervical decompression alone seems tobe insufficient to stabilise the cervical spine anda combined anterior and posterior operation hasbeen advocated.25 At present there is probablyinsufficient evidence to indicate firmly one formof surgery in preference to another.

Summary of treatmentIn Glasgow we advocate operative treatment forpatients who have rheumatoid cervical spinedisease with neurological deterioration, either asa myelopathy or radiculopathy, which includesintractable suboccipital (C2) pain. Althoughoccasionally noting considerable radiologicalchanges in patients without neurologicalfeatures, we have not as yet taken up the optionof prophylactic cervical surgery. This awaitsfurther information on the natural history andprogress of the disease; accumulation of serialCT and MRI data should help in this respect.Before the days of CT and MRI the term'reduction' referred to bony alignment. Reduc-tion should now refer to neurological compres-sion. When there is cord compression due toatlantoaxial disease, and this does not reduce byextending the cervical spine, we prefer to use acombined transoral decompression and posterioroccipitocervical fusion procedure. When theneural decompression does reduce (usually withextension) then a posterior fusion procedure atC1-2 is used. For vertical subluxation we usethe combined anterior and posterior operationas it is virtually impossible to achieve any bonyreduction, and thereby any neurologicalimprovement, by traction. We feel that simplyholding the spine in the abnormal position isinsufficient. Subaxial disease is at presenttreated by anterior decompression and fusionusing a modified Cloward technique combinedwith posterior fixation.

Technical advances continue to increase therepertoire of surgical procedures available, butwe must not lose sight of the importance ofdecision making before the operation based onsound information about the natural history ofthe disease in the cervical spine.

I Swann M. Surgical treatment of cervical spine in rheumatoidarthritis. Ann Acad Med Singapore 1983; 12: 233-42.

2 Ornilia E, Ansell B M, Swannell A J. Cervical spineinvolvement in patients with chronic arthritis undergoingorthopaedic surgery. Ann Rheum Dis 1972; 31: 364-8.

3 Martel W D. Pathogenesis of cervical discovertebral destruc-tion in rheumatoid arthritis. Arthritis Rheun 1977; 20:1217-25.

4 Davis F W, Markley H E. Rheumatoid arthritis with deathfrom medullary compression. Ann Intern Med 1951; 35:451-61.

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S Pellicci P M, Ranawat C S, Tsairis P, Bryan W J. Aprospective study of rheumatoid arthritis of the cervicalspine. Bone Joint Surg [Am] 1981; 63: 342-50.

6 Davidson R C, Herndon J H. Brain stem compression inrheumatoid arthritis. JAMA 1977; 238: 2633-4.

7 Slatis P, Santavirta S, Sandelin J, Konttinen Y T. Cranialsubluxation of the odontoid process in rheumatoid arthritis.Bone joint Surg [Am] 1989; 71: 189-95.

8 Marks J S, Sharp J. Rheumatoid cervical myelopathy. QMed 1981; 199: 307-19.

9 Meijers K A E, Cats A, Kvemer H P H, Lugendij K W,Onrlee G J, Thomeer R T W M. Cervical myelopathy inrheumatoid arthritis. Clin Exp Rheumatol 1984; 2: 239-45.

10 Ranawat C S, O'Leary P, Pellicci P, Tsairis P, Marchisello P,Dorr L. Cervical spine fusion in rheumatoid arthritis.Bone Joint Surg [Am] 1979; 61: 1003-10.

11 Bundschuh C V, Modic M T, Kearny F, Morris R, Deal C.Rheumatoid arthritis of the cervical spine: surface coil MRimaging. AJNR 1988; 9: 556-71.

12 Beltran J, Caudill J L, Herman L A, et al. Rheumatoidarthritis: MR imaging manifestations. Radiology 1987; 165:153-7.

13 Santavirta S, Kankaanpaa V, Sandelin J, Laasonen E,Konttinen Y T, Slatis P. Evaluation of patients withrheumatoid cervical spine. Scand Rheumatol 1987; 16:9-16.

14 Zoma A, Sturrock R D, Fisher W D, Freeman P, HamblenD L. Surgical stabilisation of the rheumatoid cervical spine.J' Bone Joint Surg [Br] 1987; 69: 8-12.

15 Ferlic D C, Clayton M L, Leidholt J D, Gamble W E.

Surgical treatment of the symptomatic unstable cervicalspine in rheumatoid arthritis. J7 Bone Joint Surg [Am] 1975;57: 349-54.

16 Hamblen D L. Occipito-cervical fusion. 7 Bone Joint Surg[Br] 1967; 49: 33-45.

17 Newman P, Sweetnam D R. Posterior fusion for atlanto-axialsubluxation in rheumatoid arthritis. Bone3oint Surg [Br]1969; 51: 423-8.

18 Cregan J C F. Internal fixation of the unstable rheumatoidcervical spine. Ann Rheum Dis 1966; 25: 242-52.

19 Crellin R Q, MacCabe J J, Hamilton E B D. Severesubluxation of the cervical spine in rheumatoid arthritis.Bone joint Surg [Br] 1970; 52: 244-5 1.

20 Kanavel A B. Bullet located between the atlas and the base ofthe skull: technic of removal through the mouth. SurgicalClinics of Chicago 1917; 1: 361-6.

21 Apuzzo M L J, Weiss M H, Heiden J S. Transoral exposureof the atlanto-axial region. Neurosurgery 1978; 3: 201-7.

22 Crockard H A, Essigman W K, Stevens J M, Pozo J L,Ransford A 0, Kendall B E. Surgical treatment of cervicalcord compression in rheumatoid arthritis. Ann Rheum Dis1985; 44: 809-16.

23 Hadley M N, Spetzler R F, Sonntag V K H. The transoralapproach to the cervical spine. Neurosurg 1989; 71: 16-23.

24 Brattstrom H, Granholm L. Atlanto-axial fusion in rheumatoidarthritis. A new method of fixation with wire and bonecement. Acta Orthop Scand 1976; 47: 619-28.

25 Crockard H A. The transoral approach to the base of thebrain and upper cervical cord. Ann R Coll Surg Engl 1985;67: 321-5.

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