THE SPECTRUM OF ATLANTOAXIAL FACET JOINT INVOLVEMENT IN RHEUMATOID ARTHRITIS

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1 325 THE SPECTRUM OF ATLANTOAXIAL FACET JOINT INVOLVEMENT IN RHEUMATOID ARTHRITIS JAMES T. HALLA and JOE G. HARDIN, JR. Six hundred fifty outpatients with rheumatoid arthritis (RA) were evaluated and followed up during a 7-year period. As part of their routine evaluation or because of neck-shoulder girdle symptoms, 48% of the patients underwent routine cervical spine radiography. Sixty-one RA patients (9% of the total population) had C142 involvement. Compared with the 589 patients with no evidence of Cl-C2 involvement, these 61 patients were significantly more likely to be younger, female, and seropositive, and they had significantly more nodules and erosions, as well as a longer disease duration. Based on radiographic evidence of C142 disease severity, 3 groups emerged. Group 1 (28 patients) had lateral mass collapse, group 2 (27 patients) had lateral facet joint sclerosis, erosion, or loss of joint space with no collapse, and group 3 (6 patients) had lateral subluxation with no bone or cartilage changes. Nine patients in group 1 had severe pain, and 25 had a nonreducible rotational tilt of the head. None of the patients in the other 2 groups had either of these signs or symptoms. Moreover, patients in group 1 were more likely to have other C142 or subaxial subluxations and were more likely to have myelopathy. C142 lateral facet joint involvement is common in RA, correlates with disease severity generally and specifically with that in the cervical spine, and, when severe, causes nonreducible rotational tilt of the patient s head. ~- - James T. Halla, MU: Abilene, Texas; Joe G. Hardin, Jr., MD: Professor of Medicine, University of South Alabama College of Medicine, Mobile. Address reprint requests to Joe G. Hardin, Jr., MD, University of South Alabama College of Medicine, 2451 Fillingim Street, Mobile, AL Submitted for publication May 18, 1989; accepted in revised form October 25, The atlantoaxial (CI-C2) facet joints are a common site of involvement in patients with rheumatoid arthritis (RA), and a number of derangements resulting from such involvement have been described. These abnormalities include lateral, rotatory, and vertical subluxations and lateral mass collapse (1-1 I). The frequency and spectrum of severity of CLC2 facet joint disease due to RA has been examined in only a relatively small population of hospitalized patients (I). In an effort to better define the frequency, patterns of involvement, and spectrum of severity of rheumatoid C I-C2 facet joint disease, we evaluated 650 consecutive outpatients who fulfilled the American Rheumatism Association (ARA) 1987 revised criteria for the classification of RA (12) and met criteria for inclusion in the study. PATIENTS AND METHODS All patients seen from 1981 through 1988 in one outpatient setting were included in the study if they met the ARA criteria for the classification of RA, had been seen on at least 2 occasions, and had adequate medical history and physical examination data available. The minimum historical and physical examination data required were (a) the presence or absence of neck-shoulder girdle symptoms, (b) if present, the duration, character, and severity of the neckshoulder girdle symptoms, (c) the estimated range of neck motion in 3 planes, and (d) if cervical motion was limited, the presence or absence of abnormal position of the patient s head. In addition, data from routine clinical and laboratory assessments were available for all study subjects, including age, sex, disease duration, results of peripheral joint examinations, presence or absence of subcutaneous nodules, and rheumatoid factor status. Six hundred fifty patients qualified for the study. All patients with neck-shoulder girdle symptoms and/or limited Arthritis and Rheumatism, Vol. 33, No. 3 (March 1990)

326 HALLA AND HARDIN mobility of the cervical spine on physical examination (128 patients) were evaluated radiographically, with at least 2 views of the cervical spine, one with the neck in lateral

2 326 HALLA AND HARDIN mobility of the cervical spine on physical examination (128 patients) were evaluated radiographically, with at least 2 views of the cervical spine, one with the neck in lateral flexion and the other an open-mouth view of Cl-C2. In addition, routine radiographic views of the cervical spine of another 182 patients had been taken as part of their routine evaluation, and these were available for assessment. If there was inadequate visualization of the facet joints on the routine views, multiplanar tomography of the Cl-C2 region was performed. A total of 310 patients (48%) had radiographic studies. The remaining 340 patients were assumed to have no Cl-C2 facet joint disease. Patients were assessed in followup for a mean of 2 years (range 0-6). Neck-shoulder girdle pain severity was graded on the basis of average or typical symptoms during the followup period, and was considered mild, moderate, or severe on the basis of the history. Neck flexion+xtension, rotation, and lateral flexion were estimated in degrees of motion from the neutral position. An abnormal head position (rotational head tilt) was defined clinically, and it usually consisted of both lateral flexion and rotation. Reducibility was determined by the consistent ability (or inability) of the patient and examiner to return the patient s head and neck to the neutral position. Myelopathy was defined by clinical signs and symptoms and was confirmed by evidence of cord compression by an appropriate diagnostic imaging procedure. Radiographs were evaluated for the presence of anterior Cl-C2, vertical, lateral, and subaxial subluxations and for lateral mass collapse. Anterior Cl-C2 subluxation was defined as a distance >3 mm separating the anterior surface of the odontoid from the midpoint of the posterior aspect of the anterior arch of C1, with the head in flexion (lateral view). Vertical subluxation was defined as the distance that the tip of the odontoid extends above a line (McGregor s line) drawn between the hard palate and the most caudal point of the occipital curve (normal 54.5 mm [ 131; lateral view). Lateral subluxation was considered present if the lateral masses of C1 were displaced >2 mm laterally with respect to C2 and the patient s head was not rotated (posteroanterior view). Subaxial subluxation was considered significant if there was >1 mm of forward intervertebral shift (lateral view). Lateral mass collapse was defined as a loss of bone volume of one lateral articular process in comparison with the contralateral side, with accompanying sclerosis (increased bone density), subchondral erosions, and loss of joint space of the lateral facet joints. When both facet joints were involved, loss of bone volume was identified by a lack of symmetry between the more involved side and the less involved side. Three groups of patients were identified on the basis of the severity of the facet joint disease as demonstrated radiographically. Group 1 had severe joint space narrowing and subchondral sclerosis with lateral mass collapse. Group 2 had joint space narrowing and subchondral sclerosis without lateral mass collapse. Group 3 had deformity alone, in the form of lateral subluxation, with no joint space narrowing or subchondral sclerosis. Statistical significance was calculated using the t statistic and the chi-square test with Yates correction. Table 1. General features of the 650 rheumatoid arthritis patients studied, according to the presence or absence of lateral facet joint involvement* Patients with Patients without lateral facet lateral facet joint disease joint disease Feature (n = 61) (n = 589) P Mean age (years) <0.001 Sex (% female) Mean duration of <0.001 disease (years) Rheumatoid factor (% positive) % with rheumatoid nodules % with erosions <0.001 No. (%) of deaths during 11 (18) 58 (10) NS followup period * The mean followup period was 2 years (range 0-6). NS = not significant. RESULTS Of the 128 patients with neck-shoulder girdle signs or symptoms, 53 had normal findings on cervical spine radiographs, and the cause of their signs and symptoms was not established. Fourteen had abnormal radiographic findings, but no evidence of Cl-C2 facet joint disease. Seven of these 14 patients had anterior C 1 x2 subluxation, 2 had subaxial subluxation, and 5 had odontoid erosions. The remaining 61 patients (9% of the total population of 650 patients) had radiographic evidence of Cl-C2 facet joint involvement. None of the 182 asymptomatic patients had Cl-C2 facet joint abnormalities. All but 3 of the 61 patients with Cl-C2 facet joint disease had had neck-shoulder girdle pain at some time during their followup period, and on physical examination, all had limited rotation of the head. Table 1 compares the general disease features of these 61 patients with those of the remaining 589 patients. C 1 x2 facet joint involvement predominated in the patients who had seropositive, longstanding, and severe RA. According to radiographic severity, there were 28 patients in group I, 27 in group 2, and 6 in group 3. The clinical features of these 3 groups are listed in Table 2. Lateral mass collapse was present in 4% of the entire population. Severe pain in the neckshoulder girdle region was present only in the group with lateral mass collapse, as was nonreducible rotational head tilt (NRRHT). No patient in group 1 had

3 Cl-C2 FACET JOINT INVOLVEMENT IN RA 327 Table 2. Clinical features of the 61 rheumatoid arthritis patients with lateral facet joint involvement, according to radiographic severity* Group 1 Group 2 Group 3 (n = 28) (n = 27) (n = 6) Number with neck-shoulder girdle pain Mild Moderate Severe Number with abnormal head position NRRHT deformity Reducible RHT deformity Number with normal head position Number with myelopathy Number of deaths * Group 1 patients had severe joint space narrowing and subchondral sclerosis with lateral mass collapse. Group 2 patients had joint space narrowing and subchondral sclerosis without lateral mass collapse. Group 3 patients had lateral subluxation without joint space narrowing or subchondral sclerosis. NRRHT = nonreducible rotational head tilt. normal head position; however, the tilt was reducible in 3 of them. During the followup period, 6 of the 9 group 1 patients with severe pain underwent cervical fusion. Three of them were subjected to posterior occiputto-c3 fusion because of severe pain alone; the results were excellent. The other 3 patients underwent posterior Cl-C2 fusion because of myelopathy and pain; there was partial relief of the pain and stabilization of the neurologic deficits. NRRHT was present on initial evaluation of 23 of the patients, and in 2 others, it developed in association with worsening of the lateral mass collapse. None of the deaths in group I were directly attributable to the cervical lesion or to the RA. One of the 2 deaths in group 2 was related to rheumatoid vasculitis. The radiographic features of the 61 patients with lateral facet joint disease are shown in Table 3. Of the potentially more serious subluxations (vertical and subaxial), vertical subluxations occurred in group 1 patients only, and subaxial subluxations primarily occurred in this group. Most patients in group 1 had more than one type of subluxation; for example, only 1 of the 12 patients with lateral subluxation had that derangement alone. In group 2, subluxations were usually anterior or were combinations of anterior and lateral. Neck-shoulder girdle pain appeared to wax and wane independently of radiographic changes. Table 3. Radiographic features of the 61 rheumatoid arthritis patients with lateral facet joint involvement, according to radiographic severity* Group 1 Group 2 Group 3 (n = 28) (n = 27) (n = 6) Number (%) with subluxations 21 (75) 11 (41) 6 (100) Anterior 16 (57) 9 (33) 4 (66) Vertical 8 (28) 0 (0) 0 (0) Lateral 12 (43) 4(15) 6(100) Subaxial Number (%) with bilateral facet 8 (28) 16 (57) 2 (7) 5 (18) 0 (0) 0 (0) joint disease * Group 1 patients had severe joint space narrowing and subchondral sclerosis with lateral mass collapse. Group 2 patients had joint space narrowing and subchondral sclerosis without lateral mass collapse. Group 3 patients had lateral subluxation without joint space narrowing or subchondral sclerosis. DISCUSSION We have previously reported similar patterns of Cl-C2 lateral facet joint disease in patients with RA (I,9), ankylosing spondylitis (14), juvenile rheumatoid arthritis (14), and osteoarthritis (15), and in 1 patient with Reiter s syndrome (16), but the frequency and the severity of the involvement seem to be greatest in patients with RA. In another report, lateral mass collapse was identified in 10% of 126 hospitalized patients with RA (I), but lesser degrees of Cl-C2 lateral facet joint disease were not specifically addressed. The patients who had lateral mass collapse had a distinctive clinical syndrome that consisted of occipital pain and tender points, limited head rotation, and NRRHT (1). A 7-year followup of the 24 patients with lateral mass collapse and NRRHT originally studied by us revealed a 54% mortality rate and radiographic worsening in 4 of the surviving patients (unpublished data). This suggests that a poor prognosis is associated with the presence of this lesion. Since few of the deaths in the original or current group could be attributed directly to the cervical lesion, it is likely that severe C 1-C2 disease simply reflects the overall disease severity and the multifactorial mortality known to be associated with this pattern of RA (17). The present report confirms the strong association of severe rheumatoid disease with lateral facet joint involvement, especially in the form of lateral mass collapse. Again, the association of lateral mass collapse and NRRHT was noted. We have also confirmed the tendency for lateral facet joint disease to be unilateral or to predominate on one side. This phenomenon probably accounts for the head tilt, which is always toward the most affected side. Overall, lateral

328 HALLA AND HARDIN facet joint involvement was less common in the outpatient population described here than in the hospitalized population we studied previously (I), and severe involvement in the

4 328 HALLA AND HARDIN facet joint involvement was less common in the outpatient population described here than in the hospitalized population we studied previously (I), and severe involvement in the form of lateral mass collapse was much less frequent in the present study population (4% versus 10%). There appears to be a spectrum of severity of C 1-C2 disease, varying from subluxation alone to severe cartilaginous and bony destruction. It is predominantly the latter that seems to result in severe pain and to accompany other derangements that may lead to myelopathy. While the lateral mass collapse is probably responsible for the head tilt and may account for much of the severe neck pain that accompanies it, the condition may not be directly responsible for injury to the spinal cord. In our 3 patients with myelopathy, cord compression seemed to result from C 1-C2 anterior subluxation in 2 and subaxial subluxation in 1. As might be expected, all 8 patients with vertical subluxation had bilateral lateral mass collapse; 2 of these patients had evidence of cord compression on magnetic resonance imaging studies, although they were asymptomatic. Consequently, lateral mass collapse may not be a neurologic threat unless it is bilateral. Although not observed in the present study population, vertical subluxation has been associated with a high incidence of cord and brain stem injury (lo,ll, 18). In our limited experience, the major indication for surgical fusion that can be directly related to the lateral facet joint disease is severe pain; an occiput-to-c3 fusion procedure (3 patients) was more successful in relieving pain than was Cl-C2 fusion (3 patients), perhaps raising a question about the source of the pain. The C I-C2 derangements addressed here were easily identified from adequate routine posteroanterior and lateral radiographs. When there were technical problems that rendered these routine views inadequate, multiplanar tomography clearly defined the lesions. Rotatory subluxation was the only common Cl-C2 derangement that is not addressed in this report, and it is not easily definable by routine radiographic techniques. It is probably best defined by computed axial tomography (19.20). While most of the deformities themselves are adequately defined by these routine techniques, there consequences in terms of neurologic injury are not; there is therefore a role for magnetic resonance imaging and myelography in subjects suspected of having cord compression (21,22). In patients with established RA, C I-C2 lateral facet joint involvement was common, though more severe patterns involving lateral mass collapse oc- curred in only 4% of our study population. Lateral facet joint disease, especially with osteochondral destruction, appears to correlate strongly with the overall severity of RA. Overall disease severity and poor prognosis have previously been correlated with the need for cervical spine surgery in patients with RA (23). Most patients with lateral mass collapse have a predominantly unilateral lesion that leads to a typical NRRHT deformity. They also have more neck pain and more of the other derangements typically found in the rheumatoid cervical spine. The more severe patterns of Cl-C2 facet joint involvement are strongly associated with severe pain, and severe pain is the major clinical problem that must be addressed in these patients. In this small series, myelopathy was confined to the group of patients with severe Cl-C2 facet joint involvement. REFERENCES 1. Halla JT, Fallahi S, Hardin JG: Nonreducible rotational head tilt and lateral mass collapse: a prospective study of frequency, radiographic findings, and clinical features in patients with rheumatoid arthritis. Arthritis Rheum 25: , Burry HC, Tweed JM, Robinson RG, Howes R: Lateral subluxation of the atlanto-axial joint in rheumatoid arthritis. Ann Rheum Dis 37: , Bunton RW, Grennan DM, Palmer DG: Lateral subluxation of the atlas in rheumatoid arthritis. Br J Radio1 51: , Seignon B, Tellart M, Etienne J, Gougeon J: The lateral atlanto-axial joint involvement in rheumatoid arthritis: report of two cases and review. Semin Hop Paris 55: , Weiner S, Bassett L, Spiegel T: Superior, posterior, and lateral displacement of C1 in rheumatoid arthritis. Arthritis Rheum 25: , Fielding J, Hawkins R: Atlanto-axial rotatory fixation. J Bone Joint Surg 59A:3744, Bogduk N, Major GAC, Carter J: Lateral subluxation of the atlas in rheumatoid arthritis: a case report and post-mortem study. Ann Rheum Dis 43: , Santavirta S, Hopfner-Hallikainen D, Paukku P, Sandelin J, Konttinen YT: Atlantoaxial facet joint arthritis in the rheumatoid cervical spine: a panoramic zonography study. J Rheumatol 15: , Halla JT, Hardin JG: The spectrum of atlanto-axial (C I-C2) facet joint involvement in rheumatoid arthritis (abstract). Arthritis Kheum 3l(suppl 4):S79, Menezes AH, van Gilder JC, Clark CR, El-Khoury G: Odontoid upward migration in rheumatoid arthritis: an

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5 Cl-C2 FACET JOINT INVOLVEMENT IN RA 329 analysis of 45 patients with cranial settling. J Neurosurg , El-Khoury GY, Wener MH, Menezes AH, Dolan KD, Kathol MEH: Cranial settling in rheumatoid arthritis. Radiology 137: , Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SK, Liang MH, Luthra HS, Medsger TA Jr, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT. Wilder KL, Hunder GG: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 3 1 : , McGregor M: The significance of certain measurements of the skull in the diagnosis of basilar impression. Br J Radio1 21: , Halla JT, Hardin JG: Nonreducible fixed rotational head tilt: a study of its clinical and radiographic features in patients with juvenile rheumatoid arthritis. Arch Intern Med 143:471474, Halla JT, Hardin JG Jr: Atlantoaxial (C1-C2) facet joint osteoarthritis: a distinctive clinical syndrome. Arthritis Rheum , Halla JT, Bliznak J, Hardin JG: Involvement of the craniocervical junction in Reiter s syndrome. J Kheumato1 15: , Pinals RS: Survival in rheumatoid arthritis. Arthritis Rheum 30:473475, Smith HP, Challa VR, Alexandcr E Jr: Odontoid compression of the brain stem in a patient with rheumatoid arthritis. J Neurosurg 53: , Braunstein EM, Weissman BN, Seltzer SE, Sosman JL, Wang A-M, Zamani A: Computed tomography and conventional radiographs of the craniocervical region in rheumatoid arthritis: a comparison. Arthritis Rheum 27:2631, Kaufman RL, Glenn WV Jr: Rheumatoid cervical myelopathy: evaluation by computerized tomography with multiplanar reconstruction. J Rheumatol 10:42-54, Breedveld FC, Algra PR, Vielvoye CJ, Cats A: Magnetic resonance imaging in the evaluation of patients with rheumatoid arthritis and subluxations of the cervical spine. Arthritis Rheum 30: , Aisen AM, Martel W, Ellis JH, McCune WJ: Cervical spine involvement in rheumatoid arthritis: MR imaging. Radiology 165: , Saway PA, Blackburn WD, Halla JT, Alarcbn GS: Clinical characteristics affecting survival in patients with rheumatoid arthritis undergoing cervical spine surgery: a controlled study. J Rheumatol 16: , 1989

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Rheumatoid Arthritis and the Cervical Spine Radiology Rounds November 21, 2006 Derek Haaland Laiho et al. Semin Arthritis Rheum. 2004:34;267. Laiho et al. Semin Arthritis Rheum. 2004:34;267. *Shen et al.