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The Rheumatoid Cervical Spine: Signs of Instability on Plain Cervical Radiographs
Clinical Radiology (2002) 57: 241±249 doi:10.1053/crad.2001.0745, available online at http://www.idealibrary.com on
Review The Rheumatoid Cervical Spine: Signs of Instability on Plain Cervical Radiographs C L A R E J . RO C H E *, B R I A N E . E Y E S {, G R A H A M H . W H I T E H O U S E * *Department of Medical Imaging, University of Liverpool, Liverpool, U.K. and {Department of Radiology, University Hospital Aintree, Liverpool, U.K. Received: 4 September 2000 Revised: 19 January 2001 Accepted: 2 February 2001 The cervical spine is a common focus of destruction from rheumatoid arthritis, second only to the metacarpophalangeal joints. Joint, bone and ligament damage in the cervical spine leads to subluxations which can cause cervical cord compression resulting in paralysis and even sudden death. Because many patients with signi®cant subluxations are asymptomatic, the radiologist plays a key role in recognizing the clinically important clues to instability on plain radiographs of the cervical spine±often dicult in rheumatoid arthritis when the bony landmarks are osteoporotic or eroded. This review focuses on the signs of instability on plain radiographs of the cervical spine, using diagrams and clinical examples to illustrate methods of identifying signi®cant subluxations in rheumatoid arthritis. Roche, C. J., Eyes, B. E. and Whitehouse, G. H. (2002) Clinical Radiology 57, 241±249. # 2002 The Royal College of Radiologists Key words: rheumatoid arthritis spine, arthritis of the spine, radiography of the spine, abnormalities of the atlas and axis.
How Common are Cervical Subluxations in Rheumatoid Arthritis? Cervical subluxations are reported to occur in 43±86% of all patients with rheumatoid arthritis (RA) [1±12]. The severity of cervical spine involvement correlates with the duration and severity of the systemic process [5,6,8,13,14] and is commoner in those with severe destructive peripheral arthritis, nodules and high-titre rheumatoid factor [3,6,7,8,15]. Prospective studies indicate that subluxations begin soon after the onset of rheumatoid disease, with 83% of atlantoaxial subluxations developing within 2 years [3,5]. A study of RA patients having total hip or knee joint replacement showed that 61% had cervical instability. Importantly, approximately 50% of patients with cervical instability due to RA will be asymptomatic [5,8].
What Types Are There? Anterior atlanto-axial subluxation is commonest, accounting for 50±70% of all cervical subluxations in RA [2,5,6,12]. Subaxial subluxation of the lower cervical Author for correspondence and guarantor of study: Dr Brian E. Eyes, Department of Radiology, University Hospital Aintree, Lower Lane, Liverpool L9 7AL, U.K. Fax: 44 (0)151 529 3813. 0009-9260/02/040241+09 $35.00/0
vertebrae is the second commonest form, accounting for 20±25% [2,5]. Basilar invagination is less common (10±15%), but is the most dangerous form of subluxation in RA [1,2,4,11,12,17]. Posterior and rotatory atlanto-axial subluxations are rare [5,18].
Why is it Important? Longitudinal follow-up and autopsy studies indicate that cord compression is the cause of death in 10% of patients with rheumatoid cervical spine involvement and neurological impairment is reported to occur in 11±58% [2,16,19,20,21]. Mechanical compression of the cervical cord or medulla is the most common ®nding at autopsy in these patients, followed by vascular compression involving the basilar, anterior or posterior spinal arteries [16,19,21]. Table 1 ± Summary of risk factors for cord compression . AADI 4 9 mm . PADI 5 14 mm . Basilar invagination, especially if combined with AAS of any degree . Subaxial canal diameter 5 14 mm . Cervical height index 5 2 # 2002 The Royal College of Radiologists
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Fig. 1 ± Diagram of the atlanto-axial joint showing the transverse ligament complex (shaded blue) and the alar ligaments (shaded pink). The asterisk* marks site of attachment of the alar ligament to the occipital condyle (Reproduced, with permission, from Grabb et al. [44]).
A summary of the risk factors for cord compression, described below, is given in Table 1.
What are the Challenges? Many signi®cant cervical subluxations are asymptomatic [2,5,7,8,22] and it is dicult for the clinician to detect signs
Fig. 2 ± Anterior atlanto-axial subluxation. The drawing shows forward subluxation of the atlas on the axis, pannus formation around the odontoid process and osseous erosions. There is compression of the spinal cord between the pannus anteriorly and the posterior arch of the atlas (Reproduced, with permission, from Boden et al. [1]).
of subtle neurological de®cit in a patient with a painful deforming arthritis, who may have muscle atrophy or weakness secondary to the RA or its treatment [2,4,15,23,24]. The radiologist, therefore, plays a key role in recognizing the risk factors for cord compression on plain radiographs of the cervical spine. Osteoporosis or erosion of bony landmarks makes traditional radiographic methods of assessment, such as McGregor's line, dicult to apply. Newer methods of assessment designed for use in the rheumatoid patient are more useful and are outlined below [5,25±31].
Fig. 3 ± Normal cervical spine radiograph demonstrating how the anterior atlanto-dental interval AADI (between open arrows) and the posterior atlanto-dental interval PADI (black arrow heads) are measured.
SIGNS OF INSTABILITY IN THE RHEUMATOID CERVICAL SPINE
Fig. 4 ± Gross anterior atlanto-axial subluxation shown on lateral radiograph of neck in ¯exion. The odontoid is completely eroded. The estimated AADI is 10 mm and the PADI is approximately 9 mm.
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Fig. 6 ± Basilar invagination: coronal view demonstrating how disease in the atlanto-occipital and atlanto-axial joints leads to protrusion of the odontoid into the foramen magnum (reproduced, with permission, from Boden et al. [1]).
Fig. 7 ± McGregor's line: the odontoid tip should not protrude more than 4.5 mm above a line drawn from the upper surface of the posterior edge of the hard palate to the most caudal point of the occiput. Fig. 5 ± Basilar invagination: the skull and C1 have `settled' onto C2 and the odontoid protrudes into the foramen magnum, compressing the spinal cord (Reproduced, with permission, from Boden et al. [1]).
ATLANTO-AXIAL SUBLUXATION (AAS)
Anterior atlanto-axial subluxation is the commonest form, accounting for 50±70% of all cervical subluxations in rheumatoid arthritis [1,2,4,11,12,28,32]. The atlantoaxial joint is unique and complex (Fig. 1). Its principal motion is rotation and it is the most active joint in the body, reported to move about 600 times an hour, awake and asleep [6]. It is perhaps because it is such an active joint that it is so frequently aected by the rheumatoid process. Osteoporosis, synovial joint eusion and proliferation of
synovial tissue combine to destroy the odontoid process as well as the transverse and alar ligaments, resulting in anterior atlanto-axial subluxation (Fig. 2) with concomitant narrowing of the spinal canal. AAS usually develops within 2 years of disease onset [5,6].
How do you Detect Anterior Atlanto-axial Subluxation? The Anterior Atlanto-Dental Interval AAS is de®ned as an anterior atlanto-dental interval (AADI) of greater than 3 mm in adults [33] (Fig. 3). The measurement is made from the posteroinferior margin of the anterior arch of the atlas to the anterior surface of
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Fig. 8 ± Basilar invagination: McGregor's line. The odontoid tip lies 9 mm above McGregor's line, indicating basilar invagination.
Fig. 9 ± Ranawat method: detects settling of C1 on C2, which is the ®rst step in the development of basilar invagination. It measures the distance from the centre of the pedicles (sclerotic ring) of C2 to a line drawn connecting the midpoints of the anterior and posterior arches of C1. Normal values are 15 mm or greater for men and 13 mm or greater for women.
the odontoid [4,33]. An AADI of 3±6 mm indicates early instability and implies transverse ligament damage [4]. An AADI of greater than 6 mm indicates that the alar ligaments (Fig. 1), which act as secondary stabilizers, are also damaged [15]. An AADI of greater than 9 mm (Fig. 4) is considered by some authors to be a clear indication for surgical stabilization [4,34]. Overall, however, there is poor correlation between the AADI and the development of neurological de®cit [1±3].
The Posterior Atlanto-Dental Interval Recent literature suggests that the posterior atlantodental interval (PADI) (Fig. 3) is a better method of
Fig. 10 ± Basilar invagination: Ranawat method. Distance between C2 sclerotic ring and line connecting the centres of the anterior and posterior arches of C1 is 10 mm (lower limit of normal is 13 mm).
Fig. 11 ± Redlund±Johnell method: overcomes the problem of a poorly visualized odontoid by measuring the distance between McGregor's line and the midpoint of the inferior margin of C2. Normal values are 34 mm or greater for men and 29 mm or greater for women.
assessing anterior atlanto-axial subluxation, because the PADI directly measures the spinal canal and therefore shows how much it is narrowed by the subluxation [1,2,4,5]. The PADI is the distance measured between the posterior surface of the odontoid and the anterior margin of the posterior ring of the atlas. At all levels in the cervical spine the spinal cord requires a minimum of 10 mm, the cerebrospinal ¯uid (CSF) 2 mm and the dura 2 mm of space; therefore a minimum PADI of 14 mm is required to avoid cord compression [4,11]. The normal spinal canal sagittal diameter at C1 is 17±29 mm. A PADI of less than 14 mm is a sensitive method of predicting cord compression and paralysis [1,2,5] and a reliable method of identifying high-risk patients who should be further assessed with MR. Radiographs taken in the neutral position will miss 48% of cases of AAS [35]. Controlled ¯exion views should
SIGNS OF INSTABILITY IN THE RHEUMATOID CERVICAL SPINE
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Fig. 12 ± Basilar invagination: Redlund±Johnell method. McGregor's line lies 27 mm from the base of C2 (lower limit of normal for male is 34 mm). Note also anterior atlanto-axial subluxation.
Fig. 13 ± Kauppi method: the distance between the most cranial tip of the superior facets of C2 (top of C2 sclerotic ring) and the arch of C1. Grade I: normal; grade II: inferior margin of C1 arch reaches level of C2 facet (top of sclerotic ring); grade III: midpoint of C1 arch reaches level of C2 facet; grade IV: superior margin of C1 arch reaches level of C2 facet.
therefore always be obtained, particularly considering that up to 50% of patients with AAS are asymptomatic. Sometimes AAS will seem to improve with time, but this apparent improvement is spurious, due to the development of basilar invagination: as C1 descends on C2 as a result of the collapse of the lateral atlanto-axial joints, the anterior arch of C1 will appear closer to the broader base of the odontoid, thus narrowing the AADI [12,36].
Posterior Atlanto-axial Subluxation Posterior subluxation accounts for 7% of rheumatoid subluxations and is associated with a de®cient odontoid [2,5].
Rotatory Atlanto-axial Subluxation Approximately 10% of hospitalized rheumatoid patients were found to have a persisting ®xed rotational head tilt
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Fig. 14 ± Basilar invagination: Kauppi method. (a) Kauppi Grade I: normal cervical spine. (b) Kauppi Grade II: top of C2 sclerotic ring reaches inferior margin of C1 arch. (c) Kauppi Grade III: top of C2 sclerotic ring reaches midpoint of C1 arch. (d) Kauppi Grade IV: top of C2 sclerotic ring reaches superior margin of C1 arch.
deformity [5,6,18]. The deformity is due to unilateral lateral mass collapse.
Lateral subluxation occurs in up to 20% and is de®ned as greater than 2 mm oset of the lateral mass of C1 on C2 on coronal images. It is usually associated with a rotational deformity [2,5,6].
Destruction of the lateral atlanto-axial joints and of the atlanto-occipital joints leads to upward migration of the odontoid and surrounding pannus into the foramen magnum, compressing the brainstem and spinal cord [11,17,34,37] (Figs 5 and 6). BI and AAS frequently coexist [1,5,36] and is a sinister combination. BI is often unrecognized and the radiologist may be the ®rst to suspect it [17].
BASILAR INVAGINATION
How do you Detect Basilar Invagination?
Lateral Atlanto-axial Subluxation
Basilar invagination (BI) is also known as vertical atlanto-axial subluxation, vertical subluxation, atlantoaxial impaction, cranial settling, and superior migration of the odontoid [6,11,17]. It is less common than AAS, occurring in 8±34% of RA patients [1,5,6,17,36], but it is the most sinister and dangerous form [4,11,12,16,17,34,36].
McGregor's Method Traditionally BI has been de®ned as protrusion of the odontoid tip more than 4.5 mm above McGregor's line [25] which is a line drawn from the posterosuperior aspect of the hard palate to the most caudal aspect of the occiput (Figs 7 and 8). However, odontoid erosion and osteoporosis make
SIGNS OF INSTABILITY IN THE RHEUMATOID CERVICAL SPINE
247
Fig. 16 ± Subaxial subluxation: diagram showing how the cervical height index (CHI) is calculated. The distance from the centre of the sclerotic ring of C2 to the tip of the spinous process of C2 (red line) is measured and then divided into the distance from the centre of the sclerotic ring of C2 to the midpoint of the inferior border of C7 vertebral body (green line). A CHI of less than 2 is a sensitive predictor of neurological de®cit. Fig. 15 ± Subaxial subluxation: subaxial subluxations at multiple levels producing a `step-ladder' deformity. Note also anterior atlanto-axial subluxation and an abnormal Redlund±Johnell measurement of 24 mm indicating basilar invagination. Endplate and spinous process erosions are also present at multiple levels.
McGregor's method dicult to apply in patients with RA. There are three other methods that help to overcome this problem: the Ranawat, Redlund±Johnell and Kauppi methods [6,27,29,30,31].
Ranawat Method The Ranawat method (Figs 9 and 10) detects settling of C1 on C2 due to destruction of the lateral atlanto-axial joints, which is the ®rst step in the development of BI [31]. The measurement is made from the centre of the pedicles (sclerotic ring) of C2 to a line connecting the midpoint of the anterior and posterior arches of C1 (Fig. 9). Normal values are 15 mm or greater for men and 13 mm or greater for women.
Redlund±Johnell Method The Redlund±Johnell method (Figs 11 and 12) overcomes the problem of a poorly visualized odontoid. It
measures the distance between McGregor's line and the midpoint of the inferior margin of C2 vertebral body. Normal values for men are 34 mm or greater, and for women 29 mm or greater [26].
Kauppi Method The Kauppi method (Figs 13 and 14) can also be applied with a poorly visualized odontoid and has the advantage that no `measurements' are required ± it relies on observation of how low C1 articulates on C2. Normally the arch of C1 lies well above the superior facets of C2 (top of the sclerotic ring of C2). With collapse of the lateral masses of C1, the arch of C1 descends to a lower position. The Kauppi method is graded as follows: (1) Kauppi Grade I: normal (Fig. 14a). (2) Kauppi Grade II: the top of the C2 sclerotic ring reaches the inferior margin of the arch of C1 (Fig. 14b). (3) Kauppi Grade III: the top of the C2 sclerotic ring reaches the midpoint of the arch of C1 (Fig. 14c). (4) Kauppi Grade IV: the top of the C2 sclerotic ring reaches the superior margin of C1 arch [27]. (Fig. 14d).
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of C2 (as used in the Ranawat method) to the tip of the spinous process of C2. This distance is then divided into the distance from the centre of the C2 sclerotic ring to the midpoint of the inferior border of C7 vertebral body. A CHI of less than 2 is a very sensitive predictor of neurological de®cit [5] (Fig. 16). CONCLUSION
Cervical subluxations are a common and serious complication of rheumatoid arthritis and are often clinically silent. The radiologist plays a key role in recognizing the warning signs on plain radiographs of the cervical spine. Flexion views of the cervical spine should always be included or half of all anterior atlanto-axial subluxations will be missed [35]. Even if plain radiographic measurements are normal it should be remembered that pannus and granulation tissue, invisible on plain radiographs, may compress the cord. MRI is therefore indicated if there is clinical concern [9,10,39±43] (Fig. 17). Acknowledgements. The authors wish to thank Mr Richard Hancock, Medical Illustration Department, University Hospital, Aintree, for the excellent illustrations. REFERENCES
Fig. 17 ± Sagittal T2-weighted MR image of the cervical spine showing extensive pannus around the odontoid process causing cord compression.
SUBAXIAL SUBLUXATION
Subaxial subluxations (SAS) are the second commonest type of subluxation in the rheumatoid cervical spine. The subluxations are due to facet joint arthritis, ligamentous laxity and disc involvement which combine to produce a `step-ladder' deformity of alignment of C2±C7 [5,6] (Fig. 15). Subaxial subluxation is de®ned as greater than 3.5 mm of translation of one vertebral body on another [38]. The diameter of the spinal canal is a better predictor of the development of paralysis than the degree of subluxation of one vertebral body on another [1]. The normal sagittal diameter from C3 to C7 is 14±23 mm [38]. A spinal canal sagittal diameter of at least 14 mm is critical at all levels in the cervical spine [1,38], as this is the minimum space required for cord, CSF and dura. The diameter of the subaxial canal correlates more closely with the development of paralysis than the degree of displacement of one vertebral body on another [1]. The cervical height index (CHI) is a method of assessing SAS which takes into account the contribution of subluxations at multiple levels as well as loss of disc height and bony collapse [5]. The CHI index is calculated by ®rst measuring the distance from the centre of the sclerotic ring
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Review The Rheumatoid Cervical Spine: Signs of Instability on Plain Cervical Radiographs C L A R E J . RO C H E *, B R I A N E . E Y E S {, G R A H A M H . W H I T E H O U S E * *Department of Medical Imaging, University of Liverpool, Liverpool, U.K. and {Department of Radiology, University Hospital Aintree, Liverpool, U.K. Received: 4 September 2000 Revised: 19 January 2001 Accepted: 2 February 2001 The cervical spine is a common focus of destruction from rheumatoid arthritis, second only to the metacarpophalangeal joints. Joint, bone and ligament damage in the cervical spine leads to subluxations which can cause cervical cord compression resulting in paralysis and even sudden death. Because many patients with signi®cant subluxations are asymptomatic, the radiologist plays a key role in recognizing the clinically important clues to instability on plain radiographs of the cervical spine±often dicult in rheumatoid arthritis when the bony landmarks are osteoporotic or eroded. This review focuses on the signs of instability on plain radiographs of the cervical spine, using diagrams and clinical examples to illustrate methods of identifying signi®cant subluxations in rheumatoid arthritis. Roche, C. J., Eyes, B. E. and Whitehouse, G. H. (2002) Clinical Radiology 57, 241±249. # 2002 The Royal College of Radiologists Key words: rheumatoid arthritis spine, arthritis of the spine, radiography of the spine, abnormalities of the atlas and axis.
How Common are Cervical Subluxations in Rheumatoid Arthritis? Cervical subluxations are reported to occur in 43±86% of all patients with rheumatoid arthritis (RA) [1±12]. The severity of cervical spine involvement correlates with the duration and severity of the systemic process [5,6,8,13,14] and is commoner in those with severe destructive peripheral arthritis, nodules and high-titre rheumatoid factor [3,6,7,8,15]. Prospective studies indicate that subluxations begin soon after the onset of rheumatoid disease, with 83% of atlantoaxial subluxations developing within 2 years [3,5]. A study of RA patients having total hip or knee joint replacement showed that 61% had cervical instability. Importantly, approximately 50% of patients with cervical instability due to RA will be asymptomatic [5,8].
What Types Are There? Anterior atlanto-axial subluxation is commonest, accounting for 50±70% of all cervical subluxations in RA [2,5,6,12]. Subaxial subluxation of the lower cervical Author for correspondence and guarantor of study: Dr Brian E. Eyes, Department of Radiology, University Hospital Aintree, Lower Lane, Liverpool L9 7AL, U.K. Fax: 44 (0)151 529 3813. 0009-9260/02/040241+09 $35.00/0
vertebrae is the second commonest form, accounting for 20±25% [2,5]. Basilar invagination is less common (10±15%), but is the most dangerous form of subluxation in RA [1,2,4,11,12,17]. Posterior and rotatory atlanto-axial subluxations are rare [5,18].
Why is it Important? Longitudinal follow-up and autopsy studies indicate that cord compression is the cause of death in 10% of patients with rheumatoid cervical spine involvement and neurological impairment is reported to occur in 11±58% [2,16,19,20,21]. Mechanical compression of the cervical cord or medulla is the most common ®nding at autopsy in these patients, followed by vascular compression involving the basilar, anterior or posterior spinal arteries [16,19,21]. Table 1 ± Summary of risk factors for cord compression . AADI 4 9 mm . PADI 5 14 mm . Basilar invagination, especially if combined with AAS of any degree . Subaxial canal diameter 5 14 mm . Cervical height index 5 2 # 2002 The Royal College of Radiologists
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Fig. 1 ± Diagram of the atlanto-axial joint showing the transverse ligament complex (shaded blue) and the alar ligaments (shaded pink). The asterisk* marks site of attachment of the alar ligament to the occipital condyle (Reproduced, with permission, from Grabb et al. [44]).
A summary of the risk factors for cord compression, described below, is given in Table 1.
What are the Challenges? Many signi®cant cervical subluxations are asymptomatic [2,5,7,8,22] and it is dicult for the clinician to detect signs
Fig. 2 ± Anterior atlanto-axial subluxation. The drawing shows forward subluxation of the atlas on the axis, pannus formation around the odontoid process and osseous erosions. There is compression of the spinal cord between the pannus anteriorly and the posterior arch of the atlas (Reproduced, with permission, from Boden et al. [1]).
of subtle neurological de®cit in a patient with a painful deforming arthritis, who may have muscle atrophy or weakness secondary to the RA or its treatment [2,4,15,23,24]. The radiologist, therefore, plays a key role in recognizing the risk factors for cord compression on plain radiographs of the cervical spine. Osteoporosis or erosion of bony landmarks makes traditional radiographic methods of assessment, such as McGregor's line, dicult to apply. Newer methods of assessment designed for use in the rheumatoid patient are more useful and are outlined below [5,25±31].
Fig. 3 ± Normal cervical spine radiograph demonstrating how the anterior atlanto-dental interval AADI (between open arrows) and the posterior atlanto-dental interval PADI (black arrow heads) are measured.
SIGNS OF INSTABILITY IN THE RHEUMATOID CERVICAL SPINE
Fig. 4 ± Gross anterior atlanto-axial subluxation shown on lateral radiograph of neck in ¯exion. The odontoid is completely eroded. The estimated AADI is 10 mm and the PADI is approximately 9 mm.
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Fig. 6 ± Basilar invagination: coronal view demonstrating how disease in the atlanto-occipital and atlanto-axial joints leads to protrusion of the odontoid into the foramen magnum (reproduced, with permission, from Boden et al. [1]).
Fig. 7 ± McGregor's line: the odontoid tip should not protrude more than 4.5 mm above a line drawn from the upper surface of the posterior edge of the hard palate to the most caudal point of the occiput. Fig. 5 ± Basilar invagination: the skull and C1 have `settled' onto C2 and the odontoid protrudes into the foramen magnum, compressing the spinal cord (Reproduced, with permission, from Boden et al. [1]).
ATLANTO-AXIAL SUBLUXATION (AAS)
Anterior atlanto-axial subluxation is the commonest form, accounting for 50±70% of all cervical subluxations in rheumatoid arthritis [1,2,4,11,12,28,32]. The atlantoaxial joint is unique and complex (Fig. 1). Its principal motion is rotation and it is the most active joint in the body, reported to move about 600 times an hour, awake and asleep [6]. It is perhaps because it is such an active joint that it is so frequently aected by the rheumatoid process. Osteoporosis, synovial joint eusion and proliferation of
synovial tissue combine to destroy the odontoid process as well as the transverse and alar ligaments, resulting in anterior atlanto-axial subluxation (Fig. 2) with concomitant narrowing of the spinal canal. AAS usually develops within 2 years of disease onset [5,6].
How do you Detect Anterior Atlanto-axial Subluxation? The Anterior Atlanto-Dental Interval AAS is de®ned as an anterior atlanto-dental interval (AADI) of greater than 3 mm in adults [33] (Fig. 3). The measurement is made from the posteroinferior margin of the anterior arch of the atlas to the anterior surface of
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Fig. 8 ± Basilar invagination: McGregor's line. The odontoid tip lies 9 mm above McGregor's line, indicating basilar invagination.
Fig. 9 ± Ranawat method: detects settling of C1 on C2, which is the ®rst step in the development of basilar invagination. It measures the distance from the centre of the pedicles (sclerotic ring) of C2 to a line drawn connecting the midpoints of the anterior and posterior arches of C1. Normal values are 15 mm or greater for men and 13 mm or greater for women.
the odontoid [4,33]. An AADI of 3±6 mm indicates early instability and implies transverse ligament damage [4]. An AADI of greater than 6 mm indicates that the alar ligaments (Fig. 1), which act as secondary stabilizers, are also damaged [15]. An AADI of greater than 9 mm (Fig. 4) is considered by some authors to be a clear indication for surgical stabilization [4,34]. Overall, however, there is poor correlation between the AADI and the development of neurological de®cit [1±3].
The Posterior Atlanto-Dental Interval Recent literature suggests that the posterior atlantodental interval (PADI) (Fig. 3) is a better method of
Fig. 10 ± Basilar invagination: Ranawat method. Distance between C2 sclerotic ring and line connecting the centres of the anterior and posterior arches of C1 is 10 mm (lower limit of normal is 13 mm).
Fig. 11 ± Redlund±Johnell method: overcomes the problem of a poorly visualized odontoid by measuring the distance between McGregor's line and the midpoint of the inferior margin of C2. Normal values are 34 mm or greater for men and 29 mm or greater for women.
assessing anterior atlanto-axial subluxation, because the PADI directly measures the spinal canal and therefore shows how much it is narrowed by the subluxation [1,2,4,5]. The PADI is the distance measured between the posterior surface of the odontoid and the anterior margin of the posterior ring of the atlas. At all levels in the cervical spine the spinal cord requires a minimum of 10 mm, the cerebrospinal ¯uid (CSF) 2 mm and the dura 2 mm of space; therefore a minimum PADI of 14 mm is required to avoid cord compression [4,11]. The normal spinal canal sagittal diameter at C1 is 17±29 mm. A PADI of less than 14 mm is a sensitive method of predicting cord compression and paralysis [1,2,5] and a reliable method of identifying high-risk patients who should be further assessed with MR. Radiographs taken in the neutral position will miss 48% of cases of AAS [35]. Controlled ¯exion views should
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245
Fig. 12 ± Basilar invagination: Redlund±Johnell method. McGregor's line lies 27 mm from the base of C2 (lower limit of normal for male is 34 mm). Note also anterior atlanto-axial subluxation.
Fig. 13 ± Kauppi method: the distance between the most cranial tip of the superior facets of C2 (top of C2 sclerotic ring) and the arch of C1. Grade I: normal; grade II: inferior margin of C1 arch reaches level of C2 facet (top of sclerotic ring); grade III: midpoint of C1 arch reaches level of C2 facet; grade IV: superior margin of C1 arch reaches level of C2 facet.
therefore always be obtained, particularly considering that up to 50% of patients with AAS are asymptomatic. Sometimes AAS will seem to improve with time, but this apparent improvement is spurious, due to the development of basilar invagination: as C1 descends on C2 as a result of the collapse of the lateral atlanto-axial joints, the anterior arch of C1 will appear closer to the broader base of the odontoid, thus narrowing the AADI [12,36].
Posterior Atlanto-axial Subluxation Posterior subluxation accounts for 7% of rheumatoid subluxations and is associated with a de®cient odontoid [2,5].
Rotatory Atlanto-axial Subluxation Approximately 10% of hospitalized rheumatoid patients were found to have a persisting ®xed rotational head tilt
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Fig. 14 ± Basilar invagination: Kauppi method. (a) Kauppi Grade I: normal cervical spine. (b) Kauppi Grade II: top of C2 sclerotic ring reaches inferior margin of C1 arch. (c) Kauppi Grade III: top of C2 sclerotic ring reaches midpoint of C1 arch. (d) Kauppi Grade IV: top of C2 sclerotic ring reaches superior margin of C1 arch.
deformity [5,6,18]. The deformity is due to unilateral lateral mass collapse.
Lateral subluxation occurs in up to 20% and is de®ned as greater than 2 mm oset of the lateral mass of C1 on C2 on coronal images. It is usually associated with a rotational deformity [2,5,6].
Destruction of the lateral atlanto-axial joints and of the atlanto-occipital joints leads to upward migration of the odontoid and surrounding pannus into the foramen magnum, compressing the brainstem and spinal cord [11,17,34,37] (Figs 5 and 6). BI and AAS frequently coexist [1,5,36] and is a sinister combination. BI is often unrecognized and the radiologist may be the ®rst to suspect it [17].
BASILAR INVAGINATION
How do you Detect Basilar Invagination?
Lateral Atlanto-axial Subluxation
Basilar invagination (BI) is also known as vertical atlanto-axial subluxation, vertical subluxation, atlantoaxial impaction, cranial settling, and superior migration of the odontoid [6,11,17]. It is less common than AAS, occurring in 8±34% of RA patients [1,5,6,17,36], but it is the most sinister and dangerous form [4,11,12,16,17,34,36].
McGregor's Method Traditionally BI has been de®ned as protrusion of the odontoid tip more than 4.5 mm above McGregor's line [25] which is a line drawn from the posterosuperior aspect of the hard palate to the most caudal aspect of the occiput (Figs 7 and 8). However, odontoid erosion and osteoporosis make
SIGNS OF INSTABILITY IN THE RHEUMATOID CERVICAL SPINE
247
Fig. 16 ± Subaxial subluxation: diagram showing how the cervical height index (CHI) is calculated. The distance from the centre of the sclerotic ring of C2 to the tip of the spinous process of C2 (red line) is measured and then divided into the distance from the centre of the sclerotic ring of C2 to the midpoint of the inferior border of C7 vertebral body (green line). A CHI of less than 2 is a sensitive predictor of neurological de®cit. Fig. 15 ± Subaxial subluxation: subaxial subluxations at multiple levels producing a `step-ladder' deformity. Note also anterior atlanto-axial subluxation and an abnormal Redlund±Johnell measurement of 24 mm indicating basilar invagination. Endplate and spinous process erosions are also present at multiple levels.
McGregor's method dicult to apply in patients with RA. There are three other methods that help to overcome this problem: the Ranawat, Redlund±Johnell and Kauppi methods [6,27,29,30,31].
Ranawat Method The Ranawat method (Figs 9 and 10) detects settling of C1 on C2 due to destruction of the lateral atlanto-axial joints, which is the ®rst step in the development of BI [31]. The measurement is made from the centre of the pedicles (sclerotic ring) of C2 to a line connecting the midpoint of the anterior and posterior arches of C1 (Fig. 9). Normal values are 15 mm or greater for men and 13 mm or greater for women.
Redlund±Johnell Method The Redlund±Johnell method (Figs 11 and 12) overcomes the problem of a poorly visualized odontoid. It
measures the distance between McGregor's line and the midpoint of the inferior margin of C2 vertebral body. Normal values for men are 34 mm or greater, and for women 29 mm or greater [26].
Kauppi Method The Kauppi method (Figs 13 and 14) can also be applied with a poorly visualized odontoid and has the advantage that no `measurements' are required ± it relies on observation of how low C1 articulates on C2. Normally the arch of C1 lies well above the superior facets of C2 (top of the sclerotic ring of C2). With collapse of the lateral masses of C1, the arch of C1 descends to a lower position. The Kauppi method is graded as follows: (1) Kauppi Grade I: normal (Fig. 14a). (2) Kauppi Grade II: the top of the C2 sclerotic ring reaches the inferior margin of the arch of C1 (Fig. 14b). (3) Kauppi Grade III: the top of the C2 sclerotic ring reaches the midpoint of the arch of C1 (Fig. 14c). (4) Kauppi Grade IV: the top of the C2 sclerotic ring reaches the superior margin of C1 arch [27]. (Fig. 14d).
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of C2 (as used in the Ranawat method) to the tip of the spinous process of C2. This distance is then divided into the distance from the centre of the C2 sclerotic ring to the midpoint of the inferior border of C7 vertebral body. A CHI of less than 2 is a very sensitive predictor of neurological de®cit [5] (Fig. 16). CONCLUSION
Cervical subluxations are a common and serious complication of rheumatoid arthritis and are often clinically silent. The radiologist plays a key role in recognizing the warning signs on plain radiographs of the cervical spine. Flexion views of the cervical spine should always be included or half of all anterior atlanto-axial subluxations will be missed [35]. Even if plain radiographic measurements are normal it should be remembered that pannus and granulation tissue, invisible on plain radiographs, may compress the cord. MRI is therefore indicated if there is clinical concern [9,10,39±43] (Fig. 17). Acknowledgements. The authors wish to thank Mr Richard Hancock, Medical Illustration Department, University Hospital, Aintree, for the excellent illustrations. REFERENCES
Fig. 17 ± Sagittal T2-weighted MR image of the cervical spine showing extensive pannus around the odontoid process causing cord compression.
SUBAXIAL SUBLUXATION
Subaxial subluxations (SAS) are the second commonest type of subluxation in the rheumatoid cervical spine. The subluxations are due to facet joint arthritis, ligamentous laxity and disc involvement which combine to produce a `step-ladder' deformity of alignment of C2±C7 [5,6] (Fig. 15). Subaxial subluxation is de®ned as greater than 3.5 mm of translation of one vertebral body on another [38]. The diameter of the spinal canal is a better predictor of the development of paralysis than the degree of subluxation of one vertebral body on another [1]. The normal sagittal diameter from C3 to C7 is 14±23 mm [38]. A spinal canal sagittal diameter of at least 14 mm is critical at all levels in the cervical spine [1,38], as this is the minimum space required for cord, CSF and dura. The diameter of the subaxial canal correlates more closely with the development of paralysis than the degree of displacement of one vertebral body on another [1]. The cervical height index (CHI) is a method of assessing SAS which takes into account the contribution of subluxations at multiple levels as well as loss of disc height and bony collapse [5]. The CHI index is calculated by ®rst measuring the distance from the centre of the sclerotic ring
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