**4. Radiological assessment of the rheumatoid craniocervical junction and atlantoaxial joint**

The most commonly used radiological screening tool in nonspecialist units are x-rays of the cervical spine in maximum flexion and extension. However, many cases of subluxation will only reveal themselves on maximum pain-free flexion and extension views.

Computed tomography (CT) is vital when considering which surgical approach to use when fusing posteriorly with a rod and screw fixation. Anomalies such as anomalous courses of vertebral arteries, the presence of arcuate foramina, a small pars interarticularis of C2, or a small lateral mass of C1 can all be appreciated on review of 3D-reconstruction of contiguous axial images stretching from the inion to C4, with added benefit of being suitable for use also for neuronavigation-aided screw placement (Mayer 2005). Soft tissue windowing allows evaluation of pannus. CT is also the ideal imaging modality for evaluation of rotatory subluxations (Rahimi et al 2003).

Magneitic resonance imaging (MRI) is of particular use when reviewing patients with multilevel rheumatoid involvement or in evaluating cases of cranial settling. When compared with CT, MRI is more accurate in evaluating soft-tissue and pannus. It does however have serious limitations when attempting to evaluate bony anatomy. We have performed dynamic flexion MRIs in the past as suggested by some authors, but haven't found it to be of significantly more use than conventional static MRI (Reijnierse et al 2000) in the majority of cases. It may be suitable for a small number of cases where stability or compression is in doubt. In cases being considered for surgical intervention we advocate xrays, CT, and MR imaging.

No matter which modality is presented to the clinician, he/she must be aware of the various radiographic measurements used when determining cranial settling and atlantoaxial subluxation. However, these measurements are now largely of academic interest, having been replaced in day to day practice by the direct visualisation of the anatomical structures with MRI. Projection of the odontoid peg tip above McRae's Line is considered abnormal, as is projection of the odontoid peg tip more than 3mm past Chamberlain's line. A Ranawat's distance of less than 13mm is also suggestive of cranial settling (Smoker 1994). Whilst the anterior atlantodental interval has been shown to be of great use when assessing non-rheumatoid patients for the presence or absence of spinal cord compression, rheumatoid cases are quite different. In this group of patients the pannus surrounding the odontoid peg can be quite large, and use of the anterior atlantodental interval may in fact underestimate the amount of spinal cord compression. An atlantodental interval of greater than 10mm suggests an incompetent transverse ligament (Dickman et al 1996). The transverse ligament may be lax, as in rheumatoid patients, or may be breached as is more commonly seen in trauma cases (Dickman. et al 1991). The posterior atlantodental interval has been shown to be a greater predictor of space available for cord, and of severity of neurological dysfunction (Boden et al 1993). Posterior atlantodental intervals of 14mm or more are considered to be the lower limit of normal (Oda, et al 1995). Post-operative radiographic images should be interpreted in the setting of such radiographic and craniometric measurements.

The ease of use and ready availability of MRI scanning to directly visualise the neural elements has largely superseded these measurements.

Surgical Considerations of Rheumatoid Disease

**5.3 Axis** 

ligament.

Involving the Craniocervical Junction and Atlantoaxial Vertebrae 279

longus colli muscles and the anterior longitudinal ligament, which contribute to anterolateral flexion and resistance to hyperextension of the cervical spine respectively, are attached to the anterior tubercle found in the midline on the anterior arch. Two important membranes also arise from this portion of the atlas: the anterior atlantooccipital membrane connecting the atlas to the occipital bone, and the anterior atlantoaxial ligament extending from the atlas to the axis immediately inferior. The anterior atlantal arch is usually directly opposed to the odontoid peg of the axis. The lateral masses of the atlas have a mean width of 15mm (Dong et al 2003), providing both an adequate avenue for potential instrumentation by the spine surgeon, and allowing support of the weight of the head. Atlantal lateral masses have both a superior articular facet and an inferior articular facet. These true synovial joints allow articulation with the occipital condyles and the axis respectively. The atlantooccipital joints orientation at caudal angles of 129 degrees from lateral to medial limits the rotation possible, compared with the atlantoaxial joint with a cranially biased angulation of between 130-135 degrees, where much greater rotation is possible (Konig et al 2005). A posterior tubercle is found in the midline posteriorly providing attachment for the rectus capitis and the ligamentum nuchae. The posterior atlantooccipital membrane extends from the superior border of the posterior arch of the atlas, to the anterior surface of the rim of the foramen magnum (Fitzgerald at al 2002).

The axis is formed from five ossification centres: one in the body, one in each vertebral arch, and two in the odontoid process (Lustrin et al 2003) . It acts as a pivot around which the atlas rotates; the odontoid peg which rises perpendicularly from its body, allowing this unique functionality. The pars interarticularis is found directly adjoining the lateral masslaminar junction. Successful placement of C2-pars screws mandates appreciation of the borders of this continuous bony area by the operating surgeon. The atlantoaxial joint is

Fig. 1. The Atlas with the odontoid process being restrained by the transverse atlantal

#### **5. Upper cervical spine anatomy as it applies to screw placement and kinematics in rheumatoid patients**

An in-depth knowledge of the unique anatomy in the region of the craniocervical junction and the atlantoaxial joint is mandatory when assessing neck pain or myelopathy of rheumatoid patients, and especially when considering surgical fixation of the region. The thirty two synovial lined joints of the cervical spine make this region of the body especially susceptible to becoming floridly symptomatic in individuals affected by rheumatoid arthritis. The occipitocervical and atlantoaxial motion segments have different biomechanical properties conferred on them through their bony and ligamentous relationships respectively.

### **5.1 Occipital bone**

The occipital bone extends from the clivus anteriorly to the lambdoid suture posteriorly, it's embryologic origins being four primary cartilaginous centres laid down in the chondrocranium around the foramen magnum, and a fifth membranous element (Shaprio & Robinson 1976). The superior nuchal line serves as a rough guide for the location of the transverse sinus, and the inion, found in the midline along this line, approximates the torcula herophili. The insertion of the semispinalis capitis may be the most accurate landmark for the confluence of the sinuses (Martin et al 2010). Awareness of the presence of these venous structures lurking beneath the surface of the occipital bone is paramount when placing occipital screws to avoid poor screw purchase and a devastating egress of blood if screw removal is attempted (Roberts et al 1998). The occipital bone is thickest in the midline, with the raised osseous keel being an ideal place to position screws of high pull-outstrength, compared with the thinner more inconsistent lateral portions. Safe regions for locating screws close to the occipital keel are 2cm off the midline at the nuchal line, with an 8mm occipital bone depth being usual, this "safe-zone", however, decreases in width from the midline as one approaches the opisthion (Ebraheim et al 1996). The greater occipital nerve of Arnold is found 15mm off the midline, the importance of preservation through a strict subperiosteal surgical approach lying in posterior scalp numbness or neuralgia should the nerve be damaged (Vital et al 1989).

The occipital condyles, which function as skull-base weight-bearing facets, angle medially and inferiorly at average angles of 55 and 117.5 degrees when viewed from behind (Konig et al 2005). These shape of these condyles positioned on either side of the foramen magnum allow the skull articulate with the cervical spine, whilst the angles prevent excessive axial rotation at the craniocervical junction (Noble & Smoker 1996).

#### **5.2 Atlas**

The atlas has its origins in the fourth occipital and first cervical sclerotomes. It is unique among vertebrae in not having a body, is formed from three ossification sites: the anterior arch or centrum, and two neural arches which fuse in later life to become a unified posterior arch, thereby completing the osseous ring which surrounds the spino-medullary junction (Kim et al 2007). An appreciation that this ring is incomplete in up to 5% of patients is important if one is to avoid causing a durotomy or spinal cord injury when approaching the craniocervical junction posteriorly(Torriani & Lourenco 2002, Denaro et al 2010).

The ring of the atlas consists approximately of one-fifth anterior arch, two-fifths posterior arch, with the remaining two-fifths being contributed by the lateral masses (Gray 1918). The longus colli muscles and the anterior longitudinal ligament, which contribute to anterolateral flexion and resistance to hyperextension of the cervical spine respectively, are attached to the anterior tubercle found in the midline on the anterior arch. Two important membranes also arise from this portion of the atlas: the anterior atlantooccipital membrane connecting the atlas to the occipital bone, and the anterior atlantoaxial ligament extending from the atlas to the axis immediately inferior. The anterior atlantal arch is usually directly opposed to the odontoid peg of the axis. The lateral masses of the atlas have a mean width of 15mm (Dong et al 2003), providing both an adequate avenue for potential instrumentation by the spine surgeon, and allowing support of the weight of the head. Atlantal lateral masses have both a superior articular facet and an inferior articular facet. These true synovial joints allow articulation with the occipital condyles and the axis respectively. The atlantooccipital joints orientation at caudal angles of 129 degrees from lateral to medial limits the rotation possible, compared with the atlantoaxial joint with a cranially biased angulation of between 130-135 degrees, where much greater rotation is possible (Konig et al 2005). A posterior tubercle is found in the midline posteriorly providing attachment for the rectus capitis and the ligamentum nuchae. The posterior atlantooccipital membrane extends from the superior border of the posterior arch of the atlas, to the anterior surface of the rim of the foramen magnum (Fitzgerald at al 2002).

#### **5.3 Axis**

278 Rheumatoid Arthritis – Etiology, Consequences and Co-Morbidities

An in-depth knowledge of the unique anatomy in the region of the craniocervical junction and the atlantoaxial joint is mandatory when assessing neck pain or myelopathy of rheumatoid patients, and especially when considering surgical fixation of the region. The thirty two synovial lined joints of the cervical spine make this region of the body especially susceptible to becoming floridly symptomatic in individuals affected by rheumatoid arthritis. The occipitocervical and atlantoaxial motion segments have different biomechanical properties conferred on them through their bony and ligamentous

The occipital bone extends from the clivus anteriorly to the lambdoid suture posteriorly, it's embryologic origins being four primary cartilaginous centres laid down in the chondrocranium around the foramen magnum, and a fifth membranous element (Shaprio & Robinson 1976). The superior nuchal line serves as a rough guide for the location of the transverse sinus, and the inion, found in the midline along this line, approximates the torcula herophili. The insertion of the semispinalis capitis may be the most accurate landmark for the confluence of the sinuses (Martin et al 2010). Awareness of the presence of these venous structures lurking beneath the surface of the occipital bone is paramount when placing occipital screws to avoid poor screw purchase and a devastating egress of blood if screw removal is attempted (Roberts et al 1998). The occipital bone is thickest in the midline, with the raised osseous keel being an ideal place to position screws of high pull-outstrength, compared with the thinner more inconsistent lateral portions. Safe regions for locating screws close to the occipital keel are 2cm off the midline at the nuchal line, with an 8mm occipital bone depth being usual, this "safe-zone", however, decreases in width from the midline as one approaches the opisthion (Ebraheim et al 1996). The greater occipital nerve of Arnold is found 15mm off the midline, the importance of preservation through a strict subperiosteal surgical approach lying in posterior scalp numbness or neuralgia should

The occipital condyles, which function as skull-base weight-bearing facets, angle medially and inferiorly at average angles of 55 and 117.5 degrees when viewed from behind (Konig et al 2005). These shape of these condyles positioned on either side of the foramen magnum allow the skull articulate with the cervical spine, whilst the angles prevent excessive axial

The atlas has its origins in the fourth occipital and first cervical sclerotomes. It is unique among vertebrae in not having a body, is formed from three ossification sites: the anterior arch or centrum, and two neural arches which fuse in later life to become a unified posterior arch, thereby completing the osseous ring which surrounds the spino-medullary junction (Kim et al 2007). An appreciation that this ring is incomplete in up to 5% of patients is important if one is to avoid causing a durotomy or spinal cord injury when approaching the

The ring of the atlas consists approximately of one-fifth anterior arch, two-fifths posterior arch, with the remaining two-fifths being contributed by the lateral masses (Gray 1918). The

craniocervical junction posteriorly(Torriani & Lourenco 2002, Denaro et al 2010).

**5. Upper cervical spine anatomy as it applies to screw placement and** 

**kinematics in rheumatoid patients** 

the nerve be damaged (Vital et al 1989).

**5.2 Atlas** 

rotation at the craniocervical junction (Noble & Smoker 1996).

relationships respectively.

**5.1 Occipital bone** 

The axis is formed from five ossification centres: one in the body, one in each vertebral arch, and two in the odontoid process (Lustrin et al 2003) . It acts as a pivot around which the atlas rotates; the odontoid peg which rises perpendicularly from its body, allowing this unique functionality. The pars interarticularis is found directly adjoining the lateral masslaminar junction. Successful placement of C2-pars screws mandates appreciation of the borders of this continuous bony area by the operating surgeon. The atlantoaxial joint is

Fig. 1. The Atlas with the odontoid process being restrained by the transverse atlantal ligament.

Surgical Considerations of Rheumatoid Disease

with the anterior atlantooccipital membrane.

assume that the transverse ligament is not intact.

Involving the Craniocervical Junction and Atlantoaxial Vertebrae 281

ligamentum flavum between the atlas and axis, and the ligamentum nuchae, and the intrinsic group which consists of the tectorial membrane, the accessory atlantoaxial ligament, the cruciate ligament, the odontoid apical and alar ligaments, and the anterior atlanto-occipital membrane. Our discussion will focus primarily on the intrinsic group due

The apical ligament is found in the midline between the anterior atlanto-occipital membrane, has a triangular shape and extends from the tip of the odontoid peg to the anterior most lip of the foramen magnum (Tubbs et al 2000). Though reported to be absent in up to 20% of cadaveric case series, its absence or laxity is not thought to be of functional or structural significance if such abnormality occurs in isolation. The Ligament of Barkow (Tubbs et al 2010) present in 92% of studied cases inserts anterior to the alar ligaments and is often adhered to the anterior atlantooccipital membrane. Its primary function is thought to be in resisting extension of the atlantooccipital joint, acting synergistically to achieve this

The cruciform ligament is composed of both a longitudinal part (running from upper surface of the clivus to the posterior surface of the body of the axis) and a transverse part (running between the medial sides of the lateral masses of the atlas) arching behind the odontoid peg (Debernardi et al 2011). It's thickness of 2.5mm accounts for its reputation as the strongest ligament in the entire spine (failure strength of 350N), and is composed almost exclusively of collagen fibres arranged in a special lattice arrangement (Miyamoto et al, 2004, Dvorak et al 1988). This ligament functions as the major stabiliser of the atlas, tightly constraining the odontoid peg against the ring of the atlas, thus allowing axial rotation and lateral bending of the C1/C2 junction, whilst restricting flexion. When reviewing trauma radiographs or sagittal MRIs if an increase in the anterior atlantodental space above 3mm is noted, or reduction of the posterior atlantodental distance below 13mm, the clinician must

A pair of alar V-shaped ligaments run from the upper one-third of the dens, where the origin is quite narrow, laterally to insert more broadly on the lateral masses of C1 & the occiput. The mainly horizontal alignment of the collagen fibres and their failure strength at about 200N allow them to restrict axial rotation in the craniocervical junction. The left alar ligament restricts axial rotation to the right, and vice-versa. The tensile strength of the alar

The importance of the great strength of these ligaments is clear when one considers that an intact dorsal ring of the atlas is not required for stability. Instead an intact ventral ring of atlas and intact transverse and alar ligaments suffice for stability at the atlantoaxial junction. The tectorial membrane is a cranial extension of the posterior longitudinal ligament running from the axis body to the basilar groove of the occipital bone. The central portion of the membrane merges with the dura mater, whilst the lateral portions merge with Arnold's ligaments (Tubbs 2007). A higher proportion of elastic fibres compared with other previously discussed ligaments account for its lack of tensile strength & its minimal

The accessory atlantoaxial ligament runs from the lateral mass of the atlas to the dorsal aspect of the body of the axis and to the occiput. Differences remain in the literature regarding whether this ligament is a part of or separate to Arnold's ligament (Tubbs 2004, Brolin & Halldin 2004). It is thought to play an important role in restricting craniocervical

ligaments account for the forced coupled rotation of the axis during lateral rotation.

contribution toward the stability of the craniocervical junction.

rotation.

to their importance in appreciating instability in cases of rheumatoid arthritis.

usually angled 35 degrees oblique in the coronal plane, thereby allowing a consistently safe trajectory stretching from the caudal aspect of the lamina of the axis, through the pars interarticularis of the axis into the atlantoaxial joint, finishing in the lateral mass of the atlas. Pre-operative confirmation of the course of the vertebral artery prior to undertaking any such screw placement will be stressed later in the chapter.

#### **5.4 The vertebral artery**

The vertebral artery ascends rostrally through the foramina tranversaria from C6 to C2. Prior to entering the foramen at C2 the artery passes under the pars of C2 where it is vulnerable to injury from placement of C2 OR C1/C2 screws, The vertebral artery exits the superior aspect of the axis, and then passes laterally, to pass through the C2 foramen The vessel at this stage courses posteromedially over the superior aspect of the atlas, where it is vulnerable to injury from overly aggressive dissection by an inexperienced surgeon, before piercing the dura close to the midline and coursing cephalad to the foramen magnum. The left vertebral artery is deemed dominant in 35% of patients, whereas the right side is dominant in 23%. Equivalent vertebral arteries are present in 41% of cases (Menendez & Wright 2007, Tokuda et al 1985). . Particularly in rheumatoid patients the vertebral artery groove is variable in diameter and may encroach sufficiently on the C2 pars to render safe placement of C2 screws impossible.

Fig. 2. The anatomy of the vertebral artery during its course from the C3 transverse process to its entry into the spinal dural canal at the level of C1

#### **5.5 Ligaments**

The osseous structures described in detail above articulate with each other through synovial joints, muscles, ligaments, and membranes. The slowly destructive process of rheumatoid arthritis is wrought on all of these, but it's effects on the regions ligaments are probably the most important of all. A thorough understanding of the role that ligaments play in providing both flexibility & stability to the upper cervical spine is of vital importance when considering whether a patient would benefit from internal fixation, and also when deciding on the optimum approach to be used. The ligaments of the craniovertebral junction may be broadly divided into an extrinsic group consisting of fibroelastic membranes, the

usually angled 35 degrees oblique in the coronal plane, thereby allowing a consistently safe trajectory stretching from the caudal aspect of the lamina of the axis, through the pars interarticularis of the axis into the atlantoaxial joint, finishing in the lateral mass of the atlas. Pre-operative confirmation of the course of the vertebral artery prior to undertaking any

The vertebral artery ascends rostrally through the foramina tranversaria from C6 to C2. Prior to entering the foramen at C2 the artery passes under the pars of C2 where it is vulnerable to injury from placement of C2 OR C1/C2 screws, The vertebral artery exits the superior aspect of the axis, and then passes laterally, to pass through the C2 foramen The vessel at this stage courses posteromedially over the superior aspect of the atlas, where it is vulnerable to injury from overly aggressive dissection by an inexperienced surgeon, before piercing the dura close to the midline and coursing cephalad to the foramen magnum. The left vertebral artery is deemed dominant in 35% of patients, whereas the right side is dominant in 23%. Equivalent vertebral arteries are present in 41% of cases (Menendez & Wright 2007, Tokuda et al 1985). . Particularly in rheumatoid patients the vertebral artery groove is variable in diameter and may encroach sufficiently on the C2 pars to render safe

Fig. 2. The anatomy of the vertebral artery during its course from the C3 transverse process

The osseous structures described in detail above articulate with each other through synovial joints, muscles, ligaments, and membranes. The slowly destructive process of rheumatoid arthritis is wrought on all of these, but it's effects on the regions ligaments are probably the most important of all. A thorough understanding of the role that ligaments play in providing both flexibility & stability to the upper cervical spine is of vital importance when considering whether a patient would benefit from internal fixation, and also when deciding on the optimum approach to be used. The ligaments of the craniovertebral junction may be broadly divided into an extrinsic group consisting of fibroelastic membranes, the

to its entry into the spinal dural canal at the level of C1

**5.5 Ligaments** 

such screw placement will be stressed later in the chapter.

**5.4 The vertebral artery** 

placement of C2 screws impossible.

ligamentum flavum between the atlas and axis, and the ligamentum nuchae, and the intrinsic group which consists of the tectorial membrane, the accessory atlantoaxial ligament, the cruciate ligament, the odontoid apical and alar ligaments, and the anterior atlanto-occipital membrane. Our discussion will focus primarily on the intrinsic group due to their importance in appreciating instability in cases of rheumatoid arthritis.

The apical ligament is found in the midline between the anterior atlanto-occipital membrane, has a triangular shape and extends from the tip of the odontoid peg to the anterior most lip of the foramen magnum (Tubbs et al 2000). Though reported to be absent in up to 20% of cadaveric case series, its absence or laxity is not thought to be of functional or structural significance if such abnormality occurs in isolation. The Ligament of Barkow (Tubbs et al 2010) present in 92% of studied cases inserts anterior to the alar ligaments and is often adhered to the anterior atlantooccipital membrane. Its primary function is thought to be in resisting extension of the atlantooccipital joint, acting synergistically to achieve this with the anterior atlantooccipital membrane.

The cruciform ligament is composed of both a longitudinal part (running from upper surface of the clivus to the posterior surface of the body of the axis) and a transverse part (running between the medial sides of the lateral masses of the atlas) arching behind the odontoid peg (Debernardi et al 2011). It's thickness of 2.5mm accounts for its reputation as the strongest ligament in the entire spine (failure strength of 350N), and is composed almost exclusively of collagen fibres arranged in a special lattice arrangement (Miyamoto et al, 2004, Dvorak et al 1988). This ligament functions as the major stabiliser of the atlas, tightly constraining the odontoid peg against the ring of the atlas, thus allowing axial rotation and lateral bending of the C1/C2 junction, whilst restricting flexion. When reviewing trauma radiographs or sagittal MRIs if an increase in the anterior atlantodental space above 3mm is noted, or reduction of the posterior atlantodental distance below 13mm, the clinician must assume that the transverse ligament is not intact.

A pair of alar V-shaped ligaments run from the upper one-third of the dens, where the origin is quite narrow, laterally to insert more broadly on the lateral masses of C1 & the occiput. The mainly horizontal alignment of the collagen fibres and their failure strength at about 200N allow them to restrict axial rotation in the craniocervical junction. The left alar ligament restricts axial rotation to the right, and vice-versa. The tensile strength of the alar ligaments account for the forced coupled rotation of the axis during lateral rotation.

The importance of the great strength of these ligaments is clear when one considers that an intact dorsal ring of the atlas is not required for stability. Instead an intact ventral ring of atlas and intact transverse and alar ligaments suffice for stability at the atlantoaxial junction.

The tectorial membrane is a cranial extension of the posterior longitudinal ligament running from the axis body to the basilar groove of the occipital bone. The central portion of the membrane merges with the dura mater, whilst the lateral portions merge with Arnold's ligaments (Tubbs 2007). A higher proportion of elastic fibres compared with other previously discussed ligaments account for its lack of tensile strength & its minimal contribution toward the stability of the craniocervical junction.

The accessory atlantoaxial ligament runs from the lateral mass of the atlas to the dorsal aspect of the body of the axis and to the occiput. Differences remain in the literature regarding whether this ligament is a part of or separate to Arnold's ligament (Tubbs 2004, Brolin & Halldin 2004). It is thought to play an important role in restricting craniocervical rotation.

Surgical Considerations of Rheumatoid Disease

beyond the normal limits.

poorer outcome (Sherk 1978).

mass.

Involving the Craniocervical Junction and Atlantoaxial Vertebrae 283

flexion-extension at the same joint), and is limited by the atlanto-condylar joint angulation and also by the alar ligaments (Panjabi et al 1988, Bogduk & Mercer 2000, Steinmetz et al 2010). The atlantoaxial joints on the other hand allow significant axial rotation due to the biconvex nature of the joint. Much less flexion is possible at the atlantoaxial joint compared to the occipitocervical joint due to the presence of the transverse ligament (Dvorak et al 1988), whilst extension is limited by the tectorial membrane and the atlantoaxial joint structure itself. Anterior sagittal translation of C1 on C2 is resisted by a combination of the transverse ligament, the alar and capsular ligaments, with the main resisting strength coming from the former (Dvorak et al 1987, Panjabi at al 1991). In the non-pathological state,

Significant compromise of the integrity of the transverse ligament-odontoid peg unit is commonly seen in the rheumatoid arthritis patient. Enzymatic degradation causing erosion of the odontoid process have been shown to occur (Scutellario & Orzincolob 1988, Mancur & Williams 1995), a biomechanical process of osteolysis occurring at the odontoid peg base which also causes bony resorption. This phenomenon, consistent with Wolff's Law, occurs in rheumatoid patients due to transverse ligament laxity resulting in significant odontoid peg stress reduction and resultant localised osteopenia (Puttlitz et al 2000). This ligamentous laxity-odontoid osteopenia cycle results in the commonly seen atlantoaxial instability in rheumatoid patients. Puttlitzz's study (Puttlitz et al 2000) of a validated fully threedimensional finite element model of rheumatoid development and progression also suggests a biomechanical mechanism underlying the resorption of lateral masses of rheumatoid atlases. An alteration in the contact force data, resulting in an unloading of the lateral aspects of the atlantoaxial and occipitoatlantal joints will result in localised resorption and osteopenia. The decreased articular joint force transmission is compensated to some extent at least by increased loading of the capsular ligaments, resulting over time in capsular ligamentous laxity through direct mechanical stretching of the capsule fibres. Much greater flexion-extension motion is allowed at an atlantoaxial joint with severe transverse ligamentous laxity, further eroding the lateral joint surfaces through joint range movement

Whilst atlantoaxial ventral sagittal subluxation is a relatively early development in rheumatoid arthritis, cranial subluxation tends to occur at a much later stage (Slatis et al 1989). Ligamentous laxity can on its own result in ventral subluxation, whereas osseous destruction is required in addition to earlier ligamentous derangement, to cause cranial subluxation. A partial collapse of the atlantoaxial facet-joint complexes results in a cranial subluxation of the odontoid process into the foramen magnum. This process of progressive contact of the odontoid peg with the medulla is known as cranial settling when occurring as a result of rheumatoid disease (El-Khoury et al 1980). Identification of the onset of cranial settling is especially important, as it serves as a surrogate marker for patients prone to

Lateral atlantoaxial subluxation occurs in 20% of cases of documented rheumatoid subluxation at the C1-C2 level (Lipson 1984), and is a clear indicator of asymmetric destruction of an atlantoaxial joint. Differing degrees of bone loss result in differing ranges of lateral subluxation. A limit of 2.5mm atlantal lateral subluxation is possible with 1mm loss of atlantal lateral mass or C2 articular surface subchondral bone, whereas if the bone loss depth increases more than 1mm, the lateral slippage can reach up to 5mm, being stopped at this limit only by the odontoid peg reaching the medial surface of the atlas lateral

adult anterior sagittal translation is limited to 3mm at most (Hung 2010).

Fig. 3. (a) and (b): The ligaments of the craniocervical junction

(a) Sagittal view showing the posterior longitudinal ligament continuing rostrally as the tectorial membrane

(b) View of the cruciate ligament and alar ligaments, the main stabilisers of the craniocervical junction

#### **5.6 Nerves & their role in causing pain assoc with RA**

The greater occipital nerve is the name by which the medial branch of the dorsal primary ramus of the second cervical spinal nerve is better known by. It arises between the atlas and axis, passing between the inferior oblique and semispinalis capitis muscles, through the trapezius muscle, before innervating the posterior scalp. The lesser occipital nerve innervates the lateral scalp posterior to the ear, and is composed of fibres from both the second and third cervical nerves. Occipital neuralgia refers to sharp, shooting pain arising at back of the head or upper neck, and spreading either to the top of the skull, or to the temple region. It may be present bilaterally, and arises usually in rheumatoid patients due to atlantoaxial subluxation or to C2 nerve root impingement by thickened ligaments. Published series have reported incidence rates as high as 30% in rheumatoid patients (Conroy et al 2010). C1 lateral mass screws have been reported as being an iatrogenic cause of such a syndrome also, and needs to be considered in the post-operative period (Conroy et al 2010). The use of nerve stimulators have been associated with a mean reduction of 96% on the visual analogue score (Magown et al 2009), and are the treatment of choice in our institution (in the absence of atlantoaxial instability) post-successful diagnostic occipital nerve blocks.

#### **6. Biomechanics of the upper cervical joints and the influence of rheumatoid changes on joint kinesiology**

The atlantooccipital joint's main motion is one of flexion-extension of the head. Extension is limited by the tectorial membrane, and flexion is limited in turn by the dens meeting the foramen magnum lip. Lateral bending averages 4 degrees per side (one-sixth that possible in

(a) Sagittal view showing the posterior longitudinal ligament continuing rostrally as the

(b) View of the cruciate ligament and alar ligaments, the main stabilisers of the

The greater occipital nerve is the name by which the medial branch of the dorsal primary ramus of the second cervical spinal nerve is better known by. It arises between the atlas and axis, passing between the inferior oblique and semispinalis capitis muscles, through the trapezius muscle, before innervating the posterior scalp. The lesser occipital nerve innervates the lateral scalp posterior to the ear, and is composed of fibres from both the second and third cervical nerves. Occipital neuralgia refers to sharp, shooting pain arising at back of the head or upper neck, and spreading either to the top of the skull, or to the temple region. It may be present bilaterally, and arises usually in rheumatoid patients due to atlantoaxial subluxation or to C2 nerve root impingement by thickened ligaments. Published series have reported incidence rates as high as 30% in rheumatoid patients (Conroy et al 2010). C1 lateral mass screws have been reported as being an iatrogenic cause of such a syndrome also, and needs to be considered in the post-operative period (Conroy et al 2010). The use of nerve stimulators have been associated with a mean reduction of 96% on the visual analogue score (Magown et al 2009), and are the treatment of choice in our institution (in the absence of atlantoaxial instability) post-successful

**6. Biomechanics of the upper cervical joints and the influence of rheumatoid** 

The atlantooccipital joint's main motion is one of flexion-extension of the head. Extension is limited by the tectorial membrane, and flexion is limited in turn by the dens meeting the foramen magnum lip. Lateral bending averages 4 degrees per side (one-sixth that possible in

Fig. 3. (a) and (b): The ligaments of the craniocervical junction

**5.6 Nerves & their role in causing pain assoc with RA** 

tectorial membrane

craniocervical junction

diagnostic occipital nerve blocks.

**changes on joint kinesiology** 

flexion-extension at the same joint), and is limited by the atlanto-condylar joint angulation and also by the alar ligaments (Panjabi et al 1988, Bogduk & Mercer 2000, Steinmetz et al 2010). The atlantoaxial joints on the other hand allow significant axial rotation due to the biconvex nature of the joint. Much less flexion is possible at the atlantoaxial joint compared to the occipitocervical joint due to the presence of the transverse ligament (Dvorak et al 1988), whilst extension is limited by the tectorial membrane and the atlantoaxial joint structure itself. Anterior sagittal translation of C1 on C2 is resisted by a combination of the transverse ligament, the alar and capsular ligaments, with the main resisting strength coming from the former (Dvorak et al 1987, Panjabi at al 1991). In the non-pathological state, adult anterior sagittal translation is limited to 3mm at most (Hung 2010).

Significant compromise of the integrity of the transverse ligament-odontoid peg unit is commonly seen in the rheumatoid arthritis patient. Enzymatic degradation causing erosion of the odontoid process have been shown to occur (Scutellario & Orzincolob 1988, Mancur & Williams 1995), a biomechanical process of osteolysis occurring at the odontoid peg base which also causes bony resorption. This phenomenon, consistent with Wolff's Law, occurs in rheumatoid patients due to transverse ligament laxity resulting in significant odontoid peg stress reduction and resultant localised osteopenia (Puttlitz et al 2000). This ligamentous laxity-odontoid osteopenia cycle results in the commonly seen atlantoaxial instability in rheumatoid patients. Puttlitzz's study (Puttlitz et al 2000) of a validated fully threedimensional finite element model of rheumatoid development and progression also suggests a biomechanical mechanism underlying the resorption of lateral masses of rheumatoid atlases. An alteration in the contact force data, resulting in an unloading of the lateral aspects of the atlantoaxial and occipitoatlantal joints will result in localised resorption and osteopenia. The decreased articular joint force transmission is compensated to some extent at least by increased loading of the capsular ligaments, resulting over time in capsular ligamentous laxity through direct mechanical stretching of the capsule fibres. Much greater flexion-extension motion is allowed at an atlantoaxial joint with severe transverse ligamentous laxity, further eroding the lateral joint surfaces through joint range movement beyond the normal limits.

Whilst atlantoaxial ventral sagittal subluxation is a relatively early development in rheumatoid arthritis, cranial subluxation tends to occur at a much later stage (Slatis et al 1989). Ligamentous laxity can on its own result in ventral subluxation, whereas osseous destruction is required in addition to earlier ligamentous derangement, to cause cranial subluxation. A partial collapse of the atlantoaxial facet-joint complexes results in a cranial subluxation of the odontoid process into the foramen magnum. This process of progressive contact of the odontoid peg with the medulla is known as cranial settling when occurring as a result of rheumatoid disease (El-Khoury et al 1980). Identification of the onset of cranial settling is especially important, as it serves as a surrogate marker for patients prone to poorer outcome (Sherk 1978).

Lateral atlantoaxial subluxation occurs in 20% of cases of documented rheumatoid subluxation at the C1-C2 level (Lipson 1984), and is a clear indicator of asymmetric destruction of an atlantoaxial joint. Differing degrees of bone loss result in differing ranges of lateral subluxation. A limit of 2.5mm atlantal lateral subluxation is possible with 1mm loss of atlantal lateral mass or C2 articular surface subchondral bone, whereas if the bone loss depth increases more than 1mm, the lateral slippage can reach up to 5mm, being stopped at this limit only by the odontoid peg reaching the medial surface of the atlas lateral mass.

Surgical Considerations of Rheumatoid Disease

raising the risk of inevitable surgical intervention.

compromise on MRI imaging.

**arthrodesis** 

Involving the Craniocervical Junction and Atlantoaxial Vertebrae 285

progressing to basilar invagination. Early intervention in these cases may obviate the need for later trans-oral decompression, a much more invasive procedure (Crockard et al 1986). Each case needs individual consideration both of the risks associated with surgical intervention, and also with the substantial risk of neurological compromise and mortality associated with conservative non-operative management (Sunchara et al 1997). Our practice advocates aggressive surgical management of such cases, in the belief that delaying intervention only places patients with impending neurological deficits at an unacceptably high risk of neurological compromise (Matsunaga et al 1976, Pellicci et al 1981, Casey et al 1996), whilst the patient's overall medical condition and mobility deteriorates, thereby

Identification of asymptomatic patients likely to progress to neurological deterioration without arthrodesis relies on the experienced spine surgeon liaising with his rheumatology colleagues, and facilitating quick decompression and stabilisation should signs of early myelopathy become apparent. An atlantoaxial dental interval of greater than 10mm is certainly an indication for surgical intervention (Rana et al 1973), though intervals between the 5mm and 10mm need to be considered in the setting for the potential for progression to neurological dysfunction. Conventional trauma-based measurements cannot be extrapolated to rheumatoid patients, given that 5mm AADI is often seen in rheumatoid spines, as opposed to the 3mm limit of normal in unaffected adult individuals (Oda et al 1991, Shen et al 2004). We routinely favour the use of the posterior atlantodental interval as a more accurate screening mechanism for such patients, using a cut-off of 14mm as favoured by Boden et al, to stratify those at high risk of impending neural damage (Boden et al 1993). However, in our opinion, the overriding radiological measure is the presence of significant

**8. Peri-operative considerations in rheumatoid patients undergoing** 

(Maury et al 1988, Wimmer et al 1998, Carpenter et al 1996).

A complete assessment of the patient by an internal medicine physician and an anaesthetist is vital prior to the patient undergoing general anaesthesia. Cardiological manifestations such as pericarditis, arrhymthmias, and valvular incompetence occur at much greater incidence in this cohort when compared with their peers (Conlon et al 1966, Del Rincón. et al 2001). Similarly rheumatoid patients have twice the mortality rate from pulmonary disease (Gonzolez–Juanatey et al 2003). We do routinely monitor these patients in a high dependency setting postoperatively, until they are stable enough to be transferred to a low dependency and rehabilitation setting. Anaemia is a common finding in patients with well established rheumatoid arthritis (Doyle et al 2000), though in our experience pre-operative transfusion is the exception as opposed to the rule. It is our practice to continue intravenous antibiotics for a period of 3 days post-operatively, with the initial dose being administered at time of induction, due these patients tendency to develop both early and late infections

A particularly difficult issue for surgeons to grapple with is the question of when to discontinue disease modifying drugs. Though a recent trial failed to show any significant difference (Grennan et al 2001),these medications had previously been shown to delay wound healing, a most undesirable complication in an already vulnerable group of patients (Abhilash et al 2002, Hamalainen et al 1984). Our practice is to discontinue such medications four weeks prior to surgery, having discussed the case with the patient's rheumatologist.

Posterior dislocation is found in less than 10% of cases of confirmed rheumatoid atlantoaxial dislocation (Lipson 1985). Destruction of the odontoid peg through a combination of previously described biomechanical and enzymatic means, results in the atlas subluxing posteriorly on the axis. The incidence of neurological deficit is very high due to the end position of the posterior arch of the atlas becoming wedged anterior to the spinous process of C2.

Rotatory dislocation is a less studied entity in the setting of rheumatoid disease. It is thought to occur in the setting of unilateral atlantoaxial joint destruction coinciding with severe transverse ligament laxity or destruction (Bouchaud & Liote. 2002).

It is rare when assessing a rheumatoid patient to find that the anatomical abnormality can be neatly pigeon-holed into one of the described entities. Far more commonly, patients will have subluxed in a number of axes and directions, a concept of importance when considering instrumenting such cases. As a rough rule of thumb, anterior atlantoaxial dislocation occurs first, followed by cranial settling, before subluxation of C3-C7 occurs in advanced cases (Paimela et al 1997).
