Degenerative cervical spondylolisthesis (DCS) is a pathological condition defined by anterolisthesis or anterior slippage of the cervical spine (C-spine) vertebrae. Underlying causes of this slippage include application of a shear force on the vertebra, disc degeneration, and/or hypertrophic arthropathy of the facet joint311172123). While DCS is less prevalent than spondylolisthesis at the lumbar spine, it still has an estimated prevalence of 5.2% to 11%, most commonly involving the C3-4 and C4-5 levels of the C-spine 111721). In contrast to the abundant literature on degenerative lumbar spondylolisthesis, DCS has been evaluated in only a few studies. Several predisposing factors have been reported to contribute to the development of spondylolisthesis at the lumbar spine, among which facet joint orientation is thought to play an important role181920). Gao et al.6) reported the orientation of the facet joint along the sagittal plane, known as the pedicle-facet (P-F) angle, which they measured on lateral view computed tomography (CT) scans, to be the highest intrinsically at L4-5, both in patients with lumbar spondylolisthesis and in participants in their control group. They hypothesized that a more horizontal orientation of the L4-5 facet joint (i.e., a higher sagittal plane angle) may be a predisposing anatomical factor for spondylolisthesis. However, the characteristic changes in P-F angle at the C-spine have not been well described to date.

The balance of the C-spine along the sagittal plane, in relation to the sagittal plane position of the pelvis, is increasingly being recognized as an important predisposing factor for spondylolisthesis. This sagittal plane balance is captured by the slope of the first thoracic vertebra (T1)1016). Jun et al.8) reported a greater T1 slope in patients with DCS. Therefore, we hypothesized that a high T1 slope, indicative of a loss of alignment of the spine in the sagittal plane, may be a predisposing factor for the development of DCS, increasing the magnitude of anterior shear force along the gravitational vector22). Furthermore, this chronic anterior shear force could concurrently lead to arthrotic changes of the posterior facets, which would accelerate disc degeneration and disc collapse. To the best of our knowledge, differences in P-F angle between patients with DCS and normal controls have not been specifically addressed in research. Therefore, the main objectives of this study were to compare the P-F angles, measured on simple radiographs, between patients with DCS and a control group matched on sex and age, and to evaluate the relationship between the P-F angle and the amount of vertebral anterolisthesis in patients with DCS.

Of our prospective group of 983 patients, 30 patients were diagnosed with anterolisthesis of the C-spine (3.05%). The descriptive characteristics of these patients are summarized in Table 1. The distribution of DCS by level is reported in Table 2.

The mean P-F angle values and amount of anterolisthesis, for the DCS and control groups, are reported in Table 3. The P-F angles at C4-5 were 141.14±7.14° for the DCS group and 130.54±13.50° for the control group (p=0.012). In comparison, at C5-6, the P-F angles were 137.46±8.53° and 128.53±16.01°, respectively (p=0.001). At C2-3, the P-F angles were 137.32±7.58° and 134.09±11.26°, respectively (p=0.037). However, there were no significant between-group differences in P-F angles at C3-4, C6-7, or C7-T1 levels (p≥0.051).

The mean amount of anterolisthesis in the DCS group was 2.81±0.15 mm. Age was significantly correlated with the amount of vertebral slipping in the DCS group (r=0.649, p<0.001). No significant correlation was found between any other parameters. With a linear regression analysis, statistically significant linear regression models were established by using the following formula :

The incidence of lumbar degenerative spondylolisthesis is reported to be 19.7%9). Degenerative spondylolisthesis is more rarely seen in the cervical spine. Since Lee et al.13) first reported differences in radiological findings between traumatic and degenerative listhesis of the C-spine in 1986, an overall prevalence of DCS of 5.2% to 11% has been reported. The incidence rate in our study was comparable, with DCS diagnosed in 30 of the 983 prospective participants, a prevalence of 7.64%. DCS has been reported to be most common at the C3-4 and C4-5 levels of the C-spine5711). The distribution was comparable in our study group, with evidence of DCS at C3-4 level in 18 patients (24.0%) and at C4-5 in 30 patients (40.0%).

The main cause of degenerative lumbar spondylolisthesis is disc degeneration and facet joint arthrosis. However, at the C-spine, trauma may be the most common cause of an anterior displacement of one vertebral body relative to the subjacent one. Injuries that lead to this deformity include traumatic spondylolisthesis of the axis, facet dislocation, and facet fracture/subluxation14). This anterior displacement causes progressive hypertrophic arthropathy of the facet joints, which results in joint erosions, marginal osteophyte formation, and subluxation. The secondary loss of motion, or ankylosis, between vertebral segments diminishes the mobility of the C-spine, thus increasing the stress on the adjacent discs and facets, especially during flexion and extension motions of the C-spine. The increased stress may stretch the disc and ligaments, allowing slippage to occur12).

Dean et al.5) described two types of DCS. The first type, which is more common, occurs adjacent to a relatively stiffer spondylotic segment, which is in the transition zone from stiff to more mobile segments of the spine. Considering this possible underlying pathomechanism, 'compensatory subluxation' could be a more accurate term for this type of DCS. Although disc degeneration is present in this compensatory type of anterolisthesis to some extent, the disc degeneration is radiographically and pathologically less in magnitude than in the adjacent levels with more advanced spondylosis. However, this type of spondylolisthesis is associated with osteoarthritic changes of the facet joints, including erosion, joint remodeling, and subluxation. The second type of spondylolisthesis occurs within spondylotic segments of the C-spine because of advanced disc degeneration. In comparison to Dean et al.5) classification, Woiciechowsky et al.24) classified DCS into three types : spondylolisthesis with degeneration of the facet joints; spondylolisthesis with degeneration of the facet joints and vertebral bodies; and spondylolisthesis with severe C-spine deformity. Woiciechowsky et al.24) classification is oriented toward clinical practice, being based on the assumption that degeneration of the disc and the facet joints occurs first and leads to the associated segmental instability and neck pain characteristic of DCS. However, the pathomechanism of DCS remains yet to be fully clarified.

In our study, we specifically evaluated C4-5 based on reports of the highest prevalence of DCS at this level. The highest incidence of DCS in our study group was found at the C3-4 and C4-5 levels, which is comparable to findings from several other studies2571117). Several hypotheses have been advanced to explain the higher likelihood for the development of DCS at C4-5. A number of studies have related the incidence of DCS to the relative hypermobility of the C4-5 vertebral segment, with repeated movements leading to relaxation of surrounding ligaments and, progressively, to degenerative articular changes 14610). At the lumbar spine, Nagaosa et al.15) argued that an increase in the P-F angle is a pathoanatomical risk factor for the development of degenerative spondylolisthesis. Supporting this argument, Gao et al.6) confirmed that the P-F angle was significantly larger at L4-5 in patients with degenerative spondylolisthesis compared to a control group, and that the P-F angle of the slipped vertebra was more horizontally inclined6). Our results confirmed similar findings for the C-spine, with the P-F angle being significantly larger at C4-5 in the DCS group compared to the control group. However, the mean P-F angle at the C4-5 level did not correlate with the amount of anterior slipping of the C4 vertebra; only patients' age was statistically correlated to the amount of vertebral slipping (r=0.649, p<0.001).

The limitations of our study must be acknowledged in the interpretation of results. Due to our small sample size, the characteristics of the DCS patients, and the fact that all patients were recruited from a single institution, our study group is not representative of the entire population of patients with DCS. As an example, our study did not include patients with DCS who were symptom-free. There is evidence that neck pain may in fact be the main presenting symptom of DCS7). Although we did not specifically assess neck pain in our study, more than half of the patients in our DCS group reported neck or occipital pain7). We did not consider the degree of intervertebral disc degeneration, the muscles involved in the cervical spine kinematics, or the vertebral body height in our population. In addition, we did not evaluate the relationships between the P-F angle and the amount of anterolisthesis or other factors, such as clinical manifestations, disc degeneration, and body mass index, in patients with DCS. Therefore, further research using larger patient populations may help to more comprehensively explain the risk factors for DCS. We do acknowledge, as well, that the guiding hypothesis for our research is based on previous research of the lumbar spine, which itself presents unresolved issues regarding the interaction between anatomical features, or tropism, of facet joints and the degenerative process of spondylolisthesis. Dai4) suggested that facet joint tropism was a predisposing factor to the development of disc degeneration and subsequent spondylolisthesis; however, Berlemann et al.1) argued against this functional relationship4). In our study, we used simple radiographs, which did not allow us to evaluate the relationship between facet joint tropism and the degenerative process of spondylolisthesis at the C-spine. The influence of anterolisthesis on clinical symptoms was also not specifically evaluated, and therefore we cannot comment on the relationship between the amount of slippage and symptomology.

The P-F angle was the largest at the C4-5 level in the DCS group, which might explain the predisposition of C4 to slip forward. The mean P-F angle at the C4-5 level did not correlate to the amount of vertebral slipping of C4 in DCS patients. Only age was statistically correlated with the amount of vertebral slipping.