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 ) .
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 .
patients with dcs were identified retrospectively from the total group of patients who attended the spine center in our institution between june 2002 and december 2012 . during this period ,
983 patients received plain radiographs to inform various diagnoses , such as neck pain and cervical radiculopathy .
patients with non - degenerative cervical disease - trauma , infection , tumor , deformity , and inflammatory diseases - or prior cervical spine surgery were excluded .
plain anterior - posterior and lateral view radiographs had been obtained with patients in a relaxed standing position , with the upper extremities positioned naturally at the side of the body and the head maintained in a neutral position , with horizontal gaze parallel to the frankfurt horizontal plane .
the radiographs were used to confirm a 7-segmental cervical spine and to rule - out developmental anomalies of the c - spine , signs of lytic lesions , and scoliotic deformity of > 10. following screening for exclusion criteria , 30 adult patients with a diagnosis of dcs at c4 - 5 , without evidence of dcs at any other level , consisting of 15 men and 15 women , with an average age of 40.30 years ( range , 23 - 76 years ) , were included in the study .
the control group consisted of 30 adults , matched on sex and age with patients in the dcs group , identified by retrospective analysis of patients who had attended the ear , nose , throat out - patient department of our institution between january 2008 and september 2012 , and who had received plain radiographs of the c - spine as part of their medical care .
patients in the control group had never been diagnosed with or treated for a spinal problem .
the group included 15 men and 15 women , with an average age of 41.10 years ( range , 27 - 81 years ) .
dcs was defined , using previously defined criteria , as an anterolisthesis ( i.e. , slip ) of the vertebra of more than 2 mm 2112324 ) .
the extent of anterior slip of the vertebra was measured as the distance from the postero - inferior corner of the cranial ( i.e. , superior ) vertebral body to the tangential line along the posterior border of caudal ( i.e. , lower ) vertebral body ( fig .
the p - f angle , calculated on lateral view radiographs , was formed by the intersection between a straight line connecting the midpoints of the anterior and posterior cortices of the vertebrae and a straight line positioned parallel to the facet joint ( fig .
plain radiographs were saved in the picture archiving and communication system ( pview ; infinitt , seoul , korea ) for analysis .
the quality of radiographs for measurements of p - f angles and amount of anterolisthesis was ascertained by two independent observers . after agreement ,
the outcome variables were independently measured twice , by two spinal surgeons from the neurosurgery department .
the pearson 's correlation coefficient between the two measures was calculated as an indicator of agreement .
the association of p - f angles to group characteristics , namely age and sex , was evaluated using pearson 's correlation .
between - group differences in p - f angles were evaluated using independent - samples t - test .
all statistical analyses were performed in spss , version 19.0 ( ibm spss , armonk , ny , usa ) , with p<0.05 considered to be significant .
patients with dcs were identified retrospectively from the total group of patients who attended the spine center in our institution between june 2002 and december 2012 . during this period ,
983 patients received plain radiographs to inform various diagnoses , such as neck pain and cervical radiculopathy .
patients with non - degenerative cervical disease - trauma , infection , tumor , deformity , and inflammatory diseases - or prior cervical spine surgery were excluded .
plain anterior - posterior and lateral view radiographs had been obtained with patients in a relaxed standing position , with the upper extremities positioned naturally at the side of the body and the head maintained in a neutral position , with horizontal gaze parallel to the frankfurt horizontal plane .
the radiographs were used to confirm a 7-segmental cervical spine and to rule - out developmental anomalies of the c - spine , signs of lytic lesions , and scoliotic deformity of > 10. following screening for exclusion criteria , 30 adult patients with a diagnosis of dcs at c4 - 5 , without evidence of dcs at any other level , consisting of 15 men and 15 women , with an average age of 40.30 years ( range , 23 - 76 years ) , were included in the study .
the control group consisted of 30 adults , matched on sex and age with patients in the dcs group , identified by retrospective analysis of patients who had attended the ear , nose , throat out - patient department of our institution between january 2008 and september 2012 , and who had received plain radiographs of the c - spine as part of their medical care .
patients in the control group had never been diagnosed with or treated for a spinal problem .
the group included 15 men and 15 women , with an average age of 41.10 years ( range , 27 - 81 years ) .
dcs was defined , using previously defined criteria , as an anterolisthesis ( i.e. , slip ) of the vertebra of more than 2 mm 2112324 ) .
the extent of anterior slip of the vertebra was measured as the distance from the postero - inferior corner of the cranial ( i.e. , superior ) vertebral body to the tangential line along the posterior border of caudal ( i.e. , lower ) vertebral body ( fig .
the p - f angle , calculated on lateral view radiographs , was formed by the intersection between a straight line connecting the midpoints of the anterior and posterior cortices of the vertebrae and a straight line positioned parallel to the facet joint ( fig .
plain radiographs were saved in the picture archiving and communication system ( pview ; infinitt , seoul , korea ) for analysis .
the quality of radiographs for measurements of p - f angles and amount of anterolisthesis was ascertained by two independent observers . after agreement ,
the outcome variables were independently measured twice , by two spinal surgeons from the neurosurgery department .
the pearson 's correlation coefficient between the two measures was calculated as an indicator of agreement .
the association of p - f angles to group characteristics , namely age and sex , was evaluated using pearson 's correlation .
between - group differences in p - f angles were evaluated using independent - samples t - test .
all statistical analyses were performed in spss , version 19.0 ( ibm spss , armonk , ny , usa ) , with p<0.05 considered to be significant .
of our prospective group of 983 patients , 30 patients were diagnosed with anterolisthesis of the c - spine ( 3.05% ) .
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 141.147.14 for the dcs group and 130.5413.50 for the control group ( p=0.012 ) . in comparison , at c5 - 6 , the p - f angles were 137.468.53 and 128.5316.01 , respectively ( p=0.001 ) . at c2 - 3 , the p - f angles were 137.327.58 and 134.0911.26 , 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 ( p0.051 ) .
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 : [ vertebral slippage=1.184+(0.4age ) ] , ( p=0.005 )
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% ) .
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 ) .
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 can not 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 .
 objectiveto measure the orientation of the facet joints of cervical spine ( c - spine ) segments in the sagittal plane , known as the pedicle - facet ( p - f ) angle , and to use these measurements to evaluate the relationship between the p - f angle and the amount of vertebral anterolisthesis in patients with degenerative cervical spondylolisthesis ( dcs).methodsa retrospective case - control study was performed including 30 age- and sex - matched patients with dcs and 30 control participants . 
 anterior - posterior and lateral view radiographs of the c - spine were obtained in a standing position . 
 the p - f angle at all cervical levels and the amount of anterolisthesis at c4 - 5 were measured from lateral view plain radiographs.resultsthe p - f angles at c4 - 5 were 141.147.14 for the dcs group and 130.5313.50 ( p=0.012 ) for the control group , and at c5 - 6 were 137.468.53 for the dcs group and 128.5316.01 for the control group ( p=0.001 ) . 
 the mean p - f angle at c4 - 5 did not correlate with the amount of anterolisthesis ( p=0.483 ) . 
 the amount of anterior slippage did correlate with age ( p<0.001).conclusionthe p - f angle was intrinsically higher at c4 - 5 , compared to c5 - 6 , in both the dcs and control groups , which might explain the increased likelihood for anterolisthesis of c4 . 
 higher p - f angles in the dcs group may be a predisposing factor to slippage . 
 the p - f angle may interact with age to increase incidence of anterolisthesis with increasing age . 
INTRODUCTION
MATERIALS AND METHODS
Participants
Radiographical assessment
Statistical analysis
RESULTS
DISCUSSION
CONCLUSION