cervical spondylolisthesis x ray

Meyerding classification of spondylolisthesis

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At the time the article was created Frank Gaillard had no recorded disclosures.

At the time the article was last revised Henry Knipe had the following disclosures:

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• Grading of spondylolisthesis
• Spondylolisthesis grading system
• Meyerding classification

The Meyerding classification of spondylolisthesis grades the severity of the slip.

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Classification, history and etymology.

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This classification was originally developed for anterolistheses but can be adapted for retrolistheses , and some publications have done so 3 .

To determine the grade of spondylolisthesis using the Meyerding classification, two vertical lines are drawn along the posterior cortex superior and inferior vertebra, and a measurement is taken between them (A). The length of the inferior vertebral body is also measured (B). A calculation of A/B determines the grade 4 :

grade I : 0-25%

grade II : 26-50% 

grade III : 51-75% 

grade IV : 76-100%  

grade V ( spondyloptosis ): >100%

The grades can be further grouped as 4 :

"low-grade": grades 1 and 2

"high-grade": grades 3, 4 and 5

The grading system is named after its inventor, Henry W. Meyerding (1884 - 1969), an American orthopedic surgeon at the Mayo Clinic in Rochester, Minnesota, USA. He proposed the classification in an article in 1932 2 .

Quiz questions

• 1. Wood W. Lovell, Robert B. Winter, Raymond T. Morrissy et al. Lovell and Winter's Pediatric Orthopaedics. (2006) ISBN: 9780781753586 - Google Books
• 2. Meyerding HW. Spondyloptosis. Surg Gynaecol Obstet. 1932;54:371–377.
• 3. He L, Wang Y, Gong J et al. Prevalence and Risk Factors of Lumbar Spondylolisthesis in Elderly Chinese Men and Women. Eur Radiol. 2014;24(2):441-8. doi:10.1007/s00330-013-3041-5 - Pubmed
• 4. Koslosky E & Gendelberg D. Classification in Brief: The Meyerding Classification System of Spondylolisthesis. Clin Orthop Relat Res. 2020;478(5):1125-30. doi:10.1097/CORR.0000000000001153 - Pubmed

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The Utility of Flexion-Extension Radiographs in Degenerative Cervical Spondylolisthesis

Andrew p alvarez , md, amanda anderson , md, saifal-deen farhan , md, young lu , md, yu-po lee , md, michael oh , md, charles rosen , md, douglas kiester , md, nitin bhatia , md.

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Reprints: Andrew P. Alvarez, MD, Department of Orthopaedic Surgery, University of California Irvine Medical Center, 101 The City Drive South, Pavilion 3, Orange, CA 92868 (e-mail: [email protected] ).

Corresponding author.

Received 2021 Jan 20; Accepted 2022 Jan 17; Issue date 2022 Aug.

This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. http://creativecommons.org/licenses/by-nc-nd/4.0/

Study Design:

Retrospective radiologic analysis.

The aim was to investigate if lateral flexion-extension radiographs identify additional cases of degenerative cervical spondylolisthesis (DCS) that would be missed by obtaining solely neutral upright radiographs, and determine the reliability of magnetic resonance imaging (MRI) in diagnosis.

Summary of Background Data:

DCS and instability can be a cause of neck pain, radiculopathy, and even myelopathy. Standard anteroposterior and lateral radiographs and MRI of the cervical spine will identify most cervical spine pathology, but spondylolisthesis and instability are dynamic issues. Standard imaging may also miss DCS in some cases.

We compared the number of patients who demonstrated cervical spondylolisthesis on lateral neutral and flexion-extension radiographs in addition to MRI. We used established criteria to define instability as ≥2 mm of listhesis on neutral imaging, and ≥1 mm of motion between flexion-extension radiographs.

A total of 111 patients (555 cervical levels) were analyzed. In all, 41 patients (36.9%) demonstrated cervical spondylolisthesis on neutral and/or flexion-extension radiographs. Of the 77 levels of spondylolisthesis, 17 (22.1%) were missed on neutral radiographs ( P ,0.05). Twenty levels (26.0%) were missed when flexion-extension radiographs were used alone ( P =0.02). Twenty-nine levels (37.7%) of DCS identified on radiograph were missed by MRI ( P =0.004).

Conclusions:

Lateral flexion-extension views can be useful in the diagnosis of DCS. These views provide value by identifying a significant cohort of patients that would be undiagnosed based on neutral radiographs alone. Moreover, MRI missed 38% of DCS cases identified by radiographs. Therefore, lateral radiographs can be a useful adjunct to neutral radiographs and MRI when instability is suspected or if these imaging modalities are unable to identify the source of a patient’s neck or arm pain.

Key Words: degenerative cervical spondylolisthesis, flexion-extension radiographs, neutral upright radiographs, MRI

Degenerative cervical spondylolisthesis (DCS) is characterized by vertebral body translation with respect to the caudal vertebral body. 1 , 2 The etiology of DCS is multifactorial and includes facet instability or fracture, cervical disc degeneration, and hypertrophic arthropathy of facet joints. 1 – 3 Patients with DCS typically present with neck pain and symptoms relating to radiculopathy or myelopathy. The prevalence of DCS may be as high as 5.2% in asymptomatic patients and 20% in symptomatic patients reporting neck pain or radiculopathy with or without neurological symptoms. 2 , 4 – 6

DCS has increasingly been noted in the literature as a source of neck pain and radiculopathy. In a study by Dean and colleagues, the authors performed a retrospective review on 58 patients who underwent surgery specifically for cervical spondylolisthesis. 5 The authors noted an average Nurick grade improvement of 1.5. In another study by Woiciechowsky and colleagues, the authors perfomed a retrospective review on 16 patients with cervical spondylolisthesis. The authors noted severe myelopathy in 8 patients, myeloradiculopathy in 5 paitents, and neck pain in 3 patients. 6 The authors noted that neck pain was the initial complaint in all the patients. After surgery, neurological improvement was seen in 6 of 8 patients with myelopathy and 4 of 5 patients with radiculomyelopathy. Hence, cervical spondylolisthesis can be a significant source of pain and disability.

Given the recent findings of these studies, we set out to perform a study to determine if flexion-extension radiographs held value in radiographic evaluation of DCS. We hypothesized that flexion-extension radiographs would not identify additional cases of instability, and their use may be discontinued in routine evaluation of DCS. Secondarily, we hypothesized as the Segebarth group found for DLS, MRI would not identify all cases of cervical spondylolisthesis as compared with those detected on neutral or dynamic radiographs.

After institutional IRB approval, we used billing codes to identify all patients who presented to our outpatient spine clinic from 2015 to 2018 who underwent cervical spine magnetic resonance imaging (MRI) and complete cervical spine radiograph series including, at minimum, upright anteroposterior, lateral neutral, flexion, and extension views. Exclusion criteria included MRI and radiographs completed >1 year of each other and patients with radiographic evidence or electronic medical record documentation of acute trauma or prior cervical spine surgery.

Horizontal translation of the posterior vertebral body of one level compared with the posterior vertebral body of the caudad cervical level was measured as previously described. 6 This was completed on 5 levels for each patient, including C2-C3, C3-C4, C4-C5, C5-C6, and C6-C7, on each radiograph (neutral, flexion, extension), and midline sagittal T1 reconstruction of cervical spine MRI. Anterolisthesis was recorded as a positive value, and retrolisthesis recorded as a negative value. The value of flexion listhesis minus extension listhesis was recorded at each level to determine the magnitude of dynamic instability. Final magnitudes of listheses were converted to absolute values when determining instability thresholds. All measurements were recorded to 0.1 mm. A positive case of spondylolisthesis was defined as displacement of the posterior vertebral body relative to the caudad vertebral body of at least 2 or 1 mm of adjacent cervical vertebral body motion between upright lateral flexion and extension radiographs. 7

After measurements were recorded, all computations performed in SPSS version 22.0 (IBM, Armonk, NY). Analyses were performed to identify levels in which spondylolisthesis were present as per above radiographic thresholds on lateral neutral listhesis magnitude, flexion minus extension listhesis (dynamic instability) magnitude, and MRI listhesis magnitude. We then used computational analyses to determine the number of levels with spondylolisthesis based on lateral neutral and flexion-extension radiographs, as well as on MRI. We compared these values to identify the total number of cases of spondylolisthesis and determine the number of cases that were missed on either neutral or flexion-extension radiographs, as well as on MRI. We also used this data to characterize spondylolisthesis at each level. χ 2 testing was used to identify if there were any statistically significant differences.

A total of 111 patients were identified as having appropriate imaging for study inclusion, totaling 555 cervical levels. Forty-one of these patients demonstrated cervical spondylolisthesis (36.9%) for a total of 77 of the examined levels (13.9%) based on neutral and/or flexion-extension radiographs. Of these 77 levels, 60 levels (77.9%) of spondylolisthesis were demonstrated on neutral radiographs and 57 levels (74.0%) were identified using flexion-extension radiographs. Seventeen levels (22.1%) were missed by using solely neutral radiographs. This difference was noted to be statistically significant ( P <0.05). Twenty levels (26.0%) were missed by using solely flexion-extension radiographs. This difference was also noted to be statistically significant ( P =0.02). Fifty-two levels (67.5%) demonstrated corresponding spondylolisthesis on MRI, leaving 29 levels (37.7%) missed by MRI. This difference was noted to be statistically significant ( P =0.004). These results are listed in Table 1 .

Quantification of Cases of Spondylolisthesis Identified on Various Imaging Modalities

MRI indicates magnetic resonance imaging.

The most common location of spondylolisthesis was at the C4-5 level with 29 cases identified (35.8%). The least frequent location of spondylolisthesis was demonstrated at the C6-7 level with 1 case identified (1.2%). Characteristics of spondylolisthesis per level are represented in Table 2 and Figure 1 .

Characterization of Spondylolisthesis Per Cervical Level on Neutral or Flexion-extension Radiographs

Graphical representation of spondylolisthesis per cervical level on neutral (A), flexion (B), and extension (C) radiographs.

Flexion and extension radiographs provide important information in the diagnosis and characterization of DCS. In this study, 17 levels (22.1%) were missed by using solely neutral radiographs. This was statistically significant ( P <0.05). However, it is important to note that cases of spondylolisthesis were not identified on flexion-extension views alone. Twenty levels (26.0%) were missed by using solely flexion-extension radiographs ( P =0.02). Also, 29 levels (37.7%) were missed by MRI alone ( P =0.004). So, flexion and extension radiographs should not be used in place of standard anteroposterior (AP) and lateral radiographs. But they can be a useful adjunct in identifying cervical spondylolisthesis when standard AP and lateral imaging and MRI are not able to identify the source of a patient’s complaint of neck and radicular pain. To our knowledge, this is a field of study that has not received attention in current literature.

In the cervical spine, unique force vectors and the kinematics involved in flexion and extension which may contribute to the findings obtained in this study. High-speed cineradiography has previously demonstrated the complexities of cervical flexion and extension. Flexion is initiated at the lower cervical spine levels (C4-C7), followed by motion sequentially from the occiput through C4. Continuing this motion, C6 through C7 exhibit a transient extension moment, with subsequent reversal of motion at the occiput through C2, with C6 and C7 contributing to terminal flexion. 8 , 9 Similarly, extension begins at the lower cervical spine levels (C4-C7), followed by motion at the occiput through C2, with the mid-cervical region contributing to intermediate range of motion and lower cervical spine contributing to terminal extension. 9 , 10 Initiation of flexion and extension at C4 correlates with C4-5 being the most frequent level of spondylolisthesis in our study, which may be related to this principle and an interesting further avenue of study.

This study is the first published to our knowledge with regard to the topic of flexion and extension radiographs in DCS. While it may bring up some curious findings that open up further research topics, our study does have the weaknesses of being limited to a single clinical setting. We also used all patients presenting to clinic with available imaging, and did not limit inclusion criteria to patients with delineated symptoms. Whether this would have statistical or clinical significance is unclear. There is also no clinical correlation as to whether each patient went on to subsequent surgery, which we could not completely identify, given some patients were visiting for second opinions or may have eventually had surgery at another institution. What is clear is that our knowledge of the pathology and factors associated with DCS is not complete and should be further studied to continue improving patient care. It has been reported that unfamiliarity with DCS has resulted in patients being unnecessarily placed in cervical traction and hospitalized, underpinning the importance of appropriate radiographic characterization of this pathologic process. 11

Lateral flexion-extension can be a useful adjunct to standard AP and lateral radiographs in the diagnosis and characterization of DCS. Recent studies have shown that cervical spondylolisthesis can be a source of cervical spine pain and nerve injury. This is the first study to show how lateral flexion-extension radiographs can be useful in identifying cases of cervical spondylolisthesis that standard AP and lateral radiographs, and MRI may miss.

The authors declare no conflict of interest.

Contributor Information

Andrew P. Alvarez, Email: [email protected].

Amanda Anderson, Email: [email protected].

Saifal-Deen Farhan, Email: [email protected].

Young Lu, Email: [email protected].

Yu-Po Lee, Email: [email protected].

Michael Oh, Email: [email protected].

Charles Rosen, Email: [email protected].

Douglas Kiester, Email: [email protected].

Nitin Bhatia, Email: [email protected].

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Imaging Techniques for the Diagnosis of Spondylolisthesis

Fig. 6.1 Normal frontal ( a ) and lateral ( b ) lumbosacral spine radiographs Fig. 6.2 Normal anatomy in the AP projection demonstrated at L3: Superior articular facet ( S ), inferior articular facet ( I ), pedicle ( P ), pars interarticularis ( * ), transverse process ( T ), lamina ( L ), and spinous process ( Sp ) Lateral Radiographs Vertebral body alignment and height are best assessed on well-positioned lateral radiographs (Fig. 6.1 ). Optimal positioning yields a single line denoting the posterior cortex of each vertebral body; a line along these posterior cortices will form a smooth, uninterrupted curve when the vertebral alignment is normal. However, lateral views are often compromised by patient rotation. With rotation, two posterior vertebral body cortices may be evident at the rotated levels; a line connecting the midpoints of the spaces between these cortices can be visualized and should again form a smooth curve when the alignment is normal. Alternatively the midpoints of the anterior aspects of the vertebral bodies should be smoothly aligned (Fig. 6.3 ). Vertebral anatomic landmarks demonstrated on lateral radiographs include the pedicles, superior and inferior articular facets, facet joints, neural foramina, intervertebral disc spaces, and spinous processes. The portion of the neural arch between the superior and inferior articular facets, the pars interarticularis (plural, pars interarticulari; Latin plural partes interarticulares) can be seen, of particular interest in spondylolisthesis (Fig. 6.4 ). Most of the radiographic measurements related to spondylolisthesis are performed on lateral views. Fig. 6.3 Assessment of vertebral body alignment on lateral radiographs with and without patient rotation. There is normal alignment in the examples shown. ( a ) Lateral lumbosacral spine radiograph with optimal positioning. A smooth, uninterrupted line is drawn along the posterior vertebral body margins of L1–S1 ( dashed line ). ( b ) Lateral view with patient rotation. The posterior vertebral margin of L5 is demarcated with a single dashed line . At L4 and above, two posterior margins are evident ( dashed lines ), with gradual divergence superiorly. Normal alignment is confirmed by visualizing a smooth line connecting the midpoints ( * ) between the dashed lines . ( c ) Another lateral view with patient rotation. Alignment in this case is assessed by visualizing a smooth line connecting the midpoints of the anterior borders of the vertebral bodies ( dots ) Fig. 6.4 Normal anatomy in the lateral projection on diagram ( a ) and lateral radiograph centered at L3 ( b ). Superior articular facet ( S ), inferior articular facet ( I ), facet joint ( F ), pedicle ( P ), pars interarticularis ( * ), neural foramen ( NF ), and spinous process ( Sp ). The transverse process of L2 ( T ) is seen en face in ( b ) Oblique Radiographs Oblique views are performed in the AP projection with the patient rotated 45° to his or her left (left posterior oblique) and right (right posterior oblique). In these views, the shape of the vertebral posterior elements is reminiscent of a Scottish terrier; hence, the term “Scottie dog” is used. The parts of the Scottie dog that can be identified include the eye (pedicle), snout or nose (transverse process), ear (superior articular facet), foot (inferior articular facet), and neck (pars interarticularis) (Fig. 6.5 ). Fig. 6.5 Normal “Scottie dog” anatomy in the oblique projection on diagram ( a ) and right posterior oblique radiograph ( b ). Superior articular facet ( S ) = dog’s ear, inferior articular facet ( I ) = foot, pedicle ( P ) = eye, pars interarticularis ( * ) = neck, transverse process ( T ) = snout. Also noted are the facet joint ( F ) and vertebral body ( VB ). ( c ) Unlabelled normal left posterior oblique projection Radiographic Diagnosis and Grading of Spondylolisthesis The diagnosis of spondylolisthesis is most commonly made on lateral lumbar spine radiographs where anterior slippage (anterolisthesis) or posterior slippage (retrolisthesis) of a vertebral body is noted in relation to the vertebral body directly below (Fig. 6.6 ). Spondylolisthesis, either anterior or posterior, is usually found at a single level but may be seen at multiple levels (Fig. 6.7 ) [ 2 ]. Again, the radiographic finding of spondylolisthesis, especially when mild, may not correlate with symptomatology. Fig. 6.6 ( a ) Anterolisthesis at L4–5. ( b ) Retrolisthesis at L2–3. Dashed lines on each image denote step-offs in alignment. Intervertebral disc space narrowing is noted at L4–5 in ( a ) ( arrow ) Fig. 6.7 Multilevel degenerative spondylolisthesis. There are anterolistheses at L3–4, L4–5, and L5–S1 ( dashed lines ). Degenerative narrowing with sclerosis is seen along the facet joints indicating arthropathy ( arrows ). Intervertebral disc space narrowing is noted at these levels, most severe at L4–5 In the radiographic grading of spondylolisthesis, the most commonly used tools are the classification systems of Meyerding [ 3 ] and Taillard [ 4 ] both of which have been shown to yield results with high intra- and inter-observer agreement [ 5 ]. Meyerding’s system is based on division of the superior endplate of the vertebra below the slipped vertebra into four equal parts. Alignment of the listhesed or slipped vertebra in relation to the divisions in the endplate below determines the grade. Slippages between 0 and 25 % of the endplate below are grade I, between 25 and 50 % are grade II, between 50 and 75 % are grade III, and between 75 and 100 % are grade IV. Anteriorly slipped vertebrae that descend anterior and inferior to the endplate below are classified as grade V, also called spondyloptosis (Fig. 6.8 ). Fig. 6.8 Meyerding grading system of spondylolisthesis. This method is based on division of the superior endplate of the lower vertebra at the level of spondylolisthesis into four equal parts from 0 to 100 %. In anterolisthesis, the posterior aspect of the lower endplate is 0 % and the anterior aspect of the endplate is 100 %. The 25, 50, and 75 % marks are shown on the upper left drawing . In retrolisthesis, the frame of reference would be the inferior endplate of the upper vertebral body. Grade I = slippage up to 25 %. Grade II = 25–50 %. Grade III = 50–75 %. Grade IV = 75–100 %. Grade V = anterior and inferior displacement of superior vertebral body (spondyloptosis) Taillard’s assessment method is also referred to as the “percentage slip” measurement. The distance between the posterior margins of the slipped vertebra and the vertebra below is divided by the anteroposterior dimension of the inferior vertebral endplate and expressed as a percentage (Fig. 6.9 ). Fig. 6.9 Taillard method of measuring spondylolisthesis (“percentage slip”). A  = AP dimension of the superior endplate of the lower vertebra at the level of spondylolisthesis. B  = measurement of anterior or posterior displacement of the superior vertebra. The % slippage = ( B  ÷  A ) × 100 In the cervical spine and thoracic spine, spondylolisthesis is commonly measured in millimeters rather than grades or percentage slip. Progression of spondylolisthesis can be assessed radiographically, provided that follow-up examinations are similar to prior studies in technique and positioning (Fig. 6.10 ). Fig. 6.10 Progression of spondylolisthesis. ( a ) Lateral lumbosacral spine radiograph shows a grade I anterolisthesis at L4–5 ( dashed lines ) with intervertebral disc space narrowing at L4–5 and L5–S1 ( arrows ). ( b ) Two years later, the spondylolisthesis has progressed to grade II ( dashed lines ) and there is further narrowing of the disc spaces at L4–5 and L5–S1 ( arrows ) Additional Radiographic Observations in Spondylolisthesis Spondylolysis Spondylolysis, a defect in the pars interarticularis, is a common radiographic finding in spondylolisthesis. The abnormality, discussed in detail in the section on isthmic spondylolisthesis, can be detected on lateral or coned-down lateral views (Fig. 6.11 ). On oblique views, a lucency in the pars interarticularis (representing a break in or collar on the Scottie dog’s neck) indicates spondylolysis (Fig. 6.12 ). In the presence of spondylolysis, a vertebral body can move forward (anterolisthesis) without its spinous process, resulting in a step-off between this spinous process and the spinous processes above (Figs. 6.13 and 6.14 ). Fig. 6.11 Spondylolysis and spondylolisthesis in the lateral projection. Arrows on diagram ( a ) and lateral radiograph ( b ) demonstrate the pars interarticularis defect. Spondylolisthesis is denoted by dashed lines in ( b ) Fig. 6.12 Spondylolysis in the oblique projection. Arrows on diagram ( a ) and right posterior oblique radiograph ( b ) demonstrate the broken Scottie dog neck (pars interarticularis). Note the normal Scottie dog neck at the level above ( open arrow in b ) Fig. 6.13 Spinous process step-off in spondylolisthesis (illustrated here at L5–S1) with spondylolysis. A dotted line runs along the posterior aspects of the spinous processes. ( a ) Normal alignment. The dotted line forms a smooth arc from L1 to L5. ( b ) Anterolisthesis at L5–S1 with spondylolysis. As the L5 vertebra and the vertebrae above move forward, the posterior elements of L1–4 also move forward. The spinous process of L5 remains in its original position (or in some cases slips posteriorly), resulting in disruption of the dotted line with a step-off between L4 and L5 Fig. 6.14 Radiographic demonstration of spinous process step-off in spondylolisthesis with spondylolysis. A grade I anterolisthesis at L5–S1 is noted with defects in the pars interarticulari ( arrow ). The L5 vertebral body remains aligned with L2–4. In contrast, the spinous process of L5 is now situated posterior to the spinous processes above ( dotted lines ) Dysplastic or Dystrophic Changes Dysplastic or dystrophic changes may be detected on radiographs in patients with spondylolisthesis. Dysplastic changes reflect abnormal development of the spinal elements, while dystrophic changes reflect sequelae of spondylolisthesis which occur in areas that had originally developed normally. In some cases, particularly in the pars interarticularis, dystrophic changes may not be distinguishable from dysplastic changes; evaluation of the remaining vertebral body elements is often helpful in these instances. Dysplastic changes related to spondylolisthesis include abnormalities of the pars interarticulari (defects or elongation), spina bifida, posterior element hypoplasia, rounding of the superior endplate of S1 and posterior wedging of L5. Dystrophic changes described by Vialle et al. [ 6 ] include bony condensation and sclerosis of the anterior portion of the S1 superior endplate and posterior portion of the L5 inferior endplate, a bony protuberance at the posterior part of the S1 endplate, and convexity of the S1 superior endplate. At a pars interarticularis defect, dystrophic sclerosis and attenuation may be seen. Degenerative Intervertebral Disc Disease and Facet Arthropathy Degenerative disc disease and facet arthropathy can be demonstrated on radiography. While these findings are most commonly associated with degenerative spondylolisthesis, they can be found in any of the other types of spondylolisthesis, especially in cases of instability. The radiographic hallmarks of degenerative disc disease are disc space narrowing, endplate sclerosis, and osteophyte formation. The frequently associated disc protrusions and bulges cannot be assessed on radiography. The vacuum phenomenon of disc degeneration may be present (Fig. 6.15 ). Fig. 6.15 Spondylolisthesis with degenerative disc disease in two patients. ( a ) Lateral radiograph of the lower lumbosacral spine demonstrates anterolisthesis at L5–S1. The hallmarks of degenerative disc disease are seen at this level including disc space narrowing ( straight white arrow ), osteophyte formation ( open white arrow ), and endplate sclerosis ( black arrows ). Similar but less severe changes are seen at L2–3 ( curved white arrow ). ( b ) In this patient with anterolisthesis at L4–5, the vacuum phenomenon of disc degeneration is present ( white arrow ) along with endplate sclerosis ( black arrows ) and an anterior osteophyte ( open white arrow ). Similar changes are present at the level below without spondylolisthesis Sclerosis and bony overgrowth at the facet joints indicate arthropathy (Fig. 6.7 ). Facet arthropathy may be overestimated on lateral views in the lower lumbosacral spine due to the overlying density of the pelvic bones, and should be confirmed on frontal or oblique views. Review of previous imaging, such as abdominal CT scans done for medical indications, often yields the desired information about the presence or absence of facet arthropathy. Generally, intervertebral disc degeneration is believed to precede facet joint degeneration and to be a primary cause of anterolisthesis [ 7 , 8 ]. Spondylolisthesis in Patients with Scoliosis Spondylolisthesis may be initially encountered in the workup of scoliosis (Fig. 6.16 ). The incidence of spondylolysis and spondylolisthesis in patients with idiopathic scoliosis has been shown to be equal to or only slightly higher than the general population. The two processes are generally, though not always, thought to be unrelated [ 9 ]. Fig. 6.16 Scoliosis and dysplastic spondylolisthesis. ( a ) AP thoracolumbar radiograph demonstrates mild S-shaped scoliosis in a teenager. ( b ) Lateral thoracolumbar radiograph demonstrates spondylolisthesis at the lower edge of the image ( curved arrow ). ( c ) Dedicated lateral lumbosacral spine radiograph was later performed, clearly showing spondylolisthesis ( dashed lines ) at L5–S1 with spondylolysis of L5 ( white arrow ) and convexity of the superior endplate of S1 ( black arrow ). ( d ) Dedicated AP view at the same time as ( c ) demonstrates dysplastic changes in the posterior elements of L5 ( open arrows ) In the adult population with scoliosis, lateral spondylolisthesis can be seen on frontal radiographs, either initially or with progression of disease (Fig. 6.17 ). Terms that are used synonymously with lateral spondylolisthesis include translatory shift, lateral subluxation, rotatory subluxation, and lateral slip. A significant correlation between lateral translation and vertebral rotation has been found, and nerve root compression by the convex superior articular facet of the inferior vertebra has been described [ 10 ]. Fig. 6.17 Lateral spondylolisthesis in a patient with progression of scoliosis. ( a ) Dextroscoliosis measures 17° and there is no step-off in the coronal plane ( dashed lines ). ( b ) Four years later, the dextroscoliosis has progressed to 35° and there is right lateral translation of L4 with respect to L5 ( dashed lines ) “Inverted Napoleon’s Hat” Sign In cases of high-grade L5 spondylolisthesis, the extreme anterior shift and tilting of L5 results in the superimposition of L5 over the sacrum on frontal radiographs. The rounded anterior margin of L5, now seen en face , resembles the dome of an inverted Napoleon’s hat, with the transverse processes forming the brim of the hat [ 11 ] (Fig. 6.18 ). The sign is not specific, being present in some cases of extreme lumbar lordosis without spondylolisthesis. Fig. 6.18 Spondyloptosis with inverted Napoleon’s hat sign. ( a ) Lateral radiograph shows displacement of L5 ( dotted lines ) anterior and inferior to superior aspect of S1 ( solid line ). There is curved ossification at the inferior aspect of L5 ( arrows ). ( b ) Sagittal fat-suppressed T2W MRI shows marked central spinal canal stenosis ( curved arrow ). The dark low signal area beneath L5 ( arrows ) corresponds to the ossification demonstrated in ( a ) which is seen along the anterior and inferior aspects of the L5–S1 disc that was displaced with L5 (note absence of disc at the superior endplate of S1). ( c ) AP radiograph demonstrates the inverted Napoleon’s hat sign related to the marked coronal orientation of the L5 endplate. The crown of the hat is formed by the anterior border of L5 ( straight arrows ) and the brim corresponds to the transverse processes ( open arrows ) Spinous Process Tilt or Rotation Tilting and/or lateral rotation of a spinous process on frontal radiographs of the lumbar spine has been described in cases of par interarticularis abnormalities with or without spondylolisthesis [ 12 , 13 ]. These signs reflect rotational instability in patients with pars interarticularis defects (spondylolysis) or unequally elongated or attenuated pars interarticulari. Ravichandran found lateral rotation of the spinous process to be more pronounced in patients with spondylolysis who had associated spondylolisthesis than in patients with spondylolysis alone [ 13 ] (Fig. 6.19 ). Fig. 6.19 Spinous process rotation and tilt as signs of spondylolysis with spondylolisthesis. ( a ) Lateral radiograph demonstrates anterolisthesis of L5–S1 ( dashed lines ). There is spondylolysis at L5 ( arrow ). ( b ) On the AP radiograph, the spinous process of L5 ( curved arrow ) is rotated to the left of an extension of the vertical line drawn through the spinous processes of L3 and L4 ( dashed line ) and appears tilted. ( c ) Axial CT slice through L5 confirms the spondylolyses ( open arrows ) and the rotation of the spinous process ( arrow ) relative to the midline ( dashed line ) Radiographic Measurements In addition to the measurement systems of Meyerding and Taillard, several radiographic measurements have been proposed in evaluating lateral lumbosacral spine radiographs in cases of spondylolisthesis but are not as commonly used. Among these measurements are pelvic incidence (PI), lumbosacral angle (LSA), sagittal pelvic tilt index, slip angle, angle of kyphosis, sagittal rotation, sacral inclination (SI), sacral slope, and lumbar index [ 5 , 14 , 15 ]. The various assessments were developed in efforts to better evaluate the overall severity of disease in addition to the amount of displacement, which might improve the ability to predict and measure the progression of disease. Dubousset reported that the increasing kyphosis over time measured by the LSA correlated with worsening of disease which could have surgical implications [ 15 ]. Curylo et al. suggested that patients with low-grade spondylolisthesis and higher PI angles could be at greater risk for progression to high-grade spondylolisthesis especially in the context of posterior element dysplasia [ 16 ]. In a review of six of the measurements listed above, only the SI measurement was shown to have inter- and intra-observer reliability comparable to those of Meyerding and Taillard [ 5 ]. Radiographic Assessment of Instability Lateral views in flexion and extension (Fig. 6.20 ) are used to assess stability at the site of spondylolisthesis or to elicit spondylolisthesis. These can be performed on the tabletop with the patient in a lateral decubitus position, or with the patient standing. Proponents of standing views note that weight-bearing views may better approximate normal daily activities. However, patients may achieve a higher degree of flexion and extension in the decubitus tabletop position. In other attempts to elicit the greatest movement at sites of spondylolisthesis, axial compression–traction techniques have been used [ 17 ]. Putto proposed that the flexion view be done with the patient seated and their hips flexed, while the extension view be done with the patient standing with hips against the radiography table [ 18 ]. Fig. 6.20 Normal flexion ( a ) and extension ( b ) lateral radiographs. The vertebral bodies remain smoothly aligned in both views Two types of instability are assessed. Parallel instability refers to movement of the upper vertebra in relation to the lower vertebra anteriorly with flexion or posteriorly with extension. The angle between the two vertebral endplates does not change significantly (Fig. 6.21 ). Angular instability is defined as an abnormal change in the angle between the endplates of the listhesed vertebra and the vertebra below (Fig. 6.22 ). Wide variations in vertebral body motion on flexion and extension have been reported. In an extensive review, Leone et al. concluded that between flexion and extension, the upper limit of normal total parallel excursion is 4 mm and the upper limit of normal angular change is 10° [ 19 ]. It should be noted that patients with normal alignment in the neutral position may demonstrate spondylolisthesis on flexion or extension (Fig. 6.23 ). Fig. 6.21 Parallel instability. ( a ) Anterolisthesis at L4–5 is seen ( dashed lines ). ( b ) The percentage slip at L4–5 increases from grade I to grade II with flexion ( dashed lines ), without significant change in angulation between the inferior endplate of L4 and superior endplate of L5 Fig. 6.22 Angular instability in spondylolisthesis. ( a ) Lateral radiograph in the neutral position demonstrates anterolisthesis at L4–5. A defect is seen in the L4 pars interarticularis ( curved arrow ). The inferior endplate of L4 is approximately parallel to the superior endplate of L5 ( dashed lines ). ( b ) Lateral radiograph in flexion demonstrates a change in the angle between the involved endplates ( dashed lines ) with L4 appearing to be perched on L5. The L4 spondylolysis defect ( curved arrow ) has widened compared to the neutral position. Spinous process dysplastic changes are seen at L4 ( arrows ). ( c ) On the AP radiograph, arrows denote dysplastic posterior elements of L4 and L5 Fig. 6.23 Spondylolisthesis on flexion in a patient with normal neutral alignment. ( a ) Neutral lateral radiograph demonstrates normal alignment at L4–5 ( dashed lines ). ( b ) Lateral radiograph in flexion demonstrates grade I anterolisthesis at L4–5 ( dashed lines ) While flexion and extension radiographs are the most common method of assessing stability, comparison between modalities may provide similar information. For instance, if the severity of spondylolisthesis changes between a neutral radiograph and a supine MRI study, instability has been effectively demonstrated (Fig. 6.24 ). Fig. 6.24 Comparison between modalities illustrates instability. ( a ) Upright lateral lumbosacral spine radiograph demonstrates anterolisthesis at L4–5 ( dashed lines ). ( b ) With the patient supine for MRI, the anterolisthesis reduces ( dashed lines ). A posterior disc protrusion ( arrow ) and vacuum phenomenon of disc degeneration ( open arrow ) are noted Progression of instability in spondylolisthesis can be assessed on serial studies. However, reproducibility of flexion and extension views is difficult and slight variations in patient positioning or angulation of the radiographic beam can result in discrepancies in the range of vertebral displacement. Magnetic Resonance Imaging MRI is a powerful cross-sectional imaging modality that detects the behavior of the nuclei of hydrogen atoms, the most abundant atoms in the human body, in the context of a strong magnetic field. The physics concepts related to MRI are complex and are beyond the scope of this text. Very simply put, patients undergoing MRI are placed within the strong magnetic field of the machine; this magnetic field is always “on.” Current is applied to a coil over the body part to be imaged and the coil produces energy in the form of a rapidly changing magnetic field. This energy falls within the energy frequency range commonly used in radio broadcasts, and is therefore called radiofrequency energy. While radiofrequency energy is on the same EM spectrum as X-rays, it is of a much higher wavelength (lower frequency and therefore lower energy) and cannot ionize tissues. Thus the risks associated with the ionizing radiation of radiography, computed tomography, and nuclear medicine studies do not apply to MRI. The radiofrequency energy from the coil causes alterations in the spin of the hydrogen nuclei. When the radiofrequency waves are turned off, the hydrogen nuclei “relax” to assume their original orientation. As they relax, they give off energy which is detected by a receiver coil; the information is then processed by computer and an image is generated. An array of coils and MRI scanning parameters are available for use depending on the body part and the type of information sought. MRI is the cross-sectional imaging modality of choice in the workup of spondylolisthesis as excellent soft tissue differentiation is achieved without exposing the patient to ionizing radiation. MRI Scanning Sequences and Anatomy The studies should include sequences using a variety of parameters. T1-weighted (T1W) images are useful for visualizing fracture lines and excluding abnormal marrow infiltration. Proton-density (PD) or T2-weighted (T2W) images provide good spatial resolution. Short-tau inversion recovery (STIR) sequences are excellent for detection of bone marrow edema as are fat-suppressed PD or T2W sequences. Various gradient-echo (GE) sequences are available and are useful in evaluating the intervertebral disc contours particularly in the cervical spine. Sagittal images demonstrate vertebral body heights and alignment, and are also used to evaluate intervertebral disc heights and disc hydration. The central spinal canal and neural foramina can be assessed on both sagittal and axial images. The axial sequences should include a “stacked” set of slices that are contiguous and parallel to each other, rather than angled for disc evaluation, in order to gain optimal visualization of the pars interarticulari. Coronal images are useful for visualization of scoliosis and lateral spondylolisthesis. Figure 6.25 shows normal lumbosacral spine anatomy on MRI. Fig. 6.25 Normal MRI of lumbosacral spine. ( a ) Midline sagittal T1W image demonstrates normal vertebral body alignment. The bone marrow signal in the vertebra ( VB ) is brighter than the signal in the intervertebral disc ( D ). On the sagittal STIR image ( b ), the vertebra ( VB ) is now darker than the disc ( D ). Individual nerve roots can be seen as linear low signal foci ( arrows ) within the bright cerebrospinal fluid. ( c ) Sagittal T2W image through the left neural foramina demonstrates the superior articular facet ( S ), inferior articular facet ( I ), facet joint ( F ), pedicle ( P ), pars interarticularis ( * ), and nerve root ( NR ). ( d ) Axial T2W slice through the neural foramina demonstrates the vertebral body ( VB ), exiting nerve roots ( white arrows ), facet joints ( open white arrows ), and layering descending nerve roots ( curved black arrow )

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• Published: 26 June 2020

Prevalence of cervical anterior and posterior spondylolisthesis and its association with degenerative cervical myelopathy in a general population

• Kimihide Murakami 1 ,
• Keiji Nagata 1 ,
• Hiroshi Hashizume 1 ,
• Hiroyuki Oka 2 ,
• Shigeyuki Muraki 3 ,
• Yuyu Ishimoto 1 ,
• Munehito Yoshida 4 ,
• Sakae Tanaka 5 ,
• Akihito Minamide 1 ,
• Yukihiro Nakagawa 6 ,
• Noriko Yoshimura 3   na1 &
• Hiroshi Yamada 1   na1  

Scientific Reports volume  10 , Article number:  10455 ( 2020 ) Cite this article

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• Risk factors

The purpose of this study was to examine the prevalence of cervical spondylolisthesis according to age and vertebral level and its association with degenerative cervical myelopathy (DCM). This study included 959 participants (319 men and 640 women; mean age, 66.4 years) in the Wakayama Spine Study from 2008 to 2010. The outcome measures were cervical spinal canal (CSC) diameter at C5 level on plain radiographs, the degree of cervical spondylosis using the Kellgren-Lawrence (KL) grade, cervical cord compression on sagittal T2-weighted magnetic resonance imaging, and physical signs related to DCM. The prevalence of cervical anterior and posterior spondylolisthesis was investigated in men and women by age. In addition, logistic regression analysis determined the association between CSC diameter, posterior spondylolisthesis, and clinical DCM after overall adjustment for age, sex, and body mass index. The prevalence of anterior spondylolisthesis was 6.0% in men and 6.3% in women, and that of posterior spondylolisthesis was 13.2% and 8.9%, respectively. In addition, posterior spondylolisthesis prevalence increased with age in both sexes. Logistic regression analysis revealed that developmental canal stenosis (≤13 mm) and cervical posterior spondylolisthesis are independent significant predictive factors for DCM. The prevalence of degenerative cervical posterior spondylolisthesis was increasing with age and more frequent in men than in women. Narrow canal and degenerative cervical posterior spondylolisthesis on X-ray may be useful in predicting or diagnosing DCM.

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Introduction.

Degenerative cervical myelopathy (DCM) is a disease concept that includes age-related degenerative changes of the cervical spine, such as intervertebral disc disease, vertebral remodeling, hypertrophy and/or ossification of spinal ligaments, and spondylolisthesis. Cervical spondylolisthesis prevalence has been reported as low as 5.2% to 12% 1 , 2 , 3 , whereas that of lumbar spondylolisthesis is 15.8% to 19.7% 4 , 5 . Thus, cervical spondylolisthesis has received less attention than lumbar spondylolisthesis.

Cervical anterior spondylolisthesis (AS) and posterior spondylolisthesis (PS) are mainly caused by degeneration of disc and facet joint 6 . Cervical spondylolisthesis results in not only cervical pain but also radiculopathy or myelopathy as it progresses and thus should never be neglected. In the aging society, the number of patients with degenerative changes of the cervical spine is expected to increase. Nevertheless, currently, reports on the association between cervical spondylolisthesis and DCM are few. Cervical spondylolisthesis could be relatively easily diagnosed by cervical plain X-ray (lateral view). If the association between cervical spondylolisthesis and DCM become clear, a risk assessment of DCM could be expected in patients diagnosed as having cervical spondylolisthesis using relatively easy-to-use imaging tests, such as plain radiographs.

Hence, this study aimed to examine the prevalence of cervical spondylolisthesis according to sex, age and vertebral level and its association with DCM.

Compliance with ethical standards

This study was conducted in accordance with the Declaration of Helsinki and the study design was approved by the Ethics Committee of the Wakayama Medical University. All volunteers provided written informed consent for participation.

Participants

This cross-sectional observational study was approved by the appropriate ethics committee. All participants provided written informed consent, and the study design was approved by the appropriate ethics review boards. This study is a part of “The Wakayama Spine Study: a population-based cohort,” which is a large-scale population-based magnetic resonance imaging (MRI) study. Details of The Wakayama Spine Study have been described elsewhere 7 , 8 . Briefly, the baseline survey of The Wakayama Spine Study was conducted between 2008 and 2010 in a mountainous region in Hidakagawa, Wakayama, and a coastal region in Taiji, Wakayama. A total of 1063 residents of the Hidakagawa, Taiji region were recruited for MRI examination, of which 52 people declined. Thus, 1011 inhabitants were enrolled in this study. Of the 1011 participants, those with MRI-sensitive implantable devices (such as pacemakers) and other unqualified individuals were excluded. Subsequently, the cervical spine of 985 individuals was scanned with MRI. Four participants who had undergone previous cervical surgery and another four with poor image quality were excluded from the analysis. A total of 977 participants were included in the final analysis. Radiological evaluation of the cervical vertebrae was also performed in 959 subjects. The results of both MRI and radiography were available for 959 participants (males, 319; females, 640) aged 21 to 97 years (average, 67.3 years; female 65.9 years).

Physical measurements included height (meter), body weight (kilogram), and body mass index (BMI; body weight [kilogram] / height 2 [m 2 ]). Medical information on sensory disorder, Hoffman reflex, Babinski reflex, and deep tendon reflex of the patellar tendon was obtained by an experienced orthopedic surgeon. Hoffmann reflex was tested in a neutral position by flicking the distal phalange of the middle finger and observing whether bending of the distal phalanx of the thumb occurs 9 . The Babinski reflex was elicited by firmly sweeping from the lateral part of the sole to the base of the toes with the tip of a reflex hammer and observing the hallux extensor response 10 .

Radiographic measures

All subjects underwent lateral radiograph with their neck in the neutral position. Radiographic information, which was put on film, was evaluated and calibrated using the ruler. Sagittal spinal canal diameter at C5 level was measured as the shortest distance from the midpoint between the vertebral body’s superior and inferior endplates to the spinolaminar line 11 . Slippage distance was measured as the distance from the posteroinferior corner of the cranial vertebral body to the tangential line along the posterior border of the caudal vertebral body 12 . We defined the spondylolisthesis group as those with ≥2 mm of slippage on the baseline lateral radiographs. The degree of cervical spondylosis was determined using the Kellgren-Lawrence (KL) grade as follows: KL0, normal; KL1, slight osteophytes; KL2, definite osteophytes; KL3, disc space narrowing with osteophytes; KL4, bone sclerosis, disc space narrowing, and large osteophytes (Fig.  1 ).

Radiographic measurements of the cervical spine. ( a ) Diameter of the cervical spinal canal at C5. ( b ) Measurement of cervical anterior/posterior spondylolisthesis. ( c ) Kellgren-Lawrence classification for grading of cervical spondylosis.

An MRI scan of the cervical spine was obtained for each participant using a 1.5-T Excelart imaging system (Toshiba, Tokyo, Japan). All scans were performed in the supine position, except for participants with a rounded back, who used a triangular pillow under their heads and knees. The imaging protocol included a sagittal T2-weighted fast spin-echo pulse sequence (repetition time, 4000 ms; echo time, 120 ms; field of view, 300 × 320 mm) and an axial T2-weighted fast spin-echo pulse sequence (repetition time, 4000 ms; echo time, 120 ms; field of view, 180 × 180 mm) 7 , 8 .

Definition of clinical DCM

Physical findings concerning sensory disturbances, Hoffmann reflex, Babinski reflex, and deep tendon reflex of the patellar tendon were examined by an experienced orthopedic surgeon. A myelopathic sign was defined as the presence of patellar tendon hyperreflexia, Hoffmann reflex, or Babinski reflex. Myelopathy was defined clinically by the presence of myelopathic signs (e.g., Hoffmann reflex), which was usually accompanied by bilateral sensory deficits, or poor bowel/bladder function. Among the participants with myelopathic signs, cervical cord compression was the essential condition for diagnosing DCM 13 , 14 .

Statistical analysis

Baseline characteristics were compared between sexes using Student’s t -test. Cochran-Armitage trend test was used to evaluate the association of cervical spinal canal (CSC) diameter, KL grade, and spondylolisthesis prevalence with aging. Prevalence of KL grades ≥3 and ≥4 and cervical AS and PS was compared between participants with and those without DCM using the chi-square test. Age, BMI, and CSC diameter were compared between participants with and those without DCM using non-paired Student’s t -test. To determine the association of DCM with radiographic factors, logistic regression analysis was employed after overall adjustment for age, sex, and BMI. All statistical tests were performed at a significance level of 0.05 (two-sided). Data were analyzed using JMP PRO version 14 (SAS Institute, Inc., Cary, NC, USA).

Characteristics of the participants

Baseline characteristics of the 959 participants (men, 319; women, 640), including anthropometric measurements and physical performance data, are listed in Table  1 . No significant difference in age between sexes was found. Height, weight, BMI, and grip strength were significantly higher in men than in women (p < 0.001).

Sex and age differences in AS and PS

Table  2 shows the age-related differences in AS and PS on radiograph in men and women among different age groups. AS prevalence was most frequently observed at C4 levels, while PS prevalence was mostly noted at C4 and C5 levels in both sexes.

Radiographic measures stratified by sex and age

Table  3 shows the age-related differences in CSC diameter, KL grade, and AS and PS prevalence on radiograph in men and women among different age groups. CSC diameter was significantly narrower with age in women, and the CSC diameter of women was narrower than that of men in each age group. The number of spondylosis of KL ≥ 3 (p < 0.001) and KL ≥ 4 (p < 0.001) was increasing with age. PS prevalence increased with age in men (p = 0.047) and women (p = 0.029).

Association between cervical anterior/posterior spondylolisthesis and DCM

The association between the radiographic measurement of cervical spine and DCM is shown in Table  4 . Age in both men and women was not significantly associated with DCM (p = 0.67 in men, p = 0.06 in women). Similarly, BMI showed no association with DCM. CSC diameter in men was not significantly associated with DCM (p = 0.11), whereas that in women was significantly associated with DCM (p < 0.0001).

Spondylosis of KL ≥ 3 in both men and women was not significantly associated with DCM (p = 0.49 in men, p = 0.98 in women), and spondylosis of KL ≥ 4 was also not significantly associated with DCM in both sexes (p = 0.39 in men, p = 0.21 in women). Moreover, AS was not significantly associated with DCM in men (p = 0.66) and women (p = 0.70), whereas PS was significantly associated with DCM in men (p < 0.0001) and women (p = 0.03).

Multiple logistic regression analysis of radiographic measures of cervical spine for DCM

Furthermore, multiple logistic regression analysis was performed to evaluate the predictive factors for DCM in radiographic measures after adjustment for age, sex, and BMI (Table  5 ). CSC diameter (odds ratio [OR], 2.4; 95% confidence interval [CI], 1.6–3.6; p < 0.0001) and cervical PS (OR, 4.3; 95% CI, 1.7–10.1; p = 0.0011) were independent significant predictive factors for DCM. In addition, concurrence of developmental canal stenosis (≤13 mm) and cervical PS was a more significant predictive factor for DCM (OR, 19.7; 95% CI, 5.6–63.1; p < 0.0001).

This study examined the relationship between radiographic measures of cervical spine and DCM. We found that CSC diameter on plain X-rays and cervical PS are factors significantly related to DCM in the general population.

The prevalence of AS is 6.0% in men and 6.3% in women, while that of PS is 13.2% in men and 8.9% in women; both conditions are more common in the elderly. AS most often occurs at C4 and PS at C4 or C5 in both men and women. In our study, AS was not significantly related to DCM in either men or women; however, PS was significantly related to DCM in both sexes. Moreover, this study found no relationship between cervical spondylosis (i.e., KL grade 3 or 4) and DCM. One reason why cervical spondylosis and DCM are not related is the differences in the anteroposterior diameter of the vertebral canal, i.e., participants without myelopathy in our study had a larger anteroposterior diameter of the vertebral canal than those with myelopathy. In addition, relative retention of the anteroposterior diameter of the vertebral canal despite osteophyte formation or intervertebral disc degeneration could be a reason why myelopathy did not develop 15 .

A previous study found that both AS and PS often occur at C3 and C4. Our study found that AS often occurs at C4 and PS often occurs at C4 or C5; these findings are similar to the results of previous studies 16 . Vertebral displacement or slippage, which results from intervertebral disc degeneration in the more mobile lower cervical spine, mainly occurs at the mid-cervical level with osteophyte formation and thickening of the facet joints. Degenerative changes reduce lower cervical spine mobility; thus, the load on adjacent vertebrae increases to compensate 17 . Teraguchi et al . 18 showed that intervertebral disc degeneration occurs most frequently at C5–C6 in the cervical spine. Reduced lower cervical spine mobility associated with degeneration could cause vertebral displacement or slippage at the mid-cervical level. Nevertheless, AS and PS may not necessarily occur via the same mechanism. Studies reported that the facet joints normally serve as restraints against spondylolisthesis; however, facet joint degeneration destroys those restraints, thereby causing spondylolisthesis 19 , 20 . Moreover, Jun et al . 21 reported that T1 slope is significantly larger in the degenerative cervical spondylolisthesis group than in the control group. They suggested that a high T1 slope may be a predisposing factor for the development of degenerative cervical spondylolisthesis. Hence, disc degeneration, T1 slope, and facet degeneration are possible causes of degenerative cervical AS.

Based on the tilting or sliding of vertebral bodies as observed during flexion to extension, Kokubun et al . 22 surmised that sliding is predominant in PS. In addition, Lee et al . 23 suggested that intervertebral disc space narrowing causes cervical PS.

Furthermore, facet joint degeneration has been cited as a cause of PS, and PS increased with age and was more prevalent in men than in women (13.2% vs. 8.9%). Uhrenholt et al . 24 reported that degenerative changes affecting the cartilage, osteocartilaginous junction, and subchondral bone of the facet joints are significantly related to age and are more severe in men. Ndubuisi et al . 25 suggested that changes in the cervical spine differ between sexes because men and women performed different types of work in rural areas. For example, men may perform work involving heavy loads, such as farming, while women may do work involving lighter loads, such as household chores and cooking. In our study, the subjects were from fishing and rural communities where men performed work involving a relatively heavy load, which in turn could explain why PS was more prevalent in men.

In this study, no relationship between AS and DCM was found; however, a relationship between PS and DCM was observed. The pincer mechanism reported by Penning et al . 26 plays a substantial role in the relationship between PS due to intervertebral disc degeneration and DCM. During extension of the neck, the spinal cord is pinched between the postero-inferior margin of the superior vertebral body and the antero-superior margin of the lamina of the inferior vertebra, which has been found to result in dynamic spinal cord compression. Thus, PS may be a dynamic factor for DCM. In addition, a previous study reported that ligamentum flavum buckling could lead to spinal stenosis 22 . Satomi et al . 27 stated that dynamic spinal cord compression between the postero-inferior margin of a vertebral body and the lamina of a superior vertebra resulting from AS during anteflexion is associated with the development of myelopathy. In addition, AS was noted in three participants with displacement of ≥3.5 mm; however, no patient developed DCM. Hence, AS may not necessarily be a mechanism involved in myelopathy. Myelopathy was also less likely to develop because ligament buckling did not occur in AS.

A similar study by Yukawa et al . 28 compared the anteroposterior diameter of the vertebral canal by sex and reported that women had a vertebral canal with a small anteroposterior diameter. Nagata et al . 7 reported that DCM was more likely to develop as a result of a vertebral canal with a small anteroposterior diameter. These results indicate that women have a higher risk of developing DCM. Moreover, current results revealed that a combination of developmental spinal stenosis and PS would lead to an even higher risk of developing DCM.

The key aspect of this study is that parameters, such as the CSC diameter and cervical PS on plain X-rays of the cervical spine, could be used to predict the risk of DCM. These parameters may facilitate screening for DCM.

This study has several limitations. First, although this study included more than 1000 participants, the participants may not represent the general population because they were recruited from only two areas in Japan. Nonetheless, anthropometric measurements were compared between this study’s participants and the general Japanese population, no significant differences in BMI were found in both sexes. Second, this is a cross-sectional observational study. We could not confirm a causal relationship between degenerative cervical spondylolisthesis and DCM. Third, more critical subjects might not have participated in our study; thus, selection bias is possible. Fourth, we failed to evaluate dynamic instability of the cervical spine, which should be taken into consideration in DCM evaluation.

Conclusions

This study elucidated the prevalence of cervical spondylolisthesis according to sex, age and vertebral level and its association with DCM in a Japanese population. The prevalence of degenerative cervical posterior spondylolisthesis was increasing with age and more frequent in men than in women. Narrow canal and degenerative cervical posterior spondylolisthesis on X-ray may be useful in predicting or diagnosing DCM.

Data availability

All data generated or analyzed during this study are available from the corresponding author upon reasonable request.

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Acknowledgements

The authors wish to thank Dr. Takako Nojiri and Mr. Kazuhiro Hatanaka of the Gobo Public Health Centre; Dr. Naoki Hirabayashi of the Kawakami Clinic, Hidakagawa Town; Mrs. Tomoko Takijiri, Mrs. Kumiko Shinou, Mrs. Rie Takiguchi, Mrs. Kyoko Maeda, Ms. Ikuyo Ueyama, Mrs. Michiko Mori, Mrs. Hisayo Sugimoto, and other members of the public office in Hidakagawa Town; Dr. Shinji Matsuda of the Shingu Public Health Centre; and Mrs. Tamako Tsutsumi, Mrs. Kanami Maeda, Mr. Shoichi Shimoichi, Mrs. Megumi Takino, Mrs. Shuko Okada, Mrs. Kazuyo Setoh, Mrs. Chise Ryouno, Mrs. Miki Shimosaki, Mrs. Chika Yamaguchi, Mrs. Yuki Shimoji, and other members of the public office in Taiji Town for their assistance in locating and scheduling participants for examinations. We also thank Ms. Kyoko Yoshimura, Mrs. Toki Sakurai, and Mrs. Saeko Sahara for their assistance with data reduction and administration.

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These authors contributed equally: Noriko Yoshimura and Hiroshi Yamada.

Authors and Affiliations

Department of Orthopaedic Surgery, Wakayama Medical University, 811-1 Kimiidera, Wakayama City, Wakayama, Japan

Kimihide Murakami, Keiji Nagata, Hiroshi Hashizume, Yuyu Ishimoto, Akihito Minamide & Hiroshi Yamada

Department of Medical Research and Management for Musculoskeletal Pain, 22nd Century Medical and Research Center, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan

Hiroyuki Oka

Department of Preventive Medicine for Locomotive Organ Disorders, 22nd Century Medical and Research Center, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan

Shigeyuki Muraki & Noriko Yoshimura

Department of Orthopaedic Surgery, Sumiya Orthopaedic Hospital, 337 Yoshida, Wakayama City, Wakayama, Japan

Munehito Yoshida

Department of Orthopaedic Surgery, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan

Sakae Tanaka

Department of Orthopaedic Surgery, Wakayama Medical University Kihoku Hospital, 219 Myoji, Katsuragi Town, Ito County, Wakayama, Japan

Yukihiro Nakagawa

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Contributions

K.M., K.N., H.H., H.O., S.M., Y.I., M.Y., S.T., A.M., Y.N., N.Y., and H.Y. conceived and designed this study. K.M. and K.N. wrote the manuscript. K.M., K.N., H.H., H.O., Y.I., S.M., and N.Y. performed data collection. K.M., K.N., H.H., H.O., and N.Y. analyzed the data. All authors have seen the original study data, reviewed the data analysis, and approved the final manuscript.

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Correspondence to Hiroshi Hashizume .

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Murakami, K., Nagata, K., Hashizume, H. et al. Prevalence of cervical anterior and posterior spondylolisthesis and its association with degenerative cervical myelopathy in a general population. Sci Rep 10 , 10455 (2020). https://doi.org/10.1038/s41598-020-67239-4

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DOI : https://doi.org/10.1038/s41598-020-67239-4

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Characteristic findings on imaging of cervical spondylolisthesis: Analysis of computed tomography and X-ray photography in 101 spondylolisthesis patients

Affiliations.

• 1 Department of Orthopaedic Surgery, Tokyo Dental College Ichikawa General Hospital, Tokyo, Japan.
• 2 Shiraishi Spine Clinic, Tokyo, Japan.
• 3 Department of Orthopaedic Surgery, Saiseikai Utsunomiya Hospital, Tochigi, Japan.
• 4 Department of Orthopaedic Surgery, Murayama Medical Center, Tokyo, Japan.
• 5 Department of Orthopaedic Surgery, Saiseikai Tobu Yokohama Hospital, Kanagawa, Japan.
• PMID: 31440643
• PMCID: PMC6698550
• DOI: 10.22603/ssrr.2017-0017

Introduction: The characteristics of cervical spondylolisthesis are not currently fully understood, because of the shortage of reports covering the large population of patients with cervical spondylolisthesis. The purpose of this study was to elucidate the characteristics of cervical spondylolisthesis by examining a relatively large number of cases.

Methods: We analyzed 101 cases with more than 2 mm of vertebral listhesis as determined from X-ray or computed tomography (CT) images among 731 patients who underwent surgery at a single institute. We considered the C2-7 angle, range of motion, and C2-7 sagittal vertical axis on lateral X-ray images. From sagittal CT images, classifications into five grades based on the slipped disc and adjacent caudal levels were made. We examined the orientation of facet joints at the slipped level using axial CT images.

Results: Spondylolisthesis was recognized in 101 cases at 124 levels. Anterior and posterior spondylolisthesis were detected in 68 and 40 cases, respectively. Anterior spondylolisthesis developed predominantly at C3 or C4, usually at the level adjacent to the narrowed disc, or at C7, adjacent to the stiffened thoracic spine. The disc height was relatively preserved at the anterior slipped level. Posterior spondylolisthesis developed predominantly at the level of the significantly narrowed disc associated with advanced intervertebral osteoarthritis. At the segment with listhesis in the lower cervical spine, the direction of the facet joint in the axial plane tended to be posteromedial.

Conclusions: Cervical degenerative spondylolisthesis was classified into two types. The first and more common listhesis occurred adjacent to stiffened levels, and anterior slippage was common in this type. The second and less common listhesis occurred within progressively degenerated segments, and posterior slippage was prominent. We have uniquely described the morphological changes in orientation of the cervical facet joints at the slipped level in the transverse plane.

Keywords: CT; X-ray; cervical facet joint; imaging; spondylolisthesis.