spine what are the reliable radiological indicators of lumbar ......2-5-22 nishi-machi, konan-ku,...

650 THE JOURNAL OF BONE AND JOINT SURGERY

SPINE

What are the reliable radiological indicators of lumbar segmental instability?

K. Hasegawa, H. Shimoda, K. Kitahara, K. Sasaki, T. Homma

From Niigata Spine Surgery Centre, Niigata, Japan

K. Hasegawa, MD, PhD, Professor

H. Shimoda, MD, Spine Surgeon

K. Sasaki, MD, Spine Surgeon

T. Homma, MD, PhD, DirectorNiigata Spine Surgery Centre, 2-5-22 Nishi-machi, Konan-Ku, Niigata City 950-0165, Japan.

K. Kitahara, PhD, Research DirectorShowalka Kogyo, 8-7 Nishimachi, Hanei, Toyohashi City, Aichi 441-8026, Japan.

Correspondence should be sent to Professor K. Hasegawa; e-mail: [email protected]

©2011 British Editorial Society of Bone and Joint Surgerydoi:10.1302/0301-620X.93B5. 25520 $2.00

J Bone Joint Surg [Br] 2011;93-B:650-7.Received 12 July 2010; Accepted after revision 14 January 2011

We examined the reliability of radiological findings in predicting segmental instability in 112 patients (56 men, 56 women) with a mean age of 66.5 years (27 to 84) who had degenerative disease of the lumbar spine. They underwent intra-operative biomechanical evaluation using a new measurement system. Biomechanical instability was defined as a segment with a neutral zone > 2 mm/N. Risk factor analysis to predict instability was performed on radiographs (range of segmental movement, disc height), MRI (Thompson grade, Modic type), and on the axial CT appearance of the facet (type, opening, vacuum and the presence of osteophytes, subchondral erosion, cysts and sclerosis) using multivariate logistic regression analysis with a forward stepwise procedure. The facet type was classified as sagittally orientated, coronally orientated, anisotropic or wrapped.

Stepwise multivariate regression analysis revealed that facet opening was the strongest predictor for instability (odds ratio 5.022, p = 0.009) followed by spondylolisthesis, MRI grade and subchondral sclerosis. Forward stepwise multivariate logistic regression indicated that spondylolisthesis, MRI grade, facet opening and subchondral sclerosis of the facet were risk factors. Symptoms evaluated by the Short-Form 36 and visual analogue scale showed that patients with an unstable segment were in significantly more pain than those without. Furthermore, the surgical procedures determined using the intra-operative measurement system were effective, suggesting that segmental instability influences the symptoms of lumbar degenerative disease.

Segmental instability of the lumbar spine is awidely accepted biomechanical concept,1 butthe definition of instability in the clinical settingis controversial. The decision to perform a spi-nal fusion requires evidence of instability.Although the radiological evaluation of degener-ative lumbar spines is extensively performed,2-8

its usefulness in the diagnosis of instability isstill debatable because of the large range of nor-mal movement and the considerable overlap ofunderlying pathological conditions.3,9

The concept of ‘facet opening’ in the axialviews of T2-weighted MR images was recentlyproposed to indicate instability.10-13 The pres-ence of large fluid-filled facet joints indicatesthe likelihood of positional translation inpatients with spinal stenosis and spondylolis-thesis.10-13 A relationship, however, betweenthe appearance of the facet joints and the bio-mechanical properties of the spine, has yet tobe verified. Since 1997, we have been develop-ing a new intra-operative measurement (IOM)system (patented by the Japanese PatentOffice) to evaluate the mobility of a movementsegment when all ligamentous structures are

intact.14 In a recent study, we showed that anincrease in the volume of the facet joint mea-sured by three-dimensional (3D) reconstructedCT is evidence of spinal instability, as repre-sented by a greater neutral zone15 in the degen-erative lumbar spine.16

Our aim was to clarify the radiological find-ings which reliably predict instability in patientswho had undergone biomechanical evaluationusing the IOM system.

Patients and MethodsOur IOM system comprises spinous processholders (Gi-5; Mizuhoikakikai, Niigata,Japan), a movement generator (RC-RSW-L-50-S; IAI Corporation, Shimizu, Japan) and apersonal computer. The two holders were usedto grip the adjacent spinous processes firmly. Acyclic displacement in a single direction at aspeed of 2.0 mm/s was generated to the tips ofthe holders with a maximum displacement of15.0 mm from the neutral position. The latterwas defined as the position in which no loadwas recorded between the tips of the holders.Load at the tip of the caudal spinous process

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holders was measured by a load cell (LUR-A-200NSAI;Kyowadengyo Corporation, Chofu, Japan) and displacementusing an optical displacement transducer (LB-080; Keyence,Chofu, Japan). Real-time load-displacement data wererecorded using the personal computer. The spinous processholder was connected to the movement generator by a multi-directional ball joint, which produced flexion-extension ofthe segment (Fig. 1a). The range of movement induced bycraniocaudal displacements of the spinous processes of15 mm was approximately equal to 9° of flexion-extension ofthe movement segment. No adverse effects occurred as aresult of this forced movement.14

The patient was placed in the prone position on a Hall-type frame (Mizuho Ikakogyo Co., Ltd, Tokyo, Japan) withflexion of 20° at the hips and knees. The paraspinal muscleswere detached from the spinous processes in the usual way.

Spinous process holders were attached to the two adjacentspinous processes. All the ligamentous structures of the func-tional spinal unit, including the supra- and interspinous liga-ments and facet joints, were kept intact. The movementgenerator attached to the tips of the holders loaded the seg-ment, and produced cycles of flexion-extension segmentalmovement; real-time load-displacement data were obtainedwith a sampling rate of 5 Hz. Data from the third cycle wereused for biomechanical analysis.

We defined three movement parameters using the load-displacement data, namely, stiffness, the neutralzone,15,17 and absorption energy. Stiffness (N/mm) wasdefined as the slope of the line fitting the load-displacement curve from -15 mm to -10 mm on flexion.The neutral zone was defined as the reciprocal of the loadneeded to displace the tips of the two holders from a

Fig. 1a

Diagrams showing a) the intra-operative measure-ment system and b) the definition of the biomechan-ical parameters.

Fig. 1b

652 K. HASEGAWA, H. SHIMODA, K. KITAHARA, K. SASAKI, T. HOMMA

THE JOURNAL OF BONE AND JOINT SURGERY

distance of -5 mm (flexion) to +5 mm (extension). All thelines used for measuring stiffness and the neutral zonewere calculated using the least-squares method. Absorp-tion energy (J) was defined as the area of a hysteresis loop(Fig. 1b). In a previous series of 132 patients and eightnormal segments which underwent measurement usingthe IOM system, we found that the neutral zones of allnormal discs were < 2 mm/N.18 If a neutral zone value of2 is applied to a regression curve:

neutral zone = 1.514 to 1.606*Log(Stiff)

then stiffness = 0.496, a lower value than the minimumstiffness of normal segments. Therefore, instability wasdefined as a segment with a neutral zone,15 the most reli-able parameter for determining segmental instability,> 2 mm/N (Fig. 2).

In all, 112 patients, 56 men and 56 women, wereincluded in this study. Of these, 58 had lumbar degenera-tive spondylolisthesis, and 54 other degenerative diseases.Each had neurological symptoms and/or low back pain suf-ficient to warrant surgical treatment. Patients with scolio-sis, rotational deformity or a history of previous surgerywere excluded. The mean age of the patients was 66.5 years(27 to 84). The number of the measured segments were asfollows: L2-3, 2; L3-4, 39; L4-5, 63; and L5-S1, 1.Informed consent was obtained from each patient afterobtaining approval from the Committee of Medical Ethicsof Niigata University.

Lateral radiographs were obtained as follows: a filmwas set in the sagittal plane with the centre at around L3and x-ray source at a distance of 2.5 m; the voltage andelectric current of the exposure were 110 kV and 140 mA,respectively. The range of movement was determinedusing the procedure of Dupuis et al.2 The disc height was

calculated as the mean anterior and posterior disc heightdivided by the anteroposterior width of the upper verte-bra. MRI 1.5-Tesla scans were obtained for each patient.Disc degeneration was graded on T2-weighted midsagittalfast spin-echo images (repetition time 5000 ms/echo time130 ms).19,20 The 112 discs were classified as follows:19 grade III (inhomogeneous grey nucleus with uncleardistinction of nucleus and annulus); 70 grade IV (inhomo-geneous grey to black nucleus without distinction of thenucleus and annulus); and 23 grade V (black nucleus withcollapsed disc space). A CT scan with 2.5 mm thick slicesin the axial plane was performed after the MRI to identifythe bony structure in the supine position. The middleimage on the axial plane was used for evaluation of thefacet. The facet joint angle was measured using themethod of Boden et al.21 The facet shape was classifiedinto four types as follows: sagittally orientated, coronallyorientated, anisotropic and wrapped (Fig. 3). The widthof the facet joint space was measured perpendicular to thejoint at its widest portion, and the facet-opening wasdefined as a width greater than 1.5 mm (Fig. 4).12 Thefindings of degeneration namely, the vacuum phenome-non and the presence of osteophytes, subchondral ero-sion, cysts and sclerosis20 were also recorded.

The surgical procedure to be undertaken was decided onat the time of evaluation by the IOM system. If the neutralzone of the segment was < 2 mm/N, the segment was con-sidered to be stable and laminoplasty was carried out. If theneutral zone was ≥ 2 mm/N, the segment was considered tobe unstable and decompression and transforaminal inter-body fusion were performed. Both options were covered byinformed consent. For those patients who would not con-sent to a fusion, we performed a laminoplasty even if theywere shown to be unstable by the IOM systems. Conse-quently, laminoplasty was performed in 84 patients. Therewere 39 men and 45 women with a mean age of 68.7 years(41.0 to 84.0). Transforaminal lumbar interbody fusionwas carried out in 28. There were 17 men and 11 womenwith a mean age of 59.9 years (21.0 to 78.0) years. Eachpatient was evaluated using the Short-Form 36 (physicalfunction and pain domains)22 and a visual analogue scale(VAS) for pain in the leg and back.Statistical analysis. Before multivariate analysis, values ofneutral zone were correlated with the radiological findingswhich included degenerative spondylolisthesis, MRIgrade,19,20 MRI type according to Modic et al23 and the CTfindings: facet type, opening,12 and the presence of erosion,osteophytes, subchondral cysts, and sclerosis. A linearregression analysis was performed for the neutral zone withage, range of movement and disc height.

In order to identify the most critical risk factors for insta-bility, risk-factor analysis was performed on the radiologicalappearances by multivariate logistic regression with a for-ward stepwise procedure (p < 0.10 for entry). Goodness-of-fit and significance of the model were evaluated by probabil-ity profiles and a receiver operating characteristic (ROC).

Scattergram of the neutral zone (NZ) and stiffness showing the def-inition of biomechanical instability in 132 segments with degenera-tive disease and eight normal segments from previous studies.14

Fig. 2


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This is represented by plotting the fraction of true-positiverate versus the fraction of the false-positive rate. The areaunder the ROC curve is equal to the probability that themodel actually indicates instability.

The SF-36 (physical function and pain domains) andthe VAS (low back and leg pain) scores were obtained forpatients with and without instability and compared usingthe Wilcoxon rank-sum test. The effects of surgical treat-ment were investigated by comparing the same outcomemeasures before surgery and at final follow-up of thepatients treated by transforaminal lumbar interbodyfusion and laminoplasty using Student’s t-test with poweranalysis.

The JMP software package version 5.0.1a (SAS Institute,Cary, North Carolina) was used for all statistical analyses.A p-value ≤ 0.05 was considered to be significant.

ResultsCorrelation of the neutral zone with clinical, demographicand radiological factors. This zone was significantly greaterin patients with degenerative spondylolisthesis than inthose without (Wilcoxon rank-sum test, p < 0.01). The sag-itally orientated, coronally orientated, and anisotropicfacet types tended to have a higher neutral zone than thewrapped facets. Segments with facet opening also tended tohave a higher neutral zone than those without. There was

CT axial scans showing a) a sagittally orientated facet, b) an anisotropic facet, c) a coronally orientated facet and d) a wrapped facet.

Fig. 3a Fig. 3b

Fig. 3c Fig. 3d



no significant difference in the neutral zone based on theMRI classification, the MRI Modic type, vacuum, and thepresence of osteophytes, subchondral cysts or sclerosis ofthe facet (Table I).Risk factors and segmental instability. Using a forwardstepwise multivariate logistic regression analysis spondylolis-thesis, the MRI grade, facet opening, and subchondral scle-rosis of the facet were selected as risk factors (Table II). Ofthese, facet opening (odds ratio (OR) 5.022, chi-squared test,p = 0.009) was the strongest risk factor for identifying seg-mental instability (Table III). Probability profiles of instabil-ity in the multivariate logistic model were examined. If therewas degenerative spondylolisthesis, MRI grade 3 and 4, facetopening(+) and subchondral sclerosis(-), instability was pres-ent in 103 (91.6%) patients. If the segment did not havedegenerative spondylolisthesis, MRI grade 5, facet-opening(-) and subchondral sclerosis(+), the probability ofinstability was as low as 4.2%. The radiological findings,intervertebral disc height and range of movement were notpredictors of instability. The area under the ROC curve ofthe multivariate logistic model in our study was 0.75748,which could be generally interpreted as moderate accuracy.

The pain domain in SF-36 of patients with instability wassignificantly higher than that of patients without instability(Wilcoxon rank-sum test, p < 0.01). Conversely, the VAS oflow back pain in the patients with instability was signifi-cantly higher than that in the patients without instability(Wilcoxon rank-sum test, p = 0.0224; Table IV). After sur-gery, the physical function and pain domains of the SF-36improved significantly in both the transforaminal interbodyfusion and laminectomy groups (Student’s t-test p < 0.001).The VAS of low back pain and leg pain also significantlydecreased after surgery (Student’s t-test p < 0.001; Table V).Even in the patients who were unstable the physical functionand pain domains in SF-36 improved and the VAS of low

back pain and leg pain decreased significantly after surgeryin both groups (Student’s t-test, p < 0.001).

DiscussionWe investigated the radiological risk factors for segmentalinstability. Using forward stepwise multivariate logisticregression in 112 patients, spondylolisthesis, the MRIgrade, facet opening and subchondral sclerosis of the facetwere selected as risk factors. Of these, the latter was thestrongest risk (Table II). The facet joint is a crucial compo-nent in stability of the lumbar spine. The facet joints pre-vent excessive movement from damaging the discs and theposterior annulus is protected during torsion by the facetsurfaces and during flexion by the capsular ligaments.24-26

The compliance of the joint for torsion in a normal seg-ment, however, is quite low. The physiological range ofrotational movement is approximately 10° for the entirelumbar spine, or approximately 1° on each side for eachjoint.27 Joint failure can occur after approximately 10° to30° of torsion and irreversible damage to the joints willoccur when torsion exceeds 3°.28 Therefore, radiologicalabnormalities of the facet joints contribute to the diagnosisof segmental instability.

Recent MRI studies of the degenerative lumbar spinehave shown that the presence of a large fluid-filled joint,giving a high signal change on T2-weighted axial images,especially in the upright position, is related to instabil-ity.10,11,13 Chaput et al12 investigated MRI scans and stand-ing lateral flexion/extension radiographs in 54 patientswho had a degenerative spondylolisthesis and comparedthem with those in 39 patients who did not. They concludedthat large (> 1.5 mm) facet joint effusions are highly predic-tive of degenerative spondylolisthesis at L4-5 in the absenceof a measurable anterolisthesis on supine MRI. A normalfacet joint space is fairly narrow with a thick articular carti-lage and a tight capsule. Tears gradually accumulate in thearticular cartilage and joint capsule as degeneration pro-gresses, resulting in loosening of the joint which can be veri-fied by MRI or CT as facet opening. Segmental instability,represented by the neutral zone, worsens as the volume of thefacet joint space increases in the degenerative lumbar spine,16

in line with the clinical findings.10-13 Tropism of the lumbarfacet joint does not accelerate degeneration of the facet joint.Age, spinal level and the overall angle of the facet joint aremore important factors than tropism for degeneration of thefacet joint.29 In our study, facet type (Fig. 3) was not a predic-tor of stability, but comparison of the neutral zone among thefacet types revealed that the sagittally-orientated type tendedto be unstable, while the wrapped type tended to be stable.Subchondral sclerosis of the facet joint is considered to be asign of advanced degeneration of the segment. Most patientswith subchondral sclerosis had a hypertrophic facet withlarge osteophytes, and tend to have a ‘stable’ segment.

In our study the segments with MRI grade 3 or 4, whichcorresponds to mild disc degeneration, were more prone tobeing ‘unstable’ than those with MRI grade 5. Fujiwara et al30

CT scan showing details of facet opening.

Fig. 4


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investigated the relationship between the grade of degenera-tion (disc and facet joint) and segmental movement, andreported that movement increased with increasing severity ofdisc degeneration up to grade IV, but that it decreased in bothgenders when disc degeneration advanced to grade V. Axialrotational movement increased as the cartilage of the facetjoints degenerated suggesting that cartilage degeneration, and

especially thinning of the cartilage, caused capsular ligamentlaxity, allowing for abnormal movement or hypermobility ofthe facet joint.30 These findings are compatible with ourresults.

Increased range of movement on flexion-extension radio-graphs was not a significant predictor of instability and nei-ther was degenerative spondylolisthesis as a single factor.Matsunaga, Ijiri and Hayashi31 investigated conservatively-treated patients with degenerative spondylolisthesis over tento 18 years. Their mean age at the time of the initial exami-nation was 58.6 years. They noted that at the end of thestudy period (mean age 76 years), a total of 84 (76.4%) of110 patients who had had no neurological defect at the ini-tial examination remained without a neurological defectand also without progression of their spondylolisthesis afterten years. The natural history suggested that degenerativespondylolisthesis did not always lead to instability in elderlypatients who had probably reached a stabilisation phase32

corresponding to MRI grade 5.Low back pain was significantly more severe in patients

with instability (Table IV). Furthermore, the surgicaltreatment which was decided upon during surgery usingthe IOM system was effective (Table V). This suggestedthat segmental instability influenced the symptoms oflumbar degenerative disease. The aetiology of low back

Table I. Correlation of values of the neutral zone, mean (SD) with various radiological factors

Parameters Neutral zone p-value

Spondylolisthesis Yes (n = 58) No (n = 54)2.23 (1.12) 1.76 (0.95) < 0.01

MRI classification III (n = 19) IV (n = 70) V (n = 23)2.06 (0.96) 1.97 (0.97) 2.03 (1.42) 0.599

MRI Modic type 0 (n = 85) 1 (n = 10) 2 (n = 7) 3 (n = 3)2.05 (1.13) 1.97 (0.97) 1.90 (0.71) 1.33 (0.59) 0.611

Facet type* Sag#1 (n = 58) Cor#2 (n = 7) An#3 (n = 13) Wr#4 (n = 34)2.23 (1.21) 2.19 (1.03) 1.99 (1.23) 1.56 (0.49) 0.053

Facet opening Yes (n = 15) No (n = 97) 2.56 (1.49) 1.91 (0.96) 0.076

Erosion Yes (n = 16) No (n = 96)2.62 (1.27) 1.90 (1.00) < 0.01

Vacuum Yes (n = 63) No (n = 49)2.12 (1.20) 1.84 (0.85) 0.221

Osteophytes Yes (n = 69) No (n = 43)2.03 (1.07) 1.95 (1.06) 0.578

Subchondral cysts Yes (n = 25) No (n = 87)1.78 (0.90) 2.06 (1.10) 0.174

Subchondral sclerosis Yes (n = 69) No (n = 43)1.85 (0.90) 2.24 (1.26) 0.151

* Sag#1, sagittally oriented; Cor#2, coronally oriented; An#3, Anisotropic; Wr#4, wrapped

Table II. Results of forward stepwise multivariate logisticregression (p < 0.10 for entry) on segmental instability

Factor chi-squared p-value

Facet opening 5.962 0.0146Sclerosis 5.429 0.0198Spondylolisthesis(+) 8.692 0.0032MRI grade* 2.910 0.0881

* grade 5 versus grade 3 and grade 4

Table III. Results of the application of a model bylogistic regression analysis

Factor Odds ratio p-value

Spondylolisthesis(+) 0.240 0.005MRI grade* 2.381 0.146Facet opening 5.022 0.009Sclerosis 0.199 0.002* grade 5 versus grade 3 and grade 4



pain has not been clearly addressed. A variety of causessuch as degenerative disease of discs and/or facet joints,spinal deformity, lesions of muscle and/or fascia and evenpsychological factors is thought to give rise to low backpain. Segmental instability is merely the biomechanicalfailure of a lumbar segment and does not necessarily cor-relate with the degree of pain. Previous studies, however,have mostly identified instability using flexion/extensionradiographs and have not presented biomechanical mea-surements including the neutral zone, which is the key toidentifying instability. We are the first to define segmentalinstability in the clinical setting. Using a simple bio-mechanical method, we can show a relationship betweeninstability defined by an increased neutral zone and symp-toms (Table IV). Therefore we consider that segmentalinstability, if clearly defined from a biomechanical stand-point, can cause low back pain.

Probability profiles of instability were examined. If thelumbar segment showed degenerative spondylolisthesis,MRI grade 3 and 4, facet opening(+), and subchondralsclerosis(-), 91.6% of the segments were unstable. On theother hand, if the segment showed no sign of degenerativespondylolisthesis, MRI grade 5, facet opening(-), and

subchondral sclerosis(+), the probability of instability wasas low as 4.2%. Radiological findings, intervertebral discheight, and range of movement were not predictors ofinstability. These probabilities of instability calculatedfrom the combination of the risk factors corresponded tothe clinical findings. However, the area under curve of theROC of the multivariate logistic model showed only mod-erate accuracy indicating further studies are necessary toimprove the predictability of segmental instability byradiological methods.

This work was partially supported by the grant, Research Funding: AOSpineJapan.

No benefits in any form have been received or will be received from a com-mercial party related directly or indirectly to the subject of this article.

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Table IV. Mean (SD) outcome measures of the patients with and without instabilitydetermined by the intra-operative measurement system14

Instability

Outcome measure* Yes (n = 37) No (n = 75) p-value Power (%)

SF-36Physical function 54.4 (28.0) 65.2 (21.1) 0.0626 57.5Pain 49.9 (28.4) 65.6 (26.1) < 0.01 78.3

VASLow back pain 57.0 (23.1) 40.9 (29.4) 0.0224 78.9Leg pain 48.8 (32.8) 40.7 (33.3) 0.1798 21.3

* SF-36, Short-Form 36; VAS, visual analogue scale

Table V. Results of outcome measure (SD) after the surgical treatments determined by intra-operativemeasurement system

Outcome measure* Pre-operative Final follow-up p-value Power (%)

Transforaminal lumbar interbody fusionSF-36

Physical function 52.3 (17.5) 82.2 (14.9) < 0.05 100.0Pain 44.7 (20.0) 80.5 (21.1) < 0.05 100.0

VASLow back pain 67.7 (14.0) 24.6 (25.0) < 0.05 100.0Leg pain 70.1 (21.0) 14.3 (19.8) < 0.05 100.0

LaminoplastySF-36

Physical function 39.6 (16.4) 75.9 (16.8) < 0.05 100.0Pain 38.4 (20.3) 80.0 (17.6) < 0.05 100.0

VASLow back pain 64.3 (20.9) 28.2 (21.3) < 0.05 100.0Leg pain 68.8 (21.8) 19.2 (18.0) < 0.05 100.0

* SF-36, Short-Form 36; VAS, visual analogue scale


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