Lumbar Degenerative Spondylolisthesis Is Not Always Unstable€¦ · spondylolisthesis did not indicate instability, but facet opening and sagittally oriented facets were indicative

Spine www.spinejournal.com 2127

BIOMECHANICS

SPINE Volume 39 , Number 26 , pp 2127 - 2135 ©2014, Lippincott Williams & Wilkins

Lumbar Degenerative Spondylolisthesis Is Not Always Unstable

Clinicobiomechanical Evidence

Kazuhiro Hasegawa , MD, PhD , * Ko Kitahara , PhD , † Haruka Shimoda , MD , * Keiji Ishii , MD, PhD , * Masatoshi Ono , MD , * Takao Homma , MD, PhD , * and Kei Watanabe , MD, PhD ‡

DOI: 10.1097/BRS.0000000000000621

Study Design. A clinicobiomechanical study. Objective. To clarify the clinicobiomechanical characteristics of a segment with lumbar degenerative spondylolisthesis (LDS) using an original intraoperative measurement system. Summary of Background Data. Although radiographical evaluation of LDS is extensively performed, the diagnosis of segmental instability remains controversial. The intraoperative measurement system used in this study is the fi rst clinically available system that performs cyclic fl exion-extension displacement of the segment with all ligamentous structures intact and can determine both the stiffness (N/mm) and neutral zone (NZ, [mm/N]). Methods. Forty-eight patients with LDS (males/females = 19/29, 68.5 yr; group D) were compared with 48 patients with lumbar spinal stenosis without LDS (males/females = 33/15, 64.8 yr, group N) in terms of symptoms, radiological, and biomechanical results. Instability was defi ned as a segment with NZ more than 2 mm. Symptoms (36-Item Short Form Health Survey), radiographical fi ndings (radiographs, magnetic resonance images, computed tomographic scans), stiffness, NZ, and frequency of instability were also compared. Risk factors for instability were analyzed by multivariate logistic regression with a forward stepwise procedure. Results. None of the physical function categories or radiological fi ndings of 36-Item Short Form Health Survey and low back pain (visual analogue scale) differed signifi cantly between the groups. Although NZ was signifi cantly greater in group D (1.97) than in

From the * Niigata Spine Surgery Center, Niigata, Japan ; † Showa Ikakogyo Co. Ltd, Toyohashi, Japan; and ‡ Department of Orthopaedic Surgery, Niigata University Hospital, Niigata, Japan.

Acknowledgment date: June 9, 2014. First revision date: July 29, 2014. Acceptance date: August 22, 2014.

The device(s)/drug(s) that is/are the subject of this manuscript is/are not FDA-approved for this indication and is/are not commercially available in the United States.

Niigata Industrial Creation Organization grant funds were received to partially support this work.

Relevant fi nancial activities outside the submitted work: grants.

Address correspondence and reprint requests to Kazuhiro Hasegawa, MD, PhD, Niigata Spine Surgery Center, 2-5-22, Nishi-machi, Niigata City 950-0165, Japan; E-mail: [email protected]

Lumbar degenerative spondylolisthesis (LDS), initially described in 1930, 1 is a representative degenerative disease of segmental instability. Segmental instability

justifi es lumbar fusion surgery. 2 Lumbar segmental instabil-ity, however, is diffi cult to defi ne, whether or not spondylo-listhesis is involved. Although radiographical evaluation of degenerative lumbar spines is extensively performed to deter-mine segmental instability, 3–9 its usefulness for the diagnosis of lumbar segmental instability remains controversial because the large range of normal motion signifi cantly overlaps with underlying pathological conditions. 4 , 10–14 Furthermore, a bio-mechanically based conclusion about instability cannot be drawn, because the images do not provide information about the load-deformation behavior.

Since 1997, we have been developing a new intraopera-tive measurement (IOM) system to determine the lumbar segmental properties with all ligamentous structures intact. In the preliminary basic and clinical studies, we confi rmed that the IOM system safely and reliably provides multiple param-eters based on continuous load-deformation data obtained during surgery. 15 The purpose of this study was to clarify the

group N (1.73) ( P < 0.05), the frequency of instability did not differ signifi cantly between groups. Facet opening (odds ratio, 11.0; P < 0.01) and facet type (odds ratio, 6.0; P < 0.05) were signifi cant risk factors for instability. Conclusion. Neither the symptoms nor the frequency of instability differed signifi cantly between groups. The radiological fi ndings of spondylolisthesis did not indicate instability, but facet opening and sagittally oriented facets were indicative of instability. The results of this study demonstrated that LDS is not always unstable in the measurement setting, suggesting that the instability of LDS can stabilize spontaneously during the natural course. Key words: clinicobiomechanical study , facet opening , fl exion-extension , intraoperative measurement system , lumbar degenerative spondylolisthesis , neutral zone , restabilization , risk factor for segmental instability , segmental instability , stiffness , surgical treatment . Level of Evidence: N/A Spine 2014;39:2127–2135

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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BIOMECHANICS LDS Is Not Always Unstable • Hasegawa et al

2128 www.spinejournal.com December 2014

clinicobiomechanical characteristics of segments with LDS using our original IOM system.

MATERIALS AND METHODS The IOM system comprises spinous process holders (Gi-5; Mizuhoikakikai, Niigata, Japan), a motion generator (RC-RSW-L-50-S; IAI Corporation, Shimizu, Shizuoka), and a personal computer. The 2 holders were used to fi rmly grip adjacent spinous processes. A maximum cyclic displacement of 15.0 mm from the neutral position to both fl exion and extension direction was generated at a speed of 2.0 mm/s to the tips of the holders. Neutral position was defi ned as that in which no load was recorded between the tips of the holders. Load at the tip of the caudal spinous process hold-ers was measured with a load cell (LUR-A-200NSAI; Kyow-adengyo Corporation, Chofu, Japan) and displacement was measured using an optical displacement transducer (LB-080; Keyence, Chofu, Japan). Real-time load-displacement data were recorded using a personal computer. The spinous pro-cess holder was connected to the motion generator through a multidirectional ball joint, producing fl exion-extension of the segment ( Figure 1 ). The range of motion (ROM) induced by 15-mm craniocaudal displacements of the spinous processes was equivalent to approximately 9 ° of segmental fl exion-extension. This force motion causes no adverse effects. 15

The patient was placed in the prone position on a Hall frame with 20 ° -fl exed hips and knees. The paraspinal muscles were detached from the spinous processes using standard procedures. Two spinous process holders were attached to the adjacent spinous processes. All ligamentous structures of the functional spinal unit, including the supra- and inter-spinous ligaments and facet joints, were kept intact. The motion generator attached to the tips of the holders loaded the segment, producing 5 fl exion-extension segmental motion cycles, and real-time load-displacement data were obtained with a sampling rate of 5 Hz. Data of the third cycle were used for biomechanical analysis. We obtained biomechani-cal parameters, stiffness and neutral zone (NZ), 16 , 17 using the

load-displacement data. Stiffness (N/mm) was defi ned as the slope of the line fi tting the load-displacement curve from − 15 mm to − 10 mm on fl exion. NZ (mm/N) was defi ned as the reciprocal of the load necessary to displace the 2 tips of the holders from a distance of − 5 mm (fl exion) to 5 mm (exten-sion). All the lines used for measuring stiffness and NZ were calculated using the least squares method ( Figure 2 ). In a pre-vious series of 132 degenerative and 8 normal segments that underwent measurement using the IOM system, we found that the NZs of all cases with normal discs were less than 2 mm/N. If NZ = 2 is applied to the regression curve in the scattergram of stiffness and NZ: NZ = 1.514 − 1.606 × Log (Stiff), Stiffness = 0.496, a lower value than the minimum stiffness of normal segments. 18 Therefore, instability was defi ned as a segment with NZ, the most reliable parameter for determining segmental instability, 16 more than 2 mm/N ( Figure 3 ).

Forty-eight patients with LDS (mean age: 68.5 ± 9.0 yr, males/females = 19/29, group D) who presented with neu-rogenic claudication were included in the study. Exclusion criteria of the subjects were history of spinal surgery, spinal deformity, metabolic disease affecting bone quality ( e.g ., osteoporosis), vascular disease of the lower extremities, and malignant disease. The age-matched control group included 48 patients with lumbar spinal stenosis without spondylo-listhesis (mean age: 64.8 ± 11.0 yr, males/females = 33/15, group N; Table 1 ). None of the patients had a history of L5–S1 fusion or sacralized L5 vertebra. Informed consent for measurement using the IOM system was obtained from all patients following the approval of the Committee of Medical Ethics of Niigata University (approval no. 182, 2003).

Symptoms, and radiological and biomechanical results were compared between the 2 groups. Symptoms were evalu-ated using the 36-Item Short Form Health Survey (physical function) and visual analogue scale using the 100-mm method regarding low back and leg pain. Lateral radiographs were


Figure 1. Schema of the novel IOM system. IOM indicates intraopera-tive measurement system.

Figure 2. Defi nition of biomechanical parameters.




Figure 3. A scattergram of NZ and stiffness in 132 segments with de-generative disease and 8 normal segments. Stable zone represents the area in which stable segments with NZ less than 2 mm/N and stiffness more than 0.5 N/mm are included. NZ indicates neutral zone. 15 , 18 , 38

TABLE 1. Demographic Characteristics of Group D and Group N

ParametersGroup D (n = 48)

Group N (n = 48) P

Age 68.5 + 0.90 64.8 + 11.0 N.S.*

Sex (male/fe-male) 19/28 33/15 P < 0.005†

Frequency of L3–L4:L4–L5 13:35 33:15 P < 0.05†

Neurology

Rad/cauda 34/24 42/6 P < 0.05†

* χ 2 test. †Fisher exact test, 1-tailed test. Rad indicates radiculopathy; cauda, cauda equina symptom; N.S., not signifi cant.

obtained under the following conditions: lines between the bilateral acromion processes and iliac crests were perpendicu-lar to the radiograph with a 2.5-m distance from the x-ray generator to the radiograph, with 110 kV and 140 mA. ROM was determined using the procedure proposed by Dupuis. 3 Standardized disc height (stDH) was calculated as the mean value of the anterior disc height and posterior disc height (DHp) divided by the anteroposterior width of the lower vertebra ( W ) by using the formula: stDH = (anterior disc height + posterior disc height)/ W × 100. A grade of spon-dylolisthesis (%slip) was determined according to Taillard method. 19 Magnetic resonance images were obtained in all patients with a 1.5-T magnetic resonance imager. Grade of disc degeneration 20 , 21 and Modic type 22 were investigated on T2-weighted midsagittal fast-spin echo images (repetition time: 5000 ms/echo time: 130 ms).

A Shapiro-Wilks test revealed that the biomechanical data were not normally distributed. Thus, the value of each bio-mechanical parameter was compared between groups D and N using a nonparametric Wilcoxon signed ranks test, the Fisher exact test, or χ 2 test. Linear regression analyses were performed to identify relationships among ROM, DH, and the biomechanical parameters. To identify the most crucial risk factors for instability, risk factor analysis was performed for the pooled data among the radiographical parameters by multivariate logistic regression with a forward stepwise procedure ( P < 0.25 for entry and P < 0.10 for exclusion). Goodness of fi t and signifi cance of the model were evaluated with a receiver operating characteristic that is represented equivalently by plotting the fraction of true positive rate versus the fraction of false positive rate. The area under the receiver operating characteristic curve was equal to the prob-ability that the model actually indicates instability. The JMP software package (version 5.0.1a; SAS Institute, Cary, NC) was used for all statistical analyses. A P value of less than 0.05 was considered statistically signifi cant.

RESULTS Physical function of 36-Item Short Form Health Survey (group D: 50.4 ± 17.0, group N: 44.4 ± 15.0), low back pain (visual analogue scale; group D: 63.5 ± 19.6 mm, group N: 65.3 ± 17.4 mm) did not differ signifi cantly between the groups. Leg pain was signifi cantly greater in group D (77.4 ± 7.7) than in group N (55.8 ± 29.7; Figure 4 ). With regard to the radiological measurements, there was no signifi cant difference between groups in the range of segmental motion, stDH, Thompson classifi cation in magnetic resonance imag-ing (MRI), frequency of Modic type 1 change, or computed tomography (CT) fi ndings, except facet joint changes. On the contrary, the incidence of sagittal orientation (group D/N = 33/20, P < 0.05), subchondral osteosclerosis (group D/N = 37/23, P < 0.01), and cyst formation (group D/N = 17/4, P < 0.005) was signifi cantly greater in group D than in group N ( Table 2 ).

All intraoperative biomechanical measurements using the IOM system were completed within 10 minutes without any complications related to the procedure. The spinous process holders were stable even after 5 loading cycles in all cases. The mean stiffness value (mean ± standard error) in group D (0.686 ± 0.03) had a tendency of lower value compared with that of group N (0.797 ± 0.04, P = 0.0756), whereas the NZ in group D (1.97 ± 0.12) was signifi cantly higher than that in group N (1.73 ± 0.14, P < 0.05; Figure 5 ). The incidence of segmental instability (NZ > 2 mm/N), however, was not signifi cantly different between groups ( Figure 6 ).

Multivariate Risk Factor Analysis of Segmental Instability With a forward stepwise multivariate logistic regression ( P < 0.25 for entry, P < 0.10 for exclusion) on segmental instability, facet opening, subchondral sclerosis of the facet, type of facet joint, 18 level of disc for measurement (L3–L4 vs . L4–L5), stDH, and vacuum of the facet joint were selected as





Figure 4. Comparison of SF-36 physical function and visual analogue scale (100-mm method) regarding low back and leg pain between groups D and N. SF-36 indicates 36-Item Short Form Health Survey; N.S., not signifi cant.

risk factors ( Table 3 ). Spondylolisthesis and ROM by radio-graphical evaluation were not predictors of instability. The logistic regression model following the stepwise regression analysis on segmental instability revealed that facet opening and facet type (sagittally oriented, coronally oriented, and anisotropic vs . wrapped) were signifi cant factors, with an odds ratio more than 2 and P < 0.05 ( Table 4 ). The area under the receiver operating characteristic curve of the model in this study was 0.82, which could be generally interpreted as good accuracy.

Representative Case A 62-year-old female with L4 degenerative spondylolisthesis presented with neurogenic intermittent claudication ( < 50 m) with continuous numbness of the feet and diminished Achil-les tendon refl exes bilaterally. Flexion-extension radiographs revealed a subtle segmental motion and MRI showed cen-tral stenosis ( Figure 7A, B ). Because she did not complain of mechanical low back pain and facet opening was not observed in MRI or CT, we considered that the L4–L5 segment was not unstable 18 and decompression surgery was scheduled. Bio-mechanical measurement using the IOM system revealed the following: stiffness = 0.715 N/mm and NZ = 1.709 mm/N, which are within the stable zone in the NZ-stiffness scatter-gram ( Figure 7C ). The postoperative course after muscle-pre-serving interlaminar decompression 23 was uneventful and she was active without complaints of intermittent claudication at 2 years postoperatively ( Figure 7D, E ).

DISCUSSION Segments with degenerative spondylolisthesis are generally considered “unstable.” 24 Evidence to support this notion,

TABLE 2. Comparison of Radiographical Findings

Parameters Group D Group N P *

Range of motion† 7.2 + 6.5 4.6 + 6.0 N.S.

stDH 32.9 + 4.8 31.8 + 5.4 N.S.

MRI

Grade‡ III/IV/V III/IV/V

4/34/10 13/26/9 N.S.

Modic type 1 3 3 N.S.

CT: facet joint fi ndings

Type§ Sag 33 18 P < 0.05

Cor 2 4 N.S.

An 3 6 N.S.

Wr 10 20 N.S.

Opening ¶ 7 6 N.S.

Sclerosis � 39 20 P < 0.001

Cyst ** 17 4

*Fisher exact test (1-tailed). †Range of motion in fl exion-extension in sagittal plane radiograph. ‡Grade. 20 , 21 §Facet type. 18 ¶ Facet opening. 18 � Subchondral sclerosis of facet joint. **Subchondral bone cyst formation of facet joint. StDH indicates standardized disc height; Sag, sagittally oriented; Cor, coronally oriented; An, anisotropic; Wr, wrapped; N.S., not signifi cant; CT, computed tomography; MRI, magnetic resonance imaging.





Figure 5. Comparison of stiffness and neutral zone between groups D and N.

Figure 6. Comparison of the incidence of segmental instability between group D and group N. Inst ( + ): segments with segmental instability, Inst ( − ): segments without instability.

TABLE 3. Results of Forward Stepwise Multivariate Logistic Regression (P < 0.25 for Entry, P < 0.10 for Exclusion) on Segmental Instability

Factor χ 2 P

Facet opening 9.125 0.0025

Sclerosis 7.247 0.0071

Facet type* 4.203 0.0404

Level for measurement† 3.881 0.0488

StDH‡ 2.625 0.1052

Vacuum§ 2.487 0.1148

*Wrapped type vs . other types. †L3–L4 vs . L4–L5. ‡StDH was calculated as the mean value of the DHa and DHp divided by W as follows: stDH=(DHa + DHp)/ W × 100. §Vacuum in the facet joint. StDH indicates standardized disc height; DHa, anterior disc height; DHp, posterior disc height; W , anteroposterior width of the lower vertebra.

however, has not been presented from a clinicobiomechani-cal point of view. Moreover, the defi nition of clinical insta-bility of the spine is yet to be clarifi ed. For this reason, there are no clear radiological/medical indications for surgery for LDS or for a particular surgical approach compared with another. 25 Although there are several outstanding ex vivo

and animal studies of segmental instability, 16 , 26–31 there is a gap between the experimental results and clinical instabil-ity. Here, we attempted to bridge the gap between the basic biomechanical data and the clinical manifestations induced by instability.

Intraoperative measurements of a cervical or lumbar seg-ment are occasionally performed to determine instability. 32–34 Common limitations of the previously used measurements include damage to the ligamentous or bone structures due to the fi xation of pins, screws, or a spreader to the vertebrae, and also the fact that data about the stiffness of only a single load-ing direction, fl exion, or extension are obtained. From a bio-mechanical viewpoint, segmental properties of the spine can-not be determined by measuring stiffness alone. Measurements of multiple parameters, including the NZ, are necessary. 17 The IOM system presented here is the fi rst clinically available method that can be used for measurement with all ligamentous structures intact, and provides multiple parameters based on continuous load-deformation data during surgery. 15 There are several limitations of the IOM system: (1) The measurement was performed in the segment after the paraspinal muscles were detached from the spinous process under general anes-thesia in the prone position. These conditions are not physi-ological, and the results represent the effects of passive stabiliz-ers of the functional spinal unit. (2) Although the ROM in the measurement should be adjusted according to the physical size of the patient, to adjust the loading condition to each patient may be dangerous and biomechanically uncertain. Thus, we have continued to collect the data and confi rmed that the pres-ent condition was acceptable in the previous study. 18

Among the biomechanical parameters, the NZ is thought to be affected by degeneration, leading to painful motion. 17 An in vitro study of fresh human cadavers reported that the





Figure 7. A 62-year-old female with L4 degenerative spondylolisthesis presenting with typical neurological intermittent claudication. A , Preop-erative fl exion-extension radiographs. B , Preoperative T2-weighted MRI. C , Stiffness and neutral zone data of case 1, indicating that the data are within the stable zone of the scattergram in Figure 3 (arrow). D , Flexion-extension radiographs. E , T2-weighted MRI 2 years postoperatively in case 1, after muscle-preserving interlaminar decompression. MRI indicates magnetic resonance imaging. 23

NZ is slightly increased with greater disc degeneration in lumbar fl exion-extension motion. 29 Our measurement system demonstrated that segments with spondylolisthesis (group D) were characterized by lower fl exion stiffness and a higher NZ compared with those without spondylolisthesis (group N;

Figure 5 ). These fi ndings are compatible with a biomechanical background of MacNab hypothesis that osteoarthritis of the facet joints together with body weight induces subluxation at these joints, and then the superior vertebrae slip forward, producing spondylolisthesis. 24





Figure 8. Relationship between %slip 19 and neutral zone.

TABLE 4. Risk Factors in Logistic Model Following Stepwise Regression Analysis on Segmental Instability

Factor χ 2 Odds Ratio P

Facet opening 7.72 10.995 0.0055

Facet type (wrap)* 5.33 6.032 0.0210

Level† 2.05 2.483 0.1519

Vacuum‡ 2.40 2.873 0.1214

StDH 1.61 0.182 0.2040

Sclerosis 10.85 0.086 0.0010

The factors are presented in order of the odds ratio. *Wrapped type vs . other types. †L3–L4 vs . L4–L5. ‡Vacuum in the facet joint. StDH indicates standardized disc height.

Figure 9. Comparison of the scattergram of the stiffness and NZ between group D ( A ) and group N ( B ). NZ indicates neutral zone.

There was, however, no signifi cant difference in symptoms, except leg pain, and the frequency of Instability between groups ( Figures 4–6 ). Nor was there a signifi cant correlation between NZ and %slip ( Figure 8 ). The logistic regression model on segmental instability revealed that facet opening, facet type, level for measurement, and vacuum of the facet joint are signifi cant factors with an odds ratio more than 2, whereas radiological spondylolisthesis and ROM were not predictors of instability ( Table 4 ). These fi ndings are com-patible with those of previous studies regarding the impor-tance of facet joints rather than radiological spondylolisthe-sis or ROM of the segment. 18 , 35–39 Regarding the relationship between stiffness and NZ ( Figure 9 ), although the values in the scattergram in group D were located more outside the stable zone than those in group N, there were still cases from

group D inside the stable zone and from group N outside the stable zone ( Figure 9 ). According to the concepts proposed by Kirkaldy-Willis and Farfan, 40 disc degeneration progresses from “normal to dysfunctional, unstable, and restabiliza-tion” phases. On the contrary, a cadaver study 26 showed that segmental motion increases with an increasing severity of disc degeneration up to grade IV, but decreases when disc degeneration advances to grade V. 21 Segments with LDS are also considered to change spontaneously during the natural course of the degenerated segment, consistent with the present results. Namely, segments with LDS show more instability in the unstable phase than segments without LDS, but gradu-ally stabilized and fi nally settled down in the restabilization phase during the natural course ( Figure 10 ). Matsunaga et al 41 investigated conservatively treated patients with degenera-tive spondylolisthesis during 10 to 18 years. They noted that





Figure 10. A hypothesis regarding the alteration of segmental instabil-ity of degenerative spondylolisthesis in reference to the concept of the natural course of degeneration after Kirkaldy-Willis and Farfan. 40

at the end of the study period (mean age, 76 yr), a total of 76.4% of 110 patients with no neurological defects at the ini-tial examination remained without neurological defects and also without progression of their spondylolisthesis after 10 years. Huang et al 42 reviewed a consecutive series of 1490 lumbar spine CT scans for radiological evidence of spondylo-listhesis at either L4–L5 or L5–S1, and found that 20.9% of patients with lumbar spondylolisthesis had radiological signs of spontaneous fusion. The natural history suggested that degenerative spondylolisthesis did not always lead to insta-bility in elderly patients who had probably reached a stabi-lization phase or even spontaneous fusion. Our fi ndings are consistent with their results.

CONCLUSION To date, there has not been suffi cient evidence to draw con-clusions regarding clear indications for specifi c types of surgi-cal treatment for LDS, and thus there is a critical need for a decision-making tool to facilitate daily clinical practice and to assure the appropriate treatment. 25 , 43 The results of this study demonstrated that LDS is not always unstable in the measure-ment setting, suggesting that fusion surgery is not always indi-cated for patients presenting with spondylolisthesis. Surgical indication with or without fusion should be determined on the basis of consideration of the natural course proposed by Kirkaldy-Willis 40 in reference to clinical symptoms and disc and facet joint condition in MRI and CT.

➢ Key Points

Neither the symptoms nor the frequency of instability determined by the IOM system diff ered signifi cantly between groups with and without LDS. The radiological fi ndings of spondylolisthesis did

not indicate instability, but facet opening and facet type were indicative of instability. LDS is not always unstable or symptomatic,

suggesting that LDS instability can spontaneously stabilize during the natural course.

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Lumbar Degenerative Spondylolisthesis Is Not Always Unstable€¦ · spondylolisthesis did not indicate instability, but facet opening and sagittally oriented facets were indicative