Role of tectorial membrane in the stability of the upper cervical spine

Clin. Biomech. 1992; 7: 201-207

Role of tectorial membrane the upper cervical spine T Oda MD’, M M Panjabi PhD*,J D Grob MD~, J Dvorak MD~

in the stability of

J Crisco III Pm*, H U Bueff

MD*,

‘Department of Orthopaedic Surgery, Osaka University Medical School, Osaka, Japan; *Biomechanics Laboratory, Department of Orthopaedics and Rehabilitation, Yale University School of Medicine, New Haven, Connecticut, USA; 3Departments of Neurology and Ot-thopaedics, Wilhelm Schulthess Klinik, Zurich, Switzerland

Summary The purpose of this in vitro experimental study was to determine the role of the tectorial membrane in providing stability to the upper cervical spine. Five fresh human cadaveric specimens from the occiput to C3 were studied with a flexibility protocol: we applied the physiological moments of flexion, extension, right/left axial torques, and right/left lateral bendings (up to 1.5 N m), and recorded the ensuing three-dimensional intervertebral motions. Tests were performed in the intact state and then after transection of the tectorial membrane. This injury resulted in significant increases in flexion (6.7”, 28.4%) and axial rotation (5.9”, 7.8%) of Co-C,-C2 complex. Flexion increased at both Co-C, and Cl-C2 joints, while axial rotation increased mainly at Co-C1 joint. There were minimal changes in lateral bending (2.3”, 8.0%) and no changes in extension (0.7”, 3.5%).

Relevance The results of this study establish the role of the tectorial membrane in the multidirectional stability of the upper cervical spine. They may be useful for the diagnosis and understanding of whiplash neck injuries. The results suggest that the tectorial membrane could be irreversibly stretched, especially when the head is forced to both flex and axially rotate. Key words:

Upper cervical spine, instability, tectorial membrane,

Introduction

Due to the unique anatomy of the upper cervical spine, especially the lack of intervertebral discs and the horizontal orientation of the facet joints, the stability of this region is mainly dependent upon the soft tissues. Clinically, in many whiplash neck injuries the patients have various symptoms despite the absence of bony abnormalities seen on radiographic examination’. Therefore the soft tissues are suspected of being the main causes of the pathogenesis. The definite diagnosis of these soft tissue injuries is still difficult because the direct visualization of ligamentous structures by diagnostic imaging has not yet been established, and the role of the ligaments in providing stability of this Received: 16 August 1991 Accepted: 15 October 1991 Correspondence and reprint requests to: Professor M Panjabi, Department of Orthopaedics and Rehabilitation, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510 @ 1992 Butterworth-Heinemann 0268-0033/92/040201-07

Ltd

spinal biomechanics

region is not well understood. In vitro biomechanical studies may aid in solving the latter problem. Recently the effects of transection of the alar ligaments on in vitro kinematics of the upper cervical spine were reported by Panjabi et a1.233.By measuring the three-dimensional motions of the upper cervical spine before and after transection of the alar ligaments, they quantitatively clarified the roles of these ligaments in providing stability. The mechanical function of the Cl-C2 capsular ligaments has also been reported by Crisco et a1.4. They determined not only the effect of transection of the Cl-C2 capsular ligaments but also their interdependence with the alar ligaments in providing stability. The present study was designed to investigate the tectorial membrane in a similar manner. The tectorial membrane, a continuation of the posterior longitudinal ligament, is a broad and strong band passing over the dens and its ligaments’ (Figure 1). It is attached below to the posterior surface of the body of the axis, and to the upper surface of the occipital bone in front of the foramen magnum. Its deep layers also ascend on the medial sides of the

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membrane

longitudinal

Figure 1. Tectorial membrane connects the occiput to the axis, lies posterior to the transverse ligament, and is a continuation of the posterior longitudinal ligament. (Modified from Grey’.Anatomy)5.

atlanto-occipital joints to the margins of the foramen magnum. The mechanical function of the tectorial membrane was studied by Werne over 30 years ago6. However, it was a qualitative study. The purpose of the present in vitro study was to determine the effect of transection of the tectorial membrane on kinematic behaviour of the upper cervical spine, thus helping establish its role in stabilizing this region of the spine.

Methods

Five fresh human cadaveric specimens from the base of the occiput (C,) to C3 vertebra were used. The specimens were stored frozen at -20°C in double plastic bags until testing. Prior to testing the specimens were thawed and carefully dissected of all muscular tissues. Then C3 vertebra and the occiput were cast in plaster with two pairs of protruding threaded studs, inferiorly and superiorly. These studs permitted the specimen to be fixed at C3 to the testing apparatus and at Cc, to the loading jig. During casting the specimen was oriented in a normal upright posture defined by Braakman and Penning7. Accordingly the anterior vertebral wall of C3 was inclined anteriorly by 20” and the base of the occiput was horizontal. Specially designed photoradiographic markers with at least three non-collinear points were affixed to Co, Ci, and C2 to record three-dimensional movements of these joints without any contact of the measuring system. After setting the markers, two oblique and one lateral radiographs were taken to establish geometric relationships between each vertebra and the corresponding marker points. A flexibility protocol was employed as previously reported2T3,8,9, i.e. we applied the load and recorded the ensuing displacement. The applied load was a pure moment. We used six pure moments: flexion, extension, left and right axial torque, and right and left

lateral bending. These moments were applied to the occiput in a quasi-static manner in three equal load steps of 0.5 N m, to the maximum value of 1.5 N m. Each load step was maintained for 30 s for creep to take place. The specimen was preconditioned further with three load/unload cycles. On the third load cycle, the intervertebral motions were recorded at zero load and at each load step by stereophotogrammetry. The average three-dimensional rotational precision (1 SD) of our stereophotogrammetric system was 0.37”. Details of these methods can be found elsewhere2,3T8,9. We describe the intervertebral rotations by the average of the six permutations of the Euler angles. The rotations were computed with respect to a reference position (zero displacement), which was defined as the upright posture and obtained with an axial distraction force of 0.5 N applied to the occiput at the centre of the foramen magnum. The load-displacement behaviour was highly nonlinear. This non-linearity was documented by dividing the range of motion into two parts: neutral zone and elastic zone. These kinematic parameters were defined as: Neutral zone (NZ), displacement from the reference position to the zero-load position of the third load cycle; Elastic zone (EZ), displacement from the zeroload position to the maximum-load (1.5 N m) position of the third load cycle; Range of motion (ROM), sum of the neutral and elastic zones. Using the above-mentioned load application and motion measurement systems, the kinematic behaviour of the specimens was studied in two states: (i) Intact: the osteoligamentous specimen, carefully divested of all muscle tissue; and (ii) Tect. cut: a transection at the occipital attachment site and reflection to the C2 level of the tectorial membrane. This resulted in the exposure of the bilateral alar and the transverse ligaments. To determine the effect of this injury, all statistical tests employed repeated measures using analysis of variance (ANOVA) with a Fisher LSD post-hoc test (StatView SE +, Abacus Concepts, Inc., Berkeley, CA). The statistical significance was defined at PCO.05. Results

We present the results for both main and coupled rotatory motions due to the application of six pure moments. Main motion is defined as the motion in the same direction of the applied moment, and coupled motions are the motions in directions other than the main motion. Results consist of three formats: the average load-displacement curves for main motions, the ranges of motion presented as bar graphs, and the means and standard deviations of neutral zones and ranges of motion are presented in tables. Statistical significances are also presented in the tabular formats. Load-displacement

curves for main rotary motions

The average load-displacement curves for Co-C1 and C-C2 due to the flexion/extension moment are

Oda et al. :

respectively given in Figures 2a and 2b. Each figure has two curves: Intact and Injured (Tect. cut). Note that the curves were non-linear and there were similar changes at both CO-C1 and Ci-C2 with the transection of the tectorial membrane. With this injury there was increase in flexion, but no change in extension. Results due to axial torques are shown in Figures 3a and 3b. The curves were non-linear and almost symmetric. The greater part of axial rotation of +Cr--C2 complex occurred at Ci-C2. With the injury, there was some increase at CO-C. At Ci-Cz there was an increase in the NZ, but little in the ROM. Lateral bending results are given in Figures 4a and 4b. With the injury there was some increase in bilateral lateral bending at CO-Cr. Cl-C2 right lateral bending increased slightly, while left lateral bending decreased slightly.

Role of tectorial membrane

203

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Right -20

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a

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Load (N m)

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Ranges of motion

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Ranges of motion for main and coupled motions are shown in Figures 5a to 6b. In each of these Figures, the results due to a pair (positive and negative) of the same 20

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1

2

Flexion

b

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Figure 3. Axial rotation average load-displacement curves for: 0, the intact joints; and 0, after transection of the tectorial membrane. a, Co-C1 joint; b, Cl-C2 joint.

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I 0

I 1

I 2

Load (N m)

-10

t

Extension

I

I

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Figure 2. Flexion/extension average load-displacement curves for: 0, the intact joints; and 0, after transection of the tectorial membrane. a, Co-C1 joint; b, Cl+ joint. (Note the definitions of neutral zone and ROM.)

type of moment are presented. The Figure is divided into two sets: Intact and Tect. cut. For each set there are three bars (from the left to the right): the first represents sagittal plane rotation flexion when positive or extension when negative; the second bar represents transverse plane rotation - left axial when positive or right axial when negative; and the third bar represents frontal plane rotation - right lateral bending when positive or left lateral bending when negative. Thus, each set of three bars consists of one main and two coupled motions. Means and SD are shown. Flexion and extension moments (Figures 5a and 5b) In each figure the left side shows the results due to flexion moment and the right side shows the results due to extension moment. In flexion moment we see an increase of the main motion (flexion) due to the injury at both joints. Notice that the coupled motions were small and their changes due to the injury were also small. In extension moments there were minimum changes in all motions at both CO-C1 and Ci-C2 joints except coupled Ci-C2 axial rotation. Axial torques (Figures 6a and 6b) The results due to left axial torque are given in the left side and those due to right axial torque are given in the

204

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Clin. Biomech. 1992; 7: No 4

moment, while they increased at CO-C1 and decreased at Ci-CZ when applying left bending moment.

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Statistical significance

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The data and the results of statistical analysis are given in Tables 1 and 2. These results consist of only the main motions. The data in each table are divided into two parts: the neutral zone and the range of motion. The results are shown for CO-C2 and Ci-C2 motions.

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Flexion (Table 1A) Both parameters were larger at CO-C1 joint than at Ci-C2. With injury, neutral zones and ranges of motion increased at both joints. These increases were statistically significant except CO-C1 neutral zone. The magnitude of increase was larger at Ci-C:! joint than at c()-ci. Extension (Table 1B) Similar to flexion, extension was larger at CO-C1 joint

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I

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Figure 4. Lateral bending average load-displacement curves for: 0, the intact joints; and 0, after transection of the tectorial membrane. a, Co-C1 joint; b, Cl-C2 joint.

right side. At CO-C1 joint main axial rotation increased with the injury. Coupled lateral bending was small and changed its direction with the change in the direction of the applied torque. Another coupled motion (the sagittal plane rotation), with a large standard deviation, did not have a consistent tendency. These coupled motions did not change with the injury. At Ci-C2 joint there were minimal changes in all motions with the injury. Lateral bending moments (Figures 7a and 7b) The results due to right and left lateral bending moments are respectively given in the left and the right side of each figure. The main motion (represented by the third bar in each set) increased slightly with the injury at CO-Ci, but did not change at Cl--C2. The coupled sagittal plane rotation at CO-C1 had a large SD. That at Ci-C2 was a flexion and increased with the injury. Direction of the coupled axial rotation was different according to the direction of the applied moment and the level of the joint. In right lateral bending moment the coupled axial rotations were to the right at Co-C1 and to the left at Ci-C2 respectively. In left lateral bending moment they changed to the opposite directions. With the injury they did not change at both joints when applying right bending

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Figure 5. Ranges of motion due to flexion and extension moments. Means and SD are shown. Main and coupled rotations are given for the two states: intact and tectorial cut. El, Flexion/extension (main); Cl, axial rotation (coupled); ?? , lateral bending (coupled). a, Co-C1 joint; b, Cl-C2 joint.

Oda et al.: Role of tectorial membrane

15

Left

axial

torque

Right

axial

torque

r

205

There were minimal changes with injury. Significant increases were observed only for the ranges of motion of Co-C1 right and total lateral bending. The magnitude of increase due to the injury was less than 2” for the lateral bending to one direction. Discussion

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Intact

The most common method for determination of function of a specific ligament is to document mechanical properties of the specimen before and after transection of the ligament2~3,4~10.This study focused on the tectorial membrane as a specific ligament. Regarding the function of this membrane, there has been only one study (Werne6). Based on cadaveric experimental study and simple model analysis he concluded that the tectorial membrane has three functions: it checks extension at Co-Ci, flexion at Ci-C2, and extension at Ci-C2. He also stated that the membrane has no checking effect on axial rotation. Our results contradicted his conclusions in several aspects. Firstly after transection of the membrane flexion increased significantly not only at Cl-C2 but also at Co-C,, although the increase was larger at

Right lateral bending moment

Left lateral bending moment

I

Tectorial cut

Figure 6. Ranges of motion due to axial torques. Means and SD are shown. 8, Flexion/extension (coupled); 0, axial rotation (main); H, lateral bending (coupled). a, Co-C1 joint; b, Cl-C2 joint.

than at Ci-C2. There was no statistically significant change with the injury for any extension parameter. Axial rotation (Table 1C) Left axial rotations due to left axial torque are shown in the first row and right axial rotations due to right axial torque in the second row. In the third row the sums of the right and left axial rotations, which hereafter we call ‘total’ axial rotation, are represented. Axial rotation of Co-Ci-CZ complex occurred mainly at Ci-C2, i.e. 83% of total Co-C2 axial rotation took place at Ci-Cz. Although all presented values of the neutral zone increased with injury, none was statistically significant. Regarding the range of motion, the magnitudes of increase for total axial rotation were 4.5” at Co-C1 and 1.4” at Ci-C2. Significance was observed at Co-C,, but not at Ci-C2.

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Left lateral bending moment

Right

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b Lateral bending (Table 1D) Right and left lateral bending are shown in the first and the second rows, followed by total lateral bending (sum of the right and the left bending) in the third row. Lateral bending at CL-C2 joint was 73% of the total.

-101

-10

-

-20

-

I

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I Tectorial cut

Intact

Tectorial cut

Figure 7. Ranges of motion due to lateral bending moments. Means and SD are shown. 8, Flexion/extension (coupled); 0, axial rotation (coupled); W, lateral bending (main). a, Co-C1 joint; b, C,-Cz joint.

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Clin. Biomech. 1992; 7: No 4

Table 1. The means and SD (n = 5) of the neutral zones and ranges of motion for the intact specimens and after cutting the tectorial membrane

Range of motion (degrees)

Neutral zone (degrees) Increase with Tect. Cut

Intact Level

Mean

Mean l%/

[SD/

of the upper cervical vertebrae

Increase with Tect. Cut

Intact

Statistics

Mean

Mean

[SD]

[%I

Statistics

A. Flexion Co-G G-G

6.7 [5.8] 3.6 [2.8]

2.9 i43.71 5.4 [149.7]

NS S

12.7 [4.9] 10.9 f3.01

2.9 [22.8] 3.6 [33.4]

S S

8.3 [3.9] 3.3 Il.71

0.2 [2.4] 0.0 [I.21

NS NS

13.5 14.71 7.3 13.41

0.0 IO.31 0.7 [9.41

NS NS

6.7 6.0 12.7 27.5 35.3 62.8

[0.7] [3.5] [3.9] [5.6] 19.71 [14.5]

2.9 1.5 4.5 1.0 0.4 1.4

i43.31 [25.0] L35.41 [3.6] [I.11 [2.3]

4.3 3.5 7.8 9.4 12.3 21.6

il.11 il.11 [I.21 13.41 [6.0] [9.2]

0.9 1.1 2.0 1.1 -0.7 0.4

(20.91 [31.41 [24.7] [12.21 j-5.71 [I.91

B. Extension co-c1 G-G

C. Axial rotation Co-C1 Left Right Total C,-Cp Left Right Total

1.5 1.5 2.9 15.0 17.7 32.7

[I.11 13.11 14.11 14.31 [15.2] [ 16.91

D. Lateral bending Co-C1 Left Right Total C,-C2 Left Right Total

1.8 1.0 2.8 4.7 7.9 12.7

[I.91 il.51 [2.2] [2.3] i3.51 [5.7]

1.7 0.2 1.9 4.0 8.1 12.2

[116.4] [16.4] [66.4] [26.9] [46.0] [37.2]

NS NS

0.5 0.6 1.1 1.3 0.8 2.1

i30.31 [54.9] 139.31 [28.3] [9.8] [16.7]

NS NS NS

NS NS NS NS

NS NS NS

S NS

S NS NS NS

S NS

S NS NS NS

NS, not significant; S, significant increase using ANOVA and Fisher LSD statistical analysis at 95% confidence level.

Cr-&. Secondly there was no significant change in extension. Thirdly CO-C, axial rotation increased significantly with the injury. Werne’s work was a significant step in understanding the upper cervical kinematics, but his misconceptions may have been derived from the primitive methodology used. From our results we conclude that the tectorial membrane restricts CO-C2 flexion and axial rotation. After transection of the tectorial membrane flexion increased at both CO-C1 and Cl-C2 joints, while axial rotation increased mainly at CO-C1 joint. The tectorial

Table 2. Comparison motion

of the effect of different

injuries

membrane has no limiting effect on extension. With regard to lateral bending, this transection resulted in insignificant increases. Therefore the contribution of this membrane towards lateral bending stability is minimal. The same conclusion was reached while observing coupled motions. The only observed notable change was an increase of Cr-Cz coupled flexion. Recently Crisco et a1.4 determined the interaction and interdependency between the alar ligaments and the C1-Cz capsular ligaments in providing rotatory stability of the upper cervical spine rotation. Similar

on means

and

SD

of Co-C2

Intact

A. Neutral zones (degrees] Flexion Extension Total Axial Rot. Total Lateral Bend.

10.3 11.6 35.6 15.5

8.4 0.2 14.1 3.2

B. Ranges of motion (degrees] Flexion Extension Total Axial Rot. Total Lateral Bend.

23.5 20.8 75.5 29.5

6.7 0.7 5.9 2.3

Motion

zones and ranges of

Bilateral alars + tectorial membrane cut (n = 10)“”

Tectorial membrane cut In = 5)” Increase with injury

neutral

[%I

Statistics

[20.8]

NS NS NS

17.9 18.5 54.9 22.8

[28.4] L3.51

S NS

27.1 24.9 80.7 32.3

S

S NS

Intact

Increase with injury

f%l

7.4 2.3 13.2 6.0

t::.:; [24:0] [26.7]

7.7 2.5 9.5 4.4

[28.4] P.91 [Il.81 [13.51

*Results from this study. **Results from previous studies by Panjabi et al.2.3. NS, not significant; S, significant increase, using ANOVA and Fisher LSD statistical analysis at 95% confidence level.

Statistics

z S S

Oda et al.: Role of tectorial membrane

roles of the tectorial membrane and the alar ligaments can be studied by comparing the results of the present study with those of our previous alar ligament studies2T3. For this purpose we used the results of the ‘Bilateral alar’ state of these studies. Due to the impossibility of transecting the alar ligaments without injuring the tectorial membrane, the ‘Bilateral alar’ state was a combination of the transection of the bilateral alar ligaments and the tectorial membrane. Results of these studies, neutral zones and ranges of motion, are summarized in Tables 2A and 2B respectively. In these tables we present only the Co-C2 motions because both the tectorial membrane and the alar ligaments connect C0 with C2. For axial rotation and lateral bending, ‘total’ (which means sum of the right and left motions) values are presented. This is reasonable because both the structures and injuries are symmetrical about the sagittal plane. Referring to Table 2, in flexion the main structure providing stability appears to be the tectorial membrane, since the ranges of motion respectively increased by 6.7” (28.4%) with a single injury (this study), and by 7.7” (28.4%) with combined injuries (previous studies). Thus it may be concluded that the greater part of the increase was due to the tectorial membrane transection. The transection of the tectorial membrane produced no significant increase in extension motion, while the combined injury resulted in a significant increase. Thus, in extension the alar ligaments have a checking effect while the tectorial membrane does not. The magnitudes of axial rotation increase were 5.9” by a single injury and 9.5” by combined injuries. This suggests that two-step increases may occur if the sequential transections are performed. Therefore in axial rotation both structures contribute to stability. Similarly both structures seem to contribute to stability in lateral bending, but to a lesser degree than in axial rotation. There are, however, some limitations in comparing the findings of the studies. The most important is that they were based on different groups of specimens. In spite of using the same methodology, all ‘intact’ values in this study were smaller than those in the previous studies, most probably due to variations in the specimens. We have presented the results of the neutral zone and the range of motion in this study. Previous studies showed that the neutral zone was a more sensitive parameter than the range of motion concerning the kinematic effects due to the ligamentous n the present study this was true in flexion. Both the magnitudes and percentages of increases in flexion were larger for the neutral zone than for the range of motion. Although the mean NZ in axial rotation of Cr -C2 clearly increased more than the ROM (Figure 2a), this increase was not significant. The injuries233s1’d2.

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mechanisms for the difference in sensitivity between these two parameters are not well understood. Clinically the tectorial membrane has not been given much attention. But with a better understanding of the pathogenesis of whiplash injuries of the neck, the results of the present study may be useful for the diagnosis and understanding of its function. The results of the tectorial membrane study suggest that this membrane could be irreversibly stretched, especially when the head is forced to both flex and axially rotate. This is the same mechanism suspected in the alar ligament injury 2z10. In such a situation it is possible that the tectorial membrane is more vulnerable than the alar ligaments, because the failure load and deflection of this membrane were smaller than those of the alar ligaments in the in vitro biomechanical study13. Acknowledgement

Support was provided in part by the Center for Environmental Health and Injury Control Grant R49/ CCR103551. References 1 Hohl M. Soft-tissue Cervical Spine. 2nd 1989,436-41 2 Panjabi M, Dvorak ligament transection

neck injuries. In: Sherk HH et al. The edn. Philadelphia, JB Lippincott, J, Crisco J III et al. Effects of alar on upper cervical spine rotation.

J Orthop Res 1991; 9: 584-93 3 Panjabi M, Dvorak J, Crisco J III et al. Flexion, extension

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5 6 7 8 9

and lateral bending of the upper cervical spine in response to alar ligament transections. J Spinal Disord 1991; 4: 157-67 Crisco JJ III, Oda T, Panjabi MM et al. Transections of the Ci-C2 joint capsular ligaments in the cadaveric spine. Spine (In press) Williams PL, Warwick R. (ed) Gray’s Anatomy. 36th British edn. Philadelphia, WB Saunders, 1980: 449 Werne S. Studies in spontaneous atlas dislocation. Acta Orthop Stand [Suppl] 1957; 23: 38-62 Braakman R, Penning L. Injuries of the Cervical Spine. London: Excerpta Medica, 1971 Panjabi M, Dvorak J, Duranceau J et al. Three-dimensional movements of the upper cervical spine. Spine 1988; 13: 726-30 Panjabi MM. Biomechanical evaluation of spinal fixation devices: Part 1. A conceptual framework. Spine 1988; 13: 1129-34

10 Dvorak J, Panjabi M, Gerber M, Wichmann W. CT-functional diagnostics of the rotatory instability of upper cervical spine. 1. An experimental study on cadavers. Spine 1987; 12: 197-205 11 Panjabi MM, Abumi K, Duranceau J, Oxland T. Spinal stability and intersegmental muscle forces: A biomechanical model. Spine 1989; 14: 194-200 12 Panjabi MM, Duranceau JS, Oxland TR, Bowen CE. Multidirectional instabilities of traumatic cervical spine injuries in a porcine model. Spine 1989; 14: 1111-15 13 Myklebust JB, Pintar F, Yoganandan N et al. Tensile strength of spinal ligaments. Spine 1988; 13: 526-31