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Lumbar intradiscal pressure measured in the anterior and posterolateral annular regions during asymmetrical loading
Clinical Biomechanics 13 (1998) 495-505
Lumbar intradiscal pressure measured in the anterior and posterolateral annular regions during asymmetrical loading Thomas Steffena*, Hani G. Baramki, Rick Rubin, John Antoniou, Max Aebi Orthopaedic Research Laboratory, Division of Orthopaedic Surgery, McGill University, Montreal, Quebec, Cumda
Received 27 January 1998; accepted I April 1998
Abstract Objective. To analyze the effect of asymmetrical loading on intradiscal pressure. Design. Human cddaveric lumbar spines were instrumented with multiple pressure sensors and subjected to external mechanical loads. Background. Tears and radial fissures in the posterolateral annulus with no evidence of annular protrusion or nuclear extrusion are frequently observed in non-degenerated intervertebral discs. Cadaveric studies have shown that asymmetrical loads lead to posterolateral herniation. Regional overload may be responsible for a progressive structural weakness of the posterolateral annular fibres. Methods. Three needles each equipped with three independent pressure sensors were inserted in the midplane of the L.714 intervertebral disc (n = 16) in the anterior, right posterolateral and left posterolateral regions. Axial rotation was applied in the upright, flexed and extended positions and the pressures recorded. Results. The largest intradiscal pressure increase was observed in the posterolateral inner annular regions, more so in flexion than extension, when combined with axial rotation. Significant centripetal pressure gradients were found only in the posterolateral needles during the upright and flexed positions. Conclusions. When applying compression and axial rotation, the posterolateral inner annular zones of the intervertebral disc show high stress peaks and centripetal pressure gradients. Asymmetrical loads (rotation) combined with postural changes in the sag&al plane increase these effects, and may be responsible for a chronic mechanical overload of these regions.
Relevance Our findings suggest a predilection for the posterolateral inner annular regions to mechanical asymmetrical loading. 0 1998 Elsevier Science Ltd. All rights reserved.
failure,
especially
under
Keywords: intradiscal pressure; lumbar spine; mechanical stress; posture; degeneration
1. Introduction
Pressure measurements within the intervertebral disc (IVD) provide valuable information on the biomechanical behaviour of the IVD. Nachemson [l] was first to measure the pressure in cadaveric IVDs with a needle connected to an external electromanometer. Following these cadaveric IVD pressure measurements, Nachemson and collaborators measured IVD pressures in-viva for various body postures [2,3] and during *Corresponding author: T. Steffen Orthopaedic Research Laboratory, Division of Orthopeadics, McGill University, c/o Royal Victoria Hospital, 687 Pine Ave. West, Room LA.65, Montreal, Quebec, Canada H3A 1Al.
different lifting manoeuvres [4]. Their IVD pressure measurements showed that the nucleus pulposus behaved in a hydrostatic fashion in normal and slightly degenerated IVDs. The measured pressure was found to have a linear relation with the applied external loads, but was independent of the needle’s opening direction. In cadaveric studies the intradiscal pressure slightly increased when the specimen was subjected to positional changes such as flexion/extension, lateral bending, rotation and shear [5,6]. In attempts to better understand the mechanical behaviour of the annulus fibrousus, theoretical models were used that initially related the iannulus’ stress to the pressure measured within the nucleus pulposus
0268-0033/98/$19.00+ 0.00 0 1998Elsevier Science Ltd. All rights reserved. PII: SO268-0033(98)00039-4
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[1,7]. Recently, McNally [S] introduced a new technique called stress profilometry. A strain-gauged sensor mounted to a needle was passed incrementally along a straight path through the IVD along the mid-sagittal or the mid-coronal plane. Stress profiles were obtained from the cadaveric IVD with the specimen in either a pure flexion and extension position [8], or in a flexed and extended position combined with lateral bending [9]. Based on their findings, McNally suggested there was a predisposition to prolapse in IVDs that presented an abnormal stress concentration in the posterior annulus. Posterior IVD herniation (annular protrusion or nucleus extrusion) can be the result of a gradual process [lo, 111, rarely an isolated trauma [12], or a combination of both [12,13]. Tears and radial fissures in the posterolateral annulus with no evidence of annular protrusion or nucleus extrusion are frequently observed in non-degenerated or slightly degenerated IVDs [14,15]. Cadaveric experiments using cyclic loading in flexion combined with either side bending [l l] or rotation [16] have demonstrated that physiologically reasonable repetitive loads lead to posterolateral herniation. Hyperhexion alone, under large compressive forces that simulate an acute trauma, commonly results in a centrally protruding annulus [ 13,171. It therefore seems the posterolateral annulus fails mainly because of a chronic mechanical overload. A gradual degenerative process that weakens the posterior annular ring is likely to facilitate the development of a posterolateral IVD prolapse. Simultaneous, multilocalized IVD pressure measurements could render additional information on the actual IVD stress distribution, and would help to evaluate the effect of asymmetrical loads (e.g. flexion combined with axial rotation). Three needles (one anteriorly and two posterolaterally) each equipped with three strain gauge pressure transducers were inserted into the IVD to measure pressure in a simultaneous, multilocalized manner. A custom-made mechanical testing machine that allowed for six degrees of freedom (DoF) segmental motion was used for external loading. Complex loads (a combination of axial compression, flexion/extension and axial rotation) were applied to the multisegmental spine specimen while simultaneously measuring the IVD pressure.
Ten specimens were male and six were female. They were thawed at room temperature for 12 hours while still in their sealed bags. The specimen’s uppermost (LI/L2) and lowermost (Ls/SI) motion segments were fused with screws placed through the vertebral bodies. They were then embedded in cylindrical blocks (12 cm diameter) of dental plaster so that the L3/L4 IVD plane was parallel to the attachments. The mechanical axis of axial loading was therefore perpendicular to the L3/L4 motion segment. Additional screws were used to better anchor the vertebral bodies of L, and S, within the plaster. All specimens were radiographed to exclude gross morphological anomalies (e.g., disc space narrowing, large osteophytes, skeletal anomalies, etc.). The tissues were wrapped in wet gauze during the entire procedure to minimize dehydration. 2.2. Testingmachine set-up The specimen was rigidly attached to the testing machine by fixing the cylindrical blocks to the upper and lower platforms (Fig. 1). The upper platform’s displacements were controlled by three independent stepper motors interfaced to a computer. The stepper motors could independently apply axial compression, axial rotation and flexion/extension loads. The lower platform allow low friction movement in three axes: lateral bending, and linear displacement along the two horizontal axes. Each of the lower platform’s three degrees of freedom (DoF) could be individually blocked. Together, the two platforms allowed up to six DoF motion. The lower platform incorporated a strain gauge load transducer (F/T system, Assurance Tech., garner NC, USA) that measured Cartesian force/ torque components in six DoF (Fig. 1).
2. Methods
2.1. Specimenpreparation Sixteen human cadaveric lumbar spine specimens (L,-S,) were collected from autopsies no later than 24 hours post mortem. The specimens were vacuumsealed and frozen for up to 3 months at -20°C [18]. The average age was 46.3 years (range 29-63 years).
Fig. 1. Mechanical testing apparatus for cadaveric spine testing. Legend: UF = upper fixation, LF = lower fixation, LC = load cell, MS = motion sensor, N = needle.
T. Steffen et al./Clinical
Biomrchanics
An electromagnetic cobchester position sensing system (FASTKAK, Polhemus, VT, USA) was used to measure the relative kinematics of the h, Lj, L4 and L5 vertebral bodies. Threaded Kirschner wires mounted with lightweight position sensors (2.5 mm diameter) were rigidly placed in the L,, L3 and L, vertebral bodies. A fourth position sensor was attached to the testing machine’s lower platform. Because the LZ vertebra and the load transducer were both rigidly attached to the lower platform, knowledge of its position was given. To avoid erroneous position readings caused by metal interference, the amount of metal in the vicinity of the measurement system was reduced (e.g. both mounting platforms were made of Plexiglas@).Based on results from previous studies with similar experimental conditions [ 191 the method’s accuracy was estimated to be on average 0.1” (CI 95%: 0.00-0.43”) and 0.23 mm (CI 95%: 0.0-0.8 mm). An initial calibration was done by recording the starting position of the upper endplates of L3, L4 and L!; in a neutral posture. A series of points were recorded along each endplate’s outer contour using an electromagnetic position sensor mounted to a calibrated stylus. The series of points for each endplate recorded in three dimensions was used to determine the endplate’s centroid and plane of best fit, An additional landmark (recorded in the posterior midsagittal area of the spinous process) was used to complete the definition of the vertebral body’s local coordinate system [20]. Relative segmental motion was
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calculated using the adjacent vertebral bodies’ local coordinate systems. A computer (Apple Quadra 650) customized with controlling software (LabView 3.01, National Instruments, Austin TX, USA), was responsible for reading and processing load, position and pressure values, as well as controlling the stepper motors in preprogrammed load sequences. 2.3. Pressure-measuring needles
The custom-made needles (2.1 mm diameter) were each equipped with three independent 1.6 mm diameter strain gauge pressure transducers. The transducers were mounted at a distance of 5.5, 8.5 and 11.5 mm from the tip (Fig. 2). All needles were inserted in the mid-plane of the L,/‘L, IVD (Fig. 3). One needle was placed anteriorly in the mid-sagittal plane, and the remaining two needles were inserted in the posterolateral left and right positions (at the point corresponding to the medial border of the lower pedicle and at an angle of 30” relative to the sagittal plane). The needles were gradually advanced into the IVD until the sensors were at a distance of 6, 9 and 12 mm from the outer IVD border facing upward. Each needle was fixed in place with a suture. All pressure sensors were calibrated before and after each experiment by inserting the needles into a pressure chamber. The chamber pressure was gradually decreased from 1800 kPa to 0 kPa over a time of 30 seconds, and output voltages were simultaneously
PL Fig. 2. Diagram of the needle with the three mounted sensors.All measurements are in millimeters.
-
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f.-~-
5.5_.~,
Biomechanics 13 (1998) 495-505
18.5 * 3.0, +3.0+ +-------------+
~~ Fig. 3. Needle positions within the L3/4 disc. Legend: NP = nucleus pulposus, AF = annuhrs fibrosus, A = anterior needle position, PL = posterolateral needle position, S = sensor.
recorded with a reference pressure gauge of 0.5% static accuracy (Cole-Parmer Instrument Company, Chicago IL, USA). A linear least square fit was performed to map each pressure transducer’s voltage into kPa recorded with the reference gauge. The static accuracy of each sensor was less than 3% full scale for all error sources (i.e., non-linearity, reproducibility, hysteresis). An ANOVA model was used (Statview Ver. 4.0, Abacus Concepts Inc., USA) to evaluate the effect of different factors on the recorded pressure measurements. These factors included: (i) needle position (anterior, posterolateral left, posterolateral right); (ii) sensor distance from the outer IVD border (6, 9 and 12 mm); (iii) loading condition (upright, flexed, extended); (iv) direction of axial rotation (leftneutral-right cycle, right-neutral-left cycle); and (v) specimen (sample number). As the data obtained from the two posterolateral needles were mirrored (leftright), comparison of these two sets of data allowed assessment of the method’s reproducibility for measuring intradiscal pressure. A systematic measurement bias (e.g. artifacts at the sensor-tissue interface) could not be excluded. However, the differential pressures used in subsequent data analyses were not affected by a systematic measurement bias. IVD pressures measured at the same sensor distance, the same needle position and in the same loading condition were pooled and the average was calculated. This average was used for all subsequent data analyses. Paired t-tests were used to detect any significant change in the average pressure when the specimen was moved from the upright neutral position to the other positions. The pressure gradients across the three sensors of any given needle and position were calculated using multilinear regression. 2.4. Loading protocol
A 300 N axial compression was maintained for 15 min to compensate for possible post mortem hyperhydration of the IVD. We recorded the IVD pressure patterns during 10” of axial rotation to each side with an adjusted axial load of 600 N in three different
positions*: upright, 15” flexion and 10” extension. These displacements were for the whole specimen. Two cycles of preconditioning preceded the actual recording cycle in each position. The recording cycle consisted of a left-to-right cycle and a right-to-left cycle. L3/L4 segmental flexion/extension and axial rotation angles were calculated using the position sensor data. 2.5. Post-experimental analysis
The L3/L4 segment was isolated after the experiment (Fig. 4, part A) and cut along the sagittal plane for IVD degeneration grading (Fig. 4, part B). The Thompson degeneration grading system [21] was used to quantity the degradation stage of each IVD. Any IVD with a Thompson grade of four or five (highly degenerated) was excluded from the study. The two hemivertebrae obtained by the sagittal cut were cut a second time along the mid-transverse plane of the IVD (Fig. 4, part C). The different IVD zones (annular, intermediary, and nuclear) were identified on the slices obtained. Along the needle’s insertion path structures found at 6, 9 and 12 mm from the outer IVD border were identified. These points corresponded to the location of the individual pressure sensors within the IVD. 3. Results The ANOVA model revealed that the largest influence on the pressure outcome was caused by the needle position, followed by the loading condition and the sensor distance from the outer IVD border (all p
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the pressure (p = 0.69 and 0.14, respectively). Consequently, pressures measured at the same position and for the same loading condition during the two different rotation cycles were averaged for subsequent data analysis. Table 1 and Table 2 list the mean pressure values obtained from the 16 specimens. There was no statistically significant difference between the pressures measured by the left and the right posterolateral needles during ipsilateral rotation or contralateral rotation (Table 1). Similarly, there was no statistically significant difference between the pressures measured by the anterior needle in the left rotation and the right rotation positions (Table 2). These findings underline the reproducibility of the measurement technique. The data were subsequently regrouped as follows: the pressures measured by the two posterolateral needles in the ipsilateral rotation position were pooled; the pressures measured by the same needles in the contralateral position were pooled; the pressures measured by the anterior needle in the left and right rotation positions were also pooled (Fig. 5). Figure 6 represents the change in pressure when comparing the pressures in the different postures with
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the upright neutral position. Significant pressure changes were found mainly in the rotated positions, with the highest pressure increase measured in the ipsilateral posterior needle for flexion combined with rotation (590 kPa), followed by the contralateral posterior needle for extension combined with rotation (423 kPa). The pressure gradients across the three sensors of the same needle in the different positions were calculated (Fig. 5). Significant pressure gradients were found in the posterolateral needles in the upright and the flexed posture for both the neutral and the two rotational positions. All pressure gradients were directed towards the nucleus (i.e. higher pressure values in the annular region). The highest gradient (60.6 kPa/mm) was found in the posterolateral during rotation to the ipsilateral side in flexion. The kinematic and kinetic data measured for the L3/L4segmental level are presented in Table 3. Because standardized displacements were applied to a multisegmental specimen, there exists a considerable intersample variation for the actual LJ4 segmental ROM. Regressions regions ran between the different sensor locations and segmental displacement amplitudes or angular moments generally had significant p-values, thus indicating a direct relationship between segmental displacement and intradiscal pressure rise, but the 2 values were consistently low. Also, no direct correlation could be established between IVD degeneration (Thompson grading) and IVD pressures. The IVD gross morphological evaluation of the hemivertebrae (Thompson grading) showed that 13 IVDs had a Thompson grade II and three IVDs had a Thompson grade III. One IVD was found to have a Thompson grade IV and was subsequently excluded from the study. The localization of the various pressure sensors within the IVD tissue as observed on the transverse cuts is given in Table 4. 4. Discussion 4.1. Pathophysiology of disc mechanical failure
C
Fig. 4. Steps in the cutting technique for the post-experimental disc analysis.
Nuclear herniation through the annulus occurs predominantly in the posterolateral area of the IVD [15]. It has been shown that the natural history of a “non-acute” IVD prolapse starts with morphologic changes in the inner annular zone. Decomposition of the lamellar structure [22-241 accompanied by a fibrous substitution of the matrix [25] is followed by focal tears that spread radially outwards [26]. The annulus weakens and finally permits the nuclear material to herniate. Fatigue testing mimicking a chronic mechanical overload has been used in ex-vivo studies to investigate IVD mechanical failure and to reproduce IVD protrusion and herniation [lo, 11,161.
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The predilection of this phenomenon to the posterolateral IVD regions suggests the presence of a regionspecific mechanical cause that precipitates its occurrence.
The complex anatomy of the IVD results in a non-homogeneous stress distribution throughout the IVD. In addition, this stress distribution changes with different positions and under different loads. In our
Table 1 Mean pressure values in kPa (standard error of the mean in parentheses) measured by the posterolateral left and the posterolateral right needles in the upright, flexed, and extended positions. For each position the pressure was recorded in neutral as well as in lo” rotation to both the ipsilateral and the contralateral sides. Thep-values represent the results of a paired t-test performed between the left and right needle data sets. Position
Rotation
Sensor (mm)
Posterolateral left needle
Posterolateral right needle
p-value
Upright
Neutral
12 9 6 12 9 6 12 9 6
822.2 (51.9) 956.8 (83.3) 1066.0(93.1) 924.6 (59.2) 1061.5(85.0) 1169.6(97.1) 945.4 (61.1) 1059.9(88.6) 1200.2(103.5)
871.2 (81.4) 928.5 (71.3) 1032.2(92.4) 971.1 (89.1) 1032.7(78.6) 1145.6(102.6) 970.0 (82.4) 1042.3(74.1) 1166.6(96.4)
0.425 0.357 0.621 0.587 0.663 0.641 0.401 0.274 0.668
12 9 6 12 9 6 12 9 6
899.8 (76.8) 1003.6(88.7) 1151.2(111.0) 1259.1(107.2) 1382.1(110.3) 1638.8(122.9) 984.0 (89.0) 1087.2(103.0) 1243.4(127.6)
911.8 (82.3) 1006.6(78.7) 1151.7(109.6) 1279.3(107.8) 1434.6(105.8) 1622.0(121.6) 1012.2(96.4) 1083.9(90.1) 1156.7(90.1)
0.084 0.919 0.645 0.911 0.939 0.132 0.094 0.438 0.483
12 9 6 12 9 6 12 9 6
950.7 (121.0) 973.2 (93.7) 1053.8(96.2) 995.4 (134.7) 1016.0(102.6) 1078.0(104.9) 1347.8(141.5) 1316.5(93.0) 1430.1(113.2)
893.3 (100.4) 929.1 (72.8) 969.9 (83.6) 1251.9(120.6) 1001.1(88.6) 1042.8(98.9) 1548.0(99.3) 1389.7(99.2) 1489.3(105.2)
0.126 0.248 0.081 0.235 0.474 0.775 0.082 0.703 0.525
Ipsilateral Contralateral
Flexion
Neutral Ipsilateral
Contralateral
Extension
Neutral
Ipsilateral Contralateral
Table 2 Mean pressure measured by the anterior needle in kPa (standard error of the mean in parentheses) in the upright, flexed, and extended positions. The pressure was recorded in neutral as well as in lo” rotation to both the left and right side. The p-values represent the results of a paired t-test performed between the left and right rotation data sets. Position
Sensor (mm)
Pressure in neutral
Pressure in rotation Left
Right
p-value
Upright
12 9 6
775.8 (91.0) 906.3 (77.5) 858.9 (96.8)
886.1 (90.5) 1032.9(71.9) 998.0 (94.2)
916.6 (90.0) 1049.6(91.8) 1033.8(89.7)
0.221 0.651 0.309
Flexion
12 9 6
810.9 (94.1) 923.1 (87.8) 949.3 (111.2)
939.3 (96.4) 1001.6(98.1) 1085.7(110.8)
948.4 (101.3) 1050.1(110.5) 1101.4(115.7)
0.750 0.925 0.694
Extension
12 9 6
895.8 (103.0) 1016.4(89.5) 926.4 (93.6)
990.3 (107.6) 1120.4(93.3) 1035.5(91.5)
994.7 (92.2) 1136.6(96.5) 1057.9(94.5)
0.881 0.556 0.462
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4.2. Intradiscal stress distribution
Although measuring stress within the IVD is not possible, intradiscal pressure measurements are
Neutral Wal 2ooo
23.0 (0.318)
40.9 (0.009)
---*--*.-.**..-..-.-----.-----*.-.*-..*.-.--.--.-.---....-.--.--~~~~~~-....~-.......~.~*.
0
VW 2ooo
-9mm
13.6
34.4 (0.011)
Rotation
[kPa/km] 25.1 (p-v@ue) (0.129) x
60.6
33.9
(0.002)
(0.048)
ant
pl/ipsi
plkontra
35.6 (0.014)
38.0 (0.009)
l
[kPa/Lm] 18.9 (p-value) (0.192)
*
.
4.7
ant
1
ant
ant Wal
-6mm
1
ant (0.520)
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thought to be a good indicator of stress. McNally et al. reported reliable measurements obtained [W’l throughout the nucleus pulposus and annulus fibrousus of IVD’s when using a similar pressure sensor passed incrementally through the disc. Experimentally, the ability of their technique to quantify matrix compressive stress has been demonstrated 1281.Stress distribution derived from a pressure profile obtained along the mid-sagittal axis of the IVD showed the presence of stress peaks in the posterior annulus at a distance
study, we investigated the possibility that certain postural changes may cause a localized overload in the posterolateral inner annular region. This overload could lead to structural weakness in this region and subsequent nuclear prolapse.
n112mm
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15.4
[kPa/km]
8.6
ant
PVipsi plkontra -9.0
pl/ipsi
2.7
plkontra
Fig. 5. Mean pressure and standard error bars in kPa for the different sensor locations (ant = anterior. pl = posterolateral) and for all positions (flexion, upright, extension). In rotation, the posterior pressure measurements are shown separately for the ipsi- (pliipsi) and contralateral (PI/contra) needle positions. Different sensor distances to the outer IVD’s border are identified by different filling patterns. The average pressure gradient is calculated using linear regression over the span of the three adjacent sensors of any given needle location and s expressed in kPa/mm, with positive pressure gradients in the centripetal direction. p-values for a gradient different from zero are given in parentheses, significant gradients @ ~0.05) are identified with an asterisk (*),
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varying from 4 mm to 12 mm from the posterior IVD border [9]. Intervertebral discs analysed in our study had a Thompson degeneration grade II (81%) or grade III (19%) which indicate a compact nucleus with no tears
0
Wal
12mm
and a preserved gelatinous kernel. The zone at the junction of the nucleus and the annulus is characterized by a gradually decreasing proteoglycan and water content, and an increasing amount of non-oriented fibres [25,29] This intermediary zone is therefore not
-9mm
Neutral
-6mm
1
Rotation
800 600 400 200 0
ant
I
ant
pl/ipsi plkontra
. t
ant pl/ipsi plkontra
800 P ‘; 400 c a, 200 fi
0
@ -200
ant pl/ipsi plkontra
ant
Fig. 6. Mean pressure differences and standard error bars in kPa for all positions with respect to the upright neutral position (for legend see Figure 5). The differences are calculated for each separate sensor location. Significant differences (paired I-test, p~O.01) are indicated with an asterisk (*).
Table 3 L3/L4 mean angular displacements (n = 16) recorded with the electromagnetic tracking system and mean moments at the end positions recorded with the load cell. Values in parentheses indicate standard deviations. The upright posture was defined in neutral axial rotation with the load cell reading zero moment in the sagittal plane. Posture
Upright Flexion Extension
One side axial rotation
Flexion/extension
Angle 0
Moment (nm)
-hle
2.3 (0.8) 2.5 (0.9) 1.9 (0.6)
19.0 (5.1) 16.8 (7.0) 15.4 (4.2)
Defined at 0 4.9 (2.4) 1.8 (0.7)
--___-~-.
(“1
Moment (nm) 0.0 (0.1) 12.3 (3.9) 8.4 (2.8)
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Table 4 Number of sensors (for each needle and sensor location) found in any of the three disc zones. The sensor locations were evaluated from post-experimental transversal cuts through the L3/L4 discs (n = 16). Needle
Sensor (mm)
Nuclear zone
Intermediate zone
Annular zone
Anterior
12 9 6 Total
13 0 0 13
3 9 0 12
0 7 16 23
Posterolateral (left)
12 9 6 Total
16 I 0 23
0 I 1 8
0 2 1s 17
Posterolateral (right)
12 9 6 Total
15 9 0 24
1 6 2 9
0 1 14 15
expected to behave in a purely hydrostatic fashion. Non-homogeneous stress distributions are likely to be observed across this zone. We inserted the pressure needles to a fixed depth in the anterior region and the two posterolateral regions, which resulted in stationary sensor positions at 6, 9 and 12 mm from the outer IVD border, facing upwards. Since the posterior annulus extends to an average of about 7 mm and the anterior annulus to about 9 mm from the outer IVD border, the span of the three sensors was expected to cover the area of the innermost annular fiber layers and the intermediary zone (Table 1). This area corresponds to the above mentioned site of expected non-homogeneous stress distribution. Because the sensors were not in the center of the nucleus (with its known hydrostatic behaviour), the pressure readings may be different for sensors facing sideways and upwards. In our experiment only results from the upward facing sensor position were analysed. The stationary placement of the needles provided identical measurement sites so that pressure readings obtained under different loading regimens could be compared. Asymmetrical trunk motion, such as rotation [30,31] and lateral bending [10,32], play a major role in the development of a posterior IVD prolapse, making it essential that the three needles inserted in the IVD allow simultaneous analysis of asymmetrical stresses in the left and right posterolateral, as well as the anterior annular regions. This made it possible to investigate the pressure distribution within the IVD under asymmetrical loading regimens. Multisegmental spine specimens were used for the study because they provide more realistic mechanical testing conditions [18]. As a result, a larger number of
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multisegmentally inserting ligaments were preserved, and the mechanical restraints on the specimen by the testing machine were reduced. The G4 disc level was chosen for instrumentation in order to have one intact lumbar disc level above and below. In addition, the L3/4 intervertebral disc showed less degenerative changes, therefore made the IVDs of the different specimens more uniform. 5. Interpretation
In the upright neutral position and under an axial load of 600 N, the pressures recorded by the sensors closest to the nucleus were around 0.8 MPa and increased in the sensors located closer to the annulus fibrousus (Fig. 5). Based on the data of Brinckmann and Grootenboer 1331,and assuming a linear relationship between axial load and intradiscal pressure, one would expect for a 600 N axial loacl, an intradiscal pressure of approximately 0.7 MPa at the center of the disc. The three needles inserted into the same disc increased its volume by 0.08 ml, which would result according to Ranu [34] in a 26 kPa pressure rise, which partially explains the higher pressure observations. The inner most sensors were not located in the nucleus’ center and, considering the increased pressure in the annular regions, they may have already measured a higher pressure. However, since the conclusions drawn in this paper are based on relative pressure changes, they would not be affected by such measuring artifacts. Axial rotation in the upright position produced a consistent pressure increase in all sensors of approximately 120 kPa (Fig. 6). This is in agreement with other experimental studies that measured pressure in human cadaveric lumbar spines [35,36] and using finite element models [37]. The latter reported that an increased tensile stress on the annular fibers during axial rotation would compress the disc and cause an increased intradiscal pressure in the nuclear and annular ground substance. When moving from the upright neutral position to the flexed or extended positions the increase in the measured values was less than 100 kPa. A significant increase was only measured in two conditions: in the outer posterolateral IVD region in flexion, and in the inner and intermediary anterior IVD region in extension. This observation is different from what has been reported by others, In theoretical calculations [38] as well as in experimental studies [36,39] a considerable nuclear pressure increase was reported for a pure llexion moment. An important pressure increase was observed in both posterolateral needles, more so in flexion than extension, when combined with axial rotation. Under sagittal loads combined with axial rotation, the highest fiber tensile strains in the inner most annular fiber layers of
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more than 20% were predicted in theoretical calculations [22], thus, corroborating our findings. Equally, Pearcy hypothesized [40] that in flexion the facet joint’s geometry allows for an increase in axial rotation amplitude. This, along with the flexion-induced prestraining of the posterior annular ring, may result in overstraining the annular fibers. However, different pressures measured between the two posterolateral regions under asymmetrical loads were never reported by others. In flexion, the ipsilateral needle position had maximum stress increase, with the regions closer to the outer IVD border demonstrating the largest stress increase [.590kPa (Fig. 6)]. In extension, the largest stress increase was measured by the contralateral needle. The ipsilateral needle showed a statistically significant increase only in the innermost IVD region (Fig. 6). The internal displacement of the nucleus pulposus may be responsible for these differences. A flexion movement drives the nucleus posteriorly [41] and creates a radial force component that increases the posterior pressure. In axial rotation, the coupled side bending in the L3/4 motion segment is directed toward the contralateral side [42,43]. The consequent wedging of the IVD space propels the nucleus toward the ipsilateral side. This mechanism may explain the asymmetrical pressures recorded in the two posterolateral regions during rotation. In extension, the nucleus is driven anteriorly [41] and the radial force component created by the nucleus is smaller in the posterior regions. Coupled side bending during rotation tilts the vertebral body. The predominantly contralateral posterior stress increase measured in our study may be caused by the increased compressive force that results from this tilt. Differences observed in the matrix compressive stress across the three sensors of the same needle cause a pressure gradient. Significant centripetal pressure gradients were found only in the posterolateral needle locations during the upright and flexed positions. In the extended position these stress gradients were not present (Fig. 5). This finding is consistent with the observations made by McNally and Adams [8], who reported a stress peak in the posterior annulus, which fell toward the nucleus, to a plateau value measured uniformly throughout the nucleus. This non-homogeneous stress distribution may be responsible for an inwards bulging of the innermost annular laminae in the posterolateral IVD regions, which may lead to the delamination of the inner annular fiber layers and subsequent IVD degeneration. Recent studies [44,45] that used a series of magnetic resonance images of multiple markers placed in the axially loaded cadaveric disc describe a “paradoxical” centripetal fluid flow from the annulus to the nucleus during axial compression. This change in the magnetic
resonance signal could be an artifact, which is the result of a changed ratio of “free” and “bound” water that may have occurred because of the increased pressure. On the other hand, the insertion of two needles in the inner annular and nuclear zone, connected with a tube filled with indigocarmine and a droplet of mercury, also permitted direct measurements of a centripetal pressure gradient during axial compression [45]. This observation with a maximum nuclear volume increase of approximately 7% after 40 minutes of axial compression [44] is supported by our findings. This centripetal fluid shift may be caused by the hydrostatic pressure gradient. 6. Conclusion The posterolateral inner annular zone of the IVD seems to behave in a very complex fashion. When applying compression and axial rotation, high stress peaks and centripetal pressure gradients with an initial net fluid flow into the nucleus seem to be a peculiarity of this region. These stress peaks and pressure gradients may cause a deterioration of the inner annular fiber layers, which leads to delamination and subsequent degeneration. Equally, they may affect transport of nutrients to and through this region of the IVD. The centripetal pressure gradient and the magnitude of matrix compressive stress measured in the posterior annulus change with the different postures. Lateral displacement of the nucleus because of the wedging of the disc space may be the major player. Our results indicate that asymmetrical loading patterns, such as axial rotation combined with postural changes of the spine in the sagittal plane, increase these effects. Flexion, more so than extension, subjects the posterolateral area of the inner annulus fibrousus to increased stresses and centripetal pressure gradients, which indicates a possible increased mechanical load in this area. Assuming a chronic mechanical overload to be the cause of mechanical IVD failure, reducing the frequency of such movements in a working environment could potentially lower the incidence of degenerative IVD disease. Acknowledgements This work was supported by the Medical Research Council of Canada. References [l] Nachemson A. Lumbar intradiscal pressure. Acta Orthopaed Stand 1960;43: l-105. [2] Nachemson AL, Morris J. In vivu measurements of intradiscal pressure. J Bone Joint Surg [America] 1964;46:1077-1092.
T. Steffenet &Clinical Biomechanic,s13 (1998) 495-505 [3] Anderson BJ, Ortengren R, Nachemson AL, Elfstrom G, Broman H. The sitting posture: an electromyographic and discometric study. Orthoped Clin N Am 1975;6(1):105-120. [4] Nachemson A, Elfstrom G. Intravital dynamic pressure measurements in lumbar discs. A study of common movements, maneuvers and exercises. Stand J Rehabil Med 1970:1(I Suppl):l-40. ] Berkson MH, Nachemson AL, Schultz AB. Mechanical properties of human lumbar spine motion segments - Part II: Responses in compression and shear, influence of gross morphology. J Biomech Engineer 1979;101:53-57. I] Schultz AB, Warwick DN, Berkson MH, Nachemson AL. Mechanical properties of human lumbar spine motion segments - Part I: Responses in flexion, extension, lateral bending, and torsion. J Biomechan Engineer 1979;101:46-52. [7] Broberg KB. On the mechanical behaviour of intervertebral discs. Spine 1983;8(2):351-165. [8] McNally DS, Adams MA. Internal intervertebral disc mechanics as revealed by stress profilometry. Spine 1992;17(1):66-73. [9] McNally DS, Adams MA, Goodship AE. Can intervertebral disc prolapse be predicted by disc mechanics?. Spine 1993;18(11):1525-1530. [lo] Adams MA, Hutton WC. The effect of fatigue on the lumbar intervertebral disc. J Bone Joint Surg [UK] 1983;65(2):199-203. [l I] Adams MA, Hutton WC. Gradual disc prolapse. Spine 1985;10(6):524-531. 1121Terhaag D, Frowein RA. Traumatic disc prolapses. Neurosurg Rev 1989;12(Suppl 1):588-594. [13] Adams MA, Hutton WC. The mechanics of prolapsed intervertebral disc. Internatl Orthopaed 1982;6(4):249-253. (141 Farfan HF, Huberdeau RM, Dubow HI. Lumbar intervertebral disc degeneration: the influence of geometrical features on the pattern of disc degeneration - a post mortem study. J Bone Joint Surg [American] 1972;54(3):492-510. 1151Hirsch C, Schajowicz F. Studies on structural changes in the annulus fibrosous. Acta Orthopaed Stand lumbar 1953;22:184-231. [16] Gordon SJ. Yang KH, Mayer PJ, Mace AHJ, Kish VL, Radin EL. Mechanism of disc rupture: a preliminary report. Spine 1991;16(4):450-456. [17] Adams MA, Hutton WC. Prolapsed intervertebral disc. A hyperflexion injury 1981 Volvo Award in Basic Science. Spine 1982;7(3):184-191. 1181Adams MA. Mechanical testing of the spine - an appraisal of methodology: results, and conclusions. Spine 1995;20(19):2151-2156. [19] Steffen T. Rubin RK, Baramki HG, Antoniou J, Marchesi D? Aebi M. A new technique for measuring lumbar segmental motion in viva: method. accuracy, and preliminary results. Spine 1997;22(2):156-166. [20] White AA, Panjabi MM, Clinical biomechanics of the spine (2 edn). Philadelphia: JB Lippincott, 1990. [21] Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IK, Bishop PB. Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 1990;15(5):411-415. [22] Shirazi-Adl A. Strain in fibers of a lumbar disc. Analysis of the role Of lifting in producing disc prolapse. Spine 1989;14(1):96-103. [23] Gael VK, Monroe BT, Gilbertson LG, Brinckmann P. Interlaminar shear stresses and laminae separation in a disc. Finite element analysis of the L3-L4 motion segment subjected to axial compressive loads. Spine 1995;20(6):689-698. [24] Marchand F, Ahmed AM. Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 1990;15(5):402-410. WJ. Age changes to the anulus [25] Bernick S. Walker JM, hde fibrosus in human intervertebral discs. Spine
SOS
1991;16(5):520-524. 1261Osti OL, Vernon-Roberts B. Fraser RD, 1990 Volvo Award in experimental studies. Anulus tears and intervertebral disc degeneration. An experimental study using an animal model. Spine 1990;15(8):762-767. [27] McNally DS, Adams MA, Goodship AE. Development and validation of a new transducer for intradisc#il pressure measurement. J Biomed Engineer 1992;14(6):495-498. [281 McMiIlan DW, McNally DS, Garbut G, Adams MA. Stress distributions inside intervertebral discs: the validity of experimental ‘stress profiometry’. Proc Inst Mech Engineers (H), 1996;210(2):81-87. [29] Hickcy DS. Hukins DW. Aging changes in the macromolecular organization of the intervertebral disc: an X-ray diffraction and electron microscopic study. Spine 1982;7(3):234-342. [30] Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsiun on the lumbar intervertebral joints: the role of torsion in the production of disc degeneration. J Bone Joint Surg [American] 1970;52(3):468-497. [31] Farfan HF. The torsional injury of the lumbar spine. Spine 1984;9(1):53. [32] Shirazi-Adl A. Biomechanics of the lumbar spine in sagittal/ lateral moments. Spine 1994;19(21):2407-2414. 133) Brinckmann P. Grootenboer H. Change of disc height, radial disc bulge, and intradiscal pressure from drscectomy. An in virvo investigation on human lumbar discs. Spine 1993;16(6):641-646. 1341Ranu HS. Multipoint determination of pressure-volume curves in human intervcrtehral disc\. Ann Rheum Dis 1993;52(2):142-146. [35] Schultz A. Andersson G, Ortengren R, Haderspeck K, Nachemson A. Loads on the lumbar spine. Validation of a biomechdnical analysis by measurements of intrddiscal pressures and myoelectric signals. J Bone Joi?t Surg [American] lY82;64(5):713-720. [36] Andersson GB, Ortengren R, Nachemson A. lntradiskal pressure, intra-abdominal pressure and mvoelectric back muscle activity related to posture and loading. Cl& Grthopacd Related Res 1977;129:156-164. [37] Shirazi-Ad1 A, Ahmed AM, Shrivastava SC. Mechanical response of a lumbar motion segment in ;axial torque alone and combined with compression. Spine 1986:1I (9):9 t4-927. 1381Shlrazi-Adl A. Ahmed AM, Shrivastdva SC. A finite element study of a lumbar motion segment subjected to pure sagittal plant moments. J Biomechan 1986;19(4):331-350. [39] Adams MA, Hutton WC. The effect of posture on the lumbar spine. J Bone Joint Surg [British] 1985;67(4):625-629. (401 Pearcy MJ, Twisting mobility of the human back in flexed postures. Spine 1993;18(1):114-149. [41] Serous\i RE. Krag MH, Muller DL, Pope MH. Internal deformations of intact and denucleated human lumbar discs subjected to compression, flexion. and exrension loads. J Orthopaed Res 1989:?(1):122-131. 1421Panjabi M. Yamamoto I, Oxland T, Crlsto J. How does posture affect coupling in the lumbar spine’? Spine 1989;14(9): 1002-1011. 1431Pearcy MJ, Tibrewel SB. Axial rotation and lateral bending in the normal lumbar spine measured by three-dimensional radiography. Spine 1984;9:582-587. [44] Uyemura 0, Kusaka Y, Nakajima S et al., Uneven strains of the intervertebral disc matrix under axial load causes centripetal water flow within the disc. Orthopaedic Research Society, Atlanta, Georgia, 1996,p. 269. 1451Mikami Y. Kusaka Y, Uemura 0 et al., Transient accumulation of water at the centre of the nucleus pulposus in bovine intervertebral disc under axial compression. Orthopaedic Research Society. New Orleans. Louisiana. 1994.p. 733.
Lumbar intradiscal pressure measured in the anterior and posterolateral annular regions during asymmetrical loading Thomas Steffena*, Hani G. Baramki, Rick Rubin, John Antoniou, Max Aebi Orthopaedic Research Laboratory, Division of Orthopaedic Surgery, McGill University, Montreal, Quebec, Cumda
Received 27 January 1998; accepted I April 1998
Abstract Objective. To analyze the effect of asymmetrical loading on intradiscal pressure. Design. Human cddaveric lumbar spines were instrumented with multiple pressure sensors and subjected to external mechanical loads. Background. Tears and radial fissures in the posterolateral annulus with no evidence of annular protrusion or nuclear extrusion are frequently observed in non-degenerated intervertebral discs. Cadaveric studies have shown that asymmetrical loads lead to posterolateral herniation. Regional overload may be responsible for a progressive structural weakness of the posterolateral annular fibres. Methods. Three needles each equipped with three independent pressure sensors were inserted in the midplane of the L.714 intervertebral disc (n = 16) in the anterior, right posterolateral and left posterolateral regions. Axial rotation was applied in the upright, flexed and extended positions and the pressures recorded. Results. The largest intradiscal pressure increase was observed in the posterolateral inner annular regions, more so in flexion than extension, when combined with axial rotation. Significant centripetal pressure gradients were found only in the posterolateral needles during the upright and flexed positions. Conclusions. When applying compression and axial rotation, the posterolateral inner annular zones of the intervertebral disc show high stress peaks and centripetal pressure gradients. Asymmetrical loads (rotation) combined with postural changes in the sag&al plane increase these effects, and may be responsible for a chronic mechanical overload of these regions.
Relevance Our findings suggest a predilection for the posterolateral inner annular regions to mechanical asymmetrical loading. 0 1998 Elsevier Science Ltd. All rights reserved.
failure,
especially
under
Keywords: intradiscal pressure; lumbar spine; mechanical stress; posture; degeneration
1. Introduction
Pressure measurements within the intervertebral disc (IVD) provide valuable information on the biomechanical behaviour of the IVD. Nachemson [l] was first to measure the pressure in cadaveric IVDs with a needle connected to an external electromanometer. Following these cadaveric IVD pressure measurements, Nachemson and collaborators measured IVD pressures in-viva for various body postures [2,3] and during *Corresponding author: T. Steffen Orthopaedic Research Laboratory, Division of Orthopeadics, McGill University, c/o Royal Victoria Hospital, 687 Pine Ave. West, Room LA.65, Montreal, Quebec, Canada H3A 1Al.
different lifting manoeuvres [4]. Their IVD pressure measurements showed that the nucleus pulposus behaved in a hydrostatic fashion in normal and slightly degenerated IVDs. The measured pressure was found to have a linear relation with the applied external loads, but was independent of the needle’s opening direction. In cadaveric studies the intradiscal pressure slightly increased when the specimen was subjected to positional changes such as flexion/extension, lateral bending, rotation and shear [5,6]. In attempts to better understand the mechanical behaviour of the annulus fibrousus, theoretical models were used that initially related the iannulus’ stress to the pressure measured within the nucleus pulposus
0268-0033/98/$19.00+ 0.00 0 1998Elsevier Science Ltd. All rights reserved. PII: SO268-0033(98)00039-4
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[1,7]. Recently, McNally [S] introduced a new technique called stress profilometry. A strain-gauged sensor mounted to a needle was passed incrementally along a straight path through the IVD along the mid-sagittal or the mid-coronal plane. Stress profiles were obtained from the cadaveric IVD with the specimen in either a pure flexion and extension position [8], or in a flexed and extended position combined with lateral bending [9]. Based on their findings, McNally suggested there was a predisposition to prolapse in IVDs that presented an abnormal stress concentration in the posterior annulus. Posterior IVD herniation (annular protrusion or nucleus extrusion) can be the result of a gradual process [lo, 111, rarely an isolated trauma [12], or a combination of both [12,13]. Tears and radial fissures in the posterolateral annulus with no evidence of annular protrusion or nucleus extrusion are frequently observed in non-degenerated or slightly degenerated IVDs [14,15]. Cadaveric experiments using cyclic loading in flexion combined with either side bending [l l] or rotation [16] have demonstrated that physiologically reasonable repetitive loads lead to posterolateral herniation. Hyperhexion alone, under large compressive forces that simulate an acute trauma, commonly results in a centrally protruding annulus [ 13,171. It therefore seems the posterolateral annulus fails mainly because of a chronic mechanical overload. A gradual degenerative process that weakens the posterior annular ring is likely to facilitate the development of a posterolateral IVD prolapse. Simultaneous, multilocalized IVD pressure measurements could render additional information on the actual IVD stress distribution, and would help to evaluate the effect of asymmetrical loads (e.g. flexion combined with axial rotation). Three needles (one anteriorly and two posterolaterally) each equipped with three strain gauge pressure transducers were inserted into the IVD to measure pressure in a simultaneous, multilocalized manner. A custom-made mechanical testing machine that allowed for six degrees of freedom (DoF) segmental motion was used for external loading. Complex loads (a combination of axial compression, flexion/extension and axial rotation) were applied to the multisegmental spine specimen while simultaneously measuring the IVD pressure.
Ten specimens were male and six were female. They were thawed at room temperature for 12 hours while still in their sealed bags. The specimen’s uppermost (LI/L2) and lowermost (Ls/SI) motion segments were fused with screws placed through the vertebral bodies. They were then embedded in cylindrical blocks (12 cm diameter) of dental plaster so that the L3/L4 IVD plane was parallel to the attachments. The mechanical axis of axial loading was therefore perpendicular to the L3/L4 motion segment. Additional screws were used to better anchor the vertebral bodies of L, and S, within the plaster. All specimens were radiographed to exclude gross morphological anomalies (e.g., disc space narrowing, large osteophytes, skeletal anomalies, etc.). The tissues were wrapped in wet gauze during the entire procedure to minimize dehydration. 2.2. Testingmachine set-up The specimen was rigidly attached to the testing machine by fixing the cylindrical blocks to the upper and lower platforms (Fig. 1). The upper platform’s displacements were controlled by three independent stepper motors interfaced to a computer. The stepper motors could independently apply axial compression, axial rotation and flexion/extension loads. The lower platform allow low friction movement in three axes: lateral bending, and linear displacement along the two horizontal axes. Each of the lower platform’s three degrees of freedom (DoF) could be individually blocked. Together, the two platforms allowed up to six DoF motion. The lower platform incorporated a strain gauge load transducer (F/T system, Assurance Tech., garner NC, USA) that measured Cartesian force/ torque components in six DoF (Fig. 1).
2. Methods
2.1. Specimenpreparation Sixteen human cadaveric lumbar spine specimens (L,-S,) were collected from autopsies no later than 24 hours post mortem. The specimens were vacuumsealed and frozen for up to 3 months at -20°C [18]. The average age was 46.3 years (range 29-63 years).
Fig. 1. Mechanical testing apparatus for cadaveric spine testing. Legend: UF = upper fixation, LF = lower fixation, LC = load cell, MS = motion sensor, N = needle.
T. Steffen et al./Clinical
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An electromagnetic cobchester position sensing system (FASTKAK, Polhemus, VT, USA) was used to measure the relative kinematics of the h, Lj, L4 and L5 vertebral bodies. Threaded Kirschner wires mounted with lightweight position sensors (2.5 mm diameter) were rigidly placed in the L,, L3 and L, vertebral bodies. A fourth position sensor was attached to the testing machine’s lower platform. Because the LZ vertebra and the load transducer were both rigidly attached to the lower platform, knowledge of its position was given. To avoid erroneous position readings caused by metal interference, the amount of metal in the vicinity of the measurement system was reduced (e.g. both mounting platforms were made of Plexiglas@).Based on results from previous studies with similar experimental conditions [ 191 the method’s accuracy was estimated to be on average 0.1” (CI 95%: 0.00-0.43”) and 0.23 mm (CI 95%: 0.0-0.8 mm). An initial calibration was done by recording the starting position of the upper endplates of L3, L4 and L!; in a neutral posture. A series of points were recorded along each endplate’s outer contour using an electromagnetic position sensor mounted to a calibrated stylus. The series of points for each endplate recorded in three dimensions was used to determine the endplate’s centroid and plane of best fit, An additional landmark (recorded in the posterior midsagittal area of the spinous process) was used to complete the definition of the vertebral body’s local coordinate system [20]. Relative segmental motion was
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calculated using the adjacent vertebral bodies’ local coordinate systems. A computer (Apple Quadra 650) customized with controlling software (LabView 3.01, National Instruments, Austin TX, USA), was responsible for reading and processing load, position and pressure values, as well as controlling the stepper motors in preprogrammed load sequences. 2.3. Pressure-measuring needles
The custom-made needles (2.1 mm diameter) were each equipped with three independent 1.6 mm diameter strain gauge pressure transducers. The transducers were mounted at a distance of 5.5, 8.5 and 11.5 mm from the tip (Fig. 2). All needles were inserted in the mid-plane of the L,/‘L, IVD (Fig. 3). One needle was placed anteriorly in the mid-sagittal plane, and the remaining two needles were inserted in the posterolateral left and right positions (at the point corresponding to the medial border of the lower pedicle and at an angle of 30” relative to the sagittal plane). The needles were gradually advanced into the IVD until the sensors were at a distance of 6, 9 and 12 mm from the outer IVD border facing upward. Each needle was fixed in place with a suture. All pressure sensors were calibrated before and after each experiment by inserting the needles into a pressure chamber. The chamber pressure was gradually decreased from 1800 kPa to 0 kPa over a time of 30 seconds, and output voltages were simultaneously
PL Fig. 2. Diagram of the needle with the three mounted sensors.All measurements are in millimeters.
-
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f.-~-
5.5_.~,
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18.5 * 3.0, +3.0+ +-------------+
~~ Fig. 3. Needle positions within the L3/4 disc. Legend: NP = nucleus pulposus, AF = annuhrs fibrosus, A = anterior needle position, PL = posterolateral needle position, S = sensor.
recorded with a reference pressure gauge of 0.5% static accuracy (Cole-Parmer Instrument Company, Chicago IL, USA). A linear least square fit was performed to map each pressure transducer’s voltage into kPa recorded with the reference gauge. The static accuracy of each sensor was less than 3% full scale for all error sources (i.e., non-linearity, reproducibility, hysteresis). An ANOVA model was used (Statview Ver. 4.0, Abacus Concepts Inc., USA) to evaluate the effect of different factors on the recorded pressure measurements. These factors included: (i) needle position (anterior, posterolateral left, posterolateral right); (ii) sensor distance from the outer IVD border (6, 9 and 12 mm); (iii) loading condition (upright, flexed, extended); (iv) direction of axial rotation (leftneutral-right cycle, right-neutral-left cycle); and (v) specimen (sample number). As the data obtained from the two posterolateral needles were mirrored (leftright), comparison of these two sets of data allowed assessment of the method’s reproducibility for measuring intradiscal pressure. A systematic measurement bias (e.g. artifacts at the sensor-tissue interface) could not be excluded. However, the differential pressures used in subsequent data analyses were not affected by a systematic measurement bias. IVD pressures measured at the same sensor distance, the same needle position and in the same loading condition were pooled and the average was calculated. This average was used for all subsequent data analyses. Paired t-tests were used to detect any significant change in the average pressure when the specimen was moved from the upright neutral position to the other positions. The pressure gradients across the three sensors of any given needle and position were calculated using multilinear regression. 2.4. Loading protocol
A 300 N axial compression was maintained for 15 min to compensate for possible post mortem hyperhydration of the IVD. We recorded the IVD pressure patterns during 10” of axial rotation to each side with an adjusted axial load of 600 N in three different
positions*: upright, 15” flexion and 10” extension. These displacements were for the whole specimen. Two cycles of preconditioning preceded the actual recording cycle in each position. The recording cycle consisted of a left-to-right cycle and a right-to-left cycle. L3/L4 segmental flexion/extension and axial rotation angles were calculated using the position sensor data. 2.5. Post-experimental analysis
The L3/L4 segment was isolated after the experiment (Fig. 4, part A) and cut along the sagittal plane for IVD degeneration grading (Fig. 4, part B). The Thompson degeneration grading system [21] was used to quantity the degradation stage of each IVD. Any IVD with a Thompson grade of four or five (highly degenerated) was excluded from the study. The two hemivertebrae obtained by the sagittal cut were cut a second time along the mid-transverse plane of the IVD (Fig. 4, part C). The different IVD zones (annular, intermediary, and nuclear) were identified on the slices obtained. Along the needle’s insertion path structures found at 6, 9 and 12 mm from the outer IVD border were identified. These points corresponded to the location of the individual pressure sensors within the IVD. 3. Results The ANOVA model revealed that the largest influence on the pressure outcome was caused by the needle position, followed by the loading condition and the sensor distance from the outer IVD border (all p
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the pressure (p = 0.69 and 0.14, respectively). Consequently, pressures measured at the same position and for the same loading condition during the two different rotation cycles were averaged for subsequent data analysis. Table 1 and Table 2 list the mean pressure values obtained from the 16 specimens. There was no statistically significant difference between the pressures measured by the left and the right posterolateral needles during ipsilateral rotation or contralateral rotation (Table 1). Similarly, there was no statistically significant difference between the pressures measured by the anterior needle in the left rotation and the right rotation positions (Table 2). These findings underline the reproducibility of the measurement technique. The data were subsequently regrouped as follows: the pressures measured by the two posterolateral needles in the ipsilateral rotation position were pooled; the pressures measured by the same needles in the contralateral position were pooled; the pressures measured by the anterior needle in the left and right rotation positions were also pooled (Fig. 5). Figure 6 represents the change in pressure when comparing the pressures in the different postures with
A
499
the upright neutral position. Significant pressure changes were found mainly in the rotated positions, with the highest pressure increase measured in the ipsilateral posterior needle for flexion combined with rotation (590 kPa), followed by the contralateral posterior needle for extension combined with rotation (423 kPa). The pressure gradients across the three sensors of the same needle in the different positions were calculated (Fig. 5). Significant pressure gradients were found in the posterolateral needles in the upright and the flexed posture for both the neutral and the two rotational positions. All pressure gradients were directed towards the nucleus (i.e. higher pressure values in the annular region). The highest gradient (60.6 kPa/mm) was found in the posterolateral during rotation to the ipsilateral side in flexion. The kinematic and kinetic data measured for the L3/L4segmental level are presented in Table 3. Because standardized displacements were applied to a multisegmental specimen, there exists a considerable intersample variation for the actual LJ4 segmental ROM. Regressions regions ran between the different sensor locations and segmental displacement amplitudes or angular moments generally had significant p-values, thus indicating a direct relationship between segmental displacement and intradiscal pressure rise, but the 2 values were consistently low. Also, no direct correlation could be established between IVD degeneration (Thompson grading) and IVD pressures. The IVD gross morphological evaluation of the hemivertebrae (Thompson grading) showed that 13 IVDs had a Thompson grade II and three IVDs had a Thompson grade III. One IVD was found to have a Thompson grade IV and was subsequently excluded from the study. The localization of the various pressure sensors within the IVD tissue as observed on the transverse cuts is given in Table 4. 4. Discussion 4.1. Pathophysiology of disc mechanical failure
C
Fig. 4. Steps in the cutting technique for the post-experimental disc analysis.
Nuclear herniation through the annulus occurs predominantly in the posterolateral area of the IVD [15]. It has been shown that the natural history of a “non-acute” IVD prolapse starts with morphologic changes in the inner annular zone. Decomposition of the lamellar structure [22-241 accompanied by a fibrous substitution of the matrix [25] is followed by focal tears that spread radially outwards [26]. The annulus weakens and finally permits the nuclear material to herniate. Fatigue testing mimicking a chronic mechanical overload has been used in ex-vivo studies to investigate IVD mechanical failure and to reproduce IVD protrusion and herniation [lo, 11,161.
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The predilection of this phenomenon to the posterolateral IVD regions suggests the presence of a regionspecific mechanical cause that precipitates its occurrence.
The complex anatomy of the IVD results in a non-homogeneous stress distribution throughout the IVD. In addition, this stress distribution changes with different positions and under different loads. In our
Table 1 Mean pressure values in kPa (standard error of the mean in parentheses) measured by the posterolateral left and the posterolateral right needles in the upright, flexed, and extended positions. For each position the pressure was recorded in neutral as well as in lo” rotation to both the ipsilateral and the contralateral sides. Thep-values represent the results of a paired t-test performed between the left and right needle data sets. Position
Rotation
Sensor (mm)
Posterolateral left needle
Posterolateral right needle
p-value
Upright
Neutral
12 9 6 12 9 6 12 9 6
822.2 (51.9) 956.8 (83.3) 1066.0(93.1) 924.6 (59.2) 1061.5(85.0) 1169.6(97.1) 945.4 (61.1) 1059.9(88.6) 1200.2(103.5)
871.2 (81.4) 928.5 (71.3) 1032.2(92.4) 971.1 (89.1) 1032.7(78.6) 1145.6(102.6) 970.0 (82.4) 1042.3(74.1) 1166.6(96.4)
0.425 0.357 0.621 0.587 0.663 0.641 0.401 0.274 0.668
12 9 6 12 9 6 12 9 6
899.8 (76.8) 1003.6(88.7) 1151.2(111.0) 1259.1(107.2) 1382.1(110.3) 1638.8(122.9) 984.0 (89.0) 1087.2(103.0) 1243.4(127.6)
911.8 (82.3) 1006.6(78.7) 1151.7(109.6) 1279.3(107.8) 1434.6(105.8) 1622.0(121.6) 1012.2(96.4) 1083.9(90.1) 1156.7(90.1)
0.084 0.919 0.645 0.911 0.939 0.132 0.094 0.438 0.483
12 9 6 12 9 6 12 9 6
950.7 (121.0) 973.2 (93.7) 1053.8(96.2) 995.4 (134.7) 1016.0(102.6) 1078.0(104.9) 1347.8(141.5) 1316.5(93.0) 1430.1(113.2)
893.3 (100.4) 929.1 (72.8) 969.9 (83.6) 1251.9(120.6) 1001.1(88.6) 1042.8(98.9) 1548.0(99.3) 1389.7(99.2) 1489.3(105.2)
0.126 0.248 0.081 0.235 0.474 0.775 0.082 0.703 0.525
Ipsilateral Contralateral
Flexion
Neutral Ipsilateral
Contralateral
Extension
Neutral
Ipsilateral Contralateral
Table 2 Mean pressure measured by the anterior needle in kPa (standard error of the mean in parentheses) in the upright, flexed, and extended positions. The pressure was recorded in neutral as well as in lo” rotation to both the left and right side. The p-values represent the results of a paired t-test performed between the left and right rotation data sets. Position
Sensor (mm)
Pressure in neutral
Pressure in rotation Left
Right
p-value
Upright
12 9 6
775.8 (91.0) 906.3 (77.5) 858.9 (96.8)
886.1 (90.5) 1032.9(71.9) 998.0 (94.2)
916.6 (90.0) 1049.6(91.8) 1033.8(89.7)
0.221 0.651 0.309
Flexion
12 9 6
810.9 (94.1) 923.1 (87.8) 949.3 (111.2)
939.3 (96.4) 1001.6(98.1) 1085.7(110.8)
948.4 (101.3) 1050.1(110.5) 1101.4(115.7)
0.750 0.925 0.694
Extension
12 9 6
895.8 (103.0) 1016.4(89.5) 926.4 (93.6)
990.3 (107.6) 1120.4(93.3) 1035.5(91.5)
994.7 (92.2) 1136.6(96.5) 1057.9(94.5)
0.881 0.556 0.462
T. Steffen et ah/Clinical
Bivmechanics
4.2. Intradiscal stress distribution
Although measuring stress within the IVD is not possible, intradiscal pressure measurements are
Neutral Wal 2ooo
23.0 (0.318)
40.9 (0.009)
---*--*.-.**..-..-.-----.-----*.-.*-..*.-.--.--.-.---....-.--.--~~~~~~-....~-.......~.~*.
0
VW 2ooo
-9mm
13.6
34.4 (0.011)
Rotation
[kPa/km] 25.1 (p-v@ue) (0.129) x
60.6
33.9
(0.002)
(0.048)
ant
pl/ipsi
plkontra
35.6 (0.014)
38.0 (0.009)
l
[kPa/Lm] 18.9 (p-value) (0.192)
*
.
4.7
ant
1
ant
ant Wal
-6mm
1
ant (0.520)
501
495-505
thought to be a good indicator of stress. McNally et al. reported reliable measurements obtained [W’l throughout the nucleus pulposus and annulus fibrousus of IVD’s when using a similar pressure sensor passed incrementally through the disc. Experimentally, the ability of their technique to quantify matrix compressive stress has been demonstrated 1281.Stress distribution derived from a pressure profile obtained along the mid-sagittal axis of the IVD showed the presence of stress peaks in the posterior annulus at a distance
study, we investigated the possibility that certain postural changes may cause a localized overload in the posterolateral inner annular region. This overload could lead to structural weakness in this region and subsequent nuclear prolapse.
n112mm
13 (1998)
15.4
[kPa/km]
8.6
ant
PVipsi plkontra -9.0
pl/ipsi
2.7
plkontra
Fig. 5. Mean pressure and standard error bars in kPa for the different sensor locations (ant = anterior. pl = posterolateral) and for all positions (flexion, upright, extension). In rotation, the posterior pressure measurements are shown separately for the ipsi- (pliipsi) and contralateral (PI/contra) needle positions. Different sensor distances to the outer IVD’s border are identified by different filling patterns. The average pressure gradient is calculated using linear regression over the span of the three adjacent sensors of any given needle location and s expressed in kPa/mm, with positive pressure gradients in the centripetal direction. p-values for a gradient different from zero are given in parentheses, significant gradients @ ~0.05) are identified with an asterisk (*),
502
T Steffen et al./Clinical Biomechanics 13 (1998) 495-505
varying from 4 mm to 12 mm from the posterior IVD border [9]. Intervertebral discs analysed in our study had a Thompson degeneration grade II (81%) or grade III (19%) which indicate a compact nucleus with no tears
0
Wal
12mm
and a preserved gelatinous kernel. The zone at the junction of the nucleus and the annulus is characterized by a gradually decreasing proteoglycan and water content, and an increasing amount of non-oriented fibres [25,29] This intermediary zone is therefore not
-9mm
Neutral
-6mm
1
Rotation
800 600 400 200 0
ant
I
ant
pl/ipsi plkontra
. t
ant pl/ipsi plkontra
800 P ‘; 400 c a, 200 fi
0
@ -200
ant pl/ipsi plkontra
ant
Fig. 6. Mean pressure differences and standard error bars in kPa for all positions with respect to the upright neutral position (for legend see Figure 5). The differences are calculated for each separate sensor location. Significant differences (paired I-test, p~O.01) are indicated with an asterisk (*).
Table 3 L3/L4 mean angular displacements (n = 16) recorded with the electromagnetic tracking system and mean moments at the end positions recorded with the load cell. Values in parentheses indicate standard deviations. The upright posture was defined in neutral axial rotation with the load cell reading zero moment in the sagittal plane. Posture
Upright Flexion Extension
One side axial rotation
Flexion/extension
Angle 0
Moment (nm)
-hle
2.3 (0.8) 2.5 (0.9) 1.9 (0.6)
19.0 (5.1) 16.8 (7.0) 15.4 (4.2)
Defined at 0 4.9 (2.4) 1.8 (0.7)
--___-~-.
(“1
Moment (nm) 0.0 (0.1) 12.3 (3.9) 8.4 (2.8)
T Steffen et al./Clinical
Biomechanics
Table 4 Number of sensors (for each needle and sensor location) found in any of the three disc zones. The sensor locations were evaluated from post-experimental transversal cuts through the L3/L4 discs (n = 16). Needle
Sensor (mm)
Nuclear zone
Intermediate zone
Annular zone
Anterior
12 9 6 Total
13 0 0 13
3 9 0 12
0 7 16 23
Posterolateral (left)
12 9 6 Total
16 I 0 23
0 I 1 8
0 2 1s 17
Posterolateral (right)
12 9 6 Total
15 9 0 24
1 6 2 9
0 1 14 15
expected to behave in a purely hydrostatic fashion. Non-homogeneous stress distributions are likely to be observed across this zone. We inserted the pressure needles to a fixed depth in the anterior region and the two posterolateral regions, which resulted in stationary sensor positions at 6, 9 and 12 mm from the outer IVD border, facing upwards. Since the posterior annulus extends to an average of about 7 mm and the anterior annulus to about 9 mm from the outer IVD border, the span of the three sensors was expected to cover the area of the innermost annular fiber layers and the intermediary zone (Table 1). This area corresponds to the above mentioned site of expected non-homogeneous stress distribution. Because the sensors were not in the center of the nucleus (with its known hydrostatic behaviour), the pressure readings may be different for sensors facing sideways and upwards. In our experiment only results from the upward facing sensor position were analysed. The stationary placement of the needles provided identical measurement sites so that pressure readings obtained under different loading regimens could be compared. Asymmetrical trunk motion, such as rotation [30,31] and lateral bending [10,32], play a major role in the development of a posterior IVD prolapse, making it essential that the three needles inserted in the IVD allow simultaneous analysis of asymmetrical stresses in the left and right posterolateral, as well as the anterior annular regions. This made it possible to investigate the pressure distribution within the IVD under asymmetrical loading regimens. Multisegmental spine specimens were used for the study because they provide more realistic mechanical testing conditions [18]. As a result, a larger number of
13 (1998)
495-505
503
multisegmentally inserting ligaments were preserved, and the mechanical restraints on the specimen by the testing machine were reduced. The G4 disc level was chosen for instrumentation in order to have one intact lumbar disc level above and below. In addition, the L3/4 intervertebral disc showed less degenerative changes, therefore made the IVDs of the different specimens more uniform. 5. Interpretation
In the upright neutral position and under an axial load of 600 N, the pressures recorded by the sensors closest to the nucleus were around 0.8 MPa and increased in the sensors located closer to the annulus fibrousus (Fig. 5). Based on the data of Brinckmann and Grootenboer 1331,and assuming a linear relationship between axial load and intradiscal pressure, one would expect for a 600 N axial loacl, an intradiscal pressure of approximately 0.7 MPa at the center of the disc. The three needles inserted into the same disc increased its volume by 0.08 ml, which would result according to Ranu [34] in a 26 kPa pressure rise, which partially explains the higher pressure observations. The inner most sensors were not located in the nucleus’ center and, considering the increased pressure in the annular regions, they may have already measured a higher pressure. However, since the conclusions drawn in this paper are based on relative pressure changes, they would not be affected by such measuring artifacts. Axial rotation in the upright position produced a consistent pressure increase in all sensors of approximately 120 kPa (Fig. 6). This is in agreement with other experimental studies that measured pressure in human cadaveric lumbar spines [35,36] and using finite element models [37]. The latter reported that an increased tensile stress on the annular fibers during axial rotation would compress the disc and cause an increased intradiscal pressure in the nuclear and annular ground substance. When moving from the upright neutral position to the flexed or extended positions the increase in the measured values was less than 100 kPa. A significant increase was only measured in two conditions: in the outer posterolateral IVD region in flexion, and in the inner and intermediary anterior IVD region in extension. This observation is different from what has been reported by others, In theoretical calculations [38] as well as in experimental studies [36,39] a considerable nuclear pressure increase was reported for a pure llexion moment. An important pressure increase was observed in both posterolateral needles, more so in flexion than extension, when combined with axial rotation. Under sagittal loads combined with axial rotation, the highest fiber tensile strains in the inner most annular fiber layers of
504
?: Steffen et aLiClinica1 Biomechanics 13 (199X) 495-505
more than 20% were predicted in theoretical calculations [22], thus, corroborating our findings. Equally, Pearcy hypothesized [40] that in flexion the facet joint’s geometry allows for an increase in axial rotation amplitude. This, along with the flexion-induced prestraining of the posterior annular ring, may result in overstraining the annular fibers. However, different pressures measured between the two posterolateral regions under asymmetrical loads were never reported by others. In flexion, the ipsilateral needle position had maximum stress increase, with the regions closer to the outer IVD border demonstrating the largest stress increase [.590kPa (Fig. 6)]. In extension, the largest stress increase was measured by the contralateral needle. The ipsilateral needle showed a statistically significant increase only in the innermost IVD region (Fig. 6). The internal displacement of the nucleus pulposus may be responsible for these differences. A flexion movement drives the nucleus posteriorly [41] and creates a radial force component that increases the posterior pressure. In axial rotation, the coupled side bending in the L3/4 motion segment is directed toward the contralateral side [42,43]. The consequent wedging of the IVD space propels the nucleus toward the ipsilateral side. This mechanism may explain the asymmetrical pressures recorded in the two posterolateral regions during rotation. In extension, the nucleus is driven anteriorly [41] and the radial force component created by the nucleus is smaller in the posterior regions. Coupled side bending during rotation tilts the vertebral body. The predominantly contralateral posterior stress increase measured in our study may be caused by the increased compressive force that results from this tilt. Differences observed in the matrix compressive stress across the three sensors of the same needle cause a pressure gradient. Significant centripetal pressure gradients were found only in the posterolateral needle locations during the upright and flexed positions. In the extended position these stress gradients were not present (Fig. 5). This finding is consistent with the observations made by McNally and Adams [8], who reported a stress peak in the posterior annulus, which fell toward the nucleus, to a plateau value measured uniformly throughout the nucleus. This non-homogeneous stress distribution may be responsible for an inwards bulging of the innermost annular laminae in the posterolateral IVD regions, which may lead to the delamination of the inner annular fiber layers and subsequent IVD degeneration. Recent studies [44,45] that used a series of magnetic resonance images of multiple markers placed in the axially loaded cadaveric disc describe a “paradoxical” centripetal fluid flow from the annulus to the nucleus during axial compression. This change in the magnetic
resonance signal could be an artifact, which is the result of a changed ratio of “free” and “bound” water that may have occurred because of the increased pressure. On the other hand, the insertion of two needles in the inner annular and nuclear zone, connected with a tube filled with indigocarmine and a droplet of mercury, also permitted direct measurements of a centripetal pressure gradient during axial compression [45]. This observation with a maximum nuclear volume increase of approximately 7% after 40 minutes of axial compression [44] is supported by our findings. This centripetal fluid shift may be caused by the hydrostatic pressure gradient. 6. Conclusion The posterolateral inner annular zone of the IVD seems to behave in a very complex fashion. When applying compression and axial rotation, high stress peaks and centripetal pressure gradients with an initial net fluid flow into the nucleus seem to be a peculiarity of this region. These stress peaks and pressure gradients may cause a deterioration of the inner annular fiber layers, which leads to delamination and subsequent degeneration. Equally, they may affect transport of nutrients to and through this region of the IVD. The centripetal pressure gradient and the magnitude of matrix compressive stress measured in the posterior annulus change with the different postures. Lateral displacement of the nucleus because of the wedging of the disc space may be the major player. Our results indicate that asymmetrical loading patterns, such as axial rotation combined with postural changes of the spine in the sagittal plane, increase these effects. Flexion, more so than extension, subjects the posterolateral area of the inner annulus fibrousus to increased stresses and centripetal pressure gradients, which indicates a possible increased mechanical load in this area. Assuming a chronic mechanical overload to be the cause of mechanical IVD failure, reducing the frequency of such movements in a working environment could potentially lower the incidence of degenerative IVD disease. Acknowledgements This work was supported by the Medical Research Council of Canada. References [l] Nachemson A. Lumbar intradiscal pressure. Acta Orthopaed Stand 1960;43: l-105. [2] Nachemson AL, Morris J. In vivu measurements of intradiscal pressure. J Bone Joint Surg [America] 1964;46:1077-1092.
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