Influence of varying muscle forces on lumbar intradiscal pressure: An in vitro study

Pergamon Copyright

TECHNICAL

INFLUENCE

J. Bbmechmics, Vol. 29, No. 4, pp. 549-555, 19% Q 1996 Ekwier Scima Ltd. AU righhts reserved Printed in Great Britain 0021-9290~6 515.00 + .oO

NOTE

OF VARYING MUSCLE FORCES ON LUMBAR PRESSURE: AN IN VITRO STUDY

Hans-Joachim Wilke,* Steffen Wolf,* Lutz E. C&s,*

INTRADISCAL

Markus Arandt and Alexander Wiesend*

*Department Unfallchirurgische Forschung und Biomechanik, Universitiit Uim, HehnholtzstraBe 14,89070 Ulm, Germany: TAbteilung fur Unfallchirur~c, Hand-, Plastische- und Wi~erherstellungschirur~e, Chirur~~ha Universit~~klinik, 89070 Ulna, Germany Abstract-The purposes of this study were to determine the effect of including muscle forces in the experimental loading of the spine on the intradiscal pressure and to determine whether this effect correlates with previously established in uivo data. We modeled the spine muscles as of five distinct groups and isolated the effect of each group on the intradiscal pressure (L4-LS). Seven human lumbo~cral spines were tested in pure flexion/extension, right/left lateral bending, and left/right axial rotation moments. Simulated muscle activity strongly inffuenced load-pressure characteristics, especially for the multifidus. Without muscle forces active, pressure increased proportionately with increasing moment. With five pairs of symmetrical constant muscle forces active (80 N per pair) the pressure increased more than 200% in neutral position and did not increase with increasing moment. The pressure without muscle forces and without axial pretoad was 0.12 MPa, which is about the same found by earlier in viuo studies of anesthetized subjects in prone position. With simulated muscle forces, the pressure was 0.39 MPa and in the range found for non-anesthetized subjects. We conclude that simulating muscle forces substantially affects intradiscal pressure. Keywords: Spinal biomechanics; Spine tester; Muscle simulation; Intervertebral disc; Intradiscal pressure.

Previous work has established that muscles constitute the active subsystem for stabilization of the spine (Andersson et al., 1974; Andersson and &tengren, 1974; Bergmark, 1989; Bogduk, 1987; C&co and Paniabi. 1991: Lucas and Bresler, 1961: McCitl, 1988; Morris et*&., 196l;.Panjabi, 1992; Pot& et hr., 1991; Schultz et al., 1982,1987). Presently, it is technologically impractical in in vitro experiments to fully simulate muscle forces in the spine. Some reported studies therefore reduce the muscle forces to a resultant single vector acting in the sagittal plane (Adams et al., 1980, 1994). Other investigations report the sim~ation of specific single muscle forces (Panjabi et al., 1989; El-Bohy et al., 1989) noting a strong influence on the results by the application of these loads. In this study we examined multiple groups of muscles to determine the effect each has on the intradiscal pressure as well as the total effect of all muscle groups acting together. Because these muscle groups act in different directions we hypothesize that each has a different effect on the intradiscal pressure. The validation of our data relies on their agreement with established in vivo intradiscal pressure measurements (Andersson et al,, 1974, 1977; Nachemson 1960, 1981; Nachemson and Elfstrom, 1970; Nachemson and Morris 1964, Okushima 1970). Such a comparison would allow us to determine whether it is possible to simulate in uivo loading conditions by the application of s&cted muscle forces.

Received in jinal form 3 March 1995. Address correspondence to: Dr Hans-Joachim Wilke, Department Unfallchirurgische Forschung und Biomechanik, Universitat Ulm, HelmholtxstraBe 14, 89070 Ulm Germany. 549

Seven human cadaveric lumbosacral spines (L2-Sl) with a mean age of 47 years (range 3063) were tested. The degeneration grade of the discs were radiographically determined (scale 1-4, after Mimura et al., 1994) and was grade 1.4 on average. They were kept frozen at - 20°C wrapped in double se&d plastic bags. Before testing, specimens were thawed at room temperature and all musculature was removed leaving all ligaments and bony tissue intact. The cranial vertebra (L2) and the sacrum (Sl) were potted in ~lymethylmethacrylate ~~~ovit 3040, Heraeus Kulxer GmbH, Wehrheimfls, Germany). Short screws in these two embedded vertebrae provided additional anchorage of the vertebrae in the plastic material. Ten cables representing five symmetrical pairs of muscle groups (multifidus with rotators in caudal direction, iliocostalis with lon~ssimus, psoas major inserting in vertebrae, psoas major inserting at the process transversus, multifidus and rotators in cranial direction) were fixed in the L4 vertebra by screws at the corresponding insertion sites (Fig. 1). The muscle directions were based on reports from Bogduk et af. (1992), Macintosh and Bogduk (1986), McGill (1988), and our own anatomical observations. The specimens were mounted in a spine tester (Wilke et al., 1994, 1995). Sl was fixed rigidly in the testing device while L2 was fixed in a gimbal with integrated stepper motors which could impart pure moments separately around one of the three axes (Fig. 2). The other five out of six degrees of freedom were free, enabling the specimen to move unconstrained. Cables representing the muscle groups (Fig. 1) were guided by an adjustable pulley system to provide the correct muscle force direction (Wilke et al., 1994). The other end of the muscle cabtes were fixed to pneumatic cylinders. These cables (1.4 mm diameter, consisting of 213 single steel strands, Ahlers, Siissen, Germany) were very flexible with a plastic envelope to reduce the friction at the

Technical Note

550

+ ----

-b

-.-.-.

w

M. multifidus

(+Mm. rotatorss)

M. iliocostalis

+ M. longissimus

M.

pseasmajor

... .... ... .... b

M. psoae

. ..---.

M. multifidus

b

at Corpus

to cat&al

(IO”, 1W)

(27”, 12”)

vertebrae

(is*,

6”)

at Processus

transversus

(22”. 2”)

(+Mm. rotatores)

to cranial

(24O, 14O)

major

Pig. 1. Schematic ofmuscle model in~lu~ng the most important muscle groups on the lumbar spine. The starting points of the vectors show the points of load application. The angle values with respect to the vertical axis represent the direction of these muscle vectors (sagittal, frontal).

pulleys. At the end of each pneumatic cylinder a load cell measured the applied force for the muscle vector pair. The force signals were registered by the computer with an AD-converter and served as feedback for controlling the muscle forces. The intradiscal pressure between L4 and L5 was measured with a special pressure transducer with a diameter of 1.2 mm (4 French, Mammendorfer Institut fur Physik und Medizin GmbH, Hattenhofen, Germany). The 6mm long tip with a hemisphe~~l end containing a piezoelectrical micropressure sensor was suitable for dynamic as well as for static measurements. The cables were guided in a fiberglass reinforced silicon catheter. The sensor could be placed in the center of the intervertebral disc using a needle (Venflon@)Z, 14 G/2,0 mm, length 45 mm, Viggo, Sweden). The plastic tube was inserted together with the needle into the nucleus pulposus. With the tube kept in place, the needle was exchanged with the transducer, and the tube then pulled back leaving the transducer in place. The location could be checked by marks on the silicone catheter. The exact position was checked by lateral and anterior-posterior radiographs before the experiment. A total of 21 different loading conditions were tested. First the specimens were tested without any muscle forces, applying continuously changing flexion/extension moments, right/left lateral bending moments and left/right axial rotation moments to f 3.75 Nm in each direction. This segment of the protocol provided a baseline for comparing the effect of the muscle forces and allows the dete~ination of the intrinsic effect of applying of external moments. These moments were applied in three cycles with a constant rate of 1.7” s-i. Then the same specimens were tested again under the same conditions but now with constant muscle forces of 80 N per pair. Each test was .repeated with tbe five muscle force pairs separately ,and with all muscle groups simultaneously. The pressure data were recorded continuously during the third cycle from neutral to the extremes of loading in each direction (Figs 3-5). The specimens were kept moist with

Technical Note

Fig. 2. The top vertebra is fixed in a gimbal. Integrated stepper motors directly introduce pure continuously changing flexion/extension, axial rotation, and lateral bending moments [specimen illustrated in flexion, with permission (Wilke, H., Claes, L., Schmitt, H., Wolf, S. A universal spine tester for in vitro experiments with muscle force simulation. European Spine Journal 3, 91-97, 1994.). Copyright Springer-Verlag].

551

Technical Note

552

EXTENSION

FLEXION

0.5 zo.4

m m Multifi. caudal

3 e! =I 0.3 2 E P 75: 0.2 5 $

,,II,,L/1 Iliac. + Longis. I . - Psoas maj. C.v. I m. Psoas maj. P.t. w.m Multifi. cranial

.c 0.1

0 -3.75

without muscles

-

-2.5

-1.25 0 1.25 moment Mx (Nm)

2.5

all muscles

3.75

Fig. 3. Intradiscal pressure (L4-L5) over applied flexion/extension moments with respect to different muscle forces. The muscle forces were kept constant with 80 N per vector pair. Note the butterfly-shape without muscles and the flat hysteresis loop with all muscles. Test direction is indicated by arrows in examples. Starting and ending points of the experiment are shown by the circles.

AXIAL ROTATION RIGHT

LEFT

0.5 TO.4

m.

5 E =l0.3 8 s? a 3 0.2 2 x

Multifi. caudal

**111.1* Iliac. + Longis.

.z 0.1

-3.75

without muscles

-2.5

-1.25 0 1.25 moment My (Nm)

2.5

_.I

Psoas maj. C.v.

mI

Psoas maj. P.t.

-.-

Multifi. cranial

---

all muscles

3.75

Fig. 4. Intradiscal pressure (L4L5) over applied left/right axial rotation moments with respect to different muscle forces. The muscle forces were kept constant with 80 N per vector pair. Test direction is indicated by arrows in examples. Starting and ending points of the experiment are shown by the circles. saline and wrapped in thin food packaging plastic during the entire test. To determine whether there were significant differences in the neutral positions between different muscle forces we performed a Friedman Test (p -C0.001). A statistically significant result using the Friedman test was followed by a Wilcoxon test (using median values and range) to determine which muscles create significant differences.

RESULTS Muscle activity strongly influenced intradiscal pressure (Friedman test, p < 0.001). The differences in the intradiscal pressure in neutral position between the tests with no muscle forces active and the test with individual muscle groups active were significant for all the muscle groups (Wilcoxon test,

553

Technical Note

LATERAL BENDING LEFT

RIGHT

-

kithout muscles

- -

Muitifi. caudal

S181v111 Iliac. + Longis. - = - Psoas maj. C.V. - -

boas maj. l?t.

- . - Multifi. cranial -

-3.75

-2.5

-1.25 0 1.25 moment Mz (Nm)

2.5

all muscles

3.75

Fig. 5. Intradiscal pressure (L4L5) over applied right/left lateral bending moments with respect to different muscle forces. The muscle forces were kept constant with 80 N per vector pair. Test direction is indicated by arrows in examples. Starting and ending points of the experiment are shown by the circles.

Load-pressure character (Fig. 3). In this case, a flexion moment of 3.75 Nm increased the pressure from 0.12 MPa in neutral position about 42% to 0.17 MPa, in extension about 50% to 0.18 MPa (Table 1). The load-pressure loops exhibited different shapes with simulated muscle contractions. In the extreme case, with all five muscle pairs active there was little hysteresis with an almost constant pressure value around 0.4 MPa. Axial rotation moments of f 3.75 Nm caused the highest increase (63%) of the intradiscal pressure up to 0.20 MPa compared to the 0.13 MPa in neutral position with a moment of 0 Nm (Fig. 4). All load-pressure curves for rotation showed a simitar increase and symmetrical v-shape with different pressure offsetsby acting muscle forces. The load and unload curves were almost identical. With right/left lateral bending, the relative increase of the pressure over neutral position from 0.12 MPa to 0.15 or 0.19 MPa was similar to that for flexion/extension (Fig. 5). These changing external bending moments also produced butterflyshaped load-pressure loops. The curves exhibited an almost symmetrical hhavior for the different muscles, with slightly higher pressure values with lateral bending to the right side. DISCUSSION

Fig. 6. Increase of intradiscal pressure (L4L5) with different simulated muscle forces (with 80 N per vector pair) in neutral position (M, = &f, = &I, = 0) relative to pressure values without muscles.

p < 0.05) except for the multifidus in cranial direction (Table 1, Fig. 6). The load-pressure characteristic in the nucleus pulposus of the disc changed subst~tiauy. In neutral position (i.e. without external loads) the pressure was 0.12 MPa without muscle forces and 0.39 MPa with all muscle forces acting simultaneously. Externally applied flexion/extension moments alone influenced intradiscal pressure, producing a butterfly-shaped

In this experiment, a strong influence of five selected muscle force pairs was shown in vitro on the pressure in the nucleus pulposus in a functional lumbar spinal unit. Different muscles showed different effects. The multifidus group and the iliocostalis with longissimus group showed the strongest influence. We should note several limitations of our study. The muscle forces were only attached to L4 and their influence was measured only in the L4-L5 disc although we would anticipate similar rest&s in other segments. We used cables which were fixed with screws in the vertebra and in the transverse or spinous process the simulated muscle forces were applied at discrete locations rather than broad insertions. We chose 40 N per single vector because forces higher than SON sometimes broke the transverse process as found in preliminary tests. However, this

554

Technical Note

Table 2. Data about intradiscal pressure in lumbar region in neutral position without external loads reported in literature in comparison with own results. Disc-degeneration-scale described by (*) Nachemson (1960) (**) Galante (1967) (***) Adams et al. (1986), (****) Mimura et al. (1994) Author

Year

Method

Nachemson and Morris

1964

in viva

Nachemson and Elfstiim 1970

Axial Preload

Disc level

-

L3-L4 L3-L4 L3-U L3-L4 L3-L4 L3-L4 L4-L.5

in viva

-

Okushima Andersson et cl. Quinnell

1970 1974 1983

in uiuo in vivo

-

in viuo

-

-

Nachemson et al.

1979

in vitro

Adams et al. Panjabi et al. El-Bohy et al. McNally et al.

1986 1988 1989 1992

in vitro in oitro

ON 4OON 476 N 500N 2000N

Adams et al. Present study

1993

in vitro

1994

in vitro

L4-L5, L5Sl L2-LS Ll-Sl L3-L5 L2-L5 L2-L5 I&L5 L&L5

in vitro in vitro

12OON -

should not substantially influence the results since the most important parameters are the direction and magnitude of the simulated muscle groups. These five vector pairs representing five symmetrical muscle groups were kept constant (80 N per vector pair) and roughly in the range of estimated forces on the lumbar spine (Gael et al., 1993: Macintosh et al.. 1993: McGill et al. 1988). This study design was similar to the study reported from Panjabi er al. (1989) but in this study several muscle force vectors acting in different directions were investigated. Although the muscular system is a much more complicated dynamic system,this experiment used static muscle forces. This study is considered as the first step simulating specific muscle forces in in vitro experiments. In reality, muscle force direction and magnitude are constantly changing and responding to the stability requirements of the spine. We confirmed a strong influence of muscle simulation on the intradiscal pressure much as Panjabi et al. (1989) and El-Bohy et al. (1989) documented an influence on the stability. In general, simulated muscle contraction increased the pressure. With changing pure moments around all three axes, however, typical load-pressure curves could be found. The largest influence was measured for the m multifidus, which was responsible for about half of the pressure increase. Therefore, it is very likely that Panjabi, who simulated the effect of only this muscle group with almost the same direction, tested the most important muscle in his experiment. We can compare our results directly with those of Nachemson’s goup (Nachemson and Morris, 19w Nachemson and Elfstrom, 1970; Nachemson et al., 1979), since both include similar in vitro loading conditions in some cases. Without preload they measured pressures of 0.11 MPa and 0.34 MPa with a preload of 4OON, respectively. Our data with muscles which create an axial force component of about 300 N are almost identical with theirs (Table 2). This agreement allows us to compare our in vitro data with their in vioo data to estimate the loading conditions which should be simulated in vitro. Their in vim studies revealed intradiscal pressures which vary from 0.3 to 1.0 MPa in awake subjects in different nositions (Table 2). Anesthetized subjects without muscle tone, on the other hand, demonstrated pressures of 0.14 MPa (Nachemson and Morris, 1964). These data are similar to our in vitro results. With simulated muscles in the neutral (corresponding most closely to

Spec. tested 6 6 1 9 9 5

Mean age

USC

deg.

Pressure WY

Position/remarks Standing Prone non-anesthetized Prone anesthetized Standing Sitting Prone non-anesthetized Lying Sitting Prone anesthetized Standing Sitting

4 7

43.2 43.2 ---_

1** 1** -‘. -.” -.

0.9 0.4 0.14 0.1 1.0 0.33-0.42 0.03 0.35-0.5 0.15 0.55 0.7

10 10 102 84 2 7 7 8 7

43.0 43.0 8-60 58.9 53.0 51 51 42.6 47,o

1”.5*** l-4* 3** o-3* o-3* 2*

0.11 0.34 0.12-0.24 0.04-0.12 1.1 2.3 0.5 1.09 0.12 0.39

-

1-z****

Without muscles With muscles

the non-anesthetized in civo prone position), we found 0.39 MPa. Without muscles (corresponding to the non-anesthetized in vivo condition), we measured 0.12 MPa. Data in this range were reported for lying subjects by Okushima (1970). In order to simulate positions other than the lying position we additionally must account for axial preload (e.g. El-Bohy et al., 1989 and Adams et al., 1993). Both groups measured in vitro pressure values of approximately 1.1 MPa with axial preloads of 476 N or 1200N. These values were slightly higher than 0.9 MPa on subjects in different upright positions reported by Nachemson and Morris from their in uivo investigation in 1964. This experiment, however, demonstrates that results more closely approximate in uiuo findings when additional muscle forces are simulated. Each muscle group has distinct effects.The multitidus muscle group (including the rotators) acting in a caudal direction had the strongest effect on intradiscal pressure. This indicates that muscle forces may provide more reasonable physiological loading conditions if at least some of the most important muscle groups are simulated. Acknowledgements-The authors wish to thank Karl Wenger for help in translation of the manuscript. This work was sup ported by the Deutsche Forschungsgemeinschaft (DFG CL77/2-1D).

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230,25-38.

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EM 29:4-K

555

affects the multidirectional

flexibility of the lumbar spine.

Spine 19, 13714380.

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43.

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1, L-40.

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