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Journal of Biomechanics 38 (2005) 18731880


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Intra-abdominal pressure increases stiffness of the lumbar spine


Paul W Hodgesa,b,c,, A.E. Martin Erikssond, Debra Shirleye, Simon C Gandeviab,c
a
Department of Physiotherapy, The University of Queensland, Brisbane, Qld. 4072, Australia
b
Prince of Wales Medical Research Institute, Sydney, Australia
c
University of New South Wales, Sydney, Australia
d
Department of Community Medicine and Rehabilitation, Physiotherapy, University of Umea, Umea, Sweden
e
Department of Physiotherapy, University of Sydney, Sydney, Australia
Accepted 10 August 2004

Abstract

Intra-abdominal pressure (IAP) increases during many tasks and has been argued to increase stability and stiffness of the spine.
Although several studies have shown a relationship between the IAP increase and spinal stability, it has been impossible to
determine whether this augmentation of mechanical support for the spine is due to the increase in IAP or the abdominal muscle
activity which contributes to it. The present study determined whether spinal stiffness increased when IAP increased without
concurrent activity of the abdominal and back extensor muscles. A sustained increase in IAP was evoked by tetanic stimulation of
the phrenic nerves either unilaterally or bilaterally at 20 Hz (for 5 s) via percutaneous electrodes in three subjects. Spinal stiffness was
measured as the force required to displace an indentor over the L4 or L2 spinous process with the subjects lying prone. Stiffness was
measured as the slope of the regression line tted to the linear region of the forcedisplacement curve. Tetanic stimulation of the
diaphragm increased IAP by 2761% of a maximal voluntary pressure increase and increased the stiffness of the spine by 831% of
resting levels. The increase in spinal stiffness was positively correlated with the size of the IAP increase. IAP increased stiffness at L2
and L4 level. The results of this study provide evidence that the stiffness of the lumbar spine is increased when IAP is elevated.
r 2004 Elsevier Ltd. All rights reserved.

Keywords: Intra-abdominal pressure; Spinal stiffness; Diaphragm; Trunk control

1. Introduction forces imposed on the spine in a variety of static and


dynamic tasks (Cresswell and Thorstensson, 1994;
Intra-abdominal pressure (IAP) is increased during Grillner et al., 1978; Marras et al., 1985). However,
many tasks that load the spine, such as lifting (Hemborg others have argued that the pressures generated during
et al., 1985) walking, (Grillner et al., 1978), jumping functional tasks are insufcient to provide a signicant
(Cresswell et al., 1993) and limb movement (Hodges et increase in spinal stability (McGill and Norman, 1987).
al., 1997). It has been argued that this pressure in the Yet, in a recent study, trunk stabilitymeasured as an
abdominal cavity contributes to the stiffness and increase in instantaneous trunk stiffness in response to a
stability of the spine (Bartelink, 1957; Grillner et al., sudden load releasewas shown to increase when IAP
1978). In support, several studies have identied a was voluntarily elevated by contraction of the abdom-
relationship between the magnitudes of IAP and the inal muscles (Cholewicki et al., 1999b). Although these
data are consistent with the proposed mechanical role of
Corresponding author. Department of Physiotherapy, The Uni- IAP, it is impossible to determine whether it is the IAP
versity of Queensland, Brisbane, Qld. 4072, Australia. Tel.: +61-7-
or the abdominal muscle activity associated with its
3365-2008; fax: +61-7-3365-2775 production that increases the stiffness and stability of
E-mail address: p.hodges@uq.edu.au (P. W Hodges). the spine.

0021-9290/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jbiomech.2004.08.016
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1874 P. W Hodges et al. / Journal of Biomechanics 38 (2005) 18731880

Several mechanisms have been proposed for IAP to 2.3. Measurement of spinal stiffness
augment spinal stability. First, IAP has been argued to
inuence spinal stability via the production of an Lumbar posteroanterior stiffness at L2 and L4 was
extensor moment by exerting a force down on the pelvic measured using a technique similar to that described
oor and up on the diaphragm (Bartelink, 1957; Keith, previously (Lee and Svensson, 1990). Force was applied
1923; Morris et al., 1961). Although this moment does to the spinous process of L4 and L2 (in separate trials)
not necessarily increase stiffness, antagonist exor and via a small padded probe using a motor that was servo-
extensor moments increase trunk stability (Cholewicki controlled for displacement. The applied force and
et al., 1999a). Thus, the opposing extension moment linear displacement were analysed over repeated cycles
from IAP and exion moment from abdominal muscle of displacement (69) at 1 Hz. Stiffness was taken as the
contraction may increase spinal stability and stiffness. slope of the regression line tted to the forcedisplace-
It has been conrmed recently that increased IAPin ment curve between 50 to 110 N for cycles 24. The rst
the absence of abdominal or erector spinae (ES) cycle was rejected from analysis as previous studies have
activityproduces a trunk extension moment (Hodges indicated non-linear changes in stiffness between the
et al., 2001). In that study, IAP was increased rst and subsequent cycles (Shirley et al., 2002). This
by stimulation of the phrenic nerve to evoke contraction range of force was selected because the forcedisplace-
of the diaphragm. A second possibility is that increased ment curve is usually linear in this range. Measurement
stiffness of the abdominal cavity may limit intervertebral of posteroanterior stiffness in this manner has good
translation and rotation (McGill and Norman, 1987). testretest reliability and is accurate within 1% for
Finally, IAP may prevent shortening of the abdom- measurement of stiffness of an elastic beam (Lee and
inal muscles, thus maintain the hoop-like geometry Svensson, 1990).
of these muscles around the abdominal cavity and
their ability to generate tension (McGill and Norman, 2.4. Pressure recordings
1993). It has not been established whether IAP
alone can increase the stability or stiffness of the Gastric (Pga) and oesophageal (Poe) pressures were
spine. measured with a pair of thin-lm strain gauge pressure
The aims of the present study were: (1) to identify transducers (Gaeltec, UK) inserted into the stomach and
whether increased IAP (without concurrent abdominal oesophagus via the nose. Correct placement of the
or back muscle activity) increases the posteroanterior transducers was conrmed using a series of manoeuvres
stiffness of the spine, and (2) to determine whether any (including a sniff) which produces an opposite change
affect of IAP on spinal stiffness is consistent between in Pga and Poe. Pressure data were amplied and
different levels of the lumbar spine. sampled at 100 Hz.

2.5. Electromyography

2. Methods Chest wall EMG activity was recorded with a pair of


Ag/AgCl electrodes placed in the mid-clavicular line in
2.1. Experimental design the seventh and eighth intercostal space. These electro-
des do not provide selective recordings of diaphragm
We produced an involuntary increase in IAP via a EMG, but represent evoked activity of the diaphragm in
contraction of the diaphragm evoked by percutaneous addition to any ongoing activity of the diaphragm and
stimulation of one or both phrenic nerves in the neck. other muscles. EMG of the abdominal and ES muscles
Stiffness of the spine was measured from the forcedis- was recorded with surface electrodes placed over the
placement response to application of a force to a lateral abdominal wall half-way between the rib cage
spinous process of the lumbar spine with the subject and iliac crest and 4 cm lateral to the L2 and L4 spinous
lying prone. processes, respectively. EMG data were bandpass
ltered between 20 and 1 kHz and sampled at 2 kHz
using Spike2 software and a Power1401 (CED, UK).
2.2. Subjects
2.6. Procedure
Three healthy volunteer subjects participated in the
experiment. The age, height and weight of the subjects Subjects lay prone with the pelvis and thorax
were 3044 years, 172187 cm, and 5887 kg, respec- supported on two 5 cm blocks placed above the
tively. All procedures were approved by the Institutional xiphoid process and below the anterior superior iliac
Ethics Committee and subjects provided informed spines to leave the abdomen unsupported (Fig. 1). Wide
written consent. belts were applied rmly to the abdomen and lower rib
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P. W Hodges et al. / Journal of Biomechanics 38 (2005) 18731880 1875

Sero-controlled suboptimal placement of the wire on one side. Subjects


motor Stimulating electrode were encouraged to remain relaxed throughout the
Indentor L2 ES EMG Pressure transducer procedure and received verbal feedback of the EMG
activity of the abdominal and ES muscles. Additional
Head control and stimulation trials were conducted without
support
L4 ES EMG the belt around the abdomen. An identical procedure
was used at the L2 and L4 levels. At the completion of
the trial, subjects maximally contracted the abdominal
Support Belts Support Anode muscles in a Valsalva manoeuvre against a closed glottis
Abdominal Chest wall to generate maximal IAP. Data from this trial were used
EMG EMG
for normalization of the EMG and IAP values.
Fig. 1. Experimental set-up showing subject position and measure-
ment equipment. Belts around the abdomen and rib cage maximised 2.7. Data analysis
the pressure increase from phrenic stimulation. Supports under the
pelvis and rib cage prevented contact between the abdomen and
Stiffness was calculated for the second to fourth cycle
support.
of force application. Root-mean-square (RMS) EMG
amplitude was measured at rest and during the
cage to restrict displacement of the abdominal contents application of force to the spinous processes. In the
and thus maximise the increase in IAP produced by trials with phrenic nerve stimulation cross-talk from
evoked contraction of the diaphragm. The diaphragm the diaphragm was recorded in both the abdominal and
was electrically stimulated either bilaterally or unilat- ES EMG electrodes. However, the amplitude of EMG
erally using wire electrodes inserted adjacent to the for each muscle could be measured for the period
phrenic nerves at the level of the cricoid cartilage and between the end of the evoked diaphragm compound
posterior to the sternocleidomastoid muscles (Gandevia muscle action potential and the subsequent stimulus
and McKenzie, 1986; Sarnoff et al., 1951). Prior to (20 ms). EMG data were recorded in this manner for
insertion, the sites for electrode insertion (i.e. minimal ve randomly selected stimulation trials and were
concurrent activation of surrounding neck muscles and averaged. EMG data are presented as an increase in
the brachial plexus) were identied using a small-probe EMG above baseline. Pearsons correlation coefcient
electrode. Two to three insertions were required to was calculated to determine the strength of relationship
achieve optimal placement of the wire electrodes. between the increase in IAP and spinal stiffness.
Surface electrodes were placed just below the clavicle
to act as anodes. Electrical stimuli were delivered from a
constant voltage source with a rectangular pulse (1 ms) 3. Results
at a frequency of 20 Hz for 810 s. Stimulation of the
diaphragm was conrmed by the latency of the When the diaphragm was electrically stimulated via
compound muscle action potential from the stimulus one or both phrenic nerves, IAP increased by
onset. Stimulation intensity was set to achieve the 1.85.9 kPa, which resulted in pressures equivalent to
maximal increase in IAP within the tolerance of the 2761% of the pressure increase during a maximum
subject. Long trains of stimuli were required to ensure voluntary pressurisation of the abdominal cavity with
that the IAP increase was maintained tonically without the glottis closed (Fig. 2). The maximum IAP achieved
the movement of the spine, which would interfere with for each subject is presented in Table 1. When IAP was
the measurement of the spinal stiffness. increased in this manner, the stiffness of the spine
Measurements of spinal stiffness were made with the assessed by posteroanterior pressure applied to the L4
probe of the stiffness device placed over the spinous spinous processes, increased by 831%. That is, a larger
process of L4 and L2, in different trials. When the probe force was required to displace the spinous process of L4,
(1.5  2 cm) was placed over L4, the device was angled an identical distance as in the control trial (Fig. 3).
4.51 caudally and 11.51 rostrally for application of force Stiffness increased in all trials for all subjects. Fig. 4
at L2. Control measurements of stiffness were made rst shows the relationship between the pressure increase and
with 69 cycles of force application with the breath held the resultant increase in spinal stiffness at L4 for each
at the end of a normal expiration. For stimulation trials, subject. The changes in pressure and stiffness were
phrenic stimulation was initiated at the same time as the signicantly correlated for individual subjects
onset of force application and sustained for the 69 (R2 0:4320:91; all Po0:05; Fig. 4).
cycles. Trials were conducted with the stimulation The EMG activity of the ES at L2 and L4 occurred
intensity at the maximum tolerable level and several with each loading cycle during control and stimulation
increments below this intensity. In some trials, stimuli trials. There was no activity of the abdominal muscles.
were applied to the phrenic nerve unilaterally due to During the stimulation trials the ES EMG increase was
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1876 P. W Hodges et al. / Journal of Biomechanics 38 (2005) 18731880

Stimulus Stimulus

200 mV
(R) Chest
wall EMG (R) Chest
wall EMG

500 mV
(L) Chest
wall EMG

Pga

Pga

0.5 kPa
Pdi

5 kPa
Poe

(B) 50 ms
19.34 100
Pdi Nmm-1
80

N
60
40

140 N
0 2 4
Force 140
mm

N
Force 0
Disp 8 mm 8

mm
Disp 0
(A) 1s (C)

Fig. 2. (A) Representative raw data showing sustained increase in gastric (Pga), oesophageal (Poe) and transdiaphragmatic (Pdi) pressures as a result
of tetanic stimulation of the diaphragm at 20 Hz. The lower two traces show the force and displacement data for two cycles. The section identied
with dotted lines is expanded in panel B. (B) Compound muscle action potentials recorded with the chest wall EMG electrode on the right and
corresponding changes in Pga and Pdi. (C) Method for measurement of posteroanterior stiffness of the spine. Stiffness was measured as the slope of
the regression line tted to the linear region of the force-displacement curve.

Table 1 amplitude recorded with the belts in situ and with the
Maximum absolute gastric pressure (Pga) and ES EMG amplitude same stimulation intensity), and stiffness was increased
during the stimulation trials as a proportion of the amplitude during by 1329%. Thus, the presence of the belts cannot
the control trial for L2 and L4
explain the size of the increase in stiffness recorded
Subjects Maximum Pga ES at L2 ES at L4 during the evoked diaphragm contraction.
(kPa) (proportion (proportion When the procedure was repeated with stiffness
control) control) measured at L2 the results were similar to those at L4.
S1 8.4 0.85 0.66 When IAP was increased by phrenic nerve stimulation
S2 5.1 0.94 0.85 the force required to displace the device applied to the
S3 7.8 1.17 1.05 spinous process of L2 increased. The relationship
between the increase in IAP and stiffness were correlated
for the individual subjects (r=0.590.97; Fig. 4). When
the stiffness was normalised to that recorded for the
less than or slightly more than the increase in EMG control trial the slope of the regression line was steeper
recorded during the control trials (Table 1). In one for the measurements at the L2 level than at L4
subject, an additional trial was conducted with a (Table 2). This suggests that a similar increase in IAP
voluntary increase in ES EMG matched to the increase would produce a larger increase in stiffness at the L2
in the control trials and thus exceeded the levels level than at L4. Similar to the L4 trials there was only a
occurring during the stimulation trials. Instruction was small increase ES EMG and no activity of the
given to ensure that the IAP was not elevated in this abdominal muscles during the L2 trials (Table 1).
trial. When EMG activity was increased in this way, the
stiffness increased by 16% of the control value and thus,
less than the stiffness increase of 2229% in the 4. Discussion
stimulation trials. To conrm that the stiffness increase
was not related to the application of the belts to the The results of this study provide evidence that
abdomen and rib cage, a pair of control and stimulation increased IAP augments stiffness of the spine. These
trials was conducted with the belts removed. In this data are consistent with the hypothesis that modulation
condition, the IAP increase was less (5963% of the IAP of IAP during functional tasks contributes to the
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P. W Hodges et al. / Journal of Biomechanics 38 (2005) 18731880 1877

Phrenic stimulation
Control
15

mm
Disp
0
125

N
Force 0

4 kPa
Pdi

4 kPa
Pga

Stim
(A) 1s

100 18.32 18.63 18.62


Force (N)

80

60 14.50 14.28 14.33

40
0 2 4 0 2 4 0 2 4
(B) Displacement (mm)

Fig. 3. (A) Representative raw data from a single subject showing force application in a control trial and during phrenic stimulation. During
stimulation the gastric and transdiaphragmatic pressures are elevated. There is an additional increase in pressure with force application. (B)
Forcedisplacement curves generated from the second to fourth trial for control (lled circles) and stimulation trials (open circles). Note the increase
in slope of the regression line (i.e. posteroanterior stiffness) with phrenic stimulation.

20
R2= 0.91 R2= 0.43 R2= 0.72
18
Stiffness (Nmm-1)

16

14

12

10
(A) 2.5 4.5 6.5 8.5 2.5 4.5 6.5 8.5 2.5 4.5 6.5 8.5

20 34
R2= 0.86 R2= 0.59 R2= 0.97
18 30

16 26

14 22

12 18

10 14
0.5 2.5 4.5 6.5 8.5 0.5 2.5 4.5 6.5 8.5 0.5 2.5 4.5 6.5 8.5
(B) Pga (kPa)

Fig. 4. Relationship between Pga and spinal stiffness for each subject with the indentor placed over the (A) L4 and (B) L2 spinous process. The
correlation coefcient is shown in the upper left corner. Note the strong relationship between parameters for all subjects.
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1878 P. W Hodges et al. / Journal of Biomechanics 38 (2005) 18731880

Table 2 restricted by application of a rm belt to reduce further


Regression slope for relationship between IAP and posteroanterior
compression and ensure that the rib position was
stiffness normalized to stiffness in non-stimulation trial L2 and L4
consistent between test conditions. Furthermore, the
Subjects L4 L2 abdomen was unsupported to reduce the effect of the
compliance of the abdominal contents on stiffness.
S1 1.02 0.89
Measurement of an increase in stiffness in trials without
S2 1.02 0.94
S3 2.60 0.30 application of the belts (but with lesser increase in IAP)
conrm that the effect was not simply due to the
mechanical effects of the belts. Despite the limitations of
this measure of spinal stiffness, it does provide a non-
mechanical stability of the spine. As pressure was invasive technique to evaluate spinal stiffness, at least in
increased involuntarily by electrical stimulation of the one direction. A further consideration is that although
diaphragm, these data conrm that IAP without overt the data indicate that posteroanterior stiffness of the
activity of the abdominal or back muscles, has a spine is increased by the increase in IAP, it was not
mechanical effect on the spine. possible to quantify its contribution to overall stability
of the spine; this requires further investigation.
4.1. Methodological factors
4.2. Spinal stiffness is increased by intra-abdominal
A limited number of subjects participated in the pressure
present study due to the discomfort associated with
strong tetanic electrical stimulation and the percuta- Although several previous biomechanical and in vivo
neous stimulation of the phrenic nerves. Wire stimula- studies predicted that IAP has a limited inuence on
tion electrodes were used to isolate the stimulus to the mechanical stability of the spine and production of an
phrenic nerve and minimise stimulation of neck muscles extensor moment (e.g. Bearn, 1961; McGill and Nor-
or the brachial plexus. Less selective stimulation greatly man, 1987; Nachemson et al., 1986; Ortengren and
increased the discomfort associated with the procedure Andersson, 1977), the present study provides evidence
and limited the intensity of stimulation that could be for a signicant effect of IAP on spinal stiffness. When
used. Despite the discomfort, there was no or little IAP was increased by 1.85.9 kPa, the spinal stiffness
increase in ES or abdominal muscle EMG activity was increased by 831% from control values recorded at
between the stimulation and control trials. We acknowl- the end of a normal expiratory effort. Assuming that the
edge other muscles that were not recorded, such as the relationship between IAP and stiffness is linear
deep paraspinal muscles, may inuence stiffness. In (although this may not be the case), extrapolation from
addition, stress in the abdominal wall is necessary to the linear regressions calculated for each subject
produce IAP, thus passive tension of the abdominal suggests that a large increase in stiffness may occur
muscles is not excluded in this model. Although the with IAP changes of 5220 cm H2O that have been
number of subjects was small, the results were consistent recorded during functional activities (Cresswell et al.,
and all showed a positive relationship between the 1993; Gandevia et al., 1990; Grillner et al., 1978;
amplitude of IAP and the increase in spinal stiffness. Harman et al., 1988; Hemborg et al., 1985; Hodges et
Recent data using a porcine model have conrmed these al., 1997; Marras et al., 1985). The amplitude of stiffness
ndings (Hodges et al., 2003, unpublished observations). increase (831%) is similar to the 1241% increase in
The only result that varied considerably between stiffness observed during voluntary contraction of ES at
subjects was the difference in stiffness between L2 and 1030% of a maximal voluntary contraction (Shirley et
L4 which was greater for subject 3. The reason for this al., 1999). Our data cannot be explained by activity of
difference is unclear and could not be explained by ES during the phrenic nerve stimulation because the ES
differences in muscle activity or stimulation intensity. muscle was either inactive or minimally active. Further-
The measure of posteroanterior stiffness of the spine more, while a low-level ES activity was present during
is a composite measure and is inuenced by stiffness of some stimulation trials; when this was voluntarily
the entire spine and its supporting structures, for matched in additional trials without increased IAP, the
instance soft tissue compression, extension of the spine, increase in spinal stiffness was less than that recorded
anterior rotation of the pelvis, deformation and rigid- for the stimulation trials.
body displacement of the ribcage and anterior shear of In the present study, stiffness of the spine was
the target vertebra all occur in response to the poster- increased by IAP without concurrent activity of the
oanterior pressure (Lee et al., 1995). However, the abdominal muscles. This has been suggested previously
stiffness of the segments at which the force is applied (McGill and Norman, 1993) and is consistent with the
will contribute signicantly to the overall measurement. elevation of IAP in tasks such as arm movements that
In the present study, motion of the rib cage was challenge the stability of the spine in multiple directions
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P. W Hodges et al. / Journal of Biomechanics 38 (2005) 18731880 1879

(Hodges et al., 1999), addition of loads to the front and 5. Conclusion


back of a harness over the shoulders (Cresswell et al.,
1994), with multiple directions of support surface IAPin the absence of abdominal and back extensor
translation (Hodges et al., 2004). These data suggest activityaugments stiffness of the spine. Thus, modula-
IAP modulation may contribute to the general stiffness tion of IAP provides an additional mechanism for the
of the spine for control of perturbations in multiple central nervous system to control spinal stability during
directions. functional activities and may simplify this control by
There has been debate whether IAP produces a trunk providing a non-direction-specic increase in stiffness.
extension moment and its signicance. Notably, it has
been argued that stability of the spine may be increased
by antagonist exion (abdominal muscle) and extension
(IAP) moments (Cholewicki et al., 1999a; Cholewicki Acknowledgements
and McGill, 1996; Gardner-Morse et al., 1995). As the
abdominal muscles were not active in the present study, Financial support was provided by the National
increased spinal stability from antagonist moments is Health and Medical Research Council and Physiother-
unlikely to explain the increase in stiffness identied apy Research Foundation of Australia.
here, although the stiffness of the relaxed exor muscles
cannot be excluded.
An important consideration is that IAP is not References
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