2015 the Influence of Simulated Transversus Abdominis Muscle Force on Sacroiliac Joint Flexility During Asymmetric Moment Application to the Pelvis

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The influence of simulated transversus abdominis muscle force on sacroiliacjoint flexibility during asymmetric moment application to the pelvis

Rafael Gnat, Kees Spoor, Annelies Pool-Goudzwaard

PII: S0268-0033(15)00170-9DOI: doi: 10.1016/j.clinbiomech.2015.06.006Reference: JCLB 3986

To appear in: Clinical Biomechanics

Received date: 19 February 2015Accepted date: 8 June 2015

Please cite this article as: Gnat, Rafael, Spoor, Kees, Pool-Goudzwaard, Annelies, Theinfluence of simulated transversus abdominis muscle force on sacroiliac joint flexibilityduring asymmetric moment application to the pelvis, Clinical Biomechanics (2015), doi:10.1016/j.clinbiomech.2015.06.006

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The influence of simulated transversus abdominis muscle force on sacroiliac

joint flexibility during asymmetric moment application to the pelvis

Rafael Gnat, PhDa,b,c

, Kees Spoor, PhDa, Annelies Pool-Goudzwaard, PhD

a,d

a

Department of Neuroscience, Erasmus MC, University Medical Centre Rotterdam, P.O. Box

2040, 3000 CA Rotterdam, The Netherlands.

b

Motion Analysis Laboratory, Faculty of Physiotherapy, University of Physical Education, ul.

Mikolowska 72, 40-065 Katowice, Poland.

cFaculty of Physiotherapy, Academy of Business, ul. Cieplaka 1c, 41-300 DąbrowaGórnicza,

Poland.

dResearch Institute MOVE, Faculty of Human Movement Sciences, VU University Amsterdam,

Van der Boechorststraat, 9, 1081 BT Amsterdam, The Netherlands

Corresponding author:

Rafael Gnat

University of Physical Education, Faculty of Physiotherapy

ul. Mikolowska 72

40-065 Katowice

Poland

tel: +48 515 957 646; e-mail: [email protected]

Word count abstract: 262

Word count text: 3088

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ABSTRACT

Background

The role of so-called local muscle system in motor control of the lower back and

pelvis is a subject of ongoing debate. Prevailing beliefs in stabilizing function of

this system were recently challenged. This study investigated the impact of in

vitro simulated force of transversely oriented fibres of the transversus abdominis

muscle (a part of the local system) on flexibility of the sacroiliac joint during

asymmetric moment application to the pelvis.

Methods

In 8 embalmed specimens an incremental moment was applied in the sagittal

plane to one innominate with respect to the fixed contralateral innominate.

Ranges of motion of the sacroiliac joint were recorded using the Vicon Motion

Capture System. Load-deormation curves were ploted and flexibility of the

sacroiliac joint was calculated separately for anterior and posterior rotations of

the innominate, with and without simulated muscle force.

Findings

Flexibility of the sacroiliac joint was significantly bigger during anterior rotation

of the innominate, as comapred to posterior rotation (Anova P<0.05). After

application of simulated force of transversus abdominis, flexibility of the joint did

not change both during anterior and posterior rotations of the innominate.

Interpretation

A lack of a stiffening effect of simulated transversus abdominis force on the

sacroiliac joint was demonstrated. Earlier hypotheses suggesting a stiffening

influence of this muscle on the pelvis cannot be confirmed. Consistent with

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previous findings smaller flexibility of the joint recorded during posterior rotation

of the innominate may be of clinical importance for physio- and manual

therapists. However, major limitations of the study should be acknowledged: in

vitro conditions and simulation of only solitary muscle force.

Keywords: pelvis, sacroiliac joint, transversus abdominis, flexibility

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1. INTRODUCTION

The role of so-called local muscle system (Bergmark 1989) in motor

control of the lower back and pelvis is a subject of ongoing debate.

Prevailing beliefs in an exclusive stabilizing function of this system as well as

studies leading to the formulation of such ideas (e.g. Hodges and

Richardson 1997ab, 1998, Hodges and Gandevia 2000, Sapsford et al.

2001ab, Ferreira et al. 2006, 2007, Tsao and Hodges 2007) were recently

challenged (Cleland et al. 2002, Koumantakis et al. 2005, Mills et al. 2005,

Allison and Morris 2008, Mannion et al. 2008, Lederman 2010, Burns et al.

2011, Reeves et al. 2011, Hodges et al. 2013). Indeed, earlier evidence

suggested that local (deep) muscles of this region, inserting on or deriving

from the lower lumbar spine and pelvis (e.g. transversus abdominis (TrA),

lumbar multifidus, pelvic floor), have the potential to decrease flexibility and

thus stabilize the articular junctions. In case of the pelvis, Richardson et al.

(2002) reported that after voluntary contraction of the TrA, “laxity” of the

sacroiliac joint decreases. Pool-Goudzwaard et al. (2004) provided partial

confirmation of this finding demonstrating decreased flexibility of the

sacroiliac joint during in vitro simulation of pelvic floor activity. However,

such an effect was limited to female specimens and occurred after

mimicking multiple pelvic floor muscles. In line with these studies, Pel et al.

(2008) created a biomechanical simulation model showing an increase in

compression of the sacroiliac joint linked to activation of transversely

oriented TrA fibres as suggested earlier by Snijders et al. (1995). In contrast

with these studies, recently Gnat et al. (2013) demonstrated lack of a

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stiffening effect of simulated TrA muscle force on the pubic symphysis in

vitro. In line with their results, also the claim of a stiffening effect of TrA on

the sacroiliac joint (SIJ) seems questionable, although the anatomy and

hence biomechanical action of this muscle (Askar 1977, Rizk 1980)

suggests a compressive effect on the SIJ, as partly demonstrated by

previous studies (Snijders et al. 1995, Richardson et al. 2002, Pool-

Goudzwaard et al. 2004, Pel et al. 2008).To our knowledge no in vitro study

has proven the stiffening effect of simulated TrA activity on the SIJ.

The present study investigated the impact of in vitro simulated force

of transversely oriented fibres of the TrA on flexibility of the SIJ during

asymmetric loading of the pelvis. Flexion (linked to SIJ counternutation) and

extension (linked to SIJ nutation) rotations in the sagittal plane of one

innominate with respect to the other were used to mimic the natural

behaviour of the pelvis during e.g. locomotion. Our secondary objective was

to compare SIJ flexibility for flexion and extension rotations of the

innominate. Such objective was formulated since previous studies using

similar methodology (e.g. Jacob and Kissling 1995, Smidt et al. 1995,

Sturesson et al. 2000 ab, Agarwal et al. 2014) did not address this issue.

Moreover, for quite a long time extension of the innominate (SIJ nutation)

has been regarded as the ‘position of stability’ (or close-packed position)

protected by larger ligamentous guard, as opposed to flexion of the

innominate (SIJ counternutation) limited only by the thin anterior

ligamentous complex and long dorsal sacroiliac ligament (Vleeming et al.

1989ab, 1996).

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Findings of this study can be of importance in the debate whether

local muscles indeed have a stabilizing function in contrast to other muscles

of the trunk. Outcome of this debate can interfere with current treatment

modalities employed in e.g. management of patients with postpartum pelvic

girdle pain (Stuge et al. 2004) or demonstrating difficulties in transferring

load across the pelvic ring (Mens et al. 2001, Beales et al. 2010). Analysis of

SIJ flexibility for flexion and extension of the innominate relative to the

sacrum may also add to our understanding of SIJ function in human gait.

2. METHODS

2.1. Material

Eight embalmed specimens (6 females, mean age at time of death

70.3 (±5) years, embalming time 3-6 months) consisting of the pelvis and L5

vertebrae with all ligaments and capsules intact were available.

2.2. Experimental set-up

In our specimens, an incremental torque was applied to one

innominate in the sagittal plane while the other innominate was fixed to a

custom-made frame (Fig. 1). To enable both torque application to one

innominate and fixation of the opposite innominate, a rigid metal plate was

screwed to each innominate through the compact bone at the height of the

iliac crest, above the acetabulum and through the ischial tuberosity. One

plate was attached to the frame to fix the bone, while the second was

connected to a steel bar and axle to allow application of an incremental force

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resulting in a moment in the sagittal plane. To allow three-dimensional

movements of the innominate on the non-fixed side and the sacrum, the axle

was equipped with two universal joints and one prismatic sliding joint (Fig. 1).

Torque was exerted on the axle by a custom-made pneumatic traction

system installed on the frame. The force was transmitted by non-elastic cord

to a steel disk (diameter 300 mm) and then to the axle and innominate. To

calculate the real moment applied to the bone a torque transducer was

placed between the steel disk and the bar with two universal joints (Fig.1).

Throughout the whole measurement its signals were registered with a

sampling frequency of 10 Hz.

Prior to flexibility analysis, it was necessary to record ranges of

motion of the SIJ in the sagittal plane during the specimen loading. To

achieve this the Vicon MX Motion Capture System (Vicon Motion Systems,

Oxford, UK) was used. A total of 11 reflective markers (diameter 9.5 mm)

were screwed to the specimen (4 per each innominate, 3 per sacrum). To

minimize interference by bone deformations (especially in the lower part of

the innominate), in the current analysis only the 9 markers located close to

the SIJs (Fig.2) were used and the remaining two markers in the pubic

symphysis area (not shown in the Fig.2) were omitted. Markers were

illuminated by an infrared light source mounted on each of four video

cameras equipped with a 20 mm lens (Sigma, Tokyo, Japan). A sampling

frequency of 100 Hz was used which was fairly enough for the employed,

semi-static mode of load application. The precision of the measurement

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estimated on a mechanical model was equal to 0.1 deg for angular and 0.1

mm for linear measurements.

During each test an incremental torque was first applied to either the

left or right innominate bone (randomly chosen) in a semi-static, step-wise

manner. The opposite innominate was properly fixed and remained

immovable throughout the trial. During consecutive stages of the procedure

(see below) the torque increased/decreased in load-steps ranging from 3 to

7 Nm applied with 20 s intervals. Starting from the unloaded state, we used

larger load-steps (7 Nm) and approaching maximal torques they were

gradually becoming smaller (minimally 3 Nm). This prevented specimen

destruction when maximal loads were in use. The torque during each load-

step increased/decreased at a rate of 2 Nm/s. After each load-step was

completed, the position of the markers was captured in the Vicon system

with a 10 s latency.

Using this mode of torque application, after application of the maximal

flexion torque in the sagittal plane (FT, anterior rotation about Y-axis of the

reference system (Fig.2)), the load was step-wise released until the moving

innominate returned to its neutral position. This was directly followed by a

step-wise increasing of extension torque (ET, posterior rotation about Y-axis

of the reference system). Subsequently, the ET load was released until the

neutral position. Finally, FT was step-wise applied again until its maximum.

After each step positions of the markers were captured. The number of load-

steps during application of FT and ET was not fixed. To measure the range

of motion during the procedure an electronic goniometer was mounted on

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the steel disk (Fig.1). The load increments were ceased when during two

consecutive, final load-steps the range of motion (ROM) recorded by the

goniometer increased by less than 0.1 deg.

The same procedure was repeated with simulation of the force

exerted by transversely oriented fibres of the TrA on the pelvis. To achieve

this, a rubber band was transversely screwed to the innominates through

holes at the height of the anterior superior iliac spines (Fig. 2), pulling them

towards each other with a force of 120 ± 5 N (Mens et al. 2006, Pel et al.

2008).

The whole procedure was repeated with the torque applied to the

other innominate. Therefore, in total 4 series of measurement were

performed: 1) torque applied to side 1 of the pelvis (L or R depending on

randomization); 2) torque applied to side 1 with simulated TrA force; 3)

torque applied to side 2 of the pelvis; 4) torque applied to side 2 with

simulated TrA force.

2.3. Data analysis

The first stage of each series of measurement for each specimen (i.e.

unloaded state to maximal FT) was considered a preconditioning stage and

this part of the data was ignored. In this way the tissues could ‘adjust’ to the

load and artefacts associated with this process were avoided. Therefore,

only the following two trajectories of a single loading cycle were studied: 1)

t1: maximal FT – unloaded state – maximal ET; and 2) t2: maximal ET –

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unloaded state – maximal FT (Fig. 3 shows qualitatively an example of a

load deformation curve).

The parameters of the rotation axis of relative motion between bones

were calculated from the positions of the sacral and innominate markers

after each loading step (Spoor and Veldpaus 1980, Söderkvist and Wedin

1993).The sagittal plane SIJ ROM is represented by the rotations of the

innominate in relation to the sacrum about the Y axis of the reference

system (Fig.2). These rotations are defined as follows: flexion is anterior

rotation about the Y-axis; extension is posterior rotation about the Y-axis

The coordinate system was attached to the fixed innominate bone.

Subsequently, load-deformation curves were plotted (for the 4 series

of the measurement and two directions of torque application: FT and ET) for

trajectories t1 and t2. Slopes of the adjusted linear regression lines (ROM vs

torque) were calculated. As visible in Figure 3, two regression lines for each

direction of torque application (FT and ET) were drawn and two slopes were

calculated (F1, F2 and E1, E2). The mean value of the two slopes for each

torque direction was considered a measure of SIJ flexibility. Defined in such

way, the slope is directly proportional to flexibility of the joint.

2.4. Statistical analysis

Since in small samples it is difficult to reliably test the data for normal

distribution, both parametric and non-parametric tests were applied. The

outcomes were, however, similar and therefore normal distribution of the

data was assumed. The results of the parametric tests were presented, i.e. a

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mixed model of Anova with one independent factor: torque direction (FT and

ET) as well as one repeated factor: series of measurement (side 1 of the

pelvis; side 1 with TrA; side 2 of the pelvis; side 2 with TrA). Significance

level was set at P<0.05.

3. RESULTS

Maximal recorded FT and ET for all specimens were equal to 76.40

Nm and 72.53 Nm; the maximum values averaged over all specimens were

51.75 (SD 11.14) Nm and 52.62 (SD 10.80) Nm, respectively. No significant

difference was found between them.

Mean values and standard deviations of the slopes recorded during

application of the FT and ET are presented in the Table 1. Analysis of Anova

results revealed significant main effect for the independent factor, i.e. torque

direction (F=4.826; P=0.037). The FT slope (marginal mean 0.022 deg/Nm)

was significantly bigger than ET slope (marginal mean 0.014 deg/Nm),

which means that flexibility during application of FT was bigger (Fig.4A,

Tab.1). Main effect for the repeated factor (F=0.471; P=0.703) was not

significant (marginal means of the slopes for consecutive series of

measurement 0.017 deg/Nm, 0.019 deg/Nm, 0.017 deg/Nm, 0.018

deg/Nm)(Fig.4B). So was the interaction of the independent and repeated

factors (F=2.099; P=0.107)(Tab.1). This means that after application of

simulated TrA force flexibility of the SIJ did not change both during

application of FT and ET.

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4. DISCUSSION

In this study the SIJ flexibility was investigated in two experimental

conditions (without/with TrA force simulation). It is difficult to compare the

recorded levels of flexibility with outcomes of other studies since only few

investigated this same issue in a comparable way. Pool-Goudzwaard et al.

(2003) recorded slopes of regression lines (ROM vs torque) in the range of

0.046-0.124 deg/Nm. In another study (Pool-Goudzwaard et al. 2004) slopes

of 0.06 deg/Nm in males and 0.13 deg/Nm in females were reported. In the

current study lower levels of flexibility were registered (maximal mean slope

of 0.025 deg/Nm for FT with TrA force simulation in series 2, Tab.1). Such

observations may be explained by different specimen mounting or

embalming time (the two studies mentioned above do not provide data on

embalment duration).

The main objective of this study was to investigate whether in vitro

simulated action of the TrA exerts a stiffening effect on SIJ during

asymmetric loading of the pelvis. Previous in vivo studies and biomechanical

models tended to support such an effect of TrA contraction (Snijders et al.

1995, Richardson et al. 2002, Pel et al. 2008). However, based on the

present data, this effect cannot be confirmed. No significant SIJ flexibility

decrease was recorded during simulation of the TrA force. This finding

should not be attributed to gradual tissue damage during 4 consecutive

series of measurement since flexibility shows systematic tendency to

increase after TrA force simulation (between series 1 and 2; 3 and 4) and to

decrease after removal of this force (between series 2 and 3)(Fig.4B). There

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are several possible explanations for such findings. First of all, exclusively

the transverse portion of the TrA fibres was mimicked in vitro. The rationale

for this was that only from these fibres a large compressive force on the

pelvis could be expected (Snijders et al. 1995). In vivo, a more global

activation of the TrA should be present, as well as activation of numerous

synergistic muscles of the local system, which were not included in the

current setting. Such a simplified model was unable to reflect the whole

spectrum of physiologic behaviour of both the TrA and other local muscles. It

is known that in vivo activation of the TrA takes place in synergy with pelvic

floor muscles (Sapsford et al. 2001ab) and the diaphragm (Allison et al.

1998, Hodges and Gandevia 2000). Simulation of these muscle forces might

have more strongly influence the flexibility of the SIJ. Observations from an

in vitro study by Pool-Goudzwaard et al. (2004) seem to support this notion.

Authors demonstrated a tendency to decrease SIJ flexibility only after

simulation of multiple forces produced by pelvic floor muscles. Perhaps a

more complex specimen than used in the present study (pelvis, lumbar and

lower thoracic spine with ribs), and reproduction of multiple vectors

generated by the TrA and other deep muscles, would help to more

realistically verify the hypothesis concerning their role in decreasing flexibility

of the pelvic girdle. These observations (Richardson et al. 2002, Pool-

Goudzwaard et al. 2004, Pel et al. 2008) allow to speculate that muscle

synergisms and coactivation within the local system have greater impact on

the flexibility of the pelvic region than isolated activation of single muscles.

This issue has already been addressed by others (e.g. Cholewicki et al.

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1997, Gardner-Morse and Stokes 1998). It might also be clinically relevant.

Within many therapeutic approaches (both older and modern) exercises are

implemented aiming to enhance the patient’s ability to activate single local

muscles (Pilates and Miller 1945, Richardson and Jull 1995, Hides et al.

1996, O’Sullivan et al. 1997, Comerford and Mottram 2001, Stuge et al.

2004). To date, no data are available demonstrating that restoration of such

an ability is equivalent to restoration of the desired synergisms. Probably, in

lower back motor control training and testing the ability to coactivate

numerous local muscles might deserve more attention. Further studies to

explain these issues are strongly needed.

Differences between flexibility recorded during application of FT and

ET is also worth attention and conforms to previous studies. Extension of the

innominate is linked to nutation of the SIJ, which is long regarded as the

more stable position of the joint than counternutation (linked to innominate

flexion)(Vleeming et al. 1989ab, 1996). It seems that flexibility of the SIJ

might be subjected to modulation by different flexion/extension angles of the

innominate bone. This information may be of importance for therapists

dealing with pelvic dysfunctions and trying to find associations between

them and features of individual gait. For example, one may speculate that

pelvic pain occurring at heel strike is linked to excessive flexibility of the SIJ.

In the field of manual therapy this observation suggests that clinicians may

gain different manual sensations when assessing SIJ using movements of

anterior and posterior rotations of the innominate. Anterior rotation may

produce ‘softer’ and less stiff feel as compared to stiffer posterior rotation. In

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therapy, when applying manual thrust techniques or mobilizations

incorporating anterior innominate rotation movement there may be a need to

cover larger ROM before reaching the motion barrier in comparison to

techniques incorporating posterior rotation.

Apart from the fact that only the transverse portion of the TrA fibres

was mimicked, other limitations of the present study need to be addressed.

First, the limitations linked to in vitro studies are known and inherent.

Conclusions derived from cadaveric data cannot be directly applied to living

organisms. Long-term embalming might decrease elasticity of the tissues,

and flexibility of the SIJ might differ from in vivo conditions. It is also possible

that loads applied in this study exceeded those associated with normal daily

life activity. Moreover, the SIJ loads in vivo depend on muscle forces and

are therefore different from the passive loads in cadaveric experiments, with

consequences for relative bone positions. The history of our specimens

remained unknown as well. It was only possible to exclude specimens with

evident bony anomalies. The generalizability of our conclusions is therefore

limited. Additional studies on fresh cadaveric material, and also in vivo, are

needed to verify the results of this experiment.

5. CONCLUSIONS

1. A lack of a stiffening effect of simulated TrA muscle force on SIJ was

demonstrated. Earlier hypotheses suggesting a stiffening influence of this

muscle on the pelvis cannot be confirmed.

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2. Flexibility of the SIJ was smaller for extension of the innominate relative to

the sacrum (SIJ nutation) than for flexion (SIJ counternutation).

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CONFLICT OF INTEREST

We inform that no sponsors were involved in the study. All expenses were covered by

former Department of Biomedical Physics and Technology, Erasmus University,

Rotterdam. Therefore, no conflict of interest is associated with the presented study.

ACKNOWLEDGEMENTS

We would like to acknowledge the kind assistance of very talented Mrs. Karine

Bollerot, PhD, who prepared for us figures 1 and 2.

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TABLES

Table 1. Mean values (standard deviations)(deg/Nm) of the slopes recorded for sagittal plane

rotations of the innominate in relation to the sacrum (about Y axis of the reference system)

during application of flexion (FT) and extension (ET) torques and for four series of measurement:

1) torque applied to side 1 of the pelvis; 2) torque applied to side 1 of the pelvis with simulated

transversus abdominis (TrA) force; 3) torque applied to side 2 of the pelvis; 4) torque applied to

side 2 with TrA force.

Torque series 1 series 2 series 3 series 2

FT 0.022 (0.012) 0.025 (0.017) 0.020 (0.012) 0.020 (0.013)

ET 0.13 (0.007) 0.12 (0.008) 0.14 (0.007) 0.15 (0.010)

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FIGURE CAPTIONS

Figure 1. Experimental set-up with metal plates (A) screwed to both

innominates, one fixed to the frame, the other connected to a steel bar with

two universal joints (B), a torque transducer (C), a pulley (D) and a prismatic

sliding joint (E). Electronic goniometer (F) was used to control range of

motion during the procedure. To maintain clarity, pneumatic cylinders

generating the necessary forces are not shown.

Figure 2. The coordinate system and position of the sacral (S 1,2,3) and

innominate (I 1(1), 2(2), 3(3)) markers. The spring represents an elastic

rubber band imitating the force exerted by the transversus abdominis muscle

on the two innominates.

Figure 3. A representative schematic load-deformation curve for the rotations of

the innominate in relation to the sacrum about the Y axis of the reference

system (flexion(positive)/extension(negative)). Data from the first stage (i.e.

unloaded state – maximal flexion torque (FT)) were ignored (not shown).

Only the two trajectories were used for the analysis: t1) maximal FT–

unloaded state – maximal extension torque (ET), and t2) maximal ET –

unloaded state – maximal FT. Adjusted linear regression lines for t1 and t2

are presented by dotted lines. Two regression lines were drawn for ET (E1

and E2) and two other for FT (F1 and F2). Slopes of these regression lines

were regarded as measures of flexibility. The mean value of slopes E1 and

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E2 and the mean value of slopes F1 and F2 were calculated and subjected

to further analysis. Defined this way, the slope is directly proportional to joint

flexibility.

Figure 4. Marginal mean values of the slopes of regression lines recorded for

the two factors of Anova design (main effects): independent (A) – torque

direction (flexion (FT) vs extension (ET)); and repeated (B) – series of

measurement (series 1-4: 1) torque applied to side 1 of the pelvis; 2) torque

applied to side 1 of the pelvis with simulated transversus abdominis (TrA)

force; 3) torque applied to side 2 of the pelvis; 4) torque applied to side 2

with TrA force). Whiskers indicate 95% confidence intervals.

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Figure 1

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Figure 2

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Figure 3

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Figure 4

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HIGHLIGHTS

Flexibility of the sacroiliac joint was investigated in vitro.

The force of transversus abdominis muscle was simulated during the

procedure.

Simulation o the muscle force did not decrease flexibility of the joint.

This effect ocurred both during anterior and posterior rotations of the

innominate.

Overall flexibility of the joint was smaller during innominate posterior

rotation.