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Manual Therapy 14 (2009) 484489

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Manual Therapy
journal homepage: www.elsevier.com/math

Original Article

The inuence of increasing sacroiliac joint force closure on the hip


and lumbar spine extensor muscle ring pattern
Hiroshi Takasaki a, b, *, Takeshi Iizawa b, c, Toby Hall d, Takuo Nakamura e, Shouta Kaneko b
a
Graduate School of Health Sciences, Sapporo Medical University, South-1, West-17, Chuo-ku, Sapporo, Hokkaido, Japan
b
Shinoro Orthopedic, 4-5-3-9, Shinoro, Kita-ku, Sapporo, Hokkaido, Japan.
c
School of Health Sciences, Sapporo Medical University, South-1, West-17, Chuo-ku, Sapporo, Hokkaido, Japan
d
Adjunct Senior Teaching Fellow, School of Physiotherapy, Curtin University, Perth, Western Australia
e
Department of Physical Therapy, Sapporo Medical University School of Health Sciences, South-1, West-17, Chuo-ku, Sapporo, Hokkaido, Japan

a r t i c l e i n f o a b s t r a c t

Article history: The prone hip extension (PHE) test is commonly used in the evaluation of lumbo-pelvic dysfunction. It
Received 30 May 2008 has been suggested that altered motor control identied by the PHE test can be improved with the
Received in revised form application of compression force across the pelvis, to increase force closure on the sacroiliac joint (SIJ).
14 October 2008
This repeated measure study design investigated the effect of three levels of pelvis compression (0 N,
Accepted 8 November 2008
50 N, 100 N) on the muscle ring pattern during the PHE test in 20 asymptomatic male subjects tested on
two occasions 4-weeks apart. The right gluteus maximus, right semitendinosus and bilateral lumbar
Keywords:
erector spinae were analyzed using surface electromyography (EMG). Subjects were instructed to
Muscle ring pattern
Sacroilliac joint perform right hip extension in prone position while maintaining knee-extension in each measurement
Gluteus maximus condition. Compared with the onset of the semitendinosus muscle, gluteus maximus became active
263.3  99.5 ms later with no pelvic compression, 183.5  77.9 ms later with 50 N compression,
91.5  49.7 ms later with 100 N compression. While signicant differences (a 0.05) were found in EMG
onset for gluteus maximus under different levels of pelvis compression, this was not the case for the
erector spinae, which had an inconsistent pattern of temporal onset and was not inuenced by the level
of pelvis compression force.
2008 Elsevier Ltd. All rights reserved.

1. Introduction pattern of activation of muscles during PHE represents the muscle


recruitment pattern of hip extension during gait (Lehman et al.,
Functional stability of the pelvis is generated by a combination 2004). According to Janda (Janda, 1978), the ideal sequence of
of force closure and form closure. The term form closure was muscle activation during the PHE test in temporal order is ipsilat-
coined by Snijders and Vleeming (Vleeming et al., 1990a, b; Snijders eral hamstring, ipsilateral gluteus maximus, and contralateral
et al., 1993a, b) and is used to describe how the joints shape lumbar erector spinae.
contributes to stability. On the other hand, force closure refers to It has been theorized that aberration in the temporal recruitment
other forces acting across the joint to create stability. According to pattern of these muscles decreases the stability of the pelvis during
theoretical modeling of force closure effects (Pel et al., 2008), the gait and thus hinders the bodys mechanical efciency. One of the
application of 50 N medial compression force at the anterior most commonly described patterns of dysfunction seen clinically
superior iliac spine increases SIJ compression force by 52%. during PHE is too much delay in the recruitment of the gluteus
Furthermore, it has been said that the stronger the force closure the maximus (Sahrmann, 2002). In this case hip extension is achieved
more form closure is obtained (Snijders et al., 1993a, b). by hamstring muscle activation, this creates compensatory anterior
A number of tests have been developed which are said to pelvic tilt and thus lumbar hyperlordosis. In addition poor gluteus
evaluate the functional stability and control of the pelvis (Buyruk maximus strength and activation is postulated to decrease the
et al., 1995a, b, 1999; Mens et al., 1999, 2001; Lee and Lee, 2004). efciency of gait (Janda, 1992, 1996). Moreover, Sahrmann (Sahr-
The PHE test is one commonly used in the evaluation of lumbo- mann, 2002) has suggested that if the hamstrings are dominant, and
pelvic function (Lee and Lee, 2004). It has been theorized that the gluteus maximus is inhibited, abnormal displacement of the greater
trochanter can be palpated during the PHE, which is a nding
* Corresponding author. Shinoro Orthopedic, 4-5-3-9, Shinoro, Kita-ku, Sapporo,
reported in cases of hip pain (Sahrmann, 2002).
Hokkaido, Japan. Tel.: 81 011 772 7255; fax: 81 011 772 7256. A number of studies have investigated the temporal pattern of
E-mail address: physical_therapy_takasaki@yahoo.co.jp (H. Takasaki). muscle recruitment during PHE (Bullock-Saxton et al., 1994; Vogt

1356-689X/$ see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2008.11.003
H. Takasaki et al. / Manual Therapy 14 (2009) 484489 485

and Banzer, 1997; Lehman et al., 2004). To date, no consistent


pattern of activation has been found. However, one common thread
through these various studies is the consistent report of delayed
activation of the gluteus muscle compared with the hamstrings
(Vogt and Banzer, 1997; Lehman et al., 2004).
It has been said that if the efciency of PHE was improved with
the application of compression force across the pelvis, this might
have some effect on improving force closure and therefore improve
the muscle ring pattern (Lee and Lee, 2004). However, to date no
studies have investigated the inuence of compressive force across
Fig. 2. Prone hip extension.
the pelvis on the PHE test.
The purpose of this study was to determine whether compres-
sive force applied across the pelvis inuences the muscle ring
patterns of the semitendinosus, gluteus maximus, and erector 143.2  11.2 N. As a number of subjects complained of pain when
spinae. We hypothesized that applying compression force across compression force of 150 N was applied this level of force was not
the pelvis would reduce the onset delay for gluteus maximus and used in the main study.
semitendinosus while having no inuence on the erector spinae
muscles. 2.2. Subjects

For this study, 20 males (Right leg dominant, Average height:


2. Methods
172.6 (SD 5.40) cm, Average weight: 64.3 (SD 5.2) kg, Average
age: 22.0 (SD 1.3) years old) with no history of lumbar, sacroiliac
2.1. Pilot study
or lower limb injury within the past year were recruited from
undergraduate students in Sapporo medical university. Subjects
Prior to the main experiment, a preliminary study was designed
who had a previous history of lumbar surgery, spondylophathies, or
to determine the amount of force routinely applied across the
arthritic disorders were excluded. Individuals with past episodes of
pelvis to increase force closure during the PHE. Five physical ther-
ankle sprain (grade 2 or 3) were also excluded because Bullock-
apists, each with three years post-graduate experience, were asked
Saxton et al. reported that ankle sprain inuenced the muscle ring
to apply three kinds of pressure to ve participants (ve males,
pattern of the gluteus maximus (Bullock-Saxton et al., 1994).
Average age: 22.2 (SD 0.8) years old) across the pelvis, simulating
the PHE test (Fig. 1): normal, strong, and maximum. The therapists
were required to apply the pressure on the pelvis bilaterally 2.3. Instrumentation
through hand-held dynamometers (mTas, ANIMA Co. Ltd., Tokyo).
The average force under normal pressure was 51.8  11.0 N, The activation patterns of the right gluteus maximus, right
under strong pressure 98.2  11.5 N and under maximum pressure semitendinosus muscle group and bilateral lower erector spinae
were assessed by surface EMG. Surface electrodes (Ag/AgCl) were
placed in pairs and parallel to the muscle bers (Cram et al., 1998).
For gluteus maximus, electrodes were placed at mid belly between
sacral vertebrae and the greater trochanter. For semitendinosus,
electrodes were attached at the mid point between the inferior
gluteal fold and knee joint line. For lower erector spinae electrodes
were placed longitudinally 2 cm lateral to the L3 spinous process,
bilaterally.

Condition A Condition B

PHE PHE
without pelvic without pelvic
compression compression
5 5
10 people
Rest (2min) 20 people
10 people Rest (2min)
PHE
Rest (2min) with 100 N PHE
compression without pelvic
PHE compression
with 50 N 5
Rest (2min)
compression
5 Rest (2min)
PHE
with 50 N PHE
Rest (2min)
compression without pelvic
5 compression
PHE 5
with 100 N Rest (2min)
compression Rest (2min)
5
PHE PHE
Rest (2min) without pelvic without pelvic
compression compression
5 5

Fig. 1. Procedure used in the pilot study to measure compressive force across the Fig. 3. Flow chart showing study protocol. Hatched circles indicate no measurements
pelvis using hand-held dynamometers. were taken during those trials.
486 H. Takasaki et al. / Manual Therapy 14 (2009) 484489

2.4. Procedures Table 1


Average Gluteus Maximus onset time for each subject relative to semitendinosus
muscle ring.
The protocol for testing is described in the ow chart in Fig. 2.
Due to operational and time constraints, the testing procedure was Subject No Compression 50 N 100 N No Compression
conducted in two parts with Condition A and B carried out one (1st) Compression Compression (2nd)

month apart using the same set of 20 subjects. Condition B was 1 130.4 83 60.2 61.0
2 137.2 85.8 59.0 65.0
essentially to determine the reliability of repeated measurements.
3 430.8 385.4 260.2 432.8
Subjects were instructed to lie on the measurement table in 4 243.0 214.6 124.2 131.2
a prone position and perform right hip extension until the lower 5 327.2 212.2 93.2 133.8
edge of the patella was raised more than 15 cm from the starting 6 213.2 151.4 60.0 163.6
position while maintaining knee-extension (Fig. 3). 7 324.0 271.4 123.8 244.0
8 164.0 109.4 79.2 127.4
A standardized compressive force of zero, 50 N, and 100 N was 9 249.0 200.6 104.2 144.4
applied across the pelvis by the device shown in Fig. 4. Two 10 189.4 105.0 60.5 164.6
experimental conditions were employed; Condition A was PHE 11 213.0 150.4 61.2 154.8
under the three different levels of compressive force (0 N, 50 N and 12 316.4 210.6 106.8 153.0
13 190.0 83.0 22.2 79.2
100 N). For Condition A all subjects were initially evaluated with no
14 342.2 245.6 123.4 244.6
compression force. Half the sample was then tested with increasing 15 109.2 102.2 60.6 90.6
compression force (50 N and 100 N) and the remaining half tested 16 471.8 238.2 109.6 264.6
with reducing compression force (100 N and 50 N). The nal trials 17 316.6 229.8 122.0 201.0
in Condition A were with no compression force. Condition B was 18 367.6 239.4 88.2 201.6
19 230.8 148.8 46.4 175.6
PHE without compressive force (Fig. 3). For Condition A and B a set 20 299.4 203.4 64.4 197.2
of ve trials were obtained for each level of force, with a 2-min rest
Mean 263.3 183.5 91.5 171.5
period between each set. Subjects were instructed to perform hip
SD 99.5 77.9 49.7 84.3
extension at their natural speed, repeating the movement each
time from rest. The mean onset of muscle activity for each set was
calculated from the ve trials within that set.
Before the initiation of data collection, subjects provided written signals were full wave rectied, low- and high-pass ltered, with
informed consent. This study was approved by Sapporo medical cut-off frequencies of 500 and 10 Hz, respectively, and recorded at
university. a sampling rate of 1000 Hz (Sakamoto et al., 2009).
Muscle activation patterns were described after determining the
EMG onset for each muscle. The onset of muscular activity was
2.5. Statistics
considered to occur when the value exceeded two standard devi-
ations from the mean value observed at baseline for a 50 ms period
EMG data processing was performed using Acknowledge soft-
(Hodges and Bui, 1996; Brindle et al., 1999).
ware (Chart v.5.2.1, ADInstruments Pty Ltd., Australia). The EMG
Muscle onsets were calculated with respect to onset of muscle
activity for the semitendinosus muscle. A one-way ANOVA was
used to determine the inuence of pressure across the pelvis on the
timing of muscle onset relative to the onset of semitendinosus
muscle activity. Statistical analysis was performed using SPSS
version 11.5 (SPSS Inc., Tokyo, Japan). Statistical signicance was
attributed to P values less than 0.05.

3. Results

3.1. Gluteus maximus

Under Condition A, with the semitendinosus muscle acting as


the relative starting point at 0 ms, gluteus maximus become
active 263.3  99.5 ms later with no pelvic compression, 183.5 
77.9 ms later with 50 N compression, 91.5  49.7 ms later with
100 N compression, and 171.5  84.3 ms later when no pelvic
compression was repeated. In all subjects semitendinosus muscle
onset occurred prior to gluteus maximus (Table 1). Signicant
differences were found in EMG onset between no pelvic
compression and 50 N compression (P < 0.05), between no pelvic
compression and 100 N compression (P < 0.001) and between the
two trials of no pelvic compression (P < 0.01). Additionally, there
were signicant differences between EMG onset for 100 N
compression and 50 N compression (P < 0.01), and between 100 N
compression and the second trial of no pelvic compression
(P < 0.05) (Fig. 5).
Under Condition B, gluteus maximus contracted 270.2  90.3 ms
later than semitendinosus muscle during rst ve sets of PHE, and
218.5  71.2 ms later during the last ve sets of PHE.
Signicant differences were found in EMG onset between the
Fig. 4. Pelvis compression device. second trial of no pelvic compression in Condition A and the rst
H. Takasaki et al. / Manual Therapy 14 (2009) 484489 487

*p<0.05,p<0.01,p<0.001 2nd
Condition B
1st
2nd
Condition B
1st
No Compression (2nd)

100 N Compression
No Compression (2nd) Condition A
* 50 N Compression
100 N Compression
Condition A
No Compression (1st)
50 N Compression
* -100 -50 0 50
No Compression (1st)
Latency (ms)
-500 -400 -300 -200 -100 0
Latency (ms) Fig. 6. The latency (ms) of ipsilateral erector spinae compared with the onset of
semitendinosus for condition A and B. Negative values indicate delayed activation.
Fig. 5. The latency (ms) of gluteus maximus compared with the onset of semite- There was no signicant difference between any condition (a 0.05).
ndinosus for condition A and B. Negative values indicate delayed activation.

muscle, with the rst trials of no pelvic compression, were


trial in Condition A (P < 0.01), and between the average of the rst 17.7  35.7 ms prior, 2.1  39.9 ms prior with 50 N compression,
ve sets of trials in Condition B (P < 0.01) (Fig. 5). 2.1  32.4 ms later with 100 N compression, 6.7  40.5 ms prior
with the second set of trials of no pelvic compression. Activation
3.2. Ipsilateral erector spinae prior to semitendinosus muscle was seen in 15 out of 20 subjects
(Table 3). There was no signicant difference (a 0.05) between
Under Condition A, ipsilateral erector spinae became active any of these conditions (Fig. 7).
0.1  39.6 ms before the onset of the semitendinosus muscle with Under Condition B, contralateral erector spinae become active
the rst trials of no pelvic compression, 27.3  54.3 ms later with 11.4  38.0 ms prior to the onset of the semitendinosus muscle
50 N compression, 10.2  31.4 ms later with 100 N compression, during the rst ve sets of PHE, and 11.3  30.7 ms prior during the
and 13.4  37.2 ms later with the second set of trials of no pelvic last ve sets of PHE.
compression. In 13 out of 20 subjects the ipsilateral erector spinae There was no signicant differences (a 0.05) between any of
contracted before semitendinosus muscle (Table 2). There was no Condition A and B (Fig. 7).
signicant difference (a 0.05) between any of these conditions
(Fig. 6). 4. Discussion
Under Condition B, the ipsilateral erector spinae contracted
0.5  37.2 ms before the onset of the semitendinosus muscle during This study found gluteus maximus muscle onset was consis-
rst ve sets of PHE, and 1.4  31.1 ms prior in the last ve sets of tently delayed with respect to the semitendinosus muscle during
PHE. the PHE test. No such consistent pattern of temporal activation was
Signicant differences (a 0.05) were not found between any of found for either the ipsilateral or contralateral erector spinae,
Condition A and B (Fig. 6). which is in line with previous reports (Lehman et al., 2004).
Compression force across the pelvis, appeared to reduce the
3.3. Contralateral erector spinae onset delay of gluteus maximus, but this had no such effect on the
erector spinae in asymptomatic subjects.
Under Condition A, the averaged onset of the contralateral Delayed onset gluteus maximus muscle activation (relative to
erector spinae, compared with the onset of the semitendinosus the hamstring muscles) has been suggested as a signicant factor in

Table 2 Table 3
Average ipsilateral erector spinae onset time for each subject relative to semite- Average contralateral erector spinae onset time for each subject relative to sem-
ndinosus muscle ring. itendinosus muscle ring.

Subject No Compression 50 N 100 N No Compression Subject No Compression 50 N 100 N No Compression


(1st) Compression Compression (2nd) (1st) Compression Compression (2nd)
1 13.6 5.6 16.4 26.2 1 19.0 20.2 28.0 32.0
2 6.6 3.4 24.8 21.6 2 33.8 31.0 11.8 2.2
3 28.4 139.6 29.4 12.2 3 35.4 23.6 24.0 82.4
4 53.0 72.8 27.0 76.4 4 66.2 3.8 4.6 29.2
5 31.8 81.6 24.6 9.2 5 57.2 93.6 48.8 5.8
6 30.2 55.8 6.8 31.6 6 18.8 65.6 69.0 40.4
7 35.0 10.4 13.4 99.6 7 34.6 6.2 7.2 79.0
8 29.6 15.2 9.4 33.4 8 15.8 15.4 7.4 42.4
9 57.8 44.0 59.0 28.2 9 29.8 0.4 3.4 37.4
10 69.8 80.2 65.6 27.8 10 38.8 56.4 37.6 28.0
11 79.4 48.0 47.0 39.4 11 32.6 16.6 36.8 45.8
12 10.0 22.8 30.8 0.8 12 38.6 0.4 5.8 25.4
13 58 7.2 9.2 27.4 13 51.4 10.2 15.6 19.6
14 24.0 12.0 0.4 6.0 14 31.6 43.8 50.8 42.6
15 31.4 149.6 50.2 70.2 15 31.4 90.6 50.4 32.6
16 31.0 36 8.0 16.0 16 50.6 5.4 0.4 46.2
17 29.2 0.8 10.8 26.4 17 57.6 6.2 1.0 41.6
18 4.0 30.8 58.0 16.8 18 15.8 13.2 47.8 3.4
19 22.2 5.2 9.2 13.0 19 46.6 17.6 1.8 27.2
20 10.6 4.8 17.4 19.4 20 19.4 28.8 28.8 30.8

Mean 0.1 27.3 10.2 13.4 Mean 17.7 2.1 2.1 6.7
SD 39.6 54.3 31.4 37.2 SD 35.7 39.9 32.4 40.5
488 H. Takasaki et al. / Manual Therapy 14 (2009) 484489

2nd medial compression force on the pelvis increases force closure at


Condition B the SIJ (Pel et al., 2008). Similarly both Mens and Damen (Damen
1st
et al., 2002; Mens et al., 2006) found medially applied pelvis force
(using a pelvic belt) at the level of the anterior superior iliac spines
No Compression (2nd)
produced signicantly less SIJ laxity in both healthy women and
100 N Compression
Condition A those with pelvic pain.
50 N Compression The SIJ has been reported to be richly innervated (Solonen, 1957;
No Compression (1st) Ikeda, 1991; Grob et al., 1995). Ikeda (Ikeda, 1991) reported that the
-100 -50 0 50 ventral portion of the SIJ was mainly supplied by ventral ramus of
Latency(ms) the L5, whereas the lower ventral portion was mainly supplied by
ventral ramus of the S2. Thick, thin, and unmyelinated nerve bers
Fig. 7. The latency (ms) of contralateral erector spinae compared with the onset of
have been reported, which are compatible with a broad repertoire
semitendinosus for condition A and B. Negative values indicate delayed activation.
There was no signicant difference between any conditions (a 0.05). of sensory receptors, indicating encapsulated mechanoreceptors
(Ikeda, 1991; Grob et al., 1995). According to Indahl, et al. (Indahl
et al., 1999) stimulation of the porcine SIJ capsule elicited activity in
the development of hip pain (Sahrmann, 2002; Hungerford et al., the multidus muscle (L5 level), additionally stimulation of the
2003; Vogt et al., 2003). The present study and previous studies anterior aspect of the joint elicited responses in quadratus lum-
have reported delayed gluteus maximus activation in normal borum and gluteus maximus.
subjects (Bullock-Saxton et al., 1994; Vogt and Banzer, 1997; Leh- In our study, the stronger the force applied across the pelvis, the
man et al., 2004), but failed to reach agreement on the magnitude earlier the onset of gluteus maximus activity occurred. In contrast
of the delay. Latency of gluteus maximus contraction in our study of this was not the case for the erector spinae muscles. These ndings
male subjects with no compression was approximately 270 ms, in correspond with previous reports (Indahl et al., 1999)
contrast to 500 ms reported by Sakamoto et al (Sakamoto et al., With respect to the results of the latency of gluteus maximus
2009). In that study the standard deviation was three times larger compared with the onset of semitendinosus in Condition A,
at 300 ms. This disparity might be explained by gender differences, a signicant difference was found between the rst and second trial
with participants in Sakamoto et als study of both genders. Further of no compression. In contrast, repeated trials of no compression
research investigating a more diverse sample of normal subjects force in Condition B were not different and were no different to the
and patients with hip pain is required to identify whether a greater rst trial of no compression in Condition A. It appears that the
timing delay occurs in symptomatic subjects when compared to change in onset of gluteus maximus activity continued even after
healthy controls. pelvis compression force was removed. This result, suggests
Gluteus maximus activation has a major functional role in the a lasting effect of compression force, at least temporarily. We
early stance phase of gait, where 60% of body weight is transferred suggest that stimulation of the SIJ by the compressive force across
in 0.02 s, resulting in abrupt loading of the forward limb (Anderson the pelvis causes reex changes in muscle activation, which facili-
and Pandy, 2003). At this point the gluteus maximus compresses tates an earlier onset of gluteus maximus activity. It remains
the SIJ to provide stability of the pelvis (Hossain and Nokes, 2005). unclear how long this effect is maintained.
Additionally, it has been suggested that lack of control of the pelvis It is possible that other unidentied factors inuenced the
may further increase the movement of an already mobile lumbar muscle ring pattern, besides the SIJ compression/force closure
spine segment (McConnell, 2002). It has been established that theory. For example in our study standardization of the pelvis force
excessive movement, particularly in rotation of the lumbar motion application was achieved by the use of a mechanical device. No
segment, is a contributory factor to disc injury and torsional forces subject reported pain with this device, but it is possible that
may irrevocably damage the annulus brosus (Farfan et al., 1970; subjects may have felt discomfort or experienced difculty with
Kelsey et al., 1984). movement. It is known that experimentally induced pain changes
Our study analyzed the muscle ring pattern during hip the pattern of muscle activation around the pelvis, even in normal
extension in prone, as it has been suggested that the pattern of subjects (Hodges et al., 2003). However negating this possibility is
activation of muscles during PHE represents the muscle recruit- that changes to the ring pattern were maintained even after the
ment pattern of hip extension during gait (Lehman et al., 2004). To compression force was removed, indicating a carry over effect.
our knowledge no studies have compared muscle onset patterns Many further studies are required to investigate this phenomenon
between the two positions. There may be major changes to the as well as the duration of carry over effect, and whether changes to
pattern of activation of the lumbo-pelvic stabilizing muscles in the muscle ring pattern during PHE inuences the pattern of
prone compared to the upright posture. Additionally, gravitational recruitment during normal gait before clinical implications can be
inuences in both positions are different and may inuence both considered.
force and form closure and so pelvic stability. Therefore relating our
ndings of the ring pattern during the PHE test to the normal gait
cycle is not possible. Much further research is required comparing 5. Conclusions
the muscle ring pattern during normal gait with that found during
the PHE test. In asymptomatic males, gluteus maximus muscle onset was
The synovial SIJ is supported by the anterior, posterior and consistently delayed with respect to the semitendinosus muscle
interosseous sacroiliac ligaments. While the posterior sacroiliac during the PHE test, but no consistent temporal pattern of activa-
ligament is strong, the interosseous ligament is the strongest tion of the erector spinae was found. Compressive force applied
ligament between the sacrum and ilium (Clemete, 1997). When the medially across the pelvis signicantly reduced the muscle onset
therapist applies force across the pelvis, the strong sacroiliac liga- delay for gluteus maximus but had no effect on the erector spinae.
ments increase the lever arm acting on the SIJ, which theoretically
results in much greater compression force at the SIJ surface and
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