Manual Therapy 14 (2009) 415–420

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

Original Article

Effects of lumbopelvic joint manipulation on quadriceps activation

and strength in healthy individuals
Terry L. Grindstaff a, *, Jay Hertel a, James R. Beazell b, Eric M. Magrum b, Christopher D. Ingersoll a
a
University of Virginia, Charlottesville, VA, USA
b
University of Virginia-HEALTHSOUTH, Charlottesville, VA, USA

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

Article history: Lumbopelvic joint manipulation has been shown to increase quadriceps force output and activation, but
Received 4 June 2007 the duration of effect is unknown. It is also unknown whether lower grade joint mobilisations may have
Received in revised form 24 May 2008 a similar effect. Forty-two healthy volunteers (x  SD; age ¼ 28.37.3 yr; ht ¼ 172.8  9.8 cm;
Accepted 28 June 2008
mass ¼ 76.6  21.7 kg) were randomly assigned to one of three groups (lumbopelvic joint manipulation,
1 min lumbar passive range of motion (PROM), or prone extension on elbows for 3 min). Quadriceps
Keywords:
force and activation were measured using the burst-superimposition technique during a seated isometric
Force output
knee extension task before and at 0, 20, 40, and 60 min following intervention. Collectively, all groups
Manual therapy
Muscle activation demonstrated a significant decrease (p < 0.001) in quadriceps force output without changes in activation
Sacroiliac (p > 0.05) at all time intervals following intervention. The group that received a lumbopelvic joint
manipulation demonstrated a significant increase in quadriceps force (3%) and activation (5%) (p < 0.05)
immediately following intervention, but this effect was not present after the 20 min interval. Since
participants in this study were free of knee joint pathology, it is possible that they did not have the
capacity to allow for large changes in quadriceps muscle activation to occur.
Ó 2008 Elsevier Ltd. All rights reserved.

1. Introduction
Manual therapeutic interventions such as joint mobilisation or
manipulation have been shown to alter muscle force output and
activation. Specific to the lower extremity, changes in muscle force
output and activation have been demonstrated in the hip extensors
(Yerys et al., 2002), hamstrings (Cibulka et al., 1986), quadriceps
(Suter et al., 1999, 2000; Hillermann et al., 2006), soleus (Murphy
et al., 1995), and gastrocnemius (Dishman and Bulbulian, 2000,
2001; Dishman et al., 2002b, 2005; Dishman and Burke, 2003).
Joint mobilisation or manipulation is thought to stimulate sensory
receptors in and around the joint and affects the central nervous
system at the spinal segmental level (Suter et al., 1994; Murphy
et al., 1995; Herzog et al., 1999; Pickar, 2002; Colloca et al., 2003,
2004; Sung et al., 2004) as well as the cortical level (Dishman et al.,
2002a). The associated neurophysiological effect may be dependent
on the forces (high vs. low grade joint mobilisations) applied during
the manual intervention (Dishman et al., 2002a, 2005).
Changes in muscle activation have been demonstrated in
symptomatic (Suter et al., 1999, 2000) and healthy individuals
* Corresponding author. University of Virginia, 290 Massie Road, McCue Center,
PO Box 400834, Charlottesville, VA 22903, USA. Tel.: þ1 434 823 5031/þ1 434 243
2419; fax: þ1 434 243 2430.
E-mail address: tlg6q@virginia.edu (T.L. Grindstaff).
(Murphy et al., 1995; Dishman and Bulbulian, 2000, 2001; Dishman
et al., 2002b; Dishman and Burke, 2003). A single lumbopelvic joint
manipulation has been shown to acutely increase quadriceps force
output (Suter et al., 1999, 2000; Hillermann et al., 2006) and
quadriceps activation (Suter et al., 1999, 2000) in individuals with
anterior knee pain. Unfortunately these studies are limited by not
examining the underlying physiological mechanisms for changes in
strength and function (Hillermann et al., 2006; Iverson et al., 2008)
or the duration of effects (Suter et al., 1999, 2000). It is also
unknown whether lower grade joint mobilisations would have
a similar effect.
Studying the effects of joint mobilisation and manipulation on
asymptomatic individuals may provide additional insight into the
neurophysiological muscle response of the intervention without
the confounding, uncontrolled effects of altered muscle activation
related to injury. Further understanding the neurophysiological
response and duration of altered muscle activation of the quadri-
ceps following manual intervention will help guide future studies
and begin to provide scientific rational for treatment selections.
Since previous studies (Suter et al., 1999, 2000) have only examined
immediate changes in quadriceps force output and activation
further investigation is necessary to determine if changes would be
maintained over a 60 min period of time. Therefore, the purpose of
this study was to determine the amount and duration of altered
quadriceps force output and activation following a single high or

1356-689X/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2008.06.005
416 T.L. Grindstaff et al. / Manual Therapy 14 (2009) 415–420

low grade joint mobilisation/manipulation applied at the lumbo-
pelvic region in healthy individuals over the course of 1 h.
2. Methods
2.1. Design
A randomised controlled trial with one between factor, treat-
ment group (lumbopelvic joint manipulation, passive lumbar range
of motion, and prone extension) and one within factor, time (pre/
post 0, 20, 40, 60 min) was used to examine the effects of high and
low grade joint mobilisation/manipulation on quadriceps force
output and activation in this clinic-based study. Main outcome
variables included quadriceps force output and percentage quad-
riceps activation.
2.2. Participants
Forty-two healthy subjects volunteered for this study (Table 1).
Subjects self-reported they had pain free lumbar spine and lower
extremities for the past six months. Exclusion criteria included
signs/symptoms indicating nerve root compression, previous spine
or lower extremity surgery, osteoporosis, pregnancy, and spinal or
neurological disorders. A brief health history form was completed
by each subject and a standard musculoskeletal evaluation was
performed and included assessment of the lumbar spine, sacroiliac,
and knee joints to screen for exclusionary criteria. All subjects
signed a consent form prior to participation and the study was
approved by our Institutional Review Board.
2.3. Instrumentation
2.3.1. Quadriceps force output
Isometric quadriceps force was measured using a load cell
(Model 41, Range 1–1000 lbs; Sensotec, Columbus, OH) interfaced
with a data acquisition system (MP150; Biopac Systems, Inc.,
Goleta, CA) and amplifier (DA100B; Biopac Systems Inc.), and
sampled at 125 Hz. Subjects were seated in a custom-made chair
with their hips flexed at 85 , knees flexed at 90 , and arms folded
across their chest The pelvis was secured to the chair using Velcro
straps, while a padded ankle strap was placed 3 cm proximal to the
lateral malleolus and connected to the load cell via an ‘‘S’’ hook.
2.3.2. Burst-superimposition technique
Quadriceps activation was estimated by utilising the burst-
superimposition technique on a maximum voluntary isometric
contraction (MVIC). The burst-superimposition technique provides
the muscle with a percutaneous supramaximal stimulus to recruit
any remaining muscle fibres which have not been stimulated
(Rutherford et al., 1986; Snyder-Mackler et al., 1994; Stevens et al.,
2001). A superimposed burst (100 pulses/s, 600 ms pulse duration,
10 pulse tetanic train, 125 V, 100 ms duration) was manually
applied to the quadriceps approximately 2 s after the beginning of
the MVIC when the experimenter determined a plateau in force had
occurred. Amount of muscle activation was quantified using the
Table 1
Subject demographics.
central activation ratio (CAR) and calculated by dividing the voli-
tional MVIC force by total force (combined effect of the electrical
superimposed burst stimulation upon the MVIC, Eq. (1)) (Kent-
Braun and Le Blanc, 1996). A CAR of 1.00 represents complete
quadriceps activation (Stackhouse et al., 2000, 2001; Mizner et al.,
2003; Stevens et al., 2003; Fitzgerald et al., 2004; Lewek et al.,
2004).
Fvolitional
CAR ¼ (1)
Fvolitionalþelectrical
An S88 Grass Stimulator (Astro-Med, West Warwick, RI) was
used with the SIU8T isolation unit (125 V stimulus) and two
rubber–carbon electrodes (8  14 cm) to deliver the electrical
stimuli over quadriceps. Electrode surfaces were covered with
conductive gel and secured with an elastic bandage over the
proximal lateral aspect and the distal medial aspect of the quadri-
ceps muscle. The burst-superimposition technique has been shown
to be highly reliable with repeated testing of healthy subjects
(ICC ¼ 0.98) (Snyder-Mackler et al., 1993).
2.4. Study protocol
After initial evaluation, all participants had baseline testing of
quadriceps strength and quadriceps activation. Test leg was
randomly determined by coin toss and all interventions and tests
were performed on the same side. Participants performed a stand-
ardised warm-up consisting of four submaximal isometric
contractions (50–75% MVIC) with submaximal electrical stimula-
tion of the quadriceps and one MVIC with submaximal electrical
stimulation to orient them to the test procedures. Participants were
instructed to slowly build up force and hold an MVIC for 3–5 s.
Verbal encouragement and visual feedback of real time force
output were given. A superimposed burst (100 pulses/s, 600 ms
pulse duration, 10 pulse tetanic train, 125 V, 100 ms duration) was
manually applied to the quadriceps approximately 2 s after the
beginning of the MVIC when the experimenter determined
a plateau in force had occurred. If force did not plateau, a stimulus
was not applied. A 90 s rest period was given between trials.
Participants performed three trials with superimposed burst, with
the average MVIC and CAR values used for data analysis.
Following baseline testing, participants were randomised to one
of three treatment interventions: lumbopelvic joint manipulation,
side-lying lumbar mid-range flexion/extension PROM for 1 min, or
lying prone (Prone Ext) on elbows for 3 min. The total duration to
perform each of the three interventions was estimated at 3 min and
accounted for subject positioning and intervention. Lumbopelvic
joint manipulation was selected as a high grade mobilisation, while
lumbar PROM was selected as a lower grade joint mobilisation. The
prone on elbows intervention was selected as a sham treatment to
reduce potential participant bias. Quadriceps strength and quad-
riceps activation were tested immediately following intervention
(post 0), and at 20, 40, and 60-min post-intervention time intervals,
using the same methods described above. Sixty minutes was
chosen to coincide with a 60 min rehabilitation session based on
common clinical practice. During rest periods between testing
intervals, participants were asked to remain seated. Testing
concluded after 60-min post-intervention data were collected.

Manipulation (n ¼ 15) PROM (n ¼ 13) Prone extension (n ¼ 13)

2.4.1. Lumbopelvic joint manipulation
The lumbopelvic joint manipulation (Flynn et al., 2006) was
Age 24.6 (6.2) 28.6 (8.2) 27.0 (5.9)
Height (cm) 168.4 (8.4) 170.2 (7.0) 168.0 (10.4) performed on the ipsilateral side of the test limb (Fig. 1). The term
Mass (kg) 69.1 (16.1) 68.7 (8.1) 70.7 (14.9) lumbopelvic was used to describe the targeted region since this
Force (N) 495.1 (122.1) 431.5 (105.7) 450.9 (113.9) manipulation technique is not exclusively specific to the lumbar,
CAR (%) 83.4 (9.9) 76.2 (12.3) 75.6 (11.9) sacroiliac, or pelvic regions (Flynn et al., 2006). The manipulation
Values are mean (SD). procedure utilised in this study was consistent with previously
 T.L. Grindstaff et al. / Manual Therapy 14 (2009) 415–420 417

Fig. 2. Passive range of motion.

2.5. Statistical analyses

Subject demographics and baseline values for MVIC and CAR

were compared using a one-way ANOVA. Two separate single factor
repeated measures ANOVAs were performed to compare MVIC and
CAR percent change scores from baseline between groups
(manipulation, PROM, and Prone Ext) across each time period. A
secondary analysis consisting of two post-hoc one-way ANOVAs
was performed to analyse the percent change from baseline for
quadriceps MVIC force and CAR values immediately following
intervention. This analysis was performed to assess immediate
effects of the intervention, allowing direct comparisons to similar
studies. The level of statistical significance was set a priori at
p < 0.05. Statistical analyses were performed with SPSS Version
14.0 (SPSS Inc., Chicago, IL).
Fig. 1. Lumbopelvic joint manipulation in supine with side bending (a) and rotation (b).

3. Results
used methods (Flynn et al., 2002; Fritz et al., 2004; Iverson et al.,
2008) and was performed by one of two physical therapists There were no significant differences (p > 0.05) between any of
(initials, initials) with advanced manual therapy training. Subjects the subject group demographics or baseline MVIC or CAR values
were positioned supine on a treatment table, while the experi- (Table 1). Lumbopelvic joint cavitation was achieved in 86.7% of the
menter stood on the opposite side to be manipulated. The partici- individuals (54% with one attempt, 46% requiring 2–3 attempts).
pant was passively side-bent towards and rotated away from the Only two of the subjects in the manipulation group were unable to
selected lumbopelvic joint which was followed by the delivery of achieve joint cavitation after four attempts (two per side), but were
a posterior/inferior force through the opposite anterior superior retained in the statistical analysis, since cavitation may not be
iliac spine (ASIS). If a cavitation was not heard or felt by the subject
or examiner, the technique was repeated. If the second attempt was
not successful the procedure was repeated on the contralateral side
using similar methods (Flynn et al., 2002; Fritz et al., 2004; Iverson
et al., 2008). If cavitation was not heard or felt by the participant or
examiner following the fourth attempt, the participant proceeded
with the assessment of quadriceps activation as usual.

2.4.2. PROM
Subjects were positioned side-lying on the opposite side of the
test limb (Fig. 2). The experimenter held both knees with one arm
while placing their opposite hand on the participant’s lumbar
spine. The experimenter performed 1 min of flexion and extension
PROM without reaching physiological end range in either direction
of movement.

2.4.3. Prone extension on elbows

Subjects were positioned prone with lumbar spine extension
(Fig. 3) while using their elbows for support to maintain the posi-
tion for 3 min. Fig. 3. Prone extension on elbows.
418 T.L. Grindstaff et al. / Manual Therapy 14 (2009) 415–420
necessary to achieve clinically relevant changes (Flynn et al., 2003,
2006). For quadriceps MVIC force (Fig. 4) there was not a significant
time by group interaction (F8,152 ¼ 1.41, p ¼ 0.20) or a significant
difference between groups (F2,38 ¼ 2.55, p ¼ 0.09). When all
subjects were examined independent of group assignment there
was a significant difference across time intervals (F4,152 ¼ 18.45,
p < 0.001) with a decrease (p < 0.01) in MVIC force from baseline at
all time (0, 20, 40, 60 min) intervals following intervention. For
quadriceps CAR (Fig. 5) there was not a significant time by group
interaction (F8,152 ¼ 1.02, p ¼ 0.43) or significant differences in time
(F4,152 ¼ 1.08, p ¼ 0.37) or between groups (F2,38 ¼ 1.12, p ¼ 0.34).
To allow for comparison with previous studies (Suter et al., 1999,
2000; Hillermann et al., 2006) two post-hoc one-way ANOVAs
were performed to analyse the percent change from baseline for
quadriceps MVIC force and CAR values immediately following
intervention. There was a significant difference between groups for
MVIC (F2,38 ¼ 6.93, p ¼ 0.003) and CAR (F2,38 ¼ 3.98, p ¼ 0.03). The
manipulation group demonstrated a significant increase in quad-
riceps force output (3.1%) compared to the PROM group (p ¼ 0.001,
95% CI ¼ 5.52, 19.44) and the Prone Ext group (p ¼ 0.02, 95%
CI ¼ 1.36, 15.28). The manipulation group also significantly
increased quadriceps activation (4.7%) compared to the PROM
group (p ¼ 0.04, 95% CI ¼ 0.37, 9.92) and Prone Ext group (p ¼ 0.01,
95% CI ¼ 1.34, 10.90). Effect size for immediate changes in MVIC
force (d ¼ 0.12) and CAR (d ¼ 0.38) following joint manipulation
was also calculated.
4. Discussion
The results of this study indicate that changes in quadriceps
force output and activation are not present over the course of 1 h
following high or low grade joint mobilisation/manipulation
directed at the lumbopelvic region. The original data analysis
suggested an immediate change in quadriceps force output and
activation was not present following lumbopelvic joint manipu-
lation and contrasted findings of similar studies (Suter et al., 1999,
2000; Hillermann et al., 2006). The secondary analysis was con-
ducted to only examine immediate changes following intervention
and allowed for direct comparisons with previous findings. This
analysis indicated following lumbopelvic joint manipulation an
acute increase in quadriceps force output (3.1%) and quadriceps
activation (4.7%) was present. Although changes in quadriceps
force output were less than previously reported values (11–17%)
(Suter et al., 1999, 2000; Hillermann et al., 2006), changes in
quadriceps activation (5–7.5%) were consistent with previously
reported values (Suter et al., 1999, 2000). It appears with the
10
Manipulation
* a similar nerve root level.
5 PROM
Prone Ext
0
Percent Change
-5
-10
-15
-20
-25
Baseline Post 0 Post 20 Post 40 Post 60
Fig. 4. Quadriceps MVIC force. Values are expressed as percent change from baseline
and standard error of the mean. *Significant from baseline p  0.05.
10
Manipulation
PROM
* Prone Ext
Percent Change
0
-5
-10
Baseline Post 0 Post 20 Post 40 Post 60
Fig. 5. Quadriceps activation CAR. Values are expressed as percent change from
baseline and standard error of the mean. *Significant from baseline p  0.05.
multifactorial design originally used in this study that an imme-
diate increase in quadriceps force output and activation may have
gone unrecognised. Thus we cannot discount the immediate
findings which are in agreement with previous studies. Exami-
nation of effect sizes for the manipulation group demonstrates
a small effect size (d ¼ 0.12) for immediate changes in quadriceps
force output and a small, but approaching moderate (d ¼ 0.38)
effect size for quadriceps activation. Due to the extremely short
term effect following lumbopelvic joint manipulation the clinical
relevance of these findings is questionable and interpretation
should be left to the reader.
The immediate increase in quadriceps force output and activa-
tion following lumbopelvic joint manipulation could be attributed
to a facilitation of the motoneuron pool mediated at the spinal or
cortical level. We hypothesise the underlying physiological mech-
anism for the distant response associated with lumbopelvic joint
manipulation may be due to common sensory and motor nerve root
levels with the same interneurons. Joint manipulation is thought to
affect the central nervous system at the segmental level by
activating structures in and around the manipulated joint (mech-
anoreceptors, proprioceptors, and free nerve endings) (Suter et al.,
1994; Murphy et al., 1995; Herzog et al., 1999; Pickar, 2002; Colloca
et al., 2003, 2004; Sung et al., 2004). Cortical changes have also
been demonstrated following spinal manipulation (Dishman et al.,
2002a) and may also subsequently affect motoneuron pool excit-
ability. Since the sacroiliac joint (L2–S3), quadriceps (L2–4) and
knee joints (L2–S2) share common nerve root levels (Moore and
Dalley, 1999) it is possible that afferent information from one
structure may alter efferent signals to all structures innervated by
Lumbopelvic joint manipulation has been shown to briefly
decrease H-reflexes of the soleus (Murphy et al., 1995) and
gastrocnemius (Dishman and Bulbulian, 2000, 2001; Dishman
et al., 2002b, 2005; Dishman and Burke, 2003) muscles and
increase quadriceps force output (Suter et al., 1999, 2000; Hill-
ermann et al., 2006) and activation (Suter et al., 1999, 2000). This
relationship has been demonstrated in reverse using a knee joint
effusion model, where quadriceps inhibition and soleus facilitation
were demonstrated using H-reflex measures (Hopkins et al., 2001).
It is proposed that the increase in afferent information due to joint
manipulation is mediated at the interneuron and can affect efferent
motor output to the surrounding musculature. The clinical impli-
cation of this study is in agreement that lumbopelvic joint
manipulation has the ability to immediately increase quadriceps
force output and activation, but the effects in a healthy population
 T.L. Grindstaff et al. / Manual Therapy 14 (2009) 415–420
are of limited duration and small, but approaching a moderate
effect size (d ¼ 0.38) for changes in quadriceps activation.
A limitation of this study is only healthy individuals without
joint pathology were studied. It is possible since participants
were free of joint pathology that their motoneuron pool avail-
ability could not be altered beyond the acute response observed
in this study. An explanation for the differences in magnitude of
quadriceps activation between this study (4.7%) and previous
studies (Suter et al., 1999, 2000) demonstrating that a 5–7.5%
increase in quadriceps activation occurs may be due to the fact
that facilitation of the quadriceps may not occur as easily as
disinhibition. Individuals with knee joint pathology typically have
some level of quadriceps inhibition (Stratford, 1982; Snyder-
Mackler et al., 1994; Maitland et al., 1999; Suter et al., 1999, 2000;
Urbach et al., 1999, 2001; Hopkins et al., 2001; Palmieri et al.,
2003, 2004; Williams et al., 2003; Chmielewski et al., 2004)
which may allow for greater changes in quadriceps activation to
occur following intervention. Participants in this study did have
quadriceps activation levels which were below values previously
published literature on healthy individuals (Stackhouse et al.,
2001; Lewek et al., 2004; Hart et al., 2006a,b). CAR values greater
than or equal to 0.95 have been used to describe a situation
where all motoneurons have been activated during an MVIC
(Stackhouse et al., 2001; Lewek et al., 2004). Approximately 80%
of the individuals in this study could not achieve quadriceps
activation levels above 90%. Previous studies (Stackhouse et al.,
2001; Lewek et al., 2004) have estimated that 25% of younger to
middle aged adults are not able to achieve full activation.
Procedures used in this study including warm-up, verbal
encouragement, visual feedback, and rest periods between trials
were similar to other studies (Manal and Snyder-Mackler, 2000;
Stackhouse et al., 2001; Lewek et al., 2002, 2004; Mizner et al.,
2003, 2005; Stevens et al., 2003; Chmielewski et al., 2004;
Williams et al., 2005; Hart et al., 2006a,b,c). Although the CAR
values in this study were lower, measurements in the sham
group were extremely stable (ICC3,k ¼ 0.97, 95% CI: 0.93–0.99;
SEM ¼ 2.06%) over the course of an hour indicating stability in
our measurement technique. Even if the sham intervention had
a therapeutic effect, at best, this value would be underestimated
and likely represents normal variability within each subject over
the 60 min testing period.
Results also indicated decreased quadriceps force output
occurred over the course of 1 h for all groups. Obtaining valid and
reliable CAR values is dependent on participants giving a maximal
effort (Behm et al., 1996). Subjects were verbally encouraged during
all trials to give 100% effort, but deceased force output occurred
over the course of 1 h. This may have been due local muscle fatigue
due to performing 15 MVICs augmented with a supramaximal
electrical stimulus. The decrease in quadriceps force output could
not be attributed to changes in CAR, but were more likely due to
local muscle fatigue. Future studies should utilise electromyo-
graphic analysis of muscle median frequency to quantify local
muscle fatigue associated with repeated MVICs (Hart et al.,
2006a,b).
5. Conclusion
The findings of this study indicate that there was an acute
increase in quadriceps force output and quadriceps activation
following lumbopelvic joint manipulation in healthy individuals,
but these effects diminished within 20 min of intervention. All
groups demonstrated a progressive loss of quadriceps force output
over the course of testing, which was thought to be due to muscle
fatigue. Additional research is necessary to accurately determine
duration of changes in quadriceps force output and activation
419
following lumbopelvic joint manipulation in healthy and symp-
tomatic individuals.
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