Clinical Biomechanics 34 (2016) 45–52

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Clinical Biomechanics

journal homepage: www.elsevier.com/locate/clinbiomech

Does experimental low back pain change posteroanterior lumbar spinal

stiffness and trunk muscle activity? A randomized crossover study
Arnold Y.L. Wong a,⁎, Eric C. Parent a, Narasimha Prasad a,b, Christopher Huang c,
K. Ming Chan c, Gregory N. Kawchuk a
a
Department of Physical Therapy, University of Alberta, Edmonton, Alberta, Canada
b
Department of Mathematical and Statistical Sciences, University of Alberta Hospital, Edmonton, Alberta, Canada
c
Division of Physical Medicine and Rehabilitation, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada

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

Article history: Background: While some patients with low back pain demonstrate increased spinal stiffness that decreases as
Received 9 January 2016 pain subsides, this observation is inconsistent. Currently, the relation between spinal stiffness and low back
Accepted 18 March 2016 pain remains unclear. This study aimed to investigate the effects of experimental low back pain on temporal
changes in posteroanterior spinal stiffness and concurrent trunk muscle activity.
Keywords: Method: In separate sessions five days apart, nine asymptomatic participants received equal volume injections of
Experimental pain
hypertonic or isotonic saline in random order into the L3–L5 interspinous ligaments. Pain intensity, spinal stiff-
Electromyography
Spinal stiffness
ness (global and terminal stiffness) at the L3 level, and the surface electromyographic activity of six trunk mus-
Saline cles were measured before, immediately after, and 25-minute after injections. These outcome measures under
Low back pain different saline conditions were compared by generalized estimating equations.
Findings: Compared to isotonic saline injections, hypertonic saline injections evoked significantly higher pain in-
tensity (mean difference: 5.7/10), higher global (mean difference: 0.73 N/mm) and terminal stiffness (mean dif-
ference: 0.58 N/mm), and increased activity of four trunk muscles during indentation (P b 0.05). Both spinal
stiffness and trunk muscle activity returned to baseline levels as pain subsided.
Interpretation: While previous clinical research reported inconsistent findings regarding the association between
spinal stiffness and low back pain, our study revealed that experimental pain caused temporary increases in spi-
nal stiffness and concurrent trunk muscle co-contraction during indentation, which helps explain the temporal
relation between spinal stiffness and low back pain observed in some clinical studies. Our results substantiate
the role of spinal stiffness assessments in monitoring back pain progression.
© 2016 Elsevier Ltd. All rights reserved.

1. Introduction spinal manipulation (Flynn et al., 2002). Similarly, immediate reduction

in spinal stiffness following spinal manipulation may be related to fa-
Low back pain (LBP) is the most common and debilitating musculo- vorable treatment outcomes (Wong et al., 2015).
skeletal disorder in the world (Vos et al., 2012). Given the heteroge- Despite recent interests in spinal stiffness assessments, no consensus
neous cause of LBP (Brennan et al., 2006), clinicians attempt to use has been reached regarding the relation between spinal stiffness and
various strategies to classify patients into different subgroups to guide LBP. Some clinical studies using manual/mechanical assessments
treatment selection. Posteroanterior spinal stiffness assessment is used found that people with LBP demonstrated higher lumbar stiffness than
as an objective measure to evaluate the mechanical responses of the asymptomatic controls, and some patients' spinal stiffness decreased
spine to external forces (Abbott et al., 2009). During this examination, significantly during LBP remission (Brodeur and DelRe, 1999; Ferreira
a manual/mechanical posteroanterior force is applied over the spinal et al., 2009; Latimer et al., 1996). Conversely, other studies using similar
processes of a prone patient while the corresponding spinal stiffness/ lumbar stiffness assessments revealed no relation between spinal stiff-
movement is either perceived by the clinician or measured by a me- ness and LBP (Owens et al., 2007; Wong et al., 2013).
chanical device (Maitland et al., 2005; Owens et al., 2007). The presence While these mixed results may be partly attributed to different stiff-
of hypomobile lumbar segment(s) is one of five clinical characteristics ness measurement methods, it is plausible that some, but not all,
in a clinical prediction rule for identifying likely responders to successful patients with LBP display pain-related hyperactivity of trunk muscles
that increases spinal stiffness (Hu et al., 2009; Shirley et al., 1999).
⁎ Corresponding author at: Department of Rehabilitation Sciences, Hong Kong
Shirley and Lee found that some patients with LBP, as compared to
Polytechnic University, Hong Kong, China. their asymptomatic counterparts, displayed higher spinal stiffness and
E-mail address: [email protected] (A.Y.L. Wong). concurrent bilateral erector spinae (ES) activity during mechanical

http://dx.doi.org/10.1016/j.clinbiomech.2016.03.006
0268-0033/© 2016 Elsevier Ltd. All rights reserved.
46 A.Y.L. Wong et al. / Clinical Biomechanics 34 (2016) 45–52

spinal stiffness tests (Shirley and Lee, 1993). They also found that a 10% Table 1
maximum voluntary contraction of ES in asymptomatic individuals Placement of surface electromyography electrodes and measurement of maximum volun-
tary isometric contraction of trunk muscles.
yielded an average increase in spinal stiffness of 11.8% (Shirley et al.,
1999). Unfortunately, these cross-sectional studies did not examine Muscle/ground Placement of electrodes Maximum voluntary
the interrelation among LBP, spinal stiffness and trunk muscle co- electrode isometric contraction
measurement
contraction, which may help refine the existing clinical prediction
rules (Flynn et al., 2002) or guidelines for LBP interventions. Obliquus externus Approximately 15 cm It was tested in supine with
lateral to the umbilicusbent knees and shoulder in
Because it is difficult to quantify the temporal associations among the
90° flexion and full elbow
aforementioned parameters in a heterogeneous clinical population, these extension (Hodges et al.,
relations are best investigated by an experimental pain model. Numerous 2013). Manual resistance
studies have used experimental pain models to explore the sensory and was applied at the bent
motor response of LBP (Hodges et al., 2003; Tsao et al., 2011). These knees and the arms to resist
right or left trunk rotation.
models allow the control of intensity and duration of pain in individuals Obliquus 2 cm medial and inferior to A maximal expiratory
(Dickx et al., 2010). They also enable the investigations of causal effects internus/transversus the anterior superior iliac maneuver with abdominal
of nociception on the changes of physical parameters. abdominis spine (Marshall and hollowing was performed in
For these reasons, the primary objective of the current study was to Murphy, 2003) a sit-up position (Imai et al.,
2010).
elucidate the effect of experimentally-induced pain on the temporal
Erector spinae 3 cm lateral to the L3 Performing prone extension
changes of spinal stiffness and simultaneous trunk muscle activity dur- spinous process (Kavcic against resistance applied to
ing spinal indentation. The secondary objective of the present study was et al., 2004) the upper trunk in a PA
to examine the correlation among pain intensity, spinal stiffness and direction while the arms
trunk muscle activity. We hypothesized that experimental pain would were placed beside the
body and legs were tied to
transiently increase spinal stiffness and involuntary activity of some
the plinth by a strap (Imai
trunk muscles during indentation, which would return to baseline et al., 2010).
levels during pain remission. We also hypothesized that pain intensity, Ground electrode The left acromion –
and percent changes in spinal stiffness and trunk muscle activity were
closely related to one another.
change the mechanical properties of passive tissues and result in altered
2. Methods spinal stiffness, isotonic saline was chosen to control for potential volu-
metric effects. The saline concentration injected at the first session was
2.1. Participants randomly assigned. Participants were reminded not to perform voli-
tional trunk muscle contraction during the spinal stiffness tests.
Asymptomatic volunteers (age 18–60 years) without history of During the second session, the participants underwent the same
back/pelvic pain in the last 12 months were recruited by posters at procedures but with the previously unused saline concentration. A 5-
the University of Alberta. Exclusion criteria were: major orthopedic, day washout period was chosen to mitigate any carryover effects of
neurological or cardiorespiratory diseases, history of any back or ab- previous injections. To reduce participant bias toward the anticipation
dominal surgery, malignancy, or potential/confirmed pregnancy. Writ- of saline concentrations, participants were told that they would receive
ten informed consent was obtained from participants. This study was injections of two distinct saline concentrations that might elicit different
approved by the institutional Research Ethics Board and registered pain intensities. At the end of the second session, the order of saline
with ClinicalTrials.gov (NCT01761838). injections was revealed to each participant.

2.2. Study design 2.3. Self-reported measures

This study employed a randomized crossover design. Participants On the first session, participants completed the fear of pain
attended 2 sessions at the same time of day at least 5 days apart in a re- questionnaire—III (FOP-III) (McNeil and Rainwater, 1998), which evaluat-
habilitation clinic. During the first session, participants completed a bat- ed participants' fear toward various pain provoking conditions (McNeil
tery of self-reported questionnaires and underwent a physical and Rainwater, 1998). Pain intensity was measured on an 11-point
examination. Surface electromyography (EMG) electrodes were at- numeric pain rating scale (NPRS) where 0 represents “no pain” and 10
tached to six trunk muscles (i.e. bilateral obliquus externus (OE), represents “worst pain imaginable” (Williamson and Hoggart, 2005).
obliquus internus/transversus abdominis (OI/TrA), and ES at the L3–4 Pain intensity was measured at baseline, at every 30 s after the injection
levels). Participants were instructed to perform maximum voluntary until the experimental pain completely subsided, and at 25 min after
isometric contraction (MVIC) of each trunk muscle against manual re- the injection. The location and size of the experimental pain were marked
sistance (Table 1) (Kavcic et al., 2004; Hodges et al., 2013; Marshall on a body pain diagram (Werneke et al., 1999).
and Murphy, 2003; Imai et al., 2010). The EMG signals during MVIC
were used for subsequent EMG normalization. The participant then 2.4. Spinal stiffness assessment
underwent standardized assessments at 3 time points: 1) before (base-
line), 2) immediately after, and 3) 25-min after saline injection (Fig. 1). Spinal stiffness was assessed using a mechanical indentation device
The 25-min follow-up duration was chosen because the present pain whose performance has been detailed elsewhere (Wong et al., 2015;
provocation method induced pain lasting approximately 14 min (Tsao Wong et al., 2013). Briefly, the device comprises of a motorized indenta-
et al., 2010a). The standardized assessments include three instrumented tion probe equipped with a load cell transducer and a rotary encoder.
spinal stiffness tests and concurrent trunk muscle EMG measurements Custom written LabVIEW software (National Instruments, Austin,
(Fig. 1). After the baseline standardized assessments, either 0.3 ml of USA) was used to control the loading speed (2.0 mm/s) of the probe
0.9% isotonic saline or 5% hypertonic saline was injected into the L3–4 and to collect force and displacement signals.
and the L4–5 interspinous ligaments (Tsao et al., 2011). Hypertonic The L3 spinous process of the prone participant was identified by
saline injection was used to induce pain, while isotonic saline injection ultrasonography. The indenter was then positioned above the L3 level.
was used to control for the volumetric effect of injection on spinal stiff- The participants held their breath at the end of normal exhalation dur-
ness. Because saline injections into the interspinous ligament might ing indentation at the L3 level (Wong et al., 2015; Wong et al., 2013). All
 A.Y.L. Wong et al. / Clinical Biomechanics 34 (2016) 45–52 47

Fig. 1. A flow diagram of the experiment.

indentation was performed with force applied vertically at the contact 2.6. MVIC of target muscles
site. Participants underwent several familiarization indentation trials
(Wong et al., 2013; Kawchuk and Fauvel, 2001). Three experimental Two trials of MVIC were performed for each target muscle (Table 1).
indentations were then performed with a preload of 5 N (to establish A 2-min rest was given between trials. The RMS EMG amplitude of each
a defined starting point for subsequent spinal stiffness calculation), muscle during the middle 2 s of the MVIC was calculated. The highest
and with a target load of 60 N at each time point. The resulting force amplitude of each muscle during MVIC trials was chosen for
and displacement data were used to calculate two types of spinal stiff- normalization.
ness (Fritz et al., 2011): 1) global/average stiffness (i.e. slope of the
force-displacement curve between 5 N and 60 N) (Fritz et al., 2011):
and 2) terminal/secant stiffness [i.e. (target load (60 N)–preload 2.7. Saline injection
(5 N))/(maximal displacement–displacement at the end of the
preload)] (Appendix 1) (Wong et al., 2013; Fritz et al., 2011). The 0.3 ml of 5% hypertonic saline or a 0.9% isotonic saline injection was
within- and between-day minimal detectable change of the current spi- given to all participants at the first session in random order. Hypertonic
nal stiffness measurement at 95% confidence interval were 0.3 N/mm saline was used to provoke pain while equal volume of isotonic saline
and 0.5 N/mm, respectively (Wong et al., 2013). was aimed to investigate the volumetric effect of the injected saline
on the measured spinal stiffness. An independent research assistant
used Microsoft Excel, 2011 (Microsoft, Redmond, USA) software to gen-
2.5. Surface EMG measurements erate the simple randomization code and concealed the codes in opaque
and sealed envelopes. A physician, who was blinded to the assessment
After skin preparation, disposable Ag-AgCl bipolar electrodes results, palpated the L3/4 and L4/5 interspinous spaces, sterilized the
(Bortec BiPole) with active diameter of 1 cm and inter-electrode dis-
tance of 2 cm were placed over bilateral OE, OI/TrA and ES muscles at Table 2
the L3 level to measure their EMG activity during indentation Demographic characteristics of the participants.
(Table 1). Raw EMG data were collected using the AMT-8 EMG system
Participants Age, Gender Body mass Fear of Pain-III
(Bortec biomedical, Calgary, Canada). The signal was amplified 1000 years index, kg/m2 Questionnaire
times with an input impedance of 10 MΩ and a common mode rejection scores, out of 150
ratio of 115 dB at 60 Hz, and sampled at 2400 Hz (Brereton and McGill, 1 21 F 19.5 95
1998). A custom written LabVIEW program was used to synchronize the 2 29 F 22.3 47
electronic signals from both the indentation device and the EMG 3 32 F 20.4 69
system. 4 22 M 23.7 76
5 25 M 27.3 64
Raw EMG data were band-pass filtered by a second order
6 34 F 24.1 76
Butterworth filter (10 Hz to 450 Hz) (Kavcic et al., 2004). Power line in- 7 21 F 21.2 70
terference (60 Hz and its harmonics) were removed by Notch filters 8 23 F 20.3 74
(Beck et al., 2009). An established 2-step algorithm was used to remove 9 22 M 23.2 67
10 (excluded) 25 F 20.6 54
the electrocardiographic signals (Nougarou et al., 2013).
11 (excluded) 24 F 28.1 90
To quantify the muscle activity during indentation, the root mean 12 (excluded) 25 F 21.1 76
square (RMS) EMG of each muscle during an indentation cycle was cal- Summary based on 25.4 33% 22.4 (2.4)a 70.9 (12.7)a
culated and then normalized to the respective RMS EMG during MVIC. included participants (2.4)a maleb
Normalized EMG signals of each muscle at each time point were aver- a
Average (standard deviation).
aged for the statistical analysis. b
Frequency.
48 A.Y.L. Wong et al. / Clinical Biomechanics 34 (2016) 45–52

Table 3
Pain and spinal stiffness values before, immediately after and 25-min after hypertonic and isotonic saline injections.

Conditions Hypertonic saline Isotonic saline

Pain duration NPRS during Global stiffness Terminal Pain duration NPRS during Global stiffness Terminal
(SD), minutes indentation (SE). out (SE). N/mm stiffness (SE). (SD), minutes indentation (SE). out (SE). N/mm stiffness (SE).
of 10 N/mm of 10 N/mm

Baseline NA 0.00 (0.00) 6.03 (1.25) 5.68 (1.09) NA 0.00 (0.00) 5.96 (1.16) 5.57 (1.05)
Post-injection 8.45 (3.21) 5.79 (1.37) 6.83 (1.16) 6.24 (1.10) 1.33 (1.18) 0.59 (0.64) 6.10 (0.99) 5.71 (1.00)
25-min after injection NA 0.00 (0.00) 6.11 (1.26) 5.67 (1.07) NA 0.00 (0.00) 6.11 (1.01) 5.63 (0.94)

NPRS, numeric pain rating scale.

site with an antiseptic, and then injected the assigned saline to the L3–4 pain (NPRS = 8/10) during indentation (Fig. 1). All participants' pain re-
and L4–5 interspinous ligaments. The needle (27G × 25 mm) of a solved completely after 10 min and no adverse effect was reported on or
syringe was inserted cephalically through the skin at approximately after the day of the experiment. Table 2 displays the demographic data
30° until the tip of the needle was felt touching the caudal side of the of the participants. Table 3 and Table 4 provide the descriptive analyses
upper spinous process (Tsao et al., 2011). The assigned saline was slow- of pain intensity, global stiffness, terminal stiffness, and EMG activity of
ly delivered over 10 s (Tsao et al., 2010b). Prior research revealed that all muscles at different time points. The mean duration of an indentation
injections of hypertonic saline into these ligaments would induce rela- cycle was 2.8 (0.3) seconds.
tively long-lasting acute central LBP, which was suitable for examining Since FOP-III score was not correlated with pain intensity following
the effects of pain on trunk muscle responses (Tsao et al., 2011; Tsao hypertonic (P = 0.88) or isotonic saline injection (P = 0.22), FOP-III
et al., 2010b). If the induced pain intensity on NPRS was less than 2/10 score was not adjusted for in the subsequent GEE analyses.
following the hypertonic saline injection, participants were excluded
from the study because a 2-point change in LBP intensity was consid- 3.1. Effects of saline concentrations on pain
ered as the minimal clinically meaningful change (Ostelo et al., 2008).
The GEE estimated that hypertonic and isotonic saline injection
2.8. Statistical analysis caused an average of 6.31 points and 0.63 points increase in pain inten-
sity on the NPRS, respectively (P b 0.01) (Fig. 2a) (Appendix 2). The pain
A research assistant coded all data to blind the investigator during intensity at the baseline and 25-min post-injection time point was zero
statistical analysis. All data were analyzed using SPSS version 22.0 for both concentrations. Hypertonic saline injection induced longer pain
(IBM Corp., Armonk, USA). Descriptive statistics of continuous and cat- duration than isotonic saline injection (Table 3; mean difference = 7.11
egorical variables are expressed as means and percentages, respectively. (3.57) min; t = − 5.98; P b 0.01).
The assumptions of all statistical tests were checked and confirmed. The
alpha value of all tests was set to 0.05. 3.2. Effects of saline concentrations on spinal stiffness
The effects of the two saline concentrations on pain intensity, global
stiffness, terminal stiffness, and EMG of each trunk muscle during in- There was no significant difference in the average baseline global or
dentation were analyzed by separate generalized estimating equation terminal stiffness at the L3 level on both experimental days. The esti-
(GEE) analyses using an exchangeable working correlation matrix and mated mean global stiffness immediately after hypertonic saline injec-
robust standard errors. The p values of the β coefficients were analyzed tions was significantly higher than that immediately after isotonic
by 2-tailed Wald tests. saline injections (mean difference: 0.72 N/mm, P b 0.05) (Fig. 2b)
The associations among pain intensity, FOP-III, and percent changes (Appendix 2). Global stiffness returned to the baseline level at the 25-
in spinal stiffness and trunk muscle activity were analyzed using Spear- min post-injection follow-up irrespective saline concentrations.
man correlation analysis. Similarly, the average terminal stiffness values significantly increased
immediately after injections of any of the two saline concentrations
3. Results (P b 0.05). However, the estimated terminal stiffness immediately
after hypertonic saline injection was significantly larger than that after
Of the 12 recruited participants, two were excluded because their isotonic saline injections (mean difference: 0.58 N/mm, P b 0.05)
NPRS scores were less than 2 following hypertonic saline injection. (Fig. 2c) (Appendix 2). Those elevated terminal stiffness values
One participant was excluded because of severe experimental-induced returned to the respective baseline values at 25 min after injections.

Table 4
Average surface electromyography values and (standard deviation) of different trunk muscles before, immediately after and 25-min after hypertonic and isotonic saline injections.

Conditions Resting EMG (%MVIC) Muscles EMG during indentation (%MVIC)

Left OE Right OE Left OI/TrA Right Left ES Right ES Left OE Right OE Left OI/TrA Right Left ES Right ES
OI/TrA OI/TrA

Hypertonic saline
Baseline 4.41 (1.72) 3.62 (1.86) 2.38 (1.04) 3.33 (1.94) 3.82 (2.41) 2.24 (1.43) 5.39 (3.47) 4.71 (2.53) 2.46 (1.12) 3.61 (2.18) 3.87 (2.51) 2.35 (1.42)
Post-injection 7.07 (3.74) 7.71 (7.15) 4.42 (5.38) 4.94 (4.80) 4.24 (2.97) 3.07 (1.62) 9.88 (5.84) 9.64 (8.03) 5.02 (6.99) 6.42 (7.12) 4.80 (3.31) 3.46 (1.68)
25-min after 4.78 (3.94) 4.12 (2.37) 2.43 (1.11) 3.41 (2.45) 3.86 (2.19) 2.45 (1.49) 5.23 (3.02) 4.70 (2.86) 2.54 (1.32) 3.76 (3.09) 3.88 (2.21) 2.50 (1.47)
injection

Isotonic saline
Baseline 4.42 (1.60) 3.94 (1.62) 3.50 (2.87) 3.15 (1.38) 4.27 (2.77) 2.47 (1.52) 4.98 (1.95) 5.46 (2.91) 3.64 (2.91) 3.46 (1.57) 4.34 (2.87) 2.70 (1.65)
Post-injection 5.29 (2.46) 4.28 (1.65) 3.88 (3.20) 3.69 (2.31) 4.46 (2.85) 2.61 (1.45) 5.56 (2.18) 5.06 (2.24) 3.99 (2.98) 3.70 (2.77) 4.49 (2.77) 2.82 (1.47)
25-min after 4.42 (1.51) 4.24 (1.82) 3.74 (2.85) 3.37 (1.80) 4.37 (2.73) 2.47 (1.44) 4.86 (1.76) 5.15 (2.82) 3.75 (3.01) 3.49 (1.94) 4.47 (2.78) 2.59 (1.54)
injection

EMG, electromyography; ES, erector spinae; MVIC, maximum voluntary isometric contraction OE, obliquus externus; OI, obliquus internus; TrA, transversus abdominis.
 A.Y.L. Wong et al. / Clinical Biomechanics 34 (2016) 45–52 49

3.3. Effects of saline concentrations on trunk muscle EMG values during the threat of injury, people may use individual-specific muscle acti-
indentation vation strategies (e.g. redistribution of activity within and between
muscles) to brace the spinal structure to attain spinal stability
There was no significant between-day difference in baseline EMG (Hodges and Tucker, 2011). Interestingly, our participants involun-
activity of the six muscles. Compared to isotonic saline injection, hyper- tarily co-contracted their OE, OI/TrA and ES at approximately 4–
tonic saline injection elicited significantly higher EMG activity of bilater- 10% MVIC in response to pain. This observation is in agreement
al OE, right OI/TrA and right ES during indentation (mean differences
ranged from 0.73% to 5.03% MVIC, P b 0.05) (Fig. 3) (Appendix 2).
Similar trend was observed for left ES (mean differences: 0.90% MVIC,
P = 0.051) (Fig. 3) (Appendix 2). At the 25-min post-injection follow-
up, all trunk EMG values returned to the respective baseline values
regardless of saline concentrations.

3.4. Associations among pain, FOP-III, and percent changes in spinal

stiffness and muscle activity

Increased pain intensity was significantly associated with increased

spinal stiffness (ρ ranging from 0.50 to 0.56; P b 0.05) and increased ac-
tivity of all trunk muscles (ρ ranging from 0.50 to 0.70; P b 0.05) (Ap-
pendix 3). The percent changes in spinal stiffness were positively
correlated with percent changes in all abdominal muscle activity (ρ
ranging from 0.51 to 0.64; P b 0.05) but not with percent changes in bi-
lateral ES activity (ρ ranging from 0.19 to 0.34). The percent changes of
all abdominal muscle activity were positively correlated with one an-
other (ρ ranging from 0.81 to 0.94; P b 0.01). Likewise, bilateral ES activ-
ity demonstrated strong positive correlation with each other (ρ = 0.75;
P b 0.05) (Appendix 3). The FOP-III scores were not significantly related
to any of the outcome measures (ρ ranging from 0.14 to 0.43).

4. Discussion

The present results showed that hypertonic and isotonic saline injec-
tions induced differential responses in LBP, spinal stiffness and trunk
muscle activity. As hypothesized, the hypertonic saline evoked a signif-
icantly higher transient LBP intensity, spinal stiffness, and EMG activity
of some trunk muscles during indentation when compared to the
isotonic injection. These parameters returned to baseline levels at the
25-min post-injection follow-up. The significant positive correlation be-
tween pain intensity, and percent changes in spinal stiffness and trunk
muscle activity suggested that increases in pain intensity were associat-
ed with significant increases in spinal stiffness and trunk muscle activi-
ty. Our study provided the first empirical evidence to suggest that
clinically observed changes in spinal stiffness in people with LBP may
be mediated by altered trunk muscle activity (Brodeur and DelRe,
1999; Ferreira et al., 2009; Latimer et al., 1996).

4.1. Pain-induced spinal stiffness increment

Our study revealed that experimentally-induced LBP caused clinical-

ly significant spinal stiffness increases that exceeded the minimal de-
tectable change in spinal stiffness at a 95% confidence interval and
measurement errors (0.5 N/mm) (Wong et al., 2013).

4.2. Pain-induced trunk muscle responses

Although experimental pain induced increased activity of most

trunk muscles, no participant displayed identical trunk muscle re-
sponses. Specifically, pain induced by hypertonic saline injection
elicited significantly higher mean activity of bilateral OE, right OI/
TrA and right ES during indentation as compared to isotonic saline
injections. A similar trend was noted for left ES following hypertonic Fig. 2. Estimated marginal means and standard errors of the pain score on an 11-point
saline injection (P = 0.051). These observations imply that partici- numeric pain rating scale, and global and terminal stiffness at the L3 level. * A significant
pants elevated their trunk muscle activity in order to protect painful difference in the mean value of the variable of interest between the condition
immediately after isotonic saline injections and immediately after hypertonic saline
body parts (Hodges et al., 2013) despite relatively large variability in injections. # A significant change in the mean value of the variable of interest
inter-individual neuromuscular responses (data not shown). Since immediately after a particular saline injection as compared to the respective baseline
acute post-injection nociception may be perceived as actual LBP or value.
50 A.Y.L. Wong et al. / Clinical Biomechanics 34 (2016) 45–52

with prior research in which people with LBP reflexively co-contract 4.3. Temporal changes in pain, spinal stiffness and trunk muscle activity
trunk flexors and extensors in response to sudden trunk perturba- following injections
tions in a weight bearing position (Radebold et al., 2000). Our results
also corroborate the theory that people adopt individual-specific Our study revealed specific trunk responses to acute pain that have
trunk motor control strategies to redistribute the activity within not been defined in previous clinical studies — temporary increased
and between muscles in order to protect the spinal structure. spinal stiffness and concomitant trunk muscle co-contraction during in-
(Hodges and Tucker, 2011). dentation. It was previously thought that the heightened spinal stiffness

Fig. 3. Estimated marginal means and standard errors of electromyography (EMG) of bilateral obliquus externus (OE), obliquus internus (OI), and erector spinae (ES) at the L3 level. * EMG
activity of a given muscle immediately after hypertonic saline injection was significantly higher than that immediately after isotonic saline injections. # EMG activity of a given muscle
immediately after a particular saline injection was significantly different from the respective baseline value. ß EMG activity of a given muscle immediately after hypertonic injection
had a trend to be higher than that immediately after isotonic saline injection (P = 0.051).
 A.Y.L. Wong et al. / Clinical Biomechanics 34 (2016) 45–52 51

in patients with LBP was due to bilateral ES hyperactivity (Shirley et al., The LBP-related insignificant increases in left ES activity during
1999). Our GEE results showed that, instead of activating ES alone, indentation (P = 0.051) might be due to the type 2 error given our
experimental pain significantly elicited low level trunk muscle co- small sample size. In other words, LBP may induce co-contraction of
contraction. Because such co-contraction could generate high spinal sta- most trunk muscles.
bilization forces and intra-abdominal pressure (Lee et al., 2006; Like other experimental pain studies (Hodges et al., 2003; Tsao et al.,
Essendrop et al., 2002), mild trunk muscle co-contraction was sufficient 2011; Tsao et al., 2010b), the current study had a small sample size.
to cause the observed clinically significant spinal stiffness increases. Im- However, our randomized crossover design was employed to minimize
portantly, the restoration of spinal stiffness and trunk muscle activity at between-individual variability and to increase the statistical power by
the 25-min follow-up substantiated the close relation among LBP, spinal having participants to serve as their own control. Despite the small sam-
stiffness and trunk activity. ple size, our results revealed that pain had significant effects on spinal
Interestingly, while the correlation analysis showed that increased stiffness and multiple trunk muscle activity. Our significant findings
LBP intensity was significantly associated with both increased spinal indicated that the current study generally had sufficient statistical
stiffness and muscle activity of all trunk muscles, changes in spinal stiff- power.
ness values were not significantly correlated with changes in ES activity.
This observation implies that ES may play a relatively less important 4.7. Implications
role in affecting spinal stiffness. Alternatively, the small positive correla-
tion coefficients between changes in spinal stiffness and bilateral ES Our results highlight that heightened spinal stiffness in patients with
activity might be ascribed to the relative small changes (variations) in LBP may be due to pain-related reflexive trunk muscle co-contraction.
both spinal stiffness and ES activity, which could negatively impact Instead of solely providing spinal mobilization to such cases, treatments
the resulting correlation coefficient (Portney and Watkins, 2009). How- should consider pain reduction and/or trunk muscle relaxation to nor-
ever, since GEE and Spearman correlation analysis both showed close malize elevated spinal stiffness, which may cause functional limitation.
associations among pain, spinal stiffness and trunk muscle activity, the Additionally, since multiple factors (e.g. hypermobility or spinal de-
temporary pain-related changes in spinal stiffness was likely attribut- generation) may affect the associations among LBP, spinal stiffness, and
able to trunk muscle co-contraction. trunk muscle activity in clinical populations, future studies should cate-
gorize different combinations of spinal biomechanical characteristics in
4.4. Reasons for not finding the causal relation between pain and spinal patients with LBP, investigate the underlying causes of these combina-
stiffness previously tions, and determine specific treatment strategies for each category of
patients.
Previous clinical studies reported inconsistent relation between LBP
and spinal stiffness for several reasons. First, a heterogeneous clinical 5. Conclusions
population might result in diverse lumbar stiffness responses during
LBP remission. Second, since previous clinical trials did not measure The current study provides the first empirical evidence to quantify
trunk muscle activity of patients remitted from LBP (Owens et al., the influences of LBP on spinal stiffness and concurrent trunk muscle ac-
2007; Ferreira et al., 2009), it remains unclear whether patients in re- tivity during indentation. Our results provide an explanation for the
mission of LBP would demonstrate persistent maladaptive motor strat- temporal association between changes in spinal stiffness and LBP ob-
egies that might affect the measured spinal stiffness (Butler et al., 2013). served in some clinical studies. They also support the current applica-
Third, some patients might have irreversible spinal structure changes tion of spinal stiffness and muscle activity assessments to objectively
(e.g. facet joint degeneration) that would not alter after LBP remission. monitor LBP progression.
Fourth, the suboptimal reliability of previous spinal stiffness assess-
ments might weaken their ability to accurately detect temporal changes Acknowledgments
in spinal stiffness. (ICC2,1 ranged between 0.78 and 0.79 (Owens et al.,
2007; Ferreira et al., 2009) as compared to 0.98 for our spinal stiffness The authors gratefully thank Carolyn Berendt for recoding the data
assessment (Wong et al., 2013). files for our data analysis, and Francois Nougarou, PhD for writing cus-
tomized MATLAB program for electromyography analysis. The authors
are very grateful to the River Valley Health Clinic for providing clinical
4.5. Strengths of the present study
space. Arnold Wong was supported by the Alberta Innovates-Health
Solutions Graduate Studentship and the Andrew Stewart Memorial
Our study has several strengths. First, isotonic saline was used to
Graduate Prize. Greg Kawchuk was supported by the Canada Research
control for the psychological anticipation of pain provocation that may
Chair Program.
elicit involuntary trunk muscle activation (Moseley et al., 2004) and in-
creases spinal stiffness. Second, interspinous ligament injection was
Appendices. Supplementary data
chosen because it provoked temporary LBP comparable to clinical pain
without directly injecting the muscle of interest (Tsao et al., 2011;
Supplementary data to this article can be found online at http://dx.
Tsao et al., 2010a). Third, EMG measurements of multiple trunk muscles
doi.org/10.1016/j.clinbiomech.2016.03.006.
gave a better overview on the temporal effects of pain on multiple trunk
muscle responses.
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