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SPINE Volume 32, Number 1, pp E23–E29

©2007, Lippincott Williams & Wilkins, Inc.

Superficial Lumbopelvic Muscle Overactivity and


Decreased Cocontraction After 8 Weeks of Bed Rest

Daniel L. Belavý, BPhty,*† Carolyn A. Richardson, PhD,† Stephen J. Wilson, PhD,*


Jörn Rittweger, PhD,‡ and Dieter Felsenberg, PhD§

It is not new to suggest that sedentary western lifestyle


Study Design. Longitudinal study. could be involved in lumbopelvic (LP) pain etiology.1
Objective. To gain insight into the effects of inactivity Dysfunction in the central nervous system (CNS) control
on lumbopelvic stabilization.
of the LP musculature for stabilization is considered to
Summary of Background Data. Some authors have
suggested a link between inactivity and lumbopelvic (LP) be one risk factor for LP pain.2 Inactivity itself results in
pain. Studies examining the superficial musculature in LP a number of changes in multiple body systems,3 but its
pain have shown overactivity and increased cocontrac- association to change in LP motor control for stabiliza-
tion. Studies in inactivity (bed rest, microgravity) have tion and any potential link to LP pain etiology is poorly
shown similar effects on the musculature of the legs. Here
understood.
we examine the effect of bed rest on superficial LP activity
and cocontraction. Changes in activity levels and cocontraction of the
Methods. Ten male subjects participated in the “Berlin superficial LP musculature have been implicated in LP
Bed Rest Study” and underwent 8 weeks of bed rest with a pain. In studies of activation levels, a common finding is
1-year follow-up. A repetitive knee movement model at four that of increased activity (overactivity) in superficial
movement speeds in non–weightbearing was used to as-
muscles.4 –11 Studies of LP antagonist cocontraction in
sess, via electromyography, activity (amplitude-ratios) in
five superficial LP muscles and abdominal flexor-lumbar LP pain find that it is increased and results in increased
extensor cocontraction for LP stabilization. Testing was con- spinal loads.12–14 It has been argued that these changes in
ducted at regular intervals during and after bed rest. motor control reflect “splinting” of the trunk are mal-
Results. Analysis of the amplitude-ratio data showed a adaptive for LP stabilization.15
significant effect of testing date (F ⫽ 2.38, P ⫽ 0.005). This
effect was generalized across all muscles, however (F ⫽
While it is difficult to study LP motor control changes
0.59, P ⫽ 0.989). During bed rest, subjects exhibited higher secondary to sedentary lifestyle, studies in “unloading”
levels of activity but lower levels of cocontraction (F ⫽ 8.84, (microgravity, bed rest, and related environments16,17)
P ⬍ 0.001), and the changes were still present up to 1 year do provide insight. Leg and trunk muscle antagonist co-
after bed rest. contraction has been observed to increase during18 and
Conclusions. The bed rest protocol resulted in the de-
velopment of superficial muscle overactivity but decreased
after19 –21 exposure. Although postural instability after
cocontraction. These changes could reflect dysfunction of microgravity exposure has been documented,22,23 a
central nervous system control of LP stabilization. These component of motor control change must be involved in
changes were still apparent 1 year after bed rest, suggesting the increased cocontraction as the changes develop dur-
a stable change in motor control. ing unloading, rather than solely afterwards.18,24
Key words: inactivity, sedentary lifestyle, spine, stabi-
lization, unloading, spaceflight, motor control, abdomi-
Activation levels of superficial muscles have also been
nal, erector spinae, Berlin Bed Rest Study, low back pain. studied in unloading. Generally, superficial muscles are
Spine 2007;32:E23–E29 either less active or show little change during unload-
ing.25–31 After unloading, however, studies in animals
have found superficial muscle activity to be in-
creased.21,24 Human postural studies show similar pat-
tern of increased superficial muscle activity after unload-
From the *School of Information Technology and Electrical Engineer-
ing, University of Queensland, Brisbane, Australia; †School of Health ing.20,32–36 All of these studies have, however, been
and Rehabilitation Sciences, University of Queensland, Brisbane, Aus- undertaken on the leg musculature, and no data are
tralia; ‡Institute for Biophysical and Clinical Research into Human available on the LP region.
Movement, Manchester Metropolitan University, Cheshire, England;
and §Zentrum für Muskel- und Knochenforschung, Charité Campus We hypothesized that similar changes of increased co-
Benjamin Franklin, Berlin, Germany. contraction and overactivity would occur in the superfi-
Acknowledgment date: August 2, 2006. First revision date: August 21, cial muscles of the LP region during inactivity (bed rest).
2006. Acceptance date: August 21, 2006.
The Berlin Bed Rest Study was supported by Grant No. 14431/02/NL/ The European Space Agency’s “Berlin Bed Rest Study”
SH2 from the European Space Agency. provided the opportunity to examine this hypothesis.
The manuscript submitted does not contain information about medical This has not been studied before and also begins to ad-
device(s)/drug(s).
Institutional funds were received in support of this work. No benefits in dress a large gap in the literature on the effects of unload-
any form have been or will be received from a commercial party related ing on the LP region.
directly or indirectly to the subject of this manuscript.
Address correspondence and reprint requests to Daniel L. Belavý, BPhty, Materials and Methods
Zentrum für Muskel- und Knochenforschung, Charité Campus Benjamin
Franklin, Hindenburgdamm 30, 12200 Berlin, Germany; E-mail: Bed Rest Protocol. The Berlin Bed Rest Study (BBR) was
belavy@gmail.com undertaken at the Charité Benjamin Franklin Hospital in Ber-

E23
E24 Spine • Volume 32 • Number 1 • 2007

lin, Germany, from February 2003 to May 2005. Ten male ter.44 Electrodes were also placed over the biceps femoris mus-
subjects underwent 8 weeks of bed rest with a 1-year follow-up. cle to monitor leg muscle activity at rest. A ground electrode
The bed rest protocol as well as inclusion and exclusion criteria was placed at the right elbow. Standardized skin preparation
are discussed in detail elsewhere.37 However, in brief, subjects was performed involving washing the skin, shaving and the
were required to remain in bed at all times and were required to application of an abrasive-conductive gel.
restrict activity in bed to the minimal required for hygiene and
other necessary daily tasks. Adherence to this protocol was Data Acquisition. EMG and goniometer data were sampled
monitored by continuous video recordings and force transduc- simultaneously at 2000 Hz using a Powerlab system using
ers in the frame of the bed. The institutional ethics committee Chart software (version 4.2, AD Instruments, Sydney, Austra-
approved this study and subjects gave their informed consent. lia) and were stored for offline processing. A second computer
A history of LP pain was not a specific exclusion criterion also sampled the goniometer signal and implemented custom
for the BBR. As LP suffers are known to exhibit differences in written software in the Labview environment (version 6.1, Na-
motor control, a qualified physiotherapist attained subjects’ tional Instruments) to provide real-time feedback to the subject
subjective history of LP pain at the beginning of the study. on position and movement speed.
During bed rest and the follow-up period also, subjects’ mus-
culoskeletal health was monitored at regular intervals with Goniometer Signal Processing. Offline signal processing first
pain questionnaires.37 Incidence of LP pain was defined as any
examined the goniometer signal to find which “regions” of data
report of pain or discomfort between the first lumbar vertebrae
fulfilled the criteria: 1) three consecutive movement cycles, start-
and the gluteal fold.
ing at a minimum nearest 0°, 2) each cycle’s speed within ⫾5
cyc/min of target, and 3) peak flexion and extension angles
Repetitive-Movement Model and Testing Protocol. To within ⫾ 4° of their target (45° and 0°, respectively). This process
stimulate LP muscle activity for LP stabilization, a gravity-
limited the effect of extremes of performance/movement on ob-
eliminated repetitive knee movement model was used. Subjects
served EMG patterns and also provided data on movement accu-
were positioned in prone lying with a spring attached to their
racy: mean-squared-error (MSE) of movement speed (MSEspeed),
right ankle and to the apparatus and were able to view a feed-
maxima positions (MSE45°), and minima positions (MSE0°). MSE
back-monitor under the apparatus. The setup was optimized
values were calculated both within each data “region” (to corre-
such that, at rest (no activity in the hamstring musculature), the
late with EMG variables) and also over the entire 11-second
knee was held at 60° of flexion by the spring. This biomechani-
movement repetition at each speed (to examine motor skill acqui-
cal configuration has been shown previously to eliminate the
gravitational weight of the lower-leg during movement.38,39 sition over the course of the study).
Right knee movement was conducted between 0° and 45° of
flexion at four movement speeds (50, 75, 100, and 125 cycles EMG Signal Processing. Abdominal flexor-lumbar extensor
per minute). Three repetitions were conducted at each move- antagonistic cocontraction (CoCon) was quantified using an
ment speed. Each movement repetition was performed for 11 “area-normalization” method adapted from prior work.45,46
seconds. Subjects paused their breathing during each move- The following algorithm was used: 1) generation of a “linear-
ment repetition to remove the influence respiration on LP mus- envelope” of the EMG signals of the IO, EO, LES, and TES
cle activity.40 An electrogoniometer was placed at the right muscles (high-pass filtering at 100 Hz using a digital 10th order
knee to monitor knee position. quasi-Butterworth filter, rectification, and then low-pass filter-
Baseline data collection occurred on the first day of bed rest ing using a 10 Hz digital 10th order Bessel filter) and partition-
(BR1). Further testing was conducted on the fourth, 13th, 27th, ing into the appropriate data region; 2) normalization of the
41st, and 53rd days of bed rest (BR4, BR13, BR27, BR41, and area of each linear-envelope region to “1” by dividing each
BR53) and 3rd, 7th, 14th, 28th, 90th, 180th, and 360th days of value by the total area under the curve; 3) the greater value of
recovery (R ⫹ 3, R ⫹ 7, R ⫹ 14, R ⫹ 28, R ⫹ 90, R ⫹ 180, and the LES and TES signals was taken at each data point and the
R ⫹ 360). resulting signal renormalized as in step 2, which generates an
“extensor linear-envelope”; 4) abdominal IO and EO signals
Lumbopelvic Electromyography. Five superficial LP mus- are processed in the same fashion to yield a “flexor linear-
cles were monitored. Bipolar Ag/AgCl surface electrodes were envelope”; 5) the area of overlap of the flexor and extensor
placed over the following right-sided muscles with an interelec- linear-envelopes is calculated; and 6), the overlap area ranges
trode distance of 35 mm: 1) lumbar erector spinae with multi- from 0 to 1 and generates the flexor and extensor cocontraction
fidus (LES) positioned at the level of the fifth lumbar vertebrae variable (CoCon).
between the spinous process and a line drawn from the poste- To quantify EMG amplitude, activity-ratios (ratio) across
rior superior iliac spine (PSIS) to the interspace between the first movement speeds were used. To obtain this data, root-mean-
and second lumbar vertebrae41,42; 2) thoracic erector spinae square (RMS) values of the raw EMG signal in each data region
(TES) at the level second and third lumbar interspace, 1 cm were first measured. Then, at each movement speed 75 cycles/
medial to a line drawn from PSIS to the lateral border of the min and above, the RMS value in each data region was divided
erector spinae at the 12th rib41,42; 3) internal oblique (IO): the by the median RMS value of the speed below. This resulted in
superior electrode is placed 1 cm medial to the ASIS, the infe- three activity-ratios for each muscle (ratio75/50, ratio100/75, ra-
rior electrode is placed parallel to the inguinal ligament with tio125/100). Such relative measures of EMG amplitude have
the standard interelectrode distance43; 4) external oblique (EO) been used previously40 and have been shown to reduce inter-
at the most inferior point of the costal margin orientated along subject variability.47
a line from that point to the contralateral pubic tubercle43; and
5) inferior gluteus maximus (IGM) placed inferior and medial Statistical Analyses. Linear mixed-effects models were used
to a line drawn between the PSIS and posterior greater trochan- in statistical analysis.48 Analysis of variance of the EMG data
Superficial Lumbopelvic Muscle Overactivity • Belavý et al E25

Table 1. No. of Data Sets (Subjects) Available for to calculate Spearman’s rank correlation coefficient (␳) between
Inclusion in Analysis on Each Testing Day each of the variables.

Testing Day No. of Subjects Results


BR1 8 Due, for example, to subject absence or technical difficul-
BR4 6 ties, data from each subject on every scheduled testing day
BR13 8
BR27 8 were not always available. Table 1 presents the number of
BR41 8 subjects able to be included in statistical analysis on each
BR53 10 testing day. Based on the classification used for low back
R⫹3 10
R⫹7 7 pain occurrence, 6 subjects had a prior history of LP pain
R ⫹ 14 9 and 7 subjects experienced LP pain in the 1-year period
R ⫹ 28 9 after bed rest. Two of these represented “new” incidents of
R ⫹ 90 8
R ⫹ 180 6 LP pain, the remaining being recurrences.
R ⫹ 360 4
Abdominal and Lumbar Extensor Cocontraction
BR, day of bed rest; R⫹, day of recovery.
The measure of IO, EO, LES, and TES cocontraction
(CoCon) showed a significant main effect for movement
speed (F ⫽ 42.13, P ⬍ 0.001), with decreasing antago-
examined fixed effects for muscle, testing date, movement nistic cocontraction with increasing speed (50 cycles/
speed, interactions between each variable, as well as fixed ef-
min: 0.909 ⫾ 0.012; 75 cycles/min: 0.858 ⫾ 0.012; 100
fects for incidence of LP pain in the past or in the follow-up
period. The goniometer MSE data for each repetition
cycles/min: 0.815 ⫾ 0.012; 125 cycles/min: 0.801 ⫾
(MSEspeed, MSE45° , and MSE0°) were also analyzed to examine 0.013). History of LP pain and occurrence of LP pain
improvements in movement performance. A natural-log trans- during follow-up showed no significant main effect in the
formation was used for the ratio and MSE data to approximate CoCon data set (F ⫽ 0.06, P ⫽ 0.820 and F ⫽ 0.20, P ⫽
normality. Where appropriate, allowances were made for het- 0.675, respectively). Significant effects over testing date
erogeneity of variance across different grouping levels (such as (F ⫽ 8.00, P ⬍ 0.001) and date ⫻ speed (F ⫽ 8.34, P ⬍
movement speed, muscle, or date). The “R” statistical environ- 0.001) existed for the CoCon data.
ment (version 2.0.1, www.r-project.org) was used to imple- Changes of the CoCon variable over testing date and
ment these analyses. An ␣ of 0.05 was taken for statistical each movement speed compared to baseline (BR1) data
significance. As multiple measurement sessions were under- are presented in Figure 1. Strong effects can be seen at the
taken on the same subjects, a Bonferroni adjustment was not
125 and 100 cycles/min movement speeds for decreased
performed; rather, we looked for consistent significant differ-
ences across time points.
cocontraction over testing date. The effects appear to
To consider the association between motor control and develop quickly in bed rest (by BR4) and persist until 1
movement accuracy changes, correlation analyses between year after bed rest at the 125 cycles/min speed and up to
CoCon, ratio and the goniometer MSE data (MSEspeed, MSE45°, 6 months (R ⫹ 180) at the 100 cycles/min speed (with
and MSE0° values from each data “region”) were undertaken. trend to persistence at R ⫹ 360). Weak effects for de-
SPSS for Windows (version 10.0.1, www.SPSS.com) was used creased cocontraction are seen at the 75 cycles/min speed

Figure 1. Decreases in antago-


nist lumbopelvic cocontraction
during and after bed rest. Error
bars represent standard error of
the mean difference to baseline
(BR1) values. *P ⬍ 0.05; †P ⬍
0.01; ‡P ⬍ 0.001. BR, bed rest;
R⫹, recovery.
E26 Spine • Volume 32 • Number 1 • 2007

Table 2. First Day of Bed Rest (Baseline) cle ⫻ ratio: F ⫽ 3.09, P ⫽ 0.004) as well as testing date
Amplitude-Ratio Values (F ⫽ 2.37, P ⫽ 0.005). Further interactions between
testing date, ratio and muscle did not reach significance
Ratio75/50 Ratio100/75 Ratio125/100
(testing date ⫻ ratio: F ⫽ 1.22, P ⫽ 0.209; muscle ⫻
External oblique 1.34 ⫾ 0.05 1.82 ⫾ 0.07 1.68 ⫾ 0.13 testing date: F ⫽ 0.59, P ⫽ 0.989; testing date ⫻ ratio ⫻
Internal oblique 1.67 ⫾ 0.09 2.24 ⫾ 0.13 1.53 ⫾ 0.08 muscle: F ⫽ 1.01, P ⫽ 0.456), suggesting the effect was
Inferior gluteus maximus 1.43 ⫾ 0.08 2.18 ⫾ 0.15 2.18 ⫾ 0.15
Thoracic erector spinae 1.43 ⫾ 0.10 1.74 ⫾ 0.10 2.21 ⫾ 0.19 generalized across muscles and movement speeds. His-
Lumbar erector spinae 2.64 ⫾ 0.31 2.49 ⫾ 0.21 1.96 ⫾ 0.12 tory of LP pain was not significant in the ratio data set
Values are mean ⫾ SEM. (F ⫽ 0.12, P ⫽ 0.745), nor was LP pain incidence in the
follow-up period (F ⫽ 0.54, P ⫽ 0.493).
Table 2 gives the baseline values of ratio for each
during early to mid recovery (R ⫹ 4 to R ⫹ 90). No muscle. Changes in amplitude-ratio values over testing
significant changes in cocontraction are seen over time at date are presented in Figure 2a. Increased activity levels
the 50 cycles/min speed. are seen across the study period, and this is significant
Activity Levels: Amplitude-Ratio Data immediately after bed rest up to 3 months afterwards
Significant effects existed for muscle and ratio (muscle: (R ⫹ 90) with trend to significance 6 months afterwards
F ⫽ 4.91, P ⫽ 0.004; ratio: F ⫽ 9.22, P ⬍ 0.001; mus- (R ⫹ 180, P ⫽ 0.08). Although the testing date ⫻ ratio

Figure 2. (A and B) Increases in


activation levels during and after
bed rest. Error bars represent
standard error of the mean dif-
ference to baseline (BR1) values.
*P ⬍ 0.05; †P ⬍ 0.01; ‡P ⬍ 0.001.
BR, bed rest; R⫹, recovery.
Superficial Lumbopelvic Muscle Overactivity • Belavý et al E27

Figure 3. Improvements in movement performance over the study period. Values represent mean difference to baseline (BR1) testing of
each MSE variable. Negative values imply greater accuracy. Error bars indicate the 95% confidence interval of the mean; hence, the
difference to baseline is significant when the error bars to not cross x-axis (zero). BR, bed rest; R⫹, recovery.

interaction did not reach significance, Figure 2b indi- These correlations imply that less accurate movement is
cates, similar to cocontraction, that the effect was pre- associated with higher activity levels (amplitude-ratio) and
dominantly localized to the highest movement speeds lower antagonistic abdominal flexor-lumbar extensor an-
and was persistent up to 1 year after bed rest (R ⫹ 360) tagonistic cocontraction (CoCon).
despite low subject numbers at this time point.
Discussion
Movement Accuracy
We found long-term increases in muscle activity and de-
Analysis of the goniometer MSE data from each speed-
creased cocontraction during a repetitive-movement task
repetition showed a significant effect for movement
in the superficial LP muscles after 8 weeks of bed rest.
speed (MSEspeed: F ⫽ 114.32, P ⬍ 0.001; MSE45°: F ⫽
The increased activity appears to develop during bed rest
56.73, P ⬍ 0.001; MSE0° : F ⫽ 41.87, P ⬍ 0.001) and
at the highest movement speed, be generalized across all
testing date (MSEspeed: F ⫽ 3.45, P ⬍ 0.001; MSE45°: F ⫽
five superficial LP muscles and is significant up to 1 year
2.91, P ⬍ 0.001; and MSE0°: F ⫽ 3.84, P ⬍ 0.001).
after bed rest, despite low subject numbers at this time
Interactions of movement speed over testing date were
point. While consistent with other studies’ findings of
nonsignificant (testing date ⫻ speed: MSEspeed: F ⫽ 0.70,
increased superficial muscle activity after unload-
P ⫽ 0.937; MSE45°: F ⫽ 0.88, P ⫽ 0.692; MSE0°: F ⫽
ing,20,21,24,34 –36 the development of increased activity
0.85, P ⫽ 0.753). At baseline (BR1) MSEspeed was
during bed rest is contrary to prior research conducted
3.81 ⫾ 0.42 (cycles/min), MSE45° 2.15 ⫾ 0.20 and
during unloading itself.25–31 They are, however, similar
MSE0° 0.51 ⫾ 0.09. Figure 3 shows the change these
variables over the study period. Accuracy increases (MSE
decreases) though the bed rest and early-to-mid recovery
testing dates. Later in the recovery period, with testing Table 3. Correlations Between Electromyographic and
dates occurring at greater time separations, movement Movement Accuracy Variables
accuracy appears to in general decrease. At no time point Movement Accuracy Variables
is movement accuracy significantly less than at baseline EMG
testing. Variable MSEspeed MSE45° MSE0°

Correlation Analyses Activity-ratio 0.11 0.11 0.20


A significant negative correlation (P ⬍ 0.001) existed be- Cocontraction ⫺0.16 ⫺0.17 ⫺0.27
tween the ratio and CoCon variables (␳ ⫽ ⫺0.48); implying Values represent Spearman’s rank correlation coefficient (␳). All correlations
are significant (P ⬍ 0.001). MSEspeed, movement speed accuracy; MSE45°,
that as muscle activity levels increase, cocontraction levels accuracy of peak knee flexion position; MSE0°, accuracy of terminal knee
decrease. Significant correlations (P ⬍ 0.001) existed be- extension position. A positive correlation coefficient implies less accurate
movement is associated with higher EMG variable values.
tween EMG and movement accuracy variables (Table 3).
E28 Spine • Volume 32 • Number 1 • 2007

to those in LP pain, which commonly observe superficial with a prior history of LP pain. Also, statistical assess-
LP muscle overactivity.4 –11 ment of whether risk of LP pain increases after bed rest
Some authors have suggested that superficial LP mus- may require pooling of data from a series of studies.
cle overactivity in the pain population is a CNS strategy
to “splint” the trunk in response to deep muscle dysfunc- Conclusion
tion.15 The repetitive-movement task employed in the
The results suggest that long-term inactivity (bed rest)
current study requires the development of muscle stiff-
results in motor control change in the superficial LP mus-
ness at the LP region to allow efficient knee movement.
cles. In the current study, we observed this to be a gen-
During bed rest, the same subjects show significant atro-
eralized increase in superficial LP muscle activity and
phy of the deep multifidus muscle, while this is not seen
decreased cocontraction for stabilization of the LP re-
in the lumbar erector spinae or abdominal muscles
gion during a repetitive-movement task. In light of
(Hides JA, Belavý DL, Wilson SJ, Rittweger J, Felsenberg
known motor control dysfunction in LP pain, these ad-
D, Richardson CA, unpublished observations). We sug-
aptations could be maladaptive for normal LP function,
gest that due to this deep muscle atrophy, in order to
though further work in larger populations is required.
maintain the necessary amount of LP stiffness for the
knee movement task, the CNS increased the recruitment
of the superficial LP muscle systems. Key Points
Abdominal flexor and lumbar extensor cocontraction
decreases over the study period at the higher movement ● Superficial lumbopelvic muscle activity increases
speeds. These changes are significant early in bed rest and during and after bed rest.
persist up to 1 year afterwards. These findings of de- ● Abdominal flexor and lumbar extensor cocon-
creased cocontraction are contrary to findings of both traction during a repetitive-movement task de-
prior unloading studies18 –21 and those in LP pain,12–14 creases during and after bed rest.
where an increase in LP antagonist cocontraction are ● These changes likely reflect alterations in lum-
observed. The prior research into cocontraction used bopelvic motor control for stabilization.
static tasks, such as load-release or postural perturba- ● Inactivity may result in maladaptive motor con-
tion, but also active movements of the trunk. In such trol patterns for lumbopelvic stabilization.
tasks, antagonist cocontraction typically increases with
load, exertion, or speed of movement.49 –52 Cocontrac- Acknowledgments
tion is, however, both muscle and task specific. In the The authors thank the subjects who participated in the
current study, we used a repetitive limb movement task study and the staff of ward 18A in the Charité Campus
requiring the antagonist LP muscles to stabilize the pelvis Benjamin Franklin Hospital, Berlin, Germany for their
for efficient knee movement. Although the findings of expert assistance, as well as Mr. Benny Elmann-Larsen
overactivity suggest “splinting” of the trunk, reduction of the European Space Agency.
in flexor-extensor cocontraction over time could suggest
reduced stabilization of the LP region. Further work is
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