Journal of Electromyography and Kinesiology 28 (2016) 152–157

Contents lists available at ScienceDirect

Journal of Electromyography and Kinesiology

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

Lumbopelvic flexibility modulates neuromuscular responses during

trunk flexion–extension
Daniel Sánchez-Zuriaga a,⇑, Carla Artacho-Pérez a,b, Gemma Biviá-Roig c
a
Department of Anatomy and Human Embryology, Faculty of Medicine, Universitat de València, Avda. Blasco Ibáñez n° 15, 46010 Valencia, Spain
b
Instituto de Biomecánica de Valencia (IBV), Universitat Politècnica de València, Camino de Vera s/n., 46022 Valencia, Spain
c
Department of Physiotherapy, Faculty of Health Sciences, University CEU-Cardenal Herrera, Avda. Seminario s/n., 46113 Moncada, Valencia, Spain

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

Article history: Various stimuli such as the flexibility of lumbopelvic structures influence the neuromuscular responses of
Received 25 November 2015 the trunk musculature, leading to different load sharing strategies and reflex muscle responses from the
Received in revised form 16 March 2016 afferents of lumbopelvic mechanoreceptors. This link between flexibility and neuromuscular response
Accepted 18 April 2016
has been poorly studied.
The aim of this study was to investigate the relationship between lumbopelvic flexibility and neuro-
muscular responses of the erector spinae, hamstring and abdominal muscles during trunk flexion–exten-
Keywords:
sion. Lumbopelvic movement patterns were measured in 29 healthy women, who were separated into
Flexibility
Erector spinae
two groups according to their flexibility during trunk flexion–extension. The electromyographic
Biceps femoris responses of erector spinae, rectus abdominis and biceps femoris were also recorded.
Rectus abdominis Subjects with greater lumbar flexibility had significantly less pelvic flexibility and vice versa. Subjects
Trunk flexion–extension with greater pelvic flexibility had a higher rate of relaxation and lower levels of hamstring activation
Electromyography during maximal trunk flexion.
The neuromuscular response patterns of the hamstrings seem partially modulated by pelvic flexibility.
Not so with the lumbar erector spinae and lumbar flexibility, despite the assertions of some previous
studies. The results of this study improve our knowledge of the relationships between trunk joint
flexibility and neuromuscular responses, a relationship which may play a role in low back pain.
Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction
Movements involving trunk flexion–extension are common
during everyday activities, occupational demands and sports, and
show a high frequency of associated injuries, which in turn have
been linked to disruptions in spinal tissue neuromuscular balance
and load sharing (Colloca and Hinrichs, 2005). Therefore, improv-
ing our knowledge of the biomechanics of trunk flexion–extension
is of great clinical importance.
Trunk flexion–extension is an interaction between interverte-
bral and pelvic joints known as lumbo-pelvic rhythm (Cailliet,
1994) which is associated with specific patterns of muscle
activation. An eccentric contraction of the erector spinae muscles
(ES) controls spinal flexion, whereas the eccentric contraction of
hip extensors (glutei, hamstrings) controls pelvic flexion. At some
point during trunk flexion, ES activity suddenly ceases: this is
called the flexion–relaxation phenomenon (FRP) (Floyd and
⇑ Corresponding author.
E-mail address: Daniel.Sanchez@uv.es (D. Sánchez-Zuriaga).
Silver, 1955). Numerous studies have shown that FRP is a consis-
tent and predictable response in most normal subjects without
lower back pain (LBP) (Mayer et al., 2009).
FRP occurs between 75% and 85% of maximum trunk flexion
(Mayer et al., 2009; Neblett et al., 2003); when FRP starts, lumbar
flexion is almost complete, and the potential for even more pelvic
flexion remains. Maximum lumbar flexion is achieved first, and
from then on maximum trunk flexion occurs exclusively by means
of an increase in pelvic flexion, controlled by the glutei and
hamstrings (Sihvonen, 1997).
FRP also occurs in hamstrings during terminal pelvic flexion.
Hamstring electromyographic (EMG) activity ceases at 97% of
maximum lumbar flexion. From this point on, maximum trunk
flexion is achieved with no activity of the spinal and pelvic
muscles. During extension, both muscles activate concentrically:
the hamstrings activate first, followed by the ES (Sihvonen, 1997).
At the end of trunk flexion, the abdominal muscles, rectus abdo-
minis (RA) and oblique muscles, show a unique burst of activation
(Paquet et al., 1994). Contraction of the abdominal muscles con-
tributes to maintaining spinal flexion in the sagittal plane, without

http://dx.doi.org/10.1016/j.jelekin.2016.04.007
1050-6411/Ó 2016 Elsevier Ltd. All rights reserved.
 D. Sánchez-Zuriaga et al. / Journal of Electromyography and Kinesiology 28 (2016) 152–157 153

allowing lateral deviations, and can also participate in an active maneuver. The study hypothesis is that lumbar spine and pelvic
attempt to increase maximum trunk flexion (Bogduk, 2005; flexibility could influence the trunk muscle activity pattern during
Paquet et al., 1994). a flexion–extension task. In this scenario the viscoelastic structures
The spinal stabilizing system described by Panjabi (1992) of more flexible subjects would be able to elongate to a greater
encompasses the actions of all these structures. It consists of three degree, and this could cause different neuromuscular responses
subsystems: (a) passive (vertebrae, intervertebral discs, ligaments and movement patterns between more or less flexible subjects.
and fascia), (b) active (muscles and tendons) and (c) the neural
control unit. In a normal state the three subsystems work together 2. Materials and methods
to provide sufficient stability to the spine to match the instanta-
neously varying stability demands due to changes in spinal 2.1. Subjects
posture, and static and dynamic loads. The neural control unit esti-
mates the stability demands and consequently adjusts individual 29 healthy women, none of whom suffered from back pain at
muscle tension according to variations of lever arms and inertial the time of the study or recounted a history of lower back pain,
loads of different masses, and external loads (Hashemirad et al., participated in the study. Their age and anthropometric character-
2009; Panjabi, 1992). istics are summarized in Table 1.
Passive structures are deformed, which generates information Written consent to participate in the investigation was obtained
from the mechanoreceptors contained within them; this informa- from the subjects after they had been informed about the study,
tion generates muscle activation or relaxation responses (Holm and an institutional ethical review board (Human Research Ethics
et al., 2002). Different authors have studied the relationship Committee, Universitat de València, València, Spain) approved
between the viscoelastic properties of passive spinal tissues, neu- the project. All the procedures were conducted in accordance with
romuscular responses, and even potential mechanisms of spinal the principles of the World Medical Association’s Declaration of
damage. Solomonow et al. (1999) observed that the creep induced Helsinki (Rickham, 1964).
in viscoelastic tissues by the application of repeated loading causes
desensitization of mechanoreceptors, which in turn causes a signif-
2.2. Instrumentation
icant decrease in muscle activation and thus greater exposure to
instability and possible injury. Other studies (Sánchez-Zuriaga
The angular displacement of the lumbar spine and pelvis in the
et al., 2010) have observed that after inducing creep, and the con-
sagittal plane was recorded using a Liberty 240/16 electromagnetic
sequent increase in passive structure compliance, there is a
motion capture system (Polhemus Inc., Colchester, USA). This
marked delay in reflex lumbar muscle activation.
apparatus uses a low frequency magnetic field generated by an
In general, these kinds of studies emphasize the negative effect of
electromagnetic source, which is placed in a plastic platform
reducing the spinal rigidity, which results in increased compliance
adjusted at hip level for each participant. Two sensors detect the
and alters neuromuscular responses. This may be related to the
magnetic pulses, with a sampling frequency of 240 Hz. The first
mechanisms of back injury during activities involving trunk flexion.
sensor (L1) is attached to the skin overlying the spinous process
Changes in the distensibility of elastic structures have also been
of the first lumbar vertebra, and provides data on the displacement
associated with changes in neuromuscular activity of lumbopelvic
of the trunk as a whole (lumbar and pelvis). The second sensor (S1)
muscles and trunk motion patterns. Hashemirad et al. (2009)
is placed at the level of the first sacral vertebra, and provides data
observed that individual flexibility and angles of trunk and knee
on the inclination of the sacrum at the coxofemoral joint (pelvic
flexion have a significant effect on the flexion–extension responses
flexion) (Mayer et al., 1984). Subtracting the S1 data from the L1
of spinal extensor muscles. They found that in subjects with
data gives the true lumbar spine motion (Neblett et al., 2003).
greater flexibility the ES relaxed later during flexion, i.e. at greater
The EMG activity was recorded by three EMG100C Biopac
angles of spinal and pelvic flexion, and that they reactivated before
modules (Biopac Systems, Inc., Goleta, CA), using pre-gelled dispos-
extension starts, i.e. they had a shorter FRP. These changes were
able silver–silver chloride (Ag/AgCl) surface disk electrodes (2 cm
thought to be caused by a transfer of the stabilizing action to the
diameter). Prior to EMG electrode placement, the registration
active components in more flexible subjects, whereas in subjects
points of the activity of each muscle were located following the
with less flexibility passive structures would have a greater role
recommendations of the Surface Electromyography for Non-
in the control of movement. It therefore seems to be a relationship
Invasive Assessment of Muscles (SENIAM) project (Hermens
between measures of flexibility, such as lumbar and pelvic flexion
et al., 2000). The RA was located 3 cm to the right of the navel;
angles in maximum trunk flexion, and muscle activity patterns.
the hamstrings (biceps femoris, BF) electrodes were placed at the
This interdependence between individual flexibility and neuro-
midpoint of the distance between the right ischial tuberosity and
muscular response patterns may explain, for example, the
the fibular head. The ES EMG signal was recorded at the third lum-
increased likelihood that patients with hypermobility syndrome
bar vertebra, with electrodes placed 3 cm to the right of the spi-
have of suffering from musculoskeletal injuries, which is caused
nous process. A reference electrode was placed at the level of the
by tissue laxity and the corresponding decrease in proprioceptive
sternal body. After carefully cleaning and lightly abrading the skin
acuity and alteration of neuromuscular reflexes (Simmonds and
with an alcohol pad, two recording electrodes were attached on
Keer, 2007). In fact, Greenwood et al. (2011) found differences in
each registration point, parallel to the underlying muscle fibers,
muscle activation patterns between normal subjects and those
with a center-to-center distance of 2 cm. The raw EMG signal
with joint hypermobility, which specifically affect hip and pelvis
was band-pass filtered (cutoff frequencies: 10 Hz high pass,
muscles. The increased risk of injury of these patients has been
500 Hz low pass) and amplified (input impedance greater than
linked to these altered muscle stabilization strategies.
100 MX, common mode rejection ratio of 110 dB at 60 Hz, overall
None of the previous studies on the effect of individual flexibility
gain of 1000). EMG signals were A/D converted at a sampling
in trunk neuromuscular activation patterns has simultaneously
analyzed the activity patterns of the ES, hamstring, and abdominal Table 1
muscles during a dynamic trunk flexion–extension task. Therefore Age and anthropometric measurements.
the purpose of this study is to investigate the relationship between
n Age (years) Weight (kg) Height (m) Body mass index (kg/m2)
individual flexibility and the ES, hamstring, and abdominal muscles
29 30 ± 4 60.3 ± 8.5 1.7 ± 0.1 22.4 ± 3.0
EMG activity pattern during a dynamic trunk flexion–extension
154 D. Sánchez-Zuriaga et al. / Journal of Electromyography and Kinesiology 28 (2016) 152–157
frequency of 1000 Hz with a 16-bit data acquisition system (model
MP150; Biopac Systems Inc.). A synchronic signal generated at the
beginning of each measurement simultaneously sent a ‘‘start
recording” order to both the electromagnetic motion capture sys-
tem and the EMG recorder.
2.3. Testing procedure
Subjects stood barefoot on two markers on the floor with their
feet pelvis-width apart, knees straight, arms by their sides, and
with their hands facing inwards. At the start and end of each cycle,
they stared at a mark set at eye level on the opposite wall. Individ-
uals were told to move as sagittally as possible following these
instructions: bend neck, place chin on chest, then bend forward
and try to flex as far as possible, rest for a second at maximum flex-
ion and then return to the starting position. The subjects slipped
their hands down and up the front of their lower limbs to prevent
their upper limbs from swinging, and a metronome set at one beat
per second marked the pace of the movements. Trunk flexion took
four seconds, followed by a one-second pause at maximum flexion
and four seconds of trunk extension. Five repetitions of the trunk
flexion–extension cycle were performed. Trial runs allowed sub-
jects to practice the movements, and two experienced observers
monitored the subjects’ actions during testing. When the instruc-
tions had not been correctly followed (exertion, rhythm, range of
movement), the cycles were repeated. All tests were carried out
at least two hours after the subjects had risen from bed in order
to minimize diurnal variations in their spinal mechanics (Adams
et al., 1990).
2.4. Data processing
EMG data were rectified and smoothed by calculating their root
mean square, with a time window of 0.02 s. They were then nor-
malized as a percentage of that muscle’s peak activity during a sub-
maximal voluntary contraction, which has been found to be more
reliable than maximum voluntary contractions for trunk muscle
EMG normalization (Dankaerts et al., 2004). Prior to the trunk flex-
ion–extension movements, all the subjects performed a Biering-
Sørensen maneuver (an isometric trunk extension with the upper
body suspended in the air in front of the edge of a Roman chair)
to normalize the ES and BF signals (Biering-Sørensen, 1984). The
submaximal contraction for normalizing the RA signal was
performed as follows: from a supine position on an examination
couch, the subjects elevated the top of the trunk until the scapulae
lifted from the surface and simultaneously performed a double leg
raise, with the heels separated and held 1 cm off the couch
(O’Sullivan et al., 1997). This maneuver was designed to maximize
activation, both at the upper and lower portions of the rectus
abdominis.
In order to make comparisons on the same scale as the EMG
data, and to allow motion measurements to be compared between
subjects, degrees of spine and pelvis flexion were normalized as
percentages of the maximum spine and pelvic flexion during each
flexion–extension cycle. The lumbar and pelvis flexion and EMG
percentages were plotted, which resulted in relative motion and
EMG activity curves representing the process of the movements
(Fig. 1).
In order to compare between curves, several summary
measurements were calculated for each of the three central
flexion–extension cycles (Matthews et al., 1990), and these were
subsequently averaged. ES and BF relaxation levels were quantified
by calculating a relaxation ratio (Paquet et al., 1994) by dividing
the average EMG activity at the end of lumbar (ES) or pelvic (BF)
flexion (85–100% of the flexion time, when flexion–relaxation is
already evident) by the activity in the central stages of flexion
(45–60% of the flexion time, when eccentric activity is at its peak).
Other summary measurements were: (1) the maximum range of
lumbar and pelvic flexion, (2) the spinal and pelvic postures at
the start and end of ES and BF relaxation and the RA activation
peak, (3) the average percentages of EMG activity during lumbar
(ES, RA) and pelvic (BF) maximum flexion and during the FRP
(ES, BF). The start and end of flexion, extension, and EMG activation
peaks were identified using a threshold method, as recommended
by Schinkel-Ivy et al. (2013). The start and end of flexion were
defined respectively as the start and end of the sustained and
abrupt increase in motion curves which exceeded the baseline
inclination values during standing. After the end of flexion, the
curve achieved a flat plateau which corresponded to maximum
flexion. The end of such plateau was considered the beginning of
extension, when the motion curve abruptly decreased until it
recovered baseline inclination values during standing. For the
FRP, the offset of eccentric flexion activation and the onset of con-
centric extension activation were defined respectively as the end of
the last peak in flexion EMG activity and the start of the first peak
in extension EMG activity, which exceeded the peak amplitude of
the baseline activity during the relaxation phase (Fig. 1).
MATLAB 2010a (MathWorks Inc., Massachusetts USA) was used
for all data analysis.
2.5. Statistical analysis
Pearson product-moment correlation coefficient and scatter
plots were used to check for possible links and joint variation in
the variables from all 29 participants, especially between lumbar
and hip flexibility measurements and in the variables defining
the neuromuscular response patterns. The correlation provided
by the Pearson correlation coefficient was considered acceptable
at values above 0.5 or below 0.5.
The maximum ranges of lumbar and pelvic flexion reached dur-
ing trunk flexion were used as a measure of flexibility. Quartiles of
these values were calculated, and subjects in the first quartile (less
flexible) were compared to those in the last quartile (more flexi-
ble). In the case of the lumbar spine, eight subjects were found
to be more flexible and seven less flexible, while in the case of
the pelvis seven subjects were found in each group.
The low number of subjects in each group made it difficult the
make the assumption that the data variables were normally dis-
tributed. Accordingly, the nonparametric Mann–Whitney U test
was used to show any significant differences in the variables
between more and less flexible subjects. An a level below .05
was considered significant for all the reported analyses, and all
calculations were performed using PASW Statistics for Windows,
Version 18.0 (SPSS Inc., Chicago, IL).
3. Results
No participant was in the last quartile of both lumbar and pelvic
flexibility, this is to say, no participant had both high pelvic and
lumbar flexibility. The opposite was also true, and no participant
was in the first quartile of both lumbar and pelvic flexibility.
The maximum range of lumbar flexion was significantly higher
in subjects with greater lumbar flexibility. Similarly, the maximum
range of hip flexion was significantly higher in subjects with
greater pelvic flexibility. However, subjects with greater lumbar
flexibility had a lower maximum range of hip flexion and vice
versa: subjects with greater hip flexibility had a lower maximum
range of lumbar flexion.
When compared to less flexible subjects, subjects with greater
pelvic flexibility showed less EMG activity in the right BF both dur-
ing peak pelvic flexion and during the hamstring FRP. Furthermore,
subjects with greater pelvic flexibility showed a lower BF
 D. Sánchez-Zuriaga et al. / Journal of Electromyography and Kinesiology 28 (2016) 152–157 155

Lumbar motion
Hip motion
ES EMG
BF EMG

% submaximal EMG
% maximum ROM a d

b c

0 1 2 3 4 5 6 7 8 9 10
time (seconds)

Fig. 1. Representative curves of lumbar spine and hip/pelvic motion, with simultaneous BF and ES activity patterns during trunk flexion–extension. (a, d) start and end of FRP
(ES). (b, c) start and end of FRP (BF).

Table 2
Main results.

Variables (units) Average (SD) Greater vs. lower Greater vs. lower Correlation Correlation pelvic
lumbar flexibility pelvic flexibility lumbar ROM ROM
Lumbar ROMmax (degrees) 58.56 (6.71) More flexible: 66.87 (2.94) More flexible: 53.37 (6.00) p < 0.01
Less flexible: 50.56 (4.15) Less flexible: 64.15 (4.30) r = 0.556
p < 0.01 p < 0.01
Pelvic ROMmax (degrees) 63.26 (14.39) More flexible: 53.80 (8.45) More flexible: 82.09 (7.02) p < 0.01
Less flexible: 72.51 (11.66) Less flexible: 45.53 (8.22) r = 0.556
p < 0.05 p < 0.01
Average ES ROMmax (% subMVC) 2.12 (0.97) NS NS NS NS
Average ES FRP (% subMVC) 1.87 (0.74) NS NS NS NS
Lumbar onset ES FRP (%ROMmax) 83.75 (6.12) NS NS NS NS
Lumbar offset ES FRP (%ROMmax) 97.76 (1.67) NS NS NS NS
Hip onset ES FRP (%ROMmax) 37.05 (21.11) NS NS NS NS
Hip offset ES FRP (%ROMmax) 56.83 (21.80) NS NS NS NS
Relaxation ratio ES 0.25 (0.19) NS NS NS NS
Average BF ROMmax (% subMVC) 5.43 (3.39) NS More flexible: 1.95 (1.77) NS p < 0.01
Less flexible: 8.12 (1.97) r = 0.767
p < 0.01
Average BF FRP (% subMVC) 3.29 (2.44) NS More flexible: 1.77 (1.90) NS p < 0.01
Less flexible: 5.18 (2.28) r = 0.508
p < 0.01
Lumbar onset BF FRP (%ROMmax) 94.41 (4.49) NS NS NS NS
Lumbar offset BF FRP (%ROMmax) 99.13 (0.90) NS NS NS NS
Hip onset BF FRP (%ROMmax) 75.52 (14.66) NS NS NS NS
Hip offset BF FRP (%ROMmax) 97.52 (2.28) NS NS NS NS
Relaxation ratio BF 0.43 (0.17) NS More flexible: 0.28 (0.11) NS p < 0.01
Less flexible: 0.64 (0.11) r = 0.606
p < 0.01
Average RA ROMmax (% subMVC) 26.11 (11.99) NS NS NS NS
Lumbar onset RA (%ROMmax) 94.18 (5.54) NS NS NS NS
Lumbar offset RA (%ROMmax) 94.59 (5.20) NS NS NS NS
Hip onset RA (%ROMmax) 77.39 (20.34) NS NS NS NS
Hip offset RA (%ROMmax) 54.62 (24.40) NS NS NS NS

Abbreviations: SD, standard deviation; NS, not significant; ROMmax, maximum range of movement; onset/offset: start/end (either of FRP or RA activation peak); % subMVC,
percentage of EMG activity during the submaximal normalization maneuver.

relaxation ratio, i.e. they had a higher level of BF relaxation during
full pelvic flexion. None of the other BF variables, or ES or RA
variables showed statistically significant differences between more
and less flexible subjects.
There was a strong and statistically significant inverse correla-
tion between the ranges of lumbar and pelvis flexion, and between
the range of pelvis flexion and the percentages of BF activity during
the FRP and maximum pelvis flexion. A strong and statistically sig-
nificant inverse correlation between the pelvic flexion range and
the BF relaxation ratio was also observed. In other words, greater
pelvic flexibility was associated with greater hamstring relaxation
during maximum pelvis flexion (Table 2).
156 D. Sánchez-Zuriaga et al. / Journal of Electromyography and Kinesiology 28 (2016) 152–157
4. Discussion
The purpose of this study was first to investigate the relation-
ship between lumbopelvic flexibility and patterns of EMG activity
for the ES, hamstring, and abdominal muscles during a trunk
flexion–extension task, and secondly to quantify the EMG activity
of these muscles during the same task.
Our results show that there are no differences in the patterns of
ES activity during trunk flexion and extension between subjects
with high and low pelvic or lumbar spine flexibility; similarly, there
were no differences in the EMG activity pattern of the RA, thus con-
tradicting the observations of previous studies. Hashemirad et al.
(2009) reported that, in subjects with greater flexibility, the ES
relaxes later during flexion and reactivates earlier during extension,
and therefore shows a shorter FRP, an effect they related to tension
development in the passive tissues. We did not observed this effect.
However, their work displays a number of methodological differ-
ences with the present study. Angular displacement data in the
Hashemirad et al. study were not standardized, but rather, were
presented as raw degrees of flexion. Standardization/normalization
is necessary to facilitate the interpretation of EMG and motion data,
and is essential for comparing values between different groups of
subjects on the same scale (Esola et al., 1996; Lehman and McGill,
1999). Given that in the present study there are comparisons
between independent groups, we normalized both motion and
EMG data as a percentage of the maximum range of flexion, and
as a percentage of the EMG activation during a submaximal volun-
tary contraction. Howarth and Mastragostino (2013) described how
expressing flexion angles as a percent of the full range of flexion
motion for a given condition negated any differences between con-
ditions. This effect of normalization could explain the differences
between our results and the results of Hashemirad et al.
Another methodological difference between the present study
and the one by Hashemirad et al. is that in order to measure flexibil-
ity they used a modified Schöber test and a toe-touch test, which do
not directly measure spinal curvature, and whose validity and relia-
bility for evaluating lumbar ranges of motion have been questioned.
Previous studies have concluded that both the modified Schöber and
toe-touch tests badly reflect the true lumbar angular displacement,
and should be complemented with radiographic analysis (Rezvani
et al., 2012). In our study we measured lumbar and pelvic flexibility
by means of the lumbar spine and hip ranges of motion, which are
recorded by an electromagnetic motion capture system. The reliabil-
ity, accuracy, and low error rates of this kind of electromagnetic
motion capture systems for the analysis of spinal motion are well
known (Pearcy and Hindle, 1989; Jordan et al., 2004).
Marker placement was also performed differently in the
Hashemirad et al. study. They placed their markers lateral to the
midline of the greater trochanter, iliac crest, and ribcage to
measure the angles of lumbar and hip motion. However, it has been
shown that the angles measured from lateral markers do not reflect
the actual angular displacement of the lumbar spine (Russell, 2010).
In our study we placed sensors on the center of the spinous pro-
cesses of the first lumbar and sacral vertebrae. It is true that skin
movement remains a problem over the vertebral spinous processes;
however, the fascia over the spinous processes has a rigid fixation to
bone (Lundberg, 1996), and thus skin movement will follow bone
movement more closely than in other regions.
The results of our study show how subjects possessing greater
lumbar flexibility are less flexible at the pelvic level and vice versa,
and that there is an inverse correlation between these two flexibil-
ity values. Lumbo-pelvic rhythm is the interaction between lumbar
and pelvic flexion during trunk flexion–extension (Cailliet, 1994).
The close interdependence of lumbar and pelvic flexion may make
them compensate each other, so that when the lumbar spine is
highly flexible a great degree of pelvis flexion is no longer neces-
sary for overall trunk flexion and pelvis flexion is therefore
reduced, and vice versa.
Our study also confirmed the existence of FRP in the hamstring
muscles, which follows previously described patterns (Sihvonen,
1997; Paquet et al., 1994). Regarding the abdominal muscles we
have also confirmed that their pattern of activation during flexion
and extension is characterized by a unique burst of activation at
the end of flexion (Paquet et al., 1994).
Our results show that subjects with greater flexibility at the pel-
vic level have a greater degree of biceps femoris muscle relaxation
in maximum flexion, and lower pelvic flexibility is associated to a
greater activation of the hamstrings in maximum flexion. Previous
studies have shown how an increase in the elongation of ligamen-
tous structures can cause a significant decrease in the activation of
extensor muscles such as the multifidus, through mechanoreceptor
desensitization (Solomonow et al., 1999). Our findings may be the
result of a similar effect in the hamstrings. Shortening of the ham-
strings and lower pelvic flexibility have been associated with the
presence of LBP, with some authors even recommending the use
of hamstring stretching in order to acquire more compliance and
increase the participation of the pelvis in trunk flexion–extension
(Cailliet, 1994; Esola et al., 1996). An increase in hamstring EMG
activity has also been shown in patients with LBP (Mooney and
Robertson, 1976). Our results suggest that this increase in ham-
string EMG activity in LBP might be associated to alterations in pel-
vic flexibility: this possibility should be addressed in future studies
with LBP patients.
We did not observe flexibility-dependent changes in the activa-
tion patterns of ES muscles. Apart from the aforementioned effect
of angular data normalization, one limitation of our study, which
could explain this finding, is the type of sample used. We worked
with healthy subjects with a varying, but within normal, range of
mobility. Differences between more flexible and less flexible subjects
were quite significant for the hip (almost 40 deg), and were linked to
the aforementioned alterations in the BF EMG patterns. However,
these differences were not as intense in the lumbar spine, with only
16 deg difference between the maximum lumbar flexion ranges of
more and less flexible subjects. Future studies should focus on indi-
viduals with hypermobility syndrome. In fact, Greenwood et al.
(2011) found that hypermobile subjects had greater pelvic instability
due to lower EMG activity in the erector spinae and gluteus maximus.
Interpretations of the results of this study are limited to our sub-
jects being all women. Such a sample was chosen in order to avoid
variability due to gender differences in both pelvic and spine flexi-
bility, and to make our results more comparable to previous studies
which also focused on women, such as Hashemirad et al. (2009).
Nevertheless, further studies would be needed in order to check
these parameters in male subjects. Another limitation of this study
comes from the measurement of sacral inclination in the sagittal
plane as an approximation of hip joint flexion. Given that femoral
kinematics were not recorded, and participants during unrestrained
standing forward flexion tend sometimes to posteriorly translate
the hip joints, there could have been changes in the inclination angle
of the femur which may cause pelvic sagittal inclination to underes-
timate true hip flexion. Although our approach has been used also
by several previous studies (Mayer et al., 1984; Neblett et al.,
2003), it may be worth it to check if femoral kinematics alter the
behavior of the hip joint during trunk flexion–extension, and its
relationship to lumbar motion and neuromuscular responses.
5. Conclusions
There is an inverse correlation between lumbar and pelvic flex-
ibilities. Both parameters have an influence on lumbo-pelvic
 D. Sánchez-Zuriaga et al. / Journal of Electromyography and Kinesiology 28 (2016) 152–157
rhythm during trunk flexion–extension. The flexibility of the lum-
bar spine or the pelvis does not seem to influence the patterns of
activation of the lumbar and abdominal muscles. However, pelvic
flexibility influences the pattern of hamstring activation. Specifi-
cally, subjects that are more flexible show a greater degree of BF
relaxation at maximum flexion.
Conflict of interest disclosure
None.
Acknowledgements
This study was funded by a research project from the Valencian
regional government (Spain), project number GV/2013/095 (‘‘Estu-
dio de los patrones de actividad electromiográfica de la musculat-
ura del tronco y el miembro inferior durante la flexo-extensión de
tronco, la fatiga y la marcha en personas sanas y pacientes con his-
toria de dolor lumbar” Conselleria d’Educació, Projectes d’I+D per a
grups d’investigació emergents 2013).
References
Adams, M.A., Dolan, P., Hutton, W.C., Porter, R.W., 1990. Diurnal changes in spinal
mechanics and their clinical significance. J. Bone Joint Surg. Br. 72B, 266–270.
Biering-Sørensen, F., 1984. Physical measurements as risk indicators for low back
trouble over one year period. Spine 9, 106–119.
Bogduk, N., 2005. Clinical Anatomy of the Lumbar Spine and Sacrum, fourth ed.
Elsevier, United Kingdom.
Cailliet, R., 1994. Structure and function of the lumbosacral spine. In: Low Back Pain
Syndrome. F.A. Davis Co, Philadelphia, pp. 17–55.
Colloca, Ch.J., Hinrichs, R.N., 2005. The biomechanical and clinical significance of the
lumbar erector spinae flexion-relaxation phenomenon: a review of literature. J.
Manipulative Physiol. Ther. 28, 623–631.
Dankaerts, W., O’Sullivan, P.B., Burnett, A.F., Straker, L.M., Danneels, L.A., 2004.
Reliability of EMG measurements for trunk muscles during maximal and
submaximal voluntary isometric contractions in healthy controls and CLBP
Patients. J. Electromyogr. Kinesiol. 14, 333–342.
Esola, M.A., McClure, P.W., Fitzgerald, G.K., Siegler, S., 1996. Analysis of lumbar
spine and hip motion during forward bending in subjects with and without a
history of low back pain. Spine 21, 71–78.
Floyd, W.F., Silver, P.H.S., 1955. The function of erectores spinae muscles in certain
movements and postures in man. J. Physiol. Lond. 129, 184–203.
Greenwood, N.L., Duffell, L.D., Alexander, C.M., Mc Gregor, A., 2011.
Electromyographic activity of pelvic and lower limb muscles during postural
tasks in people with benign joint hypermobility syndrome and non-
hypermobile people. A pilot study. Man. Ther. 16, 623–628.
Hashemirad, F., Talebian, S., Hatef, B., Kahlaee, A.H., 2009. The relationship between
flexibility and EMG activity pattern of the erector spinae muscles during trunk
flexion-extension. J. Electromyogr. Kinesiol. 19, 746–753.
Hermens, H.J., Freriks, B., Disselhorst-Klug, C., Rau, G., 2000. Development of
recommendations for SEMG sensors and sensor placement procedures. J.
Electromyogr. Kinesiol. 10, 361–374.
Holm, S., Indahl, A., Solomonow, M., 2002. Sensorimotor control of the spine. J.
Electromyogr. Kinesiol. 12, 219–234.
Howarth, S.J., Mastragostino, P., 2013. Use of kinetic and kinematic data to evaluate
load transfer as a mechanism for flexion relaxation in the lumbar spine. J.
Biomech. Eng. 135, 1010041–1010046.
Jordan, K., Haywood, K.L., Dziedzic, K., Garratt, A.M., Jones, P.W., Ong, B.N., et al., 2004.
Assessment of the 3-dimensional Fastrak measurement system in measuring
range of motion in ankylosing spondylitis. J. Rheumatol. 31, 2207–2215.
Lehman, G.J., McGill, S.M., 1999. The importance of normalization in the
interpretation of surface electromyography: a proof of principle. J.
Manipulative Physiol. Ther. 22, 444–446.
Lundberg, A., 1996. On the use of bone and skin markers in kinematics research.
Hum. Mov. Sci. 15, 411–422.
Matthews, J.N., Altman, D.G., Campbell, M.J., Royston, P., 1990. Analysis of serial
measurements in medical research. BMJ 300, 230–235.
Mayer, T.G., Tencer, A.F., Kristoferson, S., Mooney, V., 1984. Use of noninvasive
techniques for quantification of spinal range-of-motion in normal subjects and
chronic low-back dysfunction patients. Spine 9, 588–595.
Mayer, T.G., Neblett, R., Brede, E., Gatchel, R.J., 2009. The quantified lumbar flexion-
relaxation phenomenon is a useful measurement of improvement in a
functional restoration program. Spine 34, 2458–2465.
Mooney, V., Robertson, J., 1976. The facet syndrome. Clin. Orth. Rel. Res. 115, 149–156.
Neblett, R., Mayer, T.G., Gatchel, R.J., Keeley, J., Proctor, T., Anagnostis, C., 2003.
Quantifying the lumbar flexion-relaxation phenomenon. Theory, normative
data, and clinical applications. Spine 28, 1435–1446.
157
O’Sullivan, P., Twomey, L., Allison, G., Sinclair, J., Miller, K., 1997. Altered patterns of
abdominal muscle activation in patients with chronic low back pain. Aust. J.
Physiother. 1997 (43), 91–98.
Panjabi, M.M., 1992. The stabilizing system of the spine. Part I. Function,
dysfunction, adaptation, and enhancement. J. Spinal Disord. 5, 383–389.
Paquet, N., Malouin, F., Richards, C.L., 1994. Hip-spine movement interaction and
muscle activation patterns during sagittal trunk movements in low back pain
patients. Spine 19, 596–603.
Pearcy, M.J., Hindle, R.J., 1989. New method for the non-invasive three-dimensional
measurement of human back movement. Clin. Biomech. 4, 73–79.
Rezvani, A., Erguin, O., Karacan, I., Oncu, M., 2012. Validity and reliability of the
metric measurements in the assessment of lumbar spine motion in patients
with ankylosing spondylitis. Spine 37, 1189–1196.
Rickham, P.P., 1964. Human experimentation. Code of ethics of the world medical
association. Declaration of Helsinki. BMJ 2, 177.
Russell, B.S., 2010. The effect of high-heeled shoes on lumbar lordosis: a narrative
review and discussion of the disconnect between Internet content and peer-
reviewed literature. J. Chiropr. Med. 9, 166–173.
Sánchez-Zuriaga, D., Adams, M.A., Dolan, P., 2010. Is activation of the back muscles
impaired by creep or muscle fatigue? Spine 35, 517–525.
Schinkel-Ivy, A., Nairn, B.C., Drake, J.D.M., 2013. Evaluation of methods for the
quantification of the flexion-relaxation phenomenon in the lumbar erector
spinae muscles. J. Manipulative Physiol. Ther. 36, 349–358.
Sihvonen, T., 1997. Flexion relaxation of the hamstring muscles during lumbar-
pelvic rhythm. Arch. Phys. Med. Rehabil. 78, 486–490.
Simmonds, J.V., Keer, R.J., 2007. Hypermobility and the hypermobility syndrome.
Man. Ther. 12, 298–309.
Solomonow, M., Zhou, B.H., Baratta, R.V., Lu, Y., Harris, M., 1999. Biomechanics of
increased exposure to lumbar injury caused by cyclic loading: Part 1. Loss of
reflexive muscular stabilization. Spine 24, 2426–2434.
Daniel Sánchez-Zuriaga is an assistant professor at
the Department of Anatomy and Human Embryology
of the Universitat de València, Spain. He completed his
Ph.D. about the biomechanics of specific types of low
back injuries in 2006, and since then has kept working
on the effects of different kinds of stimuli, pathologi-
cal conditions and treatments in the neuromuscular
responses and motion patterns of the lumbopelvic
region. He has published several research papers on
the subject, and directed several research projects
about the biomechanics of low back pain.
Carla Artacho-Pérez received the MSc degree in
Biomedical Research (she also was previously graduated
in physiotherapy) from the Universitat de València,
Spain in 2013. Since 2013, she is also a Ph.D. student in
the Department of Anatomy and Human Embryology,
Faculty of Medicine, Universitat de València. Currently,
she is working as a research assistant in the Biome-
chanics Institute of Valencia. She has a wide experience
in the study of biomechanical patterns and development
of biomechanical applications. She has participated in
different national and international scientific projects.
Her research interests include rehabilitation medicine,
rehabilitation robotics and biomechanics.
Gemma Biviá-Roig got a degree in Biology from the
Universitat de València (Spain) in 2003 and a degree
in Physiotherapy from University CEU Cardenal Her-
rera, Moncada, Valencia (Spain) in 2007. She has an
MSc in Manual Therapy and Physical Therapy in
Sports from University CEU Cardenal Herrera (Spain).
Currently, she works as an assistant professor in the
Department of Physiotherapy, Faculty of Health Sci-
ences, at University CEU Cardenal Herrera. The main
focus of her research is the biomechanics of the spine
in pregnant women and postpartum. Additionally, she
cooperates in a line of research about physical activity
in older adults populations.