Effects of diaphragm stretching on posterior chain muscle kinematics and rib cage and abdominal excursion: A randomized controlled trial

Abstract

Background:
Few studies have explored the effects of stretching techniques on diaphragm and spine kinematics.

Objective:
To determine whether the application of diaphragm stretching resulted in changes in posterior chain muscle kinematics and ribcage and abdominal excursion in healthy subjects.

Method:
Eighty healthy adults were included in this randomized clinical trial. Participants were randomized into two groups: the experimental group, which received a diaphragmatic stretching technique, or the placebo group, which received a sham-ultrasound procedure. The duration of the technique, the position of participants, and the therapist who applied the technique were the same for both treatments. Participant assessment (cervical range of movement, lumbar flexibility, flexibility of the posterior chain, and rib cage and abdominal excursion) was performed at baseline and immediately after the intervention by a blinded assessor.

Results:
The mean between-group difference [95% CI] for the ribcage excursion after technique at xiphoid level was 2.48 [0.97 to 3.99], which shows significant differences in this outcome. The remaining between-group analysis showed significant differences in cervical extension, right and left flexion, flexibility of the posterior chain, and ribcage excursion at xiphoid level (p<0.05) in favor of the experimental group.

Conclusion:
Diaphragm stretching generates a significant improvement in cervical extension, right and left cervical flexion, flexibility of the posterior chain, and ribcage excursion at xiphoid level compared to a placebo technique in healthy adults.

Full text

http://dx.doi.org/10.1590/bjpt-rbf.2014.0169 1
Braz J Phys Ther.
Effects of diaphragm stretching on posterior chain
muscle kinematics and rib cage and abdominal
excursion: a randomized controlled trial
Francisco J. González-Álvarez1, Marie C. Valenza1,
Irene Torres-Sánchez1, Irene Cabrera-Martos1,
Janet Rodríguez-Torres1, Yolanda Castellote-Caballero1
ABSTRACT | Background: Few studies have explored the effects of stretching techniques on diaphragm and spine
kinematics. Objective: To determine whether the application of diaphragm stretching resulted in changes in posterior
chain muscle kinematics and ribcage and abdominal excursion in healthy subjects. Method: Eighty healthy adults were
included in this randomized clinical trial. Participants were randomized into two groups: the experimental group, which
received a diaphragmatic stretching technique, or the placebo group, which received a sham-ultrasound procedure.
The duration of the technique, the position of participants, and the therapist who applied the technique were the same
for both treatments. Participant assessment (cervical range of movement, lumbar exibility, exibility of the posterior
chain, and rib cage and abdominal excursion) was performed at baseline and immediately after the intervention by a
blinded assessor. Results: The mean between-group difference [95% CI] for the ribcage excursion after technique at
xiphoid level was 2.48 [0.97 to 3.99], which shows signicant differences in this outcome. The remaining between-group
analysis showed signicant differences in cervical extension, right and left exion, exibility of the posterior chain,
and ribcage excursion at xiphoid level (p<0.05) in favor of the experimental group. Conclusion: Diaphragm stretching
generates a signicant improvement in cervical extension, right and left cervical exion, exibility of the posterior chain,
and ribcage excursion at xiphoid level compared to a placebo technique in healthy adults.
Keywords: muscle stretching exercises; diaphragm; movement; physical therapy.
Clinical Trials Identier: NCT01753726.
BULLET POINTS
• Diaphragmatic stretching improved cervical movement and lumbar exibility.
• Diaphragmatic stretching increased exibility of the posterior chain.
• After diaphragmatic stretching, ribcage movement increased at xiphoid level.
HOW TO CITE THIS ARTICLE
González-Álvarez FJ, Valenza MC, Torres-Sánchez I, Cabrera-Martos I, Rodríguez-Torres J, Castellote-Caballero Y. Effects
of diaphragm stretching on posterior chain muscle kinematics and rib cage and abdominal excursion: a randomized controlled
trial. Braz J Phys Ther. http://dx.doi.org/10.1590/bjpt-rbf.2014.0169
1 Department of Physical Therapy, University of Granada, Granada, Spain
Received: May 05, 2015 Revised: Oct. 28, 2015 Accepted: Feb. 23, 2016
Introduction
The dynamic mobility of an articulated chain
is determined by the range of the individual joint
movements and the muscular properties, dening
the range of motion capacity1. Muscular chains
are composed of gravitational muscles that work
synergistically in the maintenance of the standing
position. It has been described that the shortening of
a muscle creates compensation in the adjacent and
also in distant muscles2.
The diaphragm is recognized as the primary muscle
of respiration that plays an important role in breathing
and physiological regulation. It is formed by a central
trefoil-shaped tendon that blends superiorly with the
brous pericardium
3
. The abdominal and thoracic
cavities on which the diaphragm action takes place
are also involved in postural stability and control.
Several studies4,5 have found a relationship between
the activity of the human diaphragm and intercostal
muscles and both respiratory and postural functions.
From a biomechanical point of view, the equilibrium
of the spine is achieved by a local and a global system
of muscle engagement. The stabilizing muscles
with insertion or origin at vertebrae (multidus,
transversus abdominis, diaphragm, internal oblique)

González-Álvarez FJ, Valenza MC, Torres-Sánchez I, Cabrera-Martos I, Rodríguez-Torres J, Castellote-Caballero Y
2Braz J Phys Ther.
provide intersegmental stability, whereas the longer
trunk muscles (erector spinae, rectus abdominis) are
dedicated to general movement
6
. Hence, the local
system, where the diaphragm plays an important
role, performs an action of stabilization and posture.
Over the last few decades, numerous studies7,8
have been conducted on the effects of stretching
and provided evidence of increased muscle control,
exibility, and range of motion. Although such studies
have traditionally focused on muscles of the lower
extremities and yielded high-quality research, the
biomechanical and structural characteristics of the
diaphragm imply an additional difculty. Techniques
aimed at the diaphragm have been used to increase
movement in the rib cage and the spine9,10.
Some evidence supports11 a relationship between
trunk muscle activity and posterior chain muscle
movement. Different studies
12-14
have used stretching
techniques including diaphragm stretching for spinal
pain relief, improving the posture12, stability13, and
the length of the posterior muscle chain14. However,
few studies have explored the effect of stretching
techniques on diaphragm and spine kinematics. Taking
into account the complex structure of the diaphragm
and its important role in the postural chain
2
, we
were prompted to verify the effects of a diaphragm
technique on posterior chain muscle kinematics and
rib cage and abdominal excursion in healthy subjects.
Method
Participants
This study was completed in the laboratory of the
Faculty of Health Sciences, University of Granada,
Granada, Spain. Asymptomatic volunteers ranging
in age from 18 to 60 years were recruited from the
general population between June 2012 and January
2015. Participants were excluded if they exhibited
history of neck trauma, history of fracture in any
part of the body, herniated disk or lumbar protrusion,
history of back surgery, signicant respiratory or
neurological condition, or regular use of analgesic or
anti-inammatory drugs. Those who were pregnant,
reported experiencing major psychological stress, or had
consumed caffeinated food and/or beverage products
within the previous 24 hours were also excluded.
The randomization sequence was drawn up and
kept off-site by a statistician who was not aware of
the study aims, using a random number generator in
blocks of eight with no stratication. The randomization
schedule was delivered, in a sealed envelope, to a
research assistant who assigned participants to the
groups and organized appointments for the participants
by phone. Each subject signed an informed consent
statement prior to involvement in the study. Approval
for the study was obtained from Ethics Committee of
the University of Granada, Granada, Spain (ID number
DF0037UG) and the procedures conducted in accordance
with the Declaration of Helsinki of 1975. The name
of the public trials registry is www.clinicaltrials.gov
and the registration number NCT01753726.
Outcome measures
The study assessor who collected the outcome
measurements was blinded to the study hypotheses
and group allocation.
Anthropometric measures
All subjects completed the same tests before and
after the intervention. For descriptive purposes,
anthropometric measurements were taken at baseline.
Body mass was measured in kilograms (Kg) to the
nearest 0.1 Kg on a calibrated digital medical scale
(Seca 843, Switzerland). Height was measured in
centimeters (cm) to the nearest 0.5 cm via a standard
wall-mounted stadiometer.
Chain muscle kinematics
Cervical range of motion
A Baseline Bubble Inclinometer (Fabrication
Enterprises Inc., White Plains, NY, USA) was used
to measure the active range of motion of the cervical
spine. The measurements were performed in two
planes of movement, lateral exion (frontal plane)
on the right and left side and exion-extension
(sagittal plane). The subject was seated comfortably
on a chair. The inclinometer was placed on the top
of his/her head, and the subject was asked to move
his/her head as far as possible in each movement.
A comparison of radiographs and inclinometer measures
showed excellent correlations (r<0.9997, P<0.05)15.
The standard values of cervical extension in healthy
subjects of 30-39 years are 36-102 degrees, for left
lateral exion 20-60 degrees and for right lateral
exion 27-62 degrees16.
Schober’s test
Schober’s test is a trunk exion test to evaluate
lumbar exibility. While the subject was in the
standing position, marks were made on the midpoint

Effects of diaphragm stretching on kinematics
3
Braz J Phys Ther.
between the posterior superior iliac spines and
10 cm above this point. The 10 cm distance was
then compared to the distance between the same two
marks when the subject was in the forward exed
position. Elongation of 5 cm or more between the
two marks during forward exion is considered to
be normal lumbar spine movement17. The validity of
Schober’s test against radiographs was found to be
strong (r=0.90) to moderate (r=0.68). The intraclass
(r=0.96) and interclass (r=0.90) reliability was found
to be excellent18.
Finger-to-floor test
In the nger-to-oor test (FFT), subjects stood on
a stool and exed the trunk forward to reach as far as
possible with both hands, without bending their knees19.
The distance (cm) between the level of the stool and
the middle nger was measured by the therapist. FFT
has high reliability and sensitivity scores19.
Abdominal and rib cage excursion measures
Abdominal and ribcage measurements can be used
as an evaluative method for diaphragmatic breathing
excursion to quantify possible alterations in thoracic
capacity and abdominal and chest wall compliance as
achieved by all expiratory and inspiratory muscles20.
By recording the abdomen and ribcage excursion
with a measuring tape over the second intercostal
space (axillary level), xiphoid process, and midpoint
between the xiphoid process and umbilicus (abdominal
level), competency in diaphragmatic breathing can be
demonstrated by a reduction in ribcage excursion20.
These indirect measurements have an intra-rater
reliability of 0.96-0.98 and an inter-rater reliability
of 0.84-0.87 with correlation coefcients not less
than 0.8420,21.
Experimental procedure
Subjects were randomly allocated by selection of
sealed envelope into one of two groups – an experimental
group or a placebo group. After all the measures were
taken, subjects were led to another room where they
received the diaphragmatic technique or the placebo
intervention. Subjects were then taken back to the
rst room for the post-treatment measures.
The stretching of the diaphragm technique was
executed as described previously by Chaitow et al.
22
.
Each subject was positioned seated erect. The therapist
stood behind the subject and passed his hands around
the thoracic cage, carefully introducing ngers
under the costal margins. The subject rounded the
trunk slightly in order to relax the rectus abdominis
(Figure 1). When the subject exhaled, the therapist
grasped the lower ribs and costal margin and eased
the hands caudally. The stretching was performed
once and the tension was maintained for 5-7 minutes.
In the placebo group, disconnected ultrasound was
applied in the same position for 7 minutes as placebo
treatment. The patients had to be seated erect, and the
ultrasound was applied in the costal margins.
Statistical analysis
Data were initially analyzed with regard to their
statistical distribution using the Shapiro-Wilks W
test. The demographic data and initial assessment
results were compared using the t-test with SPSS
software, version 17.0 (Statistical Package for the
Social Sciences, SPSS Inc., Chicago, IL, USA).
The sample size in the current study was powered
to detect statistical differences between the 2 groups
with 85% power based on a previous pilot study.
The t-test for paired samples was used to compare the
results of the assessment before and after treatment for
parametric data. The Wilcoxon signed rank test was
used to perform the above-mentioned comparisons for
non-parametric data. The independent t-test and the
Mann–Whitney U-test were used to conduct analyses
Figure 1. Diaphragm stretching technique.

González-Álvarez FJ, Valenza MC, Torres-Sánchez I, Cabrera-Martos I, Rodríguez-Torres J, Castellote-Caballero Y
4Braz J Phys Ther.
between groups for parametric and non-parametric
data, respectively. The alpha level was set at 0.05.
Results
The ow of participants through the trial is shown
in Figure 2.
Baseline characteristics (Table 1) of both groups
were similar although the stretching group had
comparatively fewer men, 19 (44.18%) vs. 15 (40.54%).
They also had very similar body mass index (BMI)
values (23.26±3.3 vs. 23.02±3.36).
Baseline characteristics between groups in the
primary outcomes are provided in Table 2, with no
signicant differences between groups in any of the
primary variables (p>0.05).
In the diaphragm stretching group, signicant
changes were found between pre- and post-intervention
measurement variables in between-group analysis
(Table 3).
For the control group, signicant differences were
found at abdominal level (p=0.02).
The between-group analysis showed signicant
differences in cervical extension, right and left exion,
exibility of the posterior chain, and ribcage excursion
at xiphoid level (p<0.01).
Discussion
The main purpose of the study was to determine
whether the application of a diaphragm stretching
resulted in changes in posterior chain muscle kinematics
Figure 2. Flow diagram of the progress through the phases of the randomized trial.
Table 1. Baseline characteristics of stretching and control group
participants.
Stretching group
(n=43)
Control group
(n=37)
Sex
n (% males)
19 (44.18) 15 (40.54)
Age (years)
Mean±SD
36.33±15.93 37.4±15.82
Height (cm)
Mean±SD
167±0.83 169±0.99
Weight (kg)
Mean±SD
65.22±12.59 66.5±12.10
BMI (kg/cm2)
Mean±SD
23.26±3.31 23.02±3.36
Smokers n (%) 22 (51.16) 19 (51.35)

Effects of diaphragm stretching on kinematics
5
Braz J Phys Ther.
and ribcage and abdominal excursion in healthy
subjects. The results supported the hypothesis that a
manual technique improves the variables measured by
Schober’s test and the nger-to-oor test, as well as
cervical mobility and xiphoid level ribcage excursion
immediately after the technique. No signicant
differences were observed in rib cage excursion at
axillary and abdominal level between groups. It is
normal that the highest changes were observed at the
xiphoid level, the nearest to the diaphragm, where
the stretching was performed. Due to the anatomical
access to the diaphragm, an anterior approach was
performed. The biomechanical relationship between the
diaphragm and other structures supports the hypothesis
that a diaphragm technique can have a repercussion
on other distant structures, as previously reported2,14.
Therefore, we have included the variables related to
mobility of the posterior chain in this study.
Table 2. Primary outcomes at baseline.
Stretching
group
(n=43)
Control
group
(n=37)
Cervical range of movement
Flexion (degrees) 46.21±9.36 49.07±6.66
Extension (degrees) 53.14±11.02 55.19±8.02
Right lateral exion
(degrees)
40.35±7.59 41.67±7.07
Left lateral exion
(degrees)
40.51±6.19 43.52±7.05
Schober’s test (cm) 14.52±1.06 14.28±1.08
Finger-to-oor test (cm) 4.66±6.76 3.37±5.24
Rib cage excursion
Axillary level (cm) 3.89±2.50 3.83±1.59
Xiphoid level (cm) 4.30±2.41 4.69±2.08
Abdominal level (cm) 0.10±2.87 –0.74±1.68
Data are expressed as mean±SD.
Table 3. Primary outcomes at baseline and post-technique.
Stretching
group
(n=43)
P-value Control group
(n=37) P-value
Mean between-group
difference
(95% CI)
Between-
groups
p value
Cervical range of movement
Flexion
Pre-technique
Post-technique
46.21±9.31
51.51±7.62 p<0.001**
49.07±6.61
50.00±6.72 0.379 1.51 [–2.06 to 5.09] 0.402
Extension
Pre-technique
Post-technique
53.14±11.0
59.3±9.9 p<0.001**
55.19±8.0
55.00±6.35 0.852 4.3 [0.006 to 8.59] 0.050*
Right lateral exion
Pre-technique
Post-technique
40.35±7.5
44.42±6.51 p<0.001**
41.67±7.01
41.30±5.90 0.646 3.12 [0.01 to 6.23] 0.049*
Left lateral exion
Pre-technique
Post-technique
40.51±6.11
46.98±6.2 p<0.001**
43.52±7.01
43.7±5.20 0.832 3.27 [0.37 to 6.17] 0.028*
Schober’s test
Pre-technique
Post-technique
14.52±1.05
15.01±1.03 p<0.001**
14.27±1.07
14.33±1.10 0.376 0.67 [0.15 to 1.19]
0.011*
Finger-to-oor test
Pre-technique
Post-technique
4.66±6.76
3.37±5.80 0.001**
3.37±5.21
3.33±5.32 0.646 0.039 [–2.72 to 2.8] 0.978
Rib cage excursion
Axillary level
Pre-technique
Post-technique
3.89±2.50
4.27±1.87 0.352
3.83±1.59
3.87±1.43 0.895 0.34 [–0.43 to 1.23] 0.347
Xiphoid level
Pre-technique
Post-technique
4.30±2.40
6.93±3.45 p<0.001**
4.69±2.08
4.44±2.36 0.582 2.48 [0.97 to 3.99] 0.002*
Abdominal level
Pre-technique
Post-technique
0.10±2.87
–0.12±2.57 0.885
–0.74±1.68
0.741±1.66 0.020* -0.75 [-1.86 to 0.35] 0.181
Data are expressed as the mean±SD. *Signicant differences p<0.05. **Signicant differences p≤0.001.

González-Álvarez FJ, Valenza MC, Torres-Sánchez I, Cabrera-Martos I, Rodríguez-Torres J, Castellote-Caballero Y
6Braz J Phys Ther.
The control group showed signicant changes in
abdominal excursion, which can be explained by the
relaxing posture adopted.
The sample of subjects included in the groups
was representative of a generally homogeneous
adult population (similar percentage of smokers, age
range, and BMI values). This homogeneity reduced
the probability of obtaining confounding factors that
might affect the value of our results.
Muscular chain contractions can cause changes in
the range of motion in other distant structures/muscles,
because muscles work synergistically in the same
chain2. It has been suggested that the shortening of a
muscle creates compensation in adjacent and also in
distant muscles2. From an anatomical viewpoint, the
diaphragm is a muscle with a central trefoil-shaped
tendon that blends superiorly with the fibrous
pericardium. The origins of the diaphragm are placed
in the crura from the bodies of the lumbar vertebrae,
the arcuate ligaments, the costal margins, and the
xiphoid23. Therefore, the biomechanical relationship
between the diaphragm and other structures support
the hypothesis that diaphragm stretching can have a
repercussion on other distant structures2, improving
the exibility of the posterior chain muscle and spine
structure mobility.
Our ndings are consistent with those previously
reported by other authors22,24 who have explored the
use of different techniques of manual therapy as an
option to increase the mobility of the spine in healthy
subjects. Saíz-Llamosas et al.24 suggested that using
a cervical myofascial induction technique increases
cervical exion, extension, and left lateral-exion.
Among the various types of manual therapy,
stretching techniques have been used in several studies
on the effects of stretching and evidenced increased
muscle control, exibility, and range of motion8,25.
Additionally, stretching techniques have been suggested
to be efcient in promoting respiratory variables such
as maximal respiratory pressures, thoracic expansion,
and abdominal mobility
26
. An interesting nding of our
study is that diaphragm stretching improves cervical
motion. Similarly, Kasunich
27
found that an abnormal
functioning of supporting distal structures can induce
biomechanical disturbances in proximal areas.
The analysis of pre-to-post stretching values provided
important data on posterior chain muscle kinematic
changes after diaphragm stretching. From a therapeutic
approach, diaphragm stretching can be used as an
effective therapeutic tool with an immediate response.
The results obtained are important in a therapeutic
context because it is evidenced that obtaining and
maintaining range of motion is very important and a
key factor in injury prevention.
Some limitations need to be mentioned, such as the
absence of follow-up in order to determine how long
the changes in kinematics were maintained and the
application in healthy subjects. Due to the anatomical
access to the diaphragm, an anterior approach was
performed and only the costal portion of the diaphragm
was lengthened, but our results have shown that there
is a positive effect in the main outcome measures.
The short length of the therapeutic session (5-7 minutes)
could be one of the limitations of this study. However,
previous studies2,14 have investigated the immediate
effects of manual techniques with benecial results.
Diaphragm stretching is a safe and well-tolerated
technique with an immediate signicant effect. Further
studies are needed to evaluate the applicability of this
technique in symptomatic populations. This research
could be used in other case scenarios and future research,
not only to prevent injury. Diaphragm stretching
could also be added to traditional interventions in
the treatment of whiplash, which can affect cervical,
thoracic, and lumbar regions as well and the rib cage.
Conclusions
Diaphragm stretching generated a signicant
improvement in posterior chain muscle kinematics
measured by Schober’s test, the nger-to-oor test,
cervical range of motion, and ribcage excursion at xiphoid
level immediately after the technique. In contrast, the
placebo technique showed no pre- or post-technique
differences in any of the measures. The between-group
analysis showed signicant differences in cervical
right and left exion, exibility of the posterior chain,
and ribcage excursion at xiphoid level.
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Correspondence
Marie Carmen Valenza
University of Granada
Department of Physical Therapy
Avda. de la Ilustración, 18016
Granada, Spain
e-mail: cvalenza@ugr.es