Manual evaluation of the diaphragm muscle

Abstract

The respiratory diaphragm is the most important muscle for breathing. It contributes to various processes such as expectoration, vomiting, swallowing, urination, and defecation. It facilitates the venous and lymphatic return and helps viscera located above and below the diaphragm to work properly. Its activity is fundamental in the maintenance of posture and body position changes. It can affect the pain perception and emotional state. Many authors reported on diaphragmatic training by using special instruments, whereas only a few studies focused on manual therapy approaches. To the knowledge of the authors, the existing scientific literature does not exhaustively examines the manual evaluation of the diaphragm in its different portions. A complete evaluation of the diaphragm is mandatory for several professional subjects, such as physiotherapists, osteopaths, and chiropractors not only to elaborate a treatment strategy but also to obtain information on the validity of the training performed on the patient. This article aims to describe a strategy of manual evaluation of the diaphragm, with particular attention to anatomical fundamentals, in order to stimulate further research on this less explored field.

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International Journal of COPD 2016:11 1949–1956
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HYPOTHESIS
open access to scientific and medical research
Open Access Full Text Article
http://dx.doi.org/10.2147/COPD.S111634
Manual evaluation of the diaphragm muscle
Bruno Bordoni1–3
F Marelli2,3
B Morabito2–4
B Sacconi5
1Department of Cardiology,
Foundation Don Carlo Gnocchi
IRCCS, Institute of Hospitalization
and Care with Scientific Address,
Milan, 2CRESO, School of Osteopathic
Centre for Research and Studies,
Castellanza, 3CRES O, School o f
Osteopathic Centre for Research
and Studies, Falconara Marittima,
4Foundation Polyclinic University
A Gemelli, University Cattolica
del Sacro Cuore, 5Radiological,
Onc ologi cal and Anat omopath ological
Sciences, Sapienza University of Rome,
Rome, Italy
Abstract: The respiratory diaphragm is the most important muscle for breathing. It contributes
to various processes such as expectoration, vomiting, swallowing, urination, and defecation.
It facilitates the venous and lymphatic return and helps viscera located above and below the
diaphragm to work properly. Its activity is fundamental in the maintenance of posture and body
position changes. It can affect the pain perception and emotional state. Many authors reported
on diaphragmatic training by using special instruments, whereas only a few studies focused on
manual therapy approaches. To the knowledge of the authors, the existing scientific literature
does not exhaustively examines the manual evaluation of the diaphragm in its different portions.
A complete evaluation of the diaphragm is mandatory for several professional subjects, such
as physiotherapists, osteopaths, and chiropractors not only to elaborate a treatment strategy but
also to obtain information on the validity of the training performed on the patient. This article
aims to describe a strategy of manual evaluation of the diaphragm, with particular attention to
anatomical fundamentals, in order to stimulate further research on this less explored field.
Keywords: diaphragm, osteopathic evaluation, manual therapy, chiropractic, physiotherapy
Introduction
Breathing is a systemic act, involving the whole body, the viscera, the nervous system,
and emotions. The diaphragm muscle is the main breathing muscle, influencing
with its contractions the respiratory activity.1 The diaphragm collaborates to various
processes such as expectoration, vomiting, swallowing, urination, and defecation.1
It facilitates the venous and lymphatic return and helps the viscera above and below
the diaphragm to work properly.1 Diaphragm’s activity is fundamental in the mainte-
nance of posture and body position changes and influences the pain perception, usually
decreased during the inspiratory apnoea.1,2 Diaphragmatic movements also change the
body pressure, as it facilitates the venous and lymphatic return.2 This pressure modula-
tion influences the blood redistribution, which could be probably correlated with the
response of baroreceptors and the reduction of pain perception, although there are not
scientific studies supporting this hypothesis yet.2
The most important stimulus for the respiratory acts is provided by chemorecep-
tors, whose task is to maintain the biochemical balance of the body.2 Breathing is also
influenced by internal and external conditions, with other ways of neural stimulation
beyond the chemoreceptorial stimulation.2 The diaphragmatic activity is not only
controlled by metabolic mechanism but also by emotional states such as sadness, fear,
anxiety, and anger.2 Breathing stimulates mechanoreceptors of the diaphragm and the
visceroceptors of viscera (moving during the respiratory acts), constituting the mecha-
nism of interoception.2 Interoception is the awareness of the body condition obtained
from information coming directly from the body itself.2 Diaphragmatic movements
also stimulate the skin and the mediastinum; this complex of afferent information
Correspondence: Bruno Bordoni
Department of Cardiology, Foundation
Don Carlo Gnocchi IRCCS, Institute
of Hospitalization and Care with
Scientic Address, S Maria Nascente,
Via Capecelatro 66, Milan 20100, Italy
Tel +39 2 34 9630 0617
Email bordonibruno@hotmail.com
Journal name: International Journal of COPD
Article Designation: Hypothesis
Year: 2016
Volume: 11
Running head verso: Bordoni et al
Running head recto: Manual evaluation of the diaphragm muscle
DOI: http://dx.doi.org/10.2147/COPD.S111634
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Bordoni et al
determines the central representation of breathing.2 The
amygdala, which is part of the limbic system, is recipro-
cally connected to each of the respiratory areas, just as the
medulla oblongata, and is considered the most important
area that manages emotive breathing.2 A respiratory disorder
certainly alters the emotional framework, such as depression
and anxiety, as well as the emotional state can negatively
affect the respiratory activity.2
In case of systemic disease, the diaphragm is always
involved, negatively contributing to the set of symptoms.
In chronic heart failure, the diaphragm is weaker, more
commonly placed in expiratory state, with more frequent
movements.3,4
The pathological changes are seen in patients with chronic
obstructive pulmonary disease (COPD).5
The progressive limitation of the airflow in COPD
patients causes a pathological adaptation of the diaphragm,
although the reasons for these changes are not fully clear.
These changes in position adversely affect the exercise
tolerance; more in detail, the dome of the diaphragm is
lowered, in inspiratory position.6 The contractile force is
decreased, with electrical and metabolic alterations. The
muscle thickness is increased, especially on the left side,
with decreased mechanical excursion, probably due to fibers’
shortening.7,8 A decrease of anaerobic type fibers (type II)
and an increase in aerobic fibers (type I) are observed;
this process progressively increases with the pathology
worsening.8 The increase in the oxidative process, however,
does not correspond to an improvement of the diaphragmatic
function. The rate of detectable myosin decreases, resulting
in altered sarcomeric organization and further decreasing of
the contractile strength.8 The phrenic activity is abnormal,
presumably due to the nerve stretching caused by the chronic
lowering of the diaphragm, resulting in such a neuropathy.9
The exercise intolerance in patients with congestive heart
failure and COPD does not correlate with the common
functional indexes (ejection frequency and forced expira-
tory volume in 1 second); rather it is the peripheral muscle
adaptation, including that of the diaphragm, to have a heavy
influence on the symptomatic scenario.10,11
As mentioned in the article, the diaphragm influences
the patient’s emotional state. In patients with COPD, the
incidence of depression varies from 8% to 80%, according
to different studies.12 Depression may be considered a pre-
dictor of mortality during hospitalization for acute respira-
tory events.13 Depression and anxiety negatively affect the
rehospitalization, but only 33% of patients are treated with a
pharmacological process taking into account these psychiatric
symptoms.13 Depression affects the physical status of the
patient, as demonstrated by some authors who observed a
worsening in the test of Cooper (12 minutes run) and an
increased mortality rate.13 Anyway, there are not enough data
exhaustively explaining this correlation.13 The copresence
of depression and anxiety in patients with COPD increases
the mortality rate (of 83% according to some authors).14,15
The incidence of depression/anxiety increases with COPD
worsening.12,15 Even in this case, the exact mechanisms lead-
ing to this correlation are unclear; probably the presence of
dyspnea, systemic inflammation, and the effects on the brain
system derived from the smoking cessation are involved.12
Anyway, improving respiratory function improves psychiat-
ric symptoms, with exercise and manual therapy.12,16
To the knowledge of the authors, the existing scientific
literature does not exhaustively examines the manual evalu-
ation of the diaphragm in its different portions. A complete
evaluation of the diaphragm is mandatory for several pro-
fessional subjects, such as physiotherapists, osteopaths,
and chiropractors not only to elaborate a treatment strategy
but also to obtain information on the validity of the train-
ing performed on the patient. This article aims to describe
a hypothesis of manual evaluation of the diaphragm, with
particular attention to anatomical fundamentals, in order to
stimulate further research on this less explored field.
Anatomy of the diaphragm: origin
and insertion
An accurate knowledge of the anatomy of diaphragm is nec-
essary in order to perform a proper manual evaluation of the
muscle, with particular focus on hands’ positioning.
According to its insertions, the diaphragm can be divided in
costal, lumbar, and sternal portions. The sternal part arises with
two small fiber bundles from the posterior aspect of the xiphoid
process, near to the apex; the costal (or lateral) portion arises
from the inner and superior aspect of the last six ribs, with
interdigitation with the transverse muscle of the abdomen.17
The lumbar portions arises from the medial, intermediate, and
lateral ligaments of the diaphragm. The medial ligaments,
before reaching the vertebral bodies, delimitate with their
internal muscular bundles, at the level of D11, the esophageal
hiatus for the passage of the esophagus and vagus nerves. The
right medial ligament, thicker and longer than the left one,
terminates in a flattened tendon on the anterior aspect of L2–L3
(sometimes up to L4).17 Laterally to the right ligament, there
is a small ligament (called accessory or intermediate), whose
tendon is inserted at the level of L1–L2. Between this ligament
and the right medial one, there is a vertical split crossed by

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Manual evaluation of the diaphragm muscle
the large splanchnic nerve and the medial root of the azygos
vein.17 The left medial ligament ends with a flattened tendon
between L2 and L3; even in this case an accessory ligament
is present, forming a split for the large splanchnic nerve and
the medial root of hemiazygos vein.17 The tendons of these
two ligaments constitute, at the level of D12, a tendinous
arch (called the median arcuate ligament), through which the
aorta and the thoracic duct cross the diaphragm.17 The lateral
ligaments arise in the form of two thick tendons at the level of
the arch of the psoas muscle, constituting the medial arcuate
ligament; the latter passes above the psoas muscle, joining
the vertebral body of L1 and its transverse apophyses, and
more laterally, above the quadrates lumborum muscle, join-
ing the transverse process of L1 and the apex of the 12° rib,
forming the lateral arcuate ligament.17
The respiratory diaphragm muscle is innervated by the
phrenic nerve (C3–C5) and the vagus nerve (cranial nerve X);
the first receives pulses from groups of medullary neurons of
the pre-Bötzinger complex and from neurons of the parafacial
retrotrapezoid complex (correlated in turn with the retroam-
biguus nucleus of the medulla); however, it is worth to men-
tion that these connections are still unclear.17 The vagus nerve
is part of the parasympathetic autonomic system, originating
from the ambiguus nucleus of the medulla.17
The normal position of the diaphragm can be seen in the
chest X-ray. On the anterior–posterior projection, the dome
of the right hemidiaphragm is located at the level of 5°–6°
rib for what regard the anterior part, whereas the posterior
one usually lies at the level of the 10° rib.18 The left hemidi-
aphragm is slightly higher (about one intercostal space).13 In
10% of people, both domes have the same height, becom-
ing difficult to be differentiated in the lateral projection.18
Computed tomography and magnetic resonance imaging are
also useful in the morphological evaluation of the diaphragm,
even though they are used in second analysis, due to their
costs and availability.18 Fluoroscopy and ultrasounds are tech-
niques employed for the real-time evaluation of the moving
diaphragm, even though affected by visibility limitations.18
In most cases, the diaphragm shows a symmetrical respira-
tory excursion of ~2–10 cm, not related to the vital capacity
of the lungs.18 The ribs open out laterally in caudal direction
during inspiration, and the opposite during expiration.1 By
aging, the diaphragm becomes thinner and more frequently
located in expiratory position, especially in males.19
Physiotherapy and diaphragm
In literature, there are many physiotherapeutic approaches
based on diaphragm’s adaptability. The resistance training
in anaerobic regimen, or other training programs in aerobic
regimen, with different devices, can be used with increased
diaphragm performance in patients affected by respiratory
diseases.20,21
The respiratory rehabilitation improves the diaphragmatic
motion in both sides (using fluoroscopy imaging) in COPD
patients and improves the performance, structural, and
metabolic characteristics of the respiratory muscle (muscle
strength [PI {max}, cm H2O]), endurance (inspiratory thresh-
old loading, kPa), exercise capacity (Borg scale for respira-
tory effort, modified Borg scale, work rate maximum, W),
dyspnea (transition dyspnea index).20–22
Several tools such as bikes or cycle ergometers for the
upper limbs, or breathing stimulators (with different resis-
tances to be overcome during the inspiration), are usually
employed.23 Diaphragm training (with the aim to improve
lung capacity) is also used in other pathologic scenarios, such
as in patients who have undergone sternotomy for cardiac
surgery, and in patients affected by stroke.24,25 Diaphragm
training also improves other symptoms, such as those cause
by gastroesophageal reflux, and improves muscle propriocep-
tion of the lumbar–sacral region.26,27
Currently, the literature shows that there are no significant
differences in the rehabilitation results of the physical therapy
in patients with COPD, in terms of comparison between the
use of endurance and resistance training.28–30
Manual therapy and diaphragm
A few studies examined the manual evaluation of the dia-
phragm; although a review of the literature was not among
the aims of this paper, some short texts on the topic need to
be mentioned.
Potential therapeutic approaches involving the diaphragm
muscle have been proposed among gentle myofascial
release techniques, in the context of the therapeutic tech-
niques addressed to other diaphragms of the human body.3,31
The myofascial technique is the application of a low load,
long duration, stretch into the myofascial complex, with the
aim to restore the optimal length of this complex.32 The opera-
tor palpates the fascial restriction and the pressure is applied
directly to the skin, into the direction of the restriction, until
resistance (the tissue barrier) is manually perceived.32 Once
found, the collagenous barrier is engaged for a few minutes,
without sliding over the skin or forcing the tissue, until the
band starts to yield the complex and a sensation of softening
is achieved.32
Other types of manual (osteopathic) techniques employ
myofascial approaches, in particular by placing the hands

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under the chondrocostal junctions, inducing and facilitating
respiratory acts.33,34 The same techniques are also used in
other fields, such as to improve the symptoms of gastroe-
sophageal reflux, and to alleviate somatic symptoms in
pregnant women.35,36
There are several studies evaluating the effects of the
manual therapy in COPD. The approach to the patient varies
widely, both in terms of techniques and time management:
thoracic spinal mobilization, lymphatic drainage or pump,
diaphragmatic release trigger points, massage, articulation
techniques for ribs, myofascial release to the thoracic outlet,
suboccipital decompression, and muscular stretching.16,37,38
The results of the various respiratory parameters are always
positive, but we have not enough information to draw defini-
tive conclusions.
Only recently, physiotherapy and manual therapy have
been used together in the treatment of patients with COPD.
A previous study aims to assess the effect of these two thera-
peutic strategies, showing that the combination of rehabilita-
tion and osteopathy led to better results in comparison with
the single approach (increase in forced expiratory volume in
1 second, 6-minute walk test, decrease in residual volume).39
A recent study on COPD patients shows that many
parameters (mobility, exercise capacity, maximal respiratory
pressure, and vital capacity) are improved by working the
anterior chondrocostal arch with manual diaphragm release
technique.40
We need to find the correct technique to manually evalu-
ate the diaphragm, in order to improve the complementary
use of the usual rehabilitation and manual therapy.
Proposal of a manual evaluation
technique for the diaphragm muscle
The technique for the manual evaluation of the diaphragm
proposed in the present article arises from the growing need
to combine physiotherapy with manual therapy, considering
the new clinical data.
It is well known that, in patients with COPD or congestive
heart failure, the diaphragm has a specific preferred position,
which can be measured with different clinical tools. Accord-
ing to a recent study, human touch can distinguish any slight
variation, measurable in microns.41
We can strongly speculate on the possibility to train
the therapist, in terms of palpation technique, to check the
mobility and function of the inspiratory muscle, in order
to obtain additional clinical information on the therapeutic
approach, before and after the physiotherapy (as usually
happens for doctors in osteopathy).42
This manual evaluation is based on the experience of
authors, consisting in 20 years of clinical practice with
patients affected by respiratory and cardiac diseases; the
proposed method for COPD patients obviously need to be
deepened with further studies. It is important to remember
that, as for many other therapeutic techniques, whether
manual or otherwise, scientific proof is not available for
every existing treatment, this does not mean that, in absence
of scientific evidence, something is not valid; otherwise
there would not be new treatments or any improvement in
rehabilitative practice.31 In this regard, we wish to recall that
the evidence-based medicine, originated in the second half of
the 19th century, is based on the individual clinical expertise,
best external evidence, patient values, and expectations:
External clinical evidence can inform, but can never replace,
individual clinical expertise, and it is this expertise that
decides whether the external evidence applies to the indi-
vidual patient at all and, if so, how it should be integrated
into a clinical decision.43
There are no previous papers dealing with a comprehen-
sive evaluation of the diaphragm through manual approach,
and a description of techniques to be performed to evaluate
this muscle in all its portions is currently missing. We do
not have complete data on what happens in the different
anatomical areas of the diaphragm in patients with respiratory
disease; this text could be used as a guideline for researchers
for further evaluation.
The patient is supine, in comfortable position. The first
step deals with the assessment of the costal movement; this
should consist of lateralization during inspiration, with a cau-
dal direction, and the opposite during expiration.44 In case of
dysfunction of the diaphragm, this costal movement is usually
limited.45 The hands must be gently hold on the lateral sides
of the costal margins, in order to have a palpatory feedback
of the costal behavior during breathing (Figure 1).
Figure 1 The hands must be gently placed on the lateral sides of the costal margins
to receive palpation feedback of the costal behavior during breathing.

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Manual evaluation of the diaphragm muscle
In the following evaluation, respecting the previously
described anatomy, the hands can be hold on the costal
margins, anteriorly, with the thumbs being at the margin’s
level and the other fingers lying on the upper ribs. Since the
diaphragm muscle is lowered during inspiration, and then
rises during expiration, this manual position can be used to
assess the diaphragmatic excursion (Figure 2).1,17
The following manual positions deal with the evaluation
of the various portions of the diaphragm: domes, postero-
lateral area, xyphocostal area, medial ligament, and lateral
ligament.
To evaluate the diaphragmatic domes, the operator’s
forearm has to be hold parallel to the abdomen of the patient,
with the thenar and hypothenar eminences of the hand at the
level of the anterior margin of the costal arch; a gentle push
must be performed in cranial direction, so as to record the
elastic response of the tissue, for the right side as well as for
the left one (Figure 3). As usually observed in manual tests,
the elasticity of the tissue is reduced when a reduced move-
ment is obtained in response to the applied stimulus.42
To evaluate the posterolateral area, the hand must be
hold as previously described for the domes, but with the
forearm forming an angle of 45° with the patient’s abdo-
men; a gentle push must be applied obliquely, following
the line of the same forearm (Figure 4). This step needs
to be repeated for the other side also. This portion of the
diaphragm shows higher movement excursion during the
respiration and has a more vertical inclination in comparison
with the domes.18
The evaluation of the xyphoid-costal area is used to
assess whether, during inspiration and expiration, there is
regular elasticity of the tissue, which is necessary for normal
breathing; in fact, this area is usually more rigid in case of
abnormal diaphragmatic activity.45 The hand and the fore-
arm are positioned as in the evaluation of the domes, but in
the xyphoid area; a gentle push must be applied cranially
(Figure 5).
For medial ligaments, the spinal elasticity needs to be
evaluated, with the patient being supine. The operator hold
the last phalanges of the fingers (of one or both hands) placed
Figure 2 The hands can be held anteriorly on the costal margins, with the
thumbs being at the level of the margins and the other ngers placed across
the upper ribs. This manual position can be used to assess the diaphragmatic
excursion.
Figure 4 To evaluate the posterolateral area, the hand must be held as previously
described for the domes, but with the forearm forming a 45° angle with the patient’s
abdomen; a gentle push must be applied obliquely, following the line of the same
forearm.
Figure 3 To evaluate the diaphragmatic domes, the operator’s forearm has to
be held parallel to the abdomen of the patient, with the thenar and hypothenar
eminences of the hand at the level of the anterior margin of the costal arch; a gentle
push must be performed in the cranial direction, so as to record the elastic response
of the tissue, for both right and let sides.
Figure 5 The evaluation of the xyphoid-costal area is used to assess whether there
is regular elasticity of the tissue during inspiration and expiration, which is necessary
for normal breathing. The hand and the forearm are positioned as in the evaluation
of the domes, but in the xyphoid area; a gentle push must be applied cranially.

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Bordoni et al
combining the manual approach to the usual rehabilitation
process (Figure 8). The combination of several techniques in
a multidisciplinary process can be of benefit for the improve-
ment of the respiratory performance.47,48
We hope that this article could contribute to the state of
the art, representing a starting point, and enhancing the need
for further research in this field.
Conclusion
The breath is a systemic activity, able to involve several
body parts. The health of the diaphragm muscle is critical
for many patients, not just those with respiratory diseases.
A proper training of the main respiratory muscle can be
of benefit in several clinical scenarios; however, there are
not so many authors reporting on therapeutic techniques
focused on manual approaches and, more in detail, on
the manual evaluation of the diaphragm. This article
aims to describe a hypothesis of manual evaluation of the
diaphragm, with particular attention to anatomical funda-
mentals. The technique for the manual evaluation of the
diaphragm proposed in the present article arises from the
increasing need to combine physiotherapy with manual
therapy, considering the new clinical data. We do not have
complete knowledge on what happens in the different ana-
tomical areas of the diaphragm in patients with respiratory
disease; this text could be used as a guideline for researchers
for further evaluation.
Disclosure
The authors report no conflicts of interest in this work.
Figure 6 For medial ligaments, the spinal elasticity needs to be evaluated, with the
patient being supine. The operator should hold the last phalanges of the ngers (of
one or both hands) placed in the interspinous spaces of D11 and D12; by using a
gentle push towards the ceiling, a passive extension of the vertebra is obtained, in
order to deduce information on their elasticity.
Figure 7 The lateral ligaments are evaluated by actively involving the last rib. On the
opposite side of the rib to be evaluated, the body of the rib must be held with one
hand, and a gentle traction must be performed toward the operator.
Figure 8 Anatomical model.
Notes: (1) center tendon, (2) anterior diaphragmatic dome, (3) xiphoid area,
(4) costal area, (5) medial ligaments, (6) lateral ligaments, and (7) aorta.
in the interspinous spaces of D11 and D12; by using a gentle
push toward the ceiling, a passive extension of the vertebra
is obtained, in order to deduce information on its elasticity
(Figure 6).42 The same technique is used to evaluate the
lumbar vertebral bodies up to L4.42 The medial ligaments
play an important role in the mechanics of the dorsolumbar
region, in synergy with the abdominal wall muscles and the
thoracolumbar fascia.1,17,46
The lateral ligaments are evaluated by actively soliciting
the last rib. On the opposite side compared to the rib to be
evaluated, the body of the rib must be hold with one hand,
and a gentle traction must be performed toward the opera-
tor (Figure 7). The lateral ligaments play an important role
in managing the tension affecting the diaphragm and the
thoracolumbar fascia.17,46
The main purpose of using such manual evaluation is
to understand whether there is a restriction of movement
in a specific area of the diaphragm muscle, in order to plan
a manual treatment focused on the dysfunctional area,

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Manual evaluation of the diaphragm muscle
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