Review

Respiration 2016;91:403–411 Received: December 28, 2015

DOI: 10.1159/000446518 Accepted after revision: April 29, 2016
Published online: May 25, 2016

A Review of the Ultrasound

Assessment of Diaphragmatic
Function in Clinical Practice
a, b a
Giuseppe Francesco Sferrazza Papa Giulia Michela Pellegrino
a a c, d d, e
Fabiano Di Marco Gianluca Imeri Laurent Brochard Ewan Goligher
a
Stefano Centanni
a Respiratory Unit, San Paolo Hospital, Dipartimento Scienze della Salute, Università degli Studi di
b c
Milano, and Casa di Cura del Policlinico, Dipartimento di Scienze Neuroriabilitative, Milan, Italy; Keenan
Research Centre,
d
Li Ka Shing Knowledge Institute, St. Michael’s Hospital, Interdepartmental Division of Critical Care
e
Medicine, and Department of Physiology, University of Toronto, Toronto, Ont., Canada

Key Words Introduction

Diaphragm · Lung function tests · Ultrasound ·
Ultrasound technique
Abstract
Ultrasonography is the only non-invasive, non-ionizing im-
aging technique widely available to directly assess diaphrag-
matic function. Two different sonographic approaches permit
the assessment of muscle thickening in the zone of apposition
and excursion of the dome of the diaphragm. Thanks to the
new hand-held ultrasound instruments, the morphology and
function of the diaphragm can be assessed in different
settings, such as outpatient clinic, pulmonary function test
laboratory, hospital department and intensive care unit, and
under different conditions. Despite the exis-tence of different
acoustic views and several codified ap-proaches, a
comprehensive sonographic examination has never been
standardized for clinical use. In this review, we summarize the
clinical indications, methods and perspec-tives of the
© 2016 S. Karger AG, Basel
The diaphragm is the skeletal muscle that separates the
chest from the abdominal cavity. It is the most important
respiratory muscle and plays a major role in maintaining
ventilation. Dysfunction of the muscle occurs in several
disease conditions, such as myopathies and neuropathies,
mechanical ventilation (MV), surgery and trauma, tu-mors,
metabolic disorders, or chronic lung diseases [1– 6], and
may involve either one or both hemidiaphragms.
Dysfunction is defined as a loss of maximal muscle force
generation leading to reduced inspiratory capacity and
impaired respiratory muscle endurance [6–8]. According to
current knowledge, diaphragmatic dysfunction is fair-ly
under-recognized in clinical practice [9].
There are several methods to examine the function of
the diaphragm. The gold standard for the diagnosis of bi-
lateral diaphragmatic paralysis is the measurement of the
transdiaphragmatic pressure (Pdi) [7, 10]. This is the dif-
ference between abdominal and esophageal pressure dur-
ing maximal voluntary contraction or upon electrical or

technique in adults.
E-Mail ka
www.karg

© 2016 S. Karger AG, Basel Giuseppe Francesco Sferrazza Papa

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magnetic stimulation (twitch Pdi) [10–13]. Due to the
in-vasive nature of this test and the technical challenges
in-volved in collecting reliable results [14], this
technique is restricted to a limited number of clinics and
laboratories and it has achieved only limited application
in clinical practice [10].
Several non-invasive tests have been proposed to as-
sess the diaphragmatic function in clinical practice. For
instance, the force of the muscle can be estimated from the
maximal static inspiratory pressure (MIP) generated
during voluntary maximal inspiratory maneuvers [15].
Studies conducted in patients affected by hemidiaphragm
or bilateral paralysis showed that MIP was reduced to 60
and 30% of the predicted values, respectively [5, 15]. Al-
ternatively, the generated nasal pressure obtained during
sniff maneuvers (rapid inspirations through the unoc-
cluded nostril while measuring the pressure developed in
the other nostril) provides a reliable means of evaluating
the strength of the inspiratory muscles [16]. As with MIP,
sniff inspiratory pressure (SNIP) is a volitional test that
depends on the extent of neuromuscular activation and is
not uniquely sensitive to the diaphragm strength [17]. Yet,
it is thought to approximate the diaphragm contrac-tion
[18], and many patients find it easier than measure-ments
of MIP.
Pulmonary function tests are affected by diaphragmat-
ic dysfunction as documented by a decrease in total lung
capacity (TLC) and vital capacity. Due to the non-linear
relationship between lung volume and muscle force, the
decrease in lung volumes occurs relatively late following
the development of muscle dysfunction [19].
Electromyography with surface electrodes may assess
the mechanisms of diaphragm dysfunction during tidal
breathing and with phrenic nerve stimulation. As such, it is
used for the diagnosis of diaphragmatic paralysis and to
differentiate neuropathic from myopathic dysfunction [9].
The test is complex to perform, and potential artefacts
limit a broad use of the technique in clinical practice [10].
A chest radiograph may show a reduction of the
inspi-ratory excursion of the muscle during maximal
respira-tory maneuvers. Yet, the lack of normative
values and low specificity in unilateral paralysis limit
its clinical applica-tion [20].
Fluoroscopy is commonly employed to diagnose dia-
phragmatic paralysis, but this method lacks specificity [4].
False positive cases have been reported in normal pa-tients
with rapid relaxation of the abdominal muscles during
inspiration following active contraction of the ab-dominal
muscles during expiration, which can be misin-terpreted as
a contraction of the diaphragm [16, 21].
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Recent studies proved that ultrasound (US), a non-in-
vasive radiation-free technique, permits the quantitative
assessment of diaphragmatic motion and function [22–
25]. Different sonographic techniques have been validat-ed
[22, 25–27], but there is yet no standardized compre-
hensive examination. In this paper, we will review the lit-
erature concerning the clinical indications, methods and
interpretation of US of the diaphragm.
Methods
Literature Search and Aims of This Review
English literature was reviewed since the first description of
ultrasonography of the diaphragm to date (1969 to July 22, 2015) on
PubMed [28, 29]. The following keywords were used: ‘dia-phragm
dysfunction’, ‘diaphragm ultrasonography’, ‘diaphragm
sonography’, ‘ultrasound diaphragm’, based on title, abstract and
MeSH terms. Original studies, editorials, published letters and re-
views were included. In most of the studies, the diaphragm func-tion
was estimated by direct observation of the excursion of the muscle
with breathing (direct techniques), whereas in a smaller se-ries the
function was assessed by excursion of neighbor structures, such as
the liver or spleen (indirect techniques). Although a formal
comparison of the two techniques has never been performed so far,
the direct methods are preferred for evaluating the function of the
muscle [9, 17, 22, 26, 27, 30–33].
Review Findings
Clinical Indications
There are several indications to assess the diaphragm by
US in clinical practice [34–37]. The test may be used in
medical, surgical or intensive care settings as listed in table
1. Usually, it is performed for diagnostic reasons, but it
may also serve as a guide for technical procedures, such as
electrode insertion in electromyography in order to
minimize the occurrence of pneumothorax [38–43]. In
clinical practice, an elevated hemidiaphragm on the chest
radiograph should prompt consideration of diaphragm
function testing. US can help to determine whether the
diaphragm elevation results from intrinsic paralysis, or-
ganomegaly, or masses pushing the muscle upwards [44,
45]. Recent studies underline the role of the technique in
assessing a wide range of chronic diseases, such as neuro-
logical, neuromuscular and respiratory conditions. Re-cent
data suggest that US can provide important informa-tion
on ventilatory impairment in amyotrophic lateral sclerosis
and hemiplegic stroke patients [36, 46]. There are also
some initial reports suggesting a role for US in the
diagnosis of infectious (e.g. subphrenic abscess) and neo-
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Table 1. Clinical indications for ultrasonography of the
diaphragm in adults in different settings

Setting Indication
All Diagnosis and monitoring of diaphragmatic
paralysis [26]
Diaphragm supra-elevation on chest X-rays [20]
Dyspnea of unknown cause [9]
Medical Stroke with respiratory impairment [36]
Neuromuscular disorders [40]
Guidance for needle electromyography [41]
Assessment in chronic diseases (e.g. COPD) [65]
Surgical Traumatic diaphragm rupture [34]
Detection of postoperative complication [30]
ICU Difficult weaning [24]
Estimating work of breathing [32]
Assess VIDD [94]
Titrating ventilatory support [66]

Fig. 1. The four functional areas of the diaphragm. 1, 4: right and

plastic diseases of the diaphragm [45, 47]. Diaphragmatic
dysfunction as a result of phrenic nerve paralysis due to
trauma, cardiothoracic or neck surgery can be detected by
the technique [30, 34, 48]. Diaphragm US may also be
employed to determine whether diaphragm dysfunction
contributes to difficult weaning from MV [23, 24, 49].
Notably, because of its non-invasive nature, US allows
clinicians to monitor the clinical course and progression of
any diaphragmatic disease conditions over time [50].
Direct Techniques
From a functional and anatomical point of view, the
diaphragm is characterized by two major areas (fig. 1): the
zone of apposition, which is in direct contact with the in-
ternal rib cage, and the dome of the diaphragm, com-posed
mainly of the central tendon of the diaphragm, which is
roughly horizontal and serves to separate the lung from the
abdomen [51–57]. Both areas are sur-rounded by the
parietal pleura that allows the muscle to move freely [58,
59]. In humans in the upright position at functional
residual capacity (FRC), the appositional area represents
55% of the entire surface of the muscle. During
contraction, this area shortens and thickens as a result of
muscle contraction [58]. The physical dimensions of the
appositional area and the configuration and motion of the
dome of the diaphragm can be quantified by US as
reported by several authors [22–24, 26, 27, 30, 32, 41, 49,
50, 60–66] (fig. 1; table 2). The costal and crural regions
of the diaphragm originate separately and exert different
left appositional area. 2, 3: right and left hemidomes.
effects on rib cage expansion during inspiration [67], but
only the costal diaphragm has been assessed by US. Refer-
ence values nowadays accepted as functional markers of
severe diaphragmatic dysfunction are provided in table 3.
Measuring the change in diaphragm thickness during
inspiration by US may also help assess the workload im-
posed to the respiratory system by the disease [32]. In 12
patients undergoing non-invasive ventilation after extu-
bation, the tidal thickening fraction of the diaphragm at
three levels of pressure support significantly correlated to
the diaphragmatic pressure-time product (PTPdi) mea-
sured from esophageal and gastric pressure. A similar
correlation between diaphragm thickening and dia-phragm
pressure generation has been demonstrated in healthy
subjects and in intubated patients on varying lev-els of
pressure support ventilation [68, 69]. These find-ings help
estimate the functional conditions of the dia-phragm under
critical conditions [32, 70].
Indirect Techniques
The movement of the diaphragm can also be evaluated
by the displacement of abdominal organs in contact with
the muscle [71–74]. The underlying rationale is that dur-
ing breathing the liver and spleen undergo a translational
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Table 2. Selected studies providing direct visualization of the diaphragm by US

First author [Ref.] Setting Subjects Approach Probe (MHz) Patient position
Wait [60] RU 10 healthy intercostal linear (15) sitting
Ueki [27] RU 13 healthy intercostal linear (7.5) sitting
Gottesman [26] DM 15 patients, 15 healthy intercostal linear (7.5 – 10) standing
Summerhill [50] RU 21 patients intercostal linear (7.5 – 10) upright and standing
Lerolle [30] ICU 28 patients intercostal convex (7.5) semirecumbent
Boussuges [22] DP 210 healthy abdominal cardiac (2.5 – 3.5) standing
Kim [61] DA 35 patients abdominal cardiac (3.5) semirecumbent
Baldwin [62] ICU 13 healthy intercostal linear (10) semirecumbent and supine
Kim [24] ICU 88 patients abdominal convex (3.5) supine
Testa [63] ED 40 healthy abdominal convex (4) supine
Voyvoda [64] DR 23 patients, 20 healthy abdominal convex (multi-frequency) supine
Vivier [32] ICU 12 patients intercostal linear (12) semirecumbent
DiNino [23] ICU 63 patients intercostal linear (12) semirecumbent
Boon [38] DN 46 patients intercostal linear (7 – 13) supine
Ferrari [49] ICU 66 patients intercostal linear (10) semirecumbent
Zanforlin [65] RU 127, patients abdominal Sector (1 – 5), convex (3.5 – 5) semirecumbent
Goligher [66] ICU 107 patients intercostal linear (13) semirecumbent

ED = Emergency Department; RU = Respiratory Unit; DM = Department of Medicine; DP = Department of Physiology; DA =

Department of Anesthesiology; DR = Department of Radiology.

Table 3. Normal and pathologic values for diaphragm US

Diaphragmatic area Parameter and test Mean normal Pathologic values Reference
values ± SD
Zone of apposition diaphragmatic thickness 2.7 ± 0.5 mm <2 mm Gottesman et al. [26], 1997
a
thickening fraction 37 ± 9% <20%
Dome diaphragmatic tidal excursion women: 16 ± 3 mm women: <9 mm Boussuges et al. [22], 2009
men: 18 ± 3 mm men: <10 mm
sniff test women: 26 ± 5 mm women: <16 mm
men: 29 ± 6 mm men: <18 mm
deep breath women: 57 ± 10 mm women: <37 mm
men: 70 ± 11 mm men: <47 mm
a
Diaphragmatic thickness is measured at FRC. SD = Standard deviation. Thickening fraction: ratio of the difference between
thickness at TLC and thickness at FRC to thickness at FRC and expressed as percentage.

motion with minimal alteration in shape [75]. Several ap-
proaches have been compared with direct methods. For
instance, displacement of the diaphragm estimated by the
cranio-caudal shift of the left intrahepatic branch of the
portal vein was similar to that measured by the radio-
graphic method [73]. Also, the cranio-caudal excursion of
the splenic hilum was found to be linearly correlated to
radiographic measurements of the left hemidiaphragm,
though absolute values obtained from the two methods
were statistically different [72]. Similar results were re-
ported in other studies by examining the cranio-caudal
movement of the liver, pancreas and kidneys during qui-et
breathing [76, 77]. Finally, in 55 patients undergoing a
weaning test during spontaneous breathing, displace-ment
of the liver or spleen by more than 11 mm predicted
successful extubation [71]. Collectively, these findings
would suggest that from a clinical point of view, examin-
ing the motion of abdominal organs during maximal in-
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Fig. 2. a Top: the linear probe is positioned
on the right appositional area. Bottom: B-
mode image; arrowheads mark the pleura
and peritoneum (white lines) delimiting
the right appositional area of a normal dia-
phragm at FRC on the left and at TLC on
the right. b Top: the convex probe is posi-
tioned on the abdomen to examine the
right diaphragmatic dome. Middle: the
right diaphragmatic dome is seen as a hy-
perechogenic line posterior to the liver.
Bottom: M-mode scan of the dome at tidal
volume respiration (first two cycles on the
left) and during a maximal inspiratory ef- a b
fort (third cycle, delimited by calipers).
spiratory maneuvers may offer important clues about
the diaphragm function. Yet, it has to be acknowledged
that these indirect methods are somewhat limited by the
in-trinsic relationship with abdominal organs and their –
even if slight – modifications during breathing, and
there-fore require an advanced expertise in abdominal
ultraso-nography.
Technical Equipment and Setting
The equipment consists of a standard US system for
general imaging [44, 45, 78]. The US system must be
equipped with a multi-frequency transducer array sector or
convex (with a bandwidth of 2.5–5 MHz) and a linear
probe of at least 7.5–10 MHz (while higher frequencies,
such as 13–15 MHz, should be preferred to obtain good-
quality images). Pulmonary function testing laboratories
are the ideal setting for the test due to the possibility to
evaluate the results in conjunction with spirometry, MIP
and blood gas analysis. However, due to the portable
characteristics of new US systems, the test can be easily
conducted in the intensive care unit (ICU) or emergency
department [24, 34, 79]. Noteworthy, the technique can be
employed in laboratories of clinical neurophysiology to
assist in invasive electromyography [40, 42].
Ultrasonography of Diaphragmatic
Function
Color version available online
Evaluation of the Appositional Area
Subjects are best examined in the upright or semire-
cumbent position. A linear probe is placed on the line of
the eighth and ninth intercostal spaces midway between
the antero- and mid-axillary lines. The right apposition-
al area can be visualized 0.5–2 cm below the phrenico-
costal sinus (fig. 2a). The diaphragm is identifiable as a
three-layered structure immediately below the chest
wall [80]. It consists of a non-echogenic muscular layer
bounded by echogenic membranes of the peritoneum
and pleura (fig. 2a) [26, 27, 60, 81]. The diaphragm is
the most superficial structure obliterated by the leading
edge of the lung during inspiration. By M-mode, the
dia-phragmatic thickness is measured from the middle
of the pleural line to the middle of the peritoneal line at
FRC and TLC. The thickening fraction is calculated as
the per-centage increase in thickness during inspiration,
with reference values provided in table 3. It is an index
of mus-cle shortening during contraction, and a lack of
shorten-ing during a deep breath defines diaphragm
paralysis on US [26]. To complete the examination, the
same meth-odology should be used for the left side,
although mea-surements of left hemidiaphragm
thickness are more dif-ficult to obtain [22, 26, 68].
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 Evaluation of the Diaphragmatic Dome
The diaphragmatic domes are best evaluated with a
convex or sector probe [22]. On the right side, the probe
should be placed between the mid-clavicular and
anterior axillary lines in the subcostal area (fig. 2b) and
then di-rected medially, cephalically and dorsally so
that the US beam reaches the right dome
perpendicularly. Once a good quality and stability of the
image is obtained, inspi-ratory excursions can be
measured in M-mode [32]. The patient must be asked to
breath normally first, and then to perform inspiratory
sniff maneuvers and maximal in-spirations [22]. To
measure the linear excursion, the first caliper should be
placed at the foot of the inspiration slope on the echoic
line produced by the diaphragm, while the second
caliper should be placed at the apex of the slope. On the
left side, the subcostal view should be performed with
the probe held between the anterior and mid-axillary
lines using the spleen as acoustic window [22].
The next section provides two examples in which
dia-phragmatic US may help address physiological and
clini-cal questions concerning the role of diaphragmatic
func-tion in COPD and MV.
Ultrasonography of the Diaphragm in COPD
Diaphragmatic function is often impaired in COPD
[82–84], but the clinical impact of diaphragmatic dys-
function in COPD remains unclear due to the complex
derangements in respiratory mechanics associated with
the condition and the technical challenges in assessing
the muscle [85]. In 1983, Macklem et al. [86] reported
the negative effects of lung hyperinflation on the reduc-
tion of the appositional area and on the relationship be-
tween the costal and crural components of the muscle.
Yet, in this chronic disease, adaptation phenomena may
compensate for the reduced length-tension relationship
due to increased lung volumes or increased resistive
load [87]. This might explain the variable findings rang-
ing from normal to reduced function reported in studies
conducted with the US technique [82, 84, 86, 87]. For
instance, Baria et al. [85] reported no significant differ-
ence in diaphragm thickness between control subjects
and patients with COPD, with the exception of the sub-
group with severe air trapping. In contrast, two studies
documented a reduction in diaphragm excursion in
COPD in part related to air trapping [88, 89]. In anoth-
er investigation, the diaphragmatic thickening was
found to be negatively related to air-trapping indices
[90]. Taken together, these findings support the use of
US in examining the diaphragmatic function in COPD
408 Respiration 2016;91:403–411
DOI: 10.1159/000446518
in clinical practice. More studies are required to stan-
dardize the technique and select the parameters that best
explore and identify the level of dysfunction according
to the severity of the disease. Presumably, this can also
be done by integrating US with newly developed tech-
niques as suggested in the conclusive remarks of this re-
view [91].
Ultrasonography of the Diaphragm in the ICU
MV is frequently complicated by infections, ventila-tor-
induced lung injury and diaphragmatic dysfunction [92,
93]. The latter condition, referred to as ventilator-induced
diaphragmatic dysfunction (VIDD), is thought to result
from muscle disuse leading to atrophy and con-tractile
dysfunction; oxidative stress and increased pro-teolytic
activity play an important mechanistic role in this
phenomenon [94–96]. The occurrence of VIDD was re-
ported in 1988 [97] and first described in a prospective
study on rats after 48 h of MV in 1994 [30] and only re-
cently in humans [66, 95]. Subsequent studies have con-
firmed these results and documented that in both animal
experimental models and humans, changes in diaphragm
structure occur rapidly following the initiation of full MV
support [98]. In a recent multicenter study, diaphragmat-ic
thickness was shown to decrease rapidly during the ear-ly
course of MV in about 40% of the patients [15]. Since
diaphragm function plays a key role in successful libera-
tion from MV, assessing the presence of diaphragm dys-
function may assist with deciding whether to extubate the
patient. This can be easily done by US at the bedside [70,
99], although the best US technique to detect and monitor
diaphragm function is debated.
Some studies have focused on excursion of the dia-
phragm in mechanically ventilated patients. Jiang et al.
[71] reported that displacement of the liver or spleen >11
mm measured during a weaning session is 84% sensi-tive
and 83% specific for successful extubation. In 28 pa-tients
requiring more than 7 days of MV after cardiac surgery
and 20 patients with uncomplicated postopera-tive course,
Lerolle et al. [30] compared the maximal di-aphragmatic
excursion visualized by US during a maxi-mal inspiratory
effort while on a T-piece trial to the Gil-bert index (the
ratio of inspiratory gastric pressure swing to
transdiaphragmatic pressure swing), a previously val-
idated measure of diaphragm function. Diaphragm ex-
cursion on US was correlated with the Gilbert index and an
excursion of <25 mm was 100% sensitive and 85%
specific for severe diaphragm dysfunction (defined by a
Gilbert index below 0). In a medical ICU, Kim et al. [24]
measured diaphragm excursion in 82 mechanically ven-
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tilated patients at the start of a T-piece trial. They found
that 29% exhibited diaphragm dysfunction based on a
threshold excursion value of <10 mm during resting
tidal breathing to define diaphragm dysfunction [22].
Notably, patients with diaphragm dysfunction showed
higher rates of weaning failure (83 vs. 59%, p < 0.1,
with-in 48 h of self-breathing, and 50 vs. 22%, p = 0.01,
after 48 h of self-breathing) [24].
Diaphragm function has also been assessed in venti-
lated patients by measuring the diaphragm-thickening
fraction. The diaphragm-thickening fraction measured
during resting tidal breathing on a trial of spontaneous
breathing has recently been shown to predict extubation
success. A threshold value of a diaphragm-thickening
fraction of 30% exhibited the best sensitivity and
specific-ity for successful extubation [23]. A separate
study found that the diaphragm-thickening fraction
measured during inspiration from residual volume to
TLC predicted the success of a spontaneous breathing
trial (with an optimal threshold value of 36%) [49].
Taken together, these findings suggest that US can
provide very useful information in the management of
critically ill patients [100, 101]. It remains unclear
wheth-er the routine use of US would significantly
impact clini-cal outcomes of acute respiratory failure.
Future Perspectives and Conclusive Remarks
Though US has been largely used to identify severe
dysfunction of the diaphragm in mechanically ventilated
patients, this is not quite the case for mild to moderate
dysfunction. Identifying early signs of dysfunction by US
might lead to important actions to avoid disease progres-
sion (i.e. persuading the patients to quit smoking or of-
fering rehabilitation programs). It has been recently sug-
gested that a comprehensive approach inclusive of mul-
tiple physiological and imaging tests could help address
these questions [79, 91, 102]. For instance, classical US
investigations could be implemented with recent techno-
logical advances, such as three- or four-dimensional im-
aging mostly used now in the obstetrician or echocardio-
graphic setting. Similarly, the adoption of new motion
techniques, such as tissue Doppler imaging (TDI) or
speckle tracking could help add further insights in differ-
entiating active from passive motion [103, 104].
In conclusion, US is a non-invasive test which allows
real-time visualization of the diaphragmatic motion. US
has great potential to investigate severe diaphragm dys-
function in clinical practice, and the development of
new US technologies may open new horizons to assess
dia-phragm function in the early stage of disease states.

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