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


0025–7931/16/0915–0403$39.50/0 Respiratory Unit, San Paolo Hospital
82.108.120144.
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magnetic stimulation (twitch Pdi) [10–13]. Due to the Recent studies proved that ultrasound (US), a non-in-
in-vasive nature of this test and the technical challenges vasive radiation-free technique, permits the quantitative
in-volved in collecting reliable results [14], this assessment of diaphragmatic motion and function [22–
technique is restricted to a limited number of clinics and 25]. Different sonographic techniques have been validat-ed
laboratories and it has achieved only limited application [22, 25–27], but there is yet no standardized compre-
in clinical practice [10]. hensive examination. In this paper, we will review the lit-
Several non-invasive tests have been proposed to as- erature concerning the clinical indications, methods and
sess the diaphragmatic function in clinical practice. For interpretation of US of the diaphragm.
instance, the force of the muscle can be estimated from the
maximal static inspiratory pressure (MIP) generated
during voluntary maximal inspiratory maneuvers [15]. Methods
Studies conducted in patients affected by hemidiaphragm
Literature Search and Aims of This Review
or bilateral paralysis showed that MIP was reduced to 60
English literature was reviewed since the first description of
and 30% of the predicted values, respectively [5, 15]. Al- ultrasonography of the diaphragm to date (1969 to July 22, 2015) on
ternatively, the generated nasal pressure obtained during PubMed [28, 29]. The following keywords were used: ‘dia-phragm
sniff maneuvers (rapid inspirations through the unoc- dysfunction’, ‘diaphragm ultrasonography’, ‘diaphragm
cluded nostril while measuring the pressure developed in sonography’, ‘ultrasound diaphragm’, based on title, abstract and
MeSH terms. Original studies, editorials, published letters and re-
the other nostril) provides a reliable means of evaluating
views were included. In most of the studies, the diaphragm func-tion
the strength of the inspiratory muscles [16]. As with MIP, was estimated by direct observation of the excursion of the muscle
sniff inspiratory pressure (SNIP) is a volitional test that with breathing (direct techniques), whereas in a smaller se-ries the
depends on the extent of neuromuscular activation and is function was assessed by excursion of neighbor structures, such as
not uniquely sensitive to the diaphragm strength [17]. Yet, the liver or spleen (indirect techniques). Although a formal
comparison of the two techniques has never been performed so far,
it is thought to approximate the diaphragm contrac-tion
the direct methods are preferred for evaluating the function of the
[18], and many patients find it easier than measure-ments muscle [9, 17, 22, 26, 27, 30–33].
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 Review Findings
relationship between lung volume and muscle force, the
decrease in lung volumes occurs relatively late following Clinical Indications
the development of muscle dysfunction [19]. There are several indications to assess the diaphragm by
Electromyography with surface electrodes may assess US in clinical practice [34–37]. The test may be used in
the mechanisms of diaphragm dysfunction during tidal medical, surgical or intensive care settings as listed in table
breathing and with phrenic nerve stimulation. As such, it is 1. Usually, it is performed for diagnostic reasons, but it
used for the diagnosis of diaphragmatic paralysis and to may also serve as a guide for technical procedures, such as
differentiate neuropathic from myopathic dysfunction [9]. electrode insertion in electromyography in order to
The test is complex to perform, and potential artefacts minimize the occurrence of pneumothorax [38–43]. In
limit a broad use of the technique in clinical practice [10]. clinical practice, an elevated hemidiaphragm on the chest
A chest radiograph may show a reduction of the radiograph should prompt consideration of diaphragm
inspi-ratory excursion of the muscle during maximal function testing. US can help to determine whether the
respira-tory maneuvers. Yet, the lack of normative diaphragm elevation results from intrinsic paralysis, or-
values and low specificity in unilateral paralysis limit ganomegaly, or masses pushing the muscle upwards [44,
its clinical applica-tion [20]. 45]. Recent studies underline the role of the technique in
Fluoroscopy is commonly employed to diagnose dia- assessing a wide range of chronic diseases, such as neuro-
phragmatic paralysis, but this method lacks specificity [4]. logical, neuromuscular and respiratory conditions. Re-cent
False positive cases have been reported in normal pa-tients data suggest that US can provide important informa-tion
with rapid relaxation of the abdominal muscles during on ventilatory impairment in amyotrophic lateral sclerosis
inspiration following active contraction of the ab-dominal and hemiplegic stroke patients [36, 46]. There are also
muscles during expiration, which can be misin-terpreted as some initial reports suggesting a role for US in the
a contraction of the diaphragm [16, 21]. 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
left appositional area. 2, 3: right and left hemidomes.
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]. effects on rib cage expansion during inspiration [67], but
Notably, because of its non-invasive nature, US allows only the costal diaphragm has been assessed by US. Refer-
clinicians to monitor the clinical course and progression of ence values nowadays accepted as functional markers of
any diaphragmatic disease conditions over time [50]. severe diaphragmatic dysfunction are provided in table 3.
Measuring the change in diaphragm thickness during
Direct Techniques inspiration by US may also help assess the workload im-
From a functional and anatomical point of view, the posed to the respiratory system by the disease [32]. In 12
diaphragm is characterized by two major areas (fig. 1): the patients undergoing non-invasive ventilation after extu-
zone of apposition, which is in direct contact with the in- bation, the tidal thickening fraction of the diaphragm at
ternal rib cage, and the dome of the diaphragm, com-posed three levels of pressure support significantly correlated to
mainly of the central tendon of the diaphragm, which is the diaphragmatic pressure-time product (PTPdi) mea-
roughly horizontal and serves to separate the lung from the sured from esophageal and gastric pressure. A similar
abdomen [51–57]. Both areas are sur-rounded by the correlation between diaphragm thickening and dia-phragm
parietal pleura that allows the muscle to move freely [58, pressure generation has been demonstrated in healthy
59]. In humans in the upright position at functional subjects and in intubated patients on varying lev-els of
residual capacity (FRC), the appositional area represents pressure support ventilation [68, 69]. These find-ings help
55% of the entire surface of the muscle. During estimate the functional conditions of the dia-phragm under
contraction, this area shortens and thickens as a result of critical conditions [32, 70].
muscle contraction [58]. The physical dimensions of the
appositional area and the configuration and motion of the Indirect Techniques
dome of the diaphragm can be quantified by US as The movement of the diaphragm can also be evaluated
reported by several authors [22–24, 26, 27, 30, 32, 41, 49, by the displacement of abdominal organs in contact with
50, 60–66] (fig. 1; table 2). The costal and crural regions the muscle [71–74]. The underlying rationale is that dur-
of the diaphragm originate separately and exert different 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- were statistically different [72]. Similar results were re-
proaches have been compared with direct methods. For ported in other studies by examining the cranio-caudal
instance, displacement of the diaphragm estimated by the movement of the liver, pancreas and kidneys during qui-et
cranio-caudal shift of the left intrahepatic branch of the breathing [76, 77]. Finally, in 55 patients undergoing a
portal vein was similar to that measured by the radio- weaning test during spontaneous breathing, displace-ment
graphic method [73]. Also, the cranio-caudal excursion of of the liver or spleen by more than 11 mm predicted
the splenic hilum was found to be linearly correlated to successful extubation [71]. Collectively, these findings
radiographic measurements of the left hemidiaphragm, would suggest that from a clinical point of view, examin-
though absolute values obtained from the two methods ing the motion of abdominal organs during maximal in-
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DOI: 10.1159/000446518 Imeri/Brochard/Goligher/Centanni
by:
82.108.120144.

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

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Function DOI: 10.1159/000446518
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82.108.120144.
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