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www.analesderadiologiamexico.com PERMANYER Anales de Radiología México.

2023;22:1-10
www.permanyer.com

REVIEW ARTICLE

Diaphragm. Anatomy and evaluation by ultrasound


Diafragma. Anatomía y evaluación por ecografía
Aloisia P. Hernández-Morales*, Lya E. Pensado-Piedra, Fortunato Juárez-Hernández y Roberto Sotelo-Robledo
Departamento de Imagenología, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Ciudad de México, México

ABSTRACT

The growing acceptance of ultrasound in the evaluation of the thorax has allowed us to be
more accurate in the diagnosis of patients with thoracic pathology; thus, ultrasound in the
evaluation of the diaphragm, as the main respiratory muscle, facilitates an easy and repro-
ducible diagnosis, with a short learning curve. So this review provides the ultrasound im-
aging characteristics of the diaphragm in terms of its anatomical and functional description.

Keywords: Diaphragm. Contraction. Excursion. Diaphragmatic thickness.

INTRODUCTION that involve the central and peripheral ner-


vous system to those that strictly speaking
Diaphragm evaluation by ultrasound has had cause muscle dysfunction, such as muscular
a growing acceptance, since morphology and
dystrophies and diseases of the neuromuscu-
function are easily assessed in a fast and ac-
lar junction. This spectrum of disease leads
curate way, either in critically ill patients as
to diaphragm dysfunction, defined as loss of
well as those hemodynamically stable.
muscle strength that gives rise to a reduction
There are numerous diseases that can dam- of the inspiratory capacity, limiting respiratory
age the diaphragm, ranging from diseases muscular resistance.

Correspondence to: Received in original form: 15-10-2020


*Aloisia P. Hernández-Morales Accepted in final form: 22-03-2021
E-mail: aloisia_hndz@yahoo.com.mx

This article must be quoted as: Hernández-Morales AP, Pensado-Piedra LE, Juárez-Hernández F, Sotelo-Robledo R. Diafragma. Anatomía y evaluación por ecografía.
Anales de Radiología México. 2022;22(1):43-52.
1665-2118/© 2021 Sociedad Mexicana de Radiologia e Imagen, AC. Published by Permanyer. This is an open access article under the CC CC BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Anales de Radiología México. 2023;22

Currently, one of the most relevant applications and the abdomen. It is the main inspiratory
of ultrasound assessment of the diaphragm is muscle and acts as a barrier for transmission
the prediction of ventilator-induced diaphrag- of abdominal and thoracic pressure.
matic dysfunction. The diaphragmatic lesion
induced by the ventilator may be present in The diaphragm has a muscle component and
nearly 80% of patients in the Intensive Care a central tendon. The muscle component may
Unit and it happens as early as in the first 24 be subdivided in two parts: the costal dia-
to 36 hours after initiation of mechanical ven- phragm and the crural diaphragm. The costal
tilation. diaphragm originates anterior to the sternum,
laterally along the internal surface of the six
In this review we show the use of ultrasound inferior ribs and anteromedially along the
in the diagnosis of diaphragmatic paralysis costal cartilages. The crural diaphragm orig-
and diaphragmatic dysfunction, and its po- inates posteriorly along the three superior
tential use in patients in the Intensive Care lumbar vertebral bodies where the medial
Unit. and lateral arcuate ligaments arise.

The muscular component to the diaphragm


METHOD attaches to the fibrous central tendon, which
has a narrow, but strong fascia. The central
An extensive literary review in the Pub Med tendon of the diaphragm is variable in size
data base was conducted to intentionally in- according to each individual: it may comprise
vestigate about the first ultrasound descrip- less than 10% of the diaphragm to 35% in
tions, using the following key words: dia- some individuals, and generally has a V
phragmatic dysfunction and diaphragmatic shape. Also, it has several openings, called
ultrasound; including original studies, edito- “hiatus” that communicate the abdominal
rials and literature reviews. In most of the and thoracic cavities.
studies, diaphragm function was estimated
through direct observation of the diaphrag- The phrenic nerve innervates the diaphragm.
matic excursion, while in small series it was It is mainly a motor nerve that originates
evaluated by means of the neighboring ana- from C3, C4 and C5, with most of the motor
tomic structures, such as the liver and the neurons originating in C4. Both phrenic
spleen (indirect technique); also, the dia- nerves, the right and the left, are divided into
phragmatic thickness was assessed. three to five rami that innervate the antero-
lateral, posteriomedial, sternal and crural
portions of the diaphragm. The rami then run
REVIEW inside the diaphragmatic muscle in a medial
plane between the pleura and the layers of
Anatomy the peritoneum1.

The diaphragm is a musculotendinous struc- Physiologically, when it contracts, it moves


ture shaped as a dome, separating the chest caudally, increasing intraabdominal pressure

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A.P. Hernández-Morales et al.  Diaphragm. Anatomy and evaluation by ultrasound

and decreasing intrapleural pressure. This re- In Table 1, the indications for ultrasound as-
duction in pleural pressure results in an intra sessment of the diaphragm are shown.
alveolar pressure decrease. Once the intra al-
veolar pressure becomes subatmospheric, the
air goes into the alveolus1. Then, the dia- Ultrasound Assessment
phragm relaxes and goes up during exhala-
tion, allowing air outlet. It also helps to in- With ultrasound, the diaphragm can be seen
crease abdominal pressure for defecation, with a direct technique including thickness,
micturition and crying, working jointly with excursion and integrity assessment, or
the esophageal sphincter to exert pressure on with an indirect technique using another
the esophageal sphincter and prevent reflux2. anatomical structure of reference for the
craniocaudal displacement, such as the left
Normally, during rapid eye movement sleep, intrahepatic ramus, the excursion of splenic
the diaphragm is the only inspiratory muscle hilum, the liver, the pancreas and the kid-
that functions and the accessory inspiratory neys.
muscles remain inactive. Consequently, indi-
viduals with weakness or diaphragmatic pa- For complete assessment, either morphologic
ralysis may have hypoventilation symptoms, or functional, the diaphragm must be visual-
such as frequent nocturnal awakenings, noc- ized with two approaches: the dome and the
turia, vivid nightmares, nocturnal sweat, hy- diaphragmatic costal muscle. (Fig. 1).
persomnolence during daytime, depression
and morning headache3. The diaphragmatic dome can easily be seen
in the subcostal area, between the clavicular
In general, a posteroanterior chest Xray should midline, using the liver or spleen as acoustic
initially be taken when diaphragmatic pathol- window, with a 2-5 MHz low frequency trans-
ogy is suspected, aiming to: ducer, and leaning the transducer cephalical-
– See diaphragmatic disease, frequently in- ly and medially. The diaphragm is identified
cidental as a hyperechoic line, convex and continuous
– Take as a fact that the diaphragm is not (Fig.  2A). With this approach the integrity,
directly visible. echogenicity and cephalocaudal movement is
– Try to decide if the abnormality is, indeed, assessed in M mode.
located in the diaphragm, or secondary to
an adjacent disease to the diaphragm. The inspiratory diaphragmatic movement is
caudal, therefore the diaphragm moves to-
Due to the variability in the presentation of ward the transducer. In expiratory phase, the
the diaphragm, many changes found in a movement is cephalic, so it moves away
chest Xray are not related to a disease, signif- from the transducer. M  mode is used
icant or not, and then decisions must be made for the evaluation of diaphragmatic ex-
about the importance of the finding and if it cursion (displacement, cm). With this dia-
is necessary to perform additional imaging phragmatic cephalocaudal displacement and
modalities, such as ultrasound assessment. its sinusoidal curve, the contraction velocity

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Anales de Radiología México. 2023;22

Table 1. Indications for ultrasound assessment of the diaphragm

Total indication
– Diagnosis and monitoring of diaphragmatic paralysis
– Diaphragmatic elevation in the chest Xray
– Dysnea of unknown cause

Medical Arrest with respiratory failure


indication Neuromuscular disturbance
Electromyographic needle guidance
Evaluation of chronic disease (COPD)
Ventilatory support assessment

Surgical Traumatic rupture of diaphragm


indication F igure   1. Ultrasound approach of the diaphragm. The arrowhead
Detection of postoperative complication points to the diaphragmatic dome and the zone of diaphragmatic
apposition is indicated in the red box.
ICU Weaning difficulties
Estimation of ventilatory work
Estimation of ventilator‑induced diaphragm
dysfunction posterior part than its anterior border. The
Ventilatory support assessment
estimated motion of the posterior part of the
diaphragm is 40% greater than in its anterior
COPD: chronic obstructive pulmonary disease; ICU: intensive care unit.
part.5

There is a similar excursion of the two hemid-


(slope, cm/s), inspiratory time (Tinsp, s) and iaphragms, although the motion of the left
duration of the cycle (Ttot, s) are assessed. hemidiaphragm may be slightly greater than
(Fig 2B) 4. the right.

In healthy subjects, the excursion measure- The right diaphragmatic dome is 1.9 cm more
ment in spontaneous respiration measure- cephalic than the left diaphragm at the end
ment and in supine decubitus position is of expiration and 1.3  cm at the end of
16 mm in males and 18 mm in females5. This inspiration during spontaneous respiration.
measurement changes according to the respi- In patients who are mechanically ventilated,
ratory technique desired in the patient for anesthesized, and patients with paralysis, the
complete assessment of the diaphragmatic difference from the right and left side is 1.7
disease. With the sniff test, it ranges from 26 and 1.6  cm at the end of expiration and the
to 29  mm, and in forced respiration it is end of inspiration respectively. In supine po-
58 mm in females and 70 in males5. However, sition, in ventilated, anesthetized or para-
previous studies have reported average ex- lyzed patients, dependent regions show less
cursion values of 42 ± 16 a 79 ± 13  mm in diaphragmatic motion5.
forced respiration and 11 ± 4  mm to 21 ±
6 mm in spontaneous respiration6. The M mode representation of a forced
expiration manouver (after a maximum inspi-
The diaphragmatic dome motion is not uni- ration) is characterized by an initial slope fol-
form. Typically, there is greater caudal motion lowed by a plateau in maximum expiration.
of the medial region of the dome and of the This curve is similar to the one obtained in

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A.P. Hernández-Morales et al.  Diaphragm. Anatomy and evaluation by ultrasound

A B

F igure   2. A: Ultrasound image of the diaphragmatic dome. Continuity, echogenicity, integrity and cephalo-caudal movement are assessed
with this approach. B: M mode. In the motion tracing, the maximal height is excursion, and the cycle is the sum or inspiration (orange)
and expiration (blue).

the time/volume measurement in spirometry. The zone of diaphragmatic apposition ac-


The analysis of this spirometric curve allows counts for 25% of the total surface of the rib
to measure expiratory volume in the first sec- cage during respiration, but may vary from
ond (FEV1) and the vital capacity (VC), and 0% to total pulmonary capacity at more than
calculate the FEV1/VC6 ratio. 50% residual volume.

Preliminary observation in M mode of the During inspiration, the contraction of the cos-
diaphragmatic excursion during expiration in tal and crural muscles results in a caudal
healthy volunteers and patients with obstruc- motion of the diaphragm. This leads to the
tive airway disease indicate that the initial creation of appositional forces resulting in the
fall of the curve in expiration is deeper in coupling of the abdominal muscles, the dia-
healthy subjects that in those with obstructive phragm and the rib cage. This force is trans-
airway disease, suggesting that the excursion mitted through the zone of apposition and
may be delayed in patients with airway ob- originates the expansion of the inferior ribs.
struction and air trapping6. The appositional force is proportional to the
zone of apposition and the abdominal pres-
The second approach for visualization of the sure. Simultaneously, the contracted costal
costal diaphragm is the zone of diaphragmat- movement exerts another force to the inser-
ic apposition: between the eighth and tenth tion sites of the inferior ribs, creating a respi-
intercostal spaces, anterior or medial axillary ratory impulse and a «bucket handle or grip»
line, 0.5-2  cm below the costophrenic sinus motion.5.
(Fig. 3). This approach is used to assess thick-
ness; normal in this zone is 1.7 ± 0.2  cm in To obtain proper images of the diaphragm
relaxed respiration, increasing to a 4.5 ± thickness a high frequency transducer is need-
0.9 mm when total pulmonary capacity respi- ed. At 1.5-3  cm two parallel echogenic lines
ration takes place5. can be easily identified: the closest line is the

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Anales de Radiología México. 2023;22

F igure   4. Normal ultrasound anatomy. At the zone of apposition


(below) is a three-layered structure: pleura, diaphragmatic
muscle and peritoneum. The pleura and peritoneum are seen
lineal and hypoechoic, and the hypoechoic muscle has
interposed hyperechoic lines.

F igure   5. The contraction fraction is calculated by the difference


F igure   3. Zone of diaphragmatic apposition. This zone is located in inspiration and expiration.
between the eighth and the tenth intercostal space, between the
anterior and medial axillary line, in the costophrenic angle. The
diaphragmatic thickness must be measured at 0.5-2 cm from the
angle.
Contraction fraction 
 Thickness at the end of inspiration 
 Grosor – end of expiration 
pleura and the deeper one is the peritoneum.  
The diaphragm is a hypoechoic structure be- Thickness at the end of expi ration  100
tween those two lines, with some interspersed
lines from the intermuscular fascia (Fig. 4). Harper et al.8 describe an average contraction
fraction of 20%, during tidal respiration, with
The diaphragmatic thickening during active no significant difference between the right
respiration reflects the magnitude of the re- hemidiaphragm and the left hemidiaphragm
spiratory effort. The best descriptor of this in patients with mechanical ventilation. Oth-
phenomenon is the diaphragmatic contrac- er authors have reported that the measure-
tion fraction, calculated as the difference be- ments of the left diaphragm may not be con-
tween thickness at the end of inspiration and sistently obtained as in the right, due to the
at the end of expiration (Fig. 5)7: apposition of the bowel loops, obscuring the

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A.P. Hernández-Morales et al.  Diaphragm. Anatomy and evaluation by ultrasound

acoustic window and in our experience, to assessment. This is attributed to the active
the more complex location of the left zone of contraction of the abdominal muscles during
apposition. expiration, followed by a sudden relaxation of
the abdominal muscles at the beginning of
inspiration resulting in a descending move-
Diaphragmatic Paralysis and ment of the paralyzed diaphragm. Potentially,
Weakness this may be misinterpreted as an active dia-
phragmatic contraction4. This finding, fol-
Diaphragmatic paralysis and weakness may lowed by the absence of increased thickness
be unilateral or bilateral, temporal or perma- with inspiration, is suggestive of diaphrag-
nent, depending on the cause. matic paralysis.

The differential diagnosis of a diaphragmatic The snif test is conducted with short inspi-
elevation in an Xray includes a film when ratory efforts only through the nares. In a
inspiration is poor, obesity with decreased paralyzed diaphragm no motion is docu-
compliance, subpulmonary pleural effusion mented, or the diaphragm moves in cephalad
and pleural adhesions, subdiaphragmatic
direction instead of towards the transducer.
processes such as ascites, ileus and enlarged
This cephalad motion of the dome is exag-
organs, among others.
gerated by a snif test. The paradoxical dome
motion is an indication of unilateral dia-
In unilateral ascites, chest Xray sensitivity is
phragmatic paralysis. The snif test is positive
as high as 90%, while specificity is low
in more than 90% of patients with unilateral
(44%)9.
paralysis (Fig.  6B). However, bilateral dia-
phragmatic paralysis cannot be confirmed
In weakness of one or both hemidiaphragms,
with the assessment of the diaphragmatic
excursion is reduced (less than 20% of con-
dome motion.
traction fraction) or delayed in spontaneous
or deep inspiration 10. Also, there may be ex-
cursion limitation and greater thickness may With bilateral paralysis, the diaphragm moves
be associated; contrary to chronically para- caudally during inspiration. This caudal mo-
lyzed diaphragms, where thickness tends to tion is associated with two compensatory
be less than 2 mm4. strategies that individuals use to breathe: the
external intercostal muscles to actively inhale
It is important to repeat measurements, since or the abdominal muscles to passively inhale.
single measurements may lead to a false neg- The diaphragm can move caudally because
ative in acute paralysis cases where atrophy the subdiaphragmatic pressure becomes more
has not yet occurred or false positive in small negative.
individuals4.
If the bilateral diaphragmatic paralysis is con-
The patients with bilateral diaphragmatic pa- firmed, nocturnal hypoventilation evaluation
ralysis (Fig.  6A) may also have a normal should be considered1.

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Anales de Radiología México. 2023;22

A B

F igure   6. A: Diaphragmatic paralysis. Note the absence of respiratory movement of the right hemidiaphragm. B: the paradoxical
movement is associated to the use of accessory muscles and can be seen as an inversion of the respiratory cycle (yellow arrow).

Ventilator-induced diaphragmatic need to be reintubated within the next 48


dysfunction hours7.

It is considered crucially important for clini- Mechanical ventilation contributes to the


cians to be familiar with imaging strategies onset of diaphragmatic myopathy and
that may allow them to quickly and timely dysfunction due to diaphragm disuse.
change the treatment and prognosis of the Ventilator-induced diaphragmatic dysfunc-
patient, previously familiar with ventilator-in- tion is defined as a reduction in forced capac-
duced diaphragmatic dysfunction and diag- ity of the diaphragm and it is associated with
nostic imaging. a significant mortality increase, as well as
with the time that mechanical ventilation is
About 13% to 26% of patients that are extu- used, so it is important to identify the dys-
bated after a spontaneous respiration trial function and establish early management.

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A.P. Hernández-Morales et al.  Diaphragm. Anatomy and evaluation by ultrasound

Diaphragmatic dysfunction is associated to respiration test with the ventilator. The cutoff
fat atrophy and loss of myofibrils, and may value reported for extubation or failure is in
be evident after 24 to 26 hours after the initi- the range of 30% to 36% during a sponta-
ation of mechanical ventilation. The mecha- neous respiration trial11.
nisms that contribute to ventilator-induced
diaphragmatic dysfunction include activation The cutoff value for diaphragmatic dysfunc-
of proteolytic pathways, caspases and proteo- tion diagnosis using M mode, through
somes, as well as disturbances in mitochon- excursion, is 10-14 mm during a spontaneous
drial transport, resulting in an increase of respiration with mechanical ventilation11.
reactive oxygen species and oxidative stress1.

The assessment of diaphragmatic function CONCLUSIONS


with fluoroscopy, stimulation of the phrenic
nerve, magnetic resonance imaging and The key ultrasound findings for the diagnosis
transdiaphragmatic pressure measurement of diaphragmatic disease are morphologic
has certain limitations, such as exposure to and functional.
ionizing radiation, low availability, invasive-
ness and the need to transport the patient.10 Limitations for assessment are:
– Poor acoustic window.
There are two ultrasound diaphragmatic – Obesity.
predictors to successfully extubate a pa- – False negative findings in acute diaphrag-
tient: diaphragmatic excursion, measuring matic paralysis and false positive findings
the distance of the diaphragm during the re- in small individuals.
spiratory cycle and the fraction of diaphrag-
matic contraction, that reflects the thickness Experience is required for measurement of
variability during respiratory effort, as previ- functional parameters of the diaphragm to be
ously mentioned. able to help the clinician with certainty. When
excursion of the diaphragm is measured, the
The definition of «weaning failure» (extuba- radiologist must place the measuring line as
tion failure) is not standard, but it covers one perpendicular as possible to the diaphragm,
or more of the following points in the first since the accuracy and repetitivity of excur-
48-72 hours: need to reintubate, unscheduled sion may be affected.
non-invasive mechanical ventilation, death,
tracheostomy, terminal extubation, extuba- It must be taken into consideration that if the
tion delay or spontaneous respiration test fail- point is measured in excursion, and the patient
ure7. is in mechanical assist ventilation, the excur-
sion may represent the two forces exerted in
Contraction fraction has proved to be the the same direction: first, the contraction force
best estimator of muscular effort during itself, and secondly, the displacement of the
non-invasive mechanical ventilation, and pre- diaphragm due to the pressure applied with
dicts extubation failure during a spontaneous the ventilator. In this case, there is no way to

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Anales de Radiología México. 2023;22

tell what part of diaphragmatic displacement of their work site on the publication of pa-
is passive, due to the external force applied by tient data.
the ventilator, or active from the contraction
action as negative pressure is generated. If the Right to privacy and informed consent. The
goal is to assess diaphragmatic excursion authors have obtained informed consent from
without the assistance of the ventilator, a brief patients and/or subjects referred to in this
recording is necessary during spontaneous paper. This document is held by the corre-
respiration. Otherwise, the contraction and the sponding author.
motion of the diaphragm must be detected
during the patient-ventilator interaction.
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