Diaphragm sniff ultrasound: Normal values, relationship with sniff nasal pressure and accuracy for predicting respiratory involvement in patients with neuromuscular disorders
Diaphragm sniff ultrasound: Normal values, relationship with sniff nasal pressure and accuracy for predicting respiratory involvement in patients with neuromuscular disorders
Abdallah FayssoilID 0 2
Lee S. NguyenID 1 2
Adam Ogna 0 2
Tanya Stojkovic 2
Paris Meng 0 2
Dominique Mompoint 2
Robert Carlier 2
Helene Prigent 2
Bernard Clair 0 2
Anthony Behin 2
Pascal Laforet 2
Guillaume Bassez 2
Pascal Crenn 2
David Orlikowski 0 2
Djillali Annane 0 2
Bruno Eymard 2
Frederic Lofaso 2
0 Service de R e ?animation m e ?dicale et unit e ? de ventilation a? domicile , CHU Raymond Poincare ? , APHP , Universit e ? de Versailles Saint Quentin en Yvelines, Garches, France, 2 Institut de Myologie, AP-HP, centre de r e ?f e ?rence des maladies neuromusculaires Nord/Est/Ile-de-France, G-H Piti e ? Salp e ?trie?re , Paris , France
1 Center of Clinical Investigation Paris-Est , Piti e ? Salpetrie?re, APHP, ICAN, Sorbonne Universite ? , Paris, France, 4 Service de Radiologie, CHU Raymond Poincar e ?, APHP , Universite ? de Versailles Saint Quentin en Yvelines, Garches, France, 5 Service de Physiologie-Explorations fonctionnelles , CHU Raymond Poincar e ?, APHP , Universit e ? de Versailles saint Quentin en Yvelines, Garches, France, 6 Service de Neurologie , CHU Raymond Poincar e ?, APHP , Universit e ? de Versailles Saint Quentin en Yvelines, Garches, France, 7 Service de m e ?decine aigue , CHU Raymond Poincar e ?, APHP , Universit e ? de Versailles Saint Quentin en Yvelines, Garches, France, 8 Centre d'Investigation clinique et Innovation technologique CIC 14.29, INSERM , Garches , France
2 Editor: Giuseppe Biagini, University of Modena and Reggio Emilia , ITALY
Data Availability Statement: All relevant data are
within the paper.
Funding: The author received no specific funding
for this work.
Competing interests: The authors have declared
that no competing interests exist.
In patients with neuromuscular disorders, assessment of respiratory function relies on forced
vital capacity (FVC) measurements. Providing complementary respiratory outcomes may be
useful for clinical trials. Diaphragm sniff ultrasound (US) is a noninvasive technique that can
assess diaphragm function that may be affected in patients with neuromuscular disorders.
We aimed to provide normal values of sniff diaphragm ultrasound, to assess the relationship
between sniff diaphragm US, vital capacity (VC) and sniff nasal pressure. Additionally, we
aimed to evaluate the diagnostic accuracy of sniff diaphragm US for predicting restrictive
Materials and methods
We included patients with neuromuscular disorders that had been tested with a sniff
diaphragm US and functional respiratory tests. Healthy subjects were also included to obtain
normal diaphragm sniff ultrasound. We performed diaphragm tissue Doppler imaging (TDI)
and time movement (TM) diaphragm echography combined with sniff maneuver.
A total of 89 patients with neuromuscular diseases and 27 healthy subjects were included in
our study. In patients, the median age was 32 years [25; 50] and the median FVC was 34% of
predicted [18; 55]. Sniff diaphragm motion using TM ultrasound was significantly associated
with sniff nasal pressure, both for the right hemidiaphragm (r = 0.6 p <0.0001) and the left
hemidiaphragm (r = 0.63 p = 0.0008). Right sniff peak TDI velocity was also significantly
associated with FVC (r = 0.72, p<0.0001) and with sniff nasal pressure (r = 0.66 p<0.0001). Sniff
diaphragm ultrasound using either TM mode or TDI displayed significant accuracy for
predicting FVC<60% with an area under curve (AUC) reaching 0.93 (p<0.0001) for the right sniff
diaphragm ultrasound in TM mode and 0.86 (p<0.001) for right peak diaphragm TDI velocity.
Sniff diaphragm TM and TDI measures were significantly associated with sniff nasal
pressure. Sniff diaphragm TM and TDI had a high level of accuracy to reveal respiratory
involvement in patients with neuromuscular disorders. This technique is useful to assess and follow
up diaphragm function in patients with neuromuscular disorders. It may be used as a
respiratory outcome for clinical trials.
Respiratory and cardiac failures are the main causes of morbidity and mortality in patients with
neuromuscular disorders. Assessment and monitoring of respiratory function relies on
functional pulmonary tests. Forced vital capacity (FVC) is used as an indicator of global respiratory
function. However, vital capacity (VC) is a late indicator of respiratory muscle involvement in
neuromuscular disorders since VC may be normal until a significant decrease in respiratory
muscle strength occurs [
]. Sniff nasal pressure and maximal inspiratory pressures, tests used to
assess inspiratory muscle strength, may be affected despite a normal FVC [
complementary respiratory outcomes may be useful for clinical trials. Among the respiratory
muscles, the diaphragm is the main inspiratory muscle. Its assessment classically relies on a
transdiaphragmatic pressure measurement. Since this test is invasive and not comfortable, it cannot
be used routinely. Recent research has focused on ultrasound to noninvasively assess diaphragm
muscle function [
4, 5, 6
]. Other techniques have been suggested to assess respiratory muscle
function. These techniques include a ratio of maximal expiratory and inspiratory pressures
(PEmax/PImax)  and the maximum relaxation rate (MRR) of inspiratory muscles [
Diaphragm function can be assessed using ultrasound at rest, during deep inspiration or during a
sniff maneuver [
]. However, this technique is limited in the assessment of the left diaphragm
during deep inspiration, due to loss of the ultrasound picture of the left diaphragm during deep
inspiration. Sniff is a physiological maneuver that is used during fluoroscopy for the assessment
of diaphragm function [
], it can be used to investigate motion of the right and left diaphragm,
and it can be coupled with ultrasound. Additionally, in cardiology, tissue Doppler imaging
(TDI) is used to assess subclinical myocardial impairment [
]. Diaphragm sniff ultrasound
may be affected earlier in patients with neuromuscular disorders. Little is known about the
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potential application of this technique in diaphragm muscle analysis. A subset of patients with
muscular dystrophy may have subclinical diaphragm impairment with normal VC values.
In this study, we aimed to complete the following:
- To provide normal values for diaphragm peak sniff velocity using TDI and sniff diaphragm
motion using time movement (M mode) ultrasound.
- To evaluate the relationship between diaphragm sniff ultrasound and sniff nasal pressure,
as well as the relationship between sniff ultrasound and FVC.
- To determine whether peak TDI velocities may be reduced in neuromuscular patients with
- To assess the diagnostic accuracy of diaphragm sniff TDI and sniff M mode ultrasound for
predicting impairment of respiratory muscles among patients with neuromuscular disorders.
Materials and methods
We retrospectively included patients with neuromuscular disorders followed at Raymond
Poincare hospital, a tertiary neuromuscular reference center specialized in the cardiac and
pulmonary management of patients with neuromuscular disorders. We included patients who
benefited from a sniff diaphragm ultrasound (right and/or left) and we recorded the functional
respiratory tests available that included sniff nasal pressure and/or FVC. Diaphragmatic
ultrasound was performed in patients with echocardiography, by the same operator (AF).
We recorded the following parameters from the medical records: age, sex, body mass index
(BMI), type of disease, peripheral skeletal muscle insufficiency (Walton score), cardiac drugs,
steroids, left ventricular ejection fraction (LVEF), history of documented sleep apnea (from polygraphy
or polysomnography), functional lung tests that included forced FVC, decubitus FVC, forced
expiratory volume in one second (FEV1), inspiratory capacity (IC), expiratory residual volume (ERV),
maximal inspiratory pressure (MIP), maximal expiratory pressure (MEP), sniff nasal pressure and
arterial partial carbon dioxide pressure (PaCO2). The study was performed in compliance with the
ethical principles formulated in the Declaration of Helsinki and was approved by the French
National Agency regulating Data Protection (commission nationale de l'informatique et des libert?s).
All data were fully anonymized before analysis. We also included a healthy control group that
underwent diaphragm ultrasound imaging, to obtain reference diaphragm ultrasound sniff values.
Lung function tests
Pulmonary function testing was performed in all patients as a part of the routine evaluation,
including spirometry that was performed according to ATS/ERS recommendations[
a Vmax 229 Sensormedics System (Yorba Linda, CA, USA) with the patient in the upright
]. Measurements are expressed as percent of predicted values [
function and pressure measurements were performed by different experimental technicians
who worked in the same respiratory muscle laboratory.
Sniff nasal pressure and maximal inspiratory pressure and expiratory
Maximal inspiratory pressure (MIP) and sniff nasal pressure (SNIP) were both measured from
functional residual capacity (FRC) in a standard manner (sitting position) and maximal
expiratory pressure (MEP) measured from total lung capacity, according to previously described
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methods. MIP is an isometric maneuver, while SNIP is a quasi-isometric maneuver [
MIP was measured with a flanged mouthpiece with the maneuvers repeated at least four times
or until two identical readings were obtained . SNIP was measured during at least 10 and
up to a maximum of 20 sniffs in a standard manner according to previously described methods
]. Briefly, the plug used to obstruct the nostril was an eartip usually used for auditory evoked
potentials (Eartips, 13 mm, Nicolet, Madison, WI). This plug was connected to a pressure
transducer via a catheter (see below). The length of this catheter was reduced to the minimum
length possible. Air leak was detected by obstructing the other nostril during an inspiratory
maneuver and when present it was eliminated by adding waxed earplug material. Detailed
instruction on how to perform the sniff maneuver was not necessary and may be
]. Patients were vigorously coached during the test maneuvers.
All pressure signals were measured using a differential pressure transducer (Validyne,
Northridge, CA), amplified by a carrier amplifier (Validyne), and passed through an
analogdigital board to a computer running Acqknowledge software (Biopac System, Santa Barbara,
CA) which allows visual feedback to improve the sniff efficiency. The signal was digitized at
100 Hz. Subjects received strong verbal encouragement with visual feedback, as previous
studies have suggested [
]. Values of MIP, MEP and SNIP were expressed in cmH2O.
Diaphragm ultrasound technique
Diaphragm ultrasound was performed in the supine position by the same operator (AF), who
was blinded to the pulmonary function tests. We used the liver window for the right
hemidiaphragm analysis and the spleen window for the left hemidiaphragm analysis. The
transducer was placed in the anterior subcostal region between the midclavicular and anterior
axillary lines so that the ultrasound beam reached the posterior part of the diaphragm. After
visualization of the diaphragm, an M mode was applied perpendicularly to the hemidiaphragm
to measure diaphragm motion during inspiration and during a sniff maneuver. Patients were
in a semirecumbent position (45?) during the procedure. In normal subjects, the normal
inspiratory motion is caudal and the operator recorded the M mode trace moving upward
(diaphragm moving toward the probe). With the sniff maneuver, the operator recorded a sharp
upstroke in the normal situation due to the high speed of diaphragm movement (Fig 1). For
Fig 1. Diaphragm ultrasound displacement from the subcostal view in a control subject and in a DMD patient. Normal right diaphragm sniff
time movement (TM) motion in the control group (left); note the sharp upstroke during a sniff maneuver. Pathological right diaphragm motion
during a sniff maneuver in a DMD patient (right). Note the reduced diaphragm motion with the sniff maneuver. DMD: Duchenne muscular
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sniff peak diaphragm TDI recording, we used the liver window or the spleen window. Using a
cardiac probe, we activated the tissue Doppler imaging modality with the beam positioned
perpendicular to the diaphragm motion; then, we recorded the peak sniff inspiratory velocity
(cm/s) (Figs 2 and 3). Diaphragm thickness was also recorded from the apposition zone
ultrasound, using a linear probe positioned in the midaxillary line perpendicular to the chest wall.
Thickness was measured at the end of a quiet expiration.
Continuous variables are reported as the median ? interquartile range [IQR] and compared
using nonparametric tests due to their distribution; categorical variables are described by
number of subjects and percentage and compared by Fisher?s exact test. Spearman correlations
were performed to evaluate associations between continuous variables. Discrimination
performances of sniff M mode and sniff TDI regarding FVC<60% and FVC<30% were assessed
using receiver-operator characteristic (ROC) analyses, and corresponding ROC curves were
drawn. C-statistics corresponded to the areas under corresponding ROC curves. Figures were
created and statistical analyses were performed using GraphPad Prism (GraphPad Software,
Inc., State of California, USA).
Clinical and respiratory functional tests and diaphragm ultrasound
A total of 89 patients with genetically confirmed neuromuscular diseases were included in our
study (35% Duchenne muscular dystrophy (DMD), 29% myotonic dystrophy type 1, 12%
sarcoglycanopathies). The median age was 32 years [25; 50] and the median BMI was 22 kg/m2.
Fig 2. Sniff right hemidiaphragm tissue Doppler imaging peak velocity (arrow) in a volunteer (peak velocity = 12
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Fig 3. Pathological right hemidiaphragm peak tissue Doppler imaging velocity during a sniff maneuver in a DMD
patient. Note the reduced peak sniff diaphragm TDI velocity (arrow).
In this sample, 57% of patients were wheelchair bound. Patients disclosed a restrictive
respiratory insufficiency pattern with a median FVC of 34% of predicted [18; 55]. In total, 63% of
patients were on home mechanical ventilation (HMV). Inspiratory muscles were affected as
attested by a median inspiratory capacity (IC) of 59% of predicted [16; 74], a median MIP of
22 cmH20 [14; 32] and a median sniff nasal pressure of 22 cmH20 [14;32]. Diaphragm
ultrasound parameters were significantly reduced in patients. Table 1 summarizes the clinical and
respiratory data in the patients. Table 2 summarizes the diaphragm ultrasound data in the
patients vs the control group.
Relationship between sniff ultrasound and sniff nasal pressure
Diaphragm sniff time movement (TM) ultrasound motion was significantly associated with
sniff nasal pressure, both for the right hemidiaphragm (r = 0.6 p <0.0001) and the left
hemidiaphragm (r = 0.63 p = 0.0008) (Fig 4). Indeed, diaphragm peak sniff TDI velocities were
significantly associated with sniff nasal pressure (Fig 5).
Relationship between diaphragm sniff ultrasound and forced vital capacity
Using the global respiratory function assessment, diaphragm sniff ultrasound TM motion was
significantly associated with FVC. This finding involved the right hemidiaphragm as well as
the left hemidiaphragm (Figs 6 and 7). We also compared sniff M mode with FVC expressed
in ml and observed a similar relationship to FVC expressed in %, which takes into account
height (Fig 8).
Right sniff peak TDI was also significantly associated with FVC (r = 0.72, p<0.0001) (Fig
9). Supine FVC was also significantly associated with sniff diaphragm right TM motion
(r = 0.59, p = 0.0003, n = 34). Additionally, Supine FVC was significantly associated with right
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diaphragm sniff TDI velocity (r = 0.59, p = 0.0007, n = 29). The level of the relationship
between the sniff diaphragm TM motion and FVC remained similar in patients with DMD vs
patients with DM1 vs patients with other myopathies (Fig 10).
Sniff diaphragm TDI velocities and TM motion in patients with FVC>80%
Figs 6, 7 and 9 provide an overview of the distribution of the right sniff TM motion and the
right sniff peak TDI velocity in patients with FVC>80%. Among those with FVC>80%, 5
(83.3%) patients had a right diaphragm sniff TM motion under the median value obtained in
controls. In patients with FVC>80%, 3 (60%) patients a had right sniff TDI peak velocity
under the median right diaphragm sniff TDI peak velocity obtained in the control group.
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Control group (N = 27)
Data are presented as number (percentage) or median [IQR]
F: female; BMI: body mass index; TM: time movement; TDI: tissue Doppler imaging.
: at rest. p = p value.
Accuracy of sniff ultrasound for the prediction of respiratory muscle
impairment in patients with muscular dystrophy
Using receiver operating characteristic (ROC) curves, sniff diaphragm ultrasound using either
TM mode or TDI accurately discriminated those with FVC<60%; the area under the curve
(AUC) reached 0.93 (p<0.0001) for the sniff right TM mode diaphragm ultrasound and 0.86
(p<0.001) for right peak diaphragm TDI velocity. In patients with significant respiratory
insufficiency (FVC<30%), the AUC remained high but with a slight decrease in the AUC of
the right diaphragm ultrasound TDI (0.76, p<0.017). The M mode right diaphragm motion
value cutoff to predict a FVC<60% was 25 mm with a sensitivity of 100% and a specificity of
64%. The M mode right diaphragm motion value cutoff to predict a FVC<30% was 10.5 mm
with a sensitivity of 84% and a specificity of 84%.
Fig 4. Relationship between right diaphragm sniff TM motion and sniff nasal pressure in patients (A), and the relationship between left
diaphragm sniff TM motion and sniff nasal pressure in patients (B). TM = time movement; Sniff TM mode = Sniff TM motion.
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Fig 5. Relationship between right diaphragm sniff peak TDI velocity and sniff nasal pressure in patients. Sniff TDI
peak inspi = sniff peak diaphragm tissue Doppler imaging velocity.
Fig 6. Relationship between right sniff TM mode and FVC in patients. FVC: forced vital capacity (%).
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Fig 7. Relationship between left sniff TM mode and FVC in patients. FVC: forced vital capacity (%).
Fig 9. Relationship between right sniff TDI peak velocity (cm/s) and FVC in patients. FVC = forced vital capacity
Fig 10. Relationship between right sniff diaphragm TM motion and FVC in DMD. DM1 and other myopathies.
DMD = Duchenne muscular dystrophy; DM1 = myotonic dystrophy type I; others = other myopathies; FVC = forced
vital capacity (%); sniff M mode = right sniff diaphragm time movement motion (mm).
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The right peak TDI velocity value cutoff to predict a FVC<60% was 7.5 cm/s with a
sensitivity of 84% and a specificity of 89%. The right peak TDI velocity value cutoff to predict a
FVC<30% was 6.5 cm/s with a sensitivity of 90% and a specificity of 56%. Figs 11 and 12
show the ROC curves of the sniff diaphragm ultrasound for predicting FVC<60% and for
predicting FVC<30%, respectively.
In the present study, we describe for the first time the diaphragmatic sniff ultrasound pattern
in patients with muscular dystrophy, investigating the relationship between sniff diaphragm
ultrasound and sniff nasal pressure as well as the relationship with FVC. We also report the
accuracy of sniff diaphragm ultrasound for predicting moderate and/or severe respiratory
muscle impairment. The main findings are the following:
- Sniff diaphragm ultrasound motion using TM mode was significantly reduced in patients
with myopathies and was correlated with FVC and sniff nasal pressure.
- Sniff peak diaphragm ultrasound TDI velocity was significantly reduced in patients with
myopathies and was correlated with FVC and sniff nasal pressure.
Fig 11. ROC (receiver operating characteristic) curves for predicting a FVC<60% in patients with neuromuscular disorders. TDI right: peak
sniff TDI velocity (cm/s) at the right hemidiaphragm; M mode left: left diaphragm motion during a sniff maneuver (mm); M mode right: right
diaphragm motion during a sniff maneuver (mm); FVC = forced vital capacity (%).
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Fig 12. ROC curves for predicting a FVC <30% in patients with neuromuscular disorders. M mode right: right diaphragm motion during a sniff
maneuver; M mode left: left diaphragm motion during sniff maneuver (mm); TDI right: peak sniff TDI velocity (cm/s) recorded at the right
hemidiaphragm; FVC: forced vital capacity (%).
Diaphragm peak sniff TDI velocities and diaphragm sniff TM motion may be impaired in
patients even with FVC>80%.
Lung volumes in patients with neuromuscular disorders are affected by weakness of the
respiratory muscles [
], and FVC provides a global evaluation of respiratory muscle function.
In patients with NMD, the classic pattern of restriction is a reduction of FVC [
]. FRC may
be normal or decreased, and RV may increase [
]. In our study, FVC was significantly
associated with sniff diaphragm ultrasound. Interestingly, we found that sniff diaphragm ultrasound
may predict restrictive impairment in patients with muscular dystrophy and was associated
with sniff nasal pressures. Classically, MIP and sniff nasal pressures have been used to assess
inspiratory muscle strength in respiratory laboratories [
]. Low values may be due to muscle
failure, however, they may also be due to a lack of motivation, lack of coordination, peribuccal
leaks and fatigue [
]. The sniff test is a natural effort maneuver that solves leak problems,
reduces the risk of fatigue and can be combined with diaphragm ultrasound. However, the
sniff value can be underestimated in cases of nasal obstruction [
]. Our data support the fact
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that sniff TDI can be used to detect early subclinical diaphragm involvement in patients with
neuromuscular diseases. Indeed, the usefulness of TDI is to depict early muscle involvement in
a pathological setting. Similar to the way TDI is used in cardiology to detect early
myocardiopathy before the onset of a reduced ejection fraction [
], TDI may be used in pneumology
and combined with sniff maneuver to detect early muscle involvement in myopathy before the
onset of reduced FVC. In the early stages of diaphragm involvement, FVC remains normal,
since FVC is a late marker of respiratory muscle involvement. In our study, in the control
group, the median normal peak sniff TDI was 13 cm/s for the right hemidiaphragm and 12
cm/s for the left hemidiaphragm, and some patients had a reduced peak sniff TDI velocity, and
at the same time, had a forced VC that was in the normal range. These findings are interesting
since they could prompt monitoring in patients with abnormal sniff TDI. Patients with
neuromuscular disorders presenting abnormal diaphragm peak TDI velocity may benefit from close
pulmonary test monitoring. In normal subjects, during the sniff maneuver, inspiratory
muscles are short at higher speed, and the pressure measured in the esophagus is closely related to
the pressure in the mouth, nasopharynx and nose [
]. Heritier et al[
] reported an excellent
correlation between sniff nasal pressure and sniff esophageal pressure (r 0.99, p<0.001).
Diaphragm ultrasound emerged recently in the literature as a noninvasive method to assess
diaphragm function [
]. Our data in the control group regarding sniff TM diaphragm
motion were similar, even higher than the data reported by Boussuges et al , 16 mm in
women and 18 mm in men [
]. Various factors (sex and height) may influence normal
diaphragm ultrasound, as reported by Scarlata et al [
]. In our study, we also compared sniff M
mode with FVC expressed in ml and observed a similar relationship to FVC expressed in %,
which takes into account height. No data have been reported regarding sniff diaphragm TDI
velocities in the literature. In our study, the correlation between peak sniff TDI velocity and
sniff nasal pressure was high (r = 0.66 p<0.0001) but was relatively reduced in comparison
with the correlation between sniff esophageal pressure and sniff nasal pressure reported by
Heritier et al [
](r = 0.99). This discrepancy may be explained by the fact that the peak sniff
TDI velocity recorded the contribution of one side of the diaphragm and the peak velocity
may be influenced by the pressure interactions between the chest and abdomen, the geometry
and pattern of the ribcage. Moreover, the sniff maneuver used during ultrasound was different
from the method used in pulmonary laboratories since the patient has two nostrils open
during diaphragm sniff ultrasound examinations. Finally, the AUC for sniff diaphragm ultrasound
using TDI or TM mode was significantly high for predicting FVC <60% and/or FVC<30%.
However, in patients with FVC<30%, the sniff right TDI velocity displayed a lower AUC
(0.76, p 0.017), in comparison with sniff right TM mode diaphragm displacement (AUC 0.86,
p<0.0001). This difference can be explained by the lower TDI velocity recorded for the
diaphragm with sniff, which sometimes rendered the recording curve analysis difficult.
The assessment and monitoring of diaphragm function requires dedicated equipment and
specialized techniques, which are not available in all centers. A single sniff diaphragm ultrasound
measuring using TDI or TM mode can help physicians detect patients with asymptomatic
restrictive pulmonary insufficiency and early diaphragm involvement in patients with
neuromuscular disorders. Diaphragm sniff TDI may be used as a presymptomatic test to reveal early
diaphragm involvement in patients with neuromuscular disorders. These findings may help
clinicians select patients for regular respiratory test evaluation during follow-up, particularly
in patients with TDI velocity impairment. Our study provided normal sniff diaphragm
ultrasound values. These findings can be used as reference values for other studies in the
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neuromuscular field. Sniff diaphragm ultrasound can be used as a screening test and could be
used as a monitoring tool for future biotherapy assessment. In patients with significant
respiratory insufficiency, it would be appropriate to focus on the right TM mode technique for
monitoring patients. Finally, studies that assess economic performance and nursing technical
requirements need to be performed with this new technique. In the future, this radiological
technique may be considered as an additional test in the arsenal of pulmonary exploratory
functional tests used in a multiparametric approach in the neuromuscular field.
This study is limited by its retrospective design. Additionally, sniff ultrasound is a volitional
test and data depend on patient motivation and fatigue. The other limitation relies on the
technical aspect of Doppler imaging. Indeed, velocity recorded with TDI depends on beam
angulation and the beam direction should be perpendicular to diaphragm displacement to obtain the
maximal TDI peak velocity. Moreover, patient position may affect respiratory function tests
]. Here, with US, patients were in a semirecumbent position (45?) that would amplify
diaphragm dysfunction and US measurements [
]. The supine position is preferred, because
there is less overall variability, less side-to-side variability, and greater reproducibility.
Additionally, diaphragm excursion is known to be greater in the supine position for the same
volume inspired than in the sitting or standing positions because the abdominal viscera more
easily moves the diaphragm in this position, and the relationship between inspired volume
and diaphragm movement has been shown to correlate better in the supine position than in
the sitting position. The supine position also exaggerates any paradoxical movement and limits
any compensatory active expiration by the anterior abdominal wall, which may mask paralysis
. According to Brown et al [
], intraobserver reliability was excellent (>0.93) for all body
positions tested. Because many of our patients were not able to maintain the strict supine
position for different reasons (e.g., tolerability), we systematically used the semirecumbent position
(45?). Nevertheless, despite the difference in position between respiratory function
measurements (90?) and diaphragmatic ultrasound measurements (45?), significant correlations were
observed. Moreover, we compared nasal pressure and diaphragm velocity and motion. These
latter measures depend on other factors that include abdominal pressure and compartment
and history of abdominal surgery, and we did not have esophageal pressure for the reference
method. Finally, nasal pressure does not necessarily reflect esophageal pressure in some
patients with neuromuscular disease due to the inability to generate a significant transnasal
Sniff diaphragm TM and TDI are significantly associated with sniff nasal pressure. Sniff
diaphragm TM and TDI had high accuracy for depicting respiratory involvement in patients with
neuromuscular disorders. This noninvasive diaphragm evaluation can reveal early diaphragm
involvement. These techniques are useful to assess and follow up diaphragm function in
patients with neuromuscular disorders and may be used as a respiratory outcome for clinical
Conceptualization: Abdallah Fayssoil, Bernard Clair.
Data curation: Abdallah Fayssoil, Paris Meng, Helene Prigent.
Formal analysis: Abdallah Fayssoil, Lee S. Nguyen, Pascal Laforet, Frederic Lofaso.
15 / 17
Investigation: Abdallah Fayssoil, Helene Prigent, Bernard Clair, Anthony Behin, Pascal
Laforet, David Orlikowski.
Methodology: Abdallah Fayssoil, Lee S. Nguyen, Tanya Stojkovic, Guillaume Bassez, David
Orlikowski, Djillali Annane, Bruno Eymard, Frederic Lofaso.
Resources: Dominique Mompoint, Robert Carlier, Anthony Behin, Pascal Crenn, Bruno
Validation: Abdallah Fayssoil.
Visualization: Dominique Mompoint, Robert Carlier, Helene Prigent, Bernard Clair, Pascal
Laforet, Guillaume Bassez, Pascal Crenn, David Orlikowski, Djillali Annane, Bruno
Eymard, Frederic Lofaso.
Writing ? original draft: Abdallah Fayssoil.
Writing ? review & editing: Abdallah Fayssoil, Adam Ogna, Tanya Stojkovic, Robert Carlier,
Bernard Clair, Anthony Behin, Pascal Laforet, Guillaume Bassez, David Orlikowski, Djillali
Annane, Frederic Lofaso.
16 / 17
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