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ULTRASONOGRAPHY
Abbreviations: DB ⫽ deep breathing; LS ⫽ left side; QB ⫽ quiet breathing; RS ⫽ right side; VS ⫽ voluntary sniffing
Various ultrasonographic methods, including changes echocardiograph (Mylab 30CV; Esaote; Genoa, Italy) connected
in diaphragm thickness during contraction,2,3 dia- to a 2.5 to 3.5 MHz transducer array. Subjects were investigated
in the morning, 2 or 3 hours after a light meal. Ultrasonographic
phragmatic motion recorded in two-dimensions4,5 or examinations were performed in the standing position. Two-
M-mode,6,7 and variation in the position of the dimensional mode was used to find the best approach and to
diaphragm relative to the kidney, have been pro- select the exploration line of each hemidiaphragm (Fig 1). The
posed.8 Diaphragmatic motion is readily assessed by liver was used as a window on the right (Fig 2), while the spleen
M-mode ultrasonography using a commercially avail- was used on the left hemidiaphragm (Fig 3). All examinations
were recorded on a personal computer for subsequent blind
able echocardiograph and has been used to assess analysis.
diaphragmatic function in patients after surgery or
high cervical spinal cord injury.9,10 Investigators have Right Hemidiaphragm Ultrasonographic Study
underlined its value. However, although the tech-
nique has been well described in pediatric patients,11 The probe was placed between the midclavicular and anterior
normal values for diaphragmatic excursion during axillary lines, in the subcostal area, and directed medially,
cranially, and dorsally, so that the ultrasound beam reached
different respiratory maneuvers and the reproduc- perpendicularly the posterior third of the right hemidiaphragm.
ibility of the methods remain poorly documented in
adult subjects. This prospective study was designed
to determine the reference values for diaphragmatic
amplitudes recorded by M-mode ultrasonography.
In addition, the intra- and inter-observer reproduc-
ibilities were assessed in a large population of
healthy adult subjects.
Variables Measured
Assessment of Reproducibility
Results
Initially, 236 healthy subjects were screened.
However, 26 subjects had lower spirometric param-
eters than normal and were excluded. In total, 210
subjects (150 men, 60 women, 50 ⫾ 14 years) were
investigated (Table 1). Their pulmonary function
tests were normal 关FVC ⫽ 3.6 ⫾ 1 (100 ⫾ 13% of
predicted), FEV1 ⫽ 3.1 ⫾ 0.9 L (95 ⫾ 11% of pre-
dicted), FEV1/FVC ⫽ 87 ⫾ 7%兴.
Right and left diaphragmatic motions were suc-
cessfully accomplished during QB in the whole
Figure 4. Measurements were performed during QB (top, 1), population. Mean excursions were measured to
VS (center, 2), and DB (bottom, 3). 1.8 ⫾ 0.3 cm on the right side (RS) and 1.8 ⫾ 0.4 cm
Table 2—Right Diaphragmatic Excursions and Limit Values in Men and Women*
population. Although complete motion could be plots12 both between and within observers. Normal
assessed in most cases during DB, the descending limit values were, therefore, established from these
lung masked the ultrasonographic images and im- measurements. To our knowledge, this is the largest
peded the measurement of the total diaphragmatic study concerning reference values of diaphragmatic
excursion in some subjects. In these circumstances, motion recorded by M-mode ultrasonography. To
the probe could be displaced caudally with an angle define the normal value in a subject, gender should
adjustment to maintain a perpendicular approach of be taken into account. Indeed, in our study, men
the right hemidiaphragmatic motion. This some- exhibited larger excursion than women in all the
times improved the recording of the complete ex- maneuvers studied.
cursion. Overall, the right diaphragmatic motion From our results, the lower limit of diaphragmatic
during DB could be measured in 93% of cases. This excursion during QB was estimated to be 0.9 cm in
high rate of success would be reduced if the study
women and 1 cm in men. These values were com-
had included patients with respiratory disease. In-
parable to those of studies using fluoroscopy14 or
deed, increased respiratory effort can result in
ultrasonographic methods.5,15
greater chest wall movement and cause the ribs and
lung to obscure the images in patients with dyspnea. VS has been described to be of value for the
In patients referred for pulmonary function test- diagnosis of diaphragmatic paralysis. A paradoxical
ing, Scott et al8 showed a 28% failure rate in movement has been observed on the paralyzed side
attempting an ultrasonographic scan of the right using fluoroscopy or ultrasonography.10 In our sub-
hemidiaphragm. jects, sniffing led to a sharp downstroke of the
Visualization of the left hemidiaphragm is recog- hemidiaphragm. Mean excursion was measured
nized as more difficult due to the smaller window of around 2.5 to 3 cm on both sides and lower limit
the spleen as compared with the liver window. values to 1.6 cm in women and 1.8 cm in men. To
However, in our healthy subject population, the left our knowledge, these values have not been assessed
hemidiaphragm was always seen and the motion previously and may be of use in the diagnosis of
during QB could be measured systematically. During diaphragmatic paresis.
VS, motion could be measured in most cases. On the A wide range of excursion was recorded during
other hand, the left hemidiaphragm was frequently DB. In a previous study of 64 healthy subjects,
obscured by the expanding lung during DB. The Kantarci et al7 assessed the diaphragmatic motion on
position of the probe could not be readily adjusted as both sides during deep DB and measured an excur-
the spleen window is small. In total, the diaphrag- sion ranging from 2.5 to 8.4 cm on the RS and from
matic motion of the left hemidiaphragm was only 2.4 to 8.1 cm on the LS. In our study, the mean
recorded in 45 of 210 subjects (21%). Gersovich13 diaphragmatic excursion was 6 to 7 cm, close to the
failed to record left hemidiaphragm excursion in 15 values measured by Cohen et al16 (6 ⫾ 0.7 cm) and
of their 23 volunteers (65%). In this study, the lack of Targhetta et al6 (6.8 ⫾ 0.8 cm). Finally, the lower
visualization of the excursion was observed in sub- limit values were estimated to be 4.7 and 3.6 cm on
jects with the greater range of excursion (⬎ 5 cm). In the RS and 5.6 and 4.3 cm on the LS for men and
our experience, during DB, part of the left hemidia- women, respectively.
phragmatic excursion could be visualized, but the A sex-difference has been noted in several studies.
lung frequently masked the dome. In the event of It was linked to the relation between diaphragmatic
hemidiaphragmatic paresis, recording of weak excur- excursion and weight and height.7,17 These observa-
sion should not be impeded by this phenomenon. tions were confirmed in our study; indeed height and
The present study demonstrated that both left and weight were found to affect the diaphragmatic mo-
right diaphragmatic excursion measurements per- tion. A weak correlation between diaphragmatic excur-
formed by M-mode ultrasonography were reproduc- sion and inspiratory or expiratory volumes was also
ible. High correlation coefficients and small mean observed. Cohen et al16 and Houston et al18 noted a
differences were observed in the Bland-Altman linear relationship between diaphragmatic excursion
and inspired volumes. In contrast, Scott et al8 stated variability as defined by the right-to-left ratio of
that measuring diaphragm movement by ultrasonog- maximal excursion on DB. They considered that a
raphy during QB and forceful maneuvers provided a measurement lying outside the range of 0.5 to 1.6
poor reflection of static and dynamic measures of should be considered to be abnormal. In our study,
pulmonary function. Several factors could explain the mean ratio was near unity for QB, VS, and DB.
these discrepancies. Diaphragmatic motion contrib- A ratio outside these limits was observed in some
utes to three fourths and thoracic expansion to one subjects during QB or VS. However, no healthy
fourth of the inspiratory volumes at the vital capacity. volunteer presented an abnormal ratio for both
Consequently, various inspiratory volumes may have maneuvers. The ratio always fell between normal
been measured for the same diaphragmatic excur- limits when right and left diaphragmatic excursions
sion. Furthermore, diaphragmatic motion could be were compared during DB. In line with studies using
affected by the examination position of the subjects. fluoroscopy or two-dimensional ultrasonography, our
In the study by Houston et al,18 the relation between observations confirm the interest of the comparison
inspired volume and hemidiaphragmatic movement between the two sides and the strong suspicion of
was better in the supine than in the sitting position. abnormal motion in the event of a right-to-left ratio
In total, the weak correlation between diaphragmatic of hemidiaphragmatic excursion outside these limits.
excursion and inspiratory volumes in our subjects Studies using fluoroscopy or MRI have shown that
was not unexpected, as the inspiratory volumes diaphragmatic motion depends somewhat on the
depended on several parameters including diaphrag- position of the subject. Our results concern the
matic motion and also rib thoracic expansion and diaphragmatic motion of healthy subjects solely in
abdominal and thoracic compliance. the erect position. Despite this limitation, it has
The relevance of the side-to-side diaphragmatic been demonstrated that diaphragmatic excursion is
motion comparison has been noted in fluoroscopy greater in the supine position than in the sitting or
studies.19 Using real time ultrasonography, Houston the standing positions.20 Consequently, in the event
et al5 determined a normal range of side-to-side of a recording of an excursion lower than our limit
values, an impairment of diaphragmatic motion 3 Gottesman E, Mc Cool FD. Ultrasound evaluation of the
should be suspected, irrespective of position. paralyzed diaphragm. Am J Respir Crit Care Med 1997;
155:1570 –1574
4 Fedullo AJ, Lerner RM, Gibson J, et al. Sonographic mea-
surement of diaphragmatic motion after coronary artery
References bypass surgery. Chest 1992; 102:1683–1686
1 Houston JG, Fleet M, Cowan MD, et al. Comparison of 5 Houston JG, Morris AD, Howie CA, et al. Technical report:
ultrasound with fluoroscopy in the assessment of suspected quantitative assessment of diaphragmatic movement: a repro-
hemidiaphragmatic movement abnormality. Clin Radiol ducible method using ultrasound. Clin Radiol 1992; 46:405–
1995; 50:95–98 407
2 Ueki J, De Bruin PF, Pride NB. In vivo assessment of 6 Targhetta R, Chavagneux R, Ayoub J, et al. Cinétique dia-
diaphragm contraction by ultrasound in normal subjects. phragmatique droite mesurée par ultrasonographie en mode
Thorax 1995; 50:1157–1161 TM avec spirométrie concomitante chez le sujet normal et