Introduction
The diaphragm along with the myocardium is an almost continuously working muscle that is not in a state of complete rest. This explains significant oxygen consumption [1] and sensitivity to excessive or insufficient load [2]. Excessive and insufficient function makes a significant contribution to development/aggravation of certain diseases, for example, bronchial asthma, chronic obstructive pulmonary disease, heart failure, pneumonia, sepsis and abdominal diseases accompanied by intra-abdominal hypertension [3-7]. Quantitative assessment of diaphragm fucntion may be of interest regarding diagnosis of respiratory failure [8].
Ultrasound examination of the diaphragm is one of the objective diagnostic methods attracting more and more attention of clinicians [7, 9, 10]. This is confirmed by various reports over the past two years [11, 12]. Nevertheless, there are still no clear quantitative ultrasonic parameters of diaphragm function for healthy and ill people [7, 13]. Diaphragmatic ultrasound may be a useful diagnostic tool for resuscitators [7, 14, 15], for example, in weaning from respiratory support. ICU patients are on strict bed rest that explains the need to consider this aspect in establishing reference ultrasound indicators of diaphragm function in healthy and ill people.
The purpose of the study was to analyze ultrasound indicators of diaphragm performance in healthy persons under conditions close to that of being in intensive care unit.
Material and methods
A descriptive cohort study was performed at the Almazov National Medical Research Centre. We analyzed structural and functional state of external respiration in 50 healthy volunteers (30 women) in supine position. Age of patients was 25.1±3.6 years, body weight 67.9±14.5 kg, height 173.1±11.0 cm, body mass index 22.4±3.3 kg/m².
The study complied with the Helsinki Declaration (2000). Exclusion criteria were any diseases and states that could influence function of diaphragm.
We analyzed structural (thickness) and functional (thickening fraction and excursion of diaphragm) parameters under inhalation and exhalation using Philips CX50 ultrasound scanner (Philips Ultrasound, Inc., USA).
We measured thickness of diaphragm using a linear high-frequency transducer (7-15 MHz) in the apposition zone (transition of US image of lung tissue into the image of diaphragm and liver/spleen) (Fig. 1).
Fig. 1. Scheme of apposition zone.
We placed transducer along anterior axillary line in intercostal space X-XI and sought the point of the best image of diaphragm (Fig. 2). Scanning was carried out on both sides in M and B modes.
Fig. 2. Image of apposition zone.
Diaphragm excursion was assessed on both sides in M-mode. We sought the best image of diaphragm along the right middle clavicular line in subcostal space with cranial direction of transducer (Fig. 3). Excursion of diaphragm on the left was assessed along the anterior-midaxillary line. The best image of diaphragm was also sought in subcostal space with cranial direction of transducer (Fig. 4). The generally accepted orientation towards averages carries the risk of partial loss of information [16]. Therefore, we presented descriptive data as mean, minimum and maximum values presumably useful for excluding overdiagnosis of certain abnormalities [16].
Fig. 3. Diaphragm excursion on the right, M-mode.
Fig. 4. Diaphragm excursion on the left, M-mode.
Mathematical analysis of data was carried out using the STATISTICA-10 software and external analysis package Real Statistics Resource Pack supplementing standard capabilities of Microsoft Excel. After testing distribution normality, we used appropriate statistical criteria (t-test and Mann-Whitney test for Gaussian and non-Gaussian distributions, respectively). Results were presented as mean and standard deviation (M±SD), as well as median and quartiles (50 (25; 75)) in between-group comparisons. Differences were significant at p-value<0.05.
Results
Results of diaphragm sonography are presented in Tables 1–3 and they are consistent with literature data [17–24].
Table 1. Ultrasonic structural and functional indicators of diaphragm: thickness and thickening fraction (n=50), descriptive statistics
|
Variable |
M±SD |
Min |
Max |
Literature data |
|
T (calm inhalation) on the right, mm |
2.0±0.4 |
1.1 |
3.1 |
2.1±0.3 [18] |
|
T (calm exhalation) on the right, mm |
1.5±0.3 |
0.9 |
2.3 |
1.7±0.2 [20] 1.6±0.4 [19] |
|
T (deep inhalation) on the right, mm |
4.5±0.3 |
3.0 |
6.7 |
4.5±0.9 [20] |
|
T (deep exhalation) on the right, mm |
1.2±0.3 |
0.6 |
1.7 |
1.6±0.2 [20] |
|
T (calm inhalation) on the left, mm |
1.8±0.4 |
1.2 |
3.2 |
— |
|
T (calm exhalation) on the left, mm |
1.4±0.3 |
1.0 |
2.8 |
— |
|
T (deep inhalation) on the left, mm |
3.9±0.3 |
2.1 |
6.2 |
— |
|
T (deep exhalation) on the left, mm |
1.1±0.3 |
0.7 |
1.8 |
— |
|
TI (calm inhalation) on the right, % |
29.0±8.5 |
14.5 |
46.7 |
30±14 [18, 21] |
|
TI (deep inhalation) on the right, % |
205.7±70.1 |
47.2 |
377.2 |
— |
|
TI (calm inhalation) on the left, % |
26.2±8.9 |
15.3 |
45.8 |
30±14 [18, 21] |
|
TI (deep inhalation) on the left, % |
177.3±63.6 |
50.7 |
324.0 |
— |
Note. T — thickness; TI — thickening index.
Table 2. Ultrasonic structural and functional indicators of diaphragm excursion on the right (n=50), descriptive statistics
|
Variable |
M±SD |
Min |
Max |
Literature data |
|
Excursion (calm breathing), cm |
1.8±0.4 |
1.1 |
2.9 |
1.6±0.3 [22] |
|
Contraction time (calm breathing), s |
1.5±0.4 |
0.5 |
2.8 |
1.27±0.1 [25] |
|
Contraction rate (calm breathing), cm/s |
1.1±0.3 |
0.6 |
1.9 |
1.12±0.4 [25] |
|
Relaxation time (calm breathing), s |
1.5±0.4 |
0.5 |
2.6 |
1.8±0.3 [25] |
|
Relaxation rate (calm breathing), cm/s |
1.3±0.5 |
0.6 |
3.3 |
— |
|
Mean contraction time / mean relaxation time (calm breathing) |
1:1 (1.5±0.4:1.5±0.4) |
— |
— |
— |
|
Excursion (deep breathing), cm |
7.0±1.5 |
5.1 |
11.9 |
6.9±1.4 [25] |
|
Contraction time (deep breathing), s |
2.6±0.6 |
1.5 |
4.0 |
— |
|
Contraction rate (deep breathing), cm/s |
2.8±0.9 |
1.5 |
5.4 |
— |
|
Relaxation time (deep breathing), s |
2.6±0.9 |
1.1 |
6.1 |
1.5±0.4 [25] |
|
Relaxation rate (deep breathing), cm/s |
2.6±0.9 |
1.0 |
6.1 |
— |
|
Mean contraction time / mean relaxation time (deep breathing) |
1:1 (2.6:2.6) |
— |
— |
— |
Table 3. Ultrasonic structural and functional indicators of diaphragm excursion on the left (n=10), descriptive statistics
|
Variable |
M±SD |
Min |
Max |
Literature data |
|
Excursion (calm breathing), cm |
1.4±0.3 |
1.0 |
1.9 |
1.6±0.3 [22] |
|
Contraction time (calm breathing), s |
1.5±0.4 |
0.9 |
2.1 |
— |
|
Contraction rate (calm breathing), cm/s |
1.4±0.5 |
0.9 |
2.2 |
— |
|
Relaxation time (calm breathing), s |
1.3±0.5 |
0.8 |
2.0 |
1.8±0.3 [25] |
|
Relaxation rate (calm breathing), cm/s |
1.5±0.5 |
0.9 |
2.3 |
— |
|
Mean contraction time / mean relaxation time (calm breathing) |
1.1:1.0 (1.5:1.3) |
— |
— |
— |
|
Excursion (deep breathing), cm |
6.3±0.9 |
5.1 |
7.9 |
6.9±1.4 [25] |
|
Contraction time (deep breathing), s |
2.9±1.3 |
1.5 |
6.0 |
— |
|
Contraction rate (deep breathing), cm/s |
2.6±0.7 |
1.5 |
3.8 |
— |
|
Relaxation time (deep breathing), s |
2.6±0.9 |
1.6 |
4.5 |
1.5±0.4 [25] |
|
Relaxation rate (deep breathing), cm/s |
2.6±0.7 |
1.4 |
3.5 |
— |
|
Mean contraction time / mean relaxation time (deep breathing) |
1.1:1.0 (2.9:2.6) |
— |
— |
— |
Diaphragm excursion on the right and thickness on both sides were visualized in 100% (n=50) of subjects, while diaphragm excursion on the left was visualized only in 20% (n=10) of patients due to objective difficulties [7, 9, 20, 25].
Structural and functional indicators of diaphragm domes are presented in Table 4. We analyzed function of diaphragm domes only in subjects with bilateral imaging of excursion.
Table 4. Comparison of ultrasonic indicators of structural and functional state of the right and left domes of diaphragm (n=10)
|
Variable |
On the right 50 (25; 75) |
On the left 50 (25;75) |
p-value (Mann-Whitney test) |
|
T (calm inhalation), mm |
1.5 (1.4; 1.9) |
1.5 (1.2; 1.8) |
0.36 |
|
T (calm exhalation), mm |
1.2 (1.1; 1.5) |
1.2 (1.0; 1.4) |
0.57 |
|
T (deep inhalation), mm |
4.3 (3.6; 5.1) |
3.0 (2.9; 4.2) |
0.15 |
|
T (deep exhalation), mm |
1.0 (0.8; 1.3) |
0.8 (0.8;1.1) |
0.40 |
|
TI (calm inhalation), % |
28.5 (25.0; 33.6) |
22.6 (20.0; 28.5) |
0.18 |
|
TI (deep inhalation), % |
224.4 (180.0; 263.6) |
179.5 (153.8; 264.2) |
0.27 |
|
Excursion (calm breathing), cm |
1.7 (1.45; 1.8) |
1.4 (1.3; 1.2; 1.6) |
0.97 |
|
Contraction time (calm breathing), s |
1.4 (1.3; 1.5) |
1.5 (0.9; 1.8) |
0.47 |
|
Contraction rate (calm breathing), cm/s |
1.3 (1.1; 1.6) |
1.4 (0.8; 1.8) |
0.47 |
|
Relaxation time (calm breathing), s |
1.4 (1.2; 1.5) |
1.2 (0.9; 1.5) |
0.09 |
|
Relaxation rate (calm breathing), cm/s |
1.4 (1.1; 1.5) |
1.6 (1.0; 1.8) |
0.31 |
|
Excursion (deep breathing), cm |
7.0 (6.3; 7.4) |
6.5 (5.4; 7.0) |
0.91 |
|
Contraction time (deep breathing), s |
3.2 (2.2; 3.5) |
2.6 (2.0; 3.4) |
0.57 |
|
Contraction rate (deep breathing), cm/s |
2.5 (2.1; 2.9) |
2.7 (2.0; 3.0) |
0.31 |
|
Relaxation time (deep breathing), s |
2.6 (2.2; 3.0) |
2.4 (2.0; 2.8) |
0.19 |
|
Relaxation rate (deep breathing), cm/s |
3.0 (2.6; 3.5) |
2.9 (1.9; 3.2) |
0.68 |
According to Table 4, thickness and excursion of both domes were similar. Thus, our findings confirm literature data on advisable analysis of only the right phrenic dome [7, 17].
Considering certain data on gender-related differences in ultrasound characteristics of diaphragm function [4, 17, 19, 20, 26], we analyzed these parameters too (Table 5).
Table 5. Ultrasonic indicators depending on gender
|
Variable |
Men 50 (25; 75) |
Women 50 (25; 75) |
p-value (Mann-Whitney test) |
|
T (calm inhalation) on the right, mm |
2.0 (1.7; 2.3) |
1.8 (1.5; 2.1) |
0.12 |
|
T (calm exhalation) on the right, mm |
1.5 (1.4; 1.8) |
1.4 (1.2; 1.6) |
0.12 |
|
T (deep inhalation) on the right, mm |
4.8 (4.2; 5.4) |
4.2 (3.5; 4.9) |
0.02* |
|
T (deep exhalation) on the right, mm |
1.3 (1.2; 1.4) |
1.1 (0.9; 1.3) |
0.01* |
|
T (calm inhalation) on the left, mm |
2.0 (1.7; 2.2) |
1.7 (1.4; 1.8) |
0.006* |
|
T (calm exhalation) on the left, mm |
1.5 (1.4; 1.7) |
1.3 (1.2; 1.5) |
0.02* |
|
T (deep inhalation) on the left, mm |
3.7 (3.2; 5.0) |
3.6 (3.1; 4.3) |
0.23 |
|
T (deep exhalation) on the left, mm |
1.2 (1.0; 1.4) |
1.1 (0.9; 1.1) |
0.02* |
|
TI (calm inhalation) on the right, % |
28.2 (22.0; 33.0) |
28.4 (22.9; 36.3) |
0.43 |
|
TI (deep inhalation) on the right, % |
213.8 (146.1; 250.0) |
188.8 (155.1; 246.0) |
0.61 |
|
TI (calm inhalation) on the left, % |
28.0 (21.0; 38.6) |
22.2 (18.0; 28.5) |
0.03* |
|
TI (deep inhalation) on the left, % |
175.6 (121.0; 198.0) |
169.0 (145.0; 214.6) |
0.9 |
|
Excursion (calm breathing) on the right, cm |
1.7 (1.5; 2.0) |
1.6 (1.5; 1.9) |
0.29 |
|
Contraction time (calm breathing) on the right, s |
1.5 (1.3; 1.9) |
1.3 (1.2; 1.7) |
0.01* |
|
Contraction rate (calm breathing) on the right, cm/s |
1.0 (0.9; 1.3) |
1.0 (0.9; 1.4) |
0.59 |
|
Relaxation time (calm breathing) on the right, s |
1.4 (1.3; 1.6) |
1.34 (1.15; 1.6) |
0.01* |
|
Relaxation rate (calm breathing) on the right, cm/s |
1.1 (0.9; 1.5) |
1.1 (0.9; 1.7) |
0.89 |
|
Excursion (deep breathing) on the right, cm |
7.4 (6.3; 8.2) |
6.6 (5.7; 7.5) |
0.04* |
|
Contraction time (deep breathing) on the right, s |
2.5 (2.2; 2.8) |
2.5 (2.1; 3.2) |
0.47 |
|
Contraction rate (deep breathing) on the right, cm/s |
2.8 (2.5; 3.5) |
2.5 (2.0; 3.0) |
0.057 |
|
Relaxation time (deep breathing) on the right, s |
2.5 (2.0; 2.6) |
2.6 (2.0; 3.3) |
0.4 |
|
Relaxation rate (deep breathing) on the right, cm/s |
3.2 (2.6; 3.6) |
2.7 (1.9; 3.6) |
0.24 |
Note. * —significant difference, p<0.05.
Structural and functional parameters of diaphragm in men and women are significantly different in some cases. In particular, thickness of diaphragm in different phases of respiratory cycle and thickening index on the left during calm breathing differ. Among functional parameters, we can emphasize differences in maximum amplitude of diaphragm excursion during deep breathing.
Discussion
According to the literature data, results of ultrasound of diaphragm in the apposition zone are comparable and reproducible [25]. Nevertheless, there is certain variability due to objective and subjective circumstances. In particular, differences are associated with operator-dependent nature of ultrasound examination [7, 9, 18], influence of anthropometric characteristics of subjects and methodological aspects (body and sensor position, size and heterogeneity of groups, etc.) [13, 18, 26]. These aspects can explain obvious differences between our own findings and literature data on diaphragm thickening index during calm breathing on both sides [20]. Natural individuality of participants and probability of arbitrary component (ability of subject to change inhalation/exhalation rate at will) are apparently the most significant reasons for some discrepancy regarding duration of diaphragm relaxation during calm breathing [24].
Analysis of diaphragm thickness on both sides and excursion on the right usually do not cause difficulties [24]. On the contrary, analysis of excursion on the left may be difficult due to small acoustic window and adjacent intestine and stomach containing air [21, 23]. According to the literature and our own data, there are no significant differences in structural and functional parameters of both domes of diaphragm. However, we observed different thickness and excursion of diaphragm domes. These findings may be due to structural and functional asymmetry of human body rather any pathology.
Significant sex-related differences can be explained by different muscle masses [27, 28]. The differences of diaphragm thickening index in men and women on the left should not be regarded as final. To confirm these findings, additional measurements in larger samples including the indicators indexed to body weight and surface area are needed. Indeed, the last ones are traditionally regarded as the most representative.
Despite certain "noise", ultrasound of diaphragm can still be successfully used in clinical practice to assess its function in dynamics of disease and concomitant spirometric changes [28, 29]. This is especially important in case of unilateral lesion [7, 13].
Ultrasonic indicators such as time and rate of diaphragm contraction/relaxation may be important diagnostic and prognostic indicators in the management of ICU patients (timely respiratory support and choice of respiratory parameters with optimal ratio of work and relaxation of diaphragm). These conclusions are based on the well-known advantages of sonography: cost-effectiveness and accessibility at the patient’s bedside, non-invasiveness and simplicity, assessing the role of diaphragm dysfunction in respiratory failure and prediction of weaning from mechanical ventilation [17, 19, 29, 30]. Many of these aspects need to be further studied.
Conclusion
Ultrasonic analysis of structural and functional parameters of diaphragm is going through the stage of data accumulation and comprehension. Our results are largely comparable with literature data that indicates a reproducible method. In addition, we presented certain indicators (duration of diaphragm contraction and relaxation under calm and deep breathing) which are just beginning to attract the attention of researchers.
Thus, we can make the following conclusions:
1) ultrasonic examination of diaphragm provides additional data on its function;
2) structural and functional parameters of both domes of diaphragm are similar that justifies assessment only on the right side;
3) ultrasonic indicators can significantly differ in men and women.
Author contribution:
Concept and design of the study — Shabaev V.S., Mazurok V.A., Orazmagomedova I.V.
Collection and analysis of data — Shabaev V.S., Orazmagomedova I.V., Vasilyeva L.G., Kirillovskaya A.G.
Statistical analysis — Shabaev V.S.
Writing the text — Shabaev V.S., Mazurok V.A.
Editing — Shabaev V.S., Mazurok V.A., Berezina A.V.
The authors declare no conflicts of interest.