what is diaphragm excursion

• Introduction
• Palp/Percus
• Auscultation

Palpation/Percussion

Thoracic expansion:.

• Is used to evaluate the symmetry and extent of thoracic movement during inspiration.
• Is usually symmetrical and is at least 2.5 centimeters between full expiration and full inspiration.
• Can be symmetrically diminished in ankylosing spondylitis .
• Can be unilaterally diminished in chronic fibrotic lung disease , extensive lobar pneumonia, large pleural effusions, bronchial obstruction and other disease states.

Percussion:

Percussion is the act of tapping on a surface, thereby setting the underlying structures in motion, creating a sound and palpable vibration. Percussion is used to determine whether underlying structures are fluid-filled, gas-filled, or solid. Percussion:

• Penetrates 5 - 6 centimeters into the chest cavity.
• May be impeded by a very thick chest wall.
• Produces a low-pitched, resonant note of high amplitude over normal gas-filled lungs.
• Produces a dull, short note whenever fluid or solid tissue replaces air filled lung (for example lobar pneumonia or mass) or when there is fluid in the pleural space (for example serous fluid, blood or pus).
• Produces a hyperresonant note over hyperinflated lungs (e.g. COPD ).
• Produces a tympanitic note over no lung tissue (e.g. pneumothorax ).

Diaphragmatic excursion:

• Can be evaluated via percussion.
• Is 4-6 centimeters between full inspiration and full expiration.
• May be abnormal with hyperinflation , atelectasis , the presence of a pleural effusion , diaphragmatic paralysis, or at times with intra-abdominal pathology.

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Citation, DOI, disclosures and article data

At the time the article was created Craig Hacking had no recorded disclosures.

At the time the article was last revised Craig Hacking had the following disclosures:

• Philips Australia, Paid speaker at Philips Spectral CT events (ongoing)

These were assessed during peer review and were determined to not be relevant to the changes that were made.

• Diaphragm fluoroscopy

The fluoroscopic sniff test , also known as diaphragm fluoroscopy , is a quick and easy real time fluoroscopic assessment of diaphragmatic motor function (excursion). It is used most often to confirm absence of muscular contraction of the diaphragm during inspiration in patients with phrenic nerve palsy or breathing difficulties following stroke . Chest radiograph demonstrating a newly elevated hemidiaphragm often precedes a sniff test.

In critically unwell patients who can not attend the fluoroscopy unit in the radiology department, bedside US assessment can be used to demonstrate appropriate diaphragmatic movement with normal respiration and when asked to sniff (see case 5).

The following technique is suggested:

ask the patient to practice sniffing before the study

with the patient either standing (preferred) or supine, perform frontal fluoroscopy of the diaphragm at rest, breathing quietly through an open mouth

ask the patient to take a few quick short breaths in with a closed mouth ('sniffs') causing rapid inspiration

occasionally, repeating (3) in the lateral projection is required to evaluate the posterior hemidiaphragms

In normal diaphragmatic motion:

the diaphragm contracts during inspiration: moves downwards

the diaphragm relaxes during expiration: moves upwards

both hemidiaphragms move together

in healthy patients 1-2.5 cm of excursion is normal in quiet breathing 2

3.6-9.2 cm of excursion is normal in deep breathing 2

up to 9 cm can be seen in young or athletic individuals in deep inspiration 2

excursion in women is slightly less than men 2

In abnormal diaphragmatic motion:

the affected hemidiaphragm does not move downwards during inspiration

paradoxical motion can occur

Interpretation

Absence of diaphragmatic movement confirms phrenic nerve palsy in the appropriate clinical setting. A mass anywhere along the course of the phrenic nerve requires further workup, usually with neck and chest CT. A hilar mass due to lung cancer is the most common finding on CT and a classic exam case.

Normal diaphragmatic excursion can also be impaired in patients with:

previous diaphragmatic trauma or surgery

neuromuscular disorders

previous stroke

• 1. Nason LK, Walker CM, McNeeley MF et-al. Imaging of the diaphragm: anatomy and function. Radiographics. 2012;32 (2): E51-70. doi:10.1148/rg.322115127 - Pubmed citation
• 2. Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values. Chest. 2009;135 (2): 391-400. doi:10.1378/chest.08-1541 - Pubmed citation
• Nason L, Walker C, McNeeley M, Burivong W, Fligner C, Godwin J. Imaging of the Diaphragm: Anatomy and Function. RadioGraphics. 2012;32(2):E51-70. doi:10.1148/rg.322115127 - Pubmed

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• Diaphragmatic paralysis
• Phrenic nerve palsy
• Ultrasound diaphragmatic sniff test
• Left hilar mass causing phrenic nerve palsy
• Large right diaphragmatic hernia
• Hemidiaphragmatic paralysis
• Abnormal sniff test
• Normal sniff test
• Phrenic nerve palsy with positive sniff test

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Sonographic evaluation of diaphragmatic thickness and excursion as a predictor for successful extubation in mechanically ventilated preterm infants

• Original Article
• Published: 28 September 2020
• Volume 180 , pages 899–908, ( 2021 )

Cite this article

• Eslam Bahgat 1 ,
• Hanan El-Halaby 2 ,
• Ashraf Abdelrahman 3 ,
• Nehad Nasef   ORCID: orcid.org/0000-0001-7650-123X 1 , 2 , 4 &
• Hesham Abdel-Hady 1 , 2  

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A Correspondence to this article was published on 12 November 2020

Sonographic assessment of diaphragmatic thickness and excursion has been found to be an accurate tool in predicting successful extubation of adult patients from invasive mechanical ventilation. We aimed to evaluate the accuracy of sonographic assessment of diaphragmatic thickness and excursion in predicting successful extubation of preterm infants from invasive conventional mechanical ventilation. Preterm infants less than 32 weeks gestation who required invasive conventional mechanical ventilation were evaluated by diaphragmatic sonography within 1 h of their planned extubation. Infants were classified into successful or failed extubation groups based on their ability to stay off invasive mechanical ventilation for 72 h after extubation. Inspiratory and expiratory thickness plus excursion of the right and left hemidiaphragm as well as diaphragmatic thickening fraction (DTF) measures were compared between groups. We included 43 eligible infants, of whom 34 infants succeeded and 9 infants failed extubation. Infants in the successful extubation group had a significantly higher expiratory thickness of the right and left hemidiaphragm, excursion of the right and left hemidiaphragm, inspiratory thickness of the left hemidiaphragm, and DTF of the left hemidiaphragm compared with infants who failed extubation. The receiver-operating characteristic curves showed that excursion of the right and left hemidiaphragm has the highest significant accuracy in predicting successful extubation of preterm infants among all diaphragmatic parameters (AUC is 0.98 and 0.96, respectively; p value < 0.001 for both).

Conclusion : We conclude that diaphragmatic excursion is a useful indicator for successful extubation of preterm infants from mechanical ventilation.

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Introduction

The decision to extubate preterm infants from mechanical ventilators is mainly based on clinical assessment, blood gases, and ventilator settings [ 7 ]. Researchers attempted to evaluate different parameters as predictors for successful extubation of preterm infants from mechanical ventilation [ 26 , 28 ]. However, up to 30% of preterm infants who are extubated based on the clinical assessment require re-intubation indicating a poor correlation with infants’ readiness for extubation [ 3 , 28 ].

The diaphragm represents the main respiratory muscle in infancy. It contributes to generation of an estimated three-fourths of the infant's tidal volume during resting inspiration in the supine position [ 23 ]. Continuous positive airway pressure (CPAP) affects the crura of diaphragm by shortening the muscle and decreasing excursion through maintaining end expiratory lung volume [ 21 ]. Moreover, prolonged mechanical ventilation triggers myofibrillar contractile dysfunction and myofilament protein loss of the diaphragmatic muscles which later results in loss of diaphragmatic force-generating capacity, poor activity, and unloading of the diaphragm [ 10 ]. This phenomenon of ventilator-induced diaphragmatic dysfunction (VIDD) has raised the attention of investigators to the correlation between duration of mechanical ventilation and failure to extubate preterm infants from mechanical ventilation [ 27 ]. However, the diagnosis of this diaphragmatic dysfunction can be hindered by the lack of appropriate quantitative assessments of neonatal diaphragm function [ 1 ].

Accurate assessment of diaphragm function in the neonate could aid to the diagnosis of respiratory distress, evaluation of therapeutic interventions, and identification of infants ready to wean from mechanical ventilation [ 20 ]. Monitoring the electrical activity of the diaphragm in infants and children has shown that higher diaphragmatic activity in relation to tidal volume indicates a better preserved diaphragmatic function and a better chance of passing the extubation readiness test [ 29 ]. However, the tools needed for monitoring the electrical activity of the diaphragm are invasive, expensive, and require trained personnel for proper interpretation. Sonographic evaluation of the diaphragm is ubiquitous in medical facilities, requires no radiation, can be used at the infant’s bedside, and useful in assessing diaphragmatic mobility and excursion [ 13 ].

We hypothesized that assessment of diaphragmatic dimensions and excursion, before planned extubation, may be helpful in predicting successful extubation of preterm infants from mechanical ventilation. We aimed to study sonographic assessment of the diaphragmatic dimensions and excursion for mechanically ventilated preterm infants as a predictor for success of extubation.

The present study was placed at the Neonatal Intensive Care Unit (NICU) of Mansoura University Children’s Hospital, Mansoura, Egypt, between January 2017 and November 2019. The study was approved by the Institutional Review Board, Mansoura Faculty of Medicine, and a fully informed written consent was obtained from the parent or infant's guardian before enrolment in the study.

Study designs

This was a prospective, observational, cohort study assessing diaphragmatic thickness and excursion for preterm infants prior to planned extubation from invasive conventional mechanical ventilation.

Participants

Preterm infants less than 32 weeks gestation who were supported by invasive conventional mechanical ventilation for a diagnosis of respiratory distress syndrome, as evident by clinical and radiological findings, and planned for extubation were eligible for this study. Preterm infants with chromosomal aberrations, hepatosplenomegaly, pleural effusion, congenital heart or lung disorders, or congenital anomalies related to diaphragm as diaphragmatic hernia and diaphragmatic paralysis were excluded from the study.

Intervention

Eligible preterm infants had sonographic assessment of diaphragmatic thickness and excursion within 1 h of planned extubation from invasive conventional mechanical ventilation to non-invasive respiratory support. Preterm infants were extubated from mechanical ventilation if they fulfilled the following criteria: spontaneous respiratory effort, presence of cough or gag induced by suctioning, acceptable arterial blood gases (pH more than 7.25, PaCO 2 less than 60 mmHg, and base deficit less than 8 mEq/L) on a mean airway pressure less than 8 cm H 2 O and respiratory rate of less than 30/min, saturation more than 90% on fraction of inspired oxygen (FiO 2 ) less than 30% in the preceding 24 h, and the decision of extubation was taken by the attending physician who was blinded to the results of sonographic measurements.

Sonographic diaphragmatic parameters were measured while infants were on spontaneous pressure support ventilation mode with a support pressure of 4 cm H 2 O over an end expiratory pressure of 4 cm H 2 O for 1 h prior to the sonographic assessment as an accommodation. The total duration on pressure support ventilation mode and sonographic diaphragmatic assessment was 2 h at most to avoid infant exhaustion. Sonographic evaluation was performed prior to the time of next feed, while infant’s stomach is empty, to avert any interference of a full stomach on diaphragmatic mobility and measurements. All infants were extubated to nasal CPAP using the Infant Nasal CPAP Assembly system (Fisher & Paykel Healthcare, Auckland, New Zealand) at a pressure of 5 cmH 2 O and FiO 2 between 21% and 30% to keep infant's saturation between 90% and 95%.

Sonographic diaphragmatic assessment technique

Ultrasonographic examinations were performed by one operator, who had ten years of experience in diaphragm sonography, using a portable Doppler ultrasonography (Micro-Maxx; SonoSite, Bothell, WA, USA) with a micro-convex transducer array (10 to 5 MHz). Diaphragmatic sonography was performed while the infant is in supine position after ensuring quiet regular breathing. For visualization of the right hemidiaphragm, the convex probe was placed over the right subcostal and lower intercostal spaces between the anterior axillary and the midclavicular lines with the probe directed cranially, dorsally, and medially so the radial beam came to be perpendicular to the posterior third of the right hemidiaphragm. For visualization of the left hemidiaphragm, the same technique, position, and direction of the probe as the right hemidiaphragm were performed apart from the probe was placed between the left anterior axillary and midaxillary lines.

At first, the two-dimensional mode was screened to detect the appropriate exploration image for each hemidiaphragm in which the diaphragm appeared as a hypoechoic line that was placed between two echogenic lines, the upper one was the reflection of the parietal pleura and the lower was for the peritoneum. After that, the M-mode ultrasonography was screened and the image was frozen after ensuring regular up and down movement of the diaphragmatic line that reflects regular breathing. The thickness of the diaphragmatic line during inspiration (upward slope) and expiration (downward slope) represents the diaphragmatic inspiratory and expiratory thickness, respectively. The perpendicular distance between the most caudal point of this line during inspiration and the most caudal point during expiration represents the diaphragmatic excursion. Diaphragmatic thickness and kinetics measures can be affected by the irregular breathing pattern, high respiratory rate, breath to breath variability, and small diaphragmatic dimensions by using M-mode technique in preterm infants. To overcome this technical limitation, the investigator observed for regular up and down movements of the diaphragmatic line in M-mode and cine for 1 min to ensure an epoch of quiet regular breathing, and then diaphragmatic measurements were obtained [ 2 ]. The technique and measurements were repeated up to 3 respiratory cycles for each hemidiaphragm, and the average one was recorded [ 5 ]. Avoidance of diaphragmatic measurements during infant’s crying or sighing movement was taken in consideration.

The diaphragmatic thickening fraction (DTF) was calculated and recorded using the following formula: DTF = [(inspiratory thickness − expiratory thickness) / expiratory thickness] × 100 [ 8 ].

The intra-observer reproducibility was evaluated by repeated measurements of sonographic diaphragmatic parameters by the same investigator with 30 min in between measurements. Ten clinically stable preterm infants, age and sex cross-matched with the studied group, were randomly selected for this purpose.

Study end point

The primary study end point was successful extubation from invasive mechanical ventilation defined as being off mechanical ventilation with transmission to oxygen therapy or non-invasive respiratory support, for at least 72 h post-extubation [ 12 ]. The indications for re-intubation were specified as follows: more than six episodes of apnea requiring stimulation within 6 h, or more than one significant episode of apnea requiring bag and mask ventilation, respiratory acidosis (PaCO 2 > 65 mmHg and pH < 7.25) or FiO 2 > 60% to maintain saturation in the target range (90–95%) [ 12 ].

Sample size calculation

Sample size calculation was based on the area under the receiver-operating characteristic curve that was 0.79 for predicting successful extubation of mechanical ventilation retrieved from previous research [ 4 ]. Using MedCalc for Windows, version 15.0 (MedCalc Software, Ostend, Belgium), sample size calculation using area under ROC curves with null hypothesis = 0.5, α-error = 0.05, power of the study = 80% ratio of positive to negative cases which will be considered as 3.3. The total calculated sample size will be 43 cases.

Statistical analysis

Statistical analysis was performed using SPSS statistical software (version 21; IBM Corporation, Armonk, NY, USA). Student’s t test was used to compare continuous parametric variables. Mann–Whitney U test was used for continuous non-parametric variables. Chi-square test or Fisher’s exact test was used for categorical variables when appropriate. Shapiro–Wilk test was done to examine the distribution of data. Pearson's correlation coefficient test was used to correlate between duration of invasive mechanical ventilation and different diaphragmatic measures. The accuracy of different diaphragmatic measurements for predicting successful extubation from invasive mechanical ventilation was evaluated using receiver-operating characteristic (ROC) curves. A p value of < 0.05 is considered to be statistically significant. Data are expressed as mean ± standard deviation, median (inter-quartile range), or number (percentage) unless otherwise stated. Reproducibility of the diaphragmatic measurements was assessed by Bland–Altman analysis and Pearson’s correlation coefficient.

Of the 164 preterm infants who were at less than 32 weeks gestation admitted to our NICU during the study period, 62 infants required invasive conventional mechanical ventilation, 43 were included in the study, and 19 were excluded due to various causes (Fig. 1 ). A total of 34 infants succeeded and 9 infants failed extubation. Infants in the failed extubation group had significantly higher postnatal age at extubation, longer duration of invasive mechanical ventilation, higher pre-extubation mean airway pressure, and higher pre-extubation FIO 2 compared with infants in the successful extubation group (Table 1 ). Of the 9 infants who failed extubation, 6 infants were reintubated for increased work of breathing in association with hypoxia, two infants were reintubated for increased work of breathing in association with hypercapnia, and one infant was reintubated for apnea which was preceded by increased work of breathing. The mean time for reintubation was 43.5 ± 13.5 h with a minimum of 29 and a maximum of 66 h, respectively. Measurements were highly reproducible with a high degree of agreement between diaphragmatic dimensions as assessed by Pearson’s correlation coefficient and Bland–Altman analysis. Pearson’s correlation coefficient values were above 0.9, and p values were < 0.001 for all measured diaphragmatic indices.

Diagram showing the flow of participants in the study

Infants in the successful extubation group had a significantly higher expiratory thickness of the right and left hemidiaphragm, excursion of the right and left hemidiaphragm, inspiratory thickness of the left hemidiaphragm, and DTF of the left hemidiaphragm compared with infants who failed extubation to nasal CPAP (Table 2 ) (Fig. 2 ). The duration of invasive mechanical ventilation had a significant negative correlation with inspiratory and expiratory thickness of the right and left hemidiaphragm, excursion of the right hemidiaphragm, and DTF of the right and left hemidiaphragm (Table 3 ).

Sonographic images showing M-mode measurements of inspiratory thickness, expiratory thickness, and excursion of the right hemidiaphragm in an infant (case number 5) from the successful extubation group and an infant (case number 11) from the failed extubation group

The ROC curves showed that expiratory thickness of the right and left hemidiaphragm, excursion of the right and left hemidiaphragm, inspiratory thickness of the left hemidiaphragm, and DTF of the left hemidiaphragm had significant accuracies in predicting successful extubation of preterm infants (Fig. 3 ). Excursion of the right and left hemidiaphragm showed the highest accuracy among all diaphragmatic parameters. A right hemidiaphragmatic excursion of 2.75 mm was associated with 94% sensitivity and 89% specificity in predicting successful extubation. A left hemidiaphragmatic excursion of 2.45 mm was associated with 94% sensitivity and 89% specificity in predicting successful extubation.

Receiver-operating characteristic curves show area under the curve (AUC) and p value of significance for inspiratory thickness of the right hemidiaphragm ( a ), expiratory thickness of the right hemidiaphragm ( b ), excursion of the right hemidiaphragm ( c ), inspiratory thickness of the left hemidiaphragm ( d ), expiratory thickness of the left hemidiaphragm ( e ), excursion of the left hemidiaphragm ( f ), and diaphragm thickening fraction (DTF) of the right hemidiaphragm ( g ) and the left hemidiaphragm ( h ) in predicting successful extubation of preterm infants from mechanical ventilation

Sonographic assessment of the lungs and diaphragm has gained the interest of neonatologists nowadays. Sonographic assessment of the lungs has shown a high sensitivity and specificity in diagnosing various respiratory disorders in neonates [ 24 ]. Ultrasound has been recently used to assess diaphragmatic thickness and excursion of diaphragmatic dome in stable spontaneously breathing infants [ 5 ]. We aimed to assess the accuracy of sonographic assessment of diaphragmatic thickness and excursion as a predictor for successful extubation of preterm infant from invasive conventional mechanical ventilation. The main finding of our study is that excursion of the right and left hemidiaphragm has the highest accuracy in predicting successful extubation of mechanically ventilated preterm infants. Diaphragmatic excursion was significantly higher in preterm infants successfully extubated from invasive conventional mechanical ventilation compared with infants who failed extubation.

Diaphragmatic activity as a predictor for successful extubation was evaluated in pediatric age group through monitoring of diaphragmatic electrical activity. Assessment of diaphragmatic electrical activity has shown that infants and children who generated higher diaphragmatic activity in relation to tidal volume had a better chance of passing the extubation readiness test as opposed to infants and children who generated lower diaphragmatic activity in relation to tidal volume [ 29 ]. Authors in this study stated that diaphragmatic activity in relation to tidal volume indicates a better preserved diaphragmatic function [ 29 ].

To the best of our knowledge, this study is the earliest to report the accuracy of assessing diaphragmatic activity by using diaphragmatic ultrasound in prediction of successful extubation in preterm infants. Over 400 participants between 1 month and 16 years, sonographic assessment of the diaphragm has shown a high accuracy in assessing diaphragmatic thickness and excursion [ 5 ]. Rehan and colleagues reported normal diaphragmatic excursion in 34 preterm infants between 26 and 37 weeks gestation to be 5.5 ± 0.2 mm at 26 to 28 weeks gestation, 4.8 ± 0.2 mm in 29 to 31 weeks gestation, 4.6 ± 0.2 mm in 32 to 34 weeks gestation, and 4.4 ± 0.3 mm in 35 to 37 weeks gestation [ 22 ]. The difference between our measurements and Rehan's study is attributed to their inclusion of clinically stable preterm infants who have no evidence of any acute illness, no culture proven sepsis, not on any oxygen supplementation, and not on CPAP or ventilator support compared with our ventilated infants. Radicioni and colleagues tested the accuracy of a model that consists of the sonographic measurements of right diaphragmatic excursions during inspiration and expiratory phases plus the oxygen saturation/FiO 2 ratio as a predictor for CPAP failure in preterm infants with respiratory distress syndrome. The authors found that integration of both measures in this model has a high accuracy, with AUC 0.95, in predicting CPAP failure [ 19 ].

In mechanically ventilated adults, sonographic assessment of diaphragmatic function showed that diaphragmatic excursion was significantly higher in the successful group compared with those who failed extubation [ 6 ]. Liu and colleagues found that diaphragmatic excursion had a sensitivity of 89.2% and a specificity of 75.0% with an AUC (ROC) of 0.849 in predicting successful extubation in mechanically ventilated adult patients. The cut-off value of diaphragmatic excursion for predicting successful extubation was determined to be 1.14 cm by ROC curve analysis [ 16 ]. Yoo et al. found that diaphragmatic excursion is more accurate than a change in the diaphragm thickness to predict extubation success in mechanically ventilated adults [ 31 ]. In a meta-analysis of 13 studies over 742 adults, Li and colleagues concluded that diaphragmatic excursion and thickness are accurate measures for predicting reintubation within 48 h of extubation despite having a large heterogeneities among the included studies [ 15 ].

In mechanically ventilated adults, McCool and colleagues [ 17 ] showed that the duration of mechanical ventilation was significantly shorter in patients diagnosed with normal diaphragmatic function as assessed by ultrasound measurement of diaphragmatic thickness and excursion. The authors stated that normal diaphragmatic function as assessed by ultrasound shows 90.9% sensitivity, 86.7% specificity, 90.9% positive predictive value, and 86.7% negative predictive value in predicting successful extubation from mechanical ventilation [ 17 ].

The proposed mechanism for diaphragmatic dysfunction in association with invasive mechanical ventilation is the loss of myofilament protein of diaphragmatic muscle which results in what is known as ventilator-induced diaphragmatic dysfunction (VIDD). A previous research revealed that only 18–24 h of invasive mechanical ventilation is sufficient to develop VIDD in both laboratory animals and humans [ 18 ]. In animal models, ventilator-induced diaphragmatic proteolysis and associated diaphragmatic atrophy occur due to increased diaphragmatic protein breakdown and decreased protein synthesis which is mediated by various proteases, such as calpain, caspase-3, autophagy, and the ubiquitin-proteasome system [ 18 ]. We have found that expiratory thickness of the right and left hemidiaphragm and inspiratory thickness of the left hemidiaphragm were significantly lower in infants who failed compared with infants who succeeded extubation from mechanical ventilation. Our results support previous results of ventilator-induced diaphragmatic atrophy which were retrieved by animal studies and human studies [ 11 , 14 ]. This is further supported by our finding of negative correlation between the duration of mechanical ventilation with inspiratory and expiratory thickness of the right and left hemidiaphragm, excursion of the right hemidiaphragm, and DTF of the right and left hemidiaphragm. The possible cause of the absence of significant difference in the inspiratory thickness and thickening fraction of the right hemidiaphragm between successfully and failed extubated preterm infants can be attributed to the supporting effect of the liver to the right hemidiaphragm during inspiration which can mask minimal effects on the muscle mass of the right hemidiaphragm. Another possibility for this non-significant difference may be related to our use of M-mode technique during measurement. Compared with B-mode, M-mode may not obtain reliable measurements of the diaphragmatic thickness, due to the subtlety of the imaging line. However, we compensated for this by obtaining our M-mode measures over the most moving point of the hemidiaphragm on B-mode. Moreover, M-mode technique has been successfully used in previous studies to measure diaphragmatic thickness in excursion in adults and pediatric age groups [ 9 , 30 ].

A potential technical limitation to our study is the use of a micro-convex transducer rather than a high-frequency micro-linear transducer for imaging. The latter has better ability for visualization of the thin muscles and superficial structures, like hemidiaphragm. However, the micro-convex transducer gives a better in-between ribs view and wider angle of image “pie-shaped image” of the whole hemidiaphragm which allows for better identification of the most moving part of the hemidiaphragm in B-mode. We compensated for this technical limitation by taking our M-mode measurements at the most moving part of hemidiaphragm in the B-mode view.

We acknowledge that the study is limited by the relatively small sample size, which is attributed to our adoption of the early administration of non-invasive respiratory support techniques to our preterm infants to minimize ventilator-induced lung injury which decreased the percentage of preterm infants who required invasive mechanical ventilation during the study period. The study is also limited by the lack of physiopathologic proof of respiratory etiology as a cause for extubation failure and the need for reintubation. It is of note that assessment of diaphragmatic function in infants who failed extubation due to non-respiratory causes, such as central apnea or poor respiratory drive, is less valuable. Moreover, our practice of extubation to a nasal CPAP of 5 cm H 2 O represents another limitation given the new guidelines of extubating preterm infants to CPAP pressure of 7–9 cm H 2 O [ 25 ]. Our low level of CPAP support may have resulted to an increased incidence of preterm infants who required reintubation. Future studies should consider evaluation of diaphragmatic thickness and excursion in relation of different modes and parameters of respiratory support to find out the appropriate approach for respiratory support in preterm infants that maintain adequate diaphragmatic stimulation and prevent VIDD.

In conclusion, sonographic assessment of diaphragmatic thickness and excursion represents a promising sensitive and specific easily applicable tool to predict successful extubation of preterm infants from invasive conventional mechanical ventilation.

Abbreviations

Area under the curve

Continuous positive airway pressure

Diaphragmatic thickening fraction

Neonatal intensive care unit

Ventilator induced diaphragmatic dysfunction

Fraction of inspired oxygen

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Eslam Bahgat, Nehad Nasef & Hesham Abdel-Hady

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Hanan El-Halaby, Nehad Nasef & Hesham Abdel-Hady

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Eslam Bahgat and Hanan El-Halaby participated in the design of the study, data collection, and writing the manuscript. Ashraf Abdelrahman participated in sonographic assessment of the diaphragm and manuscript writing. Nehad Nasef and Hesham Abdel-Hady participated in formulating the hypothesis, design of the study, data collection, data interpretation, statistical analysis, and writing of the manuscript. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

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Bahgat, E., El-Halaby, H., Abdelrahman, A. et al. Sonographic evaluation of diaphragmatic thickness and excursion as a predictor for successful extubation in mechanically ventilated preterm infants. Eur J Pediatr 180 , 899–908 (2021). https://doi.org/10.1007/s00431-020-03805-2

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Diaphragmatic excursion is correlated with the improvement in exercise tolerance after pulmonary rehabilitation in patients with chronic obstructive pulmonary disease

• Masashi Shiraishi   ORCID: orcid.org/0000-0001-5410-1331 1 , 2 ,
• Yuji Higashimoto 1 ,
• Ryuji Sugiya 1 ,
• Hiroki Mizusawa 1 ,
• Yu Takeda 1 ,
• Shuhei Fujita 1 ,
• Osamu Nishiyama 2 ,
• Shintarou Kudo 3 ,
• Tamotsu Kimura 1 ,
• Yasutaka Chiba 4 ,
• Kanji Fukuda 1 ,
• Yuji Tohda 2 &
• Hisako Matsumoto 2  

Respiratory Research volume  22 , Article number:  271 ( 2021 ) Cite this article

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In patients with chronic obstructive pulmonary disease (COPD), the maximum level of diaphragm excursion (DE max ) is correlated with dynamic lung hyperinflation and exercise tolerance. This study aimed to elucidate the utility of DE max to predict the improvement in exercise tolerance after pulmonary rehabilitation (PR) in patients with COPD.

This was a prospective cohort study. Of the 62 patients with stable COPD who participated in the outpatient PR programme from April 2018 to February 2021, 50 completed the programme. Six-minute walk distance (6MWD) was performed to evaluate exercise tolerance, and ultrasonography was performed to measure DE max . Responders to PR in exercise capacity were defined as patients who demonstrated an increase of > 30 m in 6MWD. The receiver operating characteristic (ROC) curve was used to determine the cut-off point of DE max to predict responses to PR.

Baseline levels of forced expiratory volume in 1 s, 6MWD, maximum inspiratory pressure, DE max and quadriceps muscle strength were significantly higher, and peak dyspnoea of modified Borg (mBorg) scale score was lower in responders (n = 30) than in non-responders (n = 20) to PR (p < 0.01). In multivariate analysis, DE max was significantly correlated with an increase of > 30 m in 6MWD. The area under the ROC curve of DE max to predict responders was 0.915, with a sensitivity and specificity of 83% and 95%, respectively, at a cut-off value of 44.9 mm of DE max .

DE max could adequately predict the improvement in exercise tolerance after PR in patients with COPD.

Chronic obstructive pulmonary disease (COPD) is a progressive disease characterised by minimally reversible airflow limitation [ 1 ]. The main feature of COPD is the inability of patients to cope with their activities of daily life due to shortness of breath. Although the pathophysiological mechanisms involved in the development of dyspnoea and poor exercise tolerance in patients with COPD are complex, dynamic lung hyperinflation (DLH) plays a central role [ 2 ] by increasing ventilatory workload and decreasing the pressure-generating capacity of the inspiratory muscles.

Pulmonary rehabilitation (PR) is a non-pharmacological intervention and has been reported to improve dyspnoea, exercise capacity and quality of life of patients with COPD [ 3 ]. Owing to a body of evidence, PR is now established as the standard of care for patients with COPD [ 4 ]. However, not all patients with COPD benefit from PR to the same extent. Therefore, identifying patients who are likely to achieve maximum benefit from the PR programme is crucial. So far, several studies have shown that severe airflow limitation or poor exercise tolerance at baseline may predict a better response to PR [ 5 , 6 ], but another study has reported inconsistent findings [ 7 ]. Furthermore, one study reported that patients with severe dyspnoea did not respond well to PR and patients with milder dyspnoea responded well [ 8 ].

Considering the role of DLH in the development of dyspnoea and poor exercise tolerance in patients with COPD, objective measures that reflect the degree of DLH may help in identifying good responders to PR. Previously, we reported that there was an association between increased dyspnoea due to DLH on exercise and decreased exercise capacity in patients with COPD and reduced mobility of the diaphragm, which was assessed by the maximum level of diaphragm excursion (DE max ) using ultrasonography [ 9 ]. Other research groups reported the utility of ultrasonographic assessment of diaphragmatic mobility in COPD in understanding its association with 6-min walk distance (6MWD), dyspnoea [ 10 ] and increased mortality [ 11 ].

However, there have been no reports on the association between diaphragmatic mobility and the effect of PR to improve exercise tolerance. The primary aim of this study is to clarify the role of DE max to predict the improvement in exercise tolerance after PR in patients with COPD.

Materials and methods

Study design and subjects.

This was a single-centre, observational, prospective cohort study. The study included 62 patients with clinically stable COPD who visited the Department of Respiratory Medicine and Allergology, Kindai University Hospital, between April 2018 and February 2021. The exclusion criteria included unstable medical conditions that could cause or contribute to breathlessness, such as metabolic, cardiovascular or other respiratory diseases, or any other disorders that could interfere with exercise testing, such as neuromuscular diseases or musculoskeletal problems. This study was approved by the Ethics Committee of Kindai University School of Medicine. Written informed consent was obtained from all participants.

Measurements

All participants underwent ultrasonography (Xario 200, Toshiba, Tokyo, Japan) for the assessment of their DE max . Using the liver as an acoustic window (Fig.  1 A), a convex 3.5 MHz probe was used to measure the excursions of the right hemidiaphragm according to the techniques mentioned in previous studies [ 9 , 12 , 13 ]. The M-mode cursor was rotated and placed on the axis of diaphragmatic displacement on the stored image, and displacement measurements were performed. Measurements were performed during each of the three deep breaths, and DE max was measured (Fig.  1 B). The maximum value obtained for the three deep breaths was used. 6MWD was performed to evaluate walking capacity according to the American Thoracic Society (ATS)/European Respiratory Society (ERS) statement [ 14 , 15 , 16 ]. All participants performed the 6MWD test before and after the PR programme, and the magnitude of their perceived breathlessness and their leg fatigue was rated using a 1–10-point Borg scale. Responders to PR in exercise capacity were defined as those who demonstrated more than 30 m increase in 6MWD after the PR programme, which was the definition of minimal clinically important difference (MCID) for 6MWD [ 17 ].

Representative image of the right diaphragm. The probe was positioned below the right costal margin between the midclavicular and anterior axillary lines. A Two-dimensional ultrasonographic image of the right hemidiaphragm (B-mode). Diaphragmatic movements were recorded in M-mode during deep breathing (DE max ) ( B )

Spirometry (CHESTAC-800, Chest, Tokyo, Japan) was performed following the 2005 ATS/ERS recommendations [ 18 ] for measuring forced vital capacity (FVC), forced expiratory volume in 1 s (FEV 1 ) and inspiratory capacity. Respiratory muscle strength was assessed by measuring the maximum inspiratory pressure (PI max ) generated against an occluded airway at residual volume [ 19 ] (SP-370, Fukuda Denshi, Tokyo, Japan). A hand-held dynamometer (μTasF-1, Anima Corp., Tokyo) was used to measure quadriceps muscle strength (QMS). The impact of COPD on health status was assessed using the COPD assessment test (CAT), a patient-completed questionnaire on eight items, namely, cough, phlegm, chest tightness, breathlessness, limited activities, confidence leaving home, sleeplessness and energy. The scores for each of the items range from 0 to 5 points, resulting in a CAT total score ranging from 0 to 40 points [ 20 ], and MCID of CAT is 2 points [ 21 ]. In all patients with COPD, emphysema was evaluated by computed tomography of the chest. A SYNAPSE VINCENT volume analyser (FUJIFILM Medical, Tokyo, Japan) was used to measure the low attenuation area (%LAA).

Rehabilitation programme

The outpatient PR programme was conducted twice a week for 12 weeks (24 sessions), including aerobic exercise training (ergometer and walking exercise) at 60–70% of peak workload for 20–40 min and upper- and lower-limb muscle strength training for 10–20 min.

Sample size

The sample size was estimated using R software. The analysis based on 6MWD data from the PR programme revealed that 40 subjects were required if the expected area under the curve (AUC) below the receiver operating characteristic (ROC) curve was 0.80, the power was 90%, and the significance level was 0.01. Furthermore, we anticipated a dropout from the PR programme. Thus, we set the sample size to 50 participants.

Statistical analysis

Responders and non-responders were compared using t -test, the Wilcoxon rank-sum test or χ 2 test, as appropriate. The paired t -test or the Wilcoxon signed-rank test was used to evaluate the changes in the parameters before and after the PR programme. The Pearson correlation coefficient was used to analyse the relationship between changes in 6MWD and independent variables because changes in 6MWD were normally distributed. Additionally, multivariate logistic regression models were used to assess the ability of variables to predict a response to PR. The ROC curve method was used to assess the ability of DE max to predict a response to PR. All statistical analyses were performed using the JMP software programme (JMP®, Version 14; SAS Institute Inc., Cary, NC, USA).

Out of the 62 patients included in the study, 50 completed the PR programme (Fig.  2 ). Two patients dropped out because of severe exacerbation of COPD, and 10 patients discontinued the PR owing to the coronavirus pandemic. Table 1 presents the baseline characteristics of the participants. After the PR programme, scores for CAT, 6MWD, peak dyspnoea and leg fatigue of the modified Borg (mBorg) scale, and QMS improved significantly (Table 2 ). Thirty patients showed an increase of > 30 m in 6MWD after PR (responders: 60%), and 20 patients (40%) were defined as non-responders. Baseline levels of %FEV 1 , 6MWD, PI max , DE max and QMS were significantly higher and those of CAT score and peak dyspnoea of mBorg scale were significantly lower in responders than in non-responders (Table 1 ). Changes in 6MWD were significantly correlated with baseline levels of CAT, %FEV 1 , peak dyspnoea of mBorg scale, PI max , DE max (Fig.  3 ) and QMS and marginally correlated with baseline levels of 6MWD (Table 3 ).

Study flow diagram. COPD chronic obstructive pulmonary disease, PR pulmonary rehabilitation, 6MWD 6-min walk distance

Relationship between DE max and the changes in 6MWD after pulmonary rehabilitation. Changes in 6MWD were significantly positively correlated with DE max (r = 0.72; p < 0.001). DE max maximum diaphragmatic excursion, 6MWD 6-min walk distance

In multivariate analysis, DE max alone significantly contributed to the prediction of responders (Table 4 , Model 1). When using PI max instead of DE max because PI max and DE max showed a strong association (r = 0.73), both PI max and %FEV 1 contributed to the prediction (Table 4 , Model 2). The area under the ROC curve of DE max to predict the responders was 0.915, with a sensitivity of 83% and a specificity of 95% at a cut-off value of 44.9 mm of DE max (Fig.  4 ). The significance of DE max in the predictability of responders remained even when the analysis was confined to severe patients (%FEV 1  < 50%, n = 23; AUC = 0.88, sensitivity = 70% and specificity = 100% at a cut-off value of 44.9 mm).

Receiver operating characteristic (ROC) curve for baseline DE max in relation to the response to pulmonary rehabilitation. ROC curve estimates the ability of DE max to predict a clinically important improvement in 6MWD (> 30 m) after pulmonary rehabilitation (AUC = 0.915, sensitivity = 83% and specificity = 95% at a cut-off point of 44.9 mm of DE max ). AUC area under the curve, 6MWD 6-min walk distance, DE max maximum diaphragmatic excursion

This is the first study to demonstrate the utility of DE max to predict the responsiveness of patients with COPD to 12-week PR. In this study, multivariate analysis revealed that greater baseline DE max was the only factor that predicted the responsiveness to PR, independent of baseline %FEV 1 . Additionally, the model using DE max had better prediction performance than that using PI max . The AUC of DE max to predict the 30 m or more improvement in 6MWD after the PR was 0.915, with a sensitivity of 83% and a specificity of 95% at 44.9 mm.

PR is beneficial to patients with chronic respiratory disease, including COPD [ 3 ], and generally improves exercise performance, health-related quality of life and dyspnoea [ 22 ], which was confirmed in this study. Ideally, PR was proven to be effective in all patients, but the response to PR varies considerably between individual patients [ 8 , 23 , 24 , 25 ]. Indeed, in this study, the improvement in 6MWD was less than that in MCID in 40% of the patients regardless of the degree of severity of COPD. Therefore, identifying predictors of a response is crucial in ensuring better PR efficacy and personalisation of PR programmes for patients with COPD.

In this study, the baseline values of %FEV 1 , PI max , DE max , QMS and 6MWD were positively associated with Δ6MWD in univariate analysis, suggesting that a better baseline condition was associated with a higher proportion of patients who achieved MCID after PR. These findings are consistent with those of previous studies that showed that patients with higher levels of %FEV 1 or FEV 1 /VC achieved greater improvement in 6MWD after PR [ 7 , 26 , 27 ] and a study in which patients with milder mMRC scores could achieve MCID of 6MWD after PR [ 8 ], but not for those with worst mMRC score, although others studies showed contradictory results [ 5 , 6 , 28 , 29 , 30 ] or found no significant baseline characteristics to predict a response to PR [ 31 ]. The discrepancy between the findings cannot be fully explained, but it might be due to the differences in the studied population and strength or length of PR. In this study, the mean %FEV 1 of the participants was 56.0%, which was relatively higher than that of other studies (mean %FEV 1 of 40–50% in most studies) [ 5 , 6 , 28 ], despite similar inclusion criteria throughout the studies, i.e., not limited to severe COPD in most studies. Thus, no ceiling effect with a PR programme that included high-intensity load exercise training for 20–40 min was observed in our population.

In this study, an important finding is that greater DE max at baseline was the only factor that predicted the responders in 6MWD after PR. In addition, the model using DE max had better prediction performance than that using PI max . The high predictability of DE max may be because of its strong association with DLH and dyspnoea during exercise, as reported previously [ 9 ]. DLH is involved in the development of dyspnoea, and both are important factors to determine the improvement in 6MWD in patients with COPD. Therefore, DE max that reflects the degree of DLH and dyspnoea during exercise was superior to other physiological indices to predict responders.

Furthermore, the virtuous cycle observed in our PR programme that included high-intensity load exercise training might be a result of the improvement in ventilation pattern. Improving the ventilation pattern would be easier with greater DE max , as shown in studies of mechanically ventilated patients [ 32 ], which may have reduced dyspnoea during exercise after 12 weeks of PR and improved exercise tolerance. Exercise therapy is a central component of PR, which significantly reduces blood lactate levels during exercise, reduces minute ventilation and improves exercise tolerance [ 33 ]. The high-intensity load exercise training, which is performed at 60–80% of the maximum oxygen uptake, has a higher physiological effect than low exercise load. Patients with greater DE max may be able to perform higher load training, which resulted in effective PR.

Diaphragm ultrasonography has been widely and successfully used to identify diaphragmatic dysfunction by showing its association with 6MWD, dyspnoea [ 10 ], extubation failure in mechanically ventilated patients [ 32 ], and increased mortality [ 11 ]. Recently, Lewinska and Shahnazzaryan proposed its use in pulmonary physiotherapy of patients with COPD [ 34 ]. In most previous studies, diaphragm ultrasonography was used to assess DE max , i.e., the measurement of the excursion of the right hemidiaphragm, as used in this study, and diaphragm thickness that assessed the length and thickness of the zone of apposition of the diaphragm against the rib cage [ 35 , 36 ]. However, it is difficult to measure diaphragm thickness in patients with severe COPD because the length of the zone of apposition is shorter in patients with COPD than that in control subjects [ 37 ], whereas it is easy to measure DE max, which shows high intra- and inter-observer reliability [ 38 ]. Bhatt et al. showed that improvement in 6MWD was associated with that in DE max during forced expiration when the effectiveness of pursed lips breathing was assessed in the PR of patients with COPD [ 39 ]. Corbellini et al. demonstrated greater improvement in DE max during inspiration after PR, which was associated with an increase in the inspiratory capacity [ 40 ]. The normal and cut-off values of DE max during normal respiration, forced respiration, and voluntary sniffing have been described for each gender [ 38 ]. Thus, DE max would be a useful and reliable measure for incorporation into the PR assessment. Furthermore, in clinical settings, this objective measure of DE max has additional advantages as it requires minimum effort in patients and can be applied to the PR programme at home if portable ultrasonography is used. However, the assessment of DE max has a limitation. The procedures pertaining to positioning of patients, breathing patterns, and the selected hemidiaphragm are not standardised at present, which may hamper the routine use of DE max at this moment. Standardisation of these parameters would further facilitate the use of DE max in clinical settings and for research purpose.

There are some limitations to this study. This was a single-centre study involving a relatively small number of participants, and their baseline condition might have been relatively preserved. Nonetheless, 46% of the participants showed FEV 1  < 50%, and the utility of DE max was also observed in these patients with severe airflow limitation. Furthermore, in this study, few patients discontinued the PR programme, except for patients who discontinued during the coronavirus pandemic, which indicates that there was no severe mismatch between the PR programme and the patients’ ability to successfully complete this programme. As another limitation, we did not evaluate any malnutrition factors, which could be an important determinant of diaphragmatic mobility. Nonetheless, DE max was a stronger predictor of the effectiveness of PR than other parameters, including QMS or lung function using multivariate analysis. Further studies with a large number of patients are required, and the utility of DE max should be examined in patients with the most severe form of COPD with a low-intensity load exercise programme.

In conclusion, DE max , which is a reliable and easy to perform measurement, could adequately predict the improvement in exercise tolerance after PR in patients with COPD. Assessment of DE max could aid in making medical decisions associated with therapeutic strategies.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Chronic obstructive pulmonary disease

Dynamic lung hyperinflation

• Pulmonary rehabilitation

6-Min walk distance

Minimal clinically important difference

Forced vital capacity

Forced expiratory volume in 1 s

Maximum inspiratory pressure

Quadriceps muscle strength

COPD assessment test

Low attenuation area

Area under the curve

Receiver operating characteristic

Modified Borg

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Masashi Shiraishi, Yuji Higashimoto, Ryuji Sugiya, Hiroki Mizusawa, Yu Takeda, Shuhei Fujita, Tamotsu Kimura & Kanji Fukuda

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Shiraishi, M., Higashimoto, Y., Sugiya, R. et al. Diaphragmatic excursion is correlated with the improvement in exercise tolerance after pulmonary rehabilitation in patients with chronic obstructive pulmonary disease. Respir Res 22 , 271 (2021). https://doi.org/10.1186/s12931-021-01870-1

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A narrative review of diaphragm ultrasound to predict weaning from mechanical ventilation: where are we and where are we heading?

• Peter Turton   ORCID: orcid.org/0000-0001-7974-3031 1 , 2 ,
• Sondus ALAidarous 1 , 3 &
• Ingeborg Welters 1 , 2  

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The use of ultrasound to visualize the diaphragm is well established. Over the last 15 years, certain indices of diaphragm function, namely diaphragm thickness, thickening fraction and excursion have been established for mechanically ventilated patients to track changes in diaphragm size and function over time, to assess and diagnose diaphragmatic dysfunction, and to evaluate if these indices can predict successful liberation from mechanical ventilation. In the last 2 years, three meta-analyses and a systematic review have assessed the usability of diaphragmatic ultrasound to predict successful weaning. Since then, further data have been published on the topic.

Conclusions

The aim of this narrative review is to briefly describe the common methods of diaphragmatic function assessment using ultrasound techniques, before summarizing the major points raised by the recent reviews. A narrative summary of the most recent data will be presented, before concluding with a brief discussion of future research directions in this field.

There has been much interest in the use of diaphragm ultrasound as a tool of measuring and tracking atrophy, in particular to identify patients who will wean from mechanical ventilation, and who will remain free of ventilatory support afterwards. Two meta-analyses and a systematic review have been published on the topic in the last 2 years, and more work is being produced. The aim of this narrative review is briefly re-iterate what is being measured with diaphragm ultrasound, to summarize the most recent findings from these reviews and meta-analyses, and to provide an update of current work produced after these reviews.

The diaphragm in critical care: what do we know?

The effects of atrophy of the diaphragm secondary to mechanical ventilation have been recently described; Goligher found that the development of diaphragm atrophy was associated with prolonged duration of mechanical ventilation, increased ICU length of stay, and a higher rate of complications [ 1 ]. Interestingly, patients who showed an increase in diaphragmatic thickness during their critical illness were also at higher risk of prolonged mechanical ventilation, with excessive respiratory effort as a possible underlying trigger. The authors did acknowledge that tissue oedema from fluid resuscitation may also contribute to this thickening. Diaphragmatic thickness has been shown to reduce by 6% [ 2 ] or 7.5% [ 3 ] per day in mechanically ventilated patients. However, a further study demonstrated that although nearly half of the patients in their study did suffer atrophy, the same proportion experienced no loss, and a further 10% actually had increases in diaphragmatic thickness [ 4 ]. A recent study in mechanically ventilated children suggested that diaphragmatic atrophy occurs at an average rate of 3.4% per day and is worsened by the use of neuromuscular blockade [ 5 ]. However, two papers failed to demonstrate diaphragmatic atrophy using ultrasound [ 6 , 7 ]. However, one of these studies was in extubated survivors of sepsis (82% of which had either severe sepsis or septic shock) who were approached after a period of at least 5 days of mechanical ventilation, compared to controls. However, the authors concede that these results were based on a single measurement at a point in the patients’ recovery from sepsis rather than during the acute episode.

Ultrasound and the diaphragm

Visualization of the diaphragm with ultrasound has been possible for well over 40 years [ 8 ]. However, only recently diaphragmatic ultrasound has been used to assess diaphragm function and size during mechanical ventilation. There are two commonly used measurements derived from ultrasound: diaphragm excursion and diaphragm thickness [ 9 ]. Diaphragm excursion is usually measured using a phased array probe, with the probe positioned in the subcostal margin in the mid-clavicular line, with the aim of imaging the posterior third of the diaphragm (Fig.  1 ). Although some studies have used B-mode imaging to determine diaphragmatic excursion [ 10 ], the use of M-mode produces images that visualize the movement of the diaphragm over time and allows accurate measurement of diaphragmatic displacement over a respiratory cycle (Figs.  2 and 3 ) [ 11 ]. In healthy volunteers, diaphragmatic excursion is known to vary with sex and height and can be reliably performed in a recumbent or supine position [ 12 ]. Excursion is known to positively correlate with lung inspiratory volumes [ 13 , 14 ], and is higher during forced inspiratory breathing [ 10 ].

Subcostal view of the diaphragm (b) in B-mode at end inspiration (1) and at expiration (2) seen below the liver (a)

Diaphragm excursion as assessed via M-mode ultrasonography, where a is the diaphragm, b is at the end of a deep inspiratory effort, c is at end expiration and d is the liver

M-mode ultrasonography demonstrating three tidal inspiratory efforts ( a ) and a deep inspiratory effort ( b )

Diaphragm thickness is measured in the zone of apposition, using a higher-frequency (> 10 MHz) linear probe, to view the diaphragm as a three-layered structure, sandwiched between the two echogenic layers of the pleura and the peritoneum (Fig.  4 ) [ 15 ]. Both B- and M-mode techniques can be used to measure thickness [ 16 ]. Diaphragm thickness has been previously correlated with the strength of the diaphragm [ 17 ], but not the endurance or fatigability [ 18 ]. It appears to be thicker in an upright position, compared to supine posture [ 19 ], can be measured at expiration or end inspiration, and in both tidal and maximal breathing. Comparing expiratory with inspiratory thickness gives the thickening fraction, which is usually denoted as [(End Inspiratory Thickness − End Expiratory Thickness)/End Expiratory Thickness] [ 20 ] and is an indicator of the work of breathing [ 21 ]. These measurements can be used to form a definition of diaphragm dysfunction, although there is variation in this definition: It has been defined as a thickening fraction of less than 20% or a tidal excursion of less than 10 mm [ 22 ], based on the presence of paradoxical movement in the case of the paralyzed diaphragm [ 9 ], or using non-ultrasound methods such as measurement of twitch pressures [ 23 ]. Regardless, ultrasound techniques have been shown to outperform traditional techniques such as fluoroscopy in diagnosing diaphragm dysfunction [ 24 ].

Diaphragm thickness in B-mode thoracic view at end expiration (1) and inspiration (2) in a heathy volunteer. The diaphragm can be seen between two echogenic layers (a) with the intercostal compartment above (b). The two muscle layers sit between two ribs ( c )

Summary of current literature

In 2017, a systematic review [ 25 ] and a meta-analysis [ 26 ] have been performed, assessing the evidence on diaphragm ultrasound and its ability to predict successful weaning from mechanical ventilation. Two further meta-analyses have been published in 2018 [ 27 , 28 ], and together these reviews assessed the combined work of more than 30 individual papers (excluding further 3 papers that looked exclusively at lung rather than diaphragm ultrasound).

The systematic review [ 25 ] focused on the use of diaphragmatic ultrasound in four key areas: to diagnose diaphragmatic dysfunction, to predict successful weaning from mechanical ventilation, to determine if ultrasound can assess muscular workload against other known measurements such as transdiaphragmatic pressure [ 29 ], and to describe variations in diaphragm atrophy across studies.

With respect to weaning from mechanical ventilation, four studies were analyzed, two of which described diaphragm excursion either by M-mode ultrasound [ 30 ] or by measuring organ displacement [ 31 ]. The two remaining studies assessed diaphragmatic thickening fraction [ 32 , 33 ]. All four studies concluded that their respective measurements can predict successful extubation or weaning failure, with cut-off values of 11–14 mm in excursion and 30–36% in thickening fraction being most sensitive and specific.

The three meta-analyses are broadly similar in their aims and results. A possible reason may lie in the slight differences to the selection criteria; Li et al. reviewed only publications in English and defined weaning failure as the requirement for re-intubation within 48 h, whereas Llamas-Álverez et al. included publications in all languages and had a much broader definition of weaning failure to include death, unscheduled non-invasive ventilation, tracheostomy formation or the failure of a spontaneous breathing trial within 72 h, and Qian defined weaning failure more broadly as a failed spontaneous breathing trial, re-intubation, the use of non-invasive ventilation, or death. Li and Llamas-Álverez found similar AUC characteristics for the use of diaphragm thickening fraction (0.83 versus 0.87). Llamas-Álverez et al. concluded that thickening fraction may help to predict weaning failure, and Li et al. concluded that the either measurement is suitable to predict successful extubation. Qian found that pooled specificity for predicting weaning success was similar to the work of Llamas-Álverez, and also found that weaning failure was higher in the presence of diaphragmatic dysfunction, and that both excursion and thickening fraction were higher in patients who were successfully weaned.

All papers acknowledge the heterogeneity in the studies analyzed. The definition of weaning failure varied amongst individual studies, with re-intubation limits set at either 48 or 72 h, and some studies included the use of non-invasive ventilation to define weaning failure. Inclusion criteria are different for each of the studies; while some studies recruited patients during their first spontaneous breathing trial [ 32 ], another study included only patients who had already had a failed trial [ 33 ]. Further differences arise from the ultrasonic technique chosen; in Li’s meta-analysis, 4 of the studies were conducted with the patient in a supine position, while patients were semi-recumbent in the remaining 9 studies. Although probe position was consistent in all studies, probe frequency and ultrasound machine manufacturer varied considerably, with 12 different types of ultrasound machines being used, covering a range of frequencies from 3.5 to 10 MHz. There is also variation in the patient populations, particularly with respect to age and sex. It is known that age negatively correlates with excursion in deep breathing, and that females have less diaphragmatic excursion [ 12 ]. Many of the studies included both left and right sides of the diaphragm, but some reported measurements of the right side only, probably because there is greater difficulty in imaging the left diaphragm due to the lung obscuring the view [ 13 ]. Finally, there is variation regarding the time point during a spontaneous breathing trial at which measurements are taken, with ultrasound images being obtained at the start or end of spontaneous breathing; some investigators assessed diaphragmatic function after extubation, others during mechanically ventilation with further variation in the ventilatory mode used. It has been suggested that pre-extubation is the best time to perform diaphragm ultrasound to assess the diaphragm at a time point when it may be fatigued. A protocol for a new study performing ultrasounds at regular intervals throughout 2 h of spontaneous breathing has been published, but the results are not yet available [ 34 ].

Where are we now?

Since the publication of the systematic reviews, several studies have reported diaphragmatic ultrasound parameters as a means of predicting extubation success. Our search strategy used MEDLINE only; we searched for papers published after 1st January 2017 until to the current date of writing (August 2018). Using the search string (Ultraso* AND Diaphagm* AND (critical* OR intensive OR sepsis OR mechanical * OR ventilat*) yielded 89 results. After having excluded papers that already appeared in the four systematic reviews and papers covering different topics as assessed on title and/or abstract), we identified 18 new papers since 2017 that have not been part of a systematic review.

Newer studies

Newly identified studies can be divided into three categories. In the first, there are studies in which diaphragm thickening or excursion are used alone to predict successful weaning. In the second, diaphragm ultrasound is compared to another technique; and in the third, these techniques are combined to see if they increase predictive accuracy.

A recent study describes cut-offs for diaphragm thickening to predict successful weaning prior to a spontaneous breathing trial [ 35 ]. Its results are in keeping with previously established cut-offs for patients weaning from pressure support [ 36 ]. However, there are also conflicting results. For example, a study evaluating diaphragm excursion using spleen and liver displacement found that displacement of the organs by 1.2 cm was the best cut-off for predicting successful extubation [ 37 ]. However, poor agreement between solid organ movement and diaphragm excursion has been described before [ 38 ]. Another recent study found that diaphragmatic excursion, and not thickening fraction, was the best predictor of extubation failure in patients undergoing their first spontaneous breathing trial [ 39 ]. The most recent reliability study has established values of inter- (0.987) and intra-observer variability (0.986) that are within the higher range of Intra Class Correlation (ICC) coefficients established in the systematic review [ 40 ].

Newer studies—comparative approaches

Dres and colleagues compared the performance of diaphragm ultrasound against tracheal pressure measurements obtained during supra-maximal phrenic nerve stimulation during a spontaneous breathing trial [ 23 ]. They not only found that a lower stimulated pressure than previously accepted was associated with optimum sensitivity and specificity for liberation from mechanical ventilation [ 41 ], but also described that a thickening fraction of greater than 25.8% gave equivalent accuracy of prediction in comparison to phrenic nerve stimulation, with AUC–ROC values of 0.80 and 0.82 for phrenic nerve stimulation and diaphragm thickening fraction, respectively.

Newer studies—combined approaches

Combining diaphragmatic ultrasound with echocardiography may be a promising route for prediction of successful weaning, particularly in view of potential cardiac causes for a failed respiratory wean [ 42 ]. The ratio of mitral Doppler inflow velocity (E) to annular tissue Doppler wave velocity (Ea, E /Ea ratio) has been measured with transthoracic echocardiography alongside diaphragmatic excursion in patients who were extubated after a successful spontaneous breathing trial (SBT) [ 43 ]. The authors found that respiratory failure within 48 h of extubation could be predicted from both E /Ea and left ventricular ejection fraction values, but that reintubation within a week of extubation was more accurately predicted by diaphragmatic excursion.

Another study combined echocardiography with lung ultrasound and assessment of diaphragmatic excursion to assess if all three combined could predict extubation failure in patients undergoing a trial of pressure support ventilation [ 44 ]. The results were confirmed in a smaller sub-study of patients breathing via a T-tube, although out of the three modalities, diaphragm ultrasound contributed least predicting successful weaning. Furthermore, a recent small observational study has combined echocardiography and lung ultrasound for assessment of aeration with diaphragmatic ultrasound, and reported that lung aeration and markers of diastolic dysfunction were the only strong predictors of successful extubation [ 45 ].

Another combined approach combined diaphragm thickening fraction with the Rapid Shallow Breathing Index (RSBI). First described in 1991 [ 46 ], RSBI is defined as the ratio of the respiratory frequency to the tidal volume [ 47 ], with a cut-off value of 100–105 breaths/min/liter being associated with successful extubation [ 46 , 48 ]. A recent study found that RSBI alone, in comparison to measurements derived from diaphragm ultrasound, was most accurate in predicting success of extubation, with an ROC–AUC of 0.96 and a sensitivity and specificity of 100% [ 49 ]. This supports earlier work that the sensitivity, specificity and positive predictive value of a thickening fraction cut-off 36% were comparable to RSBI, but ultimately lower than it [ 33 ]. However, the combination of RSBI with diaphragm thickening fraction of greater than 26% was a more accurate predictor of successful weaning from mechanical ventilation than RSBI alone [ 50 ]. The authors concluded that thickening fraction of the right diaphragm alone was as accurate as this combined approach, and suggested that thickening fraction could replace RSBI as the most commonly used weaning parameter in the future.

Future directions

As ultrasound technology progresses, it may be possible for clinicians to estimate diaphragm thickness and excursion using portable, hand-held devices. A recent study used both linear and phased arrays probes of a hand-held ultrasound device to assess diaphragmatic thickness and excursion, respectively, compared to a standard ultrasound device [ 22 ]. Good agreement was noted between the two devices, with ICCs of greater than 0.9 noted in all indices of measurement except for maximal excursion. Based on a definition of diaphragmatic dysfunction as tidal excursion of less than 10 mm, the detection of dysfunction was comparable between the two devices, and good inter-rater reliability was also seen. Stronger agreement between the two devices was seen in the measurement of diaphragm thickness compared to measurement of excursion, possibly because of the hand-held device lacking an M-mode for accurate measurement of excursion.

A third measurement, the contraction velocity, has also been evaluated recently. Contraction velocity is an extension of diaphragm excursion, dividing excursion by the time to reach maximal excursion [ 9 ]. None of the systematic reviews assessed contraction velocity in the prediction of successful weaning. A study of elderly ventilated patients found that right-sided contraction velocity had a similar AUC as right-sided excursion (labeled in the study as diaphragmatic motion), and that both of these were more predictive for successful weaning from mechanical ventilation than RSBI [ 51 ]. Contraction velocity has been shown to have high sensitivity and specificity, and only performed slightly worse than RSBI in a study of younger patients [ 49 ]. A more recent study, however, found that there was no difference in contraction velocity between patients who were successfully extubated, compared to those who were re-intubated [ 52 ]. It is not clear why there is such variation in results, and further research on conduction velocity is required, along with standardization whether velocity is measured over tidal or maximal inspiratory efforts. The same authors found that multiplying the diaphragmatic excursion ( E ) by the inspiratory time ( I ) to give a diaphragmatic excursion-time index gave values that were significantly higher in patients who had been successfully extubated compared to those who failed extubation [ 53 ]. The differences were still significant regardless as to whether the measurements were performed during spontaneous breathing or after extubation. However, significance was lost during pressure-assist ventilation modes.

Speckle tracking can detect tissue motion and distortion [ 54 ]. In healthy volunteers, it has been used to successfully assess diaphragmatic strain under pressure support ventilation [ 55 ] and was weakly but significantly associated with caudal diaphragm displacement [ 56 ]. This technique may provide useful information about the diaphragm during controlled mechanical ventilation, but as yet, there are no studies examining speckle tracking in the critical care population. Similarly, an “area method” [ 57 ] assessing diaphragm motion in two dimensions, correlates with lung volume using both B and M-mode ultrasound in healthy volunteers, and can be performed on both sides of the chest.

Further research focuses on the prediction of successful extubation in particular patient groups. For example, a recent study demonstrated that diaphragm thickness measured before anesthetic induction correlates with time to extubation in patients undergoing liver transplants. Time to extubation after the procedure was higher in patients with pre-operative end expiratory diaphragm thickness of less than 2 mm [ 58 ].

In patients with Chronic Obstructive Pulmonary Disease (COPD), diaphragmatic ultrasound may predict successful weaning on one side, but could also serve to predict success of non-invasive ventilation. In this context, it has been reported that COPD patients with diaphragm dysfunction (diagnosed by a thickening fraction of less than 20%), who require non-invasive ventilation, were 4.4 times more likely to need intubation, more often proceeded to tracheostomies, and had increased length of stay in ICU and hospital mortality [ 59 ]. These results were in line with an earlier smaller study that also described an association of diaphragm dysfunction with Non-Invasive Ventilation (NIV) failure and increased mortality [ 60 ]. However, reduced diaphragmatic thickening itself is not a risk factor for acute exacerbation of COPD [ 61 ].

Diaphragmatic ultrasound has been extensively studied as a predictor of successful weaning from mechanical ventilation, and continues to be studied. It remains difficult to draw general conclusions from individual studies due to the marked variation in study design and population. Even, definitions such as a failed breathing trial or failed extubation have not been standardized across studies, rendering comparison between outcome measures impossible. As yet, defined cut-offs for measurements of diaphragmatic ultrasound have been agreed, and there are no randomized control trials available. Although diaphragmatic ultrasound is a promising diagnostic tool, greater standardization of protocols, outcome measures and ventilatory settings is required for further research and clinical application.

Abbreviations

area under the curve

area under the curve (receiver-operator characteristic)

Chronic Obstructive Pulmonary Disease

intra-class correlation coefficient

intensive care unit

non-invasive ventilation

spontaneous breathing trial

Rapid Shallow Breathing Index

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PT wrote and devised the manuscript. SA provided the ultrasound images for the figures and assisted in the literature search. IW assisted in the editing and writing of the manuscript. All authors read and approved the final manuscript.

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Peter Turton, Sondus ALAidarous & Ingeborg Welters

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Peter Turton & Ingeborg Welters

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Turton, P., ALAidarous, S. & Welters, I. A narrative review of diaphragm ultrasound to predict weaning from mechanical ventilation: where are we and where are we heading?. Ultrasound J 11 , 2 (2019). https://doi.org/10.1186/s13089-019-0117-8

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• Muscle atrophy
• Diaphragm ultrasound
• Thickening fraction

Comparison of clinical utility between diaphragm excursion and thickening change using ultrasonography to predict extubation success

Affiliations.

• 1 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Korea.
• 2 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Gyeongsang National University Hospital, Jinju, Korea.
• PMID: 29050461
• PMCID: PMC5840594
• DOI: 10.3904/kjim.2016.152

Background/aims: Both diaphragmatic excursion and change in muscle thickening are measured using ultrasonography (US) to assess diaphragm function and mechanical ventilation weaning outcomes. However, which parameter can better predict successful extubation remains to be determined. The aim of this study was to compare the clinical utility of these two diaphragmatic parameters to predict extubation success.

Methods: This study included patients subjected to extubation trial in the medical or surgical intensive care unit of a university-affiliated hospital from May 2015 through February 2016. Diaphragm excursion and percent of thickening change (Δtdi%) were measured using US within 24 hours before extubation.

Results: Sixty patients were included, and 78.3% (47/60) of these patients were successfully extubated, whereas 21.7% (13/60) were not. The median degree of excursion was greater in patients with extubation success than in those with extubation failure (1.65 cm vs. 0.8 cm, p < 0.001). Patients with extubation success had a greater Δtdi% than those with extubation failure (42.1% vs. 22.5%, p = 0.03). The areas under the receiver operating curve for excursion and Δtdi% were 0.836 (95% confidence interval [CI], 0.717 to 0.919) and 0.698 (95% CI, 0.566 to 0.810), respectively ( p = 0.017).

Conclusions: Diaphragm excursion seems more accurate than a change in the diaphragm thickness to predict extubation success.

Keywords: Diaphragm; Excursion; Extubation; Thickness; Ultrasonography.

Publication types

• Comparative Study
• Airway Extubation* / statistics & numerical data
• Diaphragm / diagnostic imaging*
• Diaphragm / physiopathology
• Middle Aged
• Prospective Studies
• Retrospective Studies
• Ultrasonography
• Ventilator Weaning / statistics & numerical data

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• v.10(4); Oct-Dec 2020

Ultrasonographic Assessment of Diaphragmatic Excursion and its Correlation with Spirometry in Chronic Obstructive Pulmonary Disease Patients

Mahvish qaiser.

Department of Rehabilitation Sciences, SNSAH, Jamia Hamdard, India

Abhinav Jain

1 Department of Radiodiagnosis, Hamdard Institute of Medical Sciences and Research, New Delhi, India

Introduction:

Chronic obstructive pulmonary disease (COPD) is a common disease. Spirometry is a standard method of assessment of severity of COPD. We evaluate utility of diaphragmatic excursion using ultrasonography in COPD patients and compare this technique with spirometry.

Twenty-six COPD patients and 18 self-reported healthy controls were included in this study. After taking the sociodemographic data, measurement of diaphragm excursion was done using M-mode and B-mode ultrasound. Lung function was assessed by spirometry.

In the COPD group, diaphragmatic excursion was found to be reduced, and it correlates with forced expiratory volume in 1 s (FEV1)/forced vital capacity, whereas it did not correlate with FEV1.

Conclusion:

Ultrasound assessment of diaphragmatic excursion is an easy, noninvasive, and readily available diagnostic tool and correlates with spirometry in estimation of severity of COPD.

Introduction

Chronic obstructive pulmonary disease (COPD) is a common preventable and treatable disease as per the Global Initiative for Chronic Obstructive Lung Disease (GOLD) and is characterized by persistent respiratory symptoms and airflow limitation that is due to airway and/or alveolar abnormalities usually caused by significant exposure to noxious particles or gases.[ 1 ]

According to the GOLD report, COPD is projected to be the third leading cause of death by 2020, and currently, it is the fourth.[ 2 , 3 ] The Global Burden of Disease Study done in 2013 attributed COPD as the cause of death for >3 million people that constitutes 6% of all deaths globally.[ 2 ] A review of the published reports revealed 384 million cases of COPD in 2010 which is 11.7% globally.[ 4 ] This makes COPD a leading cause of morbidity and mortality, thus causing huge economic and social burden on the society.[ 3 , 5 ] As per the WHO estimates, 90% of COPD-related deaths occur in developing countries. India and China alone account for 66% of global COPD mortality which is approximately 33% of the total human population.[ 6 , 7 ]

COPD impairs the function of diaphragm muscle which is the primary muscle of inspiration. Diaphragm provides 75% of the increase in lung volume during quiet inspiration.[ 8 ] Movement of diaphragm during breathing is called diaphragm mobility. Movement of diaphragm from end-expiration to full inspiration is known as diaphragm excursion.

Diaphragmatic mobility has been found to be lower in patients with COPD than in healthy elderly individuals due to hyperinflated chest.[ 9 ] COPD patients with thoracic hyperkyphosis have lower diaphragm mobility than those without it. An increase in kyphosis angle decreases the diaphragmatic mobility.[ 10 ]

Ultrasonography is a cost-effective, radiation-free, widely available, and real-time investigation.[ 11 ] Many studies have proposed the possible use of ultrasonography to measure the diaphragmatic excursion.[ 11 , 12 , 13 , 14 ] Although, the literature is limited. Spirometry is a noninvasive, easy, and valid tool for COPD assessment. There are established criteria based on spirometry, according to which COPD can be classified as mild, moderate, severe, and very severe.[ 1 , 9 ] Our study evaluates the diaphragmatic excursion on the basis of preestablished protocols and compares the outcome with the spirometry results. This study explores a new opportunity of using standard ultrasonography as a tool to establish the diagnosis of COPD and assess the severity of the same.

Materials and Methods

The study was conducted between January and April 2020 at a tertiary care hospital. Forty-four study participants were recruited from chest OPD of our hospital after their due informed consent. Out of these, 26 were COPD patients who were labeled as study group and 18 were non-COPD patients who were labeled as control group. For the COPD group, only those patients who did not require oxygen supplementation and were clinically stable were recruited. Both smokers and nonsmokers were recruited in both the groups.

The exclusion criteria included any patient with recent COPD exacerbation in the last 3 months, patients with comorbidities such as cardiac disease, pulmonary fibrosis, or ankylosing spondylitis, or patients who were unable to understand and perform the test.

All these patients underwent spirometry and ultrasonographic assessment of diaphragmatic excursion on the same day as per the below-mentioned protocol. These patients and controls were randomized so that the spirometry observer and radiologist were blinded for the cases and controls.

All participants underwent a detailed postbronchodilator spirometry examination using a calibrated Spirolab III MIR Spirometer in sitting position. Spirometry was performed thrice by experienced technicians at our pulmonary function laboratory. Patients were asked to take a maximal inspiration and then to forcefully expel air for as long and as quickly as possible. Results were recorded and saved for statistical analyses.[ 15 ]

Ultrasonography

Ultrasound assessment of diaphragmatic excursion was done by experienced ultrasonologists. Diaphragmatic excursion for patients was measured on GE make, Voluson S8 series ultrasound machine. The assessment was done in supine position using M-mode and B-mode techniques in quiet and deep breathing scenarios. For M-mode assessment, the transducer was placed in the subcostal region at the midclavicular line with probe tilted cranially, and for B-mode assessment, patients were scanned by placing the transducer in the subcostal region at the midclavicular line with probe tilted horizontally[ 12 , 13 ] [ Figure 1 ]. Ultrasonologists were blinded about the spirometry results.

Ultrasound images on diaphragm (arrow). (a) M-Mode scan done at the midclavicular line to assess diaphragmatic motility. (b) B-Mode acquisition shown here as a still from cine-loop image obtained to measure diaphragmatic excursion

Sample size calculation

The sample size required for 40+ years of age group COPD in our district is 1,000,000 individuals which was calculated based on the assumption that the lowest prevalence of COPD in our district is about 4.75% with an absolute precision of 5%, CI of 80%, and design effect as 1.[ 6 , 15 , 16 ]

Sample size formula n = (DEFF * N*p*q]/[(d2/Z2 1-α/2* (N-1) +p*q].

Statistical analysis

Data was analyzed using IBM SPSS statistical package for Linux version 16.0. Bangalore, India. Demographic data were analyzed using independent samples t-test. Diaphragmatic excursion and lung function were analyzed by an independent t-test. To analyze the relationship between lung function and diaphragmatic excursion, Karl Pearson's correlation coefficient test was used. The level of significance was <0.05 ( P < 0.05).

Forty-eight participants were included in the study. Out of those, 30 were COPD and 18 were non-COPD. Four COPD patients were dropouts. Therefore, their data were not included in this study. Nineteen were male COPD and 11 were healthy male. The rest of them are females. Table 1 shows the mean and standard deviation of different variables in both the groups.

Mean and standard deviation data of study and control groups

FEV 1 : Forced expiratory volume in 1 s; FVC: Forced vital capacity, DE: Diaphragmatic excursion

Independent t -test between the groups revealed that diaphragmatic mobility and lung function are reduced in COPD patients than healthy controls with level of significance <0.01 ( P < 0.01).

Pearson's correlations between diaphragmatic excursion and lung measurements showed a positive strong correlation between forced expiratory volume in 1 s/forced vital capacity (FEV1/FVC) with M-mode ( r = 0.75) [ Table 2 and Figure 2 ] and B-mode ( r = 0.85) in the study group [ Table 3 and Figure 3 ], but this relationship was not found in control controls. There is a weak correlation between FEV1 and M-mode in the study group. There is a strong correlation between M-mode and FEV1 ( r = − 0.50) in the control group.

Relationship between diaphragmatic excursion (M-mode) and variables in study group

FEV 1 : Forced expiratory volume in 1 s; FVC: Forced vital capacity, SD: Standard deviation

Correlation between forced expiratory volume in 1 s/forced vital capacity and M-mode in study group

Relationship between diaphragmatic excursion (B-mode) and variables in study group

Correlation between forced expiratory volume in 1 s/forced vital capacity and B-mode in experimental group

Finally, we observed that diaphragmatic excursion was significantly reduced in the study group than controls ( P < 0.05). Spirometry measurements showed a significant difference between the groups. FEV1/FVC is significantly reduced in COPD [ Table 1 ].

The study establishes that COPD affects diaphragmatic excursion and lung function. We found that diaphragmatic excursion was reduced in COPD than controls. Decreased diaphragmatic excursion shows that contractile ability of diaphragm is reduced in COPD.

The reason of reduced contractility lies in the pathophysiology of the disease. COPD includes bronchitis and emphysema which cause airway obstruction and air trapping in the lungs. Normally, diaphragm moves caudally during inspiration and cranially during expiration. COPD can cause hyperinflation of the lungs, and therefore, diaphragm shifts caudally. This causes mechanical disadvantage of the diaphragm muscle.[ 1 ] Previous studies revealed that reduced diaphragmatic mobility is associated with increased perception of dyspnea. Structural changes cause flattening of the diaphragm which reduces their ability to move cranially and caudally.[ 9 , 10 , 12 ]

Another important outcome of this study is the correlation between sonographic assessment of diaphragmatic excursion and spirometry results. In the present study, we found that diaphragmatic excursion strongly correlates with FEV1/FVC and weakly correlates with FEV1 in the study group. These findings corroborate those of Rocha et al ., who found that diaphragmatic mobility is related to pulmonary parameters (FEV1, FEV1/FVC, FVC, IC, and MVV).[ 9 ] Progression of the disease causes shortening of diaphragm fibers and decreases resting diaphragm muscle length. This causes a decrease in their ventilator capacity and lung function.

COPD causes inflammation and obstruction of the airways that lead to air trapping in the alveoli. As the severity of the disease increases, lung function decreases. COPD can cause hyperkyphosis in later stage which reduces the expansion of the chest wall. A study proved that diaphragmatic mobility is correlated with kyphotic angle.[ 10 ] Hence we can say COPD affects diaphragmatic mobility and lung function.

The limitation of the present study is that only two Stage 4 COPD patients were involved because most of them came to chest OPD with acute exacerbation. Another limitation is that only right hemidiaphragm was assessed on ultrasonography.

Further studies with larger number of patients, especially with severe COPD (Stage 4), would be required covering wider geographical areas for standardized guidelines on assessment of diaphragmatic excursion in COPD patients.

This study describes the use of ultrasonography for assessing the diaphragmatic excursion. Sonographically determined diaphragmatic excursion strongly correlates with FEV1/FVC. Both the B-mode and M-mode approaches can be used to measure the diaphragmatic excursion, and these correlate well with the severity of COPD.

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Conflicts of interest.

There are no conflicts of interest.