|Year : 2019 | Volume
| Issue : 3 | Page : 709-714
The interoperator agreement and reliability of measurement of diaphragmatic movement by ultrasonography in patients with chronic obstructive pulmonary disease
Yasmeen M Elkabany1, Amani Ezz-Elarab2, Zeinab Adawy2, Eman Sobh2
1 Department of Chest Diseases, Police Hospital, Cairo, Egypt
2 Department of Chest Diseases, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt
|Date of Submission||19-Oct-2019|
|Date of Decision||19-Oct-2019|
|Date of Acceptance||29-Oct-2019|
|Date of Web Publication||10-Feb-2020|
M.D Eman Sobh
Chest Diseases Department, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt; Chest Diseases Department, Al-Zahraa University Hospital, 11517 Al-Abbaseya, Cairo
Source of Support: None, Conflict of Interest: None
Introduction Diaphragmatic motion (excursion) measurement by ultrasonography (US) has been used to evaluate diaphragmatic functions in several conditions including chronic obstructive pulmonary disease (COPD). The main limitation of US is that it is operator dependent.
Aim The aim of this study was to assess the intraoperator and interoperator agreement and reliability of US measurement of diaphragmatic movement in COPD by pulmonologists.
Patients and methods This study included 50 patients with COPD between May 2017 and August 2017 in a tertiary hospital. Readings of diaphragmatic excursion were recorded separately during inspiration and expiration using B-mode US. All measurements were recorded by two operators: one experienced and one MD student who received training to perform diaphragm US. Mean and SD of variation and intraclass correlation coefficient (ICC) in the measurement were calculated for assessment of variability and reliability, respectively.
Results Fifty patients with COPD were included in the study. The mean difference between the readings of both operators was 0.014±0.094 for quiet breathing, −0.0102±0.058 for deep breathing, and −0.0598±0.430 for sniffing, and this difference was statistically nonsignificant. There was good to excellent agreement between both operators for all readings (intraclass coefficient values were 0.998, 0.999, and 0.901 for quiet breathing, deep breathing, and sniffing, respectively). Three readings were taken by the same operator during different phases of breathing (tidal, deep, and sniffing), and Cronbach’s α for readings of operator A were 0.968, 0.935, and 0.983 for quiet breathing, deep breathing, and sniffing, respectively, and 0.995, 0.948, and 0.980 for quiet breathing, deep breathing, and sniffing, respectively, by operator B, which indicate excellent reliability.
Conclusion The measurement of diaphragmatic excursion using US in patients with COPD was reproducible and reliable test in all breathing phases when performed by pulmonologists.
Keywords: chronic obstructive pulmonary disease, diaphragmatic excursion, reliability, ultrasonography, variability
|How to cite this article:|
Elkabany YM, Ezz-Elarab A, Adawy Z, Sobh E. The interoperator agreement and reliability of measurement of diaphragmatic movement by ultrasonography in patients with chronic obstructive pulmonary disease. Sci J Al-Azhar Med Fac Girls 2019;3:709-14
|How to cite this URL:|
Elkabany YM, Ezz-Elarab A, Adawy Z, Sobh E. The interoperator agreement and reliability of measurement of diaphragmatic movement by ultrasonography in patients with chronic obstructive pulmonary disease. Sci J Al-Azhar Med Fac Girls [serial online] 2019 [cited 2020 Oct 22];3:709-14. Available from: http://www.sjamf.eg.net/text.asp?2019/3/3/709/278051
| Introduction|| |
In recent years, there has been marvelous growth in clinician-performed ultrasonography (US) in several specialties . US training is essential for clinical practice ,. It is important to evaluate variability and reliability of all personnel involved in data acquisition in clinical research as well as the learning curve of the trainee. US has gained interest in respiratory disorders and now is considered an important tool for pulmonologist . Diaphragmatic dysfunction is common in patients with chronic obstructive pulmonary disease (COPD) . Assessment of diaphragmatic function was reported to be useful in respiratory setting . The tools available for assessment of diaphragmatic function are either associated with risk of radiation (fluoroscopy or computed tomography) or are too complex (transdiaphragmatic pressure measurement, phrenic nerve stimulation, and electrophysiology) ,,. US has emerged as an effective tool to study diaphragm thickness and excursion in healthy populations as well as in different disease conditions . US is safe, can be used at bedside, and is radiation free. However, the main limitation of US is that it is operator dependent . It is important to assess operators’ variability as part of quality control . So, the aim of this study was to assess the intraoperator and interoperator agreement among operators in our research team before conducting a study involving diaphragmatic function in COPD.
| Patients and methods|| |
This prospective observational cross-sectional study was performed at Chest Diseases Department, Al-Zahraa University Hospital, Cairo, Egypt, from May 2017 to August 2017.
The study protocol was approved by the Institutional Ethical Review Board of the Faculty of Medicine for Girls, Al-Azhar University (FMG-IRB), and informed consent was obtained from all participants before inclusion in the study.
Operator one is experienced at performing diaphragm ultrasound and operator two is an MD student without prior US training who received training during the study period for performing diaphragm US for thesis project (training included attending 6-h training basic thoracic US workshop, 3 h training on diaphragm US and 3 weekly observation, and training for 1 month at our Department Ultrasonography Unit). Each operator evaluated the same measurements independently and was blind to the results obtained by the other operator.
Inclusion and exclusion criteria
We studied 50 patients with stable COPD for diaphragm US to assess diaphragmatic excursion during quiet breathing, deep breathing, and sniffing. Diagnosis of stable COPD was based on Global Initiative for Chronic Obstructive Lung Disease (GOLD) criteria . Spirometry was used according to American Thoracic Society/European Respiratory Society (ATS/ERS) guidelines  using the device Spirosift spirometry 5000 Fukuda Nenshi, Japan, and postbronchodilator forced expiratory volume in first second/forced vital capacity % less than 70%, with an increase in forced expiratory volume in first second less than 200 ml or less than 12% of baseline value, 15–20 min after 4 puffs (400 µg) of inhaled salbutamol via a metered-dose inhaler, and not experiencing acute exacerbation at time of the study . All patients who had history of recent abdominal or thoracic operation, neuromuscular disease, previous cerebrovascular stroke, or had significant comorbid illness were excluded from the study.
Diaphragmatic US was done in the supine position using Sonoscape A8 Medical Systems, Shenzhen, China, supplied with curvilinear probe (3–5 MHz) (Nanshan, China) to assess the diaphragmatic function and structure . We used a combined image with Brightness-mode (B-mode) for examination of diaphragmatic shape and position ([Figure 1]) and Motion-mode (M-mode) to assess diaphragmatic movement (excursion) in quiet breathing, deep breathing, and sniffing ([Figure 2]). The examiner applied a layer of gel to the site to be examined and then he placed the probe on the skin on the right subcostal region and searched for the right hemidiaphragm . The right hemidiaphragm was visualized through the liver as a white echogenic line moving up and down with respiration , as seen in [Figure 1]. Diaphragmatic excursion, which represents the diaphragmatic movement during breathing, was measured as the distance difference between the same peak and baseline of the diaphragmatic wave and was recorded in cm ([Figure 3]). Three consecutive measurements of each parameter were taken by the two examiners.
|Figure 2 Diaphragm excursion (M-mode) during tidal breathing, deep breathing, and sniffing.|
Click here to view
Assessment of intraoperator variability was as follows: three readings were taken by the same operator during different phases of breathing (tidal, deep, and sniffing) and analyzed for intraoperator reliability.
Assessment of interoperator variability was as follows: the two operators measured diaphragmatic excursion during different phases of breathing (tidal, deep, and sniffing) independently and analyzed for interoperator variability.
The diaphragmatic excursion was recorded by each examiner and coded, and statistical analysis was done using Statistical Package for the Social Sciences version 15 (SPSS; IBM Corp., Armonk, New York, USA). Mean and SD were calculated for each reading, and for variation among multiple readings, paired-samples t-test was used to calculate difference between readers. The intraclass correlation coefficient (ICC) was calculated for the assessment of intrarate and inter-rate reproducibility between learner and expert . Intraoperator reliability was assessed by the ICC. The confidence interval (CI) was set to 95%, and the margin of error accepted was set to 5%. Level of significance was considered at P value less than 0.05. ICC estimates and their 95% confident intervals were calculated using SPSS statistical package version 23 (SPSS Inc., Chicago, Illinois, USA) based on a mean rating (k=2), absolute agreement, and two-way mixed-effect model. ICC values less than 0.5 are indicative of poor reliability, values between 0.5 and 0.75 indicate moderate reliability, values between 0.75 and 0.9 indicate good reliability, and values greater than 0.90 indicate excellent reliability.
| Results|| |
The demographic data and basic characteristics of the studied patients with COPD are present in [Table 1]. The mean age was 59.32±7.84 years, and most of them were male (92%).
An interoperator reliability analysis using the Cronbach’s α statistic was performed to determine consistency among operators. We obtained ICC value OF 0.998; its 95% CI ranges between 0.997 and 0.999 for DET between operator A and B, indicating excellent reliability. Using a single measure will result in ICC of 0.996, with 95% CI ranging from 0.993 to 0.998, indicating also excellent reliability. For deep DED, using single reader will result in ICC of 0.999, with 95% CI from 0.998 to 0.999, indicating excellent reliability. For sniffing, using single reader will result in ICC of 0.901, with 95% CI from 0.803 to 0.943 (the level of reliability is ‘good’ to ‘excellent’).
Assessment of intraoperator variability was as follows: three readings were taken by the same operator during different phases of breathing (tidal, deep, sniffing), and Cronbach’s α values for readings of operator A were 0.968, 0.935, and 0.983 for quiet breathing, deep breathing, and sniffing, respectively, and were 0.995, 0.948, and 0.980 for quiet breathing, deep breathing, and sniffing, respectively, as presented in [Table 2], which indicate excellent reliability.
|Table 2 Intraoperator reliability testing revealed excellent reliability of both operators for all readings of diaphragmatic excursion by ultrasonography|
Click here to view
Conclusion and recommendation
In recent years, US has been proven to be a useful tool for pulmonologists. The use of US in daily clinical practice is increasing . Diaphragm ultrasound can evaluate movement and muscle thickness. In patients with COPD, diaphragmatic function is related to disease progression and to the degree of dyspnea and hyperinflation. The main limitation of ultrasound is that it is operator dependent . For that reason, to conduct a good clinical practice, it is mandatory to receive proper training and to evaluate the reliability and agreement among different operators . Before conducting research and clinical practice, assessment of the degree of agreement between operators and the reliability of the test should be carried out ,,; therefore, the aim of this study was to evaluate agreement between the two operators and to test the reliability and reproducibility of US for measurement of diaphragmatic excursion. In this study, we used intraclass coefficient test as our variables are continuous variables. Previous studies assessed diaphragm movement using fluoroscopy and radiography ,, and MRI  and were found to be reliable and reproducible; however, they either carry the risk of radiation exposure or are expensive and time-consuming. The slow speed of MRI hinders the analysis of diaphragm movement . The size and precautions required for radiography and magnetic resonance hinder the frequent daily use in clinical practice and for research work. Ultrasound is a safe, radiation-free, bedside test that gives real-time visualization of diaphragmatic structure and/or movement .In the current study after proper training, we found an excellent interoperator agreement for measurement of diaphragmatic excursion in different breathing patterns ([Table 1] and [Table 3]). At the same time, intraoperator reliability was good to excellent ([Table 4]). The difference between the readings of both operators was nonsignificant, indicating a reliable test. These results also indicate that every single reading by any of the two operators will be reliable and that researcher measurement is a valid reading.
|Table 3 Diaphragm excursion in different breathing patterns by the two operators|
Click here to view
|Table 4 Intraclass correlation coefficient values of the readings of the diaphragmatic excursion during all breathing patterns between the two operators|
Click here to view
The same results were reported by Grams et al.  who reported that ultrasound assessment of diaphragmatic movement is a reliable test; however, the ICC was lower than this study. They explained this by the learning effect and the difference in practice like pressure applied to skin. In fact, the time consumed during learning in this study makes greater effect in improving agreement between operators in our study.
The results of this study indicate that US of the diaphragm is a simple method that can be easy to learn, and the test is reliable and reproducible.
In conclusion, diaphragm ultrasound is easy to learn, and after proper training, inter-operator reliability and intraoperator reliability are excellent. US is a reliable and reproducible test for diaphragmatic excursion. US is a cheap test, is readily available, and gives immediate results. Diaphragm assessment is crucial in patients with COPD, especially those on mechanical ventilation.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Jeanmonod R, Stawicki SP, Bahner DP, Zago M. Advancing clinician-performed sonography in the twenty-first century: building on the rich legacy of the twentieth century pioneers. Eur J Trauma Emerg Med
Mullaney PJ. Qualitative ultrasound training: defining the learning curve. Clin Radiol
Pinto J, Azevedo R, Pereira E, Caldeira A. Ultrasonography in gastroenterology: the need for training. GE-Portuguese J Gastroenterol
El-Naggar T, Sharkawy SH, Abdel-Hamid HM, Mohamad HS, Mohamed RM. Role of chest ultrasonography in differentiating between acute cardiogenic pulmonary edema and acute respiratory distress syndrome. Egypt J Bronchol
Gea J, Pascual S, Casadevall C, Orozco-Levi M, Barreiro E. Muscle dysfunction in chronic obstructive pulmonary disease: update on causes and biological findings. J Thorac Dis
Yoo JW, Lee SJ, Lee JD, Kim HC. Comparison of clinical utility between diaphragm excursion and thickening change using ultrasonography to predict extubation success. Korean J Intern Med
Doorduin J, van Hees HW, van der Hoeven JG, Heunks LM. Monitoring of the respiratory muscles in the critically ill. Am J Respir Crit Care Med
Heunks LM, Doorduin J, Van Der Hoeven JG. Monitoring and preventing diaphragm injury. Curr Opinion Crit Care
Saeed AM, El Assal GI, Ali TM, Hendawy MM. Role of ultrasound in assessment of diaphragmatic function in chronic obstructive pulmonary disease patients during weaning from mechanical ventilation. Egypt J Bronchol
Fayssoil A, Behin A, Ogna A, Mompoint D, Amthor H, Clair B et al.
Diaphragm: pathophysiology and ultrasound imaging in neuromuscular disorders. J Neuromusc Dis
Ali M, Ali M, Mohamed A, Mannan S, Fallahi F. The role of ultrasonography in the diagnosis of occult scaphoid fractures. J Ultrasonogr
Popović ZB, Thomas JD. Assessing operator variability: a user’s guide. Cardiovasc Diagn Ther
Global Initiative for Chronic Obstructive Lung Disease guidelines2018. Global strategy for the diagnosis, management and prevention of chronic obstructive lung disease
. Available at: http://www.goldcopd.com
. (accessed March 24, 2018)
Miller MR, Hankinson JA, Brusasco V, Burgos F, Casaburi R, Coates A et al.
Standardisation of spirometry. Eur Respir J
Smargiassi A, Inchingolo R, Soldati G, Copetti R, Marchetti G, Zanforlin A, et al.
.. The role of chest ultrasonography in the management of respiratory diseases: document II. Multidisci Respir Med
Sarwal A, Walker FO, Cartwright MS. Neuromuscular ultrasound for evaluation of the diaphragm. Muscle Nerve
Bruton A, Conway JH, Holgate ST. Reliability: what is it, and how is it measured?. Physiotherapy
Hartung W, Nigg A, Strunk J, Wolff B. Clinical assessment and ultrasonography in the follow-up of enthesitis in patients with spondyloarthritis: a multicenter ultrasound study in daily clinical practice. Open Access Rheumatol
Moore CL, Copel JA. Point-of-care ultrasonography. N Engl J Med
Villa AD, Corsinovi L, Ntalas I, Milidonis X, Scannell C, Di Giovine G et al.
Importance of operator training and rest perfusion on the diagnostic accuracy of stress perfusion cardiovascular magnetic resonance. J Cardiovas Magn Resonance
Daly L, Bourke GJ. Interpretation and Uses of Medical Statistics
. New York, NY: John Wiley & Sons; 2008.
Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice
. Upper Saddle River, NJ: Pearson/Prentice Hall 2009.
Liu CY, Nascimento OA, Jardim JR. Reliability of an analysis method for measuring diaphragm excursion by means of direct visualization with videofluoroscopy. Archivos de Bronconeumología
Leal BE, Gonçalves MA, Lisboa LG, Linné LM, de Souza Tavares MG, Yamaguti WP, Paulin E. Validity and reliability of fluoroscopy for digital radiography: a new way to evaluate diaphragmatic mobility. BMC Pulmon Med
Pedrini A, Gonçalves MA, Leal BE, Tavares MG, Yamaguti WP, Góes DL, Paulin E. Validity and reliability of assessing diaphragmatic mobility by area on X-rays of healthy subjects. Journal Brasileiro Pneumologia
Kotani T, Minami S, Takahashi K, Isobe K, Nakata Y, Takaso M et al.
An analysis of chest wall and diaphragm motions in patients with idiopathic scoliosis using dynamic breathing MRI. Revista Spine
Roberts HC. Imaging the diaphragm. Thorac Surg Clin
Grams ST, von Saltiél R, Mayer AF, Schivinski CI, de S. Nobre LF, Nóbrega IS et al.
Assessment of the reproducibility of the indirect ultrasound method of measuring diaphragm mobility. Clin Physiol Functional Imag
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]