Skip to main content
SpringerLink
Log in

Evaluation of diaphragm thickening by diaphragm ultrasonography: a reproducibility and a repeatability study

  • Original Paper
  • Published:
Journal of Ultrasound Aims and scope Submit manuscript

Abstract

Purpose

We have focused on the two-dimensional (B-mode) and the time-motion (M-mode) analysis of the zone of apposition to determine the reliability of diaphragm ultrasonography in the clinical environment.

Methods

Ten healthy volunteers were enrolled and studied by three operators with different skills in ultrasonography. For every volunteer, each operator acquired three images of the diaphragm for each side, both in B-mode and in M-mode. Then a fourth operator calculated the thickening fraction (TF), by means of the formula TF = (TEI − TEE)/TEE (TEI is the thickness at end inspiration and TEE the thickness at end expiration). Afterwards, intraclass correlation coefficients (ICCs) were computed on TF to establish reproducibility and repeatability both in the B- and M-modes. A Coefficient of Repeatability or repeatability (CR) ≤ 0.3 was considered acceptable.

Results

Both B-mode (CRs 0.16–0.26) and M-mode (CRs 0.10–0.15) were sufficiently repeatable to assess TF, except for the less experienced operator (CRs B-Mode 0.20–0.32). Reproducibility was moderate to good between operators with CRs much narrower for the M-Mode (0.13–0.14).

Conclusions

The results of our study have shown that diaphragm ultrasound is repeatable and reproducible when carried out by a radiologist or an intensivist with a basic curriculum in ultrasonography. The method is more accurate when using the M-mode for less experienced operators, and in this case, repeatability and reproducibility are not sufficient to make clinical decisions. No TF value lower than 36% was obtained using both techniques. This suggests the existence of a cut-off value that could be used as an initial tool to discriminate healthy subjects from those affected by diaphragmatic dysfunction.

Clinical trial registration

EUDRACT 2015-004635-12.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

CT:

Computed tomography

MRI:

Magnetic resonance imaging

M-mode:

Time-motion ultrasonography

B-mode:

Two-dimensional morphological ultrasonography

ZOA:

Zone of apposition of the diaphragm to the rib cage

MV:

Mechanical ventilation

NIV:

Non-invasive ventilation

ICU:

Intensive care unit

R&R:

Repeatability and reproducibility

TEI:

Diaphragm thickness at end inspiration

TEE:

Diaphragm thickness at end expiration

TF:

Thickening fraction

ANOVA:

Analysis of variance

References

  1. Kharma N (2013) Dysfunction of the diaphragm: imaging as a diagnostic tool. Curr Opin Pulm Med 19(4):394–398

    PubMed  Google Scholar 

  2. Wait JL, Nahormek PA, Yost WT, Rochester DP, Rochester P (1989) Diaphragmatic thickness-lung volume relationship in vivo volume relationship in vivo. J Appl Physiol 67:1560–1568

    Article  CAS  Google Scholar 

  3. Boussuges A, Gole Y, Blanc P (2009) Diaphragmatic motion studied by M-mode ultrasonography methods, reproducibility, and normal values. Chest 135(2):391–400

    Article  Google Scholar 

  4. Kim SH, Na S, Choi JS, Na SH, Shin S, Koh SO (2010) An evaluation of diaphragmatic movement by M-mode sonography as a predictor of pulmonary dysfunction after upper abdominal surgery. Anesth Analg 110(5):1349–1354

    Article  Google Scholar 

  5. Lerolle N, Guérot E, Dimassi S, Zegdi R, Faisy C, Fagon J-Y, Diehl J-L (2009) Ultrasonographic diagnostic criterion for severe diaphragmatic dysfunction after cardiac surgery. Chest 135(2):401–407

    Article  Google Scholar 

  6. Summerhill EM, El-Sameed YA, Glidden TJ, McCool FD (2008) Monitoring recovery from diaphragm paralysis with ultrasound. Chest 133(3):737–743

    Article  Google Scholar 

  7. Oppersma E, Hatam N, Doorduin J, van der Hoeven JG, Marx G, Goetzenich A, Fritsch S, Heunks LMA, Bruells CS (2017) Functional assessment of the diaphragm by speckle tracking ultrasound during inspiratory loading. J Appl Physiol 123(5):1063–1070

    Article  Google Scholar 

  8. Vivier E, Mekontso Dessap A, Dimassi S, Vargas F, Lyazidi A, Thille AW, Brochard L (2012) Diaphragm ultrasonography to estimate the work of breathing during non-invasive ventilation. Intensiv Care Med 38(5):796–803

    Article  Google Scholar 

  9. Bellani G, Pesenti A (2014) Assessing effort and work of breathing. Curr Opin Crit Care 20(3):352–358

    Article  Google Scholar 

  10. Vivier E, Muller M, Putegnat JB, Steyer J, Barrau S, Boissier F, Bourdin G, Mekontso-Dessap A, Levrat A, Pommier C et al (2019) Inability of diaphragm ultrasound to predict extubation failure a multicenter study. Chest 155(6):1131–1139

    Article  Google Scholar 

  11. Fagley RE, Haney MF, Beraud AS, Comfere T, Kohl BA, Merkel MJ, Pustavoitau A, von Homeyer P, Wagner CE, Wall MH (2015) Critical care basic ultrasound learning goals for American Anesthesiology Critical Care Trainees: recommendations from an expert group. Anesth Analg 120(5):1041–1053

    Article  Google Scholar 

  12. Koo TK, Li MY (2017) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 16(4):346–346

    Article  Google Scholar 

  13. Guillory RK, Gunter OL (2008) Ultrasound in the surgical intensive care unit. Curr Opin Crit Care 14(4):415–422

    Article  Google Scholar 

  14. DeBruin PF, Ueki J, Bush A, Khan Y, Watson A, Pride NB (1997) Diaphragm thickness and inspiratory strength in patients with Duchenne muscular dystrophy. Thorax 52(5):472–475

    Article  CAS  Google Scholar 

  15. Hardy F, Walker J, Sawyer T (2009) Sonographic measurement of diaphragm movement in patients with tetraplegia. Spinal Cord 47(11):832–834

    Article  CAS  Google Scholar 

  16. Yoshioka Y, Ohwada A, Sekiya M, Takahashi F, Ueki J, Fukuchi Y (2007) Ultrasonographic evaluation of the diaphragm in patients with amyotrophic lateral sclerosis. Respirology 12(2):304–307

    Article  Google Scholar 

  17. DiNino E, Gartman EJ, Sethi JM, McCool FD (2014) Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation. Thorax 69(5):423–427

    Article  Google Scholar 

  18. Kim WY, Suh HJ, Hong S-B, Koh Y, Lim C-M (2011) Diaphragm dysfunction assessed by ultrasonography: influence on weaning from mechanical ventilation. Crit Care Med 39(12):2627–2630

    Article  Google Scholar 

  19. Blaivas M, Brannam L, Hawkins M, Lyon M, Sriram K (2004) Bedside emergency ultrasonographic diagnosis of diaphragmatic rupture in blunt abdominal trauma. Am J Emerg Med 22(7):601–604

    Article  Google Scholar 

  20. Hassan M, Rizk R, Essam H, Abouelnour A (2017) Validation of equations for pleural effusion volume estimation by ultrasonography. J Ultrasound 20(4):267–271

    Article  Google Scholar 

  21. Subotic DR, Stevic R, Gajic M, Vesovic R (2013) Diaphragm motion and lung function prediction in patients operated for lung cancer—a pilot study on 27 patients. J Cardiothorac Surg 8:213–213

    Article  Google Scholar 

  22. Lloyd T, Tang YM, Benson MD, King S (2006) Diaphragmatic paralysis: the use of M mode ultrasound for diagnosis in adults. Spinal Cord 44(8):505–508

    Article  CAS  Google Scholar 

  23. Nason LK, Walker CM, McNeeley MF, Burivong W, Fligner CL, Godwin JD (2012) Imaging of the diaphragm: anatomy and function. Radiographics 32(2):E51–E70

    Article  Google Scholar 

  24. Cohn D, Benditt JO, Eveloff S, McCool FD (1997) Diaphragm thickening during inspiration. J Appl Physiol 83(1):291–296

    Article  CAS  Google Scholar 

  25. Harper CJ, Shahgholi L, Cieslak K, Hellyer NJ, Strommen Ja, Boon AJ (2013) Variability in diaphragm motion during normal breathing, assessed with B-mode ultrasound. J Orthop Sports Phys Ther 43(12):927–931

    Article  Google Scholar 

  26. Sæverud HA, Falk RS, Dowrick A, Eriksen M, Aarrestad S, Skjønsberg OH (2019) Measuring diaphragm movement and respiratory frequency using a novel ultrasound device in healthy volunteers. J Ultrasound. https://doi.org/10.1007/s40477-019-00412-2

    Article  PubMed  Google Scholar 

  27. Goligher EC, Laghi F, Detsky ME, Farias P, Murray A, Brace D, Brochard LJ, Sebastien-Bolz S, Rubenfeld GD, Kavanagh BP et al (2015) Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity. Intensiv Care Med 41(4):642–649

    Article  Google Scholar 

  28. Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen Ja, Watson JC, Sorenson EJ (2013) Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal subjects. Muscle Nerve 47(6):884–889

    Article  Google Scholar 

  29. Ranieri G, Luigi M, Belsito F, Rocco M, Blasi RAD (2015) Propofol sedation reduces contraction and motion of diaphragm in humans: preliminary results. Crit Care 19(Suppl 1):P481–P481

    Article  Google Scholar 

  30. Grams ST, von Saltiél R, Mayer AF, Schivinski CIS, de Nobre SLF, Nóbrega IS, Jacomino MEMLP, Paulin E (2014) Assessment of the reproducibility of the indirect ultrasound method of measuring diaphragm mobility. Clin Physiol Funct Imaging 34(1):18–25

    Article  Google Scholar 

  31. Arbelot C, Dexheimer Neto FL, Gao Y, Brisson H, Chunyao W, Lv J, Valente Barbas CS, Perbet S, Prior Caltabellotta F, Gay F et al (2020) Lung ultrasound in emergency and critically ill patients: number of supervised exams to reach basic competence. Anesthesiology 132(4):899–907

    Article  Google Scholar 

Download references

Acknowledgements

CA, FP, IC, SM, and VG had access to all of the data in the study; CA took responsibility for the integrity of the data and the accuracy of data analysis. FP, IC, SM and MB contributed substantially to the study design, data collection, analysis, and interpretation. IC and FP wrote this manuscript. AC, BM, and VG revised and approved the proof, before submission.

Funding

Chiara Adembri was funded by the University of Florence.

Author information

Authors and Affiliations

  1. Department of Health Sciences, Section of Anesthesiology and Critical Care, University of Florence, Florence, Italy

    Iacopo Cappellini, Simona Matteini, Gianni Virgili & Chiara Adembri

  2. Radiology Department, Azienda Ospedaliero Universitaria Careggi, Florence, Italy

    Fabio Picciafuochi, Maurizio Bartolucci & Chiara Adembri

  3. Department of Neuroscience, Psychology, Drug Research and Child Health, University of Florence, Florence, Italy

    Gianni Virgili

Authors
  1. Iacopo Cappellini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabio Picciafuochi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurizio Bartolucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Simona Matteini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gianni Virgili
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chiara Adembri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iacopo Cappellini.

Ethics declarations

Conflict of interest

All authors declare no conflict of interest.

Ethical approval

All procedures performed in the present study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Ethical approval has been obtained for Comitato Etico Area Vasta Toscana Centro with EUDRACT number 2015-004635-12.

Informed consent

Informed consent has been collected from all participants enrolled in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cappellini, I., Picciafuochi, F., Bartolucci, M. et al. Evaluation of diaphragm thickening by diaphragm ultrasonography: a reproducibility and a repeatability study. J Ultrasound 24, 411–416 (2021). https://doi.org/10.1007/s40477-020-00462-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40477-020-00462-x

Keywords

Search

Navigation