Respiratory muscle ultrasonography: methodology, basic and advanced principles and clinical applications in ICU and ED patients-a narrative review

Pieter R Tuinman, Annemijn H Jonkman, Martin Dres, Zhong-Hua Shi, Ewan C Goligher, Alberto Goffi, Chris de Korte, Alexandre Demoule, Leo Heunks, Pieter R Tuinman, Annemijn H Jonkman, Martin Dres, Zhong-Hua Shi, Ewan C Goligher, Alberto Goffi, Chris de Korte, Alexandre Demoule, Leo Heunks

Abstract

Respiratory muscle ultrasound is used to evaluate the anatomy and function of the respiratory muscle pump. It is a safe, repeatable, accurate, and non-invasive bedside technique that can be successfully applied in different settings, including general intensive care and the emergency department. Mastery of this technique allows the intensivist to rapidly diagnose and assess respiratory muscle dysfunction in critically ill patients and in patients with unexplained dyspnea. Furthermore, it can be used to assess patient-ventilator interaction and weaning failure in critically ill patients. This paper provides an overview of the basic and advanced principles underlying respiratory muscle ultrasound with an emphasis on the diaphragm. We review different ultrasound techniques useful for monitoring of the respiratory muscle pump and possible therapeutic consequences. Ideally, respiratory muscle ultrasound is used in conjunction with other components of critical care ultrasound to obtain a comprehensive evaluation of the critically ill patient. We propose the ABCDE-ultrasound approach, a systematic ultrasound evaluation of the heart, lungs and respiratory muscle pump, in patients with weaning failure.

Keywords: Diaphragm dysfunction; Diaphragm ultrasound; Respiratory muscle ultrasound; Ultrasonography.

Conflict of interest statement

None of the authors has any conflict to declare.

Figures

Fig. 1
Fig. 1
Clinical application of respiratory muscle ultrasound: techniques and views
Fig. 2
Fig. 2
Point-of-Care Ultrasound (PoCUS) in patients with weaning failure: the ABCDE approach

References

    1. Vieillard-Baron A, Millington SJ, Sanfilippo F, Chew M, Diaz-Gomez J, McLean A, Pinsky MR, Pulido J, Mayo P, Fletcher N. A decade of progress in critical care echocardiography: a narrative review. Intensive Care Med. 2019;45:770–788.
    1. Mayo PH, Copetti R, Feller-Kopman D, Mathis G, Maury E, Mongodi S, Mojoli F, Volpicelli G, Zanobetti M. Thoracic ultrasonography: a narrative review. Intensive Care Med. 2019;45:1200–1211.
    1. Shi ZH, Jonkman A, de Vries H, Jansen D, Ottenheijm C, Girbes A, Spoelstra-de Man A, Zhou JX, Brochard L, Heunks L. Expiratory muscle dysfunction in critically ill patients: towards improved understanding. Intensive Care Med. 2019;45:1061–1071.
    1. Matamis D, Soilemezi E, Tsagourias M, Akoumianaki E, Dimassi S, Boroli F, Richard JC, Brochard L. Sonographic evaluation of the diaphragm in critically ill patients. Technique and clinical applications. Intensive Care Med. 2013;39:801–810.
    1. Haaksma ME, Atmowihardjo L, Heunks L, Spoelstra-de Man A, Tuinman PR. Ultrasound imaging of the diaphragm: facts and future. A guide for the bedside clinician. Neth J Crit Care. 2018;26:58–63.
    1. Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal subjects. Muscle Nerve. 2013;47:884–889.
    1. Carrillo-Esper R, Perez-Calatayud AA, Arch-Tirado E, Diaz-Carrillo MA, Garrido-Aguirre E, Tapia-Velazco R, Pena-Perez CA, Espinoza-de Los Monteros I, Meza-Marquez JM, Flores-Rivera OI, Zepeda-Mendoza AD, de la Torre-Leon T. Standardization of sonographic diaphragm thickness evaluations in healthy volunteers. Respir Care. 2016;61:920–924.
    1. Wait JL, Nahormek PA, Yost WT, Rochester DP. Diaphragmatic thickness lung volume relationship invivo. J Appl Physiol. 1989;67:1560–1568.
    1. Goligher EC, Laghi F, Detsky ME, Farias P, Murray A, Brace D, Brochard LJ, Bolz SS, Rubenfeld GD, Kavanagh BP, Ferguson ND. Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity (vol 41, pg 642, 2015) Intens Care Med. 2015;41:734.
    1. Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med. 1997;155:1570–1574.
    1. Cohn D, Benditt JO, Eveloff S, McCool FD. Diaphragm thickening during inspiration. J Appl Physiol. 1997;83:291–296.
    1. Dube BP, Dres M, Mayaux J, Demiri S, Similowski T, Demoule A. Ultrasound evaluation of diaphragm function in mechanically ventilated patients: comparison to phrenic stimulation and prognostic implications. Thorax. 2017;72:811–818.
    1. Goligher EC, Dres M, Fan E, Rubenfeld GD, Scales DC, Herridge MS, Vorona S, Sklar MC, Rittayamai N, Lanys A, Murray A, Brace D, Urrea C, Reid WD, Tomlinson G, Slutsky AS, Kavanagh BP, Brochard LJ, Ferguson ND. Mechanical ventilation-induced diaphragm atrophy strongly impacts clinical outcomes. Am J Respir Crit Care Med. 2018;197:204–213.
    1. Vivier E, Mekontso Dessap A, Dimassi S, Vargas F, Lyazidi A, Thille AW, Brochard L. Diaphragm ultrasonography to estimate the work of breathing during non-invasive ventilation. Intensive Care Med. 2012;38:796–803.
    1. Umbrello M, Formenti P, Longhi D, Galimberti A, Piva I, Pezzi A, Mistraletti G, Marini JJ, Iapichino G. Diaphragm ultrasound as indicator of respiratory effort in critically ill patients undergoing assisted mechanical ventilation: a pilot clinical study. Crit Care. 2015;19:161.
    1. Coirault C, Chemla D, Lecarpentier Y. Relaxation of diaphragm muscle. J Appl Physiol. 1999;87(1985):1243–1252.
    1. Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values. Chest. 2009;135:391–400.
    1. Haji K, Royse A, Green C, Botha J, Canty D, Royse C. Interpreting diaphragmatic movement with bedside imaging, review article. J Crit Care. 2016;34:56–65.
    1. Houston JG, Morris AD, Howie CA, Reid JL, Mcmillan N. Technical report—quantitative assessment of diaphragmatic movement—a reproducible method using ultrasound. Clin Radiol. 1992;46:405–407.
    1. Haji K, Royse A, Tharmaraj D, Haji D, Botha J, Royse C. Diaphragmatic regional displacement assessed by ultrasound and correlated to subphrenic organ movement in the critically ill patients–an observational study. J Crit Care. 2015;30(439):e413–e437.
    1. Toledo NS, Kodaira SK, Massarollo PC, Pereira OI, Dalmas JC, Cerri GG, Buchpiguel CA. Left hemidiaphragmatic mobility: assessment with ultrasonographic measurement of the craniocaudal displacement of the splenic hilum and the inferior pole of the spleen. J Ultrasound Med. 2006;25:41–49.
    1. Doorduin J, Roesthuis LH, Jansen D, van der Hoeven JG, van Hees HWH, Heunks LMA. Respiratory muscle effort during expiration in successful and failed weaning from mechanical ventilation. Anesthesiology. 2018;129:490–501.
    1. Yoshida R, Tomita K, Kawamura K, Nozaki T, Setaka Y, Monma M, Ohse H. Measurement of intercostal muscle thickness with ultrasound imaging during maximal breathing. J Phys Ther Sci. 2019;31:340–343.
    1. Dres M, Dupe B-P, Goligher EC et al. (2018) Intercostal muscle ultrasound activity: a feasibility and physiological study in mechanically ventilated patients. ATS: A5863
    1. Tahan N, Khademi-Kalantari K, Mohseni-Bandpei MA, Mikaili S, Baghban AA, Jaberzadeh S. Measurement of superficial and deep abdominal muscle thickness: an ultrasonography study. J Physiol Anthropol. 2016;35:17.
    1. Misuri G, Colagrande S, Gorini M, Iandelli I, Mancini M, Duranti R, Scano G. In vivo ultrasound assessment of respiratory function of abdominal muscles in normal subjects. Eur Respir J. 1997;10:2861–2867.
    1. Rankin G, Stokes M, Newham DJ. Abdominal muscle size and symmetry in normal subjects. Muscle Nerve. 2006;34:320–326.
    1. Springer BA, Mielcarek BJ, Nesfield TK, Teyhen DS. Relationships among lateral abdominal muscles, gender, body mass index, and hand dominance. J Orthop Sports Phys Ther. 2006;36:289–297.
    1. Schreiber ASU, Vorona S, Bertoni M, Piva S, Goligher E (2019) Measuring abdominal muscle function by abdominal muscle thickening on ultrasound: reproducibility, validity and normal range values. In: Book Measuring abdominal muscle function by abdominal muscle thickening on ultrasound: reproducibility, validity and normal range values
    1. Valette X, Seguin A, Daubin C, Brunet J, Sauneuf B, Terzi N, du Cheyron D. Diaphragmatic dysfunction at admission in intensive care unit: the value of diaphragmatic ultrasonography. Intensive Care Med. 2015;41:557–559.
    1. Winkler MH, Touw HR, van de Ven PM, Twisk J, Tuinman PR. Diagnostic accuracy of chest radiograph, and when concomitantly studied lung ultrasound, in critically ill patients with respiratory symptoms: a systematic review and meta-analysis. Crit Care Med. 2018;46:e707–e714.
    1. McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Engl J Med. 2012;366:932–942.
    1. Tobin MJ, Perez W, Guenther SM, Lodato RF, Dantzker DR. Does rib cage-abdominal paradox signify respiratory muscle fatigue? J Appl Physiol. 1987;63(1987):851–860.
    1. Houston JG, Fleet M, Cowan MD, Mcmillan NC. Comparison of ultrasound with fluoroscopy in the assessment of suspected hemidiaphragmatic movement abnormality. Clin Radiol. 1995;50:95–98.
    1. Chetta A, Rehman AK, Moxham J, Carr DH, Polkey MI. Chest radiography cannot predict diaphragm function. Respir Med. 2005;99:39–44.
    1. Boussuges A, Bregeon F, Blanc P, Gil JM, Poirette L. Characteristics of the paralysed diaphragm studied by M-mode ultrasonography. Clin Physiol Funct Imaging. 2019;39:143–149.
    1. Cohen E, Mier A, Heywood P, Murphy K, Boultbee J, Guz A. Diaphragmatic movement in hemiplegic patients measured by ultrasonography. Thorax. 1994;49:890–895.
    1. Sanchez-Nicolas JA, Cinesi-Gomez C, Villen-Villegas T, Pinera-Salmeron P, Garcia-Perez B. Relation between ultrasound-measured diaphragm movement and partial pressure of carbon dioxide in blood from patients with acute hypercapnic respiratory failure after the start of noninvasive ventilation in an emergency department. Emergencias. 2016;28:345–348.
    1. Cammarota G, Sguazzotti I, Zanoni M, Messina A, Colombo D, Vignazia GL, Vetrugno L, Garofalo E, Bruni A, Navalesi P, Avanzi GC, Della Corte F, Volpicelli G, Vaschetto R. Diaphragmatic ultrasound assessment in subjects with acute hypercapnic respiratory failure admitted to the emergency department. Respir Care. 2019;64:1469–1477.
    1. Dos Santos Yamaguti WP, Paulin E, Shibao S, Chammas MC, Salge JM, Ribeiro M, Cukier A, Carvalho CR. Air trapping: the major factor limiting diaphragm mobility in chronic obstructive pulmonary disease patients. Respirology. 2008;13:138–144.
    1. Antenora F, Fantini R, Iattoni A, Castaniere I, Sdanganelli A, Livrieri F, Tonelli R, Zona S, Monelli M, Clini EM, Marchioni A. Prevalence and outcomes of diaphragmatic dysfunction assessed by ultrasound technology during acute exacerbation of COPD: a pilot study. Respirology. 2017;22:338–344.
    1. Marchioni A, Tonelli R, Antenora F, Fantini R, Clini EM. COPD exacerbation and diaphragmatic dysfunction: conditions with mutual influence influencing outcomes? Reply. Respirology. 2017;22:830–831.
    1. Heunks L, Ottenheijm C. Diaphragm-protective mechanical ventilation to improve outcomes in ICU patients? Am J Respir Crit Care Med. 2018;197:150–152.
    1. Goligher EC, Fan E, Herridge MS, Murray A, Vorona S, Brace D, Rittayamai N, Lanys A, Tomlinson G, Singh JM, Bolz SS, Rubenfeld GD, Kavanagh BP, Brochard LJ, Ferguson ND. Evolution of diaphragm thickness during mechanical ventilation impact of inspiratory effort. Am J Resp Crit Care. 2015;192:1080–1088.
    1. Schepens T, Dres M, Heunks L, Goligher EC. Diaphragm-protective mechanical ventilation. Curr Opin Crit Care. 2019;25:77–85.
    1. McConville JF, Kress JP. Weaning patients from the ventilator. N Engl J Med. 2012;367:2233–2239.
    1. Dres M, Goligher EC, Heunks LMA, Brochard LJ. Critical illness-associated diaphragm weakness. Intensive Care Med. 2017;43:1441–1452.
    1. Jung B, Moury PH, Mahul M, de Jong A, Galia F, Prades A, Albaladejo P, Chanques G, Molinari N, Jaber S. Diaphragmatic dysfunction in patients with ICU-acquired weakness and its impact on extubation failure. Intensive Care Med. 2016;42:853–861.
    1. Dres M, Demoule A. Diaphragm dysfunction during weaning from mechanical ventilation: an underestimated phenomenon with clinical implications. Crit Care. 2018;22:73.
    1. Kim WY, Suh HJ, Hong SB, Koh Y, Lim CM. Diaphragm dysfunction assessed by ultrasonography: influence on weaning from mechanical ventilation. Crit Care Med. 2011;39:2627–2630.
    1. Mariani LF, Bedel J, Gros A, Lerolle N, Milojevic K, Laurent V, Hilly J, Troche G, Bedos JP, Planquette B. Ultrasonography for screening and follow-up of diaphragmatic dysfunction in the ICU: a pilot study. J Intensive Care Med. 2016;31:338–343.
    1. Farghaly S, Hasan AA. Diaphragm ultrasound as a new method to predict extubation outcome in mechanically ventilated patients. Aust Crit Care. 2017;30:37–43.
    1. Lerolle N, Guerot E, Dimassi S, Zegdi R, Faisy C, Fagon JY, Diehl JL. Ultrasonographic diagnostic criterion for severe diaphragmatic dysfunction after cardiac surgery. Chest. 2009;135:401–407.
    1. Llamas-Alvarez AM, Tenza-Lozano EM, Latour-Perez J. Diaphragm and lung ultrasound to predict weaning outcome: systematic review and meta-analysis. Chest. 2017;152:1140–1150.
    1. Spadaro S, Grasso S, Mauri T, Dalla Corte F, Alvisi V, Ragazzi R, Cricca V, Biondi G, Di Mussi R, Marangoni E, Volta CA. Can diaphragmatic ultrasonography performed during the T-tube trial predict weaning failure? The role of diaphragmatic rapid shallow breathing index. Crit Care. 2016;20:305.
    1. Palkar A, Narasimhan M, Greenberg H, Singh K, Koenig S, Mayo P, Gottesman E. Diaphragm excursion-time index: a new parameter using ultrasonography to predict extubation outcome. Chest. 2018;153:1213–1220.
    1. Vivier E, Muller M, Putegnat JB, Steyer J, Barrau S, Boissier F, Bourdin G, Mekontso-Dessap A, Levrat A, Pommier C, Thille AW. Inability of diaphragm ultrasound to predict extubation failure: a multicenter study. Chest. 2019;155:1131–1139.
    1. Zambon M, Greco M, Bocchino S, Cabrini L, Beccaria PF, Zangrillo A. Assessment of diaphragmatic dysfunction in the critically ill patient with ultrasound: a systematic review. Intensive Care Med. 2017;43:29–38.
    1. Ferrari G, De Filippi G, Elia F, Panero F, Volpicelli G, Apra F. Diaphragm ultrasound as a new index of discontinuation from mechanical ventilation. Crit Ultrasound J. 2014;6:8.
    1. DiNino E, Gartman EJ, Sethi JM, McCool FD. Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation. Thorax. 2014;69:423–427.
    1. Heunks LM, van der Hoeven JG. Clinical review: the ABC of weaning failure–a structured approach. Crit Care. 2010;14:245.
    1. Mayo P, Volpicelli G, Lerolle N, Schreiber A, Doelken P, Vieillard-Baron A. Ultrasonography evaluation during the weaning process: the heart, the diaphragm, the pleura and the lung. Intensive Care Med. 2016;42:1107–1117.
    1. Tobin MJ, Jubran A, Laghi F. Patient-ventilator interaction. Am J Respir Crit Care Med. 2001;163:1059–1063.
    1. Vaporidi K, Babalis D, Chytas A, Lilitsis E, Kondili E, Amargianitakis V, Chouvarda I, Maglaveras N, Georgopoulos D. Clusters of ineffective efforts during mechanical ventilation: impact on outcome. Intens Care Med. 2017;43:184–191.
    1. Thille AW, Rodriguez P, Cabello B, Lellouche F, Brochard L. Patient-ventilator asynchrony during assisted mechanical ventilation. Intens Care Med. 2006;32:1515–1522.
    1. 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. 2013;187:20–27.
    1. Soilemezi E, Vasileiou M, Spyridonidou C, Tsagourias M, Matamis D. Understanding patient-ventilator asynchrony using diaphragmatic ultrasonography. Am J Resp Crit Care. 2019;200:E27–E28.
    1. Goligher EC, Laghi F, Detsky ME, Farias P, Murray A, Brace D, Brochard LJ, Bolz SS, Rubenfeld GD, Kavanagh BP, Ferguson ND. Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity. Intensive Care Med. 2015;41:642–649.
    1. Yu CM, Sanderson JE, Marwick TH, Oh JK. Tissue doppler imaging a new prognosticator for cardiovascular diseases. J Am Coll Cardiol. 2007;49:1903–1914.
    1. Maurizio R, Rinaldi VE, Camerini PG, Salvatori C, Leonardi A, Bini V. Right diaphragmatic peak motion velocities on pulsed wave tissue doppler imaging in neonates: method, reproducibility, and reference values. J Ultrasound Med. 2019;38:2695–2701.
    1. Goldstone JC, Green M, Moxham J. Maximum relaxation rate of the diaphragm during weaning from mechanical ventilation. Thorax. 1994;49:54–60.
    1. Oppersma E, Hatam N, Doorduin J, van der Hoeven JG, Marx G, Goetzenich A, Fritsch S, Heunks LMA, Bruells CS. Functional assessment of the diaphragm by speckle tracking ultrasound during inspiratory loading. J Appl Physiol. 2017;123(1985):1063–1070.
    1. Goutman SA, Hamilton JD, Swihart B, Foerster B, Feldman EL, Rubin JM. Speckle tracking as a method to measure hemidiaphragm excursion. Muscle Nerve. 2017;55:125–127.
    1. Bachasson D, Dres M, Nierat MC, Gennisson JL, Hogrel JY, Doorduin J, Similowski T. Diaphragm shear modulus reflects transdiaphragmatic pressure during isovolumetric inspiratory efforts and ventilation against inspiratory loading. J Appl Physiol. 2019;126(1985):699–707.
    1. Vivier ERA, Doroszewski F, Roselli S, Pommier C, Carteaux G, Dessap AM. Atrophy of diaphragm and pectoralis muscles in critically ill patients. Anesthesiology. 2019;131:569–579.
    1. Schepens T, Verbrugghe W, Dams K, Corthouts B, Parizel PM, Jorens PG. The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study. Crit Care. 2015;19:422.
    1. Jiang JR, Tsai TH, Jerng JS, Yu CJ, Wu HD, Yang PC. Ultrasonographic evaluation of liver/spleen movements and extubation outcome. Chest. 2004;126:179–185.
    1. Ueki J, Debruin PF, Pride NB. In-vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax. 1995;50:1157–1161.

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