Diaphragm function in patients with sepsis and septic shock: A longitudinal ultrasound study

Published:March 08, 2022DOI:



      Previous literature on the determinants of diaphragm dysfunction in septic patients is limited. The goal of this study is to assess diaphragm dysfunction in terms of its prevalence and its potential associated factors in septic intensive care unit (ICU) patients.


      This prospective and observational study was conducted between June 2015 and July 2019. Ultrasound measures of diaphragm thickness were performed daily on septic patients. The primary outcome was the prevalence of diaphragm dysfunction at baseline and during the ICU stay. The secondary outcome was the diaphragm thickness. Possible associated factors were prospectively recorded.


      Fifty patients were enrolled in the study. The prevalence of diaphragm dysfunction was 58%. No diaphragm atrophy was found during the ICU stay. Diaphragm dysfunction was associated with the alteration of consciousness, intra-abdominal sepsis, hypnotics and opioids, and mechanical ventilation. Administration of hypnotics, opioids, and steroids was associated with a decreased diaphragm thickening fraction. Diaphragm dysfunction had no impact on patient outcomes.


      Our data reveal a high prevalence of diaphragm dysfunction in septic patients at the onset of sepsis. Administration of hypnotics, opioids, and steroids was associated with the alteration of diaphragm function as well as intra-abdominal sepsis.


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        • de Jonghe Bernard
        • Jean-Claude Lacherade
        • Tarek Sharshar
        • Hervé Outin
        Intensive care unit-acquired weakness: risk factors and prevention.
        Crit Care Med. 2009; 37: S309-S315
        • Callahan Leigh Ann
        • Supinski Gerald S.
        Sepsis-induced myopathy.
        Crit Care Med. 2009; 37: S354-S367
        • Alexandre Demoule
        • Jung Boris
        • Hélène Prodanovic
        • Nicolas Molinari
        • Gerald Chanques
        • Catherine Coirault
        • et al.
        Diaphragm dysfunction on admission to the intensive care unit. Prevalence, risk factors, and prognostic impact—a prospective study.
        Am J Respir Crit Care Med. 2013; 188: 213-219
        • Boris Jung
        • Stephanie Nougaret
        • Matthieu Conseil
        • Yannaël Coisel
        • Emmanuel Futier
        • Gerald Chanques
        • et al.
        Sepsis is associated with a preferential diaphragmatic atrophy: a critically ill patient study using tridimensional computed tomography.
        Anesthesiology. 2014; 120: 1182-1191
        • Samir Jaber
        • Petrof Basil J.
        • Jung Boris
        • Gérald Chanques
        • Jean-Philippe Berthet
        • Christophe Rabuel
        • et al.
        Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans.
        Am J Respir Crit Care Med. 2011; 183: 364-371
        • Baldwin Claire E.
        • Bersten Andrew D.
        Alterations in respiratory and limb muscle strength and size in patients with sepsis who are mechanically ventilated.
        Phys Ther. 2014; 94: 68-82
        • Martin Dres
        • Goligher Ewan C.
        • Heunks Leo M.A.
        • Brochard Laurent J.
        Critical illness-associated diaphragm weakness.
        Intensive Care Med. 2017; 43: 1441-1452
        • Singer Mervyn
        • Deutschman Clifford S.
        • Warren Seymour Christopher
        • Manu Shankar-Hari
        • Djillali Annane
        • Bauer Michael
        • et al.
        The third international consensus definitions for sepsis and septic shock (Sepsis-3).
        JAMA. 2016; 315: 801-810
        • Goligher Ewan C.
        • Franco Laghi
        • Detsky Michael E.
        • Farias Paulina
        • Murray Alistair
        • Deborah Brace
        • et al.
        Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity.
        Intensive Care Med. 2015; 41: 734
        • Summerhill Eleanor M.
        • El-Sameed Yaser Abu
        • Glidden Theresa J.
        • Dennis McCool F.
        Monitoring recovery from diaphragm paralysis with ultrasound.
        Chest. 2008; 133: 737-743
        • Goligher Ewan C.
        • Martin Dres
        • Fan Eddy
        • Rubenfeld Gordon D.
        • Scales Damon C.
        • Herridge Margaret S.
        • et al.
        Mechanical ventilation-induced diaphragm atrophy strongly impacts clinical outcomes.
        Am J Respir Crit Care Med. 2018; 197: 204-213
        • Bruno Falissard
        Focused principal component analysis: looking at a correlation matrix with a particular interest in a given variable.
        J Comput Graph Stat. 1999; 8: 906-912
        • Khan Jaffar
        • Harrison Taylor B.
        • Rich Mark M.
        • Moss Marc
        Early development of critical illness myopathy and neuropathy in patients with severe sepsis.
        Neurology. 2006; 67: 1421-1425
        • Santos Patrícia Dos
        • Teixeira Cassiano
        • Augusto Savi
        • Gasparetto Maccari Juçara
        • Neres Fernanda Santos
        • Machado André Sant Ana
        • et al.
        The critical illness polyneuropathy in septic patients with prolonged weaning from mechanical ventilation: is the diaphragm also affected? A pilot study.
        Respir Care. 2012; 57: 1594-1601
        • Sanford Levine
        • Nguyen Taitan
        • Taylor Nyali
        • Friscia Michael E.
        • Budak Murat T.
        • Rothenberg Pamela
        • et al.
        Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans.
        N Engl J Med. 2008; 358: 1327-1335
        • Matuszczak Y.
        • Viires N.
        • Allamedin H.
        • Aubier M.
        • Desmonts J.M.
        • Dureuil B.
        Alteration in diaphragmatic function induced by acute necrotizing pancreatitis in a rodent model.
        Am J Respir Crit Care Med. 1999; 160: 1623-1628
        • Tom Schepens
        • Walter Verbrugghe
        • Karolien Dams
        • Bob Corthouts
        • Parizel Paul M.
        • Jorens Philippe G.
        The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study.
        Crit Care. 2015; 19: 422
        • Alice Grassi
        • Daniela Ferlicca
        • Ermes Lupieri
        • Serena Calcinati
        • Silvia Francesconi
        • Sala Vittoria
        • et al.
        Assisted mechanical ventilation promotes recovery of diaphragmatic thickness in critically ill patients: a prospective observational study.
        Crit Care. 2020; 24: 85
        • Grosu Horiana B.
        • Lee Young Im
        • Lee Jarone
        • Eden Edward
        • Matthias Eikermann
        • Rose Keith M.
        Diaphragm muscle thinning in patients who are mechanically ventilated.
        Chest. 2012; 142: 1455-1460
        • Emmanuel Vivier
        • Aurore Roussey
        • Fanny Doroszewski
        • Sylvène Rosselli
        • Christian Pommier
        • Guillaume Carteaux
        • et al.
        Atrophy of diaphragm and pectoral muscles in critically ill patients.
        Anesthesiology. 2019;
        • Lu Zhihua
        • Ge Huiqing
        • Xu Lilong
        • Guo Feng
        • Zhang Ge
        • Wu Yinshan
        Alterations in diaphragmatic function assessed by ultrasonography in mechanically ventilated patients with sepsis.
        J Clin Ultrasound. 2019;
        • Cartwright Michael S.
        • Golda Kwayisi
        • Griffin Leah P.
        • Aarti Sarwal
        • Walker Francis O.
        • Harris Jessica M.
        • et al.
        Quantitative neuromuscular ultrasound in the intensive care unit.
        Muscle Nerve. 2013; 47: 255-259
        • Sophie Lanone
        • Camille Taillé
        • Jorge Boczkowski
        • Michel Aubier
        Diaphragmatic fatigue during sepsis and septic shock.
        Intensive Care Med. 2005; 31: 1611-1617
        • Pierre-Henri Moury
        • Adrien Cuisinier
        • Michel Durand
        • Jean-Luc Bosson
        • Olivier Chavanon
        • Jean-François Payen
        • et al.
        Diaphragm thickening in cardiac surgery: a perioperative prospective ultrasound study.
        Ann Intensive Care. 2019; 9: 50
        • Emmanuel Vivier
        • Dessap Armand Mekontso
        • Saoussen Dimassi
        • Frederic Vargas
        • Aissam Lyazidi
        • Thille Arnaud W.
        • et al.
        Diaphragm ultrasonography to estimate the work of breathing during non-invasive ventilation.
        Intensive Care Med. 2012; 38: 796-803
        • Martin Dres
        • Jung Boris
        • Nicolas Molinari
        • Manna Federico
        • Bruno-Pierre Dubé
        • Gerald Chanques
        • et al.
        Respective contribution of intensive care unit-acquired limb muscle and severe diaphragm weakness on weaning outcome and mortality: a post hoc analysis of two cohorts.
        Crit Care. 2019; 23: 370
        • Giorgio Conti
        • Andrea Arcangeli
        • Massimo Antonelli
        • Franco Cavaliere
        • Costa Roberta
        • Francesca Simeoni
        • et al.
        Sedation with sufentanil in patients receiving pressure support ventilation has no effects on respiration: a pilot study.
        Can J Anaesth. 2004; 51: 494-499
        • Costa Roberta
        • Paolo Navalesi
        • Gianmaria Cammarota
        • Federico Longhini
        • Giorgia Spinazzola
        • Flora Cipriani
        • et al.
        Remifentanil effects on respiratory drive and timing during pressure support ventilation and neurally adjusted ventilatory assist.
        Respir Physiol Neurobiol. 2017; 244: 10-16
        • Bernard De Jonghe
        • Tarek Sharshar
        • Jean-Pascal Lefaucheur
        • François-Jérome Authier
        • Durand-Zaleski Isabelle
        • Mohamed Boussarsar
        • et al.
        Paresis acquired in the intensive care unit: a prospective multicenter study.
        JAMA. 2002; 288: 2859-2867
        • Sassoon Catherine S.H.
        • Zhu Ercheng
        • Fang Liwei
        • Kannan Ramar
        • Jiao Guang-Yu
        • Caiozzo Vincent J.
        Interactive effects of corticosteroid and mechanical ventilation on diaphragm muscle function.
        Muscle Nerve. 2011; 43: 103-111
        • Karen Maes
        • Anouk Agten
        • Ashley Smuder
        • Powers Scott K.
        • Marc Decramer
        • Gayan-Ramirez Ghislaine
        Corticosteroid effects on ventilator-induced diaphragm dysfunction in anesthetized rats depend on the dose administered.
        Respir Res. 2010; 11: 178
        • Yasuyuki Susa
        • Masuda Yoshiki
        • Hitoshi Imaizumi
        • Akiyoshi Namiki
        Neutralization of receptor for advanced glycation end-products and high mobility group box-1 attenuates septic diaphragm dysfunction in rats with peritonitis.
        Crit Care Med. 2009; 37: 2619-2624
        • Sklar Michael C.
        • Martin Dres
        • Fan Eddy
        • Rubenfeld Gordon D.
        • Scales Damon C.
        • Herridge Margaret S.
        • et al.
        Association of low baseline diaphragm muscle mass with prolonged mechanical ventilation and mortality among critically ill adults.
        JAMA Netw Open. 2020; 3e1921520
        • Bruno-Pierre Dubé
        • Martin Dres
        • Julien Mayaux
        • Suela Demiri
        • Thomas Similowski
        • Alexandre Demoule
        Ultrasound evaluation of diaphragm function in mechanically ventilated patients: comparison to phrenic stimulation and prognostic implications.
        Thorax. 2017; 72: 811-818
        • Massimo Zambon
        • Paolo Beccaria
        • Jun Matsuno
        • Marco Gemma
        • Elena Frati
        • Colombo Sergio
        • et al.
        Mechanical ventilation and diaphragmatic atrophy in critically ill patients: an ultrasound study.
        Crit Care Med. 2016;
        • Nakanishi Nobuto
        • Jun Oto
        • Ueno Yoshitoyo
        • Emiko Nakataki
        • Taiga Itagaki
        • Nishimura Masaji
        Change in diaphragm and intercostal muscle thickness in mechanically ventilated patients: a prospective observational ultrasonography study.
        J Intensive Care. 2019; 7: 56
        • Bernie Bissett
        • Anne Leditschke I.
        • Green Margot
        • Vince Marzano
        • Collins Sarajane
        • Frank Van Haren
        Inspiratory muscle training for intensive care patients: a multidisciplinary practical guide for clinicians.
        Aust Crit Care. 2019; 32: 249-255