Semin Respir Crit Care Med 2022; 43(03): 379-389
DOI: 10.1055/s-0042-1744306
Review Article

Insights Regarding the Berlin Definition of ARDS from Prospective Observational Studies

Ciara Hanley
1   Department of Anaesthesia and Intensive Care medicine, Galway University Hospitals, Saolta University Hospital Group, Galway, Ireland
,
Camilla Giacomini
1   Department of Anaesthesia and Intensive Care medicine, Galway University Hospitals, Saolta University Hospital Group, Galway, Ireland
,
Aoife Brennan
1   Department of Anaesthesia and Intensive Care medicine, Galway University Hospitals, Saolta University Hospital Group, Galway, Ireland
2   School of Medicine, National University of Ireland, Galway, Ireland
,
Bairbre McNicholas
1   Department of Anaesthesia and Intensive Care medicine, Galway University Hospitals, Saolta University Hospital Group, Galway, Ireland
2   School of Medicine, National University of Ireland, Galway, Ireland
,
John G. Laffey
1   Department of Anaesthesia and Intensive Care medicine, Galway University Hospitals, Saolta University Hospital Group, Galway, Ireland
2   School of Medicine, National University of Ireland, Galway, Ireland
3   Regenerative Medicine Institute, National University of Ireland, Galway, Ireland
› Author Affiliations

Abstract

The definition of acute respiratory distress syndrome (ARDS), has evolved since it was first described in 1967 by Ashbaugh and Petty to the current “Berlin” definition of ARDS developed in 2012 by an expert panel, that provided clarification on the definition of “acute,” and on the cardiac failure criteria. It expanded the definition to include patients receiving non-invasive ventilation, and removed the term “acute lung injury” and added a requirement of patients to be receiving a minimum 5 cmH2O expiratory pressure.

Since 2012, a series of observational cohort studies have generated insights into the utility and robustness of this definition. This review will examine novel insights into the epidemiology of ARDS, failures in ARDS diagnosis, the role of lung imaging in ARDS, the novel ARDS cohort that is not invasively ventilated, lung compliance profiles in patients with ARDS, sex differences that exist in ARDS management and outcomes, the progression of ARDS following initial diagnosis, and the clinical profile and outcomes of confirmed versus resolved ARDS. Furthermore, we will discuss studies that challenge the utility of distinguishing ARDS from other causes of acute hypoxemic respiratory failure (AHRF) and identify issues that may need to be addressed in a revised definition.



Publication History

Article published online:
09 June 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Ashbaugh DG, Bigelow DB, Petty TL, Levine BE. Acute respiratory distress in adults. Lancet 1967; 2 (7511): 319-323
  • 2 Pearce FJ, Lyons WS. Logistics of parenteral fluids in battlefield resuscitation. Mil Med 1999; 164 (09) 653-655
  • 3 Murray JF, Matthay MA, Luce JM, Flick MR. An expanded definition of the adult respiratory distress syndrome. Am Rev Respir Dis 1988; 138 (03) 720-723
  • 4 Bernard GR, Artigas A, Brigham KL. et al. Consensus Committee. Report of the American-European Consensus conference on acute respiratory distress syndrome: definitions, mechanisms, relevant outcomes, and clinical trial coordination. J Crit Care 1994; 9 (01) 72-81
  • 5 Ranieri VM, Rubenfeld GD, Thompson BT. et al. ARDS Definition Task Force. Acute respiratory distress syndrome: the Berlin definition. JAMA 2012; 307 (23) 2526-2533
  • 6 Caser EB, Zandonade E, Pereira E, Gama AM, Barbas CS. Impact of distinct definitions of acute lung injury on its incidence and outcomes in Brazilian ICUs: prospective evaluation of 7,133 patients*. Crit Care Med 2014; 42 (03) 574-582
  • 7 Luhr OR, Antonsen K, Karlsson M. et al. The ARF Study Group. Incidence and mortality after acute respiratory failure and acute respiratory distress syndrome in Sweden, Denmark, and Iceland. Am J Respir Crit Care Med 1999; 159 (06) 1849-1861
  • 8 Bersten AD, Edibam C, Hunt T, Moran J. Australian and New Zealand Intensive Care Society Clinical Trials Group. Incidence and mortality of acute lung injury and the acute respiratory distress syndrome in three Australian States. Am J Respir Crit Care Med 2002; 165 (04) 443-448
  • 9 Rubenfeld GD, Caldwell E, Peabody E. et al. Incidence and outcomes of acute lung injury. N Engl J Med 2005; 353 (16) 1685-1693
  • 10 Linko R, Okkonen M, Pettilä V. et al. FINNALI-study group. Acute respiratory failure in intensive care units. FINNALI: a prospective cohort study. Intensive Care Med 2009; 35 (08) 1352-1361
  • 11 Manzano F, Yuste E, Colmenero M. et al. Granada Respiratory Failure Study Group. Incidence of acute respiratory distress syndrome and its relation to age. J Crit Care 2005; 20 (03) 274-280
  • 12 Brun-Buisson C, Minelli C, Bertolini G. et al. ALIVE Study Group. Epidemiology and outcome of acute lung injury in European intensive care units. Results from the ALIVE study. Intensive Care Med 2004; 30 (01) 51-61
  • 13 Sakr Y, Vincent JL, Reinhart K. et al. Sepsis Occurence in Acutely Ill Patients Investigators. High tidal volume and positive fluid balance are associated with worse outcome in acute lung injury. Chest 2005; 128 (05) 3098-3108
  • 14 Irish Critical Care Trials Group. Acute lung injury and the acute respiratory distress syndrome in Ireland: a prospective audit of epidemiology and management. Crit Care 2008; 12 (01) R30
  • 15 Bellani G, Laffey JG, Pham T. et al. LUNG SAFE Investigators, ESICM Trials Group. Group ObotLSIatET. Epidemiology, patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries. JAMA 2016; 315 (08) 788-800
  • 16 Neto AS, Barbas CSV, Simonis FD. et al. PRoVENT, PROVE Network investigators. Epidemiological characteristics, practice of ventilation, and clinical outcome in patients at risk of acute respiratory distress syndrome in intensive care units from 16 countries (PRoVENT): an international, multicentre, prospective study. Lancet Respir Med 2016; 4 (11) 882-893
  • 17 Ferguson ND, Frutos-Vivar F, Esteban A. et al. Acute respiratory distress syndrome: underrecognition by clinicians and diagnostic accuracy of three clinical definitions. Crit Care Med 2005; 33 (10) 2228-2234
  • 18 Hager DN, Krishnan JA, Hayden DL, Brower RG. ARDS Clinical Trials Network. Tidal volume reduction in patients with acute lung injury when plateau pressures are not high. Am J Respir Crit Care Med 2005; 172 (10) 1241-1245
  • 19 Needham DM, Yang T, Dinglas VD. et al. Timing of low tidal volume ventilation and intensive care unit mortality in acute respiratory distress syndrome. A prospective cohort study. Am J Respir Crit Care Med 2015; 191 (02) 177-185
  • 20 Laffey JG, Pham T, Bellani G. Continued under-recognition of acute respiratory distress syndrome after the Berlin definition: what is the solution?. Curr Opin Crit Care 2017; 23 (01) 10-17
  • 21 Bellani G, Pham T, Laffey JG. Missed or delayed diagnosis of ARDS: a common and serious problem. Intensive Care Med 2020; 46 (06) 1180-1183
  • 22 Singhal L, Garg Y, Yang P. et al. eARDS: A multi-center validation of an interpretable machine learning algorithm of early onset Acute Respiratory Distress Syndrome (ARDS) among critically ill adults with COVID-19. PLoS One 2021; 16 (09) e0257056
  • 23 Bhattarai S, Gupta A, Ali E. et al. Can big data and machine learning improve our understanding of acute respiratory distress syndrome?. Cureus 2021; 13 (02) e13529
  • 24 Rubenfeld GD, Caldwell E, Granton J, Hudson LD, Matthay MA. Interobserver variability in applying a radiographic definition for ARDS. Chest 1999; 116 (05) 1347-1353
  • 25 Sjoding MW, Hofer TP, Co I, Courey A, Cooke CR, Iwashyna TJ. Interobserver reliability of the Berlin ARDS definition and strategies to improve the reliability of ARDS diagnosis. Chest 2018; 153 (02) 361-367
  • 26 Meade MO, Cook RJ, Guyatt GH. et al. Interobserver variation in interpreting chest radiographs for the diagnosis of acute respiratory distress syndrome. Am J Respir Crit Care Med 2000; 161 (01) 85-90
  • 27 Figueroa-Casas JB, Brunner N, Dwivedi AK, Ayyappan AP. Accuracy of the chest radiograph to identify bilateral pulmonary infiltrates consistent with the diagnosis of acute respiratory distress syndrome using computed tomography as reference standard. J Crit Care 2013; 28 (04) 352-357
  • 28 Lichtenstein D, Goldstein I, Mourgeon E, Cluzel P, Grenier P, Rouby JJ. Comparative diagnostic performances of auscultation, chest radiography, and lung ultrasonography in acute respiratory distress syndrome. Anesthesiology 2004; 100 (01) 9-15
  • 29 Goddard SL, Rubenfeld GD, Manoharan V. et al. The randomized educational acute respiratory distress syndrome diagnosis study: a trial to improve the radiographic diagnosis of acute respiratory distress syndrome. Crit Care Med 2018; 46 (05) 743-748
  • 30 Ferguson ND, Fan E, Camporota L. et al. The Berlin definition of ARDS: an expanded rationale, justification, and supplementary material. Intensive Care Med 2012; 38 (10) 1573-1582
  • 31 Warren MA, Zhao Z, Koyama T. et al. Severity scoring of lung oedema on the chest radiograph is associated with clinical outcomes in ARDS. Thorax 2018; 73 (09) 840-846
  • 32 Wallet F, Delannoy B, Haquin A. et al. Evaluation of recruited lung volume at inspiratory plateau pressure with PEEP using bedside digital chest X-ray in patients with acute lung injury/ARDS. Respir Care 2013; 58 (03) 416-423
  • 33 Kotok D, Yang L, Evankovich JW. et al. The evolution of radiographic edema in ARDS and its association with clinical outcomes: a prospective cohort study in adult patients. J Crit Care 2020; 56: 222-228
  • 34 Zimatore C, Pisani L, Lippolis V. et al. Accuracy of the radiographic assessment of lung edema score for the diagnosis of ARDS. Front Physiol 2021; 12: 672823
  • 35 Pesenti A, Tagliabue P, Patroniti N, Fumagalli R. Computerized tomography scan imaging in acute respiratory distress syndrome. Intensive Care Med 2001; 27 (04) 631-639
  • 36 Mojoli F, Bouhemad B, Mongodi S, Lichtenstein D. Lung ultrasound for critically ill patients. Am J Respir Crit Care Med 2019; 199 (06) 701-714
  • 37 Lichtenstein DA. Lung ultrasound in the critically ill. Ann Intensive Care 2014; 4 (01) 1
  • 38 Falster C, Jacobsen N, Wulff Madsen L. et al. Lung ultrasound may be a valuable aid in decision making for patients admitted with COVID-19 disease. Eur Clin Respir J 2021; 8 (01) 1909521
  • 39 Dargent A, Chatelain E, Si-Mohamed S. et al. COVIDLUS study group. Lung ultrasound score as a tool to monitor disease progression and detect ventilator-associated pneumonia during COVID-19-associated ARDS. Heart Lung 2021; 50 (05) 700-705
  • 40 Bouhemad B, Brisson H, Le-Guen M, Arbelot C, Lu Q, Rouby JJ. Bedside ultrasound assessment of positive end-expiratory pressure-induced lung recruitment. Am J Respir Crit Care Med 2011; 183 (03) 341-347
  • 41 Riviello ED, Kiviri W, Twagirumugabe T. et al. Hospital incidence and outcomes of the acute respiratory distress syndrome using the Kigali modification of the Berlin definition. Am J Respir Crit Care Med 2016; 193 (01) 52-59
  • 42 Dumas G, Lemiale V, Rathi N. et al. Survival in immunocompromised patients ultimately requiring invasive mechanical ventilation: a pooled individual patient data analysis. Am J Respir Crit Care Med 2021; 204 (02) 187-196
  • 43 Ferrer M, Esquinas A, Leon M, Gonzalez G, Alarcon A, Torres A. Noninvasive ventilation in severe hypoxemic respiratory failure: a randomized clinical trial. Am J Respir Crit Care Med 2003; 168 (12) 1438-1444
  • 44 Antonelli M, Conti G, Esquinas A. et al. A multiple-center survey on the use in clinical practice of noninvasive ventilation as a first-line intervention for acute respiratory distress syndrome. Crit Care Med 2007; 35 (01) 18-25
  • 45 Bellani G, Laffey JG, Pham T. et al. Non-invasive Ventilation of Patients with ARDS: Insights from the LUNG SAFE Study. Am J Respir Crit Care Med 2017; Jan 1; 195 (01) 67-77
  • 46 Carteaux G, Millán-Guilarte T, De Prost N. et al. Failure of noninvasive ventilation for de novo acute hypoxemic respiratory failure: role of tidal volume. Crit Care Med 2016; 44 (02) 282-290
  • 47 Patel BK, Wolfe KS, Pohlman AS, Hall JB, Kress JP. Effect of noninvasive ventilation delivered by Helmet vs face mask on the rate of endotracheal intubation in patients with acute respiratory distress syndrome: a randomized clinical trial. JAMA 2016; 315 (22) 2435-2441
  • 48 Chawla R, Mansuriya J, Modi N. et al. Acute respiratory distress syndrome: predictors of noninvasive ventilation failure and intensive care unit mortality in clinical practice. J Crit Care 2016; 31 (01) 26-30
  • 49 Frat JP, Ragot S, Coudroy R. et al. REVA network. Predictors of intubation in patients with acute hypoxemic respiratory failure treated with a noninvasive oxygenation strategy. Crit Care Med 2018; 46 (02) 208-215
  • 50 Matthay MA, Thompson BT, Ware LB. The Berlin definition of acute respiratory distress syndrome: should patients receiving high-flow nasal oxygen be included?. Lancet Respir Med 2021; 9 (08) 933-936
  • 51 Gattinoni L, Caironi P, Cressoni M. et al. Lung recruitment in patients with the acute respiratory distress syndrome. N Engl J Med 2006; 354 (17) 1775-1786
  • 52 Gattinoni L, Chiumello D, Caironi P. et al. COVID-19 pneumonia: different respiratory treatments for different phenotypes?. Intensive Care Med 2020; 46 (06) 1099-1102
  • 53 Gattinoni L, Camporota L, Marini JJ. COVID-19 phenotypes: leading or misleading?. Eur Respir J 2020; 56 (02) 56
  • 54 Camporota L, Vasques F, Sanderson B, Barrett NA, Gattinoni L. Identification of pathophysiological patterns for triage and respiratory support in COVID-19. Lancet Respir Med 2020; 8 (08) 752-754
  • 55 Vandenbunder B, Ehrmann S, Piagnerelli M. et al. COVADIS study group. Static compliance of the respiratory system in COVID-19 related ARDS: an international multicenter study. Crit Care 2021; 25 (01) 52
  • 56 Ferrando C, Suarez-Sipmann F, Mellado-Artigas R. et al. COVID-19 Spanish ICU Network. Clinical features, ventilatory management, and outcome of ARDS caused by COVID-19 are similar to other causes of ARDS. Intensive Care Med 2020; 46 (12) 2200-2211
  • 57 Panwar R, Madotto F, Laffey JG, van Haren FMP. Compliance phenotypes in early acute respiratory distress syndrome before the COVID-19 pandemic. Am J Respir Crit Care Med 2020; 202 (09) 1244-1252
  • 58 Walkey AJ, Wiener RS. Risk factors for underuse of lung-protective ventilation in acute lung injury. J Crit Care 2012; 27: 323 e321-329
  • 59 Han S, Martin GS, Maloney JP. et al. Short women with severe sepsis-related acute lung injury receive lung protective ventilation less frequently: an observational cohort study. Crit Care 2011; 15 (06) R262
  • 60 LAS VEGAS investigators. Epidemiology, practice of ventilation and outcome for patients at increased risk of postoperative pulmonary complications: LAS VEGAS—an observational study in 29 countries. Eur J Anaesthesiol 2017; 34 (08) 492-507
  • 61 McNicholas BA, Madotto F, Pham T. et al. LUNG SAFE Investigators and the ESICM Trials Group. Demographics, management and outcome of females and males with acute respiratory distress syndrome in the LUNG SAFE prospective cohort study. Eur Respir J 2019; 54 (04) 54
  • 62 Schultz MJ, Karagiannidis C. Is gender inequity in ventilator management a “women's issue”?. Eur Respir J 2019; 54 (04) 54
  • 63 Swart P, Deliberato RO, Johnson AEW. et al. Impact of sex on use of low tidal volume ventilation in invasively ventilated ICU patients—a mediation analysis using two observational cohorts. PLoS One 2021; 16 (07) e0253933
  • 64 Heffernan DS, Dossett LA, Lightfoot MA. et al. Gender and acute respiratory distress syndrome in critically injured adults: a prospective study. J Trauma 2011; 71 (04) 878-883 , discussion 883–885
  • 65 Pham T, Serpa Neto A, Pelosi P. et al. LUNG SAFE Investigators* and the European Society of Intensive Care Medicine Trials Group. Outcomes of patients presenting with mild acute respiratory distress syndrome: insights from the LUNG SAFE study. Anesthesiology 2019; 130 (02) 263-283
  • 66 Madotto F, Pham T, Bellani G. et al. LUNG SAFE Investigators and the ESICM Trials Group. Resolved versus confirmed ARDS after 24 h: insights from the LUNG SAFE study. Intensive Care Med 2018; 44 (05) 564-577
  • 67 Cereda M, Xin Y, Hamedani H. et al. Tidal changes on CT and progression of ARDS. Thorax 2017; 72 (11) 981-989
  • 68 Calfee CS, Delucchi KL, Sinha P. et al. Irish Critical Care Trials Group. Acute respiratory distress syndrome subphenotypes and differential response to simvastatin: secondary analysis of a randomised controlled trial. Lancet Respir Med 2018; 6 (09) 691-698
  • 69 Fröhlich S, Murphy N, Boylan JF. ARDS: progress unlikely with non-biological definition. Br J Anaesth 2013; 111 (05) 696-699
  • 70 Villar J, Fernández RL, Ambrós A. et al. Acute Lung Injury Epidemiology and Natural history Network. A clinical classification of the acute respiratory distress syndrome for predicting outcome and guiding medical therapy*. Crit Care Med 2015; 43 (02) 346-353
  • 71 Kelly FE, Fong K, Hirsch N, Nolan JP. Intensive care medicine is 60 years old: the history and future of the intensive care unit. Clin Med (Lond) 2014; 14 (04) 376-379
  • 72 Group ST. SRLF Trial Group. Hypoxemia in the ICU: prevalence, treatment, and outcome. Ann Intensive Care 2018; 8 (01) 82
  • 73 Vincent JL, Akça S, De Mendonça A. et al. SOFA Working Group. Sequntial organ failure assessment. The epidemiology of acute respiratory failure in critically ill patients(*). Chest 2002; 121 (05) 1602-1609
  • 74 Pham T, Pesenti A, Bellani G. et al. the European Society of Intensive Care Medicine Trials G. Outcome of acute hypoxaemic respiratory failure: insights from the LUNG SAFE Study. Eur Respir J 2021; Jun 10; 57 (06) 2003317
  • 75 Choi WI, Shehu E, Lim SY. et al. Korean Study group on Respiratory Failure (KOSREF). Markers of poor outcome in patients with acute hypoxemic respiratory failure. J Crit Care 2014; 29 (05) 797-802
  • 76 Sathe NA, Zelnick LR, Mikacenic C. et al. Identification of persistent and resolving subphenotypes of acute hypoxemic respiratory failure in two independent cohorts. Crit Care 2021; 25 (01) 336
  • 77 Parhar KKS, Stelfox HT, Fiest KM. et al. Standardized management for hypoxemic respiratory failure and ARDS: systematic review and meta-analysis. Chest 2020; 158 (06) 2358-2369
  • 78 Alviar CL, Miller PE, McAreavey D. et al. ACC Critical Care Cardiology Working Group. Positive pressure ventilation in the cardiac intensive care unit. J Am Coll Cardiol 2018; 72 (13) 1532-1553
  • 79 Vallabhajosyula S, Kashani K, Dunlay SM. et al. Acute respiratory failure and mechanical ventilation in cardiogenic shock complicating acute myocardial infarction in the USA, 2000-2014. Ann Intensive Care 2019; 9 (01) 96
  • 80 Semler MW, Bernard GR, Aaron SD. et al. Identifying clinical research priorities in adult pulmonary and critical care: NHLBI working group report. Am J Respir Crit Care Med 2020; Mar 9; 202 (04) 511-523