International Journal of Critical Illness and Injury Science

CLINICAL MANAGEMENT GUIDELINE
Year
: 2020  |  Volume : 10  |  Issue : 2  |  Page : 56--63

Optimizing respiratory care in coronavirus disease-2019: A comprehensive, protocolized, evidence-based, algorithmic approach


Sagar Sinha1, Indrani Sardesai2, Sagar C Galwankar3, PW B. Nanayakkara4, Dindigal Ramakrishnan Narasimhan1, Joydeep Grover5, Harry L Anderson III6, Lorenzo Paladino7, David F Gaieski8, Salvatore Di Somma9, Stanislaw P Stawicki10,  
1 Department of Critical Care and Emergency Medicine, MGM Medical College and Hospital, Navi Mumbai, Maharashtra, India
2 Department of Accident and Emergency Medicine, Queen Elizabeth Hospital, Gateshead, United Kingdom
3 Department of Emergency Medicine, Sarasota Memorial Hospital, Florida State University, Sarasota, Florida, USA
4 Section General and Acute Internal Medicine, Amsterdam UMC, Location VU University Medical Center, Amsterdam, the, Netherlands
5 Department of Emergency Medicine, Southmead Hospital, Bristol, England, United Kingdom
6 Department of Surgery, St. Joseph Mercy Ann Arbor, Ann Arbor, Michigan
7 Department of Emergency Medicine, SUNY Downstate and Kings County Hospital Medical Center, New York, USA
8 Department of Emergency Medicine, Sidney Kimmel Medical College at Thomas Jefferson University, Philadelphia, USA
9 Department of Medical-Surgical Sciences and Translational Medicine, University of Rome “Sapienza”, Rome, Italy
10 Department of Research and Innovation, St. Luke's University Health Network, Bethlehem, Pennsylvania, USA

Correspondence Address:
Dr. Indrani Sardesai
C/O Accident and Emergency Medicine Office, Queen Elizabeth Hospital, Queen Elizabeth Avenue, Gateshead, Tyne and Wear NE96SX
United Kingdom




How to cite this article:
Sinha S, Sardesai I, Galwankar SC, B. Nanayakkara P W, Narasimhan DR, Grover J, Anderson III HL, Paladino L, Gaieski DF, Somma SD, Stawicki SP. Optimizing respiratory care in coronavirus disease-2019: A comprehensive, protocolized, evidence-based, algorithmic approach.Int J Crit Illn Inj Sci 2020;10:56-63


How to cite this URL:
Sinha S, Sardesai I, Galwankar SC, B. Nanayakkara P W, Narasimhan DR, Grover J, Anderson III HL, Paladino L, Gaieski DF, Somma SD, Stawicki SP. Optimizing respiratory care in coronavirus disease-2019: A comprehensive, protocolized, evidence-based, algorithmic approach. Int J Crit Illn Inj Sci [serial online] 2020 [cited 2020 Aug 5 ];10:56-63
Available from: http://www.ijciis.org/text.asp?2020/10/2/56/286200


Full Text



 Introduction



Respiratory management of patients with corona virus disease 2019 (COVID-19) is both complex and highly nuanced.[1] Although most patients with COVID-19 develop mild or no symptoms, a smaller proportion (up to 15%) experience progressive hypoxic respiratory failure requiring escalating levels of oxygen support.[2] Significant accumulated experience in caring for patients with SARS-CoV-2 pulmonary illness resulted in the recognition of major respiratory failure patterns, the benefits of early proning, and the importance of a step-wise escalation in levels of invasiveness across the entire spectrum from nasal cannula to extracorporeal support.[2],[3],[4] Given substantial heterogeneity among various algorithmic approaches to oxygen therapy and the need for both standardization and optimization of clinical management methodologies, the Joint ACAIM-WACEM COVID-19 Clinical Management Taskforce (CCMT) set out to establish and publish a unified approach to the patient who presents with SARS-CoV-2 lower respiratory tract infection (LRTI). In addition, the CCMT hopes that a protocol-driven strategy will lead to conservation of precious healthcare resources, such as intensive care beds and ventilators, by eliminating unnecessary interventions and various other process inefficiencies.

Clinical rationale

The Joint ACAIM-WACEM CCMT is a multidisciplinary group with participants from multiple countries and significant collective expertise in clinical management of COVID-19. Based on our shared experiences, we set out to design and optimize a uniform approach toward patients suffering from SARS-CoV-2 LRTI. The primary goal of the CCMT was to ensure broad applicability of the resultant treatment algorithms across diverse clinical settings, regardless of resource availability [Table 1]. The secondary goal was to produce a comprehensive, evidence-based resource that will provide clinicians with an easy-to-use and powerful set of tools to manage COVID-19 patients with LRTI and respiratory failure. Multiple sources were utilized when compiling this collection of algorithms and tables.[2],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20]{Table 1}

The working hypothesis adopted by the CCMT is that in COVID-19, the disease caused by SARS-CoV-2 manifests primarily as an oxygen diffusion problem rather than as alterations involving ventilation-perfusion (V/Q) mismatch, low fraction of inspired oxygen (FiO2), or hypoventilation.[1],[3],[4],[11] Consequently, we advocate that initial attempts to address the oxygenation-related impairment should include low-flow nasal cannula (LFNC) and reservoir masks, with progressive escalation to high-flow nasal cannula (HFNC) before implementing awake proning or non-invasive positive pressure ventilation (NIPPV).[11],[14],[15],[21],[22] If these maneuvers and strategies are ineffective, we advocate that a prompt transition is made toward invasive mechanical ventilatory support.[14],[22],[23] Cumulatively, the above approach serves to optimize and standardize the overall management of COVID-19 patients with LRTI. The rationale for applying different oxygen therapies to different primary pathophysiologic respiratory problems is presented in [Table 2].{Table 2}

Patient history and clinical assessment

Infection with COVID-19 should be suspected in patients presenting with “typical” signs and symptoms including fever, cough, and various degrees of hypoxia,[24] although clinical manifestations can take a number of other forms, particularly in the elderly population.[2] Patients with elevated risk of severe disease are older, immunocompromised, morbidly obese, male, or have two or more chronic comorbid conditions.[2],[24],[25],[26] Additional clinical signs and symptoms associated with severe illness include tachycardia, hyperthermia (≥39°C), encephalopathy, and hemodynamic instability.[2],[27] While a “typical” COVID-19 presentation is seen in the vast majority of cases,[2] additional specific “red flags” such as the presence of “silent hypoxia” must be kept in mind.[27],[28],[29],[30] Reliable oxygen saturation measurement (SpO2) is the cornerstone of initial risk stratification and disease severity assessment. Patients with normal (or “baseline,” if preexisting pulmonary disease exists) SpO2 are stratified as “low risk,” whereas patients with an initial SpO2 [2],[31] specific factors associated with severe respiratory disease have been identified, including the presence of myalgias, elevated hemoglobin levels, and elevated alanine aminotransferase.[2] Specific risk assessment tools may be considered including the MuLBSTA[32] and BCRSS scores.[2],[33] Moreover, laboratory findings of a neutrophil-to-lymphocyte ratio of >3.3, thrombocytopenia, markedly elevated D-dimer, and early elevations in highly sensitive troponin, are all linked to severe disease and poorer prognosis.[2],[34],[35],[36],[37] Severe COVID-19 may also be associated with elevated risk of thromboembolic events.[38]

Pertinent diagnostic and clinical monitoring criteria

Radiographic workup is an important part of the overall COVID-19 patient assessment. The initial chest radiograph shows “typical” diagnostic changes in >67% of patients, and this may increase to >95% in cases of severe disease.[35] Noncontrast computed tomography (NCCT) of the chest may correlate with both the diagnosis and severity of COVID 19, and has a reported sensitivity of >90% at 2–5 days post-onset of symptoms and 97% sensitivity thereafter.[2],[39],[40] If the NCCT findings are suspicious for COVID-19,[41] low-molecular-weight heparin administration[42] and hospital admission should be considered. If the NCCT is not suggestive of COVID-19, then contrast-enhanced CT of the chest or V/Q scanning may be considered to rule out other causes of hypoxia.

Specific clinical monitoring criteria, as directly relevant to the current manuscript, can be stratified according to patient/assessment location as well as the overall resource availability [Table 3]. Within this larger paradigm, several assessment tools need to be introduced, including the SCRUB-60 tool [Table 4][43],[44],[45] and the SBC tool [Table 5].[46],[47],[48] Finally, the risk of pneumothorax may be elevated in patients on prolonged positive pressure ventilation, necessitating tube thoracostomy placement when indicated.[49]{Table 3}{Table 4}{Table 5}

Determination of response to therapy and therapeutic escalation points

As one moves along the respiratory management algorithm, the need arises for standardized clinical checkpoints performed with a regular frequency [Table 6]. Finally, predetermined therapeutic escalation points will be important to ensure standardized application of the algorithm across different disease acuity levels [Table 7].[20]{Table 6}{Table 7}

Mechanical ventilation, proning, and extracorporeal mechanical support

Given that at least two distinct phenotypes of respiratory failure exist in COVID-19, prompt recognition of the type (L vs. H) of physiology applicable to each particular patient, followed by appropriate mechanical ventilation strategy, will be critical [Table 8].[51],[52] In addition, early and aggressive proning strategy, beginning while the patient is still on nasal cannula oxygen therapy (i.e., a strategy aimed at preventing tracheal intubation) and continuing along the entire spectrum of respiratory failure severity, is now considered critical to achieving favorable clinical outcomes.[2],[53] Finally, important considerations and limitations to prone positioning therapy are provided in [Table 9]. In terms of extracorporeal mechanical support, providers should follow established guidelines and appropriate patient suitability criteria to optimize clinical outcomes.[2]{Table 8}{Table 9}

 Summary and Conclusions



Summative algorithms for initial management of nonintubated COVID-19 patients [Figure 1]; basic mechanical ventilation approaches [Figure 2]; and advanced mechanical ventilation strategies for more severely ill patients [Figure 3] are presented at this time.[56],[57],[58] In addition, one should be ready to recognize when appropriate escalation of care transitions may be required, keeping in mind that there must be a balance between indiscriminately following a “protocol” and patient-centric consideration for individual circumstances. With that in mind, standardizing documentation ensures that all teams involved in caring for the patient remain updated and aware of previous discussions, decisions, and potential changes [Figure 4]. It is important to recognize that our understanding of SARS-CoV-2 and COVID-19 continues to evolve, and that current management strategies may change in response to increased medical and scientific knowledge of the disease process.{Figure 1}{Figure 2}{Figure 3}{Figure 4}

Special note

A full discussion regarding the complex issue of monitoring and maintaining adequate oxygenation in the outpatient/home setting is beyond the scope of this document; however, a dedicated Joint ACAIM-WACEM COVID-19 Clinical Management Taskforce guideline is forthcoming with recommendations specific to the implementation of home-based oxygenation strategy in patients with isolated hypoxia and clinically mild disease.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Dondorp AM, Hayat M, Aryal D, Beane A, Schultz MJ. Respiratory support in novel coronavirus disease (COVID-19) patients, with a focus on resource-limited settings. Am J Trop Med Hyg 2020:tpmd200283.
2Stawicki SP, Jeanmonod R, Miller AC, Paladino L, Gaieski DF, Yaffee AQ, et al. The 2019–2020 Novel Coronavirus (Severe Acute Respiratory Syndrome Coronavirus 2) Pandemic: A Joint American College of Academic International Medicine-World Academic Council of Emergency Medicine Multidisciplinary COVID-19 Working Group Consensus Paper. J Global Infect Dis 2020;(2):47-93.
3Gattinoni L, Coppola S, Cressoni M, Busana M, Rossi S, Chiumello D, et al. Covid-19 does not lead to a “typical” acute respiratory distress syndrome. Am J Resp Critical Care Med 2020;201:1299-300. PMC7233352.
4Sun Q, Qiu H, Huang M, Yang Y. Lower mortality of COVID-19 by early recognition and intervention: Experience from Jiangsu Province. Ann Intensive Care 2020;10:33.
5Brower RG, Lanken PN, MacIntyre N, Matthay MA, Morris A, Ancukiewicz M, et al., National Heart, Lung, and Blood Institute ARDS Clinical Trials Network. Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. New England J Med 2004;351:327-36.
6Chorin E, Padegimas A, Havakuk O, Birati EY, Shacham Y, Milman A, et al. Assessment of Respiratory Distress by the Roth Score. Clin Cardiol 2016;39:636-9.
7Devabhakthuni S, Armahizer MJ, Dasta JF, Kane-Gill SL. Analgosedation: A paradigm shift in intensive care unit sedation practice. Ann Pharmacother 2012;46:530-40.
8Dwyer R, Hedlund J, Henriques-Normark B, Kalin M. Improvement of CRB-65 as a prognostic tool in adult patients with community-acquired pneumonia. BMJ Open Respir Res 2014;1:e000038.
9Firstenberg MS. Extracorporeal Membrane Oxygenation: Advances in Therapy. London, England: IntechOpen; 2016.
10Festic E, Bansal V, Kor DJ, Gajic O, US Critical Illness and Injury Trials Group: Lung Injury Prevention Study Investigators (USCIITG–LIPS). SpO2/FiO2 ratio on hospital admission is an indicator of early acute respiratory distress syndrome development among patients at risk. J Intensive Care Med 2015;30:209-16.
11Gattinoni L, Chiumello D, Caironi P, Busana M, Romitti F, Brazzi L, et al. COVID-19 pneumonia: Different respiratory treatments for different phenotypes? Intensive Care Med 2020:1.
12Kądziołka I, Świstek R, Borowska K, Tyszecki P, Serednicki W. Validation of APACHE II and SAPS II scales at the intensive care unit along with assessment of SOFA scale at the admission as an isolated risk of death predictor. Anaesthesiol Intensive Ther 2019;51:107-11.
13Kolditz M, Ewig S, Schütte H, Suttorp N, Welte T, Rohde G, et al. Assessment of oxygenation and comorbidities improves outcome prediction in patients with community-acquired pneumonia with a low CRB-65 score. J Int Med 2015;278:193-202.
14Koulouras V, Papathanakos G, Papathanasiou A, Nakos G. Efficacy of prone position in acute respiratory distress syndrome patients: A pathophysiology-based review. World J Crit Care Med 2016;5:121-36.
15Marini JJ, Gattinoni L. Management of COVID-19 respiratory distress. JAMA 2020. Available from: https://www.ncbi.nlm.nih.gov/pubmed/32329799. [Last accessed on 2020 May 24].
16Marini JJ, Hotchkiss JR, Broccard AF. Bench-to-bedside review: Microvascular and airspace linkage in ventilator-induced lung injury. Critical Care 2003;7:435.
17Messerole E, Peine P, Wittkopp S, Marini JJ, Albert RK. The pragmatics of prone positioning. Am J Respir Crit Care Med 2002;165:1359-63.
18Peterson CM, Thomas DM, Blackburn GL, Heymsfield SB. Universal equation for estimating ideal body weight and body weight at any BMI. Am J Clin Nutr 2016;103:1197-203.
19Roca O, Caralt B, Messika J, Samper M, Sztrymf B, Hernández G, et al. An index combining respiratory rate and oxygenation to predict outcome of nasal high-flow therapy. Am J Respir Crit Care Med 2019;199:1368-76.
20Roca O, Messika J, Caralt B, García-de-Acilu M, Sztrymf B, Ricard JD, et al. Predicting success of high-flow nasal cannula in pneumonia patients with hypoxemic respiratory failure: The utility of the ROX index. J Crit Care 2016;35:200-5.
21Aoyama H, Yamada Y, Fan E. The future of driving pressure: a primary goal for mechanical ventilation? J Intensive Care 2018;6:64.
22Mauri T, Spinelli E, Scotti E, Colussi G, Basile MC, Crotti S, et al. Potential for lung recruitment and ventilation-perfusion mismatch in patients with the acute respiratory distress syndrome from coronavirus disease 2019. Crit Care Med 2020. Available from: https://pubmed.ncbi.nlm.nih.gov/32317591/. [Last accessed on 2020 May 24].
23Oliveira VM, Weschenfelder ME, Deponti G, Condessa R, Loss SH, Bairros PM, et al. Good practices for prone positioning at the bedside: Construction of a care protocol. Rev Assoc Med Bras (1992) 2016;62:287-93.
24Verity R, Okell LC, Dorigatti I, Winskill P, Whittaker C, Imai N, et al. Estimates of the severity of coronavirus disease 2019: A model-based analysis. Lancet Infect Dis 2020. Available from: https://www.ncbi.nlm.nih.gov/pubmed/32240634. [Last accessed on 2020 May 24].
25Tolentino JC, Stoltzfus JC, Harris R, Foltz D, Deringer P, Sakran JV, et al. Comorbidity-polypharmacy score predicts readmissions and in-hospital mortality: A six-hospital health network experience. J Basic Clin Pharmacy 2017;8:98-103.
26Stawicki SP, Kalra S, Jones C, Justiniano CF, Papadimos TJ, Galwankar SC, et al. Comorbidity polypharmacy score and its clinical utility: A pragmatic practitioner's perspective. J Emerg Trauma Shock 2015;8:224.
27Galwankar SC, Paladino L, Gaieski DF, Nanayakkara KDPWB, Di Somma S, Grover J, et al. Management algorithm for subclinical hypoxemia in COVID-19 patients: Intercepting the 'silent killer'. J Emerg Trauma Shock 2020;13:8-11.
28Uyeki TM, Bundesmann M, Alhazzani W. Clinical management of critically ill adults with coronavirus disease 2019 (COVID-19). 2020. Avaliable from: https://stacks.cdc.gov/view/cdc/86712/cdc_86712_DS1.pdf. [Last accessed on 2020 May 21].
29Levitan R. The Infection that's Silently Killing Coronavirus Patients; 20 April, 2020. Available from: https://www.nytimes.com/2020/04/20/opinion/coronavirus-testing-pneumonia.html. [Last accessed on 2020 May 21].
30Liu Y, Yan LM, Wan L, Xiang TX, Le A, Liu JM, et al. Viral dynamics in mild and severe cases of COVID-19. Lancet Infect Dis 2020; Available from: https://www.ncbi.nlm.nih.gov/pubmed/32199493. [Last accessed on 2020 May 24].
31Cascella M, Rajnik M, Cuomo A, Dulebohn SC, Di Napoli R. Features, evaluation and treatment coronavirus (COVID-19) StatPearls 2020. Available from: https://pubmed.ncbi.nlm.nih.gov/32150360/. PMID: 32150360. [Last accessed on 2020 May 24].
32Guo L, Wei D, Zhang X, Wu Y, Li Q, Zhou M, et al. Clinical features predicting mortality risk in patients with viral pneumonia: The MuLBSTA Score. Front Microbiol 2019;10:2752.
33Duca A, Piva S, Foca E, Latronico N, Rizzi M. Brescia-COVID Respiratory Severity Scale (BCRSS)/Algorithm; 8 April, 2020. Available from: https://www.mdcalc.com/brescia-covid-respiratory-severity-scale-bcrss-algorithm. [Last accessed on 2020 May 21].
34Yang AP, Liu JP, Tao WQ, Li HM. A the diagnostic and predictive role of NLR, d-NLR and PLR in COVID-19 patients. Int Immunopharmacol 2020;84:106504.
35Lippi G, Lavie CJ, Sanchis-Gomar F. Cardiac troponin I in patients with coronavirus disease 2019 (COVID-19): Evidence from a meta-analysis. Prog Cardiovasc Dis 2020. Available from: https://www.ncbi.nlm.nih.gov/pubmed/32169400. [Last accessed on 2020 May 24].
36Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 2020;395:1054-62.
37Giannis D, Ziogas IA, Gianni P. Coagulation disorders in coronavirus infected patients: COVID-19, SARS-CoV-1, MERS-CoV and lessons from the past. J Clin Virol 2020;127:104362.
38Bikdeli B, Madhavan MV, Jimenez D, Chuich T, Dreyfus I, Driggin E, et al. COVID-19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow-up. J Am Coll Cardiol 2020. Available from: https://pubmed.ncbi.nlm.nih.gov/32311448/. [Last accessed on 2020 May 21].
39Rodrigues JCL, Hare SS, Edey A, Devaraj A, Jacob J, Johnstone A, et al. An update on COVID-19 for the radiologist-A British Society of Thoracic Imaging Statement. Clin Radiol 2020;75:323-5.
40Wong HYF, Lam HYS, Fong AH, Leung ST, Chin TW, Lo CSY, et al. Frequency and Distribution of Chest Radiographic Findings in COVID-19 Positive Patients. Radiology 2019:201160.
41Ai T, Yang Z, Hou H, Zhan C, Chen C, Lv W, et al. Correlation of chest CT and RT-PCR Testing in Coronavirus Disease 2019 (COVID-19) in China: A Report of 1014 Cases. Radiology 2020:200642.
42Tang N, Bai H, Chen X, Gong J, Li D, Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemostasis 2020;18:1094-9.
43Shindo Y, Sato S, Maruyama E, Ohashi T, Ogawa M, Imaizumi K, et al. Comparison of severity scoring systems A-DROP and CURB-65 for community-acquired pneumonia. Respirology 2008;13:731-5.
44Parsonage M, Nathwani D, Davey P, Barlow G. Evaluation of the performance of CURB-65 with increasing age. Clin Microbiol Infect 2009;15:858-64.
45Mulrennan S, Tempone SS, Ling IT, Williams SH, Gan GC, Murray RJ, et al. Pandemic influenza (H1N1) 2009 pneumonia: CURB-65 score for predicting severity and nasopharyngeal sampling for diagnosis are unreliable. PLoS One 2010;5:e12849.
46Kalita J, Kumar M, Misra UK. Serial single breath count is a reliable tool for monitoring respiratory functions in Guillain-Barré Syndrome. J Clin Neurosci 2020;72:50-6.
47Kumari A, Malik S, Narkeesh K, Samuel AJ. Single breath count: A simple pulmonary function test using a mobile app. Indian J Thoracic Cardiovascular Surg 2017;33:369-370.
48Greenhalgh T, Kotze K, van Der Westhuizen HM. Are There any Evidence-Based Ways of Assessing Dyspnoea (breathlessness) by Telephone or Video; 6 May, 2020. Available from: https://www.cebm.net/covid-19/are-there-any-evidence-based-ways-of-assessing-dyspnoea-breathlessness-by-telephone-or-video/. [Last accessed on 2020 May 21].
49Sun R, Liu H, Wang X. Mediastinal emphysema, giant bulla, and pneumothorax developed during the course of COVID-19 pneumonia. Korean J Radiol 2020;21:541.]
50Kądziołka I, Świstek R, Borowska K, Tyszecki P, Serednicki W. Validation of APACHE II and SAPS II scales at the intensive care unit along with assessment of SOFA scale at the admission as an isolated risk of death predictor. Anaesthesiol Intensive Ther 2019;51:107-11.
51Gattinoni L, Chiumello D, Caironi P, Busana M, Romitti F, Brazzi L, et al. COVID-19 pneumonia: Different respiratory treatment for different phenotypes? Intensive Care Med 2020. Available from: https://pubmed.ncbi.nlm.nih.gov/32291463/. [Last accessed on 2020 May 24].
52Marini JJ, Gattinoni L. Management of COVID-19 Respiratory Distress. JAMA Insights 2020;2020:doi:10.1001/jama.2020.6825.
53Gattinoni L, Taccone P, Carlesso E, Marini JJ. Prone position in acute respiratory distress syndrome. Rationale, indications, and limits. Am J Respir Crit Care Med 2013;188:1286-93.
54Marini JJ, Hotchkiss JR, Broccard AF. Bench-to-bedside review: Microvascular and airspace linkage in ventilator-induced lung injury. Crit Care 2003;7:435-44.
55Amato MB, Meade MO, Slutsky AS, Brochard L, Costa EL, Schoenfeld DA, et al. Driving pressure and survival in the acute respiratory distress syndrome. N Engl J Med 2015;372:747-55.
56ARDSNet. Mechanical Ventilation Protocol Summary; 2008. Available from: http://www.ardsnet.org. [Last accessed on 2020 May 09].
57Brower RG, Lanken PN, MacIntyre N, Matthay MA, Morris A, Ancukiewicz M, et al. Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. N Engl J Med 2004;351:327-36.
58Vincent JL, Abraham E, Kochanek P, Moore FA, Fink MP. Textbook of Critical Care. 7th ed. Philadelphia, Pennsylvania: Elsevier. 2016.