Article Critique

REVIEW

CURRENT OPINION Setting positive end-expiratory pressure: lung and

diaphragm ultrasound

1070-5295 Copyright © 2023 The A

a,b,c a,b,c a,b,c

Amne Mousa , Peter Klompmaker and Pieter R. Tuinman

Purpose of review The purpose of this review is to summarize the role of lung ultrasound and diaphragm ultrasound in guiding ventilator settings with an emphasis on positive end-expiratory pressure (PEEP). Recent advances for using ultrasound to assess the effects of PEEP on the lungs and diaphragm are discussed.

Recent findings Lung ultrasound can accurately diagnose the cause of acute respiratory failure, including acute respiratory distress syndrome and can identify focal and nonfocal lung morphology in these patients. This is essential in determining optimal ventilator strategy and PEEP level. Assessment of the effect of PEEP on lung recruitment using lung ultrasound is promising, especially in the perioperative setting. Diaphragm ultrasound can monitor the effects of PEEP on the diaphragm, but this needs further validation. In patients with an acute exacerbation of chronic obstructive pulmonary disease, diaphragm ultrasound can be used to predict noninvasive ventilation failure. Lung and diaphragm ultrasound can be used to predict weaning outcome and accurately diagnose the cause of weaning failure.

Summary Lung and diaphragm ultrasound are useful for diagnosing the cause of respiratory failure and subsequently setting the ventilator including PEEP. Effects of PEEP on lung and diaphragm can be monitored using ultrasound.

Keywords diaphragm, lung, mechanical ventilation, positive end-expiratory pressure, ultrasonography

INTRODUCTION In this narrative review, we discuss the role of

a Department of Intensive Care, Amsterdam UMC location Vrije Univer- siteit Amsterdam, b

Amsterdam Cardiovascular Sciences research insti- tute, Amsterdam UMC and c

Amsterdam Leiden Intensive Care Focused Echography (ALIFE), Amsterdam, The Netherlands

Correspondence to Pieter R. Tuinman, MD, PhD, Amsterdam UMC location Vrije Universiteit Amsterdam, Department of Intensive Care Medicine, De Boelelaan 1117, 1081HV Amsterdam, The Netherlands. Tel: +31 20 444 4444; e-mail: [email protected]

Curr Opin Crit Care 2024, 30:53–60

DOI:10.1097/MCC.0000000000001119

This is an open access article distributed under the Creative Commons Attribution License 4.0 (CCBY), which permits unrestricted use, dis- tribution, and reproduction in any medium, provided the original work is properly cited.

The choice of ventilator settings depends upon the underlying cause of respiratory failure and condi- tion of the patient [1]. Positive end-expiratory pres- sure (PEEP) is one of the cornerstones of any ventilation strategy but remains one of the most difficult parameters to set; both too low or too high PEEP can have detrimental effects. A balance must be reached between lung recruitment and improved gas exchange versus overdistention and hemody- namic consequences [1]. Several bedside tools, such as plateau pressures, PEEP/FiO2 tables and oesopha- geal manometry, are used to set PEEP. However, thus far, none of these methods has improved outcomes in clinical trials [1].

In addition, careful bedside assessment is needed to evaluate both the positive and negative effects of PEEP. Critical care ultrasonography, increasingly used in daily practice, is a promising tool for bedside assessment in this matter [2]. Both lung ultrasound and diaphragm ultrasound are fre- quently used for diagnosing and monitoring patients with acute respiratory failure [3,4&

,5 &

] and their use has a major impact on patient manage- ment, including ventilator settings [6].

uthor(s). Published by Wolters Kluwe

lung ultrasound and diaphragm ultrasound in per- sonalisation of ventilator settings. We give a brief overview of how lung ultrasound and diaphragm ultrasound is used to determine underlying causes of respiratory failure and how to set the ventilator with an emphasis on PEEP. Furthermore, we will elaborate on how to use these ultrasound modalities during the weaning phase. Recent advances for using lung ultrasound and diaphragm ultrasound to assess the effects of PEEP will be discussed.

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KEY POINTS

 Effects of positive end-expiratory pressure (PEEP) on the lungs and diaphragm can be directly evaluated at the bedside with lung- and diaphragm ultrasound making it excellent tools for diagnosis and monitoring mechanically ventilated critically ill patients.

 Lung ultrasound can accurately diagnose the cause of acute respiratory failure and differentiate between focal and nonfocal lung morphology in patients with acute respiratory distress syndrome.

 Effects of PEEP on lung recruitment can be assessed using lung ultrasound, especially in perioperative setting.

 Diaphragm dysfunction assessed with diaphragm ultrasound in patients with an acute exacerbation of chronic obstructive pulmonary disease might be a good predictor for noninvasive ventilation failure.

 Lung and diaphragm ultrasound can guide the weaning phase of mechanical ventilation and determine cause of weaning failure.

Respiratory system

EFFECTS OF POSITIVE END-EXPIRATORY PRESSURE ON LUNGS AND DIAPHRAGM Lung ultrasound is able to accurately detect and monitor acute pulmonary pathologies [7,8]. Lung ultrasound-patterns (A-, B- and C-patterns) are dependent on the fluid-to-gas ratio of the

FIGURE 1. Effects of low and high PEEP on the lungs and d changing the fluid to gas ratio, resulting in change of detected lu causes the diaphragm to be shortened, resulting in a thicker end-e indicates individual B-lines. 1: pleura, 2: diaphragm muscle, 3: p muscle. PEEP, positive end-expiratory pressure.

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pulmonary parenchyma [9]. For details about image acquisition and interpretation, we refer to a recent review [10&

]. The Bedside Lung Ultrasound in Emer- gency (BLUE) protocol is frequently used for diag- nosing pulmonary pathology in critically ill patients. This protocol, using a decision tree based on specific lung ultrasound findings, provides a diagnosis in patients with acute respiratory failure with an accuracy of around 90% [11]. To monitor effects of treatment on lung aeration, the lung aer- ation score or lung ultrasound score, a semiquanti- tative score, can be used [8]. A greater loss of aeration results in a higher lung ultrasound score: ranging from 0 to 36. Lung ultrasound is able to detect effects of PEEP on the lung, since PEEP increases end-expir- atory lung volume and therefore changes the fluid to gas ratio, resulting in change of lung ultrasound patterns and/or score (Fig. 1) [12].

Diaphragm ultrasound is an excellent bedside tool for evaluating diaphragm anatomy and func- tion [3,4&

]. For details about image acquisition and interpretation, we refer to a recent review and expert consensus [3,4

&

]. Assessment of the diaphragm includes measurement of muscle thickness, contrac- tility (thickening fraction, TFdi) and diaphragm excursion [4&

]. Muscle thickness <1.5 mm indicates atrophy [3,13]. Muscle thickness is highly depend- ent on location of measurement, gender and patient position [3,14]. A TFdi in ICU patients of <30–34% is considered abnormal [3]. Diaphragm excursion

iaphragm. PEEP increases expiratory lung volume, thereby ng ultrasound pattern (B-profile to A-profile). In addition, PEEP xpiratory muscle with potentially less efficient contractility. eritoneum. j shows thickness measurement of the diaphragm

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<2 cm during quiet breathing without assistance of mechanical ventilation is indicative of diaphragm dysfunction [4&

]. It was recently found that PEEP has a direct

effect on diaphragm geometry; it shortens the muscle creating an overlap of thick and thin fila- ments, resulting in a less optimal length for muscle contraction. PEEP can thus reduce the contractile efficiency of the diaphragm [15&

]. Moreover, pro- longed exposure to PEEP can result in remodelling of the diaphragm. Withdrawal after prolonged expo- sure can result in reduced contractile efficiency by stretching the remodelled muscle fibres in the dia- phragm [15&

]. These effects can be visualized using ultrasound; when PEEP is increased, both TFdi and excursion decrease whilst the thickness of the diaphragm increases (Fig. 1) [16&&

].

SETTING THE VENTILATOR USING LUNG AND DIAPHRAGM ULTRASOUND The most common underlying causes of acute res- piratory failure diagnosed with either lung- or dia- phragm ultrasound and subsequent choice of initial ventilator settings, with emphasis on PEEP, are sum- marized in Fig. 2 [17]. Ultrasound findings should always be used in concert with other findings and clinical features, as some ultrasound signs can be

FIGURE 2. Lung or diaphragm ultrasound findings for common c setting PEEP. ARDS, acute respiratory distress syndrome; COPD, c positive airway pressure; DE, diaphragm excursion; PEEP, positive expiratory pressure; TFdi, diaphragm thickening fraction.

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present in more than one pulmonary pathology and critically ill patients often have multiple causes for respiratory failure [5&

].

Pneumothorax Patients with pneumothorax show A-profile with- out lung sliding, called A’-profile, on lung ultra- sound. In combination with lung point, lung ultrasound confirms pneumothorax with a specific- ity of 100% [10&

]. Positive pressures including PEEP should be kept as low as possible. Resolution of the pneumothorax can be monitored using lung ultra- sound [18].

Pulmonary embolism Patients with pulmonary embolism present with A- profile. In some cases a shred sign is seen following a pulmonary infarction. For diagnosis of pulmonary embolism, lung ultrasound should be combined with venous ultrasound to detect deep-venous thrombosis.

In pulmonary embolism, PEEP is set as low as possible to prevent a further increase of right ven- tricular afterload. Cardiac ultrasound can be used to monitor effects of treatment on right ventricular function [19].

auses of respiratory failure and corresponding guidelines for hronic obstructive pulmonary disease; CPAP, continuous end-expiratory pressure; PEEPi, intrinsic positive end-

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Respiratory system

Chronic obstructive pulmonary disease and severe asthma Patients with exacerbation of chronic obstructive pulmonary disease (COPD) or severe asthma typi- cally present with an A-profile on lung ultrasound since the lung parenchyma is usually not affected [10

&

]. Noninvasive ventilation (NIV) is the first

choice of respiratory support for patients present- ing with an exacerbation of COPD. In assisted modes of ventilation, moderate external PEEP is applied to counterbalance intrinsic PEEP and hence to reduce effort needed to trigger the ventilator and to promote patient-ventilator synchrony [20]. In controlled modes of ventilation, low or some- times even zero PEEP is advised to not further increase intrinsic PEEP and prevent dynamic hyperinflation.

Severe diaphragm dysfunction within the first 48 h of NIV, defined as TFdi <20%, is associated with an increased risk of NIV failure and worse outcomes. Diaphragm dysfunction in these patients is prob- ably caused by dynamic hyperinflation. This results in less optimal diaphragm geometry causing the diaphragm to work less efficient. Improved diaphragm function under NIV is probably an indi- cation of decreased hyperinflation [21]. Two pro- spective studies have shown that diaphragm dysfunction, especially lower excursion, identified with ultrasound can reliably predict NIV failure in emergency department settings [22&

,23]. Assess- ment of diaphragm function to predict NIV failure in patients without COPD exacerbation or in an ICU setting, although promising, needs further valida- tion [24,25].

Severe asthma patients are at risk of barotrauma due to the increased flow limitations. In these patients, PEEP settings are set as low as possible to prevent further hyperinflation of the lung [20].

Cardiogenic pulmonary oedema Patients with pulmonary congestion present with multiple, diffuse bilateral B-lines (>2 per view, so called B-profile) and regular thin pleura on lung ultrasound [26&

,27]. Applying PEEP through both noninvasive and invasive ventilation can be of great benefit in the treatment of cardiogenic pulmonary oedema (CPE) [28].

Lung ultrasound can be used to evaluate the effect of PEEP by monitoring the number of- and regions with B-lines. In the prehospital emergency setting, lung ultrasound was found to be a reliable tool for monitoring effectiveness of treatment with PEEP [29,30]. Although no studies investigated lung ultrasound-guided PEEP levels, guidelines

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recommend monitoring treatment effect with bed- side lung ultrasound in the clinical setting [31]. The consequences of too high PEEP – e.g. hemodynamic compromise, should be monitored.

Pneumonia and Acute respiratory distress syndrome Patients with pneumonia can present with unilat- eral B-profile (A/B-profile), bilateral B-profile, C-pro- file and/or posterior consolidations. Moreover, presence of dynamic air bronchograms and colour Doppler flow in consolidations are highly suggestive of pneumonia [32].

Differentiation between CPE and noncardio- genic oedema can be challenging. Nonetheless, recent studies show that lung ultrasound can accu- rately differentiate between these two diagnoses [26

&

,33 &

]. Acute respiratory distress syndrome (ARDS), the most frequent cause of noncardiogenic oedema in ICU patients, is characterized by non- homogenous distribution of B-lines and/or pleural abnormalities. In patients with pneumonia and/or ARDS, ventilator settings should be set carefully to maintain sufficient gas exchange but limit ventila- tor-induced lung injury by using low tidal volumes, driving pressure and titration of PEEP [1]. The use of ultrasound to titrate PEEP in patients with pneumo- nia or ARDS is discussed in the paragraph ‘assess- ment of lung aeration’.

Diaphragm dysfunction A less common cause of acute respiratory failure is diaphragm dysfunction. Diaphragm ultrasound can diagnose both weakness and paralysis of the (hemi-)diaphragm. In these patients, PEEP is set to prevent further atelectasis. Although, titration of pressure support for adequate ventilation is more important.

In recent years, diaphragm-protective ventila- tion in addition to lung-protective ventilation has become an important field of research [34&

,35]. It has been proposed that both over- and under assis- tance of the diaphragm should be prevented. As potential target range, based on physiological data, a TFdi between 15% and 30–40% should be main- tained [13]. A recent study found that titration of inspiratory support based on patient breathing effort greatly increased the time that patients had diaphragm effort in the predefined diaphragm-pro- tective range without compromising tidal volumes and transpulmonary pressures [34&

]. However, in this study transdiaphragmatic pressure measure- ments were used for assessment of diaphragm effort.

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ASSESSMENT OF LUNG AERATION

Acute respiratory distress syndrome lung morphology Two distinct ARDS phenotypes, focal and nonfocal, have been identified [36]. Focal ARDS is considered to respond to low PEEP and prone positioning whereas nonfocal ARDS, with patchy loss of aera- tion, generally responds to high PEEP and recruit- ment manoeuvres [36]. The largest study to date where individualisation of ventilator strategy based on these phenotypes was researched mostly used chest radiography for identification of the pheno- types with a great degree of misclassification [37]. A reduction in mortality was found after correcting for misclassification. Lung ultrasound can accurately identify these phenotypes with the Amsterdam method being the advised method (Fig. 3) [38&&

]. Using lung ultrasound to identify these phenotypes and guide ventilator strategy accordingly is cur- rently being investigated (ClinicalTrials.gov; identi- fier NCT05492344).

FIGURE 3. The Amsterdam method for lung ultrasound assessment to differentiate between focal and nonfocal lung morphology in patients with acute respiratory distress syndrome. Adapted from Pierrakos et al. (2021).

Ultrasound-guided recruitment In patients with pneumonia and/or ARDS, PEEP is mostly used to preserve lung aeration. To set PEEP in these patients recruitability should be assessed to help identify patients who are likely to benefit from higher PEEP levels (Fig. 4). Studies researching the effects of PEEP on lung recruitment assessed by lung ultrasound have found conflicting results [39,40,41

&&

]. While one study found that lung ultra- sound was able to accurately assess reaeration and identify differences in lung ultrasound scores at different PEEP levels [41&&

], other studies found that lung ultrasound was unable to consistently detect these changes when PEEP levels were changed [39,40]. These different outcomes might be explained by the fact that changes in consolidation size or a decrease in the number of B-lines are not taken into account. Thus smaller PEEP-induced aer- ation changes are not always detected. A small pilot study found that by taking these smaller changes into account it was possible to accurately assess aeration changes [42].

An important limitation of lung ultrasound is its inability to directly asses overdistention. However, there are some promising experimental studies eval- uating the potential of lung ultrasound for detecting overdistension such as quantification of lung sliding [43,44] and ultrasound elastography [45].

Although diaphragm ultrasound is not com- monly used for assessing lung aeration, a small study in patients with ARDS investigated diaphragm ultra- sound for assessing aeration [46]. They found an

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increase in diaphragm excursion in the dorsal region after an increase of PEEP. This suggests an increase in lung volume due to increased aeration after recruit- ment manoeuvres. Interestingly, they did not find a relation between increase in PEEP and diaphragm excursion in ventral regions. Since overdistension of the lungs is usually present in the ventral regions during mechanical ventilation, one can hypothesize that a lack of excursion in the ventral regions might be suggestive of overdistension. This needs further studies.

In the perioperative setting, the use of lung ultrasound to set PEEP has been extensively studied. The majority of patients undergoing general anaes- thesia develop atelectasis, which is associated with worse postoperative outcomes. Therefore, decreas- ing loss of aeration seems a logical target for improv- ing postoperative outcomes [47]. Lung ultrasound accurately detects reaeration of lung tissue after

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FIGURE 4. Effect of PEEP on reaeration of the lung. Increase of PEEP can result in recruitment of lung tissue which can be seen on lung ultrasound as a smaller consolidation when PEEP is increased from PEEP 5 (left) to PEEP 15 (right). The lines indicate the border of the consolidations. PEEP, positive end-expiratory pressure.

Respiratory system

application of PEEP during surgery [47]. Lung ultra- sound-guided recruitment and PEEP titration – i.e. recruitment manoeuvres when lung ultrasound detected atelectasis at prespecified time points - improved aeration and oxygenation intraopera- tively, but did not result in reduced pulmonary complications [48&&

,49].

THE ROLE OF LUNG AND DIAPHRAGM ULTRASOUND DURING WEANING Identifying patients who are ready to be weaned of mechanical ventilation is often challenging. Both delayed weaning and weaning failure are associated with high mortality. Therefore correct identification of patients ready to be weaned is vital [50]. Lung and diaphragm ultrasound is useful in in this context.

Role of lung ultrasound A decrease or removal of PEEP can result in dere- cruitment which can be detected with lung ultra- sound. After a spontaneous breathing trial (SBT), a lung ultrasound score of <13 is highly predictive of extubation success with a negative likelihood ratio of 0.20, whereas a score of >17 is highly predictive of failure with a positive likelihood ratio of 11.8 [51].

A decrease in intrathoracic pressure during weaning due to decreased PEEP can induce weaning induced pulmonary oedema (WIPO). This can be

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detected by lung ultrasound as development of B- lines. Patients with an increase of 6 B-lines, in four anterior regions, during a SBT showed a high risk of SBT failure with a sensitivity of 88% and specificity of 91% [52].

Role of diaphragm ultrasound Diaphragm dysfunction is an important complica- tion of mechanical ventilation and is associated with poor clinical outcomes, including weaning failure [13]. Diaphragm excursion of >1–1.5 cm (sensitivity 85%, specificity 75%) and a TFdi of 30–36% (sensitivity 80%, specificity 80%) are pre- dictive of successful extubation [3,53

&

,54]. In patients after a successful SBT, diaphragm dysfunc- tion detected by ultrasound, was not associated with an increased risk of weaning failure [55]. This indi- cates that a single ultrasound measurement should not be used to base clinical decisions on.

Holistic approach Weaning is a stress test of the whole cardiorespir- atory system. A more holistic ultrasound assessment of the heart, lung and diaphragm might therefore be more suitable to assess if the patient is ready to wean [3]. Thoracic ultrasound assessment, including heart, lung and diaphragm ultrasound, especially the presence of pulmonary oedema and increased

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left ventricle pressures are good measures (positive likelihood ratio of 22.9 and negative likelihood ratio of 0.16 when ultrasound examination is performed prior to a SBT) for predicting weaning failure [56]. Furthermore, this assessment was able to identify the cause of weaning failure in all patients [56]. However, in patients who successfully passed a SBT, thoracic ultrasound seemed to have less rele- vance for prediction of respiratory distress after extubation [57]. In summary, it is advised to use an ultrasound assessment of all components of this cardiorespiratory system to detect the cause of weaning failure and guide treatment [3].

CONCLUSION Lung ultrasound and diaphragm ultrasound are excellent tools for diagnosing the cause of acute respiratory failure, including lung morphology in ARDS patients. Thereby it can guide and monitor ventilator settings including PEEP. Ultrasound is able to detect PEEP induced changes on the lungs and diaphragm. Using lung ultrasound to assess recruitability and set PEEP in critically ill patients needs further validation, but is useful periopera- tively. In patients with acute exacerbation of COPD, diaphragm ultrasound allows for prediction of NIV failure. During weaning of mechanical ven- tilation combined ultrasound of lung, diaphragm and heart could potentially be used to help predict weaning failure and to determine the cause of wean- ing failure.

Acknowledgements

We thank M. Otten for his contribution to the figures in this article.

Financial support and sponsorship

None.

Conflicts of interest

There are no conflicts of interest.

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Volume 30  Number 1  February 2024