Electrical impedance tomography imaging of the cardiopulmonary system.

REVIEW URRENT C OPINION

Electrical impedance tomography imaging of the cardiopulmonary system Ine´z Frerichs, Tobias Becher, and Norbert Weiler

Purpose of review This review article summarizes the recent advances in electrical impedance tomography (EIT) related to cardiopulmonary imaging and monitoring on the background of the 30-year development of this technology. Recent findings EIT is expected to become a bedside tool for monitoring and guiding ventilator therapy. In this context, several studies applied EIT to determine spatial ventilation distribution during different ventilation modes and settings. EIT was increasingly combined with other signals, such as airway pressure, enabling the assessment of regional respiratory system mechanics. EIT was for the first time used prospectively to define ventilator settings in an experimental and a clinical study. Increased neonatal and paediatric use of EIT was noted. Only few studies focused on cardiac function and lung perfusion. Advanced radiological imaging techniques were applied to assess EIT performance in detecting regional lung ventilation. New approaches to improve the quality of thoracic EIT images were proposed. Summary EIT is not routinely used in a clinical setting, but the interest in EIT is evident. The major task for EIT research is to provide the clinicians with guidelines how to conduct, analyse and interpret EIT examinations and combine them with other medical techniques so as to meaningfully impact the clinical decision-making. Keywords bioimpedance, electrical impedance tomography, imaging technique, mechanical ventilation, regional ventilation

INTRODUCTION Electrical impedance tomography (EIT) has been proposed as a future real-time bedside tool for monitoring regional lung function, potentially also enabling the assessment of cardiac action and lung perfusion. The advances in EIT research achieved over the past more than 30 years resulted in the development of commercially available devices, but the technology is not yet broadly used in a routine clinical setting. Several advantageous features of EIT such as its noninvasiveness, radiation-free measuring principle, no known risk associated with its use, portability and excellent time resolution allowing the examination of highly dynamic physiological and pathological lung processes render this technology interesting for medical care providers, especially those involved in the care of critically ill patients. EIT imaging is relevant for patients of all age groups, but neonatal and paediatric patients might especially benefit from the use of this technique because of the limited availability of other imaging modalities

and the reluctance to expose infants and children to radiation. EIT research has intensified over the past years. Several research groups have been involved in fields such as the technological progress of EIT hardware, development of new EIT image reconstruction procedures and EIT data analysis concepts, validation, experimental and clinical EIT studies. The number of publications dedicated to EIT lung imaging is continuously increasing (Fig. 1). The clinical awareness of EIT, which was almost nonexistent till the

Department of Anesthesiology and Intensive Care Medicine, University Medical Center, Schleswig-Holstein, Campus Kiel, Kiel, Germany Correspondence to Dr Ine´z Frerichs, Department of Anesthesiology and Intensive Care Medicine, University Medical Center, Schleswig-Holstein, Campus Kiel, Arnold-Heller-Str. 3, D-24105 Kiel, Germany. Tel: +49 431 597 2991; fax: +49 431 597 3002; e-mail: [email protected] Curr Opin Crit Care 2014, 20:323–332 DOI:10.1097/MCC.0000000000000088

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Cardiopulmonary monitoring

KEY POINTS Significant progress was noted in EIT research regarding the detection of regional tidal volumes, changes in end-expiratory volumes and respiratory system mechanics. Small progress was found in EIT use for stroke volume and lung perfusion assessment. Several approaches improving the thoracic EIT image quality were introduced. Standardized examination protocols, findings and interpretations in combination with other medical diagnostic tools need to be defined for EIT to become an established and useful method in a clinical setting.

end of the last century, significantly improved over the last 10 years. This is documented by the increasing number of EIT articles published in clinical journals (Fig. 1). With a total of 102 articles (26.7% of all articles), the journal Physiological Measurement remains the major source of scientific EIT information, mainly because of the annually published focus issues on EIT. A large proportion of the overall number of peer-reviewed articles (13.4%) is represented by reviews (Fig. 2). This helped increasing the level of clinical interest in EIT. However, the growing interest in EIT is also associated with rising expectations. As pointed out by a group of opinion leaders on pulmonary EIT imaging in a position paper published in 2012, lung EIT is at a ‘time of transition’ [1]. A pathway by which EIT may become an established medical 60

examination tool was outlined there. The current time bears risks and opportunities. The main risk is that the enthusiasm for EIT dissipates, the main opportunity is the establishment of EIT in the most promising field of its use: for monitoring and guidance of mechanical ventilation aiming at achieving least injurious settings while securing adequate gas exchange. Several of the recent EIT publications reviewed in our article represent important advances that might help realize this opportunity. However, we also address a few studies with different foci. According to the guidelines of Current Opinion in Critical Care, we only reviewed original articles published during the past 18 months (between 1 July 2012 and 31 December 2013). We refer to the most interesting clinical, experimental and theoretical studies but would like to explicitly acknowledge the work of all authors of recent EIT articles. We do not address articles in press. Review articles and a few older publications are only referred to when they are relevant in the overall context. In the subsequent text, we present the core results of recent lung EIT research in a few sections with the headings and subheadings pointing at the main foci of these studies. The assignment of the reviewed studies to individual sections should not imply that they are not relevant in other fields as well.

MONITORING AND GUIDANCE OF MECHANICAL VENTILATION The monitoring of regional effects of mechanical ventilation aims at characterizing the spatial and

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temporal distribution of tidal volumes (VT) and the changes in regional intrathoracic gas volumes, typically the end-expiratory lung volumes (EELVs). A promising field is the assessment of regional respiratory system mechanics. This EIT-derived information is used to identify phenomena such as regional lung overdistension, recruitment and derecruitment or tidal recruitment. The detection of these phenomena by EIT is crucial in its postulated use to guide lung-protective ventilator therapy.

whole chest in the anteroposterior orientation (e.g. ventral and dorsal image halves or four layers of identical height). This is meaningful in supine patients because gravity-dependent ventilation changes can be assessed. Nonetheless, such ROIs contain a large proportion of nonpulmonary tissue. More lung-specific ROIs would be desirable [10]; however, such ROIs can easily be determined only under experimental conditions, in which baseline conditions in the normal lung can be used for ROI definition before lung disease is artificially induced [11 ]. This situation does not often occur in patients who already have diseased and heterogeneously affected lungs. Still, the selection of such lungspecific ROIs can be attempted even in patients [12]. Lung ROIs and the definition of smaller ROIs within them are needed for spatial analysis of lung function heterogeneity. The importance of this issue is evidenced by, for example, a study on automated identification of lung boundaries [13]. &&

Ventilation distribution Already in the nineties of the last century, it was realized that EIT is capable of detecting the effect of ventilator mode (controlled or assisted) on the ventilation distribution in the chest [2]. The redistribution of ventilation resulting from changes in positive end-expiratory pressure (PEEP), VT or spontaneous breaths was described [3,4]. Recent studies applied EIT to analyse the ventilation distribution during new or less commonly used modes such as noisy pressure support ventilation [5,6], high-frequency oscillatory ventilation [7 ] or neurally adjusted ventilatory assist [8]. Two studies investigated how the degree of pressure support applied during pressure-support ventilation affected the distribution of VT between the dependent and nondependent regions in patients with acute respiratory distress syndrome (ARDS) [8,9]. EIT identified higher ventilation in the dependent regions with decreasing pressure support in both study populations. The majority of the studies used simple and rather gross regions of interest (ROI) spanning the &

Distribution of end-expiratory lung volume Detection of regional rise or fall in EELV by EIT is an important feature because it may imply regional lung recruitment or derecruitment, respectively. Regional reduction in EELV induced by acute lung injury and its reversal by increased PEEP was found in experimental animals [14 ]. Application of high gas flows through a nasal cannula in healthy individuals lying in supine and prone positions revealed a more uniform increase in EELV in the prone position [15]. Two studies analysed the effect of closed endotracheal tube suctioning: The degree


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of EELV fall and its dependence on the suctioning mechanism, suction catheter size and the EELV recovery induced by sighs was followed by EIT in rabbits [16]. Postsuction recruitment was only needed when large catheters were used. Closed and open endotracheal suctionings were compared in patients after cardiac surgery: although closed suctioning induced a smaller fall in EELV, surprisingly, its long-term recovery was slower than after open suctioning [17].

Regional respiratory system mechanics Information derived from EIT examinations can be enhanced when other signals are registered in parallel. Several studies utilized this approach. By parallel sampling of airway pressures (and other ventilator data such as VT, gas flow and so on) and EIT, during either specific ventilation manoeuvres [11 ,18 ,19 ] or continuous mechanical ventilation [14 ,20 ], different measures of respiratory system mechanics could be determined. These measures were applied to identify the deleterious pulmonary processes of tidal recruitment and overdistension. Development of atelectasis or alveolar recruitment was also detected. Quasi-static inflation and deflation pressurevolume manoeuvres were performed in animals with normal and injured lungs, as well as after surfactant administration [11 ]. Several landmark points could be identified on regional pressurevolume curves derived from the acquired EIT data. Changes in regional respiratory system mechanics induced by injury and surfactant treatment were detected by EIT as shown in Fig. 3. Regional inflation pressure-volume curves were generated using EIT in another experimental study as well. Analysis of regional static compliance of the respiratory system (Crs) was performed in a dependent and nondependent ROI in the chest cross-section [21]. A recruitment manoeuvre with PEEP increments of 5 cmH2O applied for 1 min during each step was performed in an animal model of acute lung injury and regional dynamic Crs analysed in four horizontal ROIs within the lung regions [19 ]. The concurrent decrease and increase in Crs in the nondependent and dependent regions, respectively, revealed the simultaneous occurrence of overdistension and atelectasis reversal. An incremental and decremental PEEP trial, with the same pressure steps as previously used [22], was performed during EIT scanning before and after induction of acute lung injury [23]. This study confirmed that the ‘best’ PEEP, rendering the most homogeneous ventilation distribution, was identified on the decremental limb of the manoeuvre. Analysis of intratidal gas &&

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distribution using EIT identified the onset of regional overdistension. A stepwise increase in airway pressure starting at three different PEEP values and its subsequent stepwise decrease to the same PEEP was applied in patients with healthy lungs and patients with ARDS [18 ]. The sizes of the fast and slow filling and emptying compartments were analysed. Regional respiratory time constants were determined in the dependent and nondependent lung regions and significant differences between the patients with normal lungs and ARDS were found. A relatively simple but efficient approach using short-term variation of VT (6 and 10 ml/kg body weight) applied at three PEEP values was applied in patients with ARDS to identify regional tidal recruitment and lung overdistention [14 ]. Regional dynamic Crs was calculated from the EIT data and global Crs. The change in Crs, resulting from the VT variation, was determined in 32 anteroposterior ROIs. Figure 4 shows an example of this type of EIT data analysis in a patient with ARDS. This evaluation procedure was developed in an animal model described in the same article. &

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Prospective use of electrical impedance tomography to define ventilator settings For many years, EIT data were only analysed offline, mainly because of the limitations of the technology and analysis tools. Two recent studies, one experimental [20 ] and one clinical [24 ], used the results of thoracic EIT scanning for the first time prospectively. This is a major step in EIT development. An EIT-based protocol for guidance of mechanical ventilation was compared with ventilation conducted in accordance with the ARDSNet guidelines in experimental animals with acute lung injury [20 ]. The EIT protocol aimed at reversing the atelectasis in the most dependent region by increasing PEEP, until no further rise in regional Crs was identified. Overdistension in the most nondependent region was subsequently miminized by reducing PEEP in small decrements until regional Crs in the most dependent region started to fall. Extensive reference data were obtained in this study by computed tomography, serum and broncholaveolar lavage sampling, blood gas and histological analyses. Animals with EIT-guided ventilation exhibited better respiratory system mechanics, improved gas exchange and reduced lung tissue damage. Ventilation distribution was analysed in a group of mechanically ventilated preterm infants prior to extubation and initiation of nasal continuous positive airway pressure [24 ]. The ratio between the ventilation in the dependent and &&

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FIGURE 3. Regional electrical impedance tomography waveforms in the right ventral (RV) lung region of interest (ROI) acquired in a newborn piglet during baseline conditions in the normal lung (NL), after repeated bronchoalveolar lavage in the injured lung (IL) and after administration of surfactant in the treated lung (TL). The left-hand and middle diagrams show the plots of relative impedance change (rel. DZ) as a function of time and airway pressure during a quasi-static pressure-volume manoeuvre as well as during two tidal breaths preceding and following the manoeuvre. The data registered before and after the peak inflation are plotted in light and dark grey, respectively. The right-hand diagrams present the original and fitted curves obtained during the manoeuvre in thin and bold lines, respectively. The calculated pressures at the lower (Plmcc) and upper points of maximum compliance change (Pumcc) as well as the pressures at the curve inflection (Pinfl) are indicated. The letters i and d denote the inflation and deflation values, respectively. Functional EIT image (top left) shows the distribution of regional ventilation during baseline conditions and the superimposed ROIs with the RV ROI highlighted. Conventional radiological image orientation with posterior at the bottom and with the right body side on the left side of the image is used. LD, left dorsal; LM, left middle; LV, left ventral; RD, right dorsal; RM, right middle. Reproduced with permission [11 ]. &&



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FIGURE 4. Electrical impedance tomography examination of a 70-year-old patient suffering from moderate acute respiratory distress syndrome. The patient was studied in the supine posture during volume-controlled continuous positive pressure ventilation at three levels of positive end-expiratory pressures (PEEP). PEEP was set either below or above the pressure at the lower inflection point (LIP) of the quasi-static pressure-volume curve determined from a low-flow inflation manoeuvre performed before the EIT examination. At the two lower values of PEEP, EIT scanning was performed during ventilation with tidal volumes (VT) of 6 and 10 ml/kg body weight (BW), at the highest PEEP, with 6 and 8 ml/kg BW. Functional EIT images show the distribution of VT at each setting. The global values of dynamic respiratory system compliance (Crs) measured at each setting are given below the images. The bar charts show the changes in regional Crs resulting from the increase in VT at each PEEP value. (Dark bars indicate a decrease and light bars an increase in regional Crs.) Thirty-two regions of interest spanning the whole anterior (a) to posterior ( p) chest dimension are shown. The upper graph reveals pronounced tidal recruitment at the lowest PEEP that was reduced at the higher and abolished at the highest PEEP. Higher VT increased overdistension in the anterior regions at the two lower PEEP values, as can be implied from the locally reduced Crs, and in almost all regions at the highest PEEP.

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nondependent lung regions was calculated during four briefly applied decremental values of PEEP. The ratio value of 1 was arbitrarily defined as the sign of best ventilation homogeneity. The PEEP value at which the ratio was nearest to 1 was then used to set the pressure support after extubation. The authors concluded that the EIT-derived level of pressure support was higher than the usual, routinely applied pressure and that it resulted in improved lung compliance.

Neonatal and paediatric use of electrical impedance tomography Recent EIT research with the focus on neonatal and paediatric patients has produced several important results. This is remarkable because the availability of EIT technology for use, especially in low-body weight infants such as preterm neonates, is limited. The major research fields were assessment of the effects of endotracheal suctioning [16,17], monitoring of regional effects of different modes of mechanical ventilation and manoeuvres (e.g. recruitment manoeuvres) [7 ,24 ,25], assessment of the changes in lung function after surfactant treatment, identification of endotracheal tube position and examination of physiological distribution of lung ventilation in healthy infants. (The first two points were already partly addressed in the previous sections.) In contrast to adult patients, high-frequency oscillatory ventilation is often used in infants. Because of its high scan rates, EIT can measure the distribution of oscillatory volumes even when the oscillations are applied at 10 Hz [7 ] and thus provide information otherwise not accessible. It has been postulated early that EIT might be of benefit in monitoring the regional changes in lung aeration and ventilation after surfactant treatment with the first case reports published many years ago [26,27]. Finally, the first prospective study on a group of infants treated with surfactant was published [28 ]. EIT not only identified the expected increase in aeration but also the reduced right-to-left asymmetry and increased ventilation of the dependent regions after surfactant. In an experimental study, improved regional Crs was found after surfactant instillation [11 ]. The ability of EIT to determine the position of the endotracheal tube, based on the evaluation of ventilation distribution between the right and left lungs, was tested in one experimental and one clinical study [29]. The design of these studies was similar: the tube was placed either correctly in the trachea or in the main bronchus. EIT identified the dissimilar ventilation distribution patterns between these two states. Incorrect placement of the tube in &

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the oesophagus was also detected by the lack of ventilation-related EIT waveforms in the lung regions. Because EIT does not require the use of ionizing radiation, it can be applied to study unknown physiological aspects of lung ventilation in otherwise healthy children [30]. Recent studies advanced our knowledge on the ventilation distribution in preterm neonates [31,32].

ASSESSMENT OF CARDIAC ACTION AND LUNG PERFUSION Surprisingly, few studies were performed with the aim of studying the capacity of EIT to track lung perfusion, although this might decisively increase the clinical relevance of EIT by the possibility to assess regional ventilation-perfusion ratios. A short article investigated different solutions that might be used as contrast agents to determine regional indicator dilution curves [33], an approach that has previously been validated in two studies [34,35]. Children with ventricular septum defect and pronounced left-toright shunt were studied before and after corrective heart surgery and EIT detected the redistribution of lung perfusion after surgery [36]. A theoretical study [37] on a computerized chest model was published in which the ability of EIT to estimate cardiac stroke volume was tested. Because the heartbeat-related variation of electrical impedance is small and difficult to measure, another theoretical study investigated the usefulness of an internal electrode placement [38].

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ELECTRICAL IMPEDANCE TOMOGRAPHY VALIDATION The ability of EIT to detect regional lung volume changes has already been validated with different reference techniques [39–42]. Recent studies used sophisticated radiological techniques such as xenon multidetector-row computed tomography [43] and hyperpolarized helium MRI [44] in animals and confirmed that EIT was able to identify correctly changes in regional ventilation resulting from acute sublobar injury or postural changes, respectively. Another two studies were conducted in healthy volunteers. Defined changes in regional ventilation were induced by exposure to weightlessness and hypergravity [45] or modulation of resting lung volume and VT combined with postural changes [46] and examined by EIT. Both studies concluded that EIT properly detected the known physiological changes in regional ventilation and confirmed previous findings obtained with similar study goals [47,48].



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The effect of blood withdrawal and fluid volume administration on EIT ventilation data, a setting frequently encountered in patients after bleeding or fluid therapy, was analysed in an animal model [49]. A highly relevant aspect of EIT lung imaging was addressed in another study: the impact of the scan rate on the quantitative estimates of lung ventilation by EIT [50 ]. Most EIT systems use serial data acquisition, which means that the data needed to reconstruct EIT images are not collected at exactly the same time. Using neonate and adult data, the authors showed that this time lag affected the image quality and subsequent analysis. &&

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to expire a predefined percentage of volume [58 ] may be used to characterize the temporal heterogeneity of lung function. The ratios of regional air flows at predefined time points may detect airway obstruction [60]. Thanks to the high rate of EIT scanning, a small temporary decline of electrical impedance was detected in the nondependent region of the chest in a patient at the onset of spontaneous inspirations that disappeared during controlled mechanical ventilation [61]. The occurrence of this phenomenon was confirmed in a subsequent experimental study and attributed to regional pendelluft.

CONCLUSION

QUALITY OF ELECTRICAL IMPEDANCE TOMOGRAPHY IMAGES A significant proportion of recent EIT research was dedicated to the improvement of thoracic EIT image quality. The effect of breathing motion on the intrathoracic organ and electrode positions was followed in spontaneously breathing patients [51]. The knowledge of the motion pattern might improve the EIT image reconstruction, which at present is often performed with the assumption of a rigid chest. Another invalid assumption is the uniform electrical conductivity background of the chest. It was demonstrated that this makes the EIT images less accurate and that interpretation of images in heterogeneous lung diseases must be cautious [52 ]. The authors propose implementation of anatomically correct forward models in image reconstruction, a procedure studied in another study as well [53]. Taking the shape of the chest and its deformation into account was also found to improve the image quality [54–56]. Finally, an approach how the smooth edges of organs depicted in thoracic EIT images could be sharpened was proposed [57]. &

NEW PATIENTS, NEW ANALYSES, NEW PHENOMENA So far, EIT has been mainly used in patients suffering from infant or adult respiratory distress syndrome. Three recently published studies examined patients with obstructive lung diseases. Chronic obstructive pulmonary disease was found to be associated with pronounced spatial heterogeneity of ventilation [58 ]. The ability of EIT to differentiate among patients and healthy young and elderly individuals even during tidal breathing was demonstrated. The heterogeneity of lung function was also identified by EIT in patients with cystic fibrosis [59,60]. In these studies, novel types of EIT data analysis were introduced that may be relevant in other applications as well. Histograms of regional times needed

Several high-quality articles on EIT use for cardiopulmonary imaging have recently been published. This may promote the acceptance of EIT and increase the probability of its routine clinical use. Nonetheless, it must be acknowledged that a number of important issues have not been sufficiently studied yet. Issues such as the definition of standardized examination procedures and EIT measures most relevant for clinical decision-making, lacking experience with long-term patient monitoring, limited number of (especially larger) clinical trials need to be addressed in the future. At the same time, further technological progress is obligatory, as it may increase the robustness and applicability of EIT. A balanced, interdisciplinary research might be of benefit. Acknowledgements We acknowledge the funding provided by the European Union’s Seventh Framework Programme for R&D (WELCOME project, Grant No. 611223). Conflicts of interest I.F. has received reimbursement of travel costs, meeting expenses and speaking fees from CareFusion, Swisstom and Dra¨ger Medical, respectively. T.B. has received reimbursement of travel costs and meeting expenses from Dra¨ger Medical and Astellas Pharma. N.W. has received reimbursement of travel costs, meeting expenses and speaking fees from Dra¨ger Medical and Fresenius.

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