Slow moderate pressure recruitment maneuver minimizes negative circulatory and lung mechanic side effects: evaluation of recruitment maneuvers using electric impedance tomography
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To evaluate the efficacy of different lung recruitment maneuvers using electric impedance tomography.
Design and setting
Experimental study in animal model of acute lung injury in an animal research laboratory.
Fourteen pigs with saline lavage induced lung injury.
Lung volume, regional ventilation distribution, gas exchange, and hemodynamics were monitored during three different recruitment procedures: (a) vital capacity maneuver to an inspiratory pressure of 40 cmH2O (ViCM), (b) pressure-controlled recruitment maneuver with peak pressure 40 and PEEP 20 cmH2O, both maneuvers repeated three times for 30 s (PCRM), and (c) a slow recruitment with PEEP elevation to 15 cmH2O with end inspiratory pauses for 7 s twice per minute over 15 min (SLRM).
Measurements and results
Improvement in lung volume, compliance, and gas exchange were similar in all three procedures 15 min after recruitment. Ventilation in dorsal regions of the lungs increased by 60% as a result of increased regional compliance. During PCRM compliance decreased by 50% in the ventral region. Cardiac output decreased by 63±4% during ViCM, 44±2% during PCRM, and 21±3% during SLRM.
In a lavage model of acute lung injury alveolar recruitment can be achieved with a slow lower pressure recruitment maneuver with less circulatory depression and negative lung mechanic side effects than with higher pressure recruitment maneuvers. With electric impedance tomography it was possible to monitor lung volume changes continuously.
KeywordsLung recruitment End-expiratory lung volume Acute lung injury Bronchoalveolar lavage Electric impedance tomography
Lung recruitment maneuvers (RMs) are used to open up atelectasis and counteract alveolar derecruitment due to low tidal volume (TV) ventilation. Classically, rapid high-pressure RMs applied for up to 60 s have been used [1, 2, 3, 4]. However, these RMs may be associated with serious circulatory side effects [3, 5, 6], risk of baro-/volutrauma , and even worsening of oxygenation [8, 9]. It is possible that lung volume (LV) expansion can be achieved with less traumatic methods, i.e., less pressure maintained over a longer period [10, 11]. Several techniques have been used to monitor global lung expansion, including methods based on dilution of tracer gases such as helium , nitrogen , and sulfur hexafluoride . Computed tomography (CT) is a useful technique for assessing regional aeration and alveolar recruitment . Still, these techniques are intermittent and we lack a bedside tool for dynamic monitoring of lung ventilation disturbances.
Electric impedance tomography (EIT) is a technique based on the injection of small currents and voltage measurements using electrodes on the skin surface generating a cross-sectional image representing impedance changes in a slice of the thorax . A high temporal resolution makes dynamic monitoring of ventilation induced LV changes possible. The anatomical resolution is less precise than that of CT but still allows for radiation-free differentiation of regional lung ventilation disturbances [17, 18, 19].
In this study we measured changes in LV and regional distribution of ventilation using EIT to evaluate whether an RM with lower pressure performed over 15 min is as effective as three repeated 30-s high-pressure RMs performed as three sustained inflations or pressure-controlled maneuvers. The study was performed in an animal model of acute lung injury (ALI) achieved by repeated bronchoalveolar lavage.
Material and methods
The study was approved by the Committee for Ethical Review of Animal Experiments in Gothenburg, Sweden, and performed in accordance with National Institutes of Health guidelines. Fourteen pigs (25–30 kg) were included.
Animals were premedicated using 15 mg/kg ketamine (Ketalar, Park-Davis, Sweden) and 0.3 mg/kg midazolam (Dormicum, Roche, Switzerland) intramuscularly. General anesthesia was induced with 6 mg/kg pentobarbital sodium (Apoteksbolaget, Sweden) followed by hourly infusions of 4 mg/kg and 25 µg/kg fentanyl (Fentanyl Pharmalink, Pharmalink, Sweden). Muscle relaxation was achieved by 0.15 mg/kg pancuronium (Pavulon, Organon, Sweden) as a bolus followed by 0.3 mg/kg per hour. The pigs were tracheotomized with an 8-mm endotracheal tube. Mechanical ventilation was performed using a Servo 300 ventilator (Siemens-Elema, Sweden), volume-controlled mode (VCV), TV 10 ml/kg, and inspiratory oxygen fraction of 0.5. Normovolemia was maintained by hourly infusion of 10 ml/kg Ringer’s solution with 2.5% glucose. Prior to recruitment the animals were volume expanded using 8 ml/kg colloid infusion (Voluven, Fresenius Kabi, Sweden). The study was performed with animals in supine position. After the protocol the animals were killed during deepened anesthesia.
Arterial and central venous lines were surgically placed and a pulmonary artery catheter (CCOmbo/SVO2, Edwards Life Sciences, Calif., USA) inserted via the right internal jugular vein. We recorded data on heart rate, mean arterial pressure, central venous pressure, mean pulmonary artery pressure, and mixed venous oxygen saturation. Cardiac output was measured using bolus thermodilution technique. During the RMs measurements were performed as single boluses at the end of each 30-s period. Arterial oxygen (PaO2), carbon dioxide (PaCO2) pressure, and pH were monitored by a Trend CareMonitor 6000 sensor (Diametrics Medical, UK) inserted through a femoral artery catheter. Oxygen saturation was recorded using a pulsoximeter. Respiratory rate, volumes, and pressures were measured using side stream spirometry. Tracheal pressure (Ptrach) was measured at the tip of the endotracheal tube . Inspiratory and expiratory fractions of oxygen and carbon dioxide were determined by paramagnetic and infrared technology (AS/3, Datex-Ohmeda, Finland). A modified technique for nitrogen washout/washin was used to measure end-expiratory LV (EELVN2) .
Electric impedance tomography
After preparation repeated bronchoalveolar lavages with body warm saline (30 ml/kg) were performed [24, 25] with PEEP 10 cmH2O and FIO2 1.0. The procedure was continued until PaO2 was less than 26 kPa at FIO2 1.0 when PEEP was lowered to 5 cmH2O. Total amount saline ranged from 9 to 12 l. The animals were allowed to stabilize for 1 h at FIO2 0.5.
Recruitment maneuver procedures
Basal ventilation (BV) during the recruitment protocol was VCV, 10 ml/kg, RR 20/min, inspiratory to expiratory ratio (I:E) 1:2, and FIO2 0.5. Before each RM derecruitment was achieved by applying zero end-expiratory pressure, resulting in a decrease in PaO2 to below 13 kPa. RMs then started from BV with PEEP 5 cmH2O. During recovery periods within and 15 min after recruitment procedures PEEP was 10 cmH2O.
ViCM: a vital capacity maneuver in which a pressure of 40 cmH2O was applied for 30 s repeated three times with a recovery period of 30 s (BV, PEEP 10) between maneuvers
PCRM: a high-level pressure control maneuver in which the ventilator was set at PEEP 20 cmH2O, peak pressure 20 cmH2O above PEEP, I:E ratio 1:1, and RR 20/min was applied for 30 s and repeated three times with a recovery period of 30 s (BV, PEEP 10) between maneuvers
SLRM: a slow lower pressure maneuver performed for 15 min in VCV, TV 10 ml/kg, I:E 1:2, RR 20/min, PEEP 15 cmH2O and prolonged end-inspiratory pauses for 7 s twice per minute
Calculations and statistics
Respiratory, hemodynamic, and shunt calculations were made using standard formulae. Total respiratory compliance was calculated as the TV divided by the difference between end-inspiratory and end-expiratory tracheal pressure (ΔPtrach). From the EIT image four regions of interest (ROI)—ventral, midventral, middorsal, and dorsal—were chosen. The regional TV values (TVROI) were calculated as: TVROI=(ΔZROI/ΔZGLOB) x TV, where ΔZROI is the regional impedance change for a ROI and ΔZGLOB is the sum of the impedance changes in all ROIs (=global impedance changes). Regional compliance was obtained by dividing TVROI by ΔPtrach, assuming no flow at end inspiration and expiration.
Values are presented as mean ±SEM. Analysis of variance for repeated measures was performed, followed by Fisher’s protected least significant difference test. The paired t test was used to evaluate changes between measuring points and differences between maneuvers. Bonferroni’s correction for multiple comparisons was performed. A p value less than 0.05 was considered statistically significant.
Effect of recruitment procedures
Regional ventilation distribution
This study using EIT to evaluate the effect of two rapid high-pressure maneuvers (ViCM and PCRM) and one slow with lower pressure (SLRM). Improvement in LV, compliance, and gas exchange 15 min after recruitment was observed with all RMs, but circulatory depression during recruitment was significantly less using SLRM. During PCRM, in contrast to SLRM, there were signs of overdistention in ventral parts of the lung. Successful recruitment was associated with an increase in compliance in middle and dorsal regions and a redistribution of ventilation towards dependent lung areas. This study also indicates the potential usefulness of the EIT for monitoring of LV changes.
Depending on the cause of the lung injury various responses to ventilatory interventions can be expected [26, 27, 28]. The lavage model used in this study is characterized by surfactant depletion, atelectasis formation, increased extravascular lung water, and decreased compliance and is considered a stable experimental model of early acute respiratory distress syndrome (ARDS) [24, 25, 29]. However, RMs, PEEP and high TV have been shown to recruit collapsed lung areas and maintain LV more easily in lavage-induced ALI, in contrast to oleic acid and pneumonia-induced models [26, 27]. Therefore our results cannot be directly extrapolated to other experimental models or clinical situations primarily involving pulmonary edema or inflammation with secondary surfactant dysfunction.
Another limitation of this study is that LV changes and regional ventilation were assessed by analyzing lung impedance changes in only one slice (5–10 cm thick). The correlation of impedance changes with known LV changes using a super syringe allows the use of impedance changes in one slice during recruitment procedures even though the lungs may move during RMs. Concerning data obtained on regional ventilation and volumes conclusions can only be drawn on the slice measured, especially in inhomogeneous lungs such as in ALI/ARDS.
We observed that the effect of the RMs on EELV was greater measured with EIT than with a N2 washout/washin technique. This could possibly be explained by EELVN2 primarily measuring the “effective functional residual capacity” in terms of gas exchange while EIT measuring changes in electrical properties related to the total amount of air in relation to fluid in the scanned slice. Similar differences have been showed comparing measurements of functional residual capacity using SF6 and CT in ARDS patients .
This study shows that alveolar recruitment can be achieved using lower airway pressure levels maintained over a longer period. With the slow, lower pressure RM used in the present study LV initially increased rapidly, probably as an effect of PEEP elevation to 15 cmH2O, and the ensuing gradual increase throughout the 15 min of recruitment was probably a combined effect of repeated prolonged end-inspiratory pauses and PEEP elevation. Interestingly, these effects were achieved with ventilation using relatively low plateau pressure (27±0.9 cmH2O), which was maintained over a longer period than with high-pressure RMs. Previous studies have indicated that both airway pressure and time determines the effect of RMs . The plateau pressure used in this study is in agreement with current protective ventilatory strategies avoiding pressures above 30 cmH2O , while recruitment strategies including ViCM, PCRM, or sighs [32, 33] use peak airway pressure of 40–50 cmH2O. Whether increased PEEP maintained for longer period alone can increase LV remains to be further investigated [34, 35]. The high-pressure RMs increased LV significantly more than SLRM during recruitment, but even 1 min after cessation of maneuvers the gain in EELV did not differ between RMs (Fig. 3).
However, the success of a RM cannot be judged from the increase in LV alone since this could be the result of the same number of alveoli being more inflated. It has been proposed that successful recruitment should result in an increase in compliance and oxygenation and a decrease in PaCO2. This study observed an increase in LV, PaO2 and compliance and a decrease in PaCO2 15 min after completion of recruitment for all three maneuvers. Interestingly, a slow low-pressure RM resulted in greater improvement in oxygenation, shunt, and compliance than the high-pressure maneuvers.
During the RMs total as well as midventral, middorsal, and dorsal regional compliance increased significantly and compliance in ventral parts remained unchanged, confirming that the increase in EELV is the result of recruitment and not overinflation. As a result of this redistribution of the TV to the middorsal and dorsal regions occurred. This was seen irrespective of RM. However, during PCRM compliance decreased with 50% in the ventral region as a sign of baro-/volostress to these alveoli (Fig. 6). This was not seen with SLRM. Thus it seems that the PCRM results in effective recruitment of alveoli but at the cost of overdistension, whereas the slow, low pressure RM lacks this negative effect. During the ViCM it was not possible to calculate regional compliance since this is a nonventilatory maneuver, but as the pressure used is of the same magnitude as during the PCRM, mechanical stress is probably similar.
Irrespective of RM it is important to maintain an increased PEEP following recruitment [35, 36, 37]. Dyhr et al.  showed that PEEP after the RM kept the lung open, but as soon as PEEP was decreased LV returned to the pre-RM level.
In the present study, despite a PEEP of 10 cmH2O after recruitment there was a gradual decrease in EELV, stabilizing at around 15 min. The regional EIT tracing showed no decrease in EELV in the ventral regions but a prominent decrease was seen in dorsal regions (Fig. 5). Thus the regions where most of the recruitment occurred were also those most prone to lose its recruited volume. It is possible that the decrease in LV in the two lower regions could have been prevented by a higher PEEP level, combined with a lower TV to avoid overdistension of the upper regions. Possibly, regional EIT could be used for postrecruitment optimal PEEP and TV titration.
In accordance with previous studies [4, 5, 6] we observed a marked decrease in cardiac output during the RMs: ViCM>PCRM>SLRM, where the modest hemodynamic effect of the SLRM probably is explained by the relatively low airway pressures. Following release of RMs a significant decrease in arterial oxygenation occurred. This was probably due to a return of “pooled” poorly saturated blood from the periphery while a pulmonary shunt of around 10% still remained. With SLRM this phenomenon was less pronounced (Figs. 2, 4).
In this porcine surfactant deficiency ALI model representing early ARDS lung recruitment was achieved with a slow, low pressure RM with less circulatory depression and probably less risk of barotrauma. This less aggressive RM actually resulted in greater improvement in oxygenation, shunt, and compliance than high-pressure maneuvers. LV changes could be monitored by EIT and regional ventilation distribution assessed. Although the EIT technique has limitations and needs further development, it could be valuable as a dynamic monitoring tool to optimize ventilatory care of ALI patients in the future.
The authors thank Dr. Annette Nyberg and Marita Ahlqvist EMA for valuable assistance during the experiments. The EIT equipment was supplied by Dräger Medical AG, Germany, and the authors are grateful for valuable advice from Mr. Eckhard Teschner. This study was supported by grants from the Medical College of Gothenburg University, the Swedish Research Council (K2003-04X-14032-03A), and the Gothenburg Medical Society. The results of this study were in part presented at the ESA meeting in Lisbon 2004 and the ESICM meeting in Berlin, 2004.
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