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Selective Recruitment Maneuvers for Lobar Atelectasis: Effects on Lung Function and Central Hemodynamics: An Experimental Study in Pigs

Section Editor(s): Takala, JukkaHansen, Lars Kjærsgaard MD*; Sloth, Erik MD, PhD†‡; Nielsen, Jonas MD§; Koefoed-Nielsen, Jacob MD*†; Lambert, Per MD*; Lunde, Søren MS†‡; Larsson, Anders MD, PhD*†

doi: 10.1213/01.ane.0000202477.29064.49
Critical Care and Trauma: Research Report

We investigated whether selective lung recruitment of a lobar collapse would improve oxygenation and lung volume as well as a general (global) lung recruitment maneuver, with fewer circulatory side effects. In 10 ventilated, anesthetized pigs, a bronchial blocker was inserted in the right lower lobe, which was selectively lavaged to create a dense lobar collapse. The pigs were randomized into two orders of lung recruitment maneuvers (40 cm H2O airway pressure for 30 s): either a selective lung recruitment maneuver (using the inner lumen of the bronchial blocker) followed by a general lung recruitment maneuver, or vice versa. Median end-expiratory lung volume and median Pao2 increased significantly by approximately 100 mL and 16 kPa, respectively, with no significant differences between the two recruitment methods. There were no circulatory changes during the selective lung recruitment maneuver, but during the general lung recruitment maneuver, mean arterial blood pressure decreased significantly by 36 (21, 41) mm Hg (median, 25th and 75th percentiles), cardiac output by 2.1 (1.6, 2.5) L/min and left ventricular end-diastolic area by 4.4 (3.5, 4.5) cm2. In conclusion, a selective recruitment maneuver improved lung function similar to a general lung recruitment maneuver but without any circulatory side effects.

IMPLICATIONS: Lobar lung collapse is common after anesthesia and surgery. A standard, general (global) lung inflation maneuver is usually effective in improving lung function but may cause significant cardiovascular depression. This experimental study shows that selective inflation of a collapsed lobe via a balloon catheter is effective and has no significant circulatory side effects.

*Department of Anesthesia and Intensive Care Medicine, Center for Cardiovascular Research, Aalborg Hospital, Aarhus University Hospitals, Aalborg, Denmark; †Clinical Institute, Aarhus University, Århus, Denmark; ‡Department of Anesthesia and Intensive Care Medicine, Skejby Hospital, Aarhus University Hospitals, Århus, Denmark; and §Department of Anaesthesia and Intensive Care Medicine, Copenhagen University Hospital Gentofte, Hellerup, Denmark

Accepted for publication December 16, 2005.

The study was supported by Grants 22-03-0299 and 22-04-0420 from the Danish Medical Research Council, Grant 04-10-B152-A230-22194 from the Danish Heart Association, and Grant 100301 from the Clinical Institute, Århus University, Denmark.

Address correspondence to Anders Larsson, MD, PhD, Department of Anesthesia and Intensive Care Medicine, Aalborg Hospital, Århus University Hospitals, Hobrovej 18-22, DK 9000 Denmark. Address e-mail to

Atelectasis is common after cardiac surgery and frequently produces a significant intrapulmonary shunt (1). In these patients, lung recruitment maneuvers (LRMs) may be indicated. However, such maneuvers increase the intrathoracic pressure and could thus impede the right ventricular outflow, decrease the filling of the left ventricle, and significantly reduce cardiac output (2). Intramuscular fluid administration is often used to counteract this side effect; however, in our experience, patients in the postoperative phase do not always tolerate an increase in intravascular volume, and circulatory instability may follow LRMs. Thus, an alternative approach might be useful in patients with marginal circulatory reserve.

Selective recruitment of a collapsed lung lobe by the use a balloon catheter has been reported to be effective as a last resort for treatment of a lobar atelectasis (3,4). Recently, bronchial blockers have been developed for isolating lung lobes during pulmonary surgery. By using the central lumen of the blocker, a high airway pressure can be selectively directed to a collapsed lobe without affecting other parts of the lung. We hypothesized that this method would be as effective in improving oxygenation as a general LRM but without any serious circulatory side effects. The aim of the present study was to test this hypothesis in an experimental model of lobar collapse by comparing central hemodynamics, lung mechanics, and blood gases during both a general and a selective LRM.

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The study was approved by the local animal ethics committee, and the National Institutes of Health principles of laboratory care were followed. Ten pigs, 20–25 kg, were premedicated with azaperone 80 mg IM and midazolam 10 mg IM. Anesthesia was induced with fentanyl 5 μg/kg IV and ketamine 2 mg/kg IV, and the trachea was intubated with a 6-mm ID endotracheal tube. The lungs were ventilated by a Servo 900 C ventilator (Siemens-Elema, Solna, Sweden) with volume control, tidal volume of 8 mL/kg, positive end-expiratory pressure (PEEP) of 10 cmH2O, and fraction of inspired oxygen (Fio2) of 1.00. Inspiratory time was set to 35% and end-inspiratory pause time was 10%, with the rate adjusted to achieve an arterial pH of approximately 7.4. After the initial adjustment, the ventilator setting was not changed during the experiment, except during the LRMs. After a bolus dose of propofol (1 mg/kg), anesthesia was maintained with ketamine 10 mg/kg/h, fentanyl 5 μg/kg/h, propofol 2 mg/kg/h, and pancuronium 0.25 mg/kg/h. This combination of drugs has been shown in previous experiments to give adequate anesthesia (5). A tracheotomy was performed, and the orotracheal tube was replaced with a 9-mm inner diameter endotracheal tube (Portex 9.0; Smiths Medical, London, UK).

An infusion of 20 mL/kg Ringer’s acetate solution was given during the first hour, followed by 10 mL/kg/hour for the remainder of the experiment. In seven animals, 5–10 mL/kg of dextran 70 (Macrodex; Pharmalink AB, Upplands Väsby, Sweden) was administered to achieve normovolemia, as assessed by stroke volume variation < 10%, before the main experiment was initiated (6).

Catheters were placed in the right femoral artery, the right carotid artery, and the right internal jugular vein for sampling blood gases and monitoring of intravascular pressures and pulse contour cardiac output (PCCO). A pulmonary artery catheter (Swan-Ganz CCO mbo CCO/SvO2 7.5 French; Edwards Lifesciences, Irvine, CA) was placed via the external jugular vein to monitor pulmonary artery pressure and mixed venous oxygen saturation online using a Vigilance monitor (Edwards Lifesciences). A suprapubic urinary catheter was used to measure diuresis.

PCCO was obtained through the catheter (4 French, 16-cm Pulsiocath; Pulsion Medical Systems, Munich, Germany) placed in the right carotid artery connected to the PCCO monitor (Pulsion Medical Systems). The PCCO measurement was calibrated immediately after induction of anesthesia using the transpulmonary arterial thermodilution technique (10 mL of cold saline). The average result of three cardiac output measurements was used. During the entire study period, cardiac output data along with arterial blood pressure and heart rate were recorded at 1-s intervals using an interface and a computer with PiCCOwin Plus software.

Transthoracic echocardiography was performed using a 2.5 MHz probe and a Vivid 7 ultrasound machine (GE Healthcare, Horten, Norway). After obtaining a parasternal short axis view of the left ventricle (LV), three cine-loops in sinus rhythm were digitally recorded for off-line analysis. For optimal image comparison the incorporated split-screen feature was used, enabling a reference image and the real-time image to be displayed simultaneously. End-diastolic and end-systolic areas (LVEDA and LVESA, respectively) of three cine-loops were traced and averaged using dedicated software (EchoPac; GE Healthcare, Horten, Norway). The analysts were blinded to the recruitment maneuver.

End-expiratory lung volume (EELV) was measured with an inert gas washout technique using sulfur hexafluoride as tracer gas (7). This method can be used without changing the ventilator settings or interrupting ventilation.

Quasistatic compliance of the respiratory system (Crs) was calculated as tidal volume/(end-inspiratory plateau pressure – end-expiratory pressure). End-expiratory pressure was obtained after a 5-s end-expiratory hold.

Blood gases were sampled from the femoral and pulmonary arteries and analyzed by an ABL 710 (Radiometer, Copenhagen, Denmark), and venous admixture (QS/QT) was calculated using the standard formula: QS/QT = ((Cc′o2 – Cao2)/(Cc′o2 – CvO2)), where Cc′o2 is the end-capillary blood oxygen content estimated using the alveolar air equation, and Cao 2 and Cvo2 are the arterial and mixed venous oxygen content, respectively (8). Because an Fio2 of 1.0 was used, the venous admixture is a very close estimate of the pulmonary shunt (8).

(Fig. 1) Via the 9-mm endotracheal tube, a bronchial blocker (Cook C-AEBS-7.0-65-SPH; Cook Critical Care, Bloomington, IN) was inserted in the right lower lobe (approximately 50 cm distal to the endotracheal tube opening) under fiberoptic guidance (Olympus BF-3C40, Tokyo, Japan). To ensure a correct position, the balloon of the blocker was briefly inflated. Arterial blood gases were measured and the respiratory rate adjusted. No further changes to the ventilator settings were made during the experiment. To standardize the lung volume history, an LRM (using pressure-controlled ventilation with peak pressure of 40 cm H2O, PEEP 10 cm H2O, inspiratory/expiratory ratio 1:1 and respiratory rate of 6/min over 2 min) was performed, after which EELV and Crs were measured and blood gases (mixed venous and arterial) were sampled. Under fiberoptic visualization, the balloon of the bronchial blocker was then inflated, and the gas in the isolated right lower lobe exsufflated and measured (the exsufflated gas volume was recorded as “lobe volume”). Thereafter the lobe was selectively lavaged (with a lobe volume of 37°C normal saline) using a syringe, 15 times or until no frothing of the lavaged fluid was seen. The volume of injected and removed fluid was measured. The inner lumen of the bronchial blocker was connected to 10 cm H2O negative pressure and the inspiratory and expiratory tidal volumes were checked to confirm the seal between the bronchial blocker cuff and the bronchial wall. EELV, Crs, and blood gases were obtained to confirm lobar collapse and to establish baseline values.

Figure 1

Figure 1

(Fig. 1)The pigs were randomized (by sealed envelopes) into two sequences of LRMs: either an initial selective LRM followed by a general LRM, or vice versa. The second maneuver was preceded by exsufflation of the isolated lobe and application of a negative pressure (–10 cmH2O) for 10 minutes. During the selective LRM, the bronchial cuff was inflated, and the isolated lobe was inflated via the inner lumen of the bronchial blocker, whereas the general LRM was performed via the endotracheal tube with the bronchial cuff deflated.

The LRM was performed by insufflation to a pressure of 40 cmH2O for 30 s. During the selective LRM, a calibrated water manometer connected to an oxygen gas source ensured correct pressure, whereas the function of the ventilator for continuous positive airway pressure was used for the general LRM. During the selective LRM, ventilation of the noncollapsed lung was uninterrupted.

Values for LVEDA, LVESA, PCCO, and vascular pressures were recorded immediately before the maneuvers, during the final 5 s, and 3 min after termination. In addition, values for blood gases, shunt, EELV, and Crs were obtained both immediately before and 3 minutes after each LRM.

In two animals, the lobe was recollapsed after the procedure; one of the animals was thoracotomized, the lobe was inspected before, during and after inflation, and in the other animal computed tomography was performed before and after inflation of the collapsed lobe (Fig. 2).

Figure 2

Figure 2

Results are presented as median and 25th and 75th percentiles, if not otherwise indicated. Comparisons between the two modes of LRM were done with the Wilcoxon signed ranks test using the SAS 9.1 statistical package (SAS Institute, Cary, NC). Comparisons between the different measurement points (before versus end of and before versus 3 min after the LRM) were done using the Kruskal-Wallis test for nonparametric one-way analysis of variance followed by the Wilcoxon signed ranks test. In the calculation of the P values a two-tailed approach was used. We considered P < 0.05 as significant, except for comparisons between the different measurement points, where we considered P < 0.025 as significant (according to Bonferroni correction).

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The volume exsufflated from the isolated lobe (“lobe volume”) was 50 (50,75) mL. This was reflected in a decrease in EELV by 178 (128,238) mL (P = 0.0051), Crs by 12 (10,14) mL/cmH2O (P = 0.0050), Po2 by 26 (24,33) kPa (P = 0.0051) and an increase in venous admixture (n = 7) by 12 (6, 18)% (P = 0.018) (Table 1). Computed tomography and inspection of the lung showed a dense collapse (Fig. 2).

Table 1

Table 1

The selective LRMs induced an increase in EELV by 103 (70, 135) mL (P = 0.0077), in Pao2 by 16 (7,27) kPa (P = 0.0051), and in Crs by 6 (9, 4) mL/cmH2O (P = 0.0050). Venous admixture (n = 7) decreased by 6 (3, 11)% (P = 0.018) (Table 1). The general LRMs induced an increase in EELV by 110 (84, 140) mL (P = 0.0051), in Pao2 by 18 (12, 23) kPa (P = 0.0093), and in Crs by 11 (10,12) mL/cmH2O (P = 0.0050), whereas venous admixture (n = 7) decreased by 9 (–2, 11)% (P = 0.091) (Table 1). Thus the results were similar for both maneuvers, with the exception of Crs, which was significantly less improved (P = 0.0051) by the selective maneuver.

During the selective LRMs the hemodynamic variables did not change (Table 2). However, during the general LRM, mean arterial blood pressure decreased by 36 (21, 41) mm Hg (P = 0.0051), cardiac output by 2.1 (1.6, 2.5) L/min (P = 0.0077), and LVEDA by 4.4 (3.5, 4.5) cm2 (P = 0.0051) (Table 2, Fig. 3), and both central venous pressure and mean pulmonary artery pressure increased significantly (P = 0.0050 and P = 0.0050, respectively) (Table 2). There were significant differences (P = 0.0050-0.0077) in all hemodynamic variables, except heart rate, between the two maneuvers.

Table 2

Table 2

Figure 3

Figure 3

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This study shows that a selective recruitment maneuver of a lower lobar collapse was as effective as a general LRM, as assessed by lung volume gain and oxygenation but had negligible circulatory side effects.

Experimental lung lobar collapse has been induced by blocking bronchi with balloons and plugs or by bronchial ligation (9). Lung lavage is a widely used method to achieve experimental lung injury (10). However, the combined approach for inducing a dense lobar collapse, as used in the present study, has not been previously reported to our knowledge. Inspection of the lung in the thoracotomized animal showed that the collapse was very profound, and during inflation, it took approximately one minute before it fully expanded (Fig. 2). This was also reflected by the lung volume failing to recover completely after both general and selective LRMs (Table 1). This is consistent with the results of Halter and al (11). Using surface in vitro microscopy, they examined surfactant-depleted pig lungs and showed that some alveoli were first recruited after 45 seconds of a general LRM consisting of pressure-controlled ventilation with 45/35 cmH2O airway pressure.

In most patients who develop lobar collapse in connection with anesthesia, short general LRMs using airway pressures of approximately 40 cmH2O are usually effective (12). Anesthesia-induced lung collapse is due to absorption of oxygen in closed airways in combination with compression of dependent lung regions (13,14). On the other hand, lung collapse after major surgery, particularly after heart surgery performed under cardiopulmonary bypass, also includes a component of inflammatory reaction with capillary leakage and edema, and may therefore be more difficult to recruit (15). However, even in these situations, general LRMs are often effective, but can significantly depress circulation (2,16,17). In fact, in hemodynamically stable patients after coronary artery bypass surgery we have found that cardiac output and LVEDA decreased by 50% during a 10s LRM using an airway pressure of 40 cmH2O (2). Furthermore, in some of these patients, it took up to 5 min after the maneuver for cardiac output and arterial blood pressure to recover (2). Under hemodynamically unstable conditions, the negative influence on circulation by a general LRM can be even more pronounced. Indeed, in pigs in which we removed 15% of the blood volume by venesection, cardiac output almost ceased during a 10-s general LRM with 40 cmH2O airway pressure (18). Therefore, in patients with major lung collapse combined with circulatory depression (which cannot be treated with fluids), an alternative to the general LRM is needed.

Various methods for selective recruitment in cases of atelectasis have been proposed, although not as an alternative to general LRMs with the purpose of avoiding circulatory side effects, but as a last resort when other methods have failed. Sachdeva et al. (19) showed in a case report from 1974 that intubation of the main bronchus of an atelectatic lung followed by hyperinflation was effective. When fiberoptic bronchoscopy became common, inflation of air via the bronchoscope into the collapsed lobe with or without proximal occlusion of the bronchus was described (20–22). In a case report, Lee and Wright (3) inflated lobar collapse by the use of a balloon catheter, and this method has been reported in at least one case series since then (4). However, whether this method had any circulatory side effects was not reported. The circulatory depression during a general LRM is due to increased intrathoracic pressure compressing the right atrium and the pulmonary vessels, thereby impeding both the filling of the heart and the outflow from the right ventricle (2,18,23–25). In addition, hyperinflation of the lungs may induce peripheral vasodilatation, bradycardia, and a negative inotropic response, probably mediated through a vagal afferent reflex (26). In our study, the general recruitment maneuvers induced significant reductions in cardiac output and in LV areas (Table 2, Fig. 3). In contrast, the selective LRMs neither increased the intrathoracic pressure, as assessed from the airway pressures, nor produced any circulatory depression (Table 2, Fig. 3). We did not measure the vascular resistance in the affected lobe, but theoretically it should have been high during the collapse and decreased after the recruitment maneuver. However, any difference in vascular resistance in this lobe did not affect the general outflow impedance from the right ventricle, because we did not find any change of the filling of the left heart or in cardiac output.

Although the effect on lung function was very similar, the mechanism may be different for the two methods. In a general LRM, the airway pressure is applied to the whole lung. Thus, the lung regions adjacent to the collapsed lobe will be subjected to the same pressures as the collapsed lobe. Because there is no pressure difference between the collapsed and the adjacent lung, the collapsed lobe can only expand toward the chest wall (i.e., usually toward the dependent part of the diaphragm). This is governed by the pressure difference between the collapsed lobe and the pleura (i.e., the local transpulmonary pressure). In addition, a general LRM may expand other partly collapsed lung regions than the artificial atelectasis. This mechanism might explain the slightly larger improvement in compliance after the general recruitment maneuver.

In contrast to general LRMs, we hypothesize that during selective LRMs, the pressure that governs the expansion might not be the local transpulmonary pressure, but rather the pressure applied in the affected bronchus minus the general airway pressure, and theoretically the collapsed lobe may expand in all directions. Ten cmH2O of PEEP was applied to prevent derecruitment after the maneuvers. It is important to note that the inspiratory pressures induced by the application of PEEP were < 22 cmH2O, well below the pressure of approximately 40 cmH2O that is needed to induce lung recruitment per se (27).

Although results obtained in animal experiments may not be valid in humans, our results suggest that selective LRMs are effective and have minimal cardiovascular side effects. Both bronchial blockers and fiberoptic equipment are available in most hospitals, and we therefore believe that this method may prove to be an alternative to a general LRM in some patients with lobar atelectasis.

The study has several limitations. The animals were young and healthy, and the intervention was brief, with a short follow-up period. However, the main purpose was to evaluate the immediate cardiopulmonary effects of the two LRMs. We did not determine the optimal time or pressure for the selective LRM. In theory, the airway pressure should be lower and the time for recruitment should be longer. In addition, the study was performed in animals with stable circulatory systems, and we cannot judge whether the circulatory safety profile is similar during hemodynamic compromise.

In conclusion, this study showed, in pigs, that a selective LRM effectively improved oxygenation and increased lung volume in experimental lung lobar collapse without inducing any observed circulatory side effects. In addition, the study confirms that general LRMs do briefly compromise circulation to a significant degree.

We appreciate the valuable and skilled help in the laboratory of Henrik Sørensen and Carsten Riis and the kind help with CT examinations of Gratien Andersen MD, Department of Diagnostic Imaging, Skejby Hospital, Aarhus University Hospital.

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