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Effects of Lung Recruitment Maneuvers on Splanchnic Organ Perfusion During Endotoxin-Induced Pulmonary Arterial Hypertension

Daudel, Fritz*†; Gorrasi, José*†; Bracht, Hendrik*†; Brandt, Sebastian†‡; Krejci, Vladimir†‡; Jakob, Stephan M.*†; Takala, Jukka*†; Rothen, Hans Ulrich*†

doi: 10.1097/SHK.0b013e3181e03bfb
Basic Science Aspects

Lung recruitment maneuvers (RMs), used to reopen atelectatic lung units and to improve oxygenation during mechanical ventilation, may result in hemodynamic impairment. We hypothesize that pulmonary arterial hypertension aggravates the consequences of RMs in the splanchnic circulation. Twelve anesthetized pigs underwent laparotomy and prolonged postoperative ventilation. Systemic, regional, and organ blood flows were monitored. After 6 h (= baseline), a recruitment maneuver was performed with sustained inflation of the lungs. Thereafter, the pigs were randomly assigned to group C (control, n = 6) or group E with endotoxin-induced pulmonary arterial hypertension (n = 6). Endotoxemia resulted in a normotensive and hyperdynamic state and a deterioration of the oxygenation index by 33%. The RM was then repeated in both groups. Pulmonary artery pressure increased during lipopolysaccharide infusion from 17 ± 2 mmHg (mean ± SD) to 31 ± 10 mmHg and remained unchanged in controls (P < 0.05). During endotoxemia, RM decreased aortic pulse pressure from 37 ± 14 mmHg to 27 ± 13 mmHg (mean ± SD, P = 0.024). The blood flows of the renal artery, hepatic artery, celiac trunk, superior mesenteric artery, and portal vein decreased to 71% ± 21%, 69% ± 20%, 76% ± 16%, 79% ± 18%, and 81% ± 12%, respectively, of baseline flows before RM (P < 0.05 all). Organ perfusion of kidney cortex, kidney medulla, liver, and jejunal mucosa in group E decreased to 65% ± 19%, 77% ± 13%, 66% ± 26%, and 71% ± 12%, respectively, of baseline flows (P < 0.05 all). The corresponding recovery to at least 90% of baseline regional blood flow and organ perfusion lasted 1 to 5 min. Importantly, the decreases in regional blood flows and organ perfusion and the time to recovery of these flows did not differ from the controls. In conclusion, lipopolysaccharide-induced pulmonary arterial hypertension does not aggravate the RM-induced significant but short-lasting decreases in systemic, regional, and organ blood flows.

ABBREVIATIONS-CI-cardiac index; LPS-lipopolysaccharide; MAP-mean arterial pressure; MPAP-mean pulmonary artery pressure; RM-lung recruitment maneuver

*Department of Intensive Care Medicine, Inselspital, Bern University Hospital; University of Bern; and Department of Anesthesiology, Inselspital, Bern University Hospital, Bern, Switzerland

Received 7 Dec 2009; first review completed 29 Dec 2009; accepted in final form 4 Mar 2010

Address reprint requests to Fritz Daudel, MD, Department of Intensive Care Medicine, Inselspital, Bern University Hospital, and University of Bern, CH-3010 Bern, Switzerland. E-mail:

This study was supported by the Swiss National Science Foundation (grant no. SNF 3200BO-102268), Bern, Switzerland, and by the Department of Intensive Care Medicine, Bern University Hospital and University of Bern, Bern, Switzerland.

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Lung recruitment maneuvers (RMs) are frequently performed procedures in the ventilatory management of anesthetized (1, 2) and critically ill patients (3, 4) and are used to re-expand atelectasis and to improve gas exchange. The RMs produce high intrathoracic pressures, resulting in marked hemodynamic compromise (5). Because an increase in intrathoracic pressure increases pulmonary artery resistance, patients with pulmonary arterial hypertension may be at specific risk for RM-induced hemodynamic compromise. Pulmonary arterial hypertension and moderate or transient right ventricular dysfunction can frequently be detected in intensive care patients. For example, transient right ventricular dysfunction occurs after cardiac surgery (6, 7) and pulmonary arterial hypertension, and dysfunction of both ventricles is common during sepsis and endotoxemia (8-11).

Because increases in intrathoracic pressure reduce right ventricular preload and increase hepatosplanchnic vascular resistance, RMs may especially affect splanchnic perfusion (12, 13). Increases in intrathoracic pressure induced by high positive end-expiratory pressure (PEEP) levels have been shown to decrease splanchnic blood flow when associated with a decreased cardiac output (14-16). However, during stable hemodynamics, PEEP had no effect on splanchnic blood flow (17).

It is unclear to what extent regional and organ perfusion are affected by RMs in patients with pulmonary arterial hypertension. We hypothesized that acute increases in pulmonary artery pressure aggravate the adverse effects of RMs on gastrointestinal regional and organ blood flow during endotoxemia. Accordingly, the present study was designed to assess duration and extent of changes in gastrointestinal perfusion after lung RMs in a porcine model of lipopolysaccharide (LPS)-induced acute pulmonary arterial hypertension.

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The study was performed in accordance with the National Institutes of Health guidelines for the care and use of experimental animals. It was approved by the governmental Animal Care Committee of Bern, Switzerland. The experiments were performed in 12 anesthetized and paralyzed pigs with a mean weight of 39.7 ± 4.0 kg.

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Anesthesia and surgical preparation

The pigs were deprived of food but had free access to water for 24 h before the experiment. The animals were premedicated with 3 mg·kg−1 azaperone (Stresnil, Janssen Pharmaceutica, Beerse, Belgium) and 1 mg atropine i.m., followed by cannulation of an ear vein, and i.v. induction of general anesthesia with 10 mg·kg−1 pentobarbital (Vetanarcol) and 1 mg atropine before intubation. Neuromuscular blockade throughout the experiment was achieved with pancuronium at a continuous infusion of 1 mg·kg−1·h−1. Analgesia during the surgical procedure was accomplished with 25 μg·kg−1·h−1 fentanyl, which was reduced to 3 μg·kg−1·h−1 after completion of surgery and maintained at that level until the end of the experiment. Anesthesia was maintained with 7 mg·kg−1·h−1 pentobarbital. The animals were ventilated with a volume-controlled mode (Servo 900 C; Siemens, Erlangen, Germany). The PEEP was set at 5 cm H2O, and the fraction of inspired oxygen (FIO2) was adjusted to keep arterial partial oxygen pressure (PaO2) at 100 to 150 mmHg. Tidal volumes (VT) were kept at 10 mL·kg−1, and minute ventilation was adjusted to maintain an arterial partial carbon dioxide pressure (PaCO2) of 35 to 40 mmHg.

An arterial catheter was inserted in the right carotid artery and advanced toward the junction with the aortic arch. A pulmonary artery catheter (CO/mixed venous saturation Catheter; Edwards Lifesciences, Irvine, Calif) was placed via the left internal jugular vein. A second catheter was inserted into the hepatic vein via the right internal jugular vein. Standard vascular catheters were also inserted into the hepatic artery and the portal vein.

All flow probes, used to assess blood flow and microcirculation of the visceral organs (see later), were inserted via a midline laparotomy. After completion of the surgical procedures and control of the signal quality of the ultrasonic flow probes and laser Doppler probes, the abdomen was closed.

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Hemodynamics, regional blood flow, and organ perfusion

Intravascular pressures were continuously recorded with a multimodular monitor (Datex-Ohmeda S/5 Compact Critical Care monitor; Datex-Ohmeda, Helsinki, Finland). Continuous cardiac output measurements were performed with the Vigilance monitor (Baxter Healthcare Corporation, Edwards Critical Care Division, Irvine, Calif). This monitor displays a moving average of the 10 latest 1-min values. Aortic pulse pressure changes, a surrogate of cardiac stroke volume (18, 19), were assessed by measuring systolic and diastolic pressure difference beat by beat and averaged over a whole respiratory cycle for further analysis.

To assess blood flows to visceral organs, the celiac trunk and hepatic, superior mesenteric, splenic, and renal arteries were exposed and equipped with ultrasound transit time flow probes (Transonic Systems, Ithaca, NY). Signals from the flowmeters (T206 and T106, Transonic Systems) were recorded online for further analysis (Windaq 1.60, Dataq Instruments Inc, Akron, Ohio).

Splanchnic perfusion and renal organ perfusion were assessed with laser Doppler flowmetry (LDF), a technique validated for splanchnic organs that has been shown to correlate well with established techniques for regional blood flow measurements, such as microspheres (20), hydrogen gas clearance (21, 22), xenon washout (23), and reflectance spectrophotometry (24). Laser Doppler flowmetry is an application of the Doppler principle based on the measurement of frequency shifts of laser light encountering moving intravascular erythrocytes. Thereby, the velocity measurement of LDF represents the average of the velocities in all vessels of the sample volume of about 1 µL. Blood flow heterogeneity, a major parameter of microcirculation, however, is not taken into account.

Laser Doppler signals were analyzed during the RM and during a period of 20 s at all other time points. Laser Doppler flow probes (Oxyflow 2000; Oxford Optronics Ltd, Oxford, UK) were fixed to the liver, mucosa of the jejunum, renal cortex, and medulla. For liver and kidney medulla, needle probes were used. For the other organs, surface probes were attached with microsutures to ensure close tissue contact. Care was taken to avoid any pressure or traction on the laser Doppler flow probes. Laser Doppler flowmeters are not calibrated to measure absolute blood flow but to assess blood flow in arbitrary perfusion units. Accordingly, the results are expressed as relative changes compared with baseline.

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Experimental protocol

After the surgical preparation, 6 h were allowed for hemodynamic stabilization before the experimental protocol was started. Volume resuscitation was achieved with 10 mL·kg−1·h−1 Ringer's lactate solution. To maintain pulmonary artery occlusion pressure between 5 and 8 mmHg, additional fluid boluses were given as hetastarch solution (Voluven). Twenty minutes before the recruitment maneuver, an additional fluid bolus of 200 mL hetastarch solution was administered to ensure adequate volume status.

The first recruitment maneuver (RM1) was performed as previously described (25). Baseline ventilation was interrupted by a sustained inflation of the lungs to a pressure of 30 cm H2O, lasting for 10 s. Baseline ventilation was resumed thereafter.

Hemodynamic and splanchnic perfusion variables were recorded at baseline (i.e., 1 min before the RM), during the RM, and 1, 3, 5, 8, and 15 min after the RM. Respiratory gas volumes, flows, pressures, and the derived dynamic compliance were measured by an electronic spirometric system (Datex-Ohmeda S5), with the sensor positioned between the endotracheal tube and y piece. Arterial blood samples were taken before the RM and 5 min after the RM for blood gas analysis using a standard technique.

Subsequently, the animals were randomly assigned to either group C (control, n = 6) or group E (endotoxemia, n = 6). After full recovery from the RM, an LPS (from Escherichia coli 0111:B4; Sigma, Steinheim, Germany) infusion was started. The initial infusion rate was set at 0.4 μg·kg−1·min−1 and adjusted to reach a MPAP of 30 to 35 mmHg. After a period of 8 h, the LPS infusion rate was kept constant until the end of the experiment. After 12 h of LPS infusion, the same RM was performed again (RM2), and hemodynamic variables were assessed in the same manner. The animals of group C received identical treatment except for the infusion of LPS. Subsequently, the animals served for another experiment (26).

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Statistical analysis

For statistical analysis, SPSS software 15.0 (SPSS Inc, Chicago, Ill) was used. Normal distribution was confirmed with the Kolmogorov-Smirnov test. To determine the effects of the RM on hemodynamic variables, analysis of variance (ANOVA) for repeated measurements was applied using one dependent variable, one grouping factor (endotoxin versus controls), and two within-subject factors (time [RM1, RM2] and recruitment [baseline −15 min after recruitment]). Furthermore, baseline values, maximal flow decrease, and time to recovery to a flow of at least 90% of baseline for both RM1 and RM2 were compared within and between groups using paired and unpaired t tests as appropriate. Data are expressed as mean ± SD. For all statistical tests, a P < 0.05 was considered significant.

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Effects of LPS infusion

Mean pulmonary artery pressure increased during LPS infusion from 17 ± 2 mmHg to 31 ± 10 mmHg and remained unchanged in controls (time-group interaction, P < 0.05; Table 1). The increase in blood pressure, cardiac output, and regional blood flows in LPS-exposed animals was not significantly different from a similar increase in control animals (Table 1; Figs. 1 and 2).



Fig. 1

Fig. 1

Fig. 2

Fig. 2

Of note, endotoxin-induced increase of regional flows in the superior mesenteric artery (SMA), celiac trunk, and portal vein was disproportionately higher compared with the increase of the cardiac index (CI), whereas the increase of renal artery flow and hepatic artery flow was in proportion to changes of the CI. The increases of the SMA/CI ratio from RM1 to RM2 were in the controls 0.12 ± 0.03 to 0.19 ± 0.05 and in the endotoxin group 0.10 ± 0.03 to 0.14 ± 0.03, respectively (P < 0.001, between groups). The increases for the celiac trunk/CI between RM1 and RM2 were as follows: controls 0.05 ± 0.02 to 0.09 ± 0.04, endotoxin group 0.06 ± 0.03 to 0.09 ± 0.03 (P = 0.008); and for the portal vein/CI ratio: control group 0.19 ± 0.03 to 0.25 ± 0.06, endotoxin group 0.19 ± 0.04 to 0.23 ± 0.05 (P = 0.004).

The analysis of respiratory-induced pulse pressure variations revealed for the control group before RM1 14.9% ± 2.5% and before RM2 11.6% ± 3.0%, and for the endotoxin group 13.9% ± 3.8% and 11.8% ± 2.8%, respectively (P = 0.16, time; P = 0.60, between groups).

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Effects of RMs

The effect of the RMs on systemic circulation was characterized by a significant decrease in mean arterial pressure (MAP) and aortic pulse pressure-a surrogate of cardiac stroke volume-followed by a rapid recovery in both groups. Of note, endotoxemia-induced pulmonary hypertension did not aggravate this transient decrease in stroke volume and MAP (Fig. 1).

During the respective recruitment maneuvers RM1 and RM2, the regional blood flows to liver, kidneys, and gut decreased significantly. In the endotoxemic animals (group E), blood flows of renal artery, hepatic artery, celiac trunk, SMA, and portal vein dropped to 71% ± 21%, 69% ± 20%, 76% ± 16%, 79% ± 18%, and 81% ± 12%, respectively (% of baseline flows before RM, mean ± SD, P < 0.05 all; see also Figs. 1 and 2). However, these decreases in regional flow were short-lived, and there was no difference in maximal decrease of flow or in time to 90% recovery of baseline flows between the two groups (Figs. 1 and 2).

Hepatic vein pressures were slightly higher in group E. However, this difference was already observed at baseline before RM1. The other splanchnic pressures did not differ between groups (Table 2).



The effect of RMs on organ perfusion showed a pattern of flow reduction comparable to the changes in regional flows (Tables 3 and 4). Organ perfusion of kidney cortex, kidney medulla, liver, and jejunal mucosa in group E decreased to 65% ± 19%, 77% ± 13%, 66% ± 26%, and 71% ± 12%, respectively (% of baseline flows before RM, mean ± SD, P < 0.05 all). Recovery times to at least 90% of baseline microcirculatory blood flow were between 1 and 5 min. No difference was noted between the groups regarding maximal decrease of perfusion and recovery time of flows toward baseline.





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Lung function and gas exchange

Oxygenation and dynamic compliance decreased in both study groups over time but did not show any significant differences between groups (Table 5).



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In this porcine model of endotoxin-induced acute pulmonary arterial hypertension, a moderate RM resulted in a significant decrease of abdominal regional and microcirculatory blood flow. However, these changes were only short-lasting and did not differ from those observed in a control group.

The goal of this study was to determine the effects of RMs on regional and microcirculatory blood flow in abdominal organs during acute pulmonary hypertension. The invasiveness of the preparation for the measurements of regional and organ blood flow, however, precluded a human study. A pig model was chosen because of similarities to human cardiovascular physiology and gastrointestinal anatomy (27). Of note, the RMs were performed during normotensive and hyperdynamic endotoxemia in the absence of a systemic cardiovascular shock state. The respiratory-induced pulse pressure variations also suggest an adequate volume status at the time the RMs were applied and were similar to those observed in another pig model during normovolemia (28). Sufficient and timely volume resuscitation during LPS infusion may result in normotensive endotoxemia (29-32).

Recruitment maneuvers have been recommended to re-expand atelectasis occurring during mechanical ventilation in the anesthetized subject (1, 2) or in critically ill patients (3, 4). However, RMs produce high intrathoracic pressures, which may result in marked hemodynamic compromise (5). The hemodynamic impairment of RM is thought to be caused by increased intrathoracic pressures and thus impaired venous return to the heart, with a subsequent decrease of cardiac output. The effects of RMs on systemic hemodynamics have been investigated in clinical studies (33-35) and animal models (12, 36, 37). Minor negative effects of an RM have also been described recently with regard to splanchnic regional flows in healthy animals (12).

With respect to mesenteric perfusion, the short-lasting effects of the RM in the present model of acute pulmonary hypertension are in accordance with recently presented findings in a model of lung injury (38). In patients with cerebral injury, by contrast, RM resulted in prolonged deterioration of cerebral hemodynamics and oxygenation (39). The comparability between studies, however, is limited because of differences in the applied RMs, both in terms of duration and in the level of sustained end-inspiratory airway pressure.

Our results confirm the relatively short-lived hemodynamic effects of RMs previously found in healthy animals. Importantly, in our model of acute pulmonary hypertension induced by endotoxemia, the effects of RMs did not impair abdominal regional and microcirculatory blood flow beyond the decrease observed in the control group. The decrease in abdominal flows was paralleled by a concomitant reduction of aortic pulse pressure, a surrogate of cardiac stroke volume (18, 19). A dissociation of the effects of RMs between gastrointestinal organ perfusion and systemic hemodynamics was therefore not observed. Of note, continuous cardiac output measurements did not depict changes in systemic flow caused by RMs. The most likely explanation for this observation may be a time constant in continuous cardiac output measurements exceeding the transient hemodynamic consequences of the RM. An additional point worthwhile to be mentioned is the slightly decreased venous saturations (Table 1) we attributed to reduced hemoglobin levels caused by blood loss during the instrumentation and dilution after volume resuscitation.

There are several limitations to our study. A major limitation is that its results are not based on human data. As already mentioned, the invasiveness of the surgical preparations for direct measurements of regional and organ perfusion precluded an investigation in humans. An inherent limitation of the model is that it included major abdominal surgery before the induction of endotoxemia. The influence of this preceding surgery on metabolic demands and blood flow may be superimposed on the effects of the endotoxemia. Another limitation of this study may be the fact that we measured organ blood flow but not variables of metabolism. On the other hand, markers of anaerobic metabolism of tissues may be detected only relatively late and only when blood flow is substantially reduced (40). Changes of organ blood flow during the interval of the RM were studied with LDF and related to the respective baseline value before each RM. Although LDF is capable of measuring fast changes of perfusion during provocation, it is very sensitive to motion artifacts and probe displacement (41). In this perspective, a comparison between the baselines of the different RM was not feasible because of signal instability during the considerable period between the RMs. Moreover, differences between the groups have to be interpreted cautiously because results are reported as changes in percent of baseline caused by the measurement of arbitrary perfusion units.

Although euvolemia is established in clinical practice when an RM is to be performed, our protocol to administer a fluid bolus to all animals 20 min before the RM does not represent a routine procedure. A further deviation of clinical practice comprised the perpetuation of the PEEP level after the RM to avoid influences on the hemodynamic measurements. This may explain the unchanged compliance and oxygenation caused by derecruitment of opened alveoli. Of note, the RMs were not conducted under hypoxemic conditions as may occur during acute respiratory distress syndrome. However, during endotoxemia, we observed a decrease of the oxygenation index of 33%.

Future experiments are necessary to determine the impact of other types of recruitment maneuvers during different stages of cardiovascular resuscitation and possibly to examine the influence of primary lung pathologies in this setting. Furthermore, when RMs are applied in clinical practice, the patients may receive concomitantly inotropic support. It has so far not been elucidated whether this modifies the cardiovascular response to RMs.

In summary, endotoxin-induced acute pulmonary hypertension does not intensify the negative hemodynamic consequences of a lung RM. In particular, regional and microcirculatory blood flows of gastrointestinal organs are preserved when compared with controls. Overall, an RM has very short-lasting effects on the circulatory system in general, and adverse effects in the splanchnic region are not prolonged. Our study therefore suggests that the adverse circulatory effects of a moderate RM are not aggravated during acute pulmonary arterial hypertension.

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The authors thank veterinarian Daniel Mettler and study nurses Jürgen Rohner, Klaus Maier, and Judith Kaufmann for their assistance with data collection and technical help. The authors also thank Lukas E. Bruegger and Guido Beldi for their help with the instrumentation of the animals and Jeannie Wurz for careful editing of the manuscript.

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Lung recruitment; pulmonary arterial hypertension; splanchnic perfusion

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