The salient findings of this study can be summarized as follows: (1) FRC was higher in semi-Fowler's position but remained relatively unchanged among all horizontal positions, regardless of orientation and despite changes of regional aeration caused by asymmetrical extrapulmonary forces. (2) Applying PEEP10 consistently increased FRC and attenuated the negative values of end-expiratory PTP observed at PEEP1 in all positions, regardless of PLEF and its lung volume-compressing effects. (3) Both FRC and PTP were insensitive to variations of regional mechanics caused by horizontal position changes, even in this highly nonsymmetrical mechanical setting of unilateral PLEF.
Semi-Fowler's position vs. FRC
Lung volume is normally affected by position change, especially when subjects assume recumbency from the upright position [6]. Additionally, the global lung environment (pressure gradients, airway closure patterns, perfusion, and ventilation) may be influenced by positional variation [13]. In our study, all the horizontal positions tested showed similar values of global FRC, despite visually impressive redistribution of the aerated gas (Figure 1). Conversely, semi-Fowler's position countered the lung volume reduction associated with recumbency in all tested conditions, presumably by shifting the abdominal content caudally, relieving pressure against the diaphragm.
PEEP10 and PLEF interactions
As expected from a previous report [5], PEEP10 restored FRC to its non-PLEF baseline in all positions. PLEF generates a pleural hydrostatic pressure and reduces the FRC in all positions; however, our radiographic evidence and previous work support the idea that the lung progressively is lifted above the level of pleural fluid during tidal inflation, and asymmetrical chest expansion redistributes PLEF as airway pressure rises [5]. Applying PEEP10 may attenuate this exaggerated tidal inflation-deflation and/or recruitment and de-recruitment cycle by increasing the baseline airway pressure and lung volume.
Positioning and transpulmonary pressure
As opposed to spontaneous breathing, positive-pressure ventilation increases esophageal pressure (pleural pressure) during the entire inflation phase of the tidal cycle. Calculations of end-expiratory PTP when PEEP1 is applied will always tend to result in negative values. Our data revealed negative end-expiratory PTP in all positions and conditions with PEEP1 (Figure 3); however, whether these negative values actually represent lung collapse is unclear. PTP uses esophageal pressure as an estimate of global pleural pressure, and the esophageal balloon is influenced by anatomic factors that are not present elsewhere in the thorax. Thus, a negative calculated PTP may relate to actual collapse of lung units, to simple reduction of air volume, or to regional early airway closure with subsequent air trapping. In the latter setting, true regional alveolar pressure actually exceeds that measured from the airway opening at end-exhalation. Such regional gas trapping has been shown to occur in obese normal humans who breathe in the horizontal supine position without PEEP [14]. Whatever the actual explanation might be, in horizontal positions, the driving pressures calculated from airway pressures alone (as traditionally done) have the potential to mislead [4].
Based upon our data for PEEP1 and non-PLEF conditions, we believe that while regional ‘lung collapse’ might be a plausible (if not unique) interpretation for negative end-expiratory PTP in the supine position, tissue collapse is less likely to explain negative PTP for the prone and semi-Fowler's positions in the same setting. The coexistence of negative PTP and aerated lung at end-expiration also points toward the local characteristics of the pressures sensed by the esophageal catheter. The absolute PES may not represent overall pleural pressure, but it remains the most practical tool available to estimate pleural pressure in the clinical setting [15].
Unilateral PLEF and lateral positioning
In designing this experiment, we questioned whether any benefit predictably accrues to adopting a specific lateral position when right or left PLEF is present. Surprisingly, our data showed little difference among overall FRC values in any horizontal position, regardless of the laterality of PLEF. Physically, there are four main vectors of compressive pressure influencing the lower lung when adopting lateral position: (1) abdominal content shift, (2) restriction of the dependent chest wall due to its contact with the bed, (3) gravitational shift of the mediastinal contents, and (4) weight of the contralateral hemithorax (lung ± pleural liquid). This rationale encouraged us to expect important differences between FRC and PTP with changes of lateral position. However, our data showed inconsequential differences between right and left lateral positions, whatever the PLEF laterality. The unchanging global FRC strongly implicates the interdependence of forces across the various extrapulmonary compartments that envelop the lung. Apparently, in this experimental animal model, there is a balance between the upper ‘decompression’ and lower ‘compression’ of the lungs, which makes the laterality of the PLEF irrelevant when adopting different horizontal positions.
Transpulmonary pressure and collapse
Either inflating the lung with positive pressure during tidal breathing or adding 10 cm H2O PEEP caused the calculated PTP to convert from negative to neutral or positive values in all horizontal positions, with or without PLEF. Such conversion suggests the reopening of alveoli within the vicinity of the esophageal balloon and has been advocated as a marker by which to determine the PEEP needed to maintain recruitment and avoid regional tissue collapse in ARDS [3]. When supine, the vulnerability of PES to compression under mediastinal weight (relieved by lung expansion at PEEP10) might offer an alternative explanation of PTP behavior in response to PEEP that is less tightly linked or even uncoupled from airspace closure [14]. While ‘cardiac weight artifact’ certainly has plausibility for that supine posture, this possibility seems less likely to apply in lateral and prone positions [16]. Assuming that PES reflects pleural pressure accurately, an alternative explanation could be that gas trapping occurs in horizontal positions at PEEP1 [12]. When gas trapping occurs, true alveolar pressure could be substantially higher than the 1 cm H2O airway pressure recorded through the central airway at end-exhalation (causing artifactually reduced PTP). Reversal of air trapping by inflation or by PEEP would raise measured PTP into the observed positive range. Again, because calculated end-expiratory PTP was negative in all positions (including prone and Fowler), this potential explanation, though attractive for the supine position, seems less compelling for the other positions tested.
Transpulmonary pressure and FRC
Data are just not available regarding how well our only noninvasive estimator of PTP tracks FRC when the lungs are asymmetrically affected. Our data demonstrate a discrepancy between PTP calculations and global FRC changes in the setting of unilateral mechanical asymmetry. While negative end-expiratory PTP was observed in all positions and conditions with PEEP1, FRC values in semi-Fowler's position were significantly higher when compared with those in horizontal positions. As indicated by these results, as well as by those reported in our previous experience with intra-abdominal hypertension (IAH) [4], the insensitivity of PTP to changes on global FRC suggests the regional nature of PES measurements. Whether PES may be more accurate in reflecting regional changes on aeration distribution within the areas more vulnerable to collapse (e.g., the dependent lung units in proximity to the balloon) is unclear. Regional distribution changes of lung aeration and its correlation with PTP merit further investigation.
Limitations
As with all models, strong reservation is appropriate before translating these results to analogous clinical situations. While we believe that the principles elucidated here are qualitatively valid, the chest wall contours and lung compliance of pigs clearly differ from those of diseased humans, so that the magnitudes of the observed effects of position and PEEP may not tightly correspond. We studied a single tidal volume and two discreet levels of PEEP; quantitative effects would be influenced by the parameters chosen. Additionally, we cannot be sure that full recruitment was accomplished in every position, and it is clear that atelectasis of dependent lung units recurs quickly - even after a successful maneuver. The recruitment maneuvers performed in our study were based on our previous experience in comparing different recruitment maneuvers in three experimental models of acute lung injury [11]. Finally, interactive behaviors of the lung and chest wall are almost certain to be modified strongly by spontaneous breathing efforts. Although global measures of lung behavior (FRC and PTP) were less affected by horizontal positional change, this insensitivity does not imply that positional changes are inconsequential for gas exchange or breathing effort. Indeed, regional alterations visualized by CT suggest that customary global measures of bedside mechanics need to be complemented by techniques that are sensitive to the underlying components.