More than Foam

It is important to stress here that, according to extensive experimental evidence, collapse and flooding are not mutually exclusive. In fact, it is very likely that the collapse of lung units favors plasma transudation from the capillaries of collapsed septa. We believe that much of the 'liquid and foam' controversy quoted above could be avoided by adopting a straightforward definition of recruitment: the aeration of a previously collapsed, flooded or folded unit, enough to promote some gas exchange. A flooded unit can also be recruited, as commonly occurs during partial liquid ventilation, with bubbles of air filling the alveolar space, surrounded by a thick liquid layer. The recruitment achieved at end inspiration may vanish at end expiration, especially when the surfactant properties are impaired or the unit is flooded. Still, this transient aeration maybe enough to increase arterial oxygenation or CO2 elimination.

By accepting this simple definition, two important consequences follow concerning the mechanics of recruitment (now broadly considering a flooded or truly collapsed unit). First, according to the interdependence models of the lung skeleton, the flooding of a central alveolus may attenuate the alveolar wall stress caused by the expansion of surrounding units, but it does not eliminate it. According to the original conception ofinterdependence, the stresses are createdby non uniform expansion and not exclusively by complete atelectasis [21]. Second, the progression of a bubble of air inside a liquid filled airway can still cause a lot of stress, especially at the level of the lining epithelial cells of bronchioles, as demonstrated by studies from Bilek and co-workers [22].

Having arisen from a single group of experiments in dogs, submitted to the peculiar preparation of oleic acid lung injury, the conclusions of the experiments supporting the foam hypothesis contrast with overwhelming evidence coming from studies using sophisticated imaging techniques. Not sharing the so-called limitations of conventional CT, these studies strongly suggest the ubiquitous occurrence of dependent collapse, associated with loss of regional lung volume, in patients with ALI.

For instance, recent investigations using electrical impedance tomography (EIT), a bedside imaging technique representing a much thicker slice of lung tissue (10-15 cm), have corroborated the findings of the CT studies in animal models of lung injury. Briefly, EIT is based on the detection of variations in electrical tissue impedance. As changes in thoracic impedance are linearly related to changes in air volume [23], this tool is very appealing as a monitoring device for mechanical ventilation, where imbalances in ventilation are well known [24]. In a lung lavage model of ALI, pressure-volume and pressure-impedance curves were compared during lung inflation with the constant flow technique [25]. The pressure-volume and the pressure-impedance curves were significantlycorrelated (r2=0.76; p<.005). There was an identifiable lower inflection point (LIP) in both curves for the nine pigs studied. The LIP of the pressure-impedance curve was within 2 cmH2O of the LIP of the pressure-volume curve. By defining gravity-oriented regions of interest on the EIT images, it was possible to identify regional lower inflection points of each region of interest. Not surprisingly, the dependent regions showed a higher regional inflection point in the pressure-impedance curve. These findings were compatible with the presence of collapse in the dependent lung region and with an opening pressure gradient of 9 cmH2O across the vertical axis, exactly as predicted by the superimposed pressure theory.

Direct proof of the existence of tidal recruitment and collapse comes also from in vivo microscopy of subpleural alveoli. In normal lungs, this technique has demonstrated that there is little change in the alveolar volume during tidal ventilation [26] despite the large change in overall lung volume. The authors suggested that the recruitment of new units instead of alveolar inflation was the predominant phenomenon taking place during lung expansion. On the contrary, in a surfactant deactivation model of lung injury, a dramatic increase in alveolar size was observed at end inspiration, with partial or total expiratory collapse [27]. This observation is in agreement with the classic propositions of Mead that in non uniformly expanded lungs the effective distending pressure can be much higher than the global transpulmonary pressure, leading to inspiratory overinflation of air spaces neighboring collapsed or flooded alveoli [21].

Corroborating those findings, studies with fluorescent-quenching PO2 probes clearly demonstrated enormous oscillations in PaO2 associated with tidal inflation/deflations in a lung lavage model producing alveolar instability. The temporary occurrence of massive shunt at end-expiration strongly suggested the existence of tidal recruitment/derecruitment. Interestingly, these oscillations in PaO2 decreased with the addition of PEEP [28].

We believe that the skepticism against CT as a tool to diagnose lung collapse and recruitment tends to dissipate as advances in the technique permit scanning of the whole lung at acceptable radiation levels and increased spatial resolution. Recent volumetric scanning of the whole lung, apex-to-diaphragm, have cast light on the concerns expressed above (i.e., that non aerated regions might be displaced on the craniocaudal axis by increments of PEEP, causing a misleading reduction in densities). For instance, Lu and coworkers confirmed a reduction of non aerated tissue after PEEP increments in a quantitative analysis embracing the whole lung [29]. Our own experience with this technique reinforced the latter findings. In a spiral tomographic study of 11 ALI/ARDS patients [30, 31], we observed a dramatic reduction of non aerated tissue in the apex-to-diaphragm CT scans after a stepwise and intensive recruitment maneuver. This reduction was very well correlated with an increase in PaO2, compatible with a reduction in the shunt fraction to less than 10%.

Rouby and coworkers have also demonstrated that the total lung volume of patients with ARDS, assessed by spiral/volumetric CT scan, is severely reduced when compared to normal subjects. This remained so even after PEEP application (10 cmH2O) with substantial reduction in the amount of high-density zones. By considering that the total lung volume assessed by CT encompasses tissue, liquid and air, and that the tissue plus liquid components are usually increased, a profound reduction of FRC must have occurred. These results were in evident opposition to the 'flooding hypothesis' and the experiments with the parenchymal marker technique in oleic-acid induced lung injury, in which the authors reported maintenance of regional FRC.

As an additional finding to these complete volumetric CT studies, two recent investigations have suggested that a craniocaudal gradient is negligible in patients or animal models of ARDS and, therefore, the displacement of fluid densities towards the caudal regions cannot be evoked as an explanation for the density changes caused by PEEP - as observed in single CT slices [32, 33].

Finally, in contrast to the results in dogs, we have recently demonstrated the unequivocal presence of phase-lag between dependent versus non-dependent zones in patients with ARDS or ALI (Fig. 1). As indicated above, the existence of phase-lag along the gravity axis is very suggestive of a true vertical gradient of opening/collapsing pressures, confirming the predictions of the superimposed pressure theory.

In summary, the majority of evidence points to the existence of true air space collapse on the dependent lung regions in ALI/ARDS patients, with a marked loss

Mechanical Ventilator ImagesMechanical Ventilation

Fig. 1. A sequence of dynamic CT scanning obtained in a patient with ARDS. During a slow inflation maneuver at constant flow rate (1 l/min), sequential CT scans (every 2 seconds) in the same thoracic plane were obtained. After splitting the lung area into five regions of interest (ROI), as indicated in the top part of the figure, the average gas/tissue ratio for each ROI was plotted against time. As shown, after suffering a small deflation (suggestive of complete airway blockage), dependent zones start to inflate only after a delay of more than 40 seconds. The delay was proportional to the superimposed pressure gradient.

Fig. 1. A sequence of dynamic CT scanning obtained in a patient with ARDS. During a slow inflation maneuver at constant flow rate (1 l/min), sequential CT scans (every 2 seconds) in the same thoracic plane were obtained. After splitting the lung area into five regions of interest (ROI), as indicated in the top part of the figure, the average gas/tissue ratio for each ROI was plotted against time. As shown, after suffering a small deflation (suggestive of complete airway blockage), dependent zones start to inflate only after a delay of more than 40 seconds. The delay was proportional to the superimposed pressure gradient.

of regional lung volume, as predicted by the superimposed pressure theory. Obviously, some alveolar flooding may also occur, but not as the predominant phenomenon in the clinical setting. In opposition to the 'liquid and foam' hypothesis, we also believe that the eventual presence of some flooding does not simplify the matter and should not attenuate our concerns about VILI. The expected shear stress applied on the terminal airway or among adjacent alveoli with different opening pressures seems to be very high, regardless of whether the alveoli are flooded or truly collapsed.

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