Effect of prone position on regional shunt, aeration, and perfusion in experimental acute lung injury

Abstract

Rationale: The prone position is used to improve gas exchange in patients with acute respiratory distress syndrome. However, the regional mechanism by which the prone position improves gas exchange in acutely injured lungs is still incompletely defined.

Methods: We used positron emission tomography imaging of [(13)N]nitrogen to assess the regional distribution of pulmonary shunt, aeration, perfusion, and ventilation in seven surfactant-depleted sheep in supine and prone positions.

Results: In the supine position, the dorsal lung regions had a high shunt fraction, high perfusion, and poor aeration. The prone position was associated with an increase in lung gas content and with a more uniform distribution of aeration, as the increase in aeration in dorsal lung regions was not offset by loss of aeration in ventral regions. Consequently, the shunt fraction decreased in dorsal regions in the prone position without a concomitant impairment of gas exchange in ventral regions, thus leading to a significant increase in the fraction of pulmonary perfusion participating in gas exchange. In addition, the vertical distribution of specific alveolar ventilation became more uniform in the prone position. A biphasic relation between regional shunt fraction and gas fraction showed low shunt for values of gas fraction higher than a threshold, and a steep linear increase in shunt for lower values of gas fraction.

Conclusion: In a surfactant-deficient model of lung injury, the prone position improved gas exchange by restoring aeration and decreasing shunt while preserving perfusion in dorsal lung regions, and by making the distribution of ventilation more uniform.

Figure 1.

Protocol schema. *Until Pa_O2 below 100 mm Hg; **Pa_O2 below 200 mm Hg that changed by less than 10% at two consecutive 15-minute intervals. PET = positron emission tomography.

Figure 2.

Tracer kinetics of infused ¹³N₂, measured by PET in the lung field of one animal. After a 3-second intravenous injection of a bolus of ¹³N₂ dissolved in saline solution, PET images were acquired during 60 seconds of apnea (left of vertical dotted line) and 3 minutes of ensuing ventilation (right of vertical dotted line). ¹³N₂ kinetics during apnea shows an early peak in tracer activity (a_peak), corresponding to arrival of the bolus of tracer through the pulmonary circulation, followed by an exponential decrease toward a plateau (a_plat). This decrease in activity is consistent with the presence of shunting units, which do not retain ¹³N₂ during apnea, whereas the plateau reflects the retention of ¹³N₂ in units that are perfused and aerated. Specific alveolar ventilation of perfused units was calculated from the initial slope of the tracer washout curve, obtained after mechanical ventilation was resumed (right of vertical dotted line).

Figure 3.

PET images from one animal in supine and prone positions. Four of the 15 original slices of lung are shown (top to bottom, cranial to caudal). For both positions, images in the first column correspond to the peak of infused ¹³N₂ kinetics (5 seconds < t < 10 seconds) and reflect the regional distribution of perfusion. Note the preferential distribution of perfusion to dorsal regions in both positions, and the more uniform perfusion when prone. Images in the second column correspond to the plateau of infused ¹³N₂ kinetics (40 seconds < t < 60 seconds) and show the regional distribution of perfusion in units that are perfused and aerated. Regions of shunt, which do not retain ¹³N₂ during apnea, can be visualized as regions in which tracer activity is present in the peak apnea images (first column) but absent in the end apnea images (second column). Note the large amount of shunt in dorsal regions, particularly in caudal slices, in the supine position, which is annihilated by turning prone. This is consistent with the regional distribution of gas fraction, measured after equilibration of inhaled ¹³N₂ (third column), which shows restored aeration to dorsal regions and a more uniform aeration in the prone position.

Figure 4.

Topographic distribution of regional lung volume (VL_i, total length of the bars), gas volume (VGAS_i, dark gray portion of the bars), and tissue volume (VTIS_i, light gray portion of the bars) in eight horizontal regions of interest of equal height, in the supine and prone positions. The ratio of the length of the dark gray portion of each bar to the total length of the bar represents the regional gas fraction (FGAS_i), the numeric value of which is reported next to the bar for each region (in this respect it is worth noting that the unit of measure of the x axis does not apply to the gas fraction values). Note the restored aeration to dorsal regions in the prone position. Data represent means and SD.

Figure 5.

Topographic distribution of regional pulmonary perfusion (Q̇_i, total length of the bars) and pulmonary shunt flow (Q̇S_i, dark gray portion of the bars) in the supine and prone positions. Both flows are expressed as a fraction of total perfusion to the imaged lung. The ratio of the length of the dark gray portion of the bar to the total length of the bar represents regional shunt fraction (FS,PET_i), the numeric value of which is reported next to the bars for each region (in this respect it is worth noting that the scale of the x axis does not apply to the shunt fraction values). The light gray portion of the bar represents the fraction of pulmonary perfusion flowing to gas-exchanging units within the region. Note the annihilation of shunt and the preservation of perfusion in dorsal regions in the prone position. Data represent means and SD.

Figure 6.

Plots of regional shunt fraction versus gas fraction for the average values (A), and for the individual values obtained from two animals, with and without biphasic behavior (B and C, respectively). In each panel, data points for each of the eight horizontal regions of interest are shown for the supine position (solid symbols) and for the prone position (open symbols). The data points corresponding to the three most dorsal regions are marked with different symbols (diamonds, triangles, and squares in dorsal-to-ventral direction). (A) The main effect of the prone position was to shift the data points corresponding to the most dorsal regions to a more favorable portion of the FS,PET-versus-FGAS relation. (B and C) The dotted line represents the regression line obtained by fitting the equation FS,PET = 1 – FGAS/F₀ to data points with shunt fraction greater than 0.2 ([B] FS,PET = 1 – FGAS/0.36; [C] FS,PET = 1 – FGAS/0.57).

Figure 7.

Topographic distribution of regional specific alveolar ventilation (sVA_i, alveolar ventilation per unit of gas volume) in the supine and prone positions. Note the more uniform vertical distribution profile of specific ventilation in the prone position. Data represent means and SD.