Quantitative imaging of alveolar recruitment with hyperpolarized gas MRI during mechanical ventilation

Abstract

The aim of this study was to assess the utility of (3)He MRI to noninvasively probe the effects of positive end-expiratory pressure (PEEP) maneuvers on alveolar recruitment and atelectasis buildup in mechanically ventilated animals. Sprague-Dawley rats (n = 13) were anesthetized, intubated, and ventilated in the supine position ((4)He-to-O(2) ratio: 4:1; tidal volume: 10 ml/kg, 60 breaths/min, and inspiration-to-expiration ratio: 1:2). Recruitment maneuvers consisted of either a stepwise increase of PEEP to 9 cmH(2)O and back to zero end-expiratory pressure or alternating between these two PEEP levels. Diffusion MRI was performed to image (3)He apparent diffusion coefficient (ADC) maps in the middle coronal slices of lungs (n = 10). ADC was measured immediately before and after two recruitment maneuvers, which were separated from each other with a wait period (8-44 min). We detected a statistically significant decrease in mean ADC after each recruitment maneuver. The relative ADC change was -21.2 ± 4.1 % after the first maneuver and -9.7 ± 5.8 % after the second maneuver. A significant relative increase in mean ADC was observed over the wait period between the two recruitment maneuvers. The extent of this ADC buildup was time dependent, as it was significantly related to the duration of the wait period. The two postrecruitment ADC measurements were similar, suggesting that the lungs returned to the same state after the recruitment maneuvers were applied. No significant intrasubject differences in ADC were observed between the corresponding PEEP levels in two rats that underwent three repeat maneuvers. Airway pressure tracings were recorded in separate rats undergoing one PEEP maneuver (n = 3) and showed a significant relative difference in peak inspiratory pressure between pre- and poststates. These observations support the hypothesis of redistribution of alveolar gas due to recruitment of collapsed alveoli in presence of atelectasis, which was also supported by the decrease in peak inspiratory pressure after recruitment maneuvers.

Fig. 1.

A: schematic diagram of the ventilation protocol for end-inspiratory apparent diffusion coefficient (ADC) imaging in rat lungs with hyperpolarized ³He MRI. b values, diffusion gradient factors. B: schematic diagram of the two positive end-expiratory pressure (PEEP) recruitment maneuvers. The thick line segments represent ADC acquisitions. C: overall experimental protocol comprised of two recruitment maneuvers sandwiched between two pairs of ADC measurements and separated by a wait time period, as shown in Table 1.

Fig. 2.

Time history of peak inspiratory pressure (PIP) for three rats that were not imaged with hyperpolarized ³He MRI. These animals underwent the stepwise recruitment maneuver, shown in Fig. 1B, left. All three rats showed a significant change in PIP before and after application of the PEEP maneuver; a similar trend was also observed with the ³He ADC results.

Fig. 3.

Maps of ADC distribution (cm²/s) in the middle coronal slice of four representation rats that underwent the study protocol shown in Fig. 1C. The ADC map in each column corresponds to each of the four time points in the recruitment maneuver study.

Fig. 4.

Frequency distribution histograms corresponding to the ADC maps shown in Fig. 3 for the four representative rats. Also overlaid on the histograms are the best β fits for qualitative assessment of the distribution functions.

Fig. 5.

Summary of ADC measurement results described in terms of the mean (A), SD (B), and skewness (C) of the ADC distribution in each imaged slices reported for each of the four time points according to Table 1. D–F: relative changes in these three parameters corresponding to the four pairwise comparisons shown in Table 2. The edges of each box correspond to the lower and upper quartile values, and the center-dotted circle represents the median ADC of each group. The whiskers extend from each end of the box to the most extreme values within 1.5 times the interquartile range. Data points in each group with values beyond the ends of the whiskers are considered outliers and are displayed as open circles.

Fig. 6.

A: maintenance of rat 6 ventilated at zero end-expiratory pressure (ZEEP) in the supine position for >100 min after a recruitment maneuver resulted in a slowly increasing ADC trend as evidenced by intermediate measurements. ADC maps corresponding to some of the ZEEP states are shown for reference. The error bars represent the SD of the ADC distribution in the imaged slice. The areas shown by arrows depict localized changes in the ADC value. B: end-inspiratory ADC measurements during the stepwise PEEP maneuvers in rat 2 showed good repeatability after the initial recruitment maneuver. The ADC measurements at the final ZEEP levels of third and fourth cycle are missing due to depleted hyperpolarized ³He gas in the reservoir.

Fig. 7.

A: linear correlation of the relative change in mean ADC as a function of wait time showed a steady increase in the ADC value in all the imaged rats. One data point was determined as an outlier based on the 1.5 quartile and was excluded from the correlation analysis. B: linear correlation of the change in ADC skewness as a function of wait time showed a steady shift of the distribution toward the lower values in all the imaged rats. The dotted lines represent the 95% confidence intervals in both A and B.

Fig. 8.

A simple model of alveolar collapse and recruitment showing residual V_i⁰ and fractional δV_i⁰ volumes for the ith representative alveolar unit. Postatelectasis states are shown as V_i¹ and δV_i¹, respectively. A collapsed airway unit is described by both V_i¹ → 0 and δV_i¹ → 0, with nominal boundary conditions: FRC^s ≈ Σ V_i^s and V_T^s ≈ Σδ V_i^s, where FRC is functional residual capacity, V_T is tidal volume, and s is the state of interest. The underlying assumptions are V_T⁰ = V_T¹ and V_i⁰ = V_i¹ for aerated alveoli. When a fraction of alveoli is collapsed, for a fixed V_T the patent airspaces undergo a proportional increase in size due to the redistribution of inspired gas. Traction forces due to alveolar interdependence may also cause airspace enlargement in the presence of atelectasis.