Anesth Analg 2004;98:211-219
© 2004 International Anesthesia Research Society
CRITICAL CARE AND TRAUMA
Ventilation-Perfusion Distribution Related to Different Inspiratory Flow Patterns in Experimental Lung Injury
Rolf Dembinski, MD,
Dietrich Henzler, MD,
Ralf Bensberg,
Berit Prüsse,
Rolf Rossaint, MD, and
Ralf Kuhlen, MD
From the Department of Anesthesiology, University Hospital of the RWTH Aachen, Pauwelsstrasse 30, 52074 Aachen, Germany
Address correspondence and reprint requests to Dr. Rolf Dembinski, Klinik fuer Anaesthesiologie, Universitaetsklinikum der RWTH Aachen, Pauwelsstrasse 30, 52074 Aachen, Germany. Address email to Rolf.Dembinski{at}post.rwth-aachen.de
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Abstract
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In acute lung injury (ALI), controlled mechanical ventilation with decelerating inspiratory flow (
dec) has been suggested to improve oxygenation when compared with constant flow (con) by improving the distribution of ventilation and perfusion (A/
). We performed the present study to test this hypothesis in an animal model of ALI. Furthermore, the effects of combined decelerating and constant flow (deco) were evaluated. Thus, 18 pigs with experimental ALI were randomized to receive mechanical ventilation with either con, dec or a fixed combination of both flow wave forms (deco) at the same tidal volume and positive end-expiratory pressure level for 6 h. Hemodynamics, gas exchange, and A/ distribution were determined. The results revealed an improvement of oxygenation resulting from a decrease of pulmonary shunt within each group (P < 0.05). However, blood flow to lung areas with a normal A/ distribution increased only during ventilation with con (P < 0.05). Accordingly, PaO2 was higher with con than with dec and deco (P < 0.05). We conclude that contrary to the hypothesis, con provides a more favorable A/ distribution, and hence better oxygenation, when compared with dec and deco in this model of ALI.
IMPLICATIONS: In acute lung injury, mechanical ventilation with decelerating flow has been suggested to improve ventilation-perfusion distribution when compared with constant flow. We tested this hypothesis in an animal model. Contrary to the hypothesis, we found a more favorable ventilation-perfusion distribution during constant flow when compared with decelerating flow.
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Introduction
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In acute lung injury (ALI), the efficiency of mechanical ventilation to provide adequate pulmonary gas exchange depends mainly on the homogeneity of alveolar ventilation distribution in lung areas with different alveolar opening pressures, thereby determining the ratio of ventilation and perfusion (A/). According to a mathematical lung model, decelerating inspiratory flow (dec) has been suggested to provide a more uniform distribution of inspired gas when compared with constant inspiratory flow (con) (1). These assumptions were confirmed by Abraham and Yoshihara (2) in a clinical study comparing volume-controlled mechanical ventilation (VCV) with con and pressure-controlled mechanical ventilation (PCV) with dec at equal tidal volumes (VT) in patients with ALI. The authors demonstrated that changing from con to dec may be associated with increased oxygenation. In contrast, other clinical trials revealed a more homogeneous gas distribution but failed to prove an increase of oxygenation from dec in ALI (3–8). However, previous studies evaluated hemodynamics and conventional gas exchange but did not determine changes of A/ distribution. Furthermore, most of them revealed short-term effects of 30–60 min of experimental intervention (3,5–8). Thus, the potential benefits of PCV with dec in ALI are still under debate (9). In particular, prolonged effects of different flow patterns on A/ distribution in ALI remain unclear.
This study was performed to compare A/ distribution in experimental ALI in relation to con during VCV, dec during PCV and a fixed combination of both flow patterns (deco) provided by volume-assured pressure support (VAPS), a dual mode where pressure-controlled inspiration with dec may be supplemented con to ensure a preset VT (10). We hypothesized dec provides a more favorable A/ distribution when compared con. Consequently, we suggest that a certain portion of dec during VAPS may also have beneficial effects on A/ distribution.
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Methods
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Animal Preparation
The experimental protocol was approved by the appropriate governmental institution and the study was performed according to the Helsinki convention guidelines for the use and care of laboratory animals.
A total of 18 pigs weighing 32 ± 4 kg (mean ± SD) were anesthetized with propofol, followed by intubation and supine positioning. Anesthesia was maintained with continuous infusion of propofol and remifentanil. Animals were ventilated in a volume-controlled mode (Servo 300 A Ventilator; Siemens Elema, Lund, Sweden) with a VT of 8 mL/kg, a respiratory rate (RR) of 30 breaths/min, an inspiratory:expiratory time ratio of 1:1, and an external positive end-expiratory pressure (PEEP) of 5 cm H2O. Femoral vessels were cannulated for insertion of an arterial catheter and a right heart catheter. A transurethral bladder catheter was inserted to measure urine production.
Data Acquisition
Peak inspiratory flow (peak), peak airway pressure (Ppeak), mean airway pressure (Pmean), and esophageal pressure were measured continuously using the Bicore pulmonary monitor (Bicore CP-100; Irvine, CA). Furthermore, total PEEP was calculated as the sum of measured intrinsic and external PEEP. Heart rate, central venous pressure (CVP), mean pulmonary artery pressure (MPAP), pulmonary capillary wedge pressure (PCWP), mean arterial blood pressure (MAP), and cardiac output (CO) were recorded (AS/3 Compact; Datex-Ohmeda, Achim, Germany). Body temperature was determined by measuring blood temperature using the right heart catheter. Blood samples were collected simultaneously in duplicate and analysis of arterial and mixed venous blood gases (PO2, PCO2), hemoglobin, and oxygen saturation was performed immediately (ABL 510 and OSM 3; Radiometer, Copenhagen, Denmark). Oxygen delivery (DO2) and consumption (o2) were determined using standard formulas. Blood gas data are presented as the mean of each measurement taken in duplicate.
A/ distributions were analyzed using the multiple inert gas elimination technique (MIGET) as described previously (11). Briefly, two blood samples were taken to determine blood gas coefficients for 6 inert gases (sulfur hexafluoride, ethane, cyclopropane, enflurane, ether, and acetone) in duplicate for each animal. Then, 45 min before the first blood sampling for A/ calculation an isotonic saline solution equilibrated with these 6 inert gases was infused into a peripheral vein at a constant rate of 4 mL/min. Samples of arterial and mixed venous blood and mixed expired gas were collected simultaneously at each study point during several respiratory cycles using glass syringes (Popper & Sons, Hannover, Germany) and analyzed immediately by gas chromatography (GC 14 B; Shimadzu, Duisburg, Germany) with Porapak T packed columns (Agilent Technologies, Waldbronn, Germany). Sulfur hexafluoride was examined by Electron Capture Detector whereas the other 5 gases were examined by flame ionization detector. The expiratory tubing and the mixing box for the expired gas samples were heated to avoid a loss of the more soluble gases in condensed vapor. All samples were taken in duplicate. For each inert gas, retention (the ratio of the gas concentration in arterial to that in mixed venous blood) and excretion (the ratio of the gas concentration in expired gas to that in mixed venous blood) were calculated and A/ distributions were estimated using the individual blood gas coefficients of each animal. The duplicate samples were processed separately resulting in two A/ distributions for each condition investigated in this study. The presented data are the mean values of A/ distributions taken in duplicate. Shunt (S/T) was defined as the fraction of total pulmonary blood flow perfusing unventilated alveoli (A/ <0.005). Low A/ regions were defined as those with A/ ratios >0.005 and <0.1, normal A/ regions as those with A/ ratios >0.1 and <10, and high A/ regions as those with A/ ratios >10 and <100. Data for perfusion distribution are presented as percentage of total pulmonary blood flow and expressed as low, normal, and high. Data for ventilation distribution are presented as percentage of total minute ventilation and expressed normal and high. Dead space ventilation (D/T) was defined as the fraction of gas entering unperfused lung units (A/ >100). The position of the distributions was also described by the mean A/ ratio for perfusion and ventilation (mean , meanA) and their dispersion by the log standard deviation of both perfusion (log SD ) and ventilation (log SD A). Quality control was performed by calculating the residual sum of squares (RSS) between the measured and calculated A/ distributions and the differences between predicted and measured PaO2 based on perfusion distribution.
Experimental Protocol
During the experiments, adequate hydration was provided by the infusion of a balanced electrolyte solution and hydroxyethyl starch, with the aim of maintaining CVP, PCWP, and urine production unchanged. A warming cover was used to maintain body temperature at 37°C. Before the baseline measurements, the absence of spontaneous breathing activity was confirmed by the measurement of esophageal pressures and the external PEEP was set to achieve a total PEEP of 5 cm H2O. After baseline measurements, ALI was induced by surfactant depletion by means of repetitive lung lavage, as previously described (11). The experimental protocol was started when a PaO2 <100 mm Hg was achieved for >1 h with a RR set to achieve a PaCO2 <60 mm Hg. Subsequently, a new measurement was performed and animals were randomized to VCV with con, PCV with dec, or VAPS with deco using sealed envelopes with treatment assignment. In each group ventilation was performed with a VT of 8 mL/kg, a total PEEP of 8 cm H2O, an I:E ratio of 1:1, and a RR set to achieve a PaCO2 <60 mm Hg. During VAPS, each respiratory cycle was performed dec with 2/3 of the pressure amplitude required to achieve a VT of 8 mL/kg. Total VT of 8 mL/kg was then completed with supplemental VCV using con (Tbird VSO2; Bird Products Corporation, Palm Springs, CA). The different flow patterns are demonstrated schematically in flow time curves (Fig. 1). All measurements were performed after 2, 4, and 6 h. At the end of the experiments, animals were killed with IV potassium chloride in deep sedation.
Statistical Analyses
All values are expressed as means ± SD. Variables were analyzed using NCSS (NCSS Statistical Software, Kaysville, UT) by two-way analysis of variance for repeated measures to compare values after 2, 4, and 6 h with ALI values within each group and corresponding values between the groups. The Student-Newman-Keuls test for all pairwise comparisons was performed when analysis of variance revealed significant results. P values < 0.05 were considered significant. Baseline values were controlled to exclude major cardiopulmonary dysfunction before the induction of experimental ALI. Therefore, baseline values were not included in statistical analysis.
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Results
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All animals survived the entire study period. Examination of all animals by a veterinary surgeon before the study confirmed the absence of any sign of infection or pulmonary disease. Induction of ALI resulted in a higher MPAP in animals randomized to deco when compared with those randomized to con (P < 0.05). In all animals, a mean of 9 ± 3 lavages had to be performed to obtain a stable ALI with a decrease of PaO2 from 524 ± 18 mm Hg to 71 ± 16 mm Hg. Blood temperature was maintained at 37.4 ± 0.9°C during the experiment. A mean of 16 ± 6 mL · kg-1 · h-1 of a balanced electrolyte solution and 5 ± 1 mL · kg-1 · h-1 hydroxyethyl starch was administered for adequate hydration without differences between the groups. Mean urine production was 6.7 ± 2.6 mL · kg-1 · h-1.
Ventilator settings and respiratory mechanics are demonstrated in Table 1. peak increased during ventilation with dec and was higher than in the other two groups (P < 0.05). Furthermore, Pmean increased in all groups (P < 0.05) but was highest during dec (P < 0.05). After 6 h, Ppeak was higher with deco than with con.
Hemodynamics and gas exchange variables are summarized in Table 2. Experimental procedures resulted in a similar decrease of MAP in all three groups after 4 and 6 h (P < 0.05). MPAP did not change within the groups after induction of ALI. Therefore, the differences in MPAP between the con group and the deco group remained statistically demonstrable over the entire study period (P < 0.05). Other hemodynamic variables remained unchanged.
Although PaCO2 remained unchanged, PaO2 increased significantly within each group (P < 0.05). With con, this improvement was significantly more pronounced compared with dec or deco (P < 0.05). Figure 2 shows individual PaO2 values of all animals during the experiment.
MIGET data are presented in Table 3. The quality of the MIGET data was confirmed by a RSS <5.35 in 86% and <10.65 in 98% of the experimental runs (12). The mean difference between predicted and measured PaO2 was 18 ± 51 mm Hg. S/T decreased within each group (P < 0.05), whereas normal increased only during con (P < 0.05). In contrastdec resulted in small amounts of high. Ventilation distribution remained unchanged during con and deco. During dec D/T decreased and high increased (P < 0.05), whereas normal remained unchanged. No differences were found for low, mean , mean A, log SD , or log SD A.
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Discussion
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The aim of this study was to evaluate the effects of inspiratory flow patterns on A/ distribution in ALI. In particular, it was hypothesized that PCV with dec may improve gas exchange in comparison with VCV with con. Using VAPS the combination dec and con was performed in a third group to investigate whether dec may likewise provide beneficial effects on gas exchange in combination with con. However, the results were quite unexpected. Most important, con resulted in a better gas exchange compared with dec and deco as a result of a more pronounced improvement of perfusion distribution towards normal A/ regions.
In ALI, gas exchange is impaired by a mismatching of ventilation and perfusion, resulting in severe hypoxemia refractory to high inspiratory oxygen fraction (13). The formation of atelectatic lung areas causes a high amount of pulmonary shunt, thereby decreasing PaO2. Gas exchange is further impaired by the presence of lung areas with low and high A/ ratios and D/T. The nonhomogeneous A/ distribution is mainly caused by the differences in the compliance of the alveolar regions. Therefore, the efficacy of mechanical ventilation to provide adequate gas exchangedepends on the ability to distribute ventilation homogeneously in low compliant and normal compliant lung regions.
The present study was performed in animals with a well established, experimental model of ALI to provide a comparable, severe lung injury without possible disadvantages of clinical trials such as differences in the origin of ALI or other concomitant organ dysfunction. Previously published studies demonstrated that this model of ALI may cause death in animals within 3–4 hours when VCV with a PEEP of 5 cm H2O is performed without other therapeutic interventions (14,15). However, we found that VCV with a PEEP of 10 cm H2O may result in a marked improvement of oxygenation within 2 hours using the same model (16). We therefore increased PEEP after induction of ALI from 5 to 8 cm H2O to provide survival of all animals until the end of the study with a lung injury as severe as possible. Thus, beneficial effects of the increased PEEP level have to be considered in the discussion of the results. However, during the subsequent study period PEEP levels remained the same for all three groups.
Numerous studies have been performed to evaluate different ventilator strategies in ALI. Several have focused on the impact of different flow-wave forms on pulmonary gas exchange. Based on theoretical considerations and clinical trials, PCV with dec has been suggested to improve gas exchange in comparison with VCV with con (1,2). As a possible explanation, PCV has been demonstrated to increase Pmean at lower Ppeak levels, thereby increasing alveolar recruitment (17). These results correspond to the finding that by increasing Pmean, gas exchange improved, regardless of the inspiratory flow-wave form (18,19). Furthermore, it has been shown that similar Pmean levels result in comparable gas exchange during VCV and PCV (20). However, other studies have revealed that with adequate PEEP, the increase of Pmean does not further improve PaO2 but may decrease DO2 because of a decrease of CO (21,22). Thus, a decrease of Ppeak and an increase of Pmean during PCV represents a common finding in several trials but does not always provide improved gas exchange (3–7,23).
In the present study, Pmean increased with dec when compared with con. Nevertheless, PaO2 increased more with con than with dec. As a result of the increase of total PEEP from 5 cm H2O (ALI) to 8 cm H2O (2, 4, and 6 hours) S/T decreased in both groups. However, MIGET revealed that an appropriate increase of perfusion to normal A/ areas is present only with con, whereas pulmonary blood flow distribution dec appears to be more nonhomogeneously with a notable amount of perfusion to low and high A/ regions as well. The presence of high A/ areas during dec may be explained by the decrease of D/T in this group. However, the increase of Pmean during dec should increase D/T and decrease high because of a compression of alveolar vessels, whereas our study showed opposite data. Similar results have been found by Davis et al. (17) in a clinical trial. They revealed a slight reduction of D/T despite higher Pmean when comparing dec to con and speculated that Vdec may prevent alveolar overdistension and augment collateral ventilation. However, collateral ventilation is neglectable in pigs and prevention of alveolar overdistension may prevent an increase of D/T but may not explain its decrease. Other investigators also demonstrated a more favorable gas distribution during dec using computed tomography scans, but in these studies Pmean was equal to con (3,8). Thus, as we have no other explanations, we can only speculate on reasons for the decrease of D/T during dec. Obviously, these changes are not accompanied by positive effects on oxygenation. Thus, as suggested by other investigators (21,22), it appears that the increase of oxygenation using PEEP cannot be further improved by PCV with dec. Our data demonstrate that gas exchange in ALI depends not only on the amount of Pmean and PEEP but also on the concomitant inspiratory flow level and its wave form. Whereas peak is higher during ventilation with dec than during ventilation with con, end-inspiratory flow is by definition higher during con than during dec. Thus, according to our results, it can be speculated that after a recruitment phase of atelectatic lung areas during inspiration a certain amount of end-inspiratory flow as with con is necessary to provide adequate ventilation in these areas.
Hemodynamics in the present study are characterized by a decrease of MAP during ventilation with con and dec. Furthermore, it is noteworthy that the improvement in gas exchange did not result in an appropriate increase of DO2 in any of the three groups over time. This corresponds to a slight, although not statistically significant, decrease in CO over time in each group. This finding correlates well with the results of several clinical studies demonstrating a reduction of CO in the presence of increased intrathoracic pressure during mechanical ventilation with PEEP (24,25). However, with the data revealed in the present study it cannot be differentiated between the effects of increased PEEP alone and other possible mechanisms such as the additional increase of Pmean resulting from dec.
In 1992 Amato et al. (10) presented VAPS as a ventilation mode designed to combine the advantages of pressure-supported spontaneous breathing with VCV. In a clinical trial, they demonstrated that VAPS might improve respiratory mechanics in comparison with pressure support ventilation. In the present study, VAPS was used to provide the combination of different flow-wave forms (deco) without using it as a spontaneous breathing mode. We hypothesized beneficial effects on gas exchange in comparison with con because of dec during the beginning of inspiration. However, according to the unexpected data for con and dec the results revealed that, concerning gas exchange, con was superior to deco. Although there is no statistical difference in PaO2 or shunt between dec and deco, a slightly improved gas exchange deco was noted when compared with dec after 6 hours. Based on this observation, it might be speculated that, in contrast to our hypothesis, con provides beneficial effects for oxygenation even in combination with dec and not vice versa. Probably, the differences between deco and con might have revealed statistical significance with a different ratio of dec and con during VAPS. Thus, according to the results for con and dec it can be hypothesized that shortening the phase of dec for the benefit of con may result in better gas exchange compared with dec alone.
Hemodynamics during deco were comparable to those during con and dec. Indeed, statistical analysis revealed an increased MPAP in comparison with con after induction of ALI. However, as this difference remained unchanged during the entire study period we exclude a major impact on gas exchange variables obtained with deco.
This is the first study comparing the effects of different inspiratory flow patterns on A/ distribution in ALI. The results do not agree with previous clinical findings demonstrating improved gas exchange resulting from PCV with dec (2). In contrast, a significant improvement in gas exchange was found for VCV with con. In accordance with most recent results (3,8), ventilation was more favorable distributed during PCV, as can be concluded by the decrease D/T during PCV. However, our results suggest that the more marked improvement of normal A/ areas during VCV has a more important impact on oxygenation in this experimental setting.
In conclusion, the present study revealed that, in experimental ALI, mechanical ventilation with con is related to better oxygenation than dec despite lower Pmean during con. In a recently published meta-analysis of trials testing low VT ventilation in ALI, it has been pointed out that high levels of Pmean are associated with an increasing mortality rate (26). With this in mind, ventilation with con may have twofold beneficial effects by improving oxygenation and reducing high Pmean. Ventilation with VAPS had no beneficial effects on gas exchange in this study but is also associated with a lower Pmean when compared with dec. Furthermore, VAPS has the possible advantage of preserved spontaneous breathing activity. In our opinion, VAPS should be therefore re-evaluated in a clinical study using the possible advantage of spontaneous breathing activity in combination with con, thereby providing optimal ventilator-patient synchronicity, gas exchange and airway pressure.
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Acknowledgments
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Supported, in part, by a research grant from Viasys Healthcare, Conshohocken, Pennsylvania.
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Footnotes
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Presented, in part, at the 15th Congress of the European Society of Intensive Care Medicine in Barcelona, Spain, 2002.
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Accepted for publication July 25, 2003.
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Abstract
Introduction
