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The Pulmonary and Systemic Distribution and Elimination of Perflubron From Adult Patients Treated With Partial Liquid Ventilation^*

^* From the Departments of Surgery (Drs. Reickert, Pranicoff, Overbeck, Bartlett, and Hirschl), Radiology (Dr. Kazerooni), and Anesthesia (Dr. Massey), University of Michigan Medical Center, Ann Arbor, MI.

Correspondence to: Ronald B. Hirschl, MD, FCCP, F3970 Mott Children’s Hospital, 1500 E. Medical Center Dr, Ann Arbor, MI 48109-0245; e-mail: rhirschl{at}umich.edu

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Objective: To assess the pulmonary and systemic distribution and elimination of perflubron (C₈F₁₇Br₁; LiquiVent; Alliance Pharmaceutical; San Diego, CA) during and following the period of partial liquid ventilation.

Design: Prospective phase I and II clinical trial.

Setting: Adult surgical ICU.

Patients: Eighteen adult patients (mean ± SEM age, 37.9 ± 3.4 years) with severe respiratory failure, some of whom required extracorporeal life support (72%), and who were managed with partial liquid ventilation with perflubron.

Interventions: Perflubron was administered into the trachea, and gas ventilation of the perfluorocarbon-filled lung (partial liquid ventilation) was then performed. Additional doses were administered daily for from 1 to 7 days, with a median cumulative dose of 31 mL/kg (range, 3 to 60 mL/kg).

Measurements and main results: Patient blood samples were evaluated by gas chromatography for serum perflubron levels. Sequential lateral and anteroposterior radiographs were assessed, using a 5-point rating scale, for the degree of perflubron fill following the final dose. Samples of expired gas were collected, and the rate of loss of perflubron in the expired gas was measured by gas chromatography. Mean serum perflubron levels increased to 0.16 ± 0.05 mg/dL at 24 h following administration of the initial dose. A mean maximum level of 0.26 ± 0.05 mg/dL of perflubron was present in the serum 24 h following the administration of the last dose. This level slowly trended downward to 0.18 ± 0.06 mg/dL over the ensuing 7 days (p = 0.281). Perflubron elimination via expired gas occurred at a mean rate of 9.4 ± 3.0 mL/h at 1 h, and 1.0 ± 0.4 mL/h at 48 h after the last dose (p = 0.012). By radiologic evaluation, perflubron was eliminated from the lungs progressively from 4.2 ± 0.2 at the time of administration of the last dose, to 2.8 ± 0.3 at 4 days later (p < 0.001). Perflubron tended to distribute and remain for longer periods in the dependent regions of the lung when compared to the nondependent regions (96-h perflubron fill score: posterior, 3.8 ± 0.5; anterior, 1.9 ± 0.4; p = 0.004).

Conclusions: Perflubron is eliminated at a maximum rate of 9.4 ± 3.0 mL/h by evaporative loss from the airways and is retained in greater amounts in the dependent lung regions when compared to the nondependent lung regions. There is a low but measurable maximum blood concentration of 0.26 ± 0.05 mg/dL in patients after perflubron administration, which did not decrease significantly after cessation of partial liquid ventilation.

Key Words: partial liquid ventilation • perflubron • respiratory failure

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
In 1966, Clark and Gollan¹ demonstrated the ability to provide adequate gas exchange during spontaneous liquid breathing of perfluorocarbon by the mouse. Since that time, a number of studies have been performed evaluating the ability of perfluoro-carbons to enhance gas exchange and pulmonary function in the setting of lung injury.^{2 3 4 5} Liquid ventilation with perfluorocarbon has been performed, in general, by one of two techniques: (1) total liquid ventilation, in which the lungs are filledwith perfluorocarbon and ventilated with tidal volumes of perfluorocarbon using a liquid ventilator; and (2) partial liquid ventilation (PLV), in which the lungs are filled with perfluorocarbon and then ventilated with gas tidal volumes using a standard gas ventilator.^{6 7 8} For technical reasons, initial clinical application of liquid breathing has been performed using the PLV method.^{9 10 11 12 13}

We initiated phase I and II studies involving PLV in adult patients with severe respiratory failure, including those requiring extracorporeal life support (ECLS). Our initial experience with PLV in this patient population was encouraging, with improvement in gas exchange and pulmonary function demonstrated over the ensuing 72 h after the initiation of PLV.⁹ As part of these initial studies, we evaluated data with regard to the pulmonary distribution of perflubron, serum perflubron levels, and elimination of perflubron by expiration. We were specifically interested in the rate of evaporation of pulmonary perflubron following intratracheal administration and the serum levels generated during PLV. Therefore, in this study, we assessed the amount and distribution of perflubron in the lungs based on chest radiography, the volume of perflubron vapor in the expired gas, and serum perflubron levels during and following the period of PLV.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
This was a noncontrolled, phase I and II experimental study. The sample frame for this study included patients > 18 years old with severe respiratory failure. Initial patients required ECLS prior to PLV; however, several patients’ conditions did not deteriorate to the point of requiring ECLS and they were supported with PLV without ECLS. Indications for ECLS at our institution include physiologic shunt > 30%, severe barotrauma, and/or inability to ventilate despite optimal treatment.^{14 15} These criteria select a patient population who, without use of ECLS, has a predicted 10 to 20% survival in our institution. The full adult ECLS protocol is described in detail elsewhere.^{14 15} Patients who had partial response to optimal respiratory care but who still had marginal oxygenation and who were not believed to be immediate candidates for ECLS were also offered PLV. Eighteen adult patients (mean ± SEM age, 37.9 ± 3.4 years) met these criteria for PLV and were managed with PLV (Table 1 ). PLV was initiated from 1 to 11 days following institution of extracorporeal support, when ECLS was needed (13 of 18 patients [72%]).

Outcome Measures
In eight patients, daily anteroposterior and lateral chest radiographs were assessed for the degree of perflubron filling at the time of perflubron administration and for the next 6 days following administration of the final dose of perflubron. Each radiograph was evaluated by two radiologists (E.A.K. and P.C.) and by two critical-care physicians (R.B.H. and T.P.). Each lung was evaluated separately on the anteroposterior radiograph; in the lateral image, the lung was divided in three sections: anterior, middle, and posterior. Each section was scored with the ranking described. By group consensus, the relative filling of the anterior, middle, and posterior sections of the lungs on lateral chest radiograph and the left and right lung fields on the anteroposterior chest radiograph was graded using the following scoring system: grade 1, minimal perflubron present; grade 2, more than minimal to one-third full; grade 3, more than one-third full to two-thirds full; grade 4, more than two-thirds full to nearly full; and grade 5, more than full.

Samples of expired gas from the outflow of the ventilator circuit (model 7200; Puritan Bennett; San Diego, CA) circuit were collected in 12 patients via a needle sample port placed at the connection with the endotracheal tube and collected into sterile, plain vials (Vacutainer; Becton Dickinson; Franklin Lakes, NJ). Samples were obtained at 0, 1, 2, 4, 8, 16, and 24 h after initiation of PLV and then daily after administration of the final dose of perflubron until patient death or cessation of mechanical ventilation. The gas in the samples was analyzed by gas chromatography (model 3600; Varian Medical Systems; Palo Alto, CA) equipped with a 15M, 0.53-mm inner-diameter column (model RTX-1; Restek; Bellefonte, PA) and flame ionization detector. A standard curve using perflubron was developed that allowed determination of the volume percent (milliliters per deciliter) of perflubron vapor in the expired gas. This volume was converted to milliliters of liquid perflubron lost per hour with the following formula:

where PFOB is perflubron volume. The expired volume of perflubron was corrected both for the initial volume of gas present in the vials prior to sample collection and to standard temperature and pressure, dry, using the core body temperature and atmospheric pressure at the time of sample collection.

Serum samples of 1 mL in volume were collected at 0, 1, 2, 4, 8, and 24 h after initiation of PLV and daily after discontinuation of perflubron dosing in 13 patients. Samples were collected in sterile vials (Vacutainer) with 0.048-mL ethylenediamine-tetraacetic acid and frozen within 2 h of collection. The serum was analyzed by head space auto sampling and gas chromatography. Samples were prepared by transferring a 250-µL aliquot of whole blood to a 22-mL borosilicate head space vial and adding an isopropyl alcohol solution containing perfluorononyl bromide as an internal standard. A head space auto sampling system (model 7000/7500; Tekmar; Cincinnati, OH) was used to bring the mixture to equilibrium and transfer a 1-mL head space sample to a gas chromagraph (model 5890; Hewlett-Packard; Wilmington, DE) equipped with a DB-1 capillary column (J & W Scientific; Folsom, CA) capillary column and electron capture detector. Preparing calibration standards in whole swine blood created calibration curves. Swine blood was shown to be an equivalent matrix to human blood for this assay. The lower limit of quantitation for perflubron is approximately 0.25 µg/mL in whole blood. The method was validated for perflubron from approximately 0.25 µg/mL to approximately 100,000 µg/mL.

Data Analysis
Expired gas perflubron vapor and serum perflubron data were averaged at 1, 2, 4, 8, and 16 h (expired gas only) and 24 h after initiation of PLV. Mean data from each patient at the time of administration and daily following the last fill were also determined. The perflubron-fill radiologic scores for each region of the lung at each time point were averaged. Statistical comparisons were performed with repeated-measures analysis of variance (ANOVA) with post hoc comparisons performed within group using a Dunnett’s t test for the expired gas and serum perflubron data. All data are presented as mean ± SEM. Only data points with two or more values are included in the analysis.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Serum concentrations of perflubron increased over the first 24 h after dosing to 0.16 ± 0.05 mg/dL (n = 13). There was a steady increase in blood concentrations over the first 24 h of filling (p = 0.001 by repeated measures ANOVA; p = 0.017 when the 1-h and 24-h serum levels are compared by paired t test; Fig 1 ). The mean blood concentration of perflubron on the day after the last dose was 0.26 ± 0.05 mg/dL (n = 13). The mean blood concentration then followed a nonsignificant trend downward over time (p = 0.281 by repeated-measures ANOVA). The mean blood level 8 days after the last dose was 0.18 ± 0.06 mg/dL (n = 7).

View larger version (12K): [in this window] [in a new window] [Download PPT slide]   Figure 1.. Serum perflubron levels during the first 24 h after initiation of PLV (p = 0.001 by repeated-measures ANOVA and over the 8 days after administration of the last dose of perflubron [p = 0.281]). *p = 0.017 when 1-h and 24-h data are compared by paired t test.

View larger version (11K): [in this window] [in a new window] [Download PPT slide]   Figure 2.. The mean ± SE loss of perflubron vapor from the lungs over the first 24 h after initiation of PLV and over the 3 days after administration of the last dose of perflubron (p = 0.037 by repeated-measures ANOVA for data following administration of the last dose). *p = 0.012 when 0-day and 3-day data are compared by paired t test.

View larger version (24K): [in this window] [in a new window] [Download PPT slide]   Figure 3.. The perflubron fill scores for the anterior, middle, and posterior regions of the lateral chest radiograph in the supine patients over the first 4 days after discontinuation of dosing of perflubron during PLV. *p < 0.05 by Dunnett’s t test when compared to data following administration of final dose. **p < 0.01 when anterior regions are compared to posterior by paired t test.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

PLV is a novel method of ventilatory support that is currently being studied for application in the management of patients with severe pulmonary failure. Initially described in 1991 by Fuhrman et al,⁷ subsequent evaluation of this technique of liquid breathing has demonstrated the ability to improve gas exchange and pulmonary function in animal models of respiratory failure.^{3 5 16 17 18 19 20 21 22 23} The majority of such studies have been performed in premature or full-term neonatal models, although the ability to enhance gas exchange and pulmonary function in adult animal models of lung injury has been demonstrated.^{2 3 16 17 18 19 23 24} Most recently, we have explored the ability to improve gas exchange during PLV in an adult oleic acid lung injury model.¹⁹ The technique of PLV has been developed to the point where safety and efficacy are being evaluated in prospective, randomized trials in adults with respiratory insufficiency.

As part of our initial evaluation of the safety and efficacy of PLV in adult patients with respiratory failure, we assessed parameters of uptake, distribution, and elimination of perflubron. Our intent was to describe the rate of loss of perflubron and to characterize the systemic levels in patents who were managed with PLV. Such data would be helpful in determining dosing schedules and rate of clearance after discontinuation of PLV. In addition, measurement of serum perflubron levels is critical in assessing the potential for systemic effects from pulmonary perflubron administration.

As far as we know, the rate of airway loss of perflubron has not been previously assessed in adult humans. Minimal amounts of perflubron are excreted via transpiration and in the urine.²⁵ As such, pulmonary perflubron elimination appears to be the major route of clearance. Studies in premature infants¹¹ have reported an average replacement rate of 3.3 mL/h in neonates with a mean weight of 1 kg over the period of PLV, with radiographic clearance of most of the perflubron by 48 h after cessation of PLV. This study did not specifically calculate airway clearance of perfluorochemical (PFC) and extrapolated the rate of loss by the need for supplementation. There are also differences in the mode of ventilation in neonates and adults that may have contributed to differences in rate of evaporation between these two groups of patients. In adult patients in this series, pulmonary elimination of perflubron immediately following administration of the last dose was 9.4 ± 3.0 mL/h. However, airway clearance of perflubron at 72 h following administration of the last dose was relatively low (1.0 ± 0.4 mL/h). The clinical implication is that redosing to sustain airway perflubron losses of approximately 10 to 15 mL/h is required to maintain a meniscus in the airway. In addition, the rate of perflubron loss is not constant, but rather decreases steadily over the first 72 h after dose administration. No specific measurements of airway clearance of PFC were made after extubation, although none of the patients could be weaned from mechanical ventilation during the initial 72 h after cessation of PLV.

The chest radiograph perflubron fill score generally followed the trends in airway clearance. The radiographs demonstrated steady elimination of perflubron over the first 48 h following administration of the last dose. Clearance of perflubron occurred predominantly from the nondependent regions of the lung first, with the more dependent regions retaining perflubron for longer periods: the anterior nondependent segments demonstrated a mean perflubron fill score of 1.8 (minimal to one-third full) at 96 h following the last dose of perflubron, while the perflubron fill score in the posterior dependent segments only decreased to 4.3 (two-thirds full to full) over the same time period. Although an effect of regional retention of perflubron in the dependent regions cannot be excluded by these data, our impression has been that the perflubron accumulates in the dependent regions secondary to the effects of gravity. We partly base this on the observation that dependent accumulation of perflubron is posterior in the supine patient but inferior when the same patient is placed in the sitting upright position. It should be noted that the density of perflubron may confound the observer’s ability to discriminate between various levels of fill, such that the scoring system may not be linear; it could be that differing volumes of perflubron are eliminated for each unit reduction in the perflubron fill score. For example, the radiographically dense perflubron might appear to completely "fill" a region of the lung until the majority is evacuated; therefore, a large volume of perflubron would have to be eliminated before the score was reduced from 5 to 4. Lateral radiographs would tend to confirm the amount of residual PFC even if the anteroposterior score were to be less accurate.

After 48 h, the rate of elimination of perflubron appeared to decrease even though the lungs remained one-third to two-thirds full in most regions as assessed by the perflubron fill score. This raises the question of why the remaining pulmonary perflubron was not rapidly eliminated. We would speculate that there are a predominance of poorly ventilated regions in these patients with severe respiratory failure, such that until sufficient pulmonary recovery has occurred, there are areas of lung filled with perflubron without any evident contribution to ventilation. These filled areas remain for extended periods of time, even when the patient no longer requires ventilatory support. It was our impression, based on the chest radiographs, that by 48 h the remaining perflubron was "alveolarized" in the anterior and middle regions, while "pooling" of perflubron only was present in the dependent posterior regions. This alveolarized perflubron may be in nonventilated regions, which would result in slow elimination; it should be noted, however, that we cannot exclude the possibility that this alveolarized perflubron is located in the interstitium rather than the alveolus. Based on a similar evaluation of radiographs, we have previously reported that two thirds of the perflubron is eliminated by 7 days after administration of the last dose of perflubron and that minimal perflubron remains after 21 days, although an exact quantification of residual perflubron would be difficult.²⁶

The steady increase in serum perflubron levels to 0.16 ± 0.05 mg/dL over the first 24 h after initiation of PLV suggests that there is a low level of transfer of perflubron from the airway to the vascular space. However, since the mean initial administered dose of perflubron in these patients was 903 ± 122 mL and the mean estimated blood volume was 3.5 ± 0.2 L, the amount of perflubron present in the bloodstream is approximately 0.3% of the dose administered. The maximum blood level of perflubron was 0.26 ± 0.05 mg/dL. These levels are similar to those previously reported in rats and canines²⁷ following performance of total liquid ventilation and in premature neonates during PLV.¹¹ Subsequent blood levels demonstrated a statistically nonsignificant slow trend in decrease as time from the last dose increased. It cannot be stated with certainty whether the low but stable levels of perflubron are maintained by an equilibrium with the alveolarized perflubron or by active transport from sequestered stores (such as macrophages). However, there are no known medical consequences of exposure to perflubron, and problems have not been identified in long-term survivors (over years).

It is worthwhile to note that the disease process and severity of the respiratory failure of this cohort of patients may differ from others resulting in alteration in the rate of elimination of perflubron. This is especially true since the volume of minute ventilation is severely reduced in most patients requiring ECLS. In addition, ECLS could have influenced serum perflubron levels, since elimination of vapor via the artificial lung may have occurred. Measurement of the content of perflubron in volumes of ECLS sweep gas would have allowed us to better describe this error, but these samples were not obtained. We have no means for assessing the degree to which this phenomenon affected serum perflubron levels. Currently, prospective, randomized trials are underway evaluating the safety and efficacy of PLV in improving gas exchange, pulmonary function, and outcome in adults with ARDS. Such studies will evaluate the pharmacokinetics of intratracheal-administered perflubron in less severely affected patients who are not receiving extracorporeal support. In the meantime, these data demonstrate that low serum perflubron levels at a maximum of 0.26 ± 0.05 mg/dL are associated with performance of PLV, while pulmonary elimination of perflubron occurs at an initial rate of 13.6 ± 4.5 mL/h but decreases to a minimal level over the first 48 h after last-dose administration.

	Footnotes

 
Abbreviations: ANOVA = analysis of variance; ECLS = extracorporeal live support; PFC = perfluorochemical; PLV = partial liquid ventilation

Supported in part by National Institute of Health grant R29 HL-54224.

Received for publication December 7, 1999. Accepted for publication July 11, 2000.

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TOP Abstract Introduction Materials and Methods Results Discussion References

 

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