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(Chest. 2001;119:1503-1509.)
© 2001 American College of Chest Physicians

Clinical Correlation With Changing Radiographic Appearance During Partial Liquid Ventilation*

Daniel P. Schuster, MD, FCCP; Neale R. Lange, MD; Ahmet Tutuncu, MD; Mark Wedel, MD and for the LiquiVent Study Group{dagger}

* From the Division of Pulmonary and Critical Care Medicine (Drs. Schuster and Lange), Department of Internal Medicine, Washington University School of Medicine, St. Louis, MO; and Alliance Pharmaceutical Corporation (Drs. Tutuncu and Wedel), San Diego, CA. {dagger} A list of principal investigators is located in the Appendix.

Correspondence to: Daniel Schuster, MD, 660 S Euclid Ave, University Box 8225, St. Louis, MO 63110; e-mail: schusted{at}msnotes.wustl.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 
Study objectives: To evaluate the chest radiographic filling pattern associated with partial liquid ventilation (PLV) with the perfluorochemical perflubron (LiquiVent; Alliance Pharmaceutical Corp; San Diego CA) as a function of dose and timing.

Design: Post hoc review of chest radiographs by three independent observers with correlation to clinical variables.

Setting: Phase II randomized, uncontrolled, prospective, multicenter clinical trial.

Patients: Sixteen adult patients with diffuse bilateral infiltrates consistent with acute lung injury and a PaO2/fraction of inspired oxygen (FIO2) ratio < 300 with positive end-expiratory pressure of 13 cm H2O and FIO2 >= 0.5.

Interventions: All patients were treated with either a 10-mL/kg or 20-mL/kg loading dose of perflubron followed by maintenance dosing at 3-h intervals to protocol-determined levels.

Results: There was a significant relationship between inhomogeneous radiographic filling during the first 48 h of treatment and the use of the lower loading dose of perflubron. Inhomogeneous radiographic filling (in 5 patients) was associated with a lower high-dose/FIO2 ratio at 24 h compared with the remaining patients. These differences resolved by 48 h. There were no other statistically significant correlations identified.

Conclusions: The radiographic appearance of PLV with perflubron appears to depend on the dose administered. Lower doses can be associated with both inhomogeneous radiographic filling and a transient deterioration in oxygenation during the first 24 to 48 h of treatment.

Key Words: acute lung injury • ARDS • gas exchange


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 
Partial liquid ventilation (PLV) is a promising new treatment for acute lung injury.1 During PLV, conventional gas mechanical ventilation is superimposed on lungs partially filled with perflubron, an eight-carbon perfluorochemical fully saturated with fluorine atoms, except for a terminal bromine atom. Perflubron is administered by direct instillation into the lungs via an endotracheal tube. It has a number of physical properties that may confer important beneficial effects on its use during PLV, including high density, low vapor pressure and surface tension, low miscibility in water or lipid, and the ability to carry both oxygen and carbon dioxide gases in high concentrations.1

Perflubron is also radiopaque (a consequence of the bromine atom), resulting in a unique radiographic appearance.2 3 4 5 6 7 In previous reports,2 3 4 5 6 7 chest radiographs and CT scans demonstrated a symmetrical and gravity-dependent distribution of perflubron. Recently, a phase II clinical trial of PLV with perflubron was conducted in 16 patients. As part of this trial, we observed examples of chest radiographs that were significantly different from previous reports. Accordingly, in the current report, we evaluated the chest radiographs from all 16 patients during the first 48 h of the study.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Appendix 1
 References
 
Study Protocol
This phase II clinical trial was fully approved by the institutional review boards at each participating center (see "Appendix"). After obtaining informed consent, PLV with perflubron (LiquiVent [C8F17Br]; Alliance Pharmaceutical Corp; San Diego CA) was administered to 16 patients who fulfilled the criteria established by a European-North American consensus conference8 (Table 1 ) for ARDS. These patients were part of a recent phase II, uncontrolled, multicenter, unblinded clinical trial designed to evaluate the feasibility of using protocol-defined algorithms for dose initiation and dose maintenance within the standardized guidelines established for mechanical ventilation. Entry criteria for the study included a PaO2/fraction of inspired oxygen (FIO2) ratio (P/F) <= 300 with a tidal volume of <= 10 mL/kg at ideal body weight (IBW), an end-inspiratory (plateau) pressure of <= 35 cm H2O, an inspiratory-to-expiratory ratio of <= 1:1, and a positive end-expiratory pressure (PEEP) of 13 cm H2O. These settings were chosen to ensure the uniformity of ventilator settings in evaluating the P/F as an entry criterion. Based on the literature available at the time of the study, a PEEP of 13 cm H2O also was considered to be slightly greater than the average expected "lower inflection point" on the pressure-volume relationship during early ARDS.


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  		Table 1. Patient Demographics and Outcome Data*

 
Of the 16 patients, 8 were randomly chosen (by protocol) to receive a loading dose of perflubron of 10 mL/kg at IBW (the low-dose group). The other eight patients received a loading dose of 20 mL/kg (the high-dose group). The perflubron was administered, without interrupting mechanical ventilation, directly into the lung via a side port adapter placed between the end of the endotracheal tube and the ventilator circuit tubing. Loading doses were given in 5-mL/kg aliquots over 15 to 30 min, as clinical circumstances allowed. The loading doses were intended to approximate initial filling to either the carina (carinal level) or 5 cm caudal to the incisors (laryngeal level) at zero PEEP with the patient in the supine position. The level of perflubron was confirmed to be at the intended level by using a suction catheter marked to extend either 5 cm beyond the tip of the endotracheal tube or 5 cm caudal to the incisors (carinal and laryngeal levels, respectively). Excess perflubron was removed by catheter suctioning. After the initial loading dose was given, supplemental dosing was given every 3 h to replace the amount of the drug lost to evaporation. The amount was dictated by the minute ventilation level, according to protocol. The level of the drug was checked before every second maintenance dose using a marked suction catheter as just described, and dosing was discontinued if excess perflubron was obtained. Dosing was discontinued finally when arterial oxygen saturation was > 90% after 48 h of treatment on an FIO2 <= 0.5 with at least 13 cm H2O PEEP or after 120 h of treatment, whichever came first.

Radiographic Evaluation
During the treatment phase (up to 5 days), portable chest radiographs were obtained for each patient within 4 h of initiating PLV and approximately every 24 h afterward, unless PLV was discontinued earlier (eg, because of death, adverse events, achieving oxygenation targets as described above, etc). Additional radiographs were obtained if needed for clinical reasons, as determined by the medical team caring for the patient. We limited the current study, however, to the baseline radiograph and to those obtained 24 and 48 h after initiating treatment with PLV.

Radiographic filling was judged to be homogeneous if there were no filling defects within the lung parenchyma of the lower and mid-lung fields bilaterally on the anterior-posterior film. Because portions of the upper lobe are above a horizontal plane at the level of the trachea, patients in the low-dose group whose only abnormality was incomplete filling of the upper lobe were still included in the homogeneous group. In contrast, radiographic filling was judged to be inhomogeneous if radiographs showed filling defects in the mid-lung and lower lung fields after initiating PLV. Each radiograph was evaluated by three independent reviewers (DS, AT, and MW), and differences in opinion were resolved by consensus. One patient, who demonstrated homogeneous filling in one lung but no perflubron in the contralateral lung at the 24-h time point because of a mainstem intubation, was excluded from the radiographic analyses, but was not excluded from other analyses.

Each investigator in the trial was asked to decide whether the underlying cause for ARDS was direct (eg, pneumonia, aspiration, lung contusion, toxic inhalation, or near-drowning) or indirect (eg, sepsis syndrome, nonthoracic trauma, cardiopulmonary bypass, or massive blood transfusion).

Statistical Analysis
Categorical variables were analyzed with contingency tables and analysis of covariance methods. Associations between categorical variables were tested with two-tailed Fisher’s Exact Tests (because of small sample size). Continuous variables were analyzed using one-way analysis of variance. Supportive analysis of covariance models were run using the baseline oxygenation variable as the covariate. Within-group comparisons of means to baseline values were performed with either Student’s or Satterwaith t tests. The latter uses lower degrees of freedom and was used when the assumption of sampling from a common variance was rejected. Statistical significance was accepted when the p value was < 0.05. No adjustments were made for multiplicity testing. All analyses were implemented using a statistical software package (SAS, version 6.12; SAS Institute; Cary, NC) running under a commercially available operating system (Windows 95; Microsoft; Redmond, WA).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Appendix 1
 References
 
Patient demographics and outcomes are given in Table 1 .

The distribution of patients with respect to radiographic filling pattern is shown in Table 2 . At 24 h after initiating PLV, all patients in the high-dose group showed a homogeneous filling pattern on the chest radiograph, whereas only two of seven patients showed this pattern in the low-dose group (p = 0.007). By 48 h, the radiographic pattern became homogeneous in three additional patients in the low-dose group, resulting in no statistical difference in patient distribution between the two filling patterns.


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  		Table 2. Relationship Between Radiographic Filling Pattern and Treatment Group Assignment*

 
The P/F as a function of filling pattern at baseline, 24 and 48 h (homogeneous or inhomogeneous) is shown in Figure 1 . There was no statistical difference in the P/F between the two groups at baseline. At 24 h, the P/F of the inhomogeneous group was significantly less than the homogeneous group. By 48 h, this difference had disappeared. Within the inhomogeneous group, there was a trend for the P/F to fall significantly at 24 h (p = 0.11), while no such trend was apparent in the homogeneous group. When adjusted for the baseline P/F, chest radiographic inhomogeneity was associated with a significantly lower P/F at 24 h compared to homogeneous filling. Thus, the temporal relationship of oxygenation correlated with the radiographic filling pattern (Table 1) .



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  		Figure 1. Oxygenation (expressed as the P/F) as a function of radiographic filling pattern and time. * = p < 0.05; B = baseline (ie, before the initiation of treatment with perflubron); CXR = chest radiograph.

 
Similar statistical relationships were observed when the patients were analyzed by treatment group (ie, low-dose group vs high-dose group), as would be expected given the relationship between radiographic filling pattern and treatment group (see above).

There was no significant relationship between radiographic filling pattern and the underlying risk factor for ARDS (direct or indirect). Likewise, no significant relationship to static respiratory system compliance was identified (based on airway plateau pressures).

The following two case summaries illustrate some of the observations noted above.

Case 1
A 36-year-old woman with a history of chronic pancreatitis was admitted with acute abdominal pain consistent with recurrent pancreatitis. An endoscopic retrograde cholangiopancreatogram was performed without incident on the day of admission. On the evening of the third hospital day, the patient developed progressive respiratory distress and new bilateral radiographic infiltrates (Fig 2 ). The following day, she was enrolled into the study and randomized to the high-dose perflubron group. The loading dose was administered without difficulty over approximately 90 min. Subsequent chest radiographs showed progressive symmetrical filling of both lungs (Fig 2) . Perflubron administration was discontinued per protocol after 72 h. The patient was extubated on the 10th day after the onset of respiratory distress and was discharged from the hospital 3 days later.



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  		Figure 2. Chest radiographs of the patient in case 1. Top left: baseline radiograph demonstrating bilateral parenchymal infiltrates. Bottom left: radiograph obtained 2.5 h after initiating treatment with perflubron. Note the homogeneous, symmetrical airspace filling. Right: radiograph obtained 48 h after initiating treatment. Note the additional airspace filling with perflubron.

 
Case 2
A 34-year-old woman was admitted to the neurologic/neurosurgical ICU with acute hypoxic respiratory failure secondary to aspiration after vomiting related to acute bulbar dysfunction from an exacerbation of multiple sclerosis. Radiographs showed progressive bilateral diffuse interstitial infiltrates (Fig 3 ) requiring endotracheal intubation and mechanical ventilation 2 days after admission. After meeting the study criteria, the patient was randomized to receive the lower loading dose of perflubron. Administration of the loading dose was complicated by hypotension requiring dopamine administration (3 to 5 µg/kg/min). The rate of drug administration was slowed (162 mL of the 524-mL loading dose was withheld). The chest radiograph showed patchy asymmetric filling with perflubron (Fig 3) . Oxygenation then improved. However, approximately 15 h after initiating drug administration, acute hypoxemia again developed, and copious secretions were suctioned from the airway (Fig 4 ). Similar episodes of hypoxemia occurred during the next 24 h. Fiberoptic bronchoscopy was performed, but no large mucous plugs were recovered. When improved oxygenation was observed during bagging, it was assumed that the mechanism was increased mean airway pressure. Therefore, PEEP was increased to 16 cm H2O, and tidal volume was increased to 13 mL/kg. Copious secretions continued to be suctioned, and arterial oxygenation again improved. By 48 h postinitiation, the PEEP had been reduced to the starting level of 13 cm H2O, and the radiographic appearance was more homogeneous (Fig 3) . Dosing was discontinued on day 4 when oxygenation targets were achieved per the study protocol. Mechanical ventilation was ultimately discontinued 18 days postadmission. The patient was alive and well at 12-month follow-up.



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  		Figure 3. Chest radiographs of the patient in case 2. Top left: baseline radiograph. Top right: radiograph made 1.5 h after initiating treatment. Bottom left: radiograph made 12 h after initiating treatment. Bottom right: radiograph made 48 h after initiating treatment. Note that filling is asymmetric and patchy at first but, over time, becomes progressively more symmetrical and homogeneous.

 


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  		Figure 4. Suction trap demonstrating suctioned material from the patient in case 2. Clear perflubron is at the bottom, airway secretions are in the middle layer, and the saline solution used during the suctioning maneuver forms the top layer.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Appendix 1
 References
 
The clinical benefits of PLV with perflubron have not yet been proven, but certain physical characteristics of the perfluorochemical suggest several possible mechanisms by which PLV could hasten recovery from acute lung injury.1 For one, perflubron has an oxygen and carbon dioxide solubility of approximately 53 mL/dL and 210 mL/dL, respectively. Second, the density of perflubron is nearly twice that of water. Thus, perflubron administration has been shown repeatedly to be preferentially distributed to dependent lung segments,2 precisely those that are most often affected by acute lung injury.9 Third, perflubron is not miscible with either water or lipid. Together, these characteristics could result in perflubron-induced oxygen delivery to and recruitment of previously nonventilated dependent lung segments, improving both gas exchange and lung compliance (the so-called "liquid PEEP" effect).10 Furthermore, with these physical characteristics, the perflubron would be expected to displace proteinaceous alveolar edema, inflammatory cells, debris, and mediators from the alveolar space, which would then rise to the top of the more dense perflubron column of liquid, where they could be suctioned off (a so-called "lavage effect").6 11

Most preclinical studies of PLV with perflubron (reviewed by Leonard1 ) have reported improved lung physiology. Previous reports2 7 also have shown that the chest radiographic appearance of perflubron is symmetrically and homogeneously distributed, especially in dependent lung segments during PLV. Progressive lung filling (Fig 1) with repeated dosing may indicate additional lung recruitment by the dense perfluorochemical. This typical constellation of findings is exemplified by case 1.

In contrast, Figure 3 shows an asymmetric, nonhomogeneous radiographic filling that was observed during the initial administration phase (ie, during the first 24 to 36 h) in case 2. This unusual radiographic appearance prompted a review of the remaining chest radiographs during the first 48 h of this study.

As shown in Figure 1 and Table 2 , an inhomogeneous radiographic appearance was significantly associated with assignment to the low-dose treatment group, and with worsening oxygenation by the 24 h postinitiation time point. As the radiographic appearance became more homogeneous during the next 24 h of treatment, oxygenation improved (Fig 1) .

In preclinical studies, investigators generally have shown significant dose-dependent improvements in oxygenation with PLV,12 but such improvements have not been reported uniformly.12 13 14 15 16 An additional animal study15 suggests that initial improvements may not be sustained over time. In a recent experimental model of acute lung injury,16 we also reported that oxygenation deteriorated compared with a control (no PLV) group. In that study, we speculated that this effect was the result of perflubron filling of the lung that was no longer atelectatic after applying PEEP to this lung injury model. This effect did not seem to be related to the dose of perflubron used. As can be seen in Figure 1 , oxygenation fell in both treatment groups relative to baseline at the 24-h time point. However, the decrease was greater in the low-dose treatment group, resulting in a significant difference in oxygenation between the two groups at that time. Because the transient worsening of oxygenation in the current study was associated with treatment with the lower dose of the drug, an additional explanation seems warranted.

The differences in radiographic filling pattern seems to be the most likely clue as to probable mechanism, because the deterioration in oxygenation at 24 h was associated with the inhomogeneous filling pattern. With this kind of inhomogeneity, it, obviously, would be difficult to maintain an optimal local ventilation-perfusion matching. However, as filling with perflubron became more homogeneous, perfused alveolar units would be ventilated more uniformly and oxygenation would improve. Because this uniform filling can be achieved more quickly in the higher dose treatment group, oxygenation would not be expected to deteriorate to the same extent.

It is also possible that other factors may have been operative. For instance, the patient in case 2 was treated not only with the lower dose of perflubron, but also had copious secretions from presumed aspiration-induced airway injury. The distal airways of such patients are likely to be obstructed by cellular debris and inflammatory edema. If the perflubron is unable to penetrate this barrier, gas exchange may actually worsen initially during PLV. Only with repeated suctioning and saline solution lavage can these secretions be cleared (Fig 4) , allowing the perflubron to penetrate to distal airways and, ultimately, to restabilize (and eventually improve) gas exchange and hemodynamics. Indeed, once perflubron has penetrated to distal lung units, its physical characteristics actually may allow secretions to rise to a point in the airway where they can be cleared more easily. These physiologic improvements will be associated with the more typical symmetrical and homogeneous radiographic appearance previously reported with perflubron administration (Fig 2) . Despite these features of case 2, no significant association was found between the radiographic filling pattern and the underlying risk factor for ARDS (eg, aspiration).

In conclusion, the radiographic appearance of PLV with perflubron appears to depend on the dose administered. A loading dose of 10 mL/kg followed by repeated filling to a carinal level (as defined in this study protocol) can be associated with both inhomogeneous radiographic filling and a transient deterioration in oxygenation during the first 24 to 48 h of treatment. Thereafter, with continued treatment, filling becomes more homogeneous and oxygenation improves. In the small number of cases reported here, there were no serious adverse events associated with these abnormalities, and they were all adequately treated with adjustments in FIO2, PEEP, tidal volume, and suctioning. In contrast, the radiographic appearance of PLV in patients treated with 20 mL/kg perflubron, followed by repeated filling to a laryngeal level, was always symmetrical and homogeneous, and these patients showed no significant deterioration in gas exchange.

While it is important that the treating physician be prepared to respond to such clinical events, it is also important to note that of the 16 patients who were studied in this particular trial, the 28-day mortality rate was only 6%, which is far lower than the expected 30 to 50% rate for ARDS patients. Thus, there is every reason to believe that PLV with perflubron may be a valuable addition to the therapeutic armamentarium for ARDS, but this supposition will require validation in a larger-scale, controlled, clinical trial, which is currently underway.


   Appendix 1
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix 1
References
 
The following principal investigators participated in this phase II clinical trial of PLV with perflubron: Henry Fessler, MD, Johns Hopkins University School of Medicine; Stephen Mette, MD, Maine Medical Center; Dean Sandifer, MD, Watson Clinic; Daniel Schuster, MD, Washington University School of Medicine; and Herbert Wiedemann, MD, Cleveland Clinic Foundation.


   Footnotes
 
Abbreviations: FIO2 = fraction of inspired oxygen; IBW = ideal body weight; PEEP = positive end-expiratory pressure; P/F = PaO2/fraction of inspired oxygen ratio; PLV = partial liquid ventilation

Drs. Schuster and Lange were investigators in the Perflubron phase II trial described in this manuscript and received reimbursement for the costs of conducting the trial at their center.

Received for publication December 30, 1999. Accepted for publication October 18, 2000.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 

  1. Leonard, RC (1998) Liquid ventilation. Anaesth Intensive Care 26,11-21[ISI][Medline]
  2. Quintel, M, Hirschl, RB, Roth, H, et al (1998) Computer tomographic assessment of perfluorocarbon and gas distribution during partial liquid ventilation for acute respiratory failure. Am J Respir Crit Care Med 158,249-255[Abstract/Free Full Text]
  3. Hirschl, RB, Conrad, S, Kaiser, R, et al (1998) Partial liquid ventilation in adult patients with ARDS: a multicenter phase I-II trial; Adult PLV Study Group. Ann Surg 228,692-700[CrossRef][ISI][Medline]
  4. Meaney, JF, Kazerooni, EA, Garver, KA, et al (1997) Acute respiratory distress syndrome: CT findings during partial liquid ventilation. Radiology 202,570-573[Abstract/Free Full Text]
  5. Leach, CL, Greenspan, JS, Rubenstein, SD, et al (1996) Partial liquid ventilation with perflubron in premature infants with severe respiratory distress syndrome: the LiquiVent Study Group. N Engl J Med 335,761-767[Abstract/Free Full Text]
  6. Hirschl, RB, Pranikoff, T, Wise, C, et al (1996) Initial experience with partial liquid ventilation in adult patients with the acute respiratory distress syndrome. JAMA 275,383-389[Abstract]
  7. Kazerooni, EA, Pranikoff, T, Cascade, PN, et al (1996) Partial liquid ventilation with perflubron during extracorporeal life support in adults: radiographic appearance. Radiology 198,137-142[Abstract/Free Full Text]
  8. Bernard, GR, Artigas, A, Grigham, KL, et al (1994) The American-European Consensus conference on ARDS: definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 149,818-824[Abstract]
  9. Sandiford, P, Province, M, Schuster, D (1995) Distribution of regional density and vascular permeability in the adult respiratory distress syndrome. Am J Respir Crit Care Med 151,737-742[Abstract]
  10. Hirschl, RB, Overbeck, MC, Parent, A, et al (1994) Liquid ventilation provides uniform distribution of perfluorocarbon in the setting of respiratory failure. Surgery 116,159-167[ISI][Medline]
  11. Gauger, PG, Pranikoff, T, Schreiner, RJ, et al (1996) Initial experience with partial liquid ventilation in pediatric patients with the acute respiratory distress syndrome. Crit Care Med 24,16-22[CrossRef][ISI][Medline]
  12. Tutuncu, AS, Faithfull, NS, Lachmann, B (1993) Intratracheal perfluocarbon administration combined with mechanical ventilation in experimental respiratory distress syndrome: dose-dependent improvement of gas exchange. Crit Care Med 21,962-969[ISI][Medline]
  13. Younger, JG, Taqi, AS, Till, GO, et al (1997) Partial liquid ventilation protects lung during resuscitation from shock. J Appl Physiol 83,1666-1670[Abstract/Free Full Text]
  14. Colton, DM, Till, GO, Johnson, KJ, et al (1998) Neutrophil accumulation is reduced during partial liquid ventilation. Crit Care Med 26,1716-1724[CrossRef][ISI][Medline]
  15. Smith, KM, Mrozek, JD, Simonton, SC, et al (1997) Prolonged partial liquid ventilation using conventional and high frequency ventilatory techniques: gas exchange and lung pathology in an animal model of respiratory distress syndrome. Crit Care Med 25,1888-1897[CrossRef][ISI][Medline]
  16. Lange, NR, Kozlowski, JK, Gust, R, et al (2000) Effect of partial liquid ventilation on pulmonary vascular permeability and edema after experimental acute lung injury. Am J Respir Crit Care Med 162,271-277[Abstract/Free Full Text]




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