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Ann Thorac Surg 1996;62:356-362
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

A Systematic Study of Hypothermic Lung Preservation Solutions: Euro-Collins Solution

Department of Surgery, University of Kentucky Medical Center, Lexington, Kentucky

Accepted for publication March 15, 1996.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. Testing lung function after preservation is difficult because a suitable model is still lacking; thus, the effectiveness of different solutions for lung preservation has not been confirmed. This study tested the effectiveness of Euro-Collins solution alone for hypothermic preservation of rat lungs.

Methods. A living rat perfusion model was used, which allowed more than 5 hours of continuous perfusion for isolated lung function studies. Group 1 lungs (control, n = 8) were tested without preservation. In groups 2 through 6 (n = 8 lungs each), the lungs were flushed with 4°C Euro-Collins solution and preserved for 4, 6, 8, 12, and 24 hours, respectively. Lung function studies were carried out after preservation.

Results. In groups 1 and 2, pulmonary arterial blood flow and pulmonary venous oxygen tension were higher and pulmonary resistance was lower than in the other groups. Airway pressure and resistance were lowest in group 1. Lungs in groups 5 and 6 demonstrated the worst function, but the lung tissue wet to dry ratio was higher only in group 6.

Conclusions. At 4°C, Euro-Collins solution can effectively preserve rat lungs for 4 hours. Six to 8 hours of preservation resulted in depressed lung function. More than 12 hours of preservation resulted in uniformly deficient lung function, rendering the lungs unsuitable for transplantation.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The increasing demand for suitable donor lungs has far exceeded the available number of donor lungs. On the basis of a 1989 survey of cardiac donors, it was estimated that the lungs of only one in five to one in ten such donors may be suitable for transplantation [1, 2]. Thus, of all major organs, lungs are by far the least available for transplantation. According to statistics from the United Network of Organ Sharing, the waiting list for lungs contained 1,213 names in 1991, 1,240 in 1993, and 1,894 by the end of November 1995. It is estimated that approximately 3.5% of the 20,000 patients with cystic fibrosis in North America die each year of end-stage lung disease [3].

Among the strategies for improving the outcome of lung transplantation procedures is the development of methods for improving lung preservation. After many years of research, very little progress has been made in developing methods for extending lung preservation times. Currently, flushing the pulmonary artery with cold Euro-Collins solution in combination with prostacyclin and prostaglandin is the most frequently used technique for lung preservation [4]. Evaluating lung function before transplantation is critical to the survival of the recipient. So far, very few techniques are available for testing lung viability. Several reported techniques for such tests are difficult to set up, and effective perfusion still falls short [5, 6]. We have used a living rat perfusion model for isolated lung function studies after preservation and have found this model to be simple, inexpensive, and very reliable. With this model, it is possible for us to test systematically and compare various solutions for hypothermic lung preservation at different time periods. We have tested several commonly used intracellular and extracellular preservation solutions with and without additives. Because numerous modifications have been made to the standard solutions and many additives have been used with these solutions in clinical and experimental practice, the differences among these solutions have been blurred [7, 8]. In our study, individual standard preservation solutions were tested first, followed by their modifications, including changing of formulas and mixing with additives. This article reports the results of using standard Euro-Collins solution for hypothermic rat lung preservation for 4, 6, 8, 12, and 24 hours.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Healthy adult Sprague-Dawley rats (250 to 300 g) were allowed free access to food and water before operation. All animals received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and the "Guide for the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health (NIH publication no. 80-23, revised 1985).

Setup of the Perfusion Apparatus
The setup for isolated lung function studies has been reported previously in brief [9, 10]. The perfusion apparatus consisted of a temperature-controlled water bath, a perfusion chamber in which the isolated lung was suspended, a blood reservoir for storing returned blood, and a roller pump for returning blood to the host rat. The chamber was preheated by a heating-circulating pump to maintain the water temperature at 37°C. The cap of the perfusion chamber was removable and contained a tube to which the trachea of the isolated lung was attached. This tube was connected to a rodent respirator (model 683; Harvard Apparatus, South Natick, MA) for ventilation. A Y-connector was attached to the top of the tube, and a Gould pressure transducer (Gould Inc, Centerville, OH) was attached to the connector for respiratory pressure measurement. The pulmonary artery of the isolated lung was perfused with the venous blood of the host rat by gravity gradient. A 2-mm flow probe was incorporated into the perfusion line and was connected to a Transonic T-201 Flowmeter (Transonic Systems, Inc, Ithaca, NY) for perfusion flow monitoring and recording.

Preparation of the Host Rat
The rats were anesthetized by intraperitoneal injection of sodium pentobarbital (35 to 50 mg/kg weight). The cervical trachea was cannulated, and the animal was ventilated with room air by a rodent respirator. A tidal volume of 2.5 to 3.5 mL and a rate of 40 to 50 cycles per minute were used. The right internal jugular vein was cannulated with a 2-mm catheter. Heparin sodium 3 mg/kg was infused intravenously, and both carotid arteries were cannulated with 1-mm catheters. The catheter in the right carotid artery was connected to a Gould pressure transducer for blood pressure monitoring. Blood from the host rat was withdrawn by gravity from the right internal jugular vein to the perfusion chamber, where it perfused the pulmonary artery of the isolated lung. A hydrostatic pressure of 25 mm Hg was maintained by adjusting the distance between the host rat and the isolated lung. Blood returned from the pulmonary vein of the isolated lung was collected at the bottom of the perfusion chamber and stored in the reservoir. A Minipuls three-roller pump (model 312; Gilson Co, Middleton, WI) returned the blood from the reservoir to the left carotid artery of the host rat (Fig 1). Arterial blood samples were taken from the host rat every 10 minutes for blood gas and electrolyte analysis. The blood return rate, tidal volume, and respiratory rate for the host rat were adjusted during perfusion to maintain stable arterial blood pressure and arterial blood gas values in the host rat.

View larger version (35K): [in this window] [in a new window]   Fig 1. . Living rat perfusion apparatus setup. The isolated lung is perfused by blood from the internal jugular vein of the host rat. Blood returned from the isolated lung is collected in the perfusion chamber (C) and reservoir (R) and then returned to the arterial system of the host rat by a roller pump. The hollow arrows indicate the direction of flow of nonoxygenated venous blood. The filled arrows indicate the direction of flow of oxygenated blood. (PA = pulmonary artery; PV = pulmonary vein.) (Reproduced with permission from Wu G, Zhang F, Salley RK, Diana JN, Su T-P, Chien S. Delta opioid extends hypothermic preservation time of the lung. J Thorac Cardiovasc Surg 1996;111:259–67.)

Composition of the Preservation Solution
The preservation solution used in this study was a commercial product by Fresenius (Bad Homburg, Germany). After all the additives were mixed, the final concentrations of chemicals (g/1,000 mL) and ions (in mmol/L) were as follows: KH₂PO₄, 2.04; K₂HPO₄, 7.4; KCl, 1.12; NaHCO₃, 0.84; glucose•H₂O, 38.5; K⁺, 115.0; Na⁺, 10.0; Cl^-, 15.0; HCO₃^-, 10.0; H₂PO^-, 15.0; and HPO₄^2-, 42.5. Osmolarity was 375.0 mOsm/L and pH was 7.25 (4°C).

Animal Groups Studied
The study for lung preservation and function was designed in the following manner. The isolated lungs were first preserved for 24 hours, after which lung function studies were performed. If the results indicated poor lung function, the preservation time for the next set of lungs was reduced to 12 hours. If lung function was impaired after 12 hours of preservation, hypothermic storage time was reduced to 8 hours, 6 hours, and 4 hours, respectively, until all lungs showed good function. For Euro-Collins solution, this protocol resulted in five experimental groups of 8 rats each: group 2 (4 hours), group 3 (6 hours), group 4 (8 hours), group 5 (12 hours), and group 6 (24 hours). One group (group 1) of rat lungs was not subjected to hypothermic storage and was used as a normal control. In this group, the left lung was flushed with 37°C normal saline, removed, and immediately transferred to the perfusion chamber for function studies. There was no interruption of ventilation during this transfer process, and the interruption of lung perfusion was less than 20 seconds. In the other five experimental groups, the left lung was flushed with 4°C Euro-Collins solution and removed. The bronchus was clamped at the end of inspiration to maintain inflation during storage. The lungs were immersed in 4°C Euro-Collins solution for different durations of preservation. After preservation, the isolated lungs were transferred to the perfusion chamber and the bronchus was attached to the supporting cannula, which was connected to a respirator. The lung was suspended in the chamber. During the perfusion period, the isolated lung was ventilated with room air by the rodent ventilator, as stated earlier, at a respiratory rate of 40 to 50 cycles per minute, a tidal volume of 2.5 to 3.5 mL, and a positive end-expiratory pressure of 0.5 cm H₂O.

Procedure of Lung Function Studies
A period of 5 to 10 minutes was needed for equilibration. Pulmonary perfusion flow, pulmonary perfusion pressure, and airway pressure (AWP) were recorded continuously. The lungs were inspected continuously for edema, hemorrhage, and atelectasis. Blood samples were taken from the pulmonary artery and vein of the isolated lung every 10 minutes for blood gas analyses with an IL BGE Blood Gas and Electrolyte Analyzer (Instrumentation Laboratories, Lexington, MA). From these indices, pulmonary vascular resistance (PVR), airway resistance (AWR), and alveolar-arterial oxygen difference were calculated according to standard formulas.

At the end of the experiment, lung tissue samples were taken for wet to dry weight ratio measurements. The samples were blotted to remove excess water, and wet weight was determined. The samples were then placed in an oven at 80°C for 3 days, after which the dry weight was obtained.

Statistical Analysis
Data were collected and managed using a commercial spreadsheet software package (Lotus 123 for Windows, version 1.0; Lotus Development Corp, Cambridge, MA), and mean, standard deviation, and standard error were calculated for each group at each time period. A commercial statistics software package (SigmaStat, version 2.00; Jandel Corp, San Rafael, CA) was used for statistical analysis. The data were evaluated first by analyses of variance for repeated measures. Significant effects were examined further using Dunnett's procedure to compare all groups. Because six groups of lungs were compared every 10 minutes, the resultant significance level ranged from no significance to a p value as small as less than 0.00001. To simplify the illustrations, statistical significance was assumed for probability levels of 0.05 or less. All data were expressed as mean ± standard error of the mean.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Overall Performance
During reperfusion, the lungs were perfused for 90 minutes unless earlier deterioration occurred. In groups 1 and 2, the isolated lungs maintained stable oxygen tension, carbon dioxide tension, PVR, and AWR, without important pulmonary edema or hemorrhage during 90 minutes of perfusion. In groups 3 through 5, the maximum perfusion time was 60 minutes because of decreased oxygen tension, increased carbon dioxide tension, increased PVR, increased AWR, pulmonary edema, hemorrhage, or a combination of these problems. In group 6, the lungs could be perfused for only 30 minutes because of severe pulmonary edema and hemorrhage. During the perfusion period, oxygen tensions in the pulmonary veins of the isolated lungs were always higher than those in the pulmonary arteries in all groups, indicating partially or totally preserved oxygen transporting capacity, although this capacity was impaired in the lungs preserved for more than 6 hours.

Pulmonary Blood Flow and Pulmonary Vascular Resistance
Pulmonary blood flow ranged from 1.88 ± 0.28 to 3.25 ± 0.56 mL/min in group 1. In groups 2 and 3, pulmonary blood flow was similar to that in group 1. However, pulmonary blood flow was smaller in groups 4 through 6 (0.86 ± 0.18 to 0.96 ± 0.17 mL/min for group 4, p < 0.0001 as compared with group 2) (Fig 2).

View larger version (24K): [in this window] [in a new window]   Fig 2. . Comparison of pulmonary artery (PA) blood flow in the isolated rat lungs (p < 0.05, groups 1 through 3 versus groups 4 through 6).

View larger version (24K): [in this window] [in a new window]   Fig 3. . Comparison of pulmonary vascular resistance (PVR) in the six groups during perfusion.

View larger version (26K): [in this window] [in a new window]   Fig 4. . Comparison of oxygen tensions in the pulmonary vein (PVO2) in the six groups during perfusion.

View larger version (30K): [in this window] [in a new window]   Fig 5. . Comparison of alveolar-arterial oxygen tensions (A-a O2 DIFFERENCE) in the isolated rat lungs.

View larger version (29K): [in this window] [in a new window]   Fig 6. . Comparison of airway pressure of the isolated lungs in the six groups.

View larger version (31K): [in this window] [in a new window]   Fig 7. . Comparison of lung tissue wet-to-dry weight ratios after preservation and perfusion.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Despite more than three decades of extensive research, the safe clinical preservation time for lungs is still limited to 4 to 6 hours [11–13]. Because of its simplicity, single-flush hypothermic storage is the most commonly used technique for lung preservation, and Euro-Collins solution is one of the most popular solutions. Euro-Collins solution has an intracellular electrolyte composition with a high content of potassium (115 mmol/L) and no colloids or other substances with high molecular weights. When this solution is used, reported results from animal studies vary from 4 hours [14] to 24 hours [15] of preservation time. However, it is generally agreed that this solution can provide satisfactory lung preservation for 4 hours. In animal experiments, adding some chemicals such as methylprednisolone or prostaglandins can allow 6 hours of preservation, but lung edema is evident after 12 hours of cold storage and becomes severe after 24 hours [16–18].

Our results indicate that when the preservation time is limited to 4 hours, adequate gas exchange is maintained, and pulmonary flow, PVR, AWP, and AWR remain almost normal. A preservation time of 6 to 8 hours results in depressed lung function. However, damage to the lungs was not uniform. In group 3 (6-hour preservation), 5 lungs showed relatively good function during perfusion, whereas in group 4 (8-hour preservation), only 3 lungs showed relatively normal function. This good to bad lung function ratio decreased when the preservation time was extended further. After 12 hours of preservation, only 1 lung of 8 showed relatively good function. After 24 hours of preservation, no lung showed good function. More than 12 hours of preservation resulted in uniformly deficient lung function and rendered the lungs unsuitable for transplantation.

It should be noted that in this study, commercially available Euro-Collins solution was used to flush and preserve the lungs at 4°C. This solution has a pH of 7.25 and a concentration of potassium of 115 mmol/L, and no prostaglandins were added. These may not be the most favorable conditions for lung preservation, as indicated by other reports [5, 19], because high concentrations of potassium (>20 mmol/L) can cause pulmonary vasoconstriction [20, 21] and because a decrease in temperature and pH are not optimal for lung preservation [5]. In addition, uneven flushing may result from vasoconstriction [22]. However, no uneven lung perfusion was indicated in this setting, probably because our perfusion temperature was low enough to prevent vasoconstriction [23]. It is reasonable to believe that adjustment of preservation temperature, pH, and potassium concentration or the addition of prostaglandins to the solution may increase the effective lung preservation time. However, the value and mechanism of action of prostaglandins in lung preservation are still controversial because recent studies have shown little beneficial effect of prostaglandins in lung preservation [12, 16, 19, 24]. In fact, sometimes prostaglandins are believed to have a detrimental effect [25].

As in heart transplantation, the transplanted lung must function immediately after operation because alternative long-term artificial support does not exist. Primary nonfunction and delayed function can be tolerated in renal transplantation, but not to any degree in lung transplantation. As a result, viability tests before transplantation are critical to the success of the procedure. Many indices have been used to test lung function after preservation or transplantation, such as gas exchange, PVR, static and dynamic lung compliance, AWR, vascular permeability, and histologic, metabolic, and radiologic changes. It is not clear which index is the most sensitive for detecting lung damage. It is generally believed that gas exchange is a more reliable indicator of lung damage than are hemodynamic, morphologic, radiologic, or metabolic changes, because early damage can impair the lung's exchange capacity without any morphologic alterations [26]. However, our results indicated that when Euro-Collins solution was used, an increase in AWP and AWR was the first sign of impaired lung function during perfusion, whereas other indices did not indicate any difference. Many researchers have used AWP to evaluate the functional integrity of isolated lungs [27]. The relation between AWP and tidal volume is useful for the evaluation of lung compliance [28]. To compare with in situ measurement, both AWP and AWR are more accurate in isolated lung studies because the thoracic cage, chest muscle, pleural pressure, and esophageal pressure are excluded [29, 30].

It is interesting to note that both PVR and AWP increased slightly during the initial 10 minutes of perfusion in groups 1 and 2. This phenomenon did not occur in the lungs preserved for more than 6 hours. One possible explanation is that in unpreserved lungs or those preserved for only a short time, both vascular tone and bronchial tone are still maintained. Increased smooth muscle tone causes constriction, which results in increased PVR and AWP. When the preservation time is extended, smooth muscle damage occurs and the muscle loses its tone. Increased PVR and AWP are unfavorable for early functional recovery after lung transplantation. However, these increases also may serve as an indicator of tissue viability after preservation.

The model used in this experiment is worth mentioning. Several animal models have been developed for evaluating isolated lung function, but most of them require a sophisticated setup, and the perfusion time is limited to several minutes or to less than 1 hour [5–7, 27, 31]. The technique used in this study is relatively simple and very reliable. Using the animal's own blood provides an ideal perfusion medium for lung function studies and simplifies the experimental setup. The isolated lung is perfused by venous blood from the host rat. The design closely resembles the normal physiologic condition, and no artificial deoxygenation procedure is required. Blood returned from the isolated lung is infused back into the arterial system instead of the venous system of the host rat. This setting has three important advantages: (1) It reduces the load on the host rat's heart, facilitating hemodynamic stability of the host rat; (2) the host rat's venous oxygen tension remains normal, thus eliminating the possibility of high pulmonary arterial oxygen tension in the isolated lung, as seen in other models; and (3) any aggregates and particles returned from the isolated lung and the pump system will be filtered out by the peripheral microvasculature of the host rat before the blood returns to the host heart and the pulmonary arteries of both host and isolated lungs. This feature further increases the hemodynamic stability of the host rat and prevents extra damage to the isolated lung caused by the aggregates generated in any artificial pump or tubing.

The arterial pressure, blood gases and electrolytes, and respiratory pressure of the host rat were monitored continuously during the perfusion period, and it was very easy to maintain a stable condition by controlling the return speed of the blood. Careful monitoring of the host rat is required during perfusion. The host rat cannot tolerate a long period of perfusion if hypotension occurs. However, if blood loss is minimal, hemodynamic stability of the host rat is easy to maintain. With this setting, we were able to use 1 host rat to perfuse an isolated lung for more than 5 hours, or to use 1 host rat for three or more isolated lung studies. It is not clear whether the multiple use of 1 host rat can induce an immunologic reaction. We have not seen any difference among the lungs perfused by the same host rat, probably because very few, if any, blood cells are left in the isolated lung.

Although it is not always tenable to extrapolate the results from small animals such as rats to human beings, this model is a very sensitive screening method for lung preservation. When human lungs are transplanted after more than 6 hours of hypothermic preservation, some patients recover fully, but others may experience impaired lung function. Results obtained from this study reflect a similar pattern.

In conclusion, rat lungs maintain good function when preserved for 4 hours with hypothermic Euro-Collins solution without additives. Lung function is partially impaired when the preservation time extends to 6 to 8 hours. However, some lungs still maintain good function during this period. The ratio of good to bad lung function decreases continuously after 6 hours of preservation. When the preservation time exceeds 12 hours, no lungs maintain good function, and the lungs are not suitable for transplantation. It is possible to adjust the preservation environment and to add chemicals to Euro-Collins solution to extend the effective lung preservation time to 6 to 8 hours.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
This study was supported in part by National Institutes of Health grant GM-43890.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Address reprint requests to Dr Chien, Department of Surgery, University of Kentucky College of Medicine, 800 Rose St, Lexington, KY 40536.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Robert K. Salley Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wu, G. Articles by Chien, S. Search for Related Content PubMed PubMed Citation Articles by Wu, G. Articles by Chien, S.