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Ann Thorac Surg 1995;60:1210-1214
© 1995 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Perfadex Is Superior to Euro-Collins Solution Regarding 24-Hour Preservation of Vascular Function

Department of Cardiothoracic Surgery, University Hospital, Lund, Sweden

Accepted for publication May 26, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. The aim of this study was to compare Perfadex with Euro-Collins solution regarding 24-hour preservation of endothelium-dependent relaxation and vascular smooth muscle function.

Methods. The infrarenal aorta of 72 isogenic rats was studied in organ baths as fresh controls, after 24 hours of cold (4°C) storage, and after 24-hour storage followed by transplantation and examination after 7 or 30 days. The thromboxane A₂ analogue U-46619 was used to test contractility. Acetylcholine chloride was used to elicit endothelium-dependent relaxation and papaverine hydrochloride, to elicit endothelium-independent relaxation.

Results. With both solutions, all grafts were patent after 7 and 30 days. Vessels preserved in Euro-Collins solution for 24 hours lost 95% (p < 0.001) of their contractility compared with fresh controls; 7 days after transplantation, they had regained 40% of initial contractility, and after 30 days, there was no significant decrease in contractility. Vessels preserved in Perfadex manifested no significant decrease in contractility at any time. Endothelium-dependent relaxation could not be evaluated in vessels stored for 24 hours in Euro-Collins solution because they had lost almost all contractility; 7 days after transplantation, endothelium-dependent relaxation was reduced by 65% (p < 0.001), but at 30 days after transplantation, there was no significant decrease in endothelium-dependent relaxation. Vessels preserved in Perfadex for 24 hours lost 17% (p < 0.05) of endothelium-dependent relaxation, but 7 and 30 days after transplantation, there was no significant decrease in endothelium-dependent relaxation.

Conclusions. Perfadex, but not Euro-Collins solution, has the capacity to preserve vascular function after 24 hours of storage followed by in vivo reperfusion.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
The most common method of organ preservation for clinical transplantation is to flush the organ with a cold preservation solution and to keep it immersed in that solution until the transplantation can be performed. The tissue most exposed to the preservation solution is the vascular endothelium, which is in direct contact with the solution throughout the storage period. The vascular smooth muscles come into contact with the preservation solution indirectly from diffusion of the solution through the endothelium. Even if it can be demonstrated in vitro that a solution does not impair endothelium-dependent relaxation or smooth muscle function after cold storage [1, 2], it is necessary to ascertain the impact on these functions after transplantation and reperfusion with warm oxygenated blood under pressure, which occurs in the clinical situation.

There is evidence that reperfusion injury is mediated by oxygen free radicals; cold ischemic storage may alter the metabolic pathways so that toxic oxygen free radical formation occurs once oxygen is available to the tissue during the reperfusion period [3]. Although in vitro studies of blood vessels in organ baths expose the vessels to oxygen and stretching, the shear stress on the endothelium caused by the blood flow cannot be created in organ baths. In addition, during reperfusion there are the potentially injurious effects of increasing blood pressure on the endothelial cells, which are fragile because of the cold storage and low temperature during the first minutes of reperfusion [4]. It has been demonstrated that low temperatures have an adverse effect on the vascular endothelium and that mechanical pressure may further damage cold endothelial cells [5]. Therefore, it is of great interest to study endothelial cell function after in vivo reperfusion with warm oxygenated blood.

The aim of the present study was to compare Euro-Collins solution with Perfadex regarding their respective capacity to preserve endothelium-dependent relaxation and vascular smooth muscle function after prolonged storage followed by transplantation and reperfusion for 7 or 30 days. The infrarenal aorta of isogenic rats was selected for the study, as the use of this preparation allowed the investigation to be standardized [1, 2]. Previously we [6] have shown that the aorta of rats can be harvested and transplanted into other isogenic rats without disturbance of endothelium-dependent relaxation or smooth muscle function.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Seventy-two isogenic Sprague-Dawley rats weighing 275 to 325 g were used in the study. Twenty-eight animals were used as donors and 28 as recipients. Sixteen animals, 8 in each group, were used to provide samples for fresh controls and 24-hour storage. Two preservation solutions were tested: Perfadex (Medisan Pharmaceuticals, Uppsala, Sweden) and Euro-Collins solution (Fresenius AG, Bad Homburg, Germany) (Table 1). The grafts were all stored for 24 hours at 4°C in the respective solution. The animals were anesthetized with ether and treated in compliance with the ``Guide for the Care and Use of Laboratory Animals'' published by the National Institutes of Health (NIH publication 85-23, revised 1985).

Recipient Procedure
All animals were given Streptocillin vet (Boehringer Ingelheim, Ingelheim/Rhein, Germany), 0.1 mL subcutaneously, before the operation was started. The aorta was then prepared and clamped in the same way as in the donor and divided midway between the clamps. The graft segment that had been stored for 24 hours in cold Euro-Collins or Perfadex solution was then interposed in its original orientation and sutured end-to-end with resorbable 9-0 Vicryl sutures (Ethicon, Somerville, NJ). Each anastomosis consisted of eight to ten interrupted sutures.

Seven days or 30 days later, the graft was removed and immediately placed in warm (37°C) and oxygenated (95% oxygen and 5% carbon dioxide) Krebs buffer solution and freed of any surrounding connective tissue. Two ring segments, each in the range of 1.0 to 1.2 mm in length, were then taken from the midportion of the graft and transferred to the organ baths.

Controls
The infrarenal aorta was extirpated and handled in the same way as the grafted vessels. Two segments were immediately transferred to organ baths (fresh controls). The remaining part of the vessel was divided into segments and immersed in Euro-Collins or Perfadex solution for 24 hours at 4°C and then transferred to organ baths for study.

Recording Contractility and Endothelium-Dependent or Endothelium-Independent Relaxation
Isometric tension was measured in organ baths that were water-mantled to keep the temperature of the bath solution at 37°C. The bath solution (Krebs) was bubbled with 95% oxygen and 5% carbon dioxide, giving it a pH of approximately 7.4. The composition of the Krebs solution was as follows (mmol/L): 119, NaCl; 15, NaHCO₃; 4.6, KCl; 1.2, NaH₂PO₄; 1.2, MgCl₂; 1.5, CaCl₂; and 11, glucose. Each ring segment was suspended between two metal holders (0.2 mm in diameter). One holder was attached to a Grass FT 03 transducer connected to a Grass polygraph for continuous recording of isometric tension. The other metal holder was fixed to an adjustable unit by which the vessel segments were repeatedly stretched until a basal tension of about 8 mN was reached. In separate experiments, it was found that maximum response was obtained at this tension.

Contraction was then induced with the thromboxane A₂ analogue U-46619 (The Upjohn Company, Kalamazoo, MI), added at a concentration of 10^-6.5 mol/L, which gave a stable contraction in the range of 7 to 14 mN. In separate experiments, concentration–response curves have shown 10^-8 mol/L U-46619 induces half maximum contraction, and 10^-6.5 mol/L U-46619 induces contractions in the range of 90% to 100% of maximum. In separate experiments, it has also been shown that U-46619 is an endothelium-independent vasoconstrictor in this preparation. After repeated washes resulting in the restoration of basal tension, a new contraction was induced with the same concentration of U-46619.

When the degree of contraction had reached a stable plateau, increasing concentrations of acetylcholine chloride (Sigma, St. Louis, MO) were cumulatively added to the baths. Acetylcholine releases endothelium-derived relaxing factor by stimulating receptors in the endothelium. In six segments, the endothelium was removed by gently rubbing the intimal surface over a pair of microtweezers; acetylcholine elicited no relaxation. In each segment, the response to the different concentrations of acetylcholine was expressed as a percentage of the U-46619–induced contraction. If impaired relaxation was obtained with acetylcholine in the preserved vessels compared with the fresh controls, the endothelium-independent vasodilator papaverine (10^-4 mol/L) was added to the bath to ascertain whether complete relaxation could then be obtained.

Data Analysis
Results were expressed as the mean ± the standard error of the mean, n being the number of animals used in each group. Statistical evaluation of each solution was performed with one-way analysis of variance using Dunnet's test to perform the multiple comparisons. Comparisons between the two solutions were performed with unpaired Student's t test. A p value of less than 0.05 was considered significant.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Graft Patency
In both the Euro-Collins and the Perfadex groups, all grafts were patent after 7 days and after 30 days.

Preservation of Contractile Function
There was no significant loss in contractility in vessels preserved in Perfadex solution for 24 hours only or for 24 hours and then transplanted and studied after 7 or 30 days compared with fresh controls (Fig 1). Vessels preserved in Euro-Collins solution for 24 hours lost 95% (p < 0.001) of their contractility compared with fresh controls; 7 days after transplantation, they had regained 40% (p < 0.001) of initial contractile capacity, and after 30 days, there was no significant decrease in contractility (see Fig 1). Vessels stored in Perfadex showed highly significantly better contractility after 24 hours of storage and 7 days after transplantation than those stored in Euro-Collins solution (see Fig 1). However, 30 days after transplantation, there was no significant difference between groups.

View larger version (50K): [in this window] [in a new window]   Fig 1. . Contractile response of rat aorta to thromboxane A2 analogue U-46619 (upper half) and maximum endothelium-dependent relaxation elicited by acetylcholine chloride (lower half). Each bar represents the mean value ± the standard error of the mean. There were 8 animals in each group except the 30-day group (n = 6). (* p < 0.05; *** p < 0.001.)

View larger version (34K): [in this window] [in a new window]   Fig 2. . Effects of cumulative addition of acetylcholine (Ach) to rat aorta precontracted with thromboxane A2 analogue U-46619 in fresh nonstored vessels, vessels stored for 24 hours in Perfadex solution, and vessels stored for 24 hours in Perfadex solution followed by transplantation and examination after 7 or 30 days. As 10 to 15 minutes is needed to obtain a full concentration–response curve, the controls, to which no acetylcholine was given, are shown in open symbols to demonstrate that no spontaneous relaxation occurred over time. Each point indicates the mean value ± the standard error of the mean. There were 8 animals in each group except the 30-day group (n = 6). (conc = concentration.)

View larger version (31K): [in this window] [in a new window]   Fig 3. . Effects of cumulative addition of acetylcholine chloride (Ach) to rat aorta precontracted with thromboxane A2 analogue U-46619 in fresh nonstored vessels, vessels stored for 24 hours in Euro-Collins solution, and vessels stored for 24 hours in Euro-Collins solution followed by transplantation and examination after 7 or 30 days. As 10 to 15 minutes is needed to obtain a full concentration–response curve, the controls, to which no acetylcholine was given, are shown in open symbols to demonstrate that no spontaneous relaxation occurred over time. Each point indicates the mean value ± the standard error of the mean. There were 8 animals in each group except the 30-day group (n = 6). (conc = concentration.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
At the beginning of the modern era of clinical lung transplantation, preservation of the lungs was accomplished by topical cooling alone [7]. In 1988, Locke and co-workers [8] concluded that topical cooling alone did not achieve optimal 6-hour lung preservation but that flush perfusion with Euro-Collins solution, an ``intracellular'' type of solution, gave good preservation for 6 hours. Since then, the preservation of lungs for clinical transplantation has been accomplished in most centers with Euro-Collins solution. However, the high potassium content in Euro-Collins solution causes strong pulmonary vasoconstriction [9], and this vasoconstriction is not eliminated by prostaglandin E₁ or prostacyclin, which are often used together with Euro-Collins solution [10]. Several studies [11–16] have concluded that an extracellular type of solution with low potassium and dextran can improve lung preservation. It has been suggested that the addition of glucose to the low-potassium–dextran solution makes it even more efficient in prolonged lung preservation [17]. Perfadex is a low-potassium–dextran–glucose solution recently demonstrated to give excellent lung preservation for 24 hours [18].

This study demonstrates that Perfadex is superior to Euro-Collins solution regarding prolonged preservation of vascular endothelial and smooth muscle cells. However, 30 days after transplantation, vessels preserved in Euro-Collins solution had regained normal contractility and endothelium-dependent relaxing capacity, thus indicating that the initial significant reduction in these functions may be reversible.

Abebe and co-workers [19] performed a morphologic study with scanning and transmission electron microscopy of rat aorta stored in Euro-Collins solution for 24 hours. They found that the endothelial cells were markedly swollen with loss of intracellular organelles, including most mitochondria. There were breaks in the cell membrane and granularity in the chromatin of the nuclei. The interstitium was markedly edematous as were the smooth muscle cells, which had lost most of their organelles. Dense bodies and myofilaments were rare, as were mitochondria. In the same study, the researchers investigated contractility and endothelium-dependent relaxation after 24 hours of storage in Euro-Collins solution and found that these functions were significantly reduced. In contrast, aortas stored in University of Wisconsin solution for 24 hours demonstrated endothelial and smooth muscle cells that were functionally and morphologically almost intact. Recently, we [2] compared rat aortas stored for 24 hours in University of Wisconsin solution or Perfadex solution. We found the two solutions to be equally efficient, ie, contractility was not reduced, whereas endothelium-dependent relaxation was slightly reduced in both groups.

In the present study, a 24-hour storage period in Perfadex resulted in a small but significant decrease in endothelium-dependent relaxation. However, after 7 days of reperfusion, the vessels had regained full endothelium-dependent relaxing capacity. In an earlier study [20], significantly reduced endothelium-dependent relaxation was also seen in porcine pulmonary arteries after 24 hours of storage in Perfadex. Neither recovery nor further impairment was seen in that study after 24 hours of reperfusion; a significant correlation was shown to exist between endothelium-dependent relaxation and pulmonary vascular resistance, thus indicating the importance of preserving the endothelium in as optimal condition as possible.

Was the return of endothelium-dependent relaxation seen in the present study caused by a recovery of the original endothelial cells, or were the original endothelial cells replaced by migration and replication of adjacent endothelial cells from the recipient animal? Morphologically, endothelialization of a mechanically denuded rat aorta occurs at a rate of approximately 0.07 mm/day in the circumferential direction and about six times faster in the axial direction [21]. In light of this information, it would appear that the return of full endothelium-dependent relaxing capacity, as early as 7 days after transplantation in the Perfadex group, was due to recovery of the original endothelium. Regarding the increase in endothelium-dependent relaxation seen in the Euro-Collins group between 7 and 30 days after transplantation, a contribution from migrating adjacent endothelial cells cannot be excluded.

Badly preserved vascular endothelium may lead to various adverse effects, including vasoconstriction, platelet deposition, and thrombosis, which may ultimately result in loss of tissue perfusion and tissue necrosis. Damaged endothelium may also expose complement receptors on the cell surface, and the subsequent binding of complement to the endothelium has been suggested to increase the risk of graft rejection [22].

Although our experiments were performed on rats, there is a striking cross-species homogeneity, which includes humans, in endothelium-dependent physiology [21]. In conclusion, the findings of this study show that the low-potassium–dextran–glucose solution Perfadex is clearly superior to Euro-Collins solution and is able to give good 24-hour preservation of vascular smooth muscle and endothelium-dependent relaxation.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Address reprint requests to Dr Steen, Department of Cardiothoracic Surgery, University Hospital, S-221 85 Lund, Sweden.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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2. Ingemansson R, Sjöberg T, Massa G, Steen S. Long-term preservation of vascular endothelium and smooth muscle. Ann Thorac Surg 1995;59:1177–81.[Abstract/Free Full Text]
3. Detterbeck FC, Keagy BA, Paull DE, Wilcox BR. Oxygen free radical scavengers decrease reperfusion injury in lung transplantation. Ann Thorac Surg 1990;50:204–10.[Abstract]
4. Kruuv J, Glofcheski D, Cheng KH, et al. Factors influencing survival and growth of mammalian cells exposed to hypothermia. Effects of temperature and membrane lipid perturbers. J Cell Physiol 1983;115:179–85.[Medline]
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7. The Toronto Lung Transplant Group. Experience with single-lung transplantation for pulmonary fibrosis. JAMA 1988;259:2258–62.[Abstract/Free Full Text]
8. Locke TJ, Hooper TL, Flecknell PA, McGregor CGA. Preservation of the lung. J Thorac Cardiovasc Surg 1988;96:789–95.[Abstract]
9. Kimblad PO, Sjöberg T, Massa G, Solem J-O, Steen S. High potassium contents in organ preservation solutions cause strong pulmonary vasocontraction. Ann Thorac Surg 1991;52:523–8.[Abstract]
10. Kimblad PO, Steen S. Eliminating the strong pulmonary vasoconstriction caused by Euro-Collins solution. Ann Thorac Surg 1994;58:728–33.[Abstract]
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13. Maccherini M, Keshavjee SH, Slutsky AS, Patterson GA, Edelson JD. The effect of low-potassium–dextran versus Euro-Collins solution for preservation of isolated type 2 pneumocytes. Transplantation 1991;52:621–6.[Medline]
14. Oka T, Puskas JD, Mayer E, et al. Low-potassium UW solution for lung preservation. Comparison with regular UW, LPD, and Euro-Collins solutions. Transplantation 1991;52:984–8.[Medline]
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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): Richard Ingemansson Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ingemansson, R. Articles by Steen, S. Search for Related Content PubMed PubMed Citation Articles by Ingemansson, R. Articles by Steen, S.