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Ann Thorac Surg 1998;66:877-885
© 1998 The Society of Thoracic Surgeons
a Division of Cardiothoracic Surgery, University of Illinois at Chicago, Chicago, Illinois, USA
Address reprint requests to Dr Allen, Division of Cardiothoracic Surgery, Department of Surgery, University of Illinois at Chicago, Suite 417 CSB, M/C 958, 840 S Wood St, Chicago, IL 60612
Presented at the Thirty-fourth Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 26–28, 1998.
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Abstract |
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Methods. After baseline measurements, 10 pigs had the left lung flushed with a modified Euro-Collins solution, explanted, stored at 4°C for 24 hours, and transplanted into 10 other pigs. Five (group 1) underwent uncontrolled reperfusion created by removal of the vascular clamps after implantation of the new left lung, mimicking the clinical situation. The other five (group 2) underwent controlled reperfusion, which we performed by taking blood from the femoral artery, mixing it with a crystalloid solution (using a mixer heater) to make the blood hyperosmolar, alkalotic, and substrate-enriched, and pumping it through a leukocyte-depleting filter into the transplanted lung for 10 minutes at a pressure of 20 to 30 mm Hg before removing the pulmonary artery clamp. The right pulmonary artery and bronchus were then ligated, and left lung function was assessed each hour for 4 hours and compared with baseline.
Results. Controlled reperfusion (group 2) minimized the reperfusion injury, preserving posttransplant pulmonary compliance (92% ± 1% versus 68% ± 1%; p < 0.001), reducing the rise in pulmonary vascular resistance (27% ± 2% versus 166% ± 3%; p < 0.001), improving oxygenation (PO2, 425 ± 14 versus 82 ± 11 mm Hg; p < 0.001), and lowering myeloperoxidase activity (0.22 ± 0.02 versus 0.45 ± 0.02 
OD/mg protein per minute; p < 0.001) and tissue edema (83.0% ± 0.3% versus 84.9% ± 0.3%; p < 0.001) compared with uncontrolled reperfusion, which resulted in an injury so severe that 3 of 5 pigs died before the 4-hour measurements.
Conclusions. After 24 hours of cold ischemia uncontrolled reperfusion results in a severe pulmonary reperfusion injury. This injury is almost completely avoided by controlling the composition (modified solution and white blood cell filter) and conditions (pressure) of the reperfusion. Because this experiment mimics the clinical situation, it suggests surgeons should begin to use this modality to limit reperfusion injury after lung transplantation.
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Introduction |
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Over the last few years, our understanding of the ischemia–reperfusion injury in lungs and other organs has escalated. This has led to significant changes in organ preservation with improvement in clinical outcome [2–5]. Prevention of the ischemia–reperfusion injury has, however, mostly been directed at how the lungs are procured and preserved during ischemia [3–7]. Much less attention has been paid to altering the period of reperfusion. Although the pathophysiology of reperfusion injury in the lung is far from fully understood, many studies in the heart have demonstrated that it can be modified by controlling the initial period of reperfusion [8–10]. By applying these principles to the lungs, we recently found the reperfusion injury could be almost completely avoided after 2 hours of warm pulmonary ischemia by controlling the composition and condition of reperfusion [11]. In this study, the reperfusate was controlled by infusing a leukocyte-depleted modified blood solution at a low pressure for 10 minutes before removing the vascular clamps and restoring the native circulation. However, whether these concepts will prove beneficial after long-term cold ischemia, which more closely mimics the clinical situation, is unknown. Although controlled reperfusion modifies the reperfusion injury after myocardial ischemia, care must be taken not to extrapolate these findings to the lung, as the results may be different. The current study was therefore performed to determine whether controlled reperfusion is able to modify the reperfusion injury in the lung after 24 hours of cold ischemia. It uses a single-lung large animal transplant model that simulates the operating room to mimic the clinical setting.
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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Heart rate was monitored continuously by electrocardiogram. The left femoral artery and vein were cannulated for continuous monitoring of arterial blood pressure, blood gas determinations, and intravenous infusions. Urine output was assessed with an indwelling urinary catheter. Intravenous furosemide (0.5 to 1 mg/kg) was given as indicated to maintain urine output greater than 1 mL · kg-1 · h-1 and both experimental groups received similar quantities. Body temperature was monitored using esophageal temperature probe (Mon-A-Therm 400H, Mallinckrodt, St. Louis, MO), and maintained at 36° to 38°C using a heating blanket. Periodic arterial blood samples were drawn and analyzed for blood gas, potassium, ionized calcium, and hemoglobin (Blood Gas System 288; Ciba-Corning, Medfield, MA). Electrolytes were kept within normal limits and all animals had an initial hemoglobin higher than 10.0 g/dL. A 7F balloon-tipped thermodilution catheter (Baxter Health Corp, Deerfield, IL) was placed by means of the right internal jugular vein into the main pulmonary artery for determination of pressure and cardiac output. An 18-gauge catheter was placed in the left atrium for pressure measurements. All functional measurements were obtained with perfusion and ventilation to the left lung only by clamping the right lung bronchus and pulmonary artery.
Ten animals were used as donors. After obtaining baseline functional measurements from the left lung, the main pulmonary artery was cannulated with a 10F DLP (DLP Inc., Grand Rapids, MI) cannula. The left lung was then harvested in the following manner. Clamps were placed on the superior and inferior vena cavae, ascending aorta, and the main pulmonary artery proximal to the cannula. Cold modified Euro-Collins solution (4°C) was given to the lungs, using at least 50 mL/kg. The lungs were drained through the left atrium. Care was taken to continue to give the pulmoplegia until the fluid was clear. The lung was ventilated during this period with 100% oxygen, and iced slush was placed in both pleural cavities and mediastinum. The lungs and heart were then removed from the chest cavity en bloc. The left lung was separated from the other organs on the back table, and care was taken to keep it inflated. The lung was then wrapped in gauze, placed in an insulated ice bag filled with normal saline, and stored at 4°C for 24 hours. In the 10 pigs used as recipients, the left hilum was dissected out and a pneumonectomy was performed using vascular clamps for proximal control. The donor lung was then reimplanted using 4-0 Prolene (Ethicon, Somerville, NJ) for the bronchial anastomosis and 5-0 Prolene for the pulmonary artery and the left atrial anastomoses. Care was taken to continue topical hypothermia until reperfusion. Ventilation to the transplanted lung was started during reperfusion using low tidal volumes (5 mL/kg) initially.
Experimental groups
After 24 hours of cold storage, the transplanted lung was reperfused by one of two methods.
Uncontrolled reperfusion
In 5 pigs, the pulmonary artery clamp was simply removed and the lung was reperfused using the native pulmonary circulation, simulating current clinical practice. The left atrial clamp was left in place for 1 to 2 minutes, and the effluent was flushed through the venous anastomotic site before securing the anastomosis and removing the venous clamp.
Controlled reperfusion
In 5 other pigs (group 2), the initial period of reperfusion was controlled for 10 minutes using the following technique. The right femoral artery and left pulmonary artery were cannulated using an 8F DLP cannula. This allowed blood to be withdrawn from the femoral artery by a roller pump, mixed with a modified crystalloid solution (Table 1) in a 4:1 ratio using a mixer heater (BCD; Shiley Corp, Irvine, CA), and then passed through a leukocyte-depleting filter (Pall BC-1; Pall Corp, Glencove, NY) before being returned to the left lung (Fig 1). A line was also placed to allow constant monitoring of left pulmonary artery pressure during reperfusion. A pressure of 20 to 30 mm Hg was used, resulting in flows of 40 to 60 mL/min. The effluent was flushed and ventilation was started as in the control group. After 10 minutes of controlled reperfusion, the reperfusate was stopped, the pulmonary artery clamp was removed, the cannula was withdrawn, and the native circulation was restored.
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Cardiac output was measured using a Swan-Ganz catheter and an Edwards 9502 computer (Baxter Corp, Berkley, CA). Averages from three measurements were used. Pulmonary vascular resistance (PVR) was calculated using the following formula:
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Peak airway pressure was measured using a tidal volume of 15 mL/kg without positive end-expiratory pressure, and static compliance was calculated as the change in volume per change in pressure (mL/cm H2O).
Tissue measurements
A biopsy sample was taken from the inferior portion of the left upper lobe at the end of the experiment. One piece was weighed and then dried to a constant weight at 80° to 85°C. Lung water was calculated using the following formula:
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The other portion of the biopsy specimen was immediately frozen and stored in liquid nitrogen, and myeloperoxidase activity was measured using the method previously described [11]. Myeloperoxidase activity is expressed as change in optical density units per minute per milligram of tissue protein (OD · min-1 · mg protein-1).
Statistical analysis
Data were analyzed using JMP v2.0 (SAS Institute, Inc., Carey, NC) on a Macintosh IIvx computer (Apple Inc., Cupertino, CA). Group data are expressed as mean ± standard error of the mean. Unpaired Student’s t test was used for comparison of variables between experimental groups. Values of p less than 0.05 were considered statistically significant.
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Results |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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Results are summarized in Figures 2 through 4 and Table 2. All animals undergoing controlled reperfusion (group 2) were stable during the 4-hour observation period after transplantation. There was a slight tendency for these animals to improve in function over the 4-hour period, but this was not statistically significant. In contrast, 3 of 5 (60%) of the animals undergoing uncontrolled reperfusion with unmodified blood (group 1) died within 30 minutes after the nonischemic (right) lung was ligated for the first (1 hour) posttransplant measurement. Death was caused by progressive hypoxia or right heart failure secondary to pulmonary hypertension. Subsequent functional measurements at 2, 3, and 4 hours in the 2 surviving animals were worse than the initial measurements at 1 hour. The 1-hour measurements are therefore depicted and were used for statistical analysis because (1) they are the most favorable for group 1 hearts (uncontrolled reperfusion), and (2) with only two animals surviving in group 1 there are not adequate numbers for statistical comparisons beyond 1 hour. The recovery of pulmonary function 1 hour after transplantation was strikingly different between the two groups (Figs 2–4). Animals undergoing controlled reperfusion (group 2) had almost complete preservation of pulmonary function, whereas the animals undergoing uncontrolled reperfusion (group 1) had function barely compatible with life (Figs 2–4).
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Comment |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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Although ischemia alone undeniably leads to cell death, most investigators believe that within clinical relevance this injury occurs primarily during reperfusion [8, 10, 12–14]. Reperfusion injury is defined as the functional, metabolic, and structural alteration caused by reperfusion after a period of ischemia [8, 10, 12]. The potential for this damage exists in every transplanted organ, because its blood supply is always interrupted when an organ is removed from the donor, thus ensuring ischemia. Studies in the heart have found that the fate of the myocardium jeopardized by global ischemia is determined more by the method of reperfusion then by the duration of ischemia [8, 10]. Indeed, the myocardial reperfusion injury could almost completely be avoided by controlling the composition of the reperfusate and the conditions of reperfusion [8, 10]. By applying the principles of controlled reperfusion to the lung, we recently demonstrated that the reperfusion injury could also be avoided after pulmonary ischemia [11]. However, complete pulmonary functional recovery was only possible by using a multifaceted approach, which controlled both the composition of the reperfusate (modified blood solution, white blood cell filter) and the conditions of reperfusion (pressure). This supports the studies by Lu and associates [15], who also reported that a multipronged approach worked better than a single modality. This is not surprising considering what we now know about the complexity of the reperfusion injury, which causes cellular damage by a variety of mechanisms [8–10, 12–14]. We did not separate out the various components of controlled reperfusion in this study, owing to the cost and complexity of the experimental model. However, numerous studies of myocardial ischemia, and our preliminary study after 2 hours of warm lung ischemia, have documented the need to control as many facets of reperfusion as possible and indicate that omission of any component diminishes functional recovery [8–11, 15].
Leukocytes have been found to be a major mediator of reperfusion injury in various organs [11, 12, 16, 17]. The first step is adhesion of the activated leukocyte to the endothelium [17, 18]. Once bound, the activated leukocyte releases a variety of mediators such as oxygen free radicals and proteases, that ultimately cause cell injury or death [11, 13, 17, 18]. Breda and associates [16] were the first to show the benefits of leukocyte depletion in reducing the pulmonary reperfusion injury. They used an isolated lung preparation that was not clinically applicable, which may explain why the strategy of leukocyte reduction is not routinely used in patients. However, we recently confirmed their findings after 2 hours of warm pulmonary ischemia using the same clinically applicable technique as in this study [11]. Although various methods have been tried to block the leukocyte-mediated injury, prevention is generally achieved either by decreasing the number of leukocytes delivered to the ischemic organ during reperfusion or by chemicals that block leukocyte adhesion or activation, or individual cytotoxins. Leukocyte depletion is usually achieved by filtration, as was done in this study. We used the Pall-BC1 filter because it has been shown by us and others to filter more than 95% of leukocytes during a single passage [11, 16]. On the other hand, only about 40% of platelets are depleted. Total body leukopenia or platelet depletion is therefore minimal in our model, as only a part of the total blood volume passes through the leukocyte filter. However, we have shown that using this filter results in excellent leukodepletion of the reperfusate [11]. The advantages of using filtration over chemical leukocyte control are that (1) only the ischemic organ is subjected to the effects of leukodepletion, (2) total body depletion is minimal with white blood cell counts returning to normal shortly after reperfusion is completed, and (3) there are no pharmacologic side effects such as may occur with chemical blockers.
Despite the fact that neutrophils play a significant role in the pathophysiology and severity of this injury, several studies have shown that neutrophils are not necessary for ischemia–reperfusion injury to occur in the lung [19, 20]. Eppinger and associates [19] suggested a bimodal pattern of injury, consisting of both leukocyte-mediated and -independent events. This hypothesis seems likely considering that most studies using leukocyte-depletion alone have shown only partial protection against the reperfusion injury [11, 15, 19, 20]. We therefore combined leukocyte-depletion with a modified blood solution (see Table 1) in an attempt to counter some of the other mechanisms thought to contribute to the reperfusion injury.
Our current reperfusate solution is based on what we and others have found helps prevent the reperfusion injury in ischemic myocardium, as well as our studies after 2 hours of warm pulmonary ischemia [8–11]. On theoretical grounds, its components are designed to help minimize the cellular damage while accelerating repair, so that the underlying cell will be able to tolerate unmodified blood when native pulmonary circulation is restored. The solution is based on the following principles (see Table 1). Intracellular and extracellular acidosis is buffered by adding the intracellular buffer tromethamine; cellular influx of calcium, which mediates cellular injury, is prevented by the addition of citrate and magnesium; tissue edema is counteracted by making the solution hyperosmolar; and substrates for energy production are supplied by enriching the solution with aspartate, glutamate, glucose, and blood. In addition, the vasodilator nitroglycerin is added to counteract the vasomotor dysfunction often seen during reperfusion, thus ensuring delivery of our modified solution to all pulmonary cells. This solution will most likely change as we learn more about the pulmonary reperfusion injury. For instance, there are data to support that because of dual reoxygenation pathways (blood and alveolar) and use of oxygen inflation during storage, a nonleukocyte-mediated, oxygen radical–dependent injury plays a much bigger role in the lung versus other organs [19, 21]. Intense investigations are ongoing using substances that block the formation of oxygen free radicals or scavenge them after their formation. Several recent studies have shown the beneficial effects of these scavenger compounds when introduced before or during the initial reperfusion [6, 12, 17, 22]. It is very likely that these or other substances will become a valuable asset to our reperfusion solution in the future.
We also controlled the conditions of reperfusion by delivering the reperfusate at a fixed pressure of 20 to 30 mm Hg. We showed the benefits of "gentle" reperfusion after myocardial ischemia several years ago [9, 10]. Bhabra and associates [23] were the first to apply these principles to the lung. They found that by reducing the pressure during the first 10 minutes of reperfusion, the pulmonary reperfusion injury was significantly reduced. Others have since come to the same conclusion [11, 15]. The mechanism by which low pressure exerts this protective effect is not precisely known. There is no doubt that simple hydrostatic pressure plays a role, and mechanical forces (shear stress) have also been implicated [9, 10, 12, 23] Pickford and coworkers [24] found that even normal physiologic reperfusion after ischemia may cause endothelial detachment. More recently, studies of endothelial cells in culture have found that pressure can independently activate endothelial cells, which then leads to increased white cell adherence resulting in pulmonary injury [25]. In this study, we used a reperfusion pressure of 20 to 30 mm Hg. This is lower than the pressure of 40 to 50 mm Hg we used in our initial study of controlled lung reperfusion [11]. These higher initial pressures were based on our work in the myocardium, where the normal perfusion pressure is closer to 50 mm Hg. The reasons for lowering the pressure to 20 to 30 mm Hg in this study were that (1) the lung usually has a lower physiologic pressure than the heart, (2) a pressure of 20 to 30 mm Hg more closely resembles normal pulmonary artery pressures, and (3) recent unpublished data from our laboratory demonstrates that these lower reperfusion pressures further reduce the reperfusion injury and result in superior posttransplantation lung function. We infused the modified reperfusate for 10 minutes based on work by Bhabra and associates [23]. However, we have previously reported that 20 minutes of controlled reperfusion was superior to 10 minutes after myocardial ischemia [8, 10]. The length of time over which the solution should be infused, like the composition of the reperfusate solution, may therefore change, and is currently an active area of investigation.
We carried out this investigation using an in vivo model that mimics the operating room, as some investigators have suggested that an ex vivo or warm ischemic model may alter the results, making findings not clinically applicable [2, 14, 25]. Indeed, investigations of myocardial protection have yielded vastly different results depending on whether the model was in vivo or an isolated heart preparation, or used blood or crystalloid as the perfusate [10, 26, 27]. We therefore attempted to mimic the operating room as much as possible, so that these results would be clinically applicable to patients undergoing transplantation. We also used techniques that could be used in patients without increasing the operative risk. For example, the blood used for the reperfusate is taken from the pig’s femoral artery and returned through the pulmonary vein so that blood transfusions are not necessary. The only difference in a human patient would be that the arterial blood would probably be taken from the aorta instead of the femoral artery, as the chest would be open, and groin cannulation might increase morbidity (Fig 5).
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In summary, this study demonstrates that (1) after 24 hours of cold pulmonary ischemia uncontrolled reperfusion, by simply removing the vascular clamp and allowing unmodified blood to reperfuse the lung, results in a severe pulmonary injury, and (2) this injury is almost completely avoided by controlling the composition of the reperfusate (modified solution, white blood cell filter) and the conditions of reperfusion (pressure), resulting in preservation of pulmonary function. Because this model mimics the clinical situation and uses techniques that are currently available, these findings suggest surgeons should begin to use this modality in patients undergoing lung transplantation.
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Acknowledgments |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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References |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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