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Ann Thorac Surg 1995;60:38-44
© 1995 The Society of Thoracic Surgeons
Thoracic and Cardiovascular Research Laboratory, Department of Surgery, University of Virginia Health Sciences Center, Charlottesville, Virginia
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Abstract |
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Methods. Sixteen adult swine underwent left lung allotransplantation. Controls received lungs procured from heart-beating donors, NHBD pigs received lungs immediately harvested from donors after death from asphyxiation, and NHBD-15 and NHBD-30 pigs received lungs harvested after 15 and 30 minutes after asphyxiation.
Results. After 1 week of survival, mean dynamic airway compliance (mL/cm H2O ± standard error of the mean) was 16.3 ± 0.7 in controls, and 17.3 ± 1.0, 16.4 ± 6.0, and 7.3 ± 1.6 in the NHBD, NHBD-15, and NHBD-30 groups, respectively (p = 0.02, NHBD-30 versus others combined). No significant differences were noted in the pulmonary venous partial pressure of oxygen or pulmonary vascular hemodynamics compared with controls.
Conclusions. The decrease in airway compliance noted in the NHBD-30 group may reflect an exacerbation of reperfusion injury caused by 30 minutes of warm ischemia during organ retrieval. We conclude that posttransplantation lung function using an NHBD with up to 15 minutes of warm ischemia is equivalent to lung function after heart-beating harvest.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Since its introduction in 1983 by the Toronto group, lung transplantation has become an accepted therapy for a number of end stage lung diseases [1]. Despite increasing clinical success, however, the number of patients undergoing lung transplantation in the United States has been limited to approximately 600 per year by a severe shortage of acceptable donor organs [2]. Many additional patients could benefit from this therapy if organs were available. Thus, clinicians have searched for ways to increase the lung donor pool. These have included improved community education, relaxed organ acceptance criteria, increased reliance on single lung transplantation, and the use of partial organ donation. Unfortunately, these efforts have produced only modest increases in lung allograft availability [3]. Furthermore, the idea of ``presumed consent,'' although effective in increasing donor organ availability in Europe, is unlikely to be embraced in the United States [3]. Although xenotransplantation may ultimately resolve the organ availability crisis, the prospects for clinically useful xenotransplantation in the near future are remote. As such, the concept of procuring organs from recently deceased cadavers has generated new interest. Once the mainstay of organ retrieval before the acceptance of ``brain death'' criteria, so-called non–heart-beating organ donation may have the potential to increase allograft availability by as much as 20% [4].
Most of the recent clinical experience with non–heart-beating organ donation has been with kidney and liver transplantation where results have been encouraging [5–8]. However, isolated reports of successful lung transplantation after non–heart-beating donation have been published [9, 10]. These efforts have stimulated a number of investigators to begin studying non–heart-beating lung donation in experimental models to clarify the effects of warm ischemia on the lung allograft. Egan and colleagues [11] have developed a nonsurvival model of canine lung transplantation that they have used to demonstrate the feasibility of non–heart-beating donation for lung transplantation. This group has additionally demonstrated the utility of ventilating the lung with 100% oxygen during the warm ischemic interval [12, 13] and the benefit of free radical inhibitors added to the pulmonary flush during non–heart-beating harvest [14].
Drawing on previous experience in our laboratory with a survival model of porcine left lung transplantation [15], we designed a study to assess the effects of non–heart-beating organ donation on the lung allograft 7 days after implantation. We believe that success in such a survival model, in which the allograft is challenged by a clinically relevant period of reperfusion, immunologic exposure, and pharmacologic immunosuppression, is a prerequisite for wider clinical application of non–heart-beating lung procurement. We hypothesized that lung function after non–heart-beating donation associated with up to 30 minutes of warm ischemia would be equivalent to allograft function of controls harvested in the standard manner when studied 7 days after transplantation. This article reports our data regarding airway function, vascular tone, and gas exchange in a survival model of single left lung transplantation in the domestic pig after both standard and non–heart-beating organ harvest.
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Material and Methods |
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Heart-Beating Harvest
Adult domestic swine weighing between 30 and 35 kg served as left lung donors. Anesthesia was induced with intramuscular xylazine (1 mg/kg), telazol (6 mg/kg), and atropine (0.01 mg/kg), facilitating endotracheal intubation. The pigs were ventilated with room air at a rate of 20 breaths/min using a volume ventilator (Harvard Apparatus, South Natick, MAAu: location of Harvard Apparatus?), and paralyzed with metocurine (0.2 mg/kg). Anesthesia was maintained with 2.0% halothane, and each pig was anticoagulated with heparin sodium (200 U/kg). Control donors (control, n = 7) underwent lung harvest using a standard heart-beating technique. Through a left thoracotomy, the hemiazygos vein was ligated and divided, providing exposure to the left hilum. The inferior ligament was transected and the pulmonary vessels were isolated. After excising the tip of the left atrial appendage, the main pulmonary artery (PA) was clamped and a 16-gauge catheter inserted. One liter of Euro-Collins solution (ECS) at 4°CAu: OK? was infused into the PA from a height of 30 cm. Room air ventilation was continued during the ECS flush. Saline slush was applied topically. The lung was then excised with a cuff of left atrium and placed in saline slush while the recipient pig was prepared.
Non–Heart-Beating Harvest
Study donors underwent lung harvest under non–heart-beating conditions. Heparinized and paralyzed donor pigs were allowed to die by discontinuing ventilator support until cardiac fibrillation occurred. Room air ventilation was reestablished at a rate of 20 breaths/min and a tidal volume of 15 mL/kg at the moment of death by electrocardiographic criteria. ``Immediate non–heart-beating donors'' (NHBD, n = 5) underwent immediate rapid left thoracotomy, PA flush with 4°C ECS, and topical cooling once cardiac death had occurred. ``Fifteen-minute non–heart-beating donors'' (NHBD-15, n = 6) were ventilated with room air beginning at the moment of cardiac death and continuing until a total of 15 minutes of warm ischemia had elapsed since interruption of ventilation. At the end of the 15-minute warm ischemic interval, the donor lungs were then flushed with 1 L of ECS and topically cooled as were the control grafts. ``Thirty-minute non–heart-beating donors'' (NHBD-30, n = 5) were ventilated with room air from the moment of cardiac death and continuing until a total of 30 minutes of warm ischemia had elapsed since the interruption of ventilation. The PA flush and topical cooling were then similarly carried out. All NHBD lungs were excised in the same manner as controls and placed in saline slush while the recipient pig was prepared.
Recipient Preparation and Transplantation Procedure
Twenty-three adult, size-matched swine served as left lung recipients. Recipients received 18 mg/kg of cyclosporine (Sandimmune, Sandoz Pharmaceuticals Corp, East Hanover, NJ) 1 day before transplantation. On the day of operation, anesthesia was induced similarly to donors and followed by intubation and ventilation with 100% oxygen. Azathioprine (1 mg/kg) and methylprednisolone (500 mg) were administered intravenously along with cefazolin (250 mg) before making the skin incision. Anesthesia was maintained with 1.5% isoflurane and the animals were anticoagulated with heparin sodium (200 U/kg). Through a left thoracotomy, the left lung was mobilized and the hilum dissected as in donor pigs. Dissection around the recipient bronchus was minimized. Care was taken to avoid injury to the phrenic nerve. The PA and bronchus were clamped, the pulmonary veins were doubly ligated, and the native left lung was excised.
The bronchial anastomosis was carried out using a running 4-0 monofilament polyglyconate suture (Maxon; Davis + Geck, Manati, PR). The bronchial clamp was removed upon completion of the airway anastomosis, and sigh breaths were administered to eradicate atelectasis. The airway anastomosis was examined under saline for evidence of leak. Graft ventilation with 100% oxygen was then continued during completion of the remaining anastomoses. The pulmonary arterial and left atrial cuff anastomoses were carried out with running 5-0 polypropylene sutures (Prolene; Ethicon, Somerville, NJ). At this time, the animal received a second dose of heparin sodium (100 U/kg). The vascular clamps were removed and the end of the ischemic interval was noted. Care was taken to deair the pulmonary vasculature. Intercostal nerve blocks were created using 0.25% buvipicaine HCl (Sensorcaine; Astra Pharmaceutical Products, Westborough, MA). A 28F chest tube was inserted through the seventh intercostal space. The chest was closed in layers, and the chest tube was connected to 20 mL of water suction.
All animals were readily extubated 1 hour postoperatively. Chest tubes were removed on postoperative day 1 and the animals were fed. Immunosuppression was continued daily for 7 days using cyclosporine (18 mg • kg-1 • day-1), azathioprine (1 mg • kg-1 • day-1), and methylprednisolone (500 mg/day). In addition, each animal received an aspirin tablet (325 mg) and cefazolin (250 mg) daily.
Data Collection
On postoperative day 7, each animal was anesthetized with xylazine, telazol, and atropine, and intubated. A chest radiograph was obtained to document normal aeration of the transplanted lung. A tracheostomy was then performed with insertion of a No. 9, shortened, cuffed endotracheal tube. The animal was ventilated with 100% oxygen. A 16-gauge catheter was placed by cut down in the left carotid artery for pressure measurements and blood gas analysis. A cordis introducer was placed in the right internal jugular vein for intravenous access, and a balloon-tipped PA catheter was floated into the pulmonary artery using wave forms to guide placement. Carotid artery, central venous, and PA pressures were continuously measured with a multichannel recorder (Hewlett Packard 78353BAu: location of HP, Waltham, MA). Flexible bronchoscopy was performed using a 3.5-mm outer diameter pediatric bronchoscope to rule out bronchial narrowing and to suction any secretions.
Pulmonary Airway Mechanics
Airway dynamic data were recorded during double lung ventilation and again after exclusion of the native right lung. Air flow was measured using a Fleisch No. 0 pneumotachometer that was connected through a differential transducer and an analog-to-digital converter (AII Devices, San Raphael, CA) to an Apple II microcomputer (model A2M2010; Apple, Cupertino, CAAu: location of Apple). Airway pressure was simultaneously recorded using a pressure transducer (model MP45-26-871; Validyne Engineering Corp, Northridge, CA). Pressure–volume loops were constructed from single tidal inflations by hand editing the three points of zero flow (beginning inspiration, peak inspiration, and end expiration) with a manual cursor and editor. Dynamic compliance was calculated as the slope of the line of best fit (least squares method) through the origin and apex of this pressure–volume relationship. Pressure–volume loops for the transplanted lung alone were then constructed by occluding the native right lung airways using 6F Fogarty balloon catheters (model CV1048; Baxter Healthcare Corp, Santa Ana, CA). These catheters were positioned in the right mainstem and eparterial bronchi under direct brochoscopic visualization and inflated under direct vision.
Pulmonary Vascular Dynamics
After completion of the airway dynamic measurements, a median sternotomy was performed to facilitate pulmonary vascular measurements. Accurate placement of the PA catheter into the PA was confirmed by palpation. Mean PA pressure (PAP) and pulmonary capillary wedge pressure (PCWP) were recorded at end expiration. Cardiac output (CO) was measured in triplicate by the thermodilution technique using the thermistor-tipped Swan-Ganz catheter. Double lung pulmonary vascular resistance (PVR) was calculated by the equation PVR = (Mean PAP - PCWP)/CO. The PA catheter then was pulled back into the proximal PA and the right hilum was totally occluded using a large vascular clamp. Care was taken to assure complete cessation of blood flow and ventilation to the native lung and the animal allowed to stabilize for 15 minutes. Repeat measurements of mean PAP, PCWP, and CO were recorded while the animal was maintained solely by the transplanted lung. The PVR of the transplanted lung was calculated as above.
Studies of Gas Exchange
Blood gas measurements were obtained under conditions of double lung ventilation and again 15 minutes after right hilar clamping. Animals were ventilated with 100% oxygen throughout the study. Double lung ventilation was carried out with a tidal volume of 15 mL/kg. Ventilation of the transplant lung after right hilar clamping was carried out with a tidal volume of 10 mL/kg. Blood gas samples were run on a Corning Blood Gas Analyzer (Corning 178 pH/blood gas monitor; Corning, Medfield, MAAu: location?). At the completion of the study, the animal was euthanized with a lethal dose of sodium pentobarbital. The transplanted lung was excised and biopsy specimen of each lobe were placed in 10% buffered formalin for histologic analysis.
Statistical Analysis
Measurements are reported as the mean ± the standard error of the mean. Analysis of variance was used to determine whether a difference existed between the four groups. Multiple comparison analysis was performed using Tukey's honestly significant difference test when the analysis of variance indicated a significant difference. Contrast analysis was performed to determine the significance of predefined questions. A p value of 0.05 or less was used to indicate a significant difference between measurements.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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The mean cold ischemic time from the moment of PA flush until the removal of the vascular clamps including all transplant operations was 84.8 ± 27 minutes. Mean cold ischemic times did not differ significantly among groups (Fig 1
). The total warm ischemia experienced in each experimental group, measured from the onset of apnea until cold PA flush, was carefully controlled in this experiment (Fig 2). The unventilated warm ischemic time (ie, the time between interruption of ventilation and cardiac death with resumed ventilation) varied with each harvest, as the rapidity of cardiac death from asphyxia was not under our control. Some pigs fibrillated after 5 minutes of apnea, whereas 1 animal maintained a perfusing cardiac rhythm for 15 minutes. However, the mean unventilated warm ischemic intervals for each NHBD cohort were similar (Fig 3).
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). As a group, all of the transplanted lungs exhibited decreased compliance compared to data recorded during combined ventilation of both native and transplanted lungs. No significant differences were noted in compliance among control, NHBD, and NHBD-15 grafts. However, NHBD-30 lungs were significantly less compliant (p = 0.02) when compared with lungs in the control, NHBD, and NHBD-15 groups combined.
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). Moderate pulmonary hypertension after native lung exclusion was noted in all groups including the control. However, no statistically significant differences were found when NHBD groups were compared to controls. The calculated pulmonary vascular resistance (Fig 6) demonstrated an increasing trend with longer preharvest ischemic intervals; however, this trend did not reach statistical significance.
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). These data reflect no decrease in the ability of the transplanted lung to oxygenate blood as preharvest warm ischemia increased over the range of 0 to 30 minutes.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Because of these unique characteristics, the lung may soon be harvested under non–heart-beating conditions. Such an approach would not be without precedent. Before the acceptance of brain death as the legal and ethical equivalent to physiologic death, all transplantation procedures were carried out using organs from cadaveric donors [21–23]. Furthermore, in several parts of the world today such as Japan, China, and Latvia, brain death has never been recognized officially [21, 22, 24]. Transplant surgeons in these regions have been compelled to harvest organs routinely from NHBD. Unfortunately, the vast majority of this clinical experience using non–heart-beating organ donation has been with renal and hepatic transplantation [5–8]. However, recent experimental evidence has accumulated supporting the utility of NHBD for extrarenal organs including the lung.
Using a nonsurvival model of canine single lung transplantation, Egan's group has proven that non–heart-beating lung donation is possible. Donor dogs were sacrificed and allowed to remain unventilated for 1, 2, or 4 hours before standard lung harvest. Recipient animals were studied for an 8-hour period after implantation during which the animal was rendered dependent on the transplanted lung by native lung exclusion. All recipients of 1-hour lungs survived the 8-hour study period with normal pulmonary hemodynamics and oxygenation. Only 2 of 5 recipients in the 2-hour group and 1 of 5 in the 4-hour group survived the study period. However, those that did survive maintained reasonable hemodynamics and gas exchange [11]. They concluded that non–heart-beating lung donation was possible and potentially, could increase the size of the lung donor pool.
Several other questions related to non–heart-beating lung donation have been addressed. Using a similar nonsurvival canine model in which lungs were subjected to 4 hours of warm ischemia, Ulicny and colleagues [12] have shown that ventilation during the warm ischemic interval enhances early dog survival as well as allograft gas exchange during the 8-hour period of reperfusion. In addition, preharvest ventilation with oxygen was superior to nitrogen ventilation; however, nitrogen ventilation still conferred a significant functional advantage when compared to unventilated controls. Finally, the addition of the free radical scavenger, dimethylthiourea, to the pulmonary flush after 2 hours of unventilated warm ischemia enhanced recipient survival but was unable to improve gas exchange or hemodynamics when compared with controls [14].
Although these acute studies have shown that non–heart-beating donation may be feasible in the realm of lung transplantation, we thought that survival studies would need to be carried out before applying this concept clinically. Shimada and colleagues [25] published a brief report of a survival model of canine lung transplantation after non–heart-beating donation in which oxygenation and PA pressures after native lung exclusion were equivalent to standard-harvest controls. To build on these initial studies, we adapted a porcine model of left lung transplantation with which we have had extensive experience [15]. In our model, allografts were harvested without warm ischemia (standard harvest), or after periods of ventilated warm ischemia of up to 30 minutes. Several parameters of lung function were studied including dynamic airway compliance, pulmonary vascular resistance, and gas exchange. The frequency of rejection was documented histologically. In an effort to make the model as rigorous as possible, we chose to ventilate with room air ventilation rather than 100% oxygen during the harvest procedure.
The administration of heparin before withdrawal of ventilator support in our model is controversial. Anticoagulation of a potential NHBD before physiologic death (in the setting of withdrawing support) or termination of resuscitative efforts (in the setting of trauma) raises ethical questions because it represents an intervention not in any way intended to benefit the still-living patient. Careful consideration of these ethical issues should be undertaken at any center contemplating non–heart-beating organ donation. From a purely physiologic standpoint, we believe that some form of effective systemic anticoagulation will prove to be an essential component of any non–heart-beating organ harvest.
In our study, we addressed specifically the following questions: Can lung transplantation after non–heart-beating donation be carried out successfully in a survival model? If so, will reperfusion injury, already a formidable problem for some recipients of lungs procured in the standard fashion, be more severe after non–heart-beating harvest? Will rejection be more likely after non–heart-beating donation? Finally, how much ventilated, warm ischemia will an allograft tolerate, particularly when challenged to function after a 7-day period of reperfusion and immunosuppression?
From the standpoint of oxygenation, pulmonary arterial pressure, and pulmonary vascular resistance, no differences were found among our control and study groups. These data indicate that reperfusion injury was not significantly exacerbated by short periods of warm ischemia during the harvest protocol. In addition, the rejection episodes we noted were distributed among all cohorts. Non–heart-beating lung harvest did not increase the likelihood of rejection in this study. However, the NHBD-30 group demonstrated significantly decreased dynamic airway compliance when contrasted with control, NHBD, and NHBD-15 groups. Thirty minutes seems to represent the period of warm ischemia that begins to have a measurable impact on pulmonary function in our model.
Lungs subjected to short periods of warm ischemia of up to 15 minutes function as well as those harvested in the standard fashion. However, our ``window'' of warm ischemia that results in lung function completely equivalent to nonischemic controls seems to be shorter than that noted in the previous nonsurvival studies. When compared with Egan's complete survival and excellent gas exchange after 1 hour of warm ischemia, our 15-minute window might be explained by our inclusion of the airway compliance measurement that is a sensitive marker of lung function in the setting of potential reperfusion injury [26]. Furthermore, the full 7 days of reperfusion and the effects of rejection and immunosuppression may have resulted in additional functional impairment not noted in previous acute studies.
Our data support the conclusion that non–heart-beating organ procurement is a viable option for increasing the number of available donor lungs. Lungs harvested with as much as 15 minutes of total warm ischemia function no differently after transplantation and 1 week of reperfusion than those harvested without warm ischemia. In addition, allograft rejection was no more likely to occur in the non–heart-beating harvest groups as in the control harvest group. However, lungs subjected to 30 minutes of total warm ischemia did exhibit significantly decreased airway compliance in the period after transplantation compared to the other groups. This impairment of airway compliance may indicate that 30 minutes of warm ischemia during allograft harvest exacerbates subsequent reperfusion injury. However, even these 30-minute lungs demonstrated acceptable gas exchange characteristics. We believe that the loss of compliance associated with 30 minutes of warm ischemia during harvest will likely prove to be a transient and manageable phenomenon. These data have important implications regarding the tolerance of the lung to warm ischemia as physicians consider the use of non–heart-beating organ donation in the clinical setting.
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Acknowledgments |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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We express our appreciation to Mr Anthony Herring for his invaluable technical assistance.
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Footnotes |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Address reprint requests to Dr Kron, Division of Thoracic and Cardiovascular Surgery, Box 310, Department of Surgery, University of Virginia Health Sciences Center, Charlottesville, VA 22908.
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