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Ann Thorac Surg 1997;63:345-351
© 1997 The Society of Thoracic Surgeons
Departments of Cardiothoracic Surgery and Anesthesiology and Intensive Care, University Hospital of Lund, Lund, Sweden
Accepted for publication September 10, 1996.
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Methods. Domestic pigs were used (6 donors and 6 recipients) with a mean body weight of 59 ± 3 kg. Ventricular fibrillation was induced, and after 1 minute, cardiac massage was started and heparin (5 mg/kg body weight) was given via a central venous catheter. Cardiac massage was continued for 10 minutes, during which the pig was ventilated with 50% oxygen. The pleural cavities were opened and the tracheal tube disconnected from the ventilator, with the result that both lungs deflated. Saline slush was placed in both pleural cavities so that it completely covered the lungs. Within 40 minutes the lung core temperature was less than 10°C, and it was kept around 8°C for 6 hours by adjusting the amounts of ice slush. The left lung was then harvested and transplanted into a prepared recipient, followed by right pneumonectomy within 46 ± 4 minutes, thus making the recipient pig 100% dependent on the transplanted cadaver lung.
Results. The mean ischemic time for the cadaver lungs was 8 hours and 2 minutes (range, 7 hours and 25 minutes to 8 hours and 59 minutes). All animals remained in excellent condition throughout the 24-hour observation period, with arterial oxygen tensions of approximately 225 mm Hg, or 30 kPa (inspired oxygen fraction, 0.5).
Conclusions. Lungs from non-heart-beating donors may be used for transplantation if heparinization and topical cooling can be initiated within minutes of irreversible cardiac arrest.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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To make the study clinically relevant, the experiment was designed to simulate a common situation: a person suffers cardiac arrest, cardiopulmonary resuscitation is started within minutes but is unsuccessful, and the physician responsible decides to stop the resuscitation. If, in such a situation, the deceased has a valid donor card, it is mandatory to accept his or her great gift, if at all possible, from a pathophysiologic and ethical point of view.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Donor Pigs
Anesthesia was induced with intramuscularly administered ketamine (Ketalar; Parke-Davis, Morris Plains, NJ) at a dose of 30 mg/kg body weight. Thiopental sodium (Pentothal; Abbott Laboratories, North Chicago, IL) at a dose of 5 to 8 mg/kg and atropine (Kabi Pharmacia, Uppsala, Sweden) at a dose of 1 mg were given intravenously before tracheostomy (No. 8.5 tube). Anesthesia and muscular relaxation were maintained with a continuous infusion of a mixture of 8 g of ketamine (50 mg/mL; Parke-Davis), 300 mg of pancuronium bromide (2 mg/mL; Pavulon, Organon Teknika, Boxtel, the Netherlands), and 30 mg of midazolam (5 mg/mL; Dormicum, Roche, Basel, Switzerland) dissolved to 500 mL in 10% glucose and given at a rate of 30 mL/h. The animals were ventilated with a Siemens Seroventilator 300 (Siemens-Elema AB, Solna, Sweden). A volume-controlled, pressure-regulated ventilation of 10 L/min (20 breaths/min; positive end-expiratory pressure, 8 cm H2O; inspired oxygen fraction, 0.5) was used. After median sternotomy a 4-0 Prolene suture (Ethicon, Somerville, NJ) was placed, but not tightened, around the proximal right coronary artery and around the proximal left anterior descending coronary artery. The free ends of the sutures were pulled through two long tourniquets, which were brought to the outside of the thoracic wall through stab wounds. The sternotomy was then closed. The tourniquets were tightened, and ventricular fibrillation occurred within minutes. One minute after ventricular fibrillation had commenced, internal cardiac massage was initiated through a subcostal incision. Heparin (5 mg/kg body weight) was given via a central venous catheter at the same time as the cardiac massage was started. After 2 minutes of cardiac massage (and 2 minutes after heparin was given), blood was taken from the arterial catheter and a Hemochron test initiated. The cardiac massage and ventilation were continued until the Hemochron time exceeded 480 seconds. It was not necessary to give a second dose of heparin to any of the pigs. After 10 minutes of cardiac massage, the sternum was opened, the mediastinal pleura on both sides incised, and the superior and inferior cavae clamped. The tracheal tube was disconnected from the ventilator, with the result that both lungs deflated. Saline ice slush was put into the mediastinum and both pleural cavities so that it completely covered both lungs, which were protected by compresses. The core temperature of the lung was measured with a Foley catheter equipped with a temperature probe in its tip. The Foley catheter was brought deep into the right lung through a small incision in the pulmonary artery. A threadlike temperature probe (0.5 mm in diameter) was inserted into the right lung parenchyma to measure the temperature in the deep part of the lung. Within 40 minutes the lung core temperature was less than 10°C (Fig 1
), and it was kept around 8°C (range, 6°-12°C) by adjusting the amount of saline ice slush. After 6 hours, the heart and lungs were excised and the left lung dissected out with a large cuff around the left pulmonary veins. During this dissection, the lungs were kept in cold saline (8°C).
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A right thoracotomy was accomplished through the seventh intercostal space. The pulmonary ligaments were cut with a diathermy unit up to the hilus, and the pericardium was opened posterior to the phrenic nerve, thus rendering the lung hilus easily accessible to a TA-90 stapler. A left thoracotomy was performed through the sixth intercostal space, followed by a left pneumonectomy, care being taken to leave long ends to the pulmonary veins. The left main bronchus was occluded near the carina with a Satinski vascular clamp. This operation was carried out during the 6 hours that the cadaver donor lung was being cooled in situ. The cadaver lung was then transplanted into the recipient. The bronchial anastomosis was performed first with a running 4-0 Prolene suture. A gracile Satinski vascular clamp was placed intrapericardially across the lateral wall of the left atrium, incorporating the stumps of the three to four left pulmonary veins. Great care was taken to avoid occlusion of the coronary sinus or venous return from the infracardiac lobe of the right lung. An atrial cuff was then formed by making an incision joining the superior and inferior pulmonary veins. The atrial anastomosis was performed with a running 5-0 Prolene everting suture, which was left untied. A vascular clamp was placed on the proximal part of the pulmonary artery and the pulmonary artery anastomosis performed with a running 6-0 Prolene suture. The Satinski clamp on the bronchus was removed and ventilation started. The pulmonary artery clamp was removed, and when blood reached the atrial suture line, the clamp was removed from the left atrium and the atrial suture tied. A catheter for measurement of the left atrial pressure was inserted into the left atrium through a pursestring suture in the appendage. A blood flow probe (14 mm) was placed around the left pulmonary artery and the flow continuously monitored on a Transonic Flowmeter T201D (Transonic Systems Inc, Ithaca, NY). Within 10 minutes of starting ventilation, all atelectases disappeared in response to a temporary increase in the positive end-expiratory pressure from 8 to 15 cm H2O. The left thoracotomy was closed with the help of towel clips, and the animal was placed with its right side up. Right pneumonectomy was quickly carried out with the help of a TA-90 surgical stapler (United States Surgical Corporation, Norwalk, CT).
The pig was then placed with its left side (ie, the transplanted lung side) up again. The transplanted left lung was inspected to ensure that no atelectasis was present (a temporary increase in the positive end-expiratory pressure to 15 cm H2O being used to eliminate atelectasis if present). The ventilator was then set for the rest of the experiment to give a volume-controlled and pressure-regulated minute volume of 10 L/min delivered at a rate of 20 breaths/min, a positive end-expiratory pressure of 8 cm H2O, and an inspired oxygen fraction of 0.5.
The hydration during the 24-hour experimental period was kept constant in all animals and consisted of 720 mL of 10% glucose (ie, the anesthetic infusion given at 30 mL/h), 400 mL of saline solution (ie, for cardiac output measurements with the thermodilution method), and 1,000 mL of 4% human albumin. No diuretics or any other medication was allowed during the 24-hour posttransplantation observation period.
The point at which blood flow was established through the transplanted lung was defined as time zero. Blood pressure was monitored continuously with Hewlett-Packard fluoroscopes (HP78353B and HP78342B; Hewlett-Packard, Andover, MA). Analog signals from the bloodflow meter, pressure monitors, and ventilator were continuously collected throughout the experiment on a computer supplied with a data acquisition system (Viewdac; Keithley, Rochester, NY). Signals were sampled 50 times per second, the pulmonary and systemic vascular resistance were continuously computed, and all graphs were displayed on the screen. Values were computed, displayed numerically, and updated every 5 seconds as the mean value of each variable over a period of 5 seconds. These data were also stored on the hard disk. To make the graphs comprehensible, they are based on mean values for every fifth minute.
Blood gases (ABL 500; Radiometer, Copenhagen, Denmark) and oxygen saturation (OSM 3, adjusted for the pig-mode; Radiometer), urine output, the hemoglobin level, and hematocrit were recorded every 4 hours throughout the experiment, as were cardiac output and the right ventricular ejection fraction, obtained using the Edwards Critical-Care Explorer Multiple Parameter Hemodynamic Monitor. Body temperature was measured with the temperature probe in the Swan-Ganz catheter.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Efficacy of Heparinization During Cardiac Massage
Heparin (5 mg/kg body weight) was given via the central venous catheter 1 minute after ventricular fibrillation had been induced and at the same time as cardiac massage was started. The Hemochron time for arterial blood in all 6 pigs was longer than 1,000 seconds, and there was no need for a second dose of heparin in any.
Donor Lung Ischemia and Donor Lung Temperature
The time from ventricular fibrillation to the start of cardiac massage was 1 ± 0 minute. During this time the lungs were ventilated with 50% oxygen and no cooling was initiated.
Cardiac massage was continued for 10 ± 0 minutes, during which the lungs were ventilated with 50% oxygen and no cooling given.
Eleven minutes after the start of ventricular fibrillation, cardiac massage and lung ventilation were stopped and topical cooling of the deflated lungs with saline slush was initiated. The lung core temperature and the temperature in the lung tissue during the whole 6-hour period in the non-heart-beating donor are shown in Figure 1
. As can be seen, the temperature initially decreased by about 1°C each minute, and 40 minutes after the start of topical cooling it was between 7° and 12°C.
The ischemic time for the cadaver lungs in situ was 6 ± 0 hours. The mean total ischemic time before the start of reperfusion was 8 hours and 2 minutes and ranged from 7 hours and 25 minutes to 8 hours and 59 minutes.
Condition of Recipient Pigs
Left pneumonectomy and left lung transplantation were performed in all recipient pigs without any complications, and right pneumonectomy was accomplished 46 ± 4 minutes after the start of reperfusion of the transplanted left cadaver lung. This caused no hemodynamic instability in any animal. All 6 animals were in excellent condition throughout the 24-hour observation period, with normal blood gas values (Fig 2; Table 1). The mean pulmonary arterial pressure was approximately 30 mm Hg, and the pulmonary vascular resistance was approximately 500 dyne•s•cm-5; neither showed any tendency to change over time (Fig 3). The right ventricular ejection fraction was stable at around 0.30 at a heart rate of approximately 105 beats/min (Fig 4). A slight hemodilution occurred during the experiment (Fig 5) because no blood was transfused. Urine production was good throughout the experiment without the use of diuretics (Fig 6). The dynamic lung compliance was around 25 mL/cm H2O, and it did not change during the observation period (Fig 7).
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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, the arterial oxygen tension throughout the 24-hour observation period was around 30 kPa with an inspired oxygen fraction of 0.5. The preoperative arterial oxygen tension in the recipient pigs with the same inspired oxygen fraction of 0.5 was 24 ± 2 kPa (see Table 1). In another study [2], we investigated the blood gas and hemodynamic values throughout a 24-hour period in 6 pigs equal in size to that of the pigs used in the present study. However, in these latter pigs only right pneumonectomy was performed and, using the same mode of ventilation as that used in the present study, the arterial oxygen tension was around 30 kPa, with the lowest measured values approaching 25 kPa (ie, as in the present study). The pulmonary vascular resistance in these "sham-operated" pigs was around 350 dynes•s• cm-5, as compared with 500 dynes•s•cm-5 in the present study. We have shown that one reason for the increased pulmonary vascular resistance in transplanted lungs is a reduction in endothelium-dependent relaxing factor function [4–6] and that this reduction may be mitigated by the inhalation of nitric oxide [7, 8]. We have also shown that a moderate reduction in endothelium-dependent relaxing factor function caused by prolonged cold storage can be reversible and normal conditions restored within 2 hours of reperfusion; 24 hours of reperfusion or more are needed to restore normal conditions in the event of a more severe reduction [9]. The dynamic lung compliance in the present study was in the range of 25 to 30 mL/cm H2O (see Fig 7), which is within the range obtained in "sham-operated" pigs of equal size in which right pneumonectomy was carried out [2]. The reason that we did not have a control group in the present study was that the results obtained were within normal ranges, except for the moderate increase in pulmonary vascular resistance. Normal arterial oxygen tensions on an inspired oxygen fraction of 0.5 are around 30 kPa in both humans and pigs. Because we did not expect supernormal blood gas values after topical cooling, we do not think that a control group would have added further information.
The Toronto group was the first to perform lung transplantation with long-term clinical success; in 1988 they published their experience in 11 patients who underwent single-lung transplantations for pulmonary fibrosis [10]. In these patients, the preservation of the donor lung was accomplished by immersing the deflated donor lung in cold solution, that is, by using topical cooling alone. Five of these lung transplantations were performed with good results using donor lungs harvested at remote sites with ischemic periods of up to 5.5 hours. In addition, a scattergram of postoperative alveolar-arterial oxygen gradients versus ischemic times ranging from 1 to 5 hours for 15 single-lung and eight double-lung transplantations performed in humans, using cold immersion of deflated lungs as the only preservation method, showed no relationship between the duration of ischemia and early lung function [11]. Thus, experience has shown that deflated nonventilated human lungs, like porcine lungs, can be very well preserved for at least 5.5 hours by topical cooling alone.
The first clinical lung transplantation was performed by Hardy and co-workers [12] in 1963 using a lung from a non-heart-beating donor. The recipient was a 58-year-old man with respiratory insufficiency resulting from repeated attacks of pneumonia caused by cancer in the left lung. It is very instructive to read how they obtained the donor lung [12]:
At approximately 7:30 PM on the evening of June 11, 1963, a patient entered the emergency room of the University Hospital in shock and with pulmonary edema secondary to a massive myocardial infarction. When it proved impossible to effect resuscitation with endotracheal tube ventilation, closed chest cardiac massage, and other measures, a surgical resident was called and he obtained permission for an autopsy from members of the family. Meanwhile, the closed chest cardiac massage and rhythmical ventilation of the lung with pure oxygen was continued by means of the endotracheal tube; heparin was injected into the heart; and the patient was removed promptly to the operating suite. A blood specimen was drawn for future crossmatching with that of the recipient....
The deceased donor was treated with ventilation using 100% oxygen and closed chest cardiac massage while the recipient was being prepared for operation. After left pneumonectomy in the recipient, the closed chest massage was stopped, a cadaver thoracotomy quickly performed, and the left lung removed along with the full length of the bronchus and with all left lung vessels preserved. The pulmonary artery was immediately perfused with cold heparinized glucose solution and a sterile tube tied into the bronchus of the excised donor lung, which was "rhythmically inflated with pure oxygen." The lung transplantation was performed, and during the time needed for vascular anastomoses, the donor lung was supplied with pure oxygen. The sterile bronchial tube was then removed and bronchial anastomosis performed, thereby completing the transplantation, which had lasted 3 hours. Another instructive part of the report is worth quoting directly [12]:
There had been some concern that the pulmonary edema of the donor lung, secondary to the myocardial infarction from which the patient died, might render this lung poorly functional. In fact, a considerable amount of frothy secretion had been aspirated from the bronchus. Nevertheless, as the intermittent positive pressure ventilation had been continued, the pulmonary edema had subsided. And by the time the anastomoses had been completed and the lung was being ventilated by the anesthesiologist, as he simultaneously ventilated the patient's own normal lung on the opposite side, there was no further evidence of pulmonary edema. Once again the value of positive pressure ventilation in reversing pulmonary edema had been demonstrated.
The pulmonary function of the transplanted lung was good with minimal pulmonary secretions and no pulmonary edema, and peripheral arterial oxygen saturation was excellent. A pulmonary angiogram obtained on the first postoperative day demonstrated a good perfusion of the transplanted lung. Unfortunately, the patient suffered renal insufficiency along with increasing malnutrition, which gradually sapped his strength and he died on the 18th postoperative day, with his lung function intact. Autopsy confirmed that the transplanted lung was in good condition, and microscopic study showed it to have normal architecture and virtually no evidence of rejection.
Hardy and co-workers' detailed description of the first clinical lung transplantation in which a donor lung was taken from a non-heart-beating donor supports the conclusions drawn in the present study, that is, that lungs from non-heart-beating donors can be used for clinical lung transplantation.
Findings from a study conducted by Egan and co-workers [13] indicate that lungs are surprisingly resistant to warm ischemia. For example, lungs retrieved from dogs 1 hour after death without any cooling of the animal or the lungs during that hour proved to have excellent gas exchange after transplantation. In another study using pigs conducted by Buchanan and co-workers [14], the recipient animals received lungs flushed with Euro-Collins solution 15 and 30 minutes after asphyxiation and were observed for 1 week before being investigated. This group of investigators concluded that up to 15 minutes of warm ischemia is acceptable in pigs before any form of preservation is needed. However, no results have yet been published from experimental survival studies examining the healing of the bronchial anastomosis in donor lungs from cadavers. Such studies are needed before the use of cadaver lungs should be introduced into clinical practice. Another important topic to be considered is the length of time that can pass after death without deleterious coagulation of blood occurring in the lungs, if systemic anticoagulation cannot be obtained immediately after resuscitation is stopped. The anticoagulant treatment of a potential donor during resuscitation raises ethical questions, because it represents an intervention not in any way intended to benefit the still-living patient [14]. However, a sternotomy similar to the one performed in the present study would not be needed in humans to gain access to both pleural cavities with saline slush; a small left-sided anterior thoracotomy through the fourth or fifth intercostal space would be enough. This is an excellent incision when quick access to the heart is wanted to perform internal heart massage or to exclude cardiac tamponade. This incision also allows easy access to both pleural cavities via the mediastinal pleura, either to ensure that no tension pneumothorax is present during resuscitation or to cool the lungs with ice slush after the resuscitation has been given up. From an ethical point of view, such an incision can never be questioned if it is done with the intention of obtaining more effective cardiopulmonary resuscitation. In the approaching era of artificial hearts, it may furthermore be mandatory to inspect the heart before deciding definitely that the patient cannot be helped by artificial circulation.
In conclusion, the use of lungs from a non-heart-beating donor in clinical lung transplantation is possible from a biological point of view, but it raises ethical questions that require careful consideration. In situ topical cooling of nonventilated lungs in a non-heart-beating donor seems to permit a grace period of at least 6 hours before the lungs need to be harvested. During that time, it should be possible to query the relatives of the deceased person about his or her wish to be an organ donor; this will also allow the time necessary to perform the obligatory blood tests and to prepare a recipient.
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Acknowledgments |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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