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Ann Thorac Surg 2003;76:244-252
© 2003 The Society of Thoracic Surgeons

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Original article: general thoracic

Transplantation of lungs from non–heart-beating donors after functional assessment ex vivo

^a Department of Cardiothoracic Surgery, Heart-Lung Division, University Hospital of Lund, Lund, Sweden

Accepted for publication January 24, 2003.

^* Address reprint requests to Dr Steen, Department of Cardiothoracic Surgery, Heart-Lung Division, University Hospital of Lund, SE-221 85 Lund, Sweden.
e-mail: stig.steen{at}thorax.lu.se

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
BACKGROUND: If lungs from patients dying of heart attacks are to serve as donor organs in a safe way, their function should be properly assessed before transplantation. The aim of this study was to investigate donor lung function evaluation in a realistic large animal model.

METHODS: Twelve 60-kg pigs were used. Five minutes after ventricular fibrillation was induced, cardiopulmonary resuscitation was initiated and maintained for 20 minutes. After a 10-min hands-off period, heparin was administered through a central venous catheter followed by 20 chest compressions. Intrapleural cooling was initiated after 65 minutes of warm ischemia. Cooling proceeded for 6 hours within the cadaver, after which lung function was assessed ex vivo. Recipient pigs underwent left lung transplantation followed by right pneumonectomy, thus making these animals 100% dependent for their survival on the function of the donor lungs.

RESULTS: The assessment showed that all lungs had adequate function to serve as donor lungs. All recipient animals were in good condition during the 24-hour observation period after the operation. The blood gas function did not differ significantly from that in the healthy donor animals before induction of ventricular fibrillation; pulmonary vascular resistance was within normal range.

CONCLUSIONS: Lungs from non–heart-beating donors topically cooled in situ for 6 hours after 65 minutes of warm ischemia were assessed ex vivo and found to have normal function. They were then transplanted and retained normal function during a 24-hour observation period.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
About a third of all deaths in the western world are caused by ischemic heart disease. Reported estimate are that 375,000 persons in Europe [1] and 275,000 in the United States [2] undergo sudden cardiac arrest yearly. Out-of-hospital cardiac arrest accounts for about half of all deaths due to cardiovascular disease [2]. If lungs from patients dying after sudden cardiac arrest are to serve as donor organs in a safe way in clinical lung transplantation, their function should be properly assessed before transplantation.

We have previously described how a lung from a non–heart-beating donor was successfully transplanted into a patient with end-stage pulmonary disease [3]. The donor was a 54-year-old man dying of acute myocardial infarction after failed cardiopulmonary resuscitation (CPR). The next of kin gave permission to cool the lungs within the intact body, and intrapleural cooling was started 65 minutes after death. After 3 hours of topical intrapleural cooling, the heart-lung block was excised and the lung function was assessed ex vivo with a modified heart-lung machine. After a cold preservation period of 8 hours, the right lung was successfully transplanted into a 54-year-old woman with chronic obstructive pulmonary disease. The ethics and experiments making this operation possible have been published elsewhere [3–11].

The aim of the present study was to describe in detail the method used for ex vivo assessment of lung function. To make the study clinically relevant, a large animal model was used, enabling use of exactly the same equipment as in the clinical case. The experiment was designed to simulate a typical situation in which transplantation of a topically cooled lung from a non–heart-beating donor is considered, after first testing its function. If the function is found to be satisfactory, one lung will be transplanted into a recipient animal followed by contralateral pneumonectomy, thereby making the recipient animal 100% dependent for its survival on the function of the donor lung. By comparing the lung function measurements obtained before induction of cardiac arrest in the donor animals with those obtained ex vivo and after transplantation, the function of the same lung can be followed throughout the experiment. Thus we can judge if the ex vivo assessment correctly predicts the posttransplantation function.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
The experimental design is shown in Table 1.

All animals received premedication with intramuscular ketamine (Ketalar, Parke-Davis, Morris Plains, NJ), 15 mg/kg body weight and xylasin (Rompun, Bayer, Gothenburg, Sweden) 0.2 mg/kg. For anesthesia induction sodium thiopental (Pentothal; Abbot, North Chicago, IL) 5 mg/kg body weight and atropine (Atropine; Kabi Pharmacia, Uppsala, Sweden) 0.02 mg/kg were given intravenously. Pancuronium (Pavulon, Organon Teknika, Boxel, The Netherlands) was given intravenously before the tracheotomy and introduction of the tracheal tube (Portex #8; Hythe, Kent, England). During the experiment, anesthesia was maintained using a mixture of 8 g ketamine, 30 mg midazolam (Dormicum, Roche, Basel, Switzerland), and 300 mg pancuronium bromide dissolved in 5% glucose to 500 mL as a continuous infusion of 30 mL/h.

Intermittent injections of fentanyl (Leptanal, Lilly, France) 0.02 µg/kg were also given throughout the experiments. The animals were ventilated with a Siemens Servo ventilator 300 (Siemens-Elema AB, Solna, Sweden). A volume-controlled, pressure-regulated ventilation of 10 L/min (20 breaths/min; positive end-expiratory pressure [PEEP], 8 cm H₂O; inspired oxygen fraction, 0.5; max inspiratory pressure, 30 cm H₂O) was used, if not otherwise stated.

A Swan-Ganz catheter was introduced into the pulmonary artery. Catheters were placed in the arch of the aorta through the right carotid artery and in the right atrium through the right internal jugular vein. The pig was kept in a supine position for 20 minutes, and base line hemodynamic values and blood gases were recorded using a data acquisition system (Testpoint; Capital Equipment Corp, Billerica, MA).

Cardiopulmonary resuscitation of the donor pigs
Ventricular fibrillation was induced by electrical stimulation and the ventilator (fraction of inspired O₂ = 0.21) was disconnected. The animal was left untouched with ventricular fibrillation for 5 minutes. Cardiopulmonary resuscitation was then initiated. Two surgeons working in 3-min intervals applied external chest compressions and ventilation was given with 100% oxygen with the ventilator. After 20 minutes, another blood gas sample was taken and the CPR was interrupted. No animal showed signs of return of spontaneous circulation, and after a 10-min hands-off period, the animals were declared dead. Heparin 25,000 IU was then given through the central venous catheter, followed by 20 external chest compressions. The tracheal tube was disconnected from the ventilator and exposed to air, a temperature probe was inserted deep into a bronchus through the tracheal tube, and another 45-minute hands-off period was initiated.

Intrapleural topical cooling
The thorax was covered with a surgical towel kit used for caesarian section. A 1-inch stab wound was made intercostally on each side, causing bilateral pneumothorax. Infusion of cold buffered Perfadex with added calcium chloride (1 mmol/L) from 2.8-L plastic bags (Vitrolife AB, Gothenburg, Sweden) was initiated 65 minutes after failed resuscitation through an intercostal tube (Portex 28F, Hythe, UK) placed deeply into each pleural space (Fig 1A). The infusion was run until the solution started to flow out of the wound, then a second intercostal tube was introduced superficially into the pleural space on each side through the original stab wound, which was closed by towel clips. The advantage of using towel clips to close the wound is that they can be removed quickly in case of a need to check the position of the intercostal tubes. Two other cold Perfadex bags were connected to the second pair of intercostal tubes, while the two empty Perfadex bags were placed in a container of ice water, situated with the water surface 5 cm higher than the highest point of the thorax of the donor (Fig 1B). This setup ensures that the lungs will be compressed by cold Perfadex from all sides with a pressure of about 5 cm H₂O, transforming the spongy lung tissue into a semisolid tissue, which can be cooled more efficiently. The tracheal tube must be open to the air, so that intrapulmonary air can escape when the lungs are compressed by the cold Perfadex solution. The intratracheal cuff must be well filled, to eliminate the risk of stomach contents flowing over into the bronchi. The caesarian section cover kit effectively eliminates all spilling of Perfadex solution onto the operating table.

View larger version (29K): [in this window] [in a new window]   Fig 1. Topical cooling of lungs in situ. (A) After the first pair of Perfadex bags (1) have been emptied into the pleural space on each side, (B) a second pair of bags (2) are infused, while the first pair (1) are immersed in ice water in containers placed so that the water surface is 5 cm higher than the most anterior part of the thorax cavity. By switching every time the infusion bags are empty, an efficient cooling is obtained. It is important that the tracheal tube is open to the air during these procedures. (C = spinal column; LL = left lung; RL = right lung.)

View larger version (65K): [in this window] [in a new window]   Fig 2. Assessment of lung function ex vivo. (A) Schematic of the evaluation system. (temp. = temperature.) (B) The heart-lung block is placed in the evaluation box ready for cannulation.

The pulmonary artery cannula was connected to the corresponding tube of the extracorporeal circuit, the air was removed, and the shunt of the circuit clamped. A low flow perfusion (100 mL/min) at 25°C was initiated through the lungs. The first 200 mL of blood exiting the cannula in the left atrium was discarded, and then the cannula was connected to the circuit. The lungs were gradually warmed by increasing the temperature of the evaluation solution, and when the temperature of the solution exiting the left atrium was 32°C, ventilation (1 L/min) was started. The pump flow was gradually increased, but the pulmonary artery pressure was never allowed to exceed 20 mm Hg. If a flow of 4 L/min was reached, it was fixed at that rate regardless of the pulmonary artery pressure, if it was less than 20 mm Hg. When the temperature of the solution exiting the left atrium was 37°C, full ventilation was given and the PEEP was temporarily increased to eliminate atelectases. Then the ventilation rate was fixed at 2.5 times higher than the perfusion flow, with a PEEP of 8 cm H₂O and an inspired oxygen fraction of 0.5 (Fig 3). When a steady state was reached, blood gases and hemodynamics were registered, after which the perfusion flow and ventilation were reduced while core cooling of the lungs to 20°C was accomplished with the heater-cooler unit. Perfusion was then stopped and the cannulas were removed. The left lung was dissected and prepared for transplantation. It was immersed in a semi-inflated state in the evaluation solution diluted by Perfadex to a hematocrit of about 5%. This solution was run continuously (4 L/min) through the oxygenator at 12°C (topical extracorporeal membrane oxygenation [ECMO]).

View larger version (133K): [in this window] [in a new window]   Fig 3. When the temperature of the blood coming out from the lungs is 32°C, ventilation of the lungs is initiated. At 37°C, full flow is run with a maximal mean pulmonary arterial pressure of 20 mm Hg. The lungs are ventilated with an inspired oxygen fraction varying between 0.21 and 1.0, with a respiratory minute volume 2.5 times the perfusion flow, and with a positive end-expiratory pressure of 5 to 8 cm H2O. After the evaluation, topical extracorporeal membrane oxygenation is performed within the same container.

Statistics
Values are given as mean ± standard error of the mean (SEM). Wilcoxon’s signed rank test was used, and a p value of less than 0.05 was considered as statistically significant.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Circulation during cardiopulmonary resuscitation
The end tidal carbon dioxide pressure (ETCO₂) varied between 2.1 and 2.5 kPa during the 20-minute CPR period and the arterial oxygen tension measured at the end of the resuscitation was 58 ± 9 kPa. The arterial pressure produced by the chest compressions was in the range of 60 to 80 mm Hg.

Intrapleural topical cooling
During the first hour, the intrabronchial temperature decreased by about 20°C, ie, by about 0.3°C/min (Fig 4). At the end of the second hour the temperature had decreased to less than 15°C and was maintained around 12°C by adjusting the rate at which the position of the bags was shifted (Fig 1).

View larger version (15K): [in this window] [in a new window]   Fig 4. Topical cooling of lungs. The intraluminal bronchial temperature probe was introduced through the tracheal tube deep into the bronchial tree. Mean ± SEM, n = 6.

View larger version (35K): [in this window] [in a new window]   Fig 5. Ex vivo assessment of lung hemodynamics. Mean ± SEM, n = 6. (LAP = left arterial pressure; MPAP = mean pulmonary artery pressure; PVR = pulmonary vascular resistance.)

Topical extracorporeal membrane oxygenation during storage until transplantation
Maintaining the temperature in the oxygenated solution surrounding the lung at 12°C was easy because of the heater-cooler unit, in accordance with the research protocol design.

Assessment of lung function after transplantation
All animals were in excellent condition throughout the experimental period. The gas exchange function did not differ significantly from base line (Tables 2 and 3, Fig 6). The PVR was around 400 dynes x s x cm^-5 (Fig 7), ie, within the normal range for sham-operated animals who had undergone only right pneumonectomy [5].

View larger version (34K): [in this window] [in a new window]   Fig 6. Blood gases during the first 24 hours of reperfusion. Right pneumonectomy was done after 6 hours. Inspired oxygen fraction = 0.5. Mean ± SEM, n = 6. (PaO2 = arterial oxygen pressure [tension]; PvO2 = venous oxygen pressure [tension]; SaO2 = arterial oxygen percent saturation; SvO2 = mixed venous oxygen percent saturation.)

View larger version (45K): [in this window] [in a new window]   Fig 7. Hemodynamics during the first 24 hours of reperfusion. Thermodilution (Swan-Ganz catheter) was used to calculate cardiac output during the first 6 hours. Right pneumonectomy was done after 6 hours, after which the cardiac output was measured continuously through a flow probe on the left pulmonary artery. Mean ± SEM, n = 6. (LAP = left arterial pressure; MAP = mean arterial pressure; MPAP = mean pulmonary artery pressure; PVR = pulmonary vascular resistance; SVR = systemic vascular resistance.)

	Comment

Top Abstract Introduction Material and methods Results Comment References

Besides the blood gases and PVR, a most valuable measurement to follow during the ex vivo evaluation is the difference between arterial carbon dioxide pressure and ETCO₂. With perfect perfusion of the lungs, this difference is close to zero. If the difference is more than 1, the PEEP should be temporarily increased to eliminate possible atelectases and a maximum perfusion flow, creating a perfusion pressure of 20 mm Hg, should be used. If the CO₂ gradient does not decrease to less than 1 under these conditions, suboptimal perfusion, eg, as a result of pulmonary emboli, should be suspected and such lungs should not be transplanted. In this situation, thrombolytic drugs may be added to the evaluation solution to check if the perfusion obstacles thereby are eliminated.

If there is doubt that the lungs can be used for transplantation, the evaluation equipment could be used to perform a test transplantation ex vivo. The potential recipient is then cannulated percutaneously and perfusion of the donor lungs is initiated by pumping venous blood from the recipient through the donor lungs and then back to the recipient through the oxygenator equipped with a heat exchanger (veno-venous ECMO). By this technique we have revitalized "bad" porcine donor lungs within 6 hours of reperfusion with fresh blood from the potential recipient, and thereafter successfully transplanted one lung.

We performed on the pigs for 20 minutes and administered heparin 10 minutes after we had stopped the resuscitation. During this short period of circulatory arrest we think the risk of blood coagulation within the lungs is minimal; in the present study we did not observe any clots. The low gradient between the arterial CO₂ pressure and ETCO₂ values confirmed the lack of any major ventilation-perfusion mismatch. The time period of 10 minutes was chosen to follow the Maastricht guidelines for a clear 10-min interval between cessation of resuscitation and any procedures solely for organ preservation [12].

In our clinical protocol, anticoagulation may be given to the deceased without permission from the next of kin, but nothing else is allowed to facilitate organ donation. Recently, a clinical prospective study was published indicating a better survival of administering thrombolytic therapy combined with heparin to patients with out-of-hospital cardiac arrest when return of spontaneous circulation was not achieved within 15 minutes [13]. Two other clinical studies have been published recently demonstrating the efficacy of therapeutic hypothermia for treating cardiac arrest [1, 14, 15]. Someday, patients who are declared dead after failed resuscitation may be both anticoagulated and cooled. Because of this, more time is obtained to find out if organ donation is suitable.

We are convinced that using lungs from non–heart-beating donors has the potential to eliminate donor shortages if the ethical questions can be solved in full agreement with the general public [3]. The ethical issues that arose in connection with our first clinical case were recently discussed in an influential American bioethics journal and the concept found to be sound [16].

Ex vivo assessment of donor lungs followed by topical ECMO may transform clinical lung transplantation into a procedure in which only properly evaluated lungs of high quality will be transplanted. Ex vivo assessment and treatment of lungs will also open up the possibility for a second positive judgment of initially rejected donor lungs from beating heart donors.

This study was supported by grants from the University Hospital of Lund and the Swedish Heart Lung Foundation.

	References

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10. Wierup P., Bolys R., Steen S. Gas exchange function one month after lung transplantation of lungs topically cooled for 2 hours in the non-heart-beating cadaver after failed resuscitation. J Heart Lung Transplant 1999;18:133-138.[Medline]
11. Wierup P., Andersen C., Janciauskas D., Bolys R., Sjöberg T., Steen S. Bronchial healing, lung parenchymal histology, and blood gases one month after transplantation of lungs topically cooled for 2 hours in the non-heart-beating cadaver. J Heart Lung Transplant 2000;19:270-276.[Medline]
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