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Ann Thorac Surg 2006;81:2014-2019
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Evaluation of Techniques for Lung Transplantation Following Donation After Cardiac Death

^a Lung Transplant Service, Alfred Hospital and Monash University, Melbourne, Australia
^b Department of Pulmonary Medicine, University Hospital of Lund, Lund, Sweden
^c Department of Cardiothoracic Surgery, Alfred Hospital and Monash University, Melbourne, Australia

Accepted for publication January 3, 2006.

^_* Address correspondence to Dr Snell, Lung Transplant Service, Alfred Hospital, Commercial Rd, Melbourne 3004, Australia (Email: g.snell{at}alfred.org.au).

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
BACKGROUND: Lung transplantation using "donation after cardiac death" donors is a potential means to alleviate the shortage of suitable donor lungs for transplantation, but the practicality and utility of the various possible techniques need to be clarified.

METHODS: Using a dog model, we explored seven variations of standoff (ischemic) time (50 to 240 minutes), topical cooling (60 to 120 minutes), and flush cooling and cold storage (30 to 140 minutes) to mimic different human donor lung retrieval scenarios that can follow donation after cardiac death. The functional status of donation after cardiac death donor lungs was assessed initially with a 250 mL pulmonary arterial blood flush while ventilating with 100% oxygen and then on an ex-vivo perfusion rig for 120 minutes after retrieval.

RESULTS: All lungs achieved an excellent pO₂/FiO₂ ratio ranging from 472 to 586 with stable pulmonary artery pressures and pulmonary vascular resistance and no net weight gain (952 ± 221 g versus 1,006 ± 235 g) during the 120-minute evaluation period. Initial blood flush correlated well with measured perfusion rig pO₂ at 30 minutes (R² = 0.63).

CONCLUSIONS: This canine study suggests that lungs donated after cardiac death are reproducibly useable for transplantation with ischemic times of as long as 60 minutes. Although more study is needed, a blood flush evaluation is simple and may have a role as a secondary allograft assessment tool. The existing techniques of donor lung evaluation and preservation after donation following cardiac death thus appear both feasible and practical.

	Introduction

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Lung transplantation as a therapy for the management of end-stage lung disease is limited in its applicability by a lack of donor organs. Lung transplantation utilizing donation after cardiac death (DCD) donors has the potential to provide a previously untapped source of lungs for transplantation [1, 2]. As well as increasing overall numbers, DCD transplantation would allow organ donation from a pool of persons who have expressed a wish to donate their organs, facilitating lung donation from outside the intensive care unit, and potentially providing organs less damaged by the catecholamine and endocrine storm that characterizes brain death [3].

Until now, very few human DCD donor lung transplantation procedures have been performed around the world [4]. Historically, the techniques for the assessment, preservation, and retrieval of DCD lungs have been characterized by the Maastricht category descriptor of the donor (Table 1) [5]. Nunez and colleagues [6] describe a technique that has been utilized for Maastricht category I retrievals; Steen and colleagues [7], a single category II retrieval; and Love and coworkers [8], category III retrievals. These different strategies have evolved in response to local legal and donor pool circumstances (ie, prior existence of a local renal DCD program). Notwithstanding how they have been previously utilized, the variations in technique have different strengths and weaknesses that need to be carefully considered for the wider clinical application of DCD lung transplantation.

This study aimed to use an animal model to critically review and apply all existing DCD lung assessment, preservation, and surgical techniques to a range of scenarios that would cover all four Maastricht category DCD donors. The primary outcome will be the assessment of the potential allograft on an ex-vivo perfusion circuit [7, 9], utilized as a surrogate for transplantation. The studies aim to mimic the real-world clinical context of local and distant donation, and the issue of a DCD lung transplantation as part of a DCD donor multiorgan procurement.

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Animals and Anesthesia
Seven greyhound dogs weighing 28 to 34 kg were used for seven DCD lung experiments (including one combination lung, liver, and renal procedure). The experiments were structured to explore the practicality and relative efficacy of different permutations of warm ischemic time, cold preservation technique (topical cooling versus pulmonary artery flush cooling), and graft assessment technique (blood flush versus ex-vivo perfusion rig). The experimental protocols are detailed in Table 2. Experiment 1 was a negative control experiment without standoff time (ST) but as might be seen for in-house category III or IV DCD donors. Experiments 2 through 4 added 60 minutes of ST, mimicking an in-house category I through IV donor and varied the preservation technique. Experiment 5 mimicked a typical distant category I or II donor scenario with the need for graft assessment and retrieval. Experiment 6 was proposed as a positive control experiment of the effects of prolonged warm ischemia and ST. Experiment 7 represented a typical in-house category III or IV DCD donor multiorgan retrieval scenario.

All animals received premedication with subcutaneous 0.1 mg/kg acetylpromazine and intramuscular 0.05 mg/kg atropine and 0.2 mg/kg morphine. For the induction of anesthesia, 6 mg/kg propofol and 10 mg morphine were given intravenously. An infusion of propofol 0.5 mg · kg^-1 · min^-1 followed to maintain anesthesia. A cuffed tracheal tube was introduced, and lungs were ventilated 10 mL/kg on air at 20 breaths per minute through a volume cycle ventilator. Heparin sodium 10,000 IU was administered intravenously for anticoagulation. Three hundred milliliters to 500 mL blood was removed and leucocyte filtered (R-500N, Sepacell; Asahi Medical, Tokyo, Japan) for use in the perfusate and lung evaluation bolus flush, while 0.9% saline was infused to maintain arterial blood pressure. Ventricular fibrillation was induced by electrical stimulation using a needle electrode, and the ventilator was then disconnected.

The onset of ventricular fibrillation defined the onset of the warm ischemic time (WIT). Procedure time represented dissection and organ manipulation time, and may have resulted in slow cooling or warming of the organs depending on the circumstance. Cold ischemic time (CIT) was measured from the onset of the infusion of cold fluid.

Lung Preservation
Topical lung cooling was achieved by infusing 2.8 L 4°C Perfadex solution (Vitrolife, Gothenberg, Sweden) into each pleural space through 16F intercostal catheters (Trocar, Argyle, Ireland), as previously described [7, 9–11]. Pulmonary artery flush cooling was achieved by infusing 50 mL/kg 4°C Perfadex solution through a 24F catheter (DLP, Grand Rapids, Michigan), as previously described [7, 9–11]. The left atrial appendage was incised for venting and blood gas sampling (see below). Subsequently the catheter was removed, and the heart-lung block excised and stored at 4°C.

Extracorporeal Perfusion Circuit Preparation
The perfusate for extracorporeal perfusion consisted of 2 L Steen Solution (Vitrolife, Gothenberg, Sweden) mixed with 300 to 400 mL autologous leucocyte-filtered blood, trometamol buffer 20 mL (1.25 g/mL [THAM; Abbott, Sydney, Australia]), and Meropenem 500 mg (Merck Sharp & Dohme, Sydney, Australia). The final concentration was made up to achieve a hematocrit of 18% [9, 10]. The circuit consisted of a oxygenator (SX10 Terumo Cardiovascular Systems, [Austin, Texas], used here as a deoxygenator), centrifugal pump (Jostra AG, Hirrlingen, Germany), heater/cooler (Biocal 370, Anaheim, California), and continuous dual channel in-line blood gas analyzer (500; Terumo Cardiovascular Systems) [1, 9, 10]. The heart-lung block completed the circuit (see below). Oxygen and carbon dioxide and nitrogen were supplied to the membrane oxygenator at flow rates that are adjusted so that the blood entering the lungs through the pulmonary artery catheter had a blood gas analysis profile as would be seen in normal venous blood.

Heart-Lung Block Retrieval and Establishment of Ex-Vivo Perfusion and Ventilation
A midline sternotomy was performed, and the heart cannulated according to the technique of Steen and associates [7, 9] and Rega and coworkers [10]. In brief, the right ventricle and left atrium were opened widely to inspect for clot and the pulmonary artery cannulated through the right ventricle with a 28F aortic cannula. The left atrium was similarly cannulated through the left ventricle, using a 36F two-stage venous cannula. Left atrial and pulmonary arterial pressures were directly monitored by catheters placed in-situ. After appropriate deairing, the initial 200 mL of blood perfusate flush was discarded, and the extracorporeal circuit was connected at a low flow rates. The lungs were gently warmed and then ventilated (Servo 900C; Siemens, Melbourne, Australia) through an endotracheal tube, achieving 4 L/min blood flow at 37°C and 10 mL · kg^-1 · min^-1 ventilation at a positive end-expiratory pressure of 5 cmH₂0 and FiO₂ of 0.5 over 30 minutes [4].

Abdominal Organ Perfusion Circuit Preparation and Organ Retrieval
For the multiorgan experiment, an additional parallel circuit was created [12, 13], and the liver and kidney were retrieved using the DCD donor "super rapid" retrieval technique of Casavilla and coworkers [14].

Assessment
The outcomes for DCD lung evaluation included pulmonary arterial pressure, calculated pulmonary vascular resistance, left atrial PO₂, and weight after explant versus weight after ex-vivo perfusion. Measurements were performed at 5-minute intervals for the first 30 minutes, 10-minute intervals for the next 30 minutes, and thereafter every 30 minutes. After 120 minutes, left atrial pO₂ was assessed at a FiO₂ of 0.21 and 1.0 after 10 minutes stabilization time. A 250 mL autologous blood bolus was given to 4 animals to assess graft function before flush cooling. That followed a 2-minute period of ventilation with 100% oxygen and initial washout flush of cold Perfadex [6]. After the blood bolus and atrial sampling, ventilation again ceased, and the remainder of the cold Perfadex was flushed through. The temperature-corrected left atrial pO₂ was then used for comparison against the ex-vivo perfusion rig value at 30 minutes after reperfusion.

	Results

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The seven experiments resulted in actual overall total graft ischemic times that ranged between 50 minutes and 425 minutes (Fig 1 and Table 3), and notably, five experiments had an ST of 60 minutes or more.

View larger version (24K): [in this window] [in a new window]   Fig 1. A schema outlining the seven donations after cardiac death donor lung retrieval, preservation, and evaluation experiments. The timing bars are not exactly to scale. (Solid line = stand-off time; dashed line = rig evaluation; braided line = cold ischemia; solid/dash line = procedure time; down arrows = blood flush evaluation.)

View larger version (22K): [in this window] [in a new window]   Fig 2. Donation after cardiac death donor lung outcome measures versus time on the ex-vivo perfusion rig. (a) The left atrial pO2 at FiO2 0.5 (except for last 2 marked time points, which are as marked). (b) The pulmonary artery pressure (PAP) versus time. (c) The pulmonary vascular resistance (PVR) versus time. (Diamond = experiment 1; box = experiment 2; triangle = experiment 3; cross = experiment 4; asterisk = experiment 5; circle = experiment 6; hatch mark = experiment 7.)

View larger version (11K): [in this window] [in a new window]   Fig 3. Blood flush pO2 versus ex-vivo perfusion rig pO2. Boxes indicate individual points.

In the single multiorgan retrieval and rig evaluation (experiment 7), the liver and kidney were subjected to a total of 30 minutes WIT and 115 minutes CIT before rig evaluation for 240 minutes.

	Comment

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
These experiments confirm the practical potential of DCD lung transplantation. In 5 of 5 experiments where lungs were subjected to a complete ST of at least 60 minutes, they performed as well as those immediately retrieved and evaluated. The method of topical cooling is simple and can potentially precede the technically more demanding traditional flush cooling approach to lung preservation. Although more study is needed to validate its underlying accuracy and clinical utility, the blood flush evaluation is also simple and potentially provides a secondary assessment mode beyond that of clinical judgment and the more complex ex-vivo perfusion rig evaluation.

This work is consistent with that from other animal studies and limited human reports [7, 9, 14]. The lung appears unique, at least in terms of the solid organs, in being able to tolerate a prolonged period of warm ischemia. We note that within the described WIT timeframes outlined above, the techniques and tools now exist for lungs to be transplanted from any of the four Maastricht DCD donor categories, subject to local ethical, legal, and resource constraints.

Category I and II DCD donors represent the most difficult situations for DCD liver and renal transplantation, when timelines for organ procurement and assessment are almost impossibly challenging. However, as shown in experiments 2 through 7, lung transplantation appears conceivable even when the time limitation for other organs has expired. Experiment 5, in particular, represents a potential scenario in which DCD donor lung retrieval could hypothetically be facilitated by a relatively junior nontransplant surgical fellow, working in a small hospital and following an agreed protocol, to initiate topical cooling. That would allow time for the transplant surgical team to be assembled on site for a detailed assessment (through history, radiology), retrieval, and flush cooling for transport back to the transplant center.

Nunez and coworkers [6] have performed a small number of human DCD donor lung transplants from category I donors. Their technique differs from the experimental design employed by us in the use of assisted ventilation and an externally applied cardiac massage device. This type of support has been limited to 120 minutes in duration and is followed by topical cooling to preserve the lungs. A blood flush is used for lung evaluation. Five long-term survivors from 5 lung transplants are reported, with no patient having an early pO₂/FiO₂ less than 150 mm Hg [6]. It is not clear whether the assisted ventilation and cardiac massage have a net positive effect on lung quality, and indeed, our experiments 5 and 6 strongly suggest these interventions appear not to be necessary for lung retrieval alone.

Steen and colleagues [7] report a single lung transplant from a category II DCD donor. They describe an initial 105 minutes of WIT (including initial cardiopulmonary resuscitation attempts, with a subsequent 55 minutes of ST) before topical cooling, ex-vivo rig assessment, and finally lung transplantation. Early and intermediate-term graft function at 5 months was excellent. The ex-vivo circuit confirmed the excellent potential of the donor lungs, but this approach requires significant resources. Our experiments 2 through 6 reproduce this clinical situation and show it is feasible to perform a standard pulmonary artery flush after initial topical cooling for ease of transport.

There are a brief report [8] and anecdotes [4] regarding the retrieval of category III donor lungs. Love and associates [8] reported 5 cases with a mean WIT of 28 minutes (range, 19 to 40). No early graft failure was noted, and long-term function appeared satisfactory [8]. Category IV donor retrieval is limited to one positive anecdotal report [16]. We consider our experiments as supporting the safety of utilizing these category II and IV donors. With an expected WIT under 60 minutes, the retrieval team can move typically straight to pulmonary artery flush preservation (experiments 1, 2, 4, 6, and 7). Alternatively, if there are family or medical concerns or operating room access issues, then topical cooling can be instituted easily and rapidly, allowing many more hours to solve these problems (experiments 3 and 5) [11].

The simultaneous multiorgan retrieval of lungs, livers, and kidneys has been performed as part of the category I and III retrievals reported by Nunez and colleagues [6] and Love and associates [8], respectively, but as yet no details are published. In fact, only one animal study exploring the technique of multiorgan retrieval is available from the literature [17]. It is evident that DCD renal and liver retrieval with a restricted WIT (including ST) of 30 minutes or less requires primary consideration of the preservation of these organs rather than the lungs. In fact, the shorter lung allograft WITs likely in all multiorgan retrieval scenarios probably allow lung retrieval based on standard clinical judgement without the requirement of ex-vivo circuit evaluation.

There are limitations of the present study design. Firstly, multiple repeat experiments of each technical variation were not performed, as the aim was to evaluate the practicality and feasibility of existing methods across a range of different clinical scenarios (and when used additively), rather than restudying in depth one technique that may only apply to one clinical scenario or Maastricht category donor. Importantly however, we did have 5 scenarios with 60 minutes or more of ST, and irrespective of how the organs were then preserved and retrieved, it was possible on each occasion to show excellent lung function.

Secondly additional perioperative factors, both negative (namely, protracted premortem hypotension [18], the prospects of category I and II death from pulmonary emboli, and the effects of extended resuscitation) and positive (namely, potential reinstitution of postmortem donor ventilation with oxygen [15, 19], retrograde allograft flushing [20], or nitric oxide administration [21]) must also be considered in a human clinical situation.

Thirdly, the model required heparin administration to the donor to allow significant venesection. In the category I and II DCD human donors, this is an unlikely prospect and the timing and route of anticoagulation remain a issue for further study [4, 9]. Heparin and morphine have even have protective effects against graft ischemia-reperfusion injury in their own right [22].

Fourthly, although the ex-vivo perfusion rig described has been utilized similarly elsewhere in the evaluation of lungs for transplantation and represents a practical surrogate for transplantation [4, 7, 9], the blood flush has been clinically utilized in only one study [6], and basic mechanistic and practical questions about blood temperature, flow rate and efficacy remain. It is noteworthy that neither the perfusion rig nor blood flush have yet been shown to be accurate clinical outcome predictors at low levels of graft performance. However, the intriguing concept of supportive normothermic reperfusion and allograft resuscitation while on the perfusion rig is being studied further [4]. Steen's work suggests it is possible that a period of gentle normothermic reperfusion may actually let the lungs recover and be superior to traditional cold flush perfusion alone [9, 11]. Ultimately though, the perfusion circuit (and indeed animal models) cannot tell us about all of the unique circumstances of human transplantation, such as the incidence of airway complications [23] or bronchiolitis obliterans syndrome [24] using different techniques and varying WITs, and human clinical studies are required.

In conclusion, the variously described techniques of DCD donor lung evaluation, preservation, and transplantation appear both feasible and practical. Donation after cardiac death donor lung allograft evaluation tools such as basic clinical data (premortem pO₂/FiO₂ ratio, chest radiograph, and so forth), the blood bolus flush, and the ex-vivo rig, now warrant further study in a clinical human context. The range of techniques available and the apparent surprisingly robust nature of the lung allograft suggest significant potential for DCD donor lung transplantation.

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The Alfred Foundation, the Lilly Foundation, CARG (Roche Australia), the Australian Rotary Health Research Fund, and the Rotary Club of Williamstown all provided funds for this study.

	References

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Takahiro Oto Leif Eriksson Franklin Rosenfeldt Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Snell, G. I. Articles by Rosenfeldt, F. Search for Related Content PubMed PubMed Citation Articles by Snell, G. I. Articles by Rosenfeldt, F. Related Collections Lung - transplantation