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Eur J Cardiothorac Surg 2004;26:144-150
© 2004 Elsevier Science NL

Innovative pulmonary preservation of non-heart-beating donor grafts in experimental lung transplantation

^a Department of Cardiothoracic and Vascular Surgery, Friedrich-Schiller University, Bachstrasse 18, 07740 Jena, Germany
^b Department of Electron Microscopy, University of Göttingen, Germany
^c Clinical Research Group ‘Chronic Airway Diseases’, Department of Internal Medicine (Respiratory Medicine), Philipps-University Marburg, Marburg, Germany

Received 5 November 2003; received in revised form 19 January 2004; accepted 20 January 2004.

^* Corresponding author. Tel.: +49-3641-934-801; fax: +49-3641-934-802
e-mail: th.wittwer-md{at}t-online.de

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Comment References

 
Objective: Lung transplantation is limited by scarcity of donor organs. Lung retrieval from non-heart-beating donors (NHBD) might have the potential to extend the donor pool and has been reported recently. However, no studies in NHBD exist using the novel approach of retrograde preservation with Perfadex solution. Methods: Asystolic heparinized pigs (n=5/group) were continuously ventilated for 90, 180 or 300 min of warm ischemia. Lungs were then retrogradely preserved with Perfadex and stored at 4 °C in inflation. After 3 h of additional cold ischemia, left lung transplantation was performed. Hemodynamics, pO₂/F_iO₂ and dynamic compliance were monitored for 5 h. Intrapulmonary lung water was determined by both global wet-to-dry lung weight ratio (W/D ratio) and standard stereological examination of relative volume fractions of intraalveolar edema. All results were compared to sham-operated controls and to lungs obtained from standard heart-beating donors after retrograde preservation with Perfadex and 27 h of cold ischemia. Statistics comprised ANOVA analysis with repeated measures and Mann–Whitney tests. Results: No mortality was observed. During flush preservation of NHBD lungs, continuous elimination of blood clots via the pulmonary artery was observed. Oxygenation, compliance, intraalveolar edema fraction and W/D ratio were comparable between groups, whereas PVR was significantly lower in sham-controls. Conclusions: Use of NHBD lungs is feasible and results in similar postischemic outcome when compared to sham-controls and standard preservation procedures even after 5 h of pre-harvest warm ischemia. Especially, the NHBD with high-risk constellations for intravascular coagulation might benefit from retrograde preservation by elimination of thrombi from the pulmonary circulation. This innovative technique might also be considered in situations, where brain-dead organ donors become hemodynamically unstable prior to onset of organ harvest. Further trials with longer warm and cold ischemic periods are initiated to further elucidate this promising approach of donor pool expansion.

Key Words: Retrograde pulmonoplegia • Non-heart-beating donors • Perfadex lung preservation • Lung transplantation

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Comment References

 
Although lung transplantation has been proven to be an effective therapy for patients with end-stage pulmonary disease, access to this therapy is severely limited by the progredient scarcity of suitable donor organs in the last years [1]. Currently, aside from living-related organ donation, all suitable lung grafts are retrieved from brain-dead heart-beating donors. However, it is estimated that 35,000 people in the US are killed from firearms while 47,000 deaths are related to motor vehicle accidents [2]. If just a small portion of these acutely injured people after unsuccessful resuscitation were candidates for non-heart-beating organ donation, this might increase the number of available organs by up to 20–30% [3,4]. Lung retrieval from non-heart-beating donors (NHBD) is considered to be a realistic therapeutic option as the lung is unique among the transplanted solid organs in the way that it is not dependent on vascular perfusion to meet its oxygen needs. Experimentally, pulmonary cells obtained from ventilated cadavers have been cultured successfully, indicating lung parenchymal cell death does not necessarily occur at the time of clinical death [5]. Previous studies in our laboratory have shown that the quality of pulmonary preservation in terms of postischemic lung function can be significantly improved by the innovative technique of retrograde flush perfusion (RFP) via the left atrium into the pulmonary venous system [6]. However, there is no information so far concerning the feasibility of RFP with low-potassium dextran solution with regard to achievable quality of pulmonary preservation when NHBD-lungs with the high risk of microvascular thrombi formation are used for transplantation.

The present detailed study compared RFP in NHBD lungs of variable warm ischemic intervals with standard preservation procedures using heart beating donors and sham controls. The main rationale was to evaluate if the innovative strategy of retrograde preservation of NHBD lungs is feasible and safe in terms of postischemic outcome even with extended and clinically realistic ischemic intervals.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Comment References

 
2.1. Experimental groups
Female domestic pigs weighing from 28 to 32 kg were randomized into five groups of five animals each. One group served as a sham-operated control group (group 5) and was prone to surgical dissection of hilar structures, but neither organ preservation nor transplantation was performed. In the remaining groups, either NHBD lungs were preserved for 3 h of cold ischemia time (CIT) by RFP with LPD solution (Perfadex; Vitrolife, Göteborg, Sweden) after a variable ventilated warm ischemia time (WIT) of 90 (group 1), 180 (group 2) and 300 min (group 3), respectively, or lungs from standard heart beating donors were retrogradely preserved for 27 h of CIT. In all of these test groups (groups 1–4), five additional animals were used as lung recipients.

2.2. Surgical procedure
2.2.1. Donor preparation
All animals were premedicated with ketamine 10% (20 mg/kg), atropine (0.04 mg/kg) and propofol (3 mg/kg). Pigs were then put in the supine position, intubated and mechanically ventilated with 50% oxygen in a pressure-controlled mode with a peak inspiratory pressure of 20 mmHg, a rate of 18 breaths per minute, an inspiratory/expiratory ratio of 1:1 and a PEEP of 8 mmHg. Anesthesia was continued with infusion of fentanyl (0.3 µg/kg per min), midazolam (20 µg/kg per min) and pancuronium (10 µg/kg per min). All animals received 200 IE/kg of heparin intravenously. A median sternotomy was performed and the pericardium was opened longitudinally. A perfusion cannula with a sideport to measure the perfusion pressure was placed through the auricle into the left atrium. In NHBD lungs (groups 1–3), cardiac fibrillation was induced electrically, and the cadaver was ventilated at an F_iO₂ of 0.5 and left at room temperature for 90, 180 and 300 min of WIT, respectively. In the standard heart-beating group (group 4), no WIT was applied, and retrograde perfusion via the left atrium was started directly with an incision in the anterior aspect of the main pulmonary artery for drainage of the LPD solution. An 8 min period was required to infuse 1800 ml LPD solution at 4 °C with a maximum flushing pressure of 14 mmHg. Continuous topical cooling of the lungs was not performed in any group in order to specifically assess the impact of retrograde flush preservation. No prostaglandins were used neither in the donor animal nor in the preservation solution as the LPD solution induces significantly less vasoconstriction during flush preservation. Ventilation was continued throughout the entire perfusion period. After completion of the preservation, the heart–lung bloc was excised with both lungs inflated in an endinspiratory state and stored at 4 °C for 3 h.

2.2.2. Recipient/sham-preparation
The anesthetic regimen was identical to the donor procedure. A Swan-Ganz catheter (7.5F, Baxter Healthcare Corp., Irvine, CA, USA) and a catheter to monitor the arterial pressure (Leader Cath 20G 8 cm, Vygon, France) were placed into the right carotid artery and external jugular vein, respectively. All animals were placed in a right decubitus position, and a left thoracotomy was performed in the fifth intercostal space. The pulmonary bifurcation left main bronchus and left pulmonary veins were dissected in all groups. After clamping of the left pulmonary artery and bronchus, the left pulmonary veins were ligated and pneumonectomy was performed in the test groups (groups 1–4) only. The left donor lung was isolated from the heart–lung bloc and prepared for implantation with a large atrial cuff and full length of both the pulmonary artery and left main bronchus. Implantation of the donor lung started with the bronchial anastomosis using a running suture with 4–0 Prolene (Ethicon Inc., Somerville, NJ, USA) followed by the arterial anastomosis with a running suture of 6–0 Prolene. After clamping of the left atrium, a recipient atrial cuff was designed and anastomosed to the donor atrial cuff using a running suture of 5–0 Prolene. Prior to reperfusion, the donor lung was carefully de-aired retrogradely. The pulmonary artery was then unclamped and the graft reventilated in a pressure-controlled mode with a peak inspiratory pressure of 30 mmHg using a PEEP of 10 mmHg with a respiratory rate of 18/min. After 15 min of reperfusion, the contralateral right pulmonary artery and bronchus were clamped both in the sham-operated control group and all test groups. All lungs were reperfused for 5 h followed by termination of the experiment by intravenous injection of magnesium sulfate.

2.3. Functional analysis
In all experiments, arterial and pulmonary artery pressures as well as central venous and left atrial pressures were recorded continuously. Dynamic lung compliance was monitored by the ventilator (Evita 2 dura, Dräger Medical Inc., Lübeck, Germany). An arterial and mixed-venous blood gas analysis was performed initially and in 30 min intervals during the reperfusion period. Cardiac output was measured continuously by the Swan-Ganz catheter, and systemic and pulmonary vascular resistances were calculated.

2.4. Stereological analysis
After completion of the reperfusion period, the entire left lung was further processed for light microscopy by fixation using vascular perfusion via the pulmonary artery with 2 l of a 1.5% paraformaldehyde/glutaraldehyde solution in 0.1 M cacodylate buffer at 15 cmH₂O pressure. During this fixation the lung was inflated with a constant pressure of 12 cmH₂O. In order to collect lung material, which is representative for the whole lung, systematic random sampling of tissue was performed. Lungs were cut into 10 mm thick slices. A transparent paint grid was then superimposed over the section of slices. Whenever a point hit the surface of the lung slice, a 1 cm³-tissue block was excised. The tissue was dehydrated through a graded series of ethanol and embedded in a methacrylate resin (Technovit 7100, Kulzer, Heraeus, Germany). Sections of 1 µm were cut from each block (10–12 per lung) and stained with methyleneblue/Azur II (1:2). The relative volume fraction of intraalveolar edema formation referred to lung parenchyma was determined by established stereological techniques [7] using a Cast-Grid-System 2.0 (Olympus, Denmark).

2.5. Animal care
All animals received humane care in compliance with the European Convention on Animal Care and with the, ‘Principles of Laboratory Animal Care’, formulated by the National Society for Medical Research and the, ‘Guide for the Care and Use of Laboratory Animals’, prepared by the Institute of Laboratory Animal Resources, National Research Council, and published by the National Academy Press, revised 1996. The study was approved by the institutional ethics committee.

2.6. Statistical analysis
All data are expressed as mean±SD and were analyzed with the Statistical Program of Social Sciences (SPSS for MS Windows, Version 10.0; SPSS Inc., Chicago, IL, USA). Continuous data were analyzed using ANOVA with repeated measures. Statistical significance was assumed with a P-value <0.05.

For evaluation of data without repeated measures, standard analysis of variance was used. Stereological data were analyzed using Mann–Whitney tests. According to the Holm-method (modified by Shaffer), statistical significance for comparison of five groups was assumed with a P-value <0.0083.

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Comment References

 
During retrograde flush preservation, a continuous washout of small blood and fibrin clots from the pulmonary arterial venting site was noticed in all test lungs, but the extent of clot formation was quantitatively more pronounced in NHBD lungs.

3.1. Functional analysis
3.1.1. Oxygenation capacity (pO₂/F_iO₂)
All animals survived the entire observation period of 5 h with sufficient pulmonary function. Although sham-operated animals presented with highest oxygenation values (sham 460.91±50.25), there were no statistically significant differences when compared to all NHBD groups (NHBD 90, 386.49±166.89; NHBD 180, 381.38±117.71; NHBD 300, 361.93±118.06) and the standard heart beating group (PER 27h, 412.45±106.67; P=0.665, Fig. 1) .

View larger version (13K): [in this window] [in a new window]   Fig. 1. Oxygenation in terms of pO2/FiO2 of transplanted lungs of domestic pigs during the observation period of 5 h following exclusion of the native right lung. Differences are not statistically significant (P=0.665).

View larger version (13K): [in this window] [in a new window]   Fig. 2. Pulmonary vascular resistance (PVR) of transplanted lungs of domestic pigs during the observation period of 5 h following exclusion of the native right lung. Differences between sham-grafts and all test lungs are statistically significant (P<0.04).

View larger version (11K): [in this window] [in a new window]   Fig. 3. Dynamic lung compliance of transplanted lungs of domestic pigs during the observation period of 5 h following exclusion of the native right lung. Differences are not statistically significant (P>0.34).

View larger version (13K): [in this window] [in a new window]   Fig. 4. Wet-to-dry lung weight ratio (W/D) of transplanted lungs of domestic pigs after the observation period of 5 h following exclusion of the native right lung. Differences are not statistically significant (P=0.134).

View larger version (148K): [in this window] [in a new window]   Fig. 5. Parenchyma of a sham-control animal 5 h after reperfusion without any intrapulmonary edema formation. Du, ductus alveolaris.

View larger version (179K): [in this window] [in a new window]   Fig. 6. Moderate formation of intraalveolar edema (Ed) after 5 h of reperfusion in a non-heart-beating donor lung with 90 min of warm ischemia (NHBD 90).

View larger version (12K): [in this window] [in a new window]   Fig. 7. Comparison of volume fractions of intraalveolar edema referred to lung parenchyma in domestic pig lungs after 4 h of observation. Differences are not statistically significant (P>0.0083).

	4. Comment

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Comment References

Recently, the innovative approach of retrograde preservation of lung grafts has been shown to be very effective in the elimination of different kinds of thrombi from the pulmonary vasculature; macroscopic blood clots and other tissue emboli which are often seen in organ donors with major trauma and multiple bone fractures and which may both alter the uniformity of standard antegrade flushing and severely impair graft reperfusion, can easily be washed out via the pulmonary artery venting site [14–16]. Furthermore, the overall quality of organ preservation in terms of postischemic lung function was significantly improved following retrograde lung preservation [6,16,17]. This phenomenon is believed to be due to the more homogeneous distribution in the low-pressure high-capacity pulmonary venous system [18] and the concomitant preservation of the small but important bronchial circulation [19]. However, most of these reports used high-potassium solutions for lung preservation. Since there is clear evidence in the past that use of the modern low-potassium dextran containing Perfadex solution ameliorates reperfusion injury and improves primary graft function in lung transplantation [20] we thought to evaluate if retrograde preservation of NHBD lungs with Perfadex solution is technically feasible and results in sufficient preservation quality in terms of pulmonary function even after extended periods of ventilated warm ischemia.

In our series, we found a postischemic NHBD lung function in terms of oxygenation and lung compliance which was not different from the results obtained with both sham-operated controls and conventional heart beating organ donors with cold ischemia of 27 h. Stereological evaluation revealed a moderate degree of intraalveolar edema formation in NHBD grafts which, however, did not differ significantly from the sham-group. This edema formation correlates with the overall increased pulmonary vascular resistance in all test lungs and represents a mild form of ischemia/reperfusion injury.

Grossly, the functional and histological results obtained with retrogradely preserved NHBD lung allografts did not differ from the general outcome in both sham-operated controls and conventional heart beating organ donors, which further illustrates the excellent preservation properties of this innovative approach.

Of special clinical importance and one of the main results of the presented work is the finding of continuous washout of small blood and fibrin clots from the pulmonary arterial venting site during retrograde preservation in both the standard heart-beating group but especially in NHBD lungs which is also reported by others [14–16]. This phenomenon underlines that even with intravenous heparinisation of NHBD as it is recommended by some groups [21], the pulmonary circulation is still prone to some degree of microvascular thrombosis which can alter the postoperative outcome following lung transplantation. However, there are some authors indicating that heparin is not mandatory at all in NHBD [12,22]. Especially in those non-heparinized NHBD lungs the innovative retrograde preservation strategy might display a special benefit in elimination of potential microvascular thrombi and debris.

Clinically, a high proportion of multi-organ donors, especially polytrauma patients, was found to have undetected multiple pulmonary emboli consisting of fat, brain or bone tissue at the time of postmortem examination [22–24]. Therefore, in clinical lung transplantation, it seems possible that the high percentage of postischemic primary graft failure in terms of ischemia/reperfusion injury might be at least in part due to undetected preexisting multiple emboli in the donor pulmonary circulation which are not to be mobilized by standard antegrade preservation techniques. Hypothetically, a significant improvement of postoperative graft function especially in NHBD lung transplantation with the described even higher risk of intravascular thrombus formation might, therefore, be expected just due to this single mechanism of embolus evacuation at the time of organ harvest with subsequent adequate preservation of the previously occluded pulmonary segments [22].

A limitation of this pilot study is the still rather short duration of warm ischemia with up to 5 h. However, it is generally agreed that for the clinical use of NHBD lungs, the period of warm ischemia should be kept as short as possible [22]. Furthermore, in accordance with the reported outcome of short-term warm ischemia in our experiments, this novel technique might also be considered in the situation, where an accepted brain-dead organ donor becomes hemodynamically unstable on the intensive care unit or in the operating room prior to onset of organ retrieval. In those not uncommon cases, a time period of 5 h should be enough to harvest at least the continuously ventilated lungs.

Overall, these promising results strongly encourage further multicenter studies in the field of retrograde preservation using NHBD lungs with extended periods of warm and cold ischemia. A potential future use of this innovative preservation strategy might represent a highly relevant tool in the clinical arena to significantly expand the progressively limited pool of donor lungs [25].

	Acknowledgments

 
The writers gratefully acknowledge the expert technical assistance of S. Kirste, K. Hornung, S. Böhm, A. Apel, S. Freese, A. Gerken, H. Hühn and M. Kirste. This work was supported by a grant from the Deutsche Forschungsgemeinschaft (DFG, Wa 738/4-1 and Ri 790/2-1).

	Footnotes

 
Presented at the joint 17th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 11th Annual Meeting of the European Society of Thoracic Surgeons, Vienna, Austria, October 12–15, 2003.

	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): Thorsten Wittwer Ulrich F.W. Franke Thorsten Wahlers Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wittwer, T. Articles by Wahlers, T. Search for Related Content PubMed PubMed Citation Articles by Wittwer, T. Articles by Wahlers, T. Related Collections Lung - transplantation