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Eur J Cardiothorac Surg 2004;26:151-157
© 2004 Elsevier Science NL

Pulmonary preservation with LPD and celsior solution in porcine lung transplantation after 24 h of cold ischemia

Sebastian P. Sommera, Gregor Warneckea, Jens M. Hohlfeldb, Bernhard Gohrbandta, Jost Niedermeyerb, Theodoros Kofidisa, Axel Havericha, Martin Strübera*

a Division of Thoracic and Cardiovascular Surgery, Hannover Medical School, 30623 Hannover, Germany
b Department of Respiratory Medicine, Hannover Medical School, 30623 Hannover, Germany

Received 30 September 2003; accepted 9 February 2004.

* Corresponding author. Tel.: +49-511-532-6581; fax: +49-511-532-8446
e-mail: strueber{at}thg.mh-hannover.de


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Objective: Pulmonary preservation for transplantation is associated with ischemia reperfusion injury resulting in endothelial cell and surfactant dysfunction. The purpose of the study was to compare two extracellular type solutions, low potassium dextrane (LPD) and Celsior in their ability of ameliorating lung ischemia reperfusion injury. Methods: In 12 donor pigs, the left lung was perfused with either LPD (n=6) or Celsior (n=6) solution. After 24 h cold storage, the lungs were transplanted into 12 recipient animals. After reperfusion of the left lung, the right pulmonary artery and bronchus were clamped. Bronchoalveolar lavage fluid (BALF) was obtained before the surgical procedure and 2 h after reperfusion. Surfactant activity was measured from BALF using a pulsating bubble surfactometer. Hemodynamic and respiratory parameters were assessed in 30-min intervals for 7 post-operative hours. Results: In both study groups two of six animals died from severe ischemia reperfusion injury, thus survival did not differ between groups. Rise of pulmonary vascular resistance index (P=0.01) and sequestration of neutrophiles (P=0.08) was less pronounced in Celsior group when compared to LPD animals. A difference in surfactant activity between both groups was not evident after 2 h of reperfusion. Conclusions: Both solutions might provide safe pulmonary preservation for 24 h of cold ischemia. While surfactant activity was affected to the same extent in both groups, Celsior solution provided slightly superior endothelial preservation.

Key Words: Lung transplantation • Ischemia-reperfusion injury • Low potassium dextrane • Celsior


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
Ischemia-reperfusion injury still remains a significant cause of early morbidity after pulmonary transplantation [1,2]. Low potassium dextrane (LPD) solution has been increasingly used for pulmonary preservation in recent years, since experimental evidence was established over the last decade of the superiority of LPD solution as compared to other means of lung preservation, i.e. Euro-Collins solution [3,4]. The Hannover Lung Transplant Program started using LPD solution routinely in April 1998 and has thereby improved early graft function significantly [5].

Of comparable extracellular electrolyte composition is the more recently developed Celsior solution. Primarily developed for heart transplantation [6], Celsior showed improved pulmonary graft preservation in experimental rat lung transplantation models [7,8]. In our well-established warm ischemia model in minipigs preservation with Celsior solution revealed superior post-ischemic lung function as compared to Euro-Collins or histidine–tryptophane–ketoglutarate, Bretschneider's solution (HTK) controls [9]. While Celsior as well as LPD preservation of the lung performed favorable in that warm ischemia model, we decided to compare both solutions in a porcine lung transplantation model with 24 h cold ischemia that more closely matches the clinical situation of pulmonary transplantation (Table 1) .


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  		Table 1. Composition of LPD and Celsior preservation solutions

 
Therefore, the purpose of our study was to evaluate initial graft function after preservation with Celsior or LPD solution for 24 h. Above that, surfactant function analysis was carried out as a sensitive parameter for the quality of lung preservation.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
2.1. Animal care
All animals received humane care in compliance with the ‘Principles of Laboratory Animal Care’ 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 in 1996 as well as in compliance with the European Convention on Animal Care. The study was approved by the institutional ethics committee.

2.2. Donor procedure
In 12 female pigs (German landrace; weight range 24–33 kg), anesthesia was induced by application of azaperon (5 mg/kg i.m.), atropine (5 mg total dose, i.m.) and pentobarbital (1 mg/kg, i.v.). Animals were intubated and ventilated in a pressure-controlled mode with pmax=30 cmH2O, PEEP=5 cmH2O, FiO2=0.5 and I:E=1:1. Anesthesia was maintained by continuous infusion of pentobarbital (5 mg/kg per h) and fentanyl (1 µg/kg per h). After median sternotomy, the inferior and superior vena cava were encircled with ties and the pulmonary artery was dissected from the aorta. After systemic heparinization (300 IU/kg), a 5 mm cannula was inserted into the pulmonary artery. Inflow occlusion was performed and the left atrial appendage was incised. The pulmonary artery was clamped proximal, and 1 l 4 °C cold LPD solution supplemented by 0.3 ml Tris buffer or Celsior solution was infused. Perfusion pressure in the pulmonary artery was recorded by a separate probe. A mean perfusion pressure of 16 mmHg was maintained. The lungs were stored in a semi-inflated state in preservation solution at 4 °C for 24 h.

2.3. Recipient preparation
In 12 female pigs (German landrace; weight range 23–32 kg), anesthesia was induced and maintained as described before. Recipient arterial pressure was monitored by a carotid artery catheter, pulmonary artery hemodynamics by a Swan–Ganz catheter (7.5 F, Baxter Healthcare, Irvine, CA). Cardiac output and extravasal lung water (EVLW) were recorded by a femoral artery thermodilution catheter connected to a cardiac output recorder (Picco System; Pulsion Medical Systems AG, Munich, Germany). The chest was opened by a left lateral thoracotomy in the fourth intercostal space. The pericardium was incised and a catheter was placed into the left atrial appendage. Left pulmonary artery, lung veins and bronchus were dissected. After systemic administration of heparin (300 IU/kg) left-sided pneumonectomy was performed. The graft was transplanted using running polypropylene sutures for pulmonary artery and atrial cuff and bronchus. The graft was deaired by retrograde perfusion, and then the pulmonary artery and bronchus were opened. After 10 min reperfusion time the right pulmonary artery and right main bronchus were clamped.

2.4. Assessment of hemodynamics and lung function
Atrial as well as arterial and pulmonary artery pressures were recorded online. Arterial and venous blood gas analyses were performed after placement of the catheters and in 30 min intervals after initiation of reperfusion. Pulmonary vascular resistance index (PVRi) was calculated from cardiac output and pressures measured by the pulmonary artery catheter divided by the body-surface array of the pig. The system was calibrated by three repeated bolus injections of 10 ml 8 °C cold saline into the jugular vein. EVLW was calculated by means of repeated pressure curve analysis from data measured by the femoral artery thermodilution catheter. Dynamic lung compliance and airway resistance were measured continuously by a modified respirator (Evita II; Drägerwerke, Lübeck, Germany). Experiments were terminated by a pentobarbital overdose after 7 h of reperfusion or when systolic arterial pressure fell below 40 mmHg.

2.5. Surfactant, protein and phospholipid analysis
A bronchoalveolar lavage (BAL) of the recipient native lingula was performed with 100 ml warmed isotonic saline before transplantation. A second BAL of the lingula of the transplanted lung was carried out 2 h after reperfusion. The recovered lavage fluid was centrifuged at 150g, and the cell-free supernatant was frozen at –80 °C until further analysis. From the cell pellet a manual differential cell count from bronchoalveolar lavage fluid (BALF) was performed using standard techniques.

From the cell-free supernatant samples, phospholipid content was determined according to the method of Bartlett [10]. Content of protein was measured according to the technique described by Lowry [11]. All assays were performed as duplicate measures and the mean value was reported.

Surfactant was isolated from BALF by centrifugation at 48,000g for 60 min at 4 °C. Phospholipid determination of the pelleted material and the supernatant served for calculation of the small to large aggregate ratio surfactant function was determined by a pulsating bubble surfactometer (Electronetics, Buffalo, NY) according to the technique described by Enhorning [12]. Briefly, 40 µl of the pelleted surfactant, which had been adjusted to a phospholipid concentration of 1 mg/ml, was filled into the sample chamber. The surface tension at minimal bubble size ({gamma}min) was recorded after 5 min of bubble pulsation at a rate of 20 cycles/min and a temperature of 37 °C. Before bubble pulsation was started the adsorption rate was determined as surface tension 10 s after formation of a bubble ({gamma}ads). All analog data were digitalized and recorded by a personal computer.

2.6. Myeloperoxidase activity assay
Relative neutrophil sequestration into lung tissue was assessed by a myeloperoxidase activity assay [13]. Frozen lung tissue specimen was homogenized in 1.5 ml of 0.02 M potassium phosphate buffer (pH 7.4). The suspension was centrifuged at 10,000g for 15 min. The supernatant was discarded and the pellet was resuspended in 2 ml of 0.5% hexaolecyltrimethyl ammoniumbromide in 50 mmol/l potassium phosphate solution (pH 6.0) and homogenized. Tissue was disrupted by sonication and three freeze–thaw cycles (liquid nitrogen bath/37 °C water bath). The suspension was centrifuged at 10,000g for 15 min. Aliquots (0.1 ml) of supernatant were added to 1 ml of tetramethylbenzidine substrate system (Sigma Chemical; St Louis, MO) at pH 6.0. The change in absorption at 655 nm at 25 °C over 3 min was recorded. Assays were performed as repeated measures and results are expressed as means in milliunits per gram.

2.7. Histology
Specimen of recipient native right lung was collected after clamping, specimen of the graft after termination of the experiment. Tissue samples were snap frozen in liquid nitrogen and stored at –80 °C. Sections of 5 µm thickness were cut from several levels of frozen tissue samples with a cryotome (Leica, Germany) and stained with eosin and hematoxylin according to standard techniques. Each section was evaluated for edema, neutrophil count and bleeding.

2.8. Statistical analysis
Data were expressed as mean±standard error of the mean (SEM). Analysis of continuous data was performed using repeated-measures analysis of variance (ANOVA). Data without repeated measurements were analyzed using the two-sided Student's t-test. P-values less than 0.05 were considered statistically significant. All data were analyzed with the Scientific Programm of Social Sciences (SPSS for Windows Ver. 10.0; SPSS Chicago IL).


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
3.1. Animal survival
Left lungs preserved for 24 h with either LPD (n=6) or Celsior solution (n=6) show comparable early graft function. In both groups two out of six animals developed severe reperfusion injury with lethal right heart failure after 2.5 and 4 h in LPD group and 2.0 and 3.0 h in Celsior group.

3.2. Hemodynamic and respiratory parameters
Arterial oxygenation index remained slightly lower in Celsior preserved grafts as compared to LPD throughout observation time. At the end of the reperfusion time, Celsior and LPD lungs revealed oxygenation indices in a similar range (Fig. 1) . Dynamic lung compliance was comparable in both experimental groups during the observation period (Fig. 2) . An early rise in PVRi resulted in right heart failure in two animals of each group, as explained above. While the remaining four Celsior-treated animals maintained low PVRi, LPD animals revealed a substantial early rise and significantly higher PVRi (P=0.01) throughout the observation period (Fig. 3) .



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  		Fig. 1. PO2/FiO2 ratio in arterial blood samples drawn from the left atrium over 7 h of reperfusion. Data are expressed as the mean±SEM. Ratios before surgery (0) and after reperfusion (0.5–7.0) did not differ significantly among groups.

 


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  		Fig. 2. Dynamic compliance of the lung over 7 h of reperfusion. Data are expressed as the mean±SEM. Values before surgery (0) and after reperfusion (0.5–7.0) did not differ significantly among groups.

 


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  		Fig. 3. Pulmonary vascular resistance index of the lung over 7 h of reperfusion. Data are expressed as the mean±SEM. Values before surgery (0) did not differ significantly among groups. Clamping the right main pulmonary artery cause a significant increase in PVRi in both groups. Differences in PVRi over 7 h reached statistical significance among both groups (P=0.013, repeated measures Anova).

 
3.3. Lung water content
Lung tissue water content was significantly increased in grafts of both study groups after termination of the experiment when compared to native right lungs (tissue water content: 84.20±2.49 vs. 87.50±1.05%, P=0.038; LPD group and 83.40±1.95 vs. 87.60±2.19%, P=0.013; Celsior group). Water content was not statistically different when LPD lungs were compared to Celsior lungs 7 h after reperfusion (P=0.95).

3.4. Bronchoalveolar lavage fluid analysis
Right lungs of LPD and Celsior animals showed normal cell counts with a predominance of alveolar macrophages (around 90%) and approximately 2% neutrophils before surgery. After 2 h of reperfusion, a reduced percentage of macrophages combined with a substantial increase of the relative neutrophil count was observed. The relative increase of neutrophils appeared more pronounced in the Celsior group. However, total cell count in this group remained lower after reperfusion, indicating a lower absolute neutrophil count in the Celsior group. Differences between both groups did not reach statistic significance and might be due to chance. The SA/LA ratio is an indicator for the conversion of surface active surfactant aggregates into surface inactive small surfactant aggregates. Baseline values were low in both groups. Analysis of surfactant after 2 h of reperfusion revealed a 4–6 fold increase of the SA/LA ratio when compared to baseline values, but values did not differ between groups (Fig. 4 , Table 2) .



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  		Fig. 4. SA/LA ratio of the BALF phospholipid composition before surgery and 2 h after reperfusion. Data are expressed as the mean±SEM. Values before surgery (baseline) and 2 h after reperfusion did not differ significantly among groups.

 

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  		Table 2. Analyses from BALF before surgical procedure (right lungs) and 2 h reperfusion time (left lungs), tissue myeloperoxidase activity of left lungs was measured after termination of the experiment

 
3.5. Surface activity evaluated with the pulsating bubble surfactometer
The surface tension {gamma}ads of an uncycled bubble 10 s after formation was 40 mN/m (38±6 mN/m LPD, 43±14 mN/m Celsior; P=0.3) at baseline. During reperfusion values of both groups remained stable at 36 mN/m (37±11 mN/m LPD, 34±3 mN/m Celsior; P=0.6). The surface tension at minimal bubble size after 5 min of pulsation was around 3 mN/m (3.1±2.4 mN/m LPD, 2.5±3.9 mN/m Celsior; P=0.7) before the surgical procedure and increased slightly up to 6 mN/m (6.6±6.8 mN/m LPD, 5.7±6.0 mN/m Celsior; P=0.8) 2 h after transplantation without significant differences between both groups (Fig. 5) .



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  		Fig. 5. Surface tension at minimal bubble size after 5 min of bubble pulsation ({gamma}min) in BALF before surgery and 2 h after reperfusion. Data are expressed as the mean±SEM. Values before surgery (baseline) and 2 h after reperfusion did not differ significantly among groups.

 
3.6. Myeloperoxidase activity
The activity of myeloperoxidase in lung tissue reflects sequestration of neutrophil granulocytes. Tissue samples of each group's right native lungs and grafts after termination of the experiment were examined. Before transplantation, tissue activity was low in both groups (19±12 mU/g, Celsior vs. 4±3 mU/g, Perfadex; P=0.16). Myeloperoxidase activity after termination of the experiment increased more in the LPD group, although differences between groups were not significant (274±168 mU/g, LPD vs. 55±92 mU/g, Celsior; P=0.08).

3.7. Histology
Histologic injury was barely detectable in left lungs after 7 h reperfusion. In both groups alveolar edema and neutrophil infiltration were uniformly detectable to some extent. Lung tissue of right lungs showed normal histology in all specimens.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
In a recent retrospective study, King et al. described an incidence of severe ischemia-reperfusion injury in up to 22% of lung recipients, contributing to an ultimately fatal outcome in 9%, when EC was used for graft preservation [1]. While EC solution has been the gold standard for pulmonary preservation for more than a decade, the disadvantages of this intracellular type solution, i.e. high potassium and low sodium, namely endothelial cell injury and surfactant dysfunction have been well described by others and by our own group [3,14]. The introduction of the extracellular type LPD solution significantly improved results in experimental lung preservation with cold ischemic times up to 24 h. In a variety of experimental protocols LPD proved its superiority in endothelial cell and surfactant preservation when compared to EC solution [3,4,14,15]. Clinically, we and other groups demonstrated a significantly reduced duration of mechanical ventilation and of stay on the ICU after lung transplantation, when LPD was used for graft preservation as compared to EC, contributing to a reduced mortality in the early post-operative follow-up [5,15]. However, ischemia-reperfusion injury was still observed to some degree after LPD preservation of the donor lung in our experimental [3], as well as our clinical transplant program [5]. Thus, further experimental effort to prevent lung ischemia-reperfusion injury seems to be justified and might be clinically rewarding.

Celsior solution has been developed 10 years ago in France for cardiac preservation, but has been shown to provide pulmonary protection, too [8,16]. Thus, Celsior solution is currently used by some clinical lung transplant programs in France [8,17]. Celsior is an extracellular type solution that showed remarkable results in various isolated rat lung models [7,8]. Franke and co-workers presented data from a porcine 24 h ischemia lung transplantation model comparing LPD and Celsior solution. While all LPD animals survived for the entire observation period in this experiment, Celsior animals showed a markedly reduced survival [18]. Contrarily, recent data from our warm ischemia model showed a delayed increase in PVR and improved pulmonary compliance after Celsior preservation, when compared to EC [6]. Based on these results we compared LPD to Celsior solution in our porcine model of pulmonary allotransplantation after 24 h of donor lung cold ischemia [2] that more closely resembles the clinical situation of lung allografting than our warm ischemia model.

A potential limitation of this study might be the short observation time of 7 h. However, the prolonged ischemic time of our model leads to reliable occurrence of ischemia-reperfusion injury. Graft performance during the first 7 h might be representative of the entire early post-operative period since potential damage should be detectable within this period. Clamping the recipient right pulmonary artery after graft reperfusion challenges the right ventricle. Although a later time-point might have been preferable for surfactant function analysis, we decided to collect the BALF as early as 2 h after initiation of reperfusion because surfactant function of this time point proved to be predictive for ischemia reperfusion injury in our earlier studies.

Both solutions tested in this study provide comparable protection of pulmonary function for 24 h of cold ischemia. However, neither of these solutions warrants absolutely safe preservation regarding this prolonged time period. In both study groups two animals were lost by severe lung ischemia-reperfusion injury within the first 2.5 h after initiation of reperfusion. Celsior solution provided slightly improved post-ischemic graft function, when compared to LPD. Pulmonary edema and rise in PVR appeared more pronounced in the LPD group when compared to Celsior. Sequestration of neutrophiles remained lower in Celsior animals than LPD animals. Surfactant activity was uniformly impaired to some extent in both groups as shown by an increased minimal surface tension as determined in the pulsating bubble surfactometer in addition to an increased SA/LA ratio of the phospholipid fraction. Surfactant function measured in both groups was impaired only to a mild degree, therefore function of the pulmonary graft was not affected.

The remarkable results Celsior solution achieved might be due to the content of reduced glutathione. Glutathione as a radical scavenger [19,20] protects endothelium from oxygen-free radical damage [21] and reduces sequestration of neutrophiles. Crucial parameters of pulmonary function like arterial oxygenation, endothelial function and surfactant activity are at least comparably preserved by Celsior solution and showed a tendency to be improved as compared to LPD preserved lungs. Of interest is the comparison of the findings of this study with results from our warm lung ischemia minipig model that have been published previously [3,9]. In the warm ischemia model the left lung was flushed with cold preservation solution and remained thereafter in a warm ischemic state in situ for 90 min. Reperfusion and clamping of collateral lung hilus were performed as described for the cold ischemia model. Under the conditions of warm ischemia, pulmonary vascular resistance was not lower in Celsior than in LPD animals and surfactant function, measured as the surface-tension lowering properties of the surfactant material ({gamma}min) was better preserved in LPD animals. This might indicate that the high molecular colloid content of LPD whose importance has been previously shown in pulmonary preservation [22–25] reveals its protective effect more impressively under the destructive conditions of warm ischemia. The composition of Celsior solution does not contain high molecular components like dextrane. The absence of colloidal components might be the most important limitation of Celsior solution in the field of pulmonary preservation. In conclusion Celsior revealed comparable results of lung protection in both models and therefore the use of Celsior solution in clinical lung transplantation seems justified.

It could be speculated that glutathione-enriched LPD solution or colloid-supplemented Celsior solution combines the potential of colloids with radical scavengers and may further advance pulmonary preservation. These hypotheses will be addressed in future experiments.


   Acknowledgments
 
The authors thank Claudia Kelle, Adine Timke and Jost Dörr for their invaluable assistance. LPD solution was kindly provided by Vitrolife, Sweden.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 

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