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Ann Thorac Surg 2008;86:1123-1129. doi:10.1016/j.athoracsur.2008.05.048
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Late Retrograde Perfusion of Donor Lungs Does Not Decrease the Severity of Primary Graft Dysfunction

Pasquale Ferraro, MDa,*, Jocelyne Martin, MDa, Julie Dery, MDb, Julie Prenovault, MDb, Louise Samson, MDb, Marianne Coutu, MD, MSa, Long-Qi Chen, MDa, Charles Poirier, MDc, Nicolas Noiseux, MDd, Andre Duranceau, MDa, Yves Berthiaume, MDc

a Service de Chirurgie Thoracique and Service de Chirurgie Cardiaque, Département de Chirurgie, Montréal, Quebec, Canada
b Département de Radiologie, Montréal, Quebec, Canada
c Service de Pneumologie, Département de Médecine, Centre de Recherche, Montréal, Quebec, Canada
d Centre Hospitalier de l'Université de Montréal, Montréal, Quebec, Canada

Accepted for publication May 15, 2008.

* Address correspondence to Dr Ferraro, Service de Chirurgie Thoracique, Département de Chirurgie, Centre Hospitalier de l'Université de Montréal, 1560 Sherbrooke Est, Suite D-8050, Montréal, QC, H2L 4M1, Canada (Email: pasquale.ferraro{at}umontreal.ca).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: The ideal preservation strategy has yet to be established in lung transplantation. This clinical study compares primary graft dysfunction using antegrade and retrograde perfusion of donor lungs.

Methods: Over a 6-year period, 153 consecutive patients underwent lung transplantation in our institution. Group I consists of 65 patients who received lungs preserved with an antegrade flush of modified Euro-Collins solution. Group II includes 65 patients who received lungs preserved with an antegrade flush of low-potassium dextran (LPD) solution. Group III consists of 23 patients who received lungs preserved with an antegrade and a preimplantation retrograde flush of LPD solution. Endpoints evaluated were the following: acute lung injury (ALI) score, time to achieve a fraction of inspired oxygen (FiO 2) of 40% and a positive end-expiratory pressure (PEEP) of 5, length of ventilation, length of intensive care unit (ICU) stay, 90-day operative mortality, and patient survival rates.

Results: The patient demographic data, underlying diagnosis, number of single and double lung transplants, use of cardiopulmonary bypass, and mean ischemic times were similar in all 3 groups. The mean ALI score (6.2, 5.8, and 6.0) and the median length of ventilation (23.5, 24.0, and 27.0 hours) in groups I, II, and III, respectively, were not significantly different. The length of ICU stay, the 90-day operative mortality, and the survival rates were not significantly different in the 3 groups.

Conclusions: Our results suggest that late retrograde perfusion of donor lungs does not decrease the severity of primary graft dysfunction when compared with standard antegrade techniques.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Clinical lung transplantation has evolved significantly over the last two decades as a result of improved surgical technique, better perioperative care, and more efficient immunosuppression. Great strides have also been made in lung preservation and in understanding the ischemia-reperfusion induced lung injury. A wealth of knowledge has been provided by experimental studies on ischemia-reperfusion injury (IRI) at a cellular and molecular level [1]. Despite the advancements in the field of lung preservation, primary graft dysfunction (PGD) remains the most common cause of death in the early posttransplant period [2]. The occurrence of severe PGD with its associated pulmonary edema and severe hypoxemia is still reported in 10% to 15% of transplant recipients [3].

Currently, most programs use a hypothermic antegrade pulmonary artery flush of a modified Euro-Collins (EC) or low-potassium dextran (LPD) solution and topical cooling with a cold saline solution. Substantial evidence suggests that this method provides reliably well-preserved lung allografts and adequate postoperative function [1, 4]. Over the years, transplant surgeons have added a retrograde flush through the left atrium in an attempt to provide a more homogenous wash-out and cooling of the lungs and hence better preservation. First introduced into clinical practice by Sarsam and colleagues [5] in heart-lung transplant recipients, the value of a retrograde flush was later shown experimentally by a number of authors [6–9]. Studies, however, have placed the emphasis on a retrograde flush administered immediately after the antegrade perfusion (in situ or on the backtable) at the time of procurement. The concept of a late retrograde or preimplantation infusion of a preservation solution has not gained wide-scale acceptance. Limited experimental evidence [10] and a single clinical study [11] suggested that a late retrograde flush improved preservation and early graft function. The purpose of the present study was to determine if the preimplantation retrograde perfusion of donor lungs decreases the severity of PGD after transplantation.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Study Population
The study includes 153 consecutive lung transplantations carried out between July 1997 and December 2003 at the Centre Hospitalier de l'Universite de Montreal. Approval for the study as well as a waiver of the need for patient consent was obtained from the Institutional Review Board of the hospital. The clinical and radiographic records were reviewed retrospectively and the data were entered into a comprehensive database. Lung recipients were selected for transplantation according to established criteria [12]. Patients were divided into 3 groups according to the type of preservation solution used and its route of administration. Six patients who received heart-lung transplantations during the study period were not included in the analysis. Follow-up was complete in all cases.

Graft Preservation and Surgical Technique
Lungs were harvested from donors meeting standard selection criteria. Group I consisted of grafts preserved with an antegrade flush of modified Euro-Collins solution (from 1997 to 2000). Group II consisted of lungs preserved with an antegrade flush of LPD solution (from 2001 to 2003). Group III included lungs preserved with an antegrade and preimplantation retrograde flush of LPD solution (from 2000 to 2001). The antegrade solutions were administered through a catheter placed in the main pulmonary artery. Four liters of preservation solution at 4°C containing 500 ng of prostaglandin E1 (alprostadil) were used for the antegrade flush. At the time of harvest, the lungs were ventilated with an oxygen concentration of 50%. Once the flush was completed, the trachea was clamped with the lungs two-thirds inflated. The lungs were then removed and placed in sterile plastic bags containing the same preservation solution at 4°C. The retrograde flush consisted of 1 liter of LPD solution at 4°C administered to each graft through the pulmonary veins just prior to reimplantation.

Lung transplantation was performed using a standard surgical technique. In all patients, the pulmonary artery pressures, cardiac output, and arterial blood gases were closely monitored intraoperatively. Transesophageal echocardiography was used in patients with pulmonary hypertension, right heart failure, or hemodynamic instability. Cardiopulmonary bypass was used electively in patients with severe pulmonary hypertension and right ventricular dysfunction, and selectively in patients who became unstable during the transplant procedure. Intravenous (IV) methylprednisolone (500 mg) was administered immediately before reperfusion of each graft. Prophylactic antibiotics were used perioperatively and the bronchial anastomoses were inspected using fiberoptic bronchoscopy in all patients.

Postoperative Care and Immunosuppression
Standard hemodynamic monitoring was used postoperatively and aggressive diuresis was favored to maintain a negative fluid balance. Ventilator settings were adjusted to minimize the oxygen concentration and the risks of barotrauma. Weaning and extubation were carried out using standard intensive care unit (ICU) criteria. Antibiotics were administered according to cultures, and cytomegalovirus (CMV) prophylaxis with ganciclovir and immunoglobulin G (IgG) was established according to the donor and recipient CMV status. Chest radiographs were obtained on arrival in the ICU and on a daily basis thereafter. Bronchoscopy was carried out in patients who remained ventilator-dependent for 5 or more days and routinely in all patients 14 days postoperatively.

Immunosuppression consisted of a 6-day steroid taper of IV methylprednisolone, followed by a triple-drug regimen. Patients with cystic fibrosis or bronchiectasis received tacrolimus, azathioprine, and prednisolone. Patients without septic lung disease received induction with rabbit antithymocyte globulin (RATG) followed by cyclosporine, azathioprine, and prednisolone. In 1999, mycophenolate mofetil replaced azathioprine in the baseline regimen for all patients. Trough whole blood levels of 12 to 15 ng/mL for tacrolimus and 300 to 400 ng/mL for cyclosporine were targeted. Azathioprine and mycophenolate were adjusted to maintain a white blood count greater than 4,000/µL.

Radiographic Study and Acute Lung Injury Score
The severity of the reperfusion injury and the postoperative graft function were studied using clinical, physiologic, and radiographic parameters. An acute lung injury (ALI) score, as developed by Boujoukos and colleagues [13], was calculated retrospectively from the clinical records. The ALI score was based on three components (partial pressure of oxygen, arterial/fraction of inspired oxygen [PaO 2/FIO 2] ratio, highest positive end-expiratory pressure [PEEP], chest X-ray [CXR] score) and ranged from a minimum of 3 points to a maximum of 12 points (Table 1). The PaO 2/FIO 2 ratio was calculated from the worse arterial blood gases drawn 12 hours postoperatively and on a daily basis thereafter. The highest PEEP required to maintain adequate oxygenation was included in the ALI score.


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  		Table 1 Calculating the Acute Lung Injury (ALI) Score
 
The postoperative chest X-rays of all patients who survived more than 12 hours were reviewed independently by two senior chest radiologists (J.P., L.S.) who were blinded from each other. The X-rays were read without any knowledge of the clinical outcome or physiologic data, other than the underlying diagnosis and type of transplantation. Radiographs from days 0 through 5, and day 10 were read and the severity of the reperfusion injury was graded for each graft using a categoric scale from 0 (none) to 5 (severe) (Table 1), as described by Ablett and colleagues [14]. The lungs were divided into 3 zones with a grade attributed to each. An average was calculated for the 3 zones in each graft and an overall average was determined for both grafts in a double lung transplant. The scores from the 2 radiologists were then also averaged. The highest mean X-ray score on any given day after transplantation was incorporated into the final ALI score. The reperfusion injury was considered mild if the ALI score ranged from 3 to 5, moderate if the ALI score ranged from 6 to 8, and severe for a score of 9 to 12.

Statistical Analysis
Preoperative, perioperative, donor-related, and patient survival data were collected and entered into an institutional database. Endpoints studied included the acute lung injury (ALI) score, time to achieve an FIO 2 of 40% and PEEP of 5, length of ventilation, length of ICU stay, 90-operative mortality, and 1-, 3-, and 5-year survival. Statistical analysis was carried out using the SPSS 15.0 software (SPSS Inc, Chicago, IL). Normally distributed data are expressed as mean ± SD for continuous variables or as proportions for categoric variables. Some data are presented as median with the interquartile range. The t test was used for the comparison of means. The {chi}2 test was performed for categoric data or the Fisher exact test as needed. Patient survival was estimated using the Kaplan-Meier method. Survival curves were compared with the Wilcoxon signed-rank test. A two-sided p value equal or less than 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Over the 6-year study period, 153 lung transplantations were carried out. From this group, 148 were primary lung transplants, 4 were retransplantations, and 1 was a combined double lung-kidney transplant. The mean age of patients ranged from 45.0 to 50.9 years. The remaining demographic data summarized in Table 2 showed no significant differences between the 3 study groups. The underlying disease in the recipient patients showed a greater number of cystic fibrosis and pulmonary fibrosis patients in group II. The distribution of underlying diseases was not significantly different. Donor characteristics are also shown in Table 2. Age of donors and results of blood gases obtained at the time of harvest were not statistically different. The number of smokers ranged from 17.4% to 43%. The cause of death was neurologic in the majority of donors in groups I and III.


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  		Table 2 Demographic and Clinical Data
 
The number of single and double lung transplants performed in each group is shown in Table 3. The cold ischemic times ranged from 181 to 220 minutes for the first grafts and ranged from 285 to 329 minutes for the second grafts. Overall, 18 patients required cardiopulmonary bypass for their transplantation with a mean length of cardiopulmonary bypass (CPB) varying from 82 to 193 minutes. The CPB was used electively in 11 cases and required urgently in 7 patients. The total amount of IV fluids and blood products administered intraoperatively is also shown in Table 3.


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  		Table 3 Intraoperative Data
 
The results of the radiographic assessment of the reperfusion injury are shown in Figure 1. One thousand thirty-one postoperative chest X-rays were read by the 2 thoracic radiologists with an excellent correlation as reflected in a Spearman correlation factor of 0.923 (p < 0.001). X-ray records were not available in 1 patient from group I and thus excluded from the assessment. In the overall group of 152 patients, the chest radiographic score peaked on day 0 with a mean score of 2.5 (scale of 0 to 5), which represents a moderate-severe interstitial infiltrate to a mild alveolar infiltrate. The scores subsequently returned progressively to near normal values over a 5-day period. Chest X-rays on postoperative day 10 showed a persistent mild to moderate interstitial infiltrate with a mean score of 1.4. Radiographic findings in the 3 study groups did not differ significantly in terms of the highest score, the postoperative course, and the final outcome.


Figure 1
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  		Fig 1. Radiographic score according to the postoperative day (lined column = group I; {blacksquare} = group II; {square} = group III; group I: Euro-Collins antegrade; group II: LPD antegrade; group III: LPD antegrade and retrograde; LPD = low-potassium dextran solution).

 
Data on reperfusion injury and postoperative graft function are summarized in Table 4. The mean ALI scores of 6.2 in group I, 5.8 in group II, and 6 in group III were not statistically different (p = 0.614). The distribution of mild, moderate, and severe injuries was also similar in the 3 study groups. The median time required to achieve an FIO 2 of 40% and PEEP of 5 was not statistically different (p = 0.748). The median length of ventilation was 23.5 hours in group I, 24 hours in group II, and 27 hours in group III, showing no significant difference (p = 0.375). The overall 90-day operative mortality ranged from 6.2% to 10.8% and was not significantly different as shown in Table 4. In group I, 3 patients died from acute right heart failure, 2 from primary graft failure, 1 from uncontrolled sepsis, and 1 from a cerebrovascular accident. In group II, 1 patient died from primary graft failure, 1 from sepsis, 1 from a cerebrovascular accident, and 1 from an esophageal carcinoma. In group III, 1 patient died from primary graft failure and 1 from sepsis.


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  		Table 4 Primary Graft Dysfunction and Postoperative Lung Function
 
Survival data as estimated by the Kaplan-Meier method are shown in Figure 2. The 1-, 3-, and 5-year survival rates were, respectively, as follows: group I, 68%, 58%, 52%; group II, 86%, 75%, 56%; and group III, 65%, 57%, 43%. When comparing the 3 study groups the survival rates were not statistically different (p = 0.297).


Figure 2
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  		Fig 2. Estimated Kaplan-Meier survival of transplanted patients in the three study groups (black line = group I (Euro-Collins antegrade); light grey line = group II (LPD antegrade); grey line = group III (LPD antegrade and retrograde). Patients at risk at each time point listed under the abscissa.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Over the years, lung transplantation has become a mainstay of therapy for a variety of end-stage pulmonary diseases. Significant improvement in patient outcomes have been reported with one-year survival rates approaching the 90% mark in some centers [2]. Although graft preservation has also improved significantly, reducing the incidence of PGD and its associated postoperative morbidity and mortality continue to challenge transplant physicians. The ideal method of lung preservation, including the type of solution and its route of delivery, has yet to be established with certainty in the clinical setting.

The results from this retrospective study suggest that the addition of a late preimplantation retrograde flush to a standard antegrade technique does not improve graft preservation or posttransplant lung function. The ALI score, length of ventilation, and length of ICU stay were not significantly different in the study groups. Although the study is limited by its retrospective nature and the limited number of patients, the donor and recipient characteristics, as well as the intraoperative variables, were similar in the 3 groups. Ischemic times were significantly different but on average less than 4 hours for the first graft and less than 6 hours for the second graft. In fact, despite the ischemic times being shorter in the retrograde group when compared to group I, and despite the fact the retrograde group received less total IV fluids intraoperatively, postoperative graft function was not improved. Also, the type of solution administered did not seem to influence the severity of the PGD when comparing the oxygenation indices or length of ventilation. The patient survival data also show no significant differences in the early or late survival rates. Due to the small sample size in group III, a power analysis was added to study the differences in ALI scores. To show a statistically significant difference between the groups, the power of this study was only 57% (type II error of 43%).

Retrograde perfusion of pulmonary grafts presents a number of theoretical advantages including a more homogenous distribution of the perfusate through a low resistance venous system, flushing the bronchial circulation through the bronchopulmonary anastomoses and evacuating blood clots, debris, and fat emboli from the pulmonary vascular bed [7, 15, 16]. Experimentally, retrograde flushing improves oxygenation, decreases airway resistance, and reduces edema formation [6, 8, 17]. Also, histologic and ultrastructural studies have shown better preservation of type I pneumocytes, capillary endothelial cells, bronchial epithelial cells, and surfactant function [18, 19]. Cold ischemic times have been extended up to 27 hours with good graft function using a retrograde flush in a pig model, as reported by Wittwer and colleagues [9].

However, data from controlled clinical studies evaluating retrograde perfusion techniques are unfortunately scarce. Sarsam and colleagues [5] reported their initial experience with retrograde flushing at the time of harvest in 3 patients undergoing heart-lung transplantation. Venuta and colleagues [11] compared a standard antegrade flush with a combined antegrade and preimplantation retrograde flush in total of 14 patients. Although the authors suggested that the late retrograde flush was beneficial, the length of ventilation, the PaO 2/FIO 2 ratio, and extravascular lung water index were not significantly improved in the late retrograde group. The results of the present study in 153 patients seem to confirm that late retrograde flushing does not improve graft preservation or postoperative lung function. Consequently, we have stopped using a late retrograde flush and currently use an antegrade perfusion of LPD solution with an immediate in vivo retrograde flush of the donor lungs.

Over the years, LPD solution has become widely used in clinical lung transplantation based on theoretical advantages provided by experimental research [19–23]. The evidence provided by clinical studies, however, remains somewhat unsatisfactory. Most studies are retrospective in nature, use poorly defined selection criteria, include a limited number of patients, and use historic controls to compare results [24–27]. Recent clinical studies by Aziz and colleagues [28] from Newcastle, Nath and colleagues from the University of Minnesota [29], and Thabut and colleagues [30] from France report no difference in graft preservation when comparing the use of LPD with Euro-Collins solution. The University of Minnesota study of 231 well-matched patients showed no statistically significant benefit in gas exchange parameters, the incidence of PGD, patient survival, or bronchiolitis obliterans syndrome-free survival.

Based on these conflicting data, it appears that experimental results suggesting that LPD is a superior preservation solution cannot be reliably or consistently reproduced in patient studies. Much of the evidence supporting the use of LPD has been obtained from small animal models, which are not representative of larger animal models. Furthermore, as pointed out by Aziz and colleagues [28], the animal models used to assess the superiority of LPD solution were not brain-stem death models and thus not representative of the donors used in clinical practice. On the other hand, the clinical indices commonly used to measure the quality of preservation (gas exchange, chest X-rays, length of ventilation, patient survival) are probably not sensitive enough to detect subtle differences. Also, as was the case in the present study, the relatively short ischemic times (< 4 to 6 hours) and the quality of the donors may in fact have a more significant impact on lung preservation and graft function than the actual type of preservation solution.

The influence of PGD on postoperative morbidity and mortality cannot be overstated. In an important review by Christie and colleagues [3], the effects of PGD on early and long-term results were studied in a cohort of 5,262 patients from the International Society of Heart and Lung Transplantation Registry. Among subjects who died by 30 days posttransplantation, 43.6% had primary graft dysfunction. Also, in patients who were long-term survivors after presenting PGD, there was a persistent increased risk of mortality. Several studies have also shown the importance of PGD as a predictive factor for prolonged ventilatory support, increased ICU length of stay, and overall morbidity [31–33]. The relationship, however, between severe PGD and the subsequent development of bronchiolitis obliterans has not been established with any certainty and thus remains speculative [3, 34–36].

In conclusion, the results of this retrospective study suggest that late retrograde perfusion of donor lungs does not provide any added benefit to a standard antegrade technique. Also, the type of preservation solution does not seem to influence the incidence or severity of PGD. Prospective studies in marginal donors with extended ischemic times comparing different solutions and routes of delivery might provide the necessary data confirming the superiority of one preservation strategy over another. Sustained efforts in the prevention and effective treatment of PGD may in fact prove to be the key to reducing the incidence of bronchiolitis obliterans and improving the long-term results with lung transplantation. Only well-designed prospective randomized trials with sufficient numbers of patients can provide the answers to these questions.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was supported by a group grant from the Fonds de la recherche en santé du Québec: Transdisciplinary research group on characterization of early predictors of rejection and by the Fondation pour la recherche en chirurgie thoracique de Montréal.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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F. Venuta and M. Anile
Invited Commentary
Ann. Thorac. Surg., October 1, 2008; 86(4): 1129 - 1130.
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