Although the worldwide number of lung transplantations (LTXs) shows a steady increase, the demand for such a procedure and the number of patients on waiting lists rises almost in parallel (1). This results in a permanent and continuously increasing scarcity of donor lungs. An optimal use of the limited donor organ resources therefore demands even more for allocation of donor organs to patients with the highest need for transplantation (TX) and with the best outcome expectations.
The recent introduction of the lung allocation score (LAS) in the United States aimed to follow these principles and to favor those patients who own such an optimal combination of need and outcome parameters (2). In this way, LAS has also made it possible for the first time in the United States to direct organs to patients with highest urgency for TX, who naturally are patients who are not yet only ventilated but have already further advanced to mechanical support on extracorporeal membrane oxygenation (ECMO).
In Austria, allocation of lungs has always been performed as a “center allocation,” which leaves the decision, who should receive the next lung, to the center. This regulation especially favors allocation of donor organs to patient with the highest urgency status. As a result of that, our center had the opportunity to gather substantial experience with TX of patients bridged on ECMO. In this article, we aim to summarize this experience with LTX under such extreme conditions.
Bridge Time Period
Four patients (group 1) died during the waiting time after being on device for a median of 11 days (range 8–28 days). Reason for death in all of them uniformly was septic multiple organ failure.
Thirty-four of the 38 patients were transplanted after a median waiting time on device of 4.5 days (range 1–63) days. Of them, eight patients died in hospital (group 2) and 26 patients were discharged from hospital (group 3).
Demographic data, time of intubation, and time of staying on device are summarized in Table 1. There was no statistically significant difference in time on ECMO between group 3 (median 4.5 days; range 1–63 days) and group 2 (median 4 days; range 2–37 days; P=0.984). However, with a median of 11 days (range 8–28 days), patients dying during the waiting period (group 1) stayed clearly longer on ECMO compared with those transplanted (P=0.045).
The median intubation time before LTX or death was 12 (range 11–35) days for group 1, 7.5 (range 4–44) days for group 2, and 8.5 (range 0–98) days for group 3 (Kruskal-Wallis test: P=0.344; group 2 vs. group 3: Mann-Whitney U test: P=0.597).
Operative characteristics are summarized in Table 2. All patients transplanted received bilateral grafts, with the intention to remove any possible source of infection within a remaining lung. However, only in seven patients standard bilateral LTX was performed. The other types of TX were size-reduced bilateral LTX (n=8), bilateral lobar LTX (n=16), split lung LTX (n=2), and bilateral lobar LTX after ex vivo lung perfusion (n=1).
According to the severity of the clinical situation, all transplantations had to be performed with intraoperative support. Because venoarterial (v/a) ECMO represents the standard intraoperative support technique for LTX in our department anyway (5), LTX was performed on the running ECMO with inguinal v/a cannulation in 14 patients. Fifteen patients were switched from inguinal to central ECMO cannulation intraoperatively. Only three patients were transplanted on the running venovenous (v/v) ECMO, whereas cardiopulmonary bypass became necessary in two patients only.
In 24 of the 34 patients, the v/a ECMO support was prolonged into the postoperative period to provide a smooth recovery to the transplanted lung, or to overcome periods of hemodynamic instability, a strategy reported before (3). The median time of ECMO prolongation was 2 days (range 1–6 days) for group 2 and 2 days (range 1–14) for group 3. Three patients received blood group nonidentical grafts.
Complications in the postoperative period included need for hematothorax evacuation (n=11), reperfusion edema primary graft dysfunction grade 3 (n=6), a high number of different neurological complications including posterior reversible encephalopathy syndrome (n=6), cerebral embolization (n=2), grand mal epilepsia (n=4), organic psychosyndrome (n=3), critical illness polyneuropathy (n=2), and need for temporary hemofiltration or hemodialysis (n=10).
Outcome results are summarized in Table 3. The majority of the patients (n=26) were weaned from intubation over a tracheostomy.
Median intubation time after LTX was 24.5 days (range 1–180 days) for group 2 and 20.5 days (range 3–45 days) for group 3 (P=0.887). Median postoperative time in the intensive care unit was 24.5 days (range 1–180 days) for group 2 and 26 days (range 10–51 days) for group 3 (P=0.903). Median postoperative hospital stay was 24.5 days (range 1–180 days) for group 2 and 47.5 days (range 21–90 days) for group 3 (P=0.239).
Twenty-six of the 34 transplanted patients were discharged from the hospital. The eight patients dying in hospital deceased due to cardiac arrest (n=1), cerebral embolism (n=1), sepsis (n=3), and multiorgan failure (n=3).
From the 26 patients discharged, 23 are still alive. One patient died from sudden cardiac arrest of unknown origin at home 3 months after LTX, one other patient died from ongoing rejection triggered by cytomegalovirus infection 11 months after TX, and one further patient died from ongoing rejection 39 months after TX.
All patients transplanted for idiopathic pulmonary fibrosis (IPF) and pulmonary hypertension survived the perioperative period and were discharged, in contrast to patients transplanted for cystic fibrosis (CF) and other indications. However, there was no difference in the late outcome according to indication (see Figure 1, SDC 2,http://links.lww.com/TP/A617).
One-, 3-, and 5-year survival was significantly worse for the patients after bridge to LTX when compared with all other LTX patients within the same period of time (60%, 60%, and 48% vs. 80%, 72%, and 65%, respectively; P=0.003, 0.028, and 0.018, respectively; see Figure 2, SDC 3,http://links.lww.com/TP/A618).
However, no statistically significant difference was detected for 1-, 3-, and 5-year survival conditional on 3-month survival for patients bridged with ECMO to LTX (78%, 78%, and 63%) compared with all other LTX patients transplanted within the same period of time (90%, 80%, and 72%, respectively; P=0.09, 0.505, and 0.344, respectively; see Figure 3, SDC 4,http://links.lww.com/TP/A619).
This article reviews the currently largest institutional experience with LTX after bridge with ECMO. So far, the worldwide experience with this advanced form of treatment has been limited. An important reason for this fact is the existence of a general reluctance to transplant patients in such a severe condition, an attitude that is mainly based on dismal outcome expectations. Further reasons why such a procedure has been performed only in a limited number of patients lie in unfavorable allocation regulations, which in some countries do not allow to allocate organs quickly to these patients, and in the general lack of donor organs. At least the later two factors were not of relevance in the logistic background of our own institution, which gave us the opportunity to accumulate this uniquely large experience.
The hitherto existing publications about LTX after bridge with ECMO mainly consist of small patient series (3–23) (Table 4). There are only three larger institutional reports (Nr. 5, 17, and 23 in Table 4), which summarize an experience obtained in more than 10 patients. One of them derives from the Hannover group (8) and reports about 10 patients bridged for TX with the pumpless ECMO device Novalung. Outcome in this series was excellent with 8 of 10 patients surviving longer than 1 year, although it has to be taken into consideration that Novalung support usually reflects a less advanced condition of the patients. The second report derives from two Scandinavian centers (18), which describe similar good results with 10 survivors of 13 transplanted. Finally, the Pittsburgh group reported on 17 cases, including also 6 retransplant procedures for primary graft dysfunction, where 13 patients survived longer than 1 year (24). Recently, Mason et al. (25) have reported the total US experience with primary LTX from ECMO. In the time period from 1987 until 2008, a total of 15,934 patients were transplanted, of them 586 were already ventilated at the time of TX and only 51 were bridged with ECMO. One-year survival for nonintubated patients, patients on ventilation, and patients on ECMO was 79%, 62%, and 50%, respectively.
Comparing these results obtained in a large number of different institutions with the 60% 1-year survival rate described here, and with the results from the Hannover group (80%), the Scandinavian centers (92%), and the Pittsburgh group (74%), one comes to the conclusion that with increasing experience, primary LTX from ECMO can be a procedure with distinct value. Although survival is of course lower than after elective TX, it is definitely not disastrous, and the observed difference in survival is actually smaller than one might have expected. The interpretation of these results has also to be taken into consideration that the expected mortality in this particular ECMO-depending patient group would have been 100% without TX, which implies that the gain in survival for these patients is actually a huge one. It also is an important argument in the ongoing discussion, whether organs should be allocated to patients, especially patients with chronic obstructive pulmonary disease, in whom LTX leads to a clear improvement in quality of life but not necessarily in survival (26).
There is another aspect in which the herein described group of patients differ from the US data. Although in the United Network for Organ Sharing registry only non-CF patients were bridged with ECMO, 44% of our patients had CF as the underlying disease. Of these 15 patients, 10 (66%) became long-term survivors. Even much better results were observed for the group of IPF and idiopathic pulmonary hemosiderosis patients, where all patients survived the perioperative period.
This article summarizes the results obtained in all patients in our department, who were either listed for TX while being already on ECMO support or who had already been on the waiting list and needed ECMO bridging during their waiting period. In the same period of time, there were of course other patients on ECMO in our institution, who never were considered for TX and therefore did not enter this analysis. Bridging methods among our patients varied according to their clinical needs. Eighteen patients were on v/v and 15 on v/a ECMO support. Novalung alone was used for bridge in one patient only. The remaining four patients progressed from Novalung or v/v ECMO to v/a ECMO. This reflects the different clinical situations in which the patients presented and also the sometimes stepwise increasing need for higher levels of support in some of them. In fact, all three different bridging modalities, Novalung, v/v ECMO, and v/a ECMO, provide a different capacity for oxygenation, CO2 removal, and hemodynamic effects (Table 5). Novalung has a limited potential to increase PO2 and therefore is only useful in situations with isolated PCO2 elevation. v/v ECMO results in both improved oxygenation and CO2 removal. However, its effect on PAP is limited and only an indirect result of the PCO2 normalization. For this reason, v/a ECMO is indicated whenever a significant PAP reduction is required. At the same time, the three devices also own a different spectrum of invasiveness and a different potential for complications. For all these reasons, it is important to choose the optimal support device to minimize complications and at the same time to optimize the support effect.
All these transplantations, except two, were performed on intraoperative ECMO support. This, in fact, represents the standard mode for circulatory support during LTX, which is used in our department since many years (3). It has replaced the use of cardiopulmonary bypass in this indication almost completely and has allowed us to obtain a uniquely large experience with LTX on ECMO, skills that also became important for the handling of ECMO during the bridge period. In fact, v/a ECMO support is in our experience an optimal approach to provide complete hemodynamic stability during the TX, and most importantly to allow a controlled reperfusion of the first transplanted lung by taking away at least half of the cardiac output from its pulmonary circulation. It is reasonable to prolong these conditions of controlled reperfusion over the TX itself into the early postoperative period with the intention to continue these optimal conditions for stabilization of the patient and especially for recovery of the transplanted lung. Especially in the complex situation in which these patients were transplanted, with disorders in their fluid balance, impaired kidney function, and sometimes hemodynamic instability, this concept turned out to be particularly beneficial. It also allowed us using donors of marginal quality, and in this way to avoid that patients became immediately depending on the function of the transplanted lung.
Whenever a patient is waiting for LTX on ECMO support, it is of crucial importance to find a donor organ in short period of time. To make this possible, the use of donor lungs that became available was handled aggressively with regard to size matching, use of marginal donors, and TX over the blood group. This resulted in 17 patients receiving lobar TX from much larger donors, one of them after ex vivo perfusion of a lung with otherwise inacceptable quality and two further patients receiving split LTX (27). Three patients received blood group-compatible but nonidentical grafts. The short median waiting time on ECMO of 5 days only in the group of transplanted patients was the result of this strategy, and it underlines the importance to apply all available technical options to make early TX possible. On the other hand, some patients did not receive “the next” lung, simply because they were temporarily in an unstable and unpredictable situation, which did not allow to proceed to LTX. In fact, the decision whether a patient on ECMO bridge can be transplanted or should be postponed or turned down must be performed based on daily assessment. So far, in center-oriented allocation, responsibility for the patient (urgency) and responsibility for the graft (outcome) are balanced upon similar principles, but in a different way than in a patient-oriented system (LAS). For this reason, it could be of interest to calculate LAS for the patients transplanted from ECMO and to compare the score to other patients transplanted in the same period. However, this was impossible for several reasons. First, ECMO is not yet an own variable in the LAS calculator. Second, this is a retrospective study over a long period of time and LAS data were not collected in the past.
Besides the previously discussed impact of indications, we have tried to identify other prognostic factors for survival after LTX. However, it became impossible to draw further clear conclusions in that regard. One certainly would expect that length of bridge should play an important role. In fact, the longest time on bridge in our cohort of patients resulted in successful TX after 63 days, and there was also no statistically significant difference in time on bridge between survivors and nonsurvivors. Only the few patients who did not reach LTX had a significantly longer time on device.
Attitudes toward TX of patients from ECMO bridging have undergone a clear change over time. Early on, such a procedure was considered to be a desperate maneuver with limited chances for success, not worth the investment of the valuable resource of a donor lung. However, with growing experience, it became obvious that use of ECMO before LTX not only owns the potential to stabilize the patient but even more to improve his condition. This resulted in a tendency for earlier use of ECMO, which most recently cumulated in its use in nonintubated patients (13–17, 19–23) as an alternative to mechanical ventilation. This change in paradigm from simple “bridging” toward the combination of “bridging and improvement” reflects a completely new approach to the problem and opens a window of opportunity for a group of patients who otherwise would definitely have a 100% mortality. It will be an important task for the future to reposition “LTX from mechanical circulatory support” into the current selection and indication processes and to define its optimal position. The results reported in this article hopefully contribute to a better understanding of the procedure itself and at the same time intend to be of help to further develop and improve the logistic background.
MATERIALS AND METHODS
This retrospective study includes all patients bridged with mechanical circulatory support (i.e., ECMO or Novalung) for primary LTX since the initiation of our transplant program in 1989. The first patient transplanted with this strategy was identified in January 1998, and we analyzed all consecutive patients with intention to bridge to LTX without any selection until June 2011. In this time period, 930 LTX have been performed in our department; out of them, 38 patients have been bridged on ECMO with the intention for primary LTX. During this time period, the annual number of bridge procedures showed a constant rise, cumulating in 12 cases in 2010.
Of the 38 bridged patients, 14 were already on the waiting list for LTX for different time periods before they deteriorated and required ECMO support, whereas the remaining 24 patients were newly listed for LTX. Sixteen of the patients came from outside institutions, 14 in an intubated status at the time of transfer. Seven of the 14 intubated patients were transferred while already being on ECMO. ECMO support was initiated in presence of severe hypoxia (PAO2 <60 mm Hg) or hypercarbia (PaCO2>100 mm Hg) despite maximal ventilation support, or, in patients with pulmonary hypertension, in case of rapid hemodynamic deterioration despite maximal inotropic support and intravenous (IV) epoprostenol therapy.
Demographic data, type of bridging and TX, all relevant pre-intraoperative and perioperative parameters, complications, and outcome were recorded and analyzed. Patients were divided into group 1 (dead on bridge); group 2 (in hospital death); and group 3 (patients discharged).
Between 1998 and 2011, 38 patients (25 women; median age 30.1 years; range 13–66 years) underwent ECMO support with intention to bridge to primary LTX (see SDC 5,http://links.lww.com/TP/A620). Underlying diseases of the patients were CF (n=17), pulmonary hypertension (n=4), IPF (n=9), adult respiratory distress syndrome (n=4; in one patient as sequel of H1N1 infection), hemosiderosis (n=1), bronchiolitis obliterans (n=1), sarcoidosis (n=1), and bronchiectasis (n=1).
Patients had a number of relevant comorbidities, including type 1 diabetes (n=1), Crohn's disease (n=1), epilepsia (n=1), and cholestasis (n=1), together with other additional risk factors consisting of bilateral talc pleurodesis (n=1), tracheostomy (n=4), severe cachexia (n=2), heparine induced thrombocytopenia (n=2), 100% panel reactive antibodies level (n=1), temporary need for hemofiltration (n=4), and prolonged high-dose steroid medication (n=5).
v/v ECMO was used as a bridge modality in 18 patients, and in 2 of them in combination with double-lumen cannula (Avalon) cannulation. v/a ECMO was used in 15 other patients. One patient was bridged with the pumpless Novalung device alone. The remaining four patients needed a stepwise increase in their support modality with switch from v/v to v/a ECMO (n=2), from Novalung to v/v ECMO (n=1) and from Novalung to v/a ECMO (n=1).
ECMO bridging was performed with the Medtronic portable bypass system (Medtronic Bio-Console 560, Medtronic Inc., Minneapolis, MN) with a hollow fiber oxygenator (Medtronic CPMPCB Affinity BPX-80 or Affinity NT, Medtronic Inc.) or a polymethylpentene membrane oxygenator (Quadrox; Jostra, Hirrlingen, Germany; see SDC 6,http://links.lww.com/TP/A621). ECMO support was used both in v/v and v/a settings in this series. For cannulation of the artery, a Bio-Medicus Cannula 15 to 17 Fr and for venous access a Bio-Medicus Cannula 17 to19 Fr were used (all from Medtronic Inc.). An additional limb cannula of 8 to 10 Fr was used whenever clinically indicated. More recently, the single double-lumen cannula (Avalon Elite Bi-Caval dual lumen catheter; Avalon Laboratories, LLC, Rancho Dominguez, CA) (28) was used in two patients.
If patients were switched to central cannulation intraoperatively, a Medtronic DLP 22 Fr Curved Tip cannula was used in the ascending aorta, and a Medtronic MC2X Three Stage 29/37 Fr venous cannula was used in the right atrium. Both the cannulae and the circuits were fully heparin coated (Medtronic Carmeda BioActive Surface). Priming solution consisted of 200 mL Ringer's lactate solution. The flow was set according to clinical needs.
Pumpless ECMO support was performed with the recently described Novalung (interventional lung assist; Novalung GmbH; Hechingen, Germany) device (8), which allowed a arteriovenous pulsatile blood flow driven by the cardiac output over a low resistance, protein matrix-coated diffusion membrane. Cannulation was performed with Seldingers technique, using a 15 Fr cannula for the left femoral artery and a 17 Fr cannula for the right femoral vein. Priming solution was 0.9% NaCl.
A single bolus dose of 70 IU/kg body weight Na-heparin was routinely administered IV immediately before cannulation followed by a continuous IV administration of Na-heparin with the goal to keep activated clotting time between 150 and 180 sec or partial thromboplastin time between 55 and 60 sec (see SDC 7,http://links.lww.com/TP/A622). This standard anticoagulation was discontinued immediately before the TX, and the further intraoperative and postoperative heparin management was adapted on an individual basis, according to the risk-benefit scaling of the surgeon. In most cases, continuous heparin was not restarted, even when ECMO was prolonged postoperatively.
Antiinfectious Management During the Bridging Period
All patients received broad-spectrum antibiotic prophylaxis with piperacillin/tazobactam or targeted antibiotic therapy according to the most recent antibiogram (see SDC 8,http://links.lww.com/TP/A623). In patients with CF, double antibiotic therapy was standard. Fungal prophylaxis with either fluconazole or voriconazole was routine.
All patients were immunosuppressed with a triple therapy consisting of cyclosporine or tacrolimus, mycophenolate mofetil, and prednisolone (see SDC 9,http://links.lww.com/TP/A624). In some of the CF patients, induction therapy with anti-T-cell globulin (n=4) or alemtuzumab (n=1) was performed.
Continuous data are shown as median and corresponding range (see SDC 10,http://links.lww.com/TP/A625). In nonparametric distributed data, Mann-Whitney U test was used to detect significant differences between two groups and Kruskal-Wallis test for more than two groups. Survival was estimated according to the method of Kaplan-Meier and the log-rank test was used to detect significant survival differences between the corresponding groups. The association of the three groups with clinical characteristics (gender, diagnosis, and bridge type) was assessed by the two-sided chi-square test. P values are always given as two-sided and were considered statistically significant below 0.05. All statistical analyses were performed using the PASW Statistics 18.0 package (Predictive Analytics Software; SPSS Inc., Chicago, IL).
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