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Ann Thorac Surg 2011;91:250-255. doi:10.1016/j.athoracsur.2010.09.005
© 2011 The Society of Thoracic Surgeons
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Right arrow Lung - transplantation
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Original Articles: General Thoracic

Extracorporeal Circulatory Systems as a Bridge to Lung Transplantation at Remote Transplant Centers

Assad Haneya, MDa,*, Alois Philipp, ECCPa, Thomas Mueller, MDc, Matthias Lubnow, MDc, Michael Pfeifer, MD, PhDc, Wolfgang Zink, MD, PhDb, Michael Hilker, MD, PhDa, Christof Schmid, MD, PhDa, Stephan Hirt, MD, PhDa

a Department of Cardiothoracic Surgery, University Medical Center Regensburg, Regensburg, Germany
b Department of Anesthesiology, University Medical Center Regensburg, Regensburg, Germany
c Department of Internal Medicine II, University Medical Center Regensburg, Regensburg, Germany

Accepted for publication September 3, 2010.

* Address correspondence to Dr Haneya, University Medical Center Regensburg, Department of Cardiothoracic Surgery, Franz-Josef-Strauss-Allee 11, Regensburg D-93053, Germany (Email: assadhaneya{at}web.de).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Worsening of lung function in patients awaiting lung transplantation can lead to ventilation-refractory hypoxemia or hypercapnia and respiratory acidosis. This report describes the successful use of different extracorporeal circulatory systems as a bridge to transplantation at remote centers.

Methods: Between January 2003 and December 2009, we had 10 requests for implantation of extracorporeal circulatory systems (pumpless extracorporeal lung assist [PECLA] or extracorporeal membrane oxygenation [ECMO]) in patients decompensating on the waiting list to bridge to transplantation at three different transplant centers between 150 km and 570 km apart. Cannulas were inserted percutaneously with Seldinger's technique.

Results: The median patient age was 36 years (range, 24 to 53). Three patients were supported with PECLA and 7 with ECMO. The median duration of support was 23 days (range, 5 to 73). Two patients were initially provided with ECMO and then changed to PECLA after hemodynamic stabilization in the face of persisting pulmonary failure. Two patients died of multiorgan failure on ECMO while on the waiting list. One PECLA patient was successfully weaned and waiting for LTx. Before transplantation, 5 patients (4 PECLA and 1 ECMO) were successfully weaned from mechanical ventilation, and 3 PECLA patients were successfully weaned from the system. Seven patients were successfully bridged and transplanted. Five of 7 patients were discharged from the transplant centers.

Conclusions: This report suggests that implantation of extracorporeal circulatory systems is a safe method to bridge patients decompensating on the waiting list for transplantation. Support intervals of several weeks are possible.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Lung transplantation (LTx) is widely accepted as a routine surgical procedure and an established therapeutic option for end-stage respiratory failure [1, 2]. Lung transplantation is seldom an emergency procedure; the majority of pulmonary transplants are performed in patients with slowly progressive pulmonary disease, such as chronic obstructive pulmonary disease, idiopathic pulmonary fibrosis, cystic fibrosis, and primary pulmonary hypertension [3]. Increasing numbers of patients listed for LTx face a scarcity of suitable organ donors, leading to prolongation of waiting time and increasing waiting list morbidity and mortality [4]. Worsening of lung function in these patients can lead to ventilation-refractory hypercapnia and respiratory acidosis or acute hypoxemic respiratory failure. As a consequence, more patients require advanced respiratory support as a bridge to LTx. Previously reported approaches to bridge to LTx include mechanical ventilation and extracorporeal circulatory systems (ECS). Extracorporeal circulatory systems with a blood pump, the extracorporeal membrane oxygenation (ECMO), or without a blood pump, the pumpless extracorporeal lung assists (PECLA) using capillary membrane oxygenators, can provide sufficient gas exchange and prevent barotrauma of the lung. Both mechanical ventilation and ECS have been identified as risk factors of mortality after LTx when applied before LTx [4].

As lung transplantation is not possible so far in our center, patients underwent implantation of ECS as a bridge to LTx at remote transplant centers. This report describes our successful experiences in 10 consecutive patients supported with different ECS as a bridge to LTx at remote transplant centers.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Between January 2003 and December 2009, the Department of Cardiothoracic Surgery, University Medical Center, Regensburg, Germany, had 10 requests for implantation of ECS as a bridge to LTx in patients with ventilator-refractory hypoxemia or hypercapnia with accompanying severe respiratory acidosis. After approval by the local Ethics Committee, we reviewed data of these 10 patients.

Patients from regional hospitals who were potential ECS candidates were transferred to our center. If the patients were too unstable for conventional transport, they were placed on ECS at the referring hospital and then transported to our institution on active ECS. The transport team included an anesthesiologist experienced in cardiopulmonary bypass, a perfusionist, and a nurse or paramedic. For ground transport, a special intensive care transport vehicle was used. For air medical transport, a rescue helicopter of the Air Rescue Center Regensburg was available [5].

Before patients were considered potential candidates for ECS, their clinical course was carefully evaluated. That included optimization of volume and vasoactive agent requirements, lung-protective ventilation (moderate hypercapnia, increase in respiratory rate, high positive end-expiratory pressure), the use of adjunctive therapeutic measures, such as prone position [6] or continuous lateral rotation therapy [7], as well as treatment of the underlying disease in accordance with standard intensive care procedures.

Before ECS implantation, all patients received an intravenous single dose of heparin of 5,000 IU. The systemic anticoagulation therapy was given by continuous infusion of standard heparin. The effect of heparin was measured through the activated partial thromboplastin time. As the whole system was coated with heparin, a pronounced systemic anticoagulation was unnecessary, and an activated partial thromboplastin time of 1.5 normal was considered sufficient. Usually 100 mg per day of acetylsalicylic acid were given to inhibit platelet aggregation. Oxygen was used as sweep-gas with a flow of 1 to 12 L/min. All cannulas were inserted percutaneously employing the Seldinger technique in the intensive care unit [5].

Pumpless Extracorporeal Lung Assist
Pumpless extracorporeal lung assist, also termed interventional lung assist (iLA [NovaLung-GmbH, Talheim, Germany]), is an extracorporeal gas exchange procedure that was devised in our center in 1996 [8, 9]. In principle, PECLA is an artificial arteriovenous shunt with an interposed membrane oxygenator. This arteriovenous bypass procedure uses the arteriovenous pressure difference as the driving force for the blood flow (1 to 2 L/min) through an oxygenator, so that a pump is not needed. Accordingly, only patients with an adequate mean arterial blood pressure and sufficient cardiac output are suitable candidates for this procedure. It is primarily indicated for patients with inadequate elimination of CO2, namely, with severe hypercapnia and moderate hypoxia [10]. After ultrasonographic identification and assessment of the diameters of the femoral artery as well as of the contralateral femoral vein, cannulas (NovaLung-GmbH, Talheim, Germany) were implanted using Seldinger's technique. The size of the arterial cannula was individually selected, based on vessel diameter to ensure sufficient peripheral blood flow, with a residual lumen of 30% after insertion. The diameter of the arterial cannula was chosen to be 15F or 17F, based conditionally on adequate residual volume. The venous cannula was typically selected two French sizes larger than the arterial cannula in order not to compromise flow resistance. The primed oxygenator, which had a total exchange surface of 1.3 m2 and a very low inherent resistance, was then connected to the flushed cannulas. The membrane of the oxygenator was made of polymethylpentene, with the advantage of no plasma leakage [11, 12].

Extracorporeal Membrane Oxygenation
The technique of ECMO for patients with severe acute respiratory distress syndrome involves placing them on a venovenous (VV) or venoarterial (VA) life support circuit with a membrane oxygenator to temporarily the gas exchange function of the lung. While on ECMO, the mechanical ventilator settings are adjusted to minimize ventilator-induced lung injury and to maximize the recruitment of functional residual lung capacity [13, 14].

Our ECMO system consisted of a centrifugal pump (Rotaflow; Maquet Cardiopulmonary-AG, Hirrlingen, Germany) with an integrated battery for transport, a polymethylpentene membrane oxygenator (PLS-QuadroxD; Maquet Cardiopulmonary-AG), which avoided plasma leakage and had a total gas exchange surface of 1.8 m2 with a very low inherent resistance and two cannulas. The filling volume of the complete device was between 400 mL and 500 mL, depending on the length of the tubing [14].

Venovenous ECMO was the preferred mode of support for isolated respiratory failure. For outflow, commonly the right femoral vein was cannulated with a long 21F to 23F single-stage cannula (BFV 900-312; Sorin-Group Deutschland-GmbH, Munich, Germany). For reinfusion, a short 15F to 17F cannula (NovaLung-GmbH, Talheim, Germany) was used, and was usually implanted in the right internal jugular or right subclavian vein.

Venoarterial ECMO was used when systemic arterial perfusion support was necessary in addition to respiratory support. Venous access was usually gained by a femoral vein cannulation (21F to 23F) with arterial return into the common femoral artery (15F to 17F). All cannulas were inserted percutaneously employing the Seldinger technique. The size of the arterial cannula had to be smaller than the diameter of the vessel to ensure sufficient peripheral flow. Basic monitoring of the lower extremities included continuous limb pulse oxymetry distal to the arterial cannulation site, determination of serum lactate and creatine kinase levels, as well as clinical inspection for any signs of restricted perfusion or ischemia. Blood gas analysis was done with a Radiometer-700 (Radiometer, Copenhagen, Denmark).

After implementation of the ECS, invasiveness of ventilation was reduced to diminish further ventilator-induced lung injury. Accordingly, tidal volume, minute ventilation, positive inspiratory pressure (PIP), and fraction of inspired oxygen (FiO2) were decreased. Positive end-expiratory pressure was initially not reduced to avoid atelectasis due to small tidal volume (typically FiO2 less than 0.5, PIP less than 27 cm H2O) [14].

As lung transplantation is not possible so far in our center, the patients were kept in our hospital and transported to a remote transplant center (Hannover Medical School, University Medical Center Munich or Vienna General Hospital) when donor organs became available.

Statistical Analysis
The statistical analysis was performed using the SPSS 16.0 software (SPSS, Chicago, IL). Normal distribution was assessed by Lilliefors' modification of the Kolmogorow-Smirnow test. Values of continuous data are presented as mean ± SD or as median with interquartile range when appropriate. Categorical variables are displayed as frequency distributions (n) and simple percentages (%). Univariate comparison between the groups for categorical variables was made using the {chi}2 test and Fisher's exact test when appropriate. Statistical significance was considered when p was less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
During the observation period, 10 patients were considered for bridge to LTx. Eight patients were successfully implanted with an ECS device at our center. Two patients from outside hospitals were too unstable for conventional transport, and were placed on ECS at the referring hospital and then transported to our institution on active ECS. Patient characteristics are given in Table 1. The median age was 36 years (range, 24 to 53), and 70% were female. Before ECS implantation, all patients were mechanically ventilated and sedated. Indications for lung transplantation were cystic fibrosis in 4 patients, idiopathic pulmonary fibrosis in 3 patients, bronchiolitis obliterans in 1 patient who was listed for redo LTx, chronic obstructive pulmonary disease in 1 patient, and pulmonary hypertension in 1 patient. Eight patients were on the transplant waiting list at the time of ECS implementation. Two patients had been listed after their intervention. The median Sequential Organ Failure Assessment score was 9.5 (range, 4 to 15), and the median Lung Injury Score was 3.2 (range, 2.5 to 4.0). The median duration of support was 23 days (range, 5 to 73). Three of the patients were supported with PECLA, 5 were supported with VV-ECMO, and 2 were supported with VA-ECMO. In 1 case, the VV-ECMO was changed to PECLA, and in another case, the VA-ECMO was changed to PECLA (Table 2). They were initially provided with VV-ECMO or VA-ECMO and then changed to PECLA by removal of the pump from the circuit after hemodynamic stabilization in the face of persisting pulmonary failure. Table 3 summarizes changes in arterial blood gases, arterial pH, inotropic support, and mean arterial pressure over time. Two hours after ECS implantation, the PaO2/FiO2 ratio, PaCO2, and pH levels had significantly improved and remained stable.


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  		Table 1 Patient Data and Characteristics Before Extracorporeal Support (ECS)
 

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  		Table 2 Overview of Extracorporeal Support (ECS) and Patient Outcome
 

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  		Table 3 Changes in Blood Gases, Hemodynamics, and Inotropic Support
 
Technical problems that could not be controlled were not observed. The oxygenators were approved for 14 days. An exchange of the oxygenator was necessary in 5 patients. Two patients had heparin-induced thrombocytopenia type II. The anticoagulation agent was changed to argatroban (Argatra; Mitsubishi Pharma Europe, London, UK). In this case, exchange of the oxygenator was necessary at short intervals, which resulted in an average oxygenator time of 8 days overall. Transient episodes of lower limb ischemia after arterial cannulation occurred in 1 patient on PECLA, and were resolved by removal of the cannula, resulting in normalization of distal perfusion. Surgical intervention was not necessary. Other serious complications with an adverse effect on outcome were not observed (cannula thrombosis, bleeding). Infections associated with the ECS implantation were not observed. As the reason of acute deterioration in most patients was an infectious complication, all patients had been on broad-spectrum antibiotic treatment already before ECS.

Two patients died of multiorgan failure in our hospital while on ECMO on the waiting list. Before transplantation, 5 patients (4 PECLA and 1 ECMO) were successfully weaned from ventilator, and 3 PECLA patients were successfully weaned from ECS. Seven patients (4 PECLA and 3 ECMO) were successfully bridged and transplanted at remote hospitals. One patient was successfully weaned from PECLA and is still waiting for LTx. patients (3 PECLA and 2 ECMO) were discharged from the transplant centers. The postoperative intensive care unit stay was 19 days (range, 2 to 33). Two patients died of multiorgan failure 3 and 5 weeks after LTx in the transplant centers (Table 2).


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
"Bridging" patients to LTx by extracorporeal devices has a history. In 1975, the first case of ECMO as a bridge to lung transplant was performed for posttraumatic respiratory failure [15]. In 1991, the Hannover group published the first report of long-term survival after using ECMO as a bridge to redo lung transplant [16]. From 1975 to the early 1990s, 7 patients underwent lung transplantation after ECMO application for acute severe respiratory failure, with disparate results [15–17]. Consequently, ECMO was considered to be a contraindication to LTx. The widely known side effects of ECMO, such as hemolysis, bleeding complications, severe infection, and renal insufficiency, certainly contributed to this poor outcome. Moreover, ECMO could only be applied reasonably for several days.

Meanwhile, several technical improvements have occurred. The first important technical advance was the development of a new generation of centrifugal pumps. In comparison with traditional roller pumps, the centrifugal pump has virtually no risk of tubing rupture or spallation; it has a smaller priming volume, it does not require the use of a reservoir, and it has an equivalent low incidence of hemolysis [18]. The introduction of heparin-coated circuits has led to reduced platelet activation, reduced complement activation, reduced granulocyte activation, and greatly reduced heparin requirements [19]. In contrast to silicone membrane oxygenators, the polymethylpentene oxygenator has reduced red blood cell and platelet transfusion requirements, better gas exchange, lower resistance, lower priming volume, and an incorporated heat exchanger. In contrast to polypropylene microporous oxygenators, the polymethylpentene oxygenator has a greatly reduced rate of oxygenator failure [20]. We have previously reported the successful use of miniaturized ECMO systems as a bridge to recovery or to LTx in patients with respiratory failure [14].

Until 2009, in the previously published cases, 19 bridge-to-LTx procedures have been performed worldwide. The 1-year survival was 68%, which is encouraging, suggesting the use of ECMO as a bridge to LTx [21]. This compares with the current benchmark 1-year survival of 78% for lung transplant recipients from January 1994 through June 2006 [4]. In our report, 7 patients were supported with ECMO. Two ECMO patients were initially provided with ECMO and then were changed to PECLA after hemodynamic stabilization in the face of persisting pulmonary failure. Five (3 with ECMO and 2 with PECLA) of the 7 patients (71%) were successfully bridged and transplanted at remote hospitals. Three patients were discharged from the transplant centers (Table 2). Our cases are of particular interest because the duration of ECMO support was relatively long (as long as 67 days) in comparison with previously reported cases, and also because 71% of patients with initially ECMO support were successfully bridged and transplanted. None of the typical complications related to ECMO, such as bleeding, hemolysis, or ischemia of a lower limb, was observed.

Until recently, ECMO was the only treatment option for patients with ventilation-refractory lung failure require extracorporeal gas exchange while awaiting transplantation [22]. Although occasionally successful as a bridge to recovery or transplant, ECMO is associated with a range of severe complications [16]. The concept of interventional lung assistance was mentioned by Rashkind and colleagues [23] in 1967. In experimental investigations, a pumpless extracorporeal interventional lung assist system using the animals' arteriovenous pressure gradient has been described [24, 25]. The clinical development of the PECLA system has been performed in our hospital since 1996, and the experience with the first cases were published in 2000 [8, 9]. The system is characterized by a new membrane gas exchange system based on heparin-coated hollow fiber technology with optimized blood flow by reduction of resistance. The system does not need extended technical and staff support, and the main advantage is easy handling. The system runs with a "low-dose" heparin infusion that does not exceed normal antithrombotic anticoagulation of the intensive care patient [10]. In this pumpless mode, the device achieves sufficient CO2 removal, but oxygen transfer is limited owing to use of arterial blood and low blood flow. Therefore, this device is not suitable as a bridge to LTx in those patients with predominant hypoxemia. Sufficient oxygenation in patients can only be achieved with VV or VA pump-driven support, such as ECMO [22]. In 2006, the Hannover group reported the successful use of the pumpless Novalung as a bridge to LTx in 12 patients with severe ventilator-refractory hypercapnia. The duration of support was 15 ± 8 days (range, 4 to 32). Ten of these patients (83%) were successfully bridged and transplanted. The 1-year survival was 80% [22]. In this report, we could demonstrate similar findings. All 4 PECLA patients (2 patients were initially supported with ECMO) were successfully bridged and transplanted at remote hospitals. One patient was successfully weaned and waiting for LTx. Three patients were discharged from the transplant centers. The duration of support was between 5 and 64 days.

Replacement of ECMO by PECLA reduces the negative side effects of extracorporeal circulation [26]. In our report, 2 patients were initially provided with VV-ECMO or VA-ECMO and then were changed to a pumpless arteriovenous shunt with a membrane oxygenator by removal of the pump from the circuit after hemodynamic stabilization in the face of persisting pulmonary failure with inadequate elimination of CO2.

The most frequently used approach to bridge acute lung failure patients to recovery or to LTx is the use of noninvasive or invasive ventilatory support. During the past 2 decades, positive-pressure ventilation has helped to improve survival in patients with acute lung failure, but ventilator-associated lung injury remains a significant problem. There is evidence that mechanical ventilation before LTx is a significant risk factor for post-LTx mortality and often leads to multiple organ failure [27]. As a consequence, mechanical ventilation is still seen as a contraindication for LTx by many transplant centers. Our concept is to avoid mechanical ventilation by extracorporeal gas exchange or to wean from ventilation. The idea is to allow patients to be awake, to maintain or improve their muscular status, not only to achieve survival until transplantation but also to decrease early mortality after lung transplantation. After implementation of ECS, we observed a fast increase in CO2 removal and an improvement in oxygenation in all patients, allowing a significant reduction of ventilatory "aggression" rapidly. In the majority of cases, the ECS was an adjunct to mechanical ventilation that allowed use of optimized lung-protective ventilation strategies, with the objective of giving the lung time to heal while attempting to minimize ventilation-induced lung injury. In 5 cases, the patients were successfully weaned from ventilator, and the ECS was used without mechanical ventilation in the awake and nonsedated patient.

Nevertheless, our report has some limitations. The report is a single-center experience, and the number of patients is small.

In conclusion, our initial experience demonstrates the applicability of the ECS as a bridge to LTx in patients with end-stage lung failure decompensating on the waiting list. Support over a period of some weeks is possible [28]. Although ECS is often considered a contraindication to LTx, our report demonstrates the feasibility of prolonged ECS support leading to successful LTX.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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Respir Care, September 1, 2011; 56(9): 1445 - 1456.
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D. Hayes Jr, J. E. Lynch, and J. B. Zwischenberger
Invited Commentary
Ann. Thorac. Surg., January 1, 2011; 91(1): 255 - 256.
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