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Right arrow Lung - transplantation

Ann Thorac Surg 2004;78:1230-1235
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Extracorporeal Membrane Oxygenation after Lung Transplantation: Evolving Technique Improves Outcomes

Takahiho Oto, MDa,*, Franklin Rosenfeldt, MD, FRACSa, Michael Rowland, FRACSa, Adrian Pick, FRACSa, Marc Rabinov, FRACSa, Arthur Preovolos, CCPa, Gregory Snell, FRACPa, Trevor Williams, FRACPa, Donald Esmore, FRACSa

a Heart and Lung Transplant Unit, The Alfred Hospital, Monash University Medical School, Melbourne, Australia

Accepted for publication March 31, 2004.

* Address reprint requests to Dr Oto, Heart and Lung Transplant Unit, The Alfred Hospital, Commercial Rd, Melbourne 3004, VIC, Australia
takahirooto{at}aol.com


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Conclusion
 Acknowledgments
 References
 
BACKGROUND: Severe pulmonary graft failure (PGF) is the most common cause of death within the first 30 days after lung transplantation. Extracorporeal membrane oxygenation (ECMO) may provide lifesaving temporary support; however, its longer-term efficacy is controversial.

METHODS: We reviewed the use of ECMO for severe PGF after lung transplantation, and compared the outcomes between our early (1990 to 1999) and recent (2000 to 2003) experience utilizing improved initiation timing, oxygenator technology, and surgical technique.

RESULTS: Ten transplant recipients from a total of 481 (2.1%) were managed for PGF on ECMO by a multidisciplinary team at The Alfred Hospital. Four single-lung, 3 bilateral single-lung, and 3 heart-lung recipients were supported for a mean of 96 hours (range 14 to 212 hours). In the early group (operation from 1990 to 1999, n = 4) ECMO was initiated 21 days (range 7 to 40 days) after lung transplantation and in the recent group (operation from 2000 to 2003, n = 6) after 0 to 2 days (p = 0.01). Radial-arterial blood gas analysis 12 hours after initiation of ECMO showed significantly better oxygenation in the recent group (341 ± 90 mm Hg) than in the early group (90 ± 23 mm Hg, p = 0.03). Four deaths occurred as a result of bleeding (two in each group). In the early group only 1 patient was weaned from ECMO but died. In the recent group 3 were successfully weaned and were discharged from the intensive care unit; of these patients, 2 were discharged from hospital.

CONCLUSIONS: Extracorporeal membrane oxygenation results have improved with advances in oxygenator technology and surgical techniques. The procedure can allow resolution of early PGF after lung transplantation.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Conclusion
 Acknowledgments
 References
 
Despite improvements in donor lung preservation and surgical technique, 13% to 35% of patients have pulmonary graft failure (PGF) after lung transplantation (LTx) [1]. Some cases of PGF show rapid recovery; others develop prolonged allograft dysfunction with the requirement for intensive support leading to multiorgan dysfunction, irreversible organ damage, and death [1]. When PGF remains unresponsive to maximal conventional management, extracorporeal membrane oxygenation (ECMO) has the capacity to support gas exchange and to stabilize the condition of patient until the lungs recover. In the pediatric population ECMO has been shown to provide effective treatment for respiratory failure as well as PGF after lung transplantation [2]. In contrast, after adult lung transplantation only a few studies of ECMO for PGF have been reported and its efficacy in this setting is still controversial [3–5].

However, in recent years understanding of early and late graft failure has improved [1] and new materials and techniques for ECMO have been developed that may improve the efficacy of ECMO in the adult population [6]. The heparin-bonded hollow-fiber membrane oxygenator has superseded the silicone membrane oxygenator [7] and central cannulation has been shown to improve total body oxygenation [3]. In this context we reviewed our experience with the use of ECMO for severe PGF after LTx, and compared the outcomes between our early and recent experience.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Conclusion
 Acknowledgments
 References
 
The records of 12 patients placed on ECMO after LTx at The Alfred Hospital between March 1990 and September 2003 were reviewed retrospectively. During the same time period a total of 481 LTx were performed in this institution. Ten (2.1%) patients experienced PGF severe enough to require ECMO after failure of conventional therapy. Two patients required ECMO for other causes: 1 received ECMO for failure of mechanical ventilatory support due to dehiscence of the tracheal anastomosis and the other had a large pulmonary embolus 12 days after LTx and underwent resuscitative ECMO after pulmonary embolectomy. These 2 cases were excluded from this review, leaving four single-lung, three bilateral single-lung, and three heart-lung transplant recipients with PGF. One patient undergoing single-lung transplantation had pulmonary hypertension (PH) corrected by closure of an aortopulmonary window. Of the 2 patients undergoing combined heart-lung transplantation for PH secondary to cystic fibrosis, 1 patient had the procedure because of the institutional policy during the early period of our program and the other had scoliosis with rotated hilar structure that precluded bilateral single-lung transplantation. The criteria for selection of the donor and donor–recipient matching were along standard lines [8]; in addition, prospective T-cell and B-cell crossmatching was carried out routinely. Donor lung preservation involved pretreatment with a prostacyclin infusion (Flolan, Wellcome, Sydney, Australia) (40 to 80 ng · kg–1 · min–1) for approximately 10 minutes followed by a flush with cold 4 to 6 L modified Euro-Collins solution, delivered at a pressure of 40 cm H2O. Before tracheal stapling the lungs were inflated with 100% oxygen at a pressure of 5 cm H2O. Organs were stored in modified Euro-Collins solution and transported at 1° to 2°C. Immunosuppressive protocols included triple-drug therapy with corticosteroids, azathioprine or mycophenolate mofetil, and cyclosporine or tacrolimus, as described elsewhere [8].

Algorithm for Pulmonary Graft Failure After Lung Transplantation
With the start of the ECMO program at The Alfred Hospital we defined a standardized treatment protocol to guide decision making. All patients with PGF were included in this standardized treatment protocol, which proceeded conventional therapy after evaluation for the cause of PGF (Fig 1). A transesophageal echocardiography was performed to exclude lung torsion and pulmonary vascular problems, and a retrospective crossmatch was performed to exclude humoral rejection. Conventional therapy was constituted with pressure-controlled mechanical ventilation, limitation of positive end-expiratory pressure to 12 to 15 cm H2O, negative fluid balance with furosemide or continuous venovenous hemofiltration, inhaled nitric oxide at a dosage of 5 to 20 ppm, and elevation of the upper body or lateral positioning if appropriate. As an additional therapy, differential ventilation was considered for unilateral persistent PGF. Only if conventional therapy failed was ECMO considered.



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  		Fig 1. Algorithm for pulmonary graft failure after lung transplantation.

 
Extracorporeal Membrane Oxygenation Techniques
The ECMO strategy at The Alfred Hospital evolved over the 13-year period (Fig 2). In the first 2 cases, we used venovenous high-flow ECMO support by combined internal jugular and femoral vein cannulation. In the next 6 cases, we performed venoarterial ECMO cannulation through the femoral artery and femoral vein. In the last 2 cases, we avoided groin cannulation and performed direct central cannulation of the ascending aorta and the right atrium. The arterial cannula incorporated a 14-mm woven Dacron (C.R. Bard, Covington, GA) graft in place of the lighthouse tip (Abiomed, Inc, Danvers, MA); this graft was attached to the ascending aorta by an end-to-side anastomosis and venous cannulation was carried out through the right atrial appendage. Cannulas were externalized subcostally through tunnels from the pericardial space through the skin. A Medtronic Carmeda heparin-bonded tubing circuit (Medtronic Cardiopulmonary, Anaheim, CA) and the Biomedicus centrifugal pump (Medtronic, Minneapolis, MN) were used. For gas exchange the SciMed (Life-System Ltd, Minneapolis, MN) silicone fiber membrane oxygenator, Maxima PRF (Medtronic), the Affinity (Arecor Cardiovascular Ltd, Phoenix, AZ), and the Quadrox (Jostra Medizintechnik AG, Hirrlingen, Germany) hollow-fiber membrane oxygenator were used (Table 1). Heparin infusion was titrated to maintain an activated clotting time of 180 to 250 seconds for the first 24 hours, then titrated to achieve an activated partial thromboplastin time of 50 to 80 seconds. Extracorporeal membrane oxygenation flows were 2.1 to 2.4 L · min–1 · m–2. Once ECMO had been established, mechanical ventilatory parameters were reduced to minimize barotrauma and oxygen toxicity to the pulmonary grafts. Maintenance of ECMO was carried out by perfusionists and nurses under close supervision.



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  		Fig 2. Evolving extracorporeal membrane oxygenation (ECMO) strategy at The Alfred Hospital. Cannulation technique, oxygenator technology, and timing of initiation of ECMO have been improving.

 

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  		Table 1. Characteristics of Pulmonary Graft Failure Recipients Treated with ECMO

 
Statistical Analysis
Values given are mean ± SEM. Comparisons between the two groups were made using the Mann-Whitney U test for continuous variables and {chi}2 analysis for categorical variables. Significance was defined as p less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Conclusion
 Acknowledgments
 References
 
Of 32 patients with PGF after LTx that not respond to conventional therapy, 22 had unilateral PGF and 10 had bilateral PGF (Fig 1). Nine of the 32 nonresponders did not have further therapy for the following reasons: refusal by next of kin in 1, size limitation in 1, time limitation in 2, unresponsive septic shock in 3, and reason unknown in 2. All 9 had fatal outcomes. Although 15 patients underwent additional therapy, 2 of 15 were still nonresponders. The total of 10 LTx patients requiring ECMO for PGF included 4 women and 6 men, mean age 46 ± 5 years (Table 1). Cardiopulmonary bypass was used in 8 of the 10 transplant procedures for a mean of 200 ± 47 minutes. The incidence of cardiopulmonary bypass use during LTx was significantly higher in patients who required ECMO than our overall cardiopulmonary bypass use for LTx (80% versus 16%, p < 0.0001).

With the evolution of the techniques over time, for analysis we divided the patients into two groups: an early group (from March 1990 to December 1999) and a recent group (from January 2000 to September 2003) (Fig 2). The baseline characteristics of the donors including age, sex, and cause of death were similar between the two groups. No significant differences were noted between the early and the recent groups for duration of donor mechanical ventilatory support (43 ± 14 versus 49 ± 10 hours), donor PaO2 immediately before retrieval (551 ± 29 versus 512 ± 39 mm Hg), and the graft ischemic time (533 ± 57 versus 390 ± 61 minutes).

In the recent group, 4 patients were placed on ECMO on the day of LTx (day 0) and 1 patient each on day 1 and day 2, which was significantly sooner (0.5 ± 0.3 days) than in the early group (21 ± 8 days, p = 0.01) (Table 1). Recipient physiologic status 12 hours after initiation of ECMO support is shown in Table 2. Despite similar ECMO flow rates, radial-arterial blood gas analysis showed a significantly higher oxygenation in the recent group than in the early group (p = 0.03). Patients in both groups were well stabilized hemodynamically.


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  		Table 2. Physiological Results 12 Hours After Initiation of ECMO

 
In the early group 1 of 4 patients was successfully bridged to retransplantation, but died due to pulmonary hemorrhage after multisystem organ failure (MOF) 10 days after retransplantation (Fig 3). One other patient in the early group who was weaned from ECMO died due to persistent early graft dysfunction 12 days after weaning. No patient in the early group survived to be discharged from the intensive care unit (ICU). Multisystem organ failure was the most common cause of death in the early group (Table 3).



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  		Fig 3. Outcome of 10 patients who underwent extracorporeal membrane oxygenation (ECMO). (ICU = intensive care unit.)

 

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  		Table 3. Complications and Outcomes of ECMO Support

 
In the recent group 3 patients died during ECMO. One of the 3 patients died after being withdrawn from ECMO due to hypoxic brain death that probably had been sustained during resuscitation efforts before ECMO initiation. Three of 6 patients (50%) were successfully weaned from ECMO and discharged from the ICU. One of the 3 died of sepsis in hospital 3 months after weaning from ECMO. However, 2 of the 3 were long-term survivors; 1 was still alive 18 months after LTx and another survived for 3 years before dying of lung cancer.

Several complications were seen during ECMO support (Table 3). Four patients had bleeding requiring surgical exploration or multiple blood transfusions, and 1 of these also had sepsis. An ischemic limb was seen in 1 patient. These 5 patients all died. One patient required temporary hemofiltration due to acute renal failure.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Conclusion
 Acknowledgments
 References
 
After LTx, severe PGF is potentially life threatening. The incidence of severe PGF after LTx is between 13% and 35% [1]. Extracorporeal membrane oxygenation therapy may provide lifesaving temporary support, allowing time for the allograft to recover or as a bridge to retransplantation. Published series have reported that ECMO support was required for severe PGF in 2.7% of a total of 444 LTx [3], 3.6% of 220 LTx [9], 5.5% of 253 LTx [4], and 7.4% of 215 LTx [5]. In our experience, the incidence of ECMO requirement was 2.5% of 481 LTx. Although multiple factors contributed to our relatively low incidence of ECMO use, we believe the main determinants were (1) donor lung preservation involving pretreatment with a prostacyclin infusion, (2) prospective T-cell and B-cell crossmatching, (3) less use of cardiopulmonary bypass, (4) inhalation of nitric oxide during implantation, and (5) differential ventilation for unilateral PGF.

In the current study a higher incidence of ECMO support was seen after heart-lung (3/54, 5.6%) than single-lung (4/198, 2.0%) and bilateral single-lung transplantation (3/229, 1.3%). The patients with PH often had secondary cardiac disease and required heart-lung transplantation or bilateral single-lung transplantation with cardiopulmonary bypass. All the patients with PH could not be weaned from ECMO. Pulmonary hypertension seemed to be a predictor for poor outcome with the use of ECMO.

The most common indication of ECMO support after LTx is for reversible PGF; a less common indication is as a bridge to retransplantation due to irreversible PGF. Early PGF has been considered reversible and usually recovers in less than 7 days [3, 4]. Multiple factors may contribute to early PGF including prolonged ischemic time, ischemia-reperfusion injury, prolonged cardiopulmonary bypass use, massive blood transfusion, and poor quality of the donor lung itself [1, 4, 5]. In contrast, late PGF may be secondary to infection or rejection and may be irreversible [4]. Identifying specific conditions that contribute to PGF is difficult. Furthermore, the transition from early to late PGF varies according to the author's definition. Some authors defined early PGF as less than 7 days [5] and others defined it as within 24 hours of LTx [4]. All survivors in these 2 reports were in the early PGF group, whereas no survivors were noted with late PGF beyond 7 days after LTx. The authors concluded that early PGF was reversible and patients would recover while on temporary ECMO support. In our study, patients were placed on ECMO sooner in the recent group (0.5 ± 0.3 days) than the early group (21 ± 8 days, p = 0.01), and all 3 survivors in this study were in the recent group.

Extracorporeal membrane oxygenation technology—including materials and surgical techniques—has improved markedly in the last decade. Venoarterial cannulation is currently the preferred mode of ECMO support at our institution. Femoral cannulation has the advantage of easy institution at the bedside in the ICU, avoiding transport to the operating theater. Femoral cannulation may provide particular advantages after single-lung transplantation, especially after left single-lung transplantation, because it obviates the need for sternotomy, which is required for central cannulation. However, femoral cannulation has some potential disadvantages. The smaller size of the femoral vessels may lead to vascular complications in the lower limb, also the likelihood exists of the lower half of the body receiving well-oxygenated blood supply while the upper half of the body receives the poorly oxygenated blood leaving the lungs [10]. In such cases we also cannulate the distal femoral artery to perfuse the distal lower limb, to prevent lower limb complications. However, in our study, low radial-arterial PaO2 (less than 90 mm Hg) was seen in 1 patient even 12 hours after femoral venoarterial ECMO initiation; the patient died of MOF. This case encouraged us to use the central cannulation in the 2 most recent cases to avoid this problem. Central cannulation might be suitable after bilateral single-lung transplantation, especially for a smaller recipient.

Bleeding during ECMO support is often difficult to control; however, the use of a heparin-bonded hollow-fiber membrane oxygenator enabled us to reduce the amount of heparin administered. The activated clotting time in the recent group was significantly shorter than that of the early group (p = 0.04). Although the incidence of bleeding decreased from 50% (2/4) in the early group to 32% (2/6) in the recent group, the 4 patients with bleeding still had fatal outcomes.

Plasma leakage from the oxygenator is one of the disadvantages of the older type of hollow-fiber oxygenators [7]. Nevertheless, although 4 patients had plasma leakage requiring oxygenator changeover, 3 of the 4 were successfully weaned from ECMO. Plasma leakage itself seemed not to increase the mortality rate and we believe this complication is avoidable by using the new solid-type hollow-fiber membrane oxygenator (Quadrox).

In the early group, 3 of 4 patients died of MOF; 2 of the 3 had not been satisfactorily oxygenated systemically, as detected by radial-arterial blood gas analysis (PaO2 < 70 mm Hg) even 12 hours after ECMO initiation. In contrast, 5 of 6 patients in the recent group were oxygenated satisfactorily (PaO2 < 90 mm Hg). Therefore in the recent group ECMO seemed to provide more even systemic oxygenation than the early group. Possible explanations for the poor oxygenation in the early group include the following: (1) For peripheral venovenous ECMO, reverse gas exchange may have occurred in the transplanted lungs or oxygenated blood may have been recirculated by the high-flow ECMO circuit. (2) For peripheral venoarterial ECMO, the radial artery may have been supplied with deoxygenated blood from the heart when the patient had sufficient cardiac output to overcome ECMO flow, leading to an oxygenation discrepancy between the upper and the lower half of the body.

Although 3 of 6 patients in the recent group died during ECMO support, ECMO succeeded in stabilizing 2 of the 3 patients during support. One of those 2 patients was withdrawn from satisfactory ECMO due to hypoxic brain death that might have been caused by resuscitation efforts before ECMO initiation.

Due to small numbers in our series, we have not been able to identify significant predictors of outcomes; however, recent progress in ECMO technology seemed to lead to better cardiopulmonary temporary support with a lesser incidence of fatal complications and better outcomes in the more contemporary phase of our experience. Recently these results have encouraged us to use ECMO for various indications. Extracorporeal membrane oxygenation has been used after lung transplantation in 12 cases, after heart transplantation in 8 cases, after pulmonary failure (not transplant) in 20 cases, and after cardiac failure (not transplant) in 11 cases; 53% of the total were successful. The average number of ECMOs in the decade before 2000 was 2.3 per year, whereas the actual number of ECMOs in 2002 was 9 and in 2003 was 10. Use of ECMO in our institution has been increasing during the last 4 years. In our institution ECMO technology is readily available as a feature of our program of heart transplantation and mechanical circulatory support. We believe the increased use of ECMO is cost effective.


   Conclusion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Conclusion
Acknowledgments
 References
 
We conclude that ECMO as a therapeutic strategy has improved with the development of new ECMO technology, and has provided better results in our recent experience compared with earlier attempts. Extracorporeal membrane oxygenation remains the only potentially lifesaving therapy for LTx patients with PGF, who would otherwise die. However, because prolonged ECMO therapy is demanding in terms of resource consumption and personnel requirement, use of ECMO must be selective. Early PGF that occurs within 2 days after LTx is a reasonable indication. Multiple factors contribute to the outcome, and more precise identification of predictors of survival is needed.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Conclusion
 Acknowledgments
References
 
Doctor Oto was a recipient of scholarship established by the Association of Thoracic and Cardiovascular Surgeons of Asia. The authors appreciate the technical assistance provided by the transplant team at The Alfred Hospital.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Conclusion
 Acknowledgments
 References
 

  1. Lee CJ. Intensive cardiopulmonary support for otherwise dying post-heart and lung transplant recipients with extracorporeal membrane oxygenation. Artif Organs. 2001;25:597–598[Medline]
  2. Kirshbom PM, Bridges ND, Myung RJ, Gaynor JW, Clark BJ, Spray TL. Use of extracorporeal membrane oxygenation in pediatric thoracic organ transplantation. J Thorac Cardiovasc Surg. 2002;123:130–136[Abstract/Free Full Text]
  3. Meyers BF, Sundt TM III, Henry S, et al. Selective use of extracorporeal membrane oxygenation is warranted after lung transplantation. J Thorac Cardiovasc Surg. 2000;120:20–28[Abstract/Free Full Text]
  4. Nguyen DQ, Kulick DM, Bolman RM III, Dunitz JM, Hertz MI, Park SJ. Temporary ECMO support following lung and heart-lung transplantation. J Heart Lung Transplant. 2000;19:313–316[Medline]
  5. Glassman LR, Keenan RJ, Fabrizio MC, et al. Extracorporeal membrane oxygenation as an adjunct treatment for primary graft failure in adult lung transplant recipients. J Thorac Cardiovasc Surg. 1995;110:723–727[Abstract/Free Full Text]
  6. Christie JD, Bavaria JE, Palevsky HI, et al. Primary graft failure following lung transplantation. Chest. 1998;114:51–60[Abstract/Free Full Text]
  7. Peek GJ, Killer HM, Reeves R, Sosnowski AW, Firmin RK. Early experience with a polymethyl pentene oxygenator for adult extracorporeal life support. ASAIO J. 2002;48:480–482[Medline]
  8. Snell GI, Rabinov M, Griffiths A, et al. Pulmonary allograft ischemic time: an important predictor of survival after lung transplantation. J Heart Lung Transplant. 1996;15:160–168[Medline]
  9. Zenati M, Pham SM, Keenan RJ, Griffith BP. Extracorporeal membrane oxygenation for lung transplant recipients with primary severe donor lung dysfunction. Transpl Int. 1996;9:227–230[Medline]
  10. Sekela ME, Noon GP, Holland VA, Lawrence EC. Differential perfusion: potential complication of femoral-femoral bypass during single lung transplantation. J Heart Lung Transplant. 1991;10:322–324[Medline]



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