New horizons of non-emergent use of extracorporeal membranous oxygenator support
Review Article

New horizons of non-emergent use of extracorporeal membranous oxygenator support

George Makdisi1, Peter B. Makdisi2, I-Wen Wang3

1Gulf Coast Cardiothoracic Surgery Institute, Tampa General Hospital, Tampa, FL, USA; 2Mayo Clinic College of Medicine, Rochester, MN, USA; 3Indiana University School of Medicine, Division of Cardiothoracic Surgery, Indiana University Health, Methodist Hospital, Indianapolis, IN, USA

Contributions: (I) Conception and design: All authors; (II) Administrative support: None; (III) Provision of study materials or patients: All authors; (IV) Collection and assembly of data: All authors; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: I-Wen Wang, MD, PhD. Indiana University School of Medicine, Division of Cardiothoracic Surgery, Indiana University Health, Methodist Hospital, Indianapolis, IN 46202, USA. Email: IWang@iuhealth.org.

Abstract: The expansion of the extra corporeal membrane oxygenation (ECMO) use and its indication is strikingly increased in the past few years. ECMO use expanded to lung transplantation, difficult general thoracic resections, transcatheter aortic valve replacement (TAVR) and LVAD implantation. Here we will discuss the indications and the outcomes of non-emergent use of ECMO.

Keywords: Extra corporeal membrane oxygenation (ECMO); transcatheter aortic valve replacement (TAVR); TAVI; LVAD; lung transplant


Submitted Dec 23, 2015. Accepted for publication Jan 11, 2016.

doi: 10.3978/j.issn.2305-5839.2016.02.04


Introduction

Indications extra corporeal membrane oxygenation (ECMO) and its usage have rapidly expanded over the last 20 years; it has usually been applied in rescue situations and has become essential tool in the care of patients with severe cardiac and/or pulmonary dysfunction refractory to conventional management (1). These indications have been extended to more prolonged use in intensive care unit (ICU), bridge to cardiac and lung transplant. Venoarterial ECMO (VA ECMO) can also be used to stabilize the patient in emergency situations (1-5), however, it can also be used emergently or complications and as prophylaxis in very high risk patients undergoing transcatheter aortic valve replacement (TAVR) (6-8), LVAD implantation (9), and also used as support for lung resections in unstable patients (10,11). Several centers have now replaced conventional cardiopulmonary bypass (CPB) by ECMO for patients with respiratory and/or cardiac failure during transplantation (12-14). Here we will be discussing all possible usages of ECMO other than emergent use for respiratory tor cardiac failure.


Extra corporeal membrane oxygenation (ECMO) vs. cardiopulmonary bypass (CPB)

CPB is associated with undesirable effects well documented in the literature, including activation of inflammatory mediators, increased pulmonary vascular resistance, platelet activation, coagulopathy and impaired renal function (15-18).

In theory, the advantages of ECMO concept is a relatively miniaturized circuit that has lower priming volumes and the absence of both air-blood contact and cardiotomy suction. This leads to lesser anticoagulation requirement, potentially lesser coagulopathy, and attenuated systemic inflammatory response (19-22). The use of a miniaturized CPB circuit in cardiac surgery procedures has been shown to be associated with lower transfusion requirement, a reduction in peak troponin, and a lower incidence of neurologic injury in comparison with conventional CPB (20,23). Miniaturized circuits have been shown to have decreased inflammatory response, less hemodilution, less need for inotropic support, lower peak creatinine level, and a lower incidence of atrial fibrillation. These advantages were reflected in a decreases requirement for mechanical ventilation, shorter ICU and hospital stay, and ultimately decreased hospital mortality (9). In cases of major vessel injury or severe bleeding, conventional CPB with a venous reservoir allows safe cardiopulmonary support. Conventional CPB remains essential when opening the cardiac cavities and during surgery of the aortic arch or the lung artery trunk.


Using extra corporeal membrane oxygenation (ECMO) with TAVR

TAVR has emerged as a less-invasive alternative in high-risk patients with severe aortic valve stenosis. TAVR is a complex procedure and is often associated with complications that may result in hemodynamic instability. Recent published data reported the use of CPB ranging from 1.2% to 6% of TAVR cases (6-8).

Intraoperative emergent use of CPB is an effective strategy to rescue patients from myocardial collapse as a consequence of the most severe TAVR complications which allows time to perform a thorough diagnostic evaluation and facilitate a safe definitive treatment of the complication (7). These complications include severe paravalvular leak in patients with depressed left ventricular function, severe diastolic dysfunction, or significant mitral regurgitation. The ability of these patients to compensate for acute severe aortic insufficiency may be compromised (6,8,24). The use of CPB allows time for a full assessment of the leak and either reballooning of the prosthesis or preparation of a second device for valve-in-valve treatment, CPB also can be used in cases of coronary malperfusion, or severe bleeding at the apex of the left ventricle which allows decompression of the ventricle to facilitate a safe primary repair.

ECMO could replace CBP in both conditions as prophylaxis in very high risk patients undergoing TAVR insertion, used to stabilize patients in cases of hemodynamic instability with, or without ischemic changes. While there currently no data on systemic use of VA ECMO as prophylactic support, there are some reports which support this concept, as this strategy might potentially minimize the effects of procedural complications in these high risk patients (6,7,24,25).

Emergency implantation of VA ECMO for circulatory support appears to be safe and feasible to stabilize the patient for further treatment (6), in the sitting of severely impaired left ventricular function, slow recovery from rapid left ventricular pacing during testing of pacemaker, high vasopressor requirement during general anesthesia or concomitant high risk PCI might warrant the use of this prophylactic strategy (6). Banjac et al. (8) reported using ECMO in 10 patients (4.3% of all TAVR cases) as an emergent rescue strategy after TAVR complications with improved outcomes.


Using extra corporeal membrane oxygenation (ECMO) with LVAD implantation

Ventricular assist devices (VADs) implantation is typically performed with the use of CPB. The patient population that requires VAD implantation often has evidence of end-organ dysfunction, including hepatic congestion, renal insufficiency and pulmonary edema. VAD placement under CPB often exacerbates pre-existing conditions, resulting in post-operative coagulopathy, bleeding and worsening right heart failure. VAD implantation without the use of CPB could help to minimize these post-operative complications without hemodynamic compromise, or excessive bleeding during implantation (26,27). By minimizing the needs for blood transfusions, patients have decreased exposure to blood antigens which ultimately reduces the risk of sensitization in transplant candidates (28).

Anastasiadis et al. (9) has reported successful insertion of Jarvik 2000 device by using ECMO in spite of CPB for cardiac support during the procedure. This technique was associated with decreased duration of operation, reduction in blood transfusion, less inotropic support, shorter duration of mechanical ventilation, and length of hospital stay.

ECMO is also used as a bridge to LVAD insertion in patients with profound cardiogenic shock; bridging allows time for end-organ recovery from cardiogenic shock, thereby reducing the mortality rate in this critically ill group of patients (29-31). ECMO support also allows more time for adequate assessment of patients, and thus assists in choosing a management pathway (29). Haneya et al. (32) reported series of 6 patients with profound cardiogenic shock; provided on an emergency basis with a percutaneous ECMO via the peripheral vessels. After stabilization, LVAD was implanted using ECMO without switching to a conventional CPB system. These patients were compared with another 11 patients in whom the LVAD was placed with the aid of an additional CPB system. They demonstrated that the blood loss and blood product transfusions were lower in patients operated using ECMO. And the subsequent need for mechanical ventilation and inotropic support was shorter and the survival rate was higher when compared with patients who were operated using CPB.

ECMO has also been used to temporarily support for right ventricular failure in patients with recently inserted LVAD (31-34).


Using extra corporeal membrane oxygenation (ECMO) for thoracic surgery support

The first case of non-cardiac surgical application of CPB was reported by Woods et al. in 1961 (35) for resection of the carina and both main stem bronchi for a bronchial adenoma. Since then conventional CPB has been used for intraoperative respiratory support during lung resections of tumors invading the great vessels and/or the left atrium where both respiratory and circulatory support are needed. CBP use is also needed when one-lung ventilation is impossible like single lung or hypoxemia after lung exclusion where respiratory reserve is insufficient (36), or in large mediastinal tumors invading the great vessels, compromising the heart and trachea (37).

Little has been reported in the literature about using ECMO support during general thoracic procedures. Horita reported using venovenous ECMO (VV ECMO) for 2 cases of carina and sleeve lobectomy in 1996 (10). Several cases have been reported using ECMO for carinal resection-reconstruction (11,38), segmentectomy for cancer in a patient with single lung (39). Limited resection of the lung (wedge or segmentectomy) for aspergillosis or lung abscess was performed under one-lung ventilation thanks to ECMO (40,41), mediastinal tumor resection, due to compression of the trachea (42). VV ECMO was also used for emphysematous bulla resection in single lung by video assisted thoracoscopy (VATS) (43). Peripheral VA ECMO was used as well for cases of lung volume reduction surgery for severe pulmonary emphysema (44), trauma conditions including tracheo-bronchial plasty for traumatic break (45,46), iatrogenic tracheal necrosis after radiation, traumatic intubations, during carinal injury during esophageal resection, or stentings (36) in a postoperative setting. ECMO has been demonstrated to improve survival in patients with post-pneumonectomy ARDS (47). Rinieri et al. (36) reported French experience with using ECMO for thoracic surgery procedures as an alternative to conventional CPB. ECMO allowed median duration interruption of ventilation of 78 and 65 min with VV ECMO and VA ECMO respectively. They also reported over 3 h of apnea duration.

In summary, ECMO can be an alternative to CPB in complex ventilatory situations, for major tracheo-bronchial surgery and single-lung procedures without in-field ventilation. Intraoperative ECMO can ensure good hemostasis and allows better surgical exposure than mechanical ventilation. The choice of ECMO type (VV vs. VA) depends on the relative need for circulatory support and pulmonary support, as well as the degree of urgency. The site of cannulation also depends on surgical access utilized (sternotomy vs. thoracotomy); the cannulation could be central cannulation when sternotomy is used and peripheral when thoracotomy is used.


Using extra corporeal membrane oxygenation (ECMO) in Lung transplantation

CPB historically is the most used modality for intraoperative cardiorespiratory support during lung transplantation (48). The use of CPB can lead to coagulopathy, increased blood product transfusions; complement activation, activation of the systemic inflammatory response syndrome which ultimately leads to endorgan injury (49). Early graft dysfunction in clinical lung transplantation is well described in association with lung transplant supported by CPB (50-55). The use of CPB was cited as an independent factor associated with primary graft dysfunction (56). ECMO might present as an alternative to CPB. The benefits of preoperative ECMO support as a bridge to transplantation (57,58) and the positive impact of ECMO support on outcomes following graft failure after lung transplantation is well documented (50,55,59,60).

Ius et al. (61) in retrospective study, reported using intraoperative ECMO in 46 patients who underwent lung transplantation, and compared to 46 patients who underwent lung transplantation with the use of CBP, and concluded that the patients with ECMO support lung needed less requirement for mechanical ventilation, had shortened ICU and hospital length of stay, and required less blood product transfusions during the perioperative period when compared with matched recipients who were supported with conventional CPB. Patients who underwent CPB support had higher requirements for dialysis and had a higher in hospital mortality (39% vs. 13%). No differences were found with regard to time on mechanical ventilation and ICU stay. They concluded that ECMO may be considered to be the preferred choice for intraoperative cardiopulmonary support for lung transplant. Conventional CPB will certainly remain an essential support tool for patients undergoing lung transplant and concomitant cardiac repair procedures, cases of complex atrial anastomosis requiring heart arrest, and in emergency situations such as massive intraoperative bleeding (62).


Summary

In the contemporary practice of cardiothoracic surgery, ECMO is emerging as a powerful tool in non-emergent applications, such as for lung transplant, TAVR, LVAD insertion, and general thoracic surgery resections. The successful clinical outcomes and improvement of minimized CPB support warrant further exploration of additional innovative applications as well as continue development of clinical experience. Future directions may provide improved patient outcome and reducing medical costs.


Acknowledgements

None.


Footnote

Conflicts of Interest: The authors have no conflicts of interest to declare.


References

  1. Makdisi G, Wang IW. Extra corporeal membrane oxygenation (ECMO) review of a lifesaving technology. J Thorac Dis 2015;7:E166-76. [PubMed]
  2. MacLaren G, Combes A, Bartlett RH. Contemporary extracorporeal membrane oxygenation for adult respiratory failure: life support in the new era. Intensive Care Med 2012;38:210-20. [PubMed]
  3. Peek GJ, Mugford M, Tiruvoipati R, et al. Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): a multicentre randomised controlled trial. Lancet 2009;374:1351-63. [PubMed]
  4. Cooper DS, Jacobs JP, Moore L, et al. Cardiac extracorporeal life support: state of the art in 2007. Cardiol Young 2007;17:104-15. [PubMed]
  5. Combes A, Leprince P, Luyt CE, et al. Outcomes and long-term quality-of-life of patients supported by extracorporeal membrane oxygenation for refractory cardiogenic shock. Crit Care Med 2008;36:1404-11. [PubMed]
  6. Husser O, Holzamer A, Philipp A, et al. Emergency and prophylactic use of miniaturized veno-arterial extracorporeal membrane oxygenation in transcatheter aortic valve implantation. Catheter Cardiovasc Interv 2013;82:E542-51. [PubMed]
  7. Roselli EE, Idrees J, Mick S, et al. Emergency use of cardiopulmonary bypass in complicated transcatheter aortic valve replacement: importance of a heart team approach. J Thorac Cardiovasc Surg 2014;148:1413-6. [PubMed]
  8. Banjac I, Petrovic M, Akay MH, et al. Extracorporeal membrane oxygenation as a procedural rescue strategy for transcatheter aortic valve replacement cardiac complications. ASAIO J 2016;62:e1-4. [PubMed]
  9. Anastasiadis K, Antonitsis P, Argiriadou H, et al. Use of minimal extracorporeal circulation circuit for left ventricular assist device implantation. ASAIO J 2011;57:547-9. [PubMed]
  10. Horita K, Itoh T, Furukawa K, et al. Carinal reconstruction under veno-venous bypass using a percutaneous cardiopulmonary bypass system. Thorac Cardiovasc Surg 1996;44:46-9. [PubMed]
  11. Lang G, Taghavi S, Aigner C, et al. Extracorporeal membrane oxygenation support for resection of locally advanced thoracic tumors. Ann Thorac Surg 2011;92:264-70. [PubMed]
  12. Bittner HB, Binner C, Lehmann S, et al. Replacing cardiopulmonary bypass with extracorporeal membrane oxygenation in lung transplantation operations. Eur J Cardiothorac Surg 2007;31:462-7; discussion 467. [PubMed]
  13. Gulack BC, Hirji SA, Hartwig MG. Bridge to lung transplantation and rescue post-transplant: the expanding role of extracorporeal membrane oxygenation. J Thorac Dis 2014;6:1070-9. [PubMed]
  14. Bermudez CA, Shiose A, Esper SA, et al. Outcomes of intraoperative venoarterial extracorporeal membrane oxygenation versus cardiopulmonary bypass during lung transplantation. Ann Thorac Surg 2014;98:1936-42; discussion 1942-3.
  15. Pintar T, Collard CD. The systemic inflammatory response to cardiopulmonary bypass. Anesthesiol Clin North America 2003;21:453-64. [PubMed]
  16. Clive Landis R, Murkin JM, Stump DA, et al. Consensus statement: minimal criteria for reporting the systemic inflammatory response to cardiopulmonary bypass. Heart Surg Forum 2010;13:E116-23. [PubMed]
  17. Momeni M, Carlier C, Baele P, et al. Fibrinogen concentration significantly decreases after on-pump versus off-pump coronary artery bypass surgery: a systematic point-of-care ROTEM analysis. J Cardiothorac Vasc Anesth 2013;27:5-11. [PubMed]
  18. Belhaj A. Actual knowledge of systemic inflammation reaction during cardiopulmonary bypass. Recent Pat Cardiovasc Drug Discov 2012;7:165-9. [PubMed]
  19. Vohra HA, Whistance R, Modi A, et al. The inflammatory response to miniaturised extracorporeal circulation: a review of the literature. Mediators Inflamm 2009;2009:707042.
  20. Merkle F, Haupt B, El-Essawi A, et al. State of the art in cardiovascular perfusion: now and in the next decade. HSR Proc Intensive Care Cardiovasc Anesth 2012;4:211-6. [PubMed]
  21. El-Essawi A, Hajek T, Skorpil J, et al. Are minimized perfusion circuits the better heart lung machines? Final results of a prospective randomized multicentre study. Perfusion 2011;26:470-8. [PubMed]
  22. Anastasiadis K, Antonitsis P, Haidich AB, et al. Use of minimal extracorporeal circulation improves outcome after heart surgery; a systematic review and meta-analysis of randomized controlled trials. Int J Cardiol 2013;164:158-69. [PubMed]
  23. Zangrillo A, Garozzo FA, Biondi-Zoccai G, et al. Miniaturized cardiopulmonary bypass improves short-term outcome in cardiac surgery: a meta-analysis of randomized controlled studies. J Thorac Cardiovasc Surg 2010;139:1162-9. [PubMed]
  24. Seco M, Forrest P, Jackson SA, et al. Extracorporeal membrane oxygenation for very high-risk transcatheter aortic valve implantation. Heart Lung Circ 2014;23:957-62. [PubMed]
  25. Spina R, Forrest AP, Adams MR, et al. Veno-arterial extracorporeal membrane oxygenation for high-risk cardiac catheterisation procedures. Heart Lung Circ 2010;19:736-41. [PubMed]
  26. Van Meter CH Jr, Robbins RJ, Ochsner JL. Technique of right heart protection and deairing during heartmate vented electric LVAD implantation. Ann Thorac Surg 1997;63:1191-2. [PubMed]
  27. Makdisi G, Wang IW. Minimally invasive is the future of left ventricular assist device implantation. J Thorac Dis 2015;7:E283-8. [PubMed]
  28. Maltais S, Davis ME, Haglund N. Minimally invasive and alternative approaches for long-term LVAD placement: the Vanderbilt strategy. Ann Cardiothorac Surg 2014;3:563-9. [PubMed]
  29. Marasco SF, Stornebrink RK, Murphy DA, et al. Long-term right ventricular support with a centrifugal ventricular assist device placed in the right atrium. J Card Surg 2014;29:839-42. [PubMed]
  30. Pagani FD, Lynch W, Swaniker F, et al. Extracorporeal life support to left ventricular assist device bridge to heart transplant: a strategy to optimize survival and resource utilization. Circulation 1999;100:II206-10. [PubMed]
  31. Scherer M, Moritz A, Martens S. The use of extracorporeal membrane oxygenation in patients with therapy refractory cardiogenic shock as a bridge to implantable left ventricular assist device and perioperative right heart support. J Artif Organs 2009;12:160-5. [PubMed]
  32. Haneya A, Philipp A, Diez C, et al. A 5-year experience with cardiopulmonary resuscitation using extracorporeal life support in non-postcardiotomy patients with cardiac arrest. Resuscitation 2012;83:1331-7. [PubMed]
  33. De Silva RJ, Soto C, Spratt P. Extra corporeal membrane oxygenation as right heart support following left ventricular assist device placement: a new cannulation technique. Heart Lung Circ 2012;21:218-20. [PubMed]
  34. Guenther S, Theiss HD, Fischer M, et al. Percutaneous extracorporeal life support for patients in therapy refractory cardiogenic shock: initial results of an interdisciplinary team. Interact Cardiovasc Thorac Surg 2014;18:283-91. [PubMed]
  35. Woods FM, Nepture WB, Palatchi A, et al. Resection of the carina and main-stem bronchi with the use of extracorporeal circulation. N Engl J Med 1961;264:492-4. [PubMed]
  36. Rinieri P, Peillon C, Bessou JP, et al. National review of use of extracorporeal membrane oxygenation as respiratory support in thoracic surgery excluding lung transplantation. Eur J Cardiothorac Surg 2015;47:87-94. [PubMed]
  37. Said SM, Telesz BJ, Makdisi G, et al. Awake cardiopulmonary bypass to prevent hemodynamic collapse and loss of airway in a severely symptomatic patient with a mediastinal mass. Ann Thorac Surg 2014;98:e87-90. [PubMed]
  38. Lei J, Su K, Li XF, et al. ECMO-assisted carinal resection and reconstruction after left pneumonectomy. J Cardiothorac Surg 2010;5:89. [PubMed]
  39. Spaggiari L, Rusca M, Carbognani P, et al. Segmentectomy on a single lung by femorofemoral cardiopulmonary bypass. Ann Thorac Surg 1997;64:1519. [PubMed]
  40. Souilamas R, Souilamas JI, Alkhamees K, et al. Extra corporal membrane oxygenation in general thoracic surgery: a new single veno-venous cannulation. J Cardiothorac Surg 2011;6:52. [PubMed]
  41. Brenner M, O'Connor JV, Scalea TM, et al. Use of ECMO for resection of post-traumatic ruptured lung abscess with empyema. Ann Thorac Surg 2010;90:2039-41. [PubMed]
  42. Felten ML, Michel-Cherqui M, Puyo P, et al. Extracorporeal membrane oxygenation use for mediastinal tumor resection. Ann Thorac Surg 2010;89:1012. [PubMed]
  43. Oey IF, Peek GJ, Firmin RK, et al. Post-pneumonectomy video-assisted thoracoscopic bullectomy using extra-corporeal membrane oxygenation. Eur J Cardiothorac Surg 2001;20:874-6. [PubMed]
  44. Tsunezuka Y, Sato H, Tsubota M, et al. Significance of percutaneous cardiopulmonary bypass support for volume reduction surgery with severe hypercapnia. Artif Organs 2000;24:70-3. [PubMed]
  45. Korvenoja P, Pitkänen O, Berg E, et al. Veno-venous extracorporeal membrane oxygenation in surgery for bronchial repair. Ann Thorac Surg 2008;86:1348-9. [PubMed]
  46. Voelckel W, Wenzel V, Rieger M, et al. Temporary extracorporeal membrane oxygenation in the treatment of acute traumatic lung injury. Can J Anaesth 1998;45:1097-102. [PubMed]
  47. Dünser M, Hasibeder W, Rieger M, et al. Successful therapy of severe pneumonia-associated ARDS after pneumonectomy with ECMO and steroids. Ann Thorac Surg 2004;78:335-7. [PubMed]
  48. Marczin N, Royston D, Yacoub M, et al. Pro: lung transplantation should be routinely performed with cardiopulmonary bypass. J Cardiothorac Vasc Anesth 2000;14:739-45. [PubMed]
  49. McRae K. Con: lung transplantation should not be routinely performed with cardiopulmonary bypass. J Cardiothorac Vasc Anesth 2000;14:746-50. [PubMed]
  50. Fuehner T, Kuehn C, Hadem J, et al. Extracorporeal membrane oxygenation in awake patients as bridge to lung transplantation. Am J Respir Crit Care Med 2012;185:763-8. [PubMed]
  51. Gammie JS, Cheul Lee J, Pham SM, et al. Cardiopulmonary bypass is associated with early allograft dysfunction but not death after double-lung transplantation. J Thorac Cardiovasc Surg 1998;115:990-7. [PubMed]
  52. Asimakopoulos G, Smith PL, Ratnatunga CP, et al. Lung injury and acute respiratory distress syndrome after cardiopulmonary bypass. Ann Thorac Surg 1999;68:1107-15. [PubMed]
  53. De Perrot M, Sekine Y, Fischer S, et al. Interleukin-8 release during early reperfusion predicts graft function in human lung transplantation. Am J Respir Crit Care Med 2002;165:211-5. [PubMed]
  54. Aeba R, Griffith BP, Kormos RL, et al. Effect of cardiopulmonary bypass on early graft dysfunction in clinical lung transplantation. Ann Thorac Surg 1994;57:715-22. [PubMed]
  55. Mason DP, Boffa DJ, Murthy SC, et al. Extended use of extracorporeal membrane oxygenation after lung transplantation. J Thorac Cardiovasc Surg 2006;132:954-60. [PubMed]
  56. Diamond JM, Lee JC, Kawut SM, et al. Clinical risk factors for primary graft dysfunction after lung transplantation. Am J Respir Crit Care Med 2013;187:527-34. [PubMed]
  57. Fischer S, Simon AR, Welte T, et al. Bridge to lung transplantation with the novel pumpless interventional lung assist device NovaLung. J Thorac Cardiovasc Surg 2006;131:719-23. [PubMed]
  58. Del Sorbo L, Ranieri VM, Keshavjee S. Extracorporeal membrane oxygenation as "bridge" to lung transplantation: what remains in order to make it standard of care? Am J Respir Crit Care Med 2012;185:699-701. [PubMed]
  59. Fischer S, Bohn D, Rycus P, et al. Extracorporeal membrane oxygenation for primary graft dysfunction after lung transplantation: analysis of the Extracorporeal Life Support Organization (ELSO) registry. J Heart Lung Transplant 2007;26:472-7. [PubMed]
  60. Oto T, Rosenfeldt F, Rowland M, et al. Extracorporeal membrane oxygenation after lung transplantation: evolving technique improves outcomes. Ann Thorac Surg 2004;78:1230-5. [PubMed]
  61. Ius F, Kuehn C, Tudorache I, et al. Lung transplantation on cardiopulmonary support: venoarterial extracorporeal membrane oxygenation outperformed cardiopulmonary bypass. J Thorac Cardiovasc Surg 2012;144:1510-6. [PubMed]
  62. Machuca TN, Collaud S, Mercier O, et al. Outcomes of intraoperative extracorporeal membrane oxygenation versus cardiopulmonary bypass for lung transplantation. J Thorac Cardiovasc Surg 2015;149:1152-7. [PubMed]
Cite this article as: Makdisi G, Makdisi PB, Wang IW. New horizons of non-emergent use of extracorporeal membranous oxygenator support. Ann Transl Med 2016;4(4):76. doi: 10.3978/j.issn.2305-5839.2016.02.04