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Ann Thorac Surg 2004;78:1644-1649
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Extracorporeal Membrane Oxygenation is Superior to Right Ventricular Assist Device for Acute Right Ventricular Failure After Heart Transplantation

Shahrokh Taghavi, MDa,*, Andreas Zuckermann, MDa, Jan Ankersmit, MDa, Georg Wieselthaler, MDa, Angela Rajek, MDb, Günther Laufer, MDa, Ernst Wolner, MDa, Michael Grimm, MDa

a Department of Cardiothoracic Surgery, University of Vienna, Vienna, Austria
b Department of Cardiothoracic Anesthesiology, University of Vienna, Vienna, Austria

Accepted for publication April 20, 2004.

* Address reprint requests to Dr Taghavi, Department of Cardiothoracic Surgery, University of Vienna, Währinger Gürtel 18-20, A-1090 Vienna, Austria
taghavis{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Acute right ventricular failure after heart transplantation is a life-threatening condition, and sometimes the use of mechanical circulatory support is inevitable. The aim of this retrospective study was to investigate the effectiveness of two different mechanical circulatory support systems for this indication.

METHODS: From 1984 to 2003, 28 heart transplant recipients exhibited right ventricular failure resistant to drug therapy. Right ventricular assist device (n = 15) or extracorporeal membrane oxygenation (n = 13) was implanted to support the failing heart.

RESULTS: Overall in-hospital survival was 43%. In the right ventricular assist device group, only 2 patients (13%) could be weaned from mechanical circulatory support compared with 10 patients (77%) in the extracorporeal membrane oxygenation group (p = 0.001). Retransplantation was necessary in 6 patients in the right ventricular assist device group and in 1 patient in the extracorporeal membrane oxygenation group (p = 0.049). There was no difference in patient survival between groups, but graft survival was significantly better in the extracorporeal membrane oxygenation group (p = 0.005).

CONCLUSIONS: In view of these results, extracorporeal membrane oxygenation seems to be the better option as mechanical circulatory support for right ventricular failure in heart transplantation.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Heart transplantation is an established treatment for end-stage chronic heart failure [1]. Early postoperative results can be complicated by several factors, which are related to recipient, donor, or the surgical procedure [2, 3]. Preoperatively established severe pulmonary hypertension can result in right ventricular failure (RVF) at transplantation because of a very high afterload presented abruptly to the donor heart [4]. Ischemia and reperfusion injury associated with graft preservation may impair the ventricular contractility during the transplantation procedure [5–7]. These factors may lead to RVF, a condition associated with increased morbidity and mortality early after heart transplantation [8].

Effective treatment for RVF remains very challenging. Numerous therapeutic options have been suggested, including fluid management, high inspired oxygen concentrations, inotropic support and various vasodilators.

In some cases, aggressive drug treatment alone does not enable the surgeon to wean patients with RVF from cardiopulmonary bypass during the transplantation procedure, and therefore mechanical circulatory support or acute retransplantation is the only choice to overcome this life-threatening situation. Scarcity of donor hearts, long waiting lists, and high mortality on the waiting list result in an ethical dilemma to decide whether to perform retransplantation [9]. Results of acute heart retransplantation are poor: Radovancevic and colleagues [10] worked up the results of acute retransplantation from 42 heart transplant centers and suggested that emergency retransplantation should be avoided. On the other hand, results of implanting a right ventricular assist device (RVAD) for RVF after heart transplantation are very poor, with an in-hospital mortality of 73% to 100% [11–15].

Extracorporeal membrane oxygenation (ECMO) has recently been successfully used at our institution in patients with pulmonary hypertension undergoing bilateral lung transplantation and provided better initial organ function [16]. We therefore recently embarked on using peripheral venoarterial ECMO in heart transplant recipients with RVF [17].

The aim of this study was to analyze retrospectively the use of either RVAD or ECMO to treat RVF in heart transplantation.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patients
From April 1984 through December 2003, 963 patients underwent heart transplantation at our institution. Immunosuppression consisted of a triple-drug regimen (cyclosporine/tacrolimus, azathioprine/mycophenolate mofetil, and steroids) and induction therapy with rabbit-antithymocyte globuline. Twenty-eight patients (2.9%) exhibited RVF, which was defined as dilatation and hypocontractility of the right ventricle observed in the surgical field and on echocardiography at the time of weaning from cardiopulmonary bypass. It was characterized by increased mean pulmonary artery pressure (>50 mm Hg), decreased mean arterial pressure (<40 mm Hg), increased central venous pressure (>20 mm Hg), and decreased mixed venous oxygen saturation. It was not possible to wean these patients from cardiopulmonary bypass despite long reperfusion time and a maximum of drug therapy (isoproterenol, norepinephrine, milrinone, prostaglandin E1, and—since 2000—inhaled nitric oxide) [18]. These patients were considered likely to die without mechanical circulatory support. Between 1984 and 2000, 15 patients with RVF refractory to drug treatment received an RVAD. Another 13 patients with RVF were treated with ECMO between 2000 and 2003.

Right Ventricular Assist Device and Extracorporeal Membrane Oxygenation Characteristics and Technique
Our RVAD consisted of a Medtronic Bio-Medicus circuit (Medtronic Biomedical, Minneapolis, MN) with a centrifugal pump. The arterial cannula was placed close to the right atrial appendage. The pulmonary arterial cannula was connected through a polyethylene terephthalate fiber (Dacron) graft to the pulmonary artery. The sternum was closed after starting extracorporeal circulation if the patients were hemodynamically stable. Patients were anticoagulated with heparin (initial dosage 500 U/h i.v.), which was monitored by activated clotting time (target range, 160 to 200 seconds).

Our ECMO adult circuit consisted of a Medtronic console 450 or 550 and a Medtronic Biocal blood temperature control module (Medtronic Biomedical). The oxygenator was a hollow-fiber membrane oxygenator with an integrated heat exchanger. The cannulas were Medtronic Bio-Medicus cannulas, which are heparin coated, radiopaque, and wound with wire to prevent kinking. The setup of ECMO involved cut-down cannulation of the femoral vein and artery. Drainage was accomplished from the right atrium through the femoral vein, and the oxygenated blood was reinfused through the femoral artery. The distal femoral artery was perfused through an additional cannula. Anticoagulation was the same as in the RVAD group.

Weaning Procedure
Patients were evaluated daily for hemodynamic improvement and the possibility of weaning from the circulatory support. Patients received 10,000 U of heparin intravenously, and the flow rate was reduced stepwise in steps of 1 L/min while the hemodynamic variables were observed and the left and right ventricular function was assessed by transesophageal echocardiography. Inotropic and vasodilator support was increased on demand. Acceptable central venous pressure (<15 mm Hg) and mean arterial pressure (>60 mm Hg) and stable left and right ventricular function for a period of 4 to 6 hours with the reduced device flow demonstrated the improvement of cardiac function and represented an indication for removal of the device. Right ventricular assist device patients were taken to the operating room and the device was explanted after resternotomy. The removal of ECMO was completed on the intensive care unit in a bedside fashion.

Statistical Analysis
Continuous variables are expressed as mean ± standard deviation, and means were compared by independent sample Student's t test. Nominal variables are expressed as percentages and were analyzed by the {chi}2 test. Actuarial patient and graft survival was calculated by Kaplan-Meier analysis and compared by the log-rank test. Statistical significance was assumed at a p value of less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Except for sex (there were 3 female recipients in the ECMO group versus none in the RVAD group), groups were comparable with respect to demographic data, indication for transplantation, preoperative hemodynamic variables, donor age, donor-to-recipient size match, total ischemic time, and reperfusion time, which are summarized in Table 1. Table 2 summarizes hemodynamic variables immediately before implantation of the device and during circulatory support.


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  		Table 1. Demographic Data, Preoperative Hemodynamic Variables, and Donor Characteristicsa

 

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  		Table 2. Hemodynamic Variables Immediately Before Device Implantation and During Circulatory Supporta

 
Kaplan-Meier analysis showed that cumulative in-hospital survival of patients with RVF that required mechanical circulatory support (ie, both groups) was 43% (Fig 1). In the RVAD group (n = 15), only 2 patients (13%) could be weaned from the assist device. Of the 13 patients who could not be weaned from RVAD, 7 died while on RVAD as a result of sepsis (n = 3) or multiorgan failure (n = 4); the remaining 6 patients underwent retransplantation because of irreversible impairment of cardiac function. Two of these patients died 14 and 16 days after retransplantation; the remaining 4 patients were discharged from the hospital.



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  		Fig 1. Kaplan-Meier analysis of overall survival of heart transplant recipients who required mechanical circulatory support (right ventricular assist device and extracorporeal membrane oxygenation) for right ventricular failure. Numbers in brackets represent patients at risk.

 
In the ECMO group (n = 13), 1 patient underwent retransplantation while on ECMO 1 day after the initial transplantation procedure and died immediately after retransplantation. Two other patients died while on ECMO because of further deterioration of cardiac performance, 1 and 12 days after transplantation. Ten patients (77%) showed improvement of right ventricular function after a duration of 60.5 ± 40.7 hours (median, 49 hours) on mechanical circulatory support. Therefore, stepwise reduction of ECMO flow rate under stable cardiac and hemodynamic conditions was possible, and these patients were successfully weaned from ECMO. However, 3 of these patients died in the intensive care unit as a result of sepsis at 9, 12, and 18 days after successful termination of circulatory support. The outcome of mechanical circulatory support in all patients is summarized in Table 3.


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  		Table 3. Outcome of Mechanical Circulatory Support for Right Ventricular Failure in Heart Transplant Recipientsa

 
Although there was no difference in patient survival between the RVAD and ECMO groups (p = 0.261 by log-rank analysis), graft survival was significantly better in the ECMO group (p = 0.005 by log-rank analysis; Fig 2). Furthermore, a larger proportion of patients in the ECMO group could be weaned from mechanical circulatory support (77% versus 13%; p = 0.001 by the {chi}2 test). A smaller proportion of patients in the ECMO group underwent retransplantation (7% versus 40% in the RVAD group), and this difference was statistically significant (p = 0.049 by the {chi}2 test). The duration of circulatory support was shorter in the ECMO group (p = 0.056 by independent sample Student's t test), and in this group a smaller proportion of patients died while on circulatory support (p = 0.077 by the {chi}2 test).



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  		Fig 2. Kaplan-Meier analysis of graft survival in heart transplant recipients who required mechanical circulatory support (either right ventricular assist device [RVAD] or extracorporeal membrane oxygenation [ECMO]) for right ventricular failure. Numbers in brackets represent patients at risk. (p = 0.005 by log-rank analysis.)

 
A large number of complications were seen in both patient groups; they are summarized in Table 4. Except for device-related complications, which were seen more frequently in the ECMO group (p = 0.097 by the {chi}2 test), the incidence of complications was comparable between groups. Furthermore, patients in the RVAD group required more blood units intraoperatively and during device support than patients in the ECMO group (15.7 ± 5.5 versus 5.4 ± 2.6; p < 0.01 by independent sample Student's t test). This ratio was the same if patients who had undergone heart surgery before transplantation were compared (n = 5 in the RVAD and n = 6 in the ECMO groups, respectively).


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  		Table 4. Incidence of Complications Associated With Mechanical Circulatory Support for Right Ventricular Failure in Heart Transplant Recipientsa

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Heart transplantation has evolved to be the best treatment option for patients with advanced heart failure that remains refractory to medical therapy. In the clinical setting, RVF eventually results in 50% of all cardiac complications and 19% of all early deaths after this procedure [19–22]. Right ventricular failure is of multifactorial origin; preexisting increased pulmonary vascular resistance and ischemia-reperfusion injury of the myocardium associated with graft preservation are two of the main causes [5].

Effective treatment for RVF remains very challenging, and numerous therapeutic options have been suggested. The goal in the treatment of RVF is to dilate pulmonary vessels and reduce pulmonary vascular resistance while maintaining systemic blood pressure and increased ventricular contractility. Prostaglandin E1, milrinone, and nitric oxide have been shown to be potent but nonselective pulmonary vasodilators with the potential to reduce pulmonary afterload. A reduction of pulmonary vascular resistance may improve ventricular performance and prevent RVF. Furthermore, inotropic drugs are routinely given to increase ventricular contractility and heart rate and thus improve oxygen delivery.

At our institution, the administration of isoproterenol, prostaglandin E1, and inhaled nitric oxide are now mainstays of the initial treatment of RVF. Isoproterenol is usually started during the reperfusion of the allograft, and inhaled nitric oxide or prostaglandin E1 are given before weaning from cardiopulmonary bypass. Other inotropic drugs and milrinone are optional and are used in cases in which initial therapy has had little impact [18].

Despite maximal pharmacologic treatment, some patients cannot be weaned from cardiopulmonary bypass. In this situation, the use of mechanical circulatory support is inevitable. The goal of mechanical circulatory support for RVF is to provide adequate support of the transplanted heart, allowing time for recovery and eventually normal graft function.

Various types of mechanical circulatory support have been used, of which RVAD seems to have the most widespread use. In the literature, results of RVAD are poor [11]. Noon and associates [12] reported the use of RVAD in 17 patients with cardiac allograft failure after heart transplantation with a mortality of 85%. The same group published the use of RVAD in 7 patients with a hospital mortality of 100% [13]. Minev and colleagues [14] published the results of implanting a Bio-Medicus centrifugal pump for refractory RVF with an overall mortality of 84%. Our present results with RVAD for RVF in heart transplantation are similar to those published by other groups: RVAD support did rarely enable recovery of graft function, and most patients either died on RVAD or had to undergo retransplantation.

Other types of mechanical circulatory support than RVAD have been reported anecdotally. Intraaortic balloon pump has been used for RVF and was suggested to improve ventricular contractility [23]. Arpesella and coworkers [24] reported the use of extracorporeal right-to-left atrial bypass, which was implanted intrathoracically and led to recovery of RVF.

Extracorporeal membrane oxygenation has been used in isolated cases in heart transplantation [25, 26]. Motivated also by the successful utilization of ECMO at our institution in lung transplant recipients, in whom it has improved the early outcome [17], we started using venoarterial ECMO routinely in heart transplant recipients with RVF [27].

Extracorporeal membrane oxygenation provides a means of supporting the function of organ systems in these patients during a critical period and allows the freshly transplanted heart to work under less stressful conditions and eventually recover from the combined shock caused by ischemia-reperfusion injury and exposure to a previously unknown preload.

In our experience, a larger proportion of patients could be weaned from ECMO, and graft survival in the ECMO group was significantly better compared with the RVAD group. Overall patient survival was comparable between groups, but the fact that 6 patients in the RVAD group underwent retransplantation (of which 4 were discharged from the hospital) certainly influenced this result. In the ECMO group, a smaller proportion of patients had to undergo retransplantation.

The duration of circulatory support was shorter in the ECMO group than in the RVAD group, and it is probably because of the small number of subjects that this difference is not significant (p = 0.056). The shorter time on circulatory support was certainly beneficial in terms of avoiding complications, and may account for the trend for fewer deaths while on circulatory support in the ECMO group. A shorter duration of circulatory support in the ECMO group might also be explained by less severe forms of RVF in patients in this group or by better pharmacologic management of RVF in recent years. Furthermore, because of the relatively minimal invasiveness of the procedure of installing ECMO, the threshold at which the decision was taken to use circulatory support might have been lower in these patients.

Although there was a trend for more device-related complications in the ECMO group, they were easy to cope with (change of oxygenator). On the other hand, the fact that the frequency of bleeding complications was comparable between groups was surprising. However, the single case of resternotomy in the ECMO group cannot be attributed to use of this device, whereas the four cases of resternotomy in the RVAD patients may easily be related to the greater invasiveness of this type of mechanical circulatory support owing to the central cannulation required.

In our experience, during mechanical circulatory support special attention has to be given to the following points. First, infection is a major risk factor for poor outcome in these patients and was the main cause of mortality in patients from the ECMO group who died after successful weaning. This warrants aggressive prophylactic antibiotic and antimycotic therapy. Second, the heart has been doing less stroke work during the period of mechanical circulatory support as a result of diversion of the blood from the right atrium into the venous cannula of the device. Thus, during the period of weaning from support, sufficient time must be allowed to permit the right ventricle to adapt to the changing preload and stroke work imposed on it by receiving progressively more systemic venous return.

Our study is limited by several factors: it is a retrospective, single-center analysis of two consecutive groups treated more than 19 years, lacking any form of randomization; the management protocols and drug treatments have evolved and were improved during the time of the study. Inhaled nitric oxide has been routinely used for the treatment of RVF at our institution since 2000, and thus only the patients in the ECMO group have received this treatment. Whether this has had an impact on our results remains subject to speculation. Overall, there was no difference in recipient characteristics between patients who experienced RVF and patients who did not experience RVF during each period. However, in the early period, recipients and donors may have been in better condition (n = 15 patients who needed RVAD between 1984 to 2000). In recent years recipients receive more aggressive drug treatments from cardiologists for a longer period before enrollment on the heart transplantation waiting list [28]. Furthermore, sometimes hearts of marginal quality may be accepted owing to the scarcity of donor organs and the ever-increasing gap between the number of available organs and the number of patients on the waiting list [29]. These facts might explain the higher incidence of RVF requiring mechanical circulatory support in the last 3 years (n = 13 patients requiring ECMO between 2000 and 2003).

In summary, we suggest that the use of ECMO should be favored over RVAD for mechanical circulatory support of RVF in heart transplantation. In our hands, the former allowed more patients to be weaned from mechanical circulatory support and resulted in better graft survival, thus helping us to make better use of scarce donor hearts.


   References
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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