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Right arrow Transplantation - heart

J Thorac Cardiovasc Surg 2008;135:1159-1166
© 2008 The American Association for Thoracic Surgery

Cardiothoracic Transplantation

Prognosis of patients removed from a transplant waiting list for medical improvement: Implications for organ allocation and transplantation for status 2 patients

Katherine J. Hoercher, RNa,c,d,*, Edward R. Nowicki, MD, MSa, Eugene H. Blackstone, MDa,b,*, Gurmeet Singh, MDa, Joan M. Alster, MSb, Gonzalo V. Gonzalez-Stawinski, MDa,d, Randall C. Starling, MD, MPHc,d, James B. Young, MDc,d, Nicholas G. Smedira, MDa,d

a Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, Cleveland, Ohio
b Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, Ohio
c Department of Cardiovascular Medicine, Cleveland Clinic, Cleveland, Ohio
d Kaufman Center for Heart Failure, Cleveland Clinic, Cleveland, Ohio

Received for publication November 13, 2007; accepted for publication January 25, 2008.

* Address for reprints: Katherine J. Hoercher, RN, Kaufman Center for Heart Failure, Cleveland Clinic, 9500 Euclid Ave/JJ-40, Cleveland, OH 44195. (Email: hoerchk{at}ccf.org).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objectives: To address the present controversy regarding optimal management of status 2 heart transplant candidates, we studied the short- and long-term fate of medically improved patients removed from our transplant waiting list to assess return of heart failure and occurrence of sudden cardiac death, identify interventions to improve outcomes, and compare their survival with that of similar transplanted patients.

Methods: From January 1985 to February 2004, 100 status 2 patients were delisted for medical improvement (median on-list duration, 314 days). Return of heart failure, sudden cardiac death, and all-cause mortality were determined from follow-up (mean, 7.7 ± 3.9 years among survivors; 10% followed >12 years). Hazard function modeling, competing-risks analyses, simulation, and propensity matching to equivalent patients undergoing transplantation were used to analyze and compare outcomes and predict benefit of interventions.

Results: Freedom from return of heart failure was 77% at 5 years. The most common mode of death was sudden cardiac death, with risk peaking at 2.5 years after delisting but remaining at 3.5% per year thereafter. Event-free survival at 1, 5, and 10 years was 94%, 55%, and 28%, respectively; simulation demonstrated that implantable cardioverter–defibrillators could have improved this to 45% at 10 years. Overall survival after delisting was better than that of matched status 2 patients who underwent transplantation, but was demonstrably worse after 30 months.

Conclusions: Status 2 patients, including those delisted, require vigilant surveillance and optimal medical management, implantable cardioverter–defibrillators, and a revised approach to transplantation timing, such that overall salvage is maximized while allocation of scarce organs is optimized.

Abbreviations and Acronyms ICD = implantable cardioverter–defibrillator; NYHA = New York Heart Association; SCD = sudden cardiac death; UNOS = Unified Network for Organ Sharing; Formula = peak oxygen consumption


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Cardiac transplantation has long been thought to be the most appropriate therapeutic option for patients with end-stage heart failure, but with the proliferation of life-extending alternative medical and surgical therapies of the past decade, this thinking might no longer be valid. Indeed, an increasing body of observational evidence casts doubt on a clear benefit of cardiac transplantation for Unified Network for Organ Sharing (UNOS) status 2 outpatients receiving optimal medical therapy.1,2Go To date, however, these reports are limited by short-term follow-up. Although a randomized trial of transplantation versus medical therapy for such patients has been proposed, it is unlikely to be undertaken.3,4Go

In the absence of such a trial, we sought to augment short-term data with long-term information by studying the fate of status 2 patients removed over the years from our heart transplant waiting list (delisted) because of medical improvement. We considered such patients as surrogates for medical therapy versus transplantation in stable outpatients with chronic heart failure. Specifically assessed were return of heart failure and occurrence of sudden cardiac death (SCD), interventions to improve outcomes, and survival compared with that of status 2 patients undergoing transplantation.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
From January 1, 1985, to February 1, 2004, 229 patients were removed (delisted) from Cleveland Clinic's cardiac transplant waiting list for alternative nontransplantation operations (n = 70), psychosocial factors (n = 30), medical contraindications to transplantation (n = 29), and medical improvement (n = 100). This last group of 100 patients, all of whom were in UNOS status 2 at delisting, formed the study cohort. Patients transferred to other cardiac transplant programs were not considered delisted.

Cases were identified through the Cleveland Clinic Unified Transplant Database, which is used for UNOS reporting and has been approved for use in research by the institutional review board, with patient consent waived. These data were confirmed and supplemented by review of each patient's clinical records to determine the reason for delisting, time on the waiting list, UNOS status and New York Heart Association (NYHA) functional class at delisting, and, when available, peak oxygen consumption (Formula ) during exercise at listing and delisting.

Clinical characteristics of patients at listing and delisting are presented in Go Table 1. Of this group, 91% were aggressively treated with optimal medical therapy for a minimum of 9 months before listing. Despite optimal medical therapy, persistent NYHA class III or IV symptoms and Formula of less than 14 mL · kg–1 · min–1 guided the decision to list potential transplant candidates. The remaining patients were admitted with cardiogenic shock requiring mechanical circulatory support and listed for transplantation within a week of referral.


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  		Table 1 Characteristics of patients delisted for medical improvement (n = 100)
 
Substantial subjective clinical improvement in NYHA class occurred in 86% of delisted patients, and there was an objective improvement in mean Formula from 14 ± 3.3 to 19 ± 3.2 mL · kg–1 · min–1 at delisting. Mean age at delisting was 52 ± 11 years (range, 26–73 years with 9% >age 65 years); 82% were men (Table 1). Median time on the waiting list was 314 days. Diagnoses were about equally divided between dilated and ischemic cardiomyopathy. Of note, malignant ventricular dysrhythmias were a common occurrence while these patients were on the waiting list.

Definitions and Indications
Medically improved patients were those who were in UNOS status 2 for more than 6 months with objective improvement in NYHA class (all but 1 known to be in NYHA class I or II at delisting, Table 1). Indications for delisting were improved Formula during exercise from listing to delisting, subjective improvement in heart failure symptoms, and a heart failure team consensus that cardiac transplantation would not provide a survival benefit over medical management. No formal surveillance program was implemented; rather, patients were remanded to the care of their local health care providers.

Outcomes
Patients or their surviving families were followed cross-sectionally by using an institutional review board–approved telephone script, with a common closing date of September 15, 2005. Follow-up was 100% complete, with mean follow-up of 7.7 ± 3.9 years among survivors; 10% were followed more than 12 years. Outcomes elicited included (1) return of heart failure, defined as return of NYHA class IV heart failure symptoms, relisting for transplantation, institution of mechanical circulatory support, or reported death in heart failure; (2) mode of death (heart failure, SCD, or noncardiac death); (3) insertion of an implantable cardioverter–defibrillator (ICD) among the 99 patients not having such a device inserted before delisting; and (4) all-cause mortality at any time during follow-up.

Data Analysis
All time-related post-delisting events were analyzed nonparametrically by using the method of Kaplan and Meier and parametrically by multiphase hazard modeling.5Go (For additional details, see http://www.clevelandclinic.org/heartcenter/hazard.) Multivariable analysis of outcomes was performed in the hazard function domain by using bagging as the primary variable selection method.6,7Go For this, 1000 bootstrap data sets were analyzed with a selection criterion of P = .05, followed by aggregation of models by the median rule. Variables used in these analyses were age at delisting (and its potential linearizing transformations of scale), sex, race, indication for listing (ischemic vs dilated cardiomyopathy vs other), dysrhythmia during listing (atrial fibrillation or flutter, sustained ventricular tachycardia, and SCD), NYHA class at listing and delisting, UNOS status at listing, time on the waiting list, and date of delisting, expressed as the interval between 1985 and delisting.

Event-free survival was defined as freedom from 3 end states: return of heart failure, SCD, and all other modes of death, each censored at any subsequent transplantation. Nonparametric simultaneous estimation of cumulative incidence for these events used the multiple decrement method of Andersen and colleagues.8Go For parametric estimation, rate of transition (hazard function) from event-free survival to each end state was estimated, and event-free survival and cumulative incidence of end states were calculated by using numeric integration. To estimate the potential benefit of ICD insertion, we simulated event-free survival were SCD completely eliminated.

Survival after delisting for medical improvement was compared with survival after transplantation for similar patients. For this, patients who underwent transplantation as UNOS status 2 were matched with delisted patients on age, sex, race, UNOS status at listing, diagnosis at listing, transplantation date, and waiting time to transplantation or delisting by using propensity score methodology.7,9Go This yielded 85 matched pairs.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Temporal Changes in Heart Failure Severity
During follow-up, 30 of 100 patients delisted for medical improvement had return of heart failure. Of these, only 8 were relisted (5 subsequently transplanted), and 15 died of heart failure. Six others had medical contraindications to transplantation, and importantly, the remaining patients were not referred back to a transplantation center to be reevaluated for transplantation as their heart failure worsened.

Risk of return of heart failure increased rapidly to 3.5% per year and then rose more slowly thereafter—but never leveled off or decreased—such that by 5 years it was nearly double that at 1 year (7.2% per year). This resulted in freedom from return of heart failure at 1, 5, and 10 years of 97%, 77%, and 51%, respectively ( Figure 1). The only incremental risk factor for return of heart failure was older age at delisting (Go Table 2).


Figure 1
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  		Figure 1. Freedom from return of heart failure (HF; return to New York Heart Association Class IV, relisting for transplantation, implementation of mechanical circulatory support, or death from heart failure). Each symbol represents a death positioned actuarially, vertical bars are 68% confidence limits, and numbers in parentheses are patients remaining at risk. The solid line is the parametric estimate enclosed within dashed 68% confidence limits.

 

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  		Table 2 Incremental risk factors for events after delisting for medical improvement
 
Sudden Cardiac Death
SCD was the most common mode of death, occurring in 26 patients. Risk of SCD peaked about 2.5 years after delisting at 10% per year and then decreased to a constant rate of 3.5% per year (Go Figure 2). As a result, freedom from SCD at 1, 5, and 10 years was 96.5%, 75%, and 62%, respectively. Incremental risk factors for SCD were ischemic cardiomyopathy (hazard ratio, 4.5) and delisting early in the experience (Table 2). ICD insertion was not the standard of care for much of the study time frame; thus, at delisting, only 1 patient had an ICD, but during the course of patient follow-up, 18 underwent ICD implantation.


Figure 2
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  		Figure 2. Risk of sudden death after delisting among patients without an implantable cardioverter–defibrillator. Dashed lines represent 68% confidence limits.

 
Event-free Survival
Risk of death in noncardiac modes increased moderately up to 3 to 4 years and then slowly decreased (Go Figure 3, A). If one then combines the competing risks of return of heart failure, SCD, and noncardiac death, event-free survival at 1, 5, and 10 years after delisting was 94%, 55%, and 28%, respectively (Figure 3, B). If one assumes 100% effectiveness of ICDs in preventing SCD, we estimated by means of simulation that event-free survival would have been 97%, 73%, and 45%, respectively (Go Figure 4).


Figure 3
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  		Figure 3. Competing risks after delisting for medical improvement. A, Rates of transition from event-free survival to heart failure, sudden cardiac death, or death from other causes. B, Resulting proportion of patients in each state (event-free survival, heart failure, sudden cardiac death, or other modes of death) across follow-up.

 

Figure 4
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  		Figure 4. Simulated improvement in event-free survival of patients were sudden cardiac death to be eliminated by inserting implantable cardioverter–defibrillators (ICD). Parametric survival curves are formatted as for Figure 1, except parametric confidence limits are not shown.

 
Survival and Comparison With Transplantation
During follow-up, 58 patients died. Survival of patients at 1, 5, and 10 years was 93%, 63%, and 35%, respectively, with a median time to death of 7 years (Go Figure 5). Incremental risk factors for death included older age at delisting, longer duration on the waiting list, and delisting earlier in the experience (particularly within the first 5 years). Among 85 propensity-matched pairs, survival was better for about 18 months for delisted patients than for those undergoing transplantation in status 2 because of the high early risk of transplantation (Go Figure 6). After about 30 months, survival was demonstrably better after transplantation (confidence limits nonoverlapping). Thus, at 5 and 10 years, survival after transplantation of status 2 patients was 85% and 70%, respectively, compared with 63% and 36%, respectively, for matched delisted status 2 patients.


Figure 5
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  		Figure 5. Survival of medically improved patients after delisting. Format is as in Figure 1.

 

Figure 6
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  		Figure 6. Comparison of survival of medically improved patients after delisting (circles) to propensity-matched Unified Network for Organ Sharing status 2 patients after cardiac transplantation (squares). Format is as in Figure 1.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Principal Findings
Approximately one third of patients removed from the heart transplant waiting list for medical improvement experienced return of heart failure, most dying without transplantation, but SCD was the leading cause of death. Short-term survival was better than that for patients undergoing transplantation (up to 18 months), but in the long-term, return of heart failure symptoms, SCD, and death from heart failure began exacting a heavy toll. After delisting, systematic follow-up with a heart failure specialist and ICD insertion might have substantially improved outcomes.

Temporal Changes in Heart Failure Severity
An increase in peak Formula levels that occurred during listing, which might have been due to the intensity of therapy in such patients, conferred only a short-term benefit but was not predictive of late outcomes. Favorable short-term outcomes (<2 years) in listed patients who increased their Formula levels has also been reported in some,10,11Go but not all,12Go series. The 9 patients listed for cardiogenic shock and requiring temporary mechanical circulatory support all had dramatic return of cardiac function and were subsequently delisted.

Risk of return of heart failure symptoms increased rapidly within a year of delisting and then slowly but steadily continued to increase. Late return of heart failure symptoms is not surprising because heart failure is a chronic and progressive disease. Importantly, follow-up care, especially with regard to contemporary disease management, was neither systematic nor intensive. Only 5% of patients were followed by a heart failure specialist after delisting; thus, the levels of care and compliance with heart failure therapies were unknown, and critically, the majority of patients who returned to NYHA class IV heart failure were not referred back to our transplantation center. Previous studies, as well as recent data, suggest that outcomes are improved by the attentive care provided within a heart failure disease management program.13-15Go

Sudden Cardiac Death
SCD was the most common mode of death for these patients, accounting for 45% of deaths. By means of simulation, we estimated that an ICD would have substantially improved intermediate and long-term event-free survival in this population after delisting because it clearly affects a mechanism of death not captured by improved functional capacity or exercise tolerance. Results of this simulation are similar to those observed in the Multicenter Automatic Defibrillator Implantation Trial II study of ICD therapy in patients with prior myocardial infarction and reduced left ventricular function, as well as in clinical studies of stable heart transplant candidates.16-18Go Beyond optimal medical therapy, the Sudden Cardiac Death in Heart Failure Trial demonstrated a 46% relative reduction in the risk of SCD in NYHA class II patients with an ICD and further explains the high risk of SCD in our stable heart failure group, patients who, for the most part, did not have an ICD.19Go

In a recent analysis of 50,000 UNOS registrants awaiting heart transplantation between 1990 and 2005, the presence of an ICD in status 1 candidates on the day of listing correlated with improved outcomes.20Go This same study demonstrated that 1-year survival of non-transplanted status 2 candidates in the most recent era (2000–2005) is approaching that of survival after transplantation. Although the authors were unable to determine the specific reasons for these improved outcomes, it is important to note that in the most recent era, 47% of listed status 2 patients had an ICD compared with 18% between 1995 and 1999 and 0% between 1990 and 1994.

Although the results of the Multicenter Automatic Defibrillator Implantation Trial II and Sudden Cardiac Death in Heart Failure Trial in NYHA class II patients are well known, and furthermore, ICD implantation is a class IA recommendation from the 2006 American College of Cardiology/American Heart Association/European Society of Cardiology guidelines,21Go Lietz and Miller20Go have shown that even in the most recent era, fewer than half of status 2 patients on the UNOS waiting list had ICDs. The ominous findings of SCD in our own study clearly demonstrate the need for ICDs in these "low-risk" patients.

Survival
Recent studies question whether cardiac transplantation provides a survival benefit over optimal medical therapy in status 2 patients.1,2Go To date, all published survival data comparing medical management of transplant candidates with transplanted patients are limited by follow-up of only 1 to 5 years.10,11,22,23Go The strength of our investigation is the 10-year follow-up. If one assumes that our delisted patients were the healthiest or lowest-risk patients, their survival should be better than that of the average status 2 patient after transplantation, and in our experience this is in fact the case out to at least 18 months. However, heart failure and SCD escalate thereafter, and data from both our study and prior investigations are insufficient to predict who will deteriorate over time.

Limitations
This is a nonrandomized observational study encompassing 20 years of experience from a single high-volume transplantation center but involving a relatively small number of patients. Numerous changes in clinical management occurred during this time, and multiple surgeons and cardiologists were involved in caring for these patients. Unfortunately, we were unable to quantify the intensity and quality of care after delisting to determine how these might have affected outcome. Major advances in medical and device therapies occurred as well, including use of β-blockers, ICDs, cardiac resynchronization therapy, and dissemination of evidence-based care. Importantly, because of improved survival in patients treated with β-blockers, the traditional cutoff point of less than 14 mg · kg–1 · min–1 for transplantation is being reassessed; a value of less than 12 mg · kg–1 · min–1 might be more appropriate.

Clinical Implications and Recommendations for Practice Guidelines
Although the outcomes of this study cannot be extrapolated to all status 2 transplant candidates, and we do not believe it to be a direct substitute for a trial of tailored medical therapy versus transplantation, we believe our findings have several implications for both status 2 patients and those being considered for delisting.

First, all patients meeting guideline criteria should have an ICD implanted.

Second, follow-up must be intense and is best done by heart failure specialists as if patients remained on the transplant waiting list.

Third, close periodic surveillance (every 3–6 months) is required to identify patients whose cardiac function is deteriorating.

Fourth, additional methods for monitoring both listed and delisted patients should be investigated, including implantable hemodynamic devices, microvolt T-wave alternans, and biomarkers, to anticipate deterioration earlier and prompt renewed consideration for relisting or status upgrade.

Fifth, timing of transplantation in this population remains a dilemma. More detailed and longer-term investigation into the prediction of survival for status 2 patients is needed, as has already been done for status 1 patients. Reliable predictive models for status 2 patients might help discriminate low- from high-risk patients, helping to guide time of listing.

Sixth, UNOS modifications to the current allocation system might be required when accurate predictive models become available. If the number of patients listed continues to decrease and efforts to increase organ donation are successful, more status 2 patients might be offered organs. In that case, one would need to balance long-term survival of the graft and morbidity associated with long-term immunosuppression against good short-term survival of low-risk patients who do not undergo transplantation. Consequently, it might be that in this situation, the lowest-risk patients should have transplantation delayed as long as possible and undergo transplantation only when matched to a perfect heart.


   Acknowledgments
 
We thank Lucy Thiuta, MS, for data management and analysis and Tess Parry for editorial assistance.


   Footnotes
 
Read at the Thirty-third Annual Meeting of the Western Thoracic Surgical Association, Santa Ana Pueblo, NM, June 27–30, 2007.

Randall C. Starling reports consulting fees from Medtronic, James B. Young reports consulting fees from Guidant and Medtronic and grant support from Medtronic.

* Supported in part by the Kenneth Gee and Paula Shaw, PhD, Chair in Heart Research. Back


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Jimenez J, Bennett Edwards L, Higgins R, Bauerlein J, Pham S, Mallon S. Should stable UNOS Status 2 patients be transplanted?. J Heart Lung Transplant 2005;24:178-183.[Medline]
  2. Deng MC, De Meester JM, Smits JM, Heinecke J, Scheld HH. Effect of receiving a heart transplant: analysis of a national cohort entered on to a waiting list, stratified by heart failure severity. Comparative Outcome and Clinical Profiles in Transplantation (COCPIT) Study Group. BMJ 2000;321:540-545.[Abstract/Free Full Text]
  3. Deng MC, Smits JM, Young JB. Proposition: the benefit of cardiac transplantation in stable outpatients with heart failure should be tested in a randomized trial. J Heart Lung Transplant 2003;22:113-117.[Medline]
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  12. Gullestad L, Myers J, Ross H, Rickenbacher P, Slauson S, Bellin D, et al. Serial exercise testing and prognosis in selected patients considered for cardiac transplantation. Am Heart J 1998;135:221-229.[Medline]
  13. Rich MW, Beckham V, Wittenberg C, Leven CL, Freedland KE, Carney RM. A multidisciplinary intervention to prevent the readmission of elderly patients with congestive heart failure. N Engl J Med 1995;333:1190-1195.[Medline]
  14. Kasper EK, Gerstenblith G, Hefter G, Van Anden E, Brinker JA, Thiemann DR, et al. A randomized trial of the efficacy of multidisciplinary care in heart failure outpatients at high risk of hospital readmission. J Am Coll Cardiol 2002;39:471-480.[Abstract/Free Full Text]
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  16. Moss AJ, Zareba W, Hall WJ, Klein H, Wilber DJ, Cannom DS, et al. Prophylactic implantation of a defibrillator in patients with myocardial infarction and reduced ejection fraction. N Engl J Med 2002;346:877-883.[Medline]
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