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Ann Thorac Surg 2012;93:699-704. doi:10.1016/j.athoracsur.2011.09.037
© 2012 The Society of Thoracic Surgeons
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Right arrow Transplantation - heart

Original Articles: Adult Cardiac

What Predicts Long-Term Survival After Heart Transplantation? An Analysis of 9,400 Ten-Year Survivors

Arman Kilic, MD, Eric S. Weiss, MD, MPH, Timothy J. George, MD, George J. Arnaoutakis, MD, David D. Yuh, MD, Ashish S. Shah, MD, John V. Conte, MD*

Division of Cardiac Surgery, Department of Surgery, The Johns Hopkins Medical Institutions, Baltimore, Maryland

Accepted for publication September 14, 2011.

* Address correspondence to Dr Conte, Division of Cardiac Surgery, The Johns Hopkins Hospital, Blalock 618, 600 N Wolfe St, Baltimore, MD 21287 (Email: jconte{at}jhmi.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: This case-control study was conducted to identify factors predictive of 10-year survival after orthotopic heart transplantation (OHT).

Methods: Prospectively collected data from the United Network for Organ Sharing registry were reviewed to identify adult patients undergoing OHT between 1987 and 1999 (N = 22,385) who had survived 10 years. Controls were those who had died within 10 years of OHT. Factors associated with 10-year survival were identified with multivariate logistic regression analysis. Lowess smoothing plots were used to identify linear breakpoints in continuous variables, and splines were incorporated when appropriate.

Results: There were 9,404 ten-year survivors (42%; mean follow-up, 14.0 ± 3.0 years) and 10,373 controls (46%) with a mean survival of 3.7 ± 3.3 years post-OHT. Predictors of 10-year survival in the optimal multivariate model were age younger than 55 (odds ratio [OR], 1.24; 95% confidence interval [CI], 1.10 to 1.38; p < 0.001), white race (OR, 1.35; 95% CI, 1.17 to 1.56; p < 0.001), shorter ischemic time (OR, 1.11; 95% CI, 1.05 to 1.18; p < 0.001), younger donor age (OR, 1.01; 95% CI, 1.01 to 1.02; p < 0.001), annual center volume of 9 or more (OR, 1.31; 95% CI, 1.17 to 1.47; p < 0.001), mechanical ventilation (OR, 0.53; 95% CI, 0.36 to 0.78; p = 0.001), and diabetes (OR, 0.67; 95% CI, 0.57 to 0.78; p < 0.001).

Conclusions: Age younger than 55 years, annual center volume of 9 or more, white race, shorter ischemic time, and younger donor age improved the likelihood of 10-year survival after OHT. Mechanical ventilation and diabetes reduced this likelihood. These data should serve as a useful guide to long-term prognostication in adult OHT.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

ADULT CARDIAC SURGERY: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

More than 5 million Americans suffer from heart failure [1]. Most of these patients can be managed with lifestyle modifications or medical management, or both. However, for those individuals with severe, refractory end-stage heart failure, orthotopic heart transplantation (OHT) remains the gold standard treatment. Although outcomes continue to improve, the availability of OHT remains limited by a shortage in donor organ supply. Indeed, fewer than 2,500 donor organs are available each year for OHT [2]. As such, careful selection of recipients to optimize outcomes is essential.

Although prior studies have examined predictors of short-term and intermediate-term survival after adult OHT, factors associated with long-term survival remain to be elucidated. National multi-institutional registries provide a wealth of data that can be used to assess such factors on a broader scale. The aim of this study was to identify predictors of 10-year survival after adult OHT by using the United Network for Organ Sharing (UNOS) database.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Data Source
The Standard Transplant Analysis and Research files were obtained from the UNOS registry. Follow-up data were available through 2010. This data set contains prospectively collected information on transplantations performed in the United States. Exempt status was granted by the Institutional Review Board because no patient or center identifiers were included.

Study Design
This was a case-control study limited to adult patients aged 18 years or older undergoing OHT between 1987 and 1999 in the prospectively collected UNOS registry. The study period did not extend beyond 1999 to limit era biasing because 10-year survivors would need at least 10 years of follow-up. The analysis excluded those undergoing repeat cardiac or multivisceral transplantation.

Cases were recipients who survived at least 10 years after OHT. Controls were patients who underwent OHT during the same era (1987 to 1999) and died within 10 years of the transplant procedure. Patients who were alive but had follow-up of less than 10 years were therefore excluded to limit potential selection bias in identifying predictors of loss to follow-up instead of death.

Data Analysis
The primary outcome of interest was 10-year survival. Baseline characteristics were compared between 10-year survivors and controls using the t test for continuous data and the {chi}2 test for categoric data. Exploratory univariate logistic regression analysis was performed to evaluate the effect of all plausible recipient, donor, and transplant covariates on 10-year survival. A listing of variables routinely collected by UNOS can be found on its Web site (http://www.unos.org).

Those variables that were significant predictors on univariate analysis were entered into the multivariate logistic regression model. Lowess smoothing plots were constructed for each continuous variable to determine if there were linear breakpoints that could account for the significance of that variable in predicting survival, and splines were added when appropriate. The appropriateness of inclusion of each significant covariate in the multivariate model was assessed using the likelihood ratio test. All models were also examined using pseudo-R 2, area under receiver operating curve, Akaike information criterion, and Hosmer-Lemeshow goodness-of-fit. Odds ratios with 95% confidence intervals were calculated for each covariate. Statistical significance was defined as a two-tailed value of p < 0.05 for univariate and multivariate analyses. All statistical analyses were performed using Stata 11 software (StataCorp LP, College Station, TX).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Study Population
During the study period, 22,385 adults underwent primary, single-organ OHT. There were 9,404 ten-year survivors (42.0%). The controls included 10,373 OHT recipients (46.3%) who died within 10 years of transplantation. The remaining 2,608 patients (10.9%) were lost to follow-up and therefore excluded from analysis.

Patients included in the study were a mean age of 51.4 ± 10.9 years, with 4,194 women (21.2%). Mean body mass index was 25.3 ± 4.6 kg/m2, and 16,509 recipients (83.5%) were white. The biatrial technique for OHT was used in 19,307 recipients (97.9%). Aside from 1987, where only 288 (1.5%) of included patients underwent OHT, the number of transplants per year in the study group was relatively uniform throughout the study period, with between 6% and 9% of the overall volume in each year.

Baseline Characteristics
In comparing baseline characteristics, 10-year survivors were significantly younger and had lower serum creatinine levels and lower body mass indices than controls (Table 1). A higher percentage of survivors were white, and fewer had comorbidities such as hypertension and diabetes. The indication for OHT was also different: the survivor cohort had a higher percentage of dilated cardiomyopathy and valvular disease but a lower percentage of coronary artery disease. In addition, fewer 10-year survivors required mechanical ventilation or an intraaortic balloon pump for circulatory support before OHT. Hemodynamic data were similar between survivors and controls except for a higher mean pulmonary capillary wedge pressure in survivors (21.9 ± 9.4 vs 21.5 ± 9.2 mm Hg, p = 0.04).


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  		Table 1 Baseline Recipient Characteristics Between 10-Year Survivors and Controls
 
With respect to donor variables, survivors had younger donors and more male donors (Table 2). Survivors also had fewer cytomegalovirus-positive donors, fewer donors taking antihypertensive medications, and a higher proportion had at least two-antigen human leukocyte antigen matching. Ischemic time was significantly shorter in 10-year survivors as well. Survivors were also more likely to have undergone OHT in the latter part of the study period. In addition, 10-year survivors underwent OHT at centers with a higher average annual volume (12.7 ± 8.1 vs 12.4 ± 8.4, p = 0.001).


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  		Table 2 Baseline Donor and Transplant Characteristics Between 10-Year Survivors and Controls
 
Logistic Regression Analysis for 10-Year Survival
Univariate logistic regression found 21 variables were significant predictors of 10-year survival and therefore were qualified for entry into the multivariate model (Table 3). Of these, five significantly and independently improved odds of 10-year survival in multivariate analysis: recipient age younger than 55 years, white race, shorter ischemic time, younger donor age, and annual center volume of nine or more OHTs. Two covariates, mechanical ventilation and diabetes, significantly reduced the likelihood of surviving 10 years after OHT. The spline terms at the breakpoints for recipient age and annual center volume were significant, indicating that these thresholds were indeed predictive breakpoints in these covariates. Breakpoints that improved the power of the model were not identified in ischemic time or donor age. The appropriateness of inclusion of all seven of the significant covariates in the multivariate model was tested in stepwise fashion using the likelihood ratio test. The Hosmer-Lemeshow goodness-of-fit for the final model had a nonsignificant p = 0.35, suggesting that the model was an appropriate fit for the data.


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  		Table 3 Significant Covariates in Multivariable Logistic Regression for 10-Year Survival
 
Recipient Age and Race
The breakdown of age cohorts (in years) was as follows: younger than 50, 6,962 (35.2%); 50 to 54.9, 3,718 (18.8%); 55 to 59.9, 4,398 (22.2%); 60 to 64.9, 3,471 (17.6%); 65 to 69.9, 1,117 (5.7%); and 70 or older, 111 (0.6%). Recipients younger than 55 years had a 24% increase in the odds of surviving to 10 years compared with recipients aged 55 or older (p < 0.001). White race similarly conferred a survival benefit, such that white recipients were at 35% increased odds of long-term survival compared with nonwhite (p < 0.001).

Ischemic Time and Donor Age
Ischemic time and donor age were the two donor or transplant variables that had a significant impact on long-term survival. The ischemic time in 18,872 patients (95.4%), was less than 6 hours, and 2,129 (48.5%) had an ischemic time of less than 2 hours. Each 1-hour reduction in ischemic time improved the odds of 10-year survival by 11% (p < 0.001).

Donor age had no identifiable breakpoints on graphical examination. Donors were younger than 30 years in 10,883 patients (55.0%), were 30 to 39 in 4,278 patients (21.6%), and were 40 years or older in 4,616 patients (23.3%). Each 1-year reduction in donor age was associated with a 1% improvement in the likelihood of 10-year survival, or, in other words, each decade decrease in donor age carried with it a 10% increase in the odds of 10-year survival.

Center Volume
The average annual center volume in OHT was 12.5 per year, with a median of 10 OHTs per year. On either end of the distribution, 2,493 recipients (12.6%) underwent OHT at centers with an annual volume of less than 5 OHTs, and 2,428 recipients (12.3%) underwent OHT at high-volume centers that performed more than 20 OHTs per year. A significant breakpoint of nine OHTs was identified as a volume threshold above which there was a 31% increase in the odds of surviving at least 10 years after transplantation. There were 11,348 patients (57.4%) who had undergone OHT at centers performing at least nine OHTs per year.

Mechanical Ventilation and Diabetes
The two covariates that significantly reduced the odds of long-term survival were mechanical ventilation before OHT and diabetes. Although present in a minority of patients, both were strong predictors of reduced survival. Moreover, ventilated patients had a 47% reduction in the likelihood of surviving to 10 years after OHT, and diabetic recipients had a 33% reduction. Indeed, 10-year survivors comprised 52.0% of patients with neither of these factors compared with 39.8% in diabetic recipients who were also ventilated (p < 0.001).

Year of OHT
Although the year of OHT had a significant impact on 10-year survival in univariate analysis, it was not a significant predictor in the multivariate model. Despite this, examining trends in the proportion of 1-, 5-, and 10-year survivors by transplant year in our study period revealed significant trends for each of these cohorts (Fig 1). Moreover, patients who underwent OHT in later years had improved survival at each time point (1, 5, and 10 years). The strongest trend was observed for the 10-year group (R 2 = 0.85, p < 0.001).


Figure 1
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  		Fig 1. Percentage of study patients that were 1-year, 5-year, and 10-year survivors, by transplant year.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
During the past 40 years, OHT has evolved into the gold standard therapy for end-stage heart failure. Although many institutional and registry data have been published regarding outcomes and predictors of outcomes after OHT, most have been limited to short-term and intermediate-term follow-up after transplantation. As such, the aim of the current study was to identify predictors of 10-year survival after first-time adult OHT using a large cohort of patients from the UNOS database.

Excluding patients lost to follow-up, there were 19,777 patients studied in this analysis, with 9,404 ten-year survivors (47.6%). Although this 10-year survival rate correlates with well-known data, it was encouraging to observe that survival at 1, 5, and 10 years all had positive correlations with later transplant year, as illustrated in Figure 1. Perhaps most striking is that the trend for 10-year survival was strongest, demonstrating that although improvements in shorter-term outcomes have likely occurred, sustained long-term survival has improved the most dramatically. Although these trends were observed, year of transplantation did not independently affect long-term survival in our multivariate analysis and may therefore be a reflection of a higher prevalence of other strong favorable predictors in later years.

Recipient Age
The upper limit of recipient age that should be considered for OHT has been debated in recent literature. In our analysis, age 55 years was an optimal threshold above which rates of long-term survival declined. There are an increasing number of reports of acceptable outcomes in select elderly patients, with the underlying thought that physiologic age may be as important a contributor to outcomes as chronologic age [3, 4]. However, several large studies have also confirmed our finding that older age is associated with poorer survival after OHT [5–7]. These latter studies have demonstrated that a principal contributor to worse outcomes in elderly patients is that they experience more infectious complications after transplant, presumably due to a decline in immune function. In addition, renal function declines with older age and subjects elderly patients to a higher risk of renal failure postoperatively.

Race
White race was also highly predictive of 10-year survival in this study. Moreover, whites were 35% more likely to be 10-year survivors compared with nonwhites. This finding was echoed in another UNOS analysis of more than 20,000 adult OHT recipients, where African Americans had an 11% absolute decrease in long-term survival compared with whites [8]. Whether these results reflect biologic differences or socioeconomic issues that may affect access to care remains to be established. Further research is warranted to identify the causes of these survival differences.

Diabetes
In the current study, diabetes significantly decreased odds of 10-year survival after OHT. Diabetic patients represent a population at risk for renal disease, and the use of nephrotoxic immunosuppressive agents may further compromise renal function after transplant. Furthermore, data exists regarding an increased risk of coronary artery disease, rejection, and infection in diabetic recipients after OHT [9–11]. A study using the UNOS database found that severity of diabetes correlated with survival, such that recipients with uncomplicated diabetes had similar survival to nondiabetic recipients, but those with complicated diabetes had worse outcomes compared with either group [12]. These data have led some centers to favor therapeutic strategies other than OHT in severe diabetic patients with end-stage heart failure.

Ventilation
The need for mechanical ventilation before OHT also significantly decreased the odds of long-term survival. This likely represents marginal cardiopulmonary reserve in the recipient. In addition, requiring this level of physiologic support often necessitates an intensive care unit stay, which in itself may represent an increased risk of morbidity or death after transplant due to factors such as nosocomial infection, nutritional depletion, and generalized deconditioning.

Ischemic Time and Donor Age
Donor age and ischemic time are variables that are known to affect donor organ quality. Therefore, not surprisingly, younger donor age and shorter ischemic time correlated with increased likelihood of 10-year survival after OHT in this study. Indeed, analyses of prior multicenter registries have demonstrated linear relationships between increasing donor age and an increasing mortality rate after OHT [13, 14].

An analysis of more than 30,000 OHT recipients demonstrated that the effect of ischemic time on survival relies on the donor age, such that younger donor hearts are able to tolerate longer ischemic times, but older donor hearts are particularly sensitive to prolonged ischemia [15]. This was also demonstrated in our analysis, where patients with marginal donors (age ≥ 40 and ischemic time ≥ 4 hours) had a 10% absolute decrease in 10-year survival odds compared with patients with other combinations of these factors (p < 0.001).

The effect of ischemic time on organ quality is also likely influenced by other donor characteristics and organ preservation methods that were not included in this analysis. Despite poorer outcomes with marginal donors, a principal issue that remains is addressing the limited donor supply. More research into methods of augmenting the donor supply or optimizing marginal organs is therefore clearly warranted.

Center Volume
Institutional volume has been increasingly investigated as a potential contributor to outcomes of complex surgical procedures, with the thought that more experience in performing the particular procedure as well as better institutional resources in managing the patient postoperatively lead to higher survival rates. Indeed, a recent study of UNOS data demonstrated this notion, finding that annual OHT volume significantly impacted 30-day and 1-year mortality [16]. Our study suggests that a volume of nine OHT per year is the optimal breakpoint, above which 10-year survival rates are significantly improved. This was echoed in an earlier UNOS analysis looking at short-term mortality rates in patients with OHT between 1987 and 1991, where a threshold of nine annual OHTs seemed to best define high-volume vs low-volume centers [17].

The effect of other processes of care, such as nurse-to-patient ratio, house staff, and intensive care unit resources may also affect long-term survival beyond procedural volume.

Anastomotic Technique
There has been increasing interest in whether the bicaval technique improves survival after OHT compared with the traditional biatrial anastomoses. A single-center study of 200 recipients demonstrated that the bicaval technique was associated with improved survival at 5 years compared with the biatrial technique [18]. However, a recent analysis of UNOS data showed similar survival rates, although the bicaval group required pacemaker implantation less frequently after transplant and also had a shorter hospital length of stay [19]. These latter findings have been demonstrated in other studies as well [20–23].

In the current study, anastomotic technique did not affect long-term survival, but given that the study period extended only to 1999, the biatrial technique was used in 98% of patients. Whether this variable affects 10-year survival will need to be assessed in future studies when follow-up data are available for more recent transplants where the bicaval technique is used more frequently.

Limitations
This study has several limitations that should be acknowledged. The analysis did not include some data that might potentially affect survival after OHT, such as ventricular assist device support. Ventricular assist devices are increasingly being used as a bridge to transplant; however, this variable was not routinely collected during our study period. Another covariate that could potentially affect outcomes is the preservation methods of the donor organ. Moreover, preservation of the donor organ during explantation, storage, and transport is an area of significant investigation, both in the solution used and method of application, and it is becoming increasingly evident that these variables may affect survival after transplant.

As with other large multi-institutional data sets, reporting biases are present in the UNOS registry. In addition, data are missing for some patients. Owing to the need to obtain 10-year follow-up, the study was limited to OHTs performed in or before 1999, and advancements in surgical technique and medical management as well as changing practice patterns may result in different factors influencing long-term survival after OHT in the current era.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported by Departmental Funds from the Department of Surgery, Johns Hopkins Hospital.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Jessup M, Brozena S. Heart failure N Engl J Med 2003;348:2007-2018.[Medline]
  2. Zaroff JG, Rosengard BR, Armstrong WF, et al. Consensus conference report: maximizing use of organs recovered from the cadaver donor: cardiac recommendations, March 28–29, 2001, Crystal City, Va Circulation 2002;106:836-841.[Abstract/Free Full Text]
  3. Blanche C, Takkenberg JJ, Nessim S, et al. Heart transplantation in patients 65 years of age and older: a comparative analysis of 40 patients Ann Thorac Surg 1996;62:1442-1446.[Abstract/Free Full Text]
  4. Crespo-Leiro MG, Paniagua-Martin MJ, Muniz J, et al. Long-term results of heart transplant in recipients older and younger than 65 years: a comparative study of mortality, rejections, and neoplasia in a cohort of 445 patients Transplant Proc 2005;37:4031-4032.[Medline]
  5. Bull DA, Karwande SV, Hawkins JA, et al. Long-term results of cardiac transplantation in patients older than sixty years. UTAH Cardiac Transplant Program. J Thorac Cardiovasc Surg 1996;111:423-427.[Abstract/Free Full Text]
  6. Borkon AM, Muehlebach GF, Jones PG, et al. An analysis of the effect of age on survival after heart transplant J Heart Lung Transplant 1999;18:668-674.[Medline]
  7. Weiss ES, Nwakanma LU, Patel ND, Yuh DD. Outcomes in patients older than 60 years of age undergoing orthotopic heart transplantation: an analysis of the UNOS database J Heart Lung Transplant 2008;27:184-191.[Medline]
  8. Allen JG, Weiss ES, Arnaoutakis GJ, et al. The impact of race on survival after heart transplantation: an analysis of more than 20,000 patients Ann Thorac Surg 2010;89:1956-1963.[Abstract/Free Full Text]
  9. Marelli D, Laks H, Patel B, et al. Heart transplantation in patients with diabetes mellitus in the current era J Heart Lung Transplant 2003;22:1091-1097.[Medline]
  10. Morgan JA, John R, Weinberg AD, Colletti NJ, Mancini DM, Edwards NM. Heart transplantation in diabetic recipients: a decade review of 161 patients at Columbia Presbyterian J Thorac Cardiovasc Surg 2004;127:1486-1492.[Abstract/Free Full Text]
  11. Klingenberg R, Gleissner C, Koch A, et al. Impact of pre-operative diabetes mellitus upon early and late survival after heart transplantation: a possible era effect J Heart Lung Transplant 2005;24:1239-1246.[Medline]
  12. Russo MJ, Chen JM, Hong KN, et al. Survival after heart transplantation is not diminished among recipients with uncomplicated diabetes mellitus: an analysis of the United Network of Organ Sharing database Circulation 2006;114:2280-2287.[Abstract/Free Full Text]
  13. Taylor DO, Stehlik J, Edwards LB, et al. Registry of the International Society for Heart and Lung Transplantation: twenty-sixth official adult heart transplant report—2009 J Heart Lung Transplant 2009;28:1007-1022.[Medline]
  14. Stehlik J, Feldman DS, Brown RN, et al. Interactions among donor characteristics influence post-transplant survival: a multi-institutional analysis J Heart Lung Transplant 2010;29:291-298.[Medline]
  15. Russo MJ, Chen JM, Sorabella RM, et al. The effect of ischemic time on survival after heart transplantation varies by donor age: an analysis of the United Network for Organ Sharing database J Thorac Cardiovasc Surg 2007;133:554-559.[Abstract/Free Full Text]
  16. Weiss ES, Meguid RA, Patel ND, et al. Increased mortality at low-volume orthotopic heart transplantation centers: should current standards change? Ann Thorac Surg 2008;86:1250-1259.[Abstract/Free Full Text]
  17. Hosenpud JD, Breen TJ, Edwards EB, Daily OP, Hunsicker LG. The effect of transplant center volume on cardiac transplant outcome. A report of the United Network for Organ Sharing Scientific Registry. JAMA 1994;271:1844-1849.[Medline]
  18. Aziz T, Burgess M, Khafagy R, et al. Bicaval and standard techniques in orthotopic heart transplantation: medium-term experience in cardiac performance and survival J Thorac Cardiovasc Surg 1999;118:115-122.[Abstract/Free Full Text]
  19. Weiss ES, Nwakanma LU, Russell SB, Conte JV, Shah AS. Outcomes in bicaval versus biatrial techniques in heart transplantation: an analysis of the UNOS database J Heart Lung Transplant 2008;27:178-183.[Medline]
  20. Laske A, Carrel T, Niederhauser U, et al. Modified operation technique for orthotopic heart transplantation Eur J Cardiothorac Surg 1995;9:120-126.[Abstract/Free Full Text]
  21. El-Gamel A, Yonan NA, Grant S, et al. Orthotopic heart transplantation: a comparison between the standard and the bicaval Wythenshawe technique J Thorac Cardiovasc Surg 1995;109:721-730.[Abstract/Free Full Text]
  22. Milano CA, Shah AS, Van Trigt P, et al. Evaluation of early postoperative results after bicaval versus standard cardiac transplantation and review of the literature Am Heart J 2000;140:717-721.[Medline]
  23. Solomon NA, McGiven J, Chen XZ, Alison PM, Graham KJ, Gibbs H. Biatrial or bicaval technique for orthotopic heart transplantation: which is better? Heart Lung Circ 2004;13:389-394.[Medline]



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