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Ann Thorac Surg 2012;93:1549-1555. doi:10.1016/j.athoracsur.2012.01.059
© 2012 The Society of Thoracic Surgeons
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Right arrow Mechanical Circulatory Assistance

Original Articles: Adult Cardiac

Risk Factors for Early Death in Patients Bridged to Transplant With Continuous-Flow Left Ventricular Assist Devices

George J. Arnaoutakis, MDa, Timothy J. George, MDa, Arman Kilic, MDa, Claude A. Beaty, MDa, Eric S. Weiss, MD, MPHa,b, John V. Conte, MDa, Ashish S. Shah, MDa,*

a Division of Cardiac Surgery, The Johns Hopkins Medical Institutions, Baltimore, Maryland
b The Bloomberg School of Public Health, The Johns Hopkins Medical Institutions, Baltimore, Maryland

Accepted for publication January 19, 2012.

* Address correspondence to Dr Shah, Division of Cardiac Surgery, The Johns Hopkins Hospital, Blalock 618, 600 N Wolfe St, Baltimore, MD 21287 (Email: ashah29{at}jhu.edu).

Presented at the Fifty-eighth Annual Meeting of the Southern Thoracic Surgical Association, San Antonio, TX, Nov 9–12, 2011.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: Recent evidence suggests patients bridged to heart transplant (BTT) have equivalent outcomes as those undergoing conventional orthotopic heart transplantation (OHT). However, data on risk factors for early death in BTT patients are limited.

Methods: We retrospectively reviewed the United Network for Organ Sharing database of all patients bridged to OHT with a HeartMate II from January 2005 to December 2010. The primary outcome was all-cause 90-day mortality. Additional postoperative outcomes were cerebrovascular accident and need for renal replacement therapy. Kaplan-Meier analysis assessed survival. Preoperative variables associated with 90-day death on univariate analysis (p < 0.2) were included in a multivariable Cox proportional hazards regression.

Results: A HeartMate II was used to bridge 1,312 patients (average age, 52 ± 12 years) to OHT, most commonly for idiopathic cardiomyopathy (50.7%). During the study, 171 patients (13.0%) died. The unadjusted 90-day survival was 92.3%. The highest annual average center volume in this cohort, examining for BTT recipients only, was 28 BTT procedures yearly. Postoperative cerebrovascular accident occurred in 29 patients (2.2%), and 106 (8.3%) required renal replacement therapy. Cox regression revealed age, glomerular filtration rate, African American race, human leukocyte antigen mismatch, serum bilirubin, need for mechanical ventilation, donor age, and prolonged ischemia time were associated with 90-day death. Early survival was improved for patients who underwent OHT at high-volume centers (p = 0.01).

Conclusions: This study examining risk factors for early death in patients bridged to OHT using HeartMate II mechanical assistance will aid in identifying patients best suited to benefit from this technology.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

Drs Conte and Russell disclose that they have financial relationships with Thoratec.

 

Left ventricular assist devices (LVAD) are increasingly being used to bridge patients to transplant (BTT). There were early concerns that BTT patients would have inferior survival than those undergoing conventional orthotopic heart transplantation (OHT) [1, 2]. However, contemporary devices have smaller profiles and improved reliability [3]. In the modern era of continuous-flow (CF) devices, several reports suggest that BTT patients who receive CF LVADs appear to have equivalent or modestly inferior survival after OHT than those undergoing conventional OHT [4–12].

However, actual clinical risk factors for early death are not well characterized. Despite growing enthusiasm to place CF LVADs as a BTT, given the complexity of device explant, it is important to identify patients in this particular cohort at high risk for early death. Therefore, we used United Network for Organ Sharing (UNOS) data to examine risk factors for early posttransplant death among patients bridged with CF devices.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 Acknowledgments
 References
 
This study was submitted to the Institutional Review Board and granted approval because no patient or center identifiers were used.

Data Source
The UNOS Standard Transplant Analysis and Research database represents an open cohort of prospectively collected donor-specific and follow-up data from October 1987 to December 2010. The data set includes all United States patients undergoing thoracic organ transplantation, with follow-up to March 2011.

Study Design
This was a retrospective cohort design that included adults (> 17 years) undergoing primary OHT as BTT with the HeartMate II (HM2; Thoratec Corp, Pleasanton, CA) from January 2005 to December 2010. Although several CF LVAD devices are available, the HM2 is the most commonly used CF device in the United States and the only device with Food and Drug Administration approval for a BTT indication. Therefore, we studied this device exclusively. Excluded were 10,019 patients without a VAD, 845 with older-generation pulsatile-flow LVADs, 519 with biventricular VAD, 6 with heart-lung transplantation, 68 with simultaneous kidney or liver transplantation, and 34 with prior OHT.

Variables Examined and Outcome Measures
The data set used contains more than 550 preoperative, intraoperative, and postoperative variables. Variables with greater than 15% missing data in this cohort were not examined. Variables examined in univariate analysis included primary diagnosis, demographics (age, sex, race, education level, insurance type, body mass index), comorbidities (hypertension, diabetes mellitus, chronic obstructive pulmonary disease, prior cardiac operations, glomerular filtration rate), and markers of acuity (treatment in the intensive care unit, need for intraaortic balloon pump support, Index for Mortality Prediction After Cardiac Transplantation [IMPACT] risk index), hemodynamic measurements (cardiac output, mean pulmonary capillary wedge pressure, pulmonary systolic pressure), donor variables (age, sex, race, tobacco use, serum creatinine), and transplant variables (ischemic time, human leukocyte antigen [HLA] mismatch, cytomegalovirus mismatch). Average annual center volume of OHTs performed in patients bridged with HM2 LVAD was also determined.

Overall risk was assessed according to the IMPACT risk index. The IMPACT score is a 50-point composite recipient risk index derived and cross-validated using UNOS data and is highly predictive of death at 1 year for adult patients receiving first-time OHT [11]. The risk index uses 12 recipient-specific preoperative variables (age, sex, race, diagnosis, creatinine clearance, preoperative dialysis, serum bilirubin, preoperative infection, need for mechanical ventilation, intraaortic balloon pump, or temporary circulatory support, and VAD) to assign relative points (maximum, 50). Because older-generation pulsatile VAD devices and CF devices besides the HM2 may contribute up to 8 points, we assigned all patients their appropriate risk index, with the maximum possible points modified to 42. A histogram and test for skewness were used to assure the pattern of scores followed a relatively normal distribution. Quartiles of risk strata were then assigned according to the distribution of risk scores within the cohort.

The primary end point was 90-day death, and 1-year death was also examined. Secondary outcomes examined were stroke, dialysis, and length of stay.

Statistical Analysis
We examined baseline characteristics among the cohort overall. Clinical characteristics were compared between patients who did or did not survive 90 days using the Student t test for continuous variables and the {chi}2 test for categoric variables. Survival at 90 days was estimated using the Kaplan-Meier method because interval has adequate follow-up in this data set. Patients were stratified into quartiles according to the IMPACT risk index, and the Mantel-Cox log-rank test was used to test for a significant difference in the survival curves.

Multivariable Cox proportional hazards regression was used to estimate risk of death with censoring for death, loss to follow-up, and administrative reasons (end of study period). Two separate multivariable regressions were performed. The first model was constructed using independent covariates (composite IMPACT risk index not included). Covariates with potential for confounding were first tested in a univariate fashion. In addition to variables associated with death on exploratory analysis (p < 0.2), previously recognized risk factors and those with biologic plausibility were incorporated in a forward and backward stepwise fashion into this first multivariable Cox model. The likelihood ratio test and Akaike's information criterion in a nested model approach identified the covariates that increased the explanatory power of the model. This method for model construction favors more parsimonious models. Because the multivariable analysis was performed with case-wise deletion, all covariates with greater than 15% missing data were not included. Testing of Schoenfeld residuals and visual inspection of complementary log-log plots for each variable confirmed that the assumption of proportional hazards had not been violated.

A second Cox regression was performed using only the composite IMPACT risk index, donor age, and ischemic time. No individual recipient characteristics were included in this regression model. This second regression was performed to determine if the IMPACT risk index was associated with 90-day death, after adjusting for donor age and ischemic time.

For statistical analyses, values of p of less than 0.05 (two-tailed) were deemed significant. Medians are presented with their interquartile range (IQR), and means are presented with standard deviations. Hazard ratios (HR) are displayed with 95% confidence intervals (CIs). Statistical testing was conducted using STATA 12 software (StataCorp LP, College Station, TX).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 Acknowledgments
 References
 
Cohort Statistics
The HM2 was used for BTT in 1,312 OHT recipients. These transplants were performed at 95 centers. The number of BTT heart transplant recipients each year steadily increased from 47 in 2005 to 534 in 2010 (Fig 1). At the time of listing, 541 patients (41.2%) had already undergone LVAD implant, and the remaining 771 (58.8%) underwent device placement in the interval between listing and OHT. Median waiting list time was 159 days (IQR, 68 to 307), and median overall follow-up was 11 months (IQR, 4 to 19 months). During the study, 171 patients died, for an incidence of 10.5 deaths/100 person-years. The Kaplan-Meier cumulative incidence of 1-year mortality was 14.4% (n = 150).


Figure 1
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  		Fig 1. Annual number of bridge-to-transplant (BTT) orthotopic heart transplantations (OHT) performed in the United States since 2005.

 
Average age was 52 ± 12 years. Additional baseline characteristics are reported in Table 1. Donor race distribution was 889 white (67.8), 221 African American (16.8%), 173 Hispanic (13.2%), and 29 other (2.2%). Patients who died within 90 days tended to be older, had worse renal function, higher serum bilirubin, and required mechanical ventilation (Table 1).


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  		Table 1 Patient Characteristics and Postoperative Outcomes
 
IMPACT Risk Score Generation
After assigning an IMPACT risk score index to all patients, the average score for the entire cohort was 4.9 ± 3.2 (range, 0 to 22). When divided into quartiles (Q), the breakdown of scores was: Q1 (0 to < 3) in 308 (23.5%), Q2 (≥ 3 to < 5) in 320 (24.4%), Q3 (≥5 to < 7) in 315 (24.0%), and Q4 (≥9) in 369 (28.1%), of which 64 patients (4.9%) had a risk score exceeding 10.

Risk-Adjusted Cox Regression and Survival Analysis
At 90 days, the unadjusted observed survival was 92.3%. Observed 1-year survival was 85.6%, unadjusted for recipient risk. Survival at 90 days for the cohort overall is depicted in Figure 2 . Survival at 90 days and 1 year, stratified by quartiles of IMPACT recipient risk index, is shown in Figure 3 .


Figure 2
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  		Fig 2. Kaplan-Meier estimate of 90-day survival is shown for the overall cohort.

 

Figure 3
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  		Fig 3. Kaplan-Meier estimates stratified by Index for Mortality Prediction After Cardiac Transplantation risk index quartiles (quartile 1, black line; quartile 2, gray line; quartile 3, dashed black line; quartile 4, dashed gray line) are shown for (A) 90-day survival and (B) 1-year survival. The p values were determined according to the Cox-Mantel log-rank test.

 
Risk adjustment with Cox multivariable analysis showed transplant year was not associated with death at 90 days. Age older than 60 years, African American race, lower glomerular filtration rate, higher serum bilirubin, preoperative recipient mechanical ventilation, donor age, and prolonged allograft ischemic time were associated with an increased hazard of death (Table 2). A higher average annual BTT OHT procedure volume was associated with lower risk of death. A separate Cox regression incorporating the IMPACT risk index showed each 1-point increase in the IMPACT risk score was associated with a 16% increase in the hazard of death at 90 days, after adjusting for allograft ischemic time and donor age (Table 3).


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  		Table 2 Results of Cox Regression Analysis a
 

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  		Table 3 Adjusted Cox Regression Using the Index for Mortality Prediction After Cardiac Transplantation Risk Index
 
Postoperative Complications
Commonly encountered postoperative complications are reported at the bottom of Table 1 for the cohort overall. Median length of stay was 15 days (IQR, 11 to 22 days). When examining patients stratified by 90-day survivors vs nonsurvivors, patients who died before discharge were more likely to require renal replacement therapy or have sustained a postoperative stroke (Table 1).


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 Acknowledgments
 References
 
Since 2005, more than 1,300 patients have been recorded in the UNOS database as having been bridged to OHT with the HM2 device, with a steady increase each year of the study. Extensive health care resources are committed to patients with end-stage heart failure who require LVAD support and, ultimately, OHT. Given the scarcity of donor organs and the complexity of the device explant procedure, optimizing the odds of a successful operation is essential.

Several clinical risk factors were identified that may aid in identifying BTT patients at risk for poor outcomes after OHT. We do not intend for these results to be exclusionary and preclude access to OHT for high-risk patients; rather, these results will facilitate individual transplant programs in establishing a risk profile of BTT patients that they are willing to assume. Although we surmise that our findings are generally applicable to HM2 patients, there is the caveat that these observations may not be reproducible in patients with pulsatile-flow LVADs or different models of CF LVADs.

Multivariable Analysis
Because previous reports have shown that center volume influences outcomes, we also incorporated center volume in our analysis [13, 14]. Consistent with these reports, after risk-adjustment, higher center volume was independently associated with a lower hazard of 90-day death. We speculate that cardiac transplant centers with more experience dealing with LVAD patients are more aware of the myriad complications and complexities that arise in the course of LVAD therapy, thereby explaining this observation. Furthermore, centers with a large number of BTT patients may have a greater infrastructure in place, especially with respect to LVAD coordinators and support personnel who are invaluable to these patients' care before and after OHT.

The independent effect of preoperative renal dysfunction on outcomes after cardiac operations has been shown previously for a wide array of cardiac procedures [15, 16]. Preoperative renal function is an important predictor of poorer 90-day survival after OHT in BTT patients, especially given recent evidence that renal function improves during LVAD therapy [17]. Another possible use of these data relates to the clinical decision making regarding simultaneous kidney transplantation. Given the magnitude with which impaired renal function affects 90-day survival in this patient population, BTT patients with depressed GFR should be given consideration for simultaneous kidney transplantation. However, this study was not designed to delineate a GFR cut point to recommend simultaneous kidney transplant, and further study is needed to better define this issue.

Past studies have not observed an outcome relationship associated with HLA mismatch; however, different time periods and outcome measures have been used [18]. An earlier study by Taylor and colleagues [19] proposed a differential role for HLA matching in short-term and longer-term patient survival, with HLA-A matched grafts having worse outcomes [19]. Furthermore, we recently examined panel reactive antibody levels in BTT patients and found that highly sensitized patients experienced equivalent outcomes after OHT [20]. The finding in the current study may reflect an artifact of the study period we included or the main outcome measure of 90-day survival. Future studies are needed to corroborate this finding.

Although the IMPACT risk index was initially devised to predict death at 1 year, we tested the ability of this risk index to independently predict 90-day death in this cohort of patients [11]. Each 1-point increase in the risk index was associated with a 16% increase in the hazard of 90-day death. An important finding was that the CF HM2 LVAD did not add any points in the original description of this risk index.

Previous Work
In 2009, Patlolla and colleagues [2] used the UNOS database to compare BTT outcomes with those of conventional OHT and reported worse survival rates for BTT patients. Their study may have been limited by incomplete LVAD data, however. In contrast, Russo and colleagues [9] examined the UNOS database from 2001 to 2006 to determine if BTT patients undergoing OHT had worse outcomes than those undergoing conventional OHT. They concluded that patients with intracorporeal and paracorporeal devices have equivalent post-OHT survival, although early survival was worse for patients with extracorporeal devices. However, their study did not focus on risk factors for poor outcomes in the specific subset of HM2 patients. Nativi and colleagues [7] reached similar conclusions as Russo and colleagues using the International Society for Heart and Lung Transplantation registry to examine the same issue in 8,557 patients worldwide. They also observed similar rejection rates between BTT patients and those undergoing conventional OHT, dispelling concerns about sensitization in BTT patients.

More recently, John and colleagues [8] concluded that post-OHT survival is not influenced by duration of LVAD support. Their study is strengthened by the robust HM2 data set and prospective data collection methodology in 250 BTT patients who underwent OHT. They also observed a trend toward worse 1-year survival after OHT in patients with percutaneous driveline infections during LVAD support (p = 0.07). We observed a similar trend on univariate analysis, but in our study this finding did not persist on multivariable analysis.

This study has some limitations, Because of the retrospective study design, we are unable to certify that all potential confounders were identified and examined. The UNOS data set is composed of many variables available for analysis; however, the possibility remains that potentially influential variables are not included in this analysis. Furthermore, large registry databases such as UNOS depend heavily on accurate and honest coding. We have assumed that all coding errors or missing data in the database are random and are thus unlikely to render any bias. If this assumption is incorrect, our conclusions may be influenced by residual bias. To lessen the effects of missing data, we did not incorporate variables with more than 15% missing data into the regression analysis.

Furthermore, the duration of pre-OHT LVAD support is thought to be important, and this information is not encoded in the database. We advocate inclusion of this information in large national registry data sets to further address this important issue. In addition, the mortality rate during the pre-OHT support period is unknown and should be incorporated into future investigations.

This study is further limited by the relatively short follow-up period. We began the study in 2005 because before then, there were few HM2 BTT patients in the UNOS registry. As the collective experience with the HM2 device accumulates, it will be important to understand how these risk factors may change over time.

In conclusion, this large, modern-era study used UNOS data to examine risk factors for early death in patients bridged to OHT with the HM2 CF device. With increasing use of HM2 mechanical assistance to bridge patients to OHT, these findings will aid in identifying patients best suited to benefit from this therapy.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
Acknowledgments
 References
 
DR FREDERICK GROVER (Aurora, CO): That was a nice presentation on the paper addressing the major risk factors for mortality and adverse events in patients undergoing continuous flow ventricular assist device (VAD) insertion as a bridge to transplant (BTT). It appears that your greatest risk factor is a patient being on a ventilator. Where do you see yourself taking this? How do you see this playing out? With risk factors such as these with a very high odds ratio for death are present, how does this affect your judgement on whether to proceed with a VAD procedure?

DR ARNAOUTAKIS: Thank you, Dr Grover, for those points. A couple of points that I would like to emphasize based on your question, one being, with these data I would emphasize that we treat each individual patient as just that—an individual patient—and refrain from using these findings as absolute contraindications to transplantation. The other important point to emphasize is that these findings are important in characterizing risk in BTT patients, and what we really want to send out as a message to various transplant centers is that they have as their prerogative what risk profile of BTT transplant recipients they are willing to take. Individual centers can apply these findings to determine when they are faced with a given patient what that actual risk is.

Regarding mechanical ventilation, it did have certainly the highest magnitude effect, but I will reiterate that it was a very low number of patients who were supported with mechanical ventilation. And even going back to the initial trial based on the HeartMate II study, the number of patients supported with mechanical ventilation before transplant in the pivotal study that led to the Food and Drug Administration approval was a very low number as well. There is a caveat that although that is the highest magnitude, it is one of the least commonly encountered risk factors.

The other point to make is that a fair number of patients present with impaired renal function, and a possible consideration from these data is the need or decision making regarding simultaneous kidney transplantation. Certainly, it is known that postoperative dialysis affects outcomes in a broad array of surgical procedures, both in cardiac and noncardiac surgical procedures. So certainly, if people go on to develop dialysis, their prognosis is poor, and maybe we should be giving more consideration to people who have impaired renal function up front.

DR SETH D. FORCE (Atlanta, GA): When you look at your data, as you kind of alluded to, you can look at it two ways. You can say this is really a complex group of patients who had a good survival and fairly low hazard ratios for the complications, and therefore the patients are at a slightly increased risk, but these are sick patients and you should go ahead and do the procedure or you can look for some exclusionary variables to kind of cut some patients out, saying they are too high risk. In the end, how do you look at your data?

DR ARNAOUTAKIS: Again, we didn't design the study with the intent of making any sort of conclusions that would exclude a potential therapy to any patient. The way that we really interpreted the data is in terms of defining a risk for your given transplant center. That is the prerogative for each transplant center to take whether they are willing to take on a certain risk profile of patients. In certain areas, like ours, there are five transplant centers in the nearby vicinity and patients are able to, if they are too high risk, potentially be listed at another center. So we really don't mean for this to be exclusionary, rather for transplant surgeons, transplant programs to really have a clear understanding of what risk they are assuming in a given patient.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
References
 
Drs Arnaoutakis, Weiss, and Beaty are Irene Piccinini Investigators in Cardiac Surgery. Dr George is the Hugh R. Sharp Cardiac Surgery Research Fellow. This research was partly supported by National Institutes of Health Grant 1T32CA126607-01A2 to Dr Arnaoutakis and by a Health Resources and Services Administration contract (231-00-0115). The content is the responsibility of the authors alone and does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. government.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

  1. Taylor DO, Edwards LB, Aurora P, et al. Registry of the International Society for Heart and Lung Transplantation: twenty-fifth official adult heart transplant report—2008 J Heart Lung Transplant 2008;27:943-956.[Medline]
  2. Patlolla V, Patten RD, Denofrio D, Konstam MA, Krishnamani R. The effect of ventricular assist devices on post-transplant mortality an analysis of the United Network for Organ Sharing thoracic registry J Am Coll Cardiol 2009;53:264-271.[Medline]
  3. Caccamo M, Eckman P, John R. Current state of ventricular assist devices Curr Heart Fail 2011;8:91-98.
  4. Drakos SG, Kfoury AG, Long JW, et al. Effect of mechanical circulatory support on outcomes after heart transplantation J Heart Lung Transplant 2006;25:22-28.[Medline]
  5. Pal JD, Piacentino V, Cuevas AD, et al. Impact of left ventricular assist device bridging on posttransplant outcomes Ann Thorac Surg 2009;88:1457-1461.[Abstract/Free Full Text]
  6. Williams ML, Trivedi JR, McCants KC, et al. Heart transplant vs left ventricular assist device in heart transplant-eligible patients Ann Thorac Surg 2011;91:1330-1333discussion 1333–4.[Abstract/Free Full Text]
  7. Nativi JN, Drakos SG, Kucheryavaya AY, et al. Changing outcomes in patients bridged to heart transplantation with continuous- versus pulsatile-flow ventricular assist devices: an analysis of the registry of the International Society for Heart and Lung Transplantation J Heart Lung Transplant 2011;30:854-861.[Medline]
  8. John R, Pagani FD, Naka Y, et al. Post-cardiac transplant survival after support with a continuous-flow left ventricular assist device: impact of duration of left ventricular assist device support and other variables J Thorac Cardiovasc Surg 2010;140:174-181.[Abstract/Free Full Text]
  9. Russo MJ, Hong KN, Davies RR, et al. Posttransplant survival is not diminished in heart transplant recipients bridged with implantable left ventricular assist devices J Thorac Cardiovasc Surg 2009;138:1425-1432e1–3.[Abstract/Free Full Text]
  10. Smedira NG, Hoercher KJ, Yoon DY, et al. Bridge to transplant experience: factors influencing survival to and after cardiac transplant J Thorac Cardiovasc Surg 2010;139:1295-1305305 e1–4.[Abstract/Free Full Text]
  11. Weiss ES, Allen JG, Arnaoutakis GJ, et al. Creation of a quantitative recipient risk index for mortality prediction after cardiac transplantation (IMPACT) Ann Thorac Surg 2011;92:914-921discussion 921–2.[Abstract/Free Full Text]
  12. Urban M, Pirk J, Dorazilova Z, Netuka I. How does successful bridging with ventricular assist device affect cardiac transplantation outcome? Interact Cardiovasc Thorac Surg 2011;13:405-409.[Abstract/Free Full Text]
  13. Russo MJ, Iribarne A, Easterwood R, et al. Post-heart transplant survival is inferior at low-volume centers across all risk strata Circulation 2010;122(11 Suppl):S85-S91.[Abstract/Free Full Text]
  14. 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;86:1250-1260.[Abstract/Free Full Text]
  15. Arnaoutakis GJ, Bihorac A, Martin TD, et al. RIFLE criteria for acute kidney injury in aortic arch surgery J Thorac Cardiovasc Surg 2007;134:1554-1561.[Abstract/Free Full Text]
  16. Chertow GM, Levy EM, Hammermeister KE, Grover F, Daley J. Independent association between acute renal failure and mortality following cardiac surgery Am J Med 1998;104:343-348.[Medline]
  17. Russell SD, Rogers JG, Milano CA, et al. Renal and hepatic function improve in advanced heart failure patients during continuous-flow support with the HeartMate II left ventricular assist device Circulation 2009;120:2352-2357.[Abstract/Free Full Text]
  18. Nwakanma LU, Williams JA, Weiss ES, Russell SD, Baumgartner WA, Conte JV. Influence of pretransplant panel-reactive antibody on outcomes in 8,160 heart transplant recipients in recent era Ann Thorac Surg 2007;84:1556-1563.[Abstract/Free Full Text]
  19. Taylor CJ, Smith SI, Sharples LD, et al. Human leukocyte antigen compatibility in heart transplantation: evidence for a differential role of HLA matching on short- and medium-term patient survival Transplantation 1997;63:1346-1351.[Medline]
  20. Arnaoutakis GJ, George TJ, Kilic A, et al. Effect of sensitization in US heart transplant recipients bridged with a ventricular assist device: update in a modern cohort J Thorac Cardiovasc Surg 2011;142:1236-1245 e1.[Abstract/Free Full Text]




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