Do Posttransplant Outcomes Differ in Heart Transplant Recipients Bridged With Continuous and Pulsatile Flow Left Ventricular Assist Devices?
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1 Do Posttransplant Outcomes Differ in Heart Transplant Recipients Bridged With Continuous and Pulsatile Flow Left Ventricular Assist Devices? Kimberly N. Hong, MHSA, Alexander Iribarne, MD, MS, Jonathan Yang, MD, Basel Ramlawi, MD, Hiroo Takayama, MD, Yoshifumi Naka, MD, PhD, and Mark J. Russo, MD, MS Section of Cardiac and Thoracic Surgery, Department of Surgery, and Center for Health and the Social Sciences, University of Chicago, Chicago, Illinois; Division of Cardiothoracic Surgery, Department of Surgery, College of Physicians and Surgeons, Columbia University, New York, New York; and Methodist DeBakey Heart and Vascular Center, Baylor University, Houston, Texas Background. The purpose of this study was to compare posttransplantation morbidity and mortality in orthotopic heart transplant recipients bridged to transplant with (1) continuous-flow left ventricular assist device (LVAD), (2) pulsatile-flow LVAD, or (3) inotropic therapy only with no LVAD. Methods. The United Network for Organ Sharing provided deidentified patient-level data. All status 1 orthotopic heart transplant recipients (n 7,744) 18 or more years of age and transplanted between January 1, 2001, and December 31, 2008, were included. Follow-up was available through June 18, Recipients were stratified into three groups: inotropes (n 5,448, 70.4%), continuous-flow LVAD (CONT [n 564, 7.3%]), and pulsatile-flow LVAD (PULS [n 1,732, 22.4%]). The primary outcome measure was risk-adjusted posttransplant graft survival (PTGS) at 90 days. Secondary outcomes included risk-adjusted PTGS at 90 days to 1 year and 1 to 5 years. Results. Unadjusted PTGS was similar in all groups (p 0.920). When compared with recipients bridged with inotropes, PTGS for patients bridged with an LVAD (CONT or PULS) did not differ in any follow-up period analyzed (<90 days, 90 days to 1 year, and 1 to 5 years). The PTGS in the CONT group (p 0.021), but not in the PULS group (p 0.244), improved significantly between the first half of the study period (2001 to 2004) and the second half (2005 to 2008). Conclusions. Compared with recipients bridged with inotropes, neither unadjusted nor adjusted PTGS differed for either the CONT group or the PULS group. Outcomes among the CONT group improved significantly from the first to the second half of the study period. (Ann Thorac Surg 2011;91: ) 2011 by The Society of Thoracic Surgeons Accepted for publication Feb 7, Presented at the Poster Session of the Forty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 25 27, Address correspondence to Dr Russo, Section of Cardiac and Thoracic Surgery, University of Chicago Medical Center, 5841 S Maryland Ave, Ste E-500/MC 5040, Chicago, IL 60637; mrusso@uchicago. edu. Over the last decade, the number of heart transplant recipients supported by a left ventricular assist device (LVAD) at time of transplantation has more than doubled to more than 400 a year [1]. Given their smaller size and improved durability compared with firstgeneration devices, pulsatile-flow and continuous-flow devices have become the standard device for bridging patients to transplantation [2]. A number of recent studies have demonstrated promising outcomes while on support with continuous flow devices [3 5]. However, studies examining posttransplant outcomes of heart transplant recipients bridged with continuous flow devices are limited by size or the absence of a control group [6, 7]. In addition, there is evidence to suggest that long-term, continuous-flow support can result in hemodynamic dysfunction, [8] including alterations in the renin-angiotensin system [9], systemic vascular resistance [10], and vascular integrity [11], as well as bleeding disorders [12, 13]. The impact of these phenomena on clinical outcomes remains unknown. The purpose of this study was to compare posttransplant outcomes of patients bridged with continuous-flow LVADs, pulsatile-flow LVADs, and inotropes only. This study improves over previous studies because it is the largest analysis to date examining posttransplant outcomes in recipients bridged to transplantation with pulsatile-flow versus continuous-flow devices. Furthermore, to compare outcomes in a more homogenous population, the study population was limited to status 1 patients bridged with either implantable devices or inotropes. Material and Methods Data Collection Approval for this study was granted by Columbia University s Institutional Review Board. The United Network 2011 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur
2 1900 HONG ET AL Ann Thorac Surg LVAD AND POSTTRANSPLANT SURVIVAL 2011;91: for Organ Sharing (UNOS) provided deidentified eventlevel data from the Thoracic Registry (data source ), where each observation represents a heart transplant. These data include all heart transplant recipients and associated donors in the United States reported to the Organ Procurement and Transplantation Network since October Data entry by all US transplant centers is mandated by the 1984 National Transplantation Act. Study Population The study population included 7,744 orthotopic heart transplants among status 1 recipients 18 years of age or older between January 1, 2001, and December 31, Follow-up data were provided through June 18, Recipients were stratified into three groups: continuous-flow LVADs (CONT), pulsatile-flow LVADs (PULS), and inotropes with no LVAD (INO). The PULS devices included the Novacor (World Heart Inc, Salt Lake City, UT), Heartmate I (Thoratec Corp, Pleasanton, CA), Thoratec IVAD (Thoratec Corp, Pleasanton, CA), and LionHeart (Arrow International, Reading, PA). The CONT devices included the Heartmate II (Thoratec Corp, Pleasanton, CA), Micromed/Debakey (MicroMed Cardiovascular, Inc, Houston, TX), Jarvik (Jarvik Heart Inc, New York, NY) and Ventracor/ Ventrassist (Ventracor, Australia). Outcome Measures The primary outcome measure was actuarial posttransplant graft survival (PTGS). Secondary outcome measures included transplant hospitalization morbidity measured by the incidence of postoperative stroke, infection, renal failure requiring dialysis, and primary graft failure at 90 days. In addition, cause of death was grouped into one of six categories: infection, cerebrovascular, cardiovascular, renal failure, pulmonary, and rejection. Data Analysis Continuous variables were reported as the mean SD and compared by using the Student t test. To compare categorical variables, the 2 test was used. The conventional p value of 0.05 was used to determine statistical significance. All reported p values are two sided. To assess temporal trends in survival, patients were grouped into two eras based on year of transplant: era 1, 2000 to 2004; and era 2, 2005 to Survival and Other Time-to-Event Analysis Kaplan-Meier analysis was used to calculate actuarial PTGS. For PTGS analysis, the outcome of interest was death (n 1,611, 20.8%) or retransplantation (n 69, 0.9%). Other patients, including those lost to follow-up (n 146, 1.9%) or alive at last follow-up (n 5,918, 76.4%), were censored on the day of last known followup. To assess the simultaneous effect of multiple variables on PTGS after orthotopic heart transplant, multivariable Cox proportional hazards regression (backward, p 0.15) was used to determine the relationship between groups and overall PTGS. Because the relationship between PTGS and VAD type was found to be time dependent, the hazard ratios for the two VAD types during various time intervals (less than 90 days, 90 days to 1 year, and 1 to 5 years) were reported. Risk-adjusted PTGS, derived from multivariate Cox regression analysis, was expressed as hazard ratios (HR) with 95% confidence intervals. Multivariable logistic regression analysis (backward, p 0.15) was used to determine the relationship between groups and secondary outcome measures. Riskadjusted secondary outcomes, derived from multivariable logistic regression analysis, were expressed as odds ratios with 95% confidence intervals. Regression analysis included the following variables: donor age; donor diabetes mellitus more than 6 years; donor to recipient weight ratio less than 0.7; etiology of heart failure, amyloid; etiology, congenital; etiology, hypertrophic cardiomyopathy; etiology, ischemic cardiomyopathy; etiology, other; etiology, restrictive cardiomyopathy; etiology, sarcoid; etiology, valvular; female donor/female recipient, female donor/male recipient, male donor/female recipient; hepatitis C (positive) donor, hepatitis C (positive) recipient; hospitalized at time of transplant, intensive care unit admission at time of transplant; insulin-dependent donor; intubated at time of transplant; ischemic time; number of previous heart transplants; heart transplant center volume (per center per year); previous heart transplant within 90 days; recipient age; recipient estimated glomerular filtration rate; recipient total bilirubin; recipient body mass index greater than 35, recipient body mass index less than 18.5; recipient diabetes mellitus; reoperation; and transplant year. Results Study Population Analysis included 7,744 orthotopic heart transplant recipients with a mean follow-up time of years (range, 0 to 8.28). Recipients were stratified into three groups: continuous-flow LVAD (CONT [n 564; 7.3%]), pulsatile-flow LVAD (PULS [n 1,732; 22.4%]), and inotropes with no LVAD (INO [n 5,448; 70.4%]). Patient characteristics are summarized in Tables 1 and 2. Posttransplant Survival Unadjusted PTGS was similar in all three groups (p 0.920; Fig 1). Likewise, in risk-adjusted analysis, PTGS for patients bridged with an LVAD (CONT or PULS) did not differ in any follow-up period analyzed when compared with INO alone (Table 3). During the 1 to 5 year follow-up interval, however, there was a trend toward improved survival in the PULS group compared with INO alone (HR 0.78, 0.60 to 1.00, p 0.05). Transplant Hospitalization Morbidity The risk of infection, reoperation, and stroke, were higher in the CONT and PULS groups compared with the INO group; however, there was no difference among the groups in primary graft failure at 90 days and renal
3 Ann Thorac Surg HONG ET AL 2011;91: LVAD AND POSTTRANSPLANT SURVIVAL 1901 Table 1. Baseline Patient Characteristics Characteristics CONT PULS INO Total p Value a Number % 22.4% 70.4% Recipient age Mean SD Donor age Mean SD Number of previous heart transplants Mean SD Etiology: dilated cardiomyopathy n % 46.1% 42.5% 42.5% 42.8% Etiology: ischemic cardiomyopathy n % 44.7% 48.8% 41.3% 43.2% Diabetes mellitus recipient n % 27.0% 25.3% 23.2% 24.0% Body mass index 35 Mean SD 6.0% 7.6% 3.8% 4.8% Body mass index 18.5 Mean SD 2.3% 1.4% 4.1% 3.3% Intubated n % 1.6% 2.1% 2.3% 2.2% Total bilirubin 2 Mean SD 11.3% 10.9% 13.5% 12.8% Estimated glomerular filtration rate Mean SD Intensive care unit at time of transplant n , % 17.0% 21.7% 47.9% 39.8% Hospitalized at time of transplant n , % 37.4% 51.9% 69.1% 62.9% Ischemic time Mean SD Male recipient: female donor n , % 12.4% 14.7% 16.6% 15.9% Male recipient: male donor n 387 1,201 3,215 4, % 68.6% 69.3% 59.0% 62.0% Female recipient: female donor n % 8.0% 4.8% 12.0% 10.1% a The p values are based on analysis of variance and covariance. Recipients were stratified into three groups: continuous-flow left ventricular assist device (LVAD [CONT]), pulsatile-flow LVAD (PULS), and inotropes with no LVAD (INO).
4 1902 HONG ET AL Ann Thorac Surg LVAD AND POSTTRANSPLANT SURVIVAL 2011;91: Table 2. Continuous Flow recipients by Era (2001 to 2004 and 2005 to 2008) Total p Value Number n % Status 1a n % Intensive care unit at time of transplant n % Intubated n % Diabetes mellitus recipient n % Etiology: ischemic cardiomyopathy n % Etiology: dilated cardiomyopathy n % Total bilirubin 2 Mean SD Body mass index 18.5 N % Body mass index 35 n % Number of previous transplant Mean SD Donor age Mean SD Recipient age Mean SD failure requiring dialysis. Compared with the INO group, length of hospitalization was significantly higher in the PULS group ( days, p 0.001) and the CONT group ( days, p 0.001); however, length of stay in the PULS and CONT groups did not differ from each other (p 0.484). Cause of Death As described in Table 4, death due to cardiovascular, cerebrovascular, acute rejection, pulmonary, or renal failure did not differ across groups. However, there was a trend toward a higher incidence of infectionrelated death (p 0.07) in the PULS group. Changes in CONT Outcomes Over Time Between the first half of the study period (2001 to 2004) and the second half (2005 to 2008), unadjusted PTGS improved significantly in the CONT group (p 0.021), but not in the PULS group (p 0.244; Figs 2 and 3). This relationship persisted in risk-adjusted analysis. During the first half of the study period, the CONT group had significantly worse PTGS at 90 days (HR 2.314, to 5.296, p 0.047) compared with the INO group; however, during the second half of the study period, there was no difference in PTGS at 90 days between the two groups (HR 1.122, to 1.956, p 0.686). Concurrently, there was a trend toward decreased length of
5 Ann Thorac Surg HONG ET AL 2011;91: LVAD AND POSTTRANSPLANT SURVIVAL 1903 Fig 1. Unadjusted posttransplant graft survival among continuous flow (CONT) group (solid line), pulsatile flow (PUL) group (dotted line), and inotrope with no LVAD (INO) group (dashed line). stay (p ) in the CONT group from the first half ( days) to the second half of the study period ( days). However, in the CONT group, there was no improvement in infection, stroke, renal failure requiring dialysis, reoperation, or primary graft failure at 90 days from the first to second half of the study period. Comment In our previous study examining posttransplant outcomes in patients with various types of LVADs, we found that intracorporeal LVADs, including both pulsatile-flow and continuous-flow devices, were not associated with diminished posttransplant graft survival. Secondary analysis revealed that posttransplant graft survival between recipients with pulsatile-flow and continuous-flow devices did not differ. However, those with pulsatile-flow devices actually demonstrated improved survival beyond 5 years after transplant [1]. This current study contains a more detailed analysis of intracorporeal LVADs, including a larger study population and longer follow-up. Before this study, we hypothesized that recipients bridged to transplant with continuous-flow devices would have worse posttransplant outcomes relative to recipients bridged with pulsatileflow devices, especially in the short term. This hypothesis was based on preliminary evidence suggesting that hemodynamic support with long-term continuous flow may be associated with deleterious effects. Specifically, previous animal studies suggested that prolonged periods of nonpulsatile flow result in vascular remodeling, including changes in vascular tone, systemic vascular resistance, and histologic structure, as well as disruption of neuroendocrine feedback such as the renin-angiotensin system [8 11, 14 16]. Further data supporting this hypothesis include a preliminary study by our group demonstrating that recipients bridged with continuous-flow devices suffered from more severe vasodilatory shock in the posttransplant period and required greater dosages and durations of vasoactive medication support [9]. Finally, there is a growing body of evidence suggesting longer-term support on continuous-flow devices is associated with impaired platelet function [12] and higher rates of bleeding [13]. In the context of this study, the hypotheses stated above would be supported by worsened short-term outcomes among the CONT group, particularly with regard to survival and primary graft failure. However, the findings of our analysis demonstrate that posttransplant graft survival among the CONT group did not differ from either the PULS group or the INO group at any posttransplant time interval (less than 90 days, 90 days to 1 year, or 1 to 5 years). Compared with the INO group, in-hospital complications, including infection, stroke, and cardiac reoperation, were significantly higher in the CONT and PULS groups. Likewise, length of stay was longer in the PULS and CONT groups compared with the INO group. However, renal failure requiring dialysis and primary graft failure did not differ among groups. Death at 90 days due to cardiovascular, cerebrovascular, acute rejection, pulmonary, or renal failure did not differ across groups. However, there was a trend toward a higher incidence of infection-related death in the pulsatile group. After a new device is approved for use and adopted by a much broader set of providers, this dissemination may change the clinical effectiveness and cost effectiveness of the device therapy. During the first half of the study period (2001 to 2004), CONT recipients did, in fact, have significantly worse adjusted posttransplant graft survival during the first 90 days after transplant compared with the PULS and INO groups. However, unadjusted actuarial posttransplant graft survival improved significantly for CONT recipients from the first half (2001 to 2004) to the second half (2005 to 2008) of the study period. This same improvement was not observed in the PULS group. Concurrently, length of stay improved in the CONT group over this time period. Changes in Outcomes Over Time Improvements in surgical device therapy do not only occur in research and development laboratories. Clinical practice itself is also the locus of much downstream learning and innovation. Although identifying particular explanations is beyond the scope of this analysis, there are several important sources of postmarketing innovation and learning associated with LVADs, all of which may impact clinical outcomes. These improvements in outcomes over time may be related to changes in the device technology itself [17]. That includes the introduction or discontinuation of particular devices or technical modification of existing devices. In this case, introduction of new device technology does not appear to explain these temporal differences. In further analysis, only one
6 1904 HONG ET AL Ann Thorac Surg LVAD AND POSTTRANSPLANT SURVIVAL 2011;91: Table 3. Graft Survival and In-Hospital Complications Device Type HR a LL 95% UL 95% p Value a Graft survival 90 days Continuous Pulsatile days to 1 year Continuous Pulsatile to 5 years Continuous Pulsatile years Continuous Pulsatile In-hospital complications OR b p Value a Stroke Continuous Pulsatile Dialysis Continuous Pulsatile Infection Continuous Pulsatile Cardiac reoperation Continuous Pulsatile Primary graft failure 90 days Continuous Pulsatile Graft survival HR a p Value a 2001 to 2004 Continuous Pulsatile to 2008 Continuous Pulsatile In-hospital complications for CONT recipients OR b p Value b Stroke Dialysis Infection Cardiac reoperation Primary graft failure at 90 days a Compared with inotropic (INO) support. b Continuous flow (CONT) from era 2 (2005 to 2008) compared with era 1 (2001 to 2004). HR hazard ratio; LL lower limit; OR odds ratio; UL upper limit. of the four commonly used CONT devices was associated with diminished posttransplant graft survival at 90 days. This device was used more frequently in the second half of the study and, therefore, does not explain improvements in outcomes. Another source of learning, and therefore improved outcomes, relates to patient selection an understanding of which patients are good candidates for a particular therapy and which are not. There were some differences in patient population during the two periods, including an increased proportion of patients in era 1 having an ischemic etiology for their heart failure and elevated bilirubin levels. A third dimension of downstream learning is that physicians gain further knowledge about integrating a technology into the management of particular patients. These include improvements in surgical technique and advances in perioperative management. Other clinical investigators have described the adoption of improved anticoagulation regimens, better antimicrobial management [18], recognition of the association of von Willebrand factor deficiency with CONT devices [13], more aggressive management of aortic valve insufficiency [19], and adoption of practices that consider the new physiologic variables imposed by the nature of continuous flow, such as avoiding suction events. It appears that these are important advances in the field [20]. Study Limitations Patient registries often suffer from data entry variability. However, fields contained within this database were generally well populated with a 95% to 99% data entry rate for the majority of variables. Although the UNOS reporting system provided variable definitions in data guidelines, definitions may still differ by center. Second, the limited time points for collection of data in the UNOS registry (at listing, at transplantation, and at follow-up) preclude the analysis of clinical status at the time of device implantation or over the course of
7 Ann Thorac Surg HONG ET AL 2011;91: LVAD AND POSTTRANSPLANT SURVIVAL 1905 Table 4. Causes of Death at 90 Days CONT PULS INO Total p Value Number 564 1, ,744 Cardiovascular n % Cerebrovascular n % Infection n % Acute rejection n % Pulmonary n % Renal failure n % Other n % CONT continuous-flow LVAD; INO inotropes with no LVAD; PULS pulsatile-flow LVAD. mechanical circulatory support. Given that many of the CONT patients received their device as part of a study, they were likely a healthier group overall compared with the PULS patients. However, to decrease the heterogeneity of the study population, analysis was limited to status 1 recipients bridged with either implantable devices or inotropes. Furthermore, we could not stratify patients by the length of support by a particular device. Length of device support is not only a particularly strong predictor of end-organ dysfunction and poorer outcome, but may have enabled discrimination between outcomes if vascular remodeling is a time dependent event. Nevertheless, future studies are needed to better elucidate the important and complex relationship between length of device support and posttransplant outcomes. Finally, although our regression model demonstrated moderate discrimination, significant variability remains unexplained. We Fig 2. Unadjusted posttransplant graft survival over time among pulsatile flow patients, 2001 to 2004 (solid line) and 2005 to 2008 (dashed line). Fig 3. Unadjusted posttransplant graft survival overtime among continuous flow patients, 2001 to 2004 (solid line) and 2005 to 2008 (dashed line).
8 1906 HONG ET AL Ann Thorac Surg LVAD AND POSTTRANSPLANT SURVIVAL 2011;91: speculate that some of the variability stems from differences in patient functional status, severity of illness, and technical aspects of the implant procedures that were not captured by the UNOS dataset. As a result, differences among the PULS, CONT, and INO groups may, at least in part, reflect differences in the recipients and not inherent differences related to the devices types. In conclusion, compared with recipients bridged with inotropes, posttransplant graft survival at 90 days did not differ for recipients bridged with either continuous-flow or pulsatile-flow devices. Likewise, posttransplant graft survival at other time points did not differ. However, in-hospital morbidity was greater for the CONT and PULS groups than for the INO group. Outcomes among the CONT group improved significantly from the first half to the second half of the study. Additional studies, including longer-term follow-up, are needed to determine whether differences exist in long-term survival and transplant-related complications. We thank the United Network for Organ Sharing (UNOS) for supplying the data and Jennifer Wainright and Katarina Linden for assistance with our analysis. This work was supported in part by Health Resources and Services contract and the National Institutes of Health training grant 5T32HL (Dr Iribarne, Dr Yang). The views expressed in this article are those of the authors alone and do not necessarily reflect the views or policies of the Department of Health and Human Services or the National Institutes of Health, nor does the mention of trade names, commercial products, or organizations imply endorsement by the United States Government. References 1. 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: Eisen HJ, Hankins SR. Continuous flow rotary left ventricular assist device: mechanical circulatory support 2.0. J Am Coll Cardiol 2009;54: Slaughter MS, Rogers JG, Milano CA, et al. Advanced heart failure treated with continuous-flow left ventricular assist device. N Engl J Med 2009;361: Pagani FD, Miller LW, Russell SD. Extended mechanical circulatory support with a continuous-flow rotary left ventricular assist device. J Am Coll Cardiol 2009;54: Aaronson K, Slaughter M, McGee E, et al. Evaluation of the HeartWare HVAD left ventricular assist system for the treatment of advanced heart failure: results of the ADVANCE bridge to transplant trial. Presented at the American Heart Association Scientific Session; Nov 13 17, 2010; Dallas, TX. 6. Klotz S, Stypmann J, Welp H, et al. Does continuous flow left biventricular assist device technology have a positive impact on outcome pretransplant and post transplant. Ann Thorac Surg 2006;82: Garatti A, Bruschi G, Colombo T, et al. Clinical outcome and bridge to transplant rate of left ventricular assist device recipient patients; comparison between continuous-flow and pulsatile flow devices. Eur J Cardiothorac Surg 2008;34: Stewart AS, Russo MJ, Martens TP, et al. Longer duration of continuous-flow ventricular assist device support predicts greater hemodynamic compromise after return of pulsatility. J Thorac Cardiovasc Surg 2008;136: Jett GK. Physiology of nonpulsatile circulation: acute versus chronic support. ASAIO J 1999;45: Nishimura T, Tatsumi E, Nishinaka T, et al. Diminished vasoconstrictive function caused by long-term nonpulsatile left heart bypass. Artif Organs 1999;23: Westaby S, Bertoni GB, Clelland C, et al. Circulatory support with attenuated pulse pressures alters human aortic wall morphology. J Thorac Cardiovasc Surg 2007;133: Crow S, John R, Boyle A, et al. Gastrointestinal bleeding rates in recipients of nonpulsatile and pulsatile left ventricular assist devices. J Thorac Cardiovasc Surg2009;137: Klovaite J, Gustafsson F, Mortensen SA, Sander K, Nielsen LB. Severely impaired von Willebrand factor-dependent platelet aggregation in patients with a continuous-flow left ventricular assist device (HeartMate II). J Am Coll Cardiol 2009;53: Nishimura T, Tatsumi E, Taenaka Y, et al. Effects of longterm nonpulsatile left heart bypass on the mechanical properties of the aortic wall. ASAIO J 1999;45: Thohan V, Stestson SJ, Nagueh SF, et al. Cellular and hemodynamics responses of failing myocardium to continuous flow mechanical circulatory support using the De- Bakey-Noon left ventricular assist device: a comparative analysis with pulsatile-type devices. J Heart Lung Transplant 2005;24: Kihara S, Litwak KN, Nichols L, et al. Smooth muscle cell hypertrophy of renal cortex arteries with chronic continuous flow left ventricular assist. Ann Thorac Surg 2003;75: Iribarne A, Russo MJ, Moskowitz AJ, Ascheim DD, Brown LD, Gelijns AC. Assessing technological change in cardiothoracic surgery. Semin Thorac Cardiovasc Surg 2009;21: Schaffer JM, Allen JG, Weiss ES, et al. Infectious complications after pulsatile-flow and continuous-flow left ventricular assist device implantation. J Heart Lung Transplant 2011;30: Pak SW, Uriel N, Takayama H, et al. Prevalence of de novo aortic insufficiency during long-term support with left ventricular assist devices. J Heart Lung Transplant 2010;29: Slaughter MS, Pagani FD, Rogers JG, et al. Clinical management of continuous-flow left ventricular assist devices in advanced heart failure. J Heart Lung Transplant 2010; 29(Suppl):1 39.
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