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1 Long-Term Outcome of Renal Transplant Recipients in the United States After Coronary Revascularization Procedures Charles A. Herzog, MD; Jennie Z. Ma, PhD; Allan J. Collins, MD Background Retrospective studies in dialysis patients have reported increased survival after coronary artery bypass (CAB) compared with coronary artery stenting and PTCA. The purpose of this study was to compare the long-term outcome of renal transplant recipients after stent, PTCA, or CAB with or without internal mammary grafting (CAB [IMG ] or CAB [IMG ]). Methods and Results Renal transplant recipients hospitalized from 1995 to 1999 for first coronary revascularization procedure were retrospectively identified from the United States Renal Data System database. Event-free survival for the end points of all-cause death, cardiac death, acute myocardial infarction (AMI), and the combined end point of cardiac death or AMI was estimated by the life-table method. The impact of independent predictors on survival was examined in a comorbidity-adjusted Cox model. In-hospital mortality rate was 2.3% for 909 stent patients, 4.3% for 652 PTCA patients, 9.4% for 288 CAB (IMG ) patients, and 5.0% for 812 CAB (IMG ) patients. Two-year all-cause survival ( SE) was: stent, %; PTCA, %; CAB (IMG ), %; and CAB (IMG ), %. The relative risks of all-cause and cardiac death were not significantly different among revascularization groups. The relative risk of cardiac death or AMI (versus PTCA) was 0.90 (95% CI, 0.69 to 1.17) for stent, 0.80 (95% CI, 0.55 to 1.17) for CAB (IMG ), and 0.57 (95% CI, 0.42 to 0.76) for CAB (IMG ). Conclusions Renal transplant recipients in the United States have comparable long-term survival after percutaneous and surgical coronary revascularization procedures. The most favorable long-term outcome occurs after surgical coronary revascularization. (Circulation. 2004;109: ) Key Words: angioplasty bypass kidney stents survival Patients with end-stage renal disease (ESRD) are at high risk for all-cause and cardiac death. The death rate for US dialysis patients from 1997 to 1999 was 239 per 1000 patient-years, and cardiac disease accounted for 44% of all-cause death. 1 Dialysis patients with ischemic heart disease have adverse outcomes after acute myocardial infarction (AMI) 2 and coronary revascularization procedures 3 ; their survival rate is better after surgical rather than percutaneous coronary revascularization. 3 5 In 2000, there were approximately renal transplant recipients (and dialysis patients) in the United States. 6 The risk of death is considerably less for patients with ESRD with functioning kidney transplants than for dialysis patients. From 1997 to 1999, the death rate for US renal transplant recipients was 34 per 1000 patient-years, and 41% of categorized deaths were attributed to cardiac causes. 1 Compared with dialysis patients, renal transplant recipients have lower mortality rates after AMI, with a 2-year mortality rate of 30% versus a 2-year mortality rate of 73% for dialysis patients. 2 There are few data on the long-term survival of renal transplant recipients after coronary revascularization procedures. There are no published data on outcome after coronary stent placement or on the comparative long-term survival of renal transplant recipients undergoing coronary revascularization with coronary artery bypass (CAB) surgery versus PCI. Published data on survival after CAB surgery or percutaneous coronary intervention are limited to reports in small numbers of patients Also, the impact of internal mammary grafting with survival after CAB surgery in these patients is unknown. The purpose of the present study was to compare the long-term survival of renal transplant recipients in the United States after coronary artery stenting, PTCA, or CAB surgery. Methods All data were derived from the United States Renal Data System (USRDS) database. The accuracy of these data has been validated. 21 We retrospectively analyzed outcomes in 2661 renal transplant Received January 3, 2003; de novo received December 12, 2003; revision received February 17, 2004; accepted February 18, From the Cardiovascular Special Studies Center, United States Renal Data System, Minneapolis, Minn (C.A.H., J.Z.M., A.J.C.); the Department of Psychiatry and Center for Epidemiology and Biostatistics, University of Texas, San Antonio (J.Z.M.); and the Divisions of Cardiology (C.A.H.) and Nephrology (A.J.C.), Department of Internal Medicine, Hennepin County Medical Center and University of Minnesota, Minneapolis. The data reported here have been supplied by the United States Renal Data System. The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as an official policy or interpretation of the US government. Correspondence to Charles A. Herzog, MD, United States Renal Data System, 914 South 8th Street, Suite D-206, Minneapolis, MN [email protected] 2004 American Heart Association, Inc. Circulation is available at DOI: /01.CIR
2 Herzog et al Renal Transplant After Coronary Revascularization 2867 recipients hospitalized for the first coronary revascularization procedure (excluding concomitant valvular surgery) occurring after initiation of renal replacement therapy from January 1995 to December 1999, with follow-up through June 30, (For example, a patient would meet the inclusion criteria if he or she received dialysis for 5 years and then had a functioning renal transplant for 2 years, during which time the first coronary revascularization procedure occurred; however, a patient would not meet the inclusion criteria if he or she had coronary revascularization as a dialysis patient and then had a second revascularization procedure as a renal transplant recipient.) Eligible patients underwent renal replacement therapy for at least 90 days and had a renal transplant for at least 60 days before revascularization. Patients were identified through the use of International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9- CM) codes for coronary artery stenting (36.06), PTCA (36.01, 36.02, 36.05), and CAB surgery (36.1X). The use of an internal mammary graft during CAB surgery was identified from ICD-9-CM codes and Patients identified as receiving both stent placement and PTCA were included in the stent group. Thirty patients who had surgical and percutaneous coronary revascularization procedures during the same hospitalization were excluded after a preliminary survival analysis indicated that their inclusion would have no significant effect on study results. Demographic data gathered included patient age, sex, race (Hispanic patients not identified separately), duration of prior ESRD, and primary renal diagnosis. The presence of comorbid conditions was determined by using a previously developed comorbidity profiling method based on the ICD-9-CM diagnosis and procedure codes in the Medicare Part A institutional inpatient claims. 22 Comorbid conditions were identified through the use of ICD-9-CM codes from hospitalizations that occurred before the revascularization procedure. Comorbid conditions included prior AMI, other atherosclerotic heart disease (ASHD), congestive heart failure, other cardiac conditions (including valvular heart disease, arrhythmia, and pacemaker implantation), prior coronary revascularization, nonskin malignancies, peripheral vascular disease, cerebrovascular ischemia (cerebrovascular accident and transient ischemic attack), chronic obstructive pulmonary disease, gastrointestinal disease, gallbladder disease, and liver disease. The USRDS database predominantly comprises claims data (with Medicare as the primary payer). Clinical data known to be of prognostic importance for survival, such as angiographic severity of coronary artery disease and left ventricular ejection fraction, are not available in the USRDS database. Survival time was calculated from the time of revascularization to censor or end point. Study end points were all-cause death, cardiac death, AMI, and the combined end point of cardiac death or AMI. The cause of death was determined from the ESRD Death Notification Form (Form CMS-2746-U3). Censoring occurred if a patient initiated dialysis for renal graft failure, had no event at end of study, or was lost to follow-up. Long-term survival was estimated by the life-table method. The log-rank test was used to compare the difference in cumulative survival between different groups. A Cox proportional hazards model was used to assess the impact of independent predictors on patient survival. Probability values in the Cox model were based on the Wald test statistic. All statistical analyses were performed with the use of the SAS system for Windows version 8 (SAS Institute). All reported P values are 2 sided. Results Of the approximately 1.1 million patients in the USRDS database for 1978 to 1999, we identified 5349 renal transplant recipients with a total of 6919 coronary revascularization procedures. After exclusion of patients with concurrent valvular surgery, those who had not had their renal transplant for at least 60 days, and those who did not have at least 90 days of prior ESRD claims, there were 4862 patients. From January 1, 1995, through December 31, 1999, 2691 patients were identified as undergoing a first (index) coronary revascularization procedure; excluded were 30 patients who received more than 1 type of revascularization procedure during the same hospitalization. In the 2661 renal transplant recipients studied, the coronary revascularization procedures were as follows: stent, 909; PTCA, 652; and CAB surgery, Of those having CAB surgery, 288 had CAB without internal mammary grafts (CAB [IMG ]), and 812 had CAB with internal mammary grafts (CAB [IMG ]). No stent, PTCA, or CAB patients were lost to follow-up. Table 1 summarizes the demographic data. All groups studied were similar in prior ESRD duration and time to revascularization after renal transplantation (number of years SD): stent, years and years; PTCA, years and years; CAB (IMG ), years and years; and CAB (IMG ), years and years. In CAB (IMG ) patients, 66% had a concurrent diagnosis of acute coronary syndrome (AMI [ICD-9-CM code 410] or intermediate syndrome [ICD-9-CM code 411]); in CAB (IMG ) patients, 69% had concurrent acute coronary syndrome. The mean follow-up time after coronary revascularization was as follows (number of months SD [25th to 75th percentile range]): stent, months (10.7 to 30.5 months); PTCA, months (15.0 to 49.2 months); CAB (IMG ), months (6.8 to 43.5 months); and CAB (IMG ), months (11.6 to 39.3 months). Deaths during follow-up were as follows: stent, 154; PTCA, 174; CAB (IMG ), 76; and CAB (IMG ), 183. In-hospital deaths occurred in each group: stent, 21 (2.3%); PTCA, 28 (4.3%); CAB (IMG ), 27 (9.4%); and CAB (IMG ), 41 (5.0%). Stent patients died in the hospital of these causes: AMI, 6; cardiac arrest or arrhythmia, 3; sepsis, 1; other causes, 2; and unknown, 9. Patients with PTCA died of: AMI, 11; cardiac arrest or arrhythmia, 2; other causes, 1; and unknown, 14. CAB (IMG ) patients died of: AMI, 2; ASHD or cardiomyopathy, 3; sepsis, 3; other causes, 4; and unknown, 15. CAB (IMG ) patients died of: AMI, 4; ASHD, 2; cardiac arrest, 1; sepsis, 3; other causes, 2; and unknown, 29. Table 2 presents event-free survival for each group. As shown in Figure 1, there was no statistically significant difference in survival related to type of coronary revascularization; however, a trend toward increased mortality rates was observed in CAB (IMG ) patients. There was no difference in cardiac survival. As shown in Figure 2, CAB patients, particularly CAB (IMG ) patients, were less likely than other patients to reach the combined end point of cardiac death or AMI. This more favorable outcome after surgery appears to be predominantly attributable to a reduced risk of AMI. The effects of independent predictors of overall mortality rates were examined with use of the Cox proportional hazards model. Results are shown in Table 3. The most powerful predictors of death were older age ( 75 years) (relative risk [RR], 2.10; 95% CI, 1.19 to 3.70), diabetic ESRD (RR, 1.72; 95% CI, 1.42 to 2.08), congestive heart failure (RR, 1.59; 95% CI, 1.33 to 1.89), and other cardiac disorders, excepting other ASHD and prior AMI (RR, 1.56; 95% CI, 1.30 to 1.85). Both cerebrovascular and peripheral vascular diseases were associated with a 31% increased risk of death. Other ASHD
3 2868 Circulation June 15, 2004 TABLE 1. Patient Demographics Stent (n 909) PTCA (n 652) CAB (IMG ) (n 288) CAB (IMG ) (n 812) P Age, y (21) 150 (23) 44 (15) 187 (23) (58) 383 (59) 170 (59) 480 (59) (19) 109 (17) 67 (23) 137 (17) (2) 10 (2) 7 (2) 8 (1) Sex Male 623 (69) 441 (68) 200 (69) 581 (72) 0.39 Female 286 (31) 211 (32) 88 (31) 231 (28) Race White 746 (82) 531 (81) 234 (81) 704 (87) 0.07 Black 124 (14) 95 (15) 39 (14) 75 (9) Native American 14 (2) 5 (1) 3 (1) 10 (1) Other 25 (3) 21 (3) 12 (4) 23 (3) ESRD pathogenesis Diabetes 277 (30) 225 (35) 78 (27) 324 (40) Hypertension 137 (15) 109 (17) 60 (21) 109 (13) Other 495 (54) 318 (49) 150 (52) 379 (47) Values are n (%). Because of rounding, not all percentages add to 100. was paradoxically associated with a 46% reduced death risk. Race and sex were not associated with increased death risk. With PTCA patients as the reference group, stent, CAB (IMG ), and CAB (IMG ) were not associated with different all-cause survival. There was also no difference in the Cox model for predictors of cardiac death by revascularization procedure. Compared with PTCA, the cardiac death RRs were as follows: stent, 1.29 (95% CI, 0.82 to 2.02); CAB (IMG ), 0.74 (95% CI, 0.45 to 1.21); and CAB (IMG ), 0.87 (95% CI, 0.47 to 1.63). There were significant differences in the Cox models examining the effects of independent predictors for the likelihood of the combined end point of cardiac death or AMI and for AMI alone. With PTCA patients as the reference group, there was no significant difference after stent (RR, 0.90; 95% CI, 0.69 to 1.17) or CAB (IMG ) (RR, 0.80; 95% CI, 0.55 to 1.17) for the combined end point of cardiac death or AMI. In contrast, CAB (IMG ) patients had a 43% reduction in the risk of cardiac death or AMI (RR, 0.57; 95% CI, 0.42 to 0.76). Similarly, compared with PTCA, the risk of AMI was not different after stent (RR, 0.76; 95% CI, 0.56 to 1.04) or CAB (IMG ) (RR, 0.73; 95% CI, 0.47 to 1.15). There was a 48% reduction in AMI risk after CAB (IMG ) (RR, 0.52; 95% CI, 0.37 to 0.73). However, when the Cox TABLE 2. Event-Free Survival (%) After Coronary Revascularization Event Year Type of Revascularization All-Cause Death Cardiac Death AMI Cardiac Death or AMI 1 Stent PTCA CAB (IMG ) CAB (IMG ) Stent PTCA CAB (IMG ) CAB (IMG ) Stent PTCA CAB (IMG ) CAB (IMG ) All data are mean SE.
4 Herzog et al Renal Transplant After Coronary Revascularization 2869 Figure 1. Survival by type of coronary revascularization. All data are SE. model was constructed by using CAB (IMG ) patients (rather than PTCA patients) as the reference group, the previously noted advantage for CAB (IMG ) patients (relative to PTCA patients) diminished: CAB (IMG ) patients had an advantage that was of only borderline significance relative to CAB (IMG ) patients (RR, 0.72; 95% CI, 0.49 to 1.06; P 0.10) for cardiac death or AMI. The risk of all-cause and cardiac death also was analyzed in a Cox model by diabetic status; the impact on survival related to revascularization procedure did not differ from the findings noted for the entire study group. The risk of all-cause death also was analyzed in a Cox model that adjusted for duration of renal transplant before revascularization; the impact of this variable was not significant. Finally, we also constructed a Cox model to assess the additional potential impact of multivessel revascularization procedures; there was no significant difference for the risk of all-cause death. Discussion We have previously reported a survival advantage in dialysis patients undergoing surgical compared with percutaneous coronary revascularization. 3,5 In the present study of renal transplant recipients (without prior coronary revascularization), we found no difference in long-term survival related to type of coronary revascularization. Our findings confirm the importance of internal mammary graft utilization in patients undergoing CAB surgery, 23 as the 812 patients in this group had a 43% reduction in the risk of cardiac death or AMI. Moreover, the 288 patients who had CAB surgery without internal mammary grafting had a nearly 2-fold greater inhospital mortality rate than the patients who received internal mammary grafts. Our data suggest that CAB surgery may offer a slight advantage, as there is a relative reduction in the long-term risk of the combined end point of cardiac death or AMI (which appears attributable to a lowered risk of AMI; a Figure 2. Likelihood of cardiac death or AMI by type of coronary revascularization.
5 2870 Circulation June 15, 2004 TABLE 3. Cox Model: Independent Predictors of All-Cause Death Factor RR (95% CI) P Age, y (1.09, 1.75) (1.34, 2.36) (1.19, 3.70) Sex Female 1.14 (0.96, 1.36) 0.15 Race Native American 0.69 (0.28, 1.66) 0.41 Black 1.24 (0.98, 1.57) Other 1.05 (0.63, 1.73) 0.86 Prior ESRD duration, y (0.81, 44.4) (0.55, 28.3) (0.91, 45.9) 0.06 ESRD pathogenesis Diabetes 1.72 (1.42, 2.08) Hypertension 1.03 (0.80, 1.32) 0.82 Comorbidity AMI 1.10 (0.93, 1.31) 0.26 Other ASHD 0.54 (0.42, 0.69) Congestive heart failure 1.59 (1.33, 1.89) Other cardiac disorder 1.56 (1.30, 1.85) Cancer 1.34 (1.04, 1.73) COPD 1.23 (0.98, 1.54) CVA/TIA 1.31 (1.05, 1.62) Peripheral vascular disease 1.31 (1.10, 1.55) Gastrointestinal disease 1.36 (1.11, 1.67) Liver disease 1.18 (0.83, 1.67) 0.37 Gallbladder disease 1.20 (0.95, 1.53) 0.13 Prior coronary revascularization 0.89 (0.66, 1.20) 0.46 Type of revascularization Stent 0.96 (0.77, 1.20) 0.74 PTCA 1.00 (reference) CAB (IMG ) 1.13 (0.85, 1.48) 0.40 CAB (IMG ) 0.96 (0.77, 1.19) 0.68 COPD indicates chronic obstructive pulmonary disease; CVA/TIA, cerebrovascular accident/transient ischemic attack. Reference group: age 45 years, male, white, ESRD duration 1 y, other cause of ESRD, no comorbidity, no prior coronary revascularization or PTCA. trend toward improved outcome was observed in patients receiving internal mammary grafts). This finding is reminiscent of data reported in the 7-year Bypass Angioplasty Revascularization Investigation (BARI) study follow-up with regard to the reduction in long-term risk for Q-wave myocardial infarction in diabetics after CAB surgery as opposed to PTCA. 24 In renal transplant recipients, however, the risk of AMI is reduced after CAB surgery in all patients, irrespective of diabetic status. A paradoxical finding in our study is the relative survival advantage (46% reduction in death risk) present in patients with the comorbid condition of other ASHD. The identification and diagnosis of other ASHD may be associated with other medical therapy (eg, use of -blockers) that favorably affects long-term survival. Because the USRDS database contains few data on medication use, we could not analyze this finding in greater detail. The survival data reported in the present study are consistent with those given in previous reports from small singlecenter series. Dresler et al 17 reported on 31 renal transplant recipients having CAB surgery after renal transplantation; the 30-day mortality rate was 3%. The aggregate 1-year survival of 45 patients (31 with CAB surgery, 14 with valvular surgery) was 88% (only 1 death in the CAB surgery group). The largest clinical series was described by Ferguson et al. 20 They summarized a 25-year, single-institution experience. A total of 83 renal transplant recipients had coronary revascularization performed before or after transplantation. Only 45 of 83 patients were revascularized after renal transplantation (32 CAB, 13 PTCA). The small sample size precludes any meaningful comparison of CAB surgery with PTCA in terms of outcome; the authors reported a combined estimated survival for the 45 patients of 93.3% at 1 year, 77.8% at 3 years, and 59.5% at 5 years. In long-term follow-up, 48% of deaths were due to cardiac causes. We believe that the major significance of the present study of 2661 patients is that it provides a national benchmark for outcome after coronary revascularization procedures in renal transplant recipients. Importantly, we have shown that these patients do not share the relatively poor outcome reported for dialysis patients. In the present study, the estimated 2-year all-cause survival of renal transplant recipients after coronary revascularization (except for CAB[IMG ] patients) was 82%, compared with 57% after CAB surgery and 53% after PTCA in dialysis patients, as we found in a previous study. 3 Thus, it should not be assumed that all patients with ESRD have common cardiovascular fates, particularly after coronary revascularization. Although some of the relative survival advantage in renal transplant recipients (compared with dialysis patients) probably is due to the selection of healthier patients with ESRD for transplantation, our preliminary data showing improved post-ami survival of renal transplant recipients (compared with transplant wait-list patients) support the concept of an intrinsic survival advantage of renal transplant recipients with cardiovascular disease, compared with dialysis patients. 25 Our study has several limitations. The USRDS database includes few clinical data. Potentially important prognostic factors such as left ventricular ejection fraction, severity of coronary artery disease (including left main coronary artery disease), vessel size, and coronary lesion characteristics are not identified in the USRDS database. The exclusion of these variables might result in our failure to detect a difference in outcome related to type of revascularization. The survival analysis in this study is based on a retrospective design, and selection bias for choice of revascularization procedure could have confounded our findings. Our study also ignores the potentially favorable impact on survival of pharmacological agents used during percutaneous coronary intervention (such as GP IIb/IIIa platelet inhibitors). Our study does not address the survival of renal transplant recipients with ischemic heart
6 Herzog et al Renal Transplant After Coronary Revascularization 2871 disease receiving medical therapy alone without coronary revascularization. Finally, it is likely that we have underestimated the proportion of deaths from cardiac causes. In the USRDS database, the death rate for all renal transplant recipients 45 to 64 years of age in 1997 to 1999 was 43.1 per 1000 patient-years at risk, with 25.7 and 2.3 deaths per 1000 patient-years attributed to other causes and unknown causes, respectively. As we note in the Results section, the largest attributable cause of in-hospital death in the present study was unknown. However, this underestimate of the proportion of all-cause deaths from cardiac causes is unlikely to alter the conclusions of our study. We conclude that renal transplant recipients have comparable long-term survival after surgical and percutaneous coronary revascularization procedures. Our data suggest that the most favorable long-term outcome (after adjustment for comorbid conditions) is associated with CAB surgery. Any definitive conclusion about the overall superiority of a particular coronary revascularization procedure, however, would require a prospective, randomized clinical trial. Despite the burden of cardiovascular disease in patients with ESRD, renal transplant recipients (compared with dialysis patients) have relatively favorable outcomes after coronary revascularization procedures. Acknowledgments The Cardiovascular Special Studies Center of the USRDS is supported by contract No. N01-DK (National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland). References 1. US Renal Data System. USRDS 2001 Annual Data Report. National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; Herzog CA, Ma JZ, Collins AJ. Poor long-term survival after acute myocardial infarction among patients on long-term dialysis. N Engl J Med. 1998;339: Herzog CA, Ma JZ, Collins AJ. Long-term outcome of dialysis patients in the United States with coronary revascularization procedures. Kidney Int. 1999;56: Szczech LA, Reddan DN, Owen WF, et al. Differential survival after coronary revascularization procedures among patients with renal insufficiency. Kidney Int. 2001;60: Herzog CA, Ma JZ, Collins AJ. Comparative survival of dialysis patients in the United States after coronary angioplasty, coronary artery stenting, and coronary artery bypass surgery and impact of diabetes. Circulation. 2002;106: US Renal Data System. USRDS 2002 Annual Data Report. National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; Nakhjavan FK, Kahn D, Rosenbaum J, et al. Aortocoronary vein graft surgery in a cadaver kidney transplant recipient. Arch Intern Med. 1975; 135: Beauchamp GD, Sharma JN, Crouch T, et al. Coronary bypass surgery after renal transplantation. Am J Cardiol. 1976;37: Christiansen S, Splittgerber FH, Marggraf G, et al. Results of cardiac operations in five kidney transplant patients. Thorac Cardiovasc Surg. 1997;45: Golan M, Goor DA, Jacob ET. Coronary artery bypass surgery in a cadaver kidney transplant recipient. Int Surg. 1987;72: Lamberti JJ, Cohn LH, Collins JJ Jr. Cardiac surgery in patients undergoing renal dialysis or transplantation. Ann Thorac Surg. 1975;19: Menzoian JO, Davis RC, Idelson BA, et al. Coronary artery by-pass surgery and renal transplantation: a case report. Ann Surg. 1974;179: Stewart R, Sethia B, Bain WH. Cardiac surgery in patients with functional renal transplants. Thorac Cardiovasc Surg. 1986;34: Bolman RM III, Anderson RW, Molina JE, et al. Cardiac operations in patients with functioning renal allografts. J Thorac Cardiovasc Surg. 1984;88: Defraigne JO, Meurisse M, Limet R. Valvular and coronary surgery in renal transplant patients. J Cardiovasc Surg (Torino). 1990;31: DeMeyer M, Wynns W, Dion R, et al. Myocardial revascularization in patients on renal replacement therapy. Clin Nephrol. 1991;36: Dresler C, Uthoff K, Wahlers T, et al. Open heart operations after renal transplantation. Ann Thorac Surg. 1997;63: Kobayashi Y, Fukushima N, Ohtake S, et al. Cardiac surgery in renal transplant recipients. Transplant Proc. 1998;30: Sezgin A, Mercan S, Tasdelen A, et al. Coronary bypass surgery in renal transplantation patients. Transplant Proc. 1998;30: Ferguson ER, Hudson SL, Diethelm AG, et al. Outcome after myocardial revascularization and renal transplantation: a 25-year single-institution experience. Ann Surg. 1999;230: US Renal Data System. USRDS 1992 Annual Data Report. Bethesda, Md: The National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; Collins AJ, Ma J, Constantini E, et al. Dialysis unit and patient characteristics associated with reuse practices and mortality: JAm Soc Nephrol. 1998;9: Leavitt BJ, O Connor GT, Olmstead EM, et al. Use of the internal mammary artery graft and in-hospital mortality and other adverse outcomes associated with coronary artery bypass surgery. Circulation. 2001;103: Seven-year outcome in the Bypass Angioplasty Revascularization Investigation (BARI) by treatment and diabetic status. J Am Coll Cardiol. 2000;35: Herzog CA, Ma JZ, Collins AC. Do renal transplant recipients really have a better survival after acute myocardial infarction than dialysis patients? J Am Soc Nephrol. 2001;12:933A. Abstract.
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