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Ann Thorac Surg 1997;64:1270-1278
© 1997 The Society of Thoracic Surgeons
Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania
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Abstract |
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Methods. Sixty-four patients underwent 66 cardiac procedures broken down as follows: coronary artery bypass grafting, 30; single or combined valve replacement-repair, 24; combined coronary artery bypass grafting and valve repair, 3; aortic repair, 4; pericardiectomy, 3; transmyocardial laser revascularization, 1; and native cardiectomy, 1. Patients consisted of 40 kidney, 16 liver, 5 heart, 2 lung, and 1 liver and kidney transplant recipients. The mean interval from the time of transplantion to the cardiac operation was 53 months (range, 1 day to 220 months). Forty-six male and 18 female patients in New York Heart Association functional class III or IV had a mean age of 53 years (range, 19 to 77 years); 50% (32/64) were diabetic, and 97% (62/64) were hypertensive. Immunosuppressive therapy, cardiopulmonary bypass, and medical management were similar in all patients.
Results. There were two (3%) perioperative deaths, one of which was caused by an arrhythmia-induced cardiac arrest, and there were seven (11%) late deaths from non–cardiac-related causes. Major complications included 12 infections (19%), ten mediastinal reexplorations for the control of bleeding (16%), and nine others (15%). Sixteen of the 64 (25%) transplant recipients had chronic renal failure (serum creatinine levels, >3 mg/dL), including 13 of 40 (33%) kidney transplant patients. Acute renal failure developed postoperatively in 7 (54%) of these 13 patients; the grafts failed permanently in 3 (23%). Three patients (5%), 2 kidney transplant recipients and 1 lung transplant recipient, experienced transient acute rejection. Fifty of the 55 surviving patients are alive and well (New York Heart Association functional class I or II) without recurrent cardiac disease at a mean follow-up period of 22 months.
Conclusions. Although the short-term morbidity was significant, the low mortality and low incidence of permanent graft dysfunction indicate that solid organ transplant recipients can safely and effectively undergo subsequent cardiac surgical procedures.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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The remarkable advances in solid organ transplantation over the past decade resulting from improvements in the patient selection, technical refinements, immunosuppressive protocols, and postoperative management have resulted in an ever-increasing pool of older patients. Since 1986, 602 heart, 316 lung, 4,347 liver, and 2,323 kidney transplantations have been performed at the University of Pittsburgh. The average age of recipients at the time of transplantation was 41 years; it is 48 years in current survivors. As the population of transplantation survivors has aged and the number of patients has increased, the pool of recipients in whom symptomatic cardiovascular disease develops has risen. The first reported case of a cardiac operation performed on an organ transplantation survivor was that of Menzoian and colleagues, published in 1974 [1]. Since that time, there have been numerous case reports and small series supporting the performance of cardiac operations in solid organ transplant recipients [2–5]. There remain, however, neither uniform guidelines nor a comprehensive assessment of the management issues that must be considered when approaching these unique patients.
The management of cardiopulmonary bypass (CPB), immunosuppressive therapy, antibiotic prophylaxis, and the administration of particular medications are poorly defined in these patients. Additionally, outcome measures such as length of stay; the incidence of graft loss, renal dysfunction, major infectious and bleeding complications, and rejection; and overall mortality are not well documented.
We report our experience with the management techniques and the subsequent outcomes of cardiac operations in a large series of solid organ transplant recipients with functioning allografts. We additionally sought to assess the role of specific transplant allografts as risk factors for major complications and mortality. We excluded patients who were on active hemodialysis or peritoneal dialysis, as well as those who underwent a concurrent cardiac procedure and organ transplantation.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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). There were 46 male and 18 female patients whose mean age was 53 years (range, 19 to 77 years). Twenty-eight of the 64 (44%) patients were insulin-dependent diabetics, 4 of 64 (6%) were non–insulin-dependent diabetics, and all but 2 (97%) had hypertension. The patients consisted of 40 kidney, 17 liver (including one liver-kidney), 5 heart, and 2 lung transplant recipients. The mean interval from the date of transplantation to the cardiac operation was 53 months (range, 1 day to 220 months). Sixty-six cardiac operations were performed in these 64 patients, as outlined in Table 2.
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Immunosuppressive Regimen
The maintenance immunosuppressive regimen consisted of oral cyclosporine (CsA) (6 mg • kg-1 • day-1; range, 400 to 900 mg/day) or tacrolimus (0.30 mg • kg-1 • day-1, range, 2 to 20 mg/day), azathioprine (Imuran) (2 mg • kg-1 • day-1; range, 100 to 250 mg/day), and prednisone (15 to 20 mg/day). Serum CsA levels approximated 1,000 ng/mL (polyclonal immunoassay, TDX; Abbott Laboratory, Abbott Park, IL), and serum tacrolimus levels were maintained at approximately 1.0 ng/mL (enzyme-linked immunosorbent assay). The normal oral immunosuppressive medications were administered the morning of the operation in all transplant patients undergoing cardiac operations. The dose the day after operation was administered orally if the patient was extubated or by nasogastric tube if the patient continued to be ventilated. Stress doses of steroids were initiated at the time of operation, and this consisted of hydrocortisone (100 mg intravenously [IV] every 8 hours for 24 hours) or methylprednisolone (Solumedrol; The Upjohn Company, Kalamazoo, MI; 25 mg IV every 6 hours for 24 hours). Serum drug levels of CsA or tacrolimus were monitored in the perioperative period as a routine measure. If the levels were noted to be abnormally low, the dose was supplemented IV. If the drug levels were elevated, the immunosuppressive drug was withheld or the dose reduced until the levels returned to baseline. Likewise, if acute allograft failure was suspected on the basis of a decreasing urine output or an increasing serum creatinine level, the dose of the immunosuppressive drug was reduced.
Prophylaxis Against Infection
Fifty-five of the 64 patients (86%) were given broad-spectrum antibiotics prophylactically before operation, and these consisted of 1 g of vancomycin IV and 1 g of ceftriaxone (Rocephin; Roche Laboratories, Nutley, NJ) IV. Seven of 64 (11%) received 1 g of cefamandole (Mandol; Eli Lilly and Co, Indianapolis, IN) IV, and 2 of 64 patients (3%) with significant documented penicillin allergies and normal renal function were given 1 g of vancomycin with 1 to 1.5 mg/kg of gentamycin IV.
Surgical Management
Routine cardiac narcotic anesthesia and standard CPB techniques were used in all patients. High-flow CPB at a rate of 2 to 4 L • min-1 • m-2, adjusted for the calculated body surface area and mixed venous oxygen saturations, with cooling to 32°C, was maintained. Cold blood potassium cardioplegia was administered in all patients, as is the routine practice at this institution. Activated clotting times were maintained between 500 and 600 seconds for the kidney and thoracic organ transplant patients and 400 and 500 seconds for the liver transplant recipients. In all groups the perfusion pressures were maintained in the 60 to 90 mm Hg range and vasoconstrictive drugs were not used if possible. Postoperatively, inotropic drugs were administered as needed, and dopamine (3 to 5 µg • kg-1 • min-1 IV) was routinely given to kidney transplant recipients to maximize renal perfusion. Mannitol (25 g) and furosemide (20 to 40 mg) were administered IV at the conclusion of the operation in renal transplant recipients to encourage allograft diuresis. No hemostatic adjuncts, such as aminocaproic acid or aprotinin, were routinely used, because many of these patients had marginal renal function that might have been exacerbated by the use of these agents.
Medical Management
The medical management of these patients was relatively uniform throughout the perioperative period. An effort was made to minimize alterations in the patient's routine preoperative medications. If possible, medications were administered orally the morning of operation and again orally or through nasogastric tubes the morning after operation. In the immediate postoperative period, normal blood pressure and cardiac outputs were supported with dopamine and dobutamine. Hypertension was treated with IV nitroprusside or nitroglycerin to achieve mean arterial blood pressures in the target range. Close attention was paid to the intravascular volume status to maintain hydration during the perioperative period. Furosemide or bumetinide was administered judiciously as a bolus or continuous infusion to maintain a urine output of 0.5 to 1.5 mg • kg-1 • h-1, yet ensure adequate hydration and graft perfusion. Certain medications were avoided in the perioperative period, such as nonsteroidal antiinflammatory drugs (eg, ibuprofen) and captopril or other nephrotoxic or hepatotoxic medications.
Monitoring of Allograft Function and Rejection
Preoperative laboratory values that were monitored included the hematocrit, total white blood cell count with differential leukocyte and platelet count, the prothrombin time, electrolyte levels with blood urea nitrogen, and the creatinine level. Additionally, liver function tests were performed in liver transplant recipients. Laboratory values were determined again, at a minimum, on postoperative day 1 and before discharge. Fluid intake, urine output, and renal function were closely monitored in all patients. Suspected episodes of graft rejection were addressed by immediate biopsy and histologic analysis, followed by pulse steroids with 1 g of methylprednisolone IV daily for 3 days if rejection was proved by biopsy findings or strongly suspected clinically.
Length of Stay
Length of stay was assessed by evaluating both intensive care unit length of stay and total length of stay. Notably, the recent advent of clinical pathways have promoted a shorter total length of stay.
Statistical Analysis
The 
2 (contingency table) test (Statistica Software; 1993 Statsoft Inc., Tulsa, OK) was used to determine significant differences in outcomes between groups.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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Seven (11%) late deaths occurred from 7 weeks to 26 months after the cardiac operations. None was attributable to the procedure or directly related to a cardiac cause. Six late deaths occurred in kidney transplant recipients (Table 3). There was one late death in a liver transplant patient 19 months after an aortic valve replacement. The cause was sepsis and multisystem organ failure. Actuarial survival at a mean follow-up of 22 months is shown in Figure 1.
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). Coronary artery bypass grafting had been performed in 3 of these 7 patients, emergent aortic procedures in 2, and valve replacements in 2. The other 6 patients (46%) had uneventful postoperative courses and were discharged with creatinine levels similar to preoperative levels. Of the 7 patients who had acute renal failure postoperatively, 4 improved with dialysis by the time of discharge and required no further treatment, whereas the remaining 3 patients had permanent allograft loss (Table 5). Of these 3 patients, 2 had undergone CABG and 1 valve replacement electively. This cohort represents 23% (3/13) of the chronic renal allograft failure patients, 7.5% (3/40) of the total kidney transplant population, and 4.7% (3/64) of the total study group. Two of these 3 patients suffered late-term deaths from sepsis. All had perioperative immunosuppressive drug levels within the therapeutic range.
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There were two (5%) episodes of biopsy-proven rejection in kidney recipients (see Table 5
). One patient with chronic renal failure (serum creatinine, 3.2 mg/dL) underwent an emergency repair of an ascending aortic dissection, and rejection developed 5 weeks postoperatively. He was 1 of the 7 in whom acute graft failure developed but whose graft function improved with hemodialysis. This patient's immunosuppressive drug dose was reduced postoperatively because of his acute renal failure. The other was a patient with a baseline creatinine concentration of 3 mg/dL who initially tolerated an aortic valve replacement but in whom rejection developed 2 weeks later. However, acute tubular necrosis developed in this patient postoperatively that was effectively treated medically (including a reduction in the immunosuppressive drug dose), but the patient had a creatinine level of 3.4 mg/dL at the time of discharge. Both patients who suffered rejection were treated with pulsed doses of steroids, as previously described, with neither resulting in permanent graft loss.
The only other case of acute allograft rejection occurred in a lung transplant recipient who underwent a pericardiectomy for tamponade 1 day after a single left lung transplantation. Acute rejection, documented radiographically and by biopsy findings, developed 11 days later, and he was effectively treated with a 3-day course of methylprednisolone.
Renal Function
The preoperative and postoperative blood urea nitrogen and serum creatinine levels were stratified by the type of organ transplanted: kidney, liver (including one combined liver-kidney transplant recipient), and thoracic organ (Table 6). There were no statistically significant alterations observed in the preoperative and postoperative mean serum creatinine levels in any group (Fig 2), although there were minor fluctuations in the blood urea nitrogen and creatinine levels of individual patients within each transplant group, as shown in Table 6. The renal group includes the 7 patients who suffered graft failure and required hemodialysis. No patient aside from these 7 required hemodialysis regardless of fluctuations in the serum creatinine levels.
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Infectious Complications
Twelve major infections (19%) were documented, including 3 cases (5%) of mediastinitis (one long-term fatality); 2 were caused by Staphylococcus aureus and 1 by multiple organisms. Four cases (6%) of sepsis occurred, 1 each with cytomegalovirus, Candida albicans, Pseudomonas aeruginosa (short-term fatality), and Saureus. Five cases (8%) of pneumonia were effectively treated. Overall, there were ten major infections in 8 kidney recipients, one in 1 liver recipient, and one in 1 thoracic organ recipient (Table 7).
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Other Complications
Ten patients (16%) required reexploration for mediastinal hematoma with resultant tamponade postoperatively. There was 1 documented case of an intraoperative coagulopathy in a liver transplant recipient that was treated medically. Blood or clotting factor transfusion in the intraoperative or postoperative period was not considered excessive or unusual in any case. There were no significant alterations in the measured prothrombin times in those patients who required reexploration, and the activated clotting times were adequately corrected after protamine was administered following CPB. Other major and minor complications are listed in Table 8. Overall, there were 14 major complications (including bleeding) in 13 kidney recipients, four in 4 liver recipients, and one in 1 thoracic organ recipient. There were 17 minor complications in 15 kidney recipients, 12 in 10 liver recipients, and one in 1 thoracic organ recipient. A total of 31 complications (major and minor) occurred in 22 kidney recipients, 16 in 12 liver recipients, and two in 1 thoracic organ recipient. In the total group of transplant patients, there was a 77% incidence of complications (49 cases) in 55% (35/64) of the patients.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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In our series, the early mortality of 3%, with only 1 of the 2 patients dying of cardiac-related cause, was consistent with the mortality associated with cardiac operations in the nontransplant population [12]. The late mortality of 11%, with no deaths resulting from a cardiac-related cause, is arguably consistent with a patient population having numerous comorbid medical conditions. The three late-term deaths resulting from sepsis and two resulting from metastatic cancers (renal and prostatic) may represent the unique causes of death that often afflict the transplant recipients receiving long-term immunosuppressive treatment. Notably, neither emergency procedures nor reoperations were observed to have a significant effect on outcome. The actuarial 2-year survival in these patients was 86% (see Fig 1). Similar survival statistics have been found in other limited series [6, 7, 13, 14].
Sixteen of the 64 (25%) transplant patients had chronic renal failure preoperatively (creatinine, >3 mg/dL). This included 13 of 40 (33%) kidney, 2 of 17 (12%) liver, and 1 of 7 (14%) thoracic organ transplant recipients. We observed an overall 5% incidence (n = 3) of permanent allograft loss, all in kidney transplant patients with chronic renal failure. Postoperative graft dysfunction requiring hemodialysis developed in an additional 4 patients in that subgroup of 13 patients. The underlying cause of chronic renal failure in kidney transplant recipients may be chronic rejection, whereas the underlying cause of chronic renal failure in liver and thoracic transplant recipients may be long-term immunosuppressive therapy. This basic difference may account for the high failure rate in the kidney transplant population. It is also notable that no patient with a creatinine level of less than 3 mg/dL preoperatively suffered progressive graft failure. It is reasonable to conclude that renal transplant recipients with chronic renal failure (serum creatinine, >3 mg/dL) are at very high risk for acute renal failure (54%) and permanent graft loss (23%) after cardiac operations.
The preservation of perioperative renal function in all transplant patients maintained long term on nephrotoxic immunosuppressive drugs is paramount. Renal function was optimized by adequate hydration, the administration of mannitol and furosemide, the maintenance of uniform perfusion pressures during CPB, close attention to urine output, and judicious diuresis. 
-Adrenergic agents were not used, but dopamine was routinely administered, especially to renal transplant recipients. A similar management approach has been taken by Bolman and colleagues [6]; however, we did not encounter difficulties related to maintaining perfusion pressures lower than 70 mm Hg in these patients. Interestingly, although there were minor variations among individual patients within groups, we found no significant difference in the preoperative and postoperative mean serum creatinine levels in any group (see Table 6, Fig 2).
Acute rejection developed in 3 (5%) of the 64 patients in this study, including 2 kidney transplant patients and 1 lung transplant patient. Both renal transplant recipients were in their fifties and had had their allografts in place for more than 3 years. Both, however, had had preoperative creatinine levels of greater than 3 mg/dL, and graft failure that resolved with hemodialysis developed postoperatively in 1, whereas acute tubular necrosis developed in the other. Both also had a reduction in their immunosuppressive regimens postoperatively, which may account for the subsequent development of rejection. The other patient was a pulmonary transplant recipient who suffered rejection 11 days after the transplantation, a relatively common event in this patient population (90% incidence in the first year at our institution). The overall incidence of acute rejection in this series (4.7%) is evidence that transplanted allografts can manage the stress of major operations. We believe that our management of the immunosuppressive regimen and fastidious attention to maintaining consistent blood levels of tacrolimus and Csa were instrumental in ensuring a low rejection rate. We advise checking the blood level the day before operation, administering the routine dose the morning of operation checking the blood level the morning after operation, and administering the dose on the first postoperative day orally, by nasogastric tube, or IV if necessary. Should the blood levels be low on the first postoperative day, the immunosuppressive agent should be administered IV to obtain therapeutic blood levels. If the blood levels are found to be elevated or renal impairment is suspected, withholding the scheduled dose and rechecking the blood level on consecutive days are warranted.
The potential infectious and wound healing complications that are associated with immunosuppressive and systemic steroid therapy are always of concern in the transplant population. Our major infectious complication rate of 19% was considered significant and included 3 cases of mediastinitis, 1 of which contributed to the development of overwhelming sepsis and death 7 weeks after the cardiac procedure. All 3 cases occurred in diabetic renal transplant recipients who underwent CABG with a left internal mammary artery to the left anterior descending artery. Four cases of sepsis were also a problem in this subgroup of patients, 1 of which resulted in death 9 days after the patient's procedure. A high incidence of sepsis has been noted in other series [15, 16], despite a similar prophylactic regimen of broad-spectrum antibiotics administered perioperatively. Long-term immunosuppressive therapy and bacterial colonization of the airways, gastrointestinal tract, and skin may play an important etiologic role. Leg wound infections without wound breakdown developed in 3 patients and were effectively treated with antibiotics.
The incidence of reoperations for evacuation of mediastinal hematomas causing tamponade was inexplicably high, with 16% of patients requiring this intervention. Similar findings have been noted in other studies of nontransplanted renal failure patients, but not in the transplant population [17, 18]. There were no episodes of coagulopathy, no unusual or excessive clotting factor or platelet requirements, and no difficulties with reversing heparinization at the conclusion of the procedure in these patients. Additionally, coagulation study results were considered within the normal range perioperatively. Dunton and colleagues [7] found a similar lack of clotting aberrations and normal clotting values in their group of 3 liver transplant patients with no marked bleeding sequelae. The high mediastinal hematoma rate may stem from the presence of friable tissue resulting from long-term steroid use and from postcardiotomy platelet dysfunction, particularly in the patients with chronic renal failure. At reoperation, no patient was found to have an identifiable surgical cause for the bleeding. The liberal use of fresh frozen plasma and platelets may circumvent the risk of this complication. The incidences of other major complications were not considered excessive. There was one gastrointestinal complication in a kidney transplant patient. This consisted of a perforated viscus requiring exploratory laparotomy and bowel resection a few days after an aortic valve replacement. This patient tolerated both procedures with no difficulties. Interestingly, all 4 patients requiring reintubation for the management of pulmonary insufficiency were liver transplant patients, whereas all 4 patients with pleural effusions were renal transplant recipients. The serum albumin levels recorded preoperatively in 3 of the 4 liver and 2 of the 4 kidney transplant patients were in the normal range.
Outcome measures that were additionally evaluated in this study included the CPB and cross-clamp times, as one measure of technical complexity, and length of stay, as a measure of the overall physiologic reserve of these patients to compensate for the considerable stress of major operations. The mean cross-clamp and CPB times of 92 and 141 minutes, respectively, were considered acceptable. The thoracic organ transplant group, not unexpectedly, had longer times. The intensive care unit stay averaged 5.6 days and was longer than that in our nontransplant patients, as was the average 16-day total length of stay. The kidney transplant recipients fared worse than the two other subgroups in terms of both the intensive care unit and total length of stay (see Fig 3).
During a mean follow-up of 2 years, no patients had recurrent cardiac disease and all were in NYHA class I or II. Our excellent long-term results are contrary to those observed by Shafei and colleagues [19], who found that recurrent angina had developed in 5 of their 7 patients 1 month to 1 year after their cardiac operation, with 3 of 5 having myocardial infarctions. Similar outcomes were reported by Beauchamp and associates [20], who found that 2 of 3 patients had recurrent angina at the 1-year follow-up. Bolman and colleagues [6] in their series observed results similar to ours. The discrepancy in the incidence of the recurrence of late cardiac symptoms may result from patient population differences and the progression of cardiovascular disease, which emphasizes the importance of careful and complete follow-up.
In summary, we have evaluated 64 solid organ transplant recipients with functional allografts who subsequently underwent cardiac surgical procedures. The incidences of short-term infectious and bleeding complications were significant and probably related to long-term immunosuppressive therapy and the presence of co-morbid medical conditions. However, the low incidences of permanent graft failure, rejection, renal impairment, and mortality were consistent with results obtained in the nontransplant cardiac operation patient population. We propose that these patients be approached with caution and diligence but not undue apprehension.
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Footnotes |
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Presented at the Thirty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Feb 3–5, 1997.
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