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Ann Thorac Surg 2001;71:543-548
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Coronary artery bypass grafting in patients on chronic hemodialysis: surgical outcome in diabetic nephropathy versus nondiabetic nephropathy patients

Yasuyuki Hosoda, MDa, Taira Yamamoto, MDa, Kenji Takazawa, MDa, Motoshige Yamasaki, MDa, Shin Yamamoto, MDa, Ichiro Hayashi, MDa, Kazunori Kudoh, CCPa

a Department of Cardio-Thoracic Surgery, Juntendo University, Tokyo, Japan

Accepted for publication July 6, 2000.

Address reprint requests to Dr Hosoda, Department of Cardio-Thoracic Surgery, Juntendo University, 3-1-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan
e-mail: yhosoda{at}med.juntendo.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. The presence of diabetes mellitus adversely affects the late survival of patients undergoing coronary artery bypass grafting (CABG). The purpose of this study is to clarify the role of diabetic nephropathy on outcomes of a group of patients on chronic hemodialysis undergoing CABG.

Methods. Between April 1984 and July 1999, 45 patients on chronic hemodialysis underwent CABG. Forty-three had conventional CABG and 2 had off-pump CABG. There were 37 males and 8 females, and the mean age was 57 years (43 to 76 years). Twenty-one patients had diabetic nephropathy (group D) and 24 had nondiabetic nephropathy (group ND). Early and late results were determined in both groups.

Results. Early outcome was not significantly different between the groups. There was no hospital mortality, stroke, or requirement for prolonged mechanical ventilation (>24 hours) in either group. No patients in group D, and only 1 (4.2%) in group ND had low cardiac output syndrome. The difference in the incidence of arrhythmias (23.8% in group D and 25% in group ND), wound infections (9.5% in group D and 8.3% in group ND), and delayed tamponade (5% in group D and 12.5% in group ND) was not statistically significant. However, late results differed significantly between the two groups. Actuarial survival (Kaplan-Meier) at 5 and 9 years was 22.9% and 11.5% in group D and 89.1% and 45.7% in group ND (p = 0.01), respectively. Similarly, the cardiac event-free rate at the same intervals was 50.4% and 0% for group D and 100% and 65.8% for group ND (p = 0.001), respectively.

Conclusions. Using present technology, CABG can be done in patients on chronic hemodialysis with acceptable early mortality and morbidity. Late results in patients with diabetic nephropathy on hemodialysis are not as favorable as their nondiabetic cohort.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
In December 1997, there were 175,988 persons in Japan on chronic hemodialysis, and this number has been steadily increasing. The percentage of these patients with diabetic nephropathy has also increased (14% in 1990, 22.7% in 1997). Survival of patients with diabetic nephropathy at 5 and 10 years after initiation of dialysis is reported to be 47.9% and 23.2%, respectively, whereas it is 59.9% and 42.2% in nondiabetics on dialysis [1].

The most common cause of death in these patients is coronary artery disease, and many have undergone coronary artery bypass grafting (CABG) in an effort to improve survival. Long-term results are not as favorable after CABG in diabetics compared with nondiabetics. The negative influence of diabetic nephropathy on long-term outcome among patients on chronic hemodialysis undergoing CABG has not been determined.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Patients
Among 2,052 patients undergoing primary CABG at the Department of Cardiovascular Surgery, Juntendo University, between January 1984 and July 1999, there were 45 on chronic hemodialysis (2.2%). Twenty-one of 45 (46.7%) had diabetic nephropathy (group D), whereas the cause of renal failure in the remaining 24 of 45 (53.3%) was not diabetic (group ND). The causes of renal failure in group ND included chronic glomerulonephritis (n = 11), nephrosclerosis (n = 5), polycystic kidney (n = 2), tuberculosis (n = 2), toxemia of pregnancy (n = 1), neoplasm (n = 1), and unknown (n = 2). At the time of CABG, group ND patients had been on dialysis longer (79 ± 56.7 months) than group D patients (37 ± 30.4 months) (p = 0.01) [Table 1].


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  		Table 1. Preoperative Clinical Profiles

 
Three patients underwent urgent CABG because of unstable angina (group D, 1; group ND, 2), and the remaining 42 patients were performed electively. Because of severe calcification of the ascending aorta, two cases were performed "off pump," and the remaining 43 were performed using conventional cardiopulmonary bypass, moderate systemic hypothermia (28°C to 32°C), topical cardiac cooling, and either crystalloid or blood hyperkalemic cardioplegia.

Homofiltration on cardiopulmonary bypass (CPB)
No restrictions were placed on the amount of hyperkalemic cardioplegic solution used in these cases. Instead, high-volume hemofiltration was performed during CPB incorporating two parallel filters (Fresenius Filter, F80, PF80; Fresenius-Kawasaki Co Ltd, Tokyo, Japan) in the CPB circuit, adding generous amounts of physiological saline solution. The amount of saline added was controlled according to the serum potassium level of the patient. An average of 19,714 ± 5,881 mL (9,400 to 30,150 mL) of fluid was administered during filtration, and 24,346 ± 6,048 mL (10,850 to 34,680 mL) was removed. Preoperative serum creatinine was 8.4 ± 2.3 mL/dL, and came down to 3.8 ± 1.2 mg/dL, removing an average of 993 ± 387 mg. BUN was 42.7 ± 15.1 mg/dL preoperatively, and came down to 22.1 ± 7.6 mg/dL, removing an average of 6,500 ± 2,963 mg. Serum potassium averaged 4.5 ± 0.7 mEq/L preoperatively and 4.0 ± 0.6 mEq/L postoperatively, removing 90.9 ± 28.3 mEq on average (Fig 1).



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  		Fig 1. Changes of serum-creatinine, BUN, and potassium.

 
All patients had routine hemodialysis on the first postoperative day without untoward hemodynamic effect. They were placed on aspirin 81 mg/day and dipyridamole 200 mg/day. Anticoagulants were not routinely used.

Definitions
Early mortality was defined as any death occurring within 30 days of CABG or during the initial hospital stay, and late mortality was any death occurring after that time. The development of congestive heart failure (CHF), fatal or nonfatal myocardial infarction, the requirement for a cardiac intervention (redo CABG, percutaneous transluminal coronary angiography, etc) or sudden, unexplained death were considered as cardiac events.

The Canadian Cardiovascular Society (CCS) classification was used to describe the severity of symptoms. Cerebrovascular accidents (CVA) were felt to have occurred in patients with a history of transient ischemic attacks (TIA), documented cerebral infarction, or hemorrhage or computed tomography abnormalities of the brain. Vascular disorders included obstructive disease of the peripheral arteries, > 50% stenosis of the extracranial carotid arteries, or abdominal aortic aneurysms > 5 cm in diameter.

Follow-up
Follow-up information was obtained from the patient’s hospital record, interviews at the time of outpatient visits, telephone calls and follow-up letters (annually), and from referring physicians. Follow-up was 100% complete in the 45 patients.

Statistical methods
Comparison of continuous variables in the two groups was done using paired Student’s t tests, and the significance of differences in frequency was tested using {chi}2 analysis. Actuarial survival and cardiac event-free survival was calculated by the Kaplan-Meier method, and the Wilcoxon test was used to compare differences between two groups, with a p value less than 0.05 considered significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Perioperative data
Patient characteristics are shown in Table 1. The patients in group ND had been on hemodialysis longer (79 ± 56.7 vs 37 ± 30.4 months) than those in group D. Those in group D were older (60 ± 7.4 vs 55 ± 6.8 years) and had a higher incidence of vascular disease (38.1% vs 4.2%) than the nondiabetics.

Intraoperative data are shown in Table 2. The left internal thoracic artery was used to bypass the left anterior descending artery (LAD) in most cases (90% in group D and 79% in group ND). Bilateral internal thoracic artery (ITA) grafts were not used in this series. Autologous saphenous veins (SVG) were used to bypass arteries other than the LAD. The low level of attaining "complete revascularization" was felt to relate to the diffuse nature of disease in most patients, particularly the diabetics (52.3% vs 66.6%), although this difference did not reach statistical significance.


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  		Table 2. Operative Characteristics

 
Morbidity and mortality
Perioperative results are shown in Table 3. There were no early deaths in either group. There were no perioperative myocardial infarctions or cerebrovascular accidents, and no patient required prolonged mechanical ventilation (>24 hours). One patient in group ND developed low cardiac output requiring inotropic support. Delayed tamponade requiring surgical drainage developed in 1 patient in group D (5%) and in 3 patients in group ND (12.5%). Two patients in group D developed mediastinitis (9.5%), whereas 1 patient in group ND (4.2%) developed mediastinitis and another (4.2%) had septicemia. Several patients developed pleural or pericardial effusions that did not require surgical drainage.


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  		Table 3. Perioperative Morbidity

 
Graft patency
Fourteen patients underwent postoperative angiographic studies (4 in group D and 10 in group ND) at 1 month to 12 years and 9 months after CABG (average 62 ± 43.1 months). Ten of 10 LITA grafts were patent (100%) and 21 of 22 (95.5%) SVGs were patent. The only occluded graft was a SVG to an obtuse marginal studied 12 years and 9 months after CABG in a nondiabetic patient. The SVG placed to the LAD in this patient was widely patent (Fig 2).



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  		Fig 2. Widely patent SVG bypassed to LAD, 12 years and 9 months after operation in a nondiabetic patient. SVG bypassed to LCX was occluded.

 
Long-term results
Late follow-up was 100% at 31 ± 27.3 months (1.0 to 114.2 months) in group D and 58 ± 39.1 months (4.3 to 155.5 months) in group ND. Twenty patients died during the follow-up period, most commonly (70%) from cardiac causes (Table 4).


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  		Table 4. Causes and Number of Late Deaths in the Follow-up

 
Actuarial survival (Kaplan-Meier) at 5 and 9 years was 22.9% and 11.5% in group D, respectively, and 89.1% and 45.7% in group ND (p < 0.01) (Fig 3). Cardiac event-free survival at 5 and 9 years was 50.4% and 0% in Group D, respectively, and 100% and 65.8% in group ND (p < 0.01) (Fig 4).



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  		Fig 3. Actuarial survival in dialysis patients with diabetic nephropathy (D) and nondiabetic nephropathy (ND) after CABG.

 


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  		Fig 4. Actuarial freedom from occurrence of any cardiac event in dialysis patients with diabetic nephropathy (D) and nondiabetic nephropathy (ND).

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
In December 1997, there were 175,988 patients in Japan undergoing chronic hemodialysis, and there were 14,962 deaths among these patients [1]. Cardiac disease is a major cause of death among dialysis patients worldwide [1–4]. In the US, it is estimated that 20% to 30% of deaths in dialysis patients result from cardiac disease. In Japan, the estimate is slightly more than 30%, with 24% dying of heart failure and 8.4% of acute myocardial infarction.

The 1-year survival of patients on dialysis did not change between 1983 (83.6%) and 1997 (85.7%). However, the 5-year survival decreased from 62.6% in 1983 to 57.8% in 1997 [1]. This trend is felt to be from the increasing age of the patient population and the higher percentage of those with diabetic nephropathy. Both age and diabetes are known to be independent predictors of adverse long-term outcome in patients undergoing CABG [4–7].

Early mortality for CABG in dialysis patients is reported to be 6% to 16% [8–13] in western countries and 0% to 14% in Japan [14–17]. Although this operative mortality rate seems high, the annual mortality for patients on chronic dialysis known to have coronary disease is 25% [1]. The perioperative complication rate among dialysis patients undergoing CABG has been reported to be 10% to 30%, significantly higher than that seen in nondialysis patients.

In the group of patients reported in this study, there was no operative mortality, nor were there any perioperative cerebrovascular events or extended ventilator requirements. However, wound infection, delayed tamponade, and pleural/pericardial effusions were observed more frequently in this group than in the nondialysis population.

We believe that the use of high-volume hemofiltration during CPB incorporating two parallel hemofilters in the circuit is very effective in eliminating potassium, creatinine, and urea nitrogen from these patients by administering and removing large amounts of saline solution. Use of this hemofiltration system allows the use of as much potassium cardioplegia as needed. The patient’s body weight is always less at the end of the procedure than it was at the beginning. In effect, this method of high-volume hemofiltration could be called "body laundering." The patients were hemodynamically quite stable postoperatively, and usually resumed regular hemodialysis on the first postoperative day. During dialysis, either gabexate mesylate or nafamostat mesylate, proteolytic enzyme inhibitors that also inhibit parts of the coagulation cascade (not currently approved by the US Food and Drug Administration), was used as a substitute for heparin.

Recently, off-pump CABG has been advocated for patients on chronic hemodialysis to avoid the possible deleterious effects of CPB [18, 19]. The coronary arteries of patients with chronic renal disease are often diffusely diseased or calcified, and many of these patients have significant left ventricular hypertrophy, making off-pump surgery technically difficult. Using the hemofiltration technique as described, the procedure can be made much easier, and the absence of early mortality and the low perioperative morbidity attests to its safety.

Long-term survival and cardiac event-free survival rates among these patients remain disappointing. Ko and associates [10] reported 83% to 95% survival at 1 year and 48% to 60% survival at 5 years in dialysis patients. These results are similar to those reported in our series.

The survival of patients on dialysis with coronary artery disease is reported to be 76% at 1 year and 48% at 5 years [3], and it has been felt that CABG may positively influence survival. Indeed, the survival rates at 5 and 9 years in nondiabetic patients on hemodialysis undergoing CABG is 89.1% and 45.7%, respectively, whereas that in the diabetic nephropathy group is a disappointing 22.9% and 11.5% at the same intervals. These figures suggest that there may be little long-term survival improvement in those dialysis-dependent patients with diabetic nephropathy.

A similar contrast can be made when evaluating cardiac event-free survival. In the nondiabetic dialysis patients undergoing CABG, the 5- and 9-year cardiac event-free survival was 100% and 65.8%, respectively. In diabetic nephropathy patients, however, these event-free rates were 50.4% and 0% at 5 and 9 years, respectively.

Although the number of patients having follow-up angiography is small, the results were encouraging with respect to graft patency (10 of 10 LITA grafts patent and 21 of 22 SVG grafts patent). This may suggest that the cause for cardiac events during long-term follow-up may be progression of disease in the native, ungrafted coronaries. This phenomenon was, in fact, noticed in the follow-up angiograms.

We realize that this is a retrospective review of a small number of patients. Nonetheless, there is ample evidence that dialysis patients with diabetic nephropathy do not enjoy the same level of long-term benefit after CABG as those whose nephropathy is not diabetic in origin.

Conclusions
The early results of CABG in patients on chronic hemodialysis are good. The described method of hemofiltration during CPB allows for safe and easy use of conventional cardioplegic techniques.

The late prognosis of patients with diabetic nephropathy after CABG is poor. Indications for CABG in this setting should be carefully considered.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We would like to express deep appreciation to Dr William A. Gay for revising the English of this manuscript.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. An overview of regular dialysis treatment in Japan. Japanese Society for Dialysis Therapy 1997;39–131.
  2. United States Renal Annual Data Report. Cause of Death. Bethesda: National Institute of Diabetes and Digestive and Kidney Disease. 1995;79–89.
  3. Hellerstedt W.L., Johnson W.J., Ascher N., et al. Survival rates of 2,728 patients with end-stage renal disease. Mayo Clin Proc 1984;59:776-783.[Medline]
  4. Hosoda Y., Nukariya M., Watanabe M., et al. Late results of coronary bypass surgery with maximal follow-up of 7 years: analysis of determinants affecting late survival. Cardiovascular Surg 1993;4:403-409.
  5. Salomon N.W., Page U.S., Okies J.E., et al. Diabetes mellitus and coronary artery bypass: short-term risk and long-term prognosis. J Thorac Cardiovasc Surg 1983;85:264-271.[Abstract]
  6. Chychota N.N., Gau G.T., Pluth J.R., et al. Myocardial revascularization. Comparison of operability and surgical results in diabetic and nondiabetic patients. J Thorac Cardiovasc Surg 1973;65:856-862.[Medline]
  7. Hoffman R.F.G., Blumlein S.L., Anderson A.J., et al. The probability of surviving coronary bypass surgery: 5-year results from 1,718 patients. J Am Med Assoc 1980;243:1341-1344.[Abstract]
  8. Batiuk T.D., Kurtz S.B., Oh J.K., Orszulak T.A. Coronary artery bypass operation in dialysis patients. Mayo Clin Proc 1991;66:45-53.[Medline]
  9. Blakeman B.P., Sullivan H.J., Foy B.K., Sobotka P.A., Pifarra R. Internal mammary artery revascularization in patients on long term renal dialysis. Ann Thorac Surg 1990;50:766-778.
  10. Ko W., Kreger K.H., Isom W. Cardiopulmonary bypass procedures in dialysis patients. Ann Thorac Surg 1993;55:677-684.[Abstract]
  11. Owen C.H., Cummings R.G., Sell T.L., Schwab S.J., Jones R.H., Glower D.D. Coronary artery bypass grafting in patients with dialysis-dependent renal failure. Ann Thorac Surg 1994;58:1729-1733.[Abstract]
  12. Michael F., Aron K. Cardiovascular operations in patients with dialysis-dependent renal failure. Ann Thorac Surg 1999;68:887-893.[Abstract/Free Full Text]
  13. Labrousse L., Vincentiis C., Madonna F., et al. Early and long- term results of coronary artery bypass grafts in patients with dialysis-dependent renal failure. Eur J Cardiothorac Surg 1999;15:691-696.[Abstract/Free Full Text]
  14. Koyanagi T., Nishida H., Kitamura M., et al. Comparison of clinical outcomes of coronary artery bypass grafting and percutaneous transluminal coronary angioplasty in renal dialysis patients. Ann Thorac Surg 1996;61:1793-1796.[Abstract/Free Full Text]
  15. Nakayama Y., Sakata R., Ueyama K., et al. Cardiac surgery in patients with chronic renal failure on maintenance dialysis. J Jpn Thorac Surg 1997;45:1661-1666.
  16. Sawada Y., Morimoto T., Matuyama N., et al. Coronary artery bypass graft surgery in dialysis patient. J Jpn Thorac Surg 1998;46:983-986.
  17. Nakayama Y., Sakamoto R., Ura M., Miyamoto T. Coronary artery bypass grafting in dialysis patients. Ann Thorac Surg 1999;68:1257-1261.[Abstract/Free Full Text]
  18. Contini M., Iaco A., Iovino T., et al. Current results in off-pump surgery. Eur J Cardiothorac Surg 1999;16(Suppl 1):69-72.
  19. Izaat M.B., Yim A.P., El-Zufari M.H. Minimally invasive left anterior descending coronary artery revascularization in high-risk patients with three-vessel disease. Ann Thorac Cardiovasc Surg 1998;4:205-208.[Medline]



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