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Ann Thorac Surg 1999;67:1045-1052
© 1999 The Society of Thoracic Surgeons

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Original Articles

Influence of diabetes mellitus on early and late outcome after coronary artery bypass grafting

^a Division of Cardiothoracic Surgery, Department of Surgery, Emory Center for Outcomes Research, and Divisions of Cardiology and Endocrinolgoy, Department of Medicine, Emory University School of Medicine, Atlanta, Georgia USA

Accepted for publication September 26, 1998.

Address reprint requests to Dr Weintraub, Division of Cardiology, Emory University WMB 319, 1639 Pierce Dr, NE, Atlanta, GA 30322
e-mail: bill{at}hp3.eushc.org

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Diabetes mellitus is an established independent risk factor for significant morbidity and mortality after coronary artery bypass grafting.

Methods. The impact of diabetes on short- and long-term follow-up after coronary artery bypass grafting was studied by comparing the outcomes between 9,920 patients without diabetes mellitus and 2,278 patients with diabetes from 1978 to 1993.

Results. Compared with nondiabetic patients, the group with diabetes was older (62 ± 10 years versus 60 ± 10 years), comprised more women (31% versus 19%), had a greater incidence of hypertension (61% versus 44%) and previous myocardial infarction (51% versus 48%), had class III-IV angina more commonly (69% versus 63%), showed a higher incidence of congestive heart failure (11% versus 5%) or triple-vessel or left main disease (60% versus 50%), and had lower ejection fractions (0.54 versus 0.57) (all, p 0.05). Diabetic patients had a higher incidence of postoperative death (3.9% versus 1.6%) and stroke (2.9% versus 1.4%) (both, p 0.05), but not Q wave myocardial infarction (1.8% versus 2.9%). Diabetics had lower survival (5 years, 78% versus 88%; 10 years, 50% versus 71%; both, p 0.05) and lower freedom from percutaneous transluminal coronary angioplasty (5 years, 95% versus 96%; 10 years, 83% versus 86%; latter, p 0.05), but diabetics did not have lower freedom from either myocardial infarction (5-years, 92% versus 92%; 10-years, 80% versus 84%) or additional coronary artery bypass grafting (5-years, 98% versus 99%; 10-years, 90% versus 91%). Multivariate correlates of long-term mortality were diabetes, older age, reduced ejection fraction, hypertension, congestive heart failure, number of vessels diseased, and urgent or emergent operation.

Conclusions. Diabetics have a worse hospital and long-term outcome after coronary artery bypass grafting. The increased risk in such patients can only partially be explained by other demographic characteristics.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Diabetes mellitus is an established risk factor for the development of coronary artery disease. Epidemiologic data from the Framingham study [1] have shown that diabetes is a major independent risk factor for cardiovascular disease even after adjusting for other confounding risk factors such as age, hypertension, hypercholesterolemia, and tobacco abuse. Further, the incidence of congestive heart failure and cardiovascular death are even higher in female diabetic patients than in male diabetics. Compared with patients without diabetes, diabetics have a greater tendency for adverse effects on the coronary circulation, an increased propensity for accelerated atherosclerosis, and a higher incidence of extensive coronary artery disease [2]. Diabetic patients have a higher incidence of two- and three-vessel disease and a lower incidence of one-vessel disease than do nondiabetic patients [3]. Therefore, diabetic patients constitute an important and more challenging segment of the population undergoing surgical coronary revascularization.

Many series report that approximately 20% of patients who have undergone coronary artery bypass grafting have diabetes mellitus [4–6]. Diabetes has been associated with higher perioperative morbidity as well as decreased survival after coronary artery bypass grafting [5–7]. Diabetic patients undergoing surgical revascularization of coronary atherosclerosis represent a large and complex subgroup of bypass patients. As the effects of diabetes are known to progress over time, studies incorporating both short- and long-term follow-up are necessary. Here, we present the largest cohort of diabetic and nondiabetic patients undergoing coronary artery bypass grafting at one institution with both short- and long-term follow-up. The contribution of various confounding factors on survival in diabetic patients undergoing coronary artery revascularization was evaluated. We found that the presence of diabetes mellitus was a significant independent predictor of short- and long-term survival after coronary artery bypass grafting.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
From 1978 through 1993, 12,198 consecutive patients underwent cardiac catheterization followed by primary coronary artery bypass grafting at Emory University Hospitals. Patients undergoing operation for stable or unstable angina pectoris or after several days of stabilization after acute myocardial infarction were included. Patients having emergent operation for an evolving myocardial infarction or patients who underwent minimally invasive direct coronary artery bypass grafting were excluded.

During the 16 years, 9,920 of these patients were classified as nondiabetic and 2,278, as diabetic. The definition of diabetes followed that of the American College of Cardiology database. Patients were considered as having diabetes on the basis of history, regardless of duration of disease or need of antidiabetic agents. The diagnosis could also be based on a previous physician telling a patient he or she had diabetes (generally based on fasting, nonstressed blood sugar level > 140 mg/dL on at least two occasions), a current or previous regimen of oral hypoglycemic agents or insulin, or a diet therapy.

Standard surgical techniques were used for coronary artery bypass grafting [8]. Extracorporeal circulation and myocardial protection strategies were implemented as per the attending surgeon [8]. Clinical, angiographic, and procedural data, including complications, were recorded prospectively on standardized forms and entered into a computerized database. All fields were defined in a data dictionary.

Definitions
Definitions for variables studied are as follows: single-vessel disease, narrowing of the diameter of the lumen by more than 50% in the left anterior descending, left circumflex, or right coronary artery or a major branch or branches; double-vessel disease, narrowing of the diameter of the lumen by more than 50% in two of the three major epicardial vessel systems; three-vessel disease, narrowing of the diameter of the lumen by more than 50% in all three major epicardial vessel systems or in the left anterior descending and proximal circumflex coronary artery in left-dominant patients; left main coronary artery disease, narrowing of the diameter of the lumen by more than 50% in the left main coronary artery; urgent procedure, a procedure judged by the surgeon to be required within 24 hours; emergent procedure, a procedure performed in the setting of acute ischemia or infarction; complete revascularization, bypass of all major obstructions in the epicardial vessels during the operation; and postoperative myocardial infarction, development of major new Q waves. Variables defined by patient history included hypertension, severity of angina, previous myocardial infarction, and myocardial infarction during follow-up. The Canadian Cardiovascular Society Classification was used to define angina, and the New York Heart Association criteria (The Criteria Committee) were used to define congestive heart failure.

Follow-up
Follow-up information was obtained from the patients or their referring physicians. Follow-up status for each end point was also assessed at each subsequent admission. Patients not readmitted were contacted by telephone or letter. Follow-up data were available for 11,624 (95%) of the 12,198 patients; mean length of follow-up was 7.5 ± 4.7 years. Information obtained included occurrence of myocardial infarction, subsequent need for an additional revascularization procedure, death (cardiac versus noncardiac related), and recurrent angina. All follow-up information was recorded on standardized forms and entered into the computerized database. All repeat surgical interventions and angioplasty procedures performed at Emory University Hospitals were confirmed from the database.

Statistical analyses
Results are expressed as proportions or as the mean ± the standard deviation. The clinical, angiographic, and procedural characteristics of each group were determined. Differences in categoric variables were analyzed by ² analysis (or Fisher’s exact test), and differences in continuous variables were analyzed by Student t tests. Overall survival (cardiac and noncardiac related deaths) and event-free survival were determined by the Kaplan-Meier method, and the estimated probability is shown together with the standard error of the estimate. Overall survival analyses for the total population and the two diabetic subgroups (with or without need of insulin) and event-free survival analyses for the total population were performed. The following end points were analyzed: survival; freedom from myocardial infarction; freedom from additional bypass grafting procedures; freedom from additional angioplasty; and event-free survival, defined as freedom from the events of death, myocardial infarction, additional bypass procedures, and additional angioplasty. Comparisons of total and event-free survival were made using the Mantel-Cox method. Multivariate correlates of survival were determined with the Cox model analysis with repeated analyses; variables that were frequently missing were eliminated to determine the impact of missing data (and consequently fewer patients in the model) on the analyses.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Clinical characteristics of the two patient groups
The clinical and angiographic characteristics of the 12,198 patients (2,278 with diabetes mellitus and 9,920 patients without diabetes mellitus) who underwent coronary artery bypass grafting at Emory University Hospitals from 1978 to 1993 are presented in Table 1. Diabetic patients were older; the mean age in both groups was the early 60s. The percentage of women in the diabetic group was higher, as was the percentage of patients with hypertension. Patients with diabetes were seen more commonly with class III–IV angina, congestive heart failure, and previous myocardial infarction. There was a large difference in the extent of vessels diseased; the majority of patients without diabetes had one- or two-vessel disease and the majority of diabetic patients, three-vessel disease. The presence of left main coronary disease was the same. Left ventricular ejection fraction was in the normal range in both groups; however, diabetic patients had slightly lower ejection fractions.

View larger version (36K): [in this window] [in a new window]   Fig 1. Survival for the entire patient population having coronary artery bypass grafting.

View larger version (25K): [in this window] [in a new window]   Fig 2. Survival corrected for baseline differences for entire patient population.

View larger version (41K): [in this window] [in a new window]   Fig 3. Survival for diabetic subgroups having coronary artery bypass grafting.

View larger version (31K): [in this window] [in a new window]   Fig 4. Survival corrected for baseline differences for diabetic subgroups.

View larger version (36K): [in this window] [in a new window]   Fig 5. Freedom from (FF) myocardial infarction (MI) for the entire patient population having coronary artery bypass grafting.

View larger version (34K): [in this window] [in a new window]   Fig 6. Freedom from (FF) additional coronary artery bypass grafting (CABG) for the entire patient population.

View larger version (37K): [in this window] [in a new window]   Fig 7. Freedom from (FF) additional percutaneous transluminal coronary angioplasty (PTCA) for the entire patient population having coronary artery bypass grafting.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

For patients undergoing coronary artery bypass grafting, the prevalence of a history of diabetes mellitus averages 20% [4–6]. In the present study, 19% of patients had a history of diabetes mellitus. The diabetic patients in our study had a similar pattern of patient demographics and characteristics as patients in other reported series [4, 6]. In addition, the present study supports previous studies showing that diabetics, particularly patients requiring insulin therapy, have more severe and extensive coronary artery atherosclerosis, as demonstrated by the increased prevalence of triple-vessel involvement, and more diseased and occluded coronary arteries per patient [2]. Considerable scientific evidence indicates that the presence of both hypertension and diabetes accelerates the development of atherosclerosis more than either comorbid factor alone [9, 10]. In our series, a significantly greater percentage of diabetic patients (61%) compared with nondiabetic patients (44%) had a history of hypertension.

The reported incidence of postoperative complications after coronary artery bypass procedures in diabetic patients has varied. Fietsam and associates [11] found an increase in morbidity among diabetic patients; however, they did not find any increase in the occurrence of reoperation, stroke, or perioperative myocardial infarction. In contrast, Kuan and colleagues [12] reported that diabetics had an increased risk of stroke, hemorrhage, and perioperative myocardial infarction. In the present study, the incidences of perioperative neurologic complication (stroke) and hospital death were more frequent in diabetic patients than in patients without diabetes.

In this series, important predictors of long-term mortality in patients undergoing surgical coronary revascularization include older age, low ejection fraction, congestive heart failure, procedure status, and hypertension. In addition, the presence of diabetes mellitus serves as an important predictor of both short- and long-term mortality. In large retrospective studies, diabetes has been shown to be an independent predictor of mortality in multivariate analyses. In a series of 2,004 patients, Adler and coauthors [13] reported that for 329 diabetic patients (16%), the multivariate mortality rate ratio attributable to diabetes was 1.6. In a larger series, Morris and colleagues [6] analyzed 1,132 diabetic patients undergoing surgical coronary revascularization and obtained results similar to those of Adler and coworkers [13].

However, not all large cohort studies have identified diabetes as an independent predictor of mortality. In a study involving 8,000 consecutive patients undergoing bypass grafting (7% of whom had diabetes), Cosgrove and associates [14] did not find diabetes to be a univariate or multivariate predictor of mortality. In agreement with Adler [13], Morris [6], and their coworkers, we found that diabetes was a univariate and multivariate predictor of not only hospital mortality but also long-term mortality. At 5 years, diabetic patients had an 11% reduction in survival compared with patients who did not have diabetes, and at 10 years, this discrepancy increased to a 29% reduction in survival for diabetics.

Method of diabetic therapy and degree of glucose intolerance have been shown to be determinants of early and late survival in diabetics with coronary artery disease. Garcia and coauthors [15] reported a higher mortality rate for insulin-treated diabetic women compared with orally treated diabetics. Lawrie and associates [16] noted that preoperative blood glucose level was an important predictor of late mortality in diabetic patients and that overall 15-year survival was significantly reduced for insulin-treated diabetics compared with those receiving other modes of diabetic therapy. In the current study, we confirm that insulin-dependent diabetics have reduced long-term survival. Insulin-requiring patients (n = 761) more commonly were female, had a history of congestive heart failure and previous myocardial infarction, showed a lower ejection fraction, and had more extensive coronary artery disease. Although, insulin-dependent diabetics did not have increased perioperative or postoperative complications (Q wave myocardial infarction or stroke) compared with diabetics not needing insulin, insulin requirement was a significant correlate of long-term mortality in diabetic patients undergoing coronary artery bypass grafting. In contrast to these findings, Hamby and Sherman [17] noted that the degree of glucose intolerance and Salomon and associates [7] noted that the mode of diabetic therapy seems not to be a major determinant of early or late survival in the diabetic population with heart disease. Further studies evaluating acute elevation of glucose levels during coronary artery bypass grafting as a predictor of mortality and morbidity are warranted.

Although coronary artery bypass grafting is well tolerated by diabetic patients, long-term survival continues to be poorer for these patients compared with their nondiabetic counterparts as a result of the underlying pathophysiology of diabetic heart disease. Abnormalities in the vascular endothelium may explain the reduction in survival after cardiovascular events for diabetic patients. There is substantial evidence that endothelium-dependent vasodilation is abnormal in both conduit arteries and resistance vessels of diabetic animals [18, 19] and humans [20, 21]. A major mechanism hypothesized to explain the abnormal endothelium-dependent vasodilation in the presence of diabetes mellitus has been the decrease in the synthesis or release of nitric oxide [22]. This has been associated with greater inflammatory like responses to stresses such as ischemia-reperfusion, thus resulting in greater postischemic injury. Other possible mechanisms that explain endothelial dysfunction in diabetic patients include accelerated inactivation of nitric oxide by high levels of free radicals and advanced glycosylation end products [19], release of potent vasoconstrictor prostanoids that attenuate the effects of nitric oxide [18, 23], increased activation of protein kinase C [24], and decreased expression of inhibitory G proteins causing abnormalities in signal transduction [25]. Although the link between diabetes, endothelial dysfunction, and long-term morbidity, mortality, or both is not understood, the loss of the modulatory role of the endothelium may be implicated in the pathogenesis of diabetic vascular disease.

Endothelial cell dysfunction in diabetics may serve as a major initiating process to the development of vascular disease in resistance vascular conduits. Nitenberg and associates [20] reported a reduction in coronary flow reserve in epicardial arteries in diabetic patients compared with nondiabetics. Correspondingly, Nahser and coworkers [21] demonstrated reduced maximal coronary microvascular vasodilation and increased impairment in the regulation of coronary flow in the myocardial resistance vessels in response to submaximal increases in myocardial demand in diabetics compared with nondiabetic controls. The detrimental effects of sustained elevated glucose levels on the vascular endothelial cell and in the small resistance myocardial microvessels in diabetic patients may contribute to the adverse cardiovascular events and reduced survival in diabetic patients after coronary artery bypass procedures.

In conclusion, diabetes mellitus is a significant independent predictor of short- and long-term mortality in patients undergoing coronary artery bypass grafting. Specifically, insulin requirement in diabetic patients is a significant multivariate correlate of long-term mortality in that it may indicate the severity of the disease process, which may predispose to greater postsurgical complications. Studies delineating the pathophysiologic factors responsible for the increased morbidity and mortality in diabetic patients undergoing coronary artery bypass grafting are necessary. Practicing cardiologists and cardiothoracic surgeons should carefully review the short- and long-term outcomes with diabetic patients who are to undergo coronary artery bypass grafting.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
We thank Jakob Vinten-Johansen, PhD, for his insightful editorial comments and assistance with the manuscript.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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				H. Hegazy, A. Refaei, A. Assedique, S. Alsaif, M. Taha, M. Refaei, N. Elkum, H. Alomran, and Z. Al-Halees PET scan before CABG in diabetes The British Journal of Diabetes & Vascular Disease, January 1, 2007; 7(1): 32 - 37. [Abstract] [PDF]

				A. I. Duncan, C. G. Koch, M. Xu, M. Manlapaz, B. Batdorf, G. Pitas, and N. Starr Recent Metformin Ingestion Does Not Increase In-Hospital Morbidity or Mortality After Cardiac Surgery Anesth. Analg., January 1, 2007; 104(1): 42 - 50. [Abstract] [Full Text] [PDF]

				B. Kragsterman, M. Bjorck, J. Lindback, D. Bergqvist, H. Parsson, and on behalf of the Swedish Vascular Registry (Swedva Long-Term Survival After Carotid Endarterectomy for Asymptomatic Stenosis Stroke, December 1, 2006; 37(12): 2886 - 2891. [Abstract] [Full Text] [PDF]