Effect of diabetes on early and late survival after isolated first coronary bypass surgery in multivessel disease☆☆☆

Article Outline

• Abstract
• Methods
  • Surgical details
  • Postoperative course
  • Study method
  • Definitions of terms
  • Statistical analysis
• Results
  • Early mortality
  • Late actuarial survival
  • Late actuarial survival of patients who survived for 30 days
  • Results according to preoperative treatment
  • Results according to perioperative surgical strategy
• Discussion
• Appendix
• References
• Copyright

Abstract 

Objective: Diabetes has not yet been investigated as a risk factor for early and late cardiac-related death. Methods: Patients operated on from January 1988 to December 1999 were considered; 767 were diabetic (group D) and 2593 were nondiabetic (group ND). Patients with preoperative hemodynamic deterioration were excluded. Early (30-day) mortality (any causes and cardiac causes) was evaluated with univariate analysis and stepwise logistic regression. Ten-year actuarial freedom from death of any cause and cardiac death was also assessed with univariate and Cox analyses. Results: Early mortality was 2.2% (group D, 3.3%; group ND, 1.9%; P = .023). Early cardiac mortality was 1.3% (group D, 2.2%; group ND, 1.1%; P = .0016). Diabetes was an independent risk factor only for cardiac death and not for death of any cause. Five-year survival was 93.5% ± 0.5% (group D, 92.5% ± 1.1%; group ND, 93.9% ± 0.6%; P = .0304). Diabetes was not an independent risk factor. Five-year freedom for cardiac death was 96.3% ± 0.4% (group D, 94.9% ± 0.9%; group ND, 96.6% ± 0.4%; P = .0155). Diabetes was an independent risk factor. However, if only the patients who survived the first 30 days are considered, diabetes disappears as a risk factor (5-year freedom for cardiac death, 97.8% ± 0.3%; group D, 97.3% ± 0.8%; group ND, 97.9% ± 0.4%; P = 0.2389). Conclusions: Diabetes is an independent risk factor for early cardiac death only. Long-term survival in patients who survive the first 30 days is not statistically significantly different for diabetic and nondiabetic patients. In fact, the rates appear very similar.

J Thorac Cardiovasc Surg 2003;125:144-54

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• Dr Calafiore

Diabetes is a widely recognized risk factor for increased early and late mortality after myocardial revascularization in patients with multivessel disease.¹, ², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷ Even if better results after coronary artery bypass grafting (CABG) than after percutaneous transluminal coronary angioplasty had been demonstrated in the Bypass Angioplasty Revascularization Investigation trial,¹ further studies were not able to confirm this finding.¹³, ¹⁴ Therefore it seems that diabetes is a risk factor independent from the strategy used. However, in other studies diabetes seems to be weakly related to higher early and late mortality after CABG,¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²² leaving the problem open to further evaluation.

During the past decade, different surgical techniques, such as normothermic perfusion,²³ CABG on a beating heart without cardiopulmonary bypass (CPB),²⁴, ²⁵ and extensive use of arterial conduits,²⁶, ²⁷ became popular. We reviewed our experience in patients with multivessel coronary disease who underwent surgical revascularization during a 12-year period to evaluate (1) whether diabetes is a risk factor for early or late survival and, if so, (2) whether there is any technical factor that can improve survival in diabetic patients.

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Methods 

From January 1988 to December 1999, 3392 patients with multivessel disease underwent first isolated surgical myocardial revascularization. Thirty-two patients who had preoperative low-output syndrome were not included because their status could influence the early outcome more than any other risk factor. Globally, 3360 patients were entered into this study. Among them, 767 patients (22.8%) were diabetic (group D) and receiving oral (group OT, n = 596 [77.7%]) or insulin (group IT, n = 171 [22.3%]) treatment, and 2593 (77.2%) were nondiabetic (group ND). Patients on diet because of mild fasting hyperglycemia were considered in group ND. Table 1 shows some of the preoperative characteristics of both groups.

Table 1. Preoperative data in diabetic (group D) and nondiabetic (group ND) patients

EF, Ejection fraction; AMI, acute myocardial infarction; CRF, chronic renal failure; cr, creatininemia; CHF, chronic heart failure.

Surgical details 

CPB was used in 2181 (65.4%) patients and not used in 1179 (34.6%) patients. Perioperative technical data are shown in Table 2.

Table 2. Operative data according to groups ND and D

LITA, Left internal thoracic artery; RITA, right internal thoracic artery; RGEA, right gastroepiploic artery; RA, radial artery; IEA, inferior epigastric artery; BITA, bilateral internal thoracic artery; TAMR, total arterial myocardial revascularization.

Simultaneous carotid endoarterectomy was performed in 65 patients (1.9%; 47 [1.8%] in group ND and 18 [2.3%] in group D; P = .345).

Postoperative course 

After the operation, all the patients were admitted to the intensive care unit and later sent to the regular ward. They were then followed up at our outpatient clinic. The follow-up deadline was June 30, 2000. Recent information about their clinical status was obtained directly from the referring physician or by telephone. Mean follow-up was 50 ± 38 months (median, 41 months; minimum, 3 months; maximum, 150 months; 25th percentile, 20 months; 75th percentiles, 67 months), 43 ± 34 months in diabetic patients (median, 33 months; minimum, 3 months; maximum, 149 months; 25th percentile, 17 months; 75th percentile, 67 months), and 53 ± 39 months in nondiabetic patients (median, 44 months; minimum, 3 months; maximum, 150 months; 25th percentile, 21 months; 75th percentile, 72 months; P < .001). Follow-up was 98.9% completed.

Study method 

The real survival at 30 days after the operation was analyzed by using a variety of risk factors (appendix). Patients were first considered as a whole; as a second step, rates were given overall and by diabetes group to illustrate the association of factors on outcomes within the patients in groups D and ND.

The same variables were used to analyze 5-year actuarial survival, inclusive of the first month, for all patients. As a second step, the first month was withdrawn from the analysis, and the 5-year survival of patients who survived 1 month was evaluated to explore the weight of early mortality on late survival. All the analyses were repeated to evaluate the influence of diabetes on freedom from cardiac death. When some perioperative surgical strategies were evaluated, survival and freedom from cardiac death were considered at 10 years.

Definitions of terms 

Need of inotropic agents was defined as infusion of greater than 5 μg · kg⁻¹ · min⁻¹ dobutamine or any dose of epinephrine or norepinephrine for more than 12 hours.

Cerebrovascular accident (CVA) was defined as global or focal neurologic deficit lasting less (transient ischemic attack) or more (stroke) than 24 hours that could be evident after emergence from anesthesia or after first awaking without any neurologic deficits. CVA was diagnosed by a neurologist and confirmed with a brain computed tomographic scan.

Acute myocardial infarction was defined as enzymatic elevation, electrocardiographic signs of necrosis, new akinetic segments at echocardiography, and non-K⁺-related ventricular arrhythmias.

Acute renal failure was defined as a postoperative creatinine value of greater than 2.0 mg/dL for more than 24 hours if the preoperative value was less than 1.4 mg/dL or a 1-unit creatinine increase if the preoperative value was greater than 2.0 mg/dL.

Early major events were defined as the sum of death of any cause, CVA, acute myocardial infarction, low-output syndrome (defined as need for an intra-aortic balloon pump, inotropic drugs for >12 hours, or both), need for mechanical ventilation for more than 24 hours in the absence of low-output syndrome, acute renal insufficiency (defined as blood creatinine level >2.0 mg/dL and 2 times the preoperative value), or acute renal failure (need for ultrafiltration without a related operation), gastrointestinal complications with or without related surgery.

Cardiac death was defined as any cardiac-related death, sudden and unknown.

Statistical analysis 

All continuos variables were expressed as means ± SD. Groups were compared by means of unpaired 2-tailed t testing in case of normally distributed factors, whereas Mann-Whitney tests were used in case of nonnormally distributed variables, and χ² tests (Pearson χ² and Fisher exact tests) were used for categoric variables. Stepwise logistic regression was used to select the independent variables that could predict death of any cause. Actuarial survival curves were obtained with the Kaplan-Meier method. Statistical significance was calculated with the log-rank test. Cox analysis was used to evaluate the independent risk factors for reduced late survival. All the multivariable analysis included univariate variables with P values of less than .2. Results of stepwise logistic regression were expressed as odds ratios with associated 95% confidence limits and P values. Results of Cox analysis were expressed as hazard ratios, 95% confidence limits, and P values. The SPSS software (SPSS, Chicago, Ill) was used for all analyses in this study.

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Results 

Early mortality 

During the first 30 days after the operation, 72 (2.2%) patients died, 25 (3.3%) in group D and 49 (1.9%) in group ND (P = .023). Table 3 summarizes the postoperative data.

Table 3. Early postoperative data according to groups ND and D

AMI, Acute myocardial infarction; IABP, intra-aortic balloon pump; CK-MB, creatine kinase muscle and brain; ICU, intensive care unit.

The results of stepwise logistic regression are shown in Table 4. Diabetes was not a risk factor for higher 30-day mortality.

Table 4. Stepwise logistic regression: Independent risk factors for increased early mortality, any death, and cardiac deaths

HR, Hazard ratio; CL, confidence limit; EF, ejection fraction; AMI, acute myocardial infarction; CHF, chronic heart failure; CRF, chronic renal failure; AF, atrial fibrillation.

The incidence of cardiac-related 30-day mortality was 1.3% (45 patients), 2.2% (17 patients) in group D and 1.1% (28 patients) in group ND (P = .016). The incidence of cardiac deaths was higher in group D (17/25 [68.0%]) than in group ND (28/49 [57.1%]) but not significantly (P = .511). Results of stepwise logistic regression are also summarized in Table 4. The analysis showed that diabetes was an independent factor for increased 30-day cardiac-related mortality. Again, early survival was not influenced by any technical aspect.

Late actuarial survival 

During the follow-up period, 137 (4.1%) patients died, 32 (4.2%) in group D and 105 (4.0%) in group ND. Five-year overall actuarial survival, first month included, was 93.5% ± 0.5%, 93.9% ± 0.6% in group ND and 92.5% ± 1.1% in group D (P = .0304, Figure 1).

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• Fig. 1. 

  Five-year actuarial survival (first month included): group D (solid line) versus group ND (dashed line).

Table 5 shows the independent predictors of lower survival at the Cox analysis. Diabetes was not an independent predictor of higher late mortality.

Table 5. Cox analysis: Independent risk factors for increased mortality, any death, and cardiac deaths

HR, Hazard ratio; CL, confidence limit; EF, ejection fraction; AMI, acute myocardial infarction; CHF, chronic heart failure; CRF, chornic renal failure.

Seventy-three (2.2%) patients died of cardiac causes, 20 (2.6%) in group D and 53 (2.0%) in group ND. The incidence for cardiac death was higher in group D (20/32 [62.5%]) than in group ND (53/105 [50.5%]). Freedom from cardiac death, first month included, was 96.3% ± 0.4%, 94.9% ± 0.9% in group D and 96.6% ± 0.4% in group ND (P = .0155, Figure 2).

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• Fig. 2. 

  Five-year freedom from cardiac death (first month included): group D (solid line) versus group ND(dashed line).

The results of Cox analysis are also shown in Table 5 . Now diabetes is again a risk factor for increased incidence of cardiac deaths. Interestingly, the use of saphenous vein graft (SVG) on the left anterior descending artery (LAD) appeared as a new risk factor, emphasizing a direct effect of this graft on late cardiac mortality.

Late actuarial survival of patients who survived for 30 days 

Five-year actuarial survival, with the exclusion of the first month, was 95.7% ± 0.4%, 95.6% ± 0.9% in group D and 95.7% ± 0.5% in group ND (Figure 3, P = .3642).

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• Fig. 3. 

  Five-year actuarial survival (first month excluded): group D (solid line) versus group ND (dashed line).

Results of Cox analysis are shown in Table 6.

Table 6. Cox analysis: Independent risk factors for increased late mortality (first month excluded), all causes and cardiac causes

HR, Hazard ratio; CL, confidence limit; EF, ejection fraction; AMI, acute myocardial infarction; CRF, chronic renal failure.

Freedom from cardiac death was 97.8% ± 0.3%, 97.3% ± 0.8% in group D and 97.9% ± 0.4% in group ND (Figure 4, P = .2389).

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• Fig. 4. 

  Five-year freedom from cardiac death (first month excluded): group D (solid line) versus group ND (dashed line).

Results of Cox analysis are also shown in Table 6 . Diabetes was no longer a risk factor once patients who died in the first 30 days were excluded.

Results according to preoperative treatment 

The preoperative treatment of diabetes did not affect early mortality (group OT, 18/596 [3.0%]; group IT, 7/171 [4.1%]). Five-year survival was also similar (94.64% ± 1.8% in group IT vs 92.0% ± 1.3% in group OT, P = .1850), as was freedom from cardiac death after 5 years (97.1% ± 1.3% in group IT vs 94.4% ± 1.1% in group OT, P = .1225).

Analyzing the patients who survived 30 days, 5-year survival was not significantly better in group IT (98.6% ± 1.0%) than in group OT (94.8% ± 1.1%), even if Cox analysis did not confirm this hypothesis. Freedom from cardiac-related death was not different in either group (99.4% ± 0.6% in group IT vs 96.7% ± 0.9% in group OT).

There were no statistically significant differences in short- or long-term mortality for diabetic patients treated perioperatively with insulin versus those who were not.

Results according to perioperative surgical strategy 

Tables 7 and 8 show 10-year survival and 10-year freedom from cardiac death according to some technical variables used during the procedure.

Table 7. Ten-year (first month included) survival according to same surgical aspects (univariate analysis)

All intermittent antegrade; no statistical difference was present when comparing groups. ITA, Internal thoracic artery; BITA, bilateral internal thoracic artery; TAMR, total arterial myocardial revascularization; CPL, cardioplegia.

Table 8. Ten-year (first month included) freedom from cardiac death according to same surgical aspects (univariate analysis)

All intermittent antegrade; no statistical difference was present when comparing groups. ITA, Internal thoracic artery; BITA, bilateral internal thoracic artery; TAMR, total arterial myocardial revascularization; CPB, cardiopulmonary bypass; CPL, cardioplegia.

Even if there is an evident benefit at the univariate analysis in using extensive arterial grafting, the Cox analysis failed to confirm this hypothesis. Only the use of SVG on LAD was a risk factor for increased incidence of cardiac deaths with and without the exclusion of the first month (Table 5, Table 6 ).

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Discussion 

Because morbidity and mortality caused by ketoacidosis and infections have a low incidence, coronary artery disease assumes a larger responsibility as a cause of death in diabetic patients.²⁸, ²⁹ The overall prevalence of coronary disease is as high as 55% among adult diabetic patients compared with 2% to 4% for the general population.³⁰ In a large autopsy study 91% of the patients with adult diabetes and no known coronary artery disease had severe narrowing of at least one major coronary artery, and 83% had severe 2- or 3-vessel involvement.³¹ The relative risk of myocardial infarction is 50% greater in diabetic men and 150% greater in diabetic women. Similarly, diabetic men have sudden death 50% more often and diabetic women 300% more often than do their age-matched nondiabetic counterparts.³² The mortality for myocardial infarction is higher than in nondiabetic patients³³, ³⁴ with³⁵ or without³⁶, ³⁷ thrombolytic therapy. Furthermore, the presence of diabetes mellitus is an independent predictor of cardiac mortality, which ranges from 26% to 62% in the first year after myocardial infarction and can reach 79% by 5 years.³⁸, ³⁹

Diabetic patients with multivessel coronary disease who undergo myocardial revascularization, both surgical and interventional, are considered at high risk for early and late death.¹, ², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹ Because other reports were not in agreement with these findings,¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²² we tried to find a personal answer to this problem by analyzing our database, which included patients operated on during 12 years.

The analysis of 30-day mortality showed that diabetes is a univariate risk factor for higher early mortality, but multivariable analysis rejected this hypothesis. Analysis of a large cohort of patients in a New York State database found that diabetes was a risk factor in 2 different periods: 1992 to 1995 and 1996.¹¹, ¹² This finding was confirmed by others.⁷, ⁸ However, other reports failed to identify diabetes as a risk factor in the general population¹⁸, ¹⁹, ²⁰, ²² or in the elderly.²¹

In our opinion 30-day mortality is influenced by technical details more than by the disease itself. Even if no surgical aspect was able to influence the 30-day outcome in diabetic patients, some aspects allowed a reduction of mortality more in group D than in group ND. Use of SVG on LAD in group D was related to high mortality (4/53 [7.5%]); on the contrary, when the left internal thoracic artery was used, the mortality showed a 2.6-fold reduction (21/714 [2.9%]). The same aspect allowed a minor reduction in group ND (from 3.0% to 1.8%, 1.7-fold). The huge application of the non-CPB strategy reduced the early mortality from 4.0% to 2.0% in group D (2-fold) and from 2.1% to 1.5% in group ND (1.4-fold). Cumulating all these small and apparently not influential improvements, diabetic patients are no longer at higher risk for 30-day mortality.

However, if only cardiac mortality in considered, diabetes appears to have a significant influence on early outcome because the relative incidence of cardiac deaths is higher in group D than in group ND. The anatomic aspect of the disease (diffuse coronary disease, small vessels, and diffuse calcifications) can explain a higher cardiac mortality.

Late survival, including 30-day mortality, showed, at univariate analysis, that diabetes was a risk factor, but the Cox analysis did not confirm this finding. Excluding 30-day mortality, diabetes was not a risk factor at either univariable or multivariable analysis.

When only cardiac deaths were considered, diabetes was a risk factor both at the univariable and multivariable analysis for increased early cardiac mortality and for reduced life expectancy as a result of cardiac death. However, when the analysis included only the patients who survived 30 days, diabetes disappeared as a risk factor both at univariable and multivariable analysis, showing that the influence of diabetes on survival without cardiac death is mainly expressed during the first postoperative month.

Other reports show clearly that diabetes is an important risk factor for late survival. Herlitz and colleagues⁶ showed that real 2-year survival was 86.1% in diabetic and 93.5% in nondiabetic patients (P < .0001). At the multivariable analysis, diabetes had a relative risk of 1.7. Morris and coworkers⁴⁰ reported a 5-year survival of 80% in diabetic patients and 91% in nondiabetic patients and an 8-year survival of 66% and 84%, respectively (P < .0001). Diabetes was an independent risk factor with a P value of .0001. Smith and associates⁴¹ showed a 15-year survival of 40% in diabetic and 60% in nondiabetic patients. Diabetes was a strong independent risk factor (P = .0001) but only in the late phase (>1 year after the operation). The same findings were confirmed by other studies.⁸, ⁹, ¹⁰ Diabetes was rarely not recognized as an independent risk factor for late survival, often only in subgroups of patients.¹⁹ When freedom from cardiac death was considered, diabetes was again a risk factor. Pick and colleagues⁹ found that diabetes was an independent risk factor both for 10-year overall (risk hazard ratio, 2.94) and cardiac (hazard ratio, 1.73) mortality. Globally, diabetes was a risk factor in the late period, starting the first year after the procedure.

Our findings are in contrast with those in many of the published studies on this topic. Logically, if diabetic patients in the general population have higher mortality than nondiabetic patients as a result of cardiac causes, it is reasonable that a diabetic patient who undergoes myocardial revascularization has a life expectancy better than that of a nonoperated patient and similar to that of a nondiabetic patient. Even if diabetes was a risk factor for higher cardiac 5-year mortality, this finding was the consequence of a higher early cardiac mortality (2.2% in group D vs 1.1% in group ND, P = .016) and not of a late higher mortality.

In fact, survival from surgical intervention was not found to be different for diabetic versus nondiabetic patients who survived to 1 month. The preoperative treatment of diabetic patients did not influence the outcome. Surprisingly, insulin-treated patients showed a high long-term survival (94.6% by 5 years).

Perhaps long-term treatment with insulin, because antidiabetic centers are widely diffused, can better control hyperglycemia, lowering the complication rate in the long term. However, the sample size is small, and definitive conclusions can not be drawn.

Our analysis was not able to show improvement related to any technical aspect during the operation. Early and late outcomes of diabetic patients were not influenced by use of SVG on LAD. Conversely, nondiabetic patients were influenced by use of SVG on LAD only in the analysis of freedom from cardiac death, both early and late, with or without the inclusion of the first month.

This is in contrast with other reports⁹, ¹⁵, ⁴² that show a better outcome in diabetic patients if a single or a double internal thoracic artery is used. We were not able to find any benefit with the use of bilateral internal thoracic arteries in nondiabetic patients, and the use of left internal thoracic arteries to LAD demonstrated an advantage only for cardiac deaths. This is not easy to explain. We think that the patency rate of the SVG in the 1990s is perhaps better than the patency rate of the SVG in the 1980s. Worldwide use of antiplatelet agents, as well as statins, can contribute to this theoretic benefit. Moreover, the mean follow-up in our series is shorter than in other reports,⁹, ⁴² and some authors⁴⁰ did not use a multivariable analysis to demonstrate their hypothesis.

The similar late outcome in diabetic and nondiabetic patients after a mean follow-up of 50 months suggests that the effect of surgical intervention in diabetic patients is striking. The huge cardiovascular mortality is highly reduced after myocardial revascularization, and the risks of myocardial infarction with the related mortality are also reduced. However, the incidence of cardiac deaths remains higher than that in nondiabetic patients, although this finding is limited to the first 30 days after the operation. The price to pay for diabetes seems today smaller than in the past.

One must take care with interpretations of subgroup analyses. Lack of statistical significance might simply be a lack of statistical power because of the reduced sample size. Statistical significance might be due to spurious results, which are expected with multiple comparisons.

In multivariable models one must remember that not only the factors in the model but the factors in the univariable analyses were considered. Therefore any borderline statistical result should be considered especially exploratory.

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Appendix 

Appendix. List and definition of variables

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References 

1. Alderman E, Bourassa M, Brooks MM, et al.  Influences of diabetes on 5-year mortality and morbidity in a randomized trial comparing CABG and PTCA in patients with multivessel disease. The Bypass Angioplasty Revascularization Investigation (BARI). Circulation. 1997;96:1761–1769
   • View In Article
   • MEDLINE
2. Barsness GW, Peterson ED, Magnus Ohman E, et al.  Relationship between diabetes mellitus and long-term survival after coronary bypass and angioplasty. Circulation. 1997;96:2551–2556
   • View In Article
   • MEDLINE
3. Alderman EL, Corley SD, Fisher LD, et al.  Five- year angiographic follow-up of factor associated with progression of coronary artery disease in the Coronary Artery Surgery Study (CASS). J Am Coll Cardiol. 1993;22:1141–1154
   • View In Article
   • Abstract
   • Full-Text PDF (1562 KB)
   • CrossRef
4. Fietsam RJ, Basset J, Glover JL. Complication of coronary artery surgery in diabetic patients. Am Surg. 1996;57:551–557
   • View In Article
   • MEDLINE
5. Cohen Y, Raz I, Gideon M, Mozes B. Comparison of factors associated with 30-day mortality after coronary artery bypass grafting in patients with versus without diabetes mellitus. Am J Cardiol. 1998;81:7–11
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (60 KB)
   • CrossRef
6. Herlitz J, Wognsen BG, Emanuelsson H, et al.  Mortality and morbidity in diabetic and nondiabetic patients during a 2-year period after coronary artery bypass grafting. Diabetes Care. 1996;19:698–703
   • View In Article
   • MEDLINE
7. Weintraub WS, Stein B, Gebhart SSP, et al.  The impact of diabetes on the initial and long term outcome of coronary artery bypass surgery. [abstract] Circulation. 1995;92(suppl I):643–644
   • View In Article
8. James TW, Quinton HB, Birkmeyer JD, et al.  Diabetes and coronary artery bypass graft surgery risk. [abstract] Circulation. 1996;94(suppl I):412
   • View In Article
9. Pick AW, Orszulak TA, Anderson BJ, et al.  Single versus bilateral internal mammary artery graft: 10-year outcome analysis. Ann Thorac Surg. 1997;64:599–605
   • View In Article
   • MEDLINE
   • CrossRef
10. Accola KD, Jones EL, Craver JM, et al.  Bilateral mammary artery grafting: avoidance of complications with extended use. Ann Thorac Surg. 1993;56:872–879
    • View In Article
    • MEDLINE
    • CrossRef
11. Hannan EL, Kilburn H, Racz M, et al.  Improving the outcomes of coronary artery bypass surgery in New York State. JAMA. 1994;271:761–766
    • View In Article
    • MEDLINE
12. Koegh BE, Kinsman R. Database report 1998. In: National adult cardiac surgical data. Society of Cardiothoracic Surgery of Great Britain and Ireland. www.scts.org/sctsdbr98.pdf.
    • View In Article
13. Weintraub WS, Stein B, Kosinski A, et al.  Outcome of coronary artery bypass surgery versus coronary angioplasty in diabetic patients with multivessel coronary artery disease. J Am Coll Cardiol. 1998;31:10–19
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (285 KB)
    • CrossRef
14. Detre KM, Guo P, Holubkov R, et al.  Coronary revascularization in diabetic patients. A comparison of the randomized and observational components of the Bypass Angioplasty Revascularization Investigation (BARI). Circulation. 1999;99:633–640
    • View In Article
    • MEDLINE
15. Hirotani T, Kameda T, Kumamoto T, et al.  Effects of coronary artery bypass grafting using internal mammary arteries for diabetic patients. J Am Coll Cardiol. 1999;34:532–538
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (214 KB)
    • CrossRef
16. Clement R, Rousou JA, Engelman RM, et al.  Perioperative morbidity in diabetics requiring coronary artery bypass surgery. Ann Thorac Surg. 1988;46:321–323
    • View In Article
    • MEDLINE
    • CrossRef
17. Kurlansky PA, Dorman MJ, Galbut DL, et al.  Bilateral internal mammary artery grafting in women: a 21-year experience. Ann Thorac Surg. 1996;62:63–69
    • View In Article
    • MEDLINE
    • CrossRef
18. Berreklouw E, Schonberger JP, Bavinck JH, et al.  Similar hospital morbidity with the use of one or two internal thoracic arteries. Ann Thorac Surg. 1994;57:1564–1572
    • View In Article
    • MEDLINE
    • CrossRef
19. Gardner TJ, Greene PS, Rykiel MF, et al.  Routine use of the left internal mammary artery graft in the elderly. Ann Thorac Surg. 1990;49:188–194
    • View In Article
    • MEDLINE
    • CrossRef
20. Horvath KA, DiSesa VJ, Peigh PS, et al.  Favorable results of coronary artery bypass grafting in patients older than 75 years. J Thorac Cardiovasc Surg. 1990;99:92–96
    • View In Article
    • MEDLINE
21. Wei He G, Acuff TE, Ryan WH, et al.  Determinants of operative mortality in elderly patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg. 1994;108:73–81
    • View In Article
    • Abstract
    • Full Text
22. Higgins TL, Estafanous FG, Loop FD, et al.  Stratification of morbidity and mortality outcome by preoperative risk factors in coronary artery bypass patients. JAMA. 1992;267:2344–2348
    • View In Article
    • MEDLINE
23. Salerno TA, Houck JP, Barrozo CA, et al.  Retrograde continuous warm blood cardioplegia: a new concept in myocardial protection. Ann Thorac Surg. 1991;51:245–274
    • View In Article
    • MEDLINE
    • CrossRef
24. Buffolo E, Silva de Andrade JC, Rodrigues Branco JN, et al.  Coronary artery bypass surgery without cardiopulmonary bypass. Ann Thorac Surg. 1996;61:63–66
    • View In Article
    • MEDLINE
    • CrossRef
25. Calafiore AM, Di Giammarco G, Teodori G, et al.  Recent advances in multivessel coronary grafting without cardiopulmonary bypass. Heart Surg Forum. 1998;1:20–25
    • View In Article
    • MEDLINE
26. Calafiore AM, Di Giammarco G. Complete revascularization with three or more arterial conduits. Semin Thorac Cardiovasc Surg. 1996;8:15–23
    • View In Article
    • MEDLINE
27. Loop FD, Lytle BW, Cosgrove DM, et al.  Influence of the internal-mammary-artery graft on 10-year survival and other cardiac events. N Engl J Med. 1986;334:216–219
    • View In Article
    • MEDLINE
    • CrossRef
28. Abbot RD, Donahue RP, Kannel WB, et al.  The impact of diabetes on survival following myocardial infarction in men vs women: the Framingham Study. JAMA. 1988;260:3456–3460
    • View In Article
    • MEDLINE
29. Stamler J, Vaccaro O, Neaton JD, et al.  Diabetes, other risk factors, and 12 year cardiovascular mortality from men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care. 1993;16:434–444
    • View In Article
    • MEDLINE
30. Fein F, Scheuer J. Heart disease in diabetes mellitus: theory and practice. In:  Rifkin H,  Potre D editor. New York: Elsevier; 1990;p. 812–823
    • View In Article
31. Feid FS. Heart disease in diabetes. Cardiovasc Rev Rep. 1982;3:877–893
    • View In Article
32. Waller B, Palumbo P, Roberts W. Status of the coronary arteries at necropsy in diabetes mellitus with onset after age 30 years. Am J Med. 1980;69:498–506
    • View In Article
    • Abstract
    • Full-Text PDF (925 KB)
    • CrossRef
33. Jacoby RM, Nesto RW. Acute myocardial infarction in the diabetic patients: pathophysiology, clinical course and progress. J Am Coll Cardiol. 1992;20:736–744
    • View In Article
    • Abstract
    • Full-Text PDF (761 KB)
    • CrossRef
34. Nesto RW, Philips RT, Kett KG, et al.  Angina and exertional myocardial ischemia in diabetic and non diabetic patients: assessment by thallium scintigraphy. Ann Intern Med. 1988;108:170–175
    • View In Article
    • MEDLINE
35. Barbash GI, White HD, Modan M, et al.  Significance of diabetes mellitus in patients with acute myocardial infarction receiving thrombolytic therapy. J Am Coll Cardiol. 1993;22:707–713
    • View In Article
    • Abstract
    • Full-Text PDF (1323 KB)
    • CrossRef
36. Rytter L, Troelsen S, Beck-Nielsen H. Prevalence and mortality of acute myocardial infarction in patients with diabetes. Diabetes Care. 1985;8:230–234
    • View In Article
    • MEDLINE
37. Stone PH, Muller JE, Hartwell T, et al.  The effect of diabetes mellitus on prognosis and serial left ventricular function after acute myocardial infarction: contribution of both coronary disease and diastolic left ventricular dysfunction to adverse prognosis. J Am Coll Cardiol. 1989;14:49–57
    • View In Article
    • Abstract
    • Full-Text PDF (896 KB)
    • CrossRef
38. Smith JW, Marcus F, Serokman R. Prognosis of patients with diabetes mellitus after acute myocardial infarction. Am J Cardiol. 1984;54:718–721
    • View In Article
    • MEDLINE
    • CrossRef
39. Schechtman K, Capone R, Kleiger R, et al.  Differential risk pattern associated with 3 month as compared with 3-12 month mortality and reinfarction after non-Q wave myocardial infarction. J Am Coll Cardiol. 1990;15:940–947
    • View In Article
    • Abstract
    • Full-Text PDF (1504 KB)
    • CrossRef
40. Morris JJ, Smith LR, Jones RH, et al.  Influence of diabetes and mammary artery grafting on survival after coronary bypass. Circulation. 1991;84(suppl III):275–284
    • View In Article
41. Smith RL, Harrell FE, Rankin S, et al.  Determinants of early versus late cardiac death in patients undergoing coronary artery bypass graft surgery. Circulation. 1991;84(suppl III):245–253
    • View In Article
42. Lytle BW, Blackstone EH, Loop FD, et al.  Two internal thoracic artery grafts are better than one. J Thorac Cardiovasc Surg. 1999;117:855–872
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (131 KB)
    • CrossRef