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Eur J Cardiothorac Surg 2006;30:881-886
© 2006 Elsevier Science NL

The beneficial effect of coronary-artery-bypass surgery on survival in patients with diabetic retinopathy

Takayuki Ohnoa,*, Jiro Andob, Minoru Onoa, Toshihiro Moritab, Noboru Motomuraa, Yasunobu Hiratab, Shinichi Takamotoa

a Department of Cardiothoracic Surgery, The University of Tokyo, Tokyo, Japan
b Department of Cardiology, The University of Tokyo, Tokyo, Japan

Received 2 July 2006; received in revised form 8 September 2006; accepted 25 September 2006.

* Corresponding author. Address: Department of Cardiothoracic Surgery, The University of Tokyo, 7-3-1, Hongo, Bunkyo-Ku, Tokyo 113-8655, Japan. Tel.: +81 3 5800 8654; fax: +81 3 5684 3989. (Email: takohno-tky{at}umin.net).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 References
 
Objective: The presence of retinopathy is a predictor of mortality following coronary revascularization in diabetics. We studied whether revascularization by coronary-artery-bypass surgery (CABG), as compared with percutaneous coronary intervention (PCI), influences the prognosis in diabetics with retinopathy. Methods: Between April 1996 and March 2004, 1489 patients underwent revascularization as an initial procedure. Among these a total of 319 diabetics underwent retinal examination prior to the initial revascularization. These patients were classified according to whether they had retinopathy and whether they had undergone CABG, either initially or after PCI. Mortality rates were estimated from the time of initial revascularization procedure. Results: The average follow-up from the time of initial revascularization was 48.2 ± 28.6 months. In 153 diabetics with retinopathy, 59 eventually underwent CABG. During the entire follow-up period, there were 2 (3.4%) deaths in diabetics with retinopathy who underwent CABG and 14 (14.9%) deaths in those who did not have CABG. Mortality curves differed significantly between the two groups (P = 0.007). After adjustment for risk factors, the relative risk of death was 0.13 afforded by CABG (95% CI, 0.03–0.62; P = 0.011). In 166 diabetics without retinopathy, mortality curves were similar between the patients who underwent CABG and those who did not have CABG (P = 0.94). Conclusions: CABG conferred a survival advantage in diabetics with retinopathy. In contrast, no survival advantage was evident in diabetics without retinopathy undergoing CABG. Retinal status should be taken into consideration when considering revascularization strategy for diabetics who have coronary artery disease.

Key Words: Diabetic retinopathy • Coronary-artery-bypass surgery • Percutaneous coronary intervention • Survival • CABG • Surgery • Diabetes mellitus • Statistics • Survival analysis


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 References
 
Diabetic retinopathy is a frequent and early sign of microvascular complication of diabetes, and the risk of retinopathy is directly related to the degree and duration of hyperglycemia [1,2]. Of all of the complications of diabetes, retinopathy presents the physician with the unique opportunity to directly visualize and grade the progression of the disease. Ophthalmologists have recognized that diabetics with advanced retinopathy are commonly in poor general health, and have reduced life expectancy [3–8]. Epidemiological evidences demonstrate that coronary artery disease is the leading cause of morbidity and mortality among diabetics with retinopathy [9–13]. Previous studies shown that the presence of diabetic retinopathy is a predictor of all-cause mortality following coronary-artery-bypass surgery (CABG) and percutaneous coronary intervention (PCI) [14,15]. So far, however, there are no published reports comparing the prognosis of coronary revascularization between CABG and PCI in diabetics with retinopathy. The purpose of this study was to evaluate whether revascularization by CABG, as compared with PCI, influences the mortality in diabetics with retinopathy.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Statistical analysis
 4. Results
 5. Discussion
 References
 
2.1 Patients
Between April 1996 and March 2004, 1489 consecutive patients underwent either CABG or PCI with bare-metal stent as an initial revascularization procedure at the University of Tokyo Hospital, Tokyo, Japan. Patients were eligible for inclusion in this study if: (1) they were considered to have diabetes if they had medical treatment (hypoglycemic agents or insulin injection) for diabetes or they had hemoglobin A1c > 6.5% at the time of initial revascularization; and (2) they had undergone ophthalmic examination at the department of ophthalmology for detection and treatment of retinopathy within 1 year prior to the initial revascularization. Patients were excluded if they needed concomitant major surgery (e.g., valve surgery, or resection of an aortic or left ventricular aneurysm, or resection of malignant tumor); or if they cardiogenic shock complicating an acute myocardial infarction within 24 h before the initial revascularization procedure. A total of 319 patients met these criteria. The assessment method of diabetic retinopathy was as described previously [14]. Briefly, the most recent ophthalmologic records up until the time of initial revascularization were used. The patients with retinopathy were grouped into three categories of retinopathy: those with mild-to-moderate nonproliferative diabetic retinopathy (NPDR); those with severe stage of NPDR; and those with proliferative diabetic retinopathy (PDR). The patients’ base-line characteristics concerning demographic data, medical history, coronary risk factors, angiographic data, and revascularization procedure data were collected from medical and surgical records. All initial and subsequent revascularization procedures (CABG and PCI) were documented for each patient during the entire follow-up period. All patients who underwent CABG, whether as an initial or a subsequent revascularization procedure, were regarded as subject to the protective effect of CABG. Therefore, patients were classified into four groups according to whether they had retinopathy and whether they had undergone CABG, either initially or after PCI. Death from all causes was the end point, and mortality rate were estimated from the time of the initial revascularization procedure. The findings reported in this study relate to data documented for all patients as of August 31, 2005.


   3. Statistical analysis
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
4. Results
 5. Discussion
 References
 
Data was analyzed using statistical software SPSS for Windows (version 10.0, SPSS, Japan). Descriptive data for continuous variables are presented as means with standard deviation (SD). Baseline characteristics of the patient groups were compared by chi-square test for categorical variables. Student's t-test was used for continuous variables. Mortality rates were estimated according to Kaplan–Meier method and were compared using the log-rank test. A Cox proportional-hazards model was used to estimate the relative risks of death that describe the beneficial effect of CABG. Baseline characteristics included in the Cox model were factors known to be important predictors of mortality after coronary revascularization in diabetics, and factors that differed between the CABG and PCI groups at the 0.05 significance level in this study. Two-sided P values of less than 0.05 were considered to be statistically significant.


   4. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
5. Discussion
 References
 
One hundred fifty-three (48.0%) diabetics had retinopathy and 166 (52.0%) did not. Among 153 diabetics with retinopathy, 63 patients were categorized as having mild-to-moderate NPDR, 24 as having severe stage of NPDR and 66 patients as having PDR. The baseline characteristics of the 319 patients according to the presence or absence of retinopathy are shown in Table 1 . Larger proportions of diabetics with retinopathy were treated with insulin injection, had renal dysfunction, and presented with silent myocardial ischemia compared with diabetics without retinopathy. The average duration of follow-up from the time of the initial revascularization procedure was 48.2 ± 28.6 months. During the entire follow-up, 16 of 153 diabetics with retinopathy died, and 3 of 166 diabetics without retinopathy died. Table 2 shows the causes of death in both groups. Of the 16 diabetics with retinopathy who died, 11 (68.8%) died from cardiac causes. The 4-year mortality was 10.0% for diabetics with retinopathy and 1.8% for diabetics without retinopathy. Mortality curves differed significantly according to the presence or absence of retinopathy (P = 0.0069) (Fig. 1A). After adjustments were made for older age (>65 years), treatment with insulin, silent myocardial ischemia, high serum creatinine (>1.4 mg/dl), and low ejection fraction (<50%), the presence of retinopathy was found to be an independent predictor of mortality (adjusted relative risk, 4.79; 95% confidence interval (CI), 1.35–16.96; P = 0.015).


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  		Table 1. Baseline characteristics of diabetic patients who underwent coronary revascularization according to the presence or absence of diabetic retinopathy a
 

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  		Table 2. Causes of death according to the presence or absence diabetic retinopathy during the entire follow-up
 

Figure 1
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  		Fig. 1. Kaplan–Meier estimates of the mortality following the initial revascularization procedure. Panel A shows the mortality according to the presence or absence of diabetic retinopathy. Panel B shows the mortality with respect to coronary-artery-bypass surgery (CABG). Patients who did not undergo CABG were treated only with percutaneous coronary intervention. DR denotes diabetic retinopathy. P values were calculated by the log-rank test.

 
Ninety-six of the 319 patients underwent CABG as their initial revascularization procedure, and an additional 22 of the remaining 223 patients underwent CABG sometime during the entire follow-up. Overall, morality curves differed significantly according to final status with respect to CABG (P = 0.027) (Fig. 1B). The base-line characteristics at the time of the initial revascularization procedure according to CABG status for the 153 diabetics with retinopathy and the 166 diabetics without retinopathy are shown in Table 3 . Patients who eventually underwent CABG were more likely to have three-vessel coronary disease, peripheral vascular disease (in the case of diabetics with retinopathy), a history of congestive heart failure, and decreased left-ventricular ejection fraction (in the case of diabetics without retinopathy), and to have low serum cholesterol level (in the case of diabetics without retinopathy) than those who did not undergo CABG. During the entire follow-up, 2 of the 59 diabetics with retinopathy who underwent CABG died, and 14 of the 94 diabetics who did not undergo CABG died. Mortality at 4 years was 2.9% and 17.0% in the two groups, respectively. Mortality curves differed significantly according to the presence or absence of CABG (P = 0.007) (Fig. 2 ). After adjustments for older age (>65 years), treatment with insulin, high serum creatinine (>1.4 mg/dl), silent myocardial ischemia, low ejection fraction (<50%), peripheral vascular disease, and three-vessel disease, the relative risk of death afforded by CABG was 0.13 (95% CI, 0.03–0.62; P = 0.011). In contrast, among diabetics without retinopathy, 1 of 59 patients who underwent CABG died and 2 of 107 patients who did not undergo CABG died. Mortality at 4 years was 1.7% and 1.9% in the two groups, respectively. Mortality curves were very similar between the patients who underwent CABG and those who did not undergo CABG (P = 0.94) (Fig. 2).


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  		Table 3. Baseline characteristics of diabetic patients according to final status with respect to coronary-artery-bypass surgery a
 

Figure 2
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  		Fig. 2. Kaplan–Meier estimates of the mortality following the initial revascularization procedure according to retinal status and with respect to coronary-artery-bypass surgery (CABG). Patients who did not undergo CABG were treated only with percutaneous coronary intervention. DR denotes diabetic retinopathy.

 

   5. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
References
 
In this study, compared with PCI, CABG decreased the risk-adjusted mortality in diabetics with retinopathy, whether performed as an initial or a subsequent revascularization procedure. In contrast, CABG did not appear to confer any survival advantage in diabetics without retinopathy. These findings suggest retinal status should be taken into consideration when considering revascularization strategy for diabetics who have coronary artery disease.

Previously, we examined the association between the presence of retinopathy and mortality in the 12 years after CABG in diabetics, and shown that diabetic retinopathy is a predictor of mortality [14]. In this study, however, during the average of follow-up of 4 years, mortality curves were similar between diabetics undergoing CABG with and without retinopathy. This is because (1) only one patient with retinopathy died during hospital period following CABG, and the excellent surgical result of retinopathy group contributes to the similarity of mortality curves between the two groups, and (2) the follow-up period was relatively short, and the longer follow-up might be required to detect differences in mortality. In contrast, during the short period of follow-up, among diabetics undergoing PCI alone mortality curves differed significantly according to the presence or absence of retinopathy. Kim and colleagues also demonstrated that the 2-year survival rate after PCI was worse in diabetics with retinopathy than in diabetics without retinopathy [15].

Once coronary artery disease is established, diabetics with retinopathy are at a higher risk of adverse cardiac events than diabetics without retinopathy [16–18]. However, there have been very few studies addressing adverse cardiac events after coronary revascularization in diabetics with retinopathy. Recently, we prospectively studied the association between the presence of diabetic retinopathy and the occurrence of adverse cardiac events following CABG [19]. In the 12 months of follow-up, 13 (50%) of the 26 diabetics with retinopathy had cardiac events, compared with 7 (15%) of the 48 diabetics without retinopathy (P = 0.002). This poor cardiac outcome in diabetics with retinopathy undergoing CABG was mainly due to the high prevalence of congestive heart failure in patients with advanced diabetic retinopathy. Briguori and colleagues studied the association between microvascular complications (retinopathy and nephropathy) and the occurrence of cardiac events including overall death, nonfatal myocardial infarction, and repeat revascularization following PCI with stenting [20]. At 12 months, cardiac events occurred in 34 (21%) of the 161 diabetics without microvascular complications, in 18 (40%) of the 45 diabetics with nephropathy, in 22 (51%) of the 43 diabetics with retinopathy, and in 25 (73.5%) of the 34 diabetics with both retinopathy and nephropathy (P < 0.001). In addition, the severity of diabetic retinopathy was shown to correlate with the incidence of in-stent stenosis after PCI, especially for proliferative retinopathy [21].

Bypass Angioplasty Revascularization trial reported a statistically significant survival advantage of CABG over PCI in diabetic population [22]. The present study indicates that the statistically significant advantage of CABG over PCI in diabetics was driven primarily by outcomes in diabetics with retinopathy. Coronary events occur at random and typically caused by disruption of nonobstructive atheromas. PCI is targeted at the existing ‘culprit’ lesion but not future lesions, and therefore, dose not reduce the risk of coronary events following revascularization. In contrast, CABG bypasses most of the epicardial vessels including those at risk for future events, which are responsible for most of the coronary events, and may render these events to be less fatal. Diabetics with retinopathy who carry a particularly high risk of future coronary events may benefit more from CABG than PCI, and therefore, would have a particularly strong indication for CABG.

To link the stage of diabetic retinopathy at the time of CABG with the grade of clinical advantage postoperatively is a very important issue. In the present study, in the diabetics who did not undergo CABG, 4 (10.3%) of the 39 diabetics with mild-to-moderate NPDR died, 3 (18.8%) of the 16 diabetics with severe stage of NPDR died, and 7 (17.9%) of the 39 diabetics with PDR died. In the diabetics who underwent CABG, one patient with severe stage of NPDR and one with PDR died. Because of the short follow-up duration and the limited number of patients, power to detect differences in clinical outcome was not sufficient among the patients with the more specific stage of diabetic retinopathy.

Several studies demonstrate that total arterial revascularization clearly improves the long-term outcome of patients undergoing CABG [23]. However, we found that total arterial revascularization was often difficult to be achieved especially in diabetics with advanced retinopathy. Bilateral internal-thoracic-artery (ITA) grafts results in a survival benefit exceeding a single ITA graft [24,25], but we are often reluctant to use bilateral ITA grafts in diabetics with advanced retinopathy who are at risk of developing postoperative mediastinitis. The radial artery is frequently used in composite arterial grafts, but we do not use this artery in diabetics with advanced retinopathy who are at risk of developing ‘future’ chronic renal failure requiring hemodialysis. The gastroepiploic artery is used to revascularize a right coronary artery lesion, but diabetic gastroenteropathy is sometimes associated with severe diabetes [26]. Considering that graft source and durability are limited among diabetic patients, we think that it would be important for cardiac surgeons to know the retinopathy stage when CABG confer the most clinical advantage.

The present study has some caveats. First, this study included diabetics undergoing eye examination at any time from 1 year up until CABG. Hence, the status of the retina at the time of initial revascularization procedure may have been underestimated. Second, diabetics who did not have an eye examination within one year prior to the initial revascularization procedure were not included in this study. Such patients might have either a short history of diabetes or inadequate compliance with diabetic care. The potential selection bias by including only patients having an eye examination might not be generalizable to more heterogeneous populations of diabetic patients who require coronary revascularization. Third, data on the cause of death were obtained retrospectively. Therefore, we could not estimate precisely the effect of CABG on cardiac outcome.

Acknowledging these caveats, we are much encouraged by the apparent beneficial of CABG on the mortality of diabetics with retinopathy. The present study did not include the patients undergoing PCI with drug-eluting stents because we began to use drug-eluting stents in March 2004. There is the possibility that drug-eluting stents might improve the prognosis relative to bare-metal stents, but the available data suggest that they may not offer any benefit other than to reduce the need for repeat revascularization, whereas the risk of coronary events is not affected.

In summary, CABG, whether as an initial or a subsequent revascularization procedure, conferred a survival advantage among diabetics with retinopathy. In contrast, no survival advantage was evident in diabetics without retinopathy undergoing CABG. Therefore, retinal status should be used as guide for treatment decision in revascularization in diabetics, and diabetics with retinopathy would have a particularly strong indication for CABG.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 References
 

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