Ann Thorac Surg 2009;87:1090-1096. doi:10.1016/j.athoracsur.2009.01.039
© 2009 The Society of Thoracic Surgeons
Original Articles: Adult Cardiac
Impact of Off-Pump Techniques on Sex Differences in Early and Late Outcomes After Isolated Coronary Artery Bypass Grafts
Shao-peng Fu, MD*,
Zhe Zheng, MD*,
Xin Yuan, MD,
Shi-ju Zhang, MD,
Hua-wei Gao, MD,
Yan Li, MD,
Sheng-shou Hu, MD*
Chinese Academy of Medical Science, Peking Union Medical College, Fuwai Hospital & Cardiovascular Institute, Department of Surgery, Research Center for Cardiovascular Regenerative Medicine, Beijing, People's Republic of China
Accepted for publication January 16, 2009.
* Address correspondence to Dr Hu, Department of Surgery, Research Center for Cardiovascular Regenerative Medicine, Cardiovascular Institute and FuWai Hospital, Peking Union Medical College, Chinese Academy of Medical Science, 167A Beilishi Rd, Xi Chen District, Beijing, 100037, People's Republic of China (Email: shengshouhu{at}yahoo.com).
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Abstract
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Background: Off-pump coronary artery bypass graft surgery (OPCAB) is associated with lower early mortality and benefits women disproportionately. The objective of this study was to assess the impact of off-pump techniques on sex differences in late outcomes.
Methods: We reviewed a clinical database of consecutive patients who underwent isolated coronary artery bypass graft surgery (CABG) at FuWai Hospital from 1999 to 2005. Logistic regression analysis and proportional hazards modeling were used to investigate whether sex or surgery type were associated with early mortality and late outcomes (mortality, major cardiac and cerebral event).
Results: Female sex was associated with higher rates of early death (adjusted odds ratio, 4.726; p < 0.0001), and OPCAB benefited women disproportionately for early mortality. Odds ratio of death for women versus men was 4.726 (p < 0.0001) in the conventional CABG on cardiopulmonary bypass group; odds ratio of death for women versus men was 1.344 (p = 0.5617) in the OPCAB group. Analysis of late outcomes indicated that OPCAB and cardiopulmonary bypass resulted in similar survival, regardless of sex. The women versus men hazard ratio of late mortality after CABG on cardiopulmonary bypass and OPCAB for women was 0.851 (p = 0.4984) and 0.650 (p = 0.2005), respectively. Women treated with OPCAB were less likely to be free from major cardiac and cerebral events than men treated with OPCAB. The women versus men hazard ratio of major cardiac and cerebral events after CABG on cardiopulmonary bypass and OPCAB for women was 1.079 (p = 0.4992) and 1.299 (p = 0.0387), respectively.
Conclusions: Compared with men, women are a high-risk group and benefit from off-pump operation in terms of early mortality after CABG. Conversely, during follow-up, women have high adjusted risks of major cardiac and cerebral events after OPCAB.
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Introduction
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Off-pump coronary artery bypass graft surgery (OPCAB) is becoming a widely used technique and challenges the conventional on-pump coronary artery bypass graft surgery (CABG) as the standard surgical therapy for coronary artery diseases [1]. The outcomes of these two kinds of CABG have been compared in a large number of studies, and many found that OPCAB is associated with lower morbidity and lower mortality compared with CABG on cardiopulmonary bypass (CPB), especially in early postoperative periods [2–6]. The high-risk patients with comorbidities particularly profit from avoiding CPB and show significantly lower hospital mortality [2, 3, 7–9].
Female sex has been reported to be an independent predictor of operative mortality in patients undergoing CABG [10–15]. The hypothesis proposed to explain the sex differences is that female patients tend to be older and have more complicated clinical presentations than male patients. Although it is intuitive to suggest that women should benefit from OPCAB and several clinical studies have corroborated this idea [4, 5, 13, 14, 16, 17], little information is available concerning sex differences in late results of OPCAB.
The present study retrospectively reviewed the early and late outcomes of a significant number of patients of both sexes who underwent CABG with the objective to determine whether OPCAB may benefit women in terms of late outcomes.
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Patients and Methods
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Data Collection
This study was approved by the institutional research board and ethics committee of the Cardiovascular Institute and FuWai Hospital, Chinese Academy of Medical Science in compliance with the Declaration of Helsinki, and individual patient consent was waived. The data of consecutive patients who underwent CABG in the FuWai Hospital affiliated with the Chinese Academy of Medical Science between 1999 and 2005 were gathered. Patients who had CABG in combination with valvular or other cardiac surgery were excluded. Next, to minimize the impact of surgical procedures with a learning curve on long-term outcomes, the first 10 CABG/CPB patients and the first 10 OPCAB patients for each surgeon were excluded. This yielded a study group of 5,359 patients (71 in-hospital deaths and 5,288 discharged alive). These medical records, prospectively entered and retrospectively reviewed, included demographic data, preexisting comorbidities, risk factors, operative strategy, and clinical outcomes.
All patients discharged alive (5,288) were followed up, and mean follow-up duration was 57.96 ± 23.46 months (97.1% complete). Patients were followed up regularly in three ways: by telephone, by mail, or by medical records. Adverse events in the long term were confirmed by their medical records and reviewed by an experienced physician. Our primary end point was all-cause death and major cardiac and cerebral event (MACCE), which was a composite of cardiac deaths, revascularization, nonfatal myocardial infarction, or stroke.
Interventions and Surgical Technique
Operations for OPCAB and CABG/CPB were performed at the discretion of any of 10 faculty surgeons whose surgery type selections varied with personal preference. During OPCAB surgery, several cardiac positioning techniques and coronary artery stabilizers were adopted as previously described [18]. Procedures for CABG/CPB was performed with standard CPB techniques, using cold antegrade and retrograde blood cardioplegia and moderate systemic hypothermia (30° to 34°C).
Statistical Analysis
Before analysis, candidate risk factors deemed potentially important predictors of clinical outcomes were selected (Table 1). The definitions of the variables used were according to EuroSCORE [19] or the Cardiothoracic Surgery Network database (http://www.ctsnet.org/).
Statistical significance was defined as a probability value less than 0.05. Univariate comparisons of preoperative characteristics were performed between subgroups. Chi-square (
2) or Fisher's exact tests were used to compare the categorical variables; Student's t or Wilcoxon rank-sum tests were used to compare the continuous variables. The difference in unadjusted inpatient mortality was examined with the 2 test. Patients were stratified into subgroups according to the interventions of surgical type or sex. All selected variables were used in separate logistic regression models to address the impact of sex and treatment (CABG/CPB versus OPCAB) or their interaction on early outcomes.
Unadjusted late mortality data were analyzed with Kaplan–Meier curves stratified by sex. Risk-adjusted late outcomes (mortality and MACCE) between sexes after OPCAB and CABG/CPB were compared by the creation of stepwise Cox proportional hazards models. All of the available patient risk factors were used as candidate independent variables. Also, female sex was forced into the model as an independent variable for purposes of obtaining the hazard ratio (HR) and 95% confidence interval (CI) for women. To test for selection bias, we conducted a propensity analysis. Propensity scores [20] were calculated for each patient based on all risk factors (including surgeon identity and year of operation) available preoperatively. For the propensity score calculation, a multiple stepwise logistic regression model was used to predict type of procedure used. The resulting conditional probability of a patient undergoing CABG/CPB was the propensity score, and the propensity score was included as a covariate of risk in the final Cox proportional hazards models of outcomes [21].
These final models were used to assess the association between the outcomes and the selected risk predictors and to generate adjusted odds ratios of early mortality or HRs of late outcomes. Four preplanned female versus male comparisons were of interest: (1) early mortality in OPCAB patients, (2) early mortality in CABG/CPB patients, (3) late outcomes in OPCAB patients, and (4) late outcomes in CABG/CPB patients.
All analyses were performed with the SAS 9.1 software (SAS Institute, Cary, NC), and all probability values are two-tailed.
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Results
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Baseline Patient Characteristics
Table 1 shows baseline characteristics of all patients. Women and men were different in many variables. In general, women were significantly older, and had a higher incidence of mitral regurgitation (p = 0.0042), hypertension (p < 0.0001), hyperlipemia (p = 0.001), diabetes (p < 0.0001), blood product transfusion (p < 0.0001), angina (p = 0.004), and critical preoperative state (p = 0.047). On the other hand, men often were more likely to have a smoking history (p < 0.0001) and lower ejection fraction (p = 0.0007). Both women and men had a similar rate of left main coronary stenosis (p = 0.5034) and number of diseased coronary vessels (p = 0.0999).
Early Mortality
Early mortality was defined as death occurring during the operation or hospitalization after the operation. Of the 892 (16.64%) women enrolled, 33 (3.70%) died; of the 4,467 (83.36%) men enrolled, 38 (0.85%) died (unadjusted odds ratio, 4.478; 95% CI, 2.792 to 7.179; p < 0.0001). Using the EuroSCORE model, the predicted mortalities were 3.65% for women and 2.73% for men (Table 2). This measure more accurately reflected the degree of risk associated with each sex. By calculating the observed versus predicted mortality, the mortality rate of each sex was adjusted for their level of risk. A comparison of the two sexes showed that female adjusted mortality is more than three times that of males (1.01/0.31).
In Table 3, the estimated women versus men odds ratio and associated 95% confidence interval are displayed along with the associated c-statistics of the regression models. Female sex was found to be independently associated with increased early mortality after treatment with CABG (odds ratio, 2.285; p = 0.0037) or CABG/CPB (odds ratio, 4.726; p = 0.0110). In contrast, the women treated with OPCAB had outcomes statistically similar to men, with a risk-adjusted odds ratio of 1.344 (p = 0.1562) for death compared with men.
Late Outcomes
In this study, 5,288 patients were discharged alive (4,438 men and 850 women), and follow-up (57.96 ± 23.46 months) was 97.1% complete. The Kaplan–Meier survival curves for patients undergoing CABG/CPB or OPCAB stratified by sex are presented in Figures 1 and 2
respectively. There was no significant difference in survival between women and men treated with OPCAB (log-rank test p = 0.1351) and CABG/CPB (log-rank test p = 0.3780).
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Fig 1. Kaplan–Meier curves by sex for all-cause mortality for follow-up patients treated with coronary artery bypass graft surgery with cardiopulmonary bypass (CABG/CPB; p = 0.3780). Number of patients at risk is on the figure.
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Fig 2. Kaplan–Meier curves by sex for all-cause mortality for follow-up patients treated with off-pump coronary artery bypass graft surgery (OPCAB; p = 0.1351). Number of patients at risk is on the figure.
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The late mortality data were also analyzed with Cox proportional hazard models (Table 4). The estimated propensity score showed good discriminatory power (c-statistic = 0.906) as well as calibration characteristics by Hosmer-Lemeshow Goodness-of-Fit Test (p = 0.2578). The results were consistent with the findings of Kaplan–Meier survival analysis. Women and men treated with OPCAB did not differ in late mortality (HR, 0.650; 95% CI, 0.336 to 1.257; p = 0.2005); women and men treated with CABG/CPB had the same rate of late survival (HR, 0.851; 95% CI, 0.534 to 1.357; p = 0.4984).
Table 5
describes the results of Cox proportional hazard models for the analyzed MACCE. Women treated with OPCAB were significantly associated with an increased hazard of MACCE than their counterparts (HR, 1.279; 95% CI, 1.017 to 1.654; p = 0.0364). However, women treated with CABG/CPB were not associated with an increased hazard of MACCE (HR, 1.085; 95% CI, 0.875 to 1.346; p = 0.4569).
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Table 5 Cox Proportional Hazards Models for Late Major Cardiac and Cerebral Event Adjusted for Other Risk Factors
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Completeness of Revascularization
To determine whether the completeness of revascularization was different for women and men, an index of completeness of revascularization (ICOR) was calculated for each follow-up patient and compared between groups. The ICOR was defined as the number of distal anastomoses constructed divided by the number of diseased vessels reported on the preoperative coronary arteriogram. Table 6
showed that ICOR values were all significantly lower in women than in men and were significantly lower in patients treated with OPCAB than in those treated with CABG/CPB.
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Comment
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The main findings of this study were as follows. First, women undergoing CABG had a higher preoperative risk profile than their male counterparts. Second, OPCAB technique provides significant early mortality advantages, especially for women. During long-term follow-up, OPCAB and CABG/CPB resulted in similar survival, regardless of sex. However, the most striking finding in this investigation was that the rate of MACCE was significantly higher in women treated with OPCAB than in men treated with OPCAB or in women treated with CABG/CPB. Third, women treated with OPCAB received less-complete revascularization than men treated with OPCAB among follow-up patients.
The first finding is similar to a number of previous studies [22–25] that reported that women undergoing CABG had more comorbidities and a higher risk profile before surgery compared with men.
Several previous studies have also found that female sex is a risk factor for operative mortality after CABG. There is, however, little consensus about the underlying mechanisms. The possible explanations include the facts that female patients tend to be older and have a more complicated clinical presentation than male patients. We had initially anticipated that the higher prevalence of comorbid conditions would be responsible, to some extent, for the higher rate of early death in women, and the variables that have traditionally been associated with risk for early death were included in the logistics regression models. However, after adjusting for these factors by multivariable logistics regression analysis, female sex remained independently associated with a higher risk of early mortality. Therefore, the higher mortality of women after CABG must involve alternative mechanisms.
In an attempt to clarify whether CPB influenced the sex disparity after CABG, in this study, mortality data in a cohort of patients were grouped by sex and the interventions of OPCAB or CABG/CPB. Women receiving OPCAB treatment did not differ significantly from men treated with OPCAB in early mortality, whereas women receiving CABG/CPB had a distinctly higher rate of postoperative death than men treated with CABG/CPB. Our findings in the present study with respect to early mortality are similar to those of several recent studies. Patel and associates [16] collected data of a 10-year hospitalization cohort and found no significant difference in mortality between women and men, despite women requiring a longer hospitalization and having a greater incidence of sternal wound infection than men. A small clinical study from Bernet and colleagues [17] showed that in OPCAB surgery female sex did not play any predictive role for postoperative adverse events and complications influencing mortality. A large observational study from Puskas and coworkers [12] found that OPCAB was associated with a significant reduction in death among women and that it narrowed the sex disparity in clinical outcomes after CABG. Another clinical study by Puskas and associates [14] showed similar results. The present study showed that the higher early mortality in women after CABG can be explained, at least in part, by using CPB. The related mechanisms need to be explored by further research.
Despite previous reports and our results on the improved early survival of female patients achieved with OPCAB, it remains unclear whether CPB is an independent risk factor for late outcomes, and whether OPCAB is an important technique to improve late outcomes of female patients. Little information is available concerning sex-based differences in terms of late outcomes when OPCAB is involved. To fill this gap, our study reports the influence of OPCAB on sex difference in late outcomes. Puskas and colleagues [26] found that OPCAB and CPB result in similar survival, regardless of sex, after 10-year follow-up. However, their end point is all-cause mortality and does not include nonfatal events that are directly attributable to their surgical characteristics. Our results are similar to those of Puskas and coworkers when all-cause death is the end point: OPCAB and CABG/CPB result in similar survival, regardless of sex. However, when late MACCE is the end point, we found different results. In contrast to the early mortality results, an analysis of late MACCE demonstrated women treated with OPCAB had significantly higher MACCE rates than their male counterparts. On the other hand, the actuarial late MACCE of women and men was similar for CABG/CPB patients.
The observed difference in late outcomes that existed after OPCAB, despite extensive risk adjustment for women, is puzzling. This finding is important because it supplements our knowledge of late results of OPCAB technique for women. Although this new finding requires adequate clinical trial testing for confirmation in the future, we hope our results help to choose surgical revascularization strategy more accurately, especially in an era when there may be other evolving treatment options for women.
Why do women have less benefit for late outcomes from OPCAB technique? It is clear that women and men referred for CABG surgery represent two very different patient groups. Several investigations have consistently described that women undergoing CABG tend to be older and have a more complicated clinical presentation than men. Similar results were obtained in the present study. Women were significantly older and more often had mitral regurgitation, hypertension, hyperlipemia, diabetes, blood product transfusion, angina, and critical preoperative state. In the present analysis the most credible explanations, namely body habitus, demographic, medical profile, and surgeon identity, were tested as variables within our Cox proportional hazards models. Their inclusion in these Cox proportional hazards models did not negate the impact of sex or surgical technique on the risk-adjusted hazard ratios for late MACCE.
Some authors have proposed that the OPCAB procedure is more technically demanding than CABG/CPB, and smaller sizes of coronary arteries in women [27, 28] might lead to a more technically difficult anastomosis and less complete or effective revascularization [29–31]. Incomplete revascularization during CABG is associated with reduced late-term event-free survival [30–32]. To evaluate this possible explanation, the number of diseased vessels and the number of distal anastomoses were included in the Cox proportional hazards models. Moreover, an ICOR was calculated for each patient and compared between groups. The ICOR values were all slightly, but significantly, lower in females than in males and slightly, but significantly, lower in patients treated with OPCAB than in those treated with CABG/CPB. The ICOR value was lower for women treated with OPCAB than for those treated with CABG/CPB. The results of the present study showed that the higher late MACCE in women after OPCAB can be explained, at least in part, by having less completeness of revascularization.
Limitations and Strengths
The main limitation of this study is the retrospective nature of the data, although it is difficult to design a prospective trial based on sex. To control selection bias, a propensity model was developed to find significant predictors for procedure choice. Second, this study is conducted at a single hospital in Beijing; although most patients are from other provinces all over China, the results may not apply to a broader population. Third, the data available for analysis were those commonly recorded in the medical records. Information on socioeconomic variables and psychosocial characteristics were not available.
On the positive side, the present study examined the association of OPCAB technique with sex disparity in late outcomes. Another major strength of this study is the inclusion of an unselected 7-year consecutive population of patients undergoing isolated CABG.
Conclusions
Compared with men, women were a high-risk group and benefited from off-pump techniques in terms of early mortality after CABG. However, women run a higher risk of late MACCE after OPCAB than after CABG/CPB. A major goal of OPCAB technique is to improve clinical outcomes, but findings in this study suggest fewer benefits for women in the long run and this should be taken into account by cardiac surgeons in choosing surgical revascularization strategy for women.
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Acknowledgments
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The authors thank Wei Li, MD, Sheng-wen Liu, MD, and Jian-feng Hou, MD, for assistance in statistical analysis and thank Xin Pang, MD, and Li He for assistance in data collection. Funding for this study was provided by the Key Project in the National Science & Technology Pillar Program during the Eleventh Five-Year Plan Period (2006BAI01A09) and the Key Project of Beijing Municipal Science & Technology Commission (D0906004040391).
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Footnotes
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* The first two authors contributed equally to this work. 
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W. A. Ahmed, P. J. Tully, J. L. Knight, and R. A. Baker
Female Sex as an Independent Predictor of Morbidity and Survival After Isolated Coronary Artery Bypass Grafting
Ann. Thorac. Surg.,
July 1, 2011;
92(1):
59 - 67.
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[Full Text]
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Abstract
Introduction
