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Ann Thorac Surg 2003;75:1153-1160
© 2003 The Society of Thoracic Surgeons

Original article: cardiovascular

Is the female gender an independent predictor of adverse outcome after off-pump coronary artery bypass grafting?

Thanos Athanasiou, MDa, Sharif Al-Ruzzeh, FRCSa, Rex Del Stanbridge, FRCSa, Roberto P. Casula, FETCSa, Brian E. Glenville, FRCSa, Mohamed Amrani, FRCSa*

a The National Heart and Lung Institute, Imperial College of Science, Technology and Medicine, Harefield Hospital, Middlesex, United Kingdom

Accepted for publication November 6, 2002.

* Address reprint requests to Dr Amrani, Department of Cardiac Surgery, Harefield Hospital, Middlesex UB9 6JH, UK
e-mail: mr.amrani{at}rbh.nthames.nhs.uk


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: The female gender is an independent predictor of adverse outcome after conventional coronary artery bypass grafting using cardiopulmonary bypass. The aim of this study is to assess the effect of the female gender on the outcome after off-pump coronary artery bypass (OPCAB) surgery.

METHODS: This study is a retrospective review of 413 consecutive patients (181 women and 232 men) who underwent OPCAB between January 1999 and May 2001. Adverse outcomes were divided into minor adverse outcomes (MINAO), major adverse outcomes (MAJAO), and prolonged length of stay (PLOS) more than 7 days. MINAO included atrial fibrillation, respiratory complications except adult respiratory distress syndrome, and any wound infection except mediastinitis. MAJAO included stroke, myocardial infarction, renal failure, adult respiratory distress syndrome, mediastinitis, low cardiac output, mechanical ventilation more than 24 hours, intensive therapy unit stay more than 24 hours, gastrointestinal complications, cardiorespiratory arrest, and mortality within 30 days. Preoperative and intraoperative variables were evaluated as predictors of MINAO, MAJAO, and PLOS by univariate and multivariate analyses.

RESULTS: The groups were matched for age and Parsonnet score–predicted mortality. However, the women had a higher incidence of chronic obstructive airway disease (p = 0.04), diabetes (p = 0.01), obesity (p = 0.000), peripheral vascular disease (p = 0.000), hypertension (p = 0.000), unstable angina (p = 0.005), history of previous failed nonsurgical intervention (p = 0.02), and nonelective operation (p = 0.000). There were a fewer number of grafts performed in the female group (2.8 vs 3.4, p = 0.000), with the circumflex territory being revascularised less frequently (p = 0.001). Univariate analysis identified the female gender to be a predictor of only MINAO (p = 0.001) and PLOS (p = 0.000). However, with multivariate analysis, female gender was not found to be an independent predictor of MINAO, MAJAO, or PLOS.

CONCLUSIONS: In OPCAB, the female gender is not an independent predictor of MINAO, MAJAO, or PLOS.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
The female gender has previously been shown to be an independent risk factor for morbidity and mortality after conventional coronary artery bypass grafting (CABG) using cardiopulmonary bypass (CPB) [1–4]. According to the National Adult Cardiac Surgical Database report of the Society of Cardiothoracic Surgeons of Great Britain and Ireland, the mean in-hospital mortality for male patients between 1993 and 1998 was 2.8%, whereas for female patients, it was 4.9% [5]. Possible reasons for this difference in mortality include different anatomical size (women have a smaller surface area than men and a smaller size of coronary arteries), advanced age, higher number of diseased vessels, presence of more severe comorbidity (diabetes, hypertension, peripheral and cerebral vascular disease), and worse functional status at the time of the operation [6–9].

CABG with CPB in female patients is associated with a higher prevalence of recurrent angina, graft occlusion, perioperative myocardial infarction (MI), and incomplete revascularization [10]. Recently, the impact of gender on the long-term results of conventional revascularization has been evaluated. The results from the Bypass Angioplasty Revascularization Investigation (BARI) study showed a higher 5-year survival rate for women compared with men after adjustment of other risk-related variables [11].

Over the last few years, off-pump coronary artery bypass (OPCAB) surgery has been widely used and adopted by many surgical groups due to increased experience of the surgeons and improved surgical techniques and stabilization devices. Therefore, OPCAB proved to be feasible for various groups of patients (elderly, redo-CABG, patients with renal disease, acute MI, low ejection fraction [EF], and diabetic patients with cerebral or peripheral vascular disease) [12–20]. The aim of this study was to assess the impact of the female gender on outcomes after OPCAB surgery.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Clinical data
Between January 1999 and May 2001, 413 patients underwent primary isolated CABG for multivessel disease using the OPCAB technique at The National Heart and Lung Institute. They included 181 women and 232 men. Data on these patients were prospectively entered on the institute database.

Definitions of variables
Obesity was defined as body mass index (BMI) greater than 30. EF was defined as a categorical variable (good EF <= 50, moderate EF = 30 to 49, poor EF < 30). Renal dysfunction included creatinine more than 200 µmol/L on admission or history of renal transplant or dialysis. Perioperative MI was diagnosed by new electrocardiographic changes (loss of R progression, new LBBB, new ST, or T wave changes) associated with a rise in CK-MB levels greater than 50 IU/L. Mediastinitis included deep sternal wound infection requiring further operative intervention. Neurologic complications included cerebrovascular accidents (CVA) and transient ischemic attacks (TIA). Low cardiac output (LCO) was diagnosed if an intraaortic balloon pump (IABP) was inserted or an inotropic support was required for more than 8 hours, or both.

Nonelective operation was defined as the necessity to operate on the patient in the next available operating list within the same week of referral (urgent cases) or the necessity to take the patient to theater out of normal working hours (09:00 AM to 5:00 PM) and before the next morning’s operating list (emergency cases).

Dependent variables were divided into minor adverse outcome (MINAO) and major adverse outcome (MAJAO). MINAO included atrial fibrillation (AF), respiratory complications (pneumothorax, pneumonia, and pleural effusion), and any wound infection (superficial sternal, leg, and arm). MAJAO included TIA/CVA, MI, renal failure, adult respiratory distress syndrome (ARDS), mediastinitis, LCO, ventilation more than 24 hours, intensive therapy unit (ITU) stay more than 24 hours, gastrointestinal complications, postoperative arrest requiring cardiopulmonary resuscitation (CPR), and mortality due to any reason within 30 days. Prolonged length of stay (PLOS) was defined as stay in hospital more than 7 days.

The high-risk group was defined as the combination of the following variables: parsonnet score at least 9%, EuroSCORE at least 4%, and age more than 70 years. Conversion was defined strictly as the use of CPB at any stage during the treatment episode. Patients who, for example, arrested on induction of anesthesia, or who arrested in the ITU and required CPB as part of resuscitative measure, would be classified as conversions, as would patients who were converted at any stage during the course of the operation (including before onset of grafting). Criteria for intraoperative conversion to CPB were persistent hypotension (mean arterial blood pressure < 50 mm Hg) that was not responsive to pharmacological and surgical maneuvers and worsening arrhythmias related to ischemia.

Operative technique
Anaesthesia was induced using propofol 1 to 2 mg/kg, pancuronium 0.1 mg/kg, and fentanyl 8 to 15 µg/kg. For maintenance, propofol 2 to 3 mg/kg/h and ventilation with air and oxygen 45% to 50% were used. Vasoconstrictors or volume were used as required in order to maintain mean arterial pressure of 70 mm Hg. Anticoagulation was achieved using 150 U/kg of heparin given after the completion of harvesting of the tnternal thoracic arteries (ITAs). The activated clotting time (ACT) should be maintained above 250 seconds. Normothermia was maintained by using warm intravenous fluids, a heating mattress, and a humidified airway, in addition to maintaining a warm operating theater. A standby perfusionist with a primed circuit was available for all cases.

Surgical technique
Median sternotomy was used and the heart was stabilized using either Octopus 3 (Medronic Inc, Minneapolis, MN) or the Guidant Vortex Vacuum Assist (Cardio-Thoracic Systems, Cupertino, CA). One deep pericardial retraction suture was placed at the posterior pericardium close and medially to the most proximal part of the inferior vena cava (IVC), acting as a lever that helps the surgeon to rotate the heart to vertical and lateral positions. The right pleura were opened routinely to facilitate the substernal position of the heart during grafting of the circumflex territory. Intraluminal shunts were occasionally used.

The selection of the patients for either surgical technique (whether OPCAB or CPB) was done by the individual surgeons, who practiced both techniques almost equally, and the decision was completely based on their preference at the time of the operation.

Statistical analysis
Continuous variables were compared using the Student’s t test or nonparametric Mann-Whitney test whenever the data did not appear to have normal distributions, and categorical variables were compared using the {chi}2 or Fischer’s exact test. A p value less than 0.05 was considered statistically significant.

Multivariate logistic regression models for risk factors predicting MINAO, MAJAO, and PLOS were constructed and assessed by using the Hosmer-Lemeshow (HL) goodness-of-fit test. Variables were included into the multivariate model if the pvalue was found to be less than or equal to 0.05 in the univariate analysis. For the statistical analysis, the statistical software PEPI-INFO version 0.57 and the statistical package SPSS version 10.0 for windows (SPSS Inc., Chicago, IL) were used.

We performed a multivariate analysis for the calculation of the propensity score including 20 risk factors for adverse outcome (MAJAO = yes, MINAO = yes, or PLOS = yes). The variable (female gender) was excluded from the propensity score analysis. We added the variable (surgeon) as a categorical variable (with the first surgeon as a reference) to the analysis to count for differences in the surgical abilities between the contributing surgeons. After completion of the propensity model, a propensity score was calculated from the logistic equation for each patient. Then, based on this, patients were sorted by propensity and compared within five quintiles [21].

Therefore, the statistical analysis addressed confounding (patient selection) by use of a propensity score and heterogeneity (risk factors) by multivariate risk factor analysis.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Preoperative characteristics
Both groups were matched for age and Parsonnet score; however, the EuroSCORE was significantly different (3 ± 2.5 in the female group vs 2.4 ± 2.4 in the male group, p = 0.01). The preoperative data for the female and male patients are presented in Table 1.


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  		Table 1. Preoperative Variables: Comparison Between Female and Male OPCAB Groups

 
Operative variables
The operative variables are presented in Table 2. The left internal thoracic artery (LITA) was used in the vast majority of cases (92% in the female group vs 93% in the male group). Grafting of the circumflex artery was achieved in the 71% of the female group and in 85% of the male group. This difference was statistically significant (p = 0.001). Use of the right internal thoracic artery (RITA), radial artery (RA), bilateral internal thoracic arteries (BITA), number of arterial conduits, sequential grafts, Y-grafts, and endarterectomy was similar in both groups.


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  		Table 2. Operative Variables: Comparison Between Female and Male OPCAB Groups

 
The mean number of grafts used in the male group was significantly higher (3.4 ± 1.2 vs 2.8 ± 0.9 in the female group, p = 0.000), which matched the extent of coronary disease as determined by preoperative angiography (2.9 ± 1.8 in males vs 2.2 ± 1.3 in females, p < 0.001). In the high-risk group, previously defined by Parsonnet score at least 9%, EuroSCORE at least 4%, and age more than 70 years, the average number of arterial grafts was 1.7 ± 0.7 grafts in the female group versus 1.4 ± 0.5 grafts in the male group (p = 0.01).

Postoperative morbidity and mortality
The postoperative morbidity and mortality are presented in Table 3. The female patients more often developed respiratory complications (18% vs 9%; p = 0.007) and sternal wound infections (7% vs 3%; p = 0.05), and the length of hospital stay was more often longer than 7 days in the female group (41% vs 24% in the male group; p = 0.000). The conversion rate (need for CPB) was 7%, and the associated mortality for this group of patients was 1 of 16 (6.7%).


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  		Table 3. Postoperative Variables: Comparison Between Female and Male OPCAB Groups

 
The overall in-hospital mortality was 4% in the female group and 3% in the male group, but this difference did not reach a level of statistical significance.

Adverse outcomes and length of hospital stay
The risk factor analysis included preoperative, operative, and postoperative variables. By means of univariate analysis and considering as a level of significant association a p less than or equal to 0.05, variables were included in the multivariate model. Univariate analysis identified seven factors as predictors of MINAO, eight factors as predictors of MAJAO and five factors as predictors of PLOS (Table 4). Variables were tested for multicolinearity, and the variable with the strongest relationship with the independent variable was included in the model.


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  		Table 4. Univariate Risk Factor Analysis of Prolonged Hospital Stay > 7 Days, Minor Adverse Outcome, and Major Adverse Outcome

 
Two variables were identified as independent predictors of MINAO, which included conversion to CPB and use of two or more arterial grafts (Table 5). In the univariate analysis, female gender was associated more often in comparison with men with MINAO (63% vs 46%; p = 0.001). In the multivariate model, female gender was not found to be an independent predictor of MINAO (odds ratio, 0.74; 95% confidence interval [CI], 0.43 to 1.27). The HL score was 9.5 (p = 0.3), and degrees of freedom (DF) was 7.


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  		Table 5. Multivariate Analysis: Predictors of Minor Adverse Outcome

 
The only variable that was identified as an independent predictor of MAJAO was conversion to CPB (Table 6). In the univariate analysis, female gender was not associated more often with MAJAO (27% vs 23%; p = 0.3). In the multivariate model, gender was not found to be an independent predictor of MAJAO (odds ratio. 0.98; 95% CI, 0.59 to 1.64). The HL score was 9.4 (p = 0.31), and DF was 8.


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  		Table 6. Multivariate Analysis: Predictors of Major Adverse Outcome

 
Two variables were identified as independent predictors of PLOS, which included age and three or more grafts (Table 7). In the univariate analysis, female gender was associated more often with PLOS (p = 0.000). In the multivariate model, gender was not found to be an independent predictor of PLOS (odds ratio, 0.82; 95% CI, 0.52 to 1.29). The HL score was 4.03 (p = 0.67) and DF was 5.


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  		Table 7. Multivariate Analysis: Predictors of Prolonged Hospital Stay (> 7 Days)

 
The propensity score–adjusted analysis, according to the calculated propensity score, showed similar incidence of adverse outcome in all the five propensity quintiles between the male and female groups, and did not reach statistical significance in any of the quintiles (Tables 8, 9).


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  		Table 8. Logistic Regression Analysis of All Risk Factors With Regard to Adverse Outcome for the Calculation of the Propensity Score

 

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  		Table 9. Propensity Score Analysis for Adverse Outcome

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
This retrospective study shows that in OPCAB, the female gender is not an independent predictor of minor and major adverse outcomes. Female gender was previously shown to be associated with increased operative mortality, morbidity, and delayed recovery after coronary revascularization with CPB [3, 22]. The applicability and safety of beating-heart revascularization in the high-risk group of female patients was initially investigated by Petro and asociates [23]. Furthermore, Capdeville and associates recently evaluated the impact of gender in patients undergoing OPCAB, comparing 61 female with 126 male patients [24]. He demonstrated that female patients undergoing OPCAB surgery should be considered a higher-risk group, compared with men, due to the increased comorbidity and age at the time of the operation; and also, the elimination of CPB did not improve the recovery time, a finding that was identified in male patients.

In our study, we found that female gender is not an independent predictor of major or minor adverse outcomes by comparing retrospectively a sample of patients matched for risk-predicted mortality. Although the female patients had more comorbidity at the time of the operation, with higher incidence of diabetes, obesity, peripheral vascular disease, hypertension, unstable angina, history of previous failed nonsurgical intervention, and urgent surgery, the outcome was similar to the male patients, showing that OPCAB was applicable and safe for complete revascularization in women with multivessel disease.

In agreement with previous reports, the mean number of grafts and the incidence of revascularization of the circumflex territory in the male group were significantly higher than in the female group [23]. This finding can be explained by the smaller size and body surface area of women, and consequently, smaller vessels and smaller number of vessels suitable for grafting [25]. Loop and associates reported that the poorer outcome in female patients was related to the smaller size, and that the operative mortality increased as the coronary diameter became smaller. Nishida and associates showed that the extensive use of arterial grafts in patients with smaller-size vessels was associated with excellent early and long-term patency rates [26]. The use of more arterial grafts in our institution was not only because of the surgeons’ preference to achieve complete revascularization, but also because of the higher incidence of poor quality of vein conduits and peripheral venous disease in women. In our OPCAB group, it is obvious that the extensive use of arterial grafts in female patients was not associated with significant increase in operative mortality and morbidity. The high-risk subgroup analysis showed that female high-risk patients received significantly more arterial conduits than male high-risk patients, and this could have an impact on the adverse outcomes in this study. It would have been ideal if the two subgroups had similar types of conduits, and therefore, this represents a limitation of the study.

Complete revascularization using OPCAB is feasible [27], and although there has been some concern regarding the risk of compromising the quality of coronary anastomosis, especially to the circumflex territory, several reports showed patency greater than 90% [28, 29], with reduced use of blood products and cost [30], especially in units that use the OPCAB technique and routinely use revascularization (high-volume vs low-volume OPCAB revascularization programs) [31].

The association of female gender with age and age-related comorbidity has been shown in large series with the use of CPB. In these studies, age more than 70 years and female gender were identified as independent predictors of early mortality and morbidity, with similar odds ratios below 2 [2]. We have recently reported our preliminary experience in the elderly, and we found that the avoidance of CPB can be beneficial in the elderly in terms of mortality, complications, and ITU stay [32].

Capdeville and associates [24] reported that in OPCAB surgery, gender was associated with increased intubation time, ITU stay, and length of hospital stay. In our study, a trend of longer intubation time and length of hospital stay in the female group was present in the univariate analysis but not in the multivariate analysis, and was possibly related to the greater comorbidity of the female patients in comparison with men. In the multivariate model, the only predictors of length of stay were age and number of grafts.

Conversion was found to be the strongest predictor of minor and major adverse outcomes, with a relatively lower incidence (7% vs 13% in previous reports) [33]. This finding may be related to many factors: the size of the heart, recent MI, preoperative hemodynamic instability (irritable heart with minimum manipulation), and the order of revascularization (coronary arteries that supply a larger area of viable myocardium in relation to the degree of stenosis of the coronary vessel). Our study confirms the previous findings [33] that conversion is associated with significant morbidity and mortality and that the most common reasons for conversion are hemodynamic instability or arrythmia. The risk of conversion is not gender related, and strategies of prevention should be individualized for every patient.

The risk of sternal-related complications was higher in women than in men, and the coincidence of sternal fractures was significant in obese patients (5/38 [13%]) (requiring Robicsek technique for reduction of sternal fracture) during the attempt to facilitate the exposure of the distal circumflex. Prevention and cautious intraoperative and postoperative management of sternal instability can reduce the risk of infection, length of stay, and readmission rate in this group of patients. Obesity was not identified as an independent predictor of minor or major adverse outcomes, in agreement with previous reports [34].

The higher incidence of postoperative pulmonary complications in the female patients in our series was determined by the higher incidence of preoperative pulmonary morbidity in comparison with men (p = 0.04), and also by the fact that women were more obese and more often in-hospital before the operation.

Other OPCAB series identified the increased number of grafts as a predictor of adverse postoperative outcome [35]. It is not yet certain whether high-risk groups of patients, such as elderly or female patients, would benefit more from a maximum multivessel revascularization rather than a target-vessel strategy [36] . The balance between the risk of serious postoperative morbidity due to under-grafting or over-grafting and achievement of target vessel complete revascularization in OPCAB surgery can further reduce the impact of gender on adverse outcomes after CABG.

Women with coronary disease present later than men, and if we consider the fact that angioplasty does not provide better long-term results in comparison with CABG [37], we conclude that a more aggressive cardiological management can be responsible for a bias in the gender-related outcome differences. Earlier and more selective intervention would be beneficial for female patients requiring surgical revascularization.

The study is limited by its nature being nonrandomized and retrospective, and the fact that operations were performed by different surgeons with different strategies for revascularization. Although the number of patients analyzed in this study is of moderate size, the results could have been more conclusive if a larger sample was analyzed.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

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