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Ann Thorac Surg 2002;74:1517-1525
© 2002 The Society of Thoracic Surgeons
a Miami Heart Research Institute, Mount Sinai Medical Center, Miami Beach, Florida, USA
Accepted for publication April 21, 2002.
* Address reprint requests to Dr Kurlansky, Miami Heart Research Institute, 801 Arthur Godfrey Rd, 5th Floor, Miami Beach, FL 33140, USA
e-mail: doctorwul8{at}aol.com
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Abstract |
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Methods. A retrospective analysis was performed comparing 261 consecutive women patients from a single surgical practice receiving bilateral internal mammary artery (IMA) and supplemental vein grafts between January 1972 and October 1994 with a computer-matched cohort of 261 men undergoing bilateral IMA surgery during the same time period. Univariate analysis confirmed the homogeneity of the two groups based on multiple preoperative variables. The SF-36 QOL assessment tool was completed for all patients at follow-up, which ranged from 1 month to 25 years, with a mean follow-up of 9.1 years for women and 8.6 years for men.
Results. There was no significant difference in operative mortality, nor in the incidence of any of 10 postoperative complications evaluated. The actuarial survival at 15 years was 53.7% ± 4.8% for women and 50.9% ± 5.6% for men (p = 0.218). At follow-up, 97.0% of women and 94.3% of men were free of angina and in Canadian Cardiovascular Society (CCS) class I or II. The need for reoperation (1.8% vs 1.9%) and PTCA (4.8% vs. 3.2%) was comparable in both groups. However, a higher rate of late myocardial infarction was found in women than men (1.8% vs 0.6, p = 0.021). The long-term event-free survival was found to be no different in men than women (p = 0.084). QOL as measured by the SF-36 was compared with the general population corrected for age and gender. Men and women scored as well or better than the general population in a majority of the eight health scales. Moreover, with regard to the health summary scores, men scored significantly higher (p = 0.001) in physical health, whereas women scored significantly higher (p = 0.011) in mental health when compared with age-adjusted norms.
Conclusions. Men and women undergoing coronary revascularization using bilateral internal mammary artery conduits experience comparable outcomes, excellent long-term results, and enjoy a QOL comparable to or better than the general population as measured by the SF-36.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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cause of death in women [1]. Whereas remarkable advances have been achieved in the care of the cardiac surgical patient, coronary bypass surgery in women continues to carry a higher operative mortality rate than in men [2]. This trend has even been documented in off-pump coronary bypass surgery [3]. Women appear to experience decreased late survival and freedom from recurrent symptoms as well as late cardiac events when compared with their male counterparts [4, 5]. These results have been credited to numerous risk factors, including the incidence of diabetes [6, 7], smaller body habitus [8], coronary artery size [9], and functional status [10]. Whereas number of studies have contributed to an understanding of the problem, they have failed to produce a satisfactory therapeutic solution.
The internal mammary artery (IMA) has become the conduit of choice in coronary artery bypass grafting (CABG). The positive influence of the IMA graft on long-term survival and freedom from major adverse cardiovascular events (MACE) has been clearly established [11]. Use of the IMA graft has been reported to reduce perioperative mortality [12], and yield excellent long-term clinical results in women [13]. However, the relative impact of the IMA graft on the diminished perioperative and long-term results of coronary bypass grafting in women compared with men remains currently undefined.
Based on the presumed value of a second IMA, it has been reasoned that patients receiving bilateral IMA grafts would be most likely to demonstrate the benefits of this arterial conduit on short- and long-term surgical outcomes. To discern the efficacy of IMA grafting, a cohort of women receiving bilateral IMA grafting was compared with a matched group of men. Perioperative morbidity and mortality rates, freedom from recurrent angina and MACE, as well as long-term patient survival and quality of life (QOL) were examined.
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Patients and methods |
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Ejection fraction determination from left ventriculography was available in all patients (100.0%) in both groups. In the female group, the ejection fraction was greater than 50% in 203 patients (77.8%), between 30% and 50% in 51 patients (19.5%), and less than 30% in 7 patients (2.7%). In the male group, the ejection fraction was greater than 50% in 160 patients (61.3%), between 30% and 50% in 85 patients (32.6%), and less than 30% in 16 patients (6.1%). A greater proportion of men patients had an ejection fraction of 50% or less (p = 0.001).
Operative technique
Details of the operative technique applied in the current series, including IMA mobilization, orientation, and anastomotic construction in bilateral IMA grafting, have been discussed previously [14]. All operations were performed with the assistance of cardiopulmonary bypass. Since 1989, combined antegrade and retrograde infusion methods of cardioplegia have been implemented to enhance myocardial protection during the operation. The IMA was dissected as an isolated pedicle from the chest wall, free from surrounding muscle and fascia. The vein was initially dissected, but subsequently removed to allow maximal length and versatility. All side branches were carefully cauterized or clipped as necessary.
Operative data
The types of conduit and corresponding recipient arteries by patient group are presented in Table 2.
In the female group, there were 48 sequential IMA grafts. The right IMA was placed through the transverse sinus and grafted to the circumflex or obtuse marginal artery in 119 patients (45.6%); four left IMAs and 17 right IMAs were used as free grafts. An additional 32 sequential vein grafts were used.
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A total of 820 coronary artery grafts were completed in the female group (mean 3.14 per patient, range 2 to 6). In the male group, a total of 900 grafts (mean 3.46 per patient, range, 2 to 6) were performed. Men patients had a significantly higher number of grafts per patient than women (p = 0.001).
The mean cardiopulmonary bypass time for female patients was 108.1 ± 43.5 minutes (range 40 to 351 minutes) and 117.6 ± 44.1 minutes (range 25 to 296) for male patients. The mean duration of aortic cross-clamping for the female group was 66.4 ± 20.6 minutes (range 20 to 200 minutes) and for the male group was 75.7 ± 25.7 minutes (range 12 to 190 minutes). Between-group comparisons of these two variables revealed that male patients experienced an increased duration of perfusion (p = 0.013) and aortic cross-clamping times (p = 0.001).
Operative urgency
The operation was performed in the female group electively in 95 patients (36.4%), urgently in 157 patients (60.2%), and emergently in 9 patients (3.4%). In the male group, the operation was performed electively in 120 patients (46.0%), urgently in 135 patients (51.7%), and emergently in 6 patients (2.3%). A between-group comparison of the surgical urgency revealed that a significantly greater percentage of men were done electively than women (p = 0.033).
An urgent operation was defined as being required within 48 hours in an effort to prevent further clinical deterioration. Emergency operation referred to those instances when a patient had intractable angina that did not respond to aggressive clinical measures or had impending infarction, or when decompensation occurred in the cardiac catheterization laboratory and measures such as defibrillation, extended cardiac massage, balloon counterpulsation, or inotropic support were required. All other patients in the series were considered to have had elective operations.
Data sources
Perioperative data were obtained by retrospective review of the patient’s hospital record, catheterization reports, and cine angiograms. Follow-up information was obtained through comprehensive questionnaires and by telephone interview with surviving patients, family members, or the patient’s personal physician. Follow-up data included activity level, current symptoms, diagnostic tests, occurrence of late cardiac events, and medications being taken. Patients were asked to described their anginal symptoms and were ranked according to the Canadian Cardiovascular Society (CCS) classification system. The National Death Index and the Office of Vital Statistics were contacted when necessary to obtain death certificates and cause of death. Autopsy reports, when available, furnished additional information.
A patient registration form and a patient follow-up form were completed for each participant in the study. These data collection instruments provided standardized reporting of each patient’s clinical status before and after the operation. QOL assessment was conducted with the Short-Form (SF) 36 developed by Ware and Associates [15]. The SF-36 is a standardized instrument comprised of 36 items, which are designed to measure eight dimensions of overall health. These include physical functioning, social functioning, role limitations attributed to emotional problems, mental health, vitality (energy/fatigue), bodily pain, and general health perception. For each dimension, item scores are computed, totaled, and converted into a scale, which ranges from 0 for worst health to 100 representing best health.
Two summary components (a physical and mental health score) are also computed. A high score in the physical health summary component indicates no physical limitations, disabilities, decrements in well-being, and/or high energy levels. A low score indicates substantial limitations in self-care, physical, social, and role activities, severe bodily pain, or persistent tiredness. In the mental health summary component, a high score demonstrates recurring positive affect, absence of psychological distress, and a sense of emotional well-being. A low score is indicative of the presence of psychological disturbance and substantial social and role dysfunction due to emotional instability [16]. The instrument has been used in a number of public health studies. It is generally completed in approximately 10 to 15 minutes and may be administered in person, by telephone, or mail.
A 97.6% follow-up was obtained for women patients and 96.8% for men patients in the present study.
Statistical analysis
Data are presented as frequency distributions and simple percentages. Values of continuous variables are expressed as means ± standard deviation. Univariate analysis of selected preoperative and postoperative discrete variables was accomplished by 
2, the continuity-adjusted 2 analysis, or a two-tailed Fisher’s exact test with the appropriate degrees of freedom to test for the equality of proportions in the case of categorical variables. Comparison of means for continuous variables was conducted by an unpaired Student’s t test.
Patient survival for those discharged from the hospital was expressed by actuarial analysis according to the method of Cutler and Ederer [17] using time zero as the date of operation and late death as the end point (with variability expressed as the standard error of the mean) and by linearized occurrence rates with standard errors. The algorithm of Lee and Desu [18] was used to test the equality of survival distribution for the two patient groups.
Data collected were subjected to both quantitative and qualitative analysis using the Number Cruncher Statistical Systems (NCSS). A significant difference between measurements was defined as p less than or equal to 0.05.
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Results |
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Respiratory insufficiency included patients who required intubation for more than 48 hours or tracheostomy (or both). Cerebrovascular accident referred to a neurological deficit that remained unresolved and presented for more than 24 hours. Myocardial infarction was defined as a new onset of Q waves with or without elevation of myocardial enzymes, or a substantial elevation of myocardial enzymes alone and renal dysfunction included patients with a creatinine level greater than or equal to 2.0 mg/dL.
Low cardiac output referred to clinical evidence of hypotension, oliguria, and peripheral vascular constriction with normal or supranormal left ventricular filling pressure or a measured cardiac index of less than 2 L/min/m2, necessitating the administration of catecholamines or use of the intraaortic balloon pump (IABP), or both. Patients with deep sternal infection included those with instability of the sternum with positive wound cultures necessitating an additional surgical procedure, such as incision and drainage, debridement, or secondary closure.
A between-group comparison of each of the hospital complications reported revealed no significant difference. The hospital complication rates for the two groups are presented in Table 3.
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Hospital mortality rate
Hospital mortality was defined as death occurring during the operation or the hospitalization in which the procedure was performed, or death occurring after discharge from the hospital but within 30 days of the surgical procedure, unless the cause was completely unrelated to the operation. The overall hospital mortality rate for women was 3.4% (9 of 261) and was 3.8% (10 of 261) for men.
The elective mortality rate for women was 2.1% (2 of 95) and was 1.7% (2 of 120) for men; the urgent mortality rate for women was 3.8% (6 of 157) and was 5.3% (7 of 135) for men; and the emergent mortality rate for women was 11.1% (1 of 9) and was 16.7% (1 of 6) for men. A between-group comparison of the mortality rates for various urgency categories did not achieve statistical significance.
The mortality rate for first operation for women was 2.8% (7 of 249) and was 2.9% (7 of 238) for men. The mortality rate for reoperation in women was 16.7% (2 of 12) and in men was 13.0% (3 of 23). A comparison of the influence of surgical history on hospital mortality rates revealed no significant difference between male and female patients.
Univariate analyses were conducted using bivariable contingency tables for 16 potential preoperative risk factors to explore their relation to hospital mortality in each of the two groups. For statistical analysis, patients in CCS classes II and III were combined as one subgroup versus CCS class IV. In the women, CCS class IV (p = 0.027), surgical history of reoperation (p = 0.050), and preoperative insertion of IABP (p = 0.001) were found to be independent predictors of hospital mortality. In men, CCS class IV (p = 0.005) surgical history of reoperation (p = 0.047), and preoperative insertion of the IABP (p < 0.007) were also found to be predictors of hospital mortality.
Long-term follow-up
Follow-up data were collected for 246 female patients (97.6%) and 243 male patients (96.8%) discharged from the hospital. The follow-up for women ranged from 2 months to 25 years (mean 9.1 years) and for men ranged from 2 months to 25 years (mean 8.6 years). The cumulative follow-up for women patients was 2,289.6 patient-years and for men was 2,170.1 patient-years. The linearized late mortality for women was 3.45% ± 1.86% per patient-year (79 events) and was 3.92% ± 1.98% for men (85 events).
At the completion of the follow-up, 167 (66.3%) of the 252 women hospital survivors were alive and 158 (62.9%) of the 251 men hospital survivors were alive. Information concerning the causes of late death for the two groups is presented in Table 4. The actuarial survival data for 252 female patients and 251 male patients discharged from the hospital are shown in Figure 2. At 7 years, survival for female patients (± standard error of the mean) was 84.9% ± 2.3% and was 78.8 ± 2.7% for men. At 15 years, it was 53.7% ± 4.8% for women and 50.9% ± 5.6% for men. The equality of survival distribution for the two groups of patients was tested, and no significant difference was found.
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The freedom from late MACE (nonfatal myocardial infarction, PCI, absence of reoperation-coronary artery bypass grafting) in female and male survivors is shown in Figure 3. The freedom from late MACE for women patients at 15 years was 60.4% ± 6.8% and was 72.7% ± 7.7% for men patients. A comparison of the freedom from late MACE for the two cohorts of patients revealed no significant difference (p = 0.084). However, independently the occurrence of late nonfatal myocardial infarction in women was significantly greater (p = 0.021) than in men.
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Comment |
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Does this infer that the internal mammary graft may overcome the negative impact of female gender on short- and long-term outcomes in coronary bypass surgery? Although the findings here would support such a conclusion, several issues must be addressed. The sample size of this study is relatively small. With 261 patients in each group and only 167 female and 158 male hospital survivors alive at the completion of the follow-up, a statistical power to detect only a moderate difference between groups is present [19]. However, it should be noted that the Cleveland Clinic experience with bilateral IMA patients reports on only 215 female bilateral IMA patients from a total of 2,015 bilateral IMA patients in their database [20]. Moreover, Edwards’ and associates’ report from the Society of Thoracic Surgeons National Database on approximately 350,000 patients does not distinguish between single and bilateral mammary patients, nor does it provide long-term clinical follow-up [2]. Therefore, despite the constraint of sample size, this study is as well equipped as any currently available in the literature to examine the influence of bilateral IMA grafting in women.
Bilateral IMA patients were selected in this study to maximize the influence of IMA grafting. As a result, a smaller number of patients were available to conduct the present study. However, it was felt that the benefit of focusing on patients who were revascularized as completely as possible with IMA grafts compensated for any study limitations that may have occurred as a result of a reduced sample size.
The use of a matched cohort, controlling for demographic and selected clinical variables, was designed to highlight the influence of gender rather than to diminish it. Despite the advantages of matching patient groups, this approach raises an important question regarding the similarity of perioperative results: Is this finding attributable to the use of the IMA graft or merely that patients were so closely matched? Perhaps these two groups of patients would have had similar results even if the IMA had not been used.
Some authors have indicated that a careful analysis of other risk factors eliminates gender as a risk factor in perioperative outcomes [6]. Moreover, Edwards and associates found a significant difference in operative mortality between male and female patients despite the presence of an IMA graft (3.3% in women vs 1.94% in men, p < 0.0001) [2]. However, this analysis did not compare a matched group of patients. When patients were stratified according to their predicted risk, women consistently had a higher operative mortality rate than men, except in the highest risk categories, when other clinical factors may have overshadowed gender as a significant predictor of operative mortality. A limitation of that study occurred when the matched group of patients was not analyzed with respect to IMA usage, nor were the comparisons analyzed according to predicted risk. Further, IMA grafting in that database was significantly less common in women (65.2%) than in men (76.2%, p < 0.0001). As a result, it may be inferred that some if not all of the difference in operative mortality could be attributed to the relative lack of IMA grafting in women.
O’Connor and associates, while controlling for other clinical variables, reported a significant decrease in operative mortality with the use of the IMA graft [12]. Moreover, Loop and associates found, in a matched group of male and female patients in whom the use of the IMA graft was not controlled for, that the operative mortality in women (2.9%) was approximately twice that of the men (1.4%) [21]. When adjustments were made for body surface area, gender lost its value as a predictor of operative mortality. In this study, body surface area was not controlled for; therefore it might be expected to demonstrate a higher operative mortality in women. Because, it did not, it supports the findings of O’Connor and associates that the use of the IMA graft offsets the influence of gender or its comorbidities on operative mortality.
Univariate analysis of preoperative variables in the present study identified CCS class IV, angina, prior CABG, and the preoperative placement of an IABP as significant predictors of operative mortality in both men and women. These findings are consistent with the findings of previous studies [11]. Surprisingly, congestive heart failure, which has frequently been reported to be a significant risk factor for operative mortality [22], was not identified as a predictor of increased operative mortality in the current study. Interestingly, O’Connor and associates [12] found that the use of the IMA was associated with a significant decrease in risk of operative mortality from congestive heart failure. Presumably, some of the patients who died from heart failure may have also suffered from it preoperatively. Therefore, a reduction in the risk of operative mortality from congestive heart failure and from the use of the IMA could decrease its significance as a preoperative predictor variable as well. Furthermore, much of the evidence pointing to congestive heart failure as a predictor of operative mortality comes from early studies. Advances in myocardial preservation, surgical technique, and aggressive medical management, as well as the increased use of the IMA, may well have decreased the deleterious effect of this condition on hospital mortality.
Postoperative hospital morbidity in the present study was low and similar in both groups, with 82.8% (212 of 261) of women and 73.3% (207 of 261) of men experiencing no hospital complication. The low incidence of deep sternal infection, 1.5% (4 of 261) of women and 1.9% (5 of 261) of men, contrasts with reports of an increased rate of sternal infection with the use of both IMAs [23]. This may be due to the surgical technique employed in harvesting the IMA. In the present study, the IMA was harvested as a skeletonized graft rather than as a large pedicle. This approach results in less devascularization of the sternum [24], while increasing graft length and providing for a greater degree of versatility [25].
The long-term actuarial survival of male and female patients was similar in this study. Long-term follow-up of the CASS patients [26] corroborated the findings of other comparable long-term analyses [4] in documenting the reduced freedom from later mortality of hospital survivors in women compared with men. In fact, when compared with the more favorable prognosis for women, matched for age in the general population, the difference between men and women was magnified. The use of the IMA was less prevalent than in more recent studies (only 13% of CASS patients). Interestingly, long-term follow-up of 10,124 patients from the Cleveland Clinic, all of whom received either single- or double-IMA grafts, demonstrates that gender disappears as a risk factor for late mortality [20]. These findings support our contention that the use of the IMA ameliorates the impact of gender on mortality in coronary bypass patients.
Whereas late survival in both genders was comparable, a slightly higher frequency of late nonfatal myocardial infarctions in women (n = 3; 1.8%) was observed in the present study. There was, however, no difference in the low incidence of late PCI and reoperation for coronary artery bypass surgery. These data correlate with the lower number of grafts per patient in women than men (3.14 vs 3.46, p = 0.001) despite the presence of a similar extent of underlying coronary artery disease. This may suggest the occurrence of less complete revascularization in women than men. Despite this occurrence, women actually enjoyed a comparable operative mortality and a greater freedom from late cardiac mortality than men, thereby attesting to the durability and effective protection afforded by a patent IMA graft.
Several investigators have found a significantly higher incidence of late angina in women than men [4, 21, 27]. However, our female bilateral IMA patients enjoyed a similar freedom from symptoms of angina at follow-up, with 97.0% of women compared with 96.2% of men (p = 0.495) in CCS class I. Again, the markedly lower use of IMA grafting in early studies may well have contributed to the difference in outcomes.
Controversy continues to exist concerning the underlying causes for the inferior surgical results, both short and long term, that have been traditionally observed in women. One common opinion implicates the smaller body habitus of women [11, 12]. The CASS data [9] suggest that as patient size decreases, coronary artery size becomes a more significant factor in operative mortality. More recently, O’Connor and associates reported that coronary artery size significantly affected operative mortality independent of body surface area. These investigators concluded that body surface area may be a surrogate for coronary artery diameter and that the higher operative mortality in women resulted from either technical difficulties encountered with the anastomoses or early vein graft closure, which may have resulted from women’s smaller coronary artery size.
The superior patency of the IMA graft is well established [11]. Women have been shown to have a lower vein graft patency but equivalent IMA patency compared with men [21, 27]. Moreover, Suma and associates have shown that patients with smaller body structure receiving IMA grafts enjoy perioperative and midterm results that are comparable to their larger counterparts [28]. These findings strongly support the contention that it is the superior ability of the IMA graft to maintain patency, especially in patients with relatively smaller coronary arteries, that affords women a sufficiently improved perioperative and long-term outcome to overcome previously observed gender differences in coronary surgery results.
Of paramount importance in assessing outcomes in clinical practice is the measurement of patient QOL. The individual’s QOL and health-related sense of well-being provide measures of the patient’s physical, psychological, and social domains. They furnish the clinicians with a useful adjunct to assess clinical status and evaluate the effectiveness of various treatment alternatives.
In the present study, in contrast to similar clinical results, an analysis of late QOL using the SF-36 health survey demonstrates several differences between men and women. Women reported a significantly lower level of physical activity when compared with their age-matched norms, whereas men rated themselves at approximately the normal level for such activity. The differences between the genders in late physical activity and general health after coronary bypass surgery have been reported by Douglas and associates [27] and Carey and associates [5]. However, their findings accompany a concomitant higher incidence of late angina and mortality in women, whereas this cohort of patients had similar levels of these late occurrences in both genders. Furthermore, women rated their freedom from bodily pain as significantly better than age-matched norms, as did men. Thus, the causes for the female patients’ perceptions of decreased physical ability after coronary bypass surgery may not be related to recurrent cardiac symptoms but may be a function of noncardiac-related causes in this relatively elderly cohort of patients. This phenomenon merits further investigation.
Women, on the other hand, appear to score significantly higher than men in their self-assessment of overall mental health. This finding must be interpreted with caution because the SF-36 guidelines suggest that the current study sample size may be insufficient to accurately record differences in the mental health score between the study group and age-matched norms at the measured level [15]. Despite this limitation, the observed trend remains provocative, as women in the general population do not score higher than men in mental health assessment. This finding also warrants further study.
Despite the data documenting the superior graft patency and clinical benefits associated with the IMA graft, there remains a significant reluctance in clinical practice to use this conduit in women. The Society of Thoracic Surgeons National Database reveals that 76% of men and only 65% of women operated on between 1994 and 1996 received IMA grafts. The results generated in the present study demonstrate that women reap perioperative and long-term benefits from bilateral IMA grafting, which are comparable with that achieved in men, without incurring any additional risk. Based on the findings in the present study, it is clear that women should be afforded the opportunity to receive IMA grafts as readily as men. This practice may well correct the clinical differences historically reported between men and women in coronary bypass surgery. Moreover, it will allow them to receive the long-term benefits associated with the conduit of choice in myocardial revascularization.
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