Multivariate analyses comparing the women and the men on all perioperative and postoperative clinical outcomes also found no significant effect of sex after adjustment for the clinical covariates, as described in the statistical methods. Furthermore, there was no significant difference between the women and the men for 2-year cumulative survival after adjustment for clinical covariates (hazard ratio, 1.47; confidence interval, 0.68–3.21; P = 0.33; Fig. 1). The total number of deaths at any time during the study (before and after discharge) was n = 55 and not different between the sexes (P = 0.17). For the patients with a known cause of death identified through the National Death Index (International Statistical Classification of Diseases, 10th Revision, codes were used for cause of death), there was also no significant difference in the number of women and men who died as a result of cardiovascular disease [women: 10/14 (71%) vs men 7/11 (64%), P = 1.00].
The return to sinus rhythm at 6 months and 12 months for the women was 93% and 94%, which was not significantly different than the men’s rate of return to sinus rhythm of 91% and 92%, respectively. The return to sinus rhythm was also similar for both women and men off antiarrhythmic medications at 6 months (75% vs 78%, P = 0.53). This relationship held steady at 12 months, when similar results were found (81% vs 80%, P = 1.00; Table 3). In the subset of patients who agreed and underwent 1-week monitoring at 6 months off antiarrhythmic medications (n = 169; 33% were women), we found the same trend for return to sinus rhythm for both groups (89% vs 93%, P = 0.55; Table 3). For the patients with pacemaker interrogation reports at 6 months (n = 27), return to sinus rhythm was also not different between the women and the men (92% vs 86%, P = 1.00).
Less than 20% of the patients in each group required electrical cardioversion at any time point during follow-up for return to sinus rhythm after the Cox-Maze III/IV procedure (χ2 = 0.01, P = 0.91). Less than 6% of the patients in each sex (P = 0.84) required a follow-up catheter ablation to restore sinus rhythm, with the most common reason being for atrial flutter (n = 21) in both groups [women: n = 7 (4 for atypical flutter, 2 for typical flutter, 1 unknown); men: n = 14 (5 for atypical flutter, 8 for typical flutter, and 1 unknown); Table 4]. Most patients in both sexes maintained their sinus rhythm after catheter ablation at their last known follow-up (women: 75% and men: 79%). Pacemakers were required after the Cox-Maze III/IV procedure in 3% of the women and 5% of the men (P = 0.39), with the most common reasons being for sick sinus syndrome and sinus node dysfunction.
In a mean ± SD follow-up period of 40.3 ± 24.4 months and 40.4 ± 24.6 months for the women and the men, respectively (t = 0.04, P = 0.97), we found no significant differences in postdischarge stroke/transient ischemic attack morbidity or the need for follow-up interventions to restore sinus rhythm (Table 4). In the female group, there was one patient who had an embolic stroke after discharge versus three patients in the male group (P = 1.00), which translates to a very low rate of 16.5 strokes per 10,000 person-years in women and 24.8 strokes per 10,000 person-years in men. Major bleeding events (defined as a bleed that required blood transfusion, hospitalization, or surgical intervention to control bleeding or intracranial hemorrhage after the 3-month blanking period) occurred in 3.3% of the women (9 total events) and 3.6% of the men (21 total events) during the follow-up period (P = 1.00). For the patients with at least one major bleeding event, the mean preoperative CHADS2 score did not differ between the women and the men (2.0 ± 0.9 vs 2.1 ± 1.0, P = 0.88). At the time of their first major bleeding event, 63% were on warfarin, and of those on warfarin, 50% were taking it for another appropriate clinical indication. Although the sample size is very small, the male patients were more likely to be on warfarin at the time of their first major bleeding event than were the women (85% vs 17%, P = 0.01).
Health-Related Quality of Life and AF Burden
In Figure 2, a comparison of the men and the women on all domains of the SF-12 at baseline and 6 months after surgery can be found. It is clear that the scores reported by the female patients were lower at all time points. The female patients scored significantly lower on baseline physical composite scores (P = 0.005) and mental composite scores (P = 0.04), physical composite scores at 6 months (P = 0.01), and many other domain scores shown in Table 4 at the baseline and 6-month time points. Although the women consistently reported lower HRQL scores than did their male counterparts, the women did show a significant improvement within their group from baseline to 12 months in physical HRQL (39.2 ± 10.9 to 46.7 ± 9.9, t = 5.3, P < 0.001) and mental HRQL (48.8 ± 12.0 to 52.5 ± 9.4, t = 2.5, P = 0.01).
Physical composite score of HRQL showed a significant effect of time (F = 48.6, P < 0.001) and sex (F = 5.2, P = 0.02). Figure 3 demonstrates the significant quadratic effect of time (F = 20.9, P < 0.001), such that all patients improved significantly between baseline and 6 months, but this improvement leveled out between 6 and 12 months after surgery (women: n = 71, men: n = 148). In addition, the main effect of sex can be seen in Figure 3, with higher physical composite scores in the male patients regardless of time point. However, the improvement trajectories for both sexes did not differ because there was no significant interaction of time and sex on physical composite scores (F = 1.1, P = 0.31). Both groups were lower on preoperative physical composite scores when compared with their age and sex norms (women: 39.2 vs 43.6, t = 3.6, P < 0.001; men: 43.3 vs 47.6, t = 4.2, P < 0.001). By 12 months, the women surpassed their age group and sex norms (47.2 ± 10.0, t = 3.0, P = 0.003) and the men were similar to their age and sex norms (49.2 ± 9.5, t = 1.7, P = 0.09). Also of note, when comparing the physical composite score of the patients who underwent stand-alone Cox-Maze surgery with those who underwent concomitant procedures (regardless of sex), both surgery groups improved similarly from baseline to 12 months after surgery (F = 0.27, P = 0.69), but the stand-alone group had higher physical composite scores regardless of time point (F = 10.8, P = 0.001). Therefore, improvement in HRQL after the Cox-Maze was not solely related to correction of other cardiac disease processes (coronary artery disease and/or valvular disease.
For general health scores of HRQL, there was a significant effect of time (F = 19.3, P < 0.001), but not for sex (F = 3.0, P = 0.08). Overall, general health scores improved from before surgery to 12 months after surgery; however, the significant interaction of time by sex (F = 3.7, P = 0.03) indicated that the improvement trajectories for general health differed by sex (women: n = 75, men: n = 157). As illustrated in Figure 4, the male patients had a linear improvement in general health scores from baseline through 12 months. In contrast, the female patients had a sharper improvement in general health scores from baseline to 6 months but a plateau in scores between 6 and 12 months after surgery. Therefore, the interaction of time by sex was quadratic in nature (F = 5.2, P = 0.02). By 12 months, both female and male patients surpassed their age and sex norms (women: t = 2.4, P = 0.02, and men: t = 2.7, P = 0.008).
Although there was a significant effect of time (F = 11.3, P < 0.001) on mental composite scores of HRQL (women: n = 71, men: n = 148), the women and the men increased similarly (F = 1.2, P = 0.31). At 12 months, the women were similar to their age and sex norms (t = 1.6, P = 0.10) but the male patients had surpassed their age and sex norms (t = 2.9, P = 0.004).
Patient-reported AF symptom frequency showed a significant effect of time (F = 81.3, P < 0.001), such that symptom frequency declined significantly between baseline and 6 months after surgery. There was also a significant main effect of sex, which indicated that the female patients reported greater overall symptom frequency regardless of time point (F = 9.1, P = 0.003). However, the men and the women showed similar improvement in overall AF symptom frequency (F = 0.2, P = 0.62). By 6 months, the women demonstrated a 40% decrease (P < 0.001) in their symptom frequency and a 37% decrease (P < 0.001) in their severity of symptoms, and the men, at 6 months, demonstrated a 54% decrease (P < 0.001) in symptom frequency and a 52% decrease in their reported severity of symptoms (P < 0.001).
Similarly to the AF frequency findings, patient-reported AF symptom severity showed a significant effect of time (F = 66.3, P < 0.001), such that symptom severity also declined significantly between baseline and 6 months after surgery. The main effect of sex was also found for symptom severity, which indicated that the female patients reported greater symptom severity regardless of time point (F = 9.8, P = 0.002). However, again, the men and the women showed similar improvement in AF symptom severity (F = 0.3, P = 0.58). In summary, the female patients did report significantly greater frequency and severity of AF symptoms at baseline (P = 0.048 and P = 0.04) and 6 months (P = 0.003 and P = 0.003), but the level of improvement in these symptoms after surgery was similar to that of the male patients.
Investigation into the more common AF symptoms showed that although the women and the men reported shortness of breath similarly before surgery (81% vs 84%, P = 0.80), by 6 months after surgery, more women were still reporting shortness of breath (64% vs 42%, P = 0.03). The same pattern of result was found for heart fluttering (52% vs 30%, P = 0.02) and heart racing (38% vs 18%, P = 0.02) at 6 months. Although the women had more complaints of shortness of breath, heart fluttering, and heart racing, they demonstrated within their group a significant decrease in their reporting of tiredness (↓36%, P < 0.001), heart fluttering (↓65%; P < 0.001), and heart racing (↓64%, P < 0.001) as well as a significant decrease in the severity of feeling tired (↓28%; P < 0.001) and heart fluttering (↓31%; P < 0.001). The men also showed a significant decrease in the reporting of tiredness (↓40%; P < 0.001), heart fluttering (↓73%; P < 0.001), and heart racing (↓78%, P < 0.001) as well as a significant decrease in the severity of their symptoms of tiredness (↓25%; P < 0.001) and heart fluttering (↓25%; P < 0.001).
When adjustment for AF symptom frequency improvement from baseline to 6 months was included in the model, improvement in physical composite score HRQL during the same time frame became nonsignificant (F = 1.04, P = 0.31), although the significant main effect for sex remained (F = 6.0, P = 0.02). This finding indicates that AF symptom reduction as a result of the Cox-Maze procedure accounts for a large portion of the significant improvement in physical HRQL that was found across both sexes.
This large cohort study assessed the short- and long-term outcomes of the female patients when compared with the male patients after the Cox-Maze procedure for AF. Outcome across sex seems equal both early and late postoperatively. These outcomes held true even when longer term monitoring (monitoring for 7 days and/or pacemaker interrogation) was used to verify their reported rhythm.
The operative risk for the female patients was slightly higher compared with that for the male patients as defined by the EuroSCORE. The female patients were noted to have higher rates of history of congestive heart failure, which is a consistent finding for women and AF.27 In addition, we found that the women needed more valve surgeries but fewer surgeries for coronary artery disease did their male counterparts. The fact that the women present sicker for an intervention is consistent with a study recently completed and published discussing sex bias and cardiovascular disease. Current findings note that the death rate from cardiovascular disease for women has exceeded the rate for men since 1984. Women now account for 52.1% of all cardiovascular-related deaths.28
Current reports also indicate that women with AF are at a higher risk for embolic stroke, are sicker, and are more symptomatic when experiencing AF.29–33 Each year, 55,000 more women than men have a stroke. According to a national report, in 2007, a total of 60.2% of total stroke deaths occurred in women.28 Evidence has also shown that the rate of embolic stroke occurs almost six times as frequently in patients with AF compared with those without AF, and these strokes are found to be more devastating and lethal especially among elderly women.27,32–35 In this current study, only one woman had a late embolic stroke after the Cox-Maze procedure. The stroke occurred at 12 months after surgery while in sinus rhythm, with a CHADS2 of 0. These results were not significantly different from the male group, which is an encouraging result. Despite women being sicker and having a higher risk for complications, the Cox-Maze procedure was found to be equally safe and effective for women and seems to significantly reduce the risk for stroke through the return of sinus rhythm and the disarticulation of the left atrial appendage.36,37
Recent findings for the treatment and outcomes of coronary artery disease have demonstrated that sex bias is present. Women tend to undergo fewer cardiac catheterizations and revascularization procedures than do men and have a higher in-hospital mortality than do men when admitted for acute coronary syndrome.38,39 These findings are also present for women who present to their cardiologist in AF, by whom they are treated less aggressively than their male counterparts are.39–44 Another reason for the delay of treatment may be that women present for nonpharmacological intervention later in their disease course when their presenting symptoms may have been misinterpreted and appropriate treatment is then not undertaken, making them at higher risk with increased rates of heart failure rates.38,45–48 This supposition has also been recently supported in an article published in the Journal of the American Medical Association, in which the authors found that female patients who presented with a non–chest pain myocardial infarction had significantly higher mortality than men did and were not receiving timely pharmacological and nonpharmacological interventions, to include being discharged home from the emergency department without any treatment.49
The predictors for the development of AF differ between men and women, which could also lead to the underdiagnosis of AF in women. Conen and colleagues50,51 found that blood pressure was strongly associated with the incidence of AF, with systolic blood pressure a better predictor than diastolic in women. Biomarkers such as C-reactive protein have also been associated with the development of AF in women without cardiovascular disease. This was a consistent finding in our cohort of female patients as well, in that they had undergone fewer cardioversions and ablations than their male counterparts had.
However, our findings are also similar to recent research results that indicate that sex bias is not evident among women who do receive an intervention for their cardiac disease process. Aguado-Romeo et al52 discerned that sex was not associated with higher in-hospital mortality in patients who undergo some kind of percutaneous cardiovascular procedure for coronary syndrome. However, their results were dependent upon patients being correctly diagnosed and treated; otherwise, mortality was higher in women than in men. Michelena et al10 and Santangeli et al11 found that catheter ablation for AF was successful and beneficial for the correctly selected patients of either sex, although women may encounter more procedural bleeding complications. They also found that women tended to be referred less often and later for catheter ablation than men did. Outcomes reported from the German Ablation Registry found that women experienced the same outcomes as men at 1 year after undergoing left atrial ablation for AF.12
Our results also indicate that women may be referred later in their disease course for treatment of their AF, but once they are sent for further interventional treatment and are operated upon for AF, their outcomes are very good. Women can expect to have the same return to sinus rhythm off antiarrhythmic medications at the respective follow-up time points and to encounter no significant difference in postoperative morbidities than men. Although the women’s follow-up HRQL scores and reporting of and severity of symptoms are significantly different from the men’s scores, the women’s scores within their group improved significantly. By 6 months, the women had a significant increase in the physical composite of their HRQL scores and experienced a significant decrease in their reported AF frequency and severity of their symptoms especially for tiredness and heart fluttering.
Another interesting finding of our study was that there was no statistical difference in cumulative 2-year survival between the women and men. This result is encouraging in that Miyasaka et al53 found that the development of AF conveyed a high risk for new coronary events in women. Therefore, the finding that survival is high in both groups and not significantly different is encouraging for women to seek curative treatment of their AF.
The results demonstrated in this study could be a result of the performance of the full Cox-Maze procedure. Confusion abounds in the literature as to what surgical ablation procedure was actually performed. The use of the biatrial lesion set instead of a procedure limited to the left atrium has been shown to be more successful in maintaining sinus rhythm during the longer term, such as what we found in this study in which both the men and the women had a rate of return to sinus rhythm approaching 90%, with 80% off antiarrhythmic medications at 1 year. Both the men and the women in this study also demonstrated an increase in their general quality of life, in which much of the variance of the increase was noted to be an improvement in their reported AF symptom severity and frequency burden. These findings have also been confirmed in a meta-analysis performed by Barnett and Ad.54 Ad,55 in his commentary titled “How Do We Spell Maze: A Dialogue Concerning Definitions and Goals,” discusses that the use of the terms Cox-Maze or maze should only be used when the procedure that was executed was performed exactly as described by Dr James Cox. He goes on to discuss that the success of the procedure should encompass three components: (a) success in restoring rhythm, (b) decreasing the risk for thromboembolic events, and (c) improving the patients’ quality of life.56 All topics were covered in our study and demonstrated how well the women did after the Cox-Maze procedure.
This is a single-center study with highly experienced surgeons performing the Cox-Maze procedure, so these results may not be generalizable to smaller institutions. In addition, the screening process for patients to be referred for surgery may bias our results because only the sicker women may get referred, whereas the healthier women may elect to undergo other treatment options.
The overall study was powered to detect any sex differences with a small to medium effect size. However, the very low rate of observed events for perioperative outcomes presented a statistical limitation. There is a possibility that with a much larger sample size and greater event rates for these outcomes, sex differences may emerge. However, this report represents one of the largest surgical ablation samples from a single center addressing sex and sex differences. Further, studies examining sex differences in outcomes after surgical ablation are necessary to replicate the findings presented before final rejection of the null hypothesis is accepted.
As we have published previously, we recognize that electrocardiogram and 24-hour holter may not be as robust as longer term monitoring; however, this bias would be the same for both men and women, and the monitoring provided meets the Heart Rhythm Society guidelines.19,23 We will continue to lobby for more intensive and consistent follow-up methods so that results between centers can be compared. However, there are limitations with all modes of cardiac monitoring that still need to be overcome.56
This is one of the first studies completed investigating and comparing the outcomes of female and male patients who undergo the Cox-Maze procedure for AF. Similar to other studies published, our findings suggest that women do present for the Cox-Maze procedure sicker than men. However, once treatment was implemented, both the women and the men achieved acceptable outcomes after their surgical procedure. The women experienced the same return to sinus rhythm off antiarrhythmic medications, an improved quality of life, and a decrease in their reported symptoms directly related to AF as captured using an AF symptom frequency and severity tool. No differences in morbidities or survival when compared with men were found. Women and men can expect to have very good outcomes after surgical ablation, such that the Cox-Maze procedure for AF should be considered a safe, effective, and viable treatment option for women.
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56. Ad N. The challenge of defining procedural endpoints for the surgical treatment of atrial fibrillation. Eur J Cardiothorac Surg. 2012; 41: 119–120.
This retrospective review from Dr Henry and her colleagues at the Inova Heart and Vascular Institute examined 540 patients who underwent a Cox-Maze procedure (CMP) at their institution. They examined outcome differences between men and women. They found that after the CMP, there was no difference in return to sinus rhythm, all-cause mortality, and cardiac-related mortality between sexes. They also found similar relief of symptoms and improvement of quality of life. This study collaborates with previous reports that have shown that gender was not a predictor of late atrial fibrillation recurrence (Prasad SM, Maniar HS, Camillo CJ, et al. The Cox maze III procedure for atrial fibrillation: long-term efficacy in patients undergoing lone versus concomitant procedures. J Thorac Cardiovasc Surg. 2003;126:1822–1828; Damiano RJ Jr, Schwartz FH, Bailey MS, et al. The Cox maze IV procedure: predictors of late recurrence. J Thorac Cardiovasc Surg. 2011;141:113–121). This study further revealed that other clinical outcomes were similar for men and women. This work provides support to the widely held concept that the CMP is equally safe and effective for men and women.
Keywords:©2013 by the International Society for Minimally Invasive Cardiothoracic Surgery
Surgical ablation; Gender; Outcomes; Longitudinal follow-up