Early Atrial Tachyarrhythmia Recurrence Predicts Late Atrial Tachyarrhythmia Recurrence After the Cryo-Maze Procedure　― An Observational Study ―

Abstract

Background: It is unknown whether early atrial tachyarrhythmia (ATA) recurrence occurring within 3 months after the Maze procedure predicts late ATA recurrence.

Methods and Results: This study involved 610 patients who underwent the modified Cryo-Maze procedure in conjunction with other cardiac surgery. The primary outcomes were late ATA recurrence, defined as occurring ≥3 months after surgery. The effects of early ATA recurrence on late ATA recurrence were analyzed using a Cox proportional hazards model. The following 11 covariates were considered explanatory variables: early ATA recurrence, age, sex, body surface area, preoperative duration of atrial fibrillation, preoperative left atrial diameter, and concomitant surgery (mitral valve replacement, mitral valve repair, aortic valve replacement, tricuspid annuloplasty, and left atrial appendage closure). Statistical analyses were performed with a 2-sided 5% significance level. Early ATA recurrence occurred in 174 patients (28.5%). Late ATA recurrence occurred in 167 patients (27.5%), with 595 events identified in these patients. The Cox proportional hazards model showed that early ATA recurrence was an independent predictor of late ATA recurrence (hazard ratio, 4.14; 95% confidence interval, 3.00–5.70; P<0.001)

Conclusions: Early ATA recurrence was an independent predictor of late ATA recurrence among patients undergoing the modified Cryo-Maze procedure. The blanking period might not be applied to patients undergoing the modified Cryo-Maze procedure.

Surgical and catheter ablation are standard interventions for the treatment of atrial fibrillation. The Maze procedure is a promising surgical method for the treatment of atrial fibrillation. Early recurrence of atrial tachyarrhythmias (ATA), which is defined as recurrence within the first 3 months after ablation, has been reported to occur in ≥50% of patients after catheter ablation^1–5 and in up to 59% of patients after the Maze procedure.^6,7 Whether early recurrence predicts late recurrence after catheter ablation is controversial. Three months after catheter ablation is defined as the “blanking period”, which is determined on the basis of the presumed duration required for the healing of intervention-related damaged tissues. Some authors recommend not performing reintervention during this period because early recurrence resolved during long-term follow up in up to half of patients.^8–10 However, other authors showed that early recurrence was an independent predictor of late recurrence after catheter ablation.¹¹ In terms of the surgical ablation method, little is known with regard to whether early recurrence after the Maze procedure predicts late recurrence. Therefore, we hypothesized that early ATA recurrence after the Cryo-Maze procedure predicts late recurrence. To test this hypothesis, we conducted this observational study.

Methods

Study Registration and Ethical Considerations

This study was performed in compliance with the Declaration of Helsinki, and the study was approved by the National Cerebral and Cardiovascular Center Ethics Committee (registration number, M30-099). The need to obtain written consent from the study participants was waived because no clinical interventions were performed, and all protected health data were deleted after data extraction. Opportunities for potential participants to express their unwillingness to participate in the study were given on an opt-out basis.

Outcomes of Interest

The main outcome of interest was the late recurrence of ATA, namely atrial fibrillation, atrial flutter, or atrial tachyarrhythmia, in accordance with the definition from the HRS/EHRA/ECAS/APHRS/SOLAECE expert statement.¹² Patients were followed for 3 months after surgery to evaluate early ATA recurrence. A diagnosis of early ATA recurrence was confirmed if arrhythmias were captured with continuous electrocardiographic monitoring during the postoperative intensive care unit stay, daily electrocardiographic monitoring during the ward stay, or electrocardiographic monitoring during post-discharge clinic visits. In addition, late ATA recurrence, defined as recurrence ≥3 months after surgery, was investigated. A diagnosis of late ATA recurrence was confirmed if arrhythmias were captured with electrocardiographic monitoring performed during post-discharge clinic visits, continuous electrocardiographic monitoring in case of emergency department visits, or daily electrocardiographic monitoring in case of re-hospitalization. Post-discharge clinic visits were scheduled 3, 6, and 12 months postoperatively, and every 12 months thereafter in National Cerebral and Cardiovascular Center Hospital.

Study Population

In this retrospective, observational, single-center cohort study, 779 consecutive patients who underwent the modified Cryo-Maze procedure in conjunction with other cardiac surgery between January 2007 and May 2019 at the National Cerebral and Cardiovascular Center Hospital were included. Medical records, operative reports, and referral letters were reviewed for data extraction. The exclusion criteria for this study were: (1) patients with no known early ATA recurrence; and (2) patients who had early ATA recurrence without a return to sinus rhythm by 3 months postoperatively.

Surgical Indications

Surgical indications were discussed by the institutional heart team, in accordance with published guidelines.^13,14 The indications for the modified Cryo-Maze procedure were determined on the basis of our previously published data.^15,16 The exclusion criteria for the modified Cryo-Maze procedure comprised: (1) left atrial diameter >70 mm; (2) history of long-standing, persistent atrial fibrillation for ≥10 years; and (3) F-wave voltage in lead V1 of <0.1 mV. Paroxysmal atrial fibrillation was defined as recurrent atrial fibrillation episodes that terminated spontaneously within 7 days. Non-paroxysmal atrial fibrillation was defined as recurrent atrial fibrillation persisting for ≥7 days.^13,14 Patients underwent 12-lead electrocardiography and transthoracic echocardiography at our institution within 2 weeks before surgery. The amplitude of the F wave on lead V1 was measured with a preoperative 12-lead electrocardiogram in patients with non-paroxysmal atrial fibrillation. Left ventricular ejection fraction, left ventricular diastolic dimension, and left atrial volume index were reported in all patients as part of routine practice for echocardiography, according to the corresponding guideline.¹⁷

Surgical Technique for the Modified Cryo-Maze Procedure

The features of our modified Cryo-Maze procedure are: (1) a modification of the Cox–Maze III procedure using a cryo-thermal energy source; and (2) longitudinal incision of the right atrium from the inferior vena cava to the right atrial appendage and elimination of the ablation line to the superior vena cava to avoid the risk of sinus node injury. Most patients underwent the modified Cryo-Maze procedure with the median full sternotomy approach. Complete lesion sets were obtained in all patients with our institutional method for the modified Cryo-Maze procedure, as previously reported.^18,19 Briefly, the right side of the left atrium was surgically incised as for standard mitral valve exposure. Box lines encircling bilateral pulmonary veins, the left atrial appendage, and the mitral annulus were cryo-ablated to connect the incision lines. The right atrial appendage was longitudinally incised. The fossa ovalis, tricuspid annulus, and orifice of the inferior vena cava were then cryo-ablated to connect the incision lines. Exclusion of the left atrial appendage was performed by oversewing the orifice from the endocardial side or by clipping from the outside using an AtriClipVR (AtriCure Inc., Cincinnati, OH, USA). The modified Cryo-Maze procedure was completed before the main procedure. Two types of cryo-probes (linear and T-shaped) equipped with a nitrous oxide system (target temperature, −80℃ for 2 min; CCS-200; CooperSurgical Inc., Trumbull, CT, USA) were used up to December 2016. Subsequently, we used the cryoICEVR probe and nitrous oxide system (target temperature, −60℃ to −70℃ for 2 min; AtriCure Inc.).

Postoperative Management and Antiarrhythmic Treatment

Warfarin was administered to all patients for at least 3 months postoperatively, regardless of the type of valve surgery or postoperative rhythm. A β-blocker was given unless the patient presented with bradycardia or hypotension. Both early and late ATA recurrence were treated with a class Ia, Ic, or III antiarrhythmic drug. If these drugs were ineffective, direct-current cardioversion was performed. Anticoagulant medication was terminated 3–6 months after surgery if sinus rhythm was confirmed by multiple electrocardiographic examinations and no symptoms of paroxysmal atrial fibrillation were observed.

Statistical Analysis

Continuous variables were summarized as medians and interquartile ranges. Categorical and ordinal variables were summarized as numbers and percentages (%). The primary outcome of this study was the time to the first recurrence of the late ATA within 10 years. To estimate the cumulative survival probability at each follow-up time, we used the Kaplan-Meier method. Furthermore, we assessed the impact of the early ATA recurrence following the modified Cryo-Maze procedure on the late ATA recurrence using a multivariable Cox proportional hazards regression model with adjustment for the following 11 baseline covariates: age, sex, body surface area, preoperative duration of atrial fibrillation, preoperative left atrial diameter, and concomitant surgery (mitral valve replacement, mitral valve repair, aortic valve replacement, tricuspid annuloplasty, and left atrial appendage closure). These variables, which are possibly associated with the recurrence of ATA, were selected on the basis of previous studies and the availability of related data in our institutional clinical records.^{15,16,20–22} Age, body surface area, preoperative duration of atrial fibrillation, and left atrial diameter were taken into account for non-linearity using restricted-cubic-spline functions with 3 knots located at the 10^th, 50^th, and 90^th percentiles. In this model, missing data were imputed with the multiple imputation method. Missing data for all independent variables used in this statistical model were imputed 5 times. Proportional hazards were tested for using the chi-squared test for Schoenfeld residuals. In the above regression model, the time to censoring was determined as the minimum of time to the end of follow up or drop-out, including all-cause mortality.

In the primary regression model detected above, the occurrence of mortality was treated as the censoring, which probably overestimated the risk of late ATA recurrence. Therefore, we performed Fine and Gray proportional hazards regression model analysis to treat the occurrence of mortality as the competing risk event of the late ATA recurrence. The adjustments of the covariates were conducted similarly to the primary analysis using the multiple Cox proportional hazards regression model. The missing values were imputed via the single imputation method, using the MICE package in R.

All statistical hypothesis tests were performed with a 2-sided 5% significance level using R 4.1.0. The corresponding author had full access to all the data in the study and took responsibility for its integrity and the data analysis. The data of this study and the methods used in the analysis can be made available from the corresponding author upon reasonable request.

Results

Study Subjects and Outcome of Interest

A total of 779 patients were identified as potential study subjects during the study period. Among them, 31 patients whose early recurrence time point and/or duration were unknown and 138 patients whose early recurrence persisted for >3 months postoperatively were excluded. As a result, 610 patients were included in the analysis (Figure 1). The study subjects’ baseline characteristics are shown in Table. Early ATA recurrence occurred in 174 patients (28.5%), specifically in 167, 7, and 0 cases 1, 2, and 3 months postoperatively, respectively. Because all patients who relapsed in the third month progressed to late recurrence without returning to sinus rhythm, these patients were excluded from the analysis. Late ATA recurrence occurred in 167 patients (27.4%): 90 patients with early ATA recurrence and 77 patients without early ATA recurrence. In the 167 patients with late ATA recurrence, 595 late ATA recurrence events were identified. Sixteen patients died: 1 patient with early ATA recurrence and 15 patients without early ATA recurrence. The Kaplan-Meier curve for late ATA recurrence is shown in Figure 2. Regarding postoperative use of antiarrhythmic drugs, data were missing for 312 of 610 patients. For the remaining 298 patients, 62, 187, 7, and 26 were using Vaughan Williams classification group I, II, III, and IV drugs postoperatively, respectively.

Figure 1.

Flowchart of the study participants. ATA, atrial tachyarrhythmia.

Table. Baseline Patients’ Clinical and Demographic Characteristics

	Early ATA recurrence			SMD	Overall	Missing (%)
	No	Yes	P value
Number	436	174			610
Age (years) (median [IQR])	67 [60, 73]	69.50 [62, 76]	0.004	0.24	68 [60, 74]	0
Sex, Female/Male, % (freq)	45.9/54.1 (200/236)	49.4/50.6 (86/88)	0.427	0.071	46.9/53.1 (286/324)	0
Body surface area (m2) (median [IQR])	1.57 [1.43, 1.70]	1.52 [1.43, 1.73]	0.37	0.059	1.56 [1.43, 1.70]	0
Preoperative duration of AF (years) (median [IQR])	1 [0, 2]	1 [0, 2]	0.144	0.193	1 [0, 2]	13.6
Left atrial diameter (mm) (median [IQR])	51 [46, 56]	50 [46, 56]	0.564	0.043	50 [46, 56]	13.9
Paroxysmal AF, % (freq)	33.6 (125)	25.8 (40)	0.079	0.171	31.3 (165)	13.6
F wave grade, % (freq)			0.021	0.219		13.6
>0.1 mV	33.9 (126)	44.5 (69)			37.0 (195)
≤0.1 mV	66.1 (246)	55.5 (86)			63.0 (332)
CHADS2 score (median [IQR])	1 [1, 2]	2 [1, 3]	0.001	0.267	1 [1, 3]	11.1
Hypertension, No/Yes, % (freq)	47.0/53.0 (150/169)	39.1/60.9 (54/84)	0.119	0.16	44.6/55.4 (204/253)	25.1
Hyperlipidemia, No/Yes, % (freq)	66.1/33.9 (211/108)	68.8/31.2 (95/43)	0.574	0.058	67.0/33.0 (306/151)	25.1
Diabetes, No/Yes, % (freq)	86.2/13.8 (275/44)	83.3/16.7 (115/23)	0.425	0.08	85.3/14.7 (390/67)	25.1
COPD, No/Yes, % (freq)	92.8/7.2 (296/23)	89.1/10.9 (123/15)	0.193	0.128	91.7/8.3 (419/38)	25.1
Serum creatinine (μmol/L) (median [IQR])	75.2 [61.9, 89.3]	77.8 [61.9, 93.7]	0.396	0.119	76.0 [61.9, 89.3]	31.1
Mitral valve replacement, No/Yes, % (freq)	63.5/36.5 (245/141)	67.9/32.1 (106/50)	0.323	0.094	64.8/35.2 (351/191)	11.1
Mitral valve repair, No/Yes, % (freq)	56.7/43.3 (219/167)	55.1/44.9 (86/70)	0.733	0.032	56.3/43.7 (305/237)	11.1
Aortic valve replacement, No/Yes, % (freq)	72.8/27.2 (281/105)	71.8/28.2 (112/44)	0.813	0.022	72.5/27.5 (393/149)	11.1
Tricuspid annuloplasty, No/Yes, % (freq)	63.2/36.8 (244/142)	48.7/51.3 (76/80)	0.002	0.295	59.0/41.0 (320/222)	11.1
Left atrial appendage closure, No/Yes, % (freq)	44.0/56.0 (170/216)	24.5/75.5 (38/117)	<0.001	0.42	38.4/61.6 (208/333)	11.3
Coronary artery bypass grafting, No/Yes, % (freq)	88.9/11.1 (343/43)	87.2/12.8 (136/20)	0.58	0.052	88.4/11.6 (479/63)	11.1

AF, atrial fibrillation; ATA, atrial tachyarrhythmia; CHADS₂, congestive heart failure, hypertension, age >75 years, diabetes mellitus, and prior stroke or transient ischemic attack; COPD, chronic obstructive pulmonary disease; freq, frequency; IQR, interquartile range; SMD, standardized mean difference.

Figure 2.

The Kaplan-Meier curve for late atrial tachyarrhythmia recurrence.

Effect of Early ATA Recurrence on Late ATA Recurrence

The Cox proportional hazards regression model showed that early ATA recurrence was an independent predictor of late ATA recurrence (hazard ratio, 4.14; 95% confidence interval, 3.00–5.70; P<0.001) (Figure 3). The P value of the chi-squared test for Schoenfeld residuals was 1.00.

Figure 3.

The Kaplan-Meier curve for late atrial tachyarrhythmia recurrence stratified by early atrial tachyarrhythmia recurrence.

Sensitivity Analysis

The Fine and Gray proportional hazards regression model showed that early ATA recurrence was an independent predictor of late ATA recurrence (hazard ratio, 4.30; 95% confidence interval, 3.14–5.90; P<0.001) (Figure 4).

Figure 4.

Cumulative incidence of late atrial tachyarrhythmia recurrence and mortality stratified by early tachyarrhythmia recurrence.

Discussion

We investigated the modified Cryo-Maze procedure in conjunction with other cardiac surgery among 610 patients and demonstrated that postoperative early ATA recurrence was an independent predictor of late ATA recurrence. Our results showed that recurrence occurring during the 3-month postoperative blanking period was a risk factor for long-term ATA recurrence among patients undergoing the modified Cryo-Maze procedure. Because a blanking period was a concept created from studies of patients undergoing catheter ablation,^9,23 whether this concept could be applied to patients undergoing surgical ablation is not well understood. Our results suggested that a 3-month blanking period should not be applied to patients undergoing surgical ablation.

Postoperative autonomic nervous system activation and an associated inflammatory response is also a risk factor for postoperative ATA recurrence.^21,22 This postoperative situation has been considered transient and reversible, which provided the rationale for observing a blanking period among patients who underwent catheter ablation.^1,8 As for atrial fibrillation after cardiac surgery, there had been reports that atrial fibrillation did not recur once the transient postoperative inflammatory response ameliorated.^24,25 However, the results of the present study indicated that early ATA recurrence was not transient but persistent after surgical ablation. One explanation why early recurrence after surgical ablation was a risk factor for long-term recurrence was differences in study participants’ backgrounds; 73% of the patients had persistent atrial fibrillation in the present study, whereas two-thirds of the participants had paroxysmal atrial fibrillation in studies involving a blanking period.^8–10 In addition, previous reports investigating postoperative atrial fibrillation have often excluded patients with persistent atrial fibrillation from their studies.^24,25 The degree of atrial structural and electrical remodeling was considered more advanced in the present study’s patients than in patients in other studies who received catheter ablation or cardiac surgery other than the Maze procedure. This is supported by the present study’s results showing that patients with early ATA recurrence had advanced age and lower voltage in lead V1 on electrocardiography, which is correlated with advanced atrial remodeling.^15,16 Elevated atrial pressure owing to atrial remodeling alters the atrial refractory period, making atrial fibrillation more likely.^26,27 Patients with early ATA recurrence in this study had these structural and electrophysiological remodeling characteristics, which would have made the patients more prone to late ATA recurrence. For these patients, the postoperative inflammatory response would act as a stress test, revealing patients who were prone to long-term recurrence. Furthermore, the main cause of postoperative ATA recurrence following the Maze procedure is reentrant circuit remodeling, and the efficacy and safety of early re-ablation for this condition have been reported.^28,29 Thus, aggressive interventions, such as early endocardial electrophysiological studies and early re-ablation, may improve postoperative outcomes for high-risk patients, rather than observing a blanking period.

To the best of our knowledge, only a few studies have investigated the relationship between early and late ATA recurrence after surgical ablation. Choi et al reported that early ATA recurrence was an independent predictor of late ATA recurrence within 12 months postoperatively.³⁰ The authors reported that the effect of early ATA recurrence within the first month postoperatively on late ATA recurrence was small, whereas early ATA recurrence after postoperative day 58 was associated with a greater risk of late ATA recurrence. In the present study, although most of the early recurrences occurred within 1 month postoperatively, early ATA recurrence was an independent predictor of late ATA recurrence. The reason for the difference between the results of Choi et al and our results may be the difference in patient background; compared to those reported by Choi et al, the patients in our study appeared to be older and to had undergone more complex cardiac surgery. Age and structural heart disease had been reported as risk factors for ATA recurrence,^6,7,31,32 and it was possible that differences in patient background might have led to the finding that early ATA recurrence within 1 month postoperatively also contributed to late ATA recurrence.

Failure of cryo-ablation may cause ATA recurrence after surgery because it is challenging to confirm conduction block during surgery. The quality of the surgical technique was also thought to have a significant impact on postoperative ATA recurrence. The previous reports showed the sinus rhythm restoration rate was 73–83% at 4–5 years postoperatively after the Maze procedure.^33–35 In our institution, late ATA recurrence occurred in 167 patients (27.4%) during 10 years of follow up. Our results compared favorably with previous reports, and it would be unlikely that recurrence was occurring due to procedural failure. Various mechanisms of ATA recurrence after the Maze surgery have been reported. Suzuki et al reported the electrophysiological findings in 37 patients with ATA recurrence after the Maze procedure, including patients at our institution.²⁹ They found that the atrium after the Maze procedure had many electrical gaps, and most of the ATAs mechanisms were macro-reentry. Although the Maze surgery with the cut-and-sew method had been considered to cause a low ATA recurrence rate because it could create a transmural electrical gap with a high probability,³⁶ gap-related recurrences could occur in patients after cut-and-sew Maze surgery, as well as after the Maze procedure with cryo or radiofrequency energy. As recurrence due to macro-reentry was highly treatable by catheter ablation, aggressive early intervention for such patients would likely improve their mortality and morbidity.

Study Limitations

This study had several limitations. First, the ATA recurrence rate after the Cryo-Maze procedure might have been underestimated because limited post-discharge electrocardiographic monitoring might not have captured some recurrent ATAs. If cases of early ATA recurrence were not detected, the estimated effect of early ATA recurrence on late ATA recurrence might have been less that the actual effect. However, if so, this was unlikely to affect the results because the effect would be towards a conservative analysis result. Second, because patients with early ATA recurrence that persisted until 3 months postoperatively were excluded from the analysis, the effect of early ATA recurrence on late recurrence was underestimated. Third, we could not collect some data that could have potentially affected postoperative outcomes (e.g., postoperative catecholamine use, postoperative atrial pacing, and postoperative use and dose of antiarrhythmic drugs). Among these data, treatment for postoperative ATAs was considered particularly important. However, postoperative treatment of ATAs was protocolized and was expected to have little impact on outcomes. Moreover, patients with early ATA recurrence would be more likely to have received more intensive treatment, which may have had an impact on underestimating the effects of early ATA recurrence on late ATA recurrence. Finally, the present study was an analysis of data from a single institution; therefore, caution should be used when interpreting the results.

Conclusions

Early ATA recurrence after the modified Cryo-Maze procedure was an independent predictor of late ATA recurrence. Among patients with postoperative early ATA recurrence, early re-intervention might have a benefit in preventing late ATA recurrence, rather than observing a 3-month blanking period.

Acknowledgment

We thank Jane Charbonneau, DVM, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.

Sources of Funding

This work was supported by grants from the Ministry of Health, Labour and Welfare, Japan (Grant No. 21H03017).

Disclosures

All authors declare that they have no conflicts of interest.

IRB Information

This study was approved by the National Cerebral and Cardiovascular Center Ethics Committee (registration number, M30-099).

Data Availability

Data cannot be shared because permission has not been obtained from the National Cerebral and Cardiovascular Center Ethics Committee.

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