The Effect of the Cryosurgical Cox-Maze Procedure on Pulmonary Veins Diameter and Left Atrial Size: Computed Tomography Angiographic Assessment

Bogot, Naama R. MD*; Elami, Amir MD†; Shaham, Dorith MD*; Berman, Philip M. BA*; Sosna, Jacob MD‡; Ad, Niv MD‡

Innovations: Technology & Techniques in Cardiothoracic & Vascular Surgery: July/August 2009 - Volume 4 - Issue 4 - pp 209-216
doi: 10.1097/IMI.0b013e3181b0aad9
Original Article

Objective: The Cox-Maze procedure using cryoablation results in transmural lesions, which follow the lesion pattern of the cut-and-sew Cox-Maze procedure. The purpose of our study was to evaluate the effect of the Cox-Maze procedure on left atrial and pulmonary vein size using computed tomography angiogram (CTA). An additional aim was to evaluate pulmonary vein anatomic variability.

Methods: Six patients (four women and two men; ages 39–63 years, mean age 54.3) underwent chest CTA 1 day before and 38 to 104 days (mean 62.6 days) after the cryosurgical Cox-Maze procedure. Measurements of pulmonary vein ostia and left atrial cranio-caudal, left-to-right and anterior-posterior diameters were derived by consensus. The change in diameters after therapy was compared using the Wilcoxon nonparametric test for paired measurements. Four patients (1 woman and 3 men; age 57–73 years; mean age 59) were evaluated with postoperative CTA alone 296–530 days (mean 447) after surgery, for the development of postoperative pulmonary vein stenosis. A single patient underwent preoperative CTA, but surgery was not performed. Pulmonary venous anatomy was recorded in all 11 patients.

Results: Sinus rhythm was restored in all operated patients. No focal ostial stenosis of the pulmonary veins was observed. The quantitative assessment in the six patients with preoperative and postoperative studies disclosed only slight changes in pulmonary vein diameter with either reduction or dilatation of no more than 20% from baseline (P > 0.05). There was a consistent trend toward decrease in left atrial dimensions, which did not reach statistical significance. Six patients (55%) had standard pulmonary venous anatomy and five patients (45%) had at least one variation in their pulmonary vein anatomy.

Conclusions: In this study, we found that a very intensive cryoablation protocol around the pulmonary veins did not result in pulmonary vein stenosis. In addition, a relatively high incidence of anatomic variations of the pulmonary veins was documented.

From the *Departments of Radiology and †Cardiothoracic Surgery, Hebrew University-Hadassah School of Medicine, Jerusalem, Israel; and ‡Department of Cardiac Surgery, Inova Heart and Vascular Institute, Falls Church, VA, USA.

Accepted for publication May 15, 2009.

Naama Bogot and Amir Elami contributed equally to this work.

Address correspondence and reprint requests to Niv Ad, MD, Inova Heart and Vascular Institute, 3300 Gallows Road, Falls Church, VA 22402, USA. E-mail:

Article Outline

The Cox-Maze procedure has become the gold standard for the surgical treatment of atrial fibrillation with a long-term success rate in restoring sinus rhythm of more than 90%.1,2 In an effort to maintain the surgical and electrophysiological concepts of the Cox-Maze procedure together with a relatively simple technical procedure, devices that deliver ablative energy to the atrial tissue, such as cryothermal energy, radiofrequency, and microwave, have replaced the classic surgical techniques of cut and sew.3,4

In recent years, there have been reports regarding atrial wall damage and pulmonary vein stenosis, especially when unipolar radiofrequency was used.

Imaging of the pulmonary veins by computed tomography angiogram (CTA) is routinely used in patients undergoing radiofrequency catheter ablation of the pulmonary veins 5,6. Preprocedural evaluations are performed to provide a road map by delineating pulmonary veins morphology, anatomy, and size before pulmonary vein ablation and to obtain a baseline for subsequent evaluations scrutinizing for complications. Postprocedural CTA examinations are routinely used to assess for developments of pulmonary vein stenosis, which may occur as an acute or delayed complication. Initially it was reported in up to 42% of cases after ablation with radiofrequency energy.7 The prevalence of this problem has decreased as a result of modifications in ablation technique and increasing experience and was reported to range from 1% to 20%.8 However, a recent survey reported 0.32% of acute pulmonary vein stenosis and a 1.3% incidence of persistent pulmonary vein stenosis9. Patients may manifest most commonly with symptoms of dyspnea on exertion and pleuritc chest pain and less commonly with hemoptysis. Cryothermal energy is a well-recognized tool for cardiac tissue ablation with a very good safety record.10 The advantages of the use of cryothermal energy are the safety and efficacy in establishing a detectable transmural lesion, which are essential for the success of the Cox-Maze procedure. This study was designed to assess, for the first time, the effect of a very aggressive cryothermal ablation protocol in the left and right atrium on pulmonary vein diameter and on left atrial size. A secondary aim was to learn about the pulmonary vein anatomic variability in our study population.

Back to Top | Article Outline


Institutional review board approval for the study was obtained along with patient informed consent for each participant.

Back to Top | Article Outline

Study Subjects

Eleven subjects with atrial fibrillation were recruited during a period of 8 months (October 2003 to May 2004). Six of them (four women and two men; ages 39–63; mean age 54.3 years) underwent CTA of the left atrium and pulmonary veins before and 38 to 104 days (mean 62.6 days) after the cryosurgical Cox-Maze procedure (group A). To further expand the information regarding the influence of the procedure on the pulmonary veins and left atrium, we recruited additional four patients who have undergone the cryosurgical Cox-Maze procedure, for postoperative CTA evaluation only (group B). This group (1 woman and 3 men; ages 57–73; mean age 59 years) underwent CTA 296 to 530 days (mean 447 days) after the cryosurgical Cox-Maze procedure.

Atrial fibrillation was paroxysmal or persistent in four patients and permanent in six patients, according to new atrial fibrillation classifications.11 Atrial fibrillation had been first diagnosed, on the average, 4.9 years (range, 9 months to 10 years) before the surgical procedure. Structural heart disease was present in nine (90%) of the 10 patients, coronary artery disease in two (20%), and valvular heart disease in eight (80%). In another patient who underwent preprocedural CTA, unexpected surgical findings required extention of the magnitude of the surgical procedure. As a result, the Cox-Maze procedure was not performed to save cardiopulmonary and ischemic time. A total of eleven patients were thus available for analysis of pulmonary veins anatomy.

Back to Top | Article Outline

Cox-Maze Cryosurgical Procedure

In the cryosurgical approach, the atrial incisions of the standard Cox-Maze procedure are replaced by linear cryolesions, resulting in a shorter and technically less demanding procedure. Whether surgical incisions or cryolesions are used to perform the Cox-Maze procedure, it is essential to create transmural atrial lesions to prevent late recurrence of atrial fibrillation.3 Because the cryolesions can actually be watched during surgery as they develop, it is easy to determine when transmural ablation has or has not occurred (Fig. 1). During the study period, this cryosurgical technique, using cryotechnology by Cooper Surgical (Shelton, CT) was our standard procedure for the treatment of medically refractory atrial fibrillation with and without associated acquired or congenital heart diseases. All procedures were performed on bypass, with the cryoprobes applied epicardialy or endocardialy as applicable, for 2 minutes for each lesion at a temperature of −60°C to −80°C.

Back to Top | Article Outline

Computed Tomography

CTA was preformed with four-row multidedector CT scanner (MX 8000, Philips Medical Systems, Cleveland, OH). Nonionic intravenous contrast material (120 mL of Omnipaque 300, Nycomed, Inc., Princeton, NJ) was administered through an antecubital vein with a power injector at the rate of 4 mL/s. By using bolus promethod, scanning initiating time was determined, with the region of interest placed on the left atrium. Collimation of 1.3 mm was used with reconstruction interval of 0.6 mm and 7.5 high-speed pitch mode. Scanning was performed from the lung apices through the lung bases during a single breath hold.

Back to Top | Article Outline

Pulmonary Veins and Left Atrial Measurements

Pulmonary Veins

CTA data were processed on Extended Brilliance workstation (Philips Medical Systems), using multiplanar reformatting software, and on GE Advantage Windows workstation (General Electric), using Card EP software and left atrium volume protocol. All measurements were acquired by two thoracic radiologists by consensus, regarding the measurement plane and the measurement result. The optimal plane for obtaining each of the measurements was selected for each measurement, depending on the orientation of the pulmonary veins and left atrium.

Images were acquired on the axial plane and reconstructed on the coronal, coronal-oblique, axial-oblique, and sagital planes. The diameter of each pulmonary vein ostium was measured in three axes. The best location for obtaining the measurements on the preoperative CTA examination was determined by consensus, and paired measurements at the same location were performed on the postoperative examinations. The transverse diameter was measured on the oblique coronal, coronal, or axial planes as considered best. Perpendicular long and short axes were measured in orthogonal plane (Fig. 2).

Three diameters of the left atrium were derived, including the largest left-to-right and anterior-posterior diameters, measured on the axial or oblique axial planes, and the largest cranio-caudal diameter, which was measured on the sagital reconstruction plane (Fig. 3). Paired measurements at the defined anatomic sites were obtained on both preoperative and postoperative CTA examinations. The mean left atrial diameter was derived from these measurements.

Back to Top | Article Outline

Evaluation of Postoperative Pulmonary Veins Stenosis

Ten patients with postoperative CTA examinations were evaluated for postprocedural stenosis. Pulmonary vein ostia were inspected for focal waist-like stenosis or segmental narrowing. In addition, measurements of pulmonary ostial diameter were obtained in patients with both preoperative and postoperative examinations (group A) to evaluate for interval decrease in size. Significant decrease in size was defined as a reduction in diameter of 20% or more.5

Back to Top | Article Outline

Evaluation of Pulmonary Veins Anatomy

Pulmonary veins anatomy was evaluated for variation in all 11 study subjects.

Back to Top | Article Outline

Clinical Follow-Up

All patients who underwent the Cox-Maze procedure (groups A and B) were followed periodically for clinical symptoms and for the preservation of sinus rhythm. Last follow-up was performed during March 2009.

Back to Top | Article Outline

Statistical Analysis

Paired measurements of pulmonary veins and changes in left atrial diameter were evaluated with the Wilcoxon nonparametric test.

Back to Top | Article Outline


Clinical Outcome and Follow-Up

Sinus rhythm was restored in all 10 patients without any surgical complication. No patient experienced symptoms suggesting pulmonary vein stenosis8 during the follow-up period (66 ± 6 months). One patient developed supraventricular tachycardia 2 years after the operation. Medical treatment resulted in regular but slow rhythm. A pacemaker was implanted but had to be removed because of infection involving also the mitral prosthesis. She underwent successful reoperative mitral valve replacement. Another patient has recurrent paroxysmal atrial fibrillation. All other patients have remained in sinus rhythm and were asymptomatic.

Back to Top | Article Outline

Pulmonary Vein Anatomy

Of the 11 patients, six (56%) had standard pulmonary venous anatomy, with two separate pulmonary veins ostia on each side. Two patients (18%) had separate right middle lobe vein draining into the left atrium (Fig. 4). Three patients each (∼27%) had a different pulmonary venous anatomy. One had an additional right pulmonary vein draining into the atrial roof; another one had a separate lingular vein draining into the left atrium (Fig. 5); and the third one had a left common vein and two separate middle lobe veins joining the left atrium separately.

Back to Top | Article Outline

Size of the Pulmonary Vein Ostia and Assessment of Pulmonary Vein Stenosis

A total of 84 paired measurements in 28 veins in six patients were acquired in group A before and after surgery, derived from pre- and postoperative CTA examinations. The average preoperative transverse diameter and average perpendicular measurement on both the long and the short axes were calculated for each vein; the measurements are listed in Table 1. The mean ostial diameter of the superior veins was larger than that of the inferior pulmonary veins, as reported by Scarf.5

On postoperative CT examinations, a slight change in pulmonary vein diameter in general was observed, showing a reduced diameter of less than 20% or slight dilatation, with no statistical significance. The average difference was calculated for the transverse measurement and for the two perpendicular measurements. The standard deviation of difference comparing preprocedural and postprocedural size was calculated. Average change in pulmonary vein size ranged from 1.53 mm decrease to 1.42 mm increase in size. The standard deviation of the difference ranged from 2.03 to 4.08 mm; overall, there was no statistically significant difference in pulmonary vein size in any direction in any of the veins. Detailed results are shown in Table 2.

Pulmonary veins were evaluated for discrete waist-like stenosis in the postoperative studies in all 10 patients (groups A and B). No discrete or segmental stenosis was documented in any of the pulmonary veins (Fig. 6).

Back to Top | Article Outline

Left Atrial Diameter

In the six group A subjects who underwent CT before and after surgery, paired measurements of the largest anterior-posterior, cranio-caudal, and left-right diameters were compared. There was a constant decrease in left atrial size in all three axes. The average reduction in anterior-posterior diameter was 10.98 ± 1.82 mm; average reduction in cranio-caudal diameter was 1.25 ± 7.26 mm; and average reduction in left-right diameter was 10.45 ± 10.64 mm. Although we observed consistent reduction in left atrial diameters, this change did not reach statistical significance.

Back to Top | Article Outline


The lesions to isolate the pulmonary veins are considered the key lesions in any ablation protocol whether done percoutaneousely or surgically. However, in recent years, there have been reports regarding atrial wall damage and pulmonary vein stenosis, sometimes to a significant extent, especially when radiofrequency was used.5,12 Our surgical approach involved a very aggressive cryoablation protocol around and close to the pulmonary vein ostia. In this study, no pulmonary vein stenosis, either discrete or segmental, and no reduction in vein diameter of 30% or greater were documented. Furthermore, on a long-term clinical follow-up, averaging 66 months, patients did not report symptoms suggesting pulmonary vein stenosis. There were, however, slight changes in pulmonary vein diameter that we attributed to changes in intravascular volume, which is expected in such clinical situations. Scharf reports small but statistically significant reduction in pulmonary vein ostial size after radiofrequency ablation.5

The consistent reduction in left atrial diameter observed in our study was insignificant statistically. Perhaps, in a larger population, this difference would have reached statistical significance. This trend for reduction in left atrial diameter may be explained not only by correction of the structural defects but also by improvement in left atrial function. As a result of restoration of sinus rhythm left atrial contractility is improved with subsequent reduction in left atrial size. Similar findings were observed by Thomas et al13, showing decrease in left atrial size and volume, after radiofrequency ablation and restoration of left atrial sinus rhythm. In addition, decrease in intravascular volume may result in decrease in left atrial size as well. Alternatively, development of left atrial wall scarring as a consequence of cryoablation may result in the reduction of left atrial dimensions. Further study of left atrial contractility and functional analysis in patients without structural heart disease undergoing isolated Maze procedure (“Maze only”) will help elucidate this observation.

Recent reports have shown that variation in pulmonary vein anatomy is prevalent and may occur in up to 32% of subjects.14 There is substantial variation in pulmonary venous anatomy, particularly in right-sided veins. The most common variant is separate drainage of right middle lobe veins into the left atrium.14,15 On the left, the most common variant is a single common vein draining all lobes.14 There is also a significant variation in size and shape of pulmonary veins ostia.5,16 Marom et al14 found that patients with separate ostia of the right middle lobe pulmonary veins tend to have higher frequency of atrial fibrillation, suggesting an association between the two. In our study, findings of anatomic variations of the pulmonary veins were documented in 44%, a finding consistent with the reports in the literature.14,15 A successful and complete ablation of the pulmonary veins is mandatory for the success of any procedure to abolish atrial fibrillation. Failure to document an anatomic variation of the pulmonary veins may lead to failure in abolishing atrial fibrillation. In the era of percutaneous ablation of atrial fibrillation and with the minimally invasive Cox-Maze procedure, the understanding of the pulmonary vein anatomy before the procedure is important in facilitating a high success rate, and is extremely important for both cardiologists and cardiac surgeons. Knowledge of standard pulmonary venous anatomy, as demonstrated on CTA, as well as variants is important for preprocedural planning. Most of the information regarding pulmonary vein location and ostia is acquired from axial images and multiplanar reconstructions.12,16 Given the variation in pulmonary vein anatomy in our study group, we decided to change our protocol, and patients now undergo preoperative CTA as a preoperative map for the cryomaze surgical procedure.

In summary, in this preliminary study, we found that the cryosurgical Cox-Maze procedure, which uses a very intensive ablation protocol around the pulmonary veins, did not result in pulmonary vein stenosis. A relatively high incidence of anatomic variations of the pulmonary veins in patients with atrial fibrillation necessitates thorough studies to document the pulmonary veins anatomy before the ablation procedure.

Back to Top | Article Outline


1. Damiano RJ Jr, Gaynor SL, Bailey M, et al. The long-term outcome of patients with coronary disease and atrial fibrillation undergoing the Cox maze procedure. J Thorac Cardiovasc Surg. 2003;126:2016–2021.
2. 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.
3. Cox JL, Ad N. New surgical and catheter-based modifications of the Maze procedure. Semin Thorac Cardiovasc Surg. 2000;12:68–73.
4. Viola N, Williams MR, Oz MC, Ad N. The technology in use for the surgical ablation of atrial fibrillation. Semin Thorac Cardiovasc Surg. 2002;14:198–205.
5. Scharf C, Sneider M, Case I, et al. Anatomy of the pulmonary veins in patients with atrial fibrillation and effects of segmental ostial ablation analyzed by computed tomography. J Cardiovasc Electrophysiol. 2003;14:150–155.
6. Maksimovic R, Cademartiri F, Scholten M, et al. Sixteen-row multislice computed tomography in the assessment of pulmonary veins prior to ablative treatment: validation vs conventional pulmonary venography and study of reproducibility. Eur Radiol. 2004;14:369–374.
7. Chen SA, Hsieh MH, Tai CT, et al. Initiation of atrial fibrillation by ectopic beats originating from the pulmonary veins: electrophysiological characteristics, pharmacological responses, and effects of radiofrequency ablation. Circulation. 1999;100:1879–1886.
8. Packer DL, Keelan P, Munger TM, et al. Clinical presentation, investigation, and management of pulmonary vein stenosis complicating ablation for atrial fibrillation. Circulation. 2005;111:546–554.
9. Calkins H, Brugada J, Packer DL, et al. HRS/EHRA/ECAS expert consensus statement on catheter and surgical ablation of atrial fibrillation: recommendations for personnel, policy, procedures and follow-up. A report of the Heart Rhythm Society (HRS) Task Force on Catheter and Surgical Ablation of Atrial Fibrillation developed in partnership with the European Heart Rhythm Association (EHRA) and the European Cardiac Arrhythmia Society (ECAS); in collaboration with the American College of Cardiology (ACC), American Heart Association (AHA), and the Society of Thoracic Surgeons (STS). Endorsed and approved by the governing bodies of the American College of Cardiology, the American Heart Association, the European Cardiac Arrhythmia Society, the European Heart Rhythm Association, the Society of Thoracic Surgeons, and the Heart Rhythm Society. Europace. 2007;9:335–379.
10. Feld GK, Yao B, Reu G, Kudaravalli R. Acute and chronic effects of cryoablation of the pulmonary veins in the dog as a potential treatment for focal atrial fibrillation. J Interv Card Electrophysiol. 2003;8:135–140.
11. Fuster V, Ryden LE, Asinger RW, et al. ACC/AHA/ESC Guidelines for the Management of Patients With Atrial Fibrillation: Executive Summary A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and the European Society of Cardiology Committee for Practice Guidelines and Policy Conferences (Committee to Develop Guidelines for the Management of Patients With Atrial Fibrillation) Developed in Collaboration With the North American Society of Pacing and Electrophysiology. Circulation. 2001;104:2118–2150.
12. Ghaye B, Szapiro D, Dacher JN, et al. Percutaneous ablation for atrial fibrillation: the role of cross-sectional imaging. Radiographics. 2003;23 Spec No:S19–S33; discussion S48–S50.
13. Thomas L, Boyd A, Thomas SP, et al. Atrial structural remodelling and restoration of atrial contraction after linear ablation for atrial fibrillation. Eur Heart J. 2003;24:1942–1951.
14. Marom EM, Herndon JE, Kim YH, McAdams HP. Variations in pulmonary venous drainage to the left atrium: implications for radiofrequency ablation. Radiology. 2004;230:824–829.
15. Tsao HM, Wu MH, Yu WC, et al. Role of right middle pulmonary vein in patients with paroxysmal atrial fibrillation. J Cardiovasc Electrophysiol. 2001;12:1353–1357.
16. Cronin P, Sneider MB, Kazerooni EA, et al. MDCT of the left atrium and pulmonary veins in planning radiofrequency ablation for atrial fibrillation: a how-to guide. AJR Am J Roentgenol. 2004;183:767–778.
Back to Top | Article Outline


This is an interesting report from Bogot et al examining whether the use of cryoablation resulted in pulmonary stenosis. After a very intensive cryoablation protocol, the authors did not find evidence for pulmonary vein stenosis using computed tomography angiography. The authors also reported a high incidence (45%) of patients with pulmonary vein anatomical variability. This report is valuable because few groups have rigorously looked at pulmonary vein anatomy after ablation therapy. Although cryoablation has been used for 20 years, there have been very few studies examining the pulmonary veins after ablation, using modern imaging techniques. The high incidence of pulmonary vein anatomic variability has been previously reported. The principal weakness of this article is the small number of patients, and the reader is cautioned not to draw sweeping conclusions.


Cryosurgery; Maze procedure; Atrial fibrillation; Pulmonary veins

© 2009 Lippincott Williams & Wilkins, Inc.