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European Journal of Echocardiography 2006 7(6):447-456; doi:10.1016/j.euje.2006.03.008
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Copyright © 2006, The European Society of Cardiology

Transesophageal echocardiography: A screening method for pulmonary vein stenosis after catheter ablation of atrial fibrillation

Carsten Schneider, Sabine Ernst, Edda Bahlmann, Rainer Malisius, Ulrike Krumsdorf, Sigrid Boczor, Friedrun Lampe, Martin Hoffmann-Riem, Karl-Heinz Kuck* and Matthias Antz

Department of Cardiology, AK St. Georg General Hospital, II. Med. Abteilung (Kardiologie), Lohmühlenstraße 5, 20099 Hamburg, Germany

Received 30 September 2005; received in revised form 2 March 2006; accepted after revision 19 March 2006.

* Corresponding author. Tel.: +49 40 2890 2305; fax: +49 40 2890 4444. dr_c_schneider{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
Aims Pulmonary vein (PV) stenosis has been described as a complication after catheter ablation of atrial fibrillation. The aim of the study was to investigate the diagnostic role of transesophageal echocardiography (TEE) in the assessment of PV stenosis.

Methods Ninety-one patients (71 men, mean age 57±16years), initially treated by catheter ablation of atrial fibrillation, underwent re-ablation because of arrhythmia recurrences.

PV angiograms and TEE were performed before the first and second ablation. PVs were analysed in an intraindividual comparison by measurements of mean and peak flow velocity and of velocity time integrals and diameters. PV angiograms served as standard for assessment of PV stenosis.

Results Sixteen of 91 patients developed PV stenoses as a consequence of the first ablation (13 mild PV stenoses, 4 moderate PV stenoses). All patients with PV stenosis were asymptomatic. In moderate PV stenosis (50–70%) a significant increase of blood flow parameters, reduction of vessel diameter, inhomogeneous blood flow and aliasing were demonstrated by TEE. Using quantitative TEE criteria moderate PV stenosis could be identified with a sensitivity of 84% and specificity of 98%. Detection of mild PV stenosis (30–50%) is challenging (sensitivity of 48% and specificity of 75%).

Conclusions TEE identifies significant PV stenosis by assessment of flow characteristics and vessel diameter and can thereby be used as a follow-up tool after catheter ablation of atrial fibrillation.

Keywords: PV; pulmonary vein; TEE; transesophageal echocardiography; Vpeak; peak velocity; Vmean; mean velocity; VTI; velocity time integral


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusions
 References
 
Pulmonary vein (PV) stenosis has been described as a rare but severe complication after radiofrequency current ablation of atrial fibrillation (Afib).1–4 The incidence of significant PV stenosis or total PV occlusion ranges from 1% to 10%, 1.3 to 15months following ablation of Afib.3,5–7 CT or MRI has been used as gold standard to assess PV stenosis. However, these methods are not available everywhere and are associated with radiation (CT) and costs. To investigate whether transesophageal echocardiography (TEE) could serve as a screening method for PV stenosis, we compared TEE data with PV angiography findings during re-ablation procedures to assess PV integrity after PV isolation.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusions
 References
 
Patient population
A total of 91 patients, treated by primary catheter ablation of atrial fibrillation, underwent re-ablation between January 2001 and July 2003 because of recurrent symptomatic atrial fibrillation episodes (71 men, mean age 57±16years).8 All patients underwent PV-angiography at the beginning and at the end of the ablation procedure. Re-ablation was performed after a median time of 105days (range 3–156days) after the first ablation procedure. Concomitant medical therapy consisted of ß-blockers, sotalol, amiodarone, digitalis or class 1 antiarrhythmics. The study was performed observationally.

Ablation and PV angiography
Details of the electrophysiological study and radiofrequency catheter ablation have been reported previously.8 PV isolation was performed using a "Lasso" approach to deploy focal radiofrequency current lesions at the PV-left atrial junction to eliminate PV spike potentials.6,8 Using the transseptal sheath (8F, DAIG SL1, St. Jude Medical, USA) or an additional 7F angiography catheter (Multipurpose, Medtronic, USA) direct contrast injection was performed for each PV to guide catheter placement and the subsequent ablation.

The diameter of each PV was assessed in a retrospective fashion by a single investigator who was blinded to the echo findings. Calibration was performed using the transseptal sheath (8F) or a diagnostic catheter (Parahis, Bioscience Webster, Belgium) as a reference (Marvin, Germany). Using biplane projection (RAO 30°, LAO), the degree of stenosis was angiographically defined as severe if the narrowing of a vessel was more than 70%, as moderate if the narrowing was between 50% and 70% and as mild if the narrowing was between 30 and 50%. Intra-observer variability was investigated by repeated analysis of PV angiograms of 35 patients. A mean variance of measurements of 15% was found.

Data of PV-angiography before ablation served as reference for the interpretation of echo data.

Echocardiographic studies
All patients were investigated by transthoracic and transesophageal echocardiography with commercially available ultrasound imaging systems (Philips Sonos 5500 and General Electric System FiVe). TEE was performed with a multiplane transducer. All patients were studied in lateral supine position under mild sedation with an intravenous bolus of midazolam and were monitored by oximetry.

The first TEE (TEE 1) served as baseline examination before initial ablation, the second TEE (TEE 2) served as follow-up before re-ablation.

The atriovenous junction segments of the left superior and inferior PVs and of the right superior and inferior PVs were explored by multiplane TEE. Two dimensional imaging, colour and pulsed-wave Doppler measurements were performed. PVs were analysed with regard to absolute values of mean – and peak flow velocity, velocity time integrals (VTI) and PV diameter over a complete heart cycle. PV ostia were determined at the end of systole in the atriovenous junction segments by a longitudinal view and two dimensional imaging. By averaging of three consecutive measurements mean values of each parameter were determined. The percent changes of follow-up measurements were compared in an intraindividual comparison to baseline examination independent of the heart rhythm. For pulsed-wave Doppler flow measurements, the sample volume was placed 3 to 4cm inside the PV, mapping from distal to the region of the PV ostium.

In the case of a common PV ostium a separate orifice of the PV was missing. The diameter of each PV corresponded to half of the common PV ostium.

Three independent experienced echocardiographers performed the TEE studies before each ablation. Differences in interpretation were settled by consensus. In addition TEE raw-data of 35 patients were analysed off-line again by the same and by a second reader to determine the reproducibility and intra- and inter observer-variability. A mean variance of diameter measurements of 12% for intra-observer variability and 18% for inter-observer-variability was found.

Statistical analysis
Parameters were described for each of the pulmonary veins and additionally by calculated average value of the four localizations in patients with and without PV stenosis.

For all patients the relative differences between the baseline and follow-up examination were described. The relative differences within the three analysed groups (patients without PV stenosis, patients with mild and moderate PV stenosis) were compared with the paired Wilcoxon Signed Ranks Test, comparisons between the groups were calculated using the Mann–Whitney U-test.

One patient with both a mild as well as a moderate stenotic PV was shifted into the moderate PV stenosis group.

Continuous parameters are displayed as mean and standard deviation or median and range where appropriate. Beside the univariate analyses a general linear model (GLM model) was used, analysing the location of PV and time of measurement and the grade of stenosis.

Based on the analysis of receiver operating characteristic (ROC) curves a classification of TEE parameters was chosen to define sensitivity as well as specificity for all patient groups as high as possible. According to the explanatory analysis, P-values <0.05 were considered to be significant findings.

Statistics were calculated using SPSS for Windows 11.5.2.1., SPSS Inc., 1989–2002; conditional logistic regression: Egret for Windows 2.0.3, CYTEL Software Corporation.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusions
 References
 
A total of 364 PVs of 91 patients were analysed by both angiography and TEE. Angiography revealed 17 PV stenoses as the result of the first ablation procedure in 16 patients. In one patient both a mild and a moderate PV stenosis was observed. At the beginning of the second ablation procedure PV stenosis was found in 8 left superior, 5 left inferior, 3 right superior and 1 right inferior PV. Stenoses were classified as mild in 13 cases (6 left superior, 5 left inferior, 1 right superior and 1 right inferior PV) and as moderate in 4 cases (2 left superior and 2 right superior PVs). A severe PV stenosis was not seen. One patient had a mild and a moderate PV stenosis (left superior and right inferior PV).

In 8 of 91 patients a common PV ostium (5 left PVs, 3 right PVs) could be detected.

TEE was successfully performed in all 91 patients without any complications. All PVs were visualized and assessed, except for two left inferior PVs and two right inferior PVs (1.1%) where only a limited analysis was possible. In patients with angiographically defined common PV ostia seven of eight common ostia could be detected. The average TEE procedure time including analysis of all PVs was 20±5min at the beginning of the study (first 50 patients) and at the end less than 10±5min, independently of the investigator. At baseline (angiogram 1, TEE 1) 36 patients showed sinus rhythm and 55 atrial fibrillation. Before re-ablation (angiogram 2, TEE 2) 43 patients showed sinus rhythm and 48 atrial fibrillation. Patients with atrial fibrillation showed a higher averaged heart rate in comparison to patients with sinus rhythm (TEE 1: 95/min±24 vs. 74/min±12; TEE 2: 84/min±16 vs. 76/min±16, P=001). The heart rate during TEE 1 (88/min±23) did not differ significantly from heart rate during TEE 2 (82/min±16) before the second ablation (P=0.075).

Angiographic studies
In patients without PV stenosis smaller vessel diameters were detected before the second ablation (16.9mm±2.4) in comparison to the first ablation (17.1mm±2.3) (Fig. 1, Table 1b). Vessel diameters were significantly reduced in mild PV stenosis to 32% and in moderate PV stenosis to 50%. No patients with acquired PV stenosis showed any symptoms, especially no signs of pulmonary hypertension, dyspnoea, haemoptysis or periods of pneumonia.


Figure 1
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  		Figure 1 Comparison of angiographic PV diameters in non-stenotic PVs and mild and moderate pulmonary vein stenoses at baseline and during follow-up, indicated as absolute values and percent changes.

 


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  		Table 1a TEE and angiographic data by localization of PV

 


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  		Table 1b TEE and angiographic data of averaged localizations of PV

 
In the present study only patients with recurrent arrhythmias obtained a second PV angiography during the re-ablation procedure. Patients with sinus rhythm or without recurrent arrhythmias were not invasively reinvestigated so that the real incidence of PV stenosis of all ablated patients on the basis of PV angiography is unknown.

Echocardiographic studies
In general linear modelling a multivariate significant difference between the three groups (normal patients, patients with mild and moderate PV stenosis) was observed. Moreover, there was a significant difference between the time of measurement independent of the stenosis group with regard to all four blood flow measurements, as well as for the separate localizations with exception of the diameters of the PV. Echocardiographic signs of pulmonary hypertension were detected neither in patients with normal PVs nor in PV stenosis. In all patients the right ventricular function was not impaired and was unchanged after ablation. In two patients (without PV stenosis) moderate tricuspid regurgitation was detected which was interpreted before ablation as only mild. In a further eight patients mild tricuspid regurgitation with an averaged peak pressure gradient of 15±1.5mmHg was unchanged after ablation. Collapse of the vena cava inferior was assessable in both groups of all patients with normal and abnormal pulmonary veins.

Patients with normal PVs
Based on angiographic data, blood flow characteristics and vessel diameters of 343 non-stenotic PVs were analysed by TEE (Fig. 2a,b). Details of blood flow and diameter measurements for each PV before first (TEE 1) and second ablation (TEE 2) including the percentage of changes are demonstrated in Table 1a,bGo. The right and left superior PVs showed significantly larger diameters in comparison to right and left inferior PVs (P=0.001) and higher flow velocities in comparison to the left inferior PV. Regarding all non-stenotic PVs, higher blood flow velocities were observed during TEE 2 compared to the baseline examination (P=0.003). The averaged diameters did not show significant differences after ablation.


Figure 2
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  		Figure 2 Colour Doppler flow of a normal left superior pulmonary vein (LSPV) (Fig. 2a) with the corresponding normal Doppler flow pattern (Fig. 2b). The sample volume was placed in the region of the atriovenous junction (arrow). Pulsed-wave Doppler displays the peak flow velocity of 45cm/s. LA: left atrium, LAA: left atrial appendage, LV: left ventricle, Vsys: peak systolic velocity, Vdiast: peak diastolic velocity, Vrev: atrial reversal flow.

 
Patients with mild PV stenosis
In mild PV stenosis (13 PVs), higher flow velocities (VTI 31.8±17.1cm) were observed in comparison to baseline examination (VTI 20.2±8.9cm), (P=0.04). Diameter reduction was statistically not significant (TEE 1: 13.0±2.0mm, TEE 2: 12.6±0.043) (Table 1b). In comparison to patients with normal PVs, patients with mild PV stenosis showed smaller diameters (13.0mm±2.0 vs. 14.5mm±1.9, P=0.01) at baseline and during follow-up (12.6mm±2.4 vs. 14.6mm±1.8, P=0.03) (Table 1b). Significant differences in flow velocities could not be detected either at baseline or during follow-up. Regarding the percentage change of follow-up measurements to baseline, no significant differences in any parameters were detected in mild PV stenosis in comparison to normal PVs by TEE.

Patients with moderate PV stenosis
In moderate PV stenosis (4 patients), increased mean flow parameters (Vpeak 133.8±30.6cm/s, Vmean 93.8±37.5cm/s, VTI 71.0±29.5cm) and a reduced diameter (10.0±2.9mm) were detected in TEE 2. In comparison to mild PV stenosis, moderate PV stenosis showed significantly higher flow velocities (Vpeak, Vmean, VTI) (P=0.018) but not significant smaller diameters. In contrast to normal PVs and mild PV stenosis, all moderate PV stenoses showed an inhomogeneous, turbulent flow with aliasing (Fig. 3a,b) (Nyquist level 0.58m/s). In two moderate PV stenoses, the surrounding tissue of the narrowed region of the PV was very echodense, suggesting scar tissue (Fig. 4). In patients with moderate PV stenosis, higher flow velocities (Vpeak, Vmean and VTI) and smaller diameters were observed during follow-up (P<0.001) (Fig. 5) in comparison to patients without PV stenosis. Baseline data did not differ significantly in patients with moderate PV stenosis in comparison to patients with normal PVs. In moderate PV stenosis the relative increase of flow parameters (Vpeak, Vmean and VTI) was higher than in mild PV stenosis (P=0.04) and normal PVs (P<0.001) (Fig. 6). The relative reduction of vessel diameter differed significantly in moderate PV stenosis compared with normal PVs (P<0.001) but not with mild PV stenosis.


Figure 3
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  		Figure 3 Colour Doppler image of a moderate stenosis of the right superior pulmonary vein (RSPV) (Fig. 3a) with assessment of an aliased, turbulent blood flow with reduced vessel diameter (arrow) and accelerated peak flow velocity (Fig. 3b). LA: left atrium, Vpeak: peak flow velocity.

 


Figure 4
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  		Figure 4 2D image of a moderate stenosis of the same vessel as in Fig. 3 (RSPV: right superior pulmonary vein). White arrow marks the stenotic region. LA: left atrium.

 


Figure 5
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  		Figure 5 Comparison of echocardiographic diameters and flow parameters at baseline and during follow-up in non-stenotic PVs and mild and moderate pulmonary vein stenoses.

 


Figure 6
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  		Figure 6 Percent changes of echocardiographic follow-up data to baseline in non-stenotic PVs and mild and moderate pulmonary vein stenoses.

 
Quantitative TEE criteria for detection and classification of the degree of PV stenosis
Derived from TEE data of stenotic PVs and based on ROC curve analysis, we defined 8 quantitative TEE criteria regarding absolute values and percentage of changes during follow-up to classify PV stenosis (Table 2). The diagnostic values of these criteria were retrospectively analysed for all patients. Moderate and mild PV stenosis could be identified with a sensitivity of 84% and 48% and specificity of 98% and 75% using all 8 criteria (Table 2). None of the observed diagnostic parameters could be statistically identified as of special prophylactic value by conditional logistic regression.


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  		Table 2 Sensitivity and specificity of TEE 2 measurements with selected cutpoints

 
Heart rhythm, heart rate and concomitant medical therapy were similar in patients with and without stenosis so that there was no influence on the outcome of the test.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusions
 References
 
Pulmonary vein stenosis is a potential complication after radiofrequency current ablation at the atriovenous junction segments.4,6,9 The definition of the PV ostia can be difficult with wide variations from patient to patient because of the funnel-shaped orifice and the variant PV morphology.10 The long-term effects of radiofrequency current and the risk of progression of an existing PV stenosis in humans are still unclear. In experimental animal studies, the development of PV stenosis depended on the amount of energy applied.11 While acute stenosis is generally easily detected by selective angiograms at the end of the ablation procedure, the identification of slowly developing PV stenosis in the follow-up is more challenging.

Role of MRI and CT
High accuracy and reproducibility of contrast-enhanced 3D MR angiography to detect PV stenosis after radiofrequency catheter ablation have been reported in several studies.12,13 Currently 3D MRI and CT are serving as gold standard for assessing PV stenosis.9,14–18 Arentz et al. showed a high concordance of TEE and MRI in the detection of acquired PV stenosis and underlined the significance of long-term follow-up examinations by TEE or MRI because of late progression of PV stenosis after ablation.7

Echocardiographic studies in patients with non-stenotic PVs
Non-stenotic PVs showed similar flow characteristics and morphology in our study as described in previous studies.19,20 Lower flow velocities of the left inferior PVs in comparison to the right superior PVs might be caused by a non-orthograde flow and non-optimal visualization. Increased flow parameters in non-stenotic PVs after catheter ablation in comparison to pre-ablation measurements have also been reported in intracardiac Doppler echocardiography studies.21 In our study, accelerated flow velocities during follow-up might also be explained by a higher number of patients in sinus rhythm, leading to enhanced flow parameters.22 Regarding the PV ostia, there was consistent under-sizing of the pulmonary vein diameters in comparison to PV angiography, probably due to the technical differences between the two methods of visualization.

Echocardiographic studies in patients with PV stenosis
The first mayor point demonstrated by this study is, that moderate PV stenosis can be identified with high diagnostic accuracy (sensitivity 84%, specificity 98%) by quantitative analysis of blood flow parameters and vessel diameters. However, due to the limited number of PV stenoses, statistical tests failed to identify quantitative TEE factors of special diagnostic value. In our experience the relative increase of VTI >170% in follow-up measurements as well as mean flow velocities >90cm/s have the highest diagnostic value for the identification of a significant PV stenosis. Only in cases of moderate PV stenosis could effects like aliasing with an inhomogeneous turbulent flow inside a narrowed stenotic PV segment be assessed. These should be interpreted as a typical sign of a hemodynamically significant stenosis. In two of four moderate PV stenoses, the PV surrounding tissue was echodense, suggesting the presence of scar tissue. With these additional qualitative criteria, all moderate PV stenoses could be detected.

Secondly, the detection of mild PV stenosis is challenging (sensitivity of 48% and specificity of 75%) and cannot be adequately achieved by analysis of absolute values or the percentage change of follow-up data. This is probably due to the wide range of normal values, as also reported by de Marchi, who investigated 404 individuals without cardiovascular disease by TEE.19

Sohn and Schiller reported a case with a severe stenosis of the left superior PV detected 2months after ablation with an increase of peak flow velocity to more than twice that of the right superior PV.23 Packer et al. reported on 23 patients with severe stenosis of 34 PVs complicating ablation of atrial fibrillation.9 Each patient became symptomatic 103±100days after undergoing ablation, but only in one patient was a pulmonary artery systolic pressure >40mmHg detected. Robbins et al. reported on two patients with severe pulmonary hypertension due to severe stenosis of four PVs after catheter ablation.1 In our study, no patient developed pulmonary hypertension or clinical symptoms corresponding to the fact that all PV stenoses were mild or moderate, but not severe. Other studies for the evaluation of congenital or acquired PV stenosis reported similar results to our own.5,24–26

Diagnostic tools for detection of PV stenosis
Previous case reports have described the diagnostic role of TEE and MRI in detecting PV stenosis.3,14,26 Based on the diagnostic power of TEE, further expensive investigations such as MRI might not be necessary. In selected cases with poor image quality or limited interpretation in the TEE, MRI might be helpful.27

Normal TEE parameters during follow up ascertain intact PVs after catheter ablation. In contrast to MRI, TEE is a cost-effective diagnostic method that can reliably be performed everywhere.

Limitations
This study was performed retrospectively and evaluated only a small number of patients with PV stenosis. In the majority of the patients PV stenosis was only mild. There were no patients with severe stenoses.

Doppler analysis of the inferior pulmonary veins is notoriously difficult due to the unfavourable Doppler angle. Because in our study no patient with moderate stenosis of the inferior pulmonary veins were seen, the question of reduced diagnostic sensitivity of TEE for the screening of inferior stenosis could not be evaluated, but has to be supposed.

Due to the limited number, especially of higher grade PV stenoses and the irregular distribution of stenosis in our patient cohort, the TEE classification of the degree of stenosis can only serve as an orientation.

The TEE findings rely essentially on the angiogram interpretations so that misinterpretation of PV angiograms would have a falsifying effect on the TEE data.


   Conclusions
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
References
 
PV stenosis is a rare, but potentially life threatening complication of primary catheter ablation of atrial fibrillation. It may be diagnosed by TEE on the basis of dynamic evaluation of the PV blood flow. TEE enables reliable, cost-effective, non-invasive follow-up and is likely to find widespread use in the increasing number of ablation centers worldwide.


   Acknowledgements
 
We thank Detlef Hennig for excellent technical assistance.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 

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P. B. Rahmanian, J. G. Castillo, D. Mehta, D. H. Adams, and F. Filsoufi
Epicardial Pulmonary Vein Isolation: A Long-Term Histologic and Imaging Animal Study Comparing Cryothermy Versus Radiofrequency
Ann. Thorac. Surg., September 1, 2008; 86(3): 849 - 856.
[Abstract] [Full Text] [PDF]

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B. De Piccoli, A. Rossillo, C. Zanella, A. Bonso, S. Themistoclakis, A. Corrado, and A. Raviele
Role of transoesophageal echocardiography in evaluating the effect of catheter ablation of atrial fibrillation on anatomy and function of the pulmonary veins
Europace, September 1, 2008; 10(9): 1079 - 1084.
[Abstract] [Full Text] [PDF]

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