DOI: 10.1148/radiol.2373041324
(Radiology 2005;237:868-871.)
© RSNA, 2005
Corrected Tetralogy of Fallot: Delayed Enhancement in Right Ventricular Outflow Tract1
Thomas Oosterhof, MD,
Barbara J. M. Mulder, MD, PhD,
Hubert W. Vliegen, MD, PhD and
Albert de Roos, MD, PhD
1 From the Departments of Radiology (T.O., A.d.R.) and Cardiology (H.W.V.), Leiden University Medical Center, Leiden, the Netherlands; and the Department of Cardiology, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, the Netherlands (T.O., B.J.M.M.). Received July 29, 2004; revision requested October 7; revision received December 13; accepted January 10, 2005.
Address correspondence to T.O. (e-mail: a.de_roos{at}lumc.nl).
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ABSTRACT
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PURPOSE: To evaluate retrospectively the presence of fibrosis and largest diameter of the right ventricular outflow tract (RVOT) by using delayed enhancement magnetic resonance (MR) imaging in patients who had undergone initial correction for tetralogy of Fallot.
MATERIALS AND METHODS: MR imaging was performed in 24 consecutive patients (16 male, eight female; mean age, 25 years; age range, 13–47 years) with corrected tetralogy of Fallot. The study protocol was approved by the local ethics committee, and informed consent was not required. Fifteen minutes after injection of 0.2 mmol/kg gadopentetate dimeglumine, an inversion-recovery turbo field-echo sequence was applied for detection of delayed enhancement. Right ventricular volumes, ejection fraction, and anterior-posterior diameter of the RVOT were calculated. Mann-Whitney nonparametric testing was used to compare measurements of ventricular volume, function, and anterior-posterior diameter of the RVOT in the presence or absence of delayed enhancement. Correlation was tested with Pearson coefficient.
RESULTS: Delayed enhancement was seen in 17 patients in the RVOT. During initial surgery, transannular patching was performed in 13 (76%) of 17 patients, RVOT patching in one (6%) of 17 patients, and the Brock procedure in two (12%) of 17 patients. In one patient, the type of initial RVOT repair was unknown. Patients with delayed enhancement in the RVOT, as compared with those without delayed enhancement in the RVOT, had increased RVOT diameter (32 mm ± 7 [standard deviation] vs 22 mm ± 3, P < .01), decreased right ventricular ejection fraction (43% ± 6.3 vs 54% ± 10, P < .001), and increased end-diastolic volume (175 mL/m2 ± 42 vs 118 mL/m2 ± 34, P < .01). The diameter of the RVOT correlated with increased right ventricular end-systolic volume (R = 0.86) and was inversely related to ejection fraction (R = –0.65).
CONCLUSION: Delayed enhancement occurs frequently in patients after correction for tetralogy of Fallot. Delayed enhancement in the RVOT was associated with RVOT dilatation, which adversely affects right ventricular hemodynamics.
© RSNA, 2005
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INTRODUCTION
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Despite the good long-term prognosis for patients with tetralogy of Fallot, life expectancy is less than that of the normal age-matched population (1). After initial correction for tetralogy of Fallot, pulmonary regurgitation is the most common type of residual lesion (2,3). Previously, the negative effect of right ventricular outflow tract (RVOT) aneurysms on right ventricular function had been established with a semiquantitative approach (4). It is uncertain, however, which role right ventricular fibrosis plays in the development of right ventricular failure.
Segmented inversion-recovery turbo field-echo magnetic resonance (MR) imaging sequences have proved to be effective in facilitating identification of the presence and extent of scarring and fibrosis in the myocardium (5,6). In patients with nonischemic heart disease, different patterns of delayed enhancement have been observed (7,8). Thus, the purpose of our study was to evaluate retrospectively the presence of fibrosis and largest diameter of the RVOT by using delayed enhancement MR imaging in patients who had undergone initial correction for tetralogy of Fallot.
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MATERIALS AND METHODS
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Patient Population
We studied 24 consecutive patients (16 male, eight female; mean age, 25 years; age range, 13–47 years) who had undergone correction for tetralogy of Fallot (mean years after correction, 21.0 years ± 6.7 [standard deviation]). From June 2003 to April 2004, cardiac MR imaging was performed by using a routine clinical protocol. Five (21%) of 24 patients had undergone pulmonary homograft insertion for residual pulmonary regurgitation and/or stenosis. Data from electrocardiography and Holter examinations were obtained from patient records. The study protocol was approved by the local ethics committee. The ethics committee did not require informed consent for our retrospective study. Informed consent to perform the imaging, however, had been obtained from all patients.
MR Imaging and Image Review
Cardiac MR imaging was performed with a 1.5-T system (NT15 Gyroscan; Philips Medical Systems, Best, the Netherlands). A short-axis stack of 14–18 contiguous sections (section thickness of 8-mm with no section gap) was obtained with steady-state free precession cine imaging (3.2/1.6 [repetition time msec/echo time msec], 70° flip angle, and acquired spatial resolution of at least 1.6 x 1.6 x 8), which was performed from the base to the apex of the heart. With these images, ventricular volumes (end-diastolic volume [EDV] and end-systolic volume) and mass were accurately determined by using a software package (Mass; Medis, Leiden, the Netherlands); both values were corrected for body surface area by one author (T.O.). Stroke volume was calculated as EDV minus end-systolic volume, and ejection fraction (EF) was calculated as stroke volume divided by EDV.
The RVOT diameter was measured on an additional cine image and was outlined in the longitudinal axis of the RVOT (Fig 1). The largest anterior-posterior diameter was acquired perpendicular to the long axis of the RVOT during end diastole. By using velocity mapping of the pulmonary trunk, we calculated the pulmonary regurgitant fraction as pulmonary regurgitant volume divided by pulmonary forward volume. A velocity encoding of 1.5 m/sec was used for velocity mapping, and when aliasing occurred, velocity encoding was adjusted. The corrected right ventricular EF was calculated as net pulmonary forward volume divided by right ventricular EDV; net pulmonary forward volume was calculated as pulmonary forward volume minus pulmonary regurgitant volume (9). MR imaging was performed 10–15 minutes after MR angiography of the pulmonary tree by using multiple two-dimensional turbo field-echo inversion-recovery techniques and 0.2 mmol/kg intravenous gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany). Typical imaging parameters included a 400 x 400-mm field of view, 256 x 256 matrix, 5-mm section thickness, 5-mm section gap, 15° flip angle, and 4.53/1.36 (10,11). Depending on the patient's heart rate and heart size, 20–30 sections were obtained during two breath-hold acquisitions of approximately 15 seconds. The inversion time was adjusted to maintain remote myocardial nulling by using real-time imaging; inversion time varied between 200 and 275 msec (10).
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Figure 1. Steady-state free precession cine image (3.2/1.6, 70° flip angle) obtained in patient who underwent correction for tetralogy of Fallot demonstrates sagittal axis of RVOT. End-diastolic frame depicts RVOT aneurysm. Diameter (line) of RVOT measures 5.2 cm.
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Two observers (T.O. and A.d.R., with 3 and 20 years of experience in cardiac MR imaging, respectively) agreed on the presence or absence of delayed enhancement. Delayed enhancement was looked for in the outflow tract of the right ventricular free wall and in the interventricular septum.
Statistical Analysis
All statistical analyses were performed with a commercially available statistical software program (SPSS for Windows, version 12.0.2; SPSS, Chicago, Ill). The mean and standard deviation were calculated for all continuous variables. Mann-Whitney nonparametric testing was used to compare age and measurements of right and left ventricular function, as well as QRS duration and RVOT diameter in the presence or absence of delayed enhancement. Because most of these parameters were not normally distributed, nonparametric testing was used. The Fisher exact test was performed to compare noncontinuous variables in the presence or absence of delayed enhancement. The difference in pulmonary regurgitant fraction between patients with or without transannular patching was determined with Mann-Whitney nonparametric testing. Correlations were tested with the Pearson coefficient. A P value of .05 was considered to indicate a statistically significant difference.
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RESULTS
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All patients completed the protocol, and patient characteristics are summarized in the Table. In 20 (83%) of 24 patients, delayed enhancement was present in the right or left ventricle.
Location of Delayed Enhancement
Delayed enhancement was visible in four locations. First, in 17 (71%) of 24 patients, delayed enhancement was localized to the anterior-superior free wall of the right ventricle or RVOT (Fig 2a–2c). During initial surgery, transannular patching was performed in 13 (76%) of 17 patients, RVOT patching in one (6%) of 17 patients, and the Brock procedure (infundibulectomy and valvulotomy through an incision in the right ventricle) in two (12%) of 17 patients. In one patient, the type of initial RVOT repair was unknown. Second, in 21 (88%) of 24 patients, delayed enhancement was observed in the basal part of the interventricular septum at the site of the initial ventricular septal defect closure (Fig 2d). Third, in one (4%) of 24 patients, delayed enhancement was present in the apex of the left ventricle at the site where initial apical ventricular ventilation had been performed during initial correction. Finally, in eight (33%) of 24 patients, delayed enhancement was faintly observed at the anterior and posterior attachment site of the right and left ventricle.
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Figure 2a. Inversion-recovery turbo field-echo MR imaging (4.5/1.4, 15° flip angle) was used to obtain (a) longitudinal axis, (b) short axis, and (c) transverse images that demonstrated delayed enhancement (arrow in a–c) in RVOT. (d) Short-axis image in one patient showed delayed enhancement (arrow) that extended beyond site of initial ventricular septal defect repair and into right ventricular trabeculae.
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Figure 2b. Inversion-recovery turbo field-echo MR imaging (4.5/1.4, 15° flip angle) was used to obtain (a) longitudinal axis, (b) short axis, and (c) transverse images that demonstrated delayed enhancement (arrow in a–c) in RVOT. (d) Short-axis image in one patient showed delayed enhancement (arrow) that extended beyond site of initial ventricular septal defect repair and into right ventricular trabeculae.
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Figure 2c. Inversion-recovery turbo field-echo MR imaging (4.5/1.4, 15° flip angle) was used to obtain (a) longitudinal axis, (b) short axis, and (c) transverse images that demonstrated delayed enhancement (arrow in a–c) in RVOT. (d) Short-axis image in one patient showed delayed enhancement (arrow) that extended beyond site of initial ventricular septal defect repair and into right ventricular trabeculae.
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Figure 2d. Inversion-recovery turbo field-echo MR imaging (4.5/1.4, 15° flip angle) was used to obtain (a) longitudinal axis, (b) short axis, and (c) transverse images that demonstrated delayed enhancement (arrow in a–c) in RVOT. (d) Short-axis image in one patient showed delayed enhancement (arrow) that extended beyond site of initial ventricular septal defect repair and into right ventricular trabeculae.
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Clinical Correlates of Delayed Enhancement
Patients with delayed enhancement in the free wall of the right ventricle demonstrated increased right ventricular EDV, increased right ventricular end-systolic volume, increased QRS duration, and decreased right ventricular EF, with no significant difference in pulmonary regurgitation (Table). RVOT diameter was increased in patients with delayed enhancement in the RVOT (Fig 2). Of the two patients with nonsustained ventricular tachycardia, both had delayed enhancement in the RVOT, and one patient had delayed enhancement that extended beyond the original site of ventricular septal defect repair (Fig 2d).
Clinical Correlates of RVOT Diameter and Right Ventricular Function
Increased diameter in the RVOT is associated with increased right ventricular EDV (R = 0.75, P < .001), decreased right ventricular EF (Fig 3b), decreased corrected right ventricular EF (R = –0.43, P = .04), and increased QRS duration (R = 0.57, P = .01). There was a trend toward a higher pulmonary regurgitant fraction in patients with transannular patching versus those without transannular patching (37% ± 16 vs 20% ± 19, P = .142). Pulmonary regurgitation, however, was not correlated with EF (R = –0.08, P = .70). The correlation between right ventricular EDV and right ventricular EF was –0.48 (P = .05). Furthermore, right ventricular EF was correlated with both QRS duration (R = –0.76, P < .001) and left ventricular EF (R = 0.43, P = .04).
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Figure 3a. Graphs demonstrate correlation between (a) RVOT diameter and fibrosis and (b) RVOT diameter and right ventricular EF. RVOT diameter was larger in presence of fibrosis and was associated with decreased right ventricular EF (R = –0.65).
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Figure 3b. Graphs demonstrate correlation between (a) RVOT diameter and fibrosis and (b) RVOT diameter and right ventricular EF. RVOT diameter was larger in presence of fibrosis and was associated with decreased right ventricular EF (R = –0.65).
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DISCUSSION
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In this study, we used delayed enhancement MR imaging to identify fibrosis at different sites in the right and left ventricles of patients who had undergone correction for tetralogy of Fallot. The presence of fibrosis in the RVOT had the most hemodynamic consequences and was most likely the result of initial surgical intervention. Furthermore, we observed fibrosis at the site of initial ventricular septal defect repair. The presence of fibrosis may contribute to arrhythmia propensity in patients who have undergone correction for tetralogy of Fallot, as observed in two patients. Finally, the results of this study confirm the important additional role of RVOT dilatation on right ventricular function by using a quantitative approach.
Delayed enhancement MR imaging may contribute to a better understanding of the pathogenesis of right ventricular dysfunction and the presence of arrhythmias in adult patients with congenital heart disease. In the present study, we observed fibrosis mainly in the RVOT and in the basal interventricular septum. It is possible that delayed enhancement at the attachment site of the right and left ventricles may be a result not of fibrosis but rather of a different arrangement of the myocardial fibers in this area. This hypothesis, however, needs histologic confirmation. The presence of fibrosis in the RVOT had the most consequences on right ventricular hemodynamics. This is most likely explained by the type of initial RVOT repair. Right ventricular patching (ie, right ventricular or inserted transannular patching) causes the greatest amount of right ventricular fibrosis and hence right ventricular dilatation and/or dysfunction (12). More studies are needed, however, to verify whether postoperative fibrosis causes RVOT dilatation and arrhythmias or if fibrosis is only an epiphenomenon of the initial surgery.
Of interest is that, in one patient, delayed enhancement extended beyond the site of initial repair. Furthermore, two patients who did not undergo patching during initial correction and who underwent the Brock procedure had delayed enhancement in the RVOT. It is possible that a small subgroup of patients may exist for whom delayed enhancement extends beyond the site of initial repair, which would have consequences for arrhythmia propensity and right ventricular failure. It is difficult, however, to distinguish surgically related fibrosis from fibrosis that extends beyond the exact site of initial repair, especially in the RVOT.
Not all patients who had undergone previous surgery showed fibrosis at the targeted myocardium. Two patients who underwent transannular patching during initial correction and three who underwent initial ventricular septal defect repair did not show delayed enhancement in the myocardium. It is possible that the cardiac MR imaging technique that was used in the present study was not sensitive enough to demonstrate minor surgery-related injury to the myocardium.
We believe that right ventricular enlargement is a result of both pulmonary regurgitation and increased RVOT diameter owing to initial repair (2–4,13,14). Right ventricular systolic function was hampered by increased RVOT diameter in our study. This is conceivable because a part of the right ventricular free wall does not move (or moves outward) with ventricular contraction in these patients. Davlouros et al (4) used a semiquantitative approach to identify the negative effect of RVOT aneurysms or dyskinesia on right ventricular function. We confirmed this finding with a quantitative approach. Furthermore, right ventricular systolic dysfunction might be caused by right ventricular enlargement that is partly imposed by pulmonary regurgitation. Although the correlation between RVOT diameter and right ventricular EF in our study was higher than the correlation between RVOT diameter and right ventricular EDV, it is not unlikely that right ventricular EDV influences right ventricular EF in another way. Geva et al (15) suggested that the interplay between progressive right ventricular enlargement and the failure of a compensatory increase in right ventricular mass may contribute to right ventricular systolic dysfunction. Finally, increased QRS duration, which results in delayed or uncoordinated contraction owing to blockage in the right ventricular bundle branch, was strongly correlated with right ventricular systolic dysfunction. Currently, a QRS duration of 180 msec or greater is associated with development of life-threatening arrhythmias (16). In the current study, both patients with nonsustained ventricular tachycardia had a QRS duration of less than 180 msec and fibrosis in the right ventricle. The role of delayed enhancement in the identification of patients who may experience life-threatening arrhythmias, however, remains to be investigated.
The usefulness of identifying delayed enhancement in the RVOT as a marker of dilatation is limited because considerable overlap in RVOT diameters exists in patients with and those without delayed enhancement in the RVOT. Furthermore, spatial resolution limited identification of the transmural extent of delayed enhancement in the thin-walled RVOT. Finally, larger follow-up studies are needed to confirm our observations.
In conclusion, delayed enhancement occurs frequently in the RVOT and basal interventricular septum, mostly as a result of initial cardiac repair for tetralogy of Fallot. Furthermore, fibrosis in the RVOT was associated with RVOT dilatation, which adversely affects right ventricular hemodynamics.
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ACKNOWLEDGMENTS
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We thank Hildo Lamb, MD, PhD, for providing valuable input during the revision process of this article.
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FOOTNOTES
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Abbreviations: EDV = end-diastolic volume • EF = ejection fraction • RVOT = right ventricular outflow tract
Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, T.O., A.d.R.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, T.O., A.d.R.; clinical studies, T.O., A.d.R.; statistical analysis, T.O.; and manuscript editing, all authors
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ABSTRACT
INTRODUCTION
