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CLINICAL STUDY: NEW METHODS

Ultrafast three-dimensional contrast-enhanced magnetic resonance angiography and imaging in the diagnosis of partial anomalous pulmonary venous drainage

Victor A. Ferrari, MD, FACC^*, Craig H. Scott, MD, FACC^*, George A. Holland, MD , Leon Axel, PhD, MD and Martin St. John Sutton, FRCP, FACC^*

^* Adult Congenital Heart Disease Program, Cardiovascular Division, Department of Medicine (Cardiovascular Division), University of Pennsylvania Medical Center, Philadelphia, Pennsylvania, USA
Department of Radiology, University of Pennsylvania Medical Center, Philadelphia, Pennsylvania, USA
Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, Pennsylvania, USA

Manuscript received September 20, 1999; revised manuscript received November 3, 2000, accepted December 12, 2000.

Reprint requests and correspondence: Dr. Victor A. Ferrari, Cardiovascular Division, University of Pennsylvania Medical Center, 3400 Spruce Street, Philadelphia, Pennsylvania 19104
ferrariv{at}mail.med.upenn.edu

	Abstract

Top Abstract Methods Results Discussion Conclusions References

 
OBJECTIVES

The purpose of our study was to evaluate patients with suspected anomalous pulmonary veins (APVs) and atrial septal defects (ASDs) using fast cine magnetic resonance imaging (MRI) and ultrafast three-dimensional magnetic resonance angiography (MRA).

BACKGROUND

Precise anatomic definition of anomalous pulmonary and systemic veins, and the atrial septum are prerequisites for surgical correction of ASDs. Cardiac catheterization and transesophageal echocardiography (TEE) are currently used to diagnose APVs, but did not provide complete information in our patients.

METHODS

Twenty consecutive patients with suspected APVs were studied by MRA after inconclusive assessment by catheterization, TEE or both. The MRI images were acquired with a fast cine sequence and a novel ultrafast three-dimensional sequence before and after contrast injection.

RESULTS

Partial anomalous pulmonary venous drainage was demonstrated in 16 of 20 patients and was excluded in four patients. Magnetic resonance imaging correctly diagnosed APVs and ASDs in all patients (100%) who underwent surgery. For the diagnosis of APVs, the MRI and catheterization results agreed in 74% of patients and the MRI and TEE agreed in 75% of patients. For ASDs, MRI agreed with catheterization and TEE in 53% and 83% of patients, respectively.

CONCLUSIONS

Fast cine MRI with three-dimensional contrast-enhanced MRA provides rapid and comprehensive anatomic definition of APVs and ASDs in patients with adult congenital heart disease in a single examination.

Abbreviations and Acronyms   3D = three-dimensional   APV = anomalous pulmonary vein   APVD = anomalous pulmonary venous drainage   ASD = atrial septal defect   IVC = inferior vena cava   MRA = magnetic resonance angiography   MRI = magnetic resonance imaging   PA = pulmonary artery   Qp = pulmonary blood volume flows   Qs = systemic blood volume flows   Qp/Qs = shunt fraction   RUL = right upper lobe   SPGR = spoiled gradient   SVASD = sinus venosus atrial septal defect   SVC = superior vena cava   TE = echo time   TEE = transesophageal echocardiography   TR = repetition time   TTE = transthoracic echocardiography

Magnetic resonance imaging, which is an established method for evaluation of ASDs, has proven useful using both spin echo and conventional cine gradient echo techniques (15–17). In addition, recent advances have led to precise identification of the size and shape of ASDs using phase-contrast cine MRI methods (18). The advent of rapid imaging using segmented k-space techniques has reduced data acquisition time dramatically, allowing dynamic cine MRI at a desired slice location in a single breath-hold, which aids in localization of intracardiac shunts (19).

Precise anatomic knowledge of the drainage of APVs, location of associated ASDs and the presence of abnormal systemic venous connections are important prerequisites for planning optimal surgical repair (20).

The aim of this prospective study was to use these new technologic developments in MRI and ultrafast 3D MRA to define the anatomy of the pulmonary venous circulation and the atrial septum in 20 consecutive adult patients with suspected APVD and ASDs, in whom inconclusive diagnostic information was obtained at cardiac catheterization, TTE and/or TEE.

	Methods

Top Abstract Methods Results Discussion Conclusions References

 
Patient population.   We studied 20 consecutive adult patients (9 male and 11 female) aged 22 to 68 years (mean 42 ± 13), with suspected APVD and/or ASDs. All were referred specifically for ultrafast MRI and MRA to determine the presence of APVs and ascertain the presence and anatomic location of the ASDs, because prior cardiac catheterization data, TEE or both had proved inconclusive.

The most common presenting symptoms were dyspnea on exertion (75%), palpitations (40%) and fatigue (30%). Two patients presented with atypical chest pain, and two patients were seen in follow-up for a heart murmur. Two patients had documented paroxysmal atrial fibrillation. Two patients (10%) had multiple skeletal abnormalities including short humeri, distal radio-ulnar synostoses, abnormal carpal bones and bilateral digitization of the thumbs, consistent with the hand-heart or Holt-Oram syndrome (21), and one patient (5%) had Swyer-James syndrome with atresia of the right pulmonary artery (22) (Table 1).

Magnetic resonance imaging and angiography.   MR imaging
All MRI was performed on a 1.5-T Signa scanner (General Electric Medical Systems [GEMS], Milwaukee, Wisconsin), using an enhanced gradient system (maximal gradient strength = 2.3 Gauss/cm in 150 µs). We used a custom torso multicoil array surface coil set to improve signal-to-noise ratio (23). Following scout imaging, a set of interleaved T₁-weighted spin echo images (5-mm thickness with 5-mm skip) was acquired from just cephalad to the manubrium to the level of the hepatic veins.

ASD imaging
We used a combination of techniques for the assessment of ASD location, size and direction of shunt flow. An ultrafast ECG-gated multiphase segmented k-space gradient-echo sequence was used to assess the structure and potential flow across the interatrial septum, providing 10 to 14 frames through the cardiac cycle at each imaging plane (24). Single breath-hold periods of 13 to 18 s were required at each slice location. Imaging variables included 26 to 32 cm field of view; 256 x 128 acquisition matrix interpolated to 256 x 256; 6-mm slice thickness; echo time (TE) 1.8 to 2.3 ms, repetition time (TR) 6.7 to 8.3 ms; 6 to 8 k-space lines per cardiac frame; number of signal averages = 1, digital receiver bandwidth ± 32 kHz; excitation flip angle = 30°. Imaging commenced at the site of potential communication between a suspected APV (based on spin echo images) and the superior vena cava (SVC), brachiocephalic vein or other structure, and continued through the entire interatrial septum. The presence of a consistent flow disturbance (signal void or moving blood) from the left atrium to the right atrium at the level of the high interatrial septum defined a sinus venous ASD (SVASD). A flow disturbance associated with a defect in the interatrial septum at the level of the fossa ovalis defined a secundum ASD. If the diagnosis of ASD was uncertain, the TE and TR of the segmented k-space sequence was lengthened to at least twice the nominal values and then repeated at the level of the most suspicious site. If this was still unrevealing, a conventional cine gradient echo sequence was performed (TE approximately 13 ms, TR approximately 33 ms), followed by a phase-contrast cine MRI sequence to permit more sensitive flow detection. Quantitative assessment of the ASD size was determined from the maximum defect size noted on the cine images. The ASD sizes were designated as follows: small, <1 cm; moderate, 1 to 1.5 cm; and large, >1.5 cm.

MR angiography
We modified a fast 3D spoiled gradient (SPGR) sequence to minimize TE and TR by decreasing the width of the radiofrequency pulse used for slice excitation (TE) in a standard fast SPGR sequence from 3.20 to 1.28 ms (14). In addition, first-order gradient-moment nulling was eliminated and an asymmetric echo was used. Coronal ultrafast 3D SPGR (UF-3DSPGR) imaging was performed using the conventional body coil before and after intravenous administration of a gadolinium-based contrast agent (gadopentetate dimeglumine, "Magnevist," Berlex Laboratories, Cedar Knolls, New Jersey; or gadoteridol, "Prohance," Bracco Diagnostics, Princeton, New Jersey) with the following parameters: TR = 4.8 to 7 ms; flip angle 60°; matrix size 256 x 128; slice thickness 2 to 4 mm; receiver bandwidth 64 kHz; and acquisition time 18 to 34 s. A field of view of 26 to 38 cm was used to include the majority of the thorax. The patients’ arms were positioned above the head (coronal plane imaging) or on the abdomen (sagittal plane imaging) to avoid aliasing. Scans were completed in 18 to 34 s. Scan time was reduced in those patients who could not sustain breath-holds for 30 s despite hyperventilation and oxygen by nasal cannula at up to 4 liters/min. Later software improvements allowed the TE to be reduced to 1.11 ms (final three patients).

Injection
Patients underwent imaging before, during and twice after intravenous injection of contrast. All patients received 20 to 40 ml of contrast agent administered intravenously, with injections performed by hand using a stopwatch. Injection rate was modified based on the acquisition time of the scan to obtain as uniform an arterial contrast concentration as possible throughout the image acquisition. Scanning commenced approximately 10 s after contrast injection in patients with normal right and left ventricular function (assessed from cine or multiphase GRE images), and approximately 20 s after injection in patients with moderate or severe right or left ventricular dysfunction.

Image analysis
Images were analyzed on an Advantage Windows workstation (GEMS; Milwaukee, Wisconsin) featuring interactive 3D reformatting, variable reconstructed slice thickness and oblique and multiaxis reconstruction (Fig. 1), and displayed using the maximum intensity projection algorithm (25).

View larger version (115K): [in this window] [in a new window]   Figure 1 The magnetic resonance angiography 3D data set is collected as a series of contiguous slabs in either the coronal or sagittal plane. The contrast-enhanced data set shown is a coronal acquisition with the most anterior images to the left of the stack and the posterior structures to the right. Selected images from the data set demonstrate an anomalous right upper pulmonary vein entering the superior vena cava just above the junction with the right atrium (arrow, left), and the right lower lobe pulmonary vein entering the left atrium normally (arrow, right). RLL = right lower lobe; RUL = right upper lobe.

Transesophageal echocardiography.   Transesophageal echocardiograms were obtained in 12 patients. Images of the right and left heart chambers (including sizes and function) were obtained, and attempts were made to define the entire interatrial septum, all the pulmonary veins, the vena cavae and coronary sinus in all patients from multiple views. Doppler color flow mapping and peripheral venous contrast injections of agitated saline solution were performed to establish the presence, size, location and direction of blood flow across the interatrial septum.

Comparative data.   Data were analyzed using an agreement analysis that compared the number of instances in which the different techniques agreed or disagreed for a given test situation (26). This analytical approach was the most appropriate since not all patients underwent imaging with each technique, and not all patients underwent surgical correction. An overall comparison was performed among MRI, cardiac catheterization and TEE for detection of APVs and ASDs.

	Results

Top Abstract Methods Results Discussion Conclusions References

 
Magnetic resonance imaging and angiography.   Fast cine MRI with UF-3DSPGR contrast-enhanced MRA was performed in all 20 patients without complication. Total time per patient for completion of all imaging was 58 ± 12 min. Partial APVD was demonstrated in 16 of 20 patients and was definitively excluded in four patients. The region of lung drained by APV involved one pulmonary lobe in four patients (Fig. 2), two lobes in 10 and the complete right lung in two. Fifteen APVs were right-sided and one was left-sided. Drainage of the APV was supracardiac in 13 and infracardiac in three. These latter three patients had scimitar syndrome, which consisted of drainage of the whole right lung (in two) and two lobes of the right lung (in one) via an APV to the inferior vena cava (IVC) (27) (Fig. 3). One of these patients (not the subject of Fig. 3) was described in a previous report (28). Four patients had normal pulmonary venous drainage, of whom one had Eisenmenger’s syndrome with a nonrestrictive ventricular septal defect (VSD), one had a restrictive muscular VSD, one had atresia of the right pulmonary artery (Swyer-James syndrome) with a secundum ASD and one had a secundum ASD only.

View larger version (165K): [in this window] [in a new window]   Figure 2 Figure 2 shows a reformatted oblique coronal magnetic resonance angiography (MRA) from the data set in Figure 1 that now demonstrates the more complete course of the right upper lobe pulmonary vein (RUL). In this patient with anomalous pulmonary venous return from one lobe, the RUL enters the superior vena cava at a level 1.4 cm superior to the right atrium (arrow). All MRA images in this report are displayed as reformatted maximal intensity projection images.

View larger version (81K): [in this window] [in a new window]   Figure 3 (A) Oblique coronal image through a 3D dataset, showing an anomalous pulmonary vein formed by the right upper and right middle pulmonary veins that courses through the right thorax and enters the inferior vena cava below the level of the diaphragm (arrow). Despite the large field of view and the fact that the vessel crosses the diaphragm, the vessel’s course is clearly depicted. (B) Right lower lobe pulmonary vein enters the left atrium normally (arrow). The right pulmonary artery is identified by the open arrow.

View larger version (167K): [in this window] [in a new window]   Figure 4 Reformatted oblique section of a 3D contrast-enhanced magnetic resonance angiography data set demonstrating anomalous connection of the left upper and left middle pulmonary veins to a vertical vein that enters the left brachiocephalic vein (BcphV). Communication between the BcphV and the right superior vena cava (SVC) is seen proximal to the entry of the SVC into the right atrium. The aorta and left pulmonary artery (PA) are also noted. This figure demonstrates the utility of the reformatting technique, which permits reorientation of the data set from a coronal (original) to an oblique parasagittal view and delineation of the course of nearly the entire BcphV. APV = anomalous pulmonary vein.

Atrial septal defect was diagnosed by oximetry and/or selective contrast angiography in six patients (43%), and was "suspected" in two additional patients, although the location and type of defect could not be determined.

Transesophageal echocardiography.   Twelve patients underwent TEE, and APVD was diagnosed in seven patients, although the specific lung segments drained could not always be determined.

An ASD was definitively identified in eight (67%), and in another patient, the presence of a SVASD was "suspected" but not confirmed. Transesophageal echocardiography excluded ASD in one patient, but misclassified two SVASDs as normal.

ASD size.   The estimated ASD size by MRI correlated well with shunt fraction measurements by catheterization (Table 3), with no major discrepancies noted. There was 89% agreement for shunts >1.5:1 (MRI identified one shunt of 1.7:1 as small rather than moderate). One artifactual disagreement occurred in a patient with Eisenmenger’s physiology and right-to-left shunting. There was 100% agreement for shunts of <1.5:1. One patient underwent catheterization at age 10 years with a calculated shunt of 2.5:1 identified as an APV only, but 17 years later had a small, very superiorly located SVASD by TTE and MRI with slightly dilated right heart chamber sizes and a normal estimated pulmonary artery (PA) systolic pressure.

Surgical intraoperative findings.   Ten patients underwent surgical correction of APVs and/or closure of the ASDs, and the intraoperative findings are outlined in Table 1. The anatomic findings at surgery confirmed those obtained by MRI and MRA in all cases (100%), including ASD size. In this subgroup of patients with surgical correlation (Table 2), the predictive diagnostic accuracy of TEE for APV was 80%, and 78% for cardiac catheterization. For detection of ASDs, the predictive diagnostic accuracy of TEE was 80%, and 44% for catheterization. Ten patients did not undergo surgical repair: four because of severe pulmonary hypertension (one of whom died suddenly without autopsy, three are currently listed for lung transplantation), one was not a surgical candidate due to severe chronic obstructive pulmonary disease and five did not undergo surgical closure because the intracardiac shunt was small (Qp:Qs < 1.5:1) with only minimal elevation of PA pressures.

Agreement analysis.   Table 4 summarizes the agreement analysis. Specific comments for each anomaly follow.

There were three false negatives by TEE, two due to high insertion of the APV (>2.0 cm above the right atrium) into the SVC, and the third a left upper and middle lobe APV draining to the brachiocephalic vein (Fig. 4).

ASD.   Catheterization and MRI agreed in only 10 of 19 (53%) cases, and disagreed in 8 of 19 (37%), all cases being false negatives (mean shunt ratio 2.5:1). One patient’s catheterization report did not specifically comment on the presence or absence of an ASD. In eight further patients, six with sinus venous and two with small secundum defects, the ASD was not diagnosed either by oximetry or by crossing the atrial septum at catheterization. Four of six SVASDs were located high in the interatrial septum; however, two were crescent-shaped due to an extensive defect of the upper septum, yet still could not be crossed by a catheter. Both patients with small secundum defects also had APVs, one with a left-sided APV (Fig. 4), and the other had associated severe pulmonary hypertension.

There were two false negative studies with TEE. Both patients had high SVASDs that could not be fully visualized on TEE, but were well delineated on MRI and confirmed by surgery.

	Discussion

Top Abstract Methods Results Discussion Conclusions References

 
The major finding in this prospective study is that our modified imaging methods using fast segmented k-space imaging and contrast-enhanced ultrafast 3D MRA allowed unequivocal detection of APVs and ASDs in a population of patients in whom diagnosis was inconclusive by cardiac catheterization and TEE. The advantages of this technique include imaging of a larger anatomic area than possible by TEE or catheterization and rapid data acquisition in a single breath-hold, which are important for imaging vascular structures within the thorax. Magnetic resonance angiography enables PAs and pulmonary veins to be differentiated and provides visualization of even the small pulmonary venous radicles, permitting determination of the number of anomalously draining pulmonary lobes. Furthermore, the entire course of the APV can be followed from the periphery through the hilum and mediastinum to their drainage sites. Accurate identification of APVD patterns is important since the surgical correction of APVs from the right upper and middle pulmonary lobes is different from that for infracardiac drainage or left-sided APVs (20). Noninvasive definition of retrocardiac or infracardiac pulmonary venous drainage and the anatomy of the lung from which the anomalous drainage derives is possible only with MRA (29).

Difficulties in diagnosing APVs may occur with TTE or TEE and cardiac catheterization. Restricted acoustic windows limit the use of TTE, and dilution of hand-injected angiographic contrast or levophase angiography at cardiac catheterization limits visualization of the pulmonary veins. Catheterization is also limited by the inability to distinguish an ASD from an APV when oximetry indicates an intracardiac shunt at atrial level if the ASD cannot be crossed with a catheter. Crescent-shaped SVASDs or those high in the atrial septum may be difficult to cross and thereby escape detection by catheterization, and in this study accounted for most of the eight false negatives at catheterization, despite a significant shunt fraction (mean Qp:Qs = 2.5:1). Although TEE enables inspection of the entire interatrial septum, the predictive accuracy of TEE for detection of normal and anomalous pulmonary veins has varied widely from 60% to 93% (3), and in our study was 75% (Fig. 5). Anomalous pulmonary veins that insert >2 cm above the right atrium or left-sided APVs were particularly difficult to detect in our study. Furthermore, the presence of four pulmonary veins does not exclude the presence of additional APVs (2), and recognition of multiple branching APVs or atypical drainage patterns are difficult to achieve by TEE (8). Also, TEE provides only limited information regarding the extent or region of the lung that has abnormal drainage (2,8).

View larger version (155K): [in this window] [in a new window]   Figure 5 Axial spin echo MRI demonstrating a sinus venosus defect (arrow) just caudal to the insertion of the superior vena cava and between the right atrium (RA) and left atrium (LA). Due to its location high in the atrium, it is sometimes difficult to cross with a catheter or to visualize with transesophageal echocardiography (TEE). This defect was misidentified on both catheterization and TEE examinations.

In this study, we made the initial tacit assumption that MRA was the reference standard before we analyzed the data obtained at cardiac catheterization, TTE and TEE or reviewed the intraoperative findings. The intraoperative findings in all 10 surgical patients were completely concordant with the MRA findings. The definitive diagnosis of ASD and APVD was established by cardiac catheterization in 53% and 74% of patients, respectively, compared to MRI and by echocardiography (TTE and/or TEE) in 83% and 75%, respectively. Both techniques had false positive and false negative diagnoses. Magnetic resonance angiography demonstrated that most patients (94%) had right-sided APVs, 75% of the APVs involved two or more lobes and 25% were from single lobes. Transesophageal echocardiography was not helpful in making a definitive diagnosis of infracardiac pulmonary venous drainage to the IVC, although this was suspected in two cases. Both cardiac catheterization and echocardiography identified the five patients with severe pulmonary hypertension, one of whom died from end-stage right heart failure (Patient 1) and two of whom are currently listed for lung transplantation (Patients 4 and 13). Quantitative assessment of PA pressures and direction of intracardiac shunt flow by cardiac catheterization plays an important role in determining the need for surgical correction, and our MRI and MRA methods in this study were used as an adjunct to catheterization in this decision process.

Newer methods have demonstrated that MRI techniques can accurately quantitate the size and degree of shunting of ASDs, and may soon permit a completely noninvasive preoperative assessment (18,30,31).

Study limitations.   The small sample size limits the more general applicability of our findings; however, despite this fact, important concepts and pitfalls of conventional imaging techniques were revealed. The dramatic difference in performance between MRI and standard methods may be due to selection of patients in whom conventional detection strategies failed; however, the surgical confirmation of the results lends support to the overall accuracy of the method. The MRA technique is not cardiac-gated, which may obscure small areas of interest, and therefore requires the use of additional gated sequences for accurate quantitation of ASD size and visualization of flow direction.

	Conclusions

Top Abstract Methods Results Discussion Conclusions References

 
We have demonstrated that our new MRA imaging strategy, which is performed in a single breath-hold, can resolve the residual diagnostic problems in adult patients with ASDs and APVD. This challenging subgroup of patients requires highly accurate diagnostic testing to provide appropriate therapeutic guidance. These data underscore the importance of accurate identification of the pulmonary veins, especially in patients identified as having secundum ASDs and believed to be candidates for minimally invasive surgical or catheter-based closure procedures. We recommend the use of new ultrafast MRA and MRI techniques for patients in whom diagnosis remains inconclusive after cardiac catheterization, TEE or both.

	Acknowledgments

 
The authors thank Norman Butler and Tanya Kurtz for their expert technical assistance, and Janice Dawson, RN, BSN, for coordinating scans, patient recruitment and database management.

	References

Top Abstract Methods Results Discussion Conclusions References

 

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