July 2004, VOLUME 183
NUMBER 1

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July 2004, Volume 183, Number 1

Chest Imaging

HASTE MRI Versus Chest Radiography in the Detection of Pulmonary Nodules: Comparison with MDCT

+ Affiliation:
1All authors: Department of Diagnostic and Interventional Radiology, University Hospital Essen, Hufelandstrasse 55, Essen 45122, Germany.

Citation: American Journal of Roentgenology. 2004;183: 71-78. 10.2214/ajr.183.1.1830071

ABSTRACT
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OBJECTIVE. The purpose of our study was to compare the diagnostic accuracy of an ultrafast ECG-triggered black blood–prepared HASTE sequence with chest radiography for the detection of pulmonary nodules.

SUBJECTS AND METHODS. Sixty-four patients with various primary malignancies who had undergone radiography and MDCT of the chest also underwent ECG-triggered black blood–prepared HASTE MRI of the lung. MR images and radiographs were interpreted separately. The number, location, and size of detected lesions were recorded, and each hemithorax was classified as affected or not affected on the basis of a grade reflecting the conspicuity of nodular involvement. Sensitivity, specificity, and positive and negative predictive values for the detection of pulmonary nodules with diameters of 5 mm or larger were determined, using MDCT findings as the standard of reference. Lesions with diameters smaller than 5 mm were not evaluated. Additional lesion-by-lesion comparisons between MDCT and MRI findings were performed.

RESULTS. MDCT confirmed pulmonary lesions in 32 patients, whereas HASTE MRI revealed lesions in 30 patients and chest radiography, in 19 patients. MDCT revealed 226 nodules in 32 patients, whereas MRI HASTE revealed 227 lesions in 30 patients. Conspicuity scale–based sensitivity and specificity for chest radiography were 55.8% and 92.4%, respectively, whereas HASTE MRI had a sensitivity of 93.0% and a specificity of 96.2%. Positive and negative predictive values for chest radiography were 80% and 79.3%, respectively, and for HASTE MRI, 93.0% and 96.2%, respectively. The sensitivity of HASTE MRI increased with lesion size, ranging from 94.9% for nodules between 5 and 10 mm in diameter to 100% for lesions exceeding 3 cm in diameter.

CONCLUSION. ECG-triggered black blood–prepared HASTE MRI is reliable for detecting pulmonary nodules exceeding 5 mm and has proven significantly more accurate than conventional chest radiography. The technique appears useful as an adjunct to MRI of the heart, great vessels, or chest, potentially increasing the diagnostic yield of MRI examinations.

Introduction
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Substantial improvements in hardware and software have rendered scanning times sufficiently short to allow the breath-hold acquisition of even complex 3D data sets. However, MRI of the lungs has remained clinically irrelevant. Technical challenges include the low proton density and high susceptibility differences between air spaces and the pulmonary interstitium inherent to the lung, as well as the limited spatial resolution of MRI [14].

Despite these difficulties, the potential advantages of pulmonary MRI have been addressed in a number of articles describing preliminary results [510]. The ability to clearly delineate vessels from soft tissue on MRI was shown to be beneficial in the staging of bronchogenic carcinoma in hilar and mediastinal regions [11]. The unsurpassed soft-tissue contrast inherent to MRI has been successfully exploited for ventilation–perfusion imaging [12, 13]. Finally, the lack of ionizing radiation has motivated several investigators to examine the potential usefulness of MRI as a screening technique for detection of pulmonary nodules. Although preliminary results have been encouraging [510], long acquisition times and limited volume coverage have prevented the implementation of these techniques into clinical routine. New ultrafast imaging strategies promise to overcome these limitations.

The purpose of our study was to evaluate the diagnostic accuracy of an ultrafast pulmonary MRI protocol covering the entire chest in less than 40 sec. Using MDCT findings as the standard of reference, we determined sensitivity and specificity for the detection of pulmonary nodules and compared them with the sensitivity and specificity achieved with chest radiography.

Subjects and Methods
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Our study was performed in accordance with regulations of the approving local ethics committee. Sixtyfour consecutive patients (34 men and 30 women; age range, 23–95 years; mean age, 56 years) with various primary malignancies (breast cancer, n = 14; bronchial carcinoma, n = 9; colorectal cancer, n = 11; gastric cancer, n = 2; hypernephroma, n = 1; lymphoma, n = 4; melanoma, n = 6; prostate carcinoma, n = 2; testicular carcinoma, n = 4; thyroid carcinoma, n = 8; and sarcoma, n = 3) were enrolled in our study. All patients were referred to our institution to undergo conventional chest radiography and MDCT of the lungs for evaluation of suspected pulmonary metastases as part of clinically indicated staging protocols. Patients with severe claustrophobia or other contraindications to MRI such as pacemakers or metallic implants were excluded. Before undergoing MRI of the lungs, all patients gave written confirmation of informed consent. The range of the interval between the MDCT and MRI examinations was 0–3 days (mean, 1.6 days). The range of the interval between chest radiography and MDCT was 0–17 days (mean, 6.8 days).

Imaging

Posteroanterior and lateral radiographs were obtained in all patients. All chest radiographs were exposed at 125 kV and printed on 35 × 43 cm film (CR Film 100 NIF, Fuji Film Medical Systems).

MDCT scans were obtained on a 4-MDCT scanner (Volume Zoom, Siemens) with the following parameters: 140 kVp; 100 mAs; slice thickness, 5 mm; collimation, 2.5 mm; feed, 15 mm/sec; rotation speed, 0.5 sec; effective reconstructed slice thickness, 5 mm; scanning time, 12–15 sec; and inplane resolution, 0.5 × 0.5 mm2. We administered 70 mL of a nonionic contrast agent (Ultravist 300 [iopromide], Schering) using an automatic power injector (CT 9000, Liebel-Flarsheim) at a flow rate of 3 mL/sec through a 18- to 20-gauge IV catheter placed in an antecubital vein.

MR images were obtained on a 1.5-T MR scanner (Magnetom Sonata, Siemens) equipped with a high-performance gradient system characterized by an amplitude of 40 mT/m and a slew rate of 200 mT/m per millisecond. A standard phased array torso surface coil was used for signal reception. ECG-triggering with an active fiberoptic ECG system was required for the black blood preparation and for reduction of cardiac motion artifacts. On the basis of a multiplanar scout image, ECG-triggered, breath-hold proton density–weighted black blood–prepared HASTE images were obtained in the axial orientation. The imaging parameters were as follows: TR/TE, 2 R-R intervals/23; flip angle, 160°; effective slice thickness, 5 mm without interslice gaps; matrix size, 158 × 256; and spatial resolution, 2.4 × 1.5 mm2. The phase-encoding direction was anteroposterior. Thirty-six slices covering the entire chest were collected in two interleaved concatenations of 14–19 sec each, depending on the patient's heart rate.

Image Analysis

The standard of reference was defined by two experienced radiologists in consensus on the basis of MDCT scans. All round or ovoid, noncalcified lesions with diameters of 5 mm or larger within the lung parenchyma were counted as pulmonary nodules. The number, location, and size of the detected lesions were recorded. The nodule diameter was defined as the largest diameter on MDCT scans as displayed on a lung window setting (window width, 2,000 H; window level, –500 H). Particular attention was paid to the assignment of nodules into three size categories (5–10 mm, 11–30 mm, and > 30 mm).

All chest radiographs and MR images were interpreted in consensus by two experienced radiologists who were unaware of the results of the MDCT examinations. The radiologists first analyzed chest radiographs and then reviewed MR images 4 weeks later. Hard copies were used for the interpretation of all three types of examinations. The reviewers did not know the type of primary malignancy or the extent of the disease in the patients. To increase the number of observations for the statistical analysis, the reviewers reported the results for the left and the right lungs separately. The two radiologists examined chest radiographs and MR images and used a 4-point conspicuity scale to classify each hemithorax as affected or not affected by pulmonary nodules. The scale ratings were as follows: 1, definitely affected; 2, probably affected; 3, probably not affected; and 4, definitely not affected. Hemithoraces classified as grades 1 and 2 were combined and characterized as affected, whereas hemithoraces classified as grades 3 and 4 were combined and characterized as not affected. The sensitivity and specificity of chest radiography and MRI for nodule detection were determined from conspicuity-scale grades. Receiver operating characteristic (ROC) analyses were performed for chest radiography and MRI by correlating the presence or absence of lung lesions with the degree of observer's diagnostic certainty. Estimates of the area under the ROC curve were made with the method described by Metz et al. [14].

Sensitivity and specificity values for HASTE MRI and chest radiography of the lung were determined using MDCT as the standard of reference. Additionally, lesion-by-lesion comparisons between MDCT and MRI findings were performed. The size and location of lung nodules detected on HASTE MRI were compared with the size and location of lung nodules detected on the MDCT. Sensitivity and specificity values were calculated.

One-to-one comparisons between lesions detected on chest radiography and those detected on MDCT were performed because multiple lesions were visible in only one plane on chest radiographs; thus, many lesions on a chest radiograph could not have been accurately assigned to a potentially corresponding lesion on the MDCT scan.

Results
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Three patients were unable to undergo MRI because of claustrophobia and had to be excluded from the study. Thus, data sets of 61 examinations were analyzed. Both MDCT and MRI examinations were well tolerated; no adverse reactions were observed with either examination. None of the data sets was degraded by respiratory motion artifacts, and no examination had to be repeated because of poor image quality. The mean in-room time required for the MRI examination was 10 ± 4 min, compared with 8 ± 3 min for the MDCT examination. Longer in-room times for MRI examinations were due to the ECG-triggered sequence in our protocol, which required time for electrode placement.

Lesion Detection

On the basis of MDCT findings, metastases were excluded in 29 subjects and confirmed in 32 patients. HASTE MRI revealed pulmonary nodules in 30 of these 32 patients (Fig. 1A, 1B, 1C, 1D). In two patients, MRI failed to show pulmonary nodules detected on MDCT, each of which had a maximum diameter of 8 mm. In one patient, MRI showed a solitary nodule (diameter, 6 mm) that had not been identified on MDCT. Thus, 28 subjects were correctly classified as free of pulmonary metastases when interpretation was based on HASTE MRI findings.

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Fig. 1A. 39-year-old man with melanoma. Posteroanterior chest radiograph depicts both lungs as free of disease.

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Fig. 1B. 39-year-old man with melanoma. Lateral chest radiograph shows no lung nodules.

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Fig. 1C. 39-year-old man with melanoma. HASTE MR image shows pulmonary metastasis (diameter, 6 mm) (arrow) in left lower lung lobe behind heart.

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Fig. 1D. 39-year-old man with melanoma. MDCT scan obtained at same level as C shows same lesion (arrow). Metastasis was confirmed on follow-up MDCT scan obtained 3 months later that revealed increase in size.

Analysis based on chest radiography revealed metastases in 19 of 32 subjects with MDCT-confirmed lesions. Chest radiography failed to show confirmed lesions in 13 patients (Figs. 1A, 1B, 1C, 1D and 2A, 2B, 2C, 2D). The maximum diameter of the lesions missed on chest radiography was 2.4 cm. Findings on chest radiography were correctly judged as not suspicious in 27 patients. In two patients, pulmonary nodules that were suspected on the basis of chest radiography were not visualized on MDCT.

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Fig. 2A. 62-year-old man with renal adenocarcinoma. Posteroanterior chest radiograph shows no lesion in either lung.

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Fig. 2B. 62-year-old man with renal adenocarcinoma. Lateral chest radiograph reveals no lesion.

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Fig. 2C. 62-year-old man with renal adenocarcinoma. Solitary metastasis with a maximum diameter of 1.9 cm (small arrow) is seen close to pericardium on both MDCT scan (C) and HASTE MR image (D). Note residual pneumonia in right lower lobe (large arrow) which is visible on both images. Third density (arrowhead) with diameter smaller than 5 mm can be seen in lingula on MDCT scan and MR image.

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Fig. 2D. 62-year-old man with renal adenocarcinoma. Solitary metastasis with a maximum diameter of 1.9 cm (small arrow) is seen close to pericardium on both MDCT scan (C) and HASTE MR image (D). Note residual pneumonia in right lower lobe (large arrow) which is visible on both images. Third density (arrowhead) with diameter smaller than 5 mm can be seen in lingula on MDCT scan and MR image.

Table 1 summarizes the results of the analysis of 122 hemithoraces assessed in this study. When hemithoraces that were classified as grades 1 and 2 (definitely affected and probably affected) were combined for purposes of analysis, chest radiography revealed 30 affected hemithoraces, whereas MRI revealed 43 hemithoraces as affected (Table 2). The resulting sensitivity of chest radiography for the detection of affected hemithoraces was thus 55.8% and the specificity was 92.4%. The corresponding positive and negative predictive values were 80% and 79.3%, respectively. For MRI, sensitivity and specificity were calculated to be 93.0% and 96.2%, with corresponding positive and negative predictive values of 93.0% and 96.2%, respectively. The overall conspicuity index produced an ROC area of 0.8 for chest radiography, whereas the area under the ROC curve was 0.96 for MRI (Fig. 3).

TABLE 1 Number of Hemithoraces Affected by Pulmonary Nodules as Seen on Chest Radiography and HASTE MRI Based on the Grade Assigned on 4-Point Conspicuity Scale

TABLE 2 Number of Hemithoraces Affected by Pulmonary Nodules as Seen on Chest Radiology and HASTE MRI Compared with MDCT Findings as Reference

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Fig. 3. Graph shows receiver operating characteristic curves for certainty of diagnosis of pulmonary nodules based on chest radiographs (solid line) and HASTE MR images (dotted line).

Lesion-to-Lesion Comparison

Of the 226 nodules detected on MDCT in 32 patients, 179 lesions showed diameters of between 5 and 10 mm, 39 had diameters that ranged between 11 and 30 mm, and eight had diameters that exceeded 30 mm. Of the 227 lesions revealed on HASTE MRI in 30 patients, 178 nodules showed diameters that ranged between 5 and 10 mm, 41 had diameters between 11 and 30 mm, and eight had diameters larger than 30 mm (Fig. 4A, 4B, 4C, 4D).

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Fig. 4A. 63-year-old woman with renal adenocarcinoma. Posteroanterior chest radiograph presents disseminated pulmonary metastases.

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Fig. 4B. 63-year-old woman with renal adenocarcinoma. Lateral chest radiograph also illustrates disseminated pulmonary metastases.

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Fig. 4C. 63-year-old woman with renal adenocarcinoma. MDCT scan obtained at level of left atrium shows multiple scattered lung nodules.

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Fig. 4D. 63-year-old woman with renal adenocarcinoma. HASTE MR image shows good correlation with MDCT scan (C), even in visualization of small pulmonary nodules.

MRI interpretations produced 10 false-negative findings. The diameters of nine of the nodules missed on MRI ranged between 5 and 10 mm (Fig. 5A, 5B, 5C, 5D, 5E), and one lesion measured 13 mm in diameter. Most of the missed lesions were either located close to the pericardium or the pleura (n = 5), obscured by hypostasis in the posterior part of the lungs (n = 2), or misinterpreted as vessels (n = 3).

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Fig. 5A. 57-year-old man with testicular carcinoma. Posteroanterior chest radiograph was interpreted as showing bilateral pulmonary nodules.

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Fig. 5B. 57-year-old man with testicular carcinoma. Lateral chest radiograph also shows disseminated nodules in lungs.

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Fig. 5C. 57-year-old man with testicular carcinoma. Lesion-to-lesion comparison with MDCT scan reveals metastasis (diameter, 5 mm) (arrow) in anterior segment of upper lobe of right lung close to subsegmental vessel.

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Fig. 5D. 57-year-old man with testicular carcinoma. On HASTE MR image obtained at same level as C, lesion is not visible.

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Fig. 5E. 57-year-old man with testicular carcinoma. Haste MR image shows second MDCT-detected lesion (arrow) near left major fissure.

The number of false-positive findings (n =11) on MRI increased as lesion size decreased. Among lesions with diameters of between 5 and 10 mm, eight had false-positive interpretations: Six misinterpretations were caused by nonspecific artifacts, and in two cases, a subpleural scar was suspected to be a metastasis. Among lesions with diameters that ranged between 11 and 30 mm, two false-positive findings occurred: One lesion was found to be a conglomerate of two smaller lesions on MDCT, and the size of the second lesion was overestimated on MRI; MDCT revealed a diameter of less than 11 mm. No false-positive findings were found in the pulmonary lesions larger than 30 mm.

Accordingly, the sensitivity values for HASTE MRI were 94.9% for lesions between 5 and 10 mm, 97.4% for lesions between 11 and 30 mm, and 100% for lesions exceeding 30 mm. The overall sensitivity for the detection of all pulmonary lesions was 95.6% (Table 3). On the basis of these data, a positive predictive value for MRI of 94.9% was calculated.

TABLE 3 Lesion-to-Lesion Comparison of HASTE MRI–Detected Pulmonary Nodules with MDCT-Detected Pulmonary Nodules

Discussion
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ECG-triggered breath-hold HASTE MRI of the lung combined with dedicated surface coils represents a quick and robust method to reliably detect pulmonary nodules exceeding 5 mm in diameter. With MDCT as the standard of reference for the detection of pulmonary nodules, MRI proved significantly more accurate than conventional chest radiography. Both lesion-by-lesion and hemithorax-based analysis showed that MRI reliably revealed noncalcified metastatic nodules with sensitivity and specificity values exceeding 93%. Therefore, HASTE MRI of the lungs should be considered as an addition to all MRI examinations focusing on the heart and great vessels of the chest. Furthermore, in countries in which screening with ionizing radiation is prohibited, this radiation-free technique has potential for tumor staging purposes and for lung screening programs.

Vast improvements in MRI hardware and software have resulted in a considerable increase in the number of MRI examinations of the heart and great vessels [15, 16]. MR angiography represents the technique of choice for the assessment of chronic aortic disease, and cardiac MRI is now routinely used for the assessment of myocardial function and viability in patients with coronary artery disease [17]. The addition of breath-hold black blood–prepared HASTE imaging of the lungs, accomplished in merely two additional breath-holds, could enhance the diagnostic yield of thoracic MRI because risk factors predisposing patients to arterial or cardiac disease are also associated with an increased incidence of bronchogenic carcinoma. Thus, a 5% (65/1,326 patients) incidence of noncalcified pulmonary nodules has been reported when evaluating electron-beam tomographic scans of cardiac patients obtained to quantify coronary artery calcification [18, 19].

The excellent sensitivity and specificity data suggest MRI could also be used for dedicated pulmonary imaging performed for tumor staging. However, the combination of the inability to reliably detect metastases smaller than 5 mm [4, 9] and the inability to properly assess the interstitium and its possible invasion by lymphangitic tumor spread is likely to limit the clinical usefulness of MRI for this indication. In addition, calcified metastases such as those from osteosarcoma may be missed because low proton density causes them to appear dark. Despite these limitations, pulmonary MRI may be used for tumor staging in young patients with potentially curable primary tumors, such as testicular cancer or lymphoma, to reduce the radiation exposure caused by multiple staging and follow-up scans.

The ability to detect most lesions exceeding 5 mm in diameter, the lack of exposure to ionizing radiation, and relatively short data acquisition and in-room times combine to make pulmonary MRI a potentially attractive technique for lung disease screening. Screening for bronchial carcinoma on CT has been suggested to be cost-effective for high-risk patients [2022]. MDCT is accurate but exposes the patient to a considerable amount of ionizing radiation. Although the effective dose can be reduced to approximately 1 mSv using low-dose protocols [23], radiation exposure will always remain a deterrent for screening. This concern is reflected by European Union legislation that explicitly prohibits the use of diagnostic radiographic techniques for the purpose of screening with the exception of mammography [2426].

MRI of the lung is potentially hampered by several factors including low proton density, limited spatial resolution, high susceptibility differences between air spaces and the pulmonary interstitium, and the presence of respiratory and cardiac motion [9, 10, 27]. The technique we have described overcomes most of these limitations. Breath-holding and ECG-triggering eliminate respiration and flow-related artifacts. Beneficial effects on image quality have been documented in a study analyzing single-slice T2-weighted turbo spin-echo and turbo STIR sequences [9]. Advantages inherent to these sequences, including higher spatial resolution and excellent contrast properties, are tempered by long acquisition times. On the other hand, breath-hold and ECG-gated HASTE imaging provides rapid data acquisition with complete coverage of the entire chest in contiguous 5-mm sections collected within two breath-holds, each lasting less than 20 sec.

HASTE images are characterized by high signal intensity in water-rich tissues. Thus, lung parenchymal lesions and vessels appear bright whereas surrounding air-filled lung parenchyma display low signal intensity. The black blood preparation assures flow voids with no apparent signal in pulmonary vessels, thereby facilitating the differentiation of small lung nodules from arteries and veins. In addition, the short echo spacing applied in conjunction with several (180) refocusing pulses minimizes magnetic susceptibility. Hence, excellent lesion contrast is achieved without IV contrast administration.

The technical approach we have outlined is not without its limitations. All imaging was performed on a 1.5-T scanner equipped with the latest hardware and software, resulting in excellent image quality and short scanning times. However, MRI scanners with less powerful gradients or lower field strengths would not necessarily produce a comparable image quality with short scanning times.

Despite combining a torso phased array surface coil with the spine array coil, we achieved an in-plane resolution in this study of 2.4 × 1.5 mm2, which remains poor and could result in a limited sensitivity for lesions with diameters smaller than 5 mm. However, this limitation could be overcome by the implementation of parallel acquisition techniques that could enhance spatial resolution without prolonging the data acquisition time [28].

No attempt was made to distinguish benign from malignant nodules. Calcifications, which are easily depicted on CT, usually denote a benign origin. Calcifications on MRI appear dark and hence cannot be distinguished from the surrounding air-filled structures. For predominantly calcified lesions, which are almost always benign, this difficulty in differentiation causes no problems because these lesions cannot be detected on MRI. However, small calcifications in a soft-tissue nodule that most likely indicate a benign lesion may well be missed on MRI. CT cannot reliably distinguish between benign and malignant noncalcified nodules, but dynamic MRI performed with short TR and TE parameters may provide additional information. Implementation of this procedure seems worthwhile in cases in which pulmonary nodules are found incidentally on HASTE MRI data sets [2931]. Nevertheless, we would recommend a CT scan be obtained in all patients with lung nodules incidentally detected on MRI.

We conclude that ECG-triggered black blood–prepared HASTE MRI is a reliable technique for the detection of pulmonary nodules with diameters of 5 mm or larger and that the technique is significantly more accurate than conventional chest radiography. The technique appears useful as an adjunct to MRI of the heart or great vessels because it may increase the diagnostic yield of these examinations. In addition, ECG-triggered black blood– prepared HASTE MRI may be used for screening purposes.

Address correspondence to J. Barkhausen.

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