Resonance Imaging in the Evaluation
of Lung Cancer
By Warren B. Gefter
HILE THE technology of magnetic resonance imaging (MRI) continues to be refined at a rather rapid rate, sufficient knowledge has accumulated to define the current role of MRI for the evaluation of lung cancer.L-S This report will review the value and limitations of MRI for the diagnosis, staging, and posttreatment evaluation of carcinoma of the lung. An understanding of these strengths and limitations on the part of both the radiologists and referring physicians will contribute to a more efficacious use of this sophisticated modality. GENERAL
For several reasons, MRI has not replaced computed tomography (CT) in the general evaluation of patients who have lung cancer. First, the relatively low signal in the lungs limits the detection of pulmonary nodules and other lung parenchymal disease. Second, noise due to motion has been a frequent and significant problem in thoracic MRI. Sources of such motion include respiration, cardiac movement, vascular pulsations, blood flow, and bulk patient movement. A number of techniques have been developed to reduce these causes of motion, which include respiratory-ordered phase-encoding software, cardiac gating, flow compensation methods (eg, gradient-moment nulling), and methods to eliminate undesirable flow-related vascular signal (eg, spatial presaturation).6 Third, the spatial resolution of MRI has been inferior to that of CT. However, methods permitting higher resolution MRI with smaller fields-of-view (eg, surface coils and elimination of aliasing artifacts) have been developed recently. Fourth, difficulty in detecting calcification represents an intrinsic limitation of MRI for evaluating lung nodules and mediastinal adenopathy when assessing lung cancer. Finally, the higher cost, limited availability, and longer examination time of MRI compared with CT has restricted the use of thoracic MRI. Despite the above limitations, the appropriate use of MRI may provide clinically important information for the evaluation of patients who have lung cancer. The advantages of MRI can be understood by considering in general the strengths of MRI for chest imaging. These advantages Seminars
No 1 (January),
include superb vascular imaging capability (without the need for exogenous contrast agents), exquisite soft-tissue contrast, the ability to image the chest directly in multiple planes, and the potential to characterize certain tissues by their magnetic relaxation properties (eg, Tl and T2 values). These features of MRI allow for the excellent depiction of the heart and great vessels, chest wall, spinal contents, vertebral bone marrow, and brachial plexus. The ability to obtain direct sagittal and coronal sections can be useful for imaging the lung apices, diaphragmatic regions, and for clarifying craniocaudal relationships in the mediastinum. T2-weighted images may permit the differentiation of tumor and scar tissue. Specific applications of these strengths of MRI to patients who have lung cancer are discussed in the following text. It has become evident that MRI is best used as a problemsolving modality in order to clarify specific features in cases of bronchogenic carcinoma.4 TECHNICAL
The specific protocols used in MRI of the chest will necessarily vary with the particular scanner used and the available software. In general, following a coronal localizer scan, axial images using a short repetition time (TR) and short echo time (TE) (Tl-weighted) are obtained. Electrocardiographic (ECG) gating and respiratory compensation (respiratory-ordered phase-encoding) software are generally used for motion suppression. It is also useful to suppress undesirable flow-related signal in vessels by using spatial presaturation, a technique that saturates the spins of incoming blood before their entrance into the imaging volume (Fig I). The Tl-weighted scan optimizes the contrast between high-signal fat, low-signal vessels, and intermediate-signal mediastinal masses and lymph nodes. From the Department of Radiology, Hospital of the University of Pennsylvania, Philadephia. PA. Address reprint requests to Warren B. Gefter, MD. Professor of Radiology, Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce St. Philadelphia. PA 19104. o 1990 by W.B. Saunders Company. 0037-I 98X/90/2501 -0009$5.OOjO 73
Fig 1. Motion-free, highresolution image of the mediastinum acquired using combined respiratory compensation software to eliminate respiratory ghost artifacts, spatial presaturation to suppress intravaroular flow-related signal, ECG geting. and reduced field-ofview. Note excellent definition of vascular structures, trachea (T) and esophagus (~1.
The axial scan is usually repeated with a dual-echo sequence using a long TR together with both a short TE (proton density-weighted) and a long TE (T2-weighted). The maximized signal of the proton density sequence optimizes detection of lung nodules and parenchymal processes. The T2-weighted images allow further characterization of abnormal masses and enhance the detection of pleural effusions. The addition of flow compensation techniques such as gradient-moment nulling can significantly improve image quality on the T2-weighted scans. Supplementary coronal, sagittal, and/or oblique scans can be obtained as necessary to clarify anatomic relationships. Apical lesions (see section on Lung Cancer Staging) are best studied using a surface coil and small fields-ofview in the sagittal and coronal planes. Evaluation of vessel patency and thrombus is facilitated by using flow-sensitive gradient-recalled echo pulse sequences, which are sufficiently rapid to be acquired during breath-holding. Flowing blood is characterized by high signal on these “fast scans.” If used as a primary modality to evaluate bronchogenic carcinoma, the MRI scans, like those of CT, should extend through the level of the adrenal glands. LUNG CANCER DIAGNOSIS
The role of MRI in the initial diagnosis of bronchogenic carcinoma is limited. While thin-
section CT has proven to be useful in the evaluation of lung nodules to help differentiate benign from malignant lesions based on calcium content,7*8 to date MRI has not provided any specific information to aid in this distinction. As indicated above, the identification of calcification is problematic with MRI. Moreover, there is considerable overlap in the Tl and T2 values of malignant and inflammatory lesions, which applies to both lung masses and mediastinal lymph nodes.‘,” The higher spatial resolution of CT also allows better visualization of the morphology of a nodule, its relationship to pulmonary fissures and bronchi, as well as the presence of any additional lung nodules.” However, MRI can be of value when the distinction between a lung nodule and a pulmonary vessel is uncertain by CT. Two uncommon situations in which MRI also may provide useful information with regard to the characterization of lung nodules are the identification of arteriovenous malformations (AVMs)’ and lung hematomas.4 AVMs can be readily diagnosed by the identification of blood flow within these vascular lesions. It is possible to identify a pulmonary hemtioma by the characteristic MRI appearances of various stages of hemorrhage, including deoxyhemoglobin, methemoglobin, or hemosiderin (Fig 2).12 MRI can be advantageous in differentiating a hilar mass or adenopathy from an enlarged pulmonary artery in patients presenting with a
structures, trachea, or esophagus constitute unresectable cancers (stage IIIB). For this reason, it has become important that CT and MRI studies be able to discriminate between these features of stage IIIA and IIIB disease.15 Likewise, identification of the extent of chest wall invasion can provide useful preoperative information to both the surgeon and the patient in anticipating the degree of chest wall resection required. Mediastinal Lymphadenopathy
Fig 2. Hematoma secondary to ruptured aortic aneurysm. This patient was referred for a large chest mass initially felt to represent a carcinoma. Coronal Tl-weighted MRI shows high signal in periphery of mass consistent with methemoglobin in a subacute hematoma (14. Aneurysm with clot (arrow) is demonstrated in the adjacent distal aortic arch and was confirmed by thoracic eortogram. These studies established the diagnosis of a ruptured aortic
prominent hilum on chest radiographsI While such patients are frequently first examined by CT in this situation, MRI can provide useful information when the CT study is inconclusive, as may be the case when intravenous contrast enhancement is suboptimal or contraindicated. Likewise, MRI can be extremely useful as either a primary or problem-solving modality to differentiate a vascular from a nonvascular mass in the mediastinum. LUNG CANCER STAGING
The roles of both CT and MRI have been influenced by recent changes in the staging system for lung cancer.‘4*‘7 This revised staging system reflects a more aggressive surgical approach to treating these tumors. In particular, the presence of limited ipsilateral mediastinal lymphadenopathy, focal mediastinal invasion sparing the heart, great vessels, trachea, and esophagus, and limited chest wall involvement are now regarded as resectable lesions (stage IIIA). In contrast, contralateral mediastinal lymphadenopathy, significant invasion of mediastinal fat, or invasion of major cardiovascular
Unfortunately, with regard to the identification of metastatic mediastinal lymph nodes, MRI is not capable of differentiating hyperplastic from tumor-bearing lymph nodes based on imaging parameters. In fact, in vitro measurements of excised mediastinal lymph nodes have confirmed an overlap in the Tl and T2 values of benign and malignant nodes.‘Therefore, MRI currently must rely on size criteria alone, similar to CT. Studies to date have shown no significant overall differences in the accuracy of MR versus CT in staging mediastinal lymph nodes in lung cancer, with a wide range of reported sensitivity and specificity. 13~18-24 Both modalities serve to guide procedures for preoperative biopsy of any enlarged nodes, and to obviate preoperative mediastinal staging procedures in the absence of nodal enlargement. While MRI may fail to detect calcification in benign nodes readily apparent by CT, MRI can more easily distinguish lymph nodes from vascular structures. MRl is particularly useful when CT is inconclusive with regard to the presence of lymph nodes that may require preoperative biopsy, especially contralateral nodes that may determine resectability. The coronal plane of imaging afforded by MRI may be especially useful as a problem-solving technique in evaluating the aortopulmonary window, and lower left paratracheal and subcarinal regions for lymphadenopathy when transaxial CT slices are not deIinitive.24-26 Hilar Lymphadenopathy
While hilar lymphadenopathy does not preclude resectability, determination of the extent of hilar involvement influences the tumor stage and the appropriate surgical management.15231s Extensive hilar disease usually necessitates pneumonectomy, while more limited disease may be treated with lobectomy and node dissection. MRI, which
is at least as accurate as contrast-enhanced CT in hilar lymph node detection, can be particularly useful when the CT findings are equivocal, as indicated previously. However, while both contrast-enhanced CT and MR are highly sensitive in the detection of hilar lymphadenopathy, specificity for tumor is disappointingly low for each modality (66% and 50%, respectively).4*‘3V’s719V 20,24,25,27-29
With regard to direct mediastinal extension of adjacent lung tumors, neither CT nor MRI is accurate in distinguishing contiguity from limited invasion of the mediastinal pleura or fat.‘9’3’ 18-21However, both modalities can be used to identify more extensive invasion. MRI has proven to be advantageous over CT in the identification of vascular involvement by tumor either by encasement, invasion, or intraluminal tumor thrombus, findings that indicate unresectable disease. Superior vena caval involvement is not uncommon, and MRI (including the flowsensitive gradient echo images) offers advantages over CT in determining the presence and extent of superior vena caval obstruction (Fig 3).30*3’ Invasion of the pericardium or of the heart itself is best demonstrated by MRI.32*33 The normal pericardium appears as a low-signal rim. Disruption of this demarcation between tumor and heart is indicative of pericardial invasion (Fig
Fig image shows pletely fied by
3. Superior vena caval obstruction. Tl-weighted in a patient with superior vena caval syndrome tumor (arrow) invading the mediastinum and comobliterating the superior vena cave, normally identiits flow void.
4A). Central bronchogenic carcinomas also at times invade the pulmonary veins and extend into the left atrium (Fig 4B). Bronchial
While the diagnosis of endobronchial tumor ultimately rests with bronchoscopy, CT has been useful in the identification of bronchial involvement by tumor. On the other hand, MRI has been less effective for detection of endobronchial lesions due to poorer signal-to-noise and spatial resolution, especially as compared with thinsection CT.2*‘3 However, oblique coronal MRI scans have been useful in showing the relationship of tumor to the tracheal carina and proximal bronchi. This ability is relevant to the revised staging system. Tumor within 2 cm of the carina, formerly regarded as unresectable, may now be operable using tracheobronchial (sleeve) resection. However, tumors invading the carina or extending across the midline are generally regarded as unresectable.‘59’7 Chest Wall and Pleural Invasion
CT is limited in its ability to accurately assess limited chest wall and pleural invasion by peripheral lung carcinoma in the absence of rib destruction.34s37 Such chest wall invasion may be better demonstrated by MRI due to the very high soft-tissue contrast between tumor and muscle, most evident on the T2-weighted images (Fig This degree of contrast exceeds that 5). 1,4V2’,3g*39 of CT. Transgression of the pleura can also be identified on MRI by disruption of normal extrapleural fat seen on Tl-weighted scans.2*40,41 Moreover, the use of local receiver coils in combination with appropriate imaging planes can yield highresolution images of selected regions of the chest wall. As described further below, such images in the coronal and sagittal planes provide a clearer display of chest wall extension at the lung apices than is possible using transverse CT slices.25942 However, it may not be possible to separate chest wall tumor from associated inflammatory changes or edema on conventional spin echo MRI. The use of paramagnetic contrast agents may prove to be helpful in this regard, although this has not been fully investigated. Rib involvement, which is best identified on rib radiographs, CT, or bone scans, is more difficult to detect by MRI. Small pleural effusions may be more difficult to detect by MRI than CT if T2-weighted images are not
Fig 4. (A) Mediaetinal invasion. This squamous cell as the low-signal pericardium (arrow) on this Tl-weighted intravascular involvement by this central bronchogenic (open arrow) into the left atrium (closed arrow).
carcinoma coronal carcinoma.
obtained. While investigative studies suggest that MRI may have a limited role in characterizing pleural effusions, 43this has not replaced the need for cytological examination of pleural fluid to
Fig 5. Chest wall invasion. This patient, status post right pneumonectomy, was evaluated for chest pain. T2weighted image ITR 2,600 ms, TE 80 ms shows marked contrast between the high signal recurrent tumor (1) and the adjacent low-signal posterior chest wall muscles. Tumor can be seen to extend into the chest wall (arrows) fmetastatic tumor is also present in the mediastinumj.
of the left lung invades the adjacent image. (6) More posterior coronal The tumor extends via the left
mediastinal fat, as well scan depicts mediastinal superior pulmonary vein
confirm a malignant effusion and hence nonresectability. Superior Sulcus Tumors
Superior sulcus (Pancoast) tumors are distinguished from other peripheral carcinomas by their propensity for early chest wall extension at the lung apex. In particular, they often involve the brachial plexus, subclavian vessels, and spine. Survival has been significantly increased by treatment with either radiation alone or combined preoperative radiotherapy followed by lobectomy and radical en bloc chest wall resection. Accurate assessment of the extent of tumor allows proper radiotherapy planning and permits the selection of appropriate surgical candidates.4os44 Contraindications to surgery include extensive involvement of the subclavian artery, brachial plexus, or vertebral body, as well as mediastinal invasion and metastases to mediastinal lymph nodes or distant sites. MRI is the optimal modality for evaluating local extension of superior sulcus tumors.40~4*~45~48 Direct coronal and sagittal scans can accurately depict the superior extent of these tumors (Fig 6). Disruption of the normal rim of extranleural
fat between the subclavian vessels and apical pleura is indicative of tumor transgression through the lung apex. The brachial plexus, subclavian vessels, vertebral bone marrow, and intraspinal contents all can be clearly imaged. Sagittal views provide the best demonstration of the relationship of tumor to the middle and distal portions of the brachial plexus (Fig 6). Visualization of the brachial plexus and adjacent anatomy can be further enhanced with the use of local (surface) receiver coils combined with small fields-of-view (Fig 7). While Tl-weighted images best depict the relevant anatomy, T2-weighted images may show tumor invasion into muscles of the chest wall or base of the neck. The latter may preclude surgical resection.
MRI is more sensitive than CT in evaluating tumor invasion through the superior SU~CUS.~~ CT is hampered by limitation to the transverse plane, the presence of beam hardening artifacts from the shoulders, and poorer soft-tissue contrast. A tailored MRI evaluation of local tumor extent can supplement a complete conventional CT study of the chest in these cases.46*47Recently, it was also suggested that MRI of superior sulcus tumors before and after preoperative radiation therapy may provide useful prognostic information; the detection of tumor necrosis, as well as shrinkage of the lesion, implies an improved long-term survival and would favor resection in otherwise borderline surgical candidates.@ This application of MRI requires further study.
Fig 6. (Al Superior sulcus tumor. Superior extent of this left apical carcinoma (T) is diicuit to assess in the axial plane. (B) Sag&al scan (TR 2.600 ms. TE 26 me) demonstrates that the tumor extends to the apex of the lung, but does not involve the brachiil plexus (straight arrow) or subclavian artery (curved arrow). (Cl Increased tumor/ muscle contrast on this TEwaighted (TR 2,600 ms, TE 80 ms) image shows that the tumor (~1 does not grossly involve the apical chest wall musculature (ml. (Courtesy of Allan M. Haggar. MD, Henry Ford Hospital, Detroit, MI).
Normal brachial plexus. Fig 7. and relatively small fields-of-view images of branches of the brachial the lung apex. [Subclavian artery, vein, open arrow).
The use of surface coils can yield high resolution plexus (black arrow) at white arrow: subclavian
Tumor Versus Obstructive Atelectasis Another application of MRI in lung cancer staging, albeit of limited utility, is the potential differentiation of central tumors from associated obstructive atelectasis of the 1ung.2~s~‘3~49~50 This distinction can be made by CT when a dynamic bolus technique is used. On MRI, cholesterol pneumonitis in the obstructed lung, which has a high water content and long T2, may have a higher signal intensity than the adjacent central tumor on T2-weighted images (Fig 8). While this distinction may not influence decisions regarding resectability, it may be useful in radiation therapy planning to spare those portions of lung involved by obstructive atelactasis. Several studies have shown that this differentiation is possible using MRI in approximately 40% of cases.13,19,49 However, central tumor and distal atelectatic lung may be isointense when the latter is involved by organizing fibrous pneumonitis.” Distant Metastases MRI may provide useful information in the characterization of adrenal masses during the evaluation of distant metastases. Clinically oc-
cult adrenal lesions are not infrequently uncovered on CT studies performed for lung cancer staging (21%).” More than two thirds of these lesions prove to represent incidental benign adrenal adenomas.52 CT can differentiate such adenomas from malignant lesions in approximately 60% of cases.53TZweighted MRI also can potentially make this distinction, the adenoma having an intensity similar to liver compared with the higher signal of the metastases relative to liver (at 0.35T and 0.5T).‘4-‘8 Unfortunately, these signal intensity ratios are unable to differentiate benign from malignant adrenal masses in as many as 30% of cases. Data suggest that at 1ST the calculated T2 values of adrenal masses are more accurate than the signal intensity ratios.59 Recently, gadolinium-DTPA-enhanced dynamic MRI with fast gradient-echo images has shown promise in the differentiation of benign cortical adenomas from malignant adrenal lesions, with a reported accuracy of 9 1%.6o Definitive diagnosis of adrenal masses in patients with bronchogenic carcinoma can be obtained by percutaneous thinneedle aspiration biopsy, which should be considered when a tissue diagnosis is critical to patient management. MRI also may be used in the detection of distant metastases to brain, liver, and bone. The yield of preoperative screening for brain metastases in the asymptomatic patient remains controversial. Recent studies have demonstrated an increased sensitivity in the detection of intracerebral metastases using contrast (gadoliniumDTPA)-enhanced MRI compared with contrastenhanced CT.6’-63 Liver imaging may be required when hepatic metastases is suspected based on clinical or biochemical findings. MRI may be used as a primary modality in such cases, or as a secondary imaging procedure when the CT findings are equivocal or negative with a high index of suspicion. The sensitivity of MRI in the detection of hepatic metastases are superior to conventional dynamic contrast-enhanced CT, ;:lthough less than that of CT during arterial portography.64V65 MRI also may be useful in differentiating an hepatic metastasis from the commonly encountered benign hemangioma. With regard to screening for bone metastases, radionuclide scans may be obtained when there are suggestive symptoms. MRI may be used in the evaluation of abnormalities detected on such
Fig 8. (A) Central tumor differentiated from obstructive ate&task. Coronal Tl-weighted scan shows contrast between lower-intensity large central bronchogenic carcinoma fc) and higher-aignal peripheral obstructed lung (01. The latter may have been secondary to hemorrhagic or proteinaceous fluid. There was complete opacification of the left hemithorax on the chest radiograph. (8) T2-weighted axial image demonstrates increased signal in the obrnructed lung (01 relative to the tumor (Tl. The left pulmonary artery appeared involved by tumor (arrow). (Cl High-signal blood flow in this gradient-ache image confirms tumor invasion of left pulmonary artery (arrow). (M. L, R, main, left, and right pulmonary arteries, respectively). Tumor proved unresectable at thoracotomy.
bone scans when correlative plain radiographs are negative, as well as in highly symptomatic patients with negative or equivocal scans and radiographs. Post-treatment
Local recurrence of tumor in patients who have undergone surgical resection for bronchogenic carcinoma can usually be suggested by chest radiographs or CT scans. However, in patients who have been irradiated, the early detection of tumor recurrence may be more difficult if extensive radiation changes are present. MRI may offer a unique advantage in such cases. Initial studies have indicated that residual or recurrent tumor may be distinguished from mature fibrosis by their differing appearances on
TZweighted sequences.66-70Well-established fibrosis has a short T2, appearing dark on T2weighted scans, whereas tumor shows significantly higher signal intensity (relative to muscle) (Fig 9). One may elect to follow patients with low-signal radiation changes, recognizing that MRI cannot be used to exclude residual microscopic tumor. Areas of increased signal, on the other hand, may prompt biopsy for confirmation of tumor. Since there may be coexisting regions of fibrosis and tumor, MRI might serve to delineate the most efficacious sites for biopsy. However, it should be emphasized that the relatively high signal intensity of tumor on T2weighted scans may not be distinguishable from that of active radiation reaction, immature fibrotic or inflammatory tissue without biopsy or
hilum or mediastinum secondary to prior surgery (Fig lo), or when there are abundant streak artifacts from surgical clips. The improved contrast resolution and vascular display on MRI and the absence of any significant artifact from clips may facilitate evaluation of such cases. Finally, MRI can be useful in assessing the development of distant metastases, particularly to brain, adrenals, liver, and bone. The indications for MRI in evaluating these sites have been discussed (see section on Distant Metastases). SUMMARY
Fig 9. (A) Recurrent tumor following radiation for small-call carcinoma. CT scsn, unanhancad due to renal failure. demonstrates increased soft tissue (MI in the madiastinum and consolidation in the left lower lobe (~1. Distinction between recurrent tumor and radiation fibrosis was unclear. (Bl TZ-weighted (TR 2.9tXl ms. TE 80 ms) MRI scan shows regional high signal in the madiastinum (arrows), suggesting tumor, in contrast to low-signal in the left lower lobe (L) consistent with fibrosis. The findings were confirmed by biopsy.
serial examinations. The specificity of the MRI findings in this differentiation and the temporal pattern of signal changes during the evolution of radiation fibrosis have not yet been completely studied in the chest. Identification of tumor recurrence by CT also may be difficult when there is significant distortion of normal anatomic relationships in the
MRI is used most efficaciously in the evaluation of patients with bronchogenic carcinoma when employed as a tailored examination designed to answer specific questions relevant to patient management. CT continues to be used more generally in staging lung cancer when imaging beyond conventional chest radiography is required. Specific areas in which MRI can provide important and unique information (which may supplement a CT study) include the following: (1) evaluation of the local extent of superior sulcus tumors, and (2) distinction between stage IIIA (resectable) and stage IIIB (unresectable) tumors. Confirmation of tumor invasion of major mediastinal structures is necessaary before depriving a patient of potential curative resection. MRI may contribute important information when CT findings are indefinite, particularly with regard to invasion of major cardiovascular structures (eg, superior vena cava, pulmonary artery, pericardium, and heart); invasion of the tracheal carina or bilateral involvement of main bronchi; and the presence of contralateral mediastinal or hilar lymphadenopathy. MRI should be considered as a primary imaging modality to evaluate central tumors in patients for whom intravenous contrast agents are contraindicated, and as a problem-solving modality when CT is inconclusive in the detection of a possible hilar or mediastinal mass. Other specific applications of MRI include the identification of tumor recurrence in the presence of radiation fibrosis, assessment of the extent of chest wall invasion of peripheral lung tumors,
Fig 10. Tumor recurrence following surgery. This patient (also shown in Fig Sl underwent prior right pneumonectomy followed by a Cbgett procedure lmuscle flap) to repair a postoperative bronchial stump leak. TZ-weighted (TR 2.500 ms, TE 80 ms scan proved useful in diirentiating low-signal normal musole fiap (ml from multiple sites of high-signel tumor (t), identified in the posterior aspect of the flap as wall as in the mediistinum and posterior chest.
and the noninvasive characterization of adrenal masses. The scope of these MRI applications in patients with lung cancer may expand in the future with refinements in motion suppression
techniques, implementation of ultrafast MRI (using variations of the echoplanar method), and further development of MRI spectroscopy and MRI contrast agents.
REFERENCES 1. Webb WR: MR imaging in the evaluation and staging of lung cancer. Semin US CT MR 9:53-66, 1988 2. Webb WR: The role of magnetic resonance imaging in the assessment of patients with lung cancer: A comparison with computed tomography. J Thorac Imag 4:65-75,1989 3. Spritzer C, Gamsu G, Sostman HD: Magnetic resonance imaging of the thorax: Techniques, current applications, and future directions. J Thorac Imag 4: I- 18, 1989 4. Swensen SJ, Ehman RL, Brown LR: Magnetic resonance imaging of the thorax. J Thorac Imag 4:19-33,1989 5. Gefter WB: Chest applications of magnetic resonance imaging: An update. Radio1 Clin North Am 26:573-588, 1988 6. Wehrli FW: Advanced MR Imaging Techniques. GE, Medical Systems, Milwaukee, WI, 1987 7. Siegelman SS, Khouri MF, Leo FP, et al: Solitary pulmonary nodule: CT assessment. Radiology 160:307-312, 1986 8. Zerhouni EA, Stitik FP, Siegelman SS, et al: CT of the pulmonary nodule: A comparative study. Radiology 160:3 19327,1986 9. Glazer G, Orringer MB, Chenevert TL, et al: Mediastinal lymph nodes: Relaxation time/pathologic correlation and implications in staging of lung cancer with MR imaging. Radiology 168:429-431,1988 10. Dooms GC, Hricak H, Moseley ME, et al: Characterization of lymphadenopathy by magnetic resonance relaxation times: Preliminary results. Radiology 155:429-432, 1985
11. Muller NL, Gamsu G, Webb WR: Pulmonary nodules: Detection using magnetic resonance and computed tomography. Radiology 155:687-690,1985 12. Rubin JI, Gomori JM, Grossman RI, et al: High field MR imaging of extracranial hematomas. AJR 148:813-817, 1987 13. Webb WR, Jensen BG, Sollitto R, et al: Bronchogenic carcinoma: Staging with MR compared with staging with CT and surgery. Radiology 156:117-124, 1985 14. Mountain CF: A new international staging system for lung cancer. Chest 89:2255-2335, 1986 (suppl) 15. Gamsu G: The new staging of lung cancer: Implications for CT and MRI. San Diego, CA, Thoracic Imaging 1989, Society for Thoracic Radiology, Annual Postgraduate Course Syllabus, 1989, pp 65-68 16, Friedman PJ: Lung cancer: Update on staging classifications. AJR 150:261-264, 1988 17. Mann H, Karwande SV: The new proposed international staging system for lung cancer. Semin US CT MR 9:34-39, 1988 18. Martini N, Heelan R, Westcott J, et al: Comparative merits of conventional, computed tomographic, and magnetic resonance imaging in assessing mediastinal involvement in surgically confirmed lung carcinoma. J Thorac Cardiovasc Surg 90:639-648,1985 19. Levitt RG, Glazer HS, Roper CL, et al: Magnetic resonance imaging of mediastinal and hilar masses:Comparison with CT. AJR 145:9-14, 1985
20. Heelan RT, Martini N, Westcott JW, et al: Carcinomatous involvement of the hilum and mediastinum: Computed tomographic and magnetic resonance evaluation. Radiology 157:111-115, 1985 21. Musset 0, Grenier P, Carette MF, et al: Primary lung cancer staging: Prospective comparative study of MR imaging with CT. Radiology 160:607-611, 1986 22. Poon PY, Bronskill MJ, Henkelman RM, et al: Mediastinal lymph node metastases from bronchogenic carcinoma: Detection with MR imaging and CT. Radiology 162:651656, 1987 23. Patterson GA, Ginsberg RJ, Poon PY, et al: A prospective evaluation of magnetic resonance imaging, computed tomography, and mediastinoscopy in the preoperative assessment of mediastinal node status in bronchogenic carcinoma. J Thorac Cardiovasc Surg 94:679-684,1987 24. Webb WR: Magnetic resonance imaging of the hila and mediastinum. Cardiovasc Intervent Radio1 8:306-313, 1986 25. Webb WR, Jensen BG, Gamsu G, et al: Coronal magnetic resonance imaging of the chest: Normal and abnormal. Radiology 153:729-735, 1984 26. Webb WR, Moore EH: Differentiation of volume averaging and mass on magnetic resonance images of the mediastinum. Radiology 155:413-416, 1985 27. Webb WR, Gamsu G, Stark DD, et al: Magnetic resonance imaging of the normal and abnormal pulmonary hila. Radiology 152:89-94, 1984 28. Glazer GM, Gross BH, Aisen AM, et al: Imaging of the pulmonary hilum: A prospective comparative study in patients with lung cancer. AJR 145:245-248, 1985 29. Quint LE, Glazer GM, Orringer MB: Central lung masses: Prediction with CT of need for pneumonectomy versus lobectomy. Radiology 165:735-738, 1987 30. McMurdo KK, de Geer G, Webb WR, et al: Normal and occluded mediastinal veins: MR imaging. Radiology 159:33-38,1986 3 1. Weinreb JC, Mootz A, Cohen JM: MRI evaluation of mediastinal and thoracic inlet venous obstruction. AJR 146:679-684, 1986 32. Barakos JA, Brown JJ, Higgins CB: MR imaging of secondary cardiac and paracardiac lesions. AJR 153:47-50, 1989 33. Amparo EG, Higgins CB, Farmer D, et al: Gated MRI of cardiac and paracardiac masses: Initial experience. AJR 143:1151-1156,1984 34. Glazer HS, Duncan-Meyer J, Aronberg DJ, et al: Pleural and chest wall invasion by bronchogenic carcinoma: CT evaluation. Radiology 157:191-194, 1985 35. Shin MS, Anderson SD, Myers J, et al: Pitfalls in CT evaluation of chest wall invasion by lung cancer. J Comput Assist Tomogr 10:136-138, 1986 36. Pennes DR, Glazer GM, Wimbish KJ, et al: Chest wall invasion by lung cancer: Limitations of CT evaluation. AJR 144:507-511, 1985 37. Pearlberg JL, Sandler MA, Beute GH, et al: Limitations of CT in evaluation of neoplasms involving chest wall. J Comput Assist Tomogr 11:290-293, 1987
83 38. Haggar AM, Pearlberg JL, Froelich JW, et al: Chest wall invasion by carcinoma of the lung: Detection by MR imaging. AJR 148:1075-1078, 1987 39. Berquist TH, Brown LR, May GR, et al: Magnetic resonance imaging of the chest: A diagnostic comparison with computed tomography and hilar tomography. Magn Reson Imag 2:3 15-327, 1984 40. Takasugi J, Rapoport S, Shaw C: Superior sulcus tumors: The role of imaging. J Thorac Imag 4:41-48, 1989 41. Castagno AA, Shuman WP: MR imaging in clinically suspected brachial plexus tumor. AJR 149:1219-1222, 1987 42. Webb WR, Jensen BG, Gamsu G, et al: Sagittal MR imaging of the chest: Normal and abnormal. J Comput Assist Tomogr 9:471-479,1985 43. Vock P, Hedlund LW, He&ens RT, et al: Work in progress: In vitro analysis of pleural fluid analogs by proton magnetic resonance: Preliminary studies at 1.5T. Invest Radio1 22:382-387, 1987 44. Paulson DL: Management of superior sulcus carcinomas, in Choi NC, Grill0 HC (eds): Thoracic Oncology. New York, NY, Raven, 1983, pp 147-162 45. Rapoport S, Blair DN, McCarthy SM: Brachial plexus: Correlation of MR imaging with CT and pathologic findings. Radiology 167:161-165, 1988 46. Heelan RT, Demas BE, Caravelli J, et al: Superior sulcus tumors: CT and MR imaging. Radiology 170:637-641, 1989 47. McLoud TC, Filion RB, Edelman RR, et al: MR imaging of superior sulcus carcinoma. J Comput Assist Tomogr 13:233-239,1989 48. Blair DN, Rapoport S, Sostman HD, et al: Normal brachial plexus: MR imaging. Radiology 165:763-767, 1987 49. Tobler J, Levitt RC, Glazer HS, et al: Differentiation of proximal bronchogenic carcinoma from post-obstructive lobar collapse by magnetic resonance imaging: Comparison with computed tomography. Invest Radio1 22:538-543, 1987 50. Shioya S, Haida M, Ono Y, et al: Lung cancer: Differentiation of tumor, necrosis, and atelectasis by means of Tl and T2 values measured in vitro. Radiology 167:105109.1988 51. Nielson ME Jr, Heaston DK, Dunnick NR, et al: Preoperative CT evaluation of adrenal glands in non-small cell bronchogenic carcinoma. AJR 139:3 17-320, 1982 52. Oliver TW, Bernardino ME, Miller JI, et al: Isolated adrenal masses in non small-cell bronchogenic carcinoma. Radiology 153:217-218, 1984 53. Berland LL, Koslin DB, Kenney PJ, et al: Differentiation between small benign and malignant adrenal masses with dynamic incremented CT. AJR 151:95-101, 1988 54. Reinig JW, Doppman JL, Dwyer AJ, et al: Adrenal massesdifferentiated by MR. Radiology 158:81-84, 1986 55. Glazer GM, Woolsey EJ, Borrello J, et al: Adrenal tissue characterization using MR imaging. Radiology 158:7379.1986 56. Falke THM, Bloem JL, te Strake L, et al: Magnetic resonance imaging of the adrenal glands. Radiographics 7:343-370, 1987 57. Chang A, Glazer HS, Lee JKT, et al: Adrenal gland: MR imaging. Radiology 163:123-128, 1987
58. Chezman JL, Robbins SM. Nelson RC, et al: Adrenal masses: Characterization with Tl-weighted MR imaging. Radiology 166:357-359, 1988 59. Kier R, McCarthy S: MR characterization of adrenal masses: Field strengths and pulse sequence considerations. Radiology 171:671-674,1989 60. Krestin GP, Steinbrich W, Friedman G: Adrenal masses: Evaluation with fast gradient-echo MR imaging and gadolinium-DTPA enhanced dynamic studies. Radiology 171:675-680, 1989 6 1. Russell EJ, Geremia GK, Johnson CE, et al: Multiple cerebral metastases: Detectability with Gd-DTPA-enhanced magnetic resonance imaging. Radiology 165:609-617, 1987 62. Sze G, Shin J, Krol G, et al: Intraparenchymal brain metastases: MR imaging versus contrast-enhanced CT. Radiology 168:187-194, 1988 63. Healy ME, Hesselink JR, Press GA, et al: Increased detection of intracranial metastases with intravenous GdDTPA. Radiology 165:619-624,1987 64. Nelson RC, Chezman JL, Sugarbaker PH, et al: Hepatic tumors: Comparison of CT during arterial portogra-
phy, delayed CT, and MR imaging for preoperative evaluation. Radiology 172:27-34, 1989 65. Heiken JP, Weyman PJ, Lee JKT, et al: Detection of focal hepatic masses: prospective evaluation with CT, delayed CT, CT during arterial portography, and MR imaging. Radiology 171:47-51, 1989 66. Glazer HS, Lee JKT, Levitt RA, et al: Radiation fibrosis: Differentiation from recurrent tumor by MR imaging. Work in progress. Radiology 156:721-726, 1985 67. Ebner F, Kressel HY, Mintz MC, et al: Tumor recurrence versus fibrosis in the female pelvis: Differentiation with MR imaging at 1ST. Radiology 166:333-340, 1988 68. Nyman R, Rehn S, Glimelius B, et al: Magnetic resonance imaging for assessment of treatment effects in mediastinal Hodgkin’s disease. Acta Radio1 Diagn 28: 145 151,1987 69. Glazer HS, Levitt RG, Lee JKT, et al: Differentiation of radiation fibrosis from recurrent pulmonary neoplasm by magnetic resonance imaging. AJR 143:729-730, 1984 70. Nyman RS, Rehn SM, et al: Residual mediastinal masses in Hodgkin disease: Prediction of size with MR imaging. Radiology 170:435-440, 1989