Magnetic

Resonance Imaging in the Evaluation

of Lung Cancer

By Warren B. Gefter

W

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

CONSIDERATIONS

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

in Roanrgenology,

Vol XXV,

No 1 (January),

1990:

pp 73-84

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

APPROACH

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

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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

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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

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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

Mediastinaf

Invasion

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.

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4A). Central bronchogenic carcinomas also at times invade the pulmonary veins and extend into the left atrium (Fig 4B). Bronchial

Involvement

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

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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

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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.

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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).

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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).

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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-

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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

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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

Evaluation

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

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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,

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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.

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