Radiographic assessment of airway tumors

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Radiographic assessment of airway tumors Rosaleen B. Parsons, MD*, Barton N. Milestone, MD, Lee P. Adler, MD Department of Diagnostic Imaging, Fox Chase Cancer Center, 7701 Burholme Avenue, Philadelphia, PA 19111, USA

The initial imaging evaluation of a patient with a suspected tracheal abnormality is the chest radiograph. The standard protocol consists of frontal and lateral views using a high kilovoltage technique. The chest radiograph is poor for detection of central airway lesions, with reported detection rates ranging between 23% and 66% versus 97% for CT [1,2]. Prior to the development of CT, planar tomography was performed to better evaluate the deep layers of the chest. Tomography is accomplished by the simultaneous motion of the radiograph tube and the film cassette with visualization of a selective layer of tissue. The motion intentionally blurs structures surrounding the tissue of interest (Fig. 1). In the mid-1970s tomography was found to be superior to standard chest radiography for the visualization of the trachea, for detection of cavities in pulmonary tuberculosis, and for identification of metastatic disease [3,4]. Tomography is rarely performed today for chest imaging. There have been major advances in chest radiography techniques secondary to improvements in electronics and computer technology that might ultimately improve plain film assessment of the central airways. These techniques include digitization, dual energy subtraction, temporal subtraction, varying filters, phosphor plates, and selenium detectors [5,6]. Image manipulation following digital acquisition can ‘‘correct’’ filming mistakes such as the underpenetrated film, which is notorious for blurring the mediastinum. Digital units that incorporate a photostimulable storage phosphor imaging plate (also called computed radiography [CR]) are now common. CR images are superior to standard radiographs for the visualization of the mediastinum, although they are not yet in widespread use [7,8]. When a film is digitized it can be coupled with a computer-assisted reading device (CAD). The CAD assists the clinician by marking suspicious areas on the

* Corresponding author. E-mail address: [email protected] (R.B. Parsons). 1052-3359/03/$ – see front matter D 2003, Elsevier Science (USA). All rights reserved. PII: S 1 0 5 2 - 3 3 5 9 ( 0 2 ) 0 0 0 3 9 - X

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Fig. 1. Coronal tomogram showing 3-cm adenoid cystic carcinoma adherent to right tracheal wall.

radiograph. It can be used with radiographs and CT. In one small study, detection accuracy for pulmonary nodules improved significantly for all interpreting physicians [9]. This technique is in its infancy, although it does appear to be promising for the detection of pulmonary nodules. Its role in the evaluation of central airways has yet to be determined.

Computerized axial tomography Computerized axial tomography (CT) has the advantage of displaying the intraluminal and extraluminal component of airway lesions. There is no question that CT is superior to standard radiographs, although in the recent past it was found to underestimate longitudinal tumor dimensions and it was unable to distinguish strictly mucosal lesions from lesions with submucosal extension [10]. The development of multidetector CT has led to dramatic changes in the use of CT. Tube heating issues have been corrected allowing slice acquisitions in the range of millimeters, which has permitted coverage of the entire chest in one breath-hold. Hundreds of images can then be viewed axially or transferred to a workstation and reformatted with multiplanar three-dimensional reconstruction

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(Fig. 2). Three-dimensional reconstructions have been found to be helpful for characterizing tracheal abnormalities and for demonstrating the extent and location of disease [11]. In one study that examined benign abnormalities of the central airways, reformatted images increased the confidence of chest physicians in the interpretation of typical carcinoids and other benign abnormalities of the central airways [12]. Fly-through techniques, which were adopted from the movie industry, have been incorporated with three-dimensional reformatting and provide an endoscopic view of the airways. Virtual endoscopy, also called virtual bronchoscopy, puts the physician inside the bronchi. Virtual bronchoscopy is superb for

Fig. 2. (A,B) Axial and coronal volume rendered images showing normal central and peripheral airways. (From Lawler LP, Fishman EK. Multi-detector row CT of thoracic disease with emphasis on 3D volume rendering and CT angiography. Radiographics 2001;21:1257 – 73; with permission)

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providing information about postobstructive airways and tumor measurements, although the reformats are extremely time-consuming, submucosal lesions might remain undetected, and mucous plugs are occasionally confused with mucosal lesions [13 –15].

General Tracheal tumors are rare. As a group they can be divided into epithelial and mesenchymal neoplasms. Secondary tumors arise from direct extension from the thyroid, lung, or esophagus. Tracheal metastases are extremely rare and typically arise from the kidney melanoma, breast, and colon [16]. Radiographically, it is difficult to differentiate tracheal tumors. Benign lesions tend to be small ( < 2 cm), well defined, rounded, and limited by the tracheal wall (Fig. 3) [17]. While more commonly seen with benign lesions such as the

Fig. 3. (A,B) Posterior-anterior (PA) and lateral views of a benign adenoma of right upper lung bronchus in 35-year-old woman.

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Fig. 3 (continued ).

hamartoma and chondroid tumors, punctate calcifications are also seen in chondrosarcomas [18].

Carcinoid Bronchial carcinoid tumors are typically symptomatic because of the propensity of the tumor to arise centrally. The vast majority occurs in the lobar bronchi or mainstem bronchi. About 15% of these tumors occur in the segmental bronchi or lung periphery [19]. The lesions tend to be large (averaging 3 cm), and most have a dumbbell shape with airway and parenchymal components [20]. On chest films, the typical presentation is that of a central mass with either peripheral atelectastis or pneumonia (Fig. 4) [21]. Rarely, carcinoid presents as an isolated parenchymal nodule that is less than 3 cm in diameter. CT features that can aid in the diagnosis of carcinoid tumors are calcification and contrast enhancement. Calcification is seen in 26% of tumors (particularly in central carcinoids) and it can (rarely) mimic broncholithiasis [22,23]. If there is an associated deformity of the bronchus, carcinoid tumor is the most likely

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Fig. 4. (A) Five-cm central carcinoid tumor with right middle lobe consolidation. (B) Corresponding CT with central carcinoid in right bronchus.

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diagnosis [24]. When contrast is administered some lesions enhance, which aids in the visual distinction of the tumor from adjacent consolidated lung [25]. Lymphadenopathy can be a sign of metastatic disease, although reactive nodes are also common secondary to frequent lung consolidation. An octreotide scan can be used to distinguish benign from malignant nodal enlargement.

Adenoid cystic carcinoma Adenoid cystic carcinomas are considered to be low-grade tumors. They typically arise from the posterolateral wall of the lower trachea [26] and tend to be larger than 2 cm. The most common radiographic findings are of an intraluminal, irregular mass (Fig. 5). The tumors often invade the submucosa and infiltrate the perineural lymphatics; adenopathy is seen in 10% of cases [17,26 –28]. Submucosal extension frequently leads to underestimation of the tumor length. Circumferential tracheal narrowing and extraluminal tumors are common features that are demonstrated on CT [29]. In one small study of six patients, atelectasis was a common feature (demonstrated on CT in four of the patients) [17]. The imaging features of adenoid cystic carcinoma are indistinguishable from squamous cell carcinoma.

Plasma cell granuloma Plasma cell granuloma is an inflammatory lesion that has also been called inflammatory pseudotumor, histiocytoma, xanthoma, and sclerosing heman-

Fig. 5. CT of large adenoid cystic carcinoma arising from posterior wall of upper trachea.

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gioma. Plasma cells are found in all lesions, and since 1973 the lesion has been classified as a plasma cell granuloma [30]. These lesions are uncommon, and when found in the trachea they are usually present in the lower third (Fig. 6) [31]. The typical patient is a young nonsmoker who has symptoms of airway obstruction. In a large retrospective review of 23 patients, the mean tumor size was 4 cm with a range of 1 to 15 cm. Half of the patients had a large mass on chest radiograph. The cross-sectional imaging features were not described [32]. Radiographically, the lesions are smooth-walled, they can be located throughout the airway, and they do not have distinguishing features.

Fig. 6. (A) CT soft tissue window. (B) CT lung window. 28-year-old with a plasma cell granuloma (arrow) with post-obstruction pneumonia.

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Magnetic resonance imaging The major uses of MRI in the chest have been in the evaluation of tumors of the heart, congenital heart disease, mediastinal and hilar structures, and the diaphragm. The routine use of MRI in airway tumors has been limited to evaluating chest wall or mediastinal invasion in bronchogenic carcinoma. New multidetector row CT scanners can acquire high-resolution, thin-slice images in the breath-hold that permit exquisite multiplanar and three-dimensional reconstructions. The use of MRI in the assessment of airway tumors will therefore have a limited and selective role, although that role has not yet been fully elucidated. MRI does not currently match the resolution of CT, but MRI displays different tissue characteristics that yield much higher tissue contrast than CT. If a tumor is isodense to adjacent tissue on CT, better resolution will not allow discrimination between where tumor stops and normal tissue begins. In the past, magnetic susceptibility effects, which occur at air/soft tissue interfaces and result in signal loss and distortion, limited MRI imaging of the lung parenchyma and tumors in the parenchyma; however, newer pulse sequences using ultrashort echo times have eliminated most of these susceptibility problems and have even allowed imaging of lung tissue [33]. MRI (compared with CT) has direct multiplanar imaging capabilities, and often in-plane resolution from in-plane scanning will be superior to in-plane resolution from a multiplanar reconstruction. Improved phased array surface coils and fast breath-hold sequences with or without dynamic gadolinium enhancement have markedly improved MR imaging of the chest. Fast, multiplanar breath-hold T1W gradient echo and volume ultrafast gradient echo sequences with and without gadolinium enhancement in combination with breath-hold half fourier turbo/fast spin echo sequences and ECG-gated turbo/fast spin echo sequences are currently the pulse sequences that are used to assess airway tumors. Newer sequences such as true fast imaging with steady state precision (FISP) imaging might permit near real-time imaging of the airway, yielding dynamic respiratory information. Imaging at 3 Tesla and an increased number of receiver channels combined with the use of parallel processing techniques might further improve MR evaluation of chest and airway tumors. Most airway tumors have intermediate signal intensity on T1W pulse sequences, which is similar to that of thoracic musculature. On T2W pulse sequences most airway tumors have relatively high signal intensity (ie, greater than muscle). Most airway tumors are therefore indistinguishable from one another on MRI because their imaging features are nonspecific. Some exceptions to this signal pattern are discussed in this article. The role of MRI in the assessment of airway tumors is currently limited to some problem-solving issues, tissue characterization, and evaluation of mediastinal involvement. Of all the nonbronchogenic airway tumors, bronchial carcinoid tumors have been examined most frequently using MRI. Typical of carcinoid tumors in the liver, bronchial carcinoid tumors are high in signal on T2W pulse sequences [34,35] and demonstrate rapid enhancement from the bronchial artery system [36].

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In patients with ectopic occult adrenocorticotropic hormone (ACTH)-producing tumors, MRI might play a role in the early detection of small bronchial carcinoid tumors [34] in conjunction with somatostatin analogue scintigraphy. Leiomyomas and fibromas are rare airway tumors that have no reports of imaging using MRI; however, uterine leiomyomas and ovarian fibromas are routinely imaged with MRI and are typically low in signal on T1W and T2W sequences. These signal characteristics in an airway tumor suggest leiomyoma or fibroma; however, there has been a report of primary solitary amyloidoma of the lung that had similar signal characteristics [37]. Pulmonary hamartomas contain predominantly cartilage and fibrous connective tissue, with 25% to 30% containing calcification and some containing fat. The diagnosis is made readily with CT when macroscopic fat or characteristic calcification is present. Sakai et al [38] reported that the MRI appearance of pulmonary hamartomas had intermediate signal intensity on T1W images that was higher than skeletal muscle with relatively high signal septa. On T2W images the hamartomas were relatively high in signal, with 50% demonstrating a lobulated appearance secondary to lower signal intensity septa. As in other cartilage-containing tumors in the bones, pulmonary hamartomas showed marked enhancement of the connective tissue septa as rings and arcs that surrounded the cartilaginous lobules on gadolinium-enhanced images. These typical imaging characteristics and enhancement pattern in a lung nodule suggest the diagnosis of pulmonary hamartoma. MRI will readily demonstrate fat in a tumor as high signal on T1W images and intermediate signal on T2W images. This high signal on the T1W images can be saturated out with a chemically selective fat saturation pulse. As in other fat-containing tumors in the body (which contain microscopic fat), indiscernible fat in pulmonary hamartomas with standard imaging might be detected as signal loss by fat and water out of phase gradient echo imaging. Lipomas [39] of the airways (although rare) can be definitively diagnosed with MRI because of their signal characteristics and with the use of chemical shift. Adenoid cystic carcinoma arising from the tracheobronchial gland is the second most common primary tracheal tumor. Because the tumor tends to grow submucosally and invade the mediastinum, MRI can show the extent of mediastinal invasion and submucosal growth better than CT [40,41]. The signal intensity of adenoid cystic carcinomas on T1W and T2W images is not characteristic and is similar to most other airway tumors. MRI can readily demonstrate mediastinal invasion by mucoepidermoid tumors (as with other tumors invading the mediastinum). Many other rare tumors arise from the tracheobronchial tree; there are case reports of the nonspecific MRI appearance of tracheal schwannoma [42], pulmonary plasmacytoma [43], and metastatic melanoma [44]; however, most of these rare tumors have no reports of their MR appearance. As MRI continues to improve in speed and resolution, it might be useful to further evaluate its role in the assessment of airway tumors. Even now MRI is a useful adjunct in the imaging of certain airway tumors after initial assessment by CT.

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Functional imaging of neuroendocrine thoracic tumors Nuclear medicine imaging is growing rapidly and is challenging radiologists and clinicians. Nuclear imaging complements traditional diagnostic imaging techniques (chest radiographs, CT, MRI) by providing useful and important incremental information for the evaluation of solitary pulmonary nodules, staging of lung cancer, and evaluation of response to therapy. Chest radiographs and CT are extremely important in the management of patients with suspected lung cancer. These modalities provide anatomic and morphologic information, but they do not accurately characterize abnormalities as benign or malignant [45,46]. Tomographic nuclear images are replacing the traditional planar images in which true three-dimensional distribution of radioactivity can be produced. The two most common types of nuclear medicine studies are single photon emission computed tomography (SPECT) and positron emission tomography (PET). In contrast with conventional nuclear imaging studies (which measure g or b emissions), PET measures the release of positrons. When a proton decays to a neutron, it releases a positron (a positively charged particle equal in mass to an electron) from the nucleus. The positron travels few millimeters in soft tissue before colliding with a negative electron. In this collision both particles are annihilated, releasing two g rays, each with 511 keV of energy that is emitted approximately 180 to each other and recorded by two opposite detectors. By using different tracers, a multitude of physiological, biochemical, and pharmacokinetic parameters can be measured. PET is also characterized by the ability to measure regional tissue tracer concentrations with high degrees of accuracy and sensitivity [47,48]. Radionuclides used in SPECT imaging usually emit a single photon of about 140 keV. SPECT has less efficiency and resolution compared with PET. SPECT uses traditional g camera positioning logic and is used with traditional radioactive tracers [45]. Advances in radiopharmaceutical science and practical and economic aspects of SPECT instrumentation make this method of imaging attractive for many clinical studies.

Carcinoid tumors The PET tracer f-18flurodeoxyglucose (FDG), a glucose analogue, is used to image glucose metabolism. A specific application of FDG PET is differentiation of benign from malignant lesions. FDG PET is highly sensitive and specific in detecting malignancy in solitary pulmonary nodules [49], which is not the case in carcinoid tumors, in which high false-negative FDG PET is caused by the low metabolic activity in these tumors. In one report [50], six of seven pulmonary carcinoid tumors were hypometabolic. Somatostatin receptors are membrane glycoproteins. The molecular biology, pharmacology, expression, and function of these receptors were reviewed by

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Patel et al [51]. Somatostatin receptors have been demonstrated in many neuroendocrine cells and tumors [51 – 53]. Neuroendocrine tumors have (in general) increased density of somatostatin receptors; this enables their in vitro and in vivo visualization with radiolabeled somatostatin analogues [54]. Two radiolabeled peptide analogues that are particularly useful in carcinoid tumors are [(111)In-DTPA(0)]octreotide (Octreoscan; Mallinkrodt, Petten, The Netherlands) [54 – 57] and 99mTc depreotide SPECT (Neotect; Diatide, Londonderry, NH) [58 –60]. In terms of sensitivity and clinical usefulness, the value of [(111)InDTPA(0)]octreotide is high. In one study [55], 31 out of 40 patients with carcinoid tumors (histologically verified in 37 patients) proved to be positive. In another study [56], one or several lesions could be detected in 77 of 100 scintigraphic investigations. Le Rest et al [57] identified 10 out of 11 patients with metastatic carcinoid tumors. An example of a patient with a carcinoid tumor using an Octreotide scan is shown in Fig. 7. There is increased radiotracer accumulation in two foci in the superior mediastinum (large focus on the left side and smaller focus on the right

Fig. 7. Whole-body octreotide scintigraphy views after (A) 4 hours and (B) 24 hours. Note the superior mediastinal foci (arrows) and the periaortic linear focus (arrowhead).

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side), which are more intense in the 24-hour delayed image. There is also a linear collection activity in the periaortic region, which again is more intense on the delayed image. The Tc99m-labeled peptide depreotide has been used recently in the differential diagnosis of patients with solitary pulmonary nodules [58,59]. In the first report [58], Blum et al studied 30 solitary pulmonary nodules (one case was carcinoid tumor); the sensitivity was 92% and the specificity was 88% for detecting malignancy. In the second study [59], Blum et al evaluated 114 patients (four carcinoid tumors); the sensitivity and specificity for detecting malignancy were 96.6% and 73.1%, respectively. There has recently been progress in overlying nuclear images on CT or MR images that have been acquired separately or even simultaneously [61 – 63].

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