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1 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Kangnam-gu,
Seoul 135-710, South Korea.
2 Department of Thoracic Surgery, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Seoul 135-710, South Korea.
3 Department of Diagnostic Pathology, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Seoul 135-710, South Korea.
4 Division of Pulmonary and Critical Care Medicine, Department of Medicine,
Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul
135-710, South Korea.
Received December 19, 2003;
accepted after revision February 16, 2004.
Address correspondence to K. S. Lee.
Abstract
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MATERIALS AND METHODS. The CT findings of thymic epithelial tumors were analyzed in 91 patients who had undergone surgery between May 1995 and June 2002. Two observers, who were unaware of the histopathologic classification made in accordance with World Health Organization (WHO) recommendations and the prognosis of the tumors, retrospectively reviewed the initial CT findings in terms of the contours and shapes of the tumors and the presence of necrosis, calcification, mediastinal fat or great vessel invasion, pleural seeding, contrast enhancement, and lymph node enlargement. These findings were compared with the simplified subgroups of WHO histologic classification (low-risk thymomas [types A, AB, and B1], high-risk thymomas [types B2 and B3], and thymic carcinomas [type C]) and with postoperative recurrence.
RESULTS. The study found 31 low-risk thymomas (eight type A, 16 type AB, and seven type B1 tumors), 45 high-risk thymomas (25 type B2 and 20 type B3), and 15 thymic carcinomas (type C). Lobulated contour was more often seen in high-risk thymomas (26/45, 58%; p = 0.0456) and thymic carcinomas (10/15, 67%; p = 0.033) than in low-risk thymomas (9/31, 29%). Mediastinal fat invasion was more often seen in thymic carcinomas (5/15, 33%; p = 0.0133) than in low-risk thymomas (1/31, 3%). Great vessel invasion was seen only in thymic carcinomas (2/15, 13%; p = 0.0244). Tumors with a lobulated or irregular contour, an oval shape, mediastinal fat or great vessel invasion, and pleural seeding showed significantly more frequent recurrence and metastasis (all, p < 0.05).
CONCLUSION. Although CT is of limited value in differentiating histologic subtypes according to the WHO classification, CT findings may serve as predictors of postoperative recurrence or metastasis for the thymic epithelial tumors.
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Most clinicians and radiologists, however, are unfamiliar with such a complex classification scheme in daily practice. In addition, poor interobserver reliability in identifying the various WHO histologic subtypes of the tumors (especially type B tumors) has been reported [19]. Therefore, recently, an attempt to simplify the WHO classification scheme by lumping groups together with similar prognostic appearance (types A, AB, B1, and B2 as one group; type B3 as another; and type C as the third) is made to facilitate the clinicopathologic understanding of the thymic epithelial tumors [19]. However, patients with type B2 tumors have been reported to have lower survival rates than patients with type A, AB, or B1 tumors [18, 20]. According to one study dealing with large numbers of thymic epithelial tumors, overall survival rates of patients with type A, AB, or B1 tumors were higher than those of patients with type B2 or B3 tumors [20]. Therefore, we tried to simplify the WHO histologic classification of thymic epithelial tumors into three subgroups: low-risk thymomas (types A, AB, and B1), high-risk thymomas (types B2 and B3), and thymic carcinomas (type C).
The purposes of our study were to describe the CT findings of thymic epithelial tumors in terms of the newly proposed and simplified WHO classification scheme of three subgroups and to correlate the CT findings of the three subgroups of the tumors with prognosis.
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Forty-four (48%) of the 91 patients were asymptomatic. In these patients, chest radiographs helped identify the tumors incidentally by showing mediastinal widening or a mass on routine studies. The most common symptoms in the remaining 47 patients were chest pain or discomfort (22/91, 24%), followed by symptoms and signs of myasthenia gravis (18/91, 20%), dyspnea (3/91, 3%), weight loss (2/91, 2%), hoarseness (1/91, 1%), and neck swelling (1/91, 1%). Of these 91 patients, 82 underwent complete surgical resection and the remaining nine, incomplete surgical resection because of the involvement of adjacent mediastinal structures or pleural seeding. All tumors were also staged according to the Masaoka clinical–pathologic staging system [21]. This staging system is based on the presence and extent of transcapsular invasion into adjacent mediastinal tissues or neighboring organs confirmed as a surgical finding or at histopathologic examination. Stage I included encapsulated thymoma without microscopic evidence of capsule invasion; stage II, macroscopic (IIa) or microscopic (IIb) invasion of the surrounding fatty tissue or the mediastinal pleura; stage III, macroscopic invasion of a neighboring organ, such as the pericardium, great vessels, or lung; and stage IV, pleural or pericardial dissemination (IVa) and lymphogenous or hematogenous metastasis (IVb). Postoperative adjuvant therapy was administered to patients with stage II–IV disease. Of 91 patients, 55 underwent postoperative adjuvant therapy: radiation (5,400 cGy) only (n = 39), radiation and chemotherapy (n = 8), or chemotherapy only (n = 8).
All surgical specimens were reviewed and reclassified according to the 1999 WHO classification by an experienced lung pathologist who was unaware of the outcome or the tumor imaging findings. The WHO classification [15] is based on the morphology of epithelial cells and on the lymphocyte-to-epithelial cell ratio. Type A and B tumors are composed of a homogeneous population of neoplastic epithelial cells with spindle- or oval-shaped nuclei (A) and dendritic or epithelioid nuclei (B). Type AB tumors combine the morphologic features of types A and B. Type B1 tumors mainly consist of a dense population of lymphocytes, and some epithelial tumor cells with large nuclei of pale chromatin and small nucleoli. Type B2 tumors are composed of a nest of epithelial cells, and lymphocytes are less abundant than in type B1. Type B3 tumors consist predominantly of polygonal epithelial cells with nuclear atypia and some prominent nucleoli, and type C tumors consist of a nest of squamous cell carcinoma cells with severe nuclear atypia and mitotic figures. All thymic carcinomas are classified as type C.
All tumors were regrouped into three subgroups: low-risk thymomas (types A, AB, and B1), high-risk thymomas (types B2 and B3), or thymic carcinomas (type C).
Image Acquisition and Analysis
CT scans were available for all 91 patients. The mean interval between
pathologic diagnosis and CT was 17.6 days (range, 1–244 days). Before
October 2000, helical CT was performed with a HiSpeed Advantage scanner (GE
Healthcare) in 41 patients. When the main lesion site was identified on a
scanogram (i.e., the initial topography for a detailed CT section), unenhanced
thin-section CT (1-mm collimation) was performed through the lesion at 5-mm
intervals before the acquisition of helical CT, which was performed from the
lung apices to the middle portion of both kidneys with 7-mm collimation and a
pitch of 1.3. Scanning was performed after the IV injection of contrast medium
(100 mL of iopamidol [Iopamiron 300, Bracco]) at a rate of 2 mL/sec using a
power injector (MCT Plus, Medrad). Imaging data were reconstructed using 7-mm
collimation.
After October 2000, helical CT was performed using a 4-MDCT scanner (LightSpeed QX/i, GE Healthcare) on 29 of the patients. Unenhanced thin-section CT (1.25-mm collimation) was performed at 10-mm intervals before the acquisition of helical CT. Helical CT was performed from the lung apices to the middle portion of both kidneys with 5-mm collimation and a pitch of 3. Scanning was performed after the IV injection of contrast medium (100 mL of iopamidol [Iopamiron 300, Bracco]) at a rate of 2 mL/sec using a power injector (MCT Plus, Medrad).
The remaining 21 patients were scanned at other hospitals. Scanning consisted of conventional CT from the level of the thoracic inlet to the level of the middle portion of the kidneys (10-mm collimation) with the IV administration of contrast medium. In all patients, the scanning parameters were 120 kVp and 170–200 mA. All imaging data were reconstructed using a bone algorithm. Data were directly displayed on four monitors (1,536 x 2,048 image matrices, 8-bit viewable gray-scale, and luminescence of 60 foot-lamberts) of a PACS (General Electric Medical Systems Integrated Imaging Solutions). Imaging data of hard copies in 21 patients whose CT scans were obtained at other hospitals were scanned (2905M, Array Corporation) and uploaded to a PACS. All monitors showed images obtained using both mediastinal (width, 400 H; level, 20 H) and lung (width, 1,500 H; level, –700 H) window settings.
Two chest radiologists who were unaware of the histologic classifications and the prognosis of tumors assessed the CT scans retrospectively. Decisions concerning the CT findings were reached by consensus. CT scans were assessed for the location, size (short and long axes), shape, marginal characteristics, homogeneity, attenuation (compared with chest wall muscle), and degree of tumor enhancement. The presence of tumor necrosis and calcification and associated findings, if any, were also recorded.
The presence of mediastinal fat infiltration, invasion of the great vessels, pleural and pericardial effusion, pleural metastases, lymph node enlargement (short-axis diameter > 10 mm), and metastases were also evaluated. The location of the tumor was categorized as right, left, or midline in the anterior mediastinum. The longest diameter of the tumor was measured where the tumor appeared largest on an axial image. Tumor shape was classified as round if the long- to short-axis ratio was less than or equal to 1.5, oval if the ratio was greater than 1.5 but less than 3.0, or plaque if the ratio was greater than or equal to 3.0. Marginal characteristics were subclassified as smooth, lobulated, or irregular.
The pattern of enhancement was recorded as homogeneous or heterogeneous, and the degree of enhancement was classified as less than that of the chest wall muscle, equal to that of the chest wall muscle, or greater than that of the chest wall muscle by visual estimation. Tumor necrosis was presumed to be present when a focal area of low attenuation was seen on enhanced scans. Invasion of the great vessels was considered present when the tumor abutted and altered the contour of the corresponding vessels or when overt tumor thrombosis and vascular occlusion were present.
Postoperative follow-up CT scans were available in all 91 patients. The mean follow-up period was 24.3 months (range, 4–74 months). Follow-up CT scans were assessed for the presence or absence of local recurrence, pleural or pericardial seeding, or intra- or extrathoracic metastasis.
Statistical Analysis
Statistical differences in the prevalence of each CT finding for the
different simplified WHO histologic subgroups were analyzed using Fisher's
exact test with the permutation method for multiple testing. Differences in
the tumor sizes of the WHO histologic types were assessed using the analysis
of variance or Kruskal-Wallis test. Associations between imaging findings and
postoperative recurrence or metastasis were also determined using Fisher's
exact test with permutation method for multiple testing.
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CT findings of thymic epithelial tumors, based on the simplified WHO histologic classification, are summarized in Table 2. Eighty-nine of the 91 tumors were located in the anterior mediastinum: right side (n = 41), left side (n = 36), or midline (n = 12). Two of 91 tumors were located in the neck. The long- and short-axis diameters (means ± SD) of tumors in the simplified WHO histologic subgroups were 50.8 ± 24.1 and 35.4 ± 17.6 mm for low-risk thymomas; 47.2 ± 23.5 and 29.8 ± 13.9 mm for high-risk thymomas; and 60.1 ± 27.1 and 42.9 ± 16.3 mm, respectively, for thymic carcinomas. The long- and short-axis diameters of high-risk thymomas were significantly shorter than those of thymic carcinomas (p = 0.006). Lobulated contour was more often seen in high-risk thymomas (26/45, 58%; p = 0.0456) and thymic carcinomas (10/15, 67%; p = 0.033) than in low-risk thymomas (9/31, 29%) (Figs. 1 and 2A, 2B). Mediastinal fat invasion was more often seen in thymic carcinomas (5/15, 33%; p = 0.0133) than in low-risk thymomas (1/31, 3%) (Figs. 1 and 3A, 3B, 3C). Great vessel invasion was seen only in the thymic carcinomas (2/15, 13%; p = 0.0244) (Figs. 3A, 3B, and 3C). Calcification was more frequently seen in high-risk thymomas (14/45, 31%) (Figs. 2A and 2B) than in low-risk thymomas (3/31, 10%), but no significant difference between high- and low-risk thymomas was seen (p = 0.084). Pleural seeding (Figs. 2A, 2B and 3A, 3B, 3C) was more often seen in thymic carcinomas (4/15, 27%) than in low- (1/31, 3%) and high-risk (4/45, 9%) thymomas, but no statistically significant difference (p = 0.058) existed. Necrosis (Figs. 2A and 2B) was more often seen in high-risk thymomas (19/45, 42%) and thymic carcinomas (6/15, 40%) than in low-risk thymomas (6/31, 19%), with no statistically significant difference (p = 0.089). Other CT findings, including shape of tumors (p = 0.414), pattern and degree of enhancement (p = 0.267), presence or absence of lymph node (p = 0.375), and pleural (p = 0.289) or pericardial effusion (p = 0.375), were not different between WHO histologic subtypes.
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Fifteen patients (two B2, six B3, and seven C tumors) had recurrent or metastatic disease on follow-up CT. Nine (60%) of the 15 patients had only local or regional recurrence, three (20%) had hematogenous distant metastases, and the remaining three (20%) had both locoregional and distant metastases. Eight (53%) of the 15 patients with recurrent or metastatic disease had undergone complete tumor resection, whereas the remaining seven (47%) had undergone incomplete surgical resection. Tumors with a lobulated or irregular contour (p = 0.0006), an oval shape (p = 0.0087), mediastinal fat (p = 0.036), or great vessel invasion (p = 0.0256) and pleural seeding (p = 0.0005) on the initial CT scans showed significantly more recurrence and metastasis (Figs. 2A, 2B and 3A, 3B, 3C and Table 3).
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However, the CT findings of the thymic epithelial tumors have many degrees of overlap between subgroups of the simplified WHO classification in our study and are different from those reported by Tomiyama et al. [22]. Those researchers reported that smooth contours and a round shape are suggestive of type A tumor; irregular contours and mediastinal lymphadenopathy are suggestive of type C tumor; and calcification is suggestive of type B1, B2, and B3 tumors.
Of many CT findings of thymic epithelial tumors, only the contour of tumors, mediastinal fat, and great vessel invasion enabled us to differentiate subgroups of the simplified WHO classification in our study. In the studies of Tomiyama et al. and Jung et al. [24], type C tumors were significantly larger than any other type of thymic epithelial tumors. In our study, the long- and short-axis diameters of thymic carcinoma (i.e., type C tumors) were larger than those of low- and high-risk thymomas; however, the statistically significant difference was present only between high-risk thymomas and thymic carcinomas. In our study, high-risk thymomas were significantly shorter than those of thymic carcinomas (p = 0.006). These findings may be related to the proportion of myasthenia gravis. Nine (20%) of 45 patients with high-risk thymomas in our study had myasthenia gravis, whereas only one (7%) of 15 patients with thymic carcinomas had myasthenia gravis. The symptoms and signs of myasthenia gravis in these particular patients with high-risk thymomas may have led to earlier imaging studies than for patients with thymic carcinomas and without myasthenia, thus to earlier diagnoses when the tumors were still small. Therefore, our study indicates that high-risk tumors may be smaller than thymic carcinomas.
In the studies of Tomiyama et al. [22], calcifications within the tumors were suggestive of type B tumors (type B1 [4/9, 44%], B2 [8.5/14, 61%], and B3 [3/4, 75%]). Although calcification was more frequently seen in high-risk thymomas (14/45, 31%) than in low-risk thymomas (3/31, 10%) in our study, the frequency was not significantly different between high- and low-risk thymomas (p = 0.084).
The frequency of mediastinal lymphadenopathy in thymic carcinoma—type C tumors—has been reported to range from 40% to 44% [22, 24, 25]. However, we found mediastinal lymphadenopathy in only two (13%) of 15 patients with type C tumors. Selection bias may have contributed to these results. Five of the six excluded patients who received preoperative chemotherapy and radiation therapy because of extrathoracic metastases and whose initial CT scans were unavailable had type C tumors. Therefore, the frequency of mediastinal lymphadenopathy appeared to be somewhat lower in our study. We found that mediastinal fat and great vessel invasion were more frequently observed in type C tumors than in any other tumor subtype (Table 2). These results are comparable to those of a previous study by Jung et al. [24], who reported that CT findings of a large tumor with great vessel invasion, mediastinal or hilar lymphadenopathy, phrenic nerve palsy, or hematogenous metastasis favor the possibility of thymic carcinoma.
Thymic epithelial tumors show a broad spectrum of both biologic and morphologic features and a wide range (8–29%) of recurrence rates (9, 13, 16–18) after surgical resection. In our study, the recurrence rate after complete tumor surgical resection was 10% (8/82). Although no unique prognostic factor has been identified, several studies have indicated the importance of clinical features (i.e., age and the presence or absence of myasthenia gravis), Masaoka staging, the completeness of surgical resection, WHO histologic type, size of tumor, and great vessel or mediastinal invasion as predictors of recurrence and survival after resection [6–14, 16–18]. In the study by Suster and Rosai [1] on the histopathologic evaluation of resected tumors, the following morphologic features showed a poor prognosis: poorly circumscribed infiltrating tumor margins, a mitotic count greater than 10 in 10 high-power fields on microscopic examination, a lack of lobular growth, and a high-grade histology. Blumberg et al. [10] found survival rates depend on the invasion of innominate vessels. In our study, tumors with a lobulated or irregular contour, an oval shape, a mediastinal fat or great vessel invasion, or pleural seeding on the initial CT scans showed significantly more frequent recurrence and metastasis.
Our study has several limitations. As with other studies, ours was not population-based; thus, it may be subject to selection bias. As previously mentioned, several patients with type C tumors who received preoperative chemotherapy and radiation therapy because of extrathoracic metastases were excluded. Our study included eight patients who received an incomplete surgical resection. Incomplete surgical resection may affect recurrence. Our study is a retrospective review of imaging findings and medical records and did not involve the prospective identification of each tumor type. We did not evaluate overall survival rates because of the short follow-up period. However, no tumor-related death occurred during our study. The small number of deaths related directly to thymomas suggests that thymic epithelial tumors have an indolent nature and often spread locally within the mediastinum or to the adjacent pleural cavity rather than disseminate to distant organs.
In summary, our study shows that of many CT findings of thymic epithelial tumors, only the contour of tumors, mediastinal fat, and great vessel invasion could be used to differentiate subgroups of the simplified WHO classification. Tumors with a lobulated or irregular contour, oval shape, mediastinal fat or great vessel invasion, or pleural seeding show significantly high recurrence and metastasis rates. Although CT is of limited value in differentiating histologic subtypes according to the WHO classification, CT findings may serve as predictors of postoperative recurrence or metastasis for this tumor type.
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