Thymic epithelial neoplasms are malignant tumors arising from the thymus that account for 0.2% to 1.5% of all malignancies but are the most common non-lymphomatous primary neoplasms of the anterior mediastinum.1,2 Less is known about thymic epithelial neoplasms, such as thymoma, thymic carcinoma, and thymic neuroendocrine tumors, than more common thoracic tumors regarding optimal detection, staging, and treatment. Recently, increased interest in the mediastinum and lesions that may be found there has led to greater international collaboration and resulted in the formation of the International Thymic Malignancy Interest Group (ITMIG). This multidisciplinary organization provides an infrastructure for studying these lesions and, with the formation of an international thymic malignancy database, it is hoped that large-scale multi-institutional studies will continue to advance the scientific knowledge of these tumors.3 Since its inception, ITMIG has crafted and published numerous standards and policy papers, guidelines, and recommendations aimed at addressing specific topics, knowledge gaps, and limitations of existing guidelines regarding thymic epithelial neoplasms.3 – 5
Although computed tomography (CT) is typically considered the imaging modality of choice for identifying thymic tumors, characterizing the primary neoplasm, and staging of disease, the role of magnetic resonance (MR) imaging continues to expand. MR imaging is effective in distinguishing thymic epithelial neoplasms and other malignant tumors from benign lesions in the prevascular mediastinum and can be used to characterize and stage thymic tumors in those patients with contraindications to contrast-enhanced CT such as severe contrast allergy and/or renal failure.6 In addition, the excellent contrast resolution of MR imaging can reveal morphologic features of thymic tumors that enable classification into different histologic types based on aggressiveness and differentiation between advanced-stage disease and earlier-stage disease.
At least 15 different stage classification systems have been proposed and used to varying degrees clinically, most of which have been derived from data on small groups of patients.7 The most widely used staging classifications are the Masaoka and Masaoka- Koga staging systems; however, the Masaoka classification originated from data on only 91 patients and the Koga modification was derived from data on only 76 patients.8,9 In clinical practice, it has been common for institutions to interpret these staging systems differently, thus limiting the ability of clinicians from various specialties to communicate and collaborate effectively.10 Recently, an official, consistent tumor node metastasis (TNM) staging system has been recognized by the American Joint Committee on Cancer (AJCC) and the Union for International Cancer Control (UICC), based on an analysis of a retrospective database performed by the International Association for the Study of Lung Cancer (IASLC) and ITMIG.11,12
In this article, we review the clinical and MR imaging characteristics of thymic epithelial neoplasms and the recently published TNM staging system created by IASLC and ITMIG.
The first histologic classification system of thymic epithelial neoplasms was published by the World Health Organization (WHO) Consensus Committee in 1999 and subdivided thymoma into 6 subtypes (A, AB, B1, B2, B3, and C) based on morphologic features of the neoplastic epithelial cells and the lymphocyte–epithelial cell ratio. A revised scheme released in 2004 repositioned type C, or thymic carcinoma, to a distinct category.13 Several limitations of these classification schemes have been outlined previously, including the histologic heterogeneity of thymic epithelial neoplasms, as many different subtypes may coexist within the same lesion, and the lack of intra- and interobserver reproducibility and clinical predictive value.14,15
More recently, ITMIG published a consensus statement regarding the histologic classification of thymic epithelial neoplasms in 2014, which informed the updated 2015 WHO classification.16,17 This classification system maintained the established nomenclature, in which thymomas are separated from thymic carcinomas, and thymomas are subdivided into A, AB, B1, B2, and B3 types based upon the morphology of epithelial tumor cells (polygonal or spindle cells), the relative proportion of the nontumoral lymphocytic component (decreasing from type B1 to B3), and resemblance to normal thymic architecture.16 The most frequent subtype of thymic carcinoma is squamous cell carcinoma. The ITMIG consensus statement proposed major and minor morphological and immunohistochemical criteria to better individualize each thymic epithelial neoplasm.17 Thymic neuroendocrine tumors are divided into well-differentiated neuroendocrine neoplasms and poorly differentiated carcinomas, the former of which include typical and atypical carcinoids and the latter of which include large cell and small cell carcinomas.18 Typical carcinoid tumors show no necrosis and less than 2 mitoses per 2 mm2, whereas atypical carcinoid tumors demonstrate regions of necrosis and/or 2 to 10 mitoses per 2 mm2. In contrast, more aggressive neoplasms such as large cell and small cell neuroendocrine carcinomas have average mitoses of 60 to 70 per 2 mm2.18
Epidemiology and Clinical Presentation
Thymoma is the most common thymic epithelial tumor and primary malignant neoplasm of the anterior mediastinum, the incidence of which is 1 to 5 cases per million individuals per year in the U.S.1 The incidence is higher in Asians and African-Americans than in Hispanics and Caucasians, and men and women are affected equally.1 Thymomas are typically slow-growing neoplasms but may demonstrate aggressive behavior such as invasion of adjacent thoracic structures and involvement of the pleura and pericardium; however, distant metastatic disease is rare.19 Clinical symptoms may be present at the time of presentation, the most common of which are related to compression and invasion of adjacent structures, such as dysphagia, diaphragmatic paralysis, and superior vena cava (SVC) syndrome. Chest pain, dyspnea, or cough are present in one-third of patients.20 Patients with thymoma may be affected by paraneoplastic syndromes, the most common of which is myasthenia gravis. Although 30% to 50% of patients with thymoma display signs and symptoms of myasthenia gravis, only 10% to 15% of patients with myasthenia gravis have thymoma.21 Other paraneoplastic syndromes include hypogammaglobulinemia and pure red cell aplasia, which are present in 10% and 5% of cases, respectively.22
Thymic carcinoma accounts for approximately 20% of thymic epithelial neoplasms and the mean age of presentation is 50 years.23,24 Aggressive features such as local invasion and intrathoracic lymphadenopathy are much more common in thymic carcinoma than thymoma, and approximately 50% to 65% of patients present with distant metastases at the time of diagnosis.24 Most clinical symptoms are related to compression and invasion of adjacent structures and, in contrast to thymoma, paraneoplastic syndromes are rare.
Neuroendocrine thymic neoplasms, most of which are carcinoids, are the least common type of thymic epithelial neoplasm, representing 2% to 5% of all such lesions.25 The annual incidence in the U.S. is 0.2 per 1 million.26 Approximately 25% of lesions develop in patients with multiple endocrine neoplasia (MEN) syndrome type 1.27 Neuroendocrine tumors tend to demonstrate aggressive behavior such as invasion of adjacent structures and mediastinal lymph node involvement.28 Patients with thymic neuroendocrine neoplasms tend to be have symptoms at presentation, including cough, dyspnea, and chest pain related to compression and invasion of adjacent structures, hoarseness due to involvement of the recurrent laryngeal nerve, and SVC obstruction.29 Several paraneoplastic syndromes are associated with thymic neuroendocrine neoplasms, the most common of which is Cushing syndrome that results in ectopic production of adrenocorticotropic hormone. Others such as acromegaly and syndrome of inappropriate antidiuretic hormone are uncommon, and carcinoid syndrome is rare.30,31
Role of MR Imaging
General Concepts and Protocol Optimization
A variety of MR imaging protocols are available to evaluate the mediastinum, its contents, and abnormalities such as thymic epithelial tumors. Several detailed MR imaging protocols for evaluation of the mediastinum have been described.32–34 Most effective protocols include T1-weighted, T2-weighted, T2-weighted fat-saturated, in-phase, and out-of-phase gradient echo (GRE), and pre- and post-gadolinium enhanced [obtained as 3-dimensional (3D) ultrafast GRE dynamic imaging if possible] sequences.32–34 Respiratory gating may be utilized, although breath hold imaging is generally preferred given its greater reliability in halting respiratory motion and preventing associated artifacts. For cardiac gating, electrocardiogram (ECG) gating or peripheral gating may be performed, the former of which is more reliable in the halting of cardiac motion and elimination of associated pulsatility artefacts.32–34 Other sequences such as diffusion-weighted imaging (DWI) and dynamic contrast-enhanced imaging (DCE) may be employed.
Chemical shift MR imaging may be used to distinguish between malignant thymic lesions such as thymic epithelial neoplasms from thymic hyperplasia and normal thymus, as the latter demonstrate loss of signal on out-of-phase sequences due to the suppression of microscopic fat interspersed between non-neoplastic thymic tissue, whereas the former do not (Fig. 1).35,36 The chemical shift ratio (CSR) can be used to evaluate signal loss and is defined as the following: (thymus SI OP/paraspinal muscle SI OP)/(thymus SI IP/paraspinal muscle SI IP), in which SI is signal intensity, IP indicates in-phase sequences, and OP denotes out-of-phase sequences. The signal loss expected with thymic hyperplasia and normal thymus can be measured with CSRs of 0.5 to 0.6. Thymic epithelial neoplasms, lymphoma, and other malignant lesions demonstrate higher CSRs of approximately 0.9 to 1.0.35,36 DWI and DCE MR sequences have shown promise in differentiating between various types of mediastinal masses.37–39
Imaging of Thymoma
On MR imaging, thymoma most commonly appears as a prevascular mediastinal mass with low to intermediate signal intensity on T1-weighted images and high signal intensity on T2-weighted images (Fig. 2).40,41 As the signal intensity of thymoma may be similar to that of fat on T2-weighted images, fat-saturation sequences may be employed. Cystic changes and necrosis result in low signal intensity on T1-weighted images and high signal intensity on T2-weighted images (Fig. 3). The MR imaging appearance of intralesional hemorrhage is variable and depends in large part on its age. Hemosiderin typically manifests as low signal intensity on T1-weighted and T2-weighted images, whereas acute or subacute hemorrhage may show high signal intensity on T1-weighted images. Intratumoral fibrous septa and nodules result in low signal intensity. Internal regions of calcification may be present and appear as foci of low signal intensity (Fig. 4).
Sakai et al37 assessed the ability of dynamic MR imaging to distinguish early-stage (stages I and II) thymomas and advanced-stage (stage III) thymomas. They showed that the mean peak time was delayed in the latter compared with the former.37 In addition, 92% of stage II, III, and IV thymomas showed heterogenous signal intensity and 50% demonstrated lobular internal features due to fibrous septa. All stage I thymomas showed heterogeneous signal intensity but none demonstrated lobulation.37 Two studies have investigated indirect signs of advanced disease on MR imaging, with thymic carcinomas more likely than thymomas to have features such as irregular contours, cystic or necrotic components, heterogeneous enhancement, and associated lymphadenopathy.42,43 One case report has described the superiority of whole body MR imaging in demonstrating metastatic disease compared with CT.44
Imaging of Thymic Carcinoma and Thymic Neuroendocrine Tumors
On MR imaging, thymic carcinoma and thymic neuroendocrine lesions manifest as prevascular mediastinal masses that are hyperintense to muscle on both T1- and T2- weighted images (Fig. 5).45 Cystic changes, necrosis, and hemorrhage may result in heterogeneous signal intensity (Fig. 6).46 Aggressive features such as lymphadenopathy and distant metastasis suggest thymic carcinoid or thymic carcinoma rather than thymoma (Fig. 7).45,46 Following the administration of IV contrast, thymic neuroendocrine tumors such as carcinoid may demonstrate hyperenhancement.
When MR imaging is performed for the staging of thymic epithelial neoplasms, the entire chest should be included. Specific structures such as the heart and pericardium, vessels, and pleura should be assessed for local spread of disease. Fluid-sensitive sequences can be performed to identify vascular structures and evaluate for tumor involvement, which is suggested by findings such as vessel distortion and visualization of intraluminal tumor. Cardiac MR imaging is the optimal imaging modality for evaluating the presence and extent of myocardial involvement. The myocardium can be evaluated with T1- or T2-weighted double inversion recovery sequences, and regions of abnormal signal intensity are suggestive of involvement.47 Internal regions of vascularity may be present on perfusion sequences and the use of cine MR imaging should be strongly considered.48
Identification of phrenic nerve invasion is important, as it indicates advanced disease and affects treatment planning, as patients will typically receive neoadjuvant chemotherapy. Multishot spiral sequences can be obtained to evaluate for paradoxical movement of the diaphragm.3 MR findings suggestive of chest wall invasion by lung cancer, mediastinal neoplasms such as thymic epithelial neoplasms, and other lesions have been described. Due to superior soft tissue contrast and spatial resolution, MR imaging is considered superior to CT in identifying chest wall invasion.49 Key findings include disruption of the extrapleural fat plane on T1-weighted sequences and high signal intensity of the parietal pleura and other structures on T2-weighted and STIR sequences.50,51 The use of IV contrast may be helpful. Cine MR imaging during breathing can demonstrate chest wall invasion, as attachment of the tumor to the chest wall can indicate involvement.52
TNM Staging System
A TNM classification system has recently been recognized by the AJCC and the UICC, the organizations responsible for defining stage classifications for neoplasms. IASLC and ITMIG evaluated a large retrospective database of thymic epithelial neoplasms to develop proposals for the eighth edition of the stage classification manuals. A Thymic Domain of the Staging and Prognostic Factors Committee (TD-SPFC) was established to formulate the rationale, methodology, and definitions of this classification system.3,8,9 The T, N, and M descriptors, and stage groups, are listed in Tables 1–4.
Tumor (T) Classification
Thymic epithelial neoplasms that are encapsulated and those that extend beyond the capsule into the adjacent perithymic fat are classified as T1 tumors.4 The T2 descriptor includes tumors that invade the pericardium (partial or full-thickness involvement). Thymic epithelial neoplasms involving nonvascular structures such as the lung, phrenic nerve, or chest wall, and vascular structures such as the brachiocephalic vein, SVC, and extrapericardial pulmonary arteries or pulmonary veins, are classified as T3 tumors. Finally, T4 neoplasms are those that involve the myocardium, intrapericardial pulmonary arteries, thoracic aorta, vessels of the transverse thoracic aorta (brachiocephalic, carotid, and subclavian arteries), trachea, and esophagus.
Lymph Node (N) Classification
The N classification is based on the presence and location of lymph node metastasis. The absence of lymph node involvement is classified as N0. The N1 and N2 descriptors represent lymph node metastases located in the anterior and deep compartments, respectively, which have been defined in the lymph node map created for use with thymic epithelial neoplasms.5,53 The analysis of the database demonstrated better survival of patients with N1 disease compared with N2 disease (5-year survival estimates of 69% and 47%, respectively). Distinguishing between anterior and deep lymph node metastasis is important to surgeons, as the former are typically resected as part of an extended thymectomy, whereas the latter are not, and evaluation of lymph nodes in this region requires more extensive surgery.53
Metastasis (M) Classification
The M classification is based on the presence and location of metastatic disease.4 The absence of metastatic disease is classified as M0. The M1 descriptor is divided into 2 components, M1a and M1b, based on the location of metastatic disease. M1a includes pleural and pericardial metastases, and M1b denotes pulmonary metastases and extrathoracic (or distant) metastatic disease. The overall death rate for patients with M1b disease was worse (45%) than for patients with M1a disease (31%).
Stage groups are constructed from combinations of individual TNM descriptors. Stages I, II, IIIA, and IIIB are based primarily on the T classification in patients with N0 and M0 disease. However, stages IVA and IVB are determined by the N or M classification.
The role of MR imaging for the characterization and staging of thymic epithelial neoplasms continues to expand. MR imaging effectively distinguishes thymic epithelial tumors and other malignant neoplasms from benign lesions in the prevascular mediastinum and can be used to characterize and stage thymic tumors in those patients with contraindications to contrast-enhanced CT. In addition, the excellent contrast resolution of MR imaging can enable appropriate staging based on the new TNM staging system crafted by IASLC and ITMIG.
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Keywords:Copyright © 2018 Wolters Kluwer Health, Inc. All rights reserved.
magnetic resonance imaging; thymic carcinoid; thymic carcinoma; thymoma