Ectopic thymoma: Retrospective analysis of eight cases with clinical features and computed tomography findings

Journal Pre-proof Ectopic thymoma: Retrospective analysis of eight cases with clinical features and computed tomography findings

Zhou Qing, Han Lei, Ke Xiaoai, Zhou Junlin PII:

S0899-7071(19)30233-5

DOI:

https://doi.org/10.1016/j.clinimag.2019.10.017

Reference:

JCT 8774

To appear in:

Clinical Imaging

Received date:

26 August 2019

Revised date:

30 October 2019

Accepted date:

31 October 2019

Please cite this article as: Z. Qing, H. Lei, K. Xiaoai, et al., Ectopic thymoma: Retrospective analysis of eight cases with clinical features and computed tomography findings, Clinical Imaging(2019), https://doi.org/10.1016/j.clinimag.2019.10.017

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© 2019 Published by Elsevier.

Journal Pre-proof Ectopic Thymoma: Retrospective analysis of eight cases with clinical features and Computed Tomography findings Zhou Qinga,b,c，Han Leia,b,c，Ke Xiaoaia,b,c，Zhou Junlina,c* a

Department of Radiology, Lanzhou University Second Hospital, Gansu, China

b

Second Clinical School，Lanzhou University, China

c

Key Laboratory of Medical Imaging of Gansu Province, China

Corresponding author at: Department of Radiology, Lanzhou University Second

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Hospital Corresponding author：Zhou Junlin

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Cuiyingmen No.82, Chengguan District, Lanzhou, 730030, PR China

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E-mail address: [email protected]

Journal Pre-proof ABSTRACT Objective：To analyze the computed tomography (CT) and clinical features of ectopic thymoma, and to be familiar with the CT diagnosis of this disease. Materials and Methods： CT data, clinical data, and pathological data of eight cases of ectopic thymoma, confirmed by pathology from September 2013 to June 2019, were retrospectively analyzed. Results：Eight cases of thymoma were diagnosed, which included three in

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mediastinum (one of B1 type, two of C type), two in pericardium (both of B3 type), one in lung (B1 type), one in pleura (AB type), and one in right atrium (B2 type).

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Among the eight cases, four were men and four were women, aged 36–70 years. The

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clinical manifestations were chest tightness, shortness of breath and cough, and one case of myasthenia gravis. Six of the 8 patients were misdiagnosed as lymphoma,

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solitary fibrous tumor, malignant teratoma by CT. CT showed the following: the long

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diameter of tumor was 4.2 cm-19.5 cm, the shape was elliptical or round, and one case of ectopic thymoma grew in the atrium. The density was homogeneous in two

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cases and heterogeneous in six cases. The boundary was clear in three cases and unclear in five cases. Among the eight cases, three showed pleural effusion, two

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showed pericardial effusion and three showed calcification. Conclusions：Ectopic thymoma is rare and often misdiagnosed due to abnormal position. However, CT findings of ectopic thymoma are similar to those of the anterior superior mediastinal thymoma.

Keywords: ectopic thymoma; CT manifestation; clinical

1. Introduction During embryonic development, the thymus originates from the third and fourth

Journal Pre-proof pharyngeal ventral epithelium and gradually moves to the anterior mediastinum [1]. Therefore, 96% of the thymic epithelial tumors occur in the anterior superior mediastinum. Non-anterior superior mediastinal thymoma is called ectopic thymoma. Ectopic thymoma is rare, accounting for only 2–4% of total thymoma [2]. Ectopic thymoma is thought to originate from the thymus tissue displaced during thymus development [3]. Another hypothesis is that ectopic thymoma originates from stem cells [4]. According to the reports in literature, ectopic thymoma is found in the neck, lung, pleura, thyroid, pericardium, and posterior mediastinum [5]. It is often

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misdiagnosed due to abnormal position, which brings confusion to clinical diagnosis

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and treatment; so, doctors and radiologists need to have an understanding of ectopic

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thymoma.

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2. Materials and methods

2.1 Patients

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Retrospective study, informed consent was waived.

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Eight patients (four men and four women, aged 36–70 years) with a pathological diagnosis of non-anterior superior mediastinal thymoma between September 2013 and June 2019 were enrolled. All patients underwent chest CT flat scanning. Five patients underwent CT-enhanced examinations at the same time, two patients underwent CT angiography (CTA) examination, and one of them underwent ultrasound examination. CT findings and clinical manifestations of the patients were recorded. 2.2 CT scan Unenhanced CT : The multi-detector row CT (MDCT) systems (Discovery CT 750 HD, GE Healthcare, Waukesha, WI, USA or Sensation 64, Siemens, Germany) was used for routine plain scan. The patient was placed in the supine position, while the prone position was used for dyspnea. The scan ranged from the tip of the lung to the base of the lung. Scanning parameters: The acquisition parameters are as follows: 120

Journal Pre-proof kV; 160mAs; 0.6-or 0.4-second rotation time; detector collimation, 64×0.625 mm ; field of view, 500×500mm or 350×350 mm; matrix, 512×512.Image thickness is 0.625mm. Dual-phase enhanced scan:The contrast agent with iodulol was injected at the flow rate of 3-4 ml/s with a pump injector (Ulrich Medical, Ulm, Germany)at the dose of 1.0 mL/kg through the anterior elbow into the vein. The thoracic aorta monitoring trigger threshold was 80 HU.Arterial and venous-phase contrast-enhanced CT were performed after delays of 18s and 45s following intravenous administration (Ultravist

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370, Baye Schering Pharma, Berlin, Germany). Contrast-enhanced CT was

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reconstructed with a reconstruction thickness of 1.25 mm.

Chest CTA: The contrast agent with iodulol was injected at the flow rate of 5-5.5 ml/s

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with a pump injector (Ulrich Medical, Ulm, Germany)at the dose of 1.0 mL/kg

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through the anterior elbow into the vein. The thoracic aorta monitoring trigger

intravenous administration.

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2.3 Image analysis

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threshold was 150 HU.CT angiography were performed after delays of 5s following

Two radiologists with more than seven years of CT diagnostic experience analyzed

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the images separately. They recorded the location, maximum diameter, border, and calcification of the tumor; and whether the tumor was accompanied by pleural effusion and pericardial effusion. CT noncontrast-enhanced scan and contrast enhanced arterial phase and venous phase CT values were measured. In case the two opinions were not uniform, the radiologists discussed and analyzed the data, and drew a unified opinion. CT images were evaluated for the following: (1) tumor size, wherein the horizontal axis of the CT scan was measured to define the maximum diameter of the lesion; (2) the degree of enhancement, wherein, the difference between the CT value of the scanning arterial phase tumor and the unenhanced

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value (ΔCT value) was calculated. The ΔCT value <20 HU implied that the image is mildly enhanced, 20-40 HU implied moderately enhanced, and >40 HU marked enhanced.

Journal Pre-proof 2.4 Pathology All the patients underwent surgery. Total tumor resection was performed, and pathological sections of tumor specimens were prepared for Hematoxylin and Eosin staining, and immunohistochemical staining. The images were analyzed by the pathologists with more than five years of work experience. Taking into consideration the criteria of World Health Organization (2015), the tumors were classified into A type, AB type, B1 type, B2 type, B3 type, and C type according to the morphology of

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tumor cells, and the proportion of tumor cells and lymphocytes.

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3. Results

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3.1 Clinical features

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The youngest among the eight patients was 36 years old, and the oldest was 70 years old. Among the eight patients, four were men and four women. The clinical symptoms

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reported were chest tightness, shortness of breath, and cough at different times. One case of medullary thymoma with severe myasthenia gravis was diagnosed. The

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pathological results showed that among the eight patients, there were two cases each of B1 type, B3 type, and C type, one case each of AB type and B2 type (Table A). 3.2 CT image features

3.2.1 Middle Mediastinal ectopic thymoma Three cases of middle mediastinal thymoma were diagnosed in this study (Fig. A.1). They underwent contrast enhanced chest CT.CT transverse axis showed maximum tumor diameter of 4.7-9.8 cm. One patient showed punctate calcification in the tumor, while one patient showed pericardial effusion. The tumor boundaries in these patients were unclear. Two cases of tumor invasion in the superior vena cava were observed. Contrast enhanced CT showed defect in the superior vena cava (Fig. A.2). Two patients who underwent Contrast enhanced CT showed mild enhancement

Journal Pre-proof of their arterial phase. Two of the three patients were misdiagnosed for lymphoma. 3.2.2 Pericardial thymoma In this study, No other aggressive malignant tumors were seen in the anterior mediastinum, and during the surgery, the base of the tumor was located in the pericardium.One patient underwent contrast enhanced CT, and the other patient underwent Chest CTA. The CT images showed the maximum diameter of the tumor to be 6.4 cm and 12.6 cm, respectively. The tumor density was heterogeneous. Both the

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patients had pleural effusion and pericardial effusion, while typical annular

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calcification was seen in one patient's tumor mass (Fig. B.1). The mass significantly

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compressed the heart and large blood vessels (Fig. B.2). Contrast enhanced CT of another patient showed a mild enhancement of the tumor arterial phase. Pre-operative

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images of ectopic thymoma with annular calcification were misdiagnosed as

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malignant teratomas.

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3.2.3 Lung and Thoracic ectopic thymoma In this study, one patient with pulmonary ectopic thymoma and one patient with

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thoracic thymoma were enrolled. The lung ectopic thymoma showed a small, well-defined round-like mass with a maximum diameter of 4.2 cm and uniform density (Fig. C.1;C.2). The mass showed moderate enhancement on arterial phase. The ectopic thymoma in the thoracic cavity was larger. The DR showed mass in the right side of heart (Fig. D.1), and the maximum tumor diameter was 19.5 cm on the CT image. Spotted calcification could be observed in the mass, and the edge of the mass was clear and sharp. The mass had pressed the right lung tissue (Fig. D.2;D.3). The contrast enhanced CT scan showed mass to be slightly enhanced. Pre-operative images of giant ectopic thymoma in the thoracic cavity were misdiagnosed as solitary fibrous tumors. 3.2.4 Cardiac ectopic thymoma Imaging diagnosis of cardiac ectopic thymoma is extremely easy to misdiagnose.

Journal Pre-proof In this study, patient with cardiac ectopic thymoma underwent Chest CTA and ultrasonography before surgery. The patient showed a rounded mass in the right atrium with a diameter of 7.0 cm. Ultrasound analysis described it as a right atrial solid mass (Fig. E.4). The CTA showed a poor filling of the right atrium, a pleural effusion in the right thoracic cavity (Fig. E.1;E.2), and low-density emboli formation in the superior vena cava (Fig. E.3). During the surgery, the pedicle of the right atrium mass was located at the entrance of the right atrium. The absence of malignant

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was confirmed to be a type B2 thymoma (Fig. E.5).

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thymoma in the mediastinum was also confirmed during the surgery. The pathology

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4. Discussion

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During embryonic development, thymus tissue originates from the third or fourth

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pharyngeal sac, and then gradually shifts downward to the anterior superior mediastinum. It continues to develop after birth and gradually subsides after

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adulthood, and is replaced by fibrous adipose tissue [1,6]. Therefore, 96% of thymoma occurs in the anterior superior mediastinum. The non-anterior superior

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mediastinal thymoma is called as ectopic thymoma, which accounts for only 4% of the thymoma [2,7]. The occurrence of thymoma is more common in the elderly. The peak age of onset is about 50-60 years, with no gender differences [8]. About one-third cases of thymoma are associated with myasthenia gravis, but ectopic thymoma is rarely associated with myasthenia gravis [9,10]. Histologically, the thymus has two regions: a lymphocyte-rich cortex and a medulla composed of epithelial cells. Based on the morphology of the epithelial cells and the proportional relationship between these lymphocytes and epithelial cells, the thymoma is divided into A type, AB Type, B1 type, B2 type, B3 type, and C type. Chest CT examination is the preferred imaging method for thymoma, which can show the location, size, shape, density, and relationship with surrounding tissues by enhancement [11,12]. The origin of ectopic thymoma is widely believed to be the thymus tissue

Journal Pre-proof remaining during embryonic development. If the thymus tissue remains in a certain part or a small part of the thymus tissue remains during the forward mediastinal shift, it may develop into a thymus tumor [3]. Several histological studies of patients with myasthenia gravis have also shown that thymus tissue is not only widely distributed in the anterior mediastinum but is also widely distributed in other parts of the surroundings, such as the hilar [13]. Another hypothesis is that thymoma is derived from stem cells, which are pluripotent cells that can differentiate into a variety of cells. This theory explains the occurrence of distant ectopic thymoma in the lungs and other

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mediastinums [4]. According to reports in the literature, ectopic thymoma occurs most

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often in the neck [14], followed by the lungs, pleura, thyroid, pericardium, and posterior mediastinum [5]. However, rare sites other than the thymus tissue

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development pathway, such as the thoracic vertebrae and heart, have also been

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reported [15,16]. The current study identified eight cases of ectopic thymoma,

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including three cases of middle mediastinal thymoma, two cases of pericardial thymoma, one case of pulmonary ectopic thymoma, one case of thoracic ectopic

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thymoma, and one case of extremely rare atrial ectopic thymoma. The middle mediastinal ectopic thymoma is currently reported in less than twenty

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cases. According to the previous report on mediastinal ectopic thymoma, the average age of onset was 59.2 years, with no significant difference in gender. There were no obvious clinical symptoms, the tumor size was 5.2 cm, and all middle mediastinal ectopic thymoma were located on the right side of the trachea [17]. In the current study, three patients were diagnosed with middle mediastinal thymoma. Their median age was 64 years. One patient had myasthenia gravis. The tumor diameter was 4.7-9.8 cm. Unlike the literature report, tumor in one patient was located on the left side of the trachea, close to the left pulmonary artery. CT findings of the chest of three patients showed heterogeneous mass density with punctate calcification in the tumor of one patient. The boundary of the tumor was unclear. All the three cases were invasive, with pericardial effusion. Two patients showed embolus in the superior vena cava around the mass. Ectopic thymoma of the middle mediastinum is extremely easy

Journal Pre-proof to be misdiagnosed as malignant lymphoma. Lymphoma with multiple lymph nodes in other parts of the mediastinum. This can be used to identify middle mediastinal ectopic thymoma.The differential diagnosis can be confirmed by histology and immunohistochemistry. Owing to its abnormal location, middle mediastinal ectopic thymoma is difficult to diagnose and treat surgically. Though the middle mediastinal thymoma may be invasive, it needs to be completely removed [18,19]. Pericardial thymoma is extremely rare, and the clinical symptoms of ectopic

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thymoma in the pericardium are obvious. In addition, there are obvious complications, such as pericarditis, pericardial effusion, and pericardial tamponade. The average age

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of onset reported is 60.9 years old [20]. The two patients with pericardial ectopic

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thymoma we identified in the current study were 36 years old and 43 years old. They were younger than the reported pericardial thymoma patient was. The chest CT

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showed the diameters of the tumors to be 12.6 cm and 6.4 cm. Both patients showed

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pericardial effusion, while one of the patients showed typical annular calcification in tumor. If the mass is large, it can compress the heart and surrounding large blood

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vessels, and even invade the surrounding blood vessels. Pericardial thymoma is often misdiagnosed as malignant teratoma due to heterogeneous density of the mass and

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calcification.However, in addition to calcification, teratomas usually contain fat, bone, water and soft tissue density. This can be distinguished from pericardial thymoma. In addition, it also needs to be differentiated from lymphoma [21]. Besides solid density and uneven lumps, pericardial thymoma can also be expressed as cystic mass [22]. Ectopic thymoma of the lung and pleura is the most common ectopic site in addition to cervical ectopic thymoma [5]. Previous report in literature has reported that the primary thymoma of the lung occurred at about 50 years of age. The mass was small, about 3.0-3.5 cm in diameter, and the density was homogeneous.Primary thymoma of the lung in most patients was located in the right lung. The upper lobe was more common site [23,24]. In the present study, the age of the patient was 62 years and the clinical symptom was cough. The mass was located in the upper lobe of the left lung, with a diameter of 4.2 cm, uniform density, clear border, and moderate

Journal Pre-proof enhancement after CT enhancement of the mass. The ectopic pleural and intrathoracic ectopic thymoma masses are generally larger, and misdiagnosed as solitary fibrous tumors [3,25-26]. The average age of onset of pleural ectopic thymoma is about 52 years, with more prevalence in men [27]. The thoracic ectopic thymoma in the current study was very large with a diameter of 19.5 cm. CT image showed compression of the right lung and right pulmonary artery, and calcification was observed in the mass, which showed slight enhancement after contrast enhancement. The case was misdiagnosed as solitary fibrous tumor. However, Isolated fibroid tumors showed

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significant heterogeneous enhancement on contrast-enhanced CT, and vascular

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differentiated by CT-guided thoracic biopsy [3].

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shadows were visible in the tumor,thymoma and solitary fibroma may be

Primary cardiac tumors are rare. They are usually benign and occur with

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myxomas. The diagnosis of cardiac ectopic thymoma is challenging. At present, only

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one case of ectopic thymoma in the heart has been reported [16], thymoma appears in cardiac myxoma, which is considered to be tumor transformation of thymus tissue to

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myxoma. The cardiac thymoma in the current study was located in the right atrium. Chest CTA showed a solid mass in the right atrium and a filling defect in the superior

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vena cava. The diameter of the mass was 7.0 cm. During the surgery, it was observed that the right atrial mass was pedicled, and the pedicle was located at the entrance of the right atrium. No malignant tumors in the mediastinum and other parts were observed, which ruled out the possibility of metastasis. Histopathology and immunohistochemical diagnosis of right atrium suggested the thymoma to be of B2 type. We speculate that right atrial ectopic thymoma may be derived from stem cells, or the mediastinal thymus tissue that is invisible to the naked eye, which migrates into the superior vena cava and the right atrium, and develops into a thymoma. In conclusion, although ectopic thymoma is rare, we must have some knowledge of it. According to the literature reports and the cases we identified, the age of ectopic thymoma is consistent with the anterior superior mediastinal thymoma, with peak incidence in 50-60 years old. There is no gender difference and no characteristic

Journal Pre-proof clinical symptoms. It is worth noting that ectopic thymoma is rarely associated with myasthenia gravis. The CT findings of ectopic thymoma have certain characteristics. The ectopic thymoma in the lung is generally small, the edge is smooth, and the density is uniform. It needs to be differentiated from benign tumors in the lung. Pleural ectopic thymoma is generally large in volume, and it often presses lung tissue and pulmonary blood vessels and needs to be differentiated from solitary fibrous tumors. The mediastinum and pericardial ectopic thymoma are generally invasive, with pericardial effusion, and intravenous embolus formation, and need to be

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differentiated from lymphoma, malignant teratoma and metastatic tumor. In addition,

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when a neck and a thyroid mass are found, the ectopic thymoma should be

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considered. References

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[1] Suster S, Rosai J. Thymus. In: Sternberg SS, ed. Histology for pathologists. 2 nd ed,

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Philadelphia, PA: Lippincott-Raven Publishers, 1997: 687-706. [2] Detterbeck FC, Parsons AM: Thymic tumors. Ann Thorac Surg 2004,77:1860-69.

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[3] Filosso P L , Delsedime L , Cristofori R C , et al. Ectopic pleural thymoma mimicking a giant solitary fibrous tumour of the pleura[J]. Interactive CardioVascular and Thoracic Surgery, 2012,

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15(5):930-932.

[4] Marchevsky A M .Lung tumors derived from ectopic tissues.[J]. Seminars in Diagnostic Pathology, 1995, 12(2):172.

[5] Weissferdt A , Moran C A . The spectrum of ectopic thymomas[J]. Virchows Archiv, 2016, 469(3):245-254.

[6] Riedel RF, Burfeind WR: Thymoma: Benign appearance, malignant potential. Oncologist 2006, 11:887-894. [7] Venuta F, Anile M, Diso D, Vitolo D, Rendina EA, de Giacomo T et al.Thymoma and thymic carcinoma. Eur J Cardiothorac Surg 2010;37:13–25. [8] Juanpere S , Noemí Ca?ete, Ortu?O P , et al. A diagnostic approach to the mediastinal masses[J]. Insights into Imaging, 2013, 4(1):29-52. [9] Engels, Eric A . Epidemiology of Thymoma and Associated Malignancies[J]. Journal of Thoracic Oncology, 2010, 5(10):S260-S265.

Journal Pre-proof [10] Vincent A , Palace J , Hiltonjones D . Myasthenia gravis.[J]. Practitioner, 2011, 2011(9274):2122-2128. [11] Takahashi K , Al-Janabi N J . Computed tomography and magnetic resonance imaging of mediastinal tumors[J]. Journal of magnetic resonance imaging : JMRI, 2010, 32(6):1325-1339. [12] Maher M M, Shepard J A O. Imaging of thymoma[J]. Semin Thorac Cardiovasc Surg, 2005, 17(1):12-19. [13] Ashour M . Prevalence of ectopic thymic tissue in myasthenia gravis and its clinical significance[J]. Journal of Thoracic and Cardiovascular Surgery, 1995, 109(4):632-635.

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[14] Park H O , Kim S H , Moon S H , et al. Ectopic Cervical Thymoma: A Case Report and

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Review[J]. The Korean journal of thoracic and cardiovascular surgery, 2017, 50(4):312. [15] Marandino F , Zoccali C , Salducca N , et al. Ectopic primary type A thymoma located in two

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thoracic vertebras: a case report[J]. BMC Cancer, 2010, 10(1):322-0. [16] Miller D V , Tazelaar H D , Handy J R , et al. Thymoma Arising Within Cardiac Myxoma[J].

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The American Journal of Surgical Pathology, 2005, 29(9):1208-1213.

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[17] Yajima T , Mogi A , Shimizu K , et al. Ectopic thymoma in the paratracheal region of the middle mediastinum: a rare case report and literature review[J]. BMC Research Notes, 2018,

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11(1):256.

[18] Oliveira K F D , Rodrigues M M , Lopes G P , et al. Massive thymoma of the mid-posterior 49(6):403-405.

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mediastinum: an unprecedented case in a young adult[J]. Radiologia Brasileira, 2016,

[19] Nakamura H , Adachi Y , Fujioka S , et al. Thoracoscopic Resection of Middle Mediastinal Noninvasive Thymoma: Report of a Case[J]. Surgery Today, 2007, 37(9):787-789. [20] Arai H , Rino Y , Fushimi K , et al. Pericardial ectopic thymoma presenting with cardiac tamponade: report of a case[J]. Surgery Today, 2015, 45(9):1200-1204. [21] Azoulay S, Camilo Adem, Michel Gatineau, et al. Pericardial ectopic thymoma[J]. Virchows Archiv, 2005, 446(2):185-188. [22] Caramori G , Calia N , Pasquini C , et al. Ectopic thymoma simulating a pericardial cyst[J]. Monaldi archives for chest disease , 2005, 63(4). [23] Myers P O , Kritikos N , Bongiovanni M , et al. Primary intrapulmonary thymoma: A systematic review[J]. Eur J Surg Oncol, 2007, 33(10):0-1141. [24] Gong L , Li YH , He XL , et al. Primary intrapulmonary thymomas: case report and review of

Journal Pre-proof the literature.[J]. Journal of International Medical Research, 2009, 37(4):1252-1257. [25] Kitada M , Sato K , Matsuda Y , et al. Ectopic thymoma presenting as a giant intrathoracic tumor: A case report[J]. World Journal of Surgical Oncology, 2011, 9(1):66. [26] Alexiev B A , Yeldandi A V . Ectopic pleural thymoma in a 49-year-old woman: A case report[J]. Pathology - Research and Practice, 2016:S0344033816301911. [27] Attanoos R L , Galateausalle F , Gibbs A R , et al. Primary thymic epithelial tumours of the

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pleura mimicking malignant mesothelioma.[J]. Histopathology, 2010, 41(1):42-49.

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Table A: Clinical features of 8 cases of ectopic thymoma Gende r

Age

Clinical symptoms

Tumor location

WHO pathological classification

1

F

64

Myasthenia gravis

Mediastinum

Type B1

2

M

69

Dry cough for 10 days

Mediastinum

Type C

3

M

59

Chest tightness and shortness

Mediastinum

Type C

of breath M

36

Chest tightness and shortness

Pericardium

Type B3

Pericardium

Type B3

Chest tightness and shortness

Type AB

of breath

cavity

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4

43

Chest tightness, shortness of

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F

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of breath 5

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Case

7

F

8

F

47

62

Thoracic

Cough

Lung

Type B1

Chest tightness, shortness of

Right atrium

Type B2

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M

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6

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breath, cough

70

breath, dizziness

Journal Pre-proof Highlights 1. Our search found that atrial ectopic thymoma has not been reported, and our report may be the world's first. 2. Ectopic thymoma is generally reported as a case. We collected 8 cases of ectopic thymoma at various sites, reviewed the literature, and described its epidemiology and

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CT findings.

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