|Ahead of print
|Retrospective histopathology audit of thymectomy specimens: A clinicopathological study of 303 cases spanning the non-neoplastic, benign and malignant spectrum
Neha Bakshi1, Shashi Dhawan2, Seema Rao2, Arvind Kumar3
1 Department of Pathology, Sir Ganga Ram Hospital, Rajender Nagar, New Delhi, India
2 Department of Histopathology, Sir Ganga Ram Hospital, Rajender Nagar, New Delhi, India
3 Department of Thoracic Surgery, Sir Ganga Ram Hospital, Rajender Nagar, New Delhi, India
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|Date of Submission||05-Apr-2021|
|Date of Decision||30-Jan-2022|
|Date of Acceptance||31-Jan-2022|
|Date of Web Publication||24-May-2022|
| Abstract|| |
Aims: Thymectomy specimens are uncommon in routine histopathology practice. However, awareness of various pathologic entities and definite reporting of these specimens is paramount to optimal patient management. Our objective was to determine the histomorphologic spectrum of thymectomy specimens spanning the non-neoplastic, benign to malignant spectrum. Methods and Results: Thymectomies received over an 8-year period were retrospectively analyzed by reviewing clinical details and histologic findings in detail, incorporating the latest World Health Organization (WHO) 2015 histologic classification. A total of 303 thymectomy specimens (179 males/124 females, mean age 45.3 years [3–84 years]) were included. Around 51.2% (n = 155) patients had associated myasthenia gravis (MG), while 17.5% (n = 53) had incidentally detected anterior mediastinal mass (AMM). Non-neoplastic and benign pathologies comprised 31% (n = 94) cases and showed stronger association with MG (P = 0.009). Thymic follicular hyperplasia (TFH) was the commonest non-neoplastic pathology (n = 32), while the benign tumor group included thymic hemangioma/lymphangioma, thymolipoma, and ectopic parathyroid adenoma. Thymic epithelial tumors (TETs) comprised 64.7% cases, with majority being thymomas (185/303; 61.1%). Thymoma type B2 was the commonest histologic subtype and Stage I/T1 was the most frequent stage. Type A and AB thymomas affected older patients (P = 0.005) and were in lower stage (both Masaoka and American Joint Committee on Cancer [AJCC]) than type B thymomas (P = 0.007). No significant association between MG and thymoma subtype, patient sex or Masaoka stage was seen (P > 0.05). Thymic carcinomas comprised 11 cases and showed no association with MG (0/11, P < 0.001); squamous cell carcinoma was the commonest histologic type (8/11; 72.7%). Conclusion: TETs are the commonest thymic lesions; however, a diverse spectrum of pathologic processes can affect the thymus.
Keywords: Disease spectrum, histomorphology, thymectomy, thymoma, Thymic epithelial tumors, WHO 2015 classification
|How to cite this URL:|
Bakshi N, Dhawan S, Rao S, Kumar A. Retrospective histopathology audit of thymectomy specimens: A clinicopathological study of 303 cases spanning the non-neoplastic, benign and malignant spectrum. Indian J Pathol Microbiol [Epub ahead of print] [cited 2022 Jul 4]. Available from: https://www.ijpmonline.org/preprintarticle.asp?id=345867
| Introduction|| |
Thymectomy is an uncommon specimen in routine histopathology practice. Embryologic origin of the thymus from elements of two different germ cell layers potentiates differentiation across diverse neoplastic cell lines, complicating the histologic picture further. Nevertheless, awareness of various types of lesions involving the thymus is vital, given their diverse behavioral spectrum ranging from entirely benign to highly aggressive and even lethal.,, Thymic epithelial tumors (TETs), which include thymoma and thymic carcinoma, are a heterogeneous group of lesions with a wide spectrum of morphologic appearances that makes histologic classification difficult. Further, the 2015 World Health Organization (WHO) classification has refined the histological and mmunohistochemistry (IHC) diagnostic criteria for more reproducible subtyping of thymomas and for better distinction between thymoma and thymic carcinoma., Most comprehensive studies on thymus thus far have focused on TETs, with the gamut of benign and non-neoplastic lesions remaining largely unexplored. We retrospectively audited all thymectomy specimens received over an 8-year period with an aim to assess the spectrum of benign, malignant, and non-neoplastic lesions involving thymus. To our knowledge, no such study which explores the entire disease spectrum of this dynamic organ has been attempted before.
| Materials and Methods|| |
All surgically resected thymectomy specimens (January 2012 to December 2019) were retrospectively included. Resections labeled as “meditational mass” with no residual thymic tissue on microscopy, lesions arising from the pleura, pericardium, or chest wall structures and incision biopsies from thymic lesions were excluded. In our institute, all mediastinal masses are biopsied and patients with a diagnosis of germ cell tumor (GCT) or lymphoma are treated with chemotherapy rather than excision surgery. Therefore this group of tumors did not form a major part of this study. Detailed histopathologic review of hemotoxylin and eosin (H&E) stained sections was done with IHC support wherever indicated; all TETs were reclassified according to 2015 WHO classification and staged using Modified Mosaoka Koga or AJCC (eighth edition) staging system. For thymomas with mixed histology, the predominant morphology was used to define thymoma subtype for data analysis. Relevant clinical data was recorded in each case from the hospital records. Due clearance of the study protocol was obtained from the hospital ethics committee prior to commencement. Data analysis was done using IBM SPSS v20.0 software package (SPSS Inc., Chicago, Illinois, USA) statistical software. P value of <0.05 was considered to indicate a statistically significant difference. For thymoma related statistical analyses, WHO types A and AB; and types B1, B2, and B3 were grouped as two separate categories and compared.
| Results|| |
A total of 303 surgically resected thymectomy specimens (179 males/124 females, M:F ratio – 1.4:1; mean age 45.3 years (3–84 years; 15 children/288 adults) were included. Clinical profile of the patients was diverse and is detailed in [Table 1]. More than half the patients (n = 155; 51.2%) had associated myasthenia gravis (MG). Patients with MG were significantly younger (mean age 41.8 ± 15.2 years vs 49 ± 17.3 years; P < 0.001); there was no associationof MG with gender. Significant proportion of patients (n = 55, 18.2%) were asymptomatic or presented with unrelated symptoms and an anterior mediastinal mass (AMM) was detected incidentally on chest imaging. Shortness of breast, chest pain, or discomfort and persistent cough were other common presenting symptoms. Patients' sex and lesion size had no association with histologic diagnosis. However, patients with non-neoplastic and benign lesions showed stronger association with MG (P = 0.009) and were significantly younger (36.5 ± 16 years) than those with TETs and other malignant lesions (49.3 ± 15.4 years) [P < 0.001].
|Table 1: Clinicopathological characteristics of the study population (n=303)|
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MICROSCOPIC FINDINGS: Broad gamut of morphological features spanning normal to benign to malignant spectrum was encountered. Majority lesions (n = 219; 72.3%) were neoplastic in nature while the rest (n = 84; 27.7%) were non neoplastic.
NON-NEOPLASTIC LESIONS: Eighty four (27.7%) cases revealed non-neoplastic thymic lesions [Table 2]. This group included 19 cases with histologically normal resected thymus which were categorized as “normal thymus” or “true thymic hyperplasia (TTH)” depending upon the gross weight of the thymectomy specimen. Grossly normal/enlarged thymectomy cases which showed prominent secondary lymphoid follicles with reactive germinal centers on microscopy were labeled as “thymic follicular (lymphoid) hyperplasia” (TFH) [Figure 1]a, [Figure 1]b, [Figure 1]c. Cases with lymphocytic depletion and adipocytic infiltration of the parenchyma were diagnosed as “thymic involution”. Thymic cysts were further subtyped into “unilocular” or “multilocular” [Figure 1]d, [Figure 1]e, [Figure 1]f. In this group, normal resected thymus (9/9; 100%) and TFH (26/32; 81.3%) showed strongest association with MG followed by cases with thymic involution (16/20; 80%), TTH (5/10; 50%), and thymic cysts (4/13; 30.8%), respectively.
|Figure 1: (a) Enlarged thymus with vague nodularity but no well-defined mass lesion; (b) Low power view revealing hyperplastic thymic tissue with prominent lymphoid follicles [HE, 4x]; (c)High power view highlighting prominent secondary lymphoid follicles with reactive germinal centers [HE; 20x]; (d) Thymectomy specimen showing multilocular cysts with ulcerated inner lining and tan brown hemorrhagic luminal content; (e and f) Ulcerated to cuboidal cyst lining with dense lympho-plasmacytic inflammation in the cyst wall. Thymic tissue is seen at the periphery [HE; 4x, 20x]|
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Thymic epithelial tumors (TETs)
Thymomas: Thymomas comprised majority of the TETs in our study (n = 185, 61.1%). Male preponderance was seen (men 115; M:F – 1.6:1; mean age 50.1 years [13–84 years]). Clinically, 53% (98/185) patients presented with features of a paraneoplastic syndrome (PNS); of which majority (91; 49.2%) had MG; two each had inflammatory bowel disease (IBD), pure red cell aplasia (PRCA), and systemic lupus erythematosus (SLE), respectively, and one patient had autoimmune hemolytic anemia (AIHA). Majority tumors were located in mediastinum (n = 183); while two cases showed ectopic thymoma in the neck. WHO type B2 was the most common histomorphologic type (n = 77; 41.6%) followed by type AB (n = 44; 24.2%), type B1 (n = 26; 14.1%), type B3 (n = 19; 10.3%), and type A (n = 16; 8.6%). Two type A thymomas which showed increased mitosis and nuclear atypia were reclassified as atypical type A. Twenty four cases (13%) showed mixed histology with one predominant WHO type co-existing with minor component of other type. These included predominant type B2 with minor B3 component (n = 13) or vice versa (n = 3) and predominant B1 admixed with minor B2 component (n = 7). Three cases were reported as ”micronodular thymoma with lymphoid stroma (MTLS)” (2%), one of which showed unique combination of type B2 thymoma with minor component of MTLS and one was associated with thymic cyst. One case of “Metaplastic thymoma” (0.6%) was encountered. One patient had a grossly purely unilocular cyst, with a microthymoma (type B2) identified in the cyst wall on microscopic examination. Two cases of ectopic thymoma in the neck were both WHO type AB.
Patients with type A and AB thymomas were significantly older (mean age: 54.1 ± 14.5 years) than those with type B [mean age: 47.7 ± 14 years] thymomas (P = 0.005). Patient sex had no association with histomorphologic subtype. Higher prevalence of MG was seen in type B thymomas (67/122; 55%) than in type A and AB thymomas (24/60; 40%); however this association was not statistically significant (P = 0.06). [Table 3] and [Table 4] depict the details of patients with various thymoma subtypes.
|Table 4: Comparative clinicopathological profile in the two thymoma groups (n=182*)|
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Thymoma stage and its correlation with clinicopathological parameters
Modified Masaoka Koga (MMK) and AJCC stage were determined for all cases. About 88 cases (47.6%) were MMK stage I disease, while stage II, III, and IV diseases were seen in 52 (28.1%), 34 (18.4%), and 11 (5.9%) cases, respectively. Majority of type A and AB were in stage I [62.5% and 70.5%, respectively] whereas majority (63.1%) of type B thymomas were in higher stage (stage II and above). The association of type A and AB thymomas with lower MMK stage was statistically significant (P < 0.001). Patients with stage I disease had significantly smaller tumors (6.1 ± 2.8 cm) than those with higher stage (II, III, and IV) disease (7.5 ± 3.1 cm) [P = 0.002]. Patients' sex, age, and presence of MG had no significant association with MMK stage (P > 0.05). [Table 5] elucidates the association of various clinical factors with MMK stage. As per AJCC stage, majority tumors were stage T1 [n = 146; 78.9%], while stages T2, T3, and T4 comprised 11, 24 and 4 cases, respectively. Majority of group A (type A and AB) thymomas were AJCC stage T1 (95%), whereas fair percentage (28.7%) of type B thymomas were AJCC stage T2 or above. The association of type A and AB thymomas with lower AJCC stage was statistically significant (P =0.002). Comparison of MMK and AJCC stage showed that the proportion of patient with early stage (T1 vs MMK I) disease increased remarkably [79% vs 47.6%], whereas the distribution of advanced stages (T3, T4 vs MMK III/IV) did not change considerably (15.2% vs 24.3%).
|Table 5: Various parameters influencing Masaoka Koga stage of thymomas (n=185)|
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THYMIC CARCINOMAS: Eleven patients (3.6%) had thymic carcinoma [28–78 years (mean age: 56.2 years); M: F ratio 1.2:1]. Cough, breathlessness, and chest pain were the common presenting symptoms. Strong negative association with MG was seen (0/11; P = 0.001). None of the patients had previous thymoma. Three patients had received neoadjuvant chemotherapy (NACT) prior to surgery. Microscopically organotypic features were distinctly absent in all cases. Thymic squamous cell carcinoma (TSQCC) was the most common histomorphologic type, accounting for eight (72.7%) cases. A spectrum of differentiation from well to moderate to poor was seen with evidence of keratinization present in three (27.3%) cases. Adenocarcinoma accounted for two cases (18.1%). One post NACT case showed poor differentiation and extensive chemotherapy-related changes eluding further histologic subtyping (9%). Majority of the tumors were AJCC stage pT3 (5/11) followed by pT4 (3/11), pT2 (1/11), and pT1 (2/11). Immunohistochemically, CD5 immunoreactivity was seen in 72.7% (8/11) cases; staining was diffuse and intense in majority of cases (6/8; 75%), while two (25%) cases showed weak and patchy CD5 expression. CD117 was positive in 63.6% (7/11) cases. Either p63 or p40 were positive in 77.8% (7/9) cases where they were done.
THYMIC NEUROENDOCRINE TUMORS: e cases (1%) of thymic neuroendocrine tumor (NET) were encountered, including one case of intermediate grade NET/atypical carcinoid and two cases of thymic large cell neuroendocrine carcinoma (LCNEC). The tumors displayed histologic features similar to their non-thymic counterparts. Extra thymic origin (particularly pulmonary origin) was ruled out in each case through careful correlation with clinical findings and imaging results.
Other mediastinal tumors
[Table 6] lists the details of this group of tumors. As discussed previously, GCTs (n = 9) and lymphomas (n = 1) did not form a major part of our study. Of the nine cases of GCT, six were mature cystic teratoma (M:F = 4:1, age range 13–49 years). Remaining three GCT cases and the lone case of non Hodgkin lymphoma (NHL) underwent thymectomy for residual enlarged thymus post chemotherapy. Thymectomy specimens in all the four cases showed extensive necrosis, areas of hemorrhage, dense inflammation, and chemotherapy-related changes but no viable residual tumor.
|Table 6: Details of patients with mediastinal tumors other than TETs (n=20)|
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Two cases of thymolipoma were seen, both incidentally detected in clinically asymptomatic young female patients [Figure 2]c, [Figure 2]d. There were four cases of thymic hemangioma (M:F = 3:1; age range 17–62 years) [Figure 2]e, [Figure 2]f. One patient presented with history of breathlessness, the other three patients had MG; radiology in all cases showed AMMs suggestive of thymoma. An interesting case of a thymic lymphangioma was seen in a young male in his early twenties who presented with chest pain for 2 months and underwent radical thymectomy after contrast enhanced computed tomography (CECT) chest revealed an enlarged thymus. Gross and microscopic examination revealed a small multicystic lesion with tiny loculi lined by uniform flattened endothelium with few wisps of smooth muscle bundles, lymphoid tissue, and occasional atrophic thymic tissue remnants in the cyst wall. Three patients (20–62 years; M:F = 1:2) presented with features of recurrent hyperparathyroidism. Technetium-99m-sestamibi scans (99mTc-MIBI) showed intense uptake in the superior mediastinum and CT chest revealed small nodule within the residual thymus in each case. Histology showed ectopic parathyroid adenoma with the residual thymus showing atrophic changes [Figure 2]a, [Figure 2]b.
|Figure 2: (a and b) Ectopic parathyroid adenoma composed of sheets of bland chief cells with peripheral rim of residual thymic tissue [HE; 4x, 10x]; (c) Gross image from a thymolipoma showing thinly encapsulated tumor with a yellow, lobulated, bulging cut surface; (d) Lobules of mature adipocytic cells with thin septa containing thymic tissue [HE; 4x]; (e) Gross image from thymic hemangioma showing an encapsulated tumor with a dark tan, spongy cut surface; (f) Closely packed congested cavernous channels lined by bland endothelial cells [HE; 20x]. Residual thymic tissue was seen focally at the periphery (not shown)|
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| Discussion|| |
Though TETs are the commonest thymic lesions and have been the focus of most studies involving thymus, a diverse spectrum of pathologic processes can affect the thymus, as observed in our study. The benign and non-neoplastic end of this spectrum has not been explored in depth so far, and the few studies published in this regard have largely been in relation to the association between MG and the thymus. In a study by Singhal et al. involving 841 MG patients, majority (64.4%) of thymectomy cases showed non-neoplastic or benign pathologies; with thymic hyperplasia being the most frequent lesion followed by atrophic thymus, benign pathologies (ranging from cysts to lipomas), and normal thymus. To the best of our knowledge, this study is the largest study so far, focusing on the entire disease spectrum of the thymus. Non-neoplastic and benign lesions comprised 40.6% (63/155) of our MG cases, with TFH being the most frequent followed by involuted or normal thymus, TTH, thymic cysts, and thymic hemangioma. We observed stronger association of TFH with MG than TTH, a finding replicated by other studies.,,, In MG patients undergoing thymectomy, non-thymoma pathology is more common than thymoma; however, the reverse was observed in our study, with 58.7% (91/155) of MG cases showing associated thymoma., The higher frequency of thymoma in our MG cases possibly reflects a selection bias, since our institute serves as a tertiary referral facility for many patients with AMM.
TETs, particularly thymomas are the commonest anterior mediastinal tumor with an incidence of 1.3–2.5 per million per year. In our study TETs comprised 64.7% of all cases with thymomas accounting for the majority (94.4%). Globally, no sex predilection for TETs is reported, however slight male predominance was seen in our study which is similar to other studies on Indian population.,, Thymomas have well-known association with several PNS, particularly MG, which has been reported in up to 60% patients. About 52.4% of thymoma cases in this study had associated PNS, with MG accounting for majority of cases (n = 91; 49.2%), though few cases of IBD, PRCA, AIHA, and SLE were also seen. The histologic classification of thymomas has been a subject of considerable debate with numerous classifications introduced over the years, and then replaced by new or alternative schemes. WHO classification of thymic tumors, introduced in 1999 divided TETs into six histologic types: A, AB, B1, B2, B3, and thymic carcinoma. This classification, subsequently modified in 2004 and 2015, is currently the most widely accepted classification system worldwide., Application of the latest WHO 2015 classification in this study resulted in reclassification of some cases. Two type A thymomas were reclassified as “atypical type A thymoma” on the basis of cellular atypia and increased mitotic activity. Though at present there is insufficient data to determine the clinical significance of this atypical variant, it is noteworthy that both atypical type A thymomas in our study belonged to higher stage (stage III) in contrast to majority of type A cases which were in lower stage (stage I). Further, four cases earlier labeled as type A thymoma were reclassified into type AB based on results of TdT IHC as per the new diagnostic criteria. WHO 2015 classification discourages the term “combined thymic epithelial tumors,” for thymomas with mixed histology, and instead recommends that the diagnosis lists all histological types encountered, starting with the most prominent component and subsequently listing all minor components in 10% increments. Accordingly, 24 mixed histology thymomas in our study were reclassified. WHO histologic thymoma subtyping is an established prognostic factor; therefore keeping abreast with latest modifications in the classification scheme is vital for pathologists.,
Type B2 was the commonest thymoma subtype in our study, followed by types AB, B1, B3, and A; which is in agreement with multiple previous studies, including those from India and the Asian subcontinent; although our results do not corroborate with the ITMIG worldwide database which found AB and B3 as the most frequent thymoma subtypes in Asians.,, Type B thymomas showed the highest association with MG in our study, which is in concurrence with the global data.,, The association of type A and AB thymomas with lower MMK stage also corroborates with the ITMIG database as well as with the most other Indian studies., We also encountered two rare thymoma subtypes in our study, including metaplastic thymoma and MTLS. Both these subtypes are characterized by distinctive histologic picture and unique clinical profile in the form of lack of association with MG and generally indolent clinical course, with surgical excision alone being the primary treatment modality.,, Awareness of these rare thymoma subtypes is therefore crucial among pathologists to avoid misdiagnosis and ensure appropriate patient management.
Thymic carcinomas are rare, comprising 15–20% of TETs.,,, There is a lack of larger studies on thymic carcinomas in literature and no such studies have been reported from India.,, We encountered 11 cases of thymic carcinoma in the present study with a similar morphologic spectrum and clinical profile as reported by most other studies. None of our patients had associated PNS. However, well known association with thymoma was not encountered in our study.,, Immunohistochemically, the positivity rates of CD5 (72.7%) and CD117 (63.6%) in our study corroborate with data from previous studies.,,, A new marker, FoxN1 is reported to be positive 68–76% of thymic carcinomas; however, FoxN1 IHC was not performed in our study.
Primary neuroendocrine tumors of the thymus (NETTs) are rare accounting for approximately 0.4% of all carcinoid tumors and <5% of all the AMMS., NETTs are biologically very aggressive tumors which exhibit more locally advanced disease and higher rate of metastasis than thymic carcinomas. WHO 2015 classification abandoned the descriptive terms “well differentiated neuroendocrine carcinoma” (referring to carcinoids) and “poorly differentiated neuroendocrine carcinoma” (referring to LCNEC and small cell carcinoma [SCC]), which were used in the earlier editions. Atypical and typical carcinoids are now classified as low-grade and intermediate grade NETTs, to separate them from high-grade neuroendocrine carcinoma (which includes LCNEC and SCC). The clinical profile and morphological spectrum of our NETT cases matches data from previous studies.,, Since we included only thymectomy specimens in our study; lymphomas and GCTs formed only a minor part of our study. However, a previous study on mediastinal tumors from our institute revealed a similar spectrum of all mediastinal lesions as global data.,
In conclusion, the thymus is a dynamic organ which evolves over the course of a lifetime, with age-related variations in normal histology, such as involution and gradual fatty replacement. These unique characteristics, coupled with an association with a diverse range of pathologic processes and the relative infrequency of thymectomy specimens in routine pathology practice can make thymus an enigma for pathologists leading to diagnostic errors. This study is an endeavor to familiarize residents and practicing pathologists with the broad spectrum of thymic lesions, since awareness of various pathologic entities, histologic classification schemas, and clear-cut reporting of thymectomy specimens is paramount to optimal patient management.
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Conflicts of interest
There are no conflicts of interest.
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Senior Consultant, Department of Histopathology, Sir Ganga Ram Hospital, Rajender Nagar, New Delhi
Source of Support: None, Conflict of Interest: None
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]
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