Khaki et al. Diagnostic Pathology 2013, 8:98http://www.diagnosticpathology.org/content/8/1/98

CASE REPORT Open Access

CLECervical type AB thymoma (Mixed) tumourdiagnosis in a mynah as a model to study human:clinicohistological, immunohistochemical andcytohistopathological studyFariba Khaki1, Javad Javanbakht1*, Farhang Sasani1, Mohammad Javad Gharagozlou1, Alimohammad Bahrami2,Hemmat Moslemzadeh3 and Reza Sheikhzadeh4

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Abstract: Thymoma is a primary mediastinal neoplasm arising from or exhibiting differentiation towards thymicepithelial cells, typically with the presence of non-neoplastic lymphocytes. A 13-year-old male Mynah bird(acridotheres tristis) was presented for evaluation of a 2.3 × 1.5 × 1.0 cm mass in the left ventrolateral cervical region.The clinical signs, radiology, cytohistopathology and immunohistochimy findings related to the thymoma arepresented. These findings indicated that the tumor was a type AB thymoma according to the World HealthOrganization (WHO) and veterinary classification. Thymomas are rarely reported in avian species and this is the firstreport in a Mynah bird.

Virtual slides: The virtual slide(s) for this article can be found here: http://www.diagnosticpathology.diagnomx.eu/vs/1159525819982779.

Keywords: Thymoma, Lymphocytic type, Diagnosis, Mynah,Neck

RETRACTEBackgroundThymomas are rare malignancies both in human andveterinary medicine. They have been described in a widerange of domestic and laboratory animals, such as ratsand mice [1,2], and occur more frequently in olderanimals. In humans, thymomas usually present in thefourth to fifth decade but can occur at all ages withoutsex predisposition [3]. In dogs and cats, thymomas arealso found in older animals [4], and they are rarelyreported in avian species and have only been docu-mented in an African grey parrot (Psittacus erithacus),[5] a finch (unspecified species), [6] domestic chickens,[7,8] a budgerigar (Melopsittacus undulatus), [9] and aJava sparrow (Padda oryzivora) [10].The etiology of thymomas is not yet understood. In

contrast to lymphomas, there is no evidence of a eti-ology of thymomas in humans and domestic animals. Asingle report exists that describes a family with high

* Correspondence: javadjavanbakht@ut.ac.ir1Department of Pathology, Faculty of Veterinary Medicine, Tehran University,Tehran, IranFull list of author information is available at the end of the article

© 2013 Khaki et al.; licensee BioMed Central LCommons Attribution License (http://creativecreproduction in any medium, provided the or

incidence of thymomas and might point to a geneticpredisposition [11].Thymomas are derived from thymic epithelium with

variable benign lymphocytic infiltration and thus are clas-sified as lymphocyte-predominant, epithelial-predominant,or mixed [12,13]. Type AB thymoma (also known asmixed thymoma) accounts for approximately 28% to 34%of all thymomas [14,15]. Approximately 16% of this typemay be associated with myasthenia gravis [14]. Morpho-logically, type AB thymoma is a thymic tumor in whichfoci having the features of type A thymoma are admixedwith foci rich in nonneoplastic lymphocytes.[16]. Histo-logically, these tumors are composed of neoplasticthymic epithelial cells and a variable number of lympho-cytes leading to a myriad of histologic subtypes depend-ing on the proportion of these elements [17]. Thisreport describes the clinical signs, cytopathological andimmunohistichemical characteristics of a thymoma in aMynah bird and because there is no established classifica-tion of thymic neoplasms in veterinary medicine and theavian thymomas bore a striking resemblance to theirhuman counterparts, an attempt to classify this neoplasm

td. This is an Open Access article distributed under the terms of the Creativeommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andiginal work is properly cited.

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according to the new World Health Organization (WHO)classification of human thymic epithelial tumors wasmade.

Case presentationIn April 2013, a 13-year-old adult male red-tail commonMynah bird (Acridotheres tristis) was referred to theAvian and Exotics Service of the Tehran Veterinary Col-lege, University of Tehran, for evaluation of a firm,round and circular neck mass, off-white to gray, lightlyencapsulated, moveable, attached to the underlyingtissue and measured 2.3 × 1.5 × 1.0 cm diameter was pal-pated on the left ventrolateral side of the neck near thethoracic inlet. No evidence of pain or discomfort wasnoticed, and the bird did not experience any difficulty inprehension and swallowing its food or in breathing. Ithad been fed predominantly a seed-based and table-fooddiet. Its owner first noticed the mass 4 weeks beforepresentation and had progressively increased in size overthat period. On gross examination, The bird had lostover 12% of its body weight over the 1 months, decreas-ing from 184 g to 162 g, because of the size of the massand the bird's weight loss, and the bird appearedemaciated.On radiographs, degenerative changes in right tarsal

joint and inflammation of its adjacent soft tissues ac-companying mineralization of its external soft tissuewere observed. In addition, hepatomegaly was recordedas well.A fine-needle aspirate of the mass was done, and a

blood sample was collected for a complete blood cellcount (CBC) and plasma biochemical analysis. Radio-graphs were taken, and the results showed that the masswas of soft-tissue density. Results of the plasmabiochemical profile, including bile acids, were withinreference ranges (Animal Health Laboratory, Universityof Tehran). The CBC results revealed a moderatemonocytosis at 2.94 × 109 cells/L [2.94 × 103 cells/dL](reference range for Amazon parrots: 0–0.4 × 109 cells/L

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Figure 1 (A) Fine-needle aspiration of thymoma showing predominatthymoma. Note thick nuclear membranes and more prominent nucleoli. (characterized these cells. Few lymphocytes are present.

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[0–0.4 × 103 cells/dL], Animal Health Laboratory,University of Tehran). Aspiration of the mass revealeda cystic structure and results of cytologic examinationof the fluid revealed large numbers of lymphocyteswith occasional erythrocytes. The bird died duringexamination.Cytology this case demonstrated a mixture of round

and oval cells. The cytoplasm was scanty and the cellborders were indistinct. Moderate to marked nuclearpleomorphism (Figure 1A and 1B) was noted in thiscase. These pleomorphic cells displayed anisonucleosis,irregular nuclear membranes, coarse clumping of chro-matin, and prominent nucleoli. Mitoses ranged fromscant to frequent.A midline portion of the mass was processed routinely,

embedded in paraffin wax, sectioned at 5 μm, andstained with hematoxylin and eosin. For further study,paraffin sections were stained immunohistochemicallywith CK 14 and CK18 (Abcam Co., Cambridge, USA)for this case.For immunohistochemistry, sections from each tumor

were mounted on adhesive-coated slides (SuperfrostPlus, Menzel-Glaser, Braunschwaig, Germany), processedthrough xylene, and rehydrated in ethanol. Antigenretrieval was by boiling in a microwave oven (700 W)twice for 5 minutes in Tris–EDTA buffer—1.21 g Trisbase (A 1379, Applichem, Darmstadt, Germany) and0.372 g EDTA (8418, Merck, Darmstadt, Germany)—in 1liter of distilled water, pH 9. Endogenous peroxidase wasblocked with 0.6% (v/v) H2O2 in Tris-buffered saline(TBS; pH 7.6) for 15 minutes at 20°C before the monoclo-nal antibodies used included those for CK14 and CK18.

WHO classification of human thymic epithelial tumorsThe classification of human thymic epithelial tumors hasits origins in a histiogenetic classification originally pro-posed by Kirchner and Mueller-Hermelink and others[18-20]. The new WHO classification basically recognizesthe same histologic entities but uses an alphanumerical

ely round to oval cells with moderate nuclear atypia in type ABB): High power view of type AB thymoma .Marked pleomorphism

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system, i.e., combinations of letters and numbers. Thym-omas with spindle, oval-shaped epithelial cells are desig-nated type A, and those with small round epithelialcomponents are designated type B. Tumors combiningthese features are designated type AB. Nonorganotypicthymic carcinomas are classified as type C thymomas.Type B is further subdivided into B1, B2, and B3 on thebasis of increasing epithelial areas and the emergence ofnuclear atypia [21,22].Necropsy examination indicated a thin bird with a foul-

smelling oral cavity. Dried serous discharge surroundedthe incision. A large necrotic ulcer was present in theesophagus with food and caseous material in the subcuta-neous space. No gross perforations of the esophagus werepresent. The intestines appeared necrotic. The resectedmass was greatly expansible, but there was no evidence oflocal invasion or distant metastasis.Microscopic findings demonstrated that lobules of small

polygonal cells with small round or oval vesicular nucleiand indistinct nucleoli accompanied by a variable amountof lymphocytes and the tumoral cells were circular orround and more comprised of lymphoblasts with exten-sive mitotic features together with and lymphocyte-poor

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Figure 2 Mixed thymoma; A and B: the tumoral cells were circular ormitotic cells (H&E;20 μm×100), C: Hyperemic and remarkable eosinopcomponents. (H&E;30 μm×200).

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spindle cells (Figure 2A,2B and 2D). The histiocytes withlight nuclei and pink cytoplasms among tumoral lymphoidcells were observed (Figure 3D). The tissue was severelyhyperemic and remarkable eosinophils existed among cellstogether with high number of undifferentiated neoplasticcells (Figure 2C).The necrosis was found in some partswith pyknosis and karyorrhexis. In vessels, the tumoralcells were seen. Numerous eosinophils in vessels indicatedeosinophilia, (Figure 3C) and plenty of histiocytescontained hemosiderosis in the tumor.A microscopic examination showed the tumor to con-

tain round shaped cells with a lymphocyte rich compo-nent. In the immunohistochemical study, the round cellsof the tumor were all positive for CK 14 (Figure 3A) andCK18 (Figure 3B).On the basis of this case findings, tumour was classi-

fied as AB thymomas by analogy with the WHO classifi-cation for human neoplasms. Mixture of lymphocyte-associated small polygonal cells and lymphocyte-poorspindle cells areas in tumor correspond closely to ABareas in human tumuors.These cytohistopathology and immunohistochemical

findings indicated that the tumor was a type AB

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round and more comprised of lymphoblasts with extensivehils existed among cells (H&E;50 μm×400) D: Note type A and B

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Figure 3 Mix ed thymoma; Immunohistochemical staining mixed thymoma with, CK 14(A) and CK 18 (B) are positive for the roundcells of the tumor. Hematoxylin and eosin staining of tissue and cells sections. (C): In vessels, the tumoral cells were seen. Numerous eosinophilsin vessels indicated eosinophilia (H&E;20 μ×200). (D): The histiocytes with light nuclei and pink cytoplasms among tumoral lymphoid cells wereobserve. (H&E;25 μm×400).

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Tthymoma according to the World Health Organizationand veterinary medicine classification.

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RETRADiscussionThymomas were tumours arising from or exhibitingdifferentiation toward thymic epithelial cells. It has beenreported that different subtypes of thymoma have multi-farious genetic characteristics, recent studies indicatedthat chromosomal 1 gain plays an significant role in mo-lecular genetic mechanism of thymic epithelium tumors[3,12,23]. In a study, Yuqing et al., 2012 suggested thatdifferent genes on chromosome 1 might employ differ-ent functions in the generation and development ofthymic epithelium tumors [12].Thymic epithelial tumors are rare both in human and

veterinary medicine. To our knowledge, this study describesthe largest serial of mixed thymoma observed in Mynahbird. In addition to, a description of the morphologicfindings, immunohistochemical and cytohistopathologicalinvestigations were performed on this tumor with theirhuman counterparts. Because of the high resemblance ofthe avian thymomas to their human counterparts, the

current human WHO classification for thymic epithelial tu-mors was used.The avian thymus gland consists of 7 flattened lobes of

tissue that are located bilaterally in the subcutis of theneck adjacent to the trachea [24]. Thus, thymomas inbirds occur cranial and ventrolateral to the thoracic in-let. In mammals, the thymus gland is located within themediastinum in the thoracic cavity [25]. The biologicalbehaviors of thymomas are benign and the neoplasiaarises from the epithelial portion of the thymus [26].In all avian species, the differential diagnosis for a cer-

vical swelling is fairly extensive and includes foreign bodyreaction, trauma, fungal granuloma, abscess, and neoplasia[5]. In this mynah, cervical swelling was observed 4 weeksbefore presentation and had progressively increased in sizeover that period. Radiographs performed at that timedemonstrated mineral opacities in the lateral cervicalregion, and degenerative changes in right tarsal joint andinflammation of its adjacent soft tissues accompanyingmineralization of its external soft tissue were observed. Inaddition, hepatomegaly was recorded as well.In all previously reported avian thymomas, limited

presurgical diagnostics were performed before attempted

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mass resection. Ideally, a complete diagnostic work-upconsisting of complete blood count, plasma biochemicalanalysis, radiographs, and computed tomography wouldbe performed before surgical exploration.Fine-needle as-pirate (FNA) with cytologic evaluation or biopsy are usefuldiagnostic modalities that can be used for an accurate pre-operative diagnosis.FNA biopsy has gained increasing acceptance as a

rapid, noninvasive, and effective diagnostic procedure inthe investigation of cervical masses [27,28]. Becausethymomas are uncommon neoplasms, experience withthe cytologic diagnosis of these tumors is limited. Toour knowledge, the correlation between cytologic find-ings of thymomas and various histologic classificationhas not been well studied previously. Ali and Erozan[26] found that it was possible to correlate the FNA find-ings with histologic subtypes determined on resection withadequate well preserved material. In the current study,aspirates with a high L:E ratio had a tendency to belong topredominantly mixed.Tao et al. [28] suggested a classification based on the

size, shape, and pleomorphism of the epithelial compo-nent, which has been shown to have prognostic value.Riazmontazer et al. [29] also reported a case of invasivethymoma with atypical cytologic features in the aspirate.They described invasive malignant thymomas with cyto-logic atypia. Our data generally are compatible with theseobservations. The more atypical the neoplastic cells are,the more likely the tumor will display aggressive behavior.The cytologic features of thymomas include dual lymph-oid and epithelial cellular populations and unique neoplas-tic tissue fragments that reflect histology and allow theiraccurate identification.The cytologic diagnosis of thymoma can be extremely

challenging. In part, this is because a technically proficientinterventional radiologist is needed, epithelial cells may bedifficult to recognize in lymphoid rich aspirate smears,and there is inherent sampling error in a tumor thatfrequently displays heterogeneous histopathology [16,30].Immunohistochemistry for cytokeratin is helpful in this

case, since the presence of rare epithelial cells in serialsections is suggestive of thymoma [31,32]. Cytokeratinprofiles have been established in human medicine for thethymus and thymomas, and have been shown to be clinic-ally useful in determining the invasive potential of theseneoplasms [16]. Since a cytomorphologic and histologicclassification of thymomas seems not to be a useful prog-nosticator in animals, the use of a pan-specific cocktail ofantibodies for cytokeratins is sufficient for the diagnosis ofthese tumors in veterinary medicine.Thymoma should be differentiated from other anterior

mediastinal neoplasms with epithelial and/or lymphoiddifferentiation, including Non-Hodgkin (NHL) andHodgkin lymphomas, thymic carcinomas, and germ cell

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malignancies. NHL and Hodgkin lymphoma can be sep-arated from thymoma by their dispersed cell population,distinctive cytologic features, and positive staining forCD45, CD20, CD15, and CD30, and negative stainingfor CK14,CK18, CK20 respectively. Helpful cytologicand immunocytochemical features in making the diagnosisof thymic carcinoma are clear-cut cytological atypia, ab-sence of immature lymphocytes (CD3 + .CD1a+, CD99+),and expression of CD5 and CD70 by neoplastic epithelialcells [12].Immunohistochemical markers can be used to differ-

entiate the epithelial cells and lymphocytes, aside fromthe proportion of both cells type [31].In this case, theround cells of the tumor were all positive for CK 14,CK18 and negative for CK10. Based on the WHO andveterinary classification of thymomas [32], this particularcase is categorized as mixed type. Overall, the presentstudy confirms previous observations [29,30] that FNAof anterior mediastinal thymic lesions generally yieldsadequate cellular tissue with distinct cytologic andimmunophenotypic features that enables thymomadiagnosis.In this case, lymphocytes were present individually or

in small clump as lobules of small polygonal cells withsmall round or oval vesicular nuclei and indistinct nucle-oli. The proportion of neoplastic cells and nonneoplasticlymphocytes varies widely between tumors and betweendifferent lobules of the same tumor [33-35]. Based onthis study, thymomas may be categorized in veterinarymedicine as lymphocyte predominant, epithelial pre-dominant, or mixed [32].When lymphocytes predomin-ate, the neoplasm must be differentiated from thymiclymphoma.Thymomas have been described in different sites of

the body. The anterior mediastinum or thoracic inlet istheir usual site of occurrence, but these neoplasms canalso be seen elsewhere, including the cervical region andposterior mediastinum, with variable compression of ad-jacent structures such as trachea, esophagus, and medi-astinal vessels [32,36]. The majority of the thymomas arebenign. Local invasion and metastasis are considered bymost authors to be uncommon, with metastases beingreported in the pulmonary and pericardial pleura, [37]lung, [32,36] mediastinal lymph node, [35] cervical por-tion of the thymus, [38] kidney, [32] and uterus. Despite,Marx and Mueller-Hermelink considered human type Aand AB thymoma as clinically benign tumours [20].The thymomas examined in our study showed massive

local growth with compression, albeit not invasion, ofadjacent organs. Furthermore, lymphatic congestion wasseen in the cervical lymph nodes and based on theirmicroscopic features of malignancy tumor (such as areasof high cellularity, cellular pleomorphism, high mitoticindex, necrotic foci accompanied by pyknosis and

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karyorrhexis and high number of undifferentiated neo-plastic cells), in this case, the tumor was considered tobe malignant in nature.Limitations of the cytological method include an un-

proven ability to definitively separate thymoma intospecific WHO subtypes using cytology alone, and to de-termine capsular invasion [16]. Altogether, the presentreport confirms previous observations [26,27] that fineneedle aspiration of cervical thymic lesions generallyyields adequate cellular tissue with distinct cytologic,histopathologic and immunophenotypic features thatenables thymoma diagnosis.

ConclusionBased on this report, we recommend that thymomas beincluded in the differential diagnosis of neck masses inavian. Because it was highly similar to human thym-omas, the new WHO classification for human epithelialthymic tumors was used. The tumor was diagnosed asAB type thymomas, and the WHO nomenclature wasfound to be highly applicable. The incidence of thymomain avian is unknown; we hope this will become clearer. Toour knowledge, this is the first report of cervical thymomatype AB in a mynah, suggesting that this tumour shouldbe included as a differential diagnosis for neck round andspindle cell tumours. Finally, for understanding of thesecomplex neoplasms and the development of the effectivedifferential diagnosis, further investigation will be neededinto the clinical features and the basic science.

Competing interestsThe authors declare that they have no conflict of interest.

Authors’ contributionsFS and MJG participated in the histopathological evaluation, performed theliterature review, acquired photomicrographs and drafted the manuscriptand gave the final histopathological diagnosis. JJ performed sequencingalignment and manuscript writing. FK carried out the immunohistochemicalstains evaluation. HM, AMB and RS edited the manuscript and maderequired changes. All authors have read and approved the final manuscript.

AcknowledgementsThe authors thank staff of the Department of pathology, Faculty ofVeterinary Medicine, Tehran University for their valuable technical assistance.

Author details1Department of Pathology, Faculty of Veterinary Medicine, Tehran University,Tehran, Iran. 2Faculty of Para-Veterinary Medicine, University of Ilam, Ilam,Iran. 3Graduate, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.4Faculty of Veterinary Medicine, Teharn University, Tehran, Iran.

Received: 20 May 2013 Accepted: 3 June 2013Published: 18 June 2013

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doi:10.1186/1746-1596-8-98Cite this article as: Khaki et al.: Cervical type AB thymoma (Mixed)tumour diagnosis in a mynah as a model to study human:clinicohistological, immunohistochemical and cytohistopathologicalstudy. Diagnostic Pathology 2013 8:98.

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