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Year : 2019  |  Volume : 62  |  Issue : 3  |  Page : 473-476
Cytological findings of NK/T-cell lymphoma in pericardial effusion: A case report with a review of the literature

1 Department of Pathology, Soonchunhyang University Seoul Hospital, Seoul, Korea
2 Division of Hematology.Oncology, Department of Internal Medicine, Soonchunhyang University Seoul Hospital, Seoul, Korea

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Date of Web Publication26-Jul-2019


Extranodal Natural Killer/T-cell lymphoma (ENKL) is an aggressive NK or cytotoxic T-cell neoplasm. The cytological features of NK/T-cell lymphoma have been rarely described, mainly focusing on the fine needle aspiration cytology from lymph nodes or soft tissue, except for a few cases focused on body fluid. A 46-year-old man visited the hospital due to generalized weakness and weight loss. Three months prior, computed tomographic scan revealed mesenteric panniculitis and reactive lymph nodal enlargement, as well as a mildly thickened left adrenal gland, suggesting an inflammatory condition. About 100 days later, marked enlargement of both adrenal glands with pericardial effusion was noted. The pericardial effusion contained medium-sized atypical lymphocytes, suspicious for malignant lymphoma, and the left adrenal mass was histologically confirmed as ENKL on biopsied specimen. Herein, we describe the cytological features of NK/T-cell lymphoma in body fluid cytology along with a review of the literature.

Keywords: Aspiration, cytology, NK/T-cell lymphoma

How to cite this article:
Han Y, Kim KH, Choi IH. Cytological findings of NK/T-cell lymphoma in pericardial effusion: A case report with a review of the literature. Indian J Pathol Microbiol 2019;62:473-6

How to cite this URL:
Han Y, Kim KH, Choi IH. Cytological findings of NK/T-cell lymphoma in pericardial effusion: A case report with a review of the literature. Indian J Pathol Microbiol [serial online] 2019 [cited 2021 Jun 17];62:473-6. Available from: https://www.ijpmonline.org/text.asp?2019/62/3/473/263487

   Introduction Top

Extranodal Natural Killer/T-cell lymphoma (ENKL) is an aggressive NK or cytotoxic T-cell neoplasm. Its incidence rate comprises 3% to 6% of all non-Hodgkin lymphoma in Asia and Latin America,[1] showing characteristic angiodestructive histological findings as well as being associated with Epstein-Barr virus (EBV) infection. Its cytological features in body fluid have rarely been described, and most cytological features have focused on the fine needle aspiration cytology (FNAC) findings of lymph nodes.[2],[3],[4] The present case concerns a 46-year-old man who had a thickened mesentery and adrenal mass, diagnosed as NK/T-cell lymphoma (NKTCL) using a needle biopsy. A simultaneously developed pericardial effusion was cytologically examined.

   Case History Top

A 46-year-old man visited the hospital due to diarrhea for 3 months along with generalized weakness. An abdominal computed tomographic (CT) scan revealed mesenteric panniculitis as well as reactive lymph nodal enlargement and a mild thickening of the left adrenal gland. Due to the initial impression of an inflammatory condition, a follow-up visit was planned. Two months later, an additional abdominal CT scan revealed marked enlargements of both adrenal glands.

During the second visit (about 50 days later), the patient showed improved mesenteric panniculitis through an abdominal CT scan with mild anemia (Hb 12.5 g/dl) and nonspecific findings of serum chemistry. However, the patient had his third visit 2 months later due to generalized weakness and weight loss (5 kg/2 months). Laboratory findings revealed mild anemia with thrombocytopenia (Hb 12.7 g/dl, Hct 37.9%, platelet: 96000 μl), increased liver enzyme (AST/ALT: 90/70 U/L) and alkaline phosphatase (384 U/L), and markedly increased lactate dehydrogenase (678 U/L, normal range; 0~250). Radiologically, there were newly noted 6-cm-sized heterogeneously enhancing masses in both adrenal glands, suspicious for an involvement of lymphoma through an abdominal CT scan, and pericardial effusion as well as increased fat strands and infiltration of the mediastinum was noted through a chest CT scan. A percutaneous, transabdominal needle biopsy (PTNB) at the left adrenal gland was performed, and the patient was histologically confirmed to have ENKL. Simultaneously, pericardiocentesis with a cytological examination was done. Also, bone marrow evaluation and peripheral blood smear were performed. Bone marrow aspirate smears showed 40% of cellularity with increased number of megakaryocytes, 4.1:1 of M:E ratio, and there was no evidence of an involvement of malignant lymphoma. Despite undergoing chemotherapy with cyclophosphamide, hydroxydaunorubicin, oncovin, and prednisone (CHOP), the patient expired due to sepsis 3 weeks after the diagnosis.

The microscopic findings of PTNB at the left adrenal gland revealed diffuse infiltration of atypical lymphocytes, which were positive for CD3, CD56, TIA-1, and EBV-ISH [Figure 1]a, [Figure 1]b, [Figure 1]c, [Figure 1]d, [Figure 1]e, [Figure 1]f. Based on histological and immunohistochemical findings, it was histologically confirmed as ENKL.
Figure 1: Needle biopsied adrenal glands show diffuse infiltration of atypical lymphocytes (a and b, a ×12.5, b ×400). Infiltrated lymphocytes are positive for CD3(c, ×100), CD56(e, ×100), TIA-1 (not shown), and EBV in situ hybridization (f, ×100) and negative for CD20 (d, ×100)

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Cytologically, pericardial effusion had moderate cellularity, containing medium-sized atypical lymphocytes with irregularly shrunken, hyperchromatic nuclei and moderately clear cytoplasm [Figure 2]a, [Figure 2]b, [Figure 2]c, [Figure 2]d, [Figure 2]e, [Figure 2]f, [Figure 2]g. Notably, lymphophagocytic cells were prominent on the Giemsa stain [Figure 2] h].
Figure 2: Cytological findings of pericardial effusion revealed medium-sized, atypical lymphocytes with irregular hyperchromatic nuclei and moderate clear cytoplasm (a-f). Many atypical lymphoid cells were noted on necrotic background(g, cell block, x200). Lymphophagocytic cells were notable by Giemsa stain (h). (×400)

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   Discussion Top

Since the first report in 1998 by Wright et al., only a few reports have described the cytological features of NKTCL.[4] However, previous cytological reviews have depended on the FNAC smear of a lymph node or extranodal site.[5] The cytological features in the body fluid examination are summarized in [Table 1].
Table 1: Reviews of NK/T-cell lymphoma on cytological findings of body fluid cytology

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Wright et al.[4] examined a right testicular FNAC with the Diff-Quik stain and described it as cytologically cohesive, syncytial aggregates of tumor cells, showing pleomorphism-irregular nuclei with clumping of chromatin as well as clearing and marked multiple nucleoli.

Cho et al.[2] summarized the cytological features of NK/T-cell lymphoma with 10 cases of FNAC smears from soft tissues. In this study, all the specimens consisted of soft tissues, not body fluids. The cases of their study showed moderate-to-high cellularity and tumor cells varied from case to case. They range from large atypical lymphoid cells to small- to medium-sized cells, and the nucleus were described as pleomorphic irregular nuclei to oval slightly irregular nuclei. However, the necrotic background and apoptotic debris were almost consistent. Unlike the histological findings, bean-bag cells, also called phagocytic histiocytes, were found only in one case.[2]

In our case, lymphophagocytic cells were prominent. Although Cho et al. found phagocytic histiocytes in only one FNA specimen, considering all biopsy specimens showed bean-bag cells in their study, finding lymphophagocytic cells could be helpful in diagnosing NKTCL.

In addition, while the Cho et al. study showed moderate-to-high cellularity, our findings of pericardial effusion showed less cellularity, which is due to the difference of the specimen nature, the difference between FNAC smears from solid organ and cytology from body fluid. Chan et al. reviewed the cytological features of NKTCL, including two cases with nodal FNA and one case with pleural fluid, and pointed out that tumor cells appeared more shrunken when compared with lymph node FNAs.[6] Also, cytological atypia can show individual differences. Therefore, it is undesirable to depend only on the cellularity and cytological atypia when diagnosing NKTCL.

Lymphophagocytosis could be regarded as an “emperipolesis,” as both are a phenomenon characterized by the engulfment of one cell into another. The consequence of the emperipolesis could be cannibalism, host cell death, transcytosis, and syncytial.[9] Therefore, lymphophagocytosis is one of the consequences of emperipolesis.

In our experience, lymphophagocytosis(emperipolesis) was highly characteristic, and this was more prominent by Giemsa stain. However, there is no comment as to the frequency of this feature in other literature. Nevertheless, in our opinion, it is worth considering emperipolesis as a characteristic cytological feature of NKTCL.

In summary, characteristic findings of the body fluid of NKTCL have rarely been described. Here, we add a case of NKTCL with its cytological findings in the pericardial effusion fluid. In diagnosing NKTCL, many characteristic cytological findings of NKTCL on an FNAC smear were established and immunohistochemical stains provided some help for its delineation. However, it is hard to apply them on the body fluid specimen for the difference between solid organ and body fluid. Fortunately, emperipolesis was a prominent feature of NKTCL as it is associated with the NK-mediated lysosomal degradation pathway.[9] Therefore, emperipolesis may provide diagnostic clues in recognizing NKTCL besides cytological and immunohistochemical characteristics.

Declaration of patient consent

These authors certify that they have obtained all appropriate patient consent forms. In the form, the legal guardian has given/her consent for images and other clinical information to be reported in the journal. The guardian understands that names and initials will not be published and due efforts will be made to conceal patient's identity, but anonymity cannot be guaranteed.


This work was supported by the Soonchunhyang University Research Fund.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

   References Top

Chan JKC, Quintanilla-Martinez L, Ferry JA. Extranodal NK/T-cell lymphoma, Nasal Type. WHO Classification of Tumors of Haematopoietic and Lymphoid Tissues. Revised 4th ed. 2017. p. 368-71.  Back to cited text no. 1
Cho EY, Gong G, Khang SK, Kang YK, Huh J. Fine needle aspiration cytology of CD56-positive natural killer/T-cell lymphoma of soft tissue. Cancer 2002;96:344-50.  Back to cited text no. 2
Jimenez-Heffernan JA, Gonzalez-Peramato P, Perna C, Alvarez-Ferreira J, Lopez-Ferrer P, Viguer JM. Fine-needle aspiration cytology of extranodal natural killer/T-cell lymphoma. Diagn Cytopathol 2002;27:371-4.  Back to cited text no. 3
Wright CA, Cooper K, Leiman G, Davidge-Pitts M. Natural killer cell lymphoma in cytology: Breaking all the rules--a case report. Diagn Cytopathol 1998;19:9-11.  Back to cited text no. 4
Dunning KK, Wudhikarn K, Safo AO, Holman CJ, McKenna RW, Pambuccian SE. Adrenal extranodal NK/T-cell lymphoma diagnosed by fine-needle aspiration and cerebrospinal fluid cytology and immunophenotyping: A case report. Diagn Cytopathol 2009;37:686-95.  Back to cited text no. 5
Chan AB, Chan WY, Chow JH. Cytologic features of NK/T-cell lymphoma. Acta Cytol 2003;47:595-601.  Back to cited text no. 6
Dunphy CH. Natural killer cell lymphoma of the small intestine: Diagnosis by flow cytometric immunophenotyping of paracentesis fluid. Diagn Cytopathol 1999;20:246-8.  Back to cited text no. 7
Walavalkar V, Oak J, Gu M. Cytological diagnosis of extranodal NK/T-cell lymphoma, nasal type, in cerebrospinal fluid. Cytopathology 2013;24:342-4.  Back to cited text no. 8
Rastogi V, Sharma R, Misra SR, Yadav L, Sharma V. Emperipolesis-A review. J Clin Diagn Res 2014;8:Zm01-2.  Back to cited text no. 9

Correspondence Address:
In Ho Choi
Department of Pathology, Soonchunhyang University Seoul Hospital, Yongsangu, Daesagwanro 59, Seoul
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/IJPM.IJPM_540_18

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