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Neuropathology 2017
doi:10.1111/neup.12438
Case Report
Primary central nervous system extranodal nasal-type
natural killer/T-cell lymphoma with CD20 expression
Dujuan Li,1 Fangfang Fu2 and Lifei Lian3*
Departments of 1Pathology, 2Radiology, Henan Provincial People’s Hospital (People’s Hospital of Zhengzhou
University), Zhengzhou and 3Department of Neurology, Tongji Hospital, Tongji Medical College, Huazhong University
of Science and Technology, Wuhan, China
We report a unique case of primary CNS extranodal natural killer/T-cell lymphoma (PCNS ENKTCL) with CD20
expression and the monoclonal rearrangement of Ig
heavey chain (IgH) gene. Resection specimens were evaluated using HE-stained sections, immunohistochemistry,
in situ hybridization and PCR. Histopathologic examination, immunohistochemistry and molecular studies showed
the intermediate-sized lymphoma cells expressing CD2,
CD3ε, granzyme B, TIA-1, CD20 and Epstein–Barr virusencoded RNA, with germline T-cell receptor gene and the
monoclonal rearrangement of IgH gene. Clinicopathologic
and radiographic evaluation indicated the lesion was of
exclusive left cerebellar localization. Thus, PCNS
ENKTCL with the CD20 expression was diagnosed.
ENKTCL with both CD20-positive expression and the
monoclonal rearrangement of IgH gene may be mistaken
for B-cell lymphoma; thus, the comprehensive evaluation
of histomorphology, more extensive immunoprofiles and
molecular studies is essential to reach the correct diagnosis. The rare PCNS ENKTCL shows a highly aggressive
nature and a poorer prognosis.
Key words: CD20, Epstein–Barr virus, lymphoma, natural
killer/T-cell lymphoma, primary central nervous system
lymphoma.
INTRODUCTION
Primary CNS lymphoma (PCNSL) is a relatively rare disease. Among PCNSL, 98% are comprised of B-cell
lymphomas,1 and only 2% are T-cell lymphomas (TCL).2
PCNS extranodal natural killer/T-cell lymphoma
Correspondence: Lifei Lian, MD, PhD, Department of Neurology,
Tongji Hospital, Tongji Medical College, Huazhong University of
Science and Technology, Wuhan, Hubei 430030, China.
Email: llf2000@126.com
Received 04 August 2017; Revised 29 September 2017; Accepted
30 September 2017.
© 2017 Japanese Society of Neuropathology
(ENKTCL) is exceedingly rare, to the best of our knowledge, with only 10 cases reported in the literature.3–12
Aberrant expression of B-cell-associated antigens in
TCL is uncommon, but it is well recognized. CD20 expression has been documented in 5–8% of TCL,13 and most of
the cases are classified as peripheral T-cell lymphoma, not
otherwise specified (PTCL, NOS).14 Co-expressing CD20
in ENKTCL is extremely rare, with only five cases to
date.15–19
In this study, we describe a case of PCNS ENKTCL
with CD20 expression, in a 27-year-old immunocompetent
Chinese man. This case is unique in its occurrence in
PCNS ENKTCL, CD20-positive expression, and the identification of the monoclonal rearrangement of B-cell
receptor (Ig heavy chain (IgH)) gene. PCNSL ENKTCL
or CD20-positive expression in ENKTCL is respectively a
rare event, but it is unique indeed for both the phenomena
to occur concurrently. Moreover, both CD20-positive
expression and the presence of the monoclonal
rearrangement of IgH in ENKTCL, to our knowledge,
have not been previously described. Thus, this is the first
case of PCNS ENKTCL with CD20-positive expression
and the monoclonal rearrangement of IgH gene. We also
review five cases of CD20-positive ENKTCL, as well as
10 cases of PCNS ENKTCL reported in the literature.
CLINICAL SUMMARY
A 27-year-old Chinese man had presented with complaints
of dysphagia, dysarthria and facial weakness for a period of
approximately 4 weeks. There was no relevant personal or
familial medical history. The patient had been referred to a
local clinic and treated with antithrombotics for “ischemic
stroke”, but the symptoms did not improve. As a result, the
patient was referred to our hospital for examination and
treatment. On initial physical examination, no splenomegaly, lymphadenopathy, skin lesion or fever were observed.
Sinonasal involvement was not identified based on the
medical history, symptoms and physical examination
2
D Li et al.
results. Neurological examination showed the patient had
weakness in the left side of the face and bulbar paralysis. A
MRI was performed and revealed a mass located in the left
cerebellum and was observed to extend into the medulla
oblongata. The lesion exhibited hypodensity on T1weighted and hyperintensity on T2-weighted images
(Fig. 1A,B), increased signal on diffusion-weighted images
(DWI) (Fig. 1C), and slight enhancement with gadolinium
(Fig. 1D). Magnetic resonance spectroscopy (MRS)
showed a suppressed N-acetylaspartate peak and an
increased choline peak (Fig. 1E).
The CSF examination was negative for neoplastic cells,
with pleocytosis (28 × 106, normal range 0–8 × 106) and
slightly elevated protein (65.21 mg/dL, normal range
15–45 mg/dL). The ocular examination was performed
and was negative for ocular lymphoma. The patient was
immunocompetent and HIV negative. The white blood
cell count, hemoglobin level and platelets were all within
reference ranges. A bone marrow biopsy sample failed to
detect any malignant cells. The epipharyngoscope examination revealed paralysis in the left vocal cord, without
neoplasm. Abdominal ultrasonic inspection demonstrated
no hepatomegaly or splenomegaly. A whole-body positron
emission tomography (PET)-CT scan revealed intense
fluorodeoxyglucose uptake in multiple foci in the left cerebellum but no foci of increased uptake elsewhere in the
body, including the nasopharynx, or the sinuses.
The patient underwent a partial resection of the mass. A
diagnosis of PCNS ENKTCL was made. Then, the patient
received 28 Gy irradiation and steroid therapy, but the
symptoms did not improve. Two months after the operation, the patient presented with dizziness and fever. Peripheral blood cell examination showed white blood cells, red
blood cells, platelet and hemoglobin were decreased. The
second whole-body PET-CT scan revealed intense
fluorodeoxyglucose uptake in multiple foci in the left cerebellum and bone, indicating the recurrence of the lesion
and bone marrow involvement. The re-examination of bone
marrow aspiration demonstrated bone marrow invasion of
the lymphoma cells (46% of unknown cells). Finally, the
patient was discharged and died 3 months later.
MATERIAL AND METHODS
Paraffin-embedded
sections
were
stained
with
HE. Immunohistochemical studies were performed with a
variety of antibodies as described below, using heatinduced antigen retrieval on the Nichirei Bioscience
Histostainer and Leica Microsystems Bond-III autostainers
according to the manufacturer’s instructions. The antibodies used were CD45, CD20, CD79a, CD19, Pax-5,
OCT-2, Bob-1, CD2, CD3ε, CD4, CD5, CD7, CD8, CD56,
CD30, terminal deoxynucleotidyl transferase (TdT), TIA-
1, granzyme B and anaplastic lymphoma kinase (ALK). To
detect the Epstein–Barr virus (EBV)-encoded RNA
(EBER), EBV-RNA in situ hybridization was performed
on the paraffin-embedded sections using EBER probe
(BondTM Ready-to-Use ISH, Leica Biosystems, Newcastle, UK). A multiplex real-time PCR study for the detection of clonally rearranged Ig and T-cell receptor (TCR)
genes was performed on DNA extracted from the paraffin
block. Finally, a capillary electrophoresis in polyacrylamide
gel by means of the ABI-PRISM 310 genetic analyzer
(Applied Biosystems, Foster City, CA, US) was carried
out. The multiplex PCR design of primers and protocols
was performed as previously described.20
PATHOLOGICAL FINDINGS AND RESULTS
The histological examination revealed that the
intermediate-sized monomorphic atypical lymphoid cells
were arranged in a diffuse growth pattern with focal
coagulative necrosis and apoptotic bodies (Fig. 2A). The
angiocentric growth pattern was seen (Fig. 2B). The tumor
cells had irregularly folded nuclei and inconspicuous
nucleoli, with a moderate amount of eosinophilic cytoplasm. Mitotic figures were readily found. In addition,
there was a vascular proliferation and the infiltration of
some histiocytic macrophages.
Immunohistochemical studies showed that the tumor
cells were strongly positive for the leucocyte marker CD45
and the T-cell markers CD2 and CD3ε (Fig. 2C). Coexpression of CD20 (Fig. 2D) and CD30 were noted in
the majority of tumor cells. Moreover, CD20 staining
intensity was heterogeneous. However, other B-cell
markers, including CD79a, CD19, PAX5, OCT-2 or BOB1, were negative. The tumor cells were positive for the
cytotoxic markers such as granzyme B (Fig. 2E) and TIA1. The proliferation marker Ki67 was positive in approximately 85% of lymphoma cells. The tumor cells were negative for CD56, other T-cell markers (CD4, CD8, CD5,
CD7), TdT, myeloperoxidase (MPO) and ALK.
In situ hybridization for EBER was strikingly positive
in almost all the tumor cells (Fig. 2F). PCR-based molecular testing for the detection of clonally rearranged Ig and
TCR genes showed the T-cell receptor gamma (TCRγ)
gene and beta (TCRβ) gene, or the Ig light chain (Igκ)
gene with polyclonal rearrangement, but the IgH gene
showed the monoclonal rearrangement (Fig. 3).
DISCUSSION
We report a case of intermediate-sized lymphoma cells
expressing CD2, CD3ε, granzyme B, TIA-1, CD20, CD30
and EBER, with polyclonal rearrangement of TCR gene
and the monoclonal rearrangement of IgH gene. The
overall findings favored ENKTCL, despite the expression
© 2017 Japanese Society of Neuropathology
PCNS ENKTCL with CD20 expression
3
Fig. 1 Radiological investigation of the brain. Magnetic resonance axial T1-weighted imaging of the brain shows a hypointense lesion
in the left medullary dorsal (A) with gadolinium enhancement (D). The lesion is hypertense on T2-weighted imaging (B) and diffusionweighted imaging (C). There is no restricted diffusion on apparent diffusion coefficient map. Magnetic resonance spectroscopy of the
lesion suppressed N-acetyl-aspartate with an increased choline peak (E).
of CD20 and CD30, as well as with the monoclonal
rearrangement of IgH gene. To the best of our knowledge,
only five cases of CD20-positive ENKTCL are reported in
the literature; however, all are with polyclonal
rearrangement of IgH gene. Here, we report the first case
of ENKTCL with both CD20-positive expression and the
monoclonal rearrangement of IgH gene.
Not only aberrant expression of the B-cell marker
CD20 is described in T/NK-cell lymphomas,21 but also coexpression of T-cell-associated antigens such as CD2,
CD3, CD4, CD7, CD8 may be found in B-cell
lymphomas.22–24 Furthermore, aberrant expression of Tcell-associated antigens in B-cell lymphomas may be associated with the absence of PAX-5 gene or deregulated
PAX-5 activity.25,26 Therefore, in our case, B-cell lymphoma with T-cell-associated antigens should be included
as a major differential diagnosis. In the reported cases of
B-cell lymphomas with aberrant CD3 expression,23,24 lymphoma cells strongly and diffusely expressed several B-cell
© 2017 Japanese Society of Neuropathology
markers such as CD20, CD79a, PAX5, OCT-2 and BOB1. In contrast, in our case, except for the positive expression of CD20, the expression of the other B-cell-associated
antigens such as CD79a, CD19, PAX5, OCT-2 and BOB-1
were all negative, which does not support a diagnosis of
B-cell lymphomas with aberrant CD3 expression. Furthermore, lymphomatoid granulomatosis (LYG) is an EBVassociated lesion characterized by angiocentric and
angiodestructive lymphocyte infiltration, predominantly
involving the lungs and other extranodal sites, such as the
CNS. So, LYG should be included as another differential
diagnosis. The EBV-positive cells of LYG are of B-cell
origin, and express the B-cell-associated antigens such as
CD20, CD79a, CD19, PAX5, OCT-2 and BOB-1. However, in our case, EBV-positive cells express typically the
T-cell-associated antigens such as CD2, CD3ε, granzyme
B and TIA-1, except for CD20. So a diagnosis of LYG
was not favored. In addition, the tumor cells possessed the
CD30 positive and CD56 negative phenotype in a younger
4
D Li et al.
Fig. 2 Histological and immunohistochemical findings of the tumor tissues. HE staining reveals that the intermediate-sized tumor cells
had irregularly folded nuclei and inconspicuous nucleoli, with focal coagulative necrosis and apoptotic bodies (A). The angiocentric
growth pattern was seen (B). The tumor cells were positive for CD3ε (C), CD20 (D), granzyme B (E) and Epstein–Barr virus-encoded
RNA (EBER) (F). Bar = 20 μm (A–F).
patient, consequently leading to an initial diagnosis of anaplastic large cell lymphoma (ALCL). Indeed, it has been
reported that ENKTCL may show CD30-positive
expression and CD56-negative expression.27 The findings
of the absence of ALK expression and presence of EBER
expression do not favor a diagnosis of ALCL. Therefore,
Fig. 3 Molecular testing for the
gene rearrangement of the immunoglobulin light chain gene and the
immunoglobulin heavy chain (IgH)
gene. The tumor demonstrates the
monoclonal rearrangement (IGH E)
of IgH gene.
© 2017 Japanese Society of Neuropathology
PCNS ENKTCL with CD20 expression
in our case, based on the histopathologic features and the
expression of CD2, CD3ε, granzyme B, TIA-1 and EBER,
a diagnosis of ENKTCL with CD20 expression was
favored.
Another dilemma encountered in the diagnosis of this
case resulted from the observation of TCR polyclonal
rearrangement, and, contrarily, with IgH monoclonal
rearrangement. In fact, the monoclonal rearrangement of
aberrant cell lineages in B-cell or T-cell lymphomas (socalled “lineage infidelity”) has been reported.15,28,29 The
percentage of aberrant gene rearrangement is 5% for Bcell lymphomas and 29% for T-cell lymphomas. Garcia
et al. reported that 16% of TCL showed the monoclonal
rearrangement of IgH gene.28 Therefore, the final determination of cell lineage as exemplified by our case needs
to be based on the histopathologic and immunophenotypic
features.
To date, only five cases of CD20-positive ENKTCL
have been reported.15–19 Five were men and one was a
woman, with a median age of 53 years (range,
25–78 years). Three were Chinese and the other three
were Japanese, Taiwanese and Caucasian, respectively.
The tumors arose from the nasal cavity (two cases), stomach (two cases), right thenar (one case) and cerebellum
(one case). Five of the six cases showed the polyclonal
rearrangement of TCR and IgH, except for our case showing IgH monoclonal rearrangement. Follow-up information available indicated more highly aggressive clinical
course; and three patients (3/5) died within 6 months after
the diagnosis. However, the case reported by Jiang et al.
presented an indolent clinical course with 10 years duration. Because the case number is too small for analysis, it
is uncertain whether CD20-positive ENKTCL is related to
prognosis or not.
The mechanism of CD20 expression in ENKTCL
remains unknown. Two hypotheses were proposed to
explain the expression of CD20 in ENKTCL. First, CD20
positivity might represent aberrant antigen expression due
to the neoplastic process. Second, CD20 expression might
indicate neoplastic transformation of a rare cell type that
co-expresses CD20 and NK/T cell markers. Recently, a
progenitor capable of differentiating into B-cells, T-cells
and NK-cells has also been identified.30 In our case, the
tumor cells were strongly positive for CD20 in a heterogeneous staining pattern. The five cases reported showed
also CD20 immunostaining in tumor tissue varied in
staining quantity and intensity. Thus, the positivity for
CD20 in a heterogeneous staining pattern might reflect
the CD20 expression possibly as an activation marker by
neoplastic NK/T cells. Furthermore, in our case, CD30,
another activation marker, was also detected in the tumor
cells. In addition, two of the five cases were CD20 negative in the primary tumors, with acquisition of CD20
© 2017 Japanese Society of Neuropathology
5
expression in dissemination/relapse, which might represent
the clonal evolution of a tumor, or neoplastic NK/T cells
aberrantly acquiring CD20 positivity in tumor progression.
Rituximab, a chimeric monoclonal antibody against
CD20, has been widely used in the treatment of CD20positive B-cell lymphomas. However, the efficacy for
CD20-positive T/NK-cell lymphomas is yet to be known.
Kakinoki et al. proposed that the efficacy of rituximab for
CD20-positive TCL may be associated with intensity of
CD20 expression in tumor T-cells and its homogeneity in
the tumor tissue.31 Unfortunately, none of the six cases
were treated with rituximab. Further clinical studies are
required to determine whether the addition of rituximab
offers any survival advantage to these patients with CD20positive ENKTCL.
Composite clinicopathologic and radiographic evaluation indicated the lesion to be of exclusive left cerebellar
localization. Thus, our case also represented an extremely
rare case of PCNS ENKTCL. Only 10 cases of PCNS
ENKTCL are reported in the literature.3–12 Among the
10 cases, there were seven males and three females, similar to the male predominance of ENKTCL, with a median
age of 43.5 years (range 25 to 68 years), younger than
those patients with ENKTCL (median age, 53 years).
Notably, three cases (3/10) occurred in younger males in
their twenties. Four patients were Chinese, two Spanish,
two African American, one Korean and one Japanese. By
imaging studies, five patients had supratentorial lesions,
one pituitary lesions, one spine lesions, two cerebellar
involvement, two leptomeningeal involvement. Pathologically, they usually exhibited a vascular-centered infiltration
accompanied with vascular damage and coagulative necrosis. The tumor cells typically express CD2, CD56, the cytoplasmic ε chain of CD3 but not surface CD3, as well as
cytotoxic granule proteins. The presence of EBV infection
is nearly invariable. These features were shared by most
of the previous PCNS ENKTCL cases, except for two
cases reported.3,10 In the case by Ng et al., the tumor cells
expressed surface CD3 but not CD56, furthermore, showing evidence of TCR gene monoclonal rearrangement.3
These findings suggest that this case may be better categorized as a PTCL, NOS. In addition, in the case by Liao
et al., EBV infection was not detected in the malignant
cells.10 Therefore, the exact diagnosis of this case may be
questionable. Although ENKTCL often shows the
germline configuration of TCR, five out of eight PCNS
ENKTCL demonstrated monoclonal rearrangement of the
TCR gene. Whether PCNS ENKTCL is more prone to
show monoclonal rearrangement of the TCR gene is
unknown. The molecular genetic characteristics of this
tumor may be worth further study. All cases indicated a
highly aggressive nature and rapid clinical progression,
with a median overall survival of 7 months. Five patients
6
D Li et al.
died within 6 months of diagnosis; the longest survival was
18 months, indicating a poorer prognosis than with extracranial ENKTCL. Therefore, it is important to consider
this rare tumor in the differential diagnosis of CNSL.
In summary, we report the first case of PCNS ENKTCL
with both CD20-positive expression and the monoclonal
rearrangement of IgH gene. This case serves as a cautionary
note regarding the diagnostic pitfalls in determining of the
lineage of non-hodgkin lymphoma (NHL) using only B-cell
or T-cell markers, or gene rearrangement; thus,
histomorphology, more extensive immunoprofiles and
molecular studies are needed for an integrated interpretation
and accurate diagnosis. The rarity of PCNS ENKTCL and
CD20-positive ENKTCL makes it difficult to establish the
prognosis and optimal clinical management of this clinical
entity. Further studies are required to clarify the biologic
and clinical significance of rare lymphomas.
ACKNOWLEDGMENTS
This work was supported by the National Natural Science
Foundation of China (No. 81300215) and the Science and
Technology Research Project of Henan Province
(No. 132102310095).
DISCLOSURES
The authors report no disclosures.
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