International Journal of Gynecological Pathology

00:1–6, Lippincott Williams & Wilkins, Baltimore

Copyright © 2017 by the International Society of Gynecological Pathologists

Original Article

Inflammatory Stroma of Lymphoepithelioma-like Carcinoma

of the Cervix: Immunohistochemical Study of 3 Cases and
Review of the Literature

Amandine Philippe, M.D., Marc Rassy, M.D., Ligia Craciun, Ph.D.,

Céline Naveaux, M.L.T., Karen Willard-Gallo, Ph.D., Denis Larsimont, M.D., PhD,
and Isabelle Veys, M.D.

Summary: The aim of this study was to characterize the inflammatory infiltrate of the
lymphoepithelioma-like carcinoma, a variant of squamous cell carcinoma clinically
associated with a good prognosis. Immunohistochemistry was used to characterize
3 cases of lymphoepithelioma-like carcinoma in the uterine cervix, diagnosed over a
period of 3 yr. The patients were between 30 and 50 yr old. Their cervical smears had
shown atypical squamous cells of unknown significance or high-grade squamous
intraepithelial lesions, and the initial cervical biopsy showed high-grade cervical
intraepithelial neoplasia (CIN3) or squamous cell carcinoma. All patients underwent a
Wertheim operation, 2 of which were preceded by a cervicectomy. Microscopically, all
tumors were characterized by poorly defined sheets of undifferentiated squamous cells
with a syncytial pattern and a dense background of infiltrating lymphocytes.
Immunohistochemical analysis revealed that the lymphocytes were predominantly
CD3+ and CD8+ T cells. The tumor lobules contained isolated CD8+ T cells, whereas
CD4+ T cells and CD20+ B cells surrounded the tumor lobules. CD56+ NK cells and
CD79+ B cells were scattered in the tumor tissue. An in situ hybridization staining for
Epstein-Barr encoding region was negative but all cases were immunohistochemically
positive for P16. Follow-up varied between 2 mo and 2.7 yr. All 3 patients were disease
free. Lymphoepithelioma-like carcinoma of the uterine cervix is a variant of squamous
cell carcinoma, known for its better prognosis. The good prognosis of this tumor is
potentially explained by the high levels of infiltrating CD8+ T cells. Key Words: Uterine
cervix—Lymphoepithelioma-like carcinoma—Immunohistochemistry.

Lymphoepithelioma-like carcinoma is a variant nasopharyngeal undifferentiated carcinoma, which

of squamous cell carcinoma that can be identified
by poorly defined sheets with a syncytial pattern of
undifferentiated squamous cells and a dense background
of tumor-infiltrating lymphocytes. When it occurs in the
head and neck region, this tumor-type is well known as
From the Departments of Pathology (A.P., M.R., L.C., D.L.);
Surgery (I.V.); and Molecular Immunology Unit (C.N., K.W.-G.),
Institut Jules Bordet, Brussels, Belgium.
The authors declare no conflict of interest.
Address correspondence and reprint requests to Isabelle Veys, MD,
Department of Surgery, Institut Jules Bordet, 1 rue Heger-Bordet,
Brussels 1000, Belgium. E-mail: isabelle.veys@bordet.be.
is consistently (but not exclusively) associated with
Epstein-Barr virus (EBV) positivity. Lymphoepithelio-
ma-like carcinoma has also been identified in the uterine
cervix, salivary glands, lung, stomach, trachea, lacrymal
glands, ureters, bladder, vagina, ovaries, breast, soft
tissues, and skin (1) and recently in the penis as medullary
carcinoma (2). The etiology of lymphoepithelioma-like
carcinoma beyond the nasopharynx remains unclear.
Lymphoepithelioma-like carcinoma of the uterine
cervix has been infrequently reported in the literature
in only 2 series and isolated case reports. It represents
0.7% of all primary malignant cervical tumors, (3) and

1 DOI: 10.1097/PGP.0000000000000446

Copyright r 2017 International Society of Gynecological Pathologists.

2 A. PHILIPPE ET AL.

most cases are associated with a low FIGO stage at
diagnosis, a low risk of lymph node metastasis, and a
low recurrence rate (4). To our knowledge, no published
study has thoroughly described the inflammatory stroma
that characterizes this tumor, which could be the key to
its good prognosis.
This study presents 3 recent cases of lymphoepithelioma-
like carcinoma of the cervix in which we performed an
extensive immunohistochemical (IHC) analysis of the
inflammatory infiltrate.
MATERIALS AND METHODS
The institutional ethical committee approved the
study design (reference CE2624).
IHC staining was performed on the Benchmark XT
system (Roche). The list of antibodies used is shown in
Table 1.
For Epstein-Barr encoded RNA (EBER) in situ
hybridization (ISH) staining, the Ventana INFORM
EBER Probe (reference number: 800-2842) was used.
All IHC and ISH stainings were performed according
to the manufacturer’s protocols.
RESULTS
Case 1
The first case was a premenopausal 50-yr-old female
patient, G1P0, with menarche at 10 yr, and no current or
prior hormonal treatment. She was first seen for lower
abdominal pain and vaginal bleeding. An initial cervical
smear showed atypical squamous cells of unknown
significance. Qualitative real-time polymerase chain
reaction (PCR) [Abbott RealTime High-Risk Human
Papillomavirus (HPV)] was positive for HPV 16. A pelvic
magnetic resonance imaging revealed a 17×13 mm
hypointense hypoenhancing cervical lesion. The initial
cervical biopsy showed an invasive nonkeratinizing
squamous cell carcinoma developed on a high-grade
intraepithelial neoplasia (CIN3), clinically classified as
T1b1N0 and FIGO IB1. A concurrent finding was a
13 cm right ovarian tumor, with a serum CA125 level of
211.5 U/mL. The patient underwent a cervicectomy with a
peritoneal wash and bilateral adnexectomy. Cervicectomy
showed an invasive lymphoepithelioma-like carcinoma
reaching the surgical margin. EBER ISH staining was
negative. The peritoneal wash was negative for tumor cells.
The ovarian tumor was a benign Brenner tumor. A
multidisciplinary meeting proposed a Wertheim operation,
which showed a residual lymphoepithelioma-like carcino-
ma of 8 mm, with a 4 mm depth of invasion. Surgical
margins were negative. No lymphovascular emboli were
noted and no lymph node metastases were detected in
1 left and 5 right pelvic lymph nodes. Overall, the tumor
was classified as pT1b1N0 and FIGO IB1. The subsequent
decision by the multidisciplinary meeting was follow-up
and the patient was last seen 76 d following her operation,
with no postoperative complications.
Case 2
The second case was a postmenopausal 44-yr-old
woman, G2P2, treated with a combined vaginal ring
(NuvaRing) and a combined oral drug (Harmonet).
Her past medical history involved a left breast
hamartoma, and she had a familial medical history
of a cousin deceased from breast cancer at 30 yr of age
and a grandfather deceased from lung cancer. Her last
normal cervical smear was 3 yr earlier (2013). An
initial cervical smear showed high-grade squamous
intraepithelial lesions. A pelvic diffusion-weighted mag-
netic resonance imaging showed a posterior hyperintense
nonenhancing anomaly. No extension to the serosa,
vagina, or lymph nodes was seen. The initial cervical
biopsy showed a high-grade intraepithelial neoplasia
(CIN3). The patient underwent a cervicotomy, which
revealed an invasive lymphoepithelioma-like carcinoma
reaching the surgical margins and associated with
lymphovascular emboli. The patient then underwent a
Wertheim operation. The latter showed a lymphoepithe-
lioma-like carcinoma of 8 mm, with a 9 mm depth of
invasion. Surgical margins were negative. No lymph node
metastases were found in 3 left and 6 right pelvic lymph
nodes. Overall, the tumor was classified as pT1bN0 and
FIGO Ib. The decision of the multidisciplinary meeting

TABLE 1. List and Properties of Antibodies Used for Immunohistochemical Staining

Staining Antibody Antibody Reference Clone Host Dilution
Dual staining CD3 DAKO IR503 Polyclonal Rabbit Ready to use
CD20 DAKO IR604 L26 Mouse Ready to use
Dual staining CD4 Imtec BSB 5150 RBT-CD4 Rabbit Ready to use
CD8 DAKO IS623 C8/144B Mouse Ready to use
Single staining CD68 DAKO IS609 KP1 Mouse Ready to use
Single staining CD163 Cell Marque 163M-18 MRQ-26 Mouse Ready to use
Single staining P16 Ventana 725-4713 E6H4 Mouse Ready to use

Int J Gynecol Pathol Vol. 00, No. 00, ’’ 2017

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 LYMPHOEPITHELIOMA-LIKE CARCINOMA OF THE CERVIX
was follow-up. The patient was last seen 154 d after her
operation with no postoperative complications.
Case 3
The third case was a premenopausal 32-yr-old woman,
G1P1, with menarche at 14 yr, and no current or prior
hormonal treatment. Her past medical history included a
resected endometrial polyp 3 yr ago. No familial medical
history was known. She was first seen for postcoital
vaginal bleeding over 3 to 4 mo. Her last normal cervical
smear dates back 1.5 yr (2015). A pelvic US revealed a
hypoechogenic heterogenous cervical lesion, measuring
23×11×15 mm. A pelvic magnetic resonance imaging
showed a 26×19×11 mm lesion of the anterior exocervix.
The initial cervical biopsy showed an invasive non-
keratinizing moderately differentiated squamous cell
carcinoma, clinically classified as T1b1N0. The tumor
consisted of solid nests of tumor cells with a heavy
chronic inflammatory infiltrate. The patient underwent a
total hysterectomy with bilateral salpingectomy and
bilateral interiliac lymphadenectomy. The latter showed
a cervical invasive nonkeratinizing squamous cell carci-
noma of 32 mm, with a 10 mm depth of invasion. A
FIG. 1. Hematoxylin and eosin (HE) staining identifies the tumor lobules, trapped within the inflammatory infiltrate. The CD3/CD20 (brown/red)
staining shows a predominance of CD3+ T cells with a few CD20+ B cell clusters. CD4+ T cells are detected principally around tumor lobules,
whereas CD8+ T cells are seen both around and within tumor lobules.
Copyright r 2017 International Society of Gynecological Pathologists.
3
lymphoepithelioma-like component was found within the
tumor, as well as a background of high-grade intra-
epithelial neoplasia (CIN3). No lymphovascular emboli
were noted. EBER ISH staining was negative. No lymph
node metastases were found (in 9 left and 8 right iliac
lymph nodes). Overall, the tumor was classified as
pT1b1N0 and FIGO IB1. The decision of the multi-
dsciplinary meeting was follow-up. The patient was last
seen 2.7 yr after her operation, with no postoperative
complications. A follow-up qualitative real-time PCR
(Abbott RealTime High-Risk HPV) was negative.
IHC staining of tumor tissue sections was per-
formed for all 3 cases. A predominance of CD3+ T
cells compared with CD20+ B cells was observed in all
cases, similar to that observed in most tumor immune
infiltrates. The CD20+ B cells were confined to small
clusters around the tumor lobules. The CD3+ T cells
were further examined for their distinction between
CD8+ cytotoxic T cells and CD4+ helper T cells.
CD8+ T cells were found within the tumor lobules,
around the tumor lobules, and throughout the entire
tumor bed. CD4+ T cells were principally located
around the tumor lobules and around the whole
tumor. Figure 1 shows images that reflect these IHC
Int J Gynecol Pathol Vol. 00, No. 00, ’’ 2017
4 A. PHILIPPE ET AL.
findings. Scattered CD68+ and CD163+ inflammatory
cells from the monocyte/macrophage lineage were
also detected. All of the tumors were negative for
EBER ISH staining and positive for P16 using
immunohistochemistry. As previously reported, cases
1 and 3 were tested for HPV by PCR with only the
former being positive for HPV16.
DISCUSSION
Lymphoepithelioma-like carcinoma of the cervix
(LELC) is characterized by a syncytial growth pattern
and a dense lymphocytic infiltrate. Only few series and
case reports have been published for this rare tumor
type that accounts for approximatively 0.7% of all
primary malignant cervical tumors (3). We found <50
cases reported from 1993 to 2016. The age at
diagnosis ranges between 21 (5) and 79 yr (6),
averaging 52.9 yr, which is lower than that of cervical
conventional squamous cell carcinoma (7). Most
patients are multiparous. Past medical and surgical
history are irrelevant. Clinical presentation is similar
to that of cervical conventional squamous cell
carcinoma, with most patients complaining of vaginal
bleeding (7). Clinical examination reveals an exo-
phytic mass or an ulcerative lesion (7). The initial
investigation leading to the final diagnosis of LELC of
the cervix is most frequently a positive biopsy,
preceded or not by an abnormal cervical smear (8).
On gross examination, the tumor is relatively small
and well circumscribed (9). On microscopic examina-
tion, the hallmarks of the LELC are as follows: the
syncytial-like growth pattern; sheets and nests of tumor
cells; undifferentiated cells with poorly defined margins,
large nuclei, finely granular or clear chromatin, and
variably prominent nucleoli; and a dense inflammatory
infiltrate consisting mainly of small lymphocytes and
occasional plasma cells (10). Our 3 cases meet the
clinical presentation described in the literature.
As with regards to the inflammatory background,
only a few studies have described the nature and the
topography of the inflammatory infiltrate. Lymphocytes
have been predominantly identified as CD8+ (4,10) and
CD3+ (4,6,10–12) T cells. A minority are CD4+ T cells
(4,10), CD20+ B cells (4,6,10–13), CD56+ NK cells (4),
and CD79+ B cells (4,10). The coexistence of abundant
CD3+ T cells and CD20+ B cells within clusters is highly
suggestive of tertiary lymphoid structures (14). In the
cervix, Trimble et al. (15) have shown that tertiary
lymphoid structures form in response to E6/E7 vacci-
nation. Our study goes further by describing the
distribution of infiltrating lymphocytes in tumor lobules,
Int J Gynecol Pathol Vol. 00, No. 00, ’’ 2017
Copyright r 2017 International Society of Gynecological Pathologists.
around tumor lobules, and/or around the entire tumor.
The CD8+ T cells were the only immune cells found in
the tumor lobules and were hence considered true
tumor-infiltrating lymphocytes. The CD4+ T cells were
found around the tumor lobules and thus may play
a role in providing the all-important help for CD8+
T cell functions. Contributions from the various immune
cell populations, as well as their distribution within
and around the tumor lobules, may play a key role in
confining the lesion.
In order to further assess the implication of CD8+
T cells, we have screened the literature for papers
reporting lymphoepithelioma-like carcinomas and CD8
immunostaining. Overall, lymphoepithelioma-like carci-
noma differs from one organ to another. Most reported
cases in the lung (16–18), the stomach (19–21), the
endometrium, (22) and the esophagus (23) display a
predominance of CD8+ T cells, around and within tumor
lobules. In other organs like the skin (24–26), the liver
(27–29), the urinary bladder (30,31) and the salivary
glands (32), cases varied between CD4+ T cell predom-
inant and CD8+ T cell predominant, around and within
tumor lobules. Among these papers, the CD8+ T cells
were attributed a role in host defense mechanisms,
bringing a favorable prognosis in the uterine cervix (4),
the lung (17), the stomach (19), the urinary bladder (31),
the esophagus (33), and in the liver (29).
EBV positivity (tested by PCR) has been demonstrated
in 24 cases, including 9 cases with low copy numbers
detected by genomic DNA QPCR and a negative EBER
status (tested by ISH) (34,35). EBV status was negative
(tested by IHC or ISH only) in 3 patients (3,8,13) and
negative (tested by PCR) in 12 patients, including 2
patients with an additional negative EBV ISH (4,5,35-
–37). EBER status was negative (tested by ISH) in 8
patients, 2 of whom had negative EBV status (tested by
PCR) (6,10,11,38–40). LMP-1 was tested by immunohis-
tochemistry and was found to be negative in 6 of the
EBER-negative patients (6,10,11,39). Only one reported
case was tested for P16 by immunohistochemistry, and it
was found to be positive (1/1) (40). Four patients tested
for SV40 by PCR were all negative (4). HPV status was
positive (tested by PCR) in 13 patients (34,35,38,41) and
negative in 27 patients (4–6,10,13,34–36,39,42), among
which 20 were tested by PCR, 4 by IHC or ISH, and 3 by
an unspecified technique. Our 3 cases were negative for
EBER ISH staining and had a consistent positive P16
IHC staining, with 1 case being also positive by PCR for
HPV16, another negative, and the third untested. We
believe the 3 hereby reported tumors to be HPV related.
The tumor suppressor protein P16 (P16INK4A) is
considered a biomarker for transforming HPV infections.
 LYMPHOEPITHELIOMA-LIKE CARCINOMA OF THE CERVIX
P16 is expressed in infected cells in an attempt by the
virus to counteract the irregular cell cycle activation. The
latter occurs when the viral oncogene E7 dissociates
binding of retinoblastoma (pRb) protein to the E2F
transcription factor. However, cell cycle activation is not
affected by P16, leading to its overexpression and nuclear
and cytoplasmic accumulation (43). The correlation
between IHC expression of P16 by the E6H4 clone and
the presence of high-risk HPV (detected by PCR) has
been documented: Klaes et al. (44) reported 60 cases of
uterine cervix squamous cell carcinoma, in which 58 were
positive for P16 by IHC and 53 for high-risk HPV
by PCR.
LELC of the cervix is characterized by a low FIGO
stage at diagnosis: stage IB (80.4%) (3–8,10,13,34–36,
38–41,45), IIA (8.7%) (4,10,35), and IIB (10.9%) (12,35).
All of the reported cases were treated by radical
hysterectomy and bilateral lymphadenectomy, except
for 5 patients in the Tseng et al. (35) study, who received
radiotherapy and intracavitary brachytherapy. Only 10%
of the reported cases received adjuvant treatment:
radiotherapy (3.3%) (34), curitherapy (3.3%) (6), and
combined chemotherapy (6 cycles of Paclitaxel and
Carboplatin) and external beam radiation therapy (50
Gy) (3.3%) (3). Only one reported case (2.2%) had a
recurrence, at 2 yr as a lymph node metastasis, whereas
the follow-up of other cases ranged from 4 mo to over 8
yr (3,4,6,7,10–13,34–36,38–40,42,45). The cases reported
here have a follow-up ranging from 2 mo to almost 3 yr.
No complication or recurrence has occurred, even in the
absence of adjuvant treatment.
CONCLUSIONS
We have hereby reported a specific distribution of
the inflammatory infiltrate of LELC of the uterine
cervix. The high proportion of CD8+ tumor-infiltrat-
ing lymphocytes can explain the good prognosis of
this variant of an otherwise known aggressive
squamous cell carcinoma. Nevertheless, the contrib-
ution of the peritumoral CD4+ T cells and CD20+ B
cells cannot be underestimated. Additional studies are
required to investigate the interactions between these
different lymphocyte populations.
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