Lymphoepithelioma-like, a variant of urothelial carcinoma of the urinary bladder: a case report and systematic review for optimal treatment modality for disease-free survival

Abstract

Background
Lymphoepithelioma-like carcinoma (LELC) is a rare high-grade carcinoma that resembles nasopharyngeal lymphoepithelioma and can occur throughout the body. First reported in 1991, bladder LELC has an incidence of about 1% of all bladder carcinomas. Due to its rare occurrence, prognoses and ideal treatment guidelines have not been clearly defined. MethodsA PubMed search was performed using two terms, “lymphoepithelioma-like carcinoma” and “bladder.” Review articles, articles in foreign languages, expression studies, and studies not performed in the bladder were excluded. We report a case of LELC of the bladder including treatment and outcome and performed a systematic review of all 36 available English literatures from 1991 to 2016 including the present case to identify factors affecting disease-free survival. ResultsOne hundred forty cases of bladder LELC were analyzed. The mean age of the patients was 70.1 years ranging from 43 to 90 years with 72% males and 28% females. Pure LELC occurs most often at 46% followed by mixed LELC 28% and predominant LELC 26%. EBV testing was negative in all cases tested. Mean follow-up length for all cases was 33.8 months with no evidence of disease in 62.2%, while 11.1% died of disease, 10.4% alive with metastasis, and 8.2% died without disease. 5.0% of cases had recurrence at an average of 31.3 months. Prognosis is significantly favorable for patients presenting with pure or predominant forms of LELC compared to mixed type (p < 0.0001). The treatment significantly associated with the highest disease mortality and lowest disease-free survival was TURBT alone when compared to any multi-modality treatment (p < 0.01). Conclusion
We conclude that the best treatment modality associated with the highest disease-free survival is multi-modal treatment including radical cystectomy.

Full text

R E S E A R C H A R T I C L E Open Access
Lymphoepithelioma-like, a variant of
urothelial carcinoma of the urinary bladder:
a case report and systematic review for
optimal treatment modality for disease-free
survival
Andy W. Yang
*
, Aydin Pooli, Subodh M. Lele, Ina W. Kim, Judson D. Davies and Chad A. LaGrange
Abstract
Background: Lymphoepithelioma-like carcinoma (LELC) is a rare high-grade carcinoma that resembles nasopharyngeal
lymphoepithelioma and can occur throughout the body. First reported in 1991, bladder LELC has an incidence of
about 1% of all bladder carcinomas. Due to its rare occurrence, prognoses and ideal treatment guidelines have not
been clearly defined.
Methods: A PubMed search was performed using two terms, “lymphoepithelioma-like carcinoma”and “bladder.”
Review articles, articles in foreign languages, expression studies, and studies not performed in the bladder were
excluded. We report a case of LELC of the bladder including treatment and outcome and performed a systematic
review of all 36 available English literatures from 1991 to 2016 including the present case to identify factors
affecting disease-free survival.
Results: OnehundredfortycasesofbladderLELCwereanalyzed.Themeanageofthepatientswas70.1years
ranging from 43 to 90 years with 72% males and 28% females. Pure LELC occurs most often at 46% followed by
mixed LELC 28% and predominant LELC 26%. EBV testing was negative in all cases tested. Mean follow-up length
for all cases was 33.8 months with no evidence of disease in 62.2%, while 11.1% died of disease, 10.4% alive with
metastasis, and 8.2% died without disease. 5.0% of cases had recurrence at an average of 31.3 months. Prognosis
is significantly favorable for patients presenting with pure or predominant forms of LELC compared to mixed
type (p< 0.0001). The treatment significantly associated with the highest disease mortality and lowest disease-free
survival was TURBT alone when compared to any multi-modality treatment (p< 0.01).
Conclusion: We conclude that the best treatment modality associated with the highest disease-free survival is
multi-modal treatment including radical cystectomy.
Keywords: Lymphoepithelioma-like carcinoma, Bladder tumor, Systematic review, Case report
* Correspondence: ayang@unmc.edu
Division of Urologic Surgery, University of Nebraska Medical Center, Omaha,
NE, USA
© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Yang et al. BMC Urology (2017) 17:34
DOI 10.1186/s12894-017-0224-4
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Background
Lymphoepithelioma-like carcinoma (LELC) is a rare
high-grade carcinoma that resembles nasopharyngeal
lymphoepithelioma and has been reported to occur in
other sites of the body such as gastrointestinal tract [1],
liver [2], lung [3], skin [4], uterus [5], gallbladder [6],
pancreas [7], kidney [8], and breast [9]. First reported in
1991 [10], LELC of the bladder appears to resemble
LELC histologically in the nasopharynx but is actually a
variant of urothelial carcinoma and has an incidence of
about 1% of all bladder carcinomas [11]. Unlike other
sites of the body, LELC in the bladder has not been asso-
ciated with the presence of Epstein-Barr Virus to date
[12]. Due to its rare occurrence, prognoses and ideal
treatment guidelines have not been clearly defined. We
report a case of LELC in the bladder and performed a
systematic review of all available English literature in-
cluding the present case to evaluate factors affecting
disease-free survival.
Methods
A PubMed search was performed using two terms, “lym-
phoepithelioma-like carcinoma”and “bladder.”Of the 63
results generated as of July 18th, 2016, 27 review articles,
articles in foreign languages, expression studies, and
studies not performed in the urinary bladder were ex-
cluded. Attempts were made to translate foreign articles
to minimize bias but it was unsuccessful. Potential bias
due to language barrier should be minimal. A total of
140 patients, including the present case, were collected
from 36 published English articles from 1991 to 2016
[10, 11, 13–46]. Preferred reporting items for systematic
review and meta-analysis protocols (PRISMA-P) 2015
guidelines were followed including creation of a protocol
available upon request [47]. Patient data collected
include gender, age, chief complaint, LELC type, TNM
staging, EBV status, primary treatment, secondary treat-
ment, neoadjuvant therapy used, follow-up time in
months, recurrence time in months, and outcome. Stud-
ies with insufficient information for particular data were
excluded from that particular statistical analysis to re-
duce bias. LELC classification criteria was described by
Amin et al. with pure being 100% of the tumor showed
LELC pattern, pre-dominant being ≥50% mixed with
another type of tumor pattern, and mixed being < 50%
mixed with another type of tumor pattern. Student’st-
test was performed for statistical analysis.
Case report
A 69-year-old African American female presented in
February 2015 in our department with the chief complaint
of gross hematuria and dysuria that started in December
2014. Prior to urology evaluation, she had received two
courses of antibiotics without resolution for her
presenting symptoms. The patient denied history of uro-
logic trauma, nephrolithiasis, chronic Foley catheter, fam-
ily history of genitourinary (GU) malignancy, or previous
GU surgeries. The patient had a history of stage IA adeno-
carcinoma of the right upper lung in 2011 and a 20-pack
year history of smoking.
Cystoscopy revealed a large complex bladder mass on
the right lateral wall and right trigone involving the right
ureteral orifice. Abdominal and pelvic CT scan revealed
right-sided bladder mass involving the right ureterovesical
junction, right hydronephrosis and right-sided pelvic
lymphadenopathy. Transurethral resection of the bladder
tumor (TURBT) was performed and pathologic examin-
ation showed a prominent inflammatory background with
admixed high-grade undifferentiated tumor cells arranged
in sheets with ill-defined cytoplasmic borders imparting a
syncytial appearance diagnostic of the LEL variant of
urothelial carcinoma (Fig 1a and b). Foci of urothelial car-
cinoma in situ were also noted involving the surface
urothelium. Muscularis propria invasion was present.
Patient was treated with four cycles of neoadjuvant
chemotherapy of gemcitabine and cisplatin. Repeat CT
two weeks after the last round of chemotherapy revealed
smaller right-sided bladder mass (6.1 x 2.9 cm vs. 6.9 x
3.4 cm). Two months after the last round of chemother-
apy, the patient underwent a radical cystectomy with
ileal conduit diversion and pelvic lymph node dissection
in July 2015. The operation was complicated by exten-
sive adhesions from previous appendectomy, hysterec-
tomy, and hernia repair with ventral mesh placement
necessitating small bowel resection.
Final pathology report showed three high-grade tumor
foci in the bladder with the largest being high-grade
urothelial carcinoma located in the right lateral wall
measuring 2.8 cm, another tumor located in the poster-
ior wall measuring 0.9 cm with areas of squamous differ-
entiation, and the smallest tumor located at the dome
measuring 0.6 cm with pathology consistent with LEL
urothelial carcinoma. The LEL variant of urothelial car-
cinoma is rare and diagnosed by the presence of high-
grade/poorly differentiated tumor cells admixed with a
prominent inflammatory cell infiltrate. The tumor cells
have high nuclear:cytoplasmic ratios and indistinct cyto-
plasmic borders imparting a syncytium-like appearance.
The overall appearance is similar to the lymphoepithe-
liomas typically seen in the nasopharyngeal region. They
can be seen in the bladder either in the pure form or
admixed with more usual forms of high-grade urothelial
carcinoma, as seen in the present case. One obturator
lymph node was positive for metastatic urothelial carcin-
oma (1/17 nodes positive). All surgical margins were
negative. Final pathology staging was pT3bN1MX.
Patient had an uneventful recovery and was discharged
on post-operative day 12 to a skilled nursing facility.
Yang et al. BMC Urology (2017) 17:34 Page 2 of 6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Repeat abdominal and pelvis CT at 9 weeks post-op
showed no mass, lymphadenopathy, or destructive osse-
ous lesions. Patient reported improvement in appetite
and normal bowel movement with persistent mild ab-
dominal pain. However, lung cancer follow-up chest CT
in September 2015 revealed a new 3 mm left upper lobe
nodule not present in preoperative chest CT in June
2015. Repeat chest CT in February 2016 showed left
upper lobe nodule enlarged to 12 mm. CT-guided needle
biopsy showed CK7+, p40+, and GATA3+ tumor cells
similar to morphology of previous bladder cancer, con-
sistent with metastatic urothelial carcinoma. Multiple
new liver lesions were present on repeat CT in April
2016. Patient unfortunately died with metastases in
October 2016.
Results
One hundred forty cases of LELC in the bladder includ-
ing the present case were reported between 1991 and
2016. The mean age of the patients was 70.1 years ran-
ging from 43 to 90 years with 57% males, 22% females,
and 21% unknown; of those with known genders, 72%
were male and 28% female (Table 1). Primary presenta-
tion was gross hematuria in 53% of patients. Mean
Fig. 1 Note the (a) high-grade carcinoma cells with large nuclei, irregular nuclear borders and prominent nucleoli present in small aggregates
and also (b) singly with ill-defined cytoplasmic borders imparting a syncytium-like pattern and admixed with numerous inflammatory cells, typical
of a lymphoepithelioma-like urothelial carcinoma. Original magnification X400; hematoxylin and eosin stain
Table 1 LELC cases from 36 published English literature from 1991–2016 including the present case with demographic breakdown
Reference Case(s) Reference Case(s)
Zukerberg et al., 1991 [10] 1 Guresci et al., 2009 [22]1
Young et al., 1991 [44] 1 Singh et al., 2009 [35]1
Dinney et al., 1993 [19] 3 Trabelsi et al., 2009 [39]1
Amin et al., 1994 [13] 11 Yun et al., 2010 [45]1
Bianchini et al., 1996 [14] 1 Kozyrakis et al., 2011 [26]6
Holmang et al., 1998 [23] 9 Williamson et al., 2011 [41]33
Constantinides et al., 2001 [18] 3 Pantelides et al., 2012 [32]1
Lopez-B et al., 2001 [11] 13 Mori et al., 2013 [30]1
Ward et al., 2002 [40] 1 Spinelli et al., 2013 [36]1
Porcaro et al., 2003 [33] 1 Yoshino et al., 2014 [43]1
Chen et al., 2003 [16] 2 Ziouziou et al., 2014 [46]1
Izuquierdo et al., 2004 [24] 3 Kushida et al., 2015 [27]1
Guresci et al., 2005 [21] 1 Kessler et al., 2015 [25]1
Yaqoob et al., 2005 [42] 1 Mina et al., 2015 [29]1
Mayer et al., 2007 [28] 1 Raphael et al., 2015 [34]1
Tamas et al., 2007 [38] 29 Nagai et al., 2016 [31]1
Cai et al., 2008 [15] 2 Stamatiou et al., 2016 [37]1
Chikwava et al., 2008 [17] 1 Yang et al., 2017 1
Fadare et al., 2009 [20] 1 Total 140
Age Range 43–90 Male 72%
Average Age 70.1 Female 28%
Yang et al. BMC Urology (2017) 17:34 Page 3 of 6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

follow-up length for all cases was 33.8 months with no
evidence of disease in 62.2%, while 11.1% died of disease,
10.4% alive with metastasis, 8.2% died without disease,
and 8.2% lost to follow-up. 5.0% of cases had recurrence
at an average of 31.3 months. Pure LELC occurs most
often at 46% (62 cases) followed by mixed LELC 28% (38
cases) and predominant LELC 26% (36 cases). Patho-
logical staging of the tumor was pT1 in 10.1% (14 cases),
pT2 in 56.1% (78 cases), pT3 in 30.9% (43 cases), and
pT4 in 2.9% (4 cases). Lymph node metastasis was
present in 13.6% of patients, with distant metastasis
noted in 5.7%. EBV testing was performed in 51.4% of
the cases and was negative in all cases.
Comparing treatment modality, 50% of the cases uti-
lized one treatment modality only with radical cystec-
tomy being the most common (58.6%) followed by
TURBT (30.0%), partial cystectomy (7.1%), and intravesi-
cal chemotherapy (1.4%) with outcomes of no evidence
of disease (55.7%), died of disease (12.9%), alive with
metastasis (10.0%), and died without disease (7.1%). Of
the multi-modality treatments, primary treatments were
diverse and included TURBT (49.9%), radical cystectomy
(41.0%), partial cystectomy (6.0%), intravesical chemo-
therapy (1.5%), chemotherapy (0.8%), and radiation
therapy (0.8%). Secondary treatments included chemo-
therapy (51.8%), radiation therapy (28.2%), TURBT
(7.1%), intravesical chemotherapy (7.1%), radical cystec-
tomy (4.7%), and thermal ablation (1.2%). Outcomes for
those receiving multi-modal treatments include no evi-
dence of disease (67.2%), alive with metastasis (10.5%),
died without disease (9.0%), and died of disease
(7.5%) (Table 2).
Comparing surgical resection methods, TURBT alone
has the lowest disease-free survival rate (33.3%) when
compared to any combination therapy (67.9%) (p< 0.01);
TURBT alone also carries the highest mortality rate
(23.8%) when compared to any combination therapy (7.1%,
p< 0.05). Radical cystectomy is associated with the highest
disease-free survival rate at 67.8% and is significant when
compared to TURBT alone at 33.3% (p< 0.01) but not sig-
nificant when compared to partial cystectomy at 50%.
Systematic chemotherapy treatments utilized are varied
with 24 cases documenting detailed regiments. Of those,
eight cases specified MVAC treatments while 16 cases
specified GC treatments. Neoadjuvant chemotherapy was
administered in 4.3% of cases with an average disease-free
survival of 41 months and did not significantly impact
outcome. Comparing subtypes of LELC, the treatment
regiments reported did not significantly differ; of those
with pure and predominant LELC, 71.0% and 75.0% had
no evidence of disease, respectively, while only 31.6% of
mixed LELC patients had the same outcome (p< 0.0001,
Table 3). In addition, patients who underwent radical
cystectomy had the highest disease-free survival (67.8%,
p< 0.01) when compared to partial cystectomies (50%)
or TURBT only (33.3%). However, patients receiving
TURBT combined with any type of secondary treatment
have a 71.1% disease-free survival rate.
Discussion
LELC of the bladder is a rare cancer that most often pre-
sents with painless hematuria occurring in older males. By
the time of presentation, most LELCs have invaded the
muscularis propia but have not metastasized outside of
the bladder. Even though LELC in other organ systems
has been shown to be associated with EBV, no case of
LELC in the bladder has been associated with the pres-
ence of EBV. The subtypes of LELC appear to significantly
impact outcome, as disease-free survival is higher in pre-
dominant and pure LELC than mixed LELC. Highest mor-
tality is mixed LELC followed by predominant and pure
LELC and this could suggest that LELC itself is not as
aggressive as high-grade urothelial carcinoma.
As for treatment impacting outcome, TURBT alone
should not be recommended, as it is associated with both
lowest disease-free survival and highest mortality rate.
Radical cystectomy is associated with the highest disease-
free survival rate, whereas partial cystectomy was only uti-
lized as the main surgical resection method in eight cases
its impact is unknown. As for neoadjuvant chemotherapy,
it was administered in six cases and while it had a longer
Table 2 Outcomes of all cases comparing single vs. multi-modal
treatment modality
Treatments NED AWM DOD DWD
Single 55.7% 10.0% 12.9% 7.1%
Multi 67.2% 10.5% 7.5% 9.0%
Overall 62.2% 10.4% 11.1% 8.2%
NED no evidence of disease, AWM alive with metastasis, DOD died of disease,
DWD died without disease
Table 3 Outcomes for LELC types and treatment modalities
LELC Type Cases NED p-value DOD p-value
Pure 62 71.0% 0.00002 1.6% 0.0001
Predominant 36 75.0% 0.00002 5.6% 0.002
Mixed 38 31.6% - 28.9% -
Treatment Cases NED p-value DOD p-value
MM 112 67.9% 0.002 7.1% 0.04
RC+ 59 67.8% 0.002 10.2% 0.08
PC+ 8 50.0% 0.21 12.5% 0.22
TURBT+ 45 71.1% 0.002 2.2% 0.012
TURBT−21 33.3% - 23.8% -
p-values calculated against mixed type and against TURBT-only
NED no evidence of disease, DOD died of disease, MM multi-modality overall
treatments including RC+, PC+, and TURBT+; RC+, radical cystectomy + adjuvant
therapy, PC+ partial c ystectomy + adjuva nt therapy , TURBT+ transurethral
resection of the bladder + adjuvant therapy, TURBT- transurethral resection
of the bladder only
Yang et al. BMC Urology (2017) 17:34 Page 4 of 6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

disease survival, it was not significant, perhaps also due to
the small sample size. As for chemotherapy regiment, it
appears to have evolved over time and without significant
difference as all eight cases of MVAC were before 2003
and all 16 cases of GC were after.
To define best treatment strategy for rare diseases is
difficult as rare diseases are best evaluated in a prospect-
ive registry. Even though LELC in the bladder is rare
and there is currently no clear treatment guideline, our
study suggests that a combination therapy including rad-
ical cystectomy would possibly yield the best outcome.
Conclusion
LELC of the bladder is a rare cancer that most often oc-
curs in older males. Of the three subtypes, mixed LELC
carries the highest mortality rate and TURBT alone or
any single treatment is not recommended for therapy as
it is associated with both the highest mortality rate and
the lowest disease-free survival rate. Prognosis is favor-
able for patients presenting with pure or predominant
forms of LELC and those undergoing combination ther-
apies that include radical cystectomy while the impact of
neoadjuvant chemotherapy is yet undetermined.
Abbreviations
GU: Genitourinary; LELC: Lymphoepithelioma-like carcinoma; TURBT: Trans-
urethral resection of bladder tumor.
Acknowledgement
Not applicable.
Availability of data and materials
All original articles can be obtained via a PubMed search.
Authors’contributions
AWY collected and compiled the data, performed the analysis, drafted,
prepared, edited, and submitted the manuscript. AP contributed to the
manuscript. SML performed the pathology study and prepared the images
and pathological sections of the manuscript. IWK contributed to the
manuscript and treated the patient. JDD treated the patient and performed
the surgery. CAL contributed to the manuscript and directed the project. All
authors read and approved the final manuscript.
Competing interests
The authors declare that they have no competing interests.
Ethics approval and consent to participate
Consent was obtained from the patient for research and publication. IRB was
not required for a case report.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Received: 5 September 2016 Accepted: 20 April 2017
References
1. Kang BW, Seo AN, Yoon S, Bae HI, Jeon SW, Kwon OK, Chung HY, Yu W, Kim
JG. Prognostic value of tumor-infiltrating lymphocytes in Epstein-Barr Virus-
associated gastric cancer. Ann Oncol. 2016;27(3):494–501.
2. Wei J, Liu Q, Wang C, Yu S. Lymphoepithelioma-like hepatocellular
carcinoma without Epstein-Barr Virus infection: A case report and a review
of the literature. Indian J Pathol Microbiol. 2015;58(4):550–3.
3. Wang L, Lin Y, Cai Q, Long H, Zhang Y, Rong T, Ma G, Liang Y. Detection of
rearrangement of anaplastic lymphoma kinase (ALK) and mutation of
epidermal growth factor receptor (EGFR) in primary pulmonary
lymphoepithelioma-like carcinoma. J Thorac Dis. 2015;7(9):1556–62.
4. Lee J, Park J, Chang H. Lymphoepithelioma-like carcinoma of the skin in the
cheek with a malignant metastatic cervical lymph node. Arch Plast Surg.
2015;42(5):668–71.
5. Makannavar JH, KishanPrasad HL, Shetty JK. Lymphoepithelioma-like carcinoma
of endometrium: A rare case report. Indian J Surg Oncol. 2015;6(2):130–4.
6. Sinha PK, Mangla V, Behari C, Rastogi A, Chattopdhyay TK.
Lymphoepithelioma-like carcinoma: An unusual gall bladder tumor. Trop
Gastroenterol. 2014;35(3):182–3.
7. Samdani RT, Hetchman JF, O’Reilly E, DeMatteo R, Sigel CS. EBC-associated
Lymphoepithelioma-like carcinoma of the pancreas: Case report with
targeted sequencing analysis. Pancreatology. 2015;15(3):302–4.
8. Ahn H, Sim J, Kim H, Yi K, Han H, Chung Y, Rehman A, Paik SS.
Lymphoepithelioma-like carcinoma of the renal pelvis: A case report and
review of the literature. Korean J Pathol. 2014;48(60):458–61.
9. Suzuki I, Chakkabat P, Goicochea L, Campassi C, Chumsri S. Lymphoepithelioma-
like carcinoma of the breast presenting as breast abscess. World J Clin Oncol.
2014;5(5):1107–12.
10. Zukerberg LR, Harris NL, Young RH. Carcinomas of the urinary bladder
simulating malignant lymphoma. A report of five cases. Am J Surg Pathol.
1991;15(6):569–76.
11. Lopez-Beltrán A, Luque RJ, Vicioso L, Anglada F, Requena MJ, Quintero A,
Montironi R. Lymphoepithelioma-like carcinoma of the urinary bladder: a
clinicopathologic study of 13 cases. Virchows Arch. 2001;438(6):552–7.
12. Gulley ML, Amin MB, Nicholls JM, Banks PM, Ayala AG, Srigley JR, Eagan PA,
Ro JY. Epstein-Barr virus is detected in undifferentiated nasopharyngeal
carcinoma but not in lymphoepithelioma-like carcinoma of the urinary
bladder. Hum Pathol. 1995;26(11):1207–14.
13. Amin MB, Ro JY, Lee KM, Ordóñez NG, Dinney CP, Gulley ML, Ayala AG.
Lymphoepithelioma-like carcinoma of the urinary bladder. Am J Surg
Pathol. 1994;18(5):466–73.
14. Bianchini E, Lisato L, Rimondi AP, Pegoraro V. Lymphoepithelioma-like
carcinoma of the urinary bladder. J Urol Pathol. 1996;5:45–9.
15. Cai G, Parwani AV. Cytomorphology of lymphoepithelioma-like carcinoma of
the urinary bladder: report of two cases. Diagn Cytopathol. 2008;36(8):600–3.
16. Chen KC, Yeh SD, Fang CL, Chiang HS, Chen YK. Lymphoepithelioma-like
carcinoma of the urinary bladder. J Formos Med Assoc. 2003;102(10):722–5.
17. Chikwava KR, Gingrich JR, Parwani AV. Lymphoepithelioma-like carcinoma of
the urinary bladder. Pathology. 2008;40(3):310–1.
18. Constantinides C, Giannopoulos A, Kyriakou G, Androulaki A, Ioannou M,
Dimopoulos M, Kyroudi A. Lymphoepithelioma-like carcinoma of the
bladder. BJU Int. 2001;87(1):121–2.
19. Dinney CP, Ro JY, Babaian RJ, Johnson DE. Lymphoepithelioma of the
bladder: a clinicopathological study of 3 cases. J Urol. 1993;149(4):840–1.
20. Fadare O, Renshaw IL, Rubin C. Pleomorphic lymphoepithelioma-like
carcinoma of the urinary bladder. Int J Clin Exp Pathol. 2009;2(2):194–9.
21. Guresci S, Doganay L, Altaner S, Atakan HI, Kutlu K. Lymphoepithelioma-like
carcinoma of the urinary bladder: a case report and discussion of differential
diagnosis. Int Urol Nephrol. 2005;37(1):65–8.
22. Guresci S, Simsek G, Kara C, Tezer A, Bozkurt O, Unsal A. Cytology of
lymphoepithelioma-like carcinoma of the urinary bladder. Cytopathology.
2009;20(4):268–9.
23. Holmäng S, Borghede G, Johansson SL. Bladder carcinoma with
lymphoepithelioma-like differentiation: a report of 9 cases. J Urol. 1998;
159(3):779–82.
24. Izquierdo-García FM, García-Díez F, Fernández I, Pérez-Rosado A, Sáez A,
Suárez-Vilela D, Guerreiro-González R, Benéitez-Alvarez M. Lymphoepithelioma-
like carcinoma of the bladder: three cases with clinicopathological and p53
protein expression study. Virchows Arch. 2004;444(5):420–5.
25. Kessler ER, Amini A, Wilson SS, Breaker K, Raben D, La Rosa FG.
Lymphoepithelioma-like carcinoma of the urinary bladder. Oncology
(Williston Park). 2015;29(6):462. C3.
26. Kozyrakis D, Petraki C, Prombonas I, Grigorakis A, Kanellis G, Malovrouvas D.
Lymphoepithelioma-like bladder cancer: clinicopathologic study of six cases.
Int J Urol. 2011;18(10):731–4.
Yang et al. BMC Urology (2017) 17:34 Page 5 of 6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

27. Kushida N, Kushakabe T, Kataoka M, Kumagai S, Aikawa K, Kojima Y. External
beam radiotherapy for focal lymphoepithelioma-like carcinoma in the urinary
bladder: a case report and literature review. Case Rep Oncol. 2015;8(1):15–20.
28. Mayer EK, Beckley I, Winkler MH. Lymphoepithelioma-like carcinoma of the urinary
bladder–diagnostic and clinical implications. Nat Clin Pract Urol. 2007;4(3):167–71.
29. Mina SN, Antonios SN. Lymphoepithelioma-like carcinoma of the urinary
bladder associated with schistosomiasis: A case report and review of
literature. J Egypt Soc Parasitol. 2015;45(2):385–8.
30. Mori K, Ando T, Nomura T, Sato F, Mimata H. Lymphoepithelioma-like
carcinoma of the bladder: A case report and review of the literature. Case
Rep Urol. 2013;2013:356576.
31. Nagai T, Naiki T, Kawai N, Iida K, Etani T, Ando R, Hamamoto S, Sugiyama Y,
Okada A, Mizuno K, Umemoto Y, Yasui T. Pure lymphoepithelioma-like
carcinoma originating from the urinary bladder. Case Rep Oncol. 2016;9(1):
188–94.
32. Pantelides NM, Ivaz SL, Falconer A, Hazell S, Winkler M, Hrouda D, Mayer EK.
Lymphoepithelioma-like carcinoma of the urinary bladder: A case report
and review of systemic treatment options. Urol Ann. 2012;4(1):45–7.
33. Porcaro AB, Gilioli E, Migliorini F, Antoniolli SZ, Iannucci A, Comunale L.
Primary lymphoepithelioma-like carcinoma of the urinary bladder: report of
one case with review and update of the literature after a pooled analysis of
43 patients. Int Urol Nephrol. 2003;35(1):99–106.
34. Raphael V, Jitani AK, Sailo SL, Vakha M. Lymphoepithelioma-like carcinoma
of the urinary bladder: A rare case report. Urology Annals. 2015;7(4):516–9.
35. Singh NG, Mannan AA, Rifaat AA, Kahvic M. Lymphoepithelioma-like
carcinoma of the urinary bladder: report of a rare case. Ann Saudi Med.
2009;29(6):478–81.
36. Spinelli GP, Lo Russo G, Pacchiarotti A, Stati V, Prete AA, Tomao F, Sciarretta
C, Arduin M, Basso E, Chiotti S, Sinjari M, Venezia M, Zoccoli G, Tomao S. A
68-year-old Caucasian man presenting with urinary bladder
lymphoepithelioma: a case report. J Med Case Rep. 2013;7:161.
37. Stamatiou K, Christopoulos G, Tsavari A, Koulia K, Manoloudaki K, Vassilakaki
T. Lymphoepithelioma-like carcinoma of the bladder: A case report. Arch Ital
Urol Androl. 2016;88(2):147–9.
38. Tamas EF, Nielsen ME, Schoenberg MP, Epstein JI. Lymphoepithelioma-like
carcinoma of the urinary tract: a clinicopathological study of 30 pure and
mixed cases. Mod Pathol. 2007;20(8):828–34.
39. Trabelsi A, Abdelkrim SB, Rammeh S, Stita W, Sriha B, Mokni M, Korbi S.
Lymphoepithelioma-like carcinoma of the bladder in a North African man:
A case report. N Am J Med Sci. 2009;1(7):375–6.
40. Ward JN, Dong WF, Pitts Jr WR. Lymphoepithelioma-like carcinoma of the
bladder. J Urol. 2002;167(6):2523–4.
41. Williamson SR, Zhang S, Lopez-Beltran A, Shah RB, Montironi R, Tan PH,
Wang M, Baldridge LA, MacLennan GT, Cheng L. Lymphoepithelioma-like
carcinoma of the urinary bladder: clinicopathologic, immunohistochemical,
and molecular features. Am J Surg Pathol. 2011;35(4):474–83.
42. Yaqoob N, Kayani N, Piryani J, Sulaiman MN, Hasan SH. Lymphoepithelioma-
like carcinoma of urinary bladder: (LELCA). J Pak Med Assoc. 2005;55(9):402–3.
43. Yoshino T, Ohara S, Moriyama H. Lymphoepithelioma-like carcinoma of the
urinary bladder: a case report and review of the literature. BMC Res Notes.
2014;7:779.
44. Young RH, Eble JN. Unusual forms of carcinoma of the urinary bladder.
Hum Pathol. 1991;22(10):948–65.
45. Yun HK, Yun SI, Lee YH, Kang KM, Kwak EK, Kim JS, Cho SR, Kwon JB.
Lymphoepithelioma-like carcinoma of the urinary bladder. J Korean Med
Sci. 2010;25(11):1672–5.
46. Ziouziou I, Karmouni T, El Khader K, Koutani A, Andaloussi AI.
Lymphoepithelioma-like carcinoma of the bladder: a case report. J Med
Case Rep. 2014;8:424.
47. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrews M, Shekelle
P, Stewart LA, and PRISMA-P Group. Preferred reporting items for systematic
review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev.
2015;4:1.
• We accept pre-submission inquiries
• Our selector tool helps you to find the most relevant journal
• We provide round the clock customer support
• Convenient online submission
• Thorough peer review
• Inclusion in PubMed and all major indexing services
• Maximum visibility for your research
Submit your manuscript at
www.biomedcentral.com/submit
Submit your next manuscript to BioMed Central
and we will help you at every step:
Yang et al. BMC Urology (2017) 17:34 Page 6 of 6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com