DOI:10.2214/AJR.05.0244
AJR 2006; 186:1294-1299
© American Roentgen Ray Society
Lymphoepithelioma-like Carcinoma of the Lung: Radiologic Features of an Uncommon Primary Pulmonary Neoplasm
Joseph M. Hoxworth1,
Douglas K. Hanks2,
Philip A. Araoz3,
Brett M. Elicker1,
Gautham P. Reddy1,
W. Richard Webb1,
Jessica W. T. Leung1 and
Michael B. Gotway1,4
1 Department of Radiology, University of California, San Francisco, 505
Parnassus Avenue, Room M-391, Box 0628, San Francisco, CA 94110.
2 Department of Pathology, San Francisco General Hospital, San Francisco, CA
94110.
3 Department of Radiology, Mayo Clinic, Rochester, MN 55905.
4 Scottsdale Medical Imaging, Ltd., an Affiliate of Southwest Diagnostic
Imaging, Scottsdale, AZ 85252.
Received February 12, 2005;
accepted after revision March 28, 2005.
Address correspondence to M. B. Gotway
(michael.gotway{at}radiology.ucsf.edu).
Abstract
OBJECTIVE. The purpose of this study was to review the chest
radiographic, CT, and MRI appearances of primary pulmonary
lymphoepithelioma-like carcinoma (LELC).
CONCLUSION. Primary pulmonary LELC is histopathologically identical
to nasopharyngeal carcinoma. The radiographic, CT, and MRI features of primary
pulmonary LELC are nonspecific, often resembling those of bronchogenic
carcinoma. Primary pulmonary LELC usually presents as a poorly circumscribed,
enhancing, peripheral solitary pulmonary nodule on CT; necrosis may be present
and is considered a poor prognostic sign. MRI shows isointense to
low-intensity signal on T1-weighted images and mildly increased signal on
T2-weighted images; enhancement of abnormal tissue is typical. Most patients
present with early-stage disease. Primary pulmonary LELC should be suspected
in selected patients and requires differentiation from bronchogenic carcinoma
and metastatic nasopharyngeal carcinoma.
Keywords: biopsy • CT • Epstein-Barr virus • lung cancer • MRI • primary pulmonary lymphoepithelioma-like carcinoma
Introduction
Primary lymphoepithelioma-like carcinoma (LELC) of the lung is a rare
entity initially reported by Begin et al.
[1] in 1987. Nearly 100 cases
have been described in the English-language literature
[1-23].
This tumor is histologically identical to the lymphoepithelioma originally
described in nasopharyngeal tissue and consists of undifferentiated carcinoma
associated with prominent lymphoid stroma and ultrastructural features of
squamous cell carcinoma [2].
Like its nasopharyngeal counterpart, primary pulmonary LELC has a documented
strong relationship with Epstein-Barr infection in Asian populations
[14].
Most prior reports of primary pulmonary LELC have emphasized the
clinicopathologic features of the disease, with little discussion of the
radiologic manifestations. The most comprehensive analysis of the imaging
findings of primary pulmonary LELC was a recent report by Ooi et al.
[19], who detailed the CT
characteristics of advanced disease. Because primary pulmonary LELC may be
mistaken for metastatic nasopharyngeal carcinoma or lymphoma on
histopathologic specimens obtained via percutaneous transthoracic biopsy, it
is important for radiologists to understand the clinical and radiologic
features of this neoplasm to avoid misdiagnosis and improper patient
management. Therefore, we report both the clinicopathologic characteristics
and the imaging manifestations of primary pulmonary LELC, including the
previously unreported MRI findings for this rare primary pulmonary neoplasm,
and we review the literature surrounding primary pulmonary LELC so that
radiologists can become familiar with this lesion and potential pitfalls in
diagnosis.
Materials and Methods
The pathology databases at two academic medical centers were reviewed over
a 14-year period from 1990 to 2004, and four patients in whom primary LELC of
the lung had been diagnosed were identified. Institutional review board
approval was obtained for the study. Three patients were female (age, 31, 44,
and 51 years) and one was male (age, 69 years). Two additional patients were
identified with pathologic diagnoses of LELC after biopsy of thoracic masses.
However, both these patients had a history of treated nasopharyngeal LELC 3
and 5 years before the identification of lesions on chest radiography.
Comparison with nasopharyngeal and pulmonary tissue specimens showed that the
pulmonary lesions had histopathologic features similar to those of the
nasopharyngeal lesions and also had positive in situ hybridization for
Epstein-Barr virus (EBV), making the pulmonary lesions compatible with
metastases; therefore, these patients were excluded from the study.
The medical records, radiologic studies, pathologic findings, and clinical
course of the four patients in the study cohort were retrospectively reviewed.
All patients had undergone otolaryngologic examination and nasopharyngeal MRI
to exclude primary nasopharyngeal carcinoma during the course of evaluation of
the pulmonary LELC.
All primary pulmonary LELC lesions were identified first on chest
radiography performed for the following indications (n = 1 for each):
screening because of positive tuberculin skin test results and evaluation of
dermatomyositis, chest pain, or cough. All patients were subsequently examined
with thoracic CT. Helical CT (CT/i, GE Healthcare) of the thorax was performed
using 7-mm collimation, with dedicated thin-section imaging (1 mm) through the
nodules. Iohexol IV contrast medium (Omnipaque 300, GE Healthcare) was used
for three of four patients, and a dedicated nodule enhancement study, as
detailed by Swensen et al.
[24], was performed for one of
the three patients who received IV contrast medium.
Three thoracic radiologists retrospectively reviewed thoracic CT scans by
consensus for the presence, location, and imaging characteristics (size,
shape, location, margin characteristics [circumscribed vs. ill-defined], and
enhancement patterns) of thoracic lymphadenopathy, pleural disease, chest wall
abnormalities, and abnormalities within the upper abdomen. Lesions were
considered central if they were within the central third of the lung and
peripheral if they were within the outer third of the lung. Thoracic MRI was
performed for problem solving in two patients—one (patient 2) because
the patient refused IV contrast administration for thoracic CT and the
consulting surgeon desired contrast-enhanced MRI before mediastinoscopy; the
other (patient 4) because abnormal paravertebral soft tissue detected at
thoracic CT required further characterization.
The preliminary diagnosis of LELC of the lung was made on review of
cytologic specimens obtained at transthoracic needle biopsy (performed using
coaxial technique and a 22-gauge needle through a 20-gauge sheath), and the
final diagnosis was then confirmed on review of histopathologic specimens
obtained after resection by a pathologist experienced in cytologic techniques
and familiar with the histopathologic characteristics of primary pulmonary
LELC. In particular, in situ hybridization for EBV-encoded small nuclear RNA
was performed on representative paraffin sections as previously described
[10].
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Fig. 1A —69-year-old white man (patient 3) with primary pulmonary
lymphoepithelioma-like carcinoma presenting as solitary pulmonary nodule.
Soft-tissue window from unenhanced thoracic CT shows 1-cm peripheral nodule
(arrow) contacting pleura.
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Fig. 1B —69-year-old white man (patient 3) with primary pulmonary
lymphoepithelioma-like carcinoma presenting as solitary pulmonary nodule.
Thoracic CT scan (3-mm collimation) obtained 1 min after IV contrast
administration shows enhancement (45 H) of nodule (arrow).
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Fig. 1C —69-year-old white man (patient 3) with primary pulmonary
lymphoepithelioma-like carcinoma presenting as solitary pulmonary nodule. Lung
window highlights irregular nodule margins (arrow).
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Results
The clinical features of patients with primary pulmonary LELC are presented
in Table 1.
Three thoracic radiologists reviewed the imaging findings of primary
pulmonary LELC by consensus. Chest radiography showed solitary pulmonary
nodules or masses in all patients, unaccompanied by pleural or osseous
lesions. One patient (patient 2) had right paratracheal lymphadenopathy
visible on chest radiography at the time of initial diagnosis. The CT
appearances of primary pulmonary LELC at initial diagnosis in our study cohort
consisted of solitary pulmonary nodules (Figs.
1A,
1B,
1C,
2A,
2B,
2C, and
2D) or a mass (Figs.
3A,
3B, and
3C) ranging in size from 1.0
to 3.8 cm and showing varying degrees of contrast enhancement (Figs.
1A,
1B,
1C,
3A,
3B,
3C,
3D,
3E, and
3F). Lesion margins were
either lobulated or irregular for all patients (Figs.
1A,
1B,
1C,
2A,
2B,
2C,
2D,
3A,
3B,
3C,
3D,
3E, and
3F), and one lesion showed a
ground-glass attenuation halo (Fig.
3B). No nodules showed calcification or air bronchograms. Three of
the four nodules were peripheral. No patient had pleural osseous abnormalities
at initial diagnosis. Right paratracheal lymphadenopathy in patient 2 was
confirmed at thoracic MRI (Figs.
3D,
3E, and
3F).
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Fig. 2A —51-year-old Chinese woman (patient 2) with primary pulmonary
lymphoepithelioma-like carcinoma. Soft-tissue window from axial unenhanced
thoracic CT shows noncalcified 2.6-cm nodule (arrow) in right middle
lobe.
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Fig. 2B —51-year-old Chinese woman (patient 2) with primary pulmonary
lymphoepithelioma-like carcinoma. Lung window highlights irregular, lobulated
nodule margins (arrow). Ground-glass halo is also seen.
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Fig. 2C —51-year-old Chinese woman (patient 2) with primary pulmonary
lymphoepithelioma-like carcinoma. Axial T1-weighted MR image shows right
paratracheal lymphadenopathy (arrow) of low signal intensity.
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Fig. 2D —51-year-old Chinese woman (patient 2) with primary pulmonary
lymphoepithelioma-like carcinoma. Axial T1-weighted MR image after IV
gadolinium administration shows right paratracheal lymphadenopathy enhancement
(arrow).
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Fig. 3A —31-year-old Chinese woman (patient 1) with primary pulmonary
lymphoepithelioma-like carcinoma that recurred after resection. Images
A-C were obtained before resection and D-F were obtained after
resection. Contrast-enhanced thoracic CT scan shows 2.7 x 3.8 cm
lobulated mass (arrows) in right lower lobe with extensive pleural
and mediastinal contact and central necrosis.
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Fig. 3B —31-year-old Chinese woman (patient 1) with primary pulmonary
lymphoepithelioma-like carcinoma that recurred after resection. Images
A-C were obtained before resection and D-F were obtained after
resection. Low-power (20x) photomicrograph of H and E-stained cell block from
biopsy of pulmonary lesion shows island of malignant carcinoma cells
(arrows) surrounded by lymphoplasmacytic cell population.
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Fig. 3C —31-year-old Chinese woman (patient 1) with primary pulmonary
lymphoepithelioma-like carcinoma that recurred after resection. Images
A-C were obtained before resection and D-F were obtained after
resection. In-situ hybridization study confirms presence of strong nuclear
labeling for EBV-encoded small nuclear RNAs (arrows).
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Fig. 3D —31-year-old Chinese woman (patient 1) with primary pulmonary
lymphoepithelioma-like carcinoma that recurred after resection. Images
A-C were obtained before resection and D-F were obtained after
resection. T1-weighted (TR/TE, 500/9) axial MR image through upper lumbar
spine shows abnormal low-signal-intensity tissue (arrows) in
paravertebral region and extending into neural foramen.
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Fig. 3E —31-year-old Chinese woman (patient 1) with primary pulmonary
lymphoepithelioma-like carcinoma that recurred after resection. Images
A-C were obtained before resection and D-F were obtained after
resection. T1-weighted (700/9) axial MR image after IV administration of
gadolinium shows intense enhancement of abnormal paravertebral soft tissue
(arrows) extending into neural foramen.
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Fig. 3F —31-year-old Chinese woman (patient 1) with primary pulmonary
lymphoepithelioma-like carcinoma that recurred after resection. Images
A-C were obtained before resection and D-F were obtained after
resection. T2-weighted (3,000/80.2) axial MR image shows mild T2 prolongation
(arrows) in abnormal paravertebral tissue extending into neural
foramen. T2 signal hyperintensity is mild, perhaps because of extensive
lymphocytic cellularity of tumor.
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The diagnosis of primary pulmonary LELC was made at percutaneous
transthoracic biopsy of the pulmonary lesions in three patients and at
histopathologic analysis in one patient after nodule wedge resection. For the
three patients who underwent transthoracic needle biopsy, the diagnosis was
made cytologically; core biopsies were not required.
All patients in our cohort were considered to have lesions amenable to
surgical resection at the time of diagnosis. All patients underwent either
lobectomy or large wedge excision, and nodal staging was also performed at the
time of surgery.
Postoperatively, all patients were treated with combined chemotherapy
(5-fluorouracil, cisplatin, and leucovorin) and sequential external beam
radiation therapy. Serial thoracic CT scans were obtained for surveillance to
detect carcinoma recurrence, and directed CT and MRI examinations were
performed as needed for patient 1 when surveillance CT studies detected
abnormalities requiring further investigation.
In one patient (patient 1) of the three who were Chinese immigrants,
recurrent disease subsequently developed after an initial treatment response.
Patient 1 was further evaluated nearly 4 years after surgery with
thoracolumbar spine MRI to characterize an inferior right thoracic paraspinous
mass and retroperitoneal lymphadenopathy initially detected on caudal sections
of surveillance thoracic CT. Percutaneous fine-needle aspiration biopsy of the
paraspinous lesion confirmed metastatic LELC; this recurrent disease responded
to additional cycles of palliative chemotherapy. After the patient had
remained in disease remission for nearly 1 year, enlarging pulmonary nodules
compatible with metastases developed, for which she continues to undergo
treatment.
Patient 2 has remained disease-free during a follow-up period of 69 months.
Patient 3 died of an unrelated cause 6 months after surgery for pulmonary
LELC, and patient 4 remains alive and without disease recurrence 4 years after
right lower lobectomy for primary pulmonary LELC.
Discussion
Primary LELC of the lung is a rare entity that was originally described in
the nasopharynx as "lymphoepithelioma" and has since been reported
in multiple pharyngeal and foregut derivatives. It is an undifferentiated
carcinoma characterized histopathologically by a syncytial appearance,
lymphocyte infiltration, and focal squamous differentiation. This uncommon
neoplasm appears to be EBV-related in Asian patients, though the precise role
of EBV in tumorigenesis is unclear, because a similar strong association has
not been found in white patients
[4,
9,
12,
18,
20,
22,
23].
Primary pulmonary LELC has distinctive clinical features that differ from
those of non-small cell lung carcinoma
[6,
10,
13,
16,
17]. Specifically, primary
pulmonary LELC is a disease that predominantly affects adults—
occasionally affecting patients younger than those typically affected by
bronchogenic carcinoma—and has no clear sex predilection. Furthermore,
in contrast to non-small cell lung carcinoma, primary pulmonary LELC has
minimal association with cigarette smoking. Finally, patients with primary
pulmonary LELC tend to have a more favorable prognosis than do patients with
non-small cell lung carcinoma. In particular, metastases tend to develop less
frequently and appear later in the disease course in patients with primary
pulmonary LELC, and LELC has been reported to be responsive to chemotherapy
and radiation therapy [11,
12,
15-17,
21]. Tumor recurrence and
necrosis appear to be the prognostic factors predicting impaired survival
[16].
Most descriptions of the imaging features of advanced primary pulmonary
LELC have been limited and reported incidentally in a few small
clinicopathologic studies [2,
4,
6,
12,
16,
21,
22]. One study, by Ooi and
colleagues [19], compared the
CT features of similarly advanced-stage patients (stages III and IV) with LELC
and non-small cell lung carcinoma. These authors concluded that the tumors in
patients with LELC were more likely to exhibit the following features: large
size, central location, smooth margins, vascular encasement, and
peribronchovascular nodal spread. Although other prior reports have suggested
that radiologic differentiation between bronchogenic carcinoma and primary
pulmonary LELC is difficult, Ooi et al. asserted that large pulmonary lesions
closely associated with the mediastinum, especially when peribronchovascular
nodal spread and vascular encasement are present, favor the diagnosis of
primary pulmonary LELC over non-LELC neoplasms. Nevertheless, the
distinguishing features observed by Ooi et al. may be observed also in
patients with bronchogenic carcinoma. Furthermore, these investigators studied
late-stage lesions, and therefore their findings cannot be extrapolated
readily to patients with earlier-stage presentations, such as those in our
cohort and in the other major series detailing clinicopathologic features of
pulmonary LELC—by Chan et al.
[6] and Han et al.
[16]. Indeed, the results of
Ooi et al. suggest that primary pulmonary LELC presents as a large thoracic
mass with circumscribed borders in the central third of the lung and
associated with lymphadenopathy, whereas the results of our study and the
clinicopathologic studies of Chan et al.
[6] and Han et al.
[16] suggest that primary
pulmonary LELC most often presents as a poorly circumscribed peripheral nodule
measuring 3.5 cm or less and usually is not associated with
lymphadenopathy.
To our knowledge, the MRI features of thoracic LELC of the lung have not
been described previously. MRI features of primary pulmonary LELC include
intense enhancement with iso- to hypointensity on T1-weighted sequences and
iso- to hyperintensity on T2-weighted sequences. Unfortunately, these MRI
signal characteristics are nonspecific, and as in the case of CT, do not allow
definitive discrimination from bronchogenic carcinoma. As a result, the role
of MRI in evaluating LELC likely will be limited to better assessment of
invasion of adjacent structures for staging and preoperative planning.
We identified two patients with a history of nasopharyngeal carcinoma who
presented years later with intrathoracic masses that were histologically
confirmed to be LELC. Metastases from lymphoepithelial carcinoma occurring in
the nasopharynx are pathologically indistinguishable from a primary pulmonary
LELC, particularly given the close association of both to EBV infection
[6]. Distinguishing between the
two does not seem possible with imaging either. Two patients with pulmonary
lesions histopathologically identical to primary pulmonary LELC were excluded
from our study cohort because they also had nasopharyngeal lesions, and
therefore the lung nodules were presumed to be due to metastatic
nasopharyngeal carcinoma. One of these patients presented with a solitary
pulmonary nodule, whereas the other presented with a lobulated pleural mass.
Both of these presentations are previously described manifestations of primary
LELC of the lung [6,
16,
17,
19], underscoring the
importance of referring patients suspected of having primary pulmonary LELC
for otolaryngologic consultation and nasopharyngeal imaging to obtain accurate
tumor staging.
Finally, our study has several important implications for patients with
primary pulmonary LELC. Specifically, primary pulmonary LELC should be
suspected in Asian patients presenting with pulmonary nodules or masses,
particularly in patients who seem atypically young for bronchogenic carcinoma.
Furthermore, primary pulmonary LELC actively should be considered in Asian
patients for whom percutaneous transthoracic biopsies of solitary nodules have
yielded a diagnosis of either lymphoma or nasopharyngeal carcinoma. The former
is typically managed nonsurgically, and assumption of the latter would lead to
inaccurate staging. Proper identification of primary pulmonary LELC will allow
correct staging and appropriate patient management decisions.
In conclusion, the CT and MRI appearances of primary pulmonary LELC are
similar to those of bronchogenic carcinomas, although primary pulmonary LELC
may selectively affect different patient populations. In particular, primary
pulmonary LELC should be suspected in younger Asian patients presenting with
solitary pulmonary nodules or masses, and proper tumor staging and therapeutic
decisions require an accurate diagnosis. Because radiologists may encounter
primary pulmonary LELC on imaging or at biopsy, familiarity with this entity
is needed. These tumors may be mistaken histopathologically for metastatic
nasopharyngeal carcinoma or lymphoma, resulting in improper patient
management.
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Abstract
Introduction
