Key words: MALT lymphoma, adeno-
carcinoma, combined tumor, lung.
Correspondence to: Aydanur Kargi,
Patoloji Anabilim Dali, Tip Fakültesi,
Dokuz Eylül Üniversitesi, Inciralti,
Received January 5, 2009;
accepted June 19, 2009.
Primary pulmonary extranodal marginal zone
lymphoma/low grade B-cell lymphoma
of MALT type combined with well-differentiated
Aydanur Kargi1, Duygu Gürel1, Atilla Akkoclu2, Aydin Sanli3,
and Erkan Yilmaz4
1Department of Pathology,2Department of Chest Diseases,3Department of Thoracic Surgery,
and4Department of Radiology, Dokuz Eylül University, Faculty of Medicine, Izmir, Turkey
We describe a rare case of extranodal marginal zone/low-grade B-cell lymphoma of
mucosa-associated lymphoid tissue (MALT) combined with areas of well-differenti-
ated adenocarcinoma. In addition, the MALT lymphoma was synchronously sys-
Mucosa-associated lymphoid tissue (MALT) lymphomas with coexistent carcino-
mas have been previously reported in the stomach and rarely in the lungs1-3.We here
describe a case of pulmonary MALT lymphoma containing areas of well-differentiat-
ed adenocarcinoma. Another interesting feature of this case was the simultaneous
presence of MALT lymphoma in the lung, stomach and duodenum, an occurrence
which has been reported in only 3% of MALT lymphomas generally4.
A 49-year-old man with a history of heavy smoking and complaints of epigastric
pain, nausea, loss of appetite and weight loss was admitted to the hospital for evalu-
ation in November 2006. His past medical history was noncontributory. Physical ex-
amination revealed no abnormalities. A complete blood cell count showed normo-
cytic-normochromic anemia (Hb 9.9 g/dL). Serum chemistry results were normal.
The sedimentation rate was increased (70 mm/h). A chest radiograph showed a pleu-
ra-based opacity in the upper part of the upper lobe of the left lung (Figure 1). The
cephalic border of the opacity showed fine spiculations, consistent with extension of
vealed a peripherally located solid mass of 5 cm in maximum dimension. No hilar or
mediastinal lymphadenopathy was demonstrated. Systemic radiological examina-
tion of the patient did not reveal any other mass lesions. Fiberoptic bronchoscopy
showed patency of the entire bronchial tree. A gastroduodenoscopy showed hyper-
emic edematous areas in the gastric body and second segment of the duodenum.
Biopsies from the stomach and duodenum showed MALT lymphoma without associ-
ated Helicobacter pylori organisms at both locations.
The patient underwent an exploratory chest operation, during which a mass lesion
located in the apical segmentof the leftupper lobe withcomplete invasion of the tho-
racic outlet was found. Excision of the mass along with a wedge resection of the sur-
rounding lung tissue was performed.
COMBINED PRIMARY PULMONARY MALT LYMPHOMA AND ADENOCARCINOMA 169
The excised lung tissue with an exophytic mass lesion
measured 8 × 5 and 5 × 2 cm.The cut surface showed an
ill-defined, firm, grayish-tan tumoral lesion infiltrating
the lung parenchyma and extending into the adherent
visceral and parietal pleural surfaces and soft tissues.
While the areas of the tumor mainly localized in the
lung parenchyma consisted of MALT lymphoma, inti-
mately admixed with well-differentiated adenocarcino-
ma (Figure 2), the areas invading the soft tissues of the
chest wall were composed of well- to moderately well-
differentiated adenocarcinoma. Neoplastic lymphocyt-
ic cells had a monocytoid appearance with formation of
invasion. Immunohistochemical examination showed
CD20 positivity in lymphocytic tumor cells, which were
all negative for CD3, CD5, CD10, CD23, and cyclin D1.
The tumor cells of the adenocarcinoma component had
mucicarmine-positive intracytoplasmic mucin secre-
tion. They had a CK7- and TTF-1 positive and a vi-
Figure 1 - A view of the upper portion of the left hemithorax on a pos-
teroanterior radiograph shows a pleural-based opacity (arrows). The
cephalic border of the opacity has fine spiculations, consistent with di-
rect extension of the lesion to the underlying lung parenchyma.
Figure 2 - High-power view of tumoral component that contains MALT lymphoma intermixed with well-differentiated adenocarcinoma areas
mentin-, CK5/6- and CK20-negative immunopheno-
type.While p53 was positive in almost all the cells of the
adenocarcinoma, it was negative in the MALT lym-
phoma component. Staining for bcl-2 showed diffuse
positivity in MALT lymphoma cells, while occasional
positivity in adenocarcinoma cells was detected. Ki-67
was positive in less than 10% of both lymphoma and
The synchronous presence of MALT lymphoma in the
differentiated adenocarcinoma intimately admixed
with pulmonary MALT lymphoma is a very unusual
characteristic of the present case.
comprising only 0.5% of all primary lung neoplasms5.
MALT lymphoma is the most frequent type, accounting
for 72% to 90% of all primary lung lymphomas6. In a
small proportion of pulmonary and nonpulmonary
MALT lymphomas, simultaneous multiple organ local-
ization has been observed, which did not seem to
change the outcome of the patients4. Both normal and
neoplastic lymphocytes in MALT display a pronounced
homing tendency throughout the body which has been
biologically linked to specific ligand-receptor interac-
tions between lymphoid cells and high endothelial
venules of MALT. This property of MALT cells might ex-
plain the synchronous systemic occurrence of MALT
The mechanism of the simultaneous occurrence of
pulmonary MALT lymphoma and adenocarcinoma in
this is such a rare occurrence, one possibility is that
these different tumors arose in our patient by chance.
Another possibility is that a common carcinogenic
mechanism might be involved in the development of
both lymphoma and carcinoma. The most frequent co-
incidental solid tumors associated with MALT lym-
phoma are gastric carcinomas1, and in such cases Heli-
cobacter pylori infection is believed to play a possible
etiopathogenetic role in both cancers1. Hepatitis B virus
and Epstein-Barr virus (EBV) infections have also been
implicated in the pathogenesis of rare cases reported in
liver and stomach, respectively7,8. In the current case,
the existence of EBV had not been investigated. Howev-
er, for lung cancers, no such association with EBV has
been reported, except for lymphoepithelioma-like car-
cinomas and a few cases of EBV-associated pulmonary
Bronchial MALT is not thought to be a normal con-
stituent of the human bronchus and it likely develops
as a response to various antigenic stimuli, for example
smoking and autoimmune disease12,13. Although a
common association between any known antigenic
stimuli, including smoke and pulmonary MALT lym-
phoma, as seen between gastric lymphomas of MALT
origin and Helicobacter pylori infection has not been
demonstrated, in the current case, where the patient
had a long history of heavy smoking, it is possible that
smoke could be the cause of both MALT lymphoma
and adenocarcinoma. In addition to the well-estab-
lished strong association between tobacco smoke and
lung cancer, some studies indicate an increased inci-
dence of NHL among smokers14. Many carcinogens
present in tobacco smoke that act as initiators in pul-
monary epithelial cells can also cause accumulation of
genetic changes in acquired lymphoid tissue cells,
leading to the development of both lymphomas and
In conclusion, we have reported a case with unique
features. A full preoperative diagnosis is difficult in such
tumors, and complete tumor resection is required for
the diagnosis of the different components.
1. Chan AO, Chu KM, Yuen ST, Leung SY, Lam SK, Wong J:
Synchronous gastric adenocarcinoma and mucosa associ-
ated lymphoid tissue lymphoma in association with Heli-
cobacter pylori infection: comparing reported cases be-
tween the East and West. Am J Gastroenterol, 96: 1922-
2. Ichihara E, Tabata M, Takigawa N, Sato Y, Kondo E, Aoe M,
Kiura K, Tanimoto M: Synchronous pulmonary MALT lym-
phoma and pulmonary adenocarcinoma after metachro-
nous gastric MALT lymphoma and gastric adenocarcino-
ma. J Thorac Oncol, 3: 1362-1363, 2008.
3. Chanel S, Burke L, Fıche M, Molina T, Lerochais JP, Icard P,
Diebold J, Galateuau-Sallé F: Synchronous pulmonary
adenocarcinoma and extranodal marginal zone/low grade
B-cell lymphoma of MALT type. Hum Pathol, 32: 129-132,
4. Thieblemont C, Berger F, Dumontet C, Moullet I, Bouafia F,
tissue lymphoma is a disseminated disease in one third of
158 patients analyzed. Blood, 95: 802-806, 2000.
5. Koss MN: Malignant and benign lymphoid lesions of the
lung. Ann Diagn Pathol, 8:167-187, 2004.
6. Chilosi M, Zinzani PL, Poletti V: Lymphoproliferative lung
disorders. Sem Resp Crit Care Med, 26: 490-501, 2005.
7. Takeshima F, Kunisaki M, Aritomi T, Osabe M, Akama F,
Nakasone T, Niino D, Katayama S, Isomoto H, Omagari K,
Mizuta Y, Murata I, Kohno S: Hepatic mucosa-associated
lymphoid tissue lymphoma and hepatocellular carcinoma
in a patient with hepatitis B virus infection. J Clin Gas-
troenterol, 38: 823-826, 2004.
8. Nakamura S, Aoyagi K, Iwanaga S,YaoT,Tsuneyoshi M, Fu-
jishima M: Synchronous and metachronous primary gas-
tric lymphoma and adenocarcinoma. A clinicopathologi-
cal study of 12 patients. Cancer, 79: 1077-1085, 1997.
9. Grinstein S, Preciado MV, Gattuso P, Chabay PA, Warren
WH, De Matteo E, Gould VE: Demonstration of Epstein-
Barr virus in carcinomas of various sites. Cancer Res, 62:
10. Morbini P, Riboni R, Tomaselli S, Rossi A, Magrini U: Eber-
and LMP-1-expressing pulmonary lymphoepithelioma-
like carcinoma in a Caucasian patient. Hum Pathol, 34:
170 A KARGI, D GÜREL, A AKKOCLU ET AL
COMBINED PRIMARY PULMONARY MALT LYMPHOMA AND ADENOCARCINOMA 171 Download full-text
11. Conway EJ, Hudnall SD, Lazarides A, Bahler A, Fraire AE,
Cagle PT: Absence of evidence for an etiologic role for Ep-
stein-Barr virus in neoplasms of the lung and pleura. Mod
Pathol, 9: 491-495, 1996.
12. Richmond I, Pritchard GE, Ashcoft T, Avery A, Corris PA,
Walters EH: Bronchus associated lymphoid tissue (BALT)
in human lung: its distribution in smokers and non-smok-
ers. Thorax, 48: 1130-1134, 1993.
13. Nicholsen AG, Wotherspoon AC, Jones AL, Sheppard MN,
Isaacson PG, Corrin B: Pulmonary B-cell non-Hodgkin’s
lymphoma associated with autoimmune disorders: a clini-
copathological review of six cases. Eur Respir J, 9: 2022-
14. Stagnaro E, Tumino R, Parodi S, Crosignani P, Fontana A,
Masala G, Miligi L, Nanni O, Ramazzotti V, Rodella S,
Senoiri Constantini A,Vigano C,Vindigni C,Vineis P: Non-
Hodgkin’s lymphoma and type of tobacco smoke. Cancer
Epidemiol Biomarkers Prev, 13: 431-437, 2004.