Skip to main content
Top
Published in: BMC Gastroenterology 1/2013

Open Access 01-12-2013 | Research article

Endocytoscopic findings of lymphomas of the stomach

Authors: Hajime Isomoto, Kayoko Matsushima, Tomayoshi Hayashi, Yoshitaka Imaizumi, Junya Shiota, Hiroyuki Ishii, Hitomi Minami, Ken Ohnita, Fuminao Takeshima, Saburo Shikuwa, Yasushi Miyazaki, Kazuhiko Nakao

Published in: BMC Gastroenterology | Issue 1/2013

Login to get access

Abstract

Background

The gastric lesions of various lymphomas were observed at the cellular level using endocytoscopy.

Methods

Endocytoscopy and magnifying endoscopy with narrow band imaging (NBI) were performed in 17 patients with lymphomas of the stomach. The lesions consisted of 7 with low-grade mucosa-associated lymphoid tissue (MALT), 5 with gastric involvement by adult T-cell leukemia/lymphoma (ATLL), 4 with diffuse large B-cell lymphoma (DLBCL), and 1 with peripheral T-cell lymphoma.

Results

On conventional endoscopy, 9 were classified as having superficial spreading type, 7 were mass-forming type, and 1 was diffuse infiltrating type. Anti-H. pylori treatment was given in the 7 MALT lymphoma cases. NBI magnification endoscopy invariably showed dilatation or ballooning and destruction of gastric pits and elongation and distortion in microvessels. Endocytoscopy showed mucosal aggregation of interstitial cellular elements in almost all gastric lymphoma cases. The nuclear diversity in size and configuration was exclusively seen in gastric lymphomas other than MALT lymphoma, whereas the nuclei of MALT lymphoma cells were regular and small to moderate in size. Inter-glandular infiltration by lymphomatous cell elements was frequently observed in MALT lymphoma and DLBCL, but it was uncommon in peripheral gastric T-cell malignancies. Endocytoscopy could identify the disease-specific histology, the lymphoepithelial origin, as inter-glandular infiltration of cellular components in MALT lymphoma and the possibly related DLBCL cases. Complete regression (CR) was observed in 2 of the 7 MALT lymphoma patients. In the 2 patients with CR who underwent repeat endocytoscopy, the ultra-high magnification abnormalities returned to normal, while they were unchanged in those without tumor regression.

Conclusions

On endocytoscopy, intra-glandular aggregation of cellular components was invariably identified in lymphomas of the stomach. Nuclear regularity in size and configuration may indicate the cytological grade, differentiating the indolent low-grade from aggressive lymphoproliferative diseases. The inter-glandular infiltration seen on endocytoscopy can indicate the lymphoepithelial lesions seen in MALT lymphoma and related DLBCL. Endocytoscopy would be applicable for virtual histopathological diagnosis of different lymphoproliferative disorders and their clinical assessment during ongoing endoscopy.
Appendix
Available only for authorised users
Literature
2.
go back to reference Herrmann R, Panahon AM, Barcos MP, Walsh D, Stutzman L: Gastrointestinal involvement in non-Hodgkin’s lymphoma. Cancer. 1980, 46: 215-222. 10.1002/1097-0142(19800701)46:1<215::AID-CNCR2820460136>3.0.CO;2-6.CrossRefPubMed Herrmann R, Panahon AM, Barcos MP, Walsh D, Stutzman L: Gastrointestinal involvement in non-Hodgkin’s lymphoma. Cancer. 1980, 46: 215-222. 10.1002/1097-0142(19800701)46:1<215::AID-CNCR2820460136>3.0.CO;2-6.CrossRefPubMed
3.
go back to reference Isaacson P, Wright DH: Malignant lymphoma of mucosa-associated lymphoid tissue: a distinctive type of B-cell lymphoma. Cancer. 1983, 52: 1410-1416. 10.1002/1097-0142(19831015)52:8<1410::AID-CNCR2820520813>3.0.CO;2-3.CrossRefPubMed Isaacson P, Wright DH: Malignant lymphoma of mucosa-associated lymphoid tissue: a distinctive type of B-cell lymphoma. Cancer. 1983, 52: 1410-1416. 10.1002/1097-0142(19831015)52:8<1410::AID-CNCR2820520813>3.0.CO;2-3.CrossRefPubMed
4.
go back to reference Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, Isaacson PG: Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993, 342: 575-577. 10.1016/0140-6736(93)91409-F.CrossRefPubMed Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, Isaacson PG: Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993, 342: 575-577. 10.1016/0140-6736(93)91409-F.CrossRefPubMed
5.
go back to reference Stathis A, Chini C, Bertoni F, Proserpio I, Capella C, Mazzucchelli L, Pedrinis E, Cavalli F, Pinotti G, Zucca E: Long-term outcome following Helicobacter pylori eradication in a retrospective study of 105 patients with localized gastric marginal zone B-cell lymphoma of MALT type. Ann Oncol. 2009, 20: 1086-1093. 10.1093/annonc/mdn760.CrossRefPubMed Stathis A, Chini C, Bertoni F, Proserpio I, Capella C, Mazzucchelli L, Pedrinis E, Cavalli F, Pinotti G, Zucca E: Long-term outcome following Helicobacter pylori eradication in a retrospective study of 105 patients with localized gastric marginal zone B-cell lymphoma of MALT type. Ann Oncol. 2009, 20: 1086-1093. 10.1093/annonc/mdn760.CrossRefPubMed
6.
go back to reference Sugita S, Iijima T, Furuya S, Kano J, Yanaka A, Ohta K, Kojima H, Noguchi M: Gastric T-cell lymphoma with cytotoxic phenotype. Pathol Int. 2007, 57: 108-114. 10.1111/j.1440-1827.2006.02065.x.CrossRefPubMed Sugita S, Iijima T, Furuya S, Kano J, Yanaka A, Ohta K, Kojima H, Noguchi M: Gastric T-cell lymphoma with cytotoxic phenotype. Pathol Int. 2007, 57: 108-114. 10.1111/j.1440-1827.2006.02065.x.CrossRefPubMed
7.
go back to reference Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchino H: Adult T cell leukemia: clinical and hematological features of 16 cases. Blood. 1977, 50: 481-492.PubMed Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchino H: Adult T cell leukemia: clinical and hematological features of 16 cases. Blood. 1977, 50: 481-492.PubMed
8.
go back to reference Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL: Global epidemiology of HTLV-1 infection and associated diseases. Oncogene. 2005, 24: 6058-6068. 10.1038/sj.onc.1208968.CrossRefPubMed Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL: Global epidemiology of HTLV-1 infection and associated diseases. Oncogene. 2005, 24: 6058-6068. 10.1038/sj.onc.1208968.CrossRefPubMed
9.
go back to reference Sakata H, Fujimoto K, Iwakiri R, Mizuguchi M, Koyama T, Sakai T, Inoue E, Tokunaga O, Shimamoto Y: Gastric lesions in 76 patients with adult T-cell leukemia/lymphoma. Endoscopic evaluation. Cancer. 1996, 78: 396-402. 10.1002/(SICI)1097-0142(19960801)78:3<396::AID-CNCR3>3.0.CO;2-I.CrossRefPubMed Sakata H, Fujimoto K, Iwakiri R, Mizuguchi M, Koyama T, Sakai T, Inoue E, Tokunaga O, Shimamoto Y: Gastric lesions in 76 patients with adult T-cell leukemia/lymphoma. Endoscopic evaluation. Cancer. 1996, 78: 396-402. 10.1002/(SICI)1097-0142(19960801)78:3<396::AID-CNCR3>3.0.CO;2-I.CrossRefPubMed
10.
go back to reference Nakamura S, Yao T, Aoyagi K, Iida M, Fujishima M, Tsuneyoshi M: Helicobacter pylori and primary gastric lymphoma. A histopathologic and immunohistochemical analysis of 237 patients. Cancer. 1997, 79: 3-11. 10.1002/(SICI)1097-0142(19970101)79:1<3::AID-CNCR2>3.0.CO;2-P.CrossRefPubMed Nakamura S, Yao T, Aoyagi K, Iida M, Fujishima M, Tsuneyoshi M: Helicobacter pylori and primary gastric lymphoma. A histopathologic and immunohistochemical analysis of 237 patients. Cancer. 1997, 79: 3-11. 10.1002/(SICI)1097-0142(19970101)79:1<3::AID-CNCR2>3.0.CO;2-P.CrossRefPubMed
11.
go back to reference Ohnita K, Isomoto H, Mizuta Y, Maeda T, Haraguchi M, Miyazaki M, Murase K, Murata I, Tomonaga M, Kohno S: Helicobacter pylori infection in patients with gastric involvement by adult T-cell leukemia/lymphoma. Cancer. 2002, 94: 1507-1516. 10.1002/cncr.10367.CrossRefPubMed Ohnita K, Isomoto H, Mizuta Y, Maeda T, Haraguchi M, Miyazaki M, Murase K, Murata I, Tomonaga M, Kohno S: Helicobacter pylori infection in patients with gastric involvement by adult T-cell leukemia/lymphoma. Cancer. 2002, 94: 1507-1516. 10.1002/cncr.10367.CrossRefPubMed
12.
go back to reference Ono S, Kato M, Takagi K, Kodaira J, Kubota K, Matsuno Y, Komatsu Y, Asaka M: Long-term treatment of localized gastric marginal zone B-cell mucosa associated lymphoid tissue lymphoma including incidence of metachronous gastric cancer. J Gastroenterol Hepatol. 2010, 25: 804-809. 10.1111/j.1440-1746.2009.06204.x.CrossRefPubMed Ono S, Kato M, Takagi K, Kodaira J, Kubota K, Matsuno Y, Komatsu Y, Asaka M: Long-term treatment of localized gastric marginal zone B-cell mucosa associated lymphoid tissue lymphoma including incidence of metachronous gastric cancer. J Gastroenterol Hepatol. 2010, 25: 804-809. 10.1111/j.1440-1746.2009.06204.x.CrossRefPubMed
13.
go back to reference Muto M, Horimatsu T, Ezoe Y, Morita S, Miyamoto S: Improving visualization techniques by narrow band imaging and magnification endoscopy. J Gastroenterol Hepatol. 2009, 24: 1333-1346. 10.1111/j.1440-1746.2009.05925.x.CrossRefPubMed Muto M, Horimatsu T, Ezoe Y, Morita S, Miyamoto S: Improving visualization techniques by narrow band imaging and magnification endoscopy. J Gastroenterol Hepatol. 2009, 24: 1333-1346. 10.1111/j.1440-1746.2009.05925.x.CrossRefPubMed
14.
go back to reference Wallace MB, Kiesslich R: Advances in endoscopic imaging of colorectal neoplasia. Gastroenterology. 2010, 138: 2140-2150. 10.1053/j.gastro.2009.12.067.CrossRefPubMed Wallace MB, Kiesslich R: Advances in endoscopic imaging of colorectal neoplasia. Gastroenterology. 2010, 138: 2140-2150. 10.1053/j.gastro.2009.12.067.CrossRefPubMed
15.
go back to reference Isomoto H, Shikuwa S, Yamaguchi N, Miyazato K, Ohnita K, Hayashi T, Mizuta Y, Ito M, Kohno S: Magnified endoscopic findings of gastric low-grade mucosa-associated lymphoid tissue lymphoma. Endoscopy. 2008, 40: 225-228. 10.1055/s-2007-995415.CrossRefPubMed Isomoto H, Shikuwa S, Yamaguchi N, Miyazato K, Ohnita K, Hayashi T, Mizuta Y, Ito M, Kohno S: Magnified endoscopic findings of gastric low-grade mucosa-associated lymphoid tissue lymphoma. Endoscopy. 2008, 40: 225-228. 10.1055/s-2007-995415.CrossRefPubMed
16.
go back to reference Ohnita K, Isomoto H, Shikuwa S, Yamaguchi N, Nakayama T, Nishiyama H, Okamoto K, Fukuda E, Takeshima F, Hayashi T, Kohno S, Nakao K: Magnifying chromoendoscopic findings of early gastric cancer and gastric adenoma. Dig Dis Sci. 2011, 56: 2715-2722. 10.1007/s10620-011-1638-6.CrossRefPubMed Ohnita K, Isomoto H, Shikuwa S, Yamaguchi N, Nakayama T, Nishiyama H, Okamoto K, Fukuda E, Takeshima F, Hayashi T, Kohno S, Nakao K: Magnifying chromoendoscopic findings of early gastric cancer and gastric adenoma. Dig Dis Sci. 2011, 56: 2715-2722. 10.1007/s10620-011-1638-6.CrossRefPubMed
17.
go back to reference Neumann H, Fuchs FS, Vieth M, Atreya R, Siebler J, Kiesslich R, Neurath MF: Review article: in vivo imaging by endocytoscopy. Aliment Pharmacol Ther. 2011, 33: 1183-1193. 10.1111/j.1365-2036.2011.04647.x.CrossRefPubMed Neumann H, Fuchs FS, Vieth M, Atreya R, Siebler J, Kiesslich R, Neurath MF: Review article: in vivo imaging by endocytoscopy. Aliment Pharmacol Ther. 2011, 33: 1183-1193. 10.1111/j.1365-2036.2011.04647.x.CrossRefPubMed
18.
go back to reference Nakamura S, Akazawa K, Yao T, Tsuneyoshi M: Primary gastric lymphoma: a clinicopathologic study of 233 cases with special reference to evaluation with the MIB-1 index. Cancer. 1995, 76: 1313-1324. 10.1002/1097-0142(19951015)76:8<1313::AID-CNCR2820760804>3.0.CO;2-1.CrossRefPubMed Nakamura S, Akazawa K, Yao T, Tsuneyoshi M: Primary gastric lymphoma: a clinicopathologic study of 233 cases with special reference to evaluation with the MIB-1 index. Cancer. 1995, 76: 1313-1324. 10.1002/1097-0142(19951015)76:8<1313::AID-CNCR2820760804>3.0.CO;2-1.CrossRefPubMed
19.
go back to reference Rohatiner A, d’Amore F, Coiffier B, Crowther D, Gospodarowicz M, Isaacson P, Lister TA, Norton A, Salem P, Shipp M: Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994, 5: 397-400.CrossRefPubMed Rohatiner A, d’Amore F, Coiffier B, Crowther D, Gospodarowicz M, Isaacson P, Lister TA, Norton A, Salem P, Shipp M: Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994, 5: 397-400.CrossRefPubMed
20.
go back to reference Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A, Harris NL, Le Beau MM, Hellström-Lindberg E, Tefferi A, Bloomfield CD: The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009, 114: 937-951. 10.1182/blood-2009-03-209262.CrossRefPubMed Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A, Harris NL, Le Beau MM, Hellström-Lindberg E, Tefferi A, Bloomfield CD: The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009, 114: 937-951. 10.1182/blood-2009-03-209262.CrossRefPubMed
21.
go back to reference Dearden CE, Johnson R, Pettengell R, Devereux S, Cwynarski K, Whittaker S, McMillan A, British Committee for Standards in Haematology: Guidelines for the management of mature T-cell and NK-cell neoplasms (excluding cutaneous T-cell lymphoma). Br J Haematol. 2011, 153: 451-485. 10.1111/j.1365-2141.2011.08651.x.CrossRefPubMed Dearden CE, Johnson R, Pettengell R, Devereux S, Cwynarski K, Whittaker S, McMillan A, British Committee for Standards in Haematology: Guidelines for the management of mature T-cell and NK-cell neoplasms (excluding cutaneous T-cell lymphoma). Br J Haematol. 2011, 153: 451-485. 10.1111/j.1365-2141.2011.08651.x.CrossRefPubMed
22.
go back to reference Isomoto H, Ishii H, Matsushima K, Ohnita K, Nakayama T, Hayashi T, Nakao K, Gastrointestinal: Novel endocytoscopic findings of gastric low-grade mucosa-associated lymphoid tissue lymphoma. J Gastroenterol Hepatol. 2012, 27: 1535-10.1111/j.1440-1746.2012.07203.x.CrossRefPubMed Isomoto H, Ishii H, Matsushima K, Ohnita K, Nakayama T, Hayashi T, Nakao K, Gastrointestinal: Novel endocytoscopic findings of gastric low-grade mucosa-associated lymphoid tissue lymphoma. J Gastroenterol Hepatol. 2012, 27: 1535-10.1111/j.1440-1746.2012.07203.x.CrossRefPubMed
23.
go back to reference Ono S, Kato M, Ono Y, Nishida U, Yamamoto K, Shimizu Y, Asaka M: Target biopsy using magnifying endoscopy in clinical management of gastric mucosa-associated lymphoid tissue lymphoma. J Gastroenterol Hepatol. 2011, 26: 1133-1138. 10.1111/j.1440-1746.2011.06729.x.CrossRefPubMed Ono S, Kato M, Ono Y, Nishida U, Yamamoto K, Shimizu Y, Asaka M: Target biopsy using magnifying endoscopy in clinical management of gastric mucosa-associated lymphoid tissue lymphoma. J Gastroenterol Hepatol. 2011, 26: 1133-1138. 10.1111/j.1440-1746.2011.06729.x.CrossRefPubMed
24.
go back to reference Fasoli A, Pugliese V, Furnari M, Gatteschi B, Truini M, Meroni E: Signet ring cell carcinoma of the stomach: correlation between endocytoscopy and histology. Endoscopy. 2009, 41: E65-E66. 10.1055/s-0028-1119475.CrossRefPubMed Fasoli A, Pugliese V, Furnari M, Gatteschi B, Truini M, Meroni E: Signet ring cell carcinoma of the stomach: correlation between endocytoscopy and histology. Endoscopy. 2009, 41: E65-E66. 10.1055/s-0028-1119475.CrossRefPubMed
25.
go back to reference El-Zahabi LM, Jamali FR, El-Hajj II, Naja M, Salem Z, Shamseddine A, El-Saghir NS, Zaatari G, Geara F, Soweid AM: The value of EUS in predicting the response of gastric mucosa-associated lymphoid tissue lymphoma to Helicobacter pylori eradication. Gastrointest Endosc. 2007, 65: 89-96. 10.1016/j.gie.2006.05.009.CrossRefPubMed El-Zahabi LM, Jamali FR, El-Hajj II, Naja M, Salem Z, Shamseddine A, El-Saghir NS, Zaatari G, Geara F, Soweid AM: The value of EUS in predicting the response of gastric mucosa-associated lymphoid tissue lymphoma to Helicobacter pylori eradication. Gastrointest Endosc. 2007, 65: 89-96. 10.1016/j.gie.2006.05.009.CrossRefPubMed
26.
go back to reference Nakamura S, Matsumoto T, Suekane H, Takeshita M, Hizawa K, Kawasaki M, Yao T, Tsuneyoshi M, Iida M, Fujishima M: Predictive value of endoscopic ultrasonography for regression of gastric low grade and high grade MALT lymphomas after eradication of Helicobacter pylori. Gut. 2001, 48: 454-460. 10.1136/gut.48.4.454.CrossRefPubMedPubMedCentral Nakamura S, Matsumoto T, Suekane H, Takeshita M, Hizawa K, Kawasaki M, Yao T, Tsuneyoshi M, Iida M, Fujishima M: Predictive value of endoscopic ultrasonography for regression of gastric low grade and high grade MALT lymphomas after eradication of Helicobacter pylori. Gut. 2001, 48: 454-460. 10.1136/gut.48.4.454.CrossRefPubMedPubMedCentral
27.
go back to reference Sackmann M, Morgner A, Rudolph B, Neubauer A, Thiede C, Schulz H, Kraemer W, Boersch G, Rohde P, Seifert E, Stolte M, Bayerdoerffer E: Regression of gastric MALT lymphoma after eradication of Helicobacter pylori is predicted by endosonographic staging. MALT Lymphoma Study Group. Gastroenterology. 1997, 113: 1087-1090. 10.1053/gast.1997.v113.pm9322502.CrossRefPubMed Sackmann M, Morgner A, Rudolph B, Neubauer A, Thiede C, Schulz H, Kraemer W, Boersch G, Rohde P, Seifert E, Stolte M, Bayerdoerffer E: Regression of gastric MALT lymphoma after eradication of Helicobacter pylori is predicted by endosonographic staging. MALT Lymphoma Study Group. Gastroenterology. 1997, 113: 1087-1090. 10.1053/gast.1997.v113.pm9322502.CrossRefPubMed
Metadata
Title
Endocytoscopic findings of lymphomas of the stomach
Authors
Hajime Isomoto
Kayoko Matsushima
Tomayoshi Hayashi
Yoshitaka Imaizumi
Junya Shiota
Hiroyuki Ishii
Hitomi Minami
Ken Ohnita
Fuminao Takeshima
Saburo Shikuwa
Yasushi Miyazaki
Kazuhiko Nakao
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2013
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/1471-230X-13-174

Other articles of this Issue 1/2013

BMC Gastroenterology 1/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.