Abstract
The aim was to determine the prevalence of small bowel involvement in patients with gastrointestinal (GI) lymphoma by double-balloon endoscopy (DBE). We examined 29 patients with primary GI lymphoma by oral and anal DBEs. Clinicopathologic features related to the prevalence of diminutive small bowel involvement and the clinical outcome were retrospectively investigated. Diminutive small bowel lesions were found in 14 patients. The prevalence of the lesions was not different between patients with primary small bowel lymphoma and those with primary extra-small bowel lymphoma (50% versus 47%, P = 0.6). However, clinical stage was more advanced in patients with the lesions than in those without (P < 0.05). The lesions were more frequently found in T-cell lymphoma (100%) and follicular lymphoma (77%) than in the other types of lymphoma (15%) (P < 0.05). Diminutive small intestinal lesions occur in patients with GI lymphoma, especially in those with follicular lymphoma and T-cell lymphoma. GI lymphomas of these histologic types are candidates for scrutiny by DBE.
Similar content being viewed by others
References
Freeman C, Berg JW, Cutler SJ. Occurrence and prognosis of extranodal lymphomas. Cancer. 1972;29:252–260. doi:.10.1002/1097-0142(197201)29:1<252::AID-CNCR2820290138>3.0.CO;2-#
Isaacson PG. Gastrointestinal lymphoma. Hum Pathol. 1994;25:1020–1029. doi:10.1016/0046-8177(94)90060-4.
Nakamura S, Matsumoto T, Iida M, Yao T, Tsuneyoshi M. Primary gastrointestinal lymphoma in Japan. A clinicopathologic analysis of 455 patients with special reference to its time trends. Cancer. 2003;97:2462–2473. doi:10.1002/cncr.11415.
Nakamura S, Matsumoto T, Takeshita M, et al. A clinicopathologic study of primary small intestine lymphoma. Prognostic significance of mucosa-associated lymphoid tissue-derived lymphoma. Cancer. 2000;88:286–294. doi:.10.1002/(SICI)1097-0142(20000115)88:2<286::AID-CNCR7>3.0.CO;2-Z
Kohno S, Oshima K, Yoneda S, Kodama T, Shirakusa T, Kikuchi M. Clinicopathological analysis of 143 primary malignant lymphomas in the small and large intestines based on the new WHO classification. Histopathology. 2003;41:135–143. doi:10.1046/j.1365-2559.2003.01659.x.
LeBrun DP, Kamel OW, Cleary ML, Dorfman RF, Warnke RA. Follicular lymphomas of the gastrointestinal tract, pathologic features in 31 cases and bcl-2 oncogene protein expression. Am J Pathol. 1992;140:1327–1335.
Shia J, Teruya-Feodstein J, Pan D, et al. Primary follicular lymphoma of the gastrointestinal tract. A clinical and pathologic study of 26 cases. Am J Surg Pathol. 2002;26:216–224. doi:10.1097/00000478-200202000-00008.
Bende RJ, Smit LA, Bossenbroek JG, et al. Primary follicular lymphoma of the small intestine. α4β7 expression and immunoglobulin configuration suggest an origin from local antigen- experienced cells. Am J Pathol. 2003;162:105–113.
Damaj G, Verkarre V, Delmer A, et al. Primary follicular lymphoma of the gastrointestinal tract. A study of 25 cases and a literature review. Ann Oncol. 2003;14:623–628. doi:10.1093/annonc/mdg168.
Yoshino T, Miyake K, Ichimura K, et al. Increased incidence of follicular lymphoma in the duodenum. Am J Surg Pathol. 2000;24:688–693. doi:10.1097/00000478-200005000-00007.
Moynihan MJ, Bast MA, Chan WC, et al. Lymphomatous polyposis. A neoplasm of either follicular mantle or germinal center cell origin. Am J Surg Pathol. 1996;20:442–452. doi:10.1097/00000478-199604000-00007.
Hashimoto Y, Nakamura N, Kuze T, Ono N, Abe M. Multiple lymphomatous polyposis of the gastrointestinal tract is a heterogeneous group that includes mantle cell lymphoma and follicular lymphoma. Analysis of somatic mutation of immunoglobulin heavy chain gene variable region. Hum Pathol. 1999;30:581–587. doi:10.1016/S0046-8177(99)90205-8.
Kodama T, Ohshima K, Nomura K, et al. Lymphomatous polyposis of the gastrointestinal tract, including mantle cell lymphoma, follicular lymphoma and mucosa-associated lymphoid tissue lymphoma. Histopathology. 2005;47:467–478. doi:10.1111/j.1365-2559.2005.02225.x.
Iddan G, Meron G, Glukhovsky A, Swain P. Wireless capsule endoscopy. Nature. 2000;405:17. doi:10.1038/35013140.
Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc. 2001;53:216–220. doi:10.1067/mge.2001.112181.
Yamamoto H, Kita H, Sunada K, et al. Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases. Clin Gastroenterol Hepatol. 2004;2:1010–1016. doi:10.1016/S1542-3565(04)00453-7.
Flieger D, Keller R, May A, Ell C, Fischbach W. Capsule endoscopy in gastrointestinal lymphomas. Endoscopy. 2005;37:1174–1180. doi:10.1055/s-2005-921045.
Joyce AM, Burns DL, Marcello PW, Tronic B, Scholz FJ. Capsule endoscopy findings in celiac disease associated with enteropathy-type intestinal T-cell lymphoma. Endoscopy. 2005;37:594–596. doi:10.1055/s-2005-861322.
Esaki M, Matsumoto T, Nakamura S, et al. Capsule endoscopy findings in intestinal follicular lymphoma. Endoscopy. 2007;39:E86–E87. doi:10.1055/s-2006-945152.
van Deursen CT, Goedhard JG, Jie KS, Theunissen P. Primary intestinal follicular lymphoma diagnosed by video capsule endoscopy and double-balloon enteroscopy. Endoscopy. 2008;40:E8–E9. doi:10.1055/s-2007-995379.
Nakamura S, Matsumoto T, Umeno J, et al. Endoscopic features of intestinal follicular lymphoma. The value of double-balloon endoscopy. Endoscopy. 2007;39:E26–E27. doi:10.1055/s-2007-966223.
Schäfer C, Razziourrouh B, Diepolder H, Göke B. B-Cell lymphoma with bowel-to-bowel penetration diagnosed by double-balloon endoscopy. Endoscopy. 2007;39:E204. doi:10.1055/s-2007-966425.
Weigand K, Ganten TM, Andrulis M, Stremmel W, Sauer P, Schaible A. Chronic anemia masking a primary large B-cell lymphoma of the small intestine, finally diagnosed by double-balloon enteroscopy. Endoscopy. 2008;40:E149. doi:10.1055/s-2007-995772.
Hotta K, Oyama T, Kitamura Y, Tomori A, Miyata Y, Mitsuishi T. Mantle cell lymphoma presenting as multiple lymphomatous polyposis spreading widely to the small intestine and diagnosed by double-balloon endoscopy. Endoscopy. 2007;39:E347–E348. doi:10.1055/s-2007-995331.
Kodama M, Kitadai Y, Shishido T, et al. Primary follicular lymphoma of the gastrointestinal tract. A retrospective case series. Endoscopy. 2008;40:343–346. doi:10.1055/s-2007-995365.
Matsumoto T, Esaki M, Yada S, Jo Y, Moriyama T, Iida M. Is small bowel radiography necessary before double-balloon endoscopy? AJR Am J Roentgenol. 2008;191:175–181. doi:10.2214/AJR.07.3155.
Rohatiner A, D’Amore F, Coiffier B, et al. Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994;5:397–400.
May A, Nachbar L, Schneider M, Neumann M, Ell C. Push-and-pull enteroscopy using the double-balloon technique: method of assessing depth of insertion and training of the enteroscopy technique using the Erlangen Endo-Trainer. Endoscopy. 2005;37:66–70. doi:10.1055/s-2004-826177.
Jaffe ES, Harris NL, Sein H, et al. World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of Haematopoitic and Lymphoid Tissues. Lyon, France: IARC; 2001.
Fine KD, Stone MJ. Alpha-heavy chain disease, Mediterranean lymphoma, and immunoproliferative small intestinal disease. A review of clinicopathological features, pathogenesis, and differential diagnosis. Am J Gastroenterol. 1999;94:1139–1152.
Lecruit M, Abachin E, Martin A, et al. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med. 2004;350:239–248. doi:10.1056/NEJMoa031887.
Hadithi M, Al-toma A, Oudejans J, van Bodegraven AA, Mulder CJ, Jacobs M. The value of double-balloon enteroscopy in patients with refractory celiac disease. Am J Gastroenterol. 2007;102:987–996. doi:10.1111/j.1572-0241.2007.01122.x.
Yanai S, Matsumoto T, Nakamura S, et al. Endoscopic findings of enteropathy-type T-cell lymphoma. Endoscopy. 2007;39:E339–E340. doi:10.1055/s-2007-967063.
Cornes JS. Multiple lymphomatous polyposis of the gastrointestinal tract. Cancer. 1961;14:249–257. doi:.10.1002/1097-0142(196103/04)14:2<249::AID-CNCR2820140205>3.0.CO;2-8
O’Briain DS, Kennedy MJ, Daly PA, et al. Multiple lymphomatous polyposis of the gastrointestinal tract. A clinicopathologically distinctive form of non-Hodgkin’s lymphoma of B-cell centrocytic type. Am J Surg Pathol. 1989;13:691–699.
Peters JHC, Rondonotti E, Weijmer MC, Mulder CJJ, Jacobs MAJM. Lymphomatous polyposis of the small intestine. Gastrointest Endosc. 2008;67:763–765. doi:10.1016/j.gie.2007.09.035.
Du MG, Xu CF, Diss TC, et al. Intestinal dissemination of gastric mucosa-associated lymphoid tissue lymphoma. Blood. 1996;88:4445–4451.
Raderer M, Vorbeck F, Formanek M, et al. Importance of extensive staging in patients with mucosa-associated lymphoid tissue (MALT)-type lymphoma. Br J Cancer. 2000;83:454–457. doi:10.1054/bjoc.2000.1308.
Iwano M, Okazaki K, Uchida K, et al. Characteristics of gastric B-cell lymphoma of mucosa-associated lymphoid tissue type involving multiple organs. J Gastroenterol. 2004;39:739–746. doi:10.1007/s00535-004-1382-1.
Raderer M, Wöhrer S, Streubel B, et al. Assessment of disease dissemination in gastric compared with extragastric mucosa-associated lymphoid tissue lymphoma using extensive staging. A single-center experience. J Clin Oncol. 2006;24:3136–3141. doi:10.1200/JCO.2006.06.0723.
de Boer JP, Hiddink RF, Raderer M, et al. Dissemination patterns in non-gastric MALT lymphoma. Haematologica. 2008;93:201–206. doi:10.3324/haematol.11835.
Koch P, del Valle F, Berdel WE, et al. Primary gastrointestinal non-Hodgkin’s lymphoma. Anatomic and histologic distribution, clinical features, and survival data of 371 patients registered in the German multicenter study GIT NHL 01/92. J Clin Oncol. 2001;19:3861–3873.
Daum S, Ullich R, Heise W, et al. Intestinal non-Hodgkin’s lymphoma. A multicenter prospective clinical study from the German study group on intestinal non-Hodgkin’s lymphoma. J Clin Oncol. 2003;21:2740–2746. doi:10.1200/JCO.2003.06.026.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsumoto, T., Nakamura, S., Esaki, M. et al. Double-Balloon Endoscopy Depicts Diminutive Small Bowel Lesions in Gastrointestinal Lymphoma. Dig Dis Sci 55, 158–165 (2010). https://doi.org/10.1007/s10620-009-0713-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10620-009-0713-8