Document Detail

A case of enteropathy-type T-cell lymphoma diagnosed by small bowel enteroscopy: a perspective on imaging-enhanced endoscopy.
Jump to Full Text
MedLine Citation:
PMID:  23170160     Owner:  NLM     Status:  PubMed-not-MEDLINE    
Enteropathy-type T-cell lymphoma (ETL) or enteropathy-associated T-cell lymphoma is a very rare malignant intestinal tumor. ETL is usually diagnosed by surgery. Endoscopic findings of ETL are not well known, and there are few reports of findings from endoscopy that has been performed only using white light. Additionally, there are no definite treatment guidelines for ETL. Therefore, we report a case of ETL diagnosed by enteroscopy with imaging-enhanced endoscopy and also review recently developed treatment options.
Jun Yong Bae; Bong Min Ko; Seul Ki Min; Jong Chan Lee; Gun Wha Lee; La Young Yoon; Su Jin Hong; Moon Sung Lee; Hee Kyung Kim
Publication Detail:
Type:  Journal Article     Date:  2012-10-18
Journal Detail:
Title:  Gut and liver     Volume:  6     ISSN:  2005-1212     ISO Abbreviation:  Gut Liver     Publication Date:  2012 Oct 
Date Detail:
Created Date:  2012-11-21     Completed Date:  2012-11-22     Revised Date:  2013-11-13    
Medline Journal Info:
Nlm Unique ID:  101316452     Medline TA:  Gut Liver     Country:  Korea (South)    
Other Details:
Languages:  eng     Pagination:  516-9     Citation Subset:  -    
Department of Internal Medicine, Soonchunhyang University Bucheon Hospital, Soonchunhyang University College of Medicine, Bucheon, Korea.
Export Citation:
APA/MLA Format     Download EndNote     Download BibTex
MeSH Terms

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-ta): Gut Liver
Journal ID (iso-abbrev): Gut Liver
Journal ID (publisher-id): GNL
ISSN: 1976-2283
ISSN: 2005-1212
Publisher: The Korean Society of Gastroenterology; the Korean Society of Gastrointestinal Endoscopy; the Korean Association for the Study of the Liver; the Korean Society of Neurogastroenterology and Motility; Korean Association for the Study of Intestinal Diseases; Korean College of Helicobacter and Upper Gastrointestinal Research; Korean Pancreatobiliary Association; Korean Society of Gastrointestinal Cancer
Article Information
Download PDF
Copyright © 2012 by the Korean Society of Gastroenterology, the Korean Society of Gastrointestinal Endoscopy, the Korean Society of Neurogastroenterology and Motility, Korean College of Helicobacter and Upper Gastrointestinal Research, Korean Association for the Study of Intestinal Diseases, the Korean Association for the Study of the Liver, Korean Pancreatobiliary Association, and Korean Society of Gastrointestinal Cancer
Received Day: 19 Month: 8 Year: 2010
Revision Received Day: 22 Month: 11 Year: 2010
Accepted Day: 28 Month: 12 Year: 2010
Print publication date: Month: 10 Year: 2012
Electronic publication date: Day: 18 Month: 10 Year: 2012
Volume: 6 Issue: 4
First Page: 516 Last Page: 519
PubMed Id: 23170160
ID: 3493736
DOI: 10.5009/gnl.2012.6.4.516

A Case of Enteropathy-Type T-Cell Lymphoma Diagnosed by Small Bowel Enteroscopy: A Perspective on Imaging-Enhanced Endoscopy
Jun Yong Bae*
Bong Min Ko*
Seul Ki Min*
Jong Chan Lee*
Gun Wha Lee*
La Young Yoon*
Su Jin Hong*
Moon Sung Lee*
Hee Kyung Kim
*Department of Internal Medicine, Soonchunhyang University Bucheon Hospital, Soonchunhyang University College of Medicine, Bucheon, Korea.
Department of Pathology, Soonchunhyang University Bucheon Hospital, Soonchunhyang University College of Medicine, Bucheon, Korea.
Correspondence: Correspondence to: Moon Sung Lee. Department of Internal Medicine, Soonchunhyang University Bucheon Hospital, Soonchunhyang University College of Medicine, 170 Jomaru-ro, Wonmi-gu, Bucheon 420-767, Korea. Tel: +82-32-621-5096, Fax: +82-32-621-5080,


Enteropathy-type T-cell lymphoma (ETL) is primary extranodal T-cell lymphoma arising in the intestine originating from intraepitheial T-cells.1 ETL is very rare and accounts for fewer than 5% of all gastrointestinal tract lymphomas. The clinical course of ETL is very aggressive. Five-year survival rate is 20% to 25%.2-6 The treatment options are chemotherapy with or without radiotherapy and surgery. Currently, there are no definite treatment guidelines for ETL. Diagnosis of ETL was very difficult and usually made by surgery because of complications of ETL at presenting time, such as intestinal perforation or obstruction, or lack of endoscopic experiences. There were few articles about endoscopic findings of ETL with only white light and capsule endoscopy.7-12


A 70-year-old malnourished male patient visited because of anemia and hematochezia. Hemoglobin was 8.9 g/dL and albumin was 2.9 g/dL. There was no definite bleeding focus found on gastroscopy and colonoscopy. Relatively long segmental wall thickening of jejunum with mild dilatation, fluid collection and suspicious mesenteric fat infiltration was noted on abdominal computed tomography. Increased fluorodeoxyglucose (FDG) uptake (SUV, 6.0) was also noted on 18-FDG positron emission tomography (Fig. 1). To evaluate for obscure gastrointestinal bleeding and small intestinal mass, double-balloon enteroscopy (EN-450T5; Fujinon, Saitama, Japan) was performed via oral route and showed multiple small shallow ulcerations, edematous villi and fusion of villi (Fig. 2). Push enteroscopy with conventional colonoscopy via oral route (CF-H260AL; Olympus, Tokyo, Japan) showed mosaic and fissured like villi and more prominent nodularity mucosal pattern with narrow band imaging (NBI) and indigocarmin spray (Fig. 3). The biopsy result was mature T-cell lymphoma. Immunohistochemical staining showed CD3 (+), CD8 (+), CD56 (+), TLA-1 (+), CD4 (-), CD5 (-), CD20 (-), and CD30 (-) (Fig. 4).13 On bone marrow examination, there was no abnormality.

The patient was treated with rituximab, cyclophosphamide, adriamycin, vincristine, and prednisone (R-CHOP) chemotherapy and radiotherapy. Six months after the initial diagnosis, the patient underwent an operation because of intestinal obstruction with perforation and died from sepsis.


Mean age of diagnosed ETL was 60 years old and sex ratio of ETL was about 1:1 (male:female). ETL commonly arises in the proximal jejunum. But, less frequently, ETL can arise anywhere in the small intestine, stomach and colon. About 40% of ETL patients have acute clinical manifestations such as acute peritonitis due to perforation and intestinal obstruction which needs emergent operation. Other clinical manifestations are abdominal pain, weight loss and protein losing enteropathy. In early disease, ETL is localized in gastrointestinal tract or mesenteric lymph node. As progression of disease, it can spread to liver, spleen, skin, or other organs.5,14 Prognosis of ETL is very poor. Five-year survival rate is 20% to 25%.2-6

Few endoscopic findings of ETL were reported by enteroscopy and capsule endoscopy.7-12 Typical endoscopic findings of ETL are multiple shallow ulcerations and diffuse thickening of mucosa with innumerable coarse or fine granular elevations (mosaic mucosal pattern). No articles have been published about NBI of ETL. In our case of ETL, more prominent mucosal nodularity and scalloing was observed with NBI and indigocarmin spray. The specimen of ETL endoscopic mucosal biopsy shows that mucosal edema and villous distortion by tumor cell infiltration (Fig. 3). This is a reason of nodularity with NBI and indigocarmin spray.

There is no definite treatment guideline of ETL. The surgery for ETL has poor outcomes and its role is limited to debulking and/or treatment of ETL complications such as perforation and obstruction. Radiation therapy has been indicated for bulky disease or incomplete resection. Chemotherapy such as vincristine, doxorubicin, methotrexate, and prednisolone (VAMP); vincristine, doxorubicin, and prednisolone (VAP); CHOP; procarbazine, etoposide, prednisolone,and doxorubicin (PEPA); cyclophosphamide, etoposide, vincristine, and prednisone (CEOP); prednisolone, cytarabine, lomustine, etoposide, and thioguanine-bleomycin, vincrisitine and methotrexate (PEACE-BOM); and surgery are options for treatment of ETL.5 But, more than half were unable to complete their planned chemotherapy courses and early treatment failure is frequently occurred because of malnourished state and complications of disease or chemotherapy. Overall response rate of treatment is 58%. But 16% of patients died after first cycle of chemotherapy. Mean recurrence time after chemotherapy or surgery was 6 months.

Recently, some clinical trials for feasibility and activity of high-dose chemotherapy supported by autologous stem cells transplantation (ASCT) as therapeutic option for ETL in small series15-17 and retrospective studies.18-20 In these clinical trials, ASCT could increase overall survival rate, even up to 60%. There are two reports of chemotherapy with ASCT about prevention of ETL21 and reduction in aberrant T-cells in patients with refractory celiac disease.22

Alemtuzumab, humanized anti-CD52 monoclonal antibody currently used in treatment of chronic lymphocytic leukemia or T-cell lymphoma, can be another option for ETL.23,24 Alemtuzumab can treat ETL successfully with chemotherapy. But, all ETL cases who were treated by alemtuzumab were only two. There is the report about increased risk for ETL with using this monoclonal antibody for treatment of refractory celiac disease.25 So, more clinical studies are needed for alemtuzumab.

In conclusion, ETL is a very rare intestinal tumor. The endoscopic characteristics are edematous vili, fusion of vili, and multiple shallow ulcerations. In chromoendoscopy, indigocarmin and NBI, prominent mucosal noduarity, fissured or mosaic patterns are the characteristics of ETL. There is no treatment guideline for ETL. But, recently, molecular target agent such as alemtuzumab and ASCT can be the treatment options for ETL instead of conventional chemotherapy with poor outcomes.


No potential conflict of interest relevant to this article was reported.

1. O'Farrelly C,Feighery C,O'Briain DS,et al. Humoral response to wheat protein in patients with coeliac disease and enteropathy associated T cell lymphomaBr Med J (Clin Res Ed)Year: 1986293908910
2. d'Amore F,Brincker H,Gronbaek K,et al. Danish Lymphoma Study GroupNon-Hodgkin's lymphoma of the gastrointestinal tract: a population-based analysis of incidence, geographic distribution, clinicopathologic presentation features, and prognosisJ Clin OncolYear: 199412167316848040680
3. Morton JE,Leyland MJ,Vaughan Hudson G,et al. Primary gastrointestinal non-Hodgkin's lymphoma: a review of 175 British National Lymphoma Investigation casesBr J CancerYear: 1993677767828471435
4. Daum S,Hummel M,Weiss D,et al. Refractory sprue syndrome with clonal intraepithelial lymphocytes evolving into overt enteropathy-type intestinal T-cell lymphomaDigestionYear: 200062606510899727
5. Gale J,Simmonds PD,Mead GM,Sweetenham JW,Wright DH. Enteropathy-type intestinal T-cell lymphoma: clinical features and treatment of 31 patients in a single centerJ Clin OncolYear: 20001879580310673521
6. Honemann D,Prince HM,Hicks RJ,Seymour JF. Enteropathy-associated T-cell lymphoma without a prior diagnosis of coeliac disease: diagnostic dilemmas and management optionsAnn HematolYear: 20058411812115452669
7. Joyce AM,Burns DL,Marcello PW,Tronic B,Scholz FJ. Capsule endoscopy findings in celiac disease associated enteropathy-type intestinal T-cell lymphomaEndoscopyYear: 20053759459615933938
8. Hadithi M,Akol H,Al-Toma A,Jacobs M,Mulder CJ. Indigo carmine chromoendoscopic appearances of enteropathy-associated T-cell lymphoma during double-balloon endoscopy in a patient with celiac diseaseEndoscopyYear: 200739Suppl 1E212E21317614075
9. 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 diseaseAm J GastroenterolYear: 200710298799617378908
10. Yanai S,Matsumoto T,Nakamura S,et al. Endoscopic findings of enteropathy-type T-cell lymphomaEndoscopyYear: 200739Suppl 1E339E34018273786
11. Daum S,Wahnschaffe U,Glasenapp R,et al. Capsule endoscopy in refractory celiac diseaseEndoscopyYear: 20073945545817516353
12. Sato Y,Ono M,Sagawa T,et al. Endoscopic findings of enteropathy-type T-cell lymphoma by double-balloon enteroscopy and capsule endoscopyDig EndoscYear: 20102224324520642619
13. Zettl A,deLeeuw R,Haralambieva E,Mueller-Hermelink HK. Enteropathy-type T-cell lymphomaAm J Clin PatholYear: 200712770170617511112
14. Isaacson P,Wright D,Ralfkiaer E,et al. Jaffe ES,Harris NL,Stein H,et al.Enteropathy-type T-cell lymphomaPathology and genetics of tumours of haematopoietic and lymphoid tissuesYear: 2001LyonIARC Press208209
15. Okuda M,Nomura J,Tateno H,Kameoka J,Sasaki T. CD56 positive intestinal T-cell lymphoma: treatment with high dose chemotherapy and autologous peripheral blood stem cell transplantationIntern MedYear: 20024173473712322803
16. Al-Toma A,Verbeek WH,Visser OJ,et al. Disappointing outcome of autologous stem cell transplantation for enteropathy-associated T-cell lymphomaDig Liver DisYear: 20073963464117531561
17. Rongey C,Micallef I,Smyrk T,Murray J. Successful treatment of enteropathy-associated T cell lymphoma with autologous stem cell transplantDig Dis SciYear: 2006511082108616865575
18. Bishton MJ,Haynes AP. Combination chemotherapy followed by autologous stem cell transplant for enteropathy-associated T cell lymphomaBr J HaematolYear: 200713611111317116129
19. d'Amore F,Relander T,Lauritzen GF,et al. Dose-dense induction followed by autologous stem cell transplant (ASCT) leads to sustained remissions in a large fraction of patients with previously untreated peripheral t-cell lymphomas (PTCLS): overall and subtype-specific results of a phase ii study from the nordic lymphoma groupHaematologicaYear: 200994Suppl 243719176364
20. Sieniawski M,Angamuthu N,Boyd K,et al. Evaluation of enteropathy-associated T-cell lymphoma comparing standard therapies with a novel regimen including autologous stem cell transplantationBloodYear: 20101153664367020197551
21. Meijer JW,Mulder CJ,Goerres MG,Boot H,Schweizer JJ. Coeliac disease and (extra)intestinal T-cell lymphomas: definition, diagnosis, and treatmentScand J Gastroenterol SupplYear: 2004788415696854
22. Al-toma A,Visser OJ,van Roessel HM,et al. Autologous hematopoietic stem cell transplantation in refractory celiac disease with aberrant T cellsBloodYear: 20071092243224917068146
23. Gallamini A,Zaja F,Patti C,et al. Alemtuzumab (Campath-1H) and CHOP chemotherapy as first-line treatment of peripheral T-cell lymphoma: results of a GITIL (Gruppo Italiano Terapie Innovative nei Linfomi) prospective multicenter trialBloodYear: 20071102316232317581918
24. Soldini D,Mora O,Cavalli F,Zucca E,Mazzucchelli L. Efficacy of alemtuzumab and gemcitabine in a patient with enteropathy-type T-cell lymphomaBr J HaematolYear: 200814248448618510686
25. Vivas S,Ruiz de Morales JM,Ramos F,Suárez-Vilela D. Alemtuzumab for refractory celiac disease in a patient at risk for enteropathy-associated T-cell lymphomaN Engl J MedYear: 20063542514251516760460

Article Categories:
  • Case Report

Keywords: Enteropathy-type T-cell lymphoma, Imaging enhanced endoscopy, Narrow band image.

Previous Document:  A case of acute myocarditis as the initial presentation of Crohn's disease.
Next Document:  A case of nonalcoholic steatohepatitis and small intestinal bacterial overgrowth with peripheral ede...