A multicenter survey of enteroscopy for the diagnosis of intestinal follicular lymphoma

Iwamuro,Masaya; Okada,Hiroyuki; Kawano,Seiji; Shiode,Junji; Takenaka,Ryuta; Imagawa,Atsushi; Inaba,Tomoki; Suzuki,Seiyu; Nishimura,Mamoru; Mizuno,Motowo; Araki,Masashi; Mannami,Tomohiko; Ueki,Toru; Kobashi,Haruhiko; Fukatsu,Haruka; Tanaka,Shouichi; Omoto,Akiyoshi; Kawai,Yoshinari; Kitagawa,Takashi; Toyokawa,Tatsuya; Takata,Katsuyoshi; Yoshino,Tadashi; Takaki,Akinobu; Yamamoto,Kazuhide

doi:10.3892/ol.2015.3251

July-2015 Volume 10 Issue 1

Full Size Image

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

An International Open Access Journal Devoted to General Medicine.

July-2015 Volume 10 Issue 1

Full Size Image

Article Open Access

A multicenter survey of enteroscopy for the diagnosis of intestinal follicular lymphoma

Authors:
- Masaya Iwamuro
- Hiroyuki Okada
- Seiji Kawano
- Junji Shiode
- Ryuta Takenaka
- Atsushi Imagawa
- Tomoki Inaba
- Seiyu Suzuki
- Mamoru Nishimura
- Motowo Mizuno
- Masashi Araki
- Tomohiko Mannami
- Toru Ueki
- Haruhiko Kobashi
- Haruka Fukatsu
- Shouichi Tanaka
- Akiyoshi Omoto
- Yoshinari Kawai
- Takashi Kitagawa
- Tatsuya Toyokawa
- Katsuyoshi Takata
- Tadashi Yoshino
- Akinobu Takaki
- Kazuhide Yamamoto
View Affiliations / Copyright

Affiliations: Department of Molecular Hepatology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama 700‑8558, Japan, Department of Endoscopy, Okayama University Hospital, Okayama 700‑8558, Japan, Department of Internal Medicine, Okayama Saiseikai General Hospital, Okayama 700‑8511, Japan, Department of Internal Medicine, Tsuyama Chuo Hospital, Tsuyama 708‑0841, Japan, Department of Gastroenterology, Mitoyo General Hospital, Kanonji 769‑1695, Japan, Department of Gastroenterology, Kagawa Prefectural Central Hospital, Takamatsu 760‑8557, Japan, Department of Internal Medicine, Sumitomo Besshi Hospital, Niihama 792‑8543, Japan, Department of Internal Medicine, Okayama City Hospital, Okayama 700‑8557, Japan, Department of Internal Medicine, Hiroshima City Hospital, Hiroshima 730‑8518, Japan, Department of Internal Medicine, Kagawa Rosai Hospital, Marugame 763‑8502, Japan, Department of Internal Medicine, Chugoku Central Hospital, Fukuyama 720‑0001, Japan, Department of Internal Medicine, Fukuyama City Hospital, Fukuyama 721‑8511, Japan, Department of Hepatology, Japanese Red Cross Okayama Hospital, Okayama 700‑8607, Japan, Department of Internal Medicine, St. Mary's Hospital, Himeji 670‑0801, Japan, Department of Gastroenterology, Iwakuni Clinical Center, Iwakuni 740‑8510, Japan, Department of Internal Medicine, Ako Central Hospital, Ako 678‑0241, Japan, Department of Gastroenterology, Onomichi Municipal Hospital, Onomichi 722‑8503, Japan, Department of Surgery, Kitagawa Hospital, Okayama 709‑0497, Japan, Department of Gastroenterology, Fukuyama Medical Center, Fukuyama 720‑8520, Japan, Department of Pathology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama 700‑8558, Japan, Department of Gastroenterology and Hepatology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama 700‑8558, Japan

Copyright: © Iwamuro et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Pages: 131-136
|
Published online on: May 20, 2015

https://doi.org/10.3892/ol.2015.3251
Expand metrics +

Abstract

The importance of enteroscopy examinations to investigate the entire length of the small intestines has been emphasized in follicular lymphoma patients with intestinal involvement. The aim of the present study was to determine the current state of enteroscopy examinations, including the performance rate, and the prevalence of small intestinal lesions in a patient population in Japan. A retrospective multicenter survey of 17 institutions collected the case information of 110 follicular lymphoma patients with gastrointestinal involvement. The results of the enteroscopy examinations were reviewed, and in order to identify potential factors affecting the performance rate of enteroscopy, patient gender, age at lymphoma diagnosis, histopathological grade, clinical stage, the date of the initial diagnosis and the annual volume of enteroscopy at the institution were compared between the patients who underwent one or more enteroscopy procedures and the patients who did not undergo enteroscopy. A total of 34 patients (30.9%) underwent enteroscopy, and 24 of these (70.6%) presented with involvement in the jejunum and/or ileum. It was found that more patients diagnosed in recent years and more patients treated at an ultra‑high volume institution (≥101 enteroscopy examinations/year) underwent an enteroscopy. In conclusion, although the prevalence of small intestinal lesions was high (70.6%) in the follicular lymphoma patients presenting with intestinal involvement, the performance rate of enteroscopy was only 30.9%, and thus the majority of the patients have not undergone enteroscopy examinations. Further investigation is required to define the clinical significance of enteroscopy at the initial diagnostic work‑up and during the follow‑up period of these patients.

View Figures

View References

1	Harris NL, Swerdlow SH, Jaffe ES, et al: Follicular lymphomaWHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Swerdlow SH, Campo E, Harris NL, et al: IARC press; Lyon, France: pp. 220–226. 2008
2	Dreyling M, Ghielmini M, Marcus R, Salles G and Vitolo UESMO Guidelines Working Group: Newly diagnosed and relapsed follicular lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 22 (suppl 6):vi59–vi63. 2011. View Article : Google Scholar : PubMed/NCBI
3	Schmatz AI, Streubel B, Kretschmer-Chott E, et al: Primary follicular lymphoma of the duodenum is a distinct mucosal/submucosal variant of follicular lymphoma: A retrospective study of 63 cases. J Clin Oncol. 29:1445–1451. 2011. View Article : Google Scholar : PubMed/NCBI
4	Takata K, Okada H, Ohmiya N, et al: Primary gastrointestinal follicular lymphoma involving the duodenal second portion is a distinct entity: A multicenter, retrospective analysis in Japan. Cancer Sci. 102:1532–1536. 2011. View Article : Google Scholar : PubMed/NCBI
5	Yamamoto S, Nakase H, Yamashita K, et al: Gastrointestinal follicular lymphoma: Review of the literature. J Gastroenterol. 45:370–388. 2010. View Article : Google Scholar : PubMed/NCBI
6	Yoshino T, Miyake K, Ichimura K, et al: Increased incidence of follicular lymphoma in the duodenum. Am J Surg Pathol. 24:688–693. 2000. View Article : Google Scholar : PubMed/NCBI
7	Higuchi N, Sumida Y, Nakamura K, et al: Impact of double-balloon endoscopy on the diagnosis of jejunoileal involvement in primary intestinal follicular lymphomas: A case series. Endoscopy. 41:175–178. 2009. View Article : Google Scholar : PubMed/NCBI
8	Akamatsu T, Kaneko Y, Ota H, Miyabayashi H, Arakura N and Tanaka E: Usefulness of double balloon enteroscopy and video capsule endoscopy for the diagnosis and management of primary follicular lymphoma of the gastrointestinal tract in its early stages. Dig Endosc. 22:33–38. 2010. View Article : Google Scholar : PubMed/NCBI
9	Kodama M, Kitadai Y, Shishido T, et al: Primary follicular lymphoma of the gastrointestinal tract: A retrospective case series. Endoscopy. 40:343–346. 2008. View Article : Google Scholar : PubMed/NCBI
10	Nakamura S, Matsumoto T, Umeno J, et al: Endoscopic features of intestinal follicular lymphoma: The value of double-balloon enteroscopy. Endoscopy. 39 (suppl 1):E26–E27. 2007. View Article : Google Scholar : PubMed/NCBI
11	Nakamura M, Ohmiya N, Hirooka Y, et al: Endoscopic diagnosis of follicular lymphoma with small-bowel involvement using video capsule endoscopy and double-balloon endoscopy: A case series. Endoscopy. 45:67–70. 2013.PubMed/NCBI
12	Takata K, Sato Y, Nakamura N, et al: Duodenal and nodal follicular lymphomas are distinct: The former lacks activation-induced cytidine deaminase and follicular dendritic cells despite ongoing somatic hypermutations. Mod Pathol. 22:940–949. 2009. View Article : Google Scholar : PubMed/NCBI
13	Takata K, Sato Y, Nakamura N, et al: Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics. Mod Pathol. 26:22–31. 2013. View Article : Google Scholar : PubMed/NCBI
14	Takata K, Tanino M, Ennishi D, et al: Duodenal follicular lymphoma: Comprehensive gene expression analysis with insights into pathogenesis. Cancer Sci. 105:608–615. 2014. View Article : Google Scholar : PubMed/NCBI
15	Sato Y, Ichimura K, Tanaka T, et al: Duodenal follicular lymphomas share common characteristics with mucosa-associated lymphoid tissue lymphomas. J Clin Pathol. 61:377–381. 2008. View Article : Google Scholar : PubMed/NCBI
16	Iwamuro M, Okada H, Takata K, et al: Diagnostic role of 18F-fluorodeoxyglucose positron emission tomography for follicular lymphoma with gastrointestinal involvement. World J Gastroenterol. 18:6427–6436. 2012. View Article : Google Scholar : PubMed/NCBI
17	Takeuchi K, Iwamuro M, Imagawa A, et al: Primary follicular lymphoma of the duodenum with erosions as atypical macroscopic features. Case Rep Med. 2012:5826072012.PubMed/NCBI
18	Iwamuro M, Okuda M, Yumoto E, et al: Magnifying endoscopy for intestinal follicular lymphoma is helpful for prompt diagnosis. Gut Liver. 7:258–261. 2013. View Article : Google Scholar : PubMed/NCBI
19	Iwamuro M, Shinagawa K, Okada H, Takata K, Yoshino T and Yamamoto K: Elevated soluble IL-2 receptor levels correlate with tumor bulk of follicular lymphomas with intestinal involvement. Clin Biochem. 47:191–195. 2014. View Article : Google Scholar : PubMed/NCBI
20	Harris NL, Jaffe ES, Diebold J, et al: World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: Report of the Clinical Advisory Committee meeting-Airlie House, Virginia, November 1997. J Clin Oncol. 17:3835–3849. 1999.PubMed/NCBI
21	Zucca E, Roggero E, Bertoni F and Cavalli F: Primary extranodal non-Hodgkin's lymphomas. Part 1 Gastrointestinal, cutaneous and genitourinary lymphomas. Ann Oncol. 8:727–737. 1997. View Article : Google Scholar : PubMed/NCBI
22	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. 5:397–400. 1994.PubMed/NCBI
23	Yamamoto H, Yano T, Kita H, Sunada K, Ido K and Sugano K: New system of double-balloon enteroscopy for diagnosis and treatment of small intestinal disorders. Gastroenterology. 125:1556–1557. 2003. View Article : Google Scholar : PubMed/NCBI
24	Nakamura M, Ohmiya N, Niwa Y and Goto H: Endoscopic examination for the small bowel-video capsule endoscopy and double balloon enteroscopy. Nihon Rinsho. 66:1253–1258. 2008.(In Japanese). PubMed/NCBI
25	Iddan G, Meron G, Glukhovsky A and Swain P: Wireless capsule endoscopy. Nature. 405:4172000. View Article : Google Scholar : PubMed/NCBI
26	Misdraji J, Harris NL, Hasserjian RP, Lauwers GY and Ferry JA: Primary follicular lymphoma of the gastrointestinal tract. Am J Surg Pathol. 35:1255–1263. 2011. View Article : Google Scholar : PubMed/NCBI
27	Campbell BA, Voss N, Woods R, et al: Long-term outcomes for patients with limited stage follicular lymphoma: Involved regional radiotherapy versus involved node radiotherapy. Cancer. 116:3797–3806. 2010. View Article : Google Scholar : PubMed/NCBI
28	Yanai S, Nakamura S, Takeshita M, et al: Translocation t(14;18)/IGH-BCL2 in gastrointestinal follicular lymphoma: Correlation with clinicopathologic features in 48 patients. Cancer. 117:2467–2477. 2011. View Article : Google Scholar : PubMed/NCBI
29	Mac Manus MP and Hoppe RT: Is radiotherapy curative for stage I and II low-grade follicular lymphoma? Results of a long-term follow-up study of patients treated at Stanford University. J Clin Oncol. 14:1282–1290. 1996.PubMed/NCBI
30	Gustavsson A, Osterman B and Cavallin-Ståhl E: A systematic overview of radiation therapy effects in non-Hodgkin's lymphoma. Acta Oncol. 42:605–619. 2003. View Article : Google Scholar : PubMed/NCBI

Journals

International Journal of Molecular Medicine

International Journal of Oncology

Molecular Medicine Reports

Oncology Reports

Experimental and Therapeutic Medicine

Oncology Letters

Biomedical Reports

Molecular and Clinical Oncology

World Academy of Sciences Journal

International Journal of Functional Nutrition

International Journal of Epigenetics

Medicine International

A multicenter survey of enteroscopy for the diagnosis of intestinal follicular lymphoma

This article is mentioned in:

Abstract

Figure 1

Figure 2

Figure 3

Related Articles