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Digestive Diseases and Sciences

, Volume 63, Issue 10, pp 2617–2625 | Cite as

Expression of Gastric Markers Is Associated with Malignant Potential of Nonampullary Duodenal Adenocarcinoma

  • Chihiro Minatsuki
  • Nobutake Yamamichi
  • Ken-ichi Inada
  • Yu Takahashi
  • Kouhei Sakurai
  • Takeshi Shimamoto
  • Yosuke Tsuji
  • Kazuya Shiogama
  • Shinya Kodashima
  • Yoshiki Sakaguchi
  • Keiko Niimi
  • Satoshi Ono
  • Toru Niwa
  • Ken Ohata
  • Nobuyuki Matsuhashi
  • Masao Ichinose
  • Mitsuhiro Fujishiro
  • Yutaka Tsutsumi
  • Kazuhiko Koike
Original Article

Abstract

Background

Sporadic nonampullary duodenal epithelial tumors (NADETs) are uncommon, and thus their clinicopathological features have not been fully assessed.

Aims

In this study, we have analyzed a series of early sporadic NADETs, focusing on various immunohistological features.

Methods

We conducted a multicenter retrospective analysis of 68 patients with endoscopically resected sporadic NADETs. Associations between immunohistological features and clinicopathological features were statistically analyzed.

Results

The 68 patients consisted of 46 men (68%) and 22 women (32%) with a mean age of 60.7 ± 12.2 years (range 37–85 years). The 68 tumors were composed of 39 adenomas (57%) and 29 early-stage adenocarcinomas (43%). Duodenal adenocarcinomas were larger in size than adenomas and had papillary architecture in their pathological diagnosis with statistical significance. Duodenal adenocarcinomas also demonstrated a significantly higher expression of gastric markers (MUC5AC and MUC6) and a higher MIB-1 index. Duodenal adenomas were contrastively apt to express intestinal markers (MUC2, CDX1 and CDX2). Of the 68 cases analyzed, there were only 3 tumors positive for p53 staining, all of which were adenocarcinoma. When 7 submucosal invasive cancers and 21 intramucosal cancers were compared, submucosal invasion was positively associated with expression of MUC5AC. Also, submucosal invasion showed strong association with double-positivity of MUC5AC and MUC6.

Conclusions

Our results indicate that immunohistochemical evaluation is useful for predicting malignant potential of NADETs, especially focusing on the expression of gastrointestinal markers.

Keywords

Sporadic nonampullary duodenal epithelial tumors Adenocarcinoma Adenoma Gastric marker 

Notes

Acknowledgments

The authors thank Dr. Yosuke Muraki from Wakayama Medical University Hospital.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10620_2018_5179_MOESM1_ESM.tif (3.5 mb)
Supplementary material 1 (TIFF 3615 kb)
10620_2018_5179_MOESM2_ESM.doc (32 kb)
Supplementary material 2 (DOC 32 kb)

References

  1. 1.
    Neugut AI, Jacobson JS, Suh S, et al. The epidemiology of cancer of the small bowel. Cancer Epidemiol Biomark Prev. 1998;7:243–251.Google Scholar
  2. 2.
    Poultsides GA, Huang LC, Cameron JL, et al. Duodenal adenocarcinoma: clinicopathologic analysis and implications for treatment. Ann Surg Oncol. 2012;19:1928–1935.CrossRefGoogle Scholar
  3. 3.
    Aparicio T, Zaanan A, Svrcek M, et al. Small bowel adenocarcinoma: epidemiology, risk factors, diagnosis and treatment. Dig Liver Dis. 2014;46:97–104.CrossRefGoogle Scholar
  4. 4.
    Bilimoria KY, Bentrem DJ, Wayne JD, et al. Small bowel cancer in the United States: changes in epidemiology, treatment, and survival over the last 20 years. Ann Surg. 2009;249:63–71.CrossRefGoogle Scholar
  5. 5.
    Lu Y, Fröbom R, Lagergren J. Incidence patterns of small bowel cancer in a population-based study in Sweden: increase in duodenal adenocarcinoma. Cancer Epidemiol. 2012;36:e158–e163.CrossRefGoogle Scholar
  6. 6.
    Bosman FT, Carneiro F, Hruban RH, Theise ND, eds. WHO Classification of Tumours of the Digestive System, 4th edn.Google Scholar
  7. 7.
    Fernández-Esparrach G, Calderón A, de la Peña J, et al. Endoscopic submucosal dissection. Endoscopy. 2014;46:361–370.CrossRefGoogle Scholar
  8. 8.
    Obata S, Suenaga M, Araki K, et al. Use of strip biopsy in a case of early duodenal cancer. Endoscopy. 1992;24:232–234.CrossRefGoogle Scholar
  9. 9.
    Abbass R, Rigaux J, Al-Kawas FH. Nonampullary duodenal polyps: characteristics and endoscopic management. Gastrointest Endosc. 2010;71:754–759.CrossRefGoogle Scholar
  10. 10.
    Maruoka D, Arai M, Kishimoto T, et al. Clinical outcomes of endoscopic resection for nonampullary duodenal high-grade dysplasia and intramucosal carcinoma. Endoscopy. 2013;45:138–141.CrossRefGoogle Scholar
  11. 11.
    Sohn JW, Jeon SW, Cho CM, et al. Endoscopic resection of duodenal neoplasms: a single-center study. Surg Endosc. 2010;24:3195–3200.CrossRefGoogle Scholar
  12. 12.
    Nonaka S, Oda I, Tada K, et al. Clinical outcome of endoscopic resection for nonampullary duodenal tumors. Endoscopy. 2015;47:129–135.CrossRefGoogle Scholar
  13. 13.
    Takimoto K, Imai Y, Matsuyama K. Endoscopic tissue shielding method with polyglycolic acid sheets and fibrin glue to prevent delayed perforation after duodenal endoscopic submucosal dissection. Dig Endosc. 2014;26:46–49.CrossRefGoogle Scholar
  14. 14.
    Matsumoto S, Miyatani H, Yoshida Y. Future directions of duodenal endoscopic submucosal dissection. World J Gastrointest Endosc. 2015;7:389–395.CrossRefGoogle Scholar
  15. 15.
    Bourke MJ. Endoscopic resection in the duodenum: current limitations and future directions. Endoscopy. 2013;45:127–132.CrossRefGoogle Scholar
  16. 16.
    Gotoda T. Endoscopic resection of early gastric cancer. Gastric Cancer. 2007;10:1–11.CrossRefGoogle Scholar
  17. 17.
    Kakushima N, Kanemoto H, Sasaki K, et al. Endoscopic and biopsy diagnoses of superficial, nonampullary, duodenal adenocarcinomas. World J Gastroenterol. 2015;21:5560–5567.CrossRefGoogle Scholar
  18. 18.
    Goda K, Kikuchi D, Yamamoto Y, et al. Endoscopic diagnosis of superficial non-ampullary duodenal epithelial tumors in Japan: multicenter case series. Dig Endosc. 2014;26:23–29.CrossRefGoogle Scholar
  19. 19.
    Japanese GCA. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14:113–123.CrossRefGoogle Scholar
  20. 20.
    Okada K, Fujisaki J, Kasuga A, et al. Sporadic nonampullary duodenal adenoma in the natural history of duodenal cancer: a study of follow-up surveillance. Am J Gastroenterol. 2010;106:357–364.CrossRefGoogle Scholar
  21. 21.
    Maruoka D, Arai M, Ishigami H, et al. Sporadic nonampullary duodenal adenoma/carcinoma is associated with not only colon adenoma/carcinoma but also gastric cancer: association of location of duodenal lesions with comorbid diseases. Scand J Gastroenterol. 2015;50:333–340.CrossRefGoogle Scholar
  22. 22.
    Yamamichi N, Inada K, Ichinose M, et al. Frequent loss of Brm expression in gastric cancer correlates with histologic features and differentiation state. Cancer Res. 2007;67:10727–10735.CrossRefGoogle Scholar
  23. 23.
    Konno-Shimizu M, Yamamichi N, Inada K, et al. Cathepsin E is a marker of gastric differentiation and signet-ring cell carcinoma of stomach: a novel suggestion on gastric tumorigenesis. PLoS ONE. 2013;8:e56766.CrossRefGoogle Scholar
  24. 24.
    Dowsett M, Nielsen TO, A’Hern R, et al. Assessment of Ki67 in breast cancer: recommendations from the International Ki67 in Breast Cancer working group. J Natl Cancer Inst. 2011;103:1656–1664.CrossRefGoogle Scholar
  25. 25.
    Urruticoechea A, Smith IE, Dowsett M. Proliferation marker Ki-67 in early breast cancer. J Clin Oncol. 2005;23:7212–7220.CrossRefGoogle Scholar
  26. 26.
    Zhang S, Cui Y, Zhong B, et al. Clinicopathological characteristics and survival analysis of primary duodenal cancers: a 14-year experience in a tertiary centre in South China. Int J Colorectal Dis. 2011;26:219–226.CrossRefGoogle Scholar
  27. 27.
    Oka S, Tanaka S, Nagata S, et al. Clinicopathologic features and endoscopic resection of early primary nonampullary duodenal carcinoma. J Clin Gastroenterol. 2003;37:381–386.CrossRefGoogle Scholar
  28. 28.
    Ushiku T, Arnason T, Fukayama M, et al. Extra-ampullary duodenal adenocarcinoma. Am J Surg Pathol. 2014;38:1484–1493.CrossRefGoogle Scholar
  29. 29.
    Solaini L, Jamieson NB, Metcalfe M, et al. Outcome after surgical resection for duodenal adenocarcinoma in the UK. Br J Surg. 2015;102:676–681.CrossRefGoogle Scholar
  30. 30.
    Park SM, Ham JH, Kim BW, et al. Feasibility of endoscopic resection for sessile nonampullary duodenal tumors: a multicenter retrospective study. Gastroenterol Res Pract. 2015;2015:692492.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Arai T, Murata T, Sawabe M, et al. Primary adenocarcinoma of the duodenum in the elderly: clinicopathological and immunohistochemical study of 17 cases. Pathol Int. 1999;49:23–29.CrossRefGoogle Scholar
  32. 32.
    Bartman AE, Buisine MP, Aubert JP, et al. The MUC6 secretory mucin gene is expressed in a wide variety of epithelial tissues. J Pathol. 1998;186:398–405.CrossRefGoogle Scholar
  33. 33.
    Ushiku T, Arnason T, Ban S, et al. Very well-differentiated gastric carcinoma of intestinal type: analysis of diagnostic criteria. Mod Pathol. 2013;26:1620–1631.CrossRefGoogle Scholar
  34. 34.
    Saleh HA, Aburashed A, Bober P, et al. P53 protein immunohistochemical expression in colonic adenomas with and without associated carcinoma. Am J Gastroenterol. 1998;93:980–984.CrossRefGoogle Scholar
  35. 35.
    Hong MK, Laskin WB, Herman BE, et al. Expansion of the Ki-67 proliferative compartment correlates with degree of dysplasia in Barrett’s esophagus. Cancer. 1995;75:423–429.CrossRefGoogle Scholar
  36. 36.
    Matsumoto T, Iida M, Nakamura S, et al. Depressed adenoma of the duodenum in patients with familial adenomatous polyposis: endoscopic and immunohistochemical features. Cancer. 1999;86:1414–1420.CrossRefGoogle Scholar
  37. 37.
    Kushima R, Stolte M, Dirks K, et al. Gastric-type adenocarcinoma of the duodenal second portion histogenetically associated with hyperplasia and gastric-foveolar metaplasia of Brunner’s glands. Virchows Arch. 2002;440:655–659.CrossRefGoogle Scholar
  38. 38.
    Kushima R, Ruthlein HJ, Stolte M, et al. ‘Pyloric gland-type adenoma’ arising in heterotopic gastric mucosa of the duodenum, with dysplastic progression of the gastric type. Virchows Arch. 1999;435:452–457.CrossRefGoogle Scholar
  39. 39.
    Yamamichi N, Inada K, Furukawa C, et al. Cdx2 and the Brm-type SWI/SNF complex cooperatively regulate villin expression in gastrointestinal cells. Exp Cell Res. 2009;315:1779–1789.CrossRefGoogle Scholar
  40. 40.
    Zhang HY, Spechler SJ, Souza RF. Esophageal adenocarcinoma arising in Barrett esophagus. Cancer Lett. 2009;275:170–177.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Chihiro Minatsuki
    • 1
  • Nobutake Yamamichi
    • 1
  • Ken-ichi Inada
    • 2
  • Yu Takahashi
    • 1
  • Kouhei Sakurai
    • 2
  • Takeshi Shimamoto
    • 4
  • Yosuke Tsuji
    • 1
  • Kazuya Shiogama
    • 3
  • Shinya Kodashima
    • 1
  • Yoshiki Sakaguchi
    • 1
  • Keiko Niimi
    • 1
  • Satoshi Ono
    • 1
  • Toru Niwa
    • 5
  • Ken Ohata
    • 6
  • Nobuyuki Matsuhashi
    • 6
  • Masao Ichinose
    • 5
  • Mitsuhiro Fujishiro
    • 1
  • Yutaka Tsutsumi
    • 3
  • Kazuhiko Koike
    • 1
  1. 1.Department of Gastroenterology, Graduate School of MedicineThe University of TokyoHongoJapan
  2. 2.Department of Diagnostic Pathology IIFujita Health University School of MedicineNagoya CityJapan
  3. 3.Department of PathologyFujita Health University School of MedicineToyoakeJapan
  4. 4.Kameda Medical Center MakuhariChiba-shiJapan
  5. 5.Wakayama Medical University HospitalWakayama-shiJapan
  6. 6.NTT Medical Center TokyoTokyoJapan

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