Japanese Journal of Radiology

, Volume 37, Issue 12, pp 817–825 | Cite as

Usefulness of histologic differences and perivascular infiltration for preoperative T staging of advanced gastric cancer using computed tomography

  • Ji Youn Kim
  • Woo-Suk ChungEmail author
  • Hyeun Jin Lee
  • Ji Hae An
  • Jang Shin Son
Original Article



This study aimed to determine whether histologic differences and perivascular infiltration are useful for clinical T staging of advanced gastric cancer (AGC).

Materials and methods

This retrospective study included 160 patients with pathologically confirmed AGC who had available preoperative stomach computed tomography (CT). Using stomach CT, they were classified according to standard T stage, histologic T stage, and perivascular T stage. Accuracy of each T stage criteria was analyzed. Perivascular infiltrations for the evaluation of prognosis were correlated with time to tumor progression by log-rank test.


There was a significant difference between the accuracies of the standard and histologic T stages (p < 0.001), whereas there was no significant difference between the standard and perivascular T stages (p = 0.07). In 121 patients who were pathologically confirmed as having T3 or T4a tumor, there was a significant difference between the standard and perivascular T stage (p < 0.001). In patients having T3 or T4a tumor, time to tumor progression of the negative perivascular infiltration subgroup was significantly longer than the positive subgroup.


Consideration of histologic differences and perivascular infiltration may be useful for clinical T staging of AGC.


Computed tomography Gastric cancer Histology Perivascular infiltration Staging 


Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by JYK and W-SC. The first draft of the manuscript was written by JYK and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.


  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.CrossRefGoogle Scholar
  2. 2.
    Sim SH, Kim YJ, Oh DY, Lee SH, Kim DW, Kang WJ, et al. The role of PET/CT in detection of gastric cancer recurrence. BMC Cancer. 2009;9:73.CrossRefGoogle Scholar
  3. 3.
    Park YK, Yoon HM, Kim YW, Park JY, Ryu KW, Lee YJ, et al. Laparoscopy-assisted versus open D2 distal gastrectomy for advanced gastric cancer: results from a randomized phase II multicenter clinical trial (COACT 1001). Ann Surg. 2018;267:638–45.CrossRefGoogle Scholar
  4. 4.
    Kim YW, Yoon HM, Yun YH, Nam BH, Eom BW, Baik YH, et al. Long-term outcomes of laparoscopy-assisted distal gastrectomy for early gastric cancer: result of a randomized controlled trial (COACT 0301). Surg Endosc. 2013;27:4267–76.CrossRefGoogle Scholar
  5. 5.
    Bang YJ, Kim YW, Yang HK, Chung HC, Park YK, Lee KH, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet. 2012;379:315–21.CrossRefGoogle Scholar
  6. 6.
    Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11:439–49.CrossRefGoogle Scholar
  7. 7.
    Choi YY, Bae JM, An JY, Hyung WJ, Noh SH. Laparoscopic gastrectomy for advanced gastric cancer: are the long-term results comparable with conventional open gastrectomy? A systematic review and meta-analysis. J Surg Oncol. 2013;108:550–6.CrossRefGoogle Scholar
  8. 8.
    Park DJ, Han SU, Hyung WJ, Kim MC, Kim W, Ryu SY, et al. Long-term outcomes after laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective study. Surg Endosc. 2012;26:1548–53.CrossRefGoogle Scholar
  9. 9.
    Kubota K, Suzuki A, Shiozaki H, Wada T, Kyosaka T, Kishida A. Accuracy of multidetector-row computed tomography in the preoperative diagnosis of lymph node metastasis in patients with gastric cancer. Gastrointest Tumors. 2017;3:163–70.CrossRefGoogle Scholar
  10. 10.
    Botet JF, Lightdale CJ, Zauber AG, Gerdes H, Winawer SJ, Urmacher C, et al. Preoperative staging of gastric cancer: comparison of endoscopic US and dynamic CT. Radiology. 1991;181:426–32.CrossRefGoogle Scholar
  11. 11.
    Lim JS, Yun MJ, Kim MJ, Hyung WJ, Park MS, Choi JY, et al. CT and PET in stomach cancer: preoperative staging and monitoring of response to therapy. Radiographics. 2006;26:143–56.CrossRefGoogle Scholar
  12. 12.
    Choi JI, Joo I, Lee JM. State-of-the-art preoperative staging of gastric cancer by MDCT and magnetic resonance imaging. J Gastroenterol. 2014;20:4546–57.Google Scholar
  13. 13.
    Nakamura K, Sugano H, Takagi K. Carcinoma of the stomach in incipient phase: its histogenesis and histological appearances. Gan. 1968;59:251–8.PubMedGoogle Scholar
  14. 14.
    Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRefGoogle Scholar
  15. 15.
    Zheng HC, Li XH, Hara T, Masuda S, Yang XH, Guan YF, et al. Mixed-type gastric carcinomas exhibit more aggressive features and indicate the histogenesis of carcinomas. Virchows Arch. 2008;452:525–34.CrossRefGoogle Scholar
  16. 16.
    Kim TU, Kim S, Lee JW, Lee NK, Jeon TY, Park DY. MDCT features in the differentiation of T4a gastric cancer from less-advanced gastric cancer: significance of the hyperattenuating serosa sign. Br J Radiol. 2013;86:20130290.CrossRefGoogle Scholar
  17. 17.
    Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A III. AJCC cancer staging manual. 7th ed. New York: Springer; 2009. p. 117–126.Google Scholar
  18. 18.
    Sun R, Tang L, Chen Y, Li X, Sun Y, Li ZY, et al. Feasibility of differentiating T3 from T4a gastric cancer in different Lauren classification by determining serosa invasion: diagnostic performance of high enhanced serosa sign. Chin J Can Res. 2018;30:263–71.CrossRefGoogle Scholar
  19. 19.
    Kim YN, Choi D, Kim SH, Kim MJ, Lee SJ, Lee WJ, et al. Gastric cancer staging at isotropic MDCT including coronal and sagittal MPR images: endoscopically diagnosed early vs. advanced gastric cancer. Abdom Imaging. 2009;34:26–34.CrossRefGoogle Scholar
  20. 20.
    Chen CY, Wu DC, Kang WY, Hsu JS. Staging of gastric cancer with 16-channel MDCT. Abdom Imaging. 2006;31:514–20.CrossRefGoogle Scholar
  21. 21.
    Bang CS, Park JM, Baik GH, Park JJ, Joo MK, Jang JY, et al. Therapeutic outcomes of endoscopic resection of early gastric cancer with undifferentiated-type histology: a Korean ESD registry database analysis. Clin Endosc. 2017;50:569–77.CrossRefGoogle Scholar
  22. 22.
    Humar B, Blair V, Charlton A, More H, Martin I, Guilford P. E-cadherin deficiency initiates gastric signet-ring cell carcinoma in mice and man. Cancer Res. 2009;69:2050–6.CrossRefGoogle Scholar
  23. 23.
    Furue M. Epithelial tumor, invasion and stroma. Ann Dermatol. 2011;23:125–31.CrossRefGoogle Scholar
  24. 24.
    Tsurumaru D, Miyasaka M, Muraki T, Nishie A, Asayama Y, Oki E, et al. Histopathologic diversity of gastric cancers: relationship between enhancement pattern on dynamic contrast-enhanced CT and histological type. Eur J Radiol. 2017;97:90–5.CrossRefGoogle Scholar
  25. 25.
    Tsurumaru D, Miyasaka M, Muraki T, Asayama Y, Nishie A, Oki E, et al. Diffuse-type gastric cancer: specific enhancement pattern on multiphasic contrast-enhanced computed tomography. Jpn J Radiol. 2017;35:289–95.CrossRefGoogle Scholar
  26. 26.
    Lee MH, Choi D, Park MJ, Lee MW. Gastric cancer: imaging and staging with MDCT based on the 7th AJCC guidelines. Abdom Imaging. 2012;37:531–40.CrossRefGoogle Scholar
  27. 27.
    Choi JI, Joo I, Lee JM. State-of-the-art preoperative staging of gastric cancer by MDCT and magnetic resonance imaging. World J Gastroenterol. 2014;20:4546–57.CrossRefGoogle Scholar

Copyright information

© Japan Radiological Society 2019

Authors and Affiliations

  1. 1.Department of Diagnostic RadiologyKonyang University Hospital, Konyang University College of MedicineDaejeonRepublic of Korea
  2. 2.Department of PathologyKonyang University Hospital, Konyang University College of MedicineDaejeonRepublic of Korea

Personalised recommendations