Gastric Cancer

, Volume 22, Issue 4, pp 881–891 | Cite as

Pylorus-preserving gastrectomy for early cancer involving the upper third: can we go higher?

  • Chun-Chao Zhu
  • Hui Cao
  • Felix Berlth
  • Jia Xu
  • Shin-Hoo Park
  • Hwi-Nyeong Choe
  • Yun-Suhk Suh
  • Seong-Ho Kong
  • Hyuk-Joon Lee
  • Woo-Ho Kim
  • Han-Kwang YangEmail author
Original Article



Pylorus-preserving gastrectomy (PPG) is commonly performed for early gastric cancer (EGC) located in middle third of the stomach. We investigated the surgical, oncological, and functional outcomes of PPG involving the upper third of stomach.


We included all patients of the period 2013–2016 who underwent PPG, distal subtotal gastrectomy (DSG), and total gastrectomy (TG) for EGC involving the upper third by carefully defining the localization. Surgical, oncological, and functional outcome analyses included postoperative morbidity, lymph-node metastasis, tumor recurrence, postoperative body weight, body mass index, hemoglobin, total protein, albumin, quantification of intraabdominal fat, and gallstone development.


Overall, 288 cases were analyzed: 145 PPG, 61 DSG, and 82 TG. In the study period, patients potentially underwent PPG for EGC involving the upper third, if enough proximal remnant stomach was found whilst achieving a sufficient proximal margin. PPG resulted in less operation time (p < 0.001), less blood loss (p = 0.002) and lower postoperative morbidity compared to TG. For lymph-node (LN) stations being resected in all groups, no difference was found in number of resected LN. Recurrence-free survival was similar for all groups. PPG showed advantages regarding postoperative body weight, hemoglobin, total protein, albumin in postoperative 6 and 12 month follow-up. Lowest decrease of abdominal fat area after 12 months was seen for PPG. Gallstone incidence was significantly lower after PPG compared to TG (p < 0.001).


For EGC involving the upper third, PPG can be another good option with lower postoperative morbidity, better functional outcomes, and same oncological safety.


Pylorus-preserving gastrectomy Upper stomach Early gastric cancer Outcomes 



This study is supported by fund of Seoul National University Hospital College of Medicine Research Foundation (0420163130), and Projects of Science and Technology Commission of Shanghai Municipality (15410723000). Felix Berlth is supported by the German Research Foundation.

Compliance with ethical standards

Conflict of interest

No conflict of interest exists.

Ethics statement

This study was conducted in accordance with the Ethical Principles for Medical Research Involving Human Subjects, as outlined in the Declaration of Helsinki after the approval of the institutional review board of Seoul National University Hospital. Informed consent was waived by the institutional review board based on its decision that the risk of this study to the patient is minimal. The research protocol was approved by the institutional review board of Seoul National University Hospital (No. 1707-157-874).

Supplementary material

10120_2018_921_MOESM1_ESM.docx (2.7 mb)
Supplementary material 1 (DOCX 2780 KB)


  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–86.CrossRefGoogle Scholar
  2. 2.
    Leung WK, Wu MS, Kakugawa Y, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279–87.CrossRefGoogle Scholar
  3. 3.
    Information Committee of Korean Gastric Cancer A. Korean gastric cancer association nationwide survey on gastric cancer in 2014. J Gastric Cancer. 2016;16:131–40.CrossRefGoogle Scholar
  4. 4.
    Patru CL, Surlin V, Georgescu I, et al. Current issues in gastric cancer epidemiology. Rev Med Chir Soc Med Nat Iasi. 2013;117:199–204.Google Scholar
  5. 5.
    Hiki N, Nunobe S, Kubota T, et al. Function-preserving gastrectomy for early gastric cancer. Ann Surg Oncol. 2013;20:2683–92.CrossRefGoogle Scholar
  6. 6.
    Nomura E, Okajima K. Function-preserving gastrectomy for gastric cancer in Japan. World J Gastroenterol. 2016;22:5888–95.CrossRefGoogle Scholar
  7. 7.
    Suh YS, Han DS, Kong SH, et al. Laparoscopy-assisted pylorus-preserving gastrectomy is better than laparoscopy-assisted distal gastrectomy for middle-third early gastric cancer. Ann Surg. 2014;259:485–93.CrossRefGoogle Scholar
  8. 8.
    Hosoda K, Yamashita K, Sakuramoto S, et al. Postoperative quality of life after laparoscopy-assisted pylorus-preserving gastrectomy compared With laparoscopy-assisted distal gastrectomy: a cross-sectional postal questionnaire survey. Am J Surg. 2017;213:763–70.CrossRefGoogle Scholar
  9. 9.
    Aizawa M, Honda M, Hiki N, et al. Oncological outcomes of function-preserving gastrectomy for early gastric cancer: a multicenter propensity score matched cohort analysis comparing pylorus-preserving gastrectomy versus conventional distal gastrectomy. Gastric Cancer. 2017;20:709–17.CrossRefGoogle Scholar
  10. 10.
    Xiao XM, Gaol C, Yin W, et al. Pylorus-preserving versus distal subtotal gastrectomy for surgical treatment of early gastric cancer: a meta-analysis. Hepatogastroenterology. 2014;61:870–79.Google Scholar
  11. 11.
    Oh SY, Lee HJ, Yang HK. Pylorus-preserving gastrectomy for gastric cancer. J Gastric Cancer. 2016;16:63–71.CrossRefGoogle Scholar
  12. 12.
    Morita S, Katai H, Saka M, et al. Outcome of pylorus-preserving gastrectomy for early gastric cancer. Br J Surg. 2008;95:1131–5.CrossRefGoogle Scholar
  13. 13.
    Takeuchi H, Kitagawa Y. Is pylorus-preserving gastrectomy universally applicable to early gastric cancer of the mid stomach? Ann Surg Oncol. 2014;21:356–7.CrossRefGoogle Scholar
  14. 14.
    Japanese Gastric Cancer A. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20:1–19.CrossRefGoogle Scholar
  15. 15.
    Japanese Gastric Cancer A. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRefGoogle Scholar
  16. 16.
    Jeong SH, Bae K, Ha CY, et al. Effectiveness of endoscopic clipping and computed tomography gastroscopy for the preoperative localization of gastric cancer. J Korean Surg Soc. 2013;84:80–7.CrossRefGoogle Scholar
  17. 17.
    Hur H, Son SY, Cho YK, et al. Intraoperative gastroscopy for tumor localization in laparoscopic surgery for gastric adenocarcinoma. J Vis Exp. 2016. Scholar
  18. 18.
    Washington K. 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol. 2010;17:3077–9.CrossRefGoogle Scholar
  19. 19.
    Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien–Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.CrossRefGoogle Scholar
  20. 20.
    Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.CrossRefGoogle Scholar
  21. 21.
    Irlbeck T, Massaro JM, Bamberg F, et al. Association between single-slice measurements of visceral and abdominal subcutaneous adipose tissue with volumetric measurements: the Framingham Heart Study. Int J Obes. 2010;34:781–7.CrossRefGoogle Scholar
  22. 22.
    Borkan GA, Gerzof SG, Robbins AH, et al. Assessment of abdominal fat content by computed tomography. Am J Clin Nutr. 1982;36:172–7.CrossRefGoogle Scholar
  23. 23.
    Mauad FM, Chagas-Neto FA, Benedeti A, et al. Reproducibility of abdominal fat assessment by ultrasound and computed tomography. Radiol Bras. 2017;50:141–7.CrossRefGoogle Scholar
  24. 24.
    Jiang X, Hiki N, Nunobe S, et al. Laparoscopy-assisted subtotal gastrectomy with very small remnant stomach: a novel surgical procedure for selected early gastric cancer in the upper stomach. Gastric Cancer. 2011;14:194–9.CrossRefGoogle Scholar
  25. 25.
    Kosuga T, Hiki N, Nunobe S, et al. Feasibility and nutritional impact of laparoscopy-assisted subtotal gastrectomy for early gastric cancer in the upper stomach. Ann Surg Oncol. 2014;21:2028–35.CrossRefGoogle Scholar
  26. 26.
    Isozaki H, Matsumoto S, Murakami S, et al. Diminished gastric resection preserves better quality of life in patients with early gastric cancer. Acta Med Okayama. 2016;70:119–30.Google Scholar
  27. 27.
    Kim KH, Park DJ, Park YS, et al. Actual 5-year nutritional outcomes of patients with gastric cancer. J Gastric Cancer. 2017;17:99–109.CrossRefGoogle Scholar
  28. 28.
    Tsujiura M, Hiki N, Ohashi M, et al. Excellent long-term prognosis and favorable postoperative nutritional status after laparoscopic pylorus-preserving gastrectomy. Ann Surg Oncol. 2017;24:2233–40.CrossRefGoogle Scholar
  29. 29.
    Ikeguchi M, Kuroda H, Kihara K, et al. Nutritional assessment of patients after pylorus-preserving gastrectomy for early gastric cancer. Indian J Surg. 2010;72:453–7.CrossRefGoogle Scholar
  30. 30.
    Kong SH, Kim JW, Lee HJ, et al. The safety of the dissection of lymph node stations 5 and 6 in pylorus-preserving gastrectomy. Ann Surg Oncol. 2009;16:3252–8.CrossRefGoogle Scholar
  31. 31.
    Kawakatsu S, Ohashi M, Hiki N, et al. Use of endoscopy to determine the resection margin during laparoscopic gastrectomy for cancer. Br J Surg. 2017;104:1829–36.CrossRefGoogle Scholar
  32. 32.
    Han KB, Jang YJ, Kim JH, et al. Clinical significance of the pattern of lymph node metastasis depending on the location of gastric cancer. J Gastric Cancer. 2011;11:86–93.CrossRefGoogle Scholar
  33. 33.
    Jun KH, Kim JH, Kim JJ, et al. Retrospective analysis on the gallstone disease after gastrectomy for gastric cancer. Gastroenterol Res Pract. 2015. Scholar
  34. 34.
    Zhu CC, Kim TH, Berlth F, et al. Clinical outcomes of intraoperative manual dilatation of pylorus in pylorus-preserving gastrectomy: a retrospective analysis. Gastric Cancer. 2018;21:864–70.CrossRefGoogle Scholar
  35. 35.
    Bae JS, Kim SH, Shin CI, et al. Efficacy of gastric balloon dilatation and/or retrievable stent insertion for pyloric spasms after pylorus-preserving gastrectomy: retrospective analysis. PLoS One. 2015;10:e0144470.CrossRefGoogle Scholar
  36. 36.
    Nunobe S, Hiki N, Fukunaga T, et al. Laparoscopy-assisted pylorus-preserving gastrectomy: preservation of vagus nerve and infrapyloric blood flow induces less stasis. World J Surg. 2007;31:2335–40.CrossRefGoogle Scholar
  37. 37.
    Jiang X, Hiki N, Nunobe S, et al. Postoperative outcomes and complications after laparoscopy-assisted pylorus-preserving gastrectomy for early gastric cancer. Ann Surg. 2011;253:928–33.CrossRefGoogle Scholar
  38. 38.
    Nakabayashi T, Mochiki E, Garcia M, et al. Pyloric motility after pylorus-preserving gastrectomy with or without the pyloric branch of the vagus nerve. World J Surg. 2002;26:577–83.CrossRefGoogle Scholar
  39. 39.
    Tomita R. Gastric emptying function in patients 5 years after pylorus-preserving distal gastrectomy with or without preserving pyloric and hepatic branches of the vagal nerve for early gastric cancer. World J Surg. 2009;33:2119–26.CrossRefGoogle Scholar
  40. 40.
    Nakane Y, Michiura T, Inoue K, et al. Length of the antral segment in pylorus-preserving gastrectomy. Br J Surg. 2002;89:220–4.Google Scholar
  41. 41.
    Nunobe S, Sasako M, Saka M, et al. Symptom evaluation of long-term postoperative outcomes after pylorus-preserving gastrectomy for early gastric cancer. Gastric Cancer. 2007;10:167–72.CrossRefGoogle Scholar
  42. 42.
    Tomita R, Fujisaki S, Koshinaga T, et al. Clinical assessments in patients ten years after pylorus-preserving gastrectomy with or without preserving both pyloric and hepatic branches of the vagal nerve for early gastric cancer. Hepatogastroenterology. 2010;57:984–8.Google Scholar
  43. 43.
    Liang TJ, Liu SI, Chen YC, et al. Analysis of gallstone disease after gastric cancer surgery. Gastric Cancer. 2017;20:895–903.CrossRefGoogle Scholar
  44. 44.
    Yamaguchi T, Ichikawa D, Kurioka H, et al. Postoperative clinical evaluation following pylorus-preserving gastrectomy. Hepatogastroenterology. 2004;51:883–6.Google Scholar
  45. 45.
    Nakane Y, Akehira K, Inoue K, et al. Postoperative evaluation of pylorus-preserving gastrectomy for early gastric cancer. Hepatogastroenterology. 2000;47:590–5.Google Scholar
  46. 46.
    Byun C, Han SU. Current status of randomized controlled trials for laparoscopic gastric surgery for gastric cancer in Korea. Asian J Endosc Surg. 2015;8:130–8.CrossRefGoogle Scholar
  47. 47.
    Lee JH. Ongoing surgical clinical trials on minimally invasive surgery for gastric cancer: Korea. Transl Gastroenterol Hepatol. 2016;1:40.CrossRefGoogle Scholar
  48. 48.
    Liedman B, Andersson H, Bosaeus I, et al. Changes in body composition after gastrectomy: results of a controlled, prospective clinical trial. World J Surg. 1997;21:416–20.CrossRefGoogle Scholar
  49. 49.
    Bozzetti F, Ravera E, Cozzaglio L, et al. Comparison of nutritional status after total or subtotal gastrectomy. Nutrition. 1990;6:371–5.Google Scholar
  50. 50.
    Kiyama T, Mizutani T, Okuda T, et al. Postoperative changes in body composition after gastrectomy. J Gastrointest Surg. 2005;9:313–9.CrossRefGoogle Scholar
  51. 51.
    Yoon DY, Kim HK, Kim JA, et al. Changes in the abdominal fat distribution after gastrectomy: computed tomography assessment. ANZ J Surg. 2007;77:121–5.CrossRefGoogle Scholar
  52. 52.
    Maurovich-Horvat P, Massaro J, Fox CS, et al. Comparison of anthropometric, area- and volume-based assessment of abdominal subcutaneous and visceral adipose tissue volumes using multi-detector computed tomography. Int J Obes (Lond). 2007;31:500–6.CrossRefGoogle Scholar

Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2019

Authors and Affiliations

  1. 1.Department of SurgerySeoul National University HospitalSeoulSouth Korea
  2. 2.Department of Gastrointestinal Surgery, Renji HospitalShanghai Jiao Tong University School of MedicineShanghaiChina
  3. 3.Department of General, Visceral and Cancer SurgeryUniversity Hospital CologneCologneGermany
  4. 4.Cancer Research InstituteSeoul National UniversitySeoulSouth Korea
  5. 5.Department of PathologySeoul National University HospitalSeoulSouth Korea

Personalised recommendations