J Gastric Cancer.  2016 Jun;16(2):63-71. 10.5230/jgc.2016.16.2.63.

Pylorus-Preserving Gastrectomy for Gastric Cancer

• Oh SY
• Lee HJ
• Yang HK

• KMID: 2328071
• DOI: http://doi.org/10.5230/jgc.2016.16.2.63

Abstract

Pylorus-preserving gastrectomy (PPG) is a function-preserving surgery for the treatment of early gastric cancer (EGC), aiming to decrease the complication rate and improve postoperative quality of life. According to the Japanese gastric cancer treatment guidelines, PPG can be performed for cT1N0M0 gastric cancer located in the middle-third of the stomach, at least 4.0 cm away from the pylorus. Although the length of the antral cuff gradually increased, from 1.5 cm during the initial use of the procedure to 3.0 cm currently, its optimal length still remains unclear. Standard procedures for the preservation of pyloric function, infra-pyloric vessels, and hepatic branch of the vagus nerve, make PPG technically more difficult and raise concerns about incomplete lymph node dissection. The short- and long-term oncological and survival outcomes of PPG were comparable to those for distal gastrectomy, but with several advantages such as a lower incidence of dumping syndrome, bile reflux, and gallstone formation, and improved nutritional status. Gastric stasis, a typical complication of PPG, can be effectively treated by balloon dilatation and stent insertion. Robot-assisted pylorus-preserving gastrectomy is feasible for EGC in the middle-third of the stomach in terms of the short-term clinical outcome. However, any benefits over laparoscopy-assisted PPG (LAPPG) from the patient's perspective have not yet been proven. An ongoing Korean multicenter randomized controlled trial (KLASS-04), which compares LAPPG and laparoscopy-assisted distal gastrectomy for EGC in the middle-third of the stomach, may provide more clear evidence about the advantages and oncologic safety of PPG.

Keyword

Pylorus-preserving gastrectomy; Stomach neoplasms; Review

MeSH Terms

Asian Continental Ancestry Group
Bile Reflux
Dilatation
Dumping Syndrome
Gallstones
Gastrectomy*
Gastroparesis
Humans
Incidence
Lymph Node Excision
Nutritional Status
Pylorus
Quality of Life
Stents
Stomach
Stomach Neoplasms*
Vagus Nerve

Figure

• 

  Fig. 1 Station 5 and 6 lymph node metastases of gastric cancer in the middle-third of the stomach. Kong et al.30 examined the metastasis rate to each lymph node (LN) station in 1,802 patients with gastric cancer who underwent curative subtotal gastrectomy. Among patients with a distal resection margin (DRM) <6.0 cm, the metastasis rate to LN station 5 was 0.3% (1 of 317) for patients with a T1a cancer, 2.7% (8 of 293) for patients with a T1b cancer, and 8.0% (10 of 125) for patients with a T2a cancer. For metastasis to LN station 6, the rate was 0.6% (2 of 330) for patients with a T1a cancer, 9.5% (28 of 294) for patients with a T1b cancer, and 25.4% (33 of 130) for patients with a T2a cancer. M = mucosa; SM = submucosa; PM = proper muscle.

• 

  Fig. 2 Schematic diagram of the KLASS-04 study. PPG = pylorus-preserving gastrectomy; DG = distal gastrectomy.

Reference

1. Kim YG, Kong SH, Oh SY, Lee KG, Suh YS, Yang JY, et al. Effects of screening on gastric cancer management: comparative analysis of the results in 2006 and in 2011. J Gastric Cancer. 2014; 14:129–134.

2. Kim YW, Baik YH, Yun YH, Nam BH, Kim DH, Choi IJ, et al. Improved quality of life outcomes after laparoscopy-assisted distal gastrectomy for early gastric cancer: results of a prospective randomized clinical trial. Ann Surg. 2008; 248:721–727.

3. Ahn HS, Lee HJ, Yoo MW, Jeong SH, Park DJ, Kim HH, et al. Changes in clinicopathological features and survival after gastrectomy for gastric cancer over a 20-year period. Br J Surg. 2011; 98:255–260.

4. Adachi Y, Suematsu T, Shiraishi N, Katsuta T, Morimoto A, Kitano S, et al. Quality of life after laparoscopy-assisted Billroth I gastrectomy. Ann Surg. 1999; 229:49–54.

5. Lee HJ, Yang HK. Laparoscopic gastrectomy for gastric cancer. Dig Surg. 2013; 30:132–141.

6. Kim HH, Han SU, Kim MC, Hyung WJ, Kim W, Lee HJ, et al. Long-term results of laparoscopic gastrectomy for gastric cancer: a large-scale case-control and case-matched Korean multicenter study. J Clin Oncol. 2014; 32:627–633.

7. Kim W, Kim HH, Han SU, Kim MC, Hyung WJ, Ryu SW, et al. Decreased morbidity of laparoscopic distal gastrectomy compared with open distal gastrectomy for stage I gastric cancer: short-term outcomes from a multicenter randomized controlled trial (KLASS-01). Ann Surg. 2016; 263:28–35.

8. Saito T, Kurokawa Y, Takiguchi S, Mori M, Doki Y. Current status of function-preserving surgery for gastric cancer. World J Gastroenterol. 2014; 20:17297–17304.

9. Maki T, Shiratori T, Hatafuku T, Sugawara K. Pylorus-preserving gastrectomy as an improved operation for gastric ulcer. Surgery. 1967; 61:838–845.

10. Nunobe S, Sasako M, Saka M, Fukagawa T, Katai H, Sano T. Symptom evaluation of long-term postoperative outcomes after pylorus-preserving gastrectomy for early gastric cancer. Gastric Cancer. 2007; 10:167–172.

11. Park DJ, Lee HJ, Jung HC, Kim WH, Lee KU, Yang HK. Clinical outcome of pylorus-preserving gastrectomy in gastric cancer in comparison with conventional distal gastrectomy with Billroth I anastomosis. World J Surg. 2008; 32:1029–1036.

12. Suh YS, Han DS, Kong SH, Kwon S, Shin CI, Kim WH, et al. Laparoscopy-assisted pylorus-preserving gastrectomy is better than laparoscopy-assisted distal gastrectomy for middle-third early gastric cancer. Ann Surg. 2014; 259:485–493.

13. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011; 14:113–123.

14. Kodama M, Koyama K, Chida T, Arakawa A, Tur G. Early postoperative evaluation of pylorus-preserving gastrectomy for gastric cancer. World J Surg. 1995; 19:456–460. discussion 61.

15. Imada T, Rino Y, Takahashi M, Suzuki M, Tanaka J, Shiozawa M, et al. Postoperative functional evaluation of pylorus-preserving gastrectomy for early gastric cancer compared with conventional distal gastrectomy. Surgery. 1998; 123:165–170.

16. Zhang D, Shimoyama S, Kaminishi M. Feasibility of pylorus-preserving gastrectomy with a wider scope of lymphadenectomy. Arch Surg. 1998; 133:993–997.

17. Nakane Y, Michiura T, Inoue K, Sato M, Nakai K, Yamamichi K. Length of the antral segment in pylorus-preserving gastrectomy. Br J Surg. 2002; 89:220–224.

18. Nunobe S, Hiki N, Fukunaga T, Tokunaga M, Ohyama S, Seto Y, et al. Laparoscopy-assisted pylorus-preserving gastrectomy: preservation of vagus nerve and infrapyloric blood flow induces less stasis. World J Surg. 2007; 31:2335–2340.

19. Hotta T, Taniguchi K, Kobayashi Y, Johata K, Sahara M, Naka T, et al. Postoperative evaluation of pylorus-preserving procedures compared with conventional distal gastrectomy for early gastric cancer. Surg Today. 2001; 31:774–779.

20. Lee SW, Bouras G, Nomura E, Yoshinaka R, Tokuhara T, Nitta T, et al. Intracorporeal stapled anastomosis following laparoscopic segmental gastrectomy for gastric cancer: technical report and surgical outcomes. Surg Endosc. 2010; 24:1774–1780.

21. Morita S, Katai H, Saka M, Fukagawa T, Sano T, Sasako M. Outcome of pylorus-preserving gastrectomy for early gastric cancer. Br J Surg. 2008; 95:1131–1135.

22. Nagano H, Ohyama S, Sakamoto Y, Ohta K, Yamaguchi T, Muto T, et al. The endoscopic evaluation of gastritis, gastric remnant residue, and the incidence of secondary cancer after pylorus-preserving and transverse gastrectomies. Gastric Cancer. 2004; 7:54–59.

23. Nishikawa K, Kawahara H, Yumiba T, Nishida T, Inoue Y, Ito T, et al. Functional characteristics of the pylorus in patients undergoing pylorus: preserving gastrectomy for early gastric cancer. Surgery. 2002; 131:613–624.

24. Ohya T, Ohwada S, Iesato H, Takeyoshi I, Kawashima Y, Ogawa T, et al. Jejunal pouch interposition after pylorus-preserving gastrectomy. J Surg Res. 1999; 86:177–182.

25. Tomikawa M, Korenaga D, Akahoshi T, Kohshi K, Sugimachi K, Nagao Y, et al. Quality of life after laparoscopy-assisted pylorus-preserving gastrectomy: an evaluation using a questionnaire mailed to the patients. Surg Today. 2012; 42:625–632.

26. Tomita R, Fujisaki S, Tanjoh K. Pathophysiological studies on the relationship between postgastrectomy syndrome and gastric emptying function at 5 years after pylorus-preserving distal gastrectomy for early gastric cancer. World J Surg. 2003; 27:725–733.

27. Urushihara T, Sumimoto K, Shimokado K, Kuroda Y. Gastric motility after laparoscopically assisted distal gastrectomy, with or without preservation of the pylorus, for early gastric cancer, as assessed by digital dynamic x-ray imaging. Surg Endosc. 2004; 18:964–968.

28. Morita S, Sasako M, Saka M, Fukagawa T, Sano T, Katai H. Correlation between the length of the pyloric cuff and postoperative evaluation after pylorus-preserving gastrectomy. Gastric Cancer. 2010; 13:109–116.

29. Shibata C, Saijo F, Kakyo M, Kinouchi M, Tanaka N, Sasaki I, et al. Current status of pylorus-preserving gastrectomy for the treatment of gastric cancer: a questionnaire survey and review of literatures. World J Surg. 2012; 36:858–863.

30. Kong SH, Kim JW, Lee HJ, Kim WH, Lee KU, Yang HK. The safety of the dissection of lymph node stations 5 and 6 in pylorus-preserving gastrectomy. Ann Surg Oncol. 2009; 16:3252–3258.

31. Haruta S, Shinohara H, Ueno M, Udagawa H, Sakai Y, Uyama I. Anatomical considerations of the infrapyloric artery and its associated lymph nodes during laparoscopic gastric cancer surgery. Gastric Cancer. 2015; 18:876–880.

32. Sawai K, Takahashi T, Fujioka T, Minato H, Taniguchi H, Yamaguchi T. Pylorus-preserving gastrectomy with radical lymph node dissection based on anatomical variations of the infrapyloric artery. Am J Surg. 1995; 170:285–288.

33. Hiki N, Shimoyama S, Yamaguchi H, Kubota K, Kaminishi M. Laparoscopy-assisted pylorus-preserving gastrectomy with quality controlled lymph node dissection in gastric cancer operation. J Am Coll Surg. 2006; 203:162–169.

34. Tanaka N, Katai H, Saka M, Morita S, Fukagawa T. Laparoscopy-assisted pylorus-preserving gastrectomy: a matched case-control study. Surg Endosc. 2011; 25:114–118.

35. Hiki N, Kaminishi M. Pylorus-preserving gastrectomy in gastric cancer surgery: open and laparoscopic approaches. Langenbecks Arch Surg. 2005; 390:442–447.

36. Kumagai K, Hiki N, Nunobe S, Sekikawa S, Chiba T, Kiyokawa T, et al. Totally laparoscopic pylorus-preserving gastrectomy for early gastric cancer in the middle stomach: technical report and surgical outcomes. Gastric Cancer. 2015; 18:183–187.

37. Shibata C, Shiiba KI, Funayama Y, Ishii S, Fukushima K, Mizoi T, et al. Outcomes after pylorus-preserving gastrectomy for early gastric cancer: a prospective multicenter trial. World J Surg. 2004; 28:857–861.

38. Jiang X, Hiki N, Nunobe S, Fukunaga T, Kumagai K, Nohara K, et al. Postoperative outcomes and complications after laparoscopy-assisted pylorus-preserving gastrectomy for early gastric cancer. Ann Surg. 2011; 253:928–933.

39. 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; 240:205–213.

40. Sasako M, McCulloch P, Kinoshita T, Maruyama K. New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg. 1995; 82:346–351.

41. Kodera Y, Yamamura Y, Kanemitsu Y, Shimizu Y, Hirai T, Yasui K, et al. Lymph node metastasis in cancer of the middle-third stomach: criteria for treatment with a pylorus-preserving gastrectomy. Surg Today. 2001; 31:196–203.

42. Hiki N, Nunobe S, Kubota T, Jiang X. Function-preserving gastrectomy for early gastric cancer. Ann Surg Oncol. 2013; 20:2683–2692.

43. Yoo MW, Park DJ, Ahn HS, Jeong SH, Lee HJ, Kim WH, et al. Evaluation of the adequacy of lymph node dissection in pylorus-preserving gastrectomy for early gastric cancer using the maruyama index. World J Surg. 2010; 34:291–295.

44. Hiki N, Sano T, Fukunaga T, Ohyama S, Tokunaga M, Yamaguchi T. Survival benefit of pylorus-preserving gastrectomy in early gastric cancer. J Am Coll Surg. 2009; 209:297–301.

45. Xiao XM, Gaol C, Yin W, Yu WH, Qi F, Liu T. Pylorus-preserving versus distal subtotal gastrectomy for surgical treatment of early gastric cancer: a meta-analysis. Hepatogastroenterology. 2014; 61:870–879.

46. Isozaki H, Okajima K, Momura E, Ichinona T, Fujii K, Izumi N, et al. Postoperative evaluation of pylorus-preserving gastrectomy for early gastric cancer. Br J Surg. 1996; 83:266–269.

47. Mine S, Sano T, Tsutsumi K, Murakami Y, Ehara K, Saka M, et al. Large-scale investigation into dumping syndrome after gastrectomy for gastric cancer. J Am Coll Surg. 2010; 211:628–636.

48. Fujita J, Takahashi M, Urushihara T, Tanabe K, Kodera Y, Yumiba T, et al. Assessment of postoperative quality of life following pylorus-preserving gastrectomy and Billroth-I distal gastrectomy in gastric cancer patients: results of the nationwide postgastrectomy syndrome assessment study. Gastric Cancer. 2016; 19:302–311.

49. Song P, Lu M, Pu F, Zhang D, Wang B, Zhao Q. Meta-analysis of pylorus-preserving gastrectomy for middle-third early gastric cancer. J Laparoendosc Adv Surg Tech A. 2014; 24:718–727.

50. Fujita T. Outcome of pylorus-preserving gastrectomy for early gastric cancer (Br J Surg 2008;95:1131-1135). Br J Surg. 2008; 95:1429. author reply 1429-1430.

51. Bae JS, Kim SH, Shin CI, Joo I, Yoon JH, Lee HJ, 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.

52. Han DS, Suh YS, Ahn HS, Kong SH, Lee HJ, Kim WH, et al. Comparison of surgical outcomes of robot-assisted and laparoscopy-assisted pylorus-preserving gastrectomy for gastric cancer: a propensity score matching analysis. Ann Surg Oncol. 2015; 22:2323–2328.

53. Kim HI, Han SU, Yang HK, Kim YW, Lee HJ, Ryu KW, et al. Multicenter Prospective Comparative Study of Robotic Versus Laparoscopic Gastrectomy for Gastric Adenocarcinoma. Ann Surg. 2016; 263:103–109.