Nutritional safety of oncometabolic surgery for early gastric cancer patients: a prospective single-arm pilot study using a historical control group for comparison

  • Young Suk Park
  • Do Joong ParkEmail author
  • Ki Hyun Kim
  • Dong Jin Park
  • Yoontaek Lee
  • Ki Bum Park
  • Sa-Hong Min
  • Sang-Hoon Ahn
  • Hyung-Ho Kim



Oncometabolic surgery (OS) is a modification of the Roux-en Y reconstruction method, in which the lengths of the biliopancreatic and Roux limbs are longer than that with conventional surgery (CS). Although OS is performed to improve postoperative glycemic control in gastric cancer patients with type 2 diabetes mellitus (T2DM), its postoperative nutritional safety has not been clarified. This prospective pilot study evaluated the safety and feasibility of OS in early gastric cancer patients.


This study evaluated 20 patients with clinical T1N0 stage and preoperative body mass index (BMI) ≥ 32.5 kg/m2, or ≥ 27.5 kg/m2 with comorbidities, who underwent OS. Primary outcomes were cumulative incidences of anemia and deficiencies in iron and vitamin B12 after 1 year. The outcomes were compared to those of a matched historical control group.


The cumulative incidences of anemia (15.0% vs. 10.0%, P = 0.99), iron deficiency (15.0% vs. 10.0%, P = 0.99), and vitamin B12 deficiency (10.0% vs. 0%, P = 0.47) did not differ significantly in the OS and CS groups. However, median vitamin B12 concentration tended to be lower (395.8 vs. 493.7 pg/mL, P = 0.06) and reductions in vitamin B12 concentration tended to be greater (174.7 vs. 123.0 pg/mL, P = 0.07) in the OS group. BMI loss was similar in the two groups (2.9 vs. 2.8 kg/m2, P = 0.80). Remission rates of hypertension (68.8% vs. 41.2%, P = 0.22) and T2DM (77.8% vs. 50.0%, P = 0.58) were higher in the OS group.


Nutritional parameters did not differ significantly in the OS and CS groups. Vitamin B12 levels should be carefully monitored after OS.


Stomach neoplasm Nutritional status Obesity Metabolic syndrome Reconstructive surgical procedures 



The authors thank the Medical Research Collaborating Center at Seoul National University Bundang Hospital.


Young Suk Park, Do Joong Park, Ki Hyun Kim, Dong Jin Park, Yoontaek Lee, Ki Bum Park, Sa-Hong Min, Sang-Hoon Ahn, and Hyung-Ho Kim have no conflicts of interest. This study was supported by a grant from Seoul National University Bundang Hospital (Grant No. 14-2015-028).


  1. 1.
    Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, Navaneethan SD, Singh RP, Pothier CE, Nissen SE, Kashyap SR, Investigators S (2017) Bariatric surgery versus intensive medical therapy for diabetes—5-year outcomes. N Engl J Med 376:641–651CrossRefGoogle Scholar
  2. 2.
    Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Brethauer SA, Navaneethan SD, Aminian A, Pothier CE, Kim ES, Nissen SE, Kashyap SR, Investigators S (2014) Bariatric surgery versus intensive medical therapy for diabetes–3-year outcomes. N Engl J Med 370:2002–2013CrossRefGoogle Scholar
  3. 3.
    Jimenez A, Casamitjana R, Flores L, Viaplana J, Corcelles R, Lacy A, Vidal J (2012) Long-term effects of sleeve gastrectomy and Roux-en-Y gastric bypass surgery on type 2 diabetes mellitus in morbidly obese subjects. Ann Surg 256:1023–1029CrossRefGoogle Scholar
  4. 4.
    Sjostrom L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden A, Bouchard C, Carlsson B, Karason K, Lonroth H, Naslund I, Sjostrom E, Taube M, Wedel H, Svensson PA, Sjoholm K, Carlsson LM (2014) Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA, J Am Med Assoc 311:2297–2304CrossRefGoogle Scholar
  5. 5.
    Lee TH, Lee CM, Park S, Jung DH, Jang YJ, Kim JH, Park SH, Mok YJ (2017) Long-term follow-up for type 2 diabetes mellitus after gastrectomy in non-morbidly obese patients with gastric cancer: the legitimacy of onco-metabolic surgery. J Gastric Cancer 17:283–294CrossRefGoogle Scholar
  6. 6.
    Zhu Z, Shan X, Cheng Y, Xu J, Fu H, Wang W, Yan R, Cai Q (2015) Clinical course of diabetes after gastrectomy according to type of reconstruction in patients with concurrent gastric cancer and type 2 diabetes. Obes Surg 25:673–679CrossRefGoogle Scholar
  7. 7.
    Lee W, Ahn SH, Lee JH, Park do J, Lee HJ, Kim HH, Yang HK (2012) Comparative study of diabetes mellitus resolution according to reconstruction type after gastrectomy in gastric cancer patients with diabetes mellitus. Obes Surg 22:1238–1243CrossRefGoogle Scholar
  8. 8.
    Kim JW, Cheong JH, Hyung WJ, Choi SH, Noh SH (2012) Outcome after gastrectomy in gastric cancer patients with type 2 diabetes. World J Gastroenterol: WJG 18:49–54CrossRefGoogle Scholar
  9. 9.
    Lee WJ, Hur KY, Lakadawala M, Kasama K, Wong SK, Chen SC, Lee YC, Ser KH (2013) Predicting success of metabolic surgery: age, body mass index, C-peptide, and duration score. Surg Obesity Rel Dis 9:379–384CrossRefGoogle Scholar
  10. 10.
    Liu T, Xie GW, Tian QZ, Li J (2015) Radical gastrectomy combined with modified gastric bypass surgery for gastric cancer patients with type 2 diabetes. Cell Biochem Biophys 72:839–844CrossRefGoogle Scholar
  11. 11.
    Kim JW, Kim KY, Lee SC, Yang DH, Kim BC (2015) The effect of long Roux-en-Y gastrojejunostomy in gastric cancer patients with type 2 diabetes and body mass index < 35 kg/m(2): preliminary results. Ann Surg Treat Res 88:215–221CrossRefGoogle Scholar
  12. 12.
    Kim WS, Kim JW, Ahn CW, Choi SH (2013) Resolution of type 2 diabetes after gastrectomy for gastric cancer with long limb Roux-en Y reconstruction: a prospective pilot study. J Korean Surg Soc 84:88–93CrossRefGoogle Scholar
  13. 13.
    Aoyama T, Sato T, Maezawa Y, Kano K, Hayashi T, Yamada T, Yukawa N, Oshima T, Rino Y, Masuda M, Ogata T, Cho H, Yoshikawa T (2017) Postoperative weight loss leads to poor survival through poor S-1 efficacy in patients with stage II/III gastric cancer. Int J Clin Oncol 22:476–483CrossRefGoogle Scholar
  14. 14.
    Caillet P, Liuu E, Raynaud Simon A, Bonnefoy M, Guerin O, Berrut G, Lesourd B, Jeandel C, Ferry M, Rolland Y, Paillaud E (2017) Association between cachexia, chemotherapy and outcomes in older cancer patients: a systematic review. Clin Nutr 36:1473–1482CrossRefGoogle Scholar
  15. 15.
    Park YS, Park DJ, Lee Y, Park KB, Min SH, Ahn SH, Kim HH (2018) Prognostic roles of perioperative body mass index and weight loss in the long-term survival of gastric cancer patients. Cancer Epidemiol Biomark Prev 27:955–962CrossRefGoogle Scholar
  16. 16.
    Washington K (2010) 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol 17:3077–3079CrossRefGoogle Scholar
  17. 17.
    Nakajima T (2002) Gastric cancer treatment guidelines in Japan. Gastric Cancer 5:1–5CrossRefGoogle Scholar
  18. 18.
    Association JGC (2016) Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 20(1):1–19CrossRefGoogle Scholar
  19. 19.
    Park YS, Shin DJ, Son SY, Kim KH, Park DJ, Ahn SH, Park DJ, Kim HH (2018) Roux stasis syndrome and gastric food stasis after laparoscopic distal gastrectomy with uncut roux-en-Y reconstruction in gastric cancer patients: a propensity score matching analysis. World J Surg 42(12):4022–4032CrossRefGoogle Scholar
  20. 20.
    Alberti KGMM, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. The Lancet 366:1059–1062CrossRefGoogle Scholar
  21. 21.
    Association AD (2016) Standards of medical care in diabetes—2016 abridged for primary care providers. Clin Diabetes 34:3CrossRefGoogle Scholar
  22. 22.
    Van Belle G (2011) Statistical rules of thumb. Wiley, HobokenGoogle Scholar
  23. 23.
    Ahn SH, Son SY, Lee CM, Jung DH, Park do J, Kim HH (2014) Intracorporeal uncut Roux-en-Y gastrojejunostomy reconstruction in pure single-incision laparoscopic distal gastrectomy for early gastric cancer: unaided stapling closure. J Am Coll Surg 218:e17–21CrossRefGoogle Scholar
  24. 24.
    Nakamura M, Nakamori M, Ojima T, Iwahashi M, Horiuchi T, Kobayashi Y, Yamade N, Shimada K, Oka M, Yamaue H (2016) Randomized clinical trial comparing long-term quality of life for Billroth I versus Roux-en-Y reconstruction after distal gastrectomy for gastric cancer. Br J Surg 103:337–347CrossRefGoogle Scholar
  25. 25.
    Murad AJ Jr, Cohen RV, de Godoy EP, Scheibe CL, Campelo GP, Ramos AC, de Lima RC, Pinto LEV, Coelho D, Costa HBF, Pinto IMP, Pereira T, Teofilo FRS, Valadao JA (2018) A prospective single-arm trial of modified long biliopancreatic and short alimentary limbs roux-en-Y gastric bypass in type 2 diabetes patients with mild obesity. Obes Surg 28:599–605CrossRefGoogle Scholar
  26. 26.
    Nora M, Morais T, Almeida R, Guimaraes M, Monteiro MP (2017) Should Roux-en-Y gastric bypass biliopancreatic limb length be tailored to achieve improved diabetes outcomes? Medicine 96:e8859CrossRefGoogle Scholar
  27. 27.
    Miyachi T, Nagao M, Shibata C, Kitahara Y, Tanaka N, Watanabe K, Tsuchiya T, Motoi F, Naitoh T, Unno M (2016) Biliopancreatic limb plays an important role in metabolic improvement after duodenal-jejunal bypass in a rat model of diabetes. Surgery 159:1360–1371CrossRefGoogle Scholar
  28. 28.
    Allen RH, Seetharam B, Podell E, Alpers DH (1978) Effect of proteolytic enzymes on the binding of cobalamin to R protein and intrinsic factor. In vitro evidence that a failure to partially degrade R protein is responsible for cobalamin malabsorption in pancreatic insufficiency. J Clin Invest 61:47–54CrossRefGoogle Scholar
  29. 29.
    Herbert V (1988) Vitamin B-12: plant sources, requirements, and assay. Am J Clin Nutr 48:852–858CrossRefGoogle Scholar
  30. 30.
    Brolin RE, Mendelow H, Ravitch MM (1980) The manifestations of bypass enteritis following jejunoileal bypass. Surg Gynecol Obstet 151:209–214Google Scholar
  31. 31.
    Passaro E Jr, Drenick E, Wilson SE (1976) Bypass enteritis. A new complication of jejunoileal bypass for obesity. Am J Surg 131:169–174CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of SurgerySeoul National University Bundang HospitalSeongnam-SiRepublic of Korea
  2. 2.Department of SurgerySeoul National University College of MedicineSeoulRepublic of Korea

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