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http://dx.doi.org/10.5230/jgc.2021.21.e3

Pancreatic Fistula after D1+/D2 Radical Gastrectomy according to the Updated International Study Group of Pancreatic Surgery Criteria: Risk Factors and Clinical Consequences. Experience of Surgeons with High Caseloads in a Single Surgical Center in Eastern Europe  

Martiniuc, Alexandru (Department of General Surgery, Fundeni Clinical Institute)
Dumitrascu, Traian (Department of General Surgery, Fundeni Clinical Institute)
Ionescu, Mihnea (Department of General Surgery, Fundeni Clinical Institute)
Tudor, Stefan (Department of General Surgery, Fundeni Clinical Institute)
Lacatus, Monica (Department of General Surgery, Fundeni Clinical Institute)
Herlea, Vlad (Department of Pathology, Fundeni Clinical Institute)
Vasilescu, Catalin (Department of General Surgery, Fundeni Clinical Institute)
Publication Information
Journal of Gastric Cancer / v.21, no.1, 2021 , pp. 16-29 More about this Journal
Abstract
Purpose: Incidence, risk factors, and clinical consequences of pancreatic fistula (POPF) after D1+/D2 radical gastrectomy have not been well investigated in Western patients, particularly those from Eastern Europe. Materials and Methods: A total of 358 D1+/D2 radical gastrectomies were performed by surgeons with high caseloads in a single surgical center from 2002 to 2017. A retrospective analysis of data that were prospectively gathered in an electronic database was performed. POPF was defined and graded according to the International Study Group for Pancreatic Surgery (ISGPS) criteria. Uni- and multivariate analyses were performed to identify potential predictors of POPF. Additionally, the impact of POPF on early complications and long-term outcomes were investigated. Results: POPF was observed in 20 patients (5.6%), according to the updated ISGPS grading system. Cardiovascular comorbidities emerged as the single independent predictor of POPF formation (risk ratio, 3.051; 95% confidence interval, 1.161-8.019; P=0.024). POPF occurrence was associated with statistically significant increased rates of postoperative hemorrhage requiring re-laparotomy (P=0.029), anastomotic leak (P=0.002), 90-day mortality (P=0.036), and prolonged hospital stay (P<0.001). The long-term survival of patients with gastric adenocarcinoma was not affected by POPF (P=0.661). Conclusions: In this large series of Eastern European patients, the clinically relevant rate of POPF after D1+/D2 radical gastrectomy was low. The presence of co-existing cardiovascular disease favored the occurrence of POPF and was associated with an increased risk of postoperative bleeding, anastomotic leak, 90-day mortality, and prolonged hospital stay. POPF was not found to affect the long-term survival of patients with gastric adenocarcinoma.
Keywords
Radical gastrectomy; Gastric cancer; Pancreatic fistula; Complications; Survival;
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1 Galizia G, Lieto E, De Vita F, Castellano P, Ferraraccio F, Zamboli A, et al. Modified versus standard D2 lymphadenectomy in total gastrectomy for nonjunctional gastric carcinoma with lymph node metastasis. Surgery 2015;157:285-296.   DOI
2 Kang JH, Ryu SY, Jung MR, Jeong O. Comparison of long term survival outcomes between D1+ and D2 lymph node dissection for ≥ pT2 or pN+ gastric carcinoma: a large scale case-control study using propensity score matching. Eur J Surg Oncol 2020;46:1239-1246.   DOI
3 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.   DOI
4 Etoh T, Honda M, Kumamaru H, Miyata H, Yoshida K, Kodera Y, et al. Morbidity and mortality from a propensity score-matched, prospective cohort study of laparoscopic versus open total gastrectomy for gastric cancer: data from a nationwide web-based database. Surg Endosc 2018;32:2766-2773.   DOI
5 Jeong SH, Ahn HS, Yoo MW, Cho JJ, Lee HJ, Kim HH, et al. Increased morbidity rates in patients with heart disease or chronic liver disease following radical gastric surgery. J Surg Oncol 2010;101:200-204.   DOI
6 Jin LX, Sanford DE, Squires MH 3rd, Moses LE, Yan Y, Poultsides GA, et al. Interaction of postoperative morbidity and receipt of adjuvant therapy on long-term survival after resection for gastric adenocarcinoma: results from the U.S. gastric cancer collaborative. Ann Surg Oncol 2016;23:2398-2408.   DOI
7 Pasquer A, Renaud F, Hec F, Gandon A, Vanderbeken M, Drubay V, et al. Is centralization needed for esophageal and gastric cancer patients with low operative risk?: a nationwide study. Ann Surg 2016;264:823-830.   DOI
8 Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 2005;138:8-13.   DOI
9 Guerra F, Giuliani G, Formisano G, Bianchi PP, Patriti A, Coratti A. Pancreatic complications after conventional laparoscopic radical gastrectomy versus robotic radical gastrectomy: systematic review and meta-analysis. J Laparoendosc Adv Surg Tech A 2018;28:1207-1215.   DOI
10 Obama K, Okabe H, Hosogi H, Tanaka E, Itami A, Sakai Y. Feasibility of laparoscopic gastrectomy with radical lymph node dissection for gastric cancer: from a viewpoint of pancreas-related complications. Surgery 2011;149:15-21.   DOI
11 Kurokawa Y, Doki Y, Mizusawa J, Terashima M, Katai H, Yoshikawa T, et al. Bursectomy versus omentectomy alone for resectable gastric cancer (JCOG1001): a phase 3, open-label, randomised controlled trial. Lancet Gastroenterol Hepatol 2018;3:460-468.   DOI
12 Li Z, Lian B, Chen J, Song D, Zhao Q. Systematic review and meta-analysis of splenectomy in gastrectomy for gastric carcinoma. Int J Surg 2019;68:104-113.   DOI
13 Procopiuc L, Tudor S, Manuc M, Diculescu M, Vasilescu C. Open vs robotic radical gastrectomy for locally advanced gastric cancer. Int J Med Robot 2016;12:502-508.   DOI
14 Tsujiura M, Hiki N, Ohashi M, Nunobe S, Kumagai K, Ida S, et al. "Pancreas-compressionless gastrectomy": a novel laparoscopic approach for suprapancreatic lymph node dissection. Ann Surg Oncol 2017;24:3331-3337.   DOI
15 Papenfuss WA, Kukar M, Oxenberg J, Attwood K, Nurkin S, Malhotra U, et al. Morbidity and mortality associated with gastrectomy for gastric cancer. Ann Surg Oncol 2014;21:3008-3014.   DOI
16 Climent M, Hidalgo N, Vidal Ó, Puig S, Iglesias M, Cuatrecasas M, et al. Postoperative complications do not impact on recurrence and survival after curative resection of gastric cancer. Eur J Surg Oncol 2016;42:132-139.   DOI
17 Ojima T, Nakamura M, Nakamori M, Hayata K, Katsuda M, Maruoka S, et al. Robotic radical lymphadenectomy without touching the pancreas during gastrectomy for gastric cancer. Medicine (Baltimore) 2019;98:e15091.   DOI
18 Smits FJ, Verweij ME, Daamen LA, van Werkhoven CH, Goense L, Besselink MG, et al. Impact of complications after pancreatoduodenectomy on mortality, organ failure, hospital stay, and readmission: analysis of a nationwide audit. Ann Surg. Forthcoming 2020.
19 Yekebas EF, Wolfram L, Cataldegirmen G, Habermann CR, Bogoevski D, Koenig AM, et al. Postpancreatectomy hemorrhage: diagnosis and treatment: an analysis in 1669 consecutive pancreatic resections. Ann Surg 2007;246:269-280.   DOI
20 Kubota T, Hiki N, Sano T, Nomura S, Nunobe S, Kumagai K, et al. Prognostic significance of complications after curative surgery for gastric cancer. Ann Surg Oncol 2014;21:891-898.   DOI
21 Ferlay J, Colombet M, Soerjomataram I, Dyba T, Randi G, Bettio M, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer 2018;103:356-387.   DOI
22 Arnold M, Abnet CC, Neale RE, Vignat J, Giovannucci EL, McGlynn KA, et al. Global burden of 5 major types of gastrointestinal cancer. Gastroenterology 2020;159:335-349.e15.   DOI
23 Colquhoun A, Arnold M, Ferlay J, Goodman KJ, Forman D, Soerjomataram I. Global patterns of cardia and non-cardia gastric cancer incidence in 2012. Gut 2015;64:1881-1888.   DOI
24 Arnold M, Park JY, Camargo MC, Lunet N, Forman D, Soerjomataram I. Is gastric cancer becoming a rare disease? A global assessment of predicted incidence trends to 2035. Gut 2020;69:823-829.   DOI
25 Eom BW, Kim YW, Nam BH, Ryu KW, Jeong HY, Park YK, et al. The Korean Gastric Cancer Cohort Study: study protocol and brief results of a large-scale prospective cohort study. J Gastric Cancer 2016;16:182-190.   DOI
26 Hiki N, Honda M, Etoh T, Yoshida K, Kodera Y, Kakeji Y, et al. Higher incidence of pancreatic fistula in laparoscopic gastrectomy. Real-world evidence from a nationwide prospective cohort study. Gastric Cancer 2018;21:162-170.   DOI
27 Ito Y, Miyashiro I, Ishikawa T, Akazawa K, Fukui K, Katai H, et al. Determinant factors on differences in survival for gastric cancer between the US and Japan using nationwide databases. J Epidemiol 2020;
28 Kobayashi D, Iwata N, Tanaka C, Kanda M, Yamada S, Nakayama G, et al. Factors related to occurrence and aggravation of pancreatic fistula after radical gastrectomy for gastric cancer. J Surg Oncol 2015;112:381-386.   DOI
29 Bonenkamp JJ, Hermans J, Sasako M, van de Velde CJ, Welvaart K, Songun I, et al. Extended lymph-node dissection for gastric cancer. N Engl J Med 1999;340:908-914.   DOI
30 Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, et al. Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Surgical Cooperative Group. Br J Cancer 1999;79:1522-1530.   DOI
31 Degiuli M, Sasako M, Ponti A, Vendrame A, Tomatis M, Mazza C, et al. Randomized clinical trial comparing survival after D1 or D2 gastrectomy for gastric cancer. Br J Surg 2014;101:23-31.   DOI
32 Vasilescu C, Herlea V, Tidor S, Ivanov B, Stanciulea O, Manuc M, et al. D2 lymph node dissection in gastric cancer surgery: long term results--analysis of an experience with 227 patients. Chirurgia (Bucur) 2006;101:375-384.
33 Boscaiu MD, Dragomir M, Trandafir B, Herlea V, Vasilescu C. Should surgical ex vivo lymphadenectomy be a standard procedure in the management of patients with gastric cancer? Eur Surg 2018;50:169-176.   DOI
34 Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 2017;20:1-19.   DOI
35 Sano T, Sasako M, Yamamoto S, Nashimoto A, Kurita A, Hiratsuka M, et al. Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy--Japan Clinical Oncology Group study 9501. J Clin Oncol 2004;22:2767-2773.   DOI
36 Bonenkamp JJ, Songun I, Hermans J, Sasako M, Welvaart K, Plukker JT, et al. Randomised comparison of morbidity after D1 and D2 dissection for gastric cancer in 996 Dutch patients. Lancet 1995;345:745-748.   DOI
37 Cuschieri A, Fayers P, Fielding J, Craven J, Bancewicz J, Joypaul V, et al. Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomised controlled surgical trial. The Surgical Cooperative Group. Lancet 1996;347:995-999.   DOI
38 Tudor S, Dumitrascu T, Manuc M, Trandafir B, Ionescu M, Popescu I, et al. D2 lymphadenectomy for gastric adenocarcinoma: long-term results and the impact of surgeon experience on the survival rates. Chirurgia (Bucur) 2018;113:772-779.   DOI
39 Randle RW, Swords DS, Levine EA, Fino NF, Squires MH, Poultsides G, et al. Optimal extent of lymphadenectomy for gastric adenocarcinoma: a 7-institution study of the U.S. gastric cancer collaborative. J Surg Oncol 2016;113:750-755.   DOI
40 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;11:439-449.   DOI
41 Degiuli M, Sasako M, Calgaro M, Garino M, Rebecchi F, Mineccia M, et al. Morbidity and mortality after D1 and D2 gastrectomy for cancer: interim analysis of the Italian Gastric Cancer Study Group (IGCSG) randomised surgical trial. Eur J Surg Oncol 2004;30:303-308.   DOI
42 El-Sedfy A, Dixon M, Seevaratnam R, Bocicariu A, Cardoso R, Mahar A, et al. Personalized surgery for gastric adenocarcinoma: a meta-analysis of D1 versus D2 lymphadenectomy. Ann Surg Oncol 2015;22:1820-1827.   DOI
43 Karavokyros I, Michalinos A. Favoring D2-lymphadenectomy in gastric cancer. Front Surg 2018;5:42.   DOI
44 Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D, et al. Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2016;27:v38-v49.   DOI
45 Guerra F, Giuliani G, Iacobone M, Bianchi PP, Coratti A. Pancreas-related complications following gastrectomy: systematic review and meta-analysis of open versus minimally invasive surgery. Surg Endosc 2017;31:4346-4356.   DOI
46 Kamiya S, Hiki N, Kumagai K, Honda M, Nunobe S, Ohashi M, et al. Two-point measurement of amylase in drainage fluid predicts severe postoperative pancreatic fistula after gastric cancer surgery. Gastric Cancer 2018;21:871-878.   DOI
47 Herbella FA, Tineli AC, Wilson JL Jr, Del Grande JC. Gastrectomy and lymphadenectomy for gastric cancer: is the pancreas safe? J Gastrointest Surg 2008;12:1912-1914.   DOI
48 Imamura H, Kurokawa Y, Kawada J, Tsujinaka T, Takiguchi S, Fujiwara Y, et al. Influence of bursectomy on operative morbidity and mortality after radical gastrectomy for gastric cancer: results of a randomized controlled trial. World J Surg 2011;35:625-630.   DOI
49 Jiang X, Hiki N, Nunobe S, Kumagai K, Nohara K, Sano T, et al. Postoperative pancreatic fistula and the risk factors of laparoscopy-assisted distal gastrectomy for early gastric cancer. Ann Surg Oncol 2012;19:115-121.   DOI
50 Katai H, Yoshimura K, Fukagawa T, Sano T, Sasako M. Risk factors for pancreas-related abscess after total gastrectomy. Gastric Cancer 2005;8:137-141.   DOI
51 Kobayashi N, Shinohara H, Haruta S, Ohkura Y, Mizuno A, Ueno M, et al. Process of pancreas head as a risk factor for postoperative pancreatic fistula in laparoscopic gastric cancer surgery. World J Surg 2016;40:2194-2201.   DOI
52 Komatsu S, Ichikawa D, Kashimoto K, Kubota T, Okamoto K, Konishi H, et al. Risk factors to predict severe postoperative pancreatic fistula following gastrectomy for gastric cancer. World J Gastroenterol 2013;19:8696-8702.   DOI
53 Kosaka T, Akiyama H, Makino H, Kimura J, Takagawa R, Ono HA, et al. Impact of neoadjuvant chemotherapy among patients with pancreatic fistula after gastrectomy for advanced gastric cancer. Anticancer Res 2016;36:1773-1777.
54 Migita K, Matsumoto S, Wakatsuki K, Ito M, Kunishige T, Nakade H, et al. The anatomical location of the pancreas is associated with the incidence of pancreatic fistula after laparoscopic gastrectomy. Surg Endosc 2016;30:5481-5489.   DOI
55 Kumagai K, Hiki N, Nunobe S, Kamiya S, Tsujiura M, Ida S, et al. Impact of anatomical position of the pancreas on postoperative complications and drain amylase concentrations after laparoscopic distal gastrectomy for gastric cancer. Surg Endosc 2018;32:3846-3854.   DOI
56 Kung CH, Lindblad M, Nilsson M, Rouvelas I, Kumagai K, Lundell L, et al. Postoperative pancreatic fistula formation according to ISGPF criteria after D2 gastrectomy in Western patients. Gastric Cancer 2014;17:571-577.   DOI
57 Kunisaki C, Shimada H, Ono H, Otsuka Y, Matsuda G, Nomura M, et al. Predictive factors for pancreatic fistula after pancreaticosplenectomy for advanced gastric cancer in the upper third of the stomach. J Gastrointest Surg 2006;10:132-137.   DOI
58 Miki Y, Tokunaga M, Bando E, Tanizawa Y, Kawamura T, Terashima M. Evaluation of postoperative pancreatic fistula after total gastrectomy with D2 lymphadenectomy by ISGPF classification. J Gastrointest Surg 2011;15:1969-1976.   DOI
59 Miyai H, Hara M, Hayakawa T, Takeyama H. Establishment of a simple predictive scoring system for pancreatic fistula after laparoscopy-assisted gastrectomy. Dig Endosc 2013;25:585-592.   DOI
60 Nobuoka D, Gotohda N, Konishi M, Nakagohri T, Takahashi S, Kinoshita T. Prevention of postoperative pancreatic fistula after total gastrectomy. World J Surg 2008;32:2261-2266.   DOI
61 Sato Y, Inokuchi M, Otsuki S, Fujimori Y, Kojima K. Risk factor of pancreatic fistula after radical gastrectomy from the viewpoint of fatty pancreas. Dig Surg 2017;34:455-461.   DOI
62 Tanioka T, Kojima K, Saito T, Kanemoto E, Okuno K, Gokita K, et al. Intraoperative body fluid amylase as a novel indicator of postgastrectomy pancreatic fistula. World J Surg 2019;43:2061-2068.   DOI
63 Seo HS, Shim JH, Jeon HM, Park CH, Song KY. Postoperative pancreatic fistula after robot distal gastrectomy. J Surg Res 2015;194:361-366.   DOI
64 Tanaka K, Miyashiro I, Yano M, Kishi K, Motoori M, Seki Y, et al. Accumulation of excess visceral fat is a risk factor for pancreatic fistula formation after total gastrectomy. Ann Surg Oncol 2009;16:1520-1525.   DOI
65 Taniguchi Y, Kurokawa Y, Mikami J, Tanaka K, Miyazaki Y, Makino T, et al. Amylase concentration in drainage fluid as a predictive factor for severe postoperative pancreatic fistula in patients with gastric cancer. Surg Today 2017;47:1378-1383.   DOI
66 Wakahara T, Kanemitsu K, Asari S, Tsuchida S, Ueno N, Toyokawa A, et al. The combined use of drainage amylase concentration and serum C-reactive protein as predictors of pancreas-related complications after elective gastrectomy. Oncology 2020;98:111-116.   DOI
67 Yamada S, Yagi S, Sato K, Shin'e M, Sakamoto A, Utsunomiya D, et al. Serum C-reactive protein level on first postoperative day can predict occurrence of postoperative pancreatic fistula after laparoscopic gastrectomy. J Med Invest 2019;66:285-288.   DOI
68 Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M, et al. The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 2017;161:584-591.   DOI
69 Yu HW, Jung DH, Son SY, Lee CM, Lee JH, Ahn SH, et al. Risk factors of postoperative pancreatic fistula in curative gastric cancer surgery. J Gastric Cancer 2013;13:179-184.   DOI