Risk factors for the development of pancreatic fistula after pancreaticoduodenectomy
https://doi.org/10.16931/1995-5464.2024-4-144-150
Abstract
Pancreatic fistula refers to the most common and serious complication following pancreaticoduodenectomy. Various prognostic scoring systems have been developed and validated to reduce the risk of postoperative pancreatic fistula. These prognostic scores are based on preoperative data and intraoperative assessments of gland density, pancreatic duct diameter, and other parameters. The most frequently used and widely recognized prognostic scores include FRS, a-FRS, and ua-FRS. Evolution in instrumental methods of diagnosis, development of artificial intelligence, and accumulation of experience in managing patients with periampullary malignancies shift the focus towards preoperative evaluation based on CT data.
About the Authors
A. N. AtaevaRussian Federation
Aida N. Ataeva – Postgraduate Student, Department of Faculty Surgery No. 1, Pirogov Russian National Research Medical University.
1, Ostrovityanova str., Moscow, 117513
A. F. Mamedov
Russian Federation
Aslan F. Mamedov – Clinical Resident, Oncology Unit No. 2, Kommunarka Moscow City Clinical Center of Moscow Healthcare Department.
8, Sosenskij stan str., Moscow, 108814
A. O. Kurskov
Russian Federation
Anton O. Kurskov – Oncologist of Oncology Unit No. 2, Kommunarka Moscow City Clinical Center of Moscow Healthcare Department.
8, Sosenskij stan str., Moscow, 108814
M. V. Kozodaeva
Russian Federation
Margarita V. Kozodaeva – Cand. of Sci. (Med.), Oncologist, Kommunarka Moscow City Clinical Center of Moscow Healthcare Department.
8, Sosenskij stan str., Moscow, 108814
K. D Dalgatov
Russian Federation
Kamil' D. Dalgatov – Cand. of Sci. (Med.), Head of Oncology Unit No. 2, Kommunarka Moscow City Clinical Center of Moscow Healthcare Department.
8, Sosenskij stan str., Moscow, 108814
A. V. Sazhin
Russian Federation
Aleksandr V. Sazhin – Doct. of Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences, Head of the Department of Faculty Surgery No. 1, Pirogov Russian National Research Medical University.
1, Ostrovityanova str., Moscow, 117513
References
1. Nitsche U., Wenzel P., Siveke J.T., Braren R., Holzapfel K., Schlitter A.M., Stöß C., Kong B., Esposito I., Erkan M., Michalski C.W., Friess H., Kleeff J. Resectability after first-line FOLFIRINOX in initially unresectable locally advanced pancreatic cancer: a single-center experience. Ann. Surg. Oncol. 2015; 22 (3): 1212–1220. https://doi.org/10.1245/s10434-015-4851-2
2. Callery M.P., Chang K.J., Fishman E.K., Talamonti M.S., Traverso L.V., Linehan D.C. Pretreatment assessment of resectable and borderline resectable pancreatic cancer: еxpert consensus statement. Ann. Surg. Oncol. 2009; 16 (7): 1727–1733. https://doi.org/10.1245/s10434-009-0408-6
3. Petrelli F., Coinu A., Borgonovo K., Cabiddu M., Ghilardi M., Lonati V., Aitini V., Barni S. FOLFIRINOX-based neoadjuvant therapy in borderline resectable or unresectable pancreatic cancer: a meta-analytical review of published studies. Pancreas. 2015; 44 (4): 515–521. https://doi.org/10.1097/MPA.0000000000000314
4. Bassi C., Marchegiani G., Dervenis C. et al.; International Study Group on Pancreatic Surgery (ISGPS). The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery. 2017; 161 (3): 584–591. https://doi.org/10.1016/j.surg.2016.11.014
5. Nahm C.B., Connor S.J., Samra J.S., Mittal A. Postoperative pancreatic fistula: a review of traditional and emerging concepts. Clin. Exp. Gastroenterol. 2018; 15 (11): 105–118. https://doi.org/10.2147/CEG.S120217
6. Keck T., Wellner U.F., Bahra M., Klein F., Sick O., Niedergethmann M., Wilhelm T.J., Farkas S.A., Börner T., Bruns C., Kleespies A., Kleeff J., Mihaljevic A.L., Uhl W., Chromik A., Fendrich V., Heeger K., Padberg W., Hecker A., Neumann U.P., Junge K., Kalff J.C., Glowka T.R., Werner J., Knebel P., Piso P., Mayr M., Izbicki J., Vashist Y., Bronsert P., Bruckner T., Limprecht R., Diener M.K., Rossion I., Wegener I., Hopt U.T. Pancreatogastrostomy versus pancreatojejunostomy for RECOnstruction after PANCreatoduodenectomy (RECOPANC, DRKS 00000767): perioperative and long-term results of a multicenter randomized controlled trial. Ann. Surg. 2017; 263 (3): 440–449. https://doi.org/10.1097/SLA.0000000000001240
7. Shrikhande S.V., Sivasanker M., Vollmer S.M., Friess H., Besselink M.G., Fingerhut A., Yeo C.J., Fernandez-Del Castillo C., Dervenis C., Halloran C., Gouma D.J., Radenkovic D., Asbun H.J., Neoptolemos J.P., Izbicki J.R., Lillemoe K.D., Conlon K.C., Fernandez-Cruz L., Montorsi M., Bockhorn M., Adham M., Charnley R., Carter R., Hackert T., Hartwig W., Miao Y., Sarr M., Bassi C., Büchler M.W.; International Study Group of Pancreatic Surgery (ISGPS). Pancreatic anastomosis after pancreatoduodenectomy: a position statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery (United States). 2017; 161 (5): 1221–1234. https://doi.org/10.1016/j.surg.2016.11.021
8. Pedrazzoli S. Pancreatoduodenectomy (PD) and postoperative pancreatic fistula (POPF). Medicine (Baltimore). 2017; 96 (19): e6858. https://doi.org/10.1097/MD.0000000000006858
9. Schuh F., Mihaljevic A.L., Probst P., Trudeau M.T., Müller P.C., Marchegiani G., Besselink M.G., Uzunoglu F., Izbicki J.R., Falconi M., Castillo C.F., Adham M., Z'graggen K., Friess H., Werner J., Weitz J., Strobel O., Hackert T., Radenkovic D., Kelemen D., Wolfgang C., Miao Y.I., Shrikhande S.V., Lillemoe K.D., Dervenis C., Bassi C., Neoptolemos J.P., Diener M.K., Vollmer C.M. Jr., Büchler M.W. A Simple classification of pancreatic duct size and texture predicts postoperative pancreatic fistula: a classification of the International Study Group of Pancreatic Surgery. Ann. Surg. 2023; 277 (3): e597–e608. https://doi.org/10.1097/SLA.0000000000004855
10. Suurmeijer J.A., Emmen A.M., Bonsing B.A., Busch O.R., Daams F., van Eijck C.H., van Dieren S., de Hingh I.H., Mackay T.M., Mieog J.S., Molenaar I.Q., Stommel M.W., de Meijer V.E., van Santvoort H.C., Groot Koerkamp B., Besselink M.G.; Dutch Pancreatic Cancer Group. Nationwide validation of the ISGPS risk classification for postoperative pancreatic fistula after pancreatoduodenectomy: “Less is more”. Surgery. 2023; 173 (5): 1248–1253. https://doi.org/10.1016/j.surg.2023.01.004
11. Kovalenko Z.A., Efanov M.G. Scoring systems to predict pancreatic fistula after Whipple procedure. Pirogov Russian Journal of Surgery = Khirurgiya. Zurnal im. N.I. Pirogova. 2021; 7: 71–76. https://doi.org/10.17116/hirurgia202107171 (In Russian)
12. Callery M.P., Pratt W.B., Kent T.S., Chaikof E.L., Vollmer Jr C.M. A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J. Am. Coll. Surg. 2013; 216 (1): 1–14. https://doi.org/10.1016/j.jamcollsurg.2012.09.002
13. Mungroop T.H., Klompmaker S., Wellner U.F., Steyerberg E.W., Coratti A., D'Hondt M., de Pastena M., Dokmak S., Khatkov I., Saint-Marc O., Wittel U., Abu Hilal M., Fuks D., Poves I., Keck T., Boggi U., Besselink M.G.; European Consortium on Minimally Invasive Pancreatic Surgery (E-MIPS). Updated Alternative Fistula Risk Score (ua-FRS) to include minimally invasive pancreatoduodenectomy: pan-European validation. Ann. Surg. 2021; 273 (2): 334–340. https://doi.org/10.1097/SLA.0000000000003234
14. Miller B.C., Christein J.D., Behrman S.W., Drebin J.A., Pratt W.B., Callery M.P., Vollmer Jr C.M. A Multi-Institutional external validation of the Fistula Risk Score for pancreato-duodenectomy. J. Gastrointest. Surg. 2014; 18 (1): 172–179; discussion 179–180. https://doi.org/10.1007/s11605-013-2337-8
15. Kantor O., Talamonti M.S., Pitt H.A., Vollmer C.M., Riall T.S., Hall B.L., Wang C.-H., Baker M.S. Using the NSQIP pancreatic demonstration project to derive a modified Fistula Risk Score for preoperative risk stratification in patients undergoing pancreaticoduodenectomy. J. Am. Coll. Surg. 2017; 224 (5): 816–825. https://doi.org/10.1016/j.jamcollsurg.2017.01.054
16. Teränen V., Rinta-Kiikka I., Holli-Helenius K., Laaninen M., Sand J., Laukkarinen J. Perioperative acinar cell count method works well in the prediction of postoperative pancreatic fistula and other postoperative complications after pancreatico-duodenectomy. Pancreatology. 2021; 21 (2): 487–493. https://doi.org/10.1016/j.pan.2021.01.005
17. Jabłońska B., Mrowiec S. Pancreatectomy and pancreatic surgery. Life. 2023; 13 (6): 1400. https://doi.org/10.3390/life13061400
18. Shi Y., Gao F., Qi Y., Lu H., Ai F., Hou Y., Liu C., Xu Y., Zhang X., Cai X. Computed tomography-adjusted Fistula Risk Score for predicting clinically relevant postoperative pancreatic fistula after pancreatoduodenectomy: training and external validation of model upgrade. EBioMedicine. 2020; 62: 103096. https://doi.org/10.1016/j.ebiom.2020.103096
19. Tian X., Li J., Gao H., Zhuang Y., Ma Y., Chen Y., Xie X., Yang Y. Prognostic factors for disease-free survival in patients with pancreatic ductal adenocarcinoma after surgery. J. Pancreatol. 2019; 2 (1): 22–27. https://doi.org/10.1097/JP9.0000000000000011
20. Gorin D.S., Kriger A.G., Galkin G.V., Kalinin D.V., Glotov A.V., Kaldarov A.R., Galchina Yu.S., Berelavichus S.V. Predicting of pancreatic fistula after pancreatoduodenectomy. Pirogov Russian Journal of Surgery = Khirurgiya. Zurnal im. N.I. Pirogova. 2020; 7: 61–67. https://doi.org/10.17116/hirurgia202007161 (In Russian)
21. Galchina Yu.S., Kаrmаzаnovsky G.G., Kalinin D.V., Kondratyev E.V., Gorin D.S., Galkin G.V., Kriger A.G. Diagnostic criteria for a “soft” pancreas and their influence on the occurrence of pancreatic fistula after pancreatoduodenal. Annaly khirurgicheskoy gepatologii = Annals of HPB Surgery. 2020; 25 (2): 113–123. https://doi.org/10.16931/1995-5464.20202113-123 (In Russian)
22. Belyaev O., Herden H., Meier J.J., Muller C.A., Seelig M.H., Herzog T., Tannapfel A., Schmidt W.E., Uhl W. Assessment of pancreatic hardness-surgeon versus durometer. J. Surg. Res. 2010; 158 (1): 53–60. https://doi.org/10.1016/j.jss.2008.08.022
23. Belyaev O., Munding J., Herzog T., Suelberg D., Tannapfel A., Schmidt W.E., Muller C.A., Uhl W. Histomorphological features of the pancreatic remnant as independent risk factors for postoperative pancreatic fistula: a matched-pairs analysis. Pancreatology. 2011; 11 (5): 516–524. https://doi.org/10.1159/000332587
24. Marchegiani G., Ballarin R., Malleo G., Andrianello S., Allegrini W., Pulvirenti A., Paini M., Secchettin E., Boriero F., Benedetto F.Z., Bassi C., Salvia R. Quantitative assessment of pancreatic texture using a durometer: a new tool to predict the risk of developing a postoperative fistula. World J. Surg. 2017; 41 (11): 2876–2883. https://doi.org/10.1007/s00268-017-4073-9
25. Okano K., Oshima M., Kakinoki K., Yamamoto N., Akamoto S., Yachida S., Hagiike M., Kamada H., Masaki T., Suzuki Y. Pancreatic thickness as a predictive factor for postoperative pancreatic fistula after distal pancreatectomy using an endopath stapler. Surg. Today. 2013; 43 (2): 141–147. https://doi.org/10.1007/s00595-012-0235-4
26. Frozanpor F., Loizou L., Ansorge C., Segersvärd R., Lundell L., Albiin N. Preoperative pancreas CT/MRI characteristics predict fistula rate after pancreaticoduodenectomy. World J. Surg. 2012; 36 (8): 1858–1865. https://doi.org/10.1007/s00268-012-1567-3
27. Kirihara Y., Takahashi N., Hashimoto Y., Sclabas M.G., Khan S., Moriya T., Sakagami J., Huebner M., Sarr G.M., Farnell B.M. Prediction of pancreatic anastomotic failure after pancreatoduodenectomy: the use of preoperative, quantitative computed tomography to measure remnant pancreatic volume and body composition. Ann. Surg. 2013; 257 (3): 512–519. https://doi.org/10.1097/SLA.0b013e31827827d0
28. Kitagawa Y., Ishihara R., Ishikawa H., Ito Y., Oyama T., Oyama T., Kato K., Kato H., Kawakubo H., Kawachi H., Kuribayashi S., Kono K., Kojima T., Takeuchi H., Tsushima T., Toh Y., Nemoto K., Booka E., Makino T., Matsuda S., Matsubara H., Mano M., Minashi K., Miyazaki T., Muto M., Yamaji T., Yamatsuji T., Yoshida M. Pancreas-visceral fat CT value ratio and serrated pancreatic contour are strong predictors of postoperative pancreatic fistula after pancreaticojejunostomy. BMC Surg. 2020; 20 (1): 1–12. https://doi.org/10.1186/s12893-020-00785-w
29. Ingwersen E.W., Bereska J.I., Balduzzi A., Janssen B.V., Besselink M.G., Kazemier G., Marchegiani G., Malleo G., Marquering H.A., Nio C.Y., de Robertis R., Salvia R., Steyerberg E.W., Stoker J., Struik F., Verpalen I.M., Daams F. Radiomics preoperative-Fistula Risk Score (RAD-FRS) for pancreatoduodenectomy: development and external validation. BJS Open. 2023; 7 (5): 1–7. https://doi.org/10.1093/bjsopen/zrad100
30. Petrova E., Lapshyn H., Bausch D., D'Haese J., Werner J., Klier T., Nüssler N.C., Gaedcke J., Ghadimi M., Uhl W., Belyaev O., Kantor O., Baker M., Keck T., Wellner U.F. The pancreatic surgery registry (StuDoQ|Pancreas) of the German Society for General and Visceral Surgery (DGAV) – presentation and systematic quality evaluation. Pancreatology. 2017; 18 (1): 17–25. https://doi.org/10.1016/j.pan.2018.11.008
31. Wang K., Dong S.-S., Zhang W., Ni Y.-Y., Xie F., Wang J.C., Wang X.H., Li Y.-W. Surgical methods influence on the risk of anastomotic fistula after pancreaticoduodenectomy: a systematic review and network meta-analysis. Surg. Endosc. 2023; 37 (5): 3380–3397. https://doi.org/10.1007/s00464-022-09832-4
32. Yeo C.J., Cameron J.L., Maher M.M., Sauter P.K., Zahurak M.L., Talamini M.A., Lillemoe K.D., Pitt H.A. A prospective randomized trial of pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy. Ann. Surg. 1995; 222 (4): 580–592. https://doi.org/10.1097/00000658-199510000-00014
33. Hai H., Li Z., Zhang Z., Cheng Y., Liu Z., Gong J., Deng Y. Duct-to-mucosa versus other types of pancreaticojejunostomy for the prevention of postoperative pancreatic fistula following pancreaticoduodenectomy. Cochrane Database Syst. Rev. 2022; 3 (3): CD01346. https://doi.org/10.1002/14651858.CD013462.pub2
34. Halloran C.M., Neoptolemos J.P., Jackson R., Platt K., Psarelli E.E., Reddy S., Gomez D., O'Reilly D.A., Smith A., Pausch T.M., Prachalias A., Davidson B., Ghaneh P. A Multicenter, randomized, double-blinded, clinical trial comparing Cattell-Warren and Blumgart anastomoses following partial pancreatoduodenectomy. Ann. Surg. Open. 2022; 3 (3): e198. https://doi.org/10.1097/AS9.0000000000000198
35. Jiang Y., Chen Q., Shao Y., Gao Z., Jin M., Gao B., Zhou B., Yan S. The prognostic value of external vs internal pancreatic duct stents after pancreaticoduodenectomy in patients with FRS ≥ 4: a retrospective cohort study. BMC Surg. 2021; 21 (1): 1–8. https://doi.org/10.1186/s12893-021-01074-w
36. Salvia R., Lionetto G., Perri G., Malleo G., Marchegiani G. Total pancreatectomy and pancreatic fistula: friend or foe? Updates Surg. 2021; 73 (4): 1231–1236. https://doi.org/10.1007/s13304-021-01130-3
37. Motoi F., Egawa S., Rikiyama T., Katayose Y., Unno M. Randomized clinical trial of external stent drainage of the pancreatic duct to reduce postoperative pancreatic fistula after pancreaticojejunostomy. Br. J. Surg. 2012; 99 (4): 524–531. https://doi.org/10.1002/bjs.8654
38. Codjia T., Roussel E., Papet E., Pinson J., Monge M., Tortajada P., Tuech J.-J., Schwarz L. Can the realization of an external wirsungostomy be an option for high-risk pancreatic anastomosis after pancreaticoduodenectomy? World J. Surg. 2023; 47 (6): 1533–1539. https://doi.org/10.1007/s00268-023-06927-4
39. Casadei R., Ricci C., Taffurelli G., Guariniello A., Di Gioia A., Di Marco M., Pagano N., Serra C., Calculli L., Santini D., Minni F. Is total pancreatectomy as feasible, safe, efficacious, and cost-effective as pancreaticoduodenectomy? A single center, prospective, observational study. J. Gastrointest. Surg. 2016; 20 (9): 1595–1607. https://doi.org/10.1007/s11605-016-3201-4
40. Janot M.S., Belyaev O., Kersting S., Chromik A.M., Seelig M.H., Sülberg D., Mittelkötter U., Uhl W.H. Indications and early outcomes for total pancreatectomy at a high-volume pancreas center. HPB Surg. 2010; 2010: 686702. https://doi.org/10.1155/2010/686702
41. Del Chiaro M., Rangelova E., Segersvärd R., Arnelo U. Are there still indications for total pancreatectomy? Updates Surg. 2016; 68 (3): 257–263. https://doi.org/10.1007/s13304-016-0388-6
42. Ducreux M., Cuhna A.S., Caramella C., Hollebecque A., Burtin P., Goéré D., Seufferlein T., Haustermans K., Van Laethem J.L., Conroy T., Arnold D.; ESMO Guidelines Committee. Cancer of the pancreas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2015; 26 (5): v56–v68. https://doi.org/10.1093/annonc/mdv295
43. Arkadopoulos N., Kyriazi M.A., Papanikolaou I.S., Vasiliou P., Theodoraki K., Lappas C., Oikonomopoulos N., Smyrniotis V. Preoperative biliary drainage of severely jaundiced patients increases morbidity of pancreaticoduodenectomy: results of a case-control study. World J. Surg. 2014; 38 (11): 2967–2972. https://doi.org/10.1007/s00268-014-2669-x
44. Rashid Z., Musaab Munir M., Woldesenbet S., Khalil M., Katayama E., Muntazir Mehdi Khan M., Endo Y., Altaf A., Tsai S., Dillhoff M., Pawlik T. Association of preoperative cholangitis with outcomes and expenditures among patients undergoing pancreaticoduodenectomy. J. Gastrointest. Surg. 2024; 28 (7): 1137–1144. https://doi.org/10.1016/j.gassur.2024.05.009
45. D'Angelica M.I., Ellis R.J., Liu J.B., Brajcich B.C., Gönen M., Thompson V.M., Cohen M.E., Seo S.K., Zabor E.C., Babicky M.L., Bentrem D.J., Behrman S.W., Bertens K.A., Celinski S.A., Chan C.H.F., Dillhoff M., Dixon M.E.B., Fernandez-Del Castillo C., Gholami S., House M.G., Karanicolas P.J., Lavu H., Maithel S.K., McAuliffe J.C., Ott M.J., Reames B.N., Sanford D.E., Sarpel U., Scaife C.L., Serrano P.E., Smith T., Snyder R.A., Talamonti M.S., Weber S.M., Yopp A.C., Pitt H.A., Ko C.Y. Piperacillin-Tazobactam compared with cefoxitin as antimicrobial prophylaxis for pancreatoduodenectomy: a randomized clinical trial. JAMA. 2023; 329 (18): 1579–1588. https://doi.org/10.1001/jama.2023.5728
Supplementary files
Review
For citations:
Ataeva A.N., Mamedov A.F., Kurskov A.O., Kozodaeva M.V., Dalgatov K.D., Sazhin A.V. Risk factors for the development of pancreatic fistula after pancreaticoduodenectomy. Annaly khirurgicheskoy gepatologii = Annals of HPB Surgery. 2024;29(4):144-150. (In Russ.) https://doi.org/10.16931/1995-5464.2024-4-144-150