Ann Hepatobiliary Pancreat Surg.  2024 Nov;28(4):423-432. 10.14701/ahbps.24-118.

Survival after vascular resections in patients with borderline resectable or locally advanced pancreatic head cancer: A systematic review

• Papakonstantinou M
• Fiflis S
• Giakoustidis A
• Christodoulidis G
• Myriskou A
• Louri E
• Papalavrentios L
• Papadopoulos VN
• Giakoustidis D

• KMID: 2561574
• DOI: http://doi.org/10.14701/ahbps.24-118

Abstract

Pancreatic ductal adenocarcinoma (PDAC) is one of the most aggressive tumors, and the most common cause of cancer-related deaths. In the past, vascular infiltration of the tumor rendered the disease unresectable. However, today, venous or arterial involvement of a PDAC is classified as borderline resectable (BR) or locally advanced (LA) disease. Pancreaticoduodenectomy (PD) with vascular resections is a promising intervention intended for complete resection of BR- and LA-PDAC. This study aims to assess the overall survival of patients undergoing PD with vascular resections, compared to those without. A PubMed search was conducted for cohort studies that included patients with BR- or LA-PDAC treated with vascular resections. The retrieved publications were screened following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) checklist. The study protocol was registered at the International Prospective Register for Systematic Reviews (PROSPERO). Sixteen cohort studies were included in our systematic review. Fourteen of them included patients undergoing PD with venous-only resections for PDAC. The 5-year overall survival rates ranged from 8.0% to 22.2% for vascular resection patients, and 4.0% to 24.3% for standard PD patients. Three cohorts included patients with PDAC and arterial and/or venous involvement who were treated with arterial resections. Their median overall survival ranged from 13.7 to 17.0 months, similar to that of patients who did not undergo vascular resections. PD with vascular resections in patients with BR- and LA-PDAC could lead to similar overall survival to that after standard PD.

Keyword

Pancreatic neoplasms; Surgical procedures; Pancreaticoduodenectomy; Mortality

Figure

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  Fig. 1 PRISMA flowchart.

Reference

References

1. 2023. All cancer sites combined recent trends in SEER age-adjusted incidence rates, 2000-2021 [Internet]. SEER;Available from: https://seer.cancer.gov/statistics-network/explorer/application.html?site=1&data_type=1&graph_type=2&compareBy=sex&chk_sex_3=3&chk_sex_2=2&rate_type=2&race=1&age_range=1&hdn_stage=101&advopt_precision=1&advopt_show_ci=on&hdn_view=0&advopt_show_apc=on&advopt_display=2#resultsRegion0. cited 2024 May 31.

2. Park W, Chawla A, O'Reilly EM. 2021; Pancreatic cancer: a review. JAMA. 326:851–862. DOI: 10.1001/jama.2021.13027. PMID: 34547082. PMCID: PMC9363152.

3. Luketina RR, Hackert T, Büchler MW. 2015; Vascular resection in pancreatic cancer. Indian J Surg. 77:381–386. DOI: 10.1007/s12262-015-1364-y. PMID: 26722200. PMCID: PMC4689703.

4. Andersson R, Vagianos CE, Williamson RC. 2004; Preoperative staging and evaluation of resectability in pancreatic ductal adenocarcinoma. HPB (Oxford). 6:5–12. DOI: 10.1080/13651820310017093. PMID: 18333037. PMCID: PMC2020655.

5. Javed AA, Young RWC, Habib JR, Kinny-Köster B, Cohen SM, Fishman EK, et al. 2022; Cinematic rendering: novel tool for improving pancreatic cancer surgical planning. Curr Probl Diagn Radiol. 51:878–883. DOI: 10.1067/j.cpradiol.2022.04.001. PMID: 35595587.

6. Isaji S, Mizuno S, Windsor JA, Bassi C, Fernández-Del Castillo C, Hackert T, et al. 2018; International consensus on definition and criteria of borderline resectable pancreatic ductal adenocarcinoma 2017. Pancreatology. 18:2–11. DOI: 10.1016/j.pan.2017.11.011. PMID: 29191513.

7. Previous version: SEER cancer statistics review, 1975-2009 (vintage 2009 populations) [Internet]. SEER;2012. cited 2024 May 31. Available from: https://seer.cancer.gov/archive/csr/1975_2009_pops09/index.html.

8. Delpero JR, Sauvanet A. 2020; Vascular resection for pancreatic cancer: 2019 French recommendations based on a literature review from 2008 to 6-2019. Front Oncol. 10:40. DOI: 10.3389/fonc.2020.00040. PMID: 32117714. PMCID: PMC7010716.

9. Limbu Y, Regmee S, Ghimire R, Maharjan DK, Thapa PB. 2021; Arterial divestment and resection in post-neoadjuvant pancreatic adenocarcinoma. Cureus. 13:e20275. DOI: 10.7759/cureus.20275.

10. Strobel O, Hank T, Hinz U, Bergmann F, Schneider L, Springfeld C, et al. 2017; Pancreatic cancer surgery: the new R-status counts. Ann Surg. 265:565–573. DOI: 10.1097/SLA.0000000000001731. PMID: 27918310.

11. Moore GE, Sako Y, Thomas LB. 1951; Radical pancreatoduodenectomy with resection and reanastomosis of the superior mesenteric vein. Surgery. 30:550–553.

12. Appleby LH. 1953; The coeliac axis in the expansion of the operation for gastric carcinoma. Cancer. 6:704–707. DOI: 10.1002/1097-0142(195307)6:4<704::AID-CNCR2820060410>3.0.CO;2-P. PMID: 13059764.

13. Bratlie SO, Wennerblom J, Vilhav C, Persson J, Rangelova E. 2021; Resectable, borderline, and locally advanced pancreatic cancer-"the good, the bad, and the ugly" candidates for surgery? J Gastrointest Oncol. 12:2450–2460. DOI: 10.21037/jgo-2020-slapc-04. PMID: 34790406. PMCID: PMC8576252.

14. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. 2021; The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 372:n71. DOI: 10.1136/bmj.n71. PMID: 33782057. PMCID: PMC8005924.

15. Wells G, Shea B, O'Connell D, Robertson J, Peterson J, Welch V, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analysis [Internet]. Oxford (UK);2011. Available from: http://www.evidencebasedpublichealth.de/download/Newcastle_Ottowa_Scale_Pope_Bruce.pdf. cited 2024 May 31.

16. Addeo P, Velten M, Averous G, Faitot F, Nguimpi-Tambou M, Nappo G, et al. 2017; Prognostic value of venous invasion in resected T3 pancreatic adenocarcinoma: depth of invasion matters. Surgery. 162:264–274. DOI: 10.1016/j.surg.2017.03.008. PMID: 28576385.

17. Bachellier P, Rosso E, Fuchshuber P, Addeo P, David P, Oussoultzoglou E, et al. 2014; Use of a temporary intraoperative mesentericoportal shunt for pancreatic resection for locally advanced pancreatic cancer with portal vein occlusion and portal hypertension. Surgery. 155:449–456. DOI: 10.1016/j.surg.2013.09.003. PMID: 24462078.

18. Flis V, Potrc S, Kobilica N, Ivanecz A. 2016; Pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head with venous resection. Radiol Oncol. 50:321–328. DOI: 10.1515/raon-2015-0017. PMID: 27679549. PMCID: PMC5024653.

19. Han S, Choi DW, Choi SH, Heo JS, Han IW, You YH. 2021; Long-term outcomes following en bloc resection for pancreatic ductal adenocarcinoma of the head with portomesenteric venous invasion. Asian J Surg. 44:313–320. DOI: 10.1016/j.asjsur.2020.07.021. PMID: 32972828.

20. Malleo G, Maggino L, Marchegiani G, Feriani G, Esposito A, Landoni L, et al. 2017; Pancreatectomy with venous resection for pT3 head adenocarcinoma: perioperative outcomes, recurrence pattern and prognostic implications of histologically confirmed vascular infiltration. Pancreatology. 17:847–857. DOI: 10.1016/j.pan.2017.08.005. PMID: 28843714.

21. Martin D, Petermann D, Fontanella S, Pu Y, Halkic N, Demartines N, et al. 2018; Pancreatic adenocarcinoma with histologically proven portal vein infiltration: what is the outcome? Eur J Gastroenterol Hepatol. 30:1507–1513. DOI: 10.1097/MEG.0000000000001266. PMID: 30222630.

22. Ravikumar R, Sabin C, Abu Hilal M, Bramhall S, White S, Wigmore S, et al. 2014; Portal vein resection in borderline resectable pancreatic cancer: a United Kingdom multicenter study. J Am Coll Surg. 218:401–411. DOI: 10.1016/j.jamcollsurg.2013.11.017. PMID: 24484730.

23. Xie ZB, Gu JC, Zhang YF, Yao L, Jin C, Jiang YJ, et al. 2017; Portal vein resection and reconstruction with artificial blood vessels is safe and feasible for pancreatic ductal adenocarcinoma patients with portal vein involvement: Chinese center experience. Oncotarget. 8:77883–77896. DOI: 10.18632/oncotarget.20847. PMID: 29100433. PMCID: PMC5652822.

24. Bachellier P, Addeo P, Faitot F, Nappo G, Dufour P. 2020; Pancreatectomy with arterial resection for pancreatic adenocarcinoma: how can it be done safely and with which outcomes?: a single institution's experience with 118 patients. Ann Surg. 271:932–940. DOI: 10.1097/SLA.0000000000003010. PMID: 30188399.

25. Elberm H, Ravikumar R, Sabin C, Abu Hilal M, Al-Hilli A, Aroori S, et al. 2015; Outcome after pancreaticoduodenectomy for T3 adenocarcinoma: a multivariable analysis from the UK Vascular Resection for Pancreatic Cancer Study Group. Eur J Surg Oncol. 41:1500–1507. DOI: 10.1016/j.ejso.2015.08.158. PMID: 26346183.

26. Lapshyn H, Bronsert P, Bolm L, Werner M, Hopt UT, Makowiec F, et al. 2016; Prognostic factors after pancreatoduodenectomy with en bloc portal venous resection for pancreatic cancer. Langenbecks Arch Surg. 401:63–69. DOI: 10.1007/s00423-015-1363-2. PMID: 26739620.

27. Murakami Y, Uemura K, Sudo T, Hashimoto Y, Nakashima A, Kondo N, et al. 2013; Benefit of portal or superior mesenteric vein resection with adjuvant chemotherapy for patients with pancreatic head carcinoma. J Surg Oncol. 107:414–421. DOI: 10.1002/jso.23229. PMID: 22886567.

28. Turley RS, Peterson K, Barbas AS, Ceppa EP, Paulson EK, Blazer DG 3rd, et al. 2012; Vascular surgery collaboration during pancreaticoduodenectomy with vascular reconstruction. Ann Vasc Surg. 26:685–692. DOI: 10.1016/j.avsg.2011.11.009. PMID: 22305864.

29. Fang JZ, Lu CD, Wu SD, Huang J, Zhou J. 2017; Portal vein/superior mesenteric vein resection in pancreatic cancer treatment in the elderly. Medicine (Baltimore). 96:e7335. DOI: 10.1097/MD.0000000000007335. PMID: 28682880. PMCID: PMC5502153.

30. Hwang JW, Kim SC, Song KB, Yoon JH, Nam JS, Lee JH, et al. 2015; Significance of radiologic location and extent of portal venous involvement on prognosis after resection for pancreatic adenocarcinoma. Pancreas. 44:665–671. DOI: 10.1097/MPA.0000000000000309. PMID: 25806602.

31. Jeong J, Choi DW, Choi SH, Heo JS, Jang KT. 2015; Long-term outcome of portomesenteric vein invasion and prognostic factors in pancreas head adenocarcinoma. ANZ J Surg. 85:264–269. DOI: 10.1111/ans.12502. PMID: 24641800.

32. Oba A, Bao QR, Barnett CC, Al-Musawi MH, Croce C, Schulick RD, et al. 2020; Vascular resections for pancreatic ductal adenocarcinoma: vascular resections for PDAC. Scand J Surg. 109:18–28. DOI: 10.1177/1457496919900413. PMID: 31960765.

33. Małczak P, Sierżęga M, Stefura T, Kacprzyk A, Droś J, Skomarovska O, et al. 2020; Arterial resections in pancreatic cancer - systematic review and meta-analysis. HPB (Oxford). 22:961–968. DOI: 10.1016/j.hpb.2020.04.005. PMID: 32360186.

34. Miao Y, Jiang K, Cai B, Lu Z, Wu J, Gao W, et al. 2016; Arterial divestment instead of resection for locally advanced pancreatic cancer (LAPC). Pancreatology. 16:S59. DOI: 10.1016/j.pan.2016.05.201.

35. Diener MK, Mihaljevic AL, Strobel O, Loos M, Schmidt T, Schneider M, et al. 2021; Periarterial divestment in pancreatic cancer surgery. Surgery. 169:1019–1025. DOI: 10.1016/j.surg.2020.08.030. PMID: 33032819.

36. Karamarković AR, Juloski JT. 2022; Current surgical concepts and future perspectives in the treatment of borderline resectable and potentially resectable locally advanced pancreatic cancer. Chirurgia (Bucur). 117:385–398. DOI: 10.21614/chirurgia.2770. PMID: 36049095.

37. Loos M, Kester T, Klaiber U, Mihaljevic AL, Mehrabi A, Müller-Stich BM, et al. 2022; Arterial resection in pancreatic cancer surgery: effective after a learning curve. Ann Surg. 275:759–768. DOI: 10.1097/SLA.0000000000004054. PMID: 33055587.

38. Cai B, Lu Z, Neoptolemos JP, Diener MK, Li M, Yin L, et al. 2021; Sub-adventitial divestment technique for resecting artery-involved pancreatic cancer: a retrospective cohort study. Langenbecks Arch Surg. 406:691–701. DOI: 10.1007/s00423-021-02080-5. PMID: 33507403.

39. Hackert T, Strobel O, Michalski CW, Mihaljevic AL, Mehrabi A, Müller-Stich B, et al. 2017; The TRIANGLE operation - radical surgery after neoadjuvant treatment for advanced pancreatic cancer: a single arm observational study. HPB (Oxford). 19:1001–1007. DOI: 10.1016/j.hpb.2017.07.007. PMID: 28838632.

40. Masiak-Segit W, Rawicz-Pruszyński K, Skórzewska M, Polkowski WP. 2018; Surgical treatment of pancreatic cancer. Pol Przegl Chir. 90:45–53. DOI: 10.5604/01.3001.0011.7493. PMID: 29773761.

41. Klotz R, Hackert T, Heger P, Probst P, Hinz U, Loos M, et al. 2022; The TRIANGLE operation for pancreatic head and body cancers: early postoperative outcomes. HPB (Oxford). 24:332–341. DOI: 10.1016/j.hpb.2021.06.432. PMID: 34294523.

42. Dumitraşcu T, Popescu I. 2022; Pancreatico-duodenectomy for pancreatic ductal adenocarcinoma: from artery-first approaches to TRIANGLE operation. Chirurgia (Bucur). 117:377–384. DOI: 10.21614/chirurgia.2771. PMID: 36049094.

43. Zhai S, Huo Z, Wang Y, Qian H, Zhao S, Shi Y, et al. 2019; TRIANGLE operation for borderline resectable pancreatic cancer in total pancreatectomy. Transl Cancer Res. 8:2416–2424. DOI: 10.21037/tcr.2019.09.50. PMID: 35116994. PMCID: PMC8798168.

44. Rosso E, Zimmitti G, Iannelli A, Garatti M. 2020; The 'TRIANGLE operation' by laparoscopy: radical pancreaticoduodenectomy with major vascular resection for borderline resectable pancreatic head cancer. Ann Surg Oncol. 27:1613–1614. DOI: 10.1245/s10434-019-08101-4. PMID: 31802299.

45. Heger P, Hackert T, Diener MK, Feißt M, Klose C, Dörr-Harim C, et al. 2023; Conventional partial pancreatoduodenectomy versus an extended pancreatoduodenectomy (triangle operation) for pancreatic head cancers-study protocol for the randomised controlled TRIANGLE trial. Trials. 24:363. DOI: 10.1186/s13063-023-07337-6. PMID: 37254179. PMCID: PMC10228091.

46. Giuliano K, Ejaz A, He J. 2017; Technical aspects of pancreaticoduodenectomy and their outcomes. Chin Clin Oncol. 6:64. DOI: 10.21037/cco.2017.09.01. PMID: 29156887.

47. Fancellu A, Petrucciani N, Porcu A, Deiana G, Sanna V, Ninniri C, et al. 2020; the impact on survival and morbidity of portal-mesenteric resection during pancreaticoduodenectomy for pancreatic head adenocarcinoma: a systematic review and meta-analysis of comparative studies. Cancers (Basel). 12:1976. DOI: 10.3390/cancers12071976. PMID: 32698500. PMCID: PMC7409306.

48. Bockhorn M, Uzunoglu FG, Adham M, Imrie C, Milicevic M, Sandberg AA, et al. 2014; Borderline resectable pancreatic cancer: a consensus statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 155:977–988. DOI: 10.1016/j.surg.2014.02.001. PMID: 24856119.

49. Brown ZJ, Cloyd JM. 2021; Trends in the utilization of neoadjuvant therapy for pancreatic ductal adenocarcinoma. J Surg Oncol. 123:1432–1440. DOI: 10.1002/jso.26384. PMID: 33831253.