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Prognostic impact of splenic vessel involvement and tumor size in distal pancreatectomy for adenocarcinoma: a retrospective multicentric cohort study

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Abstract

Purpose

Splenic vessel involvement occurs frequently in pancreatic ductal adenocarcinoma (PDAC) of the body and the tail (B/T) but the impact on survival is unknown. We assessed the influence of radiological and pathologic involvement of splenic artery (p-SA +) and vein (p-SV +) on patient outcomes after distal pancreatectomy (DP) for PDAC.

Methods

From 2013 to 2019, all DP for PDAC in five centers were included. Factors associated with overall (OS) and disease-free (DFS) survival were identified.

Results

Among the 76 patients included, 5 (6.6%) had p-SA + only, 11 (14.5%) had p-SV + only, and 24 (31.6%) had both p-SA + and p-SV + . The preoperative CT-scan accuracy to predict p-SV + and p-SA + was high (sensitivity: 91.4% and 82.8%, respectively; negative predictive value: 89.7% and 88.3%, respectively). The 5-year OS and DFS rates were 3.9% and 8.3%, respectively. Multivariate analysis identified splenic vessel involvement (i.e., p-SA + or p-SV + , or both p-SA + and p-SV +) as the only independent factor influencing DFS (HR 4.04; 95% CI [1.22–13.44], p = 0.023). Tumor size ≥ 30 mm was the only independent factor influencing OS (HR 4.04; 95% CI [1.26–12.95], p = 0.019) and was associated with a high risk of p-SA + (p = 0.001) and p-SV + (p < 0.001).

Conclusion

Tumor size ≥ 30 mm and splenic vessel involvement occurred in more than half of the patients who underwent DP for PDAC and had negative impact on long-term survival. Preoperative CT-scan was reliable to identify splenic vessel involvement in B/T PDAC. Large tumor size and radiological splenic vessel involvement could be taken into account to propose a neoadjuvant treatment.

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Data availability

The data that support the findings of this study are available on request from the corresponding author.

Code availability

Analyses were done using SPSS 24.0 (IBM corporation, Armonk, NY).

References

  1. Ferlay J, Partensky C, Bray F (2016) More deaths from pancreatic cancer than breast cancer in the EU by 2017. Acta Oncol 55(9–10):1158–1160. https://doi.org/10.1080/0284186X.2016.1197419

    Article  CAS  PubMed  Google Scholar 

  2. Siegel RL, Miller KD, Jemal A (2018) Cancer statistics, 2018: cancer statistics, 2018. CA: Cancer J Clin 68(1):7–30. https://doi.org/10.3322/caac.21442

    Article  Google Scholar 

  3. Warshaw AL, Castillo CF (1992) Pancreatic . carcinoma N Engl J Med 13;326(7):455–65. https://doi.org/10.1056/NEJM199202133260706

    Article  Google Scholar 

  4. Sener SF, Fremgen A, Menck HR, Winchester DP (1999) Pancreatic cancer: a report of treatment and survival trends for 100,313 patients diagnosed from 1985–1995, using the National Cancer Database. J Am Coll Surg 189(1):1–7. https://doi.org/10.1016/s1072-7515(99)00075-7

    Article  CAS  PubMed  Google Scholar 

  5. Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Büchler MW (2004) Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg 91(5):586–594. https://doi.org/10.1002/bjs.4484

    Article  CAS  PubMed  Google Scholar 

  6. Paye F, MicelliLupinacci R, Bachellier P, Boher J-M, Delpero J-R (2015) The French Surgical Association (AFC). Distal pancreatectomy for pancreatic carcinoma in the era of multimodal treatment. Br J Surg 102(3):229–36. https://doi.org/10.1002/bjs.9708

    Article  CAS  PubMed  Google Scholar 

  7. Brennan MF, Moccia RD, Klimstra D (1996) Management of adenocarcinoma of the body and tail of the pancreas. Ann Surg 223(5):506–512. https://doi.org/10.1097/00000658-199605000-00006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Schwarz RE, Harrison LE, Conlon KC, Klimstra DS, Brennan MF (1999) The impact of splenectomy on outcomes after resection of pancreatic adenocarcinoma. J Am Coll Surg 188(5):516–521. https://doi.org/10.1016/s1072-7515(99)00041-1

    Article  CAS  PubMed  Google Scholar 

  9. Fujita T, Nakagohri T, Gotohda N, Takahashi S, Konishi M, Kojima M et al (2010) Evaluation of the prognostic factors and significance of lymph node status in invasive ductal carcinoma of the body or tail of the pancreas. Pancreas 39(1):e48-54. https://doi.org/10.1097/MPA.0b013e3181bd5cfa

    Article  PubMed  Google Scholar 

  10. 9th National Comprehensive Cancer Network (2019). NCCN clinical practice guidelines in oncology (NCCN Guidelines). Pancreatic adenocarcinoma. Version 3. http://www.nccn.org/professionals/ physician_gls/f_guidelines.asp. Accessed 2019

  11. Barugola G, Partelli S, Crippa S, Capelli P, D’Onofrio M, Pederzoli P et al (2012) Outcomes after resection of locally advanced or borderline resectable pancreatic cancer after neoadjuvant therapy. The American Journal of Surgery 203(2):132–139. https://doi.org/10.1016/j.amjsurg.2011.03.008

    Article  PubMed  Google Scholar 

  12. Ferrone CR, Marchegiani G, Hong TS, Ryan DP, Deshpande V, McDonnell EI et al (2015) Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann Surg 261(1):12–17. https://doi.org/10.1097/SLA.0000000000000867

    Article  PubMed  Google Scholar 

  13. Cloyd JM, Katz MHG, Prakash L, Varadhachary GR, Wolff RA, Shroff RT et al (2017) Preoperative therapy and pancreatoduodenectomy for pancreatic ductal adenocarcinoma: a 25-year single-institution experience. J Gastrointest Surg 21(1):164–174. https://doi.org/10.1007/s11605-016-3265-1

    Article  PubMed  Google Scholar 

  14. Gillen S, Schuster T, Meyer Zum Büschenfelde C, Friess H, Kleeff J (2010) Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med 7(4):e1000267. https://doi.org/10.1371/journal.pmed.1000267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wang F, Gill AJ, Neale M, Puttaswamy V, Gananadha S, Pavlakis N et al (2014) Adverse tumor biology associated with mesenterico-portal vein resection influences survival in patients with pancreatic ductal adenocarcinoma. Ann Surg Oncol 21(6):1937–1947. https://doi.org/10.1245/s10434-014-3554-4

    Article  CAS  PubMed  Google Scholar 

  16. Mierke F, Hempel S, Distler M, Aust DE, Saeger H-D, Weitz J et al (2016) Impact of portal vein involvement from pancreatic cancer on metastatic pattern after surgical resection. Ann Surg Oncol 23(S5):730–736. https://doi.org/10.1245/s10434-016-5515-6

    Article  PubMed  Google Scholar 

  17. Kanda M, Fujii T, Sahin TT, Kanzaki A, Nagai S, Yamada S et al (2010) Invasion of the splenic artery is a crucial prognostic factor in carcinoma of the body and tail of the pancreas. Ann Surg 251(3):483–487. https://doi.org/10.1097/SLA.0b013e3181cf9171

    Article  PubMed  Google Scholar 

  18. Partelli S, Crippa S, Barugola G, Tamburrino D, Capelli P, D’Onofrio M et al (2011) Splenic artery invasion in pancreatic adenocarcinoma of the body and tail: a novel prognostic parameter for patient selection. Ann Surg Oncol 18(13):3608–3614. https://doi.org/10.1245/s10434-011-1769-1

    Article  PubMed  Google Scholar 

  19. Fukami Y, Kaneoka Y, Maeda A, Takayama Y, Onoe S (2016) Prognostic impact of splenic artery invasion for pancreatic cancer of the body and tail. Int J Surg 35:64–68. https://doi.org/10.1016/j.ijsu.2016.09.076

    Article  PubMed  Google Scholar 

  20. Shimada K, Sakamoto Y, Sano T, Kosuge T (2006) Prognostic factors after distal pancreatectomy with extended lymphadenectomy for invasive pancreatic adenocarcinoma of the body and tail. Surgery 139(3):288–295. https://doi.org/10.1016/j.surg.2005.08.004

    Article  PubMed  Google Scholar 

  21. Mizumoto T, Toyama H, Asari S, Terai S, Mukubo H, Yamashita H et al (2018) Pathological and radiological splenic vein involvement are predictors of poor prognosis and early liver metastasis after surgery in patients with pancreatic adenocarcinoma of the body and tail. Ann Surg Oncol 25(3):638–646. https://doi.org/10.1245/s10434-017-6274-8

    Article  PubMed  Google Scholar 

  22. Hyun JJ, Rose JB, Alseidi AA, Biehl TR, Helton S, Coy DL et al (2019) Significance of radiographic splenic vessel involvement in the pancreatic ductal adenocarcinoma of the body and tail of the gland. J Surg Oncol 120(2):262–269. https://doi.org/10.1002/jso.25498

    Article  PubMed  Google Scholar 

  23. Dedania N, Agrawal N, Winter JM, Koniaris LG, Rosato EL, Sauter PK et al (2013) Splenic vein thrombosis is associated with an increase in pancreas-specific complications and reduced survival in patients undergoing distal pancreatectomy for pancreatic exocrine cancer. J Gastrointest Surg 17(8):1392–1398. https://doi.org/10.1007/s11605-013-2260-z

    Article  PubMed  Google Scholar 

  24. Agha R, Abdall-Razak A, Crossley E, Dowlut N, Iosifidis C, Mathew G et al (2019) STROCSS 2019 Guideline: strengthening the reporting of cohort studies in surgery. Int J Surg 72:156–165. https://doi.org/10.1016/j.ijsu.2019.11.002

    Article  PubMed  Google Scholar 

  25. Collard M, Marchese T, Guedj N, Cauchy F, Chassaing C, Ronot M et al (2019) Is routine splenectomy justified for all left-sided pancreatic cancers? Histological Reappraisal of Splenic Hilar Lymphadenectomy. Ann Surg Oncol 26(4):1071–1078. https://doi.org/10.1245/s10434-018-07123-8

    Article  PubMed  Google Scholar 

  26. Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213. https://doi.org/10.1016/j.ijsu.2019.11.002

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M et al (2017) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery 161(3):584–591. https://doi.org/10.1016/j.surg.2016.11.014

    Article  PubMed  Google Scholar 

  28. Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR et al (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142(5):761–768. https://doi.org/10.1016/j.surg.2007.05.005

    Article  PubMed  Google Scholar 

  29. Yekebas EF, Wolfram L, Cataldegirmen G, Habermann CR, Bogoevski D, Koenig AM et al (2007) Postpancreatectomy hemorrhage: diagnosis and treatment: an analysis in 1669 consecutive pancreatic resections. Ann Surg 246(2):269–280. https://doi.org/10.1097/01.sla.0000262953.77735.db

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lu DS, Reber HA, Krasny RM, Kadell BM, Sayre J (1997) Local staging of pancreatic cancer: criteria for unresectability of major vessels as revealed by pancreatic-phase, thin-section helical CT. Am J Roentgenol 168(6):1439–1443. https://doi.org/10.2214/ajr.168.6.9168704

    Article  CAS  Google Scholar 

  31. Brierley JD, Gospodarowicz MK, Wittekind C (2016) TNM classification of malignant tumours, 8th edn. Wiley-Blackwell, Hoboken

    Google Scholar 

  32. Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, Gershenwald JE, Compton CC, Hess KR et al (2017) AJCC cancer staging manual (8th edition). Springer International Publishing, American Joint Commission on Cancer

  33. Fluss R, Faraggi D, Reiser B (2005) Estimation of the Youden Index and its associated cutoff point. Biom J 47(4):458–472. https://doi.org/10.1002/bimj.200410135

    Article  PubMed  Google Scholar 

  34. 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 4(10):40. https://doi.org/10.3389/fonc.2020.00040

    Article  Google Scholar 

  35. Schwarz L, Vernerey D, Bachet J-B, Tuech J-J, Portales F, Michel P et al (2018) Resectable pancreatic adenocarcinoma neo-adjuvant FOLF(IRIN)OX-based chemotherapy - a multicenter, non-comparative, randomized, phase II trial (PANACHE01-PRODIGE48 study). BMC Cancer 24;18(1):762. https://doi.org/10.1186/s12885-018-4663-4

    Article  CAS  Google Scholar 

  36. Crippa S, Cirocchi R, Maisonneuve P, Partelli S, Pergolini I, Tamburrino D et al (2018) Systematic review and meta-analysis of prognostic role of splenic vessels infiltration in resectable pancreatic cancer. Eur J Surg Oncol 44(1):24–30. https://doi.org/10.1016/j.ejso.2017.10.217

    Article  PubMed  Google Scholar 

  37. Bissolati M, Sandri MT, Burtulo G, Zorzino L, Balzano G, Braga M (2015) Portal vein-circulating tumor cells predict liver metastases in patients with resectable pancreatic cancer. Tumor Biol 36(2):991–996. https://doi.org/10.1007/s13277-014-2716-0

    Article  CAS  Google Scholar 

  38. Kayahara M, Nakagawara H, Kitagawa H, Ohta T (2007) The nature of neural invasion by pancreatic cancer. Pancreas 35(3):218–223. https://doi.org/10.1097/mpa.0b013e3180619677

    Article  PubMed  Google Scholar 

  39. Neuzillet C, Sauvanet A, Hammel P (2011) Prognostic factors for resectable pancreatic adenocarcinoma. J Visc Surg 148(4):e232–e243. https://doi.org/10.1016/j.jviscsurg.2011.07.007

    Article  CAS  PubMed  Google Scholar 

  40. Sirri E, Castro FA, Kieschke J, Jansen L, Emrich K, Gondos A et al (2016) Recent trends in survival of patients with pancreatic cancer in Germany and the United States. Pancreas 45(6):908–914. https://doi.org/10.1097/MPA.0000000000000588

    Article  PubMed  Google Scholar 

  41. Kim BH, Kim K, Chie EK, Jang J-Y, Kim SW, Han S-W et al (2015) Prognostic value of splenic artery invasion in patients undergoing adjuvant chemoradiotherapy after distal pancreatectomy for pancreatic adenocarcinoma. Cancer Res Treat 47(2):274–281. https://doi.org/10.4143/crt.2014.025

    Article  CAS  PubMed  Google Scholar 

  42. Takahashi H, Ohigashi H, Gotoh K, Marubashi S, Yamada T, Murata M et al (2013) Preoperative gemcitabine-based chemoradiation therapy for resectable and borderline resectable pancreatic cancer. Ann Surg 258(6):1040–1050. https://doi.org/10.1097/SLA.0b013e31829b3ce4

    Article  PubMed  Google Scholar 

  43. Lof S, Korrel M, van Hilst J, Alseidi A, Balzano G, Boggi U et al (2020) Impact of neoadjuvant therapy in resected pancreatic ductal adenocarcinoma of the pancreatic body or tail on surgical an oncological outcome: a propensity-score matched multicenter study. Ann Surg Oncol 7(6):1986–1996. https://doi.org/10.1245/s10434-019-08137-6

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Authors and Affiliations

  1. Department of Digestive Surgery, Hôpital Nord, Aix-Marseille University, Marseille, France

    Dominique Gantois, Théophile Guilbaud, Olivier Picaud, Vincent Moutardier & David Jérémie Birnbaum

  2. Department of Radiology, Hôpital Nord, Aix-Marseille University, Marseille, France

    Ugo Scemama

  3. Department of Digestive Surgery and Liver Transplantation, Hôpital Michalon, Grenoble University, Grenoble, France

    Edouard Girard & Mircea Chirica

  4. Department of Anatomopathology, Institut Mutualiste Montsouris, Paris, France

    Marine Lefevre

  5. Department of Anatomopathology, Hôpital Trousseau, Tours, France

    Myriam Elgani

  6. Self Perceived Health Assessment Research Unit and Department of Public Health, Aix-Marseille University, Chemin des Bourrely, 13915, Marseille cedex 20, France

    Zeinab Hamidou

  7. Department of Digestive and Oncologic Surgery, Hôpital D’Instruction des Armées St-Anne, Toulon, France

    Paul Balandraud

  8. Department of Digestive, Oncologic, Metabolic Surgery and Liver Transplantation, Hôpital Trousseau, Tours, France

    Louise Barbier

  9. Department of Digestive, Oncologic and Metabolic Surgery, Institut Mutualiste Montsouris, Paris, France

    David Fuks

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  1. Dominique Gantois
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  2. Théophile Guilbaud
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  14. David Jérémie Birnbaum
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Contributions

Study conception and design: Dominique Gantois, Théophile Guilbaud, and David Jérémie Birnbaum.

Acquisition of data: Dominique Gantois, Théophile Guilbaud, Edouard Girard, Ugo Scemama, Olivier Picaud, Marine Lefevre, Myriam Elgani, and David Jérémie Birnbaum.

Analysis and interpretation of data: Dominique Gantois, Théophile Guilbaud, Zeinab Hamidou, Mircea Chirica, David Fuks, Louise Barbier, and David Jérémie Birnbaum.

Drafting of manuscript: Dominique Gantois, Théophile Guilbaud, Mircea Chirica, David Fuks, Louise Barbier, and David Jérémie Birnbaum.

Critical revision of manuscript: Théophile Guilbaud, Mircea Chirica, David Fuks, Louise Barbier, Vincent Moutardier, Paul Balandraud, and David Jérémie Birnbaum.

Corresponding author

Correspondence to David Jérémie Birnbaum.

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The study was approved by the local ethics committee of each hospital.

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Supplementary Information

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423_2021_2291_MOESM1_ESM.tiff

Supplementary file1 (TIFF 212 KB) Correlation between tumor size and pathological (a) splenic artery involvement, (b) splenic vein involvement. p-SA+, pathological splenic artery involvement; p-SA-, no pathological splenic artery involvement; p-SV+, pathological splenic vein involvement; p-SV-, no pathological splenic vein involvement.

423_2021_2291_MOESM2_ESM.tif

Supplementary file2 (TIF 109 KB) ROC curve analyzing correlation between tumor size and pathological (a) splenic artery involvement, (b) splenic vein involvement. A tumor size ≥ 30 mm had a Se, Sp, PPV and NPV of 79.31%, 55.32%, 52.27% and 81.25%, respectively in predicting SA involvement. A tumor size ≥ 30 mm had a Se, Sp, PPV and NPV of 62.86%, 80.49%, 73.33% and 71.74%, respectively in predicting SV involvement.

423_2021_2291_MOESM3_ESM.tiff

Supplementary file3 (TIFF 640 KB) Incidence of liver metastases regarding (a) splenic artery and (b) splenic vein pathological involvement status. Incidence of peritoneal carcinomatosis regarding (c) splenic artery and (d) splenic vein pathological involvement status. p-SA+, pathological splenic artery involvement; p-SA-, no pathological splenic artery involvement; p-SV+, pathological splenic vein involvement; p-SV-, no pathological splenic vein involvement.

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Gantois, D., Guilbaud, T., Scemama, U. et al. Prognostic impact of splenic vessel involvement and tumor size in distal pancreatectomy for adenocarcinoma: a retrospective multicentric cohort study. Langenbecks Arch Surg 407, 153–165 (2022). https://doi.org/10.1007/s00423-021-02291-w

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