DOI QR코드

DOI QR Code

Five-year follow-up after pancreatoduodenectomy performed for malignancy: A single-centre study

  • Received : 2022.06.07
  • Accepted : 2022.07.21
  • Published : 2023.02.28

Abstract

Backgrounds/Aims: The aim of this study was to describe short- and long-term outcomes of patients who underwent pancreatoduodenectomy (PD) at a typical United Kingdom hepatopancreatobiliary unit. Methods: A retrospective analysis of all PD patients with histologically-confirmed pancreatic ductal adenocarcinoma (PDAC), ampullary adenocarcinoma (AA), or distal cholangiocarcinoma (CC) from September 1st, 2006 to May 31st, 2015 was carried out. The following information was obtained: demographics, comorbidities, preoperative investigations, neoadjuvant treatment, operative details, postoperative management, complications, adjuvant treatment, five-year recurrence, and five-year survival. Effects of selected preoperative variables on short- and long-term outcomes were investigated. Results: Of 271 included patients, 57.9% had PDAC, 25.8% had AA, and 16.2% had CC. In total, 67.9% experienced morbidity and 17.3% developed a Clavien-Dindo grade ≥ III complication. The 90-day mortality was 3.3%. Clinically-relevant postoperative pancreatic fistula, bile leak, gastrojejunal leak, postpancreatectomy haemorrhage and delayed gastric emptying affected 8.1%, 4.1%, 0.0%, 9.2%, and 19.9% of patients, respectively. American Society of Anesthesiologists grade III-VI correlated with overall morbidity (p = 0.002) and major morbidity (p = 0.009), but not 90-day mortality or five-year survival. The same pattern was observed in patients with a preoperative serum bilirubin > 29 µmol/L and/or a neutrophil/lymphocyte ratio > 3.1. Five-year cancer recurrence and five-year survival were 68.3% and 22.5%, respectively. PDAC patients had higher five-year recurrence but lower five-year survival rates (both p = 0.001). Conclusions: In our series, the majority of patients experienced a complication. However, few patients experienced major morbidity. Surgical risk factors did not affect five-year survival.

Keywords

References

  1. Bekkali NLH, Oppong KW. Pancreatic ductal adenocarcinoma epidemiology and risk assessment: could we prevent? Possibility for an early diagnosis. Endosc Ultrasound 2017;6(Suppl 3):S58-S61. https://doi.org/10.4103/eus.eus_60_17
  2. Ahn DH, Bekaii-Saab T. Ampullary cancer: an overview. Am Soc Clin Oncol Educ Book 2014;34:112-115. https://doi.org/10.14694/EdBook_AM.2014.34.112
  3. Lessing Y, Pencovich N, Nevo N, Lubezky N, Goykhman Y, Nakache R, et al. Early reoperation following pancreaticoduodenectomy: impact on morbidity, mortality, and long-term survival. World J Surg Oncol 2019;17:26.
  4. Crippa S, Belfiori G, Bissolati M, Partelli S, Pagnanelli M, Tamburrino D, et al. Recurrence after surgical resection of pancreatic cancer: the importance of postoperative complications beyond tumor biology. HPB (Oxford) 2021;23:1666-1673. https://doi.org/10.1016/j.hpb.2021.04.004
  5. Pugalenthi A, Protic M, Gonen M, Kingham TP, Angelica MI, Dematteo RP, et al. Postoperative complications and overall survival after pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. J Surg Oncol 2016;113:188-193. https://doi.org/10.1002/jso.24125
  6. 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. https://doi.org/10.1016/j.surg.2016.11.014
  7. Brooke-Smith M, Figueras J, Ullah S, Rees M, Vauthey JN, Hugh TJ, et al. Prospective evaluation of the International Study Group for Liver Surgery definition of bile leak after a liver resection and the role of routine operative drainage: an international multicentre study. HPB (Oxford) 2015;17:46-51. https://doi.org/10.1111/hpb.12322
  8. Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 2007;142:20-25. https://doi.org/10.1016/j.surg.2007.02.001
  9. Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142:761-768. https://doi.org/10.1016/j.surg.2007.05.005
  10. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 2009;250:187-196. https://doi.org/10.1097/SLA.0b013e3181b13ca2
  11. El Nakeeb A, Askar W, Atef E, Hanafy EE, Sultan AM, Salah T, et al. Trends and outcomes of pancreaticoduodenectomy for periampullary tumors: a 25-year single-center study of 1000 consecutive cases. World J Gastroenterol 2017;23:7025-7036. https://doi.org/10.3748/wjg.v23.i38.7025
  12. Russell TB, Aroori S. Procedure-specific morbidity of pancreatoduodenectomy: a systematic review of incidence and risk factors. ANZ J Surg 2022;92:1347-1355. https://doi.org/10.1111/ans.17473
  13. Keck T, Wellner UF, Bahra M, Klein F, Sick O, Niedergethmann M, et al. Pancreatogastrostomy versus pancreatojejunostomy for RE-COnstruction after PANCreatoduodenectomy (RECOPANC, DRKS 00000767): perioperative and long-term results of a multicenter randomized controlled trial. Ann Surg 2016;263:440-449. https://doi.org/10.1097/SLA.0000000000001240
  14. El Nakeeb A, Atef E, El Hanafy E, Salem A, Askar W, Ezzat H, et al. Outcomes of pancreaticoduodenectomy in elderly patients. Hepatobiliary Pancreat Dis Int 2016;15:419-427. https://doi.org/10.1016/S1499-3872(16)60105-4
  15. Zhang D, Gao J, Li S, Wang F, Zhu J, Leng X. Outcome after pancreaticoduodenectomy for malignancy in elderly patients. Hepatogastroenterology 2015;62:451-454.
  16. Wiltberger G, Muhl B, Benzing C, Hau HM, Bartels M, Krenzien F. Pancreaticoduodenectomy in the elderly patient: age-adapted risk assessment. Dig Surg 2017;34:43-51. https://doi.org/10.1159/000448059
  17. Shamali A, De'Ath HD, Jaber B, Abuawad M, Barbaro S, Hamaday Z, et al. Elderly patients have similar short term outcomes and five-year survival compared to younger patients after pancreaticoduodenectomy. Int J Surg 2017;45:138-143. https://doi.org/10.1016/j.ijsu.2017.07.106
  18. Gruppo M, Tolin F, Franzato B, Pilati P, Spolverato YC, Zingales F, et al. Impact of age on short- and long-term outcomes after pancreatoduodenectomy for periampullary neoplasms. Gastroenterol Res Pract 2020;2020:1793051.
  19. Pelosi P, Croci M, Ravagnan I, Tredici S, Pedoto A, Lissoni A, et al. The effects of body mass on lung volumes, respiratory mechanics, and gas exchange during general anesthesia. Anesth Analg 1998;87:654-660. https://doi.org/10.1213/00000539-199809000-00031
  20. Members of the Working Party, Nightingale CE, Margarson MP, Shearer E, Redman JW, Lucas DN, et al. Peri-operative management of the obese surgical patient 2015: Association of Anaesthetists of Great Britain and Ireland Society for Obesity and Bariatric Anaesthesia. Anaesthesia 2015;70:859-876. https://doi.org/10.1111/anae.13101
  21. Chen YT, Deng Q, Che X, Zhang JW, Chen YH, Zhao DB, et al. Impact of body mass index on complications following pancreatectomy: ten-year experience at National Cancer Center in China. World J Gastroenterol 2015;21:7218-7224. https://doi.org/10.3748/wjg.v21.i23.7218
  22. Aoki S, Miyata H, Konno H, Gotoh M, Motoi F, Kumamaru H, et al. Risk factors of serious postoperative complications after pancreaticoduodenectomy and risk calculators for predicting postoperative complications: a nationwide study of 17,564 patients in Japan. J Hepatobiliary Pancreat Sci 2017;24:243-251. https://doi.org/10.1002/jhbp.438
  23. El Nakeeb A, Hamed H, Shehta A, Askr W, El Dosoky M, Said R, et al. Impact of obesity on surgical outcomes post-pancreaticoduodenectomy: a case-control study. Int J Surg 2014;12:488-493. https://doi.org/10.1016/j.ijsu.2014.01.017
  24. Dandona M, Linehan D, Hawkins W, Strasberg S, Gao F, Wang-Gillam A. Influence of obesity and other risk factors on survival outcomes in patients undergoing pancreaticoduodenectomy for pancreatic cancer. Pancreas 2011;40:931-937. https://doi.org/10.1097/MPA.0b013e318215a9b1
  25. Gaujoux S, Torres J, Olson S, Winston C, Gonen M, Brennan MF, et al. Impact of obesity and body fat distribution on survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg Oncol 2012;19:2908-2916. https://doi.org/10.1245/s10434-012-2301-y
  26. Del Chiaro M, Rangelova E, Ansorge C, Blomberg J, Segersvard R. Impact of body mass index for patients undergoing pancreaticoduodenectomy. World J Gastrointest Pathophysiol 2013;4:37-42. https://doi.org/10.4291/wjgp.v4.i2.37
  27. Greenblatt DY, Kelly KJ, Rajamanickam V, Wan Y, Hanson T, Rettammel R, et al. Preoperative factors predict perioperative morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol 2011;18:2126-2135. https://doi.org/10.1245/s10434-011-1594-6
  28. Tsai S, Choti MA, Assumpcao L, Cameron JL, Gleisner AL, Herman JM, et al. Impact of obesity on perioperative outcomes and survival following pancreaticoduodenectomy for pancreatic cancer: a large single-institution study. J Gastrointest Surg 2010;14:1143-1150. https://doi.org/10.1007/s11605-010-1201-3
  29. Deo KB, Kulkarni AA, Kumar-M P, Krishnamurthy G, Shenvi S, Rana SS, et al. Impact of diabetes mellitus on morbidity and survival after pancreaticoduodenectomy for malignancy. Ann Hepatobiliary Pancreat Surg 2021;25:230-241. https://doi.org/10.14701/ahbps.2021.25.2.230
  30. Lv X, Qiao W, Leng Y, Wu L, Zhou Y. Impact of diabetes mellitus on clinical outcomes of pancreatic cancer after surgical resection: a systematic review and meta-analysis. PLoS One 2017;12:e0171370.
  31. Xia X, Huang C, Cen G, Qiu ZJ. Preoperative diabetes as a protective factor for pancreatic fistula after pancreaticoduodenectomy: a meta-analysis. Hepatobiliary Pancreat Dis Int 2015;14:132-138. https://doi.org/10.1016/S1499-3872(15)60330-7
  32. Nakeeb AE, Shehta A, Said R, Dosoky ME, Moneer A, Elrefai M, et al. Impact of diabetes mellitus on the outcomes after pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: a single center experience. Surg Gastroenterol Oncol 2018;23:342-349. https://doi.org/10.21614/sgo-23-5-342
  33. King JT Jr, Goulet JL, Perkal MF, Rosenthal RA. Glycemic control and infections in patients with diabetes undergoing noncardiac surgery. Ann Surg 2011;253:158-165. https://doi.org/10.1097/SLA.0b013e3181f9bb3a
  34. Ronnekleiv-Kelly SM, Greenblatt DY, Lin CP, Kelly KJ, Cho CS, Winslow ER, e al. Impact of cardiac comorbidity on early outcomes after pancreatic resection. J Gastrointest Surg 2014;18:512-522. https://doi.org/10.1007/s11605-013-2399-7
  35. de la Fuente SG, Bennett KM, Pappas TN, Scarborough JE. Pre- and intraoperative variables affecting early outcomes in elderly patients undergoing pancreaticoduodenectomy. HPB (Oxford) 2011;13:887-892. https://doi.org/10.1111/j.1477-2574.2011.00390.x
  36. DeOliveira ML, Winter JM, Schafer M, Cunningham SC, Cameron JL, Yeo CJ, et al. Assessment of complications after pancreatic surgery: a novel grading system applied to 633 patients undergoing pancreaticoduodenectomy. Ann Surg 2006;244:931-937; discussion 937-939. https://doi.org/10.1097/01.sla.0000246856.03918.9a
  37. Shia BC, Qin L, Lin KC, Fang CY, Tsai LL, Kao YW, et al. Age comorbidity scores as risk factors for 90-day mortality in patients with a pancreatic head adenocarcinoma receiving a pancreaticoduodenectomy: a national population-based study. Cancer Med 2020;9:562-574. https://doi.org/10.1002/cam4.2730
  38. Eeson G, Chang N, McGahan CE, Khurshed F, Buczkowski AK, Scudamore CH, et al. Determination of factors predictive of outcome for patients undergoing a pancreaticoduodenectomy of pancreatic head ductal adenocarcinomas. HPB (Oxford) 2012;14:310-316. https://doi.org/10.1111/j.1477-2574.2012.00448.x
  39. Braga M, Capretti G, Pecorelli N, Balzano G, Doglioni C, Ariotti R, et al. A prognostic score to predict major complications after pancreaticoduodenectomy. Ann Surg 2011;254:702-707; discussion 707-708. https://doi.org/10.1097/SLA.0b013e31823598fb
  40. Wiltberger G, Muhl B, Benzing C, Atanasov G, Hau HM, Horn M, et al. Preoperative risk stratification for major complications following pancreaticoduodenectomy: identification of high-risk patients. Int J Surg 2016;31:33-39. https://doi.org/10.1016/j.ijsu.2016.04.034
  41. Scheufele F, Aichinger L, Jager C, Demir IE, Schorn S, Demir E, et al. INR and not bilirubin levels predict postoperative morbidity in patients with malignant obstructive jaundice. Am J Surg 2021;222:976-982. https://doi.org/10.1016/j.amjsurg.2021.04.016
  42. Pamecha V, Sadashiv Patil N, Kumar S, Rajendran V, Gupta S, Vasantrao Sasturkar S, et al. Upfront pancreaticoduodenectomy in severely jaundiced patients: is it safe? J Hepatobiliary Pancreat Sci 2019;26:524-533. https://doi.org/10.1002/jhbp.671
  43. Wang S, Wang X, Li L, Dai H, Han J. Association of preoperative obstructive jaundice with postoperative infectious complications following pancreaticoduodenectomy. Hepatogastroenterology 2013;60:1274-1279.
  44. Pavlidis ET, Pavlidis TE. Pathophysiological consequences of obstructive jaundice and perioperative management. Hepatobiliary Pancreat Dis Int 2018;17:17-21. https://doi.org/10.1016/j.hbpd.2018.01.008
  45. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-444. https://doi.org/10.1038/nature07205
  46. Clark EJ, Connor S, Taylor MA, Madhavan KK, Garden OJ, Parks RW. Preoperative lymphocyte count as a prognostic factor in resected pancreatic ductal adenocarcinoma. HPB (Oxford) 2007;9:456-460. https://doi.org/10.1080/13651820701774891
  47. Arikan T, Sozuer EM, Topal U, Dal F, Bozkurt GK, Yilmaz AZ. The value and prognostic significance of neutrophil / lymphocyte ratio in predicting pancreatic fistula in patients undergoing pancreaticoduodenectomy for periampullary tumors. Ann Med Res 2020;27:1214-1220. https://doi.org/10.5455/annalsmedres.2019.12.792
  48. Mowbray NG, Griffith D, Hammoda M, Shingler G, Kambal A, Al-Sarireh B. A meta-analysis of the utility of the neutrophil-to-lymphocyte ratio in predicting survival after pancreatic cancer resection. HPB (Oxford) 2018;20:379-384. https://doi.org/10.1016/j.hpb.2017.12.009
  49. Ida M, Tachiiri Y, Sato M, Kawaguchi M. Neutrophil-to-lymphocyte ratio as indicator to severe complication after pancreaticoduodenectomy or distal pancreatectomy. Acta Anaesthesiol Scand 2019;63:739-744. https://doi.org/10.1111/aas.13341
  50. Huang H, Wang C, Ji F, Han Z, Xu H, Cao M. Nomogram based on albumin and neutrophil-to-lymphocyte ratio for predicting postoperative complications after pancreaticoduodenectomy. Gland Surg 2021;10:877-891. https://doi.org/10.21037/gs-20-789
  51. Shen Z, Xu Z, Wang W, Xu W, Zhou Y, Lu X, et al. A novel nomogram for predicting the risk of major complications after pancreaticoduodenectomy in patients with obstructive jaundice. Clin Chim Acta 2021;517:162-170. https://doi.org/10.1016/j.cca.2021.02.018