Enucleation for low-grade branch duct intraductal papillary mucinous neoplasms: Long-term follow-up



      Pancreatic enucleation allows resection of branch-duct intraductal papillary mucinous neoplasms with full parenchyma preservation. The aim of this study was to assess intraductal papillary mucinous neoplasms recurrence and functional outcomes during long-term follow-up after enucleation.


      Patient characteristics, as well as radiologic and clinicopathologic follow-up data of patients who underwent enucleation for branch-duct intraductal papillary mucinous neoplasms between 2004 and 2014, were analyzed. Quality of life was assessed using the EORTC QLQ-C30 and QLQ-PAN26 questionnaires.


      Seventy-four patients underwent enucleation for low-grade branch-duct intraductal papillary mucinous neoplasms in 71 and high-grade branch-duct intraductal papillary mucinous neoplasms in 3 patients. Long-term follow-up data were available for 66 patients (89%; median follow-up: 87 months). Radiologic imaging (n = 56) showed intraductal papillary mucinous neoplasm recurrence in 10 patients (18%) including local recurrence at the site of enucleation in 3 patients (5%) and new onset intraductal papillary mucinous neoplasms manifestation in 7 patients (13%) at a distant site in the pancreatic remnant. Four patients (6%) underwent reoperation. Two of these patients had intraductal papillary mucinous neoplasm-associated carcinoma, one of them at the enucleation site. During the follow-up period, no intraductal papillary mucinous neoplasm-related deaths occurred and no new onsets of insulin-dependent diabetes mellitus were observed. QLQ-C30 revealed a global health status of 66.0% and overall functioning and symptom scores of 81.0% and 22.8%, respectively. Additionally, QLQ-PAN26 showed an overall symptom score of 26.5%.


      Enucleation is an organ-preserving surgical treatment option for low-grade branch-duct intraductal papillary mucinous neoplasms with low local recurrence risk and excellent functional long-term outcome. However, postoperative life-long follow-up must be performed as for any type of partial pancreatectomy for intraductal papillary mucinous neoplasms due to the risk of recurrence and potential malignancy.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Hruban R.H.
        • Pitman M.B.
        • Klimstra D.S.
        Intraductal neoplasms.
        in: 4 ed. AFIP Atlas of Tumor Pathology, Series 4: Tumors of the Pancreas Series. American Registry of Pathology, Washington, DC2007: 75-110
      1. Correa-Gallego C, Ferrone CR, Thayer SP, et al. Incidental pancreatic cysts: do we really know what we are watching? Pancreatology. 10:144–150.

        • Sohn T.A.
        • Yeo C.J.
        • Cameron J.L.
        • et al.
        Intraductal papillary mucinous neoplasms of the pancreas: an updated experience.
        Ann Surg. 2004; 239 (discussion 797–799): 788-797
        • Hruban R.H.
        • Takaori K.
        • Klimstra D.S.
        • et al.
        An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms.
        Am J Surg Pathol. 2004; 28: 977-987
        • Longnecker D.S.
        Intraductal papillary-mucinous tumors of the pancreas.
        Arch Pathol Lab Med. 1995; 119: 197-198
        • Adsay N.V.
        • Fukushima N.
        • Furukawa T.
        Intraductal Neoplasms of the Pancreas in WHO Classification of Tumor of the Digestive System.
        IARC, Lyon2010
        • Basturk O.
        • Hong S.M.
        • Wood L.D.
        • et al.
        A revised classification system and recommendations from the Baltimore Consensus Meeting for Neoplastic Precursor Lesions in the Pancreas.
        Am J Surg Pathol. 2015; 39: 1730-1741
        • Crippa S.
        • Fernández-Del Castillo C.
        • Salvia R.
        • et al.
        Mucin-producing neoplasms of the pancreas: an analysis of distinguishing clinical and epidemiologic characteristics.
        Clin Gastroenterol Hepatol. 2010; 8: 213-219
        • Tanaka M.
        • Fernández-Del Castillo C.
        • Kamisawa T.
        • et al.
        Revisions of international consensus Fukuoka guidelines for the management of IPMN of the pancreas.
        Pancreatology. 2017; 17: 738-753
        • Laffan T.A.
        • Horton K.M.
        • Klein A.P.
        • et al.
        Prevalence of unsuspected pancreatic cysts on MDCT.
        AJR Am J Roentgenol. 2008; 191: 802-807
        • Plichta J.K.
        • Ban K.
        • Fridirici Z.
        • et al.
        Should all branch-duct intraductal papillary mucinous neoplasms be resected?.
        Am J Surg. 2015; 209: 478-482
        • Jang J.Y.
        • Park T.
        • Lee S.
        • et al.
        Validation of international consensus guidelines for the resection of branch duct-type intraductal papillary mucinous neoplasms.
        Br J Surg. 2014; 101: 686-692
        • Hackert T.
        • Hinz U.
        • Fritz S.
        • et al.
        Enucleation in pancreatic surgery: indications, technique, and outcome compared to standard pancreatic resections.
        Langenbecks Arch Surg. 2011; 396: 1197-1203
        • Turrini O.
        • Schmidt C.M.
        • Pitt H.A.
        • et al.
        Side-branch intraductal papillary mucinous neoplasms of the pancreatic head/uncinate: resection or enucleation?.
        HPB. 2011; 13: 126-131
        • Strobel O.
        • Cherrez A.
        • Hinz U.
        • et al.
        Risk of pancreatic fistula after enucleation of pancreatic tumours.
        Br J Surg. 2015; 102: 1258-1266
        • Kaiser J.
        • Fritz S.
        • Klauss M.
        • et al.
        Enucleation: a treatment alternative for branch duct intraductal papillary mucinous neoplasms.
        Surgery. Nov 21 2016;
        • Ei S.
        • Mihaljevic A.L.
        • Kulu Y.
        • et al.
        Enucleation for benign or borderline tumors of the pancreas: comparing open and minimally invasive surgery.
        HPB (Oxford). 2021; 23: 921-926
        • von Elm E.
        • Altman D.G.
        • Egger M.
        • et al.
        The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies.
        Int J Surg. 2014; 12: 1495-1499
        • Aaronson N.K.
        • Ahmedzai S.
        • Bergman B.
        • et al.
        The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology.
        J Natl Cancer Inst. 1993; 85: 365-376
        • Nolte S.
        • Waldmann A.
        • Liegl G.
        • et al.
        Updated EORTC QLQ-C30 general population norm data for Germany.
        Eur J Cancer. 2020; 137: 161-170
        • Wundsam H.V.
        • Rösch C.S.
        • Kirchweger P.
        • et al.
        Long-term quality of life after pancreatic surgery for intraductal papillary mucinous neoplasm.
        Eur Surg Res. 2021; 62: 80-87
        • Hartwig W.
        • Werner J.
        • Jager D.
        • Debus J.
        • Buchler M.W.
        Improvement of surgical results for pancreatic cancer.
        Lancet Oncol. 2013; 14: e476-e485
        • Keck T.
        • Wellner U.F.
        • Bahra M.
        • et al.
        Pancreatogastrostomy versus pancreatojejunostomy for RECOnstruction After PANCreatoduodenectomy (RECOPANC, DRKS 00000767): perioperative and long-term results of a multicenter randomized controlled trial.
        Ann Surg. 2016; 263: 440-449
        • Zhang T.
        • Mu Y.
        • Qu L.
        • et al.
        Accurate combined preoperative localization of insulinomas aid the choice for enucleation: a single institution experience over 25 years.
        Hepatogastroenterology. 2012; 59: 1282-1285
        • Huttner F.J.
        • Koessler-Ebs J.
        • Hackert T.
        • Ulrich A.
        • Buchler M.W.
        • Diener M.K.
        Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms.
        Br J Surg. 2015; 102: 1026-1136
        • Song K.B.
        • Kim S.C.
        • Hwang D.W.
        • et al.
        Enucleation for benign or low-grade malignant lesions of the pancreas: single-center experience with 65 consecutive patients.
        Surgery. 2015; 158: 1203-1210
        • Crippa S.
        • Zerbi A.
        • Boninsegna L.
        • et al.
        Surgical management of insulinomas: short- and long-term outcomes after enucleations and pancreatic resections.
        Arch Surg. 2012; 147: 261-266
        • Zhang R.C.
        • Zhou Y.C.
        • Mou Y.P.
        • et al.
        Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis.
        Surg Endosc. 2016; 30: 2657-2665
        • Zhou Y.
        • Zhao M.
        • Wu L.
        • Ye F.
        • Si X.
        Short- and long-term outcomes after enucleation of pancreatic tumors: an evidence-based assessment.
        Pancreatology. 2016; 16: 1092-1098
        • Jilesen A.P.
        • van Eijck C.H.
        • Busch O.R.
        • van Gulik T.M.
        • Gouma D.J.
        • van Dijkum E.J.
        Postoperative outcomes of enucleation and standard resections in patients with a pancreatic neuroendocrine tumor.
        World J Surg. 2016; 40: 715-728
        • Hirono S.
        • Shimizu Y.
        • Ohtsuka T.
        • et al.
        Recurrence patterns after surgical resection of intraductal papillary mucinous neoplasm (IPMN) of the pancreas; a multicenter, retrospective study of 1074 IPMN patients by the Japan Pancreas Society.
        J Gastroenterol. 2020; 55: 86-99
        • Sauvanet A.
        • Gaujoux S.
        • Blanc B.
        • et al.
        Parenchyma-sparing pancreatectomy for presumed noninvasive intraductal papillary mucinous neoplasms of the pancreas.
        Ann Surg. 2014; 260: 364-371
        • Beger H.G.
        • Poch B.
        • Mayer B.
        • Siech M.
        New onset of diabetes and pancreatic exocrine insufficiency after pancreaticoduodenectomy for benign and malignant tumors: a systematic review and meta-analysis of long-term results.
        Ann Surg. 2018; 267: 259-270
        • Crippa S.
        • Bassi C.
        • Salvia R.
        • Falconi M.
        • Butturini G.
        • Pederzoli P.
        Enucleation of pancreatic neoplasms.
        Br J Surg. 2007; 94: 1254-1259
        • Giuliani T.
        • De Pastena M.
        • Paiella S.
        • et al.
        Pancreatic enucleation patients share the same quality of life as the general population at long-term follow-up: a propensity-score matched analysis.
        Ann Surg. 2021; (Online ahead of print)