Outcomes in intraductal papillary mucinous neoplasm-derived pancreatic cancer differ from PanIN-derived pancreatic cancer.

colloid intraductal papillary mucinous neoplasm invasive IPMN pancreatic cancer pancreatic cyst pancreatic neoplasms tubular

Journal

Journal of gastroenterology and hepatology
ISSN: 1440-1746
Titre abrégé: J Gastroenterol Hepatol
Pays: Australia
ID NLM: 8607909

Informations de publication

Date de publication:
31 Jul 2024
Historique:
revised: 27 05 2024
received: 17 03 2024
accepted: 13 07 2024
medline: 1 8 2024
pubmed: 1 8 2024
entrez: 1 8 2024
Statut: aheadofprint

Résumé

Intraductal papillary mucinous neoplasm (IPMN)-derived pancreatic ductal adenocarcinoma (PDAC) management is generally extrapolated from pancreatic intraepithelial neoplasia (PanIN)-derived PDAC guidelines. However, these are biologically divergent, and heterogeneity further exists between tubular and colloid subtypes. Consecutive upfront surgery patients with PanIN-derived and IPMN-derived PDAC were retrospectively identified from international centers (2000-2019). One-to-one propensity score matching for clinicopathologic factors generated three cohorts: IPMN-derived versus PanIN-derived PDAC, tubular IPMN-derived versus PanIN-derived PDAC, and tubular versus colloid IPMN-derived PDAC. Overall survival (OS) was compared using Kaplan-Meier and log-rank tests. Multivariable Cox regression determined corresponding hazard ratios (HR) and 95% confidence intervals (95% CI). The median OS (mOS) in 2350 PanIN-derived and 700 IPMN-derived PDAC patients was 23.0 and 43.1 months (P < 0.001), respectively. PanIN-derived PDAC had worse T-stage, CA19-9, grade, and nodal status. Tubular subtype had worse T-stage, CA19-9, grade, nodal status, and R1 margins, with a mOS of 33.7 versus 94.1 months (P < 0.001) in colloid. Matched (n = 495), PanIN-derived and IPMN-derived PDAC had mOSs of 30.6 and 42.8 months (P < 0.001), respectively. In matched (n = 341) PanIN-derived and tubular IPMN-derived PDAC, mOS remained poorer (27.7 vs 37.4, P < 0.001). Matched tubular and colloid cancers (n = 112) had similar OS (P = 0.55). On multivariable Cox regression, PanIN-derived PDAC was associated with worse OS than IPMN-derived (HR: 1.66, 95% CI: 1.44-1.90) and tubular IPMN-derived (HR: 1.53, 95% CI: 1.32-1.77) PDAC. Colloid and tubular subtype was not associated with OS (P = 0.16). PanIN-derived PDAC has worse survival than IPMN-derived PDAC supporting distinct outcomes. Although more indolent, colloid IPMN-derived PDAC has similar survival to tubular after risk adjustment.

Sections du résumé

BACKGROUND AND AIM OBJECTIVE
Intraductal papillary mucinous neoplasm (IPMN)-derived pancreatic ductal adenocarcinoma (PDAC) management is generally extrapolated from pancreatic intraepithelial neoplasia (PanIN)-derived PDAC guidelines. However, these are biologically divergent, and heterogeneity further exists between tubular and colloid subtypes.
METHODS METHODS
Consecutive upfront surgery patients with PanIN-derived and IPMN-derived PDAC were retrospectively identified from international centers (2000-2019). One-to-one propensity score matching for clinicopathologic factors generated three cohorts: IPMN-derived versus PanIN-derived PDAC, tubular IPMN-derived versus PanIN-derived PDAC, and tubular versus colloid IPMN-derived PDAC. Overall survival (OS) was compared using Kaplan-Meier and log-rank tests. Multivariable Cox regression determined corresponding hazard ratios (HR) and 95% confidence intervals (95% CI).
RESULTS RESULTS
The median OS (mOS) in 2350 PanIN-derived and 700 IPMN-derived PDAC patients was 23.0 and 43.1 months (P < 0.001), respectively. PanIN-derived PDAC had worse T-stage, CA19-9, grade, and nodal status. Tubular subtype had worse T-stage, CA19-9, grade, nodal status, and R1 margins, with a mOS of 33.7 versus 94.1 months (P < 0.001) in colloid. Matched (n = 495), PanIN-derived and IPMN-derived PDAC had mOSs of 30.6 and 42.8 months (P < 0.001), respectively. In matched (n = 341) PanIN-derived and tubular IPMN-derived PDAC, mOS remained poorer (27.7 vs 37.4, P < 0.001). Matched tubular and colloid cancers (n = 112) had similar OS (P = 0.55). On multivariable Cox regression, PanIN-derived PDAC was associated with worse OS than IPMN-derived (HR: 1.66, 95% CI: 1.44-1.90) and tubular IPMN-derived (HR: 1.53, 95% CI: 1.32-1.77) PDAC. Colloid and tubular subtype was not associated with OS (P = 0.16).
CONCLUSIONS CONCLUSIONS
PanIN-derived PDAC has worse survival than IPMN-derived PDAC supporting distinct outcomes. Although more indolent, colloid IPMN-derived PDAC has similar survival to tubular after risk adjustment.

Identifiants

pubmed: 39086101
doi: 10.1111/jgh.16686
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024 The Author(s). Journal of Gastroenterology and Hepatology published by Journal of Gastroenterology and Hepatology Foundation and John Wiley & Sons Australia, Ltd.

Références

Principe DR, Underwood PW, Korc M, Trevino JG, Munshi HG, Rana A. The current treatment paradigm for pancreatic ductal adenocarcinoma and barriers to therapeutic efficacy. Front. Oncol. 2021; 11: 688377.
Ren B, Liu X, Suriawinata AA. Pancreatic ductal adenocarcinoma and its precursor lesions: histopathology, cytopathology, and molecular pathology. Am. J. Pathol. 2019; 189: 9–21.
Khoury RE, Kabir C, Maker VK, Banulescu M, Wasserman M, Maker AV. What is the incidence of malignancy in resected intraductal papillary mucinous neoplasms? An analysis of over 100 US institutions in a single year. Ann. Surg. Oncol. 2018; 25: 1746–1751.
Aronsson L, Bengtsson A, Toren W, Andersson R, Ansari D. Intraductal papillary mucinous carcinoma versus pancreatic ductal adenocarcinoma: a systematic review and meta‐analysis. Int. J. Surg. 2019; 71: 91–99.
Koh YX, Chok AY, Zheng HL, Tan CS, Goh BK. Systematic review and meta‐analysis comparing the surgical outcomes of invasive intraductal papillary mucinous neoplasms and conventional pancreatic ductal adenocarcinoma. Ann. Surg. Oncol. 2014; 21: 2782–2800.
Fritz S, Fernandez‐del Castillo C, Mino‐Kenudson M et al. Global genomic analysis of intraductal papillary mucinous neoplasms of the pancreas reveals significant molecular differences compared to ductal adenocarcinoma. Ann. Surg. 2009; 249: 440–447.
Patra KC, Bardeesy N, Mizukami Y. Diversity of precursor lesions for pancreatic cancer: the genetics and biology of intraductal papillary mucinous neoplasm. Clin. Transl. Gastroenterol. 2017; 8: e86.
Fouladi DF, Raman SP, Hruban RH, Fishman EK, Kawamoto S. Invasive intraductal papillary mucinous neoplasms: CT features of colloid carcinoma versus tubular adenocarcinoma of the pancreas. AJR Am. J. Roentgenol. 2020; 214: 1092–1100.
Markovitz M, Jiang K, Kim D, Rose T, Permuth JB, Jeong D. Pancreatic colloid adenocarcinoma arising from intraductal papillary mucinous neoplasm: Radiologic‐pathologic correlation with cinematic rendering. Acta Radiol Open 2023; 12: 20584601231157046.
Marchegiani G, Mino‐Kenudson M, Sahora K et al. IPMN involving the main pancreatic duct: biology, epidemiology, and long‐term outcomes following resection. Ann. Surg. 2015; 261: 976–983.
Marchegiani G, Andrianello S, Dal Borgo C et al. Adjuvant chemotherapy is associated with improved postoperative survival in specific subtypes of invasive intraductal papillary mucinous neoplasms (IPMN) of the pancreas: it is time for randomized controlled data. HPB (Oxford) 2019; 21: 596–603.
Habib JR, Kinny‐Köster B, Amini N et al. Predictors, patterns, and timing of recurrence provide insight into the disease biology of invasive carcinomas arising in association with intraductal papillary mucinous neoplasms. J. Gastrointest. Surg. 2022; 26: 2311–2320.
Mino‐Kenudson M, Fernandez‐del Castillo C, Baba Y et al. Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes. Gut 2011; 60: 1712–1720.
Humphris JL, Chang DK, Johns AL et al. The prognostic and predictive value of serum CA19.9 in pancreatic cancer. Ann. Oncol. 2012; 23: 1713–1722.
Amin MB, Greene FL, Edge SB et al. The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population‐based to a more “personalized” approach to cancer staging. CA Cancer J. Clin. 2017; 67: 93–99.
Brookhart MA, Schneeweiss S, Rothman KJ, Glynn RJ, Avorn J, Sturmer T. Variable selection for propensity score models. Am. J. Epidemiol. 2006; 163: 1149–1156.
Rubin DB, Thomas N. Matching using estimated propensity scores: relating theory to practice. Biometrics 1996; 52: 249–264.
Waters JA, Schnelldorfer T, Aguilar‐Saavedra JR et al. Survival after resection for invasive intraductal papillary mucinous neoplasm and for pancreatic adenocarcinoma: a multi‐institutional comparison according to American Joint Committee on Cancer Stage. J. Am. Coll. Surg. 2011; 213: 275–283.
Ziogas IA, Rodriguez Franco S, Schmoke N et al. Comparison of invasive pancreatic ductal adenocarcinoma versus intraductal papillary mucinous neoplasm: a national cancer database analysis. Cancers (Basel) 2023; 15: 1185.
Gavazzi F, Capretti G, Giordano L et al. Pancreatic ductal adenocarcinoma and invasive intraductal papillary mucinous tumor: different prognostic factors for different overall survival. Dig. Liver Dis. 2022; 54: 826–833.
Yamaguchi K, Kanemitsu S, Hatori T et al. Pancreatic ductal adenocarcinoma derived from IPMN and pancreatic ductal adenocarcinoma concomitant with IPMN. Pancreas 2011; 40: 571–580.
Kaiser J, Scheifele C, Hinz U et al. IPMN‐associated pancreatic cancer: Survival, prognostic staging and impact of adjuvant chemotherapy. Eur. J. Surg. Oncol. 2022; 48: 1309–1320.
Yopp AC, Katabi N, Janakos M et al. Invasive carcinoma arising in intraductal papillary mucinous neoplasms of the pancreas: a matched control study with conventional pancreatic ductal adenocarcinoma. Ann. Surg. 2011; 253: 968–974.
Holmberg M, Ghorbani P, Gilg S, del Chiaro M, Arnelo U, Löhr JM, Sparrelid E. Outcome after resection for invasive intraductal papillary mucinous neoplasia is similar to conventional pancreatic ductal adenocarcinoma. Pancreatology 2021; 21: 1371–1377.
Poultsides GA, Reddy S, Cameron JL et al. Histopathologic basis for the favorable survival after resection of intraductal papillary mucinous neoplasm‐associated invasive adenocarcinoma of the pancreas. Ann. Surg. 2010; 251: 470–476.
Winter JM, Jiang W, Basturk O et al. Recurrence and survival after resection of small intraductal papillary mucinous neoplasm‐associated carcinomas (</=20‐mm invasive component): a multi‐institutional analysis. Ann. Surg. 2016; 263: 793–801.
Margonis GA, Pulvirenti A, Morales‐Oyarvide V et al. Performance of the 7th and 8th editions of the American Joint Committee on cancer staging system in patients with intraductal papillary mucinous neoplasm‐associated PDAC: a multi‐institutional analysis. Ann. Surg. 2023; 277: 681–688.
Escalon JG, Gerst S, Porembka M, Allen PJ, Do RK. Imaging comparison of tubular and colloid pancreatic adenocarcinoma arising from intraductal papillary mucinous neoplasm on multidetector CT. Clin. Imaging 2016; 40: 1195–1199.
Aronsson L, Marinko S, Ansari D, Andersson R. Adjuvant therapy in invasive intraductal papillary mucinous neoplasm (IPMN) of the pancreas: a systematic review. Ann. Transl. Med. 2019; 7: 689.

Auteurs

Joseph R Habib (JR)

Department of Surgery, New York University Langone Health, New York, New York, USA.
Department of Surgery, Regional Academic Cancer Center Utrecht, UMC Utrecht Cancer Center and St. Antonius Hospital Nieuwegein, Utrecht, The Netherlands.

Ingmar F Rompen (IF)

Department of Surgery, New York University Langone Health, New York, New York, USA.
Heidelberg University Hospital, Heidelberg, Germany.

Ammar A Javed (AA)

Department of Surgery, New York University Langone Health, New York, New York, USA.

Mahip Grewal (M)

Department of Surgery, New York University Langone Health, New York, New York, USA.

Benedict Kinny-Köster (B)

Heidelberg University Hospital, Heidelberg, Germany.

Paul C M Andel (PCM)

Department of Surgery, Regional Academic Cancer Center Utrecht, UMC Utrecht Cancer Center and St. Antonius Hospital Nieuwegein, Utrecht, The Netherlands.

D Brock Hewitt (DB)

Department of Surgery, New York University Langone Health, New York, New York, USA.

Greg D Sacks (GD)

Department of Surgery, New York University Langone Health, New York, New York, USA.

Marc G Besselink (MG)

Department of Surgery, Amsterdam UMC, location University of Amsterdam, Amsterdam, The Netherlands.
Cancer Center Amsterdam, Amsterdam, The Netherlands.

Hjalmar C van Santvoort (HC)

Department of Surgery, Regional Academic Cancer Center Utrecht, UMC Utrecht Cancer Center and St. Antonius Hospital Nieuwegein, Utrecht, The Netherlands.

Lois A Daamen (LA)

Department of Surgery, Regional Academic Cancer Center Utrecht, UMC Utrecht Cancer Center and St. Antonius Hospital Nieuwegein, Utrecht, The Netherlands.
Division of Imaging and Oncology, University Medical Center Utrecht, Utrecht, The Netherlands.

Martin Loos (M)

Heidelberg University Hospital, Heidelberg, Germany.

Jin He (J)

Department of Surgery, Johns Hopkins Hospital, Baltimore, Maryland, USA.

Markus W Büchler (MW)

Champalimaud Foundation, Lisbon, Portugal.

Christopher L Wolfgang (CL)

Department of Surgery, New York University Langone Health, New York, New York, USA.

I Quintus Molenaar (IQ)

Department of Surgery, Regional Academic Cancer Center Utrecht, UMC Utrecht Cancer Center and St. Antonius Hospital Nieuwegein, Utrecht, The Netherlands.

Classifications MeSH