Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes

Mari Mino-Kenudson, Carlos Fernández-del Castillo, Yoshifumi Baba, Nakul P. Valsangkar, Andrew S. Liss, Maylee Hsu, Camilo Correa-Gallego, Thun Ingkakul, Rocio Perez Johnston, Brian G. Turner, Vasiliki Androutsopoulos, Vikram Deshpande, Deborah McGrath, Dushyant V. Sahani, William R. Brugge, Shuji Ogino, Martha B. Pitman, Andrew L. Warshaw, Sarah P. Thayer

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Abstract

Objective: Invasive cancers arising from intraductal papillary mucinous neoplasm (IPMN) are recognised as a morphologically and biologically heterogeneous group of neoplasms. Less is known about the epithelial subtypes of the precursor IPMN from which these lesions arise. The authors investigate the clinicopathological characteristics and the impact on survival of both the invasive component and its background IPMN. Design and patients: The study cohort comprised 61 patients with invasive IPMN (study group) and 570 patients with pancreatic ductal adenocarcinoma (PDAC, control group) resected at a single institution. Multivariate analyses were performed using a stage-matched Cox proportional hazard model. Results: The histology of invasive components of the IPMN cohort was tubular in 38 (62%), colloid in 16 (26%), and oncocytic in seven (12%). Compared with PDAC, invasive IPMNs were associated with a lower incidence of adverse pathological features and improved mortality bymultivariate analysis (HR 0.58; 95%CI 0.39 to 0.86). In subtype analysis, this favourable outcome remained only for colloid and oncocytic carcinomas, while tubular adenocarcinoma was associated with worse overall survival, not significantly different from that of PDAC (HR 0.85; 95% CI 0.53 to 1.36). Colloid and oncocytic carcinomas arose only from intestinaland oncocytic-type IPMNs, respectively, and were mostly of the main-duct type, whereas tubular adenocarcinomas primarily originated in the gastric background, which was often associated with branch-duct IPMN. Overall survival of patients with invasive adenocarcinomas arising from gastric-type IPMN was significantly worse than that of patients with non-gastric-type IPMN (p=0.016). Conclusions: Tubular, colloid and oncocytic invasive IPMNs have varying prognosis, and arise from different epithelial subtypes. Colloid and oncocytic types have markedly improved biology, whereas the tubular type has a course that resembles PDAC. Analysis of these subtypes indicates that the background epithelium plays an equally, if not more, important role in defining the biology and prognosis of invasive IPMNs.

Original languageEnglish (US)
Pages (from-to)1712-1720
Number of pages9
JournalGut
Volume60
Issue number12
DOIs
StatePublished - Dec 1 2011

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Neoplasms
Colloids
Adenocarcinoma
Mucinous Adenocarcinoma
Survival
Stomach
Proportional Hazards Models
Histology
Cohort Studies
Multivariate Analysis
Epithelium
Control Groups
Mortality
Incidence

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Mino-Kenudson, M., Fernández-del Castillo, C., Baba, Y., Valsangkar, N. P., Liss, A. S., Hsu, M., ... Thayer, S. P. (2011). Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes. Gut, 60(12), 1712-1720. https://doi.org/10.1136/gut.2010.232272

Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes. / Mino-Kenudson, Mari; Fernández-del Castillo, Carlos; Baba, Yoshifumi; Valsangkar, Nakul P.; Liss, Andrew S.; Hsu, Maylee; Correa-Gallego, Camilo; Ingkakul, Thun; Johnston, Rocio Perez; Turner, Brian G.; Androutsopoulos, Vasiliki; Deshpande, Vikram; McGrath, Deborah; Sahani, Dushyant V.; Brugge, William R.; Ogino, Shuji; Pitman, Martha B.; Warshaw, Andrew L.; Thayer, Sarah P.

In: Gut, Vol. 60, No. 12, 01.12.2011, p. 1712-1720.

Research output: Contribution to journalArticle

Mino-Kenudson, M, Fernández-del Castillo, C, Baba, Y, Valsangkar, NP, Liss, AS, Hsu, M, Correa-Gallego, C, Ingkakul, T, Johnston, RP, Turner, BG, Androutsopoulos, V, Deshpande, V, McGrath, D, Sahani, DV, Brugge, WR, Ogino, S, Pitman, MB, Warshaw, AL & Thayer, SP 2011, 'Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes', Gut, vol. 60, no. 12, pp. 1712-1720. https://doi.org/10.1136/gut.2010.232272
Mino-Kenudson M, Fernández-del Castillo C, Baba Y, Valsangkar NP, Liss AS, Hsu M et al. Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes. Gut. 2011 Dec 1;60(12):1712-1720. https://doi.org/10.1136/gut.2010.232272
Mino-Kenudson, Mari ; Fernández-del Castillo, Carlos ; Baba, Yoshifumi ; Valsangkar, Nakul P. ; Liss, Andrew S. ; Hsu, Maylee ; Correa-Gallego, Camilo ; Ingkakul, Thun ; Johnston, Rocio Perez ; Turner, Brian G. ; Androutsopoulos, Vasiliki ; Deshpande, Vikram ; McGrath, Deborah ; Sahani, Dushyant V. ; Brugge, William R. ; Ogino, Shuji ; Pitman, Martha B. ; Warshaw, Andrew L. ; Thayer, Sarah P. / Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes. In: Gut. 2011 ; Vol. 60, No. 12. pp. 1712-1720.
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abstract = "Objective: Invasive cancers arising from intraductal papillary mucinous neoplasm (IPMN) are recognised as a morphologically and biologically heterogeneous group of neoplasms. Less is known about the epithelial subtypes of the precursor IPMN from which these lesions arise. The authors investigate the clinicopathological characteristics and the impact on survival of both the invasive component and its background IPMN. Design and patients: The study cohort comprised 61 patients with invasive IPMN (study group) and 570 patients with pancreatic ductal adenocarcinoma (PDAC, control group) resected at a single institution. Multivariate analyses were performed using a stage-matched Cox proportional hazard model. Results: The histology of invasive components of the IPMN cohort was tubular in 38 (62{\%}), colloid in 16 (26{\%}), and oncocytic in seven (12{\%}). Compared with PDAC, invasive IPMNs were associated with a lower incidence of adverse pathological features and improved mortality bymultivariate analysis (HR 0.58; 95{\%}CI 0.39 to 0.86). In subtype analysis, this favourable outcome remained only for colloid and oncocytic carcinomas, while tubular adenocarcinoma was associated with worse overall survival, not significantly different from that of PDAC (HR 0.85; 95{\%} CI 0.53 to 1.36). Colloid and oncocytic carcinomas arose only from intestinaland oncocytic-type IPMNs, respectively, and were mostly of the main-duct type, whereas tubular adenocarcinomas primarily originated in the gastric background, which was often associated with branch-duct IPMN. Overall survival of patients with invasive adenocarcinomas arising from gastric-type IPMN was significantly worse than that of patients with non-gastric-type IPMN (p=0.016). Conclusions: Tubular, colloid and oncocytic invasive IPMNs have varying prognosis, and arise from different epithelial subtypes. Colloid and oncocytic types have markedly improved biology, whereas the tubular type has a course that resembles PDAC. Analysis of these subtypes indicates that the background epithelium plays an equally, if not more, important role in defining the biology and prognosis of invasive IPMNs.",
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T1 - Prognosis of invasive intraductal papillary mucinous neoplasm depends on histological and precursor epithelial subtypes

AU - Mino-Kenudson, Mari

AU - Fernández-del Castillo, Carlos

AU - Baba, Yoshifumi

AU - Valsangkar, Nakul P.

AU - Liss, Andrew S.

AU - Hsu, Maylee

AU - Correa-Gallego, Camilo

AU - Ingkakul, Thun

AU - Johnston, Rocio Perez

AU - Turner, Brian G.

AU - Androutsopoulos, Vasiliki

AU - Deshpande, Vikram

AU - McGrath, Deborah

AU - Sahani, Dushyant V.

AU - Brugge, William R.

AU - Ogino, Shuji

AU - Pitman, Martha B.

AU - Warshaw, Andrew L.

AU - Thayer, Sarah P.

PY - 2011/12/1

Y1 - 2011/12/1

N2 - Objective: Invasive cancers arising from intraductal papillary mucinous neoplasm (IPMN) are recognised as a morphologically and biologically heterogeneous group of neoplasms. Less is known about the epithelial subtypes of the precursor IPMN from which these lesions arise. The authors investigate the clinicopathological characteristics and the impact on survival of both the invasive component and its background IPMN. Design and patients: The study cohort comprised 61 patients with invasive IPMN (study group) and 570 patients with pancreatic ductal adenocarcinoma (PDAC, control group) resected at a single institution. Multivariate analyses were performed using a stage-matched Cox proportional hazard model. Results: The histology of invasive components of the IPMN cohort was tubular in 38 (62%), colloid in 16 (26%), and oncocytic in seven (12%). Compared with PDAC, invasive IPMNs were associated with a lower incidence of adverse pathological features and improved mortality bymultivariate analysis (HR 0.58; 95%CI 0.39 to 0.86). In subtype analysis, this favourable outcome remained only for colloid and oncocytic carcinomas, while tubular adenocarcinoma was associated with worse overall survival, not significantly different from that of PDAC (HR 0.85; 95% CI 0.53 to 1.36). Colloid and oncocytic carcinomas arose only from intestinaland oncocytic-type IPMNs, respectively, and were mostly of the main-duct type, whereas tubular adenocarcinomas primarily originated in the gastric background, which was often associated with branch-duct IPMN. Overall survival of patients with invasive adenocarcinomas arising from gastric-type IPMN was significantly worse than that of patients with non-gastric-type IPMN (p=0.016). Conclusions: Tubular, colloid and oncocytic invasive IPMNs have varying prognosis, and arise from different epithelial subtypes. Colloid and oncocytic types have markedly improved biology, whereas the tubular type has a course that resembles PDAC. Analysis of these subtypes indicates that the background epithelium plays an equally, if not more, important role in defining the biology and prognosis of invasive IPMNs.

AB - Objective: Invasive cancers arising from intraductal papillary mucinous neoplasm (IPMN) are recognised as a morphologically and biologically heterogeneous group of neoplasms. Less is known about the epithelial subtypes of the precursor IPMN from which these lesions arise. The authors investigate the clinicopathological characteristics and the impact on survival of both the invasive component and its background IPMN. Design and patients: The study cohort comprised 61 patients with invasive IPMN (study group) and 570 patients with pancreatic ductal adenocarcinoma (PDAC, control group) resected at a single institution. Multivariate analyses were performed using a stage-matched Cox proportional hazard model. Results: The histology of invasive components of the IPMN cohort was tubular in 38 (62%), colloid in 16 (26%), and oncocytic in seven (12%). Compared with PDAC, invasive IPMNs were associated with a lower incidence of adverse pathological features and improved mortality bymultivariate analysis (HR 0.58; 95%CI 0.39 to 0.86). In subtype analysis, this favourable outcome remained only for colloid and oncocytic carcinomas, while tubular adenocarcinoma was associated with worse overall survival, not significantly different from that of PDAC (HR 0.85; 95% CI 0.53 to 1.36). Colloid and oncocytic carcinomas arose only from intestinaland oncocytic-type IPMNs, respectively, and were mostly of the main-duct type, whereas tubular adenocarcinomas primarily originated in the gastric background, which was often associated with branch-duct IPMN. Overall survival of patients with invasive adenocarcinomas arising from gastric-type IPMN was significantly worse than that of patients with non-gastric-type IPMN (p=0.016). Conclusions: Tubular, colloid and oncocytic invasive IPMNs have varying prognosis, and arise from different epithelial subtypes. Colloid and oncocytic types have markedly improved biology, whereas the tubular type has a course that resembles PDAC. Analysis of these subtypes indicates that the background epithelium plays an equally, if not more, important role in defining the biology and prognosis of invasive IPMNs.

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