Risk of Neoplastic Progression in Individuals at High Risk for Pancreatic Cancer Undergoing Long-term Surveillance

Marcia Canto, Jose Alejandro Almario, Richard D. Schulick, Charles J. Yeo, Alison Klein, Amanda Blackford, Eun Shin, Abanti Sanyal, Gayane Yenokyan, Anne Marie O'Broin-Lennon, Ihab R Kamel, Elliot K Fishman, Christopher Wolfgang, Matthew J Weiss, Ralph H Hruban, Michael S Goggins

Research output: Contribution to journalArticle

Abstract

Background & Aims: Screening of individuals who have a high risk of pancreatic ductal adenocarcinoma (PDAC), because of genetic factors, frequently leads to identification of pancreatic lesions. We investigated the incidence of PDAC and risk factors for neoplastic progression in individuals at high risk for PDAC enrolled in a long-term screening study. Methods: We analyzed data from 354 individuals at high risk for PDAC (based on genetic factors of family history), enrolled in Cancer of the Pancreas Screening cohort studies at tertiary care academic centers from 1998 through 2014 (median follow-up time, 5.6 years). All subjects were evaluated at study entry (baseline) by endoscopic ultrasonography and underwent surveillance with endoscopic ultrasonography, magnetic resonance imaging, and/or computed tomography. The primary endpoint was the cumulative incidence of PDAC, pancreatic intraepithelial neoplasia grade 3, or intraductal papillary mucinous neoplasm with high-grade dysplasia (HGD) after baseline. We performed multivariate Cox regression and Kaplan-Meier analyses. Results: During the follow-up period, pancreatic lesions with worrisome features (solid mass, multiple cysts, cyst size > 3 cm, thickened/enhancing walls, mural nodule, dilated main pancreatic duct > 5 mm, or abrupt change in duct caliber) or rapid cyst growth (>4 mm/year) were detected in 68 patients (19%). Overall, 24 of 354 patients (7%) had neoplastic progression (14 PDACs and 10 HGDs) over a 16-year period; the rate of progression was 1.6%/year, and 93% had detectable lesions with worrisome features before diagnosis of the PDAC or HGD. Nine of the 10 PDACs detected during routine surveillance were resectable; a significantly higher proportion of patients with resectable PDACs survived 3 years (85%) compared with the 4 subjects with symptomatic, unresectable PDACs (25%), which developed outside surveillance (log rank P <.0001). Neoplastic progression occurred at a median age of 67 years; the median time from baseline screening until PDAC diagnosis was 4.8 years (interquartile range, 1.6–6.9 years). Conclusions: In a long-term (16-year) follow-up study of individuals at high-risk for PDAC, we found most PDACs detected during surveillance (9/10) to be resectable, and 85% of these patients survived for 3 years. We identified radiologic features associated with neoplastic progression.

Original languageEnglish (US)
Pages (from-to)740-751.e2
JournalGastroenterology
Volume155
Issue number3
DOIs
StatePublished - Sep 1 2018

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Pancreatic Neoplasms
Adenocarcinoma
Cysts
Endosonography
Pancreatic Ducts
Incidence
Kaplan-Meier Estimate
Early Detection of Cancer
Tertiary Care Centers
Neoplasms
Cohort Studies
Tomography
Magnetic Resonance Imaging
Growth

Keywords

  • Early Detection
  • Familial Pancreatic Cancer
  • IPMN
  • PanIN-3

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Risk of Neoplastic Progression in Individuals at High Risk for Pancreatic Cancer Undergoing Long-term Surveillance. / Canto, Marcia; Almario, Jose Alejandro; Schulick, Richard D.; Yeo, Charles J.; Klein, Alison; Blackford, Amanda; Shin, Eun; Sanyal, Abanti; Yenokyan, Gayane; O'Broin-Lennon, Anne Marie; Kamel, Ihab R; Fishman, Elliot K; Wolfgang, Christopher; Weiss, Matthew J; Hruban, Ralph H; Goggins, Michael S.

In: Gastroenterology, Vol. 155, No. 3, 01.09.2018, p. 740-751.e2.

Research output: Contribution to journalArticle

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title = "Risk of Neoplastic Progression in Individuals at High Risk for Pancreatic Cancer Undergoing Long-term Surveillance",
abstract = "Background & Aims: Screening of individuals who have a high risk of pancreatic ductal adenocarcinoma (PDAC), because of genetic factors, frequently leads to identification of pancreatic lesions. We investigated the incidence of PDAC and risk factors for neoplastic progression in individuals at high risk for PDAC enrolled in a long-term screening study. Methods: We analyzed data from 354 individuals at high risk for PDAC (based on genetic factors of family history), enrolled in Cancer of the Pancreas Screening cohort studies at tertiary care academic centers from 1998 through 2014 (median follow-up time, 5.6 years). All subjects were evaluated at study entry (baseline) by endoscopic ultrasonography and underwent surveillance with endoscopic ultrasonography, magnetic resonance imaging, and/or computed tomography. The primary endpoint was the cumulative incidence of PDAC, pancreatic intraepithelial neoplasia grade 3, or intraductal papillary mucinous neoplasm with high-grade dysplasia (HGD) after baseline. We performed multivariate Cox regression and Kaplan-Meier analyses. Results: During the follow-up period, pancreatic lesions with worrisome features (solid mass, multiple cysts, cyst size > 3 cm, thickened/enhancing walls, mural nodule, dilated main pancreatic duct > 5 mm, or abrupt change in duct caliber) or rapid cyst growth (>4 mm/year) were detected in 68 patients (19{\%}). Overall, 24 of 354 patients (7{\%}) had neoplastic progression (14 PDACs and 10 HGDs) over a 16-year period; the rate of progression was 1.6{\%}/year, and 93{\%} had detectable lesions with worrisome features before diagnosis of the PDAC or HGD. Nine of the 10 PDACs detected during routine surveillance were resectable; a significantly higher proportion of patients with resectable PDACs survived 3 years (85{\%}) compared with the 4 subjects with symptomatic, unresectable PDACs (25{\%}), which developed outside surveillance (log rank P <.0001). Neoplastic progression occurred at a median age of 67 years; the median time from baseline screening until PDAC diagnosis was 4.8 years (interquartile range, 1.6–6.9 years). Conclusions: In a long-term (16-year) follow-up study of individuals at high-risk for PDAC, we found most PDACs detected during surveillance (9/10) to be resectable, and 85{\%} of these patients survived for 3 years. We identified radiologic features associated with neoplastic progression.",
keywords = "Early Detection, Familial Pancreatic Cancer, IPMN, PanIN-3",
author = "Marcia Canto and Almario, {Jose Alejandro} and Schulick, {Richard D.} and Yeo, {Charles J.} and Alison Klein and Amanda Blackford and Eun Shin and Abanti Sanyal and Gayane Yenokyan and O'Broin-Lennon, {Anne Marie} and Kamel, {Ihab R} and Fishman, {Elliot K} and Christopher Wolfgang and Weiss, {Matthew J} and Hruban, {Ralph H} and Goggins, {Michael S}",
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T1 - Risk of Neoplastic Progression in Individuals at High Risk for Pancreatic Cancer Undergoing Long-term Surveillance

AU - Canto, Marcia

AU - Almario, Jose Alejandro

AU - Schulick, Richard D.

AU - Yeo, Charles J.

AU - Klein, Alison

AU - Blackford, Amanda

AU - Shin, Eun

AU - Sanyal, Abanti

AU - Yenokyan, Gayane

AU - O'Broin-Lennon, Anne Marie

AU - Kamel, Ihab R

AU - Fishman, Elliot K

AU - Wolfgang, Christopher

AU - Weiss, Matthew J

AU - Hruban, Ralph H

AU - Goggins, Michael S

PY - 2018/9/1

Y1 - 2018/9/1

N2 - Background & Aims: Screening of individuals who have a high risk of pancreatic ductal adenocarcinoma (PDAC), because of genetic factors, frequently leads to identification of pancreatic lesions. We investigated the incidence of PDAC and risk factors for neoplastic progression in individuals at high risk for PDAC enrolled in a long-term screening study. Methods: We analyzed data from 354 individuals at high risk for PDAC (based on genetic factors of family history), enrolled in Cancer of the Pancreas Screening cohort studies at tertiary care academic centers from 1998 through 2014 (median follow-up time, 5.6 years). All subjects were evaluated at study entry (baseline) by endoscopic ultrasonography and underwent surveillance with endoscopic ultrasonography, magnetic resonance imaging, and/or computed tomography. The primary endpoint was the cumulative incidence of PDAC, pancreatic intraepithelial neoplasia grade 3, or intraductal papillary mucinous neoplasm with high-grade dysplasia (HGD) after baseline. We performed multivariate Cox regression and Kaplan-Meier analyses. Results: During the follow-up period, pancreatic lesions with worrisome features (solid mass, multiple cysts, cyst size > 3 cm, thickened/enhancing walls, mural nodule, dilated main pancreatic duct > 5 mm, or abrupt change in duct caliber) or rapid cyst growth (>4 mm/year) were detected in 68 patients (19%). Overall, 24 of 354 patients (7%) had neoplastic progression (14 PDACs and 10 HGDs) over a 16-year period; the rate of progression was 1.6%/year, and 93% had detectable lesions with worrisome features before diagnosis of the PDAC or HGD. Nine of the 10 PDACs detected during routine surveillance were resectable; a significantly higher proportion of patients with resectable PDACs survived 3 years (85%) compared with the 4 subjects with symptomatic, unresectable PDACs (25%), which developed outside surveillance (log rank P <.0001). Neoplastic progression occurred at a median age of 67 years; the median time from baseline screening until PDAC diagnosis was 4.8 years (interquartile range, 1.6–6.9 years). Conclusions: In a long-term (16-year) follow-up study of individuals at high-risk for PDAC, we found most PDACs detected during surveillance (9/10) to be resectable, and 85% of these patients survived for 3 years. We identified radiologic features associated with neoplastic progression.

AB - Background & Aims: Screening of individuals who have a high risk of pancreatic ductal adenocarcinoma (PDAC), because of genetic factors, frequently leads to identification of pancreatic lesions. We investigated the incidence of PDAC and risk factors for neoplastic progression in individuals at high risk for PDAC enrolled in a long-term screening study. Methods: We analyzed data from 354 individuals at high risk for PDAC (based on genetic factors of family history), enrolled in Cancer of the Pancreas Screening cohort studies at tertiary care academic centers from 1998 through 2014 (median follow-up time, 5.6 years). All subjects were evaluated at study entry (baseline) by endoscopic ultrasonography and underwent surveillance with endoscopic ultrasonography, magnetic resonance imaging, and/or computed tomography. The primary endpoint was the cumulative incidence of PDAC, pancreatic intraepithelial neoplasia grade 3, or intraductal papillary mucinous neoplasm with high-grade dysplasia (HGD) after baseline. We performed multivariate Cox regression and Kaplan-Meier analyses. Results: During the follow-up period, pancreatic lesions with worrisome features (solid mass, multiple cysts, cyst size > 3 cm, thickened/enhancing walls, mural nodule, dilated main pancreatic duct > 5 mm, or abrupt change in duct caliber) or rapid cyst growth (>4 mm/year) were detected in 68 patients (19%). Overall, 24 of 354 patients (7%) had neoplastic progression (14 PDACs and 10 HGDs) over a 16-year period; the rate of progression was 1.6%/year, and 93% had detectable lesions with worrisome features before diagnosis of the PDAC or HGD. Nine of the 10 PDACs detected during routine surveillance were resectable; a significantly higher proportion of patients with resectable PDACs survived 3 years (85%) compared with the 4 subjects with symptomatic, unresectable PDACs (25%), which developed outside surveillance (log rank P <.0001). Neoplastic progression occurred at a median age of 67 years; the median time from baseline screening until PDAC diagnosis was 4.8 years (interquartile range, 1.6–6.9 years). Conclusions: In a long-term (16-year) follow-up study of individuals at high-risk for PDAC, we found most PDACs detected during surveillance (9/10) to be resectable, and 85% of these patients survived for 3 years. We identified radiologic features associated with neoplastic progression.

KW - Early Detection

KW - Familial Pancreatic Cancer

KW - IPMN

KW - PanIN-3

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