Perioperative Modified FOLFIRINOX for Resectable Pancreatic Cancer: A Nonrandomized Controlled Trial

Authors

Michael Cecchini, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Ronald R. Salem, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut.
Marie Robert, Department of Pathology, Yale University School of Medicine, New Haven, Connecticut.
Suzanne Czerniak, Department of Radiology, Yale University School of Medicine, New Haven, Connecticut.
Ondrej Blaha, Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut.
Daniel Zelterman, Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut.
Moein Rajaei, Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut.
Jeffrey P. Townsend, Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut.
Guoping Cai, Department of Pathology, Yale University School of Medicine, New Haven, Connecticut.
Sumedha Chowdhury, Department of Therapeutic Radiology, Yale School of Public Health, New Haven, Connecticut.
Deanne Yugawa, Department of Pathology, Yale University School of Medicine, New Haven, Connecticut.
Robert Tseng, Department of Therapeutic Radiology, Yale School of Public Health, New Haven, Connecticut.
Carlos Mejia Arbelaez, Department of Pathology, Yale University School of Medicine, New Haven, Connecticut.
Jingjing Jiao, Department of Pathology, Yale University School of Medicine, New Haven, Connecticut.
Kenneth Shroyer, Department of Pathology, Renaissance School of Medicine, Stony Brook University, Stony Brook, New York.
Jaykumar Thumar, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Jeremy Kortmansky, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Wajih Zaheer, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Neal Fischbach, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Justin Persico, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Stacey Stein, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Sajid A. Khan, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut.
Charles Cha, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut.
Kevin G. Billingsley, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut.
John W. Kunstman, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut.
Kimberly L. Johung, Department of Therapeutic Radiology, Yale School of Public Health, New Haven, Connecticut.
Christina Wiess, Yale Cancer Center, Yale University School of Medicine, New Haven, Connecticut.
Mandar D. Muzumdar, Department of Internal Medicine (Medical Oncology), Yale University School of Medicine, New Haven, Connecticut.
Erik Spickard, Natera Inc, Austin, Texas.
Vasily N. Aushev, Natera Inc, Austin, Texas.
George Laliotis, Natera Inc, Austin, Texas.
Adham Jurdi, Natera Inc, Austin, Texas.

Document Type

Article

Publication Title

JAMA oncology

Abstract

IMPORTANCE: Pancreatic ductal adenocarcinoma (PDAC) is an aggressive malignant tumor, and durable disease control is rare with the current standard of care, even for patients who undergo surgical resection. OBJECTIVE: To assess whether neoadjuvant modified 5-fluorouracil, leucovorin, oxaliplatin, and irinotecan (mFOLFIRINOX) leads to early control of micrometastasis and improves survival. DESIGN, SETTING, AND PARTICIPANTS: This open-label, single-arm, phase 2 nonrandomized controlled trial for resectable PDAC was conducted at the Yale Smilow Cancer Hospital from April 3, 2014, to August 16, 2021. Pancreatic protocol computed tomography was performed at diagnosis to assess surgical candidacy. Data were analyzed from January to July 2023. INTERVENTIONS: Patients received 6 cycles of neoadjuvant mFOLFIRINOX before surgery and 6 cycles of adjuvant mFOLFIRINOX. Whole blood was collected and processed to stored plasma for analysis of circulating tumor DNA (ctDNA) levels. Tumors were evaluated for treatment response and keratin 17 (K17) expression. MAIN OUTCOMES AND MEASURES: The primary end point was 12-month progression-free survival (PFS) rate. Additional end points included overall survival (OS), ctDNA level, tumor molecular features, and K17 tumor levels. Survival curves were summarized using Kaplan-Meier estimator. RESULTS: Of 46 patients who received mFOLFIRINOX, 31 (67%) were male, and the median (range) age was 65 (46-80) years. A total of 37 (80%) completed 6 preoperative cycles and 33 (72%) underwent surgery. A total of 27 patients (59%) underwent resection per protocol (25 with R0 disease and 2 with R1 disease); metastatic or unresectable disease was identified in 6 patients during exploration. Ten patients underwent surgery off protocol. The 12-month PFS was 67% (90% CI, 56.9-100); the median PFS and OS were 16.6 months (95% CI, 13.3-40.6) and 37.2 months (95% CI, 17.5-not reached), respectively. Baseline ctDNA levels were detected in 16 of 22 patients (73%) and in 3 of 17 (18%) after 6 cycles of mFOLFIRINOX. Those with detectable ctDNA levels 4 weeks postresection had worse PFS (hazard ratio [HR], 34.0; 95% CI, 2.6-4758.6; P = .006) and OS (HR, 11.7; 95% CI, 1.5-129.9; P = .02) compared with those with undetectable levels. Patients with high K17 expression had nonsignificantly worse PFS (HR, 2.7; 95% CI, 0.7-10.9; P = .09) and OS (HR, 3.2; 95% CI, 0.8-13.6; P = .07). CONCLUSIONS AND RELEVANCE: This nonrandomized controlled trial met its primary end point, and perioperative mFOLFIRINOX warrants further evaluation in randomized clinical trials. Postoperative ctDNA positivity was strongly associated with recurrence. K17 and ctDNA are promising biomarkers that require additional validation in future prospective studies. TRIAL REGISTRATION: ClinicalTrials.gov Identifier: NCT02047474.

First Page

1027

Last Page

1035

DOI

10.1001/jamaoncol.2024.1575

Publication Date

8-1-2024

Identifier

38900452 (pubmed); PMC11190830 (pmc); 10.1001/jamaoncol.2024.1575 (doi); 2820217 (pii)

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