FOLFIRINOX or Gemcitabine-based Chemotherapy for Borderline Resectable and Locally Advanced Pancreatic Cancer: A Multi-institutional, Patient-Level, Meta-analysis and Systematic Review

Eshmuminov, Dilmurodjon; Aminjonov, Botirjon; Palm, Russell F.; Malleo, Giuseppe; Schmocker, Ryan K.; Abdallah, Raëf; Yoo, Changhoon; Shaib, Walid L; Schneider, Marcel André; Rangelova, Elena B; Choi, Yoo Jin; Kim, Hongbeom; Rose, J. Bart; Patel, Sameer; Wilson, Gregory C; Maloney, Sarah; Timmermann, Lea; Sahora, Klaus; Rössler, Fabian; Lopez-Lopez, Victor; Boyer, Emanuel F; Maggino, Laura; Malinka, Thomas; Park, Jeong Youp; Katz, Matthew H G; Prakash, Laura; Ahmad, Syed A.; Helton, Scott; Jang, Jin-Young; Hoffe, Sarah E; Salvia, Roberto; Taieb, Julien; HE, Jin; Clavien, Pierre-Alain; Held, Ulrike; Lehmann, Kuno

doi:10.1245/s10434-023-13353-2

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FOLFIRINOX or Gemcitabine-based Chemotherapy for Borderline Resectable and Locally Advanced Pancreatic Cancer: A Multi-institutional, Patient-Level, Meta-analysis and Systematic Review

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Author(s): Dilmurodjon Eshmuminov , MD ¹ , Botirjon Aminjonov , MD ¹ , Russell F. Palm , MD ² , Giuseppe Malleo , MD ³ , Ryan K. Schmocker , MD ⁴ ^, ⁵ , Raëf Abdallah , MD ⁶ , Changhoon Yoo , MD ⁷ , Walid L. Shaib , MD ⁸ , Marcel André Schneider , MD, PhD ¹ , Elena Rangelova , MD ⁹ ^, ¹⁰ , Yoo Jin Choi , MD ¹¹ , Hongbeom Kim , MD ¹¹ , J. Bart Rose , MD ¹² , Sameer Patel , MD ¹³ , Gregory C. Wilson , MD ¹³ , Sarah Maloney , MD ¹⁴ , Lea Timmermann , MD ¹⁵ , Klaus Sahora , MD ¹⁶ , Fabian Rössler , MD ¹ , Víctor Lopez-Lopez , MD ¹⁷ , Emanuel Boyer , MD ¹⁸ , Laura Maggino , MD ³ , Thomas Malinka , MD ¹⁵ , Jeong Youp Park , MD ¹⁹ , Matthew H. G. Katz , MD ²⁰ , Laura Prakash , MD ²⁰ , Syed A. Ahmad , MD ¹³ , Scott Helton , MD ²¹ , Jin-Young Jang , MD ¹¹ , Sarah E. Hoffe , MD ² , Roberto Salvia , MD ³ , Julien Taieb , MD ⁶ , Jin He , MD ⁴ , Pierre-Alain Clavien , MD ¹ , Ulrike Held ²² , Kuno Lehmann , MD, PhD ¹ ^,

Publication date (Electronic): 5 April 2023

Journal: Annals of Surgical Oncology

Publisher: Springer International Publishing

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Abstract

Background

Pancreatic cancer often presents as locally advanced (LAPC) or borderline resectable (BRPC). Neoadjuvant systemic therapy is recommended as initial treatment. It is currently unclear what chemotherapy should be preferred for patients with BRPC or LAPC.

Methods

We performed a systematic review and multi-institutional meta-analysis of patient-level data regarding the use of initial systemic therapy for BRPC and LAPC. Outcomes were reported separately for tumor entity and by chemotherapy regimen including FOLFIRINOX (FIO) or gemcitabine-based.

Results

A total of 23 studies comprising 2930 patients were analyzed for overall survival (OS) calculated from the beginning of systemic treatment. OS for patients with BRPC was 22.0 months with FIO, 16.9 months with gemcitabine/nab-paclitaxel (Gem/nab), 21.6 months with gemcitabine/cisplatin or oxaliplatin or docetaxel or capecitabine (GemX), and 10 months with gemcitabine monotherapy (Gem-mono) ( p < 0.0001). In patients with LAPC, OS also was higher with FIO (17.1 months) compared with Gem/nab (12.5 months), GemX (12.3 months), and Gem-mono (9.4 months; p < 0.0001). This difference was driven by the patients who did not undergo surgery, where FIO was superior to other regimens. The resection rates for patients with BRPC were 0.55 for gemcitabine-based chemotherapy and 0.53 with FIO. In patients with LAPC, resection rates were 0.19 with Gemcitabine and 0.28 with FIO. In resected patients, OS for patients with BRPC was 32.9 months with FIO and not different compared to Gem/nab, (28.6 months, p = 0.285), GemX (38.8 months, p = 0.1), or Gem-mono (23.1 months, p = 0.083). A similar trend was observed in resected patients converted from LAPC.

Conclusions

In patients with BRPC or LAPC, primary treatment with FOLFIRINOX compared with Gemcitabine-based chemotherapy appears to provide a survival benefit for patients that are ultimately unresectable. For patients that undergo surgical resection, outcomes are similar between GEM+ and FOLFIRINOX when delivered in the neoadjuvant setting.

Supplementary Information

The online version contains supplementary material available at 10.1245/s10434-023-13353-2.

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Most cited references 44

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The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration

Alessandro Liberati, Douglas G. Altman, Jennifer Tetzlaff … (2010)

Systematic reviews and meta-analyses are essential to summarise evidence relating to efficacy and safety of healthcare interventions accurately and reliably. The clarity and transparency of these reports, however, are not optimal. Poor reporting of systematic reviews diminishes their value to clinicians, policy makers, and other users. Since the development of the QUOROM (quality of reporting of meta-analysis) statement—a reporting guideline published in 1999—there have been several conceptual, methodological, and practical advances regarding the conduct and reporting of systematic reviews and meta-analyses. Also, reviews of published systematic reviews have found that key information about these studies is often poorly reported. Realising these issues, an international group that included experienced authors and methodologists developed PRISMA (preferred reporting items for systematic reviews and meta-analyses) as an evolution of the original QUOROM guideline for systematic reviews and meta-analyses of evaluations of health care interventions. The PRISMA statement consists of a 27-item checklist and a four-phase flow diagram. The checklist includes items deemed essential for transparent reporting of a systematic review. In this explanation and elaboration document, we explain the meaning and rationale for each checklist item. For each item, we include an example of good reporting and, where possible, references to relevant empirical studies and methodological literature. The PRISMA statement, this document, and the associated website (www.prisma-statement.org/) should be helpful resources to improve reporting of systematic reviews and meta-analyses.

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Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States.

Lola Rahib, Benjamin D Smith, Rhonda Aizenberg … (2014)

Cancer incidence and deaths in the United States were projected for the most common cancer types for the years 2020 and 2030 based on changing demographics and the average annual percentage changes in incidence and death rates. Breast, prostate, and lung cancers will remain the top cancer diagnoses throughout this time, but thyroid cancer will replace colorectal cancer as the fourth leading cancer diagnosis by 2030, and melanoma and uterine cancer will become the fifth and sixth most common cancers, respectively. Lung cancer is projected to remain the top cancer killer throughout this time period. However, pancreas and liver cancers are projected to surpass breast, prostate, and colorectal cancers to become the second and third leading causes of cancer-related death by 2030, respectively. Advances in screening, prevention, and treatment can change cancer incidence and/or death rates, but it will require a concerted effort by the research and healthcare communities now to effect a substantial change for the future. ©2014 American Association for Cancer Research.

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FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer.

Thierry Conroy, Françoise Desseigne, Marc Ychou … (2011)

Data are lacking on the efficacy and safety of a combination chemotherapy regimen consisting of oxaliplatin, irinotecan, fluorouracil, and leucovorin (FOLFIRINOX) as compared with gemcitabine as first-line therapy in patients with metastatic pancreatic cancer. We randomly assigned 342 patients with an Eastern Cooperative Oncology Group performance status score of 0 or 1 (on a scale of 0 to 5, with higher scores indicating a greater severity of illness) to receive FOLFIRINOX (oxaliplatin, 85 mg per square meter of body-surface area; irinotecan, 180 mg per square meter; leucovorin, 400 mg per square meter; and fluorouracil, 400 mg per square meter given as a bolus followed by 2400 mg per square meter given as a 46-hour continuous infusion, every 2 weeks) or gemcitabine at a dose of 1000 mg per square meter weekly for 7 of 8 weeks and then weekly for 3 of 4 weeks. Six months of chemotherapy were recommended in both groups in patients who had a response. The primary end point was overall survival. The median overall survival was 11.1 months in the FOLFIRINOX group as compared with 6.8 months in the gemcitabine group (hazard ratio for death, 0.57; 95% confidence interval [CI], 0.45 to 0.73; P<0.001). Median progression-free survival was 6.4 months in the FOLFIRINOX group and 3.3 months in the gemcitabine group (hazard ratio for disease progression, 0.47; 95% CI, 0.37 to 0.59; P<0.001). The objective response rate was 31.6% in the FOLFIRINOX group versus 9.4% in the gemcitabine group (P<0.001). More adverse events were noted in the FOLFIRINOX group; 5.4% of patients in this group had febrile neutropenia. At 6 months, 31% of the patients in the FOLFIRINOX group had a definitive degradation of the quality of life versus 66% in the gemcitabine group (hazard ratio, 0.47; 95% CI, 0.30 to 0.70; P<0.001). As compared with gemcitabine, FOLFIRINOX was associated with a survival advantage and had increased toxicity. FOLFIRINOX is an option for the treatment of patients with metastatic pancreatic cancer and good performance status. (Funded by the French government and others; ClinicalTrials.gov number, NCT00112658.).

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Author and article information

Contributors

Kuno Lehmann: kuno.lehmann@usz.ch

Journal

Journal ID (nlm-ta): Ann Surg Oncol

Journal ID (iso-abbrev): Ann Surg Oncol

Title: Annals of Surgical Oncology

Publisher: Springer International Publishing (Cham )

ISSN (Print): 1068-9265

ISSN (Electronic): 1534-4681

Publication date (Electronic): 5 April 2023

Publication date PMC-release: 5 April 2023

Publication date (Print): 2023

Volume: 30

Issue: 7

Pages: 4417-4428

Affiliations

[1 ]GRID grid.412004.3, ISNI 0000 0004 0478 9977, Department of Surgery and Transplantation, , University Hospital Zurich and University of Zurich, ; Zurich, Switzerland

[2 ]GRID grid.468198.a, ISNI 0000 0000 9891 5233, Department of Radiation Oncology, , H. Lee Moffitt Cancer Center and Research Institute, ; Tampa, Florida USA

[3 ]GRID grid.5611.3, ISNI 0000 0004 1763 1124, Unit of General and Pancreatic Surgery. Department of Surgery, Dentistry, Paediatrics and Gynaecology, , University of Verona, ; Verona, Italy

[4 ]GRID grid.411935.b, ISNI 0000 0001 2192 2723, Department of Surgery, The Division of Hepatobiliary and Pancreatic Surgery, , Johns Hopkins Hospital, ; Baltimore, MD USA

[5 ]GRID grid.411461.7, ISNI 0000 0001 2315 1184, Department of Surgery, , University of Tennessee Graduate School of Medicine, ; Knoxville, TN USA

[6 ]Hepatogastroenterology and Gastrointestinal Oncology Department, Hôpital Européen Georges-Pompidou, AGEO (Association des Gastro-Enterologues Oncologues), Université de Paris, SIRIC CARPEM, Paris, France

[7 ]GRID grid.267370.7, ISNI 0000 0004 0533 4667, Department of Oncology, Asan Medical Center, , University of Ulsan College of Medicine, ; Seoul, Korea

[8 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Department of Hematology and Oncology, , Winship Cancer Institute, Emory University School of Medicine, ; Atlanta, GA USA

[9 ]GRID grid.24381.3c, ISNI 0000 0000 9241 5705, Department of Upper Gastrointestinal Diseases, , Karolinska University Hospital and Department of Clinical Science, Intervention, and Technology (CLINTEC) at Karolinska Institute, ; Stockholm, Sweden

[10 ]GRID grid.8761.8, ISNI 0000 0000 9919 9582, Department of Surgery, The Institute of Clinical Sciences, Sahlgrenska Academy, , University of Gothenburg, ; Gothenburg, Sweden

[11 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Department of Surgery, Seoul National University College of Medicine, , Seoul National University, ; 28 Yongon-dong, Chongno-gu, Seoul, 110-744 Korea

[12 ]GRID grid.265892.2, ISNI 0000000106344187, Division of Surgical Oncology, Pancreatobiliary Disease Center at UAB, , The University of Alabama at Birmingham, ; Birmingham, USA

[13 ]GRID grid.24827.3b, ISNI 0000 0001 2179 9593, Division of Surgical Oncology, Department of Surgery, , University of Cincinnati, ; Cincinnati, OH USA

[14 ]GRID grid.412703.3, ISNI 0000 0004 0587 9093, Department of Oncology, , Royal North Shore Hospital, ; Sydney, NSW Australia

[15 ]GRID grid.7468.d, ISNI 0000 0001 2248 7639, Department of Surgery, Charité – Freie Universität Berlin, , Humboldt-Universität zu Berlin and Berlin Institute of Health, ; Berlin, Germany

[16 ]GRID grid.10420.37, ISNI 0000 0001 2286 1424, Departments of Surgery and Comprehensive Cancer Center, , University of Vienna, Medical University of Vienna, ; Vienna, Austria

[17 ]GRID grid.452553.0, ISNI 0000 0004 8504 7077, Department of General, Visceral and Transplantation Surgery, Clinic and University Hospital Virgen de la Arrixaca, , IMIB-ARRIXACA, ; Murcia, Spain

[18 ]GRID grid.170693.a, ISNI 0000 0001 2353 285X, University of South Florida School of Medicine, ; Tampa, FL USA

[19 ]GRID grid.15444.30, ISNI 0000 0004 0470 5454, Division of Gastroenterology, Department of Internal Medicine, Severance Hospital, , Yonsei University College of Medicine, ; Seoul, Korea

[20 ]GRID grid.240145.6, ISNI 0000 0001 2291 4776, University of Texas MD Anderson Cancer Center, ; Houston, TX USA

[21 ]GRID grid.416879.5, ISNI 0000 0001 2219 0587, Section of General, Thoracic and Vascular Surgery, Department of Surgery, , Virginia Mason Medical Center, ; Seattle, WA USA

[22 ]GRID grid.7400.3, ISNI 0000 0004 1937 0650, Department of Biostatistics at Epidemiology, Biostatistics and Prevention Institute, , University of Zurich, ; Hirschengraben 84, 8001 Zurich, Switzerland

Article

Publisher ID: 13353

DOI: 10.1245/s10434-023-13353-2

PMC ID: 10250524

PubMed ID: 37020094

SO-VID: 54544bd9-6f77-49c9-b226-efed8e047323

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 1 November 2022

Date accepted : 1 March 2023

Funding

Funded by: University of Zurich

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Open access funding provided by University of Zurich

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ScienceOpen disciplines: Oncology & Radiotherapy

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FOLFIRINOX or Gemcitabine-based Chemotherapy for Borderline Resectable and Locally Advanced Pancreatic Cancer: A Multi-institutional, Patient-Level, Meta-analysis and Systematic Review

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Supplementary Information

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Karger: Oncology

Most cited references 44

The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration

Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States.

FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer.

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