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Meta-Analysis
. 2018 Mar 20;3(3):CD011044.
doi: 10.1002/14651858.CD011044.pub2.

Chemotherapy and radiotherapy for advanced pancreatic cancer

Venessa Chin  1 , Adnan Nagrial, Katrin Sjoquist, Chelsie A O'Connor, Lorraine Chantrill, Andrew V Biankin, Rob Jpm Scholten, Desmond Yip
Affiliations
Meta-Analysis

Chemotherapy and radiotherapy for advanced pancreatic cancer

Venessa Chin et al. Cochrane Database Syst Rev. .

Update in

Abstract

Background: Pancreatic cancer (PC) is a highly lethal disease with few effective treatment options. Over the past few decades, many anti-cancer therapies have been tested in the locally advanced and metastatic setting, with mixed results. This review attempts to synthesise all the randomised data available to help better inform patient and clinician decision-making when dealing with this difficult disease.

Objectives: To assess the effect of chemotherapy, radiotherapy or both for first-line treatment of advanced pancreatic cancer. Our primary outcome was overall survival, while secondary outcomes include progression-free survival, grade 3/4 adverse events, therapy response and quality of life.

Search methods: We searched for published and unpublished studies in CENTRAL (searched 14 June 2017), Embase (1980 to 14 June 2017), MEDLINE (1946 to 14 June 2017) and CANCERLIT (1999 to 2002) databases. We also handsearched all relevant conference abstracts published up until 14 June 2017.

Selection criteria: All randomised studies assessing overall survival outcomes in patients with advanced pancreatic ductal adenocarcinoma. Chemotherapy and radiotherapy, alone or in combination, were the eligible treatments.

Data collection and analysis: Two review authors independently analysed studies, and a third settled any disputes. We extracted data on overall survival (OS), progression-free survival (PFS), response rates, adverse events (AEs) and quality of life (QoL), and we assessed risk of bias for each study.

Main results: We included 42 studies addressing chemotherapy in 9463 patients with advanced pancreatic cancer. We did not identify any eligible studies on radiotherapy.We did not find any benefit for chemotherapy over best supportive care. However, two identified studies did not have sufficient data to be included in the analysis, and many of the chemotherapy regimens studied were outdated.Compared to gemcitabine alone, participants receiving 5FU had worse OS (HR 1.69, 95% CI 1.26 to 2.27, moderate-quality evidence), PFS (HR 1.47, 95% CI 1.12 to 1.92) and QoL. On the other hand, two studies showed FOLFIRINOX was better than gemcitabine for OS (HR 0.51 95% CI 0.43 to 0.60, moderate-quality evidence), PFS (HR 0.46, 95% CI 0.38 to 0.57) and response rates (RR 3.38, 95% CI 2.01 to 5.65), but it increased the rate of side effects. The studies evaluating CO-101, ZD9331 and exatecan did not show benefit or harm when compared with gemcitabine alone.Giving gemcitabine at a fixed dose rate improved OS (HR 0.79, 95% CI 0.66 to 0.94, high-quality evidence) but increased the rate of side effects when compared with bolus dosing.When comparing gemcitabine combinations to gemcitabine alone, gemcitabine plus platinum improved PFS (HR 0.80, 95% CI 0.68 to 0.95) and response rates (RR 1.48, 95% CI 1.11 to 1.98) but not OS (HR 0.94, 95% CI 0.81 to 1.08, low-quality evidence). The rate of side effects increased. Gemcitabine plus fluoropyrimidine improved OS (HR 0.88, 95% CI 0.81 to 0.95), PFS (HR 0.79, 95% CI 0.72 to 0.87) and response rates (RR 1.78, 95% CI 1.29 to 2.47, high-quality evidence), but it also increased side effects. Gemcitabine plus topoisomerase inhibitor did not improve survival outcomes but did increase toxicity. One study demonstrated that gemcitabine plus nab-paclitaxel improved OS (HR 0.72, 95% CI 0.62 to 0.84, high-quality evidence), PFS (HR 0.69, 95% CI 0.58 to 0.82) and response rates (RR 3.29, 95% CI 2.24 to 4.84) but increased side effects. Gemcitabine-containing multi-drug combinations (GEMOXEL or cisplatin/epirubicin/5FU/gemcitabine) improved OS (HR 0.55, 95% CI 0.39 to 0.79, low-quality evidence), PFS (HR 0.43, 95% CI 0.30 to 0.62) and QOL.We did not find any survival advantages when comparing 5FU combinations to 5FU alone.

Authors' conclusions: Combination chemotherapy has recently overtaken the long-standing gemcitabine as the standard of care. FOLFIRINOX and gemcitabine plus nab-paclitaxel are highly efficacious, but our analysis shows that other combination regimens also offer a benefit. Selection of the most appropriate chemotherapy for individual patients still remains difficult, with clinicopathological stratification remaining elusive. Biomarker development is essential to help rationalise treatment selection for patients.

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Conflict of interest statement

VC: Venessa Chin received scholarship funding from the Research and Education Foundation of the Royal Australasian College of Physicians, Pancare Australia, Sydney Catalyst, National Health and Medical Research Council, and the Garvan Institute of Medical Research for work related to this review.

AN: none known.

KS: Katrin Sjoquist received programme grant funding from the National Health and Medical Research Council for work related to this review. She has received consultancy fees, fees for expert testimony and travel support for work unrelated to this review.

CO: none known.

LC: Lorraine Chantrill is employed (part‐time) by NSW Health as a staff specialist in medical oncology and enrolled full‐time in PhD studies supported by the Australian Federal Government. She has been paid as an advisory board member in relation to chemotherapy for pancreas cancer and has been paid for formulating educational materials and presentations. She has received grants for the practice of clinical trials in pancreas and other cancers.

AB: Andew Biankin received grant funding from the Cancer Institute NSW for work related to this review. He also received consultancy fees from Celegene and Clovis Oncology for work unrelated to this review. His institution received consultancy fees from Roche for work unrelated to this review.

RS: Rob Scholten's institution has received grant funding from the Belgian Health Care Knowledge Centre for work related to this review. His institution has also received funding from the WHO and World Federation of Haemophilia for travel and consultancy unrelated to this review.

DY: Advisory Board Member, Specialised Therapeutics.

Figures

1
1
1 Study flow diagram.
2
2
Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
3
3
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
1.1
1.1. Analysis
Comparison 1 Anti‐cancer therapy versus best supportive care, Outcome 1 Overall survival.
2.1
2.1. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 1 Overall survival.
2.2
2.2. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 2 Progression‐free survival.
2.3
2.3. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 3 Degradation of QoL at 6 months.
2.4
2.4. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 4 Response rates.
2.5
2.5. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 5 Grade 3/4 anaemia.
2.6
2.6. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 6 Grade 3/4 neutropenia.
2.7
2.7. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 7 Grade 3/4 thrombocytopenia.
2.8
2.8. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 8 Grade 3/4 nausea.
2.9
2.9. Analysis
Comparison 2 Various types of chemotherapy versus gemcitabine, Outcome 9 Grade 3/4 diarrhoea.
3.1
3.1. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 1 Overall survival.
3.2
3.2. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 2 Progression‐free survival.
3.3
3.3. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 3 Response rates.
3.4
3.4. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 4 Grade 3/4 anaemia.
3.5
3.5. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 5 Grade 3/4 neutropenia.
3.6
3.6. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 6 Grade 3/4 thrombocytopenia.
3.7
3.7. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 7 Grade 3/4 nausea.
3.8
3.8. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 8 Grade 3/4 diarrhoea.
3.9
3.9. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 9 Grade 3/4 neuropathy.
3.10
3.10. Analysis
Comparison 3 Gemcitabine combinations versus gemcitabine alone, Outcome 10 Grade 3/4 fatigue.
4.1
4.1. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 1 Overall survival.
4.2
4.2. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 2 Progression‐free survival.
4.3
4.3. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 3 Response rates.
4.4
4.4. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 4 Grade 3/4 anaemia.
4.5
4.5. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 5 Grade 3/4 neutropenia.
4.6
4.6. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 6 Grade 3/4 thrombocytopenia.
4.7
4.7. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 7 Grade 3/4 fatigue.
4.8
4.8. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 8 Grade 3/4 nausea.
4.9
4.9. Analysis
Comparison 4 Fluoropyrimidine combinations versus fluoropyrimidine alone, Outcome 9 Grade 3/4 diarrhoea.
See this image and copyright information in PMC

References

References to studies included in this review

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Ueno 2013 {published data only}
    1. Ueno H, Ioka T, Ikeda M, Ohkawa S, Yanagimoto H, Boku N, et al. Randomized phase III study of gemcitabine plus S‐1, S‐1 alone, or gemcitabine alone in patients with locally advanced and metastatic pancreatic cancer in Japan and Taiwan: GEST study. Journal of Clinical Oncology 2013;31(13):1640‐8. - PubMed
Ueno 2013 – EPA study {published data only}
    1. Ueno M, Kobayashi S, Ohkawa S, Kameda R, Andou T, Sugimori K, et al. Randomized phase II study of gemcitabine monotherapy versus gemcitabine with an EPA‐enriched oral supplement in advanced pancreatic cancer. Journal of Clinical Oncology 2013;31:e15109.
Viret 2004 {published data only}
    1. Viret F, Ychou M, Lepille D, Mineur L, Navarro F, Topart D, et al. Gemcitabine in combination with cisplatin (GP) versus gemcitabine (G) alone in the treatment of locally advanced or metastatic pancreatic cancer: final results of a multicenter randomized phase II study. Journal of Clinical Oncology 2004;22(14 Suppl):4118.
Von Hoff 2013 {published data only}
    1. Hoff DD, Ervin TJ, Arena FP, Chiorean G, Infante JR, Moore MJ, et al. Randomized phase III study of weekly nab‐paclitaxel plus gemcitabine versus gemcitabine alone in patients with metastatic adenocarcinoma of the pancreas (MPACT). Journal of Clinical Oncology 2013;31(4 Suppl):LBA148.
Wang 2002 {published data only}
    1. Wang X, Ni Q, Jin M, Li Z, Wu Y, Zhao Y, et al. Gemcitabine or gemcitabine plus cisplatin for in 42 patients with locally advanced or metastatic pancreatic cancer. Chinese Journal of Oncology 2002;24(4):404‐7. - PubMed
Xinopoulos 2008 {published data only}
    1. Xinopoulos D, Dimitroulopoulos D, Karanikas I, Fotopoulou A, Oikonomou N, Korkolis D, et al. Gemcitabine as palliative treatment in patients with unresectable pancreatic cancer previously treated with placement of a covered metal stent. A randomized controlled trial. JBUON 2008;13(3):341‐7. - PubMed

References to studies excluded from this review

Abdel Wahab 1999 {published data only}
    1. Abdel‐Wahab M, El‐Shennawy F, Agha S, Ragab E, Fathi O, Sultan A, et al. Evaluation of cell mediated immunity in advanced pancreatic carcinoma before and after treatment with interleukin‐2 (IL‐2). Hepato‐gastroenterology 1999; Vol. 46, issue Suppl 1:1293‐6. - PubMed
Aigner 1998 {published data only}
    1. Aigner K R, Gailhofer S, Kopp S. Regional versus systemic chemotherapy for advanced pancreatic cancer: a randomized study. Hepato‐gastroenterology 1998;45(22):1125‐9. - PubMed
Alberts 2005 {published data only}
    1. Alberts S R, Foster N R, Morton R F, Kugler J, Schaefer P, Wiesenfeld M, et al. PS‐341 and gemcitabine in patients with metastatic pancreatic adenocarcinoma: a North Central Cancer Treatment Group (NCCTG) randomized phase II study. Annals of Oncology 2005;16(10):1654‐61. - PubMed
Andersen 1981 {published data only}
    1. Andersen JR, Friis‐Moller A, Hancke S, Roder O, Steen J, Baden H. A controlled trial of combination chemotherapy with 5‐FU and BCNU in pancreatic cancer. Scandinavian Journal of Gastroenterology 1981;16(8):973‐5. - PubMed
Ardalan 1988 {published data only}
    1. Ardalan B, Singh G, Silberman H. A randomized phase I and II study of short‐term infusion of high‐dose fluorouracil with or without N‐(phosphonacetyl)‐L‐aspartic acid in patients with advanced pancreatic and colorectal cancers. Journal of Clinical Oncology 1988;6(6):1053‐8. - PubMed
Astsaturov 2011 {published data only}
    1. Astsaturov IA, Meropol NJ, Alpaugh RK, Burtness BA, Cheng JD, McLaughlin S, et al. Phase II and coagulation cascade biomarker study of bevacizumab with or without docetaxel in patients with previously treated metastatic pancreatic adenocarcinoma. American Journal of Clinical Oncology 2011;34(1):70‐5. - PMC - PubMed
Baker 1976 {published data only}
    1. Baker LH, Vaitkevicius VK, Gehan E. Randomized prospective trial comparing 5‐fluorouracil (NSC‐19893) to 5‐fluorouracil and methyl‐CCNU (NSC‐95441) in advanced gastrointestinal cancer. Cancer Treatment Reports 1976;60(6):733‐7. - PubMed
Benavides 2014 {published data only}
    1. Benavides M, Gallego Plazas J, Guillen C, Vera R, Iranzo V, Diaz I, et al. Gemcitabine (G)/erlotinib (E) versus gemcitabine/erlotinib/capecitabine (C) in the first‐line treatment of patients with metastatic pancreatic cancer (mPC): Efficacy and safety results of a phase IIb randomized study from the Spanish TTD Collaborative Group. Journal of Clinical Oncology 2014;32:5s. - PubMed
Benson 2014 {published data only}
    1. Benson A, Bendell J, Wainberg ZA, VyushkovD, Acs P, Kudrik F, et al. A phase 2 randomized, double‐blind, placebo controlled study of simtuzumab or placebo in combination with gemcitabine for the first line treatment of pancreatic adenocarcinoma. Annals of Oncology. 2014; Vol. 25:iv210. - PMC - PubMed
Benson 2017 {published data only}
    1. Benson AB, Wainberg ZA, Hecht JR, Vyushkov D, Dong H, Bendell J, et al. A phase II randomized, double‐blind, placebo‐controlled study of simtuzumab or placebo in combination with gemcitabine for the first‐line treatment of pancreatic adenocarcinoma. Oncologist 2017;22(3):241. - PMC - PubMed
Berglund 2010 {published data only}
    1. Berglund A, Bystrom P, Johansson B, Nygren P, Frodin JE, Pedersen D, et al. An explorative randomised phase II study of sequential chemotherapy in advanced upper gastrointestinal cancer. Medical Oncology 2010;27(1):65‐72. - PubMed
Bramhall 2001 {published data only}
    1. Bramhall SR, Rosemurgy A, Brown PD, Bowry C, Buckels JA. Marimastat as first‐line therapy for patients with unresectable pancreatic cancer: a randomized trial. Journal of Clinical Oncology 2001;19(15):3447‐55. - PubMed
Bramhall 2002 {published data only}
    1. Bramhall SR, Schulz J, Nemunaitis J, Brown PD, Baillet M, Buckels JA. A double‐blind placebo‐controlled, randomised study comparing gemcitabine and marimastat with gemcitabine and placebo as first line therapy in patients with advanced pancreatic cancer. British Journal of Cancer 2002;87(2):161‐7. - PMC - PubMed
Buanes 2009 {published data only}
    1. Buanes T, Maurel J, Liauw W, Hebbar M, Nemunaitis J. A randomized phase III study of gemcitabine (G) versus GV1001 in sequential combination with G in patients with unresectable and metastatic pancreatic cancer (PC). Journal of Clinical Oncology 2009;27(15S):4601.
Bukowski 1993 {published data only}
    1. Bukowski RM, Fleming TR, Macdonald JS, Oishi N, Taylor SA, Baker LH. Evaluation of combination chemotherapy and phase II agents in pancreatic adenocarcinoma. A Southwest Oncology Group study. Cancer 1993;71(2):322‐5. - PubMed
Burtness 2016 {published data only}
    1. Burtness B, Powell M, Catalano P, Berlin J, Liles DK, Chapman AE, et al. Randomized phase II trial of irinotecan/docetaxel or irinotecan/docetaxel plus cetuximab for metastatic pancreatic cancer: an Eastern Cooperative Oncology Group Study. American Journal of Clinical Oncology 2016;39(4):340‐5. [10.1097/COC.0000000000000068] - PMC - PubMed
Cantore 2004 {published data only}
    1. Cantore M, Fiorentini G, Luppi G, Rosati G, Caudana R, Piazza E, et al. Gemcitabine versus FLEC regimen given intra‐arterially to patients with unresectable pancreatic cancer: a prospective, randomized phase III trial of the Italian Society for Integrated Locoregional Therapy in Oncology. Journal of Chemotherapy (Florence) 2004;16(6):589‐94. - PubMed
Cascinu 2008 {published data only}
    1. Cascinu S, Berardi R, Labianca R, Siena S, Falcone A, Aitini E, et al. Cetuximab plus gemcitabine and cisplatin compared with gemcitabine and cisplatin alone in patients with advanced pancreatic cancer: a randomised, multicentre, phase II trial. Lancet Oncology 2008;9(1):39‐44. - PubMed
Cascinu 2013 {published data only}
    1. Cascinu S, Berardi R, Sobrero A, Bidoli P, Labianca R, Siena S, et al. Sorafenib does not improve efficacy of chemotherapy in advanced pancreatic cancer: a GISCAD randomized phase II study. Digestive and Liver Disease 2013;46(2):182‐6. - PubMed
Catenacci 2013 {published data only}
    1. Catenacci DVT, Bahary N, Nattam SR, Marsh RW, Wallace JA, Rajdev L, et al. Final analysis of a phase IB/randomized phase II study of gemcitabine (G) plus placebo (P) or vismodegib (V), a hedgehog (Hh) pathway inhibitor, in patients (pts) with metastatic pancreatic cancer (PC): a University of Chicago phase II consortium study. Journal of Clinical Oncology 2013;31(15 Suppl):4012.
Chai 2013 {published data only}
    1. Chai K, Ai YQ, Jiang LW. Phase II study of dendritic cell vaccination combined with recombinant adenovirus‐p53 in treatment for patients with advanced pancreatic carcinoma. Journal of Clinical Oncology 2013;31:3049.
Chauffert 2008 {published data only}
    1. Chauffert B, Mornex F, Bonnetain F, Rougier P, Mariette C, Bouche O, et al. Phase III trial comparing intensive induction chemoradiotherapy (60 Gy, infusional 5‐FU and intermittent cisplatin) followed by maintenance gemcitabine with gemcitabine alone for locally advanced unresectable pancreatic cancer. Definitive results of the 2000‐01 FFCD/SFRO study. Annals of Oncology 2008;19(9):1592‐9. - PubMed
Chen 2006 {published data only}
    1. Chen J, Röcken C, Nitsche B, Hosius C, Gschaidmeier H, Kahl S, et al. The tyrosine kinase inhibitor imatinib fails to inhibit pancreatic cancer progression. Cancer Letters 2006;233(2):328‐37. - PubMed
Chung 2004 {published data only}
    1. Chung HW, Bang SM, Park SW, Chung JB, Kang JK, Kim JW, et al. A prospective randomized study of gemcitabine with doxifluridine versus paclitaxel with doxifluridine in concurrent chemoradiotherapy for locally advanced pancreatic cancer. International Journal of Radiation Oncology, Biology, Physics 2004;60(5):1494‐501. - PubMed
Chung 2015 {published data only}
    1. Chung VM, McDonough SL, Philip PA, Cardin DB, Wang‐Gillam A, Hui L, et al. SWOG S1115: Randomized phase II trial of selumetinib (AZD6244; ARRY 142886) hydrogen sulfate (NSC‐748727) and MK‐2206 (NSC‐749607) vs. mFOLFOX in pretreated patients (Pts) with metastatic pancreatic cancer. Journal of Clinical Oncology. 2015; Vol. 33:4119.
Ciuleanu 2009 {published data only}
    1. Ciuleanu TE, Pavlovsky AV, Bodoky G, Garin AM, Langmuir VK, Kroll S, et al. A randomised Phase III trial of glufosfamide compared with best supportive care in metastatic pancreatic adenocarcinoma previously treated with gemcitabine. European Journal of Cancer 2009;45(9):1589‐96. - PubMed
Cohen 2005 {published data only}
    1. Cohen SJ, Dobelbower R Jr, Lipsitz S, Catalano PJ, Sischy B, Smith TJ, et al. A randomized phase III study of radiotherapy alone or with 5‐fluorouracil and mitomycin‐C in patients with locally advanced adenocarcinoma of the pancreas: Eastern Cooperative Oncology Group study E8282. International Journal of Radiation Oncology, Biology, Physics 2005;62(5):1345‐50. - PubMed
Cohen 2010 {published data only}
    1. Cohen SJ, Zalupski MM, Conkling P, Nugent FW, Ma W, Modiano M, et al. A phase II randomized double blind multicenter trial of gemcitabine (Gem) plus imexon (IMX) versus Gem plus placebo (P) in patients with chemotherapy‐naive pancreatic adenocarcinoma (PC). Journal of Clinical Oncology 2010;28:4076. - PubMed
Dahan 2010 {published data only}
    1. Dahan L, Bonnetain F, Ychou M, Mitry E, Gasmi M, Raoul JL, et al. Combination 5‐fluorouracil, folinic acid and cisplatin (LV5FU2‐CDDP) followed by gemcitabine or the reverse sequence in metastatic pancreatic cancer: final results of a randomised strategic phase III trial (FFCD 0301). Gut 2010;59(11):1527‐34. - PMC - PubMed
Dalgleish 2015 {published data only}
    1. Dalgleish AG, IMAGE I Trial Investigators. A multicenter randomized, open‐label, proof‐of‐concept, phase II trial comparing gemcitabine with and without IMM‐101 in advanced pancreatic cancer. Journal of Clinical Oncology 2015;33:3051.
Deplanque 2015 {published data only}
    1. Deplanque G, Demarchi M, Hebbar M, Flynn P, Milchar B, Atkins J, et al. A randomized, placebo‐controlled phase III trial of masitinib plus gemcitabine in the treatment of advanced pancreatic cancer. Annals of Oncology 2015;26:1194‐200. - PMC - PubMed
Ducreux 2002 {published data only}
    1. Ducreux M, Rougier P, Pignon JP, Douillard JY, Seitz JF, Bugat R, et al. A randomised trial comparing 5‐FU with 5‐FU plus cisplatin in advanced pancreatic carcinoma. Annals of Oncology 2002;13(8):1185‐91. - PubMed
Duffy 2015 {published data only}
    1. Duffy AG, Beg MS, Greten TF, Beatson MA, Mavroukakis S, Patel SP, et al. A multicenter randomized phase II study of NPC‐1C(N) in combination with gemcitabine (G) and nab‐paclitaxel (A) versus G and A alone in patients with metastatic or locally advanced pancreatic cancer (PC) previously treated with folfirinox (F). Journal of Clinical Oncology 2015;33(Suppl 3):TPS499.
El‐Khoueiry 2012 {published data only}
    1. El‐Khoueiry AB, Ramanathan RK, Yang DY, Zhang W, Shibata S, Wright JJ, et al. A randomized phase II of gemcitabine and sorafenib versus sorafenib alone in patients with metastatic pancreatic cancer. Investigational New Drugs 2012;30(3):1175‐83. - PMC - PubMed
Evans 2014 {published data only}
    1. Evans J, Moore M, Cutsem E, Rock E, Strauss L, ODwyer P. Phase 2 Double‐blind, placebo‐controlled trial of dasatinib added to gemcitabine for subjects with locally‐advanced pancreatic cancer (LAPC). Annals of Oncology 2014;25:ii105. - PubMed
Friess 2006 {published data only}
    1. Friess H, Langrehr JM, Oettle H, Raedle J, Niedergethmann M, Dittrich C, et al. A randomized multi‐center phase II trial of the angiogenesis inhibitor Cilengitide (EMD 121974) and gemcitabine compared with gemcitabine alone in advanced unresectable pancreatic cancer. BMC Cancer 2006;6:285. - PMC - PubMed
Fuchs 2015 {published data only}
    1. Fuchs CS, Azevedo A, Okusaka T, Laethem JL, Lipton LR, Riess H, et al. A phase 3 randomized, double‐blind, placebo‐controlledtrial of ganitumab or placebo in combination withgemcitabine as first‐line therapy for metastaticadenocarcinoma of the pancreas: the GAMMA trial. Annals of Oncology 2015;26:921‐7. - PMC - PubMed
Fukutomi 2015 {published data only}
    1. Fukutomi A, Mizusawa J, Katayama H, Nakamura S, Ito Y, Hiraoka N, et al. Randomized phase II study of S‐1 and concurrent radiotherapy with versus without induction chemotherapy of gemcitabine for locally advanced pancreatic cancer (JCOG 1106). Journal of Clinical Oncology 2015;33:4116.
Gill 2014 {published data only}
    1. Gill S, Ko YJ, Cripps C, Beaudoin A, Dhesy‐Thind SK, Zulfiqar M, et al. PANCREOX: A randomized phase 3 study of 5FU/LV with or without oxaliplatin for second‐line advanced pancreatic cancer (APC) in patients (pts) who have received gemcitabine (GEM)‐based chemotherapy (CT). Journal of Clinical Oncology 2014;32:5s. - PubMed
Gilliam 2012 {published data only}
    1. Gilliam AD, Broome P, Topuzov EG, Garin AM, Pulay I, Humphreys J, et al. An international multicenter randomized controlled trial of G17DT in patients with pancreatic cancer. Pancreas 2012;41(3):374‐9. - PubMed
GISTG 1985 (radiotherapy) {published data only}
    1. Gastrointestinal Tumour Study Group. Radiation therapy combined with Adriamycin or 5‐fluorouracil for the treatment of locally unresectable pancreatic carcinoma. Cancer 1985;56(11):2563‐8. - PubMed
GITSG 1979 {published data only}
    1. Gastrointestinal Tumor Study Group. A multi‐institutional comparative trial of radiation therapy alone and in combination with 5‐fluorouracil for locally unresectable pancreatic carcinoma. Annals of Surgery 1979;189(2):205‐8. - PMC - PubMed
GITSG 1985 {published data only}
    1. Gastrointestinal Trials Study Group. Phase II trials of maytansine, low‐dose chlorozotocin, and high‐dose chlorozotocin as single agents against advanced measurable adenocarcinoma of the pancreas. Gastrointestinal Tumor Study Group. Cancer Treatment Reports 1985;69(4):417‐20. - PubMed
GITSG 1988 {published data only}
    1. Group Gastrointestinal Tumor Study. Treatment of locally unresectable carcinoma of the pancreas: comparison of combined‐modality therapy (chemotherapy plus radiotherapy) to chemotherapy alone. Journal of the National Cancer Institute 1988;80(10):751‐5. - PubMed
Gonçalves 2012 {published data only}
    1. Gonçalves A, Gilabert M, François E, Dahan L, Perrier H, Lamy R, et al. BAYPAN study: a double‐blind phase III randomized trial comparing gemcitabine plus sorafenib and gemcitabine plus placebo in patients with advanced pancreatic cancer. Annals of Oncology 2012;23(11):2799‐805. - PubMed
Gong 2007 {published data only}
    1. Gong JF, Zhang XD, Li J, Di LJ, Jin ML, Shen L. Efficacy of gemcitabine‐based chemotherapy on advanced pancreatic cancer. Ai Zheng [Chinese Journal of Cancer] 2007;26(8):890‐4. - PubMed
Haas 2015 {published data only}
    1. Haas M, Boeck SH, Waldschmidt D, Reinacher‐Schick A, Freiberg‐Richter J, Seufferlein T, et al. ACCEPT: Afatinib as cancer therapy for exocrine pancreatic tumors‐An explorative randomized phase II trial. Journal of Clinical Oncology 2015;33:TPS4150.
Hammel 2013 {published data only}
    1. Hammel P, Huguet F, Laethem JL, Goldstein D, Glimelius B, Artru P, et al. Comparison of chemoradiotherapy (CRT) and chemotherapy (CT) in patients with a locally advanced pancreatic cancer (LAPC) controlled after 4 months of gemcitabine with or without erlotinib: final results of the international phase III LAP 07 study. Journal of Clinical Oncology 2013;31:LBA4003.
Han 2006 {published data only}
    1. Han GH, Yin ZX, Meng XJ, He CY, Zhang HB, Sun AH, et al. Prospective randomized clinical trial of two drug delivery pathway in the treatment of inoperable advanced pancreatic carcinoma. Chinese Journal of Digestive Diseases 2006;7(1):45‐8. - PubMed
Hazel 1981 {published data only}
    1. Hazel JJ, Thirlwell MP, Huggins M, Maksymiuk A, MacFarlane JK. Multi‐drug chemotherapy with and without radiation for carcinoma of the stomach and pancreas: a prospective randomized trial. Journal of the Canadian Association of Radiologists 1981;32(3):164‐5. - PubMed
Heinemann 2013 {published data only}
    1. Heinemann V, Ebert MP, Laubender RP, Bevan P, Mala C, Boeck S. Phase II randomised proof‐of‐concept study of the urokinase inhibitor upamostat (WX‐671) in combination with gemcitabine compared with gemcitabine alone in patients with non‐resectable, locally advanced pancreatic cancer. British Journal of Cancer 2013;108(4):766‐70. - PMC - PubMed
Heinemann 2013 (GUT) {published data only}
    1. Heinemann V, Vehling‐Kaiser U, Waldschmidt D, Kettner E, Marten A, Winkelmann C, et al. Gemcitabine plus erlotinib followed by capecitabine versus capecitabine plus erlotinib followed by gemcitabine in advanced pancreatic cancer: final results of a randomised phase 3 trial of the 'Arbeitsgemeinschaft Internistische Onkologie' (AIO‐PK0104). Gut 2013;62(5):751‐9. - PMC - PubMed
Herman 2013 {published data only}
    1. Herman JM, Wild AT, Wang H, Tran PT, Chang KJ, Taylor GE, et al. Randomized phase III multi‐institutional study of TNFerade biologic with fluorouracil and radiotherapy for locally advanced pancreatic cancer: final results. Journal of Clinical Oncology 2013;31(7):886. - PMC - PubMed
Hingorani 2015 {published data only}
    1. Hingorani SR, Proctor Harris W, Hendifar AE, Bullock AJ, Wu XW, Huang Y, et al. High response rate and PFS with PEGPH20 added to nab‐paclitaxel/gemcitabine in stage IV previously untreated pancreatic cancer patients with high‐HA tumors: Interim results of a randomized phase II study. Journal of Clinical Oncology 2015;33:4006.
Horton 1981 {published data only}
    1. Horton J, Gelber R D, Engstrom P, Falkson G, Moertel C, Brodovsky H, et al. Trials of single‐agent and combination chemotherapy for advanced cancer of the pancreas. Cancer Treatment Reports 1981;65(1‐2):65‐8. - PubMed
Hurwitz 2015 {published data only}
    1. Hurwitz HI, Uppal N, Wagner SA, Bendell JC, Beck T, Wade SM 3rd, et al. Randomized, double‐blind, phase II study of ruxolitinib or placebo in combination with capecitabine in patients with metastatic pancreatic cancer for whom therapy with gemcitabine has failed. Journal of Clinical Oncology 2015;33(34):4039‐47. [DOI: 10.1200/JCO.2015.61.4578.] - DOI - PMC - PubMed
Hurwitz 2015 (JANUS 1) {published data only}
    1. Hurwitz H, Garrett WM, Clark J, Brill KJ, Dawkins FW, Hidalgo M, et al. JANUS 1: A phase 3, placebo‐controlled study of ruxolitinib plus capecitabine in patients with advanced or metastatic pancreatic cancer (MPC) after failure or intolerance of first‐line chemotherapy. Journal of Clinical Oncology 2015;33:TPS4147.
Infante 2013 {published data only}
    1. Infante JR, Somer BG, Park JO, Li CP, Scheulen ME, Kasubhai SM, et al. A randomized, double‐blind, placebo‐controlled trial of trametinib, a MEK inhibitor, in combination with gemcitabine for patients with untreated metastatic adenocarcinoma of the pancreas. Journal of Clinical Oncology 2013;31(4 Suppl):291. - PubMed
Ioka 2009 {published data only}
    1. Ioka T, Takakura R, Nakaizumi A, Tanaka S, Iishi H, Nakamura S, et al. A multicenter randomized phase II study of full‐dose gemcitabine and concurrent radiotherapy comparing gemcitabine alone for the unresectable locally advanced pancreatic adenocarcinoma. Journal of Clinical Oncology 2009;27:e15512.
Ioka 2013 {published data only}
    1. Ioka T, Katayama K, Ishida N, Takada R, Yamai T, Fukutake N, et al. Randomized phase II study of best available fluoropyrimidine compared with continuation of gemcitabine (Gem) monotherapy in patients with Gem‐refractory pancreatic cancer. Journal of Clinical Oncology 2013;31:287.
Jacobs 2004 {published data only}
    1. A Jacobs. Full survival data not available. Email to V Chin 5 September 2014.
    1. Jacobs AD, Burris HA, Rivkin S, Ritch PS, Eisenberg PD, Mettinger KL. A randomized phase III study of rubitecan (ORA) vs. best choice (BC) in 409 patients with refractory pancreatic cancer report from a North‐American multi‐center study. Journal of Clinical Oncology 2004;22:4013.
Javle 2011 {published data only}
    1. Javle MM, Varadhachary GR, Fogelman DR, Shroff RT, Overman MJ, Ukegbu L, et al. Randomized phase II study of gemcitabine (G) plus anti‐IGF‐1R antibody MK‐0646, G plus erlotinib (E) plus MK‐0646 and G plus E for advanced pancreatic cancer. Journal of Clinical Oncology 2011;29:4026.
Johnson 2001 {published data only}
    1. Johnson CD, Puntis M, Davidson N, Todd S, Bryce R. Randomized, dose‐finding phase III study of lithium gamolenate in patients with advanced pancreatic adenocarcinoma. British Journal of Surgery 2001;88(5):662‐8. - PubMed
Kim 2011 {published data only}
    1. Kim GP, Foster NR, Salim M, Flynn PJ, Moore DF, Zon R, et al. Randomized phase II trial of panitumumab (P), erlotinib (E), and gemcitabine (G) versus erlotinib‐gemcitabine in patients with untreated, metastatic pancreatic adenocarcinoma. Journal of Clinical Oncology 2011;29:238.
Kindler 2008 {published data only}
    1. Kindler HL, Gangadhar T, Karrison T, Hochster HS, Moore MJ, Micetich K, et al. Final analysis of a randomized phase II study of bevacizumab (B) and gemcitabine (G) plus cetuximab (C) or erlotinib (E) in patients (pts) with advanced pancreatic cancer (PC). Journal of Clinical Oncology 2008;26:4502.
Kindler 2010 {published data only}
    1. KKindler HL, Niedzwiecki D, Hollis D, Sutherland S, Schrag D, Hurwitz H, et al. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303). Journal of Clinical Oncology 2010;28(22):3617‐22. - PMC - PubMed
Kindler 2011 {published data only}
    1. Kindler HL, Ioka T, Richel DJ, Bennouna J, Letourneau R, Okusaka T, et al. Axitinib plus gemcitabine versus placebo plus gemcitabine in patients with advanced pancreatic adenocarcinoma: a double‐blind randomised phase 3 study. Lancet Oncology 2011;12(3):256‐62. - PubMed
Kindler 2012 {published data only}
    1. Kindler HL, Richards DA, Garbo LE, Garon EB, Stephenson JJ Jr, Rocha‐Lima CM, et al. A randomized, placebo‐controlled phase 2 study of ganitumab (AMG 479) or conatumumab (AMG 655) in combination with gemcitabine in patients with metastatic pancreatic cancer. Annals of Oncology 2012;23(11):2384‐42. - PubMed
Kindler 2015 {published data only}
    1. Kindler HL, Locker GY, Mann H, Golan T. POLO: A randomized phase III trial of olaparib tablets in patients with metastatic pancreatic cancer (mPC) and a germline BRCA1/2 mutation (gBRCAm) who have not progressed following first‐line chemotherapy. Journal of Clinical Oncology. 2015; Vol. 33.
Klaassen 1985 {published data only}
    1. Klaassen DJ, MacIntyre JM, Catton GE, Engstrom PF, Moertel CG. Treatment of locally unresectable cancer of the stomach and pancreas: a randomized comparison of 5‐fluorouracil alone with radiation plus concurrent and maintenance 5‐fluorouracil‐‐an Eastern Cooperative Oncology Group study. Journal of Clinical Oncology 1985;3(3):373‐8. - PubMed
Ko 2012 {published data only}
    1. Ko AH, Youssoufian H, Gurtler J, Dicke K, Kayaleh O, Lenz H J, et al. A phase II randomized study of cetuximab and bevacizumab alone or in combination with gemcitabine as first‐line therapy for metastatic pancreatic adenocarcinoma. Investigational New Drugs 2012;30(4):1597‐606. - PubMed
Ko 2016 {published data only}
    1. Ko AH, Murphy PB, Peyton JD, Shipley D, Al‐Hazzouri A, Rodrigeuz FA, et al. RAINIER: A randomized, double‐blinded, placebo‐controlled phase II trial of gemcitabine (gem) plus nab‐paclitaxel (nab‐P) combined with apatorsen (A) or placebo (Pl) in patients (pts) with metastatic pancreatic cancer (mPC). Journal of Clinical Oncology 2016;34(4 Suppl):419.
Lasalvia‐Prisco 2012 {published data only}
    1. Lasalvia‐Prisco E, Goldschmidt P, Galmarini F, Cucchi S, Vazquez J, Aghazarian M, et al. Addition of an induction regimen of antiangiogenesis and antitumor immunity to standard chemotherapy improves survival in advanced malignancies. Medical Oncology 2012;29(5):3626‐33. - PMC - PubMed
Le (Ipilimumab) 2013 {published data only}
    1. Le DT, Lutz E, Uram JN, Sugar EA, Onners B, Solt S, et al. Evaluation of ipilimumab in combination with allogeneic pancreatic tumor cells transfected with a GM‐CSF gene in previously treated pancreatic cancer. Journal of Immunotherapy 2013;36(7):382‐9. - PMC - PubMed
Le 2013 {published data only}
    1. Le DT, Wang‐Gillam A, Picozzi VJ, Greten TF, Crocenzi TS, Springett GM, et al. Interim safety and efficacy analysis of a phase II, randomized study of GVAX pancreas and CRS‐207 immunotherapy in patients with metastatic pancreatic cancer. Journal of Clinical Oncology 2013;31:4040.
Le 2015 {published data only}
    1. Le DT, Crocenzi TS, Uram JN, Lutz ER, Laheru DA, Sugar EA, et al. Randomized phase II study of the safety, efficacy, and immune response of GVAX pancreas vaccine (with cyclophophamide) and CRS‐207 with or without nivolumab in patients with previously treated metastatic pancreatic adenocarcinomas (STELLAR). Journal for Immunotherapy of Cancer 2015;3(Suppl 2):155.
Li 2003 {published data only}
    1. Li CP, Chao Y, Chi KH, Chan WK, Teng HC, Lee RC, et al. Concurrent chemoradiotherapy treatment of locally advanced pancreatic cancer: gemcitabine versus 5‐fluorouracil, a randomized controlled study. International Journal of Radiation Oncology, Biology, Physics 2003;57(1):98‐104. - PubMed
Li 2016 {published data only}
    1. Li JQ, Yang JC, Liang JX, Wang SL. Pharmacokinetic study and clinical evaluation of a slow‐release 5‐fluorouracil implant in pancreatic cancer patients. Anticancer Drugs 2016;27(1):60‐5. - PubMed
Linstadt 1988 {published data only}
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O'Neil 2015 {published data only}
    1. O'Neil BH, Scott AJ, Ma WW, Cohen SJ, Aisner DL, Menter AR, et al. A phase II/III randomized study to compare the efficacy and safety of rigosertib plus gemcitabine versus gemcitabine alone in patients with previously untreated metastatic pancreatic cancer. Annals of Oncology 2015;26:1923‐9. - PMC - PubMed
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Oberic 2011 {published data only}
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Pelzer 2011 {published data only}
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Rougier 2013 {published data only}
    1. Rougier P, Riess H, Manges R, Karasek P, Humblet Y, Barone, et al. Randomised, placebo‐controlled, double‐blind, parallel‐group phase III study evaluating aflibercept in patients receiving first‐line treatment with gemcitabine for metastatic pancreatic cancer. European Journal of Cancer 2013;49(12):2633‐42. - PubMed
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    1. Saif MW, Oettle H, Vervenne WL, Thomas JP, Spitzer G, Visseren‐Grul C, et al. Randomized double‐blind phase II trial comparing gemcitabine plus LY293111 versus gemcitabine plus placebo in advanced adenocarcinoma of the pancreas. Cancer Journal 2009;15(4):339‐43. - PubMed
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    1. Schmitz‐Winnenthal FH, Grenacher L, Friedrich T, Lubenau H, Springer M, Breiner KM, et al. VXM01, an oral T‐cell vaccine targeting the tumor vasculature: results from a randomized, controlled, first‐in‐man study in pancreatic cancer patients. Journal of Clinical Oncology 2013;31:3090.
Senzer 2006 {published data only}
    1. Senzer N, Rosemurgy A, Javle M, Reid T, Posner MC, Chang KJ, et al. The PACT trial: Interim results of a randomized trial of TNFerade biologic plus chemoradiation (CRT) compared to CRT alone in locally advanced pancreatic cancer (LAPC). Journal of Clinical Oncology 2006;24:4102.
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    1. Sudo K, Ishihara T, Hirata N, Ozawa F, Ohshima T, Azemoto R, et al. Randomized controlled study of gemcitabine plus S‐1 combination chemotherapy versus gemcitabine for unresectable pancreatic cancer. Cancer Chemotherapy and Pharmacology 2013;73(2):389. - PubMed
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Takada 1994 {published data only}
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