Clinical outcomes of second-line chemotherapy in patients with advanced pancreatic adenocarcinoma: a real-world study

References

1. 1.↵
   2. Siegel RL,
   3. Miller KD,
   4. Wagle NS,
   5. Jemal A.

   Cancer statistics, 2023. CA Cancer J Clin. 2023; 73: 17–48.

   OpenUrlCrossRefPubMed
2. 2.↵
   2. Wood LD,
   3. Canto MI,
   4. Jaffee EM,
   5. Simeone DM.

   Pancreatic cancer: pathogenesis, screening, diagnosis, and treatment. Gastroenterology. 2022; 163: 386–402.e1.

   OpenUrl
3. 3.↵
   2. Milano G,
   3. Innocenti F,
   4. Minami H.

   Liposomal irinotecan (Onivyde): exemplifying the benefits of nanotherapeutic drugs. Cancer Sci. 2022; 113: 2224–31.

   OpenUrl
4. 4.↵
   National Comprehensive Cancer Network. The nccn pancreatic adenocarcinoma clinical practice guidelines in oncology (version 2.2023 — June 19, 2023) [eb/ol]. Fort Washington: NCCN; 2023 [cited 2023 July 19]. Available from https://www.nccn.org/guidelines/category_1.
5. 5.↵
   2. Wainberg ZA,
   3. Melisi D,
   4. Macarulla T,
   5. Pazo Cid R,
   6. Chandana SR,
   7. De La Fouchardière C, et al.

   NALIRIFOX versus nab-paclitaxel and gemcitabine in treatment-naive patients with metastatic pancreatic ductal adenocarcinoma (NAPOLI 3): a randomised, open-label, phase 3 trial. Lancet (London, England). 2023; 402: 1272–81.

   OpenUrl
6. 6.↵
   2. Chiorean EG,
   3. Von Hoff DD,
   4. Tabernero J,
   5. El-Maraghi R,
   6. Ma WW,
   7. Reni M, et al.

   Second-line therapy after nab-paclitaxel plus gemcitabine or after gemcitabine for patients with metastatic pancreatic cancer. Br J Cancer. 2016; 115: 188–94.

   OpenUrl
7. 7.↵
   2. Zhu Z,
   3. Tang H,
   4. Ying J,
   5. Cheng Y,
   6. Wang X,
   7. Wang Y, et al.

   Efficacy and safety of gemcitabine plus S-1 vs. gemcitabine plus nab-paclitaxel in treatment-naïve advanced pancreatic ductal adenocarcinoma. Cancer Biol Med. 2023; 20: 765–78.

   OpenUrlAbstract/FREE Full Text
8. 8.↵
   2. Neoptolemos JP,
   3. Kleeff J,
   4. Michl P,
   5. Costello E,
   6. Greenhalf W,
   7. Palmer DH.

   Therapeutic developments in pancreatic cancer: current and future perspectives. Nat Rev Gastroenterol Hepatol. 2018; 15: 333–48.

   OpenUrlCrossRefPubMed
9. 9.↵
   2. Mie T,
   3. Sasaki T,
   4. Takeda T,
   5. Okamoto T,
   6. Hamada T,
   7. Ishitsuka T, et al.

   Treatment outcomes and prognostic factors of gemcitabine plus nab-paclitaxel as second-line chemotherapy after modified FOLFIRINOX in unresectable pancreatic cancer. Cancers. 2023; 15: 358.

   OpenUrl
10. 10.
    2. De Dosso S,
    3. Siebenhüner AR,
    4. Winder T,
    5. Meisel A,
    6. Fritsch R,
    7. Astaras C, et al.

    Treatment landscape of metastatic pancreatic cancer. Cancer Treat Rev. 2021; 96: 102180.
11. 11.↵
    2. Portal A,
    3. Pernot S,
    4. Tougeron D,
    5. Arbaud C,
    6. Bidault AT,
    7. de la Fouchardière C, et al.

    Nab-paclitaxel plus gemcitabine for metastatic pancreatic adenocarcinoma after Folfirinox failure: an AGEO prospective multicentre cohort. Br J Cancer. 2015; 113: 989–95.

    OpenUrlCrossRefPubMed
12. 12.
    2. Hayuka K,
    3. Okuyama H,
    4. Murakami A,
    5. Okita Y,
    6. Nishiuchi T,
    7. Okano K, et al.

    Gemcitabine plus nab-paclitaxel as second-line chemotherapy following FOLFIRINOX in patients with unresectable pancreatic cancer: a single-institution, retrospective analysis. Chemotherapy. 2021; 66: 58–64.

    OpenUrl
13. 13.↵
    2. Viaud J,
    3. Brac C,
    4. Artru P,
    5. Le Pabic E,
    6. Leconte B,
    7. Bodère A, et al.

    Gemcitabine as second-line chemotherapy after Folfirinox failure in advanced pancreatic adenocarcinoma: a retrospective study. Dig Liver Dis. 2017; 49: 692–6.

    OpenUrl
14. 14.↵
    2. Foschini F,
    3. Napolitano F,
    4. Servetto A,
    5. Marciano R,
    6. Mozzillo E,
    7. Carratù AC, et al.

    FOLFIRINOX after first-line gemcitabine-based chemotherapy in advanced pancreatic cancer: a retrospective comparison with FOLFOX and FOLFIRI schedules. Ther Adv Med Oncol. 2020; 12: 1758835920947970.
15. 15.↵
    2. Fukahori M,
    3. Okabe Y,
    4. Shimokawa M,
    5. Otsuka T,
    6. Koga F,
    7. Ueda Y, et al.

    Efficacy of second-line chemotherapy after treatment with gemcitabine plus nab-paclitaxel or folfirinox in patients with metastatic pancreatic cancer. Sci Rep. 2023; 13: 19399.
16. 16.↵
    2. Wang-Gillam A,
    3. Hubner RA,
    4. Siveke JT,
    5. Von Hoff DD,
    6. Belanger B,
    7. de Jong FA, et al.

    Napoli-1 phase 3 study of liposomal irinotecan in metastatic pancreatic cancer: final overall survival analysis and characteristics of long-term survivors. Eur J Cancer (Oxford, England: 1990). 2019; 108: 78–87.

    OpenUrl
17. 17.↵
    2. Catalano M,
    3. Conca R,
    4. Petrioli R,
    5. Ramello M,
    6. Roviello G.

    FOLFOX vs. FOLFIRI as second-line of therapy after progression to gemcitabine/nab-paclitaxel in patients with metastatic pancreatic cancer. Cancer Manag Res. 2020; 12: 10271–8.

    OpenUrl
18. 18.↵
    2. Mie T,
    3. Sasaki T,
    4. Okamoto T,
    5. Takeda T,
    6. Mori C,
    7. Furukawa T, et al.

    Treatment outcomes of nanoliposomal irinotecan as second-line chemotherapy after gemcitabine and nab-paclitaxel in metastatic and recurrent pancreatic cancer. Jpn J Clin Oncol. 2022; 52: 1399–407.

    OpenUrl
19. 19.↵
    2. Kieler M,
    3. Unseld M,
    4. Bianconi D,
    5. Scheithauer W,
    6. Prager GW.

    A real-world analysis of second-line treatment options in pancreatic cancer: liposomal-irinotecan plus 5-fluorouracil and folinic acid. Ther Adv Med Oncol. 2019; 11: 1758835919853196.
20. 20.
    2. Park SJ,
    3. Kim H,
    4. Shin K,
    5. Hong TH,
    6. Suh JH,
    7. Lee MA.

    Nanoliposomal irinotecan plus fluorouracil and folinic acid as a second-line treatment option in patients with metastatic pancreatic ductal adenocarcinoma: a retrospective cohort study. BMC Cancer. 2021; 21: 1176.

    OpenUrl
21. 21.↵
    2. Yasuoka H,
    3. Naganuma A,
    4. Kurihara E,
    5. Kobatake T,
    6. Ijima M,
    7. Tamura Y, et al.

    Efficacy and safety of the combination of nano-liposomal irinotecan and 5-fluorouracil/l-leucovorin in unresectable advanced pancreatic cancer: a real-world study. Oncology. 2022; 100: 449–59.

    OpenUrl
22. 22.↵
    2. Hecht JR,
    3. Lonardi S,
    4. Bendell J,
    5. Sim HW,
    6. Macarulla T,
    7. Lopez CD, et al.

    Randomized phase III study of FOLFOX alone or with pegilodecakin as second-line therapy in patients with metastatic pancreatic cancer that progressed after gemcitabine (SEQUOIA). J Clin Oncol. 2021; 39: 1108–18.

    OpenUrlCrossRefPubMed
23. 23.↵
    2. Oettle H,
    3. Riess H,
    4. Stieler JM,
    5. Heil G,
    6. Schwaner I,
    7. Seraphin J, et al.

    Second-line oxaliplatin, folinic acid, and fluorouracil versus folinic acid and fluorouracil alone for gemcitabine-refractory pancreatic cancer: outcomes from the CONKO-003 trial. J Clin Oncol. 2014; 32: 2423–9.

    OpenUrlAbstract/FREE Full Text
24. 24.↵
    2. Gill S,
    3. Ko YJ,
    4. Cripps C,
    5. Beaudoin A,
    6. Dhesy-Thind S,
    7. Zulfiqar M, et al.

    Pancreox: a randomized phase III study of fluorouracil/leucovorin with or without oxaliplatin for second-line advanced pancreatic cancer in patients who have received gemcitabine-based chemotherapy. J Clin Oncol. 2016; 34: 3914–20.

    OpenUrlPubMed
25. 25.↵
    2. Go SI,
    3. Lee SC,
    4. Bae WK,
    5. Zang DY,
    6. Lee HW,
    7. Jang JS, et al.

    Modified FOLFIRINOX versus S-1 as second-line chemotherapy in gemcitabine-failed metastatic pancreatic cancer patients: a randomised controlled trial (MPACA-3). Eur J Cancer (Oxford, England: 1990). 2021; 157: 21–30.

    OpenUrl
26. 26.↵
    2. Park HS,
    3. Kang B,
    4. Chon HJ,
    5. Im HS,
    6. Lee CK,
    7. Kim I, et al.

    Liposomal irinotecan plus fluorouracil/leucovorin versus FOLFIRINOX as the second-line chemotherapy for patients with metastatic pancreatic cancer: a multicenter retrospective study of the Korean Cancer Study Group (KCSG). ESMO Open. 2021; 6: 100049.
27. 27.↵
    2. Dayyani F,
    3. Macarulla T,
    4. Johnson A,
    5. Wainberg ZA.

    Second-line treatment options for patients with metastatic pancreatic ductal adenocarcinoma: a systematic literature review. Cancer Treat Rev. 2023; 113: 102502.
28. 28.↵
    2. Lewis A,
    3. Nagrial A.

    Systematic review of single-agent vs. Multi-agent chemotherapy for advanced pancreatic adenocarcinoma in elderly vs. younger patients. Cancers. 2023; 15: 2289.

    OpenUrl
29. 29.↵
    2. Nagrial AM,
    3. Chin VT,
    4. Sjoquist KM,
    5. Pajic M,
    6. Horvath LG,
    7. Biankin AV, et al.

    Second-line treatment in inoperable pancreatic adenocarcinoma: a systematic review and synthesis of all clinical trials. Crit Rev Oncol Hematol. 2015; 96: 483–97.

    OpenUrl
30. 30.↵
    2. Conroy T,
    3. Desseigne F,
    4. Ychou M,
    5. Bouché O,
    6. Guimbaud R,
    7. Bécouarn Y, et al.

    FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011; 364: 1817–25.

    OpenUrlCrossRefPubMedWeb of Science
31. 31.↵
    2. Von Hoff DD,
    3. Ervin T,
    4. Arena FP,
    5. Chiorean EG,
    6. Infante J,
    7. Moore M, et al.

    Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013; 369: 1691–703.

    OpenUrlCrossRefPubMedWeb of Science
32. 32.↵
    2. Wang-Gillam A,
    3. Li CP,
    4. Bodoky G,
    5. Dean A,
    6. Shan YS,
    7. Jameson G, et al.

    Nanoliposomal irinotecan with fluorouracil and folinic acid in metastatic pancreatic cancer after previous gemcitabine-based therapy (NAPOLI-1): a global, randomised, open-label, phase 3 trial. Lancet (London, England). 2016; 387: 545–57.

    OpenUrl
33. 33.↵
    2. de Jesus VHF,
    3. Camandaroba MPG,
    4. Calsavara VF,
    5. Riechelmann RP.

    Systematic review and meta-analysis of gemcitabine-based chemotherapy after folfirinox in advanced pancreatic cancer. Ther Adv Med Oncol. 2020; 12: 1758835920905408.
34. 34.
    2. Zhang Y,
    3. Hochster H,
    4. Stein S,
    5. Lacy J.

    Gemcitabine plus nab-paclitaxel for advanced pancreatic cancer after first-line FOLFIRINOX: single institution retrospective review of efficacy and toxicity. Exp Hematol Oncol. 2015; 4: 29.

    OpenUrl
35. 35.↵
    2. Mita N,
    3. Iwashita T,
    4. Uemura S,
    5. Yoshida K,
    6. Iwasa Y,
    7. Ando N, et al.

    Second-line gemcitabine plus nab-paclitaxel for patients with unresectable advanced pancreatic cancer after first-line FOLFIRINOX failure. J Clin Med. 2019; 8: 761.

    OpenUrl
36. 36.↵
    2. Sawada M,
    3. Kasuga A,
    4. Mie T,
    5. Furukawa T,
    6. Taniguchi T,
    7. Fukuda K, et al.

    Modified FOLFIRINOX as a second-line therapy following gemcitabine plus nab-paclitaxel therapy in metastatic pancreatic cancer. BMC Cancer. 2020; 20: 449.

    OpenUrlCrossRef
37. 37.
    2. Matsumoto T,
    3. Kurioka Y,
    4. Okazaki U,
    5. Matsuo Y,
    6. Kimura S,
    7. Miura K, et al.

    FOLFIRINOX for advanced pancreatic cancer patients after nab-paclitaxel plus gemcitabine failure. Pancreas. 2020; 49: 574–8.

    OpenUrl
38. 38.↵
    2. Tsang ES,
    3. Spratlin J,
    4. Cheung WY,
    5. Kim CA,
    6. Kong S,
    7. Xu Y, et al.

    Real-world outcomes among patients treated with gemcitabine-based therapy post-FOLFIRINOX failure in advanced pancreatic cancer. Am J Clin Oncol. 2019; 42: 903–8.

    OpenUrl
39. 39.↵
    2. Pelzer U,
    3. Schwaner I,
    4. Stieler J,
    5. Adler M,
    6. Seraphin J,
    7. Dörken B, et al.

    Best supportive care (BSC) versus oxaliplatin, folinic acid and 5-fluorouracil (OFF) plus BSC in patients for second-line advanced pancreatic cancer: a phase III-study from the German CONKO-study group. Eur J Cancer (Oxford, England: 1990). 2011; 47: 1676–81.

    OpenUrl
40. 40.↵
    2. Shi S,
    3. Liang C,
    4. Xu J,
    5. Meng Q,
    6. Hua J,
    7. Yang X, et al.

    The strain ratio as obtained by endoscopic ultrasonography elastography correlates with the stroma proportion and the prognosis of local pancreatic cancer. Ann Surg. 2020; 271: 559–65.

    OpenUrl
41. 41.↵
    2. Pijnappel EN,
    3. Dijksterhuis WPM,
    4. van der Geest LG,
    5. de Vos-Geelen J,
    6. de Groot JWB,
    7. Homs MYV, et al.

    First- and second-line palliative systemic treatment outcomes in a real-world metastatic pancreatic cancer cohort. J Natl Compr Cancer Netw. 2021; 20: 443–50.e3.

    OpenUrl
42. 42.↵
    2. Chan KKW,
    3. Guo H,
    4. Cheng S,
    5. Beca JM,
    6. Redmond-Misner R,
    7. Isaranuwatchai W, et al.

    Real-world outcomes of FOLFIRINOX vs gemcitabine and nab-paclitaxel in advanced pancreatic cancer: a population-based propensity score-weighted analysis. Cancer Med. 2020; 9: 160–9.

    OpenUrl
43. 43.↵
    2. Liang Y,
    3. Sheng G,
    4. Guo Y,
    5. Zou Y,
    6. Guo H,
    7. Li Z, et al.

    Prognostic significance of grade of malignancy based on histopathological differentiation and Ki-67 in pancreatic ductal adenocarcinoma. Cancer Biol Med. 2024; 21: 416–32.

    OpenUrlAbstract/FREE Full Text
44. 44.↵
    2. Zhou T,
    3. Man Q,
    4. Li X,
    5. Xie Y,
    6. Hou X,
    7. Wang H, et al.

    Artificial intelligence-based comprehensive analysis of immune-stemness-tumor budding profile to predict survival of patients with pancreatic adenocarcinoma. Cancer Biol Med. 2023; 20: 196–217.

    OpenUrlAbstract/FREE Full Text
45. 45.↵
    2. Johnson BA, 3rd.,
    3. Yarchoan M,
    4. Lee V,
    5. Laheru DA,
    6. Jaffee EM.

    Strategies for increasing pancreatic tumor immunogenicity. Clin Cancer Res. 2017; 23: 1656–69.

    OpenUrlAbstract/FREE Full Text
46. 46.↵
    2. Royal RE,
    3. Levy C,
    4. Turner K,
    5. Mathur A,
    6. Hughes M,
    7. Kammula US, et al.

    Phase 2 trial of single agent Ipilimumab (anti-CTLA-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother. 2010; 33: 828–33.

    OpenUrlCrossRefPubMedWeb of Science
47. 47.↵
    2. Shevchenko I,
    3. Karakhanova S,
    4. Soltek S,
    5. Link J,
    6. Bayry J,
    7. Werner J, et al.

    Low-dose gemcitabine depletes regulatory T cells and improves survival in the orthotopic Panc02 model of pancreatic cancer. Int J Cancer. 2013; 133: 98–107.

    OpenUrlCrossRefPubMed
48. 48.↵
    2. Kamath SD,
    3. Kalyan A,
    4. Kircher S,
    5. Nimeiri H,
    6. Fought AJ,
    7. Benson A, 3rd., et al.

    Ipilimumab and gemcitabine for advanced pancreatic cancer: a phase Ib study. Oncologist. 2020; 25: e808–15.

    OpenUrlPubMed
49. 49.↵
    2. Orsi G,
    3. Cavaliere A,
    4. Tortora G,
    5. Lonardi S,
    6. Macchini M,
    7. Di Marco M, et al.

    Second-line therapy in pancreatic ductal adenocarcinoma (PDAC) patients with germline BRCA1-2 pathogenic variants (gBRCA1-2pv). Br J Cancer. 2023; 128: 877–85.

    OpenUrl
50. 50.↵
    2. Huffman BM,
    3. Basu Mallick A,
    4. Horick NK,
    5. Wang-Gillam A,
    6. Hosein PJ,
    7. Morse MA, et al.

    Effect of a MUC5AC antibody (NPC-1C) administered with second-line gemcitabine and nab-paclitaxel on the survival of patients with advanced pancreatic ductal adenocarcinoma: a randomized clinical trial. JAMA Netw Open. 2023; 6: e2249720.
51. 51.↵
    2. Ganguly K,
    3. Krishn SR,
    4. Rachagani S,
    5. Jahan R,
    6. Shah A,
    7. Nallasamy P, et al.

    Secretory Mucin 5AC promotes neoplastic progression by augmenting KLF4-mediated pancreatic cancer cell stemness. Cancer Res. 2021; 81: 91–102.

    OpenUrlAbstract/FREE Full Text
52. 52.↵
    2. Manne A,
    3. Esnakula A,
    4. Abushahin L,
    5. Tsung A.

    Understanding the clinical impact of MUC5AC expression on pancreatic ductal adenocarcinoma. Cancers. 2021; 13: 3059.

    OpenUrl
53. 53.↵
    2. Bockorny B,
    3. Grossman JE,
    4. Hidalgo M.

    Facts and hopes in immunotherapy of pancreatic cancer. Clin Cancer Res. 2022; 28: 4606–17.

    OpenUrl
54. 54.↵
    2. Li S,
    3. Yue M,
    4. Xu H,
    5. Zhang X,
    6. Mao T,
    7. Quan M, et al.

    Chemotherapeutic drugs-induced pyroptosis mediated by gasdermin E promotes the progression and chemoresistance of pancreatic cancer. Cancer Lett. 2023; 564: 216206.