Therapy of locally advanced pancreatic adenocarcinoma: unresectable and borderline patients

References

• Jemal A, Siegel R, Xu J, Ward E. Cancer statistics. CA Cancer J. Clin.60, 277–300 (2010).
   PubMed Web of Science ®Google Scholar
• Geer RJ, Brennan MF. Prognostic indicators for survival after resection of pancreatic adenocarcinoma. Am. J. Surg.165(1), 68–72; discussion 72–63 (1993).
   PubMed Web of Science ®Google Scholar
• Sohn TA, Yeo CJ, Cameron JL et al. Resected adenocarcinoma of the pancreas – 616 patients: results, outcomes, and prognostic indicators. J. Gastrointest. Surg.4(6), 567–579 (2000).
   PubMed Web of Science ®Google Scholar
• Callery MP, Chang KJ, Fishman EK, Talamonti MS, William TLW, Linehan DC. Pretreatment assessment of resectable and borderline-resectable pancreatic cancer: expert consensus statement. Ann. Surg. Oncol.16(7), 1727–1733 (2009).
   PubMed Web of Science ®Google Scholar
• Gastrointestinal Tumor Study Group. Further evidence of effective adjuvant combined radiation and chemotherapy following curative resection of pancreatic cancer. Cancer59(12), 2006–2010 (1987).
   PubMed Web of Science ®Google Scholar
• Klinkenbijl JH, Jeekel J, Sahmoud T et al. Adjuvant radiotherapy and 5-fluorouracil after curative resection of cancer of the pancreas and periampullary region: Phase III trial of the EORTC gastrointestinal tract cancer cooperative group. Ann. Surg.230(6), 776–782; discussion 782–774 (1999).
   PubMed Web of Science ®Google Scholar
• Neoptolemos JP, Dunn JA, Stocken DD et al. Adjuvant chemoradiotherapy and chemotherapy in resectable pancreatic cancer: a randomised controlled trial. Lancet358(9293), 1576–1585 (2001).
   PubMed Web of Science ®Google Scholar
• Kalser MH, Ellenberg SS. Pancreatic cancer. Adjuvant combined radiation and chemotherapy following curative resection. Arch. Surg.120(8), 899–903 (1985).
   PubMed Web of Science ®Google Scholar
• Neoptolemos JP, Stocken DD, Friess H et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N. Engl. J. Med.350(12), 1200–1210 (2004).
   PubMed Web of Science ®Google Scholar
• Bakkevold KE, Arnesjo B, Dahl O, Kambestad B. Adjuvant combination chemotherapy (AMF) following radical resection of carcinoma of the pancreas and papilla of Vater – results of a controlled, prospective, randomised multicentre study. Eur. J. Cancer29A(5), 698–703 (1993).
   PubMed Web of Science ®Google Scholar
• Takada T, Amano H, Yasuda H et al. Is postoperative adjuvant chemotherapy useful for gallbladder carcinoma? A Phase III multicenter prospective randomized controlled trial in patients with resected pancreaticobiliary carcinoma. Cancer95(8), 1685–1695 (2002).
   PubMed Web of Science ®Google Scholar
• Kosuge T, Kiuchi T, Mukai K, Kakizoe T. A multicenter randomized controlled trial to evaluate the effect of adjuvant cisplatin and 5-fluorouracil therapy after curative resection in cases of pancreatic cancer. Jpn. J. Clin. Oncol.36(3), 159–165 (2006).
   PubMedGoogle Scholar
• Oettle H, Post S, Neuhaus P et al. Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA297(3), 267–277 (2007).
   PubMed Web of Science ®Google Scholar
• Neoptolemos JP, Stocken DD, Bassi C et al. Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial. JAMA304(10), 1073–1081 (2010).
   PubMed Web of Science ®Google Scholar
• Roldan GE, Gunderson LL, Nagorney DM et al. External beam versus intraoperative and External-beam irradiation for locally advanced pancreatic cancer. Cancer61(6), 1110–1116 (1988).
   PubMed Web of Science ®Google Scholar
• Moertel CG, Frytak S, Hahn RG et al. Therapy of locally unresectable pancreatic carcinoma: a randomized comparison of high dose (6000 rads) radiation alone, moderate dose radiation (4000 rads + 5-fluorouracil), and high dose radiation + 5-fluorouracil: The Gastrointestinal Tumor Study Group. Cancer48(8), 1705–1710 (1981).
   PubMed Web of Science ®Google Scholar
• Cohen SJ, Dobelbower R Jr, Lipsitz S 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. Int. J. Radiat. Oncol. Biol. Phys.62(5), 1345–1350 (2005).
   PubMed Web of Science ®Google Scholar
• Sultana A, Tudur Smith C, Cunningham D et al. Systematic review, including meta-analyses, on the management of locally advanced pancreatic cancer using radiation/combined modality therapy. Br. J. Cancer96(8), 1183–1190 (2007).
   PubMed Web of Science ®Google Scholar
• Krzyzanowska MK, Weeks JC, Earle CC. Treatment of locally advanced pancreatic cancer in the real world: population-based practices and effectiveness. J. Clin. Oncol.21(18), 3409–3414 (2003).
   PubMed Web of Science ®Google Scholar
• Saif MW, Eloubeidi MA, Russo S et al. Phase I study of capecitabine with concomitant radiotherapy for patients with locally advanced pancreatic cancer: expression analysis of genes related to outcome. J. Clin. Oncol.23(34), 8679–8687 (2005).
   PubMed Web of Science ®Google Scholar
• Schneider BJ, Ben-Josef E, McGinn CJ et al. Capecitabine and radiation therapy preceded and followed by combination chemotherapy in advanced pancreatic cancer. Int. J. Radiat. Oncol. Biol. Phys.63(5), 1325–1330 (2005).
   PubMedGoogle Scholar
• Vaishampayan UN, Ben-Josef E, Philip PA et al. A single-institution experience with concurrent capecitabine and radiation therapy in gastrointestinal malignancies. Int. J. Radiat. Oncol. Biol. Phys.53(3), 675–679 (2002).
   PubMed Web of Science ®Google Scholar
• Lawrence TS, Eisbruch A, Shewach DS. Gemcitabine-mediated radiosensitization. Semin. Oncol.24(2 Suppl. 7), S7–S24; S27–S28 (1997).
   Google Scholar
• Burris HA 3rd, Moore MJ, Andersen J et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol.15(6), 2403–2413 (1997).
   PubMed Web of Science ®Google Scholar
• Wolff RA, Evans DB, Gravel DM et al. Phase I trial of gemcitabine combined with radiation for the treatment of locally advanced pancreatic adenocarcinoma. Clin. Cancer Res.7(8), 2246–2253 (2001).
   PubMed Web of Science ®Google Scholar
• Blackstock AW, Bernard SA, Richards F et al. Phase I trial of twice-weekly gemcitabine and concurrent radiation in patients with advanced pancreatic cancer. J. Clin. Oncol.17(7), 2208–2212 (1999).
   PubMed Web of Science ®Google Scholar
• Joensuu TK, Kiviluoto T, Karkkainen P et al. Phase I–II trial of twice-weekly gemcitabine and concomitant irradiation in patients undergoing pancreaticoduodenectomy with extended lymphadenectomy for locally advanced pancreatic cancer. Int. J. Radiat. Oncol. Biol. Phys.60(2), 444–452 (2004).
   PubMedGoogle Scholar
• Blackstock AW, Tepper JE, Niedwiecki D, Hollis DR, Mayer RJ, Tempero MA. Cancer and leukemia group B (CALGB) 89805: Phase II chemoradiation trial using gemcitabine in patients with locoregional adenocarcinoma of the pancreas. Int. J. Gastrointest. Cancer34(2–3), 107–116 (2003).
   PubMedGoogle Scholar
• Talamonti MS, Small W Jr, Mulcahy MF et al. A multi-institutional Phase II trial of preoperative full-dose gemcitabine and concurrent radiation for patients with potentially resectable pancreatic carcinoma. Ann. Surg. Oncol.13(2), 150–158 (2006).
   PubMed Web of Science ®Google Scholar
• Crane CH, Abbruzzese JL, Evans DB et al. Is the therapeutic index better with gemcitabine-based chemoradiation than with 5-fluorouracil-based chemoradiation in locally advanced pancreatic cancer? Int. J. Radiat. Oncol. Biol. Phys.52(5), 1293–1302 (2002).
   PubMed Web of Science ®Google Scholar
• Talamonti MS, Catalano PJ, Vaughn DJ et al. Eastern Cooperative Oncology Group Phase I trial of protracted venous infusion fluorouracil plus weekly gemcitabine with concurrent radiation therapy in patients with locally advanced pancreas cancer: a regimen with unexpected early toxicity. J. Clin. Oncol.18(19), 3384–3389 (2000).
   PubMed Web of Science ®Google Scholar
• Louvet C, Labianca R, Hammel P et al. Gemcitabine in combination with oxaliplatin compared with gemcitabine alone in locally advanced or metastatic pancreatic cancer: results of a GERCOR and GISCAD Phase III trial. J. Clin. Oncol.23(15), 3509–3516 (2005).
   PubMed Web of Science ®Google Scholar
• Van Cutsem E, van de Velde H, Karasek P et al. Phase III trial of gemcitabine plus tipifarnib compared with gemcitabine plus placebo in advanced pancreatic cancer. J. Clin. Oncol.22(8), 1430–1438 (2004).
   PubMed Web of Science ®Google Scholar
• Rocha Lima CM, Green MR, Rotche R et al. Irinotecan plus gemcitabine results in no survival advantage compared with gemcitabine monotherapy in patients with locally advanced or metastatic pancreatic cancer despite increased tumor response rate. J. Clin. Oncol.22(18), 3776–3783 (2004).
   PubMed Web of Science ®Google Scholar
• Conroy T, Desseigne F, Ychou M et al. Randomized Phase III trial comparing FOLFIRINOX (F: 5FU/leucovorin [LV], irinotecan [I], and oxaliplatin [O]) versus gemcitabine (G) as first-line treatment for metastatic pancreatic adenocarcinoma (MPA): preplanned interim analysis results of the PRODIGE 4/ACCORD 11 Trial. Presented at: ASCO Annual Meeting. Chicago, IL, USA, 4–8 June 2010.
   Google Scholar
• 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. J. Clin. Oncol.3(3), 373–378 (1985).
   PubMed Web of Science ®Google Scholar
• 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. J. Can. Assoc. Radiol.32(3), 164–165 (1981).
   PubMedGoogle Scholar
• Gastrointestinal Tumor Study Group. Treatment of locally unresectable carcinoma of the pancreas: comparison of combined-modality therapy (chemotherapy plus radiotherapy) to chemotherapy alone. J. Natl Cancer Inst.80(10), 751–755 (1988).
   PubMed Web of Science ®Google Scholar
• Chauffert B, Mornex F, Bonnetain F 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. Ann. Oncol.19(9), 1592–1599 (2008).
   PubMed Web of Science ®Google Scholar
• Loehrer PJ PM. A randomized Phase III study of gemcitabine in comination with radiation therapy versus gemcitabine alone in patients with localized, unresectable pancreatic cancer: E4201. J. Clin. Oncol.26(Suppl.), (2008) (Abstract 4506).
   Google Scholar
• Huguet F, Girard N, Guerche CS, Hennequin C, Mornex F, Azria D. Chemoradiotherapy in the management of locally advanced pancreatic carcinoma: a qualitative systematic review. J. Clin. Oncol.27(13), 2269–2277 (2009).
   PubMed Web of Science ®Google Scholar
• Huguet F, Andre T, Hammel P et al. Impact of chemoradiotherapy after disease control with chemotherapy in locally advanced pancreatic adenocarcinoma in GERCOR Phase II and III studies. J. Clin. Oncol.25(3), 326–331 (2007).
   PubMed Web of Science ®Google Scholar
• Krishnan S, Rana V, Janjan NA et al. Induction chemotherapy selects patients with locally advanced, unresectable pancreatic cancer for optimal benefit from consolidative chemoradiation therapy. Cancer110(1), 47–55 (2007).
   PubMed Web of Science ®Google Scholar
• Willett CG, Lewandrowski K, Warshaw AL, Efird J, Compton CC. Resection margins in carcinoma of the head of the pancreas. Implications for radiation therapy. Ann. Surg.217(2), 144–148 (1993).
   PubMed Web of Science ®Google Scholar
• Cameron JL, Crist DW, Sitzmann JV et al. Factors influencing survival after pancreaticoduodenectomy for pancreatic cancer. Am. J. Surg.161(1), 120–124; discussion 124–125 (1991).
   PubMed Web of Science ®Google Scholar
• Raut CP, Evans DB, Crane CH, Pisters PW, Wolff RA. Neoadjuvant therapy for resectable pancreatic cancer. Surg. Oncol. Clin. N. Am.13(4), 639–661, ix (2004).
   PubMedGoogle Scholar
• Gray LH, Conger AD, Ebert M, Hornsey S, Scott OC. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br. J. Radiol.26(312), 638–648 (1953).
   PubMed Web of Science ®Google Scholar
• Ishikawa O, Ohigashi H, Imaoka S et al. Concomitant benefit of preoperative irradiation in preventing pancreas fistula formation after pancreatoduodenectomy. Arch. Surg.126(7), 885–889 (1991).
   PubMedGoogle Scholar
• Gillen S, Schuster T, Meyer Zum Buschenfelde C, Friess H, Kleeff J. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med.7(4), e1000267 (2010).
   PubMed Web of Science ®Google Scholar
• Katz MH, Pisters PW, Evans DB et al. Borderline-resectable pancreatic cancer: the importance of this emerging stage of disease. J. Am. Coll. Surg.206(5), 833–846; discussion 846–848 (2008).
   PubMed Web of Science ®Google Scholar
• Ammori JB, Colletti LM, Zalupski MM et al. Surgical resection following radiation therapy with concurrent gemcitabine in patients with previously unresectable adenocarcinoma of the pancreas. J. Gastrointest. Surg.7(6), 766–772 (2003).
   PubMed Web of Science ®Google Scholar
• Wilkowski R, Thoma M, Schauer R, Wagner A, Heinemann V. Effect of chemoradiotherapy with gemcitabine and cisplatin on locoregional control in patients with primary inoperable pancreatic cancer. World J. Surg.28(10), 1011–1018 (2004).
   PubMedGoogle Scholar
• Landry J, Catalano PJ, Staley C et al. Randomized Phase II study of gemcitabine plus radiotherapy versus gemcitabine, 5-fluorouracil, and cisplatin followed by radiotherapy and 5-fluorouracil for patients with locally advanced, potentially resectable pancreatic adenocarcinoma. J. Surg. Oncol.101(7), 587–592 (2010).
   PubMed Web of Science ®Google Scholar
• Brunner TB, Grabenbauer GG, Meyer T, Golcher H, Sauer R, Hohenberger W. Primary resection versus neoadjuvant chemoradiation followed by resection for locally resectable or potentially resectable pancreatic carcinoma without distant metastasis. A multi-centre prospectively randomised Phase II study of the Interdisciplinary Working Group Gastrointestinal Tumours (AIO, ARO, and CAO). BMC Cancer7, 41 (2007).
   PubMedGoogle Scholar
• Moore MJ, Goldstein D, Hamm J et al. Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a Phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J. Clin. Oncol.25(15), 1960–1966 (2007).
   PubMed Web of Science ®Google Scholar
• Kulke MH, Blaszkowsky LS, Ryan DP et al. Capecitabine plus erlotinib in gemcitabine-refractory advanced pancreatic cancer. J. Clin. Oncol.25(30), 4787–4792 (2007).
   PubMed Web of Science ®Google Scholar
• Philip PA, Benedetti J, Corless CL et al. Phase III study comparing gemcitabine plus cetuximab versus gemcitabine in patients with advanced pancreatic adenocarcinoma: Southwest Oncology Group-Directed Intergroup Trial S0205. J. Clin. Oncol.28(22), 3605–3610 (2010).
   PubMed Web of Science ®Google Scholar
• Kindler HL, Niedzwiecki D, Hollis D 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). J. Clin. Oncol.28(22), 3617–3622 (2010).
   PubMed Web of Science ®Google Scholar
• Philip PA, Mooney M, Jaffe D et al. Consensus report of the national cancer institute clinical trials planning meeting on pancreas cancer treatment. J. Clin. Oncol.27(33), 5660–5669 (2009).
   PubMed Web of Science ®Google Scholar
• Wang Z, Li Y, Kong D et al. Acquisition of epithelial–mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the Notch signaling pathway. Cancer Res.69(6), 2400–2407 (2009).
   PubMed Web of Science ®Google Scholar
• Shah AN, Summy JM, Zhang J, Park S, Parikh N, Gallick GE. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann. Surg. Oncol.14(12), 3629–3637 (2007).
   PubMed Web of Science ®Google Scholar
• Arumugam T, Ramachandran V, Fournier KF et al. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res.69(14), 5820–5828 (2009).
   PubMed Web of Science ®Google Scholar
• Buck E, Eyzaguirre A, Barr S et al. Loss of homotypic cell adhesion by epithelial–mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition. Mol. Cancer Ther.6(2), 532–541 (2007).
   PubMedGoogle Scholar
• Rasheed ZA, Yang J, Wang Q et al. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J. Natl Cancer Inst.102(5), 340–351 (2010).
   PubMed Web of Science ®Google Scholar
• Gregory PA, Bert AG, Paterson EL et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell. Biol.10(5), 593–601 (2008).
   PubMed Web of Science ®Google Scholar
• Peter ME. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle8(6), 843–852 (2009).
   PubMed Web of Science ®Google Scholar
• Olive KP, Jacobetz MA, Davidson CJ et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science324(5933), 1457–1461 (2009).
   PubMed Web of Science ®Google Scholar
• Drengler RL, Wood TE, Borad MJ et al. Phase I study of nab-paclitaxel and gemcitabine combination in patients with advanced pancreatic cancer. Presented at: ASCO Annual Meeting. Chicago, IL, USA, 30 May–3 June 2008.
   Google Scholar
• Gupta PB, Onder TT, Jiang G et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell138(4), 645–659 (2009).
   PubMed Web of Science ®Google Scholar
• Kim HJ, Czischke K, Brennan MF et al. Does neoadjuvant chemoradiation downstage locally advanced pancreatic cancer? J. Gastrointest. Surg.6(5), 763–769 (2002).
   PubMed Web of Science ®Google Scholar
• Massucco P, Capussotti L, Magnino A et al. Pancreatic resections after chemoradiotherapy for locally advanced ductal adenocarcinoma: analysis of perioperative outcome and survival. Ann. Surg. Oncol.13(9), 1201–1208 (2006).
   PubMed Web of Science ®Google Scholar
• Stokes JB, Nolan NJ, Stelow EB et al. Preoperative capecitabine and concurrent radiation for borderline resectable pancreatic cancer. Ann. Surg. Oncol.18(3), 619–627 (2011).
   PubMed Web of Science ®Google Scholar