227
Views
2
CrossRef citations to date
0
Altmetric
Perspective

Current synthetic pharmacotherapy for treatment-resistant colorectal cancer: when urgent action is required

&
Pages 523-534 | Received 13 Sep 2018, Accepted 16 Dec 2018, Published online: 08 Jan 2019

References

  • American Cancer Society. Global cancer facts & figures. 3rd ed.; 2012 [cited 2018 Nov 5]. Available from: https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/global-cancer-facts-and-figures/global-cancer-facts-and-figures-3rd-edition.pdf
  • International Agency for Research on Cancer. GLOBOCAN 2012: estimated cancer incidence, mortality and prevalence worldwide in 2012. Colorectum cancer fact sheets; [ cited 2018 Nov 5]. Available from: http://globocan.iarc.fr/Default.aspx
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018 Jan;68(1):7–30.
  • National Comprehensive Cancer Network. Colon cancer. Version 3; 2018 [cited 2018 Nov 5]. Available from: https://www.nccn.org/professionals/physician_gls/pdf/colon.pdf
  • Van Cutsem E, Cervantes A, Adam R, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016 Aug 1;27(8):1386–1422.
  • Davis LE. The evolution of biomarkers to guide the treatment of metastatic colorectal cancer. Am J Manag Care. 2018;24(7):S107–S117.
  • Rogers JE, Ohinata A, Dasari A, et al. Atypical metastatic presentations in colorectal cancer: a case series. Clin Colorectal Cancer. 2014 Mar;13(1):1–4.
  • Ciombor KK, Bekaii-Saab T. A comprehensive review of sequencing and combination strategies of targeted agents in metastatic colorectal cancer. Oncologist. 2018 Jan;23(1):25–34. PubMed Central PMCID: PMCPMC5759820.
  • Wolpin BM, Mayer RJ. Systemic treatment of colorectal cancer. Gastroenterology. 2008 May;134(5):1296–1310. PubMed Central PMCID: PMCPMC2528832.
  • 5-Fluorouracil package insert. Irvine, CA: Spectrum Pharmaceuticals, Inc.; 2016 Jul [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2016/012209s040lbl.pdf
  • Xeloda (Capecitabine) package insert. South San Francisco, CA: Genentech USA, Inc.; 2015 Mar [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/020896s037lbl.pdf
  • Camptosar (Irinotecan) package insert. New York, NY: Pfizer; 2014 Dec [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2014/020571s048lbl.pdf
  • Eloxatin (Oxaliplatin) package insert. Bridgewater, NJ: Sanofi-Aventis U.S. LLC; 2011 [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/021759s019lbledt.pdf
  • Avastin (Bevacizumab) package insert. South San Francisco, CA: Genentech, Inc; 2009 May [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2009/125085s0169lbl.pdf
  • Erbitux (Cetuximab) package insert. Indianapolis, IN: Bristol-Myers Squibb; 2012 Jan [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2012/125084s0228lbl.pdf
  • Vectibix (Panitumumab) package insert. Thousand Oaks, CA: Amgen; 2009 Jul [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2009/125147s080lbl.pdf
  • Cyramza (Ramucirumab) package insert. Indianapolis, IN: Eli Lilly and Company; 2014 Nov [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2014/125477s002lbl.pdf
  • Zaltrap (Ziv-aflibercept) package insert. Bridgewater, NJ: Snofi-Aventis U.S. LLC; 2012 Aug [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2012/125418s000lbl.pdf
  • Stivarga (Regorafenib) package insert. Wayne, NJ: Bayer HealthCare Pharmaceuticals Inc.; 2017 Apr [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2012/203085lbl.pdf
  • Lonsurf (Trifluridine-Tiparacil) package insert. Princeton, NJ: Taiho Oncology, Inc; 2015 Sep [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/207981s000lbl.pdf
  • Keytruda (Pembrolizumab) package insert. Whitehouse Station, NJ: Merck and Company, Inc; 2018 [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2016/125514s012lbl.pdf
  • Opdivo (Nivolumab) package insert. Princeton, NJ: Bristol-Myers Squibb; 2018 Aug [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/125554s058lbl.pdf
  • Yervoy (Ipilimumab) package insert. Princeton, NJ: Bristol-Myers Squibb; 2018 Jul [cited 2018 Aug 20]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/125377s073lbl.pdf
  • Cancer Stat Facts: Colorectal Cancer. Surveillance, Epidemiology, and End Results Program (SEER): National Cancer Institute; [ cited 2018 Jul 8]. Available from: https://seer.cancer.gov/statfacts/html/colorect.html
  • Cremolini C, Loupakis F, Antoniotti C, et al. FOLFOXIRI plus bevacizumab versus FOLFIRI plus bevacizumab as first-line treatment of patients with metastatic colorectal cancer: updated overall survival and molecular subgroup analyses of the open-label, phase 3 TRIBE study. Lancet Oncol. 2015 Oct;16(13):1306–1315.
  • Scott AJ, Lieu CH, Messersmith WA. Therapeutic approaches to RAS mutation. Cancer J. 2016 May–Jun;22(3):165–174. PubMed Central PMCID: PMCPMC4959441.
  • Pant S, Hubbard J, Martinelli E, et al. Clinical update on K-Ras targeted therapy in gastrointestinal cancers. Crit Rev Oncol Hematol. 2018 Oct;130:78–91.
  • Porru M, Pompili L, Carusco C, et al. Targeting KRAS in metastatic colorectal cancer: current strategies and emerging opportunities. J Exp Clin Cancer Res. 2018 Mar 13;37(1):57. PubMed Central PMCID: PMCPMC5850913.
  • Montalvo SK, Li L, Westover KD. Rationale for RAS mutation-tailored therapies. Future Oncol. 2017 Feb;13(3):263–271.
  • Hobbs GA, Der CJ, Rossman KL. RAS isoforms and mutations in cancer at a glance. J Cell Sci. 2017 Apr 1;129(7):1287–1292. PubMed Central PMCID: PMCPMC4869631.
  • Zhao B, Wang L, Qui H, et al. Mechanisms of resistance to anti-EGFR therapy in colorectal cancer. Oncotarget. 2017 Jan 17;8(3):3980–4000. PubMed Central PMCID: PMCPMC5354808.
  • Atreya CE, Corcoran RB, Kopetz S. Expanded RAS: refining the patient population. J Clin Oncol. 2015 Mar 1;33(7):682–685. PubMed Central PMCID: PMCPMC4334773.
  • Schirripa M, Lenz HJ. Biomarker in colorectal cancer. Cancer J. 2016 May–Jun;22(3):156–164. PubMed Central PMCID: PMCPMC4955946.
  • Venook A, Niedzwiecki D, Innocenti F, et al. Impact of primary (1º) tumor location on overall survival (OS) and progression-free survival (PFS) in patients (pts) with metastatic colorectal cancer (mCRC): analysis of CALGB/SWOG 80405 (Alliance). J Clin Oncol. 2016 May 20;35(15):3504.
  • Tejpar S, Stintzing S, Ciardiello F, et al. Prognostic and predictive relevance of primary tumor location in patients with RAS wild-type metastatic colorectal cancer: retrospective analyses of the CRYSTAL and FIRE-3 trials. JAMA Oncol. 2017 Feb;3(2):194–201.
  • Cohen R, Cervera P, Svrcek M, et al. BRAF-mutated colorectal cancer: what is the optimal strategy for treatment? Curr Treat Options Oncol. 2017;18(2):9.
  • Lai E, Pretta A, Impera V, et al. BRAF-mutant colorectal cancer, a different breed evolving. Expert Rec Mol Diagn. 2018 Jun;18(6):499–512.
  • Ursem C, Atreya CE, Van Loon K. Emerging treatment options for BRAF-mutant colorectal cancer. Gastrointest Cancer. 2018;8:13–23. PubMed Central PMCID: PMCPMC5889076.
  • Cremolini C, Loupakis F, Antoniotti C, et al. Early tumor shrinkage and depth of response predict long term outcome in metastatic colorectal cancer patients treated with first-line chemotherapy plus bevacizumab: results from phase III TRIBE trial by the Gruppo Onologico del Nord Ovest. Ann Oncol. 2015 Jun;26(6):1188–1194.
  • Kopetz S, McDonough SL, Lenz HJ, et al. Randomized trial of irinotecan and cetuximab with or without vemurafenib in BRAF-mutant metastatic colorectal cancer (SWOG S1406). J Clin Oncol. 2017 May 20;35(4):520.
  • ClinicalTrials.gov [Internet]. Identifier: NCT02928224 - study of encorafenib + cetuximab plus or minus binimetinib vs. irinotecan/cetuximab or infusional 5-fluorouracil (5-FU)/Folinic Acid (FA)/irinotecan (FOLFIRI)/cetuximab with a safety lead-in of encorafenib + binimetinib + cetuximab in patients with BRAF V600E-mutant metastatic colorectal cancer (BEACON CRC). Bethesda (MD): U.S. National Library of Medicine; 2016 Aug 16 [cited 2018 Aug 20]. Available from: https://clinicaltrials.gov/ct2/show/record/NCT02928224
  • The ASCO Post. FDA grants breakthrough therapy designation for encorafenib plus binimetinib and cetuximab in BRAF V600E–mutant metastatic colorectal cancer; 2018. [cited 2018 Aug 14]. Available from: http://www.ascopost.com/News/59160%20%20August%2014
  • Gao C, Hu J. Targeting parallel bypass signaling to combat adaptive resistance to BRAF inhibition in colorectal cancer. Oncoscience. 2018 Apr 29;5(3–4):57–58. PubMed Central PMCID: PMC PMC5978442.
  • Stein A, Folprecht G. Immunotherapy of colon cancer. Oncol Res Treat. 2018;41(5):282–285.
  • Lee JJ, Chu E. Recent advances in the clinical development of immune checkpoint blockade therapy for mismatch repair proficient (pMMR)/non-MSI-H metastatic colorectal cancer. Clin Colorectal Cancer. 2018 Dec;17(4):258–273. DOI:10.1016/j.clcc.2018.06.004
  • Kaylan A, Kircher S, Shah H, et al. Updates on immunotherapy for colorectal cancer. J Gastrointest Oncol. 2018 Feb;9(1):160–169. PubMed Central PMCID: PMCPMC5848033.
  • Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015 Jun 25;372(26):2509–2520. PubMed Central PMCID: PMCPMC4481136.
  • Le DT, Durham JN, Smith KN, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017 Jul 28;357(6349):409–413. PubMed Central PMCID: PMCPMC5576142.
  • Overman MJ, Ernstoff MS, Morse MA. Where we stand with immunotherapy in colorectal cancer: deficient mismatch repair, proficient mismatch repair, and toxicity management. ASCO Educ Book. 2018 May 23;38: 239–247. DOI:10.1200/EDBK_200821
  • Gelsomino F, Barbolini M, Spallanzani A, et al. The evolving role of microsatellite instability in colorectal cancer: a review. Cancer Treat Rev. 2016Dec;51:19–26.
  • Bever KM, Le DT. An expanding role for immunotherapy in colorectal cancer. J Natl Compr Canc Netw. 2017 March;15(3):401–410.
  • Overman MJ, McDermott R, Leach JL, et al. Nivolumab in patients with metastatic DNA mismatch repair-deficient or microsatellite instability-high colorectal cancer (CheckMate 142): an open-label, multicentre, phase 2 study. Lancet Oncol. 2017 Sep;18(9):1182–1191.
  • Overman MJ, Lonardi S, Wong KYM, et al. Durable clinical benefit with nivolumab plus ipilimumab in DNA mismatch repair-deficient/microsatellite instability-high metastatic colorectal cancer. J Clin Oncol. 2018 Mar 10;36(8):773–779.
  • Overman MJ, Bergamo F, McDermott RS, et al. Nivolumab in patients with DNA mismatch repair-deficient/microsatellite instability-high (dMMR/MSI-H) metastatic colorectal cancer (mCRC): long-term survival according to prior line of treatment from checkmate-142. J Clin Oncol. 2018 Feb 1;36(4):554.
  • ClinicalTrials.gov [Internet]. Identifier: NCT02563002 - study of pembrolizumab (MK-3475) vs standard therapy in participants with microsatellite instability-high (MSI-H) or mismatch repair deficient (dMMR) stage iv colorectal carcinoma (MK-3475-177/KEYNOTE-177). Bethesda (MD): U.S. National Library of Medicine; 2015 Sep 29 [cited 2018 Aug 20]. Available from: https://clinicaltrials.gov/ct2/show/NCT02563002
  • ClinicalTrials.gov [Internet]. Identifier: NCT02997228 - combination chemotherapy, bevacizumab, and/or atezolizumab in treating patients with deficient dna mismatch repair metastatic colorectal cancer. Bethesda (MD): U.S. National Library of Medicine; 2016 Dec 19 [cited 2018 Aug 20]. Available from: https://clinicaltrials.gov/ct2/show/record/NCT02997228
  • Takegawa N, Yonesaka K. HER2 as an emerging oncotarget for colorectal cancer treatment after failure of anti-epidermal growth factor receptor therapy. Clin Colorectal Cancer. 2017 Dec;16(4):247–251.
  • Siena S, Sartore-Bianchi A, Marsoni S, et al. Targeting the human epidermal growth factor receptor 2 (HER2) oncogene in colorectal cancer. Ann Oncol. 2018 May 1;5:1108–1119. PubMed Central PMCID: PMCPMC5961091. DOI:10.1093/annonc/mdy100
  • Sartore-Bianchi A, Trusolino L, Martino C, et al. Dual-targeted therapy with trastuzumab and lapatinib in treatment-refractory, KRAS codon 12/13 wild-type, HER2-positive metastatic colorectal cancer (HERACLES): a proof-of-concept, multicentre, open-label, phase 2 trial. Lancet Oncol. 2016 Jun;6:738–746. DOI:10.1016/S1470-2045(16)00150-9
  • Siena S, Sartore-Bianchi A, Trusolino L, et al. Abstract CT005: final results of the HERACLES trial in HER2-amplified colorectal cancer. Cancer Res. 2017 July;77(13):CT005.
  • Hainsworth JD, Meric-Bernstam F, Swanton C, et al. Targeted therapy for advanced solid tumors on the basis of molecular profiles: results from mypathway, an open-label, phase iia multiple basket study. J Clin Oncol. 2018 Feb 20;36(6):536–542.
  • Goodman A Dual HER2 Targeting of HER2-positive metastatic colorectal cancer shows clinical benefit. 2017 [cited 2017 Apr 25]. Available from: http://www.ascopost.com/issues/april-25-2017/dual-her2-targeting-of-her2-positive-metastatic-colorectal-cancer-shows-clinical-benefit/
  • ClinicalTrials.gov [Internet]. Identifier: NCT03365882- S1613, trastuzumab and pertuzumabor cetuximab and irinotecan hydrochloride in treating patients with locally advanced or metastatic HER2/neu amplified colorectal cancer that cannot be removed by surgery. Bethesda (MD): U.S. National Library of Medicine; 2018 [cited 2018 Aug 20]. Available from: https://clinicaltrials.gov/ct2/show/NCT03365882
  • ClinicalTrials.gov [Internet]. Identifier: NCT03043313 - tucatinib (ONT-380) and trastuzumab in treating patients with HER2+ metastatic colorectal cancer. Bethesda (MD): U.S. National Library of Medicine; 2017 Jan 31 [cited 2018 Aug 20]. Available from: https://clinicaltrials.gov/ct2/show/record/NCT03043313
  • Pulte D, Jansen L, Brenner H. Disparities in colon cancer survival by insurance type: a population-based analysis. Dis Colon Rectum. 2018 May;61(5):538–546.
  • Zhang Q, Wang Y, Hanqing H, et al. Impact of socioeconomic status on survival of colorectal cancer patients. Oncotarget. 2017 Dec 1;8(62):106121–106131. PubMed Central PMCID: PMCPMC5739706.
  • Riihimaki M, Hemminki A, Sundguist J, et al. Patterns of metastasis in colon and rectal cancer. Sci Rep. 2016 Jul;15(6):29765. PubMed Central PMCID: PMCPMC4945942.
  • Cavestro GM, Mannucci A, Zuppardo RA, et al. Early onset sporadic colorectal cancer: worrisome trends and oncogenic features. Dig Liver Dis. 2018 June;50(6):521–532.
  • Campos FG. Colorectal cancer in young adults: a difficult challenge. World J Gastroenterol. 2017 Juls 28;23(28):5041–5044.
  • Connell LC, Mota JM, Braghiroli MI, et al. The rising incidence of younger patients with colorectal cancer: questions about screening, biology, and treatment. Curr Treat Options Oncol. 2017 Apr;18(4):23.
  • Simon S Study finds sharp rise in colon cancer and rectal cancer rates among young adults: american cancer society; 2017. [cited 2018 May 30]. Available from: https://www.cancer.org/latest-news/study-finds-sharp-rise-in-colon-cancer-and-rectal-cancer-rates-among-young-adults.html
  • Bailey CE, Hu CY, You YN, et al. Increasing disparities in the age-related incidences of colon and rectal cancers in the United States, 1975–2010. JAMA Surg. 2015 Jan;150(1):17–22. PubMed Central PMCID: PMCPMC4666003.
  • Siegel RL, Fedewa SA, Anderson WF, et al. Colorectal cancer incidence patterns in the United States, 1974–2013. J Natl Cancer Inst. 2017 Aug;109(8). PubMed Central PMCID: PMCPMC6059239. DOI:10.1093/jnci/djw322
  • Lieu CH, Renfro LA, de Gramont A, et al. Association of age with survival i patients with metastatic colorectal cancer: analysis from the ARCAD clinical trials program. J Clin Oncol. 2014 Sep;32(27):2975–2982.
  • Esquivel J. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for colorectal cancer: survival outcomes and patient selection. J Gastrointest Oncol. 2016 Feb;7(1):72–78. PubMed Central PMCID: PMCPMC4754309.
  • Klaver CE, Groenen H, Morton DG, et al. Recommendations and consensus on the treatment of peritoneal metastases of colorectal origin: a systematic review of national and international guidelines. Colorectal Dis. 2017 Mar;19(3):224–236.
  • Quenet F, Elias D, Roca L, et al. A unicancer phase III trial of hyperthermic intra-peritoneal chemotherapy (HIPEC) for colorectal peritoneal carcinomatosis (PC): PRODIGE 7. J Clin Oncol. 2018;36:118.
  • Klaver CE, Musters GD, Bemelman WA, et al. Adjuvant hyperthermic intraperitoneal chemotherapy (HIPEC) in patients with colon cancer at high risk of peritoneal carcinomatosis; the COLOPEC randomized multicentre trial. BMC Cancer. 2015 May;24(15):428. PubMed Central PMCID: PMCPMC4492087.
  • Arjona-Sánchez A, Barrios P, Boldo-Roda E, et al. HIPECT4: multicentre, randomized clinical trial to evaluate safety and efficacy of hyperthermic intra-peritoneal chemotherapy (HIPEC) with mitomycin C used during surgery for treatment of locally advanced colorectal carcinoma. BMC Cancer. 2018 Feb 13;18(1):183. PubMed Central PMCID: PMCPMC5812226.
  • Dienstmann R, Vermeulen L, Guinney J, et al. Consensus molecular subtypes and the evolution of precision medicine in colorectal cancer. Nat Rev Cancer. 2017 Feb;17(2):79–92.
  • Nazemalhosseini ME, Kuppen PJ, Aghdaei HA, et al. The CpG island methylator phenotype (CIMP) in colorectal cancer. Gastroenterol Hepatol Bed Bench. 2013 Summer;6(3):120–128. PubMed Central PMCID: PMCPMC4017514.
  • Inamura K. Colorectal cancers: an update on their molecular pathology. Cancers (Basel). 2018 Jan 20;10(1):E26. PubMed Central PMCID: PMC PMC5789376.
  • Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012 Jul 18;487(7407):330–337.
  • Guinney J, Dienstmann R, Wang X, et al. The consensus molecular subtypes of colorectal cancer. Nat Med. 2015 Nov;21(11):1350–1356. PubMed Central PMCID: PMCPMC4636487.
  • Goldberg RM, Montagut C, Wainberg ZA, et al. Optimising the use of cetuximab in the continuum of care for patients with metastatic colorectal cancer. ESMO Open. 2018 May;3(4):e000353. PubMed Central PMCID: PMCPMC5950648.
  • Miyamoto Y, Suyama K, Baba H. Recent advances in targeting the egfr signaling pathway for the treatment of metastatic colorectal cancer. Int J Mol Sci. 2017 April 2;18(4):E752. PubMed Central PMCID: PMCPMC5412337.
  • Pietrantonio F, Vernieri C, Siravegna G, et al. Heterogeneity of acquired resistance to anti-EGFR monoclonal antibodies in patients with metastatic colorectal cancer. Clin Cancer Res. 2017 May 15;23(10):2414–2422.
  • Parseghian CM, Loree JM, Morris JK, et al. Anti-EGFR resistant clones decay exponentially after progression: implications for anti-EGFR rechallenge. J Clin Oncol. 2018 May 20;36(15):3511.
  • National Cancer Institute. The RAS Initiative. [ cited 2018 Aug 20]. Available from: https://www.cancer.gov/research/key-initiatives/ras
  • Van Sciver RE, Lee MP, Lee CD, et al. A new strategy to control and eradicate “undruggable” oncogenic k-ras-driven pancreatic cancer: molecular insights and core principles learned from developmental and evolutionary biology. Cancers (Basel). 2018;10(5):E142.
  • ClinicalTrials.gov [Internet]. Identifier: NCT03087071 - panitumumab in combination with trametinib in cetuximab-refractory stage IV colorectal cancer. Bethesda (MD): U.S. National Library of Medicine; 2017 Mar 10 [cited 2018 Aug 20]. Available from: https://clinicaltrials.gov/ct2/show/record/NCT03087071
  • Bendell JC, Bang Y, Chee CE, et al. A phase Ib study of safety and clinical activity of atezolizumab (A) and cobimetinib (C) in patients (pts) with metastatic colorectal cancer (mCRC). J Clin Oncol. 2018 Feb 26;36(4_suppl):560.
  • Bendell J, Ciardiello F, Tabernero J, et al. Efficacy and safety results from IMblaze370, a randomised phase III study comparing atezolizumab+cobimetinib and atezolizumab monotherapy vs regorafenib in chemotherapy-refractory metastatic colorectal cancer. Ann Oncol. 2018 Jun 24;29(suppl_5):mdy208.003.
  • Tabernero J, Melero I, Ros W, et al. Phase Ia and Ib studies of the novel carcinoembryonic antigen (CEA) T-cell bispecific (CEA CD3 TCB) antibody as a single agent and in combination with atezolizumab: preliminary efficacy and safety in patients with metastatic colorectal cancer (mCRC). J Clin Oncol. 2017 May 20;35(15_suppl):3002.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.