Advanced search
Publication Cover
Expert Opinion on Emerging Drugs Volume 12, 2007 - Issue 2
Submit an article Journal homepage
176
Views
18
CrossRef citations to date
0
Altmetric
Review

Luteinising hormone-releasing hormone antagonists in prostate cancer therapy

Pavlos Msaouel University of Athens, Department of Experimental Physiology, Medical School, 75 Micras Asias, Goudi-Athens, Greece +30 210 7462597; +30 210 7462571; [email protected]
,
Evanthia Diamanti National & Kapodistrian University of Athens, 1st Department of Internal Medicine, Laikon General University Hospital, Medical School, Goudi-Athens, Greece
,
Marinela Tzanela Evangelismos General Hospital,Endocrinology & Metabolism Clinic, Athens, Greece
&
Michael Koutsilieris University of Athens, Department of Experimental Physiology, Medical School, 75 Micras Asias, Goudi-Athens, Greece +30 210 7462597; +30 210 7462571; [email protected]
Pages 285-299 | Published online: 29 Jun 2007

Bibliography

  • ROUTH JC, LEIBOVICH BC: Adenocarcinoma of the prostate: epidemiological trends, screening, diagnosis and surgical management of localized disease. Mayo Clin. Proc. (2005) 80(7):899-907.
  • TOMLINS SA, MEHRA R, RHODES DR et al.: Integrative molecular concept modeling of prostate cancer progression. Nat. Genet. (2007) 39(1):41-51.
  • LIEBERMAN R: Androgen deprivation therapy for prostate cancer chemoprevention: current status and future directions for agent development. Urology (2001) 58(2 Suppl. 1):83-90.
  • KWAK C, JEONG SJ, PARK MS, LEE E, LEE SE: Prognostic significance of the nadir prostate specific antigen level after hormone therapy for prostate cancer. J. Urol. (2002) 168(3):995-1000.
  • EISENBERGER MA, BLUMENSTEIN BA, CRAWFORD ED et al.: Bilateral orchiectomy with or without flutamide for metastatic prostate cancer. N. Engl. J. Med. (1998) 339(15):1036-1042.
  • POUND CR, PARTIN AW, EISENBERGER MA et al.: Natural history of progression after PSA elevation following radical prostatectomy. JAMA (1999) 281(17):1591-1597.
  • JEMAL A, SIEGEL R, WARD E et al.: Cancer statistics, 2007. CA Cancer. J. Clin. (2007) 57(1):43-66.
  • BRESLOW N, CHAN CW, DHOM G et al.: Latent carcinoma of prostate at autopsy in seven areas. The International Agency for Research on Cancer, Lyons, France. Int. J. Cancer (1977) 20(5):680-688.
  • JEMAL A, CLEGG LX, WARD E et al.: Annual report to the nation on the status of cancer, 1975 - 2001, with a special feature regarding survival. Cancer (2004) 101(1):3-27.
  • WEIR HK, THUN MJ, HANKEY BF et al.: Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control. J. Natl. Cancer Inst. (2003) 95(17):1276-1299.
  • D'ANCONA FC, DEBRUYNE FM: Endocrine approaches in the therapy of prostate carcinoma. Hum. Reprod. Update (2005) 11(3):309-317.
  • ZEEGERS MP, JELLEMA A, OSTRER H: Empiric risk of prostate carcinoma for relatives of patients with prostate carcinoma: a meta-analysis. Cancer (2003) 97(8):1894-1903.
  • MILLER DC, HAFEZ KS, STEWART A, MONTIE JE, WEI JT: Prostate carcinoma presentation, diagnosis and staging: an update from the National Cancer Data Base. Cancer (2003) 98(6):1169-1178.
  • JANG TL, HAN M, ROEHLKA, HAWKINS SA, CATALONA WJ: More favorable tumor features and progression-free survival rates in a longitudinal prostate cancer screening study: PSA era and threshold-specific effects. Urology (2006) 67(2):343-348.
  • COLEMAN RE: Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin. Cancer Res. (2006) 12(20 Pt 2):6243s-6249s.
  • LABRIE F, DUPONT A, SUBURU R et al.: Optimized strategy for detection of early stage, curable prostate cancer: role of prescreening with prostate-specific antigen. Clin. Invest. Med. (1993) 16(6):425-439.
  • LABRIE F, DUPONT A, CUSAN L et al.: Downstaging of localized prostate cancer by neoadjuvant therapy with flutamide and lupron: the first controlled and randomized trial. Clin. Invest. Med. (1993) 16(6):499-509.
  • KOUTSILIERIS M, DUPONT A, GOMEZ J et al.: Stratification of stage D2 prostate cancer patients by a disease aggressiveness score and its use in evaluating disease response and outcome to combination hormonal treatment (GnRH-A plus flutamide). Anticancer Res. (1994) 14(2B):627-634.
  • BEHRAKIS P, KOUTSILIERIS M: Pulmonary metastases in metastatic prostate cancer: host tissue-tumor cell interactions and response to hormone therapy. Anticancer Res. (1997) 17(3A):1517-1518.
  • BOGDANOS J, KARAMANOLAKIS D, MILATHIANAKIS C et al.: Combined androgen blockade-induced anemia in prostate cancer patients without bone involvement. Anticancer Res. (2003) 23(2C):1757-1762.
  • POTOSKY AL, DAVIS WW, HOFFMAN RM et al.: Five-year outcomes after prostatectomy or radiotherapy for prostate cancer: the prostate cancer outcomes study. J. Natl. Cancer Inst. (2004) 96(18):1358-1367.
  • SCHERR D, SWINDLE PW, SCARDINO PT: National Comprehensive Cancer Network guidelines for the management of prostate cancer. Urology (2003) 61(2 Suppl. 1):14-24.
  • HUGGINS C, HODGES CV: Studies on prostatic cancer. 1. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. Cancer Research (1941) 1:293-297.
  • LOBLAW DA, MENDELSON DS, TALCOTT JA et al.: American Society of Clinical Oncology recommendations for the initial hormonal management of androgen-sensitive metastatic, recurrent, or progressive prostate cancer. J. Clin. Oncol. (2004) 22(14):2927-2941. [published erratum appears in J. Clin. Oncol. (2004) 22(21):4435].
  • DEBRUYNE FM: Gonadotropin-releasing hormone antagonist in the management of prostate cancer. Rev. Urol. (2004)(6 Suppl. 7):S25-S32.
  • LABRIE F, BELANGER A, LUU-THE V et al.: Gonadotropin-releasing hormone agonists in the treatment of prostate cancer. Endocr. Rev. (2005) 26(3):361-379.
  • MONGIAT-ARTUS P, TEILLAC P: Role of luteinising hormone releasing hormone (LHRH) agonists and hormonal treatment in the management of prostate cancer. Eur. Urol. Suppl. (2005) 4(5):4-13.
  • KOUTSILIERIS M, TZANELAM, DIMOPOULOS T: Novel concept of antisurvival factor (ASF) therapy produces an objective clinical response in four patients with hormone-refractory prostate cancer: Case report. Prostate (1999) 38(4):313-316.
  • KOUTSILIERIS M, MITSIADES C, DIMOPOULOS T et al.: A combination therapy of dexamethasone and somatostatin analog reintroduces objective clinical responses to LHRH analog in androgen ablation-refractory prostate cancer patients. J. Clin. Endocrinol. Metab. (2001) 86(12):5729-5736.
  • MITSIADES CS, KOUTSILIERIS M: Molecular biology and cellular physiology of refractoriness to androgen ablation therapy in advanced prostate cancer. Expert. Opin. Investig. Drugs (2001) 10(6):1099-1115.
  • BOGDANOS J, KARAMANOLAKIS D, TENTA R et al.: Endocrine/paracrine/autocrine survival factor activity of bone microenvironment participates in the development of androgen ablation and chemotherapy refractoriness of prostate cancer metastasis in skeleton. Endocr. Relat. Cancer (2003) 10(2):279-289.
  • KOUTSILIERIS M, MITSIADES CS, BOGDANOS J et al.: Combination of somatostatin analog, dexamethasone and standard androgen ablation therapy in stage D3 prostate cancer patients with bone metastases. Clin. Cancer Res. (2004) 10(13):4398-4405.
  • MITSIADES CS, MITSIADES N, KOUTSILIERIS M: The Akt pathway: molecular targets for anti-cancer drug development. Curr. Cancer Drug Targets (2004) 4(3):235-256.
  • DIMOPOULOS MA, KIAMOURIS C, GIKA D et al.: Combination of LHRH analog with somatostatin analog and dexamethasone versus chemotherapy in hormone-refractory prostate cancer: a randomized Phase II study. Urology (2004) 63(1):120-125.
  • TENTA R, SOTIRIOU E, PITULIS N, THYPHRONITIS G, KOUTSILIERIS M: Prostate cancer cell survival pathways activated by bone metastasis microenvironment. J. Musculoskelet. Neuronal Interact. (2005) 5(2):135-144.
  • DAMBER JE: Endocrine therapy for prostate cancer. Acta. Oncol. (2005) 44(6):605-609.
  • HIGANO CS: Side effects of androgen deprivation therapy: monitoring and minimizing toxicity. Urology (2003) 61(2 Suppl. 1):32-38.
  • VARENHORST E, WALLENTIN L, CARLSTROM K: The effects of orchidectomy, estrogens and cyproterone acetate on plasma testosterone, LH and FSH concentrations in patients with carcinoma of the prostate. Scand. J. Urol. Nephrol. (1982) 16(1):31-36.
  • BYAR DP, CORLE DK: Hormone therapy for prostate cancer: results of the Veterans Administration Cooperative Urological Research Group studies. NCI Monogr. (1988)(7):165-170.
  • HENRIKSSON P, BLOMBACK M, BRATT G et al.: Effects of oestrogen therapy and orchidectomy on coagulation and prostanoid synthesis in patients with prostatic cancer. Med. Oncol. Tumor Pharmacother. (1989) 6(3):219-225.
  • HEDLUND PO, ALA-OPAS M, BREKKAN E et al.: Parenteral estrogen versus combined androgen deprivation in the treatment of metastatic prostatic cancer – Scandinavian Prostatic Cancer Group (SPCG) Study No. 5. Scand. J. Urol. Nephrol. (2002) 36(6):405-413.
  • OCKRIM J, LALANI ELN, ABEL P: Therapy Insight: parenteral estrogen treatment for prostate cancer – a new dawn for an old therapy. Nat. Clin. Pract. Oncol. (2006) 3(10):552-563.
  • SCHALLY AV, NAIR RM, REDDING TW, ARIMURA A: Isolation of the luteinizing hormone and follicle-stimulating hormone-releasing hormone from porcine hypothalami. J. Biol. Chem. (1971) 246(23):7230-7236.
  • SCHALLY AV, KASTIN AJ, ARIMURA A: Hypothalamic follicle-stimulating hormone (FSH) and luteinizing hormone (LH)-regulating hormone: structure, physiology and clinical studies. Fertil. Steril. (1971) 22(11):703-721.
  • WECKERMANN D, HARZMANN R: Hormone therapy in prostate cancer: LHRH antagonists versus LHRH analogues. Eur. Urol. (2004) 46(3):279-283;
  • DENMEADE SR, ISAACS JT: Development of prostate cancer treatment: the good news. Prostate (2004) 58(3):211-224.
  • SEIDENFELD J, SAMSON DJ, HASSELBLAD V et al.: Single-therapy androgen suppression in men with advanced prostate cancer: a systematic review and meta-analysis. Ann. Intern. Med. (2000) 132(7):566-577. [published erratum appears in Ann. Intern. Med. (2005) 143(10):764-765].
  • BEN-JOSEF E, YANG SY, JI TH et al.: Hormone-refractory prostate cancer cells express functional follicle-stimulating hormone receptor (FSHR). J. Urol. (1999) 161(3):970-976.
  • BUBLEY GJ: Is the flare phenomenon clinically significant? Urology(2001) 58(2 Suppl. 1):5-9.
  • KEATING NL: O'MALLEY AJ, SMITH MR: Diabetes and cardiovascular disease during androgen deprivation therapy for prostate cancer. J. Clin. Oncol. (2006) 24(27):4448-4456.
  • SAMSON DJ, SEIDENFELD J, SCHMITT B et al.: Systematic review and meta-analysis of monotherapy compared with combined androgen blockade for patients with advanced prostate carcinoma. Cancer (2002) 95(2):361-376.
  • TAMMELA T: Endocrine treatment of prostate cancer. J. Steroid Biochem. Mol. Biol. (2004) 92(4):287-295.
  • MONGIAT-ARTUS P, TEILLAC P: Abarelix: the first gonadotrophin-releasing hormone antagonist for the treatment of prostate cancer. Expert Opin. Pharmacother. (2004) 5(10):2171-2179.
  • DIAMOND T, CAMPBELL J, BRYANT C, LYNCH W: The effect of combined androgen blockade on bone turnover and bone mineral densities in men treated for prostate carcinoma: longitudinal evaluation and response to intermittent cyclic etidronate therapy. Cancer (1998) 83(8):1561-1566.
  • ROTH CL, NEU C, JARRY H, SCHOENAU E: Different effects of agonistic vs. antagonistic GnRh-analogues (triptorelin vs. cetrorelix) on bone modeling and remodeling in peripubertal female rats. Exp. Clin. Endocrinol. Diabetes (2005) 113(8):451-456.
  • RATCLIFFE KE, FRASER HM, SELLAR R, RIVIER J, MILLAR RP: Bifunctional gonadotropin-releasing hormone antagonist-progesterone analogs with increased efficacy and duration of action. Endocrinology (2006) 147(1):571-579.
  • PADULA AM: GnRH analogues – agonists and antagonists. Anim. Reprod. Sci. (2005) 88(1-2):115-126.
  • BAJUSZ S, CSERNUS VJ, JANAKY T et al.: New antagonists of LHRH, II. Inhibition and potentiation of LHRH by closely related analogues. Int. J. Pept. Protein Res. (1988) 32(6):425-435.
  • ARMER RE, SMELT KH: Non-peptidic GnRH receptor antagonists. Curr. Med. Chem. (2004) 11(22):3017-3028.
  • KOSTANSKI JW, JIANG G, DANI BA et al.: Return to fertility. after extended chemical castration with a GnRH antagonist. BMC Cancer (2001) 1:18.
  • DU L, CHENG J, CHI Q et al.: Biodegradable PLGA microspheres as a sustained release system for a new luteinizing hormone-releasing hormone (LHRH) antagonist. Chem. Pharm. Bull (Tokyo) (2006) 54(9):1259-1265.
  • SHI Y, LI LC: Current advances in sustained-release systems for parenteral drug delivery. Expert Opin. Drug Deliv. (2005) 2(6):1039-1058.
  • MILLAR RP: GnRHs and GnRH receptors. Anim. Reprod. Sci. (2005) 88(1-2):5-28.
  • WILSON EM, FRENCH FS: Binding properties of androgen receptors. Evidence for identical receptors in rat testis, epididymis and prostate. J. Biol. Chem. (1976) 251(18):5620-5629.
  • PURVIS K, BREKKE I, RUI H, SUNDE A: 5 Alpha-reductase in the non-secretory cells of the rat ventral prostate epithelium. J. Steroid Biochem. (1986) 25(6):1023-1025.
  • LABRIE C, BELANGER A, LABRIE F: Androgenic activity of dehydroepiandrosterone and androstenedione in the rat ventral prostate. Endocrinology (1988) 123(3):1412-1417.
  • LABRIE F: Intracrinology. Mol. Cell. Endocrinol. (1991) 78(3):C113-C118.
  • LABRIE F, LUU-THE V, LABRIE C et al.: Endocrine and intracrine sources of androgens in women: inhibition f breast cancer and other roles of androgens and their precursor dehydroepiandrosterone. Endocr. Rev. (2003) 24(2):152-182.
  • GRUNDKER C, SCHLOTAWA L, VIERECK V et al.: Antiproliferative effects of the GnRH antagonist cetrorelix and of GnRH-II on human endometrial and ovarian cancer cells are not mediated through the GnRH type I receptor. Eur. J. Endocrinol. (2004) 151(1):141-149.
  • EICKE N, GUNTHERT AR, EMONS G, GRUNDKER C: GnRH-II agonist [D-Lys6]GnRH-II inhibits the EGF-induced mitogenic signal transduction in human endometrial and ovarian cancer cells. Int. J. Oncol. (2006) 29(5):1223-1229.
  • MAITI K, OH DY, MOON JS et al.: Differential effects of gonadotropin-releasing hormone (GnRH)-I and GnRH-II on prostate cancer cell signaling and death. J. Clin. Endocrinol. Metab. (2005) 90(7):4287-4298.
  • KANG SK, CHENG KW, NATHWANI PS, CHOI KC, LEUNG PC: Autocrine role of gonadotropin-releasing hormone and its receptor in ovarian cancer cell growth. Endocrine (2000) 13(3):297-304.
  • HALMOS G, ARENCIBIA JM, SCHALLY AV, DAVIS R, BOSTWICK DG: High incidence of receptors for luteinizing hormone-releasing hormone (LHRH) and LHRH receptor gene expression in human prostate cancers. J. Urol. (2000) 163(2):623-629.
  • HALMOS G, SCHALLY AV, PINSKI J, VADILLO-BUENFIL M, GROOT K: Down-regulation of pituitary receptors for luteinizing hormone-releasing hormone (LH-RH) in rats by LH-RH antagonist Cetrorelix. Proc. Natl. Acad. Sci. USA (1996) 93(6):2398-2402.
  • MURASE M, UEMURA T, GAO M et al.: GnRH antagonist-induced down-regulation of the mRNA expression of pituitary receptors: comparisons with GnRH agonist effects. Endocr. J. (2005) 52(1):131-137.
  • MAHLER C, VERHELST J, CHABAN M, DENIS L: Prolactin and pituitary gonadotropin values and responses to acute luteinizing hormone-releasing hormone (LHRH) challenge in patients having long-term treatment with a depot LHRH analogue. Cancer (1991) 67(3):557-559.
  • BEER TM, GARZOTTO M, EILERS KM, LEMMON D, WERSINGER EM: Targeting FSH in androgen-independent prostate cancer: abarelix for prostate cancer progressing after orchiectomy. Urology (2004) 63(2):342-347.
  • SULLIVAN SK, BROWN MS, GAO Y et al.: Allosteric and orthosteric binding modes of two nonpeptide human gonadotropin-releasing hormone receptor antagonists. Biochemistry (2006) 45(51):15327-15337.
  • GRIESINGER G, FELBERBAUM R, DIEDRICH K: GnRH-antagonists in reproductive medicine. Arch. Gynecol. Obstet. (2005) 273(2):71-78.
  • HOGLE WP: Abarelix (plenaxis). Clin. J. Oncol. Nurs. (2004) 8(6):663-665.
  • DEBRUYNE F, BHAT G, GARNICK MB: Abarelix for injectable suspension: first-in-class gonadotropin-releasing hormone antagonist for prostate cancer. Future Oncol. (2006) 2(6):677-696.
  • SELVAGGI FP, KHOE GSS, VAN CANGH P et al.: Comparison of abarelix depot (A-D) and goserelin (G) plus bicalutamide (B) in advanced prostate cancer: results of a multicentre, open-label, randomized, Phase III study. Proceedings of the 16th Congress of the European Association of Urology. Geneva, Switzerland (2001) .Eur. Urol. 39(Suppl. 5):S78.
  • MCLEOD D, ZINNER N, TOMERA K et al.: A Phase 3, multicenter, open-label, randomized study of abarelix versus leuprolide acetate in men with prostate cancer. Urology (2001) 58(5):756-761.
  • TRACHTENBERG J, GITTLEMAN M, STEIDLE C et al.: A Phase 3, multicenter, open label, randomized study of abarelix versus leuprolide plus daily antiandrogen in men with prostate cancer. J. Urol. (2002) 167(4):1670-1674.
  • KOCH M, STEIDLE C, BROSMAN S et al.: An open-label study of abarelix in men with symptomatic prostate cancer at risk of treatment with LHRH agonists. Urology (2003) 62(5):877-882.
  • BEER TM, GARZOTTO M, EILERS KM, LEMMON D: Phase II study of abarelix depot for androgen independent prostate cancer progression during gonadotropin-releasing hormone agonist therapy. J. Urol. (2003) 169(5):1738-1741.
  • BROQUA P, RIVIERE PJ, CONN PM et al.: Pharmacological profile of a new, potent and long-acting gonadotropin-releasing hormone antagonist: degarelix. J. Pharmacol. Exp. Ther. (2002) 301(1):95-102.
  • JADHAV PR, AGERSO H, TORNOE CW, GOBBURU JV: Semi-mechanistic pharmacodynamic modeling for degarelix, a novel gonadotropin releasing hormone (GnRH) blocker. J. Pharmacokinet. Pharmacodyn. (2006) 33(5):609-634.
  • VAN POPPEL H, DE LA ROSETTE J, PERSSON BE, JENSEN JK, OLESEN TK: A one-year, multicentre, randomized study of degarelix, a gonadotrophin-releasing hormone (GnRH) receptor blocker, in prostate cancer patients. Proceedings of the 21st Annual Meeting of the European Association of Urology (EAU). Paris, France (2006). Eur. Urol. 49(Suppl. 5):S251.
  • PRINCIVALLE M, BROQUA P, WHITE R et al.: Rapid suppression of plasma testosterone levels and tumor growth in the dunning rat model treated with degarelix, a new gonadotropin-releasing hormone antagonist. J. Pharmacol. Exp. Ther. (2007) 320(3):1113-1118.
  • GONZALEZ-BARCENA D, VADILLO-BUENFIL M, CORTEZ-MORALES A et al.: Luteinizing hormone-releasing hormone antagonist cetrorelix as primary single therapy in patients with advanced prostatic cancer and paraplegia due to metastatic invasion of spinal cord. Urology (1995) 45(2):275-281.
  • JUNGWIRTH A, GALVAN G, PINSKI J et al.: Luteinizing hormone-releasing hormone antagonist cetrorelix (SB-75) and bombesin antagonist RC-3940-II inhibit the growth of androgen-independent PC-3 prostate cancer in nude mice. Prostate (1997) 32(3):164-172.
  • MACLEAN C, ULYS A,JANKEVICIUS F, KANIUSAS D, DREWE J, LARSEN F: Efficacy and safety of teverelix, a new gonadotrophin releasing hormone antagonist in patients with advanced prostate cancer. Results from a Phase 2 multicentre, open-label, pilot study investigating an initial intramuscular loading dose regimen of teverelix. Proceedings of the 21st Annual Meeting of the European Association of Urology (EAU). Paris, France (2006). Eur. Urol. 49(Suppl. 5):S251.
  • CHO N, HARADA M, IMAEDA T et al.: Discovery of a novel, potent and orally active nonpeptide antagonist of the human luteinizing hormone-releasing hormone (LHRH) receptor. J. Med. Chem. (1998) 41(22):4190-4195.
  • STRUTHERS RS, CHEN T, CAMPBELL B et al.: Suppression of serum luteinizing hormone in postmenopausal women by an orally administered nonpeptide antagonist of the gonadotropin-releasing hormone receptor (NBI-42902). J. Clin. Endocrinol. Metab. (2006) 91(10): 3903-3907.
  • STRUTHERS RS, XIE Q, SULLIVAN SK et al.: Pharmacological characterization of a novel nonpeptide antagonist of the human gonadotropin-releasing hormone receptor, NBI-42902. Endocrinology (2006) 148(2):857-867.
  • CLARK E, BOYCE M, JOHNSTON A, GEORGE M, DAVIES J, HIBBERD M: Effects of repeated oral doses of TAK-013, a new non-peptide gonadotropin-releasing hormone (GnRH) antagonist, in healthy pre-menopausal women. Proceedings of the 58th Annual Meeting of the American Society for Reproductive Medicine (ASRM). Seattle, USA (2002). Fertil. Steril. 78(3 Suppl. 1):S280-S281.
  • MSAOUEL P, NIXON AM, BRAMOS AP, BAIBA E, KENTARCHOS NE: Extracellular calcium sensing receptor: an overview of physiology, pathophysiology and clinical perspectives. In Vivo (2004) 18(6):739-753.
  • REINHART GJ, XIE Q, LIU XJ et al.: Species selectivity of nonpeptide antagonists of the gonadotropin-releasing hormone receptor is determined by residues in extracellular loops II and III and the amino terminus. J. Biol. Chem. (2004) 279(33):34115-34122.
  • YANNUCCI J, MANOLA J, GARNICK MB, BHAT G, BUBLEY GJ: The effect of androgen deprivation therapy on fasting serum lipid and glucose parameters. J. Urol. (2006) 176(2):520-525.

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:

Order Reprints Request Corporate Permissions

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:

Request Academic Permissions

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.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.