A phase I study of docetaxel plus synthetic lycopene in metastatic prostate cancer patients.
docetaxel
lycopene
phase I trial
prostate cancer
Journal
Clinical and translational medicine
ISSN: 2001-1326
Titre abrégé: Clin Transl Med
Pays: United States
ID NLM: 101597971
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
revised:
20
02
2024
received:
17
11
2023
accepted:
25
02
2024
medline:
22
3
2024
pubmed:
22
3
2024
entrez:
22
3
2024
Statut:
ppublish
Résumé
Our preclinical studies showed that lycopene enhanced the anti-prostate cancer efficacy of docetaxel in animal models. A phase I trial (NCT0149519) was conducted to identify an optimum dose of synthetic lycopene in combination with docetaxel (and androgen blockade [androgen deprivation therapy, ADT]), and to evaluate its effect on the safety and pharmacokinetics of docetaxel in men with metastatic prostate cancer. Subjects were treated with 21-day cycles of 75 mg/m Twenty-four participants were enrolled, 18 in a dose escalation cohort to define the maximum tolerated dose (MTD), and six in a pharmacokinetic cohort. Docetaxel/ADT plus 150 mg/day synthetic lycopene resulted in dose-limiting toxicity (pulmonary embolus) in one out of 12 participants with an estimated probability of .106 and thus was chosen as the MTD. Lycopene increased the AUC The combination of docetaxel/ADT and synthetic lycopene has low toxicity and favourable pharmacokinetics. The effects of lycopene on biomarkers provide additional support for the toxicity-dependent MTD definition. The maximum tolerated dose was identified as 150 mg/day of lycopene in combination with docetaxel/ADT for the treatment of metastatic prostate cancer patients. Small increases in plasma exposure to docetaxel were observed with lycopene co-administration. Mechanistically significant effects were seen on angiogenesis and insulin-like growth factor 1 signalling by lycopene co-administration with docetaxel/ADT.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1627Subventions
Organisme : NCI NIH HHS
ID : 1R21CA166839
Pays : United States
Organisme : NCI NIH HHS
ID : 1R01CA260351
Pays : United States
Informations de copyright
© 2024 The Authors. Clinical and Translational Medicine published by John Wiley & Sons Australia, Ltd on behalf of Shanghai Institute of Clinical Bioinformatics.
Références
Tannock IF, de Wit R, Berry WR, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med. 2004;351:1502‐1512.
Kyriakopoulos CE, Chen YH, Carducci MA, et al. Chemohormonal therapy in metastatic hormone‐sensitive prostate cancer: long‐term survival analysis of the randomized phase III E3805 CHAARTED trial. J Clin Oncol. 2018;36:1080‐1087.
Fizazi K, Foulon S, Carles J, et al. Abiraterone plus prednisone added to androgen deprivation therapy and docetaxel in de novo metastatic castration‐sensitive prostate cancer (PEACE‐1): a multicentre, open‐label, randomized, phase 3 study with a 2 × 2 factorial design. Lancet. 2022;399:1695‐1707.
Hussain M, Tombal B, Saad F, et al. Darolutamide plus androgen‐deprivation therapy and docetaxel in metastatic hormone‐sensitive prostate cancer by disease volume and risk subgroups in the phase III ARASENS trial. J Clin Oncol. 2023;41(20):3595‐3607.
Corn PG, Agarwal N, Araujo JC, Sonpavde G. Taxane‐based combination therapies for metastatic prostate cancer. Eur Urol Focus. 2019;5:369‐380.
Seruga B, Tannock IF. Chemotherapy‐based treatment for castration‐resistant prostate cancer. J Clin Oncol. 2011;29:3686‐3694.
Beer TM, Ryan CW, Venner PM, et al. Double‐blinded randomized study of high‐dose calcitriol plus docetaxel compared with placebo plus docetaxel in androgen‐independent prostate cancer: a report from the ASCENT investigators. J Clin Oncol. 2007;25:669‐674.
Passildas‐Jahanmohan J, Eymard JC, Pouget M, et al. Multicenter randomized phase II study comparing docetaxel plus curcumin versus docetaxel plus placebo in first‐line treatment of metastatic castration‐resistant prostate cancer. Cancer Med. 2021;10:2332‐2340.
Martin MP, Borchiellini D, Thamphya B, et al. TAXOMET: a French prospective multicentric randomized phase II study of docetaxel plus metformin versus docetaxel plus placebo in metastatic castration‐resistant prostate cancer. Clin Genitourin Cancer. 2021;19:501‐509.
Clinton SK, Emenhiser C, Schwartz SJ, et al. cis‐trans lycopene isomers, carotenoids, and retinol in the human prostate. Cancer Epidemiol Biomarkers Prev. 1996;5:823‐833.
Giovannucci E, Ascherio A, Rimm EB, Stampfer MJ, Colditz GA, Willett WC. Intake of carotenoids and retinol in relation to risk of prostate cancer. J Natl Cancer Inst 1995;87:1767‐1776.
Etminan M, Takkouche B, Caamano‐Isorna F. The role of tomato products and lycopene in the prevention of prostate cancer: a meta‐analysis of observational studies. Cancer Epidemiol Biomarkers Prev. 2004;13:340‐345.
Wu K, Erdman JW Jr, Schwartz SJ, et al. Plasma and dietary carotenoids, and the risk of prostate cancer: a nested case‐control study. Cancer Epidemiol Biomarkers Prev. 2004;13:260‐269.
Kirsh VA, Mayne ST, Peters U, et al. A prospective study of lycopene and tomato product intake and risk of prostate cancer. Cancer Epidemiol Biomarkers Prev. 2006;15:92‐98.
Karppi J, Kurl S, Nurmi T, Rissanen TH, Pukkala E, Nyyssönen K. Serum lycopene and the risk of cancer: the Kuopio Ischaemic Heart Disease Risk Factor (KIHD) study. Ann Epidemiol. 2009;19:512‐518.
Giovannucci E. Does prostate‐specific antigen screening influence the results of studies of tomatoes, lycopene, and prostate cancer risk? J Natl Cancer Inst. 2007;99:1060‐1062.
Zu K, Mucci L, Rosner BA, et al. Dietary lycopene, angiogenesis, and prostate cancer: a prospective study in the prostate‐specific antigen era. J Natl Cancer Inst. 2014;106:djt430.
Giovannucci E. Commentary: serum lycopene and prostate cancer progression: a re‐consideration of findings from the prostate cancer prevention trial. Cancer Causes Control. 2011;22:1055‐1059.
Wang Y, Jacobs EJ, Newton CC, McCullough ML. Lycopene, tomato products and prostate cancer‐specific mortality among men diagnosed with nonmetastatic prostate cancer in the cancer prevention study II nutrition cohort. Int J Cancer. 2016;138:2846‐2855.
van Breemen RB, Sharifi R, Viana M, et al. Antioxidant effects of lycopene in African American men with prostate cancer or benign prostate hyperplasia: a randomized, controlled trial. Cancer Prev Res. 2011;4:711‐718.
Schwenke C, Ubrig B, Thürmann P, Eggersmann C, Roth S. Lycopene for advanced hormone‐refractory prostate cancer: a prospective, open phase II pilot study. J Urol. 2009;181:1098‐1103.
Kumar NB, Besterman‐Dahan K, Kang L, et al. Results of a randomized clinical trial of the action of several doses of lycopene in localized prostate cancer: administration prior to radical prostatectomy. Clin Med Urol. 2008;1:1‐14.
Jatoi A, Burch P, Hillman D, et al. A tomato‐based, lycopene‐containing intervention for androgen‐independent prostate cancer: results of a phase II study from the North Central Cancer Treatment Group. Urology. 2007;69:289‐294.
Clark PE, Hall MC, Borden LS Jr, et al. Phase I‐II prospective dose‐escalating trial of lycopene in patients with biochemical relapse of prostate cancer after definitive local therapy. Urology. 2006;67:1257‐1261.
Kucuk O, Sarkar FH, Sakr W, et al. Phase II randomized clinical trial of lycopene supplementation before radical prostatectomy. Cancer Epidemiol Biomarkers Prev. 2001;10:861‐868.
Chan JM, Elkin EP, Silva SJ, et al. Total and specific complementary and alternative medicine use in a large cohort of men with prostate cancer. Urology. 2005;66:1223‐1228.
Tang Y, Parmakhtiar B, Simoneau AR, et al. Lycopene enhances docetaxel's effect in castration‐resistant prostate cancer associated with insulin‐like growth factor I receptor levels. Neoplasia. 2011;13:108‐119.
Wertz K, Siler U, Goralczyk R. Lycopene: modes of action to promote prostate health. Arch Biochem Biophys. 2004;430:127‐134.
Tzelepi V, Efstathiou E, Wen S, et al. Persistent, biologically meaningful prostate cancer after 1 year of androgen ablation and docetaxel treatment. J Clin Oncol. 2011;29:2574‐2581.
Uzoh CC, Holly JM, Biernacka KM, et al. Insulin‐like growth factor‐binding protein‐2 promotes prostate cancer cell growth via IGF‐dependent or ‐independent mechanisms and reduces the efficacy of docetaxel. Br J Cancer. 2011;104:1587‐1593.
Lyman GH, Abelia E, Pettengell R. Risk factors for febrile neutropenia among patients with cancer receiving chemotherapy: a systematic review. Crit Rev Oncol Hematol. 2014;90:190‐199.
O'Quigley J, Pepe M, Fisher L. Continual reassessment method: a practical design for phase I clinical trials in cancer. Biometrics. 1990;46:33‐48.
Yin G, Yuan Y. Bayesian model averaging continual reassessment method in phase I clinical trials. J Am Stat Assoc. 2009;104:954‐968.
Fang L, Pajkovc N, Wang Y, Gu C, van Breemen RB. Quantitative analysis of lycopene isomers in human plasma using high‐performance liquid chromatography‐tandem mass spectrometry. Anal Chem. 2003;75:812‐817.
Ardiet CJ, Tranchand B, Zanetta S, et al. A sensitive docetaxel assay in plasma by solid‐phase extraction and high performance liquid chromatography‐UV detection: validation and suitability in phase I clinical trial pharmacokinetics. Invest New Drugs. 1999;17:325‐333.
Mariucci S, Rovati B, Bencardino K, Manzoni M, Danova M. Flow cytometric detection of circulating endothelial cells and endothelial progenitor cells in healthy subjects. Int J Lab Hematol. 2010;32(1 pt 1):e40‐e48.
R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. 2022. https://www.R‐project.org/
Lenth RV. Emmeans: Estimated Marginal Means, aka Least‐Squares Means. R package version 1.8.5. 2023. https://CRAN.R‐project.org/package=emmeans
Seah TC, Tay YL, Tan HK, et al. Determination of CYP3A4 inducing properties of compounds using a laboratory‐developed cell‐based assay. Int J Toxicol. 2015;34:454‐468.
Paolini M, Poul L, Berjaud C, et al. Nano‐sized cytochrome P450 3A4 inhibitors to block hepatic metabolism of docetaxel. Int J Nanomedicine. 2017;12:5537‐5556.
Oudard S, Fizazi K, Sengeløv L, et al. Cabazitaxel versus docetaxel as first‐line therapy for patients with metastatic castration‐resistant prostate cancer: a randomized phase III trial‐FIRSTANA. J Clin Oncol. 2017;35:3189‐3197.
Pan X, Niu X, Li Y, Yao Y, Han L. Preventive mechanism of lycopene on intestinal toxicity caused by cyclophosphamide chemotherapy in mice by regulating TLR4‐MyD88/TRIF‐TRAF6 signaling pathway and gut‐liver axis. Nutrients. 2022;14:4467.
Yucel Y, Tabur S, Gozeneli O, et al. The effects of lycopene on intestinal injury due to methotrexate in rats. Redox Rep. 2016;21:113‐118.
Chen ML, Lin YH, Yang CM, Hu ML. Lycopene inhibits angiogenesis both in vitro and in vivo by inhibiting MMP‐2/uPA system through VEGFR2‐mediated PI3K‐Akt and ERK/p38 signaling pathways. Mol Nutr Food Res. 2012;56:889‐899.
Calabrese EJ. Cancer biology and hormesis: human tumor cell lines commonly display hormetic (biphasic) dose responses. Crit Rev Toxicol. 2005;35:463‐582.
Anderson LM. Cancer biology and hormesis: comments on calabrese (2005). Crit Rev Toxicol. 2005;35:583‐586.
Borriello A, Bencivenga D, Caldarelli I, et al. Resveratrol and cancer treatment: is hormesis a yet unsolved matter? Curr Pharm Des. 2013;19:5384‐5393.
Sessa C, Lorusso P, Tolcher A, et al. Phase I safety, pharmacokinetic and pharmacodynamic evaluation of the vascular disrupting agent ombrabulin (AVE8062) in patients with advanced solid tumors. Clin Cancer Res. 2013;19:4832‐4842.
Alessio AM, Beltrame MP, Nascimento MC, et al. Circulating progenitor and mature endothelial cells in deep vein thrombosis. Int J Med Sci. 2013;10:1746‐1754.
Giordano G, Napolitano M, Cellurale M, et al. Circulating endothelial cell levels correlate with treatment outcomes of splanchnic vein thrombosis in patients with chronic myeloproliferative neoplasms. J Pers Med. 2022;12:364.
Goon PK, Lip GY, Stonelake PS, Blann AD. Circulating endothelial cells and circulating progenitor cells in breast cancer: relationship to endothelial damage/dysfunction/apoptosis, clinicopathologic factors, and the Nottingham Prognostic Index. Neoplasia. 2009;11:771‐779.
Malka D, Boige V, Jacques N, et al. Clinical value of circulating endothelial cell levels in metastatic colorectal cancer patients treated with first‐line chemotherapy and bevacizumab. Ann Oncol. 2012;23:919‐927.
Boos CJ, Balakrishnan B, Blann AD, Lip GY. The relationship of circulating endothelial cells to plasma indices of endothelial damage/dysfunction and apoptosis in acute coronary syndromes: implications for prognosis. J Thromb Haemost. 2008;6:1841‐1850.
Erdbruegger U, Woywodt A, Kirsch T, Haller H, Haubitz M. Circulating endothelial cells as a prognostic marker in thrombotic microangiopathy. Am J Kidney Dis. 2006;48:564‐570.
Yu EY, Li H, Higano CS, et al. A randomized phase II study of androgen deprivation combined with cixutumumab versus androgen deprivation alone in patients with new metastatic hormone‐sensitive prostate cancer. J Clin Oncol. 2015;33:1601‐1608.
Meyer HJ, Wienke A, Surov A. Incidental pulmonary embolism in oncologic patients—a systematic review and meta‐analysis. Support Care Cancer. 2021;29:1293‐1302.