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Review

PARP Inhibitor Applicability: Detailed Assays for Homologous Recombination Repair Pathway Components

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Pages 165-180 | Published online: 24 Feb 2022

References

  • Chabner BA, Roberts TG Jr. Timeline: chemotherapy and the war on cancer. Nat Rev Cancer. 2005;5(1):65–72. doi:10.1038/nrc1529
  • Krause DS, Van Etten RA. Tyrosine kinases as targets for cancer therapy. N Engl J Med. 2005;353(2):172–187. doi:10.1056/NEJMra044389
  • Falzone L, Salomone S, Libra M. Evolution of cancer pharmacological treatments at the turn of the third millennium. Front Pharmacol. 2018;9:1300. doi:10.3389/fphar.2018.01300
  • Tsimberidou AM. Targeted therapy in cancer. Cancer Chemother Pharmacol. 2015;76(6):1113–1132. doi:10.1007/s00280-015-2861-1
  • Scott AM, Allison JP, Wolchok JD. Monoclonal antibodies in cancer therapy. Cancer Immun. 2012;12:14.
  • Chambon P, Weill JD, Mandel P. Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem Biophys Res Commun. 1963;11(1):39–43. doi:10.1016/0006-291x(63)90024-x
  • Curtin N. PARP inhibitors for anticancer therapy. Biochem Soc Trans. 2014;42(1):82–88. doi:10.1042/BST20130187
  • Durkacz BW, Omidiji O, Gray DA, Shall S. (ADP-ribose)n participates in DNA excision repair. Nature. 1980;283(5747):593–596. doi:10.1038/283593a0
  • O’Sullivan Coyne G, Chen AP, Meehan R, Doroshow JH. PARP inhibitors in reproductive system cancers: current use and developments. Drugs. 2017;77(2):113–130. doi:10.1007/s40265-016-0688-7
  • O’Connor MJ. Targeting the DNA damage response in cancer. Mol Cell. 2015;60(4):547–560. doi:10.1016/j.molcel.2015.10.040
  • Pearl LH, Schierz AC, Ward SE, Al-Lazikani B, Pearl FM. Therapeutic opportunities within the DNA damage response. Nat Rev Cancer. 2015;15(3):166–180. doi:10.1038/nrc3891
  • Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009;461(7267):1071–1078. doi:10.1038/nature08467
  • Friedberg EC. A brief history of the DNA repair field. Cell Res. 2008;18(1):3–7. doi:10.1038/cr.2007.113
  • Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem. 2004;73(1):39–85. doi:10.1146/annurev.biochem.73.011303.073723
  • Hakem R. DNA-damage repair; the good, the bad, and the ugly. EMBO J. 2008;27(4):589–605. doi:10.1038/emboj.2008.15
  • Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell. 2010;40(2):179–204. doi:10.1016/j.molcel.2010.09.019
  • Bader AS, Hawley BR, Wilczynska A, Bushell M. The roles of RNA in DNA double-strand break repair. Br J Cancer. 2020;122(5):613–623. doi:10.1038/s41416-019-0624-1
  • McCabe N, Turner NC, Lord CJ, et al. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res. 2006;66(16):8109–8115. doi:10.1158/0008-5472.CAN-06-0140
  • Caron MC, Sharma AK, O’Sullivan J, et al. Poly(ADP-ribose) polymerase-1 antagonizes DNA resection at double-strand breaks. Nat Commun. 2019;10(1):2954. doi:10.1038/s41467-019-10741-9
  • Chan CY, Tan KV, Cornelissen B. PARP inhibitors in cancer diagnosis and therapy. Clin Cancer Res. 2021;27(6):1585–1594. doi:10.1158/1078-0432.CCR-20-2766
  • Langelier MF, Planck JL, Roy S, Pascal JM. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science. 2012;336(6082):728–732. doi:10.1126/science.1216338
  • Langelier MF, Zandarashvili L, Aguiar PM, Black BE, Pascal JM. NAD(+) analog reveals PARP-1 substrate-blocking mechanism and allosteric communication from catalytic center to DNA-binding domains. Nat Commun. 2018;9(1):844. doi:10.1038/s41467-018-03234-8
  • Liu X, Shi Y, Maag DX, et al. Iniparib nonselectively modifies cysteine-containing proteins in tumor cells and is not a bona fide PARP inhibitor. Clin Cancer Res. 2012;18(2):510–523. doi:10.1158/1078-0432.CCR-11-1973
  • Murai J, Pommier Y. PARP trapping beyond homologous recombination and platinum sensitivity in cancers. Annu Rev Cancer Biol. 2019;3(1):131–150. doi:10.1146/annurev-cancerbio-030518-055914
  • Gourley C, Balmana J, Ledermann JA, et al. Moving from Poly (ADP-Ribose) polymerase inhibition to targeting DNA repair and DNA damage response in cancer therapy. J Clin Oncol. 2019;37(25):2257–2269. doi:10.1200/JCO.18.02050
  • Murai J, Huang SY, Das BB, et al. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 2012;72(21):5588–5599. doi:10.1158/0008-5472.CAN-12-2753
  • Nijman SM. Synthetic lethality: general principles, utility and detection using genetic screens in human cells. FEBS Lett. 2011;585(1):1–6. doi:10.1016/j.febslet.2010.11.024
  • Lord CJ, Ashworth A. PARP inhibitors: synthetic lethality in the clinic. Science. 2017;355(6330):1152–1158. doi:10.1126/science.aam7344
  • Miller RE, Leary A, Scott CL, et al. ESMO recommendations on predictive biomarker testing for homologous recombination deficiency and PARP inhibitor benefit in ovarian cancer. Ann Oncol. 2020;31(12):1606–1622. doi:10.1016/j.annonc.2020.08.2102
  • Radhakrishnan SK, Jette N, Lees-Miller SP. Non-homologous end joining: emerging themes and unanswered questions. DNA Repair (Amst). 2014;17:2–8. doi:10.1016/j.dnarep.2014.01.009
  • Lin KK, Harrell MI, Oza AM, et al. BRCA reversion mutations in circulating tumor DNA predict primary and acquired resistance to the PARP inhibitor rucaparib in high-grade ovarian carcinoma. Cancer Discov. 2019;9(2):210–219. doi:10.1158/2159-8290.CD-18-0715
  • Venkitaraman AR. Linking the cellular functions of BRCA genes to cancer pathogenesis and treatment. Annu Rev Pathol. 2009;4:461–487. doi:10.1146/annurev.pathol.3.121806.151422
  • den Brok WD, Schrader KA, Sun S, et al. Homologous recombination deficiency in breast cancer: a clinical review. Jco Precis Oncol. 2017;1. doi:10.1200/Po.16.00031
  • Hoppe MM, Sundar R, Tan DSP, Jeyasekharan AD. Biomarkers for homologous recombination deficiency in cancer. J Natl Cancer Inst. 2018;110(7):704–713. doi:10.1093/jnci/djy085
  • Swisher EM, Lin KK, Oza AM, et al. Rucaparib in relapsed, platinum-sensitive high-grade ovarian carcinoma (ARIEL2 Part 1): an international, multicentre, open-label, phase 2 trial. Lancet Oncol. 2017;18(1):75–87. doi:10.1016/S1470-2045(16)30559-9
  • U.S. Food & Drug Administration. List of cleared or approved companion diagnostic devices (in vitro and imaging tools). Available from: https://www.fda.gov/medical-devices/in-vitro-diagnostics/list-cleared-or-approved-companion-diagnostic-devices-in-vitro-and-imaging-tools. Accessed July 2021.
  • Swisher EM, Kwan TT, Oza AM, et al. Molecular and clinical determinants of response and resistance to rucaparib for recurrent ovarian cancer treatment in ARIEL2 (Parts 1 and 2). Nat Commun. 2021;12(1):2487. doi:10.1038/s41467-021-22582-6
  • Sharma P, Barlow WE, Godwin AK, et al. Impact of homologous recombination deficiency biomarkers on outcomes in patients with triple-negative breast cancer treated with adjuvant doxorubicin and cyclophosphamide (SWOG S9313). Ann Oncol. 2018;29(3):654–660. doi:10.1093/annonc/mdx821
  • Bhangoo MS, Costantini C, Clifford BT, et al. Biallelic deletion of PALB2 occurs across multiple tumor types and suggests responsiveness to Poly (ADP-ribose) polymerase inhibition. Jco Precis Oncol. 2017;1. doi:10.1200/Po.17.00043
  • Reiss KA, Mick R, O’Hara MH, et al. Phase II study of maintenance rucaparib in patients with platinum-sensitive advanced pancreatic cancer and a pathogenic germline or somatic variant in BRCA1, BRCA2, or PALB2. J Clin Oncol. 2021;39(22):2497–2505. doi:10.1200/JCO.21.00003
  • Mateo J, Porta N, Bianchini D, et al. Olaparib in patients with metastatic castration-resistant prostate cancer with DNA repair gene aberrations (TOPARP-B): a multicentre, open-label, randomised, phase 2 trial. Lancet Oncol. 2020;21(1):162–174. doi:10.1016/S1470-2045(19)30684-9
  • Tung NM, Robson ME, Ventz S, et al. TBCRC 048: phase II study of olaparib for metastatic breast cancer and mutations in homologous recombination-related genes. J Clin Oncol. 2020;38(36):4274–4282. doi:10.1200/JCO.20.02151
  • Yan H, Parsons DW, Jin G, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360(8):765–773. doi:10.1056/NEJMoa0808710
  • Sulkowski PL, Corso CD, Robinson ND, et al. 2-Hydroxyglutarate produced by neomorphic IDH mutations suppresses homologous recombination and induces PARP inhibitor sensitivity. Sci Transl Med. 2017;9(375). doi:10.1126/scitranslmed.aal2463
  • Eder JP, Doroshow DB, Do KT, et al. Clinical efficacy of olaparib in IDH1/IDH2-mutant mesenchymal sarcomas. Jco Precis Oncol. 2021;5:466–472. doi:10.1200/Po.20.00247
  • Coleman RL, Oza AM, Lorusso D, et al. Rucaparib maintenance treatment for recurrent ovarian carcinoma after response to platinum therapy (ARIEL3): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2017;390(10106):1949–1961. doi:10.1016/S0140-6736(17)32440-6
  • Telli ML, Timms KM, Reid J, et al. Homologous Recombination Deficiency (HRD) Score predicts response to platinum-containing neoadjuvant chemotherapy in patients with triple-negative breast cancer. Clin Cancer Res. 2016;22(15):3764–3773. doi:10.1158/1078-0432.CCR-15-2477
  • Mirza MR, Monk BJ, Herrstedt J, et al. Niraparib maintenance therapy in platinum-sensitive, recurrent ovarian cancer. N Engl J Med. 2016;375(22):2154–2164. doi:10.1056/NEJMoa1611310
  • Nguyen L, Martens JWM, Van Hoeck A, Cuppen E. Pan-cancer landscape of homologous recombination deficiency. Nat Commun. 2020;11(1):5584. doi:10.1038/s41467-020-19406-4
  • Lotan TL, Kaur HB, Salles DC, et al. Homologous recombination deficiency (HRD) score in germline BRCA2- versus ATM-altered prostate cancer. Mod Pathol. 2021;34(6):1185–1193. doi:10.1038/s41379-020-00731-4
  • Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature. 2013;500(7463):415–421. doi:10.1038/nature12477
  • Davies H, Glodzik D, Morganella S, et al. HRDetect is a predictor of BRCA1 and BRCA2 deficiency based on mutational signatures. Nat Med. 2017;23(4):517–525. doi:10.1038/nm.4292
  • Gulhan DC, Lee JJ, Melloni GEM, Cortes-Ciriano I, Park PJ. Detecting the mutational signature of homologous recombination deficiency in clinical samples. Nat Genet. 2019;51(5):912–919. doi:10.1038/s41588-019-0390-2
  • Wolf DM, Yau C, Sanil A, et al. DNA repair deficiency biomarkers and the 70-gene ultra-high risk signature as predictors of veliparib/carboplatin response in the I-SPY 2 breast cancer trial. NPJ Breast Cancer. 2017;3(1):31. doi:10.1038/s41523-017-0025-7
  • Sakai W, Swisher EM, Karlan BY, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008;451(7182):1116–1120. doi:10.1038/nature06633
  • Edwards SL, Brough R, Lord CJ, et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature. 2008;451(7182):1111–1115. doi:10.1038/nature06548
  • Dias MP, Moser SC, Ganesan S, Jonkers J. Understanding and overcoming resistance to PARP inhibitors in cancer therapy. Nat Rev Clin Oncol. 2021. doi:10.1038/s41571-021-00532-x
  • Pettitt SJ, Frankum JR, Punta M, et al. Clinical BRCA1/2 reversion analysis identifies hotspot mutations and predicted neoantigens associated with therapy resistance. Cancer Discov. 2020;10(10):1475–1488. doi:10.1158/2159-8290.CD-19-1485
  • Kondrashova O, Nguyen M, Shield-Artin K, et al. Secondary somatic mutations restoring RAD51C and RAD51D associated with acquired resistance to the PARP inhibitor rucaparib in high-grade ovarian carcinoma. Cancer Discov. 2017;7(9):984–998. doi:10.1158/2159-8290.CD-17-0419
  • Goodall J, Mateo J, Yuan W, et al. Circulating cell-free DNA to guide prostate cancer treatment with PARP inhibition. Cancer Discov. 2017;7(9):1006–1017. doi:10.1158/2159-8290.CD-17-0261
  • Christie EL, Fereday S, Doig K, Pattnaik S, Dawson SJ, Bowtell DDL. Reversion of BRCA1/2 germline mutations detected in circulating tumor DNA from patients with high-grade serous ovarian cancer. J Clin Oncol. 2017;35(12):1274–1280. doi:10.1200/JCO.2016.70.4627
  • Weigelt B, Comino-Mendez I, de Bruijn I, et al. Diverse BRCA1 and BRCA2 reversion mutations in circulating cell-free DNA of therapy-resistant breast or ovarian cancer. Clin Cancer Res. 2017;23(21):6708–6720. doi:10.1158/1078-0432.CCR-17-0544
  • Mateo J, Carreira S, Sandhu S, et al. DNA-repair defects and olaparib in metastatic prostate cancer. N Engl J Med. 2015;373(18):1697–1708. doi:10.1056/NEJMoa1506859
  • Jaspers JE, Sol W, Kersbergen A, et al. BRCA2-deficient sarcomatoid mammary tumors exhibit multidrug resistance. Cancer Res. 2015;75(4):732–741. doi:10.1158/0008-5472.CAN-14-0839
  • Rottenberg S, Jaspers JE, Kersbergen A, et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci U S A. 2008;105(44):17079–17084. doi:10.1073/pnas.0806092105
  • Patch AM, Christie EL, Etemadmoghadam D, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521(7553):489–494. doi:10.1038/nature14410
  • Bouwman P, Aly A, Escandell JM, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol. 2010;17(6):688–695. doi:10.1038/nsmb.1831
  • Bunting SF, Callen E, Wong N, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 2010;141(2):243–254. doi:10.1016/j.cell.2010.03.012
  • Waks AG, Cohen O, Kochupurakkal B, et al. Reversion and non-reversion mechanisms of resistance to PARP inhibitor or platinum chemotherapy in BRCA1/2-mutant metastatic breast cancer. Ann Oncol. 2020;31(5):590–598. doi:10.1016/j.annonc.2020.02.008
  • Johnson N, Johnson SF, Yao W, et al. Stabilization of mutant BRCA1 protein confers PARP inhibitor and platinum resistance. Proc Natl Acad Sci U S A. 2013;110(42):17041–17046. doi:10.1073/pnas.1305170110
  • Graeser M, McCarthy A, Lord CJ, et al. A marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancer. Clin Cancer Res. 2010;16(24):6159–6168. doi:10.1158/1078-0432.CCR-10-1027
  • Chopra N, Tovey H, Pearson A, et al. Homologous recombination DNA repair deficiency and PARP inhibition activity in primary triple negative breast cancer. Nat Commun. 2020;11(1):2662. doi:10.1038/s41467-020-16142-7
  • Parmar K, Kochupurakkal BS, Lazaro JB, et al. The CHK1 inhibitor prexasertib exhibits monotherapy activity in high-grade serous ovarian cancer models and sensitizes to PARP inhibition. Clin Cancer Res. 2019;25(20):6127–6140. doi:10.1158/1078-0432.CCR-19-0448
  • Shah MM, Dobbin ZC, Nowsheen S, et al. An ex vivo assay of XRT-induced Rad51 foci formation predicts response to PARP-inhibition in ovarian cancer. Gynecol Oncol. 2014;134(2):331–337. doi:10.1016/j.ygyno.2014.05.009
  • AlHilli MM, Becker MA, Weroha SJ, et al. In vivo anti-tumor activity of the PARP inhibitor niraparib in homologous recombination deficient and proficient ovarian carcinoma. Gynecol Oncol. 2016;143(2):379–388. doi:10.1016/j.ygyno.2016.08.328
  • Castroviejo-Bermejo M, Cruz C, Llop-Guevara A, et al. A RAD51 assay feasible in routine tumor samples calls PARP inhibitor response beyond BRCA mutation. EMBO Mol Med. 2018;10(12):Dec. doi:10.15252/emmm.201809172
  • Wilsker DF, Barrett AM, Dull AB, et al. Evaluation of pharmacodynamic responses to cancer therapeutic agents using DNA damage markers. Clin Cancer Res. 2019;25(10):3084–3095. doi:10.1158/1078-0432.CCR-18-2523
  • Meijer TG, Verkaik NS, van Deurzen CHM, et al. Direct ex vivo observation of homologous recombination defect reversal after DNA-damaging chemotherapy in patients with metastatic breast cancer. Jco Precis Oncol. 2019;3. doi:10.1200/Po.18.00268
  • van Wijk LM, Vermeulen S, Meijers M, et al. The RECAP test rapidly and reliably identifies homologous recombination-deficient ovarian carcinomas. Cancers. 2020;12(10):2805. doi:10.3390/cancers12102805
  • Hill SJ, Decker B, Roberts EA, et al. Prediction of DNA repair inhibitor response in short-term patient-derived ovarian cancer organoids. Cancer Discov. 2018;8(11):1404–1421. doi:10.1158/2159-8290.CD-18-0474
  • Zellweger R, Dalcher D, Mutreja K, et al. Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells. J Cell Biol. 2015;208(5):563–579. doi:10.1083/jcb.201406099
  • Berti M, Teloni F, Mijic S, et al. Sequential role of RAD51 paralog complexes in replication fork remodeling and restart. Nat Commun. 2020;11(1):3531. doi:10.1038/s41467-020-17324-z
  • Le Page C, Amuzu S, Rahimi K, Gotlieb W, Ragoussis J, Tonin PN. Lessons learned from understanding chemotherapy resistance in epithelial tubo-ovarian carcinoma from BRCA1and BRCA2mutation carriers. Semin Cancer Biol. 2021;77:110–126. doi:10.1016/j.semcancer.2020.08.005
  • Murai J, Tang SW, Leo E, et al. SLFN11 blocks stressed replication forks independently of ATR. Mol Cell. 2018;69(3):371–384e6. doi:10.1016/j.molcel.2018.01.012
  • Murai J, Thomas A, Miettinen M, Pommier Y. Schlafen 11 (SLFN11), a restriction factor for replicative stress induced by DNA-targeting anti-cancer therapies. Pharmacol Ther. 2019;201:94–102. doi:10.1016/j.pharmthera.2019.05.009
  • Murai J, Feng Y, Yu GK, et al. Resistance to PARP inhibitors by SLFN11 inactivation can be overcome by ATR inhibition. Oncotarget. 2016;7(47):76534–76550. doi:10.18632/oncotarget.12266
  • Lok BH, Gardner EE, Schneeberger VE, et al. PARP inhibitor activity correlates with SLFN11 expression and demonstrates synergy with temozolomide in small cell lung cancer. Clin Cancer Res. 2017;23(2):523–535. doi:10.1158/1078-0432.CCR-16-1040
  • Stewart CA, Tong P, Cardnell RJ, et al. Dynamic variations in epithelial-to-mesenchymal transition (EMT), ATM, and SLFN11 govern response to PARP inhibitors and cisplatin in small cell lung cancer. Oncotarget. 2017;8(17):28575–28587. doi:10.18632/oncotarget.15338
  • Takashima T, Sakamoto N, Murai J, et al. Immunohistochemical analysis of SLFN11 expression uncovers potential non-responders to DNA-damaging agents overlooked by tissue RNA-seq. Virchows Arch. 2021;478(3):569–579. doi:10.1007/s00428-020-02840-6
  • Ngoi NYL, Tan DSP. The role of homologous recombination deficiency testing in ovarian cancer and its clinical implications: do we need it? ESMO Open. 2021;6(3):100144. doi:10.1016/j.esmoop.2021.100144
  • Hodgson DR, Dougherty BA, Lai Z, et al. Candidate biomarkers of PARP inhibitor sensitivity in ovarian cancer beyond the BRCA genes. Br J Cancer. 2018;119(11):1401–1409. doi:10.1038/s41416-018-0274-8
  • Wagener-Ryczek S, Merkelbach-Bruse S, Siemanowski J. Biomarkers for homologous recombination deficiency in cancer. J Pers Med. 2021;11(7):612. doi:10.3390/jpm11070612
  • Heeke AL, Pishvaian MJ, Lynce F, et al. Prevalence of homologous recombination-related gene mutations across multiple cancer types. Jco Precis Oncol. 2018;2018. doi:10.1200/PO.17.00286
  • Resolution liquid biopsy assay receives breakthrough device designation from FDA. Available from: https://www.resolutionbio.com/company/press/2019.05.30_resolution_fda_btd.html. Accessed January 27, 2022.
  • Williams PM, Forbes T, Lund SP, et al. Validation of ctDNA quality control materials through a precompetitive collaboration of the foundation for the National Institutes of Health. Jco Precis Oncol. 2021;5. doi:10.1200/PO.20.00528
  • Plummer R, Dua D, Cresti N, et al. First-in-human study of the PARP/tankyrase inhibitor E7449 in patients with advanced solid tumours and evaluation of a novel drug-response predictor. Br J Cancer. 2020;123(4):525–533. doi:10.1038/s41416-020-0916-5
  • Bang YJ, Im SA, Lee KW, et al. Randomized, double-blind phase ii trial with prospective classification by ATM protein level to evaluate the efficacy and tolerability of olaparib plus paclitaxel in patients with recurrent or metastatic gastric cancer. J Clin Oncol. 2015;33(33):3858–3865. doi:10.1200/JCO.2014.60.0320
  • Del Campo JM, Matulonis UA, Malander S, et al. Niraparib maintenance therapy in patients with recurrent ovarian cancer after a partial response to the last platinum-based chemotherapy in the ENGOT-OV16/NOVA trial. J Clin Oncol. 2019;37(32):2968–2973. doi:10.1200/JCO.18.02238