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Review Article

Metabolic profile of oxazepam and related benzodiazepines: clinical and forensic aspects

Pages 451-463 | Received 25 Jul 2017, Accepted 03 Sep 2017, Published online: 14 Sep 2017

References

  • 1980. Systematic review of the benzodiazepines. Guidelines for data sheets on diazepam, chlordiazepoxide, medazepam, clorazepate, lorazepam, oxazepam, temazepam, triazolam, nitrazepam, and flurazepam. Committee on the review of medicines. Br Med J. 280:910–912.
  • al-Hadidi KA, Oliver JS. 1995. Stability of temazepam in blood. Sci Justice. 35:105–108.
  • Altamura AC, Moliterno D, Paletta S, Maffini M, Mauri MC, Bareggi S. 2013. Understanding the pharmacokinetics of anxiolytic drugs. Exp Opin Drug Metabol Toxicol. 9:423–440.
  • Alvan G, Odar-Cederlof I. 1978. The pharmacokinetic profile of oxazepam. Acta Psychiat Scand. 58:47–55.
  • Aso Y, Yoshioka S, Shibazaki T, Uchiyama M. 1988. The kinetics of the racemization of oxazepam in aqueous solution. ChemPharm Bull. 36:1834–1840.
  • Atanasov VN, Stoykova S, Runiov A, Dimitrova T, Aleksandrova D, Tsakovski S, Mitewa M. 2012. Stability of diazepam in blood samples at different storage conditions and in the presence of alcohol. Forensic Sci Int. 215:159–163.
  • Baselt RC. 2014. Disposition of drugs and toxic chemicals in man. Seal Beach (CA): Biomedical Publications.
  • Boudinot FD, Homon CA, Jusko WJ, Ruelius HW. 1985. Protein binding of oxazepam and its glucuronide conjugates to human albumin. Biochem Pharmacol. 34:2115–2121.
  • Boxenbaum HG, Geitner KA, Jack ML, Dixon WR, Spiegel HE, Symington J, Christian R, Moore JD, Weissman L, Kaplan SA. 1977. Pharmacokinetic and biopharmaceutic profile of chlordiazepoxide HC1 in healthy subjects: single-dose studies by the intravenous, intramuscular, and oral routes. J Pharmacokinet Biopharm. 5:3–23.
  • Breimer DD. 1979. Pharmacokinetics and metabolism of various benzodiazepines used as hypnotics. Br J Clin Pharmacol. 8:7S–13S.
  • Brunton LL, Knollman BC, Hilal-Dandan R. 2017. Goodman & Gilman’s – the pharmacological basis of therapeutics. New York: McGraw-Hill – Medical Publishing Division.
  • Chauvet A. 1995. Characterization of lorazepam and oxazepam by the thermal behavior of their degradation product. Ann Pharm Fr. 53:256–260.
  • Chin PK, Jensen BP, Larsen HS, Begg EJ. 2011. Adult age and ex vivo protein binding of lorazepam, oxazepam and temazepam in healthy subjects. Br J Clin Pharmacol. 72:985–989.
  • Chouinard G, Lefko-Singh K, Teboul E. 1999. Metabolism of anxiolytics and hypnotics: benzodiazepines, buspirone, zoplicone, and zolpidem. Cell Mol Neurobiol. 19:533–552.
  • Court MH, Duan SX, Guillemette C, Journault K, Krishnaswamy S, Von Moltke LL, Greenblatt DJ. 2002. Stereoselective conjugation of oxazepam by human UDP-glucuronosyltransferases (UGTs): S-oxazepam is glucuronidated by UGT2B15, while R-oxazepam is glucuronidated by UGT2B7 and UGT1A9. Drug Metab Disp. 30:1257–1265.
  • Court MH, Hao Q, Krishnaswamy S, Bekaii-Saab T, Al-Rohaimi A, von Moltke LL, Greenblatt DJ. 2004. UDP-glucuronosyltransferase (UGT) 2B15 pharmacogenetics: UGT2B15 D85Y genotype and gender are major determinants of oxazepam glucuronidation by human liver. J Pharmacol Exp Ther. 310:656–665.
  • Dinis-Oliveira RJ, Vieira DN, Magalhães T. 2016. Guidelines for collection of biological samples for clinical and forensic toxicological analysis. Forensic Sci Res. 1:42–51.
  • Dinis-Oliveira RJ. 2014. Metabolomics of drugs of abuse: a more realistic view of the toxicological complexity. Bioanalysis. 6:3155–3159.
  • Dinis-Oliveira RJ. 2015. Metabolomics of cocaine: implications in toxicity. Toxicol Mech Methods. 25:494–500.
  • Dinis-Oliveira RJ. 2016a. Metabolomics of Δ9-tetrahydrocannabinol: implications in toxicity. Drug Metab Rev. 48:80–87.
  • Dinis-Oliveira RJ. 2016b. Oxidative and non-oxidative metabolomics of ethanol. Curr Drug Metab. 17:327–335.
  • Dinis-Oliveira RJ. 2017. Metabolic profile of flunitrazepam: clinical and forensic toxicological aspects. Drug Metab Lett. [Epub ahead of print]. doi: 10.2174/1872312811666170407164216.
  • Diwan BA, Rice JM, Ward JM. 1986. Tumor-promoting activity of benzodiazepine tranquilizers, diazepam and oxazepam, in mouse liver. Carcinogenesis. 7:789–794.
  • Dixon RB, Mbeunkui F, Wiegel JV. 2015. Stability study of opioids and benzodiazepines in urine samples by liquid chromatography tandem mass spectrometry. J Anal Sci Technol. 6:17.
  • Dusci LJ, Good SM, Hall RW, Ilett KF. 1990. Excretion of diazepam and its metabolites in human milk during withdrawal from combination high dose diazepam and oxazepam. Br J Clin Pharmacol. 29:123–126.
  • El Mahjoub A, Staub C. 2000. Stability of benzodiazepines in whole blood samples stored at varying temperatures. J Pharm Biomed Anal. 23:1057–1063.
  • Fehske KJ, Muller WE, Wollert U. 1981. The location of drug binding sites in human serum albumin. Biochem Pharmacol. 30:687–692.
  • Frigerio A, Baker KM, Belvedere G. 1973. Gas chromatographic degradation of several drugs and their metabolites. Anal Chem. 45:1846–1851.
  • Fu S, Lewis J, Wang H, Keegan J, Dawson M. 2010. A novel reductive transformation of oxazepam to nordiazepam observed during enzymatic hydrolysis. J Anal Toxicol. 34:243–251.
  • Ghabrial H, Desmond PV, Watson KJ, Gijsbers AJ, Harman PJ, Breen KJ, Mashford ML. 1986. The effects of age and chronic liver disease on the elimination of temazepam. Eur J Clin Pharmacol. 30:93–97.
  • Golan DE, Armstrong EJ, Armstrong AW. 2017. Principles of pharmacology: the pathophysiologic basis of drug therapy. Philadelphia: Lippincott Williams & Wilkins.
  • Greenblatt DJ, Allen MD, Harmatz JS, Shader RI. 1980. Diazepam disposition determinants. Clin Pharmacol Ther. 27:301–312.
  • Greenblatt DJ, Divoll M, Harmatz JS, Shader RI. 1980. Oxazepam kinetics: effects of age and sex. J Pharmacol Exp Ther. 215:86–91.
  • Greenblatt DJ, Murray TG, Audet PR, Locniskar A, Koepke HH, Walker BR. 1983. Multiple-dose kinetics and dialyzability of oxazepam in renal insufficiency. Nephron. 34:234–238.
  • Greenblatt DJ, Shader RI, Koch-Weser J. 1975. Pharmacokinetics in clinical medicine: oxazepam versus other benzodiazepines. Dis Nerv Syst. 36:6–13.
  • Greenblatt DJ. 1981. Clinical pharmacokinetics of oxazepam and lorazepam. Clin Pharmacokinet. 6:89–105.
  • Griffin CE III, Kaye AM, Bueno FR, Kaye AD. 2013. Benzodiazepine pharmacology and central nervous system-mediated effects. Ochsner J. 13:214–223.
  • Griffin RJ, Burka LT, Cunningham ML. 1995. Activity of hepatic drug metabolizing enzymes following oxazepam-dosed feed treatment in B6C3F1 mice. Toxicol Lett. 76:251–256.
  • Griffin RJ, Burka LT, Demby KB. 1995. Oxidative biotransformation of oxazepam to reactive and nonreactive products in rat, mouse and human microsomes. Hum Exp Toxicol. 14:779–786.
  • Griffin RJ, Burka LT. 1995. Metabolism and elimination of oxazepam in F344 rats. Drug Metab Disp. 23:232–239.
  • Halapy E, Kreiger N, Cotterchio M, Sloan M. 2006. Benzodiazepines and risk for breast cancer. Ann Epidemiol. 16:632–636.
  • He X, Hesse LM, Hazarika S, Masse G, Harmatz JS, Greenblatt DJ, Court MH. 2009. Evidence for oxazepam as an in vivo probe of UGT2B15: oxazepam clearance is reduced by UGT2B15 D85Y polymorphism but unaffected by UGT2B17 deletion. Br J Clin Pharmacol. 68:721–730.
  • Hoffman RS, Howland MA, Lewin NA, Nelson LS, Goldfrank LR. 2014. Goldfrank’s toxicologic emergencies. New York: McGraw-Hill Education.
  • Howland RH. 2016. Safety and abuse liability of oxazepam: is this benzodiazepine drug underutilized? J Psychosoc Nurs Ment Health Serv. 54:22–25.
  • Inomata S, Nagashima A, Itagaki F, Homma M, Nishimura M, Osaka Y, Okuyama K, Tanaka E, Nakamura T, Kohda Y, et al. 2005. CYP2C19 genotype affects diazepam pharmacokinetics and emergence from general anesthesia. Clin Pharmacol Ther. 78:647–655.
  • Iqbal U, Nguyen PA, Syed-Abdul S, Yang HC, Huang CW, Jian WS, Hsu MH, Yen Y, Li YC. 2015. Is long-term use of benzodiazepine a risk for cancer? Medicine. 94:e483.
  • Japp M, Garthwaite K, Geeson AV, Osselton MD. 1988. Collection of analytical data for benzodiazepines and benzophenones. J Chromatogr. 439:317–339.
  • Karch SB, Drummer OH. 2016. Karch’s pathology of drug abuse. Boca Raton: CRC Press, Taylor & Francis Group.
  • Karmali RA, et al. 1979. The influence of diazepam administration in rats bearing the R3230AC mammary carcinoma. Prostaglandins Med. 3:193–198.
  • Katzung BG, Trevor AJ. 2015. Basic & clinical pharmacology. New York: McGraw-Hill.
  • Kelly E, Darke S, Ross J. 2004. A review of drug use and driving: epidemiology, impairment, risk factors and risk perceptions. Drug Alcohol Rev. 23:319–344.
  • Kleber RJ. 1980. Ketazolam compared to diazepam and placebo in the treatment of anxiety. J Int Med Res. 8:439–445.
  • Klotz U, Avant GR, Hoyumpa A, Schenker S, Wilkinson GR. 1975. The effects of age and liver disease on the disposition and elimination of diazepam in adult man. J Clin Invest. 55:347–359.
  • Knowles JA, Ruelius HW. 1972. Absorption and excretion of 7-chloro-1,3-dihydro-3-hydroxy-5-phenyl-2H-1,4-benzodiazepin-2-one (oxazepam) in humans. Determination of the drug by gas-liquid chromatography with electron capture detection. Arzneimittel-Forschung. 22:687–692.
  • Kosuge K, Jun Y, Watanabe H, Kimura M, Nishimoto M, Ishizaki T, Ohashi K. 2001. Effects of CYP3A4 inhibition by diltiazem on pharmacokinetics and dynamics of diazepam in relation to CYP2C19 genotype status. Drug Metab Disp. 29:1284–1289.
  • Kripke DF, Langer RD, Kline LE. 2012. Hypnotics' association with mortality or cancer: a matched cohort study. BMJ Open. 2:e000850.
  • Langner JG, Gan BK, Liu RH, Baugh LD, Chand P, Weng JL, Edwards C, Walia AS. 1991. Enzymatic digestion, solid-phase extraction, and gas chromatography/mass spectrometry of derivatized intact oxazepam in urine. Clin Chem. 37:1595–1601.
  • Lemke T, Williams D, Roche V. 2013. Foye's principles of medicinal chemistry. Philadelphia: Lippincott Williams & Wilkins.
  • Lu XL, Guengerich FP, Yang SK. 1991. Stereoselective metabolism of prazepam and halazepam by human liver microsomes. Drug Metab Dispos. 19:637–642.
  • Lu XL, Yang SK. 1990. Metabolism of halazepam by rat liver microsomes: stereoselective formation and N-dealkylation of 3-hydroxyhalazepam. Chirality. 2:1–9.
  • Lucek RW, Coutinho CB, Cheripko JA, Ryan J, Schwartz MA. 1975. Further studies on medazepam metabolism in the rat. Drug Metab Disp. 3:297–302.
  • Luk S, Atayee RS, Ma JD, Best BM. 2014. Urinary diazepam metabolite distribution in a chronic pain population. J Anal Toxicol. 38:135–142.
  • Mahon WA, Inaba T, Umeda T, Tsutsumi E, Stone R. 1976. Biliary elimination of diazepam in man. Clin Pharmacol Ther. 19:443–450.
  • Malamed SF. 2018. Sedation: a guide to patient management. St. Louis: Elsevier.
  • Mandrioli R, Mercolini L, Raggi MA. 2008. Benzodiazepine metabolism: an analytical perspective. Curr Drug Metab. 9:827–844.
  • Mandrioli R, Mercolini L, Raggi MA. 2010. Metabolism of benzodiazepine and non-benzodiazepine anxiolytic-hypnotic drugs: an analytical point of view. Curr Drug Metab. 11:815–829.
  • Marin SJ, Coles R, Merrell M, McMillin GA. 2008. Quantitation of benzodiazepines in urine, serum, plasma, and meconium by LC–MS–MS. J Anal Toxicol. 32:491–498.
  • Maurer H, Pfleger K. 1987. Identification and differentiation of benzodiazepines and their metabolites in urine by computerized gas chromatography-mass spectrometry. J Chromatogr. 422:85–101.
  • Meatherall R. 1994. Optimal enzymatic hydrolysis of urinary benzodiazepine conjugates. J Anal Toxicol. 18:382–384.
  • Melander A, Danielson K, Vessman J, Wahlin E. 1977. Bioavailability of oxazepam: absence of influence of food intake. Acta Pharmacol Toxicol. 40:584–588.
  • Melo P, Bastos ML, Teixeira HM. 2012. Benzodiazepine stability in postmortem samples stored at different temperatures. J Anal Toxicol. 36:52–60.
  • Miyawaki I, Moriyasu M, Funabashi H, Yasuba M, Matsuoka N. 2003. Mechanism of clobazam-induced thyroidal oncogenesis in male rats. Toxicol Lett. 145:291–301.
  • Mohler H, Okada T, Heitz P, Ulrich J. 1978. Biochemical identification of the site of action of benzodiazepines in human brain by 3H-diazepam binding. Life Sci. 22:985–995.
  • Norman TR, Fulton A, Burrows GD, Maguire KP. 1981. Pharmacokinetics of N-desmethyldiazepam after a single oral dose of clorazepate: the effect of smoking. Eur J Clin Pharmacol. 21:229–233.
  • Obach RS. 2013. Pharmacologically active drug metabolites: impact on drug discovery and pharmacotherapy. Pharmacol Rev. 65578–640.
  • Ochs HR, Greenblatt DJ, Allen MD, Harmatz JS, Shader RI, Bodem G. 1979. Effect of age and Billroth gastrectomy on absorption of desmethyldiazepam from clorazepate. Clin Pharmacol Ther. 26:449–456.
  • Odar-Cederlof I, Vessman J, Alvan G, Sjoqvist F. 1977. Oxazepam disposition in uremic patients. Acta Pharmacol Toxicol. 40(Suppl 1): 52–62.
  • Okamura T, Sugiura W, Miyazawa M. 1996. Reduction of oxazepam to desmethyldiazepam by human intestinal bacteria. Biol Pharm Bull. 19:647–648.
  • Ono S, Hatanaka T, Hotta H, Satoh T, Gonzalez FJ, Tsutsui M. 1996. Specificity of substrate and inhibitor probes for cytochrome P450s: evaluation of in vitro metabolism using cDNA-expressed human P450s and human liver microsomes. Xenobiotica. 26:681–693.
  • Ono S, Hatanaka T, Miyazawa S, Tsutsui M, Aoyama T, Gonzalez FJ, Satoh T. 1996. Human liver microsomal diazepam metabolism using cDNA-expressed cytochrome P450s: role of CYP2B6, 2C19 and the 3A subfamily. Xenobiotica. 26:1155–1166.
  • Ozdemir M, Aktan Y, Boydag BS, Cingi MI, Musmul A. 1998. Interaction between grapefruit juice and diazepam in humans. Eur J Drug Metab Pharmacokinet. 23:55–59.
  • Pacifici GM, Placidi GF. 1977. Rapid and sensitive electron-capture gas chromatographic method for the determination of pinazepam and its metabolites in human plasma, urine and milk. J Chromatogr. 135:133–139.
  • Pacifici GM, Placidi GF. 1982. First pass effect of pinazepam in the rabbit liver. Eur J Drug Metab Pharmacokinet. 7:119–122.
  • Parkinson A, Leonard N, Draper A, Ogilvie BW. 2006. On the mechanism of hepatocarcinogenesis of benzodiazepines: evidence that diazepam and oxazepam are CYP2B inducers in rats, and both CYP2B and CYP4A inducers in mice. Drug Metab Rev. 38:235–259.
  • Patel M, Tang BK, Kalow W. 1995. (S)oxazepam glucuronidation is inhibited by ketoprofen and other substrates of UGT2B7. Pharmacogenetics. 5:43–49.
  • Preat V, de Gerlache J, Lans M, Roberfroid M. 1987. Promoting effect of oxazepam in rat hepatocarcinogenesis. Carcinogenesis. 8:97–100.
  • Ries RK, Fiellin DA, Miller SC, Saitz R. 2014. Principles of addiction medicine. Philadelphia: Wolters Kluwer.
  • Rouini MR, Ardakani YH, Moghaddam KA, Solatani F. 2008. An improved HPLC method for rapid quantitation of diazepam and its major metabolites in human plasma. Talanta. 75:671–676.
  • Sakai N, Ishizuka M. 2009. Impact of rat P450 genetic polymorphism on diazepam metabolism. Exp Opin Drug Metab Toxicol. 5:1421–1433.
  • Schwartz MA, Carbone JJ. 1970. Metabolism of 14C-medazepam hydrochloride in dog, rat and man. Biochem Pharmacol. 19:343–361.
  • Schwartz MA, Kolis SJ. 1972. Pathways of medazepam metabolism in the dog and rat. J Pharmacol Exp Ther. 180:180–188.
  • Schwartz MA, Postma E. 1972. Metabolites of demoxepam, a chlordiazepoxide metabolite, in man. J Pharm Sci. 61:123–125.
  • Schwarz HJ. 1979. Pharmacokinetics and metabolism of temazepam in man and several animal species. Br J Clin Pharmacol. 8:23s–29s.
  • Scott AK, Khir AS, Bewsher PD, Hawksworth GM. 1984. Oxazepam pharmacokinetics in thyroid disease. Br J Clin Pharmacol. 17:49–53.
  • Shader RI, Georgotas A, Greenblatt DJ, Harmatz JS, Allen MD. 1978. Impaired absorption of desmethyldiazepam from clorazepate by magnesium aluminum hydroxide. Clin Pharmacol Ther. 24:308–315.
  • Shader RI, Greenblatt DJ, Ciraulo DA, Divoll M, Harmatz JS, Georgotas A. 1981. Effect of age and sex on disposition of desmethyldiazepam formed from its precursor clorazepate. Psychopharmacology. 75:193–197.
  • Shader RI, Pary RJ, Harmatz JS, Allison S, Locniskar A, Greenblatt DJ. 1984. Plasma concentrations and clinical effects after single oral doses of prazepam, clorazepate, and diazepam. J Clin Psychiatry. 45:411–413.
  • Shull HJ, Wilkinson GR, Johnson R, Schenker S. 1976. Normal disposition of oxazepam in acute viral hepatitis and cirrhosis. Ann Intern Med. 84:420–425.
  • Sisenwine SF, Tio CO, Liu AL, Politowski JF. 1987. The metabolic fate of oxazepam in mice. Drug Metab Disp. 15:579–580.
  • Sisenwine SF, Tio CO, Ruelius HW. 1970. The metabolic transformation of oxazepam in man, pig and rat. Pharmacologist. 22:272.
  • Sisenwine SF, Tio CO, Shrader SR, Ruelius HW. 1972. The biotransformation of oxazepam (7-chloro-1,3-dihydro-3-hydroxy-5-phenyl-2H-1,4-benzodiazepin-2-one) in man, miniature swine and rat. Arzneimittel-Forschung. 22:682–687.
  • Sisenwine SF, Tio CO. 1986. The metabolic disposition of oxazepam in rats. Drug Metab Disp. 14:41–45.
  • Sjodin T, Roosdorp N, Sjoholm I. 1976. Studies on the binding of benzodiazepines to human serum albumin by circular dichroism measurements. Biochem Pharmacol. 25:2131–2140.
  • Smink BE, Hofman BJ, Dijkhuizen A, Lusthof KJ, de Gier JJ, Egberts AC, Uges DR. 2008. The concentration of oxazepam and oxazepam glucuronide in oral fluid, blood and serum after controlled administration of 15 and 30 mg oxazepam. Br J Clin Pharmacol. 66:556–560.
  • Sonne J, Boesgaard S, Poulsen HE, Loft S, Hansen JM, Dossing M, Andreasen F. 1990. Pharmacokinetics and pharmacodynamics of oxazepam and metabolism of paracetamol in severe hypothyroidism. Br J Clin Pharmacol. 30:737–742.
  • Sonne J, Loft S, Dossing M, Vollmer-Larsen A, Olesen KL, Victor M, Andreasen F, Andreasen PB. 1988. Bioavailability and pharmacokinetics of oxazepam. Eur J Clin Pharmacol. 35:385–389.
  • Stebler T, Guentert TW. 1991. Determination of diazepam and nordazepam in milk and plasma in the presence of oxazepam and temazepam. J Chromatogr. 564:330–337.
  • Sternbach LH, Reeder E. 1961. Quinazolines and 1,4-benzodiazepines. II.1 the rearrangement of 6-chloro-2-chloromethyl-4-phenylquinazoline 3-oxide into 2-amino derivatives of 7-chloro-5-phenyl-3H-1,4-benzodiazepine 4-oxide. J Org Chem. 26:1111–1118.
  • Troupin AS, Friel P, Wilensky AJ, Morretti-Ojemann L, Levy RH, Feigl P. 1979. Evaluation of clorazepate (Tranxene) as an anticonvulsant-a pilot study. Neurology. 29:458–466.
  • Valavani P, Atta-Politou J, Panderi I. 2005. Development and validation of a liquid chromatographic/electrospray ionization mass spectrometric method for the quantitation of prazepam and its main metabolites in human plasma. J Mass Spectrom. 40:516–526.
  • Vida AJ. 1977. Anticonvulsants. New York: Academic Press.
  • Walkenstein SS, Wiser R, Gudmundsen CH, Kimmel HB, Corradino RA. 1964. Absorption, metabolism, and excretion of oxazepam and its succinate half-ester. J Pharm Sci. 53:1181–1186.
  • Wilensky AJ, Levy RH, Troupin AS, Moretti-Ojemann L. 1978. Clorazepate kinetics in treated epileptics. Clin Pharmacol Ther. 24:22–30.
  • Wretlind M. 1987. Excretion of oxazepam in breast milk. Eur J Clin Pharmacol. 33:209–210.
  • Wu F, Marin SJ, McMillin GA. 2016. Stability of 21 cocaine, opioid and benzodiazepine drug analytes in spiked meconium at three temperatures. J Anal Toxicol. 41:196–204.
  • Yang SK, Bao Z, Shou M. 1996. Stereoselective nucleophilic substitution of oxazepam and racemization in acidic methanol and ethanol. Chirality. 8:214–223.
  • Yang SK, Lu XL. 1989. Racemization kinetics of enantiomeric oxazepams and stereoselective hydrolysis of enantiomeric oxazepam 3-acetates in rat liver microsomes and brain homogenate. J Pharm Sci. 78:789–795.
  • Yang TJ, Krausz KW, Shou M, Yang SK, Buters JT, Gonzalez FJ, Gelboin HV. 1998. Inhibitory monoclonal antibody to human cytochrome P450 2B6. Biochem Pharmacol. 55:1633–1640.

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