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Ursolic acid, a potential anticancer compound for breast cancer therapy

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  • Adams, L. S., Seeram, N. P., Aggarwal, B. B., Takada, Y., Sand, D. and Heber, D. (2006). Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells. J. Agric. Food Chem. 54:980–985.
  • Adlercreutz, H. and Mazur, W. (1997). Phyto-oestrogens and Western diseases. Ann. Med. 29:95–120.
  • Aggarwal, B. B. and Shishodia, S. (2006). Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 71:1397–1421.
  • Aune, D., Chan, D. S., Lau, R., Vieira, R., Greenwood, D. C., Kampman, E. and Norat, T. (2011). Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ. 343:d6617.
  • Bai, K. K., Yu, Z., Chen, F. L., Li, F., Li, W. Y. and Guo, Y. H. (2012a). Synthesis and evaluation of ursolic acid derivatives as potent cytotoxic agents. Bioorg. Med. Chem. Lett. 22:2488–2493.
  • Bai, K. K., Yu, Z., Chen, F. L., Li, F., Li, W. Y. and Guo, Y. H. (2012b). Synthesis and evaluation of ursolic acid derivatives as potent cytotoxic agents. Bioorg. Med. Chem. Lett. 22:2488–2493.
  • Belding, R. D., Blankenship, S. M., Young, E. and Leidy, R. B. (1998). Composition and variability of epicuticular waxes in apple cultivars. J. Am. Soc. Hort. Sci. 123:348–356.
  • Bensouici, C., Kabouche, A., Karioti, A., Ozturk, M., Duru, M. E., Bilia, A. R. and Kabouche, Z. (2016). Compounds from Sedum caeruleum with antioxidant, anticholinesterase, and antibacterial activities. Pharm. Biol. 54:174–179.
  • Betteridge, D. J. (2000). What is oxidative stress? Metab. Clin. Exp. 49:3–8.
  • Block, G., Patterson, B. and Subar, A. (1992). Fruit, vegetables, and cancer prevention: A review of the epidemiological evidence. Nutr. Cancer. 18:1–29.
  • Cai, Y., Luo, Q., Sun, M. and Corke, H. (2004). Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci. 74:2157–2184.
  • Cai, Y. F. and Huang, Q. S. (2012). Determination of oleanolic acid and ursolic acid in Damnacanthus indicus from different places by RP-hPLC. Zhong Yao Cai. 35:694–696.
  • Chakravarti, B., Maurya, R., Siddiqui, J. A., Bid, H. K., Rajendran, S. M., Yadav, P. P. and Konwar, R. (2012). In vitro anti-breast cancer activity of ethanolic extract of Wrightia tomentosa: Role of pro-apoptotic effects of oleanolic acid and urosolic acid. J. Ethnopharm. 142:72–79.
  • Chen, J., Wong, H. S. and Ko, K. M. (2015). Mitochondrial reactive oxygen species production mediates ursolic acid-induced mitochondrial uncoupling and glutathione redox cycling, with protection against oxidant injury in H9c2 cells. Food Funct. 6:549–557.
  • Chen, K., You, J., Tang, Y., Zhou, Y., Liu, P., Zou, D., Zhou, Q. C., Zhang, T., Zhu, J. D. and Mi, M. T. (2014). Supplementation of superfine powder prepared from Chaenomeles speciosa fruit increases endurance capacity in rats via antioxidant and Nrf2/ARE signaling pathway. Evidence-Based Complement. Alternat. Med.
  • Chen, Q., Luo, S., Zhang, Y. and Chen, Z. (2011). Development of a liquid chromatography-mass spectrometry method for the determination of ursolic acid in rat plasma and tissue: application to the pharmacokinetic and tissue distribution study. Anal. Bioanal. Chem. 399:2877–2884.
  • Corvinus, F. M., Orth, C., Moriggl, R., Tsareva, S. A., Wagner, S., Pfitzner, E. B., Baus, D., Kaufmann, R., Huber, L. A., Zatloukal, K., Beug, H., Öhlschläger, P., Schütz, A., Halbhuber, K. and Friedrich, K. (2005). Persistent STAT3 activation in colon cancer is associated with enhanced cell proliferation and tumor growth. Neoplasia. 7:545–555.
  • De Angel, R. E., Smith, S. M., Glickman, R. D., Perkins, S. N. and Hursting, S. D. (2010). Antitumor effects of ursolic acid in a mouse model of postmenopausal breast cancer. Nutr. Cancer. 62:1074–1086.
  • do Nascimento, P. G. G., Lemos, T. L. G., Bizerra, A. M. C., Arriaga, A. M. C., Ferreira, D. A., Santiago, G. M. P., Braz Filho, R. and Costa, J. G. M. (2014). Antibacterial and antioxidant activities of ursolic acid and derivatives. Molecules. 19:1317–1327.
  • Eberhardt, M. V., Lee, C. Y. and Liu, R. H. (2000). Antioxidant activity of fresh apples. Nature. 405:903–904.
  • Ercan, H., Birben, E., Dizdar, E. A., Keskin, O., Karaaslan, C., Soyer, O. U., Dut, R., Sackesen, C., Besler, T. and Kalayci, O. (2006). Oxidative stress and genetic and epidemiologic determinants of oxidant injury in childhood asthma. J. Allergy Clin. Immunol. 118:1097–1104.
  • Fearon, I. M. and Faux, S. P. (2009). Oxidative stress and cardiovascular disease: Novel tools give (free) radical insight. J. Mol. Cell. Cardiol. 47:372–381.
  • Frighetto, R. T. S., Welendorf, R. M., Nigro, E. N., Frighetto, N. and Siani, A. C. (2008). Isolation of ursolic acid from apple peels by high speed counter-current chromatography. Food Chem. 106:767–771.
  • Gao, Z., Huang, K., Yang, X. and Xu, H. (1999). Free radical scavenging and antioxidant activities of flavonoids extracted from the radix of Scutellaria baicalensis Georgi. Biochim. Biophys. Acta. 1472:643–650.
  • Gemenetzidis, E., Bose, A., Riaz, A. M., Chaplin, T., Young, B. D., Ali, M., Sugden, D., Thurlow, J. K., Cheong, S. C., Teo, S. H., Wang, H., Wassem, A., Parkinson, E. K., Fortune, F. and Teh, M. T. (2009). FOXM1 upregulation is an early event in human squamous cell carcinoma and it is enhanced by nicotine during malignant transformation. PLoS One. 4:e4849.
  • Genkinger, J. M., Platz, E. A., Hoffman, S. C., Comstock, G. W. and Helzlsouer, K. J. (2004). Fruit, vegetable, and antioxidant intake and all-cause, cancer, and cardiovascular disease mortality in a community-dwelling population in Washington County, Maryland. Am. J. Epidemiol. 160:1223–1233.
  • He, X. and Liu, R. H. (2007a). Triterpenoids isolated from apple peels have potent antiproliferative activity and may be partially responsible for apple's anticancer activity. J. Agric. Food Chem. 55:4366–4370.
  • He, X. J. and Liu, R. H. (2007b). Triterpenoids isolated from apple peels have potent antiproliferative activity and may be partially responsible for apple's anticancer activity. J. Agric. Food Chem. 55:4366–4370.
  • Hsu, Y. L., Kuo, P. L. and Lin, C. C. (2004). Proliferative inhibition, cell-cycle dysregulation, and induction of apoptosis by ursolic acid in human non-small cell lung cancer A549 cells. Life Sci. 75:2303–2316.
  • Ikeda, Y., Murakami, A., Fujimura, Y., Tachibana, H., Yamada, K., Masuda, D., Hirano, K., Yamashita, S. and Ohigashi, H. (2007). Aggregated ursolic acid, a natural triterpenoid, induces IL-1beta release from murine peritoneal macrophages: Role of CD36. J. Immunol. 178:4854–4864.
  • Ikeda, Y., Murakami, A. and Ohigashi, H. (2008). Strain differences regarding susceptibility to ursolic acid-induced interleukin-1 beta release in murine macrophages. Life Sci. 83:43–49.
  • Jager, S., Trojan, H., Kopp, T., Laszczyk, M. N. and Scheffler, A. (2009). Pentacyclic triterpene distribution in various plants – rich sources for a new group of multi-potent plant extracts. Molecules. 14:2016–2031.
  • Jayaprakasam, B., Olson, L. K., Schutzki, R. E., Tai, M. H. and Nair, M. G. (2006). Amelioration of obesity and glucose intolerance in high-fat-fed C57BL/6 mice by anthocyanins and ursolic acid in Cornelian cherry (Cornus mas). J. Agric. Food Chem. 54:243–248.
  • Jezierska-Drutel, A., Rosenzweig, S. A. and Neumann, C. A. (2013). Role of oxidative stress and the microenvironment in breast cancer development and progression. Adv. Cancer Res. 119:107–125.
  • Jiang, X., Li, T. and Liu, R. H. (2016). 2α-Hydroxyursolic acid inhibited cell proliferation and induced apoptosis in MDA-MB-231 human breast cncer cells through p38/MAPK signal transduction pathway. J. Agric. Food Chem 64:1806–1816.
  • Kassi, E., Sourlingas, T. G., Spiliotaki, M., Papoutsi, Z., Pratsinis, H., Aligiannis, N. and Moutsatsou, P. (2009). Ursolic acid triggers appoptosis and Bcl-2 downregulation in MCF-7 breast cancer cells. Cancer Invest. 27:723–733.
  • Kim, K. H., Seo, H. S., Choi, H. S., Choi, I., Shin, Y. C. and Ko, S. G. (2011). Induction of apoptotic cell death by ursolic acid through mitochondrial death pathway and extrinsic death receptor pathway in MDA-MB-231 cells. Arch. Pharm. Res. 34:1363–1372.
  • Ko, E. Y. and Moon, A. (2015). Natural products for chemoprevention of breast cancer. J. Cancer Prev. 20:223–231.
  • Li, X., Wang, T. T., Zhou, B., Gao, W. Y., Cao, J. G. and Huang, L. Q. (2014). Chemical composition and antioxidant and anti-inflammatory potential of peels and flesh from 10 different pear varieties (Pyrus spp.). Food Chem. 152:531–538.
  • Liao, Q. F., Yang, W., Jia, Y., Chen, X. H., Gao, Q. T. and Bi, K. S. (2005). LC-MS determination and pharmacokinetic studies of ursolic acid in rat plasma after administration of the traditional Chinese medicinal preparation Lu-Ying extract. Yakugaku Zasshi-J. Pharm. Soc. Jap. 125:509–515.
  • Lin, Y., Vermeer, M. A. and Trautwein, E. A. (2011). Triterpenic acids present in Hawthorn lower plasma cholesterol by inhibiting intestinal ACAT activity in hamsters. Evidence Based Comp. Alternat. Med. 2011:1–9.
  • Liobikas, J., Majiene, D., Trumbeckaite, S., Kursvietiene, L., Masteikova, R., Kopustinskiene, D. M., Savickas, A. and Bernatoniene, J. (2011). Uncoupling and antioxidant effects of ursolic acid in isolated rat heart mitochondria. J. Nat. Prod. 74:1640–1644.
  • Liu, J. (1995). Pharmacology of oleanolic acid and ursolic acid. J. Ethnopharmacol. 49:57–68.
  • Liu, R. H. (2003). Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am. J. Clin. Nutr. 78:517S–520S.
  • Liu, R. H. (2004). Potential synergy of phytochemicals in cancer prevention: Mechanism of action. J. Nutr. 134:3479S–3485S.
  • Lu, J., Wu, D. M., Zheng, Y. L., Hu, B., Zhang, Z. F., Ye, Q., Liu, C. M., Shan, Q. and Wang, Y. J. (2010). Ursolic acid attenuates D-galactose-induced inflammatory response in mouse prefrontal cortex through inhibiting AGEs/RAGE/NF-kappa B pathway activation. Cereb. Cortex. 20:2540–2548.
  • Lv, Y. Y., Jin, Y., Han, G. Z., Liu, Y. X., Wu, T., Liu, P., Zhou, Q., Liu, K. X. and Sun, H. J. (2012). Ursolic acid suppresses IL-6 induced C-reactive protein expression in HepG2 and protects HUVECs from injury induced by CRP. Eur. J. Pharm Sci. 45:190–194.
  • Manu, K. A. and Kuttan, G. (2008). Ursolic acid induces apoptosis by activating p53 and caspase-3 gene expressions and suppressing NF-kappaB mediated activation of bcl-2 in B16F-10 melanoma cells. Int. Immunopharmacol. 8:974–981.
  • Martin-Aragon, S., de las Heras, B., Sanchez-Reus, M. I. and Benedi, J. (2001). Pharmacological modification of endogenous antioxidant enzymes by ursolic acid on tetrachloride-induced liver damage in rats and primary cultures of rat hepatocytes. Exp. Toxicol. Pathol. 53:199–206.
  • McGhie, T. K., Hudault, S., Lunken, R. C. M. and Christeller, J. T. (2012). Apple peels, from seven cultivars, have lipase-inhibitory activity and contain numerous ursenoic acids as identified by LC-ESI-QTOF-HRMS. J. Agric. Food Chem.. 60:482–491.
  • Mody, N., Parhami, F., Sarafian, T. A. and Demer, L. L. (2001). Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radical Biol. Med. 31:509–519.
  • Moloughney, J. G. and Weisleder, N. (2012). Poloxamer 188 (p188) as a membrane resealing reagent in biomedical applications. Recent Pat. Biotechnol. 6:200–211.
  • Najid, A., Simon, A., Cook, J., Chablerabinovitch, H., Delage, C., Chulia, A. J. and Rigaud, M. (1992). Characterization of ursolic acid as a lipoxygenase and cyclooxygenase inhibitor using macrophages, platelets and differentiated Hl-60 leukemic cells. Febs. Lett. 299:213–217.
  • Nanjo, F., Goto, K., Seto, R., Suzuki, M., Sakai, M. and Hara, Y. (1996). Scavenging effects of tea catechins and their derivatives on 1,1-diphenyl-2-picrylhydrazyl radical. Free Radical Biol. Med. 21:895–902.
  • Rai, S. N., Yadav, S. K., Singh, D. and Singh, S. P. (2016). Ursolic acid attenuates oxidative stress in nigrostriatal tissue and improves neurobehavioral activity in MPTP-induced Parkinsonian mouse model. J. Chem. Neuroanat. 71:41–49.
  • Ramachandran, S. and Prasad, N. R. (2008). Effect of ursolic acid, a triterpenoid antioxidant, on ultraviolet-B radiation-induced cytotoxicity, lipid peroxidation and DNA damage in human lymphocytes. Chem. Biol. Interact. 176:99–107.
  • Sanchez-Moreno, C., Larrauri, J. A. and Saura-Calixto, F. (1999). Free radical scavenging capacity and inhibition of lipid oxidation of wines, grape juices and related polyphenolic constituents. Food Res. Int. 32:407–412.
  • Sarbassov, D. D., Guertin, D. A., Ali, S. M. and Sabatini, D. M. (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 307:1098–1101.
  • Schwaiger, S., Zeller, I., Polzelbauer, P., Frotschnig, S., Laufer, G., Messner, B., Pieri, V., Stuppner, H. and Bernhard, D. (2011). Identification and pharmacological characterization of the anti-inflammatory principal of the leaves of dwarf elder (Sambucus ebulus L.). J. Ethnopharmacol. 133:704–709.
  • Shan, J. Z., Xuan, Y. Y., Ruan, S. Q. and Sun, M. (2011). Proliferation-inhibiting and apoptosis-inducing effects of ursolic acid and oleanolic acid on multi-drug resistance cancer cells in vitro. Chin. J. Integr. Med. 17:607–611.
  • Shanmugam, M. K., Dai, X., Kumar, A. P., Tan, B. K., Sethi, G. and Bishayee, A. (2013). Ursolic acid in cancer prevention and treatment: Molecular targets, pharmacokinetics and clinical studies. Biochem. Pharmacol. 85:1579–1587.
  • Shishodia, S., Majumdar, S., Banerjee, S. and Aggarwal, B. B. (2003). Ursolic acid inhibits nuclear factor-kappaB activation induced by carcinogenic agents through suppression of IkappaBalpha kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1. Cancer Res. 63:4375–4383.
  • Siegel, R. L., Fedewa, S. A., Miller, K. D., Goding-Sauer, A., Pinheiro, P. S., Martinez-Tyson, D. and Jemal, A. (2015). Cancer statistics for Hispanics/Latinos. CA Cancer J. Clin. 65:457–480.
  • Slavin, J., Jacobs, D. and Marquart, L. (1997). Whole-grain consumption and chronic disease: protective mechanisms. Nutr. Cancer. 27:14–21.
  • Song, Y. H., Jeong, S. J., Kwon, H. Y., Kim, B., Kim, S. H. and Yoo, D. Y. (2012). Ursolic acid from Oldenlandia diffusa induces apoptosis via activation of caspases and phosphorylation of glycogen synthase kinase 3 beta in SK-OV-3 ovarian cancer cells. Biol. Pharm. Bull. 35:1022–1028.
  • Sun, J. and Liu, R. H. (2008). Apple phytochemical extracts inhibit proliferation of estrogen-dependent and estrogen-independent human breast cancer cells through cell cycle modulation. J. Agric. Food Chem. 56:11661–11667.
  • Takada, K., Nakane, T., Masuda, K. and Ishii, H. (2010). Ursolic acid and oleanolic acid, members of pentacyclic triterpenoid acids, suppress TNF-alpha-induced E-selectin expression by cultured umbilical vein endothelial cells. Phytomedicine. 17:1114–1119.
  • Tan, K. W., Li, Y., Paxton, J. W., Birch, N. P. and Scheepens, A. (2013). Identification of novel dietary phytochemicals inhibiting the efflux transporter breast cancer resistance protein (BCRP/ABCG2). Food Chem. 138:2267–2274.
  • Terry, P., Giovannucci, E., Michels, K. B., Bergkvist, L., Hansen, H., Holmberg, L. and Wolk, A. (2001). Fruit, vegetables, dietary fiber, and risk of colorectal cancer. J. Natl. Cancer Inst. 93:525–533.
  • Tsai, S. J. and Yin, M. C. (2008). Antioxidative and anti-inflammatory protection of oleanolic acid and ursolic acid in PC12 cells. J. Food Sci. 73:H174–H178.
  • Tu, H. Y., Huang, A. M., Wei, B. L., Gan, K. H., Hour, T. C., Yang, S. C., Pu, Y. S. and Lin, C. N. (2009). Ursolic acid derivatives induce cell cycle arrest and apoptosis in NTUB1 cells associated with reactive oxygen species. Bioorg. Med. Chem. 17:7265–7274.
  • Waller, G. R., Jurzysta, M., Karns, T. K. B. and Geno, P. W. (1991). Isolation and Identification of ursolic acid from Coffea-Arabica L (coffee) leaves. In: ASIC (Association for Science and Information on Coffee): Proceedings of the 14th International Conference on Coffee Science, San Francisco, USA, 1991, pp. 245–257.
  • Wang, J. S., Ren, T. N. and Xi, T. (2012). Ursolic acid induces apoptosis by suppressing the expression of FoxM1 in MCF-7 human breast cancer cells. Med. Oncol. 29:10–15.
  • Wang, X., Zhang, F., Yang, L., Mei, Y., Long, H., Zhang, X., Zhang, J., Qimuge, S. and Su, X. (2011a). Ursolic acid inhibits proliferation and induces apoptosis of cancer cells in vitro and in vivo. J. Biomed. Biotechnol. 2011:419343.
  • Wang, Y. J., Lu, J., Wu, D. M., Zheng, Z. H., Zheng, Y. L., Wang, X. H., Ruan, J., Sun, X., Shan, Q. and Zhang, Z. F. (2011b). Ursolic acid attenuates lipopolysaccharide-induced cognitive deficits in mouse brain through suppressing p38/NF-kappaB mediated inflammatory pathways. Neurobiol. Learn Mem. 96:156–165.
  • Weickert, M. O., Mohlig, M., Schofl, C., Arafat, A. M., Otto, B., Viehoff, H., Koebnick, C., Kohl, A., Spranger, J. and Pfeiffer, A. F. (2006). Cereal fiber improves whole-body insulin sensitivity in overweight and obese women. Diabetes Care. 29:775–780.
  • Wolfe, K., Wu, X. and Liu, R. H. (2003). Antioxidant activity of apple peels. J. Agric. Food Chem. 51:609–614.
  • Wolfe, K., Kang, X., He, X., Dong, M., Zhang, Q. and Liu, R. H. (2008). Cellular antioxidant activity of common fruits. J. Agric. Food Chem. 6:8418–8426.
  • Xia, Y., Wei, G., Si, D. and Liu, C. (2011). Quantitation of ursolic acid in human plasma by ultra performance liquid chromatography tandem mass spectrometry and its pharmacokinetic study. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 879:219–224.
  • Xu, T., Wang, X., Zhong, B., Nurieva, R. I., Ding, S. and Dong, C. (2011). Ursolic acid suppresses interleukin-17 (IL-17) production by selectively antagonizing the function of RORgamma t protein. J. Biol. Chem. 286:22707–22710.
  • Yamaguchi, H., Noshita, T., Kidachi, Y., Umetsu, H., Hayashi, M., Komiyama, K., Funayama, S. and Ryoyama, K. (2008). Isolation of Ursolic Acid from apple peels and its specific efficacy as a potent antitumor agent. J. Health Sci. 54:654–660.
  • Yang, J. and Liu, R. H. (2009). Synergistic effect of apple extracts and quercetin 3-beta-d-glucoside combination on antiproliferative activity in MCF-7 human breast cancer cells in vitro. J. Agric. Food Chem. 57:8581–8586.
  • Yeh, C. T., Wu, C. H. and Yen, G. C. (2010). Ursolic acid, a naturally occurring triterpenoid, suppresses migration and invasion of human breast cancer cells by modulating c-Jun N-terminal kinase, Akt and mammalian target of rapamycin signaling. Mol. Nutr. Food Res. 54:1285–1295.
  • Yin, M. C., Lin, M. C., Mong, M. C. and Lin, C. Y. (2012a). Bioavailability, distribution, and antioxidative effects of selected triterpenes in mice. J. Agric. Food Chem. 60:7697–7701.
  • Yin, M. C., Lin, M. C., Mong, M. C. and Lin, C. Y. (2012b). Bioavailability, distribution, and antioxidative effects of selected triterpenes in mice. J. Agric. Food Chem. 60:7697–7701.
  • Yoon, H. and Liu, R. H. (2007). Effect of selected phytochemicals and apple extracts on NF-kappaB activation in human breast cancer MCF-7 cells. J. Agric. Food Chem. 55:3167–3173.
  • Yoon, H. and Liu, R. H. (2008). Effect of 2alpha-hydroxyursolic acid on NF-kappaB activation induced by TNF-alpha in human breast cancer MCF-7 cells. J. Agric. Food Chem. 56:8412–8417.
  • Zafra-Stone, S., Yasmin, T., Bagchi, M., Chatterjee, A., Vinson, J. A. and Bagchi, D. (2007). Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol. Nutr. Food Res. 51:675–683.
  • Zhang, T., Su, J., Wang, K., Zhu, T. and Li, X. (2014). Ursolic acid reduces oxidative stress to alleviate early brain injury following experimental subarachnoid hemorrhage. Neurosci. Lett. 579:12–17.
  • Zhao, C., Yin, S., Dong, Y., Guo, X., Fan, L., Ye, M. and Hu, H. (2013). Autophagy-dependent EIF2AK3 activation compromises ursolic acid-induced apoptosis through upregulation of MCL1 in MCF-7 human breast cancer cells. Autophagy. 9:196–207.
  • Zhou, X. J., Hu, X. M., Yi, Y. M., and Wan, J. (2009). Preparation and body distribution of freeze-dried powder of ursolic acid phospholipid nanoparticles. Drug Dev. Ind. Pharm. 35:305–310.

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