In vitro Antifungal Effects of Berberine Against Candida spp. In Planktonic and Biofilm Conditions

References

• LockhartSR, GuarnerJ. Emerging and reemerging fungal infections. Semin Diagn Pathol. 2019;36:177–181. doi:10.1053/j.semdp.2019.04.01031010605
   PubMed Web of Science ®Google Scholar
• PappasPG, KauffmanCA, AndesDR, et al. Executive summary: clinical Practice guideline for the management of Candidiasis: 2016 update by the Infectious Diseases Society of America. Clin Infect Dis. 2016;62(4):409–417. doi:10.1093/cid/civ119426810419
   PubMed Web of Science ®Google Scholar
• PatilS, RaoRS, MajumdarB, AnilS. Clinical appearance of oral Candida infection and therapeutic strategies. Front Microbiol. 2015;6:1391. doi:10.3389/fmicb.2015.0139126733948
   PubMed Web of Science ®Google Scholar
• AlnuaimiAD, WiesenfeldD, O’Brien-SimpsonNM, ReynoldsEC, McCulloughMJ. Oral Candida colonization in oral cancer patients and its relationship with traditional risk factors of oral cancer: a matched case-control study. Oral Oncol. 2015;51(2):139–145. doi:10.1016/j.oraloncology.2014.11.00825498921
   PubMed Web of Science ®Google Scholar
• CalandraT, RobertsJA, AntonelliM, BassettiM, VincentJL. Diagnosis and management of invasive candidiasis in the ICU: an updated approach to an old enemy. Crit Care (London, England). 2016;20(1):125. doi:10.1186/s13054-016-1313-6
   PubMed Web of Science ®Google Scholar
• ColomboAL, GuimarãesT, SukienikT, et al. Prognostic factors and historical trends in the epidemiology of candidemia in 379 critically ill patients: an analysis of five multicenter studies sequentially conducted over a 9-year period. Intensive Care Med. 2014;40:1489–1498. doi:10.1007/s00134-014-3400-y25082359
   PubMed Web of Science ®Google Scholar
• LortholaryO, RenaudatC, SitbonK, et al. Worrisome trends in incidence and mortality of candidemia in intensive care units (Paris area, 2002–2010). Intensive Care Med. 2014;40:1303–1312. doi:10.1007/s00134-014-3408-325097069
   PubMed Web of Science ®Google Scholar
• BassettiM, MerelliM, RighiE, et al. Epidemiology, species distribution, antifungal susceptibility, and outcome of candidemia across five sites in Italy and Spain. J Clin Microbiol. 2013;51(12):4167–4172. doi:10.1128/JCM.01998-1324108614
   PubMed Web of Science ®Google Scholar
• LeroyO, BaillyS, GangneuxJP, et al. Systemic antifungal therapy for proven or suspected invasive candidiasis: the AmarCAND 2 study. Ann Intensive Care. 2016;6:2. doi:10.1186/s13613-015-0103-726743881
   PubMed Web of Science ®Google Scholar
• PappasPG, KauffmanCA, AndesDR, et al. Clinical practice guideline for the management of Candidiasis: 2016 update by the Infectious Diseases Society of America. Clin Infect Dis. 2016;62(4):e1–50. doi:10.1093/cid/civ119426679628
   PubMed Web of Science ®Google Scholar
• KoehlerP, StecherM, CornelyOA, et al. Morbidity and mortality of candidaemia in Europe: an epidemiologic meta-analysis. Clin Microbiol Infect. 2019;S1198-743X(19)30202-2. doi:10.1016/j.cmi.2019.04.024
   Web of Science ®Google Scholar
• KlingsporL, TortoranoAM, PemanJ, et al. Invasive Candida infections in surgical patients in intensive care units: a prospective, multicentre survey initiated by the European Confederation of Medical Mycology (ECMM) (2006-2008). Clin Microbiol Infect. 2015;21(1):87.e81–87.e10. doi:10.1016/j.cmi.2014.08.011
   PubMedGoogle Scholar
• MontagnaMT, LoveroG, BorghiE, et al. Candidemia in intensive care unit: a nationwide prospective observational survey (GISIA-3 study) and review of the European literature from 2000 through 2013. Eur Rev Med Pharmacol Sci. 2014;18(5):661–674. doi:10.1016/j.pnpbp.2013.11.01124668706
   PubMed Web of Science ®Google Scholar
• PristovKE, GhannoumMA. Resistance of Candida to azoles and echinocandins worldwide. Clin Microbiol Infect. 2019;25:792–798. doi:10.1016/j.cmi.2019.03.02830965100
   PubMed Web of Science ®Google Scholar
• PerlinDS, Rautemaa-RichardsonR, Alastruey-IzquierdoA. The global problem of antifungal resistance: prevalence, mechanisms, and management. Lancet Infect Dis. 2017;17(12):e383–e392. doi:10.1016/S1473-3099(17)30316-X28774698
   PubMed Web of Science ®Google Scholar
• CiceroAF, BaggioniA. Berberine and its role in chronic disease. Adv Exp Med Biol. 2016;928:27–45. doi:10.1007/978-3-319-41334-1_227671811
   PubMed Web of Science ®Google Scholar
• VollekovaA, Kost’alovaD, KettmannV, TothJ. Antifungal activity of Mahonia aquifolium extract and its major protoberberine alkaloids. Phytother Res. 2003;17(7):834–837. doi:10.1002/ptr.125612916091
   PubMed Web of Science ®Google Scholar
• WangJ, WangL, LouGH, et al. Coptidis Rhizoma: a comprehensive review of its traditional uses, botany, phytochemistry, pharmacology and toxicology. Pharm Biol. 2019;57(1):193–225. doi:10.1080/13880209.2019.157746630963783
   PubMed Web of Science ®Google Scholar
• WangK, FengX, ChaiL, CaoS, QiuF. The metabolism of berberine and its contribution to the pharmacological effects. Drug Metab Rev. 2017;49(2):139–157. doi:10.1080/03602532.2017.130654428290706
   PubMed Web of Science ®Google Scholar
• ImenshahidiM, HosseinzadehH. Berberine and barberry (Berberis vulgaris): a clinical review. Phytother Res. 2019;33(3):504–523. doi:10.1002/ptr.v33.330637820
   PubMed Web of Science ®Google Scholar
• XuJH, LiuXZ, PanW, ZouDJ. Berberine protects against diet-induced obesity through regulating metabolic endotoxemia and gut hormone levels. Mol Med Rep. 2017;15(5):2765–2787. doi:10.3892/mmr.2017.632128447763
   PubMed Web of Science ®Google Scholar
• IwazakiRS, EndoEH, Ueda-NakamuraT, NakamuraCV, GarciaLB, FilhoBP. In vitro antifungal activity of the berberine and its synergism with fluconazole. Antonie Van Leeuwenhoek. 2010;97(2):201–205. doi:10.1007/s10482-009-9394-819882381
   PubMed Web of Science ®Google Scholar
• WeiGX, XuX, WuCD. In vitro synergism between berberine and miconazole against planktonic and biofilm Candida cultures. Arch Oral Biol. 2011;56(6):565–572. doi:10.1016/j.archoralbio.2010.11.02121272859
   PubMed Web of Science ®Google Scholar
• HanY, LeeJH. Berberine synergy with amphotericin B against disseminated candidiasis in mice. Biol Pharm Bull. 2005;28(3):541–544. doi:10.1248/bpb.28.54115744087
   PubMed Web of Science ®Google Scholar
• ShaoJ, ShiG, WangT, WuD, WangC. Antiproliferation of Berberine in combination with fluconazole from the perspectives of reactive oxygen species, ergosterol and drug efflux in a fluconazole-resistant Candida tropicalis isolate. Front Microbiol. 2016;7:1516. doi:10.3389/fmicb.2016.0151627721812
   PubMed Web of Science ®Google Scholar
• ShiG, ShaoJ, WangT, WuD, WangC. Mechanism of berberine-mediated fluconazole-susceptibility enhancement in clinical fluconazole-resistant Candida tropicalis isolates. Biomed Pharmacother. 2017;93:709–712. doi:10.1016/j.biopha.2017.06.10628700974
   PubMed Web of Science ®Google Scholar
• Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Approved Standard M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute; 2008.
   Google Scholar
• PierceCG, UppuluriP, TristanAR, et al. A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc. 2008;3(9):1494–1500. doi:10.1038/nprot.2008.14118772877
   PubMed Web of Science ®Google Scholar
• Di VeroliGY, FornariC, GoldlustI, et al. An automated fitting procedure and software for dose-response curves with multiphasic features. Sci Rep. 2015;5:14701. doi:10.1038/srep1470126424192
   PubMed Web of Science ®Google Scholar
• MukherjeePK, ChandraJ. Candida biofilm resistance. Drug Resist Updat. 2004;7(4–5):301–309. doi:10.1016/j.drup.2004.09.00215533767
   PubMed Web of Science ®Google Scholar
• GulatiM, NobileCJ. Candida albicans biofilms: development, regulation, and molecular mechanisms. Microbes and Infection. 2016;18(5):310–321. doi:10.1016/j.micinf.2016.01.00226806384
   PubMed Web of Science ®Google Scholar
• NakamotoK, SadamoriS, HamadaT. Effects of crude drugs and berberine hydrochloride on the activities of fungi. J Prosthet Dent. 1990;64(6):691–694. doi:10.1016/0022-3913(90)90298-Q2079677
   PubMed Web of Science ®Google Scholar
• ParkKS, KangKC, KimJH, AdamsDJ, JohngTN, PaikYK. Differential inhibitory effects of protoberberines on sterol and chitin biosyntheses in Candida albicans. J Antimicrob Chemother. 1999;43(5):667–674. doi:10.1093/jac/43.5.66710382888
   PubMed Web of Science ®Google Scholar
• da SilvaAR, de Andrade NetoJB, da SilvaCR, et al. Berberine antifungal activity in fluconazole-resistant pathogenic yeasts: action mechanism evaluated by flow cytometry and biofilm growth inhibition in Candida spp. Antimicrob Agents Chemother. 2016;60(6):3551–3557. doi:10.1128/AAC.01846-1527021328
   PubMed Web of Science ®Google Scholar
• OrozcoAS, HigginbothamLM, HitchcockCA, et al. Mechanism of fluconazole resistance in Candida krusei. Antimicrob Agents Chemother. 1998;42(10):2645–2649. doi:10.1128/AAC.42.10.26459756770
   PubMed Web of Science ®Google Scholar
• GongJ, XiaoM, WangH, et al. Genetic differentiation, diversity, and drug susceptibility of Candida krusei. Front Microbiol. 2018;9:2717. doi:10.3389/fmicb.2018.0271730524386
   PubMed Web of Science ®Google Scholar
• ZhouP, FuJ, HuaH, LiuX. In vitro inhibitory activities of magnolol against Candida spp. Drug Des Devel Ther. 2017;11:2653–2661. doi:10.2147/DDDT.S146529
   PubMed Web of Science ®Google Scholar
• RamageG, Vande WalleK, WickesBL, Lopez-RibotJL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother. 2001;45(9):2475–2479. doi:10.1128/AAC.45.9.2475-2479.200111502517
   PubMed Web of Science ®Google Scholar
• RamageG, VandewalleK, WickesBL, López-RibotJL. Characteristics of biofilm formation by Candida albicans. Rev Iberoam Micol. 2001;18(4):163–170.15496122
   PubMedGoogle Scholar
• XuY, WangY, YanL, et al. Proteomic analysis reveals a synergistic mechanism of fluconazole and berberine against fluconazole-resistant Candida albicans: endogenous ROS augmentation. J Proteome Res. 2009;8(11):5296–5304. doi:10.1021/pr900507419754040
   PubMed Web of Science ®Google Scholar