Azithromycin-liposomes as a novel approach for localized therapy of cervicovaginal bacterial infections

References

• Sáez-López E, Guiral E, Fernández-Orth D, et al. Vaginal versus obstetric infection Escherichia coli isolates among pregnant women: antimicrobial resistance and genetic virulence profile. PLoS One. 2016;11(1):e0146531. doi:10.1371/journal.pone.014653126784330
   PubMed Web of Science ®Google Scholar
• Adachi K, Klausner JD, Bristow CC, et al. Chlamydia and gonorrhea in HIV-infected pregnant women and infant HIV transmission. Sex Transm Dis. 2015;42(10):554–565. doi:10.1097/OLQ.000000000000034026372927
   PubMedGoogle Scholar
• Centers for Disease Control and Prevention (CDC), Sexually Transmitted Diseases Treatment Guidelines. 2015 Available from: https://www.cdc.gov/std/tg2015/chlamydia.htm. Accessed 115, 2019.
   Google Scholar
• Coyle EA, Prince RA. Urinary tract infections and prostatitis In: Wells BG, DiPiro JT, Schwinghammer TL, DiPiro CV, editors. Pharmacotherapy Handbook. London: McGraw Hill Medical; 2009:544–555.
   Google Scholar
• Abed N, Couvreur P. Nanocarriers for antibiotics: a promising solution to treat intracellular bacterial infections. Int J Antimicrob Agents. 2014;43(6):485–496. doi:10.1016/j.ijantimicag.2014.02.00924721232
   PubMed Web of Science ®Google Scholar
• Škalko-Basnet N, Vanić Ž. Lipid-based nanopharmaceuticals in antimicrobial therapy In: Boukherroub R, Szunerits S, Drider D, editors. Functionalized Nanomaterials for the Management of Microbial Infection, A Strategy to Address Microbial Drug Resistance. Amsterdam: Elsevier; 2017:111–152.
   Google Scholar
• Rukavina Z, Vanić Ž. Current trends in development of liposomes for targeting bacterial biofilms. Pharmaceutics. 2016;8(2):18. doi:10.3390/pharmaceutics8020018
   PubMed Web of Science ®Google Scholar
• Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Del Rev. 2013;65(1):36–48. doi:10.1016/j.addr.2012.09.037
   PubMed Web of Science ®Google Scholar
• Sala M, Diab R, Elaissari A, Fessi H. Lipid nanocarriers as skin drug delivery systems: properties, mechanisms of skin interactions and medical applications. Int J Pharm. 2018;535(1–2):1–17. doi:10.1016/j.ijpharm.2017.10.04629111097
   PubMed Web of Science ®Google Scholar
• Vanić Ž, Škalko-Basnet N. Nanopharmaceuticals for improved topical vaginal therapy: can they deliver? Eur J Pharm Sci. 2013;50(1):29–41. doi:10.1016/j.ejps.2013.04.03523684936
   PubMed Web of Science ®Google Scholar
• Peters DH, Friedel HA, McTavish D. Azithromycin: a review of its antimicrobial activity, pharmacokinetic properties and clinical efficacy. Drugs. 1992;44(5):750–799. doi:10.2165/00003495-199244050-000071280567
   PubMed Web of Science ®Google Scholar
• Wu EC, Kowalski RP, Romanowski EG, Mah FS, Gordon YJ, Shanks RMQ. AzaSite® inhibits Staphylococcus aureus and coagulase-negative Staphylococcus biofilm formation in vitro. J Ocul Pharmacol Ther. 2010;26(6):557–562. doi:10.1089/jop.2009.005921029017
   PubMed Web of Science ®Google Scholar
• Mandić Z. Voltammetric study of the partitioning of macrolide antibiotics at the water/nitrobenzene interface: relationship to the pharmacokinetic profiling of macrolides. Admet Dmpk. 2014;2(3):168–178. doi:10.5599/admet.2.3.46
   Google Scholar
• Imamura Y, Higashiyama Y, Tomono K, et al. Azithromycin exhibits bactericidal effects on Pseudomonas aeruginosa through interaction with the outer membrane. Antimicrob Agents Chemother. 2005;49(4):1377–1380. doi:10.1128/AAC.49.2.612-618.200515793115
   PubMed Web of Science ®Google Scholar
• Liu X, Li Z, Wang X, et al. Novel antimicrobial peptide-modified azithromycin-loaded liposomes against methicillin resistant Staphylococcus aureus. Int J Nanomed. 2016;11:6781–6794. doi:10.2147/IJN.S107107
   PubMed Web of Science ®Google Scholar
• Oh YK, Nix DE, Straubinger RM. Formulation and efficacy of liposome-encapsulated antibiotics for therapy of intracellular Mycobacterium avium infection. Antimicrob Agents Chemother. 1995;39(9):2104–2111. doi:10.1128/aac.39.9.19208540724
   PubMed Web of Science ®Google Scholar
• Rukavina Z, Šegvić Klarić M, Filipović-Grčić J, Lovrić J, Vanić Ž. Azithromycin-loaded liposomes for enhanced topical treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections. Int J Pharm. 2018;553(1–2):109–119. doi:10.1016/j.ijpharm.2018.10.02430312749
   PubMed Web of Science ®Google Scholar
• Solleti VS, Alhariri M, Halwani M, Omri A. Antimicrobial properties of liposomal azithromycin for Pseudomonas infections in cystic fibrosis patients. J Antimicrob Chemother. 2015;70(3):784–796. doi:10.1093/jac/dku44525416744
   PubMed Web of Science ®Google Scholar
• Owen DH, Katz DF. A vaginal fluid simulant. Contraception. 1999;59(2):91–95. doi:10.1016/S0010-7824(99)00010-410361623
   PubMed Web of Science ®Google Scholar
• Pavelić Ž, Škalko-Basnet N, Jalšenjak I. Characterisation and in vitro evaluation of bioadhesive liposome gels for local therapy of vaginitis. Int J Pharm. 2005;301(1–2):140–148. doi:10.1016/j.ijpharm.2005.05.02216024188
   PubMedGoogle Scholar
• Palac Z, Engesland A, Flaten GE, Škalko-Basnet N, Filipović-Grčić J, Vanić Ž. Liposomes for (trans)dermal drug delivery: the skin-PVPA as a novel in vitro stratum corneum model in formulation development. J Liposome Res. 2014;24(4):313–322. doi:10.3109/08982104.2014.89936824646434
   PubMed Web of Science ®Google Scholar
• Vanić Ž, Hurler J, Ferderber K, Golja Gašparović P, Škalko-Basnet N, Filipović-Grčić J. Novel vaginal drug delivery system: deformable propylene glycol liposomes-in-hydrogel. J Liposome Res. 2014;24(1):27–36. doi:10.3109/08982104.2013.82624223931627
   PubMed Web of Science ®Google Scholar
• Vanić Ž, Hafner A, Bego M, Škalko-Basnet N. Characterization of various deformable liposomes with metronidazole. Drug Dev Ind Pharm. 2013;39(3):481–488. doi:10.3109/03639045.2012.67024722455377
   PubMed Web of Science ®Google Scholar
• Manner S, Vahermo M, Skogman ME, et al. New derivatives of dehydroabietic acid target planktonic and biofilm bacteria in Staphylococcus aureus and effectively disrupt bacterial membrane integrity. Eur J Med Chem. 2015;102:68–79. doi:10.1016/j.ejmech.2015.07.03826241878
   PubMed Web of Science ®Google Scholar
• Mosolygó T, Spengler G, Endrész V, Laczi K, Perei K, Burián K. IL-17E production is elevated in the lungs of Balb/c mice in the later stages of Chlamydia muridarum infection and re-infection. In Vivo. 2013;27(6):787–792.24292583
   PubMed Web of Science ®Google Scholar
• Sabet SF, Simmons J, Caldwell HD. Enhancement of Chlamydia trachomatis infectious progeny by cultivation of HeLa 229 cells treated with DEAE-dextran and cycloheximide. J Clin Microbiol. 1984;20(2):217–222.6208215
   PubMed Web of Science ®Google Scholar
• Bogdanov A, Janovák L, Lantos I, et al. Nonactivated titanium-dioxide nanoparticles promote the growth of Chlamydia trachomatis and decrease the antimicrobial activity of silver nanoparticles. J Appl Microbiol. 2017;123:1335–1345. doi:10.1111/jam.1356028799270
   PubMedGoogle Scholar
• Eszik I, Lantos I, Önder K, et al. High dynamic range detection of Chlamydia trachomatis growth by direct quantitative PCR of the infected cells. J Microbiol Methods. 2016;120:15–22. doi:10.1016/j.mimet.2015.11.01026578244
   PubMedGoogle Scholar
• Mossman T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Meth. 1983;65(1–2):55–63.
   PubMed Web of Science ®Google Scholar
• Bhattacharjee S. DLS and zeta potential – what they are and what they are not? J Control Release. 2016;235:337–351. doi:10.1016/j.jconrel.2016.05.02427297779
   PubMed Web of Science ®Google Scholar
• Chen Y, Lu Y, Chen J, et al. Enhanced bioavailability of the poorly water-soluble drug fenofibrate by using liposomes containing a bile salt. Int J Pharm. 2009;376(1–2):153–160. doi:10.1016/j.ijpharm.2009.04.02219394416
   PubMed Web of Science ®Google Scholar
• Hoppel M, Juric S, Ettl H, Valenta C. Effect of monoacyl phosphatidylcholine content on the formation of microemulsions and the dermal delivery of flufenamic acid. Int J Pharm. 2015;479(1):70–76. doi:10.1016/j.ijpharm.2014.12.04825542986
   PubMedGoogle Scholar
• Eggert-Kruse W, Kohler A, Rohr G, Runnebaum B. The pH as an important determinant of sperm-mucus interaction. Fertil Steril. 1993;59(3):617–628.8458467
   PubMed Web of Science ®Google Scholar
• Martin C, Low WL, Gupta A, et al. Strategies for antimicrobial drug delivery to biofilm. Curr Pharm Des. 2015;21(1):43–66. doi:10.2174/138161282066614090512352925189862
   PubMed Web of Science ®Google Scholar
• Lai SK, Wang YY, Hanes J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv Drug Deliv Rev. 2009;61(2):158–171. doi:10.1016/j.addr.2008.11.00219133304
   PubMed Web of Science ®Google Scholar
• Van Bambeke F, Montenez JP, Piret J, Tulkens PM, Courtoy PJ, Mingeot-Leclercq MP. Interaction of the macrolide azithromycin with phospholipids. I. Inhibition of lysosomal phospholipase A1 activity. Eur J Pharmacol. 1996;314(1–2):203–214. doi:10.1016/s0014-2999(96)00552-38957238
   PubMed Web of Science ®Google Scholar
• Jacobsen AC, Elvang PA, Bauer-Brandl A, Brandl M. A dynamic in vitro permeation study on solid mono- and diacyl-phospholipid dispersions of celecoxib. Eur J Pharm Sci. 2019;127:199–207. doi:10.1016/j.ejps.2018.11.00330408522
   PubMed Web of Science ®Google Scholar
• Pavelić Ž, Škalko-Basnet N, Filipović-Grčić J, Martinac A, Jalšenjak I. Development and in vitro evaluation of a liposomal vaginal delivery system for acyclovir. J Control Release. 2005;106(1–2):34–43. doi:10.1016/j.jconrel.2005.03.03215979189
   PubMed Web of Science ®Google Scholar
• Cadena PG, Pereira MA, Cordeiro RBS, et al. Nanoencapsulation of quercetin and resveratrol into elastic liposomes. Biochim Biophys Acta. 2013;1828(2):309–316. doi:10.1016/j.bbamem.2012.10.02223103506
   PubMed Web of Science ®Google Scholar
• Machado D, Castro J, Palmeira-de-Oliveira A, Martinez-de-Oliveira J, Cerca N. Bacterial vaginosis biofilms: challenges to current therapies and emerging solutions. Front Microbiol. 2016;6:1528. doi:10.3389/fmicb.2015.0150826834706
   PubMedGoogle Scholar
• Jøraholmen MW, Vanić Ž, Tho I, Škalko-Basnet N. Chitosan-coated liposomes for topical vaginal therapy: assuring localized drug effect. Int J Pharm. 2014;472(1–2):94–101. doi:10.1016/j.ijpharm.2014.06.01624928137
   PubMed Web of Science ®Google Scholar
• Jøraholmen MW, Basnet P, Acharya G, Škalko-Basnet N. PEGylated liposomes for topical vaginal therapy improve delivery of interferon alpha. Eur J Pharm Biopharm. 2017;113:132–139. doi:10.1016/j.ejpb.2016.12.02928087379
   PubMed Web of Science ®Google Scholar
• New RRC. Liposomes: A Practical Approach. Oxford: IRL Press; 1990.
   Google Scholar
• Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents. 2010;35(4):322–332. doi:10.1016/j.ijantimicag.2009.12.01120149602
   PubMed Web of Science ®Google Scholar
• Beaulac C, Sachetelli S, Lagace J. In-vitro bactericidal efficacy of sub-MIC concentrations of liposome-encapsulated antibiotic against gram-negative and gram-positive bacteria. J Antimicrob Chemother. 1998;41(1):35–41. doi:10.1093/jac/41.1.359511035
   PubMedGoogle Scholar
• Nicolosi D, Scalia M, Nicolosi VM, Pignatello R. Encapsulation in fusogenic liposomes broadens the spectrum of action of vancomycin against Gram-negative bacteria. Int J Antimicrob Agents. 2010;35(6):553–558. doi:10.1016/j.ijantimicag.2010.01.01520219328
   PubMed Web of Science ®Google Scholar
• Sun X, Qiu H, Jin Y. Highly efficient treatment of aerobic vaginitis with simple acidic buffered gels: the importance of pH and buffers on the micoenvironment of vaginas. Int J Pharm. 2017;525(1):175–182. doi:10.1016/j.ijpharm.2017.04.02628414136
   PubMedGoogle Scholar
• Jones BM, Kinghorn GR, Duerden BI. In vitro activity of azithromycin and erythromycin against organisms associated with bacterial vaginosis and chancroid. Eur J Clin Microbiol Infect Dis. 1998;7(4):551–553. doi:10.1007/BF01962614
   Google Scholar
• De Backer E, Verhelst R, Verstraelen H, et al. Antibiotic susceptibility of Atopobium vaginae. BMC Infect Dis. 2006;6:51. doi:10.1186/1471-2334-6-5116542416
   PubMed Web of Science ®Google Scholar
• Bretelle F, Fenollar F, Baumstarck K, et al. Screen-and-treat program by point-of-care of Atopobium vaginae and Gardnerella vaginalis in preventing preterm birth (AuTop trial): study protocol for a randomized controlled trial. Trials. 2015;16:470. doi:10.1186/s13063-015-0731-026482128
   PubMedGoogle Scholar
• Wildfeuer A, Laufen H, Zimmermann T. Uptake of azithromycin by various cells and its intracellular activity under in vivo conditions. Antimicrob Agents Chemother. 1996;40(1):75–79. doi:10.1128/AAC.40.1.758787883
   PubMedGoogle Scholar
• Bosnar M, Kelnerić Z, Munić V, Eraković V, Parnham MJ. Cellular uptake and efflux of azithromycin, erythromycin, clarithromycin, telithromycin, and cethromycin. Antimicrob Agents Chemother. 2005;49(6):2372–2377. doi:10.1128/AAC.49.6.2372-2377.200515917536
   PubMedGoogle Scholar
• Sangare L, Morisset R, Ravaoarinoro M. In-vitro anti-chlamydial activities of free and liposomal tetracycline and doxycycline. J Med Microbiol. 1999;48(7):689–693. doi:10.1099/00222615-48-7-68910403420
   PubMedGoogle Scholar
• Zhou X, Zhang Y, Li Y, Hao X, Liu X, Wang Y. Azithromycin synergistically enhances anti-proliferative activity of vincristine in cervical and gastric cancer cells. Cancers. 2012;4(4):1318–1332. doi:10.3390/cancers404131824213508
   PubMedGoogle Scholar
• ISO10993-5, 2009. Biological evaluation of medical devices-part 5: tests for cytotoxicity: in vitro methods. Available from: https://www.iso.org/standard/36406.html. Accessed 125, 2019.
   Google Scholar
• Chang MC, Lee JJ, Chen YJ, et al. Lysophosphatidylcholine induces cytotoxicity/apoptosis and IL-8 production of human endothelial cells: related mechanisms. Oncotarget. 2017;8(63):106177–106189. doi:10.18632/oncotarget.2242529290940
   PubMedGoogle Scholar
• Alhajlan M, Alhariri M, Omri A. Efficacy and safety of liposomal clarithromycin and its effect on Pseudomonas aeruginosa virulence factors. Antimicrob Agents Chemother. 2013;57(6):2694–2704. doi:10.1128/AAC.00235-1323545534
   PubMed Web of Science ®Google Scholar