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Research ArticleSpecial Issue on Drug Delivery Technologies

Ocular Drug Delivery: Present Innovations and Future Challenges

Vrinda Gote, Sadia Sikder, Jeff Sicotte and Dhananjay Pal
Journal of Pharmacology and Experimental Therapeutics September 2019, 370 (3) 602-624; DOI: https://doi.org/10.1124/jpet.119.256933
Vrinda Gote
Division of Pharmacology and Pharmaceutical Sciences, School of Pharmacy, University of Missouri-Kansas City, Kansas City, Missouri
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Sadia Sikder
Division of Pharmacology and Pharmaceutical Sciences, School of Pharmacy, University of Missouri-Kansas City, Kansas City, Missouri
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Jeff Sicotte
Division of Pharmacology and Pharmaceutical Sciences, School of Pharmacy, University of Missouri-Kansas City, Kansas City, Missouri
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Dhananjay Pal
Division of Pharmacology and Pharmaceutical Sciences, School of Pharmacy, University of Missouri-Kansas City, Kansas City, Missouri
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  • Fig. 1.
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    Fig. 1.

    Ocular anatomic barriers and routes of drug administration. Ocular barriers to topical administration (iv) of therapeutic agents to the anterior surface of the eye and to the posterior segment are illustrated. These include (A) tear film barrier; (B) corneal barrier; (C) vitreous barrier; (D) blood–retinal barrier and (E) blood–aqueous barrier. Various methods for drug delivery to the eye include; (I) intravitreal injection, (II) subconjuctival injection, (III) subretinal injection and (IV) topical administration. Topical administration of eye drops is one of the non-invasive route of administration and has minimum side effects. Intravitreal injections on the other hand are invasive, can cause retinal damage but can easily bypass all ocular barriers. While subconjuntival and subretinal injections can bypass some of the ocular barriers and are less invasive. (Alqawlaq et al., 2012).

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    Fig. 2.

    Ocular drug-delivery system using drug-loaded soft contact lenses. (A) Opthalmic drugs delivered though conventional eye drops. Majority of the drug administered gets drained a few minutes after instillation. (B) Drug delivery through molecularly imprinted soft contact lenses. This approach can increase the residence time of the drug molecules on the ocular surface increasing drug bioavailability as compared to conventional eye drop formulations. (Tashakori-Sabzevar F et al. 2015). MIP: molecularly imprinted polymer.

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    Fig. 3.

    ECT for back of the eye disorders. CAC ECT gel treatment on rats with inherited retinal degeneration. One or two units of GDNF-delivering CAC ECT gel was intravitreally injected into the eyes of dystrophic RCS/lav rats. (A) Representative H&E sections of nontreated, single, and double gel-treated rats showed different degrees of photoreceptor nuclei retention and organization in the outer nuclear layer (ONL). (B) ONL nuclei density was calculated by normalizing ONL count with retinal length. (C) Representative images showing the distribution of apoptotic cells (green) in the retina of nontreated, single, and double gel-treated animals detected by terminal deoxynucleotidyl transferase–mediated digoxigenin-deoxyuridine nick-end labeling (TUNEL) assay with 4’,6-diamidino-2-phenylindole (DAPI) nuclear counterstaining. (D) Density of apoptotic cells in the ONL. (E) Representative scotopic and photopic electroretinogram wave forms showing the retinal function of dystrophic rats receiving 1 or 2 U of GDNF-secreting gel. (F) Scotopic a-wave. (G) Scotopic b-wave. (H) Photopic b-wave. #P < 0.05; *P ≤ 0.02; **P ≤ 0.005; ***P < 0.0005 by one-way ANOVA with Bonferroni post hoc test (Wong et al., 2019). ERG, electroretinogram; INL, inner nuclear layer.

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    Fig. 4.

    TA-encapsulated methoxy PEG (mPEG)–PLGA nanoparticles for treating experimental autoimmune uveitis (EAU). (A–D) photographs taken by a hand-held retinal camera on day 12 after treatments: the EAU group (A), the mPEG-PLGA nanoparticle–treated group (B), the TA injection–treated group (C), the TA-loaded mPEG-PLGA nanoparticle–treated group (D), and clinical scores in the different groups (E).

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    Fig. 5.

    In vivo efficacy of PLGA fenofibrate NPs (Feno-NP) on vascular leakage and vascular permeability measured with Fundus Fluorescein Angiography (FFA). Formation of subretinal neovascularization (SRNV) and intraretinal neovascularization (IRNV) evaluated by neovascular tufts in flat-mounted choroid and retina in Vldlr−/− mice 1 month after Feno-NP treatment. (A) Representative images of FFA. (B) Numbers of leakage spots in FFA. (C) Quantification of retinal vascular permeability. (D) Representative images of SRNV and IRNV in FFA. Scale bar, 1000 μm. (E) Quantification of SRNV and IRNV in flat-mounted choroid and retina. Mean ± S.E.M. (n = 8–16; one-way ANOVA followed by Bonferroni post hoc test). ***P < 0.001 vs. untreated Vldlr−/− mice; ###P < 0.001 vs. blank-NP–treated Vldlr−/− mice (Qiu et al., 2019).

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    Fig. 6.

    Microneedles for enhanced drug delivery to the cornea. Drug-loaded, DC101, and diclofenac microneedle (DL-MN) patch for synergistic effect. Mouse eyes were treated 2 days after being inflicted with alkali burn and examined on day 7. (A) Illustration of drug loadings in DL-MNs and representative images of differently treated eyes. (B) Quantifications of corneal neovascularization. The white dotted lines indicate the extent of neovascular outgrowth from the limbus. Statistical comparison between groups was performed using one-way ANOVA. *P < 0.05; **P < 0.01 vs. control; #P < 0.05; ##P < 0.01 between indicated pairs (Than et al., 2018). Diclo, Diclofenac; ED, eye drop; HA, hyaluronic acid; MeHA, methacrylated hyaluronic acid.

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    Fig. 7.

    Comparison of cyclosporine-A nanomicellar formulation (OTX-101, Cequa) and cyclosporine-A emulsion (Restasis) evaluated in New Zealand white rabbits after a single topical administration. Concentration was determined in ocular tissues such as superior bulbar conjunctiva (A), cornea (B), and sclera (C).

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    TABLE 1

    Comparison of various routes of ocular drug administration: benefits and obstacles (Gaudana et al., 2010)

    RouteBenefitsObstaclesDiseases/Disorders Treated
    TopicalPatient compliance is high; self-administration and noninvasive natureCorneal barrier difficult to penetrate; dilution and efflux via tears is highConjunctivitis, keratitis, uveitis, episcleritis, scleritis, blepharitis
    IntravitrealDirect delivery to retinal and vitreal structures; drug has high bioavailabilityPatient compliance low; risk of retinal detachment, hemorrhage, development of endophthalmitis or cataractsAMD, BRVO, CRVO, DME, CMV retinitis
    Sub-TentonRelatively noninvasive, decreased risk of comorbidity compared with intravitreal delivery, maintains high vitreal drug levelsRetinal pigment epithelium is a barrier; subconjunctival hemorrhage, chemosisDME, AMD, RVO, uveitis
    Posterior juxtascleralAdvantageous for drug depository; avoids intraocular damage, and macula can sustain drug level for 6 moRetinal pigment epithelium barrier, and surgical procedure required;AMD, risk of endophthalmitis
    Systemic/oralPromotes patient compliance, noninvasive mode of deliveryRetinal and blood-aqueous barriers; low bioavailability leading to systemic toxicityScleritis, episcleritis, CMV retinitis, posterior uveitis
    IntracameralReduces systemic and corneal side effects vs. topical steroid use; high anterior chamber drug concentrationToxic endothelial cell destruction syndrome and toxic anterior segment syndrome pose major risks to patientsAnesthesia, prevention of endophthalmitis, inflammation, pupil dilation
    SubconjunctivalAnterior and posterior delivery method, ideal for depot formationChoroidal and conjunctival circulation of therapies increases toxicityGlaucoma, CMV retinitis, AMD
    RetrobulbarMinimal IOP involvement, ideal for high local anesthetic administrationRespiratory arrest, retrobulbar hemorrhage, globe perforationAnesthesia
    • BRVO, branched retinal vein occlusion; CMV retinitis, cytomegalovirus retinitis; CRVO, central retinal vein occlusion; IOP, intraocular pressure.

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    TABLE 2

    Currently available ocular drug-delivery systems in clinical trials for the treatment of anterior segment disorders (Kang-Mieler et al., 2014)

    DrugBrand NameMode of AdministrationExcipient Controlling Release Characteristic of DrugTarget IndicationDevelopmental StageClinical Trial #
    AzithromycinAzaSite (Akorn, Inc.)Eye dropsPolycarbophil (DuraSite)Bacterial conjunctivitisLaunchedNCT00105469
    Azithromycin/dexamethasone (ISV-502)AzaSite Plus (Akorn Inc.)Eye dropsPolycarbophil (DuraSite)BlepharoconjuntivitisLaunchedNCT00578955
    BetaxololBetoptic S (Novartis pharmaceuticals)Eye dropsGlaucomaLaunchedNCT00061542
    BimatoprostLumigan (Allergan)Eye dropsGlaucomaLaunchedNCT01589510
    BromfenacProlensa (Bausch & Lomb)Eye dropsPostoperative inflammationLaunchedNCT01847638
    Cyclosporine-ARestasis (Allergan Inc.)Eye dropsCationic emulsionDry eye due to keratitis siccaLaunchedNCT02554981
    DifluprednateDurezol (Novartis Pharmaceuticals)Eye dropsEmulsionAnterior uveitisLaunchedNCT01201798
    Timolol maleateTimoptic (Bausch & Lomb)Eye dropsGlaucoma/intraocular hypertensionLaunched
    Tobramycin/dexamethasoneTobraDex ST (Novartis Pharmaceuticals)Eye dropsXanthan gumBlepharitisLaunchedNCT01102244
    Timolol maleateTimoptic-XE (Merck & Co., Inc)Eye dropsGellan gumGlaucomaLaunchedNCT01446497
    Ophthalmic emulsionCationorm (Santen Pharmaceuticals)Eye dropsCationic emulsionMild dry eyeNCT03460548
    TravoprostiStent Inject (Glaukos Healthcare)Punctum plugOpen-angle glaucomaPhase IVNCT03624699
    Cyclosporine (LX201)Episcleral implantSiliconeKeratoconjuntivitisPhase IIINCT00447642
    Dexamethasone phosphate (EGP-437)EyeGate II (Eye Gate Pharma)IontophoresisAnterior uveitisPhase IIINCT01129856
    Dexamethasone (OTX-DP)Punctum plugHydrogelPostoperative inflammationPhase IINCT00650702
    LatanoprostDurasert (pSivida Corp.)Subconjunctival insertPLGAGlaucomaPhase I/IINCT00224289
    Loteprednol etabonate mucus-penetrating particlesInveltys (Kala Pharmaceuticals, Inc)NanoparticleMucus-penetrating particlesKerato conjunctivitis siccaPhase IIINCT03616899
    UreaNanoparticleAmphiphilic block copolymer PluronicF-127CataractPhase IINCT03001466
    Omega-3 fatty acidsRemogen Omega (TRB Chemedica)MicroparticleMicroemulsion of polyunsaturated fatty acids and hydrating polymersDry eye diseasePhase I/IINCT02908282
    • View popup
    TABLE 3

    Currently available ocular drug-delivery systems in clinical trials for the treatment of posterior segment disorders (Kang-Mieler et al., 2014)

    DrugBrand NameMode of AdministrationExcipient Controlling Release Characteristic of DrugTarget IndicationDevelopmental StageClinical Trial #
    DexamethasoneOzurdex (Allergan)Intravitreal implantPLGA (Novadur)Macular edema Posterior uveitisLaunchedNCT01427751
    GanciclovirVitrasert (Auritec Pharmaceuticals Inc.)Intravitreal implantPVA/EVACMV retinitisLaunchedNCT00000135
    Fluocinolone acetonideRetisert (Bausch & Lomb)Intravitreal implantPVAPosterior uveitisLaunchedNCT00570830
    VerteporfinVisudyne (Bausch & Lomb)i.v. injectionLiposomeWet AMDLaunchedNCT00242580
    DexamethasoneDexycu (EyePoint Pharmaceuticals, Inc.)Intravitreal implantAcetyl triethyl citratePostoperative inflammationLaunchedNCT02547623
    DifluprednateDurezol (Novartis Pharmaceuticals)Eye dropsEmulsionDMEOff-labelNCT00429923
    BetamethasoneIntravitreal implantChronijectDMEPhase II/IIINCT01546402
    CNTF (NT-501)Renexus (Neurotech Pharmaceuticals)Intravitreal implantSemipermeable hollow fiber membrane/NTC-200Atrophic AMDPhase II/IIINCT03316300
    Phase II
    DexamethasoneEye dropsCyclodextrin microparticlesDMEPhase II/IIINCT01523314
    Fluocinolone acetonideIluvien (Alimera Sciences)Intravitreal implantPolyamide/PVAPosterior uveitisPhase IVNCT01304706
    Macular edemaPhase II/III
    Wet AMDPhase II
    Triamcinolone acetonide with ranibizumabIntravitreal injectionVerisomeWet AMDPhase II/IIINCT02806752
    BrimonidineIntravitreal implantPLGADry AMDPhase IINCT02087085
    RPPhase I/II
    Triamcinolone acetonide (IBI-20089)Intravitreal implantBenzyl benzoateWet AMDPhase IINCT01175395
    Triamcinolone acetonide (RETAAC)Intravitreal implantPLGADMEPhase I/IINCT00407849
    Dexamethasone prodrug (NOVA-63035)Cortiject (Novagali Pharma S.A)Intravitreal implantEmulsionDMEPhase INCT00665106
    RanibizumabDrug portRefillable portWet AMDPhase INCT03677934
    VEGFR-Fc (NT-503)Intravitreal implantSemipermeable hollow fiber membrane/NTC-200Wet AMDPhase INCT02228304
    Human embryonic stem cell–derived retinal pigment epithelium (MA09-hRPE) cellsCells transplantation via subretinal injectionCell suspensionAdvanced dry AMDPhaseI/IINCT01344993
    AR-1105 (dexamethasone implant)Intravitreal implantBiodegradable implantMacular edema due to RVOPhase IINCT03739593
    • CMV retinitis, cytomegalovirus retinitis; CNTF, ciliary neurotrophic factor; EVA, Ethylene-vinyl acetate copolymer; PVA, Poly(vinyl alcohol); RP, Retinitis pigmentosa.

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    TABLE 4

    Ocular drug-delivery systems investigated for anterior segment disorders (inflammation) (Cholkar et al., 2013)

    Delivery SystemDrugPolymeric ComponentRemarksReferences
    NanoparticlesIbuprofenEudragit RS100Significant improvement of drug bioavailability in rabbit model compared with control aqueous dropsPignatello et al., 2002
    FlurbiprofenEudragit RS100Improved ocular bioavailability due to strong interaction between positive charged nanoparticle to the anionic corneal surfacePignatello et al., 2002
    FlurbiprofenPLGA, PCLColloidal systems enhance ocular bioavailability; PLGA nanoparticles showed ∼2-fold higher drug transport than that of PCL nanoparticlesValls et al., 2008
    IndomethacinPCL, Miglyol 840, poloxamer 188Colloidal formulation shows 3-fold higher ex vivo penetration than commercial eye dropsCalvo et al., 1996
    Cyclosporine-AChitosan and cholesterol-conjugated chitosanBoth nanoparticles deliver higher amount of drugs in cornea and conjunctiva as compared with cyclosporine-A suspensionDe Campos et al., 2001
    NanomicellesDexamethasonePluronic/chitosan systemNanomicelles entrapping dexamethasone significantly improved bioavailability to anterior ocular tissues by 2.4-fold relative to unformulated dexamethasonePepic et al., 2010
    Voclosporin, dexamethasone, rapamycinVitamin E TPGS and octoxynol-40 nanomicellesIn vivo studies showed mixed nanomicellar system have higher bioavailability with topical dosing of dexamethasone and rapamycinPepic et al., 2010
    Cyclosporine-AMethoxy poly(ethylene glycol)-hexylsubstituted poly(lactide)Transparent, highly stable, biocompatible formulationDi Tommaso et al., 2011
    Plasmid DNA with lacZ genePEO-PPO-PEOSignificant elevation of β-gal activity, transgene expression marker, elevated mRNA levels of bcl-x(L) by 2.2-fold, and reduced corneal apoptosis in mouse and rabbit cornea.Tong et al., 2007
    LiposomesC6-ceramideMethoxy PEG(2000) and PEG(750)-C6-ceramideSignificantly efficacious in reducing corneal inflammationSun et al., 2008
    DexamethasoneHuman serum albumin; bis(sulfosuccinimidyl) suberate; tris(hydroxymethyl) aminomethane; 3,3-dithiobis-(sulfosuccinimidylpropionate)Significantly higher drug accumulation in the eye (∼13.5 ng/mg tissue) than unformulated drug (2.4 ng/mg tissue)Arakawa et al., 2007
    • PEO-PPO-PEO, poly(ethylene oxide)-poly(propylene oxide)-poly(ethylene oxide); TPGS, tocopheryl polyethylene glycol succinate.

    • View popup
    TABLE 5

    Topically administered therapeutic agents for back of the eye disorders in various preclinical models (Rodrigues et al., 2018)

    CompoundFormulationPreclinical DataReference
    TG100801SolutionMurine CNV model and edema in ratDoukas et al., 2008
    PazopanibSolutionRat CNV modelYafai et al., 2011, Singh et al., 2014
    AcrizanibSuspensionMurine CNVAdams et al., 2018
    MemantineSolutionDrug levels in rabbit retinaHughes et al., 2005
    DorzolamideSolutionDrug levels and carbonic anhydrase activity in corneal endothelial cells, ciliary body, lens epithelial cells, and retina in rabbitInoue et al., 2004
    DexamethasoneIontophoresisDrug levels in retina and vitreous of rabbitAmbati and Adamis, 2002
    BevacizumabSolutionDrug levels in iris/ciliary body, vitreous, retina/choroid, and plasma in rabbitAmbati et al., 2000a
    Anti-intercellular adhesion molecule-1 antibodySolution by osmotic pumpDrug levels and VEGF-induced leukostasis in the choroid and retina in rabbitAmbati et al., 2000b
    28-kD single-chain antibody fragmentSodium caprateDrug levels in vitreous in rabbitWilliams et al., 2005
    BevacizumabAnnexin A5–based liposomesDrug levels in retina of rat and rabbitDavis et al., 2014
    Transforming growth factor β1Annexin A5–based liposomesDrug levels in vitreous in rabbitPlatania et al., 2017
    Acidic fibroblast growth factorCPP (TAT)Ischemia reperfusion model in ratWang et al., 2010
    Calpain inhibitory peptideCPP (TAT)Drug levels in rabbit retinaOzaki et al., 2015
    Green fluorescent proteinCPP (POD)Drug levels in mouse corneaJohnson et al., 2010
    BevacizumabCPP (R6)Drug levels in vitreous and retina in rat and murine CNV modelde Cogan et al., 2017
    • CPP (R6), cell-penetrating peptide poly-arginine-6; POD, peptide of ocular delivery; TAT, transactivator of transcription.

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Journal of Pharmacology and Experimental Therapeutics: 370 (3)
Journal of Pharmacology and Experimental Therapeutics
Vol. 370, Issue 3
1 Sep 2019
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Research ArticleSpecial Issue on Drug Delivery Technologies

Ocular Drug Delivery: Past, Present, and Future

Vrinda Gote, Sadia Sikder, Jeff Sicotte and Dhananjay Pal
Journal of Pharmacology and Experimental Therapeutics September 1, 2019, 370 (3) 602-624; DOI: https://doi.org/10.1124/jpet.119.256933

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Research ArticleSpecial Issue on Drug Delivery Technologies

Ocular Drug Delivery: Past, Present, and Future

Vrinda Gote, Sadia Sikder, Jeff Sicotte and Dhananjay Pal
Journal of Pharmacology and Experimental Therapeutics September 1, 2019, 370 (3) 602-624; DOI: https://doi.org/10.1124/jpet.119.256933
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  • Article
    • Visual Overview
    • Abstract
    • Introduction
    • Barriers to Ocular Drug Delivery and Routes of Drug Administration
    • Past Successes in Ocular Drug-Delivery Technologies
    • Recent Inventions for Ocular Drug-Delivery Technologies
    • Novel Ocular Drug-Delivery Technologies
    • Discussions: Challenges and Future Perspectives for Ocular Drug-Delivery Technologies
    • Conclusion
    • Acknowledgments
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