Cyclosporine A delivery to the eye: A pharmaceutical challenge

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 56, Issue 3, 2003, Pages 307-318

  Lallemand, F ^a   Felt Baeyens, O ^a   Besseghir, K ^b   Behar Cohen, F ^c   Gurny, R ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b DEBIOPHARM SA   (Switzerland)

^c INSERM   (France)

Author keywords

Cyclosporine A; Delivery system; Intraocular; Ocular delivery; Prodrug; Review; Topical

Indexed keywords

ALPHA CYCLODEXTRIN; BENZALKONIUM CHLORIDE; BUCRILATE; CARBOMER; CASTOR OIL; CHITOSAN; COLLAGEN; COLLAGEN IMPLANT; CREMOPHOR; CYCLODEXTRIN DERIVATIVE; CYCLOSPORIN A; DEXAMETHASONE; DIMETHYL SULFOXIDE; GANCICLOVIR; LAUROCAPRAM; LIPOSOME; MACROGOL STEARATE; MICROSPHERE; MYGLIOL; NANOPARTICLE; OPTIMMUNE; PENETRATION ENHANCING AGENT; POLYACRYLIC ACID; POLYCAPROLACTONE; PRODRUG; UNCLASSIFIED DRUG;

ANAPHYLAXIS; AUTOIMMUNITY; BIOAVAILABILITY; BURNING SENSATION; CONJUNCTIVA DISEASE; DEVICE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG PENETRATION; DRY EYE; EMULSION; ERYTHROCYTE AGGREGATION; EYE INFECTION; GRAFT REJECTION; HUMAN; HYPERLIPIDEMIA; MICELLE; NONHUMAN; PERIPHERAL NEUROPATHY; REVIEW; SUSTAINED DRUG RELEASE; VITREOUS BODY;

EID: 0242351952     PISSN: 09396411     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0939-6411(03)00138-3     Document Type: Review

References (95)

1. Noble S., Markham A. Cyclosporin. A review of the pharmacokinetic properties, clinical efficacy and tolerability of a microemulsion-based formulation (Neoral). Drugs. 50:1995;924-941.
2. Nussenblatt R.B., Palestine A.G., Chan C.C., Stevens G., Mellow S.D., Green S.B. Randomized, double-masked study of cyclosporine compared to prednisolone in the treatment of endogenous uveitis. Am. J. Ophthalmol. 112:1991;138-146.
3. Masuda K., Nakajima A., Urayama A., Nakae K., Kogure M., Inaba G. Double-masked trial of cyclosporin versus colchicine and long-term open study of cyclosporin in Behcet's disease. Lancet. 1:1989;1093-1096.
4. Georganas C., Ioakimidis D., Iatrou C., Vidalaki B., Iliadou K., Athanassiou P., Kontomerkos T. Relapsing Wegener's granulomatosis: successful treatment with cyclosporin-A. Clin. Rheumatol. 15:1996;189-192.
5. Prummel M.F., Mourits M.P., Berghout A., Krenning E.P., van der Gaag R., Koornneef L., Wiersinga W.M. Prednisone and cyclosporine in the treatment of severe Graves' ophthalmopathy. N. Engl. J. Med. 321:1989;1353-1359.
6. Reinhard T., Sundmacher R., Godehardt E., Heering P. Preventive systemic cyclosporin A after keratoplasty at increased risk for immune reactions as the only elevated risk factor. Ophthalmologe. 94:1997;496-500.
7. BenEzra D., Maftzir G., de Courten C., Timonen P. Ocular penetration of cyclosporin A. III: The human eye. Br. J. Ophthalmol. 74:1990;350-352.
8. Mihatsch M.J., Kyo M., Morozumi K., Yamaguchi Y., Nickeleit V., Ryffel B. The side-effects of ciclosporine-A and tacrolimus. Clin. Nephrol. 49:1998;356-363.
9. Li C., Yang C.W., Ahn H.J., Kim W.Y., Park C.W., Park J.H., Cha J.H., Kim J., Kim Y.S., Bang B.K. Colchicine suppresses osteopontin expression and inflammatory cell infiltration in chronic cyclosporine nephrotoxicity. Nephron. 92:2002;422-430.
10. Ganesan V., Milford D.V., Taylor C.M., Hulton S.A., Parvaresh S., Ramani P. Cyclosporin-related nephrotoxicity in children with nephrotic syndrome. Pediatr. Nephrol. 17:2002;225-226.
11. Gupta V., Sahu P.K. Topical cyclosporin A in the management of vernal keratoconjunctivitis. Eye. 15:2001;39-41.
12. Kunert K.S., Tisdale A.S., Gipson I.K. Goblet cell numbers and epithelial proliferation in the conjunctiva of patients with dry eye syndrome treated with cyclosporine. Arch. Ophthalmol. 120:2002;330-337.
13. Perry H.D., Doshi S.J., Donnenfeld E.D., Bai G.S. Topical cyclosporin A in the management of therapeutic keratoplasty for mycotic keratitis. Cornea. 21:2002;161-163.
14. Bowers L.D., Canafax D.M. Cyclosporine: experience with therapeutic monitoring. Ther. Drug Monit. 6:1984;142-147.
15. el Tayar N., Mark A.E., Vallat P., Brunne R.M., Testa B., van Gunsteren W.F. Solvent-dependent conformation and hydrogen-bonding capacity of cyclosporin A: evidence from partition coefficients and molecular dynamics simulations. J. Med. Chem. 36:1993;3757-3764.
16. Mithani S.D., Bakatselou V., TenHoor C.N., Dressman J.B. Estimation of the increase in solubility of drugs as a function of bile salt concentration. Pharm. Res. 13:1996;163-167.
17. BenEzra D., Maftzir G. Ocular penetration of cyclosporin A. The rabbit eye. Invest. Ophthalmol. Vis. Sci. 31:1990;1362-1366.
18. el Asrar A.M., Tabbara K.F., Geboes K., Missotten L., Desmet V. An immunohistochemical study of topical cyclosporine in vernal keratoconjunctivitis. Am. J. Ophthalmol. 121:1996;156-161.
19. Olivero D.K., Davidson M.G., English R.V., Nasisse M.P., Jamieson V.E., Gerig T.M. Clinical evaluation of 1% cyclosporine for topical treatment of keratoconjunctivitis sicca in dogs. J. Am. Vet. Med. Assoc. 199:1991;1039-1042.
20. Zhao J.C., Jin X.Y. Local therapy of corneal allograft rejection with cyclosporine. Am. J. Ophthalmol. 119:1995;189-194.
21. Holland E.J., Olsen T.W., Ketcham J.M., Florine C., Krachmer J.H., Purcell J.J., Lam S., Tessler H.H., Sugar J. Topical cyclosporin A in the treatment of anterior segment inflammatory disease. Cornea. 12:1993;413-419.
22. Gunduz K., Ozdemir O. Topical cyclosporin treatment of keratoconjunctivitis sicca in secondary Sjogren's syndrome. Acta Ophthalmol. (Copenh). 72:1994;438-442.
23. Stevenson D., Tauber J., Reis B.L. Efficacy and safety of cyclosporin A ophthalmic emulsion in the treatment of moderate-to-severe dry eye disease: a dose-ranging, randomized trial. The Cyclosporin A Phase 2 Study Group. Ophthalmology. 107:2000;967-974.
24. Kaswan R.L. Intraocular penetration of topically applied cyclosporine. Transpl. Proc. 20:1988;650-655.
25. Williams D.L. A comparative approach to topical cyclosporine therapy. Eye. 11:1997;453-464.
26. Solch S., Nadler P.I., Silverman M.H. Safety and tolerability of two percent cyclosporine (Sandimmune) ophthalmic ointment in normal volunteers. J. Ocul. Pharmacol. 7:1991;301-312.
27. Knagenhjelm S.K., Froyland K., Ringvold A., Bjerkas E., Kjonniksen I. Toxicological evaluation of cyclosporine eyedrops. Acta Ophthalmol. Scand. 77:1999;200-203.
28. Kachi S., Hirano K., Takesue Y., Miura M. Unusual corneal deposit after the topical use of cyclosporine as eyedrops. Am. J. Ophthalmol. 130:2000;667-669.
29. Sznitowska M., Zurowska-Pryczkowska K., Dabrowska E., Janicki S. Increased partitioning of pilocarpine to the oily phase of submicron emulsion does not result in improved ocular bioavailability. Int. J. Pharm. 202:2000;161-164.
30. Wiederholt M., Kossendrup D., Schulz W., Hoffmann F. Pharmacokinetic of topical cyclosporin A in the rabbit eye. Invest. Ophthalmol. Vis. Sci. 27:1986;519-524.
31. Heiligenhaus A., Steuhl K.P. Treatment of HSV-1 stromal keratitis with topical cyclosporin A: a pilot study. Graefes Arch. Clin. Exp. Ophthalmol. 237:1999;435-438.
32. Morgan R.V., Abrams K.L. Topical administration of cyclosporine for treatment of keratoconjunctivitis sicca in dogs. J. Am. Vet. Med. Assoc. 199:1991;1043-1046.
33. Cheeks L., Kaswan R.L., Green K. Influence of vehicle and anterior chamber protein concentration on cyclosporine penetration through the isolated rabbit cornea. Curr. Eye Res. 11:1992;641-649.
34. Mosteller M.W., Gebhardt B.M., Hamilton A.M., Kaufman H.E. Penetration of topical cyclosporine into the rabbit cornea, aqueous humor, and serum. Arch. Ophthalmol. 103:1985;101-102.
35. Diaz-Llopis M., Menezo J.L. Penetration of 2% cyclosporin eyedrops into human aqueous humour. Br. J. Ophthalmol. 73:1989;600-603.
36. Mueller D.W. Improved extemporaneous formulation of cyclosporine ophthalmic drops. Am. J. Hosp. Pharm. 51:1994;3080-3081.
37. J. Sansom, K.C. Barnett, W. Neumann, A. Schulte-Neumann, B. Clerc, J.P. Jegou, V. Haas, A. Weingarten, Treatment of keratoconjunctivitis sicca in dogs with cyclosporine ophthalmic ointment: a European clinical field trial. Vet. Rec. 137 (1995) 504-507.
38. Loftsson T., Stefansson E. Cyclodextrins in eye drop formulations: enhanced topical delivery of corticosteroids to the eye. Acta Ophthalmol. Scand. 80:2002;144-150.
39. Kanai A., Alba R.M., Takano T., Kobayashi C., Nakajima A., Kurihara K., Yokoyama T., Fukami M. The effect on the cornea of alpha cyclodextrin vehicle for cyclosporin eye drops. Transpl. Proc. 21:1989;3150-3152.
40. Newton C., Gebhardt B.M., Kaufman H.E. Topically applied cyclosporine in azone prolongs corneal allograft survival. Invest Ophthalmol. Vis. Sci. 29:1988;208-215.
41. Tang-Liu D.D., Richman J.B., Weinkam R.J., Takruri H. Effects of four penetration enhancers on corneal permeability of drugs in vitro. J. Pharm. Sci. 83:1994;85-90.
42. van der Bijl P., van Eyk A.D., Meyer D. Effects of three penetration enhancers on transcorneal permeation of cyclosporine. Cornea. 20:2001;505-508.
43. Furrer P., Mayer J.M., Plazonnet B., Gurny R. Ocular tolerance of preservatives on the murine cornea. Eur. J. Pharm. Biopharm. 47:1999;105-112.
44. Adriaens E., Dierckens K., Bauters T.G., Nelis H.J., van Goethem F., Vanparys P., Remon J.P. The mucosal toxicity of different benzalkonium chloride analogues evaluated with an alternative test using slugs. Pharm. Res. 18:2001;937-942.
45. Monti D., Chetoni P., Burgalassi S., Najarro M., Saettone M.F. Increased corneal hydration induced by potential ocular penetration enhancers: assessment by differential scanning calorimetry (DSC) and by desiccation. Int. J. Pharm. 232:2002;139-147.
46. Gelderblom H., Verweij J., Nooter K., Sparreboom A., Cremophor E.L. The drawbacks and advantages of vehicle selection for drug formulation. Eur. J. Canc. 37:2001;1590-1598.
47. Calvo P., Alonso M.J., Vila-Jato J.L., Robinson J.R. Improved ocular bioavailability of indomethacin by novel ocular drug carriers. J. Pharm. Pharmacol. 48:1996;1147-1152.
48. Kuwano M., Ibuki H., Morikawa N., Ota A., Kawashima Y. Cyclosporine A formulation affects its ocular distribution in rabbits. Pharm. Res. 19:2002;108-111.
49. Hickok S. Polyoxyethylene stearate. Wade A., Weller P. Handbook of Pharmaceutical Excipients. 1994;379-384 The Pharmaceutical Press, London, UK.
50. Muchtar S., Almog S., Torracca M.T., Saettone M.F., Benita S. A submicron emulsion as ocular vehicle for delta-8- tetrahydrocannabinol: effect on intraocular pressure in rabbits. Ophthalmic Res. 24:1992;142-149.
51. Naveh N., Muchtar S., Benita S. Pilocarpine incorporated into a submicron emulsion vehicle causes an unexpectedly prolonged ocular hypotensive effect in rabbits. J. Ocul. Pharmacol. 10:1994;509-520.
52. S. Ding. Non-irritating emulsions for sensitive tissue, U.S. Patent 5,474,979, 1995.
53. Acheampong A.A., Shackleton M., Tang-Liu D.D., Ding S., Stern M.E., Decker R. Distribution of cyclosporin A in ocular tissues after topical administration to albino rabbits and beagle dogs. Curr. Eye Res. 18:1999;91-103.
54. Sall K., Stevenson O.D., Mundorf T.K., Reis B.L. Two multicenter, randomized studies of the efficacy and safety of cyclosporine ophthalmic emulsion in moderate to severe dry eye disease. CsA Phase 3 Study Group [published erratum appears in Ophthalmology 2000 Jul;107(7):1220.]. Ophthalmology. 107:(2000):2000;631-639.
55. Klang S., Abdulrazik M., Benita S. Influence of emulsion droplet surface charge on indomethacin ocular tissue distribution. Pharm. Dev. Technol. 5:2000;521-532.
56. Abdulrazik M., Tamilvanan S., Khoury K., Benita S. Ocular delivery of cyclosporine A. Effect of submicron emulsion's surface charge on ocular distribution of topical cyclosporin A. S. T. P. Pharma Sci. 11:2001;427-432.
57. Milani J.K., Pleyer U., Dukes A., Chou H.J., Lutz S., Ruckert D., Schmidt K.H., Mondino B.J. Prolongation of corneal allograft survival with liposome-encapsulated cyclosporine in the rat eye. Ophthalmology. 100:1993;890-896.
58. Law S.L., Huang K.J., Chiang C.H. Acyclovir-containing liposomes for potential ocular delivery. Corneal penetration and absorption. J. Controlled Rel. 63:2000;135-140.
59. Calvo P., Sanchez A., Martinez J., Lopez M.I., Calonge M., Pastor J.C., Alonso M.J. Polyester nanocapsules as new topical ocular delivery systems for cyclosporin A. Pharm. Res. 13:1996;311-315.
60. Calvo P., Thomas C., Alonso M.J., Vila-Jato J.L., Robinson J.R. Study of the mechanism of interaction of poly(E-caprolactone) nanocapsules with the cornea by confocal laser scanning microscopy. Int. J. Pharm. 103:1994;283-291.
61. Juberias J.R., Calonge M., Gomez S., Lopez M.I., Calvo P., Herreras J.M., Alonso M.J. Efficacy of topical cyclosporine-loaded nanocapsules on keratoplasty rejection in the rat. Curr. Eye Res. 17:2002;39-46.
62. Masson V., Maurin F., Fessi H., Devissaguet J.P. Influence of sterilization processes on poly(E-caprolactone) nanospheres. Biomaterials. 18:1997;327-335.
63. Le Bourlais C.A., Chevanne F., Turlin B., Acar L., Zia H., Sado P.A., Needham T.E., Leverge R. Effect of cyclosporine A formulations on bovine corneal absorption: ex-vivo study. J. Microencapsul. 14:1997;457-467.
64. Zimmer A., Kreuter J., Robinson J.R. Studies on the transport pathway of PBCA nanoparticles in ocular tissues. J. Microencapsul. 8:1991;497-504.
65. De Campos A.M., Sanchez A., Alonso M.J. Chitosan nanoparticles: a new vehicle for the improvement of the delivery of drugs to the ocular surface. Application to cyclosporin A. Int. J. Pharm. 224:2001;159-168.
66. Felt O., Furrer P., Mayer J.M., Plazonnet B., Buri P., Gurny R. Topical use of chitosan in ophthalmology: tolerance assessment and evaluation of precorneal retention. Int. J. Pharm. 180:1999;185-193.
67. Lim L.Y., Khor E., Ling C.E. Effects of dry heat and saturated steam on the physical properties of chitosan. J. Biomed. Mater. Res. 48:1999;111-116.
68. Reidy J.J., Gebhardt B.M., Kaufman H.E. The collagen shield. A new vehicle for delivery of cyclosporin A to the eye. Cornea. 9:1990;196-199.
69. Pleyer U., Elkins B., Ruckert D., Lutz S., Grammer J., Chou J., Schmidt K.H., Mondino B.J. Ocular absorption of cyclosporine A from liposomes incorporated into collagen shields. Curr. Eye Res. 13:1994;177-181.
70. Gebhardt B.M., Kaufman H.E. Collagen as a delivery system for hydrophobic drugs: studies with cyclosporine. J. Ocul. Pharmacol. Ther. 11:1995;319-327.
71. Gebhardt B.M., Varnell E.D., Kaufman H.E. Cyclosporine in collagen particles: corneal penetration and suppression of allograft rejection. J. Ocul. Pharmacol. Ther. 11:1995;509-517.
72. R. Wenger, M. Mutter, A. Hamel, F. Hubler. Pro-Drug and use thereof as a medicament, WO Patent 02/085928, 2002.
73. Meadows D. Nonaqueous fluorinated drug delivery vehicle suspensions, U.S. Patent 5,173,298, 1992.
74. Kawakami S., Nishida K., Mukai T., Yamamura K., Nakamura J., Sakaeda T., Nakashima M., Sasaki H. Controlled release and ocular absorption of tilisolol utilizing ophthalmic insert-incorporated lipophilic prodrugs. J. Controlled Rel. 76:2001;255-263.
75. Salisbury J.D., Gebhardt B.M. Suppression of corneal allograft rejection by cyclosporin A. Arch. Ophthalmol. 99:1981;1640-1643.
76. Oh C., Apel A.J., Saville B.A., Cheng Y.L., Rootman D.S. Local efficacy of cyclosporine in corneal transplant therapy. Curr. Eye Res. 13:1994;337-343.
77. Harper C.A., Khoobehi B., Peyman G.A., Gebhardt B.M., Dunlap W.A. Bioavailability of microsphere-entrapped cyclosporine A in the cornea and aqueous of rabbits. Int. Ophthalmol. 17:1993;337-340.
78. Rojas Silva M.V., Rodriguez-Ares M.T., Sanchez-Salorio M., Lamas Diaz M.J., Cuevas A.J., Vila Jato J.L., Capeans T.C. Efficacy of subconjunctival cyclosporin-containing microspheres on keratoplasty rejection in the rabbit. Graefes Arch. Clin. Exp. Ophthalmol. 237:1999;840-847.
79. Alghadyan A.A., Peyman G.A., Khoobehi B., Milner S., Liu K.R. Liposome-bound cyclosporine: aqueous and vitreous level after subconjunctival injection. Int. Ophthalmol. 12:1988;101-104.
80. Apel A., Oh C., Chiu R., Saville B., Cheng Y.L., Rootman D. A subconjunctivalde gradable implant for cyclosporine delivery in corneal transplant therapy. Curr. Eye Res. 14:1995;659-667.
81. Grisolano J., Peyman G.A. Retinal toxicity study of intravitreal cyclosporin. Ophthalmic Surg. 17:1986;155-156.
82. Lai C.C., Gouras P., Doi K., Tsang S.H., Goff S.P., Ashton P. Local immunosuppression prolongs survival of RPE xenografts labeled by retroviral gene transfer. Invest. Ophthalmol. Vis. Sci. 41:2000;3134-3141.
83. Alghadyan A.A., Peyman G.A., Khoobehi B., Liu K.R. Liposome-bound cyclosporine: retinal toxicity after intravitreal injection. Int. Ophthalmol. 12:1988;105-107.
84. Alghadyan A.A., Peyman G.A., Khoobehi B., Milner S., Liu K.R. Liposome-bound cyclosporine: clearance after intravitreal injection. Int. Ophthalmol. 12:1988;109-112.
85. Xie L., Shi W., Wang Z., Bei J., Wang S. Prolongation of corneal allograft survival using cyclosporine in a polylactide-co-glycolide polymer. Cornea. 20:2001;748-752.
86. Sanborn G.E., Anand R., Torti R.E., Nightingale S.D., Cal S.X., Yates B., Ashton P., Smith T. Sustained-release ganciclovir therapy for treatment of cytomegalovirus retinitis. Use of an intravitreal device. Arch. Ophthalmol. 110:1992;188-195.
87. Pearson P.A., Jaffe G.J., Martin D.F., Cordahi G.J., Grossniklaus H., Schmeisser E.T., Ashton P. Evaluation of a delivery system providing long-term release of cyclosporine. Arch. Ophthalmol. 114:1996;311-317.
88. Jaffe G.J., Yang C.S., Wang X.C., Cousins S.W., Gallemore R.P., Ashton P. Intravitreal sustained-release cyclosporine in the treatment of experimental uveitis. Ophthalmology. 105:1998;46-56.
89. Velez G., Whitcup S.M. New developments in sustained release drug delivery for the treatment of intraocular disease. Br. J. Ophthalmol. 83:1999;1225-1229.
90. Enyedi L.B., Pearson P.A., Ashton P., Jaffe G.J. An intravitreal device providing sustained release of cyclosporine and dexamethasone. Curr. Eye Res. 15:1996;549-557.
91. Gilger B.C., Malok E., Stewart T., Ashton P., Smith T., Jaffe G.J., Allen J.B. Long-term effect on the equine eye of an intravitreal device used for sustained release of cyclosporine A. Vet. Ophthalmol. 3:2000;105-110.
92. Gilger B.C., Malok E., Stewart T., Horohov D., Ashton P., Smith T., Jaffe G.J., Allen J.B. Effect of an intravitreal cyclosporine implant on experimental uveitis in horses. Vet. Immunol. Immunopathol. 76:2000;239-255.
93. Wakefield D., McCluskey P. Cyclosporine: a therapy in inflammatory eye disease. J. Ocul. Pharmacol. 7:1991;221-226.
94. Herbort C.P., Matsubara M., Nishi M., Mochizuki M. Penetrating keratoplasty in the rat: a model for the study of immunosuppressive treatment of graft rejection. Jpn. J. Ophthalmol. 33:1989;212-220.
95. Palmer S.L., Bowen P.A., Green K. Longitudinal tear study after cyclosporine in kidney transplant recipients. Ophthalmology. 103:1996;670-673.