A multiphase microscopic diffusion model for stratum corneum permeability. I. Formulation, solution, and illustrative results for representative compounds

Journal of Pharmaceutical Sciences

Volumn 95, Issue 3, 2006, Pages 620-648

  Wang, Tsuo Feng ^a,c   Kasting, Gerald B ^b   Nitsche, Johannes M ^a  

^a the State University of New York   (United States)

^b UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^c National Science Council   (Taiwan)

Author keywords

Corneocyte; Diffusion coefficient; Intercellular lipid; Microstructure; Partition coefficient; Permeability; Stratum corneum (SC)

Indexed keywords

ALCOHOL; NICOTINAMIDE; TESTOSTERONE; WATER;

ARTICLE; CALCULATION; DIFFUSION; HYDRATION; LIPID BILAYER; LIPID TRANSPORT; SKIN PERMEABILITY; STRATUM CORNEUM; WATER PERMEABILITY;

EID: 33645371782     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.20509     Document Type: Review

References (99)

1. Blank IH, Scheuplein RJ. 1969. Transport into and within the skin. Br J Derm 81(Suppl. 4):4-10.
2. Scheuplein RJ, Blank IH. 1971. Permeability of the skin. Physiol Rev 51:702-747.
3. Wester RC, Maibach HI. 1983. Cutaneous pharmacokinetics: 10 steps to percutaneous absorption. Drug Metabolism Rev 14:169-205.
4. Ritschel WA, Hussain AS. 1988. The principles of permeation of substances across the skin. Meth Find Exptl Clin Pharmacol 10:39-56.
5. Wester RC, Maibach HI. 1992. Percutaneous absorption of drugs. Clin Pharmacokinet 23:253-266.
6. Siddiqui O. 1989. Physicochemical, physiological, and mathematical considerations in optimizing percutaneous absorption of drugs. Crit Rev Ther Drug Carrier Syst 6:1-38.
7. Wiechers JW. 1989. The barrier function of the skin in relation to percutaneous absorption of drugs. Pharm Weekbl Sci 11:185-198.
8. Robinson PJ. 1998. Prediction: simple risk models and overview of dermal risk assessment, Chapter 8. In: Roberts MS, Walters KA, editors. Dermal absorption and toxicity assessment. New York: Marcel Dekker, pp 203-229.
9. Gerberick GF, Robinson MK, Felter SP, White IR, Basketter DA. 2001. Understanding fragrance allergy using an exposure-based risk assessment approach. Contact Derm 45:333-340.
10. Montagna W, Parakkal PF. 1974. The structure and function of skin, 3rd edn. New York: Academic Press.
11. Roberts MS, Walters KA. 1998. The relationship between structure and barrier function of skin, Chapter 1. In: Roberts MS, Walters KA, editors. Dermal absorption and toxicity assessment. New York: Marcel Dekker, pp 1-42.
12. Feldman RJ, Maibach HI. 1970.. Absorption of some organic compounds through the skin in man. J Invest Dermatol 54:399-404.
13. Zhen Y-X, Suetake T, Tagami H. 1999. Number of cell layers of the stratum corneum in normal skin - relationship to the anatomical location on the body, age, sex and physical parameters. Arch Dermatol Res 291:555-559.
14. Hou SYE, Rehfeld SJ, Plachy WZ. 1991. X-ray diffraction and electron paramagnetic resonance spectroscopy of mammalian stratum corneum lipid domains. In: Elias PM, editor. Adv lipid res, vol. 24: skin lipids. New York: Academic Press, pp 141-171.
15. Ribaud C, Garson J-C, Doucet J, Lévêque J-L. 1994. Organization of stratum corneum lipids in relation to permeability: influence of sodium lauryl sulfate and preheating. Pharm Res 11:1414-1418.
16. Brody I. 1960. The ultrastructure of the tonofibrils in the keratinization process of normal human epidermis. J Ultrastruct Res 4:264-297.
17. Potts RO, Guy RH. 1992. Predicting skin permeability. Pharm Res 9:663-669.
18. Guy RH, Potts RO. 1992. Structure-permeability relationships in percutaneous penetration. J Pharm Sci 81:603-604.
19. Kasting GB, Smith RL, Anderson BD. 1992. Prodrugs for dermal delivery: solubility, molecular size, and functional group effects, Chapter 3. In: Sloan KB, editor. Prodrugs: topical and Ocular Drug Delivery. New York: Marcel Dekker, pp 117-161.
20. Hostýnek JJ, Reifenrath WG, Melendres JL, Magee PS. 1995. Correlation of in vivo and in vitro percutaneous absorption with a mathematical model. In: Surber C, Elsner P, Bircher AJ, editors. Curr prob dermatol, vol. 22: exogenous dermatology. Basel: Karger, pp 139-145.
21. Potts RO, Guy RH. 1995. A predictive algorithm for skin permeability: the effects of molecular size and hydrogen bond activity. Pharm Res 12:1628-1633.
22. Wilschut A, ten Berge WF, Robinson PJ, McKone TE. 1995. Estimating skin permeation. The validation of five mathematical skin permeation models. Chemosphere 30:1275-1296.
23. Flynn GL. 1990. Physicochemical determinants of skin absorption. In: Gerrity TR, Henry CJ, editors. Principles of route-to-route extrapolation for risk assessment. New York: Elsevier, pp 93-127.
24. Johnson ME, Blankschtein D, Langer R. 1997. Evaluation of solute permeation through the stratum corneum: lateral bilayer diffusion as the primary transport mechanism. J Pharm Sci 86:1162-1172.
25. Elias PM. 1981. Lipids and the epidermal permeability barrier. Arch Dermatol Res 270:95-117.
26. Albery WJ, Hadgraft J. 1979. Percutaneous absorption: in vivo experiments. J Pharm Pharmacol 31:140-147.
27. Boddé HE, van den Brink I, Koerten HK, de Haan FHN. 1991. Visualization of in vitro percutaneous penetration of mercuric chloride; transport through intercellular space versus cellular uptake through desmosomes. J Control Release 15:227-236.
28. Elias PM, Friend DS. 1979. The permeability barrier in mammalian epidermis. J Cell Biol 65:180-191.
29. Potts RO, Francoeur ML. 1991. The influence of stratum corneum morphology on water permeability. J Invest Dermatol 96:495-499.
30. Mitragotri S. 2002. A theoretical analysis of permeation of small hydrophobic solutes across the stratum corneum based on scaled particle theory. J Pharm Sci 91:744-752.
31. Lange-Lieckfeldt R, Lee G. 1992. Use of a model lipid matrix to demonstrate the dependence of the stratum corneum's barrier properties on its internal geometry. J Control Release 20:183-194.
32. Frasch HF, Barbero AM. 2003. Steady-state flux and lag time in the stratum corneum lipid pathway: results from finite element models. J Pharm Sci 92:2196-2207.
33. Peck KD, Ghanem A-H, Higuchi WI. 1994. Hindered diffusion of polar molecules through and effective pore radii estimates of intact and ethanol treated human epidermal membrane. Pharm Res 11:1306-1314.
34. Ackermann C, Flynn GL. 1987. Ether-water partitioning and permeability through nude mouse skin in vitro. I. Urea, thiourea, glycerol and glucose. Int J Pharm 36:61-66.
35. Anderson BD, Raykar PV. 1989. Solute structure-permeability relationships in human stratum corneum. J Invest Dermatol 93:280-286.
36. Scheuplein RJ. 1967. Mechanism of percutaneous absorption. II. Transient diffusion and the relative importance of various routes of skin penetration. J Invest Dermatol 48:79-88.
37. Anderson BD, Higuchi WI, Raykar PV. 1988. Heterogeneity effects on permeability-partition coefficient relationships in human stratum corneum. Pharm Res 5:566-573.
38. Kim Y-H, Ghanem A-H, Mahmoud H, Higuchi WI. 1992. Short chain alkanols as transport enhancers for lipophilic and polar/ionic permeants in hairless mouse skin: mechanism(s) of action. Int J Pharm 80:17-31.
39. Hatanaka T, Manabe E, Sugibayashi K, Morimoto Y. 1994. An application of the hydrodynamic pore theory to percutaneous absorption of drugs. Pharm Res 11:654-658.
40. Yamashita F, Bando H, Koyama Y, Kitagawa S, Takakura Y, Hashida M. 1904. In vivo and in vitro analysis of skin penetration enhancement based on a two-layer diffusion model with polar and non-polar routes in the stratum corneum. Pharm Res 11:185-191.
41. Yoneto K, Ghanem A-H, Higuchi WI, Peck KD, Li SK. 1995. Mechanistic studies of the 1-alkyl-2-pyrrolidones as skin permeation enhancers. J Pharm Sci 84:312-317.
42. Lee AJ, King JR, Barrett DA. 1997. Percutaneous absorption: a multiple pathway model. J Control Release 45:141-151.
43. Raykar PV, Fung M-C, Anderson BD. 1988. The role of protein and lipid domains in the uptake of solutes by human stratum corneum. Pharm Res 5:140-150.
44. Michaels AS, Chandrasekaran SK, Shaw JE. 1975. Drug permeation through human skin: theory and in vitro experimental measurement. AIChE J 21:985-996.
45. Albery WJ, Hadgraft J. 1979. Percutaneous absorption: theoretical description. J Pharm Pharmacol 31:129-139.
46. Tojo K. 1987. Random brick model for drug transport across stratum corneum. J Pharm Sci 76:889-891.
47. Edwards DA, Langer R. 1994. A linear theory of transdermal transport phenomena. J Pharm Sci 83:1315-1334.
48. Heisig M, Lieckfeldt R, Wittum G, Mazurkevich G, Lee G. 1996. Non steady-state descriptions of drug permeation through stratum corneum. I. The biphasic brick-and-mortar model. Pharm Res 13:421-426.
49. Charalambopoulou GCh, Karamertzanis P, Kikkinides ES, Stubos AK, Kanellopoulos NK, Papaioannou ATh. 2000. A study on structural and diffusion properties of porcine stratum corneum based on very small angle neutron scattering data. Pharm Res 17:1085-1091.
50. Frasch HF. 2002. A random walk model of skin permeation. Risk Analysis 22:265-276.
51. Yotsuyanagi T, Higuchi WI. 1972. A two phase series model for the transport of steroids across the fully hydrated stratum corneum. J Pharm Pharmac 24:934-941.
52. Lieckfeldt R, Lee G. 1995. Measuring the diffusional pathlength and area within membranes of excised human stratum corneum. J Pharm Pharmacol 47:26-29.
53. Talreja PS, Kleene NK, Pickens WL, Wang T-F, Kasting GB. 2001. Visualization of the lipid barrier and measurement of lipid pathlength in human stratum corneum. AAPS Pharm Sci 3: Article 13.
54. Wang T-F. 2003. Microscopic models for the structure and permeability of the stratum corneum barrier layer of skin. Ph.D. thesis, University at Buffalo, State University of New York.
55. Wang T-F, Kasting GB, Nitsche JM. A multiphase microscopic model for stratum corneum permeability. II. Estimation of physicochemical parameters, and application to a large permeability database. J Pharm Sci (submitted).
56. Jackson JL, Coriell SR. 1963. Effective diffusion constant in a polyelectrolyte solution. J Chem Phys 38:959-968.
57. Brenner H, Edwards DA. 1993. Macrotransport processes. Boston: Butterworth-Heinemann.
58. Brenner H, Adler PM. 1982. Dispersion resulting from flow through spatially periodic porous media. II. Surface and intraparticle transport. Phil Trans R Soc London A 307:149-200.
59. Warner RR, Myers MC, Taylor DA. 1988. Electron probe analysis of human skin: determination of the water concentration profile. J Invest Dermatol 90:218-224.
60. Caspers PJ, Lucassen GW, Bruining HA, Puppels GJ. 2000. Automated depth-scanning confocal Raman microspectrometer for rapid in vivo determination of water concentration profiles in human skin. J Raman Spectrosc 31:813-818.
61. Kasting GB, Barai ND. 2003. Equilibrium water sorption in human stratum corneum. J Pharm Sci 92:1624-1631.
62. Bouwstra JA, de Graaff A, Gooris GS, Nijsse J, Wiechers JW, van Aelst AC. 2003. Water distribution and related morphology in human stratum corneum at different hydration levels. J Invest Dermatol 120:750-758.
63. Warner RR, Stone KJ, Boissy YL. 2003. Hydration disrupts human stratum corneum ultrastructure. J Invest Dermatol 120:275-284.
64. Anissimov YG, Roberts MS. 2004. Diffusion modeling of percutaneous absorption kinetics: 3. Variable diffusion and partition coefficients, consequences for stratum corneum depth profiles and desorption kinetics. J Pharm Sci 93:470-487.
65. Mueller B, Anissimov YG, Roberts MS. 2003. Unexpected clobetasol propionate profile in human stratum corneum after topical application in vitro. Pharm Res 20:1835-1837.
66. Cleek RL, Bunge AL. 1993. A new method for estimating dermal absorption from chemical exposure. 1. General approach. Pharm Res 10:497-506.
67. Bunge AL, Cleek RL. 1995. A new method for estimating dermal absorption from chemical exposure: 2. Effect of molecular weight and octanol-water partitioning. Pharm Res 12:88-95.
68. Bouwstra JA, Gooris GS, van der Spek JA, Bras W. 1991. Structural investigations of human stratum corneum by small-angle X-ray scattering. J Invest Dermatol 97:1005-1012.
69. Hatcher ME, Plachy WZ. 1993. Dioxygen diffusion in the stratum corneum: an EPR spin label study. Biochim Biophys Acta 1149:73-78.
70. Nitsche JM, Wang TF, Kasting GB. 2006. A two-phase analysis of solute partitioning into the stratum corneum. J Pharm Sci 95:649-666.
71. Jin B, Hopfinger AJ. 1996. Characterization of lipid membrane dynamics by simulation: 3. Probing molecular transport across the phospholipid bilayer. Pharm Res 13:1786-1794.
72. Marrink S-J, Berendsen HJC. 1994. Simulation of water transport through a lipid membrane. J Phys Chem 98:4155-4168.
73. Mitragotri S, Johnson ME, Blankschtein D, Langer R. 1999. An analysis of the size selectivity of solute partitioning, diffusion, and permeation across lipid bilayers. Biophys J 77:1268-1283.
74. Haines TH, Liebovitch LS. 1995. A molecular mechanism for the transport of water across phospholipid bilayers, Chapter 6. In: Disalvo EA, Simon SA, editors. Permeability and stability of lipid bilayers. Boca Raton, FL: CRC Press, pp 123-136.
75. Träuble H. 1971. The movement of molecules across lipid membranes: a molecular theory. J Membrane Biol 4:193-208.
76. Johnson ME, Berk DA, Blankschtein D, Golan DE, Jain RK, Langer RS. 1996. Lateral diffusion of small compounds in human stratum corneum and model lipid bilayer systems. Biophys J 71:2656-2668.
77. Saffman PG, Delbrück M. 1975. Brownian motion in biological membranes. Proc Natl Acad Sci USA 72:3111-3113.
78. Nemes Z, Steinert PM. 1999. Bricks and mortar of the epidermal barrier. Exp Molecular Med 31:5-19.
79. Kasting GB, Barai ND, Wang T-F, Nitsche JM. 2003. Mobility of water in human stratum corneum. J Pharm Sci 92:2326-2340.
80. Swartzendruber DC, Wertz PW, Madison KC, Downing DT. 1987. Evidence that the corneocyte has a chemically bound lipid envelope. J Invest Dermatol 88:709-713.
81. Abdulmajed K, Heard CM, McGuigan C, Pugh WJ. 2004. Topical delivery of retinyl ascorbate co-drug. 2. Comparative skin tissue and keratin binding studies. Skin Pharmacol Physiol 17:274-282.
82. Guo X, Imhof RE, de Rigal J. 2001. Spectroscopic study of water-keratin interactions in stratum corneum. Analytical Sciences 17:s342-s345.
83. Tomadakis MM, Sotirchos SV. 1993. Transport properties of random arrays of freely overlapping cylinders with various orientation distributions. J Chem Phys 98:616-626.
84. Mottram JT, Taylor R. 1987. Thermal conductivity of fibre-phenolic resin composites. Part II: numerical evaluation. Compos Sci Tech 29:211-232.
85. Packer KJ, Sellwood TC. 1978. Proton magnetic resonance studies of hydrated stratum corneum. Part 2.-Self-diffusion. J Chem Soc Faraday Trans II 74:1592-1606.
86. Poling BE, Prausnitz JM, O'Connell JP. 2001. The properties of gases and liquids, 5th edn. New York: McGraw-Hill.
87. de Gier J. 1993. Osmotic behaviour and permeability properties of liposomes. Chem Phys Lip 64:187-196.
88. MEDCHEM database and CLOGP Program Vers 2.0.0. 1999. Claremont, CA: BioByte, Inc.
89. Phillips RJ, Deen WM, Brady JF. 1990. Hindered transport in fibrous membranes and gels: effect of solute size and fiber configuration. J Colloid Interface Sci 139:363-373.
90. Nemanic MK, Elias PM. 1980. In situ precipitation: a novel cytochemical technique for visualization of permeability pathways in mammalian stratum corneum. J Histochem Cytochem 28:573-578.
91. Monteiro-Riviere NA, Inman AO, Riviere JE. 1994. Identification of the pathway of iontophoretic drug delivery: light and ultrastructural studies using mercuric chloride in pigs. Pharm Res 11:251-256.
92. Menon GK, Bommannan DB, Elias PM. 1994. High-frequency sonophoresis: permeation pathways and structural basis for enhanced permeability. Skin Pharmacol 7:130-139.
93. Simonetti O, Hoogstraate AJ, Bialik W, Kempenaar JA, Schrijvers AHGJ, Boddé HE, Ponec M. 1995. Visualization of diffusion pathways across the stratum corneum of native and in-vitro-reconstructed epidermis by confocal laser scanning microscopy. Arch Dermatol Res 287:465-473.
94. Menon GK, Elias PM. 1997. Morphologic basis for a pore-pathway in mammalian stratum corneum. Skin Pharmacol 10:235-246.
95. Yu B, Kim KH, So PTC, Blankschtein D, Langer R. 2003. Visualization of oleic acid-induced transdermal diffusion pathways using two-photon fluorescence microscopy. J Invest Dermatol 120:448-455.
96. Hanson KM, Behne MJ, Barry NP, Mauro TM, Gratton E, Clegg RM. 2002. Two-photon fluorescence lifetime imaging of the skin stratum corneum pH gradient. Biophys J 83:1682-1690.
97. Kasting GB, Miller MM, Talreja PS. 2005. Evaluation of stratum corneum heterogeneity. In: Bronaugh RL, Maibach HI, editors. Percutaneous absorption. New York: Taylor and Francis, pp 193-212.
98. Nitsche JM. 1991. Hydrodynamic coupling and non-equilibrium distribution in pore diffusion of nonspherical fine particles. Particulate Sci Technol 9:135-148.
99. Perry D, Ward WJ, Cussler EL. 1989. Unsteady diffusion in barrier membranes. J Membrane Sci 44:305-311.