Penetration of nanoparticles into human skin

Current Pharmaceutical Design

Volumn 19, Issue 35, 2013, Pages 6353-6366

  Liang, Xiao Wen ^a   Xu, Zhi Ping ^a   Grice, Jeffrey ^a   Zvyagin, Andrei V ^b   Roberts, Michael S ^a,c   Liu, Xin ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MACQUARIE UNIVERSITY   (Australia)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Nanoparticles; Skin penetration; Stratum corneum

Indexed keywords

ALCOHOL; CARBON NANOTUBE; DODECYL SULFATE SODIUM; FLUORESCENT DYE; FULLERENE; GOLD NANOPARTICLE; LIPOSOME; NANOPARTICLE; OLEIC ACID; POLYGLACTIN; POLYSTYRENE; QUANTUM DOT; SILVER NANOPARTICLE; SOLVENT; SURFACTANT; TITANIUM DIOXIDE; ZINC OXIDE;

DERMIS; EPIDERMIS; EPIDERMIS BASAL LAYER; EPIDERMIS GRANULAR LAYER; EPIDERMIS STRATUM GERMINATIVUM; HUMAN; HYDROPHILICITY; IONTOPHORESIS; LIPOPHILICITY; NANOTECHNOLOGY; NANOTOXICOLOGY; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; REVIEW; SEBACEOUS GLAND; SKIN PENETRATION; SKIN STRUCTURE; SOLUTE; SPECIES DIFFERENCE; STRATUM CORNEUM; SURFACE PROPERTY; SWEAT GLAND; TRANSPORT KINETICS;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; NANOPARTICLES; NANOTECHNOLOGY; PARTICLE SIZE; PERMEABILITY; SKIN; SKIN ABSORPTION; SURFACE PROPERTIES;

EID: 84887946546     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319350011     Document Type: Review

References (112)

1. Baroli B. Penetration of nanoparticles and nanomaterials in the skin: fiction or reality? J Pharm Sci 2010; 99: 21-50.
2. Alberti I, Grenier A, Kraus H, Carrara DN. Pharmaceutical development and clinical effectiveness of a novel gel technology for transdermal drug delivery. Expert Opin Drug Deliv 2005; 2: 935-50.
3. Barry BW. Breaching the skin's barrier to drugs. Nat Biotechnol 2004; 22: 165-7.
4. Choi EH, Lee SH, Ahn SK, Hwang SM. The pretreatment effect of chemical skin penetration enhancers in transdermal drug delivery using iontophoresis. Skin Pharmacol Appl 1999; 12: 326-35.
5. de Leeuw J, de Vijlder HC, Bjerring P, Neumann HAM. Liposomes in dermatology today. J Eur Acad Dermatol 2009; 23: 505-16.
6. Lauer AC, Lieb LM, Ramachandran C, Flynn GL, Weiner ND. Transfollicular drug delivery. Pharm Res 1995; 12: 179-86.
7. Swain S, Beg S, Singh A, Patro C, Rao ME. Advanced techniques for penetration enhancement in transdermal drug delivery system. Curr Drug Deliv 2011; 8: 456-73.
8. Warheit DB, Sayes CM, Reed KL, Swain KA. Health effects related to nanoparticle exposures: Environmental, health and safety considerations for assessing hazards and risks. Pharmacol Therapeut 2008; 120: 35-42.
9. Lewinski N, Colvin V, Drezek R. Cytotoxicity of nanoparticles. Small 2008; 4: 26-49.
10. Robertson TA, Sanchez WY, Roberts MS. Are commercially available nanoparticles safe when applied to the skin? J Biomed Nanotechnol 2010; 6: 452-68.
11. Desai P, Patlolla RR, Singh M. Interaction of nanoparticles and cell-penetrating peptides with skin for transdermal drug delivery. Mol Membr Biol 2010; 27: 247-59.
12. DeLouise LA. Applications of nanotechnology in dermatology. The Journal of investigative dermatology 2012; 132: 964-75.
13. Labouta HI, Schneider M. Interaction of inorganic nanoparticles with the skin barrier: current status and critical review. Nanomed-Nanotechnol 2013; 9: 39-54.
14. Roberts MS, Walters KA. Human skin morphology and dermal absorption. In: Roberts MS, Walters KA, ed. Dermal absorption and toxicity assessment. Healthcare: New York, 2008: 1-15.
15. Menon GK. New insights into skin structure: scratching the surface. Adv Drug Deliver Rev 2002; 54: S3-S17.
16. Monteiro-Riviere NA. Structure and function of skin. In: Monteiro-Riviere NA, ed. Toxicology of the skin. Informa Healthcare: New York 2010; pp. 3-8.
17. Magnusson BM, Walters KA, Roberts MS. Veterinary drug delivery: potential for skin penetration enhancement. Adv Drug Deliver Rev 2001; 50: 205-27.
18. Hansen S, Naegel A, Heisig M, et al. The role of corneocytes in skin transport revised--a combined computational and experimental approach. Pharm Res 2009; 26: 1379-97.
19. Proksch E, Holleran WM, Menon GK, Elias PM, Feingold KR. Barrier function regulates epidermal lipid and DNA synthesis. Br J Dermatol 1993; 128: 473-82.
20. Lademann J, Otberg N, Richter H, et al. Application of optical noninvasive methods in skin physiology: a comparison of laser scanning microscopy and optical coherent tomography with histological analysis. Skin Res Technol 2007; 13: 119-32.
21. Labouta HI, Liu DC, Lin LL, et al. Gold nanoparticle penetration and reduced metabolism in human skin by toluene. Pharm Res 2011; 28: 2931-44.
22. Silver FH, Freeman JW, DeVore D. Viscoelastic properties of human skin and processed dermis. Skin Res Technol 2001; 7: 18-23.
23. Benedetti MS, Whomsley R, Poggesi I, et al. Drug metabolism and pharmacokinetics. Drug Metab Rev 2009; 41: 344-390.
24. Donovan J. Review of the hair follicle origin hypothesis for basal cell carcinoma. Dermatol. Surg. 2009; 35: 1311-23.
25. Schatzlein A, Cevc G. Non-uniform cellular packing of the stratum corneum and permeability barrier function of intact skin: a highresolution confocal laser scanning microscopy study using highly deformable vesicles (Transfersomes). Br J Dermatol 1998; 138: 583-92.
26. Roberts MS, Cross SE, Pellett MA. Skin transport. In: Walters KA, ed. Dermatological and transdermal formulations. Marcel Dekker: New York 2002; pp. 94-9.
27. Scheuplein RJ. Permeability of the skin: a review of major concepts. Curr Probl Dermatol 1978; 7: 172-86.
28. Elias PM, Friend DS. The permeability barrier in mammalian epidermis. J Cell Biol 1975; 65: 180-91.
29. Potts RO, Guy RH. A predictive algorithm for skin permeability: the effects of molecular size and hydrogen bond activity. Pharm Res 1995; 12: 1628-33.
30. Prow TW, Grice JE, Lin LL, et al. Nanoparticles and microparticles for skin drug delivery. Adv Drug Deliver Rev 2011; 63: 470-91.
31. Toll R, Jacobi U, Richter H, Lademann J, Schaefer H, Blume-Peytavi U. Penetration profile of microspheres in follicular targeting of terminal hair follicles. J Invest Dermatol 2004; 123: 168-76.
32. Liu X, Grice JE, Lademann J, et al. Hair follicles contribute significantly to penetration through human skin only at times soon after application as a solvent deposited solid in man. Br J Clin Pharmacol 2011; 72: 768-74.
33. Grice JE, Ciotti S, Weiner N, Lockwood P, Cross SE, Roberts MS. Relative uptake of minoxidil into appendages and stratum corneum and permeation through human skin in vitro. J Pharm Sci 2010; 99: 712-8.
34. Lademann J, Richter H, Teichmann A, et al. Nanoparticles-An efficient carrier for drug delivery into the hair follicles. Eur J Pharm Biopharm 2007; 66: 159-64.
35. Otberg N, Richter H, Schaefer H, Blume-Peytavi U, Sterry W, Lademann J. Variations of hair follicle size and distribution in different body sites. J Invest Dermatol 2004; 122: 14-19.
36. Bouwstra JA, Ponec M. The skin barrier in healthy and diseased state. Bba-Biomembranes 2006; 1758: 2080-95.
37. Kao J, Patterson FK, Hall J. Skin penetration and metabolism of topically applied chemicals in six mammalian species, including man: an in vitro study with benzo[a]pyrene and testosterone. Toxicol Appl Pharm 1985; 81: 502-16.
38. Robertson K, Rees JL. Variation in epidermal morphology in human skin at different body sites as measured by reflectance confocal microscopy. Acta Derm-Venereol 2010; 90: 368-73.
39. Holbrook KA, Odland GF. Regional differences in the thickness (cell layers) of the human stratum corneum: an ultrastructural analysis. J Invest Dermatol 1974; 62: 415-22.
40. Zhen YX, Suetake T, Tagami H. 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 1999; 291: 555-9.
41. Misra SK, Mohn D, Brunner TJ, et al. Comparison of nanoscale and microscale bioactive glass on the properties of P(3HB)/Bioglass (R) composites. Biomaterials 2008; 29: 1750-61.
42. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science 2006; 311: 622-7.
43. Teow Y, Asharani PV, Hande MP, Valiyaveettil S. Health impact and safety of engineered nanomaterials. Chem Commun 2011; 47: 7025-38.
44. Gratieri T, Schaefer UF, Jing L, et al. Penetration of quantum dot particles through human skin. J Biomed Nanotechnol 2010; 6: 586-95.
45. Filon FL, Crosera M, Adami G, Bovenzi M, Rossi F, Maina G. Human skin penetration of gold nanoparticles through intact and damaged skin. Nanotoxicology 2011; 5: 493-501.
46. Larese FF, D'Agostin F, Crosera M, et al. Human skin penetration of silver nanoparticles through intact and damaged skin. Toxicology 2009; 255: 33-7.
47. Pflucker F, Wendel V, Hohenberg H, et al. The human stratum corneum layer: An effective barrier against dermal uptake of different forms of topically applied micronised titanium dioxide. Skin Pharmacol Appl 2001; 14: 92-7.
48. Gontier E, Ynsa MD, Biro T, et al. Is there penetration of titania nanoparticles in sunscreens through skin? A comparative electron and ion microscopy study. Nanotoxicology 2008; 2: 218-31.
49. Roberts MS, Roberts MJ, Robertson TA, et al. In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver. J Biophotonics 2008; 1: 478-93.
50. Vogt A, Combadiere B, Hadam S, et al. 40 nm, but not 750 or 1, 500 nm, nanoparticles enter epidermal CD1a+ cells after transcutaneous application on human skin. J Invest Dermatol 2006; 126: 1316-22.
51. Campbell CS, Contreras-Rojas LR, Delgado-Charro MB, Guy RH. Objective assessment of nanoparticle disposition in mammalian skin after topical exposure. J Control Release 2012; 162: 201-207.
52. Alvarez-Roman R, Naik A, Kalia Y, Guy RH, Fessi H. Skin penetration and distribution of polymeric nanoparticles. J Control Release 2004; 99: 53-62.
53. Sonavane G, Tomoda K, Sano A, Ohshima H, Terada H, Makino K. In vitro permeation of gold nanoparticles through rat skin and rat intestine: Effect of particle size. Colloid Surface B 2008; 65: 1-10.
54. Patzelt A, Richter H, Knorr F, et al. Selective follicular targeting by modification of the particle sizes. J Control Release 2011; 150: 45-8.
55. Lademann J, Patzelt A, Richter H, Antoniou C, Sterry W, Knorr F. Determination of the cuticula thickness of human and porcine hairs and their potential influence on the penetration of nanoparticles into the hair follicles. J Biomed Opt 2009; 14: 021014.
56. Ryman-Rasmussen JP, Riviere JE, Monteiro-Riviere NA. Penetration of intact skin by quantum dots with diverse physicochemical properties. Toxicol Sci 2006; 91: 159-65.
57. Cevc G, Blume G. Lipid vesicles penetrate into intact skin owing to the transdermal osmotic gradients and hydration force. Biochim Biophys Acta 1992; 1104: 226-32.
58. Cevc G, Blume G. Hydrocortisone and dexamethasone in very deformable drug carriers have increased biological potency, prolonged effect, and reduced therapeutic dosage. Bba-Biomembranes 2004; 1663: 61-73.
59. Gonzalez-Rodriguez ML, Rabasco AM. Charged liposomes as carriers to enhance the permeation through the skin. Expert Opin Drug Deliv 2011; 8: 857-871.
60. Geusens B, Van Gele M, Braat S, et al. Flexible nanosomes (SECosomes) enable efficient siRNA delivery in cultured primary skin cells and in the viable epidermis of ex vivo human skin. Adv Funct Mater 2010; 20: 4077-90.
61. Jung S, Patzelt A, Otberg N, Thiede G, Sterry W, Lademann J. Strategy of topical vaccination with nanoparticles. J Biomed Opt 2009; 14: 021001.
62. Kohli AK, Alpar HO. Potential use of nanoparticles for transcutaneous vaccine delivery: effect of particle size and charge. Int J Pharm 2004; 275: 13-17.
63. Lopez RF, Seto JE, Blankschtein D, Langer R. Enhancing the transdermal delivery of rigid nanoparticles using the simultaneous application of ultrasound and sodium lauryl sulfate. Biomaterials 2011; 32: 933-41.
64. Prow TW, Monteiro-Riviere NA, Inman AO, et al. Quantum dot penetration into viable human skin. Nanotoxicology 2012; 6: 173-85.
65. Wu X, Landfester K, Musyanovych A, Guy RH. Disposition of charged nanoparticles after their topical application to the skin. Skin Pharmacol Phys 2010; 23: 117-23.
66. Cornwell PA, Tubek J, van Gompel HAHP, Little CJ, Wiechers JW. Glyceryl monocaprylate/caprate as a moderate skin penetration enhancer. Int J Pharm 1998; 171: 243-55.
67. Wohlrab J, Klapperstuck T, Reinhardt HW, Albrecht M. Interaction of epicutaneously applied lipids with stratum corneum depends on the presence of either emulsifiers or hydrogenated phosphatidylcholine. Skin Pharmacol Phys 2010; 23: 298-305.
68. Baroli B, Ennas MG, Loffredo F, Isola M, Pinna R, Lopez-Quintela MA. Penetration of metallic nanoparticles in human full-thickness skin. J Invest Dermatol 2007; 127: 1701-12.
69. El Maghraby GMM, Williams AC, Barry BW. Interactions of surfactants (edge activators) and skin penetration enhancers with liposomes. Int J Pharm 2004; 276: 143-61.
70. Goppert TM, Muller RH. Polysorbate-stabilized solid lipid nanoparticles as colloidal carriers for intravenous targeting of drugs to the brain: Comparison of plasma protein adsorption patterns. J Drug Target 2005; 13: 179-87.
71. Batheja P, Sheihet L, Kohn J, Singer AJ, Michniak-Kohn B. Topical drug delivery by a polymeric nanosphere gel: Formulation optimization and in vitro and in vivo skin distribution studies. J Control Release 2011; 149: 159-67.
72. Alves MP, Scarrone AL, Santos M, Pohlmann AR, Guterres SS. Human skin penetration and distribution of nimesulide from hydrophilic gels containing nanocarriers. Int J Pharm 2007; 341: 215-20.
73. Glavas-Dodov M, Goracinova K, Mladenovska K, Fredro-Kumbaradzi E. Release profile of lidocaine HCl from topical liposomal gel formulation. Int J Pharm 2002; 242: 381-4.
74. Pople PV, Singh KK. Development and evaluation of topical formulation containing solid lipid nanoparticles of vitamin A. Aaps Pharmscitech 2006; 7: 91.
75. Muller RH, Radtke M, Wissing SA. Solid lipid nanoparticles (SLN) and nanostructured lipid carriers (NLC) in cosmetic and dermatological preparations. Adv Drug Deliver Rev 2002; 54 Suppl 1: S131-55.
76. Souto EB, Almeida AJ, Muller RH. Lipid nanoparticles (SLN (R), NLC (R) for cutaneous drug delivery: Structure, protection and skin effects. J Biomed Nanotechnol 2007; 3: 317-31.
77. Allenby AC, Fletcher J, Schock C, Tees TFS. Effect of heat, ph and organic solvents on electrical impedance and permeability of excised human skin. Brit J Dermatol 1969; 81: 31-9.
78. Barry BW. Mode of action of penetration enhancers in human skin. J Control Release 1987: 85-98.
79. Van Hal DA, Jeremiasse E, Junginger HE, Spies F, Bouwstra JA. Structure of fully hydrated human stratum corneum: A freeze fracture electron microscopy study. J Invest Dermatol 1996; 106: 89-95.
80. Wagner H, Kostka KH, Lehr CM, Schaefer UF. pH profiles in human skin: influence of two in vitro test systems for drug delivery testing. Eur J Pharm Biopharm 2003; 55: 57-65.
81. Banga AK, Bose S, Ghosh TK. Iontophoresis and electroporation: comparisons and contrasts. Int J Pharm 1999; 179: 1-19.
82. Jadoul A, Bouwstra J, Preat VV. Effects of iontophoresis and electroporation on the stratum corneum. Review of the biophysical studies. Adv Drug Deliver Rev 1999; 35: 89-105.
83. Tezel A, Sens A, Mitragotri S. A theoretical analysis of lowfrequency sonophoresis: Dependence of transdermal transport pathways on frequency and energy density. Pharm Res 2002; 19: 1841-6.
84. Grewal BS, Naik A, Irwin WJ, et al. Transdermal macromolecular delivery: Real-time visualization of iontophoretic and chemically enhanced transport using two-photon excitation microscopy. Pharm Res 2000; 17: 788-95.
85. Katikaneni S, Li GH, Badkar A, Banga AK. Transdermal delivery of a similar to 13 kDa protein-an in vivo comparison of physical enhancement methods. J Drug Target 2010; 18: 141-147.
86. Mitragotri S, Blankschtein D, Langer R. Transdermal drug delivery using low-frequency sonophoresis. Pharm Res 1996; 13: 411-20.
87. Donnelly RF, Morrow DIJ, Fay F, et al. Microneedle-mediated intradermal nanoparticle delivery: Potential for enhanced local administration of hydrophobic pre-formed photosensitisers. Photodiagn Photodyn 2010; 7: 222-31.
88. Heard CA, Kung D, Thomas CP. Skin penetration enhancement of mefenamic acid by ethanol and 1, 8-cineole can be explained by the 'pull' effect. Int J Pharm 2006; 321: 167-70.
89. Kuo TR, Wu CL, Hsu CT, et al. Chemical enhancer induced changes in the mechanisms of transdermal delivery of zinc oxide nanoparticles. Biomaterials 2009; 30: 3002-8.
90. Lo W, Ghazaryan A, Tso CH, et al. Oleic acid-enhanced transdermal delivery pathways of fluorescent nanoparticles. Appl Phys Lett 2012; 100.
91. Seto JE, Polat BE, Lopez RFV, Blankschtein D, Langer R. Effects of ultrasound and sodium lauryl sulfate on the transdermal delivery of hydrophilic permeants: Comparative in vitro studies with fullthickness and split-thickness pig and human skin. J Control Release 2010; 145: 26-32.
92. Mortensen LJ, Oberdorster G, Pentland AP, Delouise LA. In vivo skin penetration of quantum dot nanoparticles in the murine model: the effect of UVR. Nano Lett 2008; 8: 2779-87.
93. Rouse JG, Yang J, Ryman-Rasmussen JP, Barron AR, Monteiro-Riviere NA. Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin. Nano Lett 2007; 7: 155-60.
94. Holsapple MP, Farland WH, Landry TD, et al. Research strategies for safety evaluation of nanomaterials, part II: toxicological and safety evaluation of nanomaterials, current challenges and data needs. Toxicol Sci 2005; 88: 12-7.
95. Nowack B, Bucheli TD. Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 2007; 150: 5-22.
96. Benn TM, Westerhoff P. Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 2008; 42: 4133-9.
97. Zhang LW, Monteiro-Riviere NA. Assessment of quantum dot penetration into intact, tape-stripped, abraded and flexed rat skin. Skin Pharmacol Phys 2008; 21: 166-80.
98. Serpone N, Salinaro A, Emeline A. Deleterious effects of sunscreen titanium dioxide nanoparticles on DNA. Efforts to limit DNA damage by particle surface modification. P Soc Photo-Opt Ins 2001; 2: 86-98.
99. Sayes CM, Wahi R, Kurian PA, et al. Correlating nanoscale titania structure with toxicity: A cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells. Toxicol Sci 2006; 92: 174-85.
100. Pernodet N, Fang X, Sun Y, et al. Adverse effects of citrate/gold nanoparticles on human dermal fibroblasts. Small 2006; 2: 766-73.
101. Lin LL, Grice JE, Butler MK, et al. Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin. Pharm Res 2011; 28: 2920-30.
102. Bian SW, Mudunkotuwa IA, Rupasinghe T, Grassian VH. Aggregation and Dissolution of 4 nm ZnO Nanoparticles in Aqueous Environments: Influence of pH, Ionic Strength, Size, and Adsorption of Humic Acid. Langmuir 2011; 27: 6059-68.
103. Song Z, Kelf TA, Sanchez WH, et al. Characterization of optical properties of ZnO nanoparticles for quantitative imaging of transdermal transport. Biomed Opt Express 2011; 2: 3321-33.
104. Pinheiro T, Pallon J, Alves LC, et al. The influence of corneocyte structure on the interpretation of permeation profiles of nanoparticles across skin. Nucl Instrum Meth B 2007; 260: 119-23.
105. Bronaugh RL, Stewart RF, Congdon ER. Methods for in vitro percutaneous absorption studies. II. Animal models for human skin. Toxicol Appl Pharm 1982; 62: 481-8.
106. Ferry LL, Argentieri G, Lochner DH. The comparative histology of porcine and guinea pig skin with respect to iontophoretic drug delivery. Pharm Acta Helv 1995; 70: 43-56.
107. Monteiro-Riviere NA, Bristol DG, Manning TO, Rogers RA, Riviere JE. Interspecies and interregional analysis of the comparative histologic thickness and laser Doppler blood flow measurements at five cutaneous sites in nine species. J Invest Dermatol 1990; 95: 582-6.
108. Kshirsagar SV, Singh B, Fulari SP. Comparative study of human and animal hair in relation with diameter and medullary index. Indian J Foren Med Pathol 2009; 2: 105-108.
109. Adachi K, Yamada N, Yamamoto K, Yoshida Y, Yamamoto O. In vivo effect of industrial titanium dioxide nanoparticles experimentally exposed to hairless rat skin. Nanotoxicology 2010; 4: 296-306.
110. 2 nanoparticles in hairless mice and porcine skin after subchronic dermal exposure. Toxicol Lett 2009; 191: 1-8.
111. Cross SE, Innes B, Roberts MS, Tsuzuki T, Robertson TA, McCormick P. Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation. Skin Pharmacol Phys 2007; 20: 148-54.
112. Samberg ME, Oldenburg SJ, Monteiro-Riviere NA. Evaluation of silver nanoparticle toxicity in skin in vivo and keratinocytes in vitro. Environ Health Persp 2010; 118: 407-13.