• MASOUD ALI KARAMI School of pharmacy, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
  • MARZIE JALILI RAD School of pharmacy, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
  • BEHZAD SHARIF MAKHMAL ZADEH Nanotechnology Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran, School of pharmacy, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
  • ANAYATOLLAH SALIMI Nanotechnology Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran, School of pharmacy, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran



Superoxide dismutase, Niosome, Hair growth, Alopecia areata, Follicular drug delivery


Objective: Alopecia aretea is associated with an increase in free radicals causing damage to hair follicles. Superoxide dismutase (SOD) with sufficient penetration through hair follicles, can prevent their death by its strong antioxidant effects. SOD with high molecular weight underwent limitation in follicular delivery. The aim of this study was the improvement of SOD localization into hair follicles.

Methods: SOD-loaded niosomes were prepared by thin layer hydration method and were used as a vehicle for delivery to hair follicles through guinea pig skin and the synthetic membrane. Particle size, entrapment efficiency, drug release, and permeability parameters through hairly and non-hairly pig skin compared with a synthetic membrane were evaluated.

Results: Niosomes demonstrated 152-325 nm particle size and the SOD burst and sustained release from niosomes were mainly controlled by diffusion and dissolution phenomena. SOD was protected against degradation by niosomes and after six months, enzyme content and activity decreased less than 5%. In comparison with free SOD, niosomes increased SOD affinity to penetration through follicles by interaction with sebum. Likewise, niosome's characters such as type of surfactant, solid lipid/liquid lipid ratio played critical roles on SOD deposition on hair follicles.

Conclusion: Synthetic membrane and hairy guinea pig skin demonstrated similar barrier property against free-SOD thereby implying that free SOD does not interact with guinea pig sebum. Niosomes can introduce a suitable carrier for SOD localization into the hair follicles.


Download data is not yet available.


Reynolds AJ, Jahoda CA. Inductive properties of hair follicle cells. Annals New York Acad Sci 1991;642:226-41.

Sundberg JP, King LE, Basco C. Animal models for the male pattern (androgenetic) alopecia. Eur J Dermatol 2001;11:321-5.

Akar A, Arca E, Erbil H, Akay C, Sayal A, Gur AR. Antioxidant enzymes and lipid peroxidation in the scalp of patients with alopecia areata. J Dermatol Sci 2002;29:85-90.

Zafar R, Abdullateef A, Alzolibani B, Hani A, Al-Shobaili B, Saif GB, et al. Biochemical and immunological studies on erythrocytes superoxide dismutase modified by nitric oxide in patients with alopecia areata: Implications in alopecia patchy persistent and alopecia universalis. Immunol Lett 2014;160:50–7.

Alzolibani AA. Preferential recognition of hydroxyl radical-modified superoxide dismutase by circulating autoantibodies in patients with alopecia areata. Ann Dermatol 2014;25:576-83.

Trüeb RM. The impact of oxidative stress on the hair. Int J Cosmet Sci 2015;37:25-30.

Chitra KP, Pillai KS. Antioxidants in Health. Ind J Physiol Pharmacol 2002;46:1-5.

Seiberg M. Age-induced hair graying. The multiple effects of oxidative stress. Int J Cosmet Sci 2013;35:532-8.

Patzelt A, Knorr F, Blume-Pytavi U, Sterry W, Lademann J. Hair follicles, their disorder, and their opportunities. Drug Discovery Today: Disease Mechanisms 2008;5:173-81.

Fernandes B, Silva R, Ribeiro A, Matamo T, Gomes AC. Improved poly (D, L-Lactide) nanoparticles. The based formulation for hair follicle targeting. Int J Cosmet Sci 2015;32:282-94.

Emerit I, Filipe P, Freitas J. Protective effect of superoxide dismutase against hair graying in a mouse model. Photochem Photobiol 2004;80:579-82.

Diehl C. A novel efficient and safe treatment for atopic dermatitis: topical superoxide dismutase. Dermatol Res Skin Care 2017;1:1-7.

Manca ML, Manconi M, Nacher A, Carbone C, Valenti D, Maccioni AM, et al. Development of novel diolein-niosomes for cutaneous delivery of tretinoin: influence of formulation and in vitro assessment. Int J Pharm 2014;30:176-86.

Manosroi A, Ruksiriwanich W, Abe M, Manosroi J. Transfollicular enhancement of gel containing cationic niosomes loaded with unsaturated fatty acids in rice (Oryza sativa) bran semi-purified fraction. Eur J Pharm Biopharm 2012;18:303-13.

Mohawed O, Ashmonny MM, Elgazayerly ON. Nisome-encapsulated clomipramine for transdermal controlled delivery. Int J Pharm Pharm Sci 2014;6:567-75.

Acharya A, Kumar K, Ahmed MG, Paudel S. A novel approach to increase the bioavailability of candesartan cilexetil by proniosomal gel formulation in vitro evaluation. Int J Pharm Pharm Sci 2016;8:241-6.

Marianecci C, Di marzio L, Rinaldi F, Esposito S, Carafa M. Niosomes from the 80s to present: state of the art. Adv Colloid Interface Sci 2014;205:187-206.

Uchegbu IF, Florence AT. Non-ionic surfactant vesicles (niosomes): physical and pharmaceutical chemistry. Adv Collid Interface Sci 1995;58:1-55.

Tabbakhian M, Tavakoli N, Jaafari MR, Daneshamouz S. Enhancement of follicular delivery of finasteride by liposomes and niosomes: 1. In vitro permeation and in vivo deposition studies using hamster flank and ear models. Int J Pharm 2006:323;1-10.

Muhammad F, Brooks JD, Rivirere JE. Comparative mixture effects of JP-8 additives on the dermal absorption and disposition of jet fuel hydrocarbons in different membrane model systems. Toxicol Lett 2004;150:351-65.

Simon GA, Maibach HI. Relevance of hair lost mouse as an experimental model of percutaneous penetration in man. Skin Pharmacol Appl Skin Physiol 1998;11:80-6.

Anderson KE, Maibach HI, Anjo MD. The guinea pig: an animal model for human skin absorption of hydrocortisone, testosterone and benzoic acid? Br J Dermatol 1980;102:447-53.

Sharif Makhmal Zadeh B, Moghimi HR, Santos P, Lane ME, Hadgraft J. Comparative study of the in vitro permeation characteristic of sulphadiazine across synthetic membranes and eschar tissue. Int Wound J 2008;5:633-8.

Abed E, Yousef SA, Pastore MN, Telaprolu K, Mohammed YH, Namjoshi S, et al. Skin models for the testing of transdermal drugs. Clin Pharmacol 2016;8:163-76.

Bangham A, De Gie J. Osmotic properties and water permeability of phospholipid liquid crystals. Chem Phys Lipid 1967;1:225-31.

Rengel RG, Barisic K, Pavelic Z, Grubisic TZ, Cepelak Z, Filipovic Grcic J. High-efficiency entrapment of superoxide dismutase into mucoadhesive chitosan-coated niosomes. Eur J Pharm Sci 2002;15:441-8.

Celik O, Akbuga J. Preparation of superoxide dismutase loaded chitosan microspheres: characterization and release studies. Eur J Pharm Biopharm 2007;66:42–7.

Wahlberg JE. Transepidermal or transfollicular absorption in vivo and in vitro studies in hairy and non-hairy guinea pig skin with sodium and mercuric chlorides. Acta Derm Venereol 1968;48:336-44.

Otberg N, Richter H, Schaefer H, Blume-Peytavi U, Sterry W, Lademann J. Variation of hair follicle size and distribution in different body sites. J Invest Dermatol 2004;122:14-9.

Wertz PW, Downing DT. Integral lipids of human hair. Lipids 1988;23:878-81.

Schaefer H, Watts F, Brod J, Hel JB. Follicular penetration. In: RC Scott, RH Guy, J Hadgraft. (editors). Prediction of percutaneous penetration, methods, measurement, and modeling. IBC Technical services, London; 2003. p. 63-173.

Lademann J, Richte H, Teichmann A, Otberg N, Blume Peytavi U, Luengo J, et al. Nanoparticles-an efficient carrier for drug delivery into the hair follicles. Eur J Pharm Biopharm 2007;66:159-64.

Voget A, Combadiere B, Hadam S, Stieler KM, Lademann J, Schaefer H, et al. 40 nm but not 750 nm or 1500 nm, nanoparticles enter epidermal CD1cells after transcutaneous application on human skin. J Invest Dermatol 2006;126:1316-22.

Patil PY, Jadhav S. Novel methods for liposome preparation. Chem Phys Lipids 2014;177:8-18.

Wang YE, Gao GQ, Zheng CH, XU DH, Liang WQ. Biodegradable and complex microspheres used for sustained delivery and activity protection of SOD. J Biomed Material Res Part B: Appl Biomat 2006;27:74-8.

Kigasawa K, Miyashita M, Kajimoto K, Kanamura K, Harashima H, Kogure K. Efficient intra-dermal delivery of superoxide dismutase using a combination of niosomes and iontophoresis for protection against UV-Induced skin damaged. Biol Pharm Bull 2012;35:781-5.

Corvo ML, Jorge JCS, Vanthof R, Cruz M, Crommolin JA, Strom G. Superoxide dismutase entrapped in long-circulating liposomes: formulation design and therapeutic activity in rat adjuvant arthritis. Biochem Biophys Acta 2002;1564:227-36.

Porfire AS, Tomuta I, Leucuta SR, Achim M. Superoxide dismutase loaded liposomes. The influence of formulation factors on enzyme encapsulation and release. Farmacia 2013;61:865-73.

Mitragotri S. Modeling skin permeability to hydrophilic and hydrophobic solutes based on four permeation pathways. J Controlled Release 2003;86:69-92.

Schafer Korting M, Mehnert W, Korting HC. Lipid nanoparticles for improved topical application of drugs for skin diseases. Adv Drug Delivery Rev 2007;59:427-43.

Blume Peytavi U, Vogt A. Human hair follicle: reservoir function and selective targeting. Br J Dermatol 2011;165:13-7.

Betz G, Imboden R, Imboden G. Interaction of niosome formulation with human skin in vitro. Int J Pharm 2001;229:117-29.

Karami MA, Sharif Makhmal Zadeh B, Kouchak M, Moghimipur E. Superoxide dismutase loaded solid lipid nanoparticles prepared by cold homogenization method: characterization and permeation study through burned rat skin. Jundishapur J Natur Pharm Prod 2016;11. Doi:10.17795/jjnpp-33968

Toongsuwan S, Li LC, Erickson BK, Chang HC. Formulation and characterization of bupivacaine lipospheres. Int J Pharm 2004;280:57-65.

Manca ML, Castangia I, Zaru M, Nacher A, Valenti D, Fernandez Busquets X. Development of curcumin loaded sodium hyaluronate immobilized vesicles (hyalurosomes) and their potential on skin inflammation and wound restoring. Biomat 2015;77:100-9.

Manca ML, Castangia I, Matricardi P, Lampis S, Fernandez Busquets X, Fadda AM. Molecular arrangements and interconnected bilayer formation induced by alcohol or polyalcohol in phospholipid vesicles. Colloids Surface B: Biointerfaces 2014;117:360-7.



How to Cite




Original Article(s)