N-succinyl chitosan preparation, characterization, properties and biomedical applications: A state of the art review

Reviews in Chemical Engineering

Volumn 31, Issue 6, 2015, Pages 563-597

  Bashir, Shahid ^a   Teo, Yin Yin ^a   Ramesh, S ^a   Ramesh, K ^a   Khan, Amir Azam ^b  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b UNIVERSITI MALAYSIA SARAWAK   (Malaysia)

Author keywords

characteristics; drug delivery; N succinyl chitosan; tissue engineering; wound dressings

Indexed keywords

ACYLATION; BIOCHEMISTRY; BIOCOMPATIBILITY; CHITOSAN; CONTROLLED DRUG DELIVERY; DRUG DELIVERY; MEDICAL APPLICATIONS; TISSUE; TISSUE ENGINEERING;

BIOMATERIAL APPLICATION; BIOMEDICAL APPLICATIONS; BONE TISSUE ENGINEERING; CHARACTERISTICS; N-SUCCINYL-CHITOSAN; STATE-OF-THE ART REVIEWS; TRANSFECTION EFFICIENCY; WOUND DRESSINGS;

TARGETED DRUG DELIVERY;

EID: 84948407790     PISSN: 01678299     EISSN: None     Source Type: Journal    
DOI: 10.1515/revce-2015-0016     Document Type: Review

References (174)

1. Abdelrahman T, Newton H. Wound dressings: principles and practice. Surgery 2011; 29: 491-495.
2. Adkisson HD, Martin JA, Amendola RL, Milliman C, Mauch KA, Katwal AB, Seyedin M, Amendola A, Streeter PR, Buckwalter JA. The potential of human allogeneic juvenile chondrocytes for restoration of articular cartilage. Am J Sports Med 2010; 38: 1324-1333.
3. Aiping Z, Tian C, Lanhua Y, Hao W, Ping L. Synthesis and characterization of N-succinyl-chitosan and its self-assembly of nanospheres. Carbohydr Polym 2006; 66: 274-279.
4. Alves N, Mano J. Chitosan derivatives obtained by chemical modifications for biomedical and environmental applications. Int J Biol Macromol 2008; 43: 401-414.
5. Aoki N, Nishikawa M, Hattori K. Synthesis of chitosan derivatives bearing cyclodextrin and adsorption of p-nonylphenol and bisphenol A. Carbohydr Polym 2003; 52: 219-223.
6. Artursson P, Lindmark T, Davis SS, Illum L. Effect of chitosan on the permeability of monolayers of intestinal epithelial cells (Caco-2). Pharm Res 1994; 11: 1358-1361.
7. Aziz MA, Cabral JD, Brooks HJ, Moratti SC, Hanton LR. Antimicrobial properties of a chitosan dextran-based hydrogel for surgical use. Antimicrob Agents Chemother 2012; 56: 280-287.
8. Bhattarai SR, Remant KC, Aryal S, Khil MS, Kim HY. N-Acylated chitosan stabilized iron oxide nanoparticles as a novel nano-matrix and ceramic modification. Carbohydr Polym 2007; 69: 467-477.
9. Birmingham E, Niebur G, McHugh P. Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur Cell Mater 2012; 23: 13-27.
10. Braga ME, Pato MTV, Silva HS, Ferreira EI, Gil MH, Duarte CM, de Sousa HC. Supercritical solvent impregnation of ophthalmic drugs on chitosan derivatives. J Supercrit Fluids 2008, 44: 245-257.
11. Cao Y, Zhang C, Shen W, Cheng Z, Yu LL, Ping Q. Poly (N-isopropylacrylamide)-chitosan as thermosensitive in situ gel-forming system for ocular drug delivery. J Controlled Release 2007; 120: 186-194.
12. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007; 213: 341-347.
13. Casettari L, Vllasaliu D, Castagnino E, Stolnik S, Howdle S, Illum L. PEGylated chitosan derivatives: synthesis, characterizations and pharmaceutical applications. Prog Polym Sci 2012; 37: 659-685.
14. Chae SY, Son S, Lee M, Jang M-K, Nah J-W. Deoxycholic acid-conjugated chitosan oligosaccharide nanoparticles for efficient gene carrier. J Controlled Release 2005; 109: 330-344.
15. Champagne LM. The synthesis of water soluble N-acyl chitosan derivatives for characterization as antibacterial agents, Louisiana, USA: Xavier University of Louisiana, 2008.
16. Chen J, Jo S, Park K. Polysaccharide hydrogels for protein drug delivery. Carbohydr Polym 1995; 28: 69-76.
17. Choi CY, Kim SB, Pak PK, Yoo DI, Chung YS. Effect of N-acylation on structure and properties of chitosan fibers. Carbohydr Polym 2007; 68: 122-127.
18. Chourasia M, Jain S. Pharmaceutical approaches to colon targeted drug delivery systems. J Pharm Pharm Sci 2003; 6: 33-66.
19. Clark AF, Yorio T. Ophthalmic drug discovery. Nat Rev Drug Discovery 2003; 2: 448-459.
20. Comisar WA, Kazmers NH, Mooney DJ, Linderman JJ. Engineering RGD nanopatterned hydrogels to control preosteoblast behavior: a combined computational and experimental approach. Biomaterials 2007; 28: 4409-4417.
21. Costantino H, Sileno A, Johnson P. Pharmacokinetic attributes of intranasal delivery: case studies and new opportunities. Drug Deliv 2005; 3: 8-11.
22. Costantino HR, Illum L, Brandt G, Johnson PH, Quay SC. Intranasal delivery: physicochemical and therapeutic aspects. Int J Pharm 2007; 337: 1-24.
23. Dai YN, Li P, Zhang JP, Wang AQ, Wei Q. A novel pH sensitive N-succinyl chitosan/alginate hydrogel bead for nifedipine delivery. Biopharm Drug Dispos 2008; 29: 173-184.
24. Desai MP, Labhasetwar V, Amidon GL, Levy RJ. Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharmaceut Res 1996; 13: 1838-1845.
25. Domard A, Rinaudo M, Terrassin C. New method for the quaternization of chitosan. Int J Biol Macromol 1986; 8: 105-107.
26. Eweis M, Elkholy S, Elsabee M. Antifungal efficacy of chitosan and its thiourea derivatives upon the growth of some sugar-beet pathogens. Int J Biol Macromol 2006; 38: 1-8.
27. Fan L, Yu L, Xu Y, Yi C, Cai J, Li M, Huang J. The novel alginate/ N-succinyl-chitosan antibacterial blend fibers. J Appl Polym Sci 2010; 116: 2151-2156.
28. Fan M, Hu Q, Shen K. Preparation and structure of chitosan soluble in wide pH range. Carbohyd Polym 2009; 78: 66-71.
29. Genta I, Conti B, Perugini P, Pavanetto F, Spadaro A, Puglisi G. Bioadhesive microspheres for ophthalmic administration of acyclovir. J Pharm Pharmacol 1997; 49: 737-742.
30. Graisuwan W, Wiarachai O, Ananthanawat C, Puthong S, Soogarun S, Kiatkamjornwong S, Hoven VP. Multilayer film assembled from charged derivatives of chitosan: Physical characteristics and biological responses. J Colloid Interf Sci 2012; 376: 177-188.
31. Griffith LG, Naughton G. Tissue engineering-current challenges and expanding opportunities. Science 2002; 295: 1009-1014.
32. Guo Z, Xing R, Liu S, Zhong Z, Li P. Synthesis and hydroxyl radicals scavenging activity of quaternized carboxymethyl chitosan. Carbohyd Polym 2008; 73: 173-177.
33. Gupta P, Vermani K, Garg S. Hydrogels: from controlled release to pH-responsive drug delivery. Drug Discov Today 2002; 7: 569-579.
34. Ha C-S, Gardella JA. Surface chemistry of biodegradable polymers for drug delivery systems. Chem Rev 2005; 105: 4205-4232.
35. Hasegawa M, Yagi K, Iwakawa S, Hirai M. Chitosan induces apoptosis via caspase-3 activation in bladder tumor cells. Cancer Science 2001; 92: 459-466.
36. Hawary DL, Motaleb MA, Farag H, Guirguis OW, Elsabee MZ. Water-soluble derivatives of chitosan as a target delivery system of 99m Tc to some organs in vivo for nuclear imaging and biodistribution. J Radioanal Nucl Ch 2011; 290: 557-567.
37. He C, Kim SW, Lee DS. In situ gelling stimuli-sensitive block copolymer hydrogels for drug delivery. J Control Release 2008;127: 189-207.
38. Hirano S, Moriyasu T. Some novel N-(carboxyacyl) chitosan filaments. Carbohyd Polym 2004; 55: 245-248.
39. Hirano S, Yamaguchi Y, Kamiya M. Novel N-saturated-fatty-acyl derivatives of chitosan soluble in water and in aqueous acid and alkaline solutions. Carbohyd Polym 2002; 48: 203-207.
40. Hou Z, Han J, Zhan C, Zhou C, Hu Q, Zhang Q. Synthesis and evaluation of N-succinyl-chitosan nanoparticles toward local hydroxycamptothecin delivery. Carbohyd Polym 2010; 81: 765-768.
41. Hunziker E. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthr Cartilage 2002; 10: 432-463.
42. Illum L. Nasal drug delivery - possibilities, problems and solutions. J Control Release 2003; 87: 187-198.
43. Inta O, Yoksan R, Limtrakul J. Hydrophobically modified chitosan: A bio-based material for antimicrobial active film. Materials Science and Engineering: C 2014; 42: 569-577.
44. Islam A, Yasin T. Controlled delivery of drug from pH sensitive chitosan/poly (vinyl alcohol) blend. Carbohyd Polym 2012; 88: 1055-1060.
45. Ito T, Yeo Y, Highley CB, Bellas E, Benitez CA, Kohane DS. The prevention of peritoneal adhesions by in situ cross-linking hydrogels of hyaluronic acid and cellulose derivatives. Biomaterials 2007; 28: 975-983.
46. Jain N, Rajoriya V, Jain PK, Jain AK. Lactosaminated-N-succinyl chitosan nanoparticles for hepatocyte-targeted delivery of acyclovir. J Nanopart Res 2014; 16: 1-14.
47. Jayakumar R, Nwe N, Tokura S, Tamura H. Sulfated chitin and chitosan as novel biomaterials. Int J Biol Macromol 2007; 40: 175-181.
48. Jayakumar R, Prabaharan M, Nair S, Tokura S, Tamura H, Selvamurugan N. Novel carboxymethyl derivatives of chitin and chitosan materials and their biomedical applications. Prog Mater Sci 2010; 55: 675-709.
49. Jin R, Hiemstra C, Zhong Z, Feijen J. Enzyme-mediated fast in situ formation of hydrogels from dextran-tyramine conjugates. Biomaterials 2007; 28: 2791-2800.
50. Jin R, Moreira Teixeira L, Dijkstra PJ, Karperien M, Van Blitterswijk C, Zhong Z, Feijen J. Injectable chitosan-based hydrogels for cartilage tissue engineering. Biomaterials 2009; 30: 2544-2551.
51. Johnson PH, Quay SC. Advances in nasal drug delivery through tight junction technology. Expert Opin Drug Del 2005; 2: 281-298.
52. Kajihara M, Sugie T, Hojo T, Maeda H, Sano A, Fujioka K, Sugawara S, Urabe Y. Development of a new drug delivery system for protein drugs using silicone (II). J Control Release 2001; 73: 279-291.
53. Kajjari PB, Manjeshwar LS, Aminabhavi TM. Novel blend microspheres of poly (vinyl alcohol) and succinyl chitosan for controlled release of nifedipine. Polymer bulletin 2013; 70: 3387-3406.
54. Karadeniz F, Karagozlu MZ, Pyun S-Y, Kim S-K. Sulfation of chitosan oligomers enhances their anti-adipogenic effect in 3T3-L1 adipocytes. Carbohyd Polym 2011; 86: 666-671.
55. Kato Y, Onishi H, Machida Y. Biological fate of highly-succinylated N-succinyl-chitosan and antitumor characteristics of its water-soluble conjugate with mitomycin C at iv and ip administration into tumor-bearing mice. Biol Pharm Bull 2000a; 23: 1497-1503.
56. Kato Y, Onishi H, Machida Y. Evaluation of N-succinyl-chitosan as a systemic long-circulating polymer. Biomaterials 2000b; 21: 1579-1585.
57. Kato Y, Onishi H, Machida Y. Biological characteristics of lactosaminated N-succinyl-chitosan as a liver-specific drug carrier in mice. J Control Release 2001a; 70: 295-307.
58. Kato Y, Onishi H, Machida Y. Lactosaminated and intact N-succinylchitosans as drug carriers in liver metastasis. Int J Pharm 2001b; 226: 93-106.
59. Khor E. Chitin: a biomaterial in waiting. Curr Opin Solid St M 2002; 6: 313-317.
60. Kim S, Kim J-H, Jeon O, Kwon IC, Park K. Engineered polymers for advanced drug delivery. Eur J Pharm Biopharm 2009; 71: 420-430.
61. Kim IL, Mauck RL, Burdick JA. Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 2011; 32: 8771-8782.
62. Kong M, Chen XG, Xing K, Park HJ. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int J Food Microbiol 2010; 144: 51-63.
63. Kontos S, Hubbell JA. Drug development: longer-lived proteins. Chem Soc Rev 2012; 41: 2686-2695.
64. Kotzé AF, Thanou MM, Lueben HL, A. De Boer, Verhoef J, Junginger HE. Enhancement of paracellular drug transport with highly quaternized N-trimethyl chitosan chloride in neutral environments: In vitro evaluation in intestinal epithelial cells (Caco-2). J Pharm Sci 1999; 88: 253-257.
65. Kumar MNR. A review of chitin and chitosan applications. React Funct Polym 2000; 46: 1-27.
66. Kurita K. Chemical modifications of chitin and chitosan. Springer: Chitin in Nature and Technology, 1986: 287-293.
67. Kurita K. Controlled functionalization of the polysaccharide chitin. Prog Polym Sci 2001; 26: 1921-1971.
68. Kurita K. Chitin and chitosan: functional biopolymers from marine crustaceans. Mar Biotechnol 2006; 8: 203-226.
69. Kyzas GZ, Siafaka PI, Pavlidou EG, Chrissafis KJ, Bikiaris DN. Synthesis and adsorption application of succinyl-grafted chitosan for the simultaneous removal of zinc and cationic dye from binary hazardous mixtures. Chem Eng J 2015; 259: 438-448.
70. Le Bourlais C, Acar L, Zia H, Sado PA, Needham T, Leverge R. Ophthalmic drug delivery systems - recent advances. Prog Retin Eye Res 1998; 17: 33-58.
71. Li Z, Ramay HR, Hauch KD, Xiao D, Zhang M. Chitosan-alginate hybrid scaffolds for bone tissue engineering. Biomaterials 2005; 26: 3919-3928.
72. Li Y, Rodrigues J, Tomas H. Injectable and biodegradable hydrogels: gelation, biodegradation and biomedical applications. Chem Soc Rev 2012a; 41: 2193-2221.
73. Li J, Cai J, Zhong L, Du Y. Immobilization of a protease on modified chitosan beads for the depolymerization of chitosan. Carbohyd Polym 2012b; 87: 2697-2705.
74. Lim K, Kim J, Seonwoo H, Park SH, Choung P-H, Chung JH. In vitro effects of low-intensity pulsed ultrasound stimulation on the osteogenic differentiation of human alveolar bone-derived mesenchymal stem cells for tooth tissue engineering. Bio Med Res Int 2013; 2013: 1-15.
75. Liu X, Peng W, Wang Y, Zhu M, Sun T, Peng Q, Zeng Y, Feng B, Lu X, Weng J. Synthesis of an RGD-grafted oxidized sodium alginate-N-succinyl chitosan hydrogel and an in vitro study of endothelial and osteogenic differentiation. J Mater Chem B 2013; 1: 4484-4492.
76. Lu B, Sun Y-X, Li Y-Q, Zhang X-Z, Zhuo R-X. N-Succinyl-chitosan grafted with low molecular weight polyethylenimine as a serum-resistant gene vector. Mol BioSystems 2009; 5: 629-637.
77. Lu B, Wu D-Q, Zheng H, Quan C-Y, Zhang X-Z, Zhuo R-X Galactosyl conjugated N-succinyl-chitosan-graft-polyethylenimine for targeting gene transfer. Mol Biosystems 2010; 6: 2529-2538.
78. Lü S, Liu M, Ni B. An injectable oxidized carboxymethylcellulose/ N-succinyl-chitosan hydrogel system for protein delivery. Chem Eng J 2010; 160: 779-787.
79. Luo H, Li J, Chen X. Antitumor effect of N-succinyl-chitosan nanoparticles on K562 cells. Biomed Pharmacother 2010; 64: 521-526.
80. Luo H, Su H, Wang X, Wang L, Li J. N-Succinyl-chitosan nanoparticles induced mitochondria-dependent apoptosis in K562. Mol Cell Probe 2012; 26: 164-169.
81. Mao S, Shuai X, Unger F, Wittmar M, Xie X, Kissel T. Synthesis, characterization and cytotoxicity of poly (ethylene glycol)-grafttrimethyl chitosan block copolymers. Biomaterials 2005; 26: 6343-6356.
82. Mao S, Sun W, Kissel T. Chitosan-based formulations for delivery of DNA and siRNA. Adv Drug Deliver Rev 2010; 62: 12-27.
83. Martin I, Wendt D, Heberer M. The role of bioreactors in tissue engineering. Trends Biotechnol 2004; 22: 80-86.
84. Mastiholimath V, Dandagi P, Jain SS, Gadad A, Kulkarni A. Time and pH dependent colon specific, pulsatile delivery of theophylline for nocturnal asthma. Int J Pharm 2007; 328: 49-56.
85. Matevosyan G, Yukha YS, Zavlin P. Phosphorylation of chitosan. Russ J Gen Chem 2003; 73: 1725-1728.
86. Mima S, Miya M, Iwamoto R, Yoshikawa S. Highly deacetylated chitosan and its properties. J Appl Polym Sci 1983; 28: 1909-1917.
87. Miyata T, Kodaira K, Higashijima H, Kimura T, Noishiki Y. Wound dressing, succinylchitosan, atelocollagen, Google Patents. 1992.
88. Moioli EK, Clark PA, Xin X, Lal S, Mao JJ. Matrices and scaffolds for drug delivery in dental, oral and craniofacial tissue engineering. Adv Drug Deliver Rev 2007; 59: 308-324.
89. Mourya V, Inamdar NN. Chitosan-modifications and applications: opportunities galore. React Funct Polym 2008; 68: 1013-1051.
90. Mukhopadhyay P, Sarkar K, Chakraborty M, Bhattacharya S, Mishra R, Kundu P. Oral insulin delivery by self-assembled chitosan nanoparticles: In vitro and in vivo studies in diabetic animal model. Mater Sci Eng C 2013; 33: 376-382.
91. Mukhopadhyay P, Sarkar K, Bhattacharya S, Bhattacharyya A, Mishra R, Kundu P. pH sensitive N-succinyl chitosan grafted polyacrylamide hydrogel for oral insulin delivery. Carbohyd Polym 2014; 112: 627-637.
92. Mumper R, Wang J, Claspell J, Rolland A. Novel polymeric condensing carriers for gene delivery. In: Proceedings of the international symposium on controlled release bioactive materials. 1995; 22: 178-179.
93. Mura C, Manconi M, Valenti D, Manca ML, Díez-Sales O, Loy G, Fadda AM. In vitro study of N-succinyl chitosan for targeted delivery of 5-aminosalicylic acid to colon. Carbohyd Polym 2011a; 85: 578-583.
94. Mura C, Nácher A, Merino V, Merino-Sanjuan M, Carda C, Ruiz A, Manconi M, Loy G, Fadda A, Diez-Sales O. N-Succinyl-chitosan systems for 5-aminosalicylic acid colon delivery: In vivo study with TNBS-induced colitis model in rats. Int J Pharm 2011b; 416: 145-154.
95. Mura C, Nácher A, Merino V, Merino-Sanjuan M, Manconi M, Loy G, Fadda A, Díez-Sales O. Design, characterization and in vitro evaluation of 5-aminosalicylic acid loaded N-succinyl-chitosan microparticles for colon specific delivery. Colloid Surface B 2012; 94: 199-205.
96. Murakami K, Aoki H, Nakamura S, Nakamura S-i, Takikawa M, Hanzawa M, Kishimoto S, Hattori H, Tanaka Y, Kiyosawa T. Hydrogel blends of chitin/chitosan, fucoidan and alginate as healing-impaired wound dressings. Biomaterials 2010; 31: 83-90.
97. Muzzarelli RA. Chitins and chitosans for the repair of wounded skin, nerve, cartilage and bone. Carbohyd Polym 2009; 76: 167-182.
98. Muzzarelli RA, Tanfani F, Emanuelli M, Mariotti S. N-(carboxymethylidene) chitosans and N-(carboxymethyl) chitosans: novel chelating polyampholytes obtained from chitosan glyoxylate. Carbohyd Res 1982; 107: 199-214.
99. Na L, Mao S, Wang J, Sun W. Comparison of different absorption enhancers on the intranasal absorption of isosorbide dinitrate in rats. Int J Pharm 2010; 397: 59-66.
100. Na SY, Oh SH, Song KS, Lee JH. Hyaluronic acid/mildly crosslinked alginate hydrogel as an injectable tissue adhesion barrier. J Mat Sci Mat M 2012; 23: 2303-2313.
101. Na L, Wang J, Wang L, Mao S. A novel permeation enhancer: N-succinyl chitosan on the intranasal absorption of isosorbide dinitrate in rats. Eur J Pharm Sci 2013; 48: 301-306.
102. Nagai T. In vivo drug release and antitumor characteristics of water-soluble conjugates of mitomycin C with glycol-chitosan and N-succinyl-chitosan. Biol Pharm Bull 1996; 19: 1170-1177.
103. Naruphontjirakul P, Viravaidya-Pasuwat K. Development of doxorubicin - Core shell o-succinyl chitosan graft pluronic ® 27 copolymer nanoparticles to treat human cancer. Int. J. Biosci. Biochem. Bioinforma 2011; 1: 131-136.
104. Nettles DL, Elder SH, Gilbert JA. Potential use of chitosan as a cell scaffold material for cartilage tissue engineering. Tissue Eng 2002; 8: 1009-1016.
105. Nieto J, Peniche-Covas C, Del Bosque J. Preparation and characterization of a chitosan-Fe (III) complex. Carbohyd Polym 1992; 18: 221-224.
106. Onishi H, Takahashi H, Yoshiyasu M, Machida Y. Preparation and in vitro properties of N-succinylchitosan-or carboxymethylchitinmitomycin C conjugate microparticles with specified size. Drug Dev Ind Pharm 2001; 27: 659-667.
107. Overstreet DJ, Dutta D, Stabenfeldt SE, Vernon BL. Injectable hydrogels. J Polym Sci Pol Phys 2012; 50: 881-903.
108. Parisi-Amon A, Mulyasasmita W, Chung C, Heilshorn SC. Proteinengineered injectable hydrogel to improve retention of transplanted adipose-derived stem cells. Adv Healthc Mater 2013; 2: 428-432.
109. Patil J, Kamalapur M, Marapur S, Kadam D. Ionotropic gelation and polyelectrolyte complexation: the novel techniques to design hydrogel particulate sustained, modulated drug delivery system: a review. Dig J Nanomater Bios 2010; 5: 241-248.
110. Philip AK, Dabas S, Pathak K. Optimized prodrug approach: A means for achieving enhanced anti-inflammatory potential in experimentally induced colitis. J Drug Target 2009; 17: 235-241.
111. Pijls RT, Sonderkamp T, Daube GW, Krebber R, Hanssen HH, Nuijts RM, Koole LH. Studies on a new device for drug delivery to the eye. Eur J Pharm Biopharm 2005; 59: 283-288.
112. Pillai O, Panchagnula R. Polymers in drug delivery. Curr Opin Chem Biol 2001; 5: 447-451.
113. Pillai C, Paul W, Sharma CP. Chitin and chitosan polymers: Chemistry, solubility and fiber formation. Prog Polym Sci 2009; 34: 641-678.
114. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147.
115. Polnok, A, Verhoef J, Borchard G, Sarisuta N, Junginger HE. In vitro evaluation of intestinal absorption of desmopressin using drug-delivery systems based on superporous hydrogels. Int J Pharm 2004; 269: 303-310.
116. Prashanth KH, Tharanathan R. Chitin/chitosan: modifications and their unlimited application potential - an overview. Trends Food Sci Tech 2007; 18: 117-131.
117. Ramesh HP, Tharanathan RN. Carbohydrates-the renewable raw materials of high biotechnological value. Cr Rev Biotechn 2003; 23: 149-173.
118. Ravaine V, Ancla C, Catargi B. Chemically controlled closed-loop insulin delivery. J Control Release 2008; 132: 2-11.
119. Reddy SM, Sinha VR, Reddy DS. Novel oral colon-specific drug delivery systems for pharmacotherapy of peptide and nonpeptide drugs. Drugs Today 1999; 35: 537-580.
120. Rekha M, Sharma CP. pH sensitive succinyl chitosan microparticles: a preliminary investigation towards oral insulin delivery. Trends Biomater Artif Organs 2008; 21: 107-115.
121. Rekha M, Sharma CP. Synthesis and evaluation of lauryl succinyl chitosan particles towards oral insulin delivery and absorption. J Control Release 2009; 135: 144-151.
122. Richardson S, Gorton L. Characterisation of the substituent distribution in starch and cellulose derivatives. Anal Chim Acta 2003; 497: 27-65.
123. Rinaudo M. Chitin and chitosan: properties and applications. Prog Polym Sci 2006; 31: 603-632.
124. Rinaudo M. Main properties and current applications of some polysaccharides as biomaterials. Polym Int 2008; 57: 397-430.
125. Riva R, Ragelle H, des Rieux A, Duhem N, Jérôme C, Préat V. Chitosan and chitosan derivatives in drug delivery and tissue engineering. Chitosan for Biomaterials II, Springer: 2011; 19-44.
126. Rogalsky AD, Kwon H, Lee-Sullivan P. Compressive stress-strain response of covalently crosslinked oxidized-alginate/ N-succinyl-chitosan hydrogels. J Biomed Mater Res A 2011; 99: 367-375.
127. Sashiwa H, Yamamori N, Ichinose Y, Sunamoto J, Aiba Si. Chemical Modification of Chitosan, 17. Macromol Biosci 2003; 3: 231-233.
128. Siddiqui I. A. In vitro differentiation of mesenchymal stem cells into endothelial cells. Der Pharmacia Sinica 2013; 4: 106-112.
129. Sinswat P, Tengamnuay P. Enhancing effect of chitosan on nasal absorption of salmon calcitonin in rats: comparison with hydroxypropyl-and dimethyl- β-cyclodextrins. Int J Pharm 2003; 257: 15-22.
130. Song Y, Onishi H, Nagai T. Synthesis and drug-release characteristics of the conjugates of mitomycin C with N-succinyl-chitosan and carboxymethyl-chitin. Chem Pharm Bull 1992; 40: 2822-2825.
131. Song Y, Onishi H, Nagai T. Pharmacokinetic characteristics and antitumor activity of the N-succinyl-chitosan-mitomycin C conjugate and the carboxymethyl-chitin-mitomycin C conjugate. Biol Pharm Bull 1993; 16: 48-54.
132. Straccia MC, Romano I, Oliva A, Santagata G, Laurienzo P. Crosslinker effects on functional properties of alginate/ N-succinylchitosan based hydrogels. Carbohyd Polym 2014; 108: 321-330.
133. Sui W, Wang Y, Dong S, Chen Y. Preparation and properties of an amphiphilic derivative of succinyl-chitosan. Colloids Surf A Physicochem Eng Asp 2008; 316: 171-175.
134. Sun S, Wang A. Adsorption properties of N-succinyl-chitosan and cross-linked N-succinyl-chitosan resin with Pb (II) as template ions. Sep Purif Technol 2006; 51: 409-415.
135. Sun T, Xie W, Xu P. Superoxide anion scavenging activity of graft chitosan derivatives. Carbohyd Polym 2004; 58: 379-382.
136. Sun L, Du Y, Fan L, Chen X, Yang J. Preparation, characterization and antimicrobial activity of quaternized carboxymethyl chitosan and application as pulp-cap. Polymer 2006; 47: 1796-1804.
137. Sun S, Wang Q, Wang A. Adsorption properties of Cu (II) ions onto N-succinyl-chitosan and crosslinked N-succinyl-chitosan template resin. Biochem Eng J 2007; 36: 131-138.
138. Sun T, Zhu Y, Xie J, Yin X. Antioxidant activity of N-acyl chitosan oligosaccharide with same substituting degree. Bioorg Med Chem Lett 2011; 21: 798-800.
139. Sun J, Xiao C, Tan H, Hu X. Covalently crosslinked hyaluronic acid-chitosan hydrogel containing dexamethasone as an injectable scaffold for soft tissue engineering. J Appl Polym Sci 2013; 129: 682-688.
140. Tabata Y. Significance of release technology in tissue engineering. Drug Discov Today 2005; 10: 1639-1646.
141. Tan H, Chu CR, Payne KA, Marra KG. Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering. Biomaterials 2009; 30: 2499-2506.
142. Tan H, Rubin JP, Marra KG. Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for adipose tissue regeneration. Organogenesis 2010; 6: 173-180.
143. Tan H, Luan H, Hu Y, Hu X. Covalently crosslinked chitosan-poly (ethylene glycol) hybrid hydrogels to deliver insulin for adipose-derived stem cells encapsulation. Macromol Res 2013; 21: 392-399.
144. Thanou M, Verhoef J, Marbach P, Junginger H. Intestinal absorption of octreotide: N-trimethyl chitosan chloride (TMC) ameliorates the permeability and absorption properties of the somatostatin analogue in vitro and in vivo. J Pharm Sci 2000; 89: 951-957.
145. Tharanathan R. Biodegradable films and composite coatings: past, present and future. Trends Food Sci Tech 2003; 14: 71-78.
146. Tharanathan RN, Kittur FS. Chitin - the undisputed biomolecule of great potential. Crit Rev Food Sci Nutr 2003; 43: 61-87.
147. Tibbitt MW, Anseth KS. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 2009; 103: 655-663.
148. Tiwari P, Panthari P, Katare DP, Kharkwal H. Natural polymers in drug delivery. Int J Pharm Pharm Sci 2014, 3: 1395-1409.
149. Toh EK-W, Chen H-Y, Lo Y-L, Huang S-J, Wang L-F. Succinated chitosan as a gene carrier for improved chitosan solubility and gene transfection. Nanomed Nanotechnol 2011; 7: 174-183.
150. Van der Merwe S, Verhoef J, Verheijden J, Kotze A, Junginger H. Trimethylated chitosan as polymeric absorption enhancer for improved peroral delivery of peptide drugs. Eur J Pharm Biopharm 2004; 58: 225-235.
151. Vanichvattanadecha C, Supaphol P, Nagasawa N, Tamada M, Tokura S, Furuike T, Tamura H, R. Rujiravanit Effect of gamma radiation on dilute aqueous solutions and thin films of N-succinyl chitosan. Polym Degrad Stabil 2010; 95: 234-244.
152. Vinsova J, Vavrikova E. Chitosan derivatives with antimicrobial, antitumour and antioxidant activities-a review. Curr Pharm Design 2011; 17: 3596-3607.
153. Wang X, Du Y, Liu H. Preparation, characterization and antimicrobial activity of chitosan-Zn complex. Carbohyd Polym 2004; 56: 21-26.
154. Wang Y, Tu S, Li R, Yang X, Liu L, Zhang Q. Cholesterol succinyl chitosan anchored liposomes: preparation, characterization, physical stability, and drug release behavior. Nanomed- Nanotechnol 2010; 6: 471-477.
155. Wang Y, Peng W, Liu X, Zhu M, Sun T, Peng Q, Zeng Y, Feng B, Zhi W, Weng J. Study of bilineage differentiation of human-bonemarrow- derived mesenchymal stem cells in oxidized sodium alginate/N-succinyl chitosan hydrogels and synergistic effects of RGD modification and low-intensity pulsed ultrasound. Acta biomaterialia 2014; 10: 2518-2528.
156. Wongpanit P, Sanchavanakit N, Pavasant P, Supaphol P, Tokura S, Rujiravanit R. Preparation and characterization of microwavetreated carboxymethyl chitin and carboxymethyl chitosan films for potential use in wound care application. Macromol Biosci 2005; 5: 1001-1012.
157. Wu Y, Seo T, Sasaki T, Irie S, Sakurai K. Layered structures of hydrophobically modified chitosan derivatives. Carbohyd Polym 2006; 63: 493-499.
158. Yamaguchi R, Arai Y, Kaneko T, Itoh T. Utilization of partially N-succinylated derivatives of chitosan and glycolchitosan as supports for the immobilization of enzymes. Biotechnol Bioeng 1982; 24: 1081-1091.
159. Yan C, Chen D, Gu J, Qin J. Nanoparticles of 5-fluorouracil (5-FU) loaded N-succinyl-chitosan (Suc-Chi) for cancer chemotherapy: preparation, characterization - in-vitro drug release and anti-tumour activity. J Pharm Pharmacol 2006a; 58: 1177-1181.
160. Yan C, Chen D, Gu J, Hu H, Zhao X, Qiao M. Preparation of N-succinylchitosan and their physical-chemical properties as a novel excipient. Yakuga Zasshi 2006b; 126: 789-793.
161. Yan C, Gu J, Guo Y, Chen D. In vivo biodistribution for tumor targeting of 5-fluorouracil (5-FU) loaded N-succinyl-chitosan (Suc-Chi) nanoparticles. Yakuga Zasshi 2010; 130: 801-804.
162. Yan C-y, Gu J-w, Hou D-p, Jing H-y, Wang J, Guo Y-z, Katsumi H, Sakane T, Yamamoto A. Synthesis of Tat tagged and folate modified N-succinyl-chitosan self-assembly nanoparticles as a novel gene vector. Int J Biol Macromol 2015; 72: 751-756.
163. Yen G-C, Chen H-Y. Antioxidant activity of various tea extracts in relation to their antimutagenicity. J Agr Food Chem 1995; 43: 27-32.
164. Yeom J, Bhang SH, Kim B-S, Seo MS, Hwang EJ, Cho IH, Park JK, Hahn SK. Effect of cross-linking reagents for hyaluronic acid hydrogel dermal fillers on tissue augmentation and regeneration. Bioconjugate Chem 2010; 21: 240-247.
165. Ying GQ, Yang H, Yi Y, Xu F. Relationships between the molecular structure and moisture-absorption and moisture-retention abilities of succinyl chitosan. Poly Bull 2007; 59: 509-516.
166. Zhang C-g, Zhu Q-l, Zhou Y, Liu Y, Chen W-l, Yuan Z-Q, Yang S-d, Zhou X-f, Zhu A-j, Zhang X-n. N-Succinyl-chitosan nanoparticles coupled with low-density lipoprotein for targeted osthole-loaded delivery to low-density lipoprotein receptor-rich tumors. Int J Nanomed 2014; 9: 2919-2932.
167. Zhao Y, Trewyn BG, Slowing II, Lin VS-Y. Mesoporous silica nanoparticle-based double drug delivery system for glucoseresponsive controlled release of insulin and cyclic AMP. J Am Chem Soci 2009; 131: 8398-8400.
168. Zhong Z, Xing R, Liu S, Wang L, Cai S, Li P. Synthesis of acyl thiourea derivatives of chitosan and their antimicrobial activities in vitro. Carbohyd Res 2008; 343: 566-570.
169. Zhou JQ, Wang JW. Immobilization of alliinase with a water soluble- insoluble reversible N-succinyl-chitosan for allicin production. Enzyme Microb Tech 2009; 45: 299-304.
170. Zhu A-p, Yuan L-h, Chen T, Wu H, Zhao F. Interactions between N-succinyl-chitosan and bovine serum albumin. Carbohyd Polym 2007; 69: 363-370.
171. Zhu A, Yuan L, Dai S. Preparation of well-dispersed superparamagnetic iron oxide nanoparticles in aqueous solution with biocompatible N-succinyl-O-carboxymethylchitosan. J Phys. Chem. C 2008; 112: 5432-5438.
172. Zhu X-J, Yuan W, Li P, Liu X, He J-Q. Pharmacokinetics of a novel nifedipine and pH-sensitive N-succinyl chitosan/alginate hydrogel bead in rabbits. Drug Dev Ind Pharm 2010; 36: 1463-1468.
173. Zhu Q-l, Zhou Y, Guan M, Zhou X-f, Liu Y, Chen W-l, Zhang C-g, Yuan Z-q, Liu C, Zhu A-j. Low-density lipoprotein-coupled N-succinyl chitosan nanoparticles co-delivering siRNA and doxorubicin for hepatocyte-targeted therapy. Biomaterials 2014; 35: 5965-5976.
174. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7: 211-228.