Quaternized chitosan as an antimicrobial agent: Antimicrobial activity, mechanism of action and biomedical applications in orthopedics

International Journal of Molecular Sciences

Volumn 14, Issue 1, 2013, Pages 1854-1869

  Tan, Honglue ^a,b   Ma, Rui ^a   Lin, Chucheng ^b   Liu, Ziwei ^b   Tang, Tingting ^a  

^a SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Antimicrobial activity; Application; Mechanism; Orthopedics; Quaternized CS

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; BONE CEMENT; CHITOSAN DERIVATIVE; GENTAMICIN; HYDROXYL GROUP; N (2 HYDROXYL 5 NITROPHENYL) N,N DIMETHYL CHITOSAN; N (2 HYDROXYLPHENYL) N,N DIMETHYL CHITOSAN; N (4 N,N DIMETHYLAMINOCINNAMYL)CHITOSAN; N (5 BROMIC 2 HYDROXYLPHENYL) N,N DIMETHYL CHITOSAN; N (5 CHLORO 2 HYDROXYLPHENYL) N,N DIMETHYL CHITOSAN; POLY(METHYL METHACRYLATE); POLYVINYL ALCOHOL; QUATERNARY AMMONIUM DERIVATIVE; QUATERNIZED CHITOSAN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CHITOSAN;

ANTIBACTERIAL ACTIVITY; ANTIFUNGAL ACTIVITY; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BIOCOMPATIBILITY; BIOFILM; BONE IMPLANT; DRUG SOLUBILITY; DRUG SYNTHESIS; ESCHERICHIA COLI; HUMAN; MEDICAL TECHNOLOGY; NONHUMAN; ORTHOPEDIC SURGERY; PH MEASUREMENT; REVIEW; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; TOXICITY TESTING; CHEMISTRY; ORTHOPEDICS;

ANTI-INFECTIVE AGENTS; CHITOSAN; HUMANS; ORTHOPEDICS; QUATERNARY AMMONIUM COMPOUNDS;

EID: 84877833588     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14011854     Document Type: Review

References (105)

1. Rabea, E.I.; Badawy, M.E.; Stevens, C.V.; Smagghe, G.; Steurbaut, W. Chitosan as antimicrobial agent: Applications and mode of action. Biomacromolecules 2003, 4, 1457-1465.
2. Jayakumar, R.; Prabaharan, M.; Nair, S.V.; Tamura, H. Novel chitin and chitosan nanofibers in biomedical applications. Biotechnol. Adv. 2010, 28, 142-150.
3. Ignatova, M.; Starbova, K.; Markova, N.; Manolova, N.; Rashkov, I. Electrospun nano-fibre mats with antibacterial properties from quaternized chitosan and poly (vinyl alcohol). Carbohydr. Res. 2006, 341, 2098-2107.
4. Ignatova, M.; Manolova, N.; Rashkov, I. Novel antibacterial fibers of quaternized chitosan and poly(vinyl pyrrolidone) prepared by electrospinning. Eur. Polymer. J. 2007, 43, 1112-1122.
5. Sajomsang, W.; Gonil, P.; Tantayanon, S. Antibacterial activity of quaternary ammonium chitosan containing mono or disaccharide moieties: Preparation and characterization. Int. J. Biol. Macromol. 2009, 44, 419-427.
6. Peng, Z.X.; Wang, L.; Du, L.; Guo, S.R.; Wang, X.Q.; Tang, T.T. Adjustment of the antibacterial activity and biocompatibility of hydroxypropyltrimethyl ammonium chloride chitosan by varying the degree of substitution of quaternary ammonium. Carbohydr. Polym. 2010, 81, 275-283.
7. Xu, T.; Xin, M.H.; Li, M.C.; Huang, H.L.; Zhou, S.Q.; Liu, J.Z. Synthesis, characterization and antibacterial activity of N, O-quaternary ammonium chitosan. Carbohydr. Res. 2011, 346, 2445-2450.
8. Rúnarsson, Ö.V.; Holappa, J.; Nevalainen, T.; Hjálmarsdóttir, M.; Järvinen, T.; Loftsson, T.; Einarsson, J.M.; Jónsdóttir, S.; Valdimarsdóttir, M.; Másson, M. Antibacterial activity of methylated chitosan and chitooligomer derivatives: Synthesis and structure activity relationships. Eur. Polymer. J. 2007, 43, 2660-2671.
9. Ye, X.L.; Li, X.G.; Yuan, L.J.; Ge, L.H.; Zhang, B.S.; Zhou, S.B. Interaction between houttuyfonate homologues with the cell membrane of gram-positive and gram-negative bacteria. Colloid Surf. A Physicochem. Eng. Asp. 2007, 301, 412-418.
10. Snyman, D.; Govender, T.; Kotzé, A.F. Low molecular weight quaternised chitosan (I): Synthesis and characterisation. Pharmazie 2003, 58, 705-708.
11. Sajomsang, W. Synthetic methods and applications of chitosan containing pyridylmethyl moiety and its quaternized derivatives: A review. Carbohydr. Polym. 2010, 80, 631-647.
12. Mourya, V.K.; Inamdar, N.N. Trimethyl chitosan and its applications in drug delivery. J. Mater. Sci. Mater. Med. 2009, 20, 1057-1079.
13. Sajomsang, W.; Tantayanon, S.; Tangpasuthadol, V.; Daly, W.H. Quaternization of N-aryl chitosan derivatives: synthesis, characterization and antibacterial activity. Carbohydr. Res. 2009, 344, 2502-2511.
14. Sajomsang, W.; Tantayanon, S.; Tangpasuthadol, V.; Daly, W.H. Synthesis of methylated chitosan containing aromatic moieties: Chemoselectivity and effect on molecular weight. Carbohydr. Polym. 2008, 72, 740-750.
15. Masson, M.; Holappa, J.; Hjalmarsdottir, M.; Runarsson, O.V.; Nevalainen, T.; Jarvinen, T. Antimicrobial activity of piperazine derivatives of chitosan. Carbohydr. Polym. 2008, 74, 566-571.
16. Wiarachai, O.; Thongchul, N.; Kiatkamjornwongd, S.; Hovene, V.P. Surface-quaternized chitosan particles as an alternative and effective organic antibacterial material. Colloids Surf. B Biointerfaces 2012, 92, 121-129.
17. Kong, M.; Chen, X.G.; Xing, K.; Park, H.J. Antimicrobial properties of chitosan and mode of action: A state of the art review. Int. J. Food Microbiol. 2010, 144, 51-63.
18. Avadi, M.R.; Sadeghi, A.M.M.; Tahzibi, A.; Bayati, K.; Pouladzadeh, M.; Zohuriaan-Mehr, M.J.; Rafiee-Tehrani, M. Diethylmethyl chitosan as an antimicrobial agent: Synthesis, characterization and antibacterial effects. Eur. Polymer J. 2004, 40, 1355-1361.
19. Seong, H.S.; Whang, H.S.; Ko, S.W. Synthesis of a quaternary ammonium derivative of chito-oligosaccharide as antimicrobial agent for cellulosic fibers. J. Appl. Polym. Sci. 2000, 76, 2009-2015.
20. Kim, Y.H.; Nam, C.W.; Choi, J.W.; Jang, J. Durable antimicrobial treatment of cotton fabrics using N-(2-hydroxy)propyl-3-trimethylammonium chitosan chloride and polycarboxylic acids. Appl. Polym. Sci. 2003, 88, 1567-1572.
21. Chi, W.L.; Qin, C.Q.; Zeng, L.T.; Li, W.; Wang, W.J. Microbiocidal activity of chitosan-N-2-hydroxypropyl trimethyl ammonium chloride. Appl. Polym. Sci. 2007, 103, 3851-3856.
22. Qin, C.Q.; Xiao, Q.; Li, H.R.; Fang, M.; Liu, Y.; Chen, X.Y.; Li, Q. Calorimetric studies of the action of chitosan-N-2-hydroxypropyl trimethyl ammonium chloride on the growth of microorganisms. Int. J. Biol. Macromol. 2004, 34, 121-126.
23. Xu, T.; Xin, M.; Li, M.; Huang, H.; Zhou, S. Synthesis, characteristic and antibacterial activity of N, N, N-trimethyl chitosan and its carboxymethyl derivatives. Carbohydr. Polym. 2010, 81, 931-936.
24. Raafat, D.; Sahl, H.G. Chitosan and its antimicrobial potential-a critical literature survey. Microb. Biotechnol. 2009, 2, 186-201.
25. Kenawy, El-R.; Abdel-Hay, F.I.; El-Magd, A.A.; Mahmoud, Y. Biologically active polymers: Modification and anti-microbial activity of chitosan derivatives. J. Bioact. Compat. Polym. 2005, 20, 95-111.
26. Park, Y.Y.; Kim, M.H.; Park, S.C.; Cheong, H.S.; Jang, M.K.; Nah, J.W.; Hahm, K.S. Investigation of the antifungal activity and mechanism of action of LMWS-chitosan. J. Microbiol. Biotechnol. 2008, 18, 1729-1734.
27. El Ghaouth, A.; Arul, J.; Asselin, A.; Benhamou, N. Antifungal activity of chitosan on post-harvest pathogens: Induction of morphological and cytological alterations in Rhizopus. stolonifer. Mycol. Res. 1992, 96, 769-779.
28. Bautista-Baños, S.; Hernández-Lauzardo, A.N.; Velázquez-del Valle, M.G.; Hernández-López, M.; Ait Barka, E.; Bospuez-Molina, E.; Wilson, C.L. Chitosan as a potential natural compound to control pre and post harvest diseases of horticultural commodities. Crop. Prot. 2006, 25, 108-118.
29. Bautista-Baños, S.; Hernández-López, M.; Bospuez-Molina, E.; Wilson, C.L. Effects of chitosan and plant extracts on growth of Colletotrichum gloeosporioides, anthracnose levels and quality of papaya fruit. Crop. Prot. 2003, 22, 1087-1092.
30. Bautista-Baños, S.; Hernández-López, M.; Bospuez-Molina, E. Growth inhibition of selected fungi by chitosan and plant extracts. Mex. J. Phytopathol. 2004, 22, 178-186.
31. Tayel, A.A.; Moussa, S.; El-Tras, W.F.; Knittel, D.; Opwis, K.; Scholl-meyer, E. Anticandidal action of fungal chitosan against Candida albicans. Int. J. Biol. Macromol. 2010, 47, 454-457.
32. Guo, Z.Y.; Xing, R.G.; Liu, S.; Zhong, Z.M.; Ji, X.; Wang, L.; Li, P.C. The influence of the cationic of quaternized chitosan on antifungal activity. Int. J. Food Microbiol. 2007, 118, 214-217.
33. Guo, Z.Y.; Xing, R.E.; Liu, S.; Zhong, Z.M.; Ji, X.; Wang, L.; Li, P.C. The influence of molecular weight of quaternized chitosan on antifungal activity. Carbohydr. Polym. 2008, 71, 694-697.
34. De Oliveira Pedro, R.; Takaki, M.; Gorayeb, T.C.; Bianchi, V.L.; Thomeo, J.C.; Tiera, M.J.; de Oliveira Tiera, V.A. Synthesis, characterization and antifungal activity of quaternary derivatives of chitosan on Aspergillus flavus. Microbiol. Res. 2013, 168, 50-55.
35. Sajomsang, W.; Gonil, P.; Saesoo, S.; Ovatlarnporn, C. Antifungal property of quaternized chitosan and its derivatives. Int. J. Biol. Macromol. 2012, 50, 263-269.
36. Xie, Y.J.; Liu, X.F.; Chen, Q. Synthesis and characterization of water-soluble chitosan derivate and its antibacterial activity. Carbohydr. Polym. 2007, 69, 142-147.
37. Kim, C.H.; Choi, J.W.; Chun, H.J.; Choi, K.S. Synthesis of chitosan derivatives with quaternary ammonium salt and their antibacterial activity. Polym. Bull. 1997, 38, 387-393.
38. Leuba, S.; Stossel, P. Chitin in Nature and Technology; Plenum Press: New York, NY, USA, 1985.
39. Eaton, P.; Fernandes, J.C.; Pereira, E.; Pintado, M.E.; Malcata, F.X. Atomic force microscopy study of the antibacterial effects of chitosans on Escherichia coli and Staphylococcus aureus. Ultramicroscopy 2008, 108, 1128-1134.
40. Jarmila, V.; Vavríková, E. Chitosan derivatives with antimicrobial, antitumour and antioxidant activities-a review. Curr. Pharm. Des. 2011, 17, 3596-3607.
41. Kenawy, El-R.; Abdel-Hay, F.I.; El-Raheem, A.; El-Shanshoury, R.; El-Newehy, M.H. Biologically active polymers: synthesis and antimicrobial activity of modified glycidyl methacrylate polymers having a quaternary ammonium and phosphonium groups. J. Control. Release 1998, 50, 145-152.
42. Helander, I.M.; Wright, A.V.; Mattila-Sandholm, T.M. Potential of lactic acid bacteria and novel antimicrobials against Gram-negative bacteria. Trends Food Sci. Technol. 1997, 8, 146-150.
43. Kong, M.; Chen, X.G.; Liu, C.S.; Liu, C.G.; Meng, X.H.; Yu, L.J. Antibacterial mechanism of chitosan microspheres in a solid dispersing system against E. coli. Colloids Surf. B Biointerfaces 2008, 65, 197-202.
44. Helander, I.M.; Nurmiaho-Lassila, E.L.; Ahvenainen, R.; Rhoades, J.; Roller, S. Chitosan disrupts the barrier properties of the outer membrane of Gram-negative bacteria. Int. J. Food Microbiol. 2001, 71, 235-244.
45. Chung, Y.C.; Su, Y.P.; Chen, C.C.; Jia, G.; Wang, H.L.; Wu, J.C.G.; Lin, J.G. Relationship between antibacterial activity of chitosans and surface characteristics of cell wall. Acta Pharmacol. Sin. 2004, 25, 932-936.
46. Raafat, D.; Bargen, K.V.; Haas, A.; Sahl, H.G. Insights into the mode of action of chitosan as an antibacterial compound. Appl. Environ. Microbiol. 2008, 74, 3764-3773.
47. Xing, K.; Chen, X.G.; Liu, C.S.; Cha, D.S.; Park, H.J. Oleoyl-chitosan nanoparticles inhibits Escherichia coli and Staphylococcus aureus by damaging the cell membrane and putative binding to extracellular or intracellular targets. Int. J. Food Microbiol. 2009, 132, 127-133.
48. Xing, K.; Chen, X.G.; Kong, M.; Liu, C.S.; Cha, D.S.; Park, H.J. Effect of oleoyl-chitosan nanoparticles as a novel antibacterial dispersion system on viability, membrane permeability and cell morphology of Escherichia coli and Staphylococcus aureus. Carbohydr. Polym. 2009, 76, 17-22.
49. Muzzarelli, R.A.A.; Muzzarelli, C.; Tarsi, R.; Miliani, M.; Gabbanelli, F.; Cartolari, M. Fungistatic activity of modified chitosans against Saprolegnia. parasitica. Biomacromolecules 2001, 2, 165-169.
50. Roller, S.; Covill, N. The antifungal properties of chitosan in laboratory media and apple juice. Int. J. Food Microbiol. 1999, 47, 67-77.
51. Kuhn, D.M.; Ghannoum, M.A. Candida biofilms: Antifungal resistance and emerging therapeutic options. Curr. Opin. Investig. Drugs 2004, 5, 186-197.
52. Savard, T.; Beaulieu, C.; Boucher, I.; Champagne, C.P. Antimicrobial action of hydrolyzed chitosan against spoilage yeasts and lactic acid bacteria of fermented vegetables. J. Food Prot. 2002, 65,828-833.
53. Martinez, L.R.; Mihu, M.R.; Tar, M.; Cordero, R.J.; Han, G.; Friedman, A.J.; Friedman, J.M.; Nosanchuk, J.D. Demonstration of antibiofilm and antifungal efficacy of chitosan against candidal biofilms, using an in vivo central venous catheter model. J. Infect. Dis. 2010, 201, 1436-1440.
54. Li, M.Q.; Chen, X.G.; Liu, J.M.; Zhang, W.F.; Tang, X.X. Molecular weight-dependent antifungal activity and action mode of chitosan against Fulvia fulva (Cooke) Ciffrri. J. Appl. Polym. Sci. 2011, 119, 3127-3135.
55. Trampuz, A.; Osmon, D.R.; Hanssen, A.D.; Steckelberg, J.M.; Patel, R. Molecular and antibiofilm approaches to prosthetic joint infection. Clin. Orthop. Relat. Res. 2003, 414, 69-88.
56. Gu, J.; Li, H.; Li, M.; Vuong, C.; Otto, M.; Wen, Y.; Gao, Q. Bacterial insertion sequence IS256 as a potential molec-ular marker to discriminate invasive strains from commensal strains of Staphylococcus epidermidis. J. Hosp. Infect. 2005, 61, 342-348.
57. Hoyle, B.D.; Costerton, J.W. Bacterial resistance to antibiotics: the role of biofilm. Prog. Drug Res. 1991, 37, 91-105.
58. Montanaro, L.; Campoccia, D.; Arciola, C.R. Advancements in molecular epidemiology of implant infections and future perspectives. Biomaterials 2007, 28, 5155-5168.
59. Patel, R. Biofilm and antimicrobial resistance. Clin. Orthop. Relat. Res. 2005, 437, 41-47.
60. Mack, D.; Siemssen, N.; Laufs, R. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: Evidence for functional relation to intercellular adhesion. Infect. Immun. 1992, 60, 2048-2057.
61. Koskela, A.; Nilsdotter-Augustinsson, A.; Persson, L.; Söderquist, B. Prevalence of the ica operon and insertion sequence IS256 among Staphylococcus epidermidis prosthetic joint infection isolates. Eur. J. Clin. Microbiol. Infect. Dis. 2009, 28, 655-660.
62. Rohde, H.; Kalitzky, M.; Kröger, N.; Scherpe, S.; Horstkotte, M.A.; Knobloch, J.K.M.; Zander, A.R.; Mack, D. Detection of virulence-associated genes not useful for discriminating between invasive and commensal Staphylococcus epidermidis strains from a bone marrow transplant unit. J. Clin. Microbiol. 2004, 42, 5614-5619.
63. Arciola, C.R.; Campoccia, D.; Gamberini, S.; Rizzi, S.; Donati, M.E.; Baldassarri, L.; Montanaro, L. Search for the insertion element IS256 within the ica locus of Staphylococcus epidermidis clinical isolates collected from biomaterial-associated infections. Biomaterials 2004, 25, 4117-4125.
64. Gerke, C.; Kraft, A.; Süssmuth, R.; Schweitzer, O.; Götz, F. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J. Biol. Chem. 1998, 273, 18586-18593.
65. Heilmann, C.; Schweitzer, O.; Gerke, C.; Vanittanakom, N.; Mack, D.; Götz, F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 1996, 20, 1083-1091.
66. Tan, H.L.; Peng, Z.X.; Li, Q.T.; Xu, X.F.; Guo, S.R.; Tang, T.T. The use of quaternised chitosan-loaded PMMA to inhibit biofilm for-mation and downregulate the virulence-associated gene expression of antibiotic-resistant staphylococcus. Biomaterials 2012, 33, 365-377.
67. Peng, Z.X.; Tu, B.; Shen, Y; Du, L.; Wang, L.; Guo, S.R.; Tang, T.T. Quaternized chitosan inhibits icaA transcription and biofilm formation by Staphylococcus on a titanium surface. Antimicrob. Agents Chemother. 2011, 55, 860-866.
68. Hendriks, J.G.; van Horn, J.R.; van der Mei, H.C.; Busscher, H.J. Backgrounds of antibiotic-loaded bone cement and prosthesis-related infection. Biomaterials 2004, 25, 545-556.
69. Leprêtre, S.; Chai, F.; Hornez, J.C.; Vermet, G.; Neut, C.; Descamps, M.; Hildebrand, H.F.; Martel, B. Prolonged local antibiotics delivery from hydroxyapatite functionalised with cyclodextrin polymers. Biomaterials 2009, 30, 6086-6093.
70. Campoccia, D.; Montanaro, L.; Speziale, P.; Arciola, C.R. Antibiotic-loaded biomaterials and the risks for the spread of antibiotic resistance following their prophylactic and therapeutic clinical use. Biomaterials 2010, 31, 6363-6377.
71. Wahlig, H.; Dingeldein, E.; Buchholz, H.W.; Buchholz, M.; Bachmann, F. Pharmacokinetic study of gentamicin-loaded cement in total hip replacements: comparative effects of varying dosage. J. Bone Joint Surg. Br. 1984, 66, 175-179.
72. Nijhof, M.W.; Dhert, W.J.; Tilman, P.B.; Verbout, A.J.; Fleer, A. Release of tobramycin from tobramycin-containing bone cement in bone and serum of rabbits. J. Mater. Sci. Mater. Med. 1997, 8, 799-802.
73. Van de Belt, H.; Neut, D.; Schenk, W.; van Horn, J.R.; van der Mei, H.C.; Busscher, H.J. Infection of orthopedic implants and the use of antibiotic-loaded bone cements: A review. Acta. Orthop. Scand. 2001, 72, 557-571.
74. Bourne, R.B. Prophylactic use of antibiotic bone cement: An emerging standard-in the affirmative. J. Arthroplasty 2004, 19, 69-72.
75. Shi, Z.L.; Neoh, K.G.; Kang, E.T.; Poh, C.; Wang, W. Titanium with surface-grafted dextran and immobilized bone morphogenetic protein-2 for inhibition of bacterial adhesion and enhancement of osteoblast functions. Tissue Eng. Part. A 2009, 15, 417-426.
76. Montanaro, L.; Campoccia, D.; Arciol, C.R. Nanostructured materials for inhibition of bacterial adhesion in orthopedic implants: a minireview. Int. J. Artif. Organs 2008, 31, 771-776.
77. Shi, Z.L.; Chua, P.H.; Neoh, K.G.; Kang, E.T.; Wang, W. Bioactive titanium implant surfaces with bacterial inhibition and osteoblast function enhancement properties. Int. J. Artif. Organs 2008, 31, 777-785.
78. Chang, Y.H.; Goldberg, V.M.; Arnold, I.; Caplan, A.I. Toxic effects of gentamicin on marrow-derived human mesenchymal stem cells. Clin. Orthop. Relat. Res. 2006, 452, 242-249.
79. Ince, A.; Schütze, N.; Karl, N.; Löhr, J.F.; Eulert, J. Gentamicin negatively influenced osteogenic function in vitro. Int. Orthop. 2007, 31, 223-228.
80. Isefuku, S.; Joyner, C.J.; Simpson, A.H. Gentamicin may have an adverse effect on osteogenesis. J. Orthop. Trauma 2003, 17, 212-216.
81. Rathbone, C.R.; Cross, J.D.; Brown, K.V.; Murray, C.K.; Wenke, J.C. Effect of various concentrations of antibiotics on osteogenic cell viability and activity. J. Orthop. Res. 2011, 29, 1070-1074.
82. Duewelhenke, N.; Krut, O.; Eysel, P. Influence on mitochondria and cytotoxicity of different antibiotics administered in high concentrations on primary human osteoblasts and cell lines. Antimicrob. Agents Chemother. 2007, 51, 54-63.
83. Ince, A.; Schütze, N.; Hendrich, C.; Jakob, F.; Eulert, J.; Löhr, J.F. Effect of polyhexanide and gentamicin on human osteoblasts and endothelial cells. Swiss Med. Wkly. 2007, 137, 139-145.
84. Parker, R.A.; Clegg, P.D.; Taylor, S.E. The in vitro effects of antibiotics on cell viability and gene expression of equine bone marrow-derived mesenchymal stromal cells. Equine Vet. J. 2012, 44, 355-360.
85. Pountos, I.; Georgouli, T.; Bird, H.; Kontakis, G.; Giannoudis, P.V. The effect of antibiotics on bone healing: current evidence. Expert Opin. Drug Saf. 2011, 10, 935-945.
86. Tan, H.L.; Guo, S.R.; Yang, S.B.; XU, X.F.; Tang, T.T. Physical characterization and osteogenic activity of the quaternized chitosan-loaded PMMA bone cement. Acta Biomater. 2012, 8, 2166-2174.
87. Shi, Z.L.; Neoha, K.G.; Kanga, E.T.; Wang, W. Antibacterial and mechanical properties of bone cement impregnated with chitosan nanoparticles. Biomaterials 2006, 27, 2440-2449.
88. Okazaki, Y.; Gotoh, E.; Nishimori, M.; Katsuda, S.; Manabe, T.; Kobayashi, K. Osteocompatibility of stainless steel, Co-Cr-Mo, Ti-6Al-4V and Ti-15Zr-4Nb-4Ta alloy implants in rat bone tissue. Mater. Trans. 2005, 46, 1610-1617.
89. Geetha, M.; Singh, A.K.; Asokamani, R.; Gogia, A.K. Ti based biomaterials, the ultimate choice for orthopaedic implants-a review. Prog. Mater. Sci. 2009, 54, 397-425.
90. Weinlaender, M.; Kenney, E.B.; Lekovic, V.; Beumer, J.; Moy, P.K.; Lewis, S. Histomorphometry of bone apposition around three types of endosseous dental implants. Int. J. Oral Maxilofac. Implant. 1992, 7, 491-496.
91. Campoccia, D.; Montanaro, L.; Arciola, C.R. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 2006, 27, 2331-2339.
92. Widmer, A.F. New developments in diagnosis and treatment of infection in orthopedic implants. Clin. Infect. Dis. 2001, 33, 94-106.
93. Zhao, L.; Chu, P.K.; Zhang, Y.; Wu, Z. Antibacterial coatings on titanium implants. J. Biomed. Mater. Res. B Appl. Biomater. 2009, 91, 470-480.
94. Vasilev, K.; Sah, V.; Anselme, K.; Ndi, C.; Mateescu, M.; Dollmann, B.; Martinek, P.; Ys, H.; Ploux, L.; Griesser, H.J. Tunable antibacterial coatings that support mammalian cell growth. Nano Lett. 2010, 10, 202-207.
95. Subbiahdoss, G.; Grijpma, D.W.; van der Mei, H.C.; Busscher, H.J.; Kuijer, R. Microbial biofilm growth versus tissue integration on biomaterials with different wettabilities and a polymer-brush coating. J. Biomed. Mater. Res. A 2010, 94, 533-538.
96. Harris, L.G.; Tosatti, S.; Wieland, M.; Textor, M.; Richards, R.G. Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(L-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials 2004, 25, 4135-4148.
97. Della Valle, C.; Visai, L.; Santin, M.; Cigada, A.; Candiani, G.; Pezzoli, D.; Arciola. C.R.; Imbriani, M.; Chiesa, R. A novel antibacterial modification treatment of titanium capable to improve osseointegration. Int. J. Artif. Organ. 2012, 35, 864-875.
98. Hu, X.F.; Neoh, K. G; Shi, Z.L.; Kang, E.T.; Poh, C.; Wang, W. An in vitro assessment of titanium functionalized with polysaccharides conjugated with vascular endothelial growth factor for enhanced osseointegration and inhibition of bacterial adhesion. Biomaterials 2010, 31, 8854-8863.
99. Chen, K.S.; Ku, Y.A.; Lee, C.H.; Lin, H.R.; Lin, F.H.; Chen, T.M. Immobilization of chitosan gel with cross-linking reagent on PNIPAAm/gel/PP non-woven composite surface. Mat. Sci. Eng. C 2005, 25, 472-478.
100. Chen, S.P.; Wu, G.Z.; Zeng, H.Y. Preparation of high antimicrobial activity thiourea chitosan-Ag+ complex. Carbohydr. Polym. 2005, 60, 33-38.
101. Chen, S.P.; Wu, G.Z.; Long, D.W.; Liu, Y.D. Preparation, characterization and antibacterial activity of chitosan-Ca3V10O28 complex membrane. Carbohydr. Polym. 2006, 64, 92-97.
102. Fan, L.H.; Du, Y.M.; Zhang, B.Z.; Yang, J.H.; Zhou, J.P.; Kennedy, J.F. Preparation and properties of alginate/carboxymethyl chitosan blend fibers. Carbohydr. Polym. 2006, 65, 447-452.
103. Wu, Y.B.; Yu, S.H.; Mi, F.L.; Wu, C.W.; Shyu, S.S.; Peng, C.K.; Chao, A.C. Preparation and characterization on mechanical and antibacterial properties of chitosan cellulose blends. Carbohydr. Polym. 2004, 57, 435-440.
104. Deitzel, J.M.; Kleinmeyer, J.; Harris, D.; Beck, T.N.C. The effect of processing variables on the morphology of electrospun nanofibers and textiles. Polymer 2001, 42, 261-272.
105. Alipour, S.M.; Nouri, M.; Mokhtari, J.; Bahrami, S.H. Electrospinning of poly(vinyl alcohol)-water-soluble quaternized chitosan derivative blend. Carbohydr. Res. 2009, 344, 2496-2501.