Advertisement

Polymer Bulletin

, Volume 75, Issue 3, pp 985–1000 | Cite as

A novel and homogeneous scaffold material: preparation and evaluation of alginate/bacterial cellulose nanocrystals/collagen composite hydrogel for tissue engineering

  • Huiqiong Yan
  • Denggao Huang
  • Xiuqiong Chen
  • Haifang Liu
  • Yuhong Feng
  • Zhendong Zhao
  • Zihao Dai
  • Xueqin Zhang
  • Qiang Lin
Original Paper

Abstract

Alginate is a well-known biomaterial which has been widely used in tissue engineering due to its excellent property. However, there are still several drawbacks, such as weak mechanical strength, the lack of cell recognition sites for cell adhesion, extensive swelling and uncontrolled degradation that limit its practical application. Therefore, the internal gelation using CaCO3–GDL complex and the incorporation of bacterial cellulose nanocrystals (BCNs) and type I collagen (COL) as the reinforcing component into alginate matrix were proposed to prepare the novel and homogeneous alginate/bacterial cellulose nanocrystals/collagen composite scaffold (ALG/BCNs/COL). The morphology, porosity, mechanical property, swelling and degradation behavior, and cytotoxicity of the resultant scaffold were investigated. The experimental results showed that ALG/BCNs/COL revealed good three-dimensional (3D) architecture as well as lamellar and porous morphologies. The incorporation of BCNs into alginate matrix obviously decreased the pore size and maintained the porosity of ALG/BCNs/COL, which was in favour of mechanical integrity. FT-IR spectra and XRD analysis revealed that the components of ALG/BCNs/COL, such as SA, BCNs and COL were combined together by intermolecular hydrogen bonds, which could effectively inhibit large swelling and retard the biodegradation of the composite scaffold. Finally, cell studies results indicated that both MC3T3-E1 and h-AMS cells were viable and proliferate well on the composite scaffold.

Keywords

Alginate Bacterial cellulose nanocrystals Collagen Internal gelation Composite scaffold Tissue engineering 

Notes

Acknowledgements

This work was financially supported by National Natural Science Foundation of China (21366010 and 21566009), the Natural Science Foundation of Hainan Province (213010, 20152020, 20162013 and 20162016) and Key Projects in the Hainan provincial Science and Technology Program (cxy20150026).

References

  1. 1.
    Vallée F, Müller C, Durand A, Schimchowitsch S, Dellacherie E, Kelche C, Cassel JC, Leonard M (2009) Synthesis and rheological properties of hydrogels based on amphiphilic alginate-amide derivatives. Carbohyd Res 344:223–228CrossRefGoogle Scholar
  2. 2.
    Bu H, Kjøniksen AL, Elgsaeter A, Nyström B (2006) Interaction of unmodified and hydrophobically modified alginate with sodium dodecyl sulfate in dilute aqueous solution calorimetric, rheological, and turbidity studies. Colloid Surface A 278:166–174CrossRefGoogle Scholar
  3. 3.
    Pawar SN, Edgar KJ (2012) Alginate derivatization: a review of chemistry, properties and applications. Biomaterials 33:3279–3305CrossRefGoogle Scholar
  4. 4.
    Ghadban A, Albertin L, Rinaudo M, Heyraud A (2012) Biohybrid glycopolymer capable of ionotropic gelation. Biomacromolecules 13:3108–3119CrossRefGoogle Scholar
  5. 5.
    Yan H, Chen X, Li J, Feng Y, Shi Z, Wang X, Lin Q (2016) Synthesis of alginate derivative via the Ugi reaction and itscharacterization. Carbohyd Polym 136:757–763CrossRefGoogle Scholar
  6. 6.
    d’Ayala GG, Malinconico M, Laurienzo P (2008) Marine derived polysaccharides for biomedical applications: chemical modification approaches. Molecules 13:2069–2106CrossRefGoogle Scholar
  7. 7.
    Bidarra SJ, Barrias CC, Granja PL (2014) Injectable alginate hydrogels for cell delivery in tissue engineering. Acta Biomater 10:1646–1662CrossRefGoogle Scholar
  8. 8.
    Ionita M, Pandele MA, Iovu H (2013) Sodium alginate/graphene oxide composite films with enhanced thermal and mechanical properties. Carbohyd Polym 94:339–344CrossRefGoogle Scholar
  9. 9.
    Lee KY, Mooney DJ (2001) Hydrogels for tissue engineering. Chem Rev 101(7):1869–1879CrossRefGoogle Scholar
  10. 10.
    Li Q, Liu CG, Huang ZH, Xue FF (2011) Preparation and characterization of nanoparticles based on hydrophobic alginate derivative as carriers for sustained release of vitamin D3. J Agric Food Chem 59:1962–1967CrossRefGoogle Scholar
  11. 11.
    Shah N, Ul-Islam M, Khattak WA, Park JK (2013) Overview of bacterial cellulose composites: a multipurpose advanced material. Carbohyd Polym 98:1585–1598CrossRefGoogle Scholar
  12. 12.
    Bodhibukkana C, Srichana T, Kaewnopparat S, Tangthong N, Bouking P, Martin GP, Suedee R (2006) Composite membrane of bacterially-derived cellulose and molecularly imprinted polymer for use as a transdermal enantioselective controlled-release system of racemic propranolol. J Control Release 113:43–56CrossRefGoogle Scholar
  13. 13.
    Prang P, Muller R, Eljaouhari A, Heckmann K, Kunz W, Weber T, Faber C, Vroemen M, Bogdahn U, Weidner N (2006) The promotion of oriented axonal regrowth in the injured spinal cord by alginate based anisotropic capillary hydrogels. Biomaterials 27:3560–3569Google Scholar
  14. 14.
    Dhoot NO, Tobias CA, Fischer I, Wheatley MA (2004) Peptide-modified alginate surfaces as a growth permissive substrate for neurite outgrowth. J Biomed Mater Res A 71A:191–200CrossRefGoogle Scholar
  15. 15.
    Mosahebi A, Wiberg M, Terenghi G (2003) Addition of fibronectin to alginate matrix improves peripheral nerve regeneration in tissue-engineered conduits. Tissue Eng 9:209–218CrossRefGoogle Scholar
  16. 16.
    Hersel U, Dahmen C, Kessler H (2003) RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24:4385–4415CrossRefGoogle Scholar
  17. 17.
    Lin N, Dufresne A (2014) Nanocellulose in biomedicine: current status and future prospect. Eur Polym J 59:302–325CrossRefGoogle Scholar
  18. 18.
    Dugan JM, Gough JE, Eichhorn SJ (2013) Bacterial cellulose scaffolds and cellulose nanowhiskers for tissue engineering. Nanomedicine 8(2):287–298CrossRefGoogle Scholar
  19. 19.
    Domingues RMA, Gomes ME, Rui L, Reis RL (2014) The potential of cellulose nanocrystals in tissue engineering strategies. Biomacromolecules 15:2327–2346CrossRefGoogle Scholar
  20. 20.
    Shelke NB, James R, Laurencin CT, Kumbar SG (2014) Polysaccharidebiomaterials for drug delivery and regenerative engineering. Polym Advan Technol 25(5):448–460CrossRefGoogle Scholar
  21. 21.
    Ullah H, Wahid F, Santos HA, Khan T (2016) Advances in biomedical and pharmaceutical applications of functional bacterial cellulose-based nanocomposites. Carbohyd Polym 150:330–352CrossRefGoogle Scholar
  22. 22.
    Zhou C, Shi Q, Guo W, Terrell L, Qureshi AT, Hayes DJ, Wu Q (2013) Electrospun bio-nanocomposite scaffolds for bone tissue engineering by cellulose nanocrystals reinforcing maleic anhydride grafted PLA. ACS Appl Mater Interfaces 5:3847–3854CrossRefGoogle Scholar
  23. 23.
    Liu J, Cheng F, Grénman H, Spoljaric S, Seppälä J, Eriksson JE, Willför S, Xu C (2016) Development of nanocellulose scaffolds with tunable structures to support 3D cell culture. Carbohyd Polym 148:259–271CrossRefGoogle Scholar
  24. 24.
    Kuo CK, Ma PX (2001) Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: Part 1. Structure, gelation rate and mechanical properties. Biomaterials 22:511–521CrossRefGoogle Scholar
  25. 25.
    Lawrie G, Keen I, Drew B, Chandler-Temple A, Rintoul L, Fredericks P, Grøndahl L (2007) Interactions between alginate and chitosan biopolymers characterized using FTIR and XPS. Biomacromolecules 8:2533–2541CrossRefGoogle Scholar
  26. 26.
    Paximada P, Tsouko E, Kopsahelis N, Koutinas AA, Mandala I (2016) Bacterial cellulose as stabilizer of o/w emulsions. Food Hydrocolloid 53:225–232CrossRefGoogle Scholar
  27. 27.
    Zhong L, Fu S, Peng X, Zhan H, Sun R (2012) Colloidal stability of negatively charged cellulose nanocrystalline in aqueous systems. Carbohyd Polym 90(1):644–649CrossRefGoogle Scholar
  28. 28.
    Mo Y, Guo R, Liu J, Lan Y, Zhang Y, Xue W, Zhang Y (2015) Preparation and properties of PLGA nanofiber membranes reinforced with cellulose nanocrystals. Colloid Surface B 132:177–184CrossRefGoogle Scholar
  29. 29.
    Quinlan E, López-Noriega A, Thompson E, Kelly HM, Cryan SA, O’Brien FJ (2015) Development of collagen–hydroxyapatite scaffolds incorporating PLGA and alginate microparticles for the controlled delivery of rhBMP-2 for bone tissue engineering. J Control Release 198:71–79CrossRefGoogle Scholar
  30. 30.
    Romanelli SM, Fath KR, Phekoo AP, Knoll GA, Banerjee IA (2015) Layer-by-layer assembly of peptide based bioorganic–inorganic hybrid scaffolds and their interactions with osteoblastic MC3T3-E1 cells. Mater Sci Eng C 51:316–328CrossRefGoogle Scholar
  31. 31.
    Chen F, Tian M, Zhang D, Wang J, Wang Q, Yu X, Zhang X, Wan C (2012) Preparation and characterization of oxidized alginate covalently cross-linked galactosylated chitosan scaffold for liver tissue engineering. Mater Sci Eng C 32:310–320CrossRefGoogle Scholar
  32. 32.
    Hu Z, Ballinger S, Pelton R, Cranston ED (2015) Surfactant-enhanced cellulose nanocrystal Pickering emulsions. J Colloid Interface Sci 439:139–148CrossRefGoogle Scholar
  33. 33.
    Kim HL, Jung GY, Yoon JH, Han JS, Park YJ, Kim DG, Zhang M, Kim DJ (2015) Preparation and characterization of nano-sized hydroxyapatite/alginate/chitosan composite scaffolds for bone tissue engineering. Mater Sci Eng, C 54:20–25CrossRefGoogle Scholar
  34. 34.
    Hollister SJ (2005) Porous scaffold design for tissue engineering. Nat Mater 4(7):518–524CrossRefGoogle Scholar
  35. 35.
    Valente JFA, Valente TAM, Alves P, Ferreira P, Silva A, Correia IJ (2012) Alginate based scaffolds for bone tissue engineering. Mater Sci Eng C 32:2596–2603CrossRefGoogle Scholar
  36. 36.
    Islam MS, Karim MR (2010) Fabrication and characterization of poly (vinyl alcohol)/alginate blend nanofibers by electrospinning method. Colloid Surface A 366:135–140CrossRefGoogle Scholar
  37. 37.
    Yang JS, Ren HB, Xie YJ (2011) Synthesis of amidic alginate derivatives and their application in microencapsulation of λ-cyhalothrin. Biomacromolecules 12:2982–2987CrossRefGoogle Scholar
  38. 38.
    Huang C, Guo HJ, Xiong L, Wang B, Shi SL, Chen XF, Lin XQ, Wang C, Luo J, Chen XD (2016) Using wastewater after lipid fermentation as substrate for bacterial cellulose production by Gluconacetobacter xylinus. Carbohyd Polym 136:198–202CrossRefGoogle Scholar
  39. 39.
    Jia Y, Zhai X, Fu W, Liu Y, Li F, Zhong C (2016) Surfactant-free emulsions stabilized by tempo-oxidized bacterial cellulose. Carbohyd Polym 151:907–915CrossRefGoogle Scholar
  40. 40.
    Dehnad D, Mirzaei H, Emam-Djomeh Z, Jafari S, Dadashi S (2014) Thermal and antimicrobial properties of chitosan–nanocellulose films for extending shelf life of ground meat. Carbohyd Polym 109:148–154CrossRefGoogle Scholar
  41. 41.
    Moriana R, Vilaplana F, Ek M (2016) Cellulose nanocrystals from forest residues as reinforcing agents for composites: a study from macro- to nano-dimensions. Carbohyd Polym 139:139–149CrossRefGoogle Scholar
  42. 42.
    Sowjanya JA, Singh J, Mohita T, Sarvanan S, Moorthi A, Srinivasan N, Selvamurugan N (2013) Biocomposite scaffolds containing chitosan/alginate/nano-silica for bone tissue engineering. Colloid Surf B 109:294–300CrossRefGoogle Scholar
  43. 43.
    Turco G, Marsich E, Bellomo F, Semeraro S, Donati I, Brun F, Grandolfo M, Accardo A, Paoletti S (2009) Alginate/hydroxyapatite biocomposite for bone ingrowth: a trabecular structure with high and isotropic connectivity. Biomacromolecules 10:1575–1583CrossRefGoogle Scholar
  44. 44.
    Wu S, Liu X, Yeung KWK, Liu CS, Yang X (2014) Biomimetic porous scaffolds for bone tissue engineering. Mater Sci Eng R 80(2014):1–36CrossRefGoogle Scholar
  45. 45.
    Baysal K, Aroguz AZ, Adiguzel Z, Baysal BM (2013) Chitosan/alginate crosslinked hydrogels: preparation, characterization and application for cell growth purposes. Int J Biol Macromol 59:342–348CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Huiqiong Yan
    • 1
    • 2
  • Denggao Huang
    • 3
  • Xiuqiong Chen
    • 1
    • 2
  • Haifang Liu
    • 3
  • Yuhong Feng
    • 4
  • Zhendong Zhao
    • 4
  • Zihao Dai
    • 2
  • Xueqin Zhang
    • 2
  • Qiang Lin
    • 1
    • 2
  1. 1.Key Laboratory of Water Pollution Treatment and Resource Reuse of Hainan ProvinceHaikouPeople’s Republic of China
  2. 2.College of Chemistry and Chemical EngineeringHainan Normal UniversityHaikouPeople’s Republic of China
  3. 3.Central LaboratoryAffiliated Haikou Hospital Xiangya School of Medicine Central South University (Haikou Municipal People Hospital)HaikouPeople’s Republic of China
  4. 4.College of Materials and Chemical EngineeringHainan UniversityHaikouPeople’s Republic of China

Personalised recommendations