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Alginate-honey bioinks with improved cell responses for applications as bioprinted tissue engineered constructs

Published online by Cambridge University Press:  28 June 2018

Sudipto Datta ,
Ripon Sarkar ,
Veena Vyas ,
Sumant Bhutoria ,
Ananya Barui ,
Amit Roy Chowdhury  and
Pallab Datta
Sudipto Datta
Affiliation:
Centre for Healthcare Science and Technology, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India
Ripon Sarkar
Affiliation:
Centre for Healthcare Science and Technology, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India
Veena Vyas
Affiliation:
Centre for Healthcare Science and Technology, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India
Sumant Bhutoria
Affiliation:
Alfatek Systems, Kolkata-700033, W.B., India
Ananya Barui
Affiliation:
Centre for Healthcare Science and Technology, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India
Amit Roy Chowdhury
Affiliation:
Centre for Healthcare Science and Technology, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India; and Department of Aerospace Engineering and Applied Mechanics, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India
Pallab Datta*
Affiliation:
Centre for Healthcare Science and Technology, Indian Institute of Engineering Science and Technology Shibpur, Howrah-711103, W.B., India
*
a)Address all correspondence to this author. e-mail: pd@chest.iiests.ac.in, contactpallab@gmail.com
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Abstract

The polysaccharide alginate has received most extensive attention as bioink in bioprinting applications due to its ability to undergo gelation under cell-friendly conditions. However, absence of cell-binding motifs and the erratic degradation of alginate hydrogels have remained their persistent limitations. Honey is a conveniently available natural material, known for its role in wound healing and skin tissue regeneration. However, honey blending to improve biological response of alginate-based bioprinted scaffolds has not been yet reported. In the present work, honey-alginate bioinks were evaluated for their printability property (shape fidelity). It was found that honey blending reduced alginate viscosity, which gradually affected bioprinting fidelity. Therefore, the concentration that provides for acceptable bioprinting along with improvement in cell proliferations is determined. It is concluded that honey blending improves cell response of alginate bioinks and can be a facile approach to obtain bioinks especially for in situ skin tissue engineering applications.

Keywords

biologicalbiomaterialbiomedical
Type
Article
Information
Journal of Materials Research , Volume 33 , Issue 14: Focus Issue: 3D Printing of Biomaterials , 27 July 2018 , pp. 2029 - 2039
Copyright
Copyright © Materials Research Society 2018 

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References

REFERENCES

Bose, S., Ke, D., Sahasrabudhe, H., and Bandyopadhyay, A.: Additive manufacturing of biomaterials. Prog. Mater. Sci. 93, 45 (2018).CrossRefGoogle Scholar
Ozbolat, I.T., Pemg, W., and Ozbolat, V.: Application areas of 3D bioprinting. Drug Discov. Today 21, 1257 (2017).CrossRefGoogle Scholar
Egan, P.F., Gonella, V.C., Engensperger, M., Ferguson, S.J., and Shea, K.: Computationally designed lattices with tuned properties for tissue engineering using 3D printing. PLoS One 12, e0182902 (2017).CrossRefGoogle ScholarPubMed
Peng, W., Datta, P., Ayan, B., Ozbolat, V., Sosnoski, D., and Ozbolat, I.T.: 3D bioprinting for drug discovery and development in pharmaceutics. Acta Biomater. 57, 26 (2017).CrossRefGoogle ScholarPubMed
Ning, L. and Chen, X.: A brief review of extrusion-based tissue scaffold bio-printing. Biotechnol. J. 12, 1600671 (2017).CrossRefGoogle ScholarPubMed
Ozbolat, I.T. and Hospodiuk, M.: Current advances and future perspectives in extrusion-based bioprinting. Biomaterials 76, 321 (2016).CrossRefGoogle ScholarPubMed
Cubo, N., Garcia, M., Cañizo, J.F., Velasco, D., and Jorcano, J.L.: 3D bioprinting of functional human skin: Production and in vivo analysis. Biofabrication 9 (2016).CrossRefGoogle ScholarPubMed
Duchi, S., Onofrillo, C., Connell, C.D.O., Blanchard, R., Quigle, A.F., Kapsa, R.M.I., Peter, P., Wallace, G., Di Bella, C., and Choong, P.F.M.: Handheld co-axial bioprinting: Application to in situ surgical cartilage repair. Sci. Rep. 7, 5837 (2017).CrossRefGoogle ScholarPubMed
Binder, K.W., Zhao, W., Aboushwareb, T., Dice, D., Atala, A., and Yoo, J.J.: In situ bioprinting of the skin for burns. J. Am. Coll. Surg. 211, S76 (2010).CrossRefGoogle Scholar
Hospodiuk, M., Dey, M., Sosnoski, D., and Ozbolat, I.T.: The bioink: A comprehensive review on bioprintable materials. Biotechnol. Adv. 35, 217 (2017).CrossRefGoogle ScholarPubMed
Williams, S.K. and Hoying, J.B.: Bioinks for bioprinting. In Bioprinting in Regenerative Medicine, Turksen, K., ed. (Springer International Publishing, Cham, 2015); pp. 1–31.Google Scholar
Hölzl, K., Lin, S., Tytgat, L., Van Vlierberghe, S., Gu, L., and Ovsianikov, A.: Bioink properties before, during and after 3D bioprinting. Biofabrication 8, 032002 (2016).CrossRefGoogle ScholarPubMed
Abbadessa, A., Blokzijl, M.M., Mouser, V.H.M., Marica, P., Malda, J., Hennink, W.E., and Vermonden, T.: A thermo-responsive and photo-polymerizable chondroitin sulfate-based hydrogel for 3D printing applications. Carbohydr. Polym. 149, 163 (2016).CrossRefGoogle ScholarPubMed
Billiet, T., Vandenhaute, M., Schelfhout, J., Vlierberghe, S., and Dubruel, P.: A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials 33, 6020–6041 (2012).CrossRefGoogle ScholarPubMed
Wu, Z., Su, X., Xu, Y., Kong, B., Sun, W., and Mi, S.: Bioprinting three-dimensional cell-laden tissue constructs with controllable degradation. Sci. Rep. 6, 24474 (2016).CrossRefGoogle ScholarPubMed
Jia, J., Richards, D.J., Pollard, S., Tan, Y., Rodriguez, J., Visconti, R.P., Trusk, T.C., Yost, M.J., Yao, H., Markwald, R.R., and Mei, Y.: Engineering alginate as bioink for bioprinting. Acta Biomater. 10, 4323 (2014).CrossRefGoogle ScholarPubMed
Luo, Y., Luo, G., Gelinsky, M., Huang, P., and Ruan, C.: 3D bioprinting scaffold using alginate/polyvinyl alcohol bioinks. Mater. Lett. 189, 295 (2017).CrossRefGoogle Scholar
Wan, L.Q., Jiang, J., Arnold, D.E., Guo, X.E., Lu, H.H., and Mow, V.C.: Calcium concentration effects on the mechanical and biochemical properties of chondrocyte-alginate constructs. Cell. Mol. Bioeng. 1, 93 (2008).CrossRefGoogle ScholarPubMed
Vandamme, L., Heyneman, A., Hoeksema, H., Verbelen, J., and Monstrey, S.: Honey in modern wound care: A systematic review. Burns 39, 1514 (2013).CrossRefGoogle ScholarPubMed
Saikaly, S.K. and Khachemoune, A.: Honey and wound healing: An update. Am. J. Clin. Dermatol. 18, 237 (2017).CrossRefGoogle ScholarPubMed
El-kased, R.F., Amer, R.I., Attia, D., and Elmazar, M.M.: Honey-based hydrogel: In vitro and comparative in vivo evaluation for burn wound healing. Sci. Rep. 7, 9692 (2017).CrossRefGoogle ScholarPubMed
Choi, D.S., Kim, S., Lim, Y., Gwon, H., Park, J.S., Nho, Y., Kwon, J., and Honey, C.: Hydrogel incorporated with chestnut honey accelerates wound healing and promotes early HO-1 protein expression in diabetic (db/db) mice. Tissue Eng. Regener. Med. 9, 36 (2012).CrossRefGoogle Scholar
Majtan, J.: Honey: An immunomodulator in wound healing. Wound Repair Regen. 22, 187 (2014).CrossRefGoogle ScholarPubMed
Wang, T., Zhu, X.K., Xue, X.T., and Wu, D.Y.: Hydrogel sheets of chitosan, honey and gelatin as burn wound dressings. Carbohydr. Polym. 88, 75 (2012).CrossRefGoogle Scholar
Sarhan, W.A. and Azzazy, H.M.E.: High concentration honey chitosan electrospun nanofibers: Biocompatibility and antibacterial effects. Carbohydr. Polym. 122, 135 (2015).CrossRefGoogle ScholarPubMed
Tavakoli, J. and Tang, Y.: Honey/PVA hybrid wound dressings with controlled release of antibiotics: Structural, physico-mechanical and in-vitro biomedical studies. Mater. Sci. Eng., C 77, 318 (2017).CrossRefGoogle ScholarPubMed
Chaudhury, A., Bag, S., Barui, A., Banerjee, P., and Chatterjee, J.: Honey dilution impact on in vitro wound healing: Normoxic and hypoxic condition. Wound Repair Regen. 23, 412 (2015).CrossRefGoogle Scholar
Wang, L., Xu, M., Luo, L., Zhou, Y., and Si, P.: Iterative feedback bio-printing-derived cell-laden hydrogel scaffolds with optimal geometrical fidelity and cellular controllability. Sci. Rep. 8, 2802 (2018).CrossRefGoogle ScholarPubMed
Ribeiro, A., Blokzijl, M.M., Levato, R., Visser, C.W., Castilho, M., Hennink, W.E., Vermonden, T., and Malda, J.: Assessing bioink shape fidelity to aid material development in 3D bioprinting. Biofabrication 10, 014102 (2017).CrossRefGoogle ScholarPubMed
Ouyang, L., Highley, C.B., Rodell, C.B., Sun, W., and Burdick, J.A.: 3D printing of shear-thinning hyaluronic acid hydrogels with secondary cross-linking. ACS Biomater. Sci. Eng. 2, 1743 (2016).CrossRefGoogle Scholar
Ouyang, L., Yao, R., Zhao, Y., and Sun, W.: Effect of bioink properties on printability and cell viability for 3D bioplotting of embryonic stem cells. Biofabrication 8, 035020 (2016).CrossRefGoogle ScholarPubMed
Kyle, S., Jessop, Z.M., Al-sabah, A., and Whitaker, I.S.: “Printability” of candidate biomaterials for extrusion based 3D printing: State-of-the-art. Adv. Healthcare Mater. 6, 1700264 (2017).CrossRefGoogle ScholarPubMed
Di Giuseppe, M., Law, N., Webb, B., Macrae, R.A., Liew, L.J., Sercombe, T.B., Dilley, R.J., and Doyle, B.J.: Mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting. J. Mech. Behav. Biomed. Mater. 79, 150 (2018).CrossRefGoogle Scholar
Hixon, K.R., Lu, T., Carletta, M.N., McBride-Gagyi, S.H., Janowiak, B.E., and Sell, S.A.: A preliminary in vitro evaluation of the bioactive potential of cryogel scaffolds incorporated with Manuka honey for the treatment of chronic bone infections. J. Biomed. Mater. Res., Part B 106, 1918–1933 (2017).CrossRefGoogle ScholarPubMed
Sarkar, R., Ghosh, A., Barui, A., and Datta, P.: Repositing honey incorporated electrospun nanofiber membranes to provide anti-oxidant, anti-bacterial and anti-inflammatory microenvironment for wound regeneration. J. Mater. Sci.: Mater. Med. 29, 31 (2018).Google ScholarPubMed
He, Y., Yang, F., Zhao, H., Gao, Q., Xia, B., and Fu, J.: Research on the printability of hydrogels in 3D bioprinting. Sci. Rep. 6, 1 (2016).Google ScholarPubMed
Schmitt, A., Rödel, P., Anamur, C., Seeliger, C., Imhoff, A.B., Herbst, E., Vogt, S., Van Griensven, M., Winter, G., and Engert, J.: Calcium alginate gels as stem cell matrix-making paracrine stem cell activity available for enhanced healing after surgery. PLoS One 10, 1 (2015).CrossRefGoogle ScholarPubMed
Larsen, B.E., Bjørnstad, J., Pettersen, E.O., Tønnesen, H.H., and Melvik, J.E.: Rheological characterization of an injectable alginate gel system. BMC Biotechnol. 15, 1 (2015).CrossRefGoogle ScholarPubMed
Chung, J.H.Y., Naficy, S., Yue, Z., Kapsa, R., Quigley, A., Moulton, S.E., and Wallace, G.G.: Bio-ink properties and printability for extrusion printing living cells. Biomater. Sci. 1, 763 (2013).CrossRefGoogle Scholar
Park, J., Lee, S.J., Chung, S., Lee, J.H., Kim, W.D., Lee, J.Y., and Park, S.A.: Cell-laden 3D bioprinting hydrogel matrix depending on different compositions for soft tissue engineering: Characterization and evaluation. Mater. Sci. Eng., C 71, 678 (2017).CrossRefGoogle ScholarPubMed
Di Giuseppe, M., Law, N., Webb, B., Macrae, R.A., Sercombe, T.B., Dilley, R.J., Doyle, B.J., and Liew, L.J.: Journal of the mechanical behavior of biomedical materials mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting. J. Mech. Behav. Biomed. Mater. 79, 150 (2018).CrossRefGoogle Scholar
Kaklamani, G., Cheneler, D., Grover, L.M., Adams, M.J., and Bowen, J.: Mechanical properties of alginate hydrogels manufactured using external gelation. J. Mech. Behav. Biomed. Mater. 36, 135 (2014).CrossRefGoogle ScholarPubMed
Ahearne, M., Yang, Y., and Liu, K.: Mechanical characterisation of hydrogels for tissue engineering applications. Tissue Eng. 4, 1 (2008).Google Scholar
Hixon, K.R., Lu, T., McBride-Gagyi, S.H., Janowiak, B.E., and Sell, S.A.: A comparison of tissue engineering scaffolds incorporated with manuka honey of varying UMF. BioMed Res. Int. 2017, 4843065 (2017).CrossRefGoogle ScholarPubMed
Minden-Birkenmaier, B.A., Neuhalfen, R.M., Janowiak, B.E., and Sell, S.: Preliminary investigation and characterization of electrospun polycaprolactone and manuka honey scaffolds for dermal repair. J. Eng. Fibers Fabr. 10, 126 (2015).Google Scholar
Rajput, M., Bhandaru, N., Barui, A., Chaudhary, A., Paul, R.R., Mukherjee, R., and Chatterjee, J.: Nano-patterned honey incorporated silk fibroin membranes for improving cellular compatibility. RSC Adv. 4, 44674 (2014).CrossRefGoogle Scholar
Funada, M., Hara, H., Sasagawa, H., Kitagawa, Y., and Kadowaki, T.: A honey bee Dscam family member, AbsCAM, is a brain-specific cell adhesion molecule with the neurite outgrowth activity which influences neuronal wiring during development. Eur. J. Neurosci. 25, 168 (2007).CrossRefGoogle ScholarPubMed
Nordin, A., Sainik, N.Q.A.V., Zulfarina, M.S., Naina-Mohamed, I., Saim, A., and Bt Hj Idrus, R.: Honey and epithelial to mesenchymal transition in wound healing: An evidence-based review. Wound Med. 18, 8 (2017).CrossRefGoogle Scholar
Oryan, A., Alemzadeh, E., and Moshiri, A.: Biological properties and therapeutic activities of honey in wound healing: A narrative review and meta-analysis. J. Tissue Viability 25, 98 (2016).CrossRefGoogle ScholarPubMed
Daly, A.C., Freeman, F.E., Gonzalez-Fernandez, T., Critchley, S.E., Nulty, J., and Kelly, D.J.: 3D bioprinting for cartilage and osteochondral tissue engineering. Adv. Healthcare Mater. 6, 1700298 (2017).CrossRefGoogle ScholarPubMed
Nair, K., Gandhi, M., Khalil, S., Yan, K.C., Marcolongo, M., Barbee, K., and Sun, W.: Characterization of cell viability during bioprinting processes. Biotechnol. J. 4, 1168 (2009).CrossRefGoogle ScholarPubMed
He, P., Zhao, J., Zhang, J., Li, B., Gou, Z., Gou, M., and Li, X.: Bioprinting of skin constructs for wound healing. Burn. Trauma 6, 5 (2018).CrossRefGoogle ScholarPubMed
Barui, A., Banerjee, P., Chaudhary, A., Conjeti, S., Mondal, B., Dey, S., and Chatterjee, J.: Evaluation of angiogenesis in diabetic lower limb wound healing using a natural medicine: A quantitative approach. Wound Med. 6, 26 (2014).CrossRefGoogle Scholar