Succinylated Bacterial Cellulose Induce Carbonated Hydroxyapatite Deposition in a Solution Mimicking Body Fluid

Farah Nurlidar(1*), Mime Kobayashi(2)

(1) Center for Application of Isotopes and Radiation, National Nuclear Energy Agency, Jl. Lebak Bulus Raya No. 49, Jakarta Selatan 12043, Indonesia
(2) Graduate School of Materials Science, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan
(*) Corresponding Author


Incorporation of bone-like hydroxyapatite into bacterial cellulose (BC) is an attractive approach for the fabrication of a bioactive three-dimensional (3D) scaffold for bone tissue regeneration. This study investigates the influence of the succinylation of BC on its ability to incorporate bone-like hydroxyapatite. A biomimetic process using a 1.5 × Simulated Body Fluid (SBF) was used to deposit the hydroxyapatite into the succinylated-BC. After soaking the succinylated-BC in the 1.5 × SBF for six days, Scanning Electron Microscope (SEM) images were taken and the composition of the succinylated-BC was analyzed by energy dispersive X-ray spectrometry. The biocompatibility of the scaffolds was tested in vitro using rat Bone Marrow Stromal Cells (rBMSCs). The SEM images and Fourier Transform Infrared Spectroscopy (FTIR) spectra showed that carbonated hydroxyapatite was deposited on the succinylated-BC. In contrast, only a small amount of carbonated hydroxyapatite deposition was observed on unmodified BC, indicating that the succinyl group in the BC is effective for inducing hydroxyapatite deposition. In vitro studies using rBMSCs revealed the biocompatibility of the scaffold. Combining with the ability of the cells to differentiate into bone cells, the succinylated-BC scaffold is a promising 3D scaffold for bone tissue regeneration.


bacterial cellulose; carbonated hydroxyapatite; 1.5 × simulated body fluid; succinylation; 3D scaffolds

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[1] Janicki, P., and Schmidmaier, G., 2011, What should be the characteristics of the ideal bone graft substitute? Combining scaffolds with growth factor and/or stem cells, Injury, 42 (Suppl. 2), 77–581.

[2] Swetha, M., Sahithi, K., Moorthi, A., Srinivasan, N., Ramasamy, K., and Selvamurugan, N., 2010, Biocomposites containing natural polymers and hydroxyapatite for bone tissue engineering, Int. J. Biol. Macromol., 47 (1), 1–4.

[3] O’Brien, F.J., 2011, Biomaterials and scaffolds for tissue engineering, Mater. Today, 14 (3), 88–95.

[4] Kepa, K., Coleman, R., and Grøndahl, L., 2015, In vitro mineralization of functional polymers, Biosurf. Biotribol., 1 (3), 214–227.

[5] Raucci, M.G., Guarino, V., and Ambrosio, L., 2012, Biomimetic strategies for bone repair and regeneration, J. Funct. Biomater., 3 (3), 688–705.

[6] Zaborowska, M., Bodin, A., Bäckdahl, H., Popp, J., Goldstein, A., and Gatenholm, P., 2010, Microporous bacterial cellulose as a potential scaffold for bone regeneration, Acta Biomater., 6 (7), 2540–2547.

[7] Ullah, H., Wahid, F., Santos, H.A., and Khan, T., 2016, Advances in biomedical and pharmaceutical applications of functional bacterial cellulose-based nanocomposites, Carbohydr. Polym., 150, 330–352.

[8] Shah, N., Ul-Islam, M., Khattak, W.A., and Park, J.K., 2013, Overview of bacterial cellulose composites: A multipurpose advanced material, Carbohydr. Polym., 98 (2), 1585–1598.

[9] Darwis, D., Khusniya, T., Hardiningsih, L, Nurlidar, F., and Winarno, H., 2012, In-vitro degradation behaviour of irradiated bacterial cellulose membrane, Atom Indonesia, 38 (2), 78–82.

[10] Darwis, D., Hardiningsih, L., Nurlidar, F., and Fajarsyah, R., 2012, Biological Evaluation of Irradiated Bacterial Cellulose (BC) Membrane for Application in Guided Bone Regeneration, Proceedings of The International Conference on Innovation in Polymer Science and Technology 2011, Indonesian Polymer Association, Bali, 28 November – 1 December 2011, 205–210.

[11] Yang, M., Zhen, W., Chen, H., and Shan, Z., 2016, Biomimetic design of oxidized bacterial cellulose-gelatin-hydroxyapatite nanocomposites, J. Bionic Eng., 13 (4), 631–640.

[12] Palmer, L.C., Newcomb, C.J., Kaltz, S.R., Spoerke, E.D., and Stupp, S.I., 2008, Biomimetic systems for hydroxy hydroxyapatite mineralization inspired by bone and enamel, Chem. Rev., 108 (11), 4754–4783.

[13] Ahn, S.J., Shin, Y.M., Kim, S.E., Jeong, S.I., Jeong, J.O., Park, J.S. Gwon, H.J., Seo, D.E., Nho, Y.C., Kang, S.S., Kim, C.Y., Huh, J.B., and Lim, Y.M., 2015, Characterization of hydroxyapatite-coated bacterial cellulose scaffold for bone tissue engineering, Biotechnol. Bioprocess Eng., 20 (5), 948–955.

[14] Wan, Y.Z., Huang, Y., Yuan, C.D., Raman, S., Zhu, Y., Jiang, H.J., He, F., and Gao, C., 2007, Biomimetic synthesis of hydroxyapatite/bacterial cellulose nanocomposites for biomedical applications, Mater. Sci. Eng., C, 27 (4), 855–864.

[15] Morita, Y., Matsumoto, C., Miyazaki, T., Ishida, E., Tanaka, K., and Goto, T., 2009, Apatite deposition on hyaluronic acid gels in biomimetic conditions, Trans. Mater. Res. Soc. Japan, 34 (1), 85–87.

[16] Kawai, T., Ohtsuki, C., Kamitakahara, M., Hosoya, K., Tanihara, M., Miyazaki, T., Sakaguchi, Y., and Konagaya, S., 2007, In vitro apatite formation on polyamide containing carboxyl groups modified with silanol groups, J. Mater. Sci. - Mater. Med., 18, 1037–1042.

[17] Saito, A., Suzuki, Y., Ogata, S., Ohtsuki, C., and Tanihara, M., 2005, Accelerated bone repair with the use of a synthetic BMP-2-derived peptide and bone marrow stromal cells, J. Biomed. Mater. Res. Part A, 72 (1), 77–82.

[18] Stoch, A., Jastrzębski, W., Brożek, A., Trybalska, B., Cichocińska, M., and Szarawara, E., 1999, FTIR monitoring of the growth of the carbonate containing hydroxyapatite layers from simulated and natural body fluids, J. Mol. Struct., 511-512, 287–294.

[19] Garskaite, E., Gross, K.A., Yang S.W., Yang, T.C.K., Yang, J.C., and Kareiva, A., 2014, Effect of processing conditions on the crystallinity and structure of carbonated calcium hydroxyapatite (CHAp), CrystEngComm, 16 (19), 3950–3959.

[20] Nurlidar, F., Kobayashi, M., Terada, K., Ando, T., and Tanihara, M., 2017, Cytocompatible polyion complex gel of poly(Pro-Hyp-Gly) for simultaneous rat bone marrow stromal cell encapsulation, J. Biomater. Sci., Polym. Ed., 28 (14), 1480–1496.

[21] Kusumastuti, Y., Shibasaki, Y., Hirohara, S., Kobayashi, M., Terada, K., Ando, T., and Tanihara, M., 2017, Encapsulation of rat bone marrow stromal cells using a poly-ion complex gel of chitosan and succinylated poly(Pro-Hyp-Gly), J. Tissue Eng. Regener. Med., 11 (3), 869–876.


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