Engineering bone tissue using human dental pulp stem cells and an osteogenic collagen-hydroxyapatite-poly ( l -lactide-co-ɛ-caprolactone) scaffold
Abstract
The aim of this study was to design a new natural/synthetic bioactive bone scaffold for potential use in bone replacement applications. We developed a tri-component osteogenic composite scaffold made of collagen (Coll), hydroxyapatite (HA) and poly(l-lactide-co-ɛ-caprolactone) (PLCL). This Coll/HA/PLCL composite scaffold was combined with human osteoblast-like cells obtained by differentiation of dental pulp stem cells (DPSCs) to engineer bone tissue in vitro. Results show that the 3D Coll/HA/PLCL composite scaffold was highly porous, thereby enabling osteoblast-like cell adhesion and growth. Cultured in the Coll/HA/PLCL scaffold, the osteoblast-like cells expressed different osteogenic genes, produced alkaline phosphatase and formed nodules more than did PLCL alone. Micro-CT analyses revealed a significant (30%) increase of tissue mineralisation on the surface as well as inside of the Coll/HA/PLCL scaffold, thus confirming its effectiveness as a bone regeneration platform.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
PLCL combined with HA can be used to promote differentiation of mesenchymal stem cells towards osteogenesis.
“PLCL combined with HA can be used to promote the differentiation of mesenchymal stem cells towards osteogenesis [227].”
From Application of PLCL as a biodegradable polymer in biomedical engineering (2026) · cites this paper as [227]
Cites
Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo
Gronthos, S., Mankani, M. H., Brahim, J. S., Robey, P. G., & Shi, S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240309797 · Cited by 4,580 · see citing works
Murphy, C. M., Haugh, M. G., & O’Brien, F. J. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.09.063 · Cited by 2,057 · see citing works
Fracture healing: The diamond concept
Giannoudis, P. V., Einhorn, T. A., & Marsh, D. (2007) · Injury · doi:10.1016/s0020-1383(08)70003-2 · Cited by 1,092 · see citing works
d’Aquino, R., Graziano, A., Sampaolesi, M., Laino, G., Pirozzi, G., ROSA, A. D., & Papaccio, G. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402121 · Cited by 517 · see citing works
Molecular Basis and Clinical Application of Biological Markers of Bone Turnover*
Calvo, M. S., Eyre, D. R., & Gundberg, C. M. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-4-333 · Cited by 506 · see citing works
Periodontal Diseases in the United States Population
Oliver, R. C., Brown, L. J., & Löe, H. A. (1998) · Journal of Periodontology · doi:10.1902/jop.1998.69.2.269 · Cited by 424 · see citing works
Dental Pulp Stem Cells: A Promising Tool for Bone Regeneration
d’Aquino, R., Papaccio, G., Laino, G., & Graziano, A. (2008) · Stem Cell Reviews and Reports · doi:10.1007/s12015-008-9013-5 · Cited by 310 · see citing works
Riekstiņa, U., Čakstiņa, I., Parfejevs, V., Hoogduijn, M. J., Jankovskis, G., Muižnieks, I., Muceniece, R., & Ancāns, J. (2009) · Stem Cell Reviews and Reports · doi:10.1007/s12015-009-9094-9 · Cited by 307 · see citing works
Iohara, K., Zheng, L. W., Ito, M., Tomokiyo, A., Matsushita, K., & Nakashima, M. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0161 · Cited by 304 · see citing works
Perry, B. C., Zhou, D., Wu, X., Yang, F., Byers, M. A., Chu, T. G., Hockema, J. J., Woods, E. J., & Goebel, W. S. (2008) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2008.0031 · Cited by 301 · see citing works
Niu, X., Feng, Q., Wang, M., Guo, X., & Zheng, Q. (2009) · Journal of Controlled Release · doi:10.1016/j.jconrel.2008.11.020 · Cited by 296 · see citing works
Phipps, M. C., Clem, W. C., Grunda, J. M., Clines, G. A., & Bellis, S. L. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2011.09.080 · Cited by 287 · see citing works
Bio-adhesive Surfaces to Promote Osteoblast Differentiation and Bone Formation
Garcı́a, A. J., & Reyes, C. D. (2005) · Journal of Dental Research · doi:10.1177/154405910508400502 · Cited by 280 · see citing works
Surface modification of polyester biomaterials for tissue engineering
Jiao, Y., & Cui, F. (2007) · Biomedical Materials · doi:10.1088/1748-6041/2/4/r02 · Cited by 253 · see citing works
A novel spatially designed and functionally graded electrospun membrane for periodontal regeneration
Bottino, M. C., Thomas, V., & Janowski, G. M. (2010) · Acta Biomaterialia · doi:10.1016/j.actbio.2010.08.019 · Cited by 243 · see citing works
Stem cells in bone tissue engineering
Seong, J.-M., Kim, B.-C., Park, J.-H., Kwon, I. K., Mantalaris, A., & Hwang, Y. (2010) · Biomedical Materials · doi:10.1088/1748-6041/5/6/062001 · Cited by 226 · see citing works
Yuan, J., Cui, L., Zhang, W. J., Liu, W. X., & Cao, Y. (2006) · Biomaterials · doi:10.1016/j.biomaterials.2006.10.015 · Cited by 218 · see citing works
Dental Pulp Stem Cells: A Promising Tool for Bone Regeneration
Graziano, A., d’Aquino, R., Laino, G., & Papaccio, G. (2008) · Stem Cell Reviews and Reports · doi:10.1007/s12015-008-9015-3 · Cited by 198 · see citing works
Role of mesenchymal stem cells in regenerative medicine: application to bone and cartilage repair
Granero‐Moltó, F., Weis, J. A., Longobardi, L., & Spagnoli, A. (2008) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.8.3.255 · Cited by 175 · see citing works
Bue, M. D., Ricco, S., Ramoni, R., Conti, V., Gnudi, G., & Grolli, S. (2008) · Veterinary Research Communications · doi:10.1007/s11259-008-9093-3 · Cited by 138 · see citing works
Osteoblasts respond to hydroxyapatite surfaces with immediate changes in gene expression
Xie, J., Baumann, M. J., & McCabe, L. R. (2004) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.30140 · Cited by 134 · see citing works
Gong, Y., Zhou, Q., Gao, C., & Shen, J. (2007) · Acta Biomaterialia · doi:10.1016/j.actbio.2006.12.008 · Cited by 126 · see citing works
Human Primary Osteocyte Differentiation in a 3D Culture System
Boukhechba, F., Balaguer, T., Michiels, J., Ackermann, K., Quincey, D., Bouler, J., Pyerin, W. G., Carle, G. F., & Rochet, N. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090517 · Cited by 123 · see citing works
Biological therapy of bone defects: the immunology of bone allo-transplantation
Graham, S. M., Leonidou, A. O., Aslam-Pervez, N., Hamza, A., Panteliadis, P., Heliotis, M., Mantalaris, A., & Tsiridis, E. E. (2010) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2010.481669 · Cited by 117 · see citing works
Riccio, M., Maraldi, T., Pisciotta, A., Sala, G. B. L., Ferrari, A., Bruzzesi, G., Motta, A., Migliaresi, C., & Pol, A. D. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0542 · Cited by 112 · see citing works
Dental pulp stem cells: osteogenic differentiation and gene expression
Mori, G., Brunetti, G., Oranger, A., Carbone, C., Ballini, A., Muzio, L. L., Colucci, S. C., Mori, C., Grassi, F. R., & Grano, M. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06234.x · Cited by 105 · see citing works
Phipps, M. C., Clem, W. C., Catledge, S. A., Xu, Y., Hennessy, K. M., Thomas, V., Jablonsky, M. J., Chowdhury, S., Stanishevsky, A. V., Vohra, Y. K., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016813 · Cited by 92 · see citing works
Shetty, P., Cooper, K., & Viswanathan, C. (2010) · Asian Journal of Transfusion Science · doi:10.4103/0973-6247.59386 · Cited by 86 · see citing works
Sculean, A., Windisch, P., Szendroi-Kiss, D., Horváth, A., Rosta, P., Becker, J., Gera, I., & Schwarz, F. (2008) · Journal of Periodontology · doi:10.1902/jop.2008.080009 · Cited by 84 · see citing works
Osteoinductive bone graft substitutes for lumbar fusion: a systematic review
Agarwal, R. K., Williams, K., Umscheid, C. A., & Welch, W. C. (2009) · Journal of Neurosurgery Spine · doi:10.3171/2009.6.spine08669 · Cited by 75 · see citing works
Nakatsuka, R., Nozaki, T., Uemura, Y., Matsuoka, Y., Sasaki, Y., Shinohara, M., Ohura, K., & Sonoda, Y. (2010) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2010.03.003 · Cited by 67 · see citing works
Human Dental Pulp Stem Cells Hook into Biocoral Scaffold Forming an Engineered Biocomplex
Mangano, C., Paino, F., d’Aquino, R., ROSA, A. D., Iezzi, G., Piattelli, A., Laino, L., Mitsiadis, T. A., Desiderio, V., Mangano, F. G., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018721 · Cited by 57 · see citing works
Espitalier, F., Vinatier, C. S., Lerouxel, E., Guicheux, J., Pilet, P., Moreau, F., Daculsi, G., Weiss, P., & Malard, O. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.10.051 · Cited by 55 · see citing works
The enhancement of osteogenesis through the use of dental pulp pluripotent stem cells in 3D
Atari, M., Caballé‐Serrano, J., Gil-Recio, C., Giner-Delgado, C., Martínez‐Sarrà, E., García-Fernández, D. A., Barajas, M., Hernández-Alfaro, F. J., Ferrés‐Padró, E., & Giner, L. (2012) · Bone · doi:10.1016/j.bone.2012.01.005 · Cited by 48 · see citing works
Bioactivating electrically conducting polypyrrole with fibronectin and bovine serum albumin
Akkouch, A., Shi, G., Zhang, Z., & Rouabhia, M. (2009) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.32357 · Cited by 44 · see citing works
Self-citationKawase, T., Okuda, K., Kogami, H., Nakayama, H., Nagata, M., Sato, T. F., Wolff, L. F., & Yoshie, H. (2010) · Journal of Periodontology · doi:10.1902/jop.2009.090523 · Cited by 43 · see citing works
INNOVENT Technologieentwicklung e. V., P. 2., Vogt, S., Larcher, Y., Beer, B., Wilke, I., & Schnabelrauch, M. (2002) · European Cells and Materials · doi:10.22203/ecm.v004a03 · Cited by 42 · see citing works
In Vitro Osteogenic Differentiation of Cultured Human Dental Papilla-Derived Cells
Park, B.-W., Hah, Y., Choi, M.-J., Ryu, Y.-M., Lee, S.-G., Kim, D. R., Kim, J., & Byun, J. (2009) · Journal of Oral and Maxillofacial Surgery · doi:10.1016/j.joms.2008.08.037 · Cited by 41 · see citing works
A Collagen/Smooth Muscle Cell-Incorporated Elastic Scaffold for Tissue-Engineered Vascular Grafts
Park, I., Kim, S., Kim, Y. H., Kim, I. H., & Kim, S. H. (2009) · Journal of Biomaterials Science Polymer Edition · doi:10.1163/156856208x386237 · Cited by 34 · see citing works
Fabrication of collagen hybridized elastic PLCL for tissue engineering
Lim, J. I., Yu, B., & Lee, Y. (2008) · Biotechnology Letters · doi:10.1007/s10529-008-9808-0 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bone regenerative medicine: classic options, novel strategies, and future directions
Oryan, A., Alidadi, S., Moshiri, A., & Maffulli, N. (2014) · Journal of Orthopaedic Surgery and Research · doi:10.1186/1749-799x-9-18 · Cited by 1,249 · see citing works
Sol–gel based materials for biomedical applications
Owens, G. J., Singh, R. K., Foroutan, F., Al-Qaysi, M., Han, C., Mahapatra, C., Kim, H., & Knowles, J. C. (2016) · Progress in Materials Science · doi:10.1016/j.pmatsci.2015.12.001 · Cited by 961 · see citing works
FTIR analysis of natural and synthetic collagen
Riaz, T., Zeeshan, R., Zarif, F., Ilyas, K., Muhammad, N., Safi, S. Z., Rahim, A., Rizvi, S. A. A., & Rehman, I. U. (2018) · Applied Spectroscopy Reviews · doi:10.1080/05704928.2018.1426595 · Cited by 628 · see citing works
“(169) design a new natural/synthetic bioactive bone scaffold for potential use in bone replacement application.”
BackgroundTissue Engineering and Cell-Based Therapies for Fractures and Bone Defects
Perez, J. R., Kouroupis, D., Li, D. J., Best, T. M., Kaplan, L., & Correa, D. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00105 · Cited by 390 · see citing works
“Recently, Akkouch et al. demonstrated successful extracellular mineralization of osteoblast-like cells derived from DPSCs seeded onto collagen-hydroxyapatitepoly(l-lactide-co-ǫ-caprolactone) matrix (Akkouch et al., 2014).”
BackgroundDental pulp stem cells: function, isolation and applications in regenerative medicine
Tatullo, M., Marrelli, M., Shakesheff, K. M., & White, L. J. (2014) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.1899 · Cited by 354 · see citing works
“More recently, DPSCs were pre-differentiated into osteoblast-like cells and seeded onto collagen–hydroxyapatite–poly(L-lactideco-ε-caprolactone) (Col1–HA–PLCL) composite scaffolds (Akkouch et al., 2014).”
BackgroundBone tissue regeneration: biology, strategies and interface studies
Ansari, M. (2019) · Progress in Biomaterials · doi:10.1007/s40204-019-00125-z · Cited by 353 · see citing works
“DPSCs seeded/collagen-HA-poly(llactide-co-ɛ-caprolactone) scaffold confirmed effective ECM mineralization of osteoblast (Akkouch et al. 2014).”
BackgroundTissue-engineering-based Strategies for Regenerative Endodontics
de Albuquerque, M. T. P., Valera, M. C., Nakashima, M., Nor, J. E., & Bottino, M. C. (2014) · Journal of Dental Research · doi:10.1177/0022034514549809 · Cited by 247 · see citing works
Electrospun biodegradable nanofibers scaffolds for bone tissue engineering
Khajavi, R., Abbasipour, M., & Bahador, A. (2015) · Journal of Applied Polymer Science · doi:10.1002/app.42883 · Cited by 177 · see citing works
The effects of hypoxia on the stemness properties of human dental pulp stem cells (DPSCs)
Ahmed, N. E.-M. B., Murakami, M., Kaneko, S., & Nakashima, M. (2016) · Scientific Reports · doi:10.1038/srep35476 · Cited by 121 · see citing works
Artificial Bone via Bone Tissue Engineering: Current Scenario and Challenges
Kashte, S., Jaiswal, A. K., & Kadam, S. S. (2017) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-016-0001-6 · Cited by 109 · see citing works
Scaffold-free three-dimensional cell culturing using magnetic levitation
Türker, E., Demirçak, N., & Yıldız, A. A. (2018) · Biomaterials Science · doi:10.1039/c8bm00122g · Cited by 102 · see citing works
Jazayeri, H. E., Tahriri, M., Razavi, M., Khoshroo, K., Fahimipour, F., Dashtimoghadam, E., Almeida, L. E., & Tayebi, L. (2016) · Materials Science and Engineering C · doi:10.1016/j.msec.2016.08.055 · Cited by 95 · see citing works
Pulp–Dentin Tissue Healing Response: A Discussion of Current Biomedical Approaches
Shah, D. K., Lynd, T. O., Ho, D., Chen, J., Vines, J. B., Jung, H.-D., Kim, J. H., Zhang, P., Wu, H., Jun, H., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020434 · Cited by 91 · see citing works
“3D Col/HA/PLCL DPSC Differentiation and proliferation [123]”
Favi, P. M., Ospina, S. P., Kachole, M., Gao, M. X., Atehortúa, L., & Webster, T. J. (2016) · Cellulose · doi:10.1007/s10570-016-0867-4 · Cited by 86 · see citing works
“…and collagen copolymers (calcium phosphate mineralized collagen–glycosaminoglycans copolymers) (Harley et al. 2010; Lynn et al. 2010), and most often polymer–HA composites (Akkouch et al. 2014; Li et al. 2012; Torabinejad et al. 2014) have been studied for bone tissue engineering applications.”
BackgroundInfluentialBone tissue engineering: Adult stem cells in combination with electrospun nanofibrous scaffolds
Moradi, S. L., Golchin, A., Hajishafieeha, Z., Khani, M., & Ardeshirylajimi, A. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26606 · Cited by 82 · see citing works
Temporomandibular Joint Regenerative Medicine
van Bellinghen, X., Idoux‐Gillet, Y., Pugliano, M., Strub, M., Bornert, F., Clauss, F., Schwinté, P., Keller, L., Benkirane-Jessel, N., Kuchler‐Bopp, S., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020446 · Cited by 77 · see citing works
Liu, W. X., Wang, D., Huang, J., Wei, Y., Xiong, J., Zhu, W., Duan, L., Chen, J., Sun, R., & Wang, D. (2016) · Materials Science and Engineering C · doi:10.1016/j.msec.2016.04.014 · Cited by 71 · see citing works
Park, Y.-J., Cha, S., & Park, Y.-S. (2015) · Stem Cells International · doi:10.1155/2016/9305986 · Cited by 68 · see citing works
Cryopreservation and Banking of Dental Stem Cells
Hilkens, P., Driesen, R. B., Wolfs, E., Gervois, P., Vangansewinkel, T., Ratajczak, J., Dillen, Y., Bronckaers, A., & Lambrichts, I. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-45457-3_17 · Cited by 66 · see citing works
Uth, N., Mueller, J., Smucker, B. J., & Yousefi, A. (2017) · Biofabrication · doi:10.1088/1758-5090/9/1/015023 · Cited by 67 · see citing works
Jensen, J., Kraft, D. C. E., Lysdahl, H., Foldager, C. B., Chen, M., Kristiansen, A. A., Rölfing, J. D., & Bünger, C. E. (2014) · Tissue Engineering Part A · doi:10.1089/ten.tea.2014.0177 · Cited by 63 · see citing works
“Consequently, cell cultures originating from the dental pulp have received increased attention for application in bone tissue engineering.(18,26,27) Our main hypothesis was that functionalizing FDMmanufactured PCL scaffolds with either a TIPS-manufactured PCL compound or a HA/b-TCP coating, would increase the osteogen…”
BackgroundGutiérrez-Quintero, J. G., Riveros, J. Y. D., Valbuena, C. A. M., Alonso, S. P., Niño, J. C. M., & Viafara-García, S. M. (2020) · Oral and Maxillofacial Surgery · doi:10.1007/s10006-020-00862-7 · Cited by 59 · see citing works
Rolph, D. N., Deb, M., Kanji, S., Greene, C. J., Das, M., Joseph, M., Aggarwal, R., Leblebicioğlu, B., & Das, H. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.10.032 · Cited by 54 · see citing works
Polymer-Based Instructive Scaffolds for Endodontic Regeneration
Zein, N., Harmouch, E., Lutz, J., de Grado, G. F., Kuchler-Bopp, S., Clauss, F., Offner, D., Hua, G.-Q., Benkirane-Jessel, N., & Fioretti, F. (2019) · Materials · doi:10.3390/ma12152347 · Cited by 57 · see citing works
“This combination presents a very high porosity and enables adhesion and growth of DPSCs cells, as well as proliferation and pulp-tissue formation [85].”
BackgroundRamamoorthi, M., Bakkar, M., Jordan, J., & Tran, S. D. (2015) · Stem Cells International · doi:10.1155/2015/378368 · Cited by 48 · see citing works
“2014 [143] Human OIM 3D Col/HA/PLCL Micro-CT ALP assay Histochemical staining 30% increase in bone nodule formation and tissue mineralization seen on surface as well inside the scaffold.”
BackgroundMethodInfluentialCytotoxicity of alloying elements and experimental titanium alloys by WST-1 and agar overlay tests
Song, Y.-H., Kim, M.-K., Park, E., Song, H., Anusavice, K. J., & Park, Y.-J. (2014) · Dental Materials · doi:10.1016/j.dental.2014.05.012 · Cited by 48 · see citing works
“[56] Akkouch A, Zhang Z, Rouabhia M.”
MethodInterferon-γ is a master checkpoint regulator of cytokine-induced differentiation
Zha, Z., Bucher, F., Nejatfard, A., Zheng, T., Zhang, H., Yea, K., & Lerner, R. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706915114 · Cited by 48 · see citing works
Lee, S. H., Jeon, S., Qu, X., Kang, M. S., Lee, J. H., Han, D.-W., & Hong, S. W. (2022) · Nano Convergence · doi:10.1186/s40580-022-00329-3 · Cited by 39 · see citing works
Khojasteh, A. (2015) · World Journal of Stem Cells · doi:10.4252/wjsc.v7.i10.1215 · Cited by 39 · see citing works
Rather, H. A., Patel, R. P., Yadav, U. C. S., & Vasita, R. (2020) · Biomedical Materials · doi:10.1088/1748-605x/ab7978 · Cited by 32 · see citing works
Duan, R., Wang, Y., Zhang, Y., Wang, Z., Du, F., Du, B., Su, D., Liu, L., Li, X., & Zhang, Q. (2021) · ACS Omega · doi:10.1021/acsomega.1c02190 · Cited by 31 · see citing works
Ferjaoui, Z., López‐Muñoz, R., Akbari, S., Chandad, F., Mantovani, D., Rouabhia, M., & Fanganiello, R. D. (2024) · Biomedicines · doi:10.3390/biomedicines12071510 · Cited by 30 · see citing works
Self-citationDevelopment and evaluation of cross-linked collagen-hydroxyapatite scaffolds for tissue engineering
Panda, N. N., Jonnalagadda, S., & Pramanik, K. (2013) · Journal of Biomaterials Science Polymer Edition · doi:10.1080/09205063.2013.822247 · Cited by 30 · see citing works
Doğan, A., Demirci, S., Abdik, H., Abdik, E. A., & Şahi̇n, F. (2017) · Tissue and Cell · doi:10.1016/j.tice.2017.10.003 · Cited by 27 · see citing works
Dong, Z., Yang, Q., Mei, M., Liu, L., Sun, J., Li, Z., & Zhou, C. (2018) · Composites Part B Engineering · doi:10.1016/j.compositesb.2018.02.009 · Cited by 27 · see citing works
Moghadam, B. B., Shirian, S., Mirzaei, E., Sharifi, S., Karimi, I., Gharati, G., Takallu, S., & Nazari, H. (2021) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34867 · Cited by 24 · see citing works
The Use of Adipose Tissue-Derived Progenitors in Bone Tissue Engineering - a Review
Bhattacharya, I., Ghayor, C., & Weber, F. E. (2016) · Transfusion Medicine and Hemotherapy · doi:10.1159/000447494 · Cited by 24 · see citing works
AbdulQader, S. T., Rahman, I. A., Thirumulu, K., Ismail, H., & Mahmood, Z. (2016) · Journal of Biomaterials Applications · doi:10.1177/0885328215625759 · Cited by 23 · see citing works
“ALP is a common marker for osteogenic and odontogenic differentiation of human dental pulp stem cells.(57) The differentiated odontoblasts shows much higher ALP activity than dental undifferentiated mesenchymal cells.”
BackgroundTilki, E. K., Öztürk, A. A., Engür, S., & Dikmen, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-70791-y · Cited by 22 · see citing works
Application of dental stem cells in three-dimensional tissue regeneration
Hsiao, H., Nien, C.-Y., Hong, H., Cheng, M., & Yen, T. (2021) · World Journal of Stem Cells · doi:10.4252/wjsc.v13.i11.1610 · Cited by 20 · see citing works
The Use of Lactide Polymers in Bone Tissue Regeneration in Dentistry—A Systematic Review
Rajewska, J., Kowalski, J., Matys, J., Dobrzyński, M., & Wiglusz, R. J. (2023) · Journal of Functional Biomaterials · doi:10.3390/jfb14020083 · Cited by 20 · see citing works
Chakrabarti, S., Ren, J., & Wu, J. (2020) · Nutrients · doi:10.3390/nu12102998 · Cited by 19 · see citing works
Dental pulp stem cells in neuroregeneration
Mohan, S., & Ramalingam, M. (2020) · Journal of Pharmacy And Bioallied Sciences · doi:10.4103/jpbs.jpbs_229_20 · Cited by 18 · see citing works
“DPSC which is of neural crest origin have neural factors inherently and also proven to be one of the best resources for the regeneration of neuronal tissues.[24] DPSC has shown neuroprotective effect in degenerative disease such as Parkinson’s disease and Alzheimers disease.”
BackgroundGamie, Z., MacFarlane, R. J., Tomkinson, A., Moniakis, A., Tran, G. T., Gamie, Y., Mantalaris, A., & Tsiridis, E. E. (2014) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2014.945414 · Cited by 17 · see citing works
Duan, R., Wang, Y., Su, D., Wang, Z., Zhang, Y., Du, B., Liu, L., Li, X., & Zhang, Q. (2022) · Biomaterials Advances · doi:10.1016/j.bioadv.2022.212948 · Cited by 16 · see citing works
Gu, Y., Zhuang, R., Xie, X., & Bai, Y. (2019) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34512 · Cited by 15 · see citing works
Abuarqoub, D. A., Theeb, L. S., Omari, M. B., Hamadneh, Y. I., Alrawabdeh, J. A., Aslam, N., Jafar, H. D., & Awidi, A. (2023) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-022-00514-9 · Cited by 15 · see citing works
Sol-gel for delivery of molecules, its method of preparation and recent applications in medicine
Waqar, M. A., Mubarak, N., Khan, A. M., Khan, R., Khan, I. N., Riaz, M., Ahsan, A., & Munir, M. (2024) · Polymer-Plastics Technology and Materials · doi:10.1080/25740881.2024.2346331 · Cited by 17 · see citing works
“[115] uncovered the job of collagen layers in sidelong onlay unites in canines when joined with ox-like hydroxyapatite particles blended in with collagen networks.”
BackgroundLaothumthut, T., Jantarat, J., Paemanee, A., Roytrakul, S., & CHUNHABUNDIT, P. (2014) · Clinical Oral Investigations · doi:10.1007/s00784-014-1256-8 · Cited by 11 · see citing works
Aghali, A., & Arman, H. E. (2020) · Regenerative Medicine · doi:10.2217/rme-2020-0061 · Cited by 10 · see citing works
Ferjaoui, Z., López‐Muñoz, R., Akbari, S., Chandad, F., Mantovani, D., Rouabhia, M., & Fanganiello, R. D. (2024) · Preprints.org · doi:10.20944/preprints202403.1674.v1 · Cited by 10 · see citing works
Self-citationMudhafar, M., Alsailawi, H. A., Zainol, I., HAMZAH, M. S., DHAHI, S. J., & Mohammed, R. K. (2022) · International Journal of Applied Pharmaceutics · doi:10.22159/ijap.2022v14i4.44411 · Cited by 9 · see citing works
DPSC colonization of functionalized 3D textiles
Ortiz, M., Rosales‐Ibáñez, R., Pozos‐Guillén, A., de Bien, C., Toye, D., Flores, H., & Grandfils, C. (2016) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.33609 · Cited by 9 · see citing works
“The use of a degradable scaffold to support cell regeneration i) provides structural support to animal cells, which are typically anchorage dependent, ii) maintains a controlled-volume physical environment where cells can easily migrate, adhere, and grow according to a preformed architecture, iii) guarantees, during t…”
BackgroundEl‐Naggar, N. E., Sarhan, E., Ibrahim, A. A., Abo-Elwafa, A. H., Yahia, A. M., Salah, A., Maher, R. M., Wagdy, M., El-Sherbeny, G. A., & El-Sawah, A. A. (2025) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.139244 · Cited by 8 · see citing works
Application of PLCL as a biodegradable polymer in biomedical engineering
Zhao, Y., & Liu, H. (2026) · Journal of Materials Science Materials in Medicine · doi:10.1007/s10856-026-07016-3 · Cited by 7 · see citing works
Al‐Rawee, R. Y., Tawfeeq, B. A.-G., Hamodat, A. M., & Tawfek, Z. S. (2023) · Archives of Plastic Surgery · doi:10.1055/a-2113-3084 · Cited by 6 · see citing works
Seciu‐Grama, A., Crăciunescu, O., & Zărnescu, O. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.78048 · Cited by 6 · see citing works
Dental pulp stem cells and banking of teeth as a lifesaving therapeutic vista
Anil, S., Ramadoss, R., Thomas, N. G., GEORGE, J. M., & Sweety, V. K. (2022) · Biocell · doi:10.32604/biocell.2023.024334 · Cited by 5 · see citing works
Li, Q., Zhang, H., Liu, X., Li, Z., Zhang, S., Jin, H., Zhang, S., Wang, X., Jiang, J., & Hou, J. (2024) · Polymer · doi:10.1016/j.polymer.2024.127346 · Cited by 5 · see citing works
Recent Approaches to Enhance Osteogenesis of Dental Pulp Stem Cells on Electrospun Scaffolds
Safari, Z., Aghili, S. S., Hassantash, S., Iranmanesh, E., Abouali, M., Bagherianlemraski, M., Ghasemzadeh, S., Dadgar, E., Barati, G., & Saburi, E. (2023) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x18666230530153521 · Cited by 4 · see citing works
Lafzi, A., Saravi, N. V., Amid, R., Kadkhodazadeh, M., & Shojaei, N. (2022) · Journal of Indian Society of Periodontology · doi:10.4103/jisp.jisp_739_20 · Cited by 3 · see citing works
“[17-19] According to the results, the presence of a scaffold causes a remarkable difference in the rate of mineralization; Nevertheless, there was a remarkable difference in the rate of mineralization between different scaffolds.”
Development of bioceramic bone scaffolds by introducing triple liquid phases
Shuai, C., Duan, S., Wu, P., Gao, D., Feng, P., Gao, C., & Peng, S. (2016) · Journal of materials research/Pratt's guide to venture capital sources · doi:10.1557/jmr.2016.356 · Cited by 3 · see citing works
New Bioinspired Materials for Regenerative Medicine
Hege, C. S., & Schiller, S. (2015) · Current Molecular Biology Reports · doi:10.1007/s40610-015-0015-1 · Cited by 3 · see citing works
Favi, P. M., Dhar, M. S., Neilson, N., & Benson, R. S. (2014) · MRS Proceedings · doi:10.1557/opl.2014.287 · Cited by 2 · see citing works
Comparing Three Different Three-dimensional Scaffolds for Bone Tissue Engineering: An in vivo Study
Nosouhian, S., Davoudi, A., Rismanchian, M., Razavi, S. M., & Sadeghiyan, H. (2015) · The Journal of Contemporary Dental Practice · doi:10.5005/jp-journals-10024-1630 · Cited by 2 · see citing works
Dental Stem Cells for Bone Regeneration
Diamanti, E., Petridis, X., Kaparou, A., & Kitraki, E. (2016) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-319-33299-4_11 · Cited by 1 · see citing works
Stem cells from oral and maxillofacial tissues
Tahriri, M., Bader, R., Khoshroo, K., Rasoulianboroujeni, M., & Tayebi, L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-08-100961-1.00011-6
How has Tooth Manipulation been Conducted for Dental Pulp Stem Cells Isolation? A Scoping Review
Ferrúa, C. P., do Amaral, C. C., Giorgi, R., Garcia, T. F., & Nedel, F. (2018) · International Journal of Experimental Dental Science · doi:10.5005/jp-journals-10029-1182
Sivadas, V. P., Rahul, D. P., & Nair, P. D. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821085-7.00005-1
Li, Q., Zhang, H., Liu, X., Li, Z., Zhang, S., Jin, H., Zhang, S., Wang, X., Jiang, J., & Hou, J. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4762381
Wang, X., Zhang, S., Li, J., Qiao, M., Liu, X., Zou, Z., Zhang, N., Lv, Y., Jiang, J., Han, W., et al. (2025) · Polymer Engineering and Science · doi:10.1002/pen.27237
Lee, S. H., Jeon, S., Qu, X., Kang, M. S., Lee, J. H., Han, D.-W., & Hong, S. W. (2022) · Figshare · doi:10.6084/m9.figshare.20688615
Tooth Regeneration via the Scaffold–Cell–Growth Factor Triad: An Evolution in Regenerative Dentistry
Gould, M. L., Ratnayake, J. T., & Cooper, P. R. (2026) · Biologics · doi:10.3390/biologics6030022
“These mechanical properties can be enhanced by combining the hybrid scaffolds with β -TCP/polyethene [77] or hydroxyapatite [78].”
- Authors
- Akkouch, A., Zhang, Z., & Rouabhia, M.
- Affiliations
- Hôpital Saint-François d'Assise (CA)
- Université Laval (CA)
- Corresponding author
- Rouabhia, Mahmoud
- Venue
- Journal of Biomaterials Applications
- Publisher
- SAGE Publications
- Published
- 2013-05-02
- Volume
- 28
- Issue
- 6
- Pages
- 922-936
- ISSN
- 0885-3282 (ISSN-L)
- 1530-8022
- OpenAlex
- W1969122374
- Cited by
- 76
- References
- 40
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 6 · 2023: 4 · 2022: 6 · 2021: 5 · 2020: 6 · 2019: 4 · 2018: 8 · 2017: 5 · 2016: 11 · 2015: 7 · 2014: 8 · 2013: 2
- FWCI
- 5.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Biomaterials Applications (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Keywords
- bone tissue engineering, dental pulp stem cells, osteogenic differentiation, collagen, hydroxyapatite, poly(L-lactide-co-ε-caprolactone), composite scaffolds, osteoblast-like cells, bone regeneration, porous scaffolds, alkaline phosphatase
- MeSH terms
- Alkaline Phosphatase, Base Sequence, Bone Development, Collagen, Dental Pulp, Humans, Microscopy, Electron, Scanning, Polyesters, Stem Cells, Durapatite, DNA Primers, Tissue Engineering, Tissue Scaffolds, X-Ray Microtomography, Real-Time Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
