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Influence of the Changes in the Bone Mineral Density on the Guided Bone Regeneration Using Bioinspired Grafts: A Systematic Review and Meta-analysis

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Abstract

Nowadays, developing bone tissue grafts is the key to regenerative medicine. Different materials like hydroxyapatite (HAp) have been proven to guide bone regeneration. However, their design is still lacking since most do not consider the patient's requirements. HAps can be synthetic or natural, and their Ca/P ratio varies depending on the reagents for the synthesis and the biological sources. Usually, synthetic HAps are designed to have a 1.67 Ca/P ratio, but Ca/P and Mg/P ratios naturally change throughout life for different reasons, such as age, gender, lifestyle, genetics, physical activity, body weight, and diet, accompanied by changes in bone mineral density (BMD) and bone mineral content (BMC). Until now, there is not enough information about mammal bone changes based on these ratios, BMD, BMC at different life stages, and people's gender. To face this lack of knowledge, animal models such as rats can be used to identify requirements for proper bone grafting materials based on life stages since they consider the age range and gender. Findings indicate that BMD, BMC, Ca/P, and Mg/P change as a function of the age and gender of rats. Thus, it suggests that the grafts need a personalized development considering these parameters.

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References

  1. S.M. Londoño-Restrepo, R. Jeronimo-Cruz, B.M. Millán-Malo, E.M. Rivera-Muñoz, M.E. Rodriguez-García, Effect of the nano crystal size on the X-ray diffraction patterns of biogenic hydroxyapatite from human, bovine, and porcine bones. Sci. Rep. (2019). https://doi.org/10.1038/s41598-019-42269-9

    Article  Google Scholar 

  2. A.M. Castillo-Paz, S.M. Londoño-Restrepo, L. Tirado-Mejía, M.A. Mondragón, M.E. Rodríguez-García, Nano to micro size transition of hydroxyapatite in porcine bone during heat treatment with low heating rates. Prog. Nat. Sci. (2020). https://doi.org/10.1016/j.pnsc.2020.06.005

    Article  Google Scholar 

  3. L. Taha, M. Sievert, F. Eisenhut, H. Iro, M. Traxdorf, S.K. Müller, A complex fracture of the hyoid bone and the larynx after a bicycle accident—case report and review of literature. Int. J. Surg. Case Rep. (2021). https://doi.org/10.1016/j.ijscr.2021.105922

    Article  Google Scholar 

  4. H. Wei, J. Cui, K. Lin, J. Xie, X. Wang, Recent advances in smart stimuli-responsive biomaterials for bone therapeutics and regeneration. Bone Res. (2022). https://doi.org/10.1038/s41413-021-00180-y

    Article  Google Scholar 

  5. R. Zhao, R. Yang, P.R. Cooper, Z. Khurshid, A. Shavandi, J. Ratnayake, Bone grafts and substitutes in dentistry: a review of current trends and developments. Molecules (2021). https://doi.org/10.3390/molecules26103007

    Article  Google Scholar 

  6. A.M. Castillo-Paz, S.M. Londoño-Restrepo, C. Ortiz-Echeverri, R. Ramirez-Bon, M.E. Rodriguez-García, Physicochemical properties of 3D bovine natural scaffolds as a function of the anterior-posterior, lateral and superior-inferior directions. Materialia (2021). https://doi.org/10.1016/j.mtla.2021.101100

    Article  Google Scholar 

  7. N. Kantharia, S. Naik, S. Apte, M. Kheur, S. Kheur, B. Kale, Nano-hydroxyapatite and its contemporary applications. Bone (2014). https://doi.org/10.4103/2348-3407.126135

    Article  Google Scholar 

  8. M. Sadat-Shojai, M.T. Khorasani, E. Dinpanah-Khoshdargi, A. Jamshidi, Synthesis methods for nanosized hydroxyapatite with diverse structures. Acta Biomater. (2013). https://doi.org/10.1016/j.actbio.2013.04.012

    Article  Google Scholar 

  9. L.F. Zubieta-Otero, S.M. Londoño-Restrepo, G. Lopez-Chavez, E. Hernandez-Becerra, M.E. Rodriguez-Garcia, Comparative study of physicochemical properties of bio-hydroxyapatite with commercial samples. Mater. Chem. Phys. (2021). https://doi.org/10.1016/j.matchemphys.2020.124201

    Article  Google Scholar 

  10. D. Masztalerz-Kozubek, M.A. Zielinska-Pukos, J. Hamulka, Maternal diet, nutritional status, and birth-related factors influencing offspring’s bone mineral density: a narrative review of observational, cohort, and randomized controlled trials. Nutrients (2021). https://doi.org/10.3390/nu13072302

    Article  Google Scholar 

  11. D.G.D. Christofaro, W.R. Tebar, B.T.C. Saraiva, G.C.R. da Silva, A.B. Dos Santos, G.I. Mielke, R.M. Ritti-Dias, J. Mota, Comparison of bone mineral density according to domains of sedentary behavior in children and adolescents. BMC Pediatr. (2022). https://doi.org/10.1186/s12887-022-03135-2

    Article  Google Scholar 

  12. D.G. Whitney, M.S. Caird, G.A. Clines, E.A. Hurvitz, K.J. Jepsen, Clinical bone health among adults with cerebral palsy: moving beyond assessing bone mineral density alone. Dev. Med. Child. Neurol. (2022). https://doi.org/10.1111/dmcn.15093

    Article  Google Scholar 

  13. S. Iuliano, T.R. Hill, Dairy foods and bone accrual during growth and development, in Milk and dairy foods. ed. by D.I. Givens (Academic Press, London, 2020), pp.299–322

    Chapter  Google Scholar 

  14. E. Hernandez-Becerra, S.M. Londoño-Restrepo, M.I. Hernández-Urbiola, D. Jimenez-Mendoza, M.D.L.Á. Aguilera-Barreiro, E. Perez-Torrero, M.E. Rodríguez-García, Determination of basal bone mineral density in the femur bones of male and female Wistar rats. Lab. Anim. (2021). https://doi.org/10.1177/0023677220922566

    Article  Google Scholar 

  15. E. Hernandez-Becerra, M. Mendoza-Avila, D. Jiménez-Mendoza, E. Gutierrez-Cortez, M.E. Rodríguez-García, I. Rojas-Molina, Effect of Nopal (Opuntia ficus indica) consumption at different maturity stages as an only calcium source on bone mineral metabolism in growing rats. Biol. Trace Elem. Res. (2020). https://doi.org/10.1007/s12011-019-01752-0

    Article  Google Scholar 

  16. E.F. Kranioti, A. Bonicelli, J.G. García-Donas, Bone-mineral density: clinical significance, methods of quantification and forensic applications. Res. Rep. Forensic Med. Sci. (2019). https://doi.org/10.2147/RRFMS.S164933

    Article  Google Scholar 

  17. P. Mukherjee, S. Roy, D. Ghosh, S.K. Nandi, Role of animal models in biomedical research: a review. Lab. Anim. Res. (2022). https://doi.org/10.1186/s42826-022-00128-1

    Article  Google Scholar 

  18. J. Lee, S. Lee, S. Jang, O.H. Ryu, Age-related changes in the prevalence of osteoporosis according to gender and skeletal site: the Korea National Health and Nutrition Examination Survey 2008–2010. Endocrinol. Metab. (2013). https://doi.org/10.3803/EnM.2013.28.3.180

    Article  Google Scholar 

  19. I. Groenendijk, M. van Delft, P. Versloot, L.J. van Loon, L.C. de Groot, Impact of magnesium on bone health in older adults: a systematic review and meta-analysis. Bone (2022). https://doi.org/10.1016/j.bone.2021.116233

    Article  Google Scholar 

  20. E. O’Neill, G. Awale, L. Daneshmandi, O. Umerah, K.W.-H. Lo, The roles of ions on bone regeneration. Drug Discov. Today (2018). https://doi.org/10.1016/j.drudis.2018.01.049

    Article  Google Scholar 

  21. C.M. Weaver, E.M. Haney, Nutritional basis of skeletal growth, in Osteoporosis in Men, 2nd edn., ed. by E.S. Orwoll, J.P. Bilezikian, D. Vanderschueren (Academic Press, London, 2010), pp.119–129

    Chapter  Google Scholar 

  22. A.M. Weatherholt, R.K. Fuchs, S.J. Warden, Specialized connective tissue: bone, the structural framework of the upper extremity. J. Hand Ther. (2012). https://doi.org/10.1016/j.jht.2011.08.003

    Article  Google Scholar 

  23. A.P. Mamede, A.R. Vassalo, E. Cunha, D. Gonçalves, S.F. Parker, L.A.E.B. De Carvalho, M.P.M. Marques, Biomaterials from human bone—probing organic fraction removal by chemical and enzymatic methods. RSC Adv. (2018). https://doi.org/10.1039/C8RA05660A

    Article  Google Scholar 

  24. U. Kini, B.N. Nandeesh, Physiology of bone formation, remodeling, and metabolism, in Radionuclide and Hybrid Bone Imaging. ed. by I. Fogelman, G. Gnanasegaran, H. Wall (Springer, Heidelberg, 2010), pp.29–57

    Google Scholar 

  25. H. Qu, H. Fu, Z. Han, Y. Sun, Biomaterials for bone tissue engineering scaffolds: a review. RSC Adv. (2019). https://doi.org/10.1039/C9RA05214C

    Article  Google Scholar 

  26. S.M. Londoño-Restrepo, C.F. Ramirez-Gutierrez, H. Villarraga-Gómez, M.E. Rodriguez-García, Study of microstructural, structural, mechanical, and vibrational properties of defatted trabecular bovine bones: natural sponges, in Materials for Biomedical Engineering. ed. by A.-M. Holban, A. Mihai (Elsevier, Amsterdam, 2019), pp.441–485

    Chapter  Google Scholar 

  27. R. Karpiński, Ł. Jaworski, P. Czubacka, The structural and mechanical properties of the bone. J. Technol. Exploit. Mech. Eng. (2017). https://doi.org/10.35784/jteme.538

  28. K. Phan, V. Ramachandran, T. M. Tran, K.P. Shah, M. Fadhil, A. Lackey, N. Chang, A.-M. Wu, R. J. Mobbs, Systematic review of cortical bone trajectory versus pedicle screw techniques for lumbosacral spine fusion. J. Spine Surg. (2017). https://doi.org/10.21037/jss.2017.11.03

  29. P. Augat, S. Schorlemmer, The role of cortical bone and its microstructure in bone strength. Age Ageing (2006). https://doi.org/10.1093/ageing/afl081

    Article  Google Scholar 

  30. N. Eliaz, N. Metoki, Calcium phosphate bioceramics: a review of their history, structure, properties, coating technologies and biomedical applications. Materials (2017). https://doi.org/10.3390/ma10040334

    Article  Google Scholar 

  31. J. Wang, B. Zhou, X.S. Liu, A.J. Fields, A. Sanyal, X. Shi, M. Adams, T.M. Keaveny, X.E. Guo, Trabecular plates and rods determine elastic modulus and yield strength of human trabecular bone. Bone (2015). https://doi.org/10.1016/j.bone.2014.11.006

    Article  Google Scholar 

  32. H. Chen, X. Zhou, H. Fujita, M. Onozuka, K.Y. Kubo, Age-related changes in trabecular and cortical bone microstructure. Int. J. Endocrinol. (2013). https://doi.org/10.1155/2013/213234

    Article  Google Scholar 

  33. A.F. Khan, M. Awais, A.S. Khan, S. Tabassum, A.A. Chaudhry, I.U. Rehman, Raman spectroscopy of natural bone and synthetic apatites. Appl. Spectrosc. Rev. (2013). https://doi.org/10.1080/05704928.2012.721107

    Article  Google Scholar 

  34. A.K. Nair, A. Gautieri, S.W. Chang, M.J. Buehler, Molecular mechanics of mineralized collagen fibrils in bone. Nat. Commun. (2013). https://doi.org/10.1038/ncomms2720

    Article  Google Scholar 

  35. J.P. Bonjour, Calcium and phosphate: a duet of ions playing for bone health. J. Am. Coll. Nutr. (2011). https://doi.org/10.1080/07315724.2011.10719988

    Article  Google Scholar 

  36. S.M.T. Gharibzahedi, S.M. Jafari, The importance of minerals in human nutrition: bioavailability, food fortification, processing effects and nanoencapsulation. Trends Food Sci. Technol. (2017). https://doi.org/10.1016/j.tifs.2017.02.017

    Article  Google Scholar 

  37. R. Masuyama, Y. Nakaya, S. Katsumata, Y. Kajita, M. Uehara, S. Tanaka, A. Sakai, S. Kato, T. Nakamura, K. Suzuki, Dietary calcium and phosphorus ratio regulates bone mineralization and turnover in vitamin D receptor knockout mice by affecting intestinal calcium and phosphorus absorption. J. Bone Miner. Res. (2003). https://doi.org/10.1359/jbmr.2003.18.7.1217

    Article  Google Scholar 

  38. I. Groenendijk, M. van Delft, P. Versloot, L.J.C. van Loon, L.C.P.G.M. de Groot, Impact of magnesium on bone health in older adults: a systematic review and meta-analysis. Bone (2022). https://doi.org/10.1016/j.bone.2021.116233

  39. M.M. Belluci, R.S. de Molon, C. Rossa Jr., S. Tetradis, G. Giro, P.S. Cerri, E. Marcantonio Jr., S.R.P. Orrico, Severe magnesium deficiency compromises systemic bone mineral density and aggravates inflammatory bone resorption. J. Nutr. Biochem. (2020). https://doi.org/10.1016/j.jnutbio.2019.108301

    Article  Google Scholar 

  40. O.M. Gomez-Vazquez, B.A. Correa-Piña, L.F. Zubieta-Otero, A.M. Castillo-Paz, S.M. Londoño-Restrepo, M.E. Rodriguez-García, Synthesis and characterization of bioinspired nano-hydroxyapatite by wet chemical precipitation. Ceram. Int. (2021). https://doi.org/10.1016/j.ceramint.2021.08.174

    Article  Google Scholar 

  41. G. Skiba, S. Raj, M. Sobol, P. Kowalczyk, M. Barszcz, M. Taciak, E.R. Grela, Influence of the zinc and fibre addition in the diet on biomechanical bone properties in weaned piglets. Animals (2022). https://doi.org/10.3390/ani12020181

    Article  Google Scholar 

  42. N.J. Lakhkar, I. Lee, H. Kim, V. Salih, I.B. Wall, J.C. Knowles, Bone formation controlled by biologically relevant inorganic ions: role and controlled delivery from phosphate-based glasses. Adv. Drug Deliv. Rev. (2013). https://doi.org/10.1016/j.addr.2012.05.015

    Article  Google Scholar 

  43. S.M. Londoño-Restrepo, R. Jeronimo-Cruz, E. Rubio-Rosas, M.E. Rodriguez-García, The effect of cyclic heat treatment on the physicochemical properties of bio hydroxyapatite from bovine bone. J. Mater. Sci. (2018). https://doi.org/10.1007/s10856-018-6061-5

    Article  Google Scholar 

  44. B.S. Zemel, H.J. Kalkwarf, V. Gilsanz, J.M. Lappe, S. Oberfield, J.A. Shepherd, M.M. Frederick, X. Huang, M. Lu, S. Mahboubi, T. Hangartner, K.K. Winer, Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the bone mineral density in childhood study. J. Clin. Endocrinol. Metab. (2011). https://doi.org/10.1210/jc.2011-1111

    Article  Google Scholar 

  45. E.J. Castillo, S.M. Croft, J.M. Jiron, J.I. Aguirre, Bone structural, biomechanical, and histomorphometric characteristics of the hindlimb skeleton in the marsh rice rat (Oryzomys palustris). Anat. Rec. (2022). https://doi.org/10.1002/ar.24876

    Article  Google Scholar 

  46. J. Banu, L. Wang, D.N. Kalu, Age-related changes in bone mineral content and density in intact male F344 rats. Bone (2002). https://doi.org/10.1016/s8756-3282(01)00636-6

    Article  Google Scholar 

  47. K. Burrow, W. Young, N. Hammer, S. Safavi, M. Scholze, M. McConnell, A. Carne, D. Barr, M. Reid, A.E.D. Bekhit, The Effect of the supplementation of a diet low in calcium and phosphorus with either sheep milk or cow milk on the physical and mechanical characteristics of bone using a rat model. Foods (2020). https://doi.org/10.3390/foods9081070

    Article  Google Scholar 

  48. M. Bournazel, M.J. Duclos, F. Lecompte, D. Guillou, C. Peyronnet, A. Quinsac, N. Même, A. Narcy, Effects of dietary electrolyte balance and calcium supply on mineral and acid–base status of piglets fed a diversified diet. J. Nutr. Sci. (2020). https://doi.org/10.1017/jns.2020.10

    Article  Google Scholar 

  49. M.A. Gani, A.S. Budiatin, M.L.A.D. Lestari, F.A. Rantam, C. Ardianto, J. Khotib, Fabrication and characterization of submicron-scale bovine hydroxyapatite: a top-down approach for a natural biomaterial. Materials (2022). https://doi.org/10.3390/ma15062324

    Article  Google Scholar 

  50. S. Luthfiyah, B. Soegijono, F.B. Susetyo, H.A. Notonegoro, Comparing properties of bovine bone derived hydroxyapatite and synthetic hydroxyapatite. J. Appl. Sci. Eng. (2022). https://doi.org/10.6180/jase.202212_25(6).0015

    Article  Google Scholar 

  51. A. Arifin, I. Yani, S.D. Arian, The fabrication porous hydroxyapatite scaffold using sweet potato starch as a natural space holder. J. Phys. Conf. Ser. (2019). https://doi.org/10.1088/1742-6596/1198/4/042020

    Article  Google Scholar 

  52. S.M. Londoño-Restrepo, B.M. Millán-Malo, A. del Real-López, M.E. Rodriguez-García, In situ study of hydroxyapatite from cattle during a controlled calcination process using HT-XRD. Mater. Sci. Eng. C (2019). https://doi.org/10.1016/j.msec.2019.110020

    Article  Google Scholar 

  53. Q.P. Ho, L.H. Huynh, M.J. Wang, Biocomposite scaffold preparation from hydroxyapatite extracted from waste bovine bone. Green Process. Synth. (2020). https://doi.org/10.1515/gps-2020-0005

    Article  Google Scholar 

  54. R. Murugan, T.S. Kumar, K.P. Rao, Fluorinated bovine hydroxyapatite: preparation and characterization. Mater. Lett. (2002). https://doi.org/10.1016/S0167-577X(02)00805-4

    Article  Google Scholar 

  55. G.A. Clavijo-Mejía, J.A. Hermann-Muñoz, J.A. Rincón-López, H. Ageorges, J. Muñoz-Saldaña, Bovine-derived hydroxyapatite coatings deposited by high-velocity oxygen-fuel and atmospheric plasma spray processes: a comparative study. Surf. Coat. Technol. (2020). https://doi.org/10.1016/j.surfcoat.2019.125193

    Article  Google Scholar 

  56. S. Yamada, M. Onuma, M. Todoh, S. Tadano, Changes of residual stress, diaphyseal size, and micro-nano structure in bovine femurs during growth and maturation. J. Biomech. Sci. Eng. (2018). https://doi.org/10.1299/jbse.18-00110

    Article  Google Scholar 

  57. T. Nakatsuji, K. Yamamoto, D. Suga, T. Yanagitani, M. Matsukawa, K. Yamazaki, Y. Matsuyama, Three-dimensional anisotropy of ultrasonic wave velocity in bovine cortical bone: effects of hydroxyapatite crystallites orientation and microstructure. Jpn. J. Appl. Phys. (2011). https://doi.org/10.1143/JJAP.50.07HF18

    Article  Google Scholar 

  58. C.F. Ramirez-Gutierrez, S.M. Londoño-Restrepo, A. Del Real, M.A. Mondragón, M.E. Rodriguez-García, Effect of the temperature and sintering time on the thermal, structural, morphological, and vibrational properties of hydroxyapatite derived from pig bone. Ceram. Int. (2017). https://doi.org/10.1016/j.ceramint.2017.03.046

    Article  Google Scholar 

  59. E.A. Ofudje, A. Rajendran, A.I. Adeogun, M.A. Idowu, S.O. Kareem, D.K. Pattanayak, Synthesis of organic derived hydroxyapatite scaffold from pig bone waste for tissue engineering applications. Adv. Powder Technol. (2018). https://doi.org/10.1016/j.apt.2017.09.008

    Article  Google Scholar 

  60. B.A. Correa-Piña, O.M. Gomez-Vazquez, S.M. Londoño-Restrepo, L.F. Zubieta-Otero, B.M. Millan-Malo, M.E. Rodriguez-García, Synthesis and characterization of nano-hydroxyapatite added with magnesium obtained by wet chemical precipitation. Prog. Nat. Sci. (2021). https://doi.org/10.1016/j.pnsc.2021.06.006

    Article  Google Scholar 

  61. Y. Oku, S. Noda, A. Yamada, K. Nakaoka, M. Goseki-Sone, Twenty-eight days of vitamin D restriction and/or a high-fat diet influenced bone mineral density and body composition in young adult female rats. Ann. Anat. (2022). https://doi.org/10.1016/j.aanat.2022.151945

    Article  Google Scholar 

  62. Y. Oku, R. Tanabe, K. Nakaoka, A. Yamada, S. Noda, A. Hoshino, M. Haraikawa, M. Goseki-Sone, Influences of dietary vitamin D restriction on bone strength, body composition and muscle in rats fed a high-fat diet: involvement of mRNA expression of MyoD in skeletal muscle. J. Nutr. Biochem. (2016). https://doi.org/10.1016/j.jnutbio.2016.01.013

    Article  Google Scholar 

  63. A. Pelegrini, M.A. Bim, A.D. Alves, K.S. Scarabelot, G.S. Claumann, R.A. Fernandes, H.C.C. de Angelo, A. de Araújo Pinto, Relationship between muscle strength, body composition and bone mineral density in adolescents. J. Clin. Densitom. (2022). https://doi.org/10.1016/j.jocd.2021.09.001

    Article  Google Scholar 

  64. K.L. Cobb, L.K. Bachrach, G. Greendale, R. Marcus, R.M. Neer, J. Nieves, M.F. Sower, B.W. Brown, G. Gopalakrishnan, C. Luetters, H.K. Tanner, B. Ward, J.L. Kelsey, Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med. Sci. Sports Exerc. (2003). https://doi.org/10.1249/01.MSS.0000064935.68277.E7

    Article  Google Scholar 

  65. I.R. Hwang, Y.K. Choi, W.K. Lee, J.G. Kim, I.K. Lee, S.W. Kim, K.G. Park, Association between prolonged breastfeeding and bone mineral density and osteoporosis in postmenopausal women: KNHANES 2010–2011. Osteoporos. Int. (2016). https://doi.org/10.1007/s00198-015-3292-x

    Article  Google Scholar 

  66. D. Lopez-Gonzalez, J.C. Wells, M. Cortina-Borja, M. Fewtrell, A. Partida-Gaytán, P. Clark, Reference values for bone mineral density in healthy Mexican children and adolescents. Bone (2021). https://doi.org/10.1016/j.bone.2020.115734

    Article  Google Scholar 

  67. U.B. Nwogu, K.K. Agwu, A.M.C. Anakwue, F.U. Idigo, M.C. Okeji, E.O. Abonyi, J.A. Agbo, Bone mineral density in an urban and a rural children population—a comparative, population-based study in Enugu State. Nigeria. Bone (2019). https://doi.org/10.1016/j.bone.2019.05.028

    Article  Google Scholar 

  68. D. Goksen, S. Darcan, M. Coker, T. Kose, Bone mineral density of healthy Turkish children and adolescents. J. Clin. Densitom. (2006). https://doi.org/10.1016/j.jocd.2005.08.001

    Article  Google Scholar 

  69. E. Jáuregui, M. Galvis, V. Moncaleano, K. González, Y. Muñoz, Bone mineral density reference values by DXA scan in a population of healthy adults in Bogota. Rev. Colomb. de Reumatol. (2021). https://doi.org/10.1016/j.rcreue.2020.06.010

    Article  Google Scholar 

  70. A. Khawaja, P. Sabbagh, J. Prioux, G. Zunquin, G. Baquet, G. Maalouf, R. El Hage, Does muscular power predict bone mineral density in young adults? J. Clin. Densitom. (2019). https://doi.org/10.1016/j.jocd.2019.01.005

    Article  Google Scholar 

  71. N. Li, H. Jing, J. Li, F. Zhou, L. Bu, X. Yang, Study of mandible bone mineral density of Chinese adults by dual-energy X-ray absorptiometry. Int. J. Oral Maxillofac. Surg. (2011). https://doi.org/10.1016/j.ijom.2011.05.012

    Article  Google Scholar 

  72. J.S. Finkelstein, S.E. Brockwell, V. Mehta, G.A. Greendale, M.R. Sowers, B. Ettinger, J.C. Lo, J.M. Johnston, J.A. Cauley, M.E. Danielson, R.M. Neer, Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J. Clin. Endocrinol. Metab. (2008). https://doi.org/10.1210/jc.2007-1876

    Article  Google Scholar 

  73. M. Mohseni, S. Eisen, S. Stum, R. Civitelli, The Association of pelvic bone mineral density and with proximal femoral and spine bone mineral density in Post-menopausal women. J. Clin. Densitom. (2022). https://doi.org/10.1016/j.jocd.2022.01.003

    Article  Google Scholar 

  74. P.F. Lei, R.Y. Hu, Y.H. Hu, Bone defects in revision total knee arthroplasty and management. Orthop. Surg. (2019). https://doi.org/10.1111/os.12425

    Article  Google Scholar 

  75. F.J. O’Brien, Biomaterials & scaffolds for tissue engineering. Mater. Today (2011). https://doi.org/10.1016/S1369-7021(11)70058-X

    Article  Google Scholar 

  76. S.Y. Shin, H.F. Rios, W.V. Giannobile, T.J. Oh, Periodontal regeneration: current therapies, in Stem Cell Biology and Tissue Engineering in Dental Sciences. ed. by A. Vishwakarma, P. Sharpe, S. Shi, M. Ramalingam (Academic Press, London, 2015), pp.459–469

    Chapter  Google Scholar 

  77. S. Elad, M. Laryea, N. Yarom, Transplantation medicine, in Burket’s Oral Medicine (13th edn.). ed. by M. Glick, M.S. Greenberg, P.B. Lockhart, S.J. Challacombe (Wiley, PMPH USA, 2021), pp.745–783

    Chapter  Google Scholar 

  78. F.M. Chen, X. Liu, Advancing biomaterials of human origin for tissue engineering. Prog. Polym. Sci. (2016). https://doi.org/10.1016/j.progpolymsci.2015.02.004

    Article  Google Scholar 

  79. S.M. Londoño-Restrepo, C.F. Ramirez-Gutierrez, A. del Real, E. Rubio-Rosas, M.E. Rodriguez-García, Study of bovine hydroxyapatite obtained by calcination at low heating rates and cooled in furnace air. J. Mater. Sci. (2016). https://doi.org/10.1007/s10853-016-9755-4

    Article  Google Scholar 

  80. B.F. Ricciardi, M.P. Bostrom, Bone graft substitutes: claims and credibility. Semin. Arthroplasty (2013). https://doi.org/10.1053/j.sart.2013.07.002

    Article  Google Scholar 

  81. J.R. Jones, I.R. Gibson, Ceramics, glasses, and glass-ceramics: basic principles, in Biomaterials Science. ed. by W.R. Wagner, S.E. Sakiyama-Elbert, G. Zhang, M.J. Yaszemski (Academic Press, London, 2020), pp.289–305

    Chapter  Google Scholar 

  82. S. Sakai, T. Anada, K. Tsuchiya, H. Yamazaki, H.C. Margolis, O. Suzuki, Comparative study on the resorbability and dissolution behavior of octacalcium phosphate, β-tricalcium phosphate, and hydroxyapatite under physiological conditions. Dent. Mater. J. (2016). https://doi.org/10.4012/dmj.2015-255

    Article  Google Scholar 

  83. V.S. Kattimani, P.S. Chakravarthi, N.R. Kanumuru, V.V. Subbarao, A. Sidharthan, T.S. Kumar, L.K. Prasad, Eggshell derived hydroxyapatite as bone graft substitute in the healing of maxillary cystic bone defects: a preliminary report. J. Int. Oral Health. 6(3), 15–19 (2014)

    Google Scholar 

  84. C. Vullo, M. Meligrana, G. Rossi, A.M. Tambella, F. Dini, A.P. Piccionello, A. Spaterna, Use of nanohydroxyapatite in regenerative therapy in dogs affected by periodontopathy: preliminary results. Ann. Clin. Lab. Res. 3(2), 18 (2015)

    Article  Google Scholar 

  85. M.T. Chitsazi, A. Shirmohammadi, M. Faramarzie, R. Pourabbas, A.N. Rostamzadeh, A clinical comparison of nano-crystalline hydroxyapatite (Ostim) and autogenous bone graft in the treatment of periodontal intrabony defects. Med. Oral Patol. Oral Cir. Bucal (2011). https://doi.org/10.4317/medoral.16.e448

    Article  Google Scholar 

  86. M. Bayani, S. Torabi, A. Shahnaz, M. Pourali, Main properties of nanocrystalline hydroxyapatite as a bone graft material in treatment of periodontal defects. A review of literature. Biotechnol. Biotechnol. Equip. (2017). https://doi.org/10.1080/13102818.2017.1281760

    Article  Google Scholar 

  87. M. Ebrahimi, Bone grafting substitutes in dentistry: general criteria for proper selection and successful application. IOSR J. Dent. Med. Sci. (2017). https://doi.org/10.9790/0853-1604037579

    Article  Google Scholar 

  88. A.L. Giraldo-Betancur, D.G. Espinosa-Arbelaez, A. Del Real-López, B.M. Millan-Malo, E.M. Rivera-Muñoz, E. Gutierrez-Cortez, P. Pineda-Gomez, S. Jimenez-Sandoval, M.E. Rodriguez-García, Comparison of physicochemical properties of bio and commercial hydroxyapatite. Curr. Appl. Phys. (2013). https://doi.org/10.1016/j.cap.2013.04.019

    Article  Google Scholar 

  89. U. Tariq, R. Hussain, K. Tufail, Z. Haider, R. Tariq, J. Ali, Injectable dicalcium phosphate bone cement prepared from biphasic calcium phosphate extracted from lamb bone. Mater. Sci. Eng. C (2019). https://doi.org/10.1016/j.msec.2019.109863

    Article  Google Scholar 

  90. H. Nosrati, D.Q.S. Le, R.Z. Emameh, C.E. Bunger, Characterization of the precipitated dicalcium phosphate dehydrate on the graphene oxide surface as a bone cement reinforcement. J. Tissue Mater. (2019). https://doi.org/10.22034/JTM.2019.173565.1013

  91. A. Bow, D.E. Anderson, M. Dhar, Commercially available bone graft substitutes: the impact of origin and processing on graft functionality. Drug Metab. Rev. (2019). https://doi.org/10.1080/03602532.2019.1671860

    Article  Google Scholar 

  92. A. Kadam, P.W. Millhouse, C.K. Kepler, K.E. Radcliff, M.G. Fehlings, M.E. Janssen, R.C. Sasso, J.J. Benedict, A.R. Vaccaro, Bone substitutes and expanders in spine surgery: a review of their fusion efficacies. Int. J. Spine Surg. (2016). https://doi.org/10.14444/3033

  93. N.N. Bembi, S. Bembi, J. Mago, G.K. Baweja, P.S. Baweja, Comparative evaluation of bioactive synthetic NovaBone putty and calcified algae-derived porous hydroxyapatite bone grafts for the treatment of intrabony defects. Int. J. Clin. Pediatr. Dent. (2016). https://doi.org/10.5005/jp-journals-10005-1379

    Article  Google Scholar 

  94. W. Qiao, R. Liu, Z. Li, X. Luo, B. Huang, Q. Liu, Z. Chen, J.K.H. Tsoi, Y.X. Su, K.M.C. Cheung, J.P. Matinlinna, K.W.K. Yeung, Z. Chen, Contribution of the in-situ release of endogenous cations from xenograft bone driven by fluoride incorporation toward enhanced bone regeneration. Biomater. Sci. (2018). https://doi.org/10.1039/C8BM00910D

    Article  Google Scholar 

  95. R. Guarnieri, P. DeVilliers, M. Grande, L.V. Stefanelli, S. Di Carlo, G. Pompa, Histologic evaluation of bone healing of adjacent alveolar sockets grafted with bovine- and porcine-derived bone: a comparative case report in humans. Regener. Biomater. (2017). https://doi.org/10.1093/rb/rbx002

    Article  Google Scholar 

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Acknowledgements

Angelica M. Castillo-Paz, Omar M. Gomez-Vazquez, Brandon A. Correa-Piña, and Luis F. Zubieta-Otero, Harol D. Martinez-Hernandez, Dorian F. Cañon-Davila, want to thank CONACYT-Mexico for the financial support of their postgraduate studies. Sandra M. Londoño-Restrepo thanks CFATA-UNAM for her postdoctoral position. This project was supported by SEP-CONACYT Ciencia Básica 2018 (A1-S-8979) and Project PAPIIT-UNAM (IN114320). English edition by M.B. Carolina Tavares.

Funding

Funding was provided by Consejo Nacional de Ciencia y Tecnología (Grant Number A1S8979) and Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (Grant Number IN114320).

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Authors and Affiliations

  1. Centro de Investigación y de Estudios Avanzados del IPN, Unidad Querétaro, C.P. 76230, Querétaro, QRO, Mexico

    Angelica M. Castillo-Paz & Dorian F. Cañon-Davila

  2. Posgrado en Ciencia e Ingeniería de Materiales, Centro de Física Aplicada y Tecnología Avanzada, Universidad Nacional Autónoma de México, Campus Juriquilla, C.P. 76230, Querétaro, QRO, Mexico

    Brandon A. Correa-Piña, Harol D. Martinez-Hernandez, Omar M. Gomez-Vazquez & Luis F. Zubieta-Otero

  3. Departamento de Nanotecnología, Centro de Física Aplicada y Tecnología Avanzada, Universidad Nacional Autónoma de México, Campus Juriquilla, C.P. 76230, Querétaro, QRO, Mexico

    Sandra M. Londoño-Restrepo & Mario E. Rodriguez-Garcia

  4. Facultad de Ingeniería, Universidad Autónoma de Queretaro, Querétaro, QRO, Mexico

    Esther Perez-Torrero

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  1. Angelica M. Castillo-Paz
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Castillo-Paz, A.M., Correa-Piña, B.A., Martinez-Hernandez, H.D. et al. Influence of the Changes in the Bone Mineral Density on the Guided Bone Regeneration Using Bioinspired Grafts: A Systematic Review and Meta-analysis. Biomedical Materials & Devices 1, 162–178 (2023). https://doi.org/10.1007/s44174-022-00026-z

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