Ir J Med Sci DOI 10.1007/s11845-014-1199-8

REVIEW ARTICLE

Ceramic and non-ceramic hydroxyapatite as a bone graft material: a brief review S. R. Dutta • D. Passi • P. Singh • A. Bhuibhar

Received: 4 May 2014 / Accepted: 2 September 2014 Ó Royal Academy of Medicine in Ireland 2014

Abstract Treatment of dental, craniofacial and orthopedic defects with bone graft substitutes has shown promising result achieving almost complete bone regeneration depending on product resorption similar to human bone’s physicochemical and crystallographic characteristics. Among these, non-ceramic and ceramic hydroxyapatite being the main inorganic salt of bone is the most studied calcium phosphate material in clinical practices ever since 1970s and non-ceramic since 1985. Its ‘‘chemical similarity’’ with the mineralized phase of biologic bone makes it unique. Hydroxyapatite as an excellent carrier of osteoinductive growth factors and osteogenic cell populations is also useful as drug delivery vehicle regardless of its density. Porous ceramic and non-ceramic hydroxyapatite is osteoconductive, biocompatible and very inert. The need for bone graft material keeps on increasing with increased age of the population and the increased conditions of trauma. Recent advances in genetic engineering and doping techniques have made it possible to use non-ceramic

S. R. Dutta (&) Department of Oral and Maxillofacial Surgery, M. B. Kedia Dental College, Tribhuvan University, Chhapkaiya, Birgunj, Nepal e-mail: [email protected] D. Passi Department of Oral and Maxillofacial Surgery, E. S. I. C., Dental College and Hospital, Rohini, Delhi, India P. Singh Department of Physiology, Vyas Dental College and Hospital, Jodhpur, Rajasthan, India A. Bhuibhar Department of Oral and Maxillofacial surgery, Vyas Dental College and Hospital, Jodhpur, Rajasthan, India

hydroxyapatite in larger non-ceramic crystals and cluster forms as a successful bone graft substitute to treat various types of bone defects. In this paper we have mentioned some recently studied properties of hydroxyapatite and its various uses through a brief review of the literatures available to date. Keywords Bone graft substitute  Ceramic hydroxyapatite  Coralline ceramic hydroxyapatite  Bioactive non-ceramic hydroxylapatite  Osteoconductive  Biocompatible

Introduction The extensive acceptance of bone graft materials for orthopedic surgeries involving articular and osseous defects in multitudinous reconstructive procedures depends on its vast availability and immense usefulness [1]. In the past few years the use of bone graft substitutes in the treatment of distal radius fractures has also increased [2–6]. Bone graft materials promote osseous ingrowth and bone healing by providing a non loading structural substrate. Bone grafting provides structural support or augments healing in significant bone defects such as osteoporotic bone and non-union fracture. The bone graft substitutes are based on naturally occurring materials such as demineralized allograft bone matrix, bovine collagen mineral composites, ceramic hydroxyapatite (HA), non-ceramic hydroxylapatite, ceramic-coralline hydroxyapatite (CHA) and synthetic materials such as calcium sulfate pellets, and non-ceramic calcium phosphate pellets bioactive glass, and calcium phosphate cement. Extensive studies in animal model and human patient has been done to evaluate the possible advantages of using bone graft material.

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Fig. 2 HA used in alveolar defects Fig. 1 Structure of HA

Bone graft substitutes Among the several materials starting from gold to allograft used to repair bone defects [7, 8] autologous bone is still considered as the gold standard [9]. However, the use of autologous bone is limited because of high cost. Also it requires a second surgical site resulting in additional pain and complications, and is associated with significant donor site morbidity. The rapid resorption of allograft bone used in the form of fresh-frozen or demineralized freeze dried bone allograft can make it less ideal for some larger defects. Recently xenograft materials have also been used successfully as bone graft substitutes [7, 10–13]. Ceramic Bovine bone derivative is also used as a bone substitute as it mimics the natural architecture of the cancellous bone even after undergoing heat treatment and chemical extraction process [14]. A number of synthetic bone graft substitutes also have been developed for the repair of bony defects, especially in the craniofacial area. Most of these are based on HA or other calcium phosphate minerals, similar to the natural mineral found in human bone. Calcium salts, mainly HA, help in bridging large segmental defects by the process of osteoconduction, thus getting deposited on the collagenous framework of the bone by the osteoblasts [15]. Studies have shown chemical and crystallographic similarity of synthetic HA to the naturally occurring HA [16–19]. Hence, these materials are osteoconductive, biocompatible and can be easily sterilized and used in the clinic.

Hydroxyapatite Hydroxyapatite as the main inorganic salt of bone and teeth, is the most studied calcium phosphate material in

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Fig. 3 HA used in augmentation genioplasty

clinical practices ever since 1970s [20]. Hydroxyapatite is calcium phosphate bioceramic and is also referred to as ceramic hydroxylapatite used as a bone defect filler, hydroxylapatite. It is generally recognized as the natural biologic mineral component of vertebrate hard tissue and is comprised in 60–70 % bone in the formula of [Ca5(PO4)3OH] and 98 % dental enamel (Fig. 1). The composition of HA ceramic is [Ca10(PO4)6OH2] with a idealized Ca/P ratio 1.67, is not found in human biologic hydroxylapatite. The existence of a direct chemical bond between bone and ceramic and non-ceramic bioactive hydroxylapatite (OsteoGenÒ [Ca5(PO4)3(OH)]) has been reported [21]. Filling defect site with bioactive hydroxylapatite, new bone formation was evident by 95 %, in a critical side defect of 8 mm 9 1 mm wide (Valen Ricci Spivak) by histological studies of bone–hydroxylapatite interaction [21] through the combination of extracellular matrix components and direct physicochemical deposition on ceramic OsteoGenÒ, however, demonstrated sparingly 8 % new bone deposition touching the ceramic HA surface coating intermittently (Ricci, Spivak) at the tissue–titanium implant interface. Ceramic HA is generally

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Fig. 4 HA used to increasing the height of alveolar ridge

Fig. 5 HA used for reconstruction of resected mandible

produced by a hydrothermal exchange reaction of the natural reef building coral skeleton in which the calcium carbonate skeleton is converted to calcium phosphate without changing the trabecular bone imitating structure of the coral [22]. The uniqueness of this material is its chemical similarity with the mineralized phase of bone which accounts for the osteoconductive potential and excellent biocompatibility [23–25]. The clinical use of ceramic HA mainly in granular form has been reported in dental, craniofacial as well as in orthopedic surgery (Figs. 2, 3, 4, 5) [26–30]. HA is osteophilic, osteoconductive and osteointegrated. It can get bonded to the bone directly through the natural bone converting mechanism [31]. The calcium HA/tricalcium phosphate (60/40) provides a structure or scaffold in close interface with adjacent bone. Thus, its use in the treatment of load-bearing segmental bone defects is confined only to a limited number of cases, but without any failure reports at the early stages of implantation [32]. Tricalcium phosphate can undergo partial conversion to HA once it is implanted into the body and this characteristic makes it a random porous ceramic. As tri-calcium phosphate is highly porous and quickly resorbed into bone it

becomes mechanically weak in compression after conversion whereas HA is resorbed slowly and large segments of it can remain in place for years. The unpredictable biodegradation profile of tri-calcium phosphate has made it an unpopular bone graft substitute [33]. However, bone defects as an outcome of trauma, benign tumors, and unicameral cysts can be effectively filled by tri-calcium phosphate [34] or by non-ceramic bioactive hydroxylapatite. (Spivak, Ricci, Valen) (Valen Letter to the Editor— enclosed) (Kimoto Part 1) (Nordquist Part II-Part III) [21, 35–40]. The benefits of non-ceramic bioactive hydroxylapatite in dentistry have been demonstrated especially for the surface conversion to fluorapatite for bacteriostatic control and mitigation or elimination of pathogens and for cell differentiation and proliferation of human osteoblast (Ohno) [41]. Fluoridated hydroxyapatite (fluorapatite), shows promise as an adjunctive treatment component in inhibiting peri-implant infection [40]. HA is an excellent carrier of osteoinductive growth factors and osteogenic cell populations and hence also useful as a bioactive delivery vehicle [42]. Radiographic evidences are available suggesting that carbonated HA used in distal radius corrective osteotomies have 100 % union rate of graft integration into the bone tissue. There was also improvement in range of wrist motion, forearm rotation as well as grip strength [6]. Thus, these studies confirmed the use of HA as an excellent bone graft substitute in orthopedic surgeries as it facilitates bone formation, is biocompatible and slow remodeling material. The origin of HA ceramic may be natural or artificial (synthetic). Synthetic ceramic HA acts as a framework for the ingrowth and helps in subsequent deposition of new bone [43]. In recent years the technique of doping of bioceramic materials are also adopted to enhance their mechanical and biological properties as well as cytocompatibility for use in tissue engineering applications [44, 45]. Synthetic HA are also used as a coating material for dental and orthopedic implants, but its moderate to low solubility within the body and mechanical properties that differ from surrounding tissue and bone [44] limits its use. The use of doped HA with manganese and/or zinc as a bone substitute has resulted in faster resorption kinetics [46]. The use of plasma spray HA coating as a means of fixation on metallic femoral stem and cup has also been reported [47]. HAcoated pins enhance pin fixation irrespective of bone type and loading conditions. This reduces the rate of infection and loosening during external fixation [48, 49].

Porous hydroxyapatite Synthetic porous HA bone graft materials are osteoconductive, biocompatible and slowly resorbing bone

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substitute. The use of porous HA has replaced the use of dense form of HA due to its better integration to bone by direct bonding to the bone. This facilitates osteoblastic proliferation into the micropores and acts as a scaffold for bone regeneration [50–52]. Studies have shown that treatment of bony defects by HA leads to bone growth into 18–74 % pores of new bone area as compared to total implant area [53, 54]. However, probably the entire porous space of the implant is never completely filled with bone [55]. Porous HA can be produced either by homogenizing calcium phosphate powder with naphthalene particles or by the decomposition of hydrogen peroxide to generate a pore-filled structure. The interconnected high porous structure of HA has been promising for postero-lateral lumbar inter-transverse process spine fusion [56, 57]. Several studies have shown that porous HA is osteoconductive, biocompatible and very inert [58, 59]. It resorbs with time but the degradation rate is very slow [60]. However, porous HA is brittle and can be used only in nonloading sites and will act as a high stress riser, compromising the host bone with fibrous tissue encapsulation and fracture points under load. Its compressive strength is enhanced by bone ingrowth, comparable only to that of cancellous bone [53].

Coralline hydroxyapatite Coralline hydroxyapatite (CHA) is also an alternative to bone graft. The pore structure and biomechanical properties of CHA is similar to human cancellous bone. It is equally efficient to autogenous cancellous bone in the use for subchondral support during internal fixation of tibial plateau fractures. It provides the structural integrity to support an articular surface and also osteoconductive matrix for bony ingrowth [60]. CHA is processed by a hydrothermal exchange method in which the coral calcium phosphate is converted to crystalline HA with pore diameters between 200 and 500 lm, and a structure resembling human trabecular bone. Cases of articular surface depression in tibial plateau fractures have reported that the clinical performances of autologous cancellous bone graft and CHA are equivalent when used for filling bone voids [61]. The use of CHA has been successful in non-weight-bearing applications such as maxillofacial, periodontal augmentation [62] and distal radial fractures [60] as well as in weight-bearing metaphyseal defects (i.e. tibial plateau fractures) [63]. However, initially it needs support by internal fixation until completion of fibro-osseous ingrowth because of mechanical weakness. Bone graft expansion in spinal fusions [64, 65] and orbital restorations [66] are other clinical uses of CHA. A clinical study in 1999 reported that 19 distal radius fractures were treated using

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internal and external fixation implanted CHA bone graft as a substitute for autogenous bone graft to support the reduced articular surface of 21 consecutive patients with distal radius fractures treated with external fixation and K-wire [60]. This single-cohort retrospective study was undertaken to report the outcomes of treatment with this material, associated contraindications, and its efficiency in articular surface reduction. After 35 months of surgery 18 patients were available for analytical procedures involving radiography, subjective outcome analysis and independent evaluation of motion. 17 patients had good or excellent radiographic results. The use of CHA in combination with external fixation and K-wires was effective at maintaining articular surface reduction and its safety profile was comparable to other forms of the treatment. The need for bone graft material keeps on increasing with increased age of the population and the increased conditions of high velocity trauma. Autografts remain the gold standard because they contain the requisite osteoinductive, osteogenic and osteoconductive properties necessary to regenerate bone. There are drawbacks to harvesting autograft, including increased operating time, potential complications and morbidity of the harvest site and limitations in available bone quantity. Due to these limitations there has been significant effort placed on the development of various categories of bone graft substitutes, including calcium phosphate and hydroxyapatite materials. We can conclude from the study of literatures described above that in the near future these bone graft substitutes such as hydroxyapatite can form a new approach or idea of treatment in the patients with bony defects, especially in elderly people with unstable, extra-articular and comminuted distal radius fractures, thus preventing secondary collapse, providing better post-operative rehabilitation and improving functional outcome. The modern day research on available bone graft substitutes involving the methods of genetic engineering and refinements in internal fixation techniques might be, therefore, helpful in managing bone defects, including periodontal defects such as intrabony defect and maxillofacial defects such as reconstruction of excision of primary bone tumor, craniofacial defects such as cleidocranial dysplasia as well as for treating orthopedic defects such as distal radius fractures. Conflict of interest

None.

References 1. Beaman FD, Bancroft LW, Peterson JJ et al (2006) Bone graft materials and synthetic substitutes. Radiol Clin North Am 44:451–461. doi:10.1016/j.rcl.2006.01.001 2. Hegde C, Shetty V, Wasnik S et al (2013) Use of bone graft substitute in the treatment for distal radius fractures in elderly.

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3.

4.

5.

6.

7.

8.

9. 10.

11.

12.

13.

14.

15. 16.

17.

18.

19.

Eur J Orthop Surg Traumatol 23:651–656. doi:10.1007/s00590012-1057-1 Jakubietz MG, Gruenert JG, Jakubietz RG (2011) The use of beta-tricalcium phosphate bone graft substitute in dorsally plated, comminuted distal radius fractures. J Orthop Surg Res 6:24. doi:10.1186/1749-799X-6-24 Goto A, Murase T, Oka K et al (2011) Use of the volar fixed angle plate for comminuted distal radius fractures and augmentation with a hydroxyapatite bone graft substitute. Hand Surg 16:29–37. doi:10.1142/S0218810411005023 Rajan GP, Fornaro J, Trentz O et al (2006) Cancellous allograft versus autologous bone grafting for repair of comminuted distal radius fractures: a prospective, randomized trial. J Trauma 60:1322–1329. doi:10.1097/01.ta.0000195977.18035.40 Luchetti R (2004) Corrective osteotomy of malunited distal radius fractures using carbonated hydroxyapatite as an alternative to autogenous bone grafting. J Hand Surg Am 29:825–834. doi:10.1016/j.jhsa.2004.06.004 Aghazadeh A, Rutger Persson G, Renvert S (2012) A singlecentre randomized controlled clinical trial on the adjunct treatment of intra-bony defects with autogenous bone or a xenograft: results after 12 months. J Clin Periodontol 39:666–673. doi:10. 1111/j.1600-051X.2012.01880.x Meyle J, Hoffmann T, Topoll H et al (2011) A multi-centre randomized controlled clinical trial on the treatment of intra-bony defects with enamel matrix derivatives/synthetic bone graft or enamel matrix derivatives alone: results after 12 months. J Clin Periodontol 38:652–660. doi:10.1111/j.1600-051X.2011.01726.x Misch CM (2010) Autogenous bone: is it still the gold standard? Implant Dent 19:361. doi:10.1097/ID.0b013e3181f8115b Tovar N, Jimbo R, Gangolli R, Perez L et al (2014) Evaluation of bone response to various anorganic bovine bone xenografts: an experimental calvaria defect study. Int J Oral Maxillofac Surg 43:251–260. doi:10.1016/j.ijom.2013.07.005 Zafiropoulos GG, Hoffmann O, Kasaj A et al (2007) Treatment of intrabony defects using guided tissue regeneration and autogenous spongiosa alone or combined with hydroxyapatite/beta-tricalcium phosphate bone substitute or bovine-derived xenograft. J Periodontol 78:2216–2225. doi:10.1902/jop.2007.070146 Belli E, Longo B, Balestra FM (2005) Autogenous platelet-rich plasma in combination with bovine-derived hydroxyapatite xenograft for treatment of a cystic lesion of the jaw. J Craniofac Surg 16:978–980. doi:10.1097/01.scs.0000183469.93084.f3 Hanna R, Trejo PM, Weltman RL (2004) Treatment of intrabony defects with bovine-derived Xenograft alone and in combination with platelet-rich plasma: a randomized clinical trial. J Periodontol 75:1668–1677. doi:10.1902/jop.2004.75.12.1668 Baldini M, DeSanctis M, Ferrari M (2011) Deproteinized bovine bone in periodontal and implant surgery. Dent Mater 27:61–70. doi:10.1016/j.dental.2010.10.017 Cornell CN, Lane JM (1992) Newest factors in fracture healing. Clin Orthop 277:297–311 Guda T, Walker JA, Singleton B et al (2014) Hydroxyapatite scaffold pore architecture effects in large bone defects in vivo. J Biomater Appl 28:1016–1027. doi:10.1177/0885328213491790 Ong JC, Kennedy MT, Mitra A et al (2012) Fixation of tibial plateau fractures with synthetic bone graft versus natural bone graft: a comparison study. Ir J Med Sci 181:247–252. doi:10. 1007/s11845-011-0797-y Antonakos A, Liarokapis E, Leventouri T (2007) Micro-Raman and FTIR studies of synthetic and natural apatites. Biomaterials 28:3043–3054. doi:10.1016/j.biomaterials.2007.02.028 LeGeros RZ, Parsons JR, Daculsi G et al (1988) Significance of the porosity and physical chemistry of calcium phosphate ceramics. Biodegradation–bioresorption. Ann N Y Acad Sci 523:268–271. doi:10.1111/j.1749-6632.1988.tb38519.x

20. Hulbert SF, Young FA, Mathews RS et al (1970) Potential of ceramic materials as permanently implantable skeletal prostheses. J Biomed Mater Res 4:433–456. doi:10.1002/jbm.820040309 21. Spivak JM, Ricci JL, Blumenthal NC et al (1990) A new canine model to evaluate the biological response of intramedullary bone to implant materials and surfaces. J Biomed Mater Res 24:1121–1149. doi:10.1002/jbm.820240902 22. Roy DM, Linnehan SK (1974) Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange. Nature 247:220–222. doi:10.1038/247220a0 23. Nandi SK, Kundu B, Ghosh SK et al (2008) Efficacy of nano hydroxyapatite prepared by an aqueous solution combustion technique in healing bone defects of goat. J Vet Sci 9:183–191. doi:10.4142/jvs.2008.9.2.183 24. Ghosh SK, Nandi SK, Kundu B et al (2008) Invivo response of porous hydroxyapatite and beta-tricalcium phosphate prepared by aqueous solution combustion method and comparison with bioglass scaffolds. J Biomed Mater Res B Appl Biomater 86:217–227. doi:10.1002/jbm.b.31009 25. Erbe EM, Marx JG, Clineff TD et al (2001) Potential of an ultra porous beta- tricalcium phosphate synthetic cancellous bone void filler and bone marrow aspirate composite graft. Eur Spine J 10:S141–S146. doi:10.1007/s005860100287 26. Minami M, Takechi M, Ohta K et al (2013) Bone formation and osseointegration with titanium implant using granular-and blocktype porous hydroxyapatite ceramics (IP-CHA). Dent Mater J 32:753–760. doi:10.4012/dmj.201-169 27. Yamamiya K, Okuda K, Kawase T et al (2008) Tissue-engineered cultured periosteum used with platelet-rich plasma and hydroxyapatite in treating human osseous defects. J Periodontol 79:811–888. doi:10.1902/jop.2008.070518 28. den Boer FC, Wippermann BW, Blokhuis TJ et al (2003) Healing of segmental bone defects with granular porous hydroxyapatite augmented with recombinant human osteogenic protein1 or autologous bone marrow. J Orthop Res 21:521–528. doi:10.1016/ S0736-0266(02)00205-X 29. Moreira-Gonzalez A, Jackson IT, Miyawaki T et al (2003) Augmentation of the craniomaxillofacial region using porous hydroxyapatite granules. Plast Reconstr Surg 111:1808–1817. doi:10.1097/01.PRS.0000055432.20074.93 30. Itokazu M, Matsunaga T, Ishii M et al (1996) Use of arthroscopy and interporous hydroxyapatite as a bone graft substitute in tibial plateau fractures. Arch Orthop Trauma Surg 115:45–48. doi:10. 1007/BF00453217 31. Jarcho M (1986) Biomaterials aspects of calcium phosphates: properties and application. Dent Clin North Am 30:25–67 32. Balcik C, Tokdemir T, Senko¨ylu¨ A et al (2007) Early weight bearing of porous HA/TCP (60/40) ceramics invivo: a longitudinal study in a segmental bone defect model of rabbit. Acta Biomater 3:985–996. doi:10.1016/j.actbio.2007.04.004 33. Finkemeier CG (2002) Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am 84:454–464 34. Saikia KC, Bhattacharya TD, Bhuyan SK et al (2008) Calcium phosphate ceramics as bone graft substitutes in filling bone tumor defects. Indian J Orthop 42:169–172. doi:10.4103/0019-5413. 39588 35. Valen M, Ganz SD (2002) Part I—a synthetic bioactive resorbable graft (SBRG) for predictable implant reconstruction. J Oral Implantol 28(4):167–177 36. Ricci JL, Blumenthal NC, Spivak JM, Alexander H (1992) Evaluation of a low-temperature calcium phosphate particulate implant material: physical–chemical properties and in vivo bone response. J Oral Maxillofac Surg 50:969–978 37. Valen M (2013) Letter to Editor. JOI 39(2):234–235 (Re: Fluoridetreated bioresorbable synthetic hydroxylapatite promotes proliferation and differentiation of human osteoblastic MG-63 cells)

123

Ir J Med Sci 38. Kimoto K, Okudera T, Okudera H, Nordquist W, Krutchkoff D (2011) Part I: crystalline fluorapatite-coated hydroxylapatite; physical properties. JOI 37(1):27–33 39. Nordquist WD, Okudera H, Kitamura Y, Kimoto K, Okudera T, Krutchoff D (2011) Part II crystalline fluorapatite-coated hydroxylapatite implant material: a dog study with histologic comparison of osteogenesis seen with FA-coated HA grafting material versus HA controls: potential bacteriostatic effect of fluoridated HA. JOI 37(1) 40. Nordquist WD, Krutchoff D (2011) Part III: crystalline fluorapatite-coated hydroxylapatite; potential use as a bacteriostatic agent for both pre-implant cases and retreatment of infected implant sites. A report of 4 cases. JOI 37(1) 41. Ohno M, Kimoto K et al (2013) Fluoride-treated bio-resorbable synthetic hydroxyapatite promotes proliferation and differentiation of human osteoblastic MG-63 cells. JOI 39(2):154–160 42. Lalidou F, Kolios G, Drosos GI (2014) Bone infections and bone graft substitutes for local antibiotic therapy. Surg Technol Int 24:353–362 43. Jones NF, Brown EE, Mostofi A et al (2005) Healing of a scaphoid nonunion using human bone morphogenetic protein. J Hand Surg Am 30:528–533. doi:10.1016/j.jhsa.2004.12.005 44. Santos MH, Valerio P, Goes AM et al (2007) Biocompatibility evaluation of hydroxyapatite/collagen nanocomposites doped with Zn2?. Biomed Mater 2:135–141. doi:10.1088/1748-6041/2/ 2/012 45. Webster TJ, Massa-Schlueter EA, Smith JL et al (2004) Osteoblast response to hydroxyapatite doped with divalent and trivalent cations. Biomaterials 25:2111–2121. doi:10.1016/j.biomaterials. 2003.09.001 46. Irigaray JL, Oudadesse H, Jallot E et al (1999) Kinetics resorption after implantation of some hydroxyapatite compounds used as biomaterials. Adv Sci Technol 28:399–403 47. Moroni A, Pegreffi F, Cadossi M et al (2005) Hydroxyapatitecoated external fixation pins. Expert Rev Med Devices 2:465–471. doi:10.1586/17434440.2.4.465 48. Nguyen HQ, Deporter DA, Pilliar RM et al (2004) The effect of sol-gel-formed calcium phosphate coatings on bone ingrowth and osteoconductivity of porous-surfaced Ti-alloy implants. Biomaterials 25:865–876. doi:10.1016/S0142-9612(03)00607-0 49. Pommer A, Muhr G, David A (2002) Hydroxyapatite-coated Schanz pins in external fixators used for distraction osteogenesis: a randomized, controlled trial. J Bone Joint Surg Am 84:1162–1166 50. Jang DW, Franco RA, Sarkar SK et al (2014) Fabrication of porous hydroxyapatite scaffolds as artificial bone perform and its biocompatibility evaluation. ASAIO J 60:216–223. doi:10.1097/ MAT.0000000000000032 51. Kwon BJ, Kim J, Kim YH et al (2013) Biological advantages of porous hydroxyapatite scaffold made by solid freeform fabrication for bone tissue regeneration. Artif Organs 37:663–670. doi:10.1111/aor.12047

123

52. Kenny EB, Lekovic V, Han T et al (1985) The use of a porous hydroxylapatite implant in periodontal defects. I. Clinical results after six months. J Periodontol 56:82–88. doi:10.1902/jop.1985. 56.2.82 53. Martin RB, Chapman MW, Sharkey NA et al (1993) Bone ingrowth and mechanical properties of coralline hydroxyapatite 1 yr after implantation. Biomaterials 14:341–348. doi:10.1016/ 0142-9612(93)90052-4 54. Holmes RE, Wardrop RW, Wolford LM (1988) Hydroxylapatite as a bone graft substitute in orthognathic surgery: histologic and histometric findings. J Oral Maxillofac Surg 46:661–671. doi:10. 1016/0278-2391(88)90109-7 55. Rosen HM, McFarland MM (1990) The biologic behavior of hydroxyapatite implanted into the maxillofacial skeleton. Plast Reconstr Surg 85:718–723 56. Motomiya M, Ito M, Takahata M et al (2007) Effect of hydroxyapatite porous characteristics on healing outcomes in rabbit posterolateral spinal fusion model. Eur Spine J 16:2215–2224. doi:10.1007/s00586-007-0501-0 57. Kaito T, Mukai Y, Nishikawa M et al (2006) Dual hydroxyapatite composite with porous and solid parts: experimental study using canine lumbar interbody fusion model. J Biomed Mater Res B Appl Biomater 78:378–384. doi:10.1002/jbm.b.30498 58. Norman ME, Elgendy HM, Shors EC et al (1994) An in vitro evaluation of coralline porous hydroxyapatite as a scaffold for osteoblast growth. Clin Mater 17:85–91 59. Jarcho M (1981) Calcium phosphate ceramics as hard tissue prosthetics. Clin Orthop Relat Res 157:259–278 60. Wolfe SW, Pike L, Slade JF 3rd et al (1999) Augmentation of distal radius fracture fixation with coralline hydroxyapatite bone graft substitute. J Hand Surg Am 24:816–827 61. Bucholz RW, Carlton A, Holmes RE (1987) Hydroxyapatite and tricalcium phosphate bone graft substitutes. Orthop Clin North Am 18:323–334 62. Holmes RE (1979) Bone regeneration within a coralline hydroxyapatite implant. Plast Reconstr Surg 63:626–633 63. Bucholz RW, Carlton A, Holmes R (1989) Interporous hydroxyapatite as a bone graft substitute in tibial plateau fractures. Clin Orthop Relat Res 240:53–62 64. Boden SD, Martin GJ Jr, Morone M et al (1999) The use of coralline hydroxyapatite with bone marrow, autogenous bone graft, or osteoinductive bone protein extract for posterolateral lumbar spine fusion. Spine (Phila Pa 1976) 24:320–327 65. Zdeblick TA, Cooke ME, Kunz DN et al (1994) Anterior cervical discectomy and fusion using a porous hydroxyapatite bone graft substitute. Spine (Phila Pa 1976) 19:2348–2357 66. Georgiadis NS, Terzidou CD, Dimitriadis AS (1999) Coralline hydroxyapatite sphere in orbit restoration. Eur J Ophthalmol 9:302–308

Ceramic and non-ceramic hydroxyapatite as a bone graft material: a brief review.

Treatment of dental, craniofacial and orthopedic defects with bone graft substitutes has shown promising result achieving almost complete bone regener...
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