Comblements osseux par céramique phosphocalcique biphasée macroporeuse A propos de 23 cas
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1 Revue de Chirurgie Orthopédique Masson, Paris, , 81, MÉMOIRE Comblements osseux par céramique phosphocalcique biphasée macroporeuse A propos de 23 cas Biphasic macroporous calcium phosphate ceramic bone substitute for filling bone defects: A report of 23 cases F. Gouin*, J. Delécrin*/**, N. Passuti*/**, S. Touchais*, P. Poirier*, J.V. Bainvel* (Nantes) Clinique Chirurgicale Orthopédique (Pr. BAINVEL), CHRU, F44035 Nantes Cedex. Laboratoire des matériaux d'intérêt biologique (G. DACULSI), EP CNRS 59, Nantes. ABSTRACT Purpose of the study The authors report their experience with the use of a biphasic macroporous calcium phosphate bone substitute. Materials and methods In 23 cases (22 patients) a biphasic macroporous calcium phosphate ceramic was used to fill a pathological bone defect. The ceramic used in this study was a macroporous (400 to 600 µ) component consisting of 60 per cent hydroxyapatite and 40 per cent β-tricalcium phosphate. It was in the form of granules (2 to 3 mm), sticks (20x5x5 or 10x5x5mm) or custom made blocks. In 6 cases, the ceramic was used alone; in 12 cases with autologous bone marrow and in 5 cases with autologous cancellous bone grafts. In 14 cases, the bone defect was due to conservative treatment of a benign tumor, in 3 cases due to aseptic posttraumatic non union, in 3 cases due to wide resection for malignant tumors of the pelvis and in 3 cases following osteotomy. Post operative assessment was made from clinical, radiographic and histological findings. Results 2 patients died 6 and 8 months post operatively and 2 were lost to follow up at 2 and 5 months with both having good clinical and radiographic results when last seen. For the remaining 19 cases, the average follow-up was 20 months (from 6 to 62 months). No local, regional or general deleterious effects were noted. Radiologically the bone ceramic junction healed in all cases except 2 within 3 months. In these last two cases, healing required 6 and 7 months. No radiolucent line appeared around the ceramic. No stress fractures occurred in the substitute. Histologically, 3 biopsies showed new bone formation throughout the ceramic with apposition of a well differenciated lamellar bone directly apposed to the ceramic. Discussion Animal experimentations have proven the interest of similar ceramics: macroporosity enhances bone rehabitation and the biphasic characteristics associate the advantages of slow resorption of hydroxyapatite and more easily resorbed,β-calcium phosphate. No deleterious clinical, radiographical or histological effects were observed, confirming the biocompatibility of this substitute. Despite the poor mechanical properties of this macroporous ceramic before implantation, good clinical and radiographic results suggest improvement of these properties in the composite new formed bone-ceramic after implantation. Conclusion We believe that macroporous biphasic ceramic is a good substitute for use in bone defects when good primary mechanical stability and contact with the host bone are present. Further clinical and experimental studies are necessary to determine the limits of such a substitute in terms of volume and to control its mechanical properties following implantation. Reprints: F. GOUIN, address above. CODE No.: Accepted on: 7 November 1994.
2 60 F. GOUIN, J. DELÉCRIN, N. PASSUTI, S. TOUCHAIS, P. POIRIER, J. V. BAINVEL INTRODUCTION The disadvantages inherent to bone autografts and allografts have encouraged the development of synthetic bone substitutes. Calcium phosphate ceramics are one of the best choices, as they are biocompatible [Jarcho (13), Winter et al. (26)] and bioactive [Klein et al. (14)], in other words, they promote favourable biological reactions. The interactions between the bone and the bioactive material are related to the physical properties of the material, in particular the macroporous nature [Daculsi et Passuti (6), Van Blitterswijk et al. (25)], as well as its chemical properties [Daculsi et Passuti (6), Frayssinet et al. (10), Nery et al. (17)]. Thus, osteoconduction results in bone ingrowth and resorption of the biomaterial, but the kinetics and extent of the osteoconductive process vary with the physical and chemical characteristics of the calcium phosphate ceramic. These bone substitutes have been used in maxillo-facial surgery [Legeros (16)] and occasionally in ENT and orthopaedics [Daculsi et al. (7), Daculsi et al. (8), Uchida et al. (24), Zheng et al. (27), Oghushi et al. (18)]. In this paper we report our initial short-term results on the use of a biphasic macroporous calcium phosphate ceramic (BCP) to fill bone defects. MATERIALS AND METHODS The calcium phosphate (BCP) used in this study was a compound that is biphasic (60 percent hydroxyapatite (HA) and 40 percent β tricalcium phosphate (βtcp)) and macroporous (50% of the volume occupied by pores), with pore size ranging from 400 to 600 µm. Granules (2 to 3 mm) or blocks (20 X 5 X 5 mm and 10 X 5 X 5 mm) were used depending on the site. Twenty-two patients (23 cases) having had a bone defect filled with BCP with follow-up of more than 6 months were selected for this study. The study group included 10 women and 12 men who had a mean age of 30 years and 8 months at the time of the operation (range: 10 to 64 years). The cases involved: 14 benign tumours treated by curettage (7 chondromas, 2 solitary cysts, 1 chondroblastoma, 1 non-ossifying fibroma, 1 osteoid osteoma, 2 unspecified benign lesions); 3 aseptic non-unions of the lower limb (2 femur, 1 tibia); 3 wide resections of malignant pelvic tumours; 2 osteotomies for phalanx non-union; 1 open wedge high tibial osteotomy In 9 cases, the site was the lower limb, in 11 cases in the upper limb, and in 3 cases in the pelvis. In addition to the coccyx bone, bone substitute was used 12 times in the metaphyseal region, 6 times in the diaphyseal region and twice in the epiphyseal region. In these sites, the bone defect measured from 5 to 130 mm in largest diameter (30 mm on average). Nine cases involved no contact between the two bone segments, with stability ensured by osteosynthesis. In 14 cases, there was bone contact, which was reinforced preventively by osteosynthesis in 3 cases, with BCP used simply to fill a void. BCP was used 12 times in the form of granules and 11 times in the form of blocks. In two cases the block were custom cut preoperatively. BCP was used alone as a graft in 6 cases, and 12 times in association with autologous bone marrow, mixed preoperatively. In 5 cases the ceramic was used to augment the volume of an autologous cancellous bone graft, including 3 times for extensive bone defects in the pelvis. RESULTS Two patients died 6 and 8 months post operatively, of causes not related to the bone graft (malignant pelvic tumours). Two were lost to follow up at 2 and 5 months, with both having regained full function and considered cured when last seen. For the remaining patients the average follow-up was 20 months (from 6 to 62 months). Clinical Results No local complications except for a haematoma not requiring surgical revision were noted initially or during follow-up. Five patients presented limited mobility of nearby joints during the follow-up period, not attributable to the bone substitute technique. These cases involved 3 bone grafts following wide bone and muscle resection of the pelvis and 2 bone grafts involving the fingers (one insufficient correction of a non-union and one refusal on the part of a patient to comply with physical therapy). No clinical results deteriorated over time. Radiological Results Three specific points were studied: the biomaterial-bone interface; the radiological density of the material itself; the occurrence of fracture or fragmentation of the material.
3 CALCIUM PHOSPHATE CERAMIC BONE GRAFT SUBSTITUTE 61 Fig. 1. Chondroma of the first metacarpal filled with BCP. a) post-operative appearance of the granules b) 4 months postoperatively, mottled and inhomogeneous appearance of the graft. The cortical covering is healed c) 13 months postoperatively, densification and homogenization of the graft without loss of continuity with the host bone. 1a 1b 1c The transition zones began to change early with the lighter zones surrounding the BCP being colonized by radio-opaque tissue visible one month postoperatively (fig. 1). Bone-BCP contact was complete within 3 months in all but two cases. In one case, delayed healing occurred in a phalanx (considered to be solid at 7 months) and the other case involved treatment of non-union of the femur in which the bone-bcp contact was incomplete despite pain-free weight bearing at 6 months. No radiolucent lines or radiological sequestration of the substitute were noted. As regards the material itself, the progress varied greatly depending on the graft site, but it was sufficiently typical to be summarized. After one month, the contours of the blocks or granules became blurred, the overall appearance of the substitute became slightly mottled and was inhomogeneous, subsequently becoming homogeneous and dense (fig. 1 and 2). No changes appeared after the first year, with the exception of the treatment of the diaphyseal non-union of the femur where the BCP seemed to have become corticalized after 15 months. Two purely diaphyseal, non-circumferential defects had been filled all the way to the medullary canal. Though at the level of the cortical bone the BCP sticks followed the same radiological pattern as in the other cases, at the endo-medullary level, they appeared not to have changed substantially. No stress fractures or progressive osteolysis were observed. No settling of the substitute was noted in the treatment of non-union of the femur held by a dynamic intra-medullary nail, nor angular changes in the open wedge high tibial osteotomy after removal of the internal fixation device (fig. 3). Bone scintigraphy with 99mTc- MDP was performed 44 months after an upper metaphyseal defect in the femur was filled after treatment of an enchondroma in Ollier s disease (fig. 2b). Increased uptake in the late image throughout the filled zone suggested late remodelling in this patient, who presented no signs of local recurrence 16 months later (fig. 2c). Histologically, 3 biopsies were performed, at 3, 12 and 15 months follow-up. They were embedded in methylmetacrylate to obtain non-decalcified slices and microradiographs. In all 3 cases, despite different followup times and sites (through all three were from the metaphyseal zone) the microradiographs showed large amounts of mineralized bone in the pores of the BCP (fig. 4) and polarised light showed well differentiated lamellar bone deposited directly on the BCP.
4 62 F. GOUIN, J. DELÉCRIN, N. PASSUTI, S. TOUCHAIS, P. POIRIER, J. V. BAINVEL Fig. 2. Graft in a chondroma of the upper femur in Ollier s disease a) Post-operative x-ray. b) Bone scan with 99mTc-MDP. Uptake 44 months after the graft suggesting a remodelling within the BCP. No radiological signs of tumour progression 16 months later. c) At 60 months, restoration of the external cortical bone, dense and homogenous appearance of the graft. DISCUSSION Though autologous grafts are the reference in the area of bone grafts, the surgical procedure takes longer, thus increasing morbidity [Cockin (3), Laurie et al. (15), Summers et Eisenstein (21)]. In recent years, the use of BCP in spinal arthrodesis [Passuti et al. (20)] has confirmed its good tolerance and efficacy in these indications. Under the right conditions, ceramics can be an alternative bone substitute for grafting bone defects. There are two fundamental conditions: good primary stability ensured by an internal fixation device [Daculsi et al. (4), Flatey et al. (9), Gründel et al. (11), Hoofendoorn et al. (12)] and close contact between the ceramic and the host bone [Daculsi et al. (4)]. In this study we used a biphasic compound combining hydroxyapatite (HA) and β tricalcium phosphate (β TCP). The advantage of this compound in optimal proportions is that it combines the properties of each component [Nery et al. (17)]. β TCP is highly soluble and interacts quickly with the surrounding environment [Daculsi et al. (7), Legeros (16)], whereas HA is less soluble and more stable in the long term [Legeros (16)]. Osteoconduction involves many processes, including passive dissolution by biological fluids, reprecipitation of crystals [Daculsi et al. (5)], resorption by osteoclasts and other giant cells [Baslé et al. (1)] and remodelable new bone formation. Based on these experimental data, we have been using BCP as a bone substitute since 1988 in indications that were initially highly restrictive. No deleterious clinical or radiological effects were caused by using this ceramic as a bone substitute material in the limbs. The radiological evolution after implantation suggests bone formation at the periphery of the substitute and between the granules without fibrous encapsulation. The homogenization and secondary densification of the BCP, without loss of continuity on the periphery, are consistent with the radiological results of Uchida et al. (24), who used a monophasic HA compound. Of course, x-rays
5 COMBLEMENTS OSSEUX PAR CÉRAMIQUE PHOSPHOCALCIQUE 63 Fig Microradiography (x 48) 12 months after graft of an open wedge tibial osteotomy. Specimen taken from centre of the block. Well-mineralised bone trabecula (o) within the BCP (b). Fig Open wedge tibial osteotomy. Radiological appearance 15 months after the osteotomy and 3 months after removal of the internal fixation device. No settling of the graft, and the blurred margins of the wedge suggest good healing. provide only limited information on the in-vivo behaviour of a bone substitute. They show only the BCPhost bone interface zones, which can be examined for signs suggesting fibrous encapsulation, and the substitute itself, where any signs of deterioration such as a fracture or settling will be revealed. X-rays cannot provide information on the bone ingrowth of the ceramic. However, the absence of radiologically detectable stress fracture is indirect proof of bone recolonization. The mechanical characteristics of macroporous ceramics before implantation limit the use to grafts not subject to mechanical stress, or in other words bone defects neutralized by a stable fixation device or bone defects without loss of bone continuity. Recent experimental work [Trécant et al. (23)] has shown that after implantation, BCP bone ingrowth was accompanied by an significant increase in implant compression strength. The mechanical strength of the ceramic is demonstrated by the open wedge high tibial osteotomy in which the internal fixation device was removed, and the non-union of the femur with dynamic nailing, both healed and subjected to weight-bearing without settlement or fracture. This evolution can only be the result of new bone formation within the BCP, and remodelling suggested by the radiological evolution in the latter case. The histological results of the three biopsies confirm the quality of bone ingrowth in the pores, on the specimens taken both from the periphery and from the centre. In each case, well-differentiated lamellar bone was deposited on the BCP with no fibrous interposition detectable by optical microscope. These date have a qualitative interest and confirm the experimental results. However, due to the limited number of cases, the variety of indications, sites and environments, we cannot predict the resorptiondeposition kinetics for a specific application. We cannot judge the role of the addition of autologous bone marrow. However, many studies have shown the benefits of this practice in bone repair processes [Burwell (2), Palley et al. (19), Takagi et Urist (22)]. In their study, Gründel et al. (11) report on the advantages of ceramic composites in the form of granules plus bone marrow compared to ceramic blocks or autologous bone marrow alone. Further studies are necessary to determine the optimum bone marrow/ceramic ratio and the osteoinductive potential of such compounds [Oghushi et al. (18)].
6 64 F. GOUIN, J. DELÉCRIN, N. PASSUTI, S. TOUCHAIS, P. POIRIER, J. V. BAINVEL CONCLUSION Base on our prior experimental studies, we used BCP as a bone substitute material under restrictive conditions. BCP confirmed its good tolerance locally and generally. The radiological evolution, functional results and in vivo biopsies demonstrate that a BCP-bone marrow compound is an alternative to cancellous autografts. However, longer follow-up periods with thorough clinical and paraclinical assessment and more biopsies are necessary, in order to shed light on the in vivo relationship between bone ingrowth, bone remodelling within the ceramic, and its mechanical properties after implantation. All of these data are needed to determine the indications for this bone substitute. ABSTRACT A biphasic macroporous calcium phosphate ceramic consisting of 60 percent hydroxyapatite and 40 percent β- tricalcium phosphate was used to fill 23 pathological bone defects. Good mechanical stability was ensured, either by internal fixation or by stable bone continuity, and the ceramic, mixed with autologous bone marrow in most cases, was in contact with vascularized host bone. No local, regional or general deleterious effects caused by the ceramic were noted. Radiologically the boneceramic junction healed within 3 months in all but 2 cases. No stress fractures occurred in the substitute. Three biopsies confirmed the experimental results obtained with this macroporous ceramic, showing new bone formation within the pores and no fibrous encapsulation. This bone ingrowth explains the improved mechanical properties of the substitute after implantation, as illustrated in 2 of our cases. We believe that this ceramic is a good alternative to cancellous autografts when the primary mechanical conditions are respected. Références 1. BASLE MF, CHAPPARD D, GRIZON F, FILMON R, DELÉCRIN J, REBEL A: Osteoclastic resorption of Ca-P biomaterials implanted in rabbit bone. Calcif Tissue Int, 1993, 53, BURWELL RG : The function of bone marrow in the incorporation of a bone graft. Clin Orthop, 1985, 200, COCKIN J : Autologous bone graftingcomplications at donor site. J Bone Joint Surg (Br), 1971, 53, DACULSI G, PASSUTI N, MARTIN S, LE NIHOUANEN JC, BRULLIARD V, DELÉCRIN J : Etude comparative des céramiques bioactives en phosphate de calcium après implantation en site osseux spongieux chez le chien. Rev Chir Orthop, 1989, 75, DACULSI G, LEGEROS RZ, HEUGHEBAERT M, BARBIEUX I : Formation of carbonate apatite crystals after implantation of calcium phosphate ceramics. Calcif Tissue Int, 1990, 46, DACULSI G, PASSUTI N : Effect of the macroporosity for osseous substitution of calcium phosphate ceramics. Biomater, 1900, 11, DACUSI G, PASSUTI N, MARTIN S, DEUDON C, LEGEROS RZ, RAHER S : Macroporous calcium phosphate ceramic for long bone surgery in humans and dogs. Clinical and histological study. J Biomed Mater Res, 1990, 24, DACULSI G, CORLIEU P, BACOT D'ARC M, GERSDORFF M : Macroporous biphasic calcium phosphate efficiency in mastoid cavity obliteration: experimental and clinical findings. Ann Oto Rhin Laryng, 1992, 101, FLATEY TJ, LYNCH KL, BENSON M : Tissues responses to implants of calcium phosphate ceramic in the rabbit spine. Clin Orthop, 1983, FRAYSSINET P, TROUILLET JL, ROUQUET N, AUTEFAGE A, DELGA C, CONTE P : Calcium phosphate porous ceramics osseointegration: the importance of a good definition of material specifications. 1 er Congrès Européen d'orthopédie. Paris, avril Rev Chir Orthop, 1993, 79, Abstract n GRÜNDEL RE,CHAPMQN MW, YEE T, MOORE DC: Autogenie bone marrow and porous biphasic calcium phosphate ceramic for segmental bone defect in the canine ulna. Clin Orthop, 1991, 266, HOOFENDOORN HA, RENOOIJ W, ADDERMANS LMA, VISSER W, WITTISOI. P: Long-term study of large ceramic implants (Porous hydroxyapatite) in dog femora. Clin Orthop, 1984, 187, JARCHO M : Calcium Phosphate ceramics as hard tissue prosthetics. Clin Orthop, 1981, 157, KLEIN CPAT, DRIESSEN AA, DE GROOT K, VAN DEN HOOF A : Biodegradation behavior of various calcium phosphate materials in bone tissue. J Biomed Mater Res, 1983, 17, LAURIE SWS, KABAN LB, MULLIKEN JB, MURRAY JE: Donor-site morbidity after harvesting rib and iliac bone. Plast Reconstr Surg, 1984, 73, LEGEROS RZ : Calcium phosphate materials in restorative dentistry: a review. Adv Dent Res, 1988, 2, NERY EB, LEGEROS RZ, LYNCH KL, LEE K: Tissue response to biphasic calcium phosphate ceramic with different ratios of HA/βTCP in periodontal osseous defects. J Periodontol, 1992, 63, OGHUSHI H, GOLDBERG VM, CAPAN Al: Heterotopic osteogenesis in porous ceramics induced by marrow cells. J Orthop Res, 1989, 7, PALLEY D, YOUNG MC, WILLLY AM, FORNASIER VL, JACKSON RW : Percutaneous bone marrow grafting of fractures and bony defects. Clin Orthop, 1986, 208,
7 COMBLEMENTS OSSEUX PAR CÉRAMIQUE PHOSPHOCALCIQUE PASSUTI N, DACULSI G, ROGEZ JM, MARTIN S, BAINVEL JV: Macroporous calcium phosphate ceramic performance in human spine fusion. Clin Orthop, 1989, 248, SUMMERS BN, EISENSTFIN SM : Donor site pain from the ilium. A complication of lumbar spine fusion. J Bone Joint Surg (Br), 1989, 71, TAKAGI K, URIST MR : The role of bone marrow in bone morphogenetic protein-induced repair of femoral massive diaphyseal defects. Clin Orthop, 1982, 171, TRECANT M, DELEGRIN J, ROYER J, DACULSI G : Mechanical changes in macroporous calcium phosphate ceramics after implantation in bone. Clin Mater, 1994, 15, UCHIDA A, ARAKI N, SHINTO Y, YOSHIKAWA H, KURISAKI E, ONO K : The use of calcium hydroxyapatite ceramic in bone tumor surgery. J Bone Joint Surg (Br), 1990, 72, VAN BLITTERSWIJK CA, GROTE JJ, KUIJPERS W, DAEYIS WTH, DE GROOTK : Macropore tissue ingrowth : a qualitative study on hydroxyapatite ceramics. Biomaterials 1986, 7, WINTER M, GRISS P, DE GROOT K, TAGA H, HEIMKE G, VON DIGH HJA, SAWAI K: Comparative histocompatibility testing of seven calcium phosphate ceramics. Biomaterials, 1981, 2, ZHENG QX, ZHU TB, DU JY, HONG GX, L I SP, YAN YH, ZHANG ED : Artificial bone of porous tricalcium phosphate ceramics and its preliminary clinical application. J Tongji Med Univ, 1992, 12,
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