- Email: [email protected]
The response of cortical bone to hydroxyapatite ceramic
C/inical Materia/s 1986; 1 : 23-28
The response of cortical bone to hydroxyapatite ceramic E Fischer-Brandies and E Dielert Department of Maxillofacial Surgery, University of Munich, FRG and FH Feder Department of Veterinary Histology and Embryology, University of Munich, FRG
Endosseus implantation is sometimes inadvisable if the bony structures are fragile. Therefore subperiosteal implantation of porous and dense hydroxyapatite ceramic implants on the unreamed parietal bone of four dogs was studied. During the investigated period of 1 4 weeks to 1 0 months the implant was surrounded by newly formed bone which grew up against the edges of the implant and penetrated the pores. A direct contact w i t h o u t a connective tissue layer formed between bone and hydroxyapatite. Few osseous lamellae developed on the side of the implant adjacent to the periosteum.
I ntroduction
Ceramics are increasingly becoming the subject of extensive research in the field of bone surgery. One of these materials, hydroxyapatite ceramic, is particularly interesting because its chemical composition is similar to that of the mineral substance of natural bone. Calcium phosphate ceramics with an apatite structure have been implanted in contact with cancellous bone, in the alveolus 1, in the femur diaphysis 2, 3, in long tubular bones as replacement of a resected bone tube stabilized by osteosynthesis using a plate and screws 3'4, and in the mandible applying the sandwich technique 5' 6. From these studies it is known that direct contact Address for correspondenceDr Dr E Fischer-Brandies,Department of Maxillofacial Surgery, University of Munich FRG, Lindwurmstr. 2a, 8000 Munchen 2, FRG.
between bone and endossally implanted hydroxyapatite ceramics will form, but there is a lack of information on the surface reactions of unreamed cortical bone to this material. The interposition of hydroxyapatite between cortical bone and periosteum can be of clinical interest because additional weakening by resection of cortical bone can sometimes be ill-advised in cases of already diminished structures as in bony defects of the skull or severely atrophied edentulous alveolar ridges. This study therefore was carried out to investigate the reactions of bone and periosteum to subperiosteally implanted hydroxyapatite. Materials
and methods
Calcium hydroxyapatite ceramic (HEYL, Berlin (West), FRG) of two different types was used: l) densely sintered with micropores of approxi-
24
E Fischer-Brandies et al.
Diagram of Implantation external sagittal additional
~
interpasitioning
e~
~
crest
~
parietalbone
denseceramic
porousceramic
Figure 1 Diagramof subperiosteal implantation of denseand porous hydroxyapatitediscs on parietal bone.
mately 1 #m diameter and a total porosity of about 3~o, and 2) porously sintered with coarse interconnecting pores exceeding 100 ffm in diameter and a total porosity of 30-35~o.
Results
No postoperative complications occurred in the animal experiments. With light microscopy, foreign body reactions or fibrous tissue encapsulation were not detectable. Even though the hydroxyapatite discs were not To determine the reactions of the unreamed corticalls, porous and dense discs (diameter 8.5 mm; inserted fiat on the parietal bone, all specimens thickness 1.5 mm) were implanted under general showed a continuous, direct bond between the disc anaesthesia with sodium pentobarbital and the bone. Lamellar bone, originating from the (Nembutalg; 0.5 ml/kg BW) in four one-year-old cortical bone, had filled the former gap between German shepherd dogs. Starting at a median disc and bone surface after 14 weeks (Figure 2). In incision, the parietal bone periosteum was pushed the five months specimen bone tissue had also back on both sides of the internal sagittal crest and grown up against the edges of the disc. Bone growth four discs per animal were inserted on the unreamed was considerably more advanced in the gap between bone according to Figure 1. On one side, lyophilized two adjacent implants than at the edges of the dura (LyoduraR; B Braun, Melsungen, FRG) was implants: the proliferated bone extended like the inserted between the disc and the periosteum, before cap of a mushroom on to the upper surface of the it was readapted. Wound closure was performed implant and the bone was in direct contact with the hydroxyapatite ceramic (Figure 3a). with single interrupted sutures. The implants were retrieved 14 weeks, 5, 8 and A time-dependent increase of bony ingrowth 10 months after insertion. After killing the animals occurred in pores of the macroporous material, with sodium pentobarbital (Nembutal~; 1.0 ml/kg beginning at the cortical bone. Predominantly body weight), the part of the parietal bone contain- loosely arranged fibrous tissue with capillaries and ing the implants was removed together with the little bone formation was present in the pores of soft tissue. The specimens were prepared for light the implants. After 8 to 10 months, the bone had microscopic evaluation as follows: fixation in a 3~o penetrated the interconnecting pores of the 1.5 mm solution of glutaraldehyde, dehydration with thick discs. The first osseous lamella was deposited acetone, embedding in araldite, cutting with a saw directly on the pore wall, bone apposition then microtome (1600, Leitz, Wetzlar, FRG, diamond advanced towards the centre of the pore in conwafering blade) into 50 to 60/~m thick sections, and centric lamellar arrangement (Figures 3b and 3c). Osteoclasts were rarely detectable. They were not staining with methylene blue.
Response of cortical bone to hydroxyapatite ceramic
25
Figure2 Cross section through denselysintered hydroxyapatiteceramic (HA) and parietal bone (P) at site, where disc was not lyi~g directly against bone. a) "~4 weeks implant. Note clearly defined proliferated bone (B). b) Eight-month implant. Note direct contact between proliferated bone (B) with t w o osteons and implant without a fibrous interfacial layer.
directly adjacent to the ceramic surface itself. Welldeveloped osteons were found in the pores of the discs implanted for at least five months. The orientation of the osteon corresponds to the pore (Figure 3c).
Ingrowth of bone proceeded through the larger pores (150 #m) up to the periosteal side of the implant, which thus became partially covered by bone. Independent of this process, bone formed on the periosteal side. This is revealed on the densely
26
E Fischer-Brandies
et al.
sintered material. After five months, this layer was composed of two to six osseous lamellae. No fibrous connective tissue layer is interposed. During processing of the non-decalcified boneceramic specimen for histologic evaluation fractures of the implant occurred due to the brittleness of the ceramic, but the implant remained in continuity with the bone. This indicates a direct bonding at the interfacial zone. The inserted LyoduraR (Braun, Melsungen) was
no longer reliably detectable after 14 weeks by light microscopy: the fibrous lamellae overlying the implant contained capillaries and fibrocytes, so that it cannot be differentiated from the periosteum. Discussion
Heling e t al. 7 and Levin e t al. 8 observed a nonspecific foreign body reaction and multinucleated 3a
3b
Response o f cortical bone to hydroxyapatite ceramic
27
3C
Figure3 Five month implants, a) Direct contact between proliferated bone and ceramic disc (HA). Bone has grown up into narrow gap between two discs, spreading out on implant surface like the cap of a mushroom, b) Ingrowth of loosely arranged fibrous tissue (F) with capillaries (C) into pores. Ossification began in the periphery of pore (arrow). c) Complete osteon (O) with the central vessel (H) having filled the entire pore.
giant cells in the immediate neighbourhood of the hydroxyapatite implant two to four weeks after implantation. These initial reactions to the surgical intervention and the foreign body had subsided in specimens retrieved after this time 5' 6, 7 Between endossally implanted hydroxyapatite and bone a direct contact usually forms within one to three months. Fibrous connective tissue as a sign of encapsulation is not observed L 5, 6, 7 in hydroxyapatite implants in continuity with cancellous bone. Our findings indicate that even with apposition of the implant only, a direct contact forms between the bone and the hydroxyapatite. Contrary to Kato et al. ~, we did not observe that this process advanced more rapidly in densely sintered material than in porous implants. As with the insertion of hydroxyapatite in a longitudinal osteotomy without dissection of continuity, primary direct contact is not necessary for the later formation of a strong bond, at least not in non-loaded implants. Within the same period, while the space between implant and cortical bone is penetrated by bone tissue, only few osseous lamellae form on the periosteal side. As Denissen et al. 9 also observed in rats, proliferated bone grows
up against the edges of the implant when the hydroxyapatite protrudes from the bone surface. In this way, the surface is levelled by integration of the implant. Bone ingrowth into porous surfaces has been described in different materials with pore sizes of at least 100 to 150 pm, e.g. metal 1~ plastic tl, aluminium oxide lo, tz, carbonX3, calcium carbonate 10, tricalcium phosphate s, and hydroxyapatitel 0. In agreement with K6ster et al. ~4 and Osborn et al. ~5, we also observed the ingrowth of loosely arranged, vascularized fibrous tissue into the pores of the implant, followed by direct bone formation. Cartilage was not detected. As is the case with other calcium phosphate ceramics, ossification begins at the periphery of the hydroxapatite pore, directly upon the ceramic. The findings are encouraging for the use for hydroxyapatite implants in humans for augmentation of bony structures. As the resistance of the material against bending forces is limited, the use of hydroxyapatite should be restricted to areas which are subjected to minimal tensile and shearing forces only. Direct placement on compact bone can be highly advantageous, since the operation is less
28
E Fischer-Brandies et al.
extensive and therefore less stressing for the patient. The use of autologous, homologous and allogenic materials in contour reconstructions often would be unnecessary for example. Valuable substance of already weak bone can be preserved in alveolar ridge augmentation of the mandible. Insertion of Lyodura R appears to have no positive or negative effect on healing. This procedure may be one way of improving the friction of denture bearing tissue and preventing injury to the mucosa, which is often extremely thin. Conclusions
1) When hydroxyapatite ceramic was implanted on unreamed cortical bone in the dog, newly formed bone enclosed the ceramic and penetrated its pores. 2) Direct contact without a connective tissue layer formed between this bone and the hydroxyapatite ceramic. 3) It can be concluded that bony integration of hydroxyapatite ceramic is possible when using this material for augmentation of bone structures without resection of cortical bone.
Acknowledgements We would like to express our appreciation to Prof. Dr W Brendel (Director of Institut fiir Chirurgische Forschung, University of Munich) for supporting the experimental work. We also want to thank HEYL, Chemisch-Pharmazeutische Fabrik, Berlin, for their aid.
4
5
6 7 8
9
10 11
12
13 References
1 Jarcho M, Kay JF, Gumaer KI, Doremus R J, Drobeck PP. Tissue, cellular and subcellular events at a bone-ceramic hydroxylapatite interface. J Bioeng 1977; 1: 79-92. 2 K6ster K, Karbe E, Kramer H, Heide H, K6nig R. Experimenteller Knochenersatz durch resorbierbare CalciumphosphatKeramik. Langenbeck's Arch Chir 1976; 341: 77 86. 3 Werhahn C, Osborn JF, Newesely H. Por6se Hydroxylapatitkeramik---ein osteotroper
14
15
Werkstoff ffir den Knochenersatz. Hefte Unfallheilkunde 1982; 158: 71-75. K6ster K, Heide H, K6nig R. Resorbierbare Calciumphosphatkeramik im Tierexperiment unter Belastung. Langenbeck's Arch Chir 1977; 343: 173-81. Finn RA, Bell WH, Brammer JA. Interpositional 'grafting' with autogenous bone and coralline hydroxyapatite. J Max-Fac Surg 1980; 8: 217-27. Frame JW, Browne RM, Brady CL. Hydroxyapatite as a bone substitute in the jaws. Biomaterials 1981; 2: 19-22. Heling I, Heindel R, Merin B. Calciumfluorapatite. A new material for bone implants. J Oral Implant 1981; 9: 548-55. Levin MP, Getter L, Cutright DE. A comparison of iliac marrow and biodegradable ceramic in periodontal defects. J Biomed Mat Res 1975; 9: 183-95. Denissen HW, de Groot K, Makkes PCh, van den Hooff A, Klopper PJ. Tissue response to dense apatite implants in rats. J Biomed Mat Res 1980; 14: 713-21. Chiroff RT, White EW, Weber JN, Roy DM. Tissue ingrowth of replamineform implants. J Biomed Mat Res Syrup 1975; 6: 29-45. Spector M, Fleming WR, Kreutner A, Sauer BW. Bone growth into parous high-density polyethylene. J Biomed Mat Res Syrup 1976; 7: 595-603. Klawitter JJ, Weinstein AM, Cooke FW, Peterson LJ, Pennel BM, McKinney RV. An evaluation of porous alumina ceramic dental implants. J Dent Res 1977; 56: 768-76. Weber U, Rettig H. Der Einsatz yon Kohlenstoff als Herstellungsmaterial yon Endoprothesen. Z Orthop 1979; 117: 268-76. K6ster K, Heide H, K6nig R. Histologische Untersuchungen an der Grenzfl/iche zwischen Knochengewebe und Calciumphosphat-, Calciumaluminat- und Aluminiumoxidkeramik. Z Orthorp 1977; 115: 693-99. Osborn JF, Covacs E, Kallenberger A. Hydroxylapatitkeramik--Entwicklung eines neuen Biowerkstoffes und erste tierexperimentelle Ergebnisse. Dtsch Zahn~rztl Z 1980; 35: 54-56.
The response of cortical bone to hydroxyapatite ceramic E Fischer-Brandies and E Dielert Department of Maxillofacial Surgery, University of Munich, FRG and FH Feder Department of Veterinary Histology and Embryology, University of Munich, FRG
Endosseus implantation is sometimes inadvisable if the bony structures are fragile. Therefore subperiosteal implantation of porous and dense hydroxyapatite ceramic implants on the unreamed parietal bone of four dogs was studied. During the investigated period of 1 4 weeks to 1 0 months the implant was surrounded by newly formed bone which grew up against the edges of the implant and penetrated the pores. A direct contact w i t h o u t a connective tissue layer formed between bone and hydroxyapatite. Few osseous lamellae developed on the side of the implant adjacent to the periosteum.
I ntroduction
Ceramics are increasingly becoming the subject of extensive research in the field of bone surgery. One of these materials, hydroxyapatite ceramic, is particularly interesting because its chemical composition is similar to that of the mineral substance of natural bone. Calcium phosphate ceramics with an apatite structure have been implanted in contact with cancellous bone, in the alveolus 1, in the femur diaphysis 2, 3, in long tubular bones as replacement of a resected bone tube stabilized by osteosynthesis using a plate and screws 3'4, and in the mandible applying the sandwich technique 5' 6. From these studies it is known that direct contact Address for correspondenceDr Dr E Fischer-Brandies,Department of Maxillofacial Surgery, University of Munich FRG, Lindwurmstr. 2a, 8000 Munchen 2, FRG.
between bone and endossally implanted hydroxyapatite ceramics will form, but there is a lack of information on the surface reactions of unreamed cortical bone to this material. The interposition of hydroxyapatite between cortical bone and periosteum can be of clinical interest because additional weakening by resection of cortical bone can sometimes be ill-advised in cases of already diminished structures as in bony defects of the skull or severely atrophied edentulous alveolar ridges. This study therefore was carried out to investigate the reactions of bone and periosteum to subperiosteally implanted hydroxyapatite. Materials
and methods
Calcium hydroxyapatite ceramic (HEYL, Berlin (West), FRG) of two different types was used: l) densely sintered with micropores of approxi-
24
E Fischer-Brandies et al.
Diagram of Implantation external sagittal additional
~
interpasitioning
e~
~
crest
~
parietalbone
denseceramic
porousceramic
Figure 1 Diagramof subperiosteal implantation of denseand porous hydroxyapatitediscs on parietal bone.
mately 1 #m diameter and a total porosity of about 3~o, and 2) porously sintered with coarse interconnecting pores exceeding 100 ffm in diameter and a total porosity of 30-35~o.
Results
No postoperative complications occurred in the animal experiments. With light microscopy, foreign body reactions or fibrous tissue encapsulation were not detectable. Even though the hydroxyapatite discs were not To determine the reactions of the unreamed corticalls, porous and dense discs (diameter 8.5 mm; inserted fiat on the parietal bone, all specimens thickness 1.5 mm) were implanted under general showed a continuous, direct bond between the disc anaesthesia with sodium pentobarbital and the bone. Lamellar bone, originating from the (Nembutalg; 0.5 ml/kg BW) in four one-year-old cortical bone, had filled the former gap between German shepherd dogs. Starting at a median disc and bone surface after 14 weeks (Figure 2). In incision, the parietal bone periosteum was pushed the five months specimen bone tissue had also back on both sides of the internal sagittal crest and grown up against the edges of the disc. Bone growth four discs per animal were inserted on the unreamed was considerably more advanced in the gap between bone according to Figure 1. On one side, lyophilized two adjacent implants than at the edges of the dura (LyoduraR; B Braun, Melsungen, FRG) was implants: the proliferated bone extended like the inserted between the disc and the periosteum, before cap of a mushroom on to the upper surface of the it was readapted. Wound closure was performed implant and the bone was in direct contact with the hydroxyapatite ceramic (Figure 3a). with single interrupted sutures. The implants were retrieved 14 weeks, 5, 8 and A time-dependent increase of bony ingrowth 10 months after insertion. After killing the animals occurred in pores of the macroporous material, with sodium pentobarbital (Nembutal~; 1.0 ml/kg beginning at the cortical bone. Predominantly body weight), the part of the parietal bone contain- loosely arranged fibrous tissue with capillaries and ing the implants was removed together with the little bone formation was present in the pores of soft tissue. The specimens were prepared for light the implants. After 8 to 10 months, the bone had microscopic evaluation as follows: fixation in a 3~o penetrated the interconnecting pores of the 1.5 mm solution of glutaraldehyde, dehydration with thick discs. The first osseous lamella was deposited acetone, embedding in araldite, cutting with a saw directly on the pore wall, bone apposition then microtome (1600, Leitz, Wetzlar, FRG, diamond advanced towards the centre of the pore in conwafering blade) into 50 to 60/~m thick sections, and centric lamellar arrangement (Figures 3b and 3c). Osteoclasts were rarely detectable. They were not staining with methylene blue.
Response of cortical bone to hydroxyapatite ceramic
25
Figure2 Cross section through denselysintered hydroxyapatiteceramic (HA) and parietal bone (P) at site, where disc was not lyi~g directly against bone. a) "~4 weeks implant. Note clearly defined proliferated bone (B). b) Eight-month implant. Note direct contact between proliferated bone (B) with t w o osteons and implant without a fibrous interfacial layer.
directly adjacent to the ceramic surface itself. Welldeveloped osteons were found in the pores of the discs implanted for at least five months. The orientation of the osteon corresponds to the pore (Figure 3c).
Ingrowth of bone proceeded through the larger pores (150 #m) up to the periosteal side of the implant, which thus became partially covered by bone. Independent of this process, bone formed on the periosteal side. This is revealed on the densely
26
E Fischer-Brandies
et al.
sintered material. After five months, this layer was composed of two to six osseous lamellae. No fibrous connective tissue layer is interposed. During processing of the non-decalcified boneceramic specimen for histologic evaluation fractures of the implant occurred due to the brittleness of the ceramic, but the implant remained in continuity with the bone. This indicates a direct bonding at the interfacial zone. The inserted LyoduraR (Braun, Melsungen) was
no longer reliably detectable after 14 weeks by light microscopy: the fibrous lamellae overlying the implant contained capillaries and fibrocytes, so that it cannot be differentiated from the periosteum. Discussion
Heling e t al. 7 and Levin e t al. 8 observed a nonspecific foreign body reaction and multinucleated 3a
3b
Response o f cortical bone to hydroxyapatite ceramic
27
3C
Figure3 Five month implants, a) Direct contact between proliferated bone and ceramic disc (HA). Bone has grown up into narrow gap between two discs, spreading out on implant surface like the cap of a mushroom, b) Ingrowth of loosely arranged fibrous tissue (F) with capillaries (C) into pores. Ossification began in the periphery of pore (arrow). c) Complete osteon (O) with the central vessel (H) having filled the entire pore.
giant cells in the immediate neighbourhood of the hydroxyapatite implant two to four weeks after implantation. These initial reactions to the surgical intervention and the foreign body had subsided in specimens retrieved after this time 5' 6, 7 Between endossally implanted hydroxyapatite and bone a direct contact usually forms within one to three months. Fibrous connective tissue as a sign of encapsulation is not observed L 5, 6, 7 in hydroxyapatite implants in continuity with cancellous bone. Our findings indicate that even with apposition of the implant only, a direct contact forms between the bone and the hydroxyapatite. Contrary to Kato et al. ~, we did not observe that this process advanced more rapidly in densely sintered material than in porous implants. As with the insertion of hydroxyapatite in a longitudinal osteotomy without dissection of continuity, primary direct contact is not necessary for the later formation of a strong bond, at least not in non-loaded implants. Within the same period, while the space between implant and cortical bone is penetrated by bone tissue, only few osseous lamellae form on the periosteal side. As Denissen et al. 9 also observed in rats, proliferated bone grows
up against the edges of the implant when the hydroxyapatite protrudes from the bone surface. In this way, the surface is levelled by integration of the implant. Bone ingrowth into porous surfaces has been described in different materials with pore sizes of at least 100 to 150 pm, e.g. metal 1~ plastic tl, aluminium oxide lo, tz, carbonX3, calcium carbonate 10, tricalcium phosphate s, and hydroxyapatitel 0. In agreement with K6ster et al. ~4 and Osborn et al. ~5, we also observed the ingrowth of loosely arranged, vascularized fibrous tissue into the pores of the implant, followed by direct bone formation. Cartilage was not detected. As is the case with other calcium phosphate ceramics, ossification begins at the periphery of the hydroxapatite pore, directly upon the ceramic. The findings are encouraging for the use for hydroxyapatite implants in humans for augmentation of bony structures. As the resistance of the material against bending forces is limited, the use of hydroxyapatite should be restricted to areas which are subjected to minimal tensile and shearing forces only. Direct placement on compact bone can be highly advantageous, since the operation is less
28
E Fischer-Brandies et al.
extensive and therefore less stressing for the patient. The use of autologous, homologous and allogenic materials in contour reconstructions often would be unnecessary for example. Valuable substance of already weak bone can be preserved in alveolar ridge augmentation of the mandible. Insertion of Lyodura R appears to have no positive or negative effect on healing. This procedure may be one way of improving the friction of denture bearing tissue and preventing injury to the mucosa, which is often extremely thin. Conclusions
1) When hydroxyapatite ceramic was implanted on unreamed cortical bone in the dog, newly formed bone enclosed the ceramic and penetrated its pores. 2) Direct contact without a connective tissue layer formed between this bone and the hydroxyapatite ceramic. 3) It can be concluded that bony integration of hydroxyapatite ceramic is possible when using this material for augmentation of bone structures without resection of cortical bone.
Acknowledgements We would like to express our appreciation to Prof. Dr W Brendel (Director of Institut fiir Chirurgische Forschung, University of Munich) for supporting the experimental work. We also want to thank HEYL, Chemisch-Pharmazeutische Fabrik, Berlin, for their aid.
4
5
6 7 8
9
10 11
12
13 References
1 Jarcho M, Kay JF, Gumaer KI, Doremus R J, Drobeck PP. Tissue, cellular and subcellular events at a bone-ceramic hydroxylapatite interface. J Bioeng 1977; 1: 79-92. 2 K6ster K, Karbe E, Kramer H, Heide H, K6nig R. Experimenteller Knochenersatz durch resorbierbare CalciumphosphatKeramik. Langenbeck's Arch Chir 1976; 341: 77 86. 3 Werhahn C, Osborn JF, Newesely H. Por6se Hydroxylapatitkeramik---ein osteotroper
14
15
Werkstoff ffir den Knochenersatz. Hefte Unfallheilkunde 1982; 158: 71-75. K6ster K, Heide H, K6nig R. Resorbierbare Calciumphosphatkeramik im Tierexperiment unter Belastung. Langenbeck's Arch Chir 1977; 343: 173-81. Finn RA, Bell WH, Brammer JA. Interpositional 'grafting' with autogenous bone and coralline hydroxyapatite. J Max-Fac Surg 1980; 8: 217-27. Frame JW, Browne RM, Brady CL. Hydroxyapatite as a bone substitute in the jaws. Biomaterials 1981; 2: 19-22. Heling I, Heindel R, Merin B. Calciumfluorapatite. A new material for bone implants. J Oral Implant 1981; 9: 548-55. Levin MP, Getter L, Cutright DE. A comparison of iliac marrow and biodegradable ceramic in periodontal defects. J Biomed Mat Res 1975; 9: 183-95. Denissen HW, de Groot K, Makkes PCh, van den Hooff A, Klopper PJ. Tissue response to dense apatite implants in rats. J Biomed Mat Res 1980; 14: 713-21. Chiroff RT, White EW, Weber JN, Roy DM. Tissue ingrowth of replamineform implants. J Biomed Mat Res Syrup 1975; 6: 29-45. Spector M, Fleming WR, Kreutner A, Sauer BW. Bone growth into parous high-density polyethylene. J Biomed Mat Res Syrup 1976; 7: 595-603. Klawitter JJ, Weinstein AM, Cooke FW, Peterson LJ, Pennel BM, McKinney RV. An evaluation of porous alumina ceramic dental implants. J Dent Res 1977; 56: 768-76. Weber U, Rettig H. Der Einsatz yon Kohlenstoff als Herstellungsmaterial yon Endoprothesen. Z Orthop 1979; 117: 268-76. K6ster K, Heide H, K6nig R. Histologische Untersuchungen an der Grenzfl/iche zwischen Knochengewebe und Calciumphosphat-, Calciumaluminat- und Aluminiumoxidkeramik. Z Orthorp 1977; 115: 693-99. Osborn JF, Covacs E, Kallenberger A. Hydroxylapatitkeramik--Entwicklung eines neuen Biowerkstoffes und erste tierexperimentelle Ergebnisse. Dtsch Zahn~rztl Z 1980; 35: 54-56.