SECTION
RESEARCH AND EDUCATION
Ahedar ridge aupusttation ceramic
EDITOR
JOHN J. SHARRY
ate
with t&d&m
Edmund0 B. Nery, O.M.D.,* Kenneth L. Lynch, Ph.D.,** and George E. Rooney, D,D.S.*** Wood Veterans Administration Wisconsin, Milwaukee, Wis.
Center,
Marquette
University,
T instability of the lower denture affects many ederitulous patients, usually because of poor construction and/or high muscle attachment. In patients where there is inadequate edentulous residual mandibular ridge, augmentation has been attempted with autogenous bone grafts or other derivatives.‘. 2 With this method, an extra surgical procedure is inevitable and certainly provokes unnecessary inconvenience to the patient. Allogeneic bone grafting has also been attempted, but this has proved to be impractical, since the problem of host incompatibility is usually encountered, especially when bone grafting is used on a large scale. Histologic evaluation of bone grafts has demonstrated that a large portion becomes necrotic, resorbedi and then replaced by new bone over a long period of time. Frequently this requires several years for complete replacement, and sometimes part of the resorbed graft is not replaced.3 To obviate these problems, a bioceramic material was introduced for alveolar ridge augmentation by Topazian, Hammer, and others.4. j In their experiments they concluded that porous aluminate ceramic is biologically inert and remains attached to the residual alveolar ridge for 12 months. Recently, however, it has been reported that the material I, Read before the Academy of Denture Prosthetics, San Antonio, Texas. *Chief, Dental Research, Veterans Administration Center, and Assistant Clinical Professor, Department of Periodontics, School of Dentistry, Marquette University. **Head, Orthopedic Research Laboratory, Veterans Administration Center, and Lecturer, Department of Orthopedic Surgery, The Medical College of Wisconsin. ***Chief, Dental Service, Veterans Administration Center, and Associate Professor, Department of Prosthodontics, School of Dentistry, Marquette University.
668
School
of Dentistry,
and The Medical
College
of
hydrates, thereby preventing “mineralization of surrounding osteoid tissue.“6 Others have used aluminum oxide with varying results. Pedersen’ discovered that 15 months after implantation, the ceramic was still covered by “normal” soft tissue and there was no evidence of bone resorption adjacent to the implant. On the other hand, Hammer and Klawitters found that bone resorption took place beneath the ceramic material. They concluded that, with their present method, the material was not acceptable for residual alveolar ridge augmentation. The purpose of the present study was to investigate, histologically and hematologically, a different type of bioceramic material for alveolar ridge augmentation. The ceramic is porous tricalcium phosphate, which is primarily of hydroxyapatite structure (Ca,, (OH), (PO&.8 It can be manufactured with different percentile pore volumes and pore sizes to allow for tissue ingrowth when implanted in the animal body. The material investigated in this report has a pore volume of 50% and a porosity size of 400 to 500 pm. A detailed description of this material in terms of fabrication, chemical composition, mechanical properties and short-term biodegradability, has been provided by Hubbard.8 In a study in which this ceramic was used in surgically produced infrabony defects, bone and soft tissue grew into the pores, and repair of the periodontium was clearly demonstrated.g The same material, with varying degrees of porosity, was implanted in the iliac crest of rabbits, and bone likewise grew into the pores in all trials, creating an excellent biomechanical bond. No observable degradation or resorption of the material was observed during the experimental period (12 weeks).‘O
DECEMBER
1978
VOLUME
40
NUMBER 6
ALVEOLAR RIDGE AUGMENTATION
Fig.
1.
Ceramic implant, C, being inserted into a mucoperiosteal tunnel (arrow)
MATERIALS AND METHODS Ten adult mongrel dogs were used in this study. Two dogs were utilized for each survival period (7, 30, 90, 180, and 360 days). Prior to alveolar ridge augmentation all mandibular posterior teeth on the *ht side were extracted and an alveoloplastic proce&re was performed using Nembutal* anesthesia. “Ke wound was then allowed to heal for 2 months. &I the opposite side of the mandible the teeth were untouched to maintain the occlusal stop, thus peventing or minimizing the forces that might be snerated on the implant during the animal’s rigid narasticatory function. After a 2-month healing period, blood was drawn for preimplantation SMA-12 blood chemistry studics. The animals were again anesthetized for the ianplant procedure. This was accomplished with an ismision across the ridge from buccal to lingual mtibular troughs. The incision, however, was made &way from the proposed implant site so that the implant material would be completely covered by an intact mucoperiosteal flap following closure of the wound. The incision was carried through the perios*urn, and the flap was separated from the bone with a periosteal elevator to form a tunnel, the depth of which was made deeper than the length of the
implant material (25 mm). With the flap elevated, the exposed cortical bone was severed with a dental round bur to allow the implant material to be in contact with the marrow spaces. The tunnel was then irrigated with normal saline solution, and the prepared ceramic, with dimensions of approximately 15 X 5 X 5 mm, was inserted. It was manipulated into the tunnel and seated on top of the decorticated bony alveolar ridge (Fig. 1). The inherent elastic property of the mucoperiosteal flap kept the implant in place. The incision was closed with interrupted 4-O silk sutures. Postoperatively, the dogs were given a soft diet ad libitum for 1 week followed by reguiar Dog Chow. Prior to sacrifice at different time intervals (7, 30, 90, 180, and 360 days) blood was again drawn for postoperative SMA-12 studies. At this time, while under general anesthesia, two dogs were perfused with a 30% solution of barium sulfate (Micropaque*) to determine the extent of vascular penetration. For histologic evaluation, the implants, as well as their surrounding tissues, were retrieved, fixed in 10% neutral formalin, and decalcified by ionic exchange resin decalcification. They were sectioned in a buccolingual plane at an 8 Pm thickness and stained with hemotoxylin and eosin.
*Abbott
*Picker X-Ray Corp., White Plains, N. Y.
Laboratories,
THE JOURNAL
Chicago, I11
OF PROSTHETIC
DENTISTRY
669
NERY, LYNCH,
AND
ROONEJ
Fig. 2. Seven-day ceramic implant, C, showing the initial ingrowth of fibrovascular tissue (arrows) into the pores. On the lateral and medial aspects of the mandible a form of exostosis (E) is found. (Original magnification, X 4.5.) To compare the the experimental group of animals selected at random
blood chemistry values between and control groups, a separate (11 adult mongrel dogs) were for controls.
RESULTS Uneventful healing occurred in all animals. By the implants were found manual manipulation, firmly attached to all surrounding tissues at the time of sacrifice. Seven days. Histologic evaluation of 7-day specimens demonstrated generalized nonspecific inflammatory response due to postsurgical trauma. The implant was completely covered by the overlying soft tissue at the crest and by the alveolar bone at the base (Fig. 2). Proliferating endothelial cells and fibroblasts grew superficially into the pores. A few hemorrhagic areas were also seen accompanied by fibrovascular growth (Fig. 3). Other pores contained amorphous eosinophilic substances resembling serous effusion. The alveolar tissue demonstrated bone remodeling, as evidenced by the presence of osteoblasts and multinucleated giant cells. In one specimen examined, new bone formation, which appeared to be exostosis, occurred on the lateral and
670
Fig. 3. Fibrovascular tissue, (FV), growing into one of the pores with accompanying hemorrhage, H, in a Y-day ceramic implant. (Original magnification, X 160.) medial aspects of the mandible (Fig. 2). However, they were located remotely from the implant site. This growth may be the result of uplifting of the periosteum during extraction and alveoloplasty prior to augmentation. No evidence of metaplastic changes was seen. Thirty days. At 30 days, inflammation had relatively subsided. Fibrovascular tissue, osteoid, and bone seams grew into the pores. Ingress of these tissues was deeper than the initial ingrowth, and surrounded the implant material (Fig. 4). At the central portion, pores were devoid of tissues. However, amorphous eosinophilic material had infiltrated. Occasionally, at different locations where fibrovascular tissues were found, multinucleated giant ceils were seen at the interface between the ceramic and the tissue. New bone showed a definite pattern of appositional growth and osteocytes entrapped in the matrix (Fig. 5). Progressive osteoblastic activity was evident.
DECEMBER
1978
VOLUME
40
NUMBER
6
ALVEOLAR RIDGE AUGMENTATION
hig. 4. Thirty-day ceramic implant, C, showing fibrovascular and osseoustissue growing into the pore, appearing on all sides of implant (arrows). (Original magnification,
Fig. 5. Bone seam, BS,growing into one of the pores of a SO-day-old implant with accompanying osteoblastic activity, OS. (Original magnification, X 160.)
x 4.5.)
Ninety days. At 90 days, a slow progressive increase of peripheral bone growth had occurred (Fig. 6) with maturation (Fig. 7). Areas devoid of bone or osteoid seams exhibited one of the following: (1) dense collagenous material, (2) proliferating fibroblasts and budding capillaries, or (3) amorphous eosinophilic material. In one specimen which was perfused with barium sulfate, there appeared to be penetration of the material into vascular channels with the pores (Fig. 8). One hundred eighty days. At this time a large portion of the ceramic implant was infiltrated by either osseous or soft tissue ingrowth (Fig. 9). The central portion of the implant remained essentially the same as described earlier. The soft tissue ingrowth consisted either of dense connective tissue or a loose fibrovascular type with proliferating endothelial cells. In some areas, multinucleated giant cells were found next to the ceramic material. The bone extending toward the center of the implant varied in
THE JOURNAL
OF PROSTHETIC
DENTISTRY
degree of calcification. Most of the matured bone was found at the periphery, which was in apposition with the surrounding soft tissue and the alveolar bone at the base of the implant. This relationship created an excellent biomechanical bond. The immature bone was found near the central portion and was usually accompanied by fibrovascular tissue and apparent osteoblastic activity. Three hundred sixty days. Little further progression of bone ingrowth was evident at 360 days (Fig. lo), but maturation of the osseous structure continued, because some progressive osteoblastic activity was still seen (Fig. 11). The base of the ceramic implant, infiltrated with new bone, appeared to be in continuity with the old alveolar bone. No histologic evidence of bone resorption was observed in this region. Preoperatively and postoperatively, these animals demonstrated no significant change in blood chemistry. Likewise, there was no significant difference
671
NERY, LYNCH, AND ROONEY
Fig. 6. Ninety-day ceramic implant, C, showing continual process of tissue ingrowth around it (arrows) and maturation of os5eousstructures. (Original magnification,
Fig. 7. Higher magnification of bone seam, BS, showing continued maturation with the osteocytes being entrapped in the matrix. The ceramic residue C, is also seen in apposition with bone seams. (Original magnification,
x 4.5.)
x 160.)
between the experimental and our randomly selected “normal” control adult mongrel dogs.
DISCUSSION The results of this investigation indicated that porous tricalcium phosphate ceramic is a potential material for residual alveolar ridge augmentation. It is inert and becomes firmly attached to the surrounding soft and osseous tissues with no evidence of alveolar bone resorption. The process of tissue penetration into the ceramic pores may be described as similar to the “normal” process of repair in wound healing. Immediately after implantation of the ceramic it is bathed with blood. Later, through inflammation and tissue edema, liberation of autolytic enzymes from the dead cells eliminates the necrotic tissue and erythrocytes that enter the pores. This is followed by migration and proliferation of the fibroblasts and vascularization. The fibroblasts mature and form a
672
dense collagenous network accompanied by osteoblastic activity, most likely brought about by the influence of the periosteum and bone. New bone is then formed, creating an excellent bond between the ceramic and surrounding soft and osseous tissues. It is interesting to note that migration and proliferation of cells and subsequent ossification does not take place simultaneously in all pores, as shown in our experimental models, but rather at different time intervals and locations. This may be explained by the fact that clearing away blood clots and/or necrotic tissue within the pores, through enzymatic and phagocytic processes, varies in time because of size and location of the material. In many instances, however, complete clearing is not accomplished, but cell migration and proliferation continue. Distance from viable tissue may also be a factor. In pores away from the surrounding tissue, ingrowth takes much longer than in those found near the periphery. As demonstrated in our 30-day specimen, the peripheral
DECEMBER 1978
VOLUME 90
NUMBER 6
ALVEOLAR
RIDGE AUGMENTATION
Bg. 8. Fibrovascular, FV, and osseous tissue, OS, e~cupying two of the ceramic pores. Perfused barium sulfate (B) may also be found within the blood vessles, indicating extrance of vascular channel into the pores. @Original magnification, X 160.) portion of the implant is primarily infiltrated with either fibrovascular or osseous structures or a combination of both, while the central portion is still devoid of these tissues. Only a noncellular amorphous eosinophilic substance, presumably a proteinaceous material showing evidence of a channel for connective tissue migration, is found in this area. Whether or not the material found in the central portion of the implant will become bone remains unanswered, since in the 360-day implantation period bone was not found in this area. It may be suggested that the blood supply has not yet reached that portion of the implant, and therefore osseous and soft tissue growth is unlikely to occur. It is obvious that the material was well tolerated by the tissues and remained firmly attached to the surrounding structures. However, two important questions arise: (1) How long will this material remain unresorbed? We assumed that it is resorbing at a very slow rate, thereby giving the bone growing
THE JOURNAL
OF PROSTHETIC
DENTISTRY
Fig. 9. One hundred eight-day ceramic implant, C. A large portion of ,the implant is infiltrated through its pores, either by osseous or soft tissue ingrowth (urrows). (Original magnification, X 4.5.)
into pores a chance to mature. (2) Since the purpose of residual alveolar ridge augmentation is to enhance the stability of dentures, how will the ceramic implant and the surrounding tissues react to occlusal forces generated from a denture during masticatory function? We are presently investigating these two questions with the hope of presenting some answers in the near future. In addition to supporting the tissue histocompatibility of this material, we have shown that there was no significant change in the blood chemistry of these animals preoperativeiy or postoperatively, nor was there any significant difference between blood chemistry results from the experimental and “normal” control dogs. From these results we have concluded that this tricalcium phosphate ceramic material is nontoxic. SUMMARY Tricalcium phosphate ceramic, with 50% porosity and 400 to 500 pm pore diameter, was used to augment the edentulous alveolar ridge of 10 adult
673
NERY, LYNCH, AND RGGNEY
Fig. 10. Three hundred sixty-day ceramic implant, C, showing a continual maturation of osseous tissue appearing around and within their pores (arrows). Note, however, that the extent of tissue penetration does not appear extensively progressed, but a good biomechanical bonding between ceramic and tissue is evident.‘(Original magnification, X 8.)
mongrel dogs. The implants were evaluated histologically at different time intervals (7, 30, 90, 180, and 360 days). Preoperative and postoperative blood chemistry studies were also evaluated. The results showed that, other than for the expected acute nonspecific inflammatory response due to the surgery, the material was well tolerated by the tissues and was nontoxic. Bone and soft tissues grew into the pores, thereby creating an excellent biomechanical bond between the ceramic implant and surrounding structures. Preoperative and postoperative blood chemistry studies demonstrated no significant change. We wish to express our appreciation to Dr. Walter M. Hirthe and Robert Hubbard, of the Marquette University School of Engineering, for supplying us with the ceramic material; to the Allen-Bradley Medical Science Laboratory for their help and cooperation in executing the experiment; to the Orthopedic Research Laboratory and Laboratory Service, Veterans Adminis-
674
Fig. 11. Higher magnification of matured bone within the pore as evidenced by entrapment of osteocytic cells, 0, and solidification of bone matrix. Continued osteoblastic activity, OS, is also evident. (Original magnification, X 160.)
tration Center, Wood, Wis., for their technical assistance; to David H. Wimmer and Carole Russell Hilmer for preparing the illustrations; and to Catherine A. Walther for her editorial assistance.
REFERENCES 1. Boyne, P. J., and Mickels, T. E.: Restoration of alveolar ridges by intramandibular transposition osseous grafting. J Oral Surg 26:569, 1968. 2. Yeager, J. E., and Boyne, P. J.: Use of bone homografts and autogenous marrow in restoration of edentuious alveolar ridges. J Oral Surg 27:185, 1969. 3. Ham, A. W., and Harris, W. R.: Repair and transplantation of bone. in Bourne, G. H. (editor): The Biochemistry and Physiology of Bone, Vol III, ed 2. New York, 1972, Academic Press, pp 337-399. 4. Top&an, R. G., Hammer, W. B., Talbert, C. O., and Hulbert, S. F.: The use of ceramics in augmentation and replacement of portions of the mandible. J Biomed Mater Res 6~311, 1972. 5. Hammer, W. B., Topazian, R. G., McKinney, R. V., Jr., and
DECEMBER 1978
VOLUME 40
NUMBER6
ALVEOLAR
6.
7.
8.
9.
RIDGE AUGMENTATION
Hulbert, S. F.: Alveolar ridge augmentation with ceramics. J Dent Res 52:356, 1973. Hammer, W. B., and Klawitter, J.: Porous aluminum oxide and high density polyethylene sponge for augmentation of the edentulous mandible. J Dent Res 55:171, 1976. (Abst). Pedersen, K. N.: Rebuilding of deficient edentulous alveolar ridge with porous ceramic implants. Int J Oral Surg 5:133, 1976. Hubbard, W.: Physiological Calcium Phosphate as Orthopedic Implant Material. Thesis, Marquette University, 1974. Nery, E. B., Lynch, K. L., Hirthe, W. M., and Mueller, K.
H.: Bioceramic implants in surgically produced infrabony defects. J Periodontol 46~328, 1975. 10. Lynch, K. L., Mueller, K. H., Hubbard, W. G., and Hirthe, W. M.: Porous physiological calcium phosphates in orthopedic biomaterials. Clin Orthop (In press;. Reprint requeststo: DR. EDMUNDO B. NERY VETERANS ADMINISTRATION
5000 W. NATIONAL
CENTER
AVE.
WOOD, WIS. 531%
ARTICLES TO APPEAR IN FUTURE ISSUES Biwompatibility
evaluation
of casting alloys in hamsters
S. J. Piliero, Ph.D., S. Carson, Ph.D., M. LiCalzi, D.D.S., L. Pentel, D.D.S., J. A. Piliero, E. G. Kaufman, D.D.S., A. Schulman, D.D.S., M.S., and D. A. Willigan, D.V.M., Ph.D.
Pulpal response to cooling armamentaria Alfred
Schuchard.
Clinical Barry
speed
D.D.S.
evaluation
Shipman,
at ultrahigh
A.B.,
of oral Cata&& in cancer chemotherapy
patients
D.M.D.
The efficacy of remount procedures using masticatory performance tests A. B. Sidhaye,
THE JOURNAL
OF PROSTHETIC
M.D.S.,
and S. B. Master,
DENTISTRY
B.Sc., M.D.S.
675
RESEARCH AND EDUCATION
Ahedar ridge aupusttation ceramic
EDITOR
JOHN J. SHARRY
ate
with t&d&m
Edmund0 B. Nery, O.M.D.,* Kenneth L. Lynch, Ph.D.,** and George E. Rooney, D,D.S.*** Wood Veterans Administration Wisconsin, Milwaukee, Wis.
Center,
Marquette
University,
T instability of the lower denture affects many ederitulous patients, usually because of poor construction and/or high muscle attachment. In patients where there is inadequate edentulous residual mandibular ridge, augmentation has been attempted with autogenous bone grafts or other derivatives.‘. 2 With this method, an extra surgical procedure is inevitable and certainly provokes unnecessary inconvenience to the patient. Allogeneic bone grafting has also been attempted, but this has proved to be impractical, since the problem of host incompatibility is usually encountered, especially when bone grafting is used on a large scale. Histologic evaluation of bone grafts has demonstrated that a large portion becomes necrotic, resorbedi and then replaced by new bone over a long period of time. Frequently this requires several years for complete replacement, and sometimes part of the resorbed graft is not replaced.3 To obviate these problems, a bioceramic material was introduced for alveolar ridge augmentation by Topazian, Hammer, and others.4. j In their experiments they concluded that porous aluminate ceramic is biologically inert and remains attached to the residual alveolar ridge for 12 months. Recently, however, it has been reported that the material I, Read before the Academy of Denture Prosthetics, San Antonio, Texas. *Chief, Dental Research, Veterans Administration Center, and Assistant Clinical Professor, Department of Periodontics, School of Dentistry, Marquette University. **Head, Orthopedic Research Laboratory, Veterans Administration Center, and Lecturer, Department of Orthopedic Surgery, The Medical College of Wisconsin. ***Chief, Dental Service, Veterans Administration Center, and Associate Professor, Department of Prosthodontics, School of Dentistry, Marquette University.
668
School
of Dentistry,
and The Medical
College
of
hydrates, thereby preventing “mineralization of surrounding osteoid tissue.“6 Others have used aluminum oxide with varying results. Pedersen’ discovered that 15 months after implantation, the ceramic was still covered by “normal” soft tissue and there was no evidence of bone resorption adjacent to the implant. On the other hand, Hammer and Klawitters found that bone resorption took place beneath the ceramic material. They concluded that, with their present method, the material was not acceptable for residual alveolar ridge augmentation. The purpose of the present study was to investigate, histologically and hematologically, a different type of bioceramic material for alveolar ridge augmentation. The ceramic is porous tricalcium phosphate, which is primarily of hydroxyapatite structure (Ca,, (OH), (PO&.8 It can be manufactured with different percentile pore volumes and pore sizes to allow for tissue ingrowth when implanted in the animal body. The material investigated in this report has a pore volume of 50% and a porosity size of 400 to 500 pm. A detailed description of this material in terms of fabrication, chemical composition, mechanical properties and short-term biodegradability, has been provided by Hubbard.8 In a study in which this ceramic was used in surgically produced infrabony defects, bone and soft tissue grew into the pores, and repair of the periodontium was clearly demonstrated.g The same material, with varying degrees of porosity, was implanted in the iliac crest of rabbits, and bone likewise grew into the pores in all trials, creating an excellent biomechanical bond. No observable degradation or resorption of the material was observed during the experimental period (12 weeks).‘O
DECEMBER
1978
VOLUME
40
NUMBER 6
ALVEOLAR RIDGE AUGMENTATION
Fig.
1.
Ceramic implant, C, being inserted into a mucoperiosteal tunnel (arrow)
MATERIALS AND METHODS Ten adult mongrel dogs were used in this study. Two dogs were utilized for each survival period (7, 30, 90, 180, and 360 days). Prior to alveolar ridge augmentation all mandibular posterior teeth on the *ht side were extracted and an alveoloplastic proce&re was performed using Nembutal* anesthesia. “Ke wound was then allowed to heal for 2 months. &I the opposite side of the mandible the teeth were untouched to maintain the occlusal stop, thus peventing or minimizing the forces that might be snerated on the implant during the animal’s rigid narasticatory function. After a 2-month healing period, blood was drawn for preimplantation SMA-12 blood chemistry studics. The animals were again anesthetized for the ianplant procedure. This was accomplished with an ismision across the ridge from buccal to lingual mtibular troughs. The incision, however, was made &way from the proposed implant site so that the implant material would be completely covered by an intact mucoperiosteal flap following closure of the wound. The incision was carried through the perios*urn, and the flap was separated from the bone with a periosteal elevator to form a tunnel, the depth of which was made deeper than the length of the
implant material (25 mm). With the flap elevated, the exposed cortical bone was severed with a dental round bur to allow the implant material to be in contact with the marrow spaces. The tunnel was then irrigated with normal saline solution, and the prepared ceramic, with dimensions of approximately 15 X 5 X 5 mm, was inserted. It was manipulated into the tunnel and seated on top of the decorticated bony alveolar ridge (Fig. 1). The inherent elastic property of the mucoperiosteal flap kept the implant in place. The incision was closed with interrupted 4-O silk sutures. Postoperatively, the dogs were given a soft diet ad libitum for 1 week followed by reguiar Dog Chow. Prior to sacrifice at different time intervals (7, 30, 90, 180, and 360 days) blood was again drawn for postoperative SMA-12 studies. At this time, while under general anesthesia, two dogs were perfused with a 30% solution of barium sulfate (Micropaque*) to determine the extent of vascular penetration. For histologic evaluation, the implants, as well as their surrounding tissues, were retrieved, fixed in 10% neutral formalin, and decalcified by ionic exchange resin decalcification. They were sectioned in a buccolingual plane at an 8 Pm thickness and stained with hemotoxylin and eosin.
*Abbott
*Picker X-Ray Corp., White Plains, N. Y.
Laboratories,
THE JOURNAL
Chicago, I11
OF PROSTHETIC
DENTISTRY
669
NERY, LYNCH,
AND
ROONEJ
Fig. 2. Seven-day ceramic implant, C, showing the initial ingrowth of fibrovascular tissue (arrows) into the pores. On the lateral and medial aspects of the mandible a form of exostosis (E) is found. (Original magnification, X 4.5.) To compare the the experimental group of animals selected at random
blood chemistry values between and control groups, a separate (11 adult mongrel dogs) were for controls.
RESULTS Uneventful healing occurred in all animals. By the implants were found manual manipulation, firmly attached to all surrounding tissues at the time of sacrifice. Seven days. Histologic evaluation of 7-day specimens demonstrated generalized nonspecific inflammatory response due to postsurgical trauma. The implant was completely covered by the overlying soft tissue at the crest and by the alveolar bone at the base (Fig. 2). Proliferating endothelial cells and fibroblasts grew superficially into the pores. A few hemorrhagic areas were also seen accompanied by fibrovascular growth (Fig. 3). Other pores contained amorphous eosinophilic substances resembling serous effusion. The alveolar tissue demonstrated bone remodeling, as evidenced by the presence of osteoblasts and multinucleated giant cells. In one specimen examined, new bone formation, which appeared to be exostosis, occurred on the lateral and
670
Fig. 3. Fibrovascular tissue, (FV), growing into one of the pores with accompanying hemorrhage, H, in a Y-day ceramic implant. (Original magnification, X 160.) medial aspects of the mandible (Fig. 2). However, they were located remotely from the implant site. This growth may be the result of uplifting of the periosteum during extraction and alveoloplasty prior to augmentation. No evidence of metaplastic changes was seen. Thirty days. At 30 days, inflammation had relatively subsided. Fibrovascular tissue, osteoid, and bone seams grew into the pores. Ingress of these tissues was deeper than the initial ingrowth, and surrounded the implant material (Fig. 4). At the central portion, pores were devoid of tissues. However, amorphous eosinophilic material had infiltrated. Occasionally, at different locations where fibrovascular tissues were found, multinucleated giant ceils were seen at the interface between the ceramic and the tissue. New bone showed a definite pattern of appositional growth and osteocytes entrapped in the matrix (Fig. 5). Progressive osteoblastic activity was evident.
DECEMBER
1978
VOLUME
40
NUMBER
6
ALVEOLAR RIDGE AUGMENTATION
hig. 4. Thirty-day ceramic implant, C, showing fibrovascular and osseoustissue growing into the pore, appearing on all sides of implant (arrows). (Original magnification,
Fig. 5. Bone seam, BS,growing into one of the pores of a SO-day-old implant with accompanying osteoblastic activity, OS. (Original magnification, X 160.)
x 4.5.)
Ninety days. At 90 days, a slow progressive increase of peripheral bone growth had occurred (Fig. 6) with maturation (Fig. 7). Areas devoid of bone or osteoid seams exhibited one of the following: (1) dense collagenous material, (2) proliferating fibroblasts and budding capillaries, or (3) amorphous eosinophilic material. In one specimen which was perfused with barium sulfate, there appeared to be penetration of the material into vascular channels with the pores (Fig. 8). One hundred eighty days. At this time a large portion of the ceramic implant was infiltrated by either osseous or soft tissue ingrowth (Fig. 9). The central portion of the implant remained essentially the same as described earlier. The soft tissue ingrowth consisted either of dense connective tissue or a loose fibrovascular type with proliferating endothelial cells. In some areas, multinucleated giant cells were found next to the ceramic material. The bone extending toward the center of the implant varied in
THE JOURNAL
OF PROSTHETIC
DENTISTRY
degree of calcification. Most of the matured bone was found at the periphery, which was in apposition with the surrounding soft tissue and the alveolar bone at the base of the implant. This relationship created an excellent biomechanical bond. The immature bone was found near the central portion and was usually accompanied by fibrovascular tissue and apparent osteoblastic activity. Three hundred sixty days. Little further progression of bone ingrowth was evident at 360 days (Fig. lo), but maturation of the osseous structure continued, because some progressive osteoblastic activity was still seen (Fig. 11). The base of the ceramic implant, infiltrated with new bone, appeared to be in continuity with the old alveolar bone. No histologic evidence of bone resorption was observed in this region. Preoperatively and postoperatively, these animals demonstrated no significant change in blood chemistry. Likewise, there was no significant difference
671
NERY, LYNCH, AND ROONEY
Fig. 6. Ninety-day ceramic implant, C, showing continual process of tissue ingrowth around it (arrows) and maturation of os5eousstructures. (Original magnification,
Fig. 7. Higher magnification of bone seam, BS, showing continued maturation with the osteocytes being entrapped in the matrix. The ceramic residue C, is also seen in apposition with bone seams. (Original magnification,
x 4.5.)
x 160.)
between the experimental and our randomly selected “normal” control adult mongrel dogs.
DISCUSSION The results of this investigation indicated that porous tricalcium phosphate ceramic is a potential material for residual alveolar ridge augmentation. It is inert and becomes firmly attached to the surrounding soft and osseous tissues with no evidence of alveolar bone resorption. The process of tissue penetration into the ceramic pores may be described as similar to the “normal” process of repair in wound healing. Immediately after implantation of the ceramic it is bathed with blood. Later, through inflammation and tissue edema, liberation of autolytic enzymes from the dead cells eliminates the necrotic tissue and erythrocytes that enter the pores. This is followed by migration and proliferation of the fibroblasts and vascularization. The fibroblasts mature and form a
672
dense collagenous network accompanied by osteoblastic activity, most likely brought about by the influence of the periosteum and bone. New bone is then formed, creating an excellent bond between the ceramic and surrounding soft and osseous tissues. It is interesting to note that migration and proliferation of cells and subsequent ossification does not take place simultaneously in all pores, as shown in our experimental models, but rather at different time intervals and locations. This may be explained by the fact that clearing away blood clots and/or necrotic tissue within the pores, through enzymatic and phagocytic processes, varies in time because of size and location of the material. In many instances, however, complete clearing is not accomplished, but cell migration and proliferation continue. Distance from viable tissue may also be a factor. In pores away from the surrounding tissue, ingrowth takes much longer than in those found near the periphery. As demonstrated in our 30-day specimen, the peripheral
DECEMBER 1978
VOLUME 90
NUMBER 6
ALVEOLAR
RIDGE AUGMENTATION
Bg. 8. Fibrovascular, FV, and osseous tissue, OS, e~cupying two of the ceramic pores. Perfused barium sulfate (B) may also be found within the blood vessles, indicating extrance of vascular channel into the pores. @Original magnification, X 160.) portion of the implant is primarily infiltrated with either fibrovascular or osseous structures or a combination of both, while the central portion is still devoid of these tissues. Only a noncellular amorphous eosinophilic substance, presumably a proteinaceous material showing evidence of a channel for connective tissue migration, is found in this area. Whether or not the material found in the central portion of the implant will become bone remains unanswered, since in the 360-day implantation period bone was not found in this area. It may be suggested that the blood supply has not yet reached that portion of the implant, and therefore osseous and soft tissue growth is unlikely to occur. It is obvious that the material was well tolerated by the tissues and remained firmly attached to the surrounding structures. However, two important questions arise: (1) How long will this material remain unresorbed? We assumed that it is resorbing at a very slow rate, thereby giving the bone growing
THE JOURNAL
OF PROSTHETIC
DENTISTRY
Fig. 9. One hundred eight-day ceramic implant, C. A large portion of ,the implant is infiltrated through its pores, either by osseous or soft tissue ingrowth (urrows). (Original magnification, X 4.5.)
into pores a chance to mature. (2) Since the purpose of residual alveolar ridge augmentation is to enhance the stability of dentures, how will the ceramic implant and the surrounding tissues react to occlusal forces generated from a denture during masticatory function? We are presently investigating these two questions with the hope of presenting some answers in the near future. In addition to supporting the tissue histocompatibility of this material, we have shown that there was no significant change in the blood chemistry of these animals preoperativeiy or postoperatively, nor was there any significant difference between blood chemistry results from the experimental and “normal” control dogs. From these results we have concluded that this tricalcium phosphate ceramic material is nontoxic. SUMMARY Tricalcium phosphate ceramic, with 50% porosity and 400 to 500 pm pore diameter, was used to augment the edentulous alveolar ridge of 10 adult
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NERY, LYNCH, AND RGGNEY
Fig. 10. Three hundred sixty-day ceramic implant, C, showing a continual maturation of osseous tissue appearing around and within their pores (arrows). Note, however, that the extent of tissue penetration does not appear extensively progressed, but a good biomechanical bonding between ceramic and tissue is evident.‘(Original magnification, X 8.)
mongrel dogs. The implants were evaluated histologically at different time intervals (7, 30, 90, 180, and 360 days). Preoperative and postoperative blood chemistry studies were also evaluated. The results showed that, other than for the expected acute nonspecific inflammatory response due to the surgery, the material was well tolerated by the tissues and was nontoxic. Bone and soft tissues grew into the pores, thereby creating an excellent biomechanical bond between the ceramic implant and surrounding structures. Preoperative and postoperative blood chemistry studies demonstrated no significant change. We wish to express our appreciation to Dr. Walter M. Hirthe and Robert Hubbard, of the Marquette University School of Engineering, for supplying us with the ceramic material; to the Allen-Bradley Medical Science Laboratory for their help and cooperation in executing the experiment; to the Orthopedic Research Laboratory and Laboratory Service, Veterans Adminis-
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Fig. 11. Higher magnification of matured bone within the pore as evidenced by entrapment of osteocytic cells, 0, and solidification of bone matrix. Continued osteoblastic activity, OS, is also evident. (Original magnification, X 160.)
tration Center, Wood, Wis., for their technical assistance; to David H. Wimmer and Carole Russell Hilmer for preparing the illustrations; and to Catherine A. Walther for her editorial assistance.
REFERENCES 1. Boyne, P. J., and Mickels, T. E.: Restoration of alveolar ridges by intramandibular transposition osseous grafting. J Oral Surg 26:569, 1968. 2. Yeager, J. E., and Boyne, P. J.: Use of bone homografts and autogenous marrow in restoration of edentuious alveolar ridges. J Oral Surg 27:185, 1969. 3. Ham, A. W., and Harris, W. R.: Repair and transplantation of bone. in Bourne, G. H. (editor): The Biochemistry and Physiology of Bone, Vol III, ed 2. New York, 1972, Academic Press, pp 337-399. 4. Top&an, R. G., Hammer, W. B., Talbert, C. O., and Hulbert, S. F.: The use of ceramics in augmentation and replacement of portions of the mandible. J Biomed Mater Res 6~311, 1972. 5. Hammer, W. B., Topazian, R. G., McKinney, R. V., Jr., and
DECEMBER 1978
VOLUME 40
NUMBER6
ALVEOLAR
6.
7.
8.
9.
RIDGE AUGMENTATION
Hulbert, S. F.: Alveolar ridge augmentation with ceramics. J Dent Res 52:356, 1973. Hammer, W. B., and Klawitter, J.: Porous aluminum oxide and high density polyethylene sponge for augmentation of the edentulous mandible. J Dent Res 55:171, 1976. (Abst). Pedersen, K. N.: Rebuilding of deficient edentulous alveolar ridge with porous ceramic implants. Int J Oral Surg 5:133, 1976. Hubbard, W.: Physiological Calcium Phosphate as Orthopedic Implant Material. Thesis, Marquette University, 1974. Nery, E. B., Lynch, K. L., Hirthe, W. M., and Mueller, K.
H.: Bioceramic implants in surgically produced infrabony defects. J Periodontol 46~328, 1975. 10. Lynch, K. L., Mueller, K. H., Hubbard, W. G., and Hirthe, W. M.: Porous physiological calcium phosphates in orthopedic biomaterials. Clin Orthop (In press;. Reprint requeststo: DR. EDMUNDO B. NERY VETERANS ADMINISTRATION
5000 W. NATIONAL
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ARTICLES TO APPEAR IN FUTURE ISSUES Biwompatibility
evaluation
of casting alloys in hamsters
S. J. Piliero, Ph.D., S. Carson, Ph.D., M. LiCalzi, D.D.S., L. Pentel, D.D.S., J. A. Piliero, E. G. Kaufman, D.D.S., A. Schulman, D.D.S., M.S., and D. A. Willigan, D.V.M., Ph.D.
Pulpal response to cooling armamentaria Alfred
Schuchard.
Clinical Barry
speed
D.D.S.
evaluation
Shipman,
at ultrahigh
A.B.,
of oral Cata&& in cancer chemotherapy
patients
D.M.D.
The efficacy of remount procedures using masticatory performance tests A. B. Sidhaye,
THE JOURNAL
OF PROSTHETIC
M.D.S.,
and S. B. Master,
DENTISTRY
B.Sc., M.D.S.
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