CROBM 1992 Mellonig 333 52

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Autogenous and Allogeneic Bone Grafts in Periodontal Therapy
James T. Mellonig CROBM 1992 3: 333 DOI: 10.1177/10454411920030040201
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Critical Reviews in Oral Biology and Medicine, 3(4):333-352 (1992)
Autogenous and Allogeneic Bone Grafts in Periodontal Therapy

James T. Mellonig, D.D.S., M.S.
Department of Periodontics, The University of Texas, Health Science Center, San Antonio, TX 78284
ABSTRACT: This article is limited to a review of bone autografts and allografts, as used in periodontal therapy. The various graft materials are discussed with respect to case reports, controlled clinical trials, and human histology. Other reviewed areas are wound healing with periodontal bone grafts, tissue banking and freeze-dried bone allografts, and the use of bone grafts in guided tissue regeneration. KEY WORDS: Periodontal, bone autograft, bone allograft, tissue banking, guided tissue regeneration.
I. INTRODUCTION Bacterially induced periodontitis leads to the destruction of tooth-supporting tissues, culminating in tooth loss. Disease reversal with regeneration of new bone, cementum, and periodontal ligament about a root surface previously contaminated by bacterial plaque is the ultimate goal of periodontal therapy. Bone grafts, both autogenous and allogeneic, are felt by some to be essential if restoration of lost bone accompanied by a functional attachment apparatus is to be achieved. "Bone grafting materials will enhance regeneration of a new attachment apparatus" (Bowers et aL, 1989c). "Osseous grafting therapy has been shown to be clinically successful for time intervals exceeding 20 years when encompassed in a comprehensive care program based on effective daily plaque control by the patient and a professionally supervised periodontal maintenance program" (Schallhorn, 1980). Others believe that the use of bone grafts to enhance regeneration of the periodontium is unacceptable. ' 'Not one of the human implant studies has provided the type of experimental model that clearly demonstrates new attachment formation. Many of the investigators have failed to provide controls, and none have provided the unequivocal histologic evidence of new attachment to previously diseased roots" (Gara and Adams, 1981). "From the standpoint of scientific documentation, the value (of regenerative procedures) is not clear. Spectacular results of "bone fill" in intrabony pockets have been reported with or without bone implantation" (Ramfjord, 1984). Still others are convinced that bone grafts are detrimental. "Ignorance of the contribution of the various tissue components in periodontal wound healing may explain the widespread use of bone transplants in the treatment of intrabony pockets" (Karing et aL, 1984). "Since granulation tissue derived from bone has the potential to induce root resorption and ankylosis, the rationale of favoring bone growth with the use of bone transplants is highly questionable" (Karring etaL, 1980). Clinical case reports, controlled clinical trials, and human histology documenting the results with bone grafts have been reviewed previously (Pfei- fer, 1969; Groff, 1976a and b; Ellegaard, 1976; Schallhorn, 1977; Schallhorn, 1980; Mellonig, 1980; Wirthlin, 1981; Gara and Adams, 1981;
1045-4411/92/$.50 1992 by CRC Press, Inc.
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Bowers et ai, 1982; Pierce, 1982; Diaz-Arnold and Zach, 1985; Gonsalez, 1986; Mellonig, 1986; Yazdi and Schonfeld, 1987; Egelberg, 1987; Krejci and Farah, 1987; Wiseman and Tenebaum, 1988; Hancock, 1989; Mellonig and Bow- ers, 1990; Mellonig, 1991). The purpose of this article is to evaluate the literature in an attempt to clarify the current state of the art of regeneration with periodontal bone graft therapy.
II. TERMINOLOGY The definitions provided here are adapted from the American Academy of Periodontology's Glossary of Periodontic Terms. Regeneration is the reproduction or recon- stitution of a lost or injured part. As applied to periodontics, it means the formation of new bone, cementum, and periodontal ligament on a previously diseased root surface. At one time the terms regeneration and new attachment were synonymous. Today, new attachment means the reunion of connective tissue with a root surface that has been deprived of its periodontal ligament. This reunion occurs by the formation of new cementum with inserting collagen fibers. The formation of new bone is not necessarily a condition of new attachment. In addition, new attachment to a root surface may be mediated through epithelial adhesion (junctional epithelium) or connective tissue adhesion. Likewise, in the past, the terms new attachment and reattachment were often used interchangeably. Reattachment means to attach again, the reunion of connective tissue with a root surface on which viable periodontal tissue is present. The area of reattachment is not affected by bacterial contamination. Attachment apparatus refers to the cementum, the alveolar bone, and the periodontal ligament. Repair is the healing of a wound by tissue that does not fully restore the architecture or function of the part. Bone fill is the presence of hard tissue in a periodontal osseous defect, as determined by clinical re-entry of the original defect site. This term does not indicate the nature of the histologic attachment to the tooth. The amount of bone fill is usually determined by surgical reentry procedures. Intraosseous (intrabony) refers to a periodontal defect within bone. An autograft is a tissue graft (bone) trans- ferred from one position to a new position in the same individual. An allograft (homograft) is a tissue graft (bone) between individuals of the same species but with nonidentical genetic composition. A xenograft (heterograft) is a tissue graft between members of different species. III. PERIODONTAL BONE GRAFTS: HISTORICAL PERSPECTIVE The use of bone grafts in periodontal therapy can be traced to the work of Hegedus (1923). He reported success in six cases by transplanting autogenous bone from the tibia to the jaws to treat "advanced pyorrhea". Subsequent to this report and for the next several decades, the evaluation of xenografts of various types became the main focus of attention. Buebe and Silvers (1936) used boiled cow bone powder to successfully repair intrabony defects in humans. Studies in dogs (Beube, 1934 and 1942) suggested that surgically created periodontal defects had an accelerated rate of healing after placement of boiled cow bone powder, with bone and cementum being deposited more rapidly in grafted defects. Os purum is ox bone that is soaked in po- tassium hydroxide to remove collagen, in acetone to remove lipid, and in a salt solution to remove proteins. Forsberg (1956) used this material in 11 human intrabony defects. One showed excel- lent results, seven were satisfactory, and three were unsatisfactory. Anorganic bone is bovine bone from which the organic material is extracted by means of
ethylenediamine and autoclaved. Melcher (1962) grafted 187 bone defects in 163 patients with a minimum follow-up of 3 years. He felt that pro- tracted sequestration and slow resorbtion miti- gated against the use of anorganic bone. Patur and Glickman (1962) found similar results. Boplant is bovine bone that is prepared by detergent extraction, chloroform methanol ex334
traction to reduce lipid content, sterilization in propiolactone, and freeze drying. In 77 intraosseous defects in 56 patients, Scopp et al (1966) reported pocket depth reduction of 3 mm at 6 months and an additional millimeter after 1 year. Older (1967) reported good results in four cases, fair results in three, and unsuccessful results in two, as measured by probing depth reduction and increasing radiographic density. The widespread clinical use that followed these reports resulted in routine rejection and failure (Emmings, 1974). Boplant was subsequently withdrawn from the market (Emmings, 1974). IV. CASE REPORTS AND CONTROLLED CLINICAL TRIALS WITH AUTOGENOUS AND ALLOGENEIC BONE GRAFTS Case reports document the clinical success or failure of a therapeutic procedure, provide information on technique sensitivity, and may stimulate research into the validity of the procedure. They have scientific value only when a large number of cases are reported and become anec- dotal when published as isolated procedures. In addition, the repeatability of results, as reported by a significant number of investigators, lends credence to clinical predictability. Because early bone graft literature was concerned mainly with clinical feasibility and technique, comparisons with procedures that have the same or similar objectives were not accomplished. It was only later that controlled clinical trials were felt to be necessary, as several authors speculated that an equivalent amount of bone fill could be achieved irrespective of whether the procedure included a bone graft (Rosling et al., 1976; Ellegaard et al., 1971; Poison and Heijle, 1978). In addition, as judged by present-day standards, many of the early controlled studies were inadequately designed because the patient did not serve as the unit of control (Hujoel et al., 1990). Yet a critical analysis of these studies revealed that in no in- stance was the control procedure (open flap debridement) to be superior to the bone graft (Table 1). A. Autogenous Bone Grafts There are several types of autogenous bone grafts that have been or are being used clinically. They include cortical bone chips, osseous coagulum, bone blend, intraoral and extraoral cancellous bone, and marrow. 1. Cortical Bone Chips The impetus for the modern-day use of periodontal bone grafts can be traced to the work of Nabers and O'Leary (1965). They reported that shavings of cortical bone removed by hand chis- els during osteoplasty and ostectomy from sites within the surgical area could be used successfully to effect a coronal increase in bone height. The intraosseous defects so treated were primar- ily one- and two-walled and not felt by the authors to be amenable to other methods of treatment. Subsequently, Nabers reported long-term success with 18- to 24-month posttreatment clinical documentation for six cases (Nabers, 1984). Although there is a paucity of information with respect to cortical bone chips, a more recent pub- lication suggests that this type of graft is still in use and may result in bone fill with decreased probing depth (Langer et al, 1986). Cortical chips, due to their relatively large particle size 1,559.6 x 183 fxm (Zayer and Yukna, 1983) and potential for sequestration, were replaced by autogenous osseous coagulum and bone blend.
2. Osseous Coagulum and Bone Blend Intra-oral bone, when obtained with high- or low-speed round burs and mixed with blood, becomes a coagulum (Robinson, 1969; Jacobs and Rosenberg, 1984). The rationale for the use of osseous coagulum is the belief that the smaller the particle size of the donor bone, the more certain its resorption and replacement with host bone (Robinson, 1969). It was subsequently demonstrated in monkeys that small bone particles of 100 |xm could provide for earlier and greater osteogenic activity than particles ten times as large (Rivault et al, 1971). The bone blend technique was designed to overcome some of the disadvantages of osseous coagulum, including inability to aspirate during the collection process, unknown quantity and
335 TABLE 1 Human Controlled Studies with Bone Autografts and Allografts in the Treatment of Periodontal Osseous Defects
Graft material Method of evaluation Graft Mean i esults Control Ref. ICBM Probing and radiographs Equal degree of success Ellegaard and Loe(1971) OC-BB ECBM
ICBM ICMB ICBM Reentry
Probing Probing and X-rays Probing bone level 2.98 mm (71 % bone fill) 4.36 mm (61 % fill) 3.07 mm (2-wall) 2.35 mm (1-wall) 3.2 mm gain attachment 1.2 mm gain (significant only for deepest defects) 0.66 mm (22% fill)
2.15 mm (2-wall) 2.25 mm (1-wall) 2.0 mm gain attachment 0.8 mm
Froum et al. (1976)
Carraro et al. (1976) Movin et al. (1982) Renvert et al. (1985) ICBM ECBM Reentry No significant difference Graft improved results of treatment Patur(1974) ICBM ECBM CBMA ICBM CBMA CBMA CBMA FDBA
Histology
Histology
Reentry and probing bone Reentry
Reentry Regeneration consistently found New bone and cementum 4.83 mm fill 1.6 mm (54% bone fill) 60% defects >50% bone fill Lack of cementogenesis and bone formation Little if any new cementum or bone 0.22 mm fill 0.8 mm (33% bone fill) 60% defects >50% fill Hiatt et al. (1978) Listgarten and Rosenberg (1979) Hiatt et al. (1986) Schrad and Tussing (1985) Altiere et al. (1979) FDBA Histology New attachment greater in grafted sites Moomaw (1978) FDBA FDBA
+
Reentry TCN DFDBA
X-ray 1.9 mm (39% fill) 2.8 mm (61% fill)
1.38 mm fill 1.0 mm (31% fill) 1.4 mm (36% fill)
0.3 mm fill Mabry et al. (1985)
Pearson et al. (1981) DFDBA Histology No difference in healing Dragoo and Kaldahl (1983) DFDBA Reentry 2.57 mm (65% bone fill) 1.26 mm (38% fill) Mellonig (1984) DFDBA DFDBA Reentry Histology No difference between defects treated with and without IDone grafts Regeneration in both grafted and nongrafted sites in the submerged environment; greater and more frequent regeneration in grafted sites Santes et al. (1988) Bowers et al. (1989b)
336
DFDBA DFDBA
Histology Reentry New bone, cementum, PDL 2.60 mm bone fi No new attachment apparatus 0.38 mm bone fill Bowers et al. (1989c) Blumenthal and Steinberg (1990)
OC-BB ICBM ECBM CBMA FDBA FDBA + TCN DFDBA

= = = = = = Osseous coagulum-bone-blend autograft. Intraoral cancellous bone and marrow autograft. Extraoral (iliac) cancellous bone and marrow autograft. Cancellous bone and marrow allograft. Freeze-dried bone allograft. Freeze-dried bone allograft plus tetracycline.
= Decalcified freeze-dried bone allograft. = Significant difference in favor of bone grafting.
quality of collected bone fragments, and fluidity of the material (Diem et al, 1972). Bone blend is cortical or cancellous bone that is procured with a trephine or rongeurs, placed in an amal- gam capsule, and triturated to the consistency of a slushy osseous mass. The resultant particle size is in the range of 210 x 105 |xm (Zayer and Yukna, 1983). Case reports indicate that intraosseous defects can be successfully managed with this graft material (Robinson, 1969). A mean bone fill of 73% was obtained in 25 defects (Froum et al, 1975). Froum et al (1976) reported the osseous coagulum-bone-blend type of grafts provided 2.98 mm coronal growth of alveolar bone, compared with 0.66 mm obtained when open flap debridement alone was used.
3. Intraoral Cancellous Bone and Marrow Healing bony wounds, healing extraction sockets, edentulous ridges, mandibular retromolar areas, and the maxillary tuberosity have all been used as sources of intraoral cancellous bone and marrow (Hiatt and Schallhorn, 1973; Ross and Cohen, 1968; Soehren and Von Swol, 1979; Halliday, 1969; Rosenberg, 1971). Bone fill in all types of intraosseous and furcation defects has been demonstrated with this material (Hiatt and Schallhorn, 1973; Soehren and Von Swol, 1979; Halliday, 1969; Rosenberg, 1971). A mean bone fill of 3.65 mm, with up to 12 mm in some lesions, and >50% bone fill on a predictable basis have been achieved (Hiatt and Schallhorn, 1973; Rosenberg, 1971). In an evaluation of 191 defects in 91 subjects, Ellegaard and Loe (1971) reported that grafts of intraoral cancellous bone and marrow did not appear to influence the clinical outcome when compared with surgical curettage. Likewise, Renvert et al. (1985) found limited differences between grafted and nongrafted sites. They did, however, note significant differences in favor of grafted sites when only the deepest defects were compared and suggested that intraoral grafts be limited to treating deep lesions. As determined by probing depth measurements, Carrraro et al. (1976) found no difference in the response between grafted and nongrafted one-walled defects. Two-walled defects responded more favorably when grafted than ungrafted controls. Also, Movin et al. (1982) reported a 3.2-mm gain in clinical attachment in grafted defects and 2.0 mm in nongrafted defects.
4. Extra-oral Cancellous Bone and Marrow It is generally agreed that the extraoral cancellous bone and marrow offer the greatest potential for new bone growth (Cushing, 1969; Sot- tosanti and Bierly, 1975; Amler, 1984). This material is obtained from either the anterior or the posterior iliac crest (Schallhorn, 1968; Dra- goo and Irwin, 1972). Schallhorn's reports of complete eradication of furcation and interprox- imal crater defects spurred interest in this material (Schallhorn, 1967 and 1968). Subsequently, additional case reports attested to the efficacy of
337
this approach when used by different clinicians to successfully treat furcations, dehiscences, and defects of varying osseous morphology (Schal- lhorn et al, 1970; Haggerty and Maeda, 1971; Patur, 1974; Seibert, 1970; Mattout and Roche, 1984). Mean clinical bone fill of 3.33 mm in 182 defects and 4.36 mm in 7 defects has been reported (Froum et al, 1975; Schallhorn et al., 1970). Patur (1974) indicated that grafting improved the results of treatment. In addition, a mean bone apposition of 2.54 mm in crestal or zero-wall defects has been documented (Schallhorn etal., 1970). B. Bone Allog rafts The need for an allogeneic source of bone arose from the need for increased donor material and the problems associated with autogenous bone procurement, namely, the morbidity accomp- anying a second surgical site and the need for a sufficient quantity of material to fill multiple defects (Mellonig, 1980 and 1991). Three types of bone allografts are used clinically. Underminer- alized (mineralized), freeze-dried bone allograft (FDBA) and demineralized (decalcified), FDBA are used routinely; frozen iliac cancellous bone and marrow are used sparingly. 1. Iliac Cancellous Bone and Marrow Allograft The need for extensive cross-matching of do- nor and recipient and the possibility of disease transfer restrict the use of iliac cancellous bone and marrow allograft (Hiatt and Schallhorn, 1971; Schallhorn, 1977). A mean coronal gain of bone amounting to 3.07 mm in 26 patients at reentry has been reported (Schallhorn and Hiatt, 1972). When compared with open flap debridement of osseous defects, allogeneic grafts of cancellous bone and marrow resulted in greater defect fill, 1.6 mm (54% defect fill) for grafted sites and 0.8 mm (33% defect fill) for nongraft sites (Scharad and Tussing, 1985). When compared with tricalcium phosphate, frozen allogeneic bone implants led to greater bone apposition and reduction in probing depth (Strub et al, 1979). 2. Freeze-Dried Bone Allograft Undemineralized FDBA was introduced to periodontal therapy in 1976 (Mellonig et al., 1976). Freeze drying removes approximately 95% of the water from bone by a process of sublimation in a vacuum. Although freeze drying kills all cells, the morphology, solubility, and chemical integrity of the original specimen are main- tained relatively intact (Friedlaender, 1988; Mel- lonig, 1980 and 1991). Freeze drying also markedly reduces the antigenicity of a periodontal bone allograft (Turner and Mellonig, 1981; Quattlebaum et al, 1988). At no time could any donor-specific anti-HLA antibodies be detected in any human recipient who received several FDBA grafts (Quattlebaum et al, 1988). FDBA is the only graft material that has undergone extensive field testing in the treatment of adult periodontitis (Mellonig et al, 1976; Sepe et al, 1978; Sanders et al, 1983; Mellonig, 1991). Field test studies provide information as to efficacy and feasibility but suffer from lack of project control, erratic documentation, and equivocal investigator compliance. Eighty-nine clinicians implanted a total of 997 sites with FDBA alone and 524 sites with FDBA plus autogenous bone (FDBA + A), (Mellonig, 1991). Sufficient data, as determined by surgical reentry at 6 months, were collected to determine predictability in 329 sites treated with FDBA and 176 sites treated with FDBA + A. Complete or >50% bone fill was obtained in 220 (67%) sites treated with FDBA and 137 (78%) of the sites treated with FDBA -I- A. Significant probing depth reduction occurred in 69 and 79% of the sites, respectively (Mellonig, 1991). It can be concluded from this and other studies that FDBA in combination with autogenous bone is more efficacious than FDBA alone, especially in the treatment of furcation invasion defects (Pearson and Freeman, 1980; Sanders etal, 1983). Altiere et al (1979)
investigated FDBA sterilized with three Mrads of 7-irradiation, when compared with a nongraft procedure for debridement in ten paired sites. Both graft and nongraft sites demonstrated >50% bone fill in 60% of the sites. A composite graft of FDBA and tetracycline in a 4:1 volume ratio has shown promise in the treatment of the osseous defects associated with
338
localized juvenile periodontitis (Yukna and Sepe, 1981; Evans et al, 1989). A study that compared FDB A with and without tetracycline to a nongraft procedure in 12 juvenile periodontitis patients demonstrated significantly greater bone fill and resolution of osseous defects in grafted as op- posed to control sites (Mabry et al, 1985).
3. Decalcified Freeze-Dried Bone Allograft Urist and co-workers showed through numerous animal experiments that demineralization of a cortical bone graft induces new bone formation and greatly enhances its osteogenic potential (Urist, 1965; Urist etal, 1967; Urist and Dowell, 1968; Urist etal, 1968 and 1975). The work of Urist has been confirmed by others (Ko- skinen et al, 1972; Chalmers et al., 1975; Oi- karien and Korhonen, 1979; Mellonig et al., 1981a and b). Demineralization with hydrochlo- ric acid exposes the bone inductive proteins located in the bone matrix (Urist and Strates, 1970). These proteins are collectively called bone morphogenetic protein (BMP) (Urist and Strates, 1971). They are composed of a group of acidic polypeptides that have been cloned and sequenced (Urist et al., 1983a and b; Wozney et al., 1988). In addition, there appears to be homology among bone inductive proteins between mammalian species (Sampath and Reddi, 1987). BMP stimulates the formation of new bone by osteoinduction (Urist et al, 1970). That is, the demineralized graft induces host cells to differ- entiate into osteoblasts (Harakas, 1984), whereas an undemineralized allograft is felt to function by osteoconduction as it affords a scaffold for new bone formation (Goldberg and Stevenson, 1987). The sequence of bone induction with a demineralized bone graft is believed to follow a bone induction cascade (Reddi et al, 1987; Bow- ers and Reddi, 1991). At day 1, there is chemotaxis of fibroblasts and cell attachment to the implanted demineralized bone matrix. At day 5, there is continued cell proliferation and differentiation of chrondroblasts. At day 7, chrondrocytes synthesize and secrete matrix. From days 10 to 12, there is vascular invasion, differentiation of osteoblasts and bone formation, and mineralization. By day 21 , there is bone marrow differentiation. This cascade for the induction of endochondral bone has been shown to occur in heterotopic sites of animals grafted with demineralized bone matrix (Reddi et al., 1987). It has not been demonstrated to occur following implantation of this material in a periodontal osseous defect. A more likely scenario for the periodontal defect is the induction of new bone through the intermembranous route (Mellonig et al, 1981b). Libin et al (1975) were the first to report the use of cortical and cancellous decalcified FDBA (DFDBA) in humans. The three grafted sites responded with 4 to 10 mm of new bone formation. Cortical DFDBA was evaluated in 27 intraosseous periodontal defects and yielded a mean of 2.4 mm of bone fill (Quintero et al, 1982). In six cases, Werbitt (1987) showed bone fill ranging from 75 to 95% of the original defect. The results of a radiographic analysis of cancellous DFDBA in 16 patients demonstrated a mean bone fill of 1.38 mm, whereas six control sites showed 0.33 mm (Pearson et al, 1981). The reason for this meager bone fill after a graft of cancellous DFDBA may lie in the fact that the bone inductive proteins are located in the bone matrix (Urist and Iwata, 1973). Because the mass of bone matrix is lower in cancellous bone than that in cortical bone, the yield of new bone could be expected to be lower with cancellous than cortical bone (Urist et al, 1970). Another controlled study in 47 periodontal osseous defects demonstrated a mean bone fill of 2.6 mm (65% defect fill) in sites treated with cortical DFDBA in comparison with 1.3 mm (38% defect fill) in sites treated without DFDBA. Rummelhart et al (1989) clinically compared DFDBA and FDB A in 11 paired sites. No statistical difference in probing depth reduction, clinical attachment gain, or bone fill was reported, which might have been reflective of in- sufficient inductive bone protein in DFDBA or the types and depths of the grafted lesions. Ad- ditional factors might also have influenced the decision to use a mineralized or demineralized preparation. The processing of both preparations included
multiple immersions in absolute ethanol. The DFDBA underwent further processing that included immersion in 0.6 N HC1 (Mellonig,
339
1991). Each of these chemical processes was thought to inactivate HIV (Martin et al, Resnick et al, 1986; Quinnan et al, 1986). 4. Allografts Compared with Alloplasts
1985;
Both FDBA and DFDBA have been compared to porous particulate hydroxyapatite, a synthetic or alloplastic bone graft material. Studies by Burnett et al. (1989) and Bowen et al (1989) suggest that there is little difference in posttreatment clinical parameters between allograft and the hydroxyapatite graft sites. Another study suggests a slight difference in favor of the alloplast (Oreamuno et al, 1990). Histologically, grafts of DFDBA heal with regeneration of the periodontium (Bowers et al., 1989c), whereas grafts of synthetic bone heal by repair (Baldock et al., 1985; Froum et al, 1982; Stahl et al, 1986; Kenney et al, 1986; Carranza et al, 1987). Therefore, the choice of material will depend in part on the objectives of the clinician. V. WOUND HEALING WITH PERIODONTAL BONE GRAFTS The objectives of the clinician who uses bone grafts are (1) probing depth reduction; (2) clinical attachment gain; (3) bone fill of the osseous defect; and (4) regeneration of new bone, cementum, and periodontal ligament (Schallhorn, 1977). Case reports and controlled clinical trials provide valuable information with respect to the first three objectives. They do not reveal the type of wound healing adjacent to the postgrafting root surface. Therefore, histologic analysis of the nature of the attachment apparatus is needed to determine true regeneration of the periodontium. A. Animal Studies Histologic evaluations in animals are of interest because they indicate the potential of a graft material to produce favorable results. In a review of the studies performed over the past several decades comparing graft and nongraft procedures in artificially created defects in animals, 75% of the studies indicated that more favorable results might be obtained following the placement of a bone graft (Table 2). None of the nongraft control sites were found to be superior to grafted sites. The results of animal experimentation must be viewed with caution, and the tendency to ex- trapolate this information directly to the human situation should be duly tempered.
B. Human Studies Only in clinical trials can the true potential of any graft material to regenerate the periodontium be analyzed. To date, approximately 159 human periodontal bone grafts have been removed en bloc and processed for histologic evaluation (Dragoo and Sullivan, 1973; Ross and Cohen, 1968; Nabers et al, 1972; (Hiatt and Schallhorn, 1973; Hawley and Miller, 1973; Froum et al., 1975; Moomaw, 1978; Hiatt et al, 1978; Listgarten and Rosenberg, 1979; Moskow et al, 1979; Langer et al, 1981; Evans, 1981; Froum et al, 1983; Dragoo and Kaldahl, 1983; Bowers et al, 1982; Bowers, 1989a, b, and c). Most human histologic evaluations have been criticized because they failed to adequately demonstrate that the adjacent root surface was bio- logically contaminated and devoid of its connective tissue attachment. For example, biopsies were commonly evaluated from the most apical level of root planing (Hawley and Miller, 1975; Hiatt etal, 1978; Moskow et al, 1978), from a notch placed in cementum with a bur at the base of the defect (Nabers et al, 1972; Moomaw, 1978; Listgarten and Rosenberg, 1979), from a notch placed in cementum at the level of the alveolar crest (Dragoo and Sullivan, 1973), or from a naturally occurring notch in the root surface (Ross and Cohen, 1968; Evans, 1981). All of these histologic reference points, although highly suggestive of a root exposed to the oral bacterial contamination, did not prove that the root surface had lost its connective
tissue attachment (periodontal ligament). Therefore, reattachment rather than regeneration might have been the result. Us- ing the above cited examples for a histologic reference point, new bone cementum and periodontal ligament have been observed following grafts of cortical bone chips (Nabers et al, 1972),
340
TABLE 2 Animal Controlled Histologic Studies with Bone Autografts and Allografts in the Treatment of Periodontal Osseous Defects
Graft material OC
oc
ICBM
ICBM
ICBM ECBM
ICBM ECBM
ICBM
ICBM ICBM
ICBM ICBM Animal 4M Defect type created Intraosseous
4M
2- and 3-Wall
10 D
Intraosseous
10 D
Furcation
6M
Furcation
12 M
3-Wall
19 M
Furcation
6 D 8 M
Furcation Intraosseous
10 D
Furcation
6 D
Furcation Results
A sooner and greater osteogenic activity with small particle bone graft than controls In early stages, grafted defects demonstrated a more advanced level of regeneration than controls Grafted defects may be eliminated by induction of bone; control defects heal by adap- tation of epithelial attachment A coronal increase of 2 to 3 mm of bone with graft No new bone with control ICBM and frozen ECBM yielded a higher frequency of regeneration than fresh ECBM and controls Regeneration is obtained with equal success with and without graft New bone in deepest portion of defect with graft No new bone without graft Osseous grafts did not improve results Both graft and control healed with an epithelial lining along the root surface with no new connective tissue Flap support by the bone graft may facili- tate regeneration Abundant new bone, new cementum, and no ankylosis with graft; control defects filled with connective tissue and new cementum Ref. Rivault et al. (1971)
Coverly et al. (1975)
Yuktanandana (1959)
Patterson et al. (1967)
Ellegaard et al. (1973)
Elegaard et al. (1974)
Ellegaard et al. (1975)
Nilveus et al. (1978) Caton et al. (1980)
Klinge et al. (1985) Passanezi et al. (1989)
341
TABLE 2 (continued) Animal Controlled Histologic Studies with Bone Autografts and Allografts in the Treatment of Periodontal Osseous Defects
Graft material CBMA
CBMA FDBA
FDBA DFDBA DBP
DFDBA
DFDD
ICBM DFDBA Animal 12 D
4M
4D
4M
27 D
8D
4D
6D
3D Defect type created Intraosseous
2-Wall
2-Wall
Intraosseous
Intraosseous
Intraosseous Furcation
2-Wall
3-Wall
Furcation Results No significant difference in healing between graft and control Allograft induced a more rapid osseous repair than controls Convincing evidence of acceptability of graft; no advantage or disadvantage in using graft Significantly more regeneration with graft than control Graft was replaced by new bone and marrow; less new bone at control sites DBP successfully induced new bone; no differences were seen between test and control Graft healed by regeneration; control healed by a long junctional epithelium Complete regeneration of lost attachment apparatus with graft; long junctional epithelium to base of defect with controls Grafts showed more pronounced regeneration and higher periodontal attachment than did controls Ref. Hiatt(1970)
Poulsom et al. (1976) Hurt (1969)
Mellonig (1981) Narang and Wells (1972)
Sonis et al. (1985)
Blumenthal et al. (1986)
Waal et al. (1988)
Wada et al. (1989) OC ICBM ECBM CBMA FDBA DFDBA DFDDA DBP D M = Osseous coagulum autograft. = Intraoral cancellous bone and marrow autograft. = Extraoral (iliac) cancellous bone and marrow autograft. = Cancellous bone and marrow allograft. = Freeze-dried bone allograft. = Decalcified freeze-dried bone allograft. = Decalcified freeze-dried dentin allograft. = Demineralized bone powder. = Dog. = Monkey.
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osseous coagulum (Evans, 1981), bone blend (Froum et al, 1975), intraoral cancellous bone and marrow (Ross and Cohen, 1968; Hiatt and Schallhorn, 1973; Hawley and Miller, 1975; Hiatt et al., 1978; Listgarten and Rosenberg, 1979; Langer et al., 1981), iliac cancellous bone and marrow autograft (Dragoo and Sullivan, 1973; Hiatt et al., 1978), iliac cancellous bone and marrow allograft (Hiatt et al., 1979; Listgarten and Rosenberg, 1981), and undemineralized FDBA (Moomaw, 1978). Currently, only a notch placed in the most apical level of calculus on the root surface is considered scientifically valid proof of regeneration of an attachment apparatus (Cole et al., 1980; Froum et al, 1983; Dragoo and Kaldahl, 1983; Bowers et al., 1989a, b, and c). Using this criterion, new bone, cementum, and periodontal ligament have been identified following grafts of osseous coagulum-bone blend (Froum et al., 1983) and DFDBA (Bowers etal, 1989a, b, and c).
C. Bone Induction It has been stated that there is "little indi- cation that (periodontal bone) grafts of cortical or cancellous bone have any inductive effect on the formation of new bone. Also, there is little reason to believe that such bone grafts would stimulate connective tissue attachment to the root surface" (Egelberg, 1987). This concept was evaluated in a study by Bowers et al. (1989b). They compared the healing of intraosseous defects with and without the placement of DFDBA in defects about teeth that received coronalec- tomy and were completely covered by soft tissue. The most apical level of calculus on the root served as a histologic reference point to measure periodontal regeneration in 30 grafted and 19 nongrafted defects. Results indicated that in the submerged environment, regeneration was possible with and without the placement of a bone graft. However, more new attachment apparatus formed in grafted than nongrafted sites. In addition, new bone, new cementum, and periodontal ligament occurred more frequently in grafted than nongrafted sites. These results strongly suggest that bone grafts do have an inductive effect on the periodontium. D. Healing Sequence The healing sequence of an autogenous periodontal bone graft has been identified as initiation of new bone formation at 7 d, cementogenesis at 21 d, and a new periodontal ligament at 3 months (Dragoo, 1972). By 8 months, the graft should be incorporated into host bone with functionally oriented fibers coursing between bone and cementum. Maturation may take as long as 2 years (Dragoo, 1972; Dragoo and Sullivan, 1973).
E. Root Resorption and Ankylosis Because granulation tissue derived from bone may induce root resorption and ankylosis, the use of bone grafts has been questioned (Karring et al., 1980). Root resorption is reported as a se- quela of osseous grafting in humans but appears to be a significant disadvantage only with fresh iliac cancellous bone and marrow (Schallhorn et al., 1970; Schallhorn, 1972; Dragoo and Sulli- van, 1973; Hoffman and Flanagan, 1974; Hiatt et al., 1978). Clinical evidence of root resorption was noted in 7 of 250 sites (3% in one reported series (Dragoo and Sullivan, 1973) and 16 of 275 sites (5%) in another (Hiatt et al., 1978). Freez- ing seems to attenuate this problem (Schallhorn, 1972). Recently, Bowers and co-workers reported on a series of 62 cases grafted with DFDBA and removed en bloc at 6 months for histologic observations (Bowers et al., 1989b and c). Ex- tensive root resorption was not observed. Be- cause this phenomenon has been observed only with fresh material, viable marrow cells may play an etiologic role (Ellegaard, 1976). The most probable cause of root resorption is poor post- surgical plaque control with subsequent chronic gingival
inflammation (Dragoo and Sullivan, 1973). This hypothesis has been strengthened by histologic findings that connective tissue in resorptive defects always contained an infiltrate of inflammatory cells (Ellegaard, 1976). Root re-
343
sorption and ankylosis following bone grafts are more prevalent in animal models (Ellegaard et al., 1973 and 1976; Karring et al, 1980 and 1984; Nyman et al, 1980) than they are in humans and may be a function of the healing potential animal model (Sonis et al, 1985; Aukhil etal, 1990). Apical migration of junction epithelium between the alveolar bone and the root surface has been offered as an explanation of why resorption only infrequently takes place after regeneration attempts with bone grafts (Listgarten and Rosen- berg, 1979; Karring et al, 1980; Caton and Zan- der, 1976; Moskow etal, 1979). The junctional epithelium was specifically located in 74 human biopsies where bone grafting was performed (Bowers et al, 1982). The junctional epithelium was located apical to the alveolar crest in 14 (19%) sites. In an additional 32 graft sites, Bow- ers et al (1989c) showed that grafted sites consistently formed a new attachment apparatus. The junctional epithelium proliferated apically, but the epithelium was rarely observed apical to the level of active bone formation. Junctional epithelium was never observed beyond the level of new cementum formation (Bowers et al, 1989c). Authors reporting epithelial migration between the grafted site and the root surface also report chronic inflammatory cells adjacent to the epithelium (Hiatt et al, 1978) or extending into the marrow spaces (Moskow et al, 1979). Poor plaque control is therefore a likely explanation as proliferation of epithelium is more extensive and rapid in surgical sites with no postoperative plaque control than in areas where bacterial de- posits have been removed (Yumet and Poison, 1985).
VI. TISSUE BANKING AND FDBA The possibility of disease transfer with bone allografts is unlikely if the material is procured and processed by using established tissue banking protocols (Friedlaender, 1987; American Asso- ciation of Tissue Banks, 1984). If exclusionary techniques such as medical and social screening, antibody testing, direct antigen tests, other ser- ologic tests, bacterial culturing, autopsy, and follow-up studies of grafts from the same donor are used, the possibility of disease transfer are approximately one in 2 million (Buck et al, 1989). Freezing the bone allograft reduces the risk to one in 8 million (Buck et al, 1990). An estimated 40,000 periodontal grafts of mineralized and demineralized bone are performed annually (Mellonig, 1991). There are no reported cases of disease transfer with processed (treatment with virucidal agents and demineralization in hydro- chloric acid) FDBA. Concerns with disease transfer have led some tissue banks to sterilize the bone allograft with irradiation or ethylene oxide. Irradiation of a bone allograft is reported both to markedly attenuate (Buring, 1967; Towle et al, 1987; Munting et al., 1988) and not to affect (Wientroub et al, 1988) bone induction. Furthermore, the currently used dose of 1.5 Mrad will not reliably inactivate HIV in bone allografts with an acceptable safety margin (Conway et al, 1990). There is little question that ethylene oxide sterilization renders a bone allograft noninfectious (Eastlund et al, 1989). However, like irradiation, ethylene oxide may interfere with bone induction (Zislis et al, 1989). Residual levels of ethylene oxide in the graft have been shown to be toxic to fibroblasts and cause morphologic changes that may or may not be reversible (Kudryk, 1990). Others have found ethylene oxide sterilization to be acceptable and safe (Prolo et al, 1980). The processing of a bone allograft for dental use will usually include the following steps (Mellonig, 1991): 1. Cortical bone is harvested in a sterile man- ner within 12 h of death of the donor. Cor- tical bone is less antigenic than cancellous bone (Friedlaender et al, 1976) and has a higher concentration of bone-inductive proteins (Urist and Dowell, 1968; Urist et al, 1970). The bone is rough cut to 0.5 to 5 cm and immersed in 100% ethanol for 1 h. Viral infectivity is undetectable within 1 min of treatment (Resnick et al, 1986), and the ethanol completely penetrates through the cortical bone (Prewitt et al, 1991).
2.
3. 4.
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The bone is frozen. Freezing decreases the risk of disease transfer (Buck et al, 1990). The cortical bone is ground to a final par-
5. 6. 7.
tide size of approximately 250 to 800 Particle sizes within this range have been shown to promote osteogenesis, whereas a particle size below 125 |xm induces a mac- rophage response (Mellonig and Levey, 1984). The graft is again immersed in ethanol. The bone may or may not be dimineralized. The allograft is freeze dried. Freeze drying permits long-term storage and reduces antigenicity (Turner and Mellonig, 1981; Quattlebaum et al, 1988).
VII. GUIDED TISSUE REGENERATION AND BONE GRAFTS Case reports and controlled clinical trials have indicated that the placement of a physical barrier between the gingival flap and the root surface enhances the potential for wound healing (Nyman et al, 1982; Becker et al, 1987 and 1988; Pon- toriero et al, 1988 and 1989; Lekovic et al, 1989; Caffesse et al, 1990; Gager and Schultz, 1991). This procedure retards apical migration of epithelium, excludes gingival connective tissue cells from the wound, and favors healing from the periodontal ligament cells (Gottlow et al., 1986). The histologic result is new attachment (Gottlow et al, 1986; Becker et al, 1987; Nyman et al, 1987). A recent study indicates that the periodontal ligament cells migrate only a short distance and, at the same rate, with and without the placement of a physical barrier (Aukhil and Iglhaut, 1988). Therefore, the critical role of a physical barrier may be that of space creation to allow migrating cells sufficient time to undergo amplifying cell division and populate the root surface (Aukhil et al., 1990). In addition, cells from the bone may play a role in guided tissue regeneration. Cells from the endosteal spaces of alveolar bone can synthesize cementumlike tissue and may migrate from bone into the periodontal ligament (Melcher etal, 1986). A number of case reports suggest that the combination of an osseous graft and the physical barrier enhances bone fill and promotes more favorable results (Schallhorn and McClain, 1988). Anderegg et al (1991) compared 15 pairs of furcation defects in 15 patients treated by DFDBA plus an expanded polytetrafluoroethylene (Gore- Tex Periodontal Material, W. L. Gore & Asso- ciates, Flagstaff, AZ) physical barrier or by a physical barrier alone. They found both horizon- tal and vertical bone fill to be more favorable with the use of the graft plus barrier. However, Garrett et al. (1988), using a graft of DFDBA and dura mater sheets between the replaced surgical flaps and the tooth surfaces, found limited improvement of the treated defects over pretreat- ment levels. Stahl and Froum (1991) have most recently shown cementogenesis on teeth treated by osseous allograft and an expanded polytetrafluoroethylene membrane. Osseous remodeling and crestal osteogenesis were seen in association with cementogenesis. New attachment was histologically present within two of four calculus notches in this sample.
VIII. FUTURE DIRECTIONS Although bone grafts have been shown to be efficacious for the treatment of periodontal osseous lesions, the reconstruction appears to be limited to a mean bone fill of approximately 3.0 mm irrespective of the type of bone graft material (Table 1). Because the ultimate goal of periodontal therapy is to reverse the disease process and completely regenerate the periodontium, additional stimuli to enhance the regenerative process clearly are needed. Polypeptide growth factors, a potent class of natural biologic response modifiers, may be the answer. Factors such as osteogenin (Bowers and Reddi, 1991) or the combination of platelet-derived growth factor (PDGF) and insulinlike growth factor (IGF) (Lynch et al, 1989) may have potential. Other growth factors such as transforming growth factor- (3 and basic fibroblast growth factor may also have a place (Graves and Cochran, 1990). However, the use of
growth factors (GFs) to augment periodontal regeneration also poses many questions, such as 1. What is the proper dose of GFs? 2. What is the best biologic carrier for the GF? 3. When should the GF be released into the healing cascade?
345
4. 5. 6. 7. 8.
What are the possible local and systemic side effects of GFs? Can the effects of the GFs be limited to the local environment? Can results obtained with GFs in animal model systems be extrapolated to humans? What is the mechanism of action of GFs in the periodontal environment? What is the most effective GF in the periodontal environment?
IX. CONCLUSIONS 1. Numerous case reports and controlled clinical studies indicate that autogenous bone grafts can be used successfully in periodontal therapy. 2. Multiple histologic reports suggest that regeneration of a new attachment apparatus is possible with different types of autogenous bone grafts. 3. Root resorption and ankylosis may be observed only following grafts of fresh iliac cancellous bone and marrow. 4. Iliac cancellous bone and marrow are a graft of high osteogenic potential. 5. Both FDBA and DFDBA have been shown to be clinically effective in the reconstruction of periodontal bone defects. 6. Sites implanted with DFDBA demonstrate more probing depth reduction, clinical attachment gain, and bone fill than similar defects that are not grafted. 7. Regeneration of new bone, cementum, and periodontal ligament is a frequent finding with grafts of DFDBA. 8. Bone formation may be enhanced if guided tissue regeneration attempts are augmented with bone grafts. 9. Bone allografts and alloplasts offer similar advantages with respect to bone fill. Re- generation is generally the result after grafts of DFDBA, whereas repair is the result after grafts of synthetic bone. 10. Dental bone allografts are safe for human use if proper exclusionary techniques and processing are employed.
REFERENCES
Altiere, E., C. Reeve, and P. Sheridan: Lyophilized Bone Allografts in Periodontal Osseous Defects. J. Periodon- toL 50:510-519(1979). American Association of Tissue Banks: Standards for Tissue Banking. Arlington, Virginia, American Association of Tissue Banks (1984). Amler, M. H.: The Effectiveness of Regenerating Versus Mature Marrow in Physiologic Autogenous Transplants. J. PeriodontoL 55:268-272 (1984). Anderegg, C. R., S. J. Martin, J. L. Gray, J. T. Mellonig, and M. E. Gher: Clinical Evaluation of The Use of Decalcified Freeze-Dried Bone Allograft with Guided Tissue Regeneration in the Treatment of Molar Furcation Invasions. J. PeriodontoL 62:264-268 (1991). Aukhil, I. and J. Iglhaut: Periodontal Ligament Cell Kinetics Following Experimental Regenerative Procedures. J. Clin. PeriodontoL 15:374-382 (1988). Aukhil, I., K. Nishimura, and W. Fernyhough: Experi- mental Regeneration of the Periodontium. Oral Biol. OralMed. 1:101-115 (1990). Baldock, W., L. Hutchens, W. McFall, and D. Simpson: An Evaluation of Tricalcium Phosphate Implants in Hu- man Periodontal Osseous Defects in Two Patients. J. PeriodontoL 56:1-7 (1985). Barnett, J., J. Mellonig, H. Towle, and J. Gran: Comparison of Freeze-Dried Bone Allograft and Porous Hydroxy- apatite in Human Periodontal Defects. J. PeriodontoL 60:231-237(1989). Becker, W., B. Becker, C. Berg, J. Prichard, R. Caffessee, and E. Rosenberg: New Attachment After Treatment with Root Isolation Procedures: Report for Treated Class III and Class II Furcations and Vertical Osseous Defects. Int. J. Periodontics Restorative Dent. 8(3):9-24 (1988). Becker, W., B. Becker, J. Prichard, R. Caffessee, E. Ro- senberg, and J. Gian-Grasso: Root Isolation for New Attachment Procedures A Surgical and Suturing Method: Three Case Reports. J. PeriodontoL 58:819826 (1987). Beube, F. E.: Observations on the formation cementum, periodontal membrane and bone, 20 months postoper- tively,
with the use of boiled cow bone powder. J. Dent. Res. 21:298-299 (1942). Beube, F. E. and H. F. Silvers: Influence of Devitalized Heterogenous Bone-Powder on Regeneration of Alveolar and Maxillary Bone of Dogs. J. Dent. Res. 14:15-19 (1934). Beube, F. E. and H. F. Silvers: Further Studies on Bone Regeneration with the Use of Boiled Heterogenous Bone. J. PeriodontoL 7:17-21 (1936). Blumenthal, N., T. Sabe, and E. Barrington: Healing Re- sponses to Grafting of Combined Collagen-Decalcified Bone in Periodontal Defects in Dogs. J. PeriodontoL 57:84-90 (1986). Blumenthal, N. and J. Steinberg: The Use of Collagen Membrane Barriers in Conjunction with Combined De-
346
mineralized Bone-Collagen Gel Implants in Human In- trabony Defects. J. Periodontol. 61:319-327 (1990). Bowen, J., J. Mellonig, J. Gray, andH. Towle: Comparison of Decalcified Freeze-Dried Bone Allograft and Porous Particulate Hydroxyapatite in Human Periodontal Os- seous Defects. J. Periodontol. 60:647-654 (1989). Bowers, G., B. Chadroff, R. Carnevale, J. Mellonig, R. Corio, J. Emerson, M. Stevens, and E. Romberg: His- tologic Evaluation of New Human Attachment Apparatus Formation in Humans, Part I. J. Periodontol. 60:664674 (1989a). Bowers, G., B. Chadroff, R. Carnevale, J. Mellonig, R. Corio, J. Emerson, J. Stevens, and E. Romberg: His- tologic Evaluation of New Human Attachment Apparatus in Humans, Part II. J. Periodontol. 60:675-682 (1989b). Bowers, G., B. Chadroff, R. Carnevale, J. Mellonig, R. Corio, J. Emerson, M. Stevens, and E. Romberg: His- tologic Evaluation of New Human Attachment Apparatus in Humans, Part III. J. Periodontol. 60:683-693 (1989c). Bowers, G. and H. Reddi: Regenerating the Periodontium in Advanced Periodontal Disease. J. Am. Dent. Assoc. 122:45-48 (1991). Bowers, G. G., R. G. Schallhorn, and J. T. Mellonig: Histologic Evaluation of New Attachment in Human In- trabony Defects: A Literature Review. J. Periodontol. 53:509-514(1982). Buck, B., T. Malinin, and M. Brown: Bone Transplantation and Human Immunodeficiency Virus: An Estimate of Risk Acquired Immunodeficiency Syndrome (AIDS). Clin. Orthop. 240:129-134 (1989). Buck, B., B. Resnick, S. Shah, and T. Malinin: Human Immunodeficiency Virus Cultured from Bone. Impli- cations for Transplantation. Clin. Orthop. 251:249-253 (1990). Buring, K. and M. Urist: Effects of Ionizing Radiation on the Bone Induction Principle in Matrix of Bone Implants. Clin. Orthop. 55:225-234 (1967). Burwell, R.: The Function of Bone Marrow in the Incor- poration of a Bone Graft. Clin. Orthop. 200:125-141 (1985). Caffesse, R. G., B. Smith, B. Duff, E. Morrison, D. Mer- rill, and W. Becker: Class II Furcations Treated by Guided Tissue Regeneration in Humans: Case Reports. J. Per- iodontol. 61:510-514 (1990). Carranza, F., E. Kenney, V. Lekovic, E. Talamante, J. Valencia, and B. Dimitrijecic: Histologic Study of Heal- ing of Human Periodontal Defects After Placement of Porous Hydroxyapatite Implants. J. Periodontol. 58:682688 (1987). Carraro, J. J., N. Sznajder, and C. A. Alonso: Intraoral Cancellous Bone Autografts in the Treatment of Intra- bony Pockets. J. Clin. Periodontol. 3:104-113 (1976). Caton, J., S. Nyman, and H. Zander: Histometric Evalu- ation of Periodontal Surgery. II. Connective Tissue Attachment Levels After Four Regenerative Procedures. J. Clin. Periodontol. 7:224-231 (1980). Caton, J. and H. Zander: Osseous Repair of an Intrabony Pocket Without New Attachment of Connective Tissue. J. Clin. Periodontol. 3:54-58 (1976). Chalmers, J., D. Gray, and J. Rush: Observations on the Induction of Bone in Soft Tissue. J. Bone Jt. Surg. 57B:36-41 (1975). Cole, R., M. Crigger, G. Bogle, J. Elgelberg, and K. Sel- vig: A Connective Tissue Regeneration to Periodontally Diseased Teeth. J. Periodont. Res. 15:1-9 (1980). Conway, B., W. Tomford, M. Hirsch, R. Schoolwy, and H. Mankin: Effects of Gamma Irradiation on HIV-1 in a Bone Allograft Model. 36th Annual Meeting, Ortho- paedic Research Society, February 5-8 , New Orleans, Lousiana (1990). Cushing, M.: Autogenous Red Marrow Grafts: Potential for Induction of Osteogenesis. J. Periodontol. 40:492-497 (1969). Diaz-Arnold, A. and G. A. Zach: Demineralized Freeze- Dried Bone Allografts. Gen. Dent. 33:446-447 (1985). Diem, C. R., G. M. Bowers, and W. C. Moffitt: Bone Blending: A Technique for Bone Implantation. J. Periodontol. 43:295-297 (1972). Dragoo, M. and H. Sullivan: A Clinical and Histologic Evaluation of Autogenous Iliac Bone Grafts in Humans. Part I. Periodontal Bone Grafting Materials. J. Perio- dontol. 55:406; Wound Healing 2 to 8 Months. J. Per- iodontol. 44:599-613 (1973a). Dragoo, M. and H. Sullivan: A Clinical and Histologic Evaluation of Autogenous Iliac Bone Grafts in Humans. II. External Root Resorption. J. Periodontol. 44:614625 (1973b). Dragoo, M. R.: Clinical and Histologic Evaluation of Auto- genous Bone Grafts. J. Periodontol. 44:123 (1972). Dragoo, M. R. and R. K. Irwin: A Method of Procuring Cancellous Iliac Bone Utilizing a Trephine Needle. J. Periodontol. 43:82-87 (1972). Dragoo, M. R. and W. B. Kaldahl: Clinical and Histological Evaluation of Alloplasts and Allografts in Regenerative Periodontal Surgery in Humans. Int. J. PeriodonticsRes- torative Dent. 3(2):9-29 (1983). Eastlund, T., B. Jackson, G. Havrilla, and K. Sonnerud: Preliminary Study Results Using Ethylene Oxide (ETO) or Heat to Inactivate HIV in Cortical Bone. 13th Annual Meeting, American Association of Tissue Banks. Oct 1-4, 1989. Baltimore, Maryland (1989).
Egelberg, J.: Regeneration and Repair of Periodontal Tis- sues. J. Periodont. Res. 22:233-242 (1987). Ellegaard, B.: Bone Grafts in Periodontal Attachment Pro- cedures. J. Clin. Periodontol. 3:1-54 (1976). Ellegaard, B., T. Karring, R. Davies, and H. Loe: New Attachment After Treatment of Intrabony Defects in Monkeys. J. Periodontol. 45:368-376 (1974). Ellegaard, B., T. Karring, M. Listgarten, and H. Loe: New Attachment After Treatment of Interradicular Lesions. J. Periodontol. 44:209-217 (1973). Ellegaard, B., T. Karring, and H. Loe: The Fate of Vital and Devitalized Bone Grafts in the Healing of Interrad- icular Lesions. J. Periodont. Res. 10:88-97 (1975). Ellegaard, B. and H. Low: New Attachment of Periodontal Tissues after Treatment of Intrabony Lesions. J. Per- iodontol. 42:648-652 (1971).
347
Ellegaard, B., I. M. Nielsen, and T. Karring: Composite Jaw and Iliac Cancellous Bone Grafts in Intrabony De- fects in Monkeys. J. Periodont. Res. 11:299-310 (1976). Evans, G. H., R. A. Yukna, W. W. Sepe, T. W. Mabry, and E. T. Mayer: Effect of Various Graft Materials with Tetracycline in Localized Juvenile Periodontitis. J. Per- iodontoi 60:491-497 (1989). Evans, R.: Histologic Evaluation of an Autogenous Bone Graft. J. Periodont. Restorative Dent. 2(2):66-79 (1981). Forsberg, H.: Transplantation of Os Purum and Bone Chips in the Surgical Treatment of Periodontal Disease (Pre- liminary Report). Acta Odontol. Scand. 13:235-238 (1956). Friedlaender, G., M. Strong, and K. Sell: Studies on the Antigenicity of Bone. I. Freeze-Dried and Deep Frozen Allografts in Rabbits. J. Bone Jt. Surg. 58A:854-858 (1976). Friedlaender, G.: Bone Banking. Clin. Orthop. 225:17-21 (1987). Froum, S., L. Kushner, I. Scopp, and S. Stahl: Human Clinical and Histologic Responses to Durapatite Implants in Intraosseous Lesions. Case Reports. J. Periodontol. 53:719-725 (1982). Froum, S., L. Kushner, and S. Stahl: Healing Responses of Human Intraosseous Lesions Following the Use of Debridement, grafting and citric acid root treatment. I. Clinical and Histologic Observations Six Months Post- surgery. J. Periodontol. 54:67-76 (1983). Froum, S. J., M. Oritiz, R. T. Witkins, R. Thaler, I. W. Scopp, and S. S. Stahl: Osseous Autografts. III. Com- parison of Osseous Coagulum-Bone Blend Implants with Open Curettage. J. Periodontol. 47:287-294 (1976). Froum, S. J., R. Thaler, I. W. Scopp, and S. S. Stahl: Osseous Autografts. I. Clinical Responses to Bone Blend or Hip Marrow Grafts. J. Periodontol. 46:516-521 (1975). Gager, A. H. and A. J. Schultz: Treatment of Periodontal Defects with an Adsorbable Membrane (Polyglactin 910) with and without Osseous Grafting: Case Reports. J. Periodontol. 62:276-283 (1991). Gantes, B., M. Martin, S. Garrett, and J. Egelberg: Treat- ment of Periodontal Furcation Defects (II) Bone Regen- eration in Mandibular Class II Defects. J. Clin. Perio- dontol. 15:232-239 (1988). Gara, G. G. and D. F. Adams: Implant Therapy in Human Intrabony Pockets: A Review of the Literature. J. West Soc. Periodont. Abstr. 29:32-47 (1981). Garrett, S., B. Loos, D. Chamberlain, and J. Egelberg: Treatment of Intraosseous Periodontal Defects with a Combined Adjunctive Therapy of Citric Acid Condi- tioning, Bone Grafting, and Placement of Collagenous Membranes. J. Clin. Periodontol. 15:383-389 (1988). Goldberg, V. M. and S. Stevenson: Natural History of Au- tografts and Allografts. Clin. Orthop. 225:7-16 (1987). Gonzales, J. G.: Osseous Grafting Procedures in Periodontal Therapy. Rev. Odontol. P R 23:18-22 (1986). Gottlow, J., S. Nyman, J. Lindhe, T. Karring, and J. Wen- nstrom: New Attachment Formation in the Human Periodontium by Guided Tissue Regeneration. J. Clin. Per- iodontol. 13:604-616 (1986). Graves, D. and D. Cochran: Mesenchymal Cell Growth Factors. Crit. Rev. Oral BioL 1:17-36 (1990). Groff, G. B.: Treatment of Intrabony Osseous Defects by Grafting: A Review of the Literature. I: Early Research and Experimentation. US Navy Med. 67(10):9-23 (1976a). Groff, G. B.: Treatment of Infrabony Osseous Defects by Grafting: A Review of the Literature. II: Recent Success with Autografts and Homografts. US Navy Med. 67(ll):8-2 4 (1976b). Haggerty, P. C. and I. Maeda: Autogenous Bone Grafts: A Revolution in the Treatment of Vertical Bone Defects. J. Periodontol. 42:626-641 (1971). Halliday, D. G.: The grafting of Newly Formed Autogenous Bone in the Treatment of Osseous Defects. J. Perio- dontol. 40:511-514(1969). Hancock, E. B.: Regeneration Procedures. Section VI. In Proceedings of the World Workshop in Clinical Perio- dontics. The American Academy of Periodontology, pp. 1-19(1989). Harakas, N.: Demineralized Bone-Matrix-Induced Osteo- genesis. Clin. Orthop. 188:239-251 (1984). Hawley, C. and J. Miller: A Histologic Examination of a Free Osseous Autograft. J. Periodontol. 46:289-293 (1975). Hegedus, Z.: The Rebuilding of the Alveolar Process by Bone Transplantation. Dent. Cosmos. 65:736-742 (1923). Hiatt, R. G. and R. G. Schallhorn: Intraoral Transplants of Cancellous Bone and Marrow in Periodontal Lesions. J. Periodontol. 44:194-208 (1973). Hiatt, W., R. Schallhorn, and A. Aaronian: The Induction of New Bone and Cementum Formation. IV. Micro- scopic Examination of the Peridontium Following Hu- man Bone and Marrow Autograft, Allograft, and Non- graft Periodontal Regenerative Procedures. J. Periodontol. 49:495-512 (1978). Hiatt, W. H.: The Induction of New Bone and Cementum Formation. III. Utilizing Bone and Marrow Allografts in Dogs. J. Periodontol. 41:596-600 (1970). Hiatt, W. H., D. Larato, W. R. Hiatt, and K. Lindfors: The Induction of New Bone and Cementum Formation. V. A Comparison of Graft and Control in Sites in Deep Intrabony Periodontal Lesions. Int. J. Periodontics Res- torative Dent. 6(5):9-22 (1986). Hoffman, I. D. and P. Flanagan: Exophytic granulation reactions associated with autogenous iliac marrow transplantation
into periodontal defects. J. Periodontol. 45:586-594(1974). Hujoel, P. P., W. J. Loesche, and T. A. Derouen: As- sessment of Relationship between Site-Specific Vari- ables. J. Periodontol. 61:368-372 (1990). Hurt, W. C : Freeze-Dried Bone Homografts in Periodontal Lesions in Dogs. J. Periodontol. 39:89-92 (1968). Jacobs, J. E. and E. S. Rosenberg: Management of an Intrabony Defect Using Osseous Coagulum from a Lingual Torus. Compend. Contin. Educ. Dent. 5:57-61 (1984).
348
Karring, T., S. Nyman, and J. Lindhe: Healing Following Implantation of Periodontitis Affected Roots into Bone Tissue. J. Clin. Periodontol. 7:96-105 (1980). Karring, T., S. Nyman, and J. Lindhe, and M. Sirirat: Potentials for Root Resorption During Periodontal Wound Healing. J. Clin. Periodontol. 11:41-52 (1984). Kenney, E., V. Lekovic, C. Ferreira, T. Han, B. Dimitri- jevic, and F. Carranca: Bone Formation within Porous Hydroxyapatite Implants in Human Periodontal Defects. J. Periodontol. 57:76-83 (1986). Klinge, B., R. Nilveus, G. Bogle, A. Badersten, and J. Egelberg: Effect of Implants on Healing of Experimental Furcation Defects in Dogs. J. Clin. Periodontol. 12:321 326 (1985). Koskinen, E., S. Ryoppy, andT. Linkholm: Osteoinduction and Osteogenesis in Implants of Allogeneic Bone Ma- trix. Clin. Orthop. 87:116-131 (1972). Krejci, C. B. and C. F. Farah: Osseous Grafting in Per- iodontal Therapy, Part I: Osseous Graft Materials. Com- pendium 8:722-728 (1987). Kudryk, V.: Toxic Effect of Ethylene Oxide Sterilized Freeze- Dried Bone Allograft on Human Gingival Fibroblasts. J. Periodontol. 61:309 (1990). Langer, B., D. Gelb, and D. Krutchkoff: Early reentry procedure. Part II. A five year histologic evaluation. J. Periodontol. 52:135-139 (1981). Langer, B., B. Wagengerg, and L. Langer: The use of frozen autogenous bone in grafting procedures. Int. J. Periodontics Restorative Dent. 6(2):68-77 (1986). Lekovic, V., E. Kenney, K. Kovacevic, and R. Carranza: Evaluation of Guided Tissue Regeneration in Class II Furcation Defects. J. Periodontol. 60:694-698 (1989). Libin, B. M., H. Ward, and L. Fishman: Decalcified Ly- ophilized Bone Allografts for Use in Human Periodontal Defects. J. Periodontol. 45:51-56 (1975). Listgarten, M. and M. Rosenberg: Histological Study of Repair Following New Attachment Procedures in Human Periodontal Lesions. J. Periodontol. 50:333-344 (1979). Lynch, S., R. Williams, A. Poison, T. Howell, M. Reddy, and U. Zappa: A Combination of Platelet-Derived and InsulinLike Growth Factors Enhances Periodontal Re- generation. J. Clin. Periodontol. 16:545-548 (1989). Mabry, T., R. Yukna, and W. Sepe: Freeze-Dried Bone Allografts Combined with Tetracycline in the Treatment of Juvenile Periodontitis. / . Periodontol. 56:74-81 (1985). Martin, L., J. McDougal, and S. Loskoski: Disinfection and inactivation of the human T lymphocyte virus type III/lymphadenopathy-associated virus. J. Infec. Dis. 152:400-403 (1985). Mattout, P. and M. Roche: Juvenile Periodontitis: Healing Following Autogenous Iliac Marrow Graft, Long-Term Evaluation. J. Clin. Periodontol. 11:274-279 (1984). Melcher, A., T. Cheong, and J. Cox: Synthesis of Cementumlike Tissue In Vitro by Cells Cultured from Bone: A Light and Electron Microscopic Study. J. Periodont. Res. 21:592-612 (1986). Melcher, A. H.: The Use of Heterogenous Anorganic Bone as an Implant Material in Oral Procedures. Oral Surg. 15:996-1000 (1962). Mellonig, J., G. Bowers, and R. Baily: Comparison of Bone Graft Materials. I. New Bone Formation with Autografts and Allografts Determined by Strontium-85. J. Perio- dontol. 52:291-296 (1981a). Mellonig, J., G. Bowers, R. Bright, and J. Lawrence: Clin- ical Evaluation of Freeze-Dried Bone Allograft in Per- iodontal Osseous Defects. J. Periodontol. 47:125-129 (1976). Mellonig, J., G. Bowers, and W. Cotton: Comparison of Bone Graft Materials. Part II. New Bone Formation with Autografts and Allografts: A Histological Evaluation. J. Periodontol. 52:297-302 (1981b). Mellonig, J. T.: Alveolar Bone Induction: Autografts and Allografts. Dent. Clin. North Am. 24:719-737 (1980). Mellonig, J. T.: Histologic Evaluation of Freeze-Dried Bone Allografts in Periodontal Osseous Defects. J. Dent. Res. 60:388 (1981). Mellonig, J. T.: Decalcified Freeze-Dried Bone Allograft as an Implant Material in Human Periodontal Defects. Int. J. Periodontics Restorative Dent. 4(6):41-55 (1984). Mellonig, J. T.: Bone Grafts in Periodontal Therapy. NY State Dent. J. 52:27-29 (1986). Mellonig, J. T.: Freeze-Dried Bone Allografts in Periodon- tal Reconstructive Surgery. Dent. Clin. North Am. 35:505-520 (1991). Mellonig, J. T. and G. M. Bowers: Regenerating Bone in Clinical Periodontics. J. Am. Dent. Assoc. 121:497-502 (1990). Mellonig, J. T. and R. Levey: The Effect of Different Par- ticle Sizes of Freeze-Dried Bone Allograft on Bone Growth. J. Dent. Res. 63:222 (1984). Moomaw, R.: Histological Evaluation of Freeze-Dried Bone Allografts in Humans. Graduate thesis, University of North Carolina, School of Dentistry (1978). Moscow, B., F. Karsh, S. Stein: Histological Assessment of Autogenous Bone Graft: A Case Report and Critical Evaluation. J. Periodontol. 50:291-300 (1979). Movin, S. and G. Borring-Moller: Regeneration of Infra- bony Periodontal Defects in Humans After Implantation of Allogeneic Demineralized Dentin. J. Clin. Periodon- tol. 9:141-146(1982). Munting, E., J. Wilmart, A. Wijne, P. Hennebert, and C.
Delloye: Effect of Sterilization on Osteoinduction. Acta Orthop. Scand. 59:34-38 (1988). Nabers, C , O. Reed, and J. Hammer: Gross and Histologic Evaluation of an Autogenous Bone Graft 57 Months Postoperatively. J. Periodontol. 43:702-704 (1972). Nabers, C. L.: Long-Term Results of Autogenous Bone Grafts. Int. J. Periodontics Restorative Dent. 4(3): 50 57 (1984). Nabers, C. L. and T. J. O'Leary: Autogenous Bone Trans- plants in the Treatment of Osseous Defects. J. Perio- dontol. 36:5-14 (1965). Narang, R. and H. Wells: Bone Induction in Experimental Periodontal Bone Defects in Dogs with Decalcified Al-
349
logeneic Bone Matrix Grafts. Oral Surg. 33:306-313 (1972). Niveus, R., D. Johansson, and J. Egelberg: The Effect of Autogenous Cancellous Bone Grafts on Healing of Experimental Furcation Defects in Dogs. J. Periodont. Res. 13:532-537 (1978). Nyman, S., J. Gottlow, J. Lindhe, T. Karring, and J. Winnstrom: New Attachment Formation by Guided Tis- sue Regeneration. J. Periodont. Res. 22:252-254 (1987). Nyman, S., T. Karring, J. Lindhe, and S. Planten: Healing Following Implantation of Periodontitis Affected Roots into Gingival Connective Tissue. J. Clin. Periodontol. 7:394-401 (1980). Nyman, S., J. Lindhe, T. Karring, and H. Rylander: New Attachment Following Surgical Treatment of Human Periodontal Disease. J. Clin. Periodontol. 9:290-297 (1982). Oikarien, J. and L. Korhonen: The Bone Inductive Capacity of Various Bone Transplanting Materials Used for the Treatment of Experimental Bone Defects. Clin. Orthop. 140:208-215 (1979). Older, L. B.: The Use of Heterogenous Bovine Bone Im- plants in the Treatment of Periodontal Pockets. J. Periodontol. 38:359-549 (1967). Oreamuno, S., V. Lekovic, B. Kenney, F. Carranza, H. Takei, and B. Prokic: Comparative Clinical Study of Porous Hydroxyapatite and Decalcified Freeze-Dried Bone in Human Periodontal Defects. J. Periodontol. 61:399-404 (1989). Passanezzi, E., W. A. Janson, D. Nahas, and J. Campos: Newly Forming Bone Autografts to Treat Periodontal Infrabony Pockets: Clinical and Histological Events. Int. J. Periodontics Restorative Dent. 9:140-153 (1989). Patterson, R. L., C. Collings, and E. Zimmermann: Au- togenous Implants in the Alveolar Process of the Dog with Induced Periodontitis. Periodontics 5:19-25 (1967). Patur, B.: Osseous Defects: Evaluation of Diagnostic and Treatment Methods. J. Periodontol. 45:523-541 (1974). Patur, B. and I. Glickman: Clinical and Roentgenographic Evaluation of the Post-Treatment Healing of Infrabony Pockets. J. Periodontol. 33:164-171 (1962). Pearson, G. and E. Freeman: The Composite Graft: Au- togenous Cancellous Bone and Marrow Combined with FreezeDried Bone Allograft in the Treatment of Per- iodontal Osseous Defects. Ont. Dent. 57:3-10 (1980). Pearson, G., S. Rosen, and D. Deporter: Preliminary Ob- servations on the Usefulness of a Decalcified Freeze- Dried Cancellous Bone Allograft Material in Periodontal Surgery. J. Periodontol. 52:55-59 (1901). Peffier, J. E.: The Present Status of Bone Grafts in Perio- dontal Therapy. Dent. Clin. North Am. 13:193-202 (1969). Pierce, P. L.: Bone Induction in Periodontal Therapy: A Review. J. N. Z. Soc. Periodontol. 53:7-11 (1982). Poison, A. M. and L. D. Heijle: Osseous Repair in Infrabony Periodontal Defects. J. Clin. Periodontol. 5:1323 (1978). Pontoriero, R., J. Lindhe, S. Nyman, T. Karring, E. Ro- senberg, and R. Sanavi: Guided Tissue Regeneration in Degree II Furcation Involved Mandibular Molars. J. Clin. Periodontol. 15:247-254 (1988). Pontoriero, R., J. Lindhe, S. Nyman, T. Karring, E. Ro- senberg, and R. Sanavi: Guided Tissue Regeneration in the Treatment of Furcation Defects in Mandibular Mo- lars. A Clinical Study of Degree III Involvements. J. Clin. Periodontol. 16:170-178 (1989). Poulsom, R. C , A. Rubinstein, and A. W. Gargiulo: Al- logeneic Iliac Transplants in Rhesus Monkeys: A Se- quential Histologic Study. J. Periodontol. 47:187-195 (1976). Prewett, A., C. Damien, M. Te-Hua Chu, and R. O'Leary: Investigation of the Effect of Low-Dose Gamma Irra- diation on the Collagenous and Non-Collagenous Pro- teins of Bone Matrix. 14th Annual Meeting, American Association of Tissue Banks. 21-26 September, Denver, Colorado. Prolo, D., P. Pedrotti, and D. White: Ethylene Oxide Ster- ilization of Bone, Dura Mater, and Fascia Lata for Hu- man Transplantation. Neurosurgery. 6:529-539 (1980). Quattlebaum, J., J. Mellonig, and N. Hansel: Antigenicity of Freeze-Dried Cortical Bone Allograft in Human Per- iodontal Osseous Defects. J. Periodontol 59:394-397 (1988). Quinnan, G., J. Wlees, and M. Wittek: Inactivation of Human T-Cell Lymphotropic Virus, Type III by Heat Chemicals and Irradiation. Transfusion 26:481-483 (1986). Quintero, G., J. Mellonig, and V. Gambill: A Six Month Clinical Evaluation of Decalcified Freeze-Dried Bone Allograft in Human Periodontal Defects. J. Periodontol. 53:726-730 (1982). Ramfjord, S. P.: Changing Concepts in Periodontics. J. Pros. Dent. 52:781-786 (1984). Reddi, A. H., S. Wientroub, and N. Muthukmuaran: Bi- ologic Principles of Bone Induction. Orthop. Clin. North Am. 18:207-212 (1987). Renvert, S. T., S. Garrett, R. G. Schallhorn, and J. Egel- berg: Healing After Treatment of Periodontal Intraos- seous Defects. III. Effect of Osseous Grafting and Citric Acid Conditioning. J. Clin. Periodontol. 6:441-445 (1985). Resnick, L., K. Veren, S. Salahuddin, S. Tondreau, and P. Markham: Stability and Inactivation of HTLV-III/ LAV Under Clinical and Laboratory Environments. JAMA 255:1987-1991 (1986). Rivault, A. T., P. D. Toto, S. Levy, and A. W. Gargiulo: Autogenous Bone Grafts: Osseous Coagulum and Os- seous
Retrograd Procedures in Primates. J. Periodontol. 42:787-796 (1971). Robinson, R. E.: Osseous Coagulum for Bone Induction. J. Periodontol. 40:503-510 (1969). Rosenberg, M. M.: Free Osseous Tissue Autografts as a Predictable Procedure. J. Periodontol. 42:195-209 (1971). Rosling, B., S. Nyman, J. Lindhe, andB. Jern: The Healing Potential of the Periodontal Tissues Following Different Techniques of Periodontal Surgery. J. Clin. Periodontol. 3:233-250 (1976).
350
Ross, S. E. and D. W. Cohen: The Fate of a Free Osseous Tissue Autograft. A Clinical and Histologic Case Report. Periodontics 6:145-151 (1968). Rummelhardt, J., J. T. Mellonig, J. Gray, and H. Towle: Comparison of Freeze-Dried Bone Allograft in Human Periodontal Osseous Defects. J. Periodontol. 60:655663 (1989). Sampath, T., M. Nathanson, and A. Reddi: In Vitro Trans- formation of Mesenchymal Cells Derived from Embry- onic Muscle into Cartilage in Response to Extracellular Matrix Components of Bone. Proc. Natl. Acad. Sci. U.S.A. 81:3419-3423 (1984). Sampath, T. and A. Reddi: Homology of Bone Inductive Proteins from Human, Monkey, Bovine, and Rat Extra- cellular Matrix. Proc. Natl. Acad. Sci. U.S.A. 80:65916595 (1987). Sanders, J., W. Sepe, G. Bowers, R. Koch, J. Williams, J. Lekas, J. Mellonig, G. Pelleu, and B. Gambill: Clin- ical Evaluation of Freeze-Dried Bone Allograft in Per- iodontal Osseous Defects. III. Composite Freeze-Dried Bone Allografts with and Without Autogenous Bone Grafts. J. Periodontol. 1983:54:1-11 (1983). Schallhorn, R.: Postoperative Problems Associated with Il- iac Transplants. J. Periodontol. 43:3-9 (1972). Schallhorn, R. and W. Hiatt: Human Allografts of Iliac Cancellous Bone and Marrow in Periodontal Osseous Defects, II. Clinical Observations. J. Periodontol. 43:6781 (1972). Schallhorn, R. and P. McClain: Combined Osseous Com- posite Grafting, Root Conditioning, and Guided Tissue Regeneration. Int. J. Periodontics Restorative Dent. 8(4): 13-32 (1988). Schallhorn, R. G.: Eradication of Bifurcation Defects Uti- lizing Frozen Autogenous Hip Marrow Implants. J. West. Soc. Periodont. Abstr. 15:101-105 (1967). Schallhorn, R. G.: The Use of Autogenous Hip Marrow Biopsy Implants for Bony Crater Defects. J. Periodon- tol. 39:145-147 (1968). Schallhorn, R. G.: Present Status of Osseous Grafting Pro- cedures. J. Periodontol. 48:570-576 (1977). Schallhorn, R. G.: Long-Term Evaluation of Osseous Grafts in Periodontal Therapy. Int. Dent. J. 30:101-116 (1980). Schallhorn, R. G., W. Hiatt, and W. Boyce: Iliac Trans- plants in Periodontal Therapy. J. Periodontol. 41:566580(1970). Schrad, S. and G. Tussing: Human Allografts of Iliac Bone and Marrow in Periodontal Osseous Defects. J. Perio- dontol. 57:205-210 (1986). Scopp, I. W., F. H. Morgan, J. J. Dooner, H. J. Fredrics, and R. A. Heyman: Bovine Bone (Boplant) Implants for Infrabony Oral Lesions. Periodontics 4:169-176 (1966). Seibert, J. S.: Reconstructive Periodontal Surgery: Case Report. J. Periodontol. 41:113-118 (1970). Sepe, W., G. Bowers, J. Lawrence, G. Friedlaender, and R. Koch: Clinical Evaluation of Freeze-Dried Bone Al- lografts in Periodontal Osseous Defects. J. Periodontol. 49:9-14 (1978). Soehren, S. E. and R. L. Van Swol: The Healing Extraction Site: A Donor Area for Periodontal Grafting Material. J. Periodontol. 50:128-133 (1979). Sonis, S. T., R. C. Williams, M. K. Jeffcoat, R. Black, and G. Schlar: Healing of Spontaneous Periodontal De- fects in Dogs Treated with Xenogeneic Demineralized Bone. J. Periodontol. 56:470-479 (1985). Sottosanti, J. S. and J. A. Bierly: The Storage of Marrow and its Relation to Periodontal Grafting Procedures. J. Periodontol. 46:162-170 (1975). Stahl, S. S. and S. Froum: Histological Evaluation of Hu- man Intraosseous Healing Responses to the Placement of Tricalcium Phosphate Ceramic Implants. I. Three to Eight Months. J. Periodontol. 57:211-217 (1986). Stahl, S. S. and S. Froum: Histologic Healing Responses in Human Vertical Lesions Following the Use of Osseous Allografts and Barrier Membranes. J. Clin. Periodontol. 18:149-152(1991). Strub, J. R., T. W. Gaberthuel, and A. R. Firestone: Com- parison of Tricalcium Phosphate and Frozen Allogeneic Bone Implants in Man. J. Periodontol. 50:624-629 (1979). Towle, H., P. Auclair, and B. Ragsdale: Sterilization and Bone Induction by Demineralized Bone Matrix. J. Periodontol. 58:129 (1987). Turner, D. and J. T. Mellonig: Antigenicity of Freeze-Dried Bone Allograft in Periodontal Osseous Defects. J. Per- iodont. Res. 16:89-99 (1981). Urist, M., R. Delange, and G. Finerman: Bone Cell Dif- ferentiation and Growth Factors. Science 220:680-686 (1983a). Urist, M. R.: Bone Formation by Autoinduction. Science 150:893-899 (1965). Urist, M. R. and T. A. Dowell: Inductive Substratum for Osteogenesis in Pellets of Paniculate Bone Matrix. Clin. Orthop. 61:61-78 (1968). Urist, M. R., T. A. Dowell, P. H. Hay, and B. S. Strates: Inductive Substrates for Bone Formation. Clin. Orthop. 59:59-96 (1968). Urist, M. R. and H. Iwata: Preservation and Biodegradation of the Morphogenetic Property of Bone Matrix. J. Theor. Biol. 38:155-167(1973). Urist, M. R., J. Jurist, F. Dubuc, and B. Strates: Quanti- tation of New Bone Formation in Intramuscular Implants of Bone
Matrix in Rabbits. Clin. Orthop. 68:279-293 (1970). Urist, M. R., A. Mikulski, and S. D. Boyd: A Chemo- sterilized Antigen-Extracted Autodigested Alloimplant for Bone Banks. Arch. Surg. 110:416-428 (1975). Urist, M. R., K. Sato, A. Brownell, T. Malinin, A. Lietze, Y. Huo, D. Prolo, S. Oklund, G. Finerman, and R. Delange: Human Bone Morphogenetic Protein (hBMP). Proc. Soc. Exp. Biol. Med. 173:194-199 (1983). Urist, M. R. and B. Strates: Bone Formation in Implants of Partially and Wholly Demineralized bone Matrix. Clin. Orthop. 71:271-278 (1970). Urist, M. R. and B. Strates: Bone Morphogenetic Protein. J. Dent. Res. 50:1392-1406 (1971). Waal, H., M. P. Ruben, G. Castellucci, and A. Bloom: Histological Evaluation of Lyophilized Demineralized Dentin for the Treatment of Periodontal Osseous Defects in Dogs. Int. J. Periodontics Restorative Dent. 8(1):4963 (1988).
351
Wada, T., C. Wu, S. Hirozuki, N. Sugita, S. Katagiri, M. Shemizu, and H. Kohji: Autogenous, Allogeneic, and Beta TCP Grafts: Comparative Effectiveness in Exper- imental Bone Furcation Defects in Dogs. J. Oral Im- plantol. 15:231-235 (1989). Weintroub, S. and A. Reddi: Influence of Irradiation on the Osteogenic Potential of Demineralized Bone Matrix. Calcif. Tissue Int. 42:255-260 (1988). Werbitt, M.: Decalcified Freeze-Dried Bone Allografts: A Successful Procedure in the Reduction of Intrabony De- fects. Int. J. Periodontics Restorative Dent. 7(5):56-63 (1987). Wirthlin, M. R.: The Current Status of New Attachment Therapy. J. Periodontol. 52:529-544 (1981). Wiseman, L. and H. C. Tenebaum: Bone Grafting in Per- iodontal Therapy. A Review of Selected Materials. Oral Health 78:21-23 (1988). Wozney, J., V. Rosen, A. Celeste, L. Mitsock, M. Whit- ters, R. Kritz, R. He wick, and E. Wang: Novel Regu- lators of Bone Formation: Molecular Clones and Activ- ities. Science 242:1528-1534 (1988). Yazdi, M. and S. E. Schonfeld: Demineralized Bone Matrix in Treatment of Periodontal Defects. A Review of the Literature. J. Western Soc. Periodont. 35:105-108 (1987). Yukna, R. and W. Sepe: Clinical Evaluation of Localized Periodontosis Defects Treated with Freeze-Dried Bone Allografts Combined with Local and Systemic Tetra- cyclines. Int. J. Periodontics Restorative Dent. 2(5): 8 21 (1982). Yuktanandana, I.: Bone Grafts in the Treatment of Intrabony Periodontal Pockets in Dogs. A Histological Investiga- tion. J. Periodontol. 30:17-26 (1959). Yumet, J. and A. Poison: Gingival Wound Healing in the Presence of Plaque Induced Inflammation. J. Periodon- tol. 56:107-119(1985). Zayner, D. J. and R. A. Yukna: Particle Size of Periodontal Bone Grafting Materials. J. Periodontol. 55:406-409 (1984).
Zislis, T., S. Mattin, E. Cerbas, J. Heath, J. Mansfield, and J. Hollinger: A Scanning Electron Microscopic Study of In Vitro Toxicity of Ethylene-OxideSterilized Bone Repair Materials. J. Oral Implantol. 15:41-46 (1989).
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Autogenous and Allogeneic Bone Grafts in Periodontal Therapy

ICBM ICMB ICBM Reentry

2.15 mm (2-wall) 2.25 mm (1-wall) 2.0 mm gain attachment 0.8 mm

Froum et al. (1976)

Reentry and probing bone Reentry

X-ray 1.9 mm (39% fill) 2.8 mm (61% fill)

1.38 mm fill 1.0 mm (31% fill) 1.4 mm (36% fill)

0.3 mm fill Mabry et al. (1985)

OC-BB ICBM ECBM CBMA FDBA FDBA + TCN DFDBA

= Decalcified freeze-dried bone allograft. = Significant difference in favor of bone grafting.

ICBM ICBM Animal 4M Defect type created Intraosseous

Coverly et al. (1975)

Patterson et al. (1967)

Ellegaard et al. (1973)

Elegaard et al. (1974)

Ellegaard et al. (1975)

Nilveus et al. (1978) Caton et al. (1980)

Klinge et al. (1985) Passanezi et al. (1989)

FDBA DFDBA DBP

ICBM DFDBA Animal 12 D

3D Defect type created Intraosseous

Poulsom et al. (1976) Hurt (1969)

Mellonig (1981) Narang and Wells (1972)

Sonis et al. (1985)

Blumenthal et al. (1986)

Waal et al. (1988)

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