Autogenous and Allogeneic Bone Grafts in Periodontal Therapy

Critical Reviews in Oral Biology & Medicine 

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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 for- 

1045-4411/92/$.50 

© 1992 by CRC Press, Inc. 

mation. 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 (Pfeifer, 

1969; Groff, 1976a and b; Ellegaard, 1976; 

Schallhorn, 1977; Schallhorn, 1980; Mellonig, 

1980; Wirthlin, 1981; Gara and Adams, 1981; 


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333

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 Bowers, 

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 reconstitution 

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 

334 

is usually determined by surgical reentry 

procedures. 

Intraosseous (intrabony) refers to a periodontal 

defect within bone. 

An autograft is a tissue graft (bone) transferred 

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 potassium 

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 excellent 

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 protracted 

sequestration and slow resorbtion mitigated 

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 ex- 



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 anecdotal 

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 instance 

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 chisels 

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 primarily 

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 publication 

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

336 

TABLE 1 

Human Controlled Studies with Bone Autografts and Allografts in the 

Treatment of Periodontal Osseous Defects 

Graft 

material 

ICBM 

OC-BB 

ECBM 

ICBM 

ICMB 

ICBM 

ICBM 

ECBM 

ICBM 

ECBM 

CBMA 

ICBM 

CBMA 

CBMA 

CBMA 

FDBA 

FDBA 

FDBA 

FDBA 

+ 

TCN 

DFDBA 

DFDBA 

DFDBA 

DFDBA 

DFDBA 

Method of 

evaluation 

Probing and 

radiographs 

Reentry 

Probing 

Probing and 

X-rays 

Probing bone 

level 

Reentry 

Histology 

Histology 

Reentry and 

probing bone 

Reentry 

Reentry 

Histology 

Reentry 

X-ray 

Histology 

Reentry 

Reentry 

Histology 

Graft 

Mean iesults 

Equal degree of success 

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 


(significant only 

for deepest 

defects) 

Control 

0.66 mm 

(22% fill) 

2.15 mm (2-wall) 

2.25 mm (1-wall) 


attachment 

0.8 mm 

No significant difference 

Graft improved results of treatment 

Regeneration 

consistently 

found 

New bone and 

cementum 

4.83 mm fill 

1.6 mm 


Lack of cementogenesis 

and 

bone formation 

Little if any new 

cementum or 

bone 

0.22 mm fill 

0.8 mm 


60% defects 60% defects 

>50% bone fill >50% fill 

New attachment greater in grafted 

sites 

1.9 mm (39% fill) 

2.8 mm (61% fill) 

1.38 mm fill 

No difference in healing 

1.0 mm (31% fill) 

1.4 mm (36% fill) 

0.3 mm fill 

2.57 mm 

1.26 mm 

(65% bone fill) (38% fill) 

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 



Ref. 

Ellegaard and 

Loe(1971) 

Froum et al. 

(1976) 

Carraro et al. 

(1976) 

Movin et al. 

(1982) 

Renvert et al. 

(1985) 

Patur(1974) 

Hiatt et al. 

(1978) 

Listgarten and 

Rosenberg 

(1979) 

Hiatt et al. 

(1986) 

Schrad and 

Tussing 

(1985) 

Altiere et al. 

(1979) 

Moomaw 

(1978) 

Mabry et al. 

(1985) 

Pearson et al. 

(1981) 

Dragoo and 

Kaldahl 

(1983) 

Mellonig (1984) 

Santes et al. 

(1988) 

Bowers et al. 

(1989b)

DFDBA 

DFDBA 

OC-BB 

ICBM 

ECBM 

CBMA 

FDBA 

FDBA + 

TCN 

DFDBA 

Histology 

Reentry 

New bone, cementum, 

PDL 

2.60 mm bone fi 

No new attachment 

apparatus 

0.38 mm bone fill 

= 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 amalgam 

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 

Bowers et al. 

(1989c) 

Blumenthal and 

Steinberg 

(1990) 

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; Sottosanti 

and Bierly, 1975; Amler, 1984). This 

material is obtained from either the anterior or 

the posterior iliac crest (Schallhorn, 1968; Dragoo 

and Irwin, 1972). Schallhorn's reports of 

complete eradication of furcation and interproximal 

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 (Schallhorn 

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 Al log 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 accompanying 

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. Undermineralized 

(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 donor 

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). 

338 

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 maintained 

relatively intact (Friedlaender, 1988; Mellonig, 

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 



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 opposed 

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 (Koskinen 

et al, 1972; Chalmers et al., 1975; Oikarien 

and Korhonen, 1979; Mellonig et al., 

1981a and b). Demineralization with hydrochloric 

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 differentiate 

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; Bowers 

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 mi- 

neralization. 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 

FDB A (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 insufficient 

inductive bone protein in DFDBA or 

the types and depths of the grafted lesions. Additional 

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, 1985; 

Resnick et al, 1986; Quinnan et al, 1986). 

4. Allografts Compared with Alloplasts 

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 

340 

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 extrapolate 

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 biologically 

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. Using 

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), 



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 

Defect type 

Animal created 

4 M Intraosseous 

4 M 2- and 3-Wall 

10 D Intraosseous 

10 D Furcation 

6 M Furcation 

12 M 3-Wall 

19 M Furcation 

6 D Furcation 

8 M 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 adaptation 

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 facilitate 

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

342 

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 

OC = Osseous coagulum autograft. 

ICBM = Intraoral cancellous bone and marrow autograft. 

ECBM = Extraoral (iliac) cancellous bone and marrow autograft. 

CBMA = Cancellous bone and marrow allograft. 

FDBA = Freeze-dried bone allograft. 

DFDBA = Decalcified freeze-dried bone allograft. 

DFDDA = Decalcified freeze-dried dentin allograft. 

DBP = Demineralized bone powder. 

D = Dog. 

M = Monkey. 

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) 



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 indication 

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 coronalectomy 

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 sug- 

gest 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 sequela 

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 Sullivan, 

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). Freezing 

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). Extensive 

root resorption was not observed. Because 

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 postsurgical 

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 Rosenberg, 

1979; Karring et al, 1980; Caton and Zander, 

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, Bowers 

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 deposits 

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 Association 

of Tissue Banks, 1984). If exclusionary 

techniques such as medical and social screening, 

antibody testing, direct antigen tests, other serologic 

tests, bacterial culturing, autopsy, and follow-up 

studies of grafts from the same donor are 

344 

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 hydrochloric 

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 manner 

within 12 h of death of the donor. Cortical 

bone is less antigenic than cancellous 

bone (Friedlaender et al, 1976) and has a 

higher concentration of bone-inductive proteins 

(Urist and Do well, 1968; Urist et al, 

1970). 

2. 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). 

3. The bone is frozen. Freezing decreases the 

risk of disease transfer (Buck et al, 1990). 

4. The cortical bone is ground to a final par- 



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 macrophage 

response (Mellonig and Levey, 

1984). 

5. The graft is again immersed in ethanol. 

6. The bone may or may not be dimineralized. 

7. 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; Pontoriero 

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 & Associates, 

Flagstaff, AZ) physical barrier or by a 

physical barrier alone. They found both horizontal 

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 pretreatment 

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. What are the possible local and systemic 

side effects of GFs? 

5. Can the effects of the GFs be limited to the 

local environment? 

6. Can results obtained with GFs in animal 

model systems be extrapolated to humans? 

7. What is the mechanism of action of GFs in 

the periodontal environment? 

8. 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. Regeneration 

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. 

346 

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