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Review Article

Journey of Bone Graft Materials in Periodontal Therapy:

A Chronological Review
Jitendra Kumar, Vaibhav Jain1, Somesh Kishore2, Harish Pal3
Departments of Periodontics, Oral and Maxillofacial Surgery and 2Pedodontics, KVG Dental College and Hospital, Sullia, Karnataka, 3Department of General Surgery,
1

Max Super Speciality Hospital, Ghaziabad, Uttar Pradesh, India

Abstract
Bone, the basic building block of the healthy periodontium, is affected in most of the periodontal diseases and can be managed either by
mechanically recontouring it or by grafting techniques, which encourages regeneration where it has been lost. Bone replacement grafts are
widely used to promote bone formation and periodontal regeneration. Bone grafting, placing bone or bone substitutes into defects created by
the disease process, acts like a scaffold upon which the body generates its own, new bone. A wide range of bone grafting materials, including
bone grafts and bone graft substitutes, have been applied and evaluated clinically, including autografts, allografts, xenografts, and alloplasts.
This review provides an overview of the clinical application, biologic function, and advantages and disadvantages of various types of bone
graft materials used in periodontal therapy till date with emphasis on recent advances in this field.

Key words: Alloplast, bone allograft, bone autograft, periodontal regeneration, xenograft

Introduction
Modern day periodontics aims at maintaining the health of
teeth and their supporting structures with the main goal of
controlling the infection and regenerating the lost supporting
structures.[1,2] The basic dogma of tissue regeneration is to
stimulate a cascade of healing events which, if coordinated,
can result in the completion of integrated tissue formation
and may prove to be a huge step‑up in managing advanced
periodontal disease and preventing tooth loss. Hence, this
review article focuses on the advantages and disadvantages
of various bone graft materials available till date in the light
of recent advances in this field.
Historical Background
The use of bone grafts for reconstructing intraosseous defects
produced by periodontal disease dates back to Hegedus in
1923.[7] Bone grafts have undergone a major turnover from then
to the present day. Here, we are reviewing various bone graft
substitutes in a chronological way for better understanding of
the development that has taken place. After Hegedus, it was
revived in 1965 by Nabers and O’leary, they used shavings of
cortical bone removed by hand chisels during osteoplasty and
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ostectomy and they were used to treat one, two‑wall defect.[8]
Allografts of iliac bone and marrow were used by Schallhorn
et al. in 1970.[4] Freeze‑dried bone allografts (FDBAs) have
shown that 60–68% of the defects had 50% or more bone fill
on re‑entry which was found in a study done by Mellonig
et al. in 1981.[10] Dense hydroxyapatite (HA) has been shown
to compare favorably with debridement in the reduction of
probing depth and increasing clinical attachment level by
Meffert et al. in 1985.[11] Yukna in 1990 did a clinical 6‑month
study on hard tissue replacement (HTR) polymer (HTR
synthetic bone) and showed a significant defect fill and
improved attachment level relative to open flap debridement
(OFD).[12] Bio‑Oss is a bovine bone from which all inorganic
components are removed and used for regeneration by
Richardson et al. in 1999.[13]
Address for correspondence: Dr. Jitendra Kumar,
Department of Periodontics, KVG Dental College and Hospital,
Sullia, Karnataka, India.
E‑mail: kumarbaisla001@gmail.com
This is an open access article distributed under the terms of the Creative
Commons Attribution-NonCommercial-ShareAlike 3.0 License, which
allows others to remix, tweak, and build upon the work non-commercially,
as long as the author is credited and the new creations are licensed under
the identical terms.
For reprints contact: reprints@medknow.com

DOI: How to cite this article: Kumar J, Jain V, Kishore S, Pal H. Journey of
10.4103/2277-4696.185195 bone graft materials in periodontal therapy: A chronological review. J Dent
Allied Sci 2016;5:30-4.

30 © 2016 Journal of Dental and Allied Sciences | Published by Wolters Kluwer - Medknow
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Kumar, et al.: Bone graft in periodontal therapy

Objective of Bone Graft Therapy • Osteoconduction is a physical effect by which the matrix
of the graft forms a scaffold that favors outside cells to
The objectives of bone graft therapy as stated by Schallhorn
penetrate the graft and form new bone
et al. in 1970[4] include:
• Osteopromotion involves the enhancement of osteoinduction
• Probing depth reduction
• Clinical attachment gain without the possession of osteoinductive properties.
• Bone fill of the osseous defect
For example, enamel matrix derivative has been shown to
• Regeneration of new bone, cementum, and periodontal
enhance the osteoinductive effect.
ligament.

We feel that for better efficacy and result of bone graft
therapy, the following additional objectives should also be
considered – easy availability, good handling properties, easy
storage, no/less adverse tissue reactions, and cost‑effectiveness.
Classifications
Various researchers have classified bone graft materials in
different ways.
Hyatt and Butler[5] have classified tissue grafts as follows:
• Autograft: Tissue taken from one operative site and
grafted in another operative site within the same
individual
• Homograft/allograft: Tissue taken from one operative
site in one individual and grafted in the operative site in
another individual of the same species
• Heterograft/xenograft: Tissue taken from one individual
and grafted in the operative site of another individual of
the different species
• Syngensio grafts: Tissue graft removed from blood‑related
relatives
• Orthotopic graft: Tissue grafted into an anatomical site
normally occupied by that tissue, for example, bone to
bone and skin to skin.
Selection of Bone Graft Material
According to Schallhorn in 1977,[22] the considerations that
govern the selection of a material are biologic acceptability,
predictability, clinical feasibility, minimal operative hazards,
minimal postoperative sequelae, and patient acceptance.
An ideal bone graft material should be easy to use and should
provide desirable results with minimal complications. Various
bone graft materials have been used and tested in the field of
medical science in the last few decades and many are still
under trial, ensuring promising results and may put end to the
search for a suitable bone graft material. Different bone graft
materials that are available, along with their properties, are
comprehensively explained in the following sections.
Autogenous Bone Graft
Autogenous grafts can be harvested from intraoral or extraoral
sites. In 1923, Hegedus attempted to use intraoral autogenous
bone grafts for the reconstruction of bone defects produced by
periodontal disease.[8] This method was revived by Nabers and
O’leary in 1965. They used cortical bone shavings removed by
hand chisels from within the surgical site and reported coronal
increases in bone height.[9]

Carranaza and Newman[6] have broadly classified bone as Osseous Coagulum

shown in Table 1.
Mechanism of Bone Grafting
• Osteogenesis refers to the formation and development of
new bone by cells contained in the graft
• Osteoinduction is defined as a chemical process by which
molecules contained in the graft convert the neighboring
cells into osteoblasts, which, in turn, form bone
Robinson in 1969 described a technique using a mixture of
bone dust and blood that he termed as osseous coagulum. The
use of such material is based on the principle that the small
particle size is resorbed and replaced by host tissue.[10]
Disadvantages of the osseous coagulum derive from the
inability to use aspiration during accumulation of the coagulum;
another problem is the unknown quality and quantity of bone
fragments in the collected material.

Table 1: Carranza (1999) classification of bone graft materials

Autogenous bone Allograft Xenograft None bone graft Alloplast
materials
Bone from intraoral site‑ Bone from extra‑oral sites‑ Freeze dried Calf bone Sclera Porous hydroxyapatite
Osseous coagulum Iliac crest Decalcified freeze Kiel bone Cartilage Non ‑ porous hydroxyapatite
Bone blend Tibia dried bone allograft Anorganic bone Plaster of paris HTR polymer
Intraoral cancellous Calcium phosphate Beta tricalcium phosphate
bone marrow transplant biomaterials Bio‑active glass
Bone swaging Hydroxyl apatite ceramics
Tricalcium phosphate

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Kumar, et al.: Bone graft in periodontal therapy
Bone blend
The bone blend technique uses an autoclaved plastic capsule
and pestle. Bone is removed from a predetermined site,
triturated in the capsule to a workable, plastic‑like mass, and
packed into bony defects.
Bone swaging
This technique requires the existence of an edentulous area
adjacent to the defect from which the bone is pushed into contact
with the root surface without fracturing the bone at its base. Bone
swaging is technically difficult and its usefulness is limited.
Intraoral Cancellous Bone Marrow Transplants
Cancellous bone can be obtained from the maxillary tuberosity,
edentulous areas, and healing sockets. The maxillary tuberosity
frequently contains a good amount of cancellous bone,
particularly if the third molars are not present; also, foci of
the red marrow are occasionally observed.
Extraoral Autogenous Bone Graft
Schallhorn et al. in 1967 and 1968 introduced the use of
autogenous hip marrow grafts (iliac crest marrow) in the
treatment of furcation and intrabony defects. As much as
3–4 mm gain in crestal bone was reported following the
treatment of intrabony defects with hip marrow grafts by
Schallhorn et al. in 1970. Red, hemopoietic marrow is usually
obtained from the anterior or posterior superior iliac crest and
is used fresh or frozen.[3]
Disadvantages include due to the added expense, time, and
surgical procedure required, iliac crest marrow grafts are not
used in regenerative periodontal therapy today. In addition,
one of the inherent problems of using hemopoietic cells is
that they contain monoblastic precursors to osteoclasts, and
therefore, might cause some resorption when the autograft is
juxtaposed to the tooth roots.
Allograft
Allografts are grafts transferred between genetically dissimilar
members of the same species. The types of allografts used are
as follows:
• Frozen iliac cancellous bone and marrow
• Mineralized FDBAs
• Decalcified FDBAs (DFDBAs).
Freeze‑dried Bone Allograft
FDBAs were first used in periodontal therapy in the early
1970s by Mellonig et al. in 1976, although they have been used
clinically in orthopedic therapy since 1950. The development
of bone allograft as an alternative source of graft material was
spurred by the disadvantages of autogenously bone, which
include the need for a secondary surgical site to procure graft
material and the lack of intraoral sites to obtain sufficient
quantities of bone for deep or multiple grafts.[10]
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Decalcified Freeze‑dried Bone Allograft
DFDBA was first used in dentistry and medicine in 1965 by
Urist who showed through numerous animal experiments
that DFDBA could stimulate the formation of new bone
by osteoinduction. This graft material induces the host
undifferentiated mesenchymal cells to differentiate into
osteoblasts with subsequent formation of new bone. The
demineralization of the allograft with HCl induces the
bone‑inducing agent, which has been called the bone
morphogenic proteins.[14]
Xenograft
In contrast to DFDBA, bone mineral has also been produced,
which is free of organic component. This product, a xenograft,
is known as bovine anorganic cancellous bone. It is produced
from bovine bone by a special process, which removes its
organic components, but retains its inorganic structure. This
product contains biological apatite crystals, and it is either
produced as cancellous blocks or granules.
Recently, new processing and purification methods have
been utilized which make it possible to remove all inorganic
components of a bovine bone source and leave a nonorganic
bone matrix in an unchanged inorganic form (Bio‑Oss,
Endobone, Laddec, Bon‑Apatite).
A porcine nonantigenic collagen, known as Bio‑Oss collagen,
is also available. This is produced from healthy pigs, and
the collagen undergoes prolonged alkaline treatment, which
produces a bilayer structure and eliminates any risk of bacterial
and viral contamination. During further processing, the
terminal peptides (telopeptides) are split off from the collagen
molecules, and this process removes the area’s most concerned
with the antigenicity of the molecule.[15]
The main drawback with these materials is the risk of
transmission of bovine or porcine viruses or other infective
agents.
Alloplastic Materials
Alloplastic materials are synthetic, inorganic, biocompatible,
and/or bioactive bone graft substitutes, which are claimed to
promote bone healing through osteoconduction. The available
alloplastic materials are Plaster of Paris, polymers, calcium
carbonate, and ceramics.
Ceramics can be classified into resorbable  (e.g., tricalcium
phosphate and resorbable HA) and nonresorbable (dense HA,
porous HA, and bioglass).
Bioglass developed by Hench is one of the latest and promising
substitutes for bone graft materials.
Various alloplastic materials are illustrated in the following
sections.
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Kumar, et al.: Bone graft in periodontal therapy
Calcium Phosphate Ceramics
Larger number of ceramics are available, the calcium
phosphate type has been of particular interest because of
the close chemical and crystal resemblance of some of these
materials to bone mineral. Commonly used calcium phosphate
ceramics for periodontal regeneration are essentially of two
types: The relatively nonresorbable HA (Ca10(PO4) 6(OH) 2) or
the resorbable tricalcium phosphates (Ca3(PO4) 2).
Hydroxyapatite
The HA products used in periodontology are of two forms:
A particulate nonresorbable ceramic form and a particulate
resorbable nonceramic form. In controlled clinical studies,
grafting of intrabony periodontal lesions with HA resulted in
an attachment level gain of 1.1–3.3 mm which was greater
as compared with nongrafted surgically debrided controls by
Galgut et al. in 1992.[16]
Tricalcium Phosphate
Tricalcium phosphate has been shown to stimulate bone
formation, and is comparable or in most cases superior in this
regard to HA as described by Fetner et al. in 1994.[17] It has
been shown to stimulate bone formation to a greater extent than
HA, but to a much lesser extent than bioglass as described by
Wilson and Low in 1992.[18] Cultured human fibroblasts have
been demonstrated to attach readily to the surface of calcium
phosphate ceramics. HA acts as an amphoteric ion exchanger.
Selective accumulation of calcium and phosphate ion occurs
as a consequence of the negative charges on the HA surface.
This leads to the formation of more apatite and stimulates the
formation of new bone.
Plaster of Paris
Plaster of Paris is biocompatible and porous, thereby allowing
fluid exchange, which prevents flap necrosis. Plaster of Paris
resorbs completely in 1 or 2 weeks. Its usefulness in human
cases has not been proven.
Hard Tissue Replacement Polymer
HTR polymer is a nonresorbable, microporous
biocompatible composite of poly‑methylmethacrylate and
polyhydroxyethylmethacrylate, a resorbable polylactic acid
polymer. This material has been used in the fabrication of
contact lenses, lens transplants, and prosthetic heart valves over
many years. The polymer does not produce an inflammatory
or immune response in contact with bone or soft tissue as
described by Yukna in 1990.[19]
Bio‑active Glasses and Ceramics
Bioglasses are composed of Si‑CaO‑Na2O‑P2O5 and are
resorbable or not resorbable depending on the relative
proportion of these components. When bioglasses are exposed
Journal of Dental and Allied Sciences  ¦  Jan-Jun 2016  ¦  Volume 5  ¦  Issue 1
to tissue fluids, a double layer of silica gel and calcium
phosphate is formed on their surface. Through this layer, the
material promotes absorption and concentration of proteins
used by osteoblasts to form an extracellular bone matrix which
may theoretically promote bone formation as described by
Hench et al. in 1972.[20] They have been extensively used in
conjunction with medical and dental implants because they
develop a layer of hydroxy‑carbonate‑apatite on their surface
following exposure to body fluids. When used on the surface
of metal implants, this layer incorporates collagen fibrils and
in this way produces a mechanically strong bond between
implant and the adjacent bone surface as described by Hench
and West in 1996.[21]
Nonbone Graft Materials
In addition to bone graft materials, many nonbone graft
materials have been tried to restore the periodontium. Among
them are sclera, dura, cartilage, cementum, dentin, and
coral‑derived materials.
New Innovations
PepGen P‑15
It is a bone grafting material used to fill periodontal osseous
defects that is composed of anorganic bovine‑derived HA
bone matrix combined with a synthetic cell‑binding peptide.
Growth factor‑enhanced matrix 21S
Growth factor‑enhanced matrix (GEM) 21S is a synthetic
grafting system for bone and periodontal regeneration
composed of a purified recombinant growth factor and a
synthetic calcium phosphate matrix.
GEM 21S is supplied in a single‑use kit. Each GEM 21S kit
consists of the following:
• One cup containing 0.5cc of beta‑tricalcium phosphate
particles (0.25–1.0 mm)
• One syringe containing a solution of 0.5 ml recombinant
human platelet‑derived growth factor‑BB (0.3 mg/ml).
Biodegradable Composite Scaffolds
Researchers are working hard to develop a strategy to modulate
stem cell behavior by developing biodegradable composite
scaffolds. Research activities on biological applications and,
in particular, on stem cell interaction of a biodegradable
nanocomposite have started only recently. We expect that
biodegradable polymeric nanocomposites will most likely
become one of the widely used substrates for bio‑applications.
There is a great necessity for the development of these
multifunctional nanocomposite scaffolds, but there are some
difficulties and challenges to overcome in their fabrication.[23]
Conclusion
Bone grafting is one of the most commonly used options to
treat large bone defects in periodontal regenerative therapy.
33
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Kumar, et al.: Bone graft in periodontal therapy
Although not all bone grafting materials support the formation
of a new periodontal attachment apparatus, there is conclusive
evidence that periodontal regeneration is achievable with bone
replacement grafts in humans. Autografts remain the gold
standard since they provide osteogenic cells, osteoinductive
growth factors, and an osteoconductive scaffold, all essential
for new bone growth, but carry the limitations of morbidity
at the harvesting site and limited availability. Allografts,
xenografts, and tissue‑engineered grafts all have shortcomings.
New strategies such as gene therapy, polytherapy by using
scaffolds, healing promotive factors and stem cells, and finally
three‑dimensional printing are in their preliminary stages, but
may open new insights shortly.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
1. Sukumar S, Drízhal I. Bone grafts in periodontal therapy. Acta
Medica (Hradec Kralove) 2008;51:203‑7.
2. Glossary of Periodontic Terms. American academy of Periodontology;
2001.
3. Elsalanty ME, Genecov DG. Bone grafts in craniofacial surgery.
Craniomaxillofac Trauma Reconstr 2009;2:125‑34.
4. Schallhorn RG, Hiatt WH, Boyce W. Iliac transplants in periodontal
therapy. J Periodontol 1970;41:566‑80.
5. Hyatt GW, Butler MC. The procurement, storage, and clinical use of
bone homografts. Instr Course Lect 1957;14:343‑73.
6. Carranaza FA, Newman MG. Reconstructive Osseous Surgery. In:
Clinical Periodontology. Philadelphia, USA: WB Saunders Company;
1999;8:622-39.
7. Hegedus Z. The rebuilding of the alveolar process by bone
transplantation. Dent Cosmos 1923; 65:736.
34 Journal of Dental and Allied Sciences  ¦  Jan-Jun 2016  ¦  Volume 5  ¦  Issue 1
8. Nabers CL, O’leary TJ. Autogenous bone transplants in the treatment of
osseous defects. J Periodontol 1965;36:5‑14.
9. Robinson E. Osseous coagulum for bone induction. J Periodontol
1969;40:503‑10.
10. Mellonig JT, Bowers GM, Cotton WR. Comparison of bone graft
materials. Part II. New bone formation with autografts and allografts: A
histological evaluation. J Periodontol 1981;52:297‑302.
11. Meffert RM, Thomas JR, Hamilton KM, Brownstein CN.
Hydroxylapatite as an alloplastic graft in the treatment of human
periodontal osseous defects. J Periodontol 1985;56:63‑73.
12. Yukna RA. HTR polymer grafts in human periodontal osseous defects.
I 6‑month clinical results. J Periodontol 1990;61:633‑42.
13. Richardson CR, Mellonig JT, Brunsvold MA, McDonnell HT,
Cochran DL. Clinical evaluation of Bio‑Oss: A bovine‑derived
xenograft for the treatment of periodontal osseous defects in humans.
J Clin Periodontol 1999;26:421‑8.
14. Urist MR. Bone: Formation by autoinduction. Science 1965;150:893‑9.
15. Araújo M, Linder E, Wennström J, Lindhe J. The influence of Bio‑Oss
Collagen on healing of an extraction socket: An experimental study in
the dog. Int J Periodontics Restorative Dent 2008;28:123‑35.
16. Galgut PN, Waite IM, Brookshaw JD, Kingston CP. A 4‑year controlled
clinical study into the use of a ceramic hydroxylapatite implant material
for the treatment of periodontal bone defects. J Clin Periodontol
1992;19:570‑7.
17. Fetner E, Martigan MS, Low SB. Periodontal repair using PerioGlas
in non‑human primates: Clinical and histologic observations. Compend
Contin Educ Dent 1994;12:932‑9.
18. Wilson J, Low SB. Bioactive ceramics for periodontal treatment:
Comparative studies in the Patus monkey. J Appl Biomater 1992;3:123‑9.
19. Yukna RA. HTR polymer grafts in human periodontal osseous defects.
I 6‑month clinical results. J Periodontol 1990;61:633‑42.
20. Hench LL, Splinter RJ, Allen WC, Greenlee TK Jr. Bonding mechanism
at the interface of ceramics prosthetic materials. J Biomed Mater Res
Symp 1972;2:117‑41.
21. Hench LL, West JK. Biological applications of bioactive glasses. Life
Chem Rep 1996;13:187‑241.
22. Schallhorn RG. Present status of osseous grafting procedures.
J Periodontol 1977;48:570‑6.
23. Armentano I, Fortunati E, Mattioli S, Rescignano N, Kenny JM.
Biodegradable composite scaffolds: A strategy to modulate stem cell
behaviour. Recent Pat Drug Deliv Formul 2013;7:9‑17.