Hindawi Publishing Corporation

International Journal of Biomaterials

Volume 2013, Article ID 307136, 7 pages
http://dx.doi.org/10.1155/2013/307136

Review Article
Bone Substitutes for Peri-Implant Defects
of Postextraction Implants

Pâmela Letícia Santos,1 Jéssica Lemos Gulinelli,1 Cristino da Silva Telles,2 Walter Betoni
Júnior,2 Roberta Okamoto,3 Vivian Chiacchio Buchignani,1 and Thallita Pereira Queiroz4
1
Department of Oral Biology Postgraduation, Universidade do Sagrado Coração (USC), Bauru, SP, Brazil
2
School of Implantology of Cuiaba, Brazil
3
Department of Basic Sciences, School of Dentistry of Araçatuba, SP, Brazil
4
Department of Health Sciences, Implantology Post Graduation Course, Dental School,
University Center of Araraquara, UNIARA, SP, Brazil

Correspondence should be addressed to Pâmela Letı́cia Santos; [email protected]

Received 20 September 2013; Revised 8 November 2013; Accepted 11 November 2013

Academic Editor: Traian V. Chirila

Copyright © 2013 Pâmela Letı́cia Santos et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.

Placement of implants in fresh sockets is an alternative to try to reduce physiological resorption of alveolar ridge after tooth
extraction. This surgery can be used to preserve the bone architecture and also accelerate the restorative procedure. However,
the diastasis observed between bone and implant may influence osseointegration. So, autogenous bone graft and/or biomaterials
have been used to fill this gap. Considering the importance of bone repair for treatment with implants placed immediately after
tooth extraction, this study aimed to present a literature review about biomaterials surrounding immediate dental implants. The
search included 56 articles published from 1969 to 2012. The results were based on data analysis and discussion. It was observed
that implant fixation immediately after extraction is a reliable alternative to reduce the treatment length of prosthetic restoration.
In general, the biomaterial should be used to increase bone/implant contact and enhance osseointegration.

1. Introduction been used in those gaps to correct bone defects and provide
appropriate stability.
Although alveolar repair after tooth extraction can be con- Considering the importance of stability of immediate
ducted by blood clot, this repair is not complete due to physi- implants, this study presented a literature review about the
ological resorption [1]. Studies demonstrated that vertical and most common biomaterials used for immediate dental im-
horizontal dimensions are reduced around 11–22% and 29– plants.
63%, respectively, due to alveolar resorption after 6 months
following tooth extraction [2]. This atrophy is more intense in
the buccal surface (about 0.8 mm) during the first 3 months 2. Material and Method
[3].
The insertion of immediate implants in atrophic sockets The inclusion criteria assumed the studies published in
is a challenge to achieve satisfactory esthetics and function English from 1969 to 2012 searched at Medline (Pubmed) and
[4]. In this sense, in 1976, Schulte and Heimke [5] presented Bireme databases. The keywords “dental implant,” “osseointe-
the immediate implants that are placed in fresh sockets. gration,” “postextraction,” “bone substitute,” “fresh extraction
However, the diastasis observed between bone and sockets,” “immediate implant,” “bone repair,” “bone model-
implant after dental extraction may influence osseointegra- ing,” “dehiscence,” “dimension,” and “ grafting” were used for
tion [6]. So, autogenous bone grafts and/or biomaterials have searching.
2 International Journal of Biomaterials

Inclusion and evaluated the success rate of immediate implants associated

exclusion criteria with autogenous bone for filling of the peri-implant gap. In
this study, beagle dogs were used for insertion of implants
immediately after extraction of right and left maxillary and
1969–2012 mandibular lateral incisors. The gaps were filled with blood
n = 100 n = 63
English clot (control) and autogenous bone (experimental) and better
results were found for the autogenous bone graft.
Figure 1: Method flowchart. Nevertheless, this graft may cause morbidity in the dona-
tor area, hematoma, edema, infection, and vascular and nerve
lesions. In addition, this technique spends more time for
The search was based on scientific researches published surgical procedure and it is limited for large reconstructions
in English including systematic reviews and also animal and [15]. So, biomaterials have been suggested as an alternative to
human studies. The exclusion criteria were case reports and solve those limitations and reduce the gap between bone and
discussion articles. After analysis, 63 studies were selected implant.
according to the inclusion criteria. The results were based on
data analysis and discussion. (Figure 1)
3.3. Mineralized Bone Tissue. The matrix of mineralized bone
tissue is composed by deproteinized bone tissue. It has been
3. Literature Review widely used for preservation of alveolar ridge dimension after
tooth extraction, filling of bone defects near to natural teeth,
3.1. Gap Dimension. The distance between bone and implant and also during maxillary sinus lift [16–21].
is called peri-implant gap. The fresh socket is wider than In a study in monkeys, molars and premolar were
the implant diameter, which causes the peri-implant gap that extracted for fixation of titanium implants after 3 months.
influences stability and osseointegration [6, 7]. Peri-implant defects with 2.5 mm in width and 3.0 mm
In 1977, Schenk and Willenegger [8] conducted a study in height were filled with blood clot, polytetrafluorethy-
on rabbits and observed the lack of complete bone formation lene membrane, Bio-oss, and Bio-oss with membrane. The
with peri-implant gaps wider than 1.0 mm. In 1988, Carlsson histological analysis after 6 months revealed that Bio-Oss
et al. [9] used the same experimental model to compare 3 exhibits osteoconductive capacity and should be used for
values of peri-implant gap between bone and implant (group reconstruction of peri-implant bone defects [17].
A—0 mm, group B—0.35 mm, and group C—0.85 mm) and Hockers et al. [18] conducted a similar study including
observed residual gaps in groups B and C at 6 and 12 weeks one group with autogenous bone and observed that the bone
after surgery. grafts were integrated to the bone tissue.
In 1999, Akimoto et al. [10] placed postextraction Caneva et al. [19] used bone substitutes to fill the the
implants in dogs and evaluated the repair of peri-implant gap between bone and implant. The effect of bone fillers
gaps from 0.5 to 1.4 mm after 12 weeks. The results demon- (magnesium-enriched hydroxyapatite) on preservation of the
strated that the defect size is inversely proportional to the alveolar bone around immediate implants was evaluated in a
bone/implant contact. However, Botticelli et al. [6] per- dog study. Implants with a sandblasted acid etched surface
formed a similar study and found complete bone neofor- were placed into the fresh extraction sockets bilaterally
mation and osseointegration in defect with 1.0 mm after 16 into the dogs’ jaws. Magnesium-enriched hydroxyapatite was
weeks. placed at test sites,while the control sites did not receive aug-
mentation materials. After 4 months of healing, the animals
3.2. Autogenous Bone. Autogenous bone corresponds to bone were sacrificed. Histomorphometric evaluations showed that
graft obtained from the same individual. It is considered the alveolar bony crest outline was maintained to a higher
the gold standard for filling of bone defects since it allows degree at the buccal bone wall of the test sites (loss: 0.7 mm)
(I) osseointegration: direct contact with bone tissue without compared with the control sites (loss: 1.2 mm), even though
fibrous tissue [11]; (II) osteoconduction: support to bone this difference did not reach statistical significance.
growth [11]; (III) osteoinduction: differentiation of mesenchy- In another experimental study Caneva et al. [20] explored
mal cells of surrounding tissue (receptor site) into osteoblas- the effect of GBR based on deproteinized bovine bone
tic cells [12]; and (IV) osteogenesis: bone neoformation by mineral on alveolar ridge preservation and the reparation
osteoblastic cells present in the graft material [12]. Although of defects around osseointegrated implants. The authors
few mature osteoblasts survive to grafting, precursor cells are concluded that the application of DBBM concomitant with
responsible for the osteogenic potential [12]. a collagene membrane contributed in improving bone regen-
Autogenous grafts are presented as blocks or particles and eration in the defects.
can be used isolated or associated with allogenic or alloplastic Barone et al. [21] showed that regenerative techniques
grafts. The donator area can be mentonian region, retromolar (GBR) were able to limit resorption of the alveolar crest
area, maxillary tuberosity, iliac crest, rib, cranium, tibia, and after implant placement in a fresh extraction socket, tooth
fibula [13]. extraction.
Several studies evaluated peri-implant bone defects filled Hsu et al. [22] in an experimental study instead demon-
with autogenous bone. In 2013, Al-Sulaimani et al. [14] strated that the placement of implants and deproteinized
International Journal of Biomaterials 3

bovine bone mineral into fresh extraction sockets results in

significant buccal bone loss and low osseointegration.
Other clinical studies [23–25] used GBR techniques to fill
the gap between bone and implant.

3.4. Mineralized Bone Tissue with Addition of 10% Porcine

Collagen. This material is composed by mineralized bovine
bone matrix with addition of 10% porcine collagen (Bio-oss
Collagen, Geistlich). This biomaterial is indicated for filling of Figure 2: Initial panoramic radiograph.
extraction sockets, periodontal defects, and maxillary sinus
lifting [26].
Araújo et al. [27] conducted an animal study with filling
of extraction sockets with Bio-oss collagen. Biopsy and
histometric analysis were performed after 3 months and 12.35
demonstrated that the biomaterial promoted formation of
bone tissue, maintained the dimension of alveolar walls, and
preserved the alveolar crest profile.
In 2009, the same authors [28] performed a similar study 6.88
for evaluation after 2 weeks. The results showed delayed
6.44
alveolar repair with bone neoformation only at apical and
lateral walls.
Wong and Rabie [29] conducted a study in rabbits to
compare the amount of bone produced by Bio-Oss colla-
gen and collagen matrix. Eighteen bone defects (5.0 mm ×
10.0 mm) were created in the parietal bone of the rabbits and
filled with Bio-Oss collagen, collagen matrix and blood clot.
Biopsies were removed after 14 days for histological analysis.
The authors concluded that the Bio-Oss collagen presented
better results for bone neoformation in comparison to the
collagen matrix while no bone was formed with the blood
clot.
The study of Araújo et al. [30] is the only study evaluating
peri-implant defects filled with Bio-oss collagen. In this Figure 3: Initial computed tomography.
paper, dogs were used to evaluate bone repair after fixation
of immediate implants and insertion of mineralized bovine
bone with addition of 10% porcine collagen. Biopsies were [36]. Although the HA is resistant to physiological resorption
obtained after 6 months for histological analysis. The authors [37], its osteoconductive capacity remains uncertain [38, 39].
found that the presence of Bio-oss collagen changed the On the other hand, the 𝛽-tricalcium phosphate is absorbed
healing process of hard tissue, which improved bone/implant slowly and it is considered an osteoconductive material [40].
contact. Thus, the HA maintains the gap while the 𝛽-tricalcium
phosphate is absorbed to promote bone regeneration simul-
3.5. Beta-Tricalcium Phosphate. The 𝛽-tricalcium phosphate taneously [41].
has been considered a material with excellent results since In 2004, Boix et al. [42] evaluated the efficacy of this
it is absorbable, osteoconductive, and nonosteoinductive [1]. material in peri-implant defects in dogs and concluded
Animal [26, 31–33] and human [34] studies demonstrated that the biomaterial generated significant increase in bone
that this material supported bone neoformation. regeneration surrounding the dental implant.
In 2013, Daif [35] conducted a study to evaluate the
influence of 𝛽-tricalcium phosphate on bone density sur- 4. Discussion
rounding immediate dental implants using helical computer
tomography. Twenty-eight patients were selected and divided The extraction socket is usually wider than the implant
into two groups: (I) no filling and (II) filling with beta-TCP diameter, which results in a gap between the cervical region of
in the peri-implant defect. Tomography was obtained after 3 the implant and the bone tissue (Figures 2, 3, and 4). Although
and 6 months and showed that the 𝛽-tricalcium phosphate this gap can be restored by maintenance of blood clot [43],
increased bone density in the bone defect of immediate dental the use of biomaterials is indicated to preserve alveolar ridge
implants. dimensions and promote repair [36] (Figure 5). In addition,
Recently, some industries developed a synthetic bone the insertion of biomaterials simultaneously to the implant
substitute composed by a homogeneous mixture of 60% of fixation improves functional and esthetic restoration of the
hydroxyapatite (HA) and 40% of beta-tricalcium phosphate stomatognathic system (Figures 6 and 7).
4 International Journal of Biomaterials

Figure 6: Esthetic restoration.

Figure 4: Peri-implant defect.

Figure 5: Peri-implant defect filled with biomaterial.

Several animal [6, 7, 30, 44, 45] and human [34, 39, 46–
54] studies were conducted to evaluate the reconstruction
of the peri-implant gap with biomaterials through clinical
follow-up, histology, imaging, and immunohistochemistry.
However, few of the literature reviews about biomaterials for
peri-implant defects were found [55]. Figure 7: Final computed tomography.
The ideal bone graft should present limited source, lack of
morbidity in the donator site, no risk to disease transmission,
efficient bone repair, immediate stability, versatility, easy
manipulation, appropriate lifetime, and accessible cost [56]. association of both materials. No difference was observed
The autogenous bone is considered the first option for between the groups after a 5-year follow-up.
bone reconstruction in implantology since it presents char- Han et al. [60] compared bone regeneration in peri-
acteristics of the ideal graft. However, this approach requires implant defects of dogs according to the following groups: (I)
longer surgical procedure and may not obtain enough bone no filling, (II) autogenous bone, (III) Bio-Oss collagen, (IV)
volume [57]. So, alternative treatments have been suggest for Bio-Oss, (V) no filling and collagen membrane, (VI) autoge-
peri-implant reconstruction. nous bone and collagen membrane, (VII) Bio-Oss collagen
Jensen et al. [33] compared the performance of and collagen membrane, and (VIII) Bio-Oss and collagen
autogenous bone, 𝛽-tricalcium phosphate, and anorganic membrane. The authors concluded that reconstruction of
bovine bone by histological and histomorphometric analyses peri-implant defect with bone substitutes associated with
in pigs. The authors observed greater efficacy for the membrane or not increases the percentage of bone/implant
autogenous bone in comparison to the other grafts. contact.
On the other hand, Hockers et al. [18] compared grafting Guerra et al. [61] conducted a study on rabbits to compare
with autogenous bone and demineralized bovine bone for grafting with bovine bone, bovine bone associated with
reconstruction of peri-implant defects in dogs and found platelet-rich plasma, bovine bone protected by membrane,
similar integration for both materials. Similarly, Santis et al. and blood clot. A higher percentage of bone/implant contact
[58] concluded that the autogenous bone and demineralized with bovine bone protected by collagen membrane was
bovine bone provided a high level of bone regeneration and observed.
satisfactory bone/implant contact for osseointegration. Jensen et al. used immunohistochemistry in dogs to eval-
In 2009, Benić et al. [59] performed a human study to uate the performance of Bio-Oss collagen and Bone-Ceramic
assess the success rate of peri-implant defects reconstruction and found that both biomaterials are great osteoconductive
with autogenous bone, demineralized bovine bone, and materials for bone repair [33]. However, Antunes et al. [62]
International Journal of Biomaterials 5

evaluated repair with blood clot, autogenous bone, Bio-Oss, [8] R. K. Schenk and H. R. Willenegger, “Histology of primary bone
and Bone-Ceramic in dogs and observed lower stability with healing: modifications and limits of recovery of gaps in relation
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