Socket grafting with the use ofautologous bone: an experimental studyin the dog

Mauricio G. AraújoJan Lindhe

Authors’ affiliations:Mauricio G. Araújo, Department of Dentistry, StateUniversity of Maringá, Parana, BrazilMauricio G. Araújo, Jan Lindhe, Institute ofOdontology, The Sahlgrenska Academy at theUniversity of Gothenburg, Gothenburg, Sweden

Corresponding author:Mauricio G. AraújoRua Silva Jardim15/sala 0387013-010Maringá, ParanáBrazilTel.:/Fax: þ 55 44 3224 6444e-mail: odomar@hotmail.com

Key words: alveolar socket, autogenous bone, graft, ridge preservation

Abstract

Background: Studies in humans and animals have shown that following tooth removal

(loss), the alveolar ridge becomes markedly reduced. Attempts made to counteract such

ridge diminution by installing implants in the fresh extraction sockets were not successful,

while socket grafting with anorganic bovine bone mineral prevented ridge contraction.

Aim: To examine whether grafting of the alveolar socket with the use of chips of

autologous bone may allow ridge preservation following tooth extraction.

Methods: In five beagle dogs, the distal roots of the third and fourth mandibular premolars

were removed. The sockets in the right or the left jaw quadrant were grafted with either

anorganic bovine bone or with chips of autologous bone harvested from the buccal

bone plate. After 3 months of healing, biopsies of the experimental sites were sampled,

prepared for buccal–lingual ground sections and examined with respect to size and

composition.

Results: It was observed that the majority of the autologous bone chips during healing had

been resorbed and that the graft apparently did not interfere with socket healing or

processes that resulted in ridge resorption.

Conclusion: Autologous bone chips placed in the fresh extraction socket will (i) neither

stimulate nor retard new bone formation and (ii) not prevent ridge resorption that occurs

during healing following tooth extraction.

Following tooth extraction (loss), the alveo-

lar ridge undergoes a marked change (Pie-

trokovski & Massler 1967; Schropp et al.

2003; Pietrokovski et al. 2007). During the

first year after tooth extraction, about 50%

of the bucco-lingual ridge dimension will be

lost (Schropp et al. 2003). Furthermore,

ridge reduction will become more pro-

nounced from a buccal than from a lin-

gual/palatal aspect (Pietrokovski & Massler

1967). It was suggested that the ridge di-

mensions could be preserved if implants

were placed in the fresh extraction socket

(Denissen et al. 2000; Paolantonio et al.

2001). The validity of this hypothesis was

refuted by Botticelli et al. (2004) and Sanz

et al. (2010), who in prospective studies

involving large numbers of subjects and

sites, clearly documented that also follow-

ing immediate implant placement (Type 1;

Hämmerle et al. 2004), the edentulous site

underwent substantial diminution.

Processes of hard tissue modeling and

remodeling following tooth extraction were

studied in the dog model (Cardaropoli et al.

2003; Araújo & Lindhe 2005). It was de-

monstrated that the socket was first occu-

pied by a coagulum that was replaced with

granulation tissue, provisional connective

tissue and woven bone. This immature

Date:Accepted 25 January 2010

To cite this article:Araújo MG, Lindhe J. Socket grafting with the use ofautologous bone: an experimental study in the dog.Clin. Oral Impl. Res. 22, 2011; 9–13.doi: 10.1111/j.1600-0501.2010.01937.x

c� 2010 John Wiley & Sons A/S 9

mailto:odomar@hotmail.com

hard tissue was subsequently replaced with

lamellar bone and marrow. During healing,

the height of the buccal bone wall was

substantially reduced. In addition, about

30% of the marginal portion of the alveolar

process of the extraction site was modeled

and lost (Araújo et al. 2008). In later

experiments using the same model, the

post-extraction socket was grafted with

Bio-Osss

collagen (Geistlich Pharma) and

healing was monitored in biopsies sampled

after 3 months (Araújo et al. 2008) or 6

months (Araújo & Lindhe 2009) of healing.

Microscopic examinations of buccal–lin-

gual ground sections showed that place-

ment of the xenograft in the extraction

wound seemed to delay healing but also

counteract ridge contraction.

The use of autologous bone grafts from

intra- or extra oral donor sites has, for many

years, been regarded as the gold standard in

reconstructive surgery (e.g. Burchardt

1987; Goldberg & Stevenson 1987; Misch

1997; Hj�rting-Hansen 2002). However,

limited information is available regarding

the fate of autologous bone placed in alveo-

lar bone defects such as fresh extraction

sockets in humans (Becker et al. 1994,

1996). Jensen et al. (2006) studied healing

of standardized hard tissue defects that had

been prepared in the mandible of minipigs

and filled with grafts comprised of either

autologous bone chips, anorganic bovine

bone or synthetic b-tricalcium phosphate.Histological examination was performed in

biopsies sampled after 1, 2, 4 and 8 weeks

of healing. The authors reported that (i) all

defects regenerated with newly formed

bone but (ii) the bone substitutes seemed

to decelerate bone regeneration (in the early

phase) as compared with healing patterns

seen at sites augmented with the autolo-

gous bone chips.

The aim of the present experiment was

to evaluate whether grafting of the alveolar

socket with autologous bone might coun-

teract ridge resorption that occurs following

tooth extraction.

Material and methods

The research protocol was approved (State

University of Maringá, Brazil). Five beagle

dogs, about 1 year old, were used. The dogs

were anesthetized with intravenously

administered ketamine 10% (8 mg/kg,

Agener União, São Paulo, Brazil).

Sulcus incisions were made in the pos-

terior premolar region and small buccal–

lingual full-thickness flaps were elevated.

The third and fourth mandibular premolars

(3P3, 4P4) were hemi-sected. The canal of

the mesial root was reamed and filled with

gutta-percha.

In one quadrant, bone chips harvested

from the buccal surface of the mandible

using a sharp chisel were soaked in blood

and packed into the fresh sockets (auto-

graft). In the contra lateral quadrant, a

xenograft [a blend of granules of deprotei-

nized bovine bone (90%) and porcine col-

lagen fibers (10%); Bio-Osss

collagen;

Geistlichs

, Wolhusen, Switzerland] was

placed (xenograft) in a similar manner.

Three months after the grafting proce-

dure, the dogs were euthanized with an

overdose of ketamine and perfused,

through the carotid arteries, with a fixative

containing a mixture of 5% glutaraldehyde

and 4% formaldehyde (Karnovsky 1965).

The premolar sites, including the mesial

root and the distal socket area, were dis-

sected (Exacts

Apparatebeau, Norderstedt,

Hamburg, Germany). The tissue samples

were processed according to the methods

described by Donath & Breuner (1982) and

Donath (1988), dehydrated in ethanol, in-

filtrated with Technovits

7200 VLC resin

(Kulzer, Friedrichrsdorf, Germany), poly-

merized and sectioned (Exacts

Apparate-

beau). From each premolar site, four

sections were prepared, two sections from

the mesial root and two sections from the

healed socket. The sections were cut in the

buccal–lingual plane and were sampled

from the central area of either the root or

the socket. The sections were, by micro

grinding and polishing, reduced to a thick-

ness of about 25–30 mm and stained inLadewig’s fibrin stain.

Examinations

The histological examinations were per-

formed in a Leitz DM-RBEs

microscope

(Leica, Wetzlar, Germany) equipped with

an image system (Q-500 MCs

, Leica).

Size of the cross-section area of the edentulousridge

The profile of the ridge as well as the size of

the cross-section area of the edentulous

portion of the 3P3 and 4P4 sites were

determined in accordance with a method

described by Araújo et al. (2008). In brief,

the image of the profile of the alveolar

process that harbored the mesial root of

an experimental tooth site was divided into

three equally high portions. The size of

each of the apical, middle and marginal

portions was determined with a cursor

and expressed in mm2. The corresponding

measurements were then performed at the

edentulous, healed distal socket site. The

relative alteration of the size of the alveolar

process that had occurred in each dog after

tooth extraction was estimated by subtract-

ing the value obtained at the extraction site

from the corresponding value at the mesial

root site (for further details, see Araújo

et al. 2008).

Morphometric measurements

The composition of the alveolar process as

well as the newly formed tissue in the

edentulous distal socket site was deter-

mined using a point-counting procedure.

A lattice comprising 100 light points (mod-

ified from Schroeder & Münzel-Pedrazzoli

1973) was superimposed over the target

area and the percentage area occupied by

lamellar bone, newly formed bone (mainly

woven bone), BMUs (basal multicellular

units), bone marrow, provisional connec-

tive tissue and graft particles was deter-

mined (magnification �100).The mean values and standard deviations

of the different variables were calculated

using the dog as the statistical unit.

Results

In all experimental sites, healing was un-

eventful. After 3 months of healing, a

keratinized mucosa was observed to cover

the entrance of the edentulous part of all

premolar sites.

Gross histological findings

Sites with an autograft

A large portion of the central area of ex-

traction sites was occupied by bone mar-

row in which an island of newly formed,

mineralized bone could be observed (Fig. 1).

Remnants of non-vital bone chips (Fig. 2a

and b) were few in numbers, but occurred

in the entire part of the newly formed bone.

The graft particles had the nature of lamel-

lar bone and were frequently separated

Araújo & Lindhe � Socket grafting with the use of autologous bone

10 | Clin. Oral Impl. Res. 22, 2011 / 9–13 c� 2010 John Wiley & Sons A/S

from the newly formed hard tissue by

reversal lines. A varying thick layer of

mainly woven bone was present in the

entrance region of the socket site. The

old buccal bone crest was located about

2 mm apical of its lingual counterpart in all

specimens.

Sites with a xenograft

The newly formed bone and provisional

connective tissue in socket sites that had

been filled with Bio-Osss

collagen harbored

large numbers of graft particles (Fig. 3).

The marginal and middle portions of the

site were comprised of newly formed wo-

ven and parallel-fibered bone. Bone mar-

row was observed mainly in the apical

portion of the site. Bio-Osss

particles pre-

sent within the bony housing were consis-

tently surrounded by parallel-fibered bone

or were in direct contact with multinu-

cleated cells (Fig. 4a and b). A fibrous

capsule surrounded particles of the bioma-

terial that were located in the mucosa

adjacent to the bone compartment of the

ridge. The old buccal bone crest was con-

sistently located about 1–2 mm apical of

the lingual crest.

Dimensions of the ridge

In all the experimental sites, the apical and

middle portion of the edentulous alveolar

process had dimensions similar to that of

the adjacent mesial root (Table 1). While

the marginal portion of sites grafted with

Bio-Osss

collagen had a cross-section area

that was similar in size to that of the

adjacent mesial root (þ3.6� 10.7%), thecorresponding portion of the sites grafted

with the autologous bone chips was mark-

edly smaller (� 25� 16.3%).

Composition of the alveolar process andthe healed socket

Alveolar process (Table 2)

The alveolar process that harbored the

autologous bone graft was comprised of

49.1� 6.6% old lamellar bone, 24.5� 3% newly formed bone, 20.7� 8.1%bone marrow, 4.4� 1.2% BMUs and1.4� 1.6% graft material.

The corresponding values obtained from

measurements in the Bio-Osss

grafted

sites were 54� 7.5% old lamellarbone, 18.1� 7% newly formed bone,10.5� 5.5% bone marrow, 4.1� 2.7%BMUs and 8.6� 2% graft material. Inaddition, sites grafted with the biomaterial

included 4.7� 2.5% provisional connec-tive tissue.

Healed socket sites (Table 3)

The newly formed tissue and the remaining

graft material that occupied the post-extrac-

tion socket augmented with autologous bone

chips was comprised of 57.2� 8.6% miner-alized bone, 38.3� 10.9% bone marrow,2.9� 2.8% BMUs and 1.9� 1.9% non-vital bone chips.

The corresponding values for the Bio-Osss

collagen sites were 43.1� 10% for miner-alized bone, 16� 7.6% for bone marrow,2� 2.2% for BMUs, 4.7� 2.5% for provi-sional connective tissue and 24.4� 3.7%for Bio-Oss

s

particles.

Discussion

Sockets grafted with autologous bone ex-

hibited a healing pattern that had many

features in common with those described

Fig. 1. Microphotograph of a buccal–lingual section

representing an experimental site after 3 months of

healing. The fresh extraction socket was grafted

with autologous bone chips. The lingual bone wall

is wider than the buccal wall. Note the area of

mineralized bone residing in the bone marrow. The

socket entrance is occupied by a bridge of miner-

alized hard tissue. B, buccal bone wall; L, lingual

bone wall; BM, bone marrow. Ladewig fibrin stain;

original magnification �16.

Fig. 2. Higher magnification of newly formed bone. Note the presence of non-vital autologous bone chips

(asterisk) that are delineated by a dark-stained reversal line (a). The same detail presented in polarized light (b).

The autologous bone chips are made of lamellar bone and are in direct contact with woven and parallel-fibered

bone (b). Ladewig fibrin stain; original magnification �100.

Fig. 3. Microphotograph of a buccal–lingual section

representing an experimental site after 3 months of

healing. The fresh extraction socket was grafted

with Bio-Osss

collagen. The xenograft particles

(blue stain) are embedded in newly formed bone

and some provisional connective tissue. Note that

the biomaterial occupies a large portion of the socket

entrance. Bio-Osss

particles can also be seen in the

mucosa of the ridge. B, buccal bone wall; L, lingual

bone wall; BM, bone marrow. Ladewig fibrin stain;

original magnification �16.

Araújo & Lindhe � Socket grafting with the use of autologous bone

c� 2010 John Wiley & Sons A/S 11 | Clin. Oral Impl. Res. 22, 2011 / 9–13

for non-grafted post-extraction sites (Car-

daropoli et al. 2003; Araújo & Lindhe

2005; Araújo et al. 2008) Thus, in the

current study as well as in the previous

experiments, the sockets – after 3 months

of healing – had become filled with similar

amounts of mineralized bone (mainly wo-

ven bone) and marrow. This indicates that

the autograft material used in the present

study apparently failed to enhance healing

and/or to stimulate hard tissue formation

in the socket.

The mineralized bone in the grafted sites

harbored chips of non-vital autologous

bone. The chips (particles) were never ob-

served in the bone marrow but only within

the newly formed bone from which they

were consistently separated by well-

defined, often undulating reversal lines.

This suggests that the autologous bone

graft during the early, inflammatory phase

of healing had been exposed to osteoclastic

activity and that, as a consequence, after 3

months, comparatively few graft particles

remained in the socket site.

In the present study, it was furthermore

noted that in sites grafted with autologous

bone, there was pronounced resorption of

the buccal bone wall and also a marked

reduction (�25%) of the marginal portionof the ridge. Similar amounts of buccal wall

reduction (about 2 mm) and ridge diminu-

tion (�30%) were reported for non-graftedsites by Araújo & Lindhe (2005), Araújo

et al. (2008).

In other words, despite the fact that the

autogenous bone used in the current ex-

periment may have delivered an osteogenic

as well as an osteoconductive stimulus

(Burchardt 1987) to the fresh extraction

socket and although the gold standard for

bone grafting may include the use of auto-

genous hard tissue from, e.g., intra-oral

donor sites (for a review, see Hj�rting-

Hansen 2002), in the current model, this

type of graft material failed to prevent ridge

contraction.

In comparison with sockets that had

been filled with autologous bone, the Bio-

Osss

collagen-grafted sites exhibited a de-

layed healing pattern (Table 3). Thus, in

xenograft-treated sites, there was less

mineralized bone (43.5 vs. 57.2%), a smal-

ler proportion of bone marrow (16 vs.

38.3%) and a substantial amount of re-

maining provisional connective tissue (14

vs. 0%). This conclusion of a delayed

healing in Bio-Osss

-grafted sites is in

agreement with observations made pre-

viously (Artzi et al. 2004; Jensen et al.

2006) and from experiments using the ex-

traction socket model (Araújo et al. 2008,

2010; Araújo & Lindhe 2009). In a recent

experiment, Araújo et al. (2010) studied

the dynamics of Bio-Osss

incorporation in

extraction wounds and concluded that be-

fore new bone could form in the augmented

site, the biomaterial had to be exposed to a

‘‘surface cleaning’’ that was associated

with the presence of TRAP-positive multi-

nucleated cells, i.e. osteoclasts. This is in

agreement with the proposal by Jensen

et al. (2006) i.e. that the multinucleated

cells present adjacent to particles of Bio-

Osss

in a healing hard tissue wound ‘‘had

more the function of macrophages, i.e. to

clean the graft surface and thereby prepare

Fig. 4. Higher magnification of newly formed bone surrounding Bio-Osss

particles. The newly formed bone is

laid down in the provisional connective tissue and on the surface of the xenograft (a). The same detail presented

in polarized light (b). The hard tissue present on the surface of the biomaterial is comprised of woven bone and

parallel-fibered bone (b). Ladewig fibrin stain; original magnification �100.

Table 1. Mean relative alteration (% change in comparison with the tooth site� SD) of thesurface area (mm2) of the apical middle and apical third of the edentulous alveolar ridge

Area Autologous bone (%) Bio-Osss

collagen (%)

Coronal � 25 � 16.3 þ 3.6 � 10.7Middle þ 3.1 � 8 þ 6.4 � 5.4Apical þ 2.3 � 3.7 þ 6.1 � 4.4

þ , a relative increase of the cross-section area; � , a relative decrease of the cross-section area.

Table 2. Volumetric data describing the overall composition (%� SD) of the alveolarprocess in the grafted and non-grafted extraction sites

Autologous bone (%) Bio-Osss

collagen (%)

Lamellar bone 49.1 � 6.6 54 � 7.5Woven bone 24.5 � 3 18.1 � 7Bone marrow 20.7 � 8.1 10.5 � 5.5BMUs 4.4 � 1.2 4.1 � 2.7Connective tissue 0 � 0 4.7 � 2.5Graft particles 1.4 � 1.6 8.6 � 2

BMU, bone multicellular units.

Table 3. Volumetric data describing the composition (%� SD) of the newly formed tissuein the healed extraction sockets

Autologous bone (%) Bio-Osss

collagen (%)

Mineralized bone 57.2 � 8.6 43.1 � 10Bone marrow 38.3 � 10.9 16 � 7.6BMUs 2.9 � 2.8 2 � 2.2Connective tissue 0 � 0 4.7 � 2.5Graft particles 1.9 � 1.9 24.6 � 3.7

BMU, bone multicellular units.

Araújo & Lindhe � Socket grafting with the use of autologous bone

12 | Clin. Oral Impl. Res. 22, 2011 / 9–13 c� 2010 John Wiley & Sons A/S

it for deposition of newly formed bone.’’ In

the studies by e.g. Jensen et al. (2006) and

Araújo et al. (2010), the biomaterial was

apparently not engaged in the processes of

modeling/remodeling. Thus, a large num-

ber of Bio-Osss

particles remained in the

newly formed tissue (Jensen et al. 1996,

2005, 2006; Piattelli et al. 1999; Artzi et al.

2004).

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