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Araújo Effect of a xenograft on early bone

E. Linder
J. Lindhe
formation in extraction sockets:
an experimental study in dog

Authors’ affiliations: Key words: biomaterial, bone formation, extraction socket, grafting
Mauricio Araújo, Department of Dentistry,
State University of Maringá, Paraná, Brazil
Elena Linder, Jan Lindhe, Institute of Odontology, Abstract
The Sahlgrenska Academy at Göteborg University, Aim: The aim of this study was to study the effect on early bone formation resulting from
Gothenburg, Sweden
the placement of a xenograft in the fresh extraction socket in dogs.
Correspondence to: Material and methods: Five beagle dogs were used. The distal roots of the third and fourth
M. Araújo mandibular premolars were removed. In one quadrant, a graft consisting of Bio-Oss

Rua Silva Jardim

15/sala 03 Collagen was placed in the fresh extraction wound, while the corresponding premolar sites
87013-010 Maringá in the contra-lateral jaw quadrant were left non-grafted. After 2 weeks of healing, the dogs
Brazil were perfused with a fixative, the mandibles removed, the experimental sites dissected,
Tel.: þ 55 44 3224 6444 demineralized, sectioned in the mesio-distal plane and stained in hematoxyline–eosine.
Fax: þ 55 44 3224 6444
Results: The central portion of the non-grafted sockets was occupied by a provisional
matrix comprised of densely packed connective tissue fibers and mesenchymal cells. Apical
and lateral to the provisional matrix, newly formed woven bone was found to occupy most
of the sockets. In the apical part of the grafted sockets, no particles of the xenograft could
be observed but newly formed bone was present in this portion of the experimental site.
In addition, limited numbers of woven bone trabeculae occurred along the lateral socket
walls. The central and marginal segments of the grafted sockets, however, were occupied
by a non-mineralized connective tissue that enclosed Bio-Oss particles that frequently
were coated by multinucleated cells.
Conclusions: The placement of Bio-Oss Collagen in the fresh extraction wound obviously
delayed socket healing. Thus, after 2 weeks of tissue repair, only minute amounts of newly
formed bone occurred in the apical and lateral borders of the grafted sockets, while large
amounts of woven bone had formed in most parts of the non-grafted sites.

In previous experiments in dogs (Cardaro- were reported from retrospective and pro-
poli et al. 2003; Araújo & Lindhe 2005), it spective studies in man (Pietrokovski &
was observed that healing of an extraction Massler 1967; Schropp et al. 2003; Pietro-
socket included (i) early formation of wo- kovski et al. 2007; for review see Chen
ven bone (modeling) and (ii) the subse- et al. 2004).
quent replacement of this immature bone Different approaches were used to pre-
Date: with lamellar bone and marrow (remodel- vent the post-extraction ridge reductions.
Accepted 5 April 2008
ing). Healing of the edentulous site was Such methods included the utilization of
To cite this article: further characterized by (iii) loss of bundle various graft materials and application
Araújo M, Linder E, Lindhe J. Effect of a xenograft
on early bone formation in extraction sockets: bone in the walls of the socket and (iv) a techniques (e.g. Becker et al. 1998; Artzi
an experimental study in dog. marked reduction in the height of the et al. 2000; Froum et al. 2002; Carmagnola
Clin. Oral Impl. Res. 20, 2009; 1–6.
doi: 10.1111/j.1600-0501.2008.01606.x buccal bone crest. Similar observations et al. 2003; Nevins et al. 2006).

c 2009 The Authors. Journal compilation 

 c 2009 Blackwell Munksgaard 1
Araújo et al . Early bone formation in extraction sockets

In a recent study by Araújo et al. (2008), Grafted sites blocks were dehydrated in ethanol and
In one quadrant of the mandible, a graft
the dog model was used to study healing of s
isopropanol and embedded in paraffin. Se-
consisting of Bio-Oss Collagen (Geis-
an extraction socket that had been grafted s
rial sections representing the experimental
s tlich , Wolhusen, Switzerland) was placed
with Bio-Oss Collagen. It was observed sites were cut in a mesio-distal plane and
in the fresh extraction wounds (Fig. 1) in a
that the placement of the xenograft in the parallel to its long axis. The microtome
manner previously described (Araújo et al.
fresh extraction socket after a 3-month was set at 6 mm. From each site, three
2008). The marginal portion (about 2 mm)
period of healing appeared to have inter- sections, representing the central part of
of the buccal bone wall of the distal sockets
fered with the process of bone modeling the socket and about 20 mm apart, were
was also covered with the biomaterial.
and remodeling. Thus, while the non- selected for the histological examination.
grafted sites underwent marked resorption The sections were stained in hematoxy-
during the 3-month interval, the dimen- line–eosine
Non-grafted sites
sion of the walls of the grafted sockets as The corresponding premolar sites in the
well as the profile of the edentulous ridge contra-lateral jaw quadrant were exposed Histological examination
remained unchanged. The newly formed and managed in the manner described The histological examinations were per-
hard tissue in the marginal portion of the above. No biomaterial was, however,
formed in a Leitz DM-RBE microscope
grafted sites, however, contained a large placed in the fresh extraction sockets. (Leica, Wetzlar, Germany) equipped with
number of Bio-Oss particles that were The flaps were replaced in the grafted
an image system (Q-500 MC ; Leica).
surrounded by immature woven bone. A and non-grafted sites and were retained The composition of the newly formed
more detailed analysis of the newly formed with interrupted sutures. The sutures tissue in the extraction socket was deter-
tissues in the two differently treated sock- were removed after 1 week. Mechanical mined using a point counting procedure.
ets further indicated that the process of tooth cleaning was performed on days 3, 7 Thus, a lattice comprising 100 light points
tissue remodeling had progressed further and 10 after surgery. (modified from Schroeder & Münzel-
in the non-grafted than in the grafted sites. After 2 weeks of healing, the dogs were Pedrazzoli 1973) was superimposed over
Thus, while about 50% of the tissue vo- euthanized with an overdose of Ketamin the tissue in the healing socket, and the
lume in the non-grafted sites was occupied (Agener União) and perfused, through the percentage area occupied by (i) mineralized
by bone marrow, in the grafted site bone carotid arteries, with a fixative containing bone, (ii) bone marrow, (iii) provisional
marrow represented only about 25% of the a mixture of 5% glutaraldehyde and 4% matrix, (iv) granulation tissue and (v) Bio-
tissue volume. This indicates that the graft formaldehyde (Karnovsky 1965). The
Oss particles was determined (magnifica-
may in fact have delayed healing. mandibles were removed and placed in tion  200). In addition, the number of
The objective of the present experiment the fixative. Each experimental site, in-
Bio-Oss particles in the socket that were
was to evaluate the effect on early wound cluding the distal socket area, was dis- in direct contact with multinucleated cells
healing and bone modeling of the place- sected using a diamond saw (Exact
was determined and expressed as percen-
ment of a xenograft in the fresh extraction Apparatebeau, Norderstedt, Hamburg,
tage of the total number of Bio-Oss parti-
socket in dogs. Germany), and subsequently deminera- cles identified.
lized in a 10% solution of EDTA. The Mean values and standard deviations of
the different variables were calculated
Material and methods using the dog as the statistical unit.

The ethical committee of the State Uni-

versity of Maringá approved the research Results
protocol. Five beagle dogs about 1 year old
and weighing between 10 and 12 kg each Healing was uneventful at all sites. The
were used. During surgical procedures, the clinical examination of the experimental
animals were anesthetized with intrave- sites that was performed after 2 weeks (Fig.
nously administered Ketamin (10%, 2) disclosed that a slightly invaginated and
8 mg/kg; Agener União, São Paulo, Brazil). modestly inflamed soft tissue covered the
Pocket and crestal incisions were made socket entrance.
in the posterior premolar region in both
quadrants of the mandible. Buccal and Gross histological observations
lingual full thickness flaps were elevated The connective tissue of the mucosa cover-
to disclose the alveolar crest. The canal of ing the grafted as well as the non-grafted
the mesial roots of the third and fourth sockets was rich in mesenchymal cells,
mandibular premolars was reamed and vascular structures and clusters of inflam-
filled with gutta-percha. The premolars matory cells.
Fig. 1. Clinical photographs illustrating the graft of
were subsequently hemi-sected with the s
Bio-Oss Collagen placed in the fresh extraction
The central portion of the non-grafted
use of fissure burs. The distal roots were socket. Note that the graft material also covers the sockets (control site; Fig. 3) was occupied
carefully removed with the use of elevators. marginal portion of the buccal wall of the socket. by a provisional matrix comprised of

2 | Clin. Oral Impl. Res. 20, 2009 / 1–6 c 2009 The Authors. Journal compilation 
 c 2009 Blackwell Munksgaard
Araújo et al . Early bone formation in extraction sockets

Fig. 4. Microphotograph representing the provi- Fig. 6. Microphotograph representing the woven
sional matrix in the non-grafted site. Note the bone in the non-grafted site. The trabeculae of
densely packed connective tissue fibers and cells; woven bone were lined with osteoblasts and occa-
V, vessel. Hematoxyline–eosine stain; original mag- sional isolated osteoclasts (arrows). BM, primitive
nification: 200. bone marrow; V, vessel; WB, woven bone. Hema-
Fig. 2. Clinical photographs illustrating a site toxyline–eosine stain; original magnification:
grafted with Bio-Oss Collagen after 2 weeks of 200.
healing. Note the slightly invaginated crestal surface
and the slightly inflamed soft tissue.

Fig. 5. Microphotograph representing the minerali-

zation front of the woven bone in the non-grafted
site. Note that the woven projections had initiated
the formation of a primary spongiosa (primary
osteons and enclosed vascular structures). PM, pro-
visional matrix; V, vessel; WB, woven bone. Hema-
toxyline–eosine stain; original magnification:

and enclosed vascular structures (Fig. 5). Fig. 7. Microphotograph of a mesio-distal section
The trabeculae of immature bone were representing a grafted site. Note that the central
and marginal segments of the sockets were occupied
lined with osteoblasts and occasionally s
by a connective tissue that enclosed Bio-Oss parti-
isolated osteoclasts, residing in resorption cles (asterisks). PM, provisional matrix; WB, woven
Fig. 3. Microphotograph of a mesio-distal section bays, could be observed on the surface of bone. Hematoxyline–eosine stain; original magnifi-
representing a non-grafted site. Note that most of the newly formed bone (Fig. 6). cation: 16.
the alveolar socket is occupied by woven bone and No particles of the xenograft could be
provisional matrix. PM, provisional matrix; GT, observed in the apical part of the grafted tissue had the features of a provisional
granulation tissue; WB, woven bone. Hematoxyline–
sockets (test site; Fig. 7), but newly formed matrix (rich in mesenchymal cells, fibers
eosine stain; original magnification: 16.
immature bone was found to occupy this and vessels) but small amounts of mono-
portion of the post-extraction wound. In nuclear leukocytes could consistently also
densely packed connective tissue fibers and addition, limited numbers of trabeculae of be observed. In addition, the provisional
mesenchymal cells (Fig. 4). Apical and woven bone occurred along the lateral matrix harbored a multitude of large multi-
lateral to the provisional matrix, newly walls of the sockets. The central and mar- nucleated cells that were in direct contact
formed woven bone was found to occupy ginal segments of the wound were occupied with and occupied substantial portions of
most of the socket (Fig. 3). Several of the by a connective tissue that enclosed the the periphery of many of the graft particles
bone projections formed primary osteons Bio-Oss particles (Fig. 7). This connective (Figs 8 and 9). Segments of the graft that

c 2009 The Authors. Journal compilation 

 c 2009 Blackwell Munksgaard 3 | Clin. Oral Impl. Res. 20, 2009 / 1–6
Araújo et al . Early bone formation in extraction sockets

Fig. 8. Microphotograph representing the provi-

Fig. 12. Microphotograph representing a higher
sional matrix in the grafted site. The provisional
Fig. 10. Microphotograph representing the provi- magnification of a multinucleated cell present in a
matrix harbored large multinucleated cells (arrows)
sional matrix in a grafted site. Note that the Bio- shallow invagination on the surface of a Bio-Oss

that were in direct contact with and occupied differ- s

Oss particle was not only in direct contact with particle in the provisional matrix of a grafted site.
ent portions of the periphery of many of the graft
s multinucleated cells (arrows) but also with provi- s
Bp, Bio-Oss particle. Hematoxyline–eosine stain;
particles. Bp, Bio-Oss particles; PM, provisional
sional matrix or newly formed woven bone (arrow- original magnification:  1000.
matrix. Hematoxyline–eosine stain; original magni- s
heads). a, artifact; Bp, Bio-Oss particles; PM,
fication: 200.
provisional matrix; WB, woven bone. Hematoxy-
line–eosine stain; original magnification: 400.
Table 1. Mean values (SD) of the propor-
tions (%) of the different tissues in the
grafted and non-grafted alveolar sockets
Grafted Non-grafted
site site
Granulation 3.7 (0.8) 3.1 (0.5)
Provisional 62.7 (12.6) 49.1 (8.2)
Mineralized 14.7 (5.9) 47.8 (15.6)
Bio-Oss 18.9 (9.8) –

Fig. 9. Microphotograph representing a higher mag-
The present experiment indicated that the
nification of multinucleated cells (arrows) that Fig. 11. Microphotograph representing the lateral
coated the entire periphery of a Bio-Oss particle
early phase of hard tissue formation was
portions of the socket in a grafted site. Note few
in a grafted site. Bp, Bio-Oss particle. Hematoxy- s retarded in extraction sockets that, imme-
multinucleated cells at the surface of the Bio-Oss
line–eosine stain; original magnification: 1000. s
particles and that several adjacent Bio-Oss particles diately after tooth removal, had been
were bridged by newly formed woven bone. Bp, Bio- grafted with Bio-Oss Collagen. It appeared
Oss particles; V, vessel; WB, woven bone. Hema- that this delayed wound healing and bone
toxyline–eosine stain; original magnification:
were not occupied by the multinucleated modeling may have been influenced by the
cells were found to be in direct contact multinucleated cells that occurred in tis-
with provisional matrix or newly formed sues harboring the xenograft. Thus, in the
mineralized bone (Fig. 10). In the lateral grafted sites, substantial amounts of newly
portions of the socket, several adjacent Bio- granulation tissue was 3.7  0.8% (SD) formed bone could only be detected in the
Oss particles were frequently found to be in the grafted and 3.1  0.5% in non- apical portion of the socket where the graft
‘connected’ (bridged) by zones of immature grafted sites. The proportions of provi- material was absent. In the remaining
bone (Fig. 11). There were no obvious signs sional matrix were 62.7  12.6% (grafted portions of the grafted sockets, a mildly
of active degradation of the bovine mineral sites) and 49.1  8.2% (non-grafted sites), inflamed provisional matrix surrounded
and only at a few sites could multinu- and the corresponding proportions of the majority of the Bio-Oss particles, the
cleated cells be observed in shallow invagi- mineralized bone were 14.7  5.9% and surface of which was frequently, but not
nations on the surface of the graft (Fig. 12). 47.8  15.6%. The Bio-Oss particles oc- always, coated with multinucleated cells.
cupied 18.9  9.8% of the tissue present In isolated areas of the grafted sites, multi-
Morphometric measurements in the grafted sockets. The percentage of nucleated cells were absent and the foreign
The percentage area occupied by the var- Bio-Oss particles that were in direct con- material occasionally surrounded by the
ious tissues in the alveolar socket is pre- tact with multinucleated cells was woven bone that bridged adjacent granules
sented in Table 1. The proportion of 53  12.2%. of the bovine bone.

4 | Clin. Oral Impl. Res. 20, 2009 / 1–6 c 2009 The Authors. Journal compilation 
 c 2009 Blackwell Munksgaard
Araújo et al . Early bone formation in extraction sockets

In the non-grafted control sites, large et al. 2007), and the cells were identified
amounts of woven bone had formed in as osteoclasts and their presence related to
most compartments of the socket. This the resorption and gradual elimination of
finding is in agreement with observations the graft material (Berglundh & Lindhe
from similar experiments that investigated 1997; Araújo et al. 2001; Cardaropoli
tissue modeling and remodeling in extrac- et al. 2005). It has not been made clear,
tion sockets as well as in mechanically however, whether the multinucleated cells
produced defects in the alveolar ridge in found on the surface of this xenograft are
dogs (Cardaropoli et al. 2003, 2005; Araújo indeed active osteoclasts as suggested by,
& Lindhe 2005). e.g., Piatelli et al. (1999), Tadjoedin et al.
Similar amounts of new bone had formed (2003), Tapety et al. (2004) or non-active,
in the apical segments of the test and impaired osteoclasts cells as suggested by
control sites, while in the remaining por- Taylor et al. (2002). It is documented that
tions of the grafted sockets, only minute multinucleated cells originate from mono-
Fig. 13. Microphotograph representing a higher
amounts of immature bone could be found. nuclear phagocytes that belong to the he-
magnification of multinicleated cells (arrows) on
There are reasons to assume that following matopoietic line of stem cells (Bredan & the graft surface in the provisional matrix of a grafted
root extraction and graft placement, the Xing 2007). Such mononuclear phagocytes site. Note the multinucleated cells were present on a
ensuing flow of blood into the cone-shaped (macrophages) may fuse and differentiate smooth non-invaginated surface. Bp, Bio-Oss par-
socket forced the Bio-Oss Collagen mate- into osteoclasts or giant cells as reported by ticle. Hematoxyline–eosine stain; original magnifi-
cation: 1000.
rial in marginal direction. A void was Vignery (2000) who claimed that while
hereby established in the apical zone of osteoclasts develop on bone surfaces, other
the socket that could house a coagulum multinucleated cells such as giant cells
that apparently was unaffected by the differentiate ‘primarily in chronic inflam- is associated with inflammatory processes
translocated foreign material. Hence, in matory sites in response to bacterial inva- (Vignery 2000; Ratner 2001; Luttikhuizen
this apical portion of the test socket as sion and foreign bodies such as implants et al. 2006) that may impair hard tissue
well as in the entire non-grafted socket, . . ..’ In the tissue sampled from the grafted deposition. This may explain the delayed
tissue modeling evidently followed a nor- sites of the current experiment, the multi- formation of bone that was observed in the
mal patter, i.e. the clot was replaced with nucleated cells on the graft surface were graft-containing areas of the extraction
granulation tissue, provisional matrix and almost never found to reside in resorption socket, and that the multinucleated cells
primary spongiosa (Cardaropoli et al. bays (Fig. 13), while morphologically simi- found on the surface of the xenograft were
2003). lar cells present on adjacent surfaces of host giant cells.
In the non-mineralized portions of the bone were almost consistently located in Most of the graft particles present in the
newly formed tissue in the grafted sockets, characteristic Howship’s lacunae and were test sites were surrounded either by a dense
large multinucleated cells were found to classified as active osteoclasts. provisional matrix or newly formed woven
surround a substantial number of the Bio- It has been documented that a foreign bone. In such locations, multinucleated
Oss granules. Thus, 450% of the gran- body reaction can be elicited to a xenograft cells were conspicuous by their absence.
ules were more or less completely coated that is clinically non-immunogenic, non- In a previous experiment in the dog (Araújo
by multinucleated cells. In the remaining toxic and chemically inert (for review see et al. 2008), socket grafting was performed
portions of the graft, the Bio-Oss particles Luttikhuizen et al. 2006). Furthermore, it and healing evaluated 3 months after tooth
were surrounded either by a leukocyte- was proposed (Ratner 2001) that such a extraction. In sections from this longer
containing provisional matrix or occasion- reaction may occur during early phases of term study, multinucleated cells were
ally newly formed woven bone. In such wound healing. The presence of multinu- never observed at the surface of the xeno-
locations, multinucleated cells were con- cleated cells in the granulation tissue- graft, but most of the Bio-Oss granules
spicuous by their absence. provisional matrix in the grafted sockets were in direct contact with immature wo-
The occurrence of multinucleated cells of the present experiment indicated that ven bone. Hence, in the interval between 2
on the surface of Bio-Oss material was the xenograft particles may have been re- weeks and 3 months of healing, the multi-
previously described (e.g. Piatelli et al. cognized as being foreign to the host, and nuclear cells may have completed their
1999; Merkx et al. 2000; Tadjoedin et al. that a foreign body reaction may have been function, undergone apoptosis and disap-
2003; Houshmand et al. 2007; Simion elicited. The early phase of such a reaction peared.


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6 | Clin. Oral Impl. Res. 20, 2009 / 1–6 c 2009 The Authors. Journal compilation 
 c 2009 Blackwell Munksgaard