Ridge Alterations Following Tooth Extraction With and Without Flap Elevation. An Experimental Study in The Dog.

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Mauricio G.

Araújo Ridge alterations following tooth


Jan Lindhe
extraction with and without flap
elevation: an experimental study
in the dog

Authors’ affiliations: Key words: bone resorption, extraction, flapless surgery


Mauricio G. Araújo, Department of Dentistry,
State University of Maringá, Parana, Brazil
Jan Lindhe, Institute of Odontology, The Abstract
Sahlgrenska Academy at the University of Background: Different approaches were advocated to preserve or improve the dimension
Gothenburg, Gothenburg, Sweden
and contour of the ridge following tooth extraction. In some of studies, socket ‘flapless
Correspondence to: extraction’ apparently had a successful outcome.
M. G. Araújo Aim: The objective of the present experiment was to compare hard tissue healing
Department of Dentistry
State University of Maringá following tooth extraction with or without the prior elevation of mucosal full-thickness
Rua Silva Jardim, 15/sala 03 flaps.
87013-010
Maringá-Paraná-Brazil Material and methods: Five mongrel dogs were used. The two second mandibular
Tel.: þ 55 44 3224 6949 premolars (2P2) were hemi-sected. The mesial roots were retained. By random selection the
Fax: þ 55 44 3224 6444
distal root in one side was removed after the elevation of full-thickness flaps while on the
e-mail: odomar@hotmail.com
contralateral side, root extraction was performed in a flapless procedure. The soft tissue
wound was closed with interrupted sutures. After 6 months of healing, the dogs were
euthanized and biopsies were sampled. From each experimental site, four ground sections –
two from the mesial root and two from the healed socket – were prepared, stained and
examined in the microscope.
Results: The data showed that the removal of a single tooth (root) during healing caused a
marked change in the edentulous ridge. In the apical and middle portions of the socket site
minor dimensional alterations occurred while in the coronal portion of the ridge the
reduction of the hard tissue volume was substantial. Similar amounts of hard tissue loss
occurred during healing irrespective of the procedure used to remove the tooth was, i.e.
flapless or following flap elevation.
Conclusion: Tooth loss (extraction) resulted in marked alterations of the ridge. The size of
the alveolar process was reduced. The procedure used for tooth extraction – flapless or
following flap elevation – apparently did not influence the more long-term outcome of
healing.

Following tooth extraction the alveolar In a recent experiment in the dog, Fickl
process will undergo a change (e.g. Pietro- et al. (2008) showed that tooth extraction
kovski & Massler 1967; Schropp et al. after the elevation of mucosal flaps (to
Date: 2003; Araújo & Lindhe 2005). Thus, the disclose the marginal bone) during a 3-
Accepted 7 December 2008
bundle bone will disappear (Cardaropoli month period of healing caused more
To cite this article: et al. 2003) and the height of the buccal (about 14%) soft and hard tissue reduction
Araújo MG, Lindhe J. Ridge alterations following tooth
extraction with and without flap elevation. An wall of the socket will reduce (Schropp than a ‘flapless’ tooth removal. Similar
experimental study in the dog. et al. 2003; Araújo & Lindhe 2005; Araújo findings were reported by Blanco et al.
Clin. Oral Impl. Res. 20, 2009; 545–549.
doi: 10.1111/j.1600-0501.2008.01703.x et al. 2008). (2008) from a study in beagle dogs. The

c 2009 The Authors. Journal compilation 


 c 2009 John Wiley & Sons A/S 545
Araújo & Lindhe . Flapless tooth extraction

ness of about 20–30 mm by microgrinding


and polishing and stained in toluidine blue
or Ladewig’s fibrin stain (Donath 1993).
The histological examination was per-
s
formed in a Leitz DM-RBE microscope
(Leica, Wetzlar, Germany) equipped with
s
an image system (Q-500 MC , Leica).
Each histological section was examined
using a methodology previously described
in detail by Araújo et al. (2008). Briefly, the
outline of the alveolar process obtained at
the tooth site was projected over the sec-
tion using the apex of the mesial root as the
reference level. Three equally high por-
tions, apical, middle and coronal, were
Fig. 1. Clinical photograph illustrating the distal socket of a second mandibular premolar following flapless (a) outlined. The area occupied by each of
and flap elevation (b) tooth extraction. Note that in the flap elevation procedure (b) the flap was elevated so that these three portions of the alveolar process
at least 3 mm of the coronal portions of the buccal and lingual surfaces of the alveolar process were exposed. was measured with a cursor and expressed
in mm2. The relative alteration of the size
of the three portions of the alveolar process
authors stated that ‘flapless immediate flap elevations were made in the contra- that had occurred in each dog after tooth
implant surgery’ produced somewhat less lateral side (flapless group). extraction and healing was estimated by
buccal bone plate resorption than when The distal roots were carefully removed subtracting the value obtained at the ex-
mucosal flaps were elevated in conjunction with the use of elevators and the extraction traction site from the corresponding value
with tooth extraction and implant installa- wound in both sides was closed with inter- at the adjacent tooth site.
tion. rupted sutures (Fig. 1a and b). The sutures Furthermore, at the buccal and lingual
The objective of the present experiment were removed after 10 days. aspects of the tooth sites the distances
was to assess alveolar ridge alterations that The animals were placed in a plaque between the cementum–enamel junction
had occurred 6 months after tooth extrac- control regimen that called for tooth clean- (CEJ) and the apical cells of the junctional
tion with or without flap elevation. ing once every second day. epithelium (aJE) and the bone crest (BC)
After 6 months of healing, the dogs were were measured.
euthanized with an overdose of Ketamin The mean values and standard deviations
Material and methods and perfused with a fixative containing a were calculated using the dog as the statis-
mixture of 5% glutaraldehyde and 4% tical unit. Differences between groups were
The ethical committee of the State Uni- formaldehyde (Karnovsky 1965). The evaluated using Student’s t-test.
versity of Maringá approved the research mandibles were removed and placed in
protocol. Five beagle dogs about 1-year-old the fixative. Each experimental site, in-
and weighing between 12 and 14 kg each cluding the mesial root and the distal Results
were used. During the surgical procedures, socket area, was dissected using a diamond
s
the animals were anesthetized with intra- saw (Exact Apparatebeau, Norderstedt, All experimental sites healed uneventfully.
venously administered Ketamin (10%, Hamburg, Germany). The tissues were After 6 months, the mucosa covering the
8 mg/kg, Agener União, São Paulo, Brazil). processed for ground sectioning according edentulous ridge and the gingival tissues at
The second premolars on both sides of to the methods described by Donath & adjacent teeth appeared to be clinically
the mandible were hemi-sected with the Breuner (1982) and Donath (1988). The healthy.
use of fissure burs. The canal of each samples were dehydrated in increasing
mesial root was reamed and filled with grades of ethanol and infiltrated with Tech-
s Histological observations
gutta-percha. novit 7200 VLC-resin (Kulzer, Frie-
Pocket incisions were made along the drichrsdorf, Germany), polymerized and Tooth sites
distal root of the second premolar in one sectioned using a cutting–grinding unit In the second premolar region, the base of
s
randomly selected side of the mandible (Exact Apparatebeau). the mandible occupied more than 50% of
(flap group) and buccal/lingual full-thick- From each experimental site, four sec- the entire cross-section area (Fig. 2). The
ness flaps were elevated. Flap elevation tions – two from the mesial root and two medial mental foramen was located in the
was extended to a level beyond the muco- from the healed socket – were prepared. buccal bone wall and often close to the apex
gingival line and disclosed the alveolar crest The sections were cut in the buccal-lingual of the mesial root. The lingual bone wall of
and the marginal 3–4 mm of the buccal and plane and were sampled from the central the alveolar process was markedly wider
lingual bone walls. The bone tissue was area of either the root (tooth) or the socket than the corresponding buccal wall.
exposed for about 15 min. No incisions or site. The sections were reduced to a thick- Furthermore, the crest of the buccal bone

546 | Clin. Oral Impl. Res. 20, 2009 / 545–549 c 2009 The Authors. Journal compilation 
 c 2009 John Wiley & Sons A/S
Araújo & Lindhe . Flapless tooth extraction

wall was consistently located apical of the the flap group, there was some loss of lingual crests. The newly formed bone of
lingual crest. connective tissue attachment. At the lin- the bridge in the socket entrance included
The gingival margin in the flapless as gual aspect, there was no sign of attach- both woven and lamellar bone. The middle
well as in the flap group was consistently ment loss in any of the groups. and apical portions of the alveolar process
located coronal to the CEJ. The gingival At the buccal aspect of the teeth in the were occupied by bone marrow and small
connective tissue was virtually free from flap group, the distance between CEJ and the amounts of lamellar bone.
infiltrates of inflammatory cells. BC was 1  0.1 mm while the correspond- The comparison of the buccal-lingual
At the buccal surface of the mesial root ing value for the flapless group was signifi- cross-section area of the tooth and the
in the flapless group, aJE were located at cantly smaller (0.7  0.2 mm; Po0.05). extraction sites revealed that the removal
the CEJ (Fig. 3). The most coronal portion of the tooth after 6 months had caused a
of the buccal bone wall was comprised of slight reduction in the overall dimension of
Extraction sites
mainly bundle bone. In the flap group, aJE the ridge (Table 2). Thus, in the flap group
The overall histological features of the
was located apical of CEJ and the most the edentulous ridge was on average
edentulous sites were similar in the flap-
coronal portion of the BC exhibited signs of 14  6% smaller than the alveolar process
less and the flap groups (Figs 5 and 6).
resorption (Fig. 4). of the corresponding tooth site. The
Thus, in all specimens, a thick, well-ker-
In the flap group, aJE (Table 1) were equivalent reduction in the flapless group
atinized mucosa covered the healed socket.
located on the average 0.2  0.1 mm (buc- was 17  16%. This difference was not
The connective tissue was devoid of in-
cal) and 0  0 mm (lingual) apical of the statistically significant. A more detailed
flammatory cell infiltrates but was charac-
CEJ, while in the flapless group the corre- examination revealed that the reduction
terized by the presence of a dense network
sponding dimensions were 0.07  0 mm in the apical portion was 5  3% (flap)
of collagen fibers.
(buccal) and 0  0 mm (lingual). In other and 6  5% (flapless), respectively, while
The entrance of all socket sites was
words, at the buccal surface of the teeth in
‘closed’ by a hard tissue bridge of varying
dimensions that connected the buccal and

Fig. 4. Microphotograph of the buccal bone crest of


the mesial root of a second premolar in the flap
Fig. 3. Microphotograph of the buccal bone crest of group. Note that the apical cells of the junctional
the mesial root of a second premolar in the flapless epithelium were located apical of the cementum–
group. Note that the apical cells of the junctional enamel junction and the most coronal portion of the
epithelium were located at the cementum–enamel bone crest exhibited signs of resorption. BC, bone
junction. BC, bone crest. Ladewig fibrin stain; crest. Ladewig fibrin stain; original magnification
original magnification  50.  50.

Table 1. Results of the histometric measurements (expressed in mm) performed at the


buccal and lingual aspects of the mesial roots; tooth sites
Buccal Lingual
Flapless Flap Flapless Flap
Fig. 2. Microphotograph of a buccal-lingual section CEJ–aJE 0.07  0.1 0.2  0.1 00 00
representing the second mandibular premolar and CEJ–BC 0.7  0.2n 1.0  0.1 0.8  0.2 0.7  0.2
the surrounding tissues. Note that the base of the n
mandible occupied a larger area than the alveolar Po0.05.
Mean  (SD).
process. B, buccal bone wall; L, lingual bone wall.
aJE, the apical cells of the junctional epithelium; BC, bone crest; CEJ, cementum–enamel junction.
Ladewig fibrin stain; original magnification  7.

c 2009 The Authors. Journal compilation 


 c 2009 John Wiley & Sons A/S 547 | Clin. Oral Impl. Res. 20, 2009 / 545–549
Araújo & Lindhe . Flapless tooth extraction

The main observation made in the cur-


rent study, however, was that similar
amounts of hard tissue loss occurred after
the teeth (roots) had been removed in a
flapless as against a flap elevation proce-
dure. Thus, in the coronal third of the
edentulous ridge, both types of extraction,
after 6 months of healing, had resulted in a
35% reduction of the hard tissue dimen-
sion. This finding may be interpreted as
not being in agreement with data published
recently (e.g. Blanco et al. 2008; Fickl et al.
2008). Fickl et al. (2008) studied tissue
alterations after tooth extraction performed
in either a flapless or a flap procedure in the
beagle dog. Healing was studied 2 and 4
months after tooth extraction using volu-
metric measurements made on casts. In
other words, the measurements included
both soft and hard tissue components. The
authors concluded ‘. . .. leaving the perios-
teum in place decreases the resorption rate
of the extraction socket’. A more detailed
analysis of the data illustrated that both
extraction techniques resulted in loss of
Fig. 5. Microphotograph of a buccal–lingual section tissue volume, but also that the model
representing the edentulous site in the flapless group. used in the experiment did not distinguish
Fig. 6. Microphotograph of a buccal–lingual section
Note that the center of the alveolar ridge is occupied
representing the edentulous site in the flap group. between soft and hard tissue components.
mainly by bone marrow. Furthermore, the cortical
Note that the profile of the ridge has many features Blanco et al. (2008) examined ridge altera-
crest slopes in the apical direction from the lingual to
in common with that of the flapless group. B, buccal
the buccal wall of the ridge. B, buccal bone wall; BM, tions following immediate implant place-
bone wall; BM, basal body of the mandible; L,
basal body of the mandible; L, lingual bone wall.
lingual bone wall. Ladewig fibrin stain; original ment in fresh extraction sockets in a dog
Ladewig fibrin stain; original magnification  7. model. The teeth were removed either in a
magnification  7.
flapless or in a flap elevation procedure. In
the corresponding reduction in the middle Table 2. Mean  (SD) relative alteration biopsies obtained after 3 months of healing
portion was 14  11% (flap) and 9  5% (% change in comparison with the tooth following implant (Straumannt implant
site) of the surface area (mm2) of the over-
(flapless). In the marginal portion of the all and, coronal and middle and apical System) installation it was observed that
thirds of the edentulous alveolar process
edentulous ridge, there was a marked re- the buccal BC was located on average
Area Flapless site (%) Flap site (%)
duction of the dimension in both groups. 4.13 mm (flap) and 3.62 mm (flapless)
This amounted to 35  15% in the flap Overall  17  16  14  6 from the shoulder of the device. The corre-
Coronal  35  25  35  15
and 35  25% in the flapless group. This sponding distances on the lingual aspect
Middle 9  5  14  11
difference between the groups was not Apical 6  5 5  3 were 3.13 mm (flap) and 3.17 mm (flap-
statistically significant. less). In this context it should be observed
 A relative decrease of the cross-section area.
that the ‘abutment’ portion of the Strau-
Discussion mannt implant is 2.8 mm high (the dis-
flap elevation. Moreover, the buccal aspect tance between shoulder and the marginal
The present experiment confirmed that the of the mesial tooth portion in the flap group border of the SLA surface). In other words,
removal of a single tooth (root) during had undergone more attachment and bone the difference between the flapless and the
healing caused a marked change in the loss than was the case in the corresponding flap group after 3 months amounted to
edentulous ridge. Thus, in the apical and site of the flapless group. about 0.5 mm at the buccal aspect, while
middle portions of the socket site, minor The present findings are in agreement on the lingual aspect there was virtually no
dimensional alterations occurred while in with data published by e.g. Pietrokovski & difference. One important difference be-
the coronal portion of the ridge, the reduc- Massler (1967), Schropp et al. (2003) and tween the current study and the experi-
tion of the hard tissue volume was sub- Barone et al. (2008) showing that the loss ment by Blanco et al. (2008) is the length of
stantial. It was also observed that similar (extraction) of teeth will result in loss of the healing period, i.e. 6 vs. 3 months. It
amounts of bone loss occurred during heal- tissue volume in the edentulous ridge and has been shown by e.g. Schropp et al.
ing irrespective of the procedure used for that tissue loss is more pronounced from the (2003) that dimensional changes following
tooth removal, i.e. flapless or following buccal than from the lingual/palatal aspect. tooth extraction are not completed after

548 | Clin. Oral Impl. Res. 20, 2009 / 545–549 c 2009 The Authors. Journal compilation 
 c 2009 John Wiley & Sons A/S
Araújo & Lindhe . Flapless tooth extraction

3 months but that between 3 and 12 0.1 mm. This finding was confirmed by tum, periodontal ligament and bundle
months additional resorption and reduction the results of the present study. Thus, the bone) play a crucial role in the mainte-
will occur. The data from the present histometric measurements performed in nance of the dimensions of the alveolar
experiment therefore suggest that the 0.5- the tooth sites indicated that some attach- process and that the absence of a tooth
mm difference between the flap and the ment loss (CEJ – aJE) had occurred at the per se will reduce the demand for tissue
flapless group observed in the Blanco et al. buccal surface of the mesial root. In the support at that site.
(2008) study may disappear after longer flap group, this loss amounted to 200 mm Moreover, the removal of the root from
healing periods. while the corresponding number in the its socket involves a pronounced mechan-
It is well established in the periodontal flapless group was only 70 mm. Further- ical trauma to the periodontal ligament and
literature that the elevation of a full-thick- more, the height of the buccal BC in the its blood vessels as well as to the bundle
ness flap (muco-periostal flap) to gain ac- flap group was significantly reduced. bone and the bone of the alveolar process.
cess to the root surface for debridement Hence, it can be estimated that sulcus The ensuing inflammatory response is
may cause some loss of attachment and incision and full-thickness flap elevation transient but involves both hematopoietic
resorption of bone (for a review, see Tavti- will result in some loss of attachment and and mesenchymal cells in the site (e.g.
gian 1970; Heitz-Mayfield et al. 2002). crestal bone height in the thin buccal Amler 1969; Cardaropoli et al. 2003). Dur-
The extent of reduction of the supporting compartment of the ridge also in the beagle ing wound healing, new bone is formed in
bone is apparently related to the thickness dog model. There are reasons to suggest the socket while old bone on the inside and
of the bone at the surgical site (Wood et al. that the inflammatory response to the outside of the socket walls is resorbed.
1972; Karring et al. 1975; Yaffe et al. 1994). mechanical instrumentation in the site as Such post-extraction events will evidently
Thus, the thinner the bone wall, the well as an impaired vascular supply from result in a net loss of hard tissue. The
greater becomes the crestal resorption. In the severed periosteum during the initial question remains as to whether flap eleva-
a recent study in the beagle dog from our phase of healing may be considered as tion in this context induces an additional
laboratory (Araújo et al. 2005) it was de- causative factors for soft and hard tissue mechanical trauma with an ensuing in-
monstrated that flap elevation without in- resorption and loss. flammatory response that is large enough
tentional root surface instrumentation The findings of Pietrokovski & Massler to have a long-lasting effect on the final
caused about 1-mm vertical loss of the (1967), Pietrokovski et al. (2007) have been dimensions of the edentulous ridge. The
thin buccal wall while in the thick lingual interpreted to show that the tooth (root) in data from the current experiment indicate
wall the corresponding loss was only function and its supporting tissues (cemen- that this may not be the case.

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c 2009 The Authors. Journal compilation 


 c 2009 John Wiley & Sons A/S 549 | Clin. Oral Impl. Res. 20, 2009 / 545–549

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