Alveolar socket healing: what can we learn

Alveolar socket healing: what canwe learn?MAURICIO G. ARA �UJO, CL �EVERSON O. SILVA, MONICA MISAWA & FLAVIA

SUKEKAVA

In current dentistry, the healing process of thesocket following tooth extraction has become animportant topic of research, study and discussion.The reason for this relies mainly on the fact thatafter tooth extraction several changes can occur inthe alveolar process, which may prevent or renderdifficult implant installation in a prosthetically dri-ven position (23). In addition, the increasingdemand for esthetics in dentistry highlights theimportance of maintaining adequate ridge volumein order to achieve a long-term esthetically accept-able implant-support prosthesis (42). Thus, it isincreasingly expected that the results of the healingprocess should promote the formation of an alveo-lar ridge with a sufficient volume of hard and softtissues to allow an ideal implant-supported restor-ative outcome.

Tooth extraction was once described as a tissueamputation that may lead to functional, psychologi-cal, postural and local changes (14). Indeed, toothextraction is initially perceived purely as tooth loss,but local changes arise and promote hard- andsoft-tissue alterations. The process of local changesthat take place in order to close the wound andrestore tissue homeostasis is called “socket healing”.Thus, the aims of the present review were two-fold:first, to describe the socket-healing process; and, sec-ond, to discuss what is to be learned from that healingprocess that may improve the treatment outcome.

The alveolar process

In order to understand the socket-healing processand its clinical implications, it is pivotal to know thecharacteristics of the tissues that comprise the alveo-lar process. Thus, a brief anatomic and histologicdescription of such tissues is provided below (fordetailed review, see 7, 65).

Anatomic considerations

The alveolar process may be defined as the bone tis-sue that surrounds a fully erupted tooth and it isformed in harmony with the development and erup-tion of the teeth (Fig. 1). It is limited coronally by thebone margins of the socket walls, whilst an imaginaryline that cuts the bottom of the socket in a perpendic-ular direction to the long axis of the root, limits it api-cally. Beyond such a line, the basal bone of themandible or the maxilla can be found.

The morphologic characteristics of the alveolarprocess are related to: (i) the size and shape of thetooth; (ii) the site of tooth eruption; and (iii) the incli-nation of the erupted tooth. In general, teeth tend toerupt and incline to a position outside the center ofthe basal bone (62). In a recent clinical study, Janua-rio et al. (46) described some of the morphological

Fig. 1. Cone-beam tomographic image representing thealveolar process at the maxillary lateral incisor region. Thealveolar process is the bone that surrounds the root.

122

Periodontology 2000, Vol. 68, 2015, 122–134 © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Printed in Singapore. All rights reserved PERIODONTOLOGY 2000

features of the alveolar process in the anterior maxillain humans. The authors included 250 periodontallyhealthy subjects, 17–66 years of age. Cone beam com-puted tomograms were obtained from the maxillaryfront teeth. Measurements of the thickness of thebuccal bone plate of the alveolar process were per-formed at three different positions in relation to thebuccal bone crest (i.e. at distances of 1, 3 and 5 mmapical to the crest). The measurements demonstratedthat the buccal bone plate in most locations, in allanterior tooth sites examined, was ≤1 mm thick (aver-age thickness ~0.5 mm) and that close to 50% of siteshad a bone plate thickness that was ≤0.5 mm. In con-clusion, tooth sites in the anterior maxilla have a thinbuccal bone wall (Fig. 2), which probably contributesto its loss following tooth extraction.

Histologic considerations

The inner portion of socket walls is named “alveolarbone proper” or bundle bone (a histological term)and the remaining hard structure is called “alveolarbone”. The bundle bone is a lamellar bone, 0.2–0.4 mm wide (65), composed of circumferentiallamellae, whilst the alveolar bone is also of the lamel-lar type but composed of concentric and interstitiallamellae and of marrow. In the bundle bone, theSharpey’s fibers are invested in such way that theyconnect the periodontal ligament to the alveolar boneand skeleton. Likewise, on the contralateral side ofthe periodontal ligament, the dental cementuminvested with Sharpey’s fibers connects the periodon-tal ligament to the dentin. As with root cementumand the periodontal ligament, the bundle bone is atooth-dependent structure. Overall, the bundle boneand the buccal bone plate frequently exhibit a similar

thickness at the anterior front tooth region. Thus,most of the thin buccal bone wall is a tooth-depen-dent structure (Fig. 3).

Socket healing

Dimensional changes

The dimensional changes that occur in the alveolarridge following tooth extraction have been reportedin several human studies (14, 16, 47, 48, 62, 63, 66, 74)and were determined using different methodologies,including clinical, cast model and radiographic exam-inations. After multiple tooth extractions and the useof complete removable prostheses, the alveolar ridgeundergoes marked contraction in both vertical andhorizontal directions (13, 14, 32, 47, 48). Followingseveral years of full denture use, individuals mayundergo a wide variation in alveolar ridge reductionand some may exhibit a fully resorbed alveolar ridge(16). Following single-tooth extraction, the ridgeexhibits a limited reduction in its vertical dimension,but the horizontal reduction is substantial (Fig. 4; 62,63). It can be expected that: (i) up to 50% reduction ofthe original ridge width will occur; (ii) the amount of

Fig. 2. Occlusal view of a dried skull specimen. Note thelimited thickness of the buccal bone wall at the centralincisor regions.

Fig. 3. Buccal–lingual section illustrating the most coronalportion of the buccal bone wall. The buccal wall is mademainly by bundle bone. Polarized light. Toluidine bluestain; original magnification 3 50.

Alveolar socket healing

123

bone resorption will be greater at the buccal aspectthan at its lingual/palatal counterpart; and (iii) a lar-ger amount of alveolar bone reduction will take placein the molar regions.

The end of the socket-healing process is clinicallyobserved as the closure of the socket entrance by firmepithelialized soft tissue and/or radiographic bone fillof the socket. A broad variation among individualscan be expected regarding the time needed for com-pletion of socket healing (32, 47, 48, 66, 74). Thesocket entrance may be restored between 10 and20 weeks (48, 69) and radiographic bone fill observedbetween 3 and 6 months post-extraction (66). Whilstmost of the dimensional changes that comprisesocket healing occur during the first 3 months(Fig. 5), the reorganization of the alveolar ridge maycontinue for up to 1 year post-extraction (20, 66). It isreasonable to suggest that the rate of socket healing isinfluenced by biologic differences among individuals,alveolar socket size (large vs. small sockets) and theextent of surgical trauma induced during the extrac-tion procedure.

Histologic changes

The sequence of events that arise following toothextraction has been described in both human andcanine studies (1–5, 10, 32, 74). In human studies,biopsies from the marginal portion or from the cen-tral portion of the healing sockets were used todescribe the healing events, whereas in animal stud-ies (dog model), biopsies from the entire alveolarsocket were prepared for histologic analyses.Although bone modeling and remodeling is three tofive times faster in dogs than in humans (60), theoverall histologic findings from these studies

showed a remarkable similarity between sockethealing in dogs and in humans. Thus, it wasobserved that the socket-healing process may bedivided into three sequential, and frequently over-lapping, phases: inflammatory; proliferative; andmodeling/remodeling.

Inflammatory phase

The inflammatory phase may be subdivided into twoparts: blood clot formation and inflammatory cellmigration. Immediately after tooth extraction, hem-orrhage occurs and the socket is filled with blood.The blood clot plugs the severed vessels and stopsbleeding. Within 2–3 days, large numbers of inflam-matory cells migrate to the wound in order to “clean”the site before new tissue can start forming. The com-bination of inflammatory cells, vascular sprouts andimmature fibroblasts forms the granulation tissue. Asthe site becomes sterilized, the granulation tissue isgradually replaced with a provisional connective tis-sue matrix that is rich in collagen fibers and cells, andthe proliferative phase of the wound-healing processbegins.

Proliferative phase

The proliferative phase may also be divided into twoparts – fibroplasia and woven bone formation – and ischaracterized by intense and rapid tissue formation.Fibroplasia involves the rapid deposition of a

Fig. 4. Clinical photography of an alveolar ridge12 months after tooth extraction. Note the substantialreduction in the buccal–lingual dimension of the healedridge.

Fig. 5. Buccal–lingual section illustrating the crest of thesocket wall 2 months following tooth extraction. The bonesurface is covered with osteoclasts. Hematoxylin–eosinstain; original magnification 3 100.

Ara�ujo et al.

124

provisional matrix. Subsequently, the provisionalmatrix is penetrated by several vessels and bone-forming cells, and finger-like projections of wovenbone are laid down around the blood vessels. Eventu-ally, the projections completely surround a vessel andthe primary osteon is thus formed (Fig. 6). The pri-mary osteons may be occasionally reinforced byparallel-fibered bone. Woven bone can be identifiedin the healing socket as early as 2 weeks after toothextraction and remains in the wound for severalweeks. Woven bone is a provisional type of bonewithout any load-bearing capacity and thereforeneeds to be replaced with mature bone types (lamel-lar bone and bone marrow).

Bone modeling and remodeling phase

Bone modeling and remodeling is the third and lastphase of the socket-healing process. Bone modelingis defined as a change in the shape and architectureof the bone, whereas bone remodeling is defined as achange without concomitant change in the shape andarchitecture of the bone. The replacement of wovenbone with lamellar bone or bone marrow is boneremodeling, whereas the bone resorption that takesplace on the socket walls leading to a dimensionalalteration of the alveolar ridge is the result of bonemodeling. Bone remodeling in humans may take sev-eral months and exhibits substantial variability

among individuals (32, 74). In a recent study, Lindheet al. (54) examined the tissue composition of biop-sies from 36 individuals retrieved from previoussocket sites in the posterior maxilla after >16 weeks ofhealing. The authors reported that about 60–65% ofthe tissue volume was made up of lamellar bone andbone marrow. Thus, the complete remodeling of thewoven bone into lamellar bone and bone marrowmay take several months or years.

The resorption of the socket walls was studied inbiopsies obtained from human samples (32) and froma series of studies in dogs (3–6, 10). A few weeks aftertooth removal, osteoclasts could be found around thecrest of both buccal and lingual walls and on theouter and inner (bundle bone) portions of the socket(Fig. 7). Bone modeling takes place equally on buccaland lingual walls, but because the lingual bone is usu-ally wider than the buccal bone wall, modeling resultsin greater vertical bone loss at the thin buccal platethan at the wide lingual wall. In addition, bone mod-eling takes place earlier than bone remodeling, insuch way that about two-thirds of the modeling pro-cess occurs in the first 3 months of healing (66). Insummary, modeling and remodeling processes duringsocket healing result in qualitative and quantitativechanges at the edentulous site, which culminate in areduction of the dimension of the ridge.

Fig. 6. Micrograph illustrating primary osteons in thehealing socket. The collagen fibers have a woven organiza-tion. Toluidine blue stain; original magnification 3 100.

Fig. 7. Buccal–lingual section of the socket wall a fewmonths following tooth extraction. Note the intense mod-eling and remodeling process characterized by the pres-ence of bone multicellular units and reversal lines.Ladewig fibrin stain; original magnification 3 20.


125

Stimulating factors

The initial healing responses in a wound are regulatedby signaling molecules (i.e. growth factors and cyto-kines), such as platelet-derived growth factor, insulin-like growth factors, transforming growth factor-betaand fibroblastic growth factors. They initiate cellmigration, differentiation and proliferation as theyinteract with each other in highly ordered temporaland spatial sequences (53). These growth factors actas mitogenic and angiogenic signals at the early stageof bone healing. Once activated, growth factors insti-gate a series of events via ligand–receptor interac-tions, including signal transduction, genetranscription, mRNA-directed protein biosynthesisand secretion of post-translational proteins (44).

Few studies have examined the roles of growth fac-tors and cytokines during socket healing (40, 74).Fisher et al. (40) evaluated the expression of growthfactors during socket-healing events in a rabbitmodel. The authors observed that: (i) fibroblastgrowth factor-2 presented at higher levels at earlytime points, before returning to lower levels; (ii) vas-cular endothelial growth factor levels were main-tained constant during healing; (iii) platelet-derivedgrowth factor-A levels increased during the first daysof socket healing; (iv) transforming growth factor-beta1 presented a small elevation at early time points;and (v) an increased expression of bone morphoge-netic protein 2 was observed when osteoblast precur-sors accumulated and began to proliferate. Trombelliet al. (63) studied modeling and remodeling ofhuman extraction sockets and evaluated the expres-sion of bone morphogenetic protein 7 during sockethealing. The results demonstrated that bone morpho-genetic protein 7 increased during early and interme-diate healing phases, and a period of increased bonemodeling and remodeling activity occurred, leadingto the deposition of woven bone from provisionalmatrix. In summary, growth factors present multipleactivities, generally with overlapping actions, and asimplistic characterization of their effects is not possi-ble, or indeed appropriate.

What can we learn?

There are several lessons to be learned from thevarious reports of local changes following toothextraction. The healed socket eventually fills withnewly formed bone and the alveolar ridge contracts.The ridge reduction is larger in the molar region

(62), but it becomes more critical in the anteriorregion as a result of esthetic demands. The anteriormaxillary region exhibits very thin socket walls (19,46) that are frequently made up of only bundlebone. As the bundle bone is a tooth-dependentstructure, it is gradually resorbed following exodon-tia. Finally, the postextraction ridge reductionappears to be related to several factors, includingsurgical trauma, lack of a functional stimulus on thebone walls, lack of bundle bone and periodontal lig-ament and genetic information.

Tooth extraction is a traumatic procedure and, dur-ing its course, the soft tissues are disrupted, the vas-cular structures of the periodontal ligament aredamaged or destroyed and the principal fibers of theperiodontal ligament are severed (29). In addition, itis well established in the dental literature that the ele-vation of a full-thickness flap, in order to gain accessto the root, may cause resorption of thin bone walls(50, 75–77; for reviews see 43, 70). However, differentanimal and clinical studies have failed to support theconcept that tooth extraction without flap elevationprevents ridge reduction (8, 17, 33, 39). These studiesindicate that the surgical trauma promoted by theremoval of the tooth itself overlaps with the surgicaltrauma promoted by the elevation of a full-thicknessflap.

The surgical trauma caused by tooth extractionmay be limited by minimally invasive surgical proce-dures (58). Such procedures aim to prevent expansionof the socket housing, which otherwise may fracturethe thin adjacent bony walls. For this purpose, theuse of forceps to luxate the tooth by applying forcestoward the buccal palatal/lingual aspects of thesocket is not recommended. Likewise, the forcepsshould not perform rotational movements, as thecross-section shape of a root is seldom circular. Sev-eral new surgical instruments, which promote mini-mally invasive tooth extraction, are currentlycommercially available. Periotomes and verticaltooth-extraction systems are among the instrumentsmost frequently used for this purpose. Periotomes areinstruments designed to sever the periodontal liga-ment fibers at the mesial and distal aspects of thesocket, in order to facilitate and improve the effi-ciency of root elevators. Vertical tooth-extraction sys-tems are, on the other hand, designed to pull roots ina vertical direction and hence avoid any damage tothe socket walls. In both techniques described above,no pressure is applied to the buccal socket wall; how-ever, such techniques are efficient only for conical orstraight roots.

Ara�ujo et al.

126

Tab

le1.

Clin

ical

studiesthat

evaluated

graftingsock

etswithdifferentmaterialsan

dmechan

ical

barriersto

preve

ntalve

olarridge

reductionfollo

wingtooth

extrac

tion

Authors

nMaterial

Methodof

evaluation

Follow-u

pOutcome

Cam

argo

etal.

(24)

16patients32

sock

ets

Bioac

tive

glass(test)vs.e

xtraction

alone(control)

Clin

ical

6months

Chan

gein

ridge

width

(test:�3

.48�

2.68

mm;

control:�3

.06�

2.41

mm)

Chan

gein

ridge

heigh

t(test:�0

.38�

3.18

mm;

control:�1

.00�

2.25

mm)

Nodifference

betwee

ngroups

Iasella

etal.(45

)24

patients24

sock

ets

Tetracyclinehyd

ratedFDBA(test)vs.

extrac

tionalone(control)

Clin

ical

and

histologic

4–6months

Chan

gein

ridge

width

(test:from

9.2�

1.2mm

to8.0�

1.4mm;c

ontrol:from

9.1�

1.0mm

to6.4�

2.2mm)

Chan

gein

ridge

heigh

t(test:1.3�

2.0mm;c

ontrol:

0.9�

1.6mm)

FDBAim

prove

dridge

heigh

tan

dwidth

dim

ensions

compared

withextrac

tionalone

Serinoet

al.(67

)36

patients

39sock

ets

Polylactidean

dpolyglycolid

esp

onge

(test)vs.e

xtractionalone(control)

Clin

ical

and

histologic

6months

Chan

gein

ridge

heigh

t(test:0.2�

1.5mm;c

ontrol:

�0.7

�1.2mm)

Testgroupmay

preserveorreduce

alve

olarbone

resorption

Luczyszynet

al.

(55)

15patients

30sock

ets

Acellu

lardermal

matrixan

dresorbab

lehyd

roxyap

atite(test)vs.a

cellu

lar

dermal

matrixalone(control)

Clin

ical

and

histologic

6months

Ridge

width

(test:6.8�

1.26

mm;c

ontrol:

5.53

+1.06

mm)

Acellu

lardermal

matrixwas

able

topreserveridge

thickn

essan

dthead

ditional

use

ofresorbab

lehyd

roxyap

atitefavo

redpreservationoftheridge

s

Baroneet

al.(15

)40

patients

40sock

ets

Corticoca

ncello

usporcinebone(test)

vs.e


Clin

ical

and

histologic

7months

Chan

gein

ridge

width

(test:�2

.5�

1.2mm;c

ontrol:

�4.3

�0.8mm)

Chan

gein

ridge

heigh

t(test:�0

.7�

1.4mm;c

ontrol:

�3.6

�1.5mm)

Testgrouplim

ited

resorption

Cardaropoli&

Cardaropoli(30)

10patients

10sock

ets

Bovinebonemineral

(caseseries)

Clin

ical

and

histologic

4months

Chan

gein

ridge

width:from

11.8

�1.53

mm

to9.95

�2.31

mm

Neiva

etal.(61

)24

patients

24sock

ets

Putty-form

hyd

roxyap

atitematrix

combined

withthesynthetic

cell-

bindingpep

tideP-15(test)vs.

extrac

tionalone(control)

Clin

ical,h

istologic

andradiograp

hic

16wee

ksChan

gein

ridge

width

(test:�1

.31�

0.96

mm;c

ontrol:

�1.43�

1.05

mm)

Chan

gein

ridge

heigh

t(test:0.15

�1.76

mm;c

ontrol:

�0.56�

1.04

mm)

Afavo

rable

resp

onse

was

observed

when

puttyP15

was

applie

dto

extrac

tionsock

ets


127

Tab

le1.

(Con

tinued

)

Authors

nMaterial

Methodof

evaluation

Follow-u

pOutcome

Mardas

etal.(56

)26

patients

26sock

ets

B-TCP(test)vs.b

ovinebonemineral

(control)

Clin

ical

and

histologic

8months

Chan

gein

ridge

width

(test:�1

.1�

1.0mm;c

ontrol:

�2.1

�1.0mm)

Chan

gein

ridge

heigh

t(test:�0

.4�

0.5mm;c

ontrol:

�0.1

�0.7mm)

Nodifference

betwee

ngroups

Fernan

des

etal.

(38)

18patients

Acellu

lardermal

matrixan

dan

organ

icbonematrixcell-bindingpep

tideP-15

(test)vs.a

cellu

lardermal

matrixalone

Clin

ical

6months

Chan

gein

ridge

width

(test:�2

.53�

1.81

mm;c

ontrol:

�3.40�

1.39

mm)

Chan

gein

buccal

crestheigh

t(test:�1

.20�

2.02

mm;

control:�1

.50�

1.15

mm)

Nodifference

betwee

ngroups

Nam

etal.(59

)42

patients

44sock

ets

Synthetic

olig

opep

tide-co

ated

bone

mineral

(test)vs.b

onegraftwithout

pep

tide(control)

Clin

ical

and

histologic

6months

Chan

gein

ridge

width

(test:�1

.2�

1.5mm;c

ontrol:

�1.3

�1.4mm)

Chan

gein

buccal

crestheigh

t(test:�2

.3�

3.6mm;

control:�2

.3�

2.1mm)

Nodifference

betwee

ngroups

Brkovicet

al.(20

)20

patients

20sock

ets

B-TCP/typ

eIco

llage

nco

nes

with(test)

orwithout(control)abarrier

mem

brane

Clin

ical

and

histologic

9months

Chan

gein

ridge

width

(test:from

7.39

�2.00

mm

to6.53

�1.83

mm;c

ontrol:from

7.88

�2.33

mm

to6.59

�2.44

mm)

Chan

gein

ridge

heigh

t(test:from

3.00

�1.85

mm

to3.38

�1.94

mm;c

ontrol:from

3.00

�1.25

mm

to3.22

�1.48

mm)

Nodifference

betwee

ngroups

Mardas

etal.(57

)27

patients

27sock

ets

B-TCP(test)vs.b

ovinebonemineral

(control)

Rad

iograp

hic

32wee

ksChan

gesin

ridge

hight(testgroup:

Mside�0

.9�

1.2mm;D

side�0

.7�

1.8mm;

controlg

roup:M

side�0

.4�

1.3mm;D

side

�0.7

�1.3mm)

Nodifference

betwee

ngroups

Kim

etal.(51

)20

patients

20sock

ets

Colla

gensp

onge

andxenoge

neicbone

grafts

(test)vs.e

xtractionalone

(control)

Histologic

3months

Resorptionin

ridge

width

(test:14

.26%

;control:

20.74%

)Xen

ograftpreve

nts

thehorizo

ntalresorptionofthe

alve

olarridge

,andtheupper

colla

gensp

onge

block

stheinfiltrationofsofttissues

tothelower

area

Kutkutet

al.(52

)16

patients

16sock

ets

Calcium

sulfatehem

ihyd

rate

and

platelet-rich

plasm

a(test)vs.c

olla

gen

resorbab

leplug(control)

Clin

ical

and

histologic

3months

Chan

gein

ridge

width

(test:�1

.7�

1.4mm;

control:�1

.7�

1.6mm)

Chan

gein

ridge

heigh

t(test:0.2�

0.9mm;c

ontrol:

�1.0

�0.8mm)

Nodifference

betwee

ngroups

Ara�ujo et al.

128

Tab

le1.

(Con

tinued

)

Authors

nMaterial

Methodof

evaluation

Follow-u

pOutcome

Brownfield&

Weltm

a(21)

17patients

20sock

ets

Osteo

inductivedem

ineralized

bone

matrixwithca

ncello

usbonech

ips

(test)vs.e


Clin

ical,h

istologic,

radiograp

hic

and

tomograp

hic

10–1

2wee

ksChan

gein

ridge

width

(test:�1

.00�

0.40

mm;

control:�1

.30�

1.00

mm)

Chan

gein

ridge

heigh

t(test:�0

.80�

1.20

mm;

control:�1

.20�

0.40

mm)

Nodifference

betwee

ngroups

Gholamie

tal.

(41)

12patients

28sock

ets

Synthetic

nan

ocrystalline

hyd

roxyap

atite(testgroup1)

Xbovine

bonemineral

(testgroup2)

Clin

ical

and

histologic

6–8months

Thewidth

intest

group2decreased

from

7.75

�1.55

mm

to6.68

�1.85

mm

andin

test

group

1decreased

from

7.36

�1.94

mm

to6.43

�2.08

mm

Nodifference

betwee

ngroups

Toloueet

al.(72

)21

patients

31sock

ets

Calcium

sulfate(test)vs.F

DBA

(control)

Clin

ical

and

histologic

3months

Chan

gein

ridge

width

(test:�1

.33�

1.22

mm;

control:�1

.03�

0.87

mm)

Chan

gein

ridge

heigh

t(test:�0

.32�

1.69

mm;

control:�0

.05�

1.46

mm)

Nodifference

betwee

ngroups

Cardaropoliet

al.

(31)

41patients

48sock

ets

Bovinebonemineral

(test)vs.

extrac

tionalone(control)

Clin

ical

and

histologic

4months

Thetest

groupsh

owed

less

reductionin

ridge

width

(1.04�

1.08

mm

vs.4

.48�

0.65

mm)an

dheigh

t(0.46�

0.46

mm

vs.1

.54�

0.33

mm)

Bovinebonemineral

considerab

lylim

itstheam

ountof

horizo

ntala

ndve

rtical

boneresorption

Cook&Mea

ley

(35)

44patients

44sock

ets

Bovinexenograft(testgroup1)

vs.

sponge

composedof7

0%typeI

bovineco

llage

nco

ated

with30

%nonsinteredhyd

roxyap

atite(test

group2)

Clin

ical

and

histologic

21wee

ksChan

gein

buccal

ridge

heigh

t(testgroup1:

�0.14�

2.21

mm;testgroup2:

0.03

�2.81

mm)

Chan

gein

lingu

alridge

heigh

t(testgroup1:

�0.21�

3.04

mm;testgroup2:

�1.18�

1.93

mm)

Chan

gein

ridge

width

(testgroup1:

�1.57�

1.21

mm/

test

group2:

�1.16�

1.44

mm)

Nosign

ifica

ntdifference

betwee

ngroups

Clozzaet

al.(34

)13

patients

32teeth

Bioac

tive

glass(caseseries)

Tomograp

hic

3months

Preservationofa

bout77

%oftheoriginal

width

dim

ensions

Theboneloss

inwidth

was

1.8�

1.1mm;v

ertica

lboneloss

was

2.7�

1.1mm


129

Tab

le1.

(Con

tinued

)

Authors

nMaterial

Methodof

evaluation

Follow-u

pOutcome

Junget

al.(49

)40

patients

40sock

ets

Beta-tricalcium

phosp

hateparticles

(testgroup1)

vs.b

ovinebonemineral

cove

redwithaco

llage

nmatrix(test

group2)

vs.D

BBM-C

cove

redwithan

autoge

noussoft-tissu

egraft(test

group3)

vs.spontaneo

ushea

ling

(control)

Tomograp

hic

6months

Vertica

lchan

gesrange

dbetwee

n�0

.6mm

(�10

.2%)

forco

ntrola

ndaga

inof0

.3mm

(5.6%)fortest

group

3onthelin

gual

side,

andbetwee

n�2

.0mm

(�20

.9%)

forbeta-tricalcium

phosp

hatean

daga

inof1

.2mm

(8.1%)fortest

group3onthebuccal

side

Themost

accentuated

ridge

width

chan

geswere

reco

rded

1mm

below

thecrest:�3

.3mm

(�43

.3%,

control),�

6.1mm

(�77

.5%,b

eta-tricalcium

phosp

hate),�

1.2mm

(�17

.4%,testgroup2)

and

�1.4

mm

(�18

.1%,testgroup3)

DBBM-C

cove

redwithCM

orau

toge

noussoft-tissu

egraft,resu

lted

inreducedve

rtical

andhorizo

ntal

chan

ges

Shak

ibaie-M

(68)

10patients

32sock

ets

Bovinebonematerial(test

group1)

vs.

orhyd

roxyap

atitean

dsilic

ondioxide

(testgroup2)

vs.stypro

gelatinsp

onge

(control)

Clin

ical

and

histologic

12–1

4wee

ksAlveo

larridge

width

reduction(testgroup1=0.5mm;

test

group2=1.5mm;c

ontrol=2.0mm)

Alveo

larridge

heigh

treduction(testgroup1=1.0mm;

test

group2=1.5mm;c

ontrol=2.0mm)

Fixed

gingiva

width

reduction(testgroup1=0.5mm;

test

group2=2.4mm;c

ontrol=2.5mm)

Bovinexenograftresu

lted

inbetterbonequalityan

dquan

tity

Thalmairet

al.

(71)

30patients

30sock

ets

Prehyd

ratedco

llage

nated

cortico-

cancello

usporcinebonean

dfree

gingiva

lgraft(testgroup1)

vs.free

gingiva

lgraftalone(testgroup2)

vs.

xenoge

nic

bonesu

bstitute

(testgroup

3)vs.e


Clin

ical

4months

Allgroupsdisplaye

dco

ntoursh

rinka

geat

the

buccal

aspectrangingfrom

amea

nhorizo

ntal

reductionof�

0.8�

0.5mm

(testgroup1)

to�2

.3�

1.1mm

(control)

Freegingiva

lgraftlim

ited

theco

ntoursh

rinka

ge

Ara� ujo

etal.(12

)28

patients

28sock

ets

Bovinebonemineral

(test)vs.

extrac

tionalone(control)

Tomograp

hic

4months

Bovinebonemineral

counteracted

thereductionin

hardtissue

Red

uctionin

hardtissuewas

3%in

thetest

group

compared

with25

%in

theco

ntrol.

FDBA,freeze-dried

boneallograft;B-TCP,b

eta-

tricalcium

phosp

hate;

Mside,

mesialside;

Dside,

distalside;

DBBM-C

,bovinebonemineral;C

M,colla

genmatrix.

Ara�ujo et al.

130

Teeth provide support for very thin bone walls,although fenestrations and dehiscence may occurnaturally when the bone thickness is below a certainthreshold (65). It is suggested, however, that implantsshould be provided with bone walls about 1- to 2-mm-wide on buccal and lingual aspects to allow astable bone height to be maintained (22, 42). The rea-sons why teeth can support thin bone walls, and whyimplants seem to fail to do so, remains obscure. It hasbeen suggested, however, that the presence of bundlebone and periodontal ligament around teeth arelikely explanations. Bundle bone is capable of existingin thinner dimensions than are alveolar or basalbones because the periodontal ligament provides thefunctional stimulus as well as the nutritional and cel-lular source for its maintenance.

It is now well established that following toothextraction the ridge crest moves toward the long axisof the basal bone (16, 63). The shape of the jawboneappears to return to the shape that was present priorto the development of the alveolar process duringtooth eruption. The lack of a functional stimulus onthe bone walls and the need for tissue adjustment tomeet “genetically” determined demands regardingridge geometry in the absence of teeth (2) mayexplain this modification.

Grafting sockets with different materials, and theuse of mechanical barriers, have been proposed toprevent alveolar ridge reduction, secondary to bonemodeling. Clinical studies have been performed toevaluate the outcome of such surgical protocols(Table 1). The results from these studies indicatethat ridge contraction following tooth extractioncan be diminished when combined with socketgrafts and/or the use of mechanical barriers. Exper-imental studies in a dog model (6, 9) have demon-strated that placement of bone substitutes in thefresh extraction socket failed to inhibit the pro-cesses of modeling and remodeling that took placein the socket walls following tooth extraction. Theauthors observed, however, that the graft supportedde novo hard-tissue formation, in particular in thecortical region of the extraction site, and thedimension and profile of the alveolar ridge was bet-ter preserved. The authors concluded that theplacement of a biomaterial in an extraction socketmay modify modeling and compensate for the buc-cal bone loss. The histological observationsdescribed above were confirmed by a recent ran-domized clinical trial (12) that evaluated radio-graphically the dimensional alterations of thealveolar ridge at socket sites grafted with anorganicbovine bone. The authors observed that after

4 months of healing, the buccal bone wall at thegrafted socket sites was markedly reduced inheight. On the other hand, the cross-sectional areaof the grafted sites exhibited a reduction of only3% of their initial dimensions, whilst in the non-grafted sites, the corresponding reduction was 25%.

It has been well established in the literature thatimmediate implant placement in fresh extractionsockets fails to prevent bone modeling and thusmaintains the original shape of the ridge (3–5, 18, 33,36, 73). The use of hard- or soft-tissue grafts withimmediate implant placement to prevent ridgereduction has been evaluated in various clinical andexperimental studies (11, 25–28, 37, 64, 78). In thesestudies, the hard-tissue graft, mainly a bone substi-tute, was placed in the space between the implantsurface and the inner surface of the buccal bone wall,whilst the soft-tissue graft was adapted to the outersurface of the bone wall. The findings from thesereports demonstrate that graft procedures, combinedwith implant placement, may counteract ridge altera-tions following tooth extraction.

In summary, there are four fundamental learningsfrom current knowledge of the socket-healing pro-cess. First, a relatively thin buccal bone wall at theanterior maxillary region characterizes the alveolarsocket. Such a thin bony wall provides the frameworkfor the outline of the buccal aspect of the alveolarprocess. Second, the buccal bone wall will eventuallybe resorbed following tooth extraction. Followingbuccal bone resorption, the soft tissue collapses intothe socket, creating a ridge defect. Third, the immedi-ate placement of an implant does not prevent buccalbone loss, nor, indeed, does a socket graft with vari-ous biomaterials. In contrast, grafting sockets limitsthe collapse of the soft tissues into the healing alveo-lar socket and, at the same time, supports bone for-mation. Thus, the preservation of the ridgedimension occurs as a compensatory mechanism forthe buccal bone loss. Finally, tooth extraction, onceconsidered a simple and straightforward surgical pro-cedure, should be performed with the understandingthat ridge reduction will follow and thus further clini-cal steps should be considered to compensate forsuch a change when considering future reconstruc-tion or replacement of the extracted tooth.

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131

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Alveolar socket healing: what can we learn

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