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

& Sons A/S. Published by John Wiley & Sons Ltd


Printed in Singapore. All rights reserved PERIODONTOLOGY 2000

Alveolar socket healing: what can


we learn?
 O , C L EV
M A U R I C I O G. A R A UJ ^ ICA MISAWA & FLAVIA
 E R S O N O. S I L V A , M ON
SUKEKAVA

In current dentistry, the healing process of the Anatomic considerations


socket following tooth extraction has become an
important topic of research, study and discussion. The alveolar process may be defined as the bone tis-
The reason for this relies mainly on the fact that sue that surrounds a fully erupted tooth and it is
after tooth extraction several changes can occur in formed in harmony with the development and erup-
the alveolar process, which may prevent or render tion of the teeth (Fig. 1). It is limited coronally by the
difficult implant installation in a prosthetically dri- bone margins of the socket walls, whilst an imaginary
ven position (23). In addition, the increasing line that cuts the bottom of the socket in a perpendic-
demand for esthetics in dentistry highlights the ular direction to the long axis of the root, limits it api-
importance of maintaining adequate ridge volume cally. Beyond such a line, the basal bone of the
in order to achieve a long-term esthetically accept- mandible or the maxilla can be found.
able implant-support prosthesis (42). Thus, it is The morphologic characteristics of the alveolar
increasingly expected that the results of the healing process are related to: (i) the size and shape of the
process should promote the formation of an alveo- tooth; (ii) the site of tooth eruption; and (iii) the incli-
lar ridge with a sufficient volume of hard and soft nation of the erupted tooth. In general, teeth tend to
tissues to allow an ideal implant-supported restor- erupt and incline to a position outside the center of
ative outcome. the basal bone (62). In a recent clinical study, Janua-
Tooth extraction was once described as a tissue rio et al. (46) described some of the morphological
amputation that may lead to functional, psychologi-
cal, postural and local changes (14). Indeed, tooth
extraction is initially perceived purely as tooth loss,
but local changes arise and promote hard- and
soft-tissue alterations. The process of local changes
that take place in order to close the wound and
restore 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 healing
process that may improve the treatment outcome.

The alveolar process


In order to understand the socket-healing process
and its clinical implications, it is pivotal to know the
characteristics of the tissues that comprise the alveo-
lar process. Thus, a brief anatomic and histologic
Fig. 1. Cone-beam tomographic image representing the
description of such tissues is provided below (for alveolar process at the maxillary lateral incisor region. The
detailed review, see 7, 65). alveolar process is the bone that surrounds the root.

122
Alveolar socket healing

features of the alveolar process in the anterior maxilla thickness at the anterior front tooth region. Thus,
in humans. The authors included 250 periodontally most of the thin buccal bone wall is a tooth-depen-
healthy subjects, 17–66 years of age. Cone beam com- dent structure (Fig. 3).
puted tomograms were obtained from the maxillary
front teeth. Measurements of the thickness of the
buccal bone plate of the alveolar process were per- Socket healing
formed at three different positions in relation to the
buccal bone crest (i.e. at distances of 1, 3 and 5 mm
Dimensional changes
apical to the crest). The measurements demonstrated
that the buccal bone plate in most locations, in all The dimensional changes that occur in the alveolar
anterior tooth sites examined, was ≤1 mm thick (aver- ridge following tooth extraction have been reported
age thickness ~0.5 mm) and that close to 50% of sites in several human studies (14, 16, 47, 48, 62, 63, 66, 74)
had a bone plate thickness that was ≤0.5 mm. In con- and were determined using different methodologies,
clusion, tooth sites in the anterior maxilla have a thin including clinical, cast model and radiographic exam-
buccal bone wall (Fig. 2), which probably contributes inations. After multiple tooth extractions and the use
to its loss following tooth extraction. of complete removable prostheses, the alveolar ridge
undergoes marked contraction in both vertical and
horizontal directions (13, 14, 32, 47, 48). Following
Histologic considerations several years of full denture use, individuals may
undergo a wide variation in alveolar ridge reduction
The inner portion of socket walls is named “alveolar and some may exhibit a fully resorbed alveolar ridge
bone proper” or bundle bone (a histological term) (16). Following single-tooth extraction, the ridge
and the remaining hard structure is called “alveolar exhibits a limited reduction in its vertical dimension,
bone”. The bundle bone is a lamellar bone, 0.2– but the horizontal reduction is substantial (Fig. 4; 62,
0.4 mm wide (65), composed of circumferential 63). It can be expected that: (i) up to 50% reduction of
lamellae, whilst the alveolar bone is also of the lamel- the original ridge width will occur; (ii) the amount of
lar type but composed of concentric and interstitial
lamellae and of marrow. In the bundle bone, the
Sharpey’s fibers are invested in such way that they
connect the periodontal ligament to the alveolar bone
and skeleton. Likewise, on the contralateral side of
the periodontal ligament, the dental cementum
invested with Sharpey’s fibers connects the periodon-
tal ligament to the dentin. As with root cementum
and the periodontal ligament, the bundle bone is a
tooth-dependent structure. Overall, the bundle bone
and the buccal bone plate frequently exhibit a similar

Fig. 3. Buccal–lingual section illustrating the most coronal


Fig. 2. Occlusal view of a dried skull specimen. Note the portion of the buccal bone wall. The buccal wall is made
limited thickness of the buccal bone wall at the central mainly by bundle bone. Polarized light. Toluidine blue
incisor regions. stain; original magnification 3 50.

123
Alveolar socket healing

provisional matrix. Subsequently, the provisional among individuals (32, 74). In a recent study, Lindhe
matrix is penetrated by several vessels and bone- et al. (54) examined the tissue composition of biop-
forming cells, and finger-like projections of woven sies from 36 individuals retrieved from previous
bone are laid down around the blood vessels. Eventu- socket sites in the posterior maxilla after >16 weeks of
ally, the projections completely surround a vessel and healing. The authors reported that about 60–65% of
the primary osteon is thus formed (Fig. 6). The pri- the tissue volume was made up of lamellar bone and
mary osteons may be occasionally reinforced by bone marrow. Thus, the complete remodeling of the
parallel-fibered bone. Woven bone can be identified woven bone into lamellar bone and bone marrow
in the healing socket as early as 2 weeks after tooth may take several months or years.
extraction and remains in the wound for several The resorption of the socket walls was studied in
weeks. Woven bone is a provisional type of bone biopsies obtained from human samples (32) and from
without any load-bearing capacity and therefore a series of studies in dogs (3–6, 10). A few weeks after
needs to be replaced with mature bone types (lamel- tooth removal, osteoclasts could be found around the
lar bone and bone marrow). crest of both buccal and lingual walls and on the
outer and inner (bundle bone) portions of the socket
Bone modeling and remodeling phase
(Fig. 7). Bone modeling takes place equally on buccal
Bone modeling and remodeling is the third and last and lingual walls, but because the lingual bone is usu-
phase of the socket-healing process. Bone modeling ally wider than the buccal bone wall, modeling results
is defined as a change in the shape and architecture in greater vertical bone loss at the thin buccal plate
of the bone, whereas bone remodeling is defined as a than at the wide lingual wall. In addition, bone mod-
change without concomitant change in the shape and eling takes place earlier than bone remodeling, in
architecture of the bone. The replacement of woven such way that about two-thirds of the modeling pro-
bone with lamellar bone or bone marrow is bone cess occurs in the first 3 months of healing (66). In
remodeling, whereas the bone resorption that takes summary, modeling and remodeling processes during
place on the socket walls leading to a dimensional socket healing result in qualitative and quantitative
alteration of the alveolar ridge is the result of bone changes at the edentulous site, which culminate in a
modeling. Bone remodeling in humans may take sev- reduction of the dimension of the ridge.
eral months and exhibits substantial variability

Fig. 7. Buccal–lingual section of the socket wall a few


months following tooth extraction. Note the intense mod-
Fig. 6. Micrograph illustrating primary osteons in the eling and remodeling process characterized by the pres-
healing socket. The collagen fibers have a woven organiza- ence of bone multicellular units and reversal lines.
tion. Toluidine blue stain; original magnification 3 100. Ladewig fibrin stain; original magnification 3 20.

125
Alveolar socket healing

provisional matrix. Subsequently, the provisional among individuals (32, 74). In a recent study, Lindhe
matrix is penetrated by several vessels and bone- et al. (54) examined the tissue composition of biop-
forming cells, and finger-like projections of woven sies from 36 individuals retrieved from previous
bone are laid down around the blood vessels. Eventu- socket sites in the posterior maxilla after >16 weeks of
ally, the projections completely surround a vessel and healing. The authors reported that about 60–65% of
the primary osteon is thus formed (Fig. 6). The pri- the tissue volume was made up of lamellar bone and
mary osteons may be occasionally reinforced by bone marrow. Thus, the complete remodeling of the
parallel-fibered bone. Woven bone can be identified woven bone into lamellar bone and bone marrow
in the healing socket as early as 2 weeks after tooth may take several months or years.
extraction and remains in the wound for several The resorption of the socket walls was studied in
weeks. Woven bone is a provisional type of bone biopsies obtained from human samples (32) and from
without any load-bearing capacity and therefore a series of studies in dogs (3–6, 10). A few weeks after
needs to be replaced with mature bone types (lamel- tooth removal, osteoclasts could be found around the
lar bone and bone marrow). crest of both buccal and lingual walls and on the
outer and inner (bundle bone) portions of the socket
Bone modeling and remodeling phase
(Fig. 7). Bone modeling takes place equally on buccal
Bone modeling and remodeling is the third and last and lingual walls, but because the lingual bone is usu-
phase of the socket-healing process. Bone modeling ally wider than the buccal bone wall, modeling results
is defined as a change in the shape and architecture in greater vertical bone loss at the thin buccal plate
of the bone, whereas bone remodeling is defined as a than at the wide lingual wall. In addition, bone mod-
change without concomitant change in the shape and eling takes place earlier than bone remodeling, in
architecture of the bone. The replacement of woven such way that about two-thirds of the modeling pro-
bone with lamellar bone or bone marrow is bone cess occurs in the first 3 months of healing (66). In
remodeling, whereas the bone resorption that takes summary, modeling and remodeling processes during
place on the socket walls leading to a dimensional socket healing result in qualitative and quantitative
alteration of the alveolar ridge is the result of bone changes at the edentulous site, which culminate in a
modeling. Bone remodeling in humans may take sev- reduction of the dimension of the ridge.
eral months and exhibits substantial variability

Fig. 7. Buccal–lingual section of the socket wall a few


months following tooth extraction. Note the intense mod-
Fig. 6. Micrograph illustrating primary osteons in the eling and remodeling process characterized by the pres-
healing socket. The collagen fibers have a woven organiza- ence of bone multicellular units and reversal lines.
tion. Toluidine blue stain; original magnification 3 100. Ladewig fibrin stain; original magnification 3 20.

125
 jo et al.
Arau

Stimulating factors (62), but it becomes more critical in the anterior


region as a result of esthetic demands. The anterior
The initial healing responses in a wound are regulated maxillary region exhibits very thin socket walls (19,
by signaling molecules (i.e. growth factors and cyto- 46) that are frequently made up of only bundle
kines), such as platelet-derived growth factor, insulin- bone. As the bundle bone is a tooth-dependent
like growth factors, transforming growth factor-beta structure, it is gradually resorbed following exodon-
and fibroblastic growth factors. They initiate cell tia. Finally, the postextraction ridge reduction
migration, differentiation and proliferation as they appears to be related to several factors, including
interact with each other in highly ordered temporal surgical trauma, lack of a functional stimulus on the
and spatial sequences (53). These growth factors act bone walls, lack of bundle bone and periodontal lig-
as mitogenic and angiogenic signals at the early stage ament and genetic information.
of bone healing. Once activated, growth factors insti- Tooth extraction is a traumatic procedure and, dur-
gate a series of events via ligand–receptor interac- ing its course, the soft tissues are disrupted, the vas-
tions, including signal transduction, gene cular structures of the periodontal ligament are
transcription, mRNA-directed protein biosynthesis damaged or destroyed and the principal fibers of the
and secretion of post-translational proteins (44). periodontal ligament are severed (29). In addition, it
Few studies have examined the roles of growth fac- is well established in the dental literature that the ele-
tors and cytokines during socket healing (40, 74). vation of a full-thickness flap, in order to gain access
Fisher et al. (40) evaluated the expression of growth to the root, may cause resorption of thin bone walls
factors during socket-healing events in a rabbit (50, 75–77; for reviews see 43, 70). However, different
model. The authors observed that: (i) fibroblast animal and clinical studies have failed to support the
growth factor-2 presented at higher levels at early concept that tooth extraction without flap elevation
time points, before returning to lower levels; (ii) vas- prevents ridge reduction (8, 17, 33, 39). These studies
cular endothelial growth factor levels were main- indicate that the surgical trauma promoted by the
tained constant during healing; (iii) platelet-derived removal of the tooth itself overlaps with the surgical
growth factor-A levels increased during the first days trauma promoted by the elevation of a full-thickness
of socket healing; (iv) transforming growth factor- flap.
beta1 presented a small elevation at early time points; The surgical trauma caused by tooth extraction
and (v) an increased expression of bone morphoge- may be limited by minimally invasive surgical proce-
netic protein 2 was observed when osteoblast precur- dures (58). Such procedures aim to prevent expansion
sors accumulated and began to proliferate. Trombelli of the socket housing, which otherwise may fracture
et al. (63) studied modeling and remodeling of the thin adjacent bony walls. For this purpose, the
human extraction sockets and evaluated the expres- use of forceps to luxate the tooth by applying forces
sion of bone morphogenetic protein 7 during socket toward the buccal palatal/lingual aspects of the
healing. The results demonstrated that bone morpho- socket is not recommended. Likewise, the forceps
genetic protein 7 increased during early and interme- should not perform rotational movements, as the
diate healing phases, and a period of increased bone cross-section shape of a root is seldom circular. Sev-
modeling and remodeling activity occurred, leading eral new surgical instruments, which promote mini-
to the deposition of woven bone from provisional mally invasive tooth extraction, are currently
matrix. In summary, growth factors present multiple commercially available. Periotomes and vertical
activities, generally with overlapping actions, and a tooth-extraction systems are among the instruments
simplistic characterization of their effects is not possi- most frequently used for this purpose. Periotomes are
ble, or indeed appropriate. instruments designed to sever the periodontal liga-
ment fibers at the mesial and distal aspects of the
socket, in order to facilitate and improve the effi-
What can we learn? ciency of root elevators. Vertical tooth-extraction sys-
tems are, on the other hand, designed to pull roots in
There are several lessons to be learned from the a vertical direction and hence avoid any damage to
various reports of local changes following tooth the socket walls. In both techniques described above,
extraction. The healed socket eventually fills with no pressure is applied to the buccal socket wall; how-
newly formed bone and the alveolar ridge contracts. ever, such techniques are efficient only for conical or
The ridge reduction is larger in the molar region straight roots.

126
Table 1. Clinical studies that evaluated grafting sockets with different materials and mechanical barriers to prevent alveolar ridge reduction following tooth extraction

Authors n Material Method of Follow-up Outcome


evaluation

Camargo et al. 16 patients32 Bioactive glass (test) vs. extraction Clinical 6 months Change in ridge width (test: 3.48  2.68 mm;
(24) sockets alone (control) control: 3.06  2.41 mm)
Change in ridge height (test: 0.38  3.18 mm;
control: 1.00  2.25 mm)
No difference between groups
Iasella et al. (45) 24 patients24 Tetracycline hydrated FDBA (test) vs. Clinical and 4–6 months Change in ridge width (test: from 9.2  1.2 mm to
sockets extraction alone (control) histologic 8.0  1.4 mm; control: from 9.1  1.0 mm to
6.4  2.2 mm)
Change in ridge height (test: 1.3  2.0 mm; control:
0.9  1.6 mm)
FDBA improved ridge height and width dimensions
compared with extraction alone
Serino et al. (67) 36 patients Polylactide and polyglycolide sponge Clinical and 6 months Change in ridge height (test: 0.2  1.5 mm; control:
39 sockets (test) vs. extraction alone (control) histologic 0.7  1.2 mm)
Test group may preserve or reduce alveolar bone
resorption
Luczyszyn et al. 15 patients Acellular dermal matrix and resorbable Clinical and 6 months Ridge width (test: 6.8  1.26 mm; control:
(55) 30 sockets hydroxyapatite (test) vs. acellular histologic 5.53 + 1.06 mm)
dermal matrix alone (control) Acellular dermal matrix was able to preserve ridge
thickness and the additional use of resorbable
hydroxyapatite favored preservation of the ridges
Barone et al. (15) 40 patients Corticocancellous porcine bone (test) Clinical and 7 months Change in ridge width (test: 2.5  1.2 mm; control:
40 sockets vs. extraction alone (control) histologic 4.3  0.8 mm)
Change in ridge height (test: 0.7  1.4 mm; control:
3.6  1.5 mm)
Test group limited resorption
Cardaropoli & 10 patients Bovine bone mineral (case series) Clinical and 4 months Change in ridge width: from 11.8  1.53 mm to
Cardaropoli (30) 10 sockets histologic 9.95  2.31 mm

Neiva et al. (61) 24 patients Putty-form hydroxyapatite matrix Clinical, histologic 16 weeks Change in ridge width (test: 1.31  0.96 mm; control:
24 sockets combined with the synthetic cell- and radiographic 1.43  1.05 mm)
binding peptide P-15 (test) vs. Change in ridge height (test: 0.15  1.76 mm; control:
extraction alone (control) 0.56  1.04 mm)
A favorable response was observed when putty P15 was
applied to extraction sockets

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Alveolar socket healing
Table 1. (Continued)
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128
Authors n Material Method of Follow-up Outcome
evaluation
 jo et al.

Mardas et al. (56) 26 patients B-TCP (test) vs. bovine bone mineral Clinical and 8 months Change in ridge width (test: 1.1  1.0 mm; control:
26 sockets (control) histologic 2.1  1.0 mm)
Change in ridge height (test: 0.4  0.5 mm; control:
0.1  0.7 mm)
No difference between groups
Fernandes et al. 18 patients Acellular dermal matrix and anorganic Clinical 6 months Change in ridge width (test: 2.53  1.81 mm; control:
(38) bone matrix cell-binding peptide P-15 3.40  1.39 mm)
(test) vs. acellular dermal matrix alone Change in buccal crest height (test: 1.20  2.02 mm;
control: 1.50  1.15 mm)
No difference between groups
Nam et al. (59) 42 patients Synthetic oligopeptide-coated bone Clinical and 6 months Change in ridge width (test: 1.2  1.5 mm; control:
44 sockets mineral (test) vs. bone graft without histologic 1.3  1.4 mm)
peptide (control) Change in buccal crest height (test: 2.3  3.6 mm;
control: 2.3  2.1 mm)
No difference between groups
Brkovic et al. (20) 20 patients B-TCP/type I collagen cones with (test) Clinical and 9 months Change in ridge width (test: from 7.39  2.00 mm to
20 sockets or without (control) a barrier histologic 6.53  1.83 mm; control: from 7.88  2.33 mm to
membrane 6.59  2.44 mm)
Change in ridge height (test: from 3.00  1.85 mm to
3.38  1.94 mm; control: from 3.00  1.25 mm to
3.22  1.48 mm)
No difference between groups
Mardas et al. (57) 27 patients B-TCP (test) vs. bovine bone mineral Radiographic 32 weeks Changes in ridge hight (test group:
27 sockets (control) M side 0.9  1.2 mm; D side 0.7  1.8 mm;
control group: M side 0.4  1.3 mm; D side
0.7  1.3 mm)
No difference between groups
Kim et al. (51) 20 patients Collagen sponge and xenogeneic bone Histologic 3 months Resorption in ridge width (test: 14.26%; control:
20 sockets grafts (test) vs. extraction alone 20.74%)
(control) Xenograft prevents the horizontal resorption of the
alveolar ridge, and the upper collagen sponge blocks
the infiltration of soft tissues to the lower area
Kutkut et al. (52) 16 patients Calcium sulfate hemihydrate and Clinical and 3 months Change in ridge width (test: 1.7  1.4 mm;
16 sockets platelet-rich plasma (test) vs. collagen histologic control: 1.7  1.6 mm)
resorbable plug (control) Change in ridge height (test: 0.2  0.9 mm; control:
1.0  0.8 mm)
No difference between groups
Table 1. (Continued)

Authors n Material Method of Follow-up Outcome


evaluation

Brownfield & 17 patients Osteoinductive demineralized bone Clinical, histologic, 10–12 weeks Change in ridge width (test: 1.00  0.40 mm;
Weltma (21) 20 sockets matrix with cancellous bone chips radiographic and control: 1.30  1.00 mm)
(test) vs. extraction alone (control) tomographic Change in ridge height (test: 0.80  1.20 mm;
control: 1.20  0.40 mm)
No difference between groups
Gholami et al. 12 patients Synthetic nanocrystalline Clinical and 6–8 months The width in test group 2 decreased from
(41) 28 sockets hydroxyapatite (test group 1) X bovine histologic 7.75  1.55 mm to 6.68  1.85 mm and in test group
bone mineral (test group 2) 1 decreased from 7.36  1.94 mm to 6.43  2.08 mm
No difference between groups
Toloue et al. (72) 21 patients Calcium sulfate (test) vs. FDBA Clinical and 3 months Change in ridge width (test: 1.33  1.22 mm;
31 sockets (control) histologic control: 1.03  0.87 mm)
Change in ridge height (test: 0.32  1.69 mm;
control: 0.05  1.46 mm)
No difference between groups
Cardaropoli et al. 41 patients Bovine bone mineral (test) vs. Clinical and 4 months The test group showed less reduction in ridge width
(31) 48 sockets extraction alone (control) histologic (1.04  1.08 mm vs. 4.48  0.65 mm) and height
(0.46  0.46 mm vs. 1.54  0.33 mm)
Bovine bone mineral considerably limits the amount of
horizontal and vertical bone resorption
Cook & Mealey 44 patients Bovine xenograft (test group 1) vs. Clinical and 21 weeks Change in buccal ridge height (test group 1:
(35) 44 sockets sponge composed of 70% type I histologic 0.14  2.21 mm; test group 2: 0.03  2.81 mm)
bovine collagen coated with 30% Change in lingual ridge height (test group 1:
nonsintered hydroxyapatite (test 0.21  3.04 mm; test group 2: 1.18  1.93 mm)
group 2) Change in ridge width (test group 1: 1.57  1.21 mm/
test group 2: 1.16  1.44 mm)
No significant difference between groups
Clozza et al. (34) 13 patients Bioactive glass (case series) Tomographic 3 months Preservation of about 77% of the original width
32 teeth dimensions
The bone loss in width was 1.8  1.1 mm; vertical
bone loss was 2.7  1.1 mm

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Alveolar socket healing
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130
Table 1. (Continued)
 jo et al.

Authors n Material Method of Follow-up Outcome


evaluation

Jung et al. (49) 40 patients Beta-tricalcium phosphate particles Tomographic 6 months Vertical changes ranged between 0.6 mm ( 10.2%)
40 sockets (test group 1) vs. bovine bone mineral for control and a gain of 0.3 mm (5.6%) for test group
covered with a collagen matrix (test 3 on the lingual side, and between 2.0 mm ( 20.9%)
group 2) vs. DBBM-C covered with an for beta-tricalcium phosphate and a gain of 1.2 mm
autogenous soft-tissue graft (test (8.1%) for test group 3 on the buccal side
group 3) vs. spontaneous healing The most accentuated ridge width changes were
(control) recorded 1 mm below the crest: 3.3 mm ( 43.3%,
control), 6.1 mm ( 77.5%, beta-tricalcium
phosphate), 1.2 mm ( 17.4%, test group 2) and
1.4 mm ( 18.1%, test group 3)
DBBM-C covered with CM or autogenous soft-tissue
graft, resulted in reduced vertical and horizontal
changes
Shakibaie-M (68) 10 patients Bovine bone material (test group 1) vs. Clinical and 12–14 weeks Alveolar ridge width reduction (test group 1 = 0.5 mm;
32 sockets or hydroxyapatite and silicon dioxide histologic test group 2 = 1.5 mm; control = 2.0 mm)
(test group 2) vs. stypro gelatin sponge Alveolar ridge height reduction (test group 1 = 1.0 mm;
(control) test group 2 = 1.5 mm; control = 2.0 mm)
Fixed gingiva width reduction (test group 1 = 0.5 mm;
test group 2 = 2.4 mm; control = 2.5 mm)
Bovine xenograft resulted in better bone quality and
quantity
Thalmair et al. 30 patients Prehydrated collagenated cortico- Clinical 4 months All groups displayed contour shrinkage at the
(71) 30 sockets cancellous porcine bone and free buccal aspect ranging from a mean horizontal
gingival graft (test group 1) vs. free reduction of 0.8  0.5 mm (test group 1) to
gingival graft alone (test group 2) vs. 2.3  1.1 mm (control)
xenogenic bone substitute (test group Free gingival graft limited the contour shrinkage
3) vs. extraction alone (control)
Arau
 jo et al. (12) 28 patients Bovine bone mineral (test) vs. Tomographic 4 months Bovine bone mineral counteracted the reduction in
28 sockets extraction alone (control) hard tissue
Reduction in hard tissue was 3% in the test group
compared with 25% in the control.
FDBA, freeze-dried bone allograft; B-TCP, beta- tricalcium phosphate; M side, mesial side; D side, distal side; DBBM-C, bovine bone mineral; CM, collagen matrix.
Alveolar socket healing

Teeth provide support for very thin bone walls, 4 months of healing, the buccal bone wall at the
although fenestrations and dehiscence may occur grafted socket sites was markedly reduced in
naturally when the bone thickness is below a certain height. On the other hand, the cross-sectional area
threshold (65). It is suggested, however, that implants of the grafted sites exhibited a reduction of only
should be provided with bone walls about 1- to 2- 3% of their initial dimensions, whilst in the non-
mm-wide on buccal and lingual aspects to allow a grafted sites, the corresponding reduction was 25%.
stable bone height to be maintained (22, 42). The rea- It has been well established in the literature that
sons why teeth can support thin bone walls, and why immediate implant placement in fresh extraction
implants seem to fail to do so, remains obscure. It has sockets fails to prevent bone modeling and thus
been suggested, however, that the presence of bundle maintains the original shape of the ridge (3–5, 18, 33,
bone and periodontal ligament around teeth are 36, 73). The use of hard- or soft-tissue grafts with
likely explanations. Bundle bone is capable of existing immediate implant placement to prevent ridge
in thinner dimensions than are alveolar or basal reduction has been evaluated in various clinical and
bones because the periodontal ligament provides the experimental studies (11, 25–28, 37, 64, 78). In these
functional stimulus as well as the nutritional and cel- studies, the hard-tissue graft, mainly a bone substi-
lular source for its maintenance. tute, was placed in the space between the implant
It is now well established that following tooth surface and the inner surface of the buccal bone wall,
extraction the ridge crest moves toward the long axis whilst the soft-tissue graft was adapted to the outer
of the basal bone (16, 63). The shape of the jawbone surface of the bone wall. The findings from these
appears to return to the shape that was present prior reports demonstrate that graft procedures, combined
to the development of the alveolar process during with implant placement, may counteract ridge altera-
tooth eruption. The lack of a functional stimulus on tions following tooth extraction.
the bone walls and the need for tissue adjustment to In summary, there are four fundamental learnings
meet “genetically” determined demands regarding from current knowledge of the socket-healing pro-
ridge geometry in the absence of teeth (2) may cess. First, a relatively thin buccal bone wall at the
explain this modification. anterior maxillary region characterizes the alveolar
Grafting sockets with different materials, and the socket. Such a thin bony wall provides the framework
use of mechanical barriers, have been proposed to for the outline of the buccal aspect of the alveolar
prevent alveolar ridge reduction, secondary to bone process. Second, the buccal bone wall will eventually
modeling. Clinical studies have been performed to be resorbed following tooth extraction. Following
evaluate the outcome of such surgical protocols buccal bone resorption, the soft tissue collapses into
(Table 1). The results from these studies indicate the socket, creating a ridge defect. Third, the immedi-
that ridge contraction following tooth extraction ate placement of an implant does not prevent buccal
can be diminished when combined with socket bone loss, nor, indeed, does a socket graft with vari-
grafts and/or the use of mechanical barriers. Exper- ous biomaterials. In contrast, grafting sockets limits
imental studies in a dog model (6, 9) have demon- the collapse of the soft tissues into the healing alveo-
strated that placement of bone substitutes in the lar socket and, at the same time, supports bone for-
fresh extraction socket failed to inhibit the pro- mation. Thus, the preservation of the ridge
cesses of modeling and remodeling that took place dimension occurs as a compensatory mechanism for
in the socket walls following tooth extraction. The the buccal bone loss. Finally, tooth extraction, once
authors observed, however, that the graft supported considered a simple and straightforward surgical pro-
de novo hard-tissue formation, in particular in the cedure, should be performed with the understanding
cortical region of the extraction site, and the that ridge reduction will follow and thus further clini-
dimension and profile of the alveolar ridge was bet- cal steps should be considered to compensate for
ter preserved. The authors concluded that the such a change when considering future reconstruc-
placement of a biomaterial in an extraction socket tion or replacement of the extracted tooth.
may modify modeling and compensate for the buc-
cal bone loss. The histological observations
described above were confirmed by a recent ran- References
domized clinical trial (12) that evaluated radio-
graphically the dimensional alterations of the 1. Amler MH. The time sequence of tissue regeneration in
alveolar ridge at socket sites grafted with anorganic human extraction wounds. Oral Surg Oral Med Oral Pathol
1969: 27: 309–318.
bovine bone. The authors observed that after

131
 jo et al.
Arau

2. Arau jo MG, Lindhe J. Dimensional ridge alterations follow- 20. Brkovic BM, Prasad HS, Rohrer MD, Konandreas G, Agro-
ing tooth extraction. An experimental study in the dog. J giannis G, Antunovic D, Sa ndor GK. Beta-tricalcium phos-
Clin Periodontol 2005: 32: 212–218. phate/type I collagen cones with or without a barrier
3. Arau jo MG, Sukekava F, Wennstro € m JL, Lindhe J. Ridge membrane in human extraction socket healing: clinical,
alterations following implant placement in fresh extraction histologic, histomorphometric, and immunohistochemical
sockets: an experimental study in the dog. J Clin Periodon- evaluation. Clin Oral Investig 2012: 16: 581–590.
tol 2005: 32: 645–652. 21. Brownfield LA, Weltman RL. Ridge preservation with or
4. Arau jo MG, Wennstro € m JL, Lindhe J. Modeling of the lin- without an osteoinductive allograft: a clinical, radiographic,
gual bone walls of fresh extraction sites following implant micro-computed tomography, and histologic study evaluat-
installation. Clin Oral Impl Res 2006: 17: 606–614. ing dimensional changes and new bone formation of the
5. Arau jo MG, Sukekava F, Wennstro € m JL, Lindhe J. Tissue alveolar ridge. J Periodontol 2012: 83: 581–589.
modeling following implant placement in fresh extaction 22. Buser D, von Arx T, ten Bruggenkate C, Weingart D. Basic
sockets. Clin Oral Impl Res 2006: 17: 615–624. surgical principles with ITI implants. Clin Oral Impl Res
6. Arau jo MG, Linder E, Wennstro € m JL, Lindhe J. The influ- 2000: 11(Suppl): 59–68.
ence of Bio-Oss collagen on healing of an extraction socket: 23. Buser D, Martin W, Belser UC. Optimizing esthetics for
an experimental study in the dog. Int J Periodontics Restor- implant restorations in the anterior maxilla: anatomic and
ative Dent 2008: 28: 123–135. surgical considerations. Int J Oral Maxillofac Implants 2004:
7. Arau jo MG, Lindhe J. The edentulous alveolar ridge. In: 19(Suppl): 43–61.
Lindhe J, Lang NP, Thorkild K, editors. Clinical periodontol- 24. Camargo PM, Lekovic V, Weilaender M, Klokkevold PR,
ogy and implant dentistry. Oxford: Blackwell Munksgaard, Kenney EB, Dimitrijevic B, Nedic M, Jancovic S, Orsini M.
2008: 50–68. Influence of bioactive glass on chages in alveolar process
8. Arau jo MG, Lindhe J. Ridge alterations following tooth dimensions after exodontias. Oral Surg Oral Med Oral
extraction with and without flap elevation. An experimental Pathol Oral Radiol Endod 2000: 90: 581–586.
study in the dog. Clin Oral Impl Res 2009: 20: 545–549. 25. Caneva M, Botticelli D, Stellini E, Souza SL, Salata LA, Lang
9. Arau jo MG, Lindhe J. Ridge preservation with the use of NP. Magnesium-enriched hydroxyapatite at immediate
Bio-Oss collagen: a 6-month study in the dog. Clin Oral implants: a histomorphometric study in dogs. Clin Oral
Impl Res 2009: 20: 433–440. Implants Res 2011: 22: 512–517.
10. Arau jo MG, Linder E, Lindhe J. Effect of a xenograft on early 26. Caneva M, Botticelli D, Morelli F, Cesaretti G, Beolchini M,
bone formation in extraction sockets: an experimental Lang NP. Alveolar process preservation at implants installed
study in dog. Clin Oral Impl Res 2009: 20: 1–6. immediately into extraction sockets using deproteinized
11. Arau jo MG, Linder E, Lindhe J. Bio-Oss collagen in the buc- bovine bone mineral – an experimental study in dogs. Clin
cal gap at immediate implants: a 6-month study in the dog. Oral Implants Res 2012: 23: 789–796.
Clin Oral Implants Res. 2011: 22: 1–8. 27. Caneva M, Botticelli D, Pantani F, Baffone GM, Rangel IG
12. Arau jo MG, da Silva JC, de Mendoncßa AF, Lindhe J. Ridge Jr, Lang NP. Deproteinized bovine bone mineral in mar-
alterations following grafting of fresh extraction sockets in ginal defects at implants installed immediately into extrac-
man. A randomized clinical trial. Clin Oral Implants Res tion sockets: an experimental study in dogs. Clin Oral
2014. doi: 10.1111/clr.12366 [Epub ahead of print]. Implants Res 2012: 23: 106–112.
13. Atwood DA. Some clinical factors related to the rate of 28. Caneva M, Botticelli D, Vigano  P, Morelli F, Rea M, Lang
resorption of residual ridges. J Prosthet Dent 1962: 12: 441– NP. Connective tissue grafts in conjunction with implants
450. installed immediately into extraction sockets. An experi-
14. Atwood DA. Postextraction changes in the adult mandible mental study in dogs. Clin Oral Implants Res 2013: 24: 50–
as illustrate by microradiographs of midsagittal section and 56.
serial cephalometric roentgenograms. J Prosthet Dent 1963: 29. Cardaropoli G, Arau  jo MG, Lindhe J. Dynamics of bone tis-
13: 810–824. sue formation in tooth extraction sites. An experimental
15. Barone A, Aldini NN, Fini M, Giardino R, Calvo Guirado JL, study in dogs. J Clin Periodontol 2003: 30: 809–818.
Covani U. Xenograft versus extraction alone for ridge pres- 30. Cardaropoli D, Cardaropoli G. Preservation of the postex-
ervation after tooth removal: a clinical and histomorpho- traction alveolar ridge: a clinical and histologic study. Int J
metric study. J Periodontol 2008: 79: 1370–1377. Periodontics Restorative Dent 2008: 28: 469–477.
16. Bergman B, Carlsson GE. Clinical long-term study of com- 31. Cardaropoli D1, Tamagnone L, Roffredo A, Gaveglio L,
plete denture wearers. J Prosthet Dent 1985: 53: 56–61. Cardaropoli G. Socket preservation using bovine bone min-
17. Blanco J, Nunez V, Aracil L, Munoz F, Ramos I. Ridge altera- eral and collagen membrane: a randomized controlled clin-
tions following immediate implant placement in the dog: ical trial with histologic analysis. Int J Periodontics
flap versus flapless surgery. J Clin Periodontol 2008: 35: Restorative Dent 2012: 4: 421–430.
640–648. 32. Carlsson GE, Persson G. Morphologic changes of the man-
18. Botticelli D, Berglundh T, Lindhe J. Hard-tissue alterations dible after extraction and wearing of dentures. A longitudi-
following immediate implant placement in extraction sites. nal, clinical, and X-ray cephalometric study covering
J Clin Periodontol 2004: 31: 820–828. 5 years. Odontologisk Revy 1967: 18: 27–54.
19. Braut V, Bornstein MM, Belser U, Buser D. Thickness of 33. Chen ST, Darby IB, Reynolds EC, Clement JG. Immediate
the anterior maxillary facial bone wall – a retrospective implant placement postextraction without flap elevation. J
radiographic study using cone beam computed tomogra- Periodontol 2009: 80: 163–172.
phy. Int J Periodontics Restorative Dent 2011: 31: 125– 34. Clozza E, Biasotto M, Cavalli F, Moimas L, Di Lenarda R.
131. Three-dimensional evaluation of bone changes following

132
Alveolar socket healing

ridge preservation procedures. Int J Oral Maxillofac tooth extraction: a randomized controlled clinical trial. J
Implants 2012: 4: 770–775. Clin Periodontol 2013: 1: 90–98.
35. Cook DC, Mealey BL. Histologic comparison of healing fol- 50. Karring T, Cumming BR, Oliver RC, Lo €e H. The origin of
lowing tooth extraction with ridge preservation using two granulation tissue and its impact on postoperative results
different xenograft protocols. J Periodontol 2013: 5: 585– of mucogingival surgery. J Periodontol 1975: 46: 577–585.
594. 51. Kim YK, Yun PY, Lee HJ, Ahn JY, Kim SG. Ridge preservation
36. Evans CD, Chen ST. Esthetic outcomes of immediate of the molar extraction socket using collagen sponge and
implant placements. Clin Oral Impl Res 2008: 19: 73–80. xenogeneic bone grafts. Implant Dent 2011: 4: 267–272.
37. Favero G, Lang NP, Romanelli P, Pantani F, Caneva M, Bot- 52. Kutkut A, Andreana S, Kim HL, Monaco E Jr. Extraction
ticelli D. A digital evaluation of alveolar ridge preservation socket preservation graft before implant placement with
at implants placed immediately into extraction sockets: an calcium sulfate hemihydrate and platelet-rich plasma: a
experimental study in the dog. Clin Oral Implants Res 2015: clinical and histomorphometric study in humans. J Period-
26: 102–108. ontol 2012: 4: 401–409.
38. Fernandes PG, Novaes AB Jr, de Queiroz AC, de Souza SL, 53. Lalani Z, Wong M, Brey EM, Mikos AG, Duke PJ. Spatial and
Taba M Jr, Palioto DB, Grisi MF. Ridge preservation with temporal localization of transforming growth factor-beta1,
acellular dermal matrix and anorganic bone matrix cell- bone morphogenetic protein-2, and platelet-derived
binding peptide P-15 after tooth extraction in humans. J Pe- growth factor-A in healing tooth extraction sockets in a rab-
riodontol 2011: 82: 72–79. bit model. J Oral Maxillofac Surg 2003: 61: 1061–1072.
39. Fickl S, Zuhr O, Wachtel H, Bolz W, Huerzeler M. Tissue 54. Lindhe J, Cecchinato D, Bressan EA, Toia M, Arau  jo MG, Lil-
alterations after tooth extraction with and without surgical jenberg B. The alveolar process of the edentulous maxilla in
trauma: a volumetric study in the beagle dog. J Clin Period- periodontitis and non-periodontitis subjects. Clin Oral
ontol 2008: 35: 356–363. Impl Res 2012: 23: 5–11.
40. Fisher JP, Lalani Z, Bossano CM, Brey EM, Demian N, John- 55. Luczyszyn SM, Papalexiou V, Novaes AB Jr, Grisi MFM, Sou-
ston CM, Dean D, Jansen JA, Wong MEK, Mikos AG. Effect za SLS, Taba M Jr. Acellular dermal matrix and hydroxyapa-
of biomaterial properties on bone healing in a rabbit tooth tite in prevention of ridge deformities after tooth
extraction socket model. Part A. J Biomed Mater Res 2004: extraction. Implant Dent 2005: 14: 176–184.
68: 428–438. 56. Mardas N, Chadha V, Donos N. Alveolar ridge preservation
41. Gholami GA, Najafi B, Mashhadiabbas F, Goetz W, Najafi S. with guided bone regeneration and a synthetic bone substi-
Clinical, histologic and histomorphometric evaluation of tute or a bovine-derived xenograft: a randomized, con-
socket preservation using a synthetic nanocrystalline trolled clinical trial. Clin Oral Impl Res 2010: 21: 688–698.
hydroxyapatite in comparison with a bovine xenograft: a 57. Mardas N, D’Aiuto F, Mezzomo L, Arzoumanidi M, Donos
randomized clinical trial. Clin Oral Implants Res 2012: 23: N. Radiographic alveolar bone changes following ridge
1198–1204. preservation with two different biomaterials. Clin Oral
42. Grunder U, Gracis S, Capelli M. Influence of the 3-D bone- Implants Res 2011: 22: 416–423.
to-implant relationship on esthetics. Int J Periodontics 58. Muska E, Walter C, Knight A, Taneja P, Bulsara Y, Hahn M,
Restorative Dent 2005: 25: 113–119. Desai M, Dietrich T. Atraumatic vertical tooth extraction: a
43. Heitz-Mayfield LJA, Trombelli L, Heitz F, Needlemann IG, proof of principle clinical study of a novel system. Oral Surg
Moles DR. A systematic review of the effect of surgical de- Oral Med Oral Pathol Oral Radiol 2013: 116: e303–e310.
bridment vs. non-surgical debridment for the treatment of 59. Nam HW, Park JB, Lee JY, Rhee SH, Lee SC, Koo KT, Kim
chronic periodontitis. J Clin Periodontol 2002: 29: 92–102. TI, Seol YJ, Lee YM, Ku Y, Rhyu IC, Park YJ, Chung CP.
44. Hollinger J, Wong ME. The integrated processes of hard tis- Enhanced ridge preservation by bone mineral bound
sue regeneration with special emphasis on fracture healing. with collagen-binding synthetic oligopeptide: a clinical
Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996: and histologic study in humans. J Periodontol 2011: 82:
82: 594–606. 471–480.
45. Iasella JM, Greenwell H, Miller RL, Hill M, Drisko C, Bohra 60. National Research Council. Committee on animal models
AA, Scheetz JP. Ridge preservation with freeze-dried bone for research on aging. Mammalian models for research on
allograft and a collagen membrane compared to extraction aging, 1st edn. Washington, DC: National Academy Press,
alone for implant development: a clinical and histologic 1980.
study in humans. J Periodontol 2003: 74: 990–999. 61. Neiva RF, Tsao YP, Eber R, Shotwell J, Billy E, Wang HW.
46. Januario AL, Duarte WR, Barriviera M, Mesti JC, Arau  jo MG, Effects of a putty-form hydroxyapatite matrix combined
Lindhe J. Dimension of the facial bone wall in the anterior with the synthetic cell-binding peptide P-15 on alveolar
maxilla: a cone-beam computed tomography study. Clin ridge preservation. J Periodontol 2008: 79: 291–299.
Oral Impl Res 2011: 10: 1168–1171. 62. Pietrokovski J, Massler M. Alveolar ridge resorption follow-
47. Johnson K. A study of the dimensional changes occurring in ing tooth extraction. J Prosthet Dent 1967: 17: 21–27.
the maxilla after tooth extraction. Part I. Normal healing. 63. Pietrokovski J, Starinsky R, Arensburg B, Kaffe I. Morpho-
Aust Dent J 1963: 8: 428–433. logic characteristics of bony edentulous jaws. J Prosthodont
48. Johnson K. A study of the dimensional changes occurring in 2007: 16: 141–147.
the maxilla following tooth extraction. Aust Dent J 1969: 14: 64. Rungcharassaeng K, Kan JY, Yoshino S, Morimoto T, Zimm-
241–244. erman G. Immediate implant placement and provisional-
49. Jung RE, Philipp A, Annen BM, Signorelli L, Thoma DS, ization with and without a connective tissue graft: an
Ha€mmerle CH, Attin T, Schmidlin P. Radiographic evalua- analysis of facial gingival tissue thickness. Int J Periodontics
tion of different techniques for ridge preservation after Restorative Dent 2012: 6: 657–663.

133
 jo et al.
Arau

65. Schroeder HE. The periodontium. Berlin Heidelberg: 72. Toloue SM, Chesnoiu-Matei I, Blanchard SB. A clinical and
Springer-Verlag, 1986. histomorphometric study of calcium sulfate compared with
66. Schropp L, Wenzel A, Kostopoulos L, Karring T. Bone heal- freeze-dried bone allograft for alveolar ridge preservation. J
ing and soft tissue contour changes following single-tooth Periodontol 2012: 83: 847–855.
extraction: a clinical and radiographic 12-month prospec- 73. Tomasi C, Sanz M, Cecchinato D, Pjetursson B, Ferrus J,
tive study. Int J Periodontics Restorative Dent 2003: 23: 313– Lang NP, Lindhe J. Bone dimensional variations at implants
323. placed in fresh extraction sockets: a multilevel multivariate
67. Serino G, Biancu S, Iezzi G, Piatelli A. Ridge preservation analysis. Clin Oral Impl Res 2010: 21: 30–36.
following tooth extraction using a polylactide and polygly- 74. Trombelli L, Farina R, Marzola A, Bozzi L, Liljenberg B,
colide sponge as space filler: a clinical and histological Lindhe J. Modeling and remodeling of human extraction
study in humans. Clin Oral Implants Res 2003: 14: 651–658. sockets. J Clin Periodontol 2008: 35: 630–639.
68. Shakibaie-M B. Comparison of the effectiveness of two dif- 75. Wilderman MN. Repair after a periosteal retention proce-
ferent bone substitute materials for socket preservation dure. J Periodontol 1963: 34: 487–503.
after tooth extraction: a controlled clinical study. Int J Peri- 76. Wood DL, Hoag PM, Donnenfeld OW, Rosenberg DL. Alve-
odontics Restorative Dent 2013: 2: 223–228. olar crest reduction following full and partial thickness
69. Tal H. Autogenous masticatory mucosal grafts in extraction flaps. J Periodontol 1972: 43: 141–144.
socket seal procedures: a comparison between sockets 77. Yaffe A, Fine N, Binderman I. Regional accelerated phe-
grafted with demineralized freeze-dried bone and deprotei- nomena in the mandible following mucoperiosteal flap sur-
nized bovine bone mineral. Clin Oral Impl Res 1999: 10: gery. J Periodontol 1994: 65: 79–83.
289–296. 78. Yoshino S, Kan JY, Rungcharassaeng K, Roe P, Lozada JL.
70. Tavtigian R. The height of the facial radicular alveolar crest Effects of connective tissue grafting on the facial gingival
following apically positioned flap operations. J Periodontol level following single immediate implant placement and
1970: 41: 412–418. provisionalization in the esthetic zone: a 1-year randomized
71. Thalmair T, Fickl S, Schneider D, Hinze M, Wachtel H. controlled prospective study. Int J Oral Maxillofac Implants
Dimensional alterations of extraction sites after different 2014: 29: 432–440.
alveolar ridge preservation techniques – a volumetric study.
J Clin Periodontol 2013: 40: 721–727.

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