Volume 80 • Number 10
Dental Implants Placed in Extraction
Sites Grafted With Different Bone
Substitutes: Radiographic Evaluation
at 24 Months
Roberto Crespi,* Paolo Cappare,* and Enrico Gherlone*
Background: Reduction of alveolar height and width after tooth
extraction may provide some problems in implant placement, es-
pecially in the anterior maxilla for esthetic reasons. Different graft
materials have been advocated to prevent bone-volume reduction.
The aim of this study was to evaluate radiographic parameters of
implants positioned in grafted alveoli with three different biomate-
rials: magnesium-enriched hydroxyapatite (MHA), calcium sulfate
hen a fresh extraction
(CS), and heterologous porcine bone (PB). socket is too wide or re-
Methods: In 15 patients, 45 fresh extraction sockets with three sidual alveolar walls are
bone walls were selected. Fifteen sockets received MHA, 15 sockets damaged, some problems in im-
received CS, and 15 sockets received corticocancellous PB as a plant placement may occur, espe-
graft material. Three months after bone ﬁlling, titanium dental im- cially in the anterior maxilla where
plants were placed in grafted sites. Three months after implant bone volume is important for
placement, temporary restoration was performed. Follow-up ex- biologic and esthetic reasons.1-3
aminations were conducted, and intraoral digital radiographs Usually in the anterior region, post-
were taken at baseline and 12 and 24 months after implant place- extraction bone resorption and
ment to evaluate the marginal bone level in each patient. Compar- remodeling may induce an undesir-
isons for marginal bone loss over time between groups were able esthetic situation, particularly
performed by the Student two-tailed t test. when the buccal plate has been
Results: At the 24-month follow-up, a survival rate of 100% was damaged during tooth extraction.4
reported for all implants. For the MHA group, a mean mesial bone Consequently, surgical procedures
loss of -0.21 – 0.08 mm and a mean distal bone loss of -0.22 – such as guided bone regeneration,5,6
0.09 mm (mean bone loss: 0.21 – 0.09 mm) were reported; for the bone allografts, bone autografts, and
CS group, a mesial bone loss of -0.14 – 0.07 mm and a distal bone xenografts7-9 are recommended to
loss of -0.12 – 0.11 mm (mean bone loss: -0.13 – 0.09 mm) were maintain the bone volume of fresh
measured; for the PB group, a mean mesial bone loss of -0.15 – sockets.
0.10 mm and a mean distal bone loss of -0.16 – 0.06 mm (mean Due to their excellent biocom-
bone loss: -0.16 – 0.08 mm) were reported. No statistically signiﬁcant patibility and bioactivity, bioceram-
differences were reported among groups (P >0.05). ics are widely used in bone grafting
Conclusion: At the 24-month follow-up, the present study showed and dental devices as bone substi-
that placement of implants in grafted sockets was not inﬂuenced by tutes10-12 because hydroxyapatite
the three different biomaterials because they did not negatively im- (HA) ceramics have the ability to
pact the clinical outcome. J Periodontol 2009;80:1616-1621. induce mesenchymal cells to differ-
entiate toward osteoblasts rendering
HA a potential scaffold material for
Alveolar ridge preservation; dental implants; graft material; tooth bone tissue engineering.13,14
extraction. Calcium sulfate (CS) is a bio-
compatible, osteoconductive, and
bioabsorbable biomaterial that is
* Department of Dentistry, Vita Salute University, San Raffaele Hospital, Milan, Italy.
used to ﬁll bone defects and maxil-
lary sinus lift15,16 because this
J Periodontol • October 2009 `
Crespi, Cappare, Gherlone
material is well tolerated by the host. It has been his- Table 1.
tologically demonstrated that CS is completely re-
Distribution of Grafted Biomaterials
sorbed within 3 months in human fresh extraction
sockets and does not interfere with bone healing.17 Among Subjects and Sites Corresponding
Furthermore, anorganic animal bone particles to the Extracted Tooth
have been used as a graft material for ridge preserva-
tion and in maxillary sinus augmentation, providing Biomaterial and Site (tooth number)
bone volume arrangement.18-21
Subject MHA CS PB
Nevertheless, close matching of the resorption to
the bone deposition rate represents an important con- 1 19 21 11
cern when selecting biomaterial grafts because a rap-
2 19 20 12
idly resorbing scaffold might induce bone volume
reduction, whereas one that resorbs too slowly, or 3 14 3 20
not at all, would slow down bone deposition and limit
4 11 30 29
tissue remodeling and maturation for implant place-
ment.19-21 5 28, 29 3
A matter of controversy in implant dentistry con-
6 6 3 30
cerns what is the most appropriate bone substitute
for ridge preservation after tooth removal since little 7 11,12 22
has been reported to date to give any insight as to
whether such grafts can support functioning dental 8 30 14 19
implants. 9 13 30 19
The aim of this study was to evaluate radiographic
parameters of implants positioned in grafted alveoli 10 5 14 3
with three different biomaterials: magnesium-en- 11 13 20 11
riched hydroxyapatite (MHA), CS, and heterologous
porcine bone (PB). 12 19 11 29
13 20 13 5
MATERIALS AND METHODS
14 11 19 30
Between October 2006 and January 2007, 15 pa- 15 3 14 30
tients (seven women and eight men; mean age:
54.6 years; age range: 34 to 68 years) were included
in this prospective study. Each patient required ex- which were debrided before receiving graft materials.
traction of three teeth. The inclusion criteria for the For graft materials, 15 sockets received MHA Ca10-
sockets were the presence of three bone walls and xMgx(PO4)6(OH)2 available in granule form,† 15
loss of buccal plate; all patients were in good health, sockets received CS,‡ and 15 sockets received corti-
were non-smokers, and had no chronic systemic dis- cocancellous PB.§
ease. Exclusion criteria were coagulation disorders, All graft materials were hydrated with sterile solu-
presence of signs of acute infection around alveolar tion for 3 minutes prior to insertion in the sockets
bone at the surgical site, and alcohol or drug abuse. and packed into the alveolus (Fig. 1); a collagen sheet
The local ethical committee approved the study, and was used to cover the inner denuded biomaterial. The
all patients signed an informed consent form. The di- collagen was placed under the detached palatal tissue
agnosis was made clinically and radiographically. and secured with silk sutures. Three months after ex-
The patients were treated by one oral surgeon (RC) traction and bone ﬁlling,17,22 titanium plasma–spray
and one prosthodontist (EG) at the Department of Den- implants, with a machined neck of 0.8 mm and a
tistry, Vita Salute University, San Raffaele Hospital. rough-surface body with a progressive thread designi
with external hexagon as implant–abutment junc-
tions, were positioned in each site (Fig. 2). Twenty-
Patients received 1 g amoxicillin 1 hour prior to sur-
six implants had a diameter of 5 mm with a 13-mm
gery and 1 g amoxicillin twice a day for a week after
length, 10 implants had a diameter of 3.75 mm with
surgical procedure. Surgery was performed under lo-
a 13-mm length, and nine implants had a diameter
cal anesthesia (optocaine 20 mg/ml with adrenaline
1:80.000). Forty-ﬁve teeth (Table 1) were extracted, † SintLife, Finceramica, Faenza, Italy.
‡ Easy Set, Sweden & Martina, Due Carrare, Italy.
avoiding ﬂap elevation, and a periodontal probe was § Tecnoss, Giaveno, Italy.
used to verify the wall assessment of the fresh sockets, i Seven, Sweden & Martina.
Hydroxyapatite and Calcium Sulfate in Extraction Sockets Volume 80 • Number 10
logist (EG) measured the changes in marginal bone
height over time. The distance between the platform
of the implant and the most coronal point of contact
between the bone and the mesial and distal sites of
implants was considered. The difference of bone level
was measured by software.# The marginal bone loss
was evaluated at 12 and 24 months of healing from
implant placement. Mesial, distal, and mean bone loss
in the maxilla and mandible were calculated.
Three months after the placement of the implants,
temporary restoration was performed. Transfer cop-
ings were inserted into the internal hex of the implant
with a seating instrument and secured with abutment
screws. Impressions were taken with a silicon material
using an individual impression. Prepared ﬁnal metal
abutments were screwed onto dental implants (Fig.
4). All temporary crowns were in full contact in centric
occlusion. Two months later, ﬁnal metal ceramic res-
torations were cemented onto abutments. Occlusion
was checked using an 8-mm foil,** which was to resist
withdrawal only under maximal clenching. The ﬁnal
ceramic-fused-to-metal restorations were cemented
6 months after implant placement.
The following clinical parameters were checked: pain,
occlusion, and prosthesis mobility. Success criteria
for implant survival were accepted as the presence
of implant stability, absence of a radiolucent zone
around the implants, no mucosal suppuration, and
no pain. Follow-up examinations were performed at
baseline and 12 and 24 months. Probing depth (PD)
and the modiﬁed plaque and modiﬁed bleeding in-
dexes23 were determined on the mesial, distal, buccal,
and palatal surfaces of the implants with a periodontal
Data are presented as mean – SD. Comparisons be-
Figure 1. tween groups (MHA versus CS, PB versus CS, and
Clinical photographs. A) Fresh socket with three remaining walls and PB versus MHA) were performed by the Student
absence of a buccal plate. B) MHA compressed into the socket. C) two-tailed t test. P <0.05 was considered the threshold
Collagen sheet covering the inner denuded biomaterial and secured with for statistical signiﬁcance.
of 5 mm with a 10-mm length. Osteotomies passed Surgical and Prosthetic Procedure
apical to the zone of the graft so that the apical portion At the 24-month follow-up, a survival rate of 100%
of the implant engaged native bone. was reported for all implants. No pain or ﬁnal prosthe-
sis mobility was recorded. There was suitable wound
healing around temporary abutments with ﬁne adap-
Intraoral digital radiographs¶ were made at baseline
tation to temporary crowns. Minor swelling of gingival
and 12 and 24 months after implant placement
mucosa was present in the ﬁrst days after surgical
(Fig. 3). Periapical radiographs were taken perpen-
dicularly to the long axis of the implant with a long- ¶ Schick CDR, Schick Technologies, Long Island City, NY.
# Schick CDR, Schick Technologies.
cone parallel technique using an occlusal template ** Shimstock, Hanel, Germany.
to measure the marginal bone level. A masked radio- †† Hu-Friedy PGF-GFS, Hu-Friedy, Chicago, IL.
J Periodontol • October 2009 `
Crespi, Cappare, Gherlone
Radiographic results were reported at
24 months from implant placement
(Table 2). For all groups, mean distal,
mesial, and total mean bone loss values
were calculated (Table 2). No statisti-
cally signiﬁcant differences were re-
ported among groups (P >0.05).
Histologic and histomorphometric
studies22-30 about the three bone substi-
tutes used in the present study reported
large deviations for the percentage
values of residual grafted material and
vital bone formation, which may inﬂu-
ence early prognosis of such treatment
Figure 2. and the success rate of dental implants
Implants inserted into grafted sites 3 months after tooth extractions. positioned in grafted sites.
In a study22 with split-mouth design,
fresh sockets received graft material MHA, and other
sockets received CS. Radiographs revealed a greater
reduction of alveolar ridges in the CS group than in the
MHA group, with statistically signiﬁcant differences
(P <0.05). Histologic examination showed more vital
bone formation in the CS group than in the MHA group
and faster resorption of residual graft material in the
CS group (13.9% – 3.4%) than in the MHA group
(20.2% – 3.2%).
Barone et al.24 used corticocancellous PB for a
ridge preservation procedure, and 7 months after the
surgical treatment, histologic analyses revealed high-
ly mineralized and well-structured trabecular bone.
Similar results were reported from studies that used
deproteinized bovine bone remaining in amounts of
20% at the time of biopsy25,26 but with new vital bone
Although different percentages of residual graft
Figure 3. material may damage the osseointegration process
Clinical x-rays of implants in grafted sockets at 3 months with screw
ﬁnal abutments (A) and 24 months after the implant placement of positioned implants, a study29 showed that remain-
procedure (B). ing bovine bone particles embedded in the vicinity of
implants led to a normal bone implant interface at the
histologic level because these particles take place in
procedures; no mucositis or ﬂap dehiscence with sup- the remodeling process.30
puration were found. However, little is known about the healing pattern
and osseointegration process at the interface of im-
Clinical Parameters plants placed in different grafting materials in
Plaque accumulation at baseline was 0.52 – 0.23 and humans. In two different studies, two implants re-
0.73 – 0.31 after 24 months. The bleeding index at trieved due to fracture 431 and 532 years after insertion
baseline was 0.67 – 0.19 and 24 months later was in a sinus-augmentation procedure using 100% anor-
0.78 – 0.36. ganic bovine bone were removed, and the histologic
The mean PD was obtained by averaging PD mea- sections were examined. In both samples, at low mag-
surements on the mesial, distal, buccal, and palatal niﬁcation, many particles of anorganic bovine bone
surfaces of the implants; the mean values were 1.38 – were still present in the peri-implant bone in the
0.38 mm and 2.03 – 0.57 mm at baseline and 24 grafted area. Bone was interposed between the
months, respectively. grafted particles and the metal surfaces, and in no
Hydroxyapatite and Calcium Sulfate in Extraction Sockets Volume 80 • Number 10
during the osseointegration process and
subsequent functional loading periods.
Molly et al.27 evaluated bone forma-
tion histologically and biomechanically
in extraction sites after implantation of
three commercially available bone bio-
materials: polylactic–polyglycolic acid
technology, bovine porous bone min-
eral, and a natural coral derivative phys-
ically and chemically transformed into a
calcium carbonate ceramic. Biopsies
were obtained from each site 4 months
later. At that time, endosseous implants
were placed in the sites. All sites re-
vealed good primary stability at implant
insertion and proper implant rigidity at
abutment placement, indicating that
early implant osseointegration was not
inﬂuenced by the application of the
bone biomaterials used in the study.
In the present study, the absence of
Figure 4. statistically signiﬁcant differences of
Prepared ﬁnal metal abutments screwed onto dental implants. bone level around implants among
groups conﬁrmed the results reported
by Norton and Wilson,33 who evaluated
Table 2. the clinical outcome of implants placed in sites grafted
Radiographic Measurements: Mean Mesial with bioactive glass.
and Distal and Total Mean Bone Loss 24 From previous histologic studies,27-32 it is clear
that the relatively high amount of graft material used
Months After Implant Placement Among
in the present study was present in different percent-
Groups ages during different periods of osseintegration, but
clinical and radiographic observations indicated an
Sockets osseointegration process that allowed load bearing.
Group (n) Mesial Distal Mean
MHA 15 -0.21 – 0.08 -0.22 – 0.09 -0.21 – 0.09
The 24-month follow-up showed 100% implant sur-
CS 15 -0.14 – 0.07 -0.12 – 0.11 -0.13 – 0.09 vival for implants placed in sockets grafted with three
PB 15 -0.15 – 0.10 -0.16 – 0.06 -0.16 – 0.08 different materials. This result suggests that the early
prognosis of such a treatment modality was not neg-
atively inﬂuenced by grafting materials of different
cases were the graft particles in contact with the im- However, further clinical and histologic studies are
plants. No acute or chronic inﬂammatory cell inﬁltrate needed to better understand the healing pattern of
or foreign body reactions were present around the these biomaterials in relationship with dental implants
particles or at the bone–implant interface. A high per- positioned in grafted sites with bone substitutes.
centage of direct contact between bone and implant,
without the interposition of graft material particles, ACKNOWLEDGMENT
was present after 4 years (72% – 4%)31 and 5 years The authors report no conﬂicts of interest related to
(50%).32 These results showed that the slow resorp- this study.
tion of the graft particles did not compromise the os-
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