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					                                                                                                                  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

                                                                                             W
                                                                                                        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
       KEY WORDS
                                                                                             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

                                                                                             doi: 10.1902/jop.2009.090156


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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
Patient Selection
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-
Surgical Protocol
                                                           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.


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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.
                                                                             Prosthetic Protocol
                                                                             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.
                                                                             Follow-Up Evaluation
                                                                             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
                                                                             probe.††
                                                                             Statistical Analyses
                                                                             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.
    silk sutures.
                                                                             RESULTS
   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
   Radiographic Assessments
                                                                             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.


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J Periodontol • October 2009                                                                                                `
                                                                                                              Crespi, Cappare, Gherlone




                                                                                         Radiographic Evaluation
                                                                                         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).

                                                                                         DISCUSSION
                                                                                         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
                                                                          apposition.27,28
                                                                             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

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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
                                                                      CONCLUSIONS
    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
                                                                      composition.
   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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                                                                                                          Crespi, Cappare, Gherlone




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