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Marginal bone response of implants placed in post-extraction sites following ridge preservation with bovine anorganic bone
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Marginal bone response of implants placed in post-extraction sites following ridge preservation with bovine anorganic bone
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Content
MARGINAL BONE RESPONSE OF IMPLANTS PLACED IN POST-
EXTRACTION SITES FOLLOWING RIDGE
PRESERVATION WITH BOVINE ANORGANIC BONE
By
Ivy Hsiao-Han Wu
A Thesis Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
MASTER OF SCIENCE
(CRANIOFACIAL BIOLOGY)
August 2013
Copyright 2013 Ivy Hsiao-Han Wu
ii
Acknowledgements
I would like to thank Dr. Homa Zadeh for providing this valuable research
experience. His passion in research and education has inspired me to pursue this study. I
would also like to thank Dr. Mahvash Navazesh, Dr. Michael Paine, and Dr. Kian Kar for
their guidance and mentoring throughout my residency program.
I would like to thank my parents for their unconditional love, support and
patience.
I grateful acknowledged Dr. and Mrs. Baldwin and Doreen Marchack for their
inspiration, support and encouragement.
iii
Table of Contents
Acknowledgements ii
List of Table iv
List of Figures v
Abstract vi
Chapter 1: Introduction and Background 1
Chapter 2: Materials and Methods 15
Chapter 3: Results 21
Chapter 4: Discussion 29
Chapter 5: Conclusion 34
References 35
iv
List of Tables
Table 1. Implant-related outcomes following ridge preservation 11
Table 2. Implant-related outcomes following ridge preservation: Reviews 14
Table 3. Demographics of the study subjects 21
Table 4. Comparison of mean mesial of distal bone changes for socket grafted and 24
healed sites
Table 5. Mean mesial and distal bone changes for socket grafted and healed sites 26
according to tooth type, implant diameter and implant length
Table 6. The mean change in alveolar bone remodeling and mean change in bone 28
loss around the dental implants
v
List of Figures
Figure 1. Radiographic landmark 17
Figure 2. Radiographic analysis with VixWin Pro 18
Figure 3. Calibration with VixWin Pro 19
Figure 4. Marginal bone loss in different anatomical locations 23
Figure 5. Marginal bone loss in maxilla vs. mandible 24
Figure 6. Change of marginal bone level in the socket-grafted sites 27
Figure 7. Chang of marginal bone level in the non-grafted healed sites 28
vi
Abstract
Background: Following tooth extraction, the resorptive process results in altered bony
architecture of the alveolar ridge. The dimensional changes of the hard tissue may present
a challenge to implant therapy. Various techniques have been proposed to minimize
horizontal and vertical resorption. The objective of this retrospective study was to
compare the radiographic marginal bone level changes following implant placement in
post-extraction sites following ridge preservation with bovine anorganic bone compared
with non-grated healed sites.
Methods: One hundred thirty four patients treated from April 2005 to March 2013 were
included in the present restrospective study. Seventy-eight patients were treated with
reduced-trauma tooth extraction and ridge preservation procedure, which entailed
placement of bovine anorganic bone (Bio-Oss large particle size of 1-2mm) covered with
PTFE membrane (GBR-200; Osteogenics), which was retained for 4 weeks. The mean
healing time was 160 day (± 109 days) prior to implant placement. Fifty-one patients
with healed sites without history of bone grafting served as controls. Digital intraoral
radiographs were taken at the time of implant placement and during follow-up visits. The
distance from the alveolar crest to the implant platform (BC-I) and the distance from the
implant platform to the first bone-to-implant contact (I-FB) were measured at the time of
implant placement and at follow-up visits. The mean follow-up period was 2.8 years
(1016± 502 days). Four hundred sixty additional implants were included to estimate the
survival rate of the implants.
vii
Results: In the grafted sites, the mean change of marginal bone was 0.11 mm and 0.07
mm in the mesial and distal aspects, respectively. Whereas in the non-grafted healed
sites, the mean crestal bone change was 0.07 mm and 0.06 mm in the mesial and distal
aspects. These differences were not statistically significant. In the healed sites, more bone
loss was observed in the anterior region compared to the molar region in mesial and distal
sites (p<0.05). The length and the diameter of the implants did not seem to influence the
degree of marginal bone loss. The survival rate of implants in the ridge preserved sites
was estimated 97.3%, compared to 98.5% in the non-grafted sites.
Conclusion: The results of this study have demonstrated a favorable marginal bone
response to the particular ridge preservation protocol described herein, using anorganic
bovine bone and nonresorbable membrane. The crestal bone loss and bone remodeling
were similar between the sites following ridge preservation procedure and non-grafted
sites. The survival rates of implants in the ridge-preserved site and in the non-grafted
healed sites were greater than 97%. Overall, dental implants placed in socket-grafted sites
demonstrated comparable clinical outcomes to those placed in native bone.
1
Chapter 1: Introduction and Background
Healing of Extraction Socket
The healing events following tooth extraction in human has been reported in a
classical study by Amler, et al. Initially, coagulum occupies the entire extraction socket,
followed by appearance of granulation tissue on days 2-3. Connective tissue,
characterized by spindle cells and collagen fibers, predominate the socket from 4
th
to 12
th
days. Osteoid tissue first appears on day 7 and fills two third of the socket by the 38
th
day
(Amler 1960). Two phases of bone healing has been observed. In the osteogenic phase,
formation of woven bone is accompanied by proliferation of osteogenic cells from 4 to 8
weeks. From weeks 8 to 12, osteogenesis decreases and trabecular bone undergo
maturation (Evian et al., 1981).
In a dog study (Cardaropoli et al. 2003), periodontal ligament cells (PDL)-like
cells have been identified close to the coagulum between days 1 to day 7 after tooth
extraction. This observation supported the notion that PDL cells may be involved in the
formation of the provisional matrix and bone in the extraction socket. One month after
tooth extraction, the mineralized tissue was found to occupy 88% of the socket.
Ridge Remodeling Following Tooth Extraction
The alveolar bone undergoes structural changes following tooth extraction. The
dynamics of the ridge remodeling process has been studied extensively in animal models
2
(Araujo et al. 2005, 2009, Cardaropoli et al. 2003) and in human (Johnson, 1969, Devlin
and Sloan, 2002, Schropp, et al 2003, Araujo and Lindhe, 2008).
Several methods have been proposed in evaluating the alveolar ridge alteration.
In a histological study, increased osteoclastic activity within resorption bays on the
surface of the bone has been observed in the first 8 weeks following tooth extraction
(Araujo and Lidhe 2005). The osteoclastic activity results in resorption of both buccal
and lingual aspects. The buccal wall has been demonstrated to undergo more substantial
height reduction. The more pronounced facial bone remodeling has been attributed to the
fact that most of the buccal bone is composed of bundle bone (Araujo and Lidhe 2005).
Using study casts and subtraction radiography, Schropp et al. (2003) have
assessed bone alveolar ridge changes following single-tooth extraction after 3, 6, and 12
months of healing. The authors have reported that the alveolar ridge width undergoes
significant changes, while only a minor vertical ridge reduction is observed. At the end of
the study, the width of the ridge was found to be reduced by approximately 50%, of
which 2/3 of the reduction occurred during the first 3 months of healing. The percent
reduction was larger in the molar region than in the premolar region. Additionally, the
authors suggested that the bone level at the extraction site determined the level to which
the ridge heals following tooth extraction. These findings were in agreement with earlier
studies (Pietrokovski and Massler, 1967).
The number of tooth extractions may be a factor influencing ridge remodeling. In
experimental dog studies, it has been found that multiple tooth extractions lead to more
significant bone remodeling (Al-Askar et al., 2011).
3
Tooth extraction not only result in loss of hard tissue, but also results in changes
of the overlying soft tissue (Schropp et al., 2003). A recent systematic review assessed
dimensional changes for both hard and soft tissue for 12 months following tooth
extraction in humans (Tan et al., 2012). The authors observed greater magnitude of
horizontal reduction (3.79mm) than vertical reduction (1.24mm) on the buccal aspect.
The changes on the mesial and on the distal were 0.84mm and 0.80mm, respectively.
Gain of soft tissue thickness (0.4-0.5mm) have been found at 6 months. At 12 months,
the horizontal reduction of soft and hard tissue was between 0.1-6.1mm, whereas the
vertical changes was loss of 0.9mm to gain of 0.4mm.
A recent consensus report (Hammerle et al., 2012) concluded that the mean
horizontal bone loss in ridge width of 3.8mm, and the mean vertical bone loss in ridge
height of 1.24mm.
Rationale for Ridge Preservation
Ridge preservation may be defined as procedures which seek to maintain the ridge
volume within the skeletal envelope existing at the time of extraction. In contrast, ridge
augmentation, which refers to the increase of the ridge volume beyond the skeletal
envelope existing at the time of extraction (Hammerle et al., 2012).
Tooth extraction is one of the most commonly performed dental procedures. The
challenge for the clinicians lies in the management of the extraction socket. The
physiological remodeling of alveolar ridge results in horizontal and/ or vertical
deficiency. Preservation of the ridge may enable placement and stability of dental
4
implant, reduce loss of alveolar bone volume, reduce the need of additional grafting
procedures, optimize alveolar crest topography, simply therapy and improve the esthetic
outcome of the final prosthesis.
Clinical Outcomes Following Ridge Preservation
Ten Heggeler et al. (2010) assessed the benefits of ridge preservation in the
anterior and premolar regions. The PubMed and Cochrane Central Register searches
yielded 9 eligible studies. Theses studies reported results concerning osteoconductive
bone grafts, including mineralized freeze-dried bone (FDBA), alloplasts, and xenograft.
The data was evaluated as clinical and radiographic outcomes. With respect to ridge
preservation, FDBA performed the best with an increase of the height with concurrent
loss in width of 1.2mm. Overall, this review reported a width reduction of 2.6-4.6mm and
a height reduction of 0.4-3.9mm. Tooth extractions were performed with the elevation of
a full-thickness flap in most studies included.
In another systematic review, Vignoletti et al. (2012) evaluated the effects of
ridge preservation procedures on implant placement and the final restorations. The search
yielded 9 prospective randomized clinical trials with a minimum of 3-month follow-up
and reports on both hard and soft tissue changes. The meta-analysis indicated a
statistically significant greater reduction in bone height (-1.47mm) and bone width (-
1.83mm) relative to the control group. No significant differences were noted with regard
to the material used. The review also suggested that surgical protocol might be the most
significant factor influencing the outcomes. Flap elevation seemed to preserve the width
5
of the bone more effectively than the flapless approach. However, animal studies has
shown similar amount of bone loss regardless of flap or flapless procedure (Araujo and
Lindhe, 2009). The use of barrier membrane and primary closure demonstrated positive
influence on ridge preservation.
Horowitz et al. (2012) have reviewed several systematic reviews and concluded
that just over 1mm of horizontal bone resorption still occurred with the relative
preservation of height following ridge preservation procedures, while the natural healing
of extraction sockets results in greater than 3mm of horizontal bone loss and 1mm of
vertical bone loss. In regards to the choice of bone grafting materials, no one grafting
material has demonstrated clear benefits to another. The advantages of primary closure
were inconclusive. Additional research was advised to support the use of a barrier
membrane and growth factors.
Wang and Lang (2013) identified recent animal studies and clinical trials to
address several key issues on ridge preservation after tooth extraction. Contemporary
evidence has demonstrated that although immediate implant placement and immediate
loading do not prevent the resorption of the alveolar bone, bone grafting of the jumping
space around the immediate implant may reduce soft and hard tissue loss. Non-grafted
socket underwent more bone loss in the horizontal direction compared to socket grafted
with xenograft (Bio-Oss), despite that the xenograft served only as a scaffold and did not
induce new bone formation. When demineralized bone matrix was used in socket
grafting, particle size of the graft does not significantly influence the outcome. Also,
demineralized freeze-dried bone allograft (DFDBA) yielded similar effect on ridge
6
preservation to that of FDBA. Bone Ceramics has been observed to be more effective on
preserving alveolar bone compared to xenograft (Bio-Oss). However, since Bone
Ceramic seemed to interfere with the healing process of an extraction socket, the
reviewers suggested careful consideration when implant therapy is planned. Primary flap
closure result in more postoperative discomfort, however, it did not appear to provide
additional benefits on preservation of alveolar ridge.
Collectively, recent data suggests a positive effect of socket grafting in reducing
alveolar resorption in horizontal and vertical direction. Due to considerable heterogeneity
to study designs, surgical protocols, and method of evaluation, it is inconclusive
regarding which type of biomaterial is the most ideal for clinical application. There is
insufficient data on the necessity of primary closure of the extraction sockets.
Implant-Related Outcomes
The clinical outcomes of dental implants placed in grafted sites were described in
several clinical studies and reviews (Table 1, 2). Historically, autogenous bone grafting
has been considered to be the “gold standard” of hard tissue augmentation. One study
reported ridge preservation in maxillary anterior area using bone marrow from the iliac
crest (Pelegrine et al., 2010). The control sites were allowed to heal without bone
grafting. Titanium screws were used as reference points of measurements. Dental
implants were inserted 6 months following tooth extraction. The horizontal bone and
vertical bone remodeling in the test group were 1.14mm and 0.62mm, respectively,
whereas the corresponding measurements in the control group were 2.46mm and
7
1.17mm. These findings supported the use of autologous bone marrow as source of bone
graft for ridge preservation.
Majority of the studies involved ridge preservation using synthetic graft or
xenograft. Norton and Wilson (2002) investigated the clinical outcomes of implant placed
in extraction sockets grafted with bioactive glass (Perioglas or Biogran) and a Gore-Tex
barrier membrane. The implant mobility, marginal bone levels and soft tissue health were
evaluated over 2-3 years of follow up. The success rate was 88.6% and the cumulative
success was 96.8%. Forty-eight percent of implant did not exhibit marginal bone loss.
The mean marginal bone loss was 0.5mm in the mesial and 0.4mm in the distal.
In a radiographic study, the bone remodeling around dental implants placed in
socket grafted with three different biomaterials was evaluated over a 24- month follow-up
(Crespi et al., 2009). Titanium-plasma sprayed (TPS) implants were placed 3 months
following the ridge preservation procedure. In the socket grafted with magnesium-
enriched hydroxyapatite (MHA), the bone loss was 0.21mm in the mesial and 0.22mm in
the distal. In the calcium sulfate (CS) group, the bone loss was 0.14mm in the mesial and
0.12mm in the distal. Finally, in the heterologous porcine bone (PB), the bone loss in the
mesial was 0.15mm and 0.16mm in the distal. No statistically significant differences
were found among each group. Thus, the authors concluded that implant placement in
grafted sockets were not influenced by the three different bone grafting materials tested
in the study.
8
In another clinical report, Patel et al., (2013) evaluated the interproximal
radiographic bone level and the survival/ success rate of implants placed in sites grafted
with Bone Ceramic (SBC) or deproteinized bovine bone mineral (DBBM). Implants were
placed 8 months following the procedure and loading of the implants occurred 8 months
after placement. The survival rates of the implants were 100% in both groups, where as
the success rate were 85% and 83% in the SBC group and in the DBBM group,
respectively. The mean changes in height in SBC groups were 0.12mm in the mesial and
0.35mm in the distal, while the corresponding values in the DBBM group were 0.20mm
and 0.13mm. Thus, the survival/ success rate of the implants and radiographic bone level
were comparable in sites preserved with bone ceramics or bovine xenograft.
Barone, Ricci et al., (2012) studied the outcomes of socket grafting with
corticocancellous porcine bone and exposed collagen membrane. The dimensional
change of the alveolar ridge was measured using an acrylic stent. The control group
showed vertical bone loss 1mm in the mesial and 1mm in the distal, and horizontal bone
loss of 0.3mm in the mesial and 0.3mm in the distal. Test sites showed vertical bone loss
of 0.3mm in the mesial and 0.3mm in the distal, and the changes of horizontal bone was
1.6mm. Forty two percent of sites in the control group required additional bone grafting
procedures, compared to 7% in the test sites. Additionally, larger and longer implants
were inserted more frequently in the grafted sits. Using the same bone grafting material,
the authors (Barone, Orlando et al., 2012) published a randomized clinical trail to
compare the need for additional bone augmentation procedures at implant placement,
success rate, marginal bone loss for implant placed in grafted vs. non-grafted sites.
9
Implant were placed 7 months after healing and loaded in 4 months. The cumulative
success rate was 95% for both groups at 3-year follow-up. In regards to marginal bone
loss, no statistically significant differences were found between groups. These finding
lead to the conclusion that implants placed into socket-grafted sites exhibited similar
clinical outcomes, survival and marginal bone remodeling to the non-grafted sites.
Tissue engineering approach has also been adopted in ridge preservation
procedure. Bone morphogenic proteins (BMPs) have been implicated in inducing stem
cell differentiation. Fiorellini et al., (2005) described the efficacy of bone induction for
implant placement by two concentrations of recombinant human BMP-2 with acellular
collagen sponge (rhBMP-2/ACS). In Test group 1, 0.75mg/ml of rhBMP-2/ACS was
used, and 1.5mg/ml of rhBMP-2/ACS in Test group 2. Implants were placed 4 months
following tooth extraction. The authors observed that 86% of sites in test group 2
demonstrated adequate bone for implant placement, whereas 59% and 45% were found
with the placebo and the control group, respectively.
Several other studies on ridge preservation reported sufficient bone for implant
placement (Sandor et al., 2003, Serino et al., 2003, 2008, Aimetti et al., 2009). Only one
study (Baron, Orlando et al., 2013) reported long-term follow-up on the clinical outcomes
of dental implants inserted into alveolar ridge underwent ridge preservation procedures.
Clearly, much remains to be learned on implant-related outcomes. Therefore, the
objective of the present study was to compare the radiographic marginal bone level
changes after implant placement in post-extraction sites following ridge preservation with
bovine anorganic bone compared with non-grated healed sites. The following hypotheses
10
are generated to answer the questions marginal bone response around the implants placed
following the proposed ridge preservation procedure.
H
1
The clinical outcomes of implants placed in extraction sockets undergo ridge
preservation with bovine anorganic bone is comparable to the non-grafted healed
sites.
H
0
The clinical outcomes of implants placed in extraction sockets undergo ridge
preservation with bovine anorganic bone is significantly different from the non-
grafted healed sites.
11
Table 1. Implant-related outcomes following ridge preservation. Abbreviations: N/A data
not available; RCT randomized clinical trial, pts patients, ext extraction.
12
Table 1 (Continued)
13
Table 1 (Continued)
14
Table 2: Implant-related outcomes following ridge preservation in reviews.
Publication Type of
study
Inclusion Criteria Number
of eligible
studies
Conclusion
Darby et al.,
2009
Review RCT, controlled
clinical trials, and
prospective/
retrospective studies
with a minimum of 5
pts
37 Inconclusive regarding that ridge preservation
procedure improve the ability to place implants
Vignoletti et
al., 2012
Systematic
review
RCT and prospective
cohort with follow-up
>3 months were
included
14 Greater ridge reduction in bone height
(1.47mm) and bone width (1.83mm) for the
control groups. Flapped groups were
statistically favored in terms of bone width.
Inconclusive on the long-term outcomes of
implant therapy
Horvath et
al., 2013
Systematic
review
Longitudinal
prospective studies,
RCTs, CCTs, and
cohort studies with
control groups
14 Seven studies reported implant placement in
the previous sockets were successful. Four
studies reported the need of further
augmentation at the stage of implant
placement, 3 of them favored ARP group
(Fiorellini et al., 2005, Barone et al., 2008,
Pelegrine et al., 2010)
15
Chapter 2: Materials and Methods
Study Population and Design
The charts and radiographs from a private periodontal office from April 2005 to
March 2013 were thoroughly reviewed for this retrospective radiographic study. A total
of 129 patients (75 female and 54 males; mean age 63 years; range 22 to 86 years) were
included (Table 3). Patients who presented with edentulous space and required bone
augmentation procedure prior to implant placement were not included in this study. All
patients received thorough explanation and signed an inform consent form.
In addition to the 222 implants evaluated in the present study, four hundred sixty
implants placed in the same periodontal office were included solely to estimate the
survival rate of the implants.
Surgical Protocol
All patients, except those with specific allergy, received 2mg of amoxicillin 1
hour prior to the procedure and 500mg of amoxicillin 3 times a day for 1 week. For
patients who are allergic to penicillin, clindamycin 600mg, followed by 300 mg 3 times
daily for one week was prescribed. Patients were instructed to rinse with 0.12%
chlorhexidine rinse for 1 ½ minutes before the surgery, as well as rinse twice daily for
one week after surgery. Surgery was performed under local anesthesia (Lidocaine 2%
with epinephrine 1:100,000). Briefly, teeth were extracted with reduced-trauma tooth
extraction without flap elevation. The sockets were assessed to verify the integrity of the
16
alveolar wall and were thoroughly debrided. Subsequently, bovine anorganic bone (Bio-
Oss large particle size of 1-2mm) was gently placed into the fresh extraction sockets. The
sockets were covered by PTFE membrane (GBR-200; Osteogenics), which was stabilized
with 4-0 PTFE sutures. No attempt was made to achieve soft tissue closure. Margins of
the membrane were kept submerged subgingivally with the aid of horizontal mattress
sutures. Patients were instructed to take Naproxen sodium 550mg twice daily for 48
hours and as necessary thereafter for analgesia. The membrane was removed after 4
weeks.
The average healing time following ridge preservation procedure prior to implant
placement was 160 days. Following local anesthesia, a full-thickness mucoperiosteal flap
was elevated, the osteotomy sites were prepared to intended diameter and length and
implants were placed according to the manufacturer’s recommendation (Astra Tech). All
implants included in the present study received final prosthesis.
Evaluation
Digital radiographs were taken with the aid of paralleling rings at the time of
implant placement, as well as after final restoration and follow-up annual visits.
Quantitative linear measurements were made on the digital radiographs using VixWin
software (Gendex Imaging). Radiographic images were calibrated to the known distance,
which was the length of the implants. The distance from the alveolar crest to the platform
of the implant (BC-I) and the distance from the implant platform to the first point of
contact with supporting bone (I-FB) were measured at the time of implant placement and
at subsequent visits. All radiographs were quantified by one examiner (IW) (Figure 1).
17
Figure 1. Radiographic landmark
Notes. Radiographic landmarks showing the distance from the alveolar bone crest to the
platform of the implant (BC-I), and the distance from the platform to the first bone-to-
implant contact.
18
Figure 2. Radiographic analysis with VixWin Pro
19
Figure 3. Calibration with VixWin Pro
Note. Calibration was provided by measuring the known distance of the microthreads or
of the implant itself.
The primary outcome evaluated in this study for both implant groups was the
interproximal marginal bone loss, as measured by the distance from implant platform to
the first point of contact with supporting bone. Secondary outcome was remodeling of the
non-supported marginal bone, as measured by the distance from bone crest to implant
platform (BC-I). The tertiary outcome was implant survival rate. The outcomes were
assessed in relationship to the anatomic locations, length and width of the dental
implants.
Follow-up
20
The mean follow-up for the patients who underwent ridge preservation procedure
prior to implant placement was 930 days (range 222-1848 days) and for the healed sites
was 1090 days (range 161-2737 days).
Statistical Analysis
Descriptive statistics using independent t-test was performed to analyze the
available data. The difference in the interproximal bone level between socket grafted and
non-grafted sites were calculated. A p value of < 0.05 was selected as being statistically
significant. The implants that failed over the observation period were not included in the
calculation.
21
Chapter 3: Results
Patient Demographics
One hundred twenty nine patients were eligible for the present study. Seventy-
eight patients required extraction of 105 teeth (socket grafted sites). Fifty-one patients
contributed to 117 healed edentulous sites (non-grafted healed sites). The mean follow-up
time for both groups was 160 days (range 161 to 2737 days).
Table 3. Demographics of the study subjects.
Socket grafted Healed Total
Gender
Female 44 31 75
Male 34 20 54
Ethnicity
African American 1 2 3
Asian 6 7 13
Caucasian 67 41 108
Hispanic 4 1 5
Total 78 51 129
Survival Rate
A total of 682 implants, including the implants from the patient subjects of the
present study, were evaluated to estimate the survival rate of the implants. One hundred
forty seven implants were placed following ridge preservation procedure with anorganic
bovine bone (Bio-Oss). The survival rate of these implants was calculated to be 97.3%.
On the other hand, five hundred thirty five implants were placed in healed edentulous
sites. Five hundred fifteen sites presented with adequate horizontal and vertical ridge
dimension for implant placement without additional bone grafting procedures, whereas
ridge augmentation procedures were required in 20 sites prior to implant therapy. The
22
survival rate of the implants placed in sites without any grafting procedures was 98.5%,
and the survival rate the implants placed in healed ridges in conjunction with additional
bone augmentation procedures was 95%.
Anatomical Location
In the grafted sites, 14 anterior, 28 premolar, and 61 molar teeth were involved.
The corresponding numbers in the non-grafted healed sites were 18 anterior, 30 premolar,
and 69 molar teeth (Table 5).
In the anterior region of the socket-grafted sites (Figure 4), the mean marginal
bone loss (I-FB) was -0.34±0.73mm in the mesial and -0.27±0.44mm in the distal. The
corresponding values in the premolar and molar areas were -0.14±0.47mm, -
0.13±0.25mm, -0.05±0.18mm and 0.01±0.21mm. The mean change of bone loss was
statistically significant between the distal of the anterior and the molar (p<0.05), and
between the premolar and the molar (p<0.01). The mean remodeling of the crestal bone
(BC-I) around the anterior implants was -1.12±1.90mm in the mesial and -0.61±1.00mm
in the distal. The corresponding values in the premolar and the molar implants were -
0.81±0.91mm, -0.82±0.90mm, -0.46±0.93mm, and -0.27±0.86mm. The mean change of
bone remodeling was significant between the distal of the premolar and the molar
implants (p<0.01).
In the non-grafted healed sites, the mean mesial bone loss (I-FB) around the
anterior implants was -0.31±0.38mm, and the mean distal bone loss was -0.27±0.71mm.
The corresponding values in the premolar and molar areas were 0.09±0.45mm,
0.03±0.59mm, -0.02±0.45mm and -0.01±0.41mm. The mean change of bone loss was
23
statistically significant between anterior and the molar in the mesial site (p<0.05) and in
the distal sites (p<0.001). The mean bone remodeling (BC-I) in the anterior region was -
0.84±1.50mm in the mesial and -0.44±1.29mm in the distal. The corresponding values in
the premolar and molar areas were -0.67±0.95mm, -0.29±0.72mm, -0.27±0.77mm, and -
0±0.68mm. The mean change of bone remodeling was statistically significant between
the anterior and molar implants (p<0.05).
Figure 4. Marginal bone loss in the anterior, premolar and molar area.
24
Figure 5: Marginal bone loss in maxilla vs. mandible.
Table 4. Comparison of mean mesial of distal bone changes for socket grafted and healed
sites (p-values).
Δ Mesial Δ Distal
BC-I I-FB BC-I I-FB
Socket sites
Anterior vs. premolar NS NS NS NS
Anterior vs. molar NS NS NS 0.0186
Premolar vs. molar NS NS 0.0073 0.0098
Maxillary vs. mandibular NS NS NS NS
Healed sites
Anterior vs. premolar NS NS NS NS
Anterior vs. molar 0.0004 0.0338 0.0104 0.0012
Premolar vs. molar NS NS NS NS
Maxillary vs. mandibular 0.0416 NS 0.0319 NS
Socket grafted sites vs. healed sites
Initial 0.00044 0.00118 1.45E-08 0.000279
Final 0.0181 NS 0.00178 0.0049
Mean change NS NS 0.0009 NS
25
Implant Length and Diameter
Implant length varied from 8 to 15mm. Implant diameters ranged from 3 to 5mm.
No statistically significant relationships were observed between the degree of marginal
bone loss to implant length and diameter (Table 5).
26
Table 5. Mean mesial and distal bone changes for socket grafted and healed sites
according to tooth type, implant diameter and implant length.
27
In vast majority of sites, the change of marginal bone level was closed to zero in
both socket grafted and non-grafted sites (Figure 6 and 7). The marginal bone levels of
the vast majority of sites appeared stable during the period of observation. During the re-
entry procedure to place the dental implants, none of the sites with prior ridge
preservation required additional bone augmentation procedures.
Figure 6. Mesial and distal bone change from the platform of the implant to first bone-
to-implant contact (I-FB) in the socket grafted sites.
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(#
(%
'#
(# $(# )(# *(# +(# '((# '$(#
!"#$%&''(%
)*+,%
Socket Grafted Sites
,-./01#23045-##
6/.701#23045-#
28
Figure 7. Mesial and distal bone changes from the platform of the implant to first bone-
to-implant contact (I-FB) in the healed sites.
Overall, the mean bone remodeling in the socket-grafted sites was -0.56±1.02mm
and the mean marginal bone loss was -0.09±0.34mm; whereas the mean bone remodeling
in the healed non-grafted sites was -0.29±0.89mm, and the mean bone loss was -
0.06±0.51mm. The differences of crestal bone changes between the two groups were not
statistically significant (p>0.5). However, the difference in the change of bone
remodeling is statistically significant (p<0.05) (Table 6).
Table 6. The mean change in alveolar bone remodeling (BC-I) and mean change in bone
loss around the dental implants (I-FB).
Mean BC-I (mm) Mean I-FB (mm)
Socket grafted sites -0.56±1.02 -0.09±0.34
Healed sites -0.29±0.89 -0.06±0.51
p-value 0.003 0.59
!"#$%
!"%
!$%
!&%
!'#$%
'%
'#$%
&%
$%
'% "'% ('% )'% *'% &''% &"'%
!"#$%&''(%
)*+,%
Healed Sites
+,-./0%12/34,%%
5.-6/0%12/34,%%
29
Chapter 4: Discussion
Previous studies have documented alveolar bone alterations in ridge dimension
following tooth extraction. The reduction of the height and the width of the edentulous
ridge poses a potential challenge to implant therapy since adequate dimension of alveolar
ridge is of fundamental importance for implant placement in an ideal prosthetic position.
In the esthetic area, the mesial and distal crestal bone levels are important in supporting
the interdental papilla. Therefore, minimizing post-extraction remodeling of alveolar
bone could be beneficial in achieving optimal peri-implant health and enhancing overall
aesthetic outcome.
Araujo and Lindhe (2009) evaluated the effect of bovine xenograft on the early
healing phase of extraction sockets in dogs. Of interest was the observation that the
xenograft particles were enclosed in connective tissue coated by multinucleated giant
cells, presumed to be osteoclasts, in the first 2 weeks of healing. At 3-month follow-up,
the multinucleated cells were no longer visible; direct bone apposition of woven bone on
the graft particle was observed. One interpretation of these data is that osteoclasts are
recruited and attempt to resorb the xenograft, but are unsuccessful and leave. Eventually,
osteoblasts are recruited which form bone in direct apposition to the residual xenograft
material. As the bovine bone particles become surrounded by de novo bone, ridge
resorption appears to be delayed (Lindhe et al., 2013).
In view of the above, questions has been raised regarding the effect of bone
substitutes on osseointegration of dental implants. In an animal study, Fiorellini et al.
(2007) investigated the bone-to-implant contact (BIC) following guided bone
regeneration using autogenous bone, demineralized freeze-dried bone allograft
30
(DFDBA), anorganic bovine bone, and tricalcium phosphate. The results revealed high
percentage (50-65%) of bone-to-implant contact with no statistically significant
difference amongst various bone fillers. Regardless of the type of bone grafting materials,
osseointegration of implants can be achieved and maintained. Similar conclusion was
drawn from another case report (Scarano et al., 2004) that described the histological
findings of an implant placed in a sinus augmented with bovine xenograft. The authors
found new bone formation between the implant surface and the bovine xenograft particles
and that all bovine xenograft particles in direct contact with bone. All together,
preliminary evidence suggested that xenograft undergoes slow resorption and serves as
an osteoconductive scaffold for bone apposition. The resorption process does not seem to
compromise osseointegration of dental implants.
The present study assessed the radiographic changes of marginal bone level
around dental implants placed following socket grafting with bovine anorganic bone. The
results demonstrated comparable survival rates of dental implants placed in socket-
grafted vs. non-grafted healed sites over a mean observation period of 3 years. This is in
agreement with previously published studies (Norton and Wilson 2002, Baron, Orlando
et al., 2012, Patel el al., 2013.), despite application of different grafting materials.
Collectively, all implants inserted in socket grafted sites demonstrated good primary
stability and were able to sustain loading following the delivery of the final prosthesis.
Theses findings corroborated with several early studies (Serino et al., 2003, Fiorellini et
al., 2003).
The mean crestal bone loss was in the socket grafted and non-grafted healed sites
were -0.09±0.34mm and -0.06±0.51mm, respectively (Table 5). This indicated that the
31
crestal bone around the microthreaded implants placed following ridge preservation
procedure remained stable over time. Norton and Wilson (2002) observed 0.4-0.5mm of
interproximal marginal bone loss following ridge preservation with bioactive glass.
Crespi et al. (2009) reported 0.12-0.22mm of radiographic bone loss around TPS
implants. More recently, Barone and Orlando et al., (2012) recorded marginal bone loss
of 1.02mm in the control sites and 1.00mm in the test sites using coricocancellous
porcine bone graft. The magnitude of marginal bone loss measured in the current study
was less than what have been previously reported. In an 8-year longitudinal retrospective
study, Chang and Wennstrom (2012) reported mean marginal bone loss of 0.1mm around
microthreaded implants with conical implant-abutment interface. Taken together, the
difference in the amount of bone loss observed could be potentially attributed to the type
of biomaterials and implants used in the studies.
Table 5. The mean change in alveolar bone remodeling (BC-I) and mean change in bone
loss around the dental implants (I-FB).
Mean BC-I (mm) Mean I-FB (mm)
Socket grafted sites -0.56±1.02 -0.09±0.34
Healed sites -0.29±0.89 -0.06±0.51
p-value 0.003 0.59
Variables such as anatomical location, length and diameter of the implants were
considered in subgroup analysis. A general trend seemed to indicate that implants placed
in the anterior region tend to lose more interproximal crestal bone compared to those
placed in the posterior sites. It is not uncommon that implants were inserted deeper in the
anterior sites for esthetic consideration. There was no statistically significant difference
between implants placed in the maxilla vs. those placed in the mandible, except in the
32
distal site of the non-grafted healed ridge. Therefore, implant length and diameter did not
seem to influence the magnitude of marginal bone loss.
One clinical study (Baron, Ricci et al., 2012) found that 42% of sites without
socket grafting required additional bone augmentation procedure, compared to 7% of
sites in the socket-grafted sites. In the current study, since the patients who presented
with healed edentulous sites that required bone augmentation prior to implant placements
were excluded from the study, the relative percentage of sites that need bone
augmentation in the non-grafted ridge remained undetermined.
According to the current study, the survival rates of dental implants placed with or
without ridge preservation procedures were similar. The survival rate of implants placed
in bovine anorganic bone in post-extraction sockets was 97.3%, and the corresponding
value for the implants placed in the sites without socket grafting was 98.5%. In the earlier
studies, the survival rate of implants placed in various bone substitutes ranged from
93.7% to100% (Norton and Wilson, 2002, Sandor et al., 2003, Crespi et al., 2009, Patel et
al., 2009). The survival rate of implants in the present study is in agreement with the
previous research. The difference amongst individual studies may be attributed to study
designs, number of subjects, and length of the follow-up period.
The study was a retrospective in nature; therefore, limited baseline data was
available. It is well documented that most dimensional changes following tooth extraction
occurs in the buccal plate. Since the marginal bone changes were measured from digital
radiographs, the remodeling of buccal plate could not be determined from this study.
Although there are some limitations to the study design, the present study involved larger
patient sample size, greater number of implants placed, and long observation period. It is
33
one of the few studies that documented marginal bone changes following implant
placement in sites that had undergone ridge preservation procedures. Additionally, it is
also one of the first studies that compared implant-related outcomes following socket
grafting in various anatomical sites.
The evidence on peri-implant bone loss following ridge preservation procedure is
very limited. Prospective controlled randomized clinical trials are needed to further reveal
the long-term outcomes of implants placed in grafted bone. Future analysis may be
directed toward the marginal bone changes of implants in single vs. multiple extractions
as well as the influence of systematic conditions on peri-implant bone loss.
34
Chapter 5: Conclusion
The limitations of the present study included: Limited baseline data was
available because of the retrospective nature of the study. Therefore, a true control
group for the experimental group was not available. The bone remodeling of the
buccal plate cannot be determined from the radiographic study. Within the
limitation of the present study, the following conclusions may be reached.
(1) The mean crestal bone loss around implants placed in sites following ridge
perseveration procedure with bovine anorganic xenograft and non-grafted healed
sites were -0.09±0.34mm and -0.06±0.51mm, respectively (NS).
(2) The mean alveolar bone remodeling in the ridge perseveration sites and non-
grafted healed site were -0.56±1.02mm and -0.29±0.89mm, respectively (p<0.05).
(3) The survival rate of the implants placed following ridge preservation was 97.3%,
and the survival rate of the implants placed in non-grafted sites was 98.5%.
(4) Dental implants placed in ridge perseveration sites demonstrated comparable
clinical outcomes as those ones placed in native bone. Therefore the null
hypothesis was rejected.
35
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Abstract (if available)
Abstract
Background: Following tooth extraction, the resorptive process results in altered bony architecture of the alveolar ridge. The dimensional changes of the hard tissue may present a challenge to implant therapy. Various techniques have been proposed to minimize horizontal and vertical resorption. The objective of this retrospective study was to compare the radiographic marginal bone level changes following implant placement in post-extraction sites following ridge preservation with bovine anorganic bone compared with non-grated healed sites. ❧ Methods: One hundred thirty four patients treated from April 2005 to March 2013 were included in the present restrospective study. Seventy-eight patients were treated with reduced-trauma tooth extraction and ridge preservation procedure, which entailed placement of bovine anorganic bone (Bio-Oss large particle size of 1-2mm) covered with PTFE membrane (GBR-200
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Wu, Ivy Hsiao-Han
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Marginal bone response of implants placed in post-extraction sites following ridge preservation with bovine anorganic bone
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School of Dentistry
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Master of Science
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Craniofacial Biology
Publication Date
07/12/2013
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