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This report assesses the results following sinus floor augmentation performed 14 years previously in which bovine bone xenograft material was used without implant insertion. After sinus floor augmentation, using a 20:80 mixture of autogenous bone and inorganic bovine bone material (Bio-Oss), bone biopsy specimens were taken from the grafted site, processed with Donath's sawing and grinding technique, stained with toluidine blue, and mounted on high-sensitivity plates for histology and microradiography. Histologic and microradiographic analysis showed the ingrowth of newly formed bone into the graft with interspersed residual Bio-Oss granules. The percentage of Bio- Oss and newly formed bone was 10.18% and 9.32%, respectively, within a total surface area of 70.61 mm² at the site of the corresponding missing first molar, and the percentage of Bio-Oss and newly formed bone was 11.47% and 14.96%, respectively, within a total surface area of 63.92 mm² at the corresponding missing second molar. The newly formed bone was vital without signs of resorption. This study produced strong evidence that newly formed bone was distributed throughout the bone substitute material around all of its granules and that the grafted site consisted of vital bone even in its central parts. The differences in degradation rate and/or whether the effect of bone graft substitutes alone and/ or in combination with other types, shapes, and sizes of graft materials needs further clinical investigation, especially in regard to long-term changes.
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The International Journal of Periodontics & Restorative Dentistry
Volume 35, Number 4, 2015
541
Mustafa Ayna, DDS PhD, MSc1
Yahya Açil, Prof Dr Rer Nat2
Aydin Gulses, DDS PhD3
Fate of a Bovine-Derived Xenograft in
Maxillary Sinus Floor Elevation After 14 Years:
Histologic and Radiologic Analysis
This report assesses the results following sinus oor augmentation performed
14 years previously in which bovine bone xenograft material was used without
implant insertion. After sinus oor augmentation, using a 20:80 mixture
of autogenous bone and inorganic bovine bone material (Bio-Oss), bone
biopsy specimens were taken from the grafted site, processed with Donath’s
sawing and grinding technique, stained with toluidine blue, and mounted
on high-sensitivity plates for histology and microradiography. Histologic and
microradiographic analysis showed the ingrowth of newly formed bone into
the graft with interspersed residual Bio-Oss granules. The percentage of Bio-
Oss and newly formed bone was 10.18% and 9.32%, respectively, within a total
surface area of 70.61 mm2 at the site of the corresponding missing rst molar,
and the percentage of Bio-Oss and newly formed bone was 11.47% and 14.96%,
respectively, within a total surface area of 63.92 mm2 at the corresponding missing
second molar. The newly formed bone was vital without signs of resorption.
This study produced strong evidence that newly formed bone was distributed
throughout the bone substitute material around all of its granules and that the
grafted site consisted of vital bone even in its central parts. The differences in
degradation rate and/or whether the effect of bone graft substitutes alone and/
or in combination with other types, shapes, and sizes of graft materials needs
further clinical investigation, especially in regard to long-term changes. (Int J
Periodontics Restorative Dent 2015;35:541–547. doi: 10.11607/prd.2135)
Decreases in height and width of
the residual crest following tooth ex-
traction usually necessitate the use
of additional augmentation tech-
niques prior to endosseous dental
implant placement. In the posterior
maxilla, pneumatization of the max-
illary sinus often results in an addi-
tional loss of residual bone volume,
and various sinus oor augmenta-
tion techniques with different graft-
ing materials are usually needed.1–5
Among these grafting materi-
als, different biocompatible and
osteoconductive bone substitutes
were developed and successfully
marketed by various manufacturers
in the past 30 years to reduce the
need for autogenous bone, which
is accepted as the gold standard,
owing to its outstanding biologic
behavior and high survival rates.6
The healing period follow-
ing maxillary sinus bone grafting
depends on the amount of pneu-
matization, residual bone volume,
patient-related factors, and type of
graft material used. If autogenous
bone is used, the healing time can
be shortened (by approximately 4
months). However, in cases when
bone substitutes are used, longer
healing periods would be prudent.2–4
There are numerous articles in
the literature evaluating the sur-
vival rates of implants placed in
grafted maxillary sinuses. A sys-
tematic literature review conrmed
1
Lecturer, Ruhr University Bochum, Bochum, Germany, and Danube University Krems,
Krems, Austria.
2
Professor, Department of Oral and Maxillofacial Surgery, Christian-Albrechts-University,
Kiel, Germany.
3
Associate Professor, Center for Dentistry and Oral Health, Mevki Military Hospital,
Ankara, Turkey.
Correspondence to: Dr Aydin Gulses, Mevki Militar y Hospital, 06130 Diskapi Altindag,
Ankara, Turkey; fax: +903123114609; email: aydingulses@gmail.com.
©2015 by Quintessence Publishing Co Inc.
The International Journal of Periodontics & Restorative Dentistry
542
the positive early results reported
for xenografts.7 In addition, the
survival rates of implants placed
in sinuses grafted with 100% inor-
ganic bovine bone xenografts were
found to be higher than those in
grafts of 100% bone material har-
vested from the iliac crest (95.6%
and 88.0%, respectively). How-
ever, in sinuses grafted with 100%
allografts, the survival rates were
relatively poor (81.0%).8
Bovine bone xenograft is a re-
liable bone graft substitute and re-
portedly exhibits high survival rates
in maxillary sinus augmentation pro-
cedures.9–14 Bovine bone graft sub-
stitutes promote both the formation
and ingrowth of newly formed bone
and blood vessels at the grafted
site. The trabecular bone serves as
a scaffold for osteoblasts and pro-
motes osteoblast differentiation as
well as matrix synthesis.
15 Bio-Oss
(Geistlich) is a well-established de-
proteinized bovine bone xenograft
with high osteoconductive poten-
tial.16,17 Its high-porosity structure
provides an extensive internal sur-
face area of 79.7 m2/g, which is
similar to the natural bone contact
surface area.18 In addition, Bio-Oss
has a calcium phosphate index of
2.03, which precisely matches the
index of natural human bone, ie,
2.03.19
Despite the increasing num-
bers of articles that have evaluated
different bone graft materials in
implant surgery, the clinical rel-
evance of factors such as differ-
ences in degradation rate and/or
whether the effect of bone graft
substitutes alone and/or in com-
bination with other types, shapes,
and sizes of graft materials needs
further clinical investigation, es-
pecially with respect to long-term
changes.
The aim of this report was to
assess the results following sinus
oor augmentation performed 14
years ago with Bio-Oss bone graft
material.
Method and materials
In 1997, a 51-year-old healthy male
patient presented with complaints
of difculty chewing due to his re-
movable maxillary partial denture.
He wanted a xed restoration, so
an implant-supported prosthesis
was proposed. However, the radio-
graphic examination revealed high-
grade bone loss in the left posterior
maxilla; therefore, sinus oor eleva-
tion with bone grafting prior to im-
plant placement was planned.
Autogenous bone harvested
from the retromolar mandible com-
bined with a granular bone substi-
tute with a granule size of 0.25 to
1 mm (Bio-Oss) was selected for
grafting.
A palatal crestal incision was
made, mesial and distal releasing
incisions were performed, and a
full-thickness mucoperiostal ap
was elevated. The lateral sinus wall
was exposed and a 3 × 2-cm corti-
cal bone ap was raised via a dia-
mond round bur without damaging
the sinus membrane. The bone ap
was carefully released from the si-
nus wall and pushed inward and
upward. The sinus membrane re-
mained intact, and the sinus oor
was augmented with a material
consisting of a 20:80 mixture of au-
togenous bone and granular bone
substitute. The grafted sinus oor
was covered with a Bio-Gide mem-
brane (Geistlich) and secured with
three titanium screws (Fig 1). The
surgical eld was primarily closed
via 3-0 silk sutures.
Because the patient spent a
long time abroad, implant place-
ment was delayed for 14 years. In
2011, diagnostic computed tomog-
raphy scans (CT) were obtained
(Fig 2). Three implants were placed
(Nobel Replace 4.3 × 13.0 mm,
Nobel Biocare) at the grafted site
(Fig 3). During implant insertion,
bone was harvested from the origi-
nally grafted sites with a trephine
bur for histologic examination.
Sample processing, sawing,
and grinding
The samples were placed in 10%
formalin for 10 days. Using an au-
tomatic processing station (Pool
of Scientic Instruments [PSI]), the
samples were embedded in meth-
acrylate prior to sawing and grind-
ing. The processing station was
programmed for dehydration in an
ascending series of alcohol, defat-
ting in acetone and embedding in
methacrylate.
Sawing and grinding were per-
formed,20,21 and the samples were
placed in glass vessels lled with a
monomeric resin solution and in-
cubated at 37°C to 40°C for 2 to 4
days for resin impregnation. The
samples were precut with a band
saw (Exakt), and disks of about 100
µm were obtained via an oscillat-
Volume 35, Number 4, 2015
543
ing diamond saw (Exakt), grounded
with the Saphir 360 E grinder (ATM),
and highly polished with silicon
carbide paper (grades 500, 1,200,
2,400, and 4,000).
Staining
Stainings were made with toluidine.
The ground surface was decalci-
ed with 0.1% formic acid, and 20%
methanol was applied for better cell
and soft tissue staining. The sam-
ples were rinsed in distilled water
and stained in a toluidine blue solu-
tion for 2 minutes.
In this process, hard tissue
either did not stain or at best as-
sumed a light blue color, whereas
cells and their nuclei, osteoid, ce-
ment lines, and collagenbers
stained blue, and mast cell gran-
ules, cartilage matrix, and early
wound healing sites metachromati-
cally stained red violet.
Microradiography
The samples were glued onto lm-
coated, light-sensitive glass high-
resolution plates (HRP; Type 1A,
Imtek)—depending on their thick-
nessand exposed to 18 kV and
5 mA for 8 to 10 minutes in the mi-
croradiography chamber (Faxitron
X-ray Systems 43855A, Hewlett
Packard). The lms were developed
with an HRP developer and xed
in an A3000 xation bath (both by
Kodak). After drying, the sensitive
lm layer was covered with a cover
plate and mounted with Eukitt. The
microradiographs were morpho-
metrically evaluated using a digital
image analyzer (Q500MC, Leica).
A measuring frame was placed on
invariably identiable screw holes,
and the surface area of newly
formed bone was measured.
The microradiographs pro-
vided information regarding the
mineralization of the bone formed
following the augmentation pro-
cedure, which is less well mineral-
ized and appears relatively darker
compared to the original, mature
mineralized bone. Information was
obtained regarding the structure
and extent of the newly formed
bone.
Results
Histologic analysis of ground sec-
tions and three-dimensional (3D)
radiography produced the following
evidence:
3D radiography of the grafted
site showed that the original
bone at the prospective
implant site was stable 14
years postgrafting without
signs of resorption (see Fig 2).
No irregularities or perforations
were seen at the surface
facing the maxillary sinus.
Fig 1 Panoramic radiograph of the patient 14 years after the
grafting procedure.
Fig 2 Implants were placed in maxil-
lary left second premolar and rst and
second molars, and single crowns were
cemented onto them.
Fig 3 Computed tomogra-
phy image of the grafted site.
Note that the sinus is well
pneumatized and the graft
is stable.
The International Journal of Periodontics & Restorative Dentistry
544
Histologic analysis of the
toluidine bluestained
samples showed that
nonresorbed residues of the
Bio-Oss granules were still
present 14 years after sinus
oor elevation (Fig 4).
No signs of resorption
were detected even after
the long postgrafting
time, and the bone was
clear of inammation. The
trabeculae at the examined
site were separated by
large voids (see Fig 4).
Bio-Oss acted as a scaffold,
and mature brous bone
formed trabeculae, which
assembled to an interlinked
trabecular structure (see Fig 4).
The histologic examination
revealed that the grafted
site consisted of vital bone
even in its central parts.
The Bio-Oss granules were
embedded in this bone tissue
without causing any irritations
but failed to show signs of
resorption histologically
14 years postgrafting.
• Microradiography conrmed
the high percentage of Bio-Oss
(10.18%) at the site of the
corresponding missing
maxillary left rst molar; while
the amount of newly formed
bone was slightly lower (9.32%)
(Fig 5).
At the site of the correspond-
ing maxillary left second
molar, newly formed bone
exceeded the amount of
Bio-Oss (14.96% and 11.47%,
respectively; Fig 6).
Fig 4 Overview of intact biopsy specimen taken at the rst molar. Note the maturing vital bone with well-developed trabeculae and
brous bone with nonresorbed Bio-Oss granules. (a, b) Detailed view of biopsy specimen. Note that the grafting material (D) is completely
embedded in bone (E). The newly formed bone uses Bio-Oss as a scaffold for interlinking. (c) Dense mature lamellar bone (E) has en-
sheathed a large Bio-Oss granule (D) and sends a trabecular bridge to a smaller Bio-Oss granule.
500 m
abc
D
D
D
E
EE
Volume 35, Number 4, 2015
545
Discussion
Bone regeneration in the maxil-
lary sinus grafted with bovine
bone xenograft was studied quali-
tatively and quantitatively at vari-
able time points postgrafting.22,23
According to the literature, the
sinus graft incorporation could
be estimated at about 1.0 mm
per month with deproteinized bo-
vine bone xenograft. The present
case study aimed to clarify the per-
centage of vital bone and inorganic
bovine bone material 14 years fol-
lowing the sinus grafting procedure.
The amount of vital bone
formed in the sinus after a certain
time is a variable for the compara-
tive assessment of the healing and
osteoconduction potential of graft-
ing or bone substitute materials.
It also has been reported that the
graft maturation could be deter-
mined by assessing the vital new
bone formation.24, 25 Using inorgan-
ic bovine bone material with and
without autogenous bone for sinus
grafting, Froum et al evaluated the
amount of vital bone and reported
a mean volume of 24% after 6 to
9 months and 33% after 12 to 15
months.26 Valentini et al examined
maxillary sinuses grafted with 100%
inorganic bovine bone material and
found that vital bone represented
18.3% mean volume at the end of
6 months and 26.6% at the end of
12 months.27 In the current study,
the histologic examination revealed
that the grafted site consisted of vi-
tal bone even in its central parts. In
addition, a high percentage of Bio-
Oss (10.18%) was found at the site
of the corresponding missing maxil-
lary rst molar, whereas the amount
of newly formed bone was slightly
lower (9.32%). At the site of the cor-
responding maxillary second mo-
lar, newly formed bone exceeded
the amount of Bio-Oss (14.96% and
11.47%, respectively).
In a histologic study performed
by Artzi et al, the amount of newly
formed bone was found to vary
signicantly as a function of the
graft location: In the cranial parts
Fig 5 Microradiograph of the rst molar
showing 9.32% natural bone (E) and
10.18% Bio-Oss (D) within a total surface
area of 70.61 mm2.
Fig 6 Microradiograph of the second molar showing 14.96% natural bone
(E) and 11.47% Bio-Oss (D) within a total surface area of 63.92 mm2.
D
E
D
E
The International Journal of Periodontics & Restorative Dentistry
546
of the graft, increasingly less new
bone was formed, whereas more
new bone was present in the parts
close to the sinus membrane.8 This
was not conrmed by the samples
evaluated for the present study.
Conversely, newly formed bone was
distributed throughout the bone
substitute material around all of its
granules.
A histologic long-term study
over 11 years failed to show any
statistically signicant changes in
the particle size of inorganic bovine
bone material and showed a 17%
increase of a mean bovine bone
matrix.28 In another 11-year study,
little new bone had formed and
bovine bone matrix was found to
have resisted resorption.23 As the
biopsy specimen material available
for these two studies was limited,
the evidence obtained on the dis-
tribution of newly formed bone and
its ingrowth into the graft is bound
to be inconclusive. In addition, the
percentage of new bone should
be reviewed critically; thus, normal
nongrafted local bone also could
be present at the biopsy speci-
men site.23,28 For the current study,
two samples of about 70 mm2 in
size were available. These can be
expected to provide an adequate
cross section of the sinus graft.
Schulten et al29 suggested that
graft materials with a very low re-
sorption rate will not remodel and,
therefore, will not functionally adapt
to surrounding bone, which might
result in negative mechanical cues.
Slow or even a lack of resorption of
graft material prevents its replace-
ment by new bone, which may
hamper proper and timely bone-to-
dental implant interface formation.
This may result in lower implant sur-
vival. It also has been stated that Bio-
Oss degrades very slowly30 and no
clinical signs of resorption are seen
up to 6 years postgrafting.21 The
current study showed that nonre-
sorbed residues of Bio-Oss granules
were still present 14 years after sinus
oor elevation. This might be attrib-
uted to a slow osteoclast-mediated
resorption rather than spontaneous
resorption.
Conclusions
This study produced strong evi-
dence showing that newly formed
bone was distributed throughout
the bone substitute material around
all of its granules and that the graft-
ed site consisted of vital bone even
in its central parts. In addition, Bio-
Oss granules had not been com-
pletely resorbed, even after 14 years
in situ.
In the authors’ opinion, the dif-
ferences in degradation rate and/
or whether the effect of bone graft
substitutes alone and/or in combi-
nation with other types, shapes, and
sizes of graft materials needs further
clinical investigation, especially with
respect to long-term changes.
Acknowledgments
The authors reported no conicts of interest
related to this study.
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... 15 Due to the large volume of studies in which Geistlich Bio-Oss was used, this biomaterial is well established among the bone substitutes. 8,[16][17][18] Criteria Lumina Bone Porous does not have the same level of scientific evidence, even though its use has been authorized by local regulatory agencies, and more studies are needed regarding this material. Furthermore, there are differences between the above-mentioned bone substitutes in terms of processing. ...
... A clinical case report revealed the presence of the biomaterial 14 years after grafting. 16 In the histomorphometric analysis of two biopsies collected during the implant placement, the authors showed 10.18% of Geistlich Bio-Oss residue at the first implant site and 11.47% at the second. 16 Although these values are lower than those of the present study, it is interesting to note that the bovine bone substitute remained in the grafted area for a long time, thus allowing the placement of implants without additional procedures. ...
... 16 In the histomorphometric analysis of two biopsies collected during the implant placement, the authors showed 10.18% of Geistlich Bio-Oss residue at the first implant site and 11.47% at the second. 16 Although these values are lower than those of the present study, it is interesting to note that the bovine bone substitute remained in the grafted area for a long time, thus allowing the placement of implants without additional procedures. Therefore, it can be suggested that the Cri-teria Lumina Bone Porous may present similar long-term stability since a mean of 22.89 ± 4.58% of biomaterial particles was detected after a period of 6 months, allowing the implant placement and suggesting the slow resorption of the product. ...
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Objective: This study analyzed two xenogenous biomaterials based on deproteinized bovine bone mineral applied for maxillary sinus elevation. Method and materials: Fourteen patients were submitted to maxillary sinus augmentation with one of the following biomaterials: Criteria Lumina Bone Porous (test group) or Geistlich Bio-Oss (control group), both of large granules (1 to 2 mm). After 6 months, trephine biopsies were collected at the time of implant placement: 27 samples (11 patients) in the test group; 7 samples (3 patients) in the control group. Biopsies were analyzed by descriptive histology and histomorphometry, in which the percentages of newly formed bone, residual biomaterial particles, and connective tissue were evaluated. Results: Histomorphometry showed means for test and control groups, respectively, of 32.41% ± 9.42% and 26.59% ± 4.88% for newly formed bone, 22.89% ± 4.58% and 25.00% ± 4.81% for residual biomaterial, and 44.70% ± 9.54% and 48.41% ± 3.36% for connective tissue. There were no differences between groups (P > .05). Conclusion: This study concluded that Criteria Lumina Bone Porous presented similar histologic and histomorphometric characteristics to Geistlich Bio-Oss 6 months after sinus elevation surgery, identifying the tested biomaterial as an interesting alternative for bone augmentation in the maxillary sinus. .
... 18,19 Furthermore, osseointegration combined with no or minimal resorption has been reported. 8,15,20,21 The use of Bio-Oss has been well established in ridge augmentation and sinus grafting as part of dental implant placement procedures. 20,21 Cerabone (botiss biomaterials) is a sintered DBBM with a bone-like trabecular structure and was recently introduced into dental procedures. ...
... 8,15,20,21 The use of Bio-Oss has been well established in ridge augmentation and sinus grafting as part of dental implant placement procedures. 20,21 Cerabone (botiss biomaterials) is a sintered DBBM with a bone-like trabecular structure and was recently introduced into dental procedures. 5 Cerabone is sintered at a high temperature (> 1,200°C), resulting in a highly crystalline hydroxyapatite mineral phase of low bioresorbability. ...
... 34 The slow resorption of DBBM has been further confirmed by long-term studies of the control DBBM and comparative clinical studies of test and control DBBMs. 20,21,25,26 In a split-mouth, bilateral sinus augmentation study of test and control DBBMs, bone formation in both groups was comparable after 8 months, while the resorption of the DBBM in both groups was reported as very low. 25 An earlier investigation comparing both materials in the same indication at 8 months and 1 and 4 years after surgery showed a significantly higher volumetric loss for the control compared with the test material, which was most pronounced after 4 years. ...
Article
Purpose: The aim of this study was to evaluate and compare bone growth and implant integration in circumferential defects with two commercially available bone substitutes (demineralized bovine bone mineral [DBBM]). Materials and methods: Circumferential defects were created in the mandibles of minipigs (n = 10), and Bone Level Tapered implants (Straumann Roxolid with SLActive surface) were placed. The defects (4-mm-deep circumferential defect, 2 mm around each implant) were augmented with either sintered bovine bone mineral (test, cerabone) or natural bovine bone mineral (control, Bio-Oss). Bone formation and tissue composition in augmented sites were histomorphometrically assessed after 8 and 12 weeks of healing time (n = 5 each), respectively, in terms of the percentage of area of newly formed bone to total area, bone-to-implant contact (BIC), and crestal bone height relative to the implant shoulder (first bone-to-implant contact [fBIC]). Results: Bone formation in all defect sites was adequate and equivalent for both groups at individual healing time points. The amount of residual graft material was comparable in both groups after 8 and 12 weeks, with no significant resorption in either group. The mean newly formed bone area in the test group amounted to 46.7% ± 5.1% and 48.7% ± 4.0% after 8 and 12 weeks vs 47.0% ± 4.8% and 47.8% ± 7.3% in the control group, respectively. BIC and fBIC as individually assessed for the lingual and buccal aspects were comparable at both healing time points without any statistically significant differences between the groups. A slightly greater variability of fBIC was observed within the test group. Conclusion: The results of this study indicate that test and control materials both represent viable bovine bone graft material that equivalently support the formation of new and stable bone volume specifically when used for simultaneous augmentation around implants.
... [6] However, no scientific article or clinician has ever demonstrated the complete biodegradation and replacement of the bovine bone substitutes in humans. [7][8][9] On the contrary, the presence of bovine bone particles without significant size change has been found in humans even after 20 years. [10] Evidence suggests that the human host is unable to biodegrade the xenograft particles. ...
Article
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The long-term safety of xenografts and their potential association with disease are valid concerns. Bovine bone substitutes which are by far the most commonly used xenografts in dentistry are not biodegradable. The aim of the present report was to raise awareness on the long-term risks of the bovine-derived xenografts. Patients who experienced clinical complications after xenografting are reported. Patients' demographic, significant medical, and dental findings are reported. Complications included migration/encapsulation/displacement of the graft material, chronic inflammation, and soft-tissue disturbances/fenestrations. Albeit some xenograft complications are not significant enough to compromise the initial outcomes achieved, the xenografted particles seemed to be left intact favoring conditions for migration. The authors observed the inability of the human host to biodegrade the xenograft particles. The intact/migrated bovine bone particles present a risk to patients and may contribute to long-term clinical complications in implant dentistry.
... Many synthetic bone-grafting materials, such as biphasic calcium phosphate (Straumann Boneceramic ® ) [5], hydroxyapatite crystallites (NanoBone ® ) [6], deproteinized bovine bone (Bio-Oss ® ) [7] have been widely used for MSFA to enhance bone formation [8,9]. These commercially available bone-grafting materials, however, have some disadvantages or limitations, such as prolonged inflammatory response, mucosa membrane tears especially for trans-crestal sinus floor augmentation, host limitations in dealing with large volumes of materials and longer conversion times [6,[10][11][12]. Most of these materials are not a good carrier for growth factors to achieve sustained release of the growth factors in order to effectively accelerate bone formation using the growth factors in vivo. ...
... 42 Moreover, there are in vivo clinical evidences in maxillary sinus surgery, showing the remodelling of the grafting material with the patient's newly formed bone. 22 It is noteworthy that the results are consistent with those of studies using partially non-resorbable anorganic bovine bone obtained by thermal treatment, 15,[43][44][45][46] which was considered to be more effective for long-term preservation of volume. The results of the present study showed how, using enzyme-treated equine xenografts, volume preservation was possible during 13 years of follow-up, even though the grafting material was not obtained using mineral-modifying thermal treatment. ...
Article
Aim: The aim of this study is to investigate the effectiveness of a combination of an equine-derived, enzyme-treated bone graft and an equine collagen membrane to treat intrabony defects caused by periodontitis. Materials and methods: About 22 patients with a single 1-, 2-, or 3-wall intrabony defect and a probing pocket depth (PPD) of ≥5 mm, who were treated using an enzyme-deantigenated equine bone graft in addition to a collagen membrane and were followed up for at least 10 years, were retrospectively assessed. The plaque index (PI), the sulcus bleeding index (SBI), PPD, and the clinical attachment level (CAL) at each follow-up visit were compared to baseline. Results: The mean PI, SBI, PPD, and CAL were 0.22 ± 0.41, 1.86 ± 0.78, 7.86 ± 1.39 mm, and 8.84 ± 1.86 mm, respectively, at baseline, and 0.25 ± 0.44, 0.12 ± 0.32, 2.59 ± 0.50, and 4.04 ± 0.77 mm, respectively, at the last follow-up. The difference was significant for all parameters (p < 0.001) except PI (p = 0.83). The final CAL gain was 4.8 mm (49.8%). The SBI, PPD, and CAL still significantly improved at the 12-month follow-up visit but not at the 24-month follow-up visit. There were no correlations between either the number of defect walls or smoking and outcomes. In one case, a surgical re-entry at 5 years allowed a clinical evaluation, showing that intrabony defect was repaired with the newly formed bone of the patient. Conclusion: Equine bone granules in addition to an equine collagen membrane effectively and safely treated intrabony defects caused by periodontitis providing long-term results. Clinical significance: Equine-derived bone grafts have been in the market for more than 20 years. However, to the author's knowledge, no studies have reported long-term results for the use of this type of bone graft in periodontal surgery. The equine-derived bone granules used in the present study appears a promising option for treating intrabony defects due to moderate to severe periodontitis.
... 37 Although it has been statistically and radiologically proven to exhibit significant effectiveness when employed in GTR, GBR and maxillary sinus augmentation, [38][39][40] some reports argued its indifference compared with GTR alone in 1-or 2-wall intra-bony defects 41 and resorption resistance in the long term (more than 3 years). 42,43 Our mCT and histological results also showed the stability of Bio-Oss s at 16 weeks, whereas massive pre-mature bone matrix with abundant vessels and smaller residual materials were observed in the TCP@CSi-Mg10 and TCP@CSi-Mg10-p30 groups. Accordingly, in this model of rabbit alveolar bone defect, it was demonstrated that the dimensionally and temporally tailored phase distribution and porous network modification of the spherical granules exhibited superiority in dynamic osteogenic ion release and biodegradation rate relative to the conventional bone substitutes. ...
Article
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Alveolar bone defects, which are characterized by a relatively narrow space and location adjacent to the cementum, require promising substitute biomaterials for their regeneration. In this study, we introduced novel yolk–shell biphasic bio-ceramic granules with/without a customized porous shell and evaluated their biological effect together with structural transformation. Firstly, a self-made coaxial bilayer capillary system was applied for the fabrication of granules. Secondly, thorough morphological and physicochemical characterizations were performed in vitro. Subsequently, the granules were implanted into critical-size alveolar bone defects (10 × 4 × 3 mm) in New Zealand white rabbits, with Bio-Oss® as the positive control. Finally, at 2, 4, 8, and 16 weeks postoperatively, the alveolar bone specimens were harvested and assessed via radiological and histological examination. Our results showed that the yolk–shell biphasic bio-ceramic granules, especially those with porous shells, exhibited a tunable ion release performance, improved biodegradation behavior and satisfactory osteogenesis compared with the homogeneously hybrid and Bio-Oss® granules both in vitro and in vivo. This study provides the first evidence that novel yolk–shell bio-ceramic granules, on account of their adjustable porous microstructure, have great potential in alveolar bone repair.
... Many synthetic bone-grafting materials, such as biphasic calcium phosphate (Straumann Boneceramic ® ) [5], hydroxyapatite crystallites (NanoBone ® ) [6], deproteinized bovine bone (Bio-Oss ® ) [7] have been widely used for MSFA to enhance bone formation [8,9]. These commercially available bone-grafting materials, however, have some disadvantages or limitations, such as prolonged inflammatory response, mucosa membrane tears especially for trans-crestal sinus floor augmentation, host limitations in dealing with large volumes of materials and longer conversion times [6,[10][11][12]. Most of these materials are not a good carrier for growth factors to achieve sustained release of the growth factors in order to effectively accelerate bone formation using the growth factors in vivo. ...
Article
Objective Maxillary sinus floor augmentation (MSFA) is commonly used to increase the alveolar bone height in the posterior maxilla before implant placement. In the present study, we evaluated if the injectable thermosensitive chitosan/β-sodium glycerophosphate disodium salt hydrate/gelatin (CS/GP/GA) hydrogel carried erythropoietin (EPO) could enhance the new bone formation for MSFA in vivo. Methods EPO-CS/GP/GA hydrogel was prepared by ionic crosslinking. Then, characteristics of EPO-CS/GP/GA were evaluated by morphology, injectable property and pH on the gelling time (GT). The release profile of EPO was evaluated by enzyme linked immunosorbent assay (ELISA), and effects of EPO on proliferation and osteoblastic differentiation of bone marrow stromal cells (BMSC) were analyzed by 3-[4,5-dimethylthiazol-2-yl]-2,5-diphenyl tetrazolium bromide (MTT) and reverse transcription quantitative real-time PCR (RT-qPCR), respectively. Finally, EPO-CS/GP/GA was injected into the maxillary sinus floor of the rabbit to test the potential application for MSFA. Results Results showed that GT was decreased with the increase of pH value. The GT was 110 ± 15 s at pH 7.0. SEM images showed that the CS/GP/GA hydrogel had a sponge network structure. Results from ELISA assay revealed that the cumulative release of EPO from the EPO-CS/GP/GA hydrogel reached 67% at 4 h, and 94% at 15 days. MTT assay showed that EPO within EPO-CS/GP/GA hydrogel could significantly promote proliferation of BMSCs compared to control group (p < 0.001) . Results of RT-qPCR assays demonstrated that the expression of Sp7, Runx2, Col I and Alp were significantly increased from EPO-CS/GP/GA group compared to control group on day 14 (p < 0.001). Importantly, EPO-CS/GP/GA hydrogel could significantly induce bone formation (81.98 mm³) compared with control group (43.11 mm³) after 12 weeks post-implantation in vivo. The calculation of thickness of mesenchymal condensation indicated that thickness of mesenchymal condensation was significantly increased from EPO-CS/GP/GA group (∼121.4 μm) compared to control group (∼37 μm) resulting in enhancing intramembranous ossification. Significance The EPO-CS/GP/GA hydrogel provides a novel strategy for MSFA with a minimally invasive way.
... 16 Ayna y su equipo mostraron la presencia de partículas residuales de hueso bovino en humanos después de 14 años. 17 Además, Traini y su grupo reportaron partículas residuales de hueso bovino anorgánico después de 20 años en una evaluación clínica y biológica en humanos. 18 De acuerdo con nuestras observaciones, también se han informado reacciones de cuerpos extraños al hueso bovino anorgánico. ...
Article
Abstract This case report describes the successful ten‐years interdisciplinary treatment of ankylosed upper central incisors with an anterior vertical ridge defect. This treatment was challenging as ankylosis was present before the growth spurt. Orthodontic treatment in association with decoronation, a xenogeneic bone graft, an autogenous sub‐epithelial connective tissue graft, and implant placement were performed to correct the vertical ridge defect and to re‐establish appropriate function, gingival health and aesthetics. Decoronation performed during the growth spurt was the key to avoiding alveolar ridge deformity.
Article
Recently, a technical note describing a promising method for the management of infections after sinus bone grafting by irrigating the corresponding area with hydrogen peroxide based solution with an aid of a drain has been published. The aim of this paper was to present the histological and radiological results of the above mentioned technique. A total of 17 patients who have presented with infections secondary to sinus bone grafting enrolled in the study. During implant placement, bone was collected from the originally grafted site with a trephine burr for radiological examination via micro-computed tomography and histological examination. According to the results of the current study, Bio-Oss acted as a scaffold, and mature fibrous bone formed trabeculae, which assembled to an interlinked trabecular structure. Average results obtained from the microradiography confirmed the higher percentage of Bio-Oss (27.21% ± 3.31%) at the corresponding area; whereas the amount of newly formed bone was slightly lower (6.79% ± 1.13%) As a conclusion, this simple and minimally invasive technique might be beneficial in avoiding removal of bone graft material and could help in rescuing the former laborious procedure.
Article
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Retrospective data from sinus floor augmentation bone grafts were collected from 38 surgeons for 1007 sinus grafts that involved the placement of 2997 implants over a 10-year period, with the majority of the implants followed for 3 years or more postrestoration. There were 229 implant failures reported. Various root-form implants and grafting modalities were used. A consensus conference was organized to evaluate the data and reach a consensus on optimal treatment protocols. The complete database demonstrated a 90.0% success rate for implants placed in sinus grafts with at least 3 years of function. Differences in grafting materials, implant surfaces, and timing protocols were statistically analyzed. However, the database was so multivariate and multifactorial that it was difficult to draw definitive conclusions; these must await controlled prospective studies. The consensus conference therefore developed and voted on multiple consensus statements derived by committee review for bone graft materials, type of implants, timing for implant placement, failure analysis, radiographic analysis, indications/contraindications, prosthetics, and nomenclature. Several consensus statements were obtained, the most significant being that the sinus graft should now be considered a highly predictable and effective therapeutic modality.
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Bone replacement grafts (BRG) are widely used in the treatment of periodontal osseous defects; however, the clinical benefits of this therapeutic practice require further clarification through a systematic review of randomized controlled studies. The purpose of this systematic review is to access the efficacy of bone replacement grafts in proving demonstrable clinical improvements in periodontal osseous defects compared to surgical debridement alone. What is the effect of bone replacement grafts compared to other interventions on clinical, radiographic, adverse, and patient-centered outcomes in patients with periodontal osseous defects? The computerized bibliographical databases MEDLINE and EMBASE were searched from 1966 and 1974, respectively, to October 2002 for randomized controlled studies in which bone replacement grafts were compared to other surgical interventions in the treatment of periodontal osseous defects. The search strategy included screening of review articles and reference lists of retrieved articles as well as hand searches of selected journals. All searches were limited to human studies in English language publications. Non-randomized observational studies (e.g., case reports, case series), publications providing summary statistics without variance estimates or data to permit computation, and studies without BRG intervention alone were excluded. The therapeutic endpoints examined included changes in bone level, clinical attachment level, probing depth, gingival recession, and crestal resorption. For purposes of meta-analysis, change in bone level (bone fill) was used as the primary outcome measure, measured upon surgical re-entry or transgingival probing (sounding). 1. Forty-nine controlled studies met eligibility criteria and provided clinical outcome data on intrabony defects following grafting procedures. 2. Seventeen studies provided clinical outcome data on BRG materials for the treatment of furcation defects. 1. With respect to the treatment of intrabony defects, the results of meta-analysis supported the following conclusions: 1) bone grafts increase bone level, reduce crestal bone loss, increase clinical attachment level, and reduce probing depth compared to open flap debridement (OFD) procedures; 2) No differences in clinical outcome measures emerge between particulate bone allograft and calcium phosphate (hydroxyapatite) ceramic grafts; and 3) bone grafts in combination with barrier membranes increase clinical attachment level and reduce probing depth compared to graft alone. 2. With respect to the treatment of furcation defects, 15 controlled studies provided data on clinical outcomes. Insufficient studies of comparable design were available to submit data to meta-analysis. Nonetheless, outcome data from these studies generally indicated positive clinical benefits with the use of grafts in the treatment of Class II furcations. 3. With respect to histological outcome parameters, 2 randomized controlled studies provide evidence that demineralized freeze-dried bone allograft (DFDBA) supports the formation of a new attachment apparatus in intrabony defects, whereas OFD results in periodontal repair characterized primarily by the formation of a long junctional epithelial attachment. Multiple observational studies provide consistent histological evidence that autogenous and demineralized allogeneic bone grafts support the formation of new attachment. Limited data also suggest that xenogenic bone grafts can support the formation of a new attachment apparatus. In contrast, essentially all available data indicate that alloplastic grafts support periodontal repair rather than regeneration. 4. The results of this systematic review indicate that bone replacement grafts provide demonstrable clinical improvements in periodontal osseous defects compared to surgical debridement alone.
Article
Fragestellung: Die Oberfläche sowie die Mikro- und Mesoporosität von Knochenersatzmaterialien beeinflussen deren chemische und biologische Eigenschaften. Daher wurden in dieser Untersuchung die Größe der spezifischen Oberfläche sowie die Verteilung der Porendurchmesser (Poren < 1 μm) in Knochenersatzmaterialien bestimmt. Material und Methode: Die untersuchten Hydroxylapatite waren synthetischen, bovinen und phytotrophen Ursprungs. Die Trikalziumphosphate und die Biogläser umfassten nur rein synthetische Materialien. ¶Die Gasadsorptionsuntersuchung je einer Probe erfolgte mit Hilfe eines volumetrischen N 2 -Kr-Systems (ASAP 2010, Micromeritics). Zusätzlich wurde für Materialien mit spezifischen Oberflächen ¶> 2 m 2 /g die Porengrößenverteilung nach der BJH-Methode ermittelt. Ergebnisse: 1. Spezifische Oberfläche: 2 der Materialien zeigten eine auffallend große spezifische Oberfläche (BioOss 79,7 m 2 /g, Algipore neu 14,6 m 2 /g). Eine mittlere Oberfläche zeigten Algipore alt (4,9 m 2 /g) und Interpore 200 (2,64 m 2 /g). Die übrigen Materialien zeigten nur kleine Oberflächen (Ceros 80 1,8 m 2 /g, Ceros 82 ¶1,31 m 2 /g, Cerasorb 1,2 m 2 /g, Biobase 0,7 m 2 /g, Endobone 0,7 m 2 /g, Perioglas 0,6 m 2 /g, Allotropat 50 0,2 m 2 /g, Biogran 0,2 m 2 /g). 2. Häufigkeitsverteilung des Porendurchmessers: Die Materialien mit großen und mittleren spezifischen Oberflächen zeigten folgende Porendurchmesser: BioOss 2–50 nm, Algipore neu 2–¶100 nm, Algipore alt 5–50 nm, Interpore 200 2–100 nm. Porengrößen < 2 nm fanden sich kaum. Schlussfolgerungen: Die Materialien BioOss, Algipore alt und neu und Interpore 200 haben ein großes interkonnektierendes Mesoporensystem (Durchmesser < 1 μm). Für die Materialien Biobase, Endobone, Perioglas, Allotropat 50 und Biogran ist dies nicht anzunehmen. Die Materialien Ceros 80, Ceros 82 und Cerasorb zeigen eine dazwischen liegende spezifische Oberflächengröße und weisen einen mäßigen Anteil von solchen interkonnektierenden Poren auf. Ein Einfluss der interkonnektierenden Porosität und der deutlich unterschiedlichen spezifischen Oberflächen auf das Verhalten der Knochenersatzmaterialien in vivo ist nahe liegend. The surface area and the microporosity of bone regeneration materials influence their chemical and ¶biological properties. Therefore, the size of the specific surface area and the distribution of the pore diameters (pores < 1 μm) of bone regeneration materials were analyzed within this study. The analyzed hydroxyapatites were of synthetic, bovine, and phytotroph origin. The tricalcium phosphates and the bioglasses included only synthetic materials. The gas adsorption of each specimen was analyzed using a volumetric N2/Kr system (ASAP 2010, Micromeritics). Additionally, for materials with a specific surface area (> 2 m2/g) the pore size distribution was evaluated by the BJH-method. Two of the ¶materials evaluated astonishingly large dimensions of the specific surface area (BioOss 79.7 m2/g, Algipore new 14.6 m2/g). A medium ¶surface area was found for Algipore old (4.9 m2/g) and Interpore200 ¶(2.64 m2/g). All other included materials showed only small sizes of the specific surface area (Ceros80 ¶1.8 m2/g, Ceros82 1.31 m2/g, Cerasorb 1.2 m2/g, Biobase 0.7 m2/g, Endobone 0.7 m2/g, Perioglas 0.6 m2/g, Allotropat50 0.23 m2/g, Biogran ¶0.2 m2/g). The materials with large and medium sizes of the specific surface area evaluated the following pore diameters: BioOss 2–50 nm, Algipore new 2–100 nm, Algipore old 5–50 nm, Interpore200 2–100 nm. Pore sizes less than 2 nm were not found in relevant numbers. The materials BioOss, old and new Algipore, and Interpore200 contain a large interconnecting mesopore system (diameter < 1 μm). For the materials Biobase, Endobone, Perioglas, Allotropat 50, and Biogran this cannot be assumed. The materials Ceros80, Ceros82, and Cerasorb evaluated a specific surface area between those and might include only a small part of these interconnecting pores. An influence of the interconnecting porosity and the different sizes of the specific surface areas on the biological behavior of the bone regeneration materials can be suggested.
Article
Objective: The purpose of the present study was to histologically and histomorphometrically evaluate the long-term tissue response to deproteinized bovine bone (DPBB) particles used in association with autogenous bone and to compare particle size after 6 months and 11 years, in the same patients, in order to determine possible resorption. Material and methods: Twenty consecutive patients (14 women and six men) with a mean age of 62 years (range 48–69 years) with severe atrophy of the posterior maxilla were included in this study. Thirty maxillary sinuses with <5 mm subantral alveolar bone were augmented with a mixture of 80% DPBB and 20% autogenous bone. Eleven years (mean 11.5 years) after augmentation, biopsies were taken from the grafted areas of the 11 patients who volunteered to participate in this new surgical intervention. The following histomorphometrical measurements were performed in these specimens: total bone area in percentage, total area of the DPBB, total area of marrow space, the degree of DPBB–bone contact (percentage of the total surface length for each particle), the length of all DPBB particles and the area of all DPBB particles. The length and the area of the particles were compared with samples harvested from the same patients at 6 months (nine samples) and pristine particles from the manufacturer. Results: The biopsies consisted of 44.7±16.9% lamellar bone, 38±16.9% marrow space and 17.3±13.2% DPBB. The degree of DPBB to bone contact was 61.5±34%. There were no statistically significant differences between the length and area of the particles after 11 years compared with those measured after 6 months in the same patients or to pristine particles from the manufacturer. Conclusion: DPBB particles were found to be well integrated in lamellar bone, after sinus floor augmentation in humans, showing no significant changes in particle size after 11 years. To cite this article: Mordenfeld A, Hallman M, Johansson CB, Albrektsson T. Histological and histomorphometrical analyses of biopsies harvested 11 years after maxillary sinus floor augmentation with deproteinized bovine and autogenous bone. Clin. Oral Impl. Res. 21, 2010; 961–970. doi: 10.1111/j.1600-0501.2010.01939.x
Article
A new sawing-grinding method is described for the histological evaluation of jaw bones with teeth or bones containing implants (ceramic or metallic). The undecalcified bone is embedded in acrylic resin and sawed at 100 to 150 micrometers. The slices are ground automatically by a special machine to a thickness of 5-10 micrometers. The usually employed staining procedures for hard plastic embedded-tissues may be used. Plaque, fillings, crowns, bridges, implants and soft tissues are preserved in situ. Macroscopic and microscopic detail of good quality is preserved for histological and morphometrical evaluation.
Article
Since the initial application of sinus lift augmentation and implant placement in the mid-1970s, there have been some variations in technique used and graft material applied. Although most authors continue to use the lateral wall, Caldwell-Luc approach, less invasive procedures such as the osteotome procedure for sinus elevation, graft, and implant placement have been proposed. Many authors use iliac crest bone that is of both a cancellous and cortical nature. However, due to the high morbidity rate of this procedure, other donor sources are explored in this review. Good success rates are shown with intraoral bone and combinations of intraoral bone with both resorbable and nonresorbable materials. Varying results are reported with demineralized freeze-dried bone, although its use in combination with hydroxyapatite seems to improve its effectiveness. All reports of clinical success are relatively short term (6 years to 6 months). Medication recommendations and posttreatment prosthetic care are covered.
Article
To study in detail the performance of deproteinized cancellous bovine bone (DPBB, Bio-Osso) granules as a bone substitute, a histomorphometric was performed on five patients treated with DPBB for reconstruction of the severely atrophic maxilla. DPBB was used as mixture with autogenous bone particles, in concentrations that increased from 20% to 100% DPBB, with the time of healing increasing accordingly from 5 to 8 months. A total of 20 vertical biopsies was taken at the time of fixture installation and used for histomorphometry as undecalcified Goldner stained sections. The results show that in all cases, the DPBB granules had been interconnected by bridges of vital newly formed bone. The volume of bone in the grafted area correlated inversely with the concentration of DPBB grafted, and varied between 37% and 23%. However, the total volume of mineralized material (bone plus DPI3B granules) remained within the same range in all five patients (between 53% and 59%). The high values for osteoid and resorption surface, and the presence of tartrate-resistant acid phosphatase-positive multinucleated osteoclasts in resorption lacunae, indicated that bone remodeling was very active in all grafts. Osteoclasts were also observed in shallow resorption pits on DPBB surfaces. The percentage DPBB surface in contact with bone remained stable at about 35% and could not be related to the proportion of DPBB grafted. Although the number of patients examined was limited, the data suggest that deproteinized cancellous bovine bone, preferably combined with autogenous bone particles, is a suitable material for sinus floor elevation in the severely atrophic human maxilla.
Article
This study was designed to investigate the responses of bone cells to a deproteinized bovine bone material, Bio-Oss (Geistlich-Pharma, Wolhunsen, Switzerland), which was grafted in artificial bone defects of rat femurs. Standardized bone defects in the cortical bone of the right femurs were grafted with Bio-Oss particles. Narrow penetrations were prepared on the bottom of the cavity, enabling osteogenic cells to migrate from the bone marrow. A defect in the left femur without Bio-Oss was used as a control. The treated femurs were histochemically examined at 1, 3, 5, 7, and 14 days after the operation. At day 1, no osteogenic migration into the cavities occurred in either the control or experimental groups. At day 3, alkaline phosphatase (ALPase) immunohistochemistry showed a migration of the positive cells at the bottom of the cavities of the experimental groups, but not in the control ones. At day 5, new bone formation was recognized at the bottom of the cavity of both groups. In the experimental group, ALPase-positive cells were localized on Bio-Oss and/or on the thin bone matrix that covered this material. The superficial layer of Bio-Oss underlying the newly formed bone exhibited osteocalcin immunoreactivity. Transmission electron microscopy revealed osteoblasts depositing bone matrices--including collagen fibers--on the surface of Bio-Oss. At days 7 and 14, woven bone occupied the previous cavities of both control and experimental groups, accompanied by osteoclasts. Thus, Bio-Oss appears to serve as a scaffold for osteogenic cells as well as to promote osteoblastic differentiation and matrix synthesis.
Article
Bone replacement substitutes are almost unavoidable in augmentation procedures such as sinus grafting. The objective of the present study was to evaluate the osteoconductive capability of two different scaffold fillers in inducing newly formed bone in this procedure. Sinus floor augmentation and implant placement were carried out bilaterally in 12 patients. Bovine bone mineral (BBM) was grafted on one side and beta-tricalcium phosphate (beta-TCP) on the contralateral side. Both were mixed (1:1 ratio) with autogenous cortical bone chips harvested from the mandible by a scraper. Hard tissue specimen cores were retrieved from the augmented sites (at the previous window area) at 12 months. Decalcified sections were stained with haematoxylin-eosin and the fraction area of new bone and filler particles was measured. In addition to the effect of the filler on new bone formation, the latter was tested to determine whether it correlated with the tissue depth and residual amount of the grafted material. Bone area fraction increased significantly from peripheral to deeper areas at both grafted sites in all cores: from 26.0% to 37.7% at the beta-TCP sites and from 33.5% to 53.7% at the BBM-grafted sites. At each depth the amount of new bone in BBM sites was significantly greater than that in TCP sites. However, the average area fraction of grafted material particles was similar in both fillers and all depth levels (beta-TCP=27.9-23.2% and BBM=29.2-22.6%, NS). A significant negative correlation was found between bone area fraction and particle area fraction at the middle (p=0.009) and deep (p=0.014) depths in the beta-TCP sites, but not at the BBM sites. At 12 months post-augmentation, the two examined bone fillers, beta-TCP and BBM, promoted new bone formation in sinus grafting but the amount of newly formed bone was significantly greater in BBM-grafted sites. However, both exhibited similar residual grafted material area fraction at this healing period. This could imply that BBM possesses better osteoconductive properties.