STARCH-JENSEN ET AL IMPLANT DENTISTRY / VOLUME 27, NUMBER 3 2018 1

Maxillary Sinus Floor Augmentation With

Synthetic Bone Substitutes Compared
With Other Grafting Materials: A
Systematic Review and Meta-analysis
Thomas Starch-Jensen, DDS, PhD,* Arne Mordenfeld, DDS, PhD,†‡ Jonas Peter Becktor, DDS, PhD (DrMed),§
and Simon Storgård Jensen, DDS, Dr. Odont¶

axillary sinus floor augmenta- Objective: To test the hypotheses based implant survival rate of 0.98

M tion (MSFA) using the lateral

window technique is the most
commonly used method to increase the
alveolar bone height in the posterior
maxilla before or in conjunction with
implant placement, and a favorable
treatment outcome has been docu-
mented in several systematic reviews
and meta-analyses.1–5
A wide variety of grafting materials
have been used in MSFA, and autoge-
nous bone graft is generally considered
the preferred grafting material due to its
osteoinductive, osteogenic, and osteo-
conductive properties.1–6 However, the
use of autogenous bone graft is associ-
ated with risk of donor site morbidity
and unpredictable graft resorption.7–11
Hence, various bone substitutes are fre-
quently used to simplify the surgical
procedure by diminishing the need for
*Professor, Consultant, Department of Oral and Maxillofacial
Surgery, Aalborg University Hospital, Aalborg, Denmark.
†Consultant, Department of Oral and Maxillofacial Surgery,
Public Health Service, Gävle, Sweden.
‡Centre for Research and Development, Uppsala University/
Gävleborg County Council, Gävleborg, Sweden.
§Associated Professor, Consultant, Head, Department of Oral
and Maxillofacial Surgery and Oral Medicine, Malmö University,
Malmö, Sweden.
¶Consultant, Department of Oral & Maxillofacial Surgery,
Copenhagen University Hospital (Rigshospitalet), Copenhagen,
Denmark.
Reprint requests and correspondence to: Thomas
Starch-Jensen, DDS, PhD, Department of Oral and
Maxillofacial Surgery, Aalborg University Hospital, 18-
22 Hobrovej, DK-9000 Aalborg, Denmark, Phone: +45
97 66 27 98, Fax: +45 97 66 28 25, E-mail: thomas.
jensen@rn.dk
ISSN 1056-6163/18/02703-001
Implant Dentistry
Volume 27
Number 3
Copyright © 2018 Wolters Kluwer Health, Inc. All rights
reserved.
DOI: 10.1097/ID.0000000000000768
of no differences in implant treat-
ment outcome after maxillary sinus
floor augmentation (MSFA) with
synthetic bone substitutes (SBS)
compared with other grafting mate-
rials applying the lateral window
technique.
Materials and Methods: A
MEDLINE/PubMed, Embase and
Cochrane Library search in combi-
nation with hand-search of selected
journals was conducted.
Results: Five randomized con-
trolled trials with low risk of bias
fulfilled the inclusion criteria. SBS
disclosed high survival rate of supra-
structures and implants with no sig-
nificant differences compared to
autogenous bone graft or xenograft.
Meta-analysis revealed a patient-
bone harvesting and reducing graft
resorption. Bone substitutes are gener-
ally categorized as natural transplants
(allografts and xenografts) and syn-
thetic materials (alloplasts).12 The use
of bone substitutes is associated with
extra costs and provide only osteocon-
ductive properties. Recently published
systematic reviews assessing histomor-
phometric variables after MSFA, con-
cluded that autogenous bone graft
results in the highest amount of newly
formed bone in comparison with
(confidence interval: 0.89–1.08),
indicating no differences between
SBS and xenograft. SBS demon-
strated significant less newly formed
bone compared with autogenous
bone graft, whereas no significant
difference was revealed as compared
to xenograft. High implant stability
values, limited periimplant marginal
bone loss, and few complications
were reported with SBS.
Conclusions: There seem to be
no differences in implant treatment
outcome after MSFA with SBS com-
pared to other grafting materials.
(Implant Dent 2018;27:1–12)
Key Words: dental implants, guided
tissue regeneration, oral surgical
procedures, paranasal sinuses, pub-
lications
various bone substitutes, although al-
lografts, xenografts, and alloplastic
materials seem to be good alternatives
to autogenous bone grafts.13,14 How-
ever, bone substitutes of natural trans-
plants involves a risk of contamination,
activation of host immune, system and
disease transmission, as well as they
can be refused by patients for religious
reasons or because they are in contrast
with chosen lifestyle.15–17 Thus, the
ideal grafting material for MSFA re-
mains controversial.

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2 MAXILLARY SINUS FLOOR AUGMENTATION
Synthetic bone substitutes (SBS)
can be fabricated from calcium phos-
phates (eg, hydroxyapatite and trical-
cium phosphate), calcium sulfate,
bioactive glass, polymers, or metals.
SBS represent a large group of inor-
ganic biomaterials with variating struc-
tures, chemical composition, and
physical properties, which serve as
a 3-dimensional structural scaffold for
cell in-growth and bone regeneration.18
SBS have been widely used in medical
and dental fields, showing biocompati-
bility and osteoconductive proper-
ties.19–21 High long-term implant
survival rate has been reported after
MSFA with SBS mixed with particu-
lated autogenous bone graft.22 More-
over, it has previously been concluded
in a systematic review that SBS are
associated with increased bone forma-
tion, but lower graft resorption com-
pared to xenograft.23 However, the
implant treatment outcome after MSFA
with SBS compared to other bone graft-
ing materials has not yet been assessed
specifically in a systematic review.
Therefore, the objective of the
present systematic review was to test
the hypothesis of no difference in
implant treatment outcome after MSFA
with SBS alone or in combination with
particulated autogenous bone graft or
an alternative bone substitute compared
with other grafting materials.
MATERIALS AND METHODS
Protocol and Registration
The present systematic review was
conducted in accordance with the Pre-
ferred Reporting Items for Systematic
reviews and Meta-Analyses (PRISMA)
statement for reporting systematic re-
views.24 The methods of the analysis
and inclusion criteria were specified in
advance and documented in a protocol.
The review was registered in PROS-
PERO, an international prospective
register of systematic reviews. The pro-
tocol can be accessed at: https://www.
crd.york.ac.uk/PROSPERO/. Registra-
tion number: CRD42017081991.
Types of Publications
The review included studies on
humans. Letters, editorials, PhD the-
ses, letters to the editor, case reports,
abstracts, technical reports, conference
Copyright Ó 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
proceedings, animal or in vitro studies
and literature review articles were
excluded.
Types of Studies
The review included exclusively
randomized controlled trials comparing
the implant treatment outcome after
MSFA with SBS compared with other
grafting materials.
Types of Outcome Measures
The primary outcome measures are
the most important measures for evalu-
ating the final implant treatment out-
come. Secondary outcome measures
were also included in the present sys-
tematic review as surrogate measures.
The primary outcome measures
included:
1. Survival of suprastructures. Loss
of suprastructure was defined as
a total loss due to mechanical
and/or biological complications.
2. Survival of implants. Loss of im-
plants was defined as mobility of
previously clinically osseointe-
grated implants and removal of
nonmobile implants due to pro-
gressive periimplant marginal
bone loss (PIMBL) and infection.
Moreover, the following secondary
outcome measures were assessed:
1. Implant stability. Estimated by
magnetic resonance frequency
analysis or implant mobility due
to damping characteristics of the
surrounding tissue.
2. Bone-to-implant contact (BIC).
Estimated by histomorphometric
evaluation.
3. PIMBL. Evaluated by radio-
graphic measurements.
4. Bone regeneration. Estimated by
histomorphometric measure-
ments of newly formed bone, con-
nective tissue, and remaining graft
material.
5. Graft material reduction (GMR).
Evaluated by radiographic
measurements.
6. Patient-reported outcome meas-
ures (PROM).
7. Biological and technical
complications.
STARCH-JENSEN ET AL
Information Sources
The search strategy incorporated
examinations of electronic databases,
supplemented by a thorough page-by-
page hand-search of selected jour-
nals, including BioMed Research
International, British Journal of Oral
and Maxillofacial Surgery, Clinical
Implant Dentistry and Related
Research, Clinical Oral Implants
Research, European Journal of Oral
Implantology, Implant Dentistry,
International Journal of Oral and
Maxillofacial Implants, International
Journal of Oral and Maxillofacial
Surgery, International Journal of
Periodontics and Restorative Den-
tistry, International Journal of Pros-
thodontics, Journal of Clinical
Periodontology, Journal of Dental
Research, Journal of Oral Implantol-
ogy, Journal of Oral & Maxillofacial
Research, Journal of Periodontology,
Journal of Prosthetic Dentistry, Jour-
nal of Craniofacial Surgery, Journal
of Cranio-Maxillo-Facial Surgery,
Journal of Oral and Maxillofacial
Surgery, Periodontology 2000, Oral
and Maxillofacial Surgery, and Oral
Surgery Oral Medicine Oral Pathol-
ogy Oral Radiology. The manual
search also included the bibliogra-
phies of all articles selected for
full-text screening and previously
published reviews relevant for the
present systematic review.
Search
A MEDLINE (PubMed), Embase,
and Cochrane Library search was
conducted. Human studies published
in English until week 46, 2017 were
included. The search strategy was
performed in collaboration with
a librarian and used a combination of
Medical Subject Heading and free text
terms.
Selection of Studies
The PRISMA flow diagram
presents an overview of the selection
process (Fig. 1). The titles of the iden-
tified reports were initially screened.
The abstract was assessed when the title
indicated that the study was relevant.
Full-text analysis was obtained for
those with apparent relevance or when
the abstract was unavailable. The
STARCH-JENSEN ET AL IMPLANT DENTISTRY / VOLUME 27, NUMBER 3 2018 3

Outcome [O], and Study Design [S])

guidelines (Table 1).
Inclusion Criteria
Randomized controlled trials in
humans reporting implant treatment
outcome after MSFA with SBS alone
or in combination with particulated
autogenous bone graft or an alternative
bone substitute compared with other
grafting materials were included by
addressing the previously described
outcome measures. The review exclu-
sively focused on studies applying the
lateral window technique with an obser-
vation period of at least 1 year after
functional implant loading. In addition,
at least 10 patients should be included in
the study, and the number of MSFA
procedures had to be clearly specified.
Exclusion Criteria
The following exclusion criteria
were applied: nonrandomized con-
Fig. 1. PRISMA flow diagram demonstrating the results of the systematic literature search. A total trolled trials, case series, and cohort
of 102 titles were identified and 42 abstracts were reviewed. Full-text analysis included 25 articles, studies. Moreover, studies with an
and 5 randomized controlled trials in humans were finally included in the present systematic review. insufficient description of the numbers
of performed surgical procedures,
length of the observation period, and
references of the identified articles were Study Eligibility studies involving MSFA with SBS
cross-checked for unidentified articles. The inclusion criteria were devel- blocks or implant placement in medi-
The study selection was performed by oped using the PICOS (Population [P], cally compromised patients were
one reviewer (T.S.-J.). Intervention [I], Comparison [C], excluded. Likewise, studies adding
growth factors, bone morphogenetic
proteins, fibrin glue, or platelet-rich
Table 1. PICOS (Population [P], Intervention [I], Comparison [C], Outcome [O], and
plasma to the grafting material, and
Study Design [S]) Guidelines
studies involving osteotome-mediated
Patient and Healthy patients with atrophy of the posterior part of the sinus floor augmentation or studies
population (P) maxilla. comparing the implant treatment out-
Intervention (I) MSFA using the lateral window technique with a synthetic come with placement of short implants
bone substitute alone or in combination with particulated or sinus membrane elevation without
autogenous bone graft or an alternative bone substitute. a grafting material were also excluded.
Comparator or MSFA with other graft materials, including particulated
control group (C) autogenous bone graft alone, a mixture of particulated Data Extraction
autogenous bone graft, and an alternative bone substitute Data were extracted by one
or an alternative bone substitute alone. reviewer (T.S.-J.) according to a data
Outcomes (O) Primary outcome measures include survival of collection form, ensuring systematic
suprastructures and survival of implants. Secondary recording of the outcome measures. In
outcome measures include implant stability, BIC, PIMBL, addition, relevant characteristics of the
bone regeneration, vertical graft height reduction, PROM, study were recorded. The correspond-
and biological and technical complications. ing author was contacted by e-mail in
Study design (S) Randomized controlled trials.
the absence of important information or
Focused question Are there any differences in the final implant treatment
uncertainties.
outcome between MSFA with a synthetic bone substitute
alone or in combination with particulated autogenous bone Data Items
graft or an alternative bone substitute compared with MSFA The following items were collected
with particulated autogenous bone graft alone, a mixture of from the included articles and arranged
particulated autogenous bone graft and an alternative bone
in the following fields: patients, MSFA,
substitute or an alternative bone substitute alone.
implant placement, graft healing time,

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4 MAXILLARY SINUS FLOOR AUGMENTATION
implant healing time, residual vertical
bone height, follow-up after loading,
survival of suprastructures, survival of
implants, implant stability, BIC,
PIMBL, newly formed bone, connective
tissue, remaining graft material, GMR,
complications, and reference number.
Assessment of Methodological Quality
The quality assessment of the
included studies was undertaken by
one reviewer (T.S.-J.) as part of the data
extraction process. A methodological
quality rating system was used, and the
classification of the risk of bias potential
for each study was based on the follow-
ing 5 criteria:
1. Randomization of the included
subjects (yes/no).
2. Definition of inclusion and exclu-
sion criteria (yes/no).
3. Report of losses to follow-up (yes/
no).
4. Validated measurements (yes/no).
5. Statistical analysis (yes/no).
The studies were grouped accord-
ing to:
1. Low risk of bias (plausible bias
unlikely to seriously alter the re-
sults) if all above-described qual-
ity criteria were met.
2. Moderate risk of bias (plausible
bias that weakens confidence in
the results) when one of these cri-
teria were not included.
3. High risk of bias (plausible bias
that seriously weakens confidence
in the results) when 2 or more cri-
teria were missing.
Assessment of Heterogeneity
The significance of any discrepan-
cies in the estimates of the treatment
effects of the different studies was
assessed by means of Cochran test for
heterogeneity and the I2 statistic, which
describes the percentage total variation
across studies that is due to heterogene-
ity rather than chance. Heterogeneity
was considered statistically significant
if P , 0.1. A rough guide to the inter-
pretation of I2 given in the Cochrane
Handbook is as follows: (1) at 0% to
40% the heterogeneity might not be
Copyright Ó 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
important, (2) 30% to 60% may repre-
sent moderate heterogeneity, (3) 50% to
90% may represent substantial hetero-
geneity, and (4) 75% to 100% may rep-
resent considerable heterogeneity.25
RESULTS
Study Selection
The search result is outlined in Fig-
ure 1. A total of 102 titles were identi-
fied and 42 abstracts were reviewed.
Full-text analysis included 25 articles,
and 5 randomized controlled trials in
humans were finally included in the
present systematic review.26–30 Three
articles were included as the result of
hand-searching.27,29,30
Exclusion of Studies
The reasons for excluding studies
after full-text assessment were as fol-
lows: the study could not be excluded
before meticulous reading (n ¼ 11),31–
41 a nonrandomized controlled trial (n ¼
4),42–45 delayed or immediate implant
placement not specified (n ¼ 1),46 and
4 studies were excluded because the pri-
mary outcome measures in the same
patient sample was reported in publica-
tions with a 3-year30 and 5-year27
observation period, respectively (n ¼
4).47–50 The secondary outcome meas-
ures from the previous publications
were included in the following section
and Table 2.
Study Characteristics
Partially or totally edentulous pa-
tients with a residual vertical alveolar
bone height of less than 6 mm in the
posterior part of the maxilla were
enrolled in the included studies.26–30
Description of the used power calcula-
tion of sample size was only defined in
one of the included studies.27,48 Patient
demographics revealed certain dissimi-
larity, and smokers were excluded in 2
studies.26,28 SBS were used alone in all
the included studies, and implants were
inserted 5 to 9 months after MSFA.
BoneCeramic (Straumann AG, Basel,
Switzerland) was used in 3 of the
included studies and compared to Bio-
Oss (Geistlich Pharma AG, Wolhusen,
Switzerland)27 or autogenous bone
graft harvested from the tuberosity
area26 or the zygomatic buttress, the
STARCH-JENSEN ET AL
lateral sinus wall, and the tuberosity
area.28 In the remaining studies, Fisiog-
raft Bone Granular (Ghimas S.p.A.,
Italy)29 or Nanobone (Artoss GmbH,
Rostock, Germany)30 was compared
to Bio-Oss. The method used for ran-
domization was described in 4 of the
included studies involving a com-
puter-generated randomization code28
and sealed opaque envelopes.29,47,48
Different implant systems were used
involving Straumann (Straumann AG,
Basel, Switzerland),26–28 BnxEvo
(Ghimas S.p.A.),29 and Camlog (Cam-
log Biotechnologies AG, Wimsheim,
Germany).30 The created lateral win-
dows were covered with a collagen bar-
rier membrane in all the included
studies.26–30 The implant stability was
measured by magnetic resonance fre-
quency analysis (Osstell, Integration Di-
agnostics AB, Gothenburg, Sweden)49 or
by implant mobility due to damping char-
acteristics of the surrounding tissue (Peri-
otest, Medizintechnik Gulden, Modautal,
Germany).30 One of the included studies
reported that the investigators were blind
to the allocation of the biomaterial, at the
3-year clinical and radiographic examina-
tion.30 PROM was not reported in any of
the included studies and therefore not
described in the following section. The
main results are described below and
summarized in Table 2.
Data Synthesis
Meta-analyses were to be con-
ducted only if there were studies of
similar comparison, reporting identical
outcome measures. However, only few
studies were included in the present
systematic review. Moreover, the stud-
ies included revealed considerable var-
iations in design, that is, patient
demographics, unilateral and bilateral
MSFA, residual vertical alveolar bone
height, dissimilar amount of grafting
material used, length of healing period,
type of suprastructures and implants,
length of observation period, and type
of outcome measures. Therefore,
a well-defined meta-analysis was not
applicable. However, the differences in
the proportions of patient-based
implant survival across 3 similar studies
assessing SBS and xenograft were
analyzed, including a forest plot.27,29,30
The patient-based implant survival rate
 STARCH-JENSEN
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Table 2. Maxillary Sinus Floor Augmentation With Synthetic Bone Substitutes Compared With Other Grafting Materials
Materials and Methods Primary Outcome Measures

ET AL
Delayed Healing Time (Mo) Follow-Up after Survival (%) Implant
Pt MSFA Implants Graft Implant RVBH (mm) Loading (Mo) ST Implant Stability BIC
30 15 sinuses with BoneCeramic BCP NR 9 2 4.1 (3–6) 12 NR 100 NR NR
15 sinuses with autogenous bone
11 11 sinuses with BoneCeramic BCP 24 8 8 wk ,5 60 100 91.7 3y 8 mo
68.5 64.6
11 sinuses with Bio-Oss DBB 23 91.3 70.4 55.0
10 10 sinuses with BoneCeramic BCP 52 6–8 4 ,5 12 100 100 NR NR
10 sinuses with autogenous bone
28 28 sinuses with Fisiograft Bone 55 6 4 2.0 (0.5–3) 12 100 96.4 NR NR
28 sinuses with Bio-Oss DBB 52 98.1
14 14 sinuses with Nanobone 26 7 (5–9) 6 ,5 36 NR 96.2 3y NR
−4.42
14 sinuses with Bio-Oss DBB 27 96.3 −4.77

Secondary Outcome Measures

Bone Regeneration (%)

IMPLANT DENTISTRY / VOLUME 27, NUMBER 3 2018

Pt PIMBL (mm) NFB CT RGM GMR (%) COMP Ref
30 NR 9 mo NR None 26

26.7 39.6* 33.7

38.6* 0 60.6*
11 1/3/5 y 8 mo/3 y 5y None 27,47–49

0.4/1.3/1.4 41.1/29.0 NR/51% NR/20.0 6.6

0.3/1.1/1.0 41.6/32.0 NR/44.3 NR/24.0 5.8
10 NR 6–8 mo NR SMP: 2 28

28.2 38.9 32.9*

36.8* 58.4* 4.8 SMP: 3
28 NR 6 mo NR SMP: 3 29

34.9 44.5 20.6

38.5 43.5 22.3
14 NR 7 mo 7 mo None 30,50

19.0 44.2 36.8 28.5

23.7 48.7 27.6 22.4
BCP, biphasic calcium phosphate; COMP, complications; CT, connective tissue; DBB, deproteinized bovine bone; NFB, newly formed bone; NR, not reported; Pt, patients; Ref, reference; RGM, remaining graft material; RVBH, residual vertical alveolar bone height;
SMP, sinus membrane perforation; ST, suprastructures.
*Statistical significant difference.

5
6 MAXILLARY SINUS FLOOR AUGMENTATION
was expressed as the mean percentage
with the 95% confidence interval (CI).
Random effects model was used
because there were a substantial and sta-
tistical significant amount of heteroge-
neity among the few studies. The
analyses were conducted using STATA
14 (Stata Statistical Software; Release
14; Stata Corp. 2015, College Station,
TX: StataCorp LP).
METHODOLOGICAL QUALITY
The quality of the included studies
is summarized in Table 3.
Outcome Measures
The results of MSFA with SBS
compared with other grafting materials
are presented below and outlined in
Table 2. All the reported numerical val-
ues are presented as mean values. For
each outcome measure, a summary is
finally provided.
Primary Outcome Measures
Survival of suprastructures. The 5-
year survival of suprastructure was
100% after MSFA with BoneCeramic
or Bio-Oss.27 All patients were rehabil-
itated with a fixed prosthetic recon-
struction, which were all in function at
the 5-year follow-up examination.27
The 1-year survival of suprastruc-
ture was 100% after MSFA with Bone-
Ceramic or autogenous bone graft.28
Patients were rehabilitated with a non-
specified prosthetic solution.28
The 1-year survival of suprastruc-
ture was 100% after MSFA with Fi-
siograft Bone Granular or Bio-Oss.29
All patients were rehabilitated with
screwed retained metal-ceramic pros-
theses, which were all in function at the
1-year follow-up examination.29
Table 3. Quality Assessment of the Included Studies
Definition of
Randomization Inclusion and
of Included Exclusion
Subjects Criteria
Yes Yes
Yes Yes
Yes Yes
Yes Yes
Yes Yes
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Summary
MSFA with SBS demonstrated
high survival rate of suprastructures
with no differences compared to autog-
enous bone graft or xenografts.
Survival of implants. The 5-year
implant survival after bilateral MSFA
in 11 patients with BoneCeramic or
Bio-Oss and delayed placement of 24
and 23 implants was 92% and 91%,
respectively.27 There was no statisti-
cally significant difference between
the 2 treatment modalities.27
The 3-year implant survival after
bilateral MSFA in 14 patients with
Nanobone or Bio-Oss and delayed
placement of 26 and 27 implants was
96.2% and 96.3%, respectively.30
There was no statistically significant
difference between the 2 treatment
modalities.30
The 1-year implant survival was
100% after unilateral MSFA in 30
patients with either BoneCeramic or
autogenous bone graft and delayed
placement of an unknown number of
implants.26
The 1-year implant survival was
100% after bilateral MSFA in 10 pa-
tients with BoneCeramic or autogenous
bone graft and delayed placement of
a nonspecified number of implants.28
The 1-year implant survival after
bilateral MSFA in 28 patients with
Fisiograft Bone Granular or Bio-Oss
and delayed implant placement of 55
and 52 implants was 96.4% and 98.1%,
respectively.29 There was no statisti-
cally significant difference between
the 2 treatment modalities.29
Summary
MSFA with SBS and delayed
implant placement demonstrated high
implant survival with no statistically
Report of
Losses to
Follow- Validated Statistical
Up Measurements Analysis
Yes Yes Yes
Yes Yes Yes
Yes Yes Yes
Yes Yes Yes
Yes Yes Yes
STARCH-JENSEN ET AL
significant difference compared with
the use of autogenous bone graft or
xenografts.
Meta-analysis. Fixed effect analysis
and test for heterogeneity was incon-
clusive due to the limited number of
studies included. No statistically signif-
icant difference in heterogeneity
between the included studies was found
(I2 ¼ 0%, P ¼ 0.803). Meta-analysis
revealed a mean difference of patient-
based implant survival rate of 0.98 (CI:
0.89–1.08), indicating no differences
between SBS and xenograft (Fig. 2).
Secondary Outcome Measures
Implant stability. The 3-year Osstell
implant stability quotient (ISQ) value
after MSFA with BoneCeramic or Bio-
Oss was 68.5 and 70.4, respectively.27
There was no statistically significant
difference between the 2 treatment
modalities. The ISQ value increased
from 68.9 at abutment connection to
71.5 after 1 year of loading after MSFA
with BoneCeramic.27
The 3-year Periotest value after
MSFA with Nanobone or Bio-Oss was
−4.42 and −4.77.30 There was no statis-
tically significant difference between
the 2 treatment modalities.30
Summary
MSFA with SBS demonstrate high
implant stability with no statistically
significant differences compared with
the use of xenografts after 3 years.
Bone-to-implant contact. The 8-month
BIC after retrieval of micro-implants
with a sandblasted, acid-etched surface,
inserted at the grafting procedure, was
64.6% after MSFA with BoneCeramic
compared to 55.0% with Bio-Oss.47
There was no statistically significant
Risk of
Bias Reference
Low Tosta et al26
Low Mordenfeld et al27
Low Danesh-Sani et al28
Low Stacchi et al29
Low Lorenz et al30
STARCH-JENSEN ET AL
Fig. 2. Meta-analysis using a random effect assessing differences in the proportions of
patient-based implant survival across 3 similar studies assessing maxillary sinus floor aug-
mentation with SBS and xenograft. A forest plot showing a mean difference of patient-based
implant survival of 0.98 (CI: 0.89–1.08), indicating no differences between SBS and xenograft.
difference between the 2 treatment
modalities.
Summary
The BIC after MSFA with SBS
revealed no statistically significant dif-
ference compared with the use of xen-
ografts after 8 months of graft healing.
Periimplant marginal bone loss. The
5-year radiographic PIMBL after
MSFA with BoneCeramic compared
to Bio-Oss was 1.4 and 1.0 mm, respec-
tively.27 The annual PIMBL was
0.14 mm with BoneCeramic compared
to 0.1 mm with Bio-Oss. There was no
statistically significant difference be-
tween the 2 treatment modalities. The
marginal bone level was measured
mesial and distal to the implant from
a defined reference point to the bone
level at baseline (delivery of prosthetic
reconstruction), after 1 year, 3 years,
and 5 years.27
Summary
The PIMBL after MSFA with SBS
revealed no statistically significant dif-
ferences compared with the use of
xenografts.
Bone regeneration. The amount of
newly formed bone, connective tis-
sue, and remaining graft material
Copyright Ó 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 27, NUMBER 3 2018
after MSFA with BoneCeramic was
41.1%, 48.1%, and 10.8%, respec-
tively, compared to 41.6%, 46.4%,
and 12% with Bio-Oss, after 8 months
of graft healing.47 Corresponding
values after 3 years with BoneCeram-
ic was 28.6%, 51.0%, and 20.4%,
respectively, compared to 31.7%,
44.3% and 24.0% with Bio-Oss.49
There were no statistically significant
differences in the histomorphometric
outcome between the 2 treatment
modalities at 8 months or 3 years.
However, significantly more Bio-
Oss particles were in contact with
newly formed bone compared to
BoneCeramic particles after 8
months, but the difference was not
significant after 3 years.47,49
The amount of newly formed bone,
connective tissue, and remaining graft
material after MSFA with Nanobone
was 19.0%, 44.2%, and 36.8%, respec-
tively, after 7 months of graft healing.50
Corresponding values for Bio-Oss was
23.7%, 48.7%, and 27.6%. There was
no statistically significant difference in
the histomorphometric outcome
between the 2 treatment modalities.
However, a significant higher number
of multinucleated giant cells were
7
reported in augmented areas with
Nanobone.50
Histomorphometric evaluation
revealed significant less newly formed
bone after MSFA with BoneCeramic
compared to autogenous bone graft,
after 9 months of graft healing.26 The
amount of newly formed bone with
BoneCeramic in the region close to
or distant from the native bone inter-
face was 33.7% and 26.7%, respec-
tively, whereas corresponding values
for autogenous bone graft was 41.0%
and 38.6%. BoneCeramic disclosed
significantly less bone formation in
the area distant from native bone inter-
face compared to the area close to
native bone, whereas no significant
differences were observed between
the 2 areas with autogenous bone
graft.26
Histomorphometric evaluation
also revealed significant less newly
formed bone after MSFA with Bone-
Ceramic compared to autogenous bone
graft, after 6 to 8 months of graft
healing.28 The amount of newly formed
bone was 28.2% with BoneCeramic
compared to 36.8% with autogenous
bone graft.28
The amount of newly formed bone,
connective tissue, and remaining graft
material after MSFA with Fisiograft
Bone Granular was 34.9%, 44.5%,
and 20.6%, respectively, compared to
38.5%, 43.5%, and 22.3% with Bio-
Oss, after 6 months of graft healing.29
There were no statistically significant
differences in the histomorphometric
outcome between the 2 treatment
modalities.29
Summary
The amount of newly formed
bone was significantly higher with
autogenous bone graft compared to
BoneCeramic. However, no signifi-
cant difference in the histomorpho-
metric outcome between SBS and
xenografts was disclosed. Short-term
studies disclosed a significantly high-
er contact between xenograft particles
and newly formed bone compared to
SBS, whereas a significant higher
number of multinucleated giant cells
were found in biopsies obtained from
areas augmented with SBS compared
to xenografts.
8 MAXILLARY SINUS FLOOR AUGMENTATION
Graft material reduction. The 6-year
radiographic GMR after MSFA with
BoneCeramic was 6.6% compared to
5.8% with Bio-Oss.27 The height of the
grafting material after MSFA with
BoneCeramic decreased from 14.7 mm
at baseline to 14.0 mm after 2 years,
13.8 mm after 4 years, and 13.7 mm
after 6 years. Corresponding measure-
ments for Bio-Oss was 14.8 mm at base-
line decreasing to 14.2 mm after 2
years, 14.1 mm after 4 years, and
14.0 mm after 6 years, respectively.
There was no statistically significant
difference between the 2 treatment
modalities. However, BoneCeramic re-
vealed a statistically significant differ-
ence in GMR after 6 years compared to
baseline. Two-dimensional linear
measurements on conventional or digi-
tal panoramic radiographs were used to
estimate the changes in the augmented
vertical sinus height from baseline to 6
years after grafting.27
The 7-month radiographic GMR
after MSFA with Nanobone was 28.5%
compared to 22.4% with Bio-Oss.30
The average volume after MSFA with
Nanobone decreased from 2.95 cm3 at
baseline to 2.11 cm3 after 7 months of
graft healing. Corresponding measure-
ments for Bio-Oss was 3.04 and 2.36
cm3. There was no statistically signifi-
cant difference between the 2 treatment
modalities. Three-dimensional radio-
graphic measurements on computed
tomography scans were used to esti-
mate the volume changes from baseline
to 7 months of graft healing.30
Summary
The GMR after MSFA with SBS
revealed no statistically significant dif-
ferences compared with the use of
xenografts.
Biological and technical complications.
No biological complications were re-
ported in 3 studies.26,27,30 Perforation of
the sinus membrane was the only re-
ported intraoperative complication and
occurred rarely.28,29 The sinus mem-
brane perforation was sealed with a col-
lagen membrane in one study.28 In
another study, patients with sinus mem-
brane perforations were excluded.29
No technical complications were
reported in any of the included stud-
ies.26–30
Copyright Ó 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Summary
The frequency and severity of
complications with the different treat-
ment modalities seem to be compara-
ble. Perforation of the sinus membrane
was the most frequent biological com-
plication but did not seem to influence
the final implant treatment outcome.
Technical complications were not re-
ported in any of the included studies.
DISCUSSION
The objective of the present sys-
tematic review was to test the hypoth-
esis of no difference in implant
treatment outcome after MSFA with
SBS alone or in combination with
particulated autogenous bone graft or
an alternative bone substitute compared
with other grafting materials. The pri-
mary outcome measures included sur-
vival of suprastructures and survival of
implants, considered the most impor-
tant measures for the assessment of
long-term implant treatment outcome.
Secondary outcome measures included
implant stability, BIC, PIMBL, bone
regeneration, GMR, PROM, and bio-
logical and technical complications. A
total of 5 randomized controlled trials
with low risk of bias fulfilled the
inclusion criteria.26–30 SBS were used
alone in all the included studies and
compared to particulated autogenous
bone graft26,28 or xenograft.27,29,30
MSFA with SBS disclosed high sur-
vival rates of suprastructures and im-
plants with no significant differences
compared to autogenous bone graft or
xenograft. Meta-analysis revealed
a mean difference of patient-based
implant survival of 0.98 (CI: 0.89–
1.08), indicating no differences
between SBS and xenograft. SBS dem-
onstrated significant less newly formed
bone compared with autogenous bone
graft, whereas no significant difference
was revealed as compared to xenograft.
High implant stability and BIC values,
limited PIMBL and GMR, and few bio-
logical complications were reported
after MSFA with SBS. However,
long-term randomized controlled trials
comparing the different treatment
modalities are limited and several non-
comparative studies are excluded due to
the types of studies included in the
STARCH-JENSEN ET AL
present systematic review, which omits
valuable data about BIC and histomor-
phometric characteristics with the dif-
ferent treatment modalities. Moreover,
considerable heterogeneity among the
included studies prevented a well-
defined meta-analysis from being per-
formed and the diversity of the used
evaluation methods, small patient sam-
ples, dissimilar outcome measures, dif-
ferent biochemical composition of SBS,
and various methodological confound-
ing factors posed serious restrictions to
review the literature in a quantitative
systematic manner. Hence, the conclu-
sions drawn from the results of the pres-
ent systematic review should be
interpreted with caution.
High long-term survival of supra-
structures after prosthetic rehabilitation
with implants has been documented in
several systematic reviews.4,51–55 In the
present systematic review, the survival
of suprastructures after MSFA with
SBS was high and seem to be in accor-
dance with the previously reported sur-
vival rate of suprastructures after
implant placement.4,51–55
Placement of implants in partially
or totally edentulous patients without
bone augmentation have demonstrated
high long-term implant survival rates,
as documented in several reviews and
long-term studies.56–59 Survival of im-
plants within the included studies of the
present systematic review seems to be
comparable to the implant treatment
outcome obtained after MSFA with
autogenous bone grafts and xenograft.
A newly published systematic review
and meta-analysis of long-term studies
assessing MSFA disclosed high im-
plant survival rates in noncomparative
studies regardless of the used grafting
material.4 Thus, further long-term ran-
domized controlled trials assessing
MSFA with different grafting materials
are needed, before one treatment
modality can be considered superior to
others.
Implant stability is a prerequisite
for the long-term implant survival.
Periotest and Osstell are noninvasive
techniques for determining the implant
stability. Periotest values ranging from
−8 to 50 and negative Periotest values
indicate greater implant stability.60 The
3-year Periotest value after MSFA with
STARCH-JENSEN ET AL
Nanobone was −4.42 and −4.77 with
Bio-Oss, disclosing no statistically sig-
nificant differences between the 2 treat-
ment modalities.30 Osstell measure the
ISQ value ranging from 1 to 100, and
the implant stability increases with
a higher ISQ value.60 Previous studies
focusing on ISQ revealed a significant
association between ISQ values below
40 and failed implants, whereas others
concluded that ISQ values below 50 are
critical for implant survival.61,62 In
addition, it has been reported that im-
plants with ISQ values higher than 50
resulted in an implant survival of 100%
after 12 months.63 The 3-year Osstell
ISQ value after MSFA with BoneCer-
amic was 68.5 and 70.4 with Bio-Oss,
disclosing no statistically significant
differences between the 2 treatment
modalities.27 Thus, MSFA with SBS
demonstrated high implant stability
with no statistically significant differen-
ces compared with the use of xenografts
after 3 years of implant loading.27,30
The percentage of hard tissue depo-
sition on the implant surface is important
for long-term implant stability. The 8-
month BIC after MSFA with BoneCer-
amic was 64.6% compared to 55.0%
with Bio-Oss, disclosing no statistically
significant differences between the 2
treatment modalities.47 A previous study
using micro-computed tomography of
retrieved experimental mini-implants
after different sinus membrane elevation
procedures revealed no statistical differ-
ences in BIC between the different pro-
cedures, after 7 months of graft
healing.64 Histomorphometric evalua-
tion of different implant surfaces after
MSFA with a 3:1 mixture of Bio-Oss
and autogenous bone graft revealed
a BIC varying between 41.5% and
94.1%, 6 months after implant loading.65
BIC after MSFA with autogenous bone
graft and Bio-Oss have been evaluated in
a minipig study demonstrating a signifi-
cantly higher BIC for different mixtures
of autogenous bone graft and Bio-Oss
compared to Bio-Oss alone.66 The per-
centage of BIC seems to be influenced by
the topography of the implant surface
and the addition of autogenous bone graft
to the grafting material. However, the
above-mentioned studies may be com-
promised by the use of biased histo-
morphometry and different implant
Copyright Ó 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 27, NUMBER 3 2018
surfaces. Thus, further studies evaluating
BIC after MSFA with different grafting
materials should involve unbiased ster-
eologic methods and similar implant
surfaces.67,68
Several factors may influence
PIMBL, including smoking habits,
poor hygiene practices, systemic med-
ical conditions, parafunctional habits,
different connections between the
implant and suprastructure, implant
neck design, and implant surface.69–71
The 5-year radiographic PIMBL after
MSFA with BoneCeramic was 1.4 mm
compared to 1.0 mm with Bio-Oss,
revealing no statistically significant dif-
ferences between the 2 treatment modal-
ities.27 However, 2 implants inserted in
sinuses augmented with BoneCeramic
had a marginal bone levels exceeding
2.8 mm after 5 years.27 In addition, 2
implants were lost in one patient due to
periimplantitis and massive bone resorp-
tion. The patient was a former smoker
and the implant loss occurred in sinuses
augmented with BoneCeramic and Bio-
Oss, respectively.27 Nevertheless,
MSFA with BoneCeramic showed lim-
ited long-term PIMBL and in accor-
dance with the criterion of successful
implant treatment, but further long-
term studies are needed.70,71
Histomorphometric evaluation of
biopsies obtained after MSFA with
SBS demonstrated significant less
amount of newly formed bone com-
pared with autogenous bone graft,26,28
whereas no significant difference was
revealed compared to xenograft.27,29,30
It has previously been concluded in sys-
tematic reviews that MSFA with autog-
enous bone graft results in the highest
amount of newly formed bone in com-
parison to allografts, alloplastic materi-
als, and xenografts.13,14 A single newly
published study assessing MSFA with
bioactive glass, autogenous bone graft
or a mixture of bioactive glass, and
autogenous bone graft demonstrated
no significant differences in new bone
formation with the different treatment
modalities after 6 months of graft heal-
ing.41 Moreover, a meta-analysis
showed a significantly higher propor-
tion of mineralized bone during the
early healing phase when autogenous
bone was used as grafting material for
MSFA as compared with tricalcium
9
phosphate, Bio-Oss alone, or mixtures
of autogenous bone graft and Bio-
Oss.72 However, after a graft healing
period of more than 9 months, no statis-
tically significant differences were
found between the different treatment
modalities.72 These results are in con-
trast to the results of the present sys-
tematic review. Moreover, a newly
published systematic review and
meta-analysis assessing the histologi-
cal outcome after MSFA with calcium
phosphates or xenografts disclosed
a nonsignificant higher percentage of
newly formed bone with calcium phos-
phates.73 The included studies in the
present systematic review revealed
a nonsignificant higher percentage of
newly formed bone with Bio-Oss com-
pared to SBS, and significantly more
Bio-Oss particles were in contact with
newly formed bone compared to Bone-
Ceramic particles after 8 months,
although the difference was not signif-
icant after 3 years.27,29,30,47,49 Thus,
further randomized controlled trials as-
sessing the histomorphometric out-
come after MSFA with different
grafting materials are needed to eluci-
date the amount of newly formed bone
to ensure a higher osseointegration of
the inserted implants.
The GMR after MSFA with SBS
revealed no statistically significant dif-
ferences compared with xenografts as
evaluated by 2-dimensional linear meas-
urements on panoramic radiographs and
3-dimensional radiographic measure-
ments on computed tomography
scans.27,30 GMR occurred predomi-
nantly during the first years,27 which is
in accordance with previous publications
assessing dimensional changes of the
graft material after MSFA.74,75 Three-
dimensional time-dependent graft vol-
ume changes after MSFA in humans,
with different grafting materials have
been assessed in a systematic review dis-
closing GMR during the early healing
times.11 Moreover, less GMR was found
after MSFA with bone substitutes alone
or in combination with other grafting ma-
terials compared to autogenous bone
graft. However, the included studies
were categorized as high risk of bias.11
Thus, more long-term randomized con-
trolled trials using unbiased stereologic
methods or 3-dimensional volume
10 MAXILLARY SINUS FLOOR AUGMENTATION
measurements are needed to evaluate
GMR after MSFA with different grafting
materials.
Perforation of the sinus membrane
was the only biological complication
reported in the included studies, but it
did not seem to influence the final
implant treatment outcome. No techni-
cal complications were described.
Hence, the frequency of biological and
technical complications after MSFA
with SBS seem to be in accordance
with the frequency of complications
after MSFA using autogenous bone
graft or other bone substitute, as pre-
viously reported.2,4,5,76,77
MSFA with SBS or xenografts
compared to autogenous bone graft is
associated with obvious advantages for
the patient, including reduced morbid-
ity, less invasive, and reduced length of
the operation time. Consequently,
a comparison of the various treatment
modalities should contain an evaluation
of donor site morbidity after autoge-
nous bone harvesting, an economic
perspective, and PROM. However,
these aspects have not been addressed
in any of the included studies.
CONCLUSIONS
The hypothesis of no difference in
implant treatment outcome after MSFA
with SBS alone or in combination with
particulated autogenous bone graft or
an alternative bone substitute compared
with other bone grafting materials
applying the lateral window technique
could neither be confirmed nor rejected
due to insufficient knowledge. MSFA
with SBS disclosed high survival rates
of suprastructures and implants with no
significant differences compared to
autogenous bone graft or xenograft.
Moreover, high implant stability and
BIC values, limited PIMBL, dimin-
ished GMR, and few biological com-
plications were reported after MSFA
with SBS. However, SBS demonstrated
significant less amount of newly formed
bone compared with autogenous bone
graft, whereas no significant difference
was revealed as compared to xenograft.
Thus, SBS alone seem to be a suitable
grafting material for MSFA. However,
further long-term randomized con-
trolled trials assessing the final implant
Copyright Ó 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
treatment outcome after MSFA with
SBS are needed before further conclu-
sions can be made on this topic.
DISCLOSURE
The authors claim to have no
financial interest, either directly or
indirectly, in the products or informa-
tion listed in the article.
ROLES/CONTRIBUTIONS
BY AUTHORS
T. Starch-Jensen: Conceived of the
present idea in collaboration with J. P.
Becktor; participated in study concep-
tion and design; wrote the manuscript
with inputs from all co-authors; per-
formed the search strategy and selection
of studies, data extraction, statistical
analysis, analyses of data, and final
approval of the manuscript. A. Mor-
denfeld: Participated in study concep-
tion and design; discussed the final
results with interpretation of data; per-
formed analyses of data; contributed to
the manuscript with final approval. J. P.
Becktor: Discussed the final results
with interpretation of data; conceived
of the present idea in collaboration with
T. Starch-Jensen and contributed to the
manuscript with final approval. S. S.
Jensen: Participated in drafting the
article and revising it critically for
important intellectual content; dis-
cussed the final results with interpreta-
tion of data; performed analyses of data;
contributed significantly to the manu-
script with final approval.
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