Accepted: 2 April 2017

DOI: 10.1111/jcpe.12728

RANDOMIZED CLINICAL TRIAL

Volumetric changes of grafted volumes and the Schneiderian

membrane after transcrestal and lateral sinus floor elevation
procedures: A clinical, pilot study

Andy Temmerman1  | Jeroen Van Dessel2 | Simone Cortellini1 | 

Reinhilde Jacobs2 | Wim Teughels1 | Marc Quirynen1

1
Section of Periodontology, Department of
Oral Health Sciences, KU Leuven & Dentistry,
University Hospitals, Leuven, Belgium
2
Department of Maxillofacial Surgery, OMFS-
Impath Research Group, Leuven, Belgium
Correspondence
A. Temmerman, Department of
Periodontology, Department of Oral Health
Sciences, KU Leuven & Dentistry, University
Hospitals, KU Leuven, Leuven, Belgium.
Email: andy.temmerman@uzleuven.be
Abstract
Aim: To investigate the influence of various surgical techniques for sinus augmenta-
tion on the volumetric changes of graft, membrane and the post-­
operative
discomfort.
Materials and Methods: Eighteen patients in need of bilateral sinus floor elevation
(SFE) were assigned to lateral SFE, transcrestal SFE and intralift procedures. CBCT im-
ages taken at baseline, 1 week and 6 weeks were analysed for volumetric changes in
graft and Schneiderian membrane. Questionnaires were used to analyse post-­
op
discomfort.
Results: The overall average graft volume obtained after 1 week was 1.87 cm3 (range
0.12–4.72 cm3). Volumes decreased after 6 weeks to an overall mean volume of
1.33 cm3 (range 0.10–4.29 cm3 – average decrease of 27.6%). After 6 weeks, the
amount of graft volume decreased in every treatment option, ranging from −23.13%
for the tSFE, over −24.55% for the lSFE, to −33.71% for the IL. Although all treatment
options correspond in an increase in Schneiderian membrane volume, no statistically
significant correlation between this increase and loss of graft volume could be ­obtained
for all treatments (p = 0.97).
Conclusion: All SFE techniques provided sufficient graft volume for implant treatment.
All techniques provoke a partially transient swelling of the Schneiderian membrane. All
techniques resulted in a decrease in graft volume after 6 weeks; however, no signifi-
cant differences were obtained between treatments. Furthermore, no statistical sig-
nificant correlation between the post-­
operative swelling of the Schneiderian
membrane and reduction in graft volume at 6 weeks could be obtained.

KEYWORDS
bone volume, dental implants, Schneiderian membrane, sinus floor elevation, sinuslift

1 | INTRODUCTION
Vertical bone deficits in the posterior maxilla are very common after
tooth extraction. When oral implants are needed in this area, a max-
illary sinus floor elevation (SFE) procedure has become a popular
and thoroughly investigated surgical procedure to compensate for
inadequate vertical residual bone height (RBH). Nowadays, the lateral
window SFE (lSFE) procedure is widely used and considered reliable,
with implant survival rates comparable to those of implants placed in
pristine bone (Del Fabbro, Wallace, & Testori, 2013; Esposito, Felice,
& Worthington, 2014; Jensen, Schou, Stavropoulos, Terheyden, &
Holmstrup, 2012; Nkenke & Stelzle, 2009; Wallace & Froum, 2003).

660  |  © 2017 John Wiley & Sons A/S.

wileyonlinelibrary.com/journal/jcpe J Clin Periodontol. 2017;44:660–671.
Published by John Wiley & Sons Ltd
TEMMERMAN et al.
In the 1980s, a less invasive, one-­stage technique was introduced
(Boyne & James, 1980) and thereafter modified by Summers (1994).
Only a few modifications have been proposed since then (Rosen
et al., 1999; Trombelli, Minenna, Franceschetti, Minenna, & Farina,
2010; Trombelli et al., 2014). Within this technique, osteotomes
are applied via a transcrestal approach, to elevate the floor of the
sinus and to advance bone substitutes beyond the level of the orig-
inal sinus floor, and as such elevate the mucosal lining. Also for this
approach, high implant survival rates have been reported (Esposito
et al., 2014; Jensen et al., 2012; Nkenke & Stelzle, 2009). In the liter-
ature, the transcrestal SFE technique (tSFE) has been recommended
in sites where the alveolar crest is of sufficient width and where a
residual bone height (RBH) of ≥5 mm is available (Wang & Katranji,
2008). Furthermore, the anatomy of the sinus floor should not be
too oblique, as the osteotomes enter the sinus cavity at the lower
level first while still having resistance in the higher parts. The main
disadvantages of tSFE are the risk of perforating the sinus membrane
and the limited intra-­operative visibility (Al-­Almaie, Kavarodi, & Al
Faidhi, 2013; Nkenke & Stelzle, 2009; Schwartz-­Arad, Herzberg, &
Dolev, 2004).
In order to deal with these disadvantages, various alternative
SFE procedures have been proposed (Kfir, Kfir, Goldstein, Mazor,
& Kaluski, 2012; Rao & Reddy, 2014). One of them is the transcr-
estal hydrodynamic, ultrasonic, cavitational technique (Intralift™
– IL) (Troedhan, Kurrek, & Wainwright, 2012; Troedhan, Kurrek,
Wainwright, & Jank, 2014). This technique is developed based on
the atraumatic capacities of ultrasonic surgery and bone regen-
eration mechanisms beneath the mucosa of the maxillary sinus or
Schneiderian membrane.
It seems logical that different SFE procedures can result in differ-
ent volumes of augmentation. The question remains whether tSFE
procedures and lSFE procedures can result in comparable volumes
of augmentation. If so, this could eventually lead to the use of less
invasive surgical procedures on a more regular basis. Furthermore,
the volumetric changes in grafted area after SFE procedures are cru-
cial in order to avoid the possibility of not achieving the amount of
bone necessary for implant placement. Although these changes have
been described in literature, they remain unclear (Browaeys, Bouvry,
& De Bruyn, 2007; Wanschitz, Figl, Wagner, & Rolf, 2006; Zijderveld,
Schulten, Aartman, & ten Bruggenkate, 2009).
To assess the augmented bone volume, different techniques have
been proposed in literature (Szabo et al. 2005). Two-­dimensional (2D)
peri-­apical radiographs or panoramic radiographs are helpful in the
analysis of the vertical dimension of the graft. On the other hand, they
do not provide any additional information on the three-­dimensional
(3D) volume of the graft.
Recently, three-­dimensional (3D), cone-­beam computed tomogra-
phy (CBCT) analysis has been described as a fast, simple, relatively
accurate and promising approach to quantify long-­term changes in
the grafted area (Ohe et al., 2016; Umanjec-­Korac, Parsa, Darvishan
Nikoozad, Wismeijer, & Hassan, 2016).
The aim of this pilot clinical trial was to provide information
on the volumetric changes of the grafted area with different SFE
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Clinical Relevance
Scientific rationale for the study: Lots of attention in recent
year has gone to the influence of biomaterials on volumetric
stability of the grafted sites when performing sinus floor el-
evations procedures. However, no attention has gone to the
influence of the surgical technique on this volumetric stabil-
ity. Less invasive techniques are said to cause less post-­op
discomfort to the patients, however, no split-­mouth trails
are available.
Principal findings: All SFE techniques are able to augment in
sufficient way and provoke a partially transient swelling of
the Schneiderian membrane. No statistical significant cor-
relation between the post-­
operative swelling of the
Schneiderian membrane and reduction of graft volume
could be obtained. Transcrestal techniques using oste-
otomes seem to provoke more post-­
op discomfort for
patients.
Practical implications: Less invasive techniques are a valuable
treatment option in SFE. Osteotomes need to be handled
with care in order to decrease post-­op discomfort.
techniques (primary outcome measure). Furthermore, the influence
of the thickness of the Schneiderian membrane, pre-­operatively and
post-­operatively, on the volumetric changes of the grafted site was
assessed (secondary outcome measure). The impact of the different
treatment modalities on the per-­and post-­operative pain and sensa-
tion was also recorded (tertiary outcome measure).
2 | MATERIAL AND METHODS
The study was designed as a pilot prospective clinical trial. The study
was approved by the Ethical Committee of the KU Leuven, UZ Leuven
University Hospitals (S55459). This study was conducted in accord-
ance with the requirements of the Helsinki Declaration of 1975 and
revised in 2008.
2.1 | Patient population
Patients had to fulfil the following inclusion criteria: no history of sys-
temic diseases, non-­smoking, no previous attempt for SFE and no pre-
sent sinus pathology as assessed on a pre-­operative CBCT (thickening
of the sinus mucosa of more than 2.5 mm). Furthermore, they were
in need of bilateral SFE procedures in order to obtain an implant sup-
ported rehabilitation. All patients were given oral and written informa-
tion on the study protocol and its procedures and were asked to sign
the Informed Consent form. From 2012 to 2015, 18 patients were
enrolled in this study (Table 1). Patients presented with a RBH ranging
from 0.7 mm to 6.1 mm (mean 3.1 mm) as measured on the respective
CBCT cross-­sectional slices.
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662       TEMMERMAN et al.

T A B L E   1   Patient demographics and

Overall lSFE tSFE IL
overview between treatments with
Age Mean Mean Mean Mean simultaneous and delayed implant
56.6 year 57.2 year 53.9 year 57.5 year placement
(28–78 y) (43–78) (28–68) (28–78)
Gender (male/female) 7/11 5/8 4/4 5/10
Implants placed simultane- 21/38 7/20 9/1 5/17
ous/delayed
Changes in graft volume p = 0.97 p = 0.49 p = 0.97
(T2−T1) simultaneous vs.
delayed
Membrane volume changes p = 0.73 p = 0.39 p = 0.24
(T1) with simultaneous vs.
delayed
Membrane volume changes p = 0.29 p = 0.28 p = 0.03
(T2−T1) simultaneous vs.
delayed

2.2 | Patient allocation
Based on the RBH of the left and right maxillary sinus of each patient,
the following treatments were allocated: lSFE, tSFE and IL. Whenever
the RBH was ≥4 mm, one of the treatment options was randomly as-
signed. However, whenever the RBH was <4 mm, IL or lSFE were ran-
domly assigned.
2.3 | Surgical Procedures
All SFE procedures were performed under local anaesthesia and
strictly sterile conditions. Prior to surgery, a venipuncture was per-
formed. Venous blood was drawn into eight sterile, plastic 10 mL
tubes without anticoagulant. Leukocyte and platelet rich fibrin ­(L-­PRF)
clots and membranes were prepared as described by Choukroun and
co-­
workers (Choukroun, Adda, Schoeffler, & Vervelle, 2001). The
tubes were centrifuged at 2700 rpm and 409 g rotations per minute
®
for 12 min using a table centrifuge (IntraSpin™, IntraLock , Florida,
USA). After centrifugation, L-­PRF clots were removed from the tube
and separated from the red element phase at the base with pliers. Four
L-­PRF clots were squeezed between a sterile glass plate and a metal
box. All surgical procedures were performed by the same surgeon (AT).
The lSFE procedures were performed as follows:After crestal in-
cision, a mucoperiosteal flap was raised to visualize the lateral wall
of the maxillary sinus. Piezosurgery (Acteon®, Satelec, Piezotome II™,
France) was used to prepare the lateral window. The lateral sinus wall
was pushed inwards, after detachment of the Schneiderian mem-
brane from the inner maxillary sinus walls with hand instruments, via
a ‘trapped door technique’. Deproteinized bovine bone matrix (DBBM;
®
BioOss™, Geistlich , Wolhusen Switzerland) mixed with L-­
PRF (in
a 60–40%) was used to fill the antrum (Ali, Bakry, & Abd-­Elhakam,
2015; Bolukbasi, Ersanlı, Keklikoglu, Basegmez, & Ozdemir, 2015).
­L-­PRF membranes were used to cover the grafted site and the lateral
osteotomy (Gassling et al., 2013).
tSFE procedures were performed as follows:After crestal incision,
a limited mucoperiosteal flap was elevated. Rotating burs were used to
perform the initial osteotomy and to reach the inferior maxillary sinus
wall. Afterwards, an L-­PRF membrane was inserted into the osteotomy
and osteotomes were used to enter the maxillary sinus by gently tap-
ping the osteotome with a hand mallet. A mixture of DBBM and L-­PRF
(in a 60–40%) was used to fill the antrum.
The IL procedures were performed as follows:After crestal incision,
a limited mucoperiosteal flap was raised. The maxillary sinus was en-
tered using piezosurgery and the Intralift™ inserts. The Schneiderian
membrane was elevated using the hydrodynamic, cavitational effect
after inserting a collagenous sponge. A mixture of L-­PRF and DBBM
(in a 60–40%) was used to fill the antrum.
Osteotomy site preparation was performed using a conventional
rotary instrument according to the implant manufacturer guidelines
(AstraTech Osseospeed TX™, DentsplyImplants®, Mölndal, Sweden).
The possibility of placing of implants at the same time of the SFE pro-
cedure, was left to the opinion of the surgeon in charge, and was based
on the amount of RBH and bone quality, as assessed during surgery.
The amount of graft material inserted varied according to the size of
defect to be filled. Suturing (Prolene 4.0 or 5.0, Ethicon™, Johnson &
Johnson®) was performed in two layers using horizontal mattress su-
tures and individual double-­O sutures. All patients received antibiotics
(amoxicilline + clavulanic acid 500/125 mg for 7 days) and were asked
to take NSAIDs, three times a day (Ibuprofen 600 mg) for 5 days and
to use an antiseptic spray twice a day for 1 week (PerioAid™ Spray
0.12%, Dentaid®, Spain). Furthermore, they received a nasal spray
containing corticosteroids (Nasonex 50 μg, mometasonfuroate) to be
used once a day, for 7 days. Patients were asked to answer some ques-
tions regarding the surgical techniques in order to evaluate a patient’s
preference. Sutures were removed after 7–10 days.
2.4 | Pain scales
To assess post-­operative pain, the Dutch version of the McGill Pain
Questionnaire (MPQ-­DLV) was used (Melzack, 2005). The question-
naire was handed out as a diary and patients were asked to fill in the
questions every day, from day 1 until day 7. This questionnaire used
TEMMERMAN et al.
100 mm VAS-­scales to evaluate the amount of pain, ranging from 0
(no pain) to 100 (worst pain imaginable) and the amount of swelling
for each site separately.
Patients were asked to score (on VAS-­scales) the minimum and
maximum amount of pain experienced during the last 24 hr, starting
from the day of surgery to day 7. In order to enhance the quality of
pain scores, patients were asked to score every 4 hr at the day of sur-
gery. They were also asked to score the following questions: if they
would repeat the procedure in the future, if the duration of each pro-
cedure was tolerable. Questionnaires were collected at the 1 week
follow-­up visit.
2.5 | Data acquisition and quantitative visualization
resolution CBCT images (3D Accuitomo™ 170, Morita®,
High-­
Kyoto, Japan) were obtained based on clinical justification by the
treating implant surgeon as part of the treatment protocol (pre-­
operatively [T0], one [T1] and six [T2] week follow-­up) to allow
an accurate surgical planning and a reliable post-­operative evalu-
ation of the bone healing at the level of the maxillary sinus floor
(Department OMFS-­Impath). A 100 × 100 mm field of view was
chosen to include a view of both maxillary sinuses. Scanning param-
eters were fixed at 90 kV, 5 mA, 17.5 exposure time and standard
180° rotation. All data sets were exported in DICOM format with
an isotropic voxel size of 250 μm³. The post-­operative scans were
spatially matched to the pre-­operative CBCT by a rigid image regis-
tration using maximization of mutual information (Maes, Collignon,
Vandermeulen, Marchal, & Suetens, 1997). The aligned scans were
imported into MeVisLab™ (MeVis Medical Solutions AG, Bremen,
Germany) and an experienced implant surgeon, blinded for SFE
technique, applied the semi-­interactive livewire boundary extrac-
tion (Barret & Mortensen, 1997) tool to extract the sinus cavity and
membrane. The livewire technique helps the operator to objectively
select the most desirable path around edges using the lowest cost
pat algorithm. After extraction, a 3D surface of the sinus and mem-
brane were reconstructed without being smoothed to preserve its
raw volume measurement.
2.6 | Statistical analysis
2.6.1 | Graft volumes, membranes volumes and
comparisons between treatments
Membrane volumes at 1 week were compared between treatments by
means of a linear mixed model with patient and treatment as random
factor. Comparisons between treatments were corrected for simulta-
neous hypothesis testing according to Tukey. The same analysis was
repeated for the differences between membrane volume at 1 week
and the volume recorded prior to surgery, once for the absolute dif-
ferences and once for the percentage differences. Normal quantile
plots of the residuals showed that the data could be analysed without
transformation, except for the percentage differences, where a log-­
transformation was applied. Analysis was performed for the total of
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all treatments and for the treatments with and without simultaneous
implant placement.
2.6.2 | Post-­operative questionnaires
Comparisons between treatments were performed for each time
separately by means of a Wilcoxon signed rank test. Comparisons
between measurements performed at distinct times were made by
means of a paired Wilcoxon signed rank test with the patient as the
pairing factor. For both types of comparisons, a correction for simulta-
neous hypothesis testing was applied according to Sidak.
All analyses were performed using S-­Plus 8.0 for Linux (Tibco, Palo
Alto, CA, USA).
3 | RESULTS
In total, 36 SFE treatments were performed (13 lSFE, 8 tSFE and
15 IL). In total, 59 implants were placed in augmented sites (21 were
placed simultaneously with the SFE and 38 were placed after a heal-
ing period of 6 months – Supplementary Table 1). In the lSFE group,
two ruptures of the Schneiderian membrane occurred during eleva-
tion. Both of them could be treated using a L-­PRF membrane to cover
the rupture.
3.1 | Graft Volume and Schneiderian membrane
volume (Figure 1 +  Table 2 and 3)
The average pre-­operative volume of the Schneiderian membrane
(SMV) of all surgical sites was 4.53 cm3 (range: 0.59–21.12 cm3).
There was no statistical difference between initial SMV of the three
treatments (see Tables 2 and 3). One week after surgery, the volume
of the Schneiderian membrane rose to 11.27 cm3 (+148.43%) on av-
erage over all surgical sites (range 2.57–40.39 cm3). Overall, no sta-
tistical significant differences could be seen between all treatment
options with regard to the swelling of the Schneiderian membrane.
The placement of implants simultaneously with the SFE did not have
any significant influence on the swelling of the Schneiderian mem-
brane (p > 0.05).
However, when the change in SMV was calculated, the lSFE pro-
voked more swelling than the tSFE (p = 0.02). Between all other treat-
ment options, no statistically significant differences could be seen
(p > 0.05). After 6 weeks, the overall SMV was 6.85 cm3 (range 1.10–
43.19 cm3), about 39.19% less than the volume at 1 week. The decrease
in SMV was not statistically significant between all treatments, nor
treatments with or without simultaneous implant placement (p > 0.05).
The overall average graft volume obtained after 1 week was
1.87 cm3 (range 0.12–4.72 cm3). This volume decreased after 6 weeks
to an overall mean volume of 1.33 cm3 (range 0.10–4.29 cm3), which
counts for an average decrease of 27.6%. When considering obtain-
able graft volumes with the different treatment modalities, we could
see average graft volumes ranging from 0.64 cm3 for the tSFA treat-
ment, over 1.77 cm3 for the IL treatment to 2.83 mm3 for the lSFE
 |
664       TEMMERMAN et al.

F I G U R E   1   3D and volumetric analysis

of CBCT images and respective 3D models
(a) (b)
of a study patient. lSFE was performed on
the right, IL was performed on the left. (a)
pre-­operative, baseline 3D full maxillary
sinus volumes (blue) and Schneiderian
membrane volumes (red). (b) pre-­operative
maxillary sinus volumes (red). (c) post-­
operative maxillary sinus (red) and graft
volume (yellow) at T1. (d) post-­operative
(c) (d) maxillary sinus (red) and graft volume
(yellow) at T2

T A B L E   2   Overview of graft volumes & volumetric changes

Transcrestal sinus floor elevation

Surgical technique Lateral sinus floor elevation (lSFE) (tSFE) Intralift sinus floor elevation (IL)

Time points T0 T1 T2 T0 T1 T2 T0 T1 T2
3
Graft volume(cm ) 2.84 2.14 0.63 0.49 1.77 1.17
SD: 1.22 SD: 1.20 SD: 0.33 SD: 0.29 SD: 1.49 SD: 0.98
(0.8–4.72) (0.62–4.29) (0.17–1.28) (0.09–1.14) (0.12–3.91) (0.09–3.45)
Graft volume −24.55% (T2−T1) −23.13% (T2−T1) −33.7% (T2−T1)
reduction
p-­values (overall) lSFE vs. tSFE
(simultaneous) (p = 0.62)overall, (p = 0.98)simultaneous, (p = 0.39)delayed
(delayed) tSFE vs. IL
(p = 0.98)overall, (p = 0.99) simultaneous, (p = 0.87)delayed
lSFE vs. IL
(p = 0.45)overall, (p = 0.97) simultaneous, (p = 0.51)delayed

treatment. After 6 weeks, the amount of graft volume decreased in

every treatment option, ranging from −23.13% for the tSFE, over
−24.55% for the lSFE, to −33.71% for the IL. No statistically significant
difference could be obtained between tSFE and lSFE. Simultaneous
implant placement did not interfere significantly with the volumetric
changes after 6 weeks (p > 0.05).
3.2 | Influence of the swelling of the Schneiderian
membrane on the graft volume after 6 weeks
The difference between graft volumes after 6 weeks and 1 week
were graphically explored. Afterwards, a Spearman rank correlation
was used to detect any possible correlation. Although all treatment
options correspond in an increase in SMV, no statistically significant
correlation between this increase and loss of graft volume could be
obtained for all treatments (p = 0.97). When treatments with and
without implant placement were analysed separately, no differences
could be found (p = 0.58 and p = 0.38, respectively).
3.3 | Post-­operative questionnaires
Post-­operative questionnaires revealed no significant statistical dif-
ferences in subjective surgery times (lSFE vs. tSFE [p = 0.59]; lSFE vs.
IL [p = 0.62]; tSFE vs. IL [p = 0.9]) or subjective feeling or preference
towards the three procedures (p > 0.05).
Overall, no significant differences could be seen between the sub-
jective swelling sensation provoked by each treatment on day 1 and
day 2 (p > 0.05). From day 3 onwards, tSFE and IL scored significantly
less in subjective swelling when compared to lSFE (p < 0.05). For tSFE
vs. IL, no significant differences could be detected (p > 0.05) (Figure 2;
Table 4).
Concerning the post-­operative pain sensation, there is a trend that
the tSFE evokes more pain during the very early stages of healing (at
8 h compared to lSFE and at 8 h, 12 h, day 2 compared to IL). From day
3 onwards, no significant differences could be seen between tSFE and
IL. Overall, the IL procedures scored significantly better than the lSFE
during days 4, 5, 6 and 7.
 TEMMERMAN et al.

T A B L E   3   Overview of Schneiderian membrane volumes & volumetric changes

Surgical technique Lateral sinus floor elevation (lSFE) Transcrestal sinus floor elevation (tSFE) Intralift sinus floor elevation (IL)

Time points T0 T1 T2 T0 T1 T2 T0 T1 T2

Membrane volume 4.88 14.01 7.54 4.10 9.21 8.21 4.04 10.13 5.14
(in cm3) SD: 5.62 SD: 9.35 SD: 11.11 SD: 2.85 SD: 4.68 SD: 10.95 SD: 4.09 SD: 5.01 SD: 3.41
(0.59–21.13)a (4.73–40.39) (0.99–43.19) (0.65–8.32)a (2.57–17.29) (1.23–37.17) (0.03–13.64)a (2.87– (1.70–8.95)
20.24)
Membrane volume T0 + 187.14% T1-­46.1% T0 + 124.83% T1-­10.97% T0 + 172.05% T1-­53.21%
changes (T0 + 54.57%) (T0 + 100.15%) (T0 + 27.27%)
p-­value (overall) lSFE vs. tSFE
(simultaneous) (p = 0.16)T1overall, (p = 0.25)T1simultaneous, (p = 0.49)T1delayed
(delayed) at T1 & T2 (p = 0.04)T2overall, (p = 0.70)T2simultaneous, (p = 0.01)T2delayed
tSFE vs. IL
(p = 0.79)T1overall, (p = 0.38)T1simultaneous, (p = 0.97)T1delayed
(p = 0.38)T2overall, (p = 0.51)T2simultaneous, (p = 0.21)T2delayed
lSFE vs. IL
(p = 0.31)T1overall, (p = 0.88)T1simultaneous, (p = 0.37)T1delayed
(p = 0.26)T2overall, (p = 0.80)T2simultaneous, (p = 0.18)T2delayed
a
No statistical significant difference were found for the pre-­operative Schneiderian membrane volume between the three groups (p = 0.72).
|
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have been a co-­factor. Although there is no precise threshold for a nor-

4 |  DISCUSSION
mal radiographic sinus mucosa thickness, 2 mm is often used in many
studies (Cagici, Yilmazer, Hurcan, Ozer, & Ozer, 2009; Janner et al.,
The results of this pilot, clinical trial show that the surgical act of sinus
2011). In order not to include patients with enlarged mucosal thick-
augmentation, being lSFA, tSFE or IL, results in a transient clinical re-
ness and to make the included group of patients as homogenous as
action (swelling) of the Schneiderian membrane. Furthermore, there
possible, patients with a mucosal thickness of 2.5 mm were excluded.
seems to be no statistical significant correlation between the swell-
Lots of attention in recent years has gone to different types of
ing of the Schneiderian membrane and the amount of graft reduction
grafting materials. Stability of graft volume is considered an import-
after 6 weeks.
ant factor in the success of a SFE procedure. Evidence clearly shows
The transient swelling of the Schneiderian membrane has already
that autogenous particulated bone (APB) is prone to severe volumetric
been described by Quirynen and co-­
workers (Quirynen, Lefever,
changes over time. Sbordone et al. (2013) showed a decrease of the
Hellings, & Jacobs, 2014). In this study, 2D measurements were made
APB graft volume with 23% at 6 months after lSFE and with 39.2%
on CBCT images and the authors concluded that a tSFA technique
after 6 years. Results seem to be better when using autogenous bone
results in transient swelling of the membrane, 5–10 times its origi-
blocks (−21.5% after 6 years). Other studies showed an even bigger
nal thickness. After a healing period of 6 months, the thickness of
graft volume reduction (−42.30% to −49.5%) at 6 months (Cosso, de
the membrane normalized to its original thickness, leaving no post-­
Brito, Piattelli, Shibli, & Zenóbio, 2014; Johansson, Grepe, Wannfors,
operative complication for the patients. In the present study, a de-
Aberg, & Hirsch, 2001). However, when the APB was mixed with hy-
crease in SMV over 6 weeks can be seen. Recent studies indicated
droxyapatite in a 20/80 scale, the GVR could be reduced to −25.8%.
no significant changes in membrane thickness after a healing period
Therefore, it seems logical that different biomaterials may influence
of 7–9 months (Anduze-­Acher et al., 2013; Guo et al., 2016). This ob-
the graft volume stability before implant placement, but eventually
servation confirms that the mucociliary function will recover from SFE
also the stability of implants themselves (Browaeys et al., 2007). There
without having an impact on the natural sinus physiology (Timmenga
is some evidence to support that DBBM seems to offer a more stable
et al., 2003). The swelling of the membrane probably can be explained
graft volume than mineralized and composite allografts. DBBM is a
by the surgical trauma induced when elevating the sinus mucosa from
material with a very slow resorption rate and offers a good scaffold
the sinus walls, resulting in a per-­and post-­operative bleeding. On the
for natural bone growth during healing and integration period of the
other hand, the intimate contact between the sinus mucosa and the
graft. This slow resorption rate probably explains the volumetric stabil-
sharp-­edged biomaterial particles (as can be seen on scanning elec-
ity after SFE procedures, even during longer healing periods (Boyne &
tron microscope (Vivan et al., 2016)), may cause ‘microruptures’ in
James, 1980; Chiapasco, Casentini, & Zaniboni, 2009). In the present
the sinus mucosa. The present study shows that the swelling of the
study, a mixture (60/40) of DBBM and L-­PRF was used which showed
Schneiderian membrane is depended on the type of surgical proce-
a 1.4 times higher new bone formation (Zhang et al., 2012).
dure. The lSFE seems to provoke a more intense swelling as compared
To our best knowledge, this is the first study to assess the influ-
to the tSFE. This may be explained by the more intense surgical ma-
ence of various surgical SFE techniques on volumetric changes. Graft
nipulation during surgery. However, this is just speculative and needs
volumes after lSFE seems to be around 2,500 cm3 when assessed vol-
to be confirmed by studies. This study failed to prove a possible asso-
umetrically. However, a study by Mazzocco ad co-­workers was only
ciation between the transient swelling of the Schneiderian membrane
able to obtain an mean graft volume of 1.43 cm3 when performing a
and the amount of graft volume reduction after 6 weeks, which could
lSFE (Mazzocco et al., 2014). To our best knowledge, no information
lSFE tSFE IL can be found in literature on the obtainable graft volumes after a tSFE
6

Average pain
or IL. In the present study, the amount of graft volume obtainable with
the IL treatment was less than those could be obtained with the lSFE.
5

Nevertheless, this results should be considered with caution, as the

Pain score, VAS−scale

hydrodynamic pressure and cavitational effect is able to fully elevate

4

MIN pain
the Schneiderian membrane which gives the surgeon the opportunity
to graft in various sizeable volumes (Troedhan et al., 2012, 2014). The
3

graft volume obtained with tSFE was significant less than the other
2

MAX pain treatments options.

Various volumetric graft reduction rates have been reported in dif-
1

ferent studies, even when the same biomaterial was used (Cosso et al.,
2014; Gultekin, Borahan, Sirali, Karabuda, & Mijiritsky, 2016; Kim,
0

0 2 4 6 0 2 4 6 0 2 4 6 Moon, Kim, Park, & Oh, 2013; Kirmeier et al., 2008; Mazzocco et al.,
Day Day Day 2014; Sbordone et al., 2014; Umanjec-­Korac et al., 2016). The present
study can agree on this, as the same composition of biomaterials was
F I G U R E   2   Graphical presentation of VAS-­scale for the
representative treatment options. In the Y-­axis, the pain sensation used for every treatment option. In comparison to the aforementioned
and in the X-­axis the time studies, the present study has a shorter observation period, as we
TEMMERMAN et al. |
      667

T A B L E   4   Post-­operative subjective swelling and pain differences as scored on VAS-­scales, between 3 treatment options (lSFE, tSFE and IL)
with respective p-­values

Timepoint lSFE vs. tSFE p-­value lSFE vs. IL p-­value tSFE vs. IL p-­value

Surgery + 4 hr lSFE = tSFE 0.44 lSFE = IL 0.53 tSFE = IL 0.58

Surgery + 8 hr lSFE = tSFE 0.84 lSFE = IL 0.10 tSFE = IL 0.16
Surgery +12 hr lSFE = tSFE 0.69 lSFE = IL 0.11 tSFE = IL 0.50
Surgery + 2 days lSFE = tSFE 0.39 lSFE = IL 0.09 tSFE = IL 0.62
Surgery + 3 days lSFE > tSFE 0.04 lSFE > IL 0.02 tSFE = IL 0.98
Surgery + 4 days lSFE > tSFE 0.01 lSFE > IL 0.02 tSFE = IL 0.87
Surgery + 5 days lSFE > tSFE 0.01 lSFE > IL 0.02 tSFE = IL 0.77
Surgery + 6 days lSFE = tSFE 0.09 lSFE > IL 0.04 tSFE = IL 0.63
Surgery + 7 days lSFE = tSFE 0.14 lSFE > IL 0.02 tSFE = IL 0.50

Timepoint lSFE vs. tSFE p-­value lSFE vs. IL p-­value tSFE vs. IL p-­value

MAX pain Surgery + 4 hr lSFE = tSFE 0.09 lSFE = IL 0.94 tSFE = IL 0.06

sensation Surgery + 8 hr lSFE < tSFE 0.02 lSFE = IL 0.98 tSFE > IL 0.03
Surgery +12 hr lSFE = tSFE 0.12 lSFE = IL 0.50 tSFE > IL 0.04
Surgery + 2 days lSFE = tSFE 0.41 lSFE = IL 0.16 tSFE > IL 0.03
Surgery + 3 days lSFE = tSFE 0.76 lSFE = IL 0.06 tSFE = IL 0.12
Surgery + 4 days lSFE = tSFE 0.56 lSFE > IL 0.03 tSFE = IL 0.19
Surgery + 5 days lSFE = tSFE 0.15 lSFE > IL 0.02 tSFE = IL 0.43
Surgery + 6 days lSFE = tSFE 0.08 lSFE > IL 0.02 tSFE = IL 0.89
Surgery + 7 days lSFE = tSFE 0.15 lSFE > IL 0.01 tSFE = IL 0.43
MIN pain Surgery + 4 hr lSFE = tSFE 0.44 lSFE = IL 0.94 tSFE = IL 0.19
sensation Surgery + 8 hr lSFE = tSFE 0.25 lSFE = IL 0.62 tSFE = IL 0.22
Surgery +12 hr lSFE = tSFE 1 lSFE = IL 0.30 tSFE = IL 0.48
Surgery + 2 days lSFE = tSFE 0.92 lSFE = IL 0.15 tSFE = IL 0.40
Surgery + 3 days lSFE = tSFE 0.64 lSFE > IL 0.03 tSFE = IL 0.60
Surgery + 4 days lSFE = tSFE 0.38 lSFE = IL 0.07 tSFE = IL 0.61
Surgery + 5 days lSFE = tSFE 0.17 lSFE > IL 0.03 tSFE = IL 0.78
Surgery + 6 days lSFE = tSFE 0.40 lSFE = IL 0.06 tSFE = IL 0.55
Surgery + 7 days lSFE = tSFE 0.50 lSFE = IL 0.06 tSFE = IL 0.23
AVG pain Surgery + 4 hr lSFE = tSFE 0.06 lSFE = IL 0.78 tSFE > IL 0.04
sensation Surgery + 8 hr lSFE = tSFE 0.07 lSFE = IL 0.80 tSFE > IL 0.04
Surgery +12 hr lSFE < tSFE 0.04 lSFE = IL 0.40 tSFE > IL 0.03
Surgery + 2 days lSFE = tSFE 0.38 lSFE = IL 0.18 tSFE = IL 0.06
Surgery + 3 days lSFE = tSFE 0.75 lSFE = IL 0.07 tSFE = IL 0.32
Surgery + 4 days lSFE = tSFE 0.45 lSFE > IL 0.01 tSFE = IL 0.23
Surgery + 5 days lSFE = tSFE 0.18 lSFE > IL 0.01 tSFE = IL 0.51
Surgery + 6 days lSFE = tSFE 0.29 lSFE > IL 0.02 tSFE = IL 0.45
Surgery + 7 days lSFE = tSFE 0.34 lSFE = IL 0.06 tSFE = IL 0.41

wanted to examine a possible influence of the transient swelling of the
Schneiderian membrane on the attainable graft volumes. The differ-
ences in volumetric reduction rates may be explained by some patient
depended factors: number of missing teeth, anatomy of the maxillary
sinus, repneumatization capacity of the patient, contact osteogenesis
capacity of the residual wall surface area connected to the graft ma-
terial and remaining alveolar height (Kirmeier et al., 2008; Shanbhag,
Shanbhag, & Stavropoulos, 2014). Nevertheless, the surgeon himself
can influence this by choosing the graft material (Cosso et al., 2014;
Gultekin et al., 2016; Sbordone et al., 2014), influencing the compres-
sion force during insertion of the graft and the surgical technique, as
shown by the present study. Furthermore, different measuring tech-
niques and software variations will lead to differences in reduction
rates. However, quite some studies come to the conclusion that 3D
 |
668       TEMMERMAN et al.
analysis is a very promising and accurate tool in quantifying the long-­
term changes of the grafted area (Cosso et al., 2014; Gultekin et al.,
2016; Ohe et al., 2016). Studies have shown that 3D techniques are
more accurate than 2D techniques when assessing the resorption of
the grafted bone (Kim et al., 2013).
In order to perform accurate measurements, the use of high-­
resolution CBCT scans seems justifiable when taking into account the
average thickness of the Schneiderian membrane (0.79 ± 052 mm;
Insua et al., 2016) and the thickness of the inferior and lateral max-
illary sinus wall (1–2 mm; Monje et al., 2016). High-­resolution CBCT
images, like the ones used in the present study, seem to show the least
measurement errors in cortical and trabecular bone (Van Dessel et al.,
2016). Based on the results of the present study, a post-­operative
CBCT scan, 6 weeks after the surgery, seems to be of clinical impor-
tance in order to visualize the graft volume and increased thickness of
the Schneiderian membrane.
Inherently, every surgical procedure has advantages and shortcom-
ings. So do the various SFE techniques. The lSFE, can be seen as the
gold standard in SFE techniques (Del Fabbro et al., 2013). Its inherent
advantages are the per-­operative visibility and complication manage-
ment (as could be achieved in the 2 out of 13 lSFE (15%) performed in
this study) and the possibility to augment large volumes. However, one
has to be aware that a good pre-­operative planning on CBCT is a pre-
requisite when performing a lSFE (Tadinada et al., 2016; Temmerman
et al., 2011). Due to the fact that a lateral osteotomy has to be made,
the anatomical structures have to be visualized as good as possible in
order not to cause vascular damage. Indeed, the posterior superior al-
veolar artery, a branch of the infraorbital artery (Traxler et al., 1999) is
running in the bony lateral sinus wall, providing its vascularization. The
diameter can be up to 4 mm (Temmerman et al., 2011). Damaging this
vascular structure will not only provoke a per-­operative arterial bleed-
ing, but may also possibly lead to necrosis of the bony lateral sinus
wall, loss of the graft material and/or implants (Danesh-­Sani, Movahed,
ElChaar, Chong Chan, & Amintavakoli, 2016; Güncü, Yildirim, Wang, &
Tözüm, 2011; Khojastehpour, Dehbozorgi, Tabrizi, & Esfandnia, 2016).
The tSFE (Summers, 1994) is a less invasive technique and possibly
this technique reduces the treatment time. The drawbacks of this
technique are the limited intra-­operative complication management
and the, although rare, complication of benign paroxysmal positional
vertigo (BPPV). It includes the displacement of otoliths by vibratory
forces transmitted by osteotomes and mallet along with the hyperex-
tension of the head during the operation, causing them to float around
in the endolymph (Akcay, Ulu, Kelebek, & Aladag, 2016; Giannini et al.,
2015; Pjetursson & Lang, 2014). Unexpectedly, the data of this study
shows that this technique causes the most post-­operative pain during
the first two post-­operative days. The tapping of the osteotome with
a mallet seems to have a bigger impact for the patient than it was
thought to have in the past. Further research should be done on how
to replace this tapping procedure.
In literature, tSFE procedures are predominantly used when the
RBH is >5 mm, as a lesser remaining bone height may not allow a pri-
mary implant stability (Pjetursson & Lang, 2014). However, recently
tSFE have been successfully used in patients with less RBH (Nedir
et al., 2013; Si et al., 2013) and extreme cases (Nedir et al., 2014). For
now, a critical threshold in RBH cannot be indicated due to the lack on
data (Chao, Chen, Mei, Tu, & Lu, 2010). In the present study, 4 mm was
used as a threshold for the tSFE procedures. Whenever the RBH was
less, lSFE and IL where randomly allocated. It can be seen that the tSFE
technique is able to generate lesser amounts of bone. Nevertheless,
this can be argued because this technique is predominantly used in
1–2 teeth diastema.
The IL procedure is based on a minimal invasive hydrodynamic ele-
vation technique to lift the sinus mucosa from a crestal approach, using
specially developed inserts and ultrasound in order to be as atraumatic
as possible and diminish the post-­
operative discomfort (Troedhan
et al., 2012; Wainwright et al., 2016). The limited intra-­operative visi-
bility and impossibility of complication management remain the main
shortcomings of this technique. However, the main advantage is the
augmentation quantities of large scales, due to a enhanced detach-
ment of the Schneiderian membrane (Troedhan et al., 2014) and the
inherent small post-­operative burden for the patient. In the 15 IL sur-
geries performed in this study, no complications were encountered.
Nevertheless, when performing this technique, surgeons have to be
aware that ruptures of the Schneiderian membrane are very difficult
to detect. Noteworthy is the fact that an enhanced detachment of the
Schneiderian membrane can also be seen as a shortcoming, as sur-
geons (who are less experienced with this technique) will have difficul-
ties in acquiring a subjective feeling of the augmented volumes.
The simultaneous placement of implants did not seem to interfere
with the volumetric changes of the graft after 6 weeks. However, there
is a good chance that this can be explained by the rather short evalua-
tion period (6 weeks). No long-­term analysis of the graft volume, after
implant loading was performed. Although it seems reasonable that
when performing long-­term analysis, the placement of implants simul-
taneous with the SFE might become more important. This short-­term
analysis, therefore, can be seen as the main shortcoming of this study.
Studies have shown that even after functional loading of oral implants
placed in the augmented maxillary sinus, an ongoing volumetric re-
sorption takes place (Berberi et al., 2015; Zijderveld et al., 2009).
5 | CONCLUSION
Within the limitations of the present prospective, pilot clinical trial,
it can be concluded that all three surgical SFE techniques were able
to provide sufficient graft volume for further implant treatment. All
techniques provoked a partially transient swelling of the Schneiderian
membrane, which is significantly bigger when using a lSFE tech-
nique. All surgical techniques resulted in a decrease in graft volume
after 6 weeks; however, no significant differences were obtained be-
tween treatments. Furthermore, no statistical significant correlation
between the post-­operative swelling of the Schneiderian membrane
and reduction in graft volume at 6 weeks could be obtained. The IL
technique caused the least post-­operative discomfort to the patient,
definitely during the early phases of healing. This technique has to be
handled with care, as the surgeons’ subjective feeling on augmented
TEMMERMAN et al. |
      669

volumes can be hampered. The surgical act of tapping the osteotome Chiapasco, M., Casentini, P., & Zaniboni, M. (2009). Bone augmentation
during a tSFE should not be underestimated as the tSFE causes more procedures in implant dentistry. The International Journal of Oral &
Maxillofacial Implants, 24, 237–259.
post-­operative discomfort during the first days of healing.
Choukroun, J., Adda, F., Schoeffler, C., & Vervelle, A. (2001). An opportunity
in perio-­implantology: The PRF. Implantodontie, 4255–4262.
ACKNOWLE DGME N TS Cosso, M. G., de Brito, R. B., Piattelli, A., Shibli, J. A., & Zenóbio, E. G. (2014).
Volumetric dimensional changes of autogenous bone and the mixture
The authors acknowledge Dr. Wim Coucke for his support in the of hydroxyapatite and autogenous bone graft in humans maxillary sinus
augmentation. A multislice tomographic study. Clinical Oral Implants
statistical analysis. Jeroen Van Dessel is a researcher supported
Research, 25, 1251–1256.
by Research Foundation Flanders (FWO). We acknowledge GC
Danesh-Sani, S. A., Movahed, A., ElChaar, E. S., Chong Chan, K., &
Europe NV for the scientific chair in bio-regeneration and Intra- Amintavakoli, N. (2016). Radiographic evaluation of maxillary sinus lat-
Lock International Inc. for the scientific chair in optimization of eral wall and posterior superior alveolar artery anatomy: A cone-­beam
osseointegration. computed tomographic study. Clinical Implant Dentistry and Related
Research, 25, 1251–1256.
Del Fabbro, M., Wallace, S. S., & Testori, T. (2013). Long-­ term im-
CO NFLI CT OF I NTERE S T plant survival in the grafted maxillary sinus: A systematic review.
The International Journal of Periodontics & Restorative Dentistry, 33,
The authors have stated explicitly that there are no conflicts of inter- 773–783.
est in connection with this article. Esposito, M., Felice, P., & Worthington, H.V. (2014). Interventions for re-
placing missing teeth: Augmentation procedures of the maxillary sinus.
The Cochrane Database of Systematic Reviews, 13, CD008397.
REFERENCES Gassling, V., Purcz, N., Braesen, J.-H., Will, M., Gierloff, M., Behrens, E.,
… Wiltfang, J. (2013). Comparison of two different absorbable mem-
Akcay, H., Ulu, M., Kelebek, S., & Aladag, I. (2016). Benign paroxysmal
branes for the coverage of lateral osteotomy sites in maxillary sinus
positional vertigo following sinus floor elevation in patient with an-
augmentation: A preliminary study. Journal of Cranio-­Maxillo-­Facial
tecedents of vertigo. Journal of Maxillofacial and Oral Surgery, 15,
Surgery, 41, 76–82.
351–354.
Giannini, S., Signorini, L., Bonanome, L., Severino, M., Corpaci, F., & Cielo, A.
Al-Almaie, S., Kavarodi, A. M., & Al Faidhi, A. (2013). Maxillary sinus func-
(2015). Benign paroxysmal positional vertigo (BPPV): It may occur after
tions and complications with lateral window and osteotome sinus
dental implantology. A mini topical review. European Review for Medical
floor elevation procedures followed by dental implants placement: A
and Pharmacological Sciences, 19, 3543–3547.
retrospective study in 60 patients. The Journal of Contemporary Dental
Gultekin, B. A., Borahan, O., Sirali, A., Karabuda, Z. C., & Mijiritsky, E.
Practice, 14, 405–413.
(2016). Three-­ dimensional assessment of volumetric changes in si-
Ali, S., Bakry, S. A., & Abd-Elhakam, H. (2015). Platelet-­rich fibrin in max-
nuses augmented with two different bone substitutes. BioMed Research
illary sinus augmentation: A systematic review. The Journal of Oral
International, 2016, 4085079.
Implantology, 41, 746–753.
Güncü, G. N., Yildirim, Y. D., Wang, H.-L., & Tözüm, T. F. (2011). Location
Anduze-Acher, G., Brochery, B., Felizardo, R., Valentini, P., Katsahian, S., &
of posterior superior alveolar artery and evaluation of maxillary sinus
Bouchard, P. (2013). Change in sinus membrane dimension following
anatomy with computerized tomography: A clinical study. Clinical Oral
sinus floor elevation: A retrospective cohort study. Clinical Oral Implants
Implants Research, 22, 1164–1167.
Research, 24, 1123–1129.
Guo, Z.-Z., Liu, Y., Qin, L., Song, Y.-L., Xie, C., & Li, D.-H. (2016). Longitudinal
Barret, W.A., & Mortensen, E.N. (1997). Interactive live-­wire boundary ex-
response of membrane thickness and ostium patency following sinus
traction. Medical Image Analysis, 1, 331–341.
floor elevation: A prospective cohort study. Clinical Oral Implants
Berberi, A., Bouserhal, L., Nader, N., Assaf, R. B., Nassif, N. B., Bouserhal,
Research, 27, 724–729.
J., & Salameh, Z. (2015). Evaluation of three-­dimensional volumet-
Insua, A., Monje, A., Chan, H.L., Zimmo, N., Shaikh, L., & Wang, H.L. (2016).
ric changes after sinus floor augmentation with mineralized cortical
Accuracy of Schneiderian membrane thickness: A cone-­beam com-
bone allograft. Journal of Maxillofacial and Oral Surgery, 14, 624–629.
puted tomography analysis with histological validation. Clinical Oral
Bolukbasi, N., Ersanlı, S., Keklikoglu, N., Basegmez, C., & Ozdemir, T. (2015).
Implants Research. https://doi.org/10.1111/clr 12856. (Epub ahead of
Sinus augmentation with platelet-­rich fibrin in combination with bo-
print).
vine bone graft versus bovine bone graft in combination with collagen
Janner, S. F., Caverasaccio, M. D., Dubach, P., Sendi, P., Buser, D., &
membrane. The Journal of Oral Implantology, 41, 586–595.
Bornstein, M. M. (2011). Characteristics and dimensions of the
Boyne, P.J., & James, R.A. (1980). Grafting of the maxillary sinus floor with
Schneiderian membrane: A radiographic analysis using cone beam
autogenous marrow and bone. Journal of Oral Surgery(American Dental
computed tomography in patients referred for dental implant sur-
Association, 38, 613–616.
gery in the posterior maxilla. Clinical Oral Implants Research, 22,
Browaeys, H., Bouvry, P., & De Bruyn, H. (2007). A literature review on bio-
1446–1453.
materials in sinus augmentation procedures. Clinical Implant Dentistry
Jensen, T., Schou, S., Stavropoulos, A., Terheyden, H., & Holmstrup, P.
and Related Research, 9, 166–177.
(2012). Maxillary sinus floor augmentation with Bio-­Oss or Bio-­Oss
Cagici, C. A., Yilmazer, C., Hurcan, C., Ozer, C., & Ozer, F. (2009). Appropriate
mixed with autogenous bone as graft in animals: A systematic review.
interslice gap for screening coronal paranasal sinus tomography for
International Journal of Oral and Maxillofacial Surgery, 41, 114–120.
mucosal thickening. European Archives of Oto-­Rhino-­Laryngology, 266,
Johansson, B., Grepe, A., Wannfors, K., Aberg, P., & Hirsch, J. M. (2001).
519–525.
Volumetry of simulated bone grafts in the edentulous maxilla by
Chao, Y.-L., Chen, H.-H., Mei, C.-C., Tu, Y.-K., & Lu, H.-K. (2010). Meta-­
computed tomography: An experimental study. Dento Maxillo Facial
regression analysis of the initial bone height for predicting implant
Radiology, 30, 153–156.
survival rates of two sinus elevation procedures. Journal of Clinical
Kfir, E., Kfir, V., Goldstein, M., Mazor, Z., & Kaluski, E. (2012). Minimally in-
Periodontology, 37, 456–465.
vasive subnasal elevation and antral membrane balloon elevation along
 |
670       TEMMERMAN et al.
with bone augmentation and implants placement. The Journal of Oral
Implantology, 38, 365–376.
Khojastehpour, L., Dehbozorgi, M., Tabrizi, R., & Esfandnia, S. (2016).
Evaluating the anatomical location of the posterior superior alveolar ar-
tery in cone beam computed tomography images. International Journal
of Oral and Maxillofacial Surgery, 45, 354–358.
Kim, E.-S., Moon, S.-Y., Kim, S.-G., Park, H.-C., & Oh, J.-S. (2013). Three-­
dimensional volumetric analysis after sinus grafts. Implant Dentistry, 22,
170–174.
Kirmeier, R., Payer, M., Wehrschuetz, M., Jakse, N., Platzer, S., & Lorenzoni,
M. (2008). Evaluation of three-­dimensional changes after sinus floor
augmentation with different grafting materials. Clinical Oral Implants
Research, 19, 366–372.
Maes, F., Collignon, A., Vandermeulen, D., Marchal, G., & Suetens, P. (1997).
Multimodality image registration by maximization of mutual informa-
tion. IEEE Transactions on Medical Imaging, 16, 187–198.
Mazzocco, F., Lops, D., Gobbato, L., Lolato, A., Romeo, E., & del Fabbro,
M. (2014). Three-­dimensional volume change of grafted bone in the
maxillary sinus. The International Journal of Oral & Maxillofacial Implants,
29, 178–184.
Melzack, R. (2005). The McGill pain questionnaire: From description to
measurement. Anesthesiology, 103, 199–202.
Monje, A., Diaz, K. T., Aranda, L., Insua, A., Garcia-Nogales, A., & Wang, H.
L. (2016). Schneiderian membrane thickness and clinical implications
for sinus augmentation: A systematic review and meta-­regression anal-
yses. Journal of Periodontology, 87, 888–899.
Nedir, R., Nurdin, N., Khoury, P., El Hage, M., Abi Najm, S., & Bischof, M.
(2014). Paradigm shift in the management of the atrophic posterior
maxilla. Case Reports in Dentistry, 2014, 486949.
Nedir, R., Nurdin, N., Khoury, P., Perneger, T., Hage, M. E., Bernard, J.-P., &
Bischof, M. (2013). Osteotome sinus floor elevation with and without
grafting material in the severely atrophic maxilla. A 1-­year prospective ran-
domized controlled study. Clinical Oral Implants Research, 24, 1257–1264.
Nkenke, E., & Stelzle, F. (2009). Clinical outcomes of sinus floor augmenta-
tion for implant placement using autogenous bone or bone substitutes:
A systematic review. Clinical Oral Implants Research, 20, 124–133.
Ohe, J.-Y., Kim, G.-T., Lee, J.-W., Al Nawas, B., Jung, J., & Kwon, Y.-D. (2016).
Volume stability of hydroxyapatite and β-­tricalcium phosphate biphasic
bone graft material in maxillary sinus floor elevation: A radiographic
study using 3D cone beam computed tomography. Clinical Oral Implants
Research, 27, 348–353.
Pjetursson, B.E., & Lang, N.P. (2014). Sinus floor elevation utilizing the tran-
salveolar approach. Periodontology 2000, 66, 59–71.
Quirynen, M., Lefever, D., Hellings, P., & Jacobs, R. (2014). Transient swell-
ing of the Schneiderian membrane after transversal sinus augmenta-
tion: A pilot study. Clinical Oral Implants Research, 25, 36–41.
Rao, G. S., & Reddy, S. K. (2014). Antral balloon sinus elevation and grafting
prior to dental implant placement: Review of 34 cases. The International
Journal of Oral & Maxillofacial Implants, 29, 414–418.
Rosen, P. S., Summers, R., Mellado, J. R., Salkin, L. M., Shanaman, R. H.,
Marks, M. H., & Fugazzotto, P. A. (1999). The bone-­added osteotome
sinus floor elevation technique: Multicenter retrospective report
of consecutively treated patients. The International Journal of Oral &
Maxillofacial Implants, 14, 853–858.
Sbordone, C., Toti, P., Guidetti, F., Califano, L., Bufo, P., & Sbordone, L.
(2013). Volume changes of autogenous bone after sinus lifting and
grafting procedures: A 6-­year computerized tomographic follow-­up.
Journal of Cranio-­Maxillo-­Facial Surgery, 41, 235–241.
Sbordone, C., Toti, P., Guidetti, F., Califano, L., Pannone, G., & Sbordone, L.
(2014). Volumetric changes after sinus augmentation using blocks of au-
togenous iliac bone or freeze-­dried allogeneic bone. A non-­randomized
study. Journal of Cranio-­Maxillo-­Facial Surgery, 42, 113–118.
Schwartz-Arad, D., Herzberg, R., & Dolev, E. (2004). The prevalence of sur-
gical complications of the sinus graft procedure and their impact on
implant survival. Journal of Periodontology, 75, 511–516.
Shanbhag, S., Shanbhag, V., & Stavropoulos, A. (2014). Volume changes
of maxillary sinus augmentations over time: A systematic review. The
International Journal of Oral & Maxillofacial Implants, 29, 881–892.
Si, M., Zhuang, L., Gu, Y., Mo, J., Qiao, S., & Lai, H. (2013). Osteotome sinus
floor elevation with or without grafting: A 3-­year randomized con-
trolled clinical trial. Journal of Clinical Periodontology, 40, 396–403.
Summers, R.B. (1994). A new concept in maxillary implant surgery:
The osteotome technique. Compendium (Newtown, Pa.), 15, 152,
154–156.
Szabó, G., Huys, L., Coulthard, P., Maiorana, C., Garagiola, U., Barabás, J.
Németh, Z., … Suba, Z. (2005). A prospective multicenter randomized
clinical trial of autogenous bone versus beta-tricalcium phosphate
graft alone for bilateral sinus elevation: histologic and histomor-
phometric evaluation. Journal of Oral and Maxillofacial Implants, 20,
371–381.
Tadinada, A., Jalali, E., Al-Salman, W., Jambhekar, S., Katechia, B., & Almas,
K. (2016). Prevalence of bony septa, antral pathology, and dimensions
of the maxillary sinus from a sinus augmentation perspective: a retro-
spective cone-­beam computed tomography study. Imaging Science in
Dentistry, 46, 109–115.
Temmerman, A., Hertelé, S., Teughels, W., Dekeyser, C., Jacobs, R., &
Quirynen, M. (2011). Are panoramic images reliable in planning
sinus augmentation procedures? Clinical Oral Implants Research, 22,
189–194.
Timmenga, N. M., Raghoebar, G. M., Liem, R. S. B., van Weissenbruch, R.,
Manson, W. L., & Vissink, A. (2003). Effects of maxillary sinus floor el-
evation surgery on maxillary sinus physiology. European Journal of Oral
Sciences, 111, 189–197.
Traxler, H., Windisch, A., Geyerhofer, U., Surd, R., Solar, P., & Firbas, W.
(1999) Arterial blood supply of the maxillary sinus. Clinical Anatomy
(New York, N.Y.), 12, 417–421.
Troedhan, A., Kurrek, A., & Wainwright, M. (2012). Biological principles
and physiology of bone regeneration under the Schneiderian mem-
brane after sinus lift surgery: A radiological study in 14 patients treated
with the transcrestal hydrodynamic ultrasonic cavitational sinus lift
(Intralift). International Journal of Dentistry, 2012, 576238.
Troedhan, A., Kurrek, A., Wainwright, M., & Jank, S. (2014). Schneiderian
membrane detachment using transcrestal hydrodynamic ultrasonic
cavitational sinus lift: A human cadaver head study and histologic
analysis. Journal of Oral and Maxillofacial Surgery, 72(1503), e1–e10.
Trombelli, L., Franceschetti, G., Stacchi, C., Minenna, L., Riccardi, O., Di
Raimondo, R., … Farina, R. (2014). Minimally invasive transcrestal sinus
floor elevation with deproteinized bovine bone or β-­tricalcium phos-
phate: A multicenter, double-­blind, randomized, controlled clinical trial.
Journal of Clinical Periodontology, 41, 311–319.
Trombelli, L., Minenna, P., Franceschetti, G., Minenna, L., & Farina, R. (2010).
Transcrestal sinus floor elevation with a minimally invasive technique.
Journal of Periodontology, 81, 158–166.
Umanjec-Korac, S., Parsa, A., Darvishan Nikoozad, A., Wismeijer, D., &
Hassan, B. (2016). Accuracy of cone beam computed tomography in
following simulated autogenous graft resorption in maxillary sinus aug-
mentation procedure: An ex vivo study. Dento Maxillo Facial Radiology,
26, 20160092.
Van Dessel, J., Nicolielo, L. F., Huang, Y., Slagmolen, P., Politis, C., Lambrichts,
I., & Jacobs, R. (2016). Quantification of bone quality using different
cone beam computed tomography devices: Accuracy assessment for
edentulous human mandibles. European Journal of Oral Implantology, 9,
411–424.
Vivan, R. R., Mecca, C. E., Biguetti, C. C., Rennó, A. C. M., Okamoto, R.,
Cavenago, B. C., … Matsumoto, M. A. (2016). Experimental maxillary
sinus augmentation using a highly bioactive glass ceramic. Journal of
Materials Science. Materials in Medicine, 27, 41.
Wainwright, M., Torres-Lagares, D., Pérez-Dorao, B., Serrera-Figallo, M.-A.,
Gutierrez-Perez, J.-L., Troedhan, A., & Kurrek, A. (2016). Histological
and histomorphometric study using an ultrasonic crestal sinus grafting
TEMMERMAN et al. |
      671

procedure. A multicenter case study. Medicina Oral, Patología Oral Y evaluation with a minimum follow-­up of 4.5 years. Clinical Oral Implants
Cirugía Bucal, 21, e367–e373. Research, 20, 691–700.
Wallace, S. S., & Froum, S. J. (2003). Effect of maxillary sinus augmenta-
tion on the survival of endosseous dental implants. A systematic review.
Annals of Periodontology, 8, 328–343. S U P P O RT I NG I NFO R M AT I O N
Wang, H.-L., & Katranji, A. (2008). ABC sinus augmentation classification.
The International Journal of Periodontics & Restorative Dentistry, 28, Additional Supporting Information may be found online in the sup-
383–389. porting information tab for this article.
Wanschitz, F., Figl, M., Wagner, A., & Rolf, E. (2006). Measurement of vol-
ume changes after sinus floor augmentation with a phycogenic hy-
droxyapatite. The International Journal of Oral & Maxillofacial Implants,
21, 433–438. How to cite this article: Temmerman A, Van Dessel J,
Zhang, Y., Tangl, S., Huber, C. D., Lin, Y., Qiu, L., & Rausch-Fan, X. (2012).
Cortellini S, Jacobs R, Teughels W, Quirynen M. Volumetric
Effects of Choukroun’s platelet-­rich fibrin on bone regeneration in
combination with deproteinized bovine bone mineral in maxillary sinus changes of grafted volumes and the Schneiderian membrane
augmentation: A histological and histomorphometric study. Journal of after transcrestal and lateral sinus floor elevation procedures:
Cranio-­Maxillo-­Facial Surgery, 40, 321–328. A clinical, pilot study. J Clin Periodontol. 2017;44:660–671.
Zijderveld, S. A., Schulten, E. A. J. M., Aartman, I. H. A., & ten Bruggenkate,
https://doi.org/10.1111/jcpe.12728
C. M. (2009). Long-­ term changes in graft height after maxillary
sinus floor elevation with different grafting materials: Radiographic