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Bone Graft Displacement After Maxillary Sinus Floor Augmentation With or

Without Covering Barrier Membrane: A Retrospective Computed
Tomographic Image Evaluation


Laurent Ohayon, DDS / Silvio Taschieri, MD, DDS2 /
1

Anton Friedmann, DDS, PhD3 /Massimo Del Fabbro, MSc, PhD4

1
Private Practice, Saint-Maur des Fosses, France
2
Professor, Chair and Head Department of Periodontology, School of Dentistry, Faculty of Health,
University of Witten, Witten, Germany
3
Aggregate Professor, Department of Biomedical, Surgical and Dental Sciences, University of Milan,
Milan, Italy; Head of Section of Oral Physiology, IRCCS Galeazzi Institute, Milan, Italy.
4
Associate Professor, Department of Biomedical, Surgical and Dental Sciences, University of Milan,
Milan, Italy; Head of Section of Oral Physiology, IRCCS Galeazzi Institute, Milan, Italy.

The authors report no conflict of interest related to this study.

Correspondence:
Laurent Ohayon, DDS,
25, rue de la Varenne
94100 Saint-Maur des Fosses, France
Phone: +33 1 48852589 Fax: + 33 1 48850968 e-mail: ohayonl@wanadoo.fr

Submitted January 28, 2018; Accepted August 14, 2018.

Abstract:

Purpose: Scientific publications have recently found that bone graft quality and implant
survival rates were not influenced by antrostomy membrane coverage during maxillary
sinus floor augmentation with a lateral approach. The aim of this study was to evaluate

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the stability of the bone substitute after a maxillary sinus floor augmentation procedure
with or without using a covering membrane. Materials and Methods: This
retrospective study evaluated all patients who were enrolled between April 2016 and
January 2017. The stability of the bone graft inside the sinus cavity as well at the level of
the lateral bone window was assessed through preoperative and postoperative cone
beam computed tomography images up to 6-month follow-up. The clinical postoperative
morbidity was evaluated following a visual analog scale (VAS) protocol. Results:
Maxillary sinus floor augmentation with a lateral approach was performed in 41
patients. In 17 cases (10 women/7 men, mean age: 55.4 years), a barrier membrane was
used to cover the lateral bone window (control group), and in 24 cases (13 women/11
men, mean age: 56.2 years), no membrane was used (test group). The bone graft
dislodgement within the buccal mucosa at 6 months postoperative ranged from 0 to
12.2 mm (mean value: 3.8 ± 3.1 [standard deviation] mm) in the test group and from 0
to 2.3 mm (mean value: 0.5 ± 0.4 mm) in the control group. The postoperative pain and
swelling complications were significantly more important for the test group (3.3 ±
1.4/4.3 ± 4.5, respectively) than for the control group (2.1 ± 0.9/2.7 ± 0.9). Conclusion:
On the basis of this preliminary study, it appears that the use of a barrier membrane to
cover the lateral bone window during maxillary sinus floor augmentation surgery with a
lateral approach reduces the postoperative dislodgement of the bone graft throughout
the sinus antrostomy and prevents the bone substitute particles penetrating within the
buccal mucosa, which is related to postoperative morbidity. Int J Oral Maxillofac
Implants 2018. doi: 10.11607/jomi.6940




Introduction:

Maxillary sinus floor augmentation, used to increase residual bone height for implant
placement at the level of the posterior atrophic maxilla, was introduced Tatum1,2 and
published by Boyne and James in 1980 for the first time3. This surgical procedure is
considered as safe and effective when the residual bone height in the posterior maxilla is
insufficient 4,5. Autogenous bone was the gold standard to graft the new space created
between the lifted Schneiderian membrane and sinus floor because of its osteogenic,
osseoconductive, and osseoinductive properties6. However this biomaterial has been

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replaced with allografts, xenografts or alloplastic biomaterials,7-10 because of the

unpredictable resorption of the autogenous bone graft.11,12 Moreover, the necessity of a
second surgical site for bone harvesting leads to higher morbidity associated with
hemorrhagic risks as well as post-operative pain and swelling in the donor region.13
Different protocols have been proposed depending on the residual ridge condition.14-16
The lateral approach is commonly preferred to the transcrestal approach when the
residual ridge is less than 5mm high.17
A barrier membrane has been proposed to protect the bone substitute at the level of the
lateral bone window in order to promote newly formed bone.4, 18-21 The use of a covering
membrane showed positive results in terms of newly formed vital bone and implant
survival.4, 18, 19, 21 Nevertheless, the necessity of using a barrier membrane, in case of
maxillary sinus floor augmentation with a lateral approach, has been questioned by
recent studies, which evaluated the bone graft quality and the implant survival rates.22,23
However, these studies didn’t take into account post-operative morbidity, such as
swelling, pain or bone graft dislodgement throughout the sinus antrostomy towards the
buccal mucosa.
The aim of this retrospective clinical study was to evaluate the behavior of the bone
substitute in terms of mechanical stability inside the sinus cavity, and at the level of the
lateral antrostomy, after maxillary sinus floor augmentation procedure via lateral
approach with and without using barrier membrane.

Materials and Methods:

Patient selection

This report follows the STROBE guidelines for observational studies24. All patients were
treated following the Ethical Principles for Medical Research Involving Human Subjects
described in the Helsinki World Medical Association (WMA) Declaration in 1975, as
revised in 2000, and according to the modifications made up to the 59th WMA General
Assembly of Seoul in 2008. Ethical approval was not required because of the nature of
this retrospective study, which involved patients that had undergone conventional
surgical treatment. The analysis was based on a review of clinical charts and
radiographic documentation from a single private center. All data were extracted by the
treating clinician from the clinic’s standard documentation concerning diagnostic and

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follow-up procedures, and de-identified prior to statistical analysis. The risks and
benefits of the surgical procedure and related follow-up controls were explained to the
patient before they signed an inform consent form for maxillary sinus surgery and cone
beam computed tomography (CBCT) examination.
Patients were selected for sinus augmentation procedure via the lateral approach
according to standard inclusion criteria: subjects in good health condition (ASA-1 or
ASA-2 following the American Society of Anaesthesiologist Classification), able to
understand and sign an informed consent form; subjects aged over 18 years old; non-
smokers (in order to avoid any relationship between smoking and sinus membrane
swelling); patients with 3mm or less residual bone height in the posterior maxilla, as
evaluated by pre-operative CBCT, requiring maxillary sinus floor augmentation surgery
with lateral approach in order to receive implant-supported fixed rehabilitation.
The following criteria excluded patients from the study: systemic medical
contraindications to implant treatment, sinus infection, seasonal allergic rhinitis, acute
or chronic sinusitis, current pregnancy, a history of bisphosphonate treatment, previous
irradiation to the head and neck; patients requiring bilateral sinus augmentation. In case
of peroperative sinus membrane perforation the patient was also excluded because this
damage may imply the use of an additional barrier membrane layer to cover the
damaged Schneiderian membrane, and the placement of this additional material could
interfere with the sinus membrane in terms of postoperative swelling reaction.
All patients who underwent unilateral sinus augmentation with or without using a
covering barrier membrane over the lateral window between April 2016 and January
2017, and for which a complete radiographic documentation existed up to at least 6-
month follow-up (as described in the next paragraph) were eligible for this
retrospective study.
Barrier membranes, initially used to cover the sinus lateral antrostomy, were not used
in the protocol performed in our surgical center, because recent scientific publications
found no significant difference concerning the bone graft quality and the implant
survival rate with or without using a covering membrane at the level of the lateral bone
window.22-23 It was then possible to create two groups for the retrospective study: one
control group for patients who underwent maxillary sinus floor augmentation surgery
using a barrier membrane to cover the lateral bone window, and one test group for
maxillary sinus floor augmentation without covering membrane.

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Surgical protocol
One hour prior to surgery, patients took two tablets of amoxicillin plus clavulanic acid
(875+125 mg each). Immediately before surgery patients rinsed with an antiseptic
mouthwash containing 0.12% chlorhexidine digluconate to reduce surgical field
contamination. All patients were treated under local anesthesia, induced using Articaine
hydrochloride 4% with Epinephrine 1: 100,000 . After crestal and mesial releasing
incision, a full thickness flap was elevated, exposing the lateral wall of the maxillary
sinus, at which level a window was created, using piezosurgery inserts or a large
diameter round bur under a copious sterile saline solution irrigation. The lateral bone
window was infractured, then carefully mobilized and removed, or rotated medially and
superiorly towards the sinus cavity (Fig. 1a). The Schneiderian membrane was gently
elevated using large blunt curettes to become the new sinus cavity floor. The new space
obtained after the sinus membrane elevation was grafted with anorganic bovine bone
(ABB) biomaterial (Cerabone, Straumann Institute) (Fig. 1b). The test group included
patients, in which no covering membrane was used, and the control group included
patients in which a collagen barrier membrane (Collprotect, Straumann Institute) had
been placed to cover the sinus lateral bone window. A tension free flap closure was
performed using a horizontal mattress and interrupted sutures. The patients received
antibiotic coverage of 1 g amoxicillin + clavulanic acid twice daily for 7 days, 1 mg/kg
prednisolone anti-inflammatory medication once daily for 5 days to reduce
postoperative edema, oral rinses of 0.12% chlorhexidine digluconate twice a day for 2
weeks and 1g of paracetamol every 6 hours for oral pain. All the selected patients
underwent a two-stage procedure with delayed implant placement six months after
grafting.

Radiologic assessment
An Orthophos XG3D CBCT (Dentsply Sirona) was always used and an imaging volume
size of 80 mm in length x 80 mm in diameter of the cylinder, for the sinus examination of
maxillae was chosen. The CBCT data were exported in a 50/60 Mo DICOM (Digital
Imaging and Communication in Medicine) format.
The tube voltage was set at 85 kV and the tube current at 7- 8.5 mA for an average of
14.2 s of exposure time. In this situation, the calculated effective absorbed dose of

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radiation during Orthophos XG3D CBCT sinus examination was from 29 to 54 μSv, which
was related to the maxillary patient size.
The recording of anatomical landmarks of the sinus cavity in the three dimensions of
space was performed to allow identical computed tomographic slices to be reproduced
at follow-up controls. One diagnostic pre-operative CBCT (Fig1c, 1d) and three
postoperative CBCT were performed for each patient. The first postsurgical CBCT was
taken for the immediate post–surgery control (Fig 1e, 1F), the second one at 7-day post
surgery (Fig 1g, 1h) to evaluate the sinus membrane swelling and the bone graft
stability, and the third one at 6-month postoperative (Fig 1i, 1j) to analyze the remaining
sinus membrane thickness and to measure the bone graft dislodgement out of the sinus
cavity. The post-operative coronal CBCT images were used to control the bone graft
shape in the sinus cavity and to evaluate the sinus membrane swelling; the post-
operative cross-sectional CBCT images were used to analyze the bone graft
dislodgement outside the sinus cavity within the buccal mucosa. The total estimated
absorbed radiation dose of four Orthophos XG3D CBCT was less than 220 μSv for each
patient of this study, as opposed to the effective dose values from one single multi-slice
computed tomographic (MSCT) scanner for dentomaxillofacial examination, that ranges
from 474 to 1160 μSv25, knowing that the usual maxillary sinus floor augmentation
protocol requires at least two CT scans, the preoperative first one for sinus anatomy
examination,26 and the second one at 6 months post-operative, for sinus bone graft
volume evaluation27. The patient susceptible tissues were shielded by wearing a lead X-ray
apron. The fields of view were limited to the area of interest and the X-rays were used
following the principle of ALARA (as low as reasonably achievable) in order to reduce the
adsorbed radiation dose.28,29 . The Orthophos XG3D CBCT has therefore been chosen for
its low emission of radiation, which gives the opportunity to allow 7-day postoperative
imaging control, with less absorbed radiation dose for the patients than conventional
computerized tomographic (CT) scanner, in order to asses the sinus membrane swelling
relevance in the early postoperative period so as to be able to adapt the postoperative
treatment and to reduce the morbidity. The total adsorbed radiation per patient in this
study was well within the recommended limits knowing that average background
radiation in the United States is 3000 μSv per year.30

Clinical postoperative morbidity evaluation:

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Several comments had been noticed during the 7-day postoperative CBCT examination to
evaluate the pain and swelling reaction after the surgery especially concerning the patient who
underwent the most significative postoperative morbidity. All the patients of the study were
contacted to assess the postoperative complications they underwent; they were asked to
evaluate the pain and tumefaction on a scale from level 1 (low), level 5 (acceptable), to level
10 (high). 31,32 The surgical center, where the retrospective study was performed, regularly
evaluates morbidity during the 7-day post-operative CBCT imaging in case of maxillary sinus
floor augmentation, when the post surgery sinus membrane swelling can be more relevant 33,
and at 14-day post surgery, during the suture removal, for all bone reconstruction protocols in
order to control and improve the surgical techniques.

Statistical analysis
GraphPad Prism version 5.03 (GraphPad Software Inc ) was used for data analysis.
Descriptive statistics was used to resume the demographic and baseline characteristics
of the two groups, based on age, gender and operation side. These variables were
compared using Student’s t-test or Fisher’s exact test, as appropriate. The between-
group comparison regarding graft dislodgement was undertaken using the unpaired
Student’s t-test. Prior to the analysis, the D’Agostino and Pearsons omnibus test of
normality was run to assess if the data distribution followed a normal curve. The
significance level was set at p=0.05.

Results:
Forty-one patients (16 males and 22 females) were included to the study. The test group
(without membrane) was composed of 24 patients (from 37 to 74 years old, mean age
56.2± 10.3 (standard deviation) years); the control group (with covering membrane)
included 17 patients (from 39 to 71 years old, mean age of 56.3± 10.3 years). Details
about the two groups are resumed in Table 1 and 2. Patients’ age and gender
distribution, as well as operation side, was not significantly different between groups
(p=0.81, p=0.24 and p=0.25, respectively). In the test group, the immediate
postoperative CBCT images revealed well-delimited bone graft inside the sinus cavity
without any modification of the sinus membrane thickness (Fig. 2a-d). Postoperative
swelling of the sinus membrane was observed on the coronal and the cross-sectional
CBCT images at day 7 in 100% of the treated sites. The highest part of the bone graft

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appeared to be disorganized and the bone substitute particles moved away by the
pressure of the edema when the postoperative sinus membrane swelling was
pronounced and, in the same way, the bone substitute particles migrated toward the
buccal mucosa though the lateral window (Fig.2e, 2f).
The 6-month postoperative measurement on the CBCT cross-sectional images, along the
horizontal axis from the lateral sinus wall at the level of the lateral bone window
revealed bone graft dislodgement from 0 to 12.2mm with a mean distance of 3.8 ± 3.1
mm for the test group. The scans revealed the healthy conditions of the sinus membrane,
which appeared recovered back to its preoperative state (Fig 2G, 2H). In the control
group, graft dislodgement after 6 months averaged 0.46±0.38 mm. The difference
between both groups was highly significant (p<0.001).
Figures 3A to 3J show a clinical case from the test group. A postoperative edema at 7-day
was present (Fig 3E, 3F) extending over a large part of the sinus cavity. The bone graft
showed severe dislodgement through the lateral bone window towards oral mucosa
measuring in total a 12.2mm displacement on both, CBCT cross-section and axial image.
Some of the bone substitute particles detached from the bone graft and migrated deeply
into the buccal connective tissue (Fig.3G-J).
The results of the postoperative morbidity recordings revealed that the pain and
swelling complaints were significantly greater expressed in the test group (Table1: 3.3±
1.4/4.3± 4.5) than in the control group (Table 2: 2.1± 0.9/2.7± 0.9).
Moreover, the sinus membrane thickness at 7-day postoperative, measured on the CBCT
images of several test group clinical cases, revealed that the more pronounced sinus
membrane swelling reaction was, the longer bone graft dislodgement distances were
displayed by CBCT scans. The length comparison of the bone graft dislodgement at 7-day
and 6-month, from 3.9mm to 5.3mm for the patient n°2 (Fig. 2F & 2H), and from 10.1
mm to 12.2 mm for the patient n°4 (Fig.3F & 3H) showed that this phenomenon
happened at the early step of the newly bone formation and didn’t tend to spread with
time. The membrane thickness on the cross-sectional CBCT images measured 16. 4 mm
for the patient n°2 (Fig. 2F) and from 11.8mm to 19.9mm for the patient n°4 (Fig.3H),
both recorded 4/4 and 7/8 pain/swelling score on the VAS scale, respectively.

The postoperative morbidity, which was evaluated by the patient’ face swelling and oral
pain 7 days after surgery, revealed to be correlated with the bone graft dislodgement

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distance (Table 1). Following the results of the table 1, the bone graft displacement
through the lateral bone window, occurred from one to three missing teeth area sinus
grafting, but was most significant for patient needing large grafting surgery. Moreover,
no bone graft dislodgement was observed on CBCT images when the sinus membrane
swelling was very low, regardless the filling sinus volume size. These data confirmed
that the postoperative membrane swelling could be considered as the main factor
involving the bone graft dislodgement within the buccal mucosa.
The bone graft dislodgement at the level of the sinus antrostomy for the patients of the
control group apparently was reduced despite the sinus membrane swelling significance
(Table 2).
These postoperative complications tended to be reduced in the control group regardless
the sinus membrane reaction. In a few cases, migration of the bone substitute particles
along the buccal side of lateral sinus wall under the barrier membrane was observed in
all directions. Conversely, in the control group no fraction of the bone substitute
appeared separated from the graft or migrated within the connective tissue of the cheek
(Fig.4A-J).

Discussion:

Traditionally, sinus floor elevation procedure was performed using extraoral

autogenous bone harvested from the iliac crest. Given the high morbidity of such
harvesting procedure, other autogenous regions were adopted, both extraoral such as
calvarial bone, and intraoral (e.g. from the chin or the mandibular ramus). In order to
further reduce morbidity by avoiding or minimizing autogenous bone harvesting,
various types of bone substitutes have been adopted to fill the space created between
the elevated Schneiderian membrane and the sinus walls. Most bone substitutes used in
sinus augmentation procedures allowed to achieve excellent results in terms of clinical
and histomorphometric outcomes, as testified by a number of systematic reviews and
meta-analyses.4, 5,10,34 In order to protect graft healing, jeopardizing the cell competition
first described for periodontal regeneration by Melcher in 197635, barrier membrane
have been used at the level of the lateral antrostomy. The advent of guided bone
regeneration (GBR) techniques increased the popularity of barrier membranes, used to
prevent soft tissue ingrowth within the bone substitute particles during the wound

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healing period. 36 The bone substitute function is to act a space maintainer and to
provide a biocompatible and osteoconductive scaffold for new bone formation. The
surgical trauma caused by elevating of the Schneiderian membrane allows for blood
inflow from the sinus wall to colonize the bone substitute particles and to carry
mesenchymal stem cells from bone marrow. These cells are known to be induced by
growth and differentiation factors to differentiate into osteoprogenitor cells and provide
the space with the osteoblasts necessary to produce new bone.37 The blood clot formed
within the bone substitute needs at the first stage of the wound healing stability to
release bone regeneration.38-40
The sinus cavity is considered to offer a favorable anatomical environment for
integration of bone substitutes due to the origin of maxillary bone being part of the facial
skeleton and regularly presenting therefore with superior vascularization. The
mechanical stability of the grafting materials is given by numerous bone walls
surrounding the sinus cavity in general, however, the localization of the lateral window
at the bottom of the facial sinus wall together with a slight increase in physiological air
pressure normally associated with respiration tend to exfoliate the graft throughout this
window.41
Prevention of soft tissue ingrowth into the particulated bone substitute is crucial in
order to avoid any risk of fibrous encapsulation of the particles. The membrane must
represent selective permeability properties such as favoring bone cell proliferation in
front of connective tissue cell proliferation and favoring also tissue integration in order
to preserve blood vessel ingrowth within the membrane.
According to several scientific publications, the use of a barrier membrane tends to
increase formation of vital bone and also implant survival rates, if accounting for sinus
elevation procedures.19-21, 42 Several systematic reviews confirmed these
observations.4,5,34
On the contrary, some recent studies reported contradicting results showing non-
significant differences as for the newly formed bone area as for the implant survival
rates with or without a barrier membrane cover of the sinus lateral antrostomy . The
data with the barrier membrane showed a trend towards increased numbers than
without any membrane: 19% versus 16% for newly formed bone area and 96.1% versus
94.2% for implants survival rate in the study by Torres García-Denche et al. (2013),23
and 30.7% versus 28.1% for newly formed bone rate in the study by Barone et al.

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(2013).43 One limitation of these studies was the non-addressing the post operative
morbidity as well as the bone graft dislodgement throughout the sinus antrostomy into
the buccal mucosa. This important complication, which may occur during the bone graft
healing period, should be considered a factor in suggesting the use of a barrier
membrane.
The recent development of cone beam computed tomography (CBCT) allows for
accurate and reproducible analysis of the amount of mineralized tissues at a low
radiation level for the patient in 3D.44,45 The image quality also helps to appreciate the
sinus anatomy30,46 and to adequately follow the postoperative biological reactions of the
tissues as well as the fate of sinus bone graft47 along the healing period after sinus floor
augmentation procedure. The CBCT images were recently used to evaluate the effect of
sinus floor augmentation surgery on sinus membrane thickness during both, the early
and the late healing period. The authors detected an increased membrane thickness due
to the post-operative swelling reaction with a peak value at 7 days after surgery
followed by complete resolution after 6 months.33 The per-operative endoscopic
observation of the sinus membrane revealed a temporary interruption of its mucociliary
activity in the area of elevated membrane,48 although after 9 post-operative months
both, the physiological sinus mucosa structure and regular ciliary function appeared
non-affected.49
Nevertheless, in the present study the post-operative swelling of the Schneiderian membrane
contributed to an increased pressure within the sinus cavity and acting together with the
physiologically positive air pressure at the bone graft displaced it towards and even through
the lateral bone window if the sinus antrostomy remained non-covered by a membrane.
Furthermore, the postoperative graft dislodgement revealed to be associated with the sinus
membrane swelling and will probably be enhanced by any factor which action increases intra
sinus air pressure, such as nose blowing, sneezing, or hemorrhagic reaction

From the data of the present study, the increase of the sinus antrostomy size as well as the
sinus graft volume, which depend on the number of the missing teeth, could be considered as
an aggravating factor, while sinus membrane swelling revealed to be a triggering factor for
bone graft dislodgement. . Moreover, the bone graft displacement revealed to have no
influence on the implant placement in second step surgery.

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Maxillary sinus is a confined structure surrounded by bone walls, 50 for which acute maxillary
sinusitis doesn’t cause facial swelling.51 The results of the retrospective study therefore
suggest that facial tumefaction and pain can be related to the sinus antrostomy creation, which
may cause transient postoperative sinus membrane swelling and hemorrhage to spread
throughout the lateral sinus bone window within the buccal mucosa. The bone graft
dislodgement is thereby a consequence of the sinus membrane swelling and hemorrhage
pressure, which tend to displace the bone substitute outside the sinus cavity.
A significant reduction of the postoperative morbidity was observed at 7 days post-surgery for
the membrane covered group compared to the non-covered test group, in which the oral pain
and cheek tumefaction were correlated with the bone graft dislodgement into the buccal
mucosa. The early postoperative schneiderian membrane swelling33 and morbidity52 after
maxillary sinus augmentation surgery have rarely previously been evaluated, although a
low morbidity has been observed when a barrier membrane was used to cover the
lateral bone window53, which tends to confirm the data of this study.
The relevant biomechanical function of a barrier membrane placement at the level of the sinus
trapdoor, may be hypothesized, as this membrane may reduce the bone graft dislodgement
throughout the sinus bone window, possibly caused by the postoperative schneiderian
membrane swelling.

Conclusion:
After maxillary sinus floor augmentation procedure with lateral approach, if no barrier
membrane was used to cover the lateral bone window, the bone graft stability was
unpredictable for the early healing period. Within the limits of this study, the use of a
barrier membrane was helpful in preventing dislodgement of the bone substitute
particles throughout the sinus antrostomy into the buccal mucosa reducing thereby the
postoperative morbidity.

References:
1. Tatum OH. Maxillary sinus grafting for endosseous implants. Presented at the Annual
Meeting of the Alabama Implant Study Group. Birmingham, Alabama, April 1977.

12
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No part may be reproduced or transmitted in any form without written permission from the publisher.
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2. Tatum, H. Jr. Maxillary and sinus implant reconstructions. Dental Clinics of North
America 1986 ; 30: 207–229.

3. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow
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12. Le Lorc'h-Bukiet I, Tulasne JF, Llorens A, Lesclous P. Parietal bone as graft material
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Table 1: Test group (without using covering membrane): bone graft dislodgement at the
level of the sinus lateral bone window at 6-month post-operative

Patient n° Gender Age (Y) Side *Missing teeth Bone graft Pain/Swelling
location dislodgement
(mm)
1 F 54 R 14 15 0.0 2/1
2 M 58 L 3 5.3 4/4

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3 F 52 L 234 7.8 6/7

4 M 42 L 23 12.2 7/8
5 F 57 L 3 2.7 2/3
6 F 71 R 14 15 5.1 3/6
7 M 76 R 14 15 2.3 3/5
8 F 67 L 234 3.7 3/6
9 F 49 R 14 15 5.9 4/5
10 F 45 R 14 1.5 3/3
11 M 58 L 23 1.7 3/2
12 F 54 R 14 0.2 1/2
13 M 47 R 14 0.0 2/1
14 F 54 L 3 0.7 1/1
15 F 45 R 14 15 5.9 4/5
16 F 74 L 234 4.1 3/5
17 M 58 L 23 8.2 4/6
18 M 71 L 3 0.5 2/1
19 F 58 L 234 5.7 4/7
20 M 45 R 14 15 1.6 3/5
21 M 63 L 23 3.7 3/3
22 M 59 R 13 14 15 8.3 5/7
23 F 37 L 3 2.3 3/4
24 M 55 L 23 2.7 4/6
Mean ± SD 56.2 ± 10.3 3.8 ± 3.1 3.3 ± 1.4/4.3 ± 4.5

SD: standard deviation
* : American Dental Association Teeth Numbering

Table 2: Control group (using covering membrane): bone graft dislodgement at the level
of the sinus lateral bone window at 6-month post-operative

Patient n° Gender Age (Y) Side *Missing Bone graft Pain/Swelling

teeth location dislodgement
(mm)
1 F 58 L 23 0.7 2/2
2 M 43 L 234 1.2 2/4
3 M 39 L 3 0.0 1/2
4 F 62 R 14 15 0.4 2/2
5 F 47 L 23 0.7 3/4
6 M 68 L 3 0.5 3/3

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7 F 71 R 14 0.0 2/2
8 F 57 R 13 14 15 1.1 1/3
9 M 65 R 14 15 0.4 2/4
10 F 45 L 3 0.3 3/2
11 F 67 L 234 0.5 4/4
12 M 53 R 14 15 0.0 2/2
13 F 47 R 14 0.3 1/3
14 M 67 L 23 0.7 3/2
15 M 51 L 234 0.2 3/3
16 F 53 L 3 0.0 2/1
17 F 49 R 14 15 0.9 1/3
Mean ± SD 55.4 ± 9.9 0.5 ± 0.4 2.1± 0.9/2.7± 0.9

SD: standard deviation

*American Dental Association Teeth Numbering

Figures:

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Figure 1. Test group clinical case
A) The sinus lateral bone window was prepared and removed; B) The anorganic bovine
bone was gently condensed into the new space obtained between the elevated sinus

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membrane and the sinus floor; C) Preoperative CBCT Coronal view; D) Preoperative
CBCT Cross-sectional view; E) Immediate post-operative CBCT Coronal view; F)
Immediate post-operative CBCT Cross-sectional view: the bone graft contours are well
delimited inside the sinus cavity; G) 7-day post-operative CBCT Coronal view; H) 7-day
post-operative CBCT Cross-sectional view: the sinus membrane thickness is slightly
more important than the preoperative one, showing a low membrane swelling
postoperative reaction. The bone graft contours remained well delimited and did not
exceed the limit of the lateral bone window; I) 6- month post-operative CBCT Coronal
view; J) 6- month post-operative CBCT Cross-sectional view: the newly formed bone had
a compact and dense appearance and showed a clear limit at the level of the lateral bone
wall. The sinus contours didn’t change. The swelling of the sinus membrane disappeared
on the top of the bone graft.

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Figure 2. Test group clinical case with small postoperative bone graft displacement
A) Preoperative CBCT Coronal view; B) Preoperative CBCT Cross-sectional view: the
sinus membrane is healthy and not identifiable. C) Immediate post-operative CBCT
Coronal view; D) Immediate post-operative CBCT Cross-sectional view: the bone graft
contours are well delimited; E) 7-day post-operative CBCT Coronal view; F) 7-day post-

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operative CBCT Cross-sectional view: The sinus membrane edema, measured at

16.4mm, was significant and pushed away the biomaterial particles, which moved away
at the level of the upper area of the bone graft and migrated thought the lateral bone
window within the buccal mucosa. The bone graft dislodgement length was 3.9mm
G) 6- month post-operative CBCT Coronal view; H) 6- month post-operative CBCT
Cross-sectional view: The upper part the bone graft still had a disorganized aspect
(white arrow), showing a jeopardized newly bone formation in this area, due to the
postoperative swelling or hematoma of the sinus membrane. The bone graft
dislodgement length was 5.3mm

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Figure 3. Test group clinical case with significant postoperative bone graft displacement
A) Preoperative CBCT Coronal view; B) Preoperative CBCT Cross-sectional view; the
preoperative thickness of the membrane was clearly identifiable; C) Immediate post-
operative CBCT Coronal view; D) Immediate post-operative CBCT Cross-sectional view:
the bone substitute particles showed well-delimited contours. E) 7-day post-operative
CBCT Coronal view; F) 7-day post-operative CBCT Cross-sectional view. The
postoperative sinus membrane swelling occupied a large part of the sinus cavity and
was measured along its vertical axis from 11.8mm to 19.9mm. The bone substitute
particles migrated thought the lateral window and was measured at 10.1mm along its
horizontal axis. Isolated biomaterial agglomerate was localized into the connective
tissue. G) 6- month post -operative CBCT Coronal view; H) 6- month post -operative
CBCT Cross-sectional view; I) 6- month post -operative CBCT Axial view; J) 6- month
post -operative 3D CBCT image. The bone graft dislodgement was significant and the
measurement of its length was 12.2mm. The bone substitute particles, which detached
from the bone graft, deeply migrated into the buccal connective tissue (white arrow)

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Figure 4. Control group clinical case
A) Preoperative CBCT Coronal view; B) Preoperative CBCT Cross-sectional view;
C) The space between the elevated sinus membrane and the alveolar ridge was filled
with bone substitute; D) the barrier membrane was placed over the lateral bone window
to cover the biomaterial. E) Immediate post-operative CBCT Coronal view; F) Immediate
post-operative CBCT Cross-sectional view: The biomaterial showed a dense and
homogenous aspect; G) 7-day post-operative CBCT Coronal view; H) 7-day post-
operative CBCT Cross-sectional view: The postoperative swelling of the sinus membrane
caused radiolucency areas into the biomaterial. I) 6- month post -operative CBCT
Coronal view; J) 6- month post -operative CBCT Cross-sectional view. The radiolucency
areas still identifiable inside the bone graft, showing a poor mineralized bone quality at
this level. The bone substitute particles all remained inside the sinus cavity

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