Accepted Article

DR. RAMZI V. ABOU-ARRAJ (Orcid ID : 0000-0003-3552-6603)

Article type : Original Research

The impact of anatomic, patient and surgical factors on membrane perforation during
lateral wall sinus floor elevation.

Running Title: Influencing factors for sinus membrane perforation

Authors:
Andrea Pizzini, DDS, MS1
Hussein S. Basma, DDS, MS1
Peng Li, PhD2
Nicolaas C. Geurs, DDS, MS1
Ramzi V. Abou-Arraj, DDS, MS1

Affiliations:
1 Department of Periodontology, School of Dentistry, University of Alabama at Birmingham,
Birmingham, Alabama, USA
2 Department of Acute, Chronic and Continuing Care, School of Nursing, University of Alabama at
Birmingham, Birmingham, Alabama, USA

Corresponding author:
Dr. Ramzi V. Abou-Arraj
University of Alabama at Birmingham
SDB 412
1919 7th Avenue South

This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1111/CLR.13698
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 Birmingham, AL 35294-0007, USA
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(205) 934-4506
(205) 934-7901 (fax)
rva@uab.edu

Running Title: Factors affecting sinus membrane perforation

Acknowledgements:
Research reported in this paper was partially supported by the National Center for Advancing
Translational Sciences of the National Institutes of Health under award number UL1TR003096. The
content is solely the responsibility of the authors and does not necessarily represent the official views
of the National Institutes of Health.

Author Contributions:
A. Pizzini, contributed to conceptualization, data curation, investigation and writing-review and
editing; H. Basma, contributed to validation and writing-review and editing; P. Li, contributed to
formal analysis and writing-review and editing; NC Geurs, contributed to writing-review and editing,;
RV. Abou-Arraj, contributed to conceptualization, data curation, methodology, supervision, writing-
original draft.

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 ABSTRACT
Accepted Article
Objectives: This retrospective study aimed to evaluate the influence of anatomical, patient and
surgical factors on the occurrence of membrane perforation (MP) during lateral window sinus floor
elevation (LWSFE).

Material and Methods: A review of LWSFE patient records between 2014 and 2019 accounted for
MP occurrence, window surface area (WSA), intravenous sedation use, osteotomy instrument type,
and clinician experience. Preoperative cone-beam computed tomography (CBCT) scans were
analyzed for lateral wall thickness (LWT), LFM and LAM angles formed between lateral and medial
walls at the floor and anterior wall respectively, sinus width at 5-, 10- and 15-mm (LM-5, LM-10 and
LM-15) from the floor, residual bone height (RBH), sinus pathologies, septa and arterial
anastomoses. The generalized estimating equations (GEE) approach with a sandwich variance-
covariance estimator was used to evaluate the associations with MP.

Results: MP occurred in 25.74% of 202 LWSFE procedures (166 patients). Mean 1.6mm-LWT,
3.2mm-RBH, 95°-LFM, 75.5°-LAM, 12mm-LM-5, 20.79% septa, 16.83% arterial anastomosis,
37.62% sinus pathology and 29.21% intravenous sedations, 85.24% WSA ≥40mm2 and 57% >10
procedures/clinician were reported. Greater MP rates were encountered as follows: 38.3%
(LWT≥1.5mm), 38% (LFM<90°), 59.6% (LAM<70°), 45.4% (LM-5<10mm), and 36.4% (WSA ranged
>80mm2), with statistically significant associations with all these outcomes (P<.05). The presence of
pathologies was also associated with MP (P=.013). Associations between MP and the presence of
septa and arterial anastomoses, age/gender, right/left sinus, RBH, clinician’s experience, instrument
type and intravenous sedation use could not be demonstrated.

Conclusions: MP is significantly associated with thicker lateral walls, narrower sinuses, larger
windows and existing sinus pathology.

MeSH Terms: Maxillary sinus, Sinus floor augmentation, Schneiderian membrane (nasal mucosa)

Word Count: 4,854 (including in-text citations)

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 INTRODUCTION
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Sinus floor elevation procedures are commonly performed to create sufficient bone height for the
placement of dental implants following tooth loss in the posterior maxilla (Nunes, Bornstein, Sendi, &
Buser, 2013). Two main augmentation procedures have been described, lateral window sinus floor
elevation (LWSFE) and transcrestal sinus augmentation (Pjetursson, Tan, Zwahlen, & Lang, 2008).
LWSFE is the preferred method to achieve significant bone height increase when ≤5mm of native
alveolar bone height is present (Boyne & James, 1980).

LWSFE is not immune to intraoperative and postoperative complications (Pikos, 1999; Schwarz et
al., 2015). Membrane perforation (MP) is the most common intraoperative complication associated
with maxillary sinus augmentation (Lundgren et al., 2017). MPs occur in 10% to 40% of the time
during elevation procedures (Jensen, Shulman, Block, & Iacono, 1998; Shiffler, Lee, Aghaloo, Moy,
& Pi-Anfruns, 2015; Wallace & Froum, 2003). The membrane may be lacerated during the
preparation of the lateral window or perforated during membrane elevation. The instrument selection
for the lateral wall osteotomy preparation has not been found to substantially affect the risk for MP
(Barone et al., 2008). Excessive manual pressure is considered a risk for those perforations
(Weingart, Bublitz, Petrin, Kalber, & Ingimarsson, 2005). MP creates a communication with the sinus
and permits the introduction of foreign graft material into the sinus, thus placing the patient at risk for
postoperative sinusitis and infection spreading throughout paranasal sinuses (Pommer, Dvorak, et
al., 2012). Techniques to repair a perforation of the Schneiderian membrane have been described;
therefore, this complication does not always result in aborting LWSFE procedures (Nolan, Freeman,
& Kraut, 2014; Tukel & Tatli, 2018). Reported survival rates of the implants under functional loading
when placed into grafted sinus varied from 36% to 61.7%, even reaching 100% in recent meta-
analyses (Del Fabbro, Rosano, & Taschieri, 2008; Esposito et al., 2010).

Complex sinus morphology and decreased membrane thickness increases the risk of perforation
rates. MP was shown to occur with a mean membrane thickness of 0.84mm in comparison to a
mean of 2.65mm in non-perforated membranes (Lum, Ogata, Pagni, & Hur, 2017). In addition, a
mean residual alveolar ridge height of 2.78mm was found when MP occurred in contrast to 4.21mm
in the non-perforated group (Lum et al., 2017). Moreover, the extent of bone atrophy and the
presence or direction of sinus septa (20 to 30% of the time) in the posterior maxilla increase the risk

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 of MP (Pommer, Dvorak, et al., 2012; Ulm, Solar, Krennmair, Matejka, & Watzek, 1995). A recent
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study has considered that a high risk for membrane perforation exists when the membrane thickness
was <0.8mm or >3mm and residual bone height <4mm (Testori, Yu, Tavelli, & Wang, 2020).

Lateral wall thickness (LWT) has also been evaluated and averaged 1.31mm in partially dentate
patients and 0.95mm in edentulous patients. Maximum LWT was found in the first molar area and
the minimum values were at the second premolar and second molar (Kiakojori, Nasab, Abesi, &
Gholinia, 2017). In another study, LWT tended to increase from second premolar to second molar
and from 5mm up to 15mm (Monje et al., 2014). Considering that access to the Schneiderian
membrane is obtained through the lateral wall, limited information exists regarding the significance of
the relationship between LWT and MP.

The angle formed between the lateral and the medial walls with respect to the floor of the sinus
(LFM) has received some attention in previous studies. In a cross-sectional study, the mean value of
this angle was 73° (Lozano-Carrascal et al., 2017). It has been suggested that perforations occur in
37.5% of the time when the angle formed by the intersection of two bony walls relating to the inverted
pyramid-shaped maxillary sinus is less than 60° (Cho, Wallace, Froum, & Tarnow, 2001). Due to the
irregular shape of the medial wall, this risk assessment method is not always applicable as using the
intersection of the two bony walls will inaccurately offset the center of the angle apically to the floor of
the sinus, and therefore misrepresent the true angle at the floor of the sinus. In addition, the angle
formed between the lateral and medial walls with respect to the anterior wall of the sinus (LAM) has
not been evaluated in previous studies. LAM represents an area of particular importance where
membrane elevation is frequently required for proper graft placement in the most anterior aspect of
the sinus during LWSFE procedures. Furthermore, both LFM and LAM angles relate to the medio-
lateral width of the sinus cavity. Narrower distances between the lateral and medial walls of the sinus
have been previously measured by tracing the angle between the walls (Cho et al., 2001) and
considered to increase the difficulty score of LWSFE (Testori, Tavelli, et al., 2020).

Overall, the influence of the above-mentioned anatomical factors on the rate of Schneiderian MP in
LWSFE procedures has not been clearly investigated. Therefore, the aims of this retrospective study
were to: 1) evaluate reported MP occurrence in LWSFE, 2) assess mean values for maxillary sinus

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 anatomic landmarks, and 3) investigate associations between anatomical, surgical and patient
Accepted Article
factors and MP occurrence.

MATERIAL AND METHODS

This study was based upon de-identified clinical and radiographic records of LWSFE procedures
performed between 2014 and 2019 at the University of Alabama at Birmingham (UAB) School of
Dentistry. This retrospective study protocol was approved by the UAB Institutional Review board
Number IRB300003091 in compliance with the U.S. Department of Health & Human Services
Federalwide Assurance. The Strengthening the Reporting of OBservational studies in Epidemiology
(STROBE) guidelines were followed for accurate reporting (von Elm et al., 2014).

Inclusion criteria were as follows: (1) patients treated in the Graduate Periodontology Clinic; (2)
diagnostic preoperative cone beam computed tomography (CBCT) scan; (3) unilateral or bilateral
LWSFE; and (4) accessible and well-documented sinus augmentation progress notes. Exclusion
criteria included (1) lack of preoperative CBCT; (2) low-quality or non-diagnostic CBCT; and (3)
poorly documented treatment progress notes in relation to intra- and post-operative complications.

The patients’ paper or electronic records were screened for MP occurrence, window dimensions,
osteotomy instrument, and use of intravenous sedation. Maxillary sinus anatomical evaluations were
performed by the same trained operator (AP). All included CBCT scans were captured with the same
scanner (i-CAT FLX, Henry Schein, Melville, NY) with a voxel size of 0.3 mm in a 16x11 cm field of
view (FOV). Operating parameters were set at 5mAs, 120 kVp for 8.9s scan time and 3.7s exposure
time. The DICOM files of each scan were imported into a digital planning software (Simplant,
Dentsply Sirona, York, PA) and subjected to computerized analyses for the evaluation of anatomic
data. Intra-operator calibration was accepted if the difference in measurements was <0.2mm at least
90% of the time. Two measurements were made, and the mean value was calculated for the study. A
third measurement was conducted when the difference exceeded 0.2mm.

The following anatomical variables were evaluated for descriptive and analytical data:

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 1) Lateral wall thickness (LWT) measured in mm at 5mm from the most apical point on the sinus
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floor, corresponding to the center of the planned window (Fig.1). Direct lines were traced on the
planning software from the outer aspect to the inner aspect of the lateral wall after identifying the
most apical point of the sinus floor (point F) on a coronal CBCT section, point F5 at an apical
distance of 5mm from point F in a linear vertical direction and a perpendicular line to F-F5 thus
connecting point F5 to both lateral (point L) and medial (point M) walls.

2) LFM angle measured in degrees, formed between the lateral and medial walls at 5mm from the
most apical point on the sinus floor according to the following methodology on a coronal CBCT
section (Fig.2): after identifying points F, F5, L and M, two lines were traced to connect points F
and L on the lateral wall and points F and M on the medial wall. The resulting angle at point F
(LFM) was subsequently measured. The rationale for considering 5mm to determine LFM is that
the inferior border of the window typically does not extend more than 5mm with respect to the
sinus floor. In addition, LFM angle constitutes a more accurate representation of the anatomy of
the sinus floor than previously reported lateral-medial wall angles (Cho et al., 2001).

3) Distance between the medial and the lateral walls measured in mm at 5mm (LM-5), 10mm (LM-
10) and 15mm (LM-15) from the floor following the same methodology to identify LWT with the
addition of two lines at 10mm and 15mm apical to point F for a transverse measurement of the
sinus width at 3 different levels on a coronal CBCT section (Fig.3).

4) LAM angle measured in degrees, formed between the lateral and the medial walls in relation to
the anterior wall of the sinus following a methodology similar to that of LFM with some differences
(Figs. 4a,b): Point A was identified after tracing point F8 at 8mm apical to point F and connecting
a perpendicular line from F8 to the anterior wall on a sagittal CBCT section. Point A8 was then
determined on an axial section at 8mm posterior to point A as the window preparation extends at
least 8mm distal of the most anterior wall. Then, a perpendicular line was traced connecting point
A8 to both lateral (point L) and medial (point M) walls. The resulting angle created between AL
and AM was LAM. The rationale for considering 8mm to determine LAM was that the elevation of
the sinus membrane generally extends at least 8mm with respect to the sinus floor as the
reported average bone gain after LWSFE is 7.5-8.5mm (Pal et al., 2012; Starch-Jensen &
Jensen, 2017).

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Accepted Article
5) Residual bone height (RBH) measured in mm from the floor of the sinus to the alveolar ridge on a
coronal CBCT section by extending a line on the planning software from the sinus floor to the
crest of the ridge at the potential implant site (Fig.5). When the ridge height was uneven, RBH
was measured at the shortest distance.

6) Presence of sinus septa was evaluated on sagittal CBCT sections as a dichotomous outcome.

7) Presence of arterial anastomosis between posterior superior alveolar artery (PSAA) and
infraorbital artery (IOA) and location in the lateral wall on sagittal CBCT sections as a
dichotomous outcome.

LWT, LM-5, LM-10, LM-15 and RBH were evaluated within a 6-mm range, antero-posteriorly
around the proposed implant site identified by a radiographic surgical stent. It is noteworthy that the
lack of standard cutoffs for most of the anatomical sinus variables investigated in this study
prevented a preset categorization of the ranges for LWT, LFM, LAM and LM-5. Therefore, the ranges
and cutoffs were selected based on the distribution of the findings to make the observations in each
category more balanced. An effort was made to have no more than 3 categories per variable for
consistency purposes and to minimize the number of reported groups for each anatomical variable.
In addition, the statistician was blinded to the selection of those cutoffs which protected the
objectivity of the results.

The following patient and surgical parameters were collected for analyses and their influence on MP
was investigated:
a. Number of sinus augmentation procedures performed by residents. Based on the number of
procedures performed by clinicians included in the study, residents were divided into 4 categories
depending on the number of procedures performed: A (≤5), B (6-10), C (11-15) and D (>15) rather
than using their year of training.
b. Number of LWSFE procedures performed under intravenous sedation
c. Instrument (round bur, piezoelectric tip, reamer) used to perform the osteotomy
d. Presence of sinus pathology including membrane thickening, mucous retention cysts and chronic
sinusitis

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 e. Window dimensions or window surface area (WSA). A classification of WSA was created as
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follows: small (<40mm2), medium (40-80mm2) and large (>80mm2) based on the average surface
area prepration using the various instruments in our clinic protocol (mean of 30mm2 for reamer kit,
mean of 80mm2 for piezoelectric tip and round bur)

Statistical Analysis:
Descriptive statistics were used to summarize patient characteristics and clinical variables (mean
and standard deviation (SD) for continuous variables; frequency and percentage for categorical
variables). The generalized estimating equations (GEE) approach with a sandwich variance-
covariance estimator was used to evaluate the associations between the primary outcome
(membrane perforation) and the clinical variables, while accounting for correlated observations due
to multiple measurements taken from the same patients. The crude odds ratio (OR) and its 95%
confidence interval (95%CI) were reported for strength of the association in the bivariate GEE
analysis. The adjusted OR and 95%CI were obtained in the GEE analysis controlling for age, sex,
pathology status, right/left side, number of procedures and IV sedation. All analyses were conducted
using SAS 9.4 software (SAS Institute, Cary NC). A p-value < 0.05 was considered statistically
significant in two-tailed statistical tests.

RESULTS

Study sample:
A total of 202 LWSFE records from 166 patients (61.45% males, 38.55% females, mean age 64.4 ±
9.8 years old) were included after excluding 34 LWSFE for lack of appropriate radiographic or
treatment records. The left maxillary sinus and right maxillary sinus accounted for 103 (51%) and 99
(49%) LWSFE procedures respectively.
All LWSFE procedures were completed except for one case in which the procedure was aborted due
to an exceedingly large MP that was not repaired. A follow-up LWSFE procedure was successfully
perfomed after 4 months of healing. All other MPs were repaired with the use of resorbable
membranes.
One case required additional grafting at time of implant placement using a vertical sinus floor
elevation technique. MP was registered at this site during the initial LWSFE.

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 Implant placement was performed in 87.13% (176/202) of LWSFE sites. The remaining sites have
Accepted Article
not received implants either because the healing time was incomplete at the time of the data
collection (20 sites) or because the patients decided to postpone implant placement for financial
reasons (6 sites).

Descriptive findings:
Overall MP rate was 25.74% (52/202). Mean LWT of 1.6 ± 0.6 mm, RBH of 3.2 ± 1.5 mm, LFM angle
of 95.5 ± 10.1°, and LAM angle of 75.5 ± 11.0° were noted. The mean distances between the lateral
wall and the medial wall were as follows: LM-5 was 12.0 ± 2.0mm, LM-10 was 15.4 ± 3.1 mm and
LM-15 was 16.4 ± 4.6mm. Almost one third (29.21%) of LWSFE procedures were performed under
intravenous sedation.
Sinus septa were identified in 20.79% (42/202) of the sinuses. The PSAA/IOA intraosseous
anastomosis was detectable in 34 sinuses (16.83%). The average distance from the crest was
14.6mm ranged from 8.02 to 24.5mm. One hundred and twenty-six sinuses (62.38%) were clear of
pathology whereas 26.24% (53/202) of sinuses showed evidence of membrane thickening, 5.94%
(12/202) had mucous retention cysts, and 4.95% (10/202) were associated with chronic sinusitis. The
clinicians’ distribution in relation to the number of procedures was as follows: A (8%), B (35%), C
(36%) and D (21%) of total procedures. Of the 202 included LWSFE procedures, the dimensions of
the window (WSA) were reported in 183 procedures. WSA distribution was as follows: small
(14.75%), medium (61.2%) and large (24.04%) (Table 1).

Associations of outcomes with MP (Tables 1 and 2, Fig. 6):

1) LWT:
The likelihood of MP occurrence was lowest when LWT<1.5mm (14%) whereas LWT of 1.5-2mm
and >2mm displayed a significantly greater prevalence of 39.3% and 34.1% respectively. The GEE
analysis suggested that the likelihood of MP in both LWT>2mm and LWT 1.5-2mm was significantly
higher than LWT<1.5mm (OR=3.19, 95%CI [1.30, 7.80]; P=.013 and OR=4.0, 95%CI [1.71, 9.38];
P=.002, respectively). After controlling for age, sex, pathology status, right/left side, number of
procedures and IV sedation, the likelihood of MP in both LWT>2mm and LWT 1.5-2mm was still

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 significantly higher than LWT<1.5mm (the adjusted OR= 4.32, 95%CI [1.62, 11.50]; P=.005 and
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adjusted OR= 4.94, 95%CI [1.84, 13.33]; P=.003, respectively).

2) LFM angle:
Three LFM groups were distributed as follows: <90° (29%), 90-100° (35%) and >100° (36%). When
LFM angle was <90° degrees, MP rate was the highest at 38%, almost twice as frequently as
sinuses with LFM >90° (P=.043). The likelihood of MP in LFM<90° was significantly higher than both
LFM 90-100° and >100° (OR=2.30, 95%CI [1.05, 5.03]; P=.038 and OR=2.36, 95%CI [1.03, 5.45];
P=.044, respectively). After controlling for age, sex, pathology status, right/left side, number of
procedures and IV sedation, the trends were similar but not statistically significant (the adjusted OR=
1.95, 95%CI [0.83, 4.59]; P=.122 and adjusted OR= 2.05, 95%CI [0.87, 4.83]; P=.098, respectively).

3) LAM angle:
When MPs occurred, the average LAM angle was 68.2 ± 11.1° compared to 78.3 ± 9.8° in the
absence of MP (P=.0001). The significantly greater likelihood of MP in LAM<70° was demonstrated
in GEE analysis where the OR was 7.61 [3.10, 18.66] vs. LAM 70-80° (P<.001) and 14.30 [5.12,
39.88] vs. LAM>80°(P<.001). After controlling for age, sex, pathology status, right/left side, number
of procedures and IV sedation, the results were similar, with the adjusted ORs of 7.59 [3.22, 17.88]
(P<.001) and 13.53 [4.51, 40.60] (P<.001), respectively).

4) LM-5 distance:
The average sinus width was 11.4mm in the presence of MP and 12.3mm in its absence (P=.0032).
The overall distribution of MPs was relatively similar across LM-5 groups of <10, 10-12, and >12mm.
The odds of MP in LM-5<10mm was 3.29 [1.38, 7.88] times higher compared to LM-5>12mm
(P=.009); or 2.54 [1.07, 6.04] times higher compared to LM-5 10-12mm (P=.036). After controlling for
age, sex, pathology status, right/left side, number of procedures and IV sedation, the adjusted odds
of MP in LM-5<10mm was 2.65 [1.08, 6.51] times higher compared to LM-5>12mm (P=.034); or 2.08
[0.83, 5.20] times higher compared to LM-5 10-12mm (P=.113).

5) WSA:
An average window surface area (78.6±5.1mm2) with presence of MP was significantly larger than
the average window surface area (63.1±2.1mm2) with absence of MP (P=.0246). Large windows

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 (>80mm2) were associated with significantly greater MP rate (36.4%) compared to smaller WSA
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(P=.0421). However, after controlling for age, sex, pathology status, right/left side, number of
procedures and IV sedation, the association was not significant (P=.2396).The mean surface area of
the window was not affected by the presence of sinus septa (P=.43) or PSAA/IOA anastomosis
(P=.17).

6) Other anatomical, patient and surgical variables:

The presence of pathology was significantly associated with MP (P=.013). On the other hand, the
presence of septa and PSAA/IOA anastomosis were not associated with increased MP risk.
Finally, the associations of factors such as age, gender, right/left sinus, residual bone height,
clinician’s experience, instrument type and IV sedation with MP were also investigated but could not
be demonstrated (P>.05).

DISCUSSION

In this 5-year retrospective study, MP occurred in 25.74% (52/202) of LWSFE procedures, in

accordance with previously reported rates (Pikos, 1999; Schwarz et al., 2015). MP’s influence on
implant survival has been controversial, showing no negative impact in some reports (Alayan &
Ivanovski, 2018; Ardekian, Oved-Peleg, Mactei, & Peled, 2006), and reducing survival rates in others
(Hernandez-Alfaro, Torradeflot, & Marti, 2008; Vina-Almunia, Penarrocha-Diago, & Penarrocha-
Diago, 2009). In this study, implant survival was not evaluated; however, implant placement was
possible at all healed sites except for one site that required simultaneous vertical augmentation at
time of implant placement. Although previous studies have attempted to identify risk factors for MP,
limited and conflicting information exists regarding the influence of sinus anatomical, surgical and
patient parameters on MP occurrence.
In this study, MP seemed to occur significantly more often when lateral wall thickness (LWT)
exceeded 1.5mm (P=.0037). The odds ratio of MP in thicker walls remained significant even after
controlling for age, sex, pathology status, right/left side, number of procedures and IV sedation. In a
maxillary sinus difficulty scoring (MSED) system, thicker walls were also considered to increase the
difficulty of the elevation procedure (Testori, Tavelli, et al., 2020). Increasing manual pressure during
osteotomy, previously considered a risk for MP (Weingart et al., 2005), may be an influencing factor

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 in thicker walls. Another possibility is that a thicker lateral wall renders maneuvering of the sinus
Accepted Article
membrane elevation instruments more challenging especially when the window dimensions are
minimal.
The impact of residual alveolar bone height (RBH) on MP rate has been debatable in the
literature where RBH<4mm increased MP rate in some reports (Lum et al., 2017; von Arx, Fodich,
Bornstein, & Jensen, 2014) (Testori, Tavelli, et al., 2020) in contrast to a greater MP risk with
RBH=3-6mm in others (Tukel & Tatli, 2018). RBH averaged 3.2 ± 1.5 mm in this study, and failed to
demonstrate any influence on MP rate (P=.29). Theoretically, greater RBH may lead to a more apical
placement of the lateral window, thus rendering the procedure more challenging and possibly
increasing the perforation risk. Regardless of RBH, the window location should be placed in close
proximity to the sinus floor to facilitate membrane instrumentation.
Maxillary sinus floor angle (LFM) was reported to affect the rate of perforation (Cho et al.,
2001). This study applied a new methodology to calculate this angle. LFM was measured directly on
the sinus floor, taking in account the point of access for osteotomy rather than an absolute angle
between the lateral and medial walls. In this study, a narrower LFM angle (<90 degrees) was most
associated with a greater perforation risk (37.9%). The angle formed between the lateral and medial
walls was also evaluated at the most anterior aspect of the sinus (LAM), representing a considerable
anatomical challenge during LWSFE, especially when the window preparation is placed far distally
from the most anterior aspect at extended edentulous sites. MP rate significantly increased (59.6%)
with narrower LAM angles (<70 degrees). The odds ratios for MP with narrower LFM and LAM
remained significant compared to wider angles even after controlling for age, sex, pathology status,
right/left side, number of procedures and IV sedation.
Sinus width has been previously considered only in the context of the angle between medial
and lateral walls (Cho et al., 2001). In this study, the medio-lateral dimension of the sinus was
measured at three levels but significant associations were only found at 5mm from the sinus floor.
MP was most likely to occur when the distance was <10mm (45.4%) in comparison to larger widths.
Interestingly, the majority of perforations (38.5%) occurred when LM-5 >12 mm whereas the high-
perforation risk group of LM-5 <10mm accounted for 28.8% of total perforations. This discrepancy
can be explained by the uneven distribution of the sinuses among groups (n=100 in LM-5 >12mm
group vs n=33 in the LM-5 <10mm group). In addition, sinus width at LM-5 was highly correlated with
LAM, such as narrower LAM angles corresponded with shorter sinus widths (P=.0001). From an MP
risk assessment standpoint, it is therefore recommended to evaluate the sinus width at LM-5 in lieu

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 of LFM or LAM since it is far simpler to measure and more time-efficient to conduct on any imaging
Accepted Article
software. In contrast, LAM and LFM angles are more labor-intensive to trace and analyze.
Nevertheless, both direct (LM-5) and indirect (LFM, LAM angles) sinus width measurements indicate
a greater MP risk with narrower sinus cavities.
The prevalence of sinus pathology was 37.62% in this study and included membrane
thickening (MT, 26.24%), mucous retention cyst (MRC, 6.44%) and chronic sinusitis (CS, 4.95%).
The remaining sinuses (62.38%) were considered healthy. These pathologies change the
consistency of the Schneiderian membrane and a similar distribution was previously described
(Lozano-Carrascal et al., 2017). This study demonstrated a statistically significant association of
pathologies with MP (P=.0013). The sinus membrane has a mean thickness of 0.5mm, but it has
potential to thicken during inflammation (Lum et al., 2017). Membrane thickness was not measured
in this study but has been previously shown to be associated with MP. Patients with MP had a
thinner membrane (0.84 mm) compared with patients without perforation (2.65mm) (Lin, Yang, Wen,
& Wang, 2016). In another study, membrane thickness <1mm or >2mm was positively associated
with perforation during the surgery (Lum et al., 2017).
Regardless of the type of ridge (atrophy/edentulous or non-atrophy/dentate), the anatomical
variation of sinus septa is diverse in prevalence and location (Ulm 1995). In this study, sinus septa
prevalence was 20.79%, a rate lower than previously reported (Pommer, Ulm, et al., 2012; Ulm et al.,
1995). Although septa have been associated with greater MP rates (von Arx et al., 2014), this study
could not demonstrate such findings (P=.23). In addition, septa height and direction were not
evaluated in this study, but they were previously shown to be associated with greater MP risk when
their height was ≥6mm (Wen, Chan, & Wang, 2013) and MSED score was considered greater if the
septa had a sagittal direction (Testori, Tavelli, et al., 2020). Differences between these findings could
be attributed to the lower septa prevalence rate in this study as well as to the location and
dimensions of the lateral window in a deliberate attempt to avoid the septa using preoperative CBCT
information.
It has been suggested that PSAA/IOA intraosseous anastomoses are present in 100% of
cases (Solar et al., 1999), but can be identified on CT scans in only 50% of cases (Taschieri &
Rosano, 2010). The prevalence of these anastomoses in this study was 16.83% and was not found
to influence the MP rate. Anatomical variations, size of the intraosseous canal, examiner variability
and CBCT image definition could explain those differences between studies.

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 Patient factors such as gender, age and side (right vs. left sinus) were not related to an
Accepted Article
increased MP rate (P>.05), thus corroborating previous findings (Zimmo et al., 2018).
Surgical factors such as the osteotomy instrument, window surface area (WSA) and surgeon
training level were evaluated in this study. The osteotomy instrument type, i.e. piezoelectric device,
carbide/diamond round burs or reamer kit, did not seem to influence the rate of perforation (P>.05).
Interestingly, MP was significantly more prevalent with larger WSA (mean of 78.6mm2,
P=.02); nonetheless, the association was no longer significant after controlling for age, sex,
pathology status, right/left side, number of procedures and IV sedation. Theoretically, a larger
window allows the clinician better visibility and improved access for instrumentation, therefore
decreasing the chance of perforation. However, it is possible that MP occurs during constant manual
pressure on an unevenly thick wall in a large window preparation, as LWT tends to change
dramatically from one location to another (Monje et al., 2014). Alternatively, one could speculate that
MP occurred during membrane elevation following a small window preparation, thus prompting the
surgeon to extend the window dimensions for improved access (Pikos, 1999), and ultimately
reporting the final WSA in the patient’s record. This study failed to demonstrate any correlations
between window dimensions and the presence of sinus septa or PSAA/IOA anastomoses.
Nonetheless, careful CBCT planning and the use of a surgical guide is suggested for the window
location and size to avoid anatomical landmarks (Lozano-Carrascal et al., 2017).
Lastly, the clinician training level was not found to significantly affect MP rate in this study.
Similar results regarding the operator experience were previously described (Shiffler et al., 2015). It
is possible that no influence was found because residents (especially when novice) would typically
receive greater supervision by experienced instructors during advanced treatments such as LWSFE.
Main study limitations are mostly associated with its retrospective design and include the
following: 1) lack of ability to accurately identify the time of MP occurrence, i.e. during osteotomy vs.
during membrane elevation, 2) MP reporting was based on direct visualization and not postoperative
CBCT; hence, while unlikely, it could have been underreported, 3) lack of reporting on MP size and
location due to inconsistent documentation about MP dimensions in patient records, 4) lack of
reporting on septa height/orientation and location and diameter of PSAA/IOA anastomoses, 5) lower
CBCT image definition (voxel size 0.3mm) since all scans were taken for clinical purposes avoiding
unnecessary greater patient radiation, 6) possible variability in lateral inclination of the head during
CBCT scans, thus affecting sagittal views, 7) possible discrepancies between radiographic and
clinical positions of surgical guides, and 8) only including clinicians in training, although the overall

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 MP prevalence and distribution corresponded to previous reports and did not seem affected by level
Accepted Article
of training.

CONCLUSIONS

This retrospective study presented new assessment methodologies in reporting descriptive

findings of the maxillary sinus anatomy specific to LWSFE, outlined the influence of anatomical,
patient and surgical factors on MP occurrence and proposed a risk assessment based on observed
values. Within study limitations, there were significant associations between MP and the following
parameters: thicker LWT (mean 1.8mm), narrower LAM angle (mean 68.2°), narrower LFM angle
(mean 92.3°), narrower sinus width at LM-5 (mean 11.4mm), presence of sinus pathology
(membrane thickening, chronic sinusitis or mucous retention cyst), and larger WSA (mean 78.6mm2).
Larger sample sizes in prospective studies may be needed to validate these findings.
Clinical implications include recommending the evaluation of LWT and sinus width (in lieu of
LFM and LAM angles) in planning for LWSFE procedures. Clinicians should exercise caution when
performing LWSFE in the presence of thicker lateral walls, narrower medio-lateral sinus widths, and
sinus pathologies. In particular, care should be taken to design the window in close proximity to the
anterior wall and sinus floor to facilitate access to and instrumentation of the membrane, thus
reducing MP risk.

CONFLICT OF INTEREST STATEMENT

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

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 Table 1. Distribution of MP rate within and across variable categories
Accepted Article
Variable Variable
Categories
Distribution
of Sinuses
Membrane
perforation
Frequency
of MP
Distribution
of MP
Overall
distribution
Risk
Assignment
N (%) (MP) N (%) within of MP for MP
groups across
groups

LWT† No 86 (42.6%) 86.0% 57.3%

<1.5mm 100 (49.5%) Lowest
Yes 14 (6.9%) 14.0% 26.9%

No 37 (18.3%) 60.7% 24.7%

1.5-2mm 61 (30.2%) Highest
Yes 23 (11.9%) 39.3% 46.2%

No 27 (13.4%) 65.9% 18.0%

>2mm 41 (20.3%) High
Yes 15 (6.9%) 34.1% 26.9%

LFM‡ No 36 (17.8%) 62% 24%

<90° 58 (28.7%) Highest
Yes 22 (10.8%) 38% 42.3%

No 56 (27.7%) 79% 37.3%

90-100° 71 (35.2%) Lowest
Yes 15 (7.4%) 21% 28.8%

No 58 (28.7%) 79.4% 38.6%

>100° 73 (36.1%) Lowest
Yes 15 (7.4%) 20.5% 28.8%

LAM§ No 21 (10.3%) 40.3% 14%

<70° 52 (25.7%) Highest
Yes 31 (15.3%) 59.6% 59%

No 71 (35.1%) 82.5% 47.3%

70-80° 86 (42.6%) Low
Yes 15 (7.4%) 17.4% 28.8%

No 58 (28.7%) 90.6% 38.6%

>80° 64 (31.7%) Lowest
Yes 6 (2.9%) 9.3% 11.5%

LM-5¶ No 18 (9%) 54.5% 12%

<10mm 33 (16.3%) Highest
Yes 15 (7%) 45.4% 28.8%

No 52 (26%) 75.3% 34.6%

10-12mm 69 (34.2%) Low
Yes 17 (8.4%) 24.6% 32.7%

>12mm 100 (49.5%) No 80 (40%) 80% 53.3% Lowest

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 Yes 20 (10%) 20% 28.4%
Accepted Article
WSA††
L (>80mm2) 44 (24.0%)
No 28 (15.3%) 63.6% 20%
Highest
Yes 16 (8.7%) 36.4% 37.2%

No 90 (49.1%) 80.4% 64.3%

M (40-80mm2) 112 (61.2%) Low
Yes 22 (12%) 19.6% 51.2%

No 22 (12%) 81.5% 15.7%

S (<40mm2) 27 (14.8%) Lowest
Yes 5 (2.7%) 18.5% 11.6%

†LWT=Lateral Wall Thickness

‡LFM=Angle formed between lateral and medial walls of sinus at the Floor of the sinus
§LAM= Angle formed between lateral and medial walls of sinus at the Anterior wall of the sinus
¶LM-5= Sinus width or distance between lateral and medial walls at 5mm apical to the floor of the sinus
††WSA=Window Surface Area

Table 2. Associations between MP and the anatomical variables by GEE

Variable Membrane Frequency Mean Standard P Value

Perforation error (Association
(MP) w/Membrane
perforation)

LWT† No 150 1.53mm 0.05 .0013*

Yes 52 1.8mm 0.07

LFM‡ No 150 96.9° 0.7 .0059*

Yes 52 92.2° 1.5

LAM§ No 150 78.3° 0.8 .0001*

Yes 52 68.2° 1.5

LM-5¶ No 150 12.3mm 0.2 .0032*

Yes 52 11.4mm 0.2

WSA†† No 150 63.1mm2 2.1 .0246*

Yes 52 78.6mm2 5.1

†LWT=Lateral Wall Thickness
‡LFM=Angle formed between lateral and medial walls of sinus at the Floor of the sinus

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 §LAM= Angle formed between lateral and medial walls of sinus at the Anterior wall of the sinus
Accepted Article
¶LM-5= Sinus width or distance between lateral and medial walls at 5mm apical to the floor of the sinus
††WSA=Window Surface Area
*Statistically significant p-value

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 FIGURE LEGENDS
Accepted Article
Figure 1. LWT is measured at 5mm apical to the sinus floor at the presumed location of the window
preparation on a coronal CBCT slice.

Figure 2. LFM angle measurement: Point F is first identified as deepest point on sinus floor, followed
by extending a 5-mm vertical line apically (point F5), a perpendicular line to F-F5 connecting F5 to
lateral (L) and medial (M) walls. The resulting LFM angle is accurately measured on this coronal
CBCT slice.

Figure 3. Sinus width measurements on a coronal CBCT slice. LM-5, LM-10 and LM-15 are
measured by tracing horizontal lines between lateral and medial walls at 5, 10 and 15mm
respectively from the sinus floor.

Figure 4. LAM angle measurement: a. Point A is identified after tracing point F8 at 8mm apical to
point F and connecting a perpendicular line from F8 to the anterior wall on a sagittal CBCT section;
b. Point A8 was determined on an axial section at 8mm posterior to point A. Then, a perpendicular
line was traced connecting point A8 to both lateral (point L) and medial (point M) walls. The resulting
angle created between AL and AM was LAM.

Figure 5. RBH measurement on a coronal CBCT slice from sinus floor to crest of edentulous ridge.
This example shows all linear measurements completed on the coronal slice, i.e. LWT, LM-5, LM-10,
LM-15 and RBH and LFM angle.

Figure 6. Odds ratio of MP according to variables.

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