Received: 3 February 2021 Revised: 21 April 2021
DOI: 10.1111/cid.13016
ORIGINAL ARTICLE
Prevalence, risk factors, and repair mechanism of different
forms of sinus membrane perforations in lateral window sinus
lift procedure: A retrospective cohort study
Stefan Krennmair MD1 | Alexander Gugenberger DMD2 |
Michael Weinländer MD, DMD, PhD3 | Gerald Krennmair MD, DMD, PhD4
Michael Malek MD, DMD1 | Lukas Postl MD, DMD, PhD1
1
Oral and Maxillofacial Surgery, Medical (JKU)
University, Linz, Austria
2
Department of Prosthodontics, Sigmund
Freud Private-University, Vienna, Austria
3
Dental School, Karl Franzens Medical
University of Graz, Graz, Austria
4
Head Department of Prosthodontics,
Sigmund Freud University, Vienna, Austria
Correspondence
Gerald Krennmair, Department
Prosthodontics, Sigmund Freud University,
4600 Wels, Auwaldstrasse 5, 1020 Vienna,
Austria.
Email: krennmair@aon.at
Clin Implant Dent Relat Res. 2021;23:821–832.
Accepted: 29 April 2021
|
Abstract
Objectives: To evaluate prevalences, affecting risk factors and efforts for repair
mechanism for different forms of sinus membrane perforations (SMP) during sinus
floor elevation (SFE) using the lateral window technique (LWT).
Material and methods: For 334/434 patients, SFE undergoing LWT prevalence of
SMP was retrospectively evaluated including a subselection based on membrane per-
foration size (<10 mm: small–moderate/≥10 mm: large) and biotype (BT; thick
BT/thin BT) into four subgroups (SMP1: thick BT/small–moderate; SMP2: thin BT/
small–moderate; SMP3: thick BT/large; SMP4: thin BT/large). For the various sub-
groups, patient- and surgery-related/anatomic risk factors affecting SMP were evalu-
ated and the scope of sinus membrane repair (SSMR) mechanisms rated with 1 (easy)
to 5 (complex) was compared.
Results: For 103/434 SMP (27.6%) in 93/334 patients (30.8%) the prevalence of
various forms of SMP differed significantly (p < 0.001) among the four subgroups.
SMP4 with a prevalence of 45.6% (n = 47) was the most frequent type, while
SMP3 had low prevalence with 4.85% (n = 5). Small/moderate SMPs with thick
(SMP1: n = 26) or thin BT (SMP2: n = 23) were seen in 26.2% and 23.3%, respec-
tively. Univariate analysis showed significant differences between subgroups with
large perforations (SMP3/SMP4) and those with small/moderate perforations
(SMP1/SMP2) regarding anatomic risk factors such as residual ridge height
(p = 0.023) and history of previous oral surgical interventions (OSI; p = 0.026).
Most evidently, multivariate analysis showed that induction of large SMP with
thin biotype (SMP4) was significantly affected by the presence of sinus septa
(p < 0.022, OR: 2.415), reduced residual ridge height (p < 0.001, OR: 1.842), and
previous OSI (p < 0.001, OR: 4.545). SSMR differed significantly (p < 0.001)
between SMP4 (4.62 ± 0.49) and the subgroups SMP1 (1.11 ± 0.32), SMP2 (1.08
± 028), and SMP3 (2.2 ± 0.55).
Conclusion: The most frequently found type of SMP had characteristics of thin bio-
type and large size associated with risk factors such as sinus septa, reduced residual
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822 KRENNMAIR ET AL.

ridge, and previous surgical interventions and required challenging repair mechanisms
assessing clinical impact.

KEYWORDS
lateral window, repair mechanism, sinus membrane perforation

What is known
• Iatrogenic perforation of the maxillary sinus membrane during membrane elevation proce-
dure using the lateral window technique represents the most frequent intraoperative compli-
cation of sinus floor augmentation surgery.
• Only limited information is available on the prevalence of various types of sinus membrane
perforations and their characteristics.

What this study adds

• Differentiation of the perforated sinus membrane into various forms in relation to perfora-
tion size (small vs large) and sinus membrane characteristics (thick vs thin sinus membrane) is
crucial for assessing the prevalence of sinus membrane perforation with clinical impact as
well as for the adequate membrane repair mechanisms adjusted.

1 | I N T RO DU CT I O N were sutured and/or covered with tacked collagen mem-

Iatrogenic perforation of the maxillary sinus membrane during the
membrane elevation procedure using the lateral window technique
has been reported to be the most frequent intraoperative complica-
1–7
tion of sinus floor augmentation surgery. Successfully elevated and
intact sinus membranes represent the intrasinusoidal coverage of the
maxillary sinus augmentation graft material.8–10 However, perforation
of the sinus membrane may allow for graft displacement/migration
and also graft contamination resulting in postoperative complications
such as maxillary sinusitis and or graft necrosis/infection.2–4,11–16
Several reports have described patient-related risk factors, such
as smoking, age/gender, and surgery-related/anatomic risk factors,
with sinus anatomy, presence of maxillary sinus septa, reduced resid-
ual ridge height, sinus membrane thickness, gingival phenotype and
use of rotary instruments having been identified as risk factors affect-
ing sinus membrane perforation.5–7,17–19 Consequently, numerous
studies on sinus membrane perforation have also reported on suc-
cessful sinus membrane repair techniques using resorbable sutures,
patching with different membranes, bone blocks instead of particle
bone, buccal fat pads, and/or various clotting materials.20–22
However, most studies only report on the presence or absence of
perforation and only scarce information is available on the prevalence
of various types of perforations and their characteristics.1–4,11–15
With regard to sinus membrane lesions, Prossaeff and colleagues 20
23
and Pikos have given recommendations for sinus membrane
repair mechanisms of varying size. In the studies of Hernandenz
24 25
and colleagues and Almeira-Ferreira and colleagues, sinus floor
elevations (SFEs) with sinus membrane perforations were sub-
selected with respect to perforation size and evaluated for clinical
augmentation and implant outcome. In both studies, membrane
repair was adjusted to the perforation size and the perforations
branes.24,25 Interestingly, Hernandez and colleagues24 demon-
strated an inverse correlation between the extent of membrane
perforation size and the survival rate of simultaneously placed
dental implants with a significant lower implant success rate for
large perforations. In contrast, Almeida-Ferreira and colleagues25
did not find differences of clinical implant outcome between small
and large successfully repaired perforations. These findings are in
accordance with Froum and colleagues 26 reporting that the regen-
erative potential of the bone grafting procedure is not inferior fol-
lowing sinus membrane perforations after successful repair
compared to that in nonperforated sinus augmentations.
Several findings have shown that differentiation of the sinus
membrane perforation size and especially also of the membrane char-
acteristics/biotype seems to be essential for selection of the appropri-
ate repair mechanisms.17,24–31 In cases with perforated sinus
membrane implementation of a successful sinus augmentation and
consequently achievement of successful implant outcome, the repair
mechanism chosen has to be carefully adjusted to membrane biotype
and to the sinus membrane perforation size.20–25,30,31
However, although sinus membrane perforations have been
reported numerically in several studies there is an obvious lack of
information regarding the prevalence and risk factors for different
forms of sinus membrane perforations.1,5–7 Moreover, detailed
reports revealing that different forms of sinus membrane perforation
require different repair methods in conjunction with the need for
divergent clinical efforts are not available.20,21,31
The primary aim of the present study was to evaluate and com-
pare the prevalences and risk factors for different groups of sinus
membrane perforations. The secondary aim was to establish a
detailed risk factor analysis for different forms of sinus membrane
perforations and to evaluate and to describe the performance and
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KRENNMAIR ET AL. 823

TABLE 1 Patients inclusion and exclusion criteria ovoid osteotomy was made with a round bur (Komet-Dental; W&H,

Inclusion criteria Exclusion criteria Bürmoos, Austria) until the sinus mucosa was visible. A piezoelectric
device (Piezosurgery, Mectron) was used to finalize facial sinus wall
Edentulous posterior Untreated periodontitis
maxillary region osteotomy. This was followed by a careful and complete membrane

Healed sites Sinus pathology reflection from the maxillary sinus floor and medial creating space for
the bone graft. Filling material consisted of inorganic bovine bone
No sinus pathology Uncontrolled systemic disease
mineral (Bio-Oss, Geistlich, Wolhusen, Switzerland) mixed with autol-
Age: >18 years Bisphosphonate therapy
ogous bone (osteotomy sites/implant drilling) in a Bio-Oss/autoge-
RRH Uncontrolled diabetes mellitus
nous bone mixture of 4:1.32–34 After graft placement the facial sinus
(HbA1C >7.5%)
osteotomy was covered with collagen membrane (Bio-Gide, Geistlich,
Height ≤7 mm Alcoholism/drug abuse
Wolhusen, Switzerland) and the mucoperiosteal flap was
Width >6 mm Severe bruxism (CMD disorders)
repositioned and sutured (Vicryl, Ethicon, Johnson and Johnson, Ger-
No onlay grafting Lack of compliance
many; Seralon, Serag-Wiessner, Naila, Germany). Postoperative rec-
(horizontal/vertical)
ommendations included nonsteroidal analgesics, nasal decongestant
Periodontally healthy History of radiation therapy head/neck
spray, and chlorhexidine digluconate mouthwash. Antibiotic coverage
Oral hygiene recall physical handicap
was initiated 1 day prior to surgery and continued for 7 days. In addi-
Abbreviations: CMD, craniomandibular disorders; RRH, residual ridge tion, patients were instructed to refrain from blowing their nose for
height.
2 weeks.

the intensity of sinus membrane repair mechanisms for different 2.3 | Sinus membrane perforation and surgical
forms of sinus membrane perforations. repair mechanism

When detecting a sinus membrane perforation, the membrane sur-

2 | MATERIALS AND METHODS
2.1 | Patient selection
For this retrospective, single-center cohort study, patients with partial
(maxillary posterior region) or complete maxillary edentulousness with
sinus floor elevation procedures (SFEs) using the lateral window tech-
nique were included. Between January 2009 and December 2014,
355 consecutive patients (181 female/174 male, mean age: 55.9
± 10.5 years) meeting the inclusion criteria (Table 1) were included
and underwent 434 SFE procedures. Each patient signed a consent
form including sinus augmentation procedure and follow-up evalua-
tion according to the Declaration of Helsinki and the study protocol
was approved by the local ethics committee (UAE-09-92). The
STROBE (Strengthening the Report of Observational studies in Epide-
miology) guidelines for reporting cohort studies were adhered to in
the preparation of the manuscript.
2.2 | Surgical procedure
For patients included presurgical diagnosis comprised clinical and
radiographic examinations (panoramic radiography and computed
tomography [CT] or cone beam CT [CBCT]) for determining bone vol-
ume, maxillary sinus anatomy, and pathology. SFEs were performed
under light sedation and local anesthesia (Ultracain DS forte, Aventis
Pharma; Midazolam [Dormicum], Roche Pharma) by the same experi-
enced surgeon (G.K. >20 years of experience in oral and maxillofacial
surgery). Full-thickness mucoperiosteal flaps were raised and an
rounding the perforation was cautiously dissected with a blunt instru-
ment, in an attempt to relieve the tear at the perforated area. In case
of a membrane perforation, the size, the location, and the membrane
biotype were registered as follows:
• The size of the membrane perforation was measured using a peri-
odontal probe and classified as small to moderate (<10 mm) or
large (≥10 mm) perforation.24,25
• The location of the perforation was classified as “central “or “lat-
eral” (border of osteotomy sites).22,24
• The membrane biotype/thickness (BT) of the sinus membrane:
clinical measurements in the perforated setting were classified
according to the following criteria: a thin sinus membrane biotype
was defined as clear translucent membrane, often impossible to
measure with the periodontal probe, involving the risk of further
tearing and difficulties in withstanding the handling by surgical
tweezers and tension. A thick membrane was defined as a mem-
brane allowing for measurement by periodontal probe and/or
being detachable and allowing handling by surgical tweezers
without any further rupture. According to the clinical measure-
ments obtained and a threshold defined with 1.5 mm, sinus mem-
branes biotypes were classified as thick sinus membrane biotypes
(≥1.5 mm) and thin sinus membrane biotypes (<1.5 mm).17,27
According to the sinus membrane biotype defined (thick BT
[≥1.5 mm] vs thin BT [<1.5 mm]) and the extent of the perforation size
(<10/≥10 mm) four different subgroups of SFE with membrane perfora-
tions were established. For each subgroup various treatment options for
membrane repair were followed using different techniques and materials:

824
F I G U R E 2 Small/moderate perforation (<10 mm) in thin sinus
membrane biotype
• Group P1: Thick BT/small–moderate (<10 mm) perforations in cen-
tral/lateral location (Figure 1(A)): Central perforations were
repaired using a collagen membrane (Bio-Gide Geistlich, Wolhusen,
Switzerland; Figure 1(B)) and (when access was possible) using
resorbable sutures (6/0 Vicryl, Ethicon, Norderstedt, Germany). For
lateral locations of perforated thick membranes suturing was per-
formed by attaching the membrane at the osteotomy sites (drill
holes) and additional membrane coverage was extended over the
osteotomy border. Implants were placed in a 1-stage (≥5 mm RRH)
or 2-stage (<5 mm RRH) procedure depending on the pre-existing
residual ridge height (RRH) for primary implant stability.
• Group P2: Thin BT/small–moderate (<10 mm) perforations/central
or lateral location (Figure 2): Central perforations were repaired by
patching with collagen membrane (Bio-Gide, Geistlich, Wolhusen,
Switzerland); in lateral locations of thin membrane perforations the
collagen membranes used covered the perforated sinus membrane
sites extending to the osteotomy border. Implant placement was
performed in a 1- or 2-stage procedure depending on the RRH for
primary implant stability (≥/<5 mm residual ridge).
• Group P3: Thick BT/large (≥10 mm) perforations in central location
(Figure 3(A)): direct suturing of the sinus membrane and additional
collagen membrane patching (Figure 3(B)). In lateral locations of
the perforation the thick membranes were sutured to the cranial
osteotomy using transosseous drill hole sites and additionally pat-
ched with collagen membrane. Implant placement was performed
in relation to the pre-existing alveolar crest dimensions.
• Group P4: Thin BT/large (≥10 mm) perforations/central or lateral
location (Figure 4(A)): Initially it was attempted to reduce the per-
foration size with smart sutures (6.0 Vicryl; Figure 4(B)), this was
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KRENNMAIR ET AL.
F I G U R E 1 Small/moderate
perforation (<10 mm) in thick sinus
membrane biotype (A). Sinus membrane
perforation covered with collagen
membrane (B)
followed by applying a double layer of collagen membrane
patching22–25:
1. Layer of collagen membrane (Bio-Gide Geistlich, Wolhusen, Swit-
zerland; or Ossoguard, 3-I) for veneering the cranial aspect of the
cavity (Figure 4(C))
2. Tacking and/or suturing (6/0 Vicryl, Ethicon, Norderstedt, Ger-
many) a collagen membrane (Bio-Gide Geistlich; or Ossoguard, 3-I)
on the cranial osteotomy sites with extension to the outside of the
window (Figure 4(D)) and following of sinus cavity grafting
(Figure 4(E)). Implant placement was predominately performed in a
2-stage procedure regardless of the RRH.22–25
2.4 | Follow-up examinations: Outcome measures
Patients with SFE procedures were included in a regular recall pro-
gram (oral prophylaxis program) and were initially seen for the sched-
uled control visits (during the first 3 months), and thereafter at the
12-month (1-year) postaugmentation follow-up. The entire study pop-
ulation included was subdivided into a group without (“NP”) maxillary
sinus membrane perforation (SMP) and in a group with sinus mem-
brane perforation (“P”), the latter group being further subdivided into
four subgroups (SMP1–4) representing different forms of SMP as
described above. During the follow-up examinations the following pri-
mary and secondary outcome measures were assessed. Clinical mea-
surements were performed by an independent outcome assessor
(KS) trained and experienced in radiographic/clinical measuring and
being blinded to the study design.
2.4.1 | Primary outcome measurements
The primary outcome of interest to be evaluated was (1) the overall
prevalence of sinus membrane perforations (“P”) and (2) the preva-
lence of the four defined different forms of sinus membrane perfora-
tions (SMP1–4). In addition, the association of different forms
(SMP1–4) of membrane perforation with patient- and surgery-
related/anatomic risk parameters was assessed.
Patient-related risk factors as well as surgery-related/anatomic
risk factors associated with sinus membrane perforations included the
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KRENNMAIR ET AL. 825

F I G U R E 3 Large sinus membrane

perforation (≥10 mm) in thick sinus
membrane biotype (A). Direct closure with
sutures (B)

F I G U R E 4 Large sinus membrane

perforation (≥10 mm) in thin sinus
membrane biotype (A). Smart sutures to
stabilize cranial cavity (B). Sinus cavity
veneered with collagen membrane (C).
Tacked collagen membrane outside the
sinus osteotomy (D). Sinus cavity
grafting (E)

following: age, gender, smoking habits, diabetes, dimension of
the residual ridge height (RRH:mm), presence/absence of maxillary
sinus septa; previous oral surgery interventions (OSI) such as apical
root surgery or previous tooth extraction with or without oroantral
communications (OAC); maxillary sinus side (left or right); extension of
sinus augmentation in mesio-distal direction by number of tooth units
for replacement (single tooth, 2 tooth units or 3 to >3 tooth
units).1,5–7
Presence of maxillary sinus septa, height of residual ridge (RRH:
mm) and sinus membrane thickness (mm) of the facial maxillary sinus
wall were measured by CBCT.5–7,35–37 Using CBCT images evaluated
by an independent assessor (SK) sinus membrane thickness of the
facial maxillary sinus wall was measured at three regions of interest
(mesial, central, distal region of the intended facial osteotomy site)
and was averaged for a sinus mucosa thickness value.4,5–7,27
According to the averaged measured thickness value and by using a
threshold defined as 1.5 mm, sinus membranes measured were
divided into a thick sinus membrane biotype (≥1.5 mm) and a thin
sinus membrane biotype (<1.5 mm).6,7,17,27
2.4.2 | Secondary outcome measurements
1. Risk factor analysis assessing odds ratio for patient- and surgery-
related/anatomic risk factors affecting different forms of sinus
membrane perforations (SMP1–4).

826
2. Evaluation of the successful clinical performance of membrane
repair for SFE with sinus membrane perforations. The scope
(extent) of sinus membrane repair (SSMR) for maxillary sinus floor
augmentation considering different repair mechanism used for the
four subgroups selected was evaluated. Assessing the surgical
efforts applied, the amount of time and material used and the
clinician-based emotional stress involved the scope of the sinus
membrane repair (SSMR) mechanism was rated with a rating from
1 to 5 (1 = very easy, 2 = easy, 3 = moderate, 4 = difficult,
5 = very difficult to repair; complex). The rated scope of sinus
membrane repair was compared between the four subgroups of
SMP. All SSMRs were rated by the same experienced surgeon per-
forming all SFEs (G.K. >20 years of experience in oral and maxillo-
facial surgery).
2.5 | Statistical analysis
All parameters were recorded in a descriptive statistical manner, tabu-
lated, and evaluated. For the univariate analysis comparing presence/
absence of sinus membrane perforations or small/large sinus mem-
brane perforations regarding normally distributed continuous variables
the independent two-sample t test or, in the case of non-normality
(verification with the Kolmogorov–Smirnov test with Lilliefors correc-
tion, a p-value <10% was used as indicator for non-normal distribu-
tion), the exact Mann–Whitney U test was used. For comparing
categorical variables Fisher's exact test (1) total SMP and (2) the exact
chi-square test was used.
Moreover, generalized multivariate models using generalized esti-
mating equations were used for identifying statistically relevant
patient- and/or surgery-related and anatomic risk factors.
The risk factors (defined a priori based on a medical point of view)
were entered as independent variables with presence/absence of
sinus membrane perforation and small/large sinus membrane perfora-
tion as dependent dichotomous variables. For easy interpretation, the
odd ratios including 95% confidence intervals for each risk factor are
presented. The type I error was set at 5% (two-sided) without adjust-
ment for multiple testing. For statistical analysis, the statistical com-
puting software R Version 3.5.1 (R Foundation for Statistical
Computing, Vienna, Austria, http://www.R-project.org) was used.
3 | RESULTS
3.1 | Primary outcome measurements
3.1.1 | Prevalence of different types of SMP
For 355 patients with 434 SFE included in the present study an over-
all incidence of SMP of 23.8% at SFE level (103/434) and 26.5% at
patient level (94/355) was seen. According to the criteria defined, the
group of 103 sinus membrane perforations could be further sub-
divided into four subgroups (P1–P4) as follows:
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KRENNMAIR ET AL.
• (P1) group I (thick BT/<10 mm): n = 27 SFEs (26.6%); 53 implants
(1-stage: 11, 2-stage: 42).
• (P2) group II (thin BT/<10 mm): n = 24 (23.3%); 47 implants (1-
stage: 15, 2-stage: 32).
• (P3) group III (thick BT/≥10 mm): n = 5 (4.8%); 11 implants (1-
stage: 0, 2-stage: 11).
• (P4) group IV (thin BT/≥10 mm): n = 47 (45.6%); 90 implants (1-
stage: 14, 2-stage: 76).
The prevalence of the various sinus membrane perforations dif-
fered significantly (p < 0.001) among the four subgroups (SMP1–4),
showing group SMP4 (thin BT/large [≥10 mm] perforation size) as the
most frequent one (45.6%) and group SMP3 (thick BT/large [≥10 mm]
perforation) as a rare intraoperative complication (4.8%, p < 0.001). The
prevalence of large (n = 52 [50.5%]) versus small–moderate (n = 51
[49.5%]) forms of membrane perforations did no differ significantly.
However, significantly more perforations were seen for thin sinus mem-
branes than for thick membranes (71 [68.9%] vs 32 [31.1%, p < 0.001).
3.1.2 | Risk factors for SMP and for perforation
subgroups (P1–P4)
In the univariate comparative model (Table 2), no differences were
found for patient-related risk factors in general between the perfo-
rated (P) and nonperforated group (NP) except for the patients' age
(p = 0.015). However, with respect to surgery-related/anatomic risk
factors significant differences were noted. The perforation group
(P) showed a significantly lower residual ridge height (RRH; p < 0.001),
a significantly higher incidence of 2-stage SFE procedures (p < 0.001),
previous oral surgical interventions, presence of maxillary sinus septa,
and thin sinus membrane biotype (p < 0.001) than the nonperforated
group (“NP”; Table 2). Fifty-five percent (6/11) of the risk factors
included showed a significant difference.
Table 3 shows the prevalence of the subgroups of SMP (1–4) includ-
ing detailed patient- and surgery-related risk factors. In the univariate
analysis, subgroups SMP1–P4 did not differ for risk factors such as gen-
der, age, smoking, sinus side treated (left side vs right side), presence of
maxillary sinus septa, and previous oroantral communications (OAC).
However, the analysis demonstrated differences between the subgroups
for the surgical stage performed (1-stage vs 2-stage: p = 0.019), the resid-
ual ridge height (p = 0.023) and the history of previous oral surgery inter-
ventions (OSI; p = 0.026). In particular, perforations in subgroup SMP4
(thin BT/≥10 mm) showed a significantly higher frequency of 2-stage SFE
procedures (p = 0.019) as well as a higher frequency of previous oral sur-
gical interventions (OSI) such as tooth removal (p = 0.026) compared to
groups P1/P2/P3, respectively. Both groups with large SMP (SMP3 and
SMP4) had a significantly lower RRH (2.0 ± 1.0, 2.8 ± 1.3 mm) than
groups P1 and P2 with small/moderate SMP size (3.1 ± 2.1, 3.9
± 1.7 mm; p = 0.023). SFEs for single tooth (ST) replacements revealed
significantly fewer SMP in all subgroups (P1–P4) than with 2- or 3/>3
tooth replacements (Table 3). Only 3 out of 11 risk factors (RRH, stage,
OSI) showed significant overall differences (27.3%).
 17088208, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/cid.13016 by Mahidol University Library and Knowledge Center, Wiley Online Library on [06/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
KRENNMAIR ET AL. 827

T A B L E 2 Univariate analysis of
Total Nonperforation (NP) Perforation (P) p-value
patient-, surgical-, anatomical-related risk
factors in sinus floor elevation Pat. 355 261 (73.5%) 94 (26.5%)
procedures with and without sinus SFE 434 331 (76.2%) 103 (23.8%)
membrane perforation Age (years) 55.9 ± 10.5 55.2 ± 10.5 58.2 ± 9.9 0.015
Sex: female 181 (51.0%) 130 (49.8%) 51 (54.3%) 0.473
Smoker+ 152 (42.8%) 115 (44.1%) 37 (39.4%) 0.467
DM+ 37 (10.4%) 27 (10.3%) 10 (10.6%) 0.99
Right sinus 223 (51.4%) 169 (51.1%) 54 (52.4%) 0.822
RRH (mm) 3.89 ± 1.51 4.15 ± 1.46 3.05 ± 1.35 0.001
SFE: 1-stage 162 (37.3%) 140 (42.3%) 22 (21.4%) 0.001
SFE: 2-stage 272 (62.7%) 191 (57.7%) 81 (78.6%)
Septa (yes) 125 (28.8%) 47 (14.2%) 78 (75.7%) 0.001
OSI+ 93 (21.4%) 54 (16.3%) 39 (37.9%) 0.001
OAC+ 27 (6.2%) 10 (3.0%) 17 (16.5%) 0.001
SFEd: ST 89 (20.5%) 69 (20.8%) 20 (19.4%) 0.522
≥3-teeth unit 272 (62.7%) 206 (62.2%) 66 (64.1%)

Abbreviations: DM, diabetes mellitus; OAC, oroantral communication; OSI, oral surgical interventions;
RRH, residual ridge height (mm); SFE, sinus floor elevation procedure; SFEd, sinus floor elevation
dimension; ST, single tooth unit.

T A B L E 3 Characteristics of risk factors in sinus floor elevations with subtypes of sinus membrane perforations (SMP1–4) in relation to
perforation size (</≥10 mm) and membrane biotype (thick/thin BT)

SMP group I thick SMP group II thin SMP group III thick SMP group IV thin
BT/<10 mm BT/<10 mm BT/≥10 mm BT/≥10 mm p-value
SFE 27 (26.2%) 24 (23.3%) 5(4.8%) 47 (45.6%) 0.001
Pat. 25 21 5 43
Age (year) 61.0 ± 5.9 58.5 ± 10.2 64.4 ± 8.4 55.5 ± 10.7 0.052
Female 11 16 4 27 0.238
Male 16 8 1 20
Smoker (yes) 6 7 2 14 0.864
Right side 9 7 2 26 0.135
Left side 17 17 3 21
RRH (mm) 3.1 ± 2.1 3.9 ± 1.7 2.0 ± 1.0 2.8 ± 1.3 0.023
Stage-1 7 11 0 7 0.019
Stage-2 19 13 5 40
Septa (yes) 12 13 2 18 0.641
OSI 9 3 2 23 0.026
OAC 2 0 0 4 0.517
SFEd: ST 3 9 0 15 0.009
≥3 unit 22 11 5 26

Abbreviations: OAC, oroantral communication; OSI, oral surgical interventions; RRH, residual ridge height (mm); SFE, sinus floor elevation procedure; SFEd,
sinus floor elevation dimension; ST, single tooth unit.

3.2 | Secondary outcome measurements
3.2.1 | Risk factor analysis for different forms of
sinus membrane perforation (group P1–P4)
Table 4 presents the multivariate analysis of risk factors affecting vari-
ous forms of sinus membrane perforations (SMP1–4) during SFE
procedures. Patient-related risk factors such as age, gender, and
smoking habits as well as surgery-related/anatomic risk factors such
as sinus side did not differ between the subgroups and showed no sig-
nificant distribution as risk factors affecting various types of SMP.
However, the presence of maxillary sinus septa and the presence
of reduced residual ridge height were identified as risk factors affect-
ing SMP in three out of four (75%) subgroups. In addition, for the
 17088208, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/cid.13016 by Mahidol University Library and Knowledge Center, Wiley Online Library on [06/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
828 KRENNMAIR ET AL.

TABLE 4 Multivariate risk factor analysis of sinus membrane perforation for the subgroups (P1–P4) evaluated

95% CI – odds ratio

B SE p-Wert Odds ratio Lower Upper

Group I: thick/<10 mm Constant term 2.244 1.637 0.170
Age 0.059 0.060 0.114 1.061 1.012 1.112
RRH min 0.391 0.160 0.014 1.479 1.081 2.020
Sex (female vs male) 0.859 0.468 0.066 2.364 0.994 5.917
Smoker (no vs yes) 0.480 0.508 0.345 1.615 0.597 4.369
Side (right vs left) 0.837 0.461 0.069 2.309 0.936 5.682
Septa (no vs yes) 1.599 0.472 0.001 4.950 1.961 12.500
OSI (no vs yes) 1.071 0.475 0.024 2.915 1.149 7.407
Group II: thin/<10 mm Constant term 3.140 1.658 0.058
Age 0.026 0.023 0.270 1.026 0.980 1.075
RRH min 0.016 0.149 0.916 1.016 0.758 1.361
Sex (female vs male) 0.336 0.478 0.481 1.400 0.549 3.572
Smoker (no vs yes) 0.111 0.489 0.821 1.117 0.428 2.915
Side (right vs left) 1.015 0.586 0.237 1.762 0.340 0.940
Septa (no vs yes) 1.976 0.465 0.001 7.194 2.899 17.857
OSI (no vs yes) 0.538 0.664 0.418 1.712 0.466 6.297
Group III: thick ≥10 mm Constant term 6.748 4.314 0.118
Age 0.123 0.074 0.075 1.139 1.043 1.274
RRH min 1.165 0.461 0.011 3.205 1.299 7.937
Sex (female vs male) 1.216 1.298 0.349 3.374 0.265 42.974
Smoker (no vs yes) 1.194 1.111 0.283 3.300 0.374 29.412
Side (right vs left) 0.369 0.988 0.708 1.447 0.209 10.000
Septa (no vs yes) 0.732 1.026 0.476 2.079 0.278 15.625
OSI (no vs yes) 1.145 1.028 0.265 3.145 0.419 23.810
Group IV: thin/≥10 mm Constant term 1.840 1.221 0.132
Age 0.003 0.018 0.883 1.003 0.968 1.038
RRH min 0.610 0.131 0.001 1.842 1.422 2.381
Sex (female vs male) 0.095 0.358 0.791 1.099 0.545 2.217
Smoker (no vs yes) 0.137 0.372 0.712 1.147 0.554 2.376
Side (right vs left) 0.236 0.346 0.496 1.266 0.642 2.493
Septa (no vs yes) 0.883 0.387 0.022 2.415 1.133 5.155
OSI (no vs yes) 1.516 0.359 0.001 4.545 2.257 9.174

largest subgroup SMP 4 (n = 47, large ≥10 mm/thin biotype), reduced
residual ridge height (p < 0.001, OR: 1.794), presence of maxillary
sinus septa (p < 0.018, OR: 2.434), and previous oral surgery interven-
tions (p < 0.001, OR: 4.425) were identified as significant risk factors
affecting SMP perforation.
3.2.2 | Scope/intensity of SMP repair mechanisms
No form of sinus membrane perforation (P1–P4) necessitated
abandonment of the intended surgical augmentation sinus proce-
dure. Using a strict treatment regimen with patches and/or sutur-
ing as described in the subgroups of SFE with different SMP
(P1–P4), all sinus membrane perforations could be repaired suc-
cessfully and were followed by sinus augmentation and simulta-
neous or delayed implant placement. From the original group
included (355 patients/434 SFE), 346 patients with 424 SFE
including 92 patients with 101 perforated sinus membranes could
be reevaluated at the 12-month postaugmentation treatment. The
drop-out rate of SFE patients with SMP (2/94 patients [2.1%] with
2/103 [1.9%] SFE) and without SMP (7/261 patients [2.7%] with
10/331 [3.0%]) may have been due to individualized reasons (mov-
ing away, not interested in follow-up). The two patients lost to
follow-up in the perforation group had large (P4: thin BT, ≥10 mm)
perforations following successful membrane repair but did not
attend further treatment.

KRENNMAIR ET AL.
T A B L E 5 Scope (severity) of sinus
SMP I (n = 27)
membrane repair (SSMR) for the four
subgroups evaluated (rating: 1 = easy to SSMR 1 24 (88.9%)
5 = very difficult/much efforts) SSMR 2 3 (11.1%)
SSMR 3 0 (0%)
SSMR 4 0 (0%)
SSMR 5 0 (0%)
Total 1.10 ± 0.32
Table 5 shows the individual scoring scale (score: 1–5) as well as
mean and standard deviations for the scope/intensity of sinus mem-
brane repairs scored for all subgroups (P1–P4). Small to moderate
sinus membrane perforations were found easy to repair and their
repair was rated with 1.11 ± 0.32 in group P1 and with 1.08 ± 0.28 in
group P2 (p > 0.999; Table 5) in the score for the scope of sinus mem-
brane repair (SSMR) without significant difference. The biggest chal-
lenge for membrane repair was associated with the highest SSMR
score in group P4 (thin biotype/large perforations; score: 4.62 ± 0.49)
significantly different to SMP1, SMP2, and SMP 3 (2.2 ± 0.55;
p < 0.001).
Multiple comparisons of the score for the scope of sinus mem-
brane repair (SSMR) between all four subgroups showed no differ-
ences between SMP1, SMP2, and SMP3 (p = 0.343, p = 0.327,
p = 0.297; Table 5), but a significant difference for all groups as com-
pared to SMP4 (p = 0.001).
4 | DISCUSSION
The findings of the present study demonstrate that classification of
sinus membrane perforations into various subtypes helps to differen-
tiate perforations with regard to their clinical relevance and appropri-
ate repair mechanism used.21–23 In numerous studies maxillary sinus
membrane perforations in SFE procedures using the LWT have pre-
dominantly been simply rated as being either present or absent, with-
out detailed descriptions of the characteristics and forms of the
membrane perforation.2–4,10–14 However, according to the current
results presented such a detailed classification in different forms of
membrane perforations might be crucial for both the repair mecha-
20–24
nism used and for the evaluation of the augmentation outcome.
In this respect, previous subselections already presented a differ-
entiation of the perforation size of the sinus membrane as being small
21,22,24,25
and large. Evaluating the impact of the membrane perfora-
tion size with respect to the augmentation and implant outcome,
Hernandez and colleagues24 and Almeida and colleagues25 reported
24
controversial results. While the study of Hernandez and colleagues
described an inverse relationship of implant success and perforation
size with the implant loss increasing with the size of the perforation,
Almeida and colleagues25 did not find any differences in the implant
success rate between large and small sinus membrane perforations.
In addition, the present findings demonstrate that not only differ-
entiation between large and small/moderate size but especially the
17088208, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/cid.13016 by Mahidol University Library and Knowledge Center, Wiley Online Library on [06/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
829
SMP II (n = 24) SMP III (n = 5) SMP IV (n = 47)
22 (91.7%) 1 (20%) 0 (0%)
2 (8.3%) 2 (40.0%) 0 (0%)
0 (0%) 2 (40%) 0 (0%)
0 (0%) 0 0% 18 (38.3%)
0 (0%) 0 (0%) 29 (61.7%)
1.08 ± 0.28 2.20 ± 0.55 4.62 ± 0.49
determination and assessment of the biotype of the perforated sinus
membrane as thick or thin membrane are of significant clinical impor-
tance.27–29 Based on the sinus membrane biotype defined, the preva-
lences of membrane perforations could be additionally assigned to
categories of harmless and meaningful for both the repair mechanism
used and for the subsequent implant placement.20,27,29 Thus, the pre-
sent findings using a defined sinus membrane subselection show that
more than 50% of all perforations seen were only of small to moder-
ate size and easy to repair. The fact that, regardless of membrane
thickness, small perforations are easy to treat and represent complica-
tions to be easily handled has also been described by Vlassis and
colleagues,31 Karabouda and colleagues,12 and Hernandez and col-
leagues24 in separate studies. In obvious contrast, the present results
clearly show that especially larger-sized perforations with thin mem-
branes represented the most common subtype of intraoperative com-
plications with an incidence of 47%. It is especially this type of
perforation that requires a specific repair mechanism and—with regard
to clinical outcome—is to be assessed and treated in a different man-
ner than harmless, small-sized perforations.21–23,31
According to these findings it can obviously be assumed that
within the general prevalence of membrane perforations found the
meaningful prevalence is significantly lower, when only the essential
and dangerous types of membrane perforation are considered and dis-
cussed.5–7,20–25 Consequently, all the general prevalences reported
seem to be considered as being excessively high with regard to their
relevance for inducing postoperative complication and influencing
clinical implant outcome.2–4,12–16
As also reported in previous studies a generalized risk factor anal-
ysis performed confirmed a significant relationship of membrane per-
foration in SFE with individual surgical/anatomic risk factors.5–7,38–42
However, for the different subgroups evaluated most risk factors
were virtually homogenous and showed no significant difference in
distribution.17–19,27–29,38 In detail and upon isolated assessment the
univariate analysis demonstrated that the patient-related risk factors
such as age, gender, and smoking habits, but also the surgery-related/
anatomic risk factors such as sinus septa, oroantral communication
and previous surgical interventions showed no significant differences
in frequencies between the subgroups.27–29,38–42 No markedly differ-
ent incidence of these risk factors could be seen in any of the sub-
groups studied suggesting that the individual risk factors can be found
in all subgroups of perforation types studied.17–19,27–29,36–40
However, only a few anatomic/surgical risk factors such as the
residual ridge height and the surgical approach (1-stage vs 2-stage)

830
presented significant differences among the four subgroups evalu-
ated.1,6,14 Risk factors as reduced residual ridge height were signifi-
cantly more frequently found in large than in small/moderate
perforations and more frequently seen with thin than with thick bio-
types. Thus, the data obtained confirm statements of Ardekian and
colleagues,13 Schwarz and colleagues,5 Becker and colleagues,36
7
and Marin and colleagues that staged SFE procedures as a result of
reduced alveolar ridge height are associated with a higher risk
of membrane perforation than simultaneous procedures. This may be
attributed to the higher sinus membrane elevation height needed in
conjunction with the higher membrane tension and the atrophic max-
1,7,15,21
illary setting present when a staged procedure is needed.
Nevertheless, in an associated multivariate risk factor analysis indi-
vidual related risk factors expressed in odds ratios represented signifi-
cant likelihood of membrane perforation for the different perforations
subpopulation involved. In particular, the interaction of risk factors must
be considered as decisive criterion for the development of large mean-
ingful perforations.6,7,20–24,38 It could be shown that previous oral surgi-
cal interventions such as tooth removal in conjunction with the
presence of sinus septa and reduced ridge height showed a significant
odds ratio for resulting in a large perforation in the thin sinus membrane
biotype.36,42–44 In addition, maxillary sinus osteotomy in conjunction
with a history of an oroantral perforation and the presence of a thin
sinus membrane also represents a significant likelihood for developing a
large meaningful perforation.1,5–7,36,38,44
According to several reports maxillary sinus membrane perfora-
tion may be associated with a loss of sinus membrane integrity and,
consequently, with an increased likelihood of postoperative compli-
cations such as sinusitis and graft infection as a result of bacterial
graft contamination migrating into the sinus cavity.2,3,11–14,45,46
2
According to previous findings of Nolan and colleagues and
5
Schwarz and colleagues, significantly more postoperative complica-
tions such as maxillary sinusitis and graft infections have been
reported in SFE with membrane perforation than in SFE without
perforation. Moreover, significantly lower implant success/survival
rates have been reported for SFEs with sinus membrane perforation
as compared to those with intact membranes in separate studies of
Khoury and colleagues,14 Prousaeff and colleagues,20 and
24
Hernandez and colleagues. In a recent systematic review including
58 studies, Al-Morraissi and colleagues16 could confirm that an
intraoperative SMP will increase the risk of implant failure after
sinus lift surgery. On the other hand, several controversial studies
have not shown any influence of sinus membrane perforation on
postoperative SFE and implant outcome.12,25,36,47
However, the present findings demonstrate that it is crucial to
consider the perforation size and also to differentiate between thick
and thin sinus membrane biotype when selecting appropriate mem-
brane repair mechanism are selected and when scheduling the time-
point of implant placement.17,27–31,36 Because sinus mucosa thickness
may vary and will be different in different sinus regions, the risk of
causing a large and dangerous membrane perforation, especially
within a thin sinus membrane, is of more interest than that for small/
moderate size in either thin or thick sinus membranes.20–22,27
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KRENNMAIR ET AL.
However, although numerous studies have reported on sinus
membrane repair mechanisms used and clinical implant outcome,
there still is a lack of information concerning a differentiation of the
repair mechanisms mentioned in relation to the perforation size with
the sinus membrane biotype present.23–29 As obviously suggested by
the present findings, small perforations of either the thin or the thick
membrane biotype can be easily repaired using the membrane
patching technique.1,5–7,30,31 In such a setting, implant placement can
be recommended in relation to the pre-existing residual ridge height
either in a simultaneous or staged procedure with appropriate antici-
pation of minor risks for complications.5–7,10–14
In addition, as shown by the current findings, thick large perfora-
tions may be sutured using end-to-end anastomosis or may be
sutured on osteotomy borders, if permitted by surgical access and
adequate skills.22,25 Successfully sutured thick membranes with addi-
tional collagen patching constitute an appropriate repair process in a
setting in which a minor risk for implant outcome is anticipated
regardless of a 1- or 2-stage procedure.7,20,22,25
However, as shown by the findings of Almeida-Heirera and
colleagues,25 Testori and colleagues,21 and Pikos23 much more clinical
effort is required for resolving the problem of a large membrane per-
foration, especially in thin sinus membranes. By evaluating the scope
of sinus membrane repair performed, the present study confirmed
that significantly more effort is needed for membrane repair in thin/
large perforations than for all other subgroups.22–25,36 This may either
be attributed to the use of more hardware such as membranes and
pins or to the prolonged surgery time and the higher clinical/surgical
efforts needed.1,5,20–25 A direct end-to-end suturing of large perfora-
tions in a thin sinus membrane is often impossible because it may lead
to additional tearing of the membrane and may often not withstand
the pull forces.21 However, as described in the current study, smart
supporting sutures on the membranes or on adjacent drill holes on the
osteotomy borders and consecutive coverage with (tacked) mem-
branes and additional use of layered collagen membranes represent
an acceptable method for repairing large/thin sinus membrane perfo-
rations.7,21,22,25 The supporting sutures will prevent the collapse of
the collagen membrane into the sinus and stabilize the collagen mem-
brane cranially.7,21,23 Nevertheless, cavity grafting is still challenging
and should be performed cautiously avoiding violation of the repaired
membrane and displacement of the graft into the sinus.2–5 As shown
by the present findings and supported by the results of previous stud-
ies, large perforations with thin membranes frequently require a
2-stage procedure regardless of residual ridge height. For this sub-
group, staged procedure seems to be advantageous and should be
proposed because it will allow second stage implant placement in a
much safer style and additionally offers the possibility of regrafting if
necessary.5–7,10–14,32–34
Within the limitations of the present study, it must be mentioned
that the prevalence of membrane perforation, especially micro-
laceration with spontaneous occlusion, may suggest a higher rate of
harmless perforations. Moreover, the present investigation does nei-
ther include the evaluation of the window osteotomy technique used
nor comparative measurements of maxillary sinus wall thickness and

KRENNMAIR ET AL.
sinus cavity angles between mesial and lateral walls influencing the
development of sinus membrane perforation.19,47–51 In addition, it is
worth mentioning that the evaluation of the complication rate follow-
ing SMP during sinus floor elevation and clinical implant outcome with
special emphasis on perforation size and membrane biotype will be
subject of an ongoing study just having been submitted.
AUTHOR CONTRIBUTIONS
Data collection, concept/design, analysis, and statistics: Stefan
Krennmair. Approval of article, concept, data collection, analysis, and
drafting: Alexander Gugenberger. Critical revision of the article and dis-
cussion: Michael Weinländer. Drafting, discussion, and interpretation:
Gerald Krennmair. Concept/design, data interpretation, analysis, and
revision: Michael Malek. Concept/design, analysis, and statistics: Lukas
Postl.
DATA AVAI LAB ILITY S TATEMENT
The data that support the findings of this study are available from the
corresponding author upon reasonable request.
ORCID
Gerald Krennmair https://orcid.org/0000-0002-9940-1300
RE FE R ENC E S
1. von Arx T, Fodich I, Bornstein M, Jensen SS. Perforation of the sinus
membrane during sinus floor elevation: a retrospective study of fre-
quency and possible risk factors. Int J Oral Maxillofac Implants. 2014;
29:718-726.
2. Nolan PJ, Freeman K, Kraut R. Correlation between Schneiderian
membrane perforation and sinus lift graft outcome: a retrospective
evaluation of 359 augmented sinus. J Oral Maxillofac Surg. 2014;72:
47-52.
3. Moreno-Vasquez JC, de Rivera ASG, Gil HS, Mifsut RS. Complication
rate in 200 consecutive sinus lift procedures: guidelines for preven-
tion and treatment. J Oral Maxillofac Surg. 2014;72:892-901.
4. Pikos MA. Complications of maxillary sinus augmentation. In:
Jensen OT, ed. The Sinus Bone Graft. 2nd ed. Chicago, IL: Quintes-
sence Books; 2006:103-113.
5. Schwarz L, Schiebel V, Hof M, Ulm C, Watzek G, Pommer B. Risk fac-
tors of membrane perforation and postoperative complications in
sinus floor elevation surgery: review of 407 augmentation proce-
dures. J Oral Maxillofac Surg. 2012;73:1275-1282.
6. Krennmair S, Malek M, Forstner T, Krennmair G, Weinländer M,
Hunger S. Risk factor analysis affecting sinus membrane perforation
during lateral window maxillary sinus elevation surgery. Int J Oral
Maxillofac Implants. 2020;35:789-798.
7. Marin S, Kirnbauer B, Rugani P, Payer M, Jakse N. Potential risk fac-
tors for maxillary sinus membrane perforation and treatment outcome
analysis. Clin Implant Dent Relat Res. 2019;21:66-72.
8. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autoge-
nous marrow and bone. J Oral Surg. 1980;38:613-616.
9. Tatum H Jr. Maxillary and sinus implant reconstructions. Dent Clin
North Amer. 1986;30:207-229.
10. Jemt T, Lekholm U. Oral implant treatment in posterior partially eden-
tulous jaws: a 5-year follow-up report. Int J Oral Maxillofac Implants.
1993;8:635-640.
11. Wallace SS, Froum SJ. Effect of maxillary sinus augmentation on the
survival of endosseous dental implants. A systematic review. Ann Per-
iodontol. 2003;8:328-343.
17088208, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/cid.13016 by Mahidol University Library and Knowledge Center, Wiley Online Library on [06/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
831
12. Karabuda C, Arisan V, Özyuvaci H. Effects of sinus membrane perfo-
rations on the success of dental implants placed in the augmented
sinus. J Periodontol. 2006;77:1991-1997.
13. Ardekian L, Oved-Peleg E, Mactei EE, Peled M. The clinical signifi-
cance of sinus membrane perforation during augmentation of the
maxillary sinus. J Oral Maxillofac Surg. 2006;64:277-282.
14. Khoury F. Augmentation of the sinus floor with mandibular bone
block and simultaneous implantation: a 6-year clinical investigation.
Int J Oral Maxillofac Implants. 1999;14:557-564.
15. Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical
complications of the sinus graft procedure and their impact on
implant survival. J Periodontol. 2004;75:511-516.
16. Al-Moraissi E, Elsharkawy A, Abotaleb B, Alkebsi K, Al-Motwakel H.
Does intraoperative perforation of Schneiderian membrane during
sinus lift surgery causes an increased the risk of implants failure? A
systematic review and meta-regression analysis. Clin Implant Dent
Relat Res. 2018;20:882-889.
17. Lin YH, Yang YC, Wang HL. The influence of sinus membrane thick-
ness upon membrane perforation during transcrestal sinus lift proce-
dure. Clin Oral Implants Res. 2016;27:612-617.
18. Yilmaz HG, Tözüm TF. Are gingival phenotype, residual ridge height
and membrane thickness critical for the perforation of maxillary
sinus? J Periodontol. 2012;83:420-425.
19. Toscano NJ, Holtzclaw D, Rosen PS. The effect of piezoelectric use
on open sinus lift perforation: a retrospective evaluation of 56 consec-
utively treated cases from private practices. J Periodontol. 2010;81:
167-171.
20. Proussaef P, Lozada J, Kim J, Rohrer MD. Repair of the perforated
sinus membrane with a resorbable collagen membrane: a human
study. Int J Oral Maxillofac Implants. 2004;19:413-420.
21. Testori T, Wallace SS, Del Fabbro M, et al. Repair of large sinus mem-
brane perforations using stabilized collagen barrier membranes: surgi-
cal techniques with histologic and radiographic evidence of successs.
Int J Periodontics Restorative Dent. 2008;28:9-17.
22. Clementini M, Ottria L, Pandolfi C, Bollero P. A novel technique to
close large perforation of sinus membrane. Oral Implantol. 2013;6:
11-14.
23. Pikos MA. Maxillary sinus membrane repair: update on technique for
large and complete perforations. Implant Dent. 2008;17:24-31.
24. Hernandez-Alfaro F, Torradeflot MM, Marti C. Prevalence and man-
agement of Schneiderian membrane perforations during sinus-lift
procedures. Clin Oral Implants Res. 2008;19:91-98.
25. de Almeida Ferreira CE, Martinelli CB, Novaes AB Jr, et al. Effect of
maxillary sinus membrane perforation on implant survival rate: a ret-
rospective study. Int J Oral Maxillofac Implants. 2017;32:401-407.
26. Froum SJ, Khouly I, Favero G, Cho SC. Effect of maxillary sinus mem-
brane perforation on vital bone formation and implant survival: a ret-
rospective stuidy. J Periodontol. 2013;84:1094-1099.
27. Janner SF, Caversaccio MD, Dubach P, Sendi P, Buser D,
Bornstein MM. Characteristics and dimension of the Schneiderian
membrane: a radiographic analysis using cone-beam computed
tomography in patients referred for dental implant surgery in the pos-
terior maxillary. Clin Oral Implants Res. 2011;22:1446-1453.
28. Rapani M, Rapani C, Ricci L. Schneider membrane thickness clas-
sification evaluated by cone-beam computed tomography and its
importance in the practability of perforation: retrospective anal-
ysis of 200 patients. Br J Oral Maxillofac Surg. 2016;54:1106-
1110.
29. Monje A, Diaz KT, Aranda L, Insua A, Garcia-Nogales A, Wang HL.
Schneiderian membrane thickness and clinical implications for sinus
augmentation: a systematic review and meta-regression analyses.
J Periodontol. 2016;87:888-899.
30. Proussaefs P, Lozada J, Kim J. Effects of sealing the perforated sinus
membrane with a resobable collagen membrane: a pilot study in
humans. J Oral Implantol. 2003;29:235-241.

832
31. Vlassis JM, Fugazzotto PA. A classification system for sinus mem-
brane perforations during augmentation procedures with options for
repair. J Periodontol. 1999;70:692-699.
32. Jensen T, Schou S, Stavropoulos A, Terheyden H, Holmstrup P. Maxil-
lary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with
autogenous bone as graft: a systematic review. Clin Oral Implants Res.
2012;23:263-273.
33. Nkenke E, Stelzle F. Clinical outcomes of sinus floor augmentation for
implant placement using autogenous bone or bone substitutes: a sys-
tematic review. Clin Oral Implants Res. 2009;20(Suppl):124-133.
34. Krennmair S, Weinländer M, Malek M, Forstner T, Krennmair G,
Stimmelmayr M. Clinical outcome of implants placed in staged maxil-
lary sinus augmentation using bovine bone mineral mixed with autog-
enous bone at three different ratios: a 5-year prospective follow-up
study. Int J Oral Maxillofac Implants. 2018;33:1351-1361.
35. Krennmair G, Ulm CW, Lugmayr H, Solar P. The incidence, location,
and height of maxillary sinus septa in the edentulous and dentate
maxilla. J Oral Maxillofac Surg. 1999;57:667-671.
36. Becker ST, Terheyden H, Steinriede A, Behrens E, Springer I,
Wiltfang J. Prospective observation of 41 perforations of the
Schneiderian membrane during sinus floor elevation. Clin Oral
Implants Res. 2008;19:1285-1289.
37. Malkinson S, Irinakis T. The influence of interfereing septa on the inci-
dence of Schneiderian membrane perforation during maxillary sinus
elevation surgery: a retrospective study of 52 consecutive lateral win-
dow procedures. J Oral Surg. 2009;2:19-15.
38. Tükel HC, Tatli U. Risk factors and clinical outcome of sinus mem-
brane perforations during lateral window sinus lifting: analysis of
120 patients. Int J Oral Maxillofac Surg. 2018;47:1189-1194.
39. Ghasemi S, Fotouhi A, Moslemi N, Chinipardaz Z, Kolahi J,
Paknejad M. Intra- and postoperative complications of lateral maxil-
lary sinus augmentation in smokers vs nonsmokers: a systematic
review and meta-analysis. Int J Oral Maxillofac Implants. 2017;32:
759-767.
40. van den Bergh JPA, ten Bruggenkate CM, Disch FJM, Tuinzing DB.
Anatomical aspects of sinus floor elevations. Clin Oral Implants Res.
2000;11:256-265.
41. Cakur B, Sümbüllü MA, Durna D. Relationship among Schneiderian
membrane, Underwood's septa, and the maxillary sinus inferior bor-
der. Clin Implant Dent Relat Res. 2013;15:83-87.
42. Bornstein MM, Wasmer J, Sendi P, Janner SF, Buser D, von Arx T.
Characteristics and dimension of the Schneiderian membrane and api-
cal bone in maxillary molars referred for apical surgery: a comparative
radiographic analysis using limited cone beam computed tomography.
J Endod. 2012;38:51-57.
17088208, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/cid.13016 by Mahidol University Library and Knowledge Center, Wiley Online Library on [06/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
KRENNMAIR ET AL.
43. Oberli K, Bornstein MM, von Arx T. Periapical surgery and the maxil-
lary sinus: radiographic parameters for clinical outcome. Oral Surg Oral
Med Oral Pathol Oral Radiol Endod. 2007;103:848-853.
44. Stacchi C, Andolsek F, Berton F, Perinetti G, Navarra CO, Di
Lenarda R. Intraoperative complications during sinus floor elevation
with lateral approach: a systematic review. Int J Oral Maxillofac
Implants. 2017;32:e107-e118.
45. Del Fabbro M, Testori T, Francetti L, Weinstein R. Systematic review
of survival rates for implants placed in the grafted maxillary sinus. Int
J Periodontics Restorative Dent. 2004;24:565-577.
46. Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of
the success of sinus floor elevation and survival of implants inserted
in combination with sinus floor elevation. J Clin Periodontol. 2008;35:
216-240.
47. Jordi C, Mukkaddam K, Lambrecht JT, Kühl S. Membrane perforation
rate in lateral maxillary sinus floor augmentation using conventional
rotating instruments and piecoelectric device—a meta-analysis. Int J
Implant Dent. 2018;29:4.
48. Barone A, Santini S, Marconcini S, Giacomelli L, Gherlone E,
Covani U. Osteotomy and membrane elevation during the maxillary
sinus augmentation procedure: a comparative study: piecoelectric
device vs conventional rotative instruments. Clin Oral Implants Res.
2008;19:511-515.
49. Monje A, Catena A, Monje F, et al. Maxillary sinus lateral wall thick-
ness and morphologic patterns in the atrophic posterior maxilla.
J Perdiodontol. 2014;85:676-682.
50. Chan HL, Monje A, Suarez F, Benavides E, Wang HL. Palatonasal
recess on medial wall of the maxillary sinus and clinical implications
for sinus augmentation via lateral window approach. J Perdiodontol.
2013;84:1087-1093.
51. Bertl K, Mick RB, Heimel P, Gahleitner A, Stavropoulos A, Ulm C. Var-
iation in bucco-palatal maxillary sinus width does not permit a mean-
ingful sinus classification. Cin Oral Implants Res. 2018;29:1220-1229.
How to cite this article: Krennmair S, Gugenberger A,
Weinländer M, Krennmair G, Malek M, Postl L. Prevalence,
risk factors, and repair mechanism of different forms of sinus
membrane perforations in lateral window sinus lift procedure:
A retrospective cohort study. Clin Implant Dent Relat Res.
2021;23(6):821–832. https://doi.org/10.1111/cid.13016