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Perforation Risk Assessment in

Maxillary Sinus Augmentation with
Lateral Wall Technique

Tiziano Testori, MD, DDS, FICD1 The events following tooth loss with
Shan-Huey Yu, DDS, MS2 consequent alveolar ridge resorp-
Lorenzo Tavelli, DDS2 tion have been thoroughly studied.1
Hom-Lay Wang, DDS, MSD, PhD2 Especially in cases with prolonged
edentulism of the posterior max-
illa, resorption of the alveolar ridge
Maxillary sinus augmentation is a procedure commonly performed in patients may also accompany maxillary sinus
in need of maxillary posterior implants with loss of vertical ridge height and pneumatization and make placing
sinus pneumatization. Previous studies have identified some factors associated dental implants very challenging
with sinus membrane perforation during lateral-wall sinus elevation procedures.
or even impossible without ad-
Although membrane perforation does not directly link to future implant failure,
it has been shown to have an association with postoperative complications. In vanced bone-grafting procedures.
order to promote more predictable results and reduce complications during the The predictability of maxillary sinus
sinus elevation procedure, especially for the lateral window approach, articles augmentation (MSA) via lateral win-
published in peer-reviewed journals were reviewed to support the proposal dow approach (LMSA) to increase
of a new risk-evaluation system prior to the sinus surgery. This article reviews alveolar bone height has been well
anatomical and patient-related factors that might affect the risk of perforation
established in the literature. Reports
during the surgery and also aims to provide a risk assessment table to enable
clinicians to analyze these factors prior to the lateral sinus augmentation surgery. of long-term success of implants
Int J Periodontics Restorative Dent 2020;40:373–380. doi: 10.11607/prd.4179 placed in an augmented sinus2,3
support the efficacy of LMSA in re-
generating bone in the maxillary
sinus cavity. However, incidence of
intra- and postoperative complica-
tions have been reported, includ-
ing membrane perforation, sinusitis,
cyst formation, wound dehiscence,
sequestration, loss of bone grafts,
excessive bleeding, and even fu-
ture implant failure.2 Among all
Section of Implant Dentistry and Oral Rehabilitation, Dental Clinic, IRCCS Galeazzi Institute,
1 complications, perforation of sinus
Milan, Italy; Department of Biomedical, Surgical and Dental Sciences, University of Milan, membrane is considered the most
Milan, Italy; Department of Periodontics and Oral Medicine, School of Dentistry, common, with an incidence rate
University of Michigan, Ann Arbor, Michigan, USA.
2Department of Periodontics and Oral Medicine, School of Dentistry, University of Michigan,
ranging between 0% to 58.3%, with
Ann Arbor, Michigan, USA. an average of 19.5%.3 Although
membrane perforation does not
Correspondence to: Dr Hom-Lay Wang, Department of Periodontics and Oral Medicine, seem to jeopardize bone forma-
University of Michigan School of Dentistry, 1011 North University Avenue,
Ann Arbor, MI 48109-1078, USA. Email: [email protected]
tion or lower implant success rate if
properly managed during the sur-
 Submitted November 8, 2018; accepted January 28, 2019.
 ©2020 by Quintessence Publishing Co Inc. gery,2 it has been demonstrated that

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374

Table 1 Risk Factors Associated with Membrane Perforation During Lateral Sinus Augmentation
Risk factors for perforation Low risk Moderate risk High risk
Anatomical factors
Sinus membrane thickness 1.5–2.0 mm 0.8–1.49 mm, 2.01–2.99 mm < 0.8 mm, > 3 mm
Presence of sinus septa Absence of septa One septum, Multiple septa or septum
height < 6 mm height ≥ 6 mm
Direction of sinus septa Mediolateral (transverse) Anteroposterior (sagittal)
Type of edentulism and Totally missing teeth Two adjacent missing teeth Single missing tooth (between
root position relative to the (from second premolar (between first premolar to second premolar to second
sinus cavity to second molar) second molar) molar); Presence of teeth at the
sinus elevation area and root
into/near the sinus lift area
Residual bone height > 4 mm < 4 mm
Sinus width (angle between Wide Angle within 30–60 degrees Narrow (angle < 30 degrees)
the lateral and the medial (angle > 60 degrees)
sinus walls)
Palatonasal recess angle Obtuse (≥ 90 degrees) Acute (< 90 degrees)
Alveolar antral artery Diameter < 1 mm Diameter 1–2 mm Diameter > 2 mm
Patient-related factors
Smoking habit No Yes
Preoperative chronic sinusitis No Yes
Gingival biotype Thick (≥ 1 mm) Thin (< 1 mm)

membrane laceration may result in Materials and Methods sive presurgical evaluation of the risk-
acute sinusitis, bone graft infection, associated parameters may help the
or dislodgement into the sinus cav- To support the proposal of the clinician to evaluate the risk of com-
ity.4 A recent article also confirmed framework for a perforation risk as- plication during MSA and, further on,
the detrimental effect of membrane sessment (PRA) in presurgical evalu- establish a plan to avoid them during
perforation on graft success.5 ation of MSA, a review of all available procedure. Table 1 summarizes the
Several factors have been re- literature was performed searching risk factors and the situation related
ported to increase the perforation MEDLINE and the Cochrane Library to low, moderate, and high risks of
risk during MSA, such as membrane databases. Articles published in perforation. Based on the presence
thickness, presence of septa, angle peer-reviewed journals were includ- of anatomical and patient-related
between lateral and medial sinus ed and reviewed to identify the risk risk factors with high risk of perfora-
walls, location of the alveolar antral factors associated with membrane tions, a PRA tool was proposed.
artery, etc.6 However, no presurgi- perforation during LMSA.
cal sinus classification based on the
perforation risk and the difficulty of Anatomy-Related Risk Factors
MSA has yet been proposed in the Perforation Risk Factors
literature. The aim of this article is to Sinus Membrane Thickness
present a comprehensive presurgi- MSA may be challenging with the According to a systematic review, av-
cal sinus assessment score based on presence of anatomical and patient- erage sinus membrane thickness is
the risk of perforation, combining related factors that have been dem- 1 mm; it should also be noticed that
evidence from the literature and the onstrated to increase the likelihood cone beam computed tomography
authors’ expertise and experience. of complications.2,6 A comprehen- (CBCT) images tend to overestimate

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 375

a b
Fig 1  (a) Thin and (b) thick sinus membrane after removal of the bony wall.

membrane thickness by 2.5 times Similar to a previous review paper, the cutoff point for clinicians to care-
compared to histologic findings.7 1.5 to 2.0 mm was also determined fully address the surgical design,
Although this article concluded that to be a favorable membrane thick- as these cases might have a higher
there is not enough evidence linking ness, while 0.8 to 1.49 mm and 2.01 membrane perforation rate.15
membrane thickness and perforation to 2.99 mm were considered normal
risks,7 several authors have reported thickness and < 0.8 mm and > 3 mm Direction of Sinus Septa
a correlation between membrane unfavorable thickness. Membrane The majority of the septa orienta-
thickness and perforation rate.8,9 thickness between 1.5 to 2.0 mm is tion observed in the sinus cavity has
Lum et al demonstrated that patients less prone to perforations6 (Fig 1). a mediolateral direction (transverse)
who experienced membrane tear- with a frequency between 59.2% to
ing during LMSA had a much thinner Presence of Sinus Septa 87.6%, while fewer patients present-
membrane (average: 0.84 mm) than The presence of sinus septa (Under- ed with septa running anteropos-
patients who did not have a perfo- wood’s septa) can be found inside terior (sagittal).13 While transverse
ration (average: 2.65 mm).8 A similar the maxillary sinus with a frequency septa can be bypassed by creating
conclusion was obtained by Pom- between 28.4% to 44.8%13 (Fig 2), two separate bony windows or by
mer et al, who investigated the me- and a study has also linked the pres- creating one large window over the
chanical characteristics of the sinus ence of sinus septa to the thinning septa, MSA in the presence of sag-
membrane, showing the advantage of the sinus membrane, which may ittal septa can be very challenging
of thicker membranes in tolerating account for a higher perforation with an increased risk of membrane
higher forces than thinner ones.10 In rate when performing MSA.14 The perforation (Fig 3).
addition, membrane thickness could presence of septa also affects the
also be affected by age (> 40 years), design of the osteotomy window Type of Edentulism and Root
but not by gender or the time at for sinus elevation.15 Single septum Position Relative to the Sinus Cavity
which the scan was taken11; and ex- is more commonly observed than The risk of membrane perforation
cessive thickness may represent a multiple septa (4.2%), with an aver- can also be associated with the type
pathologic condition, which might age height ranging between 6.3 of edentulism at the area planned
result in a higher chance of perfora- to 7.5 mm.13 In particular, Wen et al for LMSA and future implant
tion (eg, sinusitis or inflammation).12 identified a 6-mm septa height as placement. Von Arx et al showed

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376

Fig 2  (a) Sinus septum with anteroposterior

direction detected by (b) CBCT and
removed during the surgery for elevating
the sinus membrane.

a b

Fig 3  Sinus septa with mediolateral direction. A double Fig 4  A residual alveolar ridge below the sinus floor has been
antrostomy was performed to complete the procedure. related to risk of membrane perforation.

that mixed premolar-molar sites Residual Bone Height accepted that in the presence of re-
have a relatively higher perforation Two retrospective studies report- duced bone height, particularly less
rate (41.2%) than premolar sites ed an increased risk of membrane than 4 mm, there might be a higher
(16.7%) or molar sites (26.2%).16 perforation when the patients pre- chance of membrane perforation
Moreover, more challenging situa- sented with a residual ridge height during MSA6,9 (Fig 4).
tions arise from cases with a single less than 4 mm.16,17 However, a
missing tooth; in these conditions, 7-times–higher perforation risk has Sinus Width
the membrane elevation could have been shown in patients with residual Cho et al showed that a narrow sinus
a higher risk of perforation due to bone height of 3 to 6 mm compared anatomy could relate to increased
the elevation area being closer to to patients with less than 3 mm of perforation risk. When the angle be-
adjacent teeth roots or the thicker bone height.5 Despite the conflict- tween the lateral and medial walls of
lateral wall of the sinus.6 ing results presented, it is generally the sinus is < 30 degrees, the risk of

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 377

Fig 5  A CBCT scan shows a wide maxillary sinus with an angle of Fig 6  A CBCT scan shows the palatonasal recess, defined as
approximately 44 degrees between the lateral and medial walls. the angle between the roof of the hard palate and the lateral
wall of the nasal cavity.

Fig 7  A large-diameter alveolar antral

artery in the area of the antrostomy that
was isolated and elevated together with
the membrane.

membrane tearing was found to be Palatonasal Recess Angle from the alveolar ridge. In a CBCT
higher (62.5%), compared to sinuses The palatonasal recess is defined as study, the incidence of an acute
with an angle between 30 to 60 de- the angle between the roof of the palatonasal recess was found to be
grees or even wider sinuses (> 60 hard palate and the lateral wall of 15%, 8.2%, and 2.4% at the second
degrees), where the perforation rate the nasal cavity20 (Fig 6). An acute premolar, first molar, and second
decreased to 0% to 28.6%18 (Fig 5). angle of the palatonasal recess molar sites, respectively.20
In addition, it has been shown that could increase the complexity and
a narrow sinus morphology is more difficulty when performing MSA Alveolar Antral Artery
often found in the second premolar and limit the height of elevation, The infra-osseous anastomosis of
area, where the elevation may be especially if the acute recess angle the posterior superior alveolar artery
more prone to perforation.19 is presented less then 15 mm away and the infraorbital artery has been

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378

Perforation Risk Assessment

Table 2 Perforation Risk Assessment
Risk Definition Based on the reviewed literature
Unlikely All conditions meet low risk of perforation or and the expertise of the present
< 3 conditions at moderate risk
authors, an assessment tool with
Possible One condition at high risk of perforation or low, moderate, and high perfora-
≥ 3 conditions at moderate risk
tion risks were identified for each
Likely At least two conditions at high risk of perforation of the previously discussed factors
(Table 1). When all the anatomical
and patient-related risk factors meet
defined as alveolar antral artery has to be taken into account when low risk of perforation or when less
(AAA)21 (Fig 7). It has been shown designing the bony window, as well than three conditions are at moder-
that the intraosseous anastomosis is as its distance from the alveolar crest ate risk, then perforation is unlikely.
always present, while the extraosse- or sinus floor (11.25 to 26.9 mm and In the presence of one condition at
ous anastomosis only exists in 44% 5.8 to 10.4 mm, respectively).25 a high risk of perforation or when at
of cases.21 Injury to the AAA during least three conditions at a moderate
MSA may result in bleeding that may risk, the perforation is considered
impair the visualization of the mem- Patient-Related Factors possible. Similarly, when more than
brane during the detachment, there- one risk factor is found to be at a
fore increasing the risk of membrane Patient-related factors may affect high risk of perforation, the perfora-
laceration. According to Rosano et the risk of intra- and postopera- tion is likely (Table 2).
al, the AAA can display three differ- tive complications. Among all the
ent patterns: completely intraosse- factors, a smoking habit has been
ous, partially intraosseous, or under associated with higher incidence Discussion
the periosteum of the lateral sinus of perforation and postoperative
wall. In particular, at the area from complications, such as sinusitis Membrane perforations during
second premolar to second molar, and wound dehiscence.17 However, MSA have been correlated with
the AAA is commonly found to be whether smoking affects implant an increased risk of postoperative
adjacent to the sinus membrane with survival in an augmented sinus re- complications.4,5 An acute or chron-
no bony layer interposed between mains controversial.26 It has been ic sinus inflammation, bacterial con-
the vessel and the membrane.22 reported that sex, similar to age, is tamination, and graft infections may
Based on CBCT scans, it was report- not related to increased membrane jeopardize the success of MSA.4–6
ed that in 62.2% of cases the diam- perforation.5 However, one study Furthermore, despite the fact that
eter of the AAA is less than 1 mm, concluded that preoperative chron- membrane perforation is not an ab-
while the remaining 37.8% exhibited ic sinusitis might be a significant solute contraindication to continue
a diameter of greater than 1 mm.23 cause of postoperative infection the procedure, it may prompt the
Another study also showed that a and implant loss, suggesting an ap- clinician to abort the surgery, partic-
diameter ≥ 2 mm was found in only propriate treatment of this condition ularly if the size of the perforation is
4.3% of the cases.22 An AAA with a before MSA.27 Lastly, Yilmaz and substantial. Several techniques have
diameter between 0.5 to 1 mm ac- Tözüm discovered a strong corre- been proposed to manage sinus
counts for intraoperative bleeding lation between gingival phenotype membrane perforation.28 However,
in about 10% of the cases, while the and membrane thickness, yet only a it seems that it is the dimension of
likelihood of hemorrhage is around moderate correlation was observed the perforation rather than the re-
57% when the AAA diameter is 1 to between gingival phenotype and pairing technique that affects the
2 mm.24 The location of AAA also membrane perforation.9 outcomes. Although membrane

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 379

perforations do not necessarily re- Conclusions   6. Tavelli L, Borgonovo AE, Re D, Maiorana

sult in postoperative complications C. Sinus presurgical evaluation: A lit-
erature review and a new classification
or affect the survival rate of future The presented assessment tool of- proposal. Minerva Stomatol 2017;66:
placed implants,2 there is no doubt fers a feasible method of assessing 115–131.
 7. Monje A, Diaz KT, Aranda L, Insua
that avoiding perforation will re- the risk of perforation during LMSA A, Garcia-Nogales A, Wang HL.
duce the time of the surgery and based on the presurgical evalua- Schneiderian membrane thickness and
increase the likelihood of achieving tion of key factors related to mem- clinical implications for sinus augmen-
tation: A systematic review and meta-
an uneventful healing. In addition, it brane tearing. Prospective clinical regression analyses. J Periodontol 2016;
has been speculated that the mem- studies are necessary to validate 87:888–899.
  8. Lum AG, Ogata Y, Pagni SE, Hur Y. As-
brane periosteum may possess the the proposed risk of perforation sociation between sinus membrane
cells that have the capacity for bone risk assessment. thickness and membrane perforation
regeneration and that membrane in lateral window sinus augmentation: A
retrospective study. J Periodontol 2017;
tearing may reduce the amount of 88:543–549.
regeneration.29 On the other hand, Acknowledgments  9. Yilmaz HG, Tözüm TF. Are gingival
phenotype, residual ridge height, and
placing a collagen membrane over membrane thickness critical for the per-
the perforation was shown to be The authors do not have any financial in- foration of maxillary sinus? J Periodontol
an effective technique for repairing terests, either directly or indirectly, in the 2012;83:420–425.
products or information listed in the paper. 10. Pommer B, Unger E, Sütö D, Hack N,
membrane tearing.28 Watzek G. Mechanical properties of the
This paper was partially supported by the
The present article discussed Schneiderian membrane in vitro. Clin
University of Michigan Periodontal Graduate Oral Implants Res 2009;20:633–637.
the main factors that have proved to Student Research Fund. 11. Zimmo N, Insua A, Sinjab K, Chan HL,
be associated with an increased risk Shaikh L, Wang HL. Impact of sex, age,
of membrane perforation, identify- and season on sinus membrane thick-
ness. Int J Oral Maxillofac Implants
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380

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