Management of Schneiderian membrane perforations during

REVIEW Open Access

Management of Schneiderian membraneperforations during maxillary sinus flooraugmentation with lateral approach inrelation to subsequent implant survivalrates a systematic review and meta-analysisLuis Alfredo Diacuteaz-Olivares Jorge Corteacutes-Bretoacuten Brinkmann Natalia Martiacutenez-RodriacuteguezJoseacute Mariacutea Martiacutenez-Gonzaacutelez Juan Loacutepez-Quiles Isabel Leco-Berrocal and Cristina Meniz-Garciacutea

Abstract

Background This systematic review aimed to propose a treatment protocol for repairing intraoperative perforationof the Schneiderian membrane during maxillary sinus floor augmentation (MSFA) procedures with lateral windowtechnique In turn to assess subsequent implant survival rates placed below repaired membranes compared withintact membranes and therefore determine whether membrane perforation constitutes a risk factor for implantsurvival

Material and methods This review was conducted according to PRISMA guidelines Two independent reviewersconducted an electronic search for articles published between 2008 and April 30 2020 in four databases (1) TheNational Library of Medicine (MEDLINEPubMed) via Ovid (2) Web of Science (WOS) (3) SCOPUS and (4) CochraneCentral Register of Controlled Trials (CENTRAL) also a complementary handsearch was carried out The Newcastle-Ottawa Quality Assessment Scale was used to assess the quality of evidence in the studies reviewed

Results Seven articles fulfilled the inclusion criteria and were analyzed A total of 1598 sinus lift surgeries wereincluded allowing the placement of 3604 implants A total of 1115 implants were placed under previouslyperforated and repaired membranes obtaining a survival rate of 9768 while 2495 implants were placed belowsinus membranes that were not damaged during surgery obtaining a survival rate of 9888 The rate ofSchneiderian membrane perforation shown in the systematic review was 306 In the articles reviewed the mostwidely used technique for repairing perforated membranes was collagen membrane repair

Conclusions Schneiderian membrane perforation during MFSA procedures with lateral approach is not a risk factorfor dental implant survival (p=0229 RR 0977 95 CI 0941-1015) The knowledge of the exact size of themembrane perforation is essential for deciding on the right treatment plan

Keywords Alveolar ridge atrophy Bone augmentation Lateral approach Maxillary sinus floor elevation Systematicreview

copy The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 40 International Licensewhich permits use sharing adaptation distribution and reproduction in any medium or format as long as you giveappropriate credit to the original author(s) and the source provide a link to the Creative Commons licence and indicate ifchanges were made The images or other third party material in this article are included in the articles Creative Commonslicence unless indicated otherwise in a credit line to the material If material is not included in the articles Creative Commonslicence and your intended use is not permitted by statutory regulation or exceeds the permitted use you will need to obtainpermission directly from the copyright holder To view a copy of this licence visit httpcreativecommonsorglicensesby40

Correspondence jcortesbucmcomDepartment of Dental Clinical Specialties Faculty of Dentistry ComplutenseUniversity of Madrid Pza Ramon y Cajal sn 28040 Madrid Spain

International Journal ofImplant Dentistry

Diacuteaz-Olivares et al International Journal of Implant Dentistry (2021) 791 httpsdoiorg101186s40729-021-00346-7

IntroductionMaxillary sinus floor augmentation (MSFA) surgery withsimultaneous or deferred placement of implants is ahighly predictable surgical technique in cases of atrophicposterior maxilla [1] allowing implant-supported re-habilitation in cases where there would otherwise be in-sufficient remaining bone substrate for implantplacement MSFA achieves implant survival rates similarto those achieved in pristine bone [2 3] During this sur-gical procedure perforations of the sinus membranemay occur due either to iatrogenic causes derived fromincorrect surgical handling or to anatomical consider-ations inherent to the individual patient which canmake the procedure difficult [4 5] The former includeuncontrolled pressure on the membrane or the use ofinappropriate surgical instruments [6] the latter includereduced thickness of the membrane [7] reduced friabil-ity and elasticity [8 9] greater adhesion to the bone sur-face [10] and the presence of the sinus septa [11ndash13]Membrane perforation is the most frequent complica-

tion in this type of procedure [14] According to thevarious authors reviewed percentages vary between 7and 60 [12 15ndash18]In most cases this complication is corrected intra-

operatively [19] However the treatments described torepair these perforations are diverse [20]To our knowledge no systematic review has attempted

to propose specific treatment guidelines in relation toperforation size Therefore this systematic review aimedto answer following statement of questions What is therate of Schneiderian membrane perforation duringMSFA procedures What is the survival rate of dentalimplants placed in perforated membranes once theyhave been repaired compared with the survival rate inintact membranes How are these perforations treated(depending on their extent) What are the most fre-quently occurring complications following membraneperforation

Material and methodsDatabases and search strategyThis systematic review was designed to fulfill PRISMA[21] (Preferred Reporting Items for Systematic Reviewand Meta-Analyses) guidelines and answer the followingfocused PECO question ldquoHow are Schneiderian mem-brane perforations that occur during maxillary sinusfloor augmentation (MSFA) with lateral approach man-aged and does perforation influence subsequent implantsurvival ratesrdquo(P) Patientpopulation Adult human patients requir-

ing maxillary sinus floor augmentation with lateral ap-proach for subsequent placement of dental implants(E) Exposure Repairing sinus membrane perforations

during maxillary sinus floor augmentation

(C) Comparison Maxillary sinus floor augmentationwithout membrane perforation(O) Outcomes Schneiderian membrane perforation

rate during MSFA with lateral approach available thera-peutic procedures for repairing these perforations asso-ciated complications of Schneiderian membraneperforations survival rates of implants in perforated vsnon-perforated membranesAn electronic search was conducted in four electronic

databases (1) The National Library of Medicine (MEDLINEPubmed) via Ovid (2) Web of Science (WOS) (3)Cochrane Central Register of Controlled Trials (CENTRAL) and (4) Scopus The search included studies pub-lished in English Spanish and German published be-tween 2008 and April 30 2020 The electronic searchwas complemented by a manual search in Oral andMaxillofacial Surgery and Implant Dentistry related jour-nals and in the reference sections of the studiesreviewed To perform the screening process all the ref-erences were included into EndNote X9 Library (Clari-vate Analytics Philadelphia PE USA)The search used the following key terms combined

with Boolean operators (Table 1) (maxillary sinus flooraugmentation OR dental implant) AND (sinus lift sur-gery OR membrane perforation) AND (management ofSchneiderian membrane perforations) AND (sinus mem-brane perforation OR dental implant) AND (maxillarysinus membrane repair) AND (Schneiderian membranerepair OR maxillary sinus floor augmentation) AND (re-pair system for sinus membrane perforations)Two reviewers (LADO and JC-BB) conducted the pri-

mary selection of the articles identified in the electronicand manual search by independently screening the titlesand abstracts The same reviewers selected the full man-uscripts of studies that met the inclusion criteria orthose with insufficient data in the title and abstract toreach a clear decision Any disagreement between the re-viewers was resolved by discussion with a third reviewer(CMG) Inter-reviewer reliability (percentage of agree-ment and kappa correlation coefficient) in full-text ana-lysis was calculatedThe same two reviewers performed data extraction in-

dependently in duplicate Where data were incompleteor missing from a study the authors were contacted forclarification When the results of a study were publishedmore than once only the longest follow-up wasincluded

Inclusion and exclusion of studiesThe following inclusion criteria were applied

1 Clinical studies reporting number of patientsincluded number of sinus lifts performed number

Diacuteaz-Olivares et al International Journal of Implant Dentistry (2021) 791 Page 2 of 13

of perforations produced during sinus lifts dentalimplant survival rates

2 Randomized controlled clinical trials cohortstudies and case-control studies

3 Human studies with sample sizes greater than 154 MSFA procedures using the lateral window

technique5 Studies involving both perforated and non-

perforated membranes6 Studies reporting the therapeutic options adopted

to resolve the membrane perforation7 Follow-up of at least 6 month8 Articles published in English German or Spanish

The following criteria lead to exclusion

1 Non-human studies2 Articles not in English German or Spanish3 Studies for which the full text was not available4 Case reports

Data extractionData from each included article was collected by the re-viewers (LADO and JC-BB) working together and re-corded in an Excel sheet (Version 1517 Microsoft Inc2015) including the following parameters authors yearof publication study design number of patients numberof MSFA occurrence of membrane perforation duringMSFA procedures applying the lateral window tech-nique perforation rate perforation size number of im-plants the subsequent survival rates of implants placed

below perforated vs non-perforated membranes treat-ments used to repair sinus perforations and any add-itional complications produced in sinus lift surgerieswith repaired membranes

Risk of bias assessment within the studiesThe Newcastle-Ottawa scale (NOS) for cohort studies[22] was used to assess risk of bias in individual observa-tional studies and non-randomized trials adapted byMoraschini et al [23] in 2017 This scale included aquestionnaire divided into 3 categories selection (4questions) comparability (2 question) and exposure (3questions) The resulting score can reach a maximum ofnine points Studies were classified as good fair orpoor-quality (GQ FQ or PQ) following the score algo-rithm proposed by the Agency for Healthcare Researchand Quality [24]

Statistical analysisData describing Schneiderian membrane perforationmanagement perforation rate and complications associ-ated with perforation were entered on a spreadsheet fordata analysis The relationship between perforation sizeand implant survival was also analyzedStatistical analysis was performed using the STATAcopy

program (Version 15) The results for the survival rate ofimplants inserted below perforated membranes com-pared to the survival rate of implants inserted belownon-perforated membranes were compared by means ofmeta-analysis assuming a random effects model Datawere entered on a spreadsheet to perform the meta-

Table 1 Information about search strategy based on PECO question and MeSH index terms Boolean terms and its truncations

Focused question (PECO) How are Schneiderian membrane perforations that occur during maxillary sinus floor augmentation (MSFA) withlateral approach managed and does perforation influence subsequent implant survival rates

P (Population) Adult human patients requiring maxillary sinus flooraugmentation with lateral approach for subsequent

placement of dental implants

1 (maxillary sinus floor augmentation OR membraneperforation) AND (dental implant)

E (Exposure) Repairing sinus membrane perforations during maxillarysinus floor augmentation

2 (sinus lift surgery OR membrane perforation ORmanagement of Schneiderian membrane perforationsOR repair system for sinus membrane perforations) AND(dental implant)

C (Comparison) Maxillary sinus floor augmentation without membraneperforation

3 (maxillary sinus floor augmentation OR sinus liftsurgery) AND (dental implant)

O (Outcome) Schneiderian membrane perforation rate during MSFAwith lateral approach available therapeutic proceduresfor repairing these perforations associatedcomplications of Schneiderian membrane perforationssurvival rates of implants in perforated vs non-perforated membranes

4 (implant survival rate OR complication OR outcome)

Search combination PubmedWeb of Science Cochranelibrary and Scopus

1 AND 2 AND 3 AND 4

Terms truncation PubmedWeb of Science Cochranelibrary and Scopus

(maxillary sinus floor augmentation OR dental implant) AND (sinus lift surgery OR membrane perforation) AND(management of Schneiderian membrane perforations) AND (sinus membrane perforation OR dental implant) AND(maxillary sinus membrane repair) AND (Schneiderian membrane repair OR maxillary sinus floor augmentation)AND (repair system for sinus membrane perforations) AND (implant survival rate OR complication OR outcome)

analysis with two outcome categories perforated vsnon-perforated membranes The measure of effect usedwas the risk ratio (RR) or relative risk which constitutesthe relative measure of effect by indicating how muchmore often the event tended to develop in the group ofsubjects exposed (perforated membrane) to the exposurefactor or risk factor in relation to the non-exposed group(non-perforated membrane)Heterogeneity was evaluated using the chi2 test and

the I2 statistic The significance level was set at p 005and 95 confidence interval (CI)

ResultsScreening processThe initial electronic search for the management ofSchneiderian membrane perforation during MSFA pro-cedures applying the lateral window technique located642 articles Duplicates were discarded and the titles andabstracts screened applying inclusion and exclusion cri-teria leaving a total of 56 articles Of these 27 articleswere excluded because they were in vitro ex vivo stud-ies or case reports or because their content was irrele-vant to the present reviewrsquos objectives (Table 2) A totalof 29 articles were selected for full reading After a thor-ough analysis 22 articles were excluded and so sevenstudies were included in qualitative and quantitative syn-thesis A flow chart (Fig 1) illustrates the entire searchand selection process

Study characteristicsThe seven articles selected for qualitative and quantita-tive synthesis were retrospective cohort studies pub-lished between 2008 and 2020 Table 3 summarizes theinformation extracted from each study authors year ofpublication type of study number of patients treatednumber of MSFA with lateral approach performednumber of perforations produced during surgery per-centage of perforations recorded management of theperforation performed and the main complicationsfound in cases in which Schneiderian membrane perfor-ation occurred

Table 4 details the total number of implants placed ineach study the number of implants placed below perfo-rated membranes the number of implants placed belownon-perforated membranes the survival rates () of im-plants placed under intact and perforated membranesand main follow-up of each studyTable 5 shows the results of qualitative and quantita-

tive synthesis of the studies analyzed It was found thatas the size of the Schneiderian membrane perforationsincreased so did the failure rate of the implants placedbelow perforated membranes Only one study Beck-Broichsitter et al did not report the size of the perfora-tions adjacent to failed implants [47]

Patient characteristicsA total of 1162 patients with an average age of 56 yearsundergoing 1598 MSFA procedures with lateral windowapproach were recruited in the seven studies The meanSchneiderian membrane perforation rate was 306 (489perforations) Different treatments were used to resolvethe perforations including post-perforation clot forma-tion [4] suturing [47] use of collagen membranes [16]Platelet-rich fibrin (PRF) [19] hemostatic agents [49]laminar bone [50] and block grafts [50]Of the treatments carried out it was observed that col-

lagen membrane was the most commonly used materialfor repairing membrane perforation regardless of itssize This material was used in four of the seven articlesreviewedThe most common post-operative complication found

in sinuses with perforated membranes was the appear-ance of signs of infection Park et al [4] reported agreater number of postoperative complications in pa-tients with perforated membranes including bleedingfrom the perforation site leakage of cystic fluid or puru-lent exudate displacement of the graft into the sinusnasal bleeding and facial swelling Other complicationswith lower incidence such as pain or tenderness in thetreated area were also reported [4]A total of 1598 MSFAs with lateral window technique

were performed followed by the placement of 3604 den-tal implants A total of 1115 implants were placed

Table 2 Articles excluded and reasons for exclusion

Reason for exclusion Study

Ex vivo studyexperimental study Yanfeng Li et al [25] Zhai et al [9] Alsabbagh et al [26]

A case report Xiaojun Ding et al [27] Huang et al [28] Testori et al [29] Taschieri et al [30] Pikos [31]Meleo et al [32] Gehrke et al [33] Fathima et al [34] Bassi et al [35]

No report implant survival rate under membraneperforation vs non perforation

Dragonas et al [36] Sakkas et al [37] De Oliveira H et al [38] Shiffler et al [17] Chirilă et al[39] Barbu et al [5] Starch-Jensen et al [3] Riben et al [40]

Only patients with perforated membranes wereincluded

Kim et al [41] Nooh et al [42]

No lateral approach (solely) Chaushu et al [43] Yoko Oba et al [44] Giudice et al [45] Attar et al [46] Becker ST et al[12]

Fig 1 PRISMA flowchart containing the search strategy and the respective selection process

Table 3 Information about selected studies including number of patients treated number of MSFA performed number ofperforations percentage of perforations recorded management of the perforation performed and main complications

Authoryear Type ofstudy

Patients(number)

Sinus lift(number)

Perforations(number)

Perforationsrate

Management of perforations Complications

Park et al [4] Retrospectivecohort

63 65 24 39 Clot formation Infection

Beck-Broichsitteret al [47]

Retrospectivecohort

63 79 39 493 lt5 mm collagen memb or fibringlue or clotgt5 mm suturing + collagen memb

Periimplantitis

Ferreira et al[16]

Retrospectivecohort

531 745 237 318 Collagen membr + Reabsorbablesuture for all perforations

Areas with chronicinflammatory infiltration

Oumlncuuml E et al[19]

Retrospectivecohort

16 20 10 50 PRF (lt10 mm )

Froum et al[48]

Retrospectivecohort

23 40 15 375 Resorbable collagen membrane (lt10 mm)

Oh E et al[49]

Retrospectivecohort

128 175 60 34 Resorbable hemostatic agenteSurgicelcopy (small-moderateperforations)

Infection in 3 of the 60perforations

Hernaacutendez-Alfaro et al[50]

Retrospectivecohort

338 474 104 22 0-5 -collagen membr o suturing 5-10 -collagen membr + laminarbonegt10 -laminar bone buccal fatpad mandibular bone block

Painsensitivity

Total 1162 1598 489 306 The main treatment was collagenmembrane

Infection was themost frequentcomplication

beneath previously perforated and repaired membranesobtaining a survival rate of 9768 while 2495 implantswere placed under intact sinus membranes obtaining asurvival rate of 9888The survival criteria for dental implants in the seven

articles reviewed were as follows loaded implants whichremained in situ without presenting mobility free ofradiotranslucency and peri-implant infection and with-out associated pain (whether spontaneous or underpressure)After loading the implants the mean follow-up time of

the patients (1162) in the seven studies ranged from 6 to32 months

Inter-reviewer agreementThe inter-reviewer Kappa statistic between the two re-viewers (LADO and JC-BB) was 0856plusmn0072 (CI 950716-0997)The intervention of a third reviewer for consensus

purposes was not needed

Risk of biasThe Newcastle-Ottawa scale [22] allowed to classify thestudies included in the systematic review as follows 2studies [48 50] scored 7 points and 3 studies [4 47 49]scored 6 points This indicates a low risk of bias andhigh methodological quality Only one study [19] scored5 points (Table 6)

Meta-analysisDue to the existence of heterogeneity among the fivestudies included in meta-analysis a random effectsmodel was used to relate the survival of dental implantsplaced below repaired membranes and implants placedbelow intact membranes (I2=848 p=0000 chi2=2635p=0000) The studies by Park et al and Oumlncuuml E et alwere not included in meta-analysis as they reported100 survival rates for both perforated and non-perforated membranes [4 19] There was no statisticallysignificant difference between the groups (p=0229) witha RR of 0977 (95 CI 0941-1015) (Table 7 Fig 2)

Table 4 Information about total number of implants placed number of implants placed below perforated membranes number ofimplants placed below non-perforated membranes and their survival rates () and mean follow-up period of each study

Authoryear Implants(number)

Implants inserted underperforated membranes(number)

Implants inserted underintact membranes(number)

Implant survival ratein perforatedmembranes

Implant survivalrate in intactmembranes

Mean follow-up (months)

Park et al[4]

122 44 78 100 100 Perforationgroup 1152(plusmn66)Controlgroup 1038(673)

175 92 89 989 100 Perforationgroup 31 (plusmn24)Controlgroup 20 (plusmn18)

Ferreiraet al [16]

1588 523 1065 971 977 Perforationgroup 24Controlgroup 24

35 15 20 100 100 Perforationgroup 6-12Controlgroup 6-12

Froum et al[48]

80 35 45 100 955 Perforationgroup6-32Controlgroup 6-32

Oh E et al[49]

438 134 304 9701 99 6-32

1166 272 894 9081 100 12

Total 3604 1115 2495 9768 9888

Table 5 Correlation between the size of the Schneiderian membrane perforations and the failure rate of the implants placed belowperforated membranes

Authoryear Perforationsize (inmm)

Implant failure rate (in perforated membranes) Management of Schneiderianmembrane perforations

Park et al [4] lt55-10gt10

0 (0 de 44) (not specified where each implant was inserted) Clot formation

lt5gt5

109 (1 de 92) (not specified the size of the perforations where the implant fails) lt5 mm collagen membrane orfibrin glue or clotgt5 mm suturing + collagenmembrane

Ferreira et al[16]

lt55-10gt10

23 (6 de 266)27 (4 de 150)47 (5 de 107)

Collagen membrane +reabsorbable suture for allperforations

lt10 0 (0 de 15) PRF (lt10 mm )

Froum et al[48]

lt10 0 (0 de 35) Resorbable collagen membrane (lt10 mm )

Oh E et al[49]

5-10 3 (4 de 134) Resorbable hemostatic agenteSurgicelcopy (small-moderateperforations)

lt55-10gt10

286 (4 de 140)811 (6 de 74)2514 (15 de 58)

0-5 mdashCollagen membrane or(please add r) suturing5-10 mdashCollagen membrane +laminar bonegt10 mdashLaminar bone buccal fatpad mandibular bone block

Table 6 Quality assessment of included studies using the Newcastle-Ottawa scale

Parket al [4]

Ferreiraet al [16]

Oumlncuuml Eet al [19]

Froumet al [48]

Oh Eet al[49]

Hernaacutendez-Alfaro et al [50]

Selection

bull Representativeness of the exposed cohort 0 0 0 0 0

bull Selection of the non-exposed cohort

bull Ascertainment of exposure

bull Demonstration that outcome of interest wasnot present at start of study

Comparability

bull Study controls for bone ring group 0 0 0 0 0 0 0

bull Study controls for any additional factor(duration of exposure)

Outcome

bull Assessment of outcome 0 0 0 0 0 0

bull Was follow-up long enough for outcomesto occur

bull Adequacy of follow-up of cohorts

Newcastle-Ottawa scale 6 6 6 5 7 6 7

0 noYes

Publication biasThe Eggerrsquos test (Table 8) generates a p value less than010 this is interpreted as suspected publication bias[50] The present systematic review obtained a p value of0739 (gt005) indicating that small study effects did notinfluence the results of meta-analysis

DiscussionEver since Braumlnemark discovered osseointegration in the1950s numerous surgical techniques have been pro-posed for rehabilitating atrophic maxillae with dentalimplants [51] In the absence of remaining bone in themaxillary posterior sectors MSFA procedures may be

Table 7 Statistical analysis of the included studies reflecting the risk ratio when comparing the implant survival rate in perforatedand non-perforated membranes

Study RR [95 Conf interval] Weight

Beck-Broichsitter et al [47] 0989 0960 1020 2194

Ferreira et al [16] 0994 0977 1011 2427

Froum et al [48] 1043 0963 1129 1192

Oh E et al [49] 0980 0949 1011 2163

Hernaacutendez-Alfaro et al [50] 0907 0873 0942 2024

Park et al [4] [Excluded]

Oumlncuuml E et al [19] [Excluded]

D+L pooled RR 0977 0941 1015 10000

Random-effects modelHeterogeneity p = 0000 I2 = 848Heterogeneity chi-squared = 2635 (df = 4) p = 0000I-squared (variation in RR attributable to heterogeneity) = 848 estimate of between-study variance Tau-squared = 00014Test of RR= 1 z= 120 p = 0229

Fig 2 Forest plot illustrating the results in terms of implant survival rate from meta-analysis A random effects model was used

performed with lateral window approach in order toallow implant placement either simultaneously or subse-quently [52]Maintaining the integrity of the Schneiderian membrane

and sealing any perforations are critical to the success ofthis procedure [5 53 54] Membrane perforation is a rela-tively frequent intraoperative event in the course of MSFAprocedures with lateral window technique [17 55] to theextent that they are considered the most frequent compli-cation in this type of surgery (7-60) [15 56]Therefore it is essential to minimize the risk of intra-

operative complications during sinus lift procedures bycarrying out a preliminary study of any factors thatmight increase that risk including the general health ofthe sinus endosseous anastomosis at the osteotomy sitelateral wall thickness Schneider membrane thicknessresidual bone crest height the timing of subsequent im-plant insertion and cortication of the sinus floor [57]The present systematic review included total of 1162

patients who underwent 1598 lateral access MSFA pro-cedures suffering a mean perforation rate of 306 (489perforations)The literature proposes numerous treatments to re-

solve these perforations Nevertheless although MSFAprocedures are well-known and fairly commonplace noevidenced-based guidelines for perforation closure orclear indications of when to interrupt these procedureshave been established [47]Among the treatments reported the most widely used

technique in the studies reviewed was collagen mem-brane repair although this was managed in differentways While Ferreira et al [16] placed a collagen mem-brane over the perforation and stabilized it with tacks tocontain the graft material Froum et al [48] performedthis repair using two separate bioabsorbable membranesHowever collagen membranes have several drawbacks

and so other therapeutic alternatives are currently beingexplored In this way De Oliveira et al [38] assert thatthe resorbable membrane influences the intensity of in-flammatory responses producing a reduction in boneformation which compromises the primary stability dur-ing the placement of the implants Nevertheless itshould be noted that a recent systematic review ofMonje et al [58] failed to identify a statistically signifi-cant relationship between the implant mechanical

(primary) stability and the implant survival rate Simi-larly Testori et al [29] established that in the case oflarge perforations the use of a collagen membrane runsa risk of displacement when the graft material is placedso that the material is not adequately contained There-fore they recommend that the membranes used for therepair should cover the perforation and the surroundingarea and have sufficient rigidity even when wet to avoidtheir collapse through the perforationA predictable two-stage approach technique to man-

age large perforations has been described recently in acase series by Dagba et al [59] These authors argue thatwhen a large perforation occurs further elevation of themembrane should be avoided and a collagen sponge canbe folded and placed at the perforation site which actsas a space maintainer and provides a scaffold for cell re-cruitment to the wounded area The sinus augmentationprocedure is then delayed by 3-6 weeks after repair ofthe perforation [57] This timeframe allows the mem-brane to heal facilitating re-entry [60]Choi et al [61] found that the use of fibrin glue for

membrane repair leads to a newly formed continuous epi-thelium In contrast collagen membrane-treated perfora-tions show extensive fibrosis inflammatory infiltrationand an absence of epithelium [62 63] Oumlncuuml E et al [19]used PRF to treat membrane perforations as this has au-togenous characteristics and is an inexpensive bioactivematerial Activated platelets slowly release a wide range ofproteins and growth factors (BMPs PDGFs IGFs VEGFTGF-b1 TGF-b2) which act on the bone healing processand control both inflammatory response and infectiousprocesses [64 65] Other authors [19 50] have proposedsuturing the membrane with resorbable material How-ever in addition to the inherent difficulty of the proced-ure this technique is only recommended as a singletreatment in perforations of up to 5 mm due to limited ac-cess and the friability of the membrane [12 38 50] Parket al [4] observed that the simple formation of a bloodclot after perforation did not lead to unfavorable clinicaland radiographic results Testori et al [29] postulated thatsmall perforations can be self-repairing providing thesinus membrane folds back on itselfThis systematic review showed that knowledge of the

exact size of the membrane perforation is essential fordeciding on the right treatment plan Although a widevariety of treatments have been reported a series ofguidelines can be followed Once the membrane perfor-ation has been made it is necessary to complete theMSFA without further enlargement of the perforationWhen the procedure is terminated the size of the per-foration will determine the treatment needed and thematerial requiredThe results of our review showed that implants

inserted below repaired membranes (9771) had a

Table 8 Eggerrsquos test

Std eff Coef Std err t Pgt|t| [95 Conf interval]

Slope 995262 0384472 2589 0000 8729058 1117618

Bias minus9743203 20667276 minus037 0739 minus9462784 7514143

Eggerrsquos test for small-study effects Regress standard normal deviate ofintervention effect estimate against its standard errorNumber of studies = 5 Root MSE = 2468 Test of H0 no small-study effects P= 0739

slightly lower survival rate compared with implantsinserted below intact membranes (9888) (RR 0977(95 CI 0941-1015) However the difference in survivalrates between perforated and non-perforated membraneswas not statistically significant (p=0229) Regardingthese findings we agree with Becker et al [12] who con-cluded that with appropriate treatment intraoperativesinus membrane perforations do not represent a higherrisk of implant loss infectious complications or dis-placement of the graft materialTherefore the following treatment approaches which

correspond to those carried out in the seven articles in-cluded were seen to obtain adequate implant survivalrates

Perforations smaller than 5 mm can be treated byfolding the membrane itself [4 47] or withresorbable sutures [4 50]

When perforations are between 5 and 10 mm themost widely recommended treatment is by means ofa slow-reabsorbing collagen membrane [16 47ndash50]which allows it to regenerate while facilitating clos-ure of the communication Adjuvant treatment mayinclude the use of a resorbable hemostatic agent [49]or resorbable suture [16 47] or PRF [19] PRF acti-vates the vascular system and promotes angiogen-esis As PRF has high strength due to its fibrinnetwork it can prevent graft particles from escapinginto the sinus [19]

In perforations up to 10 mm it is thought possibleto continue the MSFA procedure and even to placeimplants simultaneously [50]

When perforations greater than 10 mm occurlaminar bone and a slow resorption collagenmembrane should be used in combination [50] Inthis case it is advisable to place implants at a laterstage [48]

Several authors [66 67] consider that in the case oflarge perforations (gt10 mm) priority should be given toclosing and repairing the perforation and once this hasbeen achieved a new osteotomy site should be preparedAs stated above according to the articles reviewed im-

plants placed adjacent to repaired perforated membranesobtained a mean survival rate of 9768 while thoseplaced on intact membranes obtained (9888) In thesystematic review and meta-analysis by Al-Dajani et al[68] the mean survival rate of implants below mem-brane perforations was 93 (95 CI 847-1012) andbelow intact membranes 981 (95 CI 936-1025) Al-Moraissi et al [15] in their systematic review observedeven greater differences in implant survival between im-plants placed below perforated 8965 (10221140) andnon-perforated membranes 9751 (32903374)

Moreover these authors found that there was a statisti-cally significant association (p=006) between implantfailure rate and the number of membrane perforationsduring MSFA procedures Nevertheless it should benoted that the present systematic review only includedthe results of MSFA procedures with lateral window ap-proach while Al-Moraissi et al [15] included both lat-eral and crestal approachesThe size of the perforated membrane would appear to

be the key factor influencing the implant survival rate[31 69] In the studies included in this systematic re-view the implant failure rate increased as the size of theperforations increased (Table 5) Similarly Hernaacutendez-Alfaro F et al [50] also observed a lower survival ratewith larger membrane perforations Membrane perfor-ation is also associated with a higher risk of bone graftfailure and infection [70] The use of antibiotics can helpto avoid these negative consequences promoting normalhealing and the intended surgical outcomes [71]In the present systematic review the main complica-

tion associated with perforated membrane repair was in-fection This finding concurs with Park et al [4] whonoted that a higher number of postoperative complica-tions occurred in patients who had suffered membraneperforation during sinus lifting procedures SimilarlyNolan et al [72] observed that perforated sinuses pre-sented three times the risk of bone graft failure and sixtimes the incidence of sinusitisinfection compared withnon-perforated sinuses However Ding et al [73] statedthat neither marginal bone loss around implants norgraft loss was affected by membrane perforationThe present systematic review has some limitations

particularly the heterogeneity of the studies analyzedand the lack of randomized controlled clinical trialscomparing different implant survival outcomes in rela-tion to alternative strategies for managing perforatedmembranes Only Beck-Broisitter et al [47] and Hernaacuten-dez-Alfaro et al [50] describe different approaches ac-cording to the size of the perforation Therefore furtherresearch is needed to establish a clear and validatedprotocol as to which form of treatment should be ap-plied in response to different clinical scenarios

ConclusionsMembrane perforation is the most frequent complica-tion during MSFA with lateral window technique Ac-cording to the findings of this systematic review there isno statistically significant difference in subsequent im-plant survival rates placed below repaired membranescompared with intact membranes Nevertheless a higherpercentage of implant failures was observed as the sizeof the perforations increased The knowledge of theexact size of the membrane perforation is essential fordeciding on the right treatment plan More studies

especially prospective observational studies with longerfollow-up are needed with specific treatment guidelinesand adequate sample sizes in order to provide clear andreliable results as to which form of treatment is the mosteffective in relation to the size of the perforation or ifsome other response might be preferable

AbbreviationsMSFA Maxillary sinus floor augmentation NOS Newcastle-Ottawa scaleRR Risk ratio PRF Platelet-rich fibrin

Supplementary InformationThe online version contains supplementary material available at httpsdoiorg101186s40729-021-00346-7

Additional file 1 Annex 1 PRISMA checklist

AcknowledgementsNot applicable

Authorsrsquo contributionsAll authors read and approved the final manuscript

FundingThe authors received no specific funding for this work

Availability of data and materialsAll data are available in the manuscript and Supplementary files

Declarations

Ethics approval and consent to participateNot applicable

Consent for publicationNot applicable

Competing interestsLuis Alfredo Diacuteaz-Olivares Jorge Corteacutes-Bretoacuten Brinkmann Natalia Martiacutenez-Rodriacuteguez Joseacute Mariacutea Martiacutenez-Gonzaacutelez Juan Loacutepez-Quiles Isabel Leco-Berrocal and Cristina Meniz-Garciacutea declare that they have no competinginterests

Received 27 November 2020 Accepted 22 April 2021

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31 Pikos MA Maxillary sinus membrane repair report of a technique for largeperforations Implant Dent 19998(1)29ndash34 httpsdoiorg10109700008505-199901000-00003

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33 Gehrke S A Taschieri S Del Fabbro M Corbella S Repair of a perforatedsinus membrane with a subepithelial palatal conjunctive flap techniquereport and evaluation Int J Dent 2012 httpsdoiorg1011552012489762

34 Fathima K Harish V S Jayavely P Harinath P Perforated Schneiderianmembrane repair during sinus augmentation in conjunction withimmediate implant placement J Pharm Bioallied Sci 2014 httpsdoiorg1041030975-7406137446

35 Bassi M Adrisani C Lopez A Gaudio R Lombardo L Lauritano DEndoscopically controlled hydraulic sinus lift in combination with rotaryinstruments one year follow-up of a case series Journal of biologicalregulators amp homeostatic agents 2016

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9-year follow-up Int J Implant Dent 2020 httpsdoiorg101186s40729-020-00225-7

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47 Beck-Broichsitter B Westhoff D Behrens E Wiltfang J Becker S Impact ofsurgical management in cases of intraoperative membrane perforationduring a sinus lift procedure a follow-up on bone graft stability andimplant success Int J Implant Dent 20184(1)6 httpsdoiorg101186s40729-018-0116-8

48 Froum S Khouly I Favero G Cho S Effect of maxillary sinus membraneperforation on vital bone formation and implant survival a retrospective studyJ Periodontol 201384(8)1094ndash9 httpsdoiorg101902jop2012120458

49 Oh E Kraut E Effect of sinus membrane perforation on dental implantintegration a retrospective study on 128 patients Implant Dent 201120(1)13ndash9 httpsdoiorg101097ID0b013e3182061a73

50 Hernaacutendez-Alfaro F Torradeflot MM Marti C Prevalence and managementof Schneiderian membrane perforations during sinus-lift procedures ClinOral Impl Res 20081991ndash8

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52 Herrero M Picoacuten M Almeida F Trujillo L Nuacutentildeez J Prieto A 382 elevacionesde seno con teacutecnica de ventana lateral y uso de biomaterial de relleno RevEsp Cirug Oral y Maxilofac 2011333

53 Beck-Broichsitter B Gerle M Wiltfang J Becker S Perforation of theSchneiderian membrane during sinus floor elevations a risk factor for long-term success of dental implants Oral Maxillofac Surg 202024(2)151ndash6httpsdoiorg101007s10006-020-00829-8

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60 Burkhardt R Lang NP Fundamental principles in periodontal plastic surgeryand mucosal augmentation--a narrative review J Clin Periodontol 201441(Suppl 15)S98ndashS107 httpsdoiorg101111jcpe12193

61 Choi B Zhu S Jung J Lee S Huh J The use of autologous fibrin glue forclosing sinus membrane perforations during sinus lifts Oral Surg Oral MedOral Pathol Oral Radiol Endod 2006101(4)426ndash31

62 Von Arx T Broggini N Jensen SS Membrane durability and tissue responseof different bioresorbable barrier membranes a histologic study in therabbit calvarium Int J Oral Maxillofac Implants 201320843ndash53

63 Proussaefs P Lozada J Kim J Repair of the perforated sinus membrane witha resorbable collagen membrane a human study Int J Oral MaxillofacImplants 200419(3)413ndash20

64 Anitua E Orive G Pla R Roamn P Serrano V Andia I The effects of PRGF onbone regeneration and on titanium implant osseointegration in goats ahistologic and histomorphometric study J Biomed Mater Res A 200991(1)158ndash65 httpsdoiorg101002jbma32217

65 Choukroun J Diss A Simonpieri A Girard MO Schoeffler C Dohan SLPlatelet-rich fibrin (PRF) a second-generation platelet concentrate Part IV

clinical effects on tissue healing Oral Surg Oral Med Oral Pathol Oral RadiolEndod 2009101e56ndash60

66 Vlassis J Fugazzotto P A classifications system for sinus membraneperforations during augmentation procedures with options for repair JPeriodontol 199970(6)692ndash9 httpsdoiorg101902jop1999706692

67 Fugazzotto P Vlassis J A simplified classifications and repair system for sinusmembrane perforations J Periodontol 200374(10)1534ndash41 httpsdoiorg101902jop200374101534

68 Al-Dajani M Incidence risk factors and complications of Schneiderianmembrane perforation in sinus lift surgery a meta-analysis Implant Dent201625(3)409ndash15 httpsdoiorg101097ID0000000000000411

69 Shlomi B Horowitz I Kahn A Dobriyan A Chaushu G The effect of sinusmembrane perforation and repair with Lambone on the outcome ofmaxillary sinus floor augmentation a radiographic assessment Int J OralMaxillofac Implants 200419(4)559ndash62

70 Vintildea-Almunia J Pentildearrocha-Diago M Pentildearrocha-Diago M Influence ofperforation of the sinus membrane on the survival rate of implants placedafter direct sinus lift Literature update Med Oral Patol Oral Cir Bucal 200914(3)E133ndash6

71 Chow AW Benninger MS Brook I Brozek JL Goldstein EJ Hicks LAInfectious Diseases Society of America IDSA clinical practice guideline foracute bacterial rhinosinusitis in children and adult Clin Infect Dis 201254(8)e112

72 Nolan P Freeman K Kraut R Correlation between Schneiderian membraneperforation and sinus lift graft outcome a retrospective evaluations of 359augmented sinus J Oral Maxillofac Surg 201472(1)47ndash52 httpsdoiorg101016jjoms201307020

73 Ding X Zhu XH Wang HM Zhang XH Effect of sinus membraneperforation on the survival of implants placed in combination withosteotome sinus floor elevation J Craniofac Surg 201324(2)e102ndash4 httpsdoiorg101097SCS0b013e318264653f

Publisherrsquos NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations

Abstract

Background

Material and methods

Results

Conclusions

Introduction


Databases and search strategy

Inclusion and exclusion of studies

Data extraction

Risk of bias assessment within the studies

Statistical analysis

Results

Screening process

Study characteristics

Patient characteristics

Inter-reviewer agreement

Risk of bias

Meta-analysis

Publication bias

Discussion

Conclusions

Abbreviations

Supplementary Information

Acknowledgements

Authorsrsquo contributions

Funding

Availability of data and materials

Declarations

Ethics approval and consent to participate

Consent for publication

Competing interests

References

Publisherrsquos Note