Risk Factors of Membrane Perforation and Postoperative Complications in Sinus Floor Elevation Surgery: Review of 407 Augmentation Procedures

Risk Factors of Membrane Perforation and Postoperative Complications in Sinus Floor Elevation Surgery: Review of 407 Augmentation Procedures

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Accepted Manuscript Risk Factors of Membrane Perforation and Postoperative Complications in Sinus Floor Elevation Surgery: Review of 407 Augmentation Procedures Linda Schwarz, Vanessa Schiebel, DMD, Markus Hof, DDS, PhD, Christian Ulm, MD, DDS, PhD, Georg Watzek, MD, DDS, PhD, Bernhard Pommer, DDS, PhD PII:

S0278-2391(15)00114-7

DOI:

10.1016/j.joms.2015.01.039

Reference:

YJOMS 56660

To appear in:

Journal of Oral and Maxillofacial Surgery

Received Date: 26 October 2014 Revised Date:

26 January 2015

Accepted Date: 31 January 2015

Please cite this article as: Schwarz L, Schiebel V, Hof M, Ulm C, Watzek G, Pommer B, Risk Factors of Membrane Perforation and Postoperative Complications in Sinus Floor Elevation Surgery: Review of 407 Augmentation Procedures, Journal of Oral and Maxillofacial Surgery (2015), doi: 10.1016/ j.joms.2015.01.039. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Risk Factors of Membrane Perforation and Postoperative Complications in Sinus Floor Elevation Surgery: Review of 407 Augmentation Procedures

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Linda Schwarz

Resident, Bernhard Gottlieb School of Dentistry, Medical University of Vienna, Austria Vanessa Schiebel, DMD

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Resident, Bernhard Gottlieb School of Dentistry, Medical University of Vienna, Austria Markus Hof, DDS, PhD

Vienna, Austria Christian Ulm, MD, DDS, PhD

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University Assistant, Bernhard Gottlieb School of Dentistry, Medical University of

Interim Head of the Division of Oral Surgery, Bernhard Gottlieb School of Dentistry, Medical University of Vienna, Austria

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Georg Watzek, MD, DDS, PhD

Former Head of the Division of Oral Surgery, Bernhard Gottlieb School of Dentistry, Medical University of Vienna, Austria; Academy for Oral Implantology, Vienna, Austria

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Bernhard Pommer, DDS, PhD

Associate Professor, Bernhard Gottlieb School of Dentistry, Medical University of

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Vienna, Austria; Academy for Oral Implantology, Vienna, Austria

Corresponding author:

Bernhard Pommer, DDS, PhD Academy of Oral Implantology Lazarettgasse 19/DG, A-1090 Vienna, Austria phone: +43 1 4028668, fax: +43 1 402866810 e-mail: [email protected]

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Risk Factors of Membrane Perforation and Postoperative Complications in Sinus Floor Elevation Surgery: Review of 407 Augmentation Procedures

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Abstract

Purpose: To test patient- and sinus-related risk factors for association with intraoperative membrane perforation and postoperative complications following sinus floor augmentation surgery.

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Methods: Sinus floor elevation procedures via a lateral approach were retrospectively analyzed regarding patients' medical history and sinus anatomy on computed tomographic

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scans. Complications per sinus following membrane elevation and augmentation using a mixture of autologous bone and deproteinized bovine bone substitute (Bio-Oss®) were recorded. Logic regression (adjusted via the GEE-approach) was performed to analyze the influence of patient age, gender, smoking habits, sinus septa, residual bone height and mesiodistal elevation width.

Results: Out of 407 sinus grafts in 300 patients (mean age: 56 years) perforation of the

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Schneiderian membrane occurred in 35 sinuses (8.6%) and was significantly associated to the presence of sinus septa (odds ratio [OR] = 4.8, P = .002) and reduced residual bone height (OR = 0.01, P < .001). Smoking increased the risk of membrane perforation (OR = 4.8, P = .002), sinusitis (OR 12.3, P < .001) and wound dehiscence (OR 16.1, P = .005). Cases of

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sinus membrane perforation had higher odds for postoperative sinusitis (OR = 10.5, P < .001). The probability of wound dehiscence increased along with the size of the elevated

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area (OR = 3, P < .001).

Conclusion: The results of the study suggest that the presence of sinus septa and residual bone height below 3.5 mm are the main risk factors increasing sinus membrane perforation rates. There was a higher prevalence for sinusitis in cases of membrane perforation (31.4%) despite intraoperative closure with resorbable membranes (Bio-Guide®). Smokers generally exhibited higher chances for complications.

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Introduction

Implant-supported rehabilitation of the edentulous jaw represents a highly predictable and widely accepted therapy.1 Implant placement in the atrophic posterior maxilla, however, is

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frequently complicated by sinus pneumatization and alveolar bone resorption following tooth loss. To increase available bone volume, guided bone regeneration using the sinus membrane as a natural barrier – sinus floor elevation surgery – has been established.2 Coronal displacement of the maxillary sinus membrane with or without addition of

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bone (substitute) material allows for bone formation and, in the following, osseointegration of either delayed or simultaneously placed implants. Access to the sinus membrane is accomplished via osteotomy in the lateral sinus wall, as described by Boyne in the 1960s, or

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else via a transcrestal approach, as described by Summers in the 1990s.3 The lateral sinus augmentation technique is generally recommended in case of less than 4-5 mm of residual alveolar bone height4 as greater membrane elevation and more gain in postoperative bone volume has been recorded compared to minimally invasive techniques.5

Iatrogenic perforation of the maxillary sinus membrane in the course of membrane elevation

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represents the most frequent intraoperative complication in 10-20% of sinus floor augmentation surgeries on average3,6 and increases the chance of postoperative sinusitis due to bacterial graft contamination and/or graft migration into the sinus cavity. Various factors have been tested for potential impact on membrane perforation rates. Reduced

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membrane thickness7,8 and complex sinus morphology9 may complicate the membrane elevation procedure. Smoking may compromise wound healing10 and implant survival11,12

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and has been mentioned as a potential risk factor for intraoperative membrane perforation in several studies.12–15 Moreover, the extent of bone atrophy of the posterior maxilla has demonstrated impact on the risk of membrane perforation9,14,16 assumably due to increasing detachment forces with larger areas of membrane elevation8 and higher septa prevalence in atrophic maxillary areas.17–20 The presence of sinus septa is generally associated with a higher risk of membrane perforation.21,22 Stronger adhesion of the sinus membrane to knifeedged septa has been postulated as potential explanation.23 Prevalence and morphology of sinus septa have been first described by Underwood in 1910, and thoroughly analyzed in the literature thereafter.17,24,25

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The purpose of the present study was to evaluate the risk of intraoperative membrane perforation and postoperative complications in the course of lateral sinus augmentation surgery. The hypothesis of no relationship between complication rates and potential risk factors was adopted. Scarce data on membrane perforation rates in the presence of sinus

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septa suggest increased perforation rates ranging from 10 to 79%;9,13,15,26,27 however, no significant difference to non-septated sinuses has been substantiated to date. The aim of the present study was to assess prevalence, orientation and location of sinus septa, as well as to evaluate the impact of septa along with other possible influencing factors on membrane

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perforation rates. The specific aim of the study was to assess pre- and postoperative

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complication rates and to test their association with potential risk factors.

Material & Methods

Study design

The investigators implemented a retrospective observational study. The study population

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was composed of all patients requiring sinus augmentation for implant placement in the edentulous posterior maxilla at the Division of Oral Surgery, Medical University of Vienna (Austria) from January 2001 through December 2012. Inclusion criteria were a thorough medical history, preoperative panoramic radiographs and CT-scans, augmentation via the

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lateral approach with delayed implant placement and postoperative routine panoramic radiographs. Patients were excluded as study subjects if they were not followed for at least 1

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year.

Sinus graft procedures were conducted under local anesthesia using the lateral approach, i.e. osteotomy of the lateral wall of the maxillary sinus.33 A total of 11 surgeons performed the procedures, each of them experienced and specialized in oral surgery. A mixture of autologous bone (harvested either from the maxillary tuberosity, the retromolar area or symphysis of the mandible, or else the iliac crest) and deproteinized bovine bone substitute (Bio-Oss®, Geistlich, Wolhusen, Switzerland) was applied. Prophylactic oral premedication was performed routinely and patients were instructed to continue antibiotics for 10 days. All perforations were repaired and covered using a collagen bioabsorbable membrane (Bio-

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Gide®, Geistlich, Wolhusen, Switzerland) to avoid displacement of the graft material and sinus inflammation. The study protocol was approved by the ethics committee of the Medical University of Vienna on 12th March 2013 (EK Nr: 1968/2012).

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Variables

Prevalence of membrane perforation was assessed as dichotomous outcome and associated predictor variables comprised patient-related (age, sex, smoking habits) as well as

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anatomical factors (presence of sinus septa, residual bone height, mesio-distal size of the augmented area, i.e. elevation width). Sinus septa were further analyzed regarding exact number, location and orientation. Classification of septum location was adopted as defined

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by Underwood28 (premolar region, first molar region and second molar region) and commonly applied in literature.29–32 The extent of the augmented area corresponded to the number of teeth to be replaced, and was hence categorized into four groups, ranging from single tooth replacement to augmentation of the entire maxillary sinus region measuring four tooth gaps. Additionally, presence of sinus septa within the augmented area was assessed on postoperative panoramic radiographs. Secondary outcome variables involved

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postoperative complication rates (maxillary sinusitis, wound dehiscence, loss of bone graft). Potential risk factors for postoperative complications were defined as patient age, sex, smoking habits, event of intraoperative membrane perforation, residual bone height and

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elevation width.

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Data collection methods

Before surgery, the patients’ medical history was recorded and panoramic radiographs (Orthophos XG Plus, Sirona, Germany or Scanora, Soredex Medical System, Finland) as well as CT-scans (Tomoscan SR 6000, Philips, Netherlands) with a high-resolution bone algorithm, 75mA, 120 kV, scanning time of 2 seconds and slice thickness of 1.5 mm, were acquired to allow preoperative evaluation of the implant site, including measurement of residual bone height and assessment of septa presence, orientation and location. Perforation of the Schneiderian membrane was assessed by direct visualization, when no visible perforation was observed, the patient was asked to gently perform the Valsalva maneuver. Postoperative routine panoramic radiographs were evaluated to assess septum location in

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relation to the augmented area. All patients were subjected to a routine follow-up procedure to assess postoperative complications. In case of maxillary pathology-related symptoms, clinical findings were confirmed with postoperative CT-scans.

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Data analysis

Prevalence of intraoperative membrane perforation and postoperative complications were assessed and tested for association with the corresponding risk factors using Pearson chi-

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square or Fisher-exact tests. Residual bone height was thereby subclassified into < 3.5 mm and ≥ 3.5 mm (according to the median value of 3.5 mm), age into < 56 years and ≥ 56 years (mean age of 56) and elevation width into 1-2 tooth gaps and 3-4 tooth gaps. Mean residual

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bone height and elevation width was tested for differences using Student’s t-test. Logistic regression analysis was used to model the odds ratio of sinus membrane perforation and postoperative complications by the corresponding risk factors. To fit the logistic regression model for clustered measurements in patients who received bilateral sinus surgery, the GEE approach was used (CSLOGISTIC procedure in SPSS). Statistical analysis was performed using

Results

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IBM SPSS statistics 21 software (IBM corporation, USA) at a significance level of 0.05.

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300 patients (107 men and 193 women) were included in this study, between 20 and 83 years of age with a mean of 55.9 ± 14.0 years. 57 patients considered themselves current

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smokers (20.6% of men and 18.1% of women). A total of 407 sinus graft procedures were conducted (196 on the right and 211 on the left side).

Risk of sinus membrane perforation

Perforation of the Schneiderian membrane occurred in 35 out of 407 (8.6%) sinus augmentation procedures (Figure 1). 27 perforations (77.1%) were registered at surgical sites presenting sinus septa (45.8% perforation rate), while only 8 ruptures occurred in nonseptated augmentation areas (2.3% perforation rate, P < .001). Mean residual bone height was 3.4 ± 0.8 mm, and was significantly lower in case of membrane perforation (1.8 ± 0.8

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mm vs. 3.5 ± 0.6 mm, P < .001). Patient age, sex, smoking habits and sinus elevation width did not significantly impact membrane perforation rates (Table 1). After adjusting the risk for membrane perforation in a logistic regression analysis with residual bone height, sinus septa, sex, age, smoking and elevation width as independent variables (Table 2), association of

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membrane perforation with residual bone height (OR = 0.010, P < .001), sinus septa presence (OR = 4.77, P = .002) and smoking (OR = 4.81, P = .002) demonstrated statistical significance.

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Detailed analysis of sinus septa presence yielded an overall septa prevalence of 27.1% (110 of 407 sinuses) that was not associated with patient age (P = .393) or gender (P = .348). No significant difference in septa prevalence between left and right sinuses was observed (P =

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.720). Only 14.5% of the operated sinuses contained septa that were actually in touch with the surgical site (48.4% of all septa).26 Two septa within the same sinus were present in 2.9%, however, no second septum was observed in the area of augmentation (Table 3). 50.8% of septa were found in molar and 42.6% in premolar regions (Table 4, Figure 2). The vast majority of all observed septa was orientated transversely (93.5%). No septum was found to completely divide the sinus into two separate cavities. Septa in grafted sinus

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regions did not differ in distribution regarding location (P = .213) or orientation (P = .559). Their orientation and location did not influence the procedure’s membrane perforation rate

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(P = .237 and P = .192, respectively).

Risk of postoperative complications

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Analysis of postoperative complications revealed a sinusitis prevalence of 8.4% (34 grafted sinuses, Table 5) and wound dehiscences in 5 cases (1.2%). No loss of bone graft was documented. Eleven sinuses (31.4%) developed sinusitis after intraoperative rupture of the Schneiderian membrane, whereas only 6.2% of sinuses with intact membrane developed signs of postoperative inflammation (P < .001). Another risk factor for postoperative sinusitis was smoking, with a sinusitis prevalence of 26.2% among smokers compared to 3.7% in nonsmokers (P < .001). These risk factors were confirmed by the sinusitis regression model (independent variables age, sex, smoking, membrane perforation, residual bone height and elevation width), suggesting an odds ratio of 12.3 (P < .001) in smokers and an odds ratio of

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10.5 (P < .001) after intraoperative rupture of the Schneiderian membrane (Table 6). Risk of postoperative sinusitis was also associated with sinus elevation width (2.6 vs. 2.7 tooth gaps, OR = 0.77, P < .001) and increased slightly with every year of age (OR = 1.04, P < .001).

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No wound dehiscences occurred after membrane rupture, however, prevalence of wound dehiscence was significantly higher in smokers (4.8%, Table 5) compared to non-smokers (0.3%, P = .007). Mean elevation width measured 3.6 ± 0.6 tooth gaps at the event of postoperative wound dehiscence and 2.7 ± 1.2 when no dehiscence was reported (P = .790).

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According to the computed regression model on wound dehiscence, odds ratios were 16.1 (P < .001) for smokers and 3.0 (P < .001) for any additional tooth gap of the augmentation area

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(Table 6).

Discussion

Prevalence of Schneiderian membrane perforation was 8.6% and was significantly associated to the presence of sinus septa (OR = 4.8), smoking (OR = 4.8) and reduced residual bone

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height (OR = 0.01). The frequency of postoperative sinusitis was significantly higher in cases of sinus membrane perforation (OR = 10.5) and in smokers (OR = 12.3). Wound dehiscence

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was more frequent in smokers (OR = 16.1) as well as in large elevation areas (OR = 3.0).

Compared to the overall prevalence of maxillary sinus septa of 28.4% in both atrophic and non-atrophic alveolar ridges reported in a recent systematic review and meta-analysis17 the

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population of the present study showed a similar frequency of sinus septation (27.1%). As only patients requiring lateral sinus augmentation surgery prior to implant placement were included, however, severely resorbed alveolar ridges with a mean crestal bone height of 3.5 mm were observed. One might thus have expected higher septa prevalence, as septa have been previously described to be more prevalent in atrophic edentulous areas.18,19,28 Septa predominantly showed transversal orientation (93.5%) and were located at premolar or molar sites in 42.6 and 50.8%, respectively. This finding is in line with literature that reports the tendency of septa to display mainly transversal orientation (87.6%) and location at first and second molar sites (54.6%).17 Literature as well as the present study suggest no

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correlation of septa prevalence to patient sex or age,29–31 although few studies reported a higher frequency of sinus septation in men.18,32 In order to differentiate recesses and irregularities of the bony sinus floor from proper septa, several studies included only septa above a threshold height of 2 to 3 mm.18,20,29,30,33–36 However, studies that did not apply

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height thresholds did not reveal significantly higher septa prevalence.17 As even small septa can affect surgical procedures,37 all septa were included in this study to access their effect on surgical complication rates.

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The overall membrane perforation rate accounted 8.6%. This compares to a systematic review by Pjetursson and coworkers3 yielding a membrane perforation rate of 19.5% (range 0 – 58.3%) in the course of lateral sinus floor elevation. Data on augmentation surgery in

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septated sinuses suggest a perforation rate of 10 to 79%,9,13,15,26,27 however, no significant difference to non-septated sinuses has been observed so far. In the present study, by contrast, membrane perforation in the presence of septa was as high as 45.5% and the significant influence of sinus septa on the frequency of intraoperative membrane perforation in the course of sinus floor augmentation could be substantiated. Besides sinus septa, residual bone height showed inverse association to membrane perforation (P < .001). This

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might be due to a reduced maximum elevation height without membrane perforation in cases of low residual bone height, as suggested in a study on formalin-fixed cadavers.38 Low residual bone height, however, requires greater membrane elevation to allow for regular implant lengths.39 As a consequence, technical difficulties arise during detachment of large

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membrane areas from the bony wall22 as well as higher elevation forces required for

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membrane elevation.8

Logistic regression allows for assessment of influence of several risk factors on a dependent variable, i.e. membrane perforation, and exclusion of confounding factors when carefully interpreted. After adjusting for factors with great impact on membrane perforation (residual bone height and sinus septa), the effect of smoking could be revealed as an additional risk factor with small, but statistically significant impact (10.6 vs. 8.0% perforation rate). Out of several studies on the topic,12–15,27 however, only one further study, analyzing 110 sinus augmentation procedures with immediate implant placement,14 found smoking to be a significant risk factor for membrane perforation. Smoking results in impaired wound healing

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following several dental surgical procedures, like mucogingival surgery40, flap debridement41 and onlay-bone grafting.10 It further leads to higher incidence of peri-implantitis,42 higher implant failure rates11,12 and risk of wound dehiscence, as observed in the present study.

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Twenty-one membrane perforations were observed in 13 patients who received bilateral sinus surgery (10.9% perforation rate in bilaterally operated sinuses), this compares to 14 membrane perforations during 179 unilateral surgeries (7.8%). To minimize clustered effects of bi- and unilateral operated patients, the logistic regression model was adapted using the

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GEE approach to allow for a more precise estimation. Potential limitations may also arise from the differentiation between sinus septa within vs. outside the augmented area. In cases of membrane perforation or even difficulties during membrane elevation around sinus

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septa, the surgeon may choose to refrain from further elevation efforts and the grafted area may project in a distance to the septum on postoperative radiographs (thus leading to categorization as septum outside the augmented area). Exclusion of patients with follow-up examination data shorter than 1 year may have introduced the risk of selection bias.43 It should as well be kept in mind that diagnosis of postoperative sinusitis and wound dehiscence relies heavily on clinical symptoms; patient compliance and inherent limitations

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Conclusion

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of retrospective investigations cannot be ruled out.

The present results may assist the clinician in evaluating the risk of intra- and postoperative

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complications caused by anatomical and patient-related determinants. Smoking has aninfluence on the prevalence of both intra- as well as postoperative complications. An association of membrane perforation with postoperative sinusitis was statistically confirmed in the present study, as previously reported in literature27,44. However, neither membrane perforation nor postoperative sinusitis may necessarily lead to reduced implant survival,12,27,45 especially when treated via surgery and/or medication.44 Future research is indicated to investigate the effects of membrane perforation on long-term sinus physiology46 and possible reasons for increased sinusitis rates following membrane perforation.47

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References

1.

Moreno Vazquez JC, Gonzalez de Rivera AS, Gil HS, Mifsut RS. Complication rate in 200 consecutive sinus lift procedures: guidelines for prevention and treatment. J Oral

2.

RI PT

Maxillofac Surg. 2014;72(5):892-901.

Watzek G, Weber R, Bernhart T, Ulm C, Haas R. Treatment of patients with extreme maxillary atrophy using sinus floor augmentation and implants: preliminary results. Int J Oral Maxillofac Surg. 1998;27(6):428-434.

Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of the success of

SC

3.

sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol. 2008;35(8 Suppl):216-240.

Esposito M, Grusovin MG, Willings M, Coulthard P, Worthington H V. The

M AN U

4.

effectiveness of immediate, early, and conventional loading of dental implants: a Cochrane systematic review of randomized controlled clinical trials. Br J Oral Maxillofac Implants. 22(6):893-904. 5.

Berengo M, Sivolella S, Majzoub Z, Cordioli G. Endoscopic evaluation of the boneadded osteotome sinus floor elevation procedure. Int J Oral Maxillofac Surg.

TE D

2004;33(2):189-194. 6.

Chiapasco M, Zaniboni M. Methods to treat the edentulous posterior maxilla: implants with sinus grafting. J Oral Maxillofac Surg. 2009;67(4):867-871. Wen S-C, Lin Y-H, Yang Y-C, Wang H-L. The influence of sinus membrane thickness

EP

7.

upon membrane perforation during transcrestal sinus lift procedure. Clin Oral Implants Res. 2014:1-7.

Pommer B, Unger E, Sütö D, Hack N, Watzek G. Mechanical properties of the

AC C

8.

Schneiderian membrane in vitro. Clin Oral Implants Res. 2009;20(6):633-637.

9.

Zijderveld S a, van den Bergh JP a, Schulten E a JM, ten Bruggenkate CM. Anatomical and surgical findings and complications in 100 consecutive maxillary sinus floor elevation procedures. J Oral Maxillofac Surg. 2008;66(7):1426-1438.

10.

Levin L, Herzberg R, Dolev E, Schwartz-Arad D. Smoking and Complications of Onlay Bone Grafts and Sinus Lift Operations. Br J Oral Maxillofac Implants. 2004;19(3):369373.

ACCEPTED MANUSCRIPT

11.

Zinser MJ, Randelzhofer P, Kuiper L, Zöller JE, De Lange GL. The predictors of implant failure after maxillary sinus floor augmentation and reconstruction: a retrospective study of 1045 consecutive implants. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013;115(5):571-582. Testori T, Weinstein RL, Taschieri S, Del Fabbro M. Risk factor analysis following

RI PT

12.

maxillary sinus augmentation: a retrospective multicenter study. Br J Oral Maxillofac Implants. 2012;27(5):1170-1176. 13.

Von Arx T, Fodich I, Bornstein M, Jensen S. Perforation of the sinus membrane during

Oral Maxillofac Implants. 2014;29(3):718-726. 14.

SC

sinus floor elevation: a retrospective study of frequency and possile risk factors. Int J

Ardekian L, Oved-Peleg E, Mactei EE, Peled M. The clinical significance of sinus

Surg. 2006;64(2):277-282. 15.

M AN U

membrane perforation during augmentation of the maxillary sinus. J Oral Maxillofac

Kasabah S, Krug J, Simunek A, Lecaro MC. Can We Predict Maxillary Sinus Mucosa Perforation? Acta Medica. 2003;46(1):19-23.

16.

Yilmaz HG, Tözüm TF. Are Gingival Phenotype, Residual Ridge Height, and Membrane Thickness Critical for the Perforation of Maxillary Sinus? J Periodontol.

17.

TE D

2012;83(4):420-425.

Pommer B, Ulm C, Lorenzoni M, Palmer R, Watzek G, Zechner W. Prevalence, location and morphology of maxillary sinus septa: systematic review and meta-analysis. J Clin

18.

EP

Periodontol. 2012;39(8):769-773.

Lee W-J, Lee S-J, Kim H-S. Analysis of location and prevalence of maxillary sinus septa. J Periodontal Implant Sci. 2010;40(2):56-60. Krennmair G, Ulm CW, Lugmayr H, Solar P. The incidence, location, and height of

AC C

19.

maxillary sinus septa in the edentulous and dentate maxilla. J Oral Maxillofac Surg. 1999;57(6):667-671

20.

Ulm CW, Solar P, Krennmair G, Matejka M, Watzek G. Incidence and suggested surgical management of septa in sinus-lift procedures. Br J Oral Maxillofac Implants. 1995;10(4):462-465.

21.

Ella B, Noble RDC, Lauverjat Y, et al. Septa within the sinus: effect on elevation of the sinus floor. Br J Oral Maxillofac Surg. 2008;46(6):464-467.

ACCEPTED MANUSCRIPT

22.

Van den Bergh JP, ten Bruggenkate CM, Disch FJ, Tuinzing DB. Anatomical aspects of sinus floor elevations. Clin Oral Implants Res. 2000;11(3):256-265.

23.

Chanavaz M. Maxillary sinus: anatomy, physiology, surgery, and bone grafting related to implantology--eleven years of surgical experience (1979-1990). J Oral Implantol.

24.

RI PT

1990;16(3):199-209.

Wen S-C, Chan H-L, Wang H-L. Classification and management of antral septa for maxillary sinus augmentation. Int J Periodontics Restorative Dent. 33(4):509-517.

25.

Palma VC, Rosa a., Semenoff T a. DV, et al. Evaluation of septa frequency in the

tomography. Oral Surg. 2013;6(2):67-72. 26.

SC

maxillary sinuses with edentulous and dentulous areas through computed

Becker ST, Terheyden H, Steinriede A, Behrens E, Springer I, Wiltfang J. Prospective

M AN U

observation of 41 perforations of the Schneiderian membrane during sinus floor elevation. Clin Oral Implants Res. 2008;19(12):1285-1289. 27.

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(4):511-516.

28.

Koymen R, Gocmen-Mas N, Karacayli U, Ortakoglu K, Ozen T, Yazici AC. Anatomic

570. 29.

TE D

evaluation of maxillary sinus septa: surgery and radiology. Clin Anat. 2009;22(5):563-

Kim M-J, Jung U-W, Kim C-S, et al. Maxillary sinus septa: prevalence, height, location,

EP

and morphology. A reformatted computed tomography scan analysis. J Periodontol. 2006;77(5):903-8. doi:10.1902/jop.2006.050247. 30.

Park Y-B, Jeon H-S, Shim J-S, Lee K-W, Moon H-S. Analysis of the anatomy of the

AC C

maxillary sinus septum using 3-dimensional computed tomography. J Oral Maxillofac Surg. 2011;69(4):1070-1078.

31.

Neugebauer J, Ritter L, Mischkowski RA, Dreiseidler T, Scherer P, Ketterle M. Evaluation of Maxillary Sinus Anatomy by Cone-Beam CT Prior to Sinus Floor Elevation. Br J Oral Maxillofac Implants. 2010;25(2):258-265.

32.

Shen E-C, Fu E, Chiu T-J, Chang V, Chiang C-Y, Tu H-P. Prevalence and location of maxillary sinus septa in the Taiwanese population and relationship to the absence of molars. Clin Oral Implants Res. 2012;23(6):741-745.

ACCEPTED MANUSCRIPT

33.

Maestre-Ferrin L, Carrillo-Garcia C, Galan-Gil S, Penarrocha-Diago M, PenarrochaDiago M. Prevalence, location, and size of maxillary sinus septa: panoramic radiograph

versus

computed

tomography

scan.

J

Oral

Maxillofac

Surg.

2011;69(2):507-511. Gosau M, Rink D, Driemel O, Draenert FG. Maxillary sinus anatomy: a cadaveric study with clinical implications. Anat Rec. 2009;292(3):352-354. 35.

RI PT

34.

Rosano G, Taschieri S, Gaudy J-F, Lesmes D, Del Fabbro M. Maxillary sinus septa: a cadaveric study. J Oral Maxillofac Surg. 2010;68(6):1360-1364.

Naitoh M, Suenaga Y, Kondo S, Gotoh K, Ariji E. Assessment of maxillary sinus septa

SC

36.

using cone-beam computed tomography: etiological consideration. Clin Implant Dent Rel Res. 2009;11 Suppl 1:e52-58.

Van Zyl AW, van Heerden WFP. A retrospective analysis of maxillary sinus septa on reformatted

computerised

2009;20(12):1398-1401. 38.

M AN U

37.

tomography

scans.

Clin

Oral

Implants

Res.

Bayar GR, Yildiz S, Gulses A, Sencimen M, Acikel CH, Comert A. Correlation between the residual ridge height and the perforation limit of sinus membrane in crestal sinus elevation. Quintessence Int. 2013;44(9):689-697.

Jensen OT, Shulman LB, Block MS, Iacono VJ. Report of the Sinus Consensus

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39.

Conference of 1996. Br J Oral Maxillofac Implants. 1998;13 Suppl:11-45. 40.

Erley KJ, Swiec GD, Herold R, Bisch FC, Peacock ME. Gingival recession treatment with

1155. 41.

EP

connective tissue grafts in smokers and non-smokers. J Periodontol. 2006;77(7):1148-

Scabbia A, Cho KS, Sigurdsson TJ, Kim CK, Trombelli L. Cigarette smoking negatively

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affects healing response following flap debridement surgery. J Periodontol. 2001;72(1):43-49.

42.

Haas R, Haimböck W, Mailath G, Watzek G. The relationship of smoking on periimplant tissue: a retrospective study. J Prosthet Dent. 1996;76(6):592-596.

43.

Dodson TB. A guide for preparing a patient-oriented research manuscript. Oral Surg Oral Med Oral Pathol Oral Radiol. 2007;104(3):307-315.

44.

Kim Y, Hwang J, Yun DDSP. Relationship Between Prognosis of Dental Implants and Maxillary Sinusitis Associated with the Sinus Elevation Procedure. 2013;28(1):178183.

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45.

Nkenke E, Stelzle F. Clinical outcomes of sinus floor augmentation for implant placement using autogenous bone or bone substitutes: a systematic review. Clin Oral Implants Res. 2009;20 Suppl 4:124-133.

46.

Pommer B, Dvorak G, Jesch P, Palmer RM, Watzek G, Gahleitner A. Effect of Maxillary

Periodontol. 2012;83(5):551-556. 47.

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Sinus Floor Augmentation on Sinus Membrane Thickness in Computed Tomography. J

Nolan PJ, Freeman K, Kraut RA. Correlation between Schneiderian membrane perforation and sinus lift graft outcome: a retrospective evaluation of 359 augmented

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sinus. J Oral Maxillofac Surg. 2014;72(1):47-52.

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Tables

Table 1: Prevalence of sinus membrane

P-value

perforation .215

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female 20 (7.4%) Sex male 15 (11%) <56 16 (9%)

.781

Age ≥56 19 (8.3%) .438

No 26 (8%) Yes 27 (45.8%) <.001 Sinus septa

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No 8 (2.3%)

SC

Yes 9 (10.7%) Smoking

Residual

<3.5 mm 35 (24.7%) <.001

bone height

≥3.5 mm 0

1-2 tooth gaps 12 (7.8%)

width

3-4 tooth gaps 23 (9.1%)

.650

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Elevation

Table 2: Risk factors of sinus membrane perforation standard

Odds ratio

P-value

0.494

.189

error

0.534

EP

Sex (female)

[Cl95% 0.171 – 1.423]

0.016

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Age

Smoking

Sinus septa

0.493

0.498

0.976

.143

[Cl95% 0.945 – 1.008]

4.811

.002*

[Cl95% 1.811 – 12.780] 4.771

.002*

[Cl95% 1.777 – 12.807] Residual bone

0.625

< .001*

[Cl95% 0.003 – 0.036]

height Elevation width

0.010

0.232

0.921 [Cl95% 0.582 – 1.458]

.725

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Regression analysis was conducted for continuous (age, residual bone height and elevation width) and dichotomous (sex, smoking, sinus septa) variables. As for continuous variables, odds ratio refers to risk of membrane perforation for a one-unit increase.

Table 3: Summary of septa prevalence data No. (%)

No. with septa

No. with septa

(%)

in grafted region (%)

No. with 2 septa

SC

(%) 300

98 (32.7)

53 (17.7)

6 (2)

Male

107 (35.7)

51 (17)

24 (8)

2 (0.7)

Female

193 (64.3)

47 (15.7)

29 (9.7)

4 (1.3)

407

110 (27)

59 (14.5)

12 (2.9)

Right

196 (48.2)

51 (12.5)

32 (7.9)

5 (1.2)

Left

211 (51.8)

59 (14.5)

27 (6.6)

7 (1.7)

Sinus

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Patients

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* p-values were considered statistically significant (P < .05)

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Table 4: Septa Location and Orientation Location (%) anterior

(n=122) Septa in grafted

transversal sagittal

horizontal

(retromolar)

52 (42.6)

8 (6.6)

114 (93.5)

6 (4.9)

2 (1.6)

1 (1.7)

56 (94.9)

2 (3.4)

1 (1.7)

62

(50.8)

28 (47.5)

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region (n=59)

posterior

(premolar) (molar)

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All septa

middle

Orientation (%)

30

(50.8)

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Table 5: Prevalence of postoperative complications

p-value

female 24 (8.9%) Sex

.605 male 10 (7.4%) <56 13 (7.3%)

Age

.519

RI PT

≥56 21 (9.1%)

Yes 22 (26.2%) Smoking

<.001*

No 12 (3.7%) Prevalence of sinusitis

Yes 11 (31.4%) Perforation

<.001*

SC

No 23 (6.2%) <3.5

18 (10.2%)

bone height

≥3.5

16 (7%)

M AN U

Residual

Elevation

1-2

13 (8.4%)

width

3-4

21 (8.3%)

.246

.960

female 4 (1.5%)

Sex

.522

male 1 (0.7%) <56 3 (1.7%)

Age

.657

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≥56 2 (0.9%) Yes 4 (4.8%)

Smoking

Prevalence of wound

Perforation

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EP

dehiscence

.007 No 1 (0.3%) Yes 0 1.000 No 5 (1.3%)

Residual

<3.5 mm 2 (1.1%)

bone height

≥3.5 mm 3 (1.3%)

Elevation

1-2 0

width

3-4 5 (2%)

1.000

.162

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Table 6: Risk factors of postoperative complications standard

Odds ratio

P-value

1.618

.145

error Sex (female)

0.328

Age

0.038

RI PT

[Cl95% 0.845 – 3.099] 1.039

<.001*

[Cl95% 1.020 – 1.058] Smoking

0.291

12.316

<.001*

Perforation

0.362

10.507

SC

[Cl95% 6.923 – 21.911] Risk of sinusitis

<.001*

[Cl95% 5.131 – 21.516]

bone height Elevation width Sex (female)

0.272

12.591

M AN U

Residual

.715

[Cl95% 6.922 – 22.902]

0.104

0.774

0.015*

[Cl95% 0.630 – 0.951]

0.338

1.171

.642

TE D

[Cl95% 0.599 – 2.289]

Age

Smoking

Perforation

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dehiscence

EP

Risk of wound

Residual

0.032

0.403

width

.362

[Cl95% 0.911 – 1.035] 16.520

<.001*

[Cl95% 7.433 – 36.716]

1.586



<.001*

0.404

0.700

.379

[Cl95% 0.315 – 1.558]

bone height Elevation

0.971

0.253

2.951

<.001*

[Cl95% 1.786 – 4.874]

Regression analysis was conducted for continuous (age, residual bone height, elevation width) and dichotomous (sex, smoking, perforation) variables. As for continuous variables, odds ratio refers to risk of an event for a one-unit increase. * p-values were considered statistically significant (P < .05) ∞ refers to invalid OR, as no wound dehiscence was observed after membrane perforation

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Figure Legends

Fig. 1: Intraoperative rupture of the Schneiderian membrane in the course of sinus

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membrane elevation surgery

Fig. 2: 3-dimensional CT reconstruction in axial plane of a sinus showing a septum with

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M AN U

SC

transversal orientation in the premolar region.

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M AN U

SC

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SC

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