Placing implants in atrophic posterior maxilla is one of the daily challenges faced by implantologists.1 Dr. O. Hilt Tatum of the United States pioneered in developing the first sinus lift operation in 1974 and the first sinus graft operation in 1975. Since then, several surgical techniques have been developed to address insufficient bone quantity aiming at producing more accommodating implant cradle. Whereas the osteotome transcrestal technique is indicated in increasing the vertical bone height between 3 and 9 mm, the lateral window technique is indicated when an increase in vertical bone height of greater than 9 mm is required.1 Along with every surgical intervention comes undesirable complications.
With the increased global focus on delivering patient-oriented health care services, optimum patient care requires thorough knowledge of surgical techniques and recognition of surgical complications and possible risk factors. Being the most common surgical complication of sinus augmentation, the perforation of Schneiderian membrane is an important obstacle facing implantologists, where their implants are to be placed in atrophic posterior maxilla.
The aim of our study was to evaluate existing evidence that demonstrates the incidence of membrane perforation, identify possible risk factors associated with membrane perforations, and describe the common complications as well as the surgical management of perforations.
Materials and Methods
An exhaustive search strategy of the literature was executed to identify articles published from January 1975 to October 2015, dealing with patients who experienced perforation of Schneiderian membrane during sinus lift augmentation procedures through different surgical approaches. Articles were pinpointed using systematic searches in MEDLINE, EMBASE, Scopus, Web of Science, Trip, Cochrane Oral Health Group's Trials Register, Cochrane Central Register of Controlled Trials, and ProQuest Dissertations & Theses. The last electronic search was performed on October 15, 2015, entering the following terms: “maxillary sinus” and “membrane” and “perforation.” Literature was also identified through reference lists of selected articles.
Studies were considered appropriate for inclusion if they met the following criteria: (1) randomized controlled trials or retrospective studies that included consecutive patients, and (2) a sample size of 10 or more patients who had undergone implant surgery in the same center. The exclusion criteria were as follows: (1) nonhuman studies, (2) articles not in English language, and (3) technical reports, letters, and comments.
Articles were critically reviewed to determine the level of evidence as per the Canadian Task Force on Preventive Health Care. The quality assessment of each included study was performed using the GRADE (Grading of Recommendations Assessment, Development and Evaluation) system,2 a system that is also recommended by the Cochrane GRADEing group. The quality of evidence for reported outcomes were rated as “high,” “moderate,” “low,” or “very low” (Appendix 1).
Table 1 shows the keywords and their combinations used in the literature search. Thirty-three articles were included in the review tables and distributed as follows: 18 retrospective studies, 12 prospective cohort/case series, and 3 randomized controlled trials.
Data Extraction and Statistical Analysis
Data extracted for meta-analysis were sample size, outcome measures, and significance. Possible impact of publication bias was assessed by evaluating funnel plot asymmetry. All data were synthesized using both fixed and random effect models. Tests for heterogeneity were performed with the Cochrane Q test and I2 index for each meta-analysis. The fixed effects model was used if the result of heterogeneity test was P > 0.05 and if I2 < 50%, whereas a random effects model was used in the presence of high heterogeneity (P < 0.05, I2 > 50%). A 2-tailed P < 0.05 was considered statistically significant. Review Manager, version 5.3 (Revman; The Cochrane Collaboration, Oxford, United Kingdom) was used.
The primary data items for this meta-analysis were (1) incidence of Schneiderian membrane perforation occurring during sinus lift surgery, (2) risk factors, and (3) complications.
Schneiderian Membrane Perforation Incidence Rate
Incidence rates represented the frequency of encountering sinus perforation per sinus lift procedure. Out of 1652 sinus lift surgical procedures reported in 12 studies,3–14 388 Schneiderian membrane perforations occurred. Being the most common complication encountered in sinus lift surgery, the weighted average for the incidence rate of Schneiderian membrane perforation was 23.5% (95% confidence interval [95% CI], 21.1–25.8) (Fig. 1) ranging from 3.6% to 41.8% (Table 2).3–14 The random effects meta-analysis was applied, because there was evidence of considerable heterogeneity in the incidence rates (Q = 112.4, df = 11, P < 0.05; I2 = 90.2%).
Incidence rates of membrane perforation were not calculable in 2 studies15,16 because of data unavailability or data variability. Proussaefs et al15 study was a randomized controlled trial with a split-mouth design, in which the inclusion criteria comprised the preincidence of sinus perforation in 1 side, whereas in Karabuda et al16 study, the total number of performed sinus lift procedures was not specified.
Table 3 illustrates the role of possible risk factors in the incidence of Schneiderian membrane perforation. Although patient's age and sex as well as surgeon experience did not significantly alter the risk of perforation,3,10 both the reduced thickness of Schneiderian membrane and presence of sinus septa were associated with the incidence of perforation in several studies.3,5,13
A decrease in the incidence of Schneiderian membrane perforation was recorded with the application of piezoelectric instrumentation.5,13,14 On the other hand, 2 randomized controlled clinical trials of small sample size reported that piezoelectric surgery did not seem to present more advantages over conventional rotational instruments.11,12 Hence, further randomized controlled trials of larger sample size are still required to assess the role of piezoelectric surgery in preventing membrane perforation during sinus lift procedures.
Common Complications and Clinical Consequences
Table 4 reveals the complications associated with membrane perforation. Several researchers investigated implant survival rates after sinus membrane perforations. Hernandez-Alfaro et al (2008) and Proussaefs et al (2004) showed significant decrease in implant survival rates after the incidence of membrane perforation.4,15 However, Karabuda et al (2006), Becker et al (2008), Ding et al (2013), Froum et al (2013), Rickert et al (2013), and Cha et al (2014) did not find any significant differences in implant survival rates between the perforated and nonperforated side. The weighted average for the implant survival rate in the perforated side was 93% (95% CI, 84.7–101.2) ranging from 76.2% to 100%, and in the nonperforated side was 98.1% (95% CI, 93.6–102.5) ranging from 95.6% to 100% (Fig. 2).3,4,6,8,9,15,16 The difference in the weighted implant survival rates between perforated and nonperforated side was not statistically significant (P = 0.24) (Fig. 3). The random effects meta-analysis was applied, because there was evidence of considerable heterogeneity in implant survival rates (Tau2 = 3.02; Chi2 = 21.18, df = 6, P = 0.002; I2 = 72%).
The size of membrane perforation is a key factor in determining the change in survival rates. Hernandez-Alfaro et al4 discovered that as long as the size of sinus membrane perforation increases, the survival rate of implant placed under this reconstructed membrane decreases.
According to Proussaefs et al15 study, membrane perforation decreased bone formation in the perforated side (P < 0.0001). In a retrospective study of 359 augmented sinus, Nolan et al10 revealed that, when compared to their counterparts with intact membranes, sinuses with perforated membranes exhibit 3 times greater risk for bone graft failure (P = 0.003) and 6 times higher incidence of sinusitis/infection (P < 0.0006). Nevertheless, several other studies found that neither marginal bone loss around implant nor the absorption of sinus bone graft is affected by membrane perforation.3,6,7,16
This study comprehensively reviewed the incidence and burden of sinus membrane perforation. With a weighted incidence rate of 23.5% or approximately a ratio of 1:4, Schneiderian membrane perforation is still a common surgical complication occurring during sinus lift surgery. Surgeons can predict encountering 1 membrane perforation in every 4 procedures of sinus lift surgery.
The hard question here is, what are the risk factors that make membrane perforation more likely to occur. From physical viewpoint, the elasticity of Schneiderian membrane does tolerate its elevation without being perforated or even ruptured to a certain limit. Based on the results of an endoscopic study, the Schneiderian membrane appeared to tolerate up to 5 mm of elevation without perforating.17
Possible risk factors for Schneiderian membrane perforation can be classified into 3 categories:
- Anatomical risk factors, which include the presence of sinus septa (their number, location, and type), and thickness of Schneiderian membrane;
- Surgical risk factors, which include the surgical technique used (lateral vs osteotome approach), and the use of piezoelectric instrumentation; and
- Pathological risk factors, which include the presence of sinusitis or inflammatory-induced membrane changes.
Anatomical variations in Schneiderian membrane and sinus walls as well as sinus septa can predispose to sinus perforation. Several studies revealed an association between the presence of sinus septa and incidence of membrane perforations.1,3,5,13 Evading the negative effects of these anatomical variations requires earlier recognition in the surgical planning phase using special radiographic techniques such as cone beam computed tomography (CBCT).
Deep understanding of the modifiable surgical risk factors is an important component in avoiding the incidence of membrane perforation. During sinus lift procedure, stretching the membrane beyond its physical tolerance limits can lead to its perforation. The other factor to consider is the novice application of uncontrolled forces, when using the sharp cutting instruments. Recent instrumentation advances, increased experience in handling difficult thin membranes, and the introduction of piezoelectric surgery can play an important role in lessening and preventing the incidence of membrane perforation due to surgical risk factors.
The size of membrane perforation seems to affect implant survival. According to Hernandez-Alfaro et al,4 as long as the perforation size increases, the implant survival rate decreases. This inverse correlation is less prominent in recent studies, because surgeons nowadays are better equipped and trained to avoid the incidence of large perforations even with thin membranes. Nonetheless, once the perforation is confirmed, surgeons should exert every effort to avoid widening this perforation. We need to keep in mind that membrane perforation is associated with increased risk for bone graft failure and infection. Hence, the use of antibiotics can help not only in dodging these negative consequences but also in promoting both normal healing and typical surgical outcomes.
Conventional rotary instruments have been continually blamed for the incidence of membrane perforation. In contrast, the use of piezoelectric surgery appears to be promising in preventing membrane perforation, permitting adequate sinus lift, and maximizing patient satisfaction.1,5 The use of ultrasonic bone-cutting surgery allows cutting hard osseous tissues, while preserving the integrity of important anatomical structures.
Our study reveals no significant difference in the weighted implant survival rates between perforated and nonperforated side. To put it differently, appropriately handled and treated membrane perforation tend to show comparable implant survival when compared with intact membrane.
The management of Schneiderian membrane perforation starts immediately, once the perforation is confirmed. Gentle handling should be exerted with the avoidance of any unnecessary forces that can widen the size of perforation. Knowing the exact size of membrane perforation is important to determine the best course of action that the implantologist requires to follow (Table 5).1,18 In minor perforations of less than 1 mm, membrane folding on itself combined with a small collagen tape are usually sufficient measures to achieve appropriate closure that allows simultaneous implant placement. In small perforations between 1 and 3 mm, a collagen tape and a bioabsorbable membrane can suffice to close the perforation permitting simultaneous implant placement. In intermediate perforations between 3 and 6 mm, suturing and/or the application of fibrin adhesive is required. In most cases, closure of perforation needs to be supported with the use of bioabsorbable membrane and/or fixative tucks. If adequate closure can be achieved, implantologist can proceed with implant placement in the same session. In large perforations of greater than 6 mm, careful suturing and/or application of fibrin adhesive should be considered as well as the use of bioabsorbable membrane, that is placed only on the surface of sutured Schneiderian membrane.1,18 Fixative tucks are usually used to support the membrane and enhance bone healing. In all surgical management approaches, the osseous walls of the sinus are not covered with any membrane to maintain continuous blood supply to the bone graft.
Because the quality of the study, study design, and study population varied widely across studies addressing the risk factors and complications of membrane perforation, we could not synthesize the data quantitatively. Nevertheless, future research should focus on exploring the possible risk factors of sinus membrane perforation and its clinical consequences by means of longitudinal randomized controlled trials of large sample sizes.
With a weighted incidence rate of 23.5% (approximately a ratio of 1:4), Schneiderian membrane perforation is still a common surgical complication occurring during sinus lift surgery. Predisposing factors for membrane perforation include the reduced thickness of Schneiderian membrane and the presence of sinus septa. Although the difference in implant survival rates between perforated and nonperforated side is not significant, the size of membrane perforation seems to affect implant survival.
To achieve optimum patient care, early recognition and management of membrane perforation is necessary to reduce morbidity and to achieve higher patient satisfaction. We should keep in mind that appropriately handled and treated membrane perforation tend to show comparable implant survival when compared with intact membrane. Contemporary advancements in surgical techniques and methods aimed at preventing the perforation of Schneiderian membrane are promising.
The author claims to have no financial interest, either directly or indirectly, in the products or information listed in the article.
1. Al-Dajani M. Recent Trends in sinus lift surgery and their clinical Implications. Clin Implant Dent Relat Res. 2014;18:204–212.
2. CASP. CASP Checklists. Oxford: CASP Checklists; 2014.
3. Becker ST, Terheyden H, Steinriede A, et al.. Prospective observation of 41 perforations of the Schneiderian membrane during sinus floor elevation. Clin Oral Implants Res. 2008;19:1285–1289.
4. Hernandez-Alfaro F, Torradeflot MM, Marti C. Prevalence and management of Schneiderian membrane perforations during sinus-lift procedures. Clin Oral Implants Res. 2008;19:91–98.
5. Toscano NJ, Holtzclaw D, Rosen PS. The effect of piezoelectric use on open sinus lift perforation: A retrospective evaluation of 56 consecutively treated cases from private practices. J Periodontol. 2010;81:167–171.
6. Bae JH, Kim YK, Kim SG, et al.. Sinus bone graft using new alloplastic bone graft material (Osteon)-II: Clinical evaluation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109:e14–e20.
7. Ding X, Zhu XH, Wang HM, et al.. Effect of sinus membrane perforation on the survival of implants placed in combination with osteotome sinus floor elevation. J Craniofac Surg. 2013;24:e102–104.
8. Froum SJ, Khouly I, Favero G, et al.. Effect of maxillary sinus membrane perforation on vital bone formation and implant survival: A retrospective study. J Periodontol. 2013;84:1094–1099.
9. Cha HS, Kim A, Nowzari H, et al.. Simultaneous sinus lift and implant installation: Prospective study of consecutive two hundred seventeen sinus lift and four hundred sixty-two implants. Clin Implant Dent Relat Res. 2014;16:337–347.
10. Nolan PJ, Freeman K, Kraut RA. Correlation between Schneiderian membrane perforation and sinus lift graft outcome: A retrospective evaluation of 359 augmented sinus. J Oral Maxillofac Surg. 2014;72:47–52.
11. Barone A, Santini S, Marconcini S, et al.. Osteotomy and membrane elevation during the maxillary sinus augmentation procedure. A comparative study: Piezoelectric device vs. conventional rotative instruments. Clin Oral Implants Res. 2008;19:511–515.
12. Rickert D, Vissink A, Slater JJ, et al.. Comparison between conventional and piezoelectric surgical tools for maxillary sinus floor elevation. A randomized controlled clinical trial. Clin Implant Dent Relat Res. 2013;15:297–302.
13. Wallace SS, Mazor Z, Froum SJ, et al.. Schneiderian membrane perforation rate during sinus elevation using piezosurgery: Clinical results of 100 consecutive cases. Int J Periodontics Restorative Dent. 2007;27:413–419.
14. Cassetta M, Ricci L, Iezzi G, et al.. Use of piezosurgery during maxillary sinus elevation: Clinical results of 40 consecutive cases. Int J Periodontics Restorative Dent. 2012;32:e182–e188.
15. Proussaefs P, Lozada J, Kim J, et al.. Repair of the perforated sinus membrane with a resorbable collagen membrane: A human study. Int J Oral Maxillofac Implants. 2004;19:413–420.
16. Karabuda C, Arisan V, Ozyuvaci H. Effects of sinus membrane perforations on the success of dental implants placed in the augmented sinus. J Periodontol. 2006;77:1991–1997.
17. Engelke W, Deckwer I. Endoscopically controlled sinus floor augmentation. A preliminary report. Clin Oral Implants Res. 1997;8:527–531.
18. Fugazzotto PA, Vlassis J. A simplified classification and repair system for sinus membrane perforations. J Periodontol. 2003;74:1534–1541.
GRADE Working Group Grades of Evidence
High quality: Further research is very unlikely to change our confidence in the estimate of effect.
Moderate quality: Further research is likely to have an important impact on our confidence in the estimate of effect and may change the estimate.
Low quality: Further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate.
Very low quality: We are very uncertain about the estimate.