Mechanical properties of the Schneiderian membrane ...

Bernhard Pommer Ewald Unger Daniel Su¨to¨ Niklas Hack Georg Watzek

Mechanical properties of the Schneiderian membrane in vitro

Authors’ affiliations: Bernhard Pommer, Georg Watzek, Department of Oral Surgery, Bernhard Gottlieb School of Dentistry, Medical University of Vienna, Vienna, Austria Ewald Unger, Center for Biomedical Engineering and Physics, Medical University of Vienna, Vienna, Austria Daniel Su¨to¨, Department of Prosthodontics, Bernhard Gottlieb School of Dentistry, Medical University of Vienna, Vienna, Austria Niklas Hack, Institute of Medical Statistics, Medical University Vienna, Vienna, Austria

Key words: adhesion force, bone augmentation, mucosal elasticity, sinus floor elevation

Correspondence to: Dr Bernhard Pommer Department of Oral Surgery Bernhard Gottlieb School of Dentistry Medical University of Vienna Waehringer Strasse 25a A-1090 Vienna Austria Tel.: þ 43 1 4277 67011 Fax: þ 43 1 4277 67019 e-mail: [email protected]

well as membrane detachment from the adherent bone. Results: Perforation of the Schneiderian membrane (mean thickness: 90 mm) occurred at a

Abstract Objectives: Perforation of the Schneiderian membrane (maxillary sinus mucosa) is a common complication of maxillary sinus graft procedures. Membrane perforation increases the chance of postoperative sinusitis and endangers graft as well as implant survival. The aim of the present study was to explore the mechanical properties of the Schneiderian membrane. Material and methods: Three test methods were performed on sinus specimen of 20 fresh human cadavers: one- and two-dimensional membrane elongation as far as perforation, as

mean tension of 7.3 N/mm2. The membrane could be stretched to 132.6% of its original size in one-dimensional elongation, and to 124.7% in two-dimensional elongation. Thicker membranes demonstrated significantly higher load limits (Po0.001). The mean modulus of elasticity accounted 0.058 GPa, the mean adhesion force between sinus membrane and bone surface was 0.05 N/mm. Conclusions: Respecting the mechanical properties of the Schneiderian membrane may help reducing the complication rates and thus patient morbidity in minimally invasive maxillary sinus floor elevation.

Date: Accepted 7 October 2008 To cite this article: Pommer B, Unger E, Su¨to¨ D, Hack N, Watzek G. Mechanical properties of the Schneiderian membrane in vitro. Clin. Oral Impl. Res. 20, 2009; 633–637. doi: 10.1111/j.1600-0501.2008.01686.x

c 2009 John Wiley & Sons A/S

Postextraction alveolar bone resorption and pneumatization of the maxillary sinus frequently compromise the quantity and quality of available bone in the edentulous posterior maxilla (van den Bergh et al. 2000; Ferrigno et al. 2006). To permit reliable insertion of endosseous implants for prosthetic rehabilitation of this area, techniques for internal bone augmentation of the maxillary sinus floor have been established (Watzek et al. 1998; Lorenzoni et al. 2000). By coronal displacement of the Schneiderian membrane (maxillary sinus mucosa) with or without addition of bone (substitute) material, the formation of vital bone to allow osseointegration of delayed or

simultaneously placed implants is initiated (Berengo et al. 2004). Elevation of the sinus membrane is accomplished either via a lateral (Boyne & James 1980) or via a transcrestal (Summers 1994) approach to the antrum. Transcrestal elevation is indicated in case of initial residual bone height 44–5 mm, whereas the lateral approach can also be applied in case of severely resorbed ridges (Toffler 2004). Systematic reviews on the survival of implants placed in the grafted maxillary sinus revealed average implant survival rates between 91.5% and 92.6% for the lateral approach, compared with survival rates between 93.5% and 96.4% for the transcrestal

633

Pommer et al . Mechanical properties of the Schneiderian membrane

approach (Wallace & Forum 2003; Del Fabbro et al. 2004; Emmerich et al. 2005; Chiapasco et al. 2006). However, comparisons are difficult to be made, due to relevant differences in confounding variables, such as residual bone quantity and quality, grafting materials (or mixtures), implant geometry and surface, timing of implant placement and prosthetic loading, type of prosthesis and opposing arch dentition, patient-related factors, as well as implant success evaluation criteria (Chiapasco et al. 2006). The transcrestal approach to the maxillary sinus is advocated as ‘minimally invasive’ because of the undisturbed vascularization of the graft and less postoperative morbidity (Engelke et al. 2003). Besides the conventional osteotomemediated transcrestal elevation (Summers 1994), various minimally invasive surgical techniques have been proposed: i.e. membrane elevation by inflation of a balloon catheter (Soltan & Smiler 2005; Kfir et al. 2006), the use of hydraulic pressure (Chen & Cha 2005; Sotirakis & Gonshor 2005; Vitkov et al. 2005), and negative pressure (Suguimoto et al. 2006). The most common complication that occurs with all surgical techniques is the iatrogenic perforation of the Schneiderian membrane during elevation (Vlassis & Fugazzotto 1999; Ardekian et al. 2006). Membrane perforation rates have been reported to be 12–40% for the lateral approach (Khoury 1999; Mazor et al. 1999; De Leonardis & Pecora 2000). In transcrestal sinus elevation techniques perforation rates range between 2% and 25% (Berengo et al. 2004; Toffler 2004; Ferrigno et al. 2006). Perforation increases the chance of postoperative maxillary sinusitis due to bacterial graft contamination and/or graft migration into the sinus (Pikos 1999) and thus endangers graft as well as implant survival (Cho et al. 2001). Various options for managing these membrane tears during sinus augmentation via lateral antrostomy have been proposed, including closure with resorbable membranes (Mazor et al. 1999), fibrin adhesive (Sullivan et al. 1997), periostal patch (Nkenke et al. 2002), or resorbable sutures (Herna´ndez-Alfaro et al. 2008). However, when transcrestal ‘minimally invasive’ sinus augmentation techniques are applied, perforation of the Schneiderian membrane may not be recognized unless

634 |

Clin. Oral Impl. Res. 20, 2009 / 633–637

intraoperative antroscopy is carried out (Engelke & Deckwer 1997). Because of the limited access there is no possibility to repair the torn membrane without changing to a lateral surgical approach (Nkenke et al. 2002). The aim of the present study was to investigate the mechanical properties of the Schneiderian membrane in human cadaver specimen. Detailed knowledge on the load limits of the membrane may help avoiding iatrogenic perforations during maxillary sinus floor elevation and thus lowering the complication rate of the procedure.

Material and methods Sample material

Maxillae of 20 unfixed human cadavers (equal numbers of men and women, aged 56–87 years) were obtained from the Institute of Anatomy at Vienna Medical University, Austria. The sample material was derived from the floor and facial wall of the maxillary sinus by careful dissection immediately before experimentation. The time elapsing between sample retrieval and testing was kept to a minimum to preserve the elastic properties of the membrane samples. To prevent dehydration, the tissues were kept moistened in physiologic saline at room temperature. For the three different test methods planned, three types of sample specimen were obtained: 10 20 mm membrane stripes (n ¼ 39), 20 20 mm membrane squares (n ¼ 39), and 10 20 mm bone stripes with the sinus membrane still attached (n ¼ 22). The thickness of the membrane stripes and squares was assessed in the center of the membrane samples by two independent investigators (B. P. and E. U.) using an electronic micrometer caliper accurate s to 1 mm (Micromaster , Capa System, Switzerland).

Test methods

To investigate the mechanical properties of the Schneiderian membrane three test methods were performed using a tensile tester. One-dimensional elongation (Fig. 1): membrane stripes of 10 20 mm were clamped on both ends in an undilated position and stretched stepwise in increments of 1 mm until membrane perfora-

Fig. 1. One-dimensional membrane elongation test: the sinus membrane stripes were clamped on both ends (a) and continuously stretched (b) until perforation (c).

tion. Two-dimensional elongation (Fig. 2): membrane squares of 20 20 mm were mounted between clamping rings and centrally stretched by a spherical plunger of 3 mm diameter until perforation. Membrane detachment (Fig. 3): sinus wall bone stripes of 10 20 mm were installed into a mounting medium with the adherent membrane gripped in a clamp on one end and elevated continuously until complete detachment. The tensile force was recorded with a load cell between moving and fixed probe holder; the change in length was measured by counting the increments of the stepper motor with a constant speed of 1 mm/s (Roodenburg et al. 1990). Based on the load-elongation curves recorded during the elongation tests, following membrane characteristics were computed: burst elongation (increase in length from start until membrane perforation), burst tension (maximum load at the time of membrane perforation), and modulus of elasticity (tension per elongation). The adhesion force between the c 2009 John Wiley & Sons A/S


elongation was significantly lower than in one-dimensional testing (P ¼ 0.0018). It was found that membrane thickness had a highly significant influence on burst elongation (P ¼ 0.0001). The mean burst tension at the time of membrane perforation measured 7.3 4.2 N/mm2 (range: 2.3–12.5). No statistically significant difference in burst tension between the two test methods could be observed. The mean modulus of elasticity of the Schneiderian membrane was 0.058 0.03 GPa (range: 0.012–0.185). There was no statistically significant difference between the elastic modulus in one- and two-dimensional elongation. The adhesion force between the Schneiderian membrane and the bony maxillary sinus wall ranged between 0.015 and 0.103 N/mm with a mean of 0.05 0.025 N/mm.

Discussion

Fig. 2. Two-dimensional membrane elongation test: membrane squares were mounted between clamping rings (a) and centrally stretched by a spherical plunger (b) until perforation (c).

Schneiderian membrane and the underlying bone was calculated from the load measured during the membrane detachment test.

Fig. 3. Membrane detachment test: the Schneiderian membrane was clamped on one end (a) and continuously elevated from the underlying bone (b) until complete detachment (c).

(R Foundation for Statistical Computing, Vienna, Austria).

Statistical analysis

Mean, standard deviation, and median was calculated for each test method separately. For comparison of one- and twodimensional elongation, a mixed effect model with fixed factors ‘test method’ and ‘membrane thickness’ and random factor ‘specimen’ was used. Because differing variances in the two tests, variance estimation was performed separately for each test. P-values smaller than 0.05 were considered significant. All calculations were done using R-project software c 2009 John Wiley & Sons A/S

Results The mean thickness of the membrane samples amounted 90 45 mm (range: 24– 350, inter-observer variability not exceeding 5 mm) and did not differ significantly between the one- and two-dimensional test group (Table 1). The mean burst elongation measured 32.6 12.3% (range: 16.7–74.7) in one-dimensional testing and 24.7 4.7% (range: 15.2–35.5) in two-dimensional testing. In two-dimensional testing, burst

Avoidance of iatrogenic sinus membrane perforation is a great concern in transcrestal sinus augmentation techniques, as the elevation of the Schneiderian membrane is not performed under optic or tactile control and the access for membrane repair is limited (Toffler 2004). Membrane perforation in the course of maxillary sinus floor elevation can be attributed to inadequate surgical technique or to the presence of a thin sinus mucosa (Berengo et al. 2004). Additional risk factors comprise previous sinus surgery (ten Bruggenkate & van den Bergh 1998), absence of bone between sinus mucosa and oral mucosa (Watzak et al. 2005), and irregularities of the bony sinus floor, such as sharp ridges, antral septa, or spines (Krennmair et al. 1997; Ardekian et al. 2006). Chronic maxillary sinusitis and allergic conditions can lead to a thickened mucosa (van den Bergh et al. 2000) and even in healthy patients variations in the thickness of the Schneiderian membrane of up to 800 mm have been observed (Morgensen & Tos 1977). In the present investigation membrane thickness ranged between 24 and 350 mm, so it can be concluded that the tested membranes were not pathologically thickened, and the biomechanical properties of the unfixed human cadaver membranes should be comparable to those in healthy organisms. While the thickness of the Schneiderian

635 |



Table 1. Mechanical properties of the Schneiderian membrane: mean value standard deviation (median)

Membrane thickeness (mm) Burst elongation (%) Burst tension (N/mm2) Modulus of elasticity (GPa) Adhesion force (N/mm)

One-dimensional elongation (n ¼ 39)

Two-dimensional elongation (n ¼ 39)

Membrane detachment (n ¼ 22)

0.099 32.6 5.9 0.049 –

0.080 24.7 8.6 0.070 –

– – – – 0.050 0.025 (0.043)

0.056 (0.078) 12.3 (28.6) 2.5 (5.7) 0.019 (0.046)

membrane and maxillary sinus anatomy represent fixed risk factors for membrane perforation, the risk of rupture may be reduced by modification of the surgical elevation techniques. To predictably avoid sinus membrane perforation, elevation forces should be controlled by mechanical devices designed to regulate the applied pressure intraoperatively. The results of the present study can be utilized to calculate the critical perforation force by multiplying the burst tension of the sinus membrane (7.3 N/ mm2) by the area of force transmission (mm2). In osteotome-mediated membrane elevation (Summers 1994), the area of force transmission equals the surface area of the proximal end of the osteotome. Therefore higher forces can safely be applied using osteotomes with large diameters for elevation, due to the better load transfer. The area of force transmission is even larger when membrane elevation is achieved by inflation of a balloon catheter (Soltan & Smiler 2005; Kfir et al. 2006). An important question concerning minimally invasive sinus augmentation is, whether the obtainable amount of bone height is generally limited (Tepper et al. 2002; Engelke & Capobianco 2005) and therefore a conventional lateral approach

0.028 (0.072) 4.7 (25.7) 5.1 (8.3) 0.04 (0.070)

should be preferred in cases of severely resorbed maxillae (Nkenke et al. 2002). The average height of sinus elevation has been reported to range between 2.5 and 8.6 mm for transcrestal techniques (Nkenke et al. 2002; Engelke et al. 2003; Toffler 2004; Vitkov et al. 2005; Ferrigno et al. 2006; Nedir et al. 2006). In the course of transcrestal sinus floor elevation the force required for further membrane detachment increases along with the size of the elevated area. Applying the present results, the required detachment force may be calculated by multiplying the adhesion force between sinus membrane and underlying bone (0.05 N/mm) by the circumference of the elevated area (mm). The maximum height of membrane elevation is reached as soon as the required detachment force exceeds the critical perforation force of the sinus membrane. As the detachment force is correlated to the circumference of the elevated area, and the three-dimensional sinus anatomy significantly varies interindividually, the maximum elevation height obtainable with transcrestal techniques differs from patient to patient. In cases of narrow internal sinus anatomy the circumference of the elevated area is smaller, and thus the maximum elevation height is generally higher, compared with wide

sinuses. Three-dimensional radiographic imaging provides quantitative information on the precise maxillary sinus anatomy (Gahleitner et al. 2003). Combining this information with the presented data on the mechanical properties of the Schneiderian membrane, the obtainable amount of bone height may be determined preoperatively in patients subjected to transcrestal sinus floor elevation. The presented parameters (membrane thickness, burst elongation, burst tension, modulus of elasticity, and adhesion force) may as well be employed to investigate the dynamics of transcrestal membrane detachment using non-linear finite element analysis. In transcrestal sinus floor elevation techniques, elevation forces must be high enough to facilitate membrane detachment without exceeding its deformation capacity. No information on the load limits of the Schneiderian membrane and the force necessary for membrane detachment from the bony sinus floor has been available so far. The maximum elevation height is correlated to the elastic properties of the Schneiderian membrane and the quality of attachment to the underlying bony sinus floor (Berengo et al. 2004), as well as to the maxillary sinus anatomy and the surgical technique of force transmission. Respecting the load limits of the Schneiderian membrane may reduce complication rates and thus patient morbidity in minimally invasive sinus surgery.

Acknowledgements: The authors gratefully acknowledge the contributions of Univ. Prof. Dr Helmut Gruber at the Institute of Anatomy (Medical University of Vienna) for providing cadavers.

References Ardekian, L., Oved-Peleg, E., Mactei, E.E. & Peled, M. (2006) The clinical significance of sinus membrane perforation during augmentation of the maxillary sinus. Journal of Oral and Maxillofacial Surgery 64: 277–282. Berengo, M., Sivolella, S., Majzoub, Z. & Cordioli, G. (2004) Endoscopic evaluation of the boneadded osteotome sinus floor elevation procedure. International Journal of Oral and Maxillofacial Surgery 33: 189–194. Boyne, P.J. & James, R.A. (1980) Grafting of the maxillary sinus floor with autogenous marrow and bone. Journal of Oral Surgery 38: 613–616.

636 |


Chen, L. & Cha, J. (2005) An 8-year retrospective study: 1,100 patients receiving 1,557 implants using the minimally invasive hydraulic sinus condensing technique. Journal of Periodontology 76: 482–491. Chiapasco, M., Zaniboni, M. & Boisco, M. (2006) Augmentation procedures for the rehabilitation of deficient edentulous ridges with oral implants. Clinical Oral Implant Research 17 (Suppl. 2): 136–159. Cho, S.C., Wallace, S.S., Froum, S.J. & Tarnow, D.P. (2001) Influence of anatomy on Schneiderian membrane perforations during sinus elevation sur-

gery: three-dimensional analysis. Practical Periodontics and Aesthetic Dentistry 13: 160–163. De Leonardis, D. & Pecora, G.E. (2000) Prospective study on the augmentation of the maxillary sinus with calcium sulfate: histological results. Journal of Periodontology 71: 940–947. Del Fabbro, M., Testori, T., Francetti, L. & Weinstein, R. (2004) Systematic review of survival rates for implants placed in the grafted maxillary sinus. The International Journal of Periodontics and Restorative Dentistry 24: 565–577. Emmerich, D., Att, W. & Stappert, C. (2005) Sinus floor elevation using osteotomes: a systematic



review and meta-analysis. Journal of Periodontology 76: 1237–1251. Engelke, W. & Capobianco, M. (2005) Flapless sinus floor augmentation using endoscopy combined with CT scan-designed surgical templates: method and report of 6 consecutive cases. International Journal of Oral & Maxillofacial Implants 20: 891–897. Engelke, W. & Deckwer, I. (1997) Endoscopically controlled sinus floor augmentation. A preliminary report. Clinical Oral Implant Research 8: 527–531. Engelke, W., Schwarzwa¨ller, W., Behnsen, A. & Jacobs, H.G. (2003) Subantroscopic laterobasal sinus floor augmentation (SALSA): an up-to-5year clinical study. International Journal of Oral & Maxillofacial Implants 18: 135–143. Ferrigno, N., Laureti, M. & Fanali, S. (2006) Dental implants placement in conjunction with osteotome sinus floor elevation: a 12-year life-table analysis from a prospective study on 588 ITI implants. Clinical Oral Implant Research 17: 194–205. Gahleitner, A., Watzek, G. & Imhof, H. (2003) Dental CT: imaging technique, anatomy, and pathologic conditions of the jaws. European Radiology 13: 366–376. Herna´ndez-Alfaro, F., Torradeflot, M.M. & Marti, C. (2008) Prevalence and management of Schneiderian membrane perforations during sinus-lift procedures. Clinical Oral Implant Research 19: 91–98. Kfir, E., Kfir, V., Mijiritsky, E., Rafaeloff, R. & Kaluski, E. (2006) Minimally invasive antral membrane balloon elevation followed by maxillary bone augmentation and implant fixation. Journal of Oral Implantology 32: 26–33. Khoury, F. (1999) Augmentation of the sinus floor with mandibular bone block and simultaneous implantation: a 6-year clinical investigation. International Journal of Oral & Maxillofacial Implants 14: 557–564. Krennmair, G., Ulm, C. & Lugmayr, H. (1997) Maxillary sinus septa: incidence, morphology and clinical implications. Journal of Cranio-Maxillo-Facial Surgery 25: 261–265. Lorenzoni, M., Pertl, C., Wegscheider, W., Keil, C., Penkner, K., Polansky, R. & Bratschko, R.O.


(2000) Retrospective analysis of Frialit-2 implants in the augmented sinus. The International Journal of Periodontics and Restorative Dentistry 20: 255–267. Mazor, Z., Peleg, M. & Gross, M. (1999) Sinus augmentation for single-tooth replacement in the posterior maxilla: a 3-year follow-up clinical report. International Journal of Oral & Maxillofacial Implants 14: 55–60. Morgensen, C. & Tos, M. (1977) Quantitative histology of the maxillary sinus. Rhinology 15: 129–134. Nedir, R., Bischof, M., Vazquez, L., SzmuklerMoncler, S. & Bernard, J.P. (2006) Osteotome sinus floor elevation without grafting material: a 1-year prospective pilot study with ITI implants. Clinical Oral Implant Research 17: 679–686. Nkenke, E., Schlegel, A., Schultze-Mosgau, S., Neukam, F.W. & Wiltfang, J. (2002) The endoscopically controlled osteotome sinus floor elevation: a preliminary prospective study. International Journal of Oral & Maxillofacial Implants 17: 557–566. Pikos, M.A. (1999) Maxillary sinus membrane repair: report of a technique for large perforations. Implant Dentistry 8: 29–34. Roodenburg, J.L.N., ten Bosch, J.J. & Borsboom, P.C.F. (1990) Measurement of the uniaxial elasticity of oral mucosa in vivo after CO2-laser evaporation and surgical excision. International Journal of Oral and Maxillofacial Surgery 19: 181–183. Soltan, M. & Smiler, D.G. (2005) Antral membrane balloon elevation. The Journal of Oral Implantology 31: 85–90. Sotirakis, E.G. & Gonshor, A. (2005) Elevation of the maxillary sinus floor with hydraulic pressure. The Journal of Oral Implantology 31: 197–204. Suguimoto, R.M., Trindade, I.K. & Carvalho, R.M. (2006) The use of negative pressure for the sinus lift procedure: a technical note. International Journal of Oral & Maxillofacial Implants 21: 455–458. Sullivan, S.M., Bulard, R.A., Meaders, R. & Patterson, M.K. (1997) The use of fibrin adhesive in sinus lift procedures. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 84: 616–619.

Summers, R.B. (1994) The osteotome technique. Part 3 – less invasive methods of elevating the sinus floor. Compendium of Continuing Education in Dentistry 15: 698–708. ten Bruggenkate, C.M. & van den Bergh, J.P. (1998) Maxillary sinus floor elevation: a valuable preprosthetic procedure. Periodontology 2000 17: 176–182. Tepper, G., Haas, R., Zechner, W., Krach, W. & Watzek, G. (2002) Three-dimensional finite element analysis of implant stability in the atrophic posterior maxilla: a mathematical study of the sinus floor augmentation. Clinical Oral Implant Research 13: 657–665. Toffler, M. (2004) Osteotome-mediated sinus floor elevation: a clinical report. International Journal of Oral & Maxillofacial Implants 19: 266–273. van den Bergh, J.P., ten Bruggenkate, C.M., Disch, F.J. & Tuinzing, D.B. (2000) Anatomical aspects of sinus floor elevations. Clinical Oral Implant Research 11: 256–265. Vitkov, L., Gellrich, N.C. & Hannig, M. (2005) Sinus floor elevation via hydraulic detachment and elevation of the Schneiderian membrane. Clinical Oral Implant Research 16: 615–621. Vlassis, J.M. & Fugazzotto, P.A. (1999) A classification system for sinus membrane perforations during augmentation procedures with options for repair. Journal of Periodontology 70: 692– 699. Wallace, S.S. & Forum, S.J. (2003) Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Annals of Periodontology 8: 328–343. Watzak, G., Tepper, G., Zechner, W., Monov, G., Busenlechner, D. & Watzek, G. (2005) Bony press-fit closure of oro-antral fistulas: a technique for pre-sinus lift repair and secondary closure. Journal of Oral and Maxillofacial Surgery 63: 1288–1294. Watzek, G., Weber, R., Bernhart, T., Ulm, Ch. & Haas, R. (1998) Treatment of patients with extreme maxillary atrophy using sinus floor augmentation and implants: preliminary results. International Journal of Oral and Maxillofacial Surgery 27: 428–434.

637 |
