Evaluation of Sinus Membrane Perforation in Osteotome Sinus Floor Elevation With and Without Grafting

Sinus floor elevation and augmentation are preprosthetic surgical procedures performed in the edentulous posterior maxilla, via 2 main techniques called the lateral window approach and transcrestal sinus floor elevation. Osteotome sinus floor elevation (OSFE), which was first suggested by Tatum¹  and modified by Summers,²  uses a set of tapered osteotomes with increasing diameters and remains one of the most preferred methods of transcrestal sinus floor elevation. In the original technique, Tatum did not use any graft material to increase and maintain the elevated area, but Summers described the bone-added OSFE using a graft material placed in the space between the sinus membrane and the superior extent of the alveolar bone. As the height of the elevated sinus membrane increases, the need for graft use increases. It has been suggested that the use of a graft material stimulates new bone formation in the sinus and contributes to long-term implant stability in cases in which the vertical membrane elevation is >2–3 mm.^3,4 

The autograft is accepted as the gold standard in terms of osteogenic properties and minimizing the risk of infection.^5,6  Because autogenous bone has some disadvantages, including donor site morbidity, limited availability, graft resorption, and extended operative time, other bone substitutes including xenografts, alloplasts, allografts, growth factors, and all combinations of these have been commonly preferred for sinus augmentation. In a case series, it was reported that the use of autogenous bone particles in combination with a xenograft provided a better radiographic view and reduced the need for harvesting bone from distant donor sites.⁷  In a different case series, bovine bone and calcium sulfate were used in OSFE, and it was found that the use of calcium sulfate improved the handling properties of bovine bone and helped to stabilize the graft particles during healing.⁸  In an experimental study, Xu et al⁹  investigated the effect of graft particle size on new bone formation in sinus augmentation and reported that newly formed bone showed higher density and many interconnections in the small-particle group compared with the large-particle group. On the other hand, a literature review focusing on implant survival, bone grafting, and anatomical and surgical considerations in sinus lift surgery reported that both implant osseointegration and marginal bone loss are not dependent on the type of bone graft used for sinus augmentation.¹⁰  It should be noted that any bone graft is placed blindly into the space below the sinus membrane, and inadequate visibility of the sinus during the placement of the graft material is considered to be a drawback of transcrestal sinus grafting.¹¹  Inadequate visibility is not only a drawback during graft placement but also a problem during blind elevation of sinus membrane and can cause sinus membrane perforation, which is the most common intraoperative complication of sinus augmentation procedures.¹² 

Bone graft placement has been accepted as one of the time points for sinus membrane perforation.¹³  Garbacea et al¹⁴  suggested that there are several factors related to the graft material used that trigger membrane perforation, including the amount, level of hydration, and size and configuration of the bone graft particles. Overfilling of the graft material into the sinus might stretch the membrane beyond its elastic limit and cause perforation. In addition to the graft volume, an irregular and sharp geometry of the bone graft particles leads to potential membrane disruption, especially in thinner areas of the expanded or stretched membrane.¹⁴  At every stage of OSFE, the integrity of the sinus membrane can be checked by direct visualization and the Valsalva maneuver. Cone-beam computerized tomography (CBCT) has become an important tool for the postoperative detection of membrane perforations.^15,16 

The hypothesis of this study is that there is no difference in the effects of graft materials on sinus membrane perforation in OSFE. Therefore, the aim of the present study was to evaluate the rate of sinus membrane perforation in OSFE performed with and without graft material using CBCT.

This prospective cohort study was performed in accordance with the Declaration of Helsinki and was approved by the appropriate institutional ethics committee (study No. 2017/09-51 [KA-17118]). Written informed consent was obtained from all patients included in the study.

Adult patients were eligible for inclusion in this study if they had at least 1 unilateral edentulous area in the posterior maxilla and required implant treatment. Tooth extractions in the implant area were completed at least 3 months prior to OSFE. There were no prerequisites in terms of minimum bone height at the surgical site. Patients were excluded if they had uncontrolled metabolic diseases such as osteoporosis and diabetes, history of oral or intravenous bisphosphonate intake, radiotherapy in the head and neck region, presence of acute or chronic sinusitis, any operation in the maxillary sinuses, or a habit of smoking >10 cigarettes daily.

Patients were nonrandomly allocated to the control group (OSFE performed without graft material) and the test groups (OSFE performed with either the particulate autograft or the xenograft). In the test groups, the graft material was gradually inserted into the sinus using osteotomes, with simultaneous elevation of the membrane. In the control group without graft material, the alveolar bone was pushed into the sinus using osteotomes, with simultaneous elevation of the membrane.

All surgical procedures were performed under local anesthesia. A modified OSFE technique reported by Davarpanah et al¹⁷  was applied in all patients for sinus augmentation. Following a midcrestal incision, the implant location was marked on the alveolar crest with a round bur. An implant bed was prepared 1 mm below the sinus floor with the pilot drill of the implant system, and the 1 mm of residual bone was gradually pushed into the sinus with or without graft material, with simultaneous membrane elevation.

In the autograft group, the graft material was harvested from the maxillary tuberosity using bone forceps and used in a particulate form (Figure 1). In the xenograft group, the graft material used in the study was produced from bovine bone and prepared into a granular form (Cerabone granulate 1.0–2.0 mm, Botiss Dental, Dieburg, Germany). The volume of the graft material was measured using the water displacement method during the procedure. To measure the graft volume, a dental injector was filled with saline solution up to 1 mL. The graft material was placed into the injector, and the increase in the volume of the solution was recorded as the volume of the graft material (Figure 2).

Radiographic measurements were obtained from CBCT images (Morita Veraviewepocs X700 3D R-100 P, Kyoto, Japan) obtained preoperatively and immediately after the surgery. The tube potential, tube current, and rotation time were set to 90 kVp, 8 mA, and 9.4 seconds, respectively. All images were taken with a slice thickness of 1 mm and a field of view of 100 × 80 mm. The aim of preoperative CBCT was to assess the residual bone height (RBH), residual bone width, and membrane thickness and examine the sinus for inflammation, cysts, or other pathologies; CBCT images obtained immediately postoperatively were used to reveal the endo-sinus bone gain and sinus membrane perforation. The endo-sinus bone gain was measured by subtracting the preoperative RBH from the postoperative bone height.

Sinus membrane perforation was checked intraoperatively using both the Valsalva maneuver and immediate postoperative CBCT images. Extensively increased density in the sinus and dislocation of the graft material were criteria accepted as indicating membrane perforation in the CBCT. A dome-shaped protrusion of the graft material into the sinus was deemed to indicate success of sinus augmentation (Figure 3). Figure 4 and Figure 5 show the preoperative and postoperative CBCT images of 2 different patients without and with sinus membrane perforation during OSFE. In Figure 4a, the RBH was measured as 0.95 mm, the sinus membrane thickness was normal, and the sinus cavity was healthy based on a coronal section of CBCT. A dome-shaped view of autogenous graft in the sinus was considered to indicate that the sinus membrane remained intact after OSFE (Figure 4b). In the other patient, the RBH was 1.6 mm and the sinus membrane was thickened preoperatively, but the dislocation of the autogenous graft material and increased sinus density observed on CBCT images were regarded as indicating membrane perforation (Figure 5a and b). The same researcher (Ç.K.) evaluated the sinus membrane perforation and measured the endo-sinus bone gain on CBCT images at two different time points.

All patients were prescribed oral antibiotics (amoxicillin-clavulanic acid, 2 × 1, for 10 days), nonsteroidal anti-inflammatory analgesics (naproxen sodium, 2 × 1, for 5 days), antiseptic mouthwashes (chlorhexidine gluconate, 3 × 1, for 10 days), nasal decongestants (oxymetazoline hydrochloride, 1 × 1, for 5 days), and oral antihistamines (cetirizine, 1 × 1, for 5 days) postoperatively. All patients were advised nasal precautions such as opening the mouth while sneezing, not creating pressure during nasal cleaning, and not smoking (for 3 days to avoid the wound dehiscence in early period) in the postoperative period. Sutures were removed 7–10 days postoperatively.

The data collected were evaluated using IBM SPSS Statistics software. Descriptive statistics are used to indicate the means, medians, and minimum and maximum values in each treatment group. Differences in graft volume based on graft type were tested using Bonferroni adjustments. Fischer's exact test was used to analyze the differences in sinus membrane perforation between the graft types. The Mann-Whitney U test was used to analyze the difference in sinus membrane perforation with regard to graft volume. Differences in endo-sinus bone gain according to graft volume were analyzed using the Kruskal-Wallis test. Differences in the sinus membrane perforation rate with regard to the endo-sinus bone gain were analyzed using the t test according to the tests of normality and test of homogeneity of variance. Differences in graft materials according to RBH were analyzed using analysis of variance, and comparisons between the graft groups were tested using Bonferroni adjustments. The 95% confidence intervals were calculated. The level of significance was set at P < .05. The intraclass correlation coefficient (ICC) was used to evaluate the reliability of the measurements performed by the same researcher (Ç.K.) at 2 different time points. The reliability was defined as “poor” if the ICC was <.40, “acceptable” if the ICC was between .40 and .70, and “good” for ICC values >.70. The methodology and results of the study were reviewed by an independent statistician (H.Y.Z.).

Between October 2017 and December 2018, 30 patients (16 women and 14 men) with 52 OSFE sites were enrolled; the mean age of the patients was 48 years (range, 26–68 years). Among the study participants, the median RBH was 6.25 mm (range 1.27–11.31 mm), and the median bone width was 7.58 mm (range 4.43–14.72 mm). The median membrane thickness was 1.12 mm (range 0–15.49 mm). The rate of sinus membrane perforation was 15.4% (8/52 OSFE sites).

Of the 52 OSFE procedures, 26.9% were performed without a graft material (control group), and 34.6% and 38.5% were performed with autograft and xenograft material, respectively (test groups). The mean RBHs were 7.79 ± 1.609 mm, 5.77 ± 2.596 mm, and 5.70 ± 1.675 mm in the control group, particulate autograft, and xenograft groups, respectively. The difference between the ungrafted and grafted groups was statistically significant (P = .009), but no statistically significant difference was found between the autograft and xenograft groups (P = 1). In terms of membrane perforation, a statistically significant difference was found between the control and test groups (P = .033). Table 1 shows the correlation between graft type and the sinus membrane perforation rate.

The median volume of the graft materials was 0.3 mL (range 0–1 mL). The median volumes of autograft and xenograft were 0.4 mL. The difference in graft volumes between the autograft and xenograft groups was not statistically significant (P = .768). In patients with membrane perforation, the graft volume was 0.35 mL, while in those without membrane perforation, the graft volume was 0.2 mL. Although the median graft volume was higher in patients with membrane perforation, no statistically significant correlation was found between graft volume and membrane perforation (P = .187). In the study, the median value of endo-sinus bone gain was 6.57 mm (range 1.91–12.98 mm). The mean endo-sinus bone gain was 4.38 mm, 9.05 mm, and 6.69 mm in the control, autograft, and xenograft groups, respectively. The difference in endo-sinus bone gain between the graft and control groups was statistically significant (P = .002). The mean endo-sinus bone gain was 6.55 ± 2.573 mm in patients without membrane perforation and 8.71 ± 2.674 mm in patients with membrane perforation. This difference was statistically significant (P = .035). Table 2 shows the distribution of graft type, graft volume, and endo-sinus bone gain.

With regard to the measurements performed at the 2 different time points, the ICC varied between .944 and .955. The reliability of the measurements was regarded as “good.”

In this study, the modified OSFE technique was used in 52 surgical sites in the maxillary posterior region. The patients were divided into 3 groups according to the graft material used in sinus augmentation, and membrane perforation related to the graft material was evaluated using CBCT images.

The sinus membrane is thought to have osteogenic potential, inducing new bone formation around the inserted implants.¹⁸  Spontaneous bone formation of up to 2–3 mm in the elevated sinus has been already confirmed in an animal study.¹⁹  However, the amount of new bone formation decreases as the protruded length of an implant increases in OSFE without a graft material.⁴  The graft material is thought to improve primary stability by providing more bone in which the implant can anchor.²⁰  Moreover, the application of a graft material creates and maintains the space for new bone formation.⁴  In the literature, an increase in RBH from 3 mm to 9 mm has been reported in OSFE, both with and without grafting.¹⁰  In a different study, the average bone gain in OSFE was reported to be between 2.28 mm and 5.55 mm.²¹  In our study, the mean increase in RBH was 4.38 mm, 9.05 mm, and 6.69 mm without grafting, with autograft, and with xenograft, respectively. While no membrane perforation was observed in the control group, the highest amount of membrane perforation was observed in the autograft group. In this study, the particulate autograft was harvested from the maxillary tuberosity area with bone forceps and had irregular particle shapes and sizes, with sharp or round margins. On the other hand, the bovine bone used was a commercial product, and its particle size and shape were standardized. An autogenous material with sharp margins can traumatize the sinus membrane, resulting in laceration or perforation. The higher membrane perforation observed in the autograft group can be attributed to the physical properties of the graft material. The autogenous corticocancellous block graft with smoother and sharper margins can also be used in OSFE. Using a bone block graft is recommended to prevent the spreading of the particulated bone graft in case of membrane perforation.²²  When the membrane is perforated during sinus floor elevation, the perforation area will be in direct contact with the block graft. Sindel et al²³  reported a case series in which they performed lateral sinus lifting with autogenous bone ring locked by an implant in patients with membrane perforation. They emphasized that the surgery was completed using only autogenous bone ring blocks without additional materials to repair the membrane perforation.²³  However, harvesting autogenous bone block graft increases postoperative morbidity as compared with harvesting autogenous particulated graft and complicates OSFE with simultaneously implant placement. Therefore, to minimize the risk of membrane tearing, a bone grinder may be used to eliminate the sharp and irregular margins of the autogenous particulated graft.

Measuring the graft volume needed in sinus augmentation helps to prevent membrane perforation due to overfilling. In this study, the median volumes of both autograft and xenograft materials were 0.4 mL. In sinus augmentations, the endo-sinus bone gain increases statistically as the graft volume used increases; however, the possibility of membrane perforation should not be ignored while considering the amount of bone gain. In our study, the median graft volume was 0.2 mL, and the mean endo-sinus bone gain was 6.55 mm in patients without membrane perforation. A clinical study, which investigated the association between graft volume and obtained sinus membrane elevation using CBCT, reported that 0.3 mL of bone graft can ensure 6 mm of vertical gain with a low risk of membrane perforation.¹³  A cadaver study found a significant positive correlation between vertical elevation and membrane perforation and advocated a safe elevation of 5 mm without bone graft for implant placement using the transcrestal approach. In contrast, those authors found a lack of correlation between the graft volume and membrane perforation.²⁴  In our study, the volume of graft material used was measured using the water displacement method during the operation, but the volume of the 1 mm of residual bone sent into the sinus was neglected in all groups. The water displacement method has been commonly used to measure the graft volume intraoperatively.^25,26  Moreover, the frequent use of computerized tomography enables the digital measurement of graft volume. Verdugo et al²⁷  evaluated the mandibular symphysis volume using both the water displacement method and AutoCAD software program using computerized tomography and reported a statistically significant difference between the 2 techniques.²⁷  However, in our study, CBCT images were obtained preoperatively and immediately postoperatively. In addition, the graft materials used in this study were particulate. Therefore, the water displacement method was thought to be a suitable and useful method for measuring graft volume in our study.

The Valsalva maneuver and direct visualization are almost always used to detect membrane perforation during sinus augmentation. However, recent endoscopic and microscopic studies have suggested that these techniques can cause false-positive or false-negative results regarding membrane perforation.^14,22,24  Nkenke et al²²  detected a case of membrane perforation by endoscopy during surgery, although the Valsalva maneuver was negative. In a cadaver study, the incidence of membrane perforation during transcrestal sinus floor elevation was 50% endoscopically.²⁴  Similar results were found in different endoscopic and microscopic studies with rates of 40% and 40.62%, respectively.^14,24  Garbacea et al¹⁴  suggested that endoscopy was the most reliable method to confirm membrane perforation, and CBCT was determined to be more accurate than digital periapical radiographs when compared with direct visualization with the endoscope. In our study, membrane perforation was determined using the Valsalva maneuver and CBCT images. The membrane perforation rate was 15.4% on CBCT, although the Valsalva maneuver outcome was negative in all procedures. Apart from evaluating the membrane perforation with CBCT, the membrane thickness, RBH, and endo-sinus bone gain were also measured on CBCT images. Although CBCT is not accepted as the gold standard for determining membrane perforation, the use of CBCT for preoperative evaluation for implants with sinus grafting has been recommended by a consensus report.²⁸ 

One of the limitations of this study is its small sample size and nonrandom allocation. The lack of randomization of the small study groups prevented us from explaining the exact relationship between the graft type and the membrane perforation rate in OSFE. Another limitation of this study is that while evaluating the effect of graft materials on membrane perforation, other risk factors such as the RBH, membrane thickness, and extent of vertical membrane elevation, which cause membrane perforation, could not be standardized through the study.

In this study, sinus membrane perforation related to the graft material was evaluated in OSFE. Overall, the rate of sinus membrane perforation was 15.4%, and the highest perforation rate was found in the autograft group. In the study, the median graft volume was 0.2 mL and the mean endo-sinus bone gain in patients without membrane perforation was 6.55 ± 2.573 mm. Therefore, the hypothesis of this study is rejected. The volume and physical properties of graft materials are important factors in membrane perforation. When the particulated autogenous bone graft is used in sinus-lifting procedures, the sharp margins of the graft material may be corrected to reduce the risk of membrane perforation. However, further clinical studies with larger and standardized sample groups are needed to confirm the effects of the characteristics of graft materials on sinus membrane perforation in transcrestal sinus augmentation.

Abbreviations

CBCT:

cone-beam computerized tomography

ICC:

intraclass correlation coefficient

OSFE:

osteotome sinus floor elevation

RBH,

residual bone height

This study was supported by the Hacettepe University Scientific Research Projects Coordination Unit (grant No. THD-2018-16983). The authors thank Assistant Professor Hatice Yağmur Zengin, Hacettepe University, Faculty of Medicine, Department of Biostatistics, for reviewing the methodology and results of the study.