J Oral Maxillofac Surg 68:1327-1333, 2010

New Bone Formation in the Maxillary Sinus Using Only Absorbable Gelatin Sponge
Dong-Seok Sohn, DDS, PhD,* Jee-Won Moon, DDS, Kyung-Nam Moon, DDS, MSD, Sang-Choon Cho, DDS, and Pil-Seoung Kang, DDS
Purpose: The purpose of the present study was to evaluate the predictability of new bone formation

in the maxillary sinus using only absorbable gelatin as the graft material.
Patients and Methods: Seven patients (9 sinus augmentations) were consecutively treated with sinus

oor elevation by the lateral window approach. The lateral bony window was created using a piezoelectric device and the schneiderian membrane was elevated to make a new compartment. After 18 resorbable blast media surfaced dental implants were simultaneously placed, absorbable gelatin sponges were loosely inserted to support the sinus membrane over the implant apex and the bony portion of lateral window was repositioned to seal the lateral window. Results: After uncovering the implants an average of 6 months after placement, new bone consolidation in the maxillary sinus was observed on radiographs without bone graft. Two implants were removed due to failed osseointegration on uncovering. Failures were caused by insufcient initial stability. Conclusion: This study suggests that placement of a dental implant in the maxillary sinus with a gelatin sponge can be a predictable procedure for sinus augmentation. 2010 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 68:1327-1333, 2010 The widespread use of dental implants for replacement of missing teeth has led to complex surgical procedures to increase the amount of available bone. Placement of dental implants on the edentulous posterior maxilla could present difculties due to a de*Chairman and Professor, Department of Dentistry and Oral and Maxillofacial Surgery, Daegu Catholic University Hospital, Daegu, Republic of Korea. Resident, Department of Dentistry and Oral and Maxillofacial Surgery, Daegu Catholic University Hospital, Daegu, Republic of Korea. Private Practice, Hanbit Dental Clinic, Jeju, Korea. Assistant Research Scientist, Clinical Assistant Professor, Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, NY. Resident, Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, NY. Address correspondence and reprint requests to Dr Sohn: Department of Oral and Maxillofacial Surgery, Catholic University Hospital of Daegu, 3056-6 Daemyung-4 Dong, Namgu, Daegu, Republic of Korea; e-mail: dssohn@cu.ac.kr
2010 American Association of Oral and Maxillofacial Surgeons

0278-2391/6806-0018$36.00/0 doi:10.1016/j.joms.2010.02.014

cient posterior alveolar ridge, unfavorable bone quality, and increased pneumatization of the maxillary sinus.1,2 Increased implant failure rates in the posterior maxilla are related to insufcient residual height and poor bone quality.3,4 Such problems have been overcome by increasing the alveolar height with maxillary sinus augmentation.5,6 The lateral window approach is a commonly used technique for maxillary sinus augmentation, especially when the initial alveolar bone height cannot ensure the primary stability of simultaneous placement of implants.5-7 Numerous studies have documented the technical details for the lateral window method, and these procedures have shown clinical predictability.6-9 The sinus augmentation procedure is usually accomplished by creating a lateral bony window followed by elevation of the schneiderian membrane. The space created between the maxillary alveolar process and the elevated schneiderian membrane is typically lled with autografts, allografts, xenografts, alloplasts, or combinations of different graft materials to maintain space for new bone formation.6,10-15 Several studies have reported that factors such as the volume of graft material, the kinds of bone graft, and the amount of autogenous bone affect the amount of new bone formation,

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1328 and most of these studies have shown a correlation between the success of the bone graft and the success of dental implants.6,10-15 Elevating the maxillary sinus membrane and grafting with bone substitutes has become routine treatment over the past 40 years, and some studies have reported successful bone formation and osseointegration in cases of performing sinus membrane elevation without bone grafts.16-19 The aim of this study was to verify new bone formation by radiologic results by application of only an absorbable gelatin sponge (Cutanplast; Mascia Brunelli Spa, Milano, Italy) in the space between the elevated schneiderian membrane and simultaneously placed implants.

BONE FORMATION USING ABSORBABLE GELATIN

quality, and any existing sinus pathology were evaluated on these radiographs. The bone height of the remaining alveolar ridge was 1.5 to 7.0 mm (average, approximately 5.0 mm; Table 1). Patients were consecutively treated with sinus oor elevation by the lateral window approach. Patients who had previous failed sinus augmentations, who exhibited pathologic ndings or had a history of maxillary sinus diseases or operations, or whose medical conditions might increase surgical risks of the research protocol were excluded.
SURGICAL PROCEDURES

Patients and Methods

PATIENT SELECTION

The present study population consisted of 7 consecutive patients, 6 men and 1 woman, 40 to 75 years of age (mean age, 56.1 years). All patients were informed about the treatment procedure and provided written consent for participation, and this study was approved by the institutional review board of the Catholic Medical Center of Daegu. The patients presented with a partially or fully edentulous atrophic maxilla with sinus pneumatization. Preoperative examinations with panoramic views and dental conebeam computed tomographic scans (Combi, Pointnix, Seoul, Korea; or Implagraphy, Vatec, Kyungi, Korea) were performed. Available bone volume, bone

Prophylactic oral antibiotics (cefditoren pivoxil 300 mg 3 times/day; Meiact, Boryung Pharmacy, Seoul, Korea) were used routinely, beginning 1 day before the procedure and continuing for 7 days. Surgery was performed under local anesthesia through maxillary block anesthesia using 2% lidocaine that includes 1:100,000 epinephrine. Flomoxef sodium (Flumarin; Ildong Pharmaceutical Co, Seoul, Korea) 500 mg intravenously was administered 1 hour before surgery. Maxillary sinus oor elevation by the lateral approach was completed in all participants. The approach to the lateral wall of the maxillary sinus was followed after the elevation of a mucoperiosteal ap according to surgical needs. A piezoelectric saw (S-Saw; Bukboo Dental Co, Daegu, Korea), connected to a piezoelectric device (Surgybone; Silfradent Srl, Soa, Italy), was used with copious saline irrigation to create the lateral window of the maxillary sinus (Fig 1). The anterior vertical osteotomy was made 2 mm distal to the

Table 1. DATA ON STUDY PARTICIPANTS

Patient No. 1 2 3 4 5 6 7

Age Gender (yr) Male Male Male Female Male Male Male

Site

Mean Residual Bone Height Membrane (mm) Perforation 5.5 3.5 5.0 5.0 7.0 6.5 1.5 No No No Yes No No No

Implant System SybronPRO XRT SybronPRO XRT SybronPRO XRT SybronPRO XRT SybronPRO XRT SybronPRO XRT SybronPRO XRT

Implant Diameter Length (mm) 4.1 4.1 4.1 4.1 4.1 4.1 4.1 13 13 13 13 13 13 13

Healing Time (mo) 6 6 6 6 6 6 6

75 R max second and rst molars, L max rst and second molars 40 L max rst and second molars 51 R max second and rst molars and second premolar 62 L max rst and second molars 45 R max second and rst molars, L max rst and second molars 52 R max second and rst molars 68 R max second molar

Abbreviations: R, right; L, left; max, maxillary.

Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

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FIGURE 1. A piezoelectric saw (S-Saw; Bukboo Dental Co, Daegu, Korea), connected to a piezoelectric device (Surgybone; Silfradent Srl, Soa, Italy), was used to create the lateral window of the maxillary sinus in all cases (patient 4). Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

FIGURE 3. The lateral bony window was repositioned without additional procedures (patient 6). Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

anterior vertical wall of the maxillary sinus and the distal osteotomy was made approximately 20 mm away from the anterior vertical osteotomy. The height of the vertical osteotomy was approximately 10 mm. The anterior and inferior osteotomy line was created perpendicular to the inside of the maxillary sinus lateral wall, and then superior and posterior osteotomies perpendicular to the sinus wall were performed. This design of osteotomy facilitates the precise replacement of the bony window as a barrier over an inserted gelatin sponge in the maxillary sinus. The bony window was detached carefully to expose the sinus membrane. The schneiderian membrane was

FIGURE 2. After elevation of the schneiderian membrane and placement of implants, an absorbable gelatin sponge (Cutanplast; Mascia Brunelli Spa, Viale Monza, Italy) 70 50 1 mm was divided into 3 pieces and inserted into spaces anterior and posterior to the implants and below the elevated schneiderian membrane (patient 6). Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

carefully dissected from the sinus oor walls with a at blunt-edged instrument. Dissection of the sinus membrane was continued to reach the medial and posterior walls of the sinus cavity. After elevation of the schneiderian membrane and placement of implants (SybronPRO XRT implants; Sybron Implant Solution, Grendora, CA), an absorbable gelatin sponge (70 50 1 mm; Cutanplast) was divided into 3 pieces. The pieces were folded and inserted into the new compartment of the maxillary sinus. One piece of gelatin sponge was placed anterior to the implant site, 1 posterior to the site, and 1 directly above the implant apex to support the membrane (Fig 2). The bony portion of the lateral window was repositioned to prevent soft tissue ingrowth into the sinus cavity and to promote new bone formation from the lateral wall of the maxillary sinus (Fig 3). Flaps were sutured using interrupted mattress polytetrauoroethylene sutures (Cytoplast; Osteogenic Biomedical, Lubbock, TX) to achieve passive primary closure. Patients were instructed not to blow their nose for 2 weeks after surgery and to cough or sneeze with an open mouth. Preoperative prophylactic antibiotic therapy was continued postoperatively for 7 days, and the sutures were removed 14 days postoperatively. After sinus augmentation, postoperative panoramic radiographs and cone-beam computed tomographic scans were taken immediately after surgery. An average of 6 months was allowed for the implants to integrate. The implants were then uncovered and panoramic radiographs and dental cone-beam computed tomographic scans were obtained to assess new bone formation around the implants. Implants were loaded with provisionals for 3 months before the nal prostheses were delivered.

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BONE FORMATION USING ABSORBABLE GELATIN

FIGURE 4. Postoperative cone-beam computed tomographic scans revealed the sinus was lled with blood clots and voids under the elevated schneiderian membrane. A, Implant corresponding to the maxillary right second molar. B, Implant corresponding to the maxillary right rst molar. C, Panoramic computed tomogram (patient 6). Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

Results
Postoperative cone-beam computed tomographic scans revealed that the sinus was lled with blood clots and voids under the elevated schneiderian membrane (Fig 4). No adverse events were recorded during the healing period in any patient. There were no signs of infection. Two implants failed before loading due to insufcient initial stability when placed into an extraction socket. The schneiderian membrane was perforated in 1 case. The absorbable gelatin sponge was used for managing these perforations. After uncovering the implants, on average 6 months after placement, new bone consolidation was observed on radiographs and cone-beam computed tomographic scans (Fig 5). The newly formed maxillary sinus oor was observed around the implant apex in all cases including the failed implant sites. No apparent differences were observable on imaging of the augmentation with nonperforation or perforation sites. The patients maintained stable implant prostheses during their nal prostheses (Fig 6).

Discussion
One long-term study on the clinical success of implants placed into the augmented maxillary sinus with variable bone grafts, regardless of graft materials used,

has reported similar or better success than of implants placed using a conventional protocol with no grafting procedure.6 However, Lundgren et al16 reported successful new bone formation and osseointegration of implants in cases of sinus membrane elevation without bone grafts, with radiographic and in vitro histologic results. Palma et al17 compared the histologic results of sinus membrane elevation and simultaneous placement of implants with and without adjunctive autogenous bone grafts in primates. The results showed no differences between membrane-elevated and grafted sites with regard to implant stability, bone-to-implant contacts, and bone area within and outside implant threads histologically in animals. Nedir et al18 reported that elevation of the sinus membrane alone without the addition of bone grafting material can lead to bone formation beyond the original limits of the sinus oor from osteotomemediated sinus oor elevation. Sohn et al19 reported favorable new bone formation in the maxillary sinus without bone graft and clinical implant success with in vivo histologic evidence for the rst time. The absorbable gelatin sponge inserted loosely under the elevated sinus membrane acted as a space maintainer for new bone formation in the maxillary sinus as an alternative to bone ller in this study. All cases showed new bone formation in the new com-

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FIGURE 5. New bone consolidation was observed on computed tomographic scans. The former sinus oor disappeared and newly formed sinus oor and new bone formation were observed. A, Implant corresponding to the maxillary right second molar. B, Implant corresponding to the maxillary right rst molar. C, Panoramic computed tomogram (patient 6). Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

partment of the maxillary sinus; even the elevated sinus membrane showed repneumatization around the implant apex. In cases of bone grafts into the maxillary sinus, bone graft materials have the role of ller, resulting in space in the sinus. However, grafted bone volumes also adapt considerably in shape and volume due to repneumatization of the maxillary sinuses, with a resorption rate of 0.4% to 54%.20-23 In the present study, 2 implants failed during the uncovering procedure due to insufcient osseointegration. The failed implants could not be inserted

with sufcient primary stability in the extraction socket, and the residual bone height was shorter than 2 mm in 1 of the sites. Achievement of primary stability depends on adequate preparation of the bone site to receive the implant and demands strict adherence to surgical protocols.24 Implants with decient initial stability are susceptible to micromotion at the bone-to-implant interface, which may affect the bonehealing process and result in brous encapsulation.25 Previous studies have shown that implants with surface treatment exhibit greater bone-to-implant

FIGURE 6. Panoramic radiograph shows the augmented right maxillary sinus and xed bridges in situ. Sohn et al. Bone Formation Using Absorbable Gelatin. J Oral Maxillofac Surg 2010.

1332 contact mainly in the early stages of osseointegration and in areas of low-quality bone.26,27 SybronPRO XRT implants with resorbable blast media surfaces were placed in the present study. Piattelli et al28 reported that the resorbable blast media surface could be considered more osteoconductive than a machined surface. The study, with scanning electron microscopy and electron spectroscopy for clinical analysis, showed that implant surface treatment can improve in vitro cellular adhesion and proliferation.27 However, surface treatment processes can leave the processing material embedded in the implant surface as residual contaminants during beading or grit blasting.29 Such a problem could be avoided by the use of calcium phosphate media. Although the residual particles existed, they could be absorbed or attached to surrounding bone.28 The barrier membrane between graft materials and the overlying soft tissue is necessary to prevent growth of brous connective tissue in the augmented space.30,31 The lateral bony window was replaced after augmentation of the maxillary sinus and simultaneous placement of implants in this study. The replaceable bony window made by the piezoelectric saw could be precisely repositioned because of the tilted osteotomy into the sinus, highly controlled osteotomy, and minimal bone loss during osteotomy. Lundgren et al16 used an oscillating saw to create the lateral window as a barrier for sinus augmentation. The application of a conventional oscillating saw in creating a lateral bony window is irritating to patients because of the loud noise during surgery. Moreover, access to the oral cavity may be limited. Hence, use of a piezoelectric device is recommended to create a lateral bony window to obtain direct visibility over whole osteotomies, highly precise bone cut by micrometric, and linear vibrations.19,32-36 The precisely created bony window prevents the replaceable bony window from dropping into the maxillary sinus cavity.19,34 Whether or not bone grafting is performed in the maxillary sinus, the replaceable bony window acts as a homologous barrier over the new compartment under the elevated maxillary sinus.19 Lundgren et al16 reported that there are several advantages to using a replaceable bone window, according to the principle of guided tissue regeneration. Sohn et al19 demonstrated that there are no clinical differences in new bone formation in the maxillary sinus between the group using nonresorbable membrane and the group using replaceable bony window to seal the lateral window, according to histologic data in humans. However, a homologous bony window is free from viral cross-contamination of animal or human origin and saves the surgical cost of purchasing barrier membranes. Homologous bony windows not only prevent soft invasion into the grafted site but also act as

BONE FORMATION USING ABSORBABLE GELATIN

osteoinductive/osteoconductive substrates for new bone formation in the sinus, accelerating new bone formation in the grafted/nongrafted sinus. In conclusion, elevation of the sinus membrane, simultaneous placement of implants, and insertion of gelatin sponges demonstrate new bone formation through clinical and radiographic evaluations. New bone formation was veried by stabilization of the elevated sinus membrane from the tenting effect of placement of dental implants and absorbable gelatin sponge without any bone graft material. This study shows that there is great potential for new bone formation in the maxillary sinus without the use of additional bone grafts. It is suggested that long-term follow-up often is required for conrmation of the stability of this procedure. Acknowledgment
The authors thank Dr Paul Maupin for his valuable assistance in editing this article.

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16. Lundgren S, Andersson S, Gualini F, et al: Bone reformation with sinus membrane elevation: A new surgical technique for maxillary sinus oor augmentation. Clin Implant Dent Relat Res 6:165, 2004 17. Palma VC, Magro-Filho O, de Oliveria JA, et al: Bone reformation and implant integration following maxillary sinus membrane elevation: An experimental study in primates. Clin Implant Dent Relat Res 8:11, 2006 18. Nedir R, Bischof M, Vazquez L, et al: Osteotome sinus oor elevation without grafting material: A 1-year prospective pilot study with ITI implants. Clin Oral Implants Res 17:679, 2006 19. Sohn DS, Lee JS, Ahn MR, et al: New bone formation in the maxillary sinus without bone grafts. Implant Dent 17:321, 2008 20. Tepper G, Haas R, Zechner W, et al: Three-dimensional nite element analysis of implant stability in the atrophic posterior maxilla: A mathematical study of the sinus oor augmentation. Clin Oral Implants Res 13:657, 2002 21. Diserens V, Mericske E, Mericske-Stern R: Radiographic analysis of the transcrestal sinus oor elevation: Short-term observations. Clin Implant Dent Relat Res 7:70, 2005 22. Johansson B, Grepe A, Wannfors K, et al: A clinical study of changes in the volume of bone grafts in the atrophic maxilla. Dentomaxillofac Radiol 30:157, 2001 23. Kirmeier R, Payer M, Wehrschuetz M, et al: Evaluation of threedimensional changes after sinus oor augmentation with different grafting materials. Clin Oral Implants Res 19:366, 2008 24. Lioubavina-Hack N, Lang NP, Karring T: Signicance of primary stability for osseointegration of dental implants. Clin Oral Implants Res 17:244, 2006 25. Meredith N: Assessment of implant stability as a prognostic determinant. Int J Prosthodont 11:491, 1998 26. Martinez H, Davarpanah M, Missika P, et al: Optimal implant stabilization in low density bone. Clin Oral Implants Res 12: 423, 2001

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