* E i I • _ I 1 Second Edition H n e G S 1 raft Second edition Edited by Ole T. Jensen, DDS, MS Private Practice Oral and Maxillofacial Surgery Denver, Colorado Quintessence Publishing Cor Inc quintes/cnce Chicago, Berlin, Tokyo, London, Paris, Milan, Barcelona, Istanbul, book/ Sao Paulo, New Delhi, Moscow, Prague, and Warsaw The sinus bone graft / edited by Ole T. Jensen. — 2nd ed. p. ; cm. Includes bibliographical references and index. ISBN 0-86715-455-1 (hardcover) 1. Maxillary sinus. 2. Maxillary sinus—Surgery. 3. Bone-grafting. I. Jensen, Ole T. [DNLM: 1. Maxillary Sinus--surgery. 2. Bone Transplantation --methods. 3. Reconstructive Surgical Procedures. WV 345 S618 2006] RF421.S55 2006 617.5'2-dc22 2005032653 (|ulnle//cfiu book/ © 2006 Quintessence Publishing Co, Inc All rights reserved. This book or any part thereof may not be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, or otherwise, without prior written permission of the publisher. Quintessence Publishing Co, Inc 4350 Chandler Drive Hanover Park, Illinois 60133 www.quintpub.com Editor: Lisa C. Bywaters Production: Sue Robinson Cover and internal design: Dawn Hartman Printed in China Use of Barrier Membranes in Sinus Augmentation Stephen S. Wallace, DDS Stuart J. Frourn, DDS Dennis P. Tarnow, DDS When a lateral window approach is used, the sinus bone graft benefits from the placement of a barrier membrane over the osteotomy site. Using a resorbable membrane to repair inadvertent perforation of the sinus membrane within the sinus also has therapeutic rationale. This chapter discusses the somewhat controversial use of barrier membranes in the course of sinus grafting. History of Barrier Therapy The concept of placing a barrier membrane over the lateral sinus window is a logical extension of barrier applications in orthopedics, periodontal guided tissue regeneration, and preprosthetic guided bone regeneration. In 1959, Murray1 described bone growth under a plastic "cage" in the spine in which bone filled a cavity where soft tissue was excluded. This finding foreshadowed what we now call guided bone regeneration. Murray and subsequent dental practitioners who are experienced in guided bone regeneration provided the theoretical and practical basis for membrane-protected maxillary sinus surgery. Guided tissue regeneration is based on Melcher's2 concept of selective cell repopulation and on later studies by et a!3 and Cottlow et al.4 The regeneration of the attachment apparatus by selective cell repopulation evolved from these seminal studies. When applied to human periodontal defects, this technique includes the placement of a physical barrier (membrane) between the gingival flap and the root surface just coronal to the periodontal defect. The barrier retards repopulation of the root by gingival epithelium and gingival connective tissue and favors healing by cells from within the periodontal ligament. Human histology of cases treated with barrier membranes demonstrates regeneration of cementum, bone, and a functionally oriented periodontal ligament.3"5 A requirement for the success of guided tissue regeneration includes the creation of a space apical to the membrane that isolates the treated root surface and the defect so that desired cells migrate and populate the wound. Nonabsorbable and bioabsorbable barrier membranes are effective for periodontal regeneration.6"8 The ability to keep the membrane submerged and covered by the gingival flap influences clinical outcome.9'10 Evidence-based reviews show that guided tissue regeneration with membranes is more effective than controls in the treatment of intrabony and furcation defects.1112 The principles of guided tissue regeneration were later modified to regenerate bone for the repair of alveolar ridge defects.1315 This technique, known as guided bone regeneration, has been successfully used for site develop- 229 • • chapta Use ot Barrier Membranes in Sinus Augmentation Fig 19-1 Sinus grafted with a xenograft (Bio-Oss, Osteohealth). Proposed barrier membrane placement is outlined in yellow. Fig 19-2 Placement and stabilization of a nonabsorbable expanded polytetrafluoroethylene (e-PTFE) barrier membrane (Gore-Tex, W. L, Gore) so as to avoid incision lines. Fig 19-3 Placement of a bioabsorbable barrier membrane (Ossix, ColBar R&D) so as to avoid incision lines. Fig 19-4 Placement of a bioabsorbable barrier membrane (Bio Gide, Geistlich Biomaterials) so as to avoid incision lines. ment prior to,1617 at the time of,1819 and after implant placement. The success of guided bone regeneration depends on the maintenance of space, the stability of the membrane, the duration of barrier function, and the prevention of membrane exposure. Implants placed into regenerated bone demonstrate excellent success rates.20"26 A recent evidence-based review by Fiorellini and Nevins27 shows an implant survival rate of 97.3% for implants Membrane Placement over Lateral Window When used in sinus grafting, the surgical objective is tc position an effective barrier membrane over the latera window in such a manner as to exclude the connective tis sue from the wound. Various materials have been used a barriers over the lateral window antrostomy, includinj Membranes for Perforation Repair nonresorbable e-PTFE membranes, long- and short-term bioabsorbable cross-linked collagen membranes, synthetic membranes, titanium mesh membranes, freeze-dried lamellar bone sheets, calcium sulfate barriers, and the repositioned original lateral bony window. The membrane should cover the window by a minimum of 3 to 5 mm (Fig 19-1). Placing the membrane under the incision line should be avoided, as this may lead to the complication of exposure. Many membranes are packaged with templates that can be cut to the appropriate size after the window is made and the sinus membrane elevated. Using this template, the barrier membrane is then cut to size and hydrated prior to grafting the sinus. Once grafting is complete, the shaped membrane can be applied immediately. Experience with guided bone regeneration has shown that e-PTFE membranes must be stabilized with tacks or screws {Fig 19-2) to prevent shifting, which results in loss of barrier function as well as difficulty in removal. Depending on their stiffness, bioabsorbable barrier membranes may have the ability to remain in place without mechanical stabilization. The more adaptable (thin) membranes conform well to the surface of the lateral sinus wall (Figs 19-3 and 19-4). Most of the bioabsorbable membranes can be stabilized with tacks; however, unless the tacks are bioabsorbable, re-entry for tack removal will be required. At New York University, clinical experience has shown that these long-term, bioabsorbable membranes are still in position over the window at the time of bone core harvesting. Studies of the effectiveness of bioabsorbable barriers have found them to be similar to e-PTFE membranes with regard to vital bone formation (see below). An advantage of the bioabsorbable membrane is elimination of the reentry procedure required for e-PTFE. Membranes for Perforation Repair Perforation of the sinus membrane is a common complication of the sinus elevation procedure; reports of the incidence of membrane perforation range from 1O%28 to 44%.J9 Techniques for repairing membrane perforations delude suturing, and "patching" of the perforation with biomaterials such as Celfilm (Pfizer), CollaTape (Integra), fibrin glue, Lambone (Pacific Coast Tissue Bank), and, most commonly, bioabsorbable collagen barrier membranes. Repair techniques using collagen barriers have been reported in the literature by Vlassis and Fugazzotto,30 Pikos,31 and Proussaefs and Lozada.32 The purpose of the repair is strictly for the containment of particulate graft material. Small perforations will generally close by folding the elevated membrane back upon itself, and no further action is necessary. However, larger perforations will not close, and thus some form of corrective action must be taken. Suturing a torn membrane, while difficult, is sometimes possible, especially if the membrane is thickened. The cost of failure, however, is high. Most often, suturing merely increases the size of the perforation. A bioabsorbable collagen membrane is an effective way to seal a perforation. The barrier acts to confine the graft material until a biologic repair can take place. It is critical that the repair effort not compromise vasculariration of the sinus graft. Since the blood supply to the graft comes from the bony walls (lateral wall, crest, and medial wall), the membrane must not be placed over the endosteal blood supply. When the sinus membrane is elevated, it forms the superior and distal walls of a regenerative space or compartment that is subsequently filled with graft material. The anterior, medial, lateral, and inferior walls of this space are the bony surfaces that contain the vascular supply. Once the membrane is elevated, the perforation usually occurs superiorly or distally (Fig 19-5a). The collagen membrane should be placed so that it rests predominantly on the elevated sinus membrane (Fig 19-5b). If the perforation is close to the area of the superior hinge, the membrane is likely to shift medially as the graft material is being added, thus leaving the perforation unrepaired. This problem can be avoided by tacking the membrane outside the sinus, superior or distal to the window as the case presents, and then folding the membrane into the sinus (Fig 19-6). The membrane can be cut so that part of it remains outside the window and the other part fits in the sinus and unfolds (Fig 19-7). In extreme cases, small holes can be drilled into the lateral wall for the placement of sutures that, along with tacks, will help stabilize the reparative membrane (Fig 19-8). A membrane technique by Pikos31 for the repair of larger perforations involves modifying the membrane with diagonal slits (Fig 19-9) so that it will form a tent over the graft, thus containing the particulate graft crestally. Also chapui Use of Barrier Membranes in Sinus Augmentation Fig 19-5a Sinus membrane perforation superiorly after elevation. Fig 19-5b Collagen membrane positioned against elevated sinus membrane. Perforation will be stabilized against the sinus membrane by graft material. Fig 19-6 Stabilized membrane f< repair of a distal perforation. Fig 19-7a Perforation at superior osteotomy {model). Fig 19-7b Membrane fixated external to sinus with titanium tacks and modified by lateral cuts extending to the superior corners of the window (model). Fig 19-7c Membrane folded into positic to establish a superior repair (model). designed for large perforations is the so-called Loma Linda Pouch technique,32 which uses a bioabsorbable membrane to completely encapsulate the graft inside the sinus. The corners of the membrane extend circumferentially to the outside of the sinus, but the graft is isolated from the endosteum. Covering the elevated sinus membrane with a collagen barrier does not compromise the graft. A histologic animal study by Haas et al33 has shown the sinus membrane to be an avascular tissue, and a primate study by Hurzeler et ai34 has shown it to have minimal negative effects on bone formation. The size of the membrane used for repair should I large enough to accommodate the size of the perforatic and to stabilize the membrane in place. It should be size so that it will neither be displaced through the perforatic when the graft material is being placed or forced throuj the perforation by changes in sinus air pressure resultir from breathing, sneezing, etc. This requires either placir the edges of the barrier membrane against areas whe the sinus membrane is still intact or using additional mea of stabilization. Evidence of the efficacy of perforation repair is providt by studies showing similar outcomes for implant survival 232 Evidence for Using a Membrane over the Lateral Window Fig 19-8a Stabilization of membrane with horizontal supporting sutures. Fig 19-8b Reparative membrane positioned below suture supports and tacked externally. Fig 19-9 Modified membrane (Pikos technique) for use as a barrier to contain the particulate graft material, perforated and nonperforated cases. Only 3 of 12 studies that reported perforation rates found an increased rate of implant failure associated with perforated membranes.35-37 If a repair is successful, membrane perforation does not appear to be strongly associated with postoperative complication or reduced implant survival. Unsuccessful repairs may ultimately lead to inadequate graft density, sinusitis, and postoperative sinus infection due to loss of graft containment. Postsurgical complications result in reduced implant survival, and if the surgery is aborted an additional sinus surgery will be required. If the repair does not work, the procedure should be aborted. In such cases, the clinician should consider placing a barrier membrane over the lateral window to prevent adhesion of the repairing sinus membrane to the periosteum, which would make re-entry more difficult. Evidence for Using a Membrane over the Lateral Window The efficacy of membrane placement over the lateral window is best evaluated indirectly by comparing histologic data and survival rates of implants placed in the grafted maxillary sinuses with and without the use of a membrane. Histologic data Bone grafts placed in the maxillary sinus are vascularized by the blood vessels and surrounding perivascular progenitors in the bony walls and within the floor of the sinus. Vascularization is not significantly affected by the periosteum that resides outside the sinus bone graft site. An 233 chapter T Use of Barrier Membranes in Sinus Augmentation Fig 19-10a Osteoblasts and bone formation directly on {and within) the e-PTFE membrane surface {hematoxylin and eosin; original magnification X40). Fig 19-10b Vital bone formation in contact with e- PTFE membrane surface in area of lateral window (Stevenel blue, picric acid fuchsin; original magnification X40). Fig 19-lOc Polarized light reveals bone formation directly beneath the e-PTFE membrane. Note osteoblasts on bone surface and enclosed osteocytes (Stevenel blue, picric acid fuchsin; original magnification X50). (Reprinted with permission from Tarnow et al47). Fig 19-10d Vital bone in contact with membrane and throughout core (hematoxylin and eosin; original magnification X31.5). (Reprinted with permission from Tarnow et al1T). early fluorescence microscopy study by Boyne and Kruger38 (1962) demonstrated that the floor of the maxillary sinus responded to stimulation with reactive bone formation. Misch and Dietsch39 and Quifiones et al40 obtained the same response from sinus bony walls in primates after sinus membrane elevation. This pattern of bone formation was also demonstrated radiographically in a primate study I Margolin etal41 and in humans by Boyne etal42 and Nevi and Fiorellini.43 Bone formation from the sinus floor o curred at a rate of about 1 mm per month in four hum; core samples measured by Smiler et al.44 234 Evidence for Using a Membrane over the Lateral Window •... AB1 K 19-1 Av. Membrane type e-PTFE (Gore-Tex) Collagen (Bio-Gide) No membrane ed in sin No. of sinuses 21 37 6 ith aii Average vital bone formed (%) 16.9 17,6 12.1 d without a me Marrow (%) 51.2 56.0 63.6 Residual Bio-Oss (%) 31.9 26.4 24.3 Just as they function in guided bone regeneration, membranes prevent nonosteogenic connective tissue from developing in the grafted area and hence in the sinus, which could lead to loss of graft ossification. Soft tissue ingrowth, or encleftation, has been demonstrated in both primates and humans,45-46 and it is similar to the problems observed in periodontal ridge defects when a membrane barrier is not used or when the barrier is prematurely lost during a regenerative procedure. From a biologic point of view, the exclusion of connective tissue cells should favor the population of the sinus graft with perivascular osteoblasts emanating from the adjacent bony walls and the now-exposed vascular supply. Histologic sections taken through the lateral window that contain the barrier membrane reveal bone formation in contact with the membrane in such a manner as to restore the bony wall (Fig 19-10). Histomorphometric evidence of enhanced bone formation following membrane placement over the lateral window is available from one random controlled trial and two controlled trials conducted at the New York University Department of Implant Dentistry. A random controlled trial by Tarnow et al47 in which bilateral sinus grafts were accomplished with and without a membrane in each patient showed vital bone formation to be 25.5% with and 11.9% without a membrane. Six cases showed dramatic benefits, five cases were similar but favored the membrane side, and one case slightly favored the nonmembrane side. A controlled trial by Froum et al48 measured vital bone formation in 113 sinuses grafted with either a xenograft or a combined autograft-xenograft. Average vital bone formation was 27.6% when a membrane was used and 16% when a membrane was not used. One of the drawbacks of membrane use is the necessity to remove it after graft maturation. Nonabsorbable membranes are generally stabilized with tacks or screws, which also must be removed. Removal of membranes and tacks generally requires a surgical entry that is much more invasive than that required either for implant placement alone (delayed placement) or for stage-two surgery (simultaneous placement). If both types of membranes are equally effective, the bioabsorbable membranes would offer the clear advantage of avoiding the need for an additional surgical intervention. A recent study by Wallace et al49 compared vital bone formation in sinuses grafted with 100% Bio-Oss (Osteohealth) with different membranes placed over the lateral window. The nonabsorbable Gore-Tex membrane (W. L. Gore) and the bioabsorbable Bio-Gide membrane (Osteohealth) were compared to controls with no membrane coverage. No statistical differences were found between the absorbable (17.6%) and nonabsorbable (16.9%) membranes, and both were better than the no-membrane controls (12.1%) in vital bone development as well as implant survival rates (Table 19-1, Figs 19-11 to 19-13). Clinical efficacy Because of the relatively small number of randomized controlled human clinical trials in sinus graft surgery that have been conducted to date,50 those that have been done do not allow for evidence-based decision making. To evaluate the efficacy of membrane placement, it would be best to have more studies that use a split-mouth design to compare the survival of implants placed in grafted sinuses with and without a membrane over the lateral window. Other relevant data may be extracted from well-conducted studies that offer lower levels of evidence (controlled trials, consecutive case series, and retrospective analyses). Sufficient clinical evidence exists to justify the use of a barrier membrane over the lateral window in sinus graft surgery. A systematic review confirmed the importance of membrane placement in sinus augmentation surgery,51 citing the controlled clinical trials by Tarnow et al47 and 235 (hapter 7 y Use of Barrier Membranes in Sinus Augmentation Fig 19-11 Histologic core of graft placed with a Gore-Tex e-PTFE membrane (Stevenel blue, picric acid fuchsin; original magnification X4). (yellow, Bio-Oss; green, osteoid; red, new bone). Fig 19-12 Histologic core of graft placed with a Bio-Gide membrane {Stevenel blue, picric acid fuchsin; original magnification X4), (yellow, Bio-Oss; green, osteoid; red, new bone). Fig 19-13 Histologic core of graft placed without a membrane (Stevenel blue, picric acid fuchsin; original magnification X4). (yellow, Bio-Oss; green, osteoid; red, new bone). Froum et al48 in which more favorable bone formation and higher implant survival rates were obtained when a membrane was used. A controlled trial by Tawil and Mawla52 also achieved a higher implant survival rate with membrane use. Results from these three controlled trials are provided in Table 19-2. The aforementioned review51 also identified 20 additional studies (15 without membrane, 5 with membrane) in which higher implant survival rates were obtained when a barrier membrane was placed over the lateral window in sinuses grafted with participate grafts (93.6% with membrane versus 88.7% without membrane). A recent study by Wallace et al49 has shown similar implant survival rates when e-PTFE (Gore-Tex) (97.8%) and Bio-Gide membranes (97.6%) were used in sinus grafts composed of 100% Bio- Oss xenograft (Table 19-3), Likewise, a 5-year prospective study on guided bone regeneration by Zitzmann et al" showed no statistical differences in implant survival rates following guided bone regeneration procedures with either Bio-Oss/Gore-Tex or Bio-Oss/Bio-Gide. The increased vital bone formation achieved when a membrane is placed over the window can be observed clinically (Fig 19-14) and most likely accounts for the improved implant outcomes reported in the literature. When a membrane is not placed over the window, it is not uncommon to find a lack of corticalization of the graft surface. The incidence of this finding may increase with the size of the window. This phenomenon may be explained by the fibrogenic nature of the adult periosteum once it has been elevated from the bone surface, combined with the increased distance of the mid-window from the blood supply from the cut lateral wall. Tawil and Mawla have reported that in their study, implant survival was related to the quality of the reconstructed cortical plate." Additionally noted in nonmembrane cases is the finding of encleftation through the sinus window.45 Conclusions Systematic literature reviews have documented successful outcomes for both guided tissue regeneration around teeth11-12 and preprosthetic guided bone regeneration prior to implant placement.27 An evidence-based literature review by Wallace and Froum91 on implant survival follow- 236 Conclusions I.Mil t. 19-2 Rate's of and without a n Suich Survival rate with membrane Survival rate without membrane Tarnow et at (2000)*7 Tawil and Mawla (2OO1)52 Froum et al (1998)^ 100%; n = 28 implants 93.1%; n = 29 implants 99.2%; n = 133 implants 92.6%; n = 27 implants 78.1%; n = 32 implants 96.3%; n = 82 implants 1 IABLL19-3 Rates of i Membrane e-PTFE (Gore-Tex) Collagen (Bio-Gide) Total survival in sinuses - No. of implants placed 46 83 129 Failures 1 2 3 jle and nonabsorbablo membranes Survival (%) 97.8 97.6 97.7 Fig 19-14a Six months after placement, the bioabsorbable Ossix membrane remains intact. Fig 19-14b Beneath the membrane, corticalization of the graft surface can be seen. mg sinus augmentation and histologic/histomorphometric data documents the benefits of using a membrane over the lateral window. Following are the positive effects that have been obtained by placing a membrane over the lateral window: 1. Excludes nonosteogenic connective tissue 2. Contains particulate graft material 3. Prevents soft tissue encleftation 4. Increases vital bone formation (guided bone regeneration effect) 5. Increases implant survival rate 6. Results in positive outcomes when used for perforation repairs. The available evidence suggests that the use of a membrane over the lateral window should be considered in all sinus graft procedures that use a lateral approach. diopter Use of Barrier Membranes in Sinus Augmentation References 1. Murray C, Holden R, Roachlau W. Experimental and clinical study of new growth of bone in a cavity. Am J Orthop Surg 1959;93:385-387. 2. Melcher AH. On the repair potential of periodontal tissues. J Periodontol 1976;47:256-260. 3. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal disease. J Clin Periodontol 1982;9:290-296. 4. Gottlow J, Nyman S, Lindhe J, Karring T, Wennstrom J. New attachment formation in the human periodontium by guided tissue regeneration. J Clin Periodontol 1986; 13:604-616. 5. Stahl SS, Froum SJ, Tarnow DP. Human histologic responses to guided tissue regenerative techniques in intrabony lesions. J Clin Periodontol 1990:17.191-198. 6. Gian-Grasso J. Tooth isolation for new attachment procedures— A surgical and suturing method: Three case reports. J Periodontol 1987.58:819. 7. Shanaman R. A retrospective study of 237 sites treated consecutively with guided tissue regeneration, lot i Periodontics Restorative Dent 1994;14:293-301. 8. Laurell L, Falk H, Fornell J, Johard G, Gottlow J. Clinical use of a bioresorbable matrix barrier in guided tissue regeneration therapy. Case series. J Periodontol 1994:65:967-975. 9. Tonetti MS, Pini-Prato G, Cortellini P. Periodontal regeneration in human periodontal intrabony defects. IV. Determinants of response. J Periodontol 1993;64:934-940. 10. Murphy KG. Incidence, characterization and effect of surgical complications using Gore-Tex periodontal membranes. Effect of complications on regeneration. Int J Periodontics Restorative Dent 1995:15:549-561. 11. Reynolds MA, Aichelmann-Reidy ME, Branch-Mays GL, Gunsolley JC. The efficacy of bone replacement grafts in the treatment of periodontal osseous defects. A systematic review. Ann Periodontol 2003;8:227-265. 12. Murphy KG, Gunsolley JC. Guided tissue regeneration for the treatment of periodontal intrabony and furcation defects. A systematic review. Ann Periodontol 2003;8:266-302. 13. Dahlin C, Linde A, Gottlow J, Nyman S. Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg 1988;81: 672-676. 14. Dahlin C. Gottlow J, Linde A, Nyman 5. Healing of maxillary and mandibular bone defects using a membrane technique [abstract 385]. J Dent Res 1989:68:918. 15. Siebert J, Nyman S. Localized ridge augmentation in dogs: A pilot study using membranes and hydroxyapatite. J Periodontol 1990:61:157-165. 16. Becker W, Becker B, Handlesman M, et al. Bone formation at dehisced dental implant sites treated with implant augmentation material: A pilot study in dogs. Int J Periodontics Restorative Dent 1990:10:93-101. 17. Buser D. Bragger U, Lang NP, Nyman S. Regeneration and enlargement of jawbone using guided tissue regeneration. Clin Oral Implants Res 1990:1:22-32. 18. Nyman S, Lang NP, Buser D, Bragger U. Bone regeneration adjacent to titanium dental implants using guided tissue regeneration: A report of cases. Int J Oral Maxillofac Implants 199<y 5:9-14. 19. Lazzara RJ. Immediate implant placement into extraction sites- Surgical and restorative advantages. Int J Periodontics Restorative Dent 1989:9:333-343. 20. Buser D, Dula K, Lang NP, Nyman S. Long-term stability of osseointegrated implants in bone regenerated with the membrane technique. Five-year results of a prospective study with 12 implants. Clin Oral Implants Res 1996:7:175-183. 21. Fugazzotto PA, Shanaman R, Manos T. Shectman R. Guided bone regeneration around titanium implants: Report of the treatment of 1,503 sites with clinical re-entries. Int J Periodontics Restorative Dent 1997;17:293-299. 22. Nevins M, Mellonig JT, Clem DS, Reiser GM, Buser DA. Implants in regenerated bone: Long-term survival. Int J Periodontics Restorative Dent 1998:18:35-15. 23. Becker W, Dahlin C, Lekholm U, et al. Five-year evaluation of implants placed at extraction and with dehiscences and fenestration defects augmented with e-PTFE membranes: Results from a prospective multicenter study. Clin Implant Dent Relat Res 1999;1:27-32. 24. Simion M, Jovanovic SA, Tinti C, Parma Benfenati S. Long-term evaluation of osseointegrated implants inserted at the time of or after vertical ridge augmentation. A retrospective study of 123 implants with 1-5 year follow-up. Clin Oral Implants Res 2001; 12:35-45. 25. Corrente G, Abundo R, Cardaropoli D, Cardaropoli G, Martuscelli G. Long-term evaluation of osseointegrated implants in regenerated and nonregenerated bone. Int J Periodontics Restorative Dent 2000:20:391-397. 26. Zitzmann NU, Scharer P, Marinello CP. Long-term results of implants treated with guided bone regeneration: A 5-year prospective study. Int J Oral Maxillofac Implants 2001:16:355-366. 27. Fiorellini JP, Nevins ML. Localized ridge augmentation/preservation. A systematic review. Ann Periodontol 2003:8:321-327. 28. Misch CE. The maxillary sinus iift and sinus graft surgery. In: Misch CE. Contemporary Implant Dentistry. St Louis: Mosby, 1999;469-495. 29. Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical complications of the sinus graft procedure and their impad on implant survival. J Periodontol 2004:75:511-516. 30. Vlassis JM, Fugazzotto PA. A classification system for sinus membrane perforations during augmentation procedures with option; for repair. J Periodontoi 1999:70:692-699. 31. Pikos MA. Maxillary sinus membrane repair: Report of a tech nique for large perforations. Implant Dent 1999;8:36-46. 32. Proussaefs P, Lozada J. The "Loma Linda Pouch": A techniqu< for repairing the perforated sinus membrane. Int J Periodontic Restorative Dent 2003:23:593-597 33. Haas R, Baron M, Donath K, Zechner W, Watzek G. Porou hydroxyapatite for grafting the maxillary sinus: A histomorpho metric study in sheep. Int J Oral Maxillofac Implants 2OO2;17 337-346. 238 References 34. Hiirzeler MB, Quinones CR, Kirsch A, et al. Maxillary sinus augmentation using different grafting materials and dental implants in monkeys. Part I, Evaluation of anorganic bovine-derived matrix. Clin Oral Implants Res 1997;8:476-^86. 35 Jensen OT, Shulman LB, Block MS. lacono VJ. Report of the Sinus Consensus Conference of 1996. Int J Oral Maxillofac Implants 1998;13(suppl):11^15. 36. Khoury F. Augmentation of the sinus floor with mandibular bone block and simultaneous implantation: A 6-year clinical investigation. Int J Oral Maxillofac Implants 1998:14:557-564. 37. Proussaefs P, Lozada J, Kim J, Rohrer MD. Repair of the perforated sinus membrane with a resorbable collagen membrane A human study. Int J Oral Maxillofac Implants 2004; 19:413-420. 38- Boyne PJ, Kruger GO. Fluorescence microscopy of alveolar bone repair. Oral Surg 1962,15:265-281. 39. Misch CE, Dietsch F. Subantral augmentation in Maccaca fastcularis: A pilot study. Int J Oral Implantol 1991;17:340. 40. Quinones CR, Hurzeler MB, Schupbach P, et al. Maxillary sinus augmentation using different grafting materials and osseointegrated dental implants in monkeys. Part II. Evaluation of porous hydroxyapatite as a grafting material. Clin Oral Implants Res 1997;8:487^t96. 41. Margolin MD, Cogan AG, Taylor M, et al. Maxillary sinus augmentation in the non-human primate: A comparative radiographic and histoiogic study between recombinant human osteogenic protein-1 and natural bone mineral. J Periodontol 1998;89: 911-919. 42. Boyne PJ, Lilly IX, Marx RE, et al. De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation. J Oral Maxillofac Surg 2005;63:1693-1707. 43. Nevins M, Fiorellini JP. The maxillary sinus floor augmentation procedure to support implant prostheses. In: Nevins M, Mellonig JT (eds). Implant Therapy: Clinical Approaches and Evidence of Success. Chicago: Quintessence, 1998:171-195. 44. Smiler DC, Johnson PW, Lozada JL, et al. Sinus lift grafts and endosseous implants: Treatment of the posterior atrophic maxilla. Dent Clin North Am 1992:36:151-186. 45. McAllister BS, Margolin MD, Cogan AD, Taylor M, Wollins J. Residual lateral wall defects following sinus grafting with recombinant human osteogenic protein-1 or Bio-Oss in the chimpanzee. Int J Periodontics Restorative Dent 1998:18:227-239. 46. Jensen OT, Greer RO. Immediate placement of osseointegrated implants into the maxillary sinus augmented with mineralized cancellous allograft and Gore-Tex: Second stage surgical and histological findings. In: Laney WR, Tolman DE (eds). Tissue Integration in Oral, Orthopedic, and Maxillofacial Reconstruction. Chicago: Quintessence, 1992:321-333. 47. Tarnow DP, Wallace SS, Froum SJ. Histoiogic and clinical comparison of bilateral sinus floor elevations with and without barrier membrane placement in 12 patients: Part 3 of an ongoing prospective study. Int J Periodontics Restorative Dent 2000; 20:116-125. 48. Froum SJ, Tamow DP, Wallace SS, Rohrer MD, Cho S-C. Sinus floor elevation using anorganic bovine bone matrix (Osteo- Graf/N) with and without autogenous bone: A clinical, histoiogic, radiographic and histomorphometric analysis—Part 2 of an ongoing prospective study. Int J Periodontics Restorative Dent 1998;18:529-543. 49. Wallace SS, Froum SJ, Cho S-C, et a!. Sinus augmentation utilizing anorganic bovine bone (Bio-Oss) with absorbable and nonabsorbable membranes placed over the lateral window: A histomorphometric and clinical analysis. Int J Periodontics Restorative Dent2005;25:551-559. 50. Graziani F, Donos N, Needleman I, Gabriele M, Tonetti M. Comparison of implant survival following sinus floor augmentation procedures with implants placed in pristine posterior maxillary bone: A systematic review. Clin Oral Implants Res 2004;15: 677-682. 51. Wallace SS, Froum SJ. Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol 2003:8:328-343. 52. Tawil G, Mawla M. Sinus floor elevation using a bovine bone mineral (Bio-Oss) with or without the concomitant use of a bilayered collagen barrier (Bio-Gide): A clinical report of immediate and delayed implant placement. Int J Oral Maxillofac Implants 2001 ;16:713-721. 53. Zitzmann N, Scharer P, Marinello CP. Long-term results of implants treated with guided bone regeneration: A 5-year prospective study. IntJ Oral Maxiliofac Implants 2001 ;16:355-366. 239