Maxillary Sinus Augmentation: Evidence-Based Decision Making

With a Biological Surgical Approach Stephen S Wallace, DDS; Abstract: Sinus elevation surgery has been used by the dental profession to increase bone quantity in the posterior maxilla for the placement of root-form implants. The original treatment protocol was developed using existing bone-healing theories that relied on expert opinion. In 2003 and 2004, 2 evidence-based literature reviews were published, expanding significantly on the previous review of 1996. The new reviews were based on the best studies available and were designed to present information that would help clinicians achieve more favorable outcomes. This article discusses this information and answers further questions relating to the sinus elevation procedure. Learning Objectives: After reading this article, the reader should be able to: discuss the best evidence available on the sinus grafting technique. explain 3 decisions that will improve the outcome of the sinus grafting procedure. describe the biological aspects of the surgical technique. discuss sinus elevation as a standard in-office procedure with the use of nonautogenous grafts.

Implant dentistry has dramatically changed the way we approach fully and partially edentulous patients. A reconstructive approach introduced to specifically address patients edentulous in the mandible has evolved to a therapeutic modality that encompasses therapy in the edentulous maxilla, the partially edentulous patient, and the patient missing 1 tooth. Bone loss after tooth extraction or periodontal disease can complicate the placement of root-form implants because of a lack of sufficient height or width of

residual bone. This can be overcome with ridge augmentation procedures that can restore the lost bone volume. The posterior maxilla may present an additional obstruction to implant placement caused by pneumatization (size increase) of the maxillary sinus. Some patients have limited crestal bone height in the posterior maxilla even when teeth are present, and it is not uncommon for the sinuses to pneumatize further after the extraction of the posterior teeth. Pneumatization alone, without additional loss of crestal bone caused by periodontal disease, may be sufficient to complicate the placement of even short implants in the posterior maxilla without previous sinus elevation surgery. Maxillary sinus floor elevation was introduced to the profession by Boyne in 1980.1 In the 26 years since the introduction of that technique, a host of surgical procedures have been developed to correct bone deficiency created by sinus pneumatization. They include variations of Boynes lateral window antrostomy, the osteotome sinus floor elevation,2 crestal core elevation,3 and the localized management of the sinus floor.4 Figures 1 and 2 give an example of the change in bone height that can be achieved with the lateral window sinus elevation technique.

Recently published evidence-based literature reviews by Wallace and Froum,5 Del Fabbro and colleagues,6 and an as-yet unpublished review by Moy and Aghaloo7 have reported remarkable levels of success (survival) for implants placed in these grafted sites. Evidence-based reviews are structured, unbiased compilations of the best scientific and clinical studies available. The data from similar studies are then combined to form a large database to achieve greater statistical power. The combined data are then subjected to meta-

analysis so that the variables affecting the outcome of this procedure can be isolated and their effects quantified. Average implant survival rates reported were 91.8%, 91.5%, and 92%, respectively. Although these survival rates appear to be less than acceptable, the large databases provided by these reviews (5267, 6913, and 5128, respectively) allow the reviewers to isolate selected variables and determine their importance to successful clinical practice. This decision-making process can lead to an increase in implant survival from the average sinus lift survival rates reported in the previous paragraph to a more clinically acceptable implant survival rate of 98.6%. This is an implant survival rate comparable to what one can expect with implant placement in the noncompromised anterior mandible. The 3 goals of the sinus elevation procedure are the 1) creation of vital bone in the posterior maxilla, 2) the osseointegration of the implants placed in that bone, and 3) the survival of those implants under occlusal load. How successful we are in this endeavor will be affected by the decisions we make about the variables including graft material selection, membrane placement, and implant surface selection that have been isolated in these reviews. Evidence-Based Decision Making: Graft Materials Autogenous bone was the first graft material to be widely used for sinus grafting. Many early studies involved the harvesting of a block graft from the iliac crest and then stabilizing this graft with implants placed through the remaining crestal bone and into the graft. Autogenous bone grafts from the hip, knee, and various intraoral sites also have been used in particulate form. Although autogenous bone grafts provide a source of cells, growth factors, and bone morphogenic proteins, the use of grafts of 100% autogenous bone has a number of disadvantages. Harvesting of this bone may involve hospitalization (extraoral) or require a second surgical site (intraoral), which increases the length of time of the surgery, the surgical risk, and the morbidity of the procedure. Also, clinicians have reported a more-than-average graft resorption rate when using 100% iliac bone.8

For these reasons, it has become practical to use bone replacement grafts alone or in combination with autogenous bone as a sinus grafting material. The bone replacement graft with the highest reported clinical use is the xenograft, followed by various forms of allografts and alloplasts.5,6 Demineralized freeze-dried bone allografts also have been used as a sinus graft material. Although they have been used successfully by some clinicians, the results published after the Academy of Osseointegration Sinus Consensus Conference showed both poor bone quality and a poor implant survival rate (85%). Also, this demineralized graft is susceptible to slumping, or settling, with a concomitant loss of graft height. It has a volumetric resorption rate second only to that of autogenous bone.7 Mineralized bone allografts have macrostructures similar to autogenous bone. The maintenance of this macrostructure is said by the manufacturer to depend on the processing and sterilization techniques used to process this material. Issues of safety for this material, as for demineralized freeze-dried bone allografts and xenografts, involve factors concerning procurement of the material and methods of processing and sterilization. Xenografts have been very well documented as a sinus grafting material. They have been used alone or as part of a composite graft combined with autogenous bone, venous blood, or platelet-rich plasma. In the Wallace review, the survival rate for implants placed in xenografts was similar to that of implants placed in particulate autogenous bone grafts.5 The Del Fabbro review was even more specific in the documentation of the use of xenografts.6 Survival rates for implants placed in 100% xenograft, composite grafts, and 100% autogenous bone grafts were 96%, 94.9%, and 87.7%, respectively (Table 1).

Studies by Hallman, Hising, and Valentini all have shown a higher implant survival rate when using 100% Bio-Ossa as a bone replacement graft than when either 100% autogenous bone or composite grafts of Bio-Oss and autogenous bone are used.9-11 The Moy review shows similar findings for the use of xenografts and allografts.7 A large prospective study by Peleg and colleagues on simultaneous placement of implants (2132) in sinus grafts that are mostly composites of intraorally harvested bone with xenograft or allograft reported cumulative implant survival at 8 to 9 years was 97.9%.12 The efficacy of mineralized bone replacement grafts such as xenografts is likely because of a combination of factors: 1. osteoconductivity 2. slow resorbability 3. residual graft material does not interfere with osseointegration The most important factor that can be attributed to xenografts is their osteoconductivity.11,13,14 Osteoconductivity may be defined as the direct apposition of vital bone on the xenograft surface (Figure 3). Newly formed vital bone (red) is ultimately responsible for the osseointegration of the implant in the grafted site.

A second feature of the xenograft material is that it is slowly resorbable when placed in the maxillary sinus. This quality prevents slumping (loss of graft height) and adds approximately 25% to the overall mineral content of the matured graft. An average taken from 8 published histological studies showed 25% vital bone formation, 25% residual xenograft, and 50% marrow in the matured sinus graft. The resulting 50% total mineralized tissue (new bone plus

residual graft) makes the future implant receptor site equivalent in density to that of type 2 (dense) bone. The third feature is the repeated histological finding that implants placed in sinuses grafted with xenografts are never seen in direct contact with the graft material.13,15 This is evidence that the residual graft material, while providing support and density, does not interfere with osseointegration. Issues of safety are of paramount concern to us as dentists when placing graft material in the human body. A great amount of undue concern has been placed on xenogenic material because of the outbreak reported in the public press of bovine spongiform encephalopathy in Europe. Regulations and testing of xenografts are quite extensive. The raw material is sourced from the long bones of US cattle only. The material is processed by heat and chemicals to ensure that it is sterile and prionfree. For Bio-Oss the proof of deorganification is obtained through BioRad assay, SDS-PAGE testing, and SDS-PAGE + Western blotting.16,17 To date, there has never been a case of disease transmission attributed to particulate xenografts. Evidence-Based Decision Making: Implant Surfaces A second variable that affects implant survival in sinus grafts is the surface texture of the implants that are placed in the graft. Both the Wallace (Table 2) and Del Fabbro (Table 3) reviews show a dramatic difference in implant survival when comparing rough to machined implants.5,6

The large difference observed in implant survival in both of the reviews is most likely a result of differences in implant bone contact achieved by the rough and smooth surfaces in the grafted sinuses. Non-sinus studies using special

implants that have both surfaces on the same implant show a large difference in implant bone contact between the surfaces. By having both surfaces on the same implant, these studies rule out the variable of comparing implants that were placed in different sites. The study by Lazzara showed bone implant contact for Osseotiteb and machined surfaces to be 79.7% and 46.5%, respectively in good quality bone but only 51.7% and 8.1% respectively in poor quality bone.18 Trisi, in a similar study, has shown that the bone-implant contact with machined implants is usually less than you would expect given the bone quality of the receptor site.19 On the contrary, the Osseotite surface always had better than expected bone contact. Dziedzic has shown that the textured Osseotite surface is better able to stabilize the blood clot on the surface, allowing for bone formation directly on the surface (contact osteogenesis).20 The inability of the machined surface to stabilize the blood clot leads to retraction of the clot and bone formation away from the implant surface (distance osteogenesis). A recent retrospective analysis at the New York University Department of Implant Dentistry has shown that machine-surface implants are much more likely to fail than implants with textured surfaces when placed in sinus grafted cases with reduced residual crestal bone height (SS Wallace and colleagues, unpublished data, 2005). This is yet another clinical deficiency resulting from the poor bone implant contact that is established with a machined surface. Evidence-Based Decision Making: Membranes Membrane placement is the third major variable evaluated in the sinus reviews. The Wallace review has shown that the use of a barrier membrane over the lateral window has a positive effect on implant survival.5 The 3 controlled trials listed in Table 414,21,22 all showed higher implant survival rates when a membrane was used. Twenty additional studies showed implant survival with a membrane to be 93.6% compared with 88.7% without a membrane.

The advent of guided bone regeneration techniques in the early 1990s improved our ability to repair compromised implant receptor sites. Sinus grafting may be considered as a form of guided bone regeneration within a cavity. Guided bone regeneration uses membranes to isolate the area of regeneration, maintain space, and exclude nonosteogenic connective tissue from the graft site. When a membrane is placed over a grafted bone defect, completely sealing the defect from the outside environment, the following characteristics are observed in the regenerated tissue beneath the membrane: 1. corticalization of the graft surface 2. contiguity of the graft particles 3. increased vascularity of the graft Histological studies of sinus grafts by Tarnow and colleagues and Froum and colleagues both show these changes as well as a dramatic increase in vital bone content when a membrane is used compared with cases where it is not used (25% and 11.8%, respectively in the Tarnow study).14,21 As in guided bone regeneration, the first membranes used in sinus grafting were nonresorbable GORE-TEX e-PTFEc membranes. To be effective, these membranes had to be fixated by tacking them to the bone surface. Removal of the membrane required the flap reflection at the time of implant placement surgery to be as extensive as it was for the lateral window surgery. If bioabsorbable barrier membranes could be used over the lateral window and achieve the same results, this latter surgery could be less extensive and therefore less traumatic. A recent study has compared the results using either absorbable (Bio-Gidea) or nonabsorbable barrier membranes (GORE-TEX e-PTFE) over the lateral window.23 The results showed both a similar vital bone formation (17.6% and 16.9%, respectively) and a similar implant survival rate (97.6% and 97.8%, respectively) for the 2 types of membranes. Figure 4 shows a completely regenerated lateral window area 8 months after sinus grafting with Bio-Oss and a Bio-Gide membrane placed over the window. Surgical Technique A biologically based surgical approach that provides a large blood supply to the graft appears to be beneficial to achieve the highest level of success in the

sinus grafting procedure. The vascular supply to the grafted site comes from the bony walls of the sinus. A proper elevation of the Schneiderian membrane must include elevating the membrane from the medial wall of the sinus. This will double the blood supply to the graft, allowing for a more rapid formation of vital bone and a reduction of the time necessary for graft maturation (Figures 5 and 6). The lateral window technique begins with a full-thickness mucoperiosteal flap to gain access to the lateral bony wall of the sinus. An antrostomy, or window, is made in the lateral wall with either a diamond bur (using either a surgical or a high-speed hand piece) or with Piezosurgeryd. The bony window can then be rotated horizontally along with sinus membrane elevation, or it can be completely removed. The Schneiderian (sinus) membrane is reflected across the sinus floor and then superiorly up the medial sinus wall. The elevated membrane thus becomes the superior and distal walls of a compartment in the lower third of the sinus that will receive the bone graft. Once the graft material is placed, the lateral window should be covered with a biologic barrier membrane before suturing the flap back into position. The graft is allowed to mature (formation of new bone around the graft particles) before implant placement (delayed approach), or the implants may be placed simultaneously with grafting if sufficient crestal bone is present to stabilize them. The implants are given sufficient time to integrate in the grafted sinus and then restored with traditional implant prosthetic components. The surgical procedure is demonstrated in Figures 7 through 14.

Piezosurgery is a technique new to the United States that has an 8-year history of use in Europe. It is a safe, clean, and atraumatic technique for gaining access to the sinus. Initial studies by the New York University sinus research team show a reduction in sinus membrane perforations from the typical average of 30% to 7% in a study of over 100 consecutive cases24 (Figures 15 through 18). Conclusion One result of the Wallace evidence-based review was the publication of the following statement by the American Academy of Periodontology: There is evidence to indicate that the lateral window technique for the sinus bone augmentation procedure is successful at regenerating sufficient bone for implant placement. The implant survival rate is greater than 90%, which is similar to implants placed in native bone.5 The evidence-based reviews further identified some of the important variables that affect the outcome of this procedure. These variables are as follows: 1. Particulate bone grafts result in a higher survival rate than block grafts. 2. Bone replacement grafts result in a higher implant survival rate than autogenous bone or composite grafts. 3. Rough-surface implants result in a higher survival rate than machinesurfaced implants. 4. Membrane placement over the lateral window results in a higher implant survival rate than if a membrane is not used. Additional studies were presented in this article, showing that the xenograft BioOss achieves its predictable success through a combination of its osteoconductivity, its characteristic slow resorbability, and its lack of interference with the process of osseointegration. Evidence was also presented to show that, with regard to bone formation and implant survival, comparable positive effects are achieved with the bioabsorbable Bio-Gide and the nonabsorbable GORE-TEX e-PTFE barrier membranes. A clinician can use an evidence-based decision-making process to dramatically improve implant survival rates in the grafted maxillary sinus. In the Wallace evidence-based review, the average implant survival for the lateral window

procedure was 91.8%.5 By making the 2 decisions to use rough-surfaced implants and particulate bone grafts, the implant survival rate became 94.5%. By making a third decision to place a membrane over the lateral window, the implant survival rate became 98.6%. The ability to place implants in the compromised posterior maxilla with a very high predictability will allow us to more predictably treat our patients with more favorable treatment plans. Patient function and comfort will be improved if we choose to place fixed restorations instead of removable dentures in our partially and completely edentulous patients.

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24. Wallace SS, Mazor Z, Froum SJ, et al. Sinus membrane perferation using piezosurgery: clinical results of over 100 cases. Int J Periodontics Restorative Dent. 2006; in press.