Volume 8 • Number I • December 2003 Effect of Maxillary Sinus Augmentation on the Survival 6 3 of Endosseous Dental Implants. A Systematic Review Stephen S. Wallace and Stuart J. Froum Department of Implant Dentislry, New York University, New York. New York. Background: Grafting the floor of the maxillary sinus has become the most common surgical intervention for increasing alveolar bone height prior to the placement of endosseous dental implants in the posterior maxilla. Outcomes of this procedure may be affected by specific surgical techniques, simultaneous versus delayed implant placement, use of barrier membranes over the lateral window, selection of graft material, and the surface characteristics and the length and width of the implants. Rationale: The primary objective of this systematic review was to determine the efficacy of the sinus augmentation procedure and compare the results achieved with various surgical techniques, grafting materials, and implants. Focused Question: In patients requiring dental implant placement, what is the effect on implant survival of maxillary sinus augmentation versus implant placement in the non-grafted posterior maxilla? Search Protocol: MEDLINE, the Cochrane Oral Health Group Specialized Trials Register, and the Database of Abstracts and Reviews of Effectiveness were searched for articles published through April 2003. Hand searches were performed on Clinical Oral Implants Research, International Journal of Oral and Maxillofacial Implants, and the InternationalJournal of Periodontics & Restorative Dentistry and the bibliographies of all relevant papers and review articles. In addition, researchers, journal editors, and industry sources were contacted to see if pertinent unpublished data that had been accepted for publication were available. Selection Criteria Inclusion criteria: Human studies with a minimum of 20 interventions, a minimum follow-up period of 1-year loading, an outcome measurement of implant survival, and published in English, regardless of the evidence level, were considered. Exclusion criteria: Studies involving multiple simultaneous interventions (e.g., simultaneous ridge augmentation) and studies with missing data that could not be supplied by the study authors were excluded. Data Collection and Analysis: Where adequate data were available, subgroups of dissimilar interventions (e.g., surgical techniques, graft materials, implant surfaces, membranes) were isolated and subjected to metaregression, a form of meta-analysis. Main Results 1. Forty-three studies. 3 randomized controlled clinical trials (RCTs), 5 controlled trials (CTs), 12 case series (CS), and 23 retrospective analyses (RA) were identified. Thirty-four were lateral window interventions, 5 were osteotome interventions, 2 were localized management of the sinus floor, and 2 involved the crestal core technique. 2. Meta-regression was performed to determine the effect of the variables of block versus particulars grafting techniques, implant surface, graft material, and the use of a membrane over the lateral window. 3. The survival rate of implants placed in sinuses augmented with the lateral window technique varied between 61.7% and 100%. with an average survival rate of 91.8%. For lateral window technique: 4. Implant survival rates reported in this systematic review compare favorably to reported survival rates for implants placed in the non-grafted posterior maxilla. 5. Rough-surfaced implants have a higher survival rate than machine-surfaced implants when placed in grafted sinuses. 6. Implants placed in sinuses augmented with particulars grafts show a higher survival rate than those placed in sinuses augmented with block grafts. 7. Implant survival rates were higher when a membrane was placed over the lateral window. 8. The utilization of grafts consisting of 100% autogenous bone or the inclusion of autogenous bone as a component of a composite graft did not affect implant survival. 328 Ann Periodontol Wallace, Froum 9. There was no statistical difference between the covariates of simultaneous versus delayed implant placement, types of rough-surfaced implants, length of follow-up, year of publication, and the evidence level of the study. Reviewers' Conclusions: Insufficient data were present to statistically evaluate the effects of smoking, residual crestal bone height, screw versus press-fit implant design, or the effect of implant surface micromorphology other than machined versus rough surfaces. There are insufficient data to recommend the use of platelet-rich plasma in sinus graft surgery. Ann Periodontol 2003:8:328-343. KEY WORDS Inadequate alveolar bone height is a common limitation in the placement of endosseous root-form dental implants in the posterior maxilla. Grafting the floor of the maxillary sinus has emerged as the most common surgical modality for correcting this inadequacy. This technique, first published in 1980 by Boyne and James1 and subsequently modified by other clinicians, 2"10 can result in an increase in bone height that allows the placement of implants of conventional length in the grafted sites. In addition to the various techniques utilized to elevate the sinus floor, there are many variables that may alter the outcome of this procedure. Among them are simultaneous versus delayed implant placement; the use of a barrier membrane over the lateral window; the use of various grafting materials; and the utilization of implants with varying surface characteristics, lengths, and widths. Further, the effects of smoking and residual crestal bone height may also influence outcomes. The goal of this review was to assess the efficacy of the sinus augmentation procedure by systematically reviewing the available literature. RATIONALE The goal of this review was to assess the efficacy of the sinus augmentation procedure by systematically reviewing the available literature. FOCUSED QUESTION This review address the following question: "In patients requiring dental implant placement, what is the effect on implant survival of maxillary sinus augmentation versus implant placement in the non-grafted posterior maxilla?" SEARCH PROTOCOL Data Sources and Search Strategy The search protocol chosen by the authors utilized 3 electronic databases: MEDLIME from 1980 through April 2002 utilizing the Ovid search engine; the Cochrane Oral Health Group Specialized Trials Register through April 2002; and the Database of Abstracts of Reviews of Effectiveness through April 2002. The search strategy for electronic databases utilized a combination of MeSH terms and text words to create both a specific (human, English, randomized controlled trials, and meta-analysis) and a sensitive database. The search strategy and results utilized for MEDLINE are shown in Table 1. The search was supplemented by a thorough manual search of the following journals; Clinical Oral Implants Research, International Journal of Oral and MaxMofaciat Implants, and Internationa! Journal of Periodontics & Restorative Dentistry from 1980 or journal inception through the cut-off date of April 1, 2002, along with a search of the bibliographies of all relevant papers and review articles. As part of the review process, researchers were contacted when possible to fill in missing data or clarify ambiguous data in previously published reports. Known researchers, journal editors, and industry sources were contacted to determine if pertinent unpublished data that had been accepted for publication were available. All search strategies were updated to extend the cut-off date to April 1, 2003. Both the titles and abstracts from the search were independently screened for inclusion by the review authors. The full text of all studies of possible relevance were obtained and independently reviewed by the review authors (SSW, SJF). Disagreements at each level of the review process were resolved by discussion. Inclusion criteria: All studies involving the placement of root-form screw or cylinder implants in augmented maxillary sinuses were considered. An outcome measure of implant success or implant survival had to be reported. As the number of randomized controlled clinical trials (RCTs) was found to be limited, all levels of evidence including controlled trials (CT), case series (CS), and retrospective analyses (RA) were selected for further evaluation by the inclusion criteria. The original inclusion criteria for this review were as follows: 1) human, English language publications; 2) minimum of 20 interventions (i.e., lateral window sinus augmentations or osteotome elevations); 3) outcome measure of implant success or implant survival reported; 4) absence of multiple interventions (e.g., simultaneous ridge augmentations); 5) minimum of 1-year loaded follow-up (or a range that exceeds 1 year); and 6) a dropout/withdrawal rate of <5%. Exclusion criteria: Studies involving multiple interventions (e.g., simultaneous ridge augmentation) and 329 Effect of Sinus Augmentation on Implant Survival Volume 8 • Number I • December 2003 Table I. MEDL1NE Search Terms and Results 1. exp Dental Implants/ 2. exp Dental Implantation/ 3. 1 or 2 4. exp Bone Transplantation/ 5. exp Bone Remodeling/ 6. 4 or 5 7. exp Maxillary Sinus 8. exp Maxilla/ 9. 7 or 8 10. 6 and 9 1 1, exp Alveolar Ridge Augmentation/ 12. 10 or II 13. 12 and 3 14. maxillary sinus grafting.mp. 15. sinus augmentation.mp. 16. sinus lift.mp. 17. sinus elevation.mp. 18. 14 or 15 or I6or 17 19. 12 or 18 20. 19 and 3 21. limit 20 to (human and English language) 22. from 21 keep 1-858 23. limit 3 to (human and English language and metaanalysis or randomized controlled trial) 24. limit 19 to (human and English language and metaanalysis or randomized controlled trial) 25. limit 20 to (human and English language and metaanalysis or randomized controlled trial) 4,846 9,317 11,379 13,455 25,098 36,692 5,180 11.893 16,781 1,478 1,226 2,483 1,037 10 69 79 38 170 2,516 1,058 858 858 119 24 18 studies with missing data that could not be supplied by the study authors were excluded. Ranking of Studies Study quality was independently assessed by the reviewers and the studies grouped by general category (RCT, CT, CS, and RA). Data Collection and Analysis Multiple confounding relationships may result in significant differences in the outcome measurement of implant survival. Where adequate data existed, subgroups of dissimilar interventions (e.g., surgical technique, graft material) were isolated and subjected to meta-regression, a form of meta-analysis, to identify them as possible sources of covariance. Data sheets were prepared to extract all data of possible relevance for statistical analysis of study variables. The extraction was performed independently by both reviewers to insure accuracy. Missing data were filled in, when possible, by correspondence with the study authors. MAIN RESULTS Methodological Quality Overall study quality was deemed poor, with RCTs and CTs accounting for only 18.6% of the included studies (8 of 43). With modification of the inclusion criteria agreed upon early in the process, initial agreement between the reviewers was high with all disagreements resolved after discussion (6 studies) or the procurement of additional data from the study authors (6 studies). Rating of the included studies by defined criteria such as those of Jadad et a l . " based upon criteria including randomization, masking, and withdrawals (loss to followup) was not practical. Since loss to follow-up was unrecorded or unclear in 18 of the 43 studies (41.9%), this requirement was eliminated from the inclusion criteria of this review. Thirty-two out of the 43 studies (74.4%) used implant survival as the primary outcome measure. Among those that reported implant success, the criteria for success varied greatly. Therefore, implant survival (i.e., implant remains in function, no pain or mobility, no radiographic evidence of infection) was chosen as the default outcome, even if both values were given. Furthermore, in many studies implant survival was not reported for a standard time interval, but was reported as a range. This was accepted, with a minimum of 12 months of loading considered for inclusion in this review. Data Extraction The search strategy revealed 893 (858 electronic search, 35 manual search) articles of possible relevance. One hundred and fifty-six (156) of these articles were evaluated in full-text version and 43 met the modified inclusion criteria. Of these, 3412'45 utilized lateral window interventions, 5 utilized the osteotome technique,46"50 2 utilized localized management of the sinus floor (LMSF),51-52 and 2 utilized crestal core elevation techniques.53-54 The number of qualifying studies of each study design (RCT, CT, CS, or RA) for each of the 4 interventions (lateral window, osteotome, localized management of the sinus floor, and crestal core elevation) are shown in Tables 2 through 5. The combined raw implant data for each intervention, and the overall combined implant data are listed in Table 6. 330 Ann Periodontol Wallace, Froum Table 2. Summary of Data from Lateral Window Sinus Augmentation Studies Reference Study Type Placemeit Implant Membrane Graft N N N N Material Lift? Implants Survived Failed Survived Boyneetal.12 2003 Boyne et al.'2 2003 Tamow et al.'' 2000 Wannforsetal.M 2000 2001 Froum etal.16 1998 Blomqvist etal.l / 1998 Valentini &Abensur18 1997 Engelke etal.'9 2003 Hallmanetal.20 2002 Hallman etal.21 2002 Kahnbergetal.22 2001 RCT RCT RCT RCT CT CT CT CS CS CT CS CS Delayed Delayed Delayed Immediate/ delayed Immediate/ delayed Immediate/ delayed Delayed Immediate/ delayed Immediate/ delayed Delayed Delayed Immediate Various Various Various Machined screw Machined screw Various screws Machined screw 52 cylinder; 8 screw Various titanium Machined screw Machined screw Machined screw None None ePTFE or none None Por coll or none Various or none None None None None None None Autog autog + allo BMP-2/collagen sponge Various Iliac block vs. particulate BPBM 100% Xenograft with or without DFDBA/ autog Iliac block + cancellous chips BPBM + DFDBA 1:1 TCP, TCP + autog ChiaBPBM (1:4) Various Iliac block + cancellous [ 1 iir>S 24 (A 2.4 80 30 113 100 28 118 30 36 39 63 56 55 150 61 215 202 60 21 79 II 91 Valentini etal." 2000 van den Bergh etal.2« 2000 van den Bergh etal25 1998 Pelegetal.26 1998 Block & Kent27 1995 Keller etal.2B 1994 CS Delayed Not None specified CS Delayed Screw None CS Immediate/ Screw None delayed CS Immediate HA cylinder DLB CS Immediate/ HA cylinder None defayec and screw CS Immediate Not None specified BPBM DFDBA Iliac cancellous bone chips 1:1 iliac + DFDBA 20 30 20 various autog & 51 autog composites 57 69 62 161 55 173 51 131 161 55 171 12 25 126 24 52 21 I 170 32 56 35 56 I 69 0 81 83 96.4 84 85.2 98.2 84.2 56 200 73 101 4 II 6 10 93.3 94.8 92,4 91 61.2 98.2 100 0 100 100 98.9 hac block 23 66 Effect of Sinus Augmentation on Implant Survival Volume 8 • Number I • December 2003 Table 2. (continued) Summary of Data from Lateral Window Sinus Augmentation Studies Reference Study Type Placement Implant Membrane Graft Material Various composites BPBM + PRP BPBM, BPBM + symphysis BPBM or autogenous bone Iliac & mandh bular block N Ufts 69 24 36 42 39+ N Implar 158 70 104 98 31 Lozadaetal.29 1993 Rodriguez etal.30 2003 Hismg etal.31 2001 Lorenzoni et aJ.32 2000 Johansson et al.33 1999 Keller etal.34 1999 Khoury35 1994 fielegetal.16 Watzeketal.37 CS RA RA RA RA RA RA RA RA Immediate/ delayed Immediate Delayed Immediate/ delayed Immediate Immediate Immediate Immediate Delayed Various Various Various; 88% machined Screw Machined screw Machined screw Various HA cylinder Cylinder None None None Various None None ePTFE or none DLB None and Screw Kapteinetal.38 1998 Fugazzotto & Vlassis19 1998 Ellegand etal.40 1997 Block& Kent11 1997 Hurzeleretal.42 1996 Wheeler etal.43 1996 Blomqvist etal.44 1996 Small etal.4S 1993 RA RA RA RA RA RA RA RA Immediate/ delayed Immediate/ delayed Immediate Immediate Immediate/ delayed Immediate/ delayed Immediate Immediate HA cylinder TPS cylinder Screw Not specified 54 cylinder; 6 machined screw Machined screw TPS, HA cylinder None None None None ePTFE None None Collagen Iliac block Mandibular block + paniculate 58 216 I: I symphysis + 63 DFDBA cancellous 40 iliac, iliac + BPBM or lnt-200 2:1 iliac cancel- >88 bus + nonresorbable HA Various non-autogenous None 24+ Iliac/tibial mar- 53 row, intraorat Various HA. HA + iliac, HA + intraoral Iliac block 168 34 139 467 160 145 388 217 510 38 173 340 64 93 171 DFDBA & HA 20+ 76 145 65 160 139 35 336 61 41 76 13 92 92.9 86 18 82.7 92 6 92.7 100 31 75,3 119 20 85.6 439 28 94 0 100 95.9 342 46 88.1 495 15 97 92.1 153 20 88.4 98.8 95.3 30 82.5 0 100 Abbreviations: auto = autogenous; allog = allograft; BPBM bovine porous bone mineral; BMP = bone morphogenetic proteins; DFDBA = demineraliied Freeze dried bone allograft; DLB = demineralized laminar bone; ePTFE --• expanded polytetrafluoroethylene; HA = hydroxyapatite; por coll = porcine collagen; PRP -- platelet-rich plasma; TCP = tricalcium phosphate; TPS = titanium-sprayed surface. 332 Ann Periodontol Wallace, Frourti Table 3. Summary of Data from Osteotome Sinus Augmentation Studies Reference Study Type Placement Implant Graft N N N N Material Lifts Implants Survived Tailed % Withdrawn % Survived Zitzmann & Scharer16 1998 Deporteret al.4' 2000 Rosen et al/18 1998 Coatoam & Krieger*9 1997 Cavicchia et al.i0 2001 CT CT RA RA RA Immediate Immediate Immediate Immediate Immediate Machined screw Rough surface cylinder Various 4, mostly rough cylinder Cylinder and screw BPBM BPBM Various DFDBA + minimum auto colfagen sponge auto 59 26 174 89 97 59 26 174 89 97 56 26 66 82 86 0 94.9 100 95.4 92.1 88.6 * Mot reported. Abbreviations: BPBM = bovine porous bone mineral; auto . autogenous; DFDBA = demineralized freeze-dried bone allixjraft. Table 4. Summary of Data from Localized Management of Sinus Floor Studies Reference Study Type Placement Implant Graft N N N N Type Material Lifts Implant Survived Failed % Withdrawn % Survived Bruschi etal.51 1998 Winter etat.52 2002 Not reported. RA RA Immediate Immediate Cylinder and screw Screen Collagen sheet None 499 58 499 58 487 53 12 5 97.5 91.4 Table 5. Summary of Data from Crestal Core Elevation Studies Reference Toffler>3200l Fugazzotto & De Paoli54 2002 Study Type RA RA Placement Delayed Delayed Implant Type Various Screw Graft Material Auto + BPBM or P-15 BPBM N Lifts 37 137 N Implants 37 137 N Survived 37 134 N Failed 0 3 0/ Withdrawn 0% * % Survived 100 97.8 • riot rrporttd Abbreviations: auto ; autogenous; BPBM: bovine porous bone mineral; P-15 - peptide 15- 333 Effect of Sinus Augmentation on Implant Survival Volume 8 • Number I • December 2003 Table 6. Combined Sinus Implant Data for all Interventions Intervention N Lifts N Implants Lateral window (34) 2,178 5.267 Osteotome (5) 445 445 Localized management 557 557 of sinus floor (2) Crestal(2) 174 174 Total 3.354 6443 N Survived 4.836 416 540 N Failed 431 29 17 % Survived 91.8 93.5 96-9 171 5,963 480 98.3 92.6 Table 7. Survival Rates for Rough Versus Machined Implants Surface Standard Error Mean Least Square Mean* Machined Rough 1.98 2.82 82.4 95.2 84.0 91.6 * Includes adjustments for other variables. Table 8. Survival Rates for Implants Placed in Iliac Blocks Versus Particulate Grafts Graft Standard Error Mean Least Square Mean* Iliac block Particulate 2.96 1.72 80.4 94.8 83.3 92.3 * Includes adjustments for other variables. Table 9. Interaction of Covariates Machined/Rough, Iliac Block/Particulate Surface/Intervention Machined/iliac block Machined/particulate Rough/iliac block Rough/particulate N Stjdies 6 3 1 24 Lower 95% Cl 73.8 83.4 - 92.2 Upper 95% Cl 83.8 96.6 - 97.0 Standard Error 2.5 3.3 6.1 1.2 Mean 78.8 89.5 90,9 94.5 Least Square Mean* 78.8 90.0 89.5 94.6 • Includes adjustment for other variables. Statistical Analysis Statistical analysis was utilized to determine what factors may have influenced the survival rate of the implants placed in the grafted sinuses. Factors evaluated included the secondary outcome measures of various surgical techniques, grafting materials, implant surface micromorphology, presence of a barrier membrane over the window, simultaneous versus delayed implant placement, and length of follow-up. The following 3 factors were found to be related to implant survival: 1) machined implants versus rough implants (84.0% and 91.6%, respectively) (Table 7); 2) iliac block grafts versus particulate grafts (83.3% and 92.3%, respectively) (Table 8); the above-mentioned effects with the appropriate interaction between the 2 were modeled along with the covariates of year published and the length of followup (Table 9); 3) membrane versus no membrane over lateral window (93.6% and 88.7%, respectively). Table 10 identifies 3 studiesl3-15-'6 that directly compared implant survival following use or non-use of a membrane. In each of the 3 studies, implant survival was significantly higher when a membrane was utilized. Figure 1 presents a meta-analysis of the data from the 3 above-mentioned studies. Table 1 I gives implant survival statistics for all studies utilizing particulate grafting techniques with (5 studies) and without (15 studies) a membrane over the lateral window. As can be seen in Table 12, statistical evaluation did not indicate a difference between simultaneous versus delayed placement. Additionally, implant type (except machined), autogenous (particulate) versus bone replacement grafts, evidence level of study, length of follow-up, and year of publication were not related to implant survival. While we tested and did not find differences between the studies for the above factors, it is possible that other factors (e.g., residual crestal bone height, smoking) could be covariables that influenced these results. There were insufficient data available to evaluate the effects of residual crestal bone height and the effect of smoking on the survival of implants placed in augmented sinuses. DISCUSSION The goals of the sinus elevation procedure are 3-fold: the formation of vital bone in the pneumatized sinus, inte- 334 Ann Periodontol Wallace, Froum Table 10. Membrane Versus No Membrane (intrastudy comparison): Implant Survival Data Reference Tamow, et a l ' ' (RCT) Tawil & Mawla15 (CT) Froum, etal16 (CT) With Membrane 28 implants 100% 29 implants 93.1 133 implants 99.2% Without Membrane 27 implants 92.6% 32 implants 78.1% 82 implants 96,3% gration of implants in that bone, and long-term survival of those implants when placed under functional load. Since the first publication of this technique by Boyne and James1 in 1980 there have been many changes in implant surfaces, grafting materials, and surgical techniques. This report utilized an evidence-based review of the literature (893 studies) to establish a reliable data base (43 studies) that satisfied the selected inclusion criteria. These data were subjected to meta-regression, a form of meta-analysis, to answer the primary question relating to overall implant survival. Secondary questions relating to various surgical techniques, grafting materials, and implant surfaces were also subjected to comparison by meta-regression to determine if these potentially confounding relationships resulted in significant statistical differences. Methodological Quality Any discussion of the data presented in this systematic review must be preceded by a discussion of the methodological quality of the studies that comprise the data for the review. Study quality was deemed poor. Only 8 of 43 studies were randomized controlled clinical trials or controlled trials and, with the exception of 2 studies.1214 investigative rigor was deemed fair to poor. Randomized controlled human clinical trials, utilizing a split-mouth design, that compare the survival of implants placed in grafted sinuses to that of implants placed below the sinus floor in the nongrafted posterior maxilla, would be difficult to conduct and to date data of this kind do not exist. For this reason intra-study comparisons of implant placements in grafted sinuses to implants placed in the nongrafted posterior maxilla were not possible. Furthermore, there is a paucity of published data reporting on aborted or failed sinus grafting procedures that precluded implant placement. This would not result in a change in the impiant survival rate of placed implants. but it must be accounted for in a comparison of patient outcomes. The effectiveness of meta-analysis is dependent not only upon the quality of the included studies, but their similarity. Meta-analysis generally involves studies that are comparative in nature and is strongest when the level of evidence includes high quality RCTs. Evaluation of data from multiple studies that are one-group designs requires meta-regression. Dissimilar inter-ventions (surgical techniques), variable graft maturation and osseointegration times, varying follow- up times, differing criteria for success, the utilization of multiple grafting materials, and diverse implant macro- and micromorphologies can effect the validity of the analysis. For that reason, the present review attempted to isolate some of the significant variables to determine their effect on the overall database. Metaregression evaluates the many covariates that exist between studies to try to insure that differences in results are, in fact, real effects.55 In 1998 Jensen et al.56 published the data from the Academy of Osseointegration Sinus Consensus Conference of 1996. This report included a meta-analysis of the data collected from 38 surgeons who performed 1,007 sinus grafts with 2,997 implants placed and followed for a minimum of 3 years. The overall survival rate was reported as 90%. This report is not included in the present review as it contains data from both published and unpublished sources. Furthermore, the data from that conference would represent a duplication of some of the studies included in this review. Previous evidence-based reviews of the maxillary sinus augmentation procedure have been published by Tolman57 and Tong et al.s8 Tolman57 selected 58 of 352 screened articles for inclusion in a meta-analysis of varying grafting proce- Reference Froum" 1998 Tarnow 2000 Tawil" 2001 Fixed Combined (3) Figure 1. Effect of the use of a barrier membrane. Treated 1 /133 0/28 2/29 3/190 Control 3/82 2/27 7/32 12/141 Effect 0.199 0.179 0.265 0.229 N Total 215 55 61 331 PValm 0.126 0223 0.099 0.019 0.01 0.1 100 Membrane Without Membrane 335 Effect of Sinus Augmentation on Implant Survival Volume 8 • Number I • December 2003 Table I I . Membrane Versus No Membrane: Implant Survival Data Membrane Reference Standard Error Mean Least Square Mean* No; IS studies 14,18.20.21,23.25, 2.37 93.5 27,29 33, 37,38, 39, 40,41.43 Yes; 5 studies 26.32.36,42,45 3.13 98.6 88.7 93.6 * Includes adjustment For olher variables. Table I 2. Simultaneous Versus Delayed Placement: Summary of Implant Data Placement Simultaneous (all) Delayed (all) Simultaneous (mixed) Delayed (mixed) Total simultaneous Total delayed N Studies 12 9 8 8 20 17 N implants 1.637 1,041 547 655 2,184 1,696 N Survived 1.459 929 499 591 1.958 1,520 N Failed 178 112 48 64 226 176 % Survived 89.1 89.2 91.2 90.2 89.7 89.6 dures in the mandible and maxilla. Inclusion criteria were not specifically stated. Included studies were those that were clinically related with data on implants placed in grafted bone. Overall survival rates for implants placed in grafted sinuses were reported as 91% for implants placed in block grafts and 94% for implants placed in particulate grafts. Survival rates were lower for delayed placements than for immediate placements in both the block graft group (84% and 92%, respectively) and the particulate graft group (91% and 100%, respectively). A disproportionate number of the failures in the delayed particulate group (301 implants) involved a small number of machined implants (12 of 35 implants). In the delayed block graft group (61 implants), a small number of TPS cylinder implants accounted for the higher failure rate (8 of 24 implants). Tong et al.58 selected 10 of 28 identified articles for inclusion in their meta-analysis. Inclusion criteria were 1) at least 10 patients; 2) all patients received root-form endosseous implants; 3) less than 5% of patients were lost to follow-up over a 6-month period; 4) patient follow- up was no less than 6 months; and 5) data regarding survival of implants were reported. The overall survival rate for the 1,096 implants included was 93%.58 An independent evidence-based review on the lateral window technique by Del Fabbro etal.,59 submitted concurrently with the present review, selected 39 studies for inclusion. Of these, 29 were included in the present review along with 5 studies which they did not consider. The overall implant survival rate for the 6,990 implants included in their review was 91.3%. The inclusion criteria for the present review, while far from rigorous, appear to be more selective than those utilized in the previous reviews. Furthermore, they were designed so as not to exclude earlier studies that tended to be retrospective nature, yet may not have been as susceptible to publication bias as the more recent studies. As techniques become more universally applied, the overall quality of studies tends to improve. The present review reports on 3,354 interventions and 6,443 placed implants with an overall survival rate of 92.6%. In studies that utilized only the lateral window technique, the reported survival rate for 2,178 interventions with 5.267 implants placed was 91.8%. The database for this review is larger than that of the 3 previously mentioned reviews combined56"58 and somewhat smaller than the Del Fabbro et al. review59 with regard to lateral window placements. This reflects the recent increase in studies relating to sinus grafting after the 1996 Academy of Osseointegration Sinus Consensus Conference concluded "The sinus graft should now be considered a highly predictable and effective therapeutic modality." 56 Although the large number of interventions included in this review may be the result of liberal inclusion criteria that accepted respective studies, all the studies included for analysis do have the minimum 1-year loaded follow-up. The survival rate for implants placed in grafted sinuses compares favorably to those generally reported for implants placed in pristine bone in the non-grafted posterior maxilla.60"67 Results from 8 studies that isolate success/survival data for implant placement in the non-grafted posterior maxilla, adjusted to raw survival data, appear in Table 13. The survival rate averaged 95.1%. Results of a 3-year Veterans Administration study reported a 97.5% survival rate for 120 implants placed in grafted sinuses compared to a 90.3% survival rate for 453 implants placed in the non-grafted posterior maxilla in a conventional manner.64 It should be 336 Ann Peiiodontol Wallace, Frourn Table 13. Survival Rates of Conventionally Placed Implants in the Posterior Maxilla Reference Nevins and Langer*0 1993 Bahat61 1993 Buser et al.63 ?000 Bahat61 2000 Olson et al.M 2000 DePorteretal/'s200l Testorietal.66200l Testorietal.672002 Total Implant Type Screw Screw m Screw Various Rough surface cylinder Screw Screw Placed 652 732 298 660 453 118 184 123 • . , . • • • N Implants Survived 621 697 293 625 409 116 181 121 3.063 Failed 31 35 5 35 44 2 3 2 157 % Survived 95.2 95.2 98-3 94.7 90.3 98.3 9fi.4 98.4 95.1 noted that none of these studies presented a splitmouth randomly controlled methodology. The present review further identified 3 interventions that were not included in the 2 earlier reviews. The osteotome technique (5 studies,46'50 445 implants, and 93.5% survival), localized management of the sinus floor (2 studies,51'52 557 implants 96.9% survival) and the crestal core elevation/extraction socket technique (2 studies,5334 174 implants, 98.3% survival). While these results appear promising, the data are insufficient for statistical analysis. Grafting Materials The Academy of Osseointegration Sinus Consensus Conference of 1996 approved autogenous bone as acceptable for sinus grafting, further stating that other grafting materials (i.e., allografts, xenografts, and alloplasts) may be acceptable, but required further evaluation. 56 That evaluation has been forthcoming over the past 7 years. The present review found that the block grafting technique results in a statistically significant lower implant survival rate (83.3%) than do all paniculate grafts combined (92.3%). The lower survival rate may be indicative of a more demanding surgical procedure which requires stabilization of the block graft as well as the implant, the tendency of the iliac block graft to resorb and the covariable effect of the use of machinesurfaced implants in 6 of the 7 block graft Studi o 14.17,22.33.34.44 T h e r e v j e w b y De] pabbro et al.59 noted that 69.5% of all implants placed in 100% autogenous bone grafts had a machined surface. These machined implants accounted for 87.8% of the failures in that group. The present review identified one well conducted RCT by Wannfors et al.14 that compared simultaneous placement of implants in iliac block grafts to delayed placement in autogenous particulate grafts. The study included 20 patients in each group and an almost identical number of implants (76 and 74, respectively). Survival rates for implants placed in the iliac blocks and the particulate grafts were 78.9% and 89.2%, respectively. The authors stated that the population was too small to ascribe statistical significance to the results; however, they noted that their preference is now the 2-stage procedure. This review found no statistically significant difference in implant survival when comparing particulate autogenous bone with particulate bone replacement grafts. Froum et al.16 demonstrated similar implant survival rates for a xenograft* when utilized with or without autogenous bone. Hising etal.31 reported a higher implant survival rate in cases where a xenograft+ was used as the sole graft material (92.2%) than when it was used as a composite with autogenous bone (77.2%). In a study by Hatlman et al.21 the implant survival rates for sinuses grafted with particulated ramus autograft, a 20/80 autogenous/xenograff composite, and 100% xenograft* were 82.4%, 94.4%, and 96%, respectively. A review assessing the value of anorganic bone additives by Merkx etal.68 reported that autogenous grafts had a higher percentage of vital bone at 4 to 6 months than did anorganic bone replacement grafts. However, several histological studies16'23'69'70 showed that similar percentages of vital bone can be achieved in bone replacement grafts and in grafts with an autogenous component, provided the bone replacement grafts are allowed a longer maturation period. Further, Valentini et al.23 have reported that residual xenograft in a maturing graft resides in the connective tissue compartment and, when combined with newly formed vital bone, can create a graft of exceptionally high density {i.e., vital bone plus residual mineralized xenograft). Histology of explants from the maxillary sinus do not show residual xenograft particles in con- * OsteoGraf/N, Dentsply/CeraMed Dental, Lakewood. CO. + BioOss. OsteoHealth Co.. Shirley, MY. 337 Fffect of Sinus Augmentation on Implant Survival Volume 8 • Number I • December 2003 tact with the implant surface, thereby leaving the implant surface free to interface with newly formed vital bone.71'72 Implant Surfaces Statistical differences were apparent when comparing machine-surfaced implants versus all other implant surfaces (i.e., rough or textured titanium surfaces, hydroxyapatite- coated surfaces) with unadjusted mean implant survival rates of 95.2% and 82.4% for rough and machined implants, respectively (Table 7). The data on the effect of implant surface micromorphology on implant survival was evaluated in a covariance model with the type of grafting procedure. When this was done (Table 9), the survival rates of rough surfaced and machine-surfaced implants in particulate grafts become 94.6% and 90.0%, respectively. In iliac block grafts the survival rates for rough surfaced and machine-surfaced implants were 89.5% and 78.8%, respectively. Membranes A randomly controlled clinical trial by Tarnow etal.,13 in which the presence or absence of a barrier membrane was the only variable, reported implant survival rates of 100% and 92.6%, respectively, for grafts with and without membranes. A controlled trial by Tawit et al.15 reported 93.1% survival in the membrane group and 78.1% in the no-membrane group. Another controlled trial by Froum et al.16 reported 99.2 % survival in the membrane group and 96.3% when a membrane was not utilized {Table 10). A meta-analysis of these 3 comparative studies {Fig. 1) supports the hypothesis that membrane utilization is a useful adjunctive therapy that results in an increased survival rate {P <0.02) for implants placed in sinus grafts. In a second analysis implant survival in 5 studies with particulate grafts that utilized a membrane over the lateral window was 93.6% for 919 implants, as compared to 88.7% for 2,436 implants in 15 studies that did not utilize a membrane (Table 1]). Again the survival rate for the studies utilizing a membrane (using each study as an N = 1) was significantly better (P<0.05) than for the studies that did not utilize a membrane. The strength of this analysis was increased by the similarity of the survival rates in both the direct comparisons (3 studies)131516 and in the comparative case series (15 versus 5 studies; Table 1 1). The increase in implant survival may be explained by the reported higher percentage of vital bone that results when a membrane is placed over the window. A bilateral RCT with the presence or absence of a membrane over the window being the only variable by Tarnow et al.13 reported vital bone formation of 25.5% (SD 14.5) when a membrane was utilized and 1 1.9% (SD 7.9) when a membrane was not placed over the lateral window. Simultaneous Versus Delayed Implant Placement As presented in Table 2 for the lateral window technique, there are 12 studies with simultaneous placement, 9 studies with delayed placement, and 13 studies reporting on both techniques. Of those reporting on both techniques, 8 studies separated the data. The implant survival rates for the combined simultaneous placement and delayed placement studies (Table 12) were 89.7% and 89.6%, respectively. in evaluating these data, one must consider the number of covariables that are present when implant survival data are combined in non-controlled studies. In this case covariables include, but are not limited to, block versus particulate surgery, machined versus rough surface, and presurgical residual crestal bone height. Residual crestal bone height in the included studies varied from 1 to >8 mm. The ranges for simultaneous or delayed placements overlap, thus blending the 2 intervention types and their subsequent survival rates. Furthermore, not all studies listed the minimum or range of residual crestal bone heights included in the studies (28 of 34 reported). It is reasonable to consider that the failure rate for delayed implants is influenced by the fact that delayed placement is more likely to be utilized in cases that had lesser height of residual crestal bone as opposed to simultaneous placements that are most likely to have a greater height of residual crestal bone. It. should be noted, however, that studies by Peleg et a l .2636 have reported 100% implant survival in simultaneous placements with 1 to 2 and 3 to 5 mm of crestal bone. The data available for this review were insufficient to draw statistical conclusions on the effect of residual crestal bone height on implant survival. While 28 of 34 studies reported residual crestal bone height to range from 1 to >8 mm, none of the studies recorded the residual crestal height of failed implants. Residual crestal bone height, as it relates to achieving primary implant stability, is a primary consideration utilized by the clinician in choosing a simultaneous over a delayed implant placement. Primary stability of implants has always been considered as an important factor affecting implant survival. Given similar bone quality, primary stability should be more easily achieved when a greater height of residual crestal bone is present. However, the significance of having a specific amount of residual bone height can be questioned. DePorter et al.47 showed survival rates for short poroussurfaced implants similar to those reported for standard length implants. Testori et a ] . 6 6 6 7 demonstrated high success rates for short, acid-etched implants in poor quality bone, and Peleg et al.26 reported 100% implant survival for simultaneous placement of hydroxyapatitecoated implants in sinus grafts with 1 to 2 mm of 338 Ann Periodontol Wallace, Frotm crestal bone. This situation highlights the difficulties encountered when attempting to draw conclusions from non-controlled studies due to the presence of multiple confounding variables. The above-mentioned studies all utilized textured or coated implants, while our original paradigms date back to the machine-surfaced implant. In addition, one must consider the differences that may exist in the percent volume of vital bone available for osseointegration when comparing the residual crestal bone to a matured sinus bone graft, d m et al.73 have reported that mean trabecular bone content by volume in the maxillary molar region may be as low as 6.73% and averages 17.1% in females and 23.4% in males. Trisi and Rao74 report trabecular bone volume of 28.28% ± 12.02% for bone quality of D4 (Misch classification). Histological studies by Froum etal.16 and Valentini et al.23 found vital bone volumes in this range for sinus bone replacement grafts. When this is considered in combination with the observation from sinus explants71'72 that residual xenograft does not directly contact the implant surface, it could be speculated that osseointegration in these grafts is not hampered by the presence of the xenograft. In fact, the presence of the xenograft might provide additional structural stability to the matured graft that is lacking in grafts of pure autogenous bone and/or demineralized allograft. If this is correct, residual crestal bone height may only be important as it relates to initial mechanical primary stability, protecting the implant from micromovement resulting from inadvertent early loading. Bone Morphogenetic Proteins and Bone Growth Factors This review identified one rigorously conducted randomly controlled trial by Boyne et al.12 that compared, with similar results, recombinant human bone morphogenetic bone (rhBMP-2)/collagen sponge implants to grafts of autogenous bone and composite grafts containing an autogenous component. A retrospective study by Rodriguez et al.30 utilizing platelet-rich plasma {PRP) with no controls was also identified. This study reported an implant survival rate of 92.9%. This survival rate was lower than the average survival rate of 94.6% for the studies in this review that utilized particulate grafts and rough-surfaced implants without PRP. Histological reports by Froum etal.75 and Wiltfang etal.76 have shown only a 5 to 10% increase in vital bone formation when comparing sinus elevations using the same graft material with and without the .addition of plateiet-rich plasma. Zuffetti et al.77 in an 8-case split-mouth sinus study utilizing cancellous iliac crest marrow, showed no significant differences in bone maturation level resulting from the use of PRP. A preliminary histomorphometric evaluation by Maiorana et al.78 of 2 specimens utilizing 100% xenograft* plus PRP at 6 months postgrafting revealed a total bone percent volume (xenograft plus newly formed bone) of just below 40%. Valentini et al.,23 on the other hand, found a total bone percent volume of 60% for a 1:1 composite of demineralized freeze-dried bone allograft (DFDBA) and the same xenograft in a 6-month time period when utilized without PRP. Sanchez etal.79 in a recent review concluded that there is a lack of evidence for the utilization of PRP in combination with bone grafts based on the existing studies of small sample size and poor quality, most of which have not shown highly positive outcomes. REVIEWERS' CONCLUSIONS Within the limits of this systematic review, the following conclusions can be drawn: 1. The survival rate of implants placed in augmented sinuses varied between 61.7% and 100% with the average survival rate of all interventions being 92.6%. 2. Implant survival rates reported in this systematic review compare favorably to reported survival rates for implants placed in the non-grafted posterior maxilla. 3. Rough-surfaced implants have a higher survival rate than machine-surfaced implants when placed in grafted sinuses. 4. Implants placed in sinuses augmented with particulate grafts show a higher survival rate than those placed in sinuses that had been augmented with block grafts. 5. Implant survival rates were higher when a membrane was placed over the lateral window. 6. The utilization of grafts consisting of 100% autogenous bone or the inclusion of autogenous bone as a component of a composite graft did not affect implant survival. 7. There was no statistical difference between the covariates of simultaneous versus delayed implant placement, types of rough-surfaced implants, length of follow-up, year of publication, and the evidence level of the study. 8. Insufficient data were present to statistically evaluate the effects of smoking, residual crestal bone height, screw versus press-fit implant design, or the effect of implant surface micromorphology other than machined versus rough surfaces. 9. Insufficient evidence exists to recommend the utilization of platelet-rich plasma in sinus graft surgery. FUTURE DIRECTIONS Further research is needed to determine the effect of residual crestal bone height and smoking on implant survival. Additionally, more data are required to determine the efficacy of bone morphogenetic proteins and bone growth factors on bone formation and implant survival in the maxillary sinus. Controlled trials that limit the variables to the one that is being evaluated are required to properly identify and 339 Effect of Sinus Augmentation on Implant Survival Volume 8 • Number i • December 2003 isolate the effects of what, to date, must be considered multiple confounding variables. ACKNOWLEDGMENTS The authors thank the following co-workers who offered assistance in the preparation of this evidence-based review: Dr. Richard Niederman, Director, Center for Evidence-Based Dentistry. The Forsyth Institute, Boston, Massachusetts for providing initial direction for this evidence-based review; Dr. Dennis P. Tarnow, Professor and Chair, Ashman Department of Implant Dentistry, hew York University College of Dentistry who provided direction and editorial assistance; Mr. Luis J. Gonzalez, Assistant Director, Waldmann Dental Library, Mew York University College of Dentistry for his invaluable assistance with the electronic searches; and Dr. Sang-Choon Cho, Clinical Assistant Professor, Ashman Department of Implant Dentistry, New York University College of Dentistry for his technical assistance with data analysis. REFERENCES 1. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980:38:613-616. 2. Tatum H Jr. Maxillary and sinus implant reconstructions. Dent Clin North Am 1986:30:207-229. 3. Misch CE. Maxillary sinus augmentation for endosteal implants: Organized alternative treatment plans. Int J Oral Implantot 1987:4:49-58. 4. Smiler DG, Holmes RE. Sinus lift procedure using porous hydroxyapatite: A preliminary clinical report. J Oral Imptantot 1987; 13:239-253. 5. Wood RM, Moore DL. Grafting of the maxillary sinus with intraorally harvested autogenous bone prior to implant placement. 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JCatif DentAssoc 1993;21:31-35. 30. Rodriguez A, Anastassov GE, Lee H, Buchbinder D, Wettan H. Maxillary sinus augmentation with deproteinated bovine bone and platelet rich plasma with simultaneous insertion of endosseous implants. J Oral Maxiltofac Surg 2003:61:157-163. 31. Hising P, Bolin A, Branting C. Reconstruction of severely resorbed alveolar crests with dental implants using a bovine bone mineral for augmentation, tnt J Oral Maxiilofac Implants 2001; 16:90-97. 32. Lorenzoni M, Pertl C, Wegscheider W, et al. retrospective analysis of Frialit-2 implants in the augmented sinus. Int J Pcriodontics Restoratiue Dent 2000;20: 255-267. 33. Johansson B, Wannfors K, Ekenback J, Smedberg J-l, Hirsch J. Implants and sinus inlay bone grafts in a 1 -stage procedure on severely atrophied maxillae: Surgical aspects of a 3-year follow-up study. Int. J Oral Maxillofac Implants 1999; 14:81 1-818. 34. Keller EE. Tolman DE, Eckert SE. Maxillary antral-nasal autogenous bone graft reconstruction of the compro mised maxilla: A 12-year retrospective study. IntJOral Maxillofac Implants 1999:14:707-721. 35. Khoury F. Augmentation of the sinus floor with mandibu lar bone block and simultaneous implantation: A 6-year clinical investigation. Int J Oral Maxiltofac Implants 1999;14:557-564. 36. Peleg M, Mazor Z, Garg AK. Augmentation grafting of the maxillary sinus and simultaneous implant placement in patients with 3 to 5 mm of residual alveolar bone height. Int J Oral Maxillofac Implants 1999; 14:549-556. 37. Watzek G, Weber R, Bernhart T, (Jim C, Haas R. Treatment of patients with extreme maxillary atrophy using sinus floor augmentation and implants: Preliminary results. Int JOral Maxillofac Surg 1998:27:428-434. 38. Kaptein MLA, de Putter C, de Lange GL, Blijdorp PA. Survival of cylindrical implants in composite grafted max illary sinuses. J Oral Maxilbfac Surg 1998;56:1376-1380. 39. Fugazotto PA, Vlassis J. Long-term success of sinus augmentation using various surgical approaches and grafting materials. Int J OraI Maxillofac Implants 1998; 13: 52-58. 40. Ellegaard B, Ktflsen-Petersen J, Baelum V. Implant therapy involving maxillary sinus lift in periodontally compromised patients. Clin Oral Impl Res 1997;8:305-315. 41. Block MS, Kent J K Sinus augmentation for dental implants: The use of autogenous bone. J Oral Maxillofac Surg 1997:55:1281-1286. 42. Hurzeler MB, Kirsch A, Ackermann K-L, Quiftones CR. Reconstruction of the severely resorbed maxilla with dental implants in the augmented maxillary sinus: A 5 year clin ical investigation Int J Oral Maxillofac Implants 1996; 11: 466-475. 43. Wheeler SL, Holmes RE, Calhoun CJ. Six-year clinical and histologic study of sinus-lift grafts. Int J Oral Maxiltofac Implants 1996; 11:26-34. 44. Blomqvist JE, Alberius P, Isaksson S. retrospective analysis of one-stage maxillary sinus augmentation with endosseous implants. Int J Oral Maxillofac Implants 1996:1 1:512-521. 45. Small SA, Zinner ID, Panno FV, Shapiro HJ, Stein Jl. Augmenting the maxillary sinus for implants: Report of 27 patients. Int J Oral Maxillofac Implants 1993:8:523-528. 46. Zitzmann MG, Scharer P. Sinus elevation procedures in the resorbed posterior maxilla. Comparison of the crestal and lateral approaches. Oral Surg Oral Med Oral Patriot Oral RadiolEndod 1998:85:8-17. 47. Deporter D, Todescan R. Caudry S. Simplifying manage ment of the posterior maxilla using short, porous-surfaced dental implants and simultaneous indirect sinus elevation Int J Pcriodontics Restorative Dent 2000;20:477-485. 48. Rosen PS, Summers R, Mellado JR, et al. The bone-added osteotome sinus floor elevation technique: Multicenter retrospective report of consecutively treated patients. Int J Oral Maxiltofac Implants 1999; 14:853-858. 49. Coatoam GW, Krieger JT. A four-year study examining the results of indirect sinus augmentation procedures. J Oral Implantol 1997;23:11 7-127. 50. Cavicchia F, Bravi F, Petrelli G. Localized augmentation of the maxillary sinus floor through a coronal approach for the placement of implants, tnt J Periodorttics Restora tive Dent 2001;21:475-485. 51. Bruschi GB, Scipioni A, Calesini G, Bruschi E. Localized management of sinus floor with simultaneous implant placement: A clinical report. Int JOral Maxillofac Implants 1998; 13:219-226. 52. Winter AA, Pollack AS, Odrich RB. Placement of implants in the severely atrophic posterior maxilla using localized management of the sinus floor: A preliminary study. Int J Oral Maxillofac Implants 2002; 17:687 695. 53. Toffler M. Site development in the posterior maxilla using osteocompression and apical alveolar displacement. Compendium Continuing Educ Dent 2001;22:775-790. 54. Fugazzotto PA, De Paoli S. Sinus floor augmentation at the time of maxillary molar extraction: Success and failure rates of 137 implants in function for up to 3 years. J Periodonlol 2002;73:39-44. 55. Lewsey JD, Gilthorpe MS, Gulabivala K. An introduction to meta-analysis within the framework of multilevel modeling using the probability of success of root canal treatment as an illustration. Community Dent Health 2001 ;18: 131-137. 56. 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 -32. 57. Tolman DE. reconstructive procedures with endosseous implants in grafted bone: A review of the literature. Int J Oral Maxiltofac Implants 1995; 10:275-294. 58. Tong DC, Rioux K, Drangsholt M, Beirne OR. A review of the survival rates for implants placed in grafted maxillary sinuses using meta-analysis. Int J Oral Maxillofac Implants 1998; 13:175-182. 59. Del Fabbro M, Testori T, Francetti L, Weinstein R. Metaanalysis of survival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent Accepted for publication 2004. 60. Mevins M, Langer B. The successful application of osseointegrated implants to the posterior jaw: A longterm retrospective study. Int J Oral Maxillofac Implants 1993:8:428-432. 61. Bahat O. Treatment planning and placement of implants in the posterior maxilla: Report of 732 consecutive Nobelpharma implants. Int J Oral Maxillofac Implants 1993:8:151 161. 62. Buser D, Merictke-Stem R, Bernard JP, et al. Long-term evaluation of non-submerged ITI implants. Part 1: 8 year life table analysis of a prospective multi center study with 2359 implants. Clin Oral Impl Res 1997;8: 161-172. 63. Bahat O. Branemark system implants in the posterior maxilla: Clinical study of 660 implants followed for 5 to 12 years. Int J Oral Maxtlto/ac Implants 2000; 15:646-653. 64. Olson JW, Dent CD, Morris HF, Ochi S. Long term assessment (5 to 71 months) of endosseous dental implants placed in the augmented maxillary sinus. Ann 341 Effect of Sinus Augmentation on Implant Survival Volume 8 • Number I • December 2003 Periodontol 2000;5: ] 52-156. 65. Deporter DA, Todescan R, Watson PA, Pharoah M, Pilliar RM, Tomlinson G. A prospective human clinical trial of Endopore dental implants in restoring the partially edentulous maxilla using fixed prostheses. Int J Oral Maxillofac Implants 2001; 16:527-536. 66. Testori T, Wiseman L, Woolfe S, Porter SS. A prospective multicenter clinical study of the Osseotite implant: Four-year interim report. Int J Oral Maxillofac Implants 2001:16:193-200. 67. Testori T, Delayed Fabbro M, Feldman S, et al. A multicenter prospective evaluation of 2-months loaded Osseotite® implants placed in posterior jaws: 3-year follow up results. Clin Oral Impt Res 2002; 11:154-161. 68. Merkx MAW, Maltha JC, Stoelinga PJW. Assessment of the value of anorganic bone additives in sinus floor augmentation: A review of clinical reports. Int J Oral Maxillofac Surg 2003:32:1 -6. 69. Wallace SS, Froum SJ, Tarnow DP. Histologic evaluation of sinus elevation procedure. A clinical report. Int J Periodontics Restoratlue Dent 1996; 16:47-51. 70. Tadjoedtn ES, de Lange GL, Holzmann PJ, Kuiper L, Burger EH. Histological observations on biopsies harvested following sinus floor elevation using a bioactive glass material of narrow size range. Clin Oral Impl Res 2000:11:334-344. 71. Valentini P, Abensur D. Densari D, Graziani JIN, Hammerle CHF. Histological evaluation of Bio-Oss® in a 2-stage sinus floor elevation and implantation procedure. A human case report. Clin Oral Impl Res 1998:9:59-64. 72. Rosenlicht J, Tarnow DP. Human histologic evidence of functionally loaded hydroxyapatite-coated implants placed simultaneously with sinus augmentation: A case report 2 1/2 years post-placement. Int J Oral Implantol 1999;25:7-10. 73. (Jim C, Kneissel M, Schedle A, et al. Characteristic features of trabecuiar bone in edentulous maxillae. Clin Oral Impl Res 1999; 10:459-467. 74. Trisi P, Rao W. Bone classification: clinical-histomorphometric comparison. Clin Oral Impl Res 1999; 10:1-7. 75. Froum SJ, Wallace SS, Tarnow DP, Cho S C. Effect of platelet-rich plasma on bone growth and osseointegration in human maxillary sinus grafts: Three bilateral case reports. Int J Periodonlics Restorative Dent 2002;22: 45-53. 76. Wiltfang J, Schlegel KA, Shultze-Mosgau S, Mkenke E, Zimmerman R, Kessler P. Sinus floor augmentation with [i tricalcium phosphate {(.i-TCP): Does platelet-rich plasma promote its osseous integration and degradation? Ctin Oral Impl Res 2003:14:213-218. 77. Zuffetti F, Testori T, Fontanella W, et al. Use of platelet rich plasma in maxillary sinus lift. Preliminary histological results. Clin Oral Impl Res 2002;13(4):xli (Abst. 10). 78. Maiorana C, Sommariva L, Brivio P, Sigurta D, Santoro F. Maxillary sinus augmentation with anorganic bovine bone (Bio-Oss) and autologous platelet-rich plasma: Preliminary clinical and histologic evaluations. Int J Periodontics Restorative Dent 2003;23:227-235. 79. Sanchez AR, Sheridan PJ, Kupp LI. Is platelet-rich plasma the perfect enhancement factor? A current review. Int J Oral Maxillofac Implants 2003; 18:93 103. Correspondence: Dr. Stephen S. Wallace, 140 Grandview Ave., Waterbury, CT 06708. Fax: 203/573-0773; e-mail: sswdds.sinus@sbcglobal.net. Accepted for publication August 13, 2003. APPENDIX A CONSENSUS REPORT Members of the Section read and studied the review titled "Effect of Maxillary Sinus Augmentation on the Survival of Endosseous Dental Implants. A Systematic Review," by Stephen S. Wallace and Stuart J. Froum. The focused PICO question addressed by this evidence-based systematic review is: "In patients requiring dental implant placement, what is the effect on implant survival of maxillary sinus augmentation versus implant placement in the non-grafted posterior maxilla?" INTRODUCTION This sinus bone augmentation Consensus Report represents a collaborative effort of all Section participants. The primary reviewer presented his data for each of the 5 questions. Section participants then expressed their concerns and suggestions which, in many cases, resulted in modifications to the consensus statements. The process was repeated until final consensus was achieved. It was the consensus of all members of the Section that sufficient evidence was available to make the definitive statements presented in this report. 1. Does the Section agree that the evidence-based systematic review is complete and accurate? Yes. The Section members found that the reviewers were thorough and complete in assimilating a systematic review of evidence-based data for sinus bone augmentation. The following information should be noted. While there was ample evidence to support the lateral wall approach for sinus bone augmentation, the studies on alternative techniques (e.g.. osteotome. localized management of the sinus floor, crestal core elevation) for sinus bone augmentation are limited in number and no conclusions relating to implant survival rate can be drawn at this time. 2. Has any new information been generated or discovered since the evidence-based search cut-off date? Yes, 2 additional publications that provide supportive information have been identified: A recent evidence-based review on the lateral wall approach for sinus bone augmentation by Del Fabbro et al.1 determined an overall implant survival rate that was similar to that found with this review. A recent study found no deleterious effects on voice quality and sinus physiology following sinus bone augmentation procedures.2 3. Does the Section agree with the interpretations and conclusions of the reviewers? The Section participants found the interpretations and conclusions of the reviewers thorough and accurate. 342 Ann Periodontol Wallace, Froum 4. What further research needs to be done relative to the focused questions of the evidence-based review? The following studies were identified by the Section as areas for further research to individually evaluate the success of sinus bone augmentation and the success of implants placed in the augmented sinus. Due to concerns regarding the limited data specifically evaluating the variable of residual crestal bone height, a research project is recommended for evaluating the success rate of implants as it relates specifically to minimal crestal bone height. These studies should ideally use a bilateral sinus model. While no absolute contraindications exist in the literature, it would be beneficial to evaluate implant success as it relates to potential risk factors such as Schneiderian membrane perforations, initial implant stability, postoperative sinus infections, smoking, periodontal disease, sinus pathology, and other systemic and behavioral factors. Studies are warranted to evaluate tissue-engineering techniques (e.g., molecular, cellular, and genetic) that may reduce the time required prior to prosthesis delivery and may enhance bone quality and quantity. These studies ideally should use a bilateral sinus model. Further studies to evaluate the efficacy of alternative sinus bone augmentation techniques are recommended, due to the limited number of studies on these alternative techniques (e.g., osteotorne, localized management of the sinus floor, crestal core elevation). 5. How can the information from the evidence-based review be applied to patient management? A. 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. Level of Evidence:3 Strong. Rationale: Assignment of this level of evidence is based on 3 level I, 4 level 11-1, 11 level 11-2, and 16 level 11-3 studies. These 34 studies included 5,267 implants thus providing a well-founded estimate of the survival rate. B. There is evidence that the following factors, when adjusted for other variables, increase implant survival when performing lateral wall sinus bone augmentation procedures: Membrane coverage (93.6% survival) and no membrane coverage (88.7% survival) of the lateral window. The forest plot (Fig. 1) in the systematic review paper indicates statistical significance (P= 0.019). Level of Evidence: Strong. Rationale: Assignment of this level of evidence is based on 1 level I, 2 level II-1. 8 level 11-2, and 12 level 11-3 studies. Particulate bone grafts (92.3% survival) rather than block grafts (83.3% survival). These percentages (least square means) were adjusted for other variables as determined by meta-regression. Level of Evidence: Moderate. Rationale: Assignment of this level of evidence is based on 3 level I, 4 level II-1, 10 level 11-2, and 12 level 11-3 studies. Rough (94.6% survival) surfaces and machined (90.0% survival) surfaces for the implants. These percentages (least square means) were adjusted for other variables as determined by meta-regression. Level of Evidence: Moderate. Rationale: Assignment of this level of evidence is based on 1 level I, 2 level II-1, 7 level 11-2, and 12 level 11-3 studies. C. There is insufficient evidence to support the use of platelet-rich plasma (PRP) in lateral wall sinus bone augmentation. Level of Evidence: Insufficient. Rationale: Assignment of this level of evidence is based on 1 level 11-3 study, 8 histomorphometric studies, and 1 review. REFERENCES 1. Del Fabbro M, Testori T, Francetti L, Weinstein R. Metaanalysis of survival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent Accepted for publication 2004. 2. Timmenga MM, Raghoebar GM, van Weissenbruch R, Vissink A. Maxillary sinus floor elevation surgery. A clinical, radiographic and endoscopic evaluation. Clin Oral Imp! Res 2003; 14:322-328. 3. Newman MG, Caton, J, Gunsolley JC. The use of the evidence-based approach in a periodontal therapy contemporary science workshop. Ann Periodontol 2003;8: 111. SECTION MEMBERS Myron Mevins, Group Leader Louis F. Rose, Chair Bradley S. McAllister, Secretary Stephen F. Wallace, Reviewer Donald P. Callan Joseph P. Fiorellini Vincent J. lacono Sascha A. Jovanovic Perry Klokkevold Burton Langer Dennis P. Tarnow 343