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Non-grafted versus grafted sinus lift procedures for implantation in the atrophic maxilla: a systematic review and meta-analysis of randomized controlled trials

  • S.A.N. Lie
    Correspondence
    Address: Suen An Nynke Lie, Department of Craniomaxillofacial Surgery, Maastricht University Medical Center MUMC+, P. Debyelaan 25, 6202 AZ, Maastricht, the Netherlands. Tel +31 43 3872010. Fax +13 43 3872020.
    Affiliations
    Department of Craniomaxillofacial Surgery, Maastricht University Medical Center, Maastricht, the Netherlands

    GROW School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, the Netherlands
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  • R.M.M.A. Claessen
    Affiliations
    Department of Craniomaxillofacial Surgery, Maastricht University Medical Center, Maastricht, the Netherlands
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  • C.A.W. Leung
    Affiliations
    Department of Craniomaxillofacial Surgery, Maastricht University Medical Center, Maastricht, the Netherlands
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  • H.-A. Merten
    Affiliations
    Department of Orthodontics, Hannover Medical School, Hannover, Germany
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  • P.A.W.H. Kessler
    Affiliations
    Department of Craniomaxillofacial Surgery, Maastricht University Medical Center, Maastricht, the Netherlands

    GROW School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, the Netherlands
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Open AccessPublished:April 10, 2021DOI:https://doi.org/10.1016/j.ijom.2021.03.016

      Abstract

      The aim of this systematic review and meta-analysis was to critically evaluate the currently existing clinical evidence on the efficacy of graftless maxillary sinus membrane elevation for implantation in the atrophic posterior maxilla. A search protocol without limitations to November 2020 was followed by two independent researchers. Randomized controlled trials using the lateral window approach for graftless sinus membrane elevation were included. Uncontrolled, retrospective, non-comparative studies, case reports, and experimental studies in animals or cadavers were excluded. The search identified 2777 studies. Critical selection by two independent researchers then led to the inclusion of a total of nine studies. A risk of bias assessment was applied using the revised Cochrane risk-of-bias tool for randomized trials. A meta-analysis was conducted for seven studies. Results showed a high overall implant survival rate in both the graftless and bone-grafted sinus lift groups (97.92% and 98.73%, respectively). The graftless sinus lift group showed a significantly lower vertical bone height gain, with a mean difference of −1.73 mm (P = 0.01), and a significantly lower bone density, with a mean difference of −94.7 HU (P < 0.001). The implant stability quotient values did not differ significantly between the test and control groups (P = 0.07).

      Key words

      Dental implants require a certain amount of peri-implant bone. The primary goal in dental implantology must remain the complete and stable integration of an implant in local bone. Treatment of the highly atrophic alveolar ridge is still challenging. To increase local bone volume, lateral and vertical bone augmentation procedures are performed
      • Schultze-Mosgau S.
      • Keweloh M.
      • Wiltfang J.
      • Kessler P.
      • Neukam F.W.
      Histomorphometric and densitometric changes in bone volume and structure after avascular bone grafting in the extremely atrophic maxilla.
      • Rabelo G.D.
      • de Paula P.M.
      • Rocha F.S.
      • Jordão Silva C.
      • Zanetta-Barbosa D.
      Retrospective study of bone grafting procedures before implant placement.
      • Lutz R.
      • Berger-Fink S.
      • Stockmann P.
      • Neukam F.W.
      • Schlegel K.A.
      Sinus floor augmentation with autogenous bone vs. a bovine-derived xenograft—a 5-year retrospective study.
      • Raghoebar G.M.
      • Onclin P.
      • Boven G.C.
      • Vissink A.
      • Meijer H.J.A.
      Long-term effectiveness of maxillary sinus floor augmentation: a systematic review and meta-analysis.
      . Autogenous bone grafts are still regarded as the gold standard for all types of horizontal and vertical bone augmentation
      • Almaiman M.
      • Al-Bargi H.H.
      • Manson P.
      Complication of anterior iliac bone graft harvesting in 372 adult patients from May 2006 to May 2011 and a literature review.
      • Schmitt C.M.
      • Moest T.
      • Lutz R.
      • Neukam F.W.
      • Schlegel K.A.
      Anorganic bovine bone (ABB) vs. autologous bone (AB) plus ABB in maxillary sinus grafting. A prospective non-randomized clinical and histomorphometrical trial.
      . Common intraoral donor regions are, for example, the chin region and the retromolar area
      • Joshi A.
      An investigation of post-operative morbidity following chin graft surgery.
      • Sakkas A.
      • Wilde F.
      • Heufelder M.
      • Winter K.
      • Schramm A.
      Autogenous bone grafts in oral implantology—is it still a “gold standard”? A consecutive review of 279 patients with 456 clinical procedures.
      . Another option is the use of extraoral donor sites, such as the cranium or pelvic bone from the anterior or posterior iliac crest
      • Kessler P.
      • Thorwarth M.
      • Bloch-Birkholz A.
      • Nkenke E.
      • Neukam F.W.
      Harvesting of bone from the iliac crest—comparison of the anterior and posterior sites.
      • Kuik K.
      • Putters T.F.
      • Schortinghuis J.
      • van Minnen B.
      • Vissink A.
      • Raghoebar G.M.
      Donor site morbidity of anterior iliac crest and calvarium bone grafts: a comparative case–control study.
      .
      The osteogenic properties of autogenous bone grafts make these superior to bone substitute materials
      • Schmitt C.M.
      • Moest T.
      • Lutz R.
      • Neukam F.W.
      • Schlegel K.A.
      Anorganic bovine bone (ABB) vs. autologous bone (AB) plus ABB in maxillary sinus grafting. A prospective non-randomized clinical and histomorphometrical trial.
      • Nkenke E.
      • Neukam F.W.
      Autogenous bone harvesting and grafting in advanced jaw resorption: morbidity, resorption and implant survival.
      . However, when using autogenous transplants, there are drawbacks such as unavoidable donor morbidity and the limited availability of bone volume, especially from intraoral donor sites, and also the additional costs
      • Nkenke E.
      • Radespiel-Tröger M.
      • Wiltfang J.
      • Schultze-Mosgau S.
      • Winkler G.
      • Neukam F.W.
      Morbidity of harvesting of retromolar bone grafts: a prospective study.
      • Nkenke E.
      • Schultze-Mosgau S.
      • Radespiel-Tröger M.
      • Kloss F.
      • Neukam F.W.
      Morbidity of harvesting of chin grafts: a prospective study.
      • Raghoebar G.M.
      • Meijndert L.
      • Kalk W.W.
      • Vissink A.
      Morbidity of mandibular bone harvesting: a comparative study.
      .
      Bone substitutes are used as an alternative to avoid the use of autogenous bone
      • Al-Nawas B.
      • Schiegnitz E.
      Augmentation procedures using bone substitute materials or autogenous bone—a systematic review and meta-analysis.
      . These materials are a valid alternative and are often used in combination with membranes, in the sense of guided bone regeneration
      • Lutz R.
      • Berger-Fink S.
      • Stockmann P.
      • Neukam F.W.
      • Schlegel K.A.
      Sinus floor augmentation with autogenous bone vs. a bovine-derived xenograft—a 5-year retrospective study.
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      .
      Most augmentation procedures in the atrophic posterior maxilla are combined with elevation of the maxillary sinus membrane. The basal lining of the sinus membrane cannot be considered as pure periosteum, nevertheless numerous studies have shown new bone formation underneath the sinus membrane after elevation without the use of any bone grafts
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Cricchio G.
      • Sennerby L.
      • Lundgren S.
      Sinus bone formation and implant survival after sinus membrane elevation and implant placement: a 1- to 6-year follow-up study.
      • Lie N.
      • Merten H.A.
      • Yamauchi K.
      • Wiltfang J.
      • Kessler P.
      Pre-implantological bone formation in the floor of the maxillary sinus in a self-supporting space.
      • Lundgren S.
      • Cricchio G.
      • Palma V.C.
      • Salata L.A.
      • Sennerby L.
      Sinus membrane elevation and simultaneous insertion of dental implants: a new surgical technique in maxillary sinus floor augmentation.
      .
      The lateral window technique to approach the maxillary sinus for increasing bone volume in the posterior maxilla is a well-established and documented surgical procedure allowing for simultaneous or staged dental implant placement
      • Raghoebar G.M.
      • Onclin P.
      • Boven G.C.
      • Vissink A.
      • Meijer H.J.A.
      Long-term effectiveness of maxillary sinus floor augmentation: a systematic review and meta-analysis.
      • Boyne P.J.
      • James R.A.
      Grafting of the maxillary sinus floor with autogenous marrow and bone.
      • Summers R.B.
      A new concept in maxillary implant surgery: the osteotome technique.
      • Tatum Jr, O.H.
      • Lebowitz M.S.
      • Tatum C.A.
      • Borgner R.A.
      Sinus augmentation. Rationale, development, long-term results.
      • Zitzmann N.U.
      • Scharer P.
      Sinus elevation procedures in the resorbed posterior maxilla. Comparison of the crestal and lateral approaches.
      . Graftless sinus membrane elevation for later implant placement avoids donor site morbidity after harvesting autogenous bone and prevents the use of any kind of bone replacement material. This would mean less discomfort for the patient with regard to sinus floor augmentation
      • Kessler P.
      • Thorwarth M.
      • Bloch-Birkholz A.
      • Nkenke E.
      • Neukam F.W.
      Harvesting of bone from the iliac crest—comparison of the anterior and posterior sites.
      • Kuik K.
      • Putters T.F.
      • Schortinghuis J.
      • van Minnen B.
      • Vissink A.
      • Raghoebar G.M.
      Donor site morbidity of anterior iliac crest and calvarium bone grafts: a comparative case–control study.
      • Nkenke E.
      • Radespiel-Tröger M.
      • Wiltfang J.
      • Schultze-Mosgau S.
      • Winkler G.
      • Neukam F.W.
      Morbidity of harvesting of retromolar bone grafts: a prospective study.
      • Nkenke E.
      • Schultze-Mosgau S.
      • Radespiel-Tröger M.
      • Kloss F.
      • Neukam F.W.
      Morbidity of harvesting of chin grafts: a prospective study.
      • Raghoebar G.M.
      • Meijndert L.
      • Kalk W.W.
      • Vissink A.
      Morbidity of mandibular bone harvesting: a comparative study.
      .
      According to earlier systematic reviews that have described the graftless sinus lift, this procedure leads to a high implant survival in the atrophic maxilla
      • Dongo V.
      • von Krockow N.
      • Martins-Filho P.R.S.
      • Weigl P.
      Lateral sinus floor elevation without grafting materials. Individual- and aggregate-data meta-analysis.
      • Moraschini V.
      • Uzeda M.G.
      • Sartoretto S.C.
      • Calasans-Maia M.D.
      Maxillary sinus floor elevation with simultaneous implant placement without grafting materials: a systematic review and meta-analysis.
      • Parra M.
      • Olate S.
      • Cantín M.
      Clinical and biological analysis in graftless maxillary sinus lift.
      • Silva L.D.
      • de Lima V.N.
      • Faverani L.P.
      • de Mendonça M.R.
      • Okamoto R.
      • Pellizzer E.P.
      Maxillary sinus lift surgery—with or without graft material? A systematic review.
      • Yang J.
      • Xia T.
      • Wang H.
      • Cheng Z.
      • Shi B.
      Outcomes of maxillary sinus floor augmentation without grafts in atrophic maxilla: a systematic review and meta-analysis based on randomised controlled trials.
      • Duan D.H.
      • Fu J.H.
      • Qi W.
      • Du Y.
      • Pan J.
      • Wang H.L.
      Graft-free maxillary sinus floor elevation: a systematic review and meta-analysis.
      . However, no systematic review has been performed that has included only prospective randomized controlled trials (RCTs) using the lateral window technique for graftless sinus floor augmentation.
      The aim of this systematic review was to critically evaluate the currently existing clinical evidence on the efficacy of graftless maxillary sinus membrane elevation using the lateral window approach for implantation in the atrophic maxilla.

      Materials and methods

      This systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) statement for reporting systematic reviews
      • Moher D.
      • Liberati A.
      • Tetzlaff J.
      • Altman D.G.
      • PRISMA Group
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      . The focused questions were (1) Is the de novo bone formation in graftless maxillary sinus membrane elevation comparable to that in sinus floor augmentation with the use of bone grafts? (2) Is implant survival in the graftless sinus lift comparable to that in the sinus lift with the use of bone grafts?

      Search strategy

      A search of the MEDLINE (PubMed), Cochrane Library, and Embase (Elsevier) databases was performed, as well as a recent journal review. The search terms were “sinus membrane elevation” OR “sinus floor augmentation” OR “maxillary sinus lift” OR “sinus floor augmentation”[MeSH Terms]. No search limitations were applied.
      The end date of the search period was November 1, 2020. An additional hand-search and grey literature search was performed.

      Study selection and data extraction

      The PICOS guidelines (population, intervention, comparison, outcomes, and study type) were followed to define the eligible studies. The population (P) consisted of patients with maxillary atrophy in need of sinus floor augmentation for immediate or staged implant placement. The intervention (I) was tenting of the maxillary sinus membrane without the use of any bone substitutes. The comparison (C) was sinus floor augmentation using bone grafts. Eligible outcomes (O) were implant survival, bone height gain, and bone density measured on radiographic images, implant stability, and histology. The study design (S) was prospective RCTs with an observation period of at least 6 months.
      A minimum number of five comparative sinuses in the included studies was accepted. Staged and simultaneous implantation were both included, as long as a tenting technique of the sinus membrane was performed and the sinus was approached using the lateral window technique.
      Studies using the osteotome technique or growth factors, case reports, retrospective studies, non-comparative studies, technical notes, animal studies, cadaver studies, and reviews were excluded.
      Two reviewers (SL, CL) contributed to the elaboration of the systematic review through research, reading, critical article selection, and data extraction. All references were transferred to and screened using Rayyan (Rayyan, Qatar Computing Research Institute, Qatar Foundation)
      • Ouzzani M.
      • Hammady H.
      • Fedorowicz Z.
      • Elmagarmid A.
      Rayyan—a web and mobile app for systematic reviews.
      . After screening the titles and abstracts, potential studies were selected. A critical selection was made after reading the full texts of potential studies according to the inclusion and exclusion criteria. In the case of disagreement, a group discussion was held with a third reviewer (PK), and a decision was made regarding whether or not the article was selected. A meta-analysis of the included studies was performed.
      Data information that was extracted by the reviewers included the year of publication, study design, number of patients, tenting technique, grafts used in the control group, immediate or two-stage implantation, number of implants placed, duration of follow-up, partially dentate or completely edentulous patients, residual bone height, outcome methods, implant survival, vertical bone height gain, bone density, implant stability quotient (ISQ), other outcomes used, and complications.

      Risk of bias assessment

      The risk of bias was assessed independently by the two researchers (SL, CL) according to the revised Cochrane risk-of-bias tool for randomized trials (RoB 2)
      • Higgins J.P.T.
      • Thomas J.
      • Chandler J.
      • Cumpston M.
      • Li T.
      • Page M.J.
      • Welch V.A.
      Cochrane handbook for systematic reviews of interventions version 6.0 (updated July 2019).
      • Sterne J.A.C.
      • Savović J.
      • Page M.J.
      • Elbers R.G.
      • Blencowe N.S.
      • Boutron I.
      • Cates C.J.
      • Cheng H.Y.
      • Corbett M.S.
      • Eldridge S.M.
      • Emberson J.R.
      • Hernán M.A.
      • Hopewell S.
      • Hróbjartsson A.
      • Junqueira D.R.
      • Jüni P.
      • Kirkham J.J.
      • Lasserson T.
      • Li T.
      • McAleenan A.
      • Reeves B.C.
      • Shepperd S.
      • Shrier I.
      • Stewart L.A.
      • Tilling K.
      • White I.R.
      • Whiting P.F.
      • Higgins J.P.T.
      RoB 2: a revised tool for assessing risk of bias in randomised trials.
      . The tool classifies five domains: bias arising from the randomization process, bias due to deviations from the intended interventions, bias due to missing outcome data, bias in measurement of the outcome, bias in selection of the reported result. The Excel tool to implement RoB 2 was used for this assessment.

      Statistical analysis

      The mean and standard deviation (SD) values of vertical bone height gain, bone density, ISQ, and implant survival were extracted from the included studies. If the mean or SD values were not reported in the article, these were calculated from the available data. For continuous data, the inverse variance method was used. The Mantel–Haenszel method was used for dichotomous data. Study heterogeneity was assessed using the DerSimonian and Laird method and I-square index. I2 values were interpreted as follows: 0–40% might not be important, 40–60% indicates moderate heterogeneity, 60–80% indicates substantial heterogeneity, and 80–100% may represent considerable heterogeneity
      • Higgins J.P.T.
      • Thomas J.
      • Chandler J.
      • Cumpston M.
      • Li T.
      • Page M.J.
      • Welch V.A.
      Cochrane handbook for systematic reviews of interventions version 6.0 (updated July 2019).
      . If moderate, substantial, or considerable heterogeneity was found, the random-effects model was chosen in order to minimize any bias caused by methodological differences among studies. The fixed-effects method was chosen when there was no evidence of heterogeneity. In the meta-analysis, outcomes were expressed as the weighted mean difference (WMD) with the 95% confidence interval (CI). The level of significance was set at a P-value of <0.05. Forest plots were generated to graphically represent the difference in outcomes for all included studies. Extracted data were analysed using IBM SPSS Statistics for Windows, version 26 (IBM Corp., Armonk, NY, USA). Publication bias was assessed via a funnel plot.

      Results

      Study selection and characteristics of the studies

      The search strategy identified 2777 studies after de-duplication. There were 44 articles potentially relevant for inclusion. After full-text reading and critical selection, nine articles were eventually included in this review (Fig. 1)
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      ; seven articles were eligible for meta-analysis
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . A total of 160 patients were included in these selected studies. The tenting technique without the use of any bone graft was performed in 112 maxillary sinuses and this was compared to sinus floor augmentation with autografts, allografts, xenografts, alloplasts, or a mixture of these bone substitutes in 104 maxillary sinuses. A total of 426 implants were placed. The characteristics of the articles are described in Table 1.
      Fig. 1
      Fig. 1PRISMA flow diagram of the study selection process.
      Table 1Articles included for review: characteristics.
      First author YearStudy designPatients (n)Test group (n)Control group (n)Graftless side: tenting techniqueGraft sideImplant placementImplants test (n)Implants control (n)Follow-up (months)Patients included: partial/fully edentulousResidual bone height (mm)
      Altintas 2013
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      RCT141010ImplantAllograftImmediate12126Both4–6
      Borges 2011
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      RCT, split-mouth151515ImplantAutograftImmediate28266Both5.89 (test)
      5.34 (control)
      Felice 2009
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      RCT, split-mouth101010Resorbable barrier (Inion)XenograftAfter 6 months24 (−3)245 (after loading)Partial3.4 (test)
      2.8 (control)
      Fouad 2018
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      RCT171010ImplantXenograftImmediate17176Partial4–6
      Johansson 2013
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      Randomized, three groups2410/1010Implant (with bone window replacement/ collagen membrane)AutograftImmediate101 (total) ∼101/3×2=67.3*101 (total) ∼101/3=33.6***7Partial4.3 (test)
      3.5 (test)
      4.3 (control)
      Khaled 2019
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      RCT191010ImplantAlloplastImmediate13126Partial4–6
      Lie 2015
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      RCT, split-mouth555Resorbable membrane (PDLLA)Mixture of autograft and xenograftAfter 6 months15156 (post-loading)FullyND
      Ranaan 2018
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      RCT331820Bovine pericardium membrane + implantAllograftImmediate36406, 8 and 24Partial5.48
      4.69
      Scarano 2018
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      RCT231414Heterologous cortical laminaXenograftAfter 6 months34 (both groups) ∼34/2=17**34 (both groups) ∼34/2=17**6Both2–3
      Total = 9160112104GraftlessAutografts, allografts, xenografts, alloplasts229 (−3) (145+67.3*+17**)197 (146+33.6***+17**)
      ND, not determined; PDLLA, poly(d,l-lactic acid); RCT, randomized controlled trial.
      Different tenting techniques were used: in some studies, implants were used as a space holder to keep the sinus membrane elevated
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      ; in other studies, a resorbable material was used to keep the membrane lifted
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      . The three studies that did not use an implant as a space holder planned a two-stage procedure, where implants were placed 6 months after the sinus floor augmentation. These three studies took the opportunity to take bone biopsies immediately before placing the implants with a small trephine drill for histological research. One study even retrieved implants 6 months after placing them, to analyse bone-to-implant contact
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      .
      Table 2 describes the outcome methods and results of the nine selected studies.
      Table 2Articles included for review: outcomes.
      First authorOutcome methodImplant survival (test/control) (%)Bone height gain (mm) test/controlBone density (test/control)ISQ (test/control)Other outcomeComplications (test/control)
      Altintas
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      CBCT100/100ND254.91/16.25 (P < 0.05)NDNew bone around apices of implants (test: 0/12, control: 3/12)No complications observed
      Borges
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      CBCT, ISQ96.4/1007.91/8.31 (P > 0.05)194.42/207 (P > 0.05)51/50 (P > 0.05)Bone around implants (similar results test/control)2 sinus mucosal perforations <2 mm (1/1)
      2 postoperative wound infections (1/1)
      4 incomplete closing of lateral window (3/1)
      1 implant no osseointegration (1/0)
      Felice
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      CT, histomorphometry100/10014.4/14.1 (NS)NDNDNew bone formation on histology (test: 24.2%, control: 36.1%; P = 0.002)3 rupture of sinus membrane (2/1)
      1 window filled with fibrotic tissue → Bio-Oss was placed (1/0)
      Fouad
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      CBCT, ISQ1004.85/8.59 (P < 0.05)269.08/375.59 (P < 0.05)74/78.3 (P < 0.05)ND2 membrane perforations (2/0)
      Johansson
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      CBCT, retrieved implants3 groups (test/test/control)NDNDNDRetrieved implants, BIC (test 1: 93.5%, test 2: 92.0%, control: 93.5%)1 implant no osseointegration (1/0)
      1 failure/100/100Apico-buccal/lingual distances (test 1: 0.6/1.2, test 2: 0.5/0.8, control: 0.6/0.8)3 not completely ossified walls (3/0)
      No significant results
      Khaled
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      CT, ISQ1005.0/7.0 (P = 0.002)420/548 (P < 0.001)77/78 (P = 0.901)ND3 small membrane perforations (2/1)
      Lie
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      CBCT, histology100/1007.78/9.99 (NS)NDNDDetailed description of histology: new bone formation, less organized and immature on test sideND
      Patient satisfaction: 100% both sides
      Ranaan
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      CBCT, ISQ94.4/9512.82/14.36 (P = 0.002)ND78.95/81.45 (P = 0.108)Two different implants9 membrane perforations <2 mm (4/5)
      1 histological biopsy (test): new bone formation4 lost implants (2/2)
      Bone height after 24 months less than after 6 months
      Scarano
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      CBCT, histologyNDNDNDNDGraft volume (mm3) immediately postop., 6 months postop. (test: 2801, 1912.1; control: 3101, 2716)3 membrane perforations (2/1)
      Histology: newly formed bone (test: 27%, control: 34%)
      BIC, bone-to-implant contact; CBCT, cone beam computed tomography; CT, computed tomography; ISQ, implant stability quotient; ND, not determined; NS, no significance.

      Risk of bias assessment

      The risk of bias assessment is summarized in Fig. 2, Fig. 3. Six articles were assessed as being at low risk of bias
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . Three articles had some concerns in the risk of bias assessment
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      . None of the three described whether the randomized allocation was blinded until the day of the intervention. One article described the loss of an implant
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      . However, this implant was not included in the results. No study was determined to show a high risk of bias.
      Fig. 3
      Fig. 3Risk of bias summary: 33.3% of the studies had some concerns regarding risk of bias and 66.7% of the studies had a low risk.

      Data synthesis and meta-analysis

      Implant survival

      Of the nine selected articles, seven could be analysed with regard to implant survival
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . One study included two different test groups and a control group
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      . One implant was lost in the first test group. The exact number of implants in each group was not described. Scarano et al.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      did not mention implant survival for the 34 implants placed in the test and control groups.
      The seven articles in Fig. 4 show high overall implant survival in the test group and control group: the weighted overall survival was 97.92% and 98.73%, respectively. There was no evidence of heterogeneity (P =  1.00, I2 = 0%). The fixed-effects model was used in the meta-analysis. There was no statistically significant difference between the test and control groups, with a risk ratio (RR) of 0.99 (95% CI 0.79–1.25, P = 0.94) (Fig. 4).
      Fig. 4
      Fig. 4Forest plot comparing implant survival in the non-grafted and grafted groups.

      Bone gain on radiographic images

      Six articles described the vertical bone height gain measured on computed tomography (CT) images or cone beam computed tomography (CBCT) images
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . Due to evidence of heterogeneity (I
      • Rabelo G.D.
      • de Paula P.M.
      • Rocha F.S.
      • Jordão Silva C.
      • Zanetta-Barbosa D.
      Retrospective study of bone grafting procedures before implant placement.
       = 83.54%, P = 0.27), the random-effects model was applied in the meta-analysis. The analysis showed a significant difference (P = 0.01), with less vertical bone height gain in the graftless group: mean difference −1.73 mm (95% CI −3.04 to −0.41 mm) (Fig. 5).
      Fig. 5
      Fig. 5Forest plot comparing vertical bone height gain in the non-grafted and grafted groups.
      Four studies analysed new bone formation around the implants on CT, but no significant difference was found between the two sides
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      .
      Scarano et al.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      described the graft volume immediately postoperative after elevation of the sinus membrane and at 6 months postoperative. The graft volume was less on the test side at both time points (see Table 2).

      Bone density

      Four articles compared bone density
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      . Meta-analysis was applied using the random-effects model, because of substantial heterogeneity (I2 = 62.86%, P < 0.001). Bone density was significantly higher on the grafted side, with a mean difference of −94.7 Hounsfield units (HU) (95% CI −134.9 to −54.5 HU) (P < 0.001) (Fig. 6).
      Fig. 6
      Fig. 6Forest plot comparing bone density in the non-grafted and grafted groups.

      Implant stability

      Implant stability was measured 6 months after implantation in four studies
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . Only one study found a significant difference in favour of the grafted side
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      . Due to the substantial heterogeneity (I2 = 61.48%, P=0.60 0.00), the meta-analysis was applied using the random-effects model. No significant difference was found in the mean ISQ between the non-grafted and grafted sides, respectively 72.56 and 74.68 (−2.12, 95% CI −4.40 to 0.15, P = 0.07) (Fig. 7).
      Fig. 7
      Fig. 7Forest plot comparing implant stability in the non-grafted and grafted groups.

      Histology

      Histology showed 24% versus 36% of new bone formation in the bone cylinders on the test and the control sides, respectively, in the study by Felice et al.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      . Scarano et al.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      found comparable results, with new bone formation of 27% and 34%, respectively. The implants removed from the study of Johansson et al. showed no significant differences between the test and control groups
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      . Lie et al.
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      described new bone formation and remodelling with the presence of osteoblasts and osteoclasts in both groups. However, the test side showed less organized bone, which was of immature quality. Ranaan et al. retrieved one implant for histological analysis to prove new bone formation on the test side
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      .

      Publication bias

      A funnel plot was drawn of the studies that compared bone height gain (Fig. 8). One study (37) is found to be outside the funnel plot. Another study (16) shows a deviation of the standard error (SE) from the overall result
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      ; this asymmetry may indicate publication bias.
      Fig. 8
      Fig. 8Funnel plot assessing potential publication bias for studies reporting vertical bone height gain (SE, standard error; SMD, standard mean difference).

      Discussion

      Osseointegration of implants is essential to provide stability and long-term success. The presence of bone is mandatory to achieve reliable osseointegration. Sufficient residual bone or new bone formed by sinus membrane elevation has a positive influence on implant survival
      • Park W.B.
      • Kang K.L.
      • Han J.Y.
      Factors influencing long-term survival rates of implants placed simultaneously with lateral maxillary sinus floor augmentation: a 6- to 20-year retrospective study.
      • Pjetursson B.E.
      • Tan W.C.
      • Zwahlen M.
      • Lang N.P.
      A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation.
      .
      Tenting of the sinus membrane by simultaneous implant placement without grafting material can only be successful if the remaining alveolar height guarantees primary implant stability
      • Lundgren S.
      • Cricchio G.
      • Palma V.C.
      • Salata L.A.
      • Sennerby L.
      Sinus membrane elevation and simultaneous insertion of dental implants: a new surgical technique in maxillary sinus floor augmentation.
      • Cricchio G.
      • Palma V.C.
      • Faria P.E.
      • de Olivera J.A.
      • Lundgren S.
      • Sennerby L.
      • Salata L.A.
      Histological outcomes on the development of new space-making devices for maxillary sinus floor augmentation.
      • Thor A.
      • Wannfors K.
      • Sennerby L.
      • Rasmusson L.
      Reconstruction of the severely resorbed maxilla with autogenous bone, platelet-rich plasma, and implants: 1-year results of a controlled prospective 5-year study.
      .
      In the posterior maxilla, the vertical distance between the floor of the maxillary sinus and the crest of the posterior maxillary alveolar process constitutes the subantral bone height. This bone height is often used to determine whether implants can be placed simultaneously with sinus floor elevation in a one-step procedure or whether a staged approach should be preferred
      • Stefanski S.
      • Svensson B.
      • Thor A.
      Implant survival following sinus membrane elevation without grafting and immediate implant installation with a one-stage technique: an up-to-40-month evaluation.
      . According to the literature, a minimal remaining alveolar crest height of about 3 mm must be present for sufficient primary implant stability
      • Thor A.
      • Wannfors K.
      • Sennerby L.
      • Rasmusson L.
      Reconstruction of the severely resorbed maxilla with autogenous bone, platelet-rich plasma, and implants: 1-year results of a controlled prospective 5-year study.
      . Primary implant stability, however, can only be reached in combination with an adequate preparation of the implant socket using an undersized drilling technique and implant type, for example.
      Many studies have already proven that bone growth can be induced in the floor of the maxillary sinus by membrane elevation even without augmentation
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Cricchio G.
      • Sennerby L.
      • Lundgren S.
      Sinus bone formation and implant survival after sinus membrane elevation and implant placement: a 1- to 6-year follow-up study.
      • Lie N.
      • Merten H.A.
      • Yamauchi K.
      • Wiltfang J.
      • Kessler P.
      Pre-implantological bone formation in the floor of the maxillary sinus in a self-supporting space.
      • Duan D.H.
      • Fu J.H.
      • Qi W.
      • Du Y.
      • Pan J.
      • Wang H.L.
      Graft-free maxillary sinus floor elevation: a systematic review and meta-analysis.
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      • Lundgren S.
      • Andersson S.
      • Gualini F.
      • Sennerby L.
      Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation.
      ,
      • Lundgren S.
      • Andersson S.
      • Sennerby L.
      Spontaneous bone formation in the maxillary sinus after removal of a cyst: coincidence or consequence?.
      . As the bone-forming capacity of the sinus membrane remains unclear according to the literature, bone forming in an artificially created space under the sinus membrane must be based on a physiological process similar to callus formation in secondary bone healing or distraction osteogenesis
      • Kessler P.
      • Bumiller L.
      • Schlegel A.
      • Birkholz T.
      • Neukam F.W.
      • Wiltfang J.
      Dynamic periosteal elevation.
      . This is the most probable theory, as the vast majority of the literature dealing with this topic reports reliable new bone formation in animal, as well as human studies
      • Lie N.
      • Merten H.A.
      • Yamauchi K.
      • Wiltfang J.
      • Kessler P.
      Pre-implantological bone formation in the floor of the maxillary sinus in a self-supporting space.
      • Cricchio G.
      • Palma V.C.
      • Faria P.E.
      • de Olivera J.A.
      • Lundgren S.
      • Sennerby L.
      • Salata L.A.
      Histological outcomes on the development of new space-making devices for maxillary sinus floor augmentation.
      . This would mean that the elevation of the sinus membrane is a prerequisite for the formation of a stable blood clot, which ossifies secondarily. The membrane itself is reduced to the function of a barrier whose own questionable osteogenic potential may not be necessary at all.
      Different techniques for the graftless sinus floor elevation have been applied: the sinus can be approached from the lateral window
      • Raghoebar G.M.
      • Onclin P.
      • Boven G.C.
      • Vissink A.
      • Meijer H.J.A.
      Long-term effectiveness of maxillary sinus floor augmentation: a systematic review and meta-analysis.
      • Boyne P.J.
      • James R.A.
      Grafting of the maxillary sinus floor with autogenous marrow and bone.
      • Tatum Jr, O.H.
      • Lebowitz M.S.
      • Tatum C.A.
      • Borgner R.A.
      Sinus augmentation. Rationale, development, long-term results.
      , and another reliable option is the transalveolar approach to the sinus
      • Summers R.B.
      A new concept in maxillary implant surgery: the osteotome technique.
      • Tatum Jr, H.
      Maxillary and sinus implant reconstructions.
      . Studies that used osteotome techniques were excluded from this systematic review, since this technique is associated with different outcomes. Since the residual bone is carefully moved upwards, the biology of new bone formation is different from sinus membrane elevation through the lateral window. The space created by tenting in the lateral window approach is bigger than in the transalveolar approach.
      Recent systematic reviews have assessed studies on the graftless sinus lift
      • Dongo V.
      • von Krockow N.
      • Martins-Filho P.R.S.
      • Weigl P.
      Lateral sinus floor elevation without grafting materials. Individual- and aggregate-data meta-analysis.
      • Moraschini V.
      • Uzeda M.G.
      • Sartoretto S.C.
      • Calasans-Maia M.D.
      Maxillary sinus floor elevation with simultaneous implant placement without grafting materials: a systematic review and meta-analysis.
      • Parra M.
      • Olate S.
      • Cantín M.
      Clinical and biological analysis in graftless maxillary sinus lift.
      • Silva L.D.
      • de Lima V.N.
      • Faverani L.P.
      • de Mendonça M.R.
      • Okamoto R.
      • Pellizzer E.P.
      Maxillary sinus lift surgery—with or without graft material? A systematic review.
      • Yang J.
      • Xia T.
      • Wang H.
      • Cheng Z.
      • Shi B.
      Outcomes of maxillary sinus floor augmentation without grafts in atrophic maxilla: a systematic review and meta-analysis based on randomised controlled trials.
      • Duan D.H.
      • Fu J.H.
      • Qi W.
      • Du Y.
      • Pan J.
      • Wang H.L.
      Graft-free maxillary sinus floor elevation: a systematic review and meta-analysis.
      . However, no review has included prospective RCTs only in humans that have compared de novo bone formation in non-grafted sinus membrane elevation with sinus floor augmentation with bone substitutes using the lateral window approach.
      This systematic review shows a high survival rate for dental implants both after conventional augmentation of the posterior maxillary sinus floor with autogenous bone and bone replacement material and without augmentation material: 98.73% and 97.92%, respectively. There was no significant difference (P = 0.94) between the groups that were compared. Thus, it can be concluded that sinus membrane elevation without the use of bone grafts leads to a reliable and stable bone situation for implantation. It should be noted that the follow-up of implant survival was limited to only 6 months. A longer follow-up is needed to assess long-term stability, not only with regard to the implants, but also regarding the stability of the newly gained bone.
      Most studies showed more bone gain on the bone grafted side than on the graftless side. Three studies found significant differences
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . Felice et al.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      found no significant difference in bone height gain, with a slightly higher bone gain in the test group (P = 0.672).
      Of the four studies that compared bone density, only one showed a significantly higher bone density measured in HU on the graftless side
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      . The other three studies showed a lower bone density on the graftless side
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      .
      The meta-analysis of the radiological results at 6 months after sinus floor elevation showed that the gain in bone height (−1.73 mm, 95% CI − 3.04 to −0.41 mm, P = 0.01) and the bone density (−94.7 HU, 95% CI −134.9 to −54.5 HU, P < 0.001) were significantly lower in the non-grafted sinus lift group than in the bone grafting group. It should be noted that some studies used multi-slice CT and others used CBCT, which leads to bias. Multi-slice CT shows more scattering around implants and CBCT is less accurate, but is an optimal tool for imaging the oral and maxillofacial area and gives less radiation to the patient. The significant differences can be explained by the fact that it takes time for new bone to arise from the blood clot on the graftless side when compared to the bone substitutes, which already possess bone-like properties and immediately show opacity on a radiograph. It is histologically proven that the newly formed bone on the non-grafted side is less calcified and shows fewer fibrous cells. Nevertheless, the transplant-free bony drill cores in the study of Lie et al.
      • Lie N.
      • Merten H.A.
      • Yamauchi K.
      • Wiltfang J.
      • Kessler P.
      Pre-implantological bone formation in the floor of the maxillary sinus in a self-supporting space.
      showed intensive new bone formation.
      The meta-analysis of implant stability showed no significant difference between the non-grafted and grafted groups at 6 months after implant placement (−2.12, 95% CI − 4.40 to 0.15, P = 0.07). Both groups show a mean ISQ value above 60 (non grafted: 72.56, grafted: 74.68). If the ISQ is higher than 60, this is considered favourable for a high implant survival rate
      • Rodrigo D.
      • Aracil L.
      • Martin C.
      • Sanz M.
      Diagnosis of implant stability and its impact on implant survival: a prospective case series study.
      . This means that the ISQ values after non-grafted and grafted sinus lifts are sufficient.
      From this literature review it can be concluded that the nature of the newly formed callus-like bone with lower radiological density and opacity does not allow a prediction of higher implant failure. Despite the bone gain and bone density being significantly lower on the graftless side, this has no effect on implant survival or implant stability.
      Although this systematic review and meta-analysis included only prospective RCTs without a high risk of bias and only one surgical approach technique to the sinus was accepted, it is still subject to some limitations. The studies included are not completely homogeneous: three studies performed a two-stage procedure
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      • Scarano A.
      • de Oliveira P.S.
      • Traini T.
      • Lorusso F.
      Sinus membrane elevation with heterologous cortical lamina: a randomized study of a new surgical technique for maxillary sinus floor augmentation without bone graft.
      , whereas six studies described simultaneous implantation
      • Altintas N.Y.
      • Senel F.C.
      • Kayıpmaz S.
      • Taskesen F.
      • Pampu A.A.
      Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting.
      • Borges F.L.
      • Dias R.O.
      • Piattelli A.
      • Onuma T.
      • Gouveia Cardoso L.A.
      • Salomão M.
      • Scarano A.
      • Ayub E.
      • Shibli J.A.
      Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      • Johansson L.A.
      • Isaksson S.
      • Bryington M.
      • Dahlin C.
      Evaluation of bone regeneration after three different lateral sinus elevation procedures using micro-computed tomography of retrieved experimental implants and surrounding bone: a clinical, prospective, and randomized study.
      • Khaled H.
      • Atef M.
      • Hakam M.
      Maxillary sinus floor elevation using hydroxyapatite nano particles vs tenting technique with simultaneous implant placement: a randomized clinical trial.
      • Ranaan J.
      • Bassir S.H.
      • Andrada L.
      • Shamshiri A.R.
      • Maksoud M.
      • Raanan R.
      • Guze K.
      Clinical efficacy of the graft free slit-window sinus floor elevation procedure: A 2-year randomized controlled clinical trial.
      . The implants were used for the tenting technique of the sinus membrane. In the single-stage procedure with tenting by implants, new bone formation and osseointegration of the implants take place in the same period as after previous or graftless augmentation, which leads to a significantly shorter overall treatment time. In the two-stage procedure, the tenting technique is a pre-implant surgical procedure and the implants are placed 6 months later. The idea is to first allow bony consolidation to take place so that implants can be placed in sufficient and good quality bone substance. No significant difference between one- and two-stage implantation with regard to implant survival has been described in the literature
      • Raghoebar G.M.
      • Onclin P.
      • Boven G.C.
      • Vissink A.
      • Meijer H.J.A.
      Long-term effectiveness of maxillary sinus floor augmentation: a systematic review and meta-analysis.
      • Felice P.
      • Pistilli R.
      • Piattelli M.
      • Soardi E.
      • Barausse C.
      • Esposito M.
      1-stage versus 2-stage lateral sinus lift procedures: 1-year post-loading results of a multicentre randomised controlled trial.
      . It would be interesting to study the differences in outcome of the two techniques using elevation of the sinus membrane without augmentation materials. Felice et al.
      • Felice P.
      • Scarano A.
      • Pistilli R.
      • Checchi L.
      • Piattelli M.
      • Pellegrino G.
      • Esposito M.
      A comparison of two techniques to augment maxillary sinuses using the lateral window approach: rigid synthetic resorbable barriers versus anorganic bovine bone. Five-month post-loading clinical and histological results of a pilot randomised controlled clinical trial.
      reported that insufficient bone had grown in one sinus in their test group 6 months after a graftless sinus lift procedure. Nevertheless, they decided to implant immediately and simultaneously add bone replacement material, which was followed by a satisfactory result.
      An important factor that influences the possibility of immediate implantation is the severity of the atrophy of the posterior maxilla. If the maxilla is completely edentulous, the extension of the maxillary sinus can result in severe three-dimensional atrophy with an osteoporotic-like bone structure. The cortical layers can be too thin and must be regarded as insufficient for implant placement with primary stability. Therefore, after complete tooth loss in the upper jaw and high maxillary atrophy, the space created by the tenting technique can be much larger than in patients with only partial tooth loss. When only a limited number of teeth are missing, a sinus cavity of limited volume bordered by bony walls needs to be filled with new bone. In cases of high atrophy and complete tooth loss, it can be much more difficult to create a stable blood clot as a prerequisite for new bone formation. Lie et al.
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      presented the only study that included completely edentulous patients only. This may have affected the results. Other factors that may have influenced the results are the different space holders used, the different types of bone replacement materials, and the mean residual bone height (Table 1).
      As in all publications on surgical procedures, wound healing complications will also have an influence on the results. Table 2 lists the complications observed in the test and control groups. Particularly with the technique presented here, extensive perforation of the sinus membrane can make it impossible to perform the procedure successfully. The extent to which these perforations had an influence on the meta-analysis cannot be determined, since the focus was on the issue of bone volume gain and implant survival. The complications mentioned in the literature analysed here are obviously processed in the publications.
      Analysis of the funnel plot suggested a potential risk of publication bias for two studies
      • Lie N.
      • Merten H.A.
      • Meyns J.
      • Lethaus B.
      • Wiltfang J.
      • Kessler P.
      Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans.
      • Fouad W.
      • Osman A.
      • Atef M.
      • Hakam M.
      Guided maxillary sinus floor elevation using deproteinized bovine bone versus graftless Schneiderian membrane elevation with simultaneous implant placement: randomized clinical trial.
      . The data from these publications should be interpreted with caution.
      Further studies with a long-term observation period and including larger patient populations in prospective standardized trials will show whether the newly formed bone in the floor of the maxillary sinus remains stable over time after a graftless sinus lift. Only in this way will it be possible to make a reliable statement on the long-term osseointegration of implants.
      In conclusion, this systematic literature review and meta-analysis showed a high implant survival rate in non-grafted maxillary sinus lifts and conventional sinus lifts using augmentation materials (97.92% and 98.73%, respectively). The graftless sinus lift group showed a significantly lower vertical gain in bone height with a mean difference of −1.73 mm (P = 0.01) and a significantly lower bone density with a mean difference of −94.7 HU (P < 0.001). There was no significant difference in the ISQ values between the test and control groups (P = 0.07). The values in the test and control groups are considered to predict high implant survival for both procedures.

      Funding

      The authors declare that no funding was provided.

      Competing interests

      The authors declare no potential conflict of interest.

      Ethical approval

      Not required.

      Patient consent

      Not required.

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