Evaluating Bone Graft Substitutes Combined with Sinus Floor Elevation for Posterior Maxillary Implant Stability

Introduction

Progressive alveolar resorption, which occurs with pneumatization of the maxillary sinus (enlarging of the sinus ca­vity at the expense of the surrounding bone) complicates the rehabilitation of the edentulous posterior maxilla with dental implants. These two events combined frequently result in a very thin vertical implant envelope remaining for the clinician to deal with when taking a conventional length implant into it with acceptable primary stability. Maxillary sinus floor elevation (SFE) through either a lateral window, a transcrestal osteotome or a more recent osseodensification-based crestal approach is one of the most well documented and predictable pre-implant augmentation procedures, but the long-term success of SFE is highly dependent on the biological behavior of the bone graft substitute used to fill the space created beneath the elevated Schneiderian membrane [1–3].

These materials include autogenous bone (bones removed from the patient’s own body), allogeneic bone (human donor bone), xenogeneic bone mineral (animal bone mineral), alloplastic ceramics, composite materials (mixes of the above), and graftless membrane-stabilized protocols (no particulate material used at all). These are supplemented by increasing amounts of biologic adjuncts, including platelet rich fibrin (PRF) and recombinant human bone morphogenetic protein-2 (rhBMP-2), which seek to enhance and/or accelerate the biological quality of the regenerated bone. The osteoconductivity, osteoinductivity and volumetry of these materials are variable and therefore their selection has implications not only on the rate of new bone formation but also on implant stability, most commonly measured in clinical practice by the Implant Stability Quotient (ISQ) obtained by resonance frequency analysis (RFA) [4, 5].

The literature reviewed here summarizes the comparative data regarding bone graft substitutes and SFE with a particular interest in the outcome of implant stability, implant survival and vertical bone gain in the posterior maxilla. It also explores the interaction between surgical technique and residual bone height, the occurrence and management of the most common intraoperative complication (Schneiderian membrane perforation), and finally a practical and evidence-based approach that will assist in daily clinical decision making in material selection.

The anatomical and surgical factors to consider are listed below:

To form a sub-antral compartment, the Schneiderian membrane, a thin two-layered mucoperiosteal lining of the sinus floor consisting of a respiratory epithelium layer overlying a periosteal layer, must be atraumatically raised, and then filled with graft material or, in graftless protocols, left to fill spontaneously with a stabilized blood clot. Intraoperative perforation is the most common complication of SFE, and is consistently found to be associated with membrane thickness <1 to 2 mm and intra-sinus septa, with a pooled meta-analytic incidence of approximately 23.5%, varying from 3.6% to 41.8% across >1,600 documented procedures depending on operator experience and patient anatomy [6, 7]. When properly recognized and repaired during surgery, usually with a resorbable collagen barrier placed over the defect before placement of the graft, the effect of intraoperatively recognized perforations on implant survival does not seem to be significant when compared to elevations performed without an intraoperatively recognized perforation, but the risk of postoperative sinusitis is measurably higher, especially in smokers, and the risk for a wound dehiscence is also higher than in the non-smoking population, although this does not seem to significantly affect implant survival [6–8].

Table 1 summarizes the key anatomical factors that guide the choice of surgical approach and the timing of implant placement, with residual bone height (RBH) being the primary one that is examined using cone-beam computed tomography (CBCT), with the alveolar crest measured and the sinus floor identified. The widely used though less well validated bone-quality classification of Lekholm and Zarb still guides treatment planning: heights >~8–10 mm typically permit conventional implant placement without augmentation; heights of 4–8 mm typically permit simultaneous implant placement, either through a crestal (osteotome or osseodensification) or lateral window elevation technique; and heights <~4 mm usually require staged grafting using either the lateral window or crestal approach, with delayed implant placement following a healing interval of ~6–9 months to allow for adequate initial bone-to-implant contact prior to functional loading [9, 10].

Table 1. Residual bone height categories and corresponding SFE treatment approach

The lateral window approach is the most predictable membrane elevation and is the most commonly used approach for larger vertical augmentation or when the bone height is very low and involves a preparation of a bony window in the lateral wall of the maxillary sinus for direct visualization, but has longer surgical times and is more invasive. The transcrestal osteotome and osseodensification techniques do not access the sinus floor through the sinus window but through the implant osteotomy and are far less invasive and well tolerated by patients, but offer a lower level of direct visualization of the membrane. Comparative randomized trials and systematic reviews between osseodensification and classic osteotome-mediated elevation and lateral window augmentation have shown comparable implant survival rates between groups, higher ISQ scores at implant placement and abutment connection with osseodensification, statistically shorter surgical times, and fewer postoperative complications with osseodensification, with a slight reduction in endo-sinus bone gain between osseodensification and lateral window augmentation. The crestal elevation technique has also been evaluated using computer planning and digital guidelines to enhance the accuracy and safety of the free-hand technique compared with the transcrestal approach [11–13].

Types of bone grafts

Traditionally, SFE graft materials can be categorized according to their biological origin and action, as shown in Table 2. The osteogenic, osteoinductive, and osteoconductive combination of viable osteoprogenitor cells, growth factors, and a scaffold that can be directly incorporated into the host bone has made autogenous bone historically the biological gold standard. Even with this promising biology, however, the autogenous bone has been shown to resorb at a rate of approximately 40–46 percent within 6 months of augmentation in several controlled series — significantly faster than the resorption rates of xenogeneic or alloplastic materials (Fig. 1) [3, 13]. Interestingly, this volumetric instability does not seem to adversely affect clinical outcomes: in fact, the same is true for head-to-head randomized trials comparing autogenous bone grafts to porcine xenografts in the same patients (split-mouth design), in which superior implant survival, equivalent radiographic bone level gain, and similar histomorphometric bone formation were demonstrated without the morbidity associated with a second donor-site surgery [14, 15]. The practical disadvantages of autogenous bone are not biological, but rather: a second surgical site; a limited amount of bone available for harvesting; longer operating time; and unpredictable resorption of the graft when the goal is to support a fixed prosthesis for decades, not years.

Table 2. Overview of the principal bone graft substitute categories used in maxillary sinus floor elevation

Category	Origin	Mechanism	Volume Stability	Examples
Autogenous bone	Patient (intraoral/extraoral)	Osteogenic, osteoinductive, osteoconductive	Rapid resorption (~40–46% at 6 months)	Ramus, symphysis, iliac crest
Allograft	Human donor (processed)	Osteoconductive; osteoinductive if demineralized	Intermediate	FDBA, DFDBA, fresh-frozen bone
Xenograft	Animal-derived	Osteoconductive	High stability (~7% resorption)	Bovine DBBM, porcine mineral
Alloplast	Synthetic ceramic	Osteoconductive	Variable; tunable by HA:β-TCP ratio	HA, β-TCP, biphasic CP
Graftless	None (blood clot)	Spontaneous osteogenesis	Lower absolute bone gain	Resorbable barrier membrane

Figure 1. Comparative graft volumetric resorption by material category (illustrative, 6–12-months follow-up)

Allogeneic bone (processed as freeze dried bone allograft (FDBA), demineralized freeze dried bone allograft (DFDBA), or fresh frozen bone) has an intermediate biological profile; it contains some osteoinductive potential, specifically demineralized preparations which expose bone morphogenetic proteins within the matrix, and it also has zero donor-site morbidity. Comparative studies with autogenous bone or bovine-derived xenografts have broadly similar volumetric remodeling patterns, radiographic density dynamics, and have shown implant survival rates of >94 percent, with two-stage surgical protocols, as well as severely reduced pre-implant bone height (<4 mm) identified as independent risk factors for increased complication rates for both types of grafts [16–18]. Processing methodology is also important for allogeneic material: the demineralization of the material enhances the osteoinductive properties, but may reduce the initial mechanical scaffold rigidity, which affects material handling at surgery and the final cost of the material to the clinic; the fresh-frozen processing presents more of a tissue banking and screening process, and maintains a higher mechanical scaffold rigidity, but the properties are less osteoinductive.

Xenografts, which consist mainly of deproteinized bovine bone mineral (DBBM, such as Bio-Oss), and, more recently, collagenated porcine-derived material, are simply osteoconductive scaffolds with the natural trabecular architecture of the source bone preserved after organic and cellular elements have been removed. They offer a significant clinical benefit, namely their high volumetric stability, with network meta-analytical data showing that xenografts experience little volume reduction after the augmentation (7 percent) compared to autogenous bone (over 40 percent) after corresponding time periods, which makes them very appealing for cases where long-term maintenance of the vertical dimension is a priority. No definitive findings have emerged comparing directly the performance of the two animal sources, but direct comparisons of bovine- and porcine-derived xenogeneic mineral have indicated that the performance is generally similar in both the histological and radiological aspects [3, 4, 19]. Xenograft particles do not resorb quickly, and so very often (and perhaps paradoxically) they remain identifiable on histology and radiography for many years after implants, which may be viewed as a drawback compared to fully remodeled autogenous bone, but which seems to be the source of the excellent long-term volumetric results.

Alloplastic ceramics (hydroxyapatite (HA), beta-tricalcium phosphate (β-TCP), and biphasic calcium phosphate blends of the two) are synthetic, purely osteoconductive materials, which do not carry any risk of disease transmission or immunogenicity, and which enable manufacturers to have a precise control of the particle size, porosity, and resorption kinetics. Pure HA is resorbable very slowly over clinically-relevant periods of time and acts as a long-term space maintaining scaffold, whereas the resorption and substitution with the host bone of β-TCP is progressive and generally faster, biphasic formulations are designed to maintain the scaffold function for a certain period of time and then to resorb and be replaced by host bone. A 10-year prospective clinical series of lateral window augmentation with β-TCP yielded a high implant survival rate of 97.2 percent, and a mean vertical bone gain of about 7 mm with a starting residual ridge height below 5 mm, which indicates the long-term reliability of this material in severely atrophic ridges [2, 20, 21]. Alloplastic ceramics are also made, not harvested or donated, therefore there is a potential for unlimited supply, and in principle, lot-to-lot consistency can be tightly controlled and that is why their use has been increasing in high volume implant practices.

Many composite grafts have been used, most frequently combinations of autogenous bone and a xenograft or alloplast in different proportions, with the aim of providing biological activity from the autogenous bone with the volumetric stability provided by the slower resorbing material of the xenograft or alloplast; comparative volumetric analyses indicate that such mixed grafts can limit, but not prevent, the resorption normally associated with pure autogenous grafts. Graftless protocols are an alternative surgical concept that eliminate particulate material completely and depend upon elevation and mechanical support of the membrane (using a resorbable barrier or the coronal section of a concurrently placed implant) to establish and sustain a sub-antral space that will fill spontaneously with a stabilized blood clot. Comparative randomized studies of graftless versus grafted SFE usually show comparable implant survival and, notably, statistically similar implant stability quotient values for both methods, but a consistent and measurable decrease in vertical bone gain and radiographic bone density in the graftless technique, especially when there is at least 4 mm of residual bone height [22–25]. Finally, whether a composite blend or a graftless protocol is used depends less on the difference in implant survival, which is similar between the two, and more on the amount of absolute vertical bone volume that the clinician feels is required to support the planned implant prosthesis for the duration of its service life.

Biologic Adjuncts

Platelet-rich fibrin (PRF) and its derivatives, primarily in combination with deproteinized bovine bone mineral (dBBM), have been well researched as adjuncts to promote healing and to improve the regeneration process. However, when using the evidence for an actual biological benefit, the findings are inconclusive and seem to vary according to the specific outcome investigated with a meta-analysis of sinus elevation showing that PRF did not result in a statistically significant difference in histological new bone formation when compared to a bone graft alone, but that PRF was linked to a slight, yet measurable, augmentation of the primary stability quotient values. At the opposite extreme, leukocyte-enriched PRF that was more recently studied, when used in combination with bovine mineral, has been correlated with a statistically significant improvement in new bone formation and a significant decrease in residual graft material, indicating that the specific formulation of PRF and combination with a slowly resorbing xenograft scaffold may be more important than the use of platelet concentrate alone [26–28]. A split-mouth trial comparing PRF with freeze-dried allogeneic bone graft in one stage implant placement showed that there were no differences in implant stability between the two, indicating that PRF alone in selected cases, can achieve a similar stabilizing effect as a conventional allograft [29]. However, the popularity of PRF as an adjunct probably has much to do with its preparation on the chair, using only the patient’s own venous blood and no additives, hence it has only a material cost of a centrifuge and collection tubes, which is a significant factor.

Bone morphogenetic protein-2 (rhBMP-2) delivered on an absorbable collagen sponge is actually an osteoinductive agent that stimulates de novo bone formation, rather than just modulating healing. The original pivotal multicenter trials showed that rhBMP-2 could result in alveolar bone of density and structure similar to native bone and withstand functional implant loading, while having a success rate statistically similar to that of conventional autografts treated sinuses without the morbidity of harvesting from the iliac crest. These results have been confirmed by long-term retrospective follow-up in which an increase in implant survival at 3 and 5 years was observed when rhBMP-2 was used in conjunction with graft material, especially when the residual bone height was poor before the implant placement, while a decrease in marginal bone loss was noted during function. Pilot studies have also demonstrated that the application of rhBMP-2 is suitable in the crestal sinus augmentation technique, and initial results have confirmed that suitable bone formation for the function of the implants is achieved [30–33]. Unlike PRF, rhBMP-2 is a regulated biological product known to have a specific dose and a somewhat predictable, but generally not large, propensity for causing soft tissue swelling, resulting in a higher price tag that makes rhBMP-2 a product that is used when a high osteoinductive stimulus is specifically requested — such as larger defects, poor healing potential, or the desire to avoid an autogenous harvest altogether.

Implant Stability Assessment

The stability of implants can be conventionally divided into primary stability, which is purely mechanical and depends on the degree of contact between the implant surface and the surrounding bone during the implant placement, and the secondary stability, which is biological and comes with the subsequent weeks and months as osseointegration takes place. RFA, primarily by electromagnetic transducer devices, is the most widely used clinical approach to non-invasively quantify implant stability, and results are reported on a scale of 1 to 100, with scores above approximately 60–70 deemed acceptable [4, 5, 34] depending on the implant system and protocol used.

Repeatable and non-destructive, RFA enables that same implant to be tracked from placement to healing, and then into function, longitudinally. The clinical patterns are typical with a tendency of ISQ values to drop during the first 3 to 5 weeks after implant placement, coinciding with the loss of mechanically engaged stability faster than the gain of biologically acquired stability (dip pattern observed in both grafted and graftless sinus-augmented sites) followed by an increase as secondary stability continues to develop. In the particular case of sinus augmentation, it has been demonstrated that ISQ trajectories vary measurably by grafting material and surgical technique, offering an objective and quantifiable result to measure the relative biological performance of different bone graft substitutes, besides the binary implant survival [34, 35].

Comparative Outcomes and Complications

In the vast majority of systematic reviews and meta-analyses used in this paper, the implant survival rate after SFE surgery is consistently very high, ranging from 95 percent to over 97 to 98 percent at 1 to 10 years’ post-surgery, as detailed in Table 3 and Fig. 2. Apart from some exceptions, head-to-head randomized comparisons have not shown any statistically significant differences between materials in terms of implant survival, meaning this end-point is not a sufficiently discriminating variable for comparing the status of graft materials [1, 2, 15, 16].

Table 3. Representative implant survival, bone gain, and Implant Stability Quotient (ISQ) findings from studies

Figure 2. Representative implant survival across comparative studies

The only materials that show consistent differences in the magnitude and long-term stability of vertical bone gain are xenografts and alloplastic ceramics, which generally have the greatest long-term stability of any materials examined, whereas autogenous bone, although very good early on, has the greatest volumetric long-term stability of any materials examined. Furthermore, network meta-analytic synthesis of the histomorphometric outcomes from dozens of RCTs shows that materials with a combination of osteoconductive scaffold and osteogenic and osteoinductive component generally perform more favourably for percentage of newly formed bone than purely osteoconductive alloplastic materials without any osteoinductive or osteogenic components [3, 4, 36]. However, the number of comparative ISQ measurements is still relatively small and the data available to date are mostly not directly related to graft material, and the few randomized data available indicate similar secondary stability across well-established categories after sufficient healing time, with a randomized controlled trial comparing biphasic calcium phosphate grafting with graftless osteotome SFE showing that implant stability quotient values were significantly higher in the grafted group after 1-year follow-up [35].

The choice of graft material is NOT a primary determinant of whether or not implant placement can safely be simultaneous to grafting; rather, it is residual bone height. There have been overall high and comparable implant survival rates between the two protocols when comparing one-stage procedures and two-stage procedures in severely atrophic ridges (RBI <3 mm) with the same graft material and surgical technique used, and there were no significant differences in total bone height gain between the two groups [9, 37]. In such situations, in which medium bone height is present, the short implant (defined from 6 to 8 mm or even less) has been more and more studied as an alternative treatment without the need of a sinus augmentation or an osteosynthesis procedure. Several systemic reviews and meta-analyses of randomized trials with long-term (5 years or more) follow-up have shown that survival rates in short implants are statistically similar to those in standard length implants with simultaneous SFE, but some have indicated that the short implants had significantly less marginal bone loss and fewer biological complications; the rate of prosthetic complications was somewhat higher for short implants, which may suggest less favorable crown-to-implant ratios [38–40].

Lastly, network meta-analyses that ranked multiple graft and adjunct combinations by their histomorphometric performance have identified 3 xenograft combinations that appeared to be most favorably ranked; xenografts consisting of bovine xenograft supplemented with autologous bone marrow concentrate and xenografts of bovine xenograft combined with platelet-rich plasma, suggesting that cell and growth factor supplemented xenograft may have histological advantages over xenografts alone, but this ranking came from indirect network comparisons between combinations and is not confirmed in head-to-head comparisons between all combinations [4, 36]. It should be noted that the ranking is specific to the histomorphometric data on new bone percentage (laboratory derived) and does not necessarily reflect the overall performance of the materials in terms of implant survival, maintenance of margins and functional longevity of the prosthesis and should therefore be seen as one factor among several.

The clinical decision-making and limitations

Based on the review of the literature provided above, a few broad guidelines can be drawn for the selection of materials and techniques in sinus augmentation. Synthesizing the data above, a few general guidelines can be deduced for material and technique selection in sinus augmentation. The decision of the type of graft material to use should be independent of the surgical approach and timing of implant placement, to a large extent by the residual bone height. If there is still 4 mm or more of bone remaining and a modest augmentation required, then a graftless or minimally grafted protocol can provide implant survival and stability quotient (SQ) results that are statistically similar, but with slightly lower absolute bone gain. For those cases in which a significant amount of vertical augmentation is needed or long-term volumetric stability is important, a xenogeneic or alloplastic material, possibly supplemented with a lesser quantity of autogenous bone and/or a biologic adjunct, provides the best balance of stability and biological performance known from the comparative literature. Generally, it is not recommended to use autogenous bone as the only material for long-term volume maintenance, but its osteogenic potential is useful when specifically needed. Platelet concentrates have minimal evidence of benefit and may be used as an adjunct in early implant stability, but have a higher risk of allergy, whereas rhBMP-2 has the most evidence for a true osteoinductive effect, but is used more selectively due to cost and regulatory concerns. Lastly, short implants are a less invasive option than sinus augmentation in patients with moderate atrophy if an 8 mm or smaller implant will be sufficient for the prosthetic [1, 9, 20, 30, 38].

There is some underlying evidence that is subject to significant limitations, which dull the force of these conclusions. The sample sizes are relatively small in many of the trials, the biopsy or implant loading time varies significantly and a split-mouth design is often used to provide statistical efficiency and may or may not be generalizable to the more common single-sinus clinical scenario, and the healing time before this type of test varies among trials making cross-study comparison difficult. The overall level of bias and the comparatively low level of certainty of evidence identified in available randomized controlled trials suggest a high overall risk of bias in systematic reviews of osteotome-based and osseodensification-based crestal techniques, with inconsistent blinding, outcome reporting, and short observation periods when compared to the multi-year functional lifespan of an implant-supported restoration. Further, reporting of implant stability quotient values is also inconsistent throughout the literature both according to type of implant and the time of measurement, with comparatively few long-term data (beyond 10 years) reported for most categories of graft materials other than autogenous bone and beta-tricalcium phosphate [4, 12, 20, 34, 36]. Selection and publication bias are also possible in this literature as favourably presented series of case studies or industry-sponsored trials of newer proprietary materials may have a greater chance of being published than less favourable trial results, and relatively few studies report the funding source or manufacturer involvement in sufficient detail for formal assessment to be undertaken.

Conclusions

SFE in the posterior maxilla has a high implant survival, generally over 95 percent, with little difference in survival among the various bone graft substitutes (autogenous bone, allograft, xenograft, alloplast, or graftless membrane-stabilized protocol) utilized as long as the surgery is performed in a sound manner and sufficient healing time is allowed before functional loading. The materials that differ meaningfully from each other are those in graft volumetric stability, where autogenous bone offers the widest range of resorption rates, although it has the most positive effects on biological activity, and those in histomorphometric new bone formation, where there is a clear difference in favor of the osteogenic and osteoinductive materials and adjuncts as compared to purely osteoconductive scaffolds used alone; to a lesser, but clinically relevant extent, in implant stability quotient trajectories. The use of surgical technique and the amount of bone height lost was found as important as the type of graft material in determining the possibility of simultaneous implant placement and complication rate, with the most frequent complication being Schneiderian membrane perforation, which occurs frequently but does not seem to affect implant survival as long as it is managed appropriately. When making a choice for SFE, the clinician should consider the efficacy of the bone graft material for the desired amount of vertical augmentation, the amount of remaining bone, the presence of risk factors in the patient, and the cost and clinical proof of efficacy of the biologic agents used in combination with the bone graft material, rather than implant survival as the only outcome to be used to determine the type of bone graft material to choose. Ongoing, systematic, and long-term comparative studies will be vital to further develop evidence-based selection of materials for this frequently performed and clinically significant procedure.

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Надійшла до редакції/Received: 05.09.2026
Прийнято до друку/Accepted: 21.09.2026