A Review of Sinus Floor Elevation Techniques: Lateral Window, Transcrestal, Graft Materials, and Biologics

Clinically, sinus pneumatization together with ridge resorption crestally can diminish available bone height for future implant placement. Additionally, the posterior maxilla often has poorer bone quality, which can compromise implant placement.³ Several strategies for implant placement in the atrophic posterior maxilla are currently advocated, including block bone graft, the use of short, tilted, or zygomatic implants, and sinus floor elevation (SFE). Among these, SFE has demonstrated a predictable surgical procedure to increase the bone height in the posterior maxilla.⁴

A review of the literature on this topic results in an abundance of information, divergent views, and even a lack of consensus. While the present review does not reveal new data on this common clinical scenario, it is intended to assess current published information to provide insights on decision-making regarding SFE techniques and associated graft materials and biologics.

Sinus Floor Elevation Techniques

The most employed SFE techniques are the lateral window technique for sinus floor elevation (LSFE) and the transcrestal sinus floor elevation (TSFE). Both approaches involve the placement of bone grafts in a space created by the elevation of the sinus floor.⁵ The reported outcomes of both procedural success and implant survival have been significantly high.

Lateral Window Technique

In the LSFE approach, first conducted by Dr. Hilt Tatum, Jr. in the 1970s and first published by Boyne and James in 1980,⁶ a full-thickness flap is elevated to expose the lateral sinus wall of the maxilla. Access to the maxillary sinus is accomplishedby creation of a window on the lateral sinus wall, with the sinus membrane integrity maintained. The "incomplete fracture" technique involves tapping the bony island to reposition it as a roof, which cannot be achieved easily in the narrow sinuses. The "wall-off" technique offers complete removal of the bony island, resulting in better access to the sinus.^7,8

Piezoelectric surgery for lateral window preparation and membrane separation has been shown to reduce intraoperative complications versus rotary instruments. The main advantages of the piezoelectric device are its selective cutting action of mineralized tissue and that its precise osteotomies enhance surgical control.⁹ Once exposed, the sinus membrane is detached from the bony walls using sinus membrane elevators and/or blunt piezoelectric tips, with care taken to avoid perforations and overextension beyond the region planned for bone augmentation. This enables placement of graft material in the newly created compartment. In sites presenting sufficient alveolar bone height, usually between 3 mm and 5 mm, simultaneous implant placement (ie, "one-stage" technique) can be completed. The bone graft of choice is then distributed in the newly created compartment after elevation of the sinus membrane; this is followed by implant placement, if indicated. A collagen membrane may be placed over the osseous window, especially if the window is relatively large, prior to flap closure. The alternative is a staged procedure, where the bone is augmented during the first surgical intervention, followed by placement of the dental implant(s) after the appropriate bone volume has been created (ie, "two-stage" technique).¹⁰

Whether to use a bone graft material in maxillary sinus floor augmentation procedures is generally determined by technical preferences and anatomical factors. Graftless maxillary sinus floor augmentation has been documented as a viable alternative that is associated with satisfactory outcomes. This approach requires simultaneous placement of implants protruding into the sinus cavity to tent the Schneiderian membrane and thereby create an adequate space for blood clot formation.¹¹

The sinus membraneis assumed to have osteogenic potential, inducing new bone formation around the inserted implants.¹² Spontaneous bone formation of up to 2 mm to 3 mm in the elevated sinus has been confirmed in animal studies.¹³ However, the amount of new bone formation decreases as the protruded length of an implant increases in SFE without graft material.¹⁴ To deal with this limitation, the use of bone graft materials is generally indicated in SFE to ensure sufficient space maintenance between the sinus membrane and the floor of the sinus cavity. Graft material is believed to improve primary stability by providing more substratum in which the implant can anchor.

Bone height has been shown to be increased by 8 mm to 10 mm using the LSFE approach.¹⁵ This approach, however, is often associated with substantial patient morbidity. It requires a wide mucoperiosteal flap with at least one vertical releasing incision for the creation of a lateral-wall bony window, which may result in an increased risk of postoperative pain, facial edema, delay in healing, bleeding, and postoperative infection.¹⁶

Transcrestal Window Technique

The TSFE approach was introduced by Tatum in 1976 and modified by Summers in 1994.¹⁷ Unlike LSFE, where a buccal bone plate osteotomy must be done, TSFE involves a crestal approach to the sinus membrane through the implant osteotomy drilled. This involves up-fracturing of the sinus floor using a set of osteotomes of increasing diameter to elevate the floor of the sinus while increasing the density of the surrounding maxillary bone, which results in better primary stability of the implants than with LSFE.¹⁸

After the osteotomy area is exposed either by raising a crestal flap or using a flapless technique, a 2-mm twist drill is used to create a pilot hole to 1 mm from the sinus floor. The osteotomy is expanded to 0.5 mm to 1.2 mm less than the size of the planned implant with either osteotomes or a series of osteotomy drills. Subsequently, particles of graft are inserted into the osteotomy and pushed toward the sinus via light tapping. Fracture of the sinus floor can be detected by a change in the resistance between the osteotome and bone or a change in the sound of the tapping. The osteotome should not be advanced into the sinus, as this increases the risk of perforation of the membrane.⁷ The extent of sinus lift achievable is largely dependent on the experience of the surgeon due to the closed approach and limited vision. An important drawback of the transalveolar approach is the possibility of inadvertent perforation of the sinus membrane. This may be associated with severe complications if graft particles are projected into the antral cavity and cause blockage of the ostium, which can result in chronic rhinosinusitis.¹⁹

A study using intrasinusal endoscopy, however, demonstrated that if TSFE is carefully executed the sinus floor may be elevated up to 5 mm without perforating the membrane. Because this technique is mainly carried out without visualization, there is little opportunity to detect perforations. In such cases, elevation should be confined to a height of 3 mm on average.²⁰ In the event that better visualization is required during the crestal approach due to an unexpected sinus membrane perforation, treating clinicians must be capable of performing both protocols (crestal and lateral).

TSFE is a less invasive treatment than LSFE with shorter surgery time and less postoperative discomfort.²¹ Furthermore, most TSFE procedures are done simultaneously with implant placement, reducing overall treatment time. A network meta-analysis demonstrated that TSFE is superior to LSFE at sites with a residual bone height (RBH) of 4 mm to 8 mm.²² The study results showed that LSFE is not suitable for patients with intermediate RBH because of the unjustified increase in complications and financial cost.

Indications for Sinus Floor Elevation Techniques

A 6- to 20‐year retrospective study demonstrated that implants with less than 3 mm of preoperative RBH before SFE had a lower survival rate than those with 3 mm or more of preoperative RBH.²³ When RBH exceeds 6 mm TSFE is the most indicated approach. When RBH is between 4 mm and 6 mm, TSFE is the most recommended approach if the sinus is in a relatively healthy state, whereas the lateral approach is preferred when the sinus and membrane are compromised (eg, a minor, roughly 2 mm, thickening of the sinus membrane, cysts). If RBH is between 2 mm and 4 mm, the lateral approach would be a more convenient alternative. Also, the lateral approach is recommended if the maxillary contours tend to be wide (or too sharp) and there is a septum within the lifting region, as the stretching potential of the sinus membrane will be relatively unfavorable and surgical difficulty and risks relatively high.²⁴

TSFE Technique Methods

Common methods to create sinus access include the use of osteotomes, rotary instruments, a combination of osteotomes and trephine burs, and piezoelectric instruments. The mechanical (hydraulic) pressure for the detachment of the sinus membrane from the sinus floor can be generated by different means, including osteotomes, a combination of osteotomes and graft biomaterials, a trephined bone core plus graft biomaterials, piezoelectric inserts with internal irrigation, injection of liquids through a channel internal to the implant body, and inflatable devices.²⁵

Since 2003, modifications to the original TSFE technique avoid the use of a hand mallet method and focus on a more convenient patient experience and reduced risk for complications. During the placement of maxillary dental implants with the osteotome technique, the trauma induced by percussion along with hyperextension of the neck during the operation can displace otoliths, as reported in some studies, and may provoke benign paroxysmal positional vertigo, which can be incapacitating and cause considerable stress to the patient.²⁶

TSFE is generally associated with low intra- and postoperative morbidity, and the use of drills can result in markedly less patient discomfort during surgery and substantially higher patient preference compared with osteotomes. Moreover, replacing manual instruments, such as osteotomes and a hand mallet, with powered instruments like piezoelectric inserts and an electromagnetic mallet may further reduce morbidity while maintaining the reconstructive capabilities of the latter.²⁷

Sinus Membrane Balloon Elevation Technique

The antral membrane balloon elevation technique lifts the sinus membrane with minimal trauma and is particularly useful in areas that are difficult to access. This approach is beneficial when teeth are adjacent to the edentulous area that requires augmentation. The initial drilling sequence is the same as osteotomy preparation in normal crestal bone not requiring sinus augmentation, and when the sinus membrane is accessed through the osteotomy site a hydraulic lifter with light pressure is introduced. Usually, a tube connected to a balloon with a syringe filled with sterile saline solution is used, and by pressing the plunger the balloon inflates and consequently elevates the membrane. Because saline will cause no harm if introduced into the sinus, the balloon is optional when using this technique. Advantages of the antral balloon protocol are a low incidence of infection and bleeding and low risk of perforation of the sinus membrane.^27,28

Rotary Instrument-Mediated TSFE Osseodensification

Osseodensification (OD) is a novel surgical technique for implant site preparation that preserves bone by using specially designed burs. The burs are used with a standard surgical engine and can densify bone by rotating in the noncutting direction (counterclockwise at 800 to 1,200 rotations per minute) or drill bone by rotating in the cutting direction (clockwise at 800 to 1,200 rotations per minute) with copious irrigation.

Contrary to conventional drilling techniques, this newer technique proposes an innovative approach for bone compaction through the application of controlled deformation via contact along the inner surface of the osteotomy with the rotating lands of the densifying bur. Bone deformation occurs through viscoelastic and plastic mechanisms. Copious amounts of irrigation fluid during the procedure provide lubrication between the bur and bone surfaces to avoid overheating.²⁹

OD demonstrated significantly higher implant insertion torque and primary stability values than standard subtractive drilling. A recent systematic review reported OD presented consistently higher implant stability quotient at baseline and 4 to 6 months following implant placement compared with conventional drilling.³⁰ With OD site preparation, the osteotomy is gradually expanded in both a lateral and apical direction so it can be used not only for ridge expansion but also for TSFE in a safe, predictable way with reduced morbidity.³¹

Once the sinus floor is penetrated by the non-excavating bone compaction drilling process and irrigation solution and autogenous bone chips/graft material are inserted, a hydraulic detachment of the sinus membrane and subsequent elevation are performed. Although OD has demonstrated good results in sinus elevation in cases with reduced RBH, the minimum bone height for the safe use of this technique has yet to be well established in the literature.

This approach is less traumatic than conventional drilling, resulting in increased bone density around implants and less healing time. A clinical study concluded that OD and LSFE were similarly effective in SFE with simultaneous implant placement when RBH was 4 mm or less. However, OD significantly outperformed LSFE in pain experience, impact on self-perceived quality of life, surgery duration, postoperative edema, and analgesics intake.³²

Hydrodynamic Piezoelectric Sinus Floor Elevation

Piezoelectric-mediated sinus elevation utilizes piezoelectric ultrasonic vibration (25 to 30 kHz); the piezosurgery device precisely cuts only mineralized structures (bone) without cutting soft tissues (membrane), which remain undamaged even in instances of accidental contact. SFE is performed using a round-headed instrument, helping to prevent perforations. The round insert has depth-indicating lines marked at 2-mm intervals to measure the exact residual bone height from the alveolar crest to the sinus floor. Additionally, the piezoelectric tip has a set of stopper sleeves at 2-mm intervals to prevent accidental membrane perforation when approaching the sinus floor.

Upon entering the sinus floor, the tip is kept in the osteotomy, applying hydraulic pressure on the sinus membrane for an additional 10 to 20 seconds. In most cases the sinus membrane is easily elevated using this procedure. Next, a 2.8-mm wide cylindrical tip is used to laterally enlarge the osteotomy, and elevation of sinus mucosa is then achieved by hydraulic pressure. Upon removal of the tip from the osteotomy, the surgeon can observe up-and-down excursions of the sinus membrane during breathing. A cylindrical tip is the final osteotomy tip to accommodate a 3.7-mm to 4.2-mm wide tapered implant for good primary stability.

The piezosurgery device allows for a clear surgical site and maintains a blood-free surgical field during site preparation; this is due to the air-water cavitation effect of the ultrasonic instrument. Piezoelectric-mediated SFE has been shown to reduce the membrane perforation rate.^3,33,34

Magnetodynamic Technology

In 2012, Crespi introduced an electromagnetic mallet for oral surgical procedures (Figure 1).³⁵ One of several modalities that have been utilized for the preparation of implant osteotomies and elevation of the sinus floor, the magnetic mallet is a novel surgical device designed to deliver a controlled, high-intensity impact in a very short period of time. Magnetodynamic technology exploits the physical principles of electromagnetism to apply controlled forces on a body while minimizing the time of impact. This maximized force delivered within a short impact time is said to minimize shock wave formation. The impact generated by the magnetic mallet is so rapid that friction only generates a small amount of heat, eliminating the need for irrigation of the treatment area. This enhances visibility, helping to avoid the loss of biological factors due to irrigation, thus creating improved implant stability due to bone compaction around the osteotomy site.³⁶

The magnetic mallet comprises a handpiece energized by a power control device, delivering forces by the timing of application, which decreases heat generation and is well tolerated by the bone. Different inserts may be attached to the handpiece, pushing a shock wave at its tip. Four force modes are available: 75, 90,130, and 260 daN (decanewtons). The time of impact is 80 microseconds. The magnetic impulse generated in the handpiece energizes the instrument with a force that is 10 times greater than that delivered by manual devices, with almost zero impact time. The control and steadiness of the applied forces enhance safety for patients and surgeons.^37-39

Hydraulic Sinus Floor Elevation

The use of controlled hydraulic pressure to detach the Schneiderian membrane from the sinuses' bony walls has been advocated to reduce the occurrence of membrane perforation. This technique can be implemented in both open and closed sinus lift procedures.⁴⁰ It involves gaining access to the Schneiderian membrane through either a crestal or lateral osteotomy and applying hydraulic pressure by means of direct water flow from a handpiece, with a radiographic contrast medium, such as saline or water, injected underneath the membrane via specially designed injectors or pumps. Once the membrane is detached from the sinus walls, a graft is carefully introduced and condensed through the osteotomy to increase ridge volume.

The hydraulic sinus floor elevation technique can be used safely to elevate a larger section of the Schneiderian membrane, resulting in lower rates of membrane perforation compared to conventional intracrestal SFE. This also allows grafting a large volume, which may result in improved implant stability.^19,41 The technique requires high-level skills; thus, clinical application is still limited. The evidence supporting the effectiveness and success of this technique is mainly based on case series, and no randomized clinical trials comparing the hydraulic sinus lift procedure with conventional open or closed sinus lifting techniques have been reported.¹⁹

Other Rotary Instrument-Mediated TSFE

The advantage of rotary instrument-mediated TSFE, also known as the crestal approach technique, over the osteotome technique is the ability to enter the sinus cavity, thereby reducing the risk of membrane perforation while minimizing patient discomfort. While all crestal access techniques are recommended to be adopted in combination with immediate implant placement after sinus elevation when residual bone height is 5 mm to 6 mm,⁴² cases using the crestal approach with a residual bone height less than this have been successfully treated.³³

In 1994, Cosci started a 6-year retrospective study of his technique on 265 implants with the first described rotating instruments specially designed for SFE with crestal access.⁴³ The procedure is accomplished by using lifting burs with a flat extremity 1 mm to 8 mm long in combination with crestal stoppers. Various transcrestal approach sinus elevation kits for the Cosci technique are available on the market today. They are designed to be used with an implant handpiece and employ non-end-cutting burs.

In this technique, the sinus floor is reached with a trephine, as measured on cone-beam computed tomography (CBCT), and perforated using a lifting bur 1 mm longer than the depth reached by the core bur. After completion of the osteotomy, an instrument with a blunt tip is used to carefully sound and determine the sinus membrane versus the sinus floor. If the presence of bone is felt, a 1 mm longer atraumatic lifting drill is used, and so on, until the sinus lining is felt. After confirming that the floor is removed, a Valsalva maneuver is done to determine that the membrane is intact. This is performed using a dental mirror to observe air flow or bubbles from the osteotomy, indicating perforation.

The integrity of the membrane can be assessed visually with a mirror when the bone is only a few millimeters thick and the sinus is located closer to the crest. If no perforation is noted, the clinician may proceed with membrane elevation and graft placement. The most basic way of elevating the membrane is by introducing the bone graft itself. Graft material is carefully placed in small quantities into the osteotomy with the aid of osteotomes by gentle mallet tapping and pushed to the depth of the sinus floor but not deeper. The amount of bone graft needed is determined by the amount of elevation needed. Radiographic verification at this stage may aid in determining the amount of bone elevation. Implant placement will add additional volume because it will push the graft apically.⁴⁴

Modified Trephine/Osteotome Approach

The modified trephine/osteotome approach facilitates SFE using an osteotome to elevate a core of residual alveolar bone cylinder, obtained with a trephine carried 1 mm to 2 mm from the sinus floor, instead of a drill, as a first step. The trephine is used at a reduced cutting speed to prepare the site to within approximately 1 mm to 2 mm of the sinus membrane. A calibrated osteotome corresponding to the diameter of the trephine drill is then used under gentle malleating forces to elevate the trephine bone core to a depth approximately 1 mm less than the prepared site. The widest osteotome utilized will be one drill size narrower than the planned implant diameter. Implant placement induces lateral dispersion of the elevated alveolar core with gentle and controlled displacement.⁴⁵

Localized Management of Sinus Floor Technique

When immediate implant placement is considered for teeth in close proximity to the sinus floor, a two-stage approach is typically followed. In many instances, extraction followed by ridge preservation with or without biomaterials is the first step. Placement of an implant is usually attempted after a suitable healing period.

Implant placement in fresh extraction sockets and simultaneous maxillary sinus floor elevation would greatly shorten total treatment time while allowing placement of implants that exceed the preoperative bone dimensions in length and width, which can be considered adequate to replace a multirooted maxillary molar.⁴⁶

Localized management of sinus floor (LMSF) technique is a further application of the principles of the edentulous ridge expansion technique. In a single surgery, the procedure combines elevation of the maxillary sinus floor, buccal expansion of the residual alveolar bone, and implant placement. As in the edentulous ridge expansion technique, bone regeneration and implant osseointegration occur simultaneously. The LMSF concept can be performed in fresh molar sockets, allowing wide-body implant placement into an immediate maxillary molar socket to obtain primary stability in the interradicular septum. This surgical procedure provides horizontal expansion in the empty root spaces and vertical expansion in the interradicular septum that normally is present in the palatal bone that covers the palatal root and lines the sinus floor.⁴⁷

The interradicular bone septum represents the ideal place for immediate implant placement in the maxillary posterior region; in some cases insufficient interradicular bone septum dimensions could compromise the LMSF procedure. Morphological examination of anatomical structures, CBCT, and related software are key tools in planning accurate implant position and performing guided dental implant surgery.⁴⁸

The recommended technique in this context is OD using the surgical burs with a pumping motion with copious irrigation to eliminate overheating. The fluid pumping coupled with high-speed counterclockwise rotation induces a hydrodynamic wave, termed the compression wave, ahead of the point of contact. This increases primary stability, bone mineral density, and the percentage of bone at the implant surface compared with standard and extraction drilling.^3,29

Modified Localized Management of Sinus Floor Technique in Fresh Molar Sockets

After tooth extraction, buccal expansion of the residual intra-septum bone, elevation of the maxillary sinus floor, and implant placement, the modified LMSF technique in fresh molar sockets introduces an additional procedure, which is performed after implant placement. This procedure slightly elevates the bone-graft-implant core into the sinus by means of an electromagnetic mallet to gain up to 5 mm additional SFE without perforating the membrane.

Once atraumatic molar extraction is attained, the surgical drilling is accomplished using a digital surgical guide. A sequential osteotomy is performed 2 mm less than the desired width of the implant but 1 mm below the sinus floor (Figure 2). The use of osseodensifying burs to perform the osteotomy is recommended in this context (Figure 3). Next, a trephine is utilized at a reduced cutting speed to prepare the core around the osteotomy, but 1 mm below the sinus floor (Figure 4). The magnetic mallet is then carefully applied with controlled force to collapse the sinus floor into the sinus cavity, elevating the sinus membrane 2 mm to 3 mm along with the bone fragment and bone graft material placed into the osteotomy site (Figure 5). Minimally invasive and user-friendly, use of the magnetic mallet delivers a preconceived force in an optimal amount of time.

An implant of predetermined dimension is placed, with primary stability assessed with a torque wrench (Figure 6). A wide emergence profile healing abutment is placed on the implant to prevent inadvertent displacement of the implant into the sinus during the initial osseointegration period. Tapping on top of the healing abutment in a vertical direction using the magnetic mallet on the lightest force mode allows an additional 3 mm to 5 mm SFE to be obtained (Figure 7).

Clinical Case Example

A 68-year-old male patient presented with sensitivity on an endodontically treated tooth (No. 3) in the maxillary right posterior area. He was seeking a long-term solution to alleviate his pain and sensitivity. The patient reported that the pain was intermittent since the endodontic treatment of the tooth. A periapical radiograph was recorded to evaluate the situation (Figure 8). Bone loss was noted between teeth Nos. 2 and 3. Significant probing was noted between the two molars, and the patient was informed that a possible vertical root fracture might be present on No. 3.

Treatment options were discussed, and the patient expressed that due to the persistent sensitivity on chewing he wished to have tooth No. 3 extracted. Because tooth No. 2 had significant bone loss on its mesial aspect, it was decided to extract both teeth Nos. 2 and 3 and place an implant only at site No. 3. The patient was informed that to ensure adequate bone to support an implant a crestal sinus augmentation would be needed, which would be done simultaneously as part of the implant placement. The patient was scanned with an intraoral scanner and CBCT for fabrication of a surgical guide.

The patient presented for the surgical appointment, and after review and signing of consent forms local anesthetic was administered. A #15 scalpel blade was used to reflect the marginal gingiva, and a full-thickness mucoperiosteal flap was elevated. Tooth No. 3 was sectioned in two pieces using a 557 surgical bur with copious irrigation with sterile saline. The tooth was removed in two pieces with elevation and forceps, and tooth No. 2 was also extracted. The sockets were irrigated with sterile saline, and an intracrestal sinus approach using a mallet tapping system was used to elevate the sinus at site No. 3. Bone graft material (alloOss^® allograft [50/50 mix], Ace Southern, acesouthern.com) was mixed with allograft material (DirectGen^™ Mineralized Cortical/Cancellous Particulate, 250-1000µm 1.0cc, Implant Direct, implantdirect.com), which was mixed with blood and then placed to lift the sinus. An implant (ULT^™, 5 mm x 10 mm, Ditron Dental, ditrondentalusa.com) was placed into the prepared osteotomy. Additional graft material was placed to fill any voids around the implant and also into the extraction socket at No. 2. A 3-mm wide healing abutment was placed, and soft tissue was sutured with 4-0 chromic gut sutures. A periapical radiograph was then taken (Figure 9).

Final impressions were taken 5 months after immediate placement of the implant, and a screw-retained restoration was fabricated by the dental laboratory and returned for insertion. The patient returned and the healing abutment was removed and final restoration inserted and screw-torqued to the manufacturer's recommendation. A radiograph and clinical photographs were taken (Figure 10 and Figure 11).

Grafting Materials

The physiological properties of bone grafts and bone substitute materials are often designated as osteoinductive, osteoconductive, and osteogenic. Osteoinductivity is the capability of a graft to actively promote bone formation. Osteoconductivity is a characteristic of the scaffold that facilitates the colonization and ingrowth of host bone cells and vascularization by reason of its 3-dimensional structure. Osteoconduction is a passive process that is destined primarily by the porosity properties of the graft scaffold and to a lesser degree by its chemical and physical properties that stimulate host cell adhesion and cell growth. Osteogenicity refers to the presence of bone-forming cells within the bone graft.⁴⁹ A variety of bone grafting materials are described below.

Autografts

The first graft material documented for maxillary sinus floor augmentation was autogenous bone derived from the patient being treated. Originally, autogenous grafts were preferred because of a decreased risk of host rejection and their osteoinductive, osteoconductive, and osteogenic properties. Autologous grafts are the only grafts with osteogenic potential, as they contain osteogenic cells within the bone graft. Among graft materials, autologous bone is still considered the gold standard.⁵⁰

While autogenous bone generally renders favorable outcomes, its use in SFE has two major drawbacks. First, there is the need to harvest a variable amount of bone, typically between 0.5 cc and 5 cc, from a second surgical site. This increases surgical time and the risk of intraoperative complications and postoperative morbidity. Second, the high biodegradation rate (up to 40%) associated with particulate autogenous bone may exceed the rate of new bone formation during the consolidation phase and lead to a suboptimal bone volume gain outcome.¹⁰ To overcome these disadvantages, different biomaterials have been used either alone or in combination with autografts in SFE procedures to exploit the inherent properties of autogenous bone while simultaneously leveraging the low resorption rate of some bone substitutes for enhanced volumetric stability of the graft.⁵¹ Although this approach makes sense biologically, from a clinical standpoint no specific bone graft material or combination thereof has been shown to be clearly superior for maxillary sinus floor augmentation.⁵²

Substitute Materials

Among osteoconductive materials, allografts (fresh-frozen bone, freeze-dried bone, demineralized freeze-dried bone), xenografts (of bovine, equine, or porcine origin), and alloplastic materials (different combinations of calcium-phosphate, bioactive glasses, or polymers) have been described in the dental literature as being able to enhance bone formation.⁵³ Furthermore, several studies have shown that these biomaterials may not adversely influence clinical outcomes and implant survival when compared to autogenous bone.⁵² Thus, the material selected is an important factor to consider.

Allografts-Allografts are a frequently used alternative to autogenous bone grafting and remain a suitable replacement material for regenerative procedures used in dentistry. These include SFE, guided bone regeneration (GBR), alveolar ridge preservation for implant placement, and other adjunctive grafting procedures in implant dentistry. The main advantage of allografts over other commercially available bone substitute materials is the incorporation of osteoinductive growth factors. Studies have demonstrated their effectiveness in promoting new bone. Although allograft bone substitutes are popular in the United States, many countries strictly regulate or prohibit their use in patient treatment.³ Limitations persist relating to the risk of infectious disease transmission, such as human immunodeficiency virus (HIV) and hepatitis B and C. These concerns can generally be alleviated through tissue processing such as sterilization, mechanical debridement, ultrasonic washing, and gamma irradiation of the graft material during manufacturer's processing.

Allografts have been successfully used in combination with xenografts for SFE procedures.⁵⁴ There is a clinical trend toward using mineralized bone allografts, which are radiopaque and provide improved osteoconductive scaffolding for bone ingrowth and maintenance. The particulate mineralized products come in cortical, cancellous, and mixtures of these two forms. They have a faster turnover and more physiologic resorption profile than slower resorbing bovine (xenograft) bone mineral.¹⁹

Xenografts-Xenografts are considered a viable alternative to autogenous bone due to their high osteoconductive properties and slow resorption rate. Currently, many bovine-derived xenograft materials dominate the market for bone substitutes. Various manipulation and purification modalities of bovine-originated graft materials have been introduced in commercial products, with varying characteristics and biologic behaviors.⁵⁵ These materials maintain space well and have high radiopacity that helps clinicians identify the material in the sinus at placement.⁷

Earlier studies on xenografts showed their clinical stability and superior osteoconductivity in addition to their usability in oral surgical procedures such as SFE.⁵⁶ Xenografts provide a matrix and scaffold, promoting the migration of osteogenic cells out of the surrounding maxillary sinus bone and toward the grafted site, thus enhancing the capacity for new bone formation. A promising xenograft material currently being researched is chitosan, a naturally occurring polymer derived from the exoskeletons of shellfish composed of glucosamine and N-acetylglucosamine.⁵⁷

Silk is another novel xenograft material currently being studied. Silk, a natural biopolymer obtained from the silkworm Bombyx mori, is predominantly comprised of proteins, fibroin, and sericin. After removal of sericin through degumming, silk fibroin is commonly used as a bone scaffold in sponge, fibers, film, and hydrogel forms. Silk fibroin demonstrates excellent biocompatibility, degradability, tissue integration, and oxygen and water permeability.⁵⁸

Despite their promising outlook, some limitations associated with the use of xenograft materials as bone substitutes still remain. These include variable resorption rates, lack of viable cells and biological components, and the need for tissue treatment processes, which could enable the retention of osteoinductive cells.⁵⁴

Alloplasts-To overcome potential immunogenicity and morbidity at donor sites, artificial synthetic bone substitute materials are manufactured to closely mimic the biological properties of natural bone. These materials are synthetically produced or derived from natural materials and processed. Nonetheless, currently available synthetic materials display only osteoconductive properties providing scaffolding for new host bone ingrowth and/or replacement. Numerous different types of alloplastic materials have been successfully used for sinus bone augmentation, including hydroxyapatite, calcium sulfate, calcium phosphate, bioactive glasses, titanium granules, and polymers.⁵⁴ Tricalcium phosphate was the first bone substitute used for sinus bone grafting. In the future, these materials might be capable of being customized for cellular constructs and delivery of growth factors.³

Biologics

Biologic agents are defined as natural mediators of tissue repair that regulate cellular events in the wound healing process via established mechanisms of action.⁵⁹ These include anabolic bone formation, angiogenesis, cementogenesis, osteoblast differentiation, matrix mitosis, chemotaxis, and other processes that improve the hard- and soft-tissue healing environment. Enamel matrix derivative, platelet-derived growth factor (PDGF), bone morphogenetic protein (BMP), platelet-rich plasma (PRP), platelet-rich fibrin (PRF), fibroblast growth factor (FGF), transforming growth factor (TGF)-β1, epidermal growth factor, vascular endothelial growth factor (VEGF), insulin-like growth factor-I (IGF-I), and hepatocyte growth factor are the most common biologic agents that have been shown in vitro and/or in vivo to promote bone formation for implant site development.⁵⁸

In its best evidence consensus statement in 2022, the American Academy of Periodontology concluded regarding the use of biologics in implant site development, including horizontal/vertical alveolar ridge augmentation and SFE with simultaneous or delayed implant placement, that there is limited evidence to support the assertion that the use of the previously mentioned biologics, either as a monotherapy or in combination with bone graft materials, renders superior clinical and radiographic outcomes when compared with conventional interventions. However, the adjunctive use of these biologics seems to translate into favorable histomorphometric outcomes (ie, mineralized tissue formation observed in bone core biopsies).⁶⁰

Platelet Concentrates in Regenerative Dentistry

In dental regenerative therapy, the use of platelet-rich products (eg, PRP, PRF, and concentrated growth factor [CGF]) derived from the patient's own blood currently appears to be a favored therapeutic option. When activated, platelets establish a network in the fibrin matrix and release growth factors that initiate wound healing via the enhancement of cell adhesion, proliferation, and chemotaxis. Introduced in the late 1990s, the original concept that led toward the preparation of platelet concentrates was that concentrated platelets and autologous growth factors could be collected in plasma solutions that could then be utilized in a surgical site to promote local healing.⁶¹ Although controversial, it is generally agreed that platelet-released growth factors reduce inflammation, decrease the risk of complications, and promote bone vascularization, which may be particularly beneficial in situations where poor or impaired healing outcomes are anticipated (eg, diabetic and osteoporotic patients). In addition, platelet-derived products reportedly can act as antibacterial agents against Staphylococcus aureus and Escherichia coli.⁶² Another advantage of some biologics, particularly autologous blood-derived products, such as PRF, is that they boost the handling properties of particulate bone graft materials.⁶¹ The main generations of autologous platelet concentrates are PRP, PRF, and CGF.

PRP, the first generation of platelet concentrates, is a plasma concentration high in platelets that may be produced by centrifuging the patient's venous blood and then using it as a bone-grafting material. Because of the limits of PRP related to its anticoagulant composition, additional research by Choukroun et al in the early 2000s focused on generating a second-generation platelet concentrate that was free of anticoagulant factors. The second generation of platelet concentrates, PRF, has the same qualities as PRP but with the added benefit of osteogenicity. Additives are not required in PRF because of the presence of fibrinogen, which is converted to fibrin under the effect of physiologically accessible thrombin; this minimizes the risk of postoperative complications.^63-67 While the results of the use of PRF on soft-tissue healing, gingival recession coverage, and periodontal regeneration are well documented in the literature, PRF's use in GBR and SFE and its effects on bone formation around implants is less studied.⁴⁰ Platelets are a natural source of growth factors, including PDGF, TGF-β1 and TGF-β2, FGF, VEGF, and IGF-I, which stimulate cell proliferation, matrix remodeling, and angiogenesis.

Developed in 2011, CGF is produced by centrifuging blood samples at alternate and regulated speeds in a specially designed centrifuge.⁶⁸ Platelets are thus concentrated in a gel layer comprised of a fibrin matrix rich in growth factors and leukocytes. CGF acts by degranulation of the alpha granules in platelets, which play a vital role in early wound healing. CGF contains more growth factors than the other platelet-based preparations, such as PRF and PRP, and unlike PRP, CGF does not dissolve rapidly following application.⁶⁹

While two of the main growth factors approved by the US Food and Drug Administration, PDGF and BMP, which are both derived from recombinant sources and fabricated in bacteria or mammalian cells, are sold for hundreds of dollars, growth factors harvested purely from autologous PRF are available through low-cost methods. Therefore, it is of interest to determine the benefit of using high supra-physiological concentrations of growth factors in recombinant form (PDGF and BMP) versus lower concentrations in autologous form (PRF).

Although recombinant proteins have a regenerative potential that is well documented in the literature, many biological limitations to their use (eg, swelling, edema), coupled with their low stability in vivo, remain a limiting factor.⁷⁰ Future research, therefore, should target the comparison of the half-life and bioactivity of the growth factors found in PRF in comparison to commercially available recombinant growth factors.⁷¹

A relatively newer concept of fabricating growth factors-enriched bone graft matrix using autologous fibrin glue-was described by Sohn et al in 2015.⁷² "Sticky bone" represents a biologically solidified bone graft composed of mixed granulometry (calcium triphosphate, xenografts, and dentin allografts derived from extracted teeth) entrapped in a fibrin network.^73,74

Conclusion

When selecting the optimal graft for SFE clinicians need to assess such factors as donor site morbidity, volumetric stability of the graft, implant loading protocol, costs, and patient wishes. "Over-augmentation" of the sinus may be clinically beneficial to compensate for volume reduction during healing regardless of the choice of biomaterial, especially when a two-stage procedure is used. The position and patency of the ostium, however, should be evaluated prior to surgery to avoid its iatrogenic blockage by "overfilling" with bone graft during sinus augmentation. This should be done via CBCT scan to detect any positional abnormalities.

The body of evidence is still limited with regard to establishing solid clinical guidelines on the use of products and procedures for maxillary sinus floor augmentation in daily practice. Targeted, well-designed long-term studies are needed that evaluate the performances of different bone graft materials and tissue engineering strategies in maxillary sinus augmentation to generate additional knowledge that will aid clinicians in discerning which surgical protocol might render the most favorable and predictable results in specific clinical scenarios.

DISCLOSURE

Dr. Kurtzman received compensation from Ditron Dental for this article.

ABOUT THE AUTHORS

Álvaro Gracia, DDS, DMD

Private Practice, Norton, Massachusetts; Diplomate, American Board of Oral Implantology/Implant Dentistry; Diplomate, Fellow, International Congress of Oral Implantologists

Ole T. Jensen, DDS, MS

Clinical Assistant Professor, New York University, University of Michigan, and University of Colorado at Denver; Diplomate, American Board of Oral and Maxillofacial Surgery

Gregori M. Kurtzman, DDS, MAGD

Former Assistant Clinical Professor, University of Maryland School of Dentistry, Baltimore, Maryland; Private Practice, Silver Spring, Maryland; Diplomate, International Congress of Oral Implantologists

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