Authors:
Yong-Seok Cho, DDS, PhD
David Chong, DDS
Seung-Min Yang, DDS, MSD, PhD
Brandon Kang, DDS

In the posterior maxilla, dimensional alterations of the alveolar ridges occurring after tooth loss are due in part to the pneumatization of the maxillary sinus. To increase available bone volume, guided bone regeneration using the sinus membrane as a natural barrierdsinus floor elevation surgerydhas been established. To this date, many methods of sinus floor elevation have been suggested and practiced using various modalities of lateral, palatal and transcrestal approaches. To minimize risks of lateral sinus grafting techniques, Tatum in 1986, published a technique that used a “socket former” selected according to the size of the implant that is to be placed. The socket former was tapped in a vertical direction until a greenstick fracture of the sinus floor was obtained. Summers in 1994, modified this technique using a specific set of osteotomes for preparing the osteotomy site when the subantral residual bone height is 5 to 6 mm and the bone is of low density.

Purpose: The aim of this study was to evaluate different patterns of sinus membrane elevation in pig jaws.

Materials and Methods: A total of 30 pig jaws (60 sinuses) were used for the present investigation. The hydraulic Crestal Approach Sinus kit was used to elevate sinus membrane, and different elevation patterns were recorded.

Results: There were 4 different scenarios of membrane separation patterns: center dome-shaped elevation, off-center dome-shaped elevation, horizontally spreading membrane elevation, and perforation. The incidence of each different type was 35.0% (n Ľ 21) in center dome-shaped separation, 51.7% (n Ľ 31) in offcenter dome-shaped separation, 10.0% (n Ľ 6) in horizontally spreading separation, and 3.3% (n Ľ 2) in membrane perforation.

Conclusion: Different patterns of membrane elevations are observed in pig sinuses and introduced in this study. The off-center dome-shaped elevation was the most common pattern followed by the center dome-shaped elevation and horizontally spreading elevation, respectively. (Implant Dent 2017; 26: 706–710).

Asystematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation shows 92.8% success rate after 3 years, proving the reliability of osteotome technique. In addition, clinical studies have proved the overall success rate to be independent of the type of bone graft inserted subantrally (autologous, heterologous, xenogenic, or synthetic). In the maxillary sinus, the most important factor to consider is the initial stability of the implant, not the residual height of bone or types of graft material. From these studies, osteotomemediated sinus elevation has proven to be a very predictable treatment modality. However, 1 disadvantage of using the osteotome technique is that it is very difficult to separate the membrane broadly.

It has been only recently suggested that the osteogenic layer of the periosteum at the base of the sinus membrane plays a key role in bone regeneration after sinus lift procedures. Leaving the periosteum of the schneiderian membrane attached to the bone should be avoided because “it is known that the periosteum and the periosteal collars are responsible for bone formation and that this tissue contains mesenchymal stem cells and preosteoblasts.” Once the periosteum has been left attached to the sinus floor, bone regeneration could be obstructed by the lack of delivery of bone morphogenetic protein-2, alkaline phosphatase, osteopontin, osteonectin, and osteocalcin to the augmentation site. Broad detachment of the sinus membrane increases the exposure of this osteogenic periosteal layer, hence, increasing the amount of bone regeneration. But more importantly, broad detachment exposes more bony surfaces that take part in wound healing. By elevating the membrane from the medial wall of the sinus to the height of the lateral window as proposed by Misch an additional surface area of bone is made available for wound healing.

Methods of sinus floor elevation that apply force over a larger area of the membrane rather than a smaller concentrated area have demonstrated lower rates of mucosal tearing.

One method, and the best way in authors’ mind, of optimizing the amount of periosteal detachment and exposed sinus walls is using hydraulic pressure. The hydraulic system minimizes the chance of perforation because of even distribution of lifting pressure (Pascal Principle) using a force over a large area and separating the membrane broadly. The aim of the present experimental study was to investigate different patterns of sinus membrane elevation during the process of hydraulic lifting in pig sinuses. Human studies are currently being investigated and followed.

MATERIALS AND METHODS

Animal

As we know, the pig as an animal model is well established in implant research. The maxillary sinus of adult pigs is known to provide a sufficient volume of up to 30 cm3 for the elevation procedure and a soft tissue lining that is comparable to human conditions.16,17 Thirty frozen maxillae (60 sinuses) of adult pigs (average age of 1 year) were used for this experiment. The specimens were frozen within 3 days after the slaughter and thawed in room temperature for 5 hours on the day of the experiment.

Osteotomy Preparation and Sinus Membrane Elevation

Although the elevation process in regions with Underwood septa does not significantly yield different elevation forces compared with sinus mucosa elevations without the presence of septa relatively smooth areas of lateral walls were selected for the lifts. The lateral walls were approached using the CAS-Kit (Hiossen Implant System, Fairless Hills, PA) (Fig. 1). The system uses a series of stoppers in 1-mm increments to approach the sinus wall transcrestally. To create the access, osteotomy, Kavo (KaVo INTRAsurg 300) engine, and a surgical handpiece (Contra-Angle KaVo INTRA C3-C09) were used. The handpiece provided a 27:1 gear reduction, and the engine speed was set to 800 rpm. Cooling was provided by saline solution, tempered at 15°C running at 50 mL/min. Once the moment of penetration was felt, a hydraulic lifter (Figs. 2 and 3) was adapted to the osteotomy site and the membrane was lifted with a light syringe pressure.

The membrane was separated according to the manufacture’s manual (push and pull method of 0.5-cc increments). Once the membrane was elevated using 3 cc of saline (Fig. 4, A and B), the elevation patterns were recorded and photographs were taken for each elevated sinus.
Analysis

The recorded numbers of sinuses with each different pattern were simply divided by 60 (the total number of sinuses) and described as percentages.

RESULTS

There were 4 different scenarios of elevation (Fig. 5, A and B). In majority of the cases (51.7%), the membrane elevation occurred skewing to one direction. We termed this pattern as “offcenter dome-shaped elevation (Fig. 6, A and B).”

The next common pattern was termed as “center dome-shaped membrane elevation (35.0%). In this type, the elevation was more or less even around the sinus floor penetration area (Fig. 7, A and B). The third pattern of elevation was termed as “horizontally spreading elevation (Fig. 8, A and B).”
In this pattern (10%), the elevation occurred in horizontal directions rather than vertical directions unlike the center dome- and off-center domeshaped respectively. Clinical implication of these different patterns is to be discussed in our subsequent human study if the clinical investigations confirm the results of the present animal study. elevations that occurred in more vertical directions. And last, there were perforations (Fig. 9, A and B) that occurred in 2 sinuses (3.0%).
The perforations occurred during mechanical access to the wall, not during the elevation of the membrane. The direction of elevation in the off-center dome-shaped group (nĽ31) was also recorded in this study (Fig. 10, A–C). The anterior and inferior directions were the most common followed by anterior and anteroinferior directions. The superior and posteroinferior directions were the least common types.
DISCUSSION

The presence of a torn Schneiderian membrane encountered during lateral sinus augmentation therapy should not be viewed as a contraindication to either proceeding with planned augmentation with or without simultaneous implant placement or to the attainment of satisfactory sinus augmentation results. However, in transcrestal sinus lifts, a prerequisite for successful membrane separation is the presence of an intact membrane. It is agreed that intact periosteum of the sinus membrane covering the augmentation site is crucial for the success of bone regeneration in sinus grafts. One advantage of using the CAS-kit is that it has a stopper system that minimizes inadvertent perforations of the membrane.

More importantly, the authors prefer hydraulic systems because of their ability to separate the membrane widely and safely. The formation of woven bone and its transformation to lamellar bone would be expected to begin from the bony walls and advance toward the central area of the graft. Broad detachment of membrane increases the exposed bony surface areas, increasing the amount of osteogenesis. In addition, hydraulic detachment exerts only uniform small pressure forces that will be evenly distributed between the periosteum and the bony sinus floor, fully avoiding producing tensile shearing forces. The pneumatic balloon pressure system is also capable of separating the membrane widely. But recent results have shown that the average pressure to lift up the sinus membrane in the sheep model is much lower if hydraulic pressure is used instead of pneumatic balloon pressure making hydraulic system a safer one.

To this date, there are no studies of sinus elevation patterns in humans. In our animal study, 3 different patterns were recognized. Conceptually, center dome-shaped elevation would be the most ideal separation pattern while offcenter dome-shaped is less than ideal. Theoretically, if the off-center membrane elevation occurs to either medial or lateral wall only, there would be 1 less wall exposed for osteoconduction and wound healing as mentioned by From et al. Whether this would be significant clinically would need to be investigated further.

In this pig study, the anterior and inferior directions were the most common way of membrane separation among the off-center dome-shaped group. Uneven separation might be possibly explained by any history of sinus disease leading to uneven thickness or attachment, different shapes of the sinus, and perhaps gravity working on the hydraulic medium. Lateral walls in pig sinuses take different shapes than human sinus floors, obviating the need to investigate the difference in humans.

Furthermore, the effects of off-center dome-shaped membrane elevation on bone regeneration and implant success rate need to be studied further. This investigation was directed to the lateral sinus wall of pig jaws instead of the floor, providing limited clinical relevance to sinus lifting procedure using crestal approach. However, some clinicians are recently attempting to approach the lateral sinus wall using hydraulic method granting greater clinical significance to this study.

CONCLUSION

Different patterns of membrane elevations are observed in pig sinuses and introduced in this study. The offcenter dome-shaped elevation was the most common pattern followed by the center dome-shaped elevation and horizontally spreading elevation, respectively. Clinical implication of these different patterns is to be discussed in our subsequent human study if the clinical investigations confirm the results of the present animal study.

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