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Sinus membrane elevation and implant placement

Sinus Schneiderian membrane elevation surgery is widely performed for dental implant placement in the maxillary posterior region. With regard to sinus elevation surgery, various complications can occur and lead to implant failure. For successful implants in the maxillary posterior region, the clinician must be well acquainted with sinus anatomy and pathology, a variety of bone graft materials, the principles of sinus elevation surgery, and prevention and management of complications.


I. Introduction
Dental implants in the maxillary posterior region are known to exhibit poor clinical outcomes due to lack of residual bone height and poor bone quality. Various surgical techniques have been developed to compensate for bone quality and quantity of the maxillary posterior region. Regarding insufficient residual bone height, sinus Schneiderian membrane elevation should be performed to prevent maxillary sinus invasion of dental implants. Although bone grafting surgery is commonly accompanied by this procedure, sinus membrane elevation is performed without bone grafting. These surgical techniques have been introduced using the following terms: sinus graft, sinus bone graft, sinus lift graft, sinus augmentation, maxillary sinus augmentation, maxillary sinus floor bone grafting, sinus lift (elevation), sinus membrane elevation, sinus floor elevation, sinus filling (packing), and sinus repair 1 . Concerning sinus elevation surgery, many studies have been classified candidates into relative and absolute contraindications, but the decision of surgical technique is mainly dependent on the preference and experience of the clinician 2 . (Table 1)

II. Types of Sinus Membrane Elevation Surgery
Sinus membrane elevation surgery is classified into crestal (internal sinus lift, socket lift) and lateral (lateral sinus lift) approaches. Generally, the type of approach is selected based on residual bone height. The crestal approach is safe in cases of residual bone height greater than 5 mm, and bone height of 3-4 mm can be obtained. The lateral approach is recommended when residual bone height is 5 mm or less 3 .
Recently, however, these techniques have not been widely used due to their high risk of sinus membrane perforation and complications. In addition, many devices have been developed that can safely contribute to the crestal approach. To prevent the risk of complications such as sinus perforation, head trauma, and vertigo, devices such as balloons, hydraulic pressure, special reamers, and piezoelectric drills are used [5][6][7][8][9] . With regard to the crestal approach, many implants are simultaneously placed with the approach, and bone grafting is performed based on the amount of elevation required and the preference of the clinician.

Lateral approach
The lateral approach is mainly performed when residual bone height is <5 mm or pathologic conditions are observed in the sinus. After forming a lateral window with various instruments, the sinus membrane can be elevated. Even though special surgical techniques with various instruments and drills have been developed to minimize risk of sinus membrane perforation, surgeon skill and experience is critical to prevent complications 9,10 .

1) Sinus membrane elevation without bone grafting
Many studies have reported on the lateral approach without bone grafting. To maintain the space without lowering the membrane after sinus lift, the area is packed with a resorbable membrane, titanium mesh, collagen sponge, platelet-rich plasma (PRP) gel, resorbable polymeric thermos-reversible gel (Poloxamer), reoxidized cellulose, or venous blood [11][12][13][14] . Several studies have reported that sinus bone formed an average height of 4.7-9.1 mm. To achieve stable and successful outcomes, the condition of the maxillary sinus should be healthy, and the sinus membrane must not be perforated dur-ing surgery. This technique is recommended in cases of residual bone height >5 mm, with new bone formation expected to be approximately 3 mm 15,16 .
2) Bone graft materials for sinus grafting Autogenous bone graft has the advantage of a shortened healing period. Without autogenous bone, the healing period can be as long as 8 months 17,18 . Use of autogenous endochondral bone (e.g., tibia and iliac bone) has become rare due to complications with donor site 19 . Recently, many clinicians have been harvesting block or particulated autogenous bone at an intraoral site (e.g., mandible, maxilla, and zygoma) and including other bone substitutes to increase the amount of harvested bone [20][21][22] .
Allogeneic, xenogeneic, and alloplastic bone substitute materials are used alone or in combination. To promote new bone formation, bone substitutes can be incorporated with platelet-rich fibrin (PRF), PRP, and recombinant human bone morphogenetic protein-2 (rhBMP-2). Xenogeneic bones are mainly manufactured from bovine, equine, and porcine species. Alloplastic bone substitutes such as hydroxyapatite (HA), calcium sulfate, beta-tricalcium phosphate (β-TCP), and bioactive glass have generally been used for sinus bone grafting. In recent years, most alloplastic bone products have been composed independent of any other products or in a specific ratio with HA and β-TCP [23][24][25][26][27][28] . Generally, any bone substitutes can be expected to have a successful outcome with sinus bone grafting if there is no sinus-related pathology, a healthy Schneiderian membrane, proper residual bone height, and no perforation during surgery [29][30][31] . Some studies have suggested that application of 0.25-1.00 mm of granular bone graft could enhance bone formation because of the intimate contact surface with the recipient bone wall 32 . However, Chackartchi et al. 33 reported that particle sizes of 1.00-2.00 mm and 0.25-1.00 mm exhibited similar results, with smaller-size particles showing greater resorption. Therefore, the authors recommended a mixture of small-and large-size particulated bone graft for large defects.

3) Simultaneous versus delayed implant placement
For primary stability of implants, simultaneous implant placement should be performed on residual bone height ≥3 mm, and delayed implant placement should be considered in areas of 1-2 mm of residual bone height. When considering these indications, simultaneous and delayed methods have shown similar successful outcomes 34 .

4) Lateral window formation
It is evident that the smaller is the size of the lateral window; the better is the bone formation. A smaller window has a high risk of sinus membrane perforation due to the narrow operating field. Active new bone formation can be achieved with clear membrane elevation to create an enclosed space with surrounding bone, similar to an extraction socket.
The trapdoor technique has been widely used to form the lateral window by fracturing the window inward and moving it upward with membrane elevation. However, the risk of membrane perforation increases in cases with sinus septum. Some clinicians prefer to reposition the window after membrane elevation with bone graft material 35 . Other clinicians have argued that removal of the window with a diamond bur or reamer is easier and safer for lifting the membrane. After removing the window, a barrier membrane should be used to cover the window defect to prevent soft tissue ingrowth 36 .

III. An Alternative Technique for Sinus Membrane Elevation
Maxillary tuberosity implants, short implants, and tilted implants have been introduced to avoid the maxillary sinus during implant therapy 37 . Chiapasco and Zaniboni 38 , however, noted that sinus membrane elevation with bone grafting is better suited for the final prosthesis as it allows the implant to be placed in an ideal position even though it is more invasive and involves higher complication risk.

IV. Healing After Sinus Bone Grafting
The healing period varies depending on several variables, including residual bone height, sinus cavity width, graft material, age of the patient, smoking history, and complications such as sinus membrane perforation and infection. In general, a healing period of 6-8 months is required between placement of the bone graft material and maturation of new bone 39 . It is clear that the higher is the residual bone from the sinus floor, the shorter is the healing period, the lower is the complication risk, and the higher is the success rate of bone grafting and implant placement 40 . Bone healing after sinus grafting is related to sinus width-the narrower is the width, the better is the prognosis 41 .

V. Complications
With regard to sinus membrane elevation surgery, some complications are inevitable even though prevention is the best method. Once complications occur, the clinician should acquaint themselves with the cause, explain the issue to the patient, and treat the complications accordingly. Cases of serious complications should be promptly referred to a related specialist 42 . During surgery, the most common complication is sinus membrane perforation, which could increase the risk of postoperative infection and failure of the graft and/or implant. Therefore, it is necessary to be aware of the various methods for closing perforations. After surgery, an infection is the most common complication, early diagnosis and treatment (antibiotics and incisional drainage) of which are very important for prevention of severe problems 43,44 . (Tables 2, 3) To minimize complications such as bleeding and sinus membrane perforation, the normal anatomical structures and pathological findings should be identified and diagnosed before surgery. Cooperation with an otorhinolaryngologist should be considered in cases of asymptomatic maxillary sinus lesion, nasomeatal patency, chronic maxillary sinusitis, mucous retention cyst, and nasal septum deviation 45 . To prevent arterial bleeding, the clinician should evaluate the vertical resorption of alveolar bone and the position of the posterior superior alveolar artery 46 . Sinus lateral wall thickness is very different for each individual. If the wall thickness is too thin or thick, there is a high possibility of perforation of the sinus membrane during formation of the bony window 47 . Asymptomatic mucous retention cyst and antral pseudocyst are not a contraindication. However, mucoceles with extensive and destructive aspects are contraindication for sinus membrane elevation. Sinus elevation is often difficult in cases with  mucous retention cyst or pseudocyst, where aspiration with a 21-gauge needle could be effective for sinus elevation, bone grafting, and implant placement 48 . Sinus septum has been reported in 16%-58% of patients and could increase risk of membrane perforation 49 . Normal sinus membrane thickness is 0.3-0.8 mm, and cilia cells remove various secretions and foreign substances formed in the maxillary sinus. If there is a lesion causing maxillary sinusitis or a history of sinus-related surgery, risk of postoperative complications such as maxillary sinusitis greatly increases because the cilia cells cannot function normally 50 . The most important factor to identify before surgery is maxillary ostium patency (osteomeatal patency), lack of which could cause postoperative maxillary sinusitis due to an issue with the maxillary sinus drainage system. In addition, risk of postoperative complications also increases in cases of nasal septum deviation and nasal mucosa inflammation or injury 51 .

Implant protrusion into the maxillary sinus
In an in vivo study of implant protrusion into the maxillary sinus, protrusion ≤2 mm was well covered with maxillary sinus mucosa, but protrusion >3 mm was not completely healed by the mucosa and may have resulted in a secondary infection 52 . Ragucci et al. 53 reported in a clinical study that protrusion <4 mm resulted in a significantly lower incidence of maxillary sinusitis. Therefore, implant protrusion <3 mm with sinus membrane perforation and loss of bone graft material should not be removed because of its ability to achieve osseointegration.

Failure of sinus bone graft
Anavi et al. 54 reported the poor prognosis of implants in cases of previous sinus-related treatment and re-operation after complications from sinus bone graft surgery. Regarding treatment of chronic oroantral fistula reconstruction or reoperation with sinus bone grafting, Kim and Kim 55 noted that sinus infection management should be considered with reconstruction of the sinus roof using a pedicled buccal fat pad and collagen membrane, oroantral fistula closure, and sinus bone graft using autogenous bone.

Residual bone height and sinus width
The crestal approach sinus lifting has fewer complications and higher success rates compared to lateral approach sinus lifting. This is attributed to the typical residual bone height greater than 5 mm when using the crestal approach 56 .

Sinus membrane elevation and implant placement
Simultaneous or delayed implant placement is determined by residual bone height. Therefore, direct comparison of prognosis is not appropriate between the two, and both have good prognoses if the timing of implant placement is determined based on all indications. The primary factor for implant success is primary stability 57 . Risk of implant failure greatly increases when implants are placed simultaneously with sinus bone graft and vertical ridge augmentation 58 .

Risk factors of implant failure in the maxillary posterior region
Sinus membrane elevation surgery is not directly related to implant failure. The main risk factors associated with implant failure are smoking, non-submerged implant, insufficient residual bone height, sinus membrane perforation, and postoperative maxillary sinusitis 59,60 . VII. Summary 1) Ideal bone graft materials have yet to be determined. However, a mixed bone graft (autogenous bone and other bone substitutes) has advantages in reducing the healing period and increasing bone density at the graft site over time compared with bone grafts using a certain material alone.
2) To prevent complications, the clinician should establish a careful preoperative examination and treatment plan based on the maxillary sinus structures. If lesions originating from the sinus are diagnosed before surgery, treatment should be performed with otolaryngology consultation.
3) Early detection and appropriate management are important to treat complications and prevent severe outcomes. 4) Several factors affect healing of maxillary sinus bone graft and prognosis of implants, the most important of which is residual bone height.