M axillary sinus augmentation

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1 406 SINUS IN RELATION TO COMPLICATIONS IN LATERAL WINDOW SINUS AUGMENTATION CHAN AND WANG Sinus Pathology and Anatomy in Relation to Complications in Lateral Window Sinus Augmentation Hsun-Liang Chan, DDS,* and Hom-Lay Wang, DDS, MS, PhD M axillary sinus augmentation via a lateral window approach (SALW) is an effective procedure to gain bone height for implant placement in an atrophic posterior maxilla. 1,2 This technique was first published by Boyne and James 3 in According to them, a bony window was made on the lateral sinus wall and a space was created between the Schneiderian membrane and the sinus walls, where a grafting material was placed. One key advantage of this approach is gaining direct access to the sinus. However, despite the high success rate, do occur. 4 The most frequently encountered surgical complication is perforation of the Schneiderian membrane. 5 Other include massive bleeding, infection, implant displacement into the sinus, etc. 1 More than often these are related to the sinus anatomy and preexisting antral pathologies. Knowledge about common sinus diseases and variations in sinus anatomy would greatly reduce the occurrence of these. Therefore, this article aimed at reviewing antral diseases and anatomy that might predispose to surgical in SALW. A treatment *Resident, Graduate Periodontics, School of Dentistry, University of Michigan, Ann Arbor, MI. Professor and Director, Graduate Periodontics, School of Dentistry, University of Michigan, Ann Arbor, MI. Reprint requests and correspondence to: Hom-Lay Wang, DDS, MS, PhD, 1011 North University Avenue, Ann Arbor, MI , Phone: (734) , Fax: (734) , homlay@umich.edu ISSN /11/ Implant Dentistry Volume 20 Number 6 Copyright 2011 by Lippincott Williams & Wilkins DOI: /ID.0b013e f79 Antral pathoses and anatomical variations increase the risk of surgical during a lateral window sinus augmentation procedure. Therefore, an understanding of maxillary sinus diseases and anatomies is imperative. In the first part of this article, common sinus diseases will be reviewed, which include acute/chronic rhinosinusitis, mucoceles, pseudocysts, retention cysts, and odontogenic diseases of the maxillary sinus. In addition, a treatment strategy will be proposed toward the management of proposal aiming at managing antral diseases was introduced. In addition, the management of these surgical was discussed. MAXILLARY SINUS DISEASES One of the main functions of the maxillary sinus is to humidify and filter the air inhaled in the nose. It is achieved by a layer of specialized respiratory epithelium, classified as ciliated pseudostratified columnar epithelium. 6 The main components of this epithelial layer are basal cells, goblet cells, and ciliated cells. 7 Basal cells own the ability to proliferate and differentiate into the other 2 cell types. Goblet cells are secretory cells that produce mucin. The ciliated cells are columnar epithelial cells that possess cilia. They function by moving the mucin toward the ostium, an opening connecting the maxillary sinus to the middle meatus in the nasal cavity. Blockage of this pathway could lead to accumulation of mucin and antral these antral diseases. In the second part, anatomical variations of the maxillary sinus, for example, the septum and artery that is in approximation to the osteotomy site will be discussed. Knowledge of diagnosing and managing sinus pathoses and anatomies could assist surgeons in reducing the incidence of sinus augmentation. (Implant Dent 2011;20: ) Key Words: maxillary sinus, sinus pathology, sinus anatomy, sinus augmentation, dental implants pressure in the sinus, eventually giving rising to symptoms, such as palpation pain around infraorbital region and headache. Many of the sinus diseases and some resulting from SALW are associated with the inability of the maxillary sinus to drain mucin. Sinus diseases and abnormities are prevalent (40%) in patients scheduled for sinus lift procedures and the presence of those conditions is significantly correlated with a history of indicative symptoms. 8 In addition, their presence might increase the difficulties in performing the surgery and the risk of developing postoperative As a result, maxillary sinus diseases should be recognized and managed with care before a sinus augmentation procedure. Many of them could be identified via a thorough medical and dental history evaluation, with a special focus on any signs and symptoms that might suggest a concern in the sinus. 8 A careful

2 IMPLANT DENTISTRY / VOLUME 20, NUMBER Table 1. Common Maxillary Sinus Diseases and Their Managements for SALW Diagnosis Disease Clinical Symptoms Radiographic Findings Etiology Histological Findings Management ARS CRS Duration up to 4 wk Anterior or posterior mucopurulent drainage Nasal congestion Facial pain/pressure Decreased sense of smell Duration longer than 8 12 wk Anterior or posterior mucopurulent drainage Nasal congestion Facial pain/pressure Decreased sense of smell Opacification or air-fluid level Bacterial/viral/fungal infection Infiltration of neutrophils and macrophages Thickening of the sinus lining more or less in even width Pseudocyst Usually none Prevalence: 1.5% 10% Dome-shaped radiopacity Commonly located on the floor of the sinus Retention cyst Mucocele Usually none Very rare, more commonly found in frontal sinuses May include headache, diplopia, visual impairment, and/or nasal obstruction Mostly too small to be detected Commonly found around ostium Initial stage: cloudy sinus cavity Later stage: thinner sinus wall Mainly inflammation from low-grade infection or allergy Focal accumulation of inflammatory exudate Blockage and dilatation of ducts of the seromucinous glands Blockage of ostium due to trauma or other diseases Infiltration of lymphocytes, plasma cells, and macrophages No epithelial lining Exudates accumulation Inflammatory infiltration With epithelial lining Mucin accumulation With epithelial lining (typical respiratory epithelium or squamous metaplasia) ENT consultation ENT consultation: with symptoms or thick membrane 1/3 sinus height Otherwise, proceed with SALW ENT consultation: with symptoms or closer to medial wall Otherwise, enucleation via lateral window Proceed with SALW ENT consultation dental and periodontal examination especially for those teeth that are in the vicinity of the sinus should be executed to rule out any odontogenic lesions. Common sinus diseases that might interfere with the performance of SALW include acute/chronic rhinosinusitis, sinusitis of odontogenic origin, odontogenic cysts, pseudocysts, mucoceles, and retention cysts. The clinical and radiographic features of each of them was discussed in below and summarized in Table 1. Rhinosinusitis The term rhinosinusitis has replaced sinusitis because of the close interrelationship between the 2 diseases. 12 Rhinosinusitis is defined as inflammation of the nose and paranasal sinuses. 13 Acute rhinosinusitis (ARS) is usually infectious and lasts up to 4 weeks, whereas chronic rhinosinusitis (CRS) is more inflammatory and has a minimal duration of either 8 or 12 weeks. 12 Apart from their differences in the duration and pathogenesis, symptoms associated with the 2 diseases are similar. More than 2 of the following symptoms are required to establish the diagnosis for both ARS and CRS: (1) anterior or posterior mucopurulent drainage, (2) nasal congestion, (3) facial/pain pressure, and (4) decreased sense of smell. 13 In addition, CRS may be diagnosed with objective methods, for example, a rhinoscopic or radiographic examination with a preference for computed tomography (CT). CRS can be further categorized into 3 subtypes with distinct but overlapping clinical characteristics: CRS without nasal polyposis, CRS with nasal polyposis, and allergic fungal rhinosinusitis. 13 Radiographically, ARS might present with an airfluid interface and CRS is associated with thickening of the sinus lining and radiopacity in the sinus. 14 Odontogenic Sinus Diseases Maxillary sinusitis of odontogenic origin account for approximately one tenth of total maxillary sinus diseases. 15 Common dental diseases that can cause sinusitis include periapical infection, periodontal disease, and perforation of the antral mucosa during tooth extraction. Other dental-related maxillary diseases are odontogenic cysts, for example, the radicular and dentigerous cyst. 16 These earlier mentioned diseases might serve as a reservoir for microbes, which might contaminate the grafting material and dental implants resulting in treatment failure if left untreated. As a result, before planning a SALW, a thorough dental examination is required to rule out the earlier mentioned diseases. Pseudocyst, Retention Cyst, and Mucocele A pseudocyst, as the name implies, is not a true cyst (without epithelium lining) while a retention cyst is. 17,18 A pseudocyst is believed to be an accumulation of inflammatory exudates between the bony wall and periosteum. A retention cyst is formed when mucin is allowed to accumulate in a dilated seromucous duct that is blocked. Radiographically, a pseudocyst is characterized by its domeshaped radiopaque structure and is commonly found on the floor of the maxillary sinus. The prevalence of pseudocysts ranges from 7.3% 19 to 14% 20 on radiographs. On the other hand, a retention cyst is not readily seen on the x-ray because it is too small and if found, it is often around the ostium. Under normal conditions, both lesions are usually asymptomatic and require no treatment. However, when a SALW is planned, a pseudocyst might complicate procedures and risk the development of surgical. A mucocele, on the contrary, is invasive in nature. The pressure generated from the fluid in the mucocele

3 408 SINUS IN RELATION TO COMPLICATIONS IN LATERAL WINDOW SINUS AUGMENTATION CHAN AND WANG may resorb the bony walls of the sinus. It is also much larger in size and may fill the entire sinus thus creating sinus symptoms. The blockage of the ostium is believed to be responsible for this pathosis. 18 Fig. 1. A proposed treatment strategy for common antral diseases before SALW. Fig. 2. A proposed treatment strategy for common antral diseases during and after SALW. Management of Maxillary Sinus Diseases A proposed treatment strategy is summarized in Figures 1 and 2 for patients who are diagnosed with maxillary sinus diseases and at the same time planned for SALW. From a medicolegal and preventive standpoint, dental surgeons should collaborate closely with an otorhinolaryngologist in managing maxillary sinus diseases. The general goal is to alleviate sinusrelated symptoms, eliminate the lesion and regain sinus membrane health before sinus augmentation. The procedures to achieve this goal may include a nonsurgical or a surgical approach or a combination of both. More specifically, a mucocele should be removed first because of its aggressive nature and large size. If diagnosed during the sinus augmentation surgery, the pathologic tissue can be removed with a Caudwll-Luc procedure and the augmentation procedure is aborted. 21 CRS should be referred, when it is symptomatic or if the sinus membrane thickness is greater than one third of the height of the sinus. For maxillary sinus diseases of odontogenic origin, the lesion should resolve itself after dental procedures, which might include endodontic therapy, periodontal treatment, and extraction. 22 The retention cyst is often small, symptomless, and near the ostium. Therefore, no specific treatment is warranted. The management of the pseudocyst is somewhat controversial and different approaches have been reported in several case reports. 19,21,23,24 Sinus augmentation was performed with the presence of a pseudocyst in 2 cases. 23 One case developed an abscess postoperatively and was controlled by antibiotics, after which the implants had been followed for 7 months without further. In another study, 19 8 cases with a pseudocyst were treated with a standard SALW. acute sinusitis and membrane perforation occurred in one and 2 cases, respectively. The authors concluded that a sinus lift procedure can be performed safely even when a pseudocyst is present; however, in cases of unclear diagnosis or if the cyst is large, further evaluation is recommended. On the other hand, Lin et al 24 suggested removing the pseudocyst routinely before SALW. In their case report, a 5 mm round window was created on the lateral wall of the sinus, from where the cyst was enucleated. The SALW was performed 3 months after the removal of the cyst. The authors claimed that this procedure allowed for elimination of the cyst and shortening of treatment time (a Caldwell-Luc procedure or an endoscopic surgery for cyst removal normally requires 6 months healing). The pseudocyst should be removed before sinus augmentation because of the following reasons. First, histopathologic examination can be performed to rule out any possible malignancy. Second, the healed sinus membrane after elimination of the cyst would be healthier, and thus facilitate the sinus elevation procedure. Third, the long-term effect of the pseudocyst on the grafting material and implants are not known. Whether the enucleation procedure is referred depends on

4 IMPLANT DENTISTRY / VOLUME 20, NUMBER Table 2. Summary of Articles Studying the Prevalence, Size, Location, and Orientation of Maxillary Septa N (Subjects) Methods Dental Status Septum Definition Prevalence/Sinus Location Direction Size (mm) Ulm et al Cadavers Edentulous 2.5 mm 31.7 Premolars: 73.3; 1st molar: 19.9; 2nd molar: 6.6 Krennmair 165 Clinical et al 27 examination and CT Both NA Clinical: 27.7; CT: 16; dentate: 13.2; edentulous: 26.8 Kim et al CT Edentulous 2.5 mm Total: 26.5; edentulous: 31.8; dentate: 22.6 Shibli et al Panoramic radiographs NA 7.9 NA NA 6.8 (clinical), 8.1 (CT) 2nd premolar: 25.4; 1st and 2nd molars: 50.8; 3rd molar: 23.7 Edentulous NA 21.6 NA NA NA Neugebauer et al CBCT Both NA st molar: 31.6; 2nd molar : 27.6; 2nd premolar: 17.1 Rosano 30 Cadavers Edentulous 3 mm nd premolar-1st molar: et al 30 30; 1st-2nd molar: 40; distal to 3rd molar: 30 Park et al CT Edentulous NA st and 2nd premolar: 22.5; 1st and 2nd molar: 45.9; 3rd molar: 31.5 CT, computed tomography; CBCT, cone-beam computed tomography. NA Medial-lateral: 74.7; anterior-posterior: 25.3 Medial-lateral: 30; anterior-posterior: 70 Medial-lateral: 96.3; anterior-posterior: (lateral), 3.55 (middle), 5.46 (medial) 7.3 (mesiodistal); 11.7 (anterior-posterior) the presence of symptoms and the location of the cyst. When the cyst is symptomatic or is medially located, an endoscopic surgery might be indicated and therefore should be referred to an otorhinolaryngologist. Intraoperatively, the outcome of sinus augmentation is influenced by several factors, such as the presence of a membrane perforation, size of the perforation, presence of unexpected infection, and the ability to clean the infection. The presence of pus/exudate requires a debridement procedure and if the debridement could not be completed, the sinus augmentation should be aborted. If the size of the perforation is larger than 10 mm, the procedure generally should be terminated too. ly, decongestant medications and antibiotics should be prescribed and the patients should be informed about the possibility of having higher incidence of developing. VARIATIONS IN THE ANATOMY COULD PREDISPOSE TO COMPLICATIONS Sinus Septum and Membrane Perforation The internal structures of the maxillary sinus have been described a hundred years ago. 25 It was not until the introduction of the SALW did these internal anatomies regain attention, and in particular, the septum. Articles related to the maxillary sinus septum are summarized in Table 2. A septum is a bony projection with various sizes, locations, and orientations, most commonly arising from the floor of the maxillary sinus. The prevalence of the septum ranges from 16% to 33.3%, depending on ethnicity, methods used to identify a septum and the dentate status, etc The septum has been found more commonly in edentulous than dentate status because of the presence of the secondary septum. 27 It was hypothesized that after tooth loss, a selective bony resorption of the sinus floor resulted in areas of protrusion and depression. The protrusive bony spike formed the secondary septum, in comparison with the primary septum, which was formed along with the development of the maxillary sinus. This theory was further supported by the fact that a primary septum is higher in size and may split a sinus into 2 compartments, whereas a secondary septum is considerably shorter. The septum was most commonly found at the molar area, 26,28 30 where a sinus augmentation procedure is commonly performed. The height of the septum varies greatly among studies, ranging from to 11.7 mm. 28 A septum can be found more commonly in a mediolateral direction, partially separating the sinus into an anterior and posterior compartment, 28,29 although a septum in the transverse and sagittal directions could also be found. To summarize, a septum, varying in size, location, and orientation is commonly present in the maxillary sinus. Its presence may increase the risk of a sinus membrane perforation during the surgery. A membrane perforation is the most commonly encountered complication. 1 The mean prevalence of sinus perforation during sinus elevation procedures is 19.5%, with a range of 0% to 58.3%. 1 The highest perforation rate is associated with single tooth replacement. 27 It might be possible that the limited access had significantly increased the perforation rate. Whether membrane perforation incurs more postoperative and higher implant failure rate is debatable. Barone et al 33 found that the use of an onlay graft and/or smoking and not the membrane perforation is associated with higher postoperative infection rate. Becker et al 34 also suggested that with proper treatment, a perforation of the membrane did not elevate the risk for implant loss, infection, or displacement of grafting material. Schwartz-Arad et al 5 concluded that a membrane perforation significantly increased postoperative but it did not result in more implant failures. On the other hand, Cho-Lee et al 35 found that the implant survival rate was lower (81%) when surgical, membrane exposure or postoperative sinusitis occurred, compared with no (97.6%).

5 410 SINUS IN RELATION TO COMPLICATIONS IN LATERAL WINDOW SINUS AUGMENTATION CHAN AND WANG Table 3. Summary on Managements of Sinus Membrane Perforation Management by the Size of the Perforation References Total No. of Augmentations Total No. of Implants Perforation Rate Implant Placement Timing Perforation Size (mm) Shlomi et al Staged No. of perforations 20 Repair technique DFDLB sheet 0 rate 90 (NSS from NP group) Ardekian et al Simultaneous No. of perforations Repair technique Collagen membrane 5.7 (0 in NP group) 94.4 (NSS from NP group) rate Becker et al Both No. of perforations Repair technique rate Collagen membrane Collagen membrane suture 4.8 (1 in NP group) 98 (NSS from NP group) Discontinue the procedure Hernandez-Alfaro Simultaneous No. of perforations et al 37 Repair technique Suturing, or resorbable collagen membrane Lamellar bone resorbable collagen membrane Lamellar bone, lamellar bone buccal fat pad, or bone block graft rate NSS, not statistically significant; NP, nonperforation; DFDLB, demineralized freeze dried human lamina bone. Regardless of the controversies in the potential effect of membrane perforation on postoperative and implant failure, this intraoperative complication absolutely increase surgical difficulty and lengthen surgical time. It is, therefore, preferable to prevent the occurrence of a membrane perforation. Of equal importance is the management of a perforation once identified during the procedure. Management of Sinus Membrane Perforation Table 3 summarized methods used to repair a membrane perforation of different sizes. A perforation 5 mm is generally repaired with a collagen membrane alone or sutures. 34,36,37 A perforation size between 5 and 10 mm might be treated with a collagen membrane alone, 36 in combination with sutures 34 or lamina bone harvested from the lateral wall after osteotomy. 37 It might be corrected with a demineralized freeze-dried human lamellar bone sheet. 38 Attempts were made to repair a larger perforation ( 10 mm), including a demineralized freeze-dried human lamellar bone sheet, 38 lamina bone alone, combined with buccal fad pad, or the use of a block graft. 37 On the contrary, it was suggested to abandon the surgery. 34 From these clinical evidences, small to medium perforations might be repaired, after which the augmentation procedure could be completed without jeopardizing implant survival rate. However, when a large perforation occurs, the surgery should be terminated because lower implant survival rate was found in cases with a 10 mm perforation and a repair was attempted. 37 Distributions of Blood Vessels and Massive Hemorrhage Accidently injuring the blood vessels in the maxillary sinus might cause massive hemorrhage during an augmentation surgery. Therefore, it is important to understand the distributions and variations of these arteries. The artery that is located on the lateral wall where an osteotomy will be performed is especially important. It is the anastomosis of the posterior superior alveolar artery and infraorbital artery. In cadaver studies, this anastomosis could always be found 39,40 ; however, from CT images only 50% to 60% could be identified Its location in relation to the alveolar crest was on average 11.25, , , 42 and 19 mm. 39 Because of its location, it was estimated that 20% of normally positioned lateral window osteotomies might come across this artery, potentially causing major bleeding. 41 The use of a piezoelectric machine for osteotomy might preserve the integrity of this artery because it only cuts hard tissue. 43 With regard to its relationship with the lateral sinus bony wall, it was found to be intraosseous 39,41 or partially intraosseous. 40,42 If it is located between the interior side of the bony wall and the Schneiderian membrane (partially intraosseous), care should also be taken not to tear it when ele-

6 IMPLANT DENTISTRY / VOLUME 20, NUMBER vating the membrane. The diameter of this artery was 1 mm in 55.3%, 1 to 2 mm in 40.4%, and 2 to 3 mm in 4.3% of cases. 40 When a large diameter blood vessel (3 mm) is encountered, it may be wise to ligate it to prevent massive bleeding. 44 Location of the Ostium and Sinus Obliteration The ostium is located 40 mm above the antral floor. 45 A case was reported for a patient who complained about frequent headache, sinus congestion, and discharge after a sinus augmentation procedure. 46 CT revealed that the grafting material occupied 80% of the maxillary sinus and was just below the ostium. It was possible that the grafting material had blocked the normal fluid movement in the maxillary sinus and symptoms developed. Therefore, maxillary sinus should not be overpacked. Migration of the Implant Displacement of implant into sinus was reported sporadically in the literature. 47,48 the incidence of this complication is currently unknown and believed to be rare. The timing of its occurrence varies from several days after implant placement, 49 at abutment connection surgery, 50 or even several years after function. 51 The exact cause is not clear; however, 3 essential conditions must be present for this unfortunate incident to occur, these are a lack of osseointegration, membrane perforation, and a pushing force on the implant toward sinus. It is generally agreed that once the displacement is diagnosed, the implant should be removed as early as possible. Three main rescue therapies have been discussed and the treatment protocol has been developed, which comprises of intraoral approach (modified Caldwell-Luc procedure), functional endoscopic sinus surgery (FESS), and the combination of both. 47 According to their protocol, an intraoral approach is chosen when no symptoms of sinusitis are present and the ostium is patent, whereas a FESS is selected when there is obstruction of maxillary ostium without oroantral communications. The FESS is combined with an intraoral approach when sinusitis, obstruction of the ostium, and oroantral communications are all present. A high success rate (26 of 27 patients recovered completely) following this protocol suggests that this is an effective approach. Nevertheless, the best way is probably to prevent this complication from happening. Because of rare occurrence, it was difficult to identify the risk factors. Possible predisposing factors include inadequate residual ridge height, poor bone quality, and simultaneous implant placement with sinus augmentation. CONCLUSIONS The occurrence of surgical during SALW is most likely related to the presence of maxillary sinus pathoses and anatomical variations. Management strategies for antral diseases before, during and after the augmentation procedure were proposed. In addition, maxillary sinus anatomies, in particular the maxillary septum, ostium, and artery in the vicinity of the osteotomy site and their clinical significance were discussed. Correct diagnosis and management of sinus diseases and the knowledge of sinus anatomies could greatly reduce the incidence of surgical. DISCLOSURE The authors claim to have no financial interest in any company or any of the products mentioned in this article. REFERENCES 1. Pjetursson BE, Tan WC, Zwahlen M, et al. 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