Lateral window technique: A focus review

The posterior alveolar bone region of the maxilla has, in more than 40% of the cases, a height inferior to 4 mm, thus making rehabilitation with implants a clinical challenge. This focus literature review was carried out through an exhaustive literature search in PubMed, ScienceDirect, LILACS, Web of Science, Scielo and Cochrane Library. The aim was to illustrate and analyse various factors that should be accounted for while applying the maxillary sinus elevation technique. The lateral osteotomy technique is carefully described including its indications, complications, contraindications, as well as, different factors to take into account, such as the use of electric piezo, graft materials, membranes and the expected success rates.


I N TRODUC T ION
Placing dental implants in the posterior jaw is a challenge due to the presence of the maxillary sinus, especially when bone availability is limited.In 40% of these sites, the bone height is 4 mm or less 1 and, in cases of extreme bone resorption, it can lead to cases of bone height apically to the maxillary sinus smaller than 1 mm. 2 This two-way bone resorption that occurs in the posterior region of the maxilla is due to the centripetal loss of the alveolar bone and the pneumatization of the sinus, together with histophysiological bone characteristics, such as a very medullary and little cortical bone. 3,4One of the solutions is the regeneration of bone in the posterior maxilla through surgery using the lateral window of the maxillary sinus, the technique with the greatest scientific documentation. 1,5,6However, besides being a complex technique, its use requires a careful screening of patients and a previous risk-benefit analysis that considers the systemic pathologies and behavioural habits of the patient, 5 such as smoking or oral hygiene.][9] The purpose of this literature review is to describe the elevation of the maxillary sinus procedure using the lateral window technique, as well as to gather current data on its indications, limitations, success rates and post-intervention complications.

M ATER I A L S A N D M ETHODS
The scientific articles used in this focus literature review were screened between October 2019 and December 2019 by two research (FC and RFA).The set of initial papers were collected from the electronic databases PubMed, ScienceDirect, LILACS, Web of Science, Scielo and Cochrane Library.Electronic search was limited to English, Portuguese, Spanish, Italian and French.The keywords and/or MeSH terms 'sinus floor augmentation', 'sinus lift' and 'Sinus Floor Augmentation (Mesh) AND Humans (Mesh).' lead to 5697 articles.After elimination of duplicates and title/abstract reading, the number of articles went down to 278 and, after full-text reading, 103 papers were selected to be included in this focus review.Papers targeting animal studies, case report and case series were excluded, whereas those aiming two-stage lateral window technique complications, contraindications, as well as different factors to take into account, such as the use of electric piezo, graft materials, membranes and the expected success rates were included in this review.

W I N DOW TECH N IQU E
The lateral window technique or lateral osteotomy technique, also known as sinus lift or Caldwell-Luc technique, was first described and presented in an oral communication by Tatum H. Jr. in 1977 and only published by him in 1986, 10 being first published by Boyne and James in 1980. 11It is presented as the technique for sinus elevation with greater scientific documentation 1,5,6 and is a predictable, a safe procedure, with a low rate of complications and high rates of implant success, regardless of residual bone height. 124][15][16] The technique can be described as follows: Osteotomy just-antero-superior to the zygomatic abutment, followed by a spherical drill bit No. 6 or No. 8 at 16,000 rpm, or piezoelectric instrument.It is important to consider that the size of the lateral osteotomy varies according to the prosthetic area to be replaced, depending on the limiting anatomical factors and the initial surgical planning.
A window is made in which the 'hinge' is in a cranial position, 'the window is opened' into the sinus and, at the same time, it is possible with this maneuver to start lifting the Schneider membrane.Then, the space formed with the bone graft is filled, the opening is covered with a membrane and sutured.Figure 1 presents the different steps to perform this technique.
Different factors that need to be taken into account will be described in the next chapters of this paper, such as technique complications, contraindications, the use of electric piezo or rotating instruments, as well as the type of graft materials, the placement of a membrane on the lateral wall and the expected success rates.

Indications
This technique is mainly indicated when the bone height below the maxillary sinus varies between 1 and 5 mm in height, for subsequent placement of standard-length dental implants, allowing a median implant survival rate of 95.5% (61.2%-100%). 17n initial height of 5 mm is considered the threshold for simultaneous placement of the implants together with the elevation of the maxillary sinus using the lateral technique. 17owever, it is possible to place the implants simultaneously in ridges with an initial height ≥1 mm. 1,18The decision to perform a simultaneous (lateral osteotomy plus implant placement) or staggered (first lateral osteotomy surgery and a second implant placement surgery) should be based on an individual assessment of risk factors assessing whether it is possible to achieve primary implant stability, which is a sine qua non condition for success.For this assessment, it is crucial to evaluate also the quantity and quality of the implant, bone availability. 1,18

Contraindications
The prior evaluation of the patients' pathologies is extremely important, considering that it can interfere with the regenerative capacity and increase the rates of complications.A thick Schneider membrane or large mucous cysts can increase the risk or obstruction of the ostium or sinusitis after elevation of the maxillary sinus. 19Some authors 13,14,20,21 consider as absolute contraindications to implant placement in the posterior maxilla: chemotherapy and radiotherapy to treat a recent or impending tumour, drug or alcohol dependence and blood dyscrasias that directly affect the bone metabolism, intravenous bisphosphates, tumoural pathologies of the maxillary sinuses and destructive sinus surgery.[22][23]

Preoperative
][25] CT also allows to perform a virtual pre-surgical planning, 26 as well as, to verify the location of the upper, anterior and posterior alveolar canals, including their anastomosis. 27nother important factor, that can be analysed, is the height at which the osteotomy should be performed, to achieve optimal maxillary sinus window. 14f there is evidence of acute or chronic sinusitis or other pathologies, the patient must be referred to an otorhinolaryngologist. 1,21,28Preoperative sinusitis is a positive predictive factor for the development of acute postoperative sinusitis 1 The use of chlorhexidine mouthwash prior to surgical interventions is a preventive measure to reduce the risk of infections ensuring the aseptic control of the surgical field. 13,14,29The additional use of antibiotics is also advisable in order to avoid infections and graft reductions due to the presence of undesired bacteria. 20,27
Anatomically, the main impacting factors for this technique are the septa, and the infra-orbital neuro-vascular structures.
To observe the path of the posterior alveolar superior artery and anastomosis in the intra and extra-bony branches, a CT or CBCT are essential to analyse the height of the passage from the basal bone, the diameter and the course, avoiding haemorrhagic complications due to lacerations in the branches of the maxillary artery or intraosseous vascular channel, in the lateral antrum wall of the maxillary sinus, which can be found in more than 50% of cases. 28,44The performance of lateral osteotomy with piezoelectric instruments that selectively cut the bone without additional soft tissue injuries to the detriment of rotary drills, helps to reduce the risk. 44nother complication is the leakage of the graft material into the maxillary sinus or the movement of the membrane that causes an ostium obstruction, preventing the drainage of sinus mucus which increases the risk of infection. 21owever, despite these potential complications, the risk of infection is low and less than 5%. 21verfilling the sinus can also result in blockage of the ostium, especially if inflammation of the membrane or the presence of a thickened sinus mucosa exists.The elevated Schneiderian membrane increases in thickness after surgery, reaching more than 6 mm after 7 days, taking months until the membrane thickness returns to the initial thickness, and this recovery time is directly correlated with the extension of the maxillary sinus elevation. 45n case of an ostium block and consequently a postoperative infection without initial resolution, the re-entry and removal of a portion of the graft and the change in the antibiotic protocol may be appropriate. 21he use of filters to collect autografts translates into an increased risk of infection located in the maxillary sinus (13.0% vs. 4.0%). 29In the study by Barone et al. in 2006 41 a greater likelihood of maxillary sinus infections was also observed in smoking patients.
Sinus infections after a bone graft can cause serious complications due to the proximity of the maxillary sinus with various vital structures (example: brain, cavernous sinus), and can cause sinusitis, orbital cellulitis, meningitis, osteomyelitis, thrombosis of the cavernous sinus, among others. 13ostoperative complications occur less frequently (3.6%), sinus infections can be avoided since they tend to occur mainly in previously unhealthy sinus, and should be detected in preoperative exams. 5,24cute postoperative sinusitis occurs in approximately 3%-20% of sinus elevation procedures and represents the most common short-term complication. 13,21,46Usually, the infection starts more than a week after surgery and resolves with an antibiotic, the risk proportionally increases the amount of graft used. 21,46,47uturing stripping with an incision opening is an uncommon postoperative risk, since the site of the lateral osteotomy is at least 5 mm from the bone crest. 21The consequences of opening the incision can be delayed healing, leakage of graft material into the oral cavity and increased risk of infection.If a portion of the non-resorbable membrane is exposed, the area must be cleaned at least twice a day with a mouthwash of chlorhexidine and, if it does not close after two months, a new surgery must be performed in order to remove the membrane and reconnect the tissues. 21mplications -perforations in the Schneider membrane Regarding the intraoperative complications, the most common during maxillary sinus elevation surgery due to the lateral osteotomy is the tearing of the Schneider membrane.It can occur due to pre-existing perforation, during lateral osteotomy or when the membrane is detached and elevated, which is not influenced by age or gender. 21,37The maintenance of the Schneider membrane is desirable to guarantee better vascularisation, graft stability and environmental conditions for the maturation of the inserted bone graft materials. 4848][49][50] However, there are also studies in the literature that do not support the negative effects of membrane perforation, such as graft loss and compromised final result, increased postoperative complications, or even decreased implant survival rate. 22,35,51[54] The width of the maxillary sinus is a relevant variable.The risk of perforation is higher (62.5%) when the membrane is elevated in the anterior and narrow regions and where the lateral and median walls of the sinus have an angle of less than 30°.This risk decreases to 28.6% when it approaches the medial area (30º-60º) and becomes null when it reaches the posterior region (>60º). 31he septa are the most common bone anatomical variant in the maxillary sinus and one of the biggest causes for perforation of the Schneider membrane, varying between 13% and 59.7%. 21,33,52urgically, the approach may vary depending on the location, size and number of septa present.In the presence of a septum, the design of the lateral osteotomy window should be modified in order to provide better access to the surgical instruments and try to include them in order to minimise the risk of perforation and improve the view of the surgical site when the membrane is raised. 14,21,28,31he thickness of Schneider's membrane is also one of the relevant variables for the probability of perforation and it tends, on average, to increase from the region of the first premolar until reaching its maximum thickness in the region of the second molar. 32The thickness of the Schneider membrane may be relevant to the risk of perforation.For example, the retrospective study by Lum et al. 2017 55 reports a perforation rate of 28.1% and found an association between membrane perforation and the presence of a thinner membrane, which is directly related to a lower height bone.On the other hand, Insua et al. 53 describes that the thickness between 1 mm and 1.5 mm of the membrane presents the greatest tendency for perforation.The same authors suggest that the increased rate of perforation of the membrane may be more related to the changes induced by inflammatory conditions, which promote a change in thickness and epithelium in that membrane. 53A thicker membrane, but with epithelial damage and chronic inflammation, may be more prone to perforation than a thinner, but healthy membrane with an intact epithelial layer. 53Patients with periodontal disease and smoking patients are more likely to have a thicker membrane. 51he perforation of Schneider's membrane does not appear to be significant in the mean of vital bone and in the survival of implants.Froum et al. 2013 56 registered 26.3% ±6.3% (mean ± standard deviation) in case of membrane perforation (and its repair) and 19.1% ± 6.3% when not perforated, not being these differences translated in a statistically significant way in the survival of the implants (95.5% when perforated the membrane vs.100% when not perforated).
The treatment of a Schneider membrane perforation consists of providing a stable coverage of the perforated area to contain the graft material. 31The first step in treating a perforation is to raise the surrounding membrane to reduce the stress on the region and to prevent further perforation.Subsequently, the size and position of the area must be assessed. 31If the perforation is small, there is the hypothesis that it self-regenerates due to the formation of a clot or leaflet of the Schneider membrane. 31If the perforation is relevant (>5 mm), it must be covered by a stable resorbable membrane that serves as a barrier between the sinus and the graft material. 31In case the perforation is extensive (>10 mm), it is recommended to use a large stabilised resorbable membrane that extends over the side wall. 31When using a resorbable membrane to seal the perforation, it must overlap the margins over 5 mm in diameter around the perforation. 21After sealing the perforation, the surgical procedure can be completed in the same way as in cases where a perforation has not occurred. 21he repetition of the surgical procedure can be considered, and the second procedure should be performed never before 6 to 8 weeks after the first surgical attempt. 14

Piezo versus rotating instruments
The use of the piezoelectric instrument, in front of the rotary instruments to perform lateral osteotomy of access to the maxillary sinus, is justified by the fact that the possibility of accidental perforation of the Schneider membrane is lower, since the piezoelectric only cuts hard tissues.8][59][60][61][62] The biggest disadvantage of the piezoelectric is the delay in performing the osteotomy, which can lead to bone heating. 22,57,58,63This time difference is on average 2 minutes (3 minutes for rotary instruments vs. 5 minutes for piezoelectric). 59On the other hand, two studies 62,64 found no statistically significant differences in terms of risks, traumas or perforations of the Schneider membrane.In the systematic review by Geminiani et al. 2017, 63 intraoperative risks, including rupture of the membrane, are not reduced using piezoelectric surgery, sonic surgery, osteotome or trephine, when compared with the conventional surgical technique.The 2007 study by Wallace et al. 60 reports a 27% reduction in the occurrence of Schneider membrane perforations when using piezoelectric compared to conventional rotary instruments.

Graft materials and growth factors
The graft materials used in the lateral maxillary sinus osteotomy technique described in the literature include particulate or block autograft, particulate lyophilized demineralised frozen allograft, xenografts, non-resorbable alloplastic hydroxyapatites and combination with BMP-2, among others. 1,65he first authors to describe the use of autograft and its application to the maxillary sinus were Wood and Moore 66 in 1988.In terms of bone substitute, tricalcium phosphate was the first bone substitute to be used successfully in sinus elevation by Tatum 67 in 1986.Currently, materials from nonautologous grafts or in combination with autografts are well documented in the literature, with no statistically significant differences in clinical results and implant survival rate compared to autografts. 24,65,68owever, the use of some bone regeneration materials can lead to inflammatory reactions or infections. 43For example, in the 2017 clinical trial by Kolerman et al., 69 in which the maxillary sinuses were grafted with an alloplastic graft (biphasic calcium phosphate), evidence of a mild and chronic inflammatory infiltration was observed, which mainly included lymphocytes and multinucleated giant cells.Biomaterials such as collagen xenograft of porcine origin the maxillary sinus have a lower risk of infection or inflammation. 43,70n histomorphometric analyses, defined as the goldstandard for estimating the amount of new bone formation in the grafted sites and verifying differences in the use of different biomaterials, 31,71 there are large variations in the amount of vital bone (5% at 60%), according to the different types of graft, which histologically influences the quality of the bone obtained. 1he osteogenic properties of the autograft and the xenograft are different, allowing a reabsorption/apposition of new bone that tends to be greater in the xenograft. 70,72When bone substitutes are used, the growth of the newly formed bone is delayed by the absence of osteogenic cells and their osteogenic growth factors, which lead to the delay in placing the implants and loading them. 14he slow reabsorption when using bovine xenografts is its greatest disadvantage described in the literature, in many cases it is incomplete even after many years, which means that a considered graft volume is not replaced by new vital bone. 73For this reason, other types of xenografts that have a great capacity for resorption and deposition of new bone, such as collagen xenograft of porcine origin, may be part of the advancement in regenerative techniques of maxillary sinus elevation by lateral osteotomy 72 The ability to resorb and deposit new bone from collagen xenograft of porcine origin is a result of the influence of collagen on cellular and molecular activity, inducing the adhesion of osteoclasts to the surface of the biomaterial 72,74 Cordella et al. (2016) 71 observed that the average amount of new bone formed, and residual bone graft was not significantly different for bovine xenograft and porcine xenograft, when compared with alloplastic biomaterials.In comparison, for the mixture of xenograft and autograft with the mixture of autograft and allograft, the latter shows a faster turnover and a faster decrease in biological action after 6 months. 75he use of autograft shows results similar to the use of other bone substitutes, but it has the great advantage of rapid bone maturation due to the presence of osteogenic cells and osteogenic growth factors, 17,40,71 making it possible to perform the second early surgical phase. 24he autograft is almost completely absorbed within six months, as evidenced by Starch-Jensen et al. 40 who found a significantly higher proportion of mineralised bone during the early healing phase, when the autograft was used as a graft material (compared to several bone substitutes used alone or in combination with autologous bone).However, after a healing period of more than 9 months, no statistically significant differences were found between the different treatment modalities. 40nalysis of the literature does not allow us to glimpse scientific evidence to prove that the use of platelet-rich plasma (PRP) or platelet-rich fibrin (PRF) in sinus lift surgery has positive improvements in bone graft regeneration, especially in terms of clinical results and effectiveness.7][78] In the case of the use of cellular techniques of regenerative medicine, it is observed that the use of these promoters does not bring additional advantages 79 The use of recombinant human growth factors is hitherto limited almost exclusively to recombinant human PDGF BB homodimer (rhPDGF-BB) and recombinant human bone morphogenetic protein 2 and 7 (rhBMPs2 and 7 and growth differentiation factor 5), and there is no evidence to support their use in maxillary sinus elevation procedures. 80owever, the use of rhBMPs-2 can improve and accelerate the maturation process. 81he patient's age is also a variable that affects bone formation.However, Wolf M.'s 2014 82 clinical trial did not show significant differences between age groups (group 1-41 and 52 years old; group 2-66 and 71 years old).
It is possible to infer that bone substitute materials are as effective as autograft, when used alone or in combination with autologous bone, with an equivalent implant survival rate over an observation period of 5 years. 40,83The use of bone substitutes is associated with advantages for the patient, which include reduced morbidity, a less invasive procedure and shorter surgical time. 40

Postoperative radiological assessment
5][86] The use of 2D radiographs (orthopantomography and periapical radiographs) allows observing bone remineralisation. 879][90][91][92] The average vertical gains observed in the 2016 Bayesian network study by Merli et al. 93 were 7.44 ± 1.95 mm.When interpreting these results, we infer that when using biomaterials, we are not dependent on the patient's bone availability or the collection technique used.
Increases in bone height that exceed the length of the implant to be placed result in increases that will not be used and that tend, over time, to reabsorb regardless of the graft used. 40,92e differences in bone height gain with the use of bone graft mixed with some type of cell growth promoter are not clinically relevant. 79,94For example, the use of PRP did not positively influence the results in the 2016 Kiliç S and Güngörmüş M randomised clinical trial 95 when purchasing β-TCP +PRP and β-TCP.

Barrier membrane on the lateral wall
The placement of resorbable or non-resorbable barrier membranes on the later wall of the osteotomy at the end of the procedure for placing the graft material aims to help contain the graft, prevent soft tissue encapsulation, the invagination of connective tissue into the sinus jaw and increase the success rate of dental implants. 1The membrane also prevents the passage of epithelial cells into the grafted area.Finally, the amount of vital bone can influence implant survival. 15,23,31,96,97his influence is evident in the 2013 Barone A. splitmouth clinical trial 98 that compared the effect of placing a collagen membrane on the sidewall versus do not place, filling both maxillary sinuses with porcine xenograft.The author 98 reported that in the group where a membrane was used on the side wall there was a mean percentage of smaller connective tissue (50.6% ± 18.7% vs. 59.3% ± 15.4%), a total percentage of larger bone (49.4% ± 18.7% vs. 40.7%± 15.4%) and a percentage of residual graft also higher (18.4% ± 20.3% vs. 12, 6% ± 12.4%).

Implant success rates
The survival rates of the implants, in a first phase are closely linked to the realisation of a good surgical protocol and to a good primary stability when placing the implant.Over time, survival rates are mainly affected by smoking habits and pathologies that make patients immunocompromised (e.g.poorly controlled diabetes) and poor oral hygiene.For these reasons, control of risk factors and periodontal support treatment consultations are essential. 99,100Marginal bone loss is intrinsically related to the type of prosthetic connection (in external connections it is greater), smoking habits and history of periodontitis, these being factors that negatively influenced the maintenance of the peri-implant bone. 101valuating the literature data on the implant survival rate after maxillary sinus graft by lateral osteotomy, different systematic reviews report average rates above 90% and present results similar to implants placed in native bone.][104] The graft material used does not appear to be a highly influential factor in the survival rate of dental implants, observing similar survival rates of the implants placed in the maxillary sinuses that had been filled only with bone substitutes (96.1%) or when it was included autograft (95.8%). 17he same is observed when using PRP as a supporting material for implant failure or complications. 105When maxillary sinus elevations are performed with autologous iliac crest blocks, the survival rate is 83.5% and is reduced substantially to 78.7% when the implants are placed simultaneously. 17Considering only studies with five or more years of follow-up, there is a 97% survival rate for implants with autograft grafting.95% with bovine xenograft. 40onsidering the time window in which dental implant failure occurs, it is observed that more than 80% of cases occur during the first 6 months of loading, 97.1% in the first year and that the late loss of implants (up to 2 years from connection) is significantly affected by bone quality. 102nother important factor is the roughness of the implant surface and its influence on the biomechanical quality of the osteointegrated bone.Implants with a rough surface show greater integration and resistance of bone contact when compared to smooth surface implants, with lower rates of survival when smooth-surface implants are used. 67,99he use of a membrane to cover the lateral window increases the survival rate of the implants.This trend is observed in the 98% success rate variation vs. 92.7%,when a membrane is not used. 17It is important to note that the 2009 review by Jensen et al. 17 indicates that if studies using implants with smooth surfaces were excluded, the survival rates with and without the use of a membrane were almost identical.

CONCLUSIONS
The technique of elevating the maxillary sinus through a lateral window is a safe and well-documented technique in the literature, with high rates of survival and success of dental implants in the long term.
The commonest complication that occurs with this technique is the perforation of the Schneider membrane, which, depending on the extent of the rupture, can be repaired intrasurgically.
Simultaneous placement of dental implants should only be performed in cases where the bone height is greater than 5 mm, otherwise, a two-step technique should be chosen.
The use of different graft materials is well documented in the literature, but it is essential to bear in mind that the non-use of autograft increases the time of bone maturation.On the other hand, placing a membrane on the side wall increases the amount of vital bone and special attention should be paid to the different pathologies that may contraindicate this technique when carrying out the clinical history.

C ON F L IC T OF I N T E R E S T
The authors declare no conflict of interest, either directly or indirectly, in any of the products listed in the manuscript.
This work was supported by Portuguese funds through the Portuguese Foundation for Science and Technology (FCT), within the IEETA/UA project (UIDB/00127/2020, www.ieeta.pt)and by Portugal 2020 under the Competitiveness and Internationalization Operational Program.