Gadala, Aly S.a; Hassan, Khaledc; Ishak, Mahab
The use of dental implants in oral rehabilitation has proven to be one of the most exciting advances in dentistry in the last decades. Dental problems that were historically considered the most difficult can be solved nowadays with the use of dental implants. For instance, completely edentulous patients can now enjoy the security and function of fixed restorations. Patients missing a posterior abutment, who would ordinarily require a distal extension removable denture, finally will be able to get use of a fixed restoration as well. Furthermore, trauma victims who suffer missing teeth and bone can be successfully rehabilitated both in function and esthetics using fixed restorations.
Intrusion of dental implants into the maxillary sinus has been considered for a long period of time as a cause of undesirable complications [1–3]. However, these claims had not been assessed using evidence-based medicine. To avoid invading the sinus in the atrophied maxillary ridges, myriad techniques of sinus elevation and grafting procedures have been advocated to augment the sinus, thus providing a suitable room for the posterior maxillary implants to gain appropriate initial stability.
The maxillary posterior edentulous region represents a real challenging condition in implant dentistry compared with other regions of the jaws . The limited amount of bone volume in the atrophied ridge together with pneumatization of the maxillary sinus renders dental implant placement in the posterior maxilla to be a more complicated, demanding, and hazardous procedure.
We hypothesize that intrusion of short-length implants (maintaining acceptable initial stability) into the maxillary sinus does not cause deleterious effects [5–7]. Therefore, this study aims to investigate the possible sinus complications resulting from penetrating the dental implants by 2–4 mm, and more into the maxillary sinus cavity in patients seeking dental implant restoration and having a limited bone height.
The aim of this study is to evaluate the effect of a traumatic insertion of dental implant into the sinus cavity.
Patients and methods
Fourteen patients (five men and nine women) ranging in age from 27 to 55 years were included in this study. They were suffering from unilateral edentulous maxillary posterior area. The cases were selected according to the following criteria:
(1) All patients who were free from any systemic disease that might negatively affect the implant survival.
(2) All patients who were free from any local pathosis that is contraindicated or might interfere with the dental implant procedure.
(3) No earlier history of maxillary sinus surgery.
(4) No apparent dental and/or skeletal abnormalities.
(5) Psychologically stable to understand the nature of the procedure.
Before starting our study, the nature of the surgical procedure and its possible complications were explained to all patients. The alternative treatment modalities were also discussed. Informed consent was obtained from each patient before any surgery and after discussing all the possibilities.
Preoperative radiographic examinations by means of orthopantogram (OPG) and dental computed tomography (DCT) scan were made for all cases. Immediate postoperative radiographs in terms of OPG were also obtained for all patients. In the mean time, a digital OPG at 4 and 10 months and DCT at 16 months, postoperatively, were obtained. Preoperative OPG was performed to show bone height and trabeculations of the present ridge and to exclude general and local causes that could hinder the implant placement procedure. In contrast, DCT was performed to evaluate the sinus condition for the presence of infection or any pathosis. Moreover, it permits bone height evaluation in three dimensions (axial, coronal, and sagittal) of the proposed area that allow accurate assessment of the ridge. Immediate postoperative OPG was taken for all cases to assure that implants were protruding into the sinus floor by the planned length. Four months postoperatively, Dental orthopantomogram (DOPG) was performed to evaluate osseointegration before implant loading. Furthermore, 6 months later another DOPG was performed to evaluate postloading osseointegration of the peri-implant bone. Furthermore, DCT was performed at 12 months after implant loading to clarify the sinus condition.
The patients were selectively divided into two equal groups according to the available bone height and the intruded implant length inside the maxillary sinus. Both groups were treated using dental implants of the same length (10.5 mm) (Biohorizons Internal Implant System, Biohorizons Implant System Inc., Birmingham, UK, Al 35243).
(1) Group 1: the available bone height between the crest of the ridge and the sinus floor at the surgical site was 8 mm, so that in which the implant was inserted it extended less than 4 mm inside the maxillary sinus (10.5–8=2.5).
(2) Group 2: the available bone height was 6 mm, so that in which the implant was inserted, it extended 4 mm or more through the sinus cavity (10.5–6=4.5).
Stage 1 surgery
Profound local anesthesia was achieved for all patients. A trapezoidal mucoperiosteal flap was outlined. A sharp paracrestal incision was first made in the edentulous area ending 1 mm from the adjacent teeth to preserve the papillae. Two curvilinear releasing incisions were made mesially and distally from the ends of the paracrestal incision toward the buccal vestibule (Fig. 1). The mucoperiosteal flap was retracted to expose the site of implant placement. The surgical guide template was placed in position, and the buccopalatal location and ideal angulations were determined. The alignment drill was used to initiate the osteotomy to a depth of 5 mm (Fig. 2). Subsequently, the surgical stent was removed. The osteotomy depth was established beyond the height of the residual ridge using the depth drill that perforated the sinus floor. The ruler or depth gauge was used to confirm the sinus perforation. The osteotomy was widened using a series of enlarging drills of diameters 2.5, 3, 3.2, and 3.7 mm in the same order to enlarge the osteotomy site systematically. The drilling was done in a pumping motion under a constant stream of saline for cleaning and cooling. The paralleling pins were placed in the same order to verify the position and angulations (Fig. 3). The final drill (diameter: 4.7 mm) was used before placement of the implant (Fig. 4).
After the desired depth and diameter of the recipient site were obtained, the implant was placed. Using the hand piece adaptor, the implant was threaded in the osteotomy site; then, the primary stability was checked and confirmed. Suturing of the flap was accomplished using the interrupted technique with black silk. A tension-free closure was obtained in all cases. A panoramic radiograph was taken immediately postoperatively to evaluate the penetrated part of the implant into the maxillary sinus cavity. All patients were instructed to follow the postoperative regimen.
Stage 2 surgery
Uncovering the implant site was carried out 4 months after the first surgery. The surgical site was anesthetized and the soft tissue immediately overlying the implant fixture was removed to expose the screw cover of the fixture, which was then unscrewed. Depending on the height of the soft tissue, the healing abutment was chosen and inserted. After 10–14 days, the patients were referred to the fixed prosthodontic, where the healing abutment was removed and the permanent abutment was inserted, upon which the final crown was delivered few days later.
Clinical follow-up was carried out weekly during the first month and then after 6, 12, and 16 months, postoperatively. Healing of soft tissue, stability of the osseointegrated implant, and the clinical condition of the maxillary sinus were assessed. Panoramic radiographs were obtained for all patients at 4 months, postoperatively, and 6 months postloading for evaluation of osseointegration of inserted implants. Bone quality and the presence of any radiolucency around the implant were reported. Furthermore, 12 months postloading a DCT scan view was obtained for each patient to assess the condition of the maxillary sinus and bone osseointegration around the implants. All radiographs were evaluated through qualitative and quantitative analysis. All computed tomography images were examined using the Dicom Software (Dicomwok, version 1.3.5(C) 2000, 2008, Philippe PUECH and Loic BOUSSEL, Lyon, France) and digitized using the same digital camera (Sony Cyper Shot, 5.1 mega pixel, China). For standardization, all shooting distances and camera settings were kept constant.
All radiographs were positioned on the same homogenous light source and imaged in one session, stored in the computer's memory, and then projected onto a monitor as an array of 512×512 pixels with 256 gray levels. The digitized images were manipulated using the specially designed software of the Digora system (Digora system, Soredex, Orion Corporation, Finland). On each digital image, the mean gray values of the regions of interest, bone implant interface, and corresponding alveolar bone at three different regions (coronal, middle, and apical) were calculated using the area measurement facility of the software. The readings were presented as means and the data were checked, coded, and analyzed by using the Statistical Package for Social Sciences (SPSS) version 17.0 software (SPSS Inc., Digora, Hilsinky, Finland). The results were collected and analyzed by using the 0.05 significance level and the 0.01 high significance level; a P value of less than 0.05 was considered significant.
This study was conducted on 14 patients. A total of 14 implants were placed in the residual ridges in such a way that they penetrated the maxillary sinus floor by approximately 2 mm in seven patients (group 1) and by 4 mm or more in the rest of the patients (group 2).
The patients were evaluated clinically regarding healing of surgical site, stability of the osseointegrated implant, and clinical condition of the maxillary sinus. Evaluation of the surgical site was done with respect to edema, wound dehiscence, and infection. This study showed no postoperative edema, except in case no. 2 in group 1 and case no. 4 in group 2, which showed moderate swelling that started on the first postoperative day and disappeared gradually few days later. The same two cases had dehiscent wounds that were managed by local care. These wounds healed without considerable problems, except for the exposure of the covering screws of the inserted implants. No signs or symptoms of infection were reported at the surgical site throughout the follow-up period. All patients tolerated the surgical procedure without any significant complications.
Stability of the osseointegrated implants was evaluated before loading and at 3, 6, and 12 months after loading. Mobility of the implants was assessed clinically by placing each implant between a finger at one side and the handle of a plastic mirror at the other. The implant was then gently wiggled and clinical judgment was assessed according Miller's mobility index. Mobility was checked in all directions. All patients of both groups showed no distinguishable movement during the whole study period.
The parameters and tools for clinical assessment of the sinuses were carried out through a patient questionnaire. Pain was evaluated by using an analog score from 1 to 10. Tenderness, any nasal discharge, or signs of inflammation were evaluated by comparing the preoperative and postoperative conditions of the sinus.
This note was cleared and the aim of the study was modified.
DOPGs were obtained and analyzed (qualitatively and quantitatively) for all patients 4 months poststage 1 surgery and 6 months postloading. Evaluation of DOPG views showed good adaptation of bone around the implant with an absence of peri-implant radiolucency in all patients of both groups (Figs 5–23). There was no statistically significant difference between radiodensitometric measurements of bone/implant interface and the adjacent alveolar bone. The statistical results showed no significant difference between implant/bone interface and the surrounding alveolar bone in all patients of both groups (Tables 1 and 2).
DCTs were obtained for all patients 12 months postloading. The images of group 1 showed no abnormal reaction, except in two cases that showed mucosal thickening around the implants. In contrast, all patients in group 2 showed mucosal thickening around the intruded part of the implant, except one. Integrated bone around the implant appeared with intimate contact to the implant fixture surface in all patients of both groups. There was no statistically significant difference between the mean values of implant/bone interface and adjacent alveolar bone.
Sinus elevation and subantral augmentation techniques have allowed an increasingly more predictable use of implants in the posterior maxilla [8,9].
In fact, the sinus graft technique has become one of the most common methods for increasing bone height and density, providing excellent clinical survival statistics. However, it is accompanied by several difficulties that render this technique more complicated.
The literature is full of valuable studies discussing the dental implant and the sinus, but very few examined the sinus response to perforation by the dental implant. These studies retrospectively analyzed the sinus response to the implants that displaced completely into the sinus cavity [7,11]. In the mean time, researches that discussed the sinus reaction to the partial exposure of the implant through the sinus lumen are very scarce.
Although, it is more reliable to have a control group in any research, our study design did not involve the use of a standard control group for many reasons. First, the control group in this study would be the sinus lift group. This procedure is lengthy and complicated and its results are well documented from the literature. Thus, we can base our comparative results on the literature results. Second, we preferred to design a prospective rather than a retrospective study. Third, we also preferred to split the patients into two groups according to the penetrated distances in the sinus cavity to compare the effect of implant penetrating the sinus cavity by varying distances.
Although it seems unethical to place implants inside the sinus cavity, the accidental situation of penetrating the sinus cavity is common and not realized until it is discovered by routine postoperative radiographs. The difficult decision of removing or sparing the implant is never dependable on a solid scientific basis because of the lack of such studies in the literature. Meanwhile, removing an initially stable implant without obvious complications is a difficult decision as well. Loose or initially unstable implants will be removed. In contrast, stable implants need thorough studies on both sinus reaction and long-term implant condition.
Several investigators observed that direct accidental penetration of the implant into the sinus floor did not cause serious problems as expected. They rely on spontaneous healing of the sinus membrane after slight perforation because of implant placement [5–7]. The studies have focused primarily on showing osseointegration in implants that have penetrated the floor of the sinus [4,10]. It has been recommended that at least 4 mm or more of bone length below the sinus floor should be available for obtaining an initial stability .
Branemark et al.  discussed both sinus reaction and osseointegration of implants that protruded through both nasal and sinus cavities. They reported good results. Recently, in an experimental study, Jung et al.  investigated the possible maxillary sinus complications after intentional intrusion of dental implant. The investigators reported that implant intrusion into the maxillary sinus cavity was not associated with sinus complications. One year later, the same investigators retrospectively investigated the effects of exposing dental implants to the sinus cavity in humans. They found the implants that had been inserted more than 4 mm into the maxillary sinus were not associated with clinical complications. This coincided with our clinical findings that showed no signs or symptoms of maxillary sinus infection in any patient of both groups.
In this study, computed tomography images of both groups showed sinus mucosal thickening with varying degrees. Five patients in group 2 that had implant penetration of 4 mm or more through the sinus cavity showed mucosal thickening around the intruded parts of the implants. This was comparable with the study performed by Jung et al.  where radiographic examination showed postoperative sinus mucous thickening around 61% of all implants used. However in our study, two patients from group 1 (who had implants that intruded less than 4 mm) showed similar sinus reaction in terms of mucosal thickening. This was not the case in the study by Jung et al.  when they did not report any thickening of sinus lining around implants that intruded by 2 mm into the sinus. Interestingly, no symptoms of maxillary sinusitis were induced by the mucosal thickening in the follow-up period (16 months). This was probably because of the fact that the swelling of the mucosal lining was localized in nature.
Boyne  evaluated the long-term effect on the metal–bone interface of implants that protruded 5 mm through the sinus and reported excellent clinical function for 14 months postloading. The investigator also stated that the protrusion of the implants maximally into the sinus floor does not necessarily require a bone graft to produce functional abutments. These findings agreed with our results where the clinical postoperative follow-up showed that all implants of both groups remained clinically stable under function, despite the greater distance of intrusion through the sinus cavity in some cases. This might be attributed to good bone quality of the residual ridges, a traumatic surgery, and to proper soft tissue handling. Controlled speed, using sharp drills, and constant cooling, were essential parameters in the surgical protocol. Radiographically, no signs of pathologic bone reactions or abnormal loss of anchoring bone were seen. Furthermore, osseointegration was comparable with the natural bone in all patients of both groups. All these implants had satisfactory primary stability during surgery. This confirmed that the initial stability is the cornerstone of osseointegration and implant survival [14–17].
In this study, all implants in both groups were loaded 4 months postsurgery with fixed crowns. The loaded implants showed good function and stability through the postoperative follow-up period that extended up to 12 months for all cases and 20 months in some patients. These findings came in accordance with the results obtained by Mish . The investigator reported that implants might even penetrate the sinus floor, protrude into the sinus space, and might serve as satisfactory prosthetic abutments.
This study proved that sinus-protruding implants could be used as a less complicated procedure compared with other surgical options [19–21]. It is less time consuming and economically more accepted. It also showed good functional stability with fair loading. The follow-up showed satisfactory clinical and radiographic results with non-significant complications.
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