Although high survival rates were reported for implants placed with the sinus floor augmentation procedure,1 implant-related complications can occur in the early or late stage after the procedures.2 Implant-related maxillary sinusitis was reported in 0% to 20% of patients.3 Most literature reporting implant-related maxillary sinusitis has been on the topic of immediate complications from implant placement with sinus floor augmentation.
Sinus mucosal perforation was the most frequent intraoperative complication, resulting in displacement of the bone graft material, ostium plugging, implant protrusion into the sinus, and/or sinus mucosal thickening (SMT).4–6 Surgical trauma from the sinus floor augmentation procedure can adversely affect the mucociliary clearance and patency of the maxillary ostium.4 Such occurrence may lead to immediate complications and can cause acute maxillary sinusitis.
Diagnosis of maxillary sinusitis is based on clinical findings, radiologic findings, and nasal endoscopy.7 Sinus mucosal thickness greater than 2 mm indicates maxillary sinus inflammation.8 SMT from dental origin beside implants has been reported in relation to periodontal disease and periapical lesions.9,10 However, the influence of peri‐implantitis on SMT has not been reported.
The bone graft site in the maxillary sinus is weaker than pristine bone in terms of maintaining bone level, long-term implant survival, and infection susceptibility.11–13 Microorganisms from the peri‐implantitis may be able to spread to the sinus mucosal membrane through bone marrow, blood vessels, and lymphatics in the sinus bone graft, which is similar to the spread of periapical infections to the sinus mucosa.9,14
Endoscopic sinus surgery has been reported to be more effective than conservative treatment such as the prescription of antibiotics in dental implant–related paranasal sinusitis.15 However, no study investigated the efficacy of an intraoral approach, such as a modified Caldwell-Luc operation (CLOP), to treat maxillary sinusitis associated with peri‐implantitis. The purpose of this retrospective case series was to investigate radiographic features and characteristics of maxillary sinusitis associated with peri‐implantitis and to evaluate the outcomes of intraoral treatments for managing maxillary sinusitis associated with peri‐implantitis for a 3-year follow-up.
Materials and Methods
Subjects and Implants
The data collection and review for this case series were conducted under an approved IRB exempt protocol at the University of Maryland, Baltimore (HP-00080122, 2018). One hundred twenty-four patients received 322 implant placements with sinus floor augmentation at a private dental clinic from 1998 to 2002. The patients were followed until 2017. Sinus floor augmentation using Bio-Oss (Geistlich Biomaterials, Wolhusol, Switzerland) was performed by a lateral approach (65 patients) or a crestal approach (59 patients) based on the residual ridge height. Implants were an external-hexed submerged type. All patients received 1 or 2 periodic examination(s) and periodontal maintenance each year. Of the 124 patients, 8 patients, who were diagnosed with the maxillary sinusitis associated with peri-implantitis, were reviewed.
The following data from the 8 patients were retrieved: subject characteristics, implant characteristics, symptoms, and signs related to maxillary sinusitis associated with peri‐implantitis, clinical and radiographic parameters of failed and survived implants, and treatment procedures to manage maxillary sinusitis associated with peri‐implantitis.
The diagnosis of maxillary sinusitis associated with peri‐implantitis was confirmed by clinical symptoms and cone beam computed tomography (CBCT) finding. CBCT (rainbow CT, Dentium, Suwon, Korea) scan confirmed mucosal thickening and obstruction of ostium (Fig. 1C) in all 8 patients. The treatment plans were formulated based on severity and complexity of maxillary sinusitis associated with peri‐implantitis. The 8 patients reviewed in this study had 18 implants. One patient lost 2 implants that were involved with maxillary sinusitis associated with peri‐implantitis. Seven patients, who had 7 survived implants, were followed at 6 months and 3 years after treatment.
Treatment of Maxillary Sinusitis Associated With Peri‐implantitis
Four of the 8 patients were treated with implant removal and antibiotics; the remaining 4 patients were treated with implant removal, the modified CLOP, and antibiotics. The treatment procedures were as follows:
- Implant removal and antibiotics: This approach was selected because of the relatively low severity and complexity of the disease based on the clinical signs and symptoms and CBCT findings. Seven implants were removed. A thorough debridement was performed on the inside of the implant extraction socket. Ciprofloxacin 500 mg (Ildong Pharmaceutical Co., Seoul, Korea) and Etodolac (Etodol 200 mg; Yuhan Co., Seoul, Korea) were prescribed 3 times a day for 2 weeks. The patients were advised to rinse their mouths with 0.12% chlorhexidine solution (Hexamedine; Bukwang Pharmaceutical, Seoul, Korea) for 2 weeks.
- Implant removal, modified CLOP, and antibiotics: The modified CLOP was performed for the following conditions: (1) implant displaced into the maxillary sinus (1 patient), (2) bone graft sequestrated in the maxillary sinus (2 patients), and (3) involvement of the anterior ethmoid sinus and sphenoid sinus (1 patient) along with 4 implant removal.
Figure 1 depicts one of the modified CLOPs performed under local anesthesia in this case series. After reflecting the buccal flap, a lateral bony window was formed in a similar manner to the lateral sinus floor augmentation procedure (Fig. 1D). The polypoid tissue in the maxillary sinus was removed, and the pus was drained (Fig. 1E), but the soft tissues attached to the bony wall were left intact. Inferior meatal antrostomy was not performed. Intrasinus hemorrhage was compressed with vaseline gauze for 10 minutes. The buccal flap was closed after removal of the vaseline gauze. Ciprofloxacin 500 mg (Ildong Pharmaceutical Co.) and Etodolac (Etodol 200 mg; Yuhan Co.) were prescribed for 2 weeks. The patients were advised to rinse their mouths with 0.12% chlorhexidine solution (Hexamedine; Bukwang Pharmaceutical) for 2 weeks. The suture was removed 1 week after the procedure.
Clinical and CBCT Measurements
Comparisons of the clinical and radiographic parameters between 11 failed and 7 survived implants were conducted. Probing depths (PDs) were measured at the mesiofacial (MF), distofacial (DF), and palatal (P) sites using a Williams probe (Hu-Friedy, Frankfurt, Germany). Crestal bone loss (CBL), remaining bone thickness (BT) at the implant apex, and SMT on the cross-sectional view of the CBCTs were measured by a blind examiner (J.-Y.H.) through ImageJ analysis software program as follows.16
- CBL at the facial and palatal sites was measured from the top of the implant to the most coronal bone to implant contact of the facial and palatal bone.
- Remaining BT at the implant apex was measured from the apex of the implant to the cortical bone of the augmented sinus floor at the center of the implant apex.
- SMT was measured from the cortical bone of the augmented sinus floor to the superior margin of the sinus mucosa at the center of the implant apex, and the line was drawn along the long axis of the implant.
Figure 2 shows the changes in parameters measured on the CBCTs after the modified CLOP from one of the survived implants. Parameters on the CBCTs from 7 survived implants were compared at the diagnosis (baseline; T0), 6-month (T1), and 3-year follow-up (T2).
All data were presented in mean ± SD. Baseline parameters between the failed and the survived implants were compared using an independent t test. The Friedman test was used to compare SMT, CBL, and BT among the different time points (T0, T1, and T2) in the survived implants, followed by Dunn's post hoc tests. The analyses were performed using a commercially available software program (SPSS version 21.0, IBM Corp., Armonk, NY). The level of significance was set at P < 0.05.
Of the 124 patients, 8 patients (7 males and 1 female) were diagnosed with maxillary sinusitis associated with peri‐implantitis. Patient ages ranged from 35 to 55 years (the mean age: 48.3 ± 7 years) at diagnosis. The 8 patients exhibited no contributing medical history. Five patients were smokers. Maxillary sinusitis associated with peri‐implantitis occurred in 6 (10.2%) of the 59 patients in the crestal approach and 2 (3.1%) of the 65 patients in the lateral approach for sinus floor augmentation.
Table 1 presents the clinical symptoms of the 8 patients with maxillary sinusitis associated with peri‐implantitis. The 8 patients had at least 2 clinical symptoms, and the most frequent symptom was nasal obstruction, followed by loss of smell and mucoid rhinorrhea. Oroantral communication in the implant extraction socket occurred in 4 patients. Bony sequestration of bone grafts in the sinus occurred in 2 patients. One implant was displaced into the maxillary sinus.
SMT and obstruction of the maxillary ostium were observed on the CBCT in all patients with maxillary sinusitis associated with peri‐implantitis. Involvement of the middle meatus of the nasal cavity appeared in 6 patients. Three patients had paranasal sinus involvement (2 patients with anterior ethmoid sinuses and 1 patient with anterior ethmoid sinus and sphenoid sinus).
The 8 patients, who were diagnosed with maxillary sinusitis associated with peri‐implantitis, had 18 rough-surface implants. The implant lengths ranged from 10 to 14 mm, and their diameters ranged from 3.8 to 6 mm. All final prostheses were screw-retained fixed splinted implant-retained crowns (6 patients) or bridges (2 patients), and had been in function for an average of 13.9 ± 2.4 years after final prostheses delivery. All prostheses exhibited screw loosening at diagnosis of maxillary sinusitis associated with peri‐implantitis. Therefore, all prostheses were removed to confirm the mobility of the implants.
Table 2 presents comparisons of the characteristics between the failed and survived implants. Eleven implants were removed at 14.2 ± 2 years after delivery of the final prostheses. The failed implants exhibited mobility and deep PDs, which were significantly deeper than those of the survived implants (P < 0.001). There were no significant differences in SMT, CBL, and BT at the implant apex between the failed and survived implants.
All clinical symptoms from the 8 patients disappeared at 6 months after treatments. Three of the 4 oroantral communication were closed 2 weeks after intraoral treatment. One case, in which the closure did not occur, was covered with a subepithelial connective tissue graft. The mean follow-up period after treatment of maxillary sinusitis associated with peri‐implantitis was 2.7 ± 0.3 years.
The changes of CBL and SMT in the survived implants were evaluated (Fig. 3). There was no significant change in CBL at the facial site (P = 0.237). The CBL at the palatal site significantly increased over time from 2.2 ± 1.4 mm to 3.4 ± 1.5 mm (P = 0.0084). There was no significant change in BT at the implant apex over time (P = 0.77). The SMT was significantly reduced over time from 23.6 ± 4 mm to 2.4 ± 3 mm (P = 0.0003).
Of 124 sinus floor augmentation cases, 6 patients (10.2%) in the crestal approach and 2 patients (3.1%) in the lateral approach developed maxillary sinusitis associated with peri‐implantitis. Although many clinicians prefer the crestal approach because it is considered less invasive, the crestal approach achieves less bone graft volume and less 3-dimensional condensation than the lateral approach.17 The lateral approach may be a better approach to prevent maxillary sinusitis associated with peri‐implantitis when the residual ridge height is at the borderline since the bone density around the apex of the implant could be more compact and dense.18
While 4 patients with maxillary sinusitis associated with peri‐implantitis had oroantral communication, the average BT of the cortical later was approximately 1.5 mm at the apex of the implant in this case series. Bacteria and toxins of peri‐implantitis might spread to the maxillary sinus, even without cortical sinus floor perforation, since the sinus bone graft is porous and more vulnerable to chronic infection compared with pristine bone.11,12
Among the 8 patients diagnosed with maxillary sinusitis associated with peri‐implantitis, 5 were smokers. Smoking increases the incidence of peri‐implantitis and is a risk factor for chronic sinusitis.19,20 Smoking also increases the risk of complications with maxillary sinus bone graft.21
The modified CLOP procedure was introduced to manage odontogenic or nonextensive sinus disease because the traditional CLOP resulted in negative outcomes, such as chronic maxillary neuralgia, infraorbital nerve hyperesthesia, delayed mucocele, and recurrent sinusitis.22–24 The modified CLOP does not involve inferior meatal antrostomy and complete removal of the sinus mucous membrane. Interestingly, increased BT at the implant apex was observed in 3 among the 4 cases treated with the modified CLOP (Fig. 2) but was not observed in patients who were treated with implant removal and antibiotics only.
Spontaneous bone formation was observed after removal of the cyst before implant placement and removal of the displaced implant in the maxillary sinus.25,26 Similar intrasinus bone formation or neo-osteogenesis has been reported after the CLOP and endoscopic sinus surgery.27,28 It is assumed that surgical trauma and creation of secluded space may induce spontaneous bone formation in the maxillary sinus mucosa.25,26 It is also suggested that the intact soft tissue on the bony wall of the sinus may have osteogenic potential.27,28
Several studies emphasize the importance of endoscopic sinus surgery over intraoral approaches.2,15,29 However, SMT, which is the objective parameter to confirm maxillary sinus health,8 continued to decrease significantly for 3 years after the intraoral approaches in this case series. The complete removal of sequestrated bone graft and failed implants, as well as closure of the oroantral communication caused by peri‐implantitis, might play important roles in the improvement. Endoscopic sinus surgery may not successfully treat the sequestration of maxillary sinus bone graft and oroantral communication in complex maxillary sinusitis associated with peri-implantitis cases. To confirm the efficacy of the intraoral approaches and the spontaneous bone formation phenomenon after the modified CLOP, systematic clinical studies with a large sample size and a long-term follow-up should be conducted.
Kim et al15 reported that the implants associated with maxillary sinusitis were not removed after the endoscopic sinus surgery. In their study, only the apex of the implant surface was exposed for 2 years. In this case series, the implants likely to have caused maxillary sinusitis were removed because the implant surface was severely contaminated from chronic peri‐implantitis for 14 years along with CBL and mobility. Although the survived implants remained osseointegrated, the prognosis of the survived implants is questionable since biological and technical complications could still occur.30,31 Therefore, early intervention of peri‐implantitis and associated maxillary sinusitis is important to prevent late implant failure.
With a limitation of this case series, the progression of peri‐implantitis in sinus floor augmented sites may lead to maxillary sinusitis. To confirm the efficacy of the intraoral approaches, such as the modified CLOP, systematic clinical studies with a large sample size and a long-term follow-up should be conducted.
The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article. There is no funding related to this study.
The data collection and review for this case series were conducted under an approved IRB exempt protocol at the University of Maryland, Baltimore (HP-00080122, 2018).
Roles/Contributions by Authors
W.-B. Park: conducting clinical procedures and follow-ups and writing a draft of manuscript. J.-Y. Han: a blind evaluator. S.-L. Oh: conceptualizing the study, conducting statistical analyses, and finalizing a manuscript.
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