Successful Management of Apically Exposed Implants in the Maxillary Sinus and Associated Sinus Pathologies Via Maxillary Sinus Floor Augmentation Open Access

Lateral maxillary sinus floor augmentation (MSFA) allows for implant placement in the posterior maxilla with severe pneumatization and limited residual bone height.¹  However, thickened mucosal lesions along the Schneiderian membrane are frequent findings that may hinder clinicians from proceeding with safe and predictable sinus augmentation procedures. Postoperative complications may develop when MSFA is performed near a location with sinus membrane thickening,²  or around exposed implant surfaces inside the maxillary sinus that are not supported by the bone at the apical extent.³  Significant sinus membrane thickening associated with the presence of apically exposed implants may necessitate collaborative efforts with ear, nose, and throat (ENT) colleagues functional endoscopic sinus surgery (FESS) before sinus grafting. Occasionally, FESS and implant grafting procedures can be performed simultaneously.^4–6 

In general, sinus augmentation near the contaminated surface of an existing protruding implant involves the risk of infection.³  Specifically, if the implant apex protrudes into a diseased sinus, or if the Schneiderian membrane is thickened and surrounding the implant apex, there may be implant surface contamination; thus, there is an increased risk of postsurgery infection. However, when the protruding implant apex is surrounded by a health Schneiderian membrane with a disease-free sinus, the risk of post-surgery infection is diminished. Recently, Ueno et al and Park et al reported successful MSFA outcomes through unique decontamination methods for apically protruded implants inside the sinus cavity.^3,7  Park et al also reported that the removal of benign sinus pathologies via a lateral window approach resulted in: (1) minimal patient discomfort, (2) reduced postoperative complications, and (3) shorter treatment periods.⁸  This validates that removal of mucosal lesions during MSFA is an effective technique that can enhance overall success. The purpose of this case report is to present 4 clinical cases of apically exposed implants in the maxillary sinus that were successfully treated with decontamination of the apically exposed implants and simultaneous pathology removal. In addition, successful outcomes of newly implants with simultaneous MSFA with the limited residual bone are also presented.

The present case report contains 4 clinical cases, each with 1 implant that is protruded into the maxillary sinus without apical bony support. All cases presented with asymptomatic sinus membrane thickening. Patients were treated in 1 private dental office in Seoul, Korea. Patients were medically healthy, and none reported having sinus-related symptoms. Panoramic radiography and cone-beam computerized tomography (CBCT; Rainbow CT, Dentium, Suwon, Korea) were obtained and used to confirm the apical protrusion of implants beyond the sinus floor without surrounding bone. All implants were functionally stable despite the lack of apical bone and the presence of sinus pathologies. During MSFA, the protruding implants were treated with appropriate surface detoxification methods, and other implants were placed in the adjacent edentulous sites simultaneously. All patients were given written and verbal consents prior to all surgical procedures.

MSFA was performed with the lateral window approach as described by Tatum et al.⁹  Using local anesthesia (lidocaine 2% with epinephrine 1:100 000), mucoperiosteal flaps were raised. Proximal to the protruding implants, a lateral window osteotomy was made using a high-speed handpiece with round diamond burs. Once the window was removed, fine sinus elevation instruments of various shapes (DASK Kit, Genoss, Suwon, Korea) were used for detachment of the Schneiderian membrane from the implants. Care was taken to not tear or perforate the membrane. However, during the membrane reflection, all sites resulted in membrane perforations proximal to the implants. The resulting tears provided sufficient access to evaluate and remove soft tissue lesions from inside the sinus. An aspiration needle, dental pincettes, and tissue forceps were used to remove the lesions. The cystic fluid or exudate contents were further drained through high-volume surgical evacuation tips. Mechanical debridement was performed on the contaminated implant tips using titanium curettes and titanium brushes using a slow-speed handpiece (Genoss), followed by chemical detoxification using tetracycline hydrochloride (HCl; Oxymycin, 500 mg, Chong Kun Dang Pharmaceutical Co, Seoul, Korea) for 5 minutes at 100mg/mL with saline solution. Visible debris adhering to the implant tips was removed. The decontamination procedure was considered complete when visible changes in the surface texture of the implant surfaces were noted. The surgical fields were thoroughly irrigated with sterile 0.9% normal saline solution before adding biphasic calcium phosphate (Osteon III, Genoss) as the bone grafting material. The leakage of bone graft particles through the perforated membrane site was prevented by using the Prichard elevator; no other repair methods were used.¹⁰  In addition, each patient received 1 additional implant adjacent to the protruding implants simultaneously. Bone pieces saved from the lateral window preparation step were used to cover the grafted site as physical barriers. The mucoperiosteal flaps were repositioned in a tension-free fashion (Nylon 4-0, Ethilon 4.0, Ethicon, Cincinnati, OH, USA), and primary closures were achieved. In all cases, patients were instructed to take 2 g of amoxicillin 1 hour before surgery and ciprofloxacin 500 mg twice a day for 10 days postoperatively with nonsteroidal anti-inflammatory drugs (Etodol 200 mg, Yuhan Co, Seoul, Korea) 3 times a day for 14 days. Although the combination of amoxicillin and metronidazole is a common antibiotic regimen after sinus grafting, an alternative protocol of using ciprofloxacin was chosen. Patients were also advised to rinse the mouth with 0.12% chlorhexidine solution (Hexamedine, Bukwang Pharmaceutical, Seoul, Korea) for 30 seconds, 2 times a day for 1 week, and were asked not to blow their nose. All patients were carefully monitored. Panoramic radiographs and CBCTs were taken immediately after MSFA, at the time of final prosthesis delivery, and at the follow-up visit.

The age, sex, apically exposed implant locations, additional implant sites, fixture sizes, mucosal thickness and shapes, and total follow-up periods are listed in Table 1. After the surgical intervention, there were no reported adverse reactions other than expected postoperative pain, edema, hematoma, nasal bleeding, and transient acute sinusitis. Uncovering was performed 6 months after the surgical placement and all prostheses were delivered 2 months later. All implants survived an average follow-up period of 18.25 months. The masticatory function was well-maintained without loss of osseointegration or bone loss around the implants. CBCTs obtained at the time of the prosthesis insertion demonstrated that the previously exposed implants were surrounded by new bone, and in all but Case 1, the sinus membrane thickness was significantly decreased compared to the baseline.

A 68-year-old healthy male nonsmoker presented with a #13 implant that was placed with an osteotome technique 6 years prior to the new CBCT (Figure 1). An ENT consult was obtained, and it was confirmed via endoscopy that the ostium was fully open and the ostiomeatal complex was intact. The implant had been in function for 6 years without any adverse clinical symptoms. The CBCT revealed a large circumferential polypoid lesion occupying the maxillary sinus with the residual bone of approximately 3 mm distal to the #13 implant (Figures 1a and b). An oval-shaped lateral-window osteotomy was prepared (Figure 1c) and the Schneiderian membrane was reflected. Near the #13 implant, a perforation was noted, and the entire sinus lesion was carefully removed with a dental pincette through the perforated site (Figure 1d). Mechanical debridement of the implant surface with titanium brushes was followed by an application of tetracycline HCl (Oxymycin, 500 mg, Chong Kun Dang Pharmaceutical; Figure 1e and f). Without any repair of the perforation, biphasic calcium phosphate (Osteon III, Genoss) was tightly condensed around the exposed implant as well as around #14 and #15 sites, which received SLA-textured implants (4.3 × 10 Implantium, Dentium; Figure 1g and i). The island of bone that was saved from the osteotomy preparation was used to enclose the grafted site as a physical barrier, and flaps were sutured with primary closure (Figure g).

There were early complications of nasal bleeding, hematoma, and wound opening after the operation, but these healed uneventfully. Six months after the procedure, the prosthesis was delivered, and masticatory function has been well maintained without clinical symptoms for 12 months. However, the postoperative membrane thickness was not reduced compared to the preoperative membrane thickness (Figures 1h and i). The exact reason why the mucosal thickening was not reduced cannot be explained, but authors presume that the patient's chronic rhinitis might have contributed to this finding. The application of resorbable collagen membrane or platelet-rich fibrin membrane around the perforation of the thickened sinus mucosa could have been an alternative solution, but based on the experience of the authors, such a method did not produce consistently good clinical results.

A 72-year-old nonsmoking healthy female had the #4 implant placed with a simultaneous transcrestal sinus lifting procedure without additional bone grafting materials due to an operator-observed perforation intraoperatively. The CBCT showed that the #4 implant had penetrated 4 mm beyond the sinus floor with the presence of a large radiolucent sinus lesion. ENT consult confirmed that the ostium and ostiomeatal complex were intact. There were no reported symptoms related to these findings. The residual bone volume around missing #3 was insufficient and MSFA was indicated for the implant placement (Figure 2a and b). A membrane perforation was noted (Figure 2c) during the elevation, and a mucosal lesion was removed. Mechanical debridement of the exposed implant surface with titanium brushes and chemical detoxification was done using tetracycline HCl (Oxymycin, 500 mg, Chong Kun Dang Pharmaceutical). To prevent any migration of graft particles into the sinus via the perforated site, a Prichard elevator was used to block the passage (Figure 2d), and biphasic calcium phosphate (Osteon III, Genoss) was carefully condensed around the exposed implant and #3 site. A fixture (4.3 × 10 mm; Implantium, Dentium; Figure 2e) was placed and subsequently restored (Figure 2f).

There was transient nasal bleeding and facial swelling for 2 days postoperatively, but there were no other postoperative complications. Six months after the procedure, the prosthesis was delivered (Figure 2f). Chewing function has been well maintained for 2 years. Preoperative membrane thickness also decreased significantly after surgery (Figures 2e and f).

A 62-year-old male nonsmoker had the # 2 implant placed 2 years before the initial CBCT (Figure 3a and b). The CBCT revealed that the apex of the implant extended 1 mm beyond the sinus floor. A circumferential membrane thickening was observed, and the residual bone proximal to #3 site was approximately 2 mm (Figure 3a and b). An ENT consult confirmed that the ostium and ostiomeatal complex were intact, and the patient did not report any relevant symptoms. During membrane reflection, a perforation was observed, and the lesion was removed. A titanium brush with a slow-speed handpiece was used to mechanically debride the exposed implant and tetracycline HCl powder (Oxymycin, 500 mg, Chong Kun Dang Pharmaceutical) was used for chemical decontamination. Then, biphasic calcium phosphate (Osteon III, Genoss) was carefully grafted around the exposed implant as well as the #3 site followed by a fixture placement (4.8 × 12 mm; Implantium, Dentium).

Postoperative complications included nasal bleeding, facial swelling, and acute maxillary sinusitis. The acute maxillary sinusitis disappeared with the additional administration of ciprofloxacin 500 mg twice a day for 1 week. Reduced sinus membrane thickness was noted on the radiograph taken at the time of prosthesis delivery, and its thickness has been maintained for 3 years (Figure 3c and d).

A healthy 55-year-old non-smoker had implant #15 placed with a transcrestal sinus grafting procedure using bovine bone graft. The implant had been in function for 13 years without any complications other than the development of a cyst-like lesion inside the sinus (Figure 4a and b). An endoscopy by ENT confirmed that the ostium and ostiomeatal complex were intact, and the patient did not report any relevant symptoms. Due to the poor prognosis of tooth #14, it needed to be extracted and replaced with an implant. With only 4 mm of residual bone below the sinus floor, MSFA was used to treat #15 implant and place the #14 implant simultaneously. A lateral-window osteotomy was prepared proximal to the perforated site near the implant apex (Figure 4c). The entire lesion was carefully removed, and the exposed implant surface was further detoxified by using the titanium brush and tetracycline HCl powder (Oxymycin 500 mg, Chong Kun Dang Pharmaceutical). Biphasic calcium phosphate (Osteon III, Genoss) was used to graft around the exposed implant as well as the #14 site (Figure 4d). A fixture was simultaneously placed (4.8 × 10 mm Implantium, Dentium), and the restoration was delivered after achieving osseointegration (Figure 4e). There was transient nasal bleeding, hematoma, and facial swelling, but otherwise healing was uneventful. The prosthesis was delivered after 6 months (Figure 4d and e). The patient was followed up for 23 months post-prosthesis delivery. (Figure 4d and e)

The MSFA is a procedure with a high degree of clinical predictability that allows for implant placement in the maxillary sinus with severe pneumatization.¹¹  MSFA is a procedure that should be performed when the ostium is open and the ventilation by mucociliary transport is well maintained.¹²  However, the presence of large sinus pathologic lesions in the maxillary sinus, or the presence of contaminants such as apically protruded implants, is a relative contraindication.²  An extensive elevation of a thickened sinus membrane can potentially obstruct the natural ostium.²  Maxillary sinus grafting around a contaminated implant surface may also result in sinus graft infection and postoperative maxillary sinusitis. In addition, maxillary sinus pathologic lesions are a potential risk factor for implant failure and sinus graft infection.¹³  However, it has also been reported that successful maxillary sinus augmentation can be achieved in the presence of sinus membrane thickening.^14,15  Elevation of the maxillary sinus membrane with bone augmentation in the presence of membrane or sinus pathology remains controversial. This report presents 4 cases with sinus pathologies that were surgically removed through the perforated membranes and simultaneous management of the apically exposed and contaminated implant surfaces.

Risk factors that can induce sinus membrane perforation include sinus septum, irregular sinus floor, limited residual bone height, and sinus membrane thickening.^8,16,17  The Schneiderian membrane perforation has been reported as a major cause of complications after MSFA.^10,16–18  Therefore, the repair of the perforated sinus membrane is considered mandatory, and the repaired sinus membrane does not affect the clinical and radiological outcomes of MSFA.¹⁸  Unlike the common conception, however, Park et al reported that the nonrepair of perforated sinus membranes did not affect the clinical and radiological outcomes of MSFA and, conversely, the perforation group actually resulted in significantly more reduction of the mucosal lesions compared to the non-perforation group.¹⁰  The heterogenicity of these results appears to be due to the: (1) presence of maxillary sinus lesions, (2) ability of the operator, and (3) duration of postoperative antibiotics.¹⁹  Accidental or unavoidable membrane perforation during sinus floor elevation may generate an opportunity to eliminate pathologic sinus lesions. In the presented cases, no resorbable collagen membrane was applied to the perforated area of the thickened sinus membrane. The reason is that, according to the author's experience, when the sinus membrane is thickened, the resorption of the collagen membrane is too fast and the surrounding inflammation intensifies, leading to early loss or infection of the grafted sites. In the present cases, sinus membrane perforations occurred around all protruding implants during the membrane elevation, despite careful instrumentation. As a result, the sinus pathologies were efficiently removed through the entrance created by the membrane perforation.

Thorough decontamination of the exposed implant surfaces inside the maxillary sinus is one of the keys to the successful long-term survival of treated implants. Decontamination methods using a rotary titanium brush and tetracycline HCl for the management of contaminated implants have been reported in several studies.^7,20–23  However, only a few reports of decontamination of the implant surface exposed in the maxillary sinus exist.^3,7  Ueno et al treated the contaminated implant surface by wiping the surface with saline-soaked gauze only without additional mechanical or chemical detoxification and clinical success was reported.³  In the present cases, the degree of contamination of the exposed implant appeared to be worse than that reported by Ueno et al. The implants they reported on were not associated with any sinus pathologies, and the exposed implants were residing in healthy maxillary sinuses. Due to the presence of sinus pathology, patients reported in this report had to be treated with a more thorough detoxification method. The mechanical debridement with rotary titanium brushes and titanium curettes were used to remove visible debris attached to the implant surface, and this was performed by visual confirmation of shinier implant surfaces.⁷  However, protruding implants in the sinus were challenging to access, and the operator had to depend mostly on tactile sensation, especially around the distal aspect of the exposed implants. Therefore, additional chemical detoxification was undertaken. Park et al reported successful clinical and radiological results of decontamination of the implant surface protruded into the postoperative maxillary cyst using a rotary titanium brush and tetracycline HCl.⁷  Tetracycline HCl is known to kill bacteria on contaminated implant surfaces, inhibit collagenase activity, and eliminate endotoxins.^21,24  Additionally, authors speculate that the use of ciprofloxacin could have also contributed to the current findings in the presented cases. Although the combination of amoxicillin and clavulanic acid is most commonly used to treat sinus complications, numerous studies have shown that ciprofloxacin was an alternative antibiotic that produced comparable results when used for acute and chronic sinusitis.^25,26 

In the present cases of sinus pathology-related mucosal thickening, MSFA was an effective therapy to: (1) gain access, (2) remove pathologic lesions, (3) decontaminate apically exposed implants, and (4) successfully augment bone grafting materials around existing and newly placed implants. Without histological evidence, it is impossible to assess whether de novo bone around decontaminated implant surfaces is truly contributing to re-osseointegration or it is just bioinert adaptation. However, the grafted bone has maintained stability during the follow-up periods, and all implants and prostheses have been without clinical complications. Additional studies with enough sample sizes should be conducted to obtain statistically supported conclusions; however, the cases included in this case report should provoke interests for future research.

CBCT:

cone-beam computerized tomography

FESS:

functional endoscopic sinus surgery

MSFA:

lateral maxillary sinus floor augmentation

SLA:

sandblasted, large grit, acid-etched