Successful Management of Late Sinus Graft Infection via Functional Endoscopic Sinus Surgery and Press-Fit Block Bone Graft: A Case Report

The maxillary sinus augmentation (MSA) is often needed for implant placements in severely atrophic or pneumatized maxillary posterior sites. The MSA is evaluated as an excellent procedure with long-term clinical efficacy and a high implant survival rate.^1–3  However, implants may need to be extracted due to peri-implantitis. Moreover, peri-implantitis-triggered infections of grafted bone in the sinus have been reported to cause oroantral fistulas (OAFs) and maxillary sinusitis.³  It is a clinical challenge to replace implants at sites with OAF or sinusitis.

At MSA sites, some articles have reported that peri-implantitis may cause implant failures in combination with OAF and maxillary sinusitis after long-term loading of the prosthesis.^4,5  In a such complex situation, treatment selection, skill and experience of the operator, and cooperation with an otolaryngologist are critical factors to success. In particular, when the implant extraction socket is communicating with the maxillary sinus and is accompanied by sinusitis, the approach of cleanout (trans-nasal versus intraoral approaches) will affect the treatment outcome. Park et al⁵  reported that peri-implantitis-related maxillary sinusitis could be treated only with an intraoral approach (eg, modified Caldwell-Luc operation). However, the trans-nasal approach (eg, functional endoscopic sinus surgery [FESS]) may be better in some situations because access can be limited in an intraoral approach due to the elevated sinus floor from MSA. Kwon et al⁶  reported that treating inflammation of the maxillary sinus should be prioritized before OAF.

The OAF in the extraction socket of the tooth is easy to close because there is a sufficient amount of residual alveolar bone, whereas the OAF related to implant or MSA is complex and not easy to close. A simple and small OAF (<5 mm) can be closed with only soft tissue methods (eg, buccal flap, buccal fat pad, and rotated palatal flap).⁶  If implant placement is planned at an OAF site, it is necessary to close the fistula with bone rather than with soft tissue.⁷ 

Several reported hard tissue regeneration techniques include guided bone regeneration (GBR), onlay graft, distraction osteogenesis, ridge split, and bone ring techniques.^8,9  These techniques may be used alone or in combination depending on the size and shape of the defect and the preference and ability of the operator. Autogenous bone grafts have the advantage of being highly osteogenic, easily revascularized, and rapidly incorporated.¹⁰  The use of autogenous block bone grafts has been recommended in cases of severe peri-implant bone loss or ridge discontinuity defects.^11,12 

The purpose of this present case report is to evaluate clinically, radiologically, and histologically the results of the 2-staged approach using FESS and intraoral press-fit block bone graft to manage a failed implant site that involved a late sinus graft infection/sinusitis and OAF.

The patient was a 60-year-old female who was a nonsmoker without any systemic diseases except hypertension. Sixteen years ago, a lateral MSA was performed in the right maxillary sinus with severe pneumatization and vertical bone resorption. Xenograft (Bio-Oss, Geistlich, Biomaterials, Wolhusen, Switzerland) was used as bone graft and resorbable blast media-textured implants (4.0-mm diameter) were placed in No. 3, 4, and 5 tooth sites. Six months after implant placement, screw-retained prosthesis was delivered. The patient followed up twice a year for several years, and then disappeared until she returned with implant mobility and discomfort when chewing. The patient suffered from sinonasal symptoms such as nasal obstruction, mucoid rhinorrhea, and headache. Because of these symptoms, the patient had a habit of blowing her nose frequently.

Panoramic radiography and cone beam computed tomography (CBCT; rainbow CT, Dentium, Suwon, Korea) were taken. At the sinus augmented site, peri-implantitis caused severe bone resorption around the implant and concomitant maxillary sinusitis (Figure 1a–c). The sinus ostium was obstructed and the sinus was completely opacified (Figure 1d and e). Extraction of No. 3 and 4 implants was performed (Figure 1b). After 2 weeks of healing, symptoms of maxillary sinusitis did not improve and OAF occurred. The patient was referred to an otolaryngologist to evaluate and treat the sinonasal symptoms. The otolaryngologist performed FESS under general anesthesia to expand the ostium to facilitate ventilation. Local anesthesia was applied as needed around the middle meatus and ostium of the nasal cavity, the uncinate process was removed using a nasal endoscope, and the obstructed ostium was expanded. Purulent discharges, inflammatory tissues, and necrotic graft particles were removed (Figure 2a and b). After hemostasis, clarithromycin (Abbott Korea, Seoul, Korea), acetylcysteine (Hanwha Pharma Co, Seoul, Korea), and methylprednisolone (Jaytech Biogen, Seoul, Korea) were orally administered for 2 weeks. Two months post FESS, the patient's clinical symptoms improved significantly. The patient returned to the dental clinic to close the OAF and to replace the extracted implants.

The extraction site had severe vertical ridge defects and an OAF (Figure 3a and b). Two grams of amoxicillin was orally administered 1 hour before surgery. The surgery was operated under local anesthesia (Lidocaine 2% with epinephrine 1:100,000). A midcrestal incision was performed from canine to maxillary tuberosity. Vertical incisions were performed on the canine and maxillary tuberosity (Figure 3c). Full-thickness mucoperiosteal flap was reflected using periosteal elevator. Underneath the flap were an ovoid-shaped bony defect with a diameter of 15 mm and granulation tissues connected to the Schneiderian membrane (Figure 3c). Granulation tissues were removed. Tooth No. 2 was extracted. An autologous block bone graft was harvested from the No. 2 tooth extraction socket and the right maxillary tuberosity using a small round bur and a bone chisel. The block graft was about 20 mm in diameter and 3- to 4-mm thick (Figure 3d). The outlines and thickness of the block were prepared using a round bur on a surgical handpiece, and bone chisel was used to break off the block from the maxillary tuberosity. The block bone was trimmed to a size slightly larger than the size of the recipient site (the ovoid bony defect). An osteotome and a mallet were used to fixate the block graft. The block graft was malleted into the ovoid recipient site, resulting in a press-fit effect (Figure 3e). After covering the graft with a resorbable collagen membrane (Genoss, Suwon, Korea) (Figure 3f), the surgical flap was sutured tension-free (Figure 3g). Postoperative antibiotic (Cefradine 500 mg, Yuhan Pharmaceutical Co, LTD, Seoul, Korea) and nonsteroidal anti-inflammatory medications (etodolac 200 mg, Yuhan Pharmaceutical Co) were prescribed for 2 weeks. The patient was recommended to gargling 0.12% chlorhexidine solution (hexomedine, Bukwang Pharmaceutical, Seoul, Korea) twice a day for 1 week, and asked not to blow her nose. Sutures were removed after 14 days. The surgical site healed uneventfully.

Four months after bone graft (Figure 3h), buccal and palatal mucoperiosteal flaps were reflected under local anesthesia for implant placement. The recipient site had healed well with ossified bone, and the OAF was closed. Core-biopsy was performed using a Ø2.0-mm trephine drill at the site of implant placement for histologic analysis to confirm that the implant site had high quality bone successfully regenerated using autogenous block bone. The specimen was fixed in formalin for histologic examination. Additional drilling was done using twist drills as per manufacturer's protocol at the biopsied site. Then, 2 sandblasted, large-grit, acid-etched textured implants (Implantium, Dentium) of Ø4.3 mm × 10 mm and Ø4.8 × 10 mm were placed in grafted and native bone (Figure 3i). Primary stability of the implants was achieved. The flap was closed after the healing abutments were inserted (Figure 3j). The same antibiotic and nonsteroidal anti-inflammatory medications were prescribed for 7 days. The same chlorhexidine solution prescribed also for 1 week. Six months after implant placement, the final prosthesis was delivered (Figure 3k). Osseointegration was achieved in the implant placed at the grafted site. Two years after prosthesis delivery, the patient's chewing function was maintained without any sinonasal complications. Only a small buccal gingival recession occurred at the implant placed in the grafted bone site (Figure 3l).

The biopsied specimen was fixed in 10% formalin solution and embedded in paraffin after decalcification. The specimen was sectioned for histological examination and then treated with hematoxylin and eosin stains (H-E staining). Histological analysis was performed using a light microscope (BX-51, Olympus Optical, Tokyo Japan) (Figure 4a). De novo bone formation was observed in the sinus floor portion due to the rich vascularity of blood vessels. Osteoblasts and osteocytes were also observed (Figure 4b and c). However, in the crestal ridge portion of the autologous block bone, there was not much ingrowth of blood vessels. New bone formation was not found except in close vicinity of the blood vessels. Some osteocytes and osteoblasts were observed (Figure 4d and e).

Panoramic radiography and CBCT images were taken after the bone graft (Figure 5a and e), implant placement (Figure 5b and f), prosthesis delivery (Figure 5c and g), and at 2-year follow up (Figure 5d and h), respectively. Schneiderian membrane thickening did not decrease significantly 2 months post FESS (Figure 5e). After closure of the OAF, the sinus ostium obstruction gradually resolved (Figure 5f), and the mucosal thickening also reduced significantly (Figure 5g and h).

Long-standing peri-implantitis can cause severe bone loss around the implant, resulting in compromised extraction socket after removal of failed implant. The compromised implant extraction socket has delayed healing and poor bone quality.¹³  Moreover, there are reports that late sinus graft infection and maxillary sinusitis can occur with peri-implantitis although they are rare.^4,5  As MSA is becoming more popular, the occurrence of complex late complications due to peri-implantitis are also on the rise. Oroantral fistula is occasionally encountered in late complications of peri-implantitis.^4,5  If late sinus graft infection/sinusitis is accompanied by an OAF, management of complication becomes more involved. In addition, if a new implant is to be placed at the failed implant site with an OAF, the OAF must be reconstructed with bone, not soft tissue. This case report showed a successful management of such complication using a staged approach in which the sinusitis was addressed first and then the OAF. The patient was first treated with FESS and then the remaining OAF was closed using a press-fit block bone graft obtained from maxillary tuberosity. New implants could then be placed. Functions could be well maintained without sinonasal complications during a 2-year follow-up period.

In a challenging case involving combined sinus and implant complications such as in this report, it was difficult to decide between FESS by an otolaryngologist and intraoral approach by an oral surgeon. Of course, the main cause of the disease was sinus graft infection due to peri-implantitis, so the intraoral approach proposed by Park et al^4,5  could be considered. However, first, accessibility was limited due to the elevated sinus floor after MSA. Second, it was necessary to remove the floating necrotic graft particles in the maxillary sinus and to unblock the chronically obstructed sinus ostium. Because of these 2 reasons, the FESS was preferred over the intraoral approach. In a situation like the present case, there had been a report in which an intraoral approach was performed prior to FESS, but symptoms did not improve.⁴  In the present case, the patient's symptoms improved dramatically after FESS, but the OAF was not closed and the thickening of mucosal membrane remained. Membrane thickening was due to the invasion of oral bacteria into the maxillary sinus through the OAF. Subsequently, the closure of OAF via an intraoral approach was required after FESS.

A number of different bone grafts have been used successfully for bone augmentation in various types of peri-implant defects and pneumatized maxillary sinuses. Autograft has been evaluated as the golden standard among bone graft substitutes.¹³  However, grafts other than autogenous bone have shown long-term implant survival and excellent clinical outcomes for peri-implant regeneration and MSA.^1–3  Also, there are reports of closure of OAF with the use of synthetic bone graft and resorbable membrane.^4,7  However, it is difficult to achieve 3-dimensional bone regeneration using particulate grafts,¹⁴  and OAFs grafted with particulate bone are prone to reoccur. In the present case, the use of particulate bone would have been inappropriate because of the defect's large size, and the frequent and strong air pressure transmitted to the OAF site because of the patient's habit of nose blowing. Therefore, the authors believe that using an autogenous block bone was the appropriate choice due the need to fill a large defect predictably and the graft's capacity to become well integrated with the surrounding bone—thus enabling future implant placements. The biopsy performed showed that the implant was placed in vital bone that was successfully regenerated using autogenous block bone.

In the healing of autogenous block bone grafts, immobilization and revascularization are critical factors for graft survivability.^10,15  In general, immobilization of block bone grafts is performed using a fixation screw. However, in the present case, it would not be appropriate to use a fixation screw because the recipient site is an OAF without apical bone support. Therefore, graft immobilization was achieved as a press-fit effect between the block bone graft and the bony walls of the OAF site without the use of a fixation screw.^16–18  The press-fit effect indicates a mechanical connection due to the contact pressure between the 2 structures.¹⁶  To maximize the effect, the diameter of the block bone must be larger than the OAF, and the cortical layer must be adequately included. In the present case, this procedure was performed by securing the block bone into the OAF site with a Summers osteotome.

Intraoral donor sites for autogenous bone graft include symphysis, ascending ramus, zygomatic alveolar crest, tori, and maxillary tuberosity.^19–24  Iliac and calvaria are used as harvesting sites for extraoral block bone grafts.^25,26  Harvesting of autogenous block grafts is associated with greater morbidity compared with particulate bone.²⁷  In general, maxillary tuberosity is often composed of osteoporotic bone and fatty marrow, and so it is not a suitable donor site. However, in the present case, due to the continuous loading of the No. 2 tooth, the maxillary tuberosity maintained a high bone density. In addition, the maxillary tuberosity was adjacent to the OAF site, and harvesting the tuberosity would decrease the vertical height discrepancy between the tuberosity and the OAF. Therefore, the maxillary tuberosity was the most suitable donor site to repair the OAF in the present case.

The most important concern for all autogenous grafts is volumetric changes after healing, including surface resorption.^25,28  However, surface resorption can be reduced by using barrier membranes.²⁹  In the present case, the block bone fixed in the OAF showed little volumetric change due to adequate blood supply and the resorbable membrane. However, in clinical findings 2 years after the final prosthesis delivery, a slight gingival recession occurred only in the implant placed at the OAF site, suggesting that the grafted bone exhibited more volume change than the adjacent native bone. However, no change in the level of grafted bone was observed in the radiograph. Nevertheless, it seemed necessary to place the implant subcrestal to an appropriate depth in consideration of the surface resorption that occurs during the remodeling process of grafted bone.

The grafted bone was well incorporated with the surrounding bone 4 months after the surgery. As shown in core samples obtained during implant site preparation, bone regeneration in the deep portion of the defect site had taken place. On the other hand, few viable cells were seen in the crestal ridge portion. The presence of viable osteocytes indicated the survival of the grafted bone. In restricted areas of ridge crest portion, new bone formation was only observed around the newly developed vascular network. This demonstrated that the healing period of 4 months was slightly short for implant placement at the grafted site. However, during implant osteotomy at the grafted site, bone density and initial stability of the implants were excellent, indicating a conflict in histological and clinical findings. Rocchietta et al¹⁵  noted that 42.34% of bone-to-implant contact can be observed when the mandibular posterior ridge previously grafted with autogenous bone block was reentered 6 to 10 months after implant placement. In the present patient, osseointegration was achieved at 10 months after block bone graft, when the prosthesis was delivered.

Complications due to peri-implantitis occurring at MSA sites are very diverse. Late sinus graft infection, maxillary sinusitis, paranasal sinusitis, implant displacement into the sinus cavity, and OAF may occur alone or in combination.⁵  A wide variety of procedures can be selected depending on the size of the defect, invasion into adjacent anatomical structures, whether a referral to an otolaryngologist is indicated, and future implant treatment plans. Supportive periodontal therapy should be performed regularly to prevent peri-implant diseases. Clinicians must respond to possible complications caused by peri-implant diseases quickly.

The disadvantage of the present case report is that there is a limit to what conclusions can be drawn from a single case. However, the authors believe that this case report highlights what is possible, and it may help in the treatment of other complicated cases.

Within the limitation of the present case report, the staged approach via FESS and intraoral press-fit block bone graft can be used to successfully replace implants at an OAF site with sinus graft infection/sinusitis caused by advanced peri-implantitis.

The authors would like to thank Dr Young-Jin Kim at Yul-Lin ENT clinic for his help in performing endoscopic sinus surgery.