Complication and Salvage of Sinus Floor Elevation in the Maxillary Sinus With Asymptomatic and Noncalcified Fungus Colonization: A Case Report

Sinus pneumatization is a limiting factor of dental implant placement in the posterior maxilla. In such a situation, sinus floor elevation (SFE) can be used to achieve sufficient vertical bone height. Evidence has demonstrated that SFE using a variety of techniques and biomaterials results in a high implant survival rate.^1,2 

Despite successful outcomes reported by many studies, several predisposing risk factors are presented in SFE.³  Such factors can be classified into anatomical variations, sinus pathology, and surgically induced events (eg, sinus membrane perforation). Clinicians should carefully assess the maxillary sinus and the neighboring structures to avoid undesirable consequences before surgery using modern radiographic technology. Sinus membrane thickening may be the finding of most interest in the preoperative assessment. Studies demonstrated that sinus membrane thickening in some morphologies and above a certain threshold thickness can escalate the risk of complications,^4–6  as a thickened sinus membrane may indicate present pathologic conditions or a high risk of ostium obstruction. Sinus membrane perforation is the most frequent adverse event during SFE and may lead to postoperative infection⁷ ; this is more likely to happen in the presence of other predisposing factors.

Patients with sinus membrane thickening may present with various symptoms, such as postnasal drip, headache, nasal obstruction, facial pain, and hyposmia. In such cases, patients should be referred to an otolaryngologist in advance, but clinical outcomes may be somewhat unsatisfactory because of heterogeneous pathology (bacterial, viral or fungal infection). Moreover, some cases of sinus membrane thickening, despite being severe, are asymptomatic.⁸  This situation might make clinicians unwary of potential danger and choose to perform risky surgery.

The present study aimed to report (1) the sequela of SFE in the posterior maxilla with severe membrane thickening and fungal colonization but a patent ostium and (2) a treatment course without implant removal.

A 73-year-old woman visited a private clinic for implant placement in the left posterior maxilla. She was a nonsmoker and had no specific medical conditions presenting contraindications to dental surgery. She was previously treated with endoscopic surgery to the left sinus because of chronic rhinosinusitis. No sinonasal symptoms or signs were presented. She had no premolars or molars on the left side of the maxilla and the left/right sides of the mandible. The clinician in charge decided to place implants on the premolar and molar areas of the left side of the jaw to rehabilitate masticatory function.

A radiographic examination revealed pneumatization in the molar area of the left maxilla (Figure 1a). The septum was vertically positioned within the pneumatized sinus cavity area. In the cone-beam computerized tomography (CBCT) scans (rainbow CT, Dentium), severe sinus membrane thickening was found, but the ostium was patent (Figure 1b through d). Large Haller cells were also found. The residual bone height was 12 mm on the No. 12 tooth area, 7 mm on the No. 13 area, and 2 mm on the No. 14 area. The thickness of the lateral wall was 3.5 mm.

An otolaryngology examination revealed a healthy nasal cavity with anterior ethmoid sinuses and Haller cells (Figure 2a and b). With regard to SFE, the otolaryngologist stated that the patient was at a higher risk of postoperative complications and might require the additional treatment. The recommendation of the otolaryngologist was endoscopic sinus surgery before SFE, but the patient was refused because of her previous history of such surgery in the same area.

The patient received oral administration of 2.0 g of amoxicillin for prophylaxis 1 hour before surgery. Under local anesthesia with 2% lidocaine containing epinephrine 1:100 000, a mucoperiosteal flap was reflected, and a surgical access window was created using a carbide bur under copious saline irrigation (Figure 3 and b). The sinus membrane was carefully elevated using sinus curettes (DASK kit). The membrane was firmly attached to the sinus floor and felt heavy during its elevation. However, no membrane perforation or leakage of exudate was detected with visual inspection and saline irrigation. On the sinus floor, some tissue residue was detected and scraped off thoroughly. The implant was then placed according to the manufacturer's guideline (Ø3.8 × 12 mm for the No. 12 area, Ø3.8 × 10 mm for the No. 13 area, and Ø4.3 × 10 mm for the No. 14 area; Implantium, Dentium), and cover screws were connected (Figure 1e). No bone substitute material was grafted (Figure 3c) because of the following: (1) sufficient implant stability could be obtained because of a vertically positioned septum, (2) recent evidence indicating the predictability of graftless sinus augmentation,¹  and (3) bone graft material might be a potentially exacerbating factor in the case of postoperative complication.

To enable submerged healing, the flap was sutured (Nylon 4-0, Ethilon 4.0, Ethicon). An antibiotic (ciprofloxacin 500 mg; Ildong Pharmaceutical Co) and an anti-inflammatory drug (Etodol 200 mg, Yuhan Co) were prescribed 3 times a day for 7 days. The patient was directed to rinse her mouth twice daily with a 0.12% chlorhexidine solution (Hexamedine, Bukwang Pharmaceutical) and not blow her nose for 1 week. A CBCT scan taken immediately after SFE and implant placement revealed mucosal swelling in the maxillary sinus (Figure 1f through h).

At 1 week postoperative, the patient presented with mucoid rhinorrhea, postnasal drip, foul odor, facial pain, and severe headache. The patient was referred to an otolaryngologist. Functional endoscopic sinus surgery (FESS) was performed under local anesthesia. Because of the first FESS performed 2 years prior, no uncinate process was present. The ostium was enlarged, and the purulent exudate was drained (Figure 2c). Along with inflammatory mucosa, brownish-yellow masses were removed (Figure 2d). Meticulous saline irrigation was performed. A hemostatic gelatin sponge (Cutanplast, Brunelli) was then packed. The removed masses were fixed in 10% neutral buffered formalin solution (Sigma Aldrich) for histopathologic examination.

The following medications were prescribed for 3 weeks: Klaricid (clarithromycin, Abbott), Muteran (acetylcysteine, Hanwha Pharma Co), methylprednisolone (Jaytechbiogen), and tranexamic acid (Daiichi Sankyo Co).

Microscopic evaluation revealed a dense accumulation of fungal hyphae (Figure 4a). A radiating eosinophilic amorphous mass (ie, the Splendore-Hoeppli phenomenon) was present around the fungal hyphae (Figure 4b).

After FESS, the patient's symptoms improved over time. No implant removal was performed. Nasal endoscopy performed 2 months after the FESS revealed an enlarged ostium with clear patency and a mucosal status without inflammation (Figure 2e and f). Healing abutments were connected 6 months after SFE. The final prosthesis was delivered 1 month later. The patient was monitored every 4 to 6 months (Figure 1i and m). In CBCT scans taken 1 and 2 years after the final prosthesis delivery, the extent of the sinus membrane thickening was significantly reduced as compared with the preoperative status (Figure 1j through l, n through p). All implants exhibited successful integration. No sinonasal symptoms or signs were noted during 2 years of follow-up (Figure 3d).

The present case demonstrated (1) the risk of complications after SFE in the maxillary sinus with severe sinus membrane thickening, (2) the possibility of undiagnosed and asymptomatic fungal colonization in the thickened sinus membrane, and (3) FESS as a potential salvage treatment in the augmented maxilla with postoperative complications.

Sinus membrane thickening is not an uncommon finding on CBCT, which is true for asymptomatic patients.^5,9,10  Sinus membrane thickening is generally considered a risk factor for SFE, but very surprisingly, there are no clear guidelines regarding the threshold thickness.¹¹  implant success rates are high in the literature, even in situations with a sinus membrane thickening >15 mm and up to 22.8 mm.^10,12  These results may be contradictory with our common belief that severe sinus membrane thickening is risky in SFE, but one might suspect the importance of maintaining ostium patency over the thickened sinus membrane itself despite an insufficient evidence level.^10,12  In the present study, preoperative CBCT revealed almost complete opacification of the maxillary sinus but a patent ostium. However, this might be a misjudgment because the sinus membrane becomes swollen immediately after SFE.¹³  In a healthy sinus, postoperative sinus membrane swelling decreases without complications,^13,14  but in a sinus like in the present case, the swelling can significantly interfere with ostium function and lead to sinusitis. Moreover, the presence of Haller cells should have been more critically considered. Haller cells, known as infraorbital ethmoidal air cells, do not indicate a pathologic state, but large Haller cells can interfere with mucociliary action by compressing infundibulum.^15,16  Some studies have revealed the association between Haller cells and rhinosinusitis.^17,18  In a retrospective study assessing the correlation between anatomic variants and complications following SFE, only the presence of Haller cells was significantly associated with complications.¹⁹ 

The presence of fungal colonization in the maxillary sinus was undiagnosed in the present case. Fungal rhinosinusitis is classified into invasive and noninvasive types with subtypes.²⁰  Invasive fungal sinusitis involves neighboring anatomic structures, such as the palate, nasal septum, orbit, and other nasal sinuses. Patients with an abnormal immune system are vulnerable to developing invasive fungal sinusitis. In the clinical setting, it is relatively easy to refer the patient with this invasive type to the relevant medical field. However, noninvasive fungal colonization/sinusitis may not be easy to diagnose, especially in the dental clinical setting. Despite the presence of fungal colonization, patients are commonly asymptomatic.²⁰  Moreover, the radiographic diagnosis of fungal colonization was also difficult to make. Computerized tomography often reveals the presence of heterogenetic opacifications or metallic structures in the sinuses with a fungal ball,²¹  but the prevalence of calcification in patients with a fungal ball was reportedly less than 80%.^22–24  Otherwise, the fungal infection should be confirmed by biopsy material collected intraoperatively.²⁵  In the present study, the patient was an older women who presented with unilateral sinus involvement, which might fit with the clinical features of a fungal ball, but evidence to confirm this was insufficient. As sources of the fungal infection, contradictory findings were reported regarding overfilled dental materials.^20,26  Others demonstrated that previously failed sinus bone grafting was responsible for fungal sinusitis.²⁷ 

A histopathologic examination revealed densely packed hyphae with eosinophilic material. The formation of this eosinophilic material is called the Splendore-Hoeppli phenomenon.²⁸  The deposition of antigen–antibody complexes and debris from the host inflammatory cells are the suspected mechanisms behind this phenomenon. Fungal infection, such as aspergillosis (which predominantly induces fungus balls), zygomycosis, and candidiasis, often accompanies this phenomenon.

One should bear in mind that there was a still possibility of combined infection involving both bacteria and fungi in the present case. In previous studies regarding post-SFE infection, various bacteria (Staphylococcus aureus, Staphylococcus epidermidis, Eikenella corrodens, etc) as well as fungi (Penicillium species, Candida parapsilosis, Exophiala species, Aspergillus species) were found.^27,29  The culture of mucopurulence can further help to determine the infection source,²⁹  together with histology.

One of the particular findings is the status of the sinus membrane. During membrane elevation, the membrane felt as though it was crusted over the floor of the sinus. Consequently, some soft residue was detected after elevation. This might be attributable to osteitis in the bone walls neighboring the thickened sinus membrane³⁰  and a subsequent inflammatory change of the periosteum side of the sinus membrane.

In the present case, post-SFE sinusitis could be managed with FESS. In the literature, post-SFE sinusitis was treated with medication and intraoral/endoscopic sinus surgery. In the present case, if the initial treatment had consisted of medication including antibiotics, the sinusitis would have not been properly managed, because the resident fungus was the main source of the infection. The treatment of fungal balls consists of endoscopic sinus surgery, which exhibits a high success rate.²⁶  Even for asymptomatic patients with a fungal ball, this treatment is generally recommended.²⁰  After FESS in the present study, the patient's clinical symptoms were alleviated, and the mucosal thickening was also significantly reduced. No sinonasal symptoms or signs were noted during the 2 years of follow-up. However, it should be considered that SFE under a pathologic sinus situation followed by collateral medical referral is obviously undesirable for patients in terms of both health and cost.^11,31 

Implant removal was not performed in the present case. This decision was mainly based on incontinuity between the implant placed and intramural spaces. Even in cases of sinus perforation inducing a postoperative infection, FESS may be a salvage treatment for dental implants, but only limited evidence based on case studies is currently available.^29,32  The long-term survival of dental implants should be carefully monitored.

The etiology of sinus membrane thickening should be carefully assessed. Dentists should be aware of various contributing factors to the thickened sinus membrane, such as fungal ball in the present case. Depending on the severity of the sinus membrane thickening, more cautious pre-SFE management is required, including prophylactic medication over a certain period. In cases of post-SFE sinusitis, an early referral for FESS may resolve the infection and salvage the SFE.

Abbreviations

CBCT:

cone-beam computerized tomography

FESS:

functional endoscopic sinus surgery

SFE:

sinus floor elevation

The authors thank Jung Sun Jang, Medical Device Evaluation Team Manager, in Genoss (Suwon, Korea) for his histopathology contributions.

The authors report no conflicts of interest related to this case report.