Aspergillosis of the Maxillary Sinus Associated With Dental Implant

Sinusitis is a common disease that affects 1 in 7 adults.¹  A total of 10% of all sinusitis cases are of dental origin (odontogenic sinusitis).²  Acute or chronic bacterial sinusitis after a dental implant procedure has been frequently reported. However, fungal infection in the maxillary sinus has rarely been reported.³  Fungal sinusitis can be chronic or acute and can be classified as noninvasive or invasive based on fungal invasion of the tissue.⁴  Aspergillosis is a fungal disease caused by the fungus Aspergillus that involves the lungs and occasionally the maxillary sinus. Aspergillus is ubiquitous to the environment, as it is in soil, dust, and foods. Aspergillosis is rare in nonimmunocompromised patients.⁵  However, it can affect patients with compromised immunity. Invasive aspergillosis usually occurs in patients with altered host defense. It can spread rapidly to the nearby structures or systemically to the brain, lungs, heart, or kidneys and lead to mortality. The noninvasive form usually occurs in healthy patients. Aspergillosis in the maxillary sinus typically has the characteristics of the noninvasive form. De Foer et al⁶  suggested that spores of aspergillus may be inhaled into the maxillary sinus via the osteomeatal complex or via an oroantral fistula following dental procedures, such as an extraction.

This report presents 4 unusual cases of localized aspergillosis in the maxillary sinus associated with dental implant treatment in healthy individuals.

In the Department of Oral and Maxillofacial Surgery of Kyungpook National University Dental Hospital, 9 patients have been diagnosed with aspergillosis in the maxillary sinus (2013–2017). Four of the patients had implant-related aspergillosis. These 4 patients were initially treated with conservative antibiotic treatment or implant removal at the local clinics. Thereafter, they were transferred to the authors' department because the symptoms were not completely resolved. Patients underwent surgical curettage and thorough sinus irrigation. Histopathologic examination revealed several inflammatory cells around the maxillary sinus mucosa, and typical features of aspergillosis, including much branching and septic hyphae, were presented (Figure 1). Broad-spectrum cephalosporin antibiotics were administered to the patients before and immediately after the procedure. The postoperative prognosis was uneventful, and there was no recurrence in any patients.

A 61-year-old male with well-controlled hypertension presented with a history of the left maxillary molars (#14 and #15) having been extracted 14 months previously at a local dental clinic. After 5 months, the patient underwent dental implant installation with maxillary subantral sinus bone augmentation. Seven months following implant surgery, the fixture was fractured, and the implant was removed at the same dental clinic. However, the implant removal site did not heal adequately. The patient was transferred to our department due to symptoms of chronic headache and an oroantral fistula (OAF) with purulent discharge that had persisted for 3 months. Radiographic findings showed that radiopaque graft materials were scattered inside the left maxillary sinus, and sinus haziness was noted. Under local anesthesia, all the necrotic bones and previously grafted materials in the maxillary sinus were removed and thoroughly irrigated with normal saline (Figure 2). The OAF was closed with a buccal gingival advancement flap. The histopathologic diagnosis was maxillary aspergillosis at the maxillary sinus. Antibiotics (methylol cephalexin lysinate, cephamethyl, Daehwa Pharmaceutical Co, Ltd, Seoul, South Korea) were administrated for 3 weeks (2 weeks before surgery and 1 week after surgery), and healing was uneventful 3 months postoperatively.

A 63-year-old female with moderately controlled diabetes and hypertension visited presented with intermittent headache, dull pain in the left maxilla, and nasal congestion that had persisted for 3 months. This patient had undergone implant surgery 6 years ago, and there was no discomfort before the onset of symptoms. Radiographic findings showed that the installed dental implant lost osseointegration and migrated into the maxillary sinus. Under general anesthesia, a left anterior maxillary window was created to access the sinus (Figure 3). The floating implant and inflammatory tissues were removed, and the sinus was irrigated thoroughly with normal saline. Nasal antrostomy was performed to ensure passage for the discharge from the maxillary sinus. The histopathologic findings showed the hyphae structure, a characteristic feature of aspergillosis, and revealed that the hyphae were branched at an acute angle. The healing was favorable at 6-month follow-up.

A 62-year-old male presented with a chronic maxillary sinusitis after a maxillary subantral sinus bone augmentation and dental implant installation. As per the dental clinician who performed the procedure, 9 weeks after surgery, a sore spot under the temporary denture developed into an OAF. The patient complained of nasal congestion and pus discharge from the fistula. Radiographic image revealed mucosal thickening of the right maxillary sinus and floating sinus graft materials. The patient underwent surgical curettage of the maxillary sinus and nasal antrostomy under general anesthesia (Figure 4). The OAF was closed with a buccal fat pad flap. Three months postoperatively, the patient showed favorable uneventful healing.

A 41-year-old female had dental implant placement and subantral sinus augmentation at the maxillary second premolar and first molar site 6 months previously and reported discomfort and intermittent pain at the left maxilla postoperatively. Although this patient had functional endoscopic sinus surgery, symptoms of nasal congestion and pus discharge continued. This patient was presented, and under general anesthesia, all the inflammatory tissues and infected graft materials were removed and thoroughly irrigated with normal saline via the lateral window of the maxillary sinus (Figure 5). The histopathologic findings revealed chronic inflammation and aspergillosis at the infected graft site. Nine months postoperatively, healing was uneventful.

Aspergillosis spreads when airborne spores are inhaled and manifests itself in the upper respiratory tract and the lungs. In particular, 6%–9% of all sinusitis cases are caused by fungal infections.⁷  Aspergillosis is known to occur in immunocompromised patients who have a history of long-term antibiotic use or organ transplantation. Recently, cases of aspergillosis in healthy patients who had prior dental treatment, such as tooth extraction, bone graft, or placement of dental implants into the posterior maxilla, have been reported.²  Clinical manifestations of aspergillosis include frontal headache, orbicular pain, sneezing, nosebleeds, nasal congestion, and chronic sinus pain.

Previous studies have shown that systemic aspergillosis is common in immunocompromised patients; however, few cases of localized aspergillosis found in the maxillary sinus have been reported. In the previous 20 years, only a few cases of maxillary aspergillosis associated with implant treatment have been published.^8–11  In the present cases, aspergillosis occurred in healthy individuals with good general health. Sohn et al⁹  reported a case of fungal infection that would be caused by contaminated graft bone material during dental implant surgery. And they proposed a history of smoking and/or membrane perforation of the maxillary sinus during the surgical operation as a possible cause of aspergillosis. Sato et al¹⁰  reported that maxillary sinus aspergillosis was associated with zygomatic implants. During the placement of a zygomatic implant, a 2-mm maxillary sinus membrane perforation occurred. Two months thereafter, swelling developed at the operation site, and the zygomatic implant was removed under general anesthesia. The patient was diagnosed with sinusitis on clinical examination; however, the final diagnosis was aspergillosis. The author reported that the reason for the fungal infection was airborne fungus infection contracted during the operation. Harada et al¹¹  reported aspergillosis associated with the migration of a dental implant that was installed 4 years previously into the maxillary sinus. Oral antibiotics (levofloxacin and clarithromycin) were administered first; antifungal agents were not administered. Under general anesthesia, the implant that had migrated into the maxillary sinus was removed, and diagnosis was aspergillosis.

In these present 4 cases of sinus aspergillosis, 3 cases were associated with implant installation and sinus augmentation surgery. One case was related to implant migration into the maxillary sinus. Previous reports, including this present case series, address maxillary sinus aspergillosis related to dental implantation and are summarized in Table 1. Although it is difficult to know how the aspergillosis infection occurred in the maxillary sinus, the following 2 reasons could be responsible: (1) at the time of implant insertion or sinus graft, the sinus membrane was perforated and contaminated by the fungus, or (2) the maxillary alveolar process is resorbed by chronic peri-implantitis, and OAF may develop. OAF may permit the fungal infection to spread to the maxillary sinus. In both the cases, unfavorable healing with chronic sinusitis after dental implant placement with or without subantral sinus augmentation may develop into aspergillosis.

There were no immunocompromised patients in any of the reported cases, including patients in these present case reports. All 7 patients listed in Table 1 underwent antibiotic treatment with open surgical procedures, and systemic antifungal agents were not administered. Practically, it takes 1 or 2 weeks for the final histopathological reporting, and broad-spectrum antibiotics were frequently used after the curettage of the infected or necrotic lesion from the sinus. None of the above-mentioned cases used systemic antifungal agents because the symptoms improved after the surgical procedure was performed with the use of proper perioperative antibiotics. Therefore, further, systemic antifungal agents were not considered necessary due to the absence of invasive disease or in immunocompromised patients.⁸ 

Surgical treatment only is recommended for noninvasive localized maxillary sinus aspergillosis. The prognosis is good with adequately performed surgery.^12,13  In the case of invasive-type aspergillosis, antifungal agents, such as voriconazole and amphotericin B, are recommended along with proper surgical procedures.¹⁴  However, amphotericin B requires nephroprotection because of the possibility of nephrotoxicity. Besides nephrotoxicity, there are various complications of antifungal agents, such as nausea, vomiting, vision problems, fever, and swelling in the hands, ankles, or feet. Though rare, amphotericin B has ototoxicity and leads to irreversible hearing loss. Antifungal agents may be necessary if there is erosion of an anatomic barrier with bone destruction in immunosuppressed patients or if the clinical symptoms do not reduce postoperatively.¹¹ 

Radiographs provide useful evidence for the differentiation of fungal infections. According to Stammberger et al,¹⁵  the irregularly shaped high-tone region located in the center of the maxillary sinus is composed of tertiary calcium phosphate (apatite), calcium sulfate, and heavy metal salts, and then aspergillosis is deposited into the necrotic area that forms the radiopaque images. When augmented maxillary sinuses with graft materials are infected by Aspergillus, it can be challenging to clearly discriminate the fungal ball surrounding the graft materials. Therefore, nonhealed chronic maxillary sinusitis related to dental implants or sinus grafting needs particular attention because of the possibility of aspergillosis.

Localized aspergillosis may occur in the maxillary sinus area after dental implant placement in healthy people who are not immunocompromised or do not present with systemic disease. The surgeons need to be aware that nonhealed and chronic sinusitis can be maxillary aspergillosis, and it can be successfully treated with thorough surgical curettage of the maxillary sinus, including removal of the infected or necrotic tissues.

Abbreviations

DM:

diabetes mellitus

G/A:

general anesthesia

HTN:

hypertension

i:

implant

L/A:

local anesthesia

OAF:

oroantral fistula

The authors declare that they have no competing interests.