Since the introduction of lateral sinus floor augmentation into the field of dental implantology, several concepts have been proposed regarding the etiologic factors and treatment of postoperative maxillary sinusitis after a lateral sinus floor augmentation procedure.1–8 Mucosal thickening, caused by surgical trauma or sinus membrane perforation, adversely affects the mucociliary clearance and ostium patency and, thus, increases the probability of developing postoperative maxillary sinusitis.9–11 It was also reported that problems of the ostiomeatal complex can affect outcomes of maxillary sinus augmentation.6
There have been a few reports of postoperative maxillary sinusitis caused by infections in the sinus bone graft.12,13 A sinus graft infection occurs in the grafted bone beneath the elevated sinus membrane. The infection source can be introduced through the perforated maxillary mucosa or via contact with skin, oral mucosa, and saliva during delivery of the bone graft material into the oral cavity. Postoperative maxillary sinusitis is an infection that occurs in the elevated sinus mucosa or the maxillary sinus. Therefore, the characteristics and treatment of these 2 diseases may be considered different12 ; however, distinguishing between them by means of clinical symptoms alone, without the assistance of radiographic examinations like cone-beam computerized tomography (CBCT), can be challenging. Infection of the sinus graft may reach the sinus membrane through the bone graft, and progression to concomitant sinusitis may occur.14
The ultimate goal of treating a postoperative sinus graft infection is long-term implant survival. To treat sinus graft infection, antibiotic administration, incision and drainage (I&D), defect degranulation, Caldwell-Luc surgery, and endoscopic sinus surgery have been reported.13, 15–19 Most reports suggest that total removal of the sinus graft and removal of the contaminated implant are the only treatment.12,14,17 In this regard, the transnasal approach has received more attention than the intraoral approach, because the concomitant sinusitis invades the nasal cavity and other paranasal sinuses through the maxillary ostium.1,3 However, for the treatment of sinus graft infection, only the intraoral approach was performed in this study because sinus graft infection is not a problem of a sinus membrane but is caused by bacterial contamination of sinus graft material during the lateral sinus floor augmentation procedure. The treatment protocol for sinus graft infection has not been established yet, and to the best of our knowledge, literature on the importance of treatment timing has not been reported to date.
The purpose of the current study was to evaluate the long-term clinical and radiologic outcomes of different timings in the treatment of postoperative sinus graft infection after lateral sinus floor augmentaion.
Materials and Methods
This study was approved by the National Institute for Bioethics Policy (PO1-201808-21-014). Figure 1 summarizes the procedures performed in this study.
Lateral sinus floor augmentation procedure
From 2003 to 2017, 307 patients (741 implants) underwent lateral sinus floor augmentation and simultaneous implant placement in a private clinic. Patients who had an acute infection of endodontic or periodontal origin, an upper respiratory infection, and a history of treatment or surgery related to the maxillary sinus were excluded from the study. All patients received oral administration of 2.0 g amoxicillin (600 mg clindamycin for patients with penicillin allergy) for prophylactic antibiotic coverage 1 hour before the lateral sinus floor augmentation procedure. Under local anesthesia, a full-thickness flap was reflected, and an ovoid-shaped lateral window was formed in the facial bone. The facial bony window was pushed up, and the sinus membrane was carefully elevated with a surgical curette. The presence of membrane perforation was confirmed visually and by means of the nose-blowing test. Membrane perforations with dimensions greater than 3.0 mm were covered with absorbable collagen membrane (CollaTape, Zimmer, Carlsbad, Calif). Bone graft materials were demineralized freeze-dried bone (Dembone, Pacific Coast Tissue Bank, Los Angeles, Calif), deproteinized bovine bone mineral (Bio-Oss, Geistlich, Biomaterials, Wolhuson, Switzerland), and a mixture of deproteinized bovine bone mineral and nonresorbable hydroxyapatite (Calcitite, Centerpulse Dental Inc, Carlsbad, Calif). The implants were all external-hexed type. The surface texture of each implant was machined surface, hydroxyapatite (HA)–coated, titanium plasma spray–coated, and sandblasted, large grit, acid-etched. The lateral window area was not covered with a resorbable membrane. The flap was sutured to provide tensionless primary closure. Systemic antibiotics (amoxicillin clavulanate potassium 375 mg) and nonsteroidal anti-inflammatory drugs (3 tablets per day) were prescribed for 7 days. Patients were advised to rinse their mouth with a 0.12% chlorhexidine solution for 1 minute, twice a day, for 1 week and were asked to not blow their nose and to sneeze with an open mouth.
Diagnosis and preoperative examination of sinus graft infection
Sinus graft infection occurred acutely within 2 weeks after lateral sinus floor augmentation procedure. Seven patients were diagnosed with sinus graft infection based on clinical symptoms alone. Oral symptoms observed included severe edema, fistula, fluctuation, and pus discharge; nasal symptoms were mucoid rhinorrhea, nasal obstruction, nasal stiffness, foul odor, postnasal drip, facial pain, infraorbital tenderness, and headache (Table 1). In patient 1, concomitant sinusitis with sinus graft infection involved the middle meatus of the nasal cavity and anterior ethmoid sinus on computed tomography (CT) (Figure 2).
The following data were obtained from 7 patients: patient demographics (age and sex) and characteristics (smoking), implant characteristics (diameter, length, and surface texture), and presence or absence of sinus membrane perforation (Table 1).
Treatment of sinus graft infection
All 7 patients with sinus graft infection in the current study underwent treatment through the intraoral approach. The patients were classified into 3 groups; group I, group II, and group III, based on the timing of I&D. In group I (n = 3), Immediately after manifestation of clinical symptoms, I&D was performed. In group II (n = 2), the patients received systemic antibiotics therapy (amoxicillin clavulanate potassium 375mg, 3 times a day) for 1 week before I&D. In group III (n = 2), patients received systemic antibiotic therapy (amoxicillin clavulanate potassium 375mg, 3 times a day) for 2 weeks before I&D. In addition, all patients were prescribed systemic antibiotics and nonsteroidal anti-inflammatory drugs for 2 weeks after I&D. Patients with penicillin allergy were prescibed 300 mg levofloxacin for the same duration.
The I&D procedure was performed as follows:
Under local anesthesia, an incision was made mesiodistally to expose the infected area. The wound periphery was sutured with an absorbable suture material to keep it wide open (Figure 3).
Infected bone graft particles were removed, and pus was drained. Copious saline irrigation was performed, and Nu gauze packing strips (Johnson & Johnson, New Brunswick, NJ) were inserted (Figure 4).
The Nu gauze was removed after 1 week, and no additional Nu gauze was inserted. Natural drainage was permitted.
Additional treatment and prostheses delivery
At the 2-month follow-up after the I&D procedure, the wound was almost closed with secondary wound healing, leaving only a small trace (Figure 5). Under local anesthesia, surgical reentry was performed for additional treatment. The infected site was opened and degranulated (Figure 6). The boundary between the infected and healthy graft zone was clearly demarcated. Removal of the residual infected sinus graft and implant, detoxification using 100 mg/mL tetracycline HCl (tetracycline HCl 500 mg powder was mixed with 5 cm3 physiological saline solution), implant replacement, and additional bone grafts were selectively performed according to the extent of sinus graft infection and degree of implant stability (Figures 7 and 8). The implants that exhibited less than 10 Ncm of removal torque or displayed mobility during degranulation of the infected graft particles were removed.
In group I, defect degranulation and detoxification using 100 mg/mL tetracycline HCl were performed 2 months after I&D. The contaminated implants were not removed because the remaining sinus graft was well preserved, and the implant stability was good. After copious saline irrigation, the additional bone grafting procedure was performed without membrane covering, and the surgical site was closed with primary intention. Nonresorbable HA (Calcitite, Centerpulse Dental Inc) or biphasic calcium phosphate (Osteon III, Genoss, Suwon, Korea) was used for additional bone grafting procedures. In patient 1 with concomitant sinusitis, the involvement of ethmoid sinus was resolved, and mucosal thickening decreased after intraoral approach. Additional bone grafting was performed (Figures 9). After 2 or 3 months of additional treatment, that is, 4 to 5 months after maxillary sinus grafting, all implants were uncovered. The final prostheses were delivered after 2 months.
In group II, additional treatment was performed 2 months after I&D. Of the 4 implants, 2 were removed because of loss of implant stability. The removal torques of these implants were less than 10 Ncm. The other 2 implants in the group were immediately placed in the new location, after defect degranulation, tetracycline HCl application for 5 minutes, and copious saline irrigation, and the additional bone grafting procedures were performed. Uncovering was performed 5 or 6 months after implant replacement, and the final prostheses were delivered after 2 months.
In group III, the defect in the sinus graft was too wide to decontaminate the entire infected site. In patient 6, the sinus graft was completely removed. Even though removal torques of implants were more than 30 Ncm, 2 implants had to be removed for effective removal of the contaminated sinus graft. The infected sinus graft was partially removed in patient 7, and 3 implants were removed due to implant instability. The removal torques of these implants were less than 10 Ncm. In this group, 4 implants were replaced, along with additional bone grafting procedures, 8 or 9 months follow-up implant removal. Uncovering was performed 6 months after implant replacement. After 2 months, the final prostheses were delivered.
The most recent CBCT (Rainbow CT, Dentium, Suwon, Korea) scans were used to evaluate the preserved sinus graft status and the pathologic lesions in the sinus.
Statistical analysis was applied to the patient's demographic data and was described as mean ± standard deviation. After the normality of the distribution was assessed with a Shapiro-Wilk test, the Kruskal-Wallis test was performed to evaluate the difference of the following variables: healing time, loading period, and survival rates. Analyses were performed using a commercially available software program (SPSS version 21.0, IBM Corp, Armonk, NY).
All 7 patients with sinus graft infection were men with a mean age of 45 ± 7.83 years. Three were smokers. The maxillary sinus membrane was perforated in 3 patients. Implant surface texture and bone graft type were also examined (Table 1).
All 7 patients with sinus graft infection showed clinical improvement. Clinical results are summarized in Table 2. The mean follow-up period was 13.28 ± 5.8 years. The prostheses in the current study were screw-retained fixed splinted crown (3 patients) or bridge (4 patients). The average healing time from lateral sinus floor augmentation to prosthesis delivery varied widely among the 3 groups: 6.7 months in group I, 9.5 months in group II, and 18.5 months in group III. However, there was no statistically significant difference among groups (P = .065). After delivery of the final prosthesis, patients were assessed at 3 months to 6 months. No clinical symptoms were observed during implant loading.
In group I, most sinus graft was preserved in all 7 patients. All 9 implants survived. After intraoral treatment in patient 1, the sinus graft infection with concomitant sinusitis and the ethmoid sinus infection resolved. The remaining implants were well maintained. Neither membrane thickening nor pathologic lesion was found in the CBCT views of patient 2 (Figure 10). However, after 9 years of loading, 1 implant had to be removed due to peri-implantitis in patient 3.
In group II, both the remaining implants (n = 2) and the replaced implants (n = 2) performed well for 9 and 15.7 years, respectively, after implant loading. In patient 4, the CBCT scan showed partial preservation of the sinus graft (Figure 11). In patient 5, almost the entire sinus graft was preserved.
In group III, the 4 replaced implants were well maintained for 13.7 years to 16.4 years after implant loading. The CBCT scan of patient 6 showed no trace of maxillary sinus graft material because it was totally removed at the time of surgical reentry (Figure 12). In patient 7, the sinus graft was partially preserved.
Sinus membrane perforation can cause postoperative mucosal edema, which can adversely affect ostium patency and mucociliary clearance,10,11 and bone graft particles can be dislodged into the maxillary sinus.2,15 Postoperative maxillary sinusitis is more frequent in cases with membrane perforation.7,13,20,21 However, postoperative maxillary sinusitis may occur without membrane perforation. In this study, sinus membrane was not perforated in 4 of the 7 patients with sinus graft infection. Membrane perforation is not essential for development of a sinus graft infection. Postoperative maxillary sinusitis is presumed to be caused by bacterial contamination, which occurs during the delivery of bone graft material into the maxillary sinus. In general, maxillary sinusitis can be caused by multiple etiologies of the dental origin; including periodontal or endodontic disease, root fracture, tooth extraction, and oroantral fistula.22 However, it is not well known whether these factors influence postoperative maxillary sinusitis or sinus graft infection.
Sinus graft infection was diagnosed mainly on the basis of clinical symptoms. Generally, postoperative swelling peaks 48 to 72 hours after oral surgery and is fully resolved 1 week after the procedure. However, patients with sinus graft infection had clinical symptoms, including severe swelling and several symptoms of rhinitis or sinusitis, 7 to 14 days after the lateral sinus floor augmentation procedure. For diagnosis of sinus graft infection, CBCT is not always necessary. If symptoms were not improved despite graft infection treatment for more than 3 weeks, CBCT was recommended because sinus graft infection may progress to maxillary sinusitis combined with another paranasal sinus.12 Delayed treatment of sinus graft infection increases the necessity for CBCT.
Several methods have been introduced for treating maxillary sinusitis after lateral sinus floor augmentation.16,18,23–25 Currently, the focus is on endoscopic sinus surgery.16,18,19,25,26 This may be because postoperative maxillary sinusitis involves the middle meatus of the nasal cavity and another paranasal sinus.26 However, in the current study, only the intraoral approach was considered in treating sinus graft infection. This approach was selected because the cause of sinus graft infection was presumed to be an infection within the bone graft and not an external problem.
Postoperative maxillary sinusitis is an infection in the maxillary sinus. Infection can be treated with antibiotics or endoscopic sinus surgery without intraoral treatment.16,24,25 However, intraoral symptoms, such as intraoral swelling and fluctuation, were present in this study. Intraoral treatment performed within 2 weeks relieved all clinical signs and symptoms, and no additional rhinologic treatment was necessary. This suggests that the etiology of sinus graft infection originates from within the sinus graft. However, sinus graft infection may progress into the sinus membrane and result in concomitant sinusitis. Postoperative maxillary sinusitis may be caused by ostium obstruction due to postoperative mucosal thickening, ostium plugging of bone graft material, and problems of the ostiomeatal complex; nonetheless, it may also be caused by the progression of a sinus graft infection.4–6 Clinically, it is difficult to distinguish a sinus graft infection from postoperative maxillary sinusitis. In the present study, 7 patients with sinus graft infection presented with oral symptoms and symptoms of sinusitis. Maxillary sinusitis caused by sinus graft infection could be treated by means of the same regimen because the infection source was assumed to be the graft materials.
It is also reported that the use of antibiotics alone exacerbated sinus graft infection.14 The empirical use of antibiotics limits their therapeutic efficacy in treating sinus graft infection. Implant survival rate and preservation of bone graft were poor in patients who had delayed I&D because of the prolonged use of antibiotics. In patients who underwent I&D immediately after the manifestation of clinical signs and symptoms, defect size and contamination range were small, and thus, the implant survival rate was increased and preservation of the sinus graft was possible.
Urban et al14 reported that the infected sinus graft was removed and detoxification was performed using doxycycline putty in the acute stage of sinus graft infection. If infection is severe, sinus grafts are mostly infected and scattered in the pus. It is reasonable to maintain an open wound for additional drainage. The sinus membrane surrounding the sinus graft is thickened by inflammation, and the boundary between healthy and infected graft material is not clearly demarcated. Identification of infected grafts is subjective and requires a lot of clinical experience. In this study, the wound was not primarily closed after I&D but was left open and underwent secondary healing to facilitate additional drainage. After 2 months of healing, only a small trace of the infection site was observed, and no remaining infection was detected. Two months after I&D, surgical reentry for additional treatment showed a clear distinction between the healthy graft zone and the infected granulomatous zone; thus, the contaminated graft materials could be easily removed.
In this case series, 2 machined surface implants and 16 rough surface implants were placed. Contamination of the rough surface by infection can adversely affect the long-term survival of implants.27 An air-powder abrasive and tetracycline HCl irrigation have been used for surface treatment of implants contaminated with peri-implantitis.28 Tetracycline HCl reportedly kills microorganisms on the contaminated implant surface, removes endotoxin from the implant surface, and inhibits collagenase activity.29,30 In this study, neither an air-powder abrasive nor a titanium brush was used during the treatment of sinus graft infection. The short duration of implant contamination resulted in positive clinical outcomes, even with chemical detoxification alone. However, care should be taken to prevent particle migration into the maxillary sinus. A recent in vitro study reported that the presence of local delivery agent residues on implant surfaces might interfere with reosseointegration and act as a reservoir of microorganisms without drug efficacies.31 Researchers have also suggested that more attention is necessary during cleaning procedures of local delivery agents. In fact, detoxification with tetracycline HCl has yet to be performed on an empirical basis. In addition, tetracycline HCl is not commercially available to dentists or physicians for clinical use.
In the simultaneous implant placement with lateral sinus floor augmentation, infection can be the cause of implant loss.13 On the other hand, in the staged approach, risk is reduced because simultaneous implant placement is not done. Of the 18 implants with sinus graft infection, 8 were removed for effective defect degranulation or lack of implant stability. Nevertheless, 10 contaminated implants survived after the intraoral infection treatment. One implant was removed at 9 years due to peri-implantitis. Six replaced implants survived. The preserved sinus graft was healthy enough to maintain implant stability. This result contradicts previous reports12,14,17 claiming that removal of implants and sinus grafts is mandatory for treating sinus graft infection or postoperative maxillary sinusitis.
Additional bone grafting procedures on a previously infected graft site should be performed carefully because residual infection can remain in the sinus graft and the detoxified implant surface. However, in this study, positive clinical results were obtained after additional bone grafting, probably because of early initiation of treatment for sinus graft infection and the effect of tetracycline HCl detoxification.
If signs and symptoms of sinus graft infection persist beyond 3 weeks, the need for endoscopic sinus surgery should be assessed.12 Endoscopic sinus surgery will restore normal sinus function and ventilation through the natural ostium.25,32 It has been reported that 1-stage surgery performed under general anesthesia was also used to treat chronic maxillary sinusitis after sinus augmentation.18 However, endoscopic sinus surgery cannot resolve infections in the sinus graft and can only treat rhinitis and paranasal sinusitis, the secondary phenomenon, subsequent to sinus graft infection. This case series revealed that good clinical results can be obtained only with intraoral infection treatment under local anesthesia in cases of sinus graft infection or concomitant sinusitis after lateral sinus floor augmentation. Therefore, the intraoral approach in the treatment of sinus graft infection is mandatory and must be performed in all sinus graft infection cases. In particular, the combination of immediate pus drainage and additional treatments, such as defect degranulation, tetracycline HCl detoxification, and additional bone graft, showed the best results, and the healing time was similar to that of a normal sinus floor augmentation.
This study has several limitations. It was a retrospective study with an inherent bias, and the sample size was small. With the limitations of a case series, the results and outcomes of the treatment of sinus graft infection varied with the timing of pus drainage.
The prolonged use of antibiotics without I&D could be detrimental for implant survival and preservation of sinus bone graft. This study showed that I&D performed immediately after clinical manifestation, combined with 2 weeks of antibiotics, was the most effective treatment for sinus graft infection. To determine a more accurate and evidence-based approach for intraoral treatment of sinus graft infection, more controlled randomized clinical studies with large sample size are needed.
The authors would like to thank Dr Young-Jin Kim at Yul-Lin ENT clinic for his help in diagnosing maxillary sinusitis with CBCT, and Sung-Bae Park for illustration of figures.
The authors report no conflicts of interest with respect to this study. There is no funding related to this study.