The aim of this case report was to report the course of treatment for advanced paranasal sinus infection triggered by peri-implantitis, managed using functional endoscopic sinus surgery (FESS), with outcomes. A nonsmoking male patient received sinus augmentation with implant placement on his left posterior maxilla 15 years ago. Possibly due to noncompliance to maintenance, peri-implantitis developed and progressed into the augmented bone area in the maxilla. Eventually, maxillary sinusitis occurred concomitantly with a spread of the infection to the other paranasal sinuses. Implant removal and intraoral debridement of inflammatory tissue were performed, but there was no resolution. Subsequently, FESS was performed, with removal of nasal polyp and sequestrum. After FESS, the patient's sinusitis resolved. Histologically, the sequestrum was composed of bone substitute particles, necrotic bone, stromal fibrosis, and a very limited cellular component. Two implants were placed on the present site, and no adverse event occurred for up to 1 year after the insertion of the final prosthesis. Peri-implantitis in the posterior maxilla can trigger maxillary sinusitis with concomitant infection to the neighboring paranasal sinuses. FESS should be considered to treat this condition.

Maxillary sinus augmentation has expanded the indications of implant treatment, leading to successful implant placement even in severely pneumatized maxillae.1,2  Moreover, evidence demonstrates a high implant survival rate in the grafted maxilla with lateral sinus augmentation as well as crestal sinus augmentation.3,4  At this point in time, more than 40 years since the introduction of sinus augmentation, there has been significant advancement in the technical and material points of view,57  which has resulted in an increase in the number of sinus augmentation surgeries.

However, this seems to have caused a concomitant soar in the associated complications. Mostly, these complications mentioned in the literature or scientific meetings are events that occur during the surgery and/or within a short time following the surgery, including sinus membrane perforation, implant displacement into the sinus, acute sinusitis, and chronic sinusitis.811 

In addition, we now encounter another type of complication occurring at a later point of time after treatment: the spread of the infection from the peri-implantitis to the grafted area in the maxillary sinus.12,13  Epidemiologic studies have demonstrated that peri-implantitis is not a rare disease. A recent systematic review indicated that approximately 20% of the implant patients harbor peri-implantitis of varying extent.14  Thus, in the grafted maxilla, an orthogonal progress of peri-implantitis eventually reaches the augmented bone area, possibly affecting the neighboring anatomical structures (ie, the maxillary sinus).

Previously, very few reports of the above case12,13  were made. Prolonged and untreated peri-implantitis may deteriorate the entire augmentation that was previously performed and lead to total failure of the graft, acute/chronic sinusitis, and spread of infection to other paranasal sinuses. The conventional intraoral approach for treatment may not be sufficient in this situation. To regain the disturbed physiologic function, a nasoendoscopic approach may be required, such as functional endoscopic sinus surgery (FESS).8,10 

The aim of the present study was to report the course of treatment for advanced paranasal sinus infection triggered by peri-implantitis using FESS, with the outcomes.

Previous sinus augmentation and implant placement surgery

The first surgical intervention was performed 15 years ago.

Forty-two male nonsmoking patients required implant placement in the left posterior maxilla. These patients had no relevant medical history. Because of maxillary sinus pneumatization (residual bone height = 2 mm) and severe crestal bone resorption, lateral sinus augmentation was performed simultaneously with implant placement. After flap reflection, a bony window was removed using rotary instruments, sinus membrane was carefully elevated, and nonresorbable hydroxyapatite was grafted (Calcitite, Centerpulse Dental Inc, Carlsbad, Calif). Two implants were placed, one each in the #13 (Steri-Oss Ø5.0 × 12 mm, Steri-Oss Inc, Yorba Linda, Calif) and #15 regions (Steri-Oss Ø6.0 × 10 mm, Steri-Oss Inc), and submerged healing was provided. Healing caps were connected to the implants after 6 months. The definitive prosthesis was inserted 2 months later (Figure 1a). After several follow-up (twice a year) visits for 5 years, the patient did not visit the clinic for the next 10 years.

Clinical and radiologic evaluation of the patient after 15 years

Approximately 10 years after the last visit, the patient visited the clinic with symptoms of severe headache, mucoid rhinorrhea, postnasal drip, and foul nasal odor. The mucosae around the implants were reddish and swollen. Deep probing pocket depth was measured on both implants (>6 mm on #13 implant and >12 mm on the #15 implant) with pus discharge (Figure 2a). The #15 implant exhibited mobility. In the panoramic radiograph, grafted material in the #15 region of the maxillary sinus presented with a feathery appearance (Figure 1b). Cone-beam computerized tomography (CBCT; Rainbow CT, Dentium, Suwon, Korea) revealed mucosal edema completely occupying the maxillary sinus, leading to blockage of the ostium. The grafted material was separated and embedded in the edematous mucosa. Moreover, severe mucosal edema was also present in the left anterior and posterior ethmoid sinuses (Figure 3a through e).

Intraoral approach and medication

Because of loss of osseointegration, the #15 implant was removed using forceps. Oroantral communication was observed in the #15 implant area (Figure 2b). This area was thoroughly irrigated and debrided as much as possible. Then, the wound was closed. Systemic antibiotic (ciprofloxacin 500 mg, Ildong Pharmaceutical Co, Seoul, Korea) and a nonsteroidal anti-inflammatory drug (Etodol 200 mg, Yuhan Pharmaceutical Co, Seoul, Korea) were prescribed to be taken 3 times a day for 7 days. The patient was instructed to rinse the mouth with 0.12% chlorhexidine solution (Hexamedine, Bukwang Pharmaceutical, Seoul, Korea) 2 times a day and not to blow the nose. The oroantral fistula closed, but the clinical symptoms persisted.

Functional endoscopic sinus surgery

A further intraoral approach, such as access to the lateral wall of the maxillary sinus, was considered inadequate because of (1) involvement of other paranasal sinuses, (2) complete blockage of the ostium, and (3) surgically inaccessible high maxillary sinus floor.

The patient was referred to the otorhinolaryngology clinic for FESS. Nasal endoscopic examination revealed severe polyposis and purulent discharge from the left maxillary, ethmoid, and frontal sinuses (Figure 4a). Under local anesthesia with 2% lidocaine with 1:100 000 epinephrine, polypectomy was performed, followed by the removal of the uncinate process. The natural ostium of the maxillary sinus was then expanded. In the endoscopic camera, a mixed mass of the grafted material and inflammatory tissues was observed, covered with thick and dense purulent matter. Following the aspiration of pus, the mass was enucleated (Figure 4b). The length of the mass was approximately 1.0 cm (Figure 5a). The following medication was prescribed: Klaricid (clarithromycin, Abbott Korea, Seoul, Korea), Muteran (acetylcysteine, Hanwha Pharma Co, Seoul, Korea), and methylprednisolone (Jaytechbiogen, Seoul, Korea) orally for 3 weeks along with an intravenous injection of tranexamic acid (Shin Poong Pharm Co, Seoul, Korea).

One month after FESS, mucosal edema in the maxillary sinus was still observed on nasal endoscopy. After another 5 months, the edema disappeared. The area of the oroantral communication was blocked by soft tissue.

Implant replacement after 6 months of FESS

After confirming complete resolution of the patient's symptoms and closure of the oroantral communication (Figure 6a), reimplantation was planned. After administering local anesthesia (2% lidocaine with 1:100 000 epinephrine), the flap was reflected. No residual infection was clinically detected. Because of marginal bone loss, the #13 implant was removed using a trephine bur, and a biopsy specimen was obtained. Subsequently, 2 implants were placed on the #13 (Implantium Ø4.3 × 10 mm, Dentium) and the #14 (Implantium Ø3.8 × 10 mm, Dentium) regions (Figure 6b). The bone defect area around the implants was grafted with synthetic bone substitute material (Osteon III, Genoss, Suwon, Korea; Figure 6c). Submerged healing was provided (Figure 6d). A systemic antibiotic (cefradine 500 mg, Yuhan Co) and a nonsteroidal anti-inflammatory drug (Etodol 200 mg, Yuhan Co) were administered 3 times a day for 7 days. Uncovering was performed after 6 months, and the final prosthesis was inserted after 2 months.

Clinical observation

No recurrence of symptoms was reported after FESS. The oroantral communication was completely closed. At 1 year following the insertion of the final prosthesis, the probing depth was <4 mm with no bleeding on probing.

Radiographic observation

Panoramic radiography and CBCT were performed 1 year after the insertion of the final prosthesis. In those radiographic images, the graft material in the maxillary sinus appeared stable, and no significant marginal bone resorption was observed around the implants (Figure 1c). The ostium was enlarged and had clear patency. The mucosal thickening in the maxillary sinus had disappeared (Figure 3f through h).

Histopathologic examination

The removed mass was fixed in 10% formalin solution, decalcified, and embedded in paraffin.

Sequestrum Retrieved During FESS

The histological section demonstrated bone substitute particles mixed with necrotic bone tissue. No cellular element was found in the severe stromal fibrosis. The necrotic bony tissue seemed to have slowly degenerated because of chronic inflammation (Figure 5b).

Specimen Retrieved During Implant Placement

The specimen mainly consisted of bone substitute particles and vital bone tissue. The particles were in close contact with bone tissue. Most of the lacunae were filled with osteocytes. At the periphery of the specimen, a small amount of fibrosis was found (Figure 7).

The present case demonstrated that (1) untreated and progressive peri-implantitis in the maxilla can jeopardize the previously performed sinus augmentation and provoke paranasal sinus infection and (2) in that situation, the entire treatment course becomes complex, requiring an additional nasoendoscopic approach.

Nowadays, a variety of surgical techniques and biomaterials have been introduced to overcome the insufficiency of bone volume,6,7  leading to the expansion of implant indications. Even posterior maxilla with very thin residual bone height can be successfully treated using dental implants. However, in such a situation, it is also conceivable that the progression of peri-implantitis can easily extend to the bone-augmented area, where newly formed bone is interconnected with bone substitute particles. Despite the controversy about the susceptibility of the native bone and augmented bone to peri-implantitis,1517  the augmented area may react to the infection differently from the native bone. The remainder of the bone substitute particles provide the surface for harboring the pathogenic bacteria.18  Hence, once peri-implantitis reaches the augmented sinus cavity and remains in place for a long duration, it may become a potent source for maxillary sinusitis.

Very few previous studies have reported peri-implantitis-triggered maxillary sinusitis.12,13  In those studies, aggressive intraoral surgical curettage of the grafted bone substitute material and inflammatory tissues led to complete resolution of symptoms. However, the CBCT scans and endoscopic examination of the patient in the present study showed involvement of the neighboring paranasal sinuses (ethmoid and frontal sinuses) with complete blockage of the ostium. Moreover, intraoral surgical access was very difficult because of the high sinus floor and loss of crestal bone. Therefore, this patient eventually required FESS, which enlarged the ostium for enhancing nasal clearance.

The necessity of FESS has been discussed in several articles, but the timing of the procedure was during sinus augmentation and after sinus augmentation (early healing phase).8,10,19,20  To the best of our knowledge, the present study is the first to describe the indication of FESS in a case of peri-implantitis. During FESS, a large amount of purulent matter, sequestrum, and a nasal polyp could be removed in the present case.

One particular aspect of the present case was that the augmented bone near the #15 implant was not removed. However, mucosal thickening was resolved, and the patient's symptoms disappeared. In the biopsy specimen retrieved at the time of implant placement, no inflammatory change was found; only a small fibrosis at the periphery was observed. This proved to be controversial. In the study by Scarano et al,13  the authors reported the possibility of dissemination of inflammation into the whole graft and thereby the necessity for total removal of the grafted material. On the other hand, Urban et al21  presented a case of successful partial removal of the graft material (retaining the seemingly unaffected graft material). A recent case report found inconsistencies between the clinical/radiographic outcomes and histologic findings after FESS without the removal of the graft.10  Despite favorable clinical and radiologic results, core biopsies revealed fibrotic change in the remaining graft. Considering the above, the present case requires continuous monitoring.

Adverse events related to maxillary sinus augmentation are being increasingly reported in recent times. These events include the displacement of the dental implant into the maxillary sinus and postaugmentation acute/chronic sinusitis.810,21,22  However, peri-implantitis–triggered maxillary sinusitis has rarely been reported,12,13  even though the severity can be detrimental. The clinician should be aware of the possibility of infection spread to the augmented bone from the peri-implantitis lesion and the course of treatment including FESS.

Peri-implant inflammation that spreads toward the bone-augmented maxillary sinus cavity can cause severe infection. This situation may not be fully resolved using an intraoral approach and medication. A nasal endoscopic approach should be considered in treatment planning.

Abbreviations

Abbreviations
CBCT:

cone-beam computerized tomography

FESS:

functional endoscopic sinus surgery

The authors would like to thank Jung Sun Jang, medical device evaluation team manager at Genoss (Suwon, Korea), for his work in histopathology.

The authors have no potential conflict of interest relevant to this article.

1. 
Beretta
M,
Poli
PP,
Grossi
GB,
Pieroni
S,
Maiorana
C.
Long-term survival rate of implants placed in conjunction with 246 sinus floor elevation procedures: results of a 15-year retrospective study
.
J Dent
.
2015
;
43
:
78
86
.
2. 
Wallace
SS,
Froum
SJ.
Effect of maxillary sinus augmentation on the survival of endosseous dental implants: a systematic review
.
Ann Periodontol
.
2003
;
8
:
328
343
.
3. 
Pjetursson
BE,
Tan
WC,
Zwahlen
M,
Lang
NP.
A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation
.
J Clin Periodontol
.
2008
;
35
:
216
240
.
4. 
Tan
WC,
Lang
NP,
Zwahlen
M,
Pjetursson
BE.
A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. Part II: transalveolar technique
.
J Clin Periodontol
.
2008
;
35
:
241
254
.
5. 
Corbella
S,
Taschieri
S,
Weinstein
R,
Del Fabbro
M.
Histomorphometric outcomes after lateral sinus floor elevation procedure: a systematic review of the literature and meta-analysis
.
Clin Oral Implants Res
.
2016
;
27
:
1106
1122
.
6. 
Polak
D,
Shapira
L.
From maximally to minimally invasive surgery for sinus floor augmentation
.
Compend Contin Educ Dent.
2013
;
34(Spec No):19–24.
7. 
Raghoebar
GM,
Onclin
P,
Boven
GC,
Vissink
A,
Meijer
HJA.
Long-term effectiveness of maxillary sinus floor augmentation: a systematic review and meta-analysis
.
J Clin Periodontol
.
2019
;
(6 suppl 21)
:
307
318
.
8. 
Chiapasco
M,
Felisati
G,
Zaniboni
M,
Pipolo
C,
Borloni
R,
Lozza
P.
The treatment of sinusitis following maxillary sinus grafting with the association of functional endoscopic sinus surgery (FESS) and an intra-oral approach
.
Clin Oral Implants Res
.
2013
;
24
:
623
629
.
9. 
de Jong
MA,
Rushinek
H,
Eliashar
R.
Removal of dental implants displaced into the maxillary sinus: a case series
.
Eur J Oral Implantol
.
2016
;
9
:
427
433
.
10. 
Lim
HC,
Kim
JH,
Choi
SH,
Yu
JA,
Lee
DW.
Conflicts between histologic and clinical/radiologic findings in functional endoscopic sinus surgery for managing maxillary sinusitis following sinus augmentation: a case report
.
Int J Oral Maxillofac Implants
.
2019
;
34
:
1247
1253
.
11. 
Lim
HC,
Nam
JY,
Cha
JK,
et al.
Retrospective analysis of sinus membrane thickening: profile, causal factors, and its influence on complications
.
Implant Dent
.
2017
;
26
:
868
874
.
12. 
Park
WB,
Han
JY,
Oh
SL.
Maxillary sinusitis associated with peri-implantitis at sinus floor augmented sites: case series
.
Implant Dent
.
2019
;
28
:
484
489
.
13. 
Scarano
A,
Cholakis
AK,
Piattelli
A.
Histologic evaluation of sinus grafting materials after peri-implantitis-induced failure: a case series
.
Int J Oral Maxillofac Implants
.
2017
;
32
:
e69
e75
.
14. 
Lee
CT,
Huang
YW,
Zhu
L,
Weltman
R.
Prevalences of peri-implantitis and peri-implant mucositis: systematic review and meta-analysis
.
J Dent
.
2017
;
62
:
1
12
.
15. 
Busenlechner
D,
Furhauser
R,
Haas
R,
Watzek
G,
Mailath
G,
Pommer
B.
Long-term implant success at the Academy for Oral Implantology: 8-year follow-up and risk factor analysis
.
J Periodontal Implant Sci
.
2014
;
44
:
102
108
.
16. 
Poli
PP,
Beretta
M,
Grossi
GB,
Maiorana
C.
Risk indicators related to peri-implant disease: an observational retrospective cohort study
.
J Periodontal Implant Sci
.
2016
;
46
:
266
276
.
17. 
Schwarz
F,
Becker
K,
Sahm
N,
Horstkemper
T,
Rousi
K,
Becker
J.
The prevalence of peri-implant diseases for two-piece implants with an internal tube-in-tube connection: a cross-sectional analysis of 512 implants
.
Clin Oral Implants Res
.
2017
;
28
:
24
28
.
18. 
Geurts
J,
Chris Arts JJ, Walenkamp GH. Bone graft substitutes in active or suspected infection
.
Contra-indicated or not? Injury
.
2011
;
42
(suppl 2)
:
S82
S86
.
19. 
Abu-Ghanem
S,
Kleinman
S,
Horowitz
G,
Balaban
S,
Reiser
V,
Koren
I.
Combined maxillary sinus floor elevation and endonasal endoscopic sinus surgery for coexisting inflammatory sinonasal pathologies: a one-stage double-team procedure
.
Clin Oral Implants Res
.
2015
;
26
:
1476
1481
.
20. 
Nam
KY,
Kim
JB.
Treatment of dental implant-related maxillary sinusitis with functional endoscopic sinus surgery in combination with an intra-oral approach
.
J Korean Assoc Oral Maxillofac Surg
.
2014
;
40
:
87
90
.
21. 
Urban
IA,
Nagursky
H,
Church
C,
Lozada
JL.
Incidence, diagnosis, and treatment of sinus graft infection after sinus floor elevation: a clinical study
.
Int J Oral Maxillofac Implants
.
2012
;
27
:
449
457
.
22. 
Jiam
NT,
Goldberg
AN,
Murr
AH,
Pletcher
SD.
Surgical treatment of chronic rhinosinusitis after sinus lift
.
Am J Rhinol Allergy
.
2017
;
31
:
271
275
.