Beklen111.

qxd

3/14/08

4:03 PM

Page 401

Q U I N T E S S E N C E I N T E R N AT I O N A L

Chronic sinusitis associated with the use

of unrecognized bone substitute: A case report
Arzu Beklen, DDS, MSc1/Antti Pihakari, DDS, MD2/
Riina Rautemaa, DDS, PhD3/Jarkko Hietanen, DDS, MD, PhD4/
Ahmed Ali, DDS5/Yrj T. Konttinen, MD, PhD6
Bone grafts are used for bone augmentation to ensure optimal implant placement.
However, this procedure may sometimes cause sinusitis. The case of a 44-year-old woman
with the diagnosis of recurrent and chronic sinusitis of her right maxillary sinus with a history of dental implant surgery is presented. After several attempts with normal standard
sinusitis therapy, unrecognized bone substitute was removed from the sinus cavity, which
finally led to resolution of the sinusitis. This case reiterates the importance of a careful
examination, consultation, and second opinion for the selection of optimal treatment.
(Quintessence Int 2008;39:401405)

Key words: dental implants, foreign body, sinusitis

Maxillary sinusitis can be the result of an

inflamed tooth. It has been reported that
approximately 10% to 12% of maxillary sinus
infections originate from odontogenic infections.1 Sinusitis of odontogenic origin is not
rare and has been documented in the literature.2,3 However, during surgery, the unex-

PhD student, Institute of Clinical Medicine, Department of

pected finding of some type of bone substitute in the sinus is not usual.
A clinical case of a 44-year-old woman
who recently emigrated from a neighboring
country and had had dental implant surgery
2 years prior is presented. This case reiterates the importance of a careful examination,
consultation, and second opinion for the
selection of optimal treatment.

Medicine/Invrtes medicin, Helsinki University Hospital,

Helsinki, Finland; Institute of Biomedicine, Department of
Anatomy, University of Helsinki, Helsinki, Finland; Medico-social
Centre, Dental Clinic, Bogazici University, Istanbul, Turkey.
2

Oral surgeon, Helsinki City Teaching Clinic, Helsinki, Finland.

CASE REPORT

Oral microbiologist, Helsinki University Central Hospital,

Department

of

Oral

and

Maxillofacial

Diseases

and

Microbiology, Unit of Helsinki University Central Hospital

Laboratory Diagnostics; University of Helsinki, Haartman
Institute, Department of Bacteriology and Immunology,
Helsinki, Finland.
4

Professor and oral pathologist, Institute of Dentistry, University

of Helsinki; HUSLAB (Helsinki University Central Hospital
Laboratory), Helsinki University Central Hospital, Helsinki,
Finland.

PhD student, Department of Anatomy/Biomedicum, University

of Helsinki, Helsinki, Finland; Department of Pediatric Dentistry,
Faculty of Dentistry, University of Garyounis, Benghazi, Libya.

Professor of Medicine, Department of Medicine/Invrtes medicin, Helsinki University Hospital; ORTON (Orthopaedic Hospital
of the Invalid Foundation), Helsinki, Finland; COXA (Hospital for
Joint Replacement), Tampere, Finland.

Correspondence: Prof Yrj T. Konttinen, Department of

Medicine/Invrtes medicin, PO Box 700, FIN-00029 HUS, Finland.
Fax: 358 9 191 25218. E-mail: yrjo.konttinen@helsinki.fi

A 44-year-old woman who had had dental

implant surgery and prosthetic treatment 2
years prior presented to an ear, nose, and
throat specialist with the complaint of rhinitis,
facial pain, and fever. A radiograph disclosed
sinusitis, which was treated by sinus lavage
once a week for 2 months. Lavage fluid was
cultured and disclosed group F hemolytic
streptococci and lack of anaerobic bacteria,
suggestive of a classic upper respiratory
tractderived sinusitis. Lavage was first combined with amoxicillin 500 mg 3 times a day,
which after 1 week was changed to cefuroxim 250 mg 2 times a day so that the patient
received antibiotics for 2 months. However,
the conventional sinus lavage did not bring

COPYRIGHT 2008 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO
PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER
VOLUME 39

NUMBER 5

MAY 2008

401

Beklen111.qxd

3/14/08

4:03 PM

Page 402

Q U I N T E S S E N C E I N T E R N AT I O N A L
Beklen et al

permanent relief. After the failure of this firstline therapy, suspicion of an odontogenic
infection was raised, and the patient was
referred to a clinician for investigation. It was
thought that perhaps the dental implant treatment was perpetuating the sinusitis,
although the patient was not complaining
about her implant-supported prosthesis.
At the dental clinic, widespread periimplantitis in the maxilla was diagnosed. In
the maxillary left first molar region, the
patient had a blade-type implant together
with a rootless second molar. In the maxillary
right first and second premolar regions, she
had 2 9-mm osseointegrated dental implants. The implants were supporting a partial denture from the right second molar to
the left second molar. Bone could not be felt
in the maxillary right first premolar region,
and purulent exudate was found in the
peri-implant pocket. Based on orthopantomographic and intraoral radiograph examinations, the infection seemed to have spread to
the maxillary right second premolar, as well.
Removal of all fixed prosthetic work, together
with extensive alveolar bone transplantation,
was recommended as the first step of treatment with the goal of reimplantation-based
fixed dental prosthesis. The patient did not
want to lose her prosthesis and sought a second opinion from the Institute of Dentistry.
During the clinical examinations, the
patient complained of pain in the cheek over
the right maxillary jaw and nasal discharge
from the right nostril. Tenderness and edema
were present over the canine fossa. Externally, there was slight redness over the
cheek. Intraoral clinical examination showed
widespread peri-implantitis in the maxilla.
Although the patient had been trying to maintain good oral hygiene, the gingiva bled upon
probing. A panoramic radiograph (Fig 1a) and
intraoral periapical radiographs (Fig 1b)
revealed infection around the dental implants.
Alveolar bone loss was seen around the
implants as a radiographic sign of peri-implantitis. Occipitomental Water projection (Fig 1c)
revealed cloudiness of the right maxillary
sinus. On the maxillary right side, the partial
denture was cut between the canine and first
premolar and between the first and second
molars. After opening of the gingival margin

from the maxillary right canine to second premolar, a 1-cm-diameter oroantral fistula was
found in the second premolar region. The
sinus contained necrotic and granular tissue
and purulent exudate. Additionally, while
cleaning the sinus, some bone substitute was
found unexpectedly and removed (Fig 2).
Histopathology revealed that the cells
seemed to be edematic in the granulation
tissue. The granulation tissue was infiltrated
by mixed inflammatory cells consisting of
neutrophilic leukocytes, lymphocytes, and
plasma cells. Substitute material, which
resembled bone, was seen as elongated
pieces. Some bone had grown on the surface of the substitute material (Fig 2).
Microbiologic examination of the periimplant pus revealed anaerobic periodontal
pathogens that are specifically associated with
the teeth, such as Fusobacterium nucleatum
(5%), Prevotella melaninogenus (2%), Peptostreptococcus (0.8%), and Porphyromonas
gingivalis (0.5%) together with Streptococcus
viridans (90%) as a component of the aerobic
normal oral flora. These findings were suggestive of peri-implantitis and maxillary sinusitis of
periodontal origin.4
The patient was resistant to standard
sinusitis therapy. An antrostomy was performed 1 year later, and the normal sinus
opening was enlarged. Normally, the maxillary
sinus is lined by ciliated pseudostratified
epithelium containing some goblet cells. In
the present case, this normal epithelium had,
as a result of inflammation, been totally
replaced by nonciliated squamous mucosal
epithelium,5 which was removed, except for
from the roof of the sinus cavity. After hydrogen peroxide washes, a Kennedy tampon
was placed under the lowest nasal concha
before closure.
After 4 months, another episode of sinusitis was treated with a sinus fenestration operation for the improvement of ventilation and
drainage of the maxillary sinus. Additional
bone substitute particles were revealed and
carefully removed. The lavage culture disclosed repeatedly the same anaerobes of the
peri-implant purulent exudate until all foreign
material from the maxillary sinus was finally
removed. Nearly 1.5 years later, the sinus was
asymptomatic.

COPYRIGHT 2008 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO
PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER

402

VOLUME 39

NUMBER 5

MAY 2008

Beklen111.qxd

3/14/08

4:03 PM

Page 403

Q U I N T E S S E N C E I N T E R N AT I O N A L
Beklen et al

Figs 1a to 1c Inflammation both around implants

and in the maxillary sinus. (a) Panoramic view shows
the presence of osseointegrated (left arrow) and
blade type implants in the maxilla. (b) Intraoral periapical radiograph also demonstrates inflammation
around a dental implant (arrow). (c) Radiographs of
the maxillary sinuses were taken using the Water
projection, which demonstrates sinusitis in the right
maxillary sinus.

Fig 2 Bone substitute that was removed from the

sinus. (inset) Surgically removed bone substitute and
an osseointegrated dental implant. Photomicrograph showing bone substitute (s) and a narrow rim
of bone (arrow). Bacteria (b), hemorrhage (h), and
inflammatory cells (i) are seen, as well (bar represents
60 m).

b
s

COPYRIGHT 2008 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO
PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER
VOLUME 39

NUMBER 5

MAY 2008

403

Beklen111.qxd

3/14/08

4:03 PM

Page 404

Q U I N T E S S E N C E I N T E R N AT I O N A L
Beklen et al

DISCUSSION
Placing dental implants in optimal positions
frequently requires bone augmentation because of the lack of bone support.4 This
sinus-lifting operation may damage the antral
mucosa and can lead to the formation of an
oroantral fistula.6,7
Such a fistula was observed in the present
patient and enabled an ascending odontogenic sinus infection. In addition to aerobic
oral viridans streptococci, a mixed bacterial
population also comprising several anaerobic
species was demonstrated by culture.4,8 Microbiologic findings indicated impaired drainage
and poor penetration of antimicrobials into the
mixed bacterial biofilm and artificial bone substitute. At the same time, these culture findings
exclude primary sinusitis, which is usually
caused by pneumococci, hemophilus, or
Moraxella species and emphasizes the importance of the evaluation of the source of the
infection, ie, conventional or odontogenic
sinusitis, for the correct medical and surgical
management of the patient.9,10 In the present
case, the culture findings of the initial sinus
lavages were suggestive of an upper respiratory tractderived sinusitis and thus were somewhat misleading.
The microbiologic findings of the infected
maxillary bone, however, clearly showed the
presence of anaerobic pathogens associated
with chronic periodontitis. It is possible that the
peri-implantitis originated from periodontal
lesions of the adjacent or preexisting natural
teeth and spread to the bone substitute material, which lacked immune defenses. This
weakened response of nonvital grafted bone
contrasts with that of the well-vascularized vital
native bone, which is able to recruit immuneinflammatory cells for host defense. The
mucosal lining of the heavily infected sinus
wall was prone to infection by the upper respiratory tract microbes because of chronic local
inflammation and damage to the ciliated epithelium. Only when the continuity of the sinus
mucosa was broken did the microorganisms
from the infected fistular wall enter the sinus.
The latter microbiologic findings indicate
impaired drainage associated with the development of hypoxia leading to chronicity, as
well as poor penetration of antimicrobials into

the mixed bacterial biofilm and artificial bone

substitute in the absence of true antibiotic
resistance in the bacterial cultures.
The infection had probably started at the
time of the primary dental restorative surgery
and progressed, as odontogenic and
implant-related infections often do, in a subclinical manner leading gradually to osteolytic bone destruction. The diagnosis was not
made in the acute setting, but years later,
secondary symptoms occurred due to
obstruction of drainage and chronic irritation
of mucosa.1113 An oroantral fistula was finally
formed and led to a continuous seeding of
oral bacteria into the normally sterile maxillary sinus. This, together with the intra-antral
foreign body, led to a chronic smoldering
infection and conversion of the ciliated
epithelium into squamous epithelium and
fibrotic scar. Finally, the progressive infection
and diminishing local defense resulted in a
clinically manifested sinusitis.

ACKNOWLEDGMENT
Authors are grateful to Liisa Virkki for the translation of
patient records.

REFERENCES
1. Maloney PL, Doku HC. Maxillary sinusitis of odontogenic origin. J Can Dent Assoc 1968;34:591603.
2. Finegold SM. Anaerobic Bacteria in Human Disease.
New York: Academic Press, 1977.
3. Brook I, Friedman EM. Intracranial complications of
sinusitis in children: A sequella of periapical
abscess. Ann Otol Rhinol Laryngol 1982;91:4143.
4. Brook I. Sinusitis of odontogenic origin. Otolaryngol
Head Neck Surg 2006;135:349355.
5. Bassiouny A, Atef AM, Raouf MA, Nasr SM, Nasr M,
Ayad EE. Ultrastructural ciliary changes of maxillary
sinus mucosa following functional endoscopic
sinus surgery: An image analysis quantitative study.
J Laryngol Otol 2003;117:273279.
6. Misch CE. Maxillary sinus augmentation for
endosteal implants: Organized alternative treatment plans. Int J Oral Implantol 1987;4:4958.
7. McEvoy PE. Selecting treatment options and
sequencing treatment in the replacement of 2 maxillary central incisors with implants: A case report. J
Oral Implantol 2003;29:278283.

COPYRIGHT 2008 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO
PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER

404

VOLUME 39

NUMBER 5

MAY 2008

Beklen111.qxd

3/14/08

4:03 PM

Page 405

Q U I N T E S S E N C E I N T E R N AT I O N A L
Beklen et al

8. Legert KG, Zimmerman M, Stierna P. Sinusitis of

12. Scorticati MC, Raina G, Federico M. Cluster-like

odontogenic origin: Pathophysiological implica-

headache associated to a foreign body in the max-

tions of early treatment. Acta Otolaryngol 2004;124:

655663.

illary sinus. Neurology 2002;59:643644.

13. Macan D, Cabov T, Kobler P, Bumber Z. Inflammatory

9. Boyne PJ, James RA. Grafting of the maxillary sinus

reaction to foreign body (amalgam) in the maxillary

floor with autogenous marrow and bone. J Oral

sinus misdiagnosed as an ethmoid tumor. Dento-

Surg 1980;38:613616.

maxillofac Radiol 2006;35:303306.

10. Kaufman E. Maxillary sinus elevation surgery: An

overview. J Esthet Restor Dent 2003;15:272282.
11. Tingsgaard PK, Larsen PL. Chronic unilateral maxillary sinusitis caused by foreign bodies in the maxillary sinus [in Danish]. Ugeskr Laeger 1997;159:
44024404.

COPYRIGHT 2008 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO
PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER
VOLUME 39

NUMBER 5

MAY 2008

405