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100 Int J Oral-Med Sci 17(3)(4):100-107, 2018

Original Article

Differential Diagnosis between Fungal Maxillary Sinusitis and Odontogenic Sinusitis


Using CT Images

Kotaro Ito,1 Yoshinobu Hara,1 Norihito Iizuka,2 Eri Sawada,2 Masaaki Suemitsu,3 Kayo Kuyama,3 and
Takashi Kaneda1

Departments of 1Radiology and 3Pathology, Nihon University School of Dentistry at Matsudo, Matsudo, Chiba 271-8587, Japan
2
Nihon University Graduate School of Dentistry at Matsudo, Radiology, Matsudo, Chiba 271-8587, Japan

Article History Abstract

Received 30 November 2018 Objectives The purposes of this study were to investigate image findings and clinical
Accepted 18 December 2018 symptoms of fungal maxillary sinusitis and odontogenic sinusitis, and to assessment of
usefulness of differential diagnosis between fungal maxillary sinusitis and odontogenic
sinusitis.
Study Design The study included 32 patients (16 fungal sinusitis, 16 odontogenic
sinusitis) with a confirmed histopathologic diagnosis of fungal sinusitis or odontogenic
sinusitis. Computed tomography(CT)images were used to evaluate such as 1)location and
shape of mucosal thickening, 2)calcification, 3)osteolysis, 4)osteosclerosis and 5)thicken-
ing of bony wall. Moreover, we investigated clinical symptoms of all patients.
Results There were significant differences between fungal sinusitis and odontogenic
Keywords : sinusitis in sex difference, shape of mucosal thickening, calcification, osteosclerosis,
fungal maxillary sinusitis, thickening of bony wall and clinical symptoms.
odontogenic sinusitis, Conclusions This study suggested that these findings are useful for differential diagnosis
maxillary sinusitis between fungal maxillary sinusitis and odontogenic sinusitis.

Introduction odontogenic sinusitis also occur unilaterally in the maxillary


Occurrence of fungal infection in the paranasal sinusitis is sinus(6, 7). Furthermore, a history of previous endodontic
relatively rare(1). There are four clinicopathologic classifi- treatment is also common among patients with fungal balls.
cations of mycotic sinonasal disease acute invasive fulminant Root-filling materials based on zinc oxide-eugenol is
disease, chronic invasive infection, noninvasive mycotic considered to be a growth factor for fungal sinusitis(2, 8, 9).
colonization (mycetoma) and allergic mycotic sinusitis. That further makes it difficult to differentiate between
These four types of infection can be seen with any fungus fungal sinusitis and odontogenic sinusitis.
but are most commonly a result of Aspergillus infection. The purposes of this study were to investigate image
Aspergillus species are opportunistic fungi and widely findings and clinical symptoms of fungal maxillary sinusitis
distributed in the environment(1-4). and odontogenic sinusitis, and to assessment of usefulness of
Odontogenic sinusitis primarily results from multiplica- differential diagnosis between fungal maxillary sinusitis and
tion of bacteria invading from the mouth or the focus of a odontogenic sinusitis.
dental infection. It is very important to differential diagnosis
between fungal sinusitis and odontogenic sinusitis because Materials and methods
there have different treatment methods(1-3, 5). However, it Human rights statements and informed consent
is often difficult to differentiate because fungal sinusitis and All procedures followed were in accordance with the

Correspondence to :
ethical standards of the responsible committee on human
Kotaro Ito experimentation (institutional and national) and with the
E-mail : itou.koutarou@nihon-u.ac.jp Helsinki Declaration of 1964 and later versions. This study
Int J Oral-Med Sci 17(3)(4):100-107, 2018 101

Fig. 1. Fungus ball was composed of many fungi, shown as


tangled mycelium formed by hyphae which show Fig. 2. Odontogenic sinusitis shows respiratory epithelium
characteristic dichotomous branching at about 45 ulcerated on large areas and subjacently fibrocollagenic
degrees, and small calcified particules(×40, HE). tissue(×20, HE).

was approved by the Ethics Committee of the University mA; field of view, 240 × 240 mm; helical pitch, 41. The
School of Dentistry(No. EC12-009), and all patients signed imaging included axial (0.50 mm) and multiplanar (3.00
an informed consent agreement for the Computed tomogra- mm)images. The MDCT images were interpreted using a
phy(CT)examination. medical liquid crystal display monitor(RadiForce G31; Eizo
Nanao, Ishikawa, Japan).
Patients All images were independently evaluated by over 5 years
From April 1, 2006 to December 31, 2016, 83 patients with experienced two oral radiologists. The kappa statistic was
detection of fungal hyphae at histopathological examination used to assess the agreement between fungal sinusitis and
of tissues excised at surgery were included in the study(Fig. odontogenic sinusitis for the imaging findings (shape of
1). 16 patients were identified as fungal sinus disease at CT mucosal thickening, calcification, osteolysis, osteosclerosis
in the Department of Radiology, Nihon University School of and thickening of bony wall). Kappa values were classified
Dentistry at Matsudo. The group included 14 females and 2 as poor (0.0-0.19), fair (0.2-0.39), moderate (0.4-0.59),
males. Their age ranged from 32 to 76 years (mean, 62.4 good(0.6-0.79)and excellent(0.8-1.00).
years). Similarly, 16 patients with histopathological confir-
mation of odontogenic sinusitis who underwent CT imaging Assessment
from April 1, 2006 to December 31, 2016, were included in CT images were used to evaluate fungal sinusitis and
this study (Fig. 2). Maxillary sinusitis near the apical odontogenic sinusitis such as 1) location and shape of
periodontitis or advanced periodontal bone loss on the CT mucosal thickening, 2) calcification, 3) osteolysis, 4) osteo-
image was diagnosed with odontogenic sinusitis (Fig. 3). sclerosis and 5)thickening of bony wall(10-13). Analysis of
The group included 9 males and 7 females. Their age ranged shape of mucosal thickening was performed on the CT
from 29 to 85 years (mean, 56.8 years). Patients with images. The shape characteristics of fungal sinusitis and
squamous cell carcinoma and metal artifacts precluding odontogenic sinusitis were evaluated using coronal slices.
visualization of the maxillary sinus were excluded from this The shape of mucosal thickening of fungal sinusitis and
study. odontogenic sinusitis were differentiated into two groups
(Fig. 4): (a) conform to maxillary sinus shape and (b)
Image protocol mucosal thickening of maxillary sinus walls(1). Analysis of
CT imaging was performed with a 64-Multi-detector row calcification was evaluated using coronal slice. The calcifica-
CT(MDCT)system(Aquilion 64; Toshiba Medical Systems, tion was into four groups (Fig. 5): (a) fine punctate; (b)
Tokyo, Japan). All patients were scanned using the routine linear; (c) nodular; and (d) eggshell. When the calcification
clinical protocol for craniomaxillofacial examination at our was similar to dotted or sandy, it was classified as fine
hospital as follows: tube voltage, 120 kV; tube current, 100 punctate. When the calcification was similar to a straight or
102 Int J Oral-Med Sci 17(3)(4):100-107, 2018

Fig. 3. Maxillary sinusitis with the following CT findings were diagnosed as odontogenic sinusitis: (A)maxillary sinusitis
near the apical periodontitis(arrows); and(B)maxillary sinusitis near the advanced periodontal bone loss(arrows).

Fig. 4. The shape of fungal sinusitis and odontogenic sinusitis were differentiated into two groups: (A)conform to maxillary
sinus shape(arrows); and(B)mucosal thickening(arrows).

Fig. 5. The presence of calcification was into four groups: (a)fine punctate(arrowheads); When the calcification was similar to dotted
or sandy, it was classified as fine punctate.(b)linear(arrowheads); When the calcification was similar to a straight or curved
line, it was classified linear.(c)nodular(arrowheads); When the shape of calcification was similar to a polygon or rectangular, it
was classified as nodular.(d)eggshell(arrowheads); When the shape was globular, round, or rimlike, it was classified as eggshell.
Int J Oral-Med Sci 17(3)(4):100-107, 2018 103

Fig. 6. Analysis of the osteolysis, osteosclerosis and bony walls thickened were evaluated using axial slice.(A)Osteolysis(arrowheads)
is seen in the lateral wall of the nasal cavity.(B)Osteosclerosis(arrowheads)is seen in the anterior wall of left maxillary sinus.
(C)Thickening of bony wall(arrowheads)is seen in the front wall and posterior wall of right maxillary sinus.

curved line, it was classified linear. When the shape of Results


calcification was similar to a polygon or rectangular, it was Fungal sinusitis was diagnosed in the surgical specimens
classified as nodular. When the shape was globular, round, or of 16 of 83 patients. Location of all sinusitis was the maxillary
rimlike, it was classified as eggshell (14). Analysis of the sinus. Fungus species of all fungal sinusitis was aspergillus in
osteolysis, osteosclerosis and thickening of bony wall were this study. Evaluation of calcification of fungal sinusitis in the
evaluated using axial slice(Fig. 6). Osteolysis was defined as following findings: 9 calcifications were fine punctate
absorption of maxillary sinus wall. Osteosclerosis was (56.3%), 2 calcifications were linear (12.5%), 3 calcifica-
defined as having high density region in the anterior wall or tions were nodular (18.8%) and 2 calcifications were egg-
the posterior wall of maxillary sinus compared with the shell(12.5%). All calcifications of odontogenic sinusitis were
opposite side. Thickening of bony wall was defined as the fine punctate(3/3). Histopathologically, findings of infection
increase of maxillary sinus wall compared with the opposite with aerobic bacteria, anaerobic bacteria or both were found
side(10). in all odontogenic sinusitis.
Symptoms were evaluated from retrospective review of Demographic characteristics on patients with fungal
the medical charts. Symptoms of fungal sinusitis and sinusitis and odontogenic sinusitis are shown(Table 1). Sex
odontogenic sinusitis were evaluated such as 1)rhinorrhea, difference were significantly different between fungal
2)pain, 3)nasal obstruction 4)neurological symptoms(10). sinusitis and odontogenic sinusitis(P=0.02). Ages were not
significantly different between fungal sinusitis and odonto-
Statistical analysis genic sinusitis(P=0.27).
The statistical significance of differences in data was Image data on patients with fungal sinusitis and
determined by a two-sided Mann-Whitney U test. odontogenic sinusitis are shown(Table 2). Evaluation of the
Differences with values of P < 0.05 were considered different shape of mucosal thickening of sinusitis resulted in
significant. SPSS software for Windows (version 21; IBM the following findings: 15 fungal sinusitis (93.8%) and 8
Japan Inc., Tokyo, Japan)was used for the analysis. odontogenic sinusitis (50.0%) had a conform to maxillary
sinus shape, 1 fungal sinusitis (6.3%) and 8 odontogenic
sinusitis(50.0%)had a mucosal thickening of maxillary sinus
104 Int J Oral-Med Sci 17(3)(4):100-107, 2018

Table 1. Comparison of demographic characteristics on patients with fungal sinusitis and


odontogenic sinusitis: Two-sided Mann-Whitney U test

Table 2. Comparison of image data on patients with fungal sinusitis and odontogenic
sinusitis: Two-sided Mann-Whitney U test

walls(P<0.01). Preoperative imaging data of patients with odontogenic sinusitis are shown (Table 3). Clinical symp-
fungal sinusitis and odontogenic sinusitis resulted in the toms were observed in all fungal sinusitis (100.0%) and 9
following findings: 15 fungal sinusitis(93.8%)and 3 odonto- odontogenic sinusitis(56.3%),(P<0.01). Analysis of clinical
genic sinusitis (18.8%) were detected of calcification (P < symptoms of all fungal sinusitis patients and odontogenic
0.01), 3 fungal sinusitis(18.8%)and 1 odontogenic sinusitis sinusitis showed that 9 fungal sinusitis (56.3%) and 6
(6.3%)were detected of sinus wall osteolysis(P=0.29), 9 odontogenic sinusitis(66.7%)were observed rhinorrhea(P=
fungal sinusitis(31.3%)and 3 odontogenic sinusitis(18.8%) 0.36), 8 fungal sinusitis(50.0%)and 3 odontogenic sinusitis
were detected of osteosclerosis (P = 0.03) and 10 fungal (33.4%) were observed pain (P = 0.11), 6 fungal sinusitis
sinusitis (62.5%) and 2 odontogenic sinusitis (12.5%) were (37.5%)and 0 odontogenic sinusitis(0.0%)were observed
detected of thickening of bony wall(P<0.01). nasal obstruction(P=0.02)and 4 fungal sinusitis(25.0%)and
Clinical symptoms on patients with fungal sinusitis and 0 odontogenic sinusitis (0.0%) were observed neurological
Int J Oral-Med Sci 17(3)(4):100-107, 2018 105

Table 3. Comparison of clinical symptoms on patients with fungal sinusitis and


odontogenic sinusitis: Two-sided Mann-Whitney U test

symptoms(P=0.07). infection in patients with reduced immunity due to the use of


The agreement between fungal sinusitis and odontogenic adrenocortical steroids, immunosuppressants, antineoplastic
sinusitis was good (k = 0.79) for shape of sinusitis. The agents. It is also easy to become severe when blood is
agreement between fungal sinusitis and odontogenic inclined to ketoacidosis due to diabetes or kidney dialysis(1,
sinusitis was excellent(k=0.94)for calcification. The agree- 2). In this study, patients with these general conditions were
ment between fungal sinusitis and odontogenic sinusitis was not included. These frequencies location and fungus species
good(k=0.79)for osteolysis. The agreement between fungal of the fungal sinusitis are similar to our results. Also, the
sinusitis and odontogenic sinusitis was good (k = 0.78) for shape of mucosal thickening had a significant difference
osteosclerosis. The agreement between fungal sinusitis and between fungal sinusitis and odontogenic sinusitis. It is
odontogenic sinusitis was excellent(k=0.93)for thickening considered better to suspect fungal sinusitis in the case of
of bony wall. conform to maxillary sinus shape.
Thery et al. reported that analysis of clinical sign of
Discussion aspergillosis was 14 pain(93.3%), 3 nasal obstruction(20%),
In our study, all fungal sinusitis occurred in the maxillary 3 rhinorrhea (20%), 2 oculomotor disorders (13.3%) and 5
sinus. Moreover, Fungus species of all fungal sinusitis was neurological symptoms (33.3%) (11). From our result,
aspergillus in this study. According to Michel et al., the most Analysis of clinical symptoms of all fungus sinusitis showed
frequent sinus in fungal sinusitis was the maxillary sinus, that 9 rhinorrhea(56.3%), 8 pain(50.0%), 6 nasal obstruc-
then the sphenoid sinus, the frontal sinus, the ethmoid sinus tion (37.5%) and 4 neurological symptoms (25.0%). There
(1). Aspergillus, Schizophyllum commune and Alternaria was a difference in results between past reports and our
are known as fungal species of fungal sinusitis (15, 16). research. It was considered that this is probably because our
Additionally, they reported that fungus sinusitis can be seen research is only chronic noninvasive fungal disease, and the
with any fungus but are most commonly a result of past report was Aspergillosis including acute infiltrative
aspergillus infection (1-3, 15, 16). Acute and chronic mycosis. In addition, since our study was only performed on
invasive fungal sinusitis often develops as an opportunistic surgery, it seems that all patients had clinical symptoms.
106 Int J Oral-Med Sci 17(3)(4):100-107, 2018

Michelle AM. reported that clinical symptoms of odontogen- Osteolysis is a characteristic finding of invasive fungal
ic sinusitis was pain, cacosmia and mucopurulent discharge sinusitis and is atypical in noninvasive mycotic colonization
(1). Similarly, Simuntis R et al. reported that of clinical and odontogenic sinusitis(1). Therefore, it was considered
symptoms of odontogenic sinusitis were pain, foul smell and that there was no significant difference in Osteolysis in this
dental pain. Further, they said these symptoms did not study. However, in the case of invasive fungal sinusitis, it is
distinguish odontogenic sinusitis from other causes of suspected that there is a significant difference with dental
sinusitis(17). However, from our study showed that nasal sinusitis.
obstruction and neurological symptoms were found only In our study, there were significant differences in sex,
fungal sinusitis. Therefore, they were considered that the shape of mucosal thickening, osteosclerosis, thickening of
presence or absence of nasal obstruction and neurological bony wall and symptoms in addition to calcification between
symptoms are useful for differentiating between fungal fungal sinusitis and odontogenic sinusitis. These findings are
sinusitis and odontogenic sinusitis. thought to be useful for differential diagnosis between
From our result, there was a significant difference in sex fungal maxillary sinusitis without calcification and odonto-
difference between fungal sinusitis and odontogenic sinusi- genic sinusitis.
tis. Fungal sinusitis occurred in female predominance. There
was no sex difference in odontogenic sinusitis. Michelle et al. Conclusions
reported that there was sex difference in fungal sinusitis, The present study showed that the characteristics of
and it occurred in female predominance(1). This report is fungal sinusitis and odontogenic sinusitis. In addition to
same as our result. However, there are reports that there calcification, there were significant differences in many
was no sex difference in fungal sinusitis, and it is considered findings between fungal maxillary sinusitis and odontogenic
that there is a difference in sex difference among races(17, sinusitis.
18). This study suggested that these findings are useful for
Yoon et al. reported that the intrasinus calcification was differential diagnosis between fungal maxillary sinusitis and
found in 20(51%)of 39 patients with fungal sinusitis and in 16 odontogenic sinusitis.
(3%) of 471 patients with nonfungal sinusitis. From our
results, the intrasinus calcification was found in 15(93.8%)of References
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