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KISEP Original Articles J Rhinol 5((((2)))), 1998
A Study on the Diagnosis of Fungus Ball
Hun-Jong Dhong, M.D., Seong-Won Yoon, M.D. and Jae-Yun Jung, M.D.
ABSTRACT
Background：Fungus ball should always be considered in the differential diagnosis of chronic or recurrent sinusitis resistant to adequate medicinal treatment. Materials and Methods：From January 1, 1995, to September 31, 1997, 32 patients were dia- gnosed with fungus ball based on the pathologic confirmation. We reviewed the 32 patients from the diagnostic point of view, evaluating clinical symptoms, signs, computerized tomography (CT) findings, and operative findings. We also reviewed five cases of clinical misdiagnosis, in which pathologic confirmation failed to identify fungus despite operative and radiologic fin- dings suggesting its presence. Results：Among 32 patients, 19 cases (59%) were suspected prior to surgery as having fungus ball. Eleven cases (34%) were suspected only upon historical and physical examination. Conclusion：A high index of suspicion is necessary for the diagnosis of fungus ball. A pathologic confirmation is necessary for a definite diagnosis.
KEY WORDS：Fungus ball·Diagnosis·Nose·Paranasal sinus.
INTRODUCTION
Fungal sinusitis is becoming increasingly common due to changes in the distribution of normal bacteria and to a growing number of diverse immunocompromising factors caused by the overuse of antibiotics. Fungal sinusitis does not react even to long-term antibiotic treatment and, especially in the case of immunocompromised patients, may cause complications, or possibly death, by affecting neighboring organs like the eye or brain. Therefore, it is extremely important to make an accurate diagnosis with regard to this condition. In the case of fungus ball, the most frequently clinically observed form of fungal si- nusitis, an accurate diagnosis is still more important since it can be cured completely only with proper operative removal.
While recent developments in CT and MRI technologies have made diagnosing fungus ball easier, the clinical symp- toms of fungus ball remain hard to detect. It is, however, ess- ential that fungus ball be detected in a differential diagnosis of unilateral sinusitis or recurrent sinusitis that is not reacting to proper medical treatments and it is also necessary that sinus fungus ball should be confirmed using pathological study.
In this study, the authors looked for the clues of sinus fu- ngus ball and investigated the possibilities of clinical misdi- agnosis through pathological and radiological tests. Analysis was conducted on the diagnostic processes of 32 cases that were histologically confirmed as sinus fungus ball and of five cases in which sinus fungus ball was diagnosed clinically but not observed histologically.
MATERIALS AND METHODS
The authors investigated 32 cases diagnosed from January 1995 to September 1997 at the Department of Otorhinolaryn- gology-Head and Neck Surgery, Sung Kyun Kwan University, College of Medicine, Samsung Medical Center. Of the 32 ca- ses, 30 were confirmed histologically；in two cases, fungus was not observed but cultures for fungus ball yielded positive results from grossly definite fungus ball. The authors also in- vestigated five cases, in which sinus fungus ball was clinically suspected due to the nature of the material taken during surgery or to radiological findings, but fungal hypae was not observed histologically. For this study, the authors examined clinical signs and symptoms, pathological findings, pre-operative ra- diological findings, and findings observed during surgery. Also studied were the pre-operative findings that led to the suspicion of sinus fungus ball.
RESULTS
The diagnostic processes and clinical characteristics of the 32 cases confirmed as sinus fungus ball are as follows：
Department of ORL-HNS, Sung Kyun Kwan University College of Medicine, Samsung Medical Center, Seoul Korea
Address correspondence and reprint requests to Hun-Jong Dh- ong, M.D., Department of Otorhinolaryngology-Head and Neck Surgery, Sung Kyun Kwan University, College of Medicine, Samsung Medical Center, 50 Ilwon-dong Kangnam-gu, Seoul 135-710, Korea
Tel：82-2-3410-3573, Fax：82-2-3410-3879 Accepted for publication on September 24, 1998
Dhong, et al：Fungus Ball / 109 Age and sex distribution
Of the 32 patients with fungus ball, 19 (59%) were male and 13 (41%) were female. According to this distribution, the number of males was 1.5 times higher than that of females.
The ages of the patients ranged from 27 to 75：seven patients were aged 40 to 49 (22%)；13, from 50 to 59 (41%)；and eight, from 60 to 75 (25%). The average age was 52±8.8.
Signs and symptoms
The most common symptom for which the patients first vi- sited the clinic was nasal obstruction (17 cases, or 53.1%).
Other symptoms included postnasal drip (15 cases, or 46.
9%), headache (13 cases, or 40.6%), purulent rhinorrhea (9 cases, or 28.1%), foul odor (two cases), nasal pain (one case), and proptosis accompanied by facial edema (one case).
Nasal endoscopic findings
In the eight cases where pathological tests revealed a nasal polyp, the nasal polyp was observed on the same lateral side as the sinus fungus ball in all cases except one, where a bila- teral nasal polyp was observed. Out of the 15 cases that showed septal deviations, six cases were ipsilateral septal deviation and nine cases were contralateral deviation.
Predisposing factors and medical history
Among the 32 cases of sinus fungus ball, eight cases in- volved diabetics, one case was diagnosed during a wait for a bone marrow transplantation to treat chronic myelocytic leu- kemia, and four cases demonstrated medical histories of hyp- ertension. The remaining cases did not indicate any notable medical history. Of the 32 patients, four had previously und- ergone a Caldwell-Luc operation and one had undergone en- doscopic sinus surgery in the past.
Radiologic finding
Sinus CT scanning had been conducted on all 32 patients, and in 17 of these patients the radiologic findings suggested sinus fungus ball：in eight cases focal calcification was ob- served inside the soft tissue lesion of the sinus, and in the remaining nine sclerotic change or erosion of neighboring bone tissues, including the uncinate process, was observed in addi- tion to the focal calcification. In 16 of these cases, the findings were observed in the maxillary sinuses；one case involved the sphenoid sinus.
While a sinus PNS view was conducted in some cases, CT scanning was conducted immediately when the fungus ball was suspected during the outpatient examination, based on the ju-
dgment that a PNS view was less effective in diagnosing fu- ngus ball. Therefore, PNS view findings are not mentioned in this study.
Involved sinus and combined sinusitis
All 32 cases were unilateral, and in 25 cases, the maxillary sinus was involved. In three cases, the fungus ball was obs- erved to extend across the maxillary sinus and the anterior ethmoid sinus while, in four cases, it was observed to be loc- alized to the sphenoid sinus. Twelve cases were accompanied by inflammation in the other sinus, and ten out of these 12 were accompanied by bilateral inflammation. In the remaining 20 cases, inflammation was isolated to the sinus where the fungus ball was observed.
Preoperative diagnosis
In nineteen cases (59%), sinus fungus ball was suspected pre-operatively. In 11 (34%) of these 19 cases, surgical trea- tment was performed for fungus ball following the observation of greasy and sticky unilateral purulent pus and symptoms non-reactive to antibiotics at outpatient examination. Nine cases out of these 11 showed CT findings that confirmed fun- gus ball. In eight cases (25%), where nonspecific sinusitis was suspected upon outpatient examination, sinus fungus ball was suspected through CT scanning.
In the remaining thirteen cases (41%), surgery was perf- ormed under a pre-operative diagnosis of nonspecific sinusi- tis. The diagnosis of sinus fungus ball was made only after the operation and was not based on signs, symptoms or radiolog- ical findings observed at the time of outpatient examination (Fig. 1).
Intraoperative findings
Of the 32 cases of sinus fungus ball, 30 were treated with endoscopic sinus surgery and two with a Caldwell-Luc oper- ation. In two of the cases treated with endoscopic sinus surgery, the antero-inferior wall was too deep to be approached by en- doscopic instruments and a Caldwell-Luc operation was perf- ormed for this reason.
With regard to physical appearance, the fungus ball was observed during the operation as a greenish, cheese-like sub- stance in 19 cases (59%), as a brownish substance in nine cases (29%), and as a darkish substance in three cases (9%), and was accompanied by calcification in one case (3%).
Pathologic findings and fungus culture
Of the 32 cases, aspergillosis accounted for 31 cases (96.
110 / J Rhinol 5(2), 1998
9%) and mucormycosis accounted for one case (3.1%). In 14 cases, a fungus culture was conducted with a Sabouraud agar culture medium and the specimen extracted at the operation.
In two cases the fungus was positively identified as Aspergi- llus fumigatus.
In five cases, sinus fungus ball was clinically suspected due to the nature of the pus taken during surgery or to radiological findings but was not observed pathologic-histologically. The clinical characteristics of these cases are as follows：
Intraoperative findings
Out of the five cases, lesions where the fungus ball was su- spected were observed in the unilateral maxillary sinus in three cases, in the bilateral maxillary sinus in one case and in the sphenoid sinus in one case. With regard to appearance, the fungus ball was observed as a greenish cheese-like substance in one case and as a brownish substance in four cases.
Of the five cases, bilateral nasal polyps were observed in one case and an ipsilateral nasal polyp was observed in four cases.
Radiological findings
Out of the five cases, unilateral focal sinusitis findings were observed in three cases and bilateral sinusitis findings were observed in two cases.
In three cases, pre-operative radiological findings confirmed fungus ball. In two, pre-operative CT scanning revealed scle- rotic change or erosion of the neighboring bone tissue along with focal calcification inside the sinus soft tissue lesion. In one case, where maxillary sinus fungus ball was suspected after a pre-operative cerebral MRI conducted to diagnose pituitary adenoma, it was found that a decreased signal intensity lesion also existed inside the lesion that showed signal intensity in T2-highlighted imaging.
Pathologic findings and fungus culture
After staining with H&E and Gomori methenamine silver, four cases out of the five demonstrated nonspecific inflamm- ation accompanied by necrosis and one case showed chronic inflammation with calcification. However, fungal hyphae were not observed in any of the five cases. Fungus culture was pe- rformed in two, but yielded negative results.
DISCUSSION
Sinus fungus ball can be found in apparently healthy ind- ividuals and appears as chronic sinusitis or recurrent sinusitis that does not react to antibiotics. Because its symptoms, though chronic, are not intense, patients and even clinical otorhinol- aryngologist can often overlook its diagnosis.
It is generally understood that sinus fungus ball does not show any specific clinical symptoms.
1)2)The authors, however, were able to suspect sinus fungus ball prior to surgery：in 34%
of the cases in this study, there were signs and symptoms inc- luding unilateral rhinorrhea, unilateral nasal obstruction, nasal foul odor, greasy and sticky unilateral purulent pus and chronic sinusitis symptoms non-reactive to antibiotics (Fig. 1). Based on this finding, the authors propose the importance of consi- dering the possibility of sinus fungal ball even while examin- ing on an outpatient basis.
In many cases, a greasy and sticky pus may be observed at the opening of the maxillary or sphenoid sinus during the ou- tpatient examination, or fungal debris may be found in the middle meatus if the fungus ball has extended from the maxi- llary sinus to the middle meatus. In these cases, it becomes much easier to diagnose sinus fungus ball. It is known that fungus ball, in general, generates only in one side of the si- nus.
1)In this study, sinus fungus ball was found to be loca- lized to only one side of the sinus in 29 cases out of the 32 diagnosed. Fungus ball was found to extend across the maxi- llary sinus and ethmoid sinus in the remaining three cases.
While allergic fungal sinusitis is generally known to be as- sociated with nasal polyps, the relationship between fungus ball and nasal polyp is less clear. The authors identified nasal polyps in eight cases out of 32. In seven of these eight cases, ipsilateral nasal polyp was observed, suggesting the need for further study on the relationship between nasal polyp and fu- ngus ball. Stevens et al. have suggested that obstruction of the sinus opening by sinus fungus ball may act as an inducing fa- ctor,
3)so it seems reasonable to suggest that nasal polyp may promote the generation of sinus fungus ball.
In general, the authors did not conduct a PNS view but were able to obtain confirmation of the radiological characteristics that indicated fungus ball by conducting a CT scan immedia- tely when fungus ball was suspected or when, in some cases,
Fig. 1. Accuracy of preoperative diagnosis of fungus ball in di- fferent clinical steps.
Dhong, et al：Fungus Ball / 111
chronic sinusitis was observed not to react to medicinal treat- ments. Zinriech et al. reported in their study that the use of CT scanning to diagnose fungus ball is 75% accurate and that, with about 12% false positive and false negative rates, the di- agnostic value of CT scanning was superior to that of PNS views.
4)While the authors were able to make a pre-operative diagnosis of fungus ball with the aid of sinus CT scanning in 17 cases (53%), we propose a limit to the diagnostic value of CT scanning, since the procedure failed to show findings in 47% of the 32 cases of fungus ball.
With regard to 13 sinus fungus ball patients (41%), the au- thors failed to suspect sinus fungus ball after pre-operative pathological and radiological tests and made their diagnosis based only on the pathological test. Also, the possibility of fungus ball must be investigated through a histologic test if a greenish or brownish friable substance or a calcified mass is observed during the operation. While a general Hematoxylin Eosinophil could be used for histologic diagnosis, staining with PAS (periodic-acid Schiff) or methenamine silver has been found to be more effective,
5)especially since applying the pr- oper stain can prove to be important to improving the accur- acy of the diagnosis.
Among the various Aspergillus that comprise the mycelium that causes fungal sinusitis in men, the most common are A.
fumigatus, A. flavus and A. niger,
6)of which A. fumigatus is the most common and is green in color.
7)Sabrouraud’s agar is the material generally used for culturing, and the culturing temp- erature is 25-30 degrees Celsius. The culture takes at least several weeks to generate a positive result. The yield of the culture tends to be low in general, so it is inappropriate to ap- ply findings from this method to diagnostically confirm sinus fungus ball.
2)7)In a study by Klossek et al.,
1)culturing showed positive results in just 30% of cases of fungus ball. In the pr- esent study, the method yielded positive results in just two cases out of the 14 cases where a fungus culture was conducted.
The authors suggest the low yield to be a result of the low viability of the fungus inside the fungus ball, which would also explain the self-limiting nature demonstrated in most cases of fungus ball.
8)Among those cases where an operation was conducted after sinus fungus ball was suspected through outpatient examina- tions and radiological tests, five cases did not indicate sinus fungus ball pathologically despite the fact that the characteri- stics of fungus ball were observed during the operations. The authors suggest the possibility of the fungus ball-like contents whose calcification was radiologically observed, since they had
been dehydrated in the sinus for an extended period. In a st- udy by Zinreich et al., fungus ball was not found in three out of 25 cases that demonstrated the characteristics of fungus ball during surgery, despite the fact that CT scanning had generated radiological findings peculiar to fungus ball. Two of these three cases yielded a thick bacterial pus histologically, and one case displayed a bacterial infection with hemorrhage.
4)Thus, while it is clinically important to suspect fungus ball, it should be noted that a wrong diagnosis is possible without histological diagnosis.
CONCLUSION
For those patients showing symptoms such as unilateral rh- inorrhea, unilateral nasal obstruction, nasal foul odor, greasy and sticky unilateral purulent matter and chronic sinusitis sy- mptoms non-reactive to antibiotics, the possibility of sinus fungus ball should be considered and a CT scan should be conducted. In addition, it is possible that the dehydrated pus generated when the contents inside the sinus have been pres- ent for an extended period will look similar to fungus ball, so a histological test is required in order to confirm the diagno- sis of fungus ball.
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