Diagnostic Accuracy in Sinus Fungus Balls: CT Scan and Operative Findings
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1 tg.jar 200? _A:\ : Di3LiS/;-JESS Diagnostic Accuracy in Sinus Fungus Balls: CT Scan and Operative Findings Hun-Jong Dhong, M.D., Jae-Yun Jung, M.D., and Joo Hyun Park, M.D. ABSTRACT A fungus ball may be characterized by its radiologic and operative gross findings. Computed tomography (CT) revealed a rim of soft tissue attenuation of variable thickening along the bony walls of the isolated paranasal sinus, or mottled hyperdense foci of variable size. A small amount of friable muddy mass surrounded by purulent secretions or dirty brown claylike materials provide highly pathognomonic findings. However, these characteristics may induce clinical misdiagnosis. During the last four years we experienced 11 cases of chronic paranasal sinusitis in which pathologic examination failed to confirm fungal hyphae, despite clinical suspicion of a fungus ball based on operative or CT findings. During the same period, we also experienced another 52 patients who were diagnosed with fungus ball at pathologic examination. To evaluate the diagnostic accuracy of CT scans and operative gross findings in sinus fungus balls, we reviewed the medical records of these 63 patients and also reviewed CT scans and operative records of another 1127 patients who received endoscopic sinus surgery for chronic rhinosinusitis. The sensitivity of CT evaluation was 62%, and specificity was 99%. The false-positive and false-negative rate were 22% and 2%, respectively. With regard to operativefindings,such as clay-like inspissated mucus, the sensitivity, specificity, and predictive value positive rate were 100%, 99%, and 83%, respectively. To make a diagnosis of fungus ball, a high index of suspicion is From the Department of Otorhinolaryngology, Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul, Korea _ Address correspondence and reprint requests to Dr. Hun-Jong Dhong, Department of Otorhinolaryngology, Sungkyunkwan University, School of Medicine, Samsung Medical Center, 50 llwon-dong Kangnam-gu, Seoul , Korea necessary and a pathologic confirmation is mandatory. (American Journal of Rhinology 14, , 2000) Making an accurate diagnosis of fungal sinusitis is extremely important. Though the classification systems for fungal sinusitis have been both confusing and inconstant, misdiagnosis of noninvasive disease may lead to therapeutic misadventure. Invasive sinus disease may cause death. Also, an accurate diagnosis is still more important in fungus ball, formerly referred to as mycetoma or aspergilloma, since it can only be cured completely with proper surgical removal. However, it is hard to detect fungus ball by the clinical symptoms and signs. Fungus ball should be considered as a differential diagnosis of isolated unilateral sinusitis or recurrent sinusitis that is not responding to medical therapy. Widespread use of the nasal endoscope and recent developments in imaging technologies have made diagnosis of fungus ball easier. The discharge may exhibit unusual gray or greenish brown color. It is usually accompanied by unilateral nasal obstruction. Small amounts of a decaying, friable mass may sometimes be detected in the middle meatus. Several well-defined mottled calcifications in the unilateral isolated paranasal sinus are considered as a highly suspicious CT finding of sinus fungus ball. Intraoperatively, a dirty brown, greenish muddy mass is well known to be a specifically pathognomonic finding. However, these findings are not always observed and may sometimes induce clinical misdiagnosis. It is also necessary that the diagnosis should be confirmed in pathological study. In this study, the authors looked for the diagnostic accuracy of these clinical, radiologic, and operative findings. Analysis was performed on 1190 patients who received ESS for chronic rhinosinusitis, including 52 cases that were histologically confirmed as fungus ball, and 11 cases of clinical misdiagnosis in which fungus ball was suspected, American Journal of Rhinology 227
2 but not observed bistopathologically. The sensitivity and predictive positive values of clinical signs, CT scan, and operative finding were evaluated. MATERIALS AND METHODS Endoscopic sinus surgery for chronic rhinosinusitis was performed on 1190 patients from January 1995 through December 1998 at the Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center. Among them, 52 cases were diagnosed as fungus ball histologically. Eleven cases were clinically misdiagnosed as fungus ball. In these cases, pathologic examination failed to confirm fungal hyphae despite a clinical suspicion of fungus ball based on the operative findings. We reviewed the medical records of these 63 patients to evaluate the clinical characteristics, including intra-operative findings. The patients consisted of 31 men and 32 women, ranging in age from 27 to 84 years with a mean of 52 years. Allergic fungal sinusitis and invasive types of fungal sinusitis were excluded. We reviewed clinical signs, radiologic findings, and intra-operative gross findings retrospectively. Unilateral greasy gelatinous rhinorrhea on endoscopic examination from the middle meatus or the sphenoethmoidal recess was considered as a positive clinical sign (Fig. 1). In addition, we reviewed OMC-CT scans and operative records in another 1127 patients who received endoscopic sinus surgery to calculate sensitivity and specificity, predictive value positive, false positive and false negative rate of CT, and gross finding. All CT studies were performed with bone algorithms and a 3-mm contiguous scan technique without administration of contrast material. The CT scans were routinely evaluated with a window width of 2300 and a level of 300. The windows were changed to enhance the contrast between the focal high-density area and surrounding inflammatory tissue for optimal evaluation of the fine calcifications. Hyperattenuated foci were considered to be present when the focal high-density area was higher in CT attenuation than that of the surrounding inflammatory tissue and closer to discrete bone density (Fig. 2). However, two cases of smooth margined nodular calcification in the maxillary sinus that were compatible with osteoma were excluded. As positive operative findings, dry friable substance, dark muddy material, whitish-yellow to dirty brown masses ranging in variable consistency with or withom purulent secretion were selected. RESULTS Diagnostic Value of Clinical Signs Twelve patients demonstrated unilateral greasy gelatinous discharge on endoscopic examination. Ten patients showed discharge from the middle meatus and two cases from the sphenoethmoidal recess. All 12 patiems revealed fungal hyphae on pathologic examination. The predictive value positive rate of this finding was 100%. However, sensitivity was 23%. Nasal polyps were revcaleo in 15 patients. In 13 patients, nasal polyps were observec unilaterally on the same side as the fungus ball, whereas bilateral polyps were observed in two patients. When only ipsilateral polyps were considered as positive, sensitivity was 25%. middle meatus. sinus, which suggests fungus ball. 228 July-August 2000, Vol. 14, No. 4
3 f Agnostic Yalue of CT Findings " crty-one of 1190 patients demonstrated focal hyperat-, v.enuation in the soft-tissue sinus masses on CT exami ; tlo.i. In 39 of 41 cases the findings were observed in the traxllary sinuses; two cases involved the sphenoid sinus. f-lty-two patients revealed fungus ball histologically, Al- 'lojgt nine patients showed focal calcification in the rnaxa;y sinus, they revealed non-fungal sinusitis. Among, :,n, six cases had linear calcification along the bony wall j ne maxillary sinus (Fig. 3). At pathologic examination, tnrec of these nine patients demonstrated very thick, inspiss;.ed oacterial pus and one demonstrated inflammatory exo. ate with positive bacterial culture, and five cases showed chronic inflammation with calcification. In addition, 20 o.ttlsr.ts were not clinically diagnosed with CT scans and were only identified as fungus ball after pathology proved pos.tive. When focal hyperattenuated lesions of variable s'ze in the isolated paranasal sinus were considered as :osh'.ve, diagnostic values were as follows. Sensitivity, specificity, false positive, false negative, and predictive va.ae positives were 62%, 99%, 22%, 2%, and 78%, respscthely (Table I). TABLE I Pathologic Results versus CT Finding which Suggested Fungus Ball (n = 1190) Positive pathology Negative pathology Positive 32 9 CT Finding Negative Diagnostic Value of Intraoperative Gross Findings if the 52 cases of fungus ball, 50 were treated with sndoscopic sinus surgery and two with a Caldwell- Luc procedure. With regard to physical appearance, the fungus ball was observed during the operation as a greenish, cheese-like dry substance in 24 cases, as a brownish dry substance in 21 cases, and as a dark muddy substance in six cases, and was accompanied by a stony hard calcification in one case. Of the 11 clinically misdiagnosed cases, lesions where the fungus ball was suspected were unilateral maxillary sinus in five cases, bilateral maxillary sinus in one case, and sphenoid sinus in three cases. With regard to the operative appearance, inspissated mucus was observed as a dark greenish dry substance in one case and as a brownish muddy to dry substance in 10 cases. Gross findings were considered as positive when greenish cheese-like dry substance, brownish dry substance, and dark muddy substance with or without purulent secretion were observed. The sensitivity of positive gross finding was 100%. Specificity, false positive, false negative, and positive predictive values were 99%, 17%, 0%, and 83%, respectively (Table II). DISCUSSION Fungus ball, the most frequent form of fungal sinusitis, is defined as the presence of a mycelial mass that remains confined to the lumen of the sinus cavity, usually in the maxillary antrum. It can develop in apparently immunocompetent individuals and appears as chronic sinusitis or recurrent sinusitis that does not react to antibiotics. Usually patients, and even otorhinolaryngologists, can overlook its TABLE II "'jure 3. Linear opaciflcation along the sinus floor (A) and <.'»-;.' wall IB). The peripheral location of calcification is chari'i tcstic in non-fungal sinusitis. Pathologic Result versus Intra-Operative Gross Finding which Suggested Fungus Bali in = 1190) Positive pathology Negative pathology Intra-Operative Gross Finding Positive Negative V-erican Journal of Rhinology 229
4 diagnosis, because its symptoms, though chronic, are mild and nonspecific. It is generally understood that fungus ball does not show specific symptomatology. 1-2 However, the authors were able to suspect fungus balls prior to surgery in 36 cases (69%) among 52 patients diagnosed histopathologically, and in 19 patients simply based on clinical signs and symptoms before performing CT scans. Unilateral nasal obstruction, nasal foul odor, unilateral greasy and sticky purulent discharge, and chronic sinusitis symptoms non-reactive to antibiotics were diagnostic clues in our series. Only 15 of these 19 cases showed CT findings compatible with a fungus ball. Recent advances in nasal endoscopy have been helpful in raising preoperative diagnostic accuracy. Fungal debris may be detected in the outpatient clinic if the fungus ball has extended to the middle meatus. Sensitivity of unilateral oily gelatinous discharge in this study was 23% and positive predictive value was 100%. When nonspecific unilateral rhinorrhea was considered as positive, diagnostic accuracy was decreased. The sensitivity of positive nonspecific unilateral rhinorrhea was 17%. An oily, gelatinous discharge appears to be a more specific characteristic of fungal sinusitis. It is known that a fungus ball most often affects a single sinus, most commonly involving the maxillary antrum. 3-4 In this study, all 52 diagnosed cases were unilateral and fungus ball was localized to a single sinus in 44 cases. Fungus ball was found to extend across the maxillary sinus and ethmoid sinus or sphenoid sinus in the remaining 8 cases. The relationship between fungus ball and nasal polyps is not clear. However, allergic fungal sinusitis is usually associated with nasal polyps. The authors identified nasal polyps in 15 of 52 cases. In 13 of these 15 cases, unilateral nasal polyps adjacent to the lesion site were observed. Stevens et al. have suggested that functional obstruction of the sinus ostium may act as an inducing factor and that the fungal growth is favored by hypoxic or anaerobic conditions. 5 Therefore, it seems reasonable to suggest that nasal polyps may promote the generation of sinus fungus ball. Bacterial and viral superinfections with purulent secretion provide the fungus with nourishment. Decreased ventilation lowers the ph and favors the growth of hyphae. Damage to the mucosa and especially to the cilia in chronic recurring sinusitis hinders the transport of pathologic secretions and thus of the fungi as well. 6 In general, fulminant fungal sinusitis develops in immunocompromised patients and fungus ball in apparently immunocompetent individuals. In our series, 10 cases had diabetes among the 52 cases of fungus ball. However, the number of diabetes patients among 1138 patients who received endoscopic sinus surgery for chronic rhinosinusitis during the same^eriod was 16 (1.3%). Thus, the incidence of diabetes was higher in the fungus ball population with a statistical significance (Fisher's exact test, p < 0.001). Among 36 cases suspected preoperatively, in 17 cases where bacterial sinusitis was suspected upon outpatient ex- amination, fungus ball was suspected by CT scan. In the remaining 16 cases (31%) of 52, surgery was performed under a preoperative diagnosis of bacterial sinusitis. Zinreich et al. reported that the use of CT scans to diagnose fungus ball is 75% accurate and that, with ~12% false positive and false negative rates, the diagnostic value of CT was superior to that of standard radiography or pluridirectional tomography. 7 In this study, the authors were able to make a preoperative diagnosis of fungus ball with the aid of CT in 32 cases (62%). We think that there is a limit to the diagnostic value of CT, since the CT failed to show typical findings in the remaining 20 cases. In 16 fungus ball patients (31%), the authors failed to suspect fungus ball before operation despite careful examination and radiologic tests. The possibility of fungus ball was confirmed by a histologic test when a greenish or brownish dry friable substance or a calcified mass was observed during the operation. Of the 52 cases, aspergillus accounted for 50 cases (96%) and mucor species accounted for two cases (4%) based on pathology. In 19 cases, where fungal culture was conducted, only two cases were positively identified as Aspergillus fumigatits. While H&E staining could be used for histologic diagnosis in general, staining with PAS (periodic-acid Schiff) or methenamine silver has been found to be more effective. 8 Among the various Aspergillus species that cause fungal sinusitis in men, the most common are A. fiimigatus, A. flavus, and A. niger, 9 of which A. fitmigatus is the most common, and is green in color. 10 Sabrouraud's dextrose agar is the material generally used for culturing, and the proper culturing temperature is C. At least several weeks are required before the culture generates a positive result. However, the yield of the culture tends to be low in general, so in our hands it has been inappropriate to apply findings from this method to diagnostically confirm fungus. 10 In a study by Klossek et al. 1 culturing showed positive results in just 30% of cases of fungus ball. In the present study, the method yielded positive results in just two cases of the 19 cases where a fungus culture was conducted. The authors suggest the low yield is the 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. 11 Intraoperatively, a dirty, clay-like mass is a specifically pathognomonic finding of fungus ball. However, 11 cases did not demonstrate fungus pathologically despite characteristic intraoperative findings. After staining with H&E and Gomori methenamine silver, 9 of 11 cases demonstrated nonspecific inflammation accompanied by necrosis, one case showed chronic inflammation with calcification, and one case showed inflammatory exudate with bacterial colony. However, fungal hyphae were not observed in any of the 11 cases. Fungus culture was performed in four, but yielded negative results. 230 July-August 2000, Vol. 14, No. 4
5 CONCLUSION For those patients showing symptoms such as greasy and sticky unilateral purulent discharge and chronic sinusitis symptoms non-reactive to antibiotics, the possibility of fungus ball should be considered and a CT scan should be performed. In addition, it is possible that dehydrated pus present for a long period will look grossly similar to fungus ball, so histologic testing is essential to positively confirm the diagnosis. REFERENCES 1. Klossek JM, Serrano E, Peloquin L, et al. Functional endoscopic sinus surgery and 109 mycetomas of paranasal sinuses. Laryngoscope 107: , Morpeth JF, Rupp NT, Dolen \VK, et al. Fungal sinusitis: an update. Ann Allergy Asthma Immunol 76: , Min YG, Kim HS, Kang MK, and Han MH. Aspergillus sinusitis: clinical aspects and treatment outcomes. Otolaryngol Head & Neck Surg 115:49-52, Ferreiro JA, Carlson BA, and Cody DT. Paranasal sinus fungus balls. Head & Neck 19: , Stevens MH. Aspergillosis of the frontal sinus. Arch Otolaryngol 104: , Stammberger H. Endoscopic surgery for mycotic and chronic recurring sinusitis. Ann Otol Rhinol Laryngol 94(suppl 119):1-11, Zinreich SJ, Kennedy D\V, Malat J, et al. Fungal sinusitis: diagnosis with CT and MR imaging. Radiology 169: , Meikle D, Yarington CT, and Winterbauer RH. Aspergillosis of maxillary sinuses in otherwise healthy patients. Laryngoscope 95: , Stevens MH. Primary fungal infections of the paranasal sinuses. Am J Otolaryngol 131: , deshazo RD, O'Brien M, Chapin K, et al. Criteria for the diagnosis of sinus mycetoma. J Allergy Clin Immunol 99: , Cambell MJ, and Clayton YM. Bronchopulmonary aspergillosis: a correlation of the clinical and laboratory findings in 272 patients investigated for bronchopulmonary aspergillosis. Am Rev Respir Dis 89:186^196, American Journal of Rhinology 231
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