https://orcid.org/0000-0002-9860-3293
Abstract
Scattered reports have found that sinus fungus ball (SFB) may progress to chronic invasive fungal rhinosinusitis (CIFRS), but the mechanism is not yet understood. Distinguishing between SFB and CIFRS is sometimes tricky. The invasive features of CIFRS make the symptoms and imaging findings indistinguishable from those of malignant tumors. We herein report a case in which a patient was examined and treated very early in the transition from SFB to CIRFS. An 81-year-old woman with CIFRS was treated with surgery and Voriconazole. Computed tomography (CT) showed a typical high-intensity mass in the maxillary sinus and bony hypertrophy with unusual bony erosion. Magnetic resonance imaging (MRI) showed clear contrast between edematous mucosa and mucosa with CIFRS. The diffusion coefficient (ADC) value in particular was limited to a portion of the CIFRS lesion. The ADC value is helpful as a reference for evaluating the transition of SFB to CIFRS.
Introduction
Based on histological findings, fungal rhinosinusitis is divided into invasive and non-invasive types, and the invasive type is subdivided into acute invasive fungal rhinosinusitis (AIFRS) and chronic invasive fungal rhinosinusitis (CIFRS) [Citation1]. Immunocompromised patients are susceptible to invasive fungal rhinosinusitis (IFRS) and can suffer a fatal course [Citation2]. In contrast, sinus fungus ball (SFB) is classified as the non-invasive type. Most patients with SFB are immunocompetent and asymptomatic or have rhinosinusitis symptoms [Citation3]. Scattered reports suggest that SFB may develop into IFRS, and some authors recommend antifungal treatment as postoperative therapy for immunocompromised patients with SFB [Citation4–5]. However, performing surgery is the only way to determine the precise transition timing and make a definitive diagnostic. Furthermore, the invasive characteristics of CIFRS are sometimes misleading, causing confusion with malignant tumors.
We experienced a patient with specific imaging findings during the transition of SFB to CIFRS. We herein report the imaging findings of this patient, including computed tomography (CT) and magnetic resonance imaging (MRI), as a potential reference for the preoperative diagnosis of CIFRS. These images demonstrate the differences among mucosa with CIFRS, typical inflammatory mucosa, and malignant tumors.
Case presentation
An 81-year-old woman was referred to our department for an evaluation of right cheek pain lasting 2 weeks. The patient’s medical history revealed the presence of hepatitis C virus infection.
An endoscopic examination showed no abnormal findings in the right nostril. We confirmed the soft-tissue shadows with calcification at the right maxillary sinus and partial bone thickening and bone erosion at the posterior wall of the maxillary sinus in CT (Figure ). MRI showed a hypo-intense signal on T1-weighted imaging (T1WI) and significantly hypo-intense signal on T2-weighted imaging (T2WI) at the center of the right maxillary sinus (Figure ). The posterior wall of the maxillary sinus showed intermediate signal intensity on T1WI and a hypo-intense signal on T2WI. Although the maxillary sinus mucosa and pterygopalatine fossa showed an extensive contrast effect on gadolinium (Gd)-enhanced fat-suppression T1WI, the decrease in the apparent diffusion coefficient (ADC) was limited to the maxillary sinus (Figure ). A biochemical examination of the blood revealed β-D-glucan positivity (39.6 pg/ml). Based on these findings, we considered the possibility of CIFRS, but a malignant tumor could not be ruled out as a differential diagnosis. Endoscopic sinus surgery was therefore performed for diagnostic and therapeutic purposes.
Figure 1. Computed tomography scan showing soft-tissue shadows with calcification (arrowhead) on the right maxillary sinus with partial bone thickening and bone erosion (arrow) in the posterior wall of the maxillary sinus (a: coronal, b: axial).
Figure 2. (a) Magnetic resonance imaging showing a hypo-intense signal at the center of the right maxillary sinus and an intermediate signal intensity at the posterior of the posterior wall of the maxillary sinus on T1-weighted imaging (T1WI). (b) T2-weighted imaging shows a significant hypo-intense signal at the center of the right maxillary sinus. Maxillary mucosa showed substantial contrast between the hypo-intense signal at the posterior wall and the hyper-intense signal in the rest of the maxillary sinus. (c) Gadolinium-enhanced fat-suppression T1WI shows that the entire maxillary sinus mucosa and pterygopalatine fossa were enhanced (arrowhead). (d) in contrast, the decrease in the apparent diffusion coefficient was limited to a portion of the posterior wall of the maxillary sinus (arrow), while the rest of the maxillary mucosa and pterygopalatine fossa was not enhanced.
Thirteen days after the patient’s visit to our department, transnasal endoscopic sinus surgery was performed under general anesthesia. Endoscopic modified medial maxillectomy helped reach the lesion and secure the surgical field [Citation6]. The maxillary sinus was filled with a gray, clay-like material compatible with a fungus ball, and Aspergillus fumigatus was detected in cultivation survey (Figure ). There was no evidence of allergic mucin, suggestive of allergic fungal rhinosinusitis. When all of the material was removed, granulation formation was seen at the posterior wall of the maxillary sinus (Figure ). The mucosa of the maxillary sinus aside from that at the posterior wall was pale, thickened edematous mucosa, as commonly seen in SFBs. Granulation tissue was excised as much as possible and submitted for a rapid histological examination, the results of which showed fungal mucosal infiltration but no malignant findings (Figure ). The maxillary sinus was opened into the middle and inferior meatus.
Figure 3. Endoscopic findings showing the right maxillary sinus via the inferior Nasal meatus. (a) The maxillary sinus was filled with fungus balls. (b) Granulation formation was seen at the posterior maxillary wall.
Figure 4. A Histologic examination shows septate and branched fungi (arrowhead) infiltrating the mucosal interstitium with ulcer formation (hematoxylin and eosin ×100).
A confirmed diagnosis of CIFRS accompanying SFB was obtained, and voriconazole (VRCZ) was administered on the day of surgery. Blood biochemistry tests were performed on postoperative day 5, confirming that the trough value of VRCZ was appropriate and that the β-D-glucan level had decreased to 21.9 pg/ml. The patient was discharged from the hospital on postoperative day 12 after surgery with good progress and continues to receive treatment on an outpatient basis.
Discussion
We reported a case with specific imaging findings of concurrent SFB and CIFRS. This case is definitive proof of the transition between SFB and CIFRS. Through this case, we believe that, in addition to T2WI findings, the ADC is a critical image parameter for distinguishing CIFRS from SFB and malignant tumors. The coronavirus pandemic has led to an increasing number of infections with Aspergillus [Citation7]. Since aspergillus infection can cause serious complications, appropriate treatment should be initiated early [Citation8]. The findings obtained in this study are instructive.
The CT findings in our patient are, in part, textbook examples of SFB. Calcification spot or intralesional hyperdensity on CT is a typical finding suggestive of SFB [Citation9]. Especially in SFB in the maxillary sinus, sclerosis of the lateral sinus wall, erosion of the inner sinus wall, and irregular surface of the material were reported as characteristic findings [Citation10]. From the formation of the fungus ball and bone thickening, was can assume that the patient had been affected by SFBs for some time. Meanwhile, erosion of the posterior wall suggested invasive ness of the lesion. The probability of progression from SFBs to IFRS is estimated to be 0%-1.6%, with some variation shown among reports [Citation11–13]. Assari et al. suggested that SFBs may progress to IFRS, particularly in elderly and immunocompromised patients [Citation13]. All previous reports described the chronological transition from SFB to IFRS and lacked evidence of the moment of transition. In our patient, only the posterior wall of the maxillary sinus evolved to CIFRS, and the remaining maxillary sinus stayed an SFB. Interestingly, our 81-year-old patient was not immunocompromised and did not fit the typical CIFRS background.
In addition, a decreased ADC value was observed. It was necessary to differentiate this case from a malignant tumor, and the ADC is an objective indicator of the tissue-specific diffusion capacity. In malignant tumors, nuclear hypertrophy and increased cell density impede the diffusion of water molecules, resulting in reduced ADC values [Citation14]. In rhinology, it has been reported that the ADC is also decreased during the malignant transformation of inverted papilloma [Citation15]. Still, to our knowledge, no reports have examined the association between fungus infection and the ADC. In the present case, a decrease in the ADC was observed in the posterior maxillary wall, where pathology showed mucosal invasion of fungus but no decrease in the ADC in the rest of the maxillary sinus. This signal difference provides valuable insight into whether or not SFBs transitioned to CIFRS based on ADC values.
Li et al. compared the MRI findings of CIFRS and sinonasal squamous cell carcinoma (SNSCC) and found that CIFRS and SNSCC have different imaging characteristics, contrast enhancement patterns, and T2 signal intensity [Citation16]. According to their study, compared with SNSCC, CIFRS was associated with a hypo-intense signal on T2WI, septal enhancement, and loss of contrast enhancement. In our case, the area where pathology showed fungal submucosal invasion had a hypo-intense signal on T2WI, and the ADC was also decreased. In contrast, the maxillary sinus mucosa is circumferentially contrast-enhanced. T2WI findings and ADC values should be referenced rather than contrast enhancement to estimate the extent of fungal infiltration.
All MRI findings in the present case indicated CIFRS invasion to the pterygopalatine fossa, except for the ADC. The signal of the posterior wall of the maxillary sinus and the pterygopalatine fossa were identical on T1WI, T2WI, and Gd-enhanced contrast imaging. Interestingly, the ADC indicated an intact pterygopalatine fossa. Unfortunately, we did not take samples from the pterygopalatine fossa in order to avoid injuring the maxillary artery, and we were sure that radical surgery was not needed for CIFRS. These discrepancies between standard settings and the ADC might help distinguish CIFRS from malignant tumors. Further studies are required to confirm these inconsistencies. We believe that, in elderly patients with SFB, surgical treatment should be recommended in order to prevent conversion to IFRS.
Conclusion
We experienced a patient with specific imaging findings during the transition of SFB to CIFRS. The ADC value is helpful as a reference for evaluating the transition of SFB to CIFRS.
Informed consent
Written informed consent was obtained from the patient for the publication of these findings.
Disclosure statement
No sponsorships or competing interests must be disclosed for this article.
Additional information
Funding
References
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