Clinical Radiology (1992) 45, 319 321
CT Findings in Paranasal Aspergillosis p. J. PATEL, T. M. K O L A W O L E , T. M. M A L A B A R E Y , A. H U L A I L A H , F. H A M I D * and M. CHAKAKI1-
Radiology Department, King Khalid University Hospital, *Security Forces Hospital and ~fCentral Hospital, Riyadh, Saudi Arabia Computed tomographic (CT) scan of eight cases of paranasal sinus aspergillosis were reviewed. Different CT patterns were observed such as areas of high densities, linear interlacing network of h!gh density, radiolucent thin rim periphery to the masses, calcification, expansion of involved sinuses and bone erosion. Two cases of invasive type showed extension beyond the sinuses into the orbit and intracranially simulating a malignant tumour. The findings are similar to those described by previous authors. The differential diagnosis is also discussed. Patel, P.J., Kolawole, T.M., Malabarey, T.M., Hulaitah, A., Hamid, F. & Chakaki, M. (1992). Clinical Radiology 45, 319-321. CT Findings in Paranasal Aspergillosis.
Fungal infection of the paranasal sinuses is an u n c o m m o n disease. Aspergillosis is a fungal disease caused by the aspergillus fungus of the ascomycites group which has a worldwide distribution. Aspergillosis commonly involves the lungs. However, sinus aspergillosis remains a rare condition even though there is a recent increase in the number of isolated cases reported in the literature (Robb, 1986). This disease has been described almost exclusively in Africa, specifically in Sudan. One case has been described from Saudi Arabia (Dawlatly et al., 1988). There are only a few reports of sinus aspergillosis in the literature. The reports of computed tomographic (CT) scan findings are few (Jinkins et al., 1987; Som et al., 1987; Quiney et al., 1988). A retrospective study of aspergillosis of the paranasal sinuses as seen in Riyadh was therefore undertaken to determine the CT scan features of this disease.
presented with a history of sinusitis and headaches. One patient also had exophthalmos and fever. The duration of symptoms before diagnosis varied from 4 months to 2.5 years, with an average, of 13.2 months. Aspergillosis fumigatus was isolated from the paranasal sinuses in all cases. Plain Film Findings The maxillary antra were abnormal in all cases, and the ethmoid sinuses in six cases. The sphenoid and the frontal sinuses were involved in three and two cases respectively. Five cases showed non-homogeneous opacities whilst three showed homogeneous opacities in the involved sinuses. Other findings were calcifications in three cases, erosions of the sinus wall in two cases and expansion of the sinus in one case. CT Findings
M A T E R I A L S AND M E T H O D S We reviewed retrospectively the CT scans of sinuses in eight cases of aspergillosis from three different hospitals in Riyadh. The diagnosis was made in all cases by positive histological examination of the specimens. All the CT examinations were performed on one of three scanners: G E 9800, S o m a t o m II, or Somatom D R H , using a sinus protocol to produce contiguous axial scans, carried out parallel to the inferior orbitomeatal (IOM) plane, from the maxillary alveolus to the superior aspect of the frontal sinuses. The scans were 5 m m (GE 9800) or 4 m m (Somatom 2, Somatom D R H ) thick. Coronal scans were performed 90 ° to the I O M plane using the same slice thickness. Enhanced scans w e r e a l s o carried out after intravenous contrast medium (Conray 420, 50 ml) using the same protocol. RESULTS The patients studied were four males and four females, with ages ranging from 14 years to 39 years (mean age, 28 years). All patients (six Saudis and two Sudanese) Correspondence to: Dr P. J. Patel, Associate Professor, Radiology Department No. 40, King Khalid University Hospital, P.O. Box 2925, Riyadh, 11461, Saudi Arabia.
CT showed calcifications in seven cases, including four cases in which calcification had not been demonstrated on the plain films. More extensive calcifications were seen in each case than demonstrated by plain films. CT demonstrated bony wall erosion in five cases, and in three cases this was more extensive than shown on plain films. The CT pattern shown in two cases was of homogeneous, high attenuation, polypoidal opacities, whilst in six others it was of non-homogeneous, either linear interlacing high density or nodular opacities. One case which produced homogeneous shadowing on plain films turned out to be non-homogeneous on CT. The CT findings are listed in Table 1. DISCUSSION Stammberger et al. (1984) quote Schubert as the first person to described aspergillosis of the nose and paranasal sinuses in 1885. It is the commonest cause of fungal infection of the sinuses. However, only about 115 cases have been described in the English literature, mostly as case reports (McGuirt and Harrill, 1979). It appears that the incidence of a fungal infection in the nose and paranasal sinuses has increased because of the increasing use of antibiotics, steroids, cytotoxic and other chemotherapeutic agents (Robb, 1986). Aspergillosis of
320
CLINICAL RADIOLOGY
Table 1 - S u m m a r y of C T findings in aspergiliosis
Total cases: 8 A Sinuses Maxillary antrum Ethmoid Frontal Sphenoid B C D E F G
Unilateral 3 1 2
Nasal cavity Bone erosion of involved sinuses Expansion of sinuses Intraorbital extension Intracranial extension CT findings of mass: Homogeneous density Non-homogeneous density Average CT density (HU) Enhancement (mild) Rim of lucency Calcification Bone sclerosis
Bilateral 5 5
Total 8 6 2 3
5 5 2 2 2 2 6 764 (range 172-1023 HU) 3 4 7 1
Fig. 2 CT scan shows multiple linear interlacing network of high density with nodules in the ethmoidal sinuses which are expanded.
Fig. 1 Diffuse nodular high density masses involving the maxillary antra and nasal cavity. There is a radiolucent rim peripherally (arrows).
the sinuses is c o m m o n in S u d a n (Milosev et al., 1969), a n d only one case has been reported in a Saudi p a t i e n t (Dawlatly et al., t988). There are two types o f sinus aspergillosis: invasive a n d non-invasive. T h e m a i n difference between the two is o f b o n e destruction which typifies the invasive type. The majority of cases o f the invasive type p r o d u c e orbital or i n t r a c r a n i a l complications. A C T scan is very useful in detecting the b o n e destruction, thus differentiating the two types. O u r study confirms the view o f K o p p et al. (1985) that the maxillary a n t r u m is the most c o m m o n l y involved sinus. However, bilateral i n v o l v e m e n t of the a n t r a was c o m m o n e r in our study t h a n in other studies, where the changes were usually unilateral. The e t h m o i d sinus was the next c o m m o n e s t site, a n d in five out o f six patients the changes were again bilateral. The nasal cavity itself was involved in five cases.
Fig. 3 Invasive aspergillosis: coronal CT scan reveals non-homogeneous opacity in the left antrum extending into the left orbit and left anterior cranial fossa. Note the erosion of medial wall of left orbit and left aspect of the floor of anterior cranial fossa, through which the mass has eroded.
C T findings include slightly e n h a n c i n g masses of soft tissue density filling a sinus cavity a n d separated from the sinus wall by a thin rim of m u c o i d density material which has a lower a t t e n u a t i o n value t h a n the fungal mass (Jinkins et al., 1987). These findings were observed in four
CT FINDINGS IN PARANASAL ASPERGILLOSIS
of our cases (Fig. 1). The most characteristic pattern of multiple, linear interlacing network of high density, described by Som et al. (1987), was present only in two of our cases (Fig. 2). Concentric or polypoidal thickenings of the mucosal lining have also been reported. In a previous report, reference was made to the high attenuation values of the concretions which were found to be about 2000 H U (Kopp et al., 1985). The average CT value in our cases was much lower (about 764 HU). Calcifications were seen in seven out of eight cases (Fig. 2). The calcifications are due to tertiary calcium phosphate (apatite) d@osits within the necrotic area of the mycelium (Kopp et al., 1985). Intracranial manifestations such as granuloma formation, meningitis, meningo-encephalitis, abscesses, vasculitis, aneurysm formation, infarction and haemorrhage have been described in the literature (McGill, 1980; Som et al., 1987; Sowagar and Shadid, 1987). The commonest intracranial complication is granuloma formation. Two of our cases showed granuloma formation in frontal lobes, a direct extension from the sinuses (Fig. 3). There was no other intracranial complication in our series. lntracranial aspergillosis causes bone erosion and soft tissue enhancement which is usually surrounded by a rim of oedema (Jinkins et al., 1987). However, its continuity with the sinus aspergillosis makes the diagnosis straight forward. Extension of aspergillosis into the orbits causing proptosis was the commonest cause of a non-congenital unilateral proptosis in Sudan (Milosev et al., 1969; Kopp et al., 1985). Proptosis was only seen in one of our cases. In general, CT was useful in demonstrating the presence of calcifications, erosions, and extensions into the surrounding area as well as characterizing the type of pattern within the soft tissue densities in the sinuses In a study of 103 cases, the invasive type was associated with a far higher mortality than a non-invasive type - 16 out of 17 deaths occurring in this type (Jahrsdoerfer et al., 1979). Non-invasive aspergillosis of the sinuses is usually treated with amphotericin B, coupled with surgical removal of the infected material. The invasive type usually requires more aggressive treatment with additional drugs such as Ketokonazole, in conjunction with surgical excision of the aspergillosis mass, sinus curettage and drainage. Our two 'invasive' cases were treated successfully in this fashion. The differential diagnosis of sinus aspergillosis includes chronic bacterial sinusitis, malignant neoplasm, benign neoplasm, tuberculosis, osteomyelitis of the maxilla, Wegener's granuloma, rhinoscleroma and mucomycosis, polyps and fibrous dysplasia (Robb, 1986). A number of
321
these conditions are rare, difficult to confirm clinically and difficult to distinguish from aspergillosis radiologically. Polyps are seen as masses of low density with a cascade-like appearance, whereas aspergillosis produces streak-like densities extending from the central area (Som et al., 1987). We have not found these differentiating features to be particularly useful. A rim of low density due to mucoid material, areas of high density, erosion and expansion of the sinuses are features that are more useful in differentiating between aspergillosis and polyps in our experience, as well as others (Som et al., 1987). Radiographic investigations, especially CT, may help in the differential diagnosis of disorders affecting the sinuses but more importantly, CT is useful in delineating the extent of the disease in aspergillosis. Skin tests and serology for aspergillosis precipitins are usually inconclusive (Milosev et al., 1969; Robb, 1986). Hispathological examination of the sinus contents obtained by biopsy is therefore mandatory.
REFERENCES Dawlatly, EE, Anim, JT, Sowayan, S & E1-Hassan, AY (1988). Primary paranasal aspergillus granuloma in Saudi Arabia. Tropical and Geographical Medicine, 40, 247 250. Jahrsdoerfer, RA, Ejercito, VS, Johns, MME, Cantrell, RW & Sydney, JD (1979). Aspergillosis of the nose and paranasal sinuses. American Journal of Otalaryngology, 1, 6- 14. Jinkins, JR, Sigueira, E & Zuheir Al-Kawi, M (1987). Cranial manifestations of aspergillosis. Neuroradiology, 29, 18 L 185. Kopp, W, Fotter, R, Steiner, H, Beaufort, F & Stammberger, H (1985). Aspergillosis of the paranasal sinuses. Radiology, 156, 715 716. McGill, TJ, Simpson, G & Healey, GB (1980). Fulminant aspergillosis of the nose and paranasal sinuses. A new clinical entity. Laryngoscope, 90, 748-754. McGuirt, WF & Harrill, JA (1979). Paranasal sinus aspcrgillosis. Laryngoscope, 89, 1563-1568. Milosev, B, Mahgoub, EI-SA & Hassan, AMM (1969). Primary aspergilloma of the paranasal sinuses in Sudan: a review of seventeen cases. British Journal of Surgery, 56, 132 137. Quiney, RE, Rogers, M J, Davidson, RN & Cheesman, AD (1988). Craniofacial resection for extensive paranasal sinus aspergilloma. Journal qf Laryngology and Otology, 102, 1172 1175. Robb, PJ (1986). Aspergillosis of the paranasal sinuses: a case report and historical perspective. Journal of Laryngology and Otology, 100, 1071-1077. Sore, PM, Sachet, M, Lawson, W &Biller, H 0987). CT appearance distinguishing benign nasal polyps from malignancies. Journal of Computer Assisted Tomography, 11, 129 133. Sowdagar, R & Shadid, H (1987). Invasive aspergillosis of the paranasal sinuses. Emirates Medical Journal, 5, 67 70. Stammberger, H, Jakse, R & Beaufort, F (1984). Aspergillosis of the paranasal sinuses: X-ray diagnosis, histopathology, and clinical aspects. Annals"of Otology, Rhinology and Laryngology, 93, 251 256.
CT Findings in Paranasal Aspergillosis p. J. PATEL, T. M. K O L A W O L E , T. M. M A L A B A R E Y , A. H U L A I L A H , F. H A M I D * and M. CHAKAKI1-
Radiology Department, King Khalid University Hospital, *Security Forces Hospital and ~fCentral Hospital, Riyadh, Saudi Arabia Computed tomographic (CT) scan of eight cases of paranasal sinus aspergillosis were reviewed. Different CT patterns were observed such as areas of high densities, linear interlacing network of h!gh density, radiolucent thin rim periphery to the masses, calcification, expansion of involved sinuses and bone erosion. Two cases of invasive type showed extension beyond the sinuses into the orbit and intracranially simulating a malignant tumour. The findings are similar to those described by previous authors. The differential diagnosis is also discussed. Patel, P.J., Kolawole, T.M., Malabarey, T.M., Hulaitah, A., Hamid, F. & Chakaki, M. (1992). Clinical Radiology 45, 319-321. CT Findings in Paranasal Aspergillosis.
Fungal infection of the paranasal sinuses is an u n c o m m o n disease. Aspergillosis is a fungal disease caused by the aspergillus fungus of the ascomycites group which has a worldwide distribution. Aspergillosis commonly involves the lungs. However, sinus aspergillosis remains a rare condition even though there is a recent increase in the number of isolated cases reported in the literature (Robb, 1986). This disease has been described almost exclusively in Africa, specifically in Sudan. One case has been described from Saudi Arabia (Dawlatly et al., 1988). There are only a few reports of sinus aspergillosis in the literature. The reports of computed tomographic (CT) scan findings are few (Jinkins et al., 1987; Som et al., 1987; Quiney et al., 1988). A retrospective study of aspergillosis of the paranasal sinuses as seen in Riyadh was therefore undertaken to determine the CT scan features of this disease.
presented with a history of sinusitis and headaches. One patient also had exophthalmos and fever. The duration of symptoms before diagnosis varied from 4 months to 2.5 years, with an average, of 13.2 months. Aspergillosis fumigatus was isolated from the paranasal sinuses in all cases. Plain Film Findings The maxillary antra were abnormal in all cases, and the ethmoid sinuses in six cases. The sphenoid and the frontal sinuses were involved in three and two cases respectively. Five cases showed non-homogeneous opacities whilst three showed homogeneous opacities in the involved sinuses. Other findings were calcifications in three cases, erosions of the sinus wall in two cases and expansion of the sinus in one case. CT Findings
M A T E R I A L S AND M E T H O D S We reviewed retrospectively the CT scans of sinuses in eight cases of aspergillosis from three different hospitals in Riyadh. The diagnosis was made in all cases by positive histological examination of the specimens. All the CT examinations were performed on one of three scanners: G E 9800, S o m a t o m II, or Somatom D R H , using a sinus protocol to produce contiguous axial scans, carried out parallel to the inferior orbitomeatal (IOM) plane, from the maxillary alveolus to the superior aspect of the frontal sinuses. The scans were 5 m m (GE 9800) or 4 m m (Somatom 2, Somatom D R H ) thick. Coronal scans were performed 90 ° to the I O M plane using the same slice thickness. Enhanced scans w e r e a l s o carried out after intravenous contrast medium (Conray 420, 50 ml) using the same protocol. RESULTS The patients studied were four males and four females, with ages ranging from 14 years to 39 years (mean age, 28 years). All patients (six Saudis and two Sudanese) Correspondence to: Dr P. J. Patel, Associate Professor, Radiology Department No. 40, King Khalid University Hospital, P.O. Box 2925, Riyadh, 11461, Saudi Arabia.
CT showed calcifications in seven cases, including four cases in which calcification had not been demonstrated on the plain films. More extensive calcifications were seen in each case than demonstrated by plain films. CT demonstrated bony wall erosion in five cases, and in three cases this was more extensive than shown on plain films. The CT pattern shown in two cases was of homogeneous, high attenuation, polypoidal opacities, whilst in six others it was of non-homogeneous, either linear interlacing high density or nodular opacities. One case which produced homogeneous shadowing on plain films turned out to be non-homogeneous on CT. The CT findings are listed in Table 1. DISCUSSION Stammberger et al. (1984) quote Schubert as the first person to described aspergillosis of the nose and paranasal sinuses in 1885. It is the commonest cause of fungal infection of the sinuses. However, only about 115 cases have been described in the English literature, mostly as case reports (McGuirt and Harrill, 1979). It appears that the incidence of a fungal infection in the nose and paranasal sinuses has increased because of the increasing use of antibiotics, steroids, cytotoxic and other chemotherapeutic agents (Robb, 1986). Aspergillosis of
320
CLINICAL RADIOLOGY
Table 1 - S u m m a r y of C T findings in aspergiliosis
Total cases: 8 A Sinuses Maxillary antrum Ethmoid Frontal Sphenoid B C D E F G
Unilateral 3 1 2
Nasal cavity Bone erosion of involved sinuses Expansion of sinuses Intraorbital extension Intracranial extension CT findings of mass: Homogeneous density Non-homogeneous density Average CT density (HU) Enhancement (mild) Rim of lucency Calcification Bone sclerosis
Bilateral 5 5
Total 8 6 2 3
5 5 2 2 2 2 6 764 (range 172-1023 HU) 3 4 7 1
Fig. 2 CT scan shows multiple linear interlacing network of high density with nodules in the ethmoidal sinuses which are expanded.
Fig. 1 Diffuse nodular high density masses involving the maxillary antra and nasal cavity. There is a radiolucent rim peripherally (arrows).
the sinuses is c o m m o n in S u d a n (Milosev et al., 1969), a n d only one case has been reported in a Saudi p a t i e n t (Dawlatly et al., t988). There are two types o f sinus aspergillosis: invasive a n d non-invasive. T h e m a i n difference between the two is o f b o n e destruction which typifies the invasive type. The majority of cases o f the invasive type p r o d u c e orbital or i n t r a c r a n i a l complications. A C T scan is very useful in detecting the b o n e destruction, thus differentiating the two types. O u r study confirms the view o f K o p p et al. (1985) that the maxillary a n t r u m is the most c o m m o n l y involved sinus. However, bilateral i n v o l v e m e n t of the a n t r a was c o m m o n e r in our study t h a n in other studies, where the changes were usually unilateral. The e t h m o i d sinus was the next c o m m o n e s t site, a n d in five out o f six patients the changes were again bilateral. The nasal cavity itself was involved in five cases.
Fig. 3 Invasive aspergillosis: coronal CT scan reveals non-homogeneous opacity in the left antrum extending into the left orbit and left anterior cranial fossa. Note the erosion of medial wall of left orbit and left aspect of the floor of anterior cranial fossa, through which the mass has eroded.
C T findings include slightly e n h a n c i n g masses of soft tissue density filling a sinus cavity a n d separated from the sinus wall by a thin rim of m u c o i d density material which has a lower a t t e n u a t i o n value t h a n the fungal mass (Jinkins et al., 1987). These findings were observed in four
CT FINDINGS IN PARANASAL ASPERGILLOSIS
of our cases (Fig. 1). The most characteristic pattern of multiple, linear interlacing network of high density, described by Som et al. (1987), was present only in two of our cases (Fig. 2). Concentric or polypoidal thickenings of the mucosal lining have also been reported. In a previous report, reference was made to the high attenuation values of the concretions which were found to be about 2000 H U (Kopp et al., 1985). The average CT value in our cases was much lower (about 764 HU). Calcifications were seen in seven out of eight cases (Fig. 2). The calcifications are due to tertiary calcium phosphate (apatite) d@osits within the necrotic area of the mycelium (Kopp et al., 1985). Intracranial manifestations such as granuloma formation, meningitis, meningo-encephalitis, abscesses, vasculitis, aneurysm formation, infarction and haemorrhage have been described in the literature (McGill, 1980; Som et al., 1987; Sowagar and Shadid, 1987). The commonest intracranial complication is granuloma formation. Two of our cases showed granuloma formation in frontal lobes, a direct extension from the sinuses (Fig. 3). There was no other intracranial complication in our series. lntracranial aspergillosis causes bone erosion and soft tissue enhancement which is usually surrounded by a rim of oedema (Jinkins et al., 1987). However, its continuity with the sinus aspergillosis makes the diagnosis straight forward. Extension of aspergillosis into the orbits causing proptosis was the commonest cause of a non-congenital unilateral proptosis in Sudan (Milosev et al., 1969; Kopp et al., 1985). Proptosis was only seen in one of our cases. In general, CT was useful in demonstrating the presence of calcifications, erosions, and extensions into the surrounding area as well as characterizing the type of pattern within the soft tissue densities in the sinuses In a study of 103 cases, the invasive type was associated with a far higher mortality than a non-invasive type - 16 out of 17 deaths occurring in this type (Jahrsdoerfer et al., 1979). Non-invasive aspergillosis of the sinuses is usually treated with amphotericin B, coupled with surgical removal of the infected material. The invasive type usually requires more aggressive treatment with additional drugs such as Ketokonazole, in conjunction with surgical excision of the aspergillosis mass, sinus curettage and drainage. Our two 'invasive' cases were treated successfully in this fashion. The differential diagnosis of sinus aspergillosis includes chronic bacterial sinusitis, malignant neoplasm, benign neoplasm, tuberculosis, osteomyelitis of the maxilla, Wegener's granuloma, rhinoscleroma and mucomycosis, polyps and fibrous dysplasia (Robb, 1986). A number of
321
these conditions are rare, difficult to confirm clinically and difficult to distinguish from aspergillosis radiologically. Polyps are seen as masses of low density with a cascade-like appearance, whereas aspergillosis produces streak-like densities extending from the central area (Som et al., 1987). We have not found these differentiating features to be particularly useful. A rim of low density due to mucoid material, areas of high density, erosion and expansion of the sinuses are features that are more useful in differentiating between aspergillosis and polyps in our experience, as well as others (Som et al., 1987). Radiographic investigations, especially CT, may help in the differential diagnosis of disorders affecting the sinuses but more importantly, CT is useful in delineating the extent of the disease in aspergillosis. Skin tests and serology for aspergillosis precipitins are usually inconclusive (Milosev et al., 1969; Robb, 1986). Hispathological examination of the sinus contents obtained by biopsy is therefore mandatory.
REFERENCES Dawlatly, EE, Anim, JT, Sowayan, S & E1-Hassan, AY (1988). Primary paranasal aspergillus granuloma in Saudi Arabia. Tropical and Geographical Medicine, 40, 247 250. Jahrsdoerfer, RA, Ejercito, VS, Johns, MME, Cantrell, RW & Sydney, JD (1979). Aspergillosis of the nose and paranasal sinuses. American Journal of Otalaryngology, 1, 6- 14. Jinkins, JR, Sigueira, E & Zuheir Al-Kawi, M (1987). Cranial manifestations of aspergillosis. Neuroradiology, 29, 18 L 185. Kopp, W, Fotter, R, Steiner, H, Beaufort, F & Stammberger, H (1985). Aspergillosis of the paranasal sinuses. Radiology, 156, 715 716. McGill, TJ, Simpson, G & Healey, GB (1980). Fulminant aspergillosis of the nose and paranasal sinuses. A new clinical entity. Laryngoscope, 90, 748-754. McGuirt, WF & Harrill, JA (1979). Paranasal sinus aspcrgillosis. Laryngoscope, 89, 1563-1568. Milosev, B, Mahgoub, EI-SA & Hassan, AMM (1969). Primary aspergilloma of the paranasal sinuses in Sudan: a review of seventeen cases. British Journal of Surgery, 56, 132 137. Quiney, RE, Rogers, M J, Davidson, RN & Cheesman, AD (1988). Craniofacial resection for extensive paranasal sinus aspergilloma. Journal qf Laryngology and Otology, 102, 1172 1175. Robb, PJ (1986). Aspergillosis of the paranasal sinuses: a case report and historical perspective. Journal of Laryngology and Otology, 100, 1071-1077. Sore, PM, Sachet, M, Lawson, W &Biller, H 0987). CT appearance distinguishing benign nasal polyps from malignancies. Journal of Computer Assisted Tomography, 11, 129 133. Sowdagar, R & Shadid, H (1987). Invasive aspergillosis of the paranasal sinuses. Emirates Medical Journal, 5, 67 70. Stammberger, H, Jakse, R & Beaufort, F (1984). Aspergillosis of the paranasal sinuses: X-ray diagnosis, histopathology, and clinical aspects. Annals"of Otology, Rhinology and Laryngology, 93, 251 256.
