Detection of sinus-induced orbital mycosis with standardized orbital ultrasonography: A case report.

Abstract

Fungal involvement of the paranasal sinuses is frequently observed in the immunocompromised host, and it can become life-threatening if it is not diagnosed. Although the definitive diagnosis is made by tissue biopsy and culture, imaging is of vital importance in the clinical workup and in planning treatment. We present a case of fulminant ethmoidal sinusitis caused by Aspergillus flavus with orbital involvement in an immunocompromised patient. Standard computed tomography of the paranasal sinuses was complemented by the use of standardized orbital ultrasonography, which was able to identify the intraorbital extension. We discuss the role of standardized orbital ultrasonography as a complementary imaging modality in the diagnosis of fungal sinusitis and in the assessment of local extension. To the best of our knowledge, the role of SOU in diagnosing an orbital extension of a fungal infection of the paranasal sinuses has not been previously discussed in the literature.

Introduction

Fungal involvement of the paranasal sinuses has been reported in as many as 42% of patients who seek treatment for sinus complaints. [1] Fungal sinusitis is classified as either acute fulminant, indolent, mycetomatous, or allergic. [2] Twenty-four different fungal genera have been isolated in sinus disease; Aspergillus is the most common. [3] Fungal involvement of the paranasal sinuses requires some type of impairment of local or systemic host mechanisms, which facilitates the conversion of these organisms from saprophytic to pathogenic. Therefore, it is not surprising that these infections are encountered in chronic bacterial sinusitis, in the presence of immunocompromised states such as malignancy or diabetes mellitus, or after the administration of cancer chemotherapy. The definitive diagnosis is made by tissue biopsy and culture, but imaging is of vital importance in the clinical workup and in planning treatment.

In this article, we describe the case of an immunocompromised patient who had fulminant ethmoidal sinusitis with orbital involvement that was caused by Aspergillus flavus. We also discuss the advantages and limitations of the different imaging modalities that are available for the management of fungal sinusitis.

Case report

A 70-year-old man was referred to us from a regional community hospital for evaluation of generalized sepsis, proptosis, and ophthalmoplegia in the left eye. His medical history was significant for insulin-dependent diabetes, arterial hypertension, and left hemiparesis as a result of a stroke 2 years earlier. Two weeks prior to his referral, the patient had experienced a myocardial infarction, which was complicated by pneumonia and salmonella gastroenteritis. His complications were initially treated with chloramphenicol (4 g/day) and later with ciprofloxacin (800 mg/day) and ceftriaxone (2 g/day), but his clinical response was poor. Proptosis was first noticed 10 days prior to his referral, and within 3 days, complete ophthalmoplegia and an afferent pupillary defect appeared in his left eye.

On admission to our department, the patient was afebrile. Nasal rigid endoscopy revealed the presence of black crusts that covered the swollen mucosal lining of the left middle turbinate. Perfuse, foul-smelling pus could be seen oozing from the left middle meatus. Periorbital swelling and erythema of the left infraorbital area and cheek were also observed. Complete ophthalmoplegia was noted in the left eye. Papilledema was ruled out by an ophthalmologic examination.

Laboratory tests revealed a white blood count of 6,500/[mm.sup.3] and a normal differential. His hemoglobin level was 9.1 g/dl, his hematocrit was 28%, and his albumin concentration was 2.0 g/dl. His other laboratory test results were within normal limits, and the rest of his physical head and neck examination was normal, as well. Tissue biopsies and cultures were collected from the left middle meatus. On the basis of the clinical picture, we decided to start antimicrobial and antifungal chemotherapy without waiting for the results of cultures and histopathology. Intravenous amphotericin B (35 mg/day) and imipenem (2 g/day) were administered.

Axial and coronal computed tomography (CT) of the paranasal sinuses revealed clouding of the left ethmoid air cells; the rest of the paranasal sinuses were normal (figure 1). A marked proptosis and a mass were seen in the left orbital apex area, and the medial aspect of the left orbit was clouded. The mass had applied pressure on the globe and on the medial rectus muscle, which was thickened. It was not possible to determine on CT whether the patient had an orbital abscess or orbital cellulitis.

B-mode standardized orbital ultrasonography (SOU) demonstrated a large echolucent space that was encompassed by an echodense area, representing an abscess between the medial rectus muscle and the defective lamina papyracea (figure 2). An A-mode SOU was not performed because of the patient's lack of cooperation. In view of the rapid deterioration of the patient's general condition, it was decided to surgically drain his orbital abscess. Because he was a high-risk cardiac patient, the procedure was performed under local anesthesia. Through a modified medial canthal ligament approach, a left radical ethmoidectomy and drainage of the orbital abscess were performed. A large amount of gray-black, polypoid material was evacuated. Tissue cultures and histopathology detected the presence of A flavus. Acinetobacter isolates were also cultured from this material.

On the second postoperative day, the patient experienced severe hematemesis, which was controlled by lavage with iced saline through a nasogastric tube. Gastroscopy demonstrated an ulcerated tumor located in the large curvature of the stomach. Tissue biopsy of this lesion identified a moderately well-differentiated adenocarcinoma. The presence of ascites and a suspicion of a peritoneal metastasis (as suggested by abdominal ultrasound) made the tumor unresectable.

Postoperatively, the patient was conscious and afebrile. His proptosis had decreased, but there was no change in his ophthalmoplegia. Repeated ophthalmologic consultations continued to rule out papilledema. Postoperative axial and coronal CT showed aeration of the ethmoidal labyrinth and the significant decrease in proptosis (figure 3).

The patient continued on amphotericin B (70 mg every other day) for 4 more weeks; imipenem was discontinued after 2 weeks. Ten days after the surgical drainage, the patient was transferred back to the regional hospital for continued antifungal chemotherapy and supportive care. Four weeks after his admission there, he died of hemorrhagic shock as a result of gastric hemorrhage.

Discussion

Orbital involvement of a fungal infection is usually the result of a propagation of the infection from the paranasal sinuses, either through the lamina papyracea or through congenital dehiscences in the bone. Less often, it is a result of local thrombophlebitis and septic thromboemboli via the valveless venous channels.

Chandler et al defined the five stages of orbital complications of sinusitis as inflammatory edema, orbital cellulitis, subperiosteal abscess, orbital abscess, and cavernous sinus thrombosis. [4]

Fungal sinusitis is classified into four main types: acute fulminant, indolent, mycetomatous, and allergic. [2]

Acute fulminant. The acute fulminant form is seen in immunocompromised hosts, and it is characterized by infection with Mucor or Aspergillus strains. This form is tissue-invasive, and treatment requires radical surgical debridement supplemented by long-term antifungal chemotherapy.

Indolent. The indolent form is chronic and primarily noninvasive, and it occurs in immunocompetent hosts. The causative organisms are Aspergillus and dematiaceous fungi. There is an invasive variant of indolent fungal sinusitis, and it can be marked by orbital and intracranial extension. Wide debridement is usually sufficient unless there is orbital or intracranial extension; in that case, antifungal chemotherapy must be administered.

Mycetomatous. Mycetomas--fungal balls that are also caused by aspergillosis--also appear in immunocompetent patients. But unlike the other forms, mycetomatous fungal sinusitis involves only one of the sinuses. Cure is achieved by debridement and aeration of the involved sinus.

Allergic. The allergic form is typically seen in young atopic patients with positive skin tests, serum eosinophilia, and elevated levels of total serum IgA and specific IgG and IgE. Multiple sinuses are usually involved, and bony erosion of the sinus walls is present in as many as 50% of patients. Treatment includes debridement and steroid administration. On those rare occasions when orbital or intracranial invasion occurs, antifungal chemotherapy can be added.

Mucormycosis is uniquely characterized by a fulminant course and is associated with immunocompromising conditions such as diabetes, hematologic malignancies, adrenal suppression, and acquired immunodeficiency syndrome. [2] Cranial nerve deficits--including blindness, ophthalmoplegia, and proptosis--are common, and affected patients are often in a state of coma or stupor. [5] Other types of fungus can involve the paranasal sinuses, but they appear to be very rare.

The differential diagnosis of mycotic nasal infections include Wegener's granulomatosis, tuberculosis, syphius, sarcoidosis, malignant lymphoma, plasmacytoma, rhinoscieroma, and inflammatory pseudotumor. [2]

Radiographically, neither plain films, CT, nor magnetic resonance imaging (MRI) can accurately distinguish between bacterial and fungal involvement of the orbit.

X-rays. Plain films of the paranasal sinuses in fungal infections might show a clouding of the paranasal sinuses without air-fluid levels or foci of increased attenuation. [6,7] These attenuations are attributable to deposits of calcium phosphate, calcium sulfate, and zinc oxide and are not specific to fungal disease. Fungal involvement of the orbit is not detectable on plain films. [7]

Computed tomography. Axial and coronal CT has become a most valuable tool in the diagnosis of paranasal pathology. High-resolution CT is most useful in evaluating the orbital contents and adjoining structures. The bone window can outline bone defects that either predispose to or are the result of the inflammatory process. Inflammation of the orbit is well demonstrated by an additional soft-tissue mass, thickening of the extraocular muscles, proptosis, and a lateral displacement of the globe and the medial rectus muscle. [8,9]

Reports in the literature regarding CT imaging of orbital aspergillosis are scarce. Zinreich et al compared the accuracy of CT against tissue histopathology in diagnosing fungal sinusitis. [9] Almost all of their patients were diagnosed with Aspergillus strains. The characteristic CT finding in 25 cases of culture-positive fungal sinusitis was a hyperattenuation of the soft tissue of the involved sinus (mean value: 122 Hounsfield units). This hyperattenuation was thought to be the result of calcium deposits, and it appeared in decreasing order in the maxillary, ethmoid, sphenoid, and frontal sinuses. The accuracy of CT was 76%; false-negative and false-positive values were 12% each.

Heier et al reported the results of paranasal and orbital CT in four young immunocompetent patients who had proptosis caused by Aspergillus and other fungi. [10] Their findings included a soft-tissue mass that involved the paranasal sinuses and the orbit, with bone erosion of the medial orbital wall. However, bone erosion is not a specific finding in aspergillosis of the paranasal sinuses; it can also be seen in tumors and even in hypertrophic sinusitis. [11] Aspergillosis sinusitis is also characterized by large amount of low-density mucus. [12]

In general, CT is useful in demonstrating the full extent of fungal sinusitis. Intraorbital masses and bone erosion are nonspecific findings. On the other hand, calcifications inside the soft tissue are common in this condition and uncommon in bacterial sinusitis.

In our patient, CT was not useful in detecting calcifications, bony erosion, and areas of low density within the sinuses. It also failed to identify that the clouding in the medial aspect of the orbit was an abscess that extended from the ethmoid sinuses.

Magnetic resonance imaging. MRI is an excellent modality for demonstrating soft tissues. Nevertheless, only a few reports mention its use in the diagnosis of orbital infections. Zinreich et al reported that MRI in six cases of Aspergillus mycetoma showed isodense or decreased signal intensities on T1-weighted images, which were similar to the kinds of images that are seen in patients with bacterial sinusitis, polyps, and carcinomas. [9] They also reported that a particularly low signal was seen on T2-weighted imaging and that it was similar to the signal produced by air. This finding can best be explained by the fact that fungal infections tend to cause dry secretions; these lesions have a low water content and high iron and magnesium contents. [13] Because such a finding on T2-weighted MRI might be indistinguishable from air, it can cause confusion when it is interpreted by itself. [13] We did not order an MRI for our patient because our institution did not have this equipment at the time.

Standardized orbital ultrasonography. The global, cyst-like structure of the orbit is very amenable to SOU imaging. The sound waves travel through the orbital tissues at different velocities, and they are reflected back as echoes of different strengths. Scanning performed with transducers in the range of 10 to 100 MHz allows for a high resolution of the orbital structures; the high resolution is made possible by the very short wave lengths ([sim]0.2 mm). [14]

One-dimensional A-mode imaging and two-dimensional B-mode imaging are the most common ultrasonographic modalities. Doppler echoes can also be used to detect blood flow. Three-dimensional reconstruction by ultrasonography is a more advanced and accurate method of assessing tumor size and hemorrhages. [14] Structures such as the different parts of the globe, periorbital fat, extraocular muscles, the optic nerve, and tumors can be easily differentiated by SOU. SOU can be used as a supplement to both physical findings and other imaging studies. Like any other method of ultrasonographic imaging, SOU is noninvasive, inexpensive, readily available, and produces no ionizing radiation, so it can be performed as a bedside procedure. Because SOU can also be repeated at short intervals, it can be used to monitor both the development and resolution of orbital infections. Its main limitations are in defining abscesses of the posterior aspect of the orbit and in demonstrating paranasal sinus pathology. Therefore, SOU shoul d be used only in conjunction with, not as a replacement for, other imaging modalities.

SOU can be useful in differentiating between orbital cellulitis and subperiosteal abscess secondary to acute ethmoiditis in children. [10,15-18] Subperiosteal abscess has been identified on B-mode imaging as an echolucent space between the globe and the medial or superior orbital wall that is surrounded by an echodense area of periorbita and the bony lamina papyracea. Sometimes a defect through the lamina papyracea is recognized as a discontinuity in this echodense area. On A-mode imaging, capsular peaks of high reflectivity lining an area of low reflectivity represent the capsule and content of the abscess.

Orbital cellulitis appears on B-mode imaging as an echodense mass between the globe and the lamina papyracea. The echodensity is the result of the high water content of the inflamed periorbital fat.

SOU is not a useful tool for evaluating the ethmoid sinuses because of the bony septa between the air spaces. In a previous publication, we reported that SOU is useful in differentiating between orbital cellulitis and subperiosteal abscess in seven children who had sinus-induced orbital infections. [8] In four of these patients, CT showed a nonspecific clouding in the medial part of the orbit; SOU identified two of these as subperiosteal abscesses and two as orbital cellulitis. Accordingly, the patients with subperiosteal abscess were successfully drained surgically, and the patients with orbital cellulitis recovered with parenteral antibiotic therapy.

The patient we describe in this article had undergone repeated CT and SOU. CT determined that the fungal disease extended to the orbital apex and demonstrated the involvement of the ethmoid sinuses. CT also demonstrated the thickening of the medial rectus muscle, a finding that might be explained by the patient's ophthalmoplegia and proptosis. Based on the clinical examination and CT, the orbital involvement could have been a tumor or orbital cellulitis secondary to the nasal aspergillosis. CT could not determine whether the lamina papyracea on the left side was intact or dehiscent or whether or not there was a direct intraorbital invasion by the fungal infection. SOU was able to distinguish between a fungal infection limited to the ethmoid sinus with secondary orbital cellulitis and a direct involvement of the orbit by a fungal abscess. The distinction was essential because an orbital abscess warrants surgical drainage, while orbital cellulitis can be treated with antimicrobial and antifungal chemotherapy a lone.

We also found SOU to be useful when it was compared with CT findings on the medial aspect of the orbit. The comparison was able to prove the lack of integrity of the bony lamina papyracea. This finding strengthened the diagnosis of a direct fungal spread from the infected ethmoid sinuses rather than orbital cellulitis.

As for treatment, we performed an external ethmoidectomy under local anesthesia in light of our patient's high risk for general surgery. Today, functional endoscopic sinus surgery (FESS) is an acceptable approach to ethmoid sinusitis with an orbital abscess. We did not use FESS at the time because this type of surgery was not yet available at our institution.

We conclude that when an orbital extension of a fungal sinus infection is suspected, SOU can be very useful in diagnosis and evaluation. To the best of our knowledge, the role of SOU in diagnosing an orbital extension of a fungal infection of the paranasal sinuses has not been previously discussed in the literature.

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