Advances in Imaging of the Paranasal Sinuses Francis T.K. Ling, MD, FRCSC, and Stilianos E. Kountakis, MD, PhD

Corresponding author Stilianos E. Kountakis, MD, PhD Department of Otolaryngology–Head and Neck Surgery, Medical College of Georgia, 1120 15th Street, Augusta, GA 30912, USA. E-mail: [email protected] Current Allergy and Asthma Reports 2006, 6:502–507 Current Science Inc. ISSN 1529-7322 Copyright © 2006 by Current Science Inc.

Imaging technology has played a significant role in the diagnosis and management of sinonasal disorders. Plain sinus films are almost exclusively replaced by CT in the work-up for inflammatory sinus disease. MRI provides complementary information to CT in cases of sinonasal and skull-base neoplasms. The evolution of endoscopic surgical techniques for the paranasal sinuses and skull base is made possible by the parallel advancement of imaging technologies. Recent advances that are currently in clinical use have included multidetector row CT scanners and computer image–guidance systems for surgery. Three-dimensional CT angiography, image-guided CT–MR fusion, and intraoperative image-guidance are new techniques that are currently being evaluated. As imaging technology continues to advance, so does the capability to treat diseases beyond the sinuses and skull base with minimally invasive, endoscopic approaches.

Introduction During the past 20 years, endoscopic surgery has revolutionized the management of sinonasal diseases. It has provided a more physiologic approach to the surgical management of chronic rhinosinusitis and has reduced patient morbidity compared to the old external techniques such as the Caldwell-Luc procedure. The technique has also evolved to address problems in areas beyond the paranasal sinuses that include the orbit and optic nerve, lacrimal duct system, and skull base. Evolution of these surgical techniques would not have been possible without the parallel advancement of imaging technologies for the paranasal sinuses. Improved imaging technologies have made it possible for clinicians to obtain a detailed representation of the patient’s paranasal sinus anatomy as well

as increased insight into the pathogenesis of certain sinonasal diseases. Improved imaging also aids in decreasing the risks for intraoperative complications during endoscopic surgery, as potential anatomic or disease-causing pitfalls can be identified and anticipated prior to surgery. In this review, we discuss the various imaging modalities used in the evaluation of the paranasal sinuses. We also highlight the various advancements in imaging technology that have been integrated into diagnosis and surgical management of sinonasal diseases and related disorders.

Imaging Modalities Used in Evaluating the Paranasal Sinuses Plain films

In the past, conventional radiographs of the sinuses, which included the Waters, Caldwell, lateral, and submental vertex view, were routinely ordered for the evaluation of rhinosinusitis. They were mainly used to depict the size of the sinuses, septal deviation, and opacification of the maxillary sinuses [1•]. Although it was useful in confirming the presence of acute rhinosinusitis, this imaging modality is limited in evaluating chronic rhinosinusitis and sinonasal neoplasms. Anatomic detail is poor due to the superimposition of overlapping structures, and the accuracy required to diagnose these conditions is lacking [2]. Poor sensitivity in the evaluation of mucosal disease in the maxillary and other paranasal sinuses was noted [3]. In particular, the drainage pathways of the frontal and ethmoid sinuses are poorly visualized. In the pediatric population, plain radiographs were shown to be inaccurate in up to 75% of cases of inflammatory sinonasal disease [1•]. Without the fine anatomic detail required in planning endoscopic sinus surgery, plain films have not been useful for this purpose. For these reasons, plain radiography is obsolete in the investigation and management for the majority of sinonasal disorders.

Conventional polytomography Polytomography was an imaging technology employed 20 to 30 years ago. It provided better anatomic bony detail needed for safer surgery than did plain radiographs. Major drawbacks of this technology, however, were an increased radiation dose, increased acquisition time, and

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poor soft tissue resolution [4]. With the advent of CT, this method of image acquisition is no longer used for the paranasal sinuses.

Computed tomography The introduction of CT of the paranasal sinuses has revolutionized the diagnosis and treatment of sinonasal diseases. CT imaging provides superior resolution of bone and soft tissue compared to polytomography, with shorter image acquisition time and less radiation exposure. It is now considered the gold standard in the primary imaging of inflammatory sinonasal lesions [1•]. The current standard protocol for imaging the paranasal sinuses consists of acquiring direct contiguous sections 3 mm thick in the coronal plane [5]. Administration of intravenous contrast may be required when complications of inflammatory disease such as abscess, thrombosis, and intracranial or intraorbital spread of infection is suspected, or for the evaluation of any benign or malignant tumor [5]. Patients are placed in the prone position to drain fluid away from the ostiomeatal complex (OMC). This serves to reduce false obliteration of the OMC and provide better delineation of the bony anatomy. The main disadvantage of this technique is that patients with limited cervical extension may not tolerate this procedure well. In addition, when dental amalgam fillings are excessive, dental artifacts may obscure the image. For the diagnosis of chronic rhinosinusitis, CT imaging is far superior to conventional radiography as superimposed overlapping structures are removed, and a true tomographic representation can be obtained based on the tissue attenuation of the x-rays [6] for evaluating the health of the paranasal sinuses. Mucoperiosteal thickening, osteitis, sinus obstruction, and opacification can be easily seen. In cases of mucoceles, CT imaging provides the best assessment of bony remodeling, sinus expansion, and dehiscence [3]. CT imaging also remains the study of choice for osseous, chondrogenic, and developmental lesions such as osteoma, osteoblastoma, fibrous dysplasia, ossifying fibroma, and osteogenic and chondrogenic sarcomas [6]. CT imaging of the paranasal sinuses is essential for the preoperative planning of endoscopic sinus surgery. With the high attenuation of x-rays by cortical bone in relation to soft tissue and air, CT imaging provides an accurate assessment of the extent of pneumatization of the paranasal sinuses, facial bones, and bones of the skull base. This provides the “road map” required for safe endoscopic sinus surgery and allows better surgical planning through the analysis of anatomic variants such as Haller cells, Onodi cells, concha bullosa, or paradoxical turbinates [3]. In addition, the following key anatomic structures of the ostiomeatal complex need careful attention: ethmoid infundibulum, uncinate process, perpendicular plate, and basal lamella of middle turbinate, ethmoid bulla, frontal recess, sphenoethmoid

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recess, and fovea ethmoidalis [7••]. Awareness of surgical pitfalls such as dehiscences of the lamina papyracea, optic nerve, and carotid artery may reduce injury to such structures. Cognizance of a low-lying skull base or olfactory groove may reduce the risk for an inadvertent cerebrospinal fluid (CSF) leak. In summary, the major roles of sinus CT are to support clinical diagnosis, to evaluate the nature and extent of disease, and to assess the anatomy required to assist treatment planning [7••]. With the enormous amount of detail and information provided, it is not surprising that CT imaging of the paranasal sinuses can greatly influence surgical decision making [8].

Magnetic resonance imaging The introduction of MRI was a major milestone in radiology, and MRI is in general the best anatomic imaging technology currently available. Although CT scans can provide anatomic detail, they cannot help predict the histologic nature of pathologic processes. CT scanning in essence only measures one property of human tissue: the absorption of x-rays. In contrast, MRI actually evaluates tissue property, as its images depict the location and behavior of nuclei emitting MR signals [6]. This allows assessment of various fluid compositions within the tissues and hence provides much greater soft-tissue contrast, tissue differentiation, and marginal lesion definition. For example, MRI can more readily distinguish scar tissue from surgical material and recurrent tumors than CT scanning [3]. MRI is found to be superior to CT in demonstrating the extent of inflammatory disease and in the characterization of fungal concretions [4]. Other advantages over CT scanning include multiplanar capability, the avoidance of ionizing radiation, and the depiction of physiologic processes such as the nasal cycle and flowrelated phenomena [6]. The main disadvantage with MRI is that cortical bone and air have no signal. Therefore, the fine bony anatomy of the paranasal sinuses is not well depicted on MR sequences. Hence, this study does not provide the best “road map” required for endoscopic sinus surgery. Other disadvantages of this technology include the lengthy scanning time, high expense, and its contraindications to certain conditions such as the presence of pacemakers, cochlear implants, and aneurysmal clips. Although it is not routinely required for inflammatory disorders of the paranasal sinuses, MRI is invaluable in assessing intranasal neoplasms. It is an important diagnostic adjunct to the CT scan. In the setting of unilateral nasal polyps or masses, CT may have difficulty distinguishing between scar tissue, mucocele, meningocele, and encephalocele [3]. The use of MRI is, therefore, an important test in these situations, as it can narrow this differential using coronal T2-weighted images. In cases of encephaloceles, for example, herniation of brain tissue can be readily seen as a high-intensity mass through the

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skull base. This information greatly influences decisions in the management of these lesions. In cases of sinus opacification, MRI is superior to CT in differentiating inflammatory conditions from neoplastic processes [6]. Whereas uniform opacification is seen on CT scan, MRI can easily differentiate between soft tissue and inspissated secretions. On T2-weighted imaging, these entrapped secretions are of high signal, whereas neoplasms are of intermediate signal [3]. When intracranial complications of paranasal sinus disease occur, MRI can better detect an intracranial infection or abnormality not identified on routine CT. MRI can identify the location and extent of pathology with more specificity than CT [9]. For this reason, MRI is considered the gold standard for the diagnosis of any intracranial complication arising from inflammatory sinonasal disease. Aggressive lesions are best imaged using MRI, as it better depicts the degree of spread and invasion. The extent of disease invasion into soft tissue structures is more precisely defined [3]. For example, for intracranial extension of tumors, dural involvement can be distinguished from parenchymal involvement. Perineural spread of intranasal malignancies is better identified on MRI than with CT. MRI is more reliable because it can better evaluate the fat within the skull base foramina, and it can also interrogate the nerves directly to evaluate for enhancement. Common pathways of spread from the paranasal sinuses are from the pterygopalatine fossa into the orbits or along palatine nerves. Because involvement of dura, brain, and orbital contents is better assessed with MRI than with CT, MRI is the preferred modality for staging and follow-up of sinonasal tumors.

coronal or axial views. The sagittal view makes the relationship of these cells more obvious and will allow more effective surgical management. Other benefits include improved image quality. With reduced scan times, extensive motion artifact is reduced because patients are more comfortable. Data can be acquired in the axial plane with the patient supine, and then the data can be reformatted in the coronal plane. This significantly reduces streak artifact from dental amalgam because the data are acquired away from the teeth. Vascular channels are also better demonstrated. As the speed of the scanners improves, it is hoped that this will allow the differentiation between separate arterialand venous-phase images in the future [4]. Despite the shorter acquisition times, the protocol to obtain 1-mm scans with a standard dose multidetector CT requires a radiation dose that is approximately 20% higher than that delivered when acquiring 3-mm thick images [10]. This disadvantage of higher radiation must be weighed with the potential benefits of the imaging study. Alternatively, the dose of radiation can be reduced; however, this may affect image quality. One study examining low-dose multidetector CT scanning for chronic rhinosinusitis found that the dose reduction played a far less important role in discrepancies of detected abnormalities than did the human element of reviewer observation [10]. Their recommendations were that low-dose multidetector CT should be considered as the method of choice for imaging sinonasal cavities in patients with suspected chronic rhinosinusitis because it exposes patients to radiation doses that are no higher than those used for a four-view radiographic examination.

Image-guided surgery

Technologic Advances in Imaging with Current Applications Multidetector row CT

The replacement of the single row x-ray detectors present in single-slice CT scanners with multiple rows of detectors in multichannel helical CT scanners is an important advance in sinus imaging [3]. This technology allowed the registration of multiple channels of data within one rotation of the x-ray tube, which ultimately results in much thinner slices obtained in shorter periods of time [4]. The entirety of the paranasal sinuses is imaged in a few seconds, with the possibility of acquired images with a thickness of less than half a millimeter. With thinner slices, smooth, reformatted images in any desired plane can be constructed. This provides CT technology with the multiplanar advantage seen with MRI. The reconstruction of the sagittal plane can provide potential improvement for surgical planning, especially surgery involving the frontal recess. The highly variable anatomy of the agger nasi, frontal cells, and ethmoid air cells within the frontal recess is not well depicted on

With the potential for serious complications to the orbit and skull base in endoscopic sinus surgery, technologies have evolved to potentially reduce these complications and advance the limits of surgical dissection. Image-guidance technology provides real-time localization of surgical instruments within the operative field in relation to a preoperative CT or MR image. Image guidance in surgery is used to enhance anatomic localization, with the goals of improving safety, allowing for more complete surgical dissections, and potentially improving clinical outcomes. Current image-guidance systems employ one of two types of tracking methods: electromagnetic or optical. Electromagnetic tracking systems make use of a radiofrequency transmitter located in a specialized patient headset worn by the patient during image acquisition and during surgery. The receiver is located in the tracking instrument; its position alters the electromagnetic field generated by the transmitter and provides the data necessary to calculate tip position. Advantages of this system are autoregistration and compensation for any head movement during surgery [11]. Disadvantages include signal distortion of the electromagnetic field by large metal objects (eg, instrument

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tables, anesthesia equipment) and the logistics required in implementing the specialized headset. Optical tracking systems use an infrared camera that actively or passively tracks optical markers on the instrument in relation to a reference headset worn by the patient during surgery. Active optical markers are infrared-emitting diodes powered by cables or individual battery packs, and passive markers are highly reflective spheres (glions) that reflect infrared signals from an emitter in the camera array [12••]. For the camera to track accurately, it must have a direct line of sight to these markers on the reference frame and the tracking instrument. The main advantage of this system is the obviation of a headset during preoperative imaging, and the disadvantages are line-of-sight issues caused by improper instrument positioning or interference by operating room equipment or personnel [13]. Preoperative images are obtained from high-resolution (~1 mm) axial CT scans. From these scans, coronal and sagittal images are reconstructed and are displayed on the computer console along with the axial images. Localization of the tracking instrument tip can then be seen on all three views. An optional fourth view can be used for the surgical view from the endoscope. Several authors have studied the accuracy of image-guidance systems, and it has been shown to be within the 2-mm acceptable standard [14–17]. Although not a standard of care, image guidance has been indicated for revision sinus surgery; extensive nasal polyps; complicated frontal, posterior ethmoidal, and sphenoid sinus disease; CSF rhinorrhea and skull-base defects; benign and malignant sinonasal neoplasms; and disease in proximity to critical structures, such as the orbit, optic nerve, or carotid artery. It is useful in assisting with preoperative planning, as the surgeon can conceptualize the approach to the paranasal sinus, anterior skull base, or petrous/clival area [18•]. Although image guidance can increase a surgeon’s confidence through verification of anatomic landmarks, it cannot replace a surgeon’s experience, judgment, and technique. Long-term studies have yet to prove improved safety, reduced complications, and better outcomes using this technology [19].

Technologic Advances in Imaging with Potential Future Applications Three-dimensional CT angiography

Three-dimensional CT angiography (3DCTA) provides three-dimensional representation of the internal carotid artery (ICA) in relationship to the skull base. Leong et al. [20•] reported the use of 3DCTA during intraoperative surgical navigation in a series of sinonasal and skullbase surgeries that included neoplasm (11 cases), CSF leak (3 cases), fibro-osseous lesion (2 cases), and mucocele (2 cases). They found that the images facilitated the definition of the anatomic relationships between the

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ICA and skull-base lesion, and thus further enhanced the surgeon’s ability to appreciate 3D relationships during surgery. As endoscopic management of skull base tumors increases, this technology may become increasingly important for the extirpation of tumors intimately involved with the ICA.

Image-guided CT–MR fusion As described earlier, CT and MRI have numerous advantages and disadvantages, and the limitations of each modality alone can be overcome by combining the two. Merging the CT images with MR images affords improved visualization of a lesion using both the soft tissue and vascular details of MR imaging and the bony detail afforded by CT (Figs. 1 and 2). Chiu et al. [18•] have used this technology in the resection of an angiofibroma and a petrous apex dermoid. They found that by being able to combine the best of both imaging modalities, dissection around the ICA, cavernous sinus, and dura was greatly facilitated. CT-MR fusion for computer-guided surgery may, therefore, be helpful in further advancing endoscopic tumor surgery.

Intraoperative Imaging in Otolaryngology Although image-guided surgery provides real-time localization of surgical instruments to a preoperative image, surgical changes that occur during surgery are not captured. As the surgery progresses, potential changes to the anatomy may occur, which would be falsely represented on the image-guidance system. An example of this occurs during endoscopic tumor removal at the skull base. As tumor is being removed, normal tissue such as brain will be displaced to fill the area of the debulked tumor. Reliance on the imageguidance system in this case may produce disastrous results if the surgeon is not cognizant of this. Because of these potential pitfalls, “situation-adapted imaging” has been devised using intraoperative imaging to deliver updated images to the surgeon that reflect the changes in anatomy during the procedure. Advances in CT and MRI technology have reduced scanner sizes such that it is now possible to obtain CT and MR images in the operative suite. One study looked at intraoperative CT for several otolaryngologic procedures such as endoscopic surgery for maxillary and ethmoidal rhinosinusitis, tumor resections in the hypopharynx, and verification of electrode position in cochlear implantation using the Tomoscan M (Philips, Eindhoven, The Netherlands) [21]. Twelve procedures on the paranasal sinuses were evaluated, and it was found that intraoperative CT was beneficial in identifying the skull base and other bony structures; however, several drawbacks were noted. One drawback was that individual ethmoidal sinuses could not be evaluated because of blood artifacts. In the case of revision sur-

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Figure 1. Use of CT-MR fusion during computer-aided endoscopic repair of large sphenoid encephalocele. Left panels, Conventional CT images. Upper right panel, Fused CT–MR image. The sagittal image shows the encephalocele filling much of the sphenoid sinus. (From Leong et al. [24], with permission.)

geries, no distinction could be made between scar tissue and polyps. Additional problems included increased time required for patient positioning and data acquisition and the space required for the CT scanner. Intraoperative MRI has been plagued with similar drawbacks. A vertically open MRI has higher costs and necessitates the use of nonmagnetic instruments [21]. Still in the preclinical phase, an imaging system that combines low-dose fluoroscopy and fully 3D CT (mobile isocentric C-arm, Power Mobil, Siemens Medical Systems, Erlangen, Germany) has been used to assist the surgical approach to the frontal recess in six cadavers [22]. This system is portable and generated intraoperative, volumetric CT images rapidly with acceptably low radiation exposure. It provided near–real-time CT guidance without a registration process. Investigators found that use of this system increased surgical confidence in accessing the frontal recess, resolved ambiguities with anatomical variations, and was valuable in teaching and preoperative planning. The advantages and benefits of such a system in a clinical setting are yet to be determined. Currently, the disadvantages of using intraoperative imaging, such as higher costs, repeated exposure to radiation, and prolonged anesthesia, far outweigh the potential benefits. Therefore, using this technology for standard sinus and skull-base surgery is not currently recommended, because no substantial advantage with regard to postoperative results is seen [23]. This recommendation, however, may change as less cumbersome imaging machines with faster data acquisition times are developed.

Figure 2. CT-MR fusion used during image-guided endoscopic frontal sinusotomy for a frontal mucocele that had formed after frontal sinus obliteration. Top, lower left panels, Fused CT–MR images. Several loculations within the mucocele, as well as bony skull base erosion, are seen on the sagittal CT-MR fusion image. Navigation with the CT-MR fusion images was reported to be critical for complete drainage of each mucocele pocket. (From Leong et al. [24], with permission.)

Future Directions As imaging technology continues to advance, additional capabilities of three-dimensional sinus imaging may evolve, such as fly-through imaging that mimics the point of view of an endoscopist. This may further enhance surgical planning, as the three-dimensional aspect of the surgical field would be better appreciated. It may be possible to perform “virtual surgeries” using this information. This may enable a surgeon to assess the feasibility and/or outcome of the surgery before operating on the patient. Such an application would be invaluable in resident education and training.

Conclusions The advances in imaging of the paranasal sinuses have led to many advances in the treatment of sinonasal and skull-base diseases. Information obtained from CT and MR imaging lays out the essential road map to safely navigate the complex anatomy of the paranasal sinuses and skull base. Improved systems such as the multi-detector CT provide better images with shorter acquisition times over conventional, single-detector CT. The use of image-guidance systems can help the surgeon navigate within a complicated surgical field. Enhancements to the current image-guidance systems such as 3DCTA or CT-MR fusion further aid the surgeon when operating around potentially dangerous structures such as the internal carotid artery or the cavernous sinus. Although

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still in their infancy, intraoperative imaging and computer guidance can provide information on surgical changes occurring in real time. This may prove beneficial as we move beyond the skull base, where the position of various anatomic structures may shift during surgical removal of various disease processes. As imaging technology continues to advance, so does the capability to treat diseases beyond the sinuses and skull base with minimally invasive, endoscopic approaches.

References and Recommended Reading Papers of particular interest, published recently, have been highlighted as: • Of importance

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