Overview Transsphenoidal surgery (TSS) for pituitary tumors and other lesions of the anterior skull base has been in practice for over one hundred years. The advent of technological advancements in imaging combined with improvement in surgical skills has seen a marked evolution in transsphenoidal approaches. We describe the history of neuro-navigation and intraoperative imaging for TSS, from lateral radiographs and pneumoencephalograms to intra-operative MRI (iMRI) and electromagnetic navigation systems (EMS). 

The Evolution of Intraoperative Imaging and Neuro-Navigation in Transsphenoidal Surgery

Mark J. Winder, MD^1,2 ∙ Justin Spooler, MD^2,3 ∙ Marc R. Mayberg, MD²

Contact: Marc Mayberg, MD. E-mail This e-mail address is being protected from spambots. You need JavaScript enabled to view it . 

Citation: Winder MJ, Spooler A, Mayberg MR. The evolution of intraoperative imaging and neuro-navigation in transsphenoidal surgery. J Surg Radiol. 2011 Jan 1;2(1). Download PDF J Surg Rad January 2011 A04.pdf 7052 Kb Received: August 25, 2010; Accepted: September 22, 2010; Published: September 23, 2010 Copyright: © 2010 Surgisphere Corporation. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Contents - Introduction - History of Neuro-Navigation - Intra-Operative Fluoroscopy - CT Based Frameless Stereotactic Guidance - Intra-Operative MRI - Electromagnetic Navigation Systems - Conclusion - References

Introduction

Transsphenoidal surgery (TSS) has been widely used for surgical treatment of lesions related to the sellar and parasellar region. Recent advances in technology have enabled the application of this approach to a broader scope of lesions affecting the anterior skull base. The development of TSS has benefited from the utilization of high-resolution three-dimensional images incorporated into navigation systems providing excellent detail of both bony and soft tissue anatomy, neural and vascular structures. This has enabled operative morbidity to be significantly reduced whilst improving clinical outcomes. The origins of intra-operative imaging and neuro-navigation for TSS date to the early twentieth century, but have significantly progressed in recent years due to technological advances in frameless stereotactic navigation and portable intra-operative computed tomography (iCT) and magnetic resonance imaging (iMRI).

History of Neuro-Navigation

TSS was first attempted over one hundred years ago by Herman Schoffler in 19079, 16, 18, 20, 30 and was subtly modified by von Eiselsberg and Hochenegg.20 In 1909, Kocher performed the approach with a submucosal resection of the septum. The following year, Hirsch described the endonasal trans-septal TSS, which led to Halstead’s description of the sublabial approach in 1909.9, 16, 18, 20 Cushing began utilizing the approach for pituitary tumors in 1909 performing over 300 procedures based on Schoffler’s initial description.20, 30 Unfortunately, mixed results combined with advocates for trans-cranial surgery, including Cushing, subsequently led the TSS approach to be largely abandoned until the late 1950’s. Ironically it was the pupils of Cushing, who reignited the interest in TSS. A key factor in the revitalization of TSS was the advent of intra-operative imaging and navigation using intra-operative fluoroscopy.4, 16, 20, 30 Norman Dott, who was trained by Cushing, continued practicing the TSS in Edinburgh, whilst Hirsch, having immigrated to Boston, attempted to preserve the endonasal TSS with the help of Hamlin.9, 16, 30 The persistence of Dott to maintain the TSS along with his development of a lighted speculum retractor improved the operation significantly. He introduced the notion to Guiot of France, who subsequently performed over 1000 cases using the TSS approach, along with the use of intraoperative radiofluoroscopy to help define the sellar anatomy.9, 16, 20, 30 Although the surgical approaches of the TSS were relatively well formulated, the approach was hampered by illumination and subsequent visualization. Jules Hardy of Montreal, having been exposed to the approach as a fellow of Guiot, continued using fluoroscopy but also added pre-operative angiography and intra-operative air encephalography. In 1967 Hardy first introduced the operating microscope to high resolution TSS, allowing stereoscopic visualization in conjunction with intra-operative fluoroscopy.4, 9, 13, 30 This laid the cornerstone foundation for the development of modern TSS.

Intra-Operative Fluoroscopy

The lateral radiograph has been a standard in TSS since its inception by Guiot and Hardy, and for the past 40 years has been used to augment visualization of the sella turcica as well as helping outline tumor morphology in a sagittal plane (Figure 1). Unfortunately lateral fluoroscopy has several limitations; firstly, it provides only two-dimensional information (anterior-posterior and rostral-caudal) with an absence of critical information regarding midline and right-left lateral anatomical relationships. Secondly, soft tissue is poorly delineated and prior surgery or bony destruction by tumor may limit accurate identification of location. Thirdly, accuracy is dependent upon a “true” lateral projection and movement of the patient head requires repositioning of the fluoroscope. Lastly, the patient, surgeon and operating room personnel are exposed to ionizing radiation, often necessitating the use of cumbersome lead aprons throughout the case.

Figure 1. Lateral skull fluoroscopy as utilized for trans-sphenoidal surgery. Note the absence of soft tissue detail and right-left-midline orientation for fluoroscopic navigation.

Despite these limitations, intra-operative fluoroscopy has been able to offer some degree of operative navigation, which has proven useful. More recently, Jane et al. described TSS using a stereotactic navigation system based upon lateral fluoroscopy, enabling a reference for intra-operative surgical instruments. This fluoroscopic frameless stereotaxy, despite its limitations, confirms its utility.14 The advent of CT and subsequent CT guided stereotaxy for cranial surgery has expanded the viable options in the management of TSS.

CT Based Frameless Stereotactic Guidance

The development of systems for frameless stereotaxy represented a significant advance in intra-operative navigation. The initial prototype for a stereotactic frame was developed by Sir Victor Horsley in 1908, but was only used in experimental studies.7 Following Walter Dandy’s invention of ventriculography as a tool for navigation, the first human stereotactic operation, a percutaneous trigeminal rhizotomy, was performed by Kirschner in 1933. Spiegel and Wycis were the first to introduce a three dimensional stereotactic tool termed the “stereoencephalatome” in 1947, using it perform a thalamotomy. In 1949, Lars Leksell devised his own arc-centered, fixed skull frame stereotactic device which employed polar coordinates, which later became used for radiosurgery. Over the following 15 years several other systems were developed leading to the development of a widely used stereotactic frame by Todd and Wells. This paved the way, with the advent of CT, for the Brown-Roberts-Wells (BRW) stereotactic system, developed in 1979 and still used throughout the world, which allowed stereotactic navigation incorporated with CT data.

Figure 2. Fiducial registration using CT images for frameless stereotactic navigation. Adhesive fiducial markers are attached to the scalp prior to CT scan, then used as reference points for registration to the frameless navigation system.

The next major progression for neuro-navigation was the move from frame-based to frameless stereotaxy. Roberts and colleagues are credited with developing the first frameless neuro-navigation employing a sonic digitizer, correlating target points with either CT or MRI.44 The systems subsequently progressed from stereotactic arm-based systems to frameless, armless navigation utilizing ultrasound, providing intra-operative three dimensional localization.7, 45-47 In 1993, the first report of neuro-navigation employing infrared optical measurements was presented,48 and has since evolved in both accuracy and usability. The introduction of the multislice CT scanner augmented by the evolution of navigation systems allowed three dimensional information to be accessed intra-operatively. The stereotactic navigation systems are based on pre-operative imaging with localization dependent upon patient-positioned fiducial markers, which are then registered, or calibrated with the specific reference system at the time of surgery (Figure 2). The software algorithms are able to translate three dimensional special points based on the pre-loaded imaging referenced directly from a fixed reference point, either on or near the patient. A useful option in navigation has been the development of surface matched registration, which obviates the need for fiducials or reference markers to be directly attached to the patient. In these cases the reference frame is placed separate to the patient and a navigation reference probe is used to trace the surface of the patient’s face and is correlated with a three dimensional model created on the pre-operative imaging (Figure 3). This method of registration has become feasible due to the three dimensional image quality that is now attainable with current radiology and the computer software systems.

Figure 3. Surface Matched Registration using CT images. The preoperative CT scan without fiducials is reconstructed with a 3-dimensional representation of the scalp and facial features. These are traced and the navigation system computes registration according to surface matching algorithms.

CT-based frameless stereotactic navigation has been routinely used in cranial and spinal neurosurgical procedures for over 25 years and has been successfully applied to TSS.26 Early experiences with frameless stereotactic systems for TSS have been described, utilizing ACUSTAR, Brainlab, Stealth Station systems and Instatrak.6, 49, 50 Elias et al reported on their experience in 37 patients undergoing TSS, noting improvements in intra-operative localization and trajectory planning with minimal additional OR time, or cost.6 In a separate series of 176 patients, Jagannathan et al. compared the use of MRI or CT based frameless stereotactic navigation to fluoroscopy in patients undergoing TSS.51 In their series, CT and MR navigation provided a significant advantage over fluoroscopy, particularly in cases of recurrent tumor where traditional landmarks could not be utilized. The benefits of CT based navigation include low cost, short acquisition time, and excellent detail of sinus and bony anatomy. Conversely, CT requires exposure to ionizing radiation, and is poor at demonstrating soft tissues and critical neurovascular structures.

The use of preoperative MRI scans in conjunction with optical based navigation provides excellent detail of soft tissue and neurovascular structures, and allows for accurate intra-operative localization. Multiple reports describe the use of this modality in TSS.22, 27, 37, 51 Registration of the system may be rapidly accomplished using either implanted fiducial markers or surface registration. Shamir et al evaluated the accuracy of surface based registration at serial depths from the facial surface in 12 patients undergoing cranial surgery with intra-operative navigation. They found the average error following registration on the surface to be less than 1mm, while at increasing depths this error increased to a maximum of 4.5 mm at 150 mm from the surface.52 Navigation using MRI is inadequate for delineating bony anatomy and requires longer acquisition times with increased cost compared to CT. Optical tracking systems may also interfere with the positioning of the operating microscope or surgical instruments, particularly in transsphenoidal procedures.9, 12, 13, 20, 22

While neuro-navigation utilizing preoperative CT or MRI is useful, the concept of intra-operative scanning was considered by many to represent the gold standard, providing real time navigation and assessment of tumor resection (Figure 4a,b). Intra-operative CT scanning was first introduced by Shalit et al. in 1979, with several reports to follow in the 1980’s.8, 26, 36, 53, 54 More recently Uhl et al reported their experience using a multislice intra-operative CT scanner including 45 patients undergoing pituitary tumor surgery. Out of the 45 patients they noted 5 with accessible residual tumor identified on the intra-operative scan.38, 42 Although there is some evidence to suggest intra-operative imaging using CT improves surgical outcome, there is no data comparing clinical results to Fluoroscopy or MRI.

Figure 4 (facing page). A. Intra-operative CT scanner (top right). This portable device (Ceretom®; NeuroLogica, Danvers, MA.) has a gantry which can accommodate the head and upper cervical spine. B. Illustration of intraoperative CT scan (bottom right). A sterile cover is placed over the head during the image acquisition.

Intra-Operative MRI

The technological progression of MRI systems has allowed intra-operative MRI (iMRI) to augment neuro-navigation (Figure 5a,b,c) using either low field strength1, 2, 10, 15, 21, 24, 28, 33, 34, 41, 55-62 or high field strength scanners.24, 58, 59 Low field iMRI systems carry the advantages of lower cost, and the ability to use standard surgical instruments, as the surgical field is past the 5-Gauss line of the magnet (Figure 5). The patient or the scanner must be moved each time for image acquisition, which significantly increases the operative time. In a series of thirty patients with pituitary microadenomas undergoing transsphenoidal microscopic resection, Bohinski et al reported detection and subsequent resection of residual tumor in 66% of the patients using low field iMRI.23 Additionally, they detected a significant hematoma in one patient which led to conversion of the procedure to open craniotomy. In a separate series of forty-four patients undergoing transsphenoidal resection of pituitary macro-adenomas, Falbusch et al. reported that 34% of patients underwent resection for residual tumor detected on low field iMRI.24 While a significant percentage of residual tumor was detected in their series, the images were inconclusive in 27% of patients, with 20% having false positive exams, casting some doubt on the utility of low field iMRI.

Figure 5. A. Intra-operative MRI scanner (top left). This portable device (Polestar®; Medtronics Surgical Navigation Technologies, Louisville, CO.) enables intraoperative low-field strength (0.2 Tesla) images to be acquired in the operating room, and integration of the updated MRI images into the navigation system. B. Illustration of intraoperative portable MRI in use (bottom left). Note that ferromagnetic objects such as microscope and surgical trays can be placed in relatively close proximity to the scanner. C. Typical intraoperative MRI showing pituitary tumor.

High field iMRI systems provide significant advantages over their low field counterpart with regards to image acquisition and quality (Figure 6). For most sequences the acquisition time is shorter, and high field strengths allow for more advanced sequences to be performed, such as diffusion tensor and functional imaging, though this may be less useful in transsphenoidal surgery. As with low field iMRI, surgery is performed outside the magnetic field necessitating movement of the patient for imaging. Although this can be partially circumnavigated with the use of MRI compatible instruments, allowing surgery to be performed inside the magnetic field, the costs can be somewhat prohibitive. Nimsky et al., using high field strength iMRI, noted superior image quality and decreased acquisition time of some sequences compared to low field iMRI, with a 31% increase in complete resection of pituitary tumors.31 They also reported false positive exams for 20% patients using T1 sequences, which resulted in T2 sequences being adopted for assessment of residual tumor.

Figure 6. Electromagnetic tracking system with surface matched registration. Note registration reference marker attached to forehead and magnetic field reference frame on left. In this system, the head does not require rigid fixation and the electromagnetic signal eliminates line-of-sight issues which may be present for optical tracking systems.

Whilst iMRI is able to provide superior soft tissue detail, it is burdened by the necessity of specialized operating suites, instrumentation, and prolonged anesthesia/OR time which increases the overall cost of using this modality.10 Low field MRI leads to a diminution of image quality, with a limitation of specific sequences, which may impact the interpretation of pathology.11, 33, 61 Many authors however feel that despite these shortcomings, the ability of iMRI to detect occult residual tumor affords it a significant advantage over other forms of navigation during TSS.

Visual technology through the use of microscopes, and now endoscopes for TSS, has been augmented by intra-operative navigation using iMRI. In a series of fifteen patients of endoscopic assisted TSS, Schwartz et al detected post-operative residual tumor on iMRI in three patients.34, 35 They noted lower detection of residual tumor with iMRI with the use of the endoscope, compared to historical controls where microscopic resection was performed. In a similar comparison, Theodosopoulos et al reported their results using endoscopic resection of pituitary macroadenomas in conjunction with iMRI in twenty-seven patients,62 in which three patients underwent additional resection based on detection of residual tumor. Given the paucity of studies, the small numbers in each, and the lack of data regarding clinical effect, it is difficult to make recommendations regarding the true advantages of the endoscopic assisted technology. However, it is likely that as image quality and endoscopic technology improve, matched by the push towards minimally invasive approaches, we will hopefully see more data with which to make a definitive comparison.

Electromagnetic Navigation Systems

Neuro-navigation systems offering three dimensional tracking most commonly employ either optical or electromagnetic (EM) systems. EM systems have been in development since the late 1970s with utilization in surgical clinical applications over the past ten years.63 The concept of EM navigation is based on the generation of a low energy cubital magnetic field that encompasses the head using a single transmitter coil array. A pointer that is either rigid or flexible, can be digitally defined in space through triangulation using magnetic field voluming algorithms referenced from two distally placed probe markers. A reference frame, usually applied to the scalp, is required enabling surface registration within the cubital magnetic field. Initial EM systems relied upon radiofrequency transmitters mounted to the headsets, requiring a CT with the headset in place.40 As EM systems and software algorithms evolved, headsets and their associated risk of image drift have been augmented through the utilization of matched surface registration,64 negating the requirements of CT scans with fiducial markers (Figure 6).

EM navigation systems offer the ability of direct image fusion from previous MRI scans with either pre-operative or intra-operative CT (iCT) scans. Portable iCT, if available within the OR, may expedite workflow, minimizing additional costs.64

Magnetic tracking systems possess several essential advantages over the more traditional optical tracking neuro-navigation systems. Firstly, magnetic tracking obviates the need for rigid three-point skull fixation. Positioning the head on a horseshoe device is not only less traumatic to the patient, but it affords the surgeon the added benefit of increased comfort and better visualization by not having to rely on a fixed angle of approach throughout the case. Minor positional readjustments by changing the degrees of flexion or extension of the patient’s head as well as lateral tilt can be beneficial in approaching some skull base lesions. Alternatively, when optical based systems are utilized with rigid skull fixation, any accidental displacement of the head in relation to the reference fiducials may necessitate re-registration of the navigational device. In contrast, our experience with EM navigation systems for TSS where the reference marker is secured to the scalp usually with an adhesive, has been extremely effective ensuring high level accuracy in conjunction with the surgical freedom to move the patients head as required.64

Secondly, magnetic based devices preclude the need for a direct line of sight. One of the problems associated with optical systems is the interruption of the infrared pathways between camera and reference fiducials or probe by the operative microscope, sterile drapes, or a variety of obstacles present in the operating room. This is especially true in TS cases due to the close proximity of the operative microscope and surgeon to both the head and the operative field. EM navigation systems solve this problem by replacing the infrared tracing device with a magnetic field generator placed under the sterile drapes and close to the patient’s head. Although there have been no definitive comparative trials of EM and optical based systems in TS surgery, our experience suggests the accuracy of EM systems is at least comparable.

One of the concerns regarding EM navigation is the distortion of image accuracy due to other electromagnetic devices or ferromagnetic objects impacting the low energy cubital magnetic field. It is known that three types of sources may interfere with the normal operation of EM tracking systems: background noise from ambient electrical devices (wiring, lighting etc.), generated EM fields (electrical equipment) and ferromagnetic behavior of metallic instrumentation.65, 66 Although it is often difficult to detect the source and strength of many potential distortions (in contrast to optical systems where line of sight issues are directly apparent), inference affecting the accuracy of EM systems in a standard operating room has been shown to be minimal with most systems, maintaining millimeter accuracy.31, 32, 65, 67 Suggestions to maintain accuracy and avoid distortion include operating rooms distant to intra-operative functioning MRIs, and the avoidance of ferromagnetic metal within the EM field. In our experience, distortion by other EM devices in the room or ferromagnetic objects has not been apparent. The only alteration to our usual TS procedures has been the substitution to an MRI compatible (non-ferromagnetic) nasal speculum, which enables tracking along the barrel of the device. A further advantage of EM tracking is the ability to combine the probe with instruments in use (e.g. curette or suction), and to accurately navigate in a non-linear trajectory by bending the probe tip to interrogate anatomical points behind other structures or out of direct line of sight view. Likely these attributes will be increasingly important as flexible endoscopic devices are developed and become more utilized.

Conclusion

TSS in the modern era has been practiced for over one hundred years, undergoing gradual refinement in concordance with the development of new technologies for real-time intra-operative imaging and navigation. The evolution of neuro-imaging and subsequent navigation tools in TSS has included the progression from lateral fluoroscopy and pneumatography to frameless stereotactic navigation using intra-operative optical and electromagnetic tracking systems. This evolution has improved surgical morbidity, operative success and improved post-operative recovery. It is likely that the combination of intra-operative imaging and frameless navigation will be applied to an increasing spectrum of disorders throughout the body. As these systems continue to evolve, surgeons should recognize the benefits and limitations of the varied technologies and select the appropriate neuro-navigation tool for individual cases.

Disclosures

The authors have no disclosures or conflicts of interest related to this manuscript.

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