Transformation in Mandibular Imaging With Sweep Imaging With Fourier Transform Magnetic Resonance Imaging

Transformation in mandibular imaging with sweep imaging withfourier transform magnetic resonance imaging

Ayse Tuba Karagulle Kendi, MD*, Samir S. Khariwala, MD**, Jinjin Zhang, PhD***, Djaudat S.Idiyatullin, PhD***, Curtis A. Corum, PhD***, Shalom Michaeli, PhD***, Stefan E. Pambuccian,MD****, Michael Garwood, PhD***, and Bevan Yueh, M.D.***Department of Radiology**Department of Otolaryngology***Center for MR Research****Department of Laboratory Medicine and Pathology

AbstractObjective—Current imaging techniques are often sub-optimal for the detection of mandibularinvasion by squamous cell carcinoma. The aim of this study was to determine the feasibility of amagnetic resonance imaging (MRI) based technique known as Sweep Imaging with FourierTransform (SWIFT) to visualize the structural changes of intra-mandibular anatomy duringinvasion.

Design—Descriptive case study

Setting—Tertiary academic institution

Method—Two specimens from patients with oral carcinoma who underwent segmentalmandibulectomy were imaged using a 9.4 Tesla Varian MRI system. The SWIFT images werecorrelated with histological sections.

Results—The SWIFT technique with in vitro specimens produced images with sufficientresolution (156–273) and contrast to allow accurate depiction of tumor invasion of cortical andmedullary bone. Both specimens had histopathological evidence of mandibular invasion withtumor. A high degree of correlation was found between MR images and histopathologic findings.

Conclusion—SWIFT MRI offers three-dimensional assessment of cortical and medullary bonein fine detail with excellent qualitative agreement with histopathology. MR imaging with theSWIFT technique demonstrates great potential to identify mandibular invasion by oral carcinoma.

INTRODUCTIONAdvanced squamous cell carcinoma arising in the oral cavity often invades the mandible.Depending of the degree of invasion, patients may be surgically managed with a marginal orsegmental mandibulectomy. In many cases however, the periosteal layer serves as anadequate barrier to tumor invasion such that mandibulectomy is not required. Unfortunately,

Corresponding author: A.Tuba Karagulle Kendi, M.D. University of Minnesota, Department of Radiology MMC 292 Mayo 8292A420 Delaware St. SE Minneapolis, MN 55455 Phone: 612-626-7741 [email protected].

DISCLOSURE Dr. Garwood has an equity interest in SSI, Dr. Idiyatullin is a consultant for SSI, and Drs. Corum and Garwood andIdiyatullin are entitled to sales royalty through the University of Minnesota for products related to the research described in this paper.These relationships have been reviewed and managed by the University of Minnesota in accordance with its conflict of interestpolicies.

NIH Public AccessAuthor ManuscriptArch Otolaryngol Head Neck Surg. Author manuscript; available in PMC 2012 June 20.

Published in final edited form as:Arch Otolaryngol Head Neck Surg. 2011 September ; 137(9): 916–919. doi:10.1001/archoto.2011.155.

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detecting bone invasion prior to surgery is often difficult using currently available imagingtechniques. The preoperative determination of the presence or absence of mandibularinvasion with a high degree of accuracy would be useful for several reasons. First,knowledge of invasion necessitating segmental mandibulectomy allows the surgeon toperform the surgery without risking close margins or tumor spill while attempting marginalmandibulectomy. Second, accurate assessment of invasion has the potential to preventunnecessary mandibulectomy which can have a significant impact on a patient's functionaland cosmetic outcome. Lastly, preoperative knowledge of bone invasion allows for accurateplanning with regard to the most appropriate reconstructive technique.

Multiple imaging modalities have been applied to preoperatively assess mandibularinvolvement. These include pantomography, computed tomography (CT), magneticresonance imaging (MRI), scintigraphy, single photon emission computed tomography, and(18) F-fluorodeoxyglucose (FDG) positron emission tomography (PET)/CT1–78. CT andMRI are currently the most commonly used imaging modalities to evaluate mandibularinvasion in oral carcinoma.

CT is known to provide high sensitivity and specificity with the application of propersettings (3 mm or less section thickness, isotropic voxel acquisition)2, 9. The addition ofsoftware applications, such as Dentascan, also adds diagnostic value2, 10, 11. One of thedrawbacks of Dentascan is the difficulty in resolving the difference between corticalirregularity and tumor invasion11. Furthermore, CT is compromised by beam hardeningartifacts (produced by dental amalgam or prosthetic implants) which significantly degradethe assessment of mandibular infiltration by tumor2, 12, 13.

Magnetic resonance imaging is regarded as a highly accurate examination in the assessmentof extension of tumor in the soft tissues, however its role in depicting extension of tumor tothe mandible is considered limited due to frequent overestimation of corticalinvasion3, 14, 15. This overestimation results from signal changes associated withinflammatory conditions including periodontal disease and peritumoral edema which arecomparable to those seen with neoplastic invasion2.

Like many of the tissues of the musculoskeletal system, cortical bone produces no signalwith conventional MR techniques, limiting the characterization of image contrast anddifferentiation of adjacent soft tissues16–18. In biological tissues, MR signal comes from thespinning of magnetic moments of hydrogen nuclei. The signal is detectable after aradiofrequency (RF) pulse application. Because the molecular motion within denselymineralized bone is highly restricted, the signal from bone quickly decays after RFexcitation. The time-constant describing the signal's decay, known as the transverserelaxation time (T2)19, is approximately 200 microseconds in cortical bone. In conventionalMRI, excitation and acquisition events are separated by the length of time known as theecho time (TE), which is typically >1 ms, which is too long to detect the signal from corticalbone19–21.

The most important factor in mandibular management is to accurately identify the presenceof neoplastic invasion and its precise extent by means of preoperative evaluation to obtainadequate oncologic control and to minimize functional sequelae2. The ideal diagnostic toolshould provide non-invasive demonstration of neoplastic invasion of both cortical andmedullary bone to allow selection of an accurate surgical strategy2.

A fast and quiet method of MRI known as SWIFT (Sweep Imaging with FourierTransformation) creates new opportunities for imaging in medicine19–21. SWIFT uses time-shared excitation and signal acquisition. This allows the detection of signals with a broaddistribution of relaxation times, including extremely short T2. This technique offers

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delineated assessment of cortical and medullary bone which is not possible withconventional imaging techniques. The present study was designed to assess the feasibility ofthe SWIFT technique to visualize intra-mandibular anatomy and potential bony invasion byoral-squamous cell carcinoma through comparison with histopathologic findings.

METHODSThis study was approved by the institutional review board. Two mandibular specimens wereobtained after segmental resections. The operative specimens were handed directly to studystaff, who transported the specimens for ex-vivo imaging at the Center for MagneticResonance Research at the University of Minnesota. Following imaging, the specimens weretransported back to surgical pathology for routine histological processing.

Post resection imaging techniqueExperiments were performed with a 9.4T/31-cm horizontal MRI scanner (MagnexScientific, UK) equipped with 30 G/cm gradients (11 cm ID, 300 μs rise time; MagnexScientific) and driven by a Varian/Agilent Direct Drive console (Varian, CA). RFtransmission and signal reception were performed with a home built, single loop, 25 mmdiameter coil.

In the SWIFT sequence the excitation bandwidth and acquisition spectral width were both125 kHz. The repetition time (TR), including 2ms hyperbolic secant pulse length, was2.5ms. The total number of projections was 128000. The average acquisition time wasapproximately 8 minutes.

Figure 1(a) and figure 2(a) show SWIFT images obtained with the pulse excitationcoincident with the tissue water resonance frequency. In figure 2(b) and 2(e), A frequencyselective pulse was placed +1.5 kHz and −1.5 off resonance from water excitation pulse tosuppress short T2 and fat signal, respectively. In Figure 2(d), the water signal wassuppressed. In figure 2(a), the suppression pulse was replaced by an equal duration delay tomake the total acquisition time the same in all figures. In figure 2(c) subtraction of theSWIFT image with and without the off-resonance suppression pulse provides images of theshort T2 component.

Assessment of post resection imagesMandibular cortical invasion was diagnosed by interruption or lack of the typicalhypointense signal of cortical bone. Mandibular bone marrow involvement was diagnosedby extension of the soft tissue tumor to the marrow cavity with replacement of the marrowfat.

Histopathologic technique and assessmentMandibulectomy specimens were grossly examined by the pathologist to assess thepresence, size and location of the tumor, its relationship to the mandible and distance frommargins. The specimen was photographed and soft tissue margins were submitted forhistologic examination. The specimen was then fixed in toto in 10% buffered formalin for24 hours and then decalcified for 1 to 4 days, until soft enough to be sectioned with theknife. After decalcification, the mandible together with the surrounding soft tissues andtumor were sectioned at 0.3 cm intervals. The slices were photographed and then processedfor paraffin embedding; a single 5 μm section per slice was made and stained withhematoxylin and eosin (H&E). The presence of bone invasion, site(s) of invasion, pattern ofinvasion (erosive or infiltrative)22 and the depth of invasion into bone were evaluated by thepathologist (SEP). Histologic sections were scanned on an Aperio CS whole slide scanner

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(Aperio Technologies, Inc., Vista, CA) and exact measurements of depth of invasion anddistance to margins were made using the digital images. Gross and microscopic imagesshowing the relationship of tumor to bone in the areas imaged by MR were selected andcompared to the MR images.

RESULTSSWIFT images of the specimens revealed detailed bone and soft tissue anatomy, includingsoft tissue tumor, cortical bone and medullary bone. SWIFT demonstrated fine anatomicaldetails including nutrient vessels and fine trabecular bone structure. SWIFT producedevidence of cortical bone invasion as cortical interruption of the hypointense signal ofcortical bone. Medullary bone invasion was also demonstrated in both specimens asextension of soft tissue tumor into the medullary cavity and replacement of medullary fatwith tumor. The demarcation between tumor-free medullary bone and tumor-invadedmedullary cavity is delineated in fine detail (Figures 1 and 2). Short T2 images (Figure 2c)acquired from subtraction of the initially saturated short T2 component from the routineSWIFT image revealed a well delineated contour of cortical bone.

Histopathologic specimen findings highly correlated with SWIFT imaging findings (Figures1 and 2).

DISCUSSIONThis preliminary report demonstrates that the SWIFT imaging technique has the capacity toshow fine details of intra-mandibular anatomy. Furthermore, the correlations between thehistological and MR images of these two specimens clearly show malignant invasion thathas not been previously demonstrated with MR techniques. The data described in this reportsuggests that magnetic resonance has a great deal of potential in accurately determiningbone invasion preoperatively.

The main advantage of SWIFT originates in its nearly simultaneous excitation andacquisition scheme. SWIFT allows a TE of almost 0, meaning signal acquisition can beginwithin a few microseconds after excitation. Thus, SWIFT obtains signal from cortical bonethat has a fast decaying signal, produces less distortion from magnetic susceptibility and isless sensitive to motion artifacts (18). Also, due to an incrementally changed gradient, theSWIFT method is nearly 50dB quieter than a comparable MRI exam (18). In this study weobtained a short T2 image by subtracting an initially saturated short T2 component from theSWIFT image (Figure 2c). As conventional MR imaging techniques are not able to fullyeliminate the long T2 component, there is always a possibility of false positive results ofcortical bone invasion due to periodontal disease or inflammation. We do believe that theSWIFT technique and the associated short T2 images will overcome false positive results ofcortical bone invasion.

There were limitations to our study. First, we studied only two specimens. These specimenswere from patients with preoperative clinical and radiological evidence of cortical andmedullary bone invasion. The images served primarily to demonstrate the feasibility ofSWIFT to show intra-mandibular anatomic details. Hence, the strength of the SWIFTtechnique in assessment of early cortical bone invasion by oral cancer wasn't evaluated inthis study. Nevertheless, given the high quality images obtained, we are optimistic that thistechnique will allow identification of very early bone invasion that is not otherwise evident.Third, we are aware that the acquisition of images of similar quality in an in vivo setup withlower magnetic field strength is more challenging. For this reason, the clinical utility ofSWIFT technique needs to be determined in future clinical studies.

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In conclusion, our study is very promising in that it offers a SWIFT based MRI techniquefor accurate assessment of minute changes of cortical and medullary bone in three-dimensions without any ionizing radiation. It has the potential to precisely determine theextent of mandibular bone invasion associated with oral carcinoma. This study is a crucialstep toward the goal of developing a robust and non invasive approach for preoperativeimaging of mandibular invasion. We are currently in process of developing a human subjectstudy of SWIFT techniques in a 4 Tesla human magnet to solidify the role of this new andtransformative technology in the assessment of head and neck tumors.

AcknowledgmentsThe authors thank Andrew S. Wallschlaeger, PA for his help with gross specimens, Carrie Zine, HTL (ASCP) forher help with sectioning the specimens and Jonathan Henriksen, for his help with digital gross and microscopicpathology images.

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Figure 1.SWIFT image (1a) of the one of the specimens, with resolution of 273 micron, show largesoft tissue tumor (stars). There is cortical interruption (arrow) and extension of thesquamous cell carcinoma to the medullary cavity (arrowheads). Soft tissue invasion ofmedullary bone is well demarcated from normal fat containing bone marrow and trabecularstructure of medullary cavity. Corresponding gross image (1c) and histopathologic images(1b, 1d, 1e and 1f) demonstrate infiltrative invasion of the lingual aspect of the mandibularbone along a 15 mm front to a depth of 2.8 mm by a moderately differentiated squamouscell carcinoma. Surgical margins are clear (1b, H&E ×1, 1d H&E ×2, 1e H&E ×40, 1f H&E×100).

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Figure 2.SWIFT images (a–f) of the second specimen, with resolution of 156 micron. a) regularSWIFT image b) SWIFT image with short T2 component suppressed c) image of short T2component (subtracting fig. b) from fig. a)) d) SWIFT image with fat on resonance andwater suppressed e) SWIFT image with water on resonance and fat suppressed f) both fatand water on focus, (adding fig. d and fig. e)). Images show cortical interruption andextension of soft tissue tumor into the medullary cavity. g) Gross photograph and i), j), andk) histopathologic images showing a well-differentiated squamous cell carcinoma invadingalong a front of 6.6 mm through the alveolar ridge of the mandible with an erosive andinfiltrative pattern for a depth of 1.5 mm (2h, H&E ×1, 2i H&E ×10)

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Documents

Transformation in Mandibular Imaging With Sweep Imaging With Fourier Transform Magnetic Resonance Imaging