T HE use of computed tomography

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specimens. Five of the specimens were obtained during laryngectomies performed on patients with highstage tumors of the larynx. Four specimens were from patients with no known disease.

1 Ron Kikinis, MD #{149}Markus Wolfensberger, MD #{149} Chris Boesch, MD, PhD #{149} Ernst Martin, MD Larynx: MR Imaging at 2.35 T To study the consequences of an improvement in spatial resolution, the authors compared magnetic resonance (MR) images of nine laryngeal specimens with whole-organ histologic slides of the same specimens. Five of the specimens were obtained during laryngectomies performed on patients with highstage tumors of the larynx. Four specimens were from patients with no known disease. The MR images were obtained on a 2.35-T system with a closely fitting probe head. A conventional spin-echo sequence was used, with Ti- and T2-weighted settings. The in-plane resolution obtamed was about 0.3 mm. The T2- weighted images generally showed better contrast and allowed identification of the perichondrium. The resolutions used were not much greater than those clinically available. The findings suggest that there will be important advances in clinical MR imaging of the larynx in the near future. Index terms: Larynx, MR studies, #{149} Lamynx, neoplasms, #{149}Magnetic resonance (MR), experimental #{149} Neck, MR studies, Radiology 1989; 171: I From the Department of Magnetic Resonance, Children s Hospital (R.K., C.B., EM.), and the Department of Otonhinolanyngology, Head and Neck Surgery (MW.), University Hospital, Zurich. From the 1987 RSNA annual meeting. Received May 3, 1988; revision nequested June 14; revision received October 13; accepted November 1. Address reprint requests to R.K., Neuno MR. Department of Radiology, Brigham and Women s Hospital, 75 Francis St. Boston, MA RSNA, 1989 T HE use of computed tomography (CT) has improved the diagnostic imaging of the head and neck megion, especially the deep laryngeal structures (i). In laryngeal cancer, however, CT has many clinically important limitations (1-7). Often the tumor itself is not recognizable, only its mass effect, and submucosal infiltration is not detectable at the level of the vocal cords. Moreover, the invasion of the penichondnium and the cartilages is recognized only in very late stages, and special problems are posed by the irregular calcification of the thyroid cartilage (1,8-li). Finally, contrast-material enhancement is usually necessary, making the procedune invasive. In the last few years, magnetic resonance (MR) imaging of the larynx has become at least as effective as CT in the evaluation of laryngeal cancer (12-17). Although its diagnostic sensitivity to cancerous invasion of the laryngeal skeleton is not yet satisfactory (3,12), MR imaging is far from reaching its technical limits. The aim of this study was to explore the diagnostic potential of the improved spatial resolution possible with a highfield-strength MR unit with strong gradients. We chose to perform in vitro studies of the larynx for several reasons: (a) MR imaging is well suited to in vitro studies. (b) Laryngeal specimens are easily obtained at noutine autopsies and cancer operations. (c) Laryngeal specimens are small enough for imaging in small-bone machines. (d) Theme is a reliable technique for producing whole-organ histologic slices for histomicroscopic correlation with the MR images (18). MATERIALS AND METHODS Nine larynges were studied: four normal specimens collected at routine autopsies and five specimens obtained at lamyngectomy from patients with histologically proved high-stage glottic or supraglottic tumors. The patients were two women Figure 1. Experimental setup. Polyethylene bag containing the specimen is laid on the plaster mold, which is inserted into the probe head. Plexiglas semicircles are positioning aids and indicate the opening of the magnet. and seven men, aged years. Before imaging, eight of the larynges were fixed in 4% formalin for at least i day. The ninth specimen was imaged on the same day as the operation, before immersion in formalin. This specimen was examined again after 6 and 10 weeks, but no changes due to fixation were observed. To achieve exactly parallel positioning of the larynges, we constructed a mold with the dimensions of the bone of the antenna. The larynges were positioned as desired in wet plaster in the mold. After the plaster had hardened, the larynges were removed, and the plaster was dried thoroughly in an oven. The imaging was performed on a T, 40-cm-bone magnet (Spectrospin Medspec 24/40; Bruker, Medical Imaging, F#{227}!- landen, Switzerland). This instrument is used at our hospital for the examination of children. To obtain an optimal signalto-noise ratio (S/N) and homogeneous image quality, we used a resonator-type probe head (transmitting and receiving antenna, corresponding to coils in lowfield-strength systems) with an opening of 7.0 cm (19). The specimens were taken out of the formalin, rinsed briefly with water, and then placed in the probe head. The plaster form was used as a positioning aid (Fig i). After the system was shimmed and tuned, imaging was penformed. Conventional spin-echo (SE) se- Abbreviations: SE spin-echo, S/N signalto-noise ratio, TE echo time, TR repetition time. 165

a. b. C. d. Figure 2. Effects of different gradient settings. All examinations were performed with conventional SE (2,055/80) sequences.

The outer hypointense border of the thyroid cartilage (arrowheads) is widest on a and smallest on ; this is due to the fat shift caused by the read gradient (Fig 6), which is directed from ventral to

(d) Read and phase-encoding directions are interchanged as compared with C; all other imaging variables are identical.

Comparison of Ti (a, C) and T2 (b, d) weighting. Larynx was obtained from patient operated on for a supraglottic laryngeal cancer with infiltration of the vocal cords.

Thyroid cartilage is centrally hypointense (arrowhead) with a hypenintense rim (long arrow) on both Ti- and 12-weighted images.

Epiglottic cartilage is visible on both images, and the margins of the thyroid cartilage are blurred (arrow). quences were used.

In selected cases, sagittal and coronal sections were obtained in addition to the axial sections.

In other series, the field of view was doubled to 16 cm and then to 32 cm, while the other settings were not changed.

2 a. b. C. d. Figure 2. Effects of different gradient settings. All examinations were performed with conventional SE (2,055/80) sequences. Images with smaller gradients (larger field of view) have been zoomed mathematically. The section thickness was 2 mm; the pixel size, 1.2 X 1.2 mm (a), 0.6 X 0.6 mm (b), or 0.3 X 0.3 mm (c). The outer hypointense border of the thyroid cartilage (arrowheads) is widest on a and smallest on ; this is due to the fat shift caused by the read gradient (Fig 6), which is directed from ventral to dorsal. On a, the fat shift is so prominent that the marrow is superimposed on the pamaglottic space (arrow). (d) Read and phase-encoding directions are interchanged as compared with C; all other imaging variables are identical. The effect of the fat shift on the appearance of the outer hypointense bonder of the thyroid cartilage (arrowheads) is emphasized. a. b. C. d. Figure 3. Comparison of Ti (a, C) and T2 (b, d) weighting. Larynx was obtained from patient operated on for a supraglottic laryngeal cancer with infiltration of the vocal cords. (a, b) Axial images obtained at the level of the thyroid cartilage and through the arytenoid cartilages. Thyroid cartilage is centrally hypointense (arrowhead) with a hypenintense rim (long arrow) on both Ti- and 12-weighted images. Inside of arytenoid camtilages is hypemintense on Ti-weighted image and of intermediate intensity on T2-weighted image (short arrow). This indicates a fatty marrow. (c, d) Paramedian sagittal images. Epiglottic cartilage is visible on both images, and the margins of the thyroid cartilage are blurred (arrow). quences were used. Ti-weighted images were obtained at settings of 470/30 (repetition time [TR] msec/echo time [TE] msec) (n = 1), 700/30 (n i), on 800/30 (n = 5); T2-weighted images, at 2,500/90 (vi = i) on 2,055/80 (n 6). The section thickness was 2 mm (width at half the height of a gaussian profile), the in-plane resolution was 0.3i3 mm, and the anisotnopy (ie, ratio of in-plane resolution to thickness) of the voxel was almost 7. Two measurements were obtained. In selected cases, sagittal and coronal sections were obtained in addition to the axial sections. In one case, the imaging settings were changed to observe their influence on S/ N, chemical shift, and contrast. In one senies, the phase-encoding direction was changed. In other series, the field of view was doubled to 16 cm and then to 32 cm, while the other settings were not changed. After imaging, the larynges were processed histologically according to the technique described by Michaels and Gregom (18). Whole-organ slices 20 zm thick were obtained by means of stepwise slicing at intervals of 1-2 mm. The slices were then stained with hematoxylin and eosin. In all but one of the cases, the histologic sections were oriented axially. They were correlated with the images by both a radiologist and a lanyngologist. Regions of interest were directly examined under the microscope for definitive diagnosis. RESULTS At the level of the vocal cords, the T2-weighted images showed good contrast and allowed identification of all important glottic structures (Figs 2-5). A comparison of images obtamed at clinically available resolutions with images of the same specimens obtained at higher resolutions clearly indicates that the diagnostic sensitivity could be improved by doubling the spatial resolution (Fig 2). The soft-tissue-cartilage interface is hardly visible at a pixel size of 1.2 mm, but even the penichondnium is visible at 0.3 mm. At the glottic level, the axial images are superior to the sagittal or comona! images (Fig 3). In all inspected larynges, the interface between the thyroid cartilage and the glottis shows a characteristic banding (Fig 4): The medulla of the thyroid camtilage (ie, the central medullary space of the ossified cartilage) has an intermediate signal intensity and a granulated appearance on the T2-weighted images. Closer to the glottic lumen, a thin, hypointense line becomes visible, which correlates with bone and calcified cartilage seen histologically. Next appears a hypenintense line that represents the noncalcified cartilage, followed by another thin, hypoin Radiology April 1989

_5,. 4.. b. C. Figure 4. Penichondnial structure. (a) On T2-weighted image, marrow of ossified thyroid cartilage has a granulated, grayish appearance (small arrowhead).

thin layer of uncalcified cartilage (medium arrow).

(b) On hematoxylin-eosin-stained slice of the same organ, cut at the same level as a, same structures can be identified. (C) Magnified view of penichondnial region, as outlined in b.

3 _5,. 4.. b. C. Figure 4. Penichondnial structure. (a) On T2-weighted image, marrow of ossified thyroid cartilage has a granulated, grayish appearance (small arrowhead). Next structure toward the lumen is a thin, dark line corresponding to a layer of bone and calcified cartilage (small amrow), followed by a line of intermediate signal intensity corresponding to a thin layer of uncalcified cartilage (medium arrow). Next is a thin, hypointense line that represents the pemichondnium (large arrow), followed by the tissues of the paraglottic space (large arrowhead). (b) On hematoxylin-eosin-stained slice of the same organ, cut at the same level as a, same structures can be identified. (C) Magnified view of penichondnial region, as outlined in b. Shearing forces during histologic preparation caused an artificial cleft in the penichondnium (arrow). Because the specimen was cut after imaging, it must be assumed that the cleft did not exist during imaging. White arrow indicates uncalcified cartilage; curved arrow, calcified cartilage. Table 1 Imaging Settings Used in Various Studies Pulse Sequence Field Strength Voxel Volume Surface No. of Ti- Inter- T2- Study (T) (mm3) Coil Cases Weighted mediate Weighted Castelijns and Yes / ,000/ Doomnbos, (27) Castelijns et al Yes /38 1,500/38 1,500/ (12) Castelijns et al, Yes /38 1,500/38 1,500/ (13) Gademann et al, No 7 600/30 1,200/30 1,200/ (15) Glazer et al, No 9 500/30 1,500/30 1,500/ (10) Haelsetal, No 7 600/30 1,200/30 1,200/ (26) Lufkinand Yes / Hanafee, 1985(25) Present study Yes / ,055-2,500/ tense line, which is usually only i pixel wide. This line corresponds histologically to the fibrous perichondnium. The last visible structure of the soft-tissue-cartilage interface is the pamaglottic fatty tissue, which has a reticulated, irregular appearance. Fewer details were visible on the Ti-weighted images than on the T2- weighted images at the glottic level. The relation of the tumors to their neighboring anatomy was especially well seen on the T2-weighted images (Fig 5). All tumors reached the lamyngeal cartilage, and in four cases infiltration was diagnosed in at least one location. The MR images were comelated with the corresponding histologic slides. DISCUSSION The introduction of CT was a breakthrough in the imaging of the deeper laryngeal structures. Howeven, CT leaves some clinically important questions unanswered. It is particulanly limited in demonstrating tumonous invasion of the thyroid cartilage, with its typical irregular mix of calcified, ossified, and noncalcified cartilage (1,7,20-24). MR imaging has the potential to outperform CT in the diagnosis of Iaryngeal cancers, because of its ability to differentiate soft tissues (12,13, 16,17,25,26). The relative penformance of MR imaging depends on the voxel size (resolution) and the obtainable S/N (10). Recently published data on this subject show a wide scatter of the relevant imaging variables (Table 1). MR imaging is well suited for in vitro studies. Although some reports in the literature suggest changes in imaging due to changes in relaxation times after fixation with formalin (28), the MR appearance of the vanous tissues of the larynx does not change significantly after fixation. Due to the long examination times required with the SE sequences used in clinical practice, MR imaging is currently restricted to use in very cooperative patients. These limitations obviously do not apply to in vitro studies, which can, therefore, be used to explore the potential of this imaging modality The imaging system we used has a homogeneous magnetic field (±0.1 ppm for a 6-cm diameter) and linear gradients (up to 10 mt/m) that provide excellent image quality (29). The high field strength results in a very good S/N, which is especially important on the T2-weighted images. To optimize the S/N, we used a closely Volume 171 #{149} Number 1 Radiology #{149} i67

a. b. c. d. e. f. Figure 5. Tnansglottic tumor. (a) Contrast material-enhanced CT scan at the level of the cranial rim of the cnicoid.

(b) Ti-weighted image obtained at the same level as a. Essentially no additional information is provided concerning the tumor. Central part of the thyroid cartilage (arrowhead) looks hypointense.

Central pant is surrounded by a rim of intermediate signal intensity, corresponding to uncalcified camtilage, surrounded by a thin, hypointense line, which is the pemichondnium.

It replaces most of the endolaryngeal soft tissues, abuts against the thyroid penichondnium (arrows) without infiltrating it, and destroys parts of the contralateral cricoid cartilage (arrowheads).

At higher magnification than used for e and f, tumor cells were seen at both locations (not shown here). fitting probe head.

Because the opening of the probe head is small, plaster forms were used to position the specimen panallel to the main field.

4 a. b. c. d. e. f. Figure 5. Tnansglottic tumor. (a) Contrast material-enhanced CT scan at the level of the cranial rim of the cnicoid. Tumor is visible as a space-occupying, slightly irregularly enhancing structure on the left thyroid lamina. It is not clean whether there is infiltration of the cartilage. (b) Ti-weighted image obtained at the same level as a. Essentially no additional information is provided concerning the tumor. Central part of the thyroid cartilage (arrowhead) looks hypointense. Microscopically, this is seen as calcified cartilage. There are several hypenintense islands of bone marrow (arrow). Central pant is surrounded by a rim of intermediate signal intensity, corresponding to uncalcified camtilage, surrounded by a thin, hypointense line, which is the pemichondnium. (c) On T2-weighted image, full extent of the tumor can be delineated. It replaces most of the endolaryngeal soft tissues, abuts against the thyroid penichondnium (arrows) without infiltrating it, and destroys parts of the contralateral cricoid cartilage (arrowheads). (d) Hematoxylin-eosin-stained histologic slice. Higher-magnification views of areas outlined in d show thyroid cartilage (e) and contralatenal cnicoid cartilage (f). At higher magnification than used for e and f, tumor cells were seen at both locations (not shown here). fitting probe head. This device comesponds in some ways to the surface coils used with lower field strengths. Because the opening of the probe head is small, plaster forms were used to position the specimen panallel to the main field. There is discordance in the litenatune regarding which imaging settings should be used clinically. Table i is an overview of some of the combinations used in recent studies. Theme are considerable variations in variables relevant to image quality (voxel volume, application of surface coils, number of averages, and imaging sequences used). T2-weighted images are generally not favored, for two main reasons. First, a poor S/N is obtained with heavily T2-weighted images. Most of the published work was performed on units with a field strength of 0.6 T or less. On those devices, the S/N is especially problematic. The only group that used a 1.5-T system did not use a surface coil (15,26). The second problem is the long examination time required for T2-weighted images. Patients with laryngeal cancer are often unable to lie still for such a long period. The newly introduced fast-echo techniques may lessen the problem of motion artifacts (30). The voxel size used in this study (0.3 X 0.3 X 2 mm or 0.18 mm3) represents roughly a doubling of the resolution in all directions when compared with recently published results (Table 1). To compensate for the loss in S/N at the higher spatial resolutions, it would be necessary to acquire 64 times the number of measurements acquired at the lower resolution. This would mesuit in clinically unacceptable scanning times. Therefore, it is important to use high-field-strength units for such measurements and to optimize the examination for a better S/N. The full potential of high-fieldstrength units is obtainable only if strong gradients are available to enhance the spatial resolution. One consequence of a higher field strength is increased chemical shift. To zoom the image, one has several options: (a) Magnification of the image to increase the pixel size on the scope or the film, which provides no additional information (Fig 2a and 2b are magnified to the same size as Fig 2c). (b) Decrease in the frequency band width, which increases the mela- i68 #{149} Radiology April 1989

The same diffemence represents a smaller distance if the gradients become stronger (indicated as small arrows on the horizontal axis).

5 Fat Water Position of the image Figure 6. Gradient-dependent fat shift. For a small field of view, the gradients are strongem. The resonance frequencies of fat and water, dependent only on the main magnetic field (B0), are constant. With an active gradient, any difference in resonance frequency is translated into a distance. The same diffemence represents a smaller distance if the gradients become stronger (indicated as small arrows on the horizontal axis). This means that, for a given field strength, the fat shift is increased when the gradient is decreased. tive effect of the chemical shift. (c) The use of stronger gradients (Fig 2c), which decreases the effect of the chemical shift (Fig 6) in comparison with the two other methods. The minimization of the chemical shift is of special importance in evaluation of the soft-tissue-cartilage interface, which can be completely obscured by this artifact. A comparison of images of the same specimen obtained at diffenent gradient field strengths shows that the diagnostic gain is optimized by the combination of high field strength and strong gradients (Fig 2). For the evaluation of the penichondnium, axial images are superior to sagittal and coronal views in many ways. This is probably due to the strong anisotnopy of the voxels and the anatomy of the larynx. The penchondnium of the thyroid cartilage is sectioned perpendicularly on axial images. This means that a whole voxel is filled with pemichondnium. However, on a lateral sagittal on a ventral coronal image of the thyroid cartilage, the penichondnium is sectioned obliquely and obscured because of volume averaging with the surrounding structures (Fig 3). T2-weighted images provide much better soft-tissue differentiation than Ti-weighted images at the glottic level. Our findings did not contradict published data concerning the appeanance of the cantilages in vivo (13,25). This fact underlines the usefulness of in vitro studies with MR imaging. Calcified cantilages appear hypointense, and noncalcified cartilages are of intermediate signal intensity. The tumors that we imaged ranged from isointense to hypenintense on the T2-weighted images. The hypointense penichondnium of the cartilage therefore provides a clean diagnostic criterion for the evaluation of cartilage invasion (Table 2). This is true, however, only when the resolution is sufficient to allow detection of the penichondnium. In conclusion, we have demonstrated that the penichondnium is detectable in vitro at resolutions not much greater than those clinically available. To achieve this purpose, it is necessary to adjust the imaging variables of field strength and gradient strength to the anatomy of the larynx. While microscopic invasion is not observable with the resolution used in this study, the information gained from T2-weighted images enables early detection of tumor invasion into the cartilage. U Acknowledgments: We thank C. Cantieni and J. Terj#{233}k for their photographic skills and L. St#{246}klinfor technical assistance. References 1. Mancuso AA, Hanafee WN. Computed tomography and magnetic resonance of the head and neck. 2d ed. Baltimore: Williams & Wilkins, Wolfensbengen M, Kikinis R, Schmid S. et al. Den beitrag den computertomographie zur klassifikation von hypopharynx- und larynxkarzinomen. Laryng Rhinol Otol (Stuttg) 1987; 66: Kikinis R. Den beitnag den computentomographie zur abklaenung von karzinomen des hypophanynx und larynx: Zurich, Dissertation. University of Zurich, September 1987, p Sage) 55, Aufdenheide JF, Anonberg DJ, et a). High resolution computed tomography in the staging of carcinoma of the larynx. Laryngoscope 1981; 91: Bengmann AB, Neimann HL, Warpeha RL. Computed tomography of the larynx. Laryngoscope 1979; 89: Gamsu G, Webb WR, Shalit JB, et al. CT in carcinoma of the larynx and pyniform sinus: value of phonation scans. AIR 1981; 136: Horowitz BL, Woodson GE, Bryan RN. CT of laryngeal tumors. Radiol Clin North Am 1984; 22: Mafee MF, Schild JA, Michael AS, et al. Cartilage involvement in laryngeal carcinoma: correlation of CT and pathologic macrosection studies. J Comput Assist Tomogr 1984; 8: Mafee MF. CT of the normal larynx. Radio) Clin North Am 1984; 22: Glazer HS, Niemeyer JH, Balfe DM, et al. Neck neoplasms: MR imaging. I. Initial evaluation. Radiology 1986; 160: Archer CR, Yeager VL. Evaluation of laryngeal cantilages by computed tomography. Comput Assist Tomogr 1979; 3: Castelijns JA, Kaiser MC, Valk J, et a). MR imaging of laryngeal cancer. J Comput Assist Tomogn 1987; 11: Castelijns JA, Gemnitsen GJ, Kaiser MC, et al. MRI of normal on cancerous laryngeal cartilages: histopathologic correlation. Laryngoscope 1987; 97: Dillon WP. Applications of MRI to the head and neck. Semin US CT MR 1986; 7: Gademann G, Haels J, Konig R. et a). Nudean magnetic resonance tomognaphic staging of tumors of the oral cavity, ono- and hypopharynx and the larynx: a comparison with computed tomography and sonography. ROFO 1986; 145: Lufkin RB, Hanafee WN. Imaging the lanyngophanynx. Semin US CT MR 1986; 7: Lufkin RB, Hanafee WN, Wortham D, et a). Larynx and hypophanynx: MR imaging with surface coils. Radiology 1986; 158: Michaels L, Gregon RI. Examination of the larynx in the histopathology laboratory. Clin Pathol 1980; 33: Cross TA, Mueller S. Aue WP. Radiofrequency resonatons for high-field imaging and double-resonance spectroscopy. J Magn Reson 1985; 62: Archer CR, Yeager VL, Henbold DR. Cornputed tomography vs. histology of laryngeal cancer: their value in predicting laryngeal cartilage invasion. Lanyngoscope 1983; 93: Archer CR, Sage) SS, Yeagen VL, et a). Staging of carcinoma of the larynx: comparative accuracy of CT and lanyngography. AJR 1981; 136: Archer CR, Yeager VL. Herbold DR. Improved diagnostic accuracy in laryngeal cancer using a new classification based on cornputed tomography. Cancer 1984; 53: Reid MH. Laryngeal carcinoma: high-resolution computed tomography and thick anatomic sections. Radiology 1984; 151: Hoover LA, Calcatenra TC, Walter GA, et a). Preoperative CT scan evaluation for laryngeal carcinoma: correlation with pathological findings. Lanyngoscope 1984; 94:310-31S. 25. Lufkin RB, Hanafee WN. Application of sunface coils to MR anatomy of the larynx. AJR 1985; 145: Haels J, Lenarz I, Gademann G, et a). Nudean magnetic resonance tomography in the diagnosis of head and neck tumors: a companison of methods. Laryngol Rhino) Otol (Stuttg) 1986; 65: Castelijns JA, Doonnbos J. MR imaging of the normal larynx. J Comput Assist Tomogn 1985; 9: Kamman RL, Go KG, Stomp GP, et al. Changes of relaxation times Tl and T2 in rat tissues after biopsy and fixation. Magn Reson Imaging 1985; 3: Boesch C, Martin E. Combined application of MR imaging and MR spectroscopy in neonatal and pediatric research: installation and operation of a 2.35-T system in a clinic (abstn). Radiology 1987; 165(P): Haase A, Frahm J, Matthaei D, et a). FLASH imaging: rapid NMR imaging using low flipangle pulses. J Magn Reson 1986; 67: Volume 171 #{149} Number 1 Radiology #{149} 169

Fig year-old man with bilateral glottic cancer with subglottic extensions.

Fig year-old man with bilateral glottic cancer with subglottic extensions. 245 A B Fig. 1. 64-year-old man with bilateral glottic cancer with subglottic extensions. Axial scans at the level of the glottis (A) shows bilateral soft tissue masses protruding into the lumen. Bilateral