Magnetic Resonance Imaging of the Normal Tongue: Qualitative Evaluation of Fat-suppressed Contrast Enhanced Images

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1 Bulletin of the Osaka Medical College 49 1, , Original Article Magnetic Resonance Imaging of the Normal Tongue: Qualitative Evaluation of Fat-suppressed Contrast Enhanced Images Yasunori ARIYOSHI 1), Masashi SHIMAHARA 1), Yasuo UESUGI 2), Isamu NARABAYASHI 2) 1) Department of Oral Surgery, Osaka Medical College 2) Department of Radiology, Osaka Medical College Key Words : magnetic resonance imaging, fat suppression, tongue, anatomy ABSTRACT Objective: For diagnosing the lesions on magnetic resonance imaging (MRI), it is necessary to understand normal structures on each sequence. In this study, we attempted to clarify structures of the normal tongue on fat -suppressed enhanced MRI qualitatively. Clinical material and method: Twenty-seven fat-suppressed enhanced MR images of normal tongue were studied, which were obtained using a T1 weighted spin echo pulse sequence (T1WI- SE) with the chemical shift selective (CHESS) method by a superconducting MRI scanner operating at 1.5T. Tongue structures and their signal intensities on fat-suppressed enhanced images were assessed and compared to those obtained by non-enhanced T1WI. Results: Normal tongues were found to be composed of a symmetrical high signal area (HSA), low signal area (LSA), lingual septum, bilateral sublingual gland, and genioglossus muscle on nonenhanced T1WI. In the fat-suppressed enhanced images, HSA and lingual septum signal intensities were suppressed. Further, though the lingual mucosa was well visualized in fat-suppressed enhanced images (P<0.05), differentiation of HSA and LSA was difficult as compared to the nonenhanced scans (P<0.05). Conclusion: Fat-suppressed enhanced scans demonstrated simple anatomical structures as compared to conventional T1WI with independent signal intensity. Accordingly, we conclude that it is necessary to use both sequence for diagnosing the mass lesion located in the tongue. Introduction Magnetic resonance imaging (MRI) has become an essential modality for evaluating mass lesions in the oral and maxillofacial region, and clinical utility has also been reported (ARIYOSHI et al., 1998, 2000, 2003). In addition, fat-suppressed techniques have also been used to improve lesion detectability when surrounded by fatty tissue and/or to estimate whether the lesion includes fatty materials (LENZ et al., 2000). Lenz et al. (2000) presented the standardized protocol for evaluating head and neck lesions, which consists of plain T1-spin echo (SE), plain fat-suppressed (FS) T2 turbo-spin echo (TSE), and FS-T1-TSE after Gd-DTPA. Clinically, we have used plain T1 weighted images (conventional or fast spin echo; conventional T1WI or FSE-T1WI), FSE- T2 weighted images (T2WI) with or without fat suppression, and dynamic enhanced T1WI followed by fat-suppressed enhanced T1WI. However, for diagnosing lesions located in the tongue using a combination of these complex sequences, it is necessary to 21

2 22 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI clarify normal structures as revealed by each sequence. Especially, T1WI showed good anatomical structure of head and neck (LENZ et al., 2000), it is important to clarify whether or not the structure which could be detected on non-enhanced T1WI could also be detected on fat suppressed contrast enhanced MRI. In the present study, we observed delineated normal tongues and their surrounding structures using fat-suppressed contrast enhanced MRI and compare the results to those seen with non-enhanced T1WI. Materials and methods The study specimens were contrast enhanced fat-suppressed images of tongues from 27 patients (mean age standard deviation = years old, male to female ratio=16:11). These examinations were performed to diagnose the lesion which occurred in the oral and maxillofacial region except for the tongue and the floor of the mouth. None of the patients had lesions in the tongue or floor of the mouth seen clinically and/or radiologically, and none suffered from malignant entities or aggressive inflammatory processes systemically. The images were not affected by apparent artifacts, including motion and susceptibility, while tongue shape was determined to be symmetrical by viewing selected slices. The MRI scanner used was a SIGNA (General Electric Medical Systems, Milwaukee, WI) operating at 1.5 Tesla. The head coil that had a diameter of 28 cm or the surface coil was used. All sequences were performed with a slice thickness of 5.0 mm with an intersection gap of 0 to 1mm, a 256 x 224 imaging matrix, and a field of view of 26 cm. After obtaining conventional ( /40, TR/TE) or FSE T1WI ( /8-14/2-3, TR/TE/ET) and FSE-T2WI (4000/102/16-18, TR/TE/ET), coronal and/or axial contrast enhanced fat-suppressed T1WI were obtained by simultaneous intravenous bolus injection of gadopentetate dimeglumine (Magnevist, Japan- Scheling, Osaka, Japan) at 0.1 mmol /kg body weight. The contrast medium was injected intraveneously within 15 seconds. All image slices that included the tongue were used for estimation. The fat-suppressed method utilized in the present study was the chemical shift selective (CHESS) method (HASSE et al., 1985; SZUMOWSKI et al., 1999). 2. Images analysis Structures that composed the tongue and floor of the mouth were qualitatively assessed to determine whether those detected by non-enhanced T1WI were also detectable in fat-suppressed enhanced scans. For statistical analysis, a 2 test was used for comparing the detectability of each structure between the two types of scans, with P<0.05 considered to be significant. In addition, the signal intensity of each of those structures on fat-suppressed images were assessed and classified into 3 groups; high, intermediate, and low (Table 1). The qualitative evaluations were independently performed by two oral surgeons (Y.A. and M.S.), with findings and/or types accepted when both agreed. Result 1) Anatomical structures on non-enhanced T1WI On non-enhanced T1WI, the normal tongue was delineated as a low signal structure with nearly the same signal as the surrounding musculature, including the muscles of mastication. The Table 1 Qualitative classification of fat suppressed enhanced MRI 22 Bulletin of the Osaka Medical College 49 1, , 2003

3 Fat Suppressed MRI of the Normal Tongue 23 portion corresponding to the intrinsic tongue musculature was composed of a symmetrical high signal area (HSA) and a surrounding low signal area (LSA) in all cases. There were no cases in which the intrinsic tongue musculature could be identified. In the center of the tongue, a high signal linear structure was clearly delineated in 20 tongues. At the premolar level, the symmetrical intermediate to high signal intensity structures corresponding to the sublingual gland were able to be identified between the genioglossus muscles and mandibular body in all cases except one case. In contrast, the mucosal surface of the dorsum tongue was identified in only 5 cases. 2) Anatomical structures on fat-suppressed enhanced MRI In fat-suppressed enhanced MR images, the area corresponding to the intrinsic tongue musculatures was delineated as an intermediate signal structure in many of the cases (HSA; 18 out of 27 cases, LSA; 21 out of 27 cases, respectively), though differentiation of each intrinsic tongue musculature was impossible in all of the cases. It was difficult to divide those areas into HSA and LSA, excluding 4 cases. The genioglossus muscles could be detected in 24 cases as an intermediate to low signal structure, whereas it could not be differentiated from the intrinsic tongue musculature in the remaining 3 cases. In 9 tongues, the lingual septum could not be detected as an independent structure, and in 15 of 18, the signal intensity of the lingual septum was suppressed and depicted as a low signal linear structure, while it was depicted as a high signal linear or dot-like structure in the other 3 cases. The anterior and/or lower portion of the lingual septum tended to show a high signal intensity, while the posterior portion showed a suppressed low signal intensity. The sublingual glands were delineated as symmetrical enhanced structures, and their signal intensities showed an equal high signal intensity as compared to the surrounding structures, including the intrinsic tongue musculatures and genioglossus muscle. The mucosal surface of the tongue, especially, the dorsum surface, was enhanced strongly and more easily depicted than the ventral surface. Differentiation between the dorsum tongue mucosa and palatal mucosa was difficult in cases where an air space were absent between those two structures (Figure 1,2, Table 2). 3) Comparison between fat-suppressed enhanced scans and non-enhanced T1WI Differentiation between the HSA and LSA was quite difficult to obtain on fat-suppressed enhanced scans as compared to non-enhanced T1WI (p<0.05). Conversely, the lingual mucosa was well visualized on fat-suppressed scans as compared to non-enhanced T1WI (p<0.05). Other Table 2 Signal intensity on fat suppressed enhanced MRI Bulletin of the Osaka Medical College 49 1, ,

24 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI Fig. 1 Plain T1WI and fat suppressed enhanced image (coronal scan) Left: Non-enhanced T1WI, Right: fat-suppressed enhanced MRI.

The HSA of the intrinsic tongue musculature was also suppressed, and showed rather low signals as compared to the LSA. Fig. 2 Plain T1WI and fat-suppressed enhanced image (axial scan).

4 24 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI Fig. 1 Plain T1WI and fat suppressed enhanced image (coronal scan) Left: Non-enhanced T1WI, Right: fat-suppressed enhanced MRI. The signal from the lingual septum is apparently suppressed and shows a low signal linear structure at the center of the tongue (arrow). The HSA of the intrinsic tongue musculature was also suppressed, and showed rather low signals as compared to the LSA. Fig. 2 Plain T1WI and fat-suppressed enhanced image (axial scan). Left: Non-enhanced T1WI, Right: fat-suppressed enhanced image. The signal intensity of the lingual septum is apparently suppressed, however, the low signal linear structure cannot be detected in the fat-suppressed enhanced image. 24 Bulletin of the Osaka Medical College 49 1, , 2003

5 Fat Suppressed MRI of the Normal Tongue 25 Table 3 Detection of anatomical structures on precontrast T1WI and fat suppressed enhanced MRI structures, including the lingual septum, sublingual glands, and genioglossus muscle, showed the same degree of detectability with each type of scans (Table 3). Discussion Diagnostic imaging modalities of lesions in the oral and maxillofacial region include computed tomography (CT), ultrasound and MRI. We routinely use MRI for diagnosis of oral malignancies including tongue squamous cell carcinoma, which is the most prevalent malignant process in the oral cavity. For evaluation of these lesions, it is essential to clarify the normal anatomical structures of the tongue on MRI, using conventional T1WI and T2WI, as well as fat-suppressed enhanced scans. Sigal et al. (1996) demonstrated the normal appearance of the oral cavity using CT and MRI, and pointed out that 2 different groups of muscles were discriminated in this area by T1WI, based on their differing fat content. In addition, signal intensities in the muscles of the tongue may change from low to high, because of their variable fat content. In the present study, though each intrinsic tongue musculature could not be clearly identified, the area corresponding to the intrinsic tongue muscles was composed of a range of signals, from a relatively low signal area (LSA) to a symmetrical high signal area (HSA) on nonenhanced images. On the fat-suppressed images, except for 4 cases, the HSA could not be detected as a high signal area, however, was delineated as an intermediate or low signal that was difficult to differentiate from the LSA. That is, the signal intensity of the HSA was suppressed in fat-suppressed images indicating that its intensity was correlated to included fat tissue. In both types of sequences, the intrinsic tongue musculature could not be identified, therefore the HSA and LSA could not be used to show anatomical landmarks on fat-suppressed enhanced scans, which contrasted with non-enhanced T1WI. This result suggests that, when diagnosing the mass lesion in the tongue, T1WI is needed to understand the anatomical structure and fat-suppressed enhanced scan is needed to good contrast between the tumor and the normal portion of the tongue. Anatomically, the tongue is composed of a fibrous skeleton and a complex musculature, with the lingual septum one of fibrous skeletons portions that may contain fibrocartilage (SIGAL et al., 1996). On the other hands, Hermans et al. (1996) reported the lingual septum as a fatty space. The fibrous lingual septum is well-defined on CT scans as a midline low-density plane (MLDP) separating the paired genioglossus muscles and geniohyoid muscles into 2 symmetrical bundles, and as such is Bulletin of the Osaka Medical College 49 1, ,

6 26 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI an anatomical landmark, as is the lateral low-density plane (LLDP), which can be detected between the mylohyoid and hyoglossus muscles posteriorly and the mylohyoid and genioglossus muscles anteriorly. These landmarks can be used when diagnosing tumor extension (LARSSON et al., 1982). With MRI, the lingual septum, which is located in the center of the tongue, is depicted as a high signal linear structure on both T1WI and T2WI and is also one of the anatomical landmarks that is displaced when a large mass lesion is presented (LUFKIN et al., 1991). In fat suppressed enhanced MRI of the present study, in 15 of 18 cases in whom the lingual septum could be detected, it was shown as a low signal structure. In the other 3 tongues, the lingual septum was delineated as a high signal linear structure, while the subcutaneous fat tissue tended to show a heterogeneous high signal intensity that suggested an imperfect suppression of the fat signal. In some cases, the lingual septum was demonstrated as a high signal linear structure at the level of the premolar region, however, with a triangular shaped suppressed low signal structure in the more posterior region. Keller et al. (1987) pointed out that the chief detracting feature of chemical shift imaging lies in its dependence on magnet homogeneity. Further, Tien et al. (1991) noted disadvantages of the fat suppression technique, such as areas of incomplete fat suppression due to field inhomogeneities induced when using a large field of view. Since the lingual septum is thin in the anterior portion as compared to the posterior (SIGAL et al., 1996), the anterior part of the tongue has more possibility of movement during the examination, and it tends to affect susceptibility artifact that induced from dental prostheses, these induced the imperfect fat suppression of the anterior thin portion. For evaluation using the fat-suppressed scans, we suggest that estimation of corresponding subcutaneous fat, as well as that in the triangular posterior portion of the lingual septum be performed, to determine whether the signal intensity in those areas is suppressed. According to these considerations, our results suggest that the signal intensity of the lingual septum on MRI reflect the signal intensity of fatty tissue including in the lingual septum. The sublingual glands appear on T1WI as an area of intermediate signal intensity that is lower than that of surrounding fat tissues and higher than that of the muscles (SUMI et al., 1999). In the present study, the sublingual gland was detected in all but one case, and depicted as an Fig. 3 Schema of coronal scans at the level of molar region Left: Non-enhanced T1WI, Right: fat-suppressed enhanced MRI. 1: HSA of intrinsic tongue musculature, 2: LSA of intrinsic tongue musculature, 3: lingual septum, 4: sublingual gland, 5: genioglossus muscle, 6: lingual mucosa (dorsum surface) Each image demonstrates the lingual septum, sublingual gland, genioglossus muscle, and dorsum surface of lingual mucosa. Although differentiation of HSA and LSA was feasible on non-enhanced scans, it was difficult using fat-suppressed contrast enhanced images. Both types were able to delineate the lingual septum, though the level of brightness was contrasted between them. 26 Bulletin of the Osaka Medical College 49 1, , 2003

7 Fat Suppressed MRI of the Normal Tongue 27 intermediate to high signal intensity on pre-contrast T1WI. Sigal et al. (1996) reported that it is difficult to distinguish tumor enhancement from physiologic uptake in the salivary gland using a fat suppression sequence. In our study, the sublingual glands could be detected in 24 of the 27 cases using fat-suppressed enhanced scans, while the sublingual gland was presented as a symmetrical structure that showed a high to intermediate signal intensity and the bilateral glands were enhanced nearly equally. In the remaining 3 cases, detection of the sublingual gland was rather difficult, because there were only few contrasts between the enhanced intrinsic tongue musculature and sublingual glands and, though the sublingual glands were enhanced, the signal intensity of fat tissue in those spaces was suppressed. As a result, contrast between the sublingual glands and surrounding muscles were obscured. For evaluating these glands in a clinical situation, it is important to determine not only the signal intensity and degree of enhancement, but also morphological features. Recently, Tetsumura et al. (2001) reported in an in vitro study that high-resolution MRI could clearly demonstrate the mucosal epithelium, lamina propria, and muscles of the tongue. They also noted that for detecting these structures in vivo, it was necessary to use intra-oral surface coils and to develop a faster MR technique. In the present study, the lingual mucosa, especially the dorsum surface, was depicted as a highly enhanced single layered structure, though such enhancement of normal mucosa may obscure T1 and/or superficial tumors. Escott et al. (1997) pointed out that the first and second passes in dynamic contrast enhanced gradient echo studies best showed the lesion extent, because of increased lesion visibility with respect to background mucosa. In the present fat-suppressed enhanced scans, the dorsum surface of the lingual mucosa could not be detected in 3 cases, because the lingual and palatal mucosas were in contact. For visualizing the lingual mucosa in those situations, it is necessary to first fit the subject with a spacer made from material that shows no signal on MRI. Our results indicated that pre-contrast T1WI and fat-suppressed enhanced scans have nearly equal potential to delineate the normal structures of the tongue. However, those structures depicted in fat-suppressed enhanced scans are simple and, in some cases, visualization of the lingual septum and genioglossus muscle as well as differentiation between the HSA and LSA are difficult (Figure 3). Accordingly, we consider that both of non enhanced T1WI and fat-suppressed enhanced scans should be performed to diagnose the lesion located in the tongue. References ARIYOSHI Y, SHIMAHARA M: Determining whether a parotid tumor is in a superficial or deep lobe using magnetic resonance imaging. J Oral Maxillofac Surg. 56: 23-26, 1998 ARIYOSHI Y, SHIMAHARA M: Magnetic resonance imaging of maxillary cancer -Possibility of detecting bone destruction. Oral Oncol 36: , 2000 ARIYOSHI Y, SHIMAHARA M: Magnetic resonance imaging of a submental dermoid cyst: report of a case. J Oral Maxillofac Surg.61: , 2003 ESCOTT EJ, RAO VM, KO WD, GUITIERREZ JE: Comparison of dynamic contrast-enhanced gradient-echo and spin echo sequences in MR of head and neck neoplasms. AJNR Am J Neuroradiol 18: , 1997 HASSE A, FRAHM J, HANICKE W, MATTHAEI D: 1H NMR chemical shift selective (CHESS) imaging Phys. Med. Biol. 30: , 1985 HERMANS R, LENZ M: Imaging of the oropharynx and oral cavity Part 1: Normal anatomy. Eur. Radiol. 6: , 1996 KELLER PJ, HUNTER WW Jr, SCHMALBROCK P: Multisection fat-water imaging with chemical shift selective presaturation. Radiology 164: , 1987 LARSSON SG., MANCUSO A, HANAFEE W: Computed tomography of the tongue and floor of the mouth. Radiology 143: , 1982 LENZ M, GREESS H, DOBRITZ M, KERSTING-SOMMER- HOFF B: Methods: MRT Eur J Radiol. 33: , 2000 LENZ M, GREESS H, BAUM U., DOBRITZ M., KERST- ING-SOMMERHOFF B: Oropharynx, oral cavity, floor of the mouth: CT and MRI. Eur J Radiol 33: , 2000 LUFKIN RB, HANAFEE WN: The Raven MRI Teaching File. MRI of the head and neck. Raven Press, New York, , 1991 SIGAL R., ZAGDANSKI AM, SCHWAAB G, BOSQ J: AUPERIN A, LAPLANCHE A., et al.: CT and MRI imaging of squamous cell carcinoma of the tongue and floor of the mouth. Radiographics 16: , 1996 SUMI M, IZUMI M, YONETSU K, NAKAMURA T: Sublingual Gland: MR features of normal and diseased states. AJR Am J Rentogenol. 172: , Bulletin of the Osaka Medical College 49 1, ,

8 28 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI 1999 SZUMOWSKI J, SIMON JH: Fat and water signal separation methods. In: Magnetic resonance imaging volume 1. ed by Stark DD., Bradley WG Jr. Mosby, St Louis, , 1999 TETSUMURA A., YOSHINO N., AMAGASA T, NAGUMO K, OKADA N, SASAKI T: High-resolution magnetic resonance imaging of squamous cell carcinoma of the tongue: an in vitro study. Dentomaxilofac Radiol 30: 14-21, 2001 TIEN RD, HESSELINK JR, CHU PK, SZUMOWSKI J: Improved detection and delineation of head and neck lesions with fat suppression spin-echo MR imaging. AJNR Am J Neuroradiol 12: 19-24, 1991 Received 1 December, 2003 Accepted 27 February, Bulletin of the Osaka Medical College 49 1, , 2003

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