Bulletin of the Osaka Medical College 49 1, 2 21-28, 2003 21

Original Article

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

Yasunori ARIYOSHI1), Masashi SHIMAHARA1),

Yasuo UESUGI2), Isamu NARABAYASHI2)

1) Department of Oral Surgery, Osaka Medical College 2) Department of Radiology, Osaka Medical College

Key Words : magnetic resonance imaging, fat suppression, tongue,

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 were found to be composed of a symmetrical high signal area (HSA), low signal area (LSA), lingual septum, bilateral , and genioglossus muscle on non- enhanced 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 non- enhanced scans (P<0.05). Conclusion: Fat-suppressed enhanced scans demonstrated simple anatomical structures as com- pared 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 dardized protocol for evaluating head and neck lesions, which consists of plain T1-spin echo (SE), Magnetic resonance imaging (MRI) has become plain fat-suppressed (FS) T2 turbo-spin echo (TSE), an essential modality for evaluating mass lesions in and FS-T1-TSE after Gd-DTPA. Clinically, we have the oral and maxillofacial region, and clinical utility used plain T1 weighted images (conventional or fast has also been reported (ARIYOSHI et al., 1998, 2000, spin echo; conventional T1WI or FSE-T1WI), FSE- 2003). In addition, fat-suppressed techniques have T2 weighted images (T2WI) with or without fat sup- also been used to improve lesion detectability when pression, and dynamic enhanced T1WI followed by surrounded by fatty tissue and/or to estimate fat-suppressed enhanced T1WI. However, for diag- whether the lesion includes fatty materials (LENZ et nosing lesions located in the tongue using a combina- al., 2000). Lenz et al. (2000) presented the stan- tion of these complex sequences, it is necessary to

21 22 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI clarify normal structures as revealed by each TR/TE) or FSE T1WI (400-600/8-14/2-3, sequence. Especially, T1WI showed good anatomical TR/TE/ET) and FSE-T2WI (4000/102/16-18, structure of head and neck (LENZ et al., 2000), it is TR/TE/ET), coronal and/or axial contrast important to clarify whether or not the structure enhanced fat-suppressed T1WI were obtained by which could be detected on non-enhanced T1WI simultaneous intravenous bolus injection of could also be detected on fat suppressed contrast gadopentetate dimeglumine (Magnevist, Japan- enhanced MRI. Scheling, Osaka, Japan) at 0.1 mmol /kg body In the present study, we observed delineated nor- weight. The contrast medium was injected intra- mal tongues and their surrounding structures using veneously within 15 seconds. All image slices that fat-suppressed contrast enhanced MRI and compare included the tongue were used for estimation. the results to those seen with non-enhanced T1WI. The fat-suppressed method utilized in the present study was the chemical shift selective (CHESS) Materials and methods method (HASSE et al., 1985; SZUMOWSKI et al., 1999). The study specimens were contrast enhanced 2. Images analysis fat-suppressed images of tongues from 27 patients Structures that composed the tongue and floor (mean age standard deviation = 55.3 14.2 of the were qualitatively assessed to deter- years old, male to female ratio=16:11). These mine whether those detected by non-enhanced examinations were performed to diagnose the T1WI were also detectable in fat-suppressed lesion which occurred in the oral and maxillofacial enhanced scans. For statistical analysis, a 2 test region except for the tongue and the floor of the was used for comparing the detectability of each mouth. None of the patients had lesions in the structure between the two types of scans, with tongue or floor of the mouth seen clinically and/or P<0.05 considered to be significant. In addition, radiologically, and none suffered from malignant the signal intensity of each of those structures on entities or aggressive inflammatory processes sys- fat-suppressed images were assessed and classi- temically. The images were not affected by appar- fied into 3 groups; high, intermediate, and low ent artifacts, including motion and susceptibility, (Table 1). The qualitative evaluations were inde- while tongue shape was determined to be symmet- pendently performed by two oral surgeons (Y.A. rical by viewing selected slices. and M.S.), with findings and/or types accepted The MRI scanner used was a SIGNA (General when both agreed. Electric Medical Systems, Milwaukee, WI) operat- ing at 1.5 Tesla. The head coil that had a diameter Result of 28 cm or the surface coil was used. All sequences were performed with a slice thickness 1) Anatomical structures on non-enhanced T1WI of 5.0 mm with an intersection gap of 0 to 1mm, a On non-enhanced T1WI, the normal tongue 256 x 224 imaging matrix, and a field of view of 26 was delineated as a low signal structure with near- cm. ly the same signal as the surrounding muscula- After obtaining conventional (400-500/40, ture, including the muscles of mastication. The

Table 1 Qualitative classification of fat suppressed enhanced MRI

22 Bulletin of the Osaka Medical College 49 1, 2 21-28, 2003 Fat Suppressed MRI of the Normal Tongue 23 portion corresponding to the intrinsic tongue mus- lingual septum could not be detected as an inde- culature was composed of a symmetrical high sig- pendent structure, and in 15 of 18, the signal nal area (HSA) and a surrounding low signal area intensity of the lingual septum was suppressed (LSA) in all cases. There were no cases in which and depicted as a low signal linear structure, while the intrinsic tongue musculature could be identi- it was depicted as a high signal linear or dot-like fied. In the center of the tongue, a high signal lin- structure in the other 3 cases. The anterior and/or ear structure was clearly delineated in 20 tongues. lower portion of the lingual septum tended to At the premolar level, the symmetrical intermedi- show a high signal intensity, while the posterior ate to high signal intensity structures correspond- portion showed a suppressed low signal intensity. ing to the sublingual gland were able to be identi- The sublingual glands were delineated as symmet- fied between the genioglossus muscles and rical enhanced structures, and their signal intensi- mandibular body in all cases except one case. In ties showed an equal high signal intensity as com- contrast, the mucosal surface of the dorsum pared to the surrounding structures, including the tongue was identified in only 5 cases. intrinsic tongue musculatures and genioglossus muscle. The mucosal surface of the tongue, espe- 2) Anatomical structures on fat-suppressed cially, the dorsum surface, was enhanced strongly enhanced MRI and more easily depicted than the ventral surface. In fat-suppressed enhanced MR images, the Differentiation between the dorsum tongue area corresponding to the intrinsic tongue muscu- mucosa and palatal mucosa was difficult in cases latures was delineated as an intermediate signal where an air space were absent between those structure in many of the cases (HSA; 18 out of 27 two structures (Figure 1,2, Table 2). cases, LSA; 21 out of 27 cases, respectively), though differentiation of each intrinsic tongue 3) Comparison between fat-suppressed enhanced musculature was impossible in all of the cases. It scans and non-enhanced T1WI was difficult to divide those areas into HSA and Differentiation between the HSA and LSA was LSA, excluding 4 cases. The genioglossus muscles quite difficult to obtain on fat-suppressed could be detected in 24 cases as an intermediate enhanced scans as compared to non-enhanced to low signal structure, whereas it could not be T1WI (p<0.05). Conversely, the lingual mucosa differentiated from the intrinsic tongue muscula- was well visualized on fat-suppressed scans as ture in the remaining 3 cases. In 9 tongues, the 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, 2 21-28, 2003 23 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 sup- pressed, 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, 2 21-28, 2003 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, sublin- symmetrical high signal area (HSA) on non- gual glands, and genioglossus muscle, showed the enhanced images. On the fat-suppressed images, same degree of detectability with each type of except for 4 cases, the HSA could not be detected scans (Table 3). as a high signal area, however, was delineated as an intermediate or low signal that was difficult to Discussion differentiate from the LSA. That is, the signal intensity of the HSA was suppressed in fat-sup- Diagnostic imaging modalities of lesions in the pressed images indicating that its intensity was oral and maxillofacial region include computed correlated to included fat tissue. In both types of tomography (CT), ultrasound and MRI. We rou- sequences, the intrinsic tongue musculature could tinely use MRI for diagnosis of oral malignancies not be identified, therefore the HSA and LSA including tongue squamous cell carcinoma, which could not be used to show anatomical landmarks is the most prevalent malignant process in the oral on fat-suppressed enhanced scans, which con- cavity. For evaluation of these lesions, it is essen- trasted with non-enhanced T1WI. This result sug- tial to clarify the normal anatomical structures of gests that, when diagnosing the mass lesion in the the tongue on MRI, using conventional T1WI and tongue, T1WI is needed to understand the T2WI, as well as fat-suppressed enhanced scans. anatomical structure and fat-suppressed enhanced Sigal et al. (1996) demonstrated the normal scan is needed to good contrast between the appearance of the oral cavity using CT and MRI, tumor and the normal portion of the tongue. and pointed out that 2 different groups of muscles Anatomically, the tongue is composed of a were discriminated in this area by T1WI, based on fibrous skeleton and a complex musculature, with their differing fat content. In addition, signal the lingual septum one of fibrous skeletons por- intensities in the muscles of the tongue may tions that may contain fibrocartilage (SIGAL et al., change from low to high, because of their variable 1996). On the other hands, Hermans et al. (1996) fat content. In the present study, though each reported the lingual septum as a fatty space. The intrinsic tongue musculature could not be clearly fibrous lingual septum is well-defined on CT scans identified, the area corresponding to the intrinsic as a midline low-density plane (MLDP) separating tongue muscles was composed of a range of sig- the paired genioglossus muscles and geniohyoid nals, from a relatively low signal area (LSA) to a muscles into 2 symmetrical bundles, and as such is

Bulletin of the Osaka Medical College 49 1, 2 21-28, 2003 25 26 Y. ARIYOSHI, M. SHIMAHARA, Y. UESUGI, I. NARABAYASHI an anatomical landmark, as is the lateral low-den- Further, Tien et al. (1991) noted disadvantages of sity plane (LLDP), which can be detected the fat suppression technique, such as areas of between the mylohyoid and hyoglossus muscles incomplete fat suppression due to field inhomo- posteriorly and the mylohyoid and genioglossus geneities induced when using a large field of view. muscles anteriorly. These landmarks can be used Since the lingual septum is thin in the anterior when diagnosing tumor extension (LARSSON et al., portion as compared to the posterior (SIGAL et al., 1982). With MRI, the lingual septum, which is 1996), the anterior part of the tongue has more located in the center of the tongue, is depicted as possibility of movement during the examination, a high signal linear structure on both T1WI and and it tends to affect susceptibility artifact that T2WI and is also one of the anatomical landmarks induced from dental prostheses, these induced that is displaced when a large mass lesion is pre- the imperfect fat suppression of the anterior thin sented (LUFKIN et al., 1991). In fat suppressed portion. For evaluation using the fat-suppressed enhanced MRI of the present study, in 15 of 18 scans, we suggest that estimation of correspond- cases in whom the lingual septum could be detect- ing subcutaneous fat, as well as that in the trian- ed, it was shown as a low signal structure. In the gular posterior portion of the lingual septum be other 3 tongues, the lingual septum was delineat- performed, to determine whether the signal inten- ed as a high signal linear structure, while the sub- sity in those areas is suppressed. According to cutaneous fat tissue tended to show a heteroge- these considerations, our results suggest that the neous high signal intensity that suggested an signal intensity of the lingual septum on MRI imperfect suppression of the fat signal. In some reflect the signal intensity of fatty tissue including cases, the lingual septum was demonstrated as a in the lingual septum. high signal linear structure at the level of the pre- The sublingual glands appear on T1WI as an molar region, however, with a triangular shaped area of intermediate signal intensity that is lower suppressed low signal structure in the more poste- than that of surrounding fat tissues and higher rior region. Keller et al. (1987) pointed out that than that of the muscles (SUMI et al., 1999). In the chief detracting feature of chemical shift imag- the present study, the sublingual gland was ing lies in its dependence on magnet homogeneity. 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, 2 21-28, 2003 Fat Suppressed MRI of the Normal Tongue 27 intermediate to high signal intensity on pre-con- Accordingly, we consider that both of non trast T1WI. Sigal et al. (1996) reported that it is enhanced T1WI and fat-suppressed enhanced difficult to distinguish tumor enhancement from scans should be performed to diagnose the lesion physiologic uptake in the using a fat located in the tongue. suppression sequence. In our study, the sublin- gual glands could be detected in 24 of the 27 cases References using fat-suppressed enhanced scans, while the sublingual gland was presented as a symmetrical ARIYOSHI Y, SHIMAHARA M: Determining whether a structure that showed a high to intermediate sig- parotid tumor is in a superficial or deep lobe using nal intensity and the bilateral glands were magnetic resonance imaging. J Oral Maxillofac enhanced nearly equally. In the remaining 3 Surg. 56: 23-26, 1998 cases, detection of the sublingual gland was rather ARIYOSHI Y, SHIMAHARA M: Magnetic resonance difficult, because there were only few contrasts imaging of maxillary cancer -Possibility of detect- between the enhanced intrinsic tongue muscula- ing bone destruction. Oral Oncol 36: 499-507, ture and sublingual glands and, though the sublin- 2000 gual glands were enhanced, the signal intensity of ARIYOSHI Y, SHIMAHARA M: Magnetic resonance fat tissue in those spaces was suppressed. As a imaging of a submental dermoid cyst: report of a result, contrast between the sublingual glands and case. J Oral Maxillofac Surg.61: 507-510, 2003 surrounding muscles were obscured. For evaluat- ESCOTT EJ, RAO VM, KO WD, GUITIERREZ JE: ing these glands in a clinical situation, it is impor- Comparison of dynamic contrast-enhanced gradi- tant to determine not only the signal intensity and ent-echo and spin echo sequences in MR of head degree of enhancement, but also morphological and neck neoplasms. AJNR Am J Neuroradiol 18: features. 1411-1419, 1997 Recently, Tetsumura et al. (2001) reported in HASSE A, FRAHM J, HANICKE W, MATTHAEI D: 1H an in vitro study that high-resolution MRI could NMR chemical shift selective (CHESS) imaging clearly demonstrate the mucosal epithelium, lami- Phys. Med. Biol. 30: 341-344, 1985 na propria, and muscles of the tongue. They also HERMANS R, LENZ M: Imaging of the oropharynx noted that for detecting these structures in vivo, it and oral cavity Part 1: Normal anatomy. Eur. was necessary to use intra-oral surface coils and Radiol. 6: 362-368, 1996 to develop a faster MR technique. In the present KELLER PJ, HUNTER WW Jr, SCHMALBROCK P: study, the lingual mucosa, especially the dorsum Multisection fat-water imaging with chemical shift surface, was depicted as a highly enhanced single selective presaturation. Radiology 164: 539-541, layered structure, though such enhancement of 1987 normal mucosa may obscure T1 and/or superficial LARSSON SG., MANCUSO A, HANAFEE W: Computed tumors. Escott et al. (1997) pointed out that the tomography of the tongue and floor of the mouth. first and second passes in dynamic contrast Radiology 143: 493-500, 1982 enhanced gradient echo studies best showed the LENZ M, GREESS H, DOBRITZ M, KERSTING-SOMMER- lesion extent, because of increased lesion visibility HOFF B: Methods: MRT Eur J Radiol. 33: 178-184, with respect to background mucosa. In the pre- 2000 sent fat-suppressed enhanced scans, the dorsum LENZ M, GREESS H, BAUM U., DOBRITZ M., KERST- surface of the lingual mucosa could not be detect- ING-SOMMERHOFF B: Oropharynx, oral cavity, ed in 3 cases, because the lingual and palatal floor of the mouth: CT and MRI. Eur J Radiol 33: mucosas were in contact. For visualizing the lin- 203-215, 2000 gual mucosa in those situations, it is necessary to LUFKIN RB, HANAFEE WN: The Raven MRI Teaching first fit the subject with a spacer made from mate- File. MRI of the head and neck. Raven Press, New rial that shows no signal on MRI. York, 168-171, 1991 Our results indicated that pre-contrast T1WI SIGAL R., ZAGDANSKI AM, SCHWAAB G, BOSQ J: and fat-suppressed enhanced scans have nearly AUPERIN A, LAPLANCHE A., et al.: CT and MRI equal potential to delineate the normal structures imaging of squamous cell carcinoma of the tongue of the tongue. However, those structures depicted and floor of the mouth. Radiographics 16: 787- in fat-suppressed enhanced scans are simple and, 810, 1996 in some cases, visualization of the lingual septum SUMI M, IZUMI M, YONETSU K, NAKAMURA T: and genioglossus muscle as well as differentiation Sublingual Gland: MR features of normal and dis- between the HSA and LSA are difficult (Figure 3). eased states. AJR Am J Rentogenol. 172: 717-722,

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1999 SZUMOWSKI J, SIMON JH: Fat and water signal sepa- ration methods. In: Magnetic resonance imaging volume 1. ed by Stark DD., Bradley WG Jr. Mosby, St Louis, 159-179, 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, 2004

28 Bulletin of the Osaka Medical College 49 1, 2 21-28, 2003