|Year : 2017 | Volume
| Issue : 3 | Page : 508-513
Magnetic resonance imaging: A predictor of pathological tumor dimensions in carcinoma of anterior two-thirds of tongue – A prospective evaluation
Sandya Chirukandath Jayasankaran1, Prameela Govindalayathil Chelakkot2, Milind Karippaliyil1, Krishnakumar Thankappan3, Subramaniya Iyer3, Srikanth Moorthy1
1 Department of Radiology, Amrita Institute of Medical Sciences, Amrita University, Kochi, Kerala, India
2 Department of Radiation Oncology, Amrita Institute of Medical Sciences, Amrita University, Kochi, Kerala, India
3 Department of Head and Neck Surgery, Amrita Institute of Medical Sciences, Amrita University, Kochi, Kerala, India
|Date of Web Publication||24-May-2018|
Dr. Prameela Govindalayathil Chelakkot
Department of Radiation Oncology, Amrita Institute of Medical Sciences, Amrita University, Kochi, Kerala
Source of Support: None, Conflict of Interest: None
INTRODUCTION: Preoperative imaging is mandatory for deciding the extent of surgery in tumors of oral tongue. Previous studies have shown the significance of depth of tumor invasion in predicting nodal involvement. AIM: This prospective study aimed to assess the correlation between tumor dimensions in all three planes obtained through preoperative imaging and histopathological findings, as well as the correlation between these and pathological node positivity. MATERIALS AND METHODS: Fifty-nine consecutive patients with nonmetastatic, operable, squamous cell carcinoma of anterior two-thirds of the tongue were included in the study. Preoperative imaging findings were compared with pathological findings and analyzed. RESULTS: Histopathological dimensions were concordant with imaging findings. Anteroposterior, transverse, and craniocaudal (CC) dimensions obtained through imaging showed a significant correlation with corresponding pathological findings (0.730, 0.621, 0.810, respectively; P < 0.001). Among all three, only CC dimension showed a significant correlation with pathological nodal involvement (odds ratio [OR] = 7.875, P = 0.03, relative risk = 0.236). Pathological tumor thickness of >3 mm had a positive predictive value of 54.9% for nodal involvement (OR = 7.875, P = 0.03). CONCLUSION: With widespread availability of state-of-the-art magnetic resonance (MR) scanners, CC dimension needs to be emphasized as the most significant prognostic tumor parameter. Recent evidence, including our study, suggests that MR imaging is concordant with pathological findings, justifying its use in the pretreatment evaluation of oral tongue lesions.
Keywords: Depth of tumor invasion, extrinsic muscle invasion, magnetic resonance imaging, paralingual space, squamous cell carcinoma of anterior two-thirds of tongue, sublingual space
|How to cite this article:|
Jayasankaran SC, Chelakkot PG, Karippaliyil M, Thankappan K, Iyer S, Moorthy S. Magnetic resonance imaging: A predictor of pathological tumor dimensions in carcinoma of anterior two-thirds of tongue – A prospective evaluation. Indian J Cancer 2017;54:508-13
|How to cite this URL:|
Jayasankaran SC, Chelakkot PG, Karippaliyil M, Thankappan K, Iyer S, Moorthy S. Magnetic resonance imaging: A predictor of pathological tumor dimensions in carcinoma of anterior two-thirds of tongue – A prospective evaluation. Indian J Cancer [serial online] 2017 [cited 2020 Sep 28];54:508-13. Available from: http://www.indianjcancer.com/text.asp?2017/54/3/508/233146
| » Introduction|| |
Head and neck malignancies are the fifth most common  cancers worldwide and include a variety of sites. Among these, oral cancers have a higher incidence, being the 12th most common globally and 8th in developing countries. Almost 90% of head and neck tumors have a squamous histology. The prevalence of squamous cell carcinoma of oral cavity is higher in the Indian subcontinent, mostly attributed to tobacco chewing, either alone or in combination with lime and betel nuts, along with consumption of ethanol. Five-year survival rate for early cancers of oral cavity is 68%, falling to 27% in advanced tumors. Distant metastasis ranges from 7 to 23% in head and neck squamous cell carcinoma and is 9.2% for N2 nodal status and 20% for a stage IV disease.
Most cancers of oral cavity, including anterior two-thirds of tongue, require a multidisciplinary approach, and surgery remains the cornerstone in the management. Preoperative staging evaluation is mandatory to assess extent of primary disease and nodal involvement, which in turn helps in determining the extent of surgery. The American Joint Committee on Cancer staging system (AJCC-7th edition-2010), which is based on maximum dimensions of the tumor, has been in use for staging lesions of oral cavity. Recent studies have, however, stressed the importance of tumor depth in tumors of tongue and other subsites as a predictor of nodal involvement, local recurrence, and overall survival. Tumor thickness ≤3 mm is predicted to have 0% chance of local recurrence and 8% chance of nodal involvement. Jung et al. suggested the need for evaluating the depth of invasion before making a clear surgical plan, especially in early carcinoma of tongue. The 8th revised edition of AJCC has incorporated depth as criteria in staging of tumors of anterior two-thirds of tongue.,
Imaging in oncological practice has evolved from the earlier X-rays and panoramic views through ultrasonography to computerized axial tomography (CT), magnetic resonance imaging (MRI), and positron emission tomography. Ng et al. reported sensitivity of CT and MRI in the detection of metastases to lymph nodes in head and neck tumors as 36–94% and the specificity as 50–98%. Sigal et al. (1996) have shown the usefulness of both CT and MRI in evaluating tumors of the tongue  and the possible advantages of MRI over CT in delineation of primary tumors of tongue., Correlation between the imaging and histopathological findings has been looked into in various studies, though most of them included multiple subsites  and had small patient samples. A prospective study from North India by Goel et al., for lesions of oral cavity, showed a good correlation between the two, though the number of cases in each subsite was small. Lam et al. predicted an overall accuracy of 83% and 56% for MRI (contrast-enhanced T1- and T2-weighted images) in their study of 18 patients with tumors of oral tongue.
This prospective study done in a tertiary cancer care center focused on patients with carcinoma of the anterior two-thirds of tongue. The study aimed to analyze the correlation between tumor parameters assessed through preoperative imaging and postoperative histopathological findings, including the probability of nodal involvement, in this subset, after necessary clearance from the Institutional Scientific Review Board and Institutional Ethical Committees.
| » Materials and Methods|| |
All consecutive biopsy-confirmed cases of squamous cell carcinoma of anterior two-thirds of tongue, who had presented to this tertiary cancer care center in South India and who were planned for primary surgery followed by adjuvant treatment between August 2014 and June 2016 were included in the study. Clearance from the Institutional Scientific Review Board and Institutional Ethical Committee was obtained before the study. The following were the exclusion criteria for accrual to the study: (a) inoperable disease, (b) prior treatment with neo-adjuvant chemotherapy, (c) metastatic disease, (d) recurrent disease, (e) earlier treatment with surgery or radiation for a head and neck malignancy, (f) patients planned for palliative treatment, (g) patients who refused surgery and (h) those who had medical contraindications for embarking on a curative intent treatment.
After initial biopsy confirmation and clinical evaluation by the head and neck oncology team, patients were imaged with 3 Tesla MRI system (GE) using 8-channel head and neck coil. Imaging was done after the postbiopsy inflammatory changes had subsided, which ranged from 7 to 10 days. Interval between imaging and surgery was kept as short as feasible and was always less than a week, for accurate assessment. T1-weighted spin echo (short time to echo/repetition time [TE/TR] with slice thickness of 4 mm with no interslice gap) in coronal plane was taken. T2 sequences (long TE/TR with slice thickness of 4 mm and no interslice gap) were taken in axial, sagittal, and coronal planes. T2-weighted sequence with fat saturation was acquired in coronal plane. Three-dimensional (3D) T1-weighted sequences with fat suppression in axial plane were used to acquire the postcontrast images, which were reformatted in sagittal and coronal planes. Planes for reformatting were with reference to the midline septum of the tongue and with a slice thickness of 0.37 mm. Contrast used was gadodiamide (Omniscan GE), which was administered intravenously at a rate of 1.5 cc/s to a maximum dose of 12 cc using mechanical injector, and the images were acquired immediately after completion of contrast injection.
Maximum tumor dimensions were measured in all three planes in contrast-enhanced 3D T1-weighted sequence. The length of the horizontal line connecting the two perpendicular lines, drawn at the anterior and posterior tumor-mucosal junction, in the axial 3D image was considered as the anteroposterior (AP) dimension [Figure 1]. Both transverse and craniocaudal (CC) dimensions were measured in the coronal reformat which has a slice thickness of 0.37 mm. The maximum distance between two horizontal lines drawn at superior and inferior tumor-mucosal junction, in the coronal reformat, was taken as the CC dimension [Figure 2]. Two horizontal lines were drawn on either side (medial and lateral) of the perpendicular line connecting the superior and inferior tumor-mucosal junctions to the point of maximum tumor projection. The sum of these two was taken as the transverse dimension [Figure 3]. Level of normal mucosa was taken as the upper limit of the tumor dimension, both for exophytic and ulcerative lesions.
|Figure 1: Anteroposterior dimension: Axial three-dimensional image. Two perpendicular lines “a” and “b” drawn are the anterior and posterior tumor-mucosal junction, respectively. The length of the horizontal line “c” connecting these two perpendicular lines is considered as anteroposterior dimension|
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|Figure 2: Transverse dimension: Postcontrast T1-weighted image (coronal reformat). Two horizontal lines, “a,” “b,” were drawn on the superior and inferior tumor-mucosal junctions. A line “c” is drawn perpendicular to lines “a” and “b” through the middle of the tumor. Lines “d” and “e” are drawn on either side of line “c” (medial and lateral) to the point of maximum tumor projection. The sum of these lines, “d” and “e” gives the transverse dimension|
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|Figure 3: Craniocaudal dimension: Postcontrast T1-weighted image (Coronal reformat). Two horizontal lines, “a,” “b,” were drawn on the superior and inferior tumor-mucosal junctions. A line “c” is drawn perpendicular to lines “a” and “b” through the middle of the tumor. The length of this line “c” represents the craniocaudal dimensions|
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Other tumor parameters assessed included infiltration of sublingual space and infiltration of extrinsic muscles of tongue, namely, genioglossus, hyoglossus, and styloglossus, as well as the involvement of mylohyoid. Sublingual space is defined as the space superomedial to mylohyoid muscle and lateral to geniohyoid and genioglossus muscles. Involvement of sublingual space and extrinsic muscles was subjective through visual assessment [Figure 4].
|Figure 4: Muscle invasion. Coronal T2-weighted image. Shows muscle invasion by the tumor. G = Genioglossus, H = Hyoglossus, S = Styloglossus, and M = Mylohyoid. Tumor on the right side shows invasion of all muscles except mylohyoid|
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After appropriate staging workup, all patients were taken up for surgery, which most often was a wide local excision, with adequate margins, which is conventionally 1 cm beyond the palpable induration of the lesion. Ipsilateral or bilateral, selective, or modified neck dissection was also done based on the tumor stage. The excised specimens were analyzed by dedicated head and neck pathology team. The specimen after orienting appropriately, and inking of raw surface, is cut usually in the CC plane. Tumor dimensions are assessed in all three planes. Depth of the tumor is considered as the CC extent from the level of the superior normal mucosa to the maximum depth. Pathology reporting adheres to the international guidelines.
Details of demographics, tumor characteristics, imaging parameters, and histopathological details were tabulated and statistically analyzed. The imaging parameters were compared with the histopathological details. SPSS (Statistical Package for Social Sciences version 20.0 – IBM) was used for statistical analysis. Tools such as Chi-square test and Pearson's correlation coefficient were used to assess correlation between imaging and final histopathology findings, and the correlation factor for each parameter was determined. For each dimension, the positive predictive value (PPV) for nodal involvement was calculated after taking serial cutoffs from 3 to 7 mm. The relative risk and odds ratio (OR) for pathological nodal involvement were calculated for each of the 3D acquired through imaging using Chi-square test for cutoff value from 3 to 7 mm.
| » Results|| |
During the study period, a total of 88 cases of malignancies of the anterior two-thirds of tongue had presented to the institution, of which 59 patients were eligible for inclusion in the study. Mean age at presentation was 51.81 years (range: 18–74 years), with a male preponderance of 71.2%.
Left and right lateral tumors were almost equally represented. Of the 59, 3 (5.08%) had lesions crossing the midline. Sublingual space invasion was noted in 35.6%. Among the extrinsic muscles of tongue, hyoglossus infiltration was present in 81.4%, genioglossus in 20.3%, and styloglossus in 69.5%. Mylohyoid invasion was observed in 6.8% of patients. Only eight patients (13.6%) had very superficial lesions not infiltrating any muscles.
Surgery done was wide local excision in 91.5%, while 5.1% had hemiglossectomy and 3.4% had total glossectomy. All patients underwent ipsilateral neck dissection; selective neck dissection in 58 (98.3%) and modified radical dissection in one. Up to level IV, dissection was carried out in 93.2% of patients and 6.8% had dissection up to level III. Contralateral neck dissection was done in 15.3%; up to level II was done in 13.6% and level III in 1.7%. The patient characteristics are tabulated in [Table 1].
The dimensions observed after histopathological examinations were concordant with the imaging findings through statistical analysis using Pearson's two-tailed correlation. All three dimensions obtained thorough imaging showed a significant concordance with final histopathological dimensions; the correlation coefficient for CC dimension obtained through imaging and from histopathology was 0.810 (P < 0.001), while AP was 0.730 (P < 0.001) and transverse was 0.621 (P < 0.001). Details of imaging and histopathology parameters are represented in [Table 2]. Due to fewer patients with small tumors, OR could be obtained only for a cutoff value of 6 mm in AP, 5 mm in transverse, and 8 mm for CC dimensions. The OR was 0.900 (P = 0.94 for two-tailed and 0.74 for one-tailed) for AP, 6.480 (P = 0.06 for both two-tailed and one-tailed) for transverse, and 7.875 (P = 0.03 for both two-tailed and one-tailed) for CC dimensions. Only CC dimension among all the three showed a significant correlation with pathological nodal involvement. The relative risk of pathological nodal involvement for these cutoffs was 1.056, 0.275, and 0.236, respectively.
|Table 2: Comparison of tumor dimensions - magnetic resonance imaging versus histopathology|
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Interestingly, no significant correlation was obtained between infiltration of extrinsic muscles taken together or separately as inferred from imaging and the pathological nodal status or pathological stage [Table 3] and [Figure 5]. Among the 51 patients with muscle invasion, 28 had nodal involvement (N1-14, N2-14); and one of the eight with no muscle invasion had N1 nodal status. Imaging showed sublingual space extension in 35.6% of patients, though no significant correlation was obtained between the sublingual space extension and pathological nodal status.
|Table 3: Correlation between invasion of muscles in magnetic resonance imaging and pathological nodal status|
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|Figure 5: Graphical representation of nodal involvement without and with muscle invasion for different extrinsic muscles. (a) Genioglossus, (b) hyoglossus, (c) styloglossus, (d) mylohyoid|
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| » Discussion|| |
Like in any other solid malignancy, accurate pretreatment delineation of lesions is mandatory for head and neck tumors; for correct staging, planning appropriate treatment options, and prognostication. Imaging modalities are used for better understanding of tumor dimensions and infiltration of adjacent structures. Although both CT and MRI have been in use, recent studies have found MRI to be superior in assessing tumor extent  and is considered the imaging of choice for oral tongue lesions due to its excellent soft tissue contrast that helps in accurately differentiating tumor from adjacent normal structures.
AJCC tumor, node, and metastasis (TNM) staging system is used universally for staging tumors of head and neck, including anterior two-thirds of tongue. The limitations in TNM staging have been widely criticized, especially in view of recent evidences suggesting depth of the tumor to be predictive of nodal involvement. The recent AJCC has rectified this by adding tumor thickness as one of the parameters in staging. T1–T3 tumors are classified as <2, 2–4, and >4 cm in maximum dimension, and infiltration of extrinsic or deep muscles of tongue qualifies it a T4. The term “deep” remains vague and ambiguous, with infiltration of genioglossus, hyoglossus, palatoglossus, and/or styloglossus all being staged as T4, making it a heterogenous collection of lesions. These muscles are not exactly deep and the measure of depth in relation to these extrinsic muscles from the mucosa is unspecified. Researchers have implicated various factors including an array of molecular markers as having prognostic significance in oral squamous cell carcinoma. The tumor-related parameters assessed through imaging and believed to influence overall survival, local recurrence, and in turn the prognosis, are depth of invasion,, infiltration of muscles,, and sublingual and paralingual space extension.
Depth of invasion of tumor
Moore et al. (1986) reported the significance of tumor thickness in predicting survival, in their retrospective analysis of 151 patients of aerodigestive tract, and the definition of depth of tumor invasion proposed by Moore has been widely accepted. Tumor thickness as obtained by the coronal T2-weighted MRI was found to be significantly correlated to the cervical nodal metastases (P = 0.05) in the 43 patients studied by Okura et al., who suggested the need for actively addressing neck when the thickness of the tumor was >9.7 mm. A meta-analysis of 16 studies pooling data of 1136 patients of squamous cell carcinoma of the oral cavity published by Huang et al. from Princess Margaret Hospital in 2009 suggested tumor thickness of 4 mm as the cutoff for predicting lymph nodal involvement (P = 0.007). Bier-Laning had looked into contralateral neck nodal involvement in T1- and T2-tongue cancers and suggested that if tumor thickness was ≤3.75 mm, contralateral neck can be kept under close observation, while active intervention is indicated if the tumor thickness was ≥9.75 mm. Similar observations emphasizing the significance of pathological tumor thickness were given by other authors as well., These studies have convincingly stressed the need for assessing tumor thickness before definitive surgery and in planning surgical extent.
It needs to be emphasized that there had been no consensus in the measurement of tumor thickness among the different studies as has been clearly discussed by Gonzalez-Moles et al. (2002). They finally opined that the maximum resistance for a tumor growth is in the vertical (CC) direction and not in the superficial transverse plane. Hence, an aggressive tumor logically has to be the one with higher vertical involvement. Lydiatt et al. in AJCC 8th edition have mentioned the discrepancy between the “tumor thickness” and “depth of invasion.” In histopathological evaluations, the CC dimension measured as distance between the maximum tumor depth and an imaginary line at the level of mucosa is considered as the depth of invasion, in tumors of the anterior two-thirds of tongue. In our analysis, we found that of the three dimensions, CC showed a significant correlation with pathological nodal involvement, with an OR of 7.875 (P = 0.03) and relative risk of 0.236. Our analysis showed that, pathological tumor thickness >3 mm had a PPV of 54.9% for nodal involvement, while a cutoff of 4 mm had a PPV of 58.3%. An OR of 7.875 (P = 0.033 [two-tailed] and 0.037 [one-tailed]) was obtained for a cutoff value of 3 mm for pathological CC thickness and a relative risk of 0.236 for node positivity. The recent AJCC modification has suggested the need to identify the horizontal line at the level of the basement membrane in relation to the closest intact squamous mucosa, which has been termed as the “horizon,” and to measure the depth of invasion by dropping a “plumb line” from the horizon.
Our analysis also showed that MRI is a reliable tool in assessing the depth of invasion of tumor and has a significant correlation with the final histopathological findings, as has been shown by earlier studies., In our experience, a postcontrast T1-weighted image with fat saturation was a better sequence in delineating the tumor dimensions, as was observed by Yasumoto et al. (1995) and later by other authors.,,
“Deep” muscle invasion by tumor
Invasion of extrinsic muscles as a predictor of nodal involvement has been looked into by Chandler et al., in their retrospective histopathological study, which concluded that muscle infiltration can be considered as a surrogate for nodal involvement. Among their 61 cases, 43 had muscle invasion, of which only 10 had positive nodes, resulting in a PPV of 23.3%. Conversely, depth of invasion using a cutoff of 3 mm had a PPV of 29.3% in Chandler's study, while in this study was 54.9%. Mani et al. had concluded that extrinsic muscle infiltration was the only significant predictor of recurrence in squamous cell carcinoma of oral tongue, from their retrospective analysis of 41 patients. Of these 41, eight patients had recurrence, among which only three had muscle invasion, which is a too small sample for generalization. Boland et al. opined that classification of a lateral tumor, as T4a based on extension to styloglossus and hyoglossus, did not carry any clinical significance. They also commented that extension to genioglossus did not predict occult cervical nodal metastasis or poor disease-related survival.
Extrinsic muscle invasion was noted in 51 patients in our study, of whom 28 had pathologically positive nodes, giving a PPV of 54.9%. Despite this, our analysis failed to document any significant correlation between invasions of any of the extrinsic muscles, as observed in the imaging, and the pathological nodal status, as compared to CC dimension. As the tumor invades deeper structures, anatomical boundaries are disrupted and will lead to infiltration of extrinsic muscles of tongue. Hence, the PPV of muscle invasion noted would probably reflect the depth of tumor invasion rather than that of extrinsic muscle invasion as depicted by the CC dimension.
Paralingual and sublingual space invasion by tumor
Sublingual space extension denotes extension to the floor of mouth and is a radiological finding which is not discernable in the pathological specimen. Sublingual space extension did not show any correlation with nodal involvement as was observed by Okura et al. who opined that sublingual space distance is not a predictor of nodal involvement. It is still premature to comment on this as only further follow-up of these patients and detailed analysis of the survival can validate these assumptions.
Concept of paralingual space was revived by Okura et al. Paralingual space corresponds to the paramedian septum described by Abd-El-Malek in 1939. They opined that invasion to paralingual space and then to genioglossus muscle, one of the extrinsic muscles qualifying a T4 tumor, as assessed through MRI increased the incidence of nodal involvement. Further studies are required to assess the prognostic significance of extrinsic muscle, paralingual space, and sublingual space infiltrations, which in turn might provide better understanding of the tumor and may clarify the present staging parameters.
| » Conclusion|| |
With the widespread availability of the state-of-the-art MR scanners, inclusion of CC dimension, evidently one of the most significant dimensions among the tumor parameters, as a prognostic marker in the staging protocol, as suggested by AJCC 8th edition is very much required. Significance of putative prognostic parameters such as infiltration of “deep” muscles and paralingual and sublingual spaces needs to be further validated through prospective studies with larger samples. Our study convincingly suggests that tumor parameters assessed through MRI are concordant with the pathological findings and justify its use in pretreatment evaluation of squamous cell carcinoma of anterior two-thirds of tongue.
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| » References|| |
Quintero K, Giraldo GA, Uribe ML, Baena A, Lopez C, Alvarez E, et al.
Human papillomavirus types in cases of squamous cell carcinoma of head and neck in colombia. Braz J Otorhinolaryngol 2013;79:375-81.
Goel V, Parihar PS, Parihar A, Goel AK, Waghwani K, Gupta R, et al.
Accuracy of MRI in prediction of tumour thickness and nodal stage in oral tongue and gingivobuccal cancer with clinical correlation and staging. J Clin Diagn Res 2016;10:TC01-5.
Delantoni A. Magnetic resonance imaging staging of tongue cancer: Correlation of radiographic measurements to pathology. J Cancer Treat Res 2015;3:66-75.
Prameela CG, Ravind R, Sruthi K, Nair HM, Dinesh M. Surgical resection of solitary distant metastasis from locoregionally controlled advanced hypopharyngeal malignancy: A ray of hope. J Cancer Res Ther 2016;1-4 [Ahead of Print].
Edge SB, Compton CC. The american joint committee on cancer: The 7th
edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 2010;17:1471-4.
Jung J, Cho NH, Kim J, Choi EC, Lee SY, Byeon HK, et al.
Significant invasion depth of early oral tongue cancer originated from the lateral border to predict regional metastases and prognosis. Int J Oral Maxillofac Surg 2009;38:653-60.
Lam P, Au-Yeung KM, Cheng PW, Wei WI, Yuen AP, Trendell-Smith N, et al.
Correlating MRI and histologic tumor thickness in the assessment of oral tongue cancer. AJR Am J Roentgenol 2004;182:803-8.
Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, et al
., editors. AJCC Cancer Staging Manual. 8th
ed. Springer International Publishing, ISBN 978-3-319-40617-6:2017.
Ng SH, Yen TC, Liao CT, Chang JT, Chan SC, Ko SF, et al.
18F-FDG PET and CT/MRI in oral cavity squamous cell carcinoma: A prospective study of 124 patients with histologic correlation. J Nucl Med 2005;46:1136-43.
Sigal R, Zagdanski AM, Schwaab G, Bosq J, Auperin A, Laplanche A, et al.
CT and MR imaging of squamous cell carcinoma of the tongue and floor of the mouth. Radiographics 1996;16:787-810.
La'porte SJ, Juttla JK, Lingam RK. Imaging the floor of the mouth and the sublingual space. Radiographics 2011;31:1215-30.
Becker M, Zaidi H. Imaging in head and neck squamous cell carcinoma: The potential role of PET/MRI. Br J Radiol 2014;87:20130677.
Piazza C, Montalto N, Paderno A, Taglietti V, Nicolai P. Is it time to incorporate 'depth of infiltration' in the T staging of oral tongue and floor of mouth cancer? Curr Opin Otolaryngol Head Neck Surg 2014;22:81-9.
Clark JR, Naranjo N, Franklin JH, de Almeida J, Gullane PJ. Established prognostic variables in N0 oral carcinoma. Otolaryngol Head Neck Surg 2006;135:748-53.
Massano J, Regateiro FS, Januário G, Ferreira A. Oral squamous cell carcinoma: Review of prognostic and predictive factors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:67-76.
Chandler K, Vance C, Budnick S, Muller S. Muscle invasion in oral tongue squamous cell carcinoma as a predictor of nodal status and local recurrence: Just as effective as depth of invasion? Head Neck Pathol 2011;5:359-63.
Okura M, Iida S, Aikawa T, Adachi T, Yoshimura N, Yamada T, et al.
Tumor thickness and paralingual distance of coronal MR imaging predicts cervical node metastases in oral tongue carcinoma. AJNR Am J Neuroradiol 2008;29:45-50.
Moore C, Kuhns JG, Greenberg RA. Thickness as prognostic aid in upper aerodigestive tract cancer. Arch Surg 1986;121:1410-4.
Huang SH, Hwang D, Lockwood G, Goldstein DP, O'Sullivan B. Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: A meta-analysis of reported studies. Cancer 2009;115:1489-97.
Bier-Laning CM, Durazo-Arvizu R, Muzaffar K, Petruzzelli GJ. Primary tumor thickness as a risk factor for contralateral cervical metastases in T1/T2 oral tongue squamous cell carcinoma. Laryngoscope 2009;119:883-8.
Lodder WL, Teertstra HJ, Tan IB, Pameijer FA, Smeele LE, van Velthuysen ML, et al.
Tumour thickness in oral cancer using an intra-oral ultrasound probe. Eur Radiol 2011;21:98-106.
Gonzalez-Moles MA, Esteban F, Rodriguez-Archilla A, Ruiz-Avila I, Gonzalez-Moles S. Importance of tumour thickness measurement in prognosis of tongue cancer. Oral Oncol 2002;38:394-7.
Lydiatt WA, Patel SG, O'Sullivan B, Brandwein MS, Ridge JA, Migliacci JC, et al
. Head and neck cancers – Major changes in the AJCC 8th
edition Cancer staging manual. CA Cancer J Clin 2017;67:122-37.
Yasumoto M, Shibuya H, Takeda M, Korenaga T. Squamous cell carcinoma of the oral cavity: MR findings and value of T1-versus T2-weighted fast spin-echo images. AJR Am J Roentgenol 1995;164:981-7.
Mani C, Lakshminarayana G, Annapurneshwari KA. Predictors of recurrence in early stage oral tongue squamous cell carcinoma. J Orofac Sci 2015;7:86. [Full text]
Boland P, Pataridis K, Eley K, Golding S, Watt-Smith S. Automatic upstaging of tongue squamous cell carcinoma with lateral extrinsic muscle involvement is not justified. Int J Oral Maxillofac Surg 2013;42:1397-402.
Abd-El-Malek S. Observations on the morphology of the human tongue. J Anat 1939;73:201-10.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3]