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Table of Contents
REVIEW ARTICLE
Year : 2021  |  Volume : 4  |  Issue : 4  |  Page : 677-683

Imaging-based T stage (iT) as a predictive and prognostic marker for outcome in T4 stage tongue carcinomas: A narrative review


1 Department of Radiodiagnosis and Imaging, Tata Memorial Hospital, Mumbai, Maharashtra, India
2 Department of Head and Neck Surgical Oncology, Tata Memorial Hospital, Mumbai, Maharashtra, India

Date of Submission03-Jun-2021
Date of Decision27-Jul-2021
Date of Acceptance29-Nov-2021
Date of Web Publication29-Dec-2021

Correspondence Address:
Abhishek Mahajan
Department of Radiodiagnosis and Imaging, Tata Memorial Hospital, Room No. 125, Dr. E Borges Road, Parel, Mumbai - 400 012,Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/crst.crst_132_21

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  Abstract 


Preoperative imaging is essential for staging carcinomas of the oral tongue in addition to clinical staging. The current TNM staging of the oral cavity according to the 8th edition of the American Joint Committee on Cancer is appropriate for buccal mucosal carcinomas due to their proximity to and frequent involvement of the skin, bone, and masticator space in case of advanced disease. However, it is inadequate for the subclassification of tongue carcinomas. Tongue cancers, even those in the advanced stage, do not frequently involve these structures, thus leading to understaging of these tumors. We observed that the preoperative radiological markers such as perineural invasion, hyoid bone involvement, extrinsic muscle involvement up to their origin, and distance of the paralingual septum from the tumor are better predictors of prognosis of carcinoma of the tongue. In this article, we review the existing literature on T4 staging of tongue carcinomas and also propose a few modifications to the current staging system from a radiological perspective. A comprehensive search of abstracts of prognostic markers in tongue carcinoma and their impact on T4 stage was done. The PubMed and the Cochrane library were used. The keywords for Medical Subject Headings were as follows: Magnetic resonance imaging, Neurovascular bundle, Oral tongue, Perineural invasion, Squamous cell carcinoma, Extrinsic muscle invasion, Hyoid bone involvement, and Paralingual septum distance. The reference lists of included studies and review articles were checked manually. Unpublished data were not included in this review. We suggest a radiological T4 staging system which is more suitable for staging tongue cancers.

Keywords: 8th edition, American Joint Committee on Cancer, computed tomography, extrinsic muscle, Head and neck squamous cell cancer, hyoid, imaging, magnetic resonance imaging, neurovascular bundle, paralingual septum, perineural invasion, T4, tongue carcinoma, HNSCC


How to cite this article:
Mahajan A, Suthar M, Agarwal U, Shukla S, Thiagarajan S, Sable N. Imaging-based T stage (iT) as a predictive and prognostic marker for outcome in T4 stage tongue carcinomas: A narrative review. Cancer Res Stat Treat 2021;4:677-83

How to cite this URL:
Mahajan A, Suthar M, Agarwal U, Shukla S, Thiagarajan S, Sable N. Imaging-based T stage (iT) as a predictive and prognostic marker for outcome in T4 stage tongue carcinomas: A narrative review. Cancer Res Stat Treat [serial online] 2021 [cited 2022 Aug 20];4:677-83. Available from: https://www.crstonline.com/text.asp?2021/4/4/677/334172




  Introduction Top


Oral cavity cancers are a major public health concern worldwide, with 377,713 new cases reported in the year 2020 (constituting 2% of all cancer cases); additionally, according to GLOBOCAN 2020, oral cavity cancers account for 177,757 deaths per year (1.76% of the total deaths due to cancer).[1] However, there is a vast geographic discrepancy in the incidence across the globe, with different associated risk factors. Lip and oral cavity cancers are the third most common cancers among men in countries with low Human Development Index, after prostate and lung cancer, with a considerable disease burden in India.[1] Various studies depict that the incidence of oral cavity cancers is higher in developing countries due to widely prevalent risk factors, lack of awareness, and poor health infrastructure; moreover, it affects young patients.[2],[3] In developed countries, the risk factors include tobacco smoking, alcohol consumption, and infection with high-risk human papilloma virus.[4] Betel quid chewing is a major risk factor in developed countries, along with other less frequent factors such as smoking, alcohol, nutritional deficiency, poor dentition, and infection with viruses.[5],[6],[7],[8] The most common subsite for the occurrence of oral cavity cancers is the tongue; the incidence and mortality rate of tongue cancers are rising among young adults.[5] It is an aggressive malignancy with poor outcomes and an observed 5-year survival of 35.1% and relative survival of 44.6%.[9] The prognosis is better in early T1 and T2 stages, with a 5-year disease-specific survival of 85.6%.[10] Similarly, Rusthoven et al. reported that the survival rate for stage III/IV cancers is lower than that for stage I/II tongue carcinomas.[11] Thus, appropriate staging is essential for treatment planning. Early tongue cancers can be treated with wide local excision, whereas advanced disease requires surgery along with adjuvant chemotherapy and radiotherapy. Cross-sectional imaging is essential for evaluation of the disease extent and its spread to other structures.

TNM staging of the 8th edition of the American Joint Committee on Cancer (AJCC) is widely used for the interpretation of the stage of the disease. This system is suitable for staging of buccal mucosal disease due to its proximity and frequent involvement of the adjacent bone, skin, and masticator space in advanced cases. However, it is inadequate for the subclassification of tongue cancers. Advanced carcinomas of the tongue do not frequently involve these structures, and hence, might lead to understaging of the tumor. Limited data are available for tongue cancers invading these structures. Mandibular invasion was not found in advanced carcinoma of the tongue treated with an aggressive approach.[12] Various imaging biomarkers such as perineural invasion,[13],[14],[15] hyoid bone involvement,[16],[17] extrinsic muscle involvement up to the origin,[18] and paralingual septum distance[19],[20],[21],[22] are described as predictors of prognosis for carcinoma of the tongue. In this article, our objective was to review the existing literature on the T4 staging of tongue carcinomas and to propose a few changes to the current staging system from a radiologic perspective. We hope to be able to suggest an improved and practical imaging-based T4 staging for tongue cancers that will help choose between an aggressive and non-aggressive treatment approach.


  Methods Top


A comprehensive search of abstracts of articles related to prognostic markers in tongue carcinoma and their impact on T4 stage was done. The PubMed and the Cochrane library were used. The keywords for Medical Subject Headings were as follows: Magnetic resonance imaging (MRI), Neurovascular bundle, Oral tongue, Perineural invasion, Squamous cell carcinoma, Extrinsic muscle invasion, Hyoid bone involvement, and Paralingual septum distance. The reference lists of included studies and review articles were checked manually. Unpublished data were not included in this review.

Anatomy

Muscles of the tongue

The anterior two-third region of the tongue is a muscular organ comprising intrinsic and extrinsic muscles. It is divided into two parts by the midline lingual septum. The four paired intrinsic muscles are the superior and inferior longitudinal muscles and the transverse and vertical muscles. The superior longitudinal muscles run along the upper surface of the tongue [Figure 1]a and [Figure 1]b; the inferior longitudinal muscles are situated deep to the transverse muscles near the root of the tongue. The transverse muscles are situated between the superior and inferior longitudinal muscles and attach to the midline septa medially and mucous membrane along the lateral sides of the tongue. The vertical muscles are located in the middle of the tongue and intersect the fibers of the transverse muscles.
Figure 1: Anatomy of the tongue. (a) Extrinsic and intrinsic muscles of the tongue depicted in sagittal and coronal T1-weighted MRI images. Superior longitudinal muscles (outlined as white solid line) are seen below the oral mucosa (marked as*). Fan-shaped genioglossus muscle (yellow dotted line) can be seen arising from the genial tubercle of the mandible on both sides of the lingual septum, forming the bulk of the tongue. (b) The hyoglossus muscle is shown as a blue shaded area on the lateral margin of the tongue. The lingual neurovascular bundle (green solid) lies on both sides of the midline, lateral to the genioglossus. Geniohyoid (thin arrow) and mylohyoid (thick arrow) can be seen on the floor of the mouth. The submandibular gland (S) lies laterally to the mylohyoid muscle. (c) The hyoid bone at the base of the tongue can be seen as a rounded structure anterior to the trachea. The geniohyoid muscle (GH) on the floor of the mouth can be seen inserting into the hyoid bone (H). (d) The lingual neurovascular bundle lateral to the genioglossus can be seen as a hypointense flow void (marked in white solid line)

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The four extrinsic muscles of the tongue are the hyoglossus, genioglossus, palatoglossus, and styloglossus. These originate from the bone and extend into the tongue. The genioglossus arises from the genial tubercle of the mandible and spreads like a fan on both sides of the midline. Superiorly, it merges with the intrinsic muscles, and inferiorly, it inserts into the hyoid bone. It can be easily visualized on a computed tomography scan or MRI as a fan-shaped muscle on both sides of the midline forming the bulk of the tongue [Figure 1]a.

The hyoglossus arises from the greater cornua of the hyoid bone, ascends superiorly interdigitating with the styloglossus, and attaches to the lateral side of the tongue. It is observed as a quadrilateral plate on both sides of the tongue [Figure 1]b. The palatoglossus muscle arises from the soft palate and blends with the hyoglossus. The styloglossus arises from the styloid process and stylomandibular ligament and interdigitates with the hyoglossus.

Floor of the mouth and hyoid bone

This is primarily composed of the mylohyoid muscle, which is a U-shaped sling arising from the inner aspect of the mandible and inserts into the midline fibrous raphe and hyoid bone. The geniohyoid and anterior bellies of the digastric muscle support the floor of the mouth. The geniohyoid is visible on the coronal images above the mylohyoid muscle and on the sagittal T2-weighted images as a hypointense muscle on the floor of the mouth [Figure 1]b. The anterior bellies of the digastric are best visible on the coronal images below the mylohyoid on both sides of the midline. The sublingual space is a fat-filled space lateral to the genioglossus and superior medial to the mylohyoid. The submandibular space is located inferior to the mylohyoid [Figure 1]b. The hyoid bone is a horseshoe-shaped bone situated in the midline between the mandible and thyroid cartilage and provides attachment to the muscles of the tongue [Figure 1]c.

Lingual neurovascular bundle

The lingual nerve is a branch of the mandibular nerve, which traverses with the lingual artery in the anterior two-third of the tongue up to the tip, lying below the mucous membrane supplying the sensory fibers.[22] Tongue carcinomas are commonly seen near or abutting and encasing the lingual neurovascular bundle, resulting in perineural invasion [Figure 1]d.

Current T4 staging of carcinoma of the oral cavity and its practical implications

The 8th edition of the AJCC staging manual was published in 2018 and introduced major modifications to the 7th edition, with a “personalized medicine” approach.[23],[24] Imaging is an important aspect of the staging guidelines in the 8th edition, and in most sections, the discussion on imaging is more detailed compared to that in the previous edition. The major changes in the 8th edition of the AJCC were pertaining to the depth of invasion (DOI), which was included in all the T stages, as it is an independent predictor of overall and disease-free survival.[25],[26],[27],[28] It was observed that tumors staged as T3 according to the 7th edition have worse disease-specific survival than T4 stage disease, and the 8th edition better predicts the survival outcomes.[29] Extrinsic muscle involvement was removed from stage T4a, as the extrinsic muscles cannot be differentiated from the intrinsic muscle fibers on pathology and their involvement has no effect on disease-related survival.[30],[31]

T4a disease was described as a tumor invading the adjacent structures, including the maxillary or mandibular bone, maxillary sinus, or skin of the face. T4b disease was described as a tumor invading the masticator space, pterygoid plates, skull base, and/or encasing the internal carotid artery [Table 1].[32]
Table 1: T4 stage of oral cavity cancer according to the 8th edition of the American Joint Committee on Cancer and the proposed new radiological staging for cancer of the anterior two-third of the tongue

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However, we have realized in our practice that tongue malignancies rarely extend to the bone and skin to upstage them to T4a; even advanced disease does not frequently extend to the masticator space, pterygoid plates, skull base, or internal carotid artery. The common routes of spread of advanced oral tongue carcinoma involve the paralingual septum, ipsilateral and contralateral neurovascular bundle invasion, hyoid bone abutment, and uncommonly the origin of the extrinsic muscles of the tongue.

Proposed radiological markers and their justification in restaging T4 tumors

To overcome the limitations of the oral cavity T4 staging of the 8th edition of the AJCC for tongue carcinomas, we propose additional radiological markers that could help predict tumor prognosis and improve the management planning by clinicians.

Perineural invasion

Perineural invasion is an important predictor of disease outcome and local and nodal recurrence.[14],[15],[33],[34] Imaging can be an important method for the preoperative detection of perineural invasion. The presence of perineural invasion in oral squamous cell carcinoma is predictive of worse disease-specific survival, and distant recurrence is the most common pattern of failure.[35] Perineural invasion in oral tongue carcinomas is suspected when the tumor abuts or encases the lingual neurovascular bundle. Shah et al.[13] proposed a reproducible MRI classification for perineural invasion on the basis of the relation between the tumor and the neurovascular bundle. A type 1 tumor is far from the neurovascular bundle or more than 5 mm away from the neurovascular bundle; type 2 tumors are within a 5 mm distance from the neurovascular bundle, type 3 tumors abut the neurovascular bundle with an angle of contact of <180°; and type 4 tumors show complete encasement of the neurovascular bundle or an angle of contact of more than 180° [Table 2] and [Figure 2]. This study revealed a statistically significant correlation between abutment/encasement of the neurovascular bundle and the presence of perineural invasion on histopathological examination, and its presence influenced the disease-free survival on univariate analysis.[13] This supports the hypothesis that neurovascular bundle invasion upgrades the tongue carcinoma to a higher stage [Figure 3]. Therefore, we propose the inclusion of the ipsilateral neurovascular bundle invasion in the T4a stage.
Table 2: Proposed classification of the neurovascular bundle involvement by tongue cancer

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Figure 2: Classification of the neurovascular bundle involvement by tongue cancer depicted on coronal STIR magnetic resonance imaging sequences. (a) Type 1 tumor is far from the neurovascular bundle. White arrow points to the neurovascular bundle in all images (T=Tumor). (b) Type 2 tumor is located within 5 mm from the neurovascular bundle. (c) Type 3 tumor abuts the neurovascular bundle. (d) Type 4 tumor shows complete encasement of the neurovascular bundle

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Figure 3: Carcinoma of the tongue involving adjacent structures. (a) Coronal STIR image shows a hyperintense mass encasing the ipsilateral neurovascular bundle, crossing the midline and abutting the contralateral neurovascular bundle. (b) Coronal STIR image shows an irregular, mildly enhancing tumor predominantly in the right tongue, crossing the midline and encasing the bilateral neurovascular bundles. (c) Contrast-enhanced magnetic resonance imaging in the coronal plane displays a large heterogeneous enhancing mass occupying the entire right tongue infiltrating the hard palate (p) on the right side. It also invades the ipsilateral sublingual gland and ipsilateral neurovascular bundle, crossing the midline and approaching the contralateral neurovascular bundle. (d) Contrast-enhanced magnetic resonance imaging in the sagittal plane shows an enhancing mass in the tongue invading the hyoid bone (SG: Sublingual muscle; M: Mylohyoid muscle; H: Hyoid bone)

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Tumors crossing the midline are more likely to metastasize to the contralateral neck nodes, with adverse outcomes requiring total glossectomy.[19] The relation of tumors crossing the midline to the contralateral neurovascular bundle is an important factor in planning surgery, as the contralateral neurovascular bundle invasion excludes the possibility of a partial glossectomy. We propose contralateral neurovascular bundle invasion to be included in the T4b stage of tongue carcinoma [Figure 3]b.

Invasion of the origin of the extrinsic muscles

The invasion of the extrinsic muscles by carcinoma of the tongue was removed from the 8th edition of the AJCC on the grounds that the extrinsic and intrinsic muscles are difficult to distinguish by pathological examination.[30],[36] We observed that insertions of the extrinsic muscles of the tongue are superficially located and their involvement is not an indicator of advanced disease. However, the origin of the extrinsic muscles is deeply situated, and tumors of the oral tongue can spread to the deep structures through attachment to these extrinsic muscles.[18] Tumors invading the origin of the extrinsic muscles are suggestive of advanced disease. The origin of the four extrinsic muscles of the tongue are the hyoid bone, genial tubercle, soft palate, and styloid process, and tumors extending to these sites suggest advanced disease. Two sites of origin of the extrinsic muscles that are frequently involved by carcinoma of the tongue are the hyoid bone and palate [Figure 3]c. Junn et al.[37] in their study have described the imaging features most predictive of extrinsic tongue muscle invasion, thus enabling the assessment of disease spread in the baseline scan. We propose the inclusion of the invasion of the origin of the extrinsic muscles by the tongue cancer in the T4b stage during the radiological staging of oral cancers.

Hyoid bone involvement

Hyoid bone involvement is discussed in detail with respect to carcinomas of the base of the tongue, but its importance with respect to the malignancies of the anterior two-third of the tongue is not highlighted. The abutment/involvement of the hyoid bone is commonly seen in advanced tongue cancers[16] and is important for surgical decision-making.[17],[38],[39] We have devised a classification system for hyoid bone involvement, in which a tumor located more than 5 mm away from the hyoid bone is classified as type 1, a tumor located within 5 mm from the hyoid bone is classified as type 2, and a tumor abutting or infiltrating the hyoid bone is classified as type 3 [Table 3] and [Figure 4]. Oral tongue lesions located within 5 mm of the hyoid bone are inoperable and are treated with chemoradiation as per our institutional protocol. In addition, in a study by Heaton et al.,[40] patients with hyoid bone involvement had poorer survival metrics. Hence, we propose that the type 2 and 3 tumors based on hyoid bone involvement be included in the T4b stage of tongue carcinoma [Figure 3]d.
Table 3: Proposed classification of hyoid bone invasion by tongue cancer

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Figure 4: Classification of hyoid bone invasion by tongue cancer depicted on sagittal post contrast-enhanced magnetic resonance imaging. (a) Type 1 tumor is >5 mm away from the hyoid bone. Black arrow points to the hyoid bone on all images. (b) Type 2 tumor is located within 5 mm from the hyoid bone. (c) Type 3 tumor abuts/infiltrates the hyoid bone

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Paralingual septum distance

In addition to the DOI, the paralingual septum is an important factor in the treatment planning of tongue malignancies; tumors that are close to the septum or cross the midline are associated with an increased incidence of metastases and associated with poor outcomes.[20],[21],[41],[42],[43] Okura et al.[19] observed that a cutoff of 5.2 mm for the distance between the tumor and the paralingual septum served as a significant predictor of lymph node metastases and an important factor for preoperative decision-making with regard to neck node dissection.[19] If the tumor is <5 mm away from the lingual septum or abuts the septum or crosses it, a higher T stage is warranted. Hence, we propose that the distance of ≤5 mm between the paralingual septum and the tumor be included in the T4a stage for tongue carcinomas.

We have proposed an independent and more practical radiological T4 staging for carcinoma of the oral tongue [Table 1]. An elaborate study is, however, required to assess these proposed criteria and their implications on patient survival.


  Conclusion Top


Advanced oral tongue carcinomas spread differently from buccal mucosa cancers, and an independent imaging-based T4 staging system can help clinicians decide their management approach. However, extensive research is required to assess the role of these imaging-based biomarkers and their impact on patient survival.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]


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