Research Paper
Head, Neck Oncology
Automatic upstaging of tongue squamous cell carcinoma with lateral extrinsic muscle involvement is not justified

https://doi.org/10.1016/j.ijom.2013.06.003Get rights and content

Abstract

The TNM classification for oral malignancies has been criticized for its upstaging to T4a when tumour involves styloglossus, hyoglossus, palatoglossus and genioglossus. The aims of this study were to (1) create an anatomical computer atlas of extrinsic tongue musculature, and (2) reassess the original staging of pre-treatment archived magnetic resonance images (MRI) of tongue carcinomas using the strict extrinsic muscle criteria. The anatomy of the extrinsic tongue muscles was mapped using images from the Visible Human Project (VHP) to create a computer model of the extrinsic tongue muscles. This was co-registered with 87 archived pre-staging MRI scans of tongue carcinomas to assess tumour ingress of the extrinsic tongue muscles. Of the 87 image sets reviewed, 16 were of superficial tumours not visible on MRI. In the remaining 71 cases that showed positive extrinsic muscle tumour ingress, 52% were upstaged from T1/2/3 tumours to cT4a based upon this finding. Extrinsic lateral and genioglossus muscle invasion did not predict occult cervical lymph node invasion or disease-related survival. In conclusion, tumour invasion of styloglossus or hyoglossus would result in the majority of lateral tongue tumours being staged T4a. Such stratification is of little clinical relevance, and an alternative more reliable method is required.

Section snippets

Creation of a VHF-based anatomic atlas of extrinsic tongue musculature

The anatomy of the extrinsic tongue muscles was mapped in three dimensions using images from the Visible Human Project (VHP).7 The VHP obtained high-resolution computed tomography (CT) and MRI images prior to freezing, sectioning, and photographing two human cadavers (male 1994; female 1995). This produced three-dimensional (3D) datasets of the complete human anatomy, available free to the scientific community. The Visible Human Female (VHF) is the more comprehensive of the datasets.

Results

Fig. 1 demonstrates the final computer model to assist in extrinsic tongue muscle identification.

The demographic data of the 87 patients included in the study are summarized in Table 2. The mean age was 58 years (range 22–87 years). Of the 87 patients, 16 (18.4%) had superficial tumours not visible on MRI. These were designated as negative for extrinsic muscle involvement. Of the remaining 71 patients with positive extrinsic muscle tumour ingress, a total of 292 tumour-containing MRI slices

Discussion

The starting point of the study was the creation of a computer-based anatomical model on which to assess the accuracy of tumour staging of tongue tumours according to the TNM classification. The VHF provided intricate detail of the lingual musculature unaffected by formalin or shrinkage of tissues. Whilst the computer model was limited to data obtained from a single tongue, the close approximation to the classical anatomical texts of Abd-El-Malek and Miyawaki provided confirmation of anatomical

Funding

None.

Competing interests

None declared.

Ethical approval

Not required.

References (17)

  • C.H. Snyderman et al.

    Superiority of the T and N integer score (TANIS) staging system for squamous cell carcinoma of the oral cavity

    Otolaryngol Head Neck Surg

    (1995)
  • L.H. Sobin et al.

    International Union against Cancer. TNM classification of malignant tumours

    (2010)
  • J.F. Piccirillo

    Purposes, problems, and proposals for progress in cancer staging

    Arch Otolaryngol Head Neck Surg

    (1995)
  • P. Ambrosch et al.

    Clinical staging of oropharyngeal carcinoma: a critical evaluation of a new stage grouping proposal

    Cancer

    (1998)
  • R.P. Takes et al.

    Future of the TNM classification and staging system in head and neck cancer

    Head Neck

    (2010)
  • P.W. Boland et al.

    A detailed anatomical assessment of the lateral tongue extrinsic musculature, and proximity to the tongue mucosal surface. Does this confirm the current TNM T4a muscular subclassification?

    Surg Radiol Anat

    (2013)
  • M.J. Ackerman

    The Visible Human Project: a resource for anatomical visualization

    Stud Health Technol Inform

    (1998)
  • The University of Michigan Visible Human Project

    Visible Human Browser—female dataset

    Anatomic Browser

    (2005)
There are more references available in the full text version of this article.

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    There has been discussion about whether the invasion of styloglossus and hyoglossus muscles is truly reflected by the tumor staging. Boland et al. reported that because these muscles are located on the superficial layer from the mucosal surface of the tongue, their use as inclusion criteria in the T4a staging does not appear to be justified based upon their anatomical position [29]. The limitation was that the study was done using a computer model based on only one patient.

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    Due to the radiographic staging criteria mentioned above, this extreme proximity with the mucosa of the lateral oropharynx leads to a frequent radiographic up-staging. Based on the radiographic evidence of SG muscle involvement, Boland et al. [21] noted that up to 52% of cases clinically considered as T1-3 have been shown to be reclassified as T4a. However, the validity and relevance of radiographic up-staging is this scenario is controversial.

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