MR evaluation of tongue carcinoma in the assessment of depth of invasion with histopathological correlation: A single center experience

Abstract

Introduction:
Magnetic resonance imaging (MRI) has become the cornerstone for pretreatment evaluation of carcinoma tongue and provides accurate information regarding the extent of the lesion and depth of invasion that helps the clinician to optimize treatment strategy. Aim of the study is to correlate MRI and histopathological findings, to evaluate the role of MRI in loco-regional tumor node metastasis (TNM) staging, and to assess the depth of invasion of tongue carcinoma.

Materials and methods:
This study was undertaken on 30 patients with clinical diagnosis of tongue carcinoma referred for MR imaging at a tertiary care hospital over the 2-year period between July 2017 and June 2019. MRI was performed with GE 1.5 Tesla scanner, neurovascular (NV) array coil. Clinical and MRI staging of tongue carcinoma was done preoperatively and correlated. Post-surgery, histopathological TNM staging was done and correlated with clinical and MRI TNM staging. The cutoff value of histopathological (HP) depth that could determine the existence of nodal metastasis was 5 mm.

Results:
In 30 patients diagnosed with tongue carcinoma, the incidence was higher in males (92%). Moderate agreement (k = 0.512) was noted for T staging between clinical and MRI staging assessments. Fair agreement (k = 0.218) was noted for N stage between clinical and MRI staging assessments. There was good agreement (k = 0.871) for M stage between the clinical and MRI staging assessments. Good agreement (k = 0.822 and k = 0.767, respectively) was noted for both T staging and Nstaging between MRI and histopathology staging assessments. The agreement for the T stage was poor (k = 0.012) between the clinical and histopathology staging assessments. Agreement for the N stage was also poor (k = 0.091) between the clinical and histopathology staging assessments. Mean depth of invasion by histology and MRI was 14.22 mm and 16.12 mm, respectively. Moderate agreement (k = 0.541) was noted between clinical and pathological tumor depth and good agreement (k = 0.844) was noted between radiological and pathological tumor depth. As for the T1WGd MRI depth with a cutoff value of 5 mm, the nodal metastasis rate in the group with values >5 mm was 52%, and for those <5 mm was 24%, both of which were significantly different (P = 0.040). Pearson's correlation coefficient of HP depth and T1WGd MRI depth was 0.851 (P < 0.001) suggesting that HP depth shows a strong correlation with T1WGd MRI depth.

Conclusion:
MRI is the imaging modality of choice for evaluation of tongue carcinoma as MRI helps in accurate staging of the tumor using TNM classification which is crucial for optimizing treatment options. The current study shows a high correlation between MRI and histopathological findings regarding thickness of tumor and depth of invasion. MRI and histopathology assessments of tumor spread were equivalent to within 0.5 mm DOI. Estimation of invasion depth using MRI as a preoperative study in oral tongue carcinoma is essential in planning surgical treatment strategies such as the extent of elective neck dissection. Invasion depth, which greatly affects occult node metastases, must be included in the TNM staging of oral tongue carcinoma.

Full text

126 © 2020 Indian Journal of Radiology and Imaging | Published by Wolters Kluwer ‑ Medknow
MR evaluation of tongue carcinoma in
the assessment of depth of invasion
with histopathological correlation:
A single center experience
Reddy Ravikanth
Department of Radiology, Holy Family Hospital, Thodupuzha, Kerala, India
Correspondence: Dr. Reddy Ravikanth, Department of Radiology, Holy Family Hospital, Thodupuzha ‑ 685 605, Kerala, India.
E‑mail: ravikanthreddy06@gmail.com
Abstract
Introduction: Magnetic resonance imaging (MRI) has become the cornerstone for pretreatment evaluation of carcinoma tongue
and provides accurate information regarding the extent of the lesion and depth of invasion that helps the clinician to optimize
treatment strategy. Aim of the study is to correlate MRI and histopathological ndings, to evaluate the role of MRI in loco‑regional
tumor node metastasis (TNM) staging, and to assess the depth of invasion of tongue carcinoma. Materials and Methods: This
study was undertaken on 30 patients with clinical diagnosis of tongue carcinoma referred for MR imaging at a tertiary care hospital
over the 2‑year period between July 2017 and June 2019. MRI was performed with GE 1.5 Tesla scanner, neurovascular (NV)
array coil. Clinical and MRI staging of tongue carcinoma was done preoperatively and correlated. Post‑surgery, histopathological
TNM staging was done and correlated with clinical and MRI TNM staging. The cuto value of histopathological (HP) depth that
could determine the existence of nodal metastasis was 5 mm. Results: In 30 patients diagnosed with tongue carcinoma, the
incidence was higher in males (92%). Moderate agreement (k = 0.512) was noted for T staging between clinical and MRI staging
assessments. Fair agreement (k = 0.218) was noted for N stage between clinical and MRI staging assessments. There was good
agreement (k = 0.871) for M stage between the clinical and MRI staging assessments. Good agreement (k = 0.822 and k = 0.767,
respectively) was noted for both T staging and Nstaging between MRI and histopathology staging assessments. The agreement
for the T stage was poor (k = 0.012) between the clinical and histopathology staging assessments. Agreement for the N stage was
also poor (k = 0.091) between the clinical and histopathology staging assessments. Mean depth of invasion by histology and MRI
was 14.22 mm and 16.12 mm, respectively. Moderate agreement (k = 0.541) was noted between clinical and pathological tumor
depth and good agreement (k = 0.844) was noted between radiological and pathological tumor depth. As for the T1WGd MRI depth
with a cuto value of 5 mm, the nodal metastasis rate in the group with values >5 mm was 52%, and for those <5 mm was 24%,
both of which were signicantly dierent (P = 0.040). Pearson’s correlation coecient of HP depth and T1WGd MRI depth was
0.851 (P < 0.001) suggesting that HP depth shows a strong correlation with T1WGd MRI depth. Conclusion: MRI is the imaging
modality of choice for evaluation of tongue carcinoma as MRI helps in accurate staging of the tumor using TNM classication
which is crucial for optimizing treatment options. The current study shows a high correlation between MRI and histopathological
ndings regarding thickness of tumor and depth of invasion. MRI and histopathology assessments of tumor spread were equivalent
Head and neck ImaGInG
Cite this article as: Ravikanth R. MR evaluation of tongue carcinoma in the
assessment of depth of invasion with histopathological correlation: A single
center experience. Indian J Radiol Imaging 2020;30:126‑38.
Received: 08‑Jul‑2019 Revised: 08‑Oct‑2019
Accepted: 10‑Apr‑2020 Published: 13‑Jul‑2020
This is an open access journal, and articles are distributed under the terms of
the Creative Commons Attribution‑NonCommercial‑ShareAlike 4.0 License,
which allows others to remix, tweak, and build upon the work non‑commercially,
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the identical terms.
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DOI:
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Ravikanth: MR evaluation of tongue carcinoma
127
Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
Introduction
Most tumors of the tongue occur on the lateral and under
surface.[1] Dorsal tumors are uncommon but when they
do occur, they are usually located near the midline and
more posteriorly.[2] Oral tongue tumors tend to remain in
the tongue. Tumors in the anterior third of the oral tongue
invade the floor of the mouth.[3] Middle‑third lesions
inltrate the musculature of the tongue and later, the lateral
oor of the mouth.[4] Carcinomas involving the posterior
third of the tongue grow into the musculature of the tongue,
the oor of the mouth, the anterior tonsillar pillar, the
tongue base, the glosso‑tonsillar sulcus, and the mandible.[5]
MRI provides valuable information both within and
without the tongue. The tongue carcinoma may extend far
beyond the gross tumor margin seen on surgery, which
is often deceiving. It is known that the most important
factor governing local recurrence is the resection margin.[6]
Whereas 1 cm is generally considered adequate for most
squamous cell carcinomas, the margins for tongue cancer
should be 1.5–2.0 cm.[7] Tumors with deep margins are often
dicult to assess during surgery. In addition, these tumors
are technically more dicult to resect. Hence, deep margins
are frequently the site of positive or inadequate resection
margins. Up to 35% of patients have nodal metastasis on
presentation.[8] Five percent of these patients have bilateral
lymph node involvement.[9] The rst echelon nodes are the
submandibular and jugulodigastric nodes.[10] Submental
node involvement is uncommon except in patients with
tumor at the tip of tongue.[11] It should be noted that in
patients with clinically N0 neck, the overall occult metastatic
rate is approximately 30%.[12] Various clinical studies have
been performed to correlate the depth of tumor invasion with
the likelihood of cervical nodal metastasis. These studies
reveal that the single most important factor in predicting
lymph node metastasis is the depth of tumor invasion.[13]
Tongue base carcinoma is a clinically silent region and
tumors tend to spread with deep inltration. As a general
rule, the extent of these tumors is underestimated during
clinical examination. Tongue base tumors tend to remain
in the tongue except for laterally placed lesions or late
cases. Under such circumstances, tongue base tumors may
extend into the tonsillar fossa. Tonsillar carcinomas, on the
other hand, have a tendency to invade the tongue base.
For tongue base carcinoma, the rst echelon nodes are the
jugulodigastric nodes, followed by mid and lower jugular
nodes. Retropharyngeal nodes are occasionally involved.
Submandibular nodes may be involved if there is anterior
tumor extension. Submental nodes are rarely involved.
Seventy‑ve percent of patients have positive nodes on
presentation, while 30% have bilateral nodal metastases.[14]
Patients with clinically N0 neck have a 30%–50% rate of
occult metastases.[15]
Imaging anatomy
The tongue comprises dorsum, apex, inferior surface, and
root. The root (base) is aached to the hyoid bone and
mandible while the apex forms the tip of the tongue. The
sulcus terminalis is a shallow groove with the circumvallate
papillae just anterior to it and divides the tongue into the
oral (anterior two‑thirds) and pharyngeal (posterior third)
parts. As a general guide on axial imaging, a line joining the
anterior aspect of the mandibular rami may be used as the
dividing line between these two parts, which dier in their
developmental origins and hence their nerve supplies.[16]
The tongue muscles are divided into intrinsic and extrinsic
groups. The intrinsic muscles are entirely within the tongue
with no bony aachment and are organized into superior
and inferior longitudinal, vertical, and transverse bands.
Their principle function is altering the shape of the tongue.
The extrinsic muscles consist of genioglossus, hyoglossus,
styloglossus, and palatoglossus. These extrinsic muscles
stabilize the tongue and alter its position, as well as its shape.
All the muscles of the tongue, intrinsic and extrinsic, are
thus innervated by the hypoglossal nerve. The exception
being palatoglossus, which being essentially a palate
muscle, is supplied by the pharyngeal plexus.
The anatomy of the tongue is well demonstrated on magnetic
resonance imaging (MRI). On axial T1‑weighted images, fat
with high signal intensity can be seen interspersed between
the muscles of intermediate signal intensity. MRI is the
preferred modality in the evaluation of tongue carcinomas.
The abnormal signals seen on MRI are well correlated with
pathological ndings. Tumor invasion of the oor of the
mouth is particularly well seen on coronal images. Sagial
images provide information on tongue base involvement
and the extent of pharyngeal inltration.[17]
Genioglossus is the largest of all the tongue muscles and
forms the bulk of the tongue. It arises from the genial
to within 0.5 mm DOI. Estimation of invasion depth using MRI as a preoperative study in oral tongue carcinoma is essential in
planning surgical treatment strategies such as the extent of elective neck dissection. Invasion depth, which greatly aects occult
node metastases, must be included in the TNM staging of oral tongue carcinoma.
Key words: Depth of invasion; magnetic resonance imaging; tumor node metastasis staging; tongue carcinoma
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Figure 1 (A and B): Axial schematic representation (A) and
T1‑weighted magnetic resonance (MR) image (B) demonstrate the
root of the tongue. The high‑signal‑intensity lingual septum (ls) is
clearly seen and is anked by the genioglossus muscles (gg), which
form an inverted V anteriorly before blending into the intrinsic muscles
of the mobile tongue. The sublingual spaces (sls) are lateral to the
genioglossus and geniohyoid muscles and also show high T1 signal
intensity. Axial T1‑weighted image (B) shows the tongue muscles,
genioglossus (long arrow), and hyoglossus (short arrow)
B
A
Ravikanth: MR evaluation of tongue carcinoma
128 Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
tubercle and is easily seen on MRI. It fans out widely and
inserts inferiorly into the hyoid bone; posteriorly into the
tongue base; and superiorly into the entire ventral surface
of the tongue. Hyoglossus is a thin quadrilateral sheet of
muscle arising from the hyoid bone. It ascends superiorly,
interdigitating with the bers of the styloglossus, and
aaches to the side of the tongue. The hyoglossus muscles
dene the lateral margins of the tongue and are readily
identied on MRI. Both the styloglossus (which arises
from the styloid process and stylohyoid ligament) and
the palatoglossus (which originates from the palatine
aponeurosis) cannot be seen with certainty on imaging
studies. Lymph from the tip of the tongue drains to
the submental nodes. Marginal lymphatics from the
outer third of the rest of the oral tongue are directed to
ipsilateral submandibular and jugulodigastric nodes.
Central lymphatics of the inner two‑thirds of the oral
tongue have pathways to nodes of both sides of the
neck.[18]
TNM staging
Tumor node metastasis (TNM) classication is the most
commonly used system for describing malignant tumors,
their regional involvement, and distant metastases.[19] The
TNM and stage grouping are presented below:
Aims and objectives
Aim of the study is to correlate MRI and histopathological
ndings, to evaluate the role of MRI in loco‑regional TNM
staging, and to assess the depth of invasion of tongue
carcinoma.
Materials and Methods
This study was undertaken in the Department of Radiology
at a tertiary care hospital in India over the 2‑year period
between July 2017 and June 2019. Before subjects were
recruited, the study protocol was approved by the
institutional ethics commiee (IEC), in accordance with
the ethical principles for human investigation outlined by
the Second Declaration of Helsinki, and wrien informed
consent was obtained from all patients prior to their
enrollment in this study (IEC, Holy Family Hospital; IEC
Approval Reference Number: HFH/12/2017; IEC Approval
Date: June 12, 2017). MR examinations wereperformed
using a 1.5‑T scanner (Signa, General Electric Medical
Systems, Milwaukee, WI, USA). Neurovascular (NV)
arraycoil was used. The patient’s head was secured
using relaxing cushion; ensuring that the shoulders
touch the lower part of the coil. The protocol included
axial, sagittal, and coronal T1‑weighted turbo spin
echo (TSE), axial and coronal T2‑weighted turbo spin
echo (TSE), and gadolinium‑enhanced axial and coronal
T1‑weighted sequences with fat suppression (FS) as well
as diffusion‑weighted (DW) sequences [Table 1]. The
tumor depth was measured at post contrast T1 coronal
FS. The tumor thickness was dened by the distance from
the deepest point of invasion to the tumor surface. At
rst, a vertical line joining the maximum length between
tumor‑mucosa junctions was drawn as a reference line. The
tumor thickness was determined by the summation of two
lines drawn perpendicular from the reference line to the
point of maximum tumor extension.
Clinical and MRI staging of tongue carcinoma was done
preoperatively and correlated [Figures 1‑16]. Post‑surgery,
histopathological TNM staging was done and correlated with
clinical and MRI TNM staging [Figures 17‑20 and Tables 2‑5].
T1 tumor measures ≤2 cm in greatest dimension with depth
of invasion (DOI) ≤5 mm. T2 tumor measures ≤2 cm with
DOI >5 mm. T3 tumor measures >2 cm and ≤4 cm with
DOI >10 mm. T4a is moderately advanced local disease
tumor >4 cm with DOI >10 mm. T4b is very advanced local
disease with tumor invasion into the masticator space,
pterygoid plates, or skull base, and/or tumor encases the
internal carotid artery.
Statistical analysis
Descriptive statistics were reported using numbers and
percentages for categorical variables. Analysis was done
Table 1: Protocol for MRI Tongue in the current study is as
below
Sequence Slice Slice thickness Gap Matrix
T1 Axial 29 4 mm 0.4 mm 512
T1 Coronal 23 4 mm 0.4 mm 512
STIR Coronal 23 4 mm 0.4 mm 256
T2 Fatsat Axial 29 4 mm 0.4 mm 512
T1 Fatsat Axial+C 23 4 mm 0.4 mm 512
T1 Fatsat Coronal+C 19 4 mm 0.4 mm 512
T1 Fatsat Sagittal+C 19 4 mm 0.4 mm 512
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Figure 3 (A and B): Sagittal drawing (A) and T1‑weighted MR
image (B) demonstrate the geniohyoid muscles (gh) and the fanlike
shape of the genioglossus muscles (gg). The mylohyoid muscle (mh)
extends from the mandible to the hyoid bone and supports the oor
of the mouth. Sagittal T1‑weighted image (B) shows the fan‑shaped
genioglossus (short arrow), the longitudinal intrinsic muscle (long
arrow), and darkly hypointense geniohyoid (star) from genial tubercle
to hyoid
A B
Figure 2 (A and B): Coronal schematic representation (A) and
T1‑weighted MR image (B) demonstrate genioglossus muscles (gg)
which resemble paramidline vertical pillars. Below the genioglossus
muscles, the geniohyoid muscles (gh) appear subtly wider than they do
on axial images [Figure 1]. The sublingual spaces (sls) show high T1
signal intensity. ls = lingual septum. Coronal T1‑ weighted image (B)
shows lingual septum (short arrow) and mylohyoid (long arrow), which
form the oor of the mouth
A B
Figure 4 (A-D): Mass lesion (star) in the right lateral aspect of the anterior 2/3rd of the tongue with inferior extension into the posterior aspect
of right sublingual space. The lesion appears isointense on T1 (A), hyperintense on T2 (B), and hyperintense on STIR (C and D) and extends
medially up to the lingual septum with no obvious extension across the midline. Axial STIR image (C) demonstrates an ill‑dened nodular mass
lesion involving intrinsic muscles of the anterior tongue including genioglossus, myelohyoid, and geniohyoid. Inferiorly, the lesion invades the
right lateral oor of mouth and sublingual space (short arrow). Posteriorly, there is an invasion of right pterygomandibular raphe (long arrow)
A B C D
Ravikanth: MR evaluation of tongue carcinoma
129
Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
Table 2: T-Primary tumor
Stage Status of primary tumor
TX Primary tumor cannot be assessed
T0 No evidence of primary tumor
Tis Carcinoma in situ
T1 Tumor 2 cm or less in greatest dimension
T2 Tumor more than 2 cm but not more than 4 cm in greatest dimension
T3 Tumor more than 4 cm in greatest dimension
T4a (lip) Tumor invades through cortical bone, inferior alveolar nerve, floor
of mouth, or skin (chin or nose)
T4a (oral
cavity)
Tumor invades through cortical bone, into deep/extrinsic muscle
of tongue (genioglossus, hyoglossus, palatoglossus, and
styloglossus), maxillary sinus, or skin of face
T4b (lip and
oral cavity)
Tumor invades masticator space, pterygoid plates, or skull base; or
encases internal carotid artery
Table 3: N – regional lymph nodes
Stage Status of regional lymph nodes
NX Regional lymph nodes cannot be assessed
N0 No regional lymph node metastasis
N1 Metastasis in a single ipsilateral lymph node, 3 cm or less in
greatest dimension
N2 Metastasis as specified in N2a, 2b, 2c below
N2a Metastasis in a single ipsilateral lymph node, more than 3 cm but
not more than 6 cm in greatest dimension
N2b Metastasis in multiple ipsilateral lymph nodes, none more than
6 cm in greatest dimension
N2c Metastasis in bilateral or contralateral lymph nodes, none more
than 6 cm in greatest dimension
N3 Metastasis in a lymph node more than 6 cm in greatest dimension
Table 4: M – Distant metastasis
Stage Status of distant metastasis
MX Distant metastasis cannot be assessed
M0 No distant metastasis
M1 Distant metastasis
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Figure 5 (A-F): Mass lesion (star) involving the alveolar margin
of the mandible in the midline extending along the lingual septum
and genioglossus muscle with inltration of the sublingual spaces
anteriorly. The lesion appears isointense on T1 (A), heterogeneously
hyperintense on T2 (B), and hyperintense on STIR (C and D) showing
contrast enhancement on T1 + c images (E and F) and a central focus
of nonenhancement— suggestive of necrosis. Axial T2 weighted
fat‑suppression MR image (B) demonstrates a bulky enhancing tumor
in genioglossus of anterior tongue extending into anterior alveolar
margin of mandible causing erosion of occlusal cortices of mandible
and enhancement in the marrow (short arrow). Sagittal T1 + c image (F)
shows tumor invading the oor of the mouth (long arrow). There is
sparing of the mylohyoid muscle inferiorly
A B C
D E F
Figure 6 (A-F): Irregular shaped mass lesion (star) in the lateral aspect
of the anterior 2/3rd of the left tongue with no extension across the
midline and no obvious involvement of the oor of the mouth/sublingual
space. The lesion appears isointense on T1 (A), heterogeneously
hyperintense on T2 (B), and hyperintense on STIR (C and D) showing
contrast enhancement on T1 + c images (E and F) with a central focus
of nonenhancement—s/o necrosis. Axial T2 weighted fat‑suppression
MR image (B) demonstrates a nodular mass lesion in the anterior
2/3rd of the oral tongue with inltration of the genioglossus (short arrow)
and reaching up to sublingual space invading mylohyoid (long arrow).
Coronal T1 + c image (E) shows no obvious invasion of the oor of mouth
A B C
D E F
Ravikanth: MR evaluation of tongue carcinoma
130 Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
Table 6: Correlation between MRI and clinical tumor (T) staging
Clinical
“T”staging
MRI “T”staging Total
T1 T2 T3 T4
T1 1 0 0 0 1
T2 0 6 2 0 8
T3 0 3 6 2 11
T4 0 1 4 5 10
Total 1 10 12 7 30
Sensitivity 90.1%
Specificity 93.8%
PPV 95.0%
Kappa coefficient 0.612, 95% CI (0.521-1.00)
By applying the Chi-square test and kappa statistics, P and k come out to be 0.01 and 0.512,
respectively, showing moderate agreement between the clinical and MRI staging assessments
using Microsoft Excel 2013, Microsoft Corp., Redmond, WA,
USA and SPSS Statistical Package Version 20.0, IBM Corp.,
Armonk, New York, USA. P value (<0.05) was considered
statistically signicant. The inter‑observer agreement was
assessed using Kappa statistics.
Results
This study was undertaken on 30 patients with clinical
diagnosis of tongue carcinoma referred for MR imaging
at a tertiary care hospital over the 2‑year period. 68% of
the patients belonged to age group of 51–60 years, which
was followed by the age group of 41–50 years comprising
of 18% of the patients and 61–70 years comprising 13%
of the patients. The incidence of oral cancers is higher
in males constituting 92% of total patients. There was
moderate agreement (k = 0.612) for the T stage between
the clinical and MRI staging assessments [Table 6] and fair
agreement (k = 0.218) for N stage between MRI and clinical
staging assessments [Table 7]. Good (k = 0.822) agreement
for the T stage was seen between MRI and histopathology
staging assessments [Table 8] and for N stage (k = 0.931)
between MRI and histopathology staging assessments
[Table 9]. There was good agreement (k = 0.871) for M stage
between the clinical and MRI staging assessments. The
agreement for the T stage was poor (k = 0.012) between the
Table 5: Stage grouping
Group Primary tumor Regional lymph nodes Distant metastasis
Stage 0 Tis (in‑situ) N0 M0
Stage I T1 N0 M0
Stage II T2 N0 M0
Stage III T3 N0 M0
T1, T2, T3 N1 M0
Stage IVa T4a N0, N1 M0
T1, T2, T3, T4a N2 M0
Stage IVb T4b Any N M0
Any T N3 M0
Stage IVc Any T Any N M1
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Figure 9: 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 which corresponds to T3 stage
Figure 10: 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 which
correspond to T2 stage
Figure 7 (A-F): Ill‑dened mass lesion (star) extending along the
anterior and left alveolar margins of the mandible with inltration of
bilateral genioglossus muscles, the lingual septum, bilateral sublingual
spaces, left masticator space, left submandibular gland, and left
geniohyoid muscle inferiorly. The lesion appears isointense on T1 (A),
hyperintense on T2 (B), and hyperintense on STIR (C and D) showing
contrast enhancement on T1 + c images (E and F). There is sparing
of the mylohyoid muscle. Axial T2‑weighted fat‑suppression image (B)
reveals an ill‑dened heterogeneous signal intensity nodular mass
lesion involving the anterior tongue on left side. It crosses midline
anteriorly and involves genioglossus and geniohyoid. Coronal STIR
image (D) shows tumor inltration of the oor of the mouth. Note
the involvement of ipsilateral mylohyoid muscle (short arrow) and
normal contralateral mylohyoid. Note the tumor inltration into bilateral
sublingual glands (long arrows) on T2FS axial image (B)
A B C
D E F
Figure 8 (A-F): Irregular shaped mass lesion (star) in the left side of the
tongue appearing isointense on T1 (A), heterogeneously hyperintense
on T2 (B), and hyperintense on STIR (C and D) showing contrast
enhancement on T1 + c images (E and F). The lesion extends across
the midline into the right side. Inferiorly the lesion extends into the left
sublingual space causing loss of fat plane with the mylohyoid muscle
and to the anterior aspect of the right sublingual space. Axial STIR
image (C) demonstrates an ill‑dened nodular hyperintense mass
lesion of tongue invading genioglossus, myelohyoid, and geniohyoid
in the left lateral and anterolateral aspects of the tongue extending up
to lingual septum (short arrow) and crossing the midline (white line).
Posteriorly, the lesion invades the base of tongue and vallecula on left
side and abuts the anterior tonsillar pillar (long arrow)
A B C
D E F
Ravikanth: MR evaluation of tongue carcinoma
131
Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
clinical and histopathology staging assessments [Table 10].
Agreement for the N stage was poor (k = 0.091) between the
clinical and histopathology staging assessments [Table 11].
Mean depth of invasion by histology and MRI was14.22 mm
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Figure 14: Axial T1 weighted image shows a tongue cancer (T4aN2aM0)
with mandible invasion. However, the early involvement of cortical
bones is better seen on CT images. Radiological DOI measured
14.4 mm and histopathological DOI measured 14.1 mm. MRI and
histopathology assessments of tumor spread were equivalent to within
0.5 mm DOI
Figure 11: Coronal T2‑weighted image demonstrating muscle
invasion. Shows muscle invasion by the tumor. G = Genioglossus,
H = Hyoglossus, S = Styloglossus, and M = Mylohyoid. Tumor on the
right side shows the invasion of all muscles except myelohyoid
Figure 12 (A and B): (A) Axial T2 weighted fat‑suppression image
shows a right‑sided tongue cancer (T1N1M0) extending more
than 5 mm from the lateral margin of the tongue. (B) Coronal T2
weighted fat‑suppression image shows bilateral submandibular
lymphadenopathy (arrows), a result of the lymphatic drainage pathways
of the inner two‑thirds of the oral tongue. Radiological depth of
invasion (DOI) measured 3.5 mm and histopathological DOI measured
3.2 mm. MRI and histopathology assessments of tumor spread were
equivalent to within 0.5 mm DOI
A B
Figure 13 (A and B): (A) Axial T2 weighted fat‑suppression image
shows a right‑sided tongue base cancer (T4aN2aM0‑long arrows).
An enlarged right jugulodigastric node is also seen (short arrow),
the rst echelon node of tongue base carcinoma. (B) Sagittal T2
weighted fat‑suppression image of the same patient shows the extent
of pharyngeal invasion of the tongue base tumor (arrow).Radiological
DOI measured 13.2 mm and histopathological DOI measured 12.8 mm.
MRI and histopathology assessments of tumor spread were equivalent
to within 0.5 mm DOI
A B
Ravikanth: MR evaluation of tongue carcinoma
132 Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
and 16.12 mm, respectively. Moderate agreement (k = 0.541)
was noted between clinical and pathological tumor
depth [Table 12] and good agreement (k = 0.844) was
noted between radiological and pathological tumor depth
[Table 13]. The correlation between depth of invasion
reported on MRI and pathologic depth of invasion (r = 0.93;
P < 0.001).
Cuto values for histopathological (HP) depth and MRI depth
The cuto value of HP depth that could determine the
existence of nodal metastasis was 8 mm. The cuto value
for T1WGd MRI depth was 5 mm. With the HP depth cuto
value of 5 mm as a standard, groups were subdivided into
those >5 mm and those <5 mm; the nodal metastasis rates
for each group were 52% and 24%, respectively (P = 0.040).
Correlation between histopathological (HP) depth and MRI depth
Pearson’s correlation coecient of HP depth and T1WGd
MRI depth was 0.851 (P < 0.001) suggesting that HP depth
shows a strong correlation with T1WGd MRI depth.
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Figure 16 (A and B): (A) Coronal T2 weighted fat‑suppression image
shows a carcinoma in the middle third of the oral tongue (T3N1M0)
with early infiltration (long arrow) of the tongue musculature
(genioglossus). Note the ipsilateral submandibular lymphadenopathy
(short arrow). (B) Coronal post‑contrast T1 weighted fat‑suppression
image of a more advanced case shows the tumor invading the lateral
oor of the mouth (T4aN1M0‑arrow). Radiological DOI measured
9.2 mm and histopathological DOI measured 8.8 mm. MRI and
histopathology assessments of tumor spread were equivalent to
within 0.5 mm DOI
A B
Figure 15 (A and B): (A) Sagittal T2 weighted fat‑suppression image shows
carcinoma in the anterior third of the oral tongue (T4aN1M0‑arrow). (B)
Sagittal T2 weighted fat‑suppression image (same patient) shows tumor
invading the oor of the mouth (arrow). Radiological DOI measured
13.2 mm and histopathological DOI measured 12.9 mm. MRI and
histopathology assessments of tumor spread were equivalent to within
0.5 mm DOI
A B
Ravikanth: MR evaluation of tongue carcinoma
133
Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
Table 7: Correlation between MRI and clinical nodal (N) staging
Clinical
“N”staging
MRI “N”staging Total
N0 N1 N2
N0 6 3 4 13
N1 0 6 6 12
N2 0 0 5 5
Total 6 9 15 30
Sensitivity 93.7%
Specificity 95.2%
PPV 93.8%
Kappa coefficient 0.218, 95% CI (0.347-1.00)
By applying the Chi-square test and kappa statistics, P and k come out to be 0.03 and
0.218, respectively, which shows fair agreement between the clinical and MRI staging
assessments
Table 8: Correlation between MRI and histopathological tumor (T)
staging
MRI “T”staging HPE “T”staging Total
T1 T2 T3 T4
T1 10001
T2 0 10 0 0 10
T3 04307
T4 0 4 4 4 12
Total 1 18 7 4 30
Sensitivity 94.2%
Specificity 96.1%
PPV 92%
Kappa coefficient 0.822, 95% CI (0.631-1.00)
By applying the Chi-square test and kappa statistics, P and k come out to be 0.01and
0.822, respectively, which shows good/substantial agreement between the clinical and MRI
staging assessments
Discussion
In the current study, the extent of primary tumor (T)
and metastasis to regional lymph nodes (N) was initially
evaluated by clinical examinations followed by MR
imaging. The nal diagnosis was made by histopathological
examination (HPE). Kappa Index was used for data
analysis which showed moderate agreement (kappa value
0.512) between the clinical and MRI “T” staging. This is
consistent with the studies performed by Paiva et al.[20]
and Hirunpat et al.[21] which also showed that mis‑staging
by clinical examination in the overall stage grouping
was high. Also, there was good agreement (kappa value
0.822) for the T staging (tumor depth and width) between
MRI and HPE assessments. The final staging assessed
by MR imaging in the current study remains the same in
30 patients who underwent surgery and nal staging by
HPE. These results are consistent with the study conducted
by Tetsumura et al.[22] in which the tumor depth and width
were measured on both MR images and HPE and the
authors observed a high correlation between the values
measured by MRI and HPE.
In this study, clinical examination and MRI were both
adequate at determining depth of invasion compared with
nal pathology when tumors were ≥5 mm in depth, but
not for those less than 5 mm. We used 5 mm as a cuto
as this is the depth at which the risk of nodal metastases
increases, based on the literature.[13,23] Since the clinical
importance is to be able to detect deeper tumors, the
decreased ability of either examination to be able to
accurately predict the depth of supercial lesions is less
clinically signicant.
There have been previous studies investigating the
accuracy of MRI in predicting the depth of invasion of
oral tongue SCC; however, these studies primarily have a
small sample size and retrospective study design, and none
have compared MRI with clinical examination. Preda et al.
investigated 33 oral tongue SCC in a retrospective series.[24]
The authors demonstrated that MRI thicknesses correlated
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Figure 17 (A-C): (A) An example of minimal residual squamous
cell carcinoma of the oral tongue (hematoxylin and eosin (H and E),
original magnication ×40). (B) A minute focus of residual squamous
cell carcinoma, about 1mm wide and 1mm deep, with submucosal
scar in the left lower corner (H and E, original magnication ×100). (C)
The diagnostic biopsy was represented by ve tissue fragments,
all of which were smaller than 5mm in greatest dimension and had
invasive squamous cell carcinoma. The exact measurement of the
depth of invasion in this case is difcult given the fragmented nature
of diagnostic biopsy. Only one biopsy fragment had normal squamous
mucosa allowing measurement of the depth of invasion (H and E,
original magnication ×40)
A
B
C
Figure 18 (A and B): An example of a T2 squamous cell carcinoma
of the oral tongue with positive deep margin, indicating that the
depth of invasion may be underestimated. (A) The apparent depth
of invasion is 7mm; however, the deep margin is involved by
carcinoma (hematoxylin and eosin (H and E), original magnication
×20). (B) Carcinoma at deep margin. Hypothetically, if there is
additional 4mm (along the “plumb line”) of residual carcinoma in
the tumor bed, this carcinoma is more appropriately staged as
T3 (H and E, original magnication ×100)
A B
Ravikanth: MR evaluation of tongue carcinoma
134 Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
Table 9: Correlation between MRI and histopathological (N)
staging
MRI “N”staging HPE“N”staging Total
N0 N1 N2
N0 5 0 0 5
N1 5 3 2 10
N2 4 3 8 15
Total 14 6 10 30
Sensitivity 94.3%
Specificity 95.1%
PPV 93%
Kappa coefficient 0.931, 95% CI (0.751-1.00)
By applying the Chi-square test and kappa statistics, P and k come out to be 0.01 and
0.931, respectively, which shows good agreement between the clinical and MRI staging
assessments
Table 10: Correlation between clinical and histopathological
tumor (T) staging
Clinical
“T”staging
HPE“T”staging Total
T1 T2 T3 T4
T1 4 0 0 0 4
T2 0 9 2 0 11
T3 0 5 1 2 8
T4 0 3 1 3 7
Total 4 17 4 5 30
By applying the Chi-square test and kappa statistics, P and k come out to be 0.01and
0.012, respectively, which shows poor agreement between the clinical and MRI staging
assessments
strongly with histological tumor thicknesses (correlation
coecient = 0.68, P < 0.0001). Park et al.[25] evaluated
114 patients with oral cavity and oropharyngeal SCC
of which 49 patients had oral tongue SCC. Relationship
between MRI and histologic depth of invasion in oral
tongue subsite was high with a correlation coecient of
0.949. In the current study, the mean depth of invasion by
histology and MRI was 14.2 mm and 16.1 mm, respectively.
This group reported on deeper tumors, explaining the
beer correlation.
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Ravikanth: MR evaluation of tongue carcinoma
135
Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
As pointed out by Lwin et al.,[26] there is tumor shrinkage
after resection aecting all oral cavity subsites, including
the oral tongue. The tumor shrinkage factor for oral tongue
cancer has been reported to be 87%. Most of the studies
assessing the relationship between tumor depth of invasion
and risk of nodal metastases are based on pathologic
assessment and not clinical or radiographic assessment.
Therefore, clinical and MRI examination may under or
over estimate depth of invasion and may not have the same
ability to predict nodal metastases.
Sentinel lymph node (SLN) biopsy has been evaluated
in recent years in head and neck cancer. A few studies
evaluated SLN for oral and oropharyngeal cancer; however,
most of these studies included advanced T stage and did not
study specic subsite.[27‑29] Sagheb et al. did a pilot study to
examine the role of SLN in early T stage tongue SCC with
N0 neck. A SLN was followed by a neck dissection during
the same operation.[30] It was concluded that the sensitivity
of SLN is about 75% and further investigation is needed.
While MRI was shown to correlate well with pathological
depth and is more sensitive and specific for depth
measurements than clinical assessment, the laer test is
complementary and useful in situations where either MRI
is unavailable or dicult to interpret due to artefacts. In a
prospective study, Yuen et al.[31] examined the correlation
between ultrasound and pathologic tumor thickness in 45
oral tongue carcinoma patients during general anesthesia
and before commencing surgery. There was a statistically
signicant correlation coecient of 0.940 (P < .005). While
this technique may be dicult to perform in clinic due to
Table 11: Correlation between clinical and histopathological (N)
staging
Clinical
“N”staging
HPE“N”staging Total
N0 N1 N2
N0 6 0 2 8
N1 6 5 4 15
N2 3 0 4 7
Total 15 5 10 30
By applying the Chi-square test and kappa statistics, P and k comeout to be 0.01 and
0.091, respectively, which shows poor agreement between the clinical and MRI staging
assessments
Figure 20 (A-C): (A) Two clusters of invasive squamous cell
carcinoma (each with about 15 cells, by the black asterisk and in
B and C) were 6.5 mm from the bulk of the tumor, suggestive of
lymphatic invasion and representing the deepest point of invasion. The
black line illustrates the way the distance between the invasive tumor
front and remote foci of carcinoma was measured. The T1 stage was
assigned based on the depth of invasion by the bulk of the tumor which
was 4.5 mm. (B) One of the small clusters of carcinoma is in the left
upper corner and the second focus of carcinoma is in the right lower
corner. (C) Hematoxylin and eosin, images taken from the scanned
whole slide image with original magnication of ×1.2
C
B
A
Figure 19 (A and B): Cross‑section through left partial glossectomy with
dorsal, lateral, and ventral (toward oor of mouth) mucosa (clockwise,
starting from the top). (A) The focus of residual squamous cell
carcinoma (between the white and black asterisks) shows no
connection to mucosa. (B) Residual carcinoma is represented by foci
of extensive perineural invasion. The potential reference points to
measure the depth of invasion are along the dorsal, lateral, and ventral
mucosa. On this section, depth of invasion was measured from the
lateral mucosa (next to exclamation mark), because this area showed
a focus of moderate‑to‑severe dysplasia. Hematoxylin and eosin,
frozen section, images taken from the scanned whole slide image with
original magnication of ×1.2
B
A
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Ravikanth: MR evaluation of tongue carcinoma
136 Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
Table 12: Sensitivity and specificity of clinical depth in comparison
to pathological depth
Clinical depth (mm) Pathological depth (mm)
<5 >5 Total
<5 11 3 14
>5 5 11 16
Total 16 14 30
Sensitivity - 70%
Specificity - 78.5%
PPV - 70%
Kappa coefficient - 0.541, 95% CI (0.327-0.807)
Kappa coefficients were used to determine the agreement between measures once
categorized according to the cutoff point. Closer values to 1 mean higher agreement
between categories.
Table 13: Sensitivity and specificity of radiological depth in
comparison to pathological depth
Radiological depth (mm) Pathological depth (mm)
<5 >5 Total
<5 14 1 15
>5 2 13 15
Total 16 14 30
Sensitivity - 90%
Specificity - 92.8%
PPV - 90%
Kappa coefficient - 0.844, 95% CI (0.563-1.00)
Kappa coefficients were used to determine the agreement between measures once
categorized according to the cutoff point. Closer values to 1 mean higher agreement
between categories
pain or trismus, its improved ability to measure tumor
thickness does warrant further investigation. Despite the
importance of depth of invasion, other histopathological
parameters have been found to correlate with nodal
metastasis including size of the tumor in greatest dimension,
and other pathologic features such as paern of invasion,
density of cancer‑associated broblasts, and perineural and
vascular invasion.[32] All these need to be taken in account
to determine the risk of regional metastasis.
Multiple pulse sequences had been used in the previous
works to detect small tongue carcinoma and accurately
identify tumor margins, including T2WI, STIR, and
T1‑weighted fat‑suppressed contrast‑enhanced sequences.
Lam et al.[33] reported that particularly contrast‑enhanced
T1‑weighted MRI provides a satisfactory accurate correlation
between MRI tumor thickness and histologic tumor thickness
in oral tongue cancer. Background diffusion‑weighted
imaging obtained with magnetic resonance (DW‑MRI)
is a noninvasive imaging tool potentially able to provide
information about micro‑structure tumor characteristics.
The inclusion of DWI/ADC values might be helpful for
dierentiation between true tumor margin and edema,
and also for distinction between benign and malignant
head and neck tumors. Multiple studies reported high
diagnostic accuracy of DWI for dierentiation of malignant
from benign status of metastatic cervical lymph nodes.[34]
There are several studies[35] which tested the reliability of
MRI in measuring tongue tumor thickness and correlated
it well with histologic tumor thickness. Spiro et al.[36]
postulated that disease‑related death is apparently unusual
when oral tumors are thin, regardless of tumor stage, and
that tumor thickness rather than stage may have the best
correlation with treatment failure and survival. However,
tongue carcinoma may vary in shape and growth paern.
Therefore, depth of invasion (represented by para‑lingual
distance), not merely tumor thickness, is another important
prognostic factor.
The current study evaluated the clinical assessment
of tumor thickness in comparison to radiographic
interpretation. There are strong correlations between
pathological, radiological, and clinical measurements.
Specifically, for oral tongue, cut‑off of 5mm has been
suggested. Finally, just where to measure DOI from can
be dicult to determine in oral tongue (with mucosa on
dorsal, lateral, and ventral aspects) and in undulating
hyperplastic epithelium, which can create an uneven
basement membrane. One has to imagine an arcuate
reference line and then drop a “plumb‑line” which can be
equally as dicult due to variations in normal mucosa and
DOI at dierent tumor section. The study highlighted the
potential impact on T staging of extratumoral foci of SCC
due to perineural invasion. It must be noted that a large
proportion of extratumoral NI or LI occurs in tumors that
are already T3, thus diminishing their impact on staging.
Extratumoral perineural invasion represents a challenge to
DOI measurement in isolated cases only. These scenarios
are not currently directly addressed in the AJCC 8th edition
description of DOI. However, they are covered under
a more general TNM principle: when in doubt, the less
advanced aribute should be selected (i.e., smaller DOI
measurement, not including the extratumoral perineural
invasion).
The oral tongue is covered by mucosa on its dorsal, lateral,
and ventral aspects and a simple “plumb line” method may
be dicult to apply in some cases. When residual carcinoma
is small and not connected to the mucosal surface, the
reference point from which to measure the DOI is perhaps
best represented by mucosa with squamous dysplasia.
In oral tongue, the level of the basement membrane of
the closest adjacent normal mucosa is probably better
represented by an arcuaterather than a straight line,
especially when the line is drawn through two points,
i.e., normal mucosa on both sides of carcinoma.
The current study showed that in up to 12% of apparently
T2 cases, DOI may be underestimated due to the positive
deep margin. Rarely, extratumoral perineural invasion
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Ravikanth: MR evaluation of tongue carcinoma
137
Indian Journal of Radiology and Imaging / Volume 30 / Issue 2 / April‑June 2020
may be the deepest point of invasion, but it is unlikely
to aect T stage. DOI measurement for early SCC of the
oral tongue may require re‑examination of the diagnostic
biopsy slides in up to 20% of cases due to the absence
or only minimal residual carcinoma in glossectomy
specimens. A proactive assessment and reporting of DOI
on diagnostic biopsies or documentation of factors limiting
DOI measurement (e.g., fragmentation, lack of normal
mucosa, absence of intrinsic tongue musculature) may
minimize the need to re‑review the original diagnostic
biopsy when the glossectomy reveals no or minimal
residual carcinoma.
Conclusion
MRI is the imaging modality of choice for evaluation of
tongue carcinoma as MRI helps in the accurate staging
of the tumor using TNM classication which is crucial
for optimizing treatment options. The current study
shows a high correlation between MRI and HPE ndings
regarding thickness of tumor and depth of invasion. MRI
and histopathology assessments of tumor spread were
equivalent to within 0.5 mm DOI. In conclusion, estimation
of invasion depth using MRI as a preoperative study in
oral tongue carcinoma is essential in planning surgical
treatment strategies such as the extent of elective neck
dissection. Invasion depth, which greatly aects occult
node metastases, must be included in the TNM staging of
oral tongue carcinoma.
Limitations of the study
The limitations of our study include a relatively small
number of cases and errors caused by manual measurement
of tumor thickness during clinical examination.
Declaration of patient consent
The authors certify that they have obtained all appropriate
patient consent forms. In the form, the patients have given
their consent for their images and other clinical information
to be reported in the journal. The patients understand that
their names and initials will not be published and due eorts
will be made to conceal their identity, but anonymity cannot
be guaranteed.
Acknowledgement
The author would like to thank Mr. Retheesh, Senior
Radiographer, Department of Radiology, Holy Family
Hospital, Thodupuzha for the help rendered in the
preparation of schematic diagrams and acquisition of MR
images.
Financial support and sponsorship
Nil.
Conicts of interest
There are no conicts of interest.
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