Introduction

Oral cancer is the most common malignancy in Indian men, and the oral tongue is frequently involved [1]. The most common site of metastasis from carcinoma of the tongue is to the cervical lymph nodes [2]. The chance of nodal metastasis correlates most strongly with the T (tumour) stage of the primary tumour with nodal involvement seen more in larger tumours. While advanced tumours present with clinically and radiologically obvious neck nodes, 15–30% of early tumours with no obvious nodal disease (N0) may also harbour micrometastasis [3]. For this reason, all patients who undergo surgery receive wide excision of the tongue lesion and ipsilateral cervical lymph node dissection [4]. The presence of even a single positive node reduced the survival by 50% compared to a patient with no positive cervical nodes. Several other primary tumour characteristics like degree of differentiation, depth of invasion, perineural invasion, and lymphovascular emboli have been studied to predict the probability of occult metastasis. Of these factors the depth of invasion is perhaps the most important predictor of neck node metastasis [5, 6].

Depth of invasion (DOI) of a tumour measures its invasiveness irrespective of an exophytic component. The latest 8th edition of American Joint Committee on Cancer (AJCC) cancer staging manual for head and neck cancers acknowledges the importance of depth of invasion and recognizes it as a factor for T staging independent of tumour size which has so far been the only criteria to decide between T1, T2, and T3 stages. This is because a more deeply invasive tumour predicts a worse prognosis compared to a lesser invasive tumour which could be due to the higher incidence of lymph node metastasis in deeper tumours [7].

In literature, tumour thickness (TT) and depth of invasion have often been used interchangeably. Tumour thickness (TT) is measured from the surface of the invasive squamous cell carcinoma for an exophytic tumour and from the ulcer base for an ulcerated tumour to the deepest point of invasion [8]. DOI was traditionally defined as the measurement from the surface of the adjacent uninvolved mucosa perpendicularly to the deepest point of invasion. See Fig. 1.

Fig. 1
figure 1

Tumour thickness vs depth of invasion

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The current AJCC/CAP (College of American Pathologists) seeks to standardise the measurement of DOI. As per the new guidelines, depth of invasion is measured from the horizon of the basement membrane of the adjacent squamous mucosa to the deepest point of the tumour in a perpendicular direction [9] (Fig. 2).

Fig. 2
figure 2

Depth of invasion as per new CAP/AJCC guidelines

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Purpose of the Study

This study seeks to assess whether the incidence of neck node metastasis in carcinoma tongue correlates with depth of invasion as per the new guidelines.

Patients and Methods

This is a case series analysis of records of 131 patients who presented with squamous cell carcinoma of the tongue and underwent primary surgery, i.e. wide excision of the tongue lesion and ipsilateral neck dissection in the department of surgical oncology at Medical College Kozhikode from March 2019 to July 2023. Histopathological analysis of both the tongue specimen and neck dissection specimen was done in the department of pathology at the same institute. DOI was measured in all these patients as per the new CAP guidelines and is recorded in millimetres. Patient characteristics and clinical findings are summarized in Table 1, and pathologic characteristics are summarised in Table 2

Table 1 Patient characteristics
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Table 2 Pathologic characteristics
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Results

The DOI of the specimens examined varied from 1 to 14 mm. The nodal positivity varied from 0 to 75%. Table 3 shows the distribution of specimens according to the DOI and nodal positivity.

Table 3 Distribution of specimens according to depth of invasion
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The coefficient of correlation between depth of invasion and nodal positivity rate is 0.89. The same data when plotted as a graph enabled us to chart a trend line on it. From this line, we calculated that the lymph node positivity rate exceeds 15% when the DOI exceeds 4 mm (Fig. 3).

Fig. 3
figure 3

Trendline for lymph node positivity vs DOI

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We also examined how addition of DOI to TNM staging in the AJCC 8th edition has changed the staging of the tumours from AJCC 7th edition. The new staging results in tumours getting upstaged compared to the 7th staging. 28 out of 47 T1 tumours (59.5%) and 19 out of 67 T2 (28.4%) tumours as per AJCC 7th have upstaged when AJCC 8th edition has been used for staging (Table 4).

Table 4 T staging (AJCC 7th Vs 8th Editions)
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Discussion

Since 1986 several studies have looked into tumour thickness as a predictor of lymph node metastasis in the clinically N0 neck. Weiss et al. used decision tree analysis to suggest that if the incidence of occult metastasis is more than 15% then it is worthwhile doing elective neck dissection in N0 neck [10]. Fukano et al. concluded that above 5 mm tumour thickness the incidence of occult metastasis in the N0 neck is high enough to warrant elective neck dissection in these cases [5]. A review of different definitions used for tumour thickness and depth of invasion was done by Pentenero et al. [12]. Moore et al. in 1986 defined tumour thickness from the level of the surface of adjacent uninvolved epithelium to deepest point of tumour [13]. Woolgar et al. recommended measuring depth from the surface of the epithelium of the adjacent non-ulcerated mucosal surface but termed it depth of invasion instead of tumour thickness. This increased DOI compared to TT in ulcerated tumours and decreased DOI compared to TT in polypoidal tumours [14].

DOI correlates strongly with nodal positivity as shown in our data. The addition of DOI to T staging in the 8th edition of AJCC has resulted in significant upstaging of tumours. This will result in larger number of patients receiving adjuvant treatment after surgery. We believe the addition of DOI to staging captures the aggressiveness of oral cancer better and is a better staging guideline.