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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 8  |  Issue : 3  |  Page : 62-65

Analysis of tongue squamous cell carcinoma with Doppler sonography and strain elastography using intraoral ultrasonography


1 Comprehensive Dental Care, The Nippon Dental University Niigata Hospital, Niigata, Japan
2 Department of Oral and Maxillofacial Radiology, The Nippon Dental University School of Life Dentistry at Niigata, Niigata, Japan
3 Department of Pathology, The Nippon Dental University School of Life Dentistry at Niigata, Niigata, Japan

Date of Submission09-Dec-2020
Date of Decision02-Jan-2021
Date of Acceptance12-Jan-2021
Date of Web Publication26-Feb-2021

Correspondence Address:
Ichiro Ogura
Department of Oral and Maxillofacial Radiology, The Nippon Dental University School of Life Dentistry at Niigata, 1-8 Hamaura-cho, Chuo-Ku, Niigata, Niigata
Japan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jomr.jomr_26_20

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  Abstract 


Background: Depth of invasion (DOI) in oral carcinoma has been integrated into the primary tumor categories in the current tumor-node metastasis staging, and intraoral ultrasonography provides sufficient accuracy for the measurement of tumor DOI in oral tongue carcinoma. Aims: The objectives of this study were to analyze the tongue squamous cell carcinoma (SCC) with Doppler sonography and strain elastography using intraoral ultrasonography. Materials and Methods: Six patients with tongue SCC who underwent Doppler sonography and strain elastography using intraoral ultrasonography were prospectively included. Doppler sonography and strain elastography using intraoral ultrasonography were obtained with a linear 14 MHz transducer using our protocol. The tumor thickness using ultrasonography and tumor with/without vascular signals were evaluated by the Mann–Whitney U-test. The relationship between tumor thickness using ultrasonography and pathological tumor thickness and DOI was assessed by the Pearson's rank correlation test. P values lower than 0.05 indicate statistically significant differences. Results: The tumor thickness using ultrasonography in the vascular signal's presence group (5.8 ± 1.4 mm) was larger than that of the absence group (3.1 ± 1.5 mm, P = 0.050). The strain values of tumor and control in the tongue SCC were 0% and 0.534% ± 0.236%, respectively. Tumor thickness using ultrasonography was correlated with pathological tumor thickness (r = 0.811, P = 0.050) and pathological DOI (r = 0.599, P = 0.209), respectively. Conclusions: Doppler sonography and strain elastography using intraoral ultrasonography are useful for the analysis of tongue SCC.

Keywords: Depth of invasion, elasticity imaging techniques, tongue squamous cell carcinoma, ultrasonography


How to cite this article:
Sugawara Y, Minami Y, Ono J, Okada Y, Ogura I. Analysis of tongue squamous cell carcinoma with Doppler sonography and strain elastography using intraoral ultrasonography. J Oral Maxillofac Radiol 2020;8:62-5

How to cite this URL:
Sugawara Y, Minami Y, Ono J, Okada Y, Ogura I. Analysis of tongue squamous cell carcinoma with Doppler sonography and strain elastography using intraoral ultrasonography. J Oral Maxillofac Radiol [serial online] 2020 [cited 2021 Apr 17];8:62-5. Available from: https://www.joomr.org/text.asp?2020/8/3/62/310383




  Introduction Top


Intraoral ultrasonography is a noninvasive and easy-to-use diagnostic tool.[1] Intraoral ultrasonography is very accurate in determining tumor thickness in early oral tongue cancer.[2],[3] Intraoral ultrasonography of the tongue revealed the nature of the lesions including the border, size, location, tumor thickness, the presence or absence of a capsule, and the internal structure including vascularity of the mass.[4] Furthermore, intraoral Color Doppler sonography is recommended, as it may identify the predictive factors of cervical lymph node metastasis.[5] Vascularity as assessed by Doppler intraoral ultrasound around the invasion front of tongue cancer is a predictor of pathological grade of malignancy and cervical lymph node metastasis.[6]

Depth of invasion (DOI) in oral carcinoma has been integrated into the primary tumor categories in the current tumor-node metastasis staging, and intraoral ultrasonography provides sufficient accuracy for the measurement of tumor DOI in oral tongue carcinoma.[7] However, more experience is needs to determine if it is reliable in determining preoperative DOI.[8]

Strain elastography using intraoral ultrasonography is relatively new to sonographic imaging, and the use of intraoral strain elastography for tongue carcinoma[9] and palatal tumors[10] has been recently reported in the literature. It is a dynamic imaging technique that is simply based on the elasticity of tissues. The objectives of this study were to analyze tongue squamous cell carcinoma (SCC) with Doppler sonography and strain elastography using intraoral ultrasonography.


  Materials and Methods Top


Patient population

Between November 2017 and October 2019, six patients with tongue SCC (4 men and 2 women; mean age 68.8 years; age range, 55–81 years) who underwent Doppler sonography and strain elastography using intraoral ultrasonography at our hospital were prospectively included. The histopathological diagnoses of those lesions were made by surgery. Informed consent was obtained from patients who participated in clinical investigations. This study was approved by the Ethics Committee (ECNG-R-400).

Image acquisition and analysis

Doppler sonography and strain elastography using intraoral ultrasonography were obtained with a linear 14 MHz transducer (Aplio 300; Canon Medical Systems, Otawara, Japan) using our protocol.[9] The ultrasonography examination was performed by an oral and maxillofacial radiologist with more than 20 years of experience. Doppler sonography was performed to evaluate the tumor thickness and vascular signals within tongue tumor [Figure 1]a and [Figure 2]a. Strain values (%) by strain elastography were measured for tumor and control (normal tissue) in the tongue [Figure 1]b and [Figure 2]b. Two oral and maxillofacial pathologists reviewed all histological slides. All archival slides were stained with hematoxylin and eosin. Those slides were evaluated the differentiated, tumor thickness, and DOI [Figure 1]c, [Figure 1]d and [Figure 2]c, [Figure 2]d.
Figure 1: Case 1. Tongue squamous cell carcinoma in a 55-year-old male. (a) Doppler sonography shows tumor thickness (5.6 mm) and tumor with vascular signals. (b) Strain elastography shows strain values of tumor (T1: 0.000%) and control (R: 0.448%). (c and d) Histological slides show well-differentiated squamous cell carcinoma with exophytic growth. The maximum depth of invasion of the tumor is 1.5 mm (c, red line), and the maximum thickness is 6.4 mm (d, black line). The values are rounded off the second decimal place. Red pin: deepest portion. Light blue line: Reference plane. Scale bar: 2.5 mm

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Figure 2: Case 2. Tongue squamous cell carcinoma in a 59-year-old male. (a) Doppler sonography shows tumor thickness (3.8 mm) and tumor without vascular signals. (b) Strain elastography shows strain values of tumor (T1: 0.000%) and control (R: 0.967%). (c and d) Histological slides show well to moderately differentiated squamous cell carcinoma with exophytic and endophytic growth. The tumor invades into the muscle. The maximum depth of invasion of the tumor is 3.6 mm (c, red line), and the maximum thickness is 6.1 mm (d, black line). The values are rounded off the second decimal place. Red pin: Deepest portion. Light blue line: Reference plane. Scale bar: 5.0 mm

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Statistical analysis

The tumor thickness using ultrasonography and tumor with/without vascular signals was evaluated by the Mann–Whitney U-test. The relationship between tumor thickness using ultrasonography and pathological tumor thickness and DOI was assessed by the Pearson's rank correlation test. P values lower than 0.05 indicate significant differences using statistical software (IBM SPSS Statistics 26 (IBM Japan, Tokyo, Japan).


  Results Top


[Table 1] shows the analysis of tongue SCC with Doppler sonography and strain elastography using intraoral ultrasonography. The tumor thickness using ultrasonography in the vascular signal's presence group (5.8 ± 1.4 mm) was larger than that of the absence group (3.1 ± 1.5 mm, P = 0.050). The strain values of tumor and control in the tongue SCC were 0% and 0.534% ± 0.236%, respectively. Tumor thickness using ultrasonography was correlated with pathological tumor thickness (r = 0.811, P = 0.050) and pathological DOI (r = 0.599, P = 0.209), respectively.
Table 1: Analysis of tongue squamous cell carcinoma with Doppler sonography and strain elastography using intraoral ultrasonography

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  Discussion Top


Doppler sonography has gained wide acceptance as a valuable diagnostic aid in the evaluation of head and neck lesions.[11] In this study, we analyzed the tongue SCC with Doppler sonography and strain elastography using intraoral ultrasonography.

Ariji et al.[5] evaluated the intraoral Doppler sonographic features of tongue cancer and showed that significant differences in tumor thickness and vascular index of the tumor area were observed between patients with cervical lymph node metastasis and those without. Yamamoto et al.[6] evaluated the tongue cancer of vascularity as assessed by Doppler intraoral ultrasonography and indicated that the blood flow signal number ratio and blood flow signal width ratio of patients with cervical lymph node metastasis were significantly higher than those of patients without nodal involvement. In this study using Doppler intraoral ultrasonography, the tumor thickness using ultrasonography in the vascular signal's presence group (5.8 ± 1.4 mm) was larger than that of the absence group (3.1 ± 1.5 mm, P = 0.050). We should evaluate the relationship between Doppler sonographic features, such as vascular signal of tongue carcinoma and presence of cervical lymph node metastases as future study.

In recent years, ultrasound elastography-based imaging techniques have received substantial attention for noninvasive assessment of tissue mechanical properties and take the advantage of changed soft-tissue elasticity in various pathologies to provide quantitative information that can be used for the diagnostic purposes.[12] Cindil et al.[13] assessed the pathological sonoelastographic changes in the major salivary glands and showed that sonoelastography is a modality which can contribute to the diagnosis by improving specificity in the differential diagnosis of Sjögren's syndrome. Elbeblawy et al.[14] showed that ultrasound elastography may be potentially useful for the diagnosis of chronic inflammatory conditions of the major salivary glands. Furthermore, Ogura et al. showed that intraoral strain elastography can be useful for evaluating tongue carcinoma[9] and palatal lesions.[10] In this study using intraoral ultrasound strain elastography, the strain values of tumor and control in the tongue SCC were 0% and 0.534% ± 0.236%, respectively. We should evaluate the relationship between the strain values and tumor thickness, vascular signal of tongue carcinoma, and presence of cervical lymph node metastases as future study.

Klein Nulent et al.[2] showed that the correlation between intraoral ultrasonography and histopathological thickness measurements in tongue tumors was high (r = 0.88). Iida et al.[7] indicated that the correlation between the ultrasonography-obtained and histologically obtained DOIs was significant (r = 0.867). In this study, tumor thickness using ultrasonography was correlated with pathological tumor thickness (r = 0.811, P = 0.050) and pathological DOI (r = 0.599, P = 0.209), respectively. We concluded that intraoral ultrasonography is very accurate in determining tumor thickness in tongue carcinoma; however, more experience is needs to determine if it is reliable in determining preoperative DOI.

There were several limitations of this study. The sample was small. We consider that the most interesting point of Doppler sonography and strain elastography using intraoral ultrasonography of tongue SCC is how early to detest and diagnose tumor thickness and DOI, and those methods may identify the predictive factors of cervical lymph node metastasis. Further, research is necessary to validate these results.


  Conclusions Top


We analyzed the tongue SCC with Doppler sonography and strain elastography using intraoral ultrasonography. Doppler sonography and strain elastography using intraoral ultrasonography are useful for the analysis of tongue SCC.

Financial support and sponsorship

This work was financially supported by JSPS KAKENHI Grant Number JP 18K09754.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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2.
Klein Nulent TJ, Noorlag R, Van Cann EM, Pameijer FA, Willems SM, Yesuratnam A, et al. Intraoral ultrasonography to measure tumor thickness of oral cancer: A systematic review and meta-analysis. Oral Oncol 2018;77:29-36.  Back to cited text no. 2
    
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Sugawara C, Takahashi A, Kawano F, Kudo Y, Ishimaru N, Miyamoto Y. Intraoral ultrasonography of tongue mass lesions. Dentomaxillofac Radiol 2016;45:20150362.  Back to cited text no. 4
    
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Ariji Y, Goto M, Fukano H, Sugita Y, Izumi M, Ariji E. Role of intraoral color Doppler sonography in predicting delayed cervical lymph node metastasis in patients with early-stage tongue cancer: A pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol 2015;119:246-53.  Back to cited text no. 5
    
6.
Yamamoto C, Yuasa K, Okamura K, Shiraishi T, Miwa K. Vascularity as assessed by Doppler intraoral ultrasound around the invasion front of tongue cancer is a predictor of pathological grade of malignancy and cervical lymph node metastasis. Dentomaxillofac Radiol 2016;45:20150372.  Back to cited text no. 6
    
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Iida Y, Kamijo T, Kusafuka K, Omae K, Nishiya Y, Hamaguchi N, et al. Depth of invasion in superficial oral tongue carcinoma quantified using intraoral ultrasonography. Laryngoscope 2018;128:2778-82.  Back to cited text no. 7
    
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Ogura I, Sasaki Y, Sue M, Oda T. Strain elastography of tongue carcinoma using intraoral ultrasonography: A preliminary study to characterize normal tissues and lesions. Imaging Sci Dent 2018;48:45-9.  Back to cited text no. 9
    
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Ogura I, Toshima H, Akashiba T, Ono J, Okada Y. Strain elastography of palatal tumors in conjunction with intraoral ultrasonography, computed tomography, and magnetic resonance imaging: 2 case reports. Imaging Sci Dent 2020;50:73-9.  Back to cited text no. 10
    
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Ogura I, Kaneda T, Sasaki Y, Sekiya K, Tokunaga S. Characteristic power Doppler sonographic images of tumorous and non-tumorous buccal space lesions. Dentomaxillofac Radiol 2013;42:20120460.  Back to cited text no. 11
    
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Sigrist RM, Liau J, Kaffas AE, Chammas MC, Willmann JK. Ultrasound elastography: Review of techniques and clinical applications. Theranostics 2017;7:1303-29.  Back to cited text no. 12
    
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Cindil E, Oktar SO, Akkan K, Sendur HN, Mercan R, Tufan A, et al. Ultrasound elastography in assessment of salivary glands involvement in primary Sjögren's syndrome. Clin Imaging 2018;50:229-34.  Back to cited text no. 13
    
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Elbeblawy YM, Eshaq Amer Mohamed M. Strain and shear wave ultrasound elastography in evaluation of chronic inflammatory disorders of major salivary glands. Dentomaxillofac Radiol 2020;49:20190225.  Back to cited text no. 14
    


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