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Neuroradiology

, Volume 61, Issue 12, pp 1415–1424 | Cite as

Discrimination of HPV status using CT texture analysis: tumour heterogeneity in oropharyngeal squamous cell carcinomas

  • Ji Young Lee
  • Miran HanEmail author
  • Kap Seon Kim
  • Su-Jin Shin
  • Jin Wook Choi
  • Eun Ju Ha
Head-Neck-ENT Radiology

Abstract

Purpose

To evaluate the diagnostic performance of texture analysis for discriminating human papillomavirus (HPV) status in patients with oropharyngeal squamous cell carcinoma (OPSCC) in the primary tumours and metastatic lymph nodes.

Methods

Ninety-five patients with primary tumour and 91 with metastatic lymph nodes with confirmed HPV status, who underwent pretreatment contrast-enhanced CT (CECT), were included as the discovery population. CT texture analysis was performed using commercially available software. Differences between HPV-positive and HPV-negative groups were analysed using the χ2 test (or Mann-Whitney U test) and independent t test (or Fisher’s exact test). ROC curve analysis was performed to discriminate HPV status according to heterogeneity parameters. Diagnostic accuracy was evaluated in the separate validation population (n = 36) from an outside hospital.

Results

HPV positivity was 52.6% for primary tumours and 56.0% for metastatic lymph nodes. The entropy and standard deviation (SD) values in the HPV-positive group were significantly lower. Entropy using the medium filter was the best discriminator between HPV-positive and HPV-negative primary OPSCCs (AUC, 0.85) and SD without the filter for metastatic lymph nodes (AUC, 0.82). Diagnostic accuracy of entropy for the primary tumour was 80.0% in the discovery group and 75.0% in the validation group. In cases of metastatic lymph node, the accuracy of SD was 79.1% and 78.8%, respectively.

Conclusion

Significant differences were found in heterogeneity parameters from texture analysis of pretreatment CECT, according to HPV status. Texture analysis could be used as an adjunctive tool for diagnosis of HPV status in clinical practice.

Keywords

Squamous cell carcinoma Oropharyngeal cancer Human papilloma virus Computed tomography 

Notes

Funding information

The authors state that this work has not received any funding.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

For this retrospective study, formal consent is not required.

Informed consent

Written informed consent was waived by the Institutional Review Board. Institutional Review Board approval was obtained (AJIRB-MED-MDB-18-235 and HYUH 2018-08-015)

Supplementary material

234_2019_2295_MOESM1_ESM.docx (23 kb)
ESM 1 (DOCX 23 kb)

References

  1. 1.
    Ang KK, Sturgis EM (2012) Human papillomavirus as a marker of the natural history and response to therapy of head and neck squamous cell carcinoma. Semin Radiat Oncol 22:128–142CrossRefGoogle Scholar
  2. 2.
    Lydiatt WM, Patel SG, O'Sullivan B et al (2017) Head and Neck cancers-major changes in the American Joint Committee on cancer eighth edition cancer staging manual. CA Cancer J Clin 67:122–137CrossRefGoogle Scholar
  3. 3.
    Amin MB, Greene FL, Edge SB et al (2017) The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin 67:93–99CrossRefGoogle Scholar
  4. 4.
    Ang KK, Harris J, Wheeler R et al (2010) Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 363:24–35CrossRefGoogle Scholar
  5. 5.
    Marur S, D'Souza G, Westra WH, Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11:781–789CrossRefGoogle Scholar
  6. 6.
    Boscolo-Rizzo P, Pawlita M, Holzinger D (2016) From HPV-positive towards HPV-driven oropharyngeal squamous cell carcinomas. Cancer Treat Rev 42:24–29CrossRefGoogle Scholar
  7. 7.
    Mirghani H, Amen F, Blanchard P et al (2015) Treatment de-escalation in HPV-positive oropharyngeal carcinoma: ongoing trials, critical issues and perspectives. Int J Cancer 136:1494–1503CrossRefGoogle Scholar
  8. 8.
    Rath TJ, Narayanan S, Hughes MA, Ferris RL, Chiosea SI, Branstetter BF (2017) Solid lymph nodes as an imaging biomarker for risk stratification in human papillomavirus-related oropharyngeal squamous cell carcinoma. AJNR Am J Neuroradiol 38:1405–1410CrossRefGoogle Scholar
  9. 9.
    Cantrell SC, Peck BW, Li G, Wei Q, Sturgis EM, Ginsberg LE (2013) Differences in imaging characteristics of HPV-positive and HPV-Negative oropharyngeal cancers: a blinded matched-pair analysis. AJNR Am J Neuroradiol 34:2005–2009CrossRefGoogle Scholar
  10. 10.
    Goldenberg D, Begum S, Westra WH et al (2008) Cystic lymph node metastasis in patients with head and neck cancer: an HPV-associated phenomenon. Head Neck 30:898–903CrossRefGoogle Scholar
  11. 11.
    Corey AS, Hudgins PA (2012) Radiographic imaging of human papillomavirus related carcinomas of the oropharynx. Head Neck Pathol 6(Suppl 1):S25–S40CrossRefGoogle Scholar
  12. 12.
    Han M, Lee SJ, Lee D, Kim SY, Choi JW (2018) Correlation of human papilloma virus status with quantitative perfusion/diffusion/metabolic imaging parameters in the oral cavity and oropharyngeal squamous cell carcinoma: comparison of primary tumour sites and metastatic lymph nodes. Clin Radiol 73:757.e721-757.e727Google Scholar
  13. 13.
    Choi YS, Park M, Kwon HJ, Koh YW, Lee SK, Kim J (2016) Human papillomavirus and epidermal growth factor receptor in oral cavity and oropharyngeal squamous cell carcinoma: correlation with dynamic contrast-enhanced MRI parameters. AJR Am J Roentgenol 206:408–413CrossRefGoogle Scholar
  14. 14.
    Ravanelli M, Grammatica A, Tononcelli E et al (2018) Correlation between human papillomavirus status and quantitative MR imaging parameters including diffusion-weighted imaging and texture features in oropharyngeal carcinoma. AJNR Am J Neuroradiol 39:1878–1883CrossRefGoogle Scholar
  15. 15.
    Schouten CS, de Graaf P, Bloemena E et al (2015) Quantitative diffusion-weighted MRI parameters and human papillomavirus status in oropharyngeal squamous cell carcinoma. AJNR Am J Neuroradiol 36:763–767CrossRefGoogle Scholar
  16. 16.
    Nakahira M, Saito N, Yamaguchi H, Kuba K, Sugasawa M (2014) Use of quantitative diffusion-weighted magnetic resonance imaging to predict human papilloma virus status in patients with oropharyngeal squamous cell carcinoma. Eur Arch Otorhinolaryngol 271:1219–1225CrossRefGoogle Scholar
  17. 17.
    Driessen JP, van Bemmel AJ, van Kempen PM et al (2016) Correlation of human papillomavirus status with apparent diffusion coefficient of diffusion-weighted MRI in head and neck squamous cell carcinomas. Head Neck 38(Suppl 1):E613–E618CrossRefGoogle Scholar
  18. 18.
    Schouten CS, Hakim S, Boellaard R et al (2016) Interaction of quantitative (18)F-FDG-PET-CT imaging parameters and human papillomavirus status in oropharyngeal squamous cell carcinoma. Head Neck 38:529–535CrossRefGoogle Scholar
  19. 19.
    Tahari AK, Alluri KC, Quon H, Koch W, Wahl RL, Subramaniam RM (2014) FDG PET/CT imaging of oropharyngeal squamous cell carcinoma: characteristics of human papillomavirus-positive and -negative tumors. Clin Nucl Med 39:225–231CrossRefGoogle Scholar
  20. 20.
    Ganeshan B, Panayiotou E, Burnand K, Dizdarevic S, Miles K (2012) Tumour heterogeneity in non-small cell lung carcinoma assessed by CT texture analysis: a potential marker of survival. Eur Radiol 22:796–802CrossRefGoogle Scholar
  21. 21.
    Ganeshan B, Goh V, Mandeville HC, Ng QS, Hoskin PJ, Miles KA (2013) Non-small cell lung cancer: histopathologic correlates for texture parameters at CT. Radiology 266:326–336CrossRefGoogle Scholar
  22. 22.
    Yip C, Landau D, Kozarski R et al (2014) Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology 270:141–148CrossRefGoogle Scholar
  23. 23.
    Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K (2012) Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol 67:157–164CrossRefGoogle Scholar
  24. 24.
    Ng F, Ganeshan B, Kozarski R, Miles KA, Goh V (2013) Assessment of primary colorectal cancer heterogeneity by using whole-tumor texture analysis: contrast-enhanced CT texture as a biomarker of 5-year survival. Radiology 266:177–184CrossRefGoogle Scholar
  25. 25.
    Zhang H, Graham CM, Elci O et al (2013) Locally advanced squamous cell carcinoma of the head and neck: CT texture and histogram analysis allow independent prediction of overall survival in patients treated with induction chemotherapy. Radiology 269:801–809CrossRefGoogle Scholar
  26. 26.
    Kuno H, Qureshi MM, Chapman MN et al (2017) CT texture analysis potentially predicts local failure in head and neck squamous cell carcinoma treated with chemoradiotherapy. AJNR Am J Neuroradiol 38:2334–2340CrossRefGoogle Scholar
  27. 27.
    Skogen K, Ganeshan B, Good C, Critchley G, Miles K (2013) Measurements of heterogeneity in gliomas on computed tomography relationship to tumour grade. J Neurooncol 111:213–219CrossRefGoogle Scholar
  28. 28.
    Buch K, Fujita A, Li B, Kawashima Y, Qureshi MM, Sakai O (2015) Using texture analysis to determine human papillomavirus status of oropharyngeal squamous cell carcinomas on CT. AJNR Am J Neuroradiol 36:1343–1348CrossRefGoogle Scholar
  29. 29.
    Huang SH, O'Sullivan B (2017) Overview of the 8th Edition TNM Classification for Head and Neck Cancer. Curr Treat Options Oncol 18:40CrossRefGoogle Scholar
  30. 30.
    Chaudhary AK, Pandya S, Mehrotra R, Bharti AC, Singh M, Singh M (2010) Comparative study between the Hybrid Capture II test and PCR based assay for the detection of human papillomavirus DNA in oral submucous fibrosis and oral squamous cell carcinoma. Virol J 7:253CrossRefGoogle Scholar
  31. 31.
    Burd EM (2016) Human papillomavirus laboratory testing: the changing paradigm. Clin Microbiol Rev 29:291–319CrossRefGoogle Scholar
  32. 32.
    Schache A, Croud J, Robinson M, Thavaraj S (2014) Human papillomavirus testing in head and neck squamous cell carcinoma: best practice for diagnosis. Methods Mol Biol 1180:237–255CrossRefGoogle Scholar
  33. 33.
    Ng F, Kozarski R, Ganeshan B, Goh V (2013) Assessment of tumor heterogeneity by CT texture analysis: can the largest cross-sectional area be used as an alternative to whole tumor analysis? Eur J Radiol 82:342–348CrossRefGoogle Scholar
  34. 34.
    Gonen M, Panageas KS, Larson SM (2001) Statistical issues in analysis of diagnostic imaging experiments with multiple observations per patient. Radiology 221:763–767CrossRefGoogle Scholar
  35. 35.
    Galbraith S, Daniel JA, Vissel B (2010) A study of clustered data and approaches to its analysis. J Neurosci 30:10601–10608CrossRefGoogle Scholar
  36. 36.
    Miles KA, Ganeshan B, Hayball MP (2013) CT texture analysis using the filtration-histogram method: what do the measurements mean? Cancer Imaging 13:400–406CrossRefGoogle Scholar
  37. 37.
    Lubner MG, Smith AD, Sandrasegaran K, Sahani DV, Pickhardt PJ (2017) CT texture analysis: definitions, applications, biologic correlates, and challenges. Radiographics 37:1483–1503CrossRefGoogle Scholar
  38. 38.
    Ganeshan B, Miles KA, Young RC, Chatwin CR (2009) Texture analysis in non-contrast enhanced CT: impact of malignancy on texture in apparently disease-free areas of the liver. Eur J Radiol 70:101–110CrossRefGoogle Scholar
  39. 39.
    Ganeshan B, Miles KA, Young RC, Chatwin CR (2007) In search of biologic correlates for liver texture on portal-phase CT. Acad Radiol 14:1058–1068CrossRefGoogle Scholar
  40. 40.
    El-Mofty SK, Zhang MQ, Davila RM (2008) Histologic identification of human papillomavirus (HPV)-related squamous cell carcinoma in cervical lymph nodes: a reliable predictor of the site of an occult head and neck primary carcinoma. Head Neck Pathol 2:163–168CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of RadiologyHanyang University Medical CenterSeoulRepublic of Korea
  2. 2.Department of Radiology, Ajou University School of MedicineAjou University Medical CenterSuwonRepublic of Korea
  3. 3.Department of PathologyHanyang University Medical CenterSeoulRepublic of Korea

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