Skip to main content

Advertisement

Log in

CT assessment of tumor heterogeneity and the potential for the prediction of human papillomavirus status in oropharyngeal squamous cell carcinoma

  • COMPUTED TOMOGRAPHY
  • Published:
La radiologia medica Aims and scope Submit manuscript

Abstract

The aim of this study is to find a correlation between tumoral heterogeneity of squamous cell carcinoma of the oropharynx and human papillomavirus (HPV) status and to determine whether analysis of texture features of primary lesion on contrast-enhanced CT (CECT) images can be useful in predicting the HPV positivity. Fifty patients with diagnosis of oropharyngeal carcinoma and pre-treatment CECT were included; tumoral heterogeneity of each lesion was evaluated by extracting quantitative texture parameters of first and higher orders. T test and logistic regression were conducted to evaluate the effects of different textural characteristics. There were 35 HPV+ and 15 HPV− lesions. Statistically significant (p < 0.05) differences were seen in multiple higher-order extracted parameters. The logistic regression model correctly classified lesions with an accuracy of 95.2%. CT texture analysis of primary oropharyngeal cancer may be used as a tool for predicting the HPV status.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Marur S, D’Souza G, Westra WH, Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11:781–789. https://doi.org/10.1016/S1470-2045(10)70017-6

    Article  PubMed  PubMed Central  Google Scholar 

  2. Gillison ML, Chaturvedi AK, Anderson WF, Fakhry C (2015) Epidemiology of human papillomavirus-positive head and neck squamous cell carcinoma. J Clin Oncol 33:3235–3242. https://doi.org/10.1200/JCO.2015.61.6995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dahlstrom KR, Calzada G, Hanby JD, Garden AS, Glisson BS et al (2013) An evolution in demographics, treatment, and outcomes of oropharyngeal cancer at a major cancer center: a staging system in need of repair. Cancer 119:81–89. https://doi.org/10.1002/cncr.27727

    Article  PubMed  Google Scholar 

  4. Farsi NJ, Rousseau M-C, Schlecht N, Castonguay G, Allison P et al (2017) Aetiological heterogeneity of head and neck squamous cell carcinomas: the role of human papillomavirus infections, smoking, and alcohol. Carcinogenesis 38:1188–1195. https://doi.org/10.1093/carcin/bgx106

    Article  CAS  PubMed  Google Scholar 

  5. Ragin CCR, Taioli E (2007) Survival of squamous cell carcinoma of the head and neck in relation to human papillomavirus infection: review and meta-analysis. Int J Cancer 121:1813–1820. https://doi.org/10.1002/ijc.22851

    Article  CAS  PubMed  Google Scholar 

  6. Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446. https://doi.org/10.1016/j.ejca.2011.11.036

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kumar V, Gu Y, Basu S, Berglund A, Eschrich SA et al (2012) Radiomics: the process and the challenges. Magn Reson Imaging 30:1234–1248. https://doi.org/10.1016/j.mri.2012.06.010

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bashir U, Siddique MM, McLean E, Goh V, Cook GJ (2016) Imaging heterogeneity in lung cancer: techniques, applications, and challenges. AJR Am J Roentgenol 207:534–543. https://doi.org/10.2214/AJR.15.15864

    Article  PubMed  Google Scholar 

  9. Lubner MG, Smith AD, Sandrasegaran K, Sahani DV, Pickhardt PJ (2017) CT texture analysis: definitions, applications, biologic correlates, and challenges. RadioGraphics 37:1483–1503. https://doi.org/10.1148/rg.2017170056

    Article  PubMed  Google Scholar 

  10. Nioche C, Orlhac F, Boughdad S, Reuze S, Soussan M et al (2017) A freeware for tumor heterogeneity characterization in PET, SPECT, CT, MRI and US to accelerate advances in radiomics. J Nucl Med 58:1316

    Google Scholar 

  11. Tixier F, Hatt M, Le Rest CC, Le Pogam A, Corcos L, Visvikis D (2012) Reproducibility of tumor uptake heterogeneity characterization through textural feature analysis in 18F-FDG PET. J Nucl Med 53:693–700. https://doi.org/10.2967/jnumed.111.099127

    Article  PubMed  PubMed Central  Google Scholar 

  12. Haralick R, Shanmugan K, Dinstein I (1973) Textural features for image classification. IEEE Trans Syst Man Cybern 3:610–621

    Article  Google Scholar 

  13. Thibault G, Fertil B, Navarro C, Pereira S, Cau P et al (2009) Texture indexes and gray level size zone matrix application to cell nuclei classification. In: 10th International Conference on Pattern Recognition and Information Processing. Minsk, Belarus, pp 140–145

  14. Amadasun M, King R (1989) Textural features corresponding to textural properties. IEEE Trans. Syst Man Cybern 19:1264–1274. https://doi.org/10.1109/21.44046

    Article  Google Scholar 

  15. Braakhuis BJM, Snijders PJF, Keune W-JH, Meijer CJ, Ruijter-Schippers HJ et al (2004) Genetic patterns in head and neck cancers that contain or lack transcriptionally active human papillomavirus. JNCI J Natl Cancer Inst 96:998–1006

    Article  CAS  Google Scholar 

  16. Kuo K-T, Hsiao C-H, Lin C-H, Kuo L-T, Huang S-H, Lin M-C (2008) The biomarkers of human papillomavirus infection in tonsillar squamous cell carcinoma-molecular basis and predicting favorable outcome. Mod Pathol 21:376–386. https://doi.org/10.1038/modpathol.380097

    Article  CAS  PubMed  Google Scholar 

  17. Karpathiou G, Monaya A, Forest F, Froudarakis M, Casteillo F et al (2016) P16 and P53 expression status in head and neck squamous cell carcinoma: a correlation with histological, histoprognostic and clinical parameters. Pathology 48:341–348. https://doi.org/10.1016/j.pathol.2016.01.005

    Article  CAS  PubMed  Google Scholar 

  18. Chernock RD, El-Mofty SK, Thorstad WL, Parvin CA, Lewis JS (2009) HPV-related nonkeratinizing squamous cell carcinoma of the oropharynx: utility of microscopic features in predicting patient outcome. Head Neck Pathol 3:186–194. https://doi.org/10.1007/s12105-009-0126-1

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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 34:2005–2009. https://doi.org/10.3174/ajnr.A3524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Goldenberg D, Begum S, Westra WH, Khan Z, Sciubba J et al (2008) Cystic lymph node metastasis in patients with head and neck cancer: an HPV-associated phenomenon. Head Neck 30:898–903. https://doi.org/10.1002/hed.20796

    Article  PubMed  Google Scholar 

  21. Morani AC, Eisbruch A, Carey TE, Hauff SJ, Walline HM, Mukherji SK (2014) Intranodal cystic changes: a potential radiologic signature/biomarker to assess the human papillomavirus status of cases with oropharyngeal malignancies. J Comput Assist Tomogr 37:343–345. https://doi.org/10.1097/RCT.0b013e318282d7c3

    Article  Google Scholar 

  22. O‘Sullivan B, Lydiatt WM, Haughey B, Brandwein-Gensler M, Glastonbury CM, Shah JP (2017) HPV-mediated (p16+) oropharyngeal cancer. In: Amin MB, Edge SB, Greene FL (eds) AJCC cancer staging manual, 8th edn. Springer, New York, pp 113–121

    Chapter  Google Scholar 

  23. 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. Am J Neuroradiol 36:1343–1348. https://doi.org/10.3174/ajnr.A4285

    Article  CAS  PubMed  Google Scholar 

  24. Fujita A, Buch K, Li B, Kawashima Y, Qureshi MM, Sakai O (2016) Difference between HPV-positive and HPV-negative non-oropharyngeal head and neck cancer. J Comput Assist Tomogr 40:43–47. https://doi.org/10.1097/RCT.0000000000000320

    Article  PubMed  Google Scholar 

  25. Bogowicz M, Riesterer O, Ikenberg K, Stieb S, Moch H et al (2017) Computed tomography radiomics predicts HPV status and local tumor control after definitive radiochemotherapy in head and neck squamous cell carcinoma. Int J Radiat Oncol Biol Phys 99:921–928. https://doi.org/10.1016/j.ijrobp.2017.06.002

    Article  PubMed  Google Scholar 

  26. Kuno H, Qureshi MM, Chapman MN, Li B, Andreu-Arasa VC et al (2017) CT texture analysis potentially predicts local failure in head and neck squamous cell carcinoma treated with chemoradiotherapy. AJNR Am J Neuroradiol 38:2334–2340. https://doi.org/10.3174/ajnr.A5407

    Article  CAS  PubMed  Google Scholar 

  27. Ranjbar S, Ning S, Zwart CM, Wood CP, Weindling SM et al (2018) Computed tomography-based texture analysis to determine human papillomavirus status of oropharyngeal squamous cell carcinoma. J Comput Assist Tomogr 42:299–305. https://doi.org/10.1097/RCT.0000000000000682

    Article  PubMed  Google Scholar 

  28. Grove O, Berglund AE, Schabath MB, Aerts HJ, Dekker A et al (2015) Quantitative computed tomographic descriptors associate tumor shape complexity and intratumor heterogeneity with prognosis in lung adenocarcinoma. PLoS ONE 10:e0118261. https://doi.org/10.1371/journal.pone.0118261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luigi Bonasera.

Ethics declarations

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. Informed consent was obtained from all individual participants included in the study.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mungai, F., Verrone, G.B., Pietragalla, M. et al. CT assessment of tumor heterogeneity and the potential for the prediction of human papillomavirus status in oropharyngeal squamous cell carcinoma. Radiol med 124, 804–811 (2019). https://doi.org/10.1007/s11547-019-01028-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11547-019-01028-6

Keywords

Navigation