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Prognostic Value of Radiologic Extranodal Extension in Human Papillomavirus-Related Oropharyngeal Squamous Cell Carcinoma

  • Boeun Lee (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Young Jun Choi (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Seon-Ok Kim (Department of Clinical Epidemiology and Biostatistics, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Yoon Se Lee (Department of Otolaryngology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Jung Yong Hong (Department of Oncology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Jung Hwan Baek (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Jeong Hyun Lee (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine)
  • Received : 2018.10.23
  • Accepted : 2019.05.02
  • Published : 2019.08.01

Abstract

Objective: To determine whether radiologic extranodal extension (ENE) appearing on pretreatment CT and MRI could predict the prognosis in patients with human papillomavirus (HPV)-related oropharyngeal squamous cell carcinoma (OPSCC). Materials and Methods: The study population was obtained from a historical cohort diagnosed with HPV-related OPSCC. A total of 134 OPSCC patients who had a metastatic lymph node on pretreatment CT or MRI were included, and radiologic ENE was evaluated by two experienced head and neck radiologists. Kaplan-Meier and multivariate Cox regression analyses were performed to evaluate the impact of radiologic ENE on progression-free survival (PFS). The diagnostic performance of CT and MRI for the diagnosis of ENE was also evaluated in patients who underwent neck dissection. Results: Seventy patients (52.2%) showed radiologic ENE-positive findings. Although patients showing radiologic ENE had a worse 3-year PFS (83.7% vs. 95.3%, p = 0.023), the association between radiologic ENE and PFS was not statistically significant on multivariate analysis (p = 0.141; hazard ratio, 2.68; 95% confidence interval, 0.72-9.97). CT or MRI had a sensitivity of 62%, specificity of 77.8%, and accuracy of 71.9% for predicting pathologic ENE. Conclusion: Radiologic ENE on CT or MRI did not predict poor PFS in patients with HPV-related OPSCC, although there was a trend towards worse PFS. Further studies are warranted to determine whether radiologic ENE is a useful imaging biomarker to risk-stratify patients with HPV-related OPSCC.

Keywords

References

  1. Gillison ML, Chaturvedi AK, Anderson WF, Fakhry C. Epidemiology of human papillomavirus-positive head and neck squamous cell carcinoma. J Clin Oncol 2015;33:3235-3242 https://doi.org/10.1200/JCO.2015.61.6995
  2. Pytynia KB, Dahlstrom KR, Sturgis EM. Epidemiology of HPV-associated oropharyngeal cancer. Oral Oncol 2014;50:380-386 https://doi.org/10.1016/j.oraloncology.2013.12.019
  3. Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, et al. AJCC cancer staging manual, 8th ed. New York, NY: springer, 2017
  4. Haughey BH, Sinha P. Prognostic factors and survival unique to surgically treated p16+ oropharyngeal cancer. Laryngoscope 2012;122 Suppl 2:S13-S33 https://doi.org/10.1002/lary.23493
  5. Lydiatt WM, Patel SG, O'Sullivan B, Brandwein MS, Ridge JA, Migliacci JC, et al. Head and Neck cancers-major changes in the American Joint Committee on cancer eighth edition cancer staging manual. CA Cancer J Clin 2017;67:122-137 https://doi.org/10.3322/caac.21389
  6. Wreesmann VB, Katabi N, Palmer FL, Montero PH, Migliacci JC, Gonen M, et al. Influence of extracapsular nodal spread extent on prognosis of oral squamous cell carcinoma. Head Neck 2016;38 Suppl 1:E1192-E1199 https://doi.org/10.1002/hed.24190
  7. Sinha P, Lewis JS Jr, Piccirillo JF, Kallogjeri D, Haughey BH. Extracapsular spread and adjuvant therapy in human papillomavirus-related, p16-positive oropharyngeal carcinoma. Cancer 2012;118:3519-3530 https://doi.org/10.1002/cncr.26671
  8. Myers JN, Greenberg JS, Mo V, Roberts D. Extracapsular spread. A significant predictor of treatment failure in patients with squamous cell carcinoma of the tongue. Cancer 2001;92:3030-3036 https://doi.org/10.1002/1097-0142(20011215)92:12<3030::AID-CNCR10148>3.0.CO;2-P
  9. Prabhu RS, Magliocca KR, Hanasoge S, Aiken AH, Hudgins PA, Hall WA, et al. Accuracy of computed tomography for predicting pathologic nodal extracapsular extension in patients with head-and-neck cancer undergoing initial surgical resection. Int J Radiat Oncol Biol Phys 2014;88:122-129 https://doi.org/10.1016/j.ijrobp.2013.10.002
  10. Ragin CC, Taioli E. Survival of squamous cell carcinoma of the head and neck in relation to human papillomavirus infection: review and meta-analysis. Int J Cancer 2007;121:1813-1820 https://doi.org/10.1002/ijc.22851
  11. Kaka AS, Kumar B, Kumar P, Wakely PE Jr, Kirsch CM, Old MO, et al. Highly aggressive human papillomavirus-related oropharyngeal cancer: clinical, radiologic, and pathologic characteristics. Oral Surg Oral Med Oral Pathol Oral Radiol 2013;116:327-335 https://doi.org/10.1016/j.oooo.2013.04.011
  12. Spector ME, Gallagher KK, Light E, Ibrahim M, Chanowski EJ, Moyer JS, et al.; University of Michigan Head Neck Specialized Program of Research Excellence (SPORE) Program. Matted nodes: poor prognostic marker in oropharyngeal squamous cell carcinoma independent of HPV and EGFR status. Head Neck 2012;34:1727-1733
  13. Huang SH, Perez-Ordonez B, Liu FF, Waldron J, Ringash J, Irish J, et al. Atypical clinical behavior of p16-confirmed HPV-related oropharyngeal squamous cell carcinoma treated with radical radiotherapy. Int J Radiat Oncol Biol Phys 2012;82:276-283 https://doi.org/10.1016/j.ijrobp.2010.08.031
  14. Rath TJ, Narayanan S, Hughes MA, Ferris RL, Chiosea SI, Branstetter BF 4th. Solid lymph nodes as an imaging biomarker for risk stratification in human papillomavirus-related oropharyngeal squamous cell carcinoma. AJNR Am J Neuroradiol 2017;38:1405-1410 https://doi.org/10.3174/ajnr.A5177
  15. Liu JT, Kann BH, De B, Buckstein M, Bakst RL, Genden EM, et al. Prognostic value of radiographic extracapsular extension in locally advanced head and neck squamous cell cancers. Oral Oncol 2016;52:52-57 https://doi.org/10.1016/j.oraloncology.2015.11.008
  16. Lee KC, Moon WK, Chung JW, Choi SH, Cho N, Cha JH, et al. Assessment of lymph node metastases by contrast-enhanced MR imaging in a head and neck cancer model. Korean J Radiol 2007;8:9-14 https://doi.org/10.3348/kjr.2007.8.1.9
  17. Vandenbroucke JP, von Elm E, Altman DG, Gotzsche PC, Mulrow CD, Pocock SJ, et al.; STROBE Initiative. Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. PLoS Med 2007;4:e297
  18. Lee S, Lee SW, Park S, Yoon SM, Park JH, Song SY, et al. Refining prognostic stratification of human papillomavirus-related oropharyngeal squamous cell carcinoma: different prognosis between T1 and T2. Radiat Oncol J 2017;35:233-240 https://doi.org/10.3857/roj.2017.00465
  19. Sargent DJ, Wieand HS, Haller DG, Gray R, Benedetti JK, Buyse M, et al. Disease-free survival versus overall survival as a primary end point for adjuvant colon cancer studies: individual patient data from 20,898 patients on 18 randomized trials. J Clin Oncol 2005;23:8664-8670 https://doi.org/10.1200/JCO.2005.01.6071
  20. Chai RL, Rath TJ, Johnson JT, Ferris RL, Kubicek GJ, Duvvuri U, et al. Accuracy of computed tomography in the prediction of extracapsular spread of lymph node metastases in squamous cell carcinoma of the head and neck. JAMA Otolaryngol Head Neck Surg 2013;139:1187-1194 https://doi.org/10.1001/jamaoto.2013.4491
  21. Souter MA, Allison RS, Clarkson JH, Cowan IA, Coates MH, Wells JE. Sensitivity and specificity of computed tomography for detection of extranodal spread from metastatic head and neck squamous cell carcinoma. J Laryngol Otol 2009;123:778-782 https://doi.org/10.1017/S0022215109004332
  22. Som PM, Brandwein-Gensler MS. Lymph nodes of the neck. In: Som PM, Curtin HD, eds. Head and neck imaging, 5th ed. St. Louis, MO: Mosby, 2011:2287-2384
  23. Patel MR, Hudgins PA, Beitler JJ, Magliocca KR, Griffith CC, Liu Y, et al. Radiographic imaging does not reliably predict macroscopic extranodal extension in human papilloma virus-associated oropharyngeal cancer. ORL J Otorhinolaryngol Relat Spec 2018;80:85-95 https://doi.org/10.1159/000487239
  24. Huang YH, Yeh CH, Cheng NM, Lin CY, Wang HM, Ko SF, et al. Cystic nodal metastasis in patients with oropharyngeal squamous cell carcinoma receiving chemoradiotherapy: relationship with human papillomavirus status and failure patterns. PLoS One 2017;12:e0180779
  25. Kundel HL, Polansky M. Measurement of observer agreement. Radiology 2003;228:303-308 https://doi.org/10.1148/radiol.2282011860
  26. Kim S, Lee JW, Chai JW, Yoo HJ, Kang Y, Seo J, et al. A new MRI grading system for cervical foraminal stenosis based on axial T2-weighted images. Korean J Radiol 2015;16:1294-1302 https://doi.org/10.3348/kjr.2015.16.6.1294
  27. Park JE, Han K, Sung YS, Chung MS, Koo HJ, Yoon HM, et al. Selection and reporting of statistical methods to assess reliability of a diagnostic test: conformity to recommended methods in a peer-reviewed journal. Korean J Radiol 2017;18:888-897 https://doi.org/10.3348/kjr.2017.18.6.888
  28. Geltzeiler M, Clayburgh D, Gleysteen J, Gross ND, Hamilton B, Andersen P, et al. Predictors of extracapsular extension in HPV-associated oropharyngeal cancer treated surgically. Oral Oncol 2017;65:89-93 https://doi.org/10.1016/j.oraloncology.2016.12.025
  29. Mermod M, Tolstonog G, Simon C, Monnier Y. Extracapsular spread in head and neck squamous cell carcinoma: a systematic review and meta-analysis. Oral Oncol 2016;62:60-71 https://doi.org/10.1016/j.oraloncology.2016.10.003
  30. Maxwell JH, Rath TJ, Byrd JK, Albergotti WG, Wang H, Duvvuri U, et al. Accuracy of computed tomography to predict extracapsular spread in p16-positive squamous cell carcinoma. Laryngoscope 2015;125:1613-1618 https://doi.org/10.1002/lary.25140
  31. Mizumachi T, Homma A, Sakashita T, Kano S, Hatakeyama H, Fukuda S. Confirmation of the eighth edition of the AJCC/UICC TNM staging system for HPV-mediated oropharyngeal cancer in Japan. Int J Clin Oncol 2017;22:682-689 https://doi.org/10.1007/s10147-017-1107-0