Skip to main content
SpringerLink
Log in

Prediction model for cervical lymph node metastasis in human papillomavirus-related oropharyngeal squamous cell carcinomas

  • Head and Neck
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To develop and validate a risk scoring system based on clinical and imaging findings to predict lymph node metastasis from HPV-related oropharyngeal squamous cell carcinomas.

Methods

This study population who had undergone neck dissections or lymph node biopsies in patients with HPV+ OPSCC was obtained from a historical cohort from two tertiary referral hospitals. The training set from one hospital included 455 lymph nodes from 82 patients, and the test set from the other hospital included 150 lymph nodes from 42 patients. The baseline clinical and imaging findings on pretreatment CT or MR were investigated and the reference standards were the histopathologic results. A risk scoring system was constructed based on logistic regression and validated both internally and externally.

Results

A 7-point risk scoring system was developed based on the following variables: central necrosis, infiltration of adjacent planes, lymph node level, and the maximal axial diameter of the lymph node. This risk scoring system showed good discriminative ability for metastasis in the training set (C-statistic 0.952; 95% CI, 0.931–0.972) and test set (C-statistic 0.968, 95% CI, 0.936–0.999) and good calibration ability in the training set (p = 0.723) and test set (p = 0.253).

Conclusions

We developed and validated a reliable risk scoring system that predicts lymph node metastasis from HPV+ OPSCCs based on the clinical data and pretreatment imaging findings. We expect this risk scoring system to be a useful guide for better decision-making in practice.

Key Points

• It is important to diagnose lymph node metastasis from HPV+ OPSCC for treatment planning; however, there has been little research on that.

• We developed and externally validated a new scoring system for stratifying the risk of lymph node metastasis from HPV+ OPSCC based on clinical and imaging data.

• A predictive model combining both clinical and imaging data showed high diagnostic accuracy and efficiency for lymph node metastasis from HPV+ OPSCC.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CT:

Computed tomography

HPV+ OPSCC(s):

HPV-related oropharyngeal squamous cell carcinoma(s)

MR:

Magnetic resonance imaging

References

  1. Ang KK, Harris J, Wheeler R et al (2010) Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 363:24–35

    Article  CAS  Google Scholar 

  2. Chaturvedi AK, Engels EA, Pfeiffer RM et al (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29:4294–4301

    Article  Google Scholar 

  3. O’Sullivan B, Huang SH, Su J et al (2016) Development and validation of a staging system for HPV-related oropharyngeal cancer by the International Collaboration on Oropharyngeal cancer Network for Staging (ICON-S): a multicentre cohort study. Lancet Oncol 17:440–451

    Article  Google Scholar 

  4. Chaturvedi AK, Anderson WF, Lortet-Tieulent J et al (2013) Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol 31:4550–4559

    Article  Google Scholar 

  5. 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 67:93–99

    Article  Google Scholar 

  6. Gillison ML, Broutian T, Pickard RK et al (2012) Prevalence of oral HPV infection in the United States, 2009-2010. JAMA 307:693–703

    Article  CAS  Google Scholar 

  7. Taberna M, Mena M, Pavon MA, Alemany L, Gillison ML, Mesia R (2017) Human papillomavirus-related oropharyngeal cancer. Ann Oncol 28:2386–2398

    Article  CAS  Google Scholar 

  8. Oosthuizen JC, Doody J (2019) De-intensified treatment in human papillomavirus-positive oropharyngeal cancer. Lancet 393:5–7

    Article  Google Scholar 

  9. Masterson L, Moualed D, Liu ZW et al (2014) De-escalation treatment protocols for human papillomavirus-associated oropharyngeal squamous cell carcinoma: a systematic review and meta-analysis of current clinical trials. Eur J Cancer 50:2636–2648

    Article  Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. Collins GS, Reitsma JB, Altman DG, Moons KG (2015) Transparent Reporting of a multivariable prediction model for Individual Prognosis or Diagnosis (TRIPOD): the TRIPOD statement. Ann Intern Med 162:55–63

    Article  Google Scholar 

  12. von Elm E, Altman DG, Egger M et al (2007) Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ 335:806–808

    Article  Google Scholar 

  13. Han K, Song K, Choi BW (2016) How to develop, validate, and compare clinical prediction models involving radiological parameters: study design and statistical methods. Korean J Radiol 17:339–350

    Article  Google Scholar 

  14. Steinkamp HJ, Cornehl M, Hosten N, Pegios W, Vogl T, Felix R (1995) Cervical lymphadenopathy: ratio of long- to short-axis diameter as a predictor of malignancy. Br J Radiol 68:266–270

    Article  CAS  Google Scholar 

  15. Yousem DM, Som PM, Hackney DB, Schwaibold F, Hendrix RA (1992) Central nodal necrosis and extracapsular neoplastic spread in cervical lymph nodes: MR imaging versus CT. Radiology 182:753–759

    Article  CAS  Google Scholar 

  16. Som PM (1987) Lymph nodes of the neck. Radiology 165:593–600

    Article  CAS  Google Scholar 

  17. Kaji AV, Mohuchy T, Swartz JD (1997) Imaging of cervical lymphadenopathy. Semin Ultrasound CT MR 18:220–249

    Article  CAS  Google Scholar 

  18. Som PM (1992) Detection of metastasis in cervical lymph nodes: CT and MR criteria and differential diagnosis. AJR Am J Roentgenol 158:961–969

    Article  CAS  Google Scholar 

  19. 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 30:898–903

    Article  Google Scholar 

  20. Kalnins IK, Leonard AG, Sako K, Razack MS, Shedd DP (1977) Correlation between prognosis and degree of lymph node involvement in carcinoma of the oral cavity. Am J Surg 134:450–454

    Article  CAS  Google Scholar 

  21. Mancuso AA, Harnsberger HR, Muraki AS, Stevens MH (1983) Computed tomography of cervical and retropharyngeal lymph nodes: normal anatomy, variants of normal, and applications in staging head and neck cancer. Part II: pathology. Radiology 148:715–723

    Article  CAS  Google Scholar 

  22. Snow GB, Annyas AA, van Slooten EA, Bartelink H, Hart AA (1982) Prognostic factors of neck node metastasis. Clin Otolaryngol Allied Sci 7:185–192

    Article  CAS  Google Scholar 

  23. Sullivan LM, Massaro JM, D’Agostino RB Sr (2004) Presentation of multivariate data for clinical use: the Framingham Study risk score functions. Stat Med 23:1631–1660

    Article  Google Scholar 

  24. Murali R, Desilva C, Thompson JF, Scolyer RA (2010) Non-Sentinel Node Risk Score (N-SNORE): a scoring system for accurately stratifying risk of non-sentinel node positivity in patients with cutaneous melanoma with positive sentinel lymph nodes. J Clin Oncol 28:4441–4449

    Article  Google Scholar 

  25. Liu W, Cheng R, Ma Y et al (2018) Establishment and validation of the scoring system for preoperative prediction of central lymph node metastasis in papillary thyroid carcinoma. Sci Rep 8:6962

    Article  Google Scholar 

  26. Jeong JJ, Lee YS, Lee SC et al (2011) A scoring system for prediction of lateral neck node metastasis from papillary thyroid cancer. J Korean Med Sci 26:996–1000

    Article  Google Scholar 

  27. He N, Xie C, Wei W et al (2012) A new, preoperative, MRI-based scoring system for diagnosing malignant axillary lymph nodes in women evaluated for breast cancer. Eur J Radiol 81:2602–2612

    Article  Google Scholar 

  28. Lee L, Ronellenfitsch U, Hofstetter WL et al (2013) Predicting lymph node metastases in early esophageal adenocarcinoma using a simple scoring system. J Am Coll Surg 217:191–199

    Article  Google Scholar 

  29. Tran TB, Worhunsky DJ, Squires MH et al (2018) Clinicopathologic score predicting lymph node metastasis in T1 gastric cancer. Surgery 163:889–893

    Article  Google Scholar 

  30. Imai K, Kato H, Katayama K et al (2016) A preoperative risk-scoring system to predict lymph node metastasis in endometrial cancer and stratify patients for lymphadenectomy. Gynecol Oncol 142:273–277

    Article  Google Scholar 

  31. Chung MS, Choi YJ, Kim SO et al (2019) A scoring system for prediction of cervical lymph node metastasis in patients with head and neck squamous cell carcinoma. AJNR Am J Neuroradiol 40:1049–1054

    Article  CAS  Google Scholar 

  32. King AD, Tse GM, Ahuja AT et al (2004) Necrosis in metastatic neck nodes: diagnostic accuracy of CT, MR imaging, and US. Radiology 230:720–726

    Article  Google Scholar 

  33. Som PM, Brandwein-Gensler MS (2011) Lymph nodes of the neck. In: Som PM, Curtin HD (eds) Head and neck imaging, 5th edn. Mosby Elsevier, St. Louis, pp 2287–2384

    Chapter  Google Scholar 

  34. Ballantyne AJ (1964) Significance of retropharyngeal nodes in cancer of the head and neck. Am J Surg 108:500–504

    Article  CAS  Google Scholar 

  35. Schwartz DL, Ford E, Rajendran J et al (2005) FDG-PET/CT imaging for preradiotherapy staging of head-and-neck squamous cell carcinoma. Int J Radiat Oncol Biol Phys 61:129–136

    Article  Google Scholar 

  36. Park JT, Roh JL, Kim JS et al (2016) (18)F FDG PET/CT versus CT/MR imaging and the prognostic value of contralateral neck metastases in patients with head and neck squamous cell carcinoma. Radiology 279:481–491

    Article  Google Scholar 

  37. Wong WL, Hussain K, Chevretton E et al (1996) Validation and clinical application of computer-combined computed tomography and positron emission tomography with 2-[18F]fluoro-2-deoxy-D-glucose head and neck images. Am J Surg 172:628–632

    Article  CAS  Google Scholar 

  38. Ha PK, Hdeib A, Goldenberg D et al (2006) The role of positron emission tomography and computed tomography fusion in the management of early-stage and advanced-stage primary head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 132:12–16

    Article  Google Scholar 

  39. Zanation AM, Sutton DK, Couch ME, Weissler MC, Shockley WW, Shores CG (2005) Use, accuracy, and implications for patient management of [18F]-2-fluorodeoxyglucose-positron emission/computerized tomography for head and neck tumors. Laryngoscope 115:1186–1190

    Article  Google Scholar 

Download references

Funding

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

Author information

Author notes

  1. Leehi Joo and Yun Jung Bae have equally contributed to this paper.

Authors and Affiliations

  1. Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 86 Asanbyeongwon-Gil, Songpa-Gu, Seoul, 138-736, Republic of Korea

    Leehi Joo, Young Jun Choi, Sae Rom Chung, Chong Hyun Suh, Jung Hwan Baek & Jeong Hyun Lee

  2. Department of Radiology, Seoul National University Bundang Hospital 82, Gumi-ro 173beon-gil, Bundang-gu, Seongnam, Gyeonggi, 13620, Republic of Korea

    Yun Jung Bae

  3. Department of Otolaryngology, Asan Medical Center, University of Ulsan College of Medicine, 86 Asanbyeongwon-Gil, Songpa-Gu, Seoul, 138-736, Republic of Korea

    Yoon Se Lee

  4. Department of Clinical Epidemiology and Biostatistics, Asan Medical Center, University of Ulsan College of Medicine, 86 Asanbyeongwon-Gil, Songpa-Gu, Seoul, 138-736, Republic of Korea

    Seon-Ok Kim

Authors
  1. Leehi Joo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yun Jung Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Young Jun Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoon Se Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sae Rom Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chong Hyun Suh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Seon-Ok Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jung Hwan Baek
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jeong Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young Jun Choi.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Young Jun Choi.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors (Seon-Ok Kim) kindly provided statistical advice for this manuscript.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• diagnostic or prognostic study

• multicenter study

Additional information

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Joo, L., Bae, Y.J., Choi, Y.J. et al. Prediction model for cervical lymph node metastasis in human papillomavirus-related oropharyngeal squamous cell carcinomas. Eur Radiol 31, 7429–7439 (2021). https://doi.org/10.1007/s00330-021-07766-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-021-07766-4

Keywords

Search

Navigation