[18F]FDG PET/MRI versus contrast-enhanced MRI in detecting regional HNSCC metastases

Abstract

Objective

To compare the accuracy of contrast-enhanced MRI using established dimensional and morphological criteria versus integrated [18F]FDG PET/MRI in identifying regional lymph node metastases in patients with newly diagnosed head and neck squamous cell carcinoma (HNSCC). For this purpose, we compare MRI and PET/MRI using the histopathological findings in dissected lymph nodes as the gold standard.

Methods

We retrospectively reviewed 26 patients with histologically proven HNSCC who underwent gadolinium-enhanced [18F]FDG PET/MRI as part of their staging. All neck lymph nodes were classified on MRI using dimensional and/or morphological criteria. Then, they were jointly assessed by a nuclear medicine physician and a radiologist using integrated [18F]PET/MR images. ROC curves were obtained to compare the techniques. Lymph node histopathology was considered as the reference standard.

Results

Out of 865 lymph nodes, 35 were malignant at histopathology (3 with micro-metastases). Sensitivity and specificity were 48.6% and 99.5% for MRI using dimensional criteria; 60.0% and 99.6% for MRI using morphological criteria; 60.0% and 99.4% for MRI using both; and 74.3% and 97.6% for PET using MR as anatomic localization. The area under the ROC curve was higher for PET and MRI localization (0.859) than for MRI using dimensional (0.740; p < 0.05), or morphological (0.798; p < 0.05), or both criteria (0.797; p < 0.05). PET/MR using a PET SUVmax cutoff of 5.7 combined with MRI using dimensional and/or morphological criteria reached high values for accuracy (98.2%), NPV (98.2%), and PPV (95.2%).

Conclusions

Compared with traditional contrast-enhanced MRI or PET alone, integrated PET/MRI could improve diagnostic accuracy in detecting metastatic lymph nodes in patients with HNSCC.

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References

  1. 1.

    Boscolo-Rizzo P, Furlan C, Lupato V, Polesel J, Fratta E. Novel insights into epigenetic drivers of oropharyngeal squamous cell carcinoma: role of HPV and lifestyle factors. Clin Epigenetics. 2017;9:124.

    Article  Google Scholar 

  2. 2.

    Leemans CR, Tiwari R, Nauta JJ, van der Waal I, Snow GB. Recurrence at the primary site in head and neck cancer and the significance of neck lymph node metastases as a prognostic factor. Cancer. 1994;73(1):187–90.

    CAS  Article  Google Scholar 

  3. 3.

    Grégoire V, Lefebvre J-L, Licitra L, Felip E, EHNS-ESMO-ESTRO Guidelines Working Group. Squamous cell carcinoma of the head and neck: EHNS-ESMO-ESTRO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol Off J Eur Soc Med Oncol. 2010;21(Suppl 5):v184-6.

    Google Scholar 

  4. 4.

    Mehanna H, Wong W-L, McConkey CC, Rahman JK, Robinson M, Hartley AGJ, et al. PET-CT surveillance versus neck dissection in advanced head and neck cancer. N Engl J Med. 2016;374(15):1444–54.

    CAS  Article  Google Scholar 

  5. 5.

    Ng S-H, Yen T-C, Liao C-T, Chang JT-C, Chan S-C, Ko S-F, et al. 18F-FDG PET and CT/MRI in oral cavity squamous cell carcinoma: a prospective study of 124 patients with histologic correlation. J Nucl Med. 2005;46(7):1136–43.

    PubMed  Google Scholar 

  6. 6.

    de Bondt RBJ, Nelemans PJ, Hofman PAM, Casselman JW, Kremer B, van Engelshoven JMA, et al. Detection of lymph node metastases in head and neck cancer: a meta-analysis comparing US, USgFNAC, CT and MR imaging. Eur J Radiol. 2007;64(2):266–72.

    Article  Google Scholar 

  7. 7.

    Nakamoto Y, Tamai K, Saga T, Higashi T, Hara T, Suga T, et al. Clinical value of image fusion from MR and PET in patients with head and neck cancer. Mol Imaging Biol. 2009;11(1):46–53.

    Article  Google Scholar 

  8. 8.

    Heusch P, Sproll C, Buchbender C, Rieser E, Terjung J, Antke C, et al. Diagnostic accuracy of ultrasound, 18F-FDG-PET/CT, and fused 18F-FDG-PET-MR images with DWI for the detection of cervical lymph node metastases of HNSCC. Clin Oral Investig. 2014;18(3):969–78.

    Article  Google Scholar 

  9. 9.

    Hafidh MA, Lacy PD, Hughes JP, Duffy G, Timon CV. Evaluation of the impact of addition of PET to CT and MR scanning in the staging of patients with head and neck carcinomas. Eur Arch Otorhinolaryngol. 2006;263(9):853–9.

    Article  Google Scholar 

  10. 10.

    Nahmias C, Carlson ER, Duncan LD, Blodgett TM, Kennedy J, Long MJ, et al. Positron emission tomography/computerized tomography (PET/CT) scanning for preoperative staging of patients with oral/head and neck cancer. J Oral Maxillofac Surg. 2007;65(12):2524–35.

    Article  Google Scholar 

  11. 11.

    Eiber M, Martinez-Möller A, Souvatzoglou M, Holzapfel K, Pickhard A, Löffelbein D, et al. Value of a Dixon-based MR/PET attenuation correction sequence for the localization and evaluation of PET-positive lesions. Eur J Nucl Med Mol Imaging. 2011;38(9):1691–701.

    Article  Google Scholar 

  12. 12.

    Boellaard R, Delgado-Bolton R, Oyen WJG, Giammarile F, Tatsch K, Eschner W, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 20. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54.

    CAS  Article  Google Scholar 

  13. 13.

    Castelijns JA, van den Brekel MW. Imaging of lymphadenopathy in the neck. Eur Radiol. 2002;12(4):727–38. https://doi.org/10.1007/s003300101102.

    Article  PubMed  Google Scholar 

  14. 14.

    van den Brekel MW, Stel HV, Castelijns JA, Nauta JJ, van der Waal I, Valk J, et al. Cervical lymph node metastasis: assessment of radiologic criteria. Radiology. 1990;177(2):379–84. https://doi.org/10.1148/radiology.177.2.2217772.

    Article  PubMed  Google Scholar 

  15. 15.

    King AD, Tse GMK, Ahuja AT, Yuen EHY, Vlantis AC, To EWH, et al. Necrosis in metastatic neck nodes: diagnostic accuracy of CT, MR imaging, and US. Radiology. 2004;230(3):720–6. https://doi.org/10.1148/radiol.2303030157.

    Article  PubMed  Google Scholar 

  16. 16.

    de Bondt RBJ, Nelemans PJ, Bakers F, Casselman JW, Peutz-Kootstra C, Kremer B, et al. Morphological MRI criteria improve the detection of lymph node metastases in head and neck squamous cell carcinoma: multivariate logistic regression analysis of MRI features of cervical lymph nodes. Eur Radiol. 2009;19(3):626–33. https://doi.org/10.1007/s00330-008-1187-3.

    Article  PubMed  Google Scholar 

  17. 17.

    R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available from: https://www.r-project.org/.

  18. 18.

    Platzek I, Beuthien-Baumann B, Schneider M, Gudziol V, Langner J, Schramm G, et al. PET/MRI in head and neck cancer: initial experience. Eur J Nucl Med Mol Imaging. 2013;40(1):6–11. https://doi.org/10.1007/s00259-012-2248-z.

    Article  PubMed  Google Scholar 

  19. 19.

    Kim SG, Friedman K, Patel S, Hagiwara M. Potential role of PET/MRI for imaging metastatic lymph nodes in head and neck cancer. Am J Roentgenol. 2016;207(2):248–56. https://doi.org/10.2214/AJR.16.16265.

    Article  Google Scholar 

  20. 20.

    Queiroz MA, Huellner MW. PET/MR in cancers of the head and neck. Semin Nucl Med. 2015;45(3):248–65.

    Article  Google Scholar 

  21. 21.

    Galgano SJ, Marshall RV, Middlebrooks EH, McConathy JE, Bhambhvani P. PET/MR imaging in head and neck cancer. Magn Reson Imaging Clin N Am. 2018;26(1):167–78.

    Article  Google Scholar 

  22. 22.

    Lee YZ, Ramalho J, Kessler B. PET–MR imaging in head and neck. Magn Reson Imaging Clin N Am. 2017;25(2):315–24.

    Article  Google Scholar 

  23. 23.

    Schaarschmidt BM, Heusch P, Buchbender C, Ruhlmann M, Bergmann C, Ruhlmann V, et al. Locoregional tumour evaluation of squamous cell carcinoma in the head and neck area: a comparison between MRI, PET/CT and integrated PET/MRI. Eur J Nucl Med Mol Imaging. 2016;43(1):92–102. https://doi.org/10.1007/s00259-015-3145-z.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Platzek I, Beuthien-Baumann B, Schneider M, Gudziol V, Kitzler HH, Maus J, et al. FDG PET/MR for lymph node staging in head and neck cancer. Eur J Radiol. 2014;83(7):1163–8.

    Article  Google Scholar 

  25. 25.

    Loeffelbein DJ, Souvatzoglou M, Wankerl V, Dinges J, Ritschl LM, Mücke T, et al. Diagnostic value of retrospective PET-MRI fusion in head-and-neck cancer. BMC Cancer. 2014;14(1):846. https://doi.org/10.1186/1471-2407-14-846.

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Richards PS. The role of ultrasound in the detection of cervical lymph node metastases in clinically N0 squamous cell carcinoma of the head and neck. Cancer Imaging. 2007;7(1):167–78.

    CAS  Article  Google Scholar 

  27. 27.

    Souren C, Kloss-Brandstätter A, Stadler A, Kross K, Yamauchi K, Ketelsen D, et al. Ultrasound-guided fine-needle aspiration cytology as a diagnostic tool in comparison to ultrasound and MRI for staging in oral- and oropharyngeal squamous cell tumors. J Cranio-Maxillofacial Surg. 2016;44(2):197–201.

    Article  Google Scholar 

  28. 28.

    Norling R, Buron BMD, Therkildsen MH, Henriksen BM, von Buchwald C, Nielsen MB. Staging of cervical lymph nodes in oral squamous cell carcinoma: adding ultrasound in clinically lymph node negative patients may improve diagnostic work-up. PLoS One. 2014;9(3):e90360. https://doi.org/10.1371/journal.pone.0090360.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The acquisition of PET/MRI system of the University-Hospital of Padova was founded by the “Fondazione Cassa di Risparmio di Padova e Rovigo” and co-founded by the Hospital of Padova.

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Correspondence to Daniele Borsetto.

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Crimì, F., Borsetto, D., Stramare, R. et al. [18F]FDG PET/MRI versus contrast-enhanced MRI in detecting regional HNSCC metastases. Ann Nucl Med 35, 260–269 (2021). https://doi.org/10.1007/s12149-020-01565-5

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Keywords

  • HNSCC
  • PET/MRI
  • Lymph nodes