Abstract
Purpose
In this prospective study, we sought to compare the clinical utility of fluorodeoxyglucose PET/MRI, MRI, and PET/CT in the detection of synchronous cancers and distant metastases in patients with oropharyngeal and hypopharyngeal squamous cell carcinoma (OHSCC).
Methods
We examined 198 consecutive patients with biopsy-proven OHSCC who agreed to receive chemoradiation. All patients underwent pretreatment PET/MRI and PET/CT on the same day. Patients were followed-up for a minimum of 12 months or until death. The McNemar’s test and receiver-operating characteristic (ROC) curves were used to compare sensitivity/specificity and the diagnostic capabilities of PET/MRI, MRI, and PET/CT, respectively.
Results
We identified 55 patients (27.7%) who had synchronous cancers and/or distant metastases (number of involved sites: 83). The results of site-based analysis revealed that the sensitivity of PET/MRI was 15.7% higher than that of MRI (73.5% versus 57.8%, p < 0.001) and 3.6% higher compared with PET/CT (73.5% versus 69.9%, p = 0.083), whereas the sensitivity of PET/CT was 12.1% higher than that of MRI (69.9% versus 57.8%, p = 0.012). On a patient-basis, ROC curve analysis demonstrated that PET/MRI yielded a greater area under curve than MRI (0.930 versus 0.905, p = 0.023). There were no significant differences in terms of diagnostic capability between MRI and PET/CT (0.905 versus 0.917, p = 0.469) and between PET/MRI and PET/CT (0.930 versus 0.917, p = 0.062).
Conclusions
In our cohort, PET/MRI showed a significantly higher diagnostic capability than MRI and no significant difference compared with PET/CT for the detection of synchronous cancers or distant metastases in patients with OHSCC.
Similar content being viewed by others
References
Mohadjer C, Dietz A, Maier H, Weidauer H. Distant metastasis and incidence of second carcinomas in patients with oropharyngeal and hypopharyngeal carcinomas. Hno. 1996;44:134–9.
Erkal HS, Mendenhall WM, Amdur RJ, Villaret DB, Stringer SP. Synchronous and metachronous squamous cell carcinomas of the head and neck mucosal sites. J Clin Oncol. 2001;19:1358–62. https://doi.org/10.1200/JCO.2001.19.5.1358.
Ng SH, Chan SC, Liao CT, Chang JT, Ko SF, Wang HM, et al. Distant metastases and synchronous second primary tumors in patients with newly diagnosed oropharyngeal and hypopharyngeal carcinomas: evaluation of (18)F-FDG PET and extended-field multi-detector row CT. Neuroradiology. 2008;50:969–79. https://doi.org/10.1007/s00234-008-0426-2.
Chan SC, Wang HM, Yen TC, Lin CY, Chin SC, Liao CT, et al. (1)(8)F-FDG PET/CT and 3.0-T whole-body MRI for the detection of distant metastases and second primary tumours in patients with untreated oropharyngeal/hypopharyngeal carcinoma: a comparative study. Eur J Nucl Med Mol Imaging. 2011;38:1607–19. https://doi.org/10.1007/s00259-011-1824-y.
Chuang SC, Scelo G, Tonita JM, Tamaro S, Jonasson JG, Kliewer EV, et al. Risk of second primary cancer among patients with head and neck cancers: a pooled analysis of 13 cancer registries. Int J Cancer. 2008;123:2390–6. https://doi.org/10.1002/ijc.23798.
Rohde M, Nielsen AL, Johansen J, Sorensen JA, Nguyen N, Diaz A, et al. Head-to-head comparison of chest x-ray/head and neck MRI, chest CT/head and neck MRI, and (18)F-FDG PET/CT for detection of distant metastases and synchronous cancer in oral, pharyngeal, and laryngeal cancer. J Nucl Med. 2017;58:1919–24. https://doi.org/10.2967/jnumed.117.189704.
Kim Y, Roh JL, Kim JS, Lee JH, Choi SH, Nam SY, et al. Chest radiography or chest CT plus head and neck CT versus (18)F-FDG PET/CT for detection of distant metastasis and synchronous cancer in patients with head and neck cancer. Oral Oncol. 2019;88:109–14. https://doi.org/10.1016/j.oraloncology.2018.11.026.
Choi JY, Lee KS, Kwon OJ, Shim YM, Baek CH, Park K, et al. Improved detection of second primary cancer using integrated [18F] fluorodeoxyglucose positron emission tomography and computed tomography for initial tumor staging. J Clin Oncol. 2005;23:7654–9. https://doi.org/10.1200/JCO.2005.01.4340.
Ng SH, Chan SC, Yen TC, Liao CT, Lin CY, Tung-Chieh Chang J, et al. PET/CT and 3-T whole-body MRI in the detection of malignancy in treated oropharyngeal and hypopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2011;38:996–1008. https://doi.org/10.1007/s00259-011-1740-1.
Ng SH, Chan SC, Yen TC, Chang JT, Liao CT, Ko SF, et al. Pretreatment evaluation of distant-site status in patients with nasopharyngeal carcinoma: accuracy of whole-body MRI at 3-Tesla and FDG-PET-CT. Eur Radiol. 2009. https://doi.org/10.1007/s00330-009-1504-5.
Schick F. Whole-body MRI at high field: technical limits and clinical potential. Eur Radiol. 2005;15:946–59. https://doi.org/10.1007/s00330-005-2678-0.
Delso G, Furst S, Jakoby B, Ladebeck R, Ganter C, Nekolla SG, et al. Performance measurements of the Siemens mMR integrated whole-body PET/MR scanner. J Nucl Med. 2011;52:1914–22. https://doi.org/10.2967/jnumed.111.092726.
Kubiessa K, Purz S, Gawlitza M, Kuhn A, Fuchs J, Steinhoff KG, et al. Initial clinical results of simultaneous 18F-FDG PET/MRI in comparison to 18F-FDG PET/CT in patients with head and neck cancer. Eur J Nucl Med Mol Imaging. 2014;41:639–48. https://doi.org/10.1007/s00259-013-2633-2.
Kuhn FP, Hullner M, Mader CE, Kastrinidis N, Huber GF, von Schulthess GK, et al. Contrast-enhanced PET/MR imaging versus contrast-enhanced PET/CT in head and neck cancer: how much MR information is needed? J Nucl Med. 2014;55:551–8. https://doi.org/10.2967/jnumed.113.125443.
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;83:1163–8. https://doi.org/10.1016/j.ejrad.2014.03.023.
Queiroz MA, Hullner M, Kuhn F, Huber G, Meerwein C, Kollias S, et al. PET/MRI and PET/CT in follow-up of head and neck cancer patients. Eur J Nucl Med Mol Imaging. 2014;41:1066–75. https://doi.org/10.1007/s00259-014-2707-9.
Queiroz MA, Hullner M, Kuhn F, Huber G, Meerwein C, Kollias S, et al. Use of diffusion-weighted imaging (DWI) in PET/MRI for head and neck cancer evaluation. Eur J Nucl Med Mol Imaging. 2014;41:2212–21. https://doi.org/10.1007/s00259-014-2867-7.
Partovi S, Kohan A, Vercher-Conejero JL, Rubbert C, Margevicius S, Schluchter MD, et al. Qualitative and quantitative performance of (1)(8)F-FDG-PET/MRI versus (1)(8)F-FDG-PET/CT in patients with head and neck cancer. AJNR Am J Neuroradiol. 2014;35:1970–5. https://doi.org/10.3174/ajnr.A3993.
Varoquaux A, Rager O, Poncet A, Delattre BM, Ratib O, Becker CD, et al. Detection and quantification of focal uptake in head and neck tumours: (18)F-FDG PET/MR versus PET/CT. Eur J Nucl Med Mol Imaging. 2014;41:462–75. https://doi.org/10.1007/s00259-013-2580-y.
Covello M, Cavaliere C, Aiello M, Cianelli MS, Mesolella M, Iorio B, et al. Simultaneous PET/MR head-neck cancer imaging: preliminary clinical experience and multiparametric evaluation. Eur J Radiol. 2015;84:1269–76. https://doi.org/10.1016/j.ejrad.2015.04.010.
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;43:92–102. https://doi.org/10.1007/s00259-015-3145-z.
Spick C, Herrmann K, Czernin J. 18F-FDG PET/CT and PET/MRI perform equally well in cancer: evidence from studies on more than 2,300 patients. Eur J Surg Oncol. 2016;57:420–30. https://doi.org/10.2967/jnumed.115.158808.
Chan SC, Yeh CH, Yen TC, Ng SH, Chang JT, Lin CY, et al. Clinical utility of simultaneous whole-body (18)F-FDG PET/MRI as a single-step imaging modality in the staging of primary nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2018;45:1297–308. https://doi.org/10.1007/s00259-018-3986-3.
Brouwer J, de Bree R, Hoekstra OS, Golding RP, Langendijk JA, Castelijns JA, et al. Screening for distant metastases in patients with head and neck cancer: is chest computed tomography sufficient? Laryngoscope. 2005;115:1813–7. https://doi.org/10.1097/01.mlg.0000174954.51514.b7.
Liu FY, Chang JT, Wang HM, Liao CT, Kang CJ, Ng SH, et al. [18F]fluorodeoxyglucose positron emission tomography is more sensitive than skeletal scintigraphy for detecting bone metastasis in endemic nasopharyngeal carcinoma at initial staging. J Clin Oncol. 2006;24:599–604. https://doi.org/10.1200/JCO.2005.03.8760.
Dhooge IJ, De Vos M, Van Cauwenberge PB. Multiple primary malignant tumors in patients with head and neck cancer: results of a prospective study and future perspectives. Laryngoscope. 1998;108:250–6.
Jones AS, Morar P, Phillips DE, Field JK, Husband D, Helliwell TR. Second primary tumors in patients with head and neck squamous cell carcinoma. Cancer. 1995;75:1343–53.
Schwartz LH, Ozsahin M, Zhang GN, Touboul E, De Vataire F, Andolenko P, et al. Synchronous and metachronous head and neck carcinomas. Cancer. 1994;74:1933–8.
Krishnatreya M, Rahman T, Kataki AC, Das A, Das AK, Lahkar K. Synchronous primary cancers of the head and neck region and upper aero digestive tract: defining high-risk patients. Indian J Cancer. 2013;50:322–6. https://doi.org/10.4103/0019-509X.123610.
Wang YK, Chuang YS, Wu TS, Lee KW, Wu CW, Wang HC, et al. Endoscopic screening for synchronous esophageal neoplasia among patients with incident head and neck cancer: prevalence, risk factors, and outcomes. Int J Cancer. 2017;141:1987–96. https://doi.org/10.1002/ijc.30911.
Ferlito A, Shaha AR, Silver CE, Rinaldo A, Mondin V. Incidence and sites of distant metastases from head and neck cancer. ORL J Otorhinolaryngol Relat Spec. 2001;63:202–7. https://doi.org/10.1159/000055740.
Garavello W, Ciardo A, Spreafico R, Gaini RM. Risk factors for distant metastases in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg. 2006;132:762–6. https://doi.org/10.1001/archotol.132.7.762.
Li X, Di B, Shang Y, Zhou Y, Cheng J, He Z. Clinicopathologic risk factors for distant metastases from head and neck squamous cell carcinomas. Eur J Surg Oncol. 2009;35:1348–53. https://doi.org/10.1016/j.ejso.2009.06.010.
Kuperman DI, Auethavekiat V, Adkins DR, Nussenbaum B, Collins S, Boonchalermvichian C, et al. Squamous cell cancer of the head and neck with distant metastasis at presentation. Head Neck. 2011;33:714–8. https://doi.org/10.1002/hed.21529.
Liu JC, Bhayani M, Kuchta K, Galloway T, Fundakowski C. Patterns of distant metastasis in head and neck cancer at presentation: implications for initial evaluation. Oral Oncol. 2019;88:131–6. https://doi.org/10.1016/j.oraloncology.2018.11.023.
O’Neill JP, Moynagh M, Kavanagh E, O’Dwyer T. Prospective, blinded trial of whole-body magnetic resonance imaging versus computed tomography positron emission tomography in staging primary and recurrent cancer of the head and neck. J Laryngol Otol. 2010;124:1274–7. https://doi.org/10.1017/S0022215110001398.
Schmidt GP, Haug AR, Schoenberg SO, Reiser MF. Whole-body MRI and PET-CT in the management of cancer patients. Eur Radiol. 2006;16:1216–25. https://doi.org/10.1007/s00330-006-0183-8.
Yi CA, Shin KM, Lee KS, Kim BT, Kim H, Kwon OJ, et al. Non-small cell lung cancer staging: efficacy comparison of integrated PET/CT versus 3.0-T whole-body MR imaging. Radiology. 2008;248:632–42. https://doi.org/10.1148/radiol.2482071822.
Pfannenberg C, Aschoff P, Schanz S, Eschmann SM, Plathow C, Eigentler TK, et al. Prospective comparison of 18F-fluorodeoxyglucose positron emission tomography/computed tomography and whole-body magnetic resonance imaging in staging of advanced malignant melanoma. Eur J Cancer. 2007;43:557–64. https://doi.org/10.1016/j.ejca.2006.11.014.
Antoch G, Vogt FM, Freudenberg LS, Nazaradeh F, Goehde SC, Barkhausen J, et al. Whole-body dual-modality PET/CT and whole-body MRI for tumor staging in oncology. JAMA. 2003;290:3199–206. https://doi.org/10.1001/jama.290.24.3199.
Funding
This study was supported by a grant (MOST 104-2314-B-182A -091 -MY3) from the Taiwan Ministry of Science and Technology.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All of the study procedures 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.
Informed consent
Informed consent was obtained from all participants.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Oncology – Head and Neck
Rights and permissions
About this article
Cite this article
Yeh, CH., Chan, SC., Lin, CY. et al. Comparison of 18F-FDG PET/MRI, MRI, and 18F-FDG PET/CT for the detection of synchronous cancers and distant metastases in patients with oropharyngeal and hypopharyngeal squamous cell carcinoma. Eur J Nucl Med Mol Imaging 47, 94–104 (2020). https://doi.org/10.1007/s00259-019-04510-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00259-019-04510-5