Skip to main content

Advertisement

SpringerLink
Log in

Head and neck MRI-based T stage and [18F]FDG PET/CT-based N/M stage improved prognostic stratification in primary nasopharyngeal carcinoma

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

Abstract

Objectives

To evaluate whether MRI-based T stage (TMRI), [18F]FDG PET/CT-based N (NPET/CT), and M stage (MPET/CT) are superior in NPC patients’ prognostic stratification based on long-term survival evidences, and whether TNM staging method involving TMRI + NPET/CT + MPET/CT could improve NPC patients’ prognostic stratification.

Methods

From April 2007 to December 2013, 1013 consecutive untreated NPC patients with complete imaging data were enrolled. All patients’ initial stages were repeated based on (1) the NCCN guideline recommended “TMRI + NMRI + MPET/CT” (“MMP”) staging method; (2) the traditional “TMRI + NMRI + Mconventional work-up (CWU)” (“MMC”) staging method; (3) the single-step “TPET/CT + NPET/CT + MPET/CT” (“PPP”) staging method; or (4) the “TMRI + NPET/CT + MPET/CT” (“MPP”) staging method recommended in present research. Survival curve, ROC curve, and net reclassification improvement (NRI) analysis were used to evaluate the prognosis predicting ability of different staging methods.

Results

[18F]FDG PET/CT performed worse on T stage (NRI =  − 0.174, p < 0.001) but better on N (NRI = 0.135, p = 0.004) and M stage (NRI = 0.126, p = 0.001). The patients whose N stage upgraded by [18F]FDG PET/CT had worse survival (p = 0.011). The “TMRI + NPET/CT + MPET/CT” (“MPP”) method performed better on survival prediction when compared with “MMP” (NRI = 0.079, p = 0.007), “MMC” (NRI = 0.190, p < 0.001), or “PPP” method (NRI = 0.107, p < 0.001). The “TMRI + NPET/CT + MPET/CT” (“MPP”) method could reclassify patients’ TNM stage to a more appropriate stage. The improvement is significant in patients with more than 2.5-years follow-up according to the time-dependent NRI values.

Conclusions

The MRI is superior to [18F]FDG PET/CT in T stage, and [18F]FDG PET/CT is superior to CWU in N/M stage. The “TMRI + NPET/CT + MPET/CT” (“MPP”) staging method could significantly improve NPC patients’ long-term prognostic stratification.

Clinical relevance statement

The present research provided long-term follow-up evidence for benefits of MRI and [18F]FDG PET/CT in TNM staging for nasopharyngeal carcinoma, and proposes a new imaging procedure for TNM staging incorporating MRI-based T stage and [18F]FDG PET/CT-based N and M stage, which significantly improves long-term prognostic stratification for patients with NPC.

Key Points

• The long-term follow-up evidence of a large-scale cohort was provided to evaluate the advantages of MRI, [ 18 F]FDG PET/CT, and CWU in the TNM staging of nasopharyngeal carcinoma.

• A new imaging procedure for TNM stage of nasopharyngeal carcinoma was proposed.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

[18F]FDG:

[18F]Fluorodeoxyglucose

“MMC” staging method:

The TNM staging method involving MRI based T and N stage and CWU-based M stage

“MMP” staging method:

The TNM staging method involving MRI based T and N stage and [18F]FDG PET/CT-based M stage

“MPP” staging method:

The TNM staging method involving MRI based T stage and [18F]FDG PET/CT-based N and M stage

“PPP” staging method:

The TNM staging method involving [18F]FDG PET/CT-based T, N, and M stage

2DRT:

2-Dimensional radiotherapy

AC:

Adjuvant chemotherapy

AUC:

Area under the receiver-operating-characteristic curve

CLN:

Cervical lymph node

CT:

Computed tomography

CTVs:

Clinical target volumes

CWU:

Conventional workup

DNA:

Deoxyribonucleic acid

EBV:

Epstein-Barr virus

FOV:

Field of view

GTV:

Gross tumor volume

Gy:

Gray

HNSCC:

Head and neck squamous cell carcinoma

IMRT:

Intensity-modulated radiation therapy

IQR:

Interquartile range

LN:

Lymph node

MCWU :

M stage based on CWU imaging

MPET/CT :

M stage based on [18F]FDG PET/CT imaging

MRI:

Magnetic resonance imaging

NACT:

Neoadjuvant chemotherapy

NCCN:

National Comprehensive Cancer Network

NMRI :

N stage based on MRI imaging

NPC:

Nasopharyngeal carcinoma

NPET/CT :

N stage based on [18F]FDG PET/CT imaging

NRI:

The net reclassification improvement

OS:

Overall survival

PET/CT:

Positron emission tomography and computed tomography

RI:

Reclassification improvement

RLN:

Retropharyngeal lymph node

RT:

Radiation therapy

TMRI :

T stage based on MRI imaging

TNM:

Tumor node metastasis

TPET/CT :

T stage based on [18F]FDG PET/CT imaging

UICC:

The Union for International Cancer Control

WHO:

World Health Organization

References

  1. Cao S-M, Simons MJ, Qian C-N (2011) The prevalence and prevention of nasopharyngeal carcinoma in China. Chin J Cancer 30:114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Lee AW, Lin JC, Ng WT (2012) Current management of nasopharyngeal cancer. Semin Radiat Oncol 22:233–244

  3. National Comprehensive Cancer Network. Head and Neck Cancers (Version 2.2022). Available via https://www.nccn.org/professionals/physician_gls/pdf/head-and-neck.pdf. Accessed 26 Apr 2022

  4. Webber C, Gospodarowicz M, Sobin LH et al (2014) Improving the TNM classification: findings from a 10-year continuous literature review. Int J Cancer 135:371–378

    Article  CAS  PubMed  Google Scholar 

  5. Chen Y-P, Chan AT, Le Q-T, Blanchard P, Sun Y, Ma J (2019) Nasopharyngeal carcinoma. Lancet 394:64-80

  6. Beyer T, Townsend DW, Brun T et al (2000) A combined PET/CT scanner for clinical oncology. J Nucl Med 41:1369–1379

    CAS  PubMed  Google Scholar 

  7. Ng S-H, Yen T-C, Chang JT-C et al (2006) Prospective study of (18F) fluorodeoxyglucose positron emission tomography and computed tomography and magnetic resonance imaging in oral cavity squamous cell carcinoma with palpably negative neck. J Clin Oncol 24:4371–4376

    Article  PubMed  Google Scholar 

  8. Ng S-H, Chan S-C, Yen T-C et al (2009) Staging of untreated nasopharyngeal carcinoma with PET/CT: comparison with conventional imaging work-up. Eur J Nucl Med Mol Imaging 36:12

    Article  PubMed  Google Scholar 

  9. Kim JH, Choi KY, Lee S-H et al (2020) The value of CT, MRI, and PET-CT in detecting retropharyngeal lymph node metastasis of head and neck squamous cell carcinoma. BMC Med Imaging 20:1–8

    Article  Google Scholar 

  10. Lowe VJ, Duan F, Subramaniam RM et al (2019) Multicenter trial of [18F] fluorodeoxyglucose positron emission tomography/computed tomography staging of head and neck cancer and negative predictive value and surgical impact in the N0 neck: results from ACRIN 6685. J Clin Oncol 37:1704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lonneux M, Hamoir M, Reychler H et al (2010) Positron emission tomography with [18F] fluorodeoxyglucose improves staging and patient management in patients with head and neck squamous cell carcinoma: a multicenter prospective study. J Clin Oncol 28:1190–1195

    Article  CAS  PubMed  Google Scholar 

  12. Troost EG, Schinagl DA, Bussink J, Oyen WJ, Kaanders JH (2010) Clinical evidence on PET–CT for radiation therapy planning in head and neck tumours. Radiother Oncol 96:328–334

    Article  PubMed  Google Scholar 

  13. Facey K, Bradbury I, Laking G, Payne E (2007) Overview of the clinical effectiveness of positron emission tomography imaging in selected cancers. Health Technology Assessment –Southampton 11:44

  14. Hafidh MA, Lacy PD, Hughes JP, Duffy G, Timon CV (2006) 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 263:853

    Article  PubMed  Google Scholar 

  15. Comoretto M, Balestreri L, Borsatti E, Cimitan M, Franchin G, Lise M (2008) Detection and restaging of residual and/or recurrent nasopharyngeal carcinoma after chemotherapy and radiation therapy: comparison of MR imaging and FDG PET/CT. Radiology 249:203–211

    Article  PubMed  Google Scholar 

  16. Tang L-Q, Chen Q-Y, Fan W et al (2013) Prospective study of tailoring whole-body dual-modality [18F] fluorodeoxyglucose positron emission tomography/computed tomography with plasma Epstein-Barr virus DNA for detecting distant metastasis in endemic nasopharyngeal carcinoma at initial staging. J Clin Oncol 31:2861–2869

    Article  CAS  PubMed  Google Scholar 

  17. Liu F-Y, Chang JT, Wang H-M et al (2006) [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 24:599–604

    Article  PubMed  Google Scholar 

  18. Chang JT-C, Chan S-C, Yen T-C et al (2005) Nasopharyngeal carcinoma staging by (18) F-fluorodeoxyglucose positron emission tomography. Int J Radiat Oncol Biol Phys 62:501–507

  19. Shanmugaratnam K, Sobin LH (1993) The World Health Organization histological classification of tumours of the upper respiratory tract and ear. A commentary on the second edition. Cancer 71:2689–2697

  20. Kim M, Roh J-L, Kim J et al (2007) Utility of 18F-fluorodeoxyglucose positron emission tomography in the preoperative staging of squamous cell carcinoma of the oropharynx. Eur J Surg Oncol 33:633–638

    Article  CAS  PubMed  Google Scholar 

  21. Ng SH, Yen TC, Chang JT et al (2006) Prospective study of [18F]fluorodeoxyglucose positron emission tomography and computed tomography and magnetic resonance imaging in oral cavity squamous cell carcinoma with palpably negative neck. J Clin Oncol 24:4371-4376

  22. Ryu IS, Roh J-L, Kim JS et al (2016) Impact of 18F-FDG PET/CT staging on management and prognostic stratification in head and neck squamous cell carcinoma: a prospective observational study. Eur J Cancer 63:88–96

    Article  PubMed  Google Scholar 

  23. Amin MB, Edge S, Greene F et al (2017) AJCC Cancer Staging Manual, 8th edn. Springer, New York

    Book  Google Scholar 

  24. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 1977:159–174

  25. Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Measur 20:37–46

    Article  Google Scholar 

  26. Viera AJ, Garrett JM (2005) Understanding interobserver agreement: the kappa statistic. Fam Med 37:360–363

    PubMed  Google Scholar 

  27. Pencina MJ, D’Agostino RB, Vasan RS (2008) Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med 27:157–172

    Article  PubMed  Google Scholar 

  28. Inker LA, Schmid CH, Tighiouart H et al (2012) Estimating glomerular filtration rate from serum creatinine and cystatin C. N Engl J Med 367:20–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pischon T, Boeing H, Hoffmann K et al (2008) General and abdominal adiposity and risk of death in Europe. N Engl J Med 359:2105–2120

    Article  CAS  PubMed  Google Scholar 

  30. D’agostino RB, Vasan RS, Pencina MJ et al (2008) General cardiovascular risk profile for use in primary care. Circulation 117:743–753

    Article  PubMed  Google Scholar 

  31. Steyerberg EW, Vickers AJ, Cook NR et al (2010) Assessing the performance of prediction models: a framework for some traditional and novel measures. Epidemiology 21:128

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zethelius B, Berglund L, Sundström J et al (2008) Use of multiple biomarkers to improve the prediction of death from cardiovascular causes. N Engl J Med 358:2107–2116

    Article  CAS  PubMed  Google Scholar 

  33. Nakamura A, Kaneko N, Villemagne VL et al (2018) High performance plasma amyloid-β biomarkers for Alzheimer’s disease. Nature 554:249

    Article  CAS  PubMed  Google Scholar 

  34. Lehmann N, Erbel R, Mahabadi AA et al (2018) Value of progression of coronary artery calcification for risk prediction of coronary and cardiovascular events: result of the HNR study (Heinz Nixdorf Recall). Circulation 137:665–679

    Article  PubMed  PubMed Central  Google Scholar 

  35. Koshy M, Paulino AC, Howell R, Schuster D, Halkar R, Davis LW (2005) F‐18 FDG PET‐CT fusion in radiotherapy treatment planning for head and neck cancer. Head Neck-J Sci Spec 27:494–502

  36. Kitajima K, Nakamoto Y, Okizuka H et al (2008) Accuracy of whole-body FDG-PET/CT for detecting brain metastases from non-central nervous system tumors. Ann Nucl Med 22:595–602

    Article  PubMed  Google Scholar 

  37. Li Y, Jin G, Su D (2017) Comparison of gadolinium-enhanced MRI and 18FDG PET/PET-CT for the diagnosis of brain metastases in lung cancer patients: a meta-analysis of 5 prospective studies. Oncotarget 8:35743–35749

    Article  PubMed  PubMed Central  Google Scholar 

  38. VanderWalde NA, Salloum RG, Liu T-L et al (2014) Positron emission tomography and stage migration in head and neck cancer. JAMA Otolaryngol Head Neck Surg 140:654–661

    Article  PubMed  PubMed Central  Google Scholar 

  39. Zhang W, Chen Y, Chen L et al (2015) The clinical utility of plasma Epstein–Barr virus DNA assays in nasopharyngeal carcinoma: the dawn of a new era?: A systematic review and meta-analysis of 7836 cases. Medicine (Baltimore) 94:20

  40. Chan S, Yeh C, Yen T et al (2018) Clinical utility of simultaneous whole-body F-FDG PET/MRI as a single-step imaging modality in the staging of primary nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging 45:1297–1308

    Article  PubMed  Google Scholar 

  41. Stolzmann P, Veit-Haibach P, Chuck N et al (2013) Detection rate, location, and size of pulmonary nodules in trimodality PET/CT-MR: comparison of low-dose CT and Dixon-based MR imaging. Invest Radiol 48:241–246

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by grants from the National Key R&D Program of China (SQ2022YFC2500174), the National Natural Science Foundation of China (No. 32200651, 82203776, 82203125, 82222050, 82272739, 82272882, 82173287, 82073003, 82003267, 82002852), Guangdong Major Project of Basic and Applied Basic Research (HRB103), the Sci-Tech Project Foundation of Guangzhou City (202201011561), the Sun Yat-sen University Clinical Research 5010 Program (No. 201315, 2015021, 2017010, 2019023), Innovative Research Team of High-level Local Universities in Shanghai (SSMU-ZLCX20180500), the Special Support Plan of Guangdong Province (No. 2014TX01R145), the Natural Science Foundation of Guangdong Province (No.2017A030312003, No.2018A0303131004), the Natural Science Foundation of Guangdong Province for Distinguished Young Scholar(No.2018B030306001), Postdoctoral Innovative Talent Support Program (BX20220361), the Sci-Tech Project Foundation of Guangdong Province (No. 2014A020212103), the Health and Medical Collaborative Innovation Project of Guangzhou City (No. 201400000001, No.201803040003), Pearl River S&T Nova Program of Guangzhou (No. 201806010135), the Planned Science and Technology Project of Guangdong Province (2019B020230002), the National Science and Technology Pillar Program during the Twelfth Five-year Plan Period (No. 2014BAI09B10), Key Youth Teacher Cultivating Program of Sun Yat-sen University (20ykzd24), and the Fundamental Research Funds for the Central Universities.

Author information

Author notes

  1. Hao-Jun Xie and Xue-Song Sun contributed equally to this study.

  2. The senior authors Qiu-Yan Chen, Hai-Qiang Mai, and Lin-Quan Tang contributed equally to this study.

Authors and Affiliations

  1. Sun Yat-sen University Cancer Center; State Key Laboratory of Oncology in South China; Collaborative Innovation Center for Cancer Medicine; Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, 510060, Guangzhou, China

    Hao-Jun Xie, Xue-Song Sun, Xu Zhang, Bei-Bei Xiao, Da-Feng Lin, Xiao-Ping Lin, Xiao-Fei Lv, Li-Zhi Liu, Feng Han, Ru-Hai Zou, Ji-Bin Li, Wei Fan, Qiu-Yan Chen, Hai-Qiang Mai & Lin-Quan Tang

  2. Department of Nasopharyngeal Carcinoma, Sun Yat-sen University Cancer Center, 651 Dongfeng Road East, 510060, Guangzhou, People’s Republic of China

    Hao-Jun Xie, Xue-Song Sun, Bei-Bei Xiao, Da-Feng Lin, Qiu-Yan Chen, Hai-Qiang Mai & Lin-Quan Tang

  3. Department of Head and Neck Cancer, Sun Yat-sen University Cancer Center, Guangzhou, People’s Republic of China

    Hao-Jun Xie

  4. Department of Nuclear Medicine, Sun Yat-sen University Cancer Center, Guangzhou, People’s Republic of China

    Xu Zhang, Xiao-Ping Lin & Wei Fan

  5. Imaging Diagnostic and Interventional Center, Sun Yat-sen University Cancer Center, Guangzhou, People’s Republic of China

    Xiao-Fei Lv & Li-Zhi Liu

  6. Department of Ultrasound, Sun Yat-sen University Cancer Center, Guangzhou, People’s Republic of China

    Feng Han & Ru-Hai Zou

Authors
  1. Hao-Jun Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xue-Song Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bei-Bei Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Da-Feng Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao-Ping Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiao-Fei Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Li-Zhi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Feng Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ru-Hai Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ji-Bin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Wei Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Qiu-Yan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hai-Qiang Mai
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Lin-Quan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hai-Qiang Mai or Lin-Quan Tang.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Lin-Quan Tang.

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 has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• observational

• performed at one institution

Additional information

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 992 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xie, HJ., Sun, XS., Zhang, X. et al. Head and neck MRI-based T stage and [18F]FDG PET/CT-based N/M stage improved prognostic stratification in primary nasopharyngeal carcinoma. Eur Radiol 33, 7952–7966 (2023). https://doi.org/10.1007/s00330-023-09815-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-023-09815-6

Keywords

Search

Navigation