Top

European Journal of Nuclear Medicine and Molecular Imaging

Published in:

Open Access 01-11-2018 | Original Article

What is the prognostic impact of FDG PET in locally advanced head and neck squamous cell carcinoma treated with concomitant chemo-radiotherapy? A systematic review and meta-analysis

Authors: Pierluigi Bonomo, A. Merlotti, E. Olmetto, A. Bianchi, I. Desideri, A. Bacigalupo, P. Franco, C. Franzese, E. Orlandi, L. Livi, S. Caini

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 12/2018

Abstract

Purpose

Evidence is conflicting on the prognostic value of ¹⁸F-fluorodeoxyglucose (FDG) positron emission tomography (PET) in head and neck squamous cell carcinoma. The aim of our study was to determine the impact of semiquantitative and qualitative metabolic parameters on the outcome in patients managed with standard treatment for locally advanced disease.

Methods

A systematic review of the literature was conducted. A meta-analysis was performed of studies providing estimates of relative risk (RR) for the association between semiquantitative metabolic parameters and efficacy outcome measures.

Results

The analysis included 25 studies, for a total of 2,223 subjects. The most frequent primary tumour site was the oropharynx (1,150/2,223 patients, 51.7%). According to the available data, the majority of patients had stage III/IV disease (1,709/1,799, 94.9%; no information available in four studies) and were treated with standard concurrent chemoradiotherapy (1,562/2,009 patients, 77.7%; only one study without available information). A total of 11, 8 and 4 independent studies provided RR estimates for the association between baseline FDG PET metrics and overall survival (OS), progression-free survival (PFS) and locoregional control (LRC), respectively. High pretreatment metabolic tumour volume (MTV) was significantly associated with a worse OS (summary RR 1.86, 95% CI 1.08–3.21), PFS (summary RR 1.81, 95% CI 1.14–2.89) and LRC (summary RR 3.49, 95% CI 1.65–7.35). Given the large heterogeneity (I² > 50%) affecting the summary measures, no cumulative threshold for an unfavourable prognosis could be defined. No statistically significant association was found between SUV_max and any of the outcome measures.

Conclusion

FDG PET has prognostic relevance in the context of locally advanced head and neck squamous cell carcinoma. Pretreatment MTV is the only metabolic variable with a significant impact on patient outcome. Because of the heterogeneity and the lack of standardized methodology, no definitive conclusions on optimal cut-off values can be drawn.

Available only for authorised users

Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24:2137–50. https://doi.org/10.1200/JCO.2005.05.2308.CrossRefPubMed

Machtay M, Moughan J, Trotti A, Garden AS, Weber RS, Cooper JS, et al. Factors associated with severe late toxicity after concurrent chemoradiation for locally advanced head and neck cancer: an RTOG analysis. J Clin Oncol. 2008;26:3582–9. https://doi.org/10.1200/JCO.2007.14.8841.CrossRefPubMedPubMedCentral

Pulte D, Brenner H. Changes in survival in head and neck cancers in the late 20th and early 21st century: a period analysis. Oncologist. 2010;15:994–1001. https://doi.org/10.1634/theoncologist.2009-0289.CrossRefPubMedPubMedCentral

Gillison ML, Zhang Q, Jordan R, Xiao W, Westra WH, Trotti A, et al. Tobacco smoking and increased risk of death and progression for patients with p16-positive and p16-negative oropharyngeal cancer. J Clin Oncol. 2012;30:2102–11. https://doi.org/10.1200/JCO.2011.38.4099.CrossRefPubMedPubMedCentral

Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tan PF, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med. 2010;363:24–35. https://doi.org/10.1056/NEJMoa0912217.CrossRefPubMedPubMedCentral

Cancer Genome Atlas Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. 2015;517(7536):576–82. https://doi.org/10.1038/nature14129.CrossRef

Bentzen SM. Theragnostic imaging for radiation oncology: dose-painting by numbers. Lancet Oncol. 2005;6:112–7.CrossRef

Ling CC, Humm J, Larson S, Amols H, Fuks Z, Leibel S, et al. Towards multidimensional radiotherapy (MD-CRT): biological imaging and biological conformality. Int J Radiat Oncol Biol Phys. 2000;47:551–60.CrossRef

Daisne J-F, Duprez T, Weynand B, Lonneux M, Hamoir M, Reychler H, et al. Tumor volume in pharyngolaryngeal squamous cell carcinoma: comparison at CT, MR imaging, and FDG PET and validation with surgical specimen. Radiology. 2004;233:93–100.CrossRef

10.

Lonneux M, Hamoir M, Reychler H, Maingon P, Duvillard C, Calais G, et al. 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. 2010;28:1190–5. https://doi.org/10.1200/JCO.2009.24.6298.CrossRefPubMed

11.

Mehanna H, Wong WL, McConkey CC, Rahman JK, Robinson M, Hartley AG, et al. PET-CT surveillance versus neck dissection in advanced head and neck cancer. N Engl J Med. 2016;374(15):1444–54. https://doi.org/10.1056/NEJMoa1514493.CrossRefPubMed

12.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):e1–34. https://doi.org/10.1016/j.jclinepi.2009.06.006.CrossRef

13.

Aslam S, Emmanuel P. Formulating a researchable question: a critical step for facilitating good clinical research. Indian J Sex Transm Dis. 2010;31(1):47–50. https://doi.org/10.4103/0253-7184.69003.CrossRef

14.

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 2.0. Eur J Nucl Med Mol Imaging. 2014;42:328–54. https://doi.org/10.1007/s00259-014-2961-x.CrossRefPubMedPubMedCentral

15.

Greenland S. Quantitative methods in the review of epidemiologic literature. Epidemiol Rev. 1987;9:1–30.CrossRef

16.

Begg C, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.CrossRef

17.

Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.CrossRefPubMedCentral

18.

Akagunduz OO, Savas R, Yalman D, Kocacelebi K, Esassolak M. Can adaptive threshold-based metabolic tumor volume (MTV) and lean body mass corrected standard uptake value (SUL) predict prognosis in head and neck cancer patients treated with definitive radiotherapy/chemoradiotherapy? Nucl Med Biol. 2015;42:899–904. https://doi.org/10.1016/j.nucmedbio.2015.06.007.CrossRefPubMed

19.

Castaldi P, Rufini V, Bussu F, Miccichè F, Dinapoli N, Autorino R, et al. Can “early” and “late”18F-FDG PET-CT be used as prognostic factors for the clinical outcome of patients with locally advanced head and neck cancer treated with radio-chemotherapy? Radiother Oncol. 2012;103:63–8. https://doi.org/10.1016/j.radonc.2012.03.001.CrossRefPubMed

20.

Castelli J, Depeursinge A, Ndoh V, Prior JO, Ozsahin M, Devillers A, et al. A PET-based nomogram for oropharyngeal cancers. Eur J Cancer. 2017;75:222–30. https://doi.org/10.1016/j.ejca.2017.01.018.CrossRefPubMed

21.

Chen S-W, Hsieh T-C, Yen K-Y, Yang S-N, Wang Y-C, Chien C-R, et al. Interim FDG PET/CT for predicting the outcome in patients with head and neck cancer. Laryngoscope. 2014;124:2732–8. https://doi.org/10.1002/lary.24826.CrossRefPubMed

22.

Cheng N-M, Dean Fang Y-H, Tung-Chieh Chang J, Huang C-G, Tsan D-L, Ng S-H, et al. Textural features of pretreatment 18F-FDG PET/CT images: prognostic significance in patients with advanced T-stage oropharyngeal squamous cell carcinoma. J Nucl Med. 2013;54:1703–9. https://doi.org/10.2967/jnumed.112.119289.CrossRefPubMed

23.

Man KC, Jeong HS, Sang GP, Jeon YJ, Son YI, Joon YC, et al. Metabolic tumor volume of [18F]-fluorodeoxyglucose positron emission tomography/computed tomography predicts short-term outcome to radiotherapy with or without chemotherapy in pharyngeal cancer. Clin Cancer Res. 2009;15:5861–8. https://doi.org/10.1158/1078-0432.CCR-08-3290.CrossRef

24.

Higgins KA, Hoang JK, Roach MC, Chino J, Yoo DS, Turkington TG, et al. Analysis of pretreatment FDG-PET SUV parameters in head-and-neck cancer: tumor SUV mean has superior prognostic value. Int J Radiat Oncol Biol Phys. 2012;82:548–53. https://doi.org/10.1016/j.ijrobp.2010.11.050.CrossRefPubMed

25.

Katahira-Suzuki R, Hata M, Tateishi U, Taguchi T, Takano S, Omura-Minamisawa M, et al. Definitive chemo-radiotherapy for squamous cell carcinoma of the pharynx: impact of baseline low hemoglobin level (<12 g/dL) and post-radiation therapy F-18 FDG-PET/CT. Ann Nucl Med. 2015;29:37–45. https://doi.org/10.1007/s12149-014-0907-9.CrossRefPubMed

26.

Kim R, Ock C-Y, Keam B, Kim TM, Kim JH, Paeng JC, et al. Predictive and prognostic value of PET/CT imaging post-chemoradiotherapy and clinical decision-making consequences in locally advanced head & neck squamous cell carcinoma: a retrospective study. BMC Cancer. 2016;16:116. https://doi.org/10.1186/s12885-016-2147-y.CrossRefPubMedPubMedCentral

27.

Koyasu S, Nakamoto Y, Kikuchi M, Suzuki K, Hayashida K, Itoh K, et al. Prognostic value of pretreatment 18F-FDG PET/CT parameters including visual evaluation in patients with head and neck squamous cell carcinoma. AJR Am J Roentgenol. 2014;202:851–8. https://doi.org/10.2214/AJR.13.11013.CrossRefPubMed

28.

Lin P, Min M, Lee M, Holloway L, Forstner D, Bray V, et al. Nodal parameters of FDG PET/CT performed during radiotherapy for locally advanced mucosal primary head and neck squamous cell carcinoma can predict treatment outcomes: SUVmean and response rate are useful imaging biomarkers. Eur J Nucl Med Mol Imaging. 2017;44:801–11. https://doi.org/10.1007/s00259-016-3584-1.CrossRefPubMed

29.

Marcus C, Ciarallo A, Tahari AK, Mena E, Koch W, Wahl RL, et al. Head and neck PET/CT: therapy response interpretation criteria (Hopkins criteria) – interreader reliability, accuracy, and survival outcomes. J Nucl Med. 2014;55:1411–6. https://doi.org/10.2967/jnumed.113.136796.CrossRefPubMedPubMedCentral

30.

Matoba M, Tuji H, Shimode Y, Kondo T, Oota K, Tonami H. The role of changes in maximum standardized uptake value of FDG PET-CT for post-treatment surveillance in patients with head and neck squamous cell carcinoma treated with chemoradiotherapy: preliminary findings. Br J Radiol. 2017;90(1071):20150404. https://doi.org/10.1259/bjr.20150404.CrossRefPubMedPubMedCentral

31.

Min M, Lin P, Lee M, Ho Shon I, Lin M, Forstner D, et al. Prognostic value of 2-[18F] fluoro-2-deoxy-D-glucose positron emission tomography-computed tomography scan carried out during and after radiation therapy for head and neck cancer using visual therapy response interpretation criteria. Clin Oncol. 2016;28:393–401. https://doi.org/10.1016/j.clon.2015.12.026.CrossRef

32.

Min M, Lin P, Lee MT, Shon IH, Lin M, Forstner D, et al. Prognostic role of metabolic parameters of 18F-FDG PET-CT scan performed during radiation therapy in locally advanced head and neck squamous cell carcinoma. Eur J Nucl Med Mol Imaging. 2015;42:1984–94. https://doi.org/10.1007/s00259-015-3104-8.CrossRefPubMedPubMedCentral

33.

Miyabe J, Hanamoto A, Inohara H. Prognostic value of metabolic tumor volume in head and neck cancer. Otolaryngol Head Neck Surg. 2009;155(1S).

34.

Miyabe J, Hanamoto A, Tatsumi M, Hamasaki T, Takenaka Y, Nakahara S, et al. Metabolic tumor volume of primary tumor predicts survival better than T classification in the larynx preservation approach. Cancer Sci. 2017;108:2030–8. https://doi.org/10.1111/cas.13345.CrossRefPubMedPubMedCentral

35.

Murphy JD, La TH, Chu K, Quon A, FIschbein NJ, Maxim PG, et al. Postradiation metabolic tumor volume predicts outcome in head-and-neck cancer. Int J Radiat Oncol Biol Phys. 2011;80(2):514–21. https://doi.org/10.1016/j.ijrobp.2010.01.057.CrossRefPubMed

36.

Ng SH, Liao CT, Lin CY, Chan SC, Lin YC, Yen TC, et al. Dynamic contrast-enhanced MRI, diffusion-weighted MRI and 18F-FDG PET/CT for the prediction of survival in oropharyngeal or hypopharyngeal squamous cell carcinoma treated with chemoradiation. Eur Radiol. 2016;26:4162–72. https://doi.org/10.1007/s00330-016-4276-8.CrossRefPubMed

37.

Park GC, Kim JS, Roh J-L, Choi S-H, Nam SY, Kim SY. Prognostic value of metabolic tumor volume measured by 18F-FDG PET/CT in advanced-stage squamous cell carcinoma of the larynx and hypopharynx. Ann Oncol. 2013;24:208–14. https://doi.org/10.1093/annonc/mds247.CrossRefPubMed

38.

Rasmussen JH, Vogelius IR, Fischer BM, Friborg J, Aznar MC, Persson GF, et al. Prognostic value of 18F-fludeoxyglucose uptake in 287 patients with head and neck squamous cell carcinoma. Head Neck. 2015;37(9):1274–81. https://doi.org/10.1002/hed.23745.CrossRefPubMed

39.

Romesser PB, Lim R, Spratt DE, Setton J, Riaz N, Lok B, et al. The relative prognostic utility of standardized uptake value, gross tumor volume, and metabolic tumor volume in oropharyngeal cancer patients treated with platinum based concurrent chemoradiation with a pre-treatment [(18)F] fluorodeoxyglucose positron emission tomography scan. Oral Oncol. 2014;50(9):802–8. https://doi.org/10.1016/j.oraloncology.2014.06.018.CrossRefPubMedPubMedCentral

40.

Schwartz DL, Harris J, Yao M, Rosenthal DI, Opanowski A, Levering A, et al. Metabolic tumor volume as a prognostic imaging-based biomarker for head-and-neck cancer: pilot results from Radiation Therapy Oncology Group protocol 0522. Int J Radiat Oncol Biol Phys. 2015;91:721–9. https://doi.org/10.1016/j.ijrobp.2014.12.023.CrossRefPubMedPubMedCentral

41.

Van Den Wyngaert T, Helsen N, Carp L, De Bree R, Martens MJ, Van Laer C, et al. ECLYPS: multicenter trial of FDG-PET/CT to detect residual nodal disease in locally advanced head-and-neck squamous cell carcinoma (LAHNSCC) after chemoradiotherapy (CRT). J Clin Oncol. 2016;34(15_suppl):6021. https://doi.org/10.1200/JCO.2016.34.15_suppl.6021.CrossRef

42.

Van Den Wyngaert T, Helsen N, Carp L, Hakim S, Martens MJ, Hutsebaut I, et al. Fluorodeoxyglucose-positron emission tomography/computed tomography after concurrent chemoradiotherapy in locally advanced head-and-neck squamous cell cancer: the ECLYPS study. J Clin Oncol. 2017;35:3458–64. https://doi.org/10.1200/JCO.2017.73.5845.CrossRefPubMed

43.

Yoon Y-H, Lee S-H, Hong S-L, Kim S-J, Roh H-J, Cho K-S. Prognostic value of metabolic tumor volume as measured by fluorine-18-fluorodeoxyglucose positron emission tomography/computed tomography in nasopharyngeal carcinoma. Int Forum Allergy Rhinol. 2014;4:845–50. https://doi.org/10.1002/alr.21363.CrossRefPubMed

44.

Zschaeck S, Löck S, Leger S, Haase R, Bandurska-Luque A, Appold S, et al. FDG uptake in normal tissues assessed by PET during treatment has prognostic value for treatment results in head and neck squamous cell carcinomas undergoing radiochemotherapy. Radiother Oncol. 2017;122:437–44. https://doi.org/10.1016/j.radonc.2017.01.019.CrossRefPubMed

45.

Castelli J, Depeursinge A, De Bari B, Devillers A, De Crevoisier R, Bourhis J, et al. Metabolic tumor volume and total lesion glycolysis in oropharyngeal cancer treated with definitive radiotherapy which threshold is the best predictor of local control? Clin Nucl Med. 2017;42:e281–5. https://doi.org/10.1097/RLU.0000000000001614.CrossRefPubMed

46.

Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.CrossRef

47.

O’Connor JP, Aboagye EO, Adams JE, Aerts HJ, Barrington SF, Beer AJ, et al. Imaging biomarker roadmap for cancer studies. Nat Rev Clin Oncol. 2017;14(3):169–86. https://doi.org/10.1038/nrclinonc.2016.162.CrossRefPubMed

48.

Halfpenny W, Hain SF, Biassoni L, Maisey MN, Sherman JA, McGurk M. FDG-PET. A possible prognostic factor in head and neck cancer. Cancer. 2002;86:512–6. https://doi.org/10.1038/sj.bjc.6600114.CrossRef

49.

Thorwarth D. Functional imaging for radiotherapy treatment planning: current status and future directions – a review. Br J Radiol. 2015;88(1051):20150056. https://doi.org/10.1259/bjr.20150056.CrossRefPubMedPubMedCentral

50.

Garibaldi C, Ronchi S, Cremonesi M, Gilardi L, Travaini L, Ferrari M, et al. Interim 18F-FDG PET/CT during chemoradiation therapy in the management of head and neck cancer patients: a systematic review. Radiat Oncol Biol. 2017;98:555–73. https://doi.org/10.1016/j.ijrobp.2017.02.217.CrossRef

51.

Pak K, Cheon GJ, Nam H-Y, Kim S-J, Kang KW, Chung J-K, et al. Prognostic value of metabolic tumor volume and total lesion glycolysis in head and neck cancer: a systematic review and meta-analysis. J Nucl Med. 2014;55:884–90. https://doi.org/10.2967/jnumed.113.133801.CrossRefPubMed

52.

Schinagl DA, Span PN, Oyen WJ, Kaanders JH. Can FDG PET predict radiation treatment outcome in head and neck cancer? Results of a prospective study. Eur J Nucl Med Mol Imaging. 2011;38(8):1449–58. https://doi.org/10.1007/s00259-011-1789-x.CrossRefPubMedPubMedCentral

53.

Tang C, Murphy JD, Khong B, La TH, Kong C, Fischbein NJ, et al. Validation that metabolic tumor volume predicts outcome in head-and-neck cancer. Radiat Oncol Biol. 2012;83:1514–20. https://doi.org/10.1016/j.ijrobp.2011.10.023.CrossRef

54.

Due AK, Vogelius IR, Aznar MC, Bentzen SM, Berthelsen AK, Korreman SS, et al. Recurrences after intensity modulated radiotherapy for head and neck squamous cell carcinoma more likely to originate from regions with high baseline [18F]-FDG uptake. Radiother Oncol. 2014;111:360–5. https://doi.org/10.1016/j.radonc.2014.06.001.CrossRefPubMedPubMedCentral

55.

Leclerc M, Lartigau E, Lacornerie T, Daisne J, Kramar A, Grégoire V. Primary tumor delineation based on 18 FDG PET for locally advanced head and neck cancer treated by chemo-radiotherapy. Radiother Oncol. 2015;116:87–93. https://doi.org/10.1016/j.radonc.2015.06.007.CrossRefPubMed

56.

Mohamed ASR, Cardenas CE, Garden AS, Awan MJ, Rock CD, Westergaard SA, et al. Patterns-of-failure guided biological target volume definition for head and neck cancer patients: FDG-PET and dosimetric analysis of dose escalation candidate subregions. Radiother Oncol. 2017;124:248–55. https://doi.org/10.1016/j.radonc.2017.07.017.CrossRefPubMedPubMedCentral

57.

Welz S, Mönnich D, Pfannenberg C, Nikolaou K, Reimold M, La C, et al. Prognostic value of dynamic hypoxia PET in head and neck cancer: results from a planned interim analysis of a randomized phase II hypoxia-image guided dose escalation trial. Radiother Oncol. 2017;124:526–32. https://doi.org/10.1016/j.radonc.2017.04.004.CrossRefPubMed

58.

Lambrecht M, Van Calster B, Vandecaveye V, De Keyzer F, Roebben I, Hermans R, et al. Integrating pretreatment diffusion weighted MRI into a multivariable prognostic model for head and neck squamous cell carcinoma. Radiother Oncol. 2014;110(3):429–34. https://doi.org/10.1016/j.radonc.2014.01.004.CrossRefPubMed

Title: What is the prognostic impact of FDG PET in locally advanced head and neck squamous cell carcinoma treated with concomitant chemo-radiotherapy? A systematic review and meta-analysis
Authors: Pierluigi Bonomo
A. Merlotti
E. Olmetto
A. Bianchi
I. Desideri
A. Bacigalupo
P. Franco
C. Franzese
E. Orlandi
L. Livi
S. Caini
Publication date: 01-11-2018
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Nuclear Medicine and Molecular Imaging / Issue 12/2018
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI: https://doi.org/10.1007/s00259-018-4065-5

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

What is the prognostic impact of FDG PET in locally advanced head and neck squamous cell carcinoma treated with concomitant chemo-radiotherapy? A systematic review and meta-analysis

Abstract

Purpose

Methods

Results

Conclusion

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 12/2018

Can integrated 18F-FDG PET/MR replace sentinel lymph node resection in malignant melanoma?

18F-NaF and 18F-FDG as molecular probes in the evaluation of atherosclerosis

Delivering PET imaging results to cancer patients: steps for handling ethical issues

Martin Vahlensieck and Maximilian Reiser (Eds). MRI of the Musculoskeletal System, Second Edition

Could we avoid computing TMTV of DLBCL patients in routine practice?

[18F]DOPA PET/ceCT in diagnosis and staging of primary medullary thyroid carcinoma prior to surgery