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Published in: European Radiology 12/2016

01-12-2016 | Head and Neck

Combining standardized uptake value of FDG-PET and apparent diffusion coefficient of DW-MRI improves risk stratification in head and neck squamous cell carcinoma

Published in: European Radiology | Issue 12/2016

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Abstract

Objectives

To assess the independent prognostic value of standardized uptake value (SUV) and apparent diffusion coefficient (ADC), separately and combined, in order to evaluate if the combination of these two variables allows further prognostic stratification of patients with head and neck squamous cell carcinomas (HNSCC).

Methods

Pretreatment SUV and ADC were calculated in 57 patients with HNSCC. Mean follow-up was 21.3 months. Semiquantitative analysis of primary tumours was performed using SUVmaxT/B, ADCmean, ADCmin and ADCmax. The prognostic value of SUVmaxT/B, ADCmean, ADCmin and ADCmax in predicting disease-free survival (DFS) was evaluated with log-rank test and Cox regression models.

Results

Patients with SUVmaxT/B ≥5.75 had an overall worse prognosis (p = 0.003). After adjusting for lymph node status and diameter, SUVmaxT/B and ADCmin were both significant predictors of DFS with hazard ratio (HR) = 10.37 (95 % CI 1.22–87.95) and 3.26 (95 % CI 1.20–8.85) for SUVmaxT/B ≥5.75 and ADCmin ≥0.58 × 10−3 mm2/s, respectively. When the analysis was restricted to subjects with SUVmaxT/B ≥5.75, high ADCmin significantly predicted a worse prognosis, with adjusted HR = 3.11 (95 % CI 1.13–8.55).

Conclusions

The combination of SUVmaxT/B and ADCmin improves the prognostic role of the two separate parameters; patients with high SUVmaxT/B and high ADCmin are associated with a poor prognosis.

Key Points

High SUV maxT/B is a poor prognostic factor in HNSCC
High ADC min is a poor prognostic factor in HNSCC
In patients with high SUV maxT/B , high ADC min identified those with worse prognosis
Appendix
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Literature
1.
2.
go back to reference Partovi S, Kohan A, Vercher-Conejero JL et al (2014) Qualitative and quantitative performance of 18F-FDG-PET/MRI versus 18F-FDG-PET/CT in patients with head and neck cancer. AJNR Am J Neuroradiol 35:1970–1975CrossRefPubMed Partovi S, Kohan A, Vercher-Conejero JL et al (2014) Qualitative and quantitative performance of 18F-FDG-PET/MRI versus 18F-FDG-PET/CT in patients with head and neck cancer. AJNR Am J Neuroradiol 35:1970–1975CrossRefPubMed
3.
go back to reference Partovi S, Robbin MR, Steinbach OC et al (2014) Initial experience of MR/PET in a clinical cancer center. J Magn Reson Imaging 39:768–780CrossRefPubMed Partovi S, Robbin MR, Steinbach OC et al (2014) Initial experience of MR/PET in a clinical cancer center. J Magn Reson Imaging 39:768–780CrossRefPubMed
4.
go back to reference Varoquaux A, Rager O, Lovblad KO et al (2013) Functional imaging of head and neck squamous cell carcinoma with diffusion-weighted MRI and FDG PET/CT: quantitative analysis of ADC and SUV. Eur J Nucl Med Mol Imaging 40:842–852CrossRefPubMedPubMedCentral Varoquaux A, Rager O, Lovblad KO et al (2013) Functional imaging of head and neck squamous cell carcinoma with diffusion-weighted MRI and FDG PET/CT: quantitative analysis of ADC and SUV. Eur J Nucl Med Mol Imaging 40:842–852CrossRefPubMedPubMedCentral
5.
go back to reference Choi SH, Paeng JC, Sohn CH et al (2011) Correlation of 18F-FDG uptake with apparent diffusion coefficient ratio measured on standard and high b value diffusion MRI in head and neck cancer. J Nucl Med 52:1056–1062CrossRefPubMed Choi SH, Paeng JC, Sohn CH et al (2011) Correlation of 18F-FDG uptake with apparent diffusion coefficient ratio measured on standard and high b value diffusion MRI in head and neck cancer. J Nucl Med 52:1056–1062CrossRefPubMed
6.
go back to reference Purohit BS, Ailianou A, Dulguerov N, Becker CD, Ratib O, Becker M (2014) FDG-PET/CT pitfalls in oncological head and neck imaging. Insights Imaging 5:585–602CrossRefPubMedPubMedCentral Purohit BS, Ailianou A, Dulguerov N, Becker CD, Ratib O, Becker M (2014) FDG-PET/CT pitfalls in oncological head and neck imaging. Insights Imaging 5:585–602CrossRefPubMedPubMedCentral
7.
go back to reference Zhang XY, Sun YS, Tang L, Xue WC, Zhang XP (2011) Correlation of diffusion-weighted imaging data with apoptotic and proliferation indexes in CT26 colorectal tumor homografts in balb/c mouse. J Magn Reson Imaging 33:1171–1176CrossRefPubMed Zhang XY, Sun YS, Tang L, Xue WC, Zhang XP (2011) Correlation of diffusion-weighted imaging data with apoptotic and proliferation indexes in CT26 colorectal tumor homografts in balb/c mouse. J Magn Reson Imaging 33:1171–1176CrossRefPubMed
8.
go back to reference Chen Z, Ma L, Lou X, Zhou Z (2010) Diagnostic value of minimum apparent diffusion coefficient values in prediction of neuroepithelial tumor grading. J Magn Reson Imaging 31:1331–1338CrossRefPubMed Chen Z, Ma L, Lou X, Zhou Z (2010) Diagnostic value of minimum apparent diffusion coefficient values in prediction of neuroepithelial tumor grading. J Magn Reson Imaging 31:1331–1338CrossRefPubMed
9.
go back to reference Thoeny HC, De Keyzer F, King AD (2012) Diffusion-weighted MR imaging in the head and neck. Radiology 263:19–32CrossRefPubMed Thoeny HC, De Keyzer F, King AD (2012) Diffusion-weighted MR imaging in the head and neck. Radiology 263:19–32CrossRefPubMed
10.
go back to reference Driessen JP, Caldas-Magalhaes J, Janssen LM et al (2014) Diffusion-weighted MR imaging in laryngeal and hypopharyngeal carcinoma: association between apparent diffusion coefficient and histologic findings. Radiology 272:456–463CrossRefPubMed Driessen JP, Caldas-Magalhaes J, Janssen LM et al (2014) Diffusion-weighted MR imaging in laryngeal and hypopharyngeal carcinoma: association between apparent diffusion coefficient and histologic findings. Radiology 272:456–463CrossRefPubMed
11.
go back to reference Roh JL, Pae KH, Choi SH et al (2007) 2-[18F]-Fluoro-2-deoxy-D-glucose positron emission tomography as guidance for primary treatment in patients with advanced-stage resectable squamous cell carcinoma of the larynx and hypopharynx. Eur J Surg Oncol 33:790–795CrossRefPubMed Roh JL, Pae KH, Choi SH et al (2007) 2-[18F]-Fluoro-2-deoxy-D-glucose positron emission tomography as guidance for primary treatment in patients with advanced-stage resectable squamous cell carcinoma of the larynx and hypopharynx. Eur J Surg Oncol 33:790–795CrossRefPubMed
12.
go back to reference Machtay M, Natwa M, Andrel J et al (2009) Pretreatment FDG-PET standardized uptake value as a prognostic factor for outcome in head and neck cancer. Head Neck 31:195–201CrossRefPubMed Machtay M, Natwa M, Andrel J et al (2009) Pretreatment FDG-PET standardized uptake value as a prognostic factor for outcome in head and neck cancer. Head Neck 31:195–201CrossRefPubMed
13.
go back to reference Hatakenaka M, Shioyama Y, Nakamura K et al (2011) Apparent diffusion coefficient calculated with relatively high b-values correlates with local failure of head and neck squamous cell carcinoma treated with radiotherapy. AJNR Am J Neuroradiol 32:1904–1910CrossRefPubMed Hatakenaka M, Shioyama Y, Nakamura K et al (2011) Apparent diffusion coefficient calculated with relatively high b-values correlates with local failure of head and neck squamous cell carcinoma treated with radiotherapy. AJNR Am J Neuroradiol 32:1904–1910CrossRefPubMed
14.
go back to reference Kim S, Loevner L, Quon H et al (2009) Diffusion-weighted magnetic resonance imaging for predicting and detecting early response to chemoradiation therapy of squamous cell carcinoma of the head and neck. Clin Cancer Res 15:986–994CrossRefPubMedPubMedCentral Kim S, Loevner L, Quon H et al (2009) Diffusion-weighted magnetic resonance imaging for predicting and detecting early response to chemoradiation therapy of squamous cell carcinoma of the head and neck. Clin Cancer Res 15:986–994CrossRefPubMedPubMedCentral
15.
go back to reference Lambrecht M, Van Calster B, Vandecaveye V et al (2014) Integrating pretreatment diffusion weighted MRI into a multivariable prognostic model for head and neck squamous cell carcinoma. Radiother Oncol 110:429–434CrossRefPubMed Lambrecht M, Van Calster B, Vandecaveye V et al (2014) Integrating pretreatment diffusion weighted MRI into a multivariable prognostic model for head and neck squamous cell carcinoma. Radiother Oncol 110:429–434CrossRefPubMed
16.
go back to reference Nakajo M, Nakajo M, Kajiya Y et al (2012) FDG PET/CT and diffusion-weighted imaging of head and neck squamous cell carcinoma: comparison of prognostic significance between primary tumor standardized uptake value and apparent diffusion coefficient. Clin Nucl Med 37:475–480CrossRefPubMed Nakajo M, Nakajo M, Kajiya Y et al (2012) FDG PET/CT and diffusion-weighted imaging of head and neck squamous cell carcinoma: comparison of prognostic significance between primary tumor standardized uptake value and apparent diffusion coefficient. Clin Nucl Med 37:475–480CrossRefPubMed
17.
go back to reference King AD, Mo FK, Yu KH et al (2010) Squamous cell carcinoma of the head and neck: diffusion-weighted MR imaging for prediction and monitoring of treatment response. Eur Radiol 20:2213–2220CrossRefPubMed King AD, Mo FK, Yu KH et al (2010) Squamous cell carcinoma of the head and neck: diffusion-weighted MR imaging for prediction and monitoring of treatment response. Eur Radiol 20:2213–2220CrossRefPubMed
18.
go back to reference King AD, Chow KK, Yu KH et al (2013) Head and neck squamous cell carcinoma: diagnostic performance of diffusion-weighted MR imaging for the prediction of treatment response. Radiology 266:531–538CrossRefPubMed King AD, Chow KK, Yu KH et al (2013) Head and neck squamous cell carcinoma: diagnostic performance of diffusion-weighted MR imaging for the prediction of treatment response. Radiology 266:531–538CrossRefPubMed
19.
go back to reference Partovi S, Kohan AA, Zipp L et al (2014) Hybrid PET/MR imaging in two sarcoma patients - clinical benefits and implications for future trials. Int J Clin Exp Med 7:640–648PubMedPubMedCentral Partovi S, Kohan AA, Zipp L et al (2014) Hybrid PET/MR imaging in two sarcoma patients - clinical benefits and implications for future trials. Int J Clin Exp Med 7:640–648PubMedPubMedCentral
20.
go back to reference Boellaard R, Delgado-Bolton R, Oyen WJ et al (2015) FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging 42:328–354CrossRefPubMed Boellaard R, Delgado-Bolton R, Oyen WJ et al (2015) FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging 42:328–354CrossRefPubMed
21.
go back to reference Petralia G, Bonello L, Summers P et al (2011) Intraobserver and interobserver variability in the calculation of apparent diffusion coefficient (ADC) from diffusion-weighted magnetic resonance imaging (DW-MRI) of breast tumours. Radiol Med 116:466–476CrossRefPubMed Petralia G, Bonello L, Summers P et al (2011) Intraobserver and interobserver variability in the calculation of apparent diffusion coefficient (ADC) from diffusion-weighted magnetic resonance imaging (DW-MRI) of breast tumours. Radiol Med 116:466–476CrossRefPubMed
22.
go back to reference Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMed Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMed
24.
go back to reference Zhang B, Geng J, Nie F, Li X (2015) Primary tumor standardized uptake value predicts survival in head and neck squamous cell carcinoma. Oncol Res Treat 38:45–48CrossRefPubMed Zhang B, Geng J, Nie F, Li X (2015) Primary tumor standardized uptake value predicts survival in head and neck squamous cell carcinoma. Oncol Res Treat 38:45–48CrossRefPubMed
25.
go back to reference Minn H, Lapela M, Klemi PJ et al (1997) Prediction of survival with fluorine-18-fluoro-deoxyglucose and PET in head and neck cancer. J Nucl Med 38:1907–1911PubMed Minn H, Lapela M, Klemi PJ et al (1997) Prediction of survival with fluorine-18-fluoro-deoxyglucose and PET in head and neck cancer. J Nucl Med 38:1907–1911PubMed
26.
go back to reference Torizuka T, Tanizaki Y, Kanno T et al (2009) Prognostic value of 18F-FDG PET in patients with head and neck squamous cell cancer. Am J Roentgenol 192:156–160CrossRef Torizuka T, Tanizaki Y, Kanno T et al (2009) Prognostic value of 18F-FDG PET in patients with head and neck squamous cell cancer. Am J Roentgenol 192:156–160CrossRef
27.
go back to reference Minn H, Clavo AC, Grenman R et al (1995) In vitro comparison of cell proliferation kinetics and uptake of tritiated fluorodeoxyglucose and L-methionine in squamous cell carcinoma of the head and neck. J Nucl Med 36:252–258PubMed Minn H, Clavo AC, Grenman R et al (1995) In vitro comparison of cell proliferation kinetics and uptake of tritiated fluorodeoxyglucose and L-methionine in squamous cell carcinoma of the head and neck. J Nucl Med 36:252–258PubMed
28.
go back to reference Takahashi Y, Oriuchi N, Otake H, Endo K, Murase K (2008) Variability of lesion detectability and standardized uptake value according to the acquisition procedure and reconstruction among five PET scanners. Ann Nucl Med 22:543–548CrossRefPubMed Takahashi Y, Oriuchi N, Otake H, Endo K, Murase K (2008) Variability of lesion detectability and standardized uptake value according to the acquisition procedure and reconstruction among five PET scanners. Ann Nucl Med 22:543–548CrossRefPubMed
29.
go back to reference Chu KP, Murphy JD, La TH et al (2012) Prognostic value of metabolic tumor volume and velocity in predicting head-and-neck cancer outcomes. Int J Radiat Oncol Biol Phys 83:1521–1527CrossRefPubMedPubMedCentral Chu KP, Murphy JD, La TH et al (2012) Prognostic value of metabolic tumor volume and velocity in predicting head-and-neck cancer outcomes. Int J Radiat Oncol Biol Phys 83:1521–1527CrossRefPubMedPubMedCentral
30.
go back to reference Hoang JK, Das SK, Choudhury KR, Yoo DS, Brizel DM (2013) Using FDG-PET to measure early treatment response in head and neck squamous cell carcinoma: quantifying intrinsic variability in order to understand treatment-induced change. AJNR Am J Neuroradiol 34:1428–1433CrossRefPubMed Hoang JK, Das SK, Choudhury KR, Yoo DS, Brizel DM (2013) Using FDG-PET to measure early treatment response in head and neck squamous cell carcinoma: quantifying intrinsic variability in order to understand treatment-induced change. AJNR Am J Neuroradiol 34:1428–1433CrossRefPubMed
31.
go back to reference Kolff-Gart AS, Pouwels PJ, Noij DP et al (2015) Diffusion-weighted imaging of the head and neck in healthy subjects: reproducibility of ADC values in different MRI systems and repeat sessions. AJNR Am J Neuroradiol 36:384–390CrossRefPubMed Kolff-Gart AS, Pouwels PJ, Noij DP et al (2015) Diffusion-weighted imaging of the head and neck in healthy subjects: reproducibility of ADC values in different MRI systems and repeat sessions. AJNR Am J Neuroradiol 36:384–390CrossRefPubMed
33.
go back to reference Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:101–125CrossRef Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:101–125CrossRef
34.
go back to reference Le Bihan D, Breton E, Lallemand D et al (1988) Separation of diffusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505CrossRefPubMed Le Bihan D, Breton E, Lallemand D et al (1988) Separation of diffusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505CrossRefPubMed
35.
go back to reference Brizel DM, Sibley GS, Prosnitz LR et al (1997) Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 38:259–285CrossRef Brizel DM, Sibley GS, Prosnitz LR et al (1997) Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 38:259–285CrossRef
36.
go back to reference Stadler P, Becker A, Feldmann HJ et al (1999) Influence of the hypoxic subvolume on the survival of the patients with head and neck cancer. Int J Radiat Oncol Biol Phys 44:749–754CrossRefPubMed Stadler P, Becker A, Feldmann HJ et al (1999) Influence of the hypoxic subvolume on the survival of the patients with head and neck cancer. Int J Radiat Oncol Biol Phys 44:749–754CrossRefPubMed
38.
go back to reference Wang K, Ma W, Wang J et al (2012) Tumor-stroma ratio is an independent predictor for survival in esophageal squamous cell carcinoma. J Thorac Oncol 7:1457–1461CrossRefPubMed Wang K, Ma W, Wang J et al (2012) Tumor-stroma ratio is an independent predictor for survival in esophageal squamous cell carcinoma. J Thorac Oncol 7:1457–1461CrossRefPubMed
39.
go back to reference De Kruif EM, van Nes JG, van de Velde CJ et al (2011) Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients. Breast Cancer Res Treat 125:687–696CrossRef De Kruif EM, van Nes JG, van de Velde CJ et al (2011) Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients. Breast Cancer Res Treat 125:687–696CrossRef
40.
go back to reference Huibers A, Tollenaar RA, v Pelt GW et al (2013) The proportion of tumor-stroma as strong prognosticator for stage II and stage III colon cancer patients: validation in the VICTOR trial. Ann Oncol 24:179–185CrossRef Huibers A, Tollenaar RA, v Pelt GW et al (2013) The proportion of tumor-stroma as strong prognosticator for stage II and stage III colon cancer patients: validation in the VICTOR trial. Ann Oncol 24:179–185CrossRef
41.
go back to reference Koontongkaew S (2013) The tumor microenvironment contribution to development, growth, invasion and metastasis of head and neck squamous cell carcinoma. J Cancer 4:66–83CrossRefPubMedPubMedCentral Koontongkaew S (2013) The tumor microenvironment contribution to development, growth, invasion and metastasis of head and neck squamous cell carcinoma. J Cancer 4:66–83CrossRefPubMedPubMedCentral
42.
go back to reference Neesse A, Michl P, Frese KK et al (2011) Stromal biology and therapy in pancreatic cancer. Gut 60:861–868CrossRefPubMed Neesse A, Michl P, Frese KK et al (2011) Stromal biology and therapy in pancreatic cancer. Gut 60:861–868CrossRefPubMed
43.
go back to reference Mueller MM, Fusening NE (2004) Friends or foes - bipolar effects of the tumor stroma in cancer. Nat Rev Cancer 4:839–849CrossRefPubMed Mueller MM, Fusening NE (2004) Friends or foes - bipolar effects of the tumor stroma in cancer. Nat Rev Cancer 4:839–849CrossRefPubMed
44.
45.
go back to reference Maeda M, Kato H, Sakuma H, Maier SE, Takeda K (2005) Usefulness of the apparent diffusion coefficient in line scan diffusion-weighted imaging for distinguishing between squamous cell carcinomas and malignant lymphomas of the head and neck. AJNR Am J Neuroradiol 26:1186–1192PubMed Maeda M, Kato H, Sakuma H, Maier SE, Takeda K (2005) Usefulness of the apparent diffusion coefficient in line scan diffusion-weighted imaging for distinguishing between squamous cell carcinomas and malignant lymphomas of the head and neck. AJNR Am J Neuroradiol 26:1186–1192PubMed
46.
go back to reference Wang J, TakashimaS TF et al (2001) Head and neck lesions: characterization with diffusion-weighted echoplanar MR imaging. Radiology 220:621–630CrossRefPubMed Wang J, TakashimaS TF et al (2001) Head and neck lesions: characterization with diffusion-weighted echoplanar MR imaging. Radiology 220:621–630CrossRefPubMed
47.
go back to reference Reichert M, Ai T, Morelli JN, Nittka M, Attenberger U, Runge VM (2015) Metal artefact reduction in MRI at both 1.5 and 3.0 T using slice encoding for metal artefact correction and view angle tilting. Br J Radiol 88:20140601CrossRefPubMedPubMedCentral Reichert M, Ai T, Morelli JN, Nittka M, Attenberger U, Runge VM (2015) Metal artefact reduction in MRI at both 1.5 and 3.0 T using slice encoding for metal artefact correction and view angle tilting. Br J Radiol 88:20140601CrossRefPubMedPubMedCentral
Metadata
Title
Combining standardized uptake value of FDG-PET and apparent diffusion coefficient of DW-MRI improves risk stratification in head and neck squamous cell carcinoma
Publication date
01-12-2016
Published in
European Radiology / Issue 12/2016
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-016-4284-8

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