Top

European Journal of Nuclear Medicine and Molecular Imaging

Published in:

Open Access 01-05-2018 | Original Article

Diagnostic and prognostic value of baseline FDG PET/CT skeletal textural features in diffuse large B cell lymphoma

Authors: Nicolas Aide, Marjolaine Talbot, Christophe Fruchart, Gandhi Damaj, Charline Lasnon

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 5/2018

Abstract

Purpose

Our purpose was to evaluate the diagnostic and prognostic value of skeletal textural features (TFs) on baseline FDG PET in diffuse large B cell lymphoma (DLBCL) patients.

Methods

Eighty-two patients with DLBCL who underwent a bone marrow biopsy (BMB) and a PET scan between December 2008 and December 2015 were included. Two readers blinded to the BMB results visually assessed PET images for bone marrow involvement (BMI) in consensus, and a third observer drew a volume of interest (VOI) encompassing the axial skeleton and the pelvis, which was used to assess skeletal TFs. ROC analysis was used to determine the best TF able to diagnose BMI among four first-order, six second-order and 11 third-order metrics, which was then compared for diagnosis and prognosis in disease-free patients (BMB−/PET-) versus patients considered to have BMI (BMB+/PET-, BMB−/PET+, and BMB+/PET+).

Results

Twenty-two out of 82 patients (26.8%) had BMI: 13 BMB−/PET+, eight BMB+/PET+ and one BMB+/PET-. Among the nine BMB+ patients, one had discordant BMI identified by both visual and TF PET assessment. ROC analysis showed that SkewnessH, a first-order metric, was the best parameter for identifying BMI with sensitivity and specificity of 81.8% and 81.7%, respectively. SkewnessH demonstrated better discriminative power over BMB and PET visual analysis for patient stratification: hazard ratios (HR), 3.78 (P = 0.02) versus 2.81 (P = 0.06) for overall survival (OS) and HR, 3.17 (P = 0.03) versus 1.26 (P = 0.70) for progression-free survival (PFS). In multivariate analysis accounting for IPI score, bulky status, haemoglobin and SkewnessH, the only independent predictor of OS was the IPI score, while the only independent predictor of PFS was SkewnessH.

Conclusion

The better discriminative power of skeletal heterogeneity for risk stratification compared to BMB and PET visual analysis in the overall population, and more specifically in BMB−/PET- patients, suggests that it can be useful to identify diagnostically overlooked BMI.

Tilly H, Gomes da Silva M, Vitolo U, Jack A, Meignan M, Lopez-Guillermo A, et al. Diffuse large B-cell lymphoma (DLBCL): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of oncology : official journal of the European Society for Medical Oncology. 2015;26(Suppl 5):v116–25. https://doi.org/10.1093/annonc/mdv304.CrossRef

Barrington SF, Mikhaeel NG, Kostakoglu L, Meignan M, Hutchings M, Mueller SP, et al. Role of imaging in the staging and response assessment of lymphoma: consensus of the international conference on malignant lymphomas imaging working group. J Clin Oncol : Off J Am Soc Clin Oncol. 2014;32:3048–58. https://doi.org/10.1200/jco.2013.53.5229.CrossRef

Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol : Off J Am Soc Clin Oncol. 2014;32:3059–68. https://doi.org/10.1200/jco.2013.54.8800.CrossRef

Cheson BD. Role of functional imaging in the management of lymphoma. J Clin Oncol : Off J Am Soc Clin Oncol. 2011;29:1844–54. https://doi.org/10.1200/jco.2010.32.5225.CrossRef

Berthet L, Cochet A, Kanoun S, Berriolo-Riedinger A, Humbert O, Toubeau M, et al. In newly diagnosed diffuse large B-cell lymphoma, determination of bone marrow involvement with 18F-FDG PET/CT provides better diagnostic performance and prognostic stratification than does biopsy. J Nucl Med : Off publ, Soc Nucl Med. 2013;54:1244–50. https://doi.org/10.2967/jnumed.112.114710.CrossRef

Khan AB, Barrington SF, Mikhaeel NG, Hunt AA, Cameron L, Morris T, et al. PET-CT staging of DLBCL accurately identifies and provides new insight into the clinical significance of bone marrow involvement. Blood. 2013;122:61–7. https://doi.org/10.1182/blood-2012-12-473389.CrossRefPubMed

Pelosi E, Penna D, Douroukas A, Bello M, Amati A, Arena V, et al. Bone marrow disease detection with FDG-PET/CT and bone marrow biopsy during the staging of malignant lymphoma: results from a large multicentre study. Quarter J Nucl Med Molec Imag : Off Publ Italian Assoc Nucl Med (AIMN) [and] Int Assoc Radiopharmacol (IAR), [and] Sect So. 2011;55:469–75.

Adams HJ, Kwee TC, de Keizer B, Fijnheer R, de Klerk JM, Nievelstein RA. FDG PET/CT for the detection of bone marrow involvement in diffuse large B-cell lymphoma: systematic review and meta-analysis. Eur J Nucl Med Mol Imaging. 2014;41:565–74. https://doi.org/10.1007/s00259-013-2623-4.CrossRefPubMed

Paone G, Itti E, Haioun C, Gaulard P, Dupuis J, Lin C, et al. Bone marrow involvement in diffuse large B-cell lymphoma: correlation between FDG-PET uptake and type of cellular infiltrate. Eur J Nucl Med Mol Imaging. 2009;36:745–50. https://doi.org/10.1007/s00259-008-1021-9.CrossRefPubMed

10.

Hong J, Lee Y, Park Y, Kim SG, Hwang KH, Park SH, et al. Role of FDG-PET/CT in detecting lymphomatous bone marrow involvement in patients with newly diagnosed diffuse large B-cell lymphoma. Ann Hematol. 2012;91:687–95. https://doi.org/10.1007/s00277-011-1353-6.CrossRefPubMed

11.

Tixier F, Hatt M, Valla C, Fleury V, Lamour C, Ezzouhri S, et al. Visual versus quantitative assessment of intratumor 18F-FDG PET uptake heterogeneity: prognostic value in non-small cell lung cancer. J Nucl Med : Off Publ, Soc Nucl Med. 2014;55:1235–41. https://doi.org/10.2967/jnumed.113.133389.CrossRef

12.

Tixier F, Le Rest CC, Hatt M, Albarghach N, Pradier O, Metges JP, et al. Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med : Off Publ, Soc Nucl Med. 2011;52:369–78. https://doi.org/10.2967/jnumed.110.082404.CrossRef

13.

Lee YS, Kim JS, Kim KM, Kang JH, Lim SM, Kim HJ. Performance measurement of PSF modeling reconstruction (true X) on Siemens biograph TruePoint TrueV PET/CT. Ann Nucl Med. 2014;28:340–8. https://doi.org/10.1007/s12149-014-0815-z.CrossRefPubMed

14.

van der Vos CS, Koopman D, Rijnsdorp S, Arends AJ, Boellaard R, van Dalen JA, et al. Quantification, improvement, and harmonization of small lesion detection with state-of-the-art PET. Eur J Nucl Med Mol Imaging. 2017;44:4–16. https://doi.org/10.1007/s00259-017-3727-z.CrossRefPubMedPubMedCentral

15.

Soret M, Bacharach SL, Buvat I. Partial-volume effect in PET tumor imaging. J Nucl Med : Off Publ, Soc Nucl Med. 2007;48:932–45. https://doi.org/10.2967/jnumed.106.035774.CrossRef

16.

Orlhac F, Nioche C, Soussan M, Buvat I. Understanding changes in tumor texture indices in PET: a comparison between visual assessment and index values in simulated and patient data. J Nucl Med : Off Publ, Soc Nucl Med. 2017;58:387–92. https://doi.org/10.2967/jnumed.116.181859.CrossRef

17.

Reuze S, Orlhac F, Chargari C, Nioche C, Limkin E, Riet F, et al. Prediction of cervical cancer recurrence using textural features extracted from 18F-FDG PET images acquired with different scanners. Oncotarget. 2017;8:43169–79. https://doi.org/10.18632/oncotarget.17856.CrossRefPubMedPubMedCentral

18.

Hatt M, Majdoub M, Vallieres M, Tixier F, Le Rest CC, Groheux D, et al. 18F-FDG PET uptake characterization through texture analysis: investigating the complementary nature of heterogeneity and functional tumor volume in a multi-cancer site patient cohort. J Nucl Med : Off Publ, Soc Nucl Med. 2015;56:38–44. https://doi.org/10.2967/jnumed.114.144055.CrossRef

19.

Vallieres M, Freeman CR, Skamene SR, El Naqa I. A radiomics model from joint FDG-PET and MRI texture features for the prediction of lung metastases in soft-tissue sarcomas of the extremities. Phys Med Biol. 2015;60:5471–96. https://doi.org/10.1088/0031-9155/60/14/5471.CrossRefPubMed

20.

Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.CrossRefPubMed

21.

Jin H, Lu Y. A non-inferiority test of areas under two parametric ROC curves. Contemporary Clin Trials. 2009;30:375–9. https://doi.org/10.1016/j.cct.2009.03.003.CrossRef

22.

Boellaard R, Delgado-Bolton R, Oyen WJ, 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. 2015;42:328–54. https://doi.org/10.1007/s00259-014-2961-x.CrossRefPubMed

23.

Wagner F, Hakami YA, Warnock G, Fischer G, Huellner MW, Veit-Haibach P. Comparison of contrast-enhanced CT and [18F]FDG PET/CT analysis using kurtosis and Skewness in patients with primary colorectal cancer. Molec Imaging Biol : MIB : Off Publ Acad Molec Imaging. 2017; https://doi.org/10.1007/s11307-017-1066-x.

24.

Adams HJ, Nievelstein RA, Kwee TC. Opportunities and limitations of bone marrow biopsy and bone marrow FDG-PET in lymphoma. Blood Rev. 2015;29:417–25. https://doi.org/10.1016/j.blre.2015.06.003.CrossRefPubMed

25.

Brunning RD, Bloomfield CD, McKenna RW, Peterson LA. Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic diseases. Ann Intern Med. 1975;82:365–6.CrossRefPubMed

26.

Coller BS, Chabner BA, Gralnick HR. Frequencies and patterns of bone marrow involvement in non-Hodgkin lymphomas: observations on the value of bilateral biopsies. Am J Hematol. 1977;3:105–19.CrossRefPubMed

27.

Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer. 2002;94:1522–31.CrossRefPubMed

28.

Lasnon C, Majdoub M, Lavigne B, Do P, Madelaine J, Visvikis D, et al. 18F-FDG PET/CT heterogeneity quantification through textural features in the era of harmonisation programs: a focus on lung cancer. Eur J Nucl Med Mol Imaging. 2016;43:2324–35. https://doi.org/10.1007/s00259-016-3441-2.CrossRefPubMed

29.

Shiri I, Rahmim A, Ghaffarian P, Geramifar P, Abdollahi H, Bitarafan-Rajabi A. The impact of image reconstruction settings on 18F-FDG PET radiomic features: multi-scanner phantom and patient studies. Eur Radiol. 2017:1–12. https://doi.org/10.1007/s00330-017-4859-z.

30.

Galavis PE, Hollensen C, Jallow N, Paliwal B, Jeraj R. Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta oncologica (Stockholm, Sweden). 2010;49:1012–6. https://doi.org/10.3109/0284186x.2010.498437.CrossRef

31.

Aide N, Lasnon C, Veit-Haibach P, Sera T, Sattler B, Boellaard R. EANM/EARL harmonization strategies in PET quantification: from daily practice to multicentre oncological studies. Eur J Nucl Med Mol Imaging. 2017;44:17–31. https://doi.org/10.1007/s00259-017-3740-2.CrossRefPubMedPubMedCentral

Title: Diagnostic and prognostic value of baseline FDG PET/CT skeletal textural features in diffuse large B cell lymphoma
Authors: Nicolas Aide
Marjolaine Talbot
Christophe Fruchart
Gandhi Damaj
Charline Lasnon
Publication date: 01-05-2018
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Nuclear Medicine and Molecular Imaging / Issue 5/2018
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI: https://doi.org/10.1007/s00259-017-3899-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Diagnostic and prognostic value of baseline FDG PET/CT skeletal textural features in diffuse large B cell lymphoma

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 5/2018

Combination of baseline FDG PET/CT total metabolic tumour volume and gene expression profile have a robust predictive value in patients with diffuse large B-cell lymphoma

Targeting PSMA by radioligands in non-prostate disease—current status and future perspectives

Preoperative prediction of microvascular invasion of hepatocellular carcinoma using 18F-FDG PET/CT: a multicenter retrospective cohort study

Yuji Kuge, Tohru Shiga, Nagara Tamaki (editors): Perspectives on nuclear medicine for molecular diagnosis and integrated therapy

The diagnostic value of 18F–FDG-PET/CT and MRI in suspected vertebral osteomyelitis – a prospective study

Comparison of positron emission tomography/computed tomography and magnetic resonance imaging for posttherapy evaluation in patients with advanced cervical cancer receiving definitive concurrent chemoradiotherapy