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Evaluation of a convolution neural network for baseline total tumor metabolic volume on [18F]FDG PET in diffuse large B cell lymphoma

  • Nuclear Medicine
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

New PET data-processing tools allow for automatic lesion selection and segmentation by a convolution neural network using artificial intelligence (AI) to obtain total metabolic tumor volume (TMTV) and total lesion glycolysis (TLG) routinely at the clinical workstation. Our objective was to evaluate an AI implemented in a new version of commercial software to verify reproducibility of results and time savings in a daily workflow.

Methods

Using the software to obtain TMTV and TLG, two nuclear physicians applied five methods to retrospectively analyze data for 51 patients. Methods 1 and 2 were fully automated with exclusion of lesions ≤ 0.5 mL and ≤ 0.1 mL, respectively. Methods 3 and 4 were fully automated with physician review. Method 5 was semi-automated and used as reference. Time and number of clicks to complete the measurement were recorded for each method. Inter-instrument and inter-observer variation was assessed by the intra-class coefficient (ICC) and Bland-Altman plots.

Results

Between methods 3 and 5, for the main user, the ICC was 0.99 for TMTV and 1.0 for TLG. Between the two users applying method 3, ICC was 0.97 for TMTV and 0.99 for TLG. Mean processing time (± standard deviation) was 20 s ± 9.0 for method 1, 178 s ± 125.7 for method 3, and 326 s ± 188.6 for method 5 (p < 0.05).

Conclusion

AI-enabled lesion detection software offers an automated, fast, reliable, and consistently performing tool for obtaining TMTV and TLG in a daily workflow.

Key Points

• Our study shows that artificial intelligence lesion detection software is an automated, fast, reliable, and consistently performing tool for obtaining total metabolic tumor volume and total lesion glycolysis in a daily workflow.

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Abbreviations

AI:

Artificial intelligence

CIER :

Internal Ethics and Research Committee

CNN:

Convolution neural network

DICOM:

Digital Imaging and COmmunications in Medicine

DLBCL :

Diffuse large cell lymphoma

FDG :

Fluorodeoxyglucose

GHICL:

Groupement des Hôpitaux de l'Institut Catholique de Lille

ICC :

Intra-class correlation coefficient

ICL:

Institut Catholique de Lille

IPI:

International Prognostic Index

MIP:

Maximum intensity projection

NCCN-IPI:

National Comprehensive Cancer Network- International Prognostic Index

NHL:

Non-Hodgkin’s lymphoma

PERCIST :

PET response criteria in solid tumors

PET:

Positron emission tomography

PFS:

Progression-free survival

ROI:

Region of interest

SD:

Standard deviation

SUV:

Standardized uptake value

TLG:

Total lesion glycolysis

TMTV:

Total metabolic tumor volume

References

  1. Flodr P, Latalova P, Tichy M, et al (2014) Diffuse large B-cell lymphoma: the history, current view and new perspectives. Neoplasma 62:491–504. https://doi.org/10.4149/neo_2014_062

  2. Cottereau A-S, Lanic H, Mareschal S et al (2016) Molecular profile and FDG-PET/CT total metabolic tumor volume improve risk classification at diagnosis for patients with diffuse large B-cell lymphoma. Clin Cancer Res 22:3801–3809. https://doi.org/10.1158/1078-0432.CCR-15-2825

    Article  CAS  PubMed  Google Scholar 

  3. Shagera QA, Cheon GJ, Koh Y et al (2019) Prognostic value of metabolic tumour volume on baseline 18F-FDG PET/CT in addition to NCCN-IPI in patients with diffuse large B-cell lymphoma: further stratification of the group with a high-risk NCCN-IPI. Eur J Nucl Med Mol Imaging 46:1417–1427. https://doi.org/10.1007/s00259-019-04309-4

    Article  CAS  PubMed  Google Scholar 

  4. Wight JC, Chong G, Grigg AP, Hawkes EA (2018) Prognostication of diffuse large B-cell lymphoma in the molecular era: moving beyond the IPI. Blood Rev 32:400–415. https://doi.org/10.1016/j.blre.2018.03.005

    Article  CAS  PubMed  Google Scholar 

  5. Nowakowski GS, Feldman T, Rimsza LM et al (2019) Integrating precision medicine through evaluation of cell of origin in treatment planning for diffuse large B-cell lymphoma. Blood Cancer J 9:48. https://doi.org/10.1038/s41408-019-0208-6

    Article  PubMed  PubMed Central  Google Scholar 

  6. Barrington SF, Mikhaeel NG, Kostakoglu L et al (2014) 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 32:3048–3058. https://doi.org/10.1200/JCO.2013.53.5229

    Article  PubMed  PubMed Central  Google Scholar 

  7. Vercellino L, Cottereau A-S, Casasnovas O et al (2020) High total metabolic tumor volume at baseline predicts survival independent of response to therapy. Blood 135:1396–1405. https://doi.org/10.1182/blood.2019003526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji - an Open Source platform for biological image analysis. Nat Methods 9. https://doi.org/10.1038/nmeth.2019

  9. Barrington SF, Zwezerijnen BGJC, de Vet HCW et al (2021) Automated segmentation of baseline metabolic total tumor burden in diffuse large B-cell lymphoma: which method is most successful? A Study on Behalf of the PETRA Consortium. J Nucl Med 62:332–337. https://doi.org/10.2967/jnumed.119.238923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ilyas H, Mikhaeel NG, Dunn JT et al (2018) Defining the optimal method for measuring baseline metabolic tumour volume in diffuse large B cell lymphoma. Eur J Nucl Med Mol Imaging 45:1142–1154. https://doi.org/10.1007/s00259-018-3953-z

    Article  PubMed  PubMed Central  Google Scholar 

  11. Barrington SF, Meignan M (2019) Time to prepare for risk adaptation in lymphoma by standardizing measurement of metabolic tumor burden. J Nucl Med 60:1096–1102. https://doi.org/10.2967/jnumed.119.227249

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sibille L, Seifert R, Avramovic N et al (2020) 18F-FDG PET/CT uptake classification in lymphoma and lung cancer by using deep convolutional neural networks. Radiology 294:445–452. https://doi.org/10.1148/radiol.2019191114

    Article  PubMed  Google Scholar 

  13. Hans CP, Weisenburger DD, Greiner TC et al (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103:275–282. https://doi.org/10.1182/blood-2003-05-1545

    Article  CAS  PubMed  Google Scholar 

  14. Wahl RL, Jacene H, Kasamon Y, Lodge MA (2009) From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med 50:122S–150S. https://doi.org/10.2967/jnumed.108.057307

    Article  CAS  PubMed  Google Scholar 

  15. Meignan M, Sasanelli M, Casasnovas RO et al (2014) Metabolic tumour volumes measured at staging in lymphoma: methodological evaluation on phantom experiments and patients. Eur J Nucl Med Mol Imaging 41:1113–1122. https://doi.org/10.1007/s00259-014-2705-y

    Article  CAS  PubMed  Google Scholar 

  16. Boellaard R, Delgado-Bolton R, Oyen WJG et al (2015) FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging 42:328–354. https://doi.org/10.1007/s00259-014-2961-x

  17. Guo B, Tan X, Ke Q, Cen H (2019) Prognostic value of baseline metabolic tumor volume and total lesion glycolysis in patients with lymphoma: a meta-analysis. PLoS One 14:e0210224. https://doi.org/10.1371/journal.pone.0210224

  18. Blanc-Durand P, Jégou S, Kanoun S et al (2021) Fully automatic segmentation of diffuse large B cell lymphoma lesions on 3D FDG-PET/CT for total metabolic tumour volume prediction using a convolutional neural network. Eur J Nucl Med Mol Imaging 48:1362–1370. https://doi.org/10.1007/s00259-020-05080-7

    Article  CAS  PubMed  Google Scholar 

  19. Tout M, Casasnovas O, Meignan M et al (2017) Rituximab exposure is influenced by baseline metabolic tumor volume and predicts outcome of DLBCL patients: a Lymphoma Study Association report. Blood 129:2616–2623. https://doi.org/10.1182/blood-2016-10-744292

    Article  CAS  PubMed  Google Scholar 

  20. Capobianco N, Meignan M, Cottereau A-S et al (2021) Deep-learning 18F-FDG uptake classification enables total metabolic tumor volume estimation in diffuse large B-cell lymphoma. J Nucl Med 62:30–36. https://doi.org/10.2967/jnumed.120.242412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Pinochet P, Eude F, Becker S et al (2021) Evaluation of an automatic classification algorithm using convolutional neural networks in oncological positron emission tomography. Front Med (Lausanne) 8:628179. https://doi.org/10.3389/fmed.2021.628179

    Article  PubMed  Google Scholar 

  22. Burggraaff CN, Rahman F, Kaßner I et al (2020) Optimizing workflows for fast and reliable metabolic tumor volume measurements in diffuse large B cell lymphoma. Mol Imaging Biol 22:1102–1110. https://doi.org/10.1007/s11307-020-01474-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nguyen NC, Vercher-Conejero J, Faulhaber P (2019) Tumor volume delineation: a pilot study comparing a digital positron-emission tomography prototype with an analog positron-emission tomography system. World J Nucl Med 18:45–51. https://doi.org/10.4103/wjnm.WJNM_22_18

    Article  PubMed  PubMed Central  Google Scholar 

  24. de Jong TL, Koopman D, van Dalen JA et al (2022) Performance of digital PET/CT compared with conventional PET/CT in oncologic patients: a prospective comparison study. Ann Nucl Med 36:756–764. https://doi.org/10.1007/s12149-022-01758-0

    Article  CAS  PubMed  Google Scholar 

  25. Koopman D, van Dalen JA, Stevens H et al (2020) Performance of digital PET compared with high-resolution conventional PET in patients with cancer. J Nucl Med 61:1448–1454. https://doi.org/10.2967/jnumed.119.238105

    Article  CAS  PubMed  Google Scholar 

  26. Cottereau A-S, Buvat I, Kanoun S et al (2018) Is there an optimal method for measuring baseline metabolic tumor volume in diffuse large B cell lymphoma? Eur J Nucl Med Mol Imaging 45:1463–1464. https://doi.org/10.1007/s00259-018-4005-4

    Article  PubMed  Google Scholar 

  27. Sun R, Deutsch E, Fournier L (2022) Intelligence artificielle et imagerie médicale. Bull Cancer 109:83–88. https://doi.org/10.1016/j.bulcan.2021.09.009

  28. Iacoboni G, Simó M, Villacampa G et al (2021) Prognostic impact of total metabolic tumor volume in large B-cell lymphoma patients receiving CAR T-cell therapy. Ann Hematol 100:2303–2310. https://doi.org/10.1007/s00277-021-04560-6

    Article  CAS  PubMed  Google Scholar 

  29. Schmidkonz C, Cordes M, Schmidt D et al (2018) 68Ga-PSMA-11 PET/CT-derived metabolic parameters for determination of whole-body tumor burden and treatment response in prostate cancer. Eur J Nucl Med Mol Imaging 45:1862–1872. https://doi.org/10.1007/s00259-018-4042-z

    Article  PubMed  Google Scholar 

  30. Capobianco N, Sibille L, Chantadisai M et al (2022) Whole-body uptake classification and prostate cancer staging in 68Ga-PSMA-11 PET/CT using dual-tracer learning. Eur J Nucl Med Mol Imaging 49:517–526. https://doi.org/10.1007/s00259-021-05473-2

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Mourtaza Karimdjee.

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The scientific guarantor of this publication is Mourtaza Karimdjee.

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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. No complex statistical methods were necessary for this paper.

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Written informed consent was obtained from all patients in this study. Written informed consent was waived by the Institutional Review Board.

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All procedures performed in studies involving human participants 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 or comparable ethical standards.

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Karimdjee, M., Delaby, G., Huglo, D. et al. Evaluation of a convolution neural network for baseline total tumor metabolic volume on [18F]FDG PET in diffuse large B cell lymphoma. Eur Radiol 33, 3386–3395 (2023). https://doi.org/10.1007/s00330-022-09375-1

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