Texture analysis of 18F-FDG PET/CT and CECT: Prediction of refractoriness of Hodgkin lymphoma with mediastinal bulk involvement.

Hodgkin lymphoma PET bulky refractory disease textural analysis

Journal

Hematological oncology
ISSN: 1099-1069
Titre abrégé: Hematol Oncol
Pays: England
ID NLM: 8307268

Informations de publication

Date de publication:
Mar 2024
Historique:
revised: 18 01 2024
received: 26 09 2023
accepted: 22 02 2024
medline: 8 3 2024
pubmed: 8 3 2024
entrez: 8 3 2024
Statut: ppublish

Résumé

To recognize patients at high risk of refractory disease, the identification of novel prognostic parameters improving stratification of newly diagnosed Hodgkin Lymphoma (HL) is still needed. This study investigates the potential value of metabolic and texture features, extracted from baseline 18F-FDG Positron Emission Tomography/Computed Tomography (PET) and Contrast-Enhanced Computed Tomography scan (CECT), together with clinical data, in predicting first-line therapy refractoriness (R) of classical HL (cHL) with mediastinal bulk involvement. We reviewed 69 cHL patients who underwent staging PET and CECT. Lesion segmentation and texture parameter extraction were performed using the freeware software LIFEx 6.3. The prognostic significance of clinical and imaging features was evaluated in relation to the development of refractory disease. Receiver operating characteristic curve, Cox proportional hazard regression and Kaplan-Meier analyses were performed to examine the potential independent predictors and to evaluate their prognostic value. Among clinical characteristics, only stage according to the German Hodgkin Group (GHSG) classification system significantly differed between R and not-R. Among CECT variables, only parameters derived from second order matrices (gray-level co-occurrence matrix (GLCM) and gray-level run length matrix (GLRLM) demonstrated significant prognostic power. Among PET variables, SUVmean, several variables derived from first (histograms, shape), and second order analyses (GLCM, GLRLM, NGLDM) exhibited significant predictive power. Such variables obtained accuracies greater than 70% at receiver operating characteristic analysis and their PFS curves resulted statistically significant in predicting refractoriness. At multivariate analysis, only HISTO_EntropyPET extracted from PET (HISTO_Entropy

Identifiants

pubmed: 38454623
doi: 10.1002/hon.3261
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3261

Informations de copyright

© 2024 John Wiley & Sons Ltd.

Références

Mauch P, Goodman R, Hellman S. The significance of mediastinal involvement in early stage Hodgkin's disease. Cancer. 1978;42(3):1039-1045. https://doi.org/10.1002/1097-0142(197809)42:3<1039::aid-cncr2820420302>3.0.co;2-r
Moskowitz CH, Kewalramani T, Nimer SD, Gonzalez M, Zelenetz AD, Yahalom J. Effectiveness of high dose chemoradiotherapy and autologous stem cell transplantation for patients with biopsy-proven primary refractory Hodgkin’s disease. Br J Haematol. 3004;124(5):645-652. https://doi.org/10.1111/j.1365-2141.2003.04828.x
Allen PB, Gordon LI. Frontline therapy for classical Hodgkin lymphoma by stage and prognostic factors. Clin Med Insights Oncol. 2017;11:117955491773107. https://doi.org/10.1177/1179554917731072
Schomberg PJ, Evans RG, O'Connell MJ, et al. Prognostic significance of mediastinal mass in adult Hodgkin's disease. Cancer. 1984;53(2):324-328. https://doi.org/10.1002/1097-0142(19840115)53:2<324::aid-cncr2820530225>3.0.co;2-e
Aleman BM, Raemaekers JM, Tirelli U, et al. European organization for research and treatment of cancer lymphoma group. Involved-Field radiotherapy for advanced Hodgkin’s lymphoma. N Engl J Med. 2003;348(24):2396-2406. https://doi.org/10.1056/NEJMoa022628
Eichenauer DA, Aleman BMP, André M, et al. ESMO guidelines committee. Hodgkin lymphoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29(4):iv19-iv29. https://doi.org/10.1093/annonc/mdy080
Hasenclever D, Diehl V, Armitage JO, et al. A prognostic score for advanced Hodgkin’s disease. International prognostic factors project on advanced Hodgkin’s disease. N Engl J Med. 1998;339(21):1506-1514. https://doi.org/10.1056/NEJM199811193392104
Fermé C, Mounier N, Casasnovas O, et al. Groupe d'Etude des Lymphomes de l'Adulte. Long-term results and competing risk analysis of the H89 trial in patients with advanced-stage Hodgkin lymphoma: a study by the Groupe d'Etude des Lymphomes de l'Adulte (GELA). Blood. 2006;107(12):4636-4642. https://doi.org/10.1182/blood-2005-11-4429
Russell J, Collins A, Fowler A, et al. Advanced Hodgkin lymphoma in the East of England: a 10-year comparative analysis of outcomes for real-world patients treated with ABVD or escalated-BEACOPP, aged less than 60 years, compared with 5-year extended follow-up from the RATHL trial. Ann Hematol. 2021;100(4):1049-1058. https://doi.org/10.1007/s00277-021-04460-9
Hutchings M, Loft A, Hansen M, et al. FDG-PET after two cycles of chemotherapy predicts treatment failure and progression-free survival in Hodgkin lymphoma. Blood. 2006;107(1):52-59. https://doi.org/10.1182/blood-2005-06-2252
Ceriani L, Martelli M, Zinzani PL, et al. Utility of baseline 18FDG-PET/CT functional parameters in defining prognosis of primary mediastinal (thymic) large B-cell lymphoma. Blood. 2015;126(8):950-956. https://doi.org/10.1182/blood-2014-12-616474
Evens AM, Kostakoglu L. The role of FDG-PET in defining prognosis of Hodgkin lymphoma for early -stage disease. Blood. 2014;124(23):3356-3364. https://doi.org/10.1182/blood-2014-05-577627
Danielewicz I, Małkowski B, Zaucha R, Zalewska M, Leśniewski-Kmak K, Zaucha JM. Early treatment intensification with escalated BEACOPP in patients with Hodgkins lymphoma not responding to ABVD therapy. Acta Oncol. 2014;53(2):286-288. https://doi.org/10.3109/0284186X.2013.862344
Pardal E, Coronado M, Martín A, et al. Intensification treatment based on early FDG-PET in patients with high-risk diffuse large B-cell lymphoma: a phase II GELTAMO trial. Br J Haematol. 2014;167(3):327-336. https://doi.org/10.1111/bjh.13036
Kanoun S, Rossi C, Casasnovas O. [18F] FDG-PET/CT in Hodgkin lymphoma:current usefulness and perspectives. Cancer. 2018;10(5):145. https://doi.org/10.1111/bjh.13036
Abenavoli EM, Barbetti M, Linguanti F, et al. Characterization of mediastinal bulky lymphomas with FDG-PET-based radiomics and machine learning techniques. Cancers. 2023;15(7):1931. https://doi.org/10.3390/cancers15071931
Pugachev A, Ruan S, Carlin S, et al. Dependence of FDG uptake on tumour microenvironment. Int J Radiat Oncol Biol Phys. 2005;62(2):545-553. https://doi.org/10.1016/j.ijrobp.2005.02.009.30
Zhao S, Kuge Y, Mochizuki T, et al. Biologic correlates of intratu18 moral heterogeneity in F-FDG distribution with regional expression of glucose transporters and hexokinase-II in experimental tumor. J Nucl Med. 2005;46:675-682.
Knogler T, El -Rabadi K, Weber M, Karanikas G, Mayerhoefer ME. Three -dimensional texture analysis of contrast enhanced CT images for treatment response assessment in Hodgkin lymphoma: comparison with F -18 -FDG PET. Med Phys. 2014;41(12):121904. https://doi.org/10.1118/1.4900821
Ganeshan B, Miles KA, Babikir S, et al. CT -based texture analysis potentially provides prognostic information complementary to interim FDG PET for patients with Hodgkin's and aggressive non Hodgkin's lymphomas. Eur Radiol. 2017;27(3):1012-1020. https://doi.org/10.1007/s00330-016-4470-8
Harrison LC, Luukkaala T, Pertovaara H, et al. Non Hodgkin lymphoma response evaluation with MRI texture classification. J Exp Clin Cancer Res. 2009;28(1):87. https://doi.org/10.1186/1756-9966-28-87
Milgrom SA, Elhalawani H, Lee J, et al. A PET radiomics model to predict refractory mediastinal Hodgkin lymphoma. Sci Rep. 2019;9(1):1322. https://doi.org/10.1038/s41598-018-37197-z
Hatt M, Majdoub M, Vallières M, et al. 18F-FDG PET uptake characterization through texture analysis: investigating the complementary nature of heterogeneity and functionnal tumor volume in a multi-cancer site patient cohort. J Nucl Med. 2015;56(1):38-44. https://doi.org/10.2967/jnumed.114.144055
Ricardi U, Levis M, Evangelista A, et al. Role of radiotherapy to bulky sites of advanced Hodgkin lymphoma treated with ABVD: final results of FIL HD0801 trial. Blood Adv. 2021;5(21):4504-4514. https://doi.org/10.1182/bloodadvances.2021005150
Zinzani PL, Broccoli A, Gioia DM, et al. Interim positron emission tomography response-adapted therapy in advanced-stage Hodgkin lymphoma: final results of the phase II part of the HD0801 study. J Clin Oncol. 2016;34(12):1376-1385. Epub 2016 Feb 16. https://doi.org/10.1200/JCO.2015.63.0699
Meignan M, Gallamini A, Haioun C, Haioun C. Report on the first international workshop on interim-PET scan in lymphoma. Leuk Lymphoma. 2009;50(8):1257-1260. https://doi.org/10.1080/10428190903040048
Moskowitz CH, Walewski J, Nademanee A, et al. Five-year PFS from the AETHERA trial of brentuximab vedotin for Hodgkin lymphoma at high risk of progression or relapse. Blood. 2018;132(25):2639-2642. https://doi.org/10.1182/blood-2018-07-861641
Moskowitz CH, Nademanee A, Masszi T, et al. Brentuximab vedotin as consolidation therapy after autologous stem-cell transplantation in patients with Hodgkin's lymphoma at risk of relapse or progression (AETHERA): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2015;385(9980):1853-1862. Epub 2015 Mar 19. Erratum in: Lancet. 2015 Aug 8;386(9993). https://doi.org/10.1016/S0140-6736(15)60165-9
Nioche C, Orlhac F, Boughdad S, et al. LIFEx: a freeware for radiomic feature calculation in multimodality imaging to accelerate advances in the characterization of tumor heterogeneity. Cancer Res. 2018;78(16):4786-4789. (linfexsoft.org). https://doi.org/10.1158/0008-5472.CAN-18-0125
Kanoun S, Tal I, Berriolo-Riedinger A, et al. Influence of software tool and methodological aspects of total metabolic tumor volume calculation on baseline [18F]FDG PET to predict survival in Hodgkin lymphoma. PLoS One. 2015;10(10):e0140830. https://doi.org/10.1371/journal.pone.0140830
Barrington SF, Zwezerijnen BGJC, de Vet HCW, et al. 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. 2021;62(3):332-337. Epub 2020 Jul 17. https://doi.org/10.2967/jnumed.119.238923
Orlhac F, Boughdad S, Philippe C, et al. Postreconstruction harmonization method for multicenter radiomic studies in PET. J Nuclr Med Aug. 2018;59(8):1321-1328. https://doi.org/10.2967/jnumed.117.199935
Schieda N, Thornhill RE, Al-Subhi M, et al. Diagnosis of sarcomatoid renal cell carcinoma with CT: evaluation by qualitative imaging features and texture analysis. AJR Am J Roentgenol. 2015;204(5):1013-1023. https://doi.org/10.2214/AJR.14.13279
Fakhry C, Zhang Q, Nguyen-Tan PF, et al. Human papillomavirus and overall survival after progression of oropharyngeal squamous cell carcinoma. J Clin Oncol. 2014;32:3365-3373. https://doi.org/10.1200/JCO.2014.55.1937
Albano D, Mazzoletti A, Spallino M, et al. Prognostic role of baseline 18F-FDG PET/CT metabolic parameters in elderly HL: a two-center experience in 123 patients. Ann Hematol. 2020;99(6):1321-1330. https://doi.org/10.1007/s00277-020-04039-w
Angelopoulou MK, Mosa E, Pangalis GA, et al. The significance of PET/ CT in the initial staging of Hodgkin lymphoma: experience outside clinical trials. Anticancer Res. 2017;37:5727-5736. https://doi.org/10.21873/anticanres.12011
Minn H, Joensuu H, Ahonen A, Klemi P. Florodeoxyglucose imaging: a method to assess the proliferative activity of human cancer in vivo. Comparison with DNA flow cytometry in head and neck tumors. Cancer. 1988;61(9):1776-1781. https://doi.org/10.1002/1097-0142(19880501)61:9<1776::aid-cncr2820610909>3.0.co;2-7
Higashi K, Ueda Y, Yagishita M, et al. FDG PET measurement of the proliferative potential of non-small cell lung cancer. J Nucl Med. 2000;41(1):85-92.
Shou Y, Lu J, Chen T, Ma D, Tong L. Correlation of fluorodeoxyglucose uptake and tumor-proliferating antigen Ki-67 in lymphomas. J Cancer Res Ther. 2012;8(1):96-102. https://doi.org/10.4103/0973-1482.95182
Mettler J, Müller H, Voltin CA, et al. Metabolic tumour volume for response prediction in advanced-stage Hodgkin lymphoma. J Nucl Med. 2018;60(2):207-211. https://doi.org/10.2967/jnumed.118.210047
Kupik O, Akin S, Tuncel M, et al. Comparison of clinical and PET-derived prognostic factors in patients with non-Hodgkin lymphoma: a special emphasis on bone marrow involvement. Nucl Med Commun. 2020;41(6):540-549. https://doi.org/10.1097/MNM.0000000000001182
Frood R, Burton C, Tsoumpas C, et al. Baseline PET/CT imaging parameters for prediction of treatment outcome in Hodgkin and diffuse large B cell lymphoma: a systematic review. Eur J Nucl Med Mol Imag. 2021;48(10):3198-3220. https://doi.org/10.1007/s00259-021-05233-2
Ben Bouallègue F, Tabaa YA, Kafrouni M, Cartron G, Vauchot F, Mariano-Goulart D. Association between textural and morphological tumor indices on baseline PET-CT and early metabolic response on interim PET-CT in bulky malignant lymphomas. Med Phys. 2017;44(9):4608-4619. https://doi.org/10.1002/mp.12349
Karahan Şen NP, Aksu A, Kaya GÇ. Value of volumetric and textural analysis in predicting the treatment response in patients with locally advanced rectal cancer. Ann Nucl Med. 2020;34(12):960-967. https://doi.org/10.1007/s12149-020-01527-x
Zhang Y, Chen C, Tian Z, Cheng Y, Xu J. Differentiation of pituitary adenoma from rathke cleft cyst: combining MR image features with texture features. Contrast Media Mol Imaging. 2019;2019:1-9. https://doi.org/10.1155/2019/6584636
Xu R, Kido S, Suga K, et al. Texture analysis on (18)F-FDG PET/CT images to differentiate malignant and benign bone and soft-tissue lesions. Ann Nucl Med. 2014;28(9):926-935. https://doi.org/10.1007/s12149-014-0895-9
Sun YW, Ji CF, Wang H, et al. Differentiating gastric cancer and gastric lymphoma using texture analysis (TA) of positron emission tomography (PET). Chin Med J. 2020;134(4):439-447. https://doi.org/10.1097/CM9.0000000000001206
Tixier F, Le Rest CC, Hatt M, 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. 2011;52(3):369-378. https://doi.org/10.2967/jnumed.110.082404

Auteurs

Elisabetta M Abenavoli (EM)

Nuclear Medicine Unit, Department of Experimental and Clinical Biomedical Sciences 'Mario Serio', University of Florence, Florence, Italy.

Flavia Linguanti (F)

Nuclear Medicine Unit, Department of Experimental and Clinical Biomedical Sciences 'Mario Serio', University of Florence, Florence, Italy.

Matilde Anichini (M)

Department of Radiology, Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Vittorio Miele (V)

Department of Radiology, Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Francesco Mungai (F)

Department of Radiology, Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Marianna Palazzo (M)

Hematology Department, University of Florence and Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Luca Nassi (L)

Hematology Department, University of Florence and Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Benedetta Puccini (B)

Hematology Department, University of Florence and Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Ilaria Romano (I)

Hematology Department, University of Florence and Azienda Ospedaliero Universitaria Careggi, Florence, Italy.

Benedetta Sordi (B)

Hematology Department, University of Florence and Azienda Ospedaliero Universitaria Careggi, Florence, Italy.
Department of Experimental and Clinical Medicine, CRIMM, Center Research and Innovation of Myeloproliferative Neoplasms, Azienda Ospedaliera Universitaria Careggi, University of Florence, Florence, Italy.

Roberto Sciagrà (R)

Nuclear Medicine Unit, Department of Experimental and Clinical Biomedical Sciences 'Mario Serio', University of Florence, Florence, Italy.

Gabriele Simontacchi (G)

Radiation Oncology Unit, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy.

Alessandro M Vannucchi (AM)

Department of Experimental and Clinical Medicine, CRIMM, Center Research and Innovation of Myeloproliferative Neoplasms, Azienda Ospedaliera Universitaria Careggi, University of Florence, Florence, Italy.

Valentina Berti (V)

Nuclear Medicine Unit, Department of Experimental and Clinical Biomedical Sciences 'Mario Serio', University of Florence, Florence, Italy.

Classifications MeSH