Informativeness of whole-body diffusion-weighted magnetic resonance imaging and positron emission tomography with computed tomography in follicular lymphoma

Abstract

Aim. This study conducted the possibilities of diffusion-weighted magnetic resonance imaging of the whole body – diffusion WB-MRI (in comparison with positron emission tomography with computed tomography – PET/CT) in assessing the volume and prevalence of the tumor, as well as determining bone marrow (BM) damage (for various cytological types) in the diagnosis and staging of the disease in patients with FL.

Materials and methods. A prospective comparative search study included 15 patients (4 men and 11 women, with a median age of 53 years) with newly diagnosed FL. Patients have not received antitumor chemotherapy previously. After the diagnosis was established, all patients (with the blindness of both the cases themselves and some specialists regarding the results of other specialists) were examined by PET/CT and diffusion WB-MRI, after which a BM examination was performed (histological examination and determination of B-cell clonality in BM puncture by PCR). Using the diffusion WB-MRI method, the prevalence of tumor lesion (nodal and extranodal foci) in each patient was estimated, and the total tumor volume was calculated, BM lesion was detected, and BM lesion volume was calculated. For lesions of different localization, the measured diffusion coefficient (DC) of the diffusion WB-MRI and the standardized rate of accumulation of the radiopharmaceutical in tissues (SUV) of the PET/CT method were determined and compared with each other (for the same areas). Statistical analysis was performed using the estimate of agreement (by Cohen’s kappa coefficient and asymptotic test) of the results of the compared methods.

Results. Estimates of the prevalence of tumor damage (lymph nodes and extranodal foci) using the diffusion WB-MRI and PET/CT methods were the same. High DC and SUV were observed in the peripheral lymph nodes, extranodal foci and bulky, low DC and SUV – in the foci of BM. All 4 methods successfully determined BM damage, however, the diffusion WB-MRI had comparatively less negative results. The highest values of SUV and CD were noted in cases of the 3 grade of FL. Using the diffusion WB-MRI method, the prevalence of tumor lesion was assessed in each patient (nodal and extranodal foci were detected) and the total tumor volume was calculated, BM lesion detection was performed, and the volume of BM lesion was calculated. It is important to note that with the help of diffusion WB-MRI, it was possible to measure separately the total tumor volume (46–2025 cm3) and separately the volume of bulky (25–1358 cm3). The diffusion WB-MRI allowed us to differentiate the volume of tumor tissue (reduced as a result of treatment) and residual (fibrous-adipose) tissue in residual formations (which averaged 21% of the initial volume). The predictors of a poor antitumor response were the maximum SUV values (more than 14.0) and the minimum DC values (0.5¥10-3 mm2/s) in the BM foci.

Conclusion. The diffusion WB-MRI allows for detailed visualization of BM lesions and surrounding soft tissues both in the debut of the FL and in the process of tracking the effectiveness of chemotherapy, which makes it possible to use it along with PET/CT. Diffusion WB-MRI allows to separately evaluate the volume of true tumor tissue and residual tissue. Cases of the 3 grade of FL (including the transformation of FL into diffuse B-large cell lymphoma) are isolated due to low DC values (and high SUV values) in the tumor tissue. BM foci of FL lesion also have (in comparison with nodal and extranodal foci) lower DC values. The predictors of a poor antitumor response were high (from 14.0 or more) SUV valuesin the tumor (and especially in bulky), and low (about 0.5¥103 mm2/s) DC values of BM foci. The PET/CT and diffusion WB-MRI have proven to be reliable diagnostic tools for establishing the stage of FL and detecting BM damage. Diffusion WB-MRI for FL is an informative first-line diagnostic method that allows regular monitoring of the disease and early detection of foci of relapse and disease progression.

About the authors

E. S. Nesterova

National Research Center for Hematology

Author for correspondence.
Email: nest.ek@yandex.ru
ORCID iD: 0000-0002-6035-9547

к.м.н., науч. сотр., врач-гематолог отд-ния интенсивной высокодозной химиотерапии гемобластозов с дневным и круглосуточным стационаром

Russian Federation, Moscow

G. A. Yatsyk

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0001-8589-6122

к.м.н., зав. отд-нием магнитно-резонансной томографии и ультразвуковой диагностики

Russian Federation, Moscow

N. S. Lutsik

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0002-7556-2054

врач-рентгенолог отделения магнитно-резонансной томографии и ультразвуковой диагностики

Russian Federation, Moscow

S. K. Kravchenko

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0002-1269-1449

к.м.н., зав. отд-нием интенсивной высокодозной химиотерапии гемобластозов с дневным и круглосуточным стационаром

Russian Federation, Moscow

A. B. Sudarikov

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0001-9463-9187

д.б.н., зав. лаб. молекулярной гематологии

Russian Federation, Moscow

I. V. Krasil‘nikova

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0002-0399-4309
Russian Federation, Moscow

E. G. Gemdzhian

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0002-8357-977X

с.н.с. лаб. биостатистики

Russian Federation, Moscow

A. M. Kovrigina

National Research Center for Hematology

Email: nest.ek@yandex.ru
ORCID iD: 0000-0002-1082-8659

д.б.н., зав. патологоанатомическим отд-нием

Russian Federation, Moscow

References

  1. Cheson BD, Fisher RI, Barrington SF, et al. Recommendations for initial evaluation, staging and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059-67. doi: 10.1200/JCO.2013.54.8800
  2. Galia M, Albano D, Tarella C, et al. Whole Body Magnetic Resonance in Indolent Lymphomas Under Watchful Waiting: The Time Is Now. Eur Radiol. 2018;28(3):1187-93. PMID: 29018927. doi: 10.1007/s00330-017-5071-x
  3. Cavo M, Terpos E, Nanni Cr, et al. Role of 18 F-FDG PET/CT in the Diagnosis and Management of Multiple Myeloma and Other Plasma Cell Disorders: A Consensus Statement by the International Myeloma Working Group. Lancet Oncol. 2017;18(4):e206-e217. doi: 10.1016/S1470-2045(17)30189-4
  4. Hallek M, Cheson BD, Catovsky D, et al. IwCLL Guidelines for Diagnosis, Indications for Treatment, Response Assessment, and Supportive Management of CLL. Blood. 2018;131(25):2745-60. PMID: 29540348. doi: 10.1182/blood-2017-09-806398
  5. Kwee TC, Takahara T, Ochiai R, et al. Whole-body diffusionweighted magnetic resonance imaging. Eur Radiol. 2009;70:409-17. PMID: 19403255. doi: 10.1016/j.ejrad.2009.03.054
  6. Darge K, Jaramillo D, Siegel MJ. Whole-body MRI in children: Current status and future applications. Eur Radiol. 2008;68:289-98. PMID: 18799279. doi: 10.1016/j.ejrad.2008.05.018
  7. Vilanova JC, Barcel´o J. Diffusion-weighted whole-body MR screening. Eur Radiol. 2008;67:440-7. PMID: 18430538. doi: 10.1016/j.ejrad.2008.02.040
  8. Giraudo Ch, Karanikas G, Weber M, et al. Correlation between glycolytic activity on [18F]-FDG-PET and cell density on diffusion-weighted MRI in lymphoma at staging. J Magn Reson Imaging. 2018 May;47(5):1217-26. PMID: 29086453. doi: 10.1002/jmri.25884
  9. Wu X, Sikiö M, Pertovaara H, et al. Differentiation of Diffuse Large B-cell Lymphoma From Follicular Lymphoma Using Texture Analysis on Conventional MR Images at 3.0 Tesla. Acad Radiol. 2016 Jun;23(6):696-703. doi: 10.1016/j.acra.2016.01.012
  10. Нестерова Е.С., Кравченко С.К., Ковригина А.М. и др. Фолликулярная лимфома: критерии выбора терапии первой линии. Терапевтический архив. 2019;91(8):75-83 [Nesterova ES, Kravchenko SK, Kovrigina AM, et al. Follicular lymphoma: first-line selection criteria of treatment. Therapeutic Archive. 2019;91(8):75-83 (In Russ.)]. doi: 10.26442/00403660.2019.08.000388
  11. Нестерова Е.С., Кравченко С.К., Ковригина А.М. и др. Фолликулярная лимфома: результаты многоцентрового исследования терапии первой линии препаратами бендамустин и ритуксимаб; факторы риска неблагоприятных событий (протокол FL-RUS-2013). Онкогематология. 2018;13(3):10-24 [Nesterova ES, Kravchenko SK, Kovrigina AM, et al. Follicular lymphoma: results of multicenter study of first-line therapy with bendamustine and rituximab; risk factors for adverse events (FL-RUS-2013 protocol). Onkogematologiya = Oncohematology. 2018;13(3):10-24 (In Russ.)]. doi: 10.17650/1818-8346- 2018-13-3-10-24
  12. Нестерова Е.С., Кравченко С.К., Барях Е.А. и др. Tрансплантация аутологичных стволовых клеток крови в первой ремиссии фолликулярной лимфомы как «терапия спасения» пациентов с факторами неблагоприятного прогноза. Результаты первого проспективного исследования. Современная онкология. 2016;18(5):31-2 [Nestero- va ES, Kravchenko SK, Baryakh EA, et al. Autologous stem cells transplantation in the first remission of follicular lymphoma as “rescue therapy” in patients with unfavorable prognosis factors. The first prospective study results. Journal of Modern Oncology. 2016;18(5):31-2 (In Russ.)]. doi: 10.26442/1815-1434_2016.5.31-32
  13. Воробьев В.И., Гемджян Э.Г., Дубровин Е.И. и др. Риск-адаптированная интенсивная индукционная терапия, аутологичная трансплантация стволовых кроветворных клеток и поддерживающая терапия ритуксимабом позволяют достигнуть высоких показателей 7-летней выживаемости у больных лимфомой из клеток мантийной зоны. Терапевтический архив. 2019;91(7):41-51. doi: 10.26442/00403660.2019.07.000322 [Vorobyev VI, Gemdzhian EG, Dubrovin EI, et al. Risk-adapted intensive induction therapy, autologous stem cell transplantation, and rituximab maintenance allow to reach a high 7-year survival rate in patients with mantle cell lymphoma. Therapeutic Archive. 2019;91(7):41-51 (In Russ.)]. doi: 10.26442/00403660.2019.07.000322
  14. Bammer R. Basic principles of diffusion-weighted imaging. Eur Radiol. 2003;45:169-84. PMID: 12595101. doi: 10.1016/s0720-048x(02)00303-0
  15. Wong FC, Kim EE. A review of molecular imaging studies reaching the clinical stage. Eur Radiol. 2009;70:205-211. PMID: 19299097. doi: 10.1016/j.ejrad.2009.01.049
  16. Abdulqadhr G, Molin D, Aström G. Whole body diffusion weighted imaging compared with FDG PET/CT in staging of lymphoma patients. Acta Radiol 2011;52:173-80. PMID: 21498346. doi: 10.1258/ar.2010.100246
  17. Mayerhoefer ME, Karanikas G, Kletter K. Evaluation of diffusion-weighted MRI for pretherapeutic assessment and staging of lymphoma: Results of a prospective study in 140 patients. Clin Cancer Res. 2014;20:2984-93. PMID: 2469632. doi: 10.1158/1078-0432.CCR-13-3355
  18. Нестерова Е.С., Кравченко С.К., Мангасарова Я.К. и др. Фолликулярная лимфома. Высокодозная иммунохимиотерапия с трансплантацией аутологичных стволовых клеток крови: результаты первого проспективного исследования в России. Терапевтический архив. 2016;88(7):62-71 [Nesterova ES, Kravchenko SK, Mangasarova YaK, et al. Follicular lymphoma. High-dose immunochemotherapy with autologous blood stem cell transplantation: Results of the first prospective study in Russia. Therapeutic Archive. 2016;88(7):62-71 (In Russ.)]. doi: 10.17116/terarkh201688762-71
  19. Nesterova ES, Kravchenko SK, Baryakh EA. Autologous stem cell transplantation (AutoSCT) in first remission of follicular lymphoma (FL) “save“ patients (pts) with poor prognosis. results of the first Russian prospective study. Blood. 2015;126(23):5079. doi: 10.1182/blood.V126.23.5079.5079
  20. Nesterova ES, Kravchenko SK, Kovrigina AM, et al. Front-line high dose therapy with following autologous stem cell transplantation (ASCT) for follicular lymphoma patients. Blood. 2014;124(21):5908. doi: 10.1182/blood.V124.21.5908.5908
  21. Нестерова Е.С., Кравченко С.К., Гемджян Э.Г. и др. Итоги десятилетнего опыта лечения больных фолликулярной лимфомой. Гематология и трансфузиология. 2012;57(5):3-8 [Nesterova ES, Kravchenko SK, Gemdzhian EG, et al. The results of ten years’ experience treating patients with follicular lymphoma. Gematologiya i Transfuziologiya = Hematology and Transfusiology. 2012;57(5):3-8 (In Russ.)]. doi: 20.500.11925/257570
  22. Хоружик С.А., Жаврид Э.А., Сачивко Н.В. Новый алгоритм стадирования лимфомы на основе диффузионно-взвешенной магнитно-резонансной томографии всего тела. Вест. Нац. aкад. навук Беларусі. Сер. мед. навук. 2018;15(2):179-98 [Kharuzhyk SA, Zhavrid EA, Sachivko NV. New algorithm for lymphoma staging based on whole body diffusion-weighted magnetic resonance imaging. Proceedings of the National Academy of Sciences of Belarus. Medical series. 2018;15(2):179-98 (In Russ.)]. doi: 10.29235/1814-6023-2018-15-2-179-198
  23. Кравченко С.К., Нестерова Е.С. Алгоритмы диагностики и протоколы лечения заболеваний системы крови. Рандомизированное, контролируемое (сравнительное) открытое, проспективное исследование по оценке эффективности программ R-EPOCH-21, R-CHOP-21 и трансплантации аутологичных стволовых клеток крови у больных фолликулярной лимфомой из группы высокого риска. Под ред. В.Г. Савченко. В 2 т. Т. 2. М.: Практика, 2018; с. 497-530 [Kravchenko SK, Nesterova ES. Diagnostic algorithms and protocols for the treatment of blood system diseases. A randomized, controlled (comparative) open, prospective study evaluating the effectiveness of the R-EPOCH-21, R-CHOP-21 programs and transplantation of autologous blood stem cells in patients with high-risk follicular lymphoma. Ed. VG Savchenko. In two volumes. Volume 2. Moscow: Practice, 2018; p. 497-530 (In Russ.)].
  24. Кравченко С.К., Нестерова Е.С. Алгоритмы диагностики и протоколы лечения заболеваний системы крови. Проспективное многоцентровое исследование: комбинированная терапия первой линии препаратами бендамустин и ритуксимаб с последующей поддерживающей терапией ритуксимабом у больных фолликулярной лимфомой (протокол FL-RUS-2013). Под ред. В.Г. Савченко. В 2 т. Т. 2. М.: Практика, 2018. с. 101-31 [Kravchenko SK, Nesterova ES. Diagnostic algorithms and protocols for the treatment of diseases of the blood system. A prospective multicenter study: first-line combination therapy with bendamustine and rituximab followed by rituximab maintenance therapy in patients with follicular lymphoma (protocol FL-RUS-2013). VG Savchenko. In two volumes. Volume 2. Moscow: Practice, 2018; p. 101-31 (In Russ.)].
  25. Кравченко С.К., Нестерова Е.С., Барях Е.А. Сборник алгоритмов диагностики и протоколов лечения заболеваний системы крови. Протокол лечения фолликулярной лимфомы у больных из группы высокого риска. Под ред. В. Г. Савченко. ФГБУ «Гематологический науч. центр» Министерства здравоохранения России. М.: Практика, 2012; с. 595-618 [Kravchenko SK, Nesterova ES, Baryakh EA. Collection of diagnostic algorithms and protocols for the treatment of diseases of the blood system. Protocol for the treatment of follicular lymphoma in patients at high risk. Hematological Scientific Center of the Russian Ministry of Health. Ed. VG Savchenko. Moscow: Practice, 2012; p. 595-618 (In Russ.)].
  26. Weiler-Sagie M, Bushelev O, Epelbaum R. (18) F-FDG avidity in lymphoma readdressed: a study of 766 patients. J Nucl Med. 2010;51(1):25-30. doi: 10.2967/jnumed.109.067892
  27. Schoder H, Noy A, Gonen M. Intensity of 18fluorodeoxyglucose uptake in positron emission tomography distinguishes between indolent and aggressive non-Hodgkin’s lymphoma. J Clin Oncol. 2005;23(21):4643-51. doi: 10.1200/JCO.2005.12.072
  28. Nesterova ES, Yatsyk GA, Lutsik NS, et al. The Possibilities of Diffusion-Weighted Magnetic Resonance Imaging in Determining the Burden of a Tumor in Patients with Follicular Lymphoma. Blood. 2019;134(Suppl. 1):5264. doi: 10.1182/blood-2019-126502
  29. Wang D, Huo Y, Chen S. Whole-body MRI versus18F-FDG PET/CT for pretherapeutic assessment and staging of lymphoma: a meta-analysis. Onco Targets Ther. 2018 Jun 20;11:3597-608. doi: 10.2147/OTT.S148189
  30. Hynes JP, Hughes N, Cunningham P. Whole-body MRI of bone marrow: A review. J Magn Reson Imaging. 2019 Dec;50(6):1687-701. doi: 10.1002/jmri.26759
  31. Badawi RD, Shi H, Hu P. First Human Imaging Studies with the EXPLORER Total-Body PET Scanner. J Nucl Med. 2019 Mar;60(3):299-303. doi: 10.2967/jnumed.119.226498
  32. Swerdlow SH, Swerdlow S, Campo E, Harris N. WHO classification of tumours of haematopoietic and lymphoid tissues. World Health Organization 2017; Volume 2: Revised 4th edition.
  33. Balbo-Mussetto A, Cirillo S, Bruna R. Whole-body MRI with diffusion-weighted imaging: A valuable alternative to contrast-enhanced CT for initial staging of aggressive lymphoma. Clin Radiol. 2016;71:271-9. doi: 10016/j.ejrnm2017.06.002
  34. Adams HJ, Kwee TC, Vermoolen MA. Whole-body MRI for the detection of bone marrow involvement in lymphoma: prospective study in 116 patients and comparison with FDG-PET. Eur Radiol. 2013;23:2271-8. PMID: 23591618. doi: 10.1007/s00330-013-2835-9

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2020 Consilium Medicum

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
 
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies