Skip to main content
Top
Published in: European Radiology 3/2018

01-03-2018 | Oncology

Whole body magnetic resonance in indolent lymphomas under watchful waiting: The time is now

Authors: Massimo Galia, Domenico Albano, Corrado Tarella, Caterina Patti, Luca Maria Sconfienza, Antonino Mulè, Pierpaolo Alongi, Massimo Midiri, Roberto Lagalla

Published in: European Radiology | Issue 3/2018

Login to get access

Abstract

The indolent non-Hodgkin lymphomas (i-NHLs) are characterised by ‘indolent’ clinical behaviour with slow growth and prolonged natural history. The watchful waiting (WW) strategy is a frequently employed treatment option in these patients. This implies a strict monitoring by imaging examinations, including 18F-fluorodeoxyglucose-positron emission tomography/computed tomography (18F-FDG-PET/CT) and CT. A major concern is radiation exposure due to regularly monitoring by conventional imaging procedures. Several studies have demonstrated the reliability of whole-body magnetic resonance imaging (WB-MRI) for lymphoma staging. WB-MRI could be useful for active surveillance in i-NHLs providing the suspect of disease progression that can be then confirmed by additional diagnostic procedures, including 18F-FDG-PET/CT. The directive 2013/59 by the European Union claims that if a radiation-free imaging technique allows obtaining the same diagnostic results, it should be invariably used. In this setting, WB-MRI may be considered a reasonable option in i-NHLs under WW, replacing imaging modalities that cause exposure to ionising radiations. This will help to reduce the cancer risk in i-NHL patients for whom chemo-/radiotherapy remain the usual treatment options following the usually long WW phase. The scientific community should raise the awareness of the risk of ionising radiations in i-NHLs and the emphasise the need for establishing the proper place of WB-MRI in lymphoma imaging.

Key Points

Watchful waiting is a reasonable option in patients with indolent non-Hodgkin lymphomas.
Imaging is crucial to monitor patients with indolent non-Hodgkin lymphomas.
CT and 18 F-FDG-PET/CT are commonly used, implying a substantial radiation exposure.
WB-MRI is highly reliable in lymphoma staging.
WB-MRI may be considered to monitor indolent non-Hodgkin lymphomas under watchful waiting.
Literature
2.
go back to reference Armitage JO, Longo DL (2016) Is watch and wait still acceptable for patients with low-grade follicular lymphoma? Blood 127:2804–2808CrossRefPubMed Armitage JO, Longo DL (2016) Is watch and wait still acceptable for patients with low-grade follicular lymphoma? Blood 127:2804–2808CrossRefPubMed
3.
go back to reference Sorigue M, Sancho JM, Ribera JM (2016) Open questions in watchful waiting for follicular lymphoma. Br J Haematol (in press) Sorigue M, Sancho JM, Ribera JM (2016) Open questions in watchful waiting for follicular lymphoma. Br J Haematol (in press)
4.
go back to reference Zinzani PL, Marchetti M, Billio A et al (2013) Expert Panel of the Italian Society of Hematology. SIE, SIES, GITMO revised guidelines for the management of follicular lymphoma. Am J Hematol 88:185–192CrossRefPubMed Zinzani PL, Marchetti M, Billio A et al (2013) Expert Panel of the Italian Society of Hematology. SIE, SIES, GITMO revised guidelines for the management of follicular lymphoma. Am J Hematol 88:185–192CrossRefPubMed
5.
go back to reference Tarella C, Arcaini L, Baldini L et al (2015) Italian Society of Hematology, Italian Society of Experimental Hematology, and Italian Group for Bone Marrow Transplantation guidelines for the management of indolent, nonfollicular B-cell lymphoma (marginal zone, lymphoplasmacytic, and small lymphocytic lymphoma). Clin Lymphoma Myeloma Leuk 15:75–85CrossRefPubMed Tarella C, Arcaini L, Baldini L et al (2015) Italian Society of Hematology, Italian Society of Experimental Hematology, and Italian Group for Bone Marrow Transplantation guidelines for the management of indolent, nonfollicular B-cell lymphoma (marginal zone, lymphoplasmacytic, and small lymphocytic lymphoma). Clin Lymphoma Myeloma Leuk 15:75–85CrossRefPubMed
6.
go back to reference Arcaini L, Lazzarino M, Colombo N et al (2006) Splenic marginal zone lymphoma: a prognostic model for clinical use. Blood 107:4643–4649CrossRefPubMed Arcaini L, Lazzarino M, Colombo N et al (2006) Splenic marginal zone lymphoma: a prognostic model for clinical use. Blood 107:4643–4649CrossRefPubMed
7.
go back to reference Matutes E, Oscier D, Montalban C et al (2008) Splenic marginal zone lymphoma proposals for a revision of diagnostic, staging and therapeutic criteria. Leukemia 22:487–495CrossRefPubMed Matutes E, Oscier D, Montalban C et al (2008) Splenic marginal zone lymphoma proposals for a revision of diagnostic, staging and therapeutic criteria. Leukemia 22:487–495CrossRefPubMed
8.
go back to reference Raderer M, Kiesewetter B, Ferreri AJ (2016) Clinicopathologic characteristics and treatment of marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). CA Cancer J Clin 66:153–171CrossRefPubMed Raderer M, Kiesewetter B, Ferreri AJ (2016) Clinicopathologic characteristics and treatment of marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). CA Cancer J Clin 66:153–171CrossRefPubMed
9.
go back to reference Tanimoto K, Kaneko A, Suzuki S et al (2006) Long-term follow-up results of no initial therapy for ocular adnexal MALT lymphoma. Ann Oncol 17:135–140CrossRefPubMed Tanimoto K, Kaneko A, Suzuki S et al (2006) Long-term follow-up results of no initial therapy for ocular adnexal MALT lymphoma. Ann Oncol 17:135–140CrossRefPubMed
10.
go back to reference Troch M, Streubel B, Petkov V, Turetschek K, Chott A, Raderer M (2007) Does MALT lymphoma of the lung require immediate treatment? An analysis of 11 untreated cases with long-term follow-up. Anticancer Res 27:3633–3637PubMed Troch M, Streubel B, Petkov V, Turetschek K, Chott A, Raderer M (2007) Does MALT lymphoma of the lung require immediate treatment? An analysis of 11 untreated cases with long-term follow-up. Anticancer Res 27:3633–3637PubMed
11.
go back to reference Ardeshna KM, Smith P, Norton A et al (2003) Long-term effect of a watch and wait policy versus immediate systemic treatment for asymptomatic advanced-stage non-Hodgkin lymphoma: a randomised controlled trial. Lancet 362:516–522CrossRefPubMed Ardeshna KM, Smith P, Norton A et al (2003) Long-term effect of a watch and wait policy versus immediate systemic treatment for asymptomatic advanced-stage non-Hodgkin lymphoma: a randomised controlled trial. Lancet 362:516–522CrossRefPubMed
12.
go back to reference Tadmor T, Polliack A (2012) Optimal management of older patients with chronic lymphocytic leukemia: some facts and principles guiding therapeutic choices. Blood Rev 26:15–23CrossRefPubMed Tadmor T, Polliack A (2012) Optimal management of older patients with chronic lymphocytic leukemia: some facts and principles guiding therapeutic choices. Blood Rev 26:15–23CrossRefPubMed
13.
go back to reference Martin P, Chadburn A, Christos P et al (2009) Outcome of deferred initial therapy in mantle-cell lymphoma. J Clin Oncol 27:1209–1213CrossRefPubMed Martin P, Chadburn A, Christos P et al (2009) Outcome of deferred initial therapy in mantle-cell lymphoma. J Clin Oncol 27:1209–1213CrossRefPubMed
14.
go back to reference Dreyling M, Ferrero S, Hermine O (2014) How to manage mantle cell lymphoma. Leukemia 28:2117–2130CrossRefPubMed Dreyling M, Ferrero S, Hermine O (2014) How to manage mantle cell lymphoma. Leukemia 28:2117–2130CrossRefPubMed
15.
go back to reference Cheson BD, Fisher RI, Barrington SF et al (2014) Recommendations for initial evaluation, staging and response assessment of Hodgkin and non-Hodgkin lymphoma: the lugano classification. J Clin Oncol 32:3059–3067CrossRefPubMedPubMedCentral Cheson BD, Fisher RI, Barrington SF et al (2014) Recommendations for initial evaluation, staging and response assessment of Hodgkin and non-Hodgkin lymphoma: the lugano classification. J Clin Oncol 32:3059–3067CrossRefPubMedPubMedCentral
16.
go back to reference Cheson BD, Ansell S, Schwartz L et al (2016) Refinement of the Lugano classification response criteria for lymphoma in the era of immunomodulatory therapy. Blood 128:2489–2496CrossRefPubMed Cheson BD, Ansell S, Schwartz L et al (2016) Refinement of the Lugano classification response criteria for lymphoma in the era of immunomodulatory therapy. Blood 128:2489–2496CrossRefPubMed
17.
go back to reference Brenner DJ, Hall EJ (2007) Computed tomography: an increasing source of radiation exposure. N Engl J Med 357:2277–2284CrossRefPubMed Brenner DJ, Hall EJ (2007) Computed tomography: an increasing source of radiation exposure. N Engl J Med 357:2277–2284CrossRefPubMed
18.
go back to reference Shenoy P, Sinha R, Tumeh JW, Lechowicz MJ, Flowers CR (2010) Surveillance computed tomography scans for patients with lymphoma: is the risk worth the benefits? Clin. Lymphoma Myeloma Leuk 10:270–277CrossRef Shenoy P, Sinha R, Tumeh JW, Lechowicz MJ, Flowers CR (2010) Surveillance computed tomography scans for patients with lymphoma: is the risk worth the benefits? Clin. Lymphoma Myeloma Leuk 10:270–277CrossRef
19.
go back to reference Chien SH, Liu CJ, Hu YW et al (2015) Frequency of surveillance computed tomography in non-Hodgkin lymphoma and the risk of secondary primary malignancies: a nationwide population-based study. Int J Cancer 137:658–665CrossRefPubMed Chien SH, Liu CJ, Hu YW et al (2015) Frequency of surveillance computed tomography in non-Hodgkin lymphoma and the risk of secondary primary malignancies: a nationwide population-based study. Int J Cancer 137:658–665CrossRefPubMed
20.
go back to reference Huang B, Law MW, Khong PL (2009) Whole-body PET/CT scanning: estimation ofradiation dose and cancer risk. Radiology 251:166–174CrossRefPubMed Huang B, Law MW, Khong PL (2009) Whole-body PET/CT scanning: estimation ofradiation dose and cancer risk. Radiology 251:166–174CrossRefPubMed
21.
go back to reference Luminari S, Biasoli I, Arcaini L et al (2013) The use of FDG-PET in the initial staging of 142 patients with follicular lymphoma: a retrospective study from the FOLL05 randomized trial of the Fondazione Italiana Linfomi. Ann Oncol 24:2108–2112CrossRefPubMed Luminari S, Biasoli I, Arcaini L et al (2013) The use of FDG-PET in the initial staging of 142 patients with follicular lymphoma: a retrospective study from the FOLL05 randomized trial of the Fondazione Italiana Linfomi. Ann Oncol 24:2108–2112CrossRefPubMed
24.
go back to reference Albano D, Patti C, La Grutta L et al (2016) Comparison between whole-body MRI with diffusion-weighted imaging and PET/CT in staging newly diagnosed FDG-avid lymphomas. Eur J Radiol 85:313–318CrossRefPubMed Albano D, Patti C, La Grutta L et al (2016) Comparison between whole-body MRI with diffusion-weighted imaging and PET/CT in staging newly diagnosed FDG-avid lymphomas. Eur J Radiol 85:313–318CrossRefPubMed
25.
go back to reference Mayerhoefer ME, Karanikas G, Kletter K et al (2015) Evaluation of diffusion-weighted magnetic resonance imaging for follow-up and treatment response assessment of lymphoma: results of an 18F-FDG-PET/CT–controlled prospective study in 64 patients. Clin Cancer Res 21:2506–2513CrossRefPubMed Mayerhoefer ME, Karanikas G, Kletter K et al (2015) Evaluation of diffusion-weighted magnetic resonance imaging for follow-up and treatment response assessment of lymphoma: results of an 18F-FDG-PET/CT–controlled prospective study in 64 patients. Clin Cancer Res 21:2506–2513CrossRefPubMed
26.
go back to reference Lin C, Luciani A, Itti E et al (2010) Whole-body diffusion-weighted magnetic resonance imaging with apparent diffusion coefficient mapping for staging patients with diffuse large B-cell lymphoma. Eur Radiol 20:2027–2038CrossRefPubMed Lin C, Luciani A, Itti E et al (2010) Whole-body diffusion-weighted magnetic resonance imaging with apparent diffusion coefficient mapping for staging patients with diffuse large B-cell lymphoma. Eur Radiol 20:2027–2038CrossRefPubMed
27.
go back to reference Littooij AS, Kwee TC, Barber I et al (2014) Whole-body MRI for initial staging of paediatric lymphoma: prospective comparison to an FDG-PET/CT-based reference standard. Eur Radiol 24:1153–1165CrossRefPubMed Littooij AS, Kwee TC, Barber I et al (2014) Whole-body MRI for initial staging of paediatric lymphoma: prospective comparison to an FDG-PET/CT-based reference standard. Eur Radiol 24:1153–1165CrossRefPubMed
28.
go back to reference Albano D, La Grutta L, Grassedonio E et al (2016) Pitfalls in whole body MRI with diffusion weighted imaging performed on patients with lymphoma: what radiologists should know. Magn Reson Imaging 34:922–931CrossRefPubMed Albano D, La Grutta L, Grassedonio E et al (2016) Pitfalls in whole body MRI with diffusion weighted imaging performed on patients with lymphoma: what radiologists should know. Magn Reson Imaging 34:922–931CrossRefPubMed
29.
go back to reference King AD, Ahuja AT, Yeung DK et al (2007) Malignant cervical lymphadenopathy: Diagnostic accuracy of diffusion-weighted MR imaging. Radiology 245:806–813CrossRefPubMed King AD, Ahuja AT, Yeung DK et al (2007) Malignant cervical lymphadenopathy: Diagnostic accuracy of diffusion-weighted MR imaging. Radiology 245:806–813CrossRefPubMed
30.
go back to reference Kwee TC, Vermoolen MA, Akkerman EA et al (2013) Whole-body MRI, including diffusion-weighted imaging, for staging lymphoma: Comparison with CT in a prospective multicenter study. J Magn Reson Imaging 40:26–36CrossRefPubMed Kwee TC, Vermoolen MA, Akkerman EA et al (2013) Whole-body MRI, including diffusion-weighted imaging, for staging lymphoma: Comparison with CT in a prospective multicenter study. J Magn Reson Imaging 40:26–36CrossRefPubMed
31.
go back to reference Balbo-Mussetto A, Cirillo S, Bruna R et al (2016) Whole-body MRI with diffusion-weighted imaging: A valuable alternative to contrast-enhanced CT for initial staging of aggressive lymphoma. Clinical Radiology 71:271–279CrossRefPubMed Balbo-Mussetto A, Cirillo S, Bruna R et al (2016) Whole-body MRI with diffusion-weighted imaging: A valuable alternative to contrast-enhanced CT for initial staging of aggressive lymphoma. Clinical Radiology 71:271–279CrossRefPubMed
32.
go back to reference Adams HJ, Kwee TC, Vermoolen MA et al (2013) Whole-body MRI for the detection of bone marrow involvement in lymphoma: prospective study in 116 patients and comparison with FDG-PET. Eur Radiol 23:2271–2278CrossRefPubMed Adams HJ, Kwee TC, Vermoolen MA et al (2013) Whole-body MRI for the detection of bone marrow involvement in lymphoma: prospective study in 116 patients and comparison with FDG-PET. Eur Radiol 23:2271–2278CrossRefPubMed
33.
go back to reference Albano D, Patti C, Lagalla R, Midiri M, Galia M (2017) Whole-body MRI, FDG-PET/CT, and bone marrow biopsy, for the assessment of bone marrow involvement in patients with newly diagnosed lymphoma. J Magn Reson Imaging 45:1082–1089CrossRefPubMed Albano D, Patti C, Lagalla R, Midiri M, Galia M (2017) Whole-body MRI, FDG-PET/CT, and bone marrow biopsy, for the assessment of bone marrow involvement in patients with newly diagnosed lymphoma. J Magn Reson Imaging 45:1082–1089CrossRefPubMed
34.
35.
go back to reference Vose JM (2015) Mantle cell lymphoma: 2015 update on diagnosis, risk stratification, and clinical management. Am J Hematol 90:739–745CrossRefPubMed Vose JM (2015) Mantle cell lymphoma: 2015 update on diagnosis, risk stratification, and clinical management. Am J Hematol 90:739–745CrossRefPubMed
37.
go back to reference Albano D, Patti C, La Grutta L et al (2017) Osteonecrosis detected by whole body magnetic resonance in patients with Hodgkin lymphoma treated by BEACOPP. Eur Radiol 27:2129–2136CrossRefPubMed Albano D, Patti C, La Grutta L et al (2017) Osteonecrosis detected by whole body magnetic resonance in patients with Hodgkin lymphoma treated by BEACOPP. Eur Radiol 27:2129–2136CrossRefPubMed
38.
go back to reference Littooij AS, Kwee TC, Goya E et al (2017) Whole-body MRI reveals high incidence of osteonecrosis in children treated for Hodgkin lymphoma. Br J Haematol 176:637–642CrossRefPubMed Littooij AS, Kwee TC, Goya E et al (2017) Whole-body MRI reveals high incidence of osteonecrosis in children treated for Hodgkin lymphoma. Br J Haematol 176:637–642CrossRefPubMed
39.
go back to reference Albano D, Patti C, Sconfienza LM, Galia M (2017) Whole-body MRI in the early detection of multifocal osteonecrosis. Br J Radiol 190:20170240CrossRef Albano D, Patti C, Sconfienza LM, Galia M (2017) Whole-body MRI in the early detection of multifocal osteonecrosis. Br J Radiol 190:20170240CrossRef
40.
go back to reference Messina C, Banfi G, Aliprandi A et al (2016) Ultrasound guidance to perform intra-articular injection of gadolinium-based contrast material for magnetic resonance arthrography as an alternative to fluoroscopy: the time is now. Eur Radiol 26:1221–1225CrossRefPubMed Messina C, Banfi G, Aliprandi A et al (2016) Ultrasound guidance to perform intra-articular injection of gadolinium-based contrast material for magnetic resonance arthrography as an alternative to fluoroscopy: the time is now. Eur Radiol 26:1221–1225CrossRefPubMed
41.
go back to reference Wu X, Sikiö M, Pertovaara H et al (2016) Differentiation of diffuse large B-cell lymphoma from follicular lymphoma using texture analysis on conventional MR images at 3.0 Tesla. Acad Radiol 23:696–703CrossRefPubMed Wu X, Sikiö M, Pertovaara H et al (2016) Differentiation of diffuse large B-cell lymphoma from follicular lymphoma using texture analysis on conventional MR images at 3.0 Tesla. Acad Radiol 23:696–703CrossRefPubMed
Metadata
Title
Whole body magnetic resonance in indolent lymphomas under watchful waiting: The time is now
Authors
Massimo Galia
Domenico Albano
Corrado Tarella
Caterina Patti
Luca Maria Sconfienza
Antonino Mulè
Pierpaolo Alongi
Massimo Midiri
Roberto Lagalla
Publication date
01-03-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 3/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-5071-x

Other articles of this Issue 3/2018

European Radiology 3/2018 Go to the issue