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Whole body MRI with qualitative and quantitative analysis of DWI for assessment of bone marrow involvement in lymphoma

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Abstract

Aim

Our study aimed to investigate the role of qualitative and quantitative whole body MRI with DWI for assessment of bone marrow involvement (BMI) in newly diagnosed lymphoma using FDG PET–CT and bone marrow biopsy (BMB) as reference standard.

Materials and methods

We retrospectively evaluated 56 patients with newly diagnosed lymphoma (21 Hodgkin’s lymphoma and 35 non-Hodgkin’s lymphoma) who underwent random unilateral BMB, FDG PET–CT and Wb-MRI-DWI for initial staging. In a patient-based analysis, results of Wb-MRI-DWI were compared with FDG PET–CT and BMB. For quantitative analysis, mean ADC values of posterior iliac crest were correlated with BMI and bone marrow cellularity.

Results

WB-MR-DWI obtained excellent concordance with FDG PET–CT both in HL (k = 1.000; 95% CI 1.000–1.000) and in DLBCL (k = 1.000; 95% CI 1.000–1.000). In other NHL, WB-MRI-DWI obtained a good correlation with BMB (k = 0.611; 95% CI 0.295–0.927) while FDG PET–CT had poor concordance (k = 0.067; 95% CI 0.372–0.505). WB-MR-DWI has no false negative errors but 4 false positive results consisting in focal lesions consensually reported by FDG PET–CT and resolved after therapy. No significant correlation between ADC mean value and BMI was found (p = 0.0586).

Conclusion

Our data suggest that Wb-MRI-DWI is a valid technique for BMI assessment in lymphoma patients, thanks to its excellent concordance with FDG PET–CT and good concordance with BMB (superior than FDG PET–CT). If further investigations will confirm our results on larger patient groups, it could become a useful tool in the clinical workup.

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References

  1. Connors JM (2005) State-of-the-art therapeutics: Hodgkin’s Lymphoma. J Clin Oncol 23(26):6400–6408

    Article  CAS  PubMed  Google Scholar 

  2. Shankland KR, Armitage JO, Hancock BW (2012) Non-Hodgkin lymphoma. Lancet 380(9844):848–857. doi:10.1016/S0140-6736(12)60605-9

    Article  PubMed  Google Scholar 

  3. Armitage JO (2005) Staging non-Hodgkin lymphoma. CA Cancer J Clin 55(6):368–376

    Article  PubMed  Google Scholar 

  4. Hasenclever D, Diehl V (1998) A prognostic score for advanced Hodgkin’s disease. International prognostic factors project on advanced Hodgkin’s disease. N Engl J Med 339(21):1506–1514

    Article  CAS  PubMed  Google Scholar 

  5. (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. The International Non-Hodgkin’s Lymphoma Prognostic Factors Project. N Engl J Med 329(14):987–994

  6. Zhou Z, Sehn LH, Rademaker AW, Gordon LI, Lacasce AS, Crosby-Thompson A et al (2014) An enhanced International Prognostic Index (NCCN-IPI) for patients with Diffuse Large B-cell lymphoma treated in the rituximab era. Blood 123(6):837–842. doi:10.1182/blood-2013-09-524108

    Article  CAS  PubMed  Google Scholar 

  7. Solal-Celigny P, Roy P, Colombat P, White J, Armitage JO et al (2004) Follicular lymphoma international prognostic index. Blood 104(5):1258–1265

    Article  CAS  PubMed  Google Scholar 

  8. Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A, Vitolo U et al (2009) Follicular Lymphoma Prognostic Index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol 27(27):4555–4562. doi:10.1200/JCO.2008.21.3991

    Article  PubMed  Google Scholar 

  9. (1950) Biopsy bone-marrow. Br Med 1(4657):825–828

  10. Bain BJ (2003) Bone marrow biopsy and morbidity and mortality. Br J Haematol 121(6):949–951

    Article  PubMed  Google Scholar 

  11. Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ et al (2002) Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer 94(5):1522–1531

    Article  PubMed  Google Scholar 

  12. Weiler-Sagie M, Bushelev O, Epelbaum R, Dann EJ, Haim N, Avivi I et al (2010) (18)F-FDG avidity in lymphoma readdressed: a study of 766 patiens. J Nucl Med 51(1):25–30. doi:10.2967/jnumed.109.067892

    Article  PubMed  Google Scholar 

  13. Kwee TC, Kwee RM, Nievelstein RA (2008) Imaging in staging of malignant lymphoma: a systematic review. Blood 111:504–516

    Article  CAS  PubMed  Google Scholar 

  14. Brennan DD, Gleeson T, Coate LE, Cronin C, Carney D, Eustace SJ (2005) A comparison of whole-body MRI and CT for the staging of lymphoma. AJR Am J Roentgenol 185(3):711–716

    Article  CAS  PubMed  Google Scholar 

  15. Abdulqadhr G, Molin D, Astrom G, Suurkula M, Johansson L, Hagberg H, Ahlstrom H (2011) Whole-body diffusion-weighted imaging compared with FDG-PET/CT in staging of lymphoma patients. Acta Radiol 52:173–180. doi:10.1258/ar.2010.100246

    Article  PubMed  Google Scholar 

  16. Azzedine B, Kahina MB, Dimitri P, Christophe P, Alain D, Claude M (2015) Whole-body diffusion-weighted MRI for staging lymphoma at 3.0 T: comparative study with MR imaging at 1.5 T. Clin Imaging 39(1):104–119. doi:10.1016/j.clinimag.2014.06.017

    Article  PubMed  Google Scholar 

  17. Ferrari C, Minoia C, Asabella AN, Nicoletti A, Altini C, Antonica F et al (2014) Whole body magnetic resonance with diffusion weighted sequences with body signal suppression compared to (18)F-FDG PET/CT in newly diagnosed lymphoma. Hell J Nucl Med 17(Suppl 1):40–49

    PubMed  Google Scholar 

  18. Kwee TC, van Hufford HM, Beek FJ, Takahara T, Uiterwaal CS, Bierings MB et al (2009) Whole-body MRI, including diffusion-weighted imaging, for the initial staging of malignant lymphoma. Comparison to computed tomography. Invest Radiol 44:683–690. doi:10.1097/RLI.0b013e3181afbb36

    Article  PubMed  Google Scholar 

  19. Velasco S, Samuel B, Vincent D, Joelle G, Remy P, Francois GG et al (2013) Comparison of PET-CT and magnetic resonance diffusion weighted imaging with body suppression (DWIBS) for initial staging of malignant lymphomas. Eur J Radiol 82(11):211–217. doi:10.1016/j.ejrad.2013.05.042

    Google Scholar 

  20. Gu J, Chan T, Zhang J, Leung AY, Kwong YL, Khong PL (2011) Whole-body diffusion weighted imaging: the added value to whole body MRI at initial diagnosis of lymphoma. AJR 197:384–391. doi:10.2214/AJR.10.5692

    Article  Google Scholar 

  21. van Ufford HM, Kwee TC, Beek FJ, van Leeuwen MS, Takahara T, Fijnheer R et al (2011) Newly diagnosed lymphoma: initial results with whole body T1 weighted, STIR, and diffusion weighted MRI compared with 18F-FDG PET/CT. AJR 196:662–669. doi:10.2214/AJR.10.4743

    Article  PubMed  Google Scholar 

  22. Kwee TC, Vermoolen MA, Akkerman EA, Kersten MJ, Fijnheer R, Ludwig I, Beek FJ et al (2014) Whole-body MRI, including Diffusion Weighted Imaging, for staging lymphoma: comparison with CT in a prospectives multicenter study. J Magn Res Imaging 40(1):26–36. doi:10.1002/jmri.24356

    Article  Google Scholar 

  23. Mayerhoefer ME, Karanikas G, Kletter K, Prosch H, Kiesewetter B, Skrabs C et al (2014) Evaluation of diffusion-weighted MRI for pretherapeutic assessment and staging of lymphoma: results of a prospective study in 140 patients. Clin Cancer Res 20(11):2984–2993. doi:10.1158/1078-0432.CCR-13-3355

    Article  PubMed  Google Scholar 

  24. Balbo-Mussetto A, Cirillo S, Bruna R, Gueli A, Saviolo C, Petracchini M, Fornari A, Lario CV, Gottardi D, De Crescenzo A, Tarella C (2016) Whole-body MRI with diffusion-weighted imaging: a valuable alternative to contrast-enhanced CT for initial staging of aggressive lymphoma. Clin Radiol 71(3):271–279. doi:10.1016/j.crad.2015.11.018

    Article  CAS  PubMed  Google Scholar 

  25. Vande Berg BC, Lecouvet FE, Michaux L, Ferrant A, Maldague B, Malghem J (1998) Magnetic resonance imaging of the bone marrow in hematological malignancies. Eur Radiol 8:1335–1344

    Article  CAS  PubMed  Google Scholar 

  26. Adams H, Kwee TC, Vermoolen MA, de Kaizer B, de Klerk JM, Adam JA 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(8):2271–2278. doi:10.1007/s00330-013-2835-9

    Article  PubMed  Google Scholar 

  27. Mayerhoefer ME, Raderer M (2015) Diffusion-weighted MRI for Lymphoma staging—response. Clin Cancer Res 21:222–223. doi:10.1158/1078-0432.CCR-14-2617

    Article  PubMed  Google Scholar 

  28. Cheson BD, Fisher RJ, Barrington SF, Cavalli F, Schwartz LH, Zucca E, Lister TA (2014) Recommendations for initial evaluation, staging, and response assessment of Hodgkin and Non-Hodgkin Lymphoma: the Lugano Classification. J Clin Oncol 32(27):3059–3067. doi:10.1200/JCO.2013.54.8800

    Article  PubMed  PubMed Central  Google Scholar 

  29. Adams HJA, Nievelstein RAJ, Kwee TC (2015) Opportunities and limitations of bone marrow biopsy and bone marrow FDG-PET in lymphoma. Blood Rev 29(6):417–425. doi:10.1016/j.blre.2015.06.003

    Article  PubMed  Google Scholar 

  30. Adams HJ, Kwee TC, de Keizer B, Fijnheer R, de Klerk JM, Nievelstein RA (2014) FDG-PET/CT for detection of bone marrow involvement in diffuse large B–cell lymphoma: systematic review and meta-analysis. Eur J Nucl Mol Imaging 41(3):565–574

    Article  CAS  Google Scholar 

  31. Cohen J (1968) Weighed kappa: nominal scale agreement with provision for scaled disagreement or partial credit. Psychol Bull 70(4):213–220

    Article  CAS  PubMed  Google Scholar 

  32. Wu LM, Chen FY, Jiang XX, Gu HY, Yin Y, Xu JR (2012) 18F-FDG PET, combined FDG-PET/CT and MRI for evaluation of bone marrow infiltration in staging of lymphoma: a systematic review and meta-analysis. Eur Radiol 81(2):303–311. doi:10.1016/j.ejrad.2010.11.020

    Article  Google Scholar 

  33. Jiang XX, Yan ZX, Song YY, Zhao WL (2013) A pooled analysis of MRI in the detection of bone marrow infiltration in patients with malignant lymphoma. Clin Radiol 68:143–153. doi:10.1016/j.crad.2012.11.002

    Article  Google Scholar 

  34. Goncalves M, De Paula H, Linardi C, Cerci J, Aldred V, Siquera S, Buccheri S, Zerbini M (2015) Dealing with bone marrow biopsies in the staging of classical Hodgkin Lymphoma: an old issue revisited in the F-fluorodeoxyglucose-positron emission tomography era. Leuk Lymphoma 56(10):2883–2888. doi:10.3109/10428194.2015.1016928

    Article  CAS  Google Scholar 

  35. El-Galady TC, d’Amore F, Mylam KJ et al (2012) Routine bone marrow biopsy has little or no therapeutic consequence for positron emission tomography/computed tomography-staged treatment-naïve patients with Hodgkin lymphoma. J Clin Oncol 30:4508–4514. doi:10.1200/JCO.2012.42.4036

    Article  Google Scholar 

  36. Khan AB, Barrington SF, Mikhaeel NG et al (2013) PET-CT staging DLBCL accurately identifies and provides new insight into the clinical significance of bone marrow involvement. Blood 122:61–67. doi:10.1182/blood-2012-12-473389

    Article  CAS  PubMed  Google Scholar 

  37. Berthet L, Cochet A, Kanoun S et al (2013) In newly diagnosed diffuse large B-cell lymphoma, determination of bone marrow involvement of 18F-FDG PET/CT provides better diagnostic performance and prognostic stratification than does biopsy. J Nucl Med 54:1244–1250. doi:10.2967/jnumed.112.114710

    Article  CAS  PubMed  Google Scholar 

  38. Kwee TC, Ludwig I, Uiterwaal CS, van Ufford H, Vermoolen MA, Fijnheer R, Bierings MB, Nievelstein RA (2011) ADC measurements in the evaluation of lymph nodes in patients with non-Hodgkin lymphoma: feasibility study. MAGMA 24(1):1–8. doi:10.1007/s10334-010-0226-7

    Article  CAS  PubMed  Google Scholar 

  39. Cui FZ, Cui JL, Wang SL, Yu H, Sun YC, Zhao N, Cui SJ (2016) Signal characteristics of normal adult bone marrow in whole body diffusion weighted imaging. Acta Radiol 57(10):1230–1237. doi:10.1177/0284185115626477

    Article  PubMed  Google Scholar 

  40. Lavdas I, Rockal AG, Castelli F, Sandhu RS, Papadaki A, Honeyfield L, Waldman AD, Aboagye EO (2015) Apparent diffusion coefficient of normal abdominal organs and bone marrow from whole body DWI at 1.5 T: the effect of sex and age. AJR 205(2):242–250. doi:10.2214/AJR.14.13964

    Article  PubMed  Google Scholar 

  41. Nonomura Y, Yasumoto M, Yoshimura R, Haraguchi K, Ito S, Akashi T, Ohashi I (2001) Relationship between bone marrow cellularity and apparent diffusion coefficient. J Magn Reson Imaging 13(5):757–760

    Article  CAS  PubMed  Google Scholar 

  42. 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(4):1082–1089. doi:10.1002/jmri.25439

    Article  PubMed  Google Scholar 

  43. Albano D, La Grutta L, Grassedonio E, Patti C, Lagalla R, Midiri M, Galia M (2016) Pitfalls in whole body MRI with diffusion weighted imaging performed on patients with lymphoma: what radiologists should know. Magn Reson Imaging 34(7):922–931. doi:10.1016/j.mri.2016.04.023

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Fondazione Scientifica Mauriziana ONLUS for the support.

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Author notes

  1. Corrado Tarella

    Present address: Hemato-oncology Division, European Institute of Oncology, Milan, Italy

Authors and Affiliations

  1. Radiology Department, Mauriziano-Umberto I Hospital, Turin, Italy

    Annalisa Balbo-Mussetto, Chiara Saviolo, Alberto Fornari, Massimo Petracchini, Annalisa Macera, Chiara Valentina Lario, Teresa Gallo & Stefano Cirillo

  2. Hematology and Cell Therapy Division, Mauriziano-Umberto I Hospital and University, Turin, Italy

    Daniela Gottardi & Corrado Tarella

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  1. Annalisa Balbo-Mussetto
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Correspondence to Annalisa Balbo-Mussetto.

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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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Balbo-Mussetto, A., Saviolo, C., Fornari, A. et al. Whole body MRI with qualitative and quantitative analysis of DWI for assessment of bone marrow involvement in lymphoma. Radiol med 122, 623–632 (2017). https://doi.org/10.1007/s11547-017-0762-6

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