Diffuse Marrow Changes

ABSTRACT

Magnetic resonance imaging (MRI) to date remains the only imaging modality allowing direct visualization of the bone marrow compartment, in general having high sensitivity for bone marrow abnormalities. However, signal intensity changes in many different diseases presented with diffuse bone marrow infiltration show more overlap than difference, resulting in poor specificity. Therefore, MRI cannot be applied for initial diagnostic purposes in most diseases but should be reserved for staging, monitoring of therapy, and detection of disease recurrence after treatment. Diffuse infiltrative disease occurring at the hematopoietically active bone marrow, the vertebrae, pelvis, and femora should be areas included in imaging studies at a minimum if whole-body imaging cannot be applied.

In this article, in-depth information is provided on selected topics, including Gaucher's disease, Hodgkin's disease and non-Hodgkin's lymphoma, chronic lymphocytic leukemia, and changes in bone marrow after different medication strategies, with overviews of the field provided by multiple recent papers in the literature.

KEYWORDS

Magnetic resonance imaging - bone marrow - musculoskeletal - imaging

REFERENCES

• 1 Nöbauer I, Uffmann M. Differential diagnosis of focal and diffuse neoplastic diseases of bone marrow in MRI.  Eur J Radiol. 2005;  55(1) 2-32
• 2 Tall M A, Thompson A K, Vertinsky T, Palka P S. MR imaging of the spinal bone marrow.  Magn Reson Imaging Clin N Am. 2007;  15(2) 175-198 , vi
• 3 Alyas F, Saifuddin A, Connell D. MR imaging evaluation of the bone marrow and marrow infiltrative disorders of the lumbar spine.  Magn Reson Imaging Clin N Am. 2007;  15(2) 199-219 , vi
• 4 Cox T M, Aerts J M, Belmatoug N et al.. Management of non-neuronopathic Gaucher disease with special reference to pregnancy, splenectomy, bisphosphonate therapy, use of biomarkers and bone disease monitoring.  J Inherit Metab Dis. 2008;  31(3) 319-336
• 5 Rosenthal D I, Scott J A, Barranger J et al.. Evaluation of Gaucher disease using magnetic-resonance-imaging.  J Bone Joint Surg Am. 1986;  68(6) 802-808
• 6 Lanir A, Hadar H, Cohen I et al.. Gaucher disease: assessment with MR imaging.  Radiology. 1986;  161(1) 239-244
• 7 Hermann G, Shapiro R, Abdelwahab I, Grabowski G. MR imaging in adults with Gaucher disease type I: evaluation of marrow involvement and disease activity.  Skeletal Radiol. 1993;  22(4) 247-251
• 8 Terk M R, Esplin J, Lee K, Magre G, Colletti P M. MR imaging of patients with type 1 Gaucher's disease: relationship between bone and visceral changes.  AJR Am J Roentgenol. 1995;  165(3) 599-604
• 9 Cremin B J, Davey H, Goldblatt J. Skeletal complications of type I Gaucher disease: the magnetic resonance features.  Clin Radiol. 1990;  41(4) 244-247
• 10 Hermann G, Goldblatt J, Levy R et al.. Gaucher's disease type 1: assessment of bone involvement by CT and scintigraphy.  AJR Am J Roentgenol. 1986;  147(5) 943-948
• 11 Rosenthal D I, Barton N W, McKusick K A et al.. Quantitative imaging of Gaucher disease.  Radiology. 1992;  185(3) 841-845
• 12 Maas M, Hangartner T, Mariani G et al.. Recommendations for the assessment and monitoring of skeletal manifestations in children with Gaucher disease.  Skeletal Radiol. 2008;  37(3) 185-188
• 13 Vom Dahl S, Poll L, Di Rocco M et al.. Evidence-based recommendations for monitoring bone disease and the response to enzyme replacement therapy in Gaucher patients.  Curr Med Res Opin. 2006;  22(6) 1045-1064
• 14 Johnson L A, Hoppel B E, Gerard E L et al.. Quantitative chemical shift imaging of vertebral bone marrow in patients with Gaucher disease.  Radiology. 1992;  182(2) 451-455
• 15 Dixon W T. Simple proton spectroscopic imaging.  Radiology. 1984;  153(1) 189-194
• 16 Hollak C, Maas M, Akkerman E, den Heeten A, Aerts H. Dixon quantitative chemical shift imaging is a sensitive tool for the evaluation of bone marrow responses to individualized doses of enzyme supplementation therapy in type 1 Gaucher disease.  Blood Cells Mol Dis. 2001;  27(6) 1005-1012
• 17 Rosenthal D I, Doppelt S H, Mankin H J et al.. Enzyme replacement therapy for Gaucher disease: skeletal responses to macrophage-targeted glucocerebrosidase.  Pediatrics. 1995;  96(4 Pt 1) 629-637
• 18 Maas M, Poll L, Terk M. Imaging and quantifying skeletal involvement in Gaucher disease.  Br J Radiol. 2002;  75(suppl) A13-A24
• 19 Maas M, Akkerman E, Venema H, Stoker J, Den Heeten G. Dixon quantitative chemical shift MRI for bone marrow evaluation in the lumbar spine: a reproducibility study in healthy volunteers.  J Comput Assist Tomogr. 2001;  25(5) 691-697
• 20 Poll L W, Koch J A, vom Dahl S et al.. Magnetic resonance imaging of bone marrow changes in Gaucher disease during enzyme replacement therapy: first German long-term results.  Skeletal Radiol. 2001;  30(9) 496-503
• 21 Terk M R, Dardashti S, Liebman H A. Bone marrow response in treated patients with Gaucher disease: evaluation by T1-weighted magnetic resonance images and correlation with reduction in liver and spleen volume.  Skeletal Radiol. 2000;  29(10) 563-571
• 22 Maas M, van Kuijk C, Stoker J et al.. Quantification of bone involvement in Gaucher disease: MR imaging bone marrow burden score as an alternative to Dixon quantitative chemical shift MR imaging—initial experience.  Radiology. 2003;  229(2) 554-561
• 23 de Fost M, Hollak C, Groener J et al.. Superior effects of high-dose enzyme replacement therapy in type 1 Gaucher disease on bone marrow involvement and chitotriosidase levels: a 2-center retrospective analysis.  Blood. 2006;  108(3) 830-835
• 24 Robertson P L, Maas M, Goldblatt J. Semiquantitative assessment of skeletal response to enzyme replacement therapy for Gaucher's disease using the bone marrow burden score.  AJR Am J Roentgenol. 2007;  188(6) 1521-1528
• 25 DeMayo R F, Haims A H, McRae M C, Yang R, Mistry P K. Correlation of MRI-based bone marrow burden score with genotype and spleen status in Gaucher's disease.  AJR Am J Roentgenol. 2008;  191(1) 115-123
• 26 Kwee T C, Kwee R M, Verdonck L F, Bierings M B, Nievelstein R A. Magnetic resonance imaging for the detection of bone marrow involvement in malignant lymphoma.  Br J Haematol. 2008;  141(1) 60-68
• 27 Pelosi E, Penna D, Deandreis D et al.. FDG-PET in the detection of bone marrow disease in Hodgkin's disease and aggressive non-Hodgkin's lymphoma and its impact on clinical management.  Q J Nucl Med Mol Imaging. 2008;  52(1) 9-16
• 28 Tamburrini O, Cova M A, Console D, Martingano P. The evolving role of MRI in oncohaematological disorders.  Radiol Med. 2007;  112(5) 703-721
• 29 Tsunoda S, Takagi S, Tanaka O, Miura Y. Clinical and prognostic significance of femoral marrow magnetic resonance imaging in patients with malignant lymphoma.  Blood. 1997;  89(1) 286-290
• 30 Varan A, Cila A, Büyükpamukçu M. Prognostic importance of magnetic resonance imaging in bone marrow involvement of Hodgkin disease.  Med Pediatr Oncol. 1999;  32(4) 267-271
• 31 Yasumoto M, Nonomura Y, Yoshimura R et al.. MR detection of iliac bone marrow involvement by malignant lymphoma with various MR sequences including diffusion-weighted echo-planar imaging.  Skeletal Radiol. 2002;  31(5) 263-269
• 32 Baur A, Dietrich O, Reiser M. Diffusion-weighted imaging of bone marrow: current status.  Eur Radiol. 2003;  13(7) 1699-1708
• 33 Rahmouni A, Montazel J, Divine M et al.. Bone marrow with diffuse tumor infiltration in patients with lymphoproliferative diseases: dynamic gadolinium-enhanced MR imaging.  Radiology. 2003;  229(3) 710-717
• 34 Daldrup-Link H E, Rummeny E J, Ihssen B, Kienast J, Link T M. Iron-oxide-enhanced MR imaging of bone marrow in patients with non-Hodgkin's lymphoma: differentiation between tumor infiltration and hypercellular bone marrow.  Eur Radiol. 2002;  12(6) 1557-1566
• 35 Metz S, Lohr S, Settles M et al.. Ferumoxtran-10-enhanced MR imaging of the bone marrow before and after conditioning therapy in patients with non-Hodgkin lymphomas.  Eur Radiol. 2006;  16(3) 598-607
• 36 Elstrom R, Guan L, Baker G et al.. Utility of FDG-PET scanning in lymphoma by WHO classification.  Blood. 2003;  101(10) 3875-3876
• 37 Pakos E E, Fotopoulos A D, Ioannidis J P. 18F-FDG PET for evaluation of bone marrow infiltration in staging of lymphoma: a meta-analysis.  J Nucl Med. 2005;  46(6) 958-963
• 38 Karam M, Novak L, Cyriac J et al.. Role of fluorine-18 fluoro-deoxyglucose positron emission tomography scan in the evaluation and follow-up of patients with low-grade lymphomas.  Cancer. 2006;  107(1) 175-183
• 39 Jerusalem G, Beguin Y, Najjar F et al.. Positron emission tomography (PET) with 18F-fluorodeoxyglucose (18F-FDG) for the staging of low-grade non-Hodgkin's lymphoma (NHL).  Ann Oncol. 2001;  12(6) 825-830
• 40 Agool A, Schot B, Jager P, Vellenga E. 18F-FLT PET in hematologic disorders: a novel technique to analyze the bone marrow compartment.  J Nucl Med. 2006;  47(10) 1592-1598
• 41 Kwee T C, Kwee R M, Nievelstein R A. Imaging in staging of malignant lymphoma: a systematic review.  Blood. 2008;  111(2) 504-516
• 42 Ribrag V, Vanel D, Leboulleux S et al.. Prospective study of bone marrow infiltration in aggressive lymphoma by three independent methods: whole-body MRI, PET/CT and bone marrow biopsy.  Eur J Radiol. 2008;  66(2) 325-331
• 43 Xie Y, Davies S, Xiang Y, Robison L, Ross J. Trends in leukemia incidence and survival in the United States (1973–1998).  Cancer. 2003;  97(9) 2229-2235
• 44 Vande Berg B C, Lecouvet F E, Michaux L, Ferrant A, Maldague B, Malghem J. Magnetic resonance imaging of the bone marrow in hematological malignancies.  Eur Radiol. 1998;  8(8) 1335-1344
• 45 Lecouvet F E, Vande Berg B C, Michaux L et al.. Early chronic lymphocytic leukemia: prognostic value of quantitative bone marrow MR imaging findings and correlation with hematologic variables.  Radiology. 1997;  204(3) 813-818
• 46 Lecouvet F E, Vande Berg B C, Michaux L et al.. Chronic lymphocytic leukemia: changes in bone marrow composition and distribution assessed with quantitative MRI.  J Magn Reson Imaging. 1998;  8(3) 733-739
• 47 Ballon D, Dyke J, Schwartz L et al.. Bone marrow segmentation in leukemia using diffusion and T (2) weighted echo planar magnetic resonance imaging.  NMR Biomed. 2000;  13(6) 321-328
• 48 Vande Berg B C, Malghem J, Lecouvet F E et al.. Fat conversion of femoral marrow in glucocorticoid-treated patients: a cross-sectional and longitudinal study with magnetic resonance imaging.  Arthritis Rheum. 1999;  42(7) 1405-1411
• 49 Daldrup-Link H E, Henning T, Link T M. MR imaging of therapy-induced changes of bone marrow.  Eur Radiol. 2007;  17(3) 743-761
• 50 Roebuck D J. Skeletal complications in pediatric oncology patients.  Radiographics. 1999;  19(4) 873-885
• 51 Saini A, Saifuddin A. MRI of osteonecrosis.  Clin Radiol. 2004;  59(12) 1079-1093
• 52 Islam A, Catovsky D, Galton D. Histological study of bone marrow regeneration following chemotherapy for acute myeloid leukaemia and chronic granulocytic leukaemia in blast transformation.  Br J Haematol. 1980;  45(4) 535-540
• 53 Moulopoulos L A, Dimopoulos M A, Alexanian R, Leeds N E, Libshitz H I. Multiple myeloma: MR patterns of response to treatment.  Radiology. 1994;  193(2) 441-446
• 54 Salmon S E, Smith B A. Immunoglobulin synthesis and total body tumor cell number in IgG multiple myeloma.  J Clin Invest. 1970;  49(6) 1114-1121
• 55 Rahmouni A, Divine M, Mathieu D et al.. MR appearance of multiple myeloma of the spine before and after treatment.  AJR Am J Roentgenol. 1993;  160(5) 1053-1057
• 56 Zini J, Tobelem G. Angiogenesis and hematologic malignancy.  [in French] Bull Cancer. 2007;  94 S241-S246
• 57 Daldrup-Link H E, Okuhata Y, Wolfe A et al.. Decrease in tumor apparent permeability-surface area product to a MRI macromolecular contrast medium following angiogenesis inhibition with correlations to cytotoxic drug accumulation.  Microcirculation. 2004;  11(5) 387-396
• 58 Smith A R, Hennessy J M, Kurth M A, Nelson S C. Reversible skeletal changes after treatment with bevacizumab in a child with cutaneovisceral angiomatosis with thrombocytopenia syndrome.  Pediatr Blood Cancer. 2008;  51(3) 418-420
• 59 Lieschke G J, Burgess A W. Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor (2).  N Engl J Med. 1992;  327(2) 99-106
• 60 Kröger N, Zander A. Dose and schedule effect of G-GSF for stem cell mobilization in healthy donors for allogeneic transplantation.  Leuk Lymphoma. 2002;  43(7) 1391-1394
• 61 Hartman R P, Sundaram M, Okuno S H, Sim F H. Effect of granulocyte-stimulating factors on marrow of adult patients with musculoskeletal malignancies: incidence and MRI findings.  AJR Am J Roentgenol. 2004;  183(3) 645-653
• 62 Fletcher B D, Wall J E, Hanna S L. Effect of hematopoietic growth factors on MR images of bone marrow in children undergoing chemotherapy.  Radiology. 1993;  189(3) 745-751
• 63 Ryan S P, Weinberger E, White K S et al.. MR imaging of bone marrow in children with osteosarcoma: effect of granulocyte colony-stimulating factor.  AJR Am J Roentgenol. 1995;  165(4) 915-920
• 64 Vanel D, Missenard G, Le Cesne A, Guinebretière J. Red marrow recolonization induced by growth factors mimicking an increase in tumor volume during preoperative chemotherapy: MR study.  J Comput Assist Tomogr. 1997;  21(4) 529-531
• 65 Kricun M E. Red-yellow marrow conversion: its effect on the location of some solitary bone lesions.  Skeletal Radiol. 1985;  14(1) 10-19