MR imaging of therapy-induced changes of bone marrow

European Radiology

Volumn 17, Issue 3, 2007, Pages 743-761

  Daldrup Link, Heike E ^a   Henning, Tobias ^a   Link, Thomas M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bone marrow; Contrast agents; MR imaging; Treatment effects

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; B 22956 1; CODE 7228; CONTRAST MEDIUM; CORTISONE ACETATE; CYCLODEXTRIN DERIVATIVE; CYCLODEXTRIN TETRADECASULFATE; CYTARABINE; CYTOTOXIC AGENT; GADOFOSVESET; GADOLINIUM PENTETATE; GADOMER 17; GRANULOCYTE COLONY STIMULATING FACTOR; MINOCYCLINE; RESOVIST S; SHU 555C; STEROID; SUPERPARAMAGNETIC IRON OXIDE; TETRAHYDROCORTISOL; THALIDOMIDE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG; VASCULOTROPIN ANTIBODY; VSOP;

ACUTE GRANULOCYTIC LEUKEMIA; AMYLOIDOSIS; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APLASIA; AUTOLOGOUS STEM CELL TRANSPLANTATION; AVASCULAR NECROSIS; BONE CANCER; BONE MARROW DISEASE; BONE MARROW METASTASIS; BONE MARROW TOXICITY; BONE MARROW TRANSPLANTATION; CELL PROLIFERATION; CLINICAL TRIAL; DRUG MEGADOSE; DRUG POTENTIATION; FRACTURE; GRAFT VERSUS HOST REACTION; HEMATOLOGIC MALIGNANCY; HUMAN; INTERMETHOD COMPARISON; IRON OVERLOAD; LEUKEMIA; LYMPHOMA; MICROCIRCULATION; MICROENVIRONMENT; MYELOFIBROSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOCHONDROMA; OSTEOSARCOMA; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RADIATION EXPOSURE; REVIEW; TREATMENT INDICATION; WHOLE BODY RADIATION;

ANTI-INFLAMMATORY AGENTS; ANTINEOPLASTIC AGENTS; BONE MARROW; CONTRAST MEDIA; CORTISONE; HEMATOLOGIC NEOPLASMS; HUMANS; LYMPHOMA; MAGNETIC RESONANCE IMAGING;

EID: 33846946169     PISSN: 09387994     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00330-006-0404-1     Document Type: Review

References (86)

1. Plecha DM (2000) Imaging of bone marrow disease in the spine. Semin Musculoskelet Radiol 4:321-327
2. Durie BG, Salmon SE (1975) A clinical staging system for multiple myeloma. Correlation of measured myeloma cell mass with presenting clinical features, response to treatment, and survival. Cancer 36:842-854
3. Coller BS, Chabner BA, Gralnick HR (1977) Frequencies and patterns of bone marrow involvement in non-Hodgkin lymphomas: Observations on the value of bilateral biopsies. Am J Hematol 3:105-119
4. Brunning RD, Bloomfield CD, McKenna RW, Peterson LA (1975) Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic diseases. Ann Intern Med 82:365-366
5. Schirrmeister H, Bommer M, Buck AK, Muller S, Messer P, Bunjes D, Dohner H, Bergmann L, Reske SN (2002) Initial results in the assessment of multiple myeloma using 18F-FDG PET. Eur J Nucl Med Mol Imaging 29:361-366
6. Lecouvet FE, Malghem J, Michaux L, Maldague B, Ferrant A, Michaux JL, Vande Berg BC (1999) Skeletal survey in advanced multiple myeloma: radiographic versus MR imaging survey. Br J Haematol 106:35-39
7. Baur A, Stabler A, Nagel D, Lamerz R, Bartl R, Hiller E, Wendtner C, Bachner F, Reiser M (2002) Magnetic resonance imaging as a supplement for the clinical staging system of Durie and Salmon? Cancer 95:1334-1345
8. Dimopoulos MA, Moulopoulos A, Smith T, Delasalle KB, Alexanian R (1993) Risk of disease progression in asymptomatic multiple myeloma. Am J Med 94:57-61
9. Van de Berg BC, Lecouvet FE, Michaux L, Labaisse M, Malghem J, Jamart J, Maldague BE, Ferrant A, Michaux JL (1996) Stage I multiple myeloma: value of MR imaging of the bone marrow in the determination of prognosis. Radiology 201:243-246
10. Smith DB, Scarffe JH, Eddleston B (1988) The prognostic significance of X-ray changes at presentation and reassessment in patients with multiple myeloma. Hematol Oncol 6:1-6
11. Moulopoulos LA, Varma DG, Dimopoulos MA, Leeds NE, Kim EE, Johnston DA, Alexanian R, Libshitz HI (1992) Multiple myeloma: Spinal MR imaging in patients with untreated newly diagnosed disease. Radiology 185:833-840
12. Hoane BR, Shields AF, Porter BA, Shulman HM (1991) Detection of lymphomatous bone marrow involvement with magnetic resonance imaging. Blood 78:728-738
13. Tsunoda S, Takagi S, Tanaka O, Miura Y (1997) Clinical and prognostic significance of femoral marrow magnetic resonance imaging in patients with malignant lymphoma. Blood 89:286-290
14. Munk PL, Helms CA, Holt RG (1989) Immature bone infarcts: Findings on plain radiographs and MR scans. Am J Roentgenol 152:547-549
15. Ishibashi Y, Okamura Y, Otsuka H, Nishizawa K, Sasaki T, Toh S (2002) Comparison of scintigraphy and magnetic resonance imaging for stress injuries of bone. Clin J Sport Med 12:79-84
16. Ghanem N, Lohrmann C, Engelhardt M, Pache G, Uhl M, Saueressig U, Kotter E, Langer M (2006) Whole-body MRI in the detection of bone marrow infiltration in patients with plasma cell neoplasms in comparison to the radiological skeletal survey. Eur Radiol 16:1005-1014
17. Metz S, Lohr S, Settles M, Beer A, Woertler K, Rummeny EJ, Daldrup-Link HE (2006) Ferumoxtran-10-enhanced MR imaging of the bone marrow before and after conditioning therapy in patients with non-Hodgkin lymphomas. Eur Radiol 16:598-607
18. Delfaut EM, Beltran J, Johnson G, Rousseau J, Marchandise X, Cotten A (1999) Fat suppression in MR imaging: Techniques and pitfalls. Radiographics 19:373-382
19. Rahmouni A, Montazel JL, Divine M, Lepage E, Belhadj K, Gaulard P, Bouanane M, Golli M, Kobeiter H (2003) Bone marrow with diffuse tumor infiltration in patients with lymphoproliferative diseases: Dynamic gadolinium-enhanced MR imaging. Radiology 229:710-717
20. Baur A, Stabler A, Bruning R, Bartl R, Krodel A, Reiser M, Deimling M (1998) Diffusion-weighted MR imaging of bone marrow: Differentiation of benign versus pathologic compression fractures. Radiology 207:349-356
21. Ballon D, Watts R, Dyke JP, Lis E, Morris MJ, Scher HI, Ulug AM, Jakubowski AA (2004) Imaging therapeutic response in human bone marrow using rapid whole-body MRI. Magn Reson Med 52:1234-1238
22. Vacca A, Ribatti D, Roncali L, Ranieri G, Serio G, Silvestris F, Dammacco F (1994) Bone marrow angiogenesis and progression in multiple myeloma. Br J Haematol 87:503-508
23. Rahmouni A, Tempany C, Jones R, Mann R, Yang A, Zerhouni E (1993) Lymphoma: Monitoring tumor size and signal intensity with MR imaging. Radiology 188:445-451
24. Vande Berg BC, Lecouvet FE, Galant C, Maldague BE, Malghem J (2005) Normal variants and frequent marrow alterations that simulate bone marrow lesions at MR imaging. Radiol Clin North Am 43:761-770, ix
25. Montazel JL, Divine M, Lepage E, Kobeiter H, Breil S, Rahmouni A (2003) Normal spinal bone marrow in adults: Dynamic gadolinium-enhanced MR imaging. Radiology 229:703-709
26. Baur A, Stabler A, Bartl R, Lamerz R, Scheidler J, Reiser M (1997) MRI gadolinium enhancement of bone marrow: Age-related changes in normals and in diffuse neoplastic infiltration. Skeletal Radiol 26:414-418
27. Daldrup-Link HE, Link TM, Rummeny EJ, August C, Konemann S, Jurgens H, Heindel W (2000) Assessing permeability alterations of the blood-bone marrow barrier due to total body irradiation: In vivo quantification with contrast enhanced magnetic resonance imaging. Bone Marrow Transplant 25:71-78
28. Seneterre E, Weissleder R, Jaramillo D, Reimer P, Lee AS, Brady TJ, Wittenberg J (1991) Bone marrow: Ultrasmall superparamagnetic iron oxide for MR imaging. Radiology 179:529-533
29. Bush CH, Mladinich CR, Montgomery WJ (1997) Evaluation of an ultrasmall superparamagnetic iron oxide in MRI in a bone tumor model in rabbits. J Magn Reson Imaging 7:579-584
30. Simon GH, Raatschen HJ, Wendland MF, von Vopelius-Feldt J, Fu Y, Chen MH, Daldrup-Link HE (2005) Ultrasmall superparamagnetic iron-oxide-enhanced MR imaging of normal bone marrow in rodents: original research original research. Acad Radiol 12:1190-1197
31. Daldrup-Link HE, Rummeny EJ, Ihssen B, Kienast J, Link TM (2002) 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 12:1557-1566
32. Wang CK, Li CW, Hsieh TJ, Chien SH, Liu GC, Tsai KB (2004) Characterization of bone and soft-tissue tumors with in vivo 1H MR spectroscopy: Initial results. Radiology 232:599-605
33. Somer EJ, Marsden PK, Benatar NA, Goodey J, O'Doherty MJ, Smith MA (2003) PET-MR image fusion in soft tissue sarcoma: Accuracy, reliability and practicality of interactive point-based and automated mutual information techniques. Eur J Nucl Med Mol Imaging 30:54-62
34. Pichler BJ, Judenhofer MS, Catana C, Walton JH, Kneilling M, Nutt RE, Siegel SB, Claussen CD, Cherry SR (2006) Performance Test of an LSO-APD Detector in a 7-T MRI Scanner for Simultaneous PET/MRI. J Nucl Med 47:639-647
35. Babyn PS, Ranson M, McCarville ME (1998) Normal bone marrow: Signal characteristics and fatty conversion. Magn Reson Imaging Clin N Am 6:473-495
36. Zawin JK, Jaramillo D (1993) Conversion of bone marrow in the humerus, sternum, and clavicle: Changes with age on MR images. Radiology 188:159-164
37. Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, Zerhouni EA (1990) Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 177:83-88
38. Moore SG, Dawson KL (1990) Red and yellow marrow in the femur: age-related changes in appearance at MR imaging. Radiology 175:219-223
39. Wasser K, Moehler T, Nosas-Garcia S, Rehm C, Bartl R, Goldschmidt H, Duber C, Kauczor HU, Delorme S (2005) Correlation of MRI and histopathology of bone marrow in patients with multiple myeloma. Rofo 177:1116-1122
40. Lecouvet FE, Vande Berg BC, Michaux L, Malghem J, Maldague BE, Jamart J, Ferrant A, Michaux JL (1998) Stage III multiple myeloma: Clinical and prognostic value of spinal bone marrow MR imaging. Radiology 209:653-660
41. Moehler TM, Hawighorst H, Neben K, Egerer G, Hillengass J, Max R, Benner A, Ho AD, van Kaick G, Goldschmidt H (2001) Bone marrow microcirculation analysis in multiple myeloma by contrast-enhanced dynamic magnetic resonance imaging. Int J Cancer 93:862-868
42. Nosas-Garcia S, Moehler T, Wasser K, Kiessling F, Bartl R, Zuna I, Hillengass J, Goldschmidt H, Kauczor HU, Delorme S (2005) Dynamic contrast-enhanced MRI for assessing the disease activity of multiple myeloma: A comparative study with histology and clinical markers. J Magn Reson Imaging 22:154-162
43. Stabler A, Baur A, Bartl R, Munker R, Lamerz R, Reiser MF (1996) Contrast enhancement and quantitative signal analysis in MR imaging of multiple myeloma: Assessment of focal and diffuse growth patterns in marrow correlated with biopsies and survival rates. Am J Roentgenol 167:1029-1036
44. Yankelevitz DF, Henschke CI, Knapp PH, Nisce L, Yi Y, Cahill P (1991) Effect of radiation therapy on thoracic and lumbar bone marrow: evaluation with MR imaging. Am J Roentgenol 157:87-92
45. Otake S, Mayr NA, Ueda T, Magnotta VA, Yuh WT (2002) Radiation-induced changes in MR signal intensity and contrast enhancement of lumbosacral vertebrae: Do changes occur only inside the radiation therapy field? Radiology 222:179-183
46. Blomlie V, Rofstad EK, Skjonsberg A, Tvera K, Lien HH (1995) Female pelvic bone marrow: Serial MR imaging before, during, and after radiation therapy. Radiology 194:537-543
47. Roebuck DJ (1999) Skeletal complications in pediatric oncology patients. Radiographics 19:873-885
48. Fletcher BD, Crom DB, Krance RA, Kun LE (1994) Radiation-induced bone abnormalities after bone marrow transplantation for childhood leukemia. Radiology 191:231-235
49. Perez CA, Vietti T, Ackerman LV, Eagleton MD, Powers WE (1967) Tumors of the sympathetic nervous system in children. An appraisal of treatment and results. Radiology 88:750-760
50. Maghami EG, St-John M, Bhuta S, Abemayor E (2005) Postirradiation sarcoma: A case report and current review. Am J Otolaryngol 26:71-74
51. Tountas AA, Fornasier VL, Harwood AR, Leung PM (1979) Postirradiation sarcoma of bone: A perspective. Cancer 43:182-187
52. Iida S, Harada Y, Shimizu K, Sakamoto M, Ikenoue S, Akita T, Kitahara H, Moriya H (2000) Correlation between bone marrow edema and collapse of the femoral head in steroid-induced osteonecrosis. Am J Roentgenol 174:735-743
53. Turner DA, Templeton AC, Selzer PM, Rosenberg AG, Petasnick JP (1989) Femoral capital osteonecrosis: MR finding of diffuse marrow abnormalities without focal lesions. Radiology 171:135-140
54. Mitchell DG, Rao VM, Dalinka MK, Spritzer CE, Alavi A, Steinberg ME, Fallon M, Kressel HY (1987) Femoral head avascular necrosis: Correlation of MR imaging, radiographic staging, radionuclide imaging, and clinical findings. Radiology 162:709-715
55. Maheshwari PR, Nagar AM, Prasad SS, Shah JR, Patkar DP (2004) Avascular necrosis of spine: A rare appearance. Spine 29:E119-E122
56. Gerard EL, Ferry JA, Amrein PC, Harmon DC, McKinstry RC, Hoppel BE, Rosen BR (1992) Compositional changes in vertebral bone marrow during treatment for acute leukemia: Assessment with quantitative chemical shift imaging. Radiology 183:39-46
57. Islam A, Catovsky D, Galton DA (1980) Histological study of bone marrow regeneration following chemotherapy for acute myeloid leukaemia and chronic granulocytic leukaemia in blast transformation. Br J Haematol 45:535-540
58. Moulopoulos LA, Dimopoulos MA, Alexanian R, Leeds NE, Libshitz HI (1994) Multiple myeloma: MR patterns of response to treatment. Radiology 193:441-446
59. Zinzani PL (2005) Lymphoma: Diagnosis, staging, natural history, and treatment strategies. Semin Oncol 32:S4-S10
60. Rahmouni A, Divine M, Mathieu D, Golli M, Haioun C, Dao T, Anglade MC, Reyes F, Vasile N (1993) MR appearance of multiple myeloma of the spine before and after treatment. Am J Roentgenol 160:1053-1057
61. Lien HH, Holte H (1996) Fat replacement of Hodgkin disease of bone marrow after chemotherapy: Report of three cases. Skeletal Radiol 25:671-674
62. Fassas AB, Muwalla F, Berryman T, Benramdane R, Joseph L, Anaissie E, Sethi R, Desikan R, Siegel D, Badros A, Toor A, Zangari M, Morris C, Angtuaco E, Mathew S, Wilson C, Hough A, Harik S, Barlogie B, Tricot G (2002) Myeloma of the central nervous system: Association with high-risk chromosomal abnormalities, plasmablastic morphology and extramedullary manifestations. Br J Haematol 117:103-108
63. Angtuaco EJ, Fassas AB, Walker R, Sethi R, Barlogie B (2004) Multiple myeloma: Clinical review and diagnostic imaging. Radiology 231:11-23
64. Smith SR, Martin PA, Edwards RH (1991) tumor pH and response to chemotherapy: An in vivo 31P magnetic resonance spectroscopy study in non-Hodgkin's lymphoma. Br J Radiol 64:923-928
65. Kuliszkiewicz-Janus M, Baczynski S, Jurczyk A (2004) Bone marrow transplantation in the course of hematological malignancies-follow-up study in blood serum by 31P MRS. Med Sci Monit 10:CR485-CR492
66. Fletcher BD, Wall JE, Hanna SL (1993) Effect of hematopoietic growth factors on MR images of bone marrow in children undergoing chemotherapy. Radiology 189:745-751
67. Layer G, Sander W, Traber F, Block W, Ko Y, Ziske CG, Konig R, Vahlensieck M, Schild HH (2000) The diagnostic problems in magnetic resonance tomography of the bone marrow in patients with malignomas under G-CSF therapy. Radiologe 40:710-715
68. Vanel D, Missenard G, Le Cesne A, Guinebretiere JM (1997) Red marrow recolonization induced by growth factors mimicking an increase in tumor volume during preoperative chemotherapy: MR study. J Comput Assist Tomogr 21:529-531
69. Hawighorst H, Libicher M, Knopp MV, Moehler T, Kauffmann GW, Kaick G (1999) Evaluation of angiogenesis and perfusion of bone marrow lesions: role of semiquantitative and quantitative dynamic MRI. J Magn Reson Imaging 10:286-294
70. Bollow M, Knauf W, Korfel A, Taupitz M, Schilling A, Wolf KJ, Hamm B (1997) Initial experience with dynamic MR imaging in evaluation of normal bone marrow versus malignant bone marrow infiltrations in humans. J Magn Reson Imaging 7:241-250
71. Moulopoulos LA, Maris TG, Papanikolaou N, Panagi G, Vlahos L, Dimopoulos MA (2003) Detection of malignant bone marrow involvement with dynamic contrast-enhanced magnetic resonance imaging. Ann Oncol 14:152-158
72. Lieschke GJ, Burgess AW (1992) Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor (1). N Engl J Med 327:28-35
73. Vande Berg BC, Lecouvet FE, Kanku JP, Jamart J, Van Beers BE, Maldague B, Malghem J (1999) Ferumoxides-enhanced quantitative magnetic resonance imaging of the normal and abnormal bone marrow: Preliminary assessment. J Magn Reson Imaging 9:322-328
74. Singhal S, Mehta J, Desikan R, Ayers D, Roberson P, Eddlemon P, Munshi N, Anaissie E, Wilson C, Dhodapkar M, Zeddis J, Barlogie B (1999) Antitumor activity of thalidomide in refractory multiple myeloma. N Engl J Med 341:1565-1571
75. Pham CD, Roberts TP, van Bruggen N, Melnyk O, Mann J, Ferrara N, Cohen RL, Brasch RC (1998) Magnetic resonance imaging detects suppression of tumor vascular permeability after administration of antibody to vascular endothelial growth factor. Cancer Invest 16:225-230
76. Daldrup-Link HE, Okuhata Y, Wolfe A, Srivastav S, Oie S, Ferrara N, Cohen RL, Shames DM, Brasch RC (2004) Decrease in tumor apparent permeability-surface area product to a MRI macromolecular contrast medium following angiogenesis inhibition with correlations to cytotoxic drug accumulation. Microcirculation 11:387-396
77. Teicher BA, Sotomayor EA, Huang ZD (1992) Antiangiogenic agents potentiate cytotoxic cancer therapies against primary and metastatic disease. Cancer Res 52:6702-6704
78. Lee K, Erturk E, Mayer R, Cockett AT (1987) Efficacy of antitumor chemotherapy in C3H mice enhanced by the antiangiogenesis steroid, cortisone acetate. Cancer Res 47:5021-5024
79. Gali-Muhtasib H, Sidani M, Geara F, Mona AD, Al-Hmaira J, Haddadin MJ, Zaatari G (2004) Quinoxaline 1,4-dioxides are novel angiogenesis inhibitors that potentiate antitumor effects of ionizing radiation. Int J Oncol 24:1121-1131
80. Lecouvet FE, Dechambre S, Malghem J, Ferrant A, Vande Berg BC, Maldague B (2001) Bone marrow transplantation in patients with multiple myeloma: prognostic significance of MR imaging. Am J Roentgenol 176:91-96
81. Negendank W, Soulen RL (1993) Magnetic resonance imaging in patients with bone marrow disorders. Leuk Lymphoma 10:287-298
82. Stevens SK, Moore SG, Amylon MD (1990) Repopulation of marrow after transplantation: MR imaging with pathologic correlation. Radiology 175:213-218
83. Moulopoulos LA, Dimopoulos MA (1997) Magnetic resonance imaging of the bone marrow in hematologic malignancies. Blood 90:2127-2147
84. Tanner SF, Clarke J, Leach MO, Mesbahi MH, Nicolson V, Powles R, Husband JE, Tait D (1996) MRI in the evaluation of late bone marrow changes following bone marrow transplantation. Br J Radiol 69:1145-1151
85. Lien HH, Blomlie V, Blystad AK, Holte H, Langholm R, Kvaloy S (1997) Bone-marrow MR imaging before and after autologous marrow transplantation in lymphoma patients without known bone-marrow involvement. Acta Radiol 38:896-902
86. Kornreich L, Horev G, Yaniv I, Stein J, Grunebaum M, Zaizov R (1997) Iron overload following bone marrow transplantation in children: MR findings. Pediatr Radiol 27:869-872