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Published in: European Radiology 3/2007

Open Access 01-03-2007 | Musculoskeletal

MR imaging of therapy-induced changes of bone marrow

Authors: Heike E. Daldrup-Link, Tobias Henning, Thomas M. Link

Published in: European Radiology | Issue 3/2007

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Abstract

MR imaging of bone marrow infiltration by hematologic malignancies provides non-invasive assays of bone marrow cellularity and vascularity to supplement the information provided by bone marrow biopsies. This article will review the MR imaging findings of bone marrow infiltration by hematologic malignancies with special focus on treatment effects. MR imaging findings of the bone marrow after radiation therapy and chemotherapy will be described. In addition, changes in bone marrow microcirculation and metabolism after anti-angiogenesis treatment will be reviewed. Finally, new specific imaging techniques for the depiction of regulatory events that control blood vessel growth and cell proliferation will be discussed. Future developments are directed to yield comprehensive information about bone marrow structure, function and microenvironment.
Literature
1.
go back to reference Plecha DM (2000) Imaging of bone marrow disease in the spine. Semin Musculoskelet Radiol 4:321–327PubMedCrossRef Plecha DM (2000) Imaging of bone marrow disease in the spine. Semin Musculoskelet Radiol 4:321–327PubMedCrossRef
2.
go back to reference 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 36:842–854PubMedCrossRef 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 36:842–854PubMedCrossRef
3.
go back to reference 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 3:105–119PubMed 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 3:105–119PubMed
4.
go back to reference Brunning RD, Bloomfield CD, McKenna RW, Peterson LA (1975) Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic diseases. Ann Intern Med 82:365–366PubMed Brunning RD, Bloomfield CD, McKenna RW, Peterson LA (1975) Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic diseases. Ann Intern Med 82:365–366PubMed
5.
go back to reference 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 29:361–366PubMedCrossRef 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 29:361–366PubMedCrossRef
6.
go back to reference 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 106:35–39PubMedCrossRef 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 106:35–39PubMedCrossRef
7.
go back to reference 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 95:1334–1345PubMedCrossRef 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 95:1334–1345PubMedCrossRef
8.
go back to reference Dimopoulos MA, Moulopoulos A, Smith T, Delasalle KB, Alexanian R (1993) Risk of disease progression in asymptomatic multiple myeloma. Am J Med 94:57–61PubMedCrossRef Dimopoulos MA, Moulopoulos A, Smith T, Delasalle KB, Alexanian R (1993) Risk of disease progression in asymptomatic multiple myeloma. Am J Med 94:57–61PubMedCrossRef
9.
go back to reference 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 201:243–246PubMed 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 201:243–246PubMed
10.
go back to reference 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 6:1–6PubMed 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 6:1–6PubMed
11.
go back to reference 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 185:833–840PubMed 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 185:833–840PubMed
12.
go back to reference Hoane BR, Shields AF, Porter BA, Shulman HM (1991) Detection of lymphomatous bone marrow involvement with magnetic resonance imaging. Blood 78:728–738PubMed Hoane BR, Shields AF, Porter BA, Shulman HM (1991) Detection of lymphomatous bone marrow involvement with magnetic resonance imaging. Blood 78:728–738PubMed
13.
go back to reference 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 89:286–290PubMed 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 89:286–290PubMed
14.
go back to reference Munk PL, Helms CA, Holt RG (1989) Immature bone infarcts: findings on plain radiographs and MR scans. Am J Roentgenol 152:547–549PubMed Munk PL, Helms CA, Holt RG (1989) Immature bone infarcts: findings on plain radiographs and MR scans. Am J Roentgenol 152:547–549PubMed
15.
go back to reference 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 12:79–84PubMedCrossRef 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 12:79–84PubMedCrossRef
16.
go back to reference 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 16:1005–1014PubMedCrossRef 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 16:1005–1014PubMedCrossRef
17.
go back to reference 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 16:598–607PubMedCrossRef 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 16:598–607PubMedCrossRef
18.
go back to reference Delfaut EM, Beltran J, Johnson G, Rousseau J, Marchandise X, Cotten A (1999) Fat suppression in MR imaging: techniques and pitfalls. Radiographics 19:373–382PubMed Delfaut EM, Beltran J, Johnson G, Rousseau J, Marchandise X, Cotten A (1999) Fat suppression in MR imaging: techniques and pitfalls. Radiographics 19:373–382PubMed
19.
go back to reference 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 229:710–717PubMed 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 229:710–717PubMed
20.
go back to reference 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 207:349–356PubMed 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 207:349–356PubMed
21.
go back to reference 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 52:1234–1238PubMedCrossRef 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 52:1234–1238PubMedCrossRef
22.
go back to reference 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 87:503–508PubMed 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 87:503–508PubMed
23.
go back to reference Rahmouni A, Tempany C, Jones R, Mann R, Yang A, Zerhouni E (1993) Lymphoma: monitoring tumor size and signal intensity with MR imaging. Radiology 188:445–451PubMed Rahmouni A, Tempany C, Jones R, Mann R, Yang A, Zerhouni E (1993) Lymphoma: monitoring tumor size and signal intensity with MR imaging. Radiology 188:445–451PubMed
24.
go back to reference 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, ixCrossRef 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, ixCrossRef
25.
go back to reference 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 229:703–709PubMed 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 229:703–709PubMed
26.
go back to reference 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 26:414–418PubMedCrossRef 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 26:414–418PubMedCrossRef
27.
go back to reference 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 25:71–78PubMedCrossRef 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 25:71–78PubMedCrossRef
28.
go back to reference 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 179:529–533PubMed 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 179:529–533PubMed
29.
go back to reference 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 7:579–584PubMed 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 7:579–584PubMed
30.
go back to reference 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 12:1190–1197PubMedCrossRef 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 12:1190–1197PubMedCrossRef
31.
go back to reference 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 12:1557–1566PubMedCrossRef 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 12:1557–1566PubMedCrossRef
32.
go back to reference 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 232:599–605PubMed 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 232:599–605PubMed
33.
go back to reference 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 30:54–62PubMedCrossRef 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 30:54–62PubMedCrossRef
34.
go back to reference 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 47:639–647PubMed 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 47:639–647PubMed
35.
go back to reference Babyn PS, Ranson M, McCarville ME (1998) Normal bone marrow: signal characteristics and fatty conversion. Magn Reson Imaging Clin N Am 6:473–495PubMed Babyn PS, Ranson M, McCarville ME (1998) Normal bone marrow: signal characteristics and fatty conversion. Magn Reson Imaging Clin N Am 6:473–495PubMed
36.
go back to reference Zawin JK, Jaramillo D (1993) Conversion of bone marrow in the humerus, sternum, and clavicle: changes with age on MR images. Radiology 188:159–164PubMed Zawin JK, Jaramillo D (1993) Conversion of bone marrow in the humerus, sternum, and clavicle: changes with age on MR images. Radiology 188:159–164PubMed
37.
go back to reference 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 177:83–88PubMed 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 177:83–88PubMed
38.
go back to reference Moore SG, Dawson KL (1990) Red and yellow marrow in the femur: age-related changes in appearance at MR imaging. Radiology 175:219–223PubMed Moore SG, Dawson KL (1990) Red and yellow marrow in the femur: age-related changes in appearance at MR imaging. Radiology 175:219–223PubMed
39.
go back to reference 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 177:1116–1122PubMed 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 177:1116–1122PubMed
40.
go back to reference 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 209:653–660PubMed 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 209:653–660PubMed
41.
go back to reference 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 93:862–868PubMedCrossRef 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 93:862–868PubMedCrossRef
42.
go back to reference 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 22:154–162PubMedCrossRef 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 22:154–162PubMedCrossRef
43.
go back to reference 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 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.
go back to reference 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 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.
go back to reference 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 222:179–183PubMed 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 222:179–183PubMed
46.
go back to reference 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 194:537–543PubMed 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 194:537–543PubMed
47.
go back to reference Roebuck DJ (1999) Skeletal complications in pediatric oncology patients. Radiographics 19:873–885PubMed Roebuck DJ (1999) Skeletal complications in pediatric oncology patients. Radiographics 19:873–885PubMed
48.
go back to reference Fletcher BD, Crom DB, Krance RA, Kun LE (1994) Radiation-induced bone abnormalities after bone marrow transplantation for childhood leukemia. Radiology 191:231–235PubMed Fletcher BD, Crom DB, Krance RA, Kun LE (1994) Radiation-induced bone abnormalities after bone marrow transplantation for childhood leukemia. Radiology 191:231–235PubMed
49.
go back to reference 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 88:750–760PubMed 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 88:750–760PubMed
50.
go back to reference Maghami EG, St-John M, Bhuta S, Abemayor E (2005) Postirradiation sarcoma: a case report and current review. Am J Otolaryngol 26:71–74PubMedCrossRef Maghami EG, St-John M, Bhuta S, Abemayor E (2005) Postirradiation sarcoma: a case report and current review. Am J Otolaryngol 26:71–74PubMedCrossRef
51.
go back to reference Tountas AA, Fornasier VL, Harwood AR, Leung PM (1979) Postirradiation sarcoma of bone: a perspective. Cancer 43:182–187PubMedCrossRef Tountas AA, Fornasier VL, Harwood AR, Leung PM (1979) Postirradiation sarcoma of bone: a perspective. Cancer 43:182–187PubMedCrossRef
52.
go back to reference 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 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.
go back to reference Turner DA, Templeton AC, Selzer PM, Rosenberg AG, Petasnick JP (1989) Femoral capital osteonecrosis: MR finding of diffuse marrow abnormalities without focal lesions. Radiology 171:135–140PubMed Turner DA, Templeton AC, Selzer PM, Rosenberg AG, Petasnick JP (1989) Femoral capital osteonecrosis: MR finding of diffuse marrow abnormalities without focal lesions. Radiology 171:135–140PubMed
54.
go back to reference 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 162:709–715PubMed 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 162:709–715PubMed
55.
go back to reference Maheshwari PR, Nagar AM, Prasad SS, Shah JR, Patkar DP (2004) Avascular necrosis of spine: a rare appearance. Spine 29:E119–E122PubMedCrossRef Maheshwari PR, Nagar AM, Prasad SS, Shah JR, Patkar DP (2004) Avascular necrosis of spine: a rare appearance. Spine 29:E119–E122PubMedCrossRef
56.
go back to reference 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 183:39–46PubMed 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 183:39–46PubMed
57.
go back to reference 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 45:535–540PubMed 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 45:535–540PubMed
58.
go back to reference Moulopoulos LA, Dimopoulos MA, Alexanian R, Leeds NE, Libshitz HI (1994) Multiple myeloma: MR patterns of response to treatment. Radiology 193:441–446PubMed Moulopoulos LA, Dimopoulos MA, Alexanian R, Leeds NE, Libshitz HI (1994) Multiple myeloma: MR patterns of response to treatment. Radiology 193:441–446PubMed
59.
go back to reference Zinzani PL (2005) Lymphoma: diagnosis, staging, natural history, and treatment strategies. Semin Oncol 32:S4–S10PubMedCrossRef Zinzani PL (2005) Lymphoma: diagnosis, staging, natural history, and treatment strategies. Semin Oncol 32:S4–S10PubMedCrossRef
60.
go back to reference 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 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.
go back to reference Lien HH, Holte H (1996) Fat replacement of Hodgkin disease of bone marrow after chemotherapy: report of three cases. Skeletal Radiol 25:671–674PubMedCrossRef Lien HH, Holte H (1996) Fat replacement of Hodgkin disease of bone marrow after chemotherapy: report of three cases. Skeletal Radiol 25:671–674PubMedCrossRef
62.
go back to reference 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 117:103–108PubMedCrossRef 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 117:103–108PubMedCrossRef
63.
go back to reference Angtuaco EJ, Fassas AB, Walker R, Sethi R, Barlogie B (2004) Multiple myeloma: clinical review and diagnostic imaging. Radiology 231:11–23PubMed Angtuaco EJ, Fassas AB, Walker R, Sethi R, Barlogie B (2004) Multiple myeloma: clinical review and diagnostic imaging. Radiology 231:11–23PubMed
64.
go back to reference 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 64:923–928PubMedCrossRef 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 64:923–928PubMedCrossRef
65.
go back to reference 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–CR492PubMed 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–CR492PubMed
66.
go back to reference Fletcher BD, Wall JE, Hanna SL (1993) Effect of hematopoietic growth factors on MR images of bone marrow in children undergoing chemotherapy. Radiology 189:745–751PubMed Fletcher BD, Wall JE, Hanna SL (1993) Effect of hematopoietic growth factors on MR images of bone marrow in children undergoing chemotherapy. Radiology 189:745–751PubMed
67.
go back to reference 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 40:710–715PubMedCrossRef 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 40:710–715PubMedCrossRef
68.
go back to reference 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 21:529–531PubMedCrossRef 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 21:529–531PubMedCrossRef
69.
go back to reference 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 10:286–294PubMedCrossRef 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 10:286–294PubMedCrossRef
70.
go back to reference 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 7:241–250PubMed 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 7:241–250PubMed
71.
go back to reference 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 14:152–158PubMedCrossRef 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 14:152–158PubMedCrossRef
72.
go back to reference Lieschke GJ, Burgess AW (1992) Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor (1). N Engl J Med 327:28–35PubMedCrossRef Lieschke GJ, Burgess AW (1992) Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor (1). N Engl J Med 327:28–35PubMedCrossRef
73.
go back to reference 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 9:322–328PubMedCrossRef 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 9:322–328PubMedCrossRef
74.
go back to reference 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 341:1565–1571PubMedCrossRef 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 341:1565–1571PubMedCrossRef
75.
go back to reference 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 16:225–230PubMed 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 16:225–230PubMed
76.
go back to reference 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 11:387–396PubMedCrossRef 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 11:387–396PubMedCrossRef
77.
go back to reference Teicher BA, Sotomayor EA, Huang ZD (1992) Antiangiogenic agents potentiate cytotoxic cancer therapies against primary and metastatic disease. Cancer Res 52:6702–6704PubMed Teicher BA, Sotomayor EA, Huang ZD (1992) Antiangiogenic agents potentiate cytotoxic cancer therapies against primary and metastatic disease. Cancer Res 52:6702–6704PubMed
78.
go back to reference 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 47:5021–5024PubMed 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 47:5021–5024PubMed
79.
go back to reference 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 24:1121–1131PubMed 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 24:1121–1131PubMed
80.
go back to reference 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 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.
go back to reference Negendank W, Soulen RL (1993) Magnetic resonance imaging in patients with bone marrow disorders. Leuk Lymphoma 10:287–298PubMedCrossRef Negendank W, Soulen RL (1993) Magnetic resonance imaging in patients with bone marrow disorders. Leuk Lymphoma 10:287–298PubMedCrossRef
82.
go back to reference Stevens SK, Moore SG, Amylon MD (1990) Repopulation of marrow after transplantation: MR imaging with pathologic correlation. Radiology 175:213–218PubMed Stevens SK, Moore SG, Amylon MD (1990) Repopulation of marrow after transplantation: MR imaging with pathologic correlation. Radiology 175:213–218PubMed
83.
go back to reference Moulopoulos LA, Dimopoulos MA (1997) Magnetic resonance imaging of the bone marrow in hematologic malignancies. Blood 90:2127–2147PubMed Moulopoulos LA, Dimopoulos MA (1997) Magnetic resonance imaging of the bone marrow in hematologic malignancies. Blood 90:2127–2147PubMed
84.
go back to reference 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 69:1145–1151PubMed 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 69:1145–1151PubMed
85.
go back to reference 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 38:896–902PubMedCrossRef 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 38:896–902PubMedCrossRef
86.
go back to reference 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 27:869–872PubMedCrossRef 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 27:869–872PubMedCrossRef
Metadata
Title
MR imaging of therapy-induced changes of bone marrow
Authors
Heike E. Daldrup-Link
Tobias Henning
Thomas M. Link
Publication date
01-03-2007
Publisher
Springer-Verlag
Published in
European Radiology / Issue 3/2007
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-006-0404-1

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