Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
European Journal of Nuclear Medicine and Molecular Imaging
Published in: European Journal of Nuclear Medicine and Molecular Imaging 1/2011

Open Access 01-01-2011 | Review Article

Radionuclide imaging of bone marrow disorders

Authors: Ali Agool, Andor W. J. M. Glaudemans, Hendrikus H. Boersma, Rudi A. J. O. Dierckx, Edo Vellenga, Riemer H. J. A. Slart

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 1/2011

Login to get access

Abstract

Noninvasive imaging techniques have been used in the past for visualization the functional activity of the bone marrow compartment. Imaging with radiolabelled compounds may allow different bone marrow disorders to be distinguished. These imaging techniques, almost all of which use radionuclide-labelled tracers, such as 99mTc-nanocolloid, 99mTc-sulphur colloid, 111In-chloride, and radiolabelled white blood cells, have been used in nuclear medicine for several decades. With these techniques three separate compartments can be recognized including the reticuloendothelial system, the erythroid compartment and the myeloid compartment. Recent developments in research and the clinical use of PET tracers have made possible the analysis of additional properties such as cellular metabolism and proliferative activity, using 18F-FDG and 18F-FLT. These tracers may lead to better quantification and targeting of different cell systems in the bone marrow. In this review the imaging of different bone marrow targets with radionuclides including PET tracers in various bone marrow diseases are discussed.
Literature
1.
Rubin R, Strayer DS. Rubin's pathology: clinicopathologic foundations of medicine. Philadelphia: Lippincott Williams & Wilkins; 2007.
2.
Rizo A, Vellenga E, de Haan G, Schuringa JJ. Signaling pathways in self-renewing hematopoietic and leukemic stem cells: do all stem cells need a niche? Hum Mol Genet 2006;15(Spec no 2):R210–9
3.
Johnsen HE, Kjeldsen MK, Urup T, Fogd K, Pilgaard L, Boegsted M, et al. Cancer stem cells and the cellular hierarchy in haematological malignancies. Eur J Cancer 2009;45 Suppl 1:194–201.CrossRefPubMed
4.
Vardimann JW. Myelodysplastic/myeloproliferative diseases. In: Finn WG, Peterson LC, editors. Hematopathology in oncology. New York: Springer US; 2004. p. 13–43.CrossRef
5.
Schepers H, van Gosliga D, Wierenga AT, Eggen BJ, Schuringa JJ, Vellenga E. STAT5 is required for long-term maintenance of normal and leukemic human stem/progenitor cells. Blood 2007;110:2880–8.CrossRefPubMed
6.
Koch CA, Li CY, Mesa RA, Tefferi A. Nonhepatosplenic extramedullary hematopoiesis: associated diseases, pathology, clinical course, and treatment. Mayo Clin Proc 2003;78:1223–33.CrossRefPubMed
7.
Charache S, Page DL. Infarction of bone marrow in the sickle cell disorders. Ann Intern Med 1967;67:1195–200.PubMed
8.
Lutzker LG, Alavi A. Bone and marrow imaging in sickle cell disease: diagnosis of infarction. Semin Nucl Med 1976;6:83–93.CrossRefPubMed
9.
Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. World Health Organization (WHO) classification of tumors of hematopoietic and lymphoid tissues. 4th ed. Lyon: IARC Press; 2009.
10.
Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A, et al. Mutation in TET2 in myeloid cancers. N Engl J Med 2009;360:2289–301.CrossRefPubMed
11.
Jaffe ES, Harris NL, Stein H, Vardiman JW. Tumours of haematopoietic and lymphoid tissue, pathology and genetics. World Health Organization classification of tumours. Lyon: IARC Press, 2001.
12.
Tefferi A, Spivak JL. Polycythemia vera: scientific advances and current practice. Semin Hematol 2005;42:206–20.CrossRefPubMed
13.
Tennvall J, Brans B. EANM procedure guideline for 32P phosphate treatment of myeloproliferative diseases. Eur J Nucl Med Mol Imaging 2007;34:1324–7.CrossRefPubMed
14.
Tam CS, Kantarjian H, Cortes J, Lynn A, Pierce S, Zhou L, et al. Dynamic model for predicting death within 12 months in patients with primary or post-polycythemia vera/essential thrombocythemia myelofibrosis. J Clin Oncol 2009;27:5587–93.CrossRefPubMed
15.
Greenberg P, Anderson J, de Witte T, Estey E, Fenaux P, Gupta P, et al. Problematic WHO reclassification of myelodysplastic syndromes Members of the International MDS Study Group. J Clin Oncol 2000;18:3447–52.PubMed
16.
Williamson PJ, Kruger AR, Reynolds PJ, Hamblin TJ, Oscier DG. Establishing the incidence of myelodysplastic syndrome. Br J Haematol 1994;87:743–5.CrossRefPubMed
17.
Young NS. Acquired aplastic anemia. Ann Intern Med 2002;136:534–46.PubMed
18.
19.
Pitcher LA, Hann IM, Evans JP, Veys P, Chessells JM, Webb DK. Improved prognosis for acquired aplastic anaemia. Arch Dis Child 1999;80:158–62.CrossRefPubMed
20.
Desai AG, Thakur ML. Radiopharmaceuticals for spleen and bone marrow studies. Semin Nucl Med 1985;15:229–38.CrossRefPubMed
21.
22.
Milner PF, Brown M. Bone marrow infarction in sickle cell anemia: correlation with hematologic profiles. Blood 1982;60:1411–9.PubMed
23.
Blebea JS, Houseni M, Torigian DA, Fan C, Mavi A, Zhuge Y, et al. Structural and functional imaging of normal bone marrow and evaluation of its age-related changes. Semin Nucl Med 2007;37:185–94.CrossRefPubMed
24.
Ferrant A, Rodhain J, Leners N, Cogneau M, Verwilghen RL, Michaux JL, et al. Quantitative assessment of erythropoiesis in bone marrow expansion areas using 52Fe. Br J Haematol 1986;62:247–55.CrossRefPubMed
25.
Datz FL, Taylor A Jr. The clinical use of radionuclide bone marrow imaging. Semin Nucl Med 1985;15:239–59.CrossRefPubMed
26.
Itoh H, Kanamori M, Takahashi N. Dissociation between In-111 chloride and Tc-99m colloid bone marrow scintigraphy in refractory anemia with excess blasts. Clin Nucl Med 1990;15:124–5.CrossRefPubMed
27.
Sayle BA, Helmer III RE, Birdsong BA, Balachandran S, Gardner FH. Bone-marrow imaging with indium-111 chloride in aplastic anemia and myelofibrosis: concise communication. J Nucl Med 1982;23:121–5.PubMed
28.
Rain JD, Najean Y. Bone marrow scintigraphy in myelofibrosis. Nouv Rev Fr Hematol 1993;35:101–2.PubMed
29.
McNeil BJ, Rappeport JM, Nathan DG. Indium chloride scintigraphy: an index of severity in patients with aplastic anaemia. Br J Haematol 1976;34:599–604.CrossRefPubMed
30.
Hotta T, Murate T, Inoue C, Kagami T, Tsushita K, Wang JY, et al. Patchy haemopoiesis in long-term remission of idiopathic aplastic anaemia. Eur J Haematol 1990;45:73–7.CrossRefPubMed
31.
Huic D, Ivancevic V, Richter WS, Munz DL. Immunoscintigraphy of the bone marrow: normal uptake values of technetium-99m-labeled monoclonal antigranulocyte antibodies. J Nucl Med 1997;38:1755–8.PubMed
32.
Wahren B, Gahrton G, Hammarstrom S. Nonspecific cross-reacting antigen in normal and leukemic myeloid cells and serum of leukemic patients. Cancer Res 1980;40:2039–44.PubMed
33.
Becker W, Borst U, Fischbach W, Pasurka B, Schafer R, Borner W. Kinetic data of in-vivo labeled granulocytes in humans with a murine Tc-99m-labelled monoclonal antibody. Eur J Nucl Med 1989;15:361–6.CrossRefPubMed
34.
Reske SN, Karstens JH, Gloeckner W, Steinstrasser A, Schwarz A, Ammon J, et al. Radioimmunoimaging for diagnosis of bone marrow involvement in breast cancer and malignant lymphoma. Lancet 1989;1:299–301.CrossRefPubMed
35.
Munz DL, Voth E, Emrich D. Different approaches to determine the uptake ratio of bone-marrow-seeking radiopharmaceuticals for classifying the scintigraphic bone marrow status. Nuc Compact 1987;18:192–4.
36.
Bonner H. Pathology. Philadelphia: Lippincott; 2009.
37.
Inoue K, Goto R, Okada K, Kinomura S, Fukuda H. A bone marrow F-18 FDG uptake exceeding the liver uptake may indicate bone marrow hyperactivity. Ann Nucl Med 2009;23:643–9.CrossRefPubMed
38.
Sugawara Y, Fisher SJ, Zasadny KR, Kison PV, Baker LH, Wahl RL. Preclinical and clinical studies of bone marrow uptake of fluorine-1-fluorodeoxyglucose with or without granulocyte colony-stimulating factor during chemotherapy. J Clin Oncol 1998;16:173–80.PubMed
39.
Knopp MV, Bischoff H, Rimac A, Oberdorfer F, van Kaick G. Bone marrow uptake of fluorine-18-fluorodeoxyglucose following treatment with hematopoietic growth factors: initial evaluation. Nucl Med Biol 1996;23:845–9.CrossRefPubMed
40.
Basu S, Asopa R, Peshwe H, Mohandas KM. Diffuse intense FDG uptake in the bone marrow in gastrointestinal stromal tumor with coexistent polycythemia rubra vera. Clin Nucl Med 2008;33:782–3.CrossRefPubMed
41.
Quarles van Ufford HM, de Jong JA, Baarslag HJ, de Haas MJ, Oud K, de Klerk JM. FDG PET in a patient with polycythemia vera. Clin Nucl Med 2008;33:780–781CrossRefPubMed
42.
43.
Inoue K, Okada K, Harigae H, Taki Y, Goto R, Kinomura S, et al. Diffuse bone marrow uptake on F-18 FDG PET in patients with myelodysplastic syndromes. Clin Nucl Med 2006;31:721–3.CrossRefPubMed
44.
Cheran SK, Herndon JE, Patz EF Jr. Comparison of whole-body FDG-PET to bone scan for detection of bone metastases in patients with a new diagnosis of lung cancer. Lung Cancer 2004;44:317–25.CrossRefPubMed
45.
Kumar R, Alavi A. Fluorodeoxyglucose-PET in the management of breast cancer. Radiol Clin N Am 2004;42:1113–22.CrossRefPubMed
46.
Kumar R, Maillard I, Schuster SJ, Alavi A. Utility of fluorodeoxyglucose-PET imaging in the management of patients with Hodgkin's and non-Hodgkin's lymphomas. Radiol Clin N Am 2004;42:1083–100.CrossRefPubMed
47.
Mavi A, Lakhani P, Zhuang H, Gupta NC, Alavi A. Fluorodeoxyglucose-PET in characterizing solitary pulmonary nodules, assessing pleural diseases, and the initial staging, restaging, therapy planning, and monitoring response of lung cancer. Radiol Clin N Am 2005;43:1–21.CrossRefPubMed
48.
Moog F, Bangerter M, Kotzerke J, Guhlmann A, Frickhofen N, Reske SN. 18-F-fluorodeoxyglucose-positron emission tomography as a new approach to detect lymphomatous bone marrow. J Clin Oncol 1998;16:603–9.PubMed
49.
Paone G, Itti E, Haioun C, Gaulard P, Dupuis J, Lin C, et al. Bone marrow involvement in diffuse large B-cell lymphoma: correlation between FDG-PET uptake and type of cellular infiltrate. Eur J Nucl Med Mol Imaging 2009;36:745–50.CrossRefPubMed
50.
Salaun PY, Gastinne T, Bodet-Milin C, Campion L, Cambefort P, Moreau A, et al. Analysis of 18F-FDG PET diffuse bone marrow uptake and splenic uptake in staging of Hodgkin's lymphoma: a reflection of disease infiltration or just inflammation? Eur J Nucl Med Mol Imaging 2009;36:1813–21.CrossRefPubMed
51.
Becker S, Becker-Pergola G, Wallwiener D, Solomayer EF, Fehm T. Detection of cytokeratin-positive cells in the bone marrow of breast cancer patients undergoing adjuvant therapy. Breast Cancer Res Treat 2006;97:91–6.CrossRefPubMed
52.
Endo T, Sato N, Koizumi K, Nishio M, Fujimoto K, Sakai T, et al. Localized relapse in bone marrow of extremities after allogeneic stem cell transplantation for acute lymphoblastic leukemia. Am J Hematol 2004;76:279–82.CrossRefPubMed
53.
Nakajo M, Jinnouchi S, Inoue H, Otsuka M, Matsumoto T, Kukita T, et al. FDG PET findings of chronic myeloid leukemia in the chronic phase before and after treatment. Clin Nucl Med 2007;32:775–8.CrossRefPubMed
54.
Jadvar H, Conti PS. Diagnostic utility of FDG PET in multiple myeloma. Skeletal Radiol 2002;31:690–4.CrossRefPubMed
55.
Agool A, Slart RH, Dierckx RA, Kluin PM, Visser L, Jager PL, et al. Somatostatin receptor scintigraphy might be useful for detecting skeleton abnormalities in patients with multiple myeloma and plasmacytoma. Eur J Nucl Med Mol Imaging 2010;37:124–30.CrossRefPubMed
56.
Pace L, Catalano L, Pinto A, De Renzo A, Di Gennaro F, Califano C, et al. Different patterns of technetium-99m sestamibi uptake in multiple myeloma. Eur J Nucl Med 1998;25:714–20.CrossRefPubMed
57.
Fonti R, Salvatore B, Quarantelli M, Sirignano C, Segreto S, Petruzziello F, et al. 18F-FDG PET/CT, 99mTc-MIBI, and MRI in evaluation of patients with multiple myeloma. J Nucl Med 2008;49:195–200.CrossRefPubMed
58.
Shields AF, Grierson JR, Dohmen BM, Machulla HJ, Stayanoff JC, Lawhorn-Crews JM, et al. Imaging proliferation in vivo with [F-18]FLT and positron emission tomography. Nat Med 1998;4:1334–6.CrossRefPubMed
59.
Buck AK, Bommer M, Juweid ME, Glatting G, Stilgenbauer S, Mottaghy FM, et al. First demonstration of leukemia imaging with the proliferation marker 18F-fluorodeoxythymidine. J Nucl Med 2008;49:1756–62.CrossRefPubMed
60.
Agool A, Schot BW, Jager PL, Vellenga E. 18F-FLT PET in hematologic disorders: a novel technique to analyze the bone marrow compartment. J Nucl Med 2006;47:1592–8.PubMed
61.
Woolthuis C, Agool A, Olthof S, Slart RH, Huls G, Smid WM, et al. Auto-SCT induces a phenotypic shift from CMP to GMP progenitors, reduces clonogenic potential and enhances in vitro and in vivo cycling activity defined by (18)F-FLT PET scanning. Bone Marrow Transplant 2010. DOI: 10.​1038/​bmt.​2010.​75
62.
Nunez R, Macapinlac HA, Yeung HW, Akhurst T, Cai S, Osman I, et al. Combined 18F-FDG and 11C-methionine PET scans in patients with newly progressive metastatic prostate cancer. J Nucl Med 2002;43:46–55.PubMed
63.
Dankerl A, Liebisch P, Glatting G, Friesen C, Blumstein NM, Kocot D, et al. Multiple myeloma: molecular imaging with 11C-methionine PET/CT – initial experience. Radiology 2007;242:498–508.CrossRefPubMed
64.
Cimitan M, Bortolus R, Morassut S, Canzonieri V, Garbeglio A, Baresic T, et al. [18F]Fluorocholine PET/CT imaging for the detection of recurrent prostate cancer at PSA relapse: experience in 100 consecutive patients. Eur J Nucl Med Mol Imaging 2006;33:1387–98.CrossRefPubMed
65.
Kwee SA, Thibault GP, Stack RS, Coel MN, Furusato B, Sesterhenn IA. Use of step-section histopathology to evaluate 18F-fluorocholine PET sextant localization of prostate cancer. Mol Imaging 2008;7:12–20.PubMed
66.
Zheng QH, Gardner TA, Raikwar S, Kao C, Stone KL, Martinez TD, et al. [11C]Choline as a PET biomarker for assessment of prostate cancer tumor models. Bioorg Med Chem 2004;12:2887–93.CrossRefPubMed
67.
de Jong IJ, Pruim J, Elsinga PH, Vaalburg W, Mensink HJ. Visualization of prostate cancer with 11C-choline positron emission tomography. Eur Urol 2002;42:18–23.CrossRefPubMed
68.
Shreve P, Chiao PC, Humes HD, Schwaiger M, Gross MD. Carbon-11-acetate PET imaging in renal disease. J Nucl Med 1995;36:1595–601.PubMed
69.
Albrecht S, Buchegger F, Soloviev D, Zaidi H, Vees H, Khan HG, et al. (11)C-Acetate PET in the early evaluation of prostate cancer recurrence. Eur J Nucl Med Mol Imaging 2007;34:185–96.CrossRefPubMed
70.
Ponde DE, Dence CS, Oyama N, Kim J, Tai YC, Laforest R, et al. 18F-Fluoroacetate: a potential acetate analog for prostate tumor imaging – in vivo evaluation of 18F-fluoroacetate versus 11C-acetate. J Nucl Med 2007;48:420–8.PubMed
71.
Souvatzoglou M, Grosu AL, Roper B, Krause BJ, Beck R, Reischl G, et al. Tumour hypoxia imaging with [18F]FAZA PET in head and neck cancer patients: a pilot study. Eur J Nucl Med Mol Imaging 2007;34:1566–75.CrossRefPubMed
72.
73.
Baumann P, Mandl-Weber S, Volkl A, Adam C, Bumeder I, Oduncu F, et al. Dihydroorotate dehydrogenase inhibitor A771726 (leflunomide) induces apoptosis and diminishes proliferation of multiple myeloma cells. Mol Cancer Ther 2009;8:366–75.CrossRefPubMed
74.
Neumaier B, Mottaghy FM, Buck AK, Glatting G, Blumstein NM, Mahren B, et al. (18)F-Immuno-PET: Determination of anti-CD66 biodistribution in a patient with high-risk leukemia. Cancer Biother Radiopharm 2008;23:819–24CrossRefPubMed
75.
Ringhoffer M, Blumstein N, Neumaier B, Glatting G, von Harsdorf S, Buchmann I, et al. 188Re or 90Y-labelled anti-CD66 antibody as part of a dose-reduced conditioning regimen for patients with acute leukaemia or myelodysplastic syndrome over the age of 55: results of a phase I-II study. Br J Haematol 2005;130:604–13.CrossRefPubMed
76.
Nagengast WB, de Vries EG, Hospers GA, Mulder NH, de Jong JR, Hollema H, et al. In vivo VEGF imaging with radiolabeled bevacizumab in a human ovarian tumor xenograft. J Nucl Med 2007;48:1313–9.CrossRefPubMed
77.
de Bont ES, Rosati S, Jacobs S, Kamps WA, Vellenga E. Increased bone marrow vascularization in patients with acute myeloid leukaemia: a possible role for vascular endothelial growth factor. Br J Haematol 2001;113:296–304.CrossRefPubMed
Metadata
Title
Radionuclide imaging of bone marrow disorders
Authors
Ali Agool
Andor W. J. M. Glaudemans
Hendrikus H. Boersma
Rudi A. J. O. Dierckx
Edo Vellenga
Riemer H. J. A. Slart
Publication date
01-01-2011
Publisher
Springer-Verlag
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 1/2011
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-010-1531-0

Other articles of this Issue 1/2011

European Journal of Nuclear Medicine and Molecular Imaging 1/2011 Go to the issue

Editorial Commentary

The flare phenomenon: still learning after 35 years

Focus On...

PET/CT in paediatric oncology: clinical usefulness and dosimetric concerns

Guidelines

EANM Dosimetry Committee guidance document: good practice of clinical dosimetry reporting

Original Article

Post-treatment [18F]FDG maximum standardized uptake value as a prognostic marker of recurrence in endometrial carcinoma

Image of the Month

Don’t blame the bones!

Original Article

18F-Fluoromethylcholine (FCH) PET imaging in patients with castration-resistant prostate cancer: prospective comparison with standard imaging