Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 11/2009

01-11-2009 | Original Article

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?

Authors: Pierre Y. Salaun, Thomas Gastinne, Caroline Bodet-Milin, Loïc Campion, Pierre Cambefort, Anne Moreau, Steven Le Gouill, Christian Berthou, Philippe Moreau, Françoise Kraeber-Bodéré

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 11/2009

Login to get access

Abstract

Purpose

18F-FDG PET has been successfully evaluated in the management of Hodgkin’s lymphoma (HL) and the most recent international guidelines recommended 18F-FDG PET for initial staging and final therapeutic assessment. However, 18F-FDG PET diffuse bone marrow uptake (BMU) and splenic uptake (SU) are frequently observed at the initial imaging and remain difficult to analyse. The aim of this retrospective study was to evaluate the significance of 18F-FDG diffuse BMU and SU in initial staging of HL.

Methods

A total of 106 patients (median age: 31 years, range: 9–81, 51 female, 55 male) underwent 18F-FDG PET/CT for initial staging of HL. BMU level was assessed visually according to liver uptake (1 = below liver uptake, 2 = corresponding to liver uptake, 3 = above liver uptake) and semi-quantitatively using the maximum standardized uptake value (SUVmax) measured in the sacral area. SU was assessed visually according to liver uptake (1 = below liver uptake, 2 = corresponding to liver uptake, 3 = above liver uptake). These data were compared with the patient’s characteristics including sex, age, Ann Arbor staging, bulky disease (tumour burden > 10 cm), presence of B symptoms, bone foci on PET (n = 106), bone marrow involvement (BMI) on biopsy (n = 75), leukocyte count (n = 74), lactic dehydrogenase (LDH) (n = 87), C-reactive protein (CRP) (n = 83) and fibrinogen (n = 60). Univariate and multivariate analyses were performed.

Results

Multivariate analysis found an independent correlation between BMU visual grading and CRP level (p = 0.007). For semi-quantitative BMU evaluation, multivariate analysis found an independent correlation between sacral SUVs and CRP level (p = 0.032) and Ann Arbor stage (p = 0.005). No BMI was found in patients who presented with SUVmax below 3.4. For splenic evaluation, multivariate analysis found an independent correlation between SU and splenic foci (p = 0.034). No statistical link was found between SU and inflammatory markers.

Conclusion

Our study demonstrates that diffuse BMU at initial staging of HL could be due to bone marrow involvement but more likely to bone marrow inflammatory change and that diffuse SU in contrast is probably more associated with disease involvement than with inflammatory change.
Literature
1.
go back to reference Stumpe KD, Urbinelli M, Steinert HC, Glanzmann C, Buck A, von Schulthess GK. Whole-body positron emission tomography using fluorodeoxyglucose for staging of lymphoma: effectiveness and comparison with computed tomography. Eur J Nucl Med 1998;25:721–8. doi:10.1007/s002590050275.CrossRefPubMed Stumpe KD, Urbinelli M, Steinert HC, Glanzmann C, Buck A, von Schulthess GK. Whole-body positron emission tomography using fluorodeoxyglucose for staging of lymphoma: effectiveness and comparison with computed tomography. Eur J Nucl Med 1998;25:721–8. doi:10.​1007/​s002590050275.CrossRefPubMed
2.
go back to reference Buchmann I, Moog F, Schirrmeister H, Reske SN. Positron emission tomography for detection and staging of malignant lymphoma. Recent Results Cancer Res 2000;156:78–89.PubMed Buchmann I, Moog F, Schirrmeister H, Reske SN. Positron emission tomography for detection and staging of malignant lymphoma. Recent Results Cancer Res 2000;156:78–89.PubMed
3.
go back to reference Kostakoglu L, Coleman M, Leonard JP, Kuji I, Zoe H, Goldsmith SJ. PET predicts prognosis after 1 cycle of chemotherapy in aggressive lymphoma and Hodgkin’s disease. J Nucl Med 2002;43:1018–27.PubMed Kostakoglu L, Coleman M, Leonard JP, Kuji I, Zoe H, Goldsmith SJ. PET predicts prognosis after 1 cycle of chemotherapy in aggressive lymphoma and Hodgkin’s disease. J Nucl Med 2002;43:1018–27.PubMed
4.
go back to reference Juweid ME, Stroobants S, Hoekstra OS, Mottaghy FM, Dietlein M, Guermazi A, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol 2007;25:571–8. doi:10.1200/JCO.2006.08.2305.CrossRefPubMed Juweid ME, Stroobants S, Hoekstra OS, Mottaghy FM, Dietlein M, Guermazi A, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol 2007;25:571–8. doi:10.​1200/​JCO.​2006.​08.​2305.CrossRefPubMed
6.
go back to reference Juweid ME. Utility of positron emission tomography (PET) scanning in managing patients with Hodgkin lymphoma. Hematology Am Soc Hematol Educ Program 2006;259–65:510–1. Juweid ME. Utility of positron emission tomography (PET) scanning in managing patients with Hodgkin lymphoma. Hematology Am Soc Hematol Educ Program 2006;259–65:510–1.
7.
go back to reference Carr R, Barrington SF, Madan B, O’Doherty MJ, Saunders CA, van der Walt J, et al. Detection of lymphoma in bone marrow by whole-body positron emission tomography. Blood 1998;91:3340–6.PubMed Carr R, Barrington SF, Madan B, O’Doherty MJ, Saunders CA, van der Walt J, et al. Detection of lymphoma in bone marrow by whole-body positron emission tomography. Blood 1998;91:3340–6.PubMed
8.
go back to reference 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 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
9.
go back to reference Pakos EE, Fotopoulos AD, Ioannidis JP. 18F-FDG PET for evaluation of bone marrow infiltration in staging of lymphoma: a meta-analysis. J Nucl Med 2005;46:958–63.PubMed Pakos EE, Fotopoulos AD, Ioannidis JP. 18F-FDG PET for evaluation of bone marrow infiltration in staging of lymphoma: a meta-analysis. J Nucl Med 2005;46:958–63.PubMed
10.
11.
go back to reference 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 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
12.
go back to reference Brunning RD, Bloomfield CD, McKenna RW, Peterson L. Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic disease. Ann Intern Med 1975;82:365–6.PubMed Brunning RD, Bloomfield CD, McKenna RW, Peterson L. Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic disease. Ann Intern Med 1975;82:365–6.PubMed
13.
go back to reference Ebie N, Loew JM, Gregory SA. Bilateral trephine bone marrow biopsy for staging non-Hodgkin’s lymphoma—a second look. Hematol Pathol 1989;3:29–33.PubMed Ebie N, Loew JM, Gregory SA. Bilateral trephine bone marrow biopsy for staging non-Hodgkin’s lymphoma—a second look. Hematol Pathol 1989;3:29–33.PubMed
14.
go back to reference Haddy TB, Parker RI, Magrath IT. Bone marrow involvement in young patients with non-Hodgkin’s lymphoma: the importance of multiple bone marrow samples for accurate staging. Med Pediatr Oncol 1989;17:418–23.PubMedCrossRef Haddy TB, Parker RI, Magrath IT. Bone marrow involvement in young patients with non-Hodgkin’s lymphoma: the importance of multiple bone marrow samples for accurate staging. Med Pediatr Oncol 1989;17:418–23.PubMedCrossRef
16.
go back to reference Okada J, Yoshikawa K, Imazeki K, Minoshima S, Uno K, Itami J, et al. The use of FDG-PET in the detection and management of malignant lymphoma: correlation of uptake with prognosis. J Nucl Med 1991;32:686–91.PubMed Okada J, Yoshikawa K, Imazeki K, Minoshima S, Uno K, Itami J, et al. The use of FDG-PET in the detection and management of malignant lymphoma: correlation of uptake with prognosis. J Nucl Med 1991;32:686–91.PubMed
17.
go back to reference Hoh CK, Glaspy J, Rosen P, Dahlbom M, Lee SJ, Kunkel L, et al. Whole-body FDG-PET imaging for staging of Hodgkin’s disease and lymphoma. J Nucl Med 1997;38:343–8.PubMed Hoh CK, Glaspy J, Rosen P, Dahlbom M, Lee SJ, Kunkel L, et al. Whole-body FDG-PET imaging for staging of Hodgkin’s disease and lymphoma. J Nucl Med 1997;38:343–8.PubMed
21.
go back to reference Luoni M, Declich P, De Paoli A, Fava S, Marinoni P, Montalbetti L, et al. Bone marrow biopsy for the staging of non-Hodgkin’s lymphoma: bilateral or unilateral trephine biopsy? Tumori 1995;81:410–3.PubMed Luoni M, Declich P, De Paoli A, Fava S, Marinoni P, Montalbetti L, et al. Bone marrow biopsy for the staging of non-Hodgkin’s lymphoma: bilateral or unilateral trephine biopsy? Tumori 1995;81:410–3.PubMed
22.
go back to reference Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer 2002;94:1522–31. doi:10.1002/cncr.10364.CrossRefPubMed Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer 2002;94:1522–31. doi:10.​1002/​cncr.​10364.CrossRefPubMed
23.
go back to reference Ribrag V, Vanel D, Leboulleux S, Lumbroso J, Couanet D, Bonniaud G, 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;66:325–31. doi:10.1016/j.ejrad.2007.06.014.CrossRefPubMed Ribrag V, Vanel D, Leboulleux S, Lumbroso J, Couanet D, Bonniaud G, 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;66:325–31. doi:10.​1016/​j.​ejrad.​2007.​06.​014.CrossRefPubMed
24.
go back to reference Newman JS, Francis IR, Kaminski MS, Wahl RL. Imaging of lymphoma with PET with 2-[F-18]-fluoro-2-deoxy-D-glucose: correlation with CT. Radiology 1994;190:111–6.PubMed Newman JS, Francis IR, Kaminski MS, Wahl RL. Imaging of lymphoma with PET with 2-[F-18]-fluoro-2-deoxy-D-glucose: correlation with CT. Radiology 1994;190:111–6.PubMed
26.
go back to reference Zielinski CC, Preis P, Aiginger P, Eibl MM. Acute-phase-proteins and parameters of humoral immunity in patients with advanced Hodgkin’s disease. J Cancer Res Clin Oncol 1985;110:65–70. doi:10.1007/BF00402504.CrossRefPubMed Zielinski CC, Preis P, Aiginger P, Eibl MM. Acute-phase-proteins and parameters of humoral immunity in patients with advanced Hodgkin’s disease. J Cancer Res Clin Oncol 1985;110:65–70. doi:10.​1007/​BF00402504.CrossRefPubMed
27.
go back to reference Axdorph U, Sjöberg J, Grimfors G, Landgren O, Porwit-MacDonald A, Björkholm M. Biological markers may add to prediction of outcome achieved by the International Prognostic Score in Hodgkin’s disease. Ann Oncol 2000;11:1405–11. doi:10.1023/A:1026551727795.CrossRefPubMed Axdorph U, Sjöberg J, Grimfors G, Landgren O, Porwit-MacDonald A, Björkholm M. Biological markers may add to prediction of outcome achieved by the International Prognostic Score in Hodgkin’s disease. Ann Oncol 2000;11:1405–11. doi:10.​1023/​A:​1026551727795.CrossRefPubMed
28.
go back to reference Núñez R, Rini JN, Tronco GG, Tomas MB, Nichols K, Palestro CJ. Correlation of hematologic parameters with bone marrow and spleen uptake in FDG PET [in Spanish]. Rev Esp Med Nucl 2005;24:107–12. doi:10.1157/13071686.CrossRefPubMed Núñez R, Rini JN, Tronco GG, Tomas MB, Nichols K, Palestro CJ. Correlation of hematologic parameters with bone marrow and spleen uptake in FDG PET [in Spanish]. Rev Esp Med Nucl 2005;24:107–12. doi:10.​1157/​13071686.CrossRefPubMed
29.
go back to reference Rueffer U, Sieber M, Josting A, Breuer K, Grotenhermen F, Bredenfeld H, et al. Prognostic factors for subdiaphragmatic involvement in clinical stage I-II supradiaphragmatic Hodgkin’s disease: a retrospective analysis of the GHSG. Ann Oncol 1999;10:1343–8. doi:10.1023/A:1008377629280.CrossRefPubMed Rueffer U, Sieber M, Josting A, Breuer K, Grotenhermen F, Bredenfeld H, et al. Prognostic factors for subdiaphragmatic involvement in clinical stage I-II supradiaphragmatic Hodgkin’s disease: a retrospective analysis of the GHSG. Ann Oncol 1999;10:1343–8. doi:10.​1023/​A:​1008377629280.CrossRefPubMed
30.
go back to reference Trotter MC, Cloud GA, Davis M, Sanford SP, Urist MM, Soong SJ, et al. Predicting the risk of abdominal disease in Hodgkin’s lymphoma. A multifactorial analysis of staging laparotomy results in 255 patients. Ann Surg 1985;201:465–9.CrossRefPubMed Trotter MC, Cloud GA, Davis M, Sanford SP, Urist MM, Soong SJ, et al. Predicting the risk of abdominal disease in Hodgkin’s lymphoma. A multifactorial analysis of staging laparotomy results in 255 patients. Ann Surg 1985;201:465–9.CrossRefPubMed
34.
go back to reference Plat M, Erk JU. Abdominal ultrasound diagnosis of malignant lymphomas [in German]. Gastroenterol J 1990;50:117–23.PubMed Plat M, Erk JU. Abdominal ultrasound diagnosis of malignant lymphomas [in German]. Gastroenterol J 1990;50:117–23.PubMed
36.
go back to reference Hancock SL, Scidmore NS, Hopkins KL, Cox RS, Bergin CJ. Computed tomography assessment of splenic size as a predictor of splenic weight and disease involvement in laparotomy staged Hodgkin’s disease. Int J Radiat Oncol Biol Phys 1994;28:93–9.PubMed Hancock SL, Scidmore NS, Hopkins KL, Cox RS, Bergin CJ. Computed tomography assessment of splenic size as a predictor of splenic weight and disease involvement in laparotomy staged Hodgkin’s disease. Int J Radiat Oncol Biol Phys 1994;28:93–9.PubMed
Metadata
Title
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?
Authors
Pierre Y. Salaun
Thomas Gastinne
Caroline Bodet-Milin
Loïc Campion
Pierre Cambefort
Anne Moreau
Steven Le Gouill
Christian Berthou
Philippe Moreau
Françoise Kraeber-Bodéré
Publication date
01-11-2009
Publisher
Springer-Verlag
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 11/2009
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-009-1183-0

Other articles of this Issue 11/2009

European Journal of Nuclear Medicine and Molecular Imaging 11/2009 Go to the issue