Skip to main content
SpringerLink
Log in

Characterizing bone marrow involvement in Hodgkin’s lymphoma by FDG-PET/CT

  • Original Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

Fluoro-deoxyglucose positron emmission tomography combined with computed tomography (FDG-PET/CT) is superior to iliac bone marrow biopsy (iBMB) for detection of bone marrow involvement (BMI) in staging of Hodgkin’s lymphoma (HL). The present study aims to characterize the patterns and distribution of BMI in HL as determined by FDG-PET/CT.

Methods

Reports of FDG-PET/CT studies performed for staging of HL were reviewed. BMI was defined as positive iBMB and/or foci of pathological FDG uptake in the skeleton that behaved in concordance with other sites of lymphoma in studies following chemotherapy. Number of FDG uptake foci, their specific location in the skeleton and the presence of corresponding lesions in the CT component of the study, and stage according to the Ann Arbor staging system, were recorded.

Results

The study included 473 patients. iBMB was performed in 336 patients. Nine patients had positive iBMB (9/336, 3 %). Seventy-three patients (73/473, 15 %) had FDG-PET/CT-defined BMI. The BM was the only extranodal site of HL in 52/473 patients (11 %). Forty-five patients had three or more foci of pathological skeletal FDG uptake (45/73, 62 %). Sixty-four patients (64/73, 88 %) had at least one uptake focus in the pelvis or vertebrae. In 60 patients (60/73, 82 %), the number of skeletal FDG uptake foci without corresponding CT lesions was equal to or higher than the number of foci with morphological abnormalities.

Conclusion

FDG-PET/CT demonstrated BMI in 15 % of patients with newly diagnosed HL. Diagnosis of BMI in HL by FDG-PET/CT was more sensitive than iBMB with potential upstage in 11 % of patients. The most common pattern of FDG-PET/CT BMI was multifocal (at least three foci) skeletal FDG uptake, with at least one focus in the pelvis or vertebrae and no corresponding CT lesions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Diehl V. Hodgkin’s disease–from pathology specimen to cure. N Engl J Med. 2007;357:1968–71.

    Article  CAS  PubMed  Google Scholar 

  2. Howlader N NA, Krapcho M, Garshell J, Neyman N, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds). National Cancer Institute. Bethesda, MD, . SEER Cancer Statistics Review, 1975–2010. p. based on November 2012 SEER data submission, posted to the SEER web site, http://seer.cancer.gov/csr/1975_2010/.

  3. Skoetz N, Trelle S, Rancea M, Haverkamp H, Diehl V, Engert A, et al. Effect of initial treatment strategy on survival of patients with advanced-stage Hodgkin’s lymphoma: a systematic review and network meta-analysis. Lancet Oncol. 2013;14:943–52.

    Article  PubMed  Google Scholar 

  4. Fletcher JW, Djulbegovic B, Soares HP, Siegel BA, Lowe VJ, Lyman GH, et al. Recommendations on the use of 18F-FDG PET in oncology. J Nucl Med. 2008;49:480–508.

    Article  PubMed  Google Scholar 

  5. NCCN Clinical Practice Guidelines in Oncology™ Hodgkin Lymphoma v.1.2013. National Comprehensive Cancer Network; 2013. http://www.nccn.org/professionals/physician_gls/PDF/hodgkins.

  6. 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.

    Article  PubMed  Google Scholar 

  7. Barekman CL, Fair KP, Cotelingam JD. Comparative utility of diagnostic bone-marrow components: a 10-year study. Am J Hematol. 1997;56:37–41.

    Article  CAS  PubMed  Google Scholar 

  8. Brunning RD, Bloomfield CD, McKenna RW, Peterson LA. Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic diseases. Ann Intern Med. 1975;82:365–6.

    Article  CAS  PubMed  Google Scholar 

  9. Shields AF, Porter BA, Churchley S, Olson DO, Appelbaum FR, Thomas ED. The detection of bone marrow involvement by lymphoma using magnetic resonance imaging. J Clin Oncol. 1987;5:225–30.

    CAS  PubMed  Google Scholar 

  10. Linden A, Zankovich R, Theissen P, Diehl V, Schicha H. Malignant lymphoma: bone marrow imaging versus biopsy. Radiology. 1989;173:335–9.

    CAS  PubMed  Google Scholar 

  11. Hoane BR, Shields AF, Porter BA, Shulman HM. Detection of lymphomatous bone marrow involvement with magnetic resonance imaging. Blood. 1991;78:728–38.

    CAS  PubMed  Google Scholar 

  12. Altehoefer C, Blum U, Bathmann J, Wustenberg C, Uhrmeister P, Laubenberger J, et al. Comparative diagnostic accuracy of magnetic resonance imaging and immunoscintigraphy for detection of bone marrow involvement in patients with malignant lymphoma. J Clin Oncol. 1997;15:1754–60.

    CAS  PubMed  Google Scholar 

  13. Eichenauer DA, Engert A, Dreyling M. Hodgkin’s lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2011;22 Suppl 6:vi55–8.

    PubMed  Google Scholar 

  14. Munker R, Hasenclever D, Brosteanu O, Hiller E, Diehl V. Bone marrow involvement in Hodgkin’s disease: an analysis of 135 consecutive cases. German Hodgkin’s Lymphoma Study Group. J Clin Oncol. 1995;13:403–9.

    CAS  PubMed  Google Scholar 

  15. Howell SJ, Grey M, Chang J, Morgenstern GR, Cowan RA, Deakin DP, et al. The value of bone marrow examination in the staging of Hodgkin’s lymphoma: a review of 955 cases seen in a regional cancer centre. Br J Haematol. 2002;119:408–11.

    Article  PubMed  Google Scholar 

  16. Eichenauer DA, Engert A, Diehl V. Hodgkin lymphoma: clinical manifestation, staging, and therapy. In: Hoffman R, Benz EJ, Silberstein LE, Heslop H, Weitz J, Anastasi J, editors. Hematology, Basic Principles and Practice. Philadelphia: Elsevier Saunders; 2013. p. 1138–56.

  17. National Cancer Institute: PDQ® Adult Hodgkin Lymphoma Treatment. Retrieved 18/08/2013, from http://www.cancer.gov/cancertopics/pdq/treatment/adulthodgkins/HealthProfessional/page3.

  18. Moog F, Bangerter M, Diederichs CG, Guhlmann A, Kotzerke J, Merkle E, et al. Lymphoma: role of whole-body 2-deoxy-2-[F-18]fluoro-D-glucose (FDG) PET in nodal staging. Radiology. 1997;203:795–800.

    CAS  PubMed  Google Scholar 

  19. Munker R, Glass J, Griffeth LK, Sattar T, Zamani R, Heldmann M, et al. Contribution of PET imaging to the initial staging and prognosis of patients with Hodgkin’s disease. Ann Oncol. 2004;15:1699–704.

    Article  CAS  PubMed  Google Scholar 

  20. Isasi CR, Lu P, Blaufox MD. A metaanalysis of 18F-2-deoxy-2-fluoro-D-glucose positron emission tomography in the staging and restaging of patients with lymphoma. Cancer. 2005;104:1066–74.

    Article  PubMed  Google Scholar 

  21. Weiler-Sagie M, Bushelev O, Epelbaum R, Dann EJ, Haim N, Avivi I, et al. (18)F-FDG avidity in lymphoma readdressed: a study of 766 patients. J Nucl Med. 2010;51:25–30.

    Article  PubMed  Google Scholar 

  22. Purz S, Mauz-Korholz C, Korholz D, Hasenclever D, Krausse A, Sorge I, et al. [18F]Fluorodeoxyglucose positron emission tomography for detection of bone marrow involvement in children and adolescents with Hodgkin’s lymphoma. J Clin Oncol. 2011;29:3523–8.

    Article  PubMed  Google Scholar 

  23. 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.

    CAS  PubMed  Google Scholar 

  24. Kabickova E, Sumerauer D, Cumlivska E, Drahokoupilova E, Nekolna M, Chanova M, et al. Comparison of 18F-FDG-PET and standard procedures for the pretreatment staging of children and adolescents with Hodgkin’s disease. Eur J Nucl Med Mol Imaging. 2006;33:1025–31.

    Article  PubMed  Google Scholar 

  25. Schaefer NG, Strobel K, Taverna C, Hany TF. Bone involvement in patients with lymphoma: the role of FDG-PET/CT. Eur J Nucl Med Mol Imaging. 2007;34:60–7.

    Article  PubMed  Google Scholar 

  26. 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.

    Article  PubMed  Google Scholar 

  27. Cerci JJ, Pracchia LF, Soares Junior J, Linardi Cda C, Meneghetti JC, Buccheri V. Positron emission tomography with 2-[18F]-fluoro-2-deoxy-D-glucose for initial staging of hodgkin lymphoma: a single center experience in Brazil. Clinics (Sao Paulo). 2009;64:491–8.

    Article  Google Scholar 

  28. Moulin-Romsee G, Hindie E, Cuenca X, Brice P, Decaudin D, Benamor M, et al. (18)F-FDG PET/CT bone/bone marrow findings in Hodgkin’s lymphoma may circumvent the use of bone marrow trephine biopsy at diagnosis staging. Eur J Nucl Med Mol Imaging. 2010;37:1095–105.

    Article  PubMed  Google Scholar 

  29. El-Galaly TC, d’Amore F, Mylam KJ, de Nully Brown P, Bogsted M, Bukh A, et al. Routine bone marrow biopsy has little or no therapeutic consequence for positron emission tomography/computed tomography-staged treatment-naive patients with Hodgkin lymphoma. J Clin Oncol. 2012;30:4508–14.

    Article  PubMed  Google Scholar 

  30. 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.

    Article  PubMed  Google Scholar 

  31. Paes FM, Kalkanis DG, Sideras PA, Serafini AN. FDG PET/CT of extranodal involvement in non-Hodgkin lymphoma and Hodgkin disease. Radiographics. 2010;30:269–91.

    Article  PubMed  Google Scholar 

  32. 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.

    Article  PubMed  Google Scholar 

  33. Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. Report of the Committee on Hodgkin’s Disease Staging Classification. Cancer Res. 1971;31:1860–1.

    CAS  PubMed  Google Scholar 

  34. Lister TA, Crowther D, Sutcliffe SB, Glatstein E, Canellos GP, Young RC, et al. Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin’s disease: Cotswolds meeting. J Clin Oncol. 1989;7:1630–6.

    CAS  PubMed  Google Scholar 

  35. Cheng G, Chen W, Chamroonrat W, Torigian DA, Zhuang H, Alavi A. Biopsy versus FDG PET/CT in the initial evaluation of bone marrow involvement in pediatric lymphoma patients. Eur J Nucl Med Mol Imaging. 2011;38:1469–76.

    Article  PubMed  Google Scholar 

  36. Muzahir S, Mian M, Munir I, Nawaz MK, Faruqui ZS, Mufti KA, et al. Clinical utility of (1)(8)F FDG-PET/CT in the detection of bone marrow disease in Hodgkin’s lymphoma. Br J Radiol. 2012;85:e490–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Kricun ME. Red-yellow marrow conversion: its effect on the location of some solitary bone lesions. Skeletal Radiol. 1985;14:10–9.

    Article  CAS  PubMed  Google Scholar 

  38. Vanel D, Husband JE, Padhani AR. Bone metastases. In: Husband JE, Reznek RH, editors. Imaging in Oncology. 2 ed. London: Taylor & Francis; 2004. p. 1041–58.

  39. Delbeke D, Coleman RE, Guiberteau MJ, Brown ML, Royal HD, Siegel BA, et al. Procedure guideline for tumor imaging with 18F-FDG PET/CT 1.0. J Nucl Med. 2006;47:885–95.

    PubMed  Google Scholar 

  40. Stauss J, Franzius C, Pfluger T, Juergens KU, Biassoni L, Begent J, et al. Guidelines for 18F-FDG PET and PET-CT imaging in paediatric oncology. Eur J Nucl Med Mol Imaging. 2008;35:1581–8.

    Article  CAS  PubMed  Google Scholar 

  41. Boellaard R, O’Doherty MJ, Weber WA, Mottaghy FM, Lonsdale MN, Stroobants SG, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37:181–200.

    Article  PubMed Central  PubMed  Google Scholar 

  42. Aoki J, Watanabe H, Shinozaki T, Takagishi K, Ishijima H, Oya N, et al. FDG PET of primary benign and malignant bone tumors: standardized uptake value in 52 lesions. Radiology. 2001;219:774–7.

    Article  CAS  PubMed  Google Scholar 

  43. Nakamoto Y, Cohade C, Tatsumi M, Hammoud D, Wahl RL. CT appearance of bone metastases detected with FDG PET as part of the same PET/CT examination. Radiology. 2005;237:627–34.

    Article  PubMed  Google Scholar 

  44. Metser U, Even-Sapir E. Increased (18)F-fluorodeoxyglucose uptake in benign, nonphysiologic lesions found on whole-body positron emission tomography/computed tomography (PET/CT): accumulated data from four years of experience with PET/CT. Semin Nucl Med. 2007;37:206–22.

    Article  PubMed  Google Scholar 

  45. Costelloe CM, Murphy Jr WA, Chasen BA. Musculoskeletal pitfalls in 18F-FDG PET/CT: pictorial review. AJR Am J Roentgenol. 2009;193:WS1–13. Quiz S26-30.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Drs. Daniela Militianu and Saher Srour from the radiology department for their continuing support and advice.

Conflicts of interest

None

Author information

Authors and Affiliations

  1. Nuclear Medicine Department, Rambam Health Care Campus, Haifa, Israel

    Michal Weiler-Sagie & Olga Kagna

  2. Hematology Department, Rambam Health Care Campus and B. & R. Rappaport Faculty of Medicine, Technion, Haifa, Israel

    Eldad J. Dann

  3. Pediatric Hemato-Oncology Department, Rambam Health Care Campus and B. & R. Rappaport Faculty of Medicine, Technion, Haifa, Israel

    Ayelet Ben-Barak

  4. Nuclear Medicine Department, Rambam Health Care Campus and B. & R. Rappaport Faculty of Medicine, Technion, Haifa, Israel

    Ora Israel

Authors
  1. Michal Weiler-Sagie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olga Kagna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eldad J. Dann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ayelet Ben-Barak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ora Israel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michal Weiler-Sagie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weiler-Sagie, M., Kagna, O., Dann, E.J. et al. Characterizing bone marrow involvement in Hodgkin’s lymphoma by FDG-PET/CT. Eur J Nucl Med Mol Imaging 41, 1133–1140 (2014). https://doi.org/10.1007/s00259-014-2706-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00259-014-2706-x

Keywords

Search

Navigation