18F-FDG PET/CT bone/bone marrow findings in Hodgkin’s lymphoma may circumvent the use of bone marrow trephine biopsy at diagnosis staging

  • Gerard Moulin-Romsee
  • Elif Hindié
  • Xavier Cuenca
  • Pauline Brice
  • Didier Decaudin
  • Myriam Bénamor
  • Josette Brière
  • Marcela Anitei
  • Jean-Emmanuel Filmont
  • David Sibon
  • Eric de Kerviler
  • Jean-Luc Moretti
Original Article



Accurate staging of Hodgkin’s lymphoma (HL) is necessary in selecting appropriate treatment. Bone marrow trephine biopsy (BMB) is the standard procedure for depicting bone marrow involvement. BMB is invasive and explores a limited part of the bone marrow. 18F-FDG PET/CT is now widely used for assessing response to therapy in HL and a baseline study is obtained to improve accuracy. The aim of this retrospective analysis was to assess whether routine BMB remains necessary with concomitant 18F-FDG PET/CT.


Data from 83 patients (newly diagnosed HL) were reviewed. All patients had received contrast-enhanced CT, BMB and 18F-FDG PET/CT. Results of BMB were not available at the time of 18F-FDG PET/CT imaging.


Seven patients had lymphomatous involvement on BMB. Four patients had bone involvement on conventional CT (two with negative BMB). All patients with bone marrow and/or bone lesions at conventional staging were also diagnosed on 18F-FDG PET/CT scan. PET/CT depicted FDG-avid bone/bone marrow foci in nine additional patients. Four of them had only one or two foci, while the other had multiple foci. However, the iliac crest, site of the BMB, was not involved on 18F-FDG PET/CT. Osteolytic/sclerotic lesions matching FDG-avid foci were visible on the CT part of PET/CT in three patients. MRI ordered in three other patients suggested bone marrow involvement. Interim and/or end-therapy 18F-FDG PET/CT documented response of FDG-avid bone/bone marrow foci to chemotherapy in every patient.


18F-FDG PET/CT highly improves sensitivity for diagnosis of bone/bone marrow lesions in HL compared to conventional staging.


Hodgkin’s lymphoma PET/CT 18F-FDG Bone marrow trephine biopsy Staging 


  1. 1.
    Diehl V. Hodgkin’s disease–from pathology specimen to cure. N Engl J Med 2007;357(19):1968–71.CrossRefPubMedGoogle Scholar
  2. 2.
    Brice P, Bastion Y, Divine M, Nedellec G, Ferrant A, Gabarre J, et al. Analysis of prognostic factors after the first relapse of Hodgkin’s disease in 187 patients. Cancer 1996;78(6):1293–9.CrossRefPubMedGoogle Scholar
  3. 3.
    Moskowitz CH, Nimer SD, Zelenetz AD, Trippett T, Hedrick EE, Filippa DA, et al. A 2-step comprehensive high-dose chemoradiotherapy second-line program for relapsed and refractory Hodgkin disease: analysis by intent to treat and development of a prognostic model. Blood 2001;97(3):616–23.CrossRefPubMedGoogle Scholar
  4. 4.
    Josting A, Franklin J, May M, Koch P, Beykirch MK, Heinz J, et al. New prognostic score based on treatment outcome of patients with relapsed Hodgkin’s lymphoma registered in the database of the German Hodgkin’s lymphoma study group. J Clin Oncol 2002;20(1):221–30.CrossRefPubMedGoogle Scholar
  5. 5.
    Brice P. Managing relapsed and refractory Hodgkin lymphoma. Br J Haematol 2008;141(1):3–13.CrossRefPubMedGoogle Scholar
  6. 6.
    Eghbali H, Raemaekers J, Carde P, EORTC Lymphoma Group. The EORTC strategy in the treatment of Hodgkin’s lymphoma. Eur J Haematol Suppl 2005 Jul;(66):135–40.Google Scholar
  7. 7.
    Connors JM. State-of-the-art therapeutics: Hodgkin’s lymphoma. J Clin Oncol 2005;23(26):6400–8.CrossRefPubMedGoogle Scholar
  8. 8.
    Diehl V, Fuchs M. Early, intermediate and advanced Hodgkin’s lymphoma: modern treatment strategies. Ann Oncol 2007;18 Suppl 9:ix71–9.CrossRefPubMedGoogle Scholar
  9. 9.
    Favier O, Heutte N, Stamatoullas-Bastard A, Carde P, Van’t Veer MB, Aleman BM, et al. Survival after Hodgkin lymphoma: causes of death and excess mortality in patients treated in 8 consecutive trials. Cancer 2009;115(8):1680–91.CrossRefPubMedGoogle Scholar
  10. 10.
    Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. Report of the Committee on Hodgkin’s Disease Staging Classification. Cancer Res 1971;31(11):1860–1.PubMedGoogle Scholar
  11. 11.
    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(11):1630–6. Erratum in: J Clin Oncol 1990 Sep;8(9):1602.PubMedGoogle Scholar
  12. 12.
    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(2):408–11.CrossRefPubMedGoogle Scholar
  13. 13.
    Vassilakopoulos TP, Angelopoulou MK, Constantinou N, Karmiris T, Repoussis P, Roussou P, et al. Development and validation of a clinical prediction rule for bone marrow involvement in patients with Hodgkin lymphoma. Blood 2005;105(5):1875–80.CrossRefPubMedGoogle Scholar
  14. 14.
    Brusamolino E, Bacigalupo A, Barosi G, Biti G, Gobbi PG, Levis A, et al. Classical Hodgkin’s lymphoma in adults: guidelines of the Italian Society of Hematology, the Italian Society of Experimental Hematology, and the Italian Group for Bone Marrow Transplantation on initial work-up, management, and follow-up. Haematologica 2009;94(4):550–65.CrossRefPubMedGoogle Scholar
  15. 15.
    Hasenclever D, Diehl V. A prognostic score for advanced Hodgkin’s disease. International Prognostic Factors Project on Advanced Hodgkin’s Disease. N Engl J Med 1998;339(21):1506–14.CrossRefPubMedGoogle Scholar
  16. 16.
    Spaepen K, Stroobants S, Dupont P, Thomas J, Vandenberghe P, Balzarini J, et al. Can positron emission tomography with [(18)F]-fluorodeoxyglucose after first-line treatment distinguish Hodgkin’s disease patients who need additional therapy from others in whom additional therapy would mean avoidable toxicity? Br J Haematol 2001;115(2):272–8.CrossRefPubMedGoogle Scholar
  17. 17.
    Weihrauch MR, Re D, Scheidhauer K, Ansén S, Dietlein M, Bischoff S, et al. Thoracic positron emission tomography using 18F-fluorodeoxyglucose for the evaluation of residual mediastinal Hodgkin disease. Blood 2001;98(10):2930–4.CrossRefPubMedGoogle Scholar
  18. 18.
    Cheson BD, Pfistner B, Juweid ME, Gascoyne RD, Specht L, Horning SJ, et al. Revised response criteria for malignant lymphoma. J Clin Oncol 2007;25(5):579–86.CrossRefPubMedGoogle Scholar
  19. 19.
    Hutchings M, Mikhaeel NG, Fields PA, Nunan T, Timothy AR. Prognostic value of interim FDG-PET after two or three cycles of chemotherapy in Hodgkin lymphoma. Ann Oncol 2005;16(7):1160–8.CrossRefPubMedGoogle Scholar
  20. 20.
    Hutchings M, Loft A, Hansen M, Pedersen LM, Buhl T, Jurlander J, et al. FDG-PET after two cycles of chemotherapy predicts treatment failure and progression-free survival in Hodgkin lymphoma. Blood 2006;107(1):52–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Kostakoglu L, Goldsmith SJ, Leonard JP, Christos P, Furman RR, Atasever T, et al. FDG-PET after 1 cycle of therapy predicts outcome in diffuse large cell lymphoma and classic Hodgkin disease. Cancer 2006;107(11):2678–87.CrossRefPubMedGoogle Scholar
  22. 22.
    Zinzani PL, Tani M, Fanti S, Alinari L, Musuraca G, Marchi E, et al. Early positron emission tomography (PET) restaging: a predictive final response in Hodgkin’s disease patients. Ann Oncol 2006;17(8):1296–300.CrossRefPubMedGoogle Scholar
  23. 23.
    Gallamini A, Hutchings M, Rigacci L, Specht L, Merli F, Hansen M, et al. Early interim 2-[18F]fluoro-2-deoxy-D-glucose positron emission tomography is prognostically superior to international prognostic score in advanced-stage Hodgkin’s lymphoma: a report from a joint Italian-Danish study. J Clin Oncol 2007;25(24):3746–52.CrossRefPubMedGoogle Scholar
  24. 24.
    Furth C, Steffen IG, Amthauer H, Ruf J, Misch D, Schönberger S, et al. Early and late therapy response assessment with [18F]fluorodeoxyglucose positron emission tomography in pediatric Hodgkin’s lymphoma: analysis of a prospective multicenter trial. J Clin Oncol 2009;27(26):4385–91.CrossRefPubMedGoogle Scholar
  25. 25.
    Terasawa T, Lau J, Bardet S, Couturier O, Hotta T, Hutchings M, et al. Fluorine-18-fluorodeoxyglucose positron emission tomography for interim response assessment of advanced-stage Hodgkin’s lymphoma and diffuse large B-cell lymphoma: a systematic review. J Clin Oncol 2009;27(11):1906–14.CrossRefPubMedGoogle Scholar
  26. 26.
    Hutchings M, Loft A, Hansen M, Pedersen LM, Berthelsen AK, Keiding S, et al. Positron emission tomography with or without computed tomography in the primary staging of Hodgkin’s lymphoma. Haematologica 2006;91(4):482–9.PubMedGoogle Scholar
  27. 27.
    Girinsky T, Specht L, Ghalibafian M, Edeline V, Bonniaud G, Van Der Maazen R, et al. The conundrum of Hodgkin lymphoma nodes: to be or not to be included in the involved node radiation fields. The EORTC-GELA lymphoma group guidelines. Radiother Oncol 2008;88(2):202–10.CrossRefPubMedGoogle Scholar
  28. 28.
    Townsend DW. Positron emission tomography/computed tomography. Semin Nucl Med 2008;38(3):152–66.CrossRefPubMedGoogle Scholar
  29. 29.
    Fend F, Kremer M. Diagnosis and classification of malignant lymphoma and related entities in the bone marrow trephine biopsy. Pathobiology 2007;74(2):133–43.CrossRefPubMedGoogle Scholar
  30. 30.
    Kwee TC, Kwee RM, Verdonck LF, Bierings MB, Nievelstein RA. Magnetic resonance imaging for the detection of bone marrow involvement in malignant lymphoma. Br J Haematol 2008;141(1):60–8.CrossRefPubMedGoogle Scholar
  31. 31.
    Hutchings M, Loft A, Hansen M, Ralfkiaer E, Specht L. Different histopathological subtypes of Hodgkin lymphoma show significantly different levels of FDG uptake. Hematol Oncol 2006;24(3):146–50.CrossRefPubMedGoogle Scholar
  32. 32.
    Küppers R. The biology of Hodgkin’s lymphoma. Nat Rev Cancer 2009;9(1):15–27.CrossRefPubMedGoogle Scholar
  33. 33.
    Munker R, Hasenclever D, Brosteanu O, Hiller E, Diehl V. Bone marrow involvement in Hodgkin’ disease: an analysis of 135 consecutive cases. German Hodgkin’s Lymphoma Study Group. J Clin Oncol 1995;13(2):403–9.PubMedGoogle Scholar
  34. 34.
    Brunning RD, Bloomfield CD, McKenna RW, Peterson LA. Bilateral trephine bone marrow biopsies in lymphoma and other neoplastic diseases. Ann Intern Med 1975;82(3):365–6.PubMedGoogle Scholar
  35. 35.
    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(5):1522–31.CrossRefPubMedGoogle Scholar
  36. 36.
    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(9):3340–6.PubMedGoogle Scholar
  37. 37.
    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(6):958–63.PubMedGoogle Scholar
  38. 38.
    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.Google Scholar
  39. 39.
    Bain BJ. Bone marrow biopsy morbidity and mortality: 2002 data. Clin Lab Haematol 2004;26(5):315–8.CrossRefPubMedGoogle Scholar
  40. 40.
    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(11):1699–704.CrossRefPubMedGoogle Scholar
  41. 41.
    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(9):1025–31.CrossRefPubMedGoogle Scholar
  42. 42.
    Rigacci L, Vitolo U, Nassi L, Merli F, Gallamini A, Pregno P, et al. Positron emission tomography in the staging of patients with Hodgkin’s lymphoma. A prospective multicentric study by the Intergruppo Italiano Linfomi. Ann Hematol 2007;86(12):897–903.CrossRefPubMedGoogle Scholar
  43. 43.
    Pelosi E, Penna D, Deandreis D, Chiappella A, Skanjeti A, Vitolo U, et al. FDG-PET in the detection of bone marrow disease in Hodgkin’s disease and aggressive non-Hodgkin’s lymphoma and its impact on clinical management. Q J Nucl Med Mol Imaging 2008;52(1):9–16.PubMedGoogle Scholar
  44. 44.
    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.Google Scholar
  45. 45.
    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(1):60–7.CrossRefPubMedGoogle Scholar
  46. 46.
    Young CS, Young BL, Smith SM. Staging Hodgkin’s disease with 18-FDG PET. Comparison with CT and surgery. Clin Positron Imaging 1998;1(3):161–4.CrossRefPubMedGoogle Scholar
  47. 47.
    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(2):603–9.PubMedGoogle Scholar
  48. 48.
    Engert A, Diehl V, Franklin J, Lohri A, Dörken B, Ludwig WD, et al. Escalated-dose BEACOPP in the treatment of patients with advanced-stage Hodgkin’s lymphoma: 10 years of follow-up of the GHSG HD9 study. J Clin Oncol 2009;27(27):4548–54.CrossRefPubMedGoogle Scholar
  49. 49.
    Fermé C, Eghbali H, Meerwaldt JH, Rieux C, Bosq J, Berger F, et al. Chemotherapy plus involved-field radiation in early-stage Hodgkin’s disease. N Engl J Med 2007;357(19):1916–27.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Gerard Moulin-Romsee
    • 1
    • 2
  • Elif Hindié
    • 1
  • Xavier Cuenca
    • 3
  • Pauline Brice
    • 3
  • Didier Decaudin
    • 4
  • Myriam Bénamor
    • 2
  • Josette Brière
    • 5
  • Marcela Anitei
    • 4
  • Jean-Emmanuel Filmont
    • 1
  • David Sibon
    • 3
  • Eric de Kerviler
    • 6
  • Jean-Luc Moretti
    • 1
  1. 1.Service de Médicine Nucléaire, Hôpital Saint-Louis, Assistance Publique-Hôpitaux de ParisUniversité Paris 7Paris cedex 10France
  2. 2.Nuclear MedicineInstitut CurieParisFrance
  3. 3.Haemato-OncologyHôpital Saint-LouisParisFrance
  4. 4.HaematologyInstitut CurieParisFrance
  5. 5.PathologyHôpital Saint-LouisParisFrance
  6. 6.RadiologyHôpital Saint-LouisParisFrance

Personalised recommendations