Annals of Hematology

, Volume 90, Issue 2, pp 165–171 | Cite as

The role of routine imaging procedures in the detection of relapse of patients with Hodgkin lymphoma and aggressive non-Hodgkin lymphoma

  • Neta Goldschmidt
  • Omer Or
  • Martine Klein
  • Bella Savitsky
  • Ora Paltiel
Original Article


Despite improved initial therapies, a subgroup of patients with aggressive non-Hodgkin (A-NHL) and Hodgkin lymphomas (HL) will relapse after first remission. The optimal follow-up strategy for the detection of relapse has not been clarified and periodic imaging is not recommended in most written guidelines. We identified 125 patients with HL and A-NHL diagnosed between January 1993 and September 2008 who relapsed at least 1 month after the end of initial therapy. We assessed whether relapse was detected based on clinical signs or periodic computed tomography (CT), [18F] fluorodeoxyglucose positron emission tomography (PET), or combined PET/CT and whether the mode of detection influenced the pattern and outcome of relapsed disease. Overall, most relapses (62%) were diagnosed clinically especially in A-NHL and in patients with extranodal involvement at diagnosis (p < 0.05); however, relapses of HL occurring after 2001 when PET/CT became available were more commonly detected by routine imaging (p < 0.05). Imaging-detected relapse was not associated with improved survival. While clinical exam remains the most common mode of detecting relapse, our results suggest a potential role for routine PET/CT surveillance in HL patients; however, survival does not appear to be affected by mode of detection.


Follow-up Lymphoma PET/CT Relapse Surveillance 





  1. 1.
    Quddus F, Armitage JO (2009) Salvage therapy for Hodgkin's lymphoma. Cancer J 15:161–163CrossRefPubMedGoogle Scholar
  2. 2.
    Seshadri T, Kuruvilla J, Crump M, Keating A (2008) Salvage therapy for relapsed/refractory diffuse large B cell lymphoma. Biol Blood Marrow Transplant 14:259–267CrossRefPubMedGoogle Scholar
  3. 3.
    Josting A, Rudolph C, Mapara M, Glossmann JP, Sieniawski M, Sieber M, Kirchner HH, Dorken B, Hossfeld DK, Kisro J, Metzner B, Berdel WE, Diehl V, Engert A (2005) Cologne high-dose sequential chemotherapy in relapsed and refractory Hodgkin lymphoma: results of a large multicenter study of the German Hodgkin Lymphoma Study Group (GHSG). Ann Oncol 16:116–123CrossRefPubMedGoogle Scholar
  4. 4.
    Philip T, Guglielmi C, Hagenbeek A, Somers R, Van der Lelie H, Bron D, Sonneveld P, Gisselbrecht C, Cahn JY, Harousseau JL et al (1995) Autologous bone marrow transplantation as compared with salvage chemotherapy in relapses of chemotherapy-sensitive non-Hodgkin's lymphoma. N Engl J Med 333:1540–1545CrossRefPubMedGoogle Scholar
  5. 5.
    Connors JM (2009) Clinical manifestations and natural history of Hodgkin's lymphoma. Cancer J 15:124–128CrossRefPubMedGoogle Scholar
  6. 6.
    Hamlin PA, Zelenetz AD, Kewalramani T, Qin J, Satagopan JM, Verbel D, Noy A, Portlock CS, Straus DJ, Yahalom J, Nimer SD, Moskowitz CH (2003) Age-adjusted International Prognostic Index predicts autologous stem cell transplantation outcome for patients with relapsed or primary refractory diffuse large B-cell lymphoma. Blood 102:1989–1996CrossRefPubMedGoogle Scholar
  7. 7.
    Josting A, Franklin J, May M, Koch P, Beykirch MK, Heinz J, Rudolph C, Diehl V, Engert A (2002) 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 20:221–230CrossRefPubMedGoogle Scholar
  8. 8.
    NCCN Practice Guidelines in Oncology, Hodgkin’s disease/Lymphoma and Non-Hodgkin’s lymphoma. 2009; V.2.2009Google Scholar
  9. 9.
    Engert A, Eichenauer DA, Dreyling M (2009) Hodgkin's lymphoma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 20(Suppl 4):108–109PubMedGoogle Scholar
  10. 10.
    Tilly H, Dreyling M (2009) Diffuse large B-cell non-Hodgkin's lymphoma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 20(Suppl 4):110–112PubMedGoogle Scholar
  11. 11.
    Jerusalem G, Beguin Y, Fassotte MF, Najjar F, Paulus P, Rigo P, Fillet G (2001) Whole-body positron emission tomography using 18F-fluorodeoxyglucose compared to standard procedures for staging patients with Hodgkin's disease. Haematologica 86:266–273PubMedGoogle Scholar
  12. 12.
    Sasaki M, Kuwabara Y, Koga H, Nakagawa M, Chen T, Kaneko K, Hayashi K, Nakamura K, Masuda K (2002) Clinical impact of whole body FDG-PET on the staging and therapeutic decision making for malignant lymphoma. Ann Nucl Med 16:337–345CrossRefPubMedGoogle Scholar
  13. 13.
    Hutchings M, Loft A, Hansen M, Pedersen LM, Berthelsen AK, Keiding S, D’Amore F, Boesen AM, Roemer L, Specht L (2006) Position emission tomography with or without computed tomography in the primary staging of Hodgkin's lymphoma. Haematologica 91:482–489PubMedGoogle Scholar
  14. 14.
    Isasi CR, Lu P, Blaufox MD (2005) A metaanalysis of 18F-2-deoxy-2-fluoro-D-glucose positron emission tomography in the staging and restaging of patients with lymphoma. Cancer 104:1066–1074CrossRefPubMedGoogle Scholar
  15. 15.
    Gallamini A, Hutchings M, Rigacci L, Specht L, Merli F, Hansen M, Patti C, Loft A, Di Raimondo F, D’Amore F, Biggi A, Vitolo U, Stelitano C, Sancetta R, Trentin L, Luminari S, Iannitto E, Viviani S, Pierri I, Levis A (2007) 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 25:3746–3752CrossRefPubMedGoogle Scholar
  16. 16.
    Schot BW, Zijlstra JM, Sluiter WJ, van Imhoff GW, Pruim J, Vaalburg W, Vellenga E (2007) Early FDG-PET assessment in combination with clinical risk scores determines prognosis in recurring lymphoma. Blood 109:486–491CrossRefPubMedGoogle Scholar
  17. 17.
    Cheson B (2009) The case against heavy PETing. J Clin Oncol 27:1742–1743CrossRefPubMedGoogle Scholar
  18. 18.
    Liedtke M, Hamlin PA, Moskowitz CH, Zelenetz AD (2006) Surveillance imaging during remission identifies a group of patients with more favorable aggressive NHL at time of relapse: a retrospective analysis of a uniformly-treated patient population. Ann Oncol 17:909–913CrossRefPubMedGoogle Scholar
  19. 19.
    Dryver ET, Jernstrom H, Tompkins K, Buckstein R, Imrie KR (2003) Follow-up of patients with Hodgkin's disease following curative treatment: the routine CT scan is of little value. Br J Cancer 89:482–486CrossRefPubMedGoogle Scholar
  20. 20.
    Elis A, Blickstein D, Klein O, Eliav-Ronen R, Manor Y, Lishner M (2002) Detection of relapse in non-Hodgkin's lymphoma: role of routine follow-up studies. Am J Hematol 69:41–44CrossRefPubMedGoogle Scholar
  21. 21.
    (1993) A predictive model for aggressive non-Hodgkin's lymphoma. The International Non-Hodgkin's Lymphoma Prognostic Factors Project. N Engl J Med 329:987–994Google Scholar
  22. 22.
    Noordijk EM, Carde P, Mandard AM, Mellink WA, Monconduit M, Eghbali H, Tirelli U, Thomas J, Somers R, Dupouy N et al (1994) Preliminary results of the EORTC-GPMC controlled clinical trial H7 in early-stage Hodgkin's disease. EORTC Lymphoma Cooperative Group. Groupe Pierre-et-Marie-Curie. Ann Oncol 5(Suppl 2):107–112PubMedGoogle Scholar
  23. 23.
    Hasenclever D, Diehl V (1998) A prognostic score for advanced Hodgkin's disease. International Prognostic Factors Project on Advanced Hodgkin's Disease. N Engl J Med 339:1506–1514CrossRefPubMedGoogle Scholar
  24. 24.
    Guppy AE, Tebbutt NC, Norman A, Cunningham D (2003) The role of surveillance CT scans in patients with diffuse large B-cell non-Hodgkin's lymphoma. Leuk Lymphoma 44:123–125CrossRefPubMedGoogle Scholar
  25. 25.
    Nakamura K, Sasaki M, Kunitake N, Kimura M, Watanabe T, Sasaki T, Terashima H, Kuwabara Y, Sakai S, Masuda K (2001) Relapse patterns of localized non-Hodgkin's lymphoma of the head and neck after clinical remission: results of a strict follow-up procedure. Int J Clin Oncol 6:302–305CrossRefPubMedGoogle Scholar
  26. 26.
    Radford JA, Eardley A, Woodman C, Crowther D (1997) Follow up policy after treatment for Hodgkin's disease: too many clinic visits and routine tests? A review of hospital records. Bmj 314:343–346PubMedGoogle Scholar
  27. 27.
    Crocchiolo R, Fallanca F, Giovacchini G, Ferreri AJ, Assanelli A, Verona C, Pescarollo A, Bregni M, Ponzoni M, Gianolli L, Fazio F, Ciceri F (2009) Role of 18FDG-PET/CT in detecting relapse during follow-up of patients with Hodgkin's lymphoma. Ann Hematol 88:1229–1236CrossRefPubMedGoogle Scholar
  28. 28.
    Zinzani PL, Stefoni V, Tani M, Fanti S, Musuraca G, Castellucci P, Marchi E, Fina M, Ambrosini V, Pellegrini C, Alinari L, Derenzini E, Montini G, Broccoli A, Bacci F, Pileri S, Baccarani M (2009) Role of [18F]fluorodeoxyglucose positron emission tomography scan in the follow-up of lymphoma. J Clin Oncol 27:1781–1787CrossRefPubMedGoogle Scholar
  29. 29.
    Jerusalem G, Beguin Y, Fassotte MF, Belhocine T, Hustinx R, Rigo P, Fillet G (2003) Early detection of relapse by whole-body positron emission tomography in the follow-up of patients with Hodgkin's disease. Ann Oncol 14:123–130CrossRefPubMedGoogle Scholar
  30. 30.
    Gisselbrecht C, Glass B, Mounier N, Gill D, Linch D, Trneny M, Bosly A, Shpilberg O, Ketterer N, Moskowitz C, Schmitz N (2009) R-ICE versus R-DHAP in relapsed patients with CD20 diffuse large B-cell lymphoma (DLBCL) followed by autologous stem cell transplantation: CORAL study. J Clin Oncol 27:8509Google Scholar
  31. 31.
    Sehn LH, Donaldson J, Chhanabhai M, Fitzgerald C, Gill K, Klasa R, MacPherson N, O’Reilly S, Spinelli JJ, Sutherland J, Wilson KS, Gascoyne RD, Connors JM (2005) Introduction of combined CHOP plus rituximab therapy dramatically improved outcome of diffuse large B-cell lymphoma in British Columbia. J Clin Oncol 23:5027–5033CrossRefPubMedGoogle Scholar
  32. 32.
    Levine JM, Weiner M, Kelly KM (2006) Routine use of PET scans after completion of therapy in pediatric Hodgkin disease results in a high false positive rate. J Pediatr Hematol Oncol 28:711–714CrossRefPubMedGoogle Scholar
  33. 33.
    Juweid ME, Vose JM (2010) Imaging in early-stage Hodgkin's lymphoma. N Engl J Med 362:962CrossRefPubMedGoogle Scholar
  34. 34.
    Guadagnolo BA, Punglia RS, Kuntz KM, Mauch PM, Ng AK (2006) Cost-effectiveness analysis of computerized tomography in the routine follow-up of patients after primary treatment for Hodgkin's disease. J Clin Oncol 24:4116–4122CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Neta Goldschmidt
    • 1
    • 4
  • Omer Or
    • 1
  • Martine Klein
    • 2
  • Bella Savitsky
    • 3
  • Ora Paltiel
    • 1
    • 3
  1. 1.Department of HematologyHadassah-Hebrew University Medical CenterJerusalemIsrael
  2. 2.Department of Biophysics and Nuclear MedicineHadassah-Hebrew University Medical CenterJerusalemIsrael
  3. 3.School of Public HealthHadassah-Hebrew University Medical CenterJerusalemIsrael
  4. 4.Department of HematologyJerusalemIsrael

Personalised recommendations