Journal of Cancer Research and Clinical Oncology

, Volume 142, Issue 1, pp 167–175 | Cite as

Are epidemiological data on lymphoma incidence comparable? Results from an application of the coding recommendations of WHO, InterLymph, ENCR and SEER to a cancer registry dataset

  • Karl-Heinrich Adzersen
  • Susanne Friedrich
  • Nikolaus BeckerEmail author
Original Article – Cancer Research



The REAL classification of 1994 and the subsequent WHO classification of 2001 can be considered a breakthrough of international harmonization of lymphoma characterization, terminology and codification. These efforts promised to produce internationally comparable cancer registry data in the future. However, in practice discrepancies of usage of these classifications occurred which hamper comparability of registration outcome and must be taken into account by epidemiologic research.


In order to analyze such discrepancies, we used the assignment recommendations of the World Health Organisation 2008, InterLymph 2010, European Network of Cancer Registry 2009 and Surveillance, Epidemiology, and End Results Program 2010 for lymphoid neoplasms in groups and major NHL groups. We used data of the Federal State Cancer Registry of Baden-Wuerttemberg 2010–2011 to test differences in incidence outcome when evaluated according to the different recommendations of these institutions.


Depending on the recommendations of the above institutions, extraction of lymphoid neoplasms provided 4021, 4295, 3873 and 3848 incident cases, respectively. Case numbers for some major NHL groups diverge substantially by recommendation.


Epidemiologists must be aware of potential discrepancies in coding conventions of cancer registries and have to consider them in comparative data analyses. Cancer registries should make transparent which recommendations were applied for lymphoma codification, currently and in the past. Conversion rules should be offered to ascertain proper mapping of lymphoma entities which were coded under varying coding practices over time.


Lymphoma Classification Epidemiology WHO InterLymph ENCR SEER 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Adamson P, Bray F, Costantini AS, Tao MH, Weiderpass E, Roman E (2007) Time trends in the registration of Hodgkin and non-Hodgkin lymphomas in Europe. Eur J Cancer (Oxford England: 1990) 43:391–401. doi: 10.1016/j.ejca.2006.10.008 CrossRefGoogle Scholar
  2. Alexander DD, Mink PJ, Adami HO, Chang ET, Cole P, Mandel JS, Trichopoulos D (2007) The non-Hodgkin lymphomas: a review of the epidemiologic literature. Int J Cancer J Int Cancer 120(Suppl 12):1–39. doi: 10.1002/ijc.22719 CrossRefGoogle Scholar
  3. Brown LM, Gridley G, Check D, Landgren O (2008) Risk of multiple myeloma and monoclonal gammopathy of undetermined significance among white and black male United States veterans with prior autoimmune, infectious, inflammatory, and allergic disorders. Blood 111:3388–3394. doi: 10.1182/blood-2007-10-121285 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Burg G et al (2005) WHO/EORTC classification of cutaneous lymphomas 2005: histological and molecular aspects. J Cutan Pathol 32:647–674. doi: 10.1111/j.0303-6987.2005.00495.x PubMedCrossRefGoogle Scholar
  5. Cabrera Q, Macro M, Hebert B, Cornet E, Collignon A, Troussard X (2014) Epidemiology of monoclonal gammopathy of undetermined significance (MGUS): the experience from the specialized registry of hematologic malignancies of Basse-Normandie (France). Cancer Epidemiol 38:354–356. doi: 10.1016/j.canep.2014.04.006 PubMedCrossRefGoogle Scholar
  6. Cartwright R et al (1999) The rise in incidence of lymphomas in Europe 1985–1992. Eur J Cancer (Oxford England: 1990) 35:627–633CrossRefGoogle Scholar
  7. DIMDI (2011) Aktualisierungsliste zur Vorabversion der ICD-O-3 2013 gegenüber ICD-O-3 2003, Köln, DIMDI. Accessed 24 July 2014
  8. DIMDI (2014) ICD-O-3, Dritte Ausgabe, Erste Revision. Köln, Stand 27.02.2014. German Institute of Medical Documentation and Information DIMDI. Accessed 24 July 2014
  9. Fritz APC, Jack A, Shanmugaratnam K, Sobin L, Parkin DM, Whelan S (2003) International classification of diseases for oncology (ICDO-3), 3rd edn. World Health Organization German edition. DIMDI, CologneGoogle Scholar
  10. Go RS, Gundrum JD, Neuner JM (2015) Determining the clinical significance of monoclonal gammopathy of undetermined significance: a SEER-medicare population analysis. Clin Lymphoma Myeloma Leuk 15(177–186):e174. doi: 10.1016/j.clml.2014.09.004 Google Scholar
  11. Grulich AE, Vajdic CM (2005) The epidemiology of non-Hodgkin lymphoma. Pathology 37:409–419. doi: 10.1080/00313020500370192 PubMedCrossRefGoogle Scholar
  12. Harris NL et al (1994) A revised European–American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 84:1361–1392PubMedGoogle Scholar
  13. Hennessy BT, Hanrahan EO, Daly PA (2004) Non-Hodgkin lymphoma: an update. Lancet Oncol 5:341–353. doi: 10.1016/S1470-2045(04)01490-1 PubMedCrossRefGoogle Scholar
  14. IARC/WHO (2011) Updates to ICDO-3. International Agency for Research on Cancer and World Health Organization. Accessed 24 July 2014
  15. Jaffe ES, Harris NL, Stein H, Vardiman JW (eds) (2001) Pathology and genetics of tumours of haematopoietic and lymphoid tissues. World Health Organization classification of tumours. IARC Press, LyonGoogle Scholar
  16. Johnson CH AM, Peace S, Percy-Laurry A (eds) (2010) Case report-ability and coding manual. Effective with cases diagnosed 1/1/2010 and after. National Cancer Institute, Bethesda MD 20892-831. Accessed 24 July 2014
  17. Kempf W, Sander CA (2010) Classification of cutaneous lymphomas—an update. Histopathology 56:57–70. doi: 10.1111/j.1365-2559.2009.03455.x PubMedCrossRefGoogle Scholar
  18. Landgren O et al (2009) Pesticide exposure and risk of monoclonal gammopathy of undetermined significance in the Agricultural Health Study. Blood 113:6386–6391. doi: 10.1182/blood-2009-02-203471 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Morgan G et al (1997) Changing trends in the incidence of non-Hodgkin’s lymphoma in Europe. Biomed study group. Ann oncol: official journal of the European Society for Medical Oncology/ESMO 8(Suppl 2):49–54CrossRefGoogle Scholar
  20. Morton LM et al (2007) Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology working group of the International Lymphoma Epidemiology Consortium (interlymph). Blood 110:695–708. doi: 10.1182/blood-2006-11-051672 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Ruhl J AM, Dickie L, Sun, L, Johnson, CH. (2014) Hematopoietic and lymphoid neoplasm coding manual. National Cancer Institute, Bethesda MD 20850-9765. Accessed 24 July 2014
  22. Sant MK-LM, Maynadié M, Raphaël M, Ferretti S, Giacomin A, Tereanu C, Giraldo-Castellano P, Marcos-Gragera R, Martos-Jiménez C, Lutz JM, Visser O (eds) (2009) Manual for coding and reporting haematological malignancies, ENCR. Accessed 24 July 2014
  23. Seer (2001) Definitions of single and subsequent primaries for hematologic malignancies based on ICDO-3 reportable malignancies, effective with diagnoses 01/01/2001 and after. Accessed 24 July 2014
  24. Senff NJ et al (2007) Reclassification of 300 primary cutaneous B-Cell lymphomas according to the new WHO-EORTC classification for cutaneous lymphomas: comparison with previous classifications and identification of prognostic markers. J clin oncol: official journal of the American Society of Clinical Oncology 25:1581–1587. doi: 10.1200/JCO.2006.09.6396 CrossRefGoogle Scholar
  25. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) (2008) WHO classification of tumours of haematopoietic and lymphoid tissues. WHO classification of tumours. IARC Press, LyonGoogle Scholar
  26. Turner JJ et al (2010) InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood 116:e90–e98. doi: 10.1182/blood-2010-06-289561 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Willemze R et al (2005) WHO-EORTC classification for cutaneous lymphomas Blood 105:3768–3785. doi: 10.1182/blood-2004-09-3502 PubMedGoogle Scholar
  28. Wong KY et al (2013) Epigenetic inactivation of the MIR129-2 in hematological malignancies. Journal of hematology and oncology 6:16. doi: 10.1186/1756-8722-6-16 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Karl-Heinrich Adzersen
    • 1
  • Susanne Friedrich
    • 1
  • Nikolaus Becker
    • 1
    Email author
  1. 1.Federal State Cancer Registry of Baden-Württemberg, Epidemiological Cancer RegistryGerman Cancer Research CenterHeidelbergGermany

Personalised recommendations