Skip to main content
SpringerLink
Log in

Classifications of lymphoma; reflections of time and technology

  • Review and Perspective
  • Published:
Virchows Archiv Aims and scope Submit manuscript

Abstract

‘Nowhere in pathology has a chaos of names so clouded clear concepts as in the subject lymphoid tumors’. R.A. Willis.

In 1858, Rudolf Virchow, with a primitive microscope and limited experiential base, recognized ‘at least three different conditions here, hyperinosis, leucocytosis and leukemia….’. One hundred and fifty years later, the World Health Organization (WHO 2008), with a much more extensive armamentarium of tools, and a wealth of diverse experience, promulgated criteria distinguishing more than 100 types of ‘Tumors of the Hematopoietic and Lymphoid Tissues’. From three to one hundred and three; this is progress! And this is history! Our goal is to examine the course and causes of this history; how we moved from three entities to a hundred and three, what we have learned from it, and how we may use the insights that we have gained to anticipate ‘future histories’ in this marvelously dynamic area of biology and disease.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  1. Linnaeus C (1756) Systema Naturae, 9th edn. Theodor Haak, Leiden (Lugdunum Batavorum)

    Google Scholar 

  2. Darwin CR, Wallace AR (1858) On the tendency of species to form varieties; and on the perpetuation of varieties and species by natural means of selection. Journal of the Proceedings of the Linnean Society of London Zoology 3:46–50 [Read 1st. July, 1858]

    Article  Google Scholar 

  3. Barlow N (1958) The autobiography of Charles Darwin 1809–1882. Collins, London, p 122

    Google Scholar 

  4. Virchow R (1858) Die Cellularpathologie in ihrer Begrundung auf physiologische und pathologische Gewebelehre. Berlin. Verlag von August Hirschwald, Berlin (English translation). Chance F (1860) Cellular Pathology. John Churchill, London. Reissued; Classics of Medicine Library, Birmingham. Alabama, 1979, pp 170–171

  5. Swerdlow SH, Campo E, Harris NL et al (2008) WHO classification of tumors of the haematopoietic and lymphoid tissues. IARC. WHO, Geneva

    Google Scholar 

  6. Taylor CR (2010) From anatomy to surgery to pathology: eighteenth century London and the Hunterian schools. Virchows Arch 247:405–414

    Article  Google Scholar 

  7. Hodgkin T (1832) On some morbid appearances of the absorbent glands and spleen. Med-Chir Trans 17:68–114

    PubMed  CAS  Google Scholar 

  8. Wilks SS (1865) Cases of enlargement of the lymphatic glands and spleen (or Hodgkin’s Disease) with remarks. Guy’s Hosp Rep 11:56–67

    Google Scholar 

  9. Robb-Smith AHT, Taylor CR (1980) Lymph node biopsy. Oxford University Press, Oxford

  10. Greenfield WS (1878) Specimens illustrative of the pathology of lymphadenoma and leucocythemia. Trans Path Soc Lond 29:272–304

    Google Scholar 

  11. Taylor CR (1978) A history of the Reed–Sternberg cell. Biomedicine 28:196–203

    PubMed  CAS  Google Scholar 

  12. Taylor CR (2005) Hodgkin’s disease is a non-Hodgkin lymphoma. Hum Pathol 36:1–4

    Article  PubMed  Google Scholar 

  13. Aschoff L (1924) Das reticulo-endotheliale system. Ergebn inn Med Kinderheilkd 26:1–118

    Google Scholar 

  14. Maximow AA (1927) In: von Mollendorf W (ed) Handbuch der Mikrosp Anat des Menschen, II. Springer, Berlin, p 359

    Google Scholar 

  15. Maximow AA (1909) Der Lymphozyt als gemeinsame Stammzelle der verschiedenen Blutelemente in der embryonalen Entwicklung und im postfetalen Leben der Säugetiere. (Demonstrationsvortrag, gehalten in der ausserordentlichen Sitzung der Berliner Hämatologischen Gesellschaft am 1. Juni, 1909). Folia Haematol 8:125–134

    Google Scholar 

  16. Adami JG (1913) On the relationship between tumours proper (blastomas) and hyperblastosis. Communicated to the Pathological Section of the 17th International Medical Congress, London, August 1913. Can Med Assoc J III:953–961. Available at http://www.ncbi.nlm.nih.gov. Accessed June 2010

  17. Letterer E (1924) Aleukamische Retikulose: Ein Beitrag zu den proliferativen Erkrankungen des Retikuloendothelialapparates. Frankf Z Pathol 30:377–394

    Google Scholar 

  18. Oberling C (1928) Les reticulosarcomes et les reticulo-endothelialsarcomes de la moelle osseuse (sarcomes D’Ewing). Bull Cancer (Paris) 17:259

    Google Scholar 

  19. Ewing J (1928) The classification and treatment of bone sarcoma. Report of the International Conference on Cancer 17th to 20th of July 1928, 3rd ed. John Wright and Sons Ltd, Bristol. Simkin Marshall Ltd, London, p 365

  20. Callender GR (1934) Tumors and tumor-like conditions of the lymphocyte, the myelocyte, the erythrocyte and the reticulum cell. Am J Pathol 10:443–466

    PubMed  CAS  Google Scholar 

  21. Robb-Smith AHT (1938) Reticulosis and reticulosarcoma: a histological classification. J Path XLVII:457–480

    Article  Google Scholar 

  22. Robb-Smith AHT (1947) In: Dyke SC (ed) Recent advances in clinical pathology. Churchill, London, p 350

    Google Scholar 

  23. Jackson H, Parker F (1947) Hodgkin’s disease and allied disorders. Oxford University Press, New York

    Google Scholar 

  24. Lennert K (1967) In: Ruttiman AG (ed) Progress in lymphology. Thieme, Stuttgart, p 103

    Google Scholar 

  25. Mallory FB (1914) The principles of pathological histology. Saunders, Philadelphia

    Google Scholar 

  26. Warthin AS (1931) The genetic neoplastic relationships of Hodgkin’s disease. Ann Surg 93:153–161

    Article  PubMed  CAS  Google Scholar 

  27. Pullinger BD (1932) In: Gordon MH (ed) Rose research on lymphadenoma. Wright, Bristol, p 117

    Google Scholar 

  28. Gall EA, Mallory FB (1942) Malignant lymphoma. A clinico-pathological survey of 618 cases. Am J Pathol 18:381–429

    PubMed  CAS  Google Scholar 

  29. Custer RP, Bernhard WG (1948) The interrelationship of Hodgkin’s disease and other lymphatic tumors. Am J Med Sci 216:625–642

    Article  PubMed  CAS  Google Scholar 

  30. Custer RP (1953) Borderlands dim in malignant disease. Radiology 61:764–770

    PubMed  CAS  Google Scholar 

  31. Custer RP (1960) The changing patterns of lymphocytic malignancies. In: Rebuck JW (ed) The lymphocyte and lymphocytic tissues. International Academy of Pathology Monograph. Hoeber, New York, pp 181–193

    Google Scholar 

  32. Willis RA (1960) Pathology of tumours, 1st edn. Butterworths, London, 1948

    Google Scholar 

  33. Willis RA (1958) The borderland of embryology and pathology. Butterworths, London

    Google Scholar 

  34. Rappaport H, Winter WJ, Hicks EB (1956) Follicular lymphoma. A re-evaluation of its position in the scheme of malignant lymphomas based on a survey of 253 cases. Cancer 9:792–821

    Article  PubMed  Google Scholar 

  35. Rappaport H (1966) Tumors of the hematopoietic system (atlas of tumor pathology, section 3, fasc. 8). Armed Forces Institute of Pathology, Washington

    Google Scholar 

  36. Chang TS, Glick B, Winter AR (1955) The significance of the bursa of Fabricius of chickens in antibody production. Poultry Sci 34:1187

    Google Scholar 

  37. Glick B (1955) Growth and function of the bursa of Fabricius in the domestic fowl. Ph.D. thesis, Ohio State University

  38. Sternberg SS (2003) Bottoms up to a Nobel-worthy chicken’s bottom. Am J Surg Pathol 27:1471–1472

    Article  PubMed  Google Scholar 

  39. Cooper MD, Peterson RDA, Good RA (1965) Delineation of the thymic and bursal lymphoid systems in chickens. Nature (Lond) 205:143–146

    Article  CAS  Google Scholar 

  40. Yoffey JM, Winter GCB, Osmond DG et al (1965) Morphological studies in the culture of human leucocytes with phytohaemagglutinin. Brit J Haematol 11:488–497

    Article  CAS  Google Scholar 

  41. Moffatt DJ, Rosse C, Yoffey JM (1965) Hypothesis. Identity of the haematopoietic stem cell. Lancet 290:547–548

    Article  Google Scholar 

  42. Dameshek W (1963) Editorial: “immunoblasts” and “immunocytes”—an attempt at a functional nomenclature. Blood 21:243–245

    PubMed  CAS  Google Scholar 

  43. Good RA (1954) Agammaglobulinemia: an experimental study. Am J Dis Child 88:625–626

    Google Scholar 

  44. Bruton OC (1952) Agammaglobulinemia. Pediatrics 9:722–728

    PubMed  CAS  Google Scholar 

  45. Peterson RDA, Burmester BR, Cooper MD, Good RA (1967) Lymphomagenesis in relation to germinal centers and the bursa of Fabricius. In: Germinal center in immune responses. Springer, New York, pp 443–446

    Google Scholar 

  46. Flemming W (1882) Zellsubstanz, Kern und Zelltheilung. Vogel, Liepzig

    Google Scholar 

  47. Taylor CR (1978) Classification of lymphomas: ‘new thinking’ on old thoughts. Arch Pathol Lab Med 102:549–554

    PubMed  CAS  Google Scholar 

  48. Taylor CR (1982) Pathobiology of lymphocyte transformation. In: Ioachim HL (ed) Lecture, Leukemia Research Fund Symposium, Royal College of Physicians, London, April, 1981. Pathobiology Annual 1982. Raven, New York, pp 65–83

    Google Scholar 

  49. Taylor CR (1980) Changing concepts in classification of lymphoma. In: Bosman F, van den Tweel J, Taylor CR (eds) Malignant lymphomas, the pathophysiology of the lymphocyte and its neoplasms. Leiden University Press, Leiden, pp 175–184

    Google Scholar 

  50. Gerard Marchant R, Hamlin I, Lennert K et al (1974) Classification of non-Hodgkin’s lymphomas. Lancet II:405–408

    Google Scholar 

  51. Lukes RJ, Collins RD (1974) A functional approach to the classification of the lymphomata. Rec Res Cancer Res 46:18–30

    Google Scholar 

  52. Musshoff K, Schmidt-Vollmer H, Lennert K, Sandritter W (1976) Preliminary clinical findings on the Kiel classification of malignant lymphomas. Z Krebsforsch 87:229–238

    Article  CAS  Google Scholar 

  53. Lukes RJ, Parker JW, Taylor CR et al (1978) Immunologic approach to non-Hodgkin’s lymphomas and related leukemias. An analysis of the results of multiparameter studies of 425 cases. Semin Hematol 15:322–351

    PubMed  CAS  Google Scholar 

  54. Lennert K, Collins RD, Lukes RJ (1983) Concordance of the Kiel and Lukes–Collins classifications of non-Hodgkin’s lymphomas. Histopathology. Intersciences.Wiley.com

  55. Taylor CR, Burns J (1974) The demonstration of plasma cells and other immunoglobulin-containing cells in formalin-fixed, paraffin-embedded tissues using peroxidase-labelled antibody. J Clin Pathol 27:14–20

    Article  PubMed  CAS  Google Scholar 

  56. Taylor CR (1974) The nature of Reed–Sternberg cells and other malignant reticulum cells. Lancet II:802–807

    Article  Google Scholar 

  57. Kohler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256:495–497

    Article  PubMed  CAS  Google Scholar 

  58. Shi S-R, Cote RJ, Taylor CR (2001) Antigen retrieval immunohistochemistry and molecular morphology in the year 2001. Appl Immunohistol Mol Morphol 9:107–116

    Article  CAS  Google Scholar 

  59. Shi SR, Taylor CR (eds) (2010) Immunohistochemistry and antigen retrieval based research and diagnosis. Wiley, Hoboken

  60. Harris NL, Jaffe ES, Diebold J et al (2000) Lymphoma classification—from controversy to consensus: the R.E.A.L. and WHO Classification of lymphoid neoplasms. Ann Oncol S 1:3–10

    Article  Google Scholar 

  61. Harris NL et al (1994) A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 84:1361–1392

    PubMed  CAS  Google Scholar 

  62. Jaffe ES, Harris NL, Stein H, Vardiman JW (eds) (2001) World Health Organization classification of tumours. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. IARC, Lyon

  63. Nowell PC, Hungerford DA (1960) A minute chromosome in human chronic granulocytic leukemia. Science 132:147

    Article  Google Scholar 

  64. Danna K, Nathans D (1971) Specific cleavage of simian virus 40 DNA by restriction endonuclease of Hemophilus influenzae. Proc Nat Acad Sci 68:2913–2917

    Article  PubMed  CAS  Google Scholar 

  65. Mullis KB (1990) The unusual origin of the polymerase chain reaction. Scientific American, April, pp 56–65

  66. Taylor CR, Becker KF (2011) Liquid morphology: immunochemical analysis of proteins extracted from formalin fixed paraffin embedded tissues: combining proteomics with immunohistochemistry. Appl Immunohistochem Mol Morphol 19:1–9

    Article  PubMed  Google Scholar 

  67. Taylor CR (1994) Viewpoint: an exaltation of experts: concerted efforts in the standardization of immunohistochemistry. Appl Immunohistochem 1:232–243, Reproduced in Hum Pathol 25:2–11, 1994

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Editorial Board of Virchows Archiv for the opportunity to develop this history, in particular Fred Bosman, M.D. and Jan Van den Tweel, M.D. for encouragement and review.

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pathology, Keck School of Medicine, Los Angeles, CA, USA

    Clive R. Taylor

  2. Allegheny Valley Hospital, Natrona Heights, PA, USA

    Robert J. Hartsock

Authors
  1. Clive R. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert J. Hartsock
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clive R. Taylor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taylor, C.R., Hartsock, R.J. Classifications of lymphoma; reflections of time and technology. Virchows Arch 458, 637–648 (2011). https://doi.org/10.1007/s00428-011-1083-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00428-011-1083-0

Keywords

Search

Navigation