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Evolution of lymphoma staging and response evaluation: current limitations and future directions

Nature Reviews Clinical Oncology volume 14, pages 631–645 (2017)Cite this article

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Abstract

The accurate detection and precise assessment of therapeutic responses is critical to the optimal management of patients with lymphoma. Over the past 50 years, dramatic advances in technology have established imaging as the cornerstone of disease evaluation. However, the appropriate application of current techniques requires acknowledgement of their strengths and weaknesses, and appreciation of the full diversity of lymphoid neoplasms. The role of anatomical and functional imaging in detection, treatment escalation/de-escalation and prognostication of patients with lymphoma can be misinterpreted. The development of disease assessment criteria, without an appreciation of the limitations of current imaging technologies, reflects a potential overreach of imaging science. Furthermore, the introduction of various novel therapies adds to the complexity of disease monitoring. In this Perspectives, the authors evaluate the available evidence in this rapidly evolving field and propose a reporting framework, named 'Specialist Integrated Haematological Malignancy Imaging Reporting' (SIHMIR), with a goal of providing a robust and adaptable system for lymphoma assessment. We predict a future model of multimodal disease assessment using novel molecular and imaging techniques, and highlight the key outstanding research questions in this field.

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Figure 1: Timeline depicting the development of clinicopathological classifications, staging, and response assessment guidelines, and radiographic techniques in lymphoma.
Figure 2: New functional imaging techniques in lymphoma.
Figure 3: Risk-adapted and response-adapted strategies, staging, response assessment and surveillance.
Figure 4: New PET radiotracers in lymphoma.

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References

  1. Swerdlow, S. H. et al. The 2016 revision of the World Health Organization (WHO) classification of lymphoid neoplasms. Blood 127, 2375–2390 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2015. CA Cancer J. Clin. 65, 5–29 (2015).

    PubMed  Google Scholar 

  3. Cheson, B. D. et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and Non-Hodgkin lymphoma: the Lugano classification. J. Clin. Oncol. 32, 3059–3068 (2014).

    PubMed  PubMed Central  Google Scholar 

  4. National Institute for Health and Care Excellence. Non-Hodgkin's lymphoma: diagnosis management (NG52) [online]. https://www.nice.org.uk/guidance/ng52 (NICE, 2016).

  5. National Institute for Health and Care Excellence. Myeloma: diagnosis management (NG35) [online]. https://www.nice.org.uk/guidance/ng35 (NICE, 2016).

  6. National Institute for Health and Care Excellence. Haematological cancers: improving outcomes (NG47) [online]. https://www.nice.org.uk/guidance/ng47 (NICE, 2016).

  7. Johnson, P. et al. Adapted treatment guided by interim PET-CT scan in advanced Hodgkin's lymphoma. N. Engl. J. Med. 374, 2419–2429 (2016).

    PubMed  PubMed Central  Google Scholar 

  8. Press, O. W. et al. US Intergroup trial of response-adapted therapy for stage III to IV Hodgkin lymphoma using early interim fluorodeoxyglucose — positron emission tomography imaging: Southwest Oncology Group S0816. J. Clin. Oncol. 34, 2020–2027 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Rosenberg, S. A. Validity of the Ann Arbor staging classification for the non-Hodgkin's lymphomas. Cancer Treat. Rep. 61, 1023–1027 (1977).

    CAS  PubMed  Google Scholar 

  10. Bernard, J. et al. Proposition d'une classification des different formes cliniques de la maladie de Hodgkin [French]. Nouv. Rev. Fr. Hematol. 6, 175–176 (1966).

    Google Scholar 

  11. Rosenberg, S. A. Report of the Committee on the Staging of Hodgkin's Disease. Cancer Res. 26, 1310 (1966).

    Google Scholar 

  12. Rosenberg, S. A. & Kaplan, H. S. Evidence for an orderly progression in the spread of Hodgkin's disease. Cancer Res. 26, 1225–1231 (1966).

    CAS  PubMed  Google Scholar 

  13. Aisenberg, A. C. Primary management of Hodgkin's disease. CA Cancer J. Clin. 18, 158–162 (1968).

    CAS  PubMed  Google Scholar 

  14. Musshoff, K. Prognostic and therapeutic implications of staging in extranodal Hodgkin's disease. Cancer Res. 31, 1814–1827 (1971).

    CAS  PubMed  Google Scholar 

  15. Glatstein, E., Guernsey, J. M., Rosenberg, S. A. & Kaplan, H. S. The value of laparotomy and splenectomy in the staging of Hodgkin's disease. Cancer 24, 709–718 (1969).

    CAS  PubMed  Google Scholar 

  16. Kadin, M. E., Glatstein, E. & Dorfman, R. F. Clinicopathologic studies of 117 untreated patients subjected to laparotomy for the staging of Hodgkin's Disease. Cancer 27, 1277–1294 (1971).

    CAS  PubMed  Google Scholar 

  17. Strum, S. B. & Rappaport, H. Significance of focal involvement of lymph nodes for the diagnosis and staging of Hodgkin's disease. Cancer 25, 1314–1319 (1970).

    CAS  PubMed  Google Scholar 

  18. Carbone, P. P., Kaplan, H. S., Musshoff, K., Smithers, D. W. & Tubiana, M. Report of the Committee on Hodgkin's Disease Staging Classification. Cancer Res. 31, 1860–1861 (1971).

    CAS  PubMed  Google Scholar 

  19. Rosenberg, S. A. et al. Report of the Committee on Hodgkin's Disease Staging Procedures. Cancer Res. 31, 1862–1863 (1971).

    CAS  PubMed  Google Scholar 

  20. Hounsfield, G. N. Computerized transverse axial scanning (tomography): part 1. Description of system. Br. J. Radiol. 46, 1016–1022 (1973).

    CAS  PubMed  Google Scholar 

  21. Ambrose, J. Computerized transverse axial scanning (tomography): part 2. Clinical application. Br. J. Radiol. 46, 1023–1047 (1973).

    CAS  PubMed  Google Scholar 

  22. Lister, T. A. et al. Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin's disease: Cotswolds meeting. J. Clin. Oncol. 7, 1630–1636 (1989).

    CAS  PubMed  Google Scholar 

  23. Cheson, B. D. et al. Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. J. Clin. Oncol. 17, 1244–1253 (1999).

    CAS  PubMed  Google Scholar 

  24. Reivich, M. et al. The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Circ. Res. 44, 127–137 (1979).

    CAS  PubMed  Google Scholar 

  25. Warburg, O., Posener, K. & Negelein, E. Uber den Stoffwechsel der Carcinomzelle [German]. Biochem. Zeitschr. 152, 129–169 (1924).

    Google Scholar 

  26. Strauss, L. G. & Conti, P. S. The applications of PET in clinical oncology. J. Nucl. Med. 32, 623–648 (1991).

    CAS  PubMed  Google Scholar 

  27. Rigo, P. et al. Oncological applications of positron emission tomography with fluorine-18 fluorodeoxyglucose. Eur. J. Nucl. Med. 23, 1641–1674 (1996).

    CAS  PubMed  Google Scholar 

  28. Spaepen, K. et al. [18F]FDG PET monitoring of tumour response to chemotherapy: does [18F]FDG uptake correlate with the viable tumour cell fraction? Eur. J. Nucl. Med. Mol. Imaging 30, 682–688 (2003).

    CAS  PubMed  Google Scholar 

  29. Gatenby, R. A. & Gillies, R. J. Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4, 891–899 (2004).

    CAS  PubMed  Google Scholar 

  30. Spaepen, K., Stroobants, S., Verhoef, G. & Mortelmans, L. Positron emission tomography with [18F]FDG for therapy response monitoring in lymphoma patients. Eur. J. Nucl. Med. Mol. Imaging 30, S97–S105 (2003).

    PubMed  Google Scholar 

  31. Isasi, C. R., Lu, P. & Blaufox, M. D. A metaanalysis of 18F-2-deoxy-2-fluoro-D-glucose positron emission tomography in the staging and restaging of patients with lymphoma. Cancer 104, 1066–1074 (2005).

    PubMed  Google Scholar 

  32. Terasawa, T., Nihashi, T., Hotta, T. & Nagai, H. 18F-FDG PET for posttherapy assessment of Hodgkin's disease and aggressive non-Hodgkin's lymphoma: a systematic review. J. Nucl. Med. 49, 13–21 (2008).

    PubMed  Google Scholar 

  33. Juweid, M. E. & Cheson, B. D. Role of positron emission tomography in lymphoma. J. Clin. Oncol. 23, 4577–4580 (2005).

    PubMed  Google Scholar 

  34. Juweid, M. E. 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. 25, 571–578 (2007).

    PubMed  Google Scholar 

  35. Juweid, M. E. & Cheson, B. D. Positron-emission tomography and assessment of cancer therapy. N. Engl. J. Med. 354, 496–507 (2006).

    CAS  PubMed  Google Scholar 

  36. Beyer, T. et al. A combined PET/CT scanner for clinical oncology. J. Nucl. Med. 41, 1369–1379 (2000).

    CAS  PubMed  Google Scholar 

  37. Cheson, B. D. et al. Revised response criteria for malignant lymphoma. J. Clin. Oncol. 25, 579–586 (2007).

    PubMed  Google Scholar 

  38. Parker, A. et al. Best Practice in Lymphoma Diagnosis and Reporting [online]. www.bloodmed.com/contentimage/guidelines/3455.pdf (2010).

    Google Scholar 

  39. Barrington, S. F. et al. Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J. Clin. Oncol. 32, 3048–3058 (2014).

    PubMed  PubMed Central  Google Scholar 

  40. Meignan, M., Gallamini, A. & Haioun, C. Report on the First International Workshop on interim-PET-scan in lymphoma. Leuk. Lymphoma 50, 1257–1260 (2009).

    PubMed  Google Scholar 

  41. Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).

    CAS  PubMed  Google Scholar 

  42. Sharma, B., Martin, A., Stanway, S., Johnston, S. R. D. & Constantinidou, A. Imaging in oncology — over a century of advances. Nat. Rev. Clin. Oncol. 9, 728–737 (2012).

    CAS  PubMed  Google Scholar 

  43. Castellino, R. A. et al. Computed tomography, lymphography, and staging laparotomy: correlations in initial staging of Hodgkin disease. AJR Am. J. Roentgenol. 143, 37–41 (1984).

    CAS  PubMed  Google Scholar 

  44. Hasenclever, D. & Diehl, V. A. Prognostic score for advanced Hodgkin's disease. N. Engl. J. Med. 339, 1506–1514 (1998).

    CAS  PubMed  Google Scholar 

  45. Josting, A. 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. 20, 221–230 (2002).

    PubMed  Google Scholar 

  46. Sehn, L. H. et al. The revised International Prognostic Index (R-IPI) is a better predictor of outcome than the standard IPI for patients with diffuse large B-cell lymphoma treated with R-CHOP. Blood 109, 1857–1861 (2007).

    CAS  PubMed  Google Scholar 

  47. Hoster, E. et al. A new prognostic index (MIPI) for patients with advanced-stage mantle cell lymphoma. Blood 111, 558–565 (2008).

    CAS  PubMed  Google Scholar 

  48. Federico, M. et al. Follicular lymphoma international prognostic index 2: a new prognostic index for follicular lymphoma developed by the International Follicular Lymphoma Prognostic Factor Project. J. Clin. Oncol. 27, 4555–4562 (2009).

    PubMed  Google Scholar 

  49. Zhou, Z. et al. An enhanced International Prognostic Index (NCCN-IPI) for patients with diffuse large B-cell lymphoma treated in the rituximab era. Blood 123, 837–843 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Pastore, A. et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol. 16, 1111–1122 (2015).

    CAS  PubMed  Google Scholar 

  51. Jurinovic, V. et al. Clinicogenetic risk models predict early progression of follicular lymphoma after first-line immunochemotherapy. Blood 128, 1112–1120 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Schmitz, N. et al. CNS International Prognostic Index: a risk model for CNS relapse in patients with diffuse large B-cell lymphoma treated with R-CHOP. J. Clin. Oncol. 34, 3150–3156 (2016).

    CAS  PubMed  Google Scholar 

  53. Scherer, F. et al. Distinct biological subtypes and patterns of genome evolution in lymphoma revealed by circulating tumor DNA. Sci. Transl Med. 8, 364ra155 (2016).

    PubMed  PubMed Central  Google Scholar 

  54. Aukema, S. M. et al. Double-hit B-cell lymphomas. Blood 117, 2319–2331 (2011).

    CAS  PubMed  Google Scholar 

  55. Cortelazzo, S. et al. Randomized trial comparing R-CHOP versus high-dose sequential chemotherapy in high-risk patients with diffuse large B-cell lymphomas. J. Clin. Oncol. 34, 4015–4022 (2016).

    CAS  PubMed  Google Scholar 

  56. Schmitz, N. et al. Conventional chemotherapy (CHOEP-14) with rituximab or high-dose chemotherapy (MegaCHOEP) with rituximab for young, high-risk patients with aggressive B-cell lymphoma: an open-label, randomised, phase 3 trial (DSHNHL 2002–2001). Lancet Oncol. 13, 1250–1259 (2012).

    CAS  PubMed  Google Scholar 

  57. Miller, T. P. et al. Chemotherapy alone compared with chemotherapy plus radiotherapy for localized intermediate- and high-grade non-Hodgkin's lymphoma. N. Engl. J. Med. 339, 21–26 (1998).

    CAS  PubMed  Google Scholar 

  58. Shenkier, T. N. et al. Brief chemotherapy and involved-region irradiation for limited-stage diffuse large-cell lymphoma: an 18-year experience from the British Columbia Cancer Agency. J. Clin. Oncol. 20, 197–204 (2002).

    CAS  PubMed  Google Scholar 

  59. Leitch, H. A. et al. Limited-stage mantle-cell lymphoma. Ann. Oncol. 14, 1555–1561 (2003).

    CAS  PubMed  Google Scholar 

  60. Vandenberghe, E. et al. The clinical outcome of 65 cases of mantle cell lymphoma initially treated with non-intensive therapy by the British National Lymphoma Investigation Group. Br. J. Haematol. 99, 842–847 (1997).

    CAS  PubMed  Google Scholar 

  61. MacManus, M. P. & Hoppe, R. T. Is radiotherapy curative for stage I and II low-grade follicular lymphoma? Results of a long-term follow-up study of patients treated at Stanford University. J. Clin. Oncol. 14, 1282–1290 (1996).

    CAS  Google Scholar 

  62. Pugh, T. J., Ballonoff, A., Newman, F. & Rabinovitch, R. Improved survival in patients with early stage low-grade follicular lymphoma treated with radiation. Cancer 116, 3843–3851 (2010).

    PubMed  Google Scholar 

  63. Engert, A. et al. Reduced treatment intensity in patients with early-stage Hodgkin's lymphoma. N. Engl. J. Med. 363, 640–652 (2010).

    CAS  PubMed  Google Scholar 

  64. Noordijk, E. M. et al. Combined-modality therapy for clinical stage I or II Hodgkin's lymphoma: long-term results of the European Organisation for Research and Treatment of Cancer H7 randomized controlled trials. J. Clin. Oncol. 24, 3128–3135 (2006).

    PubMed  Google Scholar 

  65. Carde, P. et al. Eight cycles of ABVD versus four cycles of BEACOPPescalated plus four cycles of BEACOPPbaseline in stage III to IV, International Prognostic Score ≥3, high-risk Hodgkin lymphoma: first results of the phase III EORTC 20012 Intergroup trial. J. Clin. Oncol. 34, 2028–2036 (2016).

    CAS  PubMed  Google Scholar 

  66. Buchmann, I. et al. 2-(fluorine-18)fluoro-2-deoxy-D-glucose positron emission tomography in the detection and staging of malignant lymphoma: a bicenter trial. Cancer 91, 889–899 (2001).

    CAS  PubMed  Google Scholar 

  67. Salaun, P. Y. 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 36, 1813–1821 (2009).

    PubMed  Google Scholar 

  68. Long, N. M. & Smith, C. S. Causes and imaging features of false positives and false negatives on 18F-PET/CT in oncologic imaging. Insights Imaging 2, 679–698 (2011).

    PubMed  PubMed Central  Google Scholar 

  69. Gawande, R. S. et al. Differentiation of normal thymus from anterior mediastinal lymphoma and lymphoma recurrence at pediatric PET/CT. Radiology 262, 613–622 (2012).

    PubMed  Google Scholar 

  70. Jerushalmi, J., Frenkel, A., Bar-Shalom, R., Khoury, J. & Israel, O. Physiologic thymic uptake of 18F-FDG in children and young adults: a PET/CT evaluation of incidence, patterns, and relationship to treatment. J. Nucl. Med. 50, 849–853 (2009).

    PubMed  Google Scholar 

  71. Dunleavy, K. et al. Dose-adjusted EPOCH-rituximab therapy in primary mediastinal B-cell lymphoma. N. Engl. J. Med. 368, 1408–1416 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Boellaard, R. et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur. J. Nucl. Med. Mol. Imaging 42, 328–354 (2015).

    CAS  PubMed  Google Scholar 

  73. Martelli, M. et al. [18F]Fluorodeoxyglucose positron emission tomography predicts survival after chemoimmunotherapy for primary mediastinal large B-cell lymphoma: results of the International Extranodal Lymphoma Study Group IELSG-26 Study. J. Clin. Oncol. 32, 1769–1775 (2014).

    PubMed  Google Scholar 

  74. Huttmann, A., Muller, S., Jockel, K.-H. & Duhrsen, U. Pitfalls of interim positron emission tomography scanning in diffuse large B-cell lymphoma. J. Clin. Oncol. 28, e488–e489 (2010).

    PubMed  Google Scholar 

  75. Itti, E. et al. An international confirmatory study of the prognostic value of early PET/CT in diffuse large B-cell lymphoma: comparison between Deauville criteria and ΔSUVmax. Eur. J. Nucl. Med. Mol. Imaging 40, 1312–1320 (2013).

    PubMed  Google Scholar 

  76. Hasenclever, D. et al. qPET — a quantitative extension of the Deauville scale to assess response in interim FDG-PET scans in lymphoma. Eur. J. Nucl. Med. Mol. Imaging 41, 1301–1308 (2014).

    PubMed  Google Scholar 

  77. Le Roux, P. Y. et al. Prognostic value of interim FDG PET/CT in Hodgkin's lymphoma patients treated with interim response-adapted strategy: comparison of International Harmonization Project (IHP), Gallamini and London criteria. Eur. J. Nucl. Med. Mol. Imaging 38, 1064–1071 (2011).

    PubMed  Google Scholar 

  78. Lim, E. et al. Guidelines on the radical management of patients with lung cancer. Thorax 65, iii1–iii27 (2010).

    PubMed  Google Scholar 

  79. Kako, S. et al. FDG-PET in T-cell and NK-cell neoplasms. Ann. Oncol. 18, 1685–1690 (2007).

    CAS  PubMed  Google Scholar 

  80. Perry, C. et al. Diagnostic accuracy of PET/CT in patients with extranodal marginal zone MALT lymphoma. Eur. J. Haematol. 79, 205–209 (2007).

    PubMed  Google Scholar 

  81. Bodet-Milin, C. et al. Prognostic impact of 18F-fluoro-deoxyglucose positron emission tomography in untreated mantle cell lymphoma: a retrospective study from the GOELAMS group. Eur. J. Nucl. Med. Mol. Imaging 37, 1633–1642 (2010).

    CAS  PubMed  Google Scholar 

  82. Friedberg, J. W. Relapsed/refractory diffuse large B-cell lymphoma. Hematology Am. Soc. Hematol. Educ. Program 2011, 498–505 (2011).

    PubMed  Google Scholar 

  83. Engert, A. et al. Reduced-intensity chemotherapy and PET-guided radiotherapy in patients with advanced stage Hodgkin's lymphoma (HD15 trial): a randomised, open-label, phase 3 non-inferiority trial. Lancet 379, 1791–1799 (2012).

    CAS  PubMed  Google Scholar 

  84. Dupuis, J. et al. Impact of [18F]fluorodeoxyglucose positron emission tomography response evaluation in patients with high-tumor burden follicular lymphoma treated with immunochemotherapy: a prospective study from the Groupe d'Etudes des Lymphomes de l'Adulte and GOELAMS. J. Clin. Oncol. 30, 4317–4322 (2012).

    CAS  PubMed  Google Scholar 

  85. Gallamini, A. 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. 25, 3746–3752 (2007).

    CAS  PubMed  Google Scholar 

  86. Moskowitz, C. H. et al. Risk-adapted dose-dense immunochemotherapy determined by interim FDG-PET in advanced-stage diffuse large B-cell lymphoma. J. Clin. Oncol. 28, 1896–1903 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Radford, J. et al. Results of a trial of PET-directed therapy for early-stage Hodgkin's lymphoma. N. Engl. J. Med. 372, 1598–1607 (2015).

    CAS  PubMed  Google Scholar 

  88. Raemaekers, J. M. M. et al. Omitting radiotherapy in early positron emission tomography-negative stage I/II Hodgkin lymphoma is associated with an increased risk of early relapse: clinical results of the preplanned interim analysis of the randomized EORTC/LYSA/FIL H10 trial. J. Clin. Oncol. 32, 1188–1194 (2014).

    PubMed  Google Scholar 

  89. Meyer, R. M. et al. ABVD alone versus radiation-based therapy in limited-stage Hodgkin's lymphoma. N. Engl. J. Med. 366, 399–408 (2012).

    CAS  PubMed  Google Scholar 

  90. Schaapveld, M. et al. Second cancer risk up to 40 years after treatment for Hodgkin's lymphoma. N. Engl. J. Med. 373, 2499–2511 (2015).

    CAS  PubMed  Google Scholar 

  91. Kumar, A. et al. Brentuximab vedotin and AVD followed by involved-site radiotherapy in early stage, unfavorable risk Hodgkin lymphoma. Blood 128, 1458–1464 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Barrington, S. F. & Mikhaeel, N. G. PET scans for staging and restaging in diffuse large B-cell and follicular lymphomas. Curr. Hematol. Malig. Rep. 11, 185–195 (2016).

    PubMed  PubMed Central  Google Scholar 

  93. Rapoport, A. P. et al. One hundred autotransplants for relapsed or refractory Hodgkin's disease and lymphoma: value of pretransplant disease status for predicting outcome. J. Clin. Oncol. 11, 2351–2361 (1993).

    CAS  PubMed  Google Scholar 

  94. Jagannath, S. et al. Prognostic factors for response and survival after high-dose cyclophosphamide, carmustine, and etoposide with autologous bone marrow transplantation for relapsed Hodgkin's disease. J. Clin. Oncol. 7, 179–185 (1989).

    CAS  PubMed  Google Scholar 

  95. Moskowitz, A. J. et al. Pretransplantation functional imaging predicts outcome following autologous stem cell transplantation for relapsed and refractory Hodgkin lymphoma. Blood 116, 4934–4937 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Moskowitz, C. H. Interim PET-CT in the management of diffuse large B-cell lymphoma. Hematology 2012, 397–401 (2012).

    PubMed  Google Scholar 

  97. Moskowitz, C. H. et al. High-dose chemo-radiotherapy for relapsed or refractory Hodgkin lymphoma and the significance of pre-transplant functional imaging: research paper. Br. J. Haematol. 148, 890–897 (2010).

    PubMed  PubMed Central  Google Scholar 

  98. Cocorocchio, E. et al. High-dose chemotherapy in relapsed or refractory Hodgkin lymphoma patients: a reappraisal of prognostic factors. Hematol. Oncol. 31, 34–40 (2013).

    CAS  PubMed  Google Scholar 

  99. Moskowitz, C. H. et al. Normalization of pre-ASCT, FDG-PET imaging with second-line, non-cross-resistant, chemotherapy programs improves event-free survival in patients with Hodgkin lymphoma. Blood 119, 1665–1670 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Moskowitz, A. J. et al. PET-adapted sequential salvage therapy with brentuximab vedotin followed by augmented ifosamide, carboplatin, and etoposide for patients with relapsed and refractory Hodgkin's lymphoma: a non-randomised, open-label, single-centre, phase 2 study. Lancet Oncol. 16, 284–292 (2015).

    CAS  PubMed  Google Scholar 

  101. Derenzini, E. et al. Pretransplantation positron emission tomography scan is the main predictor of autologous stem cell transplantation outcome in aggressive B-cell non-Hodgkin lymphoma. Cancer 113, 2496–2503 (2008).

    PubMed  Google Scholar 

  102. Dickinson, M. et al. Improved survival for relapsed diffuse large B cell lymphoma is predicted by a negative pre-transplant FDG-PET scan following salvage chemotherapy. Br. J. Haematol. 150, 39–45 (2010).

    PubMed  Google Scholar 

  103. Hoppe, B. S. et al. The role of FDG-PET imaging and involved field radiotherapy in relapsed or refractory diffuse large B-cell lymphoma. Bone Marrow Transplant. 43, 941–948 (2009).

    CAS  PubMed  Google Scholar 

  104. Sauter, C. S. et al. Prognostic value of FDG-PET prior to autologous stem cell transplantation for relapsed and refractory diffuse large B-cell lymphoma. Blood 125, 2579–2582 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Armand, P. et al. Prognostic factors for patients with diffuse large B cell lymphoma and transformed indolent lymphoma undergoing autologous stem cell transplantation in the positron emission tomography era. Br. J. Haematol. 160, 608–617 (2013).

    PubMed  Google Scholar 

  106. Reyal, Y. et al. Impact of pretransplantation 18F-fluorodeoxyglucose-positron emission tomography on survival outcomes after T cell-depleted allogeneic transplantation for Hodgkin lymphoma. Biol. Blood Marrow Transplant. 22, 1234–1241 (2016).

    PubMed  Google Scholar 

  107. Sauter, C. S. et al. Pretransplantation fluorine-18- deoxyglucose-positron emission tomography scan lacks prognostic value in chemosensitive B cell non-Hodgkin lymphoma patients undergoing nonmyeloablative allogeneic stem cell transplantation. Biol. Blood Marrow Transplant. 20, 881–903 (2014).

    PubMed  PubMed Central  Google Scholar 

  108. Bachanova, V. et al. Impact of pretransplantation 18F-fluorodeoxy glucose-positron emission tomography status on outcomes after allogeneic hematopoietic cell transplantation for non-Hodgkin lymphoma. Biol. Blood Marrow Transplant. 21, 1605–1611 (2015).

    PubMed  PubMed Central  Google Scholar 

  109. Armitage, J. O. Who benefits from surveillance imaging in lymphoma? J. Clin. Oncol. 30, 2579–2580 (2012).

    PubMed  Google Scholar 

  110. Dann, E. J. et al. Hodgkin lymphoma patients in first remission: routine positron emission tomography/computerized tomography imaging is not superior to clinical follow-up for patients with no residual mass. Br. J. Haematol. 164, 694–700 (2014).

    PubMed  Google Scholar 

  111. Thompson, C. A. et al. Utility of routine post-therapy surveillance imaging in diffuse large B-cell lymphoma. J. Clin. Oncol. 32, 3506–3512 (2014).

    PubMed  PubMed Central  Google Scholar 

  112. Cohen, J. B., Behera, M., Thompson, C. A. & Flowers, C. R. Evaluating surveillance imaging for diffuse large B-cell lymphoma and Hodgkin lymphoma. Blood 129, 561–564 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Lambert, J. R. et al. Prognostic role of PET scanning before and after reduced-intensity allogeneic stem cell transplantation for lymphoma. Blood 115, 2763–2768 (2010).

    CAS  PubMed  Google Scholar 

  114. Ulaner, G. A. et al. False-positive [18F]fluorodeoxyglucose-avid lymph nodes on positron emission tomography-computed tomography after allogeneic but not autologous stem-cell transplantation in patients with lymphoma. J. Clin. Oncol. 32, 51–56 (2013).

    PubMed  Google Scholar 

  115. Therasse, P., Eisenhauer, E. A. & Verweij, J. RECIST revisited: a review of validation studies on tumour assessment. Eur. J. Cancer 42, 1031–1039 (2006).

    CAS  PubMed  Google Scholar 

  116. Younes, A. et al. International Working Group consensus response evaluation criteria in lymphoma (RECIL 2017). Ann. Oncol. http://dx.doi.org/10.1093/annonc/mdx097 (2017).

  117. Kumar, A. et al. Definition of bulky disease in early stage Hodgkin lymphoma in computed tomography era: prognostic significance of measurements in the coronal and transverse planes. Haematologica 101, 1237–1243 (2016).

    PubMed  PubMed Central  Google Scholar 

  118. Zasadny, K. R., Kison, P. V., Francis, I. R. & Wahl, R. L. FDG-PET determination of metabolically active tumor volume and comparison with CT. Clin. Positron Imaging 1, 123–129 (1998).

    PubMed  Google Scholar 

  119. Larson, S. M. et al. Tumor treatment response based on visual and quantitative changes in global tumor glycolysis using PET-FDG imaging: the visual response score and the change in total lesion glycolysis. Clin. Positron Imaging 2, 159–171 (1999).

    PubMed  Google Scholar 

  120. Schöder, H. & Moskowitz, C. Metabolic tumor volume in lymphoma: hype or hope? J. Clin. Oncol. 34, 3591–3594 (2016).

    PubMed  Google Scholar 

  121. Ng, A. K., LaCasce, A. & Travis, L. B. Long-term complications of lymphoma and its treatment. J. Clin. Oncol. 29, 1885–1892 (2011).

    PubMed  Google Scholar 

  122. Lee, C. I., Haims, A. H., Monico, E. P., Brink, J. A. & Forman, H. P. Diagnostic CT scans: assessment of patient, physician, and radiologist awareness of radiation dose and possible risks. Radiology 231, 393–398 (2004).

    PubMed  Google Scholar 

  123. National Council on Radiation Protection and Measurements. Ionizing radiation exposure of the population of the United States http://dx.doi.org/10.1017/CBO9781107415324.004 (NCRP, 2009).

  124. Committee on Medical Aspects of Radiation in the Environment (COMARE). Patient radiation dose issues resulting from the use of CT in the UK (Public Health England, 2014).

  125. Pierce, D. A. & Preston, D. L. Radiation-related cancer risks at low doses among atomic bomb survivors. Radiat. Res. 154, 178–186 (2000).

    CAS  PubMed  Google Scholar 

  126. Cardis, E. et al. The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: estimates of radiation-related cancer risks. Radiat. Res. 167, 396–416 (2007).

    CAS  PubMed  Google Scholar 

  127. Shrimpton, P. C., Jansen, J. T. M. & Harrison, J. D. Updated estimates of typical effective doses for common CT examinations in the UK following the 2011 national review. Br. J. Radiol. 89, 20150346 (2016).

    PubMed  Google Scholar 

  128. Quinn, B., Dauer, Z., Pandit-Taskar, N., Schoder, H. & Dauer, L. T. Radiation dosimetry of 18F-FDG PET/CT: incorporating exam-specific parameters in dose estimates. BMC Med. Imaging 16, 41 (2016).

    PubMed  PubMed Central  Google Scholar 

  129. Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation. Health Risks from Exposure to Low Levels of Ionizing Radiation: BEIR VII Phase 2 (National Research Council of the National Academies, 2006).

  130. Brenner, D. J., Elliston, C. D., Hall, E. J. & Berdon, W. E. Estimated risks of radiation-induced fatal cancer from pediatric CT. AJR Am. J. Roentgenol. 176, 289–296 (2001).

    CAS  PubMed  Google Scholar 

  131. Pearce, M. S. et al. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet 380, 499–505 (2012).

    PubMed  PubMed Central  Google Scholar 

  132. Hicks, L. K. et al. The ASH Choosing Wisely campaign: five hematologic tests and treatments to question. Blood 122, 3879–3883 (2013).

    CAS  PubMed  Google Scholar 

  133. Howlader, N. et al. SEER Cancer Statistics Review, 1975–2013 (National Cancer Institute, 2015).

    Google Scholar 

  134. Lukes, R. J. Relationship of histologic features to clinical stages in Hodgkin's disease. Am. J. Roentgenol. Radium Ther. Nucl. Med. 90, 944–955 (1963).

    CAS  PubMed  Google Scholar 

  135. Coppleson, L., Rappaport, H., Strum, S. & Rose, J. Analysis of the Rye classification of Hodgkin's disease. The prognostic significance of cellular composition. J. Natl Cancer Inst. 51, 379–390 (1973).

    CAS  PubMed  Google Scholar 

  136. Richards, S. J. & Jack, A. S. The development of integrated haematopathology laboratories: a new approach to the diagnosis of leukaemia and lymphoma. Clin. Lab. Haematol. 25, 337–342 (2003).

    CAS  PubMed  Google Scholar 

  137. Meignan, M. et al. Report on the Third International Workshop on Interim Positron Emission Tomography in Lymphoma held in Menton, France, 26–27 September 2011 and Menton 2011 consensus. Leuk. Lymphoma 53, 1876–1881 (2012).

    PubMed  Google Scholar 

  138. Meignan, M. et al. Report on the 4th International Workshop on Positron Emission Tomography in Lymphoma held in Menton, France, 3–5 October 2012. Leuk. Lymphoma 55, 31–37 (2014).

    PubMed  Google Scholar 

  139. Meignan, M. et al. Report on the 5th International Workshop on Positron Emission Tomography in Lymphoma held in Menton, France, 19–20 September 2014. Leuk. Lymphoma 56, 1229–1232 (2015).

    PubMed  Google Scholar 

  140. Falchi, L. et al. Correlation between FDG/PET, histology, characteristics, and survival in 332 patients with chronic lymphoid leukemia. Blood 123, 2783–2791 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Arnold, C. W. et al. RadPath: a web-based system for integrating and correlating radiology and pathology findings during cancer diagnosis. Acad. Radiol. 23, 90–100 (2016).

    PubMed  Google Scholar 

  142. Ansell, S. M. et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N. Engl. J. Med. 372, 311–319 (2015).

    PubMed  Google Scholar 

  143. Han, H. S., Escalón, M. P., Hsiao, B., Serafini, A. & Lossos, I. S. High incidence of false-positive PET scans in patients with aggressive non-Hodgkin's lymphoma treated with rituximab-containing regimens. Ann. Oncol. 20, 309–318 (2009).

    CAS  PubMed  Google Scholar 

  144. Chanan-Khan, A. et al. Tumor flare reaction associated with lenalidomide treatment in patients with chronic lymphocytic leukemia predicts clinical response. Cancer 117, 2127–2135 (2011).

    CAS  PubMed  Google Scholar 

  145. Cheson, B. D. et al. Refinement of the Lugano classification lymphoma response criteria in the era of immunomodulatory therapy. Blood 128, 2489–2496 (2016).

    CAS  PubMed  Google Scholar 

  146. Cheson, B. D. et al. Novel targeted agents and the need to refine clinical end points in chronic lymphocytic leukemia. J. Clin. Oncol. 30, 2820–2822 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Byrd, J. C. et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N. Engl. J. Med. 371, 213–223 (2014).

    PubMed  PubMed Central  Google Scholar 

  148. Bottcher, S. et al. Minimal residual disease quantification is an independent predictor of progression-free and overall survival in chronic lymphocytic leukemia: a multivariate analysis from the randomized GCLLSG CLL8 trial. J. Clin. Oncol. 30, 980–988 (2012).

    PubMed  Google Scholar 

  149. Thompson, P. A. & Wierda, W. G. Eliminating minimal residual disease as a therapeutic endpoint: working toward cure for patients with CLL. Blood 127, 1–30 (2015).

    Google Scholar 

  150. Galimberti, S. et al. Minimal residual disease after conventional treatment significantly impacts on progression-free survival of patients with follicular lymphoma: the FIL FOLL05 trial. Clin. Cancer Res. 20, 6398–6405 (2014).

    CAS  PubMed  Google Scholar 

  151. Pott, C. et al. Molecular remission is an independent predictor of clinical outcome in patients with mantle cell lymphoma after combined immunochemotherapy: a European MCL Intergroup study. Blood 115, 3215–3223 (2010).

    CAS  PubMed  Google Scholar 

  152. van der Velder, V. H. & van Dongen, J. J. MRD detection in acute lymphoblastic leukemia patients using Ig/TCR gene rearrangements as targets for real-time quantitative PCR. Methods Mol. Biol. 538, 115–150 (2009).

    Google Scholar 

  153. Böttcher, S. et al. Minimal residual disease detection in mantle cell lymphoma: methods and significance of four-color flow cytometry compared to consensus IGH-polymerase chain reaction at initial staging and for follow-up examinations. Haematologica 93, 551–559 (2008).

    PubMed  Google Scholar 

  154. Pott, C. et al. MRD detection in B-cell non-Hodgkin lymphomas using Ig gene rearrangements and chromosomal translocations as targets for real-time quantitative PCR. Methods Mol. Biol. 971, 175–200 (2013).

    CAS  PubMed  Google Scholar 

  155. Ladetto, M. et al. Next-generation sequencing and real-time quantitative PCR for minimal residual disease detection in B-cell disorders. Leukemia 28, 1299–1307 (2014).

    CAS  PubMed  Google Scholar 

  156. Roschewski, M. et al. Circulating tumour DNA and CT monitoring in patients with untreated diffuse large B-cell lymphoma: a correlative biomarker study. Lancet Oncol. 16, 541–549 (2015).

    PubMed  PubMed Central  Google Scholar 

  157. Kurtz, D. M. et al. Noninvasive monitoring of diffuse large B-cell lymphoma by immunoglobulin high-throughput sequencing. Blood 125, 3679–3687 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Bohers, E. et al. Somatic mutations of cell-free circulating DNA detected by next-generation sequencing reflect the genetic changes in both germinal center B-cell-like and activated B-cell-like diffuse large B-cell lymphomas at the time of diagnosis. Haematologica 100, e280–e284 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Vandenberghe, P. et al. Non-invasive detection of genomic imbalances in Hodgkin/Reed-Sternberg cells in early and advanced stage Hodgkin's lymphoma by sequencing of circulating cell-free DNA: a technical proof-of-principle study. Lancet Haematol. 2, e55–e65 (2015).

    PubMed  Google Scholar 

  160. Luminari, S. et al. Positron emission tomography response and minimal residual disease impact on progression-free survival in patients with follicular lymphoma. A subset analysis from the FOLL05 trial of the Fondazione Italiana Linfom. Haematologica 101, e66–e68 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Mansfield, P. & Maudsley, A. A. Medical imaging by NMR. Br. J. Radiol. 50, 188–194 (1977).

    CAS  PubMed  Google Scholar 

  162. Takahara, T. et al. Diffusion weighted whole body imaging with background body signal suppression (DWIBS): technical improvement using free breathing, STIR and high resolution 3D display. Radiat. Med. 22, 275–282 (2004).

    PubMed  Google Scholar 

  163. Punwani, S. et al. Quantitative diffusion weighted MRI: a functional biomarker of nodal disease in Hodgkin lymphoma? Cancer Biomark. 7, 249–259 (2010).

    PubMed  Google Scholar 

  164. Mayerhoefer, M. E. et al. Evaluation of diffusion-weighted MRI for pretherapeutic assessment and staging of lymphoma: results of a prospective study in 140 patients. Clin. Cancer Res. 20, 2984–2993 (2014).

    PubMed  Google Scholar 

  165. Mayerhoefer, M. E. et al. Evaluation of diffusion-weighted magnetic resonance imaging for follow-up and treatment response assessment of lymphoma: results of an 18F-FDG-PET/CT-controlled prospective study in 64 patients. Clin. Cancer Res. 21, 2506–2513 (2015).

    CAS  PubMed  Google Scholar 

  166. Huang, M. Q. et al. Monitoring response to chemotherapy of non-Hodgkin's lymphoma xenografts by T2-weighted and diffusion-weighted MRI. NMR Biomed. 21, 1021–1029 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Chen, Y., Zhong, J., Wu, H. & Chen, N. The clinical application of whole-body diffusion-weighted imaging in the early assessment of chemotherapeutic effects in lymphoma: the initial experience. Magn. Reson. Imaging 30, 165–170 (2012).

    PubMed  Google Scholar 

  168. Hagtvedt, T. et al. Diffusion-weighted MRI compared to FDG PET/CT for assessment of early treatment response in lymphoma. Acta Radiol. 56, 152–158 (2015).

    PubMed  Google Scholar 

  169. Littooij, A. S. et al. Whole-body MRI-DWI for assessment of residual disease after completion of therapy in lymphoma: a prospective multicenter study. J. Magn. Reson. Imaging 42, 1646–1655 (2015).

    PubMed  Google Scholar 

  170. Pichler, B. J., Judenhofer, M. S. & Wehrl, H. F. PET/MRI hybrid imaging: devices and initial results. Eur. Radiol. 18, 1077–1086 (2008).

    PubMed  Google Scholar 

  171. Lishner, M. et al. Hematologic malignancies in pregnancy: management guidelines from an international consensus meeting. J. Clin. Oncol. 34, 501–508 (2016).

    CAS  PubMed  Google Scholar 

  172. Shields, A. F. et al. Imaging proliferation in vivo with [F-18]FLT and positron emission tomography. Nat. Med. 4, 1334–1336 (1998).

    CAS  PubMed  Google Scholar 

  173. Buck, A. K. et al. 3-deoxy-3-[18F]fluorothymidine-positron emission tomography for noninvasive assessment of proliferation in pulmonary nodules. Cancer Res. 62, 3331–3334 (2002).

    CAS  PubMed  Google Scholar 

  174. Minamimoto, R. et al. Diffuse large B-cell lymphoma: prospective multicenter comparison of early interim FLT PET/CT versus FDG PET/CT with IHP, EORTC, Deauville, and PERCIST criteria for early therapeutic monitoring. Radiology 280, 220–229 (2016).

    PubMed  Google Scholar 

  175. Schöder, H. et al. Prospective study of 3′-deoxy-3′-18F-fluorothymidine PET for early interim response assessment in advanced stage B-cell lymphoma. J. Nucl. Med. 57, 728–734 (2016).

    PubMed  Google Scholar 

  176. Rice, S. L., Roney, C. A., Daumar, P. & Lewis, J. S. The next generation of positron emission tomography radiopharmaceuticals in oncology. Semin. Nucl. Med. 41, 265–282 (2011).

    PubMed  PubMed Central  Google Scholar 

  177. Lam, W. W. C. et al. Promising role of [18F] fluorocholine PET/CT versus [18F] fluorodeoxyglucose PET/CT in primary brain tumors — early experience. Clin. Neurol. Neurosurg. 113, 156–161 (2011).

    PubMed  Google Scholar 

  178. Segal, E. et al. Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat. Biotechnol. 25, 675–680 (2007).

    CAS  PubMed  Google Scholar 

  179. Colen, R. et al. NCI workshop report: clinical and computational requirements for correlating imaging phenotypes with genomics signatures. Transl Oncol. 7, 556–569 (2014).

    PubMed  PubMed Central  Google Scholar 

  180. Aerts, H. J. W. L. et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat. Commun. 5, 4006 (2014).

    CAS  PubMed  Google Scholar 

  181. Gerlinger, M. et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883–892 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Tomita, N. et al. Central nervous system event in patients with diffuse large B-cell lymphoma in the rituximab era. Cancer Sci. 103, 245–251 (2012).

    CAS  PubMed  Google Scholar 

  183. Fletcher, C. D. & Kahl, B. S. Central nervous system involvement in diffuse large B-cell lymphoma: an analysis of risks and prevention strategies in the post-rituximab era. Leuk. Lymphoma 55, 2228–2240 (2014).

    CAS  PubMed  Google Scholar 

  184. McMillan, A. et al. Guideline on the prevention of secondary central nervous system lymphoma. Br. J. Haematol. 163, 168–181 (2013).

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  186. Wilks, S. Cases of enlargement of the lymphatic glands and spleen, (or Hodgkin's disease) with remarks. Guys Hosp. Rep. 11, 56–67 (1865).

    Google Scholar 

  187. Trousseau, A. in Lectures on Clinical Medicine 180–211 (The New Sydenham Society, 1868).

    Google Scholar 

  188. Anglesio, E. The Treatment of Hodgkin's Disease (Springer, 1969).

    Google Scholar 

  189. Röntgen, W. K. A new form of radiation. Science 3, 726–729 (1896).

    PubMed  Google Scholar 

  190. Reed, D. M. On the pathological changes in Hodgkin's disease, with especial reference to its relationship to tuberculosis. Johns Hopkins Hosp. Rep. 10, 113–196 (1902).

    Google Scholar 

  191. Kinmonth, J. B. Lymphangiography in clinical surgery and particularly in the treatment of lymphoedema. Ann. R. Coll. Surg. Engl. 15, 300–315 (1954).

    CAS  PubMed  PubMed Central  Google Scholar 

  192. Hudack, S. S. & McMaster, P. D. The lymphatic participation in human cutaneous phenomena; a study of the minute lymphatics of the living skin. J. Exp. Med. 57, 751–774 (1933).

    CAS  PubMed  PubMed Central  Google Scholar 

  193. Gall, E. A. & Mallory, T. B. Malignant lymphoma: a clinico-pathologic survey of 618 cases. Am. J. Pathol. 18, 381–429 (1942).

    CAS  PubMed  PubMed Central  Google Scholar 

  194. Craver, L. F. Recent advances in treatment of lymphomas, leukemias and allied disorders. Bull. N. Y. Acad. Med. 24, 3–25 (1948).

    CAS  PubMed  PubMed Central  Google Scholar 

  195. Jackson, H. & Parker, F. Hodgkin's Disease and Allied Disorders (Oxford Univ. Press, 1947).

    Google Scholar 

  196. Peters, M. V. A study of survivals in Hodgkin's disease treated radiologically. Am. J. Roentgenol. Radium Ther. 63, 299–311 (1950).

    Google Scholar 

  197. Rappaport, H., Winter, W. & Hicks, E. Follicular lymphoma: a re-evaluation of its position in the scheme of malignant lymphoma based on a survey of 253 cases. Cancer 9, 792–814 (1956).

    PubMed  Google Scholar 

  198. Rappaport, H. in Atlas of Tumor Pathology Section III, Fascicle 8 (Armed Forces Institute of Pathology, 1966).

    Google Scholar 

  199. Phelps, M. E., Hoffman, E. J., Mullani, N. A. & Ter-Pogossian, M. M. Application of annihilation coincidence detection to transaxial reconstruction tomography. J. Nucl. Med. 16, 210–224 (1975).

    CAS  PubMed  Google Scholar 

  200. Lauterbur, P. C. Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature 242, 190–191 (1973).

    CAS  Google Scholar 

  201. Lukes, R. J. & Collins, R. D. Immunologic characterization of human malignant lymphomas. Cancer 34, 1488–1503 (1974).

    Google Scholar 

  202. Gerard-Marchant, R. et al. Classification of non-Hodgkin's lymphomas. Lancet 2, 406–408 (1974).

    Google Scholar 

  203. [No authors listed.] National Cancer Institute sponsored study of classifications of non-Hodgkin's lymphomas; summary and description of a working formulation for clinical usage. The Non-Hodgkin's Lymphoma Pathologic Classification Project. Cancer 49, 2112–2135 (1982).

  204. Harris, N. L. et al. A revised European-American classification of lymphoid neoplasms: Blood 84, 1361–1392 (1994).

    CAS  PubMed  Google Scholar 

  205. Jaffe, E. S., Harris, N. L., Stein, H. & Vardiman, J. W. Tumors of Haematopoietic and Lymphoid Tissues (IARC Press, 2001).

    Google Scholar 

  206. Swerdlow, S. H. et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues (IARC Press, 2008).

    Google Scholar 

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Acknowledgements

We are grateful to Hannah Holmes of the Royal Marsden Hospital for providing secretarial and research support, Isabel Castellano of the Royal Marsden Hospital for providing medical physics-related collaborative input, and to Barry Jenkins of the Institute of the Cancer Research Library Service for obtaining the original historical references from The British Library.

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  1. Joel Cunningham and Sunil Iyengar are at the Department of Haemato-Oncology, Royal Marsden Hospital, Fulham Road, London SW3 6JJ, UK.,

    Joel Cunningham & Sunil Iyengar

  2. Bhupinder Sharma is at the Department of Radiology, Royal Marsden Hospital, Fulham Road, London SW3 6JJ, UK.,

    Bhupinder Sharma

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Cunningham, J., Iyengar, S. & Sharma, B. Evolution of lymphoma staging and response evaluation: current limitations and future directions. Nat Rev Clin Oncol 14, 631–645 (2017). https://doi.org/10.1038/nrclinonc.2017.78

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