Abstract
The staging of Hodgkin lymphoma lays the groundwork for optimal treatment decision making. For a long time, bone marrow assessment has been an integral part of staging. The study of bone marrow involvement in tumor progression includes radiological method and morphological analysis of its core biopsy samples. During the last five decades of using bone marrow core biopsy, the attitude of oncologists and hematologists to this invasive and painful procedure remained ambivalent between denying and affirming the need to carry it out in all or most Hodgkin lymphoma cases. The present review provides the historical background of bone marrow core biopsy and considers its appropriateness for patients with classical Hodgkin lymphoma.
References
- Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. doi: 10.3322/caac.21708.
- Sasse S, Brockelmann PJ, Goergen H, et al. Long-Term Follow-Up of Contemporary Treatment in Early-Stage Hodgkin Lymphoma: Updated Analyses of the German Hodgkin Study Group HD7, HD8, HD10, and HD11 Trials. J Clin Oncol. 2017;35:1999–2007. doi: 10.1200/JCO.2016.70.9410.
- Subramanian G, Basu D, Badhe B, Dutta TK. Role of bone marrow trephine biopsy in the diagnosis of marrow involvement in Hodgkin’s disease. Indian J Pathol Microbiol. 2007;50(3):640–3.
- Weiler-Sagie M, Kagna O, Dann EJ, et al. Characterizing bone marrow involvement in Hodgkin’s lymphoma by FDG-PET/CT. Eur J Nucl Med Mol Imaging. 2014;41(6):1133–40. doi: 10.1007/s00259-014-2706-x
- Ghedini G. Per la patogenesi e per la diagnosi delle malattie del sangue e degli organi emopoietici, punture esplorativa del midollo osseo. Clinic Medica Italiana. 1908;47:724–36.
- Seyfarth C. Eine einfache Methode zur diagnostichen Entnahme von Knochenmark beim Lebenden. Arch fur Schiffs-und Tropen-Hygiene, Pathologie und Therapie exotischer Krankheiten. 1922;26:337–41.
- Arinkin MI. Die Intravitale Untersuchungsmethodik des Knochenmarks. Folia Haematologica. 1929;38:233–40.
- Arjeff MJ. Zur Methodik der Diagnostischen Punktion des Brustbeines. Folia Haematologica. 1931;45:55.
- Воробьев А.И. И.А. Кассирский и его вклад в медицину. М.: Медицина, 1988.
- [Vorob’ev AI. I.A. Kassirskii i ego vklad v meditsinu. (I.A. Kassirskii and his contribution to medicine.) Moscow: Meditsina; 1988. (In Russ)]
- Rubinstein MA. The technic and diagnostic value of aspiration of bone marrow from the iliac crest. Ann Intern Med. 1950;32:1905–8.
- Bierman HR. Bone marrow aspiration of the posterior iliac crest, an additional safe site. California Med. 1952;77:138–9.
- Jamshidi K, Swaim WR. Bone marrow biopsy with unaltered architecture: a new biopsy device. J Lab Clin Med. 1971;77(2):335–42.
- Hernandez-Garcia MT, Hernandez-Nieto L, Perez-Gonzalez E, Brito-Barroso ML. Bone marrow trephine biopsy: anterior superior iliac spine versus posterior superior iliac spine. Clin Lab Haematol. 1993;15(1):15–9. doi: 10.1111/j.1365-2257.1993.tb00117.x.
- Tomasian A, Jennings JW. Bone marrow aspiration and biopsy: techniques and practice implications. Skeletal Radiol. 2022;51(1):81–8. doi: 10.1007/s00256-021-03882-w.
- Draganski E, Deason T, Craig FE. Bone Marrow Aspiration and Biopsy Performed by RNs: A Review of Clinical Practice. Am J Nurs. 2019;119(9):47–53. doi: 10.1097/01.NAJ.0000580260.18537.ca.
- Криволапов Ю.А. Биопсия костного мозга: научно-практическое издание. М.: Практическая медицина, 2014. 528 с.
- [Krivolapov YuA. Biopsiya kostnogo mozga: nauchno-prakticheskoe izdanie. (Bone marrow biopsy: research and practice edition.) Moscow: Prakticheskaya meditsina Publ.; 2014. 528 p. (In Russ)]
- Howell SJ, Grey M, Changet L, 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. doi: 10.1046/j.1365-2141.2002.03842.x.
- 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. doi: 10.1159/000101712.
- 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. doi: 10.7326/0003-4819-82-3-365.
- Levis A, Pietrasanta D, Godio L, et al. A large-scale study of bone marrow involvement in patients with Hodgkin’s lymphoma. Clin Lymphoma. 2004;5(1):50–5. doi: 10.3816/clm.2004.n.010.
- Wang J, Weiss LM, Chang KL, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer. 2002;94(5):1522–31. doi: 10.1002/cncr.10364.
- Menon NC, Buchanan JG. Bilateral trephine bone marrow biopsies in Hodgkin’s and non-Hodgkin’s lymphoma. Pathology. 1979;11(1):53–7. doi: 10.3109/00313027909063538.
- Almeida J, Garcia-Marcos MA, Vallejo C, et al. Results of a series of 104 consecutive bilateral bone marrow biopsy specimens in lymphoproliferative disorders. Sangre (Barc). 1995;40(5):365–8.
- Luoni M, Fava S, Declich PJ. Bone marrow biopsy for staging Hodgkin’s lymphoma: the value of bilateral or unilateral trephine biopsy. J Clin Oncol. 1996;14(2):682–3. doi: 10.1200/JCO.1996.14.2.682.
- Kluin-Nelemans HC, Noordijk EM. Staging of patients with Hodgkin’s disease: what should be done? Leukemia. 1990;4(2):132–5.
- Bartl R, Frisch B, Burkhardt R, et al. Assessment of bone marrow histology in the malignant lymphomas (non-Hodgkin’s): correlation with clinical factors for diagnosis, prognosis, classification and staging. Br J Haematol. 1982;51(4):511–30. doi: 10.1111/j.1365-2141.1982.tb02815.x.
- Straus DJ, Gaynor JJ, Myers J, et al. Prognostic factors among 185 adults with newly diagnosed advanced Hodgkin’s disease treated with alternating potentially noncross-resistant chemotherapy and intermediate-dose radiation therapy. J Clin Oncol. 1990;8(7):1173–86. doi: 10.1200/JCO.1990.8.7.1173.
- Даниленко А.А. Поражение костного мозга у больных лимфогранулематозом (диагностика, клинические формы, патогенез): Автореф. дис. … канд. мед. наук. М., 2004.
- [Danilenko AA. Porazhenie kostnogo mozga u bolnykh limfogranulematozom (diagnostika, klinicheskie formy, patogenez). (Bone marrow lesions in Hodgkin lymphoma patients (diagnosis, clinical presentations, pathogenesis). [dissertation] Moscow; 2004. (In Russ)]
- Kaplan HS. Contiguity and progression in Hodgkin’s disease. Cancer Res. 1971;31(11):1811–3.
- Macintyre EA, Vaughan Hudson B, Linch DC, et al. The value of staging bone marrow trephine biopsy in Hodgkin’s disease. Eur J Haematol. 1987;39(1):66–70. doi: 10.1111/j.1600-0609.1987.tb00166.x.
- Carbone PP, Kaplan HS, Musshoff K, et al. Report of the Committee on Hodgkin’s Disease Staging Classification. Cancer Res. 1971;31(11):1860–1.
- Hines-Thomas MR, Howard SC, Hudson MM, et al. Utility of bone marrow biopsy at diagnosis in pediatric Hodgkin’s lymphoma. Haematologica. 2010;95(10):1691–6. doi: 10.3324/haematol.2010.025072.
- Ellis ME, Diehl LF, Granger E, Elson E. Trephine needle bone marrow biopsy in the initial staging of Hodgkin disease: sensitivity and specificity of the Ann Arbor staging procedure criteria. Am J Hematol. 1989;30(3):115–20. doi: 10.1002/ajh.2830300302.25.
- Doll DC, Ringenberg QS, Anderson SP, et al. Bone marrow biopsy in the initial staging of Hodgkin’s disease. Med Pediatr Oncol. 1989;17(1):1–5. doi: 10.1002/mpo. 2950170102.
- Munker R, Hasenclever D, Brosteanu O, et al. Bone marrow involvement in Hodgkin’s disease: an analysis of 135 consecutive cases. German Hodgkin’s Lymphoma Study Group. J Clin Oncol. 1995;13(2):403–9. doi: 10.1200/JCO.1995.13.2.403.
- Howard MR, Taylor PR, Lucraft HH, et al. Bone marrow examination in newly diagnosed Hodgkin’s disease: current practice in the United Kingdom. Br J Cancer. 1995;71(1):210–2. doi: 10.1038/bjc.1995.43.
- MacCormick R, Covert A, Gross M. Primary bony involvement in Hodgkin’s disease. CMAJ. 1989;140(9):1059–60.
- Borg MF, Chowdhury AD, Bhoopal S, Benjamin CS. Bone involvement in Hodgkin’s disease. Australas Radiol. 1993;37(1):63–6. doi: 10.1111/j.1440-1673.1993.tb 00011.x.
- Ostrowski ML, Inwards CY, Strickler JG. Osseous Hodgkin disease. Cancer. 1999;85(5):1166–78. doi: 10.1002/(sici)1097-0142(19990301)85:5<1166::aid-cncr22>3.0.co;2-v.
- Langley CR, Garrett SJ, Urand J, et al. Primary multifocal osseous Hodgkin’s lymphoma. World J Surg Oncol. 2008;6:34. doi: 10.1186/1477-7819-6-34.
- Anderson KC, Kaplan WD, Leonard RC, et al. Role of 99mTc methylene diphosphonate bone imaging in the management of lymphoma. Cancer Treat Rep. 1985;69(12):1347–51.
- Ferrant A, Rodhain J, Michaux JL, et al. Detection of skeletal involvement in Hodgkin’s disease: A comparison of radiography, bone scanning, and bone marrow biopsy in 38 patients. Cancer. 1975;35(5):1346–53. doi: 10.1002/1097-0142(197505)35:5<1346::aid-cncr2820350516>3.0.co;2-i.
- Daffner RH, Lupetin AR, Dash N, et al. MRI in the detection of malignant infiltration of bone marrow. Am J Roentgenol. 1986;146(2):353–8. doi: 10.2214/ajr.146.2.353.
- Vogler JB, Murphy WA. Bone marrow imaging. Radiology. 1988;168(3):679–93. doi: 10.1148/radiology.168.3.3043546.
- Guckel F, Semmler W, Dohner H, et al. NMR tomographic imaging of bone marrow infiltrates in malignant lymphoma. Rofo. 1989;150(1):26–31. doi: 10.1055/s-2008-1046968.
- Chiarilli MG, Delli Pizzi A, Mastrodicasa D, et al. Bone marrow magnetic resonance imaging: physiologic and pathologic findings that radiologist should know. Radiol Med. 2021;126(2):264–76. doi: 10.1007/s11547-020-01239-2.
- Hoane BR, Shields AF, Porter BA, Shulman HM. Detection of lymphomatous bone marrow involvement with magnetic resonance imaging. Blood. 1991;78(3):728–38.
- Dohner H, Guckel F, Knauf W, et al. Magnetic resonance imaging of bone marrow in lymphoproliferative disorders: correlation with bone marrow biopsy. Br J Haematol. 1989;73(1):12–7. doi: 10.1111/j.1365-2141.1989.tb00211.x.
- Linden A, Zankovich R, Theissen P, et al. Malignant lymphoma: bone marrow imaging versus biopsy. Radiology. 1989;173(2):335–9. doi: 10.1148/radiology.173.2.2678249.
- Shields AF, Porter BA, Churchley S, et al. The detection of bone marrow involvement by lymphoma using magnetic resonance imaging. J Clin Oncol. 1987;5(2):225–30. doi: 10.1200/JCO.1987.5.2.225.
- Tardivon AA, Munck JN, Shapeero LG. Can clinical data help to screen patients with lymphoma for MR imaging of bone marrow? Ann Oncol. 1995;6(8):795–800. doi: 10.1093/oxfordjournals.annonc.a059318.
- Skillings JR, Bramwell V, Nicholson RL, et al. A prospective study of magnetic resonance imaging in lymphoma staging. Cancer. 1991;67(7):1838–43. doi: 10.1002/1097-0142(19910401)67:7<1838::aid-cncr2820670704>3.0.co;2-o.
- Vinnicombe SJ, Reznek RH. Computerised tomography in the staging of Hodgkin’s disease and non-Hodgkin’s lymphoma. Eur J Nucl Med Mol Imaging. 2003;30(Suppl 1):S42–S55. doi: 10.1007/s00259-003-1159-4.
- Kniseley RM, Andrews GA, Edwards CL, Hayes RL. Bone-marrow and skeletal scanning. Radiol Clin North Am. 1969;7(2):265–80.
- Lilien DL, Berger HG, Anderson DP, Bennett LR. 111 In-chloride: a new agent for bone marrow imaging. J Nucl Med. 1973;14(3):184–6.
- Krause T, Eisenmann N, Reinhardt M, et al. Bone marrow scintigraphy using technetium-99m antigranulocyte antibody in malignant lymphomas. Ann Oncol. 1999;10(1):79–85. doi: 10.1023/a:1008356910239.
- Lister TA, Crowther D, Sutcliffe SB, 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. doi: 10.1200/JCO.1989.7.11.1630.
- Dahlbom M, Hoffman EJ, Hoh CK, et al. Whole-body positron emission tomography: Part I. Methods and performance characteristics. J Nucl Med. 1992;33(6):1191–9.
- Hoh CK, Hawkins RA, Glaspy JA, et al. Cancer detection with whole-body PET using 2-[18F]fluoro-2-deoxy-D-glucose. J Comput Assist Tomogr. 1993;17(4):582–9. doi: 10.1097/00004728-199307000-00012.
- Basu S, Hess S, Nielsen Braad PE, et al. The Basic Principles of FDG-PET/CT Imaging. PET Clin. 2014;9(4):355–70. doi: 10.1016/j.cpet.2014.07.006.
- Paul R. Comparison of fluorine-18-2-fluorodeoxyglucose and gallium-67 citrate imaging for detection of lymphoma. J Nucl Med. 1987;28(3):288–92.
- Newman JS, Francis IR, Kaminski MR, Wahl RL. Imaging of lymphoma with PET with 2-[F-18]-fluoro-2-deoxy-D-glucose: correlation with CT. Radiology. 1994;190(1):111–6. doi: 10.1148/radiology.190.1.8259386.
- Hoh CK, Glaspy J, Rosen P, et al. Whole-body FDG-PET imaging for staging of Hodgkin’s disease and lymphoma. J Nucl Med. 1997;38(3):343–8.
- Buchmann I, Reinhardt M, Elsner K, 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. 2001;91(5):889–99.
- Schaefer NG, Hany TF, Taverna C et al. Non-Hodgkin lymphoma and Hodgkin disease: coregistered FDG PET and CT at staging and restaging – do we need contrast-enhanced CT? Radiology. 2004;232(3):823–9. doi: 10.1148/radiol.2323030985.
- Hoh CK, Hawkins RA, Dahlbom M, et al. Whole body skeletal imaging with [18F]fluoride ion and PET. J Comput Assist Tomogr. 1993;17(1):34–41. doi: 10.1097/00004728-199301000-00005.
- Bangerter M, Moog F, Buchmann I, et al. Whole-body 2-[18F]-fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) for accurate staging of Hodgkin’s disease. Ann Oncol. 1998;9(10):1117–22. doi: 10.1023/a:1008486928190.
- Meignan M, Gallamini A, Haioun C. Report on the First International Workshop on Interim-PET-Scan in Lymphoma. Leuk Lymphoma. 2009;50(8):1257–60. doi: 10.1080/10428190903040048.
- Barrington SF, Mikhaeel NG, Kostakoglu L, 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. 2014;32(27):3048–58. doi: 10.1200/JCO.2013.53.5229.
- Moulin-Romsee G, Hindie E, Cuenca X, et al. (18)F-FDG PET/CT bone/bone marrow findings in Hodgkin’s lymphoma may circumvent the use of bone marrow trephine biopsy at diagnosis staging. Eur J Nucl Med Mol Imaging. 2010;37(6):1095–105. doi: 10.1007/s00259-009-1377-5.
- Adams HJ, Kwee TC, de Keizer B, et al. Systematic review and meta-analysis on the diagnostic performance of FDG-PET/CT in detecting bone marrow involvement in newly diagnosed Hodgkin lymphoma: is bone marrow biopsy still necessary? Ann Oncol. 2014;25(5):921–7. doi: 10.1093/annonc/mdt533.
- Cheson BD, Fisher RI, Barrington SF, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32(27):3059–68. doi: 10.1200/JCO.2013.54.8800.
- Puccini B, Nassi L, Minoia C, et al. Role of bone marrow biopsy in staging of patients with classical Hodgkin’s lymphoma undergoing positron emission tomography/computed tomography. Ann Hematol. 2017;96(7):1147–53. doi: 10.1007/s00277-017-2996-8.
- Voltin CA, Goergen H, Baues C, et al. Value of bone marrow biopsy in Hodgkin lymphoma patients staged by FDG PET: results from the German Hodgkin Study Group trials HD16, HD17, and HD18. Ann Oncol. 2018;29(9):1926–31. doi: 10.1093/annonc/mdy250.
- Gallamini A. Hodgkin lymphoma staging 50 years later: no more knives or needles! Ann Oncol. 2018;29(9):1892–3. doi: 10.1093/annonc/mdy262.
- Gaudio F, Pedote P, Niccoli Asabella A, et al. Bone Involvement in Hodgkin’s Lymphoma: Clinical Features and Outcome. Acta Haematol. 2018;140(3):178–82. doi: 10.1159/000490489.
- Kwee TC, de Klerk JMH, Nix M, et al. Benign Bone Conditions That May Be FDG-avid and Mimic Malignancy. Semin Nucl Med. 2017;47(4):322–51. doi: 10.1053/j.semnuclmed. 2017.02.004.
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