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Erschienen in: International Journal of Hematology 5/2021

30.01.2021 | Original Article

Biopsy remains indispensable for evaluating bone marrow involvement in DLBCL patients despite the use of positron emission tomography

verfasst von: Yusuke Saiki, Naoto Tomita, Akiko Uchida, Yu Uemura, Yoshinori Suzuki, Tsuneaki Hirakawa, Masayuki Kato, Masahiro Hoshikawa, Tsuyoshi Kawano, Naoya Nakamura, Ikuo Miura, Ayako Arai

Erschienen in: International Journal of Hematology | Ausgabe 5/2021

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Abstract

Initial staging by positron emission tomography/computed tomography (PET/CT) scanning is recommended for patients with diffuse large B-cell lymphoma (DLBCL). Whether both PET/CT and bone marrow biopsy (BMB) are required remains unclear. This study examined whether staging by PET/CT is sufficient. Participants with untreated DLBCL assessed using both PET/CT and BMB were included. Patients received independent diagnostic assessments from a radiologist and a hematopathologist. Both hematoxylin–eosin staining and CD20 immunostaining were performed to determine the bone marrow involvement in BMB. A total of 84 patients were included. The number of patients with positive bone marrow involvement identified by PET/CT and BMB was 16 (19%) and 22 (26%), respectively. Eight (10%) patients showed positive results in both tests. When considering BMB as a reference, PET/CT showed 36% sensitivity and 87% specificity, with positive and negative predictive values of 50% and 79%, respectively. BMB-positive patients had shorter progression-free (PFS) and overall (OS) survival than their BMB-negative counterparts. Compared to PET/CT-negative patients, patients with positive results did not show any significant differences in PFS and OS. However, among 16 PET/CT-positive patients, poor PFS and OS were observed among patients who were also BMB positive. BMB remains a mandatory step in staging of untreated DLBCL patients.
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Literatur
1.
Zurück zum Zitat The Non-Hodgkin’s Lymphoma Classification Project. A clinical evaluation of the international lymphoma study group classification of non-Hodgkin’s lymphoma. Blood. 1997;89:3909–18.CrossRef The Non-Hodgkin’s Lymphoma Classification Project. A clinical evaluation of the international lymphoma study group classification of non-Hodgkin’s lymphoma. Blood. 1997;89:3909–18.CrossRef
2.
Zurück zum Zitat Chung R, Lai R, Wei P, Lee J, Hanson J, Belch AR, et al. Concordant but not discordant bone marrow involvement in diffuse large B-cell lymphoma predicts a poor clinical outcome independent of the international prognostic index. Blood. 2007;110:1278–82.CrossRef Chung R, Lai R, Wei P, Lee J, Hanson J, Belch AR, et al. Concordant but not discordant bone marrow involvement in diffuse large B-cell lymphoma predicts a poor clinical outcome independent of the international prognostic index. Blood. 2007;110:1278–82.CrossRef
3.
Zurück zum Zitat Sehn LH, Scott DW, Chhanabhai M, Berry B, Ruskova A, Berkahn L, et al. Impact of concordant and discordant bone marrow involvement on outcome in diffuse large B-cell lymphoma treated with R-CHOP. J Clin Oncol. 2011;29:1452–7.CrossRef Sehn LH, Scott DW, Chhanabhai M, Berry B, Ruskova A, Berkahn L, et al. Impact of concordant and discordant bone marrow involvement on outcome in diffuse large B-cell lymphoma treated with R-CHOP. J Clin Oncol. 2011;29:1452–7.CrossRef
4.
Zurück zum Zitat Adams HJ, Nievelstein RA, Kwee TC. Opportunities and limitations of bone marrow biopsy and bone marrow FDG-PET in lymphoma. Blood Rev. 2015;29:417–25.CrossRef Adams HJ, Nievelstein RA, Kwee TC. Opportunities and limitations of bone marrow biopsy and bone marrow FDG-PET in lymphoma. Blood Rev. 2015;29:417–25.CrossRef
5.
Zurück zum Zitat Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059–68.CrossRef Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059–68.CrossRef
6.
Zurück zum Zitat International Non-Hodgkin’s Lymphoma Prognostic Factors Project. A predictive model for aggressive non-Hodgkin’s lymphoma. N Engl J Med. 1993;329:987–94.CrossRef International Non-Hodgkin’s Lymphoma Prognostic Factors Project. A predictive model for aggressive non-Hodgkin’s lymphoma. N Engl J Med. 1993;329:987–94.CrossRef
7.
Zurück zum Zitat Tomita N, Sakai R, Fujisawa S, Fujimaki K, Taguchi J, Hashimoto C, et al. SIL index, comprising stage, soluble interleukin-2 receptor, and lactate dehydrogenase, is a useful prognostic predictor in diffuse large B-cell lymphoma. Cancer Sci. 2012;103:1518–23.CrossRef Tomita N, Sakai R, Fujisawa S, Fujimaki K, Taguchi J, Hashimoto C, et al. SIL index, comprising stage, soluble interleukin-2 receptor, and lactate dehydrogenase, is a useful prognostic predictor in diffuse large B-cell lymphoma. Cancer Sci. 2012;103:1518–23.CrossRef
8.
Zurück zum Zitat Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer. 2002;94:1522–31.CrossRef Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer. 2002;94:1522–31.CrossRef
9.
Zurück zum Zitat Kim B, Lee ST, Kim HJ, Kim SH. Bone marrow flow cytometry in staging of patients with B-cell non-Hodgkin lymphoma. Ann Lab Med. 2015;35:187–93.CrossRef Kim B, Lee ST, Kim HJ, Kim SH. Bone marrow flow cytometry in staging of patients with B-cell non-Hodgkin lymphoma. Ann Lab Med. 2015;35:187–93.CrossRef
10.
Zurück zum Zitat Cabezas-Quintario MA, Gomez P, Yuste-Del Pozo V, Valencia-Mesa AL, Sosa G, Ricard P, et al. Bone marrow trephine biopsy involvement by lymphoma: pattern of involvement and concordance with flow cytometry, in 10 years from a single institution. Clin Transl Oncol. 2016;18:537–40.CrossRef Cabezas-Quintario MA, Gomez P, Yuste-Del Pozo V, Valencia-Mesa AL, Sosa G, Ricard P, et al. Bone marrow trephine biopsy involvement by lymphoma: pattern of involvement and concordance with flow cytometry, in 10 years from a single institution. Clin Transl Oncol. 2016;18:537–40.CrossRef
11.
Zurück zum Zitat Martín-Moro F, Piris-Villaespesa M, Marquet-Palomanes J, Garcia-Cosio M, Villarrubia J, Lario A, et al. Bone marrow infiltration by flow cytometry at diffuse large B-cell lymphoma NOS diagnosis implies worse prognosis without considering bone marrow histology. Cytometry B Clin Cytom. 2019. https://doi.org/10.1002/cyto.b.21863.CrossRefPubMed Martín-Moro F, Piris-Villaespesa M, Marquet-Palomanes J, Garcia-Cosio M, Villarrubia J, Lario A, et al. Bone marrow infiltration by flow cytometry at diffuse large B-cell lymphoma NOS diagnosis implies worse prognosis without considering bone marrow histology. Cytometry B Clin Cytom. 2019. https://​doi.​org/​10.​1002/​cyto.​b.​21863.CrossRefPubMed
12.
Zurück zum Zitat Wolach O, Fraser A, Luchiansky M, Shaporo C, Radnay J, Shpilberg O, et al. Can flow cytometry of bone marrow aspirate predict outcome of patients with diffuse large B cell lymphoma? A retrospective single centre study. Hematol Oncol. 2015;33:42–7.CrossRef Wolach O, Fraser A, Luchiansky M, Shaporo C, Radnay J, Shpilberg O, et al. Can flow cytometry of bone marrow aspirate predict outcome of patients with diffuse large B cell lymphoma? A retrospective single centre study. Hematol Oncol. 2015;33:42–7.CrossRef
13.
Zurück zum Zitat Kim S, Kim H, Kang H, Kim J, Eom H, Kim T, et al. Clinical significance of cytogenetic aberrations in bone marrow of patients with diffuse large B-cell lymphoma: prognostic significance and relevance to histologic involvement. J Hematol Oncol. 2013;6:76.CrossRef Kim S, Kim H, Kang H, Kim J, Eom H, Kim T, et al. Clinical significance of cytogenetic aberrations in bone marrow of patients with diffuse large B-cell lymphoma: prognostic significance and relevance to histologic involvement. J Hematol Oncol. 2013;6:76.CrossRef
14.
Zurück zum Zitat Hong J, Lee Y, Park Y, Kim SG, Hwang KH, Park SH, et al. Role of FDG-PET/CT in detecting lymphomatous bone marrow involvement in patients with newly diagnosed diffuse large B-cell lymphoma. Ann Hematol. 2012;91:687–95.CrossRef Hong J, Lee Y, Park Y, Kim SG, Hwang KH, Park SH, et al. Role of FDG-PET/CT in detecting lymphomatous bone marrow involvement in patients with newly diagnosed diffuse large B-cell lymphoma. Ann Hematol. 2012;91:687–95.CrossRef
15.
Zurück zum Zitat Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Nievelstein RA, de Klerk JM. Bone marrow 18F-fluoro-2-deoxy-d-glucose positron emission tomography/computed tomography cannot replace bone marrow biopsy in diffuse large B-cell lymphoma. Am J Hematol. 2014;89:726–31.CrossRef Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Nievelstein RA, de Klerk JM. Bone marrow 18F-fluoro-2-deoxy-d-glucose positron emission tomography/computed tomography cannot replace bone marrow biopsy in diffuse large B-cell lymphoma. Am J Hematol. 2014;89:726–31.CrossRef
16.
Zurück zum Zitat Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Nievelstein RA, de Klerk JM. Direct comparison of visual and quantitative bone marrow FDG-PET/CT findings with bone marrow biopsy results in diffuse large B-cell lymphoma: does bone marrow FDG-PET/CT live up to its promise? Acta Radiol. 2015;56:1230–5.CrossRef Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Nievelstein RA, de Klerk JM. Direct comparison of visual and quantitative bone marrow FDG-PET/CT findings with bone marrow biopsy results in diffuse large B-cell lymphoma: does bone marrow FDG-PET/CT live up to its promise? Acta Radiol. 2015;56:1230–5.CrossRef
17.
Zurück zum Zitat Chen-Liang TH, Martín-Santos T, Jerez A, Rodriguez-Garcia G, Senent L, Martinez-Millan C, et al. Bone marrow biopsy superiority over PET/CT in predicting progression-free survival in a homogeneously-treated cohort of diffuse large B-cell lymphoma. Cancer Med. 2017;6:2507–14.CrossRef Chen-Liang TH, Martín-Santos T, Jerez A, Rodriguez-Garcia G, Senent L, Martinez-Millan C, et al. Bone marrow biopsy superiority over PET/CT in predicting progression-free survival in a homogeneously-treated cohort of diffuse large B-cell lymphoma. Cancer Med. 2017;6:2507–14.CrossRef
18.
Zurück zum Zitat Khan AB, Barrington SF, Mikhaeel NG, Hunt AA, Cameron L, Morris T, et al. PET-CT staging of DLBCL accurately identifies and provides new insight into the clinical significance of bone marrow involvement. Blood. 2013;122:61–7.CrossRef Khan AB, Barrington SF, Mikhaeel NG, Hunt AA, Cameron L, Morris T, et al. PET-CT staging of DLBCL accurately identifies and provides new insight into the clinical significance of bone marrow involvement. Blood. 2013;122:61–7.CrossRef
19.
Zurück zum Zitat Berthet L, Cochet A, Kanoun S, Berriolo-Riedinger A, Humbert O, Toubeau M, et al. In newly diagnosed diffuse large B-cell lymphoma, determination of bone marrow involvement with 18F-FDG PET/CT provides better diagnostic performance and prognostic stratification than does biopsy. J Nucl Med. 2013;54:1244–50.CrossRef Berthet L, Cochet A, Kanoun S, Berriolo-Riedinger A, Humbert O, Toubeau M, et al. In newly diagnosed diffuse large B-cell lymphoma, determination of bone marrow involvement with 18F-FDG PET/CT provides better diagnostic performance and prognostic stratification than does biopsy. J Nucl Med. 2013;54:1244–50.CrossRef
20.
Zurück zum Zitat Cortés-Romera M, Sabaté-Llobera A, Mercadal-Vilchez S, Climent-Esteller F, Serrano-Maestro A, Gamez-Cenzano C, et al. Bone marrow evaluation in initial staging of lymphoma: 18F-FDG PET/CT versus bone marrow biopsy. Clin Nucl Med. 2014;39:e46-52.CrossRef Cortés-Romera M, Sabaté-Llobera A, Mercadal-Vilchez S, Climent-Esteller F, Serrano-Maestro A, Gamez-Cenzano C, et al. Bone marrow evaluation in initial staging of lymphoma: 18F-FDG PET/CT versus bone marrow biopsy. Clin Nucl Med. 2014;39:e46-52.CrossRef
21.
Zurück zum Zitat Ujjani CS, Hill EM, Wang H, Nassif S, Esposito G, Ozdemirli, et al. 18F-FDG PET-CT and trephine biopsy assessment of bone marrow involvement in lymphoma. Br J Haematol. 2016;174:410–6.CrossRef Ujjani CS, Hill EM, Wang H, Nassif S, Esposito G, Ozdemirli, et al. 18F-FDG PET-CT and trephine biopsy assessment of bone marrow involvement in lymphoma. Br J Haematol. 2016;174:410–6.CrossRef
22.
Zurück zum Zitat El Karak F, Bou-Orm IR, Ghosn M, Kattan J, Farhat F, Ibrahim T, et al. PET/CT Scanner and bone marrow biopsy in detection of bone marrow involvement in diffuse large B-cell lymphoma. PLoS ONE. 2017;12:e0170299.CrossRef El Karak F, Bou-Orm IR, Ghosn M, Kattan J, Farhat F, Ibrahim T, et al. PET/CT Scanner and bone marrow biopsy in detection of bone marrow involvement in diffuse large B-cell lymphoma. PLoS ONE. 2017;12:e0170299.CrossRef
23.
Zurück zum Zitat Alzahrani M, El-Galaly TC, Hutchings M, Hansen JW, Loft A, Johnsen HE, et al. The value of routine bone marrow biopsy in patients with diffuse large B-cell lymphoma staged with PET/CT: a Danish-Canadian study. Ann Oncol. 2016;27:1095–9.CrossRef Alzahrani M, El-Galaly TC, Hutchings M, Hansen JW, Loft A, Johnsen HE, et al. The value of routine bone marrow biopsy in patients with diffuse large B-cell lymphoma staged with PET/CT: a Danish-Canadian study. Ann Oncol. 2016;27:1095–9.CrossRef
24.
Zurück zum Zitat Vishnu P, Wingerson A, Lee M, Mandelson MT, Aboulafia DM. Utility of bone marrow biopsy and aspirate for staging of diffuse large B-cell lymphoma in the era of positron emission tomography with 2-deoxy-2-[fluorine-18]fluoro-deoxyglucose integrated with computed tomography. Clin Lymphoma Myeloma Leuk. 2017;17:631–6.CrossRef Vishnu P, Wingerson A, Lee M, Mandelson MT, Aboulafia DM. Utility of bone marrow biopsy and aspirate for staging of diffuse large B-cell lymphoma in the era of positron emission tomography with 2-deoxy-2-[fluorine-18]fluoro-deoxyglucose integrated with computed tomography. Clin Lymphoma Myeloma Leuk. 2017;17:631–6.CrossRef
25.
Zurück zum Zitat Cerci JJ, Györke T, Fanti S, Paez D, Meneghetti JC, Redondo F, et al. Combined PET and biopsy evidence of marrow involvement improves prognostic prediction in diffuse large B-cell lymphoma. J Nucl Med. 2014;55:1591–7.CrossRef Cerci JJ, Györke T, Fanti S, Paez D, Meneghetti JC, Redondo F, et al. Combined PET and biopsy evidence of marrow involvement improves prognostic prediction in diffuse large B-cell lymphoma. J Nucl Med. 2014;55:1591–7.CrossRef
26.
Zurück zum Zitat Adams HJ, Kwee TC, de Keizer B, Fijnheer R, de Klerk JM, Nievelstein RA. FDG PET/CT for the detection of bone marrow involvement in diffuse large B-cell lymphoma: systematic review and meta-analysis. Eur J Nucl Med Mol Imaging. 2014;41:565–74.CrossRef Adams HJ, Kwee TC, de Keizer B, Fijnheer R, de Klerk JM, Nievelstein RA. FDG PET/CT for the detection of bone marrow involvement in diffuse large B-cell lymphoma: systematic review and meta-analysis. Eur J Nucl Med Mol Imaging. 2014;41:565–74.CrossRef
27.
Zurück zum Zitat Jackson AE, Smeltzer JP, Habermann TM, Jones JM, Burnette B, Ristow K, et al. The utility of restaging bone marrow biopsy in PET-negative patients with diffuse large B-cell lymphoma and baseline bone marrow involvement. Am J Hematol. 2014;89:865–7.CrossRef Jackson AE, Smeltzer JP, Habermann TM, Jones JM, Burnette B, Ristow K, et al. The utility of restaging bone marrow biopsy in PET-negative patients with diffuse large B-cell lymphoma and baseline bone marrow involvement. Am J Hematol. 2014;89:865–7.CrossRef
28.
Zurück zum Zitat Rutherford SC, Herold M, Hiddemann W, Kostakoglu L, Marcus R, Martelli M, et al. Impact of bone marrow biopsy on response assessment in immunochemotherapy-treated lymphoma patients in GALLIUM and GOYA. Blood Adv. 2020;4:1589–93.CrossRef Rutherford SC, Herold M, Hiddemann W, Kostakoglu L, Marcus R, Martelli M, et al. Impact of bone marrow biopsy on response assessment in immunochemotherapy-treated lymphoma patients in GALLIUM and GOYA. Blood Adv. 2020;4:1589–93.CrossRef
29.
Zurück zum Zitat Brudno J, Tadmor T, Pittaluga S, Nicolae A, Polliack A, Dunleavy K. Discordant bone marrow involvement in non-Hodgkin lymphoma. Blood. 2016;127:965–70.CrossRef Brudno J, Tadmor T, Pittaluga S, Nicolae A, Polliack A, Dunleavy K. Discordant bone marrow involvement in non-Hodgkin lymphoma. Blood. 2016;127:965–70.CrossRef
30.
Zurück zum Zitat Park MJ, Park SH, Park PW, Seo YH, Kim KH, Seo JY, et al. Prognostic impact of concordant and discordant bone marrow involvement and cell-of-origin in Korean patients with diffuse large B-cell lymphoma treated with R-CHOP. J Clin Pathol. 2015;68:733–8.CrossRef Park MJ, Park SH, Park PW, Seo YH, Kim KH, Seo JY, et al. Prognostic impact of concordant and discordant bone marrow involvement and cell-of-origin in Korean patients with diffuse large B-cell lymphoma treated with R-CHOP. J Clin Pathol. 2015;68:733–8.CrossRef
31.
Zurück zum Zitat Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Nievelstein RA, de Klerk JM. Diffusely increased bone marrow FDG uptake in recently untreated lymphoma: incidence and relevance. Eur J Haematol. 2015;95:83–9.CrossRef Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Nievelstein RA, de Klerk JM. Diffusely increased bone marrow FDG uptake in recently untreated lymphoma: incidence and relevance. Eur J Haematol. 2015;95:83–9.CrossRef
32.
Zurück zum Zitat Abramson JS. Bone marrow biopsies for staging of diffuse large B-cell lymphoma: are we looking too closely? Leuk Lymphoma. 2017;58:4–5.CrossRef Abramson JS. Bone marrow biopsies for staging of diffuse large B-cell lymphoma: are we looking too closely? Leuk Lymphoma. 2017;58:4–5.CrossRef
Metadaten
Titel
Biopsy remains indispensable for evaluating bone marrow involvement in DLBCL patients despite the use of positron emission tomography
verfasst von
Yusuke Saiki
Naoto Tomita
Akiko Uchida
Yu Uemura
Yoshinori Suzuki
Tsuneaki Hirakawa
Masayuki Kato
Masahiro Hoshikawa
Tsuyoshi Kawano
Naoya Nakamura
Ikuo Miura
Ayako Arai
Publikationsdatum
30.01.2021
Verlag
Springer Singapore
Erschienen in
International Journal of Hematology / Ausgabe 5/2021
Print ISSN: 0925-5710
Elektronische ISSN: 1865-3774
DOI
https://doi.org/10.1007/s12185-021-03080-3

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