Abstract
Detection of bone marrow involvement (BMI) for patients with follicular lymphoma (FL) is of great significance for staging and treatment. The clinical value of positron emission tomography/computed tomography (PET/CT) in assessing BMI is still under debate and investigation. PubMed, Embase, Web of Science, and Cochrane Library databases were systematically searched to identify studies evaluating PET/CT in detecting BMI in FL patients. Data extraction and quality evaluation were independently conducted by two reviewers, and nine eligible studies were selected as final quantitative analysis. Nine studies comprising 1119 FL patients were included. The pooled sensitivity was 0.67 (95% CI, 0.38–0.87), and the pooled specificity was 0.82 (95% CI, 0.75–0.87). The pooled positive likelihood ratio, negative likelihood ratio, and diagnostic odds ratio were 3.7 (95% CI, 2.1–6.3), 0.4 (95% CI, 0.18–0.91), and 9 (95% CI, 2–33), respectively. The area under the curve of PET/CT to detect BMI in FL patients was 0.83 (95% CI, 0.8–0.86). Current evidence suggests that PET/CT cannot replace bone marrow biopsy to detect BMI, but it is still of partial clinical significance for the prognosis of patients with follicular lymphoma.
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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Freedman A, Jacobsen E (2020) Follicular lymphoma: 2020 update on diagnosis and management. Am J Hematol 95(3):316–327
Kwee TC, de Klerk JM, Nievelstein RA (2011) Imaging of bone marrow involvement in lymphoma: state of the art and future directions. Sci World J 11:391–402
Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A et al (2009) 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(27):4555–4562
Barrington SF, Johnson PWM (2017) 18F-FDG PET/CT in lymphoma: has imaging-directed personalized medicine become a reality? J Nucl Med 58(10):1539–1544
Le Dortz L, De Guibert S, Bayat S, Devillers A, Houot R et al (2010) Diagnostic and prognostic impact of 18F-FDG PET/CT in follicular lymphoma. Eur J Nucl Med Mol Imaging 37(12):2307–2314
Moher D, Liberati A, Tetzlaff J, PRISMA Group (2009) Altman DG Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Plos Med 6(7):e1000097
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, QUADAS-2 Group et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 155(8):529–536
Devillé WL, Buntinx F, Bouter LM, Montori VM, de Vet HC et al (2002) Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol 2:9
Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM (2003) The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 56(11):1129–1135
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560
Perry C, Lerman H, Joffe E, Sarid N, Amit O et al (2016) The value of PET/CT in detecting bone marrow involvement in patients with follicular lymphoma. Medicine (Baltimore) 95(9):e2910
El-Najjar I, Montoto S, McDowell A, Matthews J, Gribben J, Szyszko TA (2014) The value of semiquantitative analysis in identifying diffuse bone marrow involvement in follicular lymphoma. Nucl Med Commun 35(3):311–315
Adams HJ, Kwee TC, Fijnheer R, Dubois SV, Blase PE et al (2014) Utility of quantitative FDG-PET/CT for the detection of bone marrow involvement in follicular lymphoma: a histopathological correlation study. Skeletal Radiol 43(9):1231–1236
Göçer M, Kurtoğlu E (2021) Comparison of bone marrow involvement with bone marrow biopsy and PET-CT and evaluation of any effects on survival in patients diagnosed with Hodgkin and non-Hodgkin lymphoma. Indian J Hematol Blood Transfus 37(1):52–59
Nakajima R, Moskowitz AJ, Michaud L, Mauguen A, Batlevi CL et al (2020) Baseline FDG-PET/CT detects bone marrow involvement in follicular lymphoma and provides relevant prognostic information. Blood Adv 4(8):1812–1823
St-Pierre F, Broski SM, LaPlant BR, Maurer MJ, Ristow K et al (2020) Fluorodeoxyglucose-positron emission tomography predicts bone marrow involvement in the staging of follicular lymphoma. Oncologist 25(8):689–695
Teagle AR, Barton H, Charles-Edwards E, Dizdarevic S, Chevassut T (2017) Use of FDG PET/CT in identification of bone marrow involvement in diffuse large B cell lymphoma and follicular lymphoma: comparison with iliac crest bone marrow biopsy. Acta Radiol 58(12):1476–1484
Ujjani CS, Hill EM, Wang H, Nassif S, Esposito G et al (2016) (18) F-FDG PET-CT and trephine biopsy assessment of bone marrow involvement in lymphoma. Br J Haematol 174(3):410–416
Wöhrer S, Jaeger U, Kletter K, Becherer A, Hauswirth A et al (2006) 18F-fluoro-deoxy-glucose positron emission tomography (18F-FDG-PET) visualizes follicular lymphoma irrespective of grading. Ann Oncol 17(5):780–784
Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH et al (2014) Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 32(27):3059–3068
Gheysens O, Thielemans S, Morscio J, Boeckx N, Goffin KE et al (2016) Detection of bone marrow involvement in newly diagnosed post-transplant lymphoproliferative disorder: (18)F-fluorodeoxyglucose positron emission tomography/computed tomography versus bone marrow biopsy. Leuk Lymphoma 57(10):2382–2388
Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K et al (2002) Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer 94(5):1522–1531
Kaddu-Mulindwa D, Altmann B, Held G, Angel S, Stilgenbauer S et al (2021) FDG PET/CT to detect bone marrow involvement in the initial staging of patients with aggressive non-Hodgkin lymphoma: results from the prospective, multicenter PETAL and OPTIMAL>60 trials. Eur J Nucl Med Mol Imaging 48(11):3550–3559
Pakos EE, Fotopoulos AD, Ioannidis JP (2005) 18F-FDG PET for evaluation of bone marrow infiltration in staging of lymphoma: a meta-analysis. J Nucl Med 46(6):958–963
Caraguel CG, Vanderstichel R (2013) The two-step Fagan’s nomogram: ad hoc interpretation of a diagnostic test result without calculation. Evid Based Med 18(4):125–128
Muslimani AA, Farag HL, Francis S, Spiro TP, Chaudhry AA et al (2008) The utility of 18-F-fluorodeoxyglucose positron emission tomography in evaluation of bone marrow involvement by non-Hodgkin lymphoma. Am J Clin Oncol 31(5):409–412
Elstrom R, Guan L, Baker G, Nakhoda K, Vergilio JA, Zhuang H, Pitsilos S, Bagg A, Downs L, Mehrotra A, Kim S, Alavi A, Schuster SJ (2003) Utility of FDG-PET scanning in lymphoma by WHO classification. Blood 101(10):3875–3876
Funding
C. T. is supported by the Natural Science Foundation of Xinjiang Autonomous Region (2022D01A09), Grant ZC20171, from Tianjin Health Science and Technology Project and Tianjin Key Medical Discipline (Specialty) Construction Project (TJYXZDXK-009A).
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Y. Z., X. L., and H. L. acquired and analyzed the data, and wrote the paper. J. L., J. S., Q. X., D. C., and R. N. revised the manuscript. C. T. and Y. W. proposed the research idea and critically revised the manuscript. All authors approved all versions including the final version, and were responsible for the accuracy and integrity of all aspects of the manuscript.
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PET/CT cannot replace bone marrow biopsy to diagnose bone marrow infiltration, but it is still of partial clinical significance for the prognosis of patients with follicular lymphoma.
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Zheng, Y., Liu, J., Si, J. et al. Positron emission tomography to detect bone marrow involvement for patients with follicular lymphoma: a systematic review and meta-analysis. Ann Hematol 102, 2403–2412 (2023). https://doi.org/10.1007/s00277-023-05274-7
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DOI: https://doi.org/10.1007/s00277-023-05274-7