The Incidence of Epstein-Barr Virus-Positive Diffuse Large B-Cell Lymphoma: A Systematic Review and Meta-Analysis
Abstract
:Simple Summary
Abstract
1. Introduction
2. Methods
2.1. Search Strategy and Selection Criteria
2.2. Data Extraction and Quality Assessment
2.3. Data Synthesis and Analysis
3. Results
3.1. Study Search and Quality Assessment
3.2. Study Characteristics
3.3. The Pooled Proportion of EBER Positivity and Subgroup Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Authors, Publication Years | Patient Enrollment Period | Institution | Country | Design | EBER Cut-Off Values |
---|---|---|---|---|---|
Ahn JS et al., 2013 [20] | 2003–2011 | Chonnam National University Hwasun Hospital, Chonbuk National University Medical School | Korea | Retrospective | 10 |
Aladily TN et al., 2019 [21] | NA | Jordan University Hospital, Necmettin Erbakan University | Jordan, Turkey | Retrospective | 10 |
Beltran BE et al., 2018 [12] | 2006–2015 | Hospital Nacional Edgardo Rebagliati Martins | Peru | Retrospective | 20 |
Carreras J et al., 2017 [22] | 2002–2013 | Tokai University, School of Medicine | Japan | NA | NA |
Chang ST et al., 2014 [23] | 1989–2010 | Chi-Mei Medical Centre | Taiwan | Retrospective | 10 |
Cohen M et al., 2017 [24] | 1987–2013, 2009–2013 | Ricardo Gutiérrez Children’s Hospital, National Academy of Medicine | Argentina | Retrospective | 20 |
Gibson SE et al., 2009 [25] | 2002–2008 | Cleveland Clinic | USA | Retrospective | NA |
Hong JY et al., 2015 [5] | 1995–2011 | Samsung Medical Center | Korea | Secondary analysis | 20 |
Hsueh CY et al., 2019 [26] | 1995–2017 | Taipei Veterans General Hospital | Taiwan | Retrospective | NA |
Hu LY et al., 2017 [27] | 2005–2012 | Sun Yat-sen University Cancer Center | China | Retrospective | 10 |
Keane C et al., 2019 [28] | 2003–2014 | Multicenter | Australia | NA | 10 |
Lu TX et al., 2015 [13] | 2006–2014 | Jiangsu Province Hospital | China | NA | 20, 50 |
Miyagi S et al., 2020 [8] | 1995–2018 | Nagoya University Hospital | Japan | Retrospective | 80 |
Monabati A et al., 2016 [6] | 2012–2014 | Shahid Fagihi hospital | Iran | Retrospective | 20 |
Naeini YB et al., 2016 [29] | 2008–2015 | Clarient Pathology Services | USA | NA | 10 |
Ohashi A et al., 2017 [30] | NA–2012 | Fujita Health University School | Japan | NA | 80 |
Ok CY et al., 2014 [9] | NA | Multicenter (the International DLBCL Rituximab-CHOP Consortium Program Study) | Western countries | NA | 10, 30, 50 |
Okamoto A et al., 2017 [31] | 2007–2012 | Fujita Health University Hospital | Japan | Retrospective | 20 |
Ozsan N et al., 2013 [32] | 2009–2012 | Ege University Faculty of Medicine | Turkey | Retrospective | 20 |
Pan Y et al., 2013 [33] | 1999–2010 | Tianjin Medical University Cancer Institute and Hospital | China | NA | 50 |
Salas MQ et al., 2020 [34] | 2012–2016 | Catalan Institue of Oncology | Spain | Retrospective | NA |
Sato A et al., 2014 [35] | 2007–2011 | Tokai University Hospital | Japan | NA | 30 |
Slack GW et al., 2014 [36] | 1999–2016 | British Columbia Cancer Agency | Canada | NA | NA |
Song CG et al., 2015 [37] | 2001–2011 | Sun Yat-Sen University Cancer Center | China | Retrospective | NA |
Stuhlmann-Laeisz C et al., 2016 [38] | NA | Multicenter | Switzerland, Germany | NA | 50 |
Tokuyama K et al., 2017 [39] | 2007–2016 | Oita University Faculty of Medicine | Japan | Retrospective | 50 |
Uccini S et al., 2015 [40] | 2008–2013 | Children’s Welfare Teaching Hospital | Iraq | NA | NA |
Uner A et al., 2011 [41] | 1999–2009 | Hacettepe University and Gazi University Medical Schools | Turkey | Retrospective | NA |
Wada N et al., 2011 [42] | 1999–2009 | Multicenter (Osaka Lymphoma Study Group) | Japan | NA | 20, 50 |
Xie Y et al., 2014 [43] | 2002–2012 | University of Southern California Medical Center | USA | Retrospective | 20 |
Ziarkiewicz M et al., 2016 [10] | 1994–2011 | Medical University of Warsaw | Poland | Retrospective | 5 |
Authors | Patients (N) | Age (Range) | Male to Female Ratio | Clinical Setting | IPI Category | Ann Arbor Stage | Elevated LDH | Treatment Arm |
---|---|---|---|---|---|---|---|---|
Ahn JS et al., 2013 [20] | 222 | 66 (51–82) in EBV+, 67 (50–86) in EBV− | 131:91 | DLBCL | 0–1 (33%), 2 (20%), 3 (19%), 4–5 (24%) | 3–4 (52%) | 56.0% | R-CHOP |
Aladily TN et al., 2019 [21] | 100 | NA | NA | DLBCL | NA | NA | NA | NA |
Beltran BE et al., 2018 [12] | 117 | NA | NA | DLBCL | 0–2 (40.2%), 3–5 (59.8%) | 3–4 (43.6%) | 51.3% | R-CHOP, CHOP |
Carreras J et al., 2017 [22] | 29 | NA | 20:9 | Primary sinonasal DLBCL | 0–2 (72.4%), 3–5 (20.7%) | 1–2 (72.4%), 3–4 (27.6%) | 34.5% | R-CHOP, R-CHOP-like |
Chang ST et al., 2014 [23] | 424 | 74 (41–91) in EBV+, 65 (14–94) in EBV− | 194:138 | DLBCL | NA | NA | NA | CEOP, CHOP, R-CEOP in EBV+ |
Cohen M et al., 2017 [24] | 102 | 52 (2–84) | 50:52 | DLBCL | NA | 3–4 (57%) | NA | GATLA treatment protocols (pediatric), R-CHOP (adult) |
Gibson SE et al., 2009 [25] | 90 | NA | NA | DLBCL | NA | NA | NA | NA |
Hong JY et al., 2015 [5] | 571 | 55 (16–88) | 335:236 | DLBCL | 0–2 (69.5), 4–5 (30.5%) | 1–2 (57.7%), 3–4 (42.3%) | 65.4% | R-CHOP, CHOP, others |
Hsueh CY et al., 2019 [26] | 17 | 61.59 (17–88) | 9:8 | Nasopharyngeal DLBCL | NA | 1 (23.5%), 2 (47.1%), 4 (29.4%) | NA | NA |
Hu LY et al., 2017 [27] | 204 | 52 (18–86) | 115:89 | DLBCL | 0–2 (77.9%), 3–5 (22.0%) | 3–4 (51.0%) | 48.4% | R-CHOP or R-CHO-like regimen, CHOP or CHOP-like regimen, MA regimen |
Keane C et al., 2019 [28] | 433 | NA | 192:241 | DLBCL | 0 (10.5%), 1–2 (45.0%), 3–5 (44.5%) | 3–4 (52.9%) | 44.1% | R-CHOP, alternative regimens |
Lu TX et al., 2015 [13] | 250 | NA | 144:106 | DLBCL | 0–2 (73.4%), 3–5 (26.6%) | 1–2 (50%), 3–4 (50.0%) | 45.6% | R-CHOP, R-DA-EPOCH, CHOP |
Miyagi S et al., 2020 [8] | 312 | 69.5 (35–84) | 16:20 | Primary gastrointestinal tract DLBCL | 3–5 (28.6%) in EBV+ | a I (25%), II1-IV (75%) in EBV+ | 42.8% in EBV+ | R-containing CTx in 25/28 (89.3%) |
Monabati A et al., 2016 [6] | 95 | 53.9 (12–90) | 52:43 | DLBCL | NA | NA | NA | NA |
Naeini YB et al., 2016 [29] | 677 | 67 (11–96) | 378:285 | DLBCL | NA | NA | NA | NA |
Ohashi A et al., 2017 [30] | 667 | NA | 385:278 | DLBCL | 4–5 (46.8) | 3–4 (54.4%) | 58.9% | NA |
Ok CY et al., 2014 [9] | 732 | 63 (16–95) | 421:311 | DLBCL | 0–2 (59.3%), 3–5 (40.7%) | 1–2 (46.4%), 3–4 (53.6%) | 62.3% | R-CHOP |
Okamoto A et al., 2017 [31] | 134 | 77 (62–91) in EBV+, 38 (33–93) in EBV− | 79:55 | DLBCL | 0–2 (47.8%), 3–5 (52.2%) | 1–2 (42.5%), 3–4 (57.5%) | 61.2% | Rituximab+anthracycline-based CTx in 93% |
Ozsan N et al., 2013 [32] | 149 | >50 | NA | DLBCL | NA | NA | NA | R-CHOP in EBV+ |
Pan Y et al., 2013 [33] | 212 | 58.5 (22–91) | 115:97 | DLBCL | NA | NA | NA | R-CHOP, CHOP in EBV+ |
Salas MQ et al., 2020 [34] | 216 | 63 (19–90) | 105:111 | DLBCL | 1–2 (49.5%), 3–5 (50.5%) | 1–2 (31.0%), 3–4 (68.9%) | 56.5% | Various |
Sato A et al., 2014 [35] | 239 | 71.5 in EBV+, 68.0 in EBV− | 130:109 | DLBCL | 3–5 (48.6%) | 3–4 (53.5%) | 61.1% | R-CHOP, R-CHOP-like |
Slack GW et al., 2014 [36] | 385 | 64 (16–92) | 195:113 | DLBCL | 0–2 (35%), 3–5 (65%) | 1–2 (46%), 3–4 (58%) | 50.0% | R-CHOP |
Song CG et al., 2015 [37] | 230 | 62 (51–76) | 147:83 | DLBCL | 0–2 (75.2%), 3–5 (24.8%) | 1–2 (35.7%) | 48.7% | CHOP or EPOCH +/− Rituximab |
Stuhlmann-Laeisz C et al., 2016 [38] | 598 | 70 (50–98) | NA | DLBCL | NA | NA | NA | CHOP, R-CHOP, R-Bendamustin in EBV+ |
Tokuyama K et al., 2017 [39] | 48 | 76.2 (72–83) in EBV+, 71.3 (53–91) in EBV− | 15:23 | DLBCL | NA | 1–2 (35.4%), 3–4 (64.6%) | NA | NA |
Uccini S et al., 2015 [40] | 13 | 8.8 in EBV+, 7.5 in EBV− | 10:3 | pediatric DLBCL | NA | b 1 (7.7%), 2 (15.4%), 3 (53.8%), 4 (23.0%) | NA | Various |
Uner A et al., 2011 [41] | 340 | 54.5 (6–101) | 170:170 | DLBCL | NA | NA | NA | NA |
Wada N et al., 2011 [42] | 484 | 68 (16–95) | 1.29:1 | DLBCL | NA | NA | NA | NA |
Xie Y et al., 2014 [43] | 85 | 54 (20–89) | 51:34 | DLBCL | 0–2 (65%), 3–5 (36%) | 1 (21%), 2 (26%), 3 (12%), 4 (41%) | 53.0% | R-CHOP, R-CHOP-like |
Ziarkiewicz M et al., 2016 [10] | 74 | 63.5 (23–86) | 37:37 | DLBCL | 0–2 (58.6%) | 0–2 (40.8%) | 71.9% | CHOP, CHOP-variant, +/−Rituximab |
Outcome | No. of Studies | Summary Estimate | p-Value by Test for Subgroup Differences | ||
---|---|---|---|---|---|
Pooled Proportion (%) (95% CI) | p Value for Heterogeneity | I2 (%) | |||
EBER positive | 31 | 7.9 (6.2–10.0) | <0.001 | 85 | – |
Asia and South America | 22 | 9.2 (7.0–12.0) | <0.001 | 83 | 0.005 |
Western | 7 | 4.7 (3.2–6.8) | <0.001 | 74 | |
EBER positive (cut-off: 10%) | 7 | 6.8 (5.0–9.3) | 0.004 | 68 | 0.17 |
EBER positive (cut-off: 20%) | 9 | 9.6 (6.1–14.8) | <0.001 | 89 | |
EBER positive (cut-off: 50%) | 6 | 4.2 (1.9–9.2) | <0.001 | 92 | |
Elderly EBER positive | 13 | 7.6 (5.4–10.4) | <0.001 | 78 | 0.10 |
Young EBER positive | 5 | 14.4 (7.1–27.1) | <0.001 | 79 |
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Hwang, J.; Suh, C.H.; Won Kim, K.; Kim, H.S.; Armand, P.; Huang, R.Y.; Guenette, J.P. The Incidence of Epstein-Barr Virus-Positive Diffuse Large B-Cell Lymphoma: A Systematic Review and Meta-Analysis. Cancers 2021, 13, 1785. https://doi.org/10.3390/cancers13081785
Hwang J, Suh CH, Won Kim K, Kim HS, Armand P, Huang RY, Guenette JP. The Incidence of Epstein-Barr Virus-Positive Diffuse Large B-Cell Lymphoma: A Systematic Review and Meta-Analysis. Cancers. 2021; 13(8):1785. https://doi.org/10.3390/cancers13081785
Chicago/Turabian StyleHwang, Jisun, Chong Hyun Suh, Kyung Won Kim, Ho Sung Kim, Philippe Armand, Raymond Y. Huang, and Jeffrey P. Guenette. 2021. "The Incidence of Epstein-Barr Virus-Positive Diffuse Large B-Cell Lymphoma: A Systematic Review and Meta-Analysis" Cancers 13, no. 8: 1785. https://doi.org/10.3390/cancers13081785