Association of B Cells with Idiopathic Recurrent Pregnancy Loss: A Systematic Review and Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Eligibility Criteria and Study Selection
2.3. Data Extraction and Quality Assessment
2.4. Data Synthesis
3. Results
3.1. Study Selection
3.2. Characteristics of Included Studies
Reference | Country | n (Mean ± SD Age in Years) | iRPL Criteria | N of Miscarriages * | n (Mean ± SD Age in Years) | Obstetric History * | n of Studied Groups | Sample & Method | Sample Collection Phase | Markers | Results * |
---|---|---|---|---|---|---|---|---|---|---|---|
Alosh et al., 1998 [42] | Egypt | n = 20 (31.6 ± 4.2 yrs; 24–36 range) | 3+ | 4.3 miscarriages (3–6 range) | n = 12 (33.2 ± 5.5; 28–38 range) | ≥2 successful pregnancies. | 2 | EB|FC | Lutheal | CD20 | ↑ proportion of endometrial B cells in IRPL (17 ± 7%) compared to HC (5.5 ± 6%)—p < 0.05 |
Bohlmann et al., 2010 [31] | Germany | n = 25 (32.8 ± 5.6 yrs; 21–41 range) | 2+ | 3.3 ± 1.17 miscarriages (2–6 range) | n = 10 (33.5 ± 4.3; 23–37 range) | No history of miscarriage. | 2 | EB|IHC | Lutheal | CD19 | Similar CD19 staining score in IRPL (0.66 ± 0.64) and HC (0.38 ± 0.72). |
Carbone et al., 2009 [43] | Spain | n = 36 (37 yrs, 30–43 range) | 2+ | 2.89 miscarriages (2–7 range) 0.44 live-born babies (0–3 range) | n = 37 (37.0; 22–48 range) | ≥1 live-born babies (1–3 range). No history of miscarriage. | 5 | PB|FC | Not specified | CD19, IgD, CD27 CD40, CD5 | Similar % of B cells in IRPL (8 ± 3%, 7–8 95% CI) and HC (8 ± 4%, 7–10 95% CI). Similar B cell counts in IRPL (155 ± 76 cells/µL) and HC (159 ± 95 cells/µL). No significant differences regarding other B cell subsets. |
Carbone et al., 2016 [44] | Spain | n = 24 (37 yrs; 32–43 range) | 3+ | NA | n = 37 (37,0) | History of a live child. No history of miscarriage. | 3 | PB|FC | Follicular | CD19, CD27, IgD | Similar total, naive (85 ± 52 vs. 99 ± 72 cells/µL) and class-switched memory B cell levels in IRPL and HC. ↑ levels of unswitched memory B cells in the IRPL group |
Darmochwal-Kolarz et al., 2002 [19] | Poland | n = 14 (28.92 yrs; 25–34 range) | 3+ | NA | n = 18 (27.42; 26–35 range) | History of successful pregnancies. | 2 | PB|FC | Not specified | CD19+ CD19+ CD5+ | ↓ total B cell% in IRPL [8.5 (3.2–15.9)] # compared to HC [14.45 (10.9–20.7)] #—p < 0.005. ↑ % of CD5+ B cell in IRPL [2.0 (0.7–5.9)] # compared to HC [0.9 (0.5–2.5)] #—p < 0.05 |
Gao et al., 2014 [46] | China | n = 67 (30.28 ± 4.12 yrs) | 2+ | Total of 182 miscarriages | n = 22 (29.67 ± 3.29) | ≥1 live birth. | 3 | PB|FC | Lutheal | CD19 | Similar % of B cells in IRPL (13.19 ± 4.31) and HC (12.56 ± 3.36)—p = 0.232 |
Gao et al., 2021 [45] | China | n = 411 (30.22 ± 4.10 yrs) | 3+ | 3.39 ± 0.66 miscarriages | n = 179 (30.82 ± 3.70) | ≥1 live birth. | 3 | PB|FC | Not specified | CD19 | Similar % of B cells in IRPL [11.0 (8.8–13.9)] $ and HC [11.8 (10.4–13.0)] $. |
Ghafourian et al., 2014 [20] | Iran | n = 25 (20–35 yrs) | 3+ | NA | n = 25 | History of a live child. No history of miscarriage. | 2 | PB|FC | Not specified | CD20 | Similar % of B cells in IRPL (9.45 ± 0.71) and HC (11.34 ± 0.76). |
Kwak et al., 1995 [17] | USA | n = 81 (33.6 ± 4.8 yrs) | 3+ | 4.1 ± 1.4 miscarriages | n = 17 (36.5 ±7.0) | ≥2 successful pregnancies. No history of miscarriage. | 4 | PB|FC | Not specified | CD19+ CD19+ CD5+ | Similar % of B cells and CD5+ B cells in IRPL and HC. |
Kwak et al., 1998 [47] | USA | n = 33 (34.0 yrs; 25–43 range) | 2+ | 3.0 miscarriages (2–8 range) | n = 8 | NA | 2 | PB|FC | Not specified | CD19+ CD19+ CD5+ | The % of B cells was 12.8 ± 0.8 in the IRPL and 10.4 ± 1.4 in HC. The % of CD5+ B cells within total B cells was 43.7 ± 4.4 in the IRPL and 55.2 ± 13.0 in HC. |
Lachapelle et al., 1996 [32] | Canada | 1 ary IRPL: n = 11 (30 ± 4 yrs; 22–37 range) 2 ary IRPL: n = 9 (33 ± 2 yrs; 26–39 range) | 3+ | 1 ary IRPL: 4 ± 1 miscarriages (3–6 range) 2 ary IRPL: 4 ± 1 miscarriages (3–5 range) | n = 15 (35.0 ± 4.0; 27–40 range) | ≥1 live birth. 0.3 ± 0.5 miscarriages (0–1 range). | 3 | EB|FC | Lutheal | CD20 | ↑ % of endometrial B cells in IRPL (16.0 ± 8.0%) compared to HC (5.0 ± 6.0%)—p < 0.05. ↓ % of endometrial B cells in the IRPL group who had maintained an intact conceptus for extended periods compared to patients with continued miscarriages. |
Mahmoud et al., 2001 [48] | USA | n = 10 (31.4 ± 2.2 yrs; 22–42 range) | 3+ | NA | n = 20 (29.5 ± 1.8, 20–43 range) | No history of RPL. | 3 | PB|FC | Not specified | CD19+ CD19+ CD5+ | ↓ % of B cells in RPL subjects (9.9 ± 1.1) compared to HC (13.9 ± 1.0)—p < 0.05. |
Marron et al., 2019 [49] | Ireland | n = 121 (37.9 ± 4.0 yrs) | 2+ | Total of 320 miscarriages. Total of 47 live births. | n = 29 (35.2 ± 3.1) | Total of 4 miscarriages. Total of 10 live births. | 5 | EB|FC | Lutheal | CD19 | ↑ concentration endometrial of B cells in IRPL (79.6 cells/mg) compared to HC (48.8 cells/mg)—p = 0.002; |
Marron et al., 2019 [30] | Ireland | n = 155 (38.0 ± 4.0 yrs) | 2+ | Total of 442 miscarriages. Total of 61 live births. | n = 35 (35.1 ± 2.9) | Total of 6 miscarriages. Total of 10 live births. | 5 | EB|FC | Lutheal | CD19 | ↑ % of endometrial B cells (within total CD45+ endometrial lymphocytes) in IRPL (0.77%) compared to HC (0.43%)—p < 0.001. |
Psarra et al., 2001 [50] | Greece | n = 244 (26–39 yrs) | 2+ | NA | n = 44 (23–42 range) | NA | 2 | PB|FC | Not specified | CD19+ CD19+ CD5+ | Similar % of B cells in IRPL (10.6 ± 3.8) and HC (11.4 ± 6.0). ↓ % of CD19+CD5+B cells within total lymphocytes in IRPL (0.4 ± 0.6) compared to HC (1.4 ± 0.8). |
Quenby et al., 1999 [51] | UK | n = 22 (33.9 yrs; 20–41 range) | 3+ | 4.4 miscarriages (3–17 range) 0.3 live births (0–2 range) | n = 9 (33.1; 24–41 range) | ≥2 live births (2–4 range). 0.4 miscarriages (0–1 range). | 2 | EB|IHC | Lutheal | CD22 | Similar median % of endometrial B cells within total cells in IRPL (0.18, 0–4 range) and HC (0, 0–0.8 range). |
Souza et al., 2002 [52] | Brazil | n = 9 | 2+ | NA | n = 9 (<40) | ≥2 term pregnancies. No history of miscarriage. | 2 | PB|FC | Lutheal | CD19 | ↑ B cell counts in IRPL [215 (188–236) cells/mm3] $ than in HC [182(151–185) cells/mm3] $—p = 0.05 |
Zhao et al., 2020 [53] | China | n = 30 (35.40 ± 0.62 yrs) | 3+ | 3.0 miscarriages (3–5 range) | n = 30 (29.47 ± 0.66) | ≥1 live births. No history of spontaneous miscarriages. | 2 | EB|IHC | Lutheal | CD20 | Similar B cell density in IRPL (0.5%, 0.2–2.5% range) and HC (0.4%, 0.1–2.2% range)—p = 0.0693 |
Zhu et al., 2015 [54] | China | n = 39 (28.3 ± 3.22 yrs) | 2+ | 2.8 ± 0.6 miscarriages | n = 25 (26.8 ± 2.34) | Normal pregnancy history. 0.7 ± 0.34 miscarriages. | 4 | PB|FC | Not specified | CD19 | Similar % of CD19+ B cells in IRPL (11.7 ± 3.31) and HC (11.7 ± 2.45) |
3.3. Methodological Quality
3.4. Results of Individual Studies and Meta-Analyses
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Inclusion Criteria | Exclusion Criteria |
---|---|
Studies on living humans | Animal studies |
Women of reproductive age (18–45 years) | Women with current pregnancy |
Recurrent pregnancy loss of unknown aetiology | Studies not reporting B cell levels |
IRPL group with at least two consecutives miscarriages | Genetic studies |
B cell compartment evaluation | No primary research |
Case-report studies |
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Ângelo-Dias, M.; Martins, C.; Dias, S.S.; Borrego, L.M.; Lima, J. Association of B Cells with Idiopathic Recurrent Pregnancy Loss: A Systematic Review and Meta-Analysis. Int. J. Mol. Sci. 2022, 23, 15200. https://doi.org/10.3390/ijms232315200
Ângelo-Dias M, Martins C, Dias SS, Borrego LM, Lima J. Association of B Cells with Idiopathic Recurrent Pregnancy Loss: A Systematic Review and Meta-Analysis. International Journal of Molecular Sciences. 2022; 23(23):15200. https://doi.org/10.3390/ijms232315200
Chicago/Turabian StyleÂngelo-Dias, Miguel, Catarina Martins, Sara Simões Dias, Luís Miguel Borrego, and Jorge Lima. 2022. "Association of B Cells with Idiopathic Recurrent Pregnancy Loss: A Systematic Review and Meta-Analysis" International Journal of Molecular Sciences 23, no. 23: 15200. https://doi.org/10.3390/ijms232315200