Table 1.
Studies Included in the Systematic Review and Meta-Analysesa
| Study | Study Site | Study Design | n | Follow- Up Period | Maternal Malaria Type | Outcome of Offspring | Measure of Effect | Unadjusted Effect | Adjusted Effect | Factors Adjusted for | NOS, Stars |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Studies Included in Systematic Review and Meta-Analyses | |||||||||||
| Asante et al [14] | Ghana | Cohort | 1855 | 12 mo | PM | First parasitemia | HR (multigravidae) | 1.06 (0.91–1.23) | 1.02 (0.88–1.19) | Wealth index, thatched roof, residence area, and distance from health facility | 8 |
| PM | First clinical malaria | HR (multigravidae) | 1.08 (0.91–1.27) | 1.01 (0.85–1.20) | Wealth index, thatched roof, residence area, and distance from health facility | ||||||
| PM | All episodes of parasitemia | HR (multigravidae) | 1.03 (0.89–1.19) | 0.98 (0.85–1.12) | Wealth index, thatched roof, residence area, and distance from health facility, infant ITN use, malaria exposure score | ||||||
| PM | All episodes of clinical malaria | HR (multigravidae) | 1.00 (0.86–1.17) | 0.94 (0.81–1.10) | Wealth index, thatched roof, residence area, and distance from health facility, infant ITN use, malaria exposure score | ||||||
| Bardají et al [37] | Mozam bique | RCT | 997 | 12 mo | PM (acute) | Clinical malaria | OR | 4.20 (1.94–9.12) | 4.63 (2.10–10.24) | HIV status, malaria during pregnancy, and maternal mid-upper arm circumference | 7 |
| PM (chronic) | Clinical malaria | OR | 3.82 (2.06–7.08) | 3.95 (2.07–7.55) | HIV status, malaria during pregnancy, and maternal mid-upper arm circumference | ||||||
| Clinical malaria | Clinical malaria | OR | 2.40 (1.45–3.98) | 1.96 (1.13–3.41) | HIV status, PM, and maternal mid-upper arm circumference | ||||||
| Borgella et al [13] | Benin | Cohort | 194 | 12 mo | PAM (1st trimester) | Parasitemia | OR | 1.33 (0.36–4.94) | 1.12 (0.23–5.45) | PM, age, distance from lake, bednet use, and birth season | 9 |
| PAM (1st trimester) | Clinical malaria | OR | 1.19 (0.35–4.08) | 0.83 (0.13–5.18) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (2nd trimester) | Parasitemia | OR | 1.14 (0.58–2.23) | 0.87 (0.35–2.09) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (2nd trimester) | Clinical malaria | OR | 1.24 (0.61–2.52) | 0.81 (0.31–2.12) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (3rd trimester) | Parasitemia | OR | 2.77 (1.49–5.15) | 4.16 (1.64–10.54) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (3rd trimester) | Clinical malaria | OR | 2.80 (1.45–5.42) | 4.61 (1.70–12.45) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PM | Parasitemia | OR | 1.58 (0.75–3.32) | 0.72 (0.25–2.11) | PAM, age, distance from lake, bednet use, and birth season | ||||||
| PM | Clinical malaria | OR | 1.53 (0.70–3.34) | 0.59 (0.18–1.88) | PAM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (1st trimester) | First parasitemia | HR | 1.30 (0.57–2.92) | 1.00 (0.42–2.39) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (1st trimester) | First clinical malaria | HR | 1.44 (0.49–4.19) | 0.97 (0.32–2.92) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (2nd trimester) | First parasitemia | HR | 1.27 (0.73–2.19) | 1.14 (0.62–2.12) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (2nd trimester) | First clinical malaria | HR | 1.35 (0.74–2.47) | 1.15 (0.58–2.28) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (3rd trimester) | First parasitemia | HR | 2.23 (1.36–3.65) | 2.95 (1.58–5.50) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PAM (3rd trimester) | First clinical malaria | HR | 2.26 (1.29–3.96) | 3.19 (1.59–6.38) | PM, age, distance from lake, bednet use, and birth season | ||||||
| PM | First parasitemia | HR | 1.41 (0.79–2.52) | 0.68 (0.34–1.38) | PAM, age, distance from lake, bednet use, and birth season | ||||||
| PM | First clinical malaria | HR | 1.33 (0.69–2.54) | 0.60 (0.28–1.32) | PAM, age, distance from lake, bednet use, and birth season | ||||||
| Boudová et al [20] | Malawi | RCT | 473 | 1 y | PM | Parasitemia | OR | 2.7(1.1–6.7) | 2.5 (1.0–6.3) | Age, GA, and clinical trial arm | 6 |
| PM | Clinical malaria | OR | 4.1 (1.3–13.1) | 3.9 (1.2–13.0) | Age, GA, and clinical trial arm | ||||||
| Parasitemia | Parasitemia | OR | 1.5 (0.5–4.4) | 1.5 (0.5–4.4) | Age, GA, and clinical trial arm | ||||||
| Parasitemia | Clinical malaria | OR | 1.5 (0.3–7.3) | 1.4 (0.3–7.0) | Age, GA, and clinical trial arm | ||||||
| 2 y | PM | Parasitemia | OR | 2.6 (1.0–6.6) | 2.8 (1.1–7.5) | Age, GA, and clinical trial arm | |||||
| PM | Clinical malaria | OR | 2.8 (1.0–7.9) | 3.2 (1.1–9.4) | Age, GA, and clinical trial arm | ||||||
| Parasitemia | Parasitemia | OR | 1.4 (0.5–3.8) | 1.5 (0.6–4.1) | Age, GA, and clinical trial arm | ||||||
| Parasitemia | Clinical malaria | OR | 1.3 (0.4–4.4) | 1.5 (0.4–4.9) | Age, GA, and clinical trial arm | ||||||
| PM | Cum. parasitemia | RRR | 1.6 (1.0–2.6) | NA | NA | ||||||
| PM | Cum. clinical malaria | RRR | 2.3 (1.1–4.8) | NA | NA | ||||||
| Parasitemia | Cum. parasitemia | RRR | 1.4 (0.8–2.4) | NA | NA | ||||||
| Parasitemia | Cum. clinical malaria | RRR | 2.1 (1.0– 4.5) | NA | NA | ||||||
| Gonçalves et al [12] | Tanzania | Cohort | 882 | 4 y | PM (1st delivery) | First clinical malaria | HR | NA | 1.12 (0.44–2.82) | Hgb genotype, bednet use, sex, village of residence, and season | 9 |
| 4 y | PM (1st delivery) | Parasite density | Coefficient | NA | 0.16 (−0.20 to 0.52) | Hgb genotype, bednet use, sex, village of residence, and season | |||||
| Le Port et al [33] | Benin | Cohort | 545 | 18 mo | PM | First parasitemia | HR | 1.59 (1.17–2.16) | 1.57 (1.16–2.14) | Exposure prediction | 9 |
| Mutabingwa et al [35] | Tanzania | Cohort | 453 | 54 wk | PM | First parasitemia | HR | 1.33 (0.97–1.83) | 1.41 (1.01–1.99) | Residence area, birth season, gravidity, and bednet use | 9 |
| Ndibazza et al [19] | Uganda | RCT | 2289 | 5 y | PAM | All episodes of clinical malaria | HR | NA | 1.23 (1.01–1.51) | Age, parity, education, bednet ownership, SES, HIV status, and residence area | 8 |
| PAM | All episodes of asymptomatic malaria | HR | NA | 1.27 (0.83–1.97) | Age, parity, education, bednet ownership, SES, HIV status, and residence area | ||||||
| Schwarz et al [36] | Gabon | RCT | 527 | 30 mo | PM | First clinical malaria | HR | 2.3 (1.3–3.9) | 2.1 (1.2–3.7) | Gravidity, residence area, birth season, preventive treatment, and bednet use | 7 |
| Sylvester et al [34] | Tanzania | Cohort | 206 | 24 mo | PM | Clinical malaria | OR | 4.632 (2.248–9.541) | 4.791 (2.21–10.38) | Gravidity, birth weight, age, and birth season | 9 |
| Tassi Yunga et al [11] | Cameroon | Cohort | 72 | 12 mo | PM (PM + High) | First parasitemia | HR | 1.5 (0.8–2.8) | 1.5 (0.7–3.1) | Residence area, gravidity, birth season, Hgb genotype, and cord MSP1 IgG level | 7 |
| PM (PM + Low) | First parasitemia | HR | 2.6 (1.3–4.8) | 2.8 (1.3–6.0) | Residence area, gravidity, birth season, Hgb genotype, and cord MSP1 IgG level | ||||||
| Studies Included in Systematic Review but Not Meta-Analyses | |||||||||||
| Awine et al [41] | Ghana | RCT | 686 | 12 mo | PM | Clinical malaria | Rate ratio | NA | 0.86 (0.54–1.37) | Age, parasitemia status at enrolment, Hgb, birth season, sex, SES, residence area, irrigated area, and ITN use | 8 |
| Bonner et al [39] | Kenya | Case Control | 100 | 12 mo | PM | Parasitemia | Proportion | 15.6% in PM+ and 14.7% in PM− | NA | NA | 6 |
| Clinical malaria | Proportion | 3.6% in PM+ and 1.4% in PM− | NA | NA | |||||||
| Cot et al [44] | Cameroon | Cohort | 79 | 2 y | PM | High, medium, and low density parasitemia | OR | NA | 2.3 (0.38–14), 2.6 (0.46–15), and 0.4 (0.05–2.90) | 2H3 chondroitin sulfate, gravidity, and residence area | 6 |
| PM | High, medium, and low density parasitemia | OR | NA | 2.6 (0.39–17), 2.8 (0.50–16), and 0.4 (0.05–3.4) | Palo Alto chondroitin sulfate, gravidity, and residence area | ||||||
| De Beaudrap et al [40] | Uganda | RCT | 832 | 12 mo | Parasitemia | First parasitemia | RR | NA | 2.97 (1.37–6.42) | Education, age, gravidity, residence area, season, HIV status, and bednet use | 8 |
| PM | First parasitemia | RR | NA | 10.42 (2.64–41.10) | Education, age, gravidity, residence area, season, HIV status, and bednet use | ||||||
| Le Hesran et al [43] | Cameroon | Cohort | 197 | 2 y | PM | Parasitemia | Prevalence | Higher in PM+ between 5 and 8 mo | NA | NA | 6 |
| PM | Clinical malaria | Prevalence | 46.5% in PM+ and 38.5% in PM− | NA | NA | ||||||
| Malhotra et al [10] | Kenya | Cohort | 586 | 3 y | PAM | Parasitemia | RR | Exposed/sensitized: 1.4 (0.97–2.07), not exposed: 1.61 (1.10–2.43) | NA | NA | 9 |
| Mutabingwa et al [38] | Tanzania | CT | 327 | 1 y | Parasitemia | Parasitemia | N (episodes) | 3–5 vs 6–7 median no. of parasitemia episodes in infants of mothers who had no parasitemia vs 2+ episodes of parasitemia, respiratory | NA | NA | 7 |
| Slutsker et al [42] | Malawi | RCT | 3915 | 3 mo | Parasitemia | Parasitemia | OR | 1.1 (0.7–1.9) | NA | NA | 6 |
| PM | Parasitemia | OR | 1.2 (0.9–1.4) | NA | NA |
Abbreviations: Cum., cumulative; CT, clinical trial (not randomized); GA, gestational age at delivery; Hgb, hemoglobin; HIV, human immunodeficiency virus; HR, hazard ratio; IgG, immunoglobulin G; ITN, insecticide-treated bed net; mo, months; n, number; NA, not applicable; NOS, Newcastle-Ottawa quality scale; OR, odds ratio; PAM, pregnancy-associated malaria; PM, placental malaria; PM+/−, PM positive/negative group; RCT, randomized controlled trial; RR, relative risk; RRR, relative rate ratio; SES, socioeconomic status; wk, weeks; y, years.
aAge and HIV status refer to maternal age and HIV status.