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Review
. 2016 May 6;2016(5):CD004073.
doi: 10.1002/14651858.CD004073.pub4.

Vitamin supplementation for preventing miscarriage

Olukunmi O Balogun  1 , Katharina da Silva Lopes, Erika Ota, Yo Takemoto, Alice Rumbold, Mizuki Takegata, Rintaro Mori
Affiliations
Review

Vitamin supplementation for preventing miscarriage

Olukunmi O Balogun et al. Cochrane Database Syst Rev. .

Abstract

Background: Miscarriage is a common complication of pregnancy that can be caused by a wide range of factors. Poor dietary intake of vitamins has been associated with an increased risk of miscarriage, therefore supplementing women with vitamins either prior to or in early pregnancy may help prevent miscarriage.

Objectives: The objectives of this review were to determine the effectiveness and safety of any vitamin supplementation, on the risk of spontaneous miscarriage.

Search methods: We searched the Cochrane Pregnancy and Childbirth Group Trials Register (6 November 2015) and reference lists of retrieved studies.

Selection criteria: All randomised and quasi-randomised trials comparing supplementation during pregnancy with one or more vitamins with either placebo, other vitamins, no vitamins or other interventions. We have included supplementation that started prior to conception, periconceptionally or in early pregnancy (less than 20 weeks' gestation).

Data collection and analysis: Three review authors independently assessed trials for inclusion, extracted data and assessed trial quality. We assessed the quality of the evidence using the GRADE approach. The quality of evidence is included for numerical results of outcomes included in the 'Summary of findings' tables.

Main results: We included a total of 40 trials (involving 276,820 women and 278,413 pregnancies) assessing supplementation with any vitamin(s) starting prior to 20 weeks' gestation and reporting at least one primary outcome that was eligible for the review. Eight trials were cluster-randomised and contributed data for 217,726 women and 219,267 pregnancies in total.Approximately half of the included trials were assessed to have a low risk of bias for both random sequence generation and adequate concealment of participants to treatment and control groups. Vitamin C supplementation There was no difference in the risk of total fetal loss (risk ratio (RR) 1.14, 95% confidence interval (CI) 0.92 to 1.40, seven trials, 18,949 women; high-quality evidence); early or late miscarriage (RR 0.90, 95% CI 0.65 to 1.26, four trials, 13,346 women; moderate-quality evidence); stillbirth (RR 1.31, 95% CI 0.97 to 1.76, seven trials, 21,442 women; moderate-quality evidence) or adverse effects of vitamin supplementation (RR 1.16, 95% CI 0.39 to 3.41, one trial, 739 women; moderate-quality evidence) between women receiving vitamin C with vitamin E compared with placebo or no vitamin C groups. No clear differences were seen in the risk of total fetal loss or miscarriage between women receiving any other combination of vitamin C compared with placebo or no vitamin C groups. Vitamin A supplementation No difference was found in the risk of total fetal loss (RR 1.01, 95% CI 0.61 to 1.66, three trials, 1640 women; low-quality evidence); early or late miscarriage (RR 0.86, 95% CI 0.46 to 1.62, two trials, 1397 women; low-quality evidence) or stillbirth (RR 1.29, 95% CI 0.57 to 2.91, three trials, 1640 women; low-quality evidence) between women receiving vitamin A plus iron and folate compared with placebo or no vitamin A groups. There was no evidence of differences in the risk of total fetal loss or miscarriage between women receiving any other combination of vitamin A compared with placebo or no vitamin A groups. Multivitamin supplementation There was evidence of a decrease in the risk for stillbirth among women receiving multivitamins plus iron and folic acid compared iron and folate only groups (RR 0.92, 95% CI 0.85 to 0.99, 10 trials, 79,851 women; high-quality evidence). Although total fetal loss was lower in women who were given multivitamins without folic acid (RR 0.49, 95% CI 0.34 to 0.70, one trial, 907 women); and multivitamins with or without vitamin A (RR 0.60, 95% CI 0.39 to 0.92, one trial, 1074 women), these findings included one trial each with small numbers of women involved. Also, they include studies where the comparison groups included women receiving either vitamin A or placebo, and thus require caution in interpretation.We found no difference in the risk of total fetal loss (RR 0.96, 95% CI 0.93 to 1.00, 10 trials, 94,948 women; high-quality evidence) or early or late miscarriage (RR 0.98, 95% CI 0.94 to 1.03, 10 trials, 94,948 women; moderate-quality evidence) between women receiving multivitamins plus iron and folic acid compared with iron and folate only groups.There was no evidence of differences in the risk of total fetal loss or miscarriage between women receiving any other combination of multivitamins compared with placebo, folic acid or vitamin A groups. Folic acid supplementation There was no evidence of any difference in the risk of total fetal loss, early or late miscarriage, stillbirth or congenital malformations between women supplemented with folic acid with or without multivitamins and/or iron compared with no folic acid groups. Antioxidant vitamins supplementation There was no evidence of differences in early or late miscarriage between women given antioxidant compared with the low antioxidant group (RR 1.12, 95% CI 0.24 to 5.29, one trial, 110 women).

Authors' conclusions: Taking any vitamin supplements prior to pregnancy or in early pregnancy does not prevent women experiencing miscarriage. However, evidence showed that women receiving multivitamins plus iron and folic acid had reduced risk for stillbirth. There is insufficient evidence to examine the effects of different combinations of vitamins on miscarriage and miscarriage-related outcomes.

PubMed Disclaimer

Conflict of interest statement

Alice Rumbold is an investigator on the Australian Collaborative Trial of Supplements with vitamin C and vitamin E for the prevention of pre‐eclampsia (Rumbold 2006). This trial is included in this review but its eligibility for inclusion, trial quality assessments and data extraction were carried out independently by two of the review authors not involved in the original trial.

Erika Ota: none known.

Olukunmi O Balogun: none known.

Katharina da Silva Lopes: none known.

Yo Takemoto: none known.

Mizuki Takegata: none known.

Rintaro Mori's institution receives government funding from the Clinical Research Program for Child Health and Development, AMED, Japan to provide support for the PCG Satellite in Japan.

Figures

1
1
'Risk of bias' graph: review authors' judgements about each risk of bias item presented as percentages across all included studies
2
2
'Risk of bias' summary: review authors' judgements about each risk of bias item for each included study
3
3
Funnel plot of comparison: 9 Multivitamin plus iron and folic acid versus iron and folic acid, outcome: 9.1 Total fetal loss.
4
4
Funnel plot of comparison: 9 Multivitamin plus iron and folic acid versus iron and folic acid, outcome: 9.2 Early or late miscarriage.
5
5
Funnel plot of comparison: 9 Multivitamin plus iron and folic acid versus iron and folic acid, outcome: 9.3 Stillbirth.
1.1
1.1. Analysis
Comparison 1 Vitamin C plus vitamin E versus placebo, Outcome 1 Total fetal loss.
1.2
1.2. Analysis
Comparison 1 Vitamin C plus vitamin E versus placebo, Outcome 2 Early or late miscarriage.
1.3
1.3. Analysis
Comparison 1 Vitamin C plus vitamin E versus placebo, Outcome 3 Stillbirth.
1.4
1.4. Analysis
Comparison 1 Vitamin C plus vitamin E versus placebo, Outcome 4 Congenital malformations.
1.5
1.5. Analysis
Comparison 1 Vitamin C plus vitamin E versus placebo, Outcome 5 Any adverse effects of vitamin supplementation sufficient to stop supplementation.
2.1
2.1. Analysis
Comparison 2 Vitamin C versus no supplement/placebo, Outcome 1 Total fetal loss.
2.2
2.2. Analysis
Comparison 2 Vitamin C versus no supplement/placebo, Outcome 2 Early or late miscarriage.
2.3
2.3. Analysis
Comparison 2 Vitamin C versus no supplement/placebo, Outcome 3 Stillbirth.
3.1
3.1. Analysis
Comparison 3 Vitamin C plus multivitamins versus placebo plus multivitamins or multivitamins alone, Outcome 1 Total fetal loss.
3.2
3.2. Analysis
Comparison 3 Vitamin C plus multivitamins versus placebo plus multivitamins or multivitamins alone, Outcome 2 Early or late miscarriage.
4.1
4.1. Analysis
Comparison 4 Vitamin A plus iron and folate versus iron and folate, Outcome 1 Total fetal loss.
4.2
4.2. Analysis
Comparison 4 Vitamin A plus iron and folate versus iron and folate, Outcome 2 Early or late miscarriage.
4.3
4.3. Analysis
Comparison 4 Vitamin A plus iron and folate versus iron and folate, Outcome 3 Stillbirth.
5.1
5.1. Analysis
Comparison 5 Vitamin A versus placebo, Outcome 1 Total fetal loss.
5.2
5.2. Analysis
Comparison 5 Vitamin A versus placebo, Outcome 2 Early of late miscarriage.
5.3
5.3. Analysis
Comparison 5 Vitamin A versus placebo, Outcome 3 Stillbirth.
6.1
6.1. Analysis
Comparison 6 Beta‐carotene versus placebo, Outcome 1 Total fetal loss.
6.2
6.2. Analysis
Comparison 6 Beta‐carotene versus placebo, Outcome 2 Early or late miscarriage.
6.3
6.3. Analysis
Comparison 6 Beta‐carotene versus placebo, Outcome 3 Stillbirth.
7.1
7.1. Analysis
Comparison 7 Vitamin A or beta‐carotene versus placebo, Outcome 1 Total fetal loss.
8.1
8.1. Analysis
Comparison 8 Vitamin A (with/without multivitamins) versus multivitamins or placebo, Outcome 1 Total fetal loss.
8.2
8.2. Analysis
Comparison 8 Vitamin A (with/without multivitamins) versus multivitamins or placebo, Outcome 2 Early or late miscarriage.
8.3
8.3. Analysis
Comparison 8 Vitamin A (with/without multivitamins) versus multivitamins or placebo, Outcome 3 Stillbirth.
9.1
9.1. Analysis
Comparison 9 Multivitamin plus iron and folic acid versus iron and folic acid, Outcome 1 Total fetal loss.
9.2
9.2. Analysis
Comparison 9 Multivitamin plus iron and folic acid versus iron and folic acid, Outcome 2 Early or late miscarriage.
9.3
9.3. Analysis
Comparison 9 Multivitamin plus iron and folic acid versus iron and folic acid, Outcome 3 Stillbirth.
9.4
9.4. Analysis
Comparison 9 Multivitamin plus iron and folic acid versus iron and folic acid, Outcome 4 Congenital malformation.
10.1
10.1. Analysis
Comparison 10 Multivitamin without folic acid versus no multivitamin/folic acid, Outcome 1 Total fetal loss.
10.2
10.2. Analysis
Comparison 10 Multivitamin without folic acid versus no multivitamin/folic acid, Outcome 2 Early or late miscarriage.
10.3
10.3. Analysis
Comparison 10 Multivitamin without folic acid versus no multivitamin/folic acid, Outcome 3 Stillbirth.
10.4
10.4. Analysis
Comparison 10 Multivitamin without folic acid versus no multivitamin/folic acid, Outcome 4 Congenital malformations.
11.1
11.1. Analysis
Comparison 11 Multivitamin with/without folic acid versus no multivitamin/folic acid, Outcome 1 Total fetal loss.
11.2
11.2. Analysis
Comparison 11 Multivitamin with/without folic acid versus no multivitamin/folic acid, Outcome 2 Early or late miscarriage.
11.3
11.3. Analysis
Comparison 11 Multivitamin with/without folic acid versus no multivitamin/folic acid, Outcome 3 Stillbirth.
11.4
11.4. Analysis
Comparison 11 Multivitamin with/without folic acid versus no multivitamin/folic acid, Outcome 4 Congenital malformations.
12.1
12.1. Analysis
Comparison 12 Multivitamin plus folic acid versus folic acid, Outcome 1 Total fetal loss.
12.2
12.2. Analysis
Comparison 12 Multivitamin plus folic acid versus folic acid, Outcome 2 Early or late miscarriage.
12.3
12.3. Analysis
Comparison 12 Multivitamin plus folic acid versus folic acid, Outcome 3 Stillbirth.
12.4
12.4. Analysis
Comparison 12 Multivitamin plus folic acid versus folic acid, Outcome 4 Congenital malformations.
13.1
13.1. Analysis
Comparison 13 Multivitamin without folic acid versus folic acid, Outcome 1 Total fetal loss.
13.2
13.2. Analysis
Comparison 13 Multivitamin without folic acid versus folic acid, Outcome 2 Early or late miscarriage.
13.3
13.3. Analysis
Comparison 13 Multivitamin without folic acid versus folic acid, Outcome 3 Stillbirth.
13.4
13.4. Analysis
Comparison 13 Multivitamin without folic acid versus folic acid, Outcome 4 Congenital malformations.
14.1
14.1. Analysis
Comparison 14 Multivitamin with/without folic acid versus folic acid, Outcome 1 Total fetal loss.
14.2
14.2. Analysis
Comparison 14 Multivitamin with/without folic acid versus folic acid, Outcome 2 Early of late miscarriage.
14.3
14.3. Analysis
Comparison 14 Multivitamin with/without folic acid versus folic acid, Outcome 3 Stillbirth.
14.4
14.4. Analysis
Comparison 14 Multivitamin with/without folic acid versus folic acid, Outcome 4 Congenital malformations.
15.1
15.1. Analysis
Comparison 15 Multivitamin with/without vitamin A versus vitamin A or placebo, Outcome 1 Total fetal loss.
16.1
16.1. Analysis
Comparison 16 Multivitamin versus control, Outcome 1 Total fetal loss.
16.2
16.2. Analysis
Comparison 16 Multivitamin versus control, Outcome 2 Stillbirth.
17.1
17.1. Analysis
Comparison 17 Multivitamin plus vitamin E versus multivitamin without vitamin E or control, Outcome 1 Total fetal loss.
17.2
17.2. Analysis
Comparison 17 Multivitamin plus vitamin E versus multivitamin without vitamin E or control, Outcome 2 Early or late miscarriage.
17.3
17.3. Analysis
Comparison 17 Multivitamin plus vitamin E versus multivitamin without vitamin E or control, Outcome 3 Stillbirth.
18.1
18.1. Analysis
Comparison 18 Multivitamin plus folic acid versus no multivitamin/folic acid, Outcome 1 Total fetal loss.
18.2
18.2. Analysis
Comparison 18 Multivitamin plus folic acid versus no multivitamin/folic acid, Outcome 2 Early or late miscarriage.
18.3
18.3. Analysis
Comparison 18 Multivitamin plus folic acid versus no multivitamin/folic acid, Outcome 3 Stillbirth.
18.4
18.4. Analysis
Comparison 18 Multivitamin plus folic acid versus no multivitamin/folic acid, Outcome 4 Congenital malformations.
19.1
19.1. Analysis
Comparison 19 Folic acid plus multivitamin versus no folic acid/multivitamin, Outcome 1 Total fetal loss.
19.2
19.2. Analysis
Comparison 19 Folic acid plus multivitamin versus no folic acid/multivitamin, Outcome 2 Early or late miscarriage.
19.3
19.3. Analysis
Comparison 19 Folic acid plus multivitamin versus no folic acid/multivitamin, Outcome 3 Stillbirth.
19.4
19.4. Analysis
Comparison 19 Folic acid plus multivitamin versus no folic acid/multivitamin, Outcome 4 Congenital malformations.
20.1
20.1. Analysis
Comparison 20 Folic acid without multivitamin versus no folic acid/multivitamin, Outcome 1 Total fetal loss.
20.2
20.2. Analysis
Comparison 20 Folic acid without multivitamin versus no folic acid/multivitamin, Outcome 2 Early or late miscarriage.
20.3
20.3. Analysis
Comparison 20 Folic acid without multivitamin versus no folic acid/multivitamin, Outcome 3 Stillbirth.
20.4
20.4. Analysis
Comparison 20 Folic acid without multivitamin versus no folic acid/multivitamin, Outcome 4 Congenital malformations.
21.1
21.1. Analysis
Comparison 21 Folic acid with/without multivitamin versus no folic acid/multivitamin, Outcome 1 Total fetal loss.
21.2
21.2. Analysis
Comparison 21 Folic acid with/without multivitamin versus no folic acid/multivitamin, Outcome 2 Early or late miscarriage.
21.3
21.3. Analysis
Comparison 21 Folic acid with/without multivitamin versus no folic acid/multivitamin, Outcome 3 Stillbirth.
21.4
21.4. Analysis
Comparison 21 Folic acid with/without multivitamin versus no folic acid/multivitamin, Outcome 4 Congenital malformations.
22.1
22.1. Analysis
Comparison 22 Folic acis plus multivitamin versus multivitamin, Outcome 1 Total fetal loss.
22.2
22.2. Analysis
Comparison 22 Folic acis plus multivitamin versus multivitamin, Outcome 2 Early or late miscarriage.
22.3
22.3. Analysis
Comparison 22 Folic acis plus multivitamin versus multivitamin, Outcome 3 Stillbirth.
22.4
22.4. Analysis
Comparison 22 Folic acis plus multivitamin versus multivitamin, Outcome 4 Congenital malformations.
23.1
23.1. Analysis
Comparison 23 Folic acid without multivitamin versus multivitamin, Outcome 1 Total fetal loss.
23.2
23.2. Analysis
Comparison 23 Folic acid without multivitamin versus multivitamin, Outcome 2 Early or late miscarriage.
23.3
23.3. Analysis
Comparison 23 Folic acid without multivitamin versus multivitamin, Outcome 3 Stillbirth.
23.4
23.4. Analysis
Comparison 23 Folic acid without multivitamin versus multivitamin, Outcome 4 Congenital malformations.
24.1
24.1. Analysis
Comparison 24 Folic acid with or without multivitamin versus multivitamin, Outcome 1 Total fetal loss.
24.2
24.2. Analysis
Comparison 24 Folic acid with or without multivitamin versus multivitamin, Outcome 2 Early or late miscarriage.
24.3
24.3. Analysis
Comparison 24 Folic acid with or without multivitamin versus multivitamin, Outcome 3 Stillbirth.
24.4
24.4. Analysis
Comparison 24 Folic acid with or without multivitamin versus multivitamin, Outcome 4 Congenital malformations.
25.1
25.1. Analysis
Comparison 25 Folic acid plus iron versus iron, Outcome 1 Total fetal loss.
25.2
25.2. Analysis
Comparison 25 Folic acid plus iron versus iron, Outcome 2 Early or late miscarriage.
25.3
25.3. Analysis
Comparison 25 Folic acid plus iron versus iron, Outcome 3 Stillbirth.
26.1
26.1. Analysis
Comparison 26 Folic acid plus iron and antimalarials versus iron and antimalarials, Outcome 1 Total fetal loss.
26.2
26.2. Analysis
Comparison 26 Folic acid plus iron and antimalarials versus iron and antimalarials, Outcome 2 Early or late miscarriage.
27.1
27.1. Analysis
Comparison 27 Antioxidant vitamin supplementation, Outcome 1 Early or late miscarriage.
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References

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Poston 2006 {published data only}
    1. Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH, for the Vitamins in Pre‐eclampsia (VIP) Trial Consortium. Vitamin C and vitamin E in pregnant women at risk forpre‐eclampsia (VIP trial): randomised placebo‐controlled trial. Lancet 2006;367:1145–54. - PubMed
Prawirohartono 2011 {published data only}
    1. Prawirohartono EP, Nystrom L, Ivarsson A, Stenlund H, Lind T. The impact of prenatal vitamin A and zinc supplementation on growth of children up to 2 years of age in rural Java, Indonesia. Public Health Nutrition 2011;14(12):2197‐206. - PubMed
    1. Prawirohartono EP, Nystrom L, Nurdiati DS, Hakimi M, Lind T. The impact of prenatal vitamin A and zinc supplementation on birth size and neonatal survival ‐ a double‐blind, randomized controlled trial in a rural area of Indonesia. International Journal for Vitamin and Nutrition Research 2013;83(1):14‐25. - PubMed
Roberfroid 2008 {published data only}
    1. Roberfroid D, Huybregts L, Habicht JP, Lanou H, Henry MC, Meda N, et al. Randomized controlled trial of 2 prenatal iron supplements: is there a dose‐response relation with maternal hemoglobin?. American Journal of Clinical Nutrition 2011;93(5):1012‐8. - PubMed
    1. Roberfroid D, Huybregts L, Lanou H, Habicht JP, Henry MC, Meda N, et al. Prenatal micronutrient supplements cumulatively increase fetal growth. Journal of Nutrition 2012;142(3):548‐54. - PubMed
    1. Roberfroid D, Huybregts L, Lanou H, Henry MC, Meda N, Kolsteren FP, et al. Effect of maternal multiple micronutrient supplements on cord blood hormones: a randomized controlled trial. American Journal of Clinical Nutrition 2010;91(6):1649‐58. - PubMed
    1. Roberfroid D, Huybregts L, Lanou H, Henry MC, Meda N, Menten J, et al. Effects of maternal multiple micronutrient supplementation on fetal growth: a double‐blind randomized controlled trial in rural Burkina Faso. American Journal of Clinical Nutrition 2008;88(5):1330‐40. - PubMed
    1. Roberfroid D, Huybregts L, Lanou H, Ouedraogo L, Henry MC, Meda N, et al. Impact of prenatal multiple micronutrients on survival and growth during infancy: a randomized controlled trial. American Journal of Clinical Nutrition 2012;95(4):916‐24. - PubMed
Roberts 2010 {published data only}
    1. Gandley R, Abramovici A. Prenatal vitamin C and e supplementation is associated with a reduction in placental abruption and preterm birth in smokers. Pregnancy Hypertension 2012;2(3):331‐2. - PubMed
    1. Hauth J, for the Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal‐Fetal Medicine Units Network. Vitamin C and E supplementation to prevent preterm premature rupture of membranes. American Journal of Obstetrics and Gynecology 2009;201(6 Suppl 1):S175‐S176.
    1. Hauth JC. Maternal insulin resistance and preeclampsia. American Journal of Obstetrics & Gynecology 2011;204(1 Suppl):S12. - PMC - PubMed
    1. Hauth JC, Clifton RG, Roberts JM, Myatt L, Spong CY, Leveno KJ, et al. Maternal insulin resistance and preeclampsia. American Journal of Obstetrics and Gynecology 2011;204(4):327.e1‐6. - PMC - PubMed
    1. Hauth JC, Clifton RG, Roberts JM, Spong CY, Myatt L, Leveno KJ, et al. Vitamin C and E supplementation to prevent spontaneous preterm birth: a randomized controlled trial. Obstetrics & Gynecology 2010;116(3):653‐8. - PMC - PubMed
Rumbold 2006 {published data only}
    1. Rumbold AR, Crowther CA, Haslam RR, Dekker GA, Robinson JS. Australian collaborative trial of supplements (ACTS) with vitamin C and E for the prevention of pre‐eclampsia ‐ a randomised controlled trial. Perinatal Society of Australia and New Zealand 10th Annual Congress; 2006 April 3‐6; Perth, Australia. 2006:180.
    1. Rumbold AR, Crowther CA, Haslam RR, Dekker GA, Robinson JS, for the ACTS Study Group. Vitamins C and E and the risks of preeclampsia and perinatal complications. New England Journal of Medicine 2006;354(17):1796‐806. - PubMed
Rumiris 2006 {published data only}
    1. Rumiris D, Purwosunu Y, Wibowo N, Farina A, Sekizawa A. Lower rate of preeclampsia after antioxidant supplementation in pregnant women with low antioxidant status. Hypertension in Pregnancy 2006;25(3):241‐53. - PubMed
Rush 1980 {published data only}
    1. Rush D, Kristal A, Navarro C, Chaunhan P, Blanc W, Naeye R, et al. The effects of dietary supplementation during pregnancy on placental morphology, pathology and histomorphometry. American Journal of Clinical Nutrition 1984;39:863‐71. - PubMed
    1. Rush D, Stein Z, Susser M. A randomized trial of prenatal nutritional supplementation in New York City. Pediatrics 1980;65(4):683‐97. - PubMed
Schmidt 2001 {published data only}
    1. Muslimatun S, Schmidt MK, Schultink W, West CE, Hautvast JA, Gross R, et al. Weekly supplementation with iron and vitamin A during pregnancy increases hemoglobin concentration but decreases serum ferritin concentration in Indonesian pregnant women. Journal of Nutrition 2001;131(1):85‐90. - PubMed
    1. Muslimatun S, Schmidt MK, West CE, Schultink W, Gross R, Hautvast JG. Determinants of weight and length of Indonesian neonates. European Journal of Clinical Nutrition 2002;56(10):947‐51. - PubMed
    1. Muslimatun S, Schmidt MK, West CE, Schultink W, Hautvast JG, Karyadi D. Weekly vitamin A and iron supplementation during pregnancy increases vitamin A concentration of breast milk but not iron status in Indonesian lactating women. Journal of Nutrition 2001;131(10):2664‐9. - PubMed
    1. Schmidt MK, Muslimatun S, West CE, Schultink W, Hautvast JG. Randomised double‐blind trial of the effect of vitamin A supplementation of Indonesian pregnant women on morbidity and growth of their infants during the first year of life. European Journal of Clinical Nutrition 2002;56:338‐46. - PubMed
    1. Schmidt MK, Muslimatun S, West CE, Schultink W, Hautvast JG. Vitamin A and iron supplementation of Indonesian pregnant women benefits vitamin A status of their infants. British Journal of Nutrition 2001;86:607‐15. - PubMed
Spinnato 2007 {published data only}
    1. Spinnato II JA, Freire S, Silva JL, Cunha Rudge MV, Martins‐Costa S, Koch MA, et al. Antioxidant therapy to prevent preeclampsia: a randomized controlled trial. Obstetrics & Gynecology 2007;110(6):1311‐8. - PubMed
Steyn 2003 {published data only}
    1. Schoeman J, Steyn PS, Odendaal HJ, Grove D. Bacterial vaginosis diagnosed at the first antenatal visit better predicts preterm labour than diagnosis later in pregnancy. Journal of Obstetrics and Gynaecology 2005;25(8):751‐3. - PubMed
    1. Steyn PS, Odendaal HJ, Schoeman J, Grove D. Vitamin c, pre‐eclampsia and preterm labour: a randomized, placebo‐controlled, double blind trial [abstract]. Hypertension in Pregnancy 2002;21(Suppl 1):43.
    1. Steyn PS, Odendaal HJ, Schoeman J, Stander C, Fanie N, Grove D. A randomised, double blind placebo‐controlled trial of ascorbic acid supplementation for the prevention of preterm labour. Journal of Obstetrics and Gynaecology 2003;23(2):150‐5. - PubMed
Summit 2008 {published data only}
    1. Prado E, Sebayang S, Apriatni M, Hidayati N, Adawiyah S, Islamiyah A, et al. Maternal multiple micronutrient supplementation and children's cognition at age 9‐12 years in Indonesia. FASEB Journal 2015;29(1 Suppl):[28.7]. - PubMed
    1. Prado EL, Alcock KJ, Muadz H, Ullman MT, Shankar AH, for the SUMMIT Study Group. Maternal multiple micronutrient supplements and child cognition: a randomized trial in Indonesia. Pediatrics 2012;130(3):e536‐e546. - PubMed
    1. Prado EL, Ullman MT, Muadz H, Alcock KJ, Shankar AH. The effect of maternal multiple micronutrient supplementation on cognition and mood during pregnancy and postpartum in indonesia: A randomized trial. PLoS ONE 2012;7(3):e32519. - PMC - PubMed
    1. Sebayang SK, Dibley MJ, Kelly P, Shankar AV, Shankar AH. Modifying effect of maternal nutritional status on the impact of maternal multiple micronutrient supplementation on birthweight in Indonesia. European Journal of Clinical Nutrition 2011;65(10):1110‐7. - PubMed
    1. Shankar AV, Asrilla Z, Kadha JK, Sebayang S, Apriatni M, Sulastri A, et al. Programmatic effects of a large‐scale multiple‐micronutrient supplementation trial in Indonesia: using community facilitators as intermediaries for behavior change. Food and Nutrition Bulletin 2009;30(2 Suppl):S207‐14. - PubMed
Sunawang 2009 {published data only}
    1. Sunawang, Utomo B, Hidayat A, Kusharisupeni, Subarkah. Preventing low birthweight through maternal multiple micronutrient supplementation: a cluster‐randomized, controlled trial in Indramayu, West Java. Food & Nutrition Bulletin 2009;30(4):S488‐95. - PubMed
Tofail 2008 {published data only}
    1. Ekstrom EC, Eneroth H, Arifeen SE, Persson L. Efficacy of micronutrient supplement intake in increasing hemoglobin in pregnancy: Dose‐effect comparisons with multiple micronutrient in the MINIMat trial in rural Bangladesh. FASEB Journal 2013;27 Suppl:Abstract no: 845.25.
    1. Eneroth H, Arifeen S, Persson LA, Lonnerdal B, Hossain MB, Stephensen CB, et al. Maternal multiple micronutrient supplementation has limited impact on micronutrient status of Bangladeshi infants compared with standard iron and folic acid supplementation. Journal of Nutrition 2010;140(3):618‐24. - PubMed
    1. Eneroth H, Persson LA, Arifeen S, Ekstrom EC. Infant anaemia is associated with infection, low birthweight and iron deficiency in rural Bangladesh. Acta Paediatrica 2011;100(2):220‐5. - PubMed
    1. Hawkesworth S, Wagatsuma Y, Kahn AI, Hawlader MD, Fulford AJ, Arifeen SE, et al. Combined food and micronutrient supplements during pregnancy have limited impact on child blood pressure and kidney function in rural Bangladesh. Journal of Nutrition 2013;143(5):728‐34. - PMC - PubMed
    1. Khan A, Kabir I, Ekstrom EC, Asling‐Monemi K, Alam D, Frongillo EA, et al. Effects of prenatal food and micronutrient supplementation on child growth from birth to 54 months of age: A randomized trial in Bangladesh. Nutrition Journal 2011;10(1):134. - PMC - PubMed
Van den Broek 2006 {published data only}
    1. Broek N. Vitamin A supplementation for anaemia in pregnancy. Personal communication 1998.
    1. Broek NR, White SA, Flowers C, Cook JD, Letsky EA, Tanumihardjo SA, et al. Randomised trial of vitamin A supplementation in pregnant women in rural Malawi found to be anaemic on screening by HemoCue. BJOG: an International Journal of Obstetrics and Gynaecology 2006;113(5):569‐76. - PubMed
Villar 2009 {published data only}
    1. Villar J, Purwar M, Merialdi M, Zavaleta N, Ngoc N, Anthony J, et al. Effect of vitamin C & E supplementation of pregnant women at risk of preeclampsia plus low nutritional status: the WHO trial. Hypertension in Pregnancy 2008;27(4):501.
    1. Villar J, Purwar M, Merialdi M, Zavaleta N, Thi Nhu Ngoc N, Anthony J, et al. World Health Organisation multicentre randomised trial of supplementation with vitamins C and E among pregnant women at high risk for pre‐eclampsia in populations of low nutritional status from developing countries. BJOG: an international journal of obstetrics and gynaecology 2009;116(6):780‐8. - PubMed
    1. Villar J, Purwar M, Merialdi M, Zavaleta N, Tien NN, Anthony J. WHO randomized trial of vitamin C and E supplementation among women at high risk for preeclampsia and nutritional deficiency. American Journal of Obstetrics and Gynecology 2007;197(6 Suppl 1):S4, Abstract no: 8.
West 2011 {published data only}
    1. Christian P, Klemm R, Shamim AA, Ali H, Rashid M, Shaikh S, et al. Effects of vitamin A and beta‐carotene supplementation on birth size and length of gestation in rural Bangladesh: a cluster‐randomized trial. American Journal of Clinical Nutrition 2013;97(1):188‐94. - PubMed
    1. Christian P, Labrique AB, Ali H, Richman MJ, Wu L, Rashid M, et al. Maternal vitamin A and beta‐carotene supplementation and risk of bacterial vaginosis: a randomized controlled trial in rural Bangladesh. American Journal of Clinical Nutrition 2011;94(6):1643‐9. - PubMed
    1. Labrique AB, Christian P, Klemm RDW, Rashid M, Shamim AA, Massie A, et al. A cluster‐randomized, placebo‐controlled, maternal vitamin A or beta‐carotene supplementation trial in Bangladesh: design and methods. Trials 2011;12:102. - PMC - PubMed
    1. West KPJ, Christian P, Labrique AB, Rashid M, Shamim AA, Klemm RD, et al. Effects of vitamin A or beta carotene supplementation on pregnancy‐related mortality and infant mortality in rural Bangladesh: a cluster randomized trial. JAMA 2011;305(19):1986‐95. - PubMed
West 2014 {published data only}
    1. Gernand AD, Schulze KJ, Nanayakkara‐Bind A, Arguello M, Shamim AA, Ali H, et al. Effects of prenatal multiple micronutrient supplementation on fetal growth factors: a cluster‐randomized, controlled trial in rural Bangladesh. Plos One 2015;10(10):e0137269. - PMC - PubMed
    1. West KP. Antenatal micronutrient supplementation and infant survival (JiVitA‐3). ClinicalTrials.gov (http://clinicaltrials.gov) (accessed 8 July 2011). NCT00860470 2011.
    1. West KP, Shamim AA, Labrique AB, Ali H, Shaikh S, Mehra S, et al. Efficacy of antenatal multiple micronutrient (MM) vs iron‐folic acid (IFA) supplementation in improving gestational and postnatal viability in rural Bangladesh: The JiVitA‐3 trial. FASEB Journal 2013;27 Suppl:Abstract no: 358.6.
    1. West KPJ, Shamim AA, Mehra S, Labrique AB, Ali H, Shaikh S, et al. Effect of maternal multiple micronutrient vs iron‐folic acid supplementation on infant mortality and adverse birth outcomes in rural Bangladesh: the JiVitA‐3 randomized trial. JAMA 2014;312(24):2649‐58. - PubMed
Wibowo 2012 {published data only}
    1. Sezikawa A. Antioxidant supplementation in pregnant women with low antioxidant status. ClinicalTrials.gov (http://clinicaltrials.gov/) (accessed 21 June 2007) 2007.
    1. Wibowo N, Purwosunu Y, Sekizawa A, Farina A, Idriansyah L, Fitriana I. Antioxidant supplementation in pregnant women with low antioxidant status. Journal of Obstetrics & Gynaecology Research 2012;38(9):1152‐61. - PubMed
Xu 2010 {published data only}
    1. Xu H, Perez‐Cuevas R, Xiong X, Reyes H, Roy C, Julien P, et al. An international trial of antioxidants in the prevention of preeclampsia (INTAPP). American Journal of Obstetrics and Gynecology 2010;202(3):239.e1‐10. - PubMed
Zagre 2007 {published data only}
    1. Zagre NM, Desplats G, Adou P, Mamadoultaibou A, Aguayo VM. Prenatal multiple micronutrient supplementation has greater impact on birthweight than supplementation with iron and folic acid: a cluster‐randomized, double‐blind, controlled programmatic study in rural Niger. Food and Nutrition Bulletin 2007;28(3):317‐27. - PubMed
Zeng 2008 {published data only}
    1. Cao Y, Wang T, Zeng L. Risk of childhood malnutrition at 24 months related to small for gestational age and low birth weight in rural Western China. Annals of Nutrition & Metabolism 2013;63(Suppl 1):556, Abstract no: PO619.
    1. Chang S, Zeng L, Brouwer ID, Kok FJ, Yan H. Effect of iron deficiency anemia in pregnancy on child mental development in rural China. Pediatrics 2013;131(3):e755‐63. - PubMed
    1. Li Q, Yan H, Zeng L, Cheng Y, Liang W, Dang S, et al. Effects of maternal multimicronutrient supplementation on the mental development of infants in rural western China: follow‐up evaluation of a double‐blind, randomized, controlled trial. Pediatrics 2009;123(4):e685‐92. - PubMed
    1. Wang W, Yan H, Zeng L, Cheng Y, Wang D, Li Q. No effect of maternal micronutrient supplementation on early childhood growth in rural western China: 30 month follow‐up evaluation of a double blind, cluster randomized controlled trial. European Journal of Clinical Nutrition 2012;66(2):261‐8. - PubMed
    1. Yan H. Impact of iron/folate versus multi‐micronutrient supplementation during pregnancy on birth weight: a randomised controlled trial in rural Western China. ISRCTN Registry (http://www.isrctn.com/) [accessed 15 February 2007] 2007.

References to studies excluded from this review

Baumslag 1970 {published data only}
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Biswas 1984 {published data only}
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Blot 1981 {published data only}
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Chanarin 1968 {published data only}
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Chelchowska 2004 {published data only}
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Christian 2003 {published data only}
    1. Christian P, Khatry SK, Katz J, Pradhan EK, LeClerq SC, Shrestha SR, et al. Effects of alternative maternal micronutrient supplements on low birth weight in rural Nepal: double blind randomised community trial. BMJ 2003;326(7389):571. - PMC - PubMed
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Colman 1974 {published data only}
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Correia 1982 {published data only}
    1. Correia JM, Silva Cruz A, Silva Meirinho M. The importance of the contribution of folic acid in gestation [Importancia del aporte de acido folico en las gestacion]. Progresos de Obstetricia y Ginecologia 1982;25(6):381‐6.
Coutsoudis 1999 {published data only}
    1. Coutsoudis A, Pillay K, Spooner E, Kuhn L, Coovadia HM. Randomized trial testing the effect of vitamin A supplementation on pregnancy outcomes and early mother‐to‐child HIV‐1 transmission in Durban, South Africa. South African vitamin A study group. AIDS 1999;13(12):1517‐24. - PubMed
Dawson 1962 {published data only}
    1. Dawson DW, More JR, Aird DC. Prevention of megalo‐blastic anaemia in pregnancy by folic acid. Lancet 1962;2(7264):1015‐8. - PubMed
Edelstein 1968 {published data only}
    1. Edelstein T, Stevens K, Baumslag N, Metz J. Folic acid and vitamin B12 supplementation during pregnancy in a population subsisting on a suboptimal diet. Journal of Obstetrics and Gynaecology of the British Commonwealth 1968;75(2):133‐7. - PubMed
Ferguson 1955 {published data only}
    1. Ferguson JH. Methionine‐vitamin B therapy. Obstetrics & Gynecology 1955;6(2):221‐7. - PubMed
Feyi‐Waboso 2005 {published data only}
    1. Feyi‐Waboso PA, Chris A, Nwaogu GC, Archibong EI, Ejikem EC. The role of parenteral multivitamin preparation (Eldervit‐12) in the prevention of anaemia in pregnancy. Tropical Journal of Obstetrics and Gynaecology 2005;22(2):159‐63.
Fletcher 1971 {published data only}
    1. Fletcher J, Gurr A, Fellingham FR, Prankerd TAJ, Brant HA, Menzies DN. The value of folic acid supplements in pregnancy. Journal of Obstetrics and Gynaecology of the British Commonwealth 1971;78:781‐5. - PubMed
Giles 1971 {published data only}
    1. Giles PFH, Harcourt AG, Whiteside MG. The effect of prescribing folic acid during pregnancy on birth weight and duration of pregnancy, a double blind trial. Medical Journal of Australia 1971;5:17‐21. - PubMed
Hampel 1974 {published data only}
    1. Hampel KP, Roetz R. Influence of a long term substitution with a folate‐iron preparation on serum folate, serum iron and haematological data during pregnancy: result of a prospective study. Geburtshilfe und Frauenheilkd 1974;34:409‐17. - PubMed
Hankin 1966 {published data only}
    1. Hankin ME, Cellier KM. Studies of nutrition in pregnancy V: ascorbic acid levels of blood and milk in pregnancy and lactation. Australian and New Zealand Journal of Obstetrics and Gynaecology 1966;6:153‐60. - PubMed
Hekmatdoost 2011 {published data only}
    1. Hekmatdoost A. Comparison of the effect of folic acid and 5‐methyltetrahydrofolate (5MTHF) on serum folate and homocysteine levels, and abortion rates in women suffering from recurrent abortion. IRCT Iranian Registry of Clinical Trials (www.irct.ir) (accessed 8 July 2011) 2011.
    1. Hekmatdoost A, Vahid F, Yari Z, Sadeghi M, Eini‐Zinab H, Lakpour Niknam, et al. Methyltetrahydrofolate vs folic acid supplementation in idiopathic recurrent miscarriage with respect to methylenetetrahydrofolate reductase C677T and A1298C polymorphisms: a randomized controlled trial. PLoS ONE 2015;10(12):e0143569. - PMC - PubMed
Hibbard 1969 {published data only}
    1. Hibbard BM, Hibbard ED. The prophylaxis of folate deficiency in pregnancy. Acta Obstetricia et Gynecologica Scandinavica 1969;48:339‐48. - PubMed
    1. Hibbard BM, Hibbard ED. The treatment of folate deficiency in pregnancy. Acta Obstetricia et Gynecologica Scandinavica 1969;48:349‐56. - PubMed
Hunt 1984 {published data only}
    1. Hunt IF, Murphy NJ, Cleaver AE, Faraji B, Swendseid ME, Coulson AH, et al. Zinc supplementation during pregnancy: effects on selected blood constituents and on progress and outcome of pregnancy in low‐income women of Mexican descent. American Journal of Clinical Nutrition 1984;40:508‐21. - PubMed
Huybregts 2009 {published data only}
    1. Huybregts L, Roberfroid D, Lanou H, Kolsteren P, Camp J. Prenatal lipid‐based nutrient supplements increase cord leptin concentration in pregnant women from rural Burkina Faso. Annals of Nutrition & Metabolism 2013;63(Suppl 1):799, Abstract no: PO1134. - PubMed
    1. Huybregts L, Roberfroid D, Lanou H, Meda N, Taes Y, Valea I, et al. Prenatal lipid‐based nutrient supplements increase cord leptin concentration in pregnant women from rural Burkina Faso. Journal of Nutrition 2013;143(5):576‐83. - PubMed
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Kaestel 2005 {published data only}
    1. Andersen GS, Friis H, Michaelsen KF, Rodrigues A, Benn CS, Aaby P, et al. Effects of maternal micronutrient supplementation on fetal loss and under‐2‐years child mortality: long‐term follow‐up of a randomised controlled trial from Guinea‐Bissau. African Journal of Reproductive Health 2010;14(2):17‐26. - PubMed
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Laurence 1981 {published data only}
    1. Laurence KM. Prevention of neural tube defects by improvement in maternal diet and preconceptional folic acid supplementation. Progress in Clincial and Biological Research 1985;163:383‐8. - PubMed
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Lin 2010 {published data only}
    1. Lin JH, Yang YK, Liu H, Lin QD, Zhang WY. Effect of antioxidants on amelioration of high‐risk factors inducing hypertensive disorders in pregnancy. Chinese Medical Journal 2010;123(18):2548‐54. - PubMed
Lira 1989 {published data only}
    1. Lira P, Barrena N, Foradori A, Gormaz G, Grebe G. Folate deficiency in pregnancy: effect of supplemental folate [Deficiencia de folatos en el embarazo: Efecto de una suplementacion con acido folico]. Sangre 1989;34(1):24‐7. - PubMed
Lumeng 1976 {published data only}
    1. Lumeng L, Cleary RE, Wagner R, Pao‐Lo Y, Ting‐Kai L. Adequacy of vitamin B6 supplementation during pregnancy: a prospective study. American Journal of Clinical Nutrition 1976;29:1379‐83. - PubMed
Marya 1981 {published data only}
    1. Marya RK, Rathee S, Lata V, Mudgil S. Effects of vitamin D supplementation in pregnancy. Gynecologic and Obstetric Investigation 1981;12:155‐61. - PubMed
Meirinho 1987 {published data only}
    1. Meirinho M, Correia JM, Silva Cruz A. Administration of folic acid during pregnancy and trophoblastic disease [Administracion de acido folico en la gestacion y actividad trofoblastica]. Progresos de Obstetricia y Ginecologia 1987;30(2):87‐91.
Metz 1965 {published data only}
    1. Metz J, Festenstein H, Welch P. Effect of folic acid and vitamin B12 supplementation on tests of folate and vitamin B12 nutrition in pregnancy. American Journal of Clinical Nutrition 1965;16:472‐9. - PubMed
Mock 2002 {published data only}
    1. Mock DM, Quirk JG, Mock NI. Marginal biotin deficiency during normal pregnancy. American Journal of Clinical Nutrition 2002;75:295‐9. - PMC - PubMed
Moldenhauer 2002 {published data only}
    1. Moldenhauer J, Guo S, Liang R, Prada J. Dietary intake levels of the antioxidants vitamin C and vitamin E are adequately achieved with standard prenatal vitamin supplementation in high risk pregnancy groups [abstract]. American Journal of Obstetrics and Gynecology 2002;187(6 Pt 2):S99.
Owen 1966 {published data only}
    1. Owen GM, Nelsen CE, Baker GL, Connor WE, Jacobs JP. Use of vitamin K1 in pregnancy: effect of serum bilirubin and plasma prothrombin in the newborn. American Journal of Obstetrics and Gynecology 1967;99(3):368‐73.
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Potdar 2014 {published data only}
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