A Systematic Review and Meta-Analysis on the Effects of Probiotic Species on Iron Absorption and Iron Status
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy and Study Selection
2.2. Eligibility Criteria
2.3. Data Extraction and Management
2.4. Assessment Methodological Quality of Included Studies
2.5. Data Synthesis
2.6. Meta-Analysis
3. Results
3.1. Description of Selected Articles
3.2. Bias
3.3. Iron Absorption
3.4. Iron Status Markers and Hemoglobin
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Study/Year | Subjects | Baseline Iron Status | Design/ Blinding | Study Groups or Product | Iron Compound | Intervention Delivery Method, Frequency and Duration | Effect on Iron Status or Iron Absorption | Included in Meta-Analysis |
---|---|---|---|---|---|---|---|---|
RCTs and Nonrandomized Clinical Trials | ||||||||
Agustina et al., 2013 [21] | Indonesia N = 494 Children Age: 1–6 Healthy Non-breastfed | IDA n (%) Group 1: 12 (10) Group 2: 17 (14) Group 3: 13 (11) Group 4: 14 (11) | RCT double-blinded | Group 1: Placebo–Low calcium, ~50 mg/d Group 2: Placebo–Regular calcium, ~440 mg/d Group 3: L. casei 431 1: 5 × 108 CFU/d plus regular calcium Group 4: L. reuteri 17,938 5 × 108 CFU/d plus regular calcium | Not reported | 180 mL low-lactose milk and coated straws Twice daily across 6 months | ↔ Hb ↔ Hct ↔ serum ferritin↔ sTfR | No |
Asemi et al., 2013 [11] | Iran N = 70 Pregnant, third trimester Age: 18–30 | Iron (mg/dL) Group 1: 124 ± 88.3 Group 2: 118 ± 61.8 | RCT single-blinded | Group 1: Placebo Group 2: L. acidophilus 1 × 107 CFU, B. lactis 1 × 107 CFU | Not reported | 200 g yogurt Daily across 9 weeks | ↔ serum iron | No |
Asemi et al., 2015 [25] | Iran N = 58 Diabetic patients, not pregnant Age: 52.1 ± 6.9 (Group 1) 49.6 ± 9.9 (Group 2) Female % not reported | Iron (mg/dL) Group 1: 66.1 ± 33 Group 2: 69.5 ± 62.9 | RCT double-blinded | Group 1: Placebo Group 2: L. acidophilus 2 × 109 CFU, L. casei 7 × 109 CFU, L. bulgaricus 2 × 108 CFU, B. breve 2 × 108 CFU, B. longum 7 × 109 CFU, S. thermophiles 1.5 × 109 CFU | Not reported | Capsule Daily across 8 weeks | ↔ serum iron | No |
Endo et al., 2011 [22] | Japan N = 25 Female 28% Age: 70.3 ± 6.2 (Group 1) 73.9 ± 8.5 (Group 2) Unexplained IDA on chronic low-dose aspirin | Hb (g/dl) Group 1: 10.9 ± 1.7 Group 2: 10.2 ± 2 | RCT single-blinded | Group 1: No placebo Group 2: L. casei 45 × 108–63 × 10 CFU | Not reported | Powder Daily for 3 months | ↔ Hb (between groups) ↑ Hb (within L. casei group) | No |
Korcok et al., 2018 [23] | Serbia N = 20 Female 100% Healthy | Not reported | Two group comparison | Group 1: Placebo Group 2: L. plantarum 299v 1.1 × 109 CFU | Sucrosomal iron 10 mg | Capsule plus supplemental iron and 15 mg vitamin C 7 consecutive mornings Empty stomach | ↑ serum iron a↔ serum ferritin ↔ TIBC ↔ Hb | No |
Rosen et al., 2019 [29] | United States N = 52 Children with mild iron deficiency (ferritin < 50 ng/mL), and insomnia or restless sleep, 58% had psychiatric and/or mental health diagnosis Age: 5–18 | Not reported | RCT Double-blinded | Group 1: placebo Group 2: L. plantarum 299v 1.7 × 1010 CFU | Ferrous sulphate 325 mg or ferrous sulphate 15 mg elemental iron/mL (if children < 20 kg, dose of 3 mg/kg/d up to maximum dose 65 mg; in children > 20 kg range 0.4–3 mg/kg/d) | Capsule plus supplemental iron and vitamin C (125 mg < 5 years of age and 250 mg > 5 years of age) 6–8 weeks No milk or food within 2 h of medication | ↔ serum ferritin | No |
Silva et al., 2008 [24] | Brazil N = 109 Children Age: 20–62 months | Iron (µg/dL) Group 1: 48.9 ± 9.8 Group 2: 49 ± 10.5 Hb (g/dL) Group 1: 12.2 ± 0.7 G 2: 12.1 ± 0.7 Ferritin (ng/mL) Group 1: 41.2 ± 21.4 Group 2: 38.5 ± 19 | Two group comparison | Group 1: Placebo Group 2: L. acidophilus 108 CFU | Not reported | 80 mL whole milk beverage with 3 mg iron 1.2 g culture of L. acidophilus Daily between lunch and afternoon snack Monday to Friday during 101 class days | Between groups ↔ Hb Within L. acidophilus group ↓ Hb ↓ Hct ↓ serum iron ↓ serum ferritin Within Placebo group ↓ Hb ↓ Hct ↔ serum iron ↑ serum ferritin | No |
Cross-over Studies | ||||||||
Bering et al., 2006 [12] | Denmark N = 24 Female 100% Age: 25 ± 4 low iron stores not anemic, not pregnant, not lactating | Hb (g/L) Range: 111–137 Ferritin (µg/L) Range 12–40 | Cross-over double-blinded | Product A: L. plantarum 299v 1.1 × 109 CFU, fermented gruel Product B: pasteurized Product A Product C: non-fermented gruel (pH adjusted with lactic acid) Product D: control meal non-fermented gruel with added organic acids (lactic acid and acetic acid) | Not reported | 100 g oat gruel Product A, B & D: non-heme Fe 2.8 mg Product C: non-heme Fe 2.5 mg Twice on four consecutive mornings 12 h of fasting | ↑ non-heme iron absorption | Yes |
Bering et al., 2007 [19] | Denmark N = 18 Female 100% Age: 22 ± 3 low iron stores not anemic, not pregnant, not lactating | Hb (g/L) Range: 116–135 Ferritin (µg/L) Range 13–29 | Cross-over double-blinded | Product A: heat-inactivated lactic acid gruel Product B: viable lypholized L. Plantarum 299v 1.1 × 109 CFU, heat-inactivated lactic acid gruel | Not reported | 100 g fermented, pasteurized oat gruel plus 140 g whole-wheat roll Product A & B: non-heme Fe 1.9 mg Twice on two consecutive mornings12 h of fasting | ↔ non-heme iron absorption | Yes |
Hoppe et al., 2015 [18] | Sweden N = 10 (Study 1) N = 11 (Study 2) Female 100% Healthy Age: 24.3, range 20–40 (Total sample) | Iron (µmol/L) Study 1: 15 ± 6 Study 2: 18 ± 7 Hb (g/L) Study 1: 138 ± 8 Study 2: 135 ± 9 Ferritin (µg/L) Study 1: 33 ± 13 Study 2: 33 ± 14 | Cross-over single-blinded | Product A: Placebo Product B: L. plantarum 299v 1.3 × 109 CFU (Study 1) L. plantarum 299v 1.7 × 1010 CFU (Study 2) | Ferrous lactate dehydrate 4.2 mg | 200 mL fruit drink with fermented oat base plus iron (2.1 mg/100 mL) Product A: non-heme Fe 5.2 mg (Study 1) non-heme Fe 5.4 mg (Study 2) Product B: non-heme Fe 4.6 mg (Study 1) non-heme Fe 5.2 mg (Study 2) 4 consecutive days Empty stomach | ↑ non-heme iron absorption (Study 1) ↔ non-heme iron absorption (Study 2) | Yes |
Hoppe et al., 2017 [13] | Sweden N = 14 (Study 1) N = 28 (Study 2) Female 100% Age: 26.2 ± 4.6 (Study 1) 25.6 ± 6.8 (Study 2) Healthy | Iron (µmol/L) Study 1: 15 ± 5 Study 2: 16 ± 7 Hb (g/L) Study 1: 135 ± 6 Study 2: 134 ± 10 Ferritin (µg/L) Study 1: 30 ± 21 Study 2: 27 ± 14 | Cross-over single-blinded | Product A: Placebo Product B: L. plantarum 299v 1010 CFU (Study 1 & 2) | Not reported | Capsule plus two wheat breakfast buns made with fermented dough Product A & B: non-heme Fe 4.2 mg 4 consecutive days Empty stomach | ↑ non-heme iron absorption (Study 1) ↑ non-heme iron absorption (Study 2) | Yes |
Scheers et al., 2016 [20] | Sweden N = 8 low-phytate (Study 1) N = 9 high-phytate (Study 2) Female 35% Age: 21–54 Healthy | Not reported | Cross-over | Product A: Fresh vegetables Product B: L. plantarum 299v 2.4 × 109 CFU fermented vegetables | Not reported | 140 g bread rolls (low phytate had wheat flour; or high phytate had wheat bran and wheat flour) plus 100 g fermented or fresh vegetables Low phytate non-heme Fe 4.4 mg High phytate non-heme Fe 4.0 mg Alternate mornings on 4 consecutive days Overnight fast | ↑ non-heme iron absorption | Yes |
Number of Studies | Model | Effect: Pooled SMD | 95% CI | p-Value | Q | p-Value | Tau Squared |
---|---|---|---|---|---|---|---|
8 | random | 0.55 | 0.22, 0.88 | 0.001 | 10.62 | 0.156 | 0.0747 |
6 a | random | 0.72 | 0.29, 1.15 | 0.001 | 8.01 | 0.156 | 0.1058 |
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Vonderheid, S.C.; Tussing-Humphreys, L.; Park, C.; Pauls, H.; OjiNjideka Hemphill, N.; LaBomascus, B.; McLeod, A.; Koenig, M.D. A Systematic Review and Meta-Analysis on the Effects of Probiotic Species on Iron Absorption and Iron Status. Nutrients 2019, 11, 2938. https://doi.org/10.3390/nu11122938
Vonderheid SC, Tussing-Humphreys L, Park C, Pauls H, OjiNjideka Hemphill N, LaBomascus B, McLeod A, Koenig MD. A Systematic Review and Meta-Analysis on the Effects of Probiotic Species on Iron Absorption and Iron Status. Nutrients. 2019; 11(12):2938. https://doi.org/10.3390/nu11122938
Chicago/Turabian StyleVonderheid, Susan C., Lisa Tussing-Humphreys, Chang Park, Heather Pauls, Nefertiti OjiNjideka Hemphill, Bazil LaBomascus, Andrew McLeod, and Mary Dawn Koenig. 2019. "A Systematic Review and Meta-Analysis on the Effects of Probiotic Species on Iron Absorption and Iron Status" Nutrients 11, no. 12: 2938. https://doi.org/10.3390/nu11122938
APA StyleVonderheid, S. C., Tussing-Humphreys, L., Park, C., Pauls, H., OjiNjideka Hemphill, N., LaBomascus, B., McLeod, A., & Koenig, M. D. (2019). A Systematic Review and Meta-Analysis on the Effects of Probiotic Species on Iron Absorption and Iron Status. Nutrients, 11(12), 2938. https://doi.org/10.3390/nu11122938