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Meta-Analysis
. 2019 Dec 18;12(12):CD011400.
doi: 10.1002/14651858.CD011400.pub2.

Food fortification with multiple micronutrients: impact on health outcomes in general population

Jai K Das  1 , Rehana A Salam  1   2 , Salman Bin Mahmood  3 , Anoosh Moin  1 , Rohail Kumar  1 , Kashif Mukhtar  1 , Zohra S Lassi  1   4 , Zulfiqar A Bhutta  5
Affiliations
Meta-Analysis

Food fortification with multiple micronutrients: impact on health outcomes in general population

Jai K Das et al. Cochrane Database Syst Rev. .

Abstract

Background: Vitamins and minerals are essential for growth and maintenance of a healthy body, and have a role in the functioning of almost every organ. Multiple interventions have been designed to improve micronutrient deficiency, and food fortification is one of them.

Objectives: To assess the impact of food fortification with multiple micronutrients on health outcomes in the general population, including men, women and children.

Search methods: We searched electronic databases up to 29 August 2018, including the Cochrane Central Register of Controlled Trial (CENTRAL), the Cochrane Effective Practice and Organisation of Care (EPOC) Group Specialised Register and Cochrane Public Health Specialised Register; MEDLINE; Embase, and 20 other databases, including clinical trial registries. There were no date or language restrictions. We checked reference lists of included studies and relevant systematic reviews for additional papers to be considered for inclusion.

Selection criteria: We included randomised controlled trials (RCTs), cluster-RCTs, quasi-randomised trials, controlled before-after (CBA) studies and interrupted time series (ITS) studies that assessed the impact of food fortification with multiple micronutrients (MMNs). Primary outcomes included anaemia, micronutrient deficiencies, anthropometric measures, morbidity, all-cause mortality and cause-specific mortality. Secondary outcomes included potential adverse outcomes, serum concentration of specific micronutrients, serum haemoglobin levels and neurodevelopmental and cognitive outcomes. We included food fortification studies from both high-income and low- and middle-income countries (LMICs).

Data collection and analysis: Two review authors independently screened, extracted and quality-appraised the data from eligible studies. We carried out statistical analysis using Review Manager 5 software. We used random-effects meta-analysis for combining data, as the characteristics of study participants and interventions differed significantly. We set out the main findings of the review in 'Summary of findings' tables, using the GRADE approach.

Main results: We identified 127 studies as relevant through title/abstract screening, and included 43 studies (48 papers) with 19,585 participants (17,878 children) in the review. All the included studies except three compared MMN fortification with placebo/no intervention. Two studies compared MMN fortification versus iodised salt and one study compared MMN fortification versus calcium fortification alone. Thirty-six studies targeted children; 20 studies were conducted in LMICs. Food vehicles used included staple foods, such as rice and flour; dairy products, including milk and yogurt; non-dairy beverages; biscuits; spreads; and salt. Fourteen of the studies were fully commercially funded, 13 had partial-commercial funding, 14 had non-commercial funding and two studies did not specify the source of funding. We rated all the evidence as of low to very low quality due to study limitations, imprecision, high heterogeneity and small sample size. When compared with placebo/no intervention, MMN fortification may reduce anaemia by 32% (risk ratio (RR) 0.68, 95% confidence interval (CI) 0.56 to 0.84; 11 studies, 3746 participants; low-quality evidence), iron deficiency anaemia by 72% (RR 0.28, 95% CI 0.19 to 0.39; 6 studies, 2189 participants; low-quality evidence), iron deficiency by 56% (RR 0.44, 95% CI 0.32 to 0.60; 11 studies, 3289 participants; low-quality evidence); vitamin A deficiency by 58% (RR 0.42, 95% CI 0.28 to 0.62; 6 studies, 1482 participants; low-quality evidence), vitamin B2 deficiency by 64% (RR 0.36, 95% CI 0.19 to 0.68; 1 study, 296 participants; low-quality evidence), vitamin B6 deficiency by 91% (RR 0.09, 95% CI 0.02 to 0.38; 2 studies, 301 participants; low-quality evidence), vitamin B12 deficiency by 58% (RR 0.42, 95% CI 0.25 to 0.71; 3 studies, 728 participants; low-quality evidence), weight-for-age z-scores (WAZ) (mean difference (MD) 0.1, 95% CI 0.02 to 0.17; 8 studies, 2889 participants; low-quality evidence) and weight-for-height/length z-score (WHZ/WLZ) (MD 0.1, 95% CI 0.02 to 0.18; 6 studies, 1758 participants; low-quality evidence). We are uncertain about the effect of MMN fortification on zinc deficiency (RR 0.84, 95% CI 0.65 to 1.08; 5 studies, 1490 participants; low-quality evidence) and height/length-for-age z-score (HAZ/LAZ) (MD 0.09, 95% CI 0.01 to 0.18; 8 studies, 2889 participants; low-quality evidence). Most of the studies in this comparison were conducted in children. Subgroup analyses of funding sources (commercial versus non-commercial) and duration of intervention did not demonstrate any difference in effects, although this was a relatively small number of studies and the possible association between commercial funding and increased effect estimates has been demonstrated in the wider health literature. We could not conduct subgroup analysis by food vehicle and funding; since there were too few studies in each subgroup to draw any meaningful conclusions. When we compared MMNs versus iodised salt, we are uncertain about the effect of MMN fortification on anaemia (R 0.86, 95% CI 0.37 to 2.01; 1 study, 88 participants; very low-quality evidence), iron deficiency anaemia (RR 0.40, 95% CI 0.09 to 1.83; 2 studies, 245 participants; very low-quality evidence), iron deficiency (RR 0.98, 95% CI 0.82 to 1.17; 1 study, 88 participants; very low-quality evidence) and vitamin A deficiency (RR 0.19, 95% CI 0.07 to 0.55; 2 studies, 363 participants; very low-quality evidence). Both of the studies were conducted in children. Only one study conducted in children compared MMN fortification versus calcium fortification. None of the primary outcomes were reported in the study. None of the included studies reported on morbidity, adverse events, all-cause or cause-specific mortality.

Authors' conclusions: The evidence from this review suggests that MMN fortification when compared to placebo/no intervention may reduce anaemia, iron deficiency anaemia and micronutrient deficiencies (iron, vitamin A, vitamin B2 and vitamin B6). We are uncertain of the effect of MMN fortification on anthropometric measures (HAZ/LAZ, WAZ and WHZ/WLZ). There are no data to suggest possible adverse effects of MMN fortification, and we could not draw reliable conclusions from various subgroup analyses due to a limited number of studies in each subgroup. We remain cautious about the level of commercial funding in this field, and the possibility that this may be associated with higher effect estimates, although subgroup analysis in this review did not demonstrate any impact of commercial funding. These findings are subject to study limitations, imprecision, high heterogeneity and small sample sizes, and we rated most of the evidence low to very low quality. and hence no concrete conclusions could be drawn from the findings of this review.

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Conflict of interest statement

JKD: no competing interests.

RAS: no competing interests.

SBM: no competing interests.

AM: no competing interests.

RK: no competing interests.

KM: no competing interests.

ZL: Participated in a Nestlé Nutrition Institute workshop on Health and Nutrition in Adolescents and Young Women: preparing for the next generation for the related publication Nestlé Nutrition Institute Series Volume 80 (2015)

ZAB: Participated in a Nestlé Nutrition Institute workshop on Health and Nutrition in Adolescents and Young Women: preparing for the next generation and co‐edited the related publication Nestlé Nutrition Institute Series Volume 80 (2015). ZAB declares previous travel support from the Nestlé Nutrition Institute for attendance at a meeting on fortification strategies at the University of Winterthur, Winterthur, Switzerland, in October 2011. ZAB received an institutional grant from GAIN on fortification program evidence review in 2014. The paper is currently in press.

Figures

1
1
Study flow diagram showing results of the literature search.
2
2
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
3
3
Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
4
4
Forest plot of comparison: 1 MMN vs Placebo/No intervention, outcome: 1.1 Anaemia.
5
5
Forest plot of comparison: 1 MMN vs Placebo, outcome: 1.2 Iron deficiency anaemia.
6
6
Forest plot of comparison: 1 MMN vs placebo/no intervention, outcome: 1.3 Micronutrient deficiencies: Iron.
7
7
Forest plot of comparison: 1 MMN vs placebo/no intervention, outcome: 1.4 Micronutrient deficiencies: Vitamin A.
8
8
Forest plot of comparison: 1 MMN vs placebo/no intervention, outcome: 1.6 Micronutrient deficiencies: Zinc.
9
9
Funnel plot of comparison: 1 MMN vs Placebo/No intervention, outcome: 1.1 Anaemia.
10
10
Funnel plot of comparison: 1 MMN vs placebo/no intervention, outcome: 1.3 Micronutrient deficiencies: Iron.
11
11
Funnel plot of comparison: 1 MMN vs placebo/no intervention, outcome: 1.10 Biochemical: Serum haemoglobin (g/L).
12
12
Funnel plot of comparison: 1 MMN vs Placebo/No intervention, outcome: 1.13 Biochemical: Serum Vitamin A (umol/L).
13
13
Funnel plot of comparison: 1 MMN vs Placebo/No intervention, outcome: 1.14 Biochemical: Serum Zinc (ug/dL).
1.1
1.1. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 1 Anaemia.
1.2
1.2. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 2 Iron deficiency anaemia.
1.3
1.3. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 3 Micronutrient deficiencies: Iron.
1.4
1.4. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 4 Micronutrient deficiencies: Vitamin A.
1.5
1.5. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 5 Micronutrient deficiencies: B Vitamin.
1.6
1.6. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 6 Micronutrient deficiencies: Zinc.
1.7
1.7. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 7 Anthropometric: WAZ.
1.8
1.8. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 8 Anthropometric: WHZ/WLZ.
1.9
1.9. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 9 Anthropometric: HAZ/LAZ.
1.10
1.10. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 10 Biochemical: Serum haemoglobin (g/L).
1.11
1.11. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 11 Biochemical: Serum ferritin (μg/mL).
1.12
1.12. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 12 Biochemical: B Vitamin.
1.13
1.13. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 13 Biochemical: Serum vitamin A (μmol/L).
1.14
1.14. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 14 Biochemical: Serum zinc (μg/dL).
1.15
1.15. Analysis
Comparison 1 MMN vs placebo/no intervention, Outcome 15 Neuro‐cognitive outcomes.
2.1
2.1. Analysis
Comparison 2 MMN vs placebo/no intervention (Subgroup analysis by duration of intervention), Outcome 1 Anthropometric: WAZ.
2.2
2.2. Analysis
Comparison 2 MMN vs placebo/no intervention (Subgroup analysis by duration of intervention), Outcome 2 Anthropometric: HAZ/LAZ.
3.1
3.1. Analysis
Comparison 3 MMN vs placebo/no intervention (Subgroup analysis by funding), Outcome 1 Anaemia.
3.2
3.2. Analysis
Comparison 3 MMN vs placebo/no intervention (Subgroup analysis by funding), Outcome 2 Micronutrient Deficiencies: Iron.
4.1
4.1. Analysis
Comparison 4 MMN vs iodised salt, Outcome 1 Anaemia.
4.2
4.2. Analysis
Comparison 4 MMN vs iodised salt, Outcome 2 Iron deficiency anaemia.
4.3
4.3. Analysis
Comparison 4 MMN vs iodised salt, Outcome 3 Micronutrient deficiencies: Iron.
4.4
4.4. Analysis
Comparison 4 MMN vs iodised salt, Outcome 4 Micronutrient deficiencies: Vitamin A.
4.5
4.5. Analysis
Comparison 4 MMN vs iodised salt, Outcome 5 Biochemical: Serum haemoglobin (g/L).
4.6
4.6. Analysis
Comparison 4 MMN vs iodised salt, Outcome 6 Biochemical: Serum ferritin (ug/L).
4.7
4.7. Analysis
Comparison 4 MMN vs iodised salt, Outcome 7 Biochemical: B Vitamin.
4.8
4.8. Analysis
Comparison 4 MMN vs iodised salt, Outcome 8 Biochemical: Serum vitamin A (umol/L).
4.9
4.9. Analysis
Comparison 4 MMN vs iodised salt, Outcome 9 Biochemical: Serum zinc.
5.1
5.1. Analysis
Comparison 5 MMN vs calcium fortification alone, Outcome 1 Biochemical: Serum vitamin E.
5.2
5.2. Analysis
Comparison 5 MMN vs calcium fortification alone, Outcome 2 Biochemical: Serum vitamin D.
5.3
5.3. Analysis
Comparison 5 MMN vs calcium fortification alone, Outcome 3 Biochemical: Serum calcium.
5.4
5.4. Analysis
Comparison 5 MMN vs calcium fortification alone, Outcome 4 Biochemical: Serum vitamin A (umol/L).
See this image and copyright information in PMC

Update of

  • doi: 10.1002/14651858.CD011400

References

References to studies included in this review

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Economos 2014 {published data only}
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Hieu 2012 {published data only}
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Hyder 2007 {published data only}
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Järvenpaa 2007 {published data only}
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Jinabhai 2001 {published data only}
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Mardones 2007 {published data only}
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Nesamvuni 2005 {published data only}
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Nga 2009 {published data only}
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Oelofse 2003 {published data only}
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Perignon 2016 {published data only}
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Pinkaew 2013 {published data only}
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Powers 2016 {published data only}
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Rahman 2015 {published data only}
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Tapola 2004 {published data only}
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Tatala 2002 {published data only}
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Van Stuijvenberg 1999 {published data only}
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Villalpando 2006 {published data only}
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Vinodkumar 2009 {published data only}
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Zimmerman 2004 {published data only}
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References to studies excluded from this review

Aburto 2010 {published data only}
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Agte 2006 {published data only}
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Anand 2007 {published data only}
    1. Anand K, Lakshmy R, Janakarajan VN, Ritvik A, Misra P, Pandey RM, et al. Effect of consumption of micronutrient fortified candies on the iron and vitamin A status of children aged 3‐6 years in rural Haryana. Indian Pediatrics 2007;44(11):823. - PubMed
Angeles Agdeppa 2011 {published data only}
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Angeles‐Agdeppa 2017 {published data only}
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Gathwala 2007 {published data only}
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Glosz 2018 {published data only}
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Grieger 2009 {published data only}
    1. Grieger JA, Nowson CA. Use of calcium, folate, and vitamin D₃‐fortified milk for 6 months improves nutritional status but not bone mass or turnover, in a group of Australian aged care residents. Journal of Nutrition for the Elderly 2009;28(3):236‐54. - PubMed
Hoffman 2007 {published data only}
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    1. Hund L, Northrop‐Clewes CA, Nazario R, Suleymanova D, Mirzoyan L, Irisova M, et al. A novel approach to evaluating the iron and folate status of women of reproductive age in Uzbekistan after 3 years of flour fortification with micronutrients. PLoS One 2013;8(11):e79726. [DOI: 10.1371/journal.pone.0079726] - DOI - PMC - PubMed
Huybregts 2009 {published data only}
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Iannotti 2016 {published data only}
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Jaatinen 2014 {published data only}
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Janmohamed 2016 {published data only}
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    1. Kanellakis S, Moschonis G, Tenta R, Schaafsma A, Heuvel EG, Papaioannou N, et al. Changes in parameters of bone metabolism in postmenopausal women following a 12‐month intervention period using dairy products enriched with calcium, vitamin D, and phylloquinone (vitamin K(1)) or menaquinone‐7 (vitamin K (2)): the Postmenopausal Health Study II. Calcified Tissue International 2012;90(4):251‐62. - PubMed
Krebs 2012 {published data only}
    1. Krebs NF, Mazariegos M, Chomba E, Sami N, Pasha O, Tshefu A, et al. Randomized controlled trial of meat compared with multi‐micronutrient‐fortified cereal in infants and toddlers with high stunting rates in diverse settings. American Journal of Clinical Nutrition 2012;96(4):840‐7. - PMC - PubMed
Kruger 2010 {published data only}
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Kumar 2007 {published data only}
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Kuriyan 2016 {published data only}
    1. Kuriyan R, Thankachan P, Selvam S, Pauline M, Srinivasan K, Kamath‐Jha S, et al. The effects of regular consumption of a multiple micronutrient fortified milk beverage on the micronutrient status of school children and on their mental and physical performance. Clinical Nutrition 2016;35(1):190‐8. - PubMed
Kuusipalo 2006 {published data only}
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Lartey 1999 {published data only}
    1. Lartey A, Manu A, Brown KH, Peerson JM, Dewey KG. A randomized, community‐based trial of the effects of improved, centrally processed complementary foods on growth and micronutrient status of Ghanaian infants from 6 to 12 mo of age. American Journal of Clinical Nutrition 1999;70(3):391‐404. - PubMed
Layrisse 1996 {published data only}
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Lönnerdal 1994 {published data only}
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Loui 2004 {published data only}
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Lutter 2007 {published data only}
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Malpeli 2013 {published data only}
    1. Malpeli A, Ferrari MG, Varea A, Falivene M, Etchegoyen G, Vojkovic M, et al. Short‐term evaluation of the impact of a fortified food aid program on the micronutrient nutritional status of Argentinian pregnant women. Biological Trace Element Research 2013;155(2):176‐83. - PubMed
Manders 2009 {published data only}
    1. Manders M, Groot LC, Hoefnagels WH, Dhonukshe‐Rutten RA, Wouters‐Wesseling W, Mulders AJ, et al. The effect of a nutrient dense drink on mental and physical function in institutionalized elderly people. Journal of Nutrition, Health & Aging 2009;13(9):760‐7. - PubMed
Manno 2011 {published data only}
    1. Manno D, Siame J, Larke N, Baisley K, Kasonka L, Filteau S. Effect of multiple micronutrient‐fortified food on mild morbidity and clinical symptoms in Zambian infants: results from a randomised controlled trial. European Journal of Clinical Nutrition 2011;65(10):1163. - PubMed
Matilsky 2009 {published data only}
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Mendoza 2004 {published data only}
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Mishaan 2004 {published data only}
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Mukhopadhyay 2007 {published data only}
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Muthayya 2009 {published data only}
    1. Muthayya S, Eilander A, Transler C, Thomas T, Knaap HC, Srinivasan K, et al. Effect of fortification with multiple micronutrients and n–3 fatty acids on growth and cognitive performance in Indian schoolchildren: the CHAMPION (Children’s Health and Mental Performance Influenced by Optimal Nutrition) Study. American Journal of Clinical Nutrition 2009;89(6):1766‐75. - PubMed
Osei 2010 {published data only}
    1. Osei AK, Rosenberg IH, Houser RF, Bulusu S, Mathews M, Hamer DH. Community‐level micronutrient fortification of school lunch meals improved vitamin A, folate, and iron status of schoolchildren in Himalayan villages of India. Journal of Nutrition 2010;140(6):1146‐54. - PubMed
Ouédraogo 2010 {published data only}
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Parker 2015 {published data only}
    1. Parker ME, Mosites E, Reider K, Ndayishimiye N, Waring M, Nyandimbane G, et al. A blinded, cluster‐randomized, placebo‐controlled school feeding trial in Burundi using rice fortified with iron, zinc, thiamine, and folic acid. Food and Nutrition Bulletin 2015;36(4):481‐92. - PubMed
Pettifor 1989 {published data only}
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Phu 2010 {published data only}
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Pullakhandam 2011 {published data only}
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Ramakrishnan 2004 {published data only}
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Ramírez‐Silva 2013 {published data only}
    1. Ramírez‐Silva I, Rivera JA, Leroy JL, Neufeld LM. The Oportunidades program's fortified food supplement, but not improvements in the home diet, increased the intake of key micronutrients in rural Mexican children aged 12‐59 months. Journal of Nutrition 2013;143(5):656. - PubMed
Rohner 2016 {published data only}
    1. Rohner F, Raso G, Aké‐Tano SO, Tschannen AB, Mascie‐Taylor CG, Northrop‐Clewes CA. The effects of an oil and wheat flour fortification program on pre‐school children and women of reproductive age living in Côte d'Ivoire, a malaria‐endemic area. Nutrients 2016;8(3):148. [DOI: 10.3390/nu8030148] - DOI - PMC - PubMed
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Seal 2008 {published data only}
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Semba 2011 {published data only}
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Shatrugna 2006 {published data only}
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Thomas 2012 {published data only}
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Varea 2012 {published data only}
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Varma 2007 {published data only}
    1. Varma JL, Das S, Sankar R, Mannar MG, Levinson FJ, Hamer DH. Community‐level micronutrient fortification of a food supplement in India: a controlled trial in preschool children aged 36‐66 mo. American Journal of Clinical Nutrition 2007;85(4):1127. - PubMed
Yeh 2013 {published data only}
    1. Yeh KY, Wang HM, Chang JW, Huang JS, Lai CH, Lan YJ, et al. Omega‐3 fatty acid‐, micronutrient‐, and probiotic‐enriched nutrition helps body weight stabilization in head and neck cancer cachexia. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 2013;116(1):41‐8. - PubMed
Zagré 2007 {published data only}
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