Iron Absorption from Iron-Biofortified Sweetpotato Is Higher Than Regular Sweetpotato in Malawian Women while Iron Absorption from Regular and Iron-Biofortified Potatoes Is High in Peruvian Women

Roelinda Jongstra, Martin N Mwangi, Gabriela Burgos, Christophe Zeder, Jan W Low, Glory Mzembe, Reyna Liria, Mary Penny, Maria I Andrade, Susan Fairweather-Tait, Thomas Zum Felde, Hugo Campos, Kamija S Phiri, Michael B Zimmermann, Rita Wegmüller, Roelinda Jongstra, Martin N Mwangi, Gabriela Burgos, Christophe Zeder, Jan W Low, Glory Mzembe, Reyna Liria, Mary Penny, Maria I Andrade, Susan Fairweather-Tait, Thomas Zum Felde, Hugo Campos, Kamija S Phiri, Michael B Zimmermann, Rita Wegmüller

Abstract

Background: Sweetpotato and potato are fast-maturing staple crops and widely consumed in low- and middle-income countries. Conventional breeding to biofortify these crops with iron could improve iron intakes. To our knowledge, iron absorption from sweetpotato and potato has not been assessed.

Objective: The aim was to assess iron absorption from regular and iron-biofortified orange-fleshed sweetpotato in Malawi and yellow-fleshed potato and iron-biofortified purple-fleshed potato in Peru.

Methods: We conducted 2 randomized, multiple-meal studies in generally healthy, iron-depleted women of reproductive age. Malawian women (n = 24) received 400 g regular or biofortified sweetpotato test meals and Peruvian women (n = 35) received 500 g regular or biofortified potato test meals. Women consumed the meals at breakfast for 2 wk and were then crossed over to the other variety. We labeled the test meals with 57Fe or 58Fe and measured cumulative erythrocyte incorporation of the labels 14 d after completion of each test-meal sequence to calculate iron absorption. Iron absorption was compared by paired-sample t tests.

Results: The regular and biofortified orange-fleshed sweetpotato test meals contained 0.55 and 0.97 mg Fe/100 g. Geometric mean (95% CI) fractional iron absorption (FIA) was 5.82% (3.79%, 8.95%) and 6.02% (4.51%, 8.05%), respectively (P = 0.81), resulting in 1.9-fold higher total iron absorption (TIA) from biofortified sweetpotato (P < 0.001). The regular and biofortified potato test meals contained 0.33 and 0.69 mg Fe/100 g. FIA was 28.4% (23.5%, 34.2%) from the regular yellow-fleshed and 13.3% (10.6%, 16.6%) from the biofortified purple-fleshed potato meals, respectively (P < 0.001), resulting in no significant difference in TIA (P = 0.88).

Conclusions: FIA from regular yellow-fleshed potato was remarkably high, at 28%. Iron absorbed from both potato test meals covered 33% of the daily absorbed iron requirement for women of reproductive age, while the biofortified orange-fleshed sweetpotato test meal covered 18% of this requirement. High polyphenol concentrations were likely the major inhibitors of iron absorption. These trials were registered at www.clinicaltrials.gov as NCT03840031 (Malawi) and NCT04216030 (Peru).

Keywords: biofortification; iron absorption; orange-fleshed sweetpotato; potato; stable isotopes.

© The Author(s) 2020. Published by Oxford University Press on behalf of the American Society for Nutrition.

Figures

FIGURE 1
FIGURE 1
Study overview diagrams for the sweetpotato study in Malawi and the potato study in Peru. CRP, C-reactive protein; Hb, hemoglobin; PF, plasma ferritin; SF, serum ferritin.
FIGURE 2
FIGURE 2
Study design for the sweetpotato study in Malawi (M) and the potato study in Peru (P). In both studies women were randomly assigned to either the regular OFSP (M), YFP (P), or iron-biofortified OFSP (M), PFP (P) test meals with iron isotopic administration (regular test meal, 57Fe, or iron-biofortified test meal, 58Fe) for 10 consecutive days, after which they crossed over to the other test meal sequence. OFSP, orange-fleshed sweetpotato; PFP, purple-fleshed potato; Sobo® (Southern Bottlers Ltd); YFP, yellow-fleshed potato.
FIGURE 3
FIGURE 3
Fractional iron absorption (%) (A, C) and total iron absorption (mg/d) (B, D) from regular and iron-biofortified OFSP test meals in Malawian women (A, B; n = 24) and from regular YFP and iron-biofortified PFP test meals in Peruvian women (C, D; n = 35). Isotopic administration in both studies: 57Fe for the regular test meal and 58Fe for the iron-biofortified test meal. The horizontal lines represent geometric means (95% CIs). OFSP, orange-fleshed sweetpotato; PFP, purple-fleshed potato; YFP, yellow-fleshed potato.

References

    1. Camaschella C. Iron deficiency. Blood. 2019;133:30–9.
    1. Camaschella C. Iron-deficiency anemia. N Engl J Med. 2015;372:1832–43.
    1. Dewey KG, Oaks BM. U-shaped curve for risk associated with maternal hemoglobin, iron status, or iron supplementation. Am J Clin Nutr. 2017;106:1694S–702S.
    1. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet North Am Ed. 2007;370:511–20.
    1. National Statistical Office–NSO/Malawi; Community Health Sciences Unit–CHSU/Malawi; Centers for Disease Control and Prevention; Emory University Malawi Micronutrient Survey 2015–16: key indicators report. Atlanta, GA: National Statistical Office and ICF; 2016.
    1. Instituto Nacional de Estadística e Informática Perú Informe Principal Encuesta Demográfica y de Salud Familiar—ENDES 2018. Lima, Peru: INEI/Peru; 2019.
    1. Paganini D, Uyoga MA, Kortman GA, Cercamondi CI, Moretti D, Barth-Jaeggi T, Schwab C, Boekhorst J, Timmerman HM, Lacroix C. Prebiotic galacto-oligosaccharides mitigate the adverse effects of iron fortification on the gut microbiome: a randomised controlled study in Kenyan infants. Gut. 2017;66:1956–67.
    1. Prentice AM, Mendoza YA, Pereira D, Cerami C, Wegmuller R, Constable A, Spieldenner J. Dietary strategies for improving iron status: balancing safety and efficacy. Nutr Rev. 2016;75:49–60.
    1. Khush GS, Lee S, Cho J-I, Jeon J-S. Biofortification of crops for reducing malnutrition. Plant Biotechnology Reports. 2012;6:195–202.
    1. Finkelstein JL, Haas JD, Mehta S. Iron-biofortified staple food crops for improving iron status: a review of the current evidence. Curr Opin Biotechnol. 2017;44:138–45.
    1. Cercamondi CI, Egli IM, Mitchikpe E, Tossou F, Zeder C, Hounhouigan JD, Hurrell RF. Total iron absorption by young women from iron-biofortified pearl millet composite meals is double that from regular millet meals but less than that from post-harvest iron-fortified millet meals. J Nutr. 2013;143:1376–82.
    1. Low JW, Mwanga RO, Andrade M, Carey E, Ball A-M. Tackling vitamin A deficiency with biofortified sweetpotato in sub-Saharan Africa. Global Food Security. 2017;14:23–30.
    1. Food and Agriculture Organization Statistical database. 2019; [cited 2019 Jul 23] [Internet]. Available from: .
    1. Nyekanyeka T, Heck S, McLean S, Mnjengezulu G, Chipungu F, Chimsale R, Botha B. Less hunger, better health and more wealth: the benefits of knowledge sharing in Malawi's Orange-Fleshed Sweet Potato project. Hunger Nutrition Climate Justice; presented in Dublin, Ireland 15–16 April, 2013.
    1. de Haan S, Burgos G, Liria R, Rodriguez F, Creed-Kanashiro HM, Bonierbale M. The nutritional contribution of potato varietal diversity in Andean food systems: a case study. Am J Potato Res. 2019;96:151–63.
    1. Sindi K, Kiria C, Low J, Sopo O, Abidin P. Rooting out hunger in Malawi with nutritious orange-fleshed sweetpotato: a baseline survey report, Blantyre, Malawi. Lima, Peru: International Potato Center (CIP); 2013.
    1. Bonierbale MW, Amoros WR, Salas E, de Jong W. Chapter 6, Potato breeding. In: The potato crop: its agricultural, nutritional, and social contribution to humankind. Campos H, Ortiz O, editors. Cham, Switzerland: Springer Nature; 2020, p. 163–219.
    1. Mwanga RO, Andrade MI, Carey EE, Low JW, Yencho GC, Grüneberg WJ. Sweetpotato (Ipomoea batatas L.). In: Genetic improvement of tropical crops. Campos H, Caligari PDS, editors. Cham: Springer; 2017. p. 181–218.
    1. Amoros W, Salas E, Hualla V, Burgos G, De Boeck B, Eyzaguirre R, zum Felde T, Bonierbale M. Heritability and genetic gains for iron and zinc concentration in diploid potato. Crop Sci. 2020;60:1884–96.
    1. Christides T, Amagloh F, Coad J. Iron bioavailability and provitamin A from sweet potato-and cereal-based complementary foods. Foods. 2015;4:463–76.
    1. Andre CM, Burgos G, Ziebel J, Guignard C, Hausman J-F, zum Felde T. In vitro iron bioaccessibility and uptake from orange-fleshed sweet potato (Ipomoea batatas (L.) Lam.) clones grown in Peru. J Food Compos Anal. 2018;68:79–86.
    1. Andre CM, Ghislain M, Bertin P, Oufir M, del Rosario Herrera M, Hoffmann L, Hausman J-F, Larondelle Y, Evers D. Andean potato cultivars (Solanum tuberosum L.) as a source of antioxidant and mineral micronutrients. J Agric Food Chem. 2007;55:366–78.
    1. Andre CM, Oufir M, Guignard C, Hoffmann L, Hausman J-F, Evers D, Larondelle Y. Antioxidant profiling of native Andean potato tubers (Solanum tuberosum L.) reveals cultivars with high levels of β-carotene, α-tocopherol, chlorogenic acid, and petanin. J Agric Food Chem. 2007;55:10839–49.
    1. Andre CM, Evers Dl, Ziebel J, Guignard CD, Hausman J-F, Bonierbale M, zum Felde T, Burgos G. In vitro bioaccessibility and bioavailability of iron from potatoes with varying vitamin C, carotenoid, and phenolic concentrations. J Agric Food Chem. 2015;63:9012–21.
    1. Petry N, Boy E, Wirth JP, Hurrell RF. Review: the potential of the common bean (Phaseolus vulgaris) as a vehicle for iron biofortification. Nutrients. 2015;7:1144–73.
    1. Cercamondi CI, Icard-Vernière C, Egli IM, Vernay M, Hama F, Brouwer ID, Zeder C, Berger J, Hurrell RF, Mouquet-Rivier C. A higher proportion of iron-rich leafy vegetables in a typical Burkinabe maize meal does not increase the amount of iron absorbed in young women. J Nutr. 2014;144:1394–400.
    1. World Health Organization Iron deficiency anaemia: assessment, prevention, and control A guide for programme managers. Geneva, Switzerland: World Health Organization; 2001, p. 114.
    1. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42:377–81.
    1. Makower RU. Extraction and determination of phytic acid in beans (Phaseolus vulgaris). Cereal Chem. 1970;47:288–95.
    1. Paganini D, Uyoga MA, Cercamondi CI, Moretti D, Mwasi E, Schwab C, Bechtler S, Mutuku FM, Galetti V, Lacroix C. Consumption of galacto-oligosaccharides increases iron absorption from a micronutrient powder containing ferrous fumarate and sodium iron EDTA: a stable-isotope study in Kenyan infants. Am J Clin Nutr. 2017;106:1020–31.
    1. Troesch B, Egli I, Zeder C, Hurrell RF, De Pee S, Zimmermann MB. Optimization of a phytase-containing micronutrient powder with low amounts of highly bioavailable iron for in-home fortification of complementary foods. Am J Clin Nutr. 2008;89:539–44.
    1. Singleton VL, Orthofer R, Lamuela-Raventós RM. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 1999;299:152–78.
    1. Burgos G, Muñoa L, Sosa P, Cayhualla E, Carpio R, Zum Felde T. Procedures for chemical analysis of potato and sweetpotato samples at CIP's Quality and Nutrition Laboratory. Lima, Peru: International Potato Center; 2014.
    1. Erhardt JG, Estes JE, Pfeiffer CM, Biesalski HK, Craft NE. Combined measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein by an inexpensive, sensitive, and simple sandwich enzyme-linked immunosorbent assay technique. J Nutr. 2004;134:3127–32.
    1. Hotz K, Krayenbuehl P-A, Walczyk T. Mobilization of storage iron is reflected in the iron isotopic composition of blood in humans. J Biol Inorgan Chem. 2012;17:301–9.
    1. Brown E, Hopper J, Hodges J, Bradley B, Wennesland R, Yamauchi H. Red cell, plasma, and blood volume in healthy women measured by radiochromium cell-labeling and hematocrit. J Clin Invest. 1962;41:2182–90.
    1. Walczyk T, Davidsson L, Zavaleta N, Hurrell RF. Stable isotope labels as a tool to determine the iron absorption by Peruvian school children from a breakfast meal. Fresen J Anal Chem. 1997;359:445–9.
    1. Hosain F, Marsaglia G, Noyes W, Finch C. The nature of internal iron exchange in man. Trans Assoc Am Physicians. 1962;75:59–63.
    1. Institute of Medicine (US) Panel on Micronutrients. Dietary Reference Intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc: a report of the Panel on Micronutrients. Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. Washington, DC: National Academy Press; 2001.
    1. World Health Organization Vitamin and mineral requirements in human nutrition. Geneva, Switzerland: World Health Organization; Food and Agriculture Organization; 2004.
    1. Kumar V, Sinha AK, Makkar HP, Becker K. Dietary roles of phytate and phytase in human nutrition: a review. Food Chem. 2010;120:945–59.
    1. Hurrell R, Egli I. Iron bioavailability and dietary reference values. Am J Clin Nutr. 2010;91:1461S–7S.
    1. Petry N, Egli I, Gahutu JB, Tugirimana PL, Boy E, Hurrell R. Stable iron isotope studies in Rwandese women indicate that the common bean has limited potential as a vehicle for iron biofortification. J Nutr. 2012;142:492–7.
    1. Petry N, Rohner F, Gahutu JB, Campion B, Boy E, Tugirimana PL, Zimmerman MB, Zwahlen C, Wirth JP, Moretti D. In Rwandese women with low iron status, iron absorption from low-phytic acid beans and biofortified beans is comparable, but low-phytic acid beans cause adverse gastrointestinal symptoms. J Nutr. 2016;146:970–5.
    1. Teow CC, Truong V-D, McFeeters RF, Thompson RL, Pecota KV, Yencho GC. Antioxidant activities, phenolic and β-carotene contents of sweet potato genotypes with varying flesh colours. Food Chem. 2007;103:829–38.
    1. Petry N, Egli I, Zeder C, Walczyk T, Hurrell R. Polyphenols and phytic acid contribute to the low iron bioavailability from common beans in young women. J Nutr. 2010;140:1977–82.
    1. Cercamondi CI, Egli IM, Zeder C, Hurrell RF. Sodium iron EDTA and ascorbic acid, but not polyphenol oxidase treatment, counteract the strong inhibitory effect of polyphenols from brown sorghum on the absorption of fortification iron in young women. Br J Nutr. 2014;111:481–9.
    1. Kurata R, Sun H-N, Oki T, Okuno S, Ishiguro K, Sugawara T. Sweet potato polyphenols. In: Sweet potato, Mu T-H, Singh J. Chennai, India: Academic Press; 2019, p. 177–222.
    1. Miranda L, Deußer H, Evers D. The impact of in vitro digestion on bioaccessibility of polyphenols from potatoes and sweet potatoes and their influence on iron absorption by human intestinal cells. Food Funct. 2013;4:1595–601.
    1. Ezekiel R, Singh N, Sharma S, Kaur A. Beneficial phytochemicals in potato—a review. Food Res Int. 2013;50:487–96.
    1. Graham RD, Rosser JM.. Carotenoids in staple foods: their potential to improve human nutrition. Food Nutr Bull. 2000;21:404–9.
    1. García-Casal MN, Layrisse M, Solano L, Barón MA, Arguello F, Llovera D, Ramírez J, Leets I, Tropper E. Vitamin A and β-carotene can improve nonheme iron absorption from rice, wheat and corn by humans. J Nutr. 1998;128:646–50.
    1. Teucher B, Olivares M, Cori H. Enhancers of iron absorption: ascorbic acid and other organic acids. Int J Vitam Nutr Res. 2004;74:403–19.
    1. Burgos G, Auqui S, Amoros W, Salas E, Bonierbale M. Ascorbic acid concentration of native Andean potato varieties as affected by environment, cooking and storage. J Food Compos Anal. 2009;22:533–8.
    1. Tudela JA, Espın J, Gil M. Vitamin C retention in fresh-cut potatoes. Postharvest Biol Technol. 2002;26:75–84.
    1. Hallberg L, Brune M, Erlandsson M, Sandberg A-S, Rossander-Hulten L. Calcium: effect of different amounts on nonheme-and heme-iron absorption in humans. Am J Clin Nutr. 1991;53:112–19.
    1. Hallberg L, Hulthén L.. Prediction of dietary iron absorption: an algorithm for calculating absorption and bioavailability of dietary iron. Am J Clin Nutr. 2000;71:1147–60.
    1. USDA, Agricultural Research Service FoodData Central. 2019. [cited 2020 Jan 7] [Internet]. Available from: .
    1. Lönnerdal B. Calcium and iron absorption—mechanisms and public health relevance. Int J Vitam Nutr Res. 2010;80:293–99.
    1. Thompson BA, Sharp PA, Elliott R, Fairweather-Tait SJ. Inhibitory effect of calcium on non-heme iron absorption may be related to translocation of DMT-1 at the apical membrane of enterocytes. J Agric Food Chem. 2010;58:8414–17.
    1. Moretti D, Zimmermann MB, Wegmüller R, Walczyk T, Zeder C, Hurrell RF. Iron status and food matrix strongly affect the relative bioavailability of ferric pyrophosphate in humans. Am J Clin Nutr. 2006;83:632–8.
    1. Ganz T. Hepcidin and iron regulation, 10 years later. Blood. 2011;117:4425–33.
    1. Thurnham DI, McCabe LD, Haldar S, Wieringa FT, Northrop-Clewes CA, McCabe GP. Adjusting plasma ferritin concentrations to remove the effects of subclinical inflammation in the assessment of iron deficiency: a meta-analysis. Am J Clin Nutr. 2010;92:546–55.
    1. Cook JD, Boy E, Flowers C, del Carmen Daroca M. The influence of high-altitude living on body iron. Blood. 2005;106:1441–6.
    1. Renassia C, Peyssonnaux C.. New insights into the links between hypoxia and iron homeostasis. Curr Opin Hematol. 2019;26:125–30.
    1. Witt KE, Huerta-Sánchez E.. Convergent evolution in human and domesticate adaptation to high-altitude environments. Philosophical Transactions of the Royal Society B. 2019;374:20180235.
    1. Walczyk T, Muthayya S, Wegmüller R, Thankachan P, Sierksma A, Frenken LG, Thomas T, Kurpad A, Hurrell RF. Inhibition of iron absorption by calcium is modest in an iron-fortified, casein-and whey-based drink in Indian children and is easily compensated for by addition of ascorbic acid. J Nutr. 2014;144:1703–9.

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi