The Nutrient and Metabolite Profile of 3 Complementary Legume Foods with Potential to Improve Gut Health in Rural Malawian Children

Erica C Borresen, Lei Zhang, Indi Trehan, Nora Jean Nealon, Kenneth M Maleta, Mark J Manary, Elizabeth P Ryan, Erica C Borresen, Lei Zhang, Indi Trehan, Nora Jean Nealon, Kenneth M Maleta, Mark J Manary, Elizabeth P Ryan

Abstract

Background: Environmental enteric dysfunction (EED), frequently seen in rural Malawian children, causes chronic inflammation and increases the risk of stunting. Legumes may be beneficial for improving nutrition and reducing the risk of developing EED in weaning children. Objective: The objectives of this study were to determine the nutritional value, verify the food safety, and identify metabolite profiles of 3 legume-based complementary foods: common bean (CB), cowpea (CP), and traditional corn-soy blend (CSB). Methods: Foods were prepared by using local ingredients and analyzed for nutrient composition with the use of Association of Official Analytical Chemists (AOAC) standards (950.46, 991.43, 992.15, 996.06, and 991.36) for macro- and micronutrient proximate analysis. Food safety analysis was conducted in accordance with the Environmental Protection Agency (7471B) and AOAC (2008.02) standards. The metabolite composition of foods was determined with nontargeted ultra-performance LC-tandem mass spectrometry metabolomics. Results: All foods provided similar energy; CB and CP foods contained higher protein and dietary fiber contents than did the CSB food. Iron and zinc were highest in the CSB and CP foods, whereas CB and CP foods contained higher amounts of magnesium, phosphorus, and potassium. A total of 652 distinct metabolites were identified across the 3 foods, and 23, 14, and 36 metabolites were specific to the CSB, CB, and CP foods, respectively. Among the potential dietary biomarkers of intake to distinguish legume foods were pipecolic acid and oleanolic acid for CB; arabinose and serotonin for CSB; and quercetin and α- and γ-tocopherol acid for CP. No heavy metals were detected, and aflatoxin was measured only in the CSB (5.2 parts per billion). Conclusions: Legumes in the diet provide a rich source of protein, dietary fiber, essential micronutrients, and phytochemicals that may reduce EED. These food metabolite analyses identified potential dietary biomarkers of legume intake for stool, urine, and blood detection that can be used in future studies to assess the relation between the distinct legumes consumed and health outcomes. This trial was registered at clinicaltrials.gov as NCT02472262 and NCT02472301.

Keywords: Phaseolus vulgaris; Vigna unguiculata; complementary foods; corn-soybean blend; enteric disease; environmental enteric dysfunction; foodomics; infant; malnutrition; metabolomics.

Figures

FIGURE 1
FIGURE 1
Venn diagram of the total number of metabolites detected across the 3 legume foods.
FIGURE 2
FIGURE 2
Relative abundance z score distributions of selected metabolites detected in all 3 legume foods to visualize the distinct profiles. These include essential amino acids and common nonprotein nitrogen components in the amino acid pathway (A), FAs in the lipid pathway (B), the cofactors and vitamins pathway (C), and phytochemicals in the xenobiotic pathway (D). Dotted lines represent a relative abundance z score of 0. CB, common bean; CP, cowpea; CSB, corn-soybean blend.

References

    1. Keusch GT, Denno DM, Black RE, Duggan C, Guerrant RL, Lavery JV, Nataro JP, Rosenberg IH, Ryan ET, Tarr PI, et al. . Environmental enteric dysfunction: pathogenesis, diagnosis, and clinical consequences. Clin Infect Dis 2014;59:S207–12.
    1. Crane RJ, Jones KDJ, Berkley JA.. Environmental enteric dysfunction: an overview. Food Nutr Bull 2015;36:S76–87.
    1. Prendergast A, Kelly P.. Review: enteropathies in the developing world: neglected effects on global health. Am J Trop Med Hyg 2012;86:756–63.
    1. Korpe PS, Petri WA.. Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol Med 2012;18:328–36.
    1. Trehan I, Benzoni NS, Wang AZ, Bollinger LB, Ngoma TN, Chimimba UK, Stephenson KB, Agapova SE, Maleta KM, Manary MJ.. Common beans and cowpeas as complementary foods to reduce environmental enteric dysfunction and stunting in Malawian children: study protocol for two randomized controlled trials. Trials 2015;16:520.
    1. Messina MJ.. Legumes and soybeans: overview of their nutritional profiles and health effects. Am J Clin Nutr 1999;70(Suppl):439S–50S.
    1. Hayat I, Ahmad A, Masud T, Ahmed A, Bashir S.. Nutritional and health perspectives of beans (Phaseolus vulgaris L.): an overview. Crit Rev Food Sci Nutr 2014;54:580–92.
    1. Marchione TJ.. Foods provided through U.S. government emergency food aid programs: policies and customs governing their formulation, selection and distribution. J Nutr 2002;132(Suppl):2104S–11S.
    1. de Pee S, Bloem MW.. Current and potential role of specially formulated foods and food supplements for preventing malnutrition among 6- to 23-month-old children and for treating moderate malnutrition among 6- to 59-month-old children. Food Nutr Bull 2009;30(3Suppl):S434–63.
    1. Agostoni C, Riva E, Giovannini M.. Dietary fiber in weaning foods of young children. Pediatrics 1995;96:1002–5.
    1. Chen Y, McGee R, Vandemark G, Brick M, Thompson HJ.. Dietary fiber analysis of four pulses using AOAC 2011.25: implications for human health. Nutrients 2016;8:829.
    1. Cai R, Hettiarachchy NS, Jalaluddin M.. High-performance liquid chromatography determination of phenolic constituents in 17 varieties of cowpeas. J Agric Food Chem 2003;51:1623–7.
    1. Moray C, Game ET, Maxted N.. Prioritising in situ conservation of crop resources: a case study of African cowpea (Vigna unguiculata). Sci Rep 2014;4:5247.
    1. Siddiq M, Uebersax MA.. Dry beans and pulses production and consumption—an overview. In: Siddiq M, Uebersax MA, editors. Dry beans and pulses production, processing and nutrition. Hoboken (NJ): Blackwell Publishing Ltd.; 2012. p. 1–22.
    1. Hartman TJ, Albert PS, Zhang ZY, Bagshaw D, Kris-Etherton PM, Ulbrecht J, Miller CK, Bobe G, Colburn NH, Lanza E.. Consumption of a legume-enriched, low-glycemic index diet is associated with biomarkers of insulin resistance and inflammation among men at risk for colorectal cancer. J Nutr 2010;140:60–7.
    1. Campos-Vega R, Oomah B, Loarca-Piña G, Vergara-Castañeda H.. Common beans and their non-digestible fraction: cancer inhibitory activity—an overview. Foods 2013;2:374–392.
    1. Ayogu RN, Nnam NM, Mbah M.. Evaluation of two local cowpea species for nutrient, antinutrient, and phytochemical compositions and organoleptic attributes of their wheat-based cookies. Food Nutr Res 2016;60:29600.
    1. Kyei-Boahen S, Savala CEN, Chikoye D, Abaidoo R.. Growth and yield responses of cowpea to inoculation and phosphorus fertilization in different environments. Front Plant Sci 2017;8:646.
    1. Abizari AR, Pilime N, Armar-Klemesu M, Brouwer ID.. Cowpeas in Northern Ghana and the factors that predict caregivers' intention to give them to schoolchildren. PLoS One 2013;8:e72087.
    1. Scalbert A, Brennan L, Manach C, Andres-Lacueva C, Dragsted LO, Draper J, Rappaport SM, van der Hooft JJJ, Wishart DS.. The food metabolome: a window over dietary exposure. Am J Clin Nutr 2014;99:1286–308.
    1. Ramalingam A, Kudapa H, Pazhamala LT, Weckwerth W, Varshney RK.. Proteomics and metabolomics: two emerging areas for legume improvement. Front Plant Sci 2015;6:1116.
    1. Joshi T, Fitzpatrick MR, Chen SY, Liu Y, Zhang HX, Endacott RZ, Gaudiello EC, Stacey G, Nguyen HT, Xu D.. Soybean knowledge base (SoyKB): a web resource for integration of soybean translational genomics and molecular breeding. Nucleic Acids Res 2014;42(D1):D1245–52.
    1. Chebrolu KK, Fritschi FB, Ye SQ, Krishnan HB, Smith JR, Gillman JD.. Impact of heat stress during seed development on soybean seed metabolome. Metabolomics 2016;12:28.
    1. Forster GM, Heuberger AL, Broeckling CD, Bauer JE, Ryan EP.. Consumption of cooked navy bean powders modulate the canine fecal and urine metabolome. Curr Metabolomics 2015;3:90–101.
    1. Mensack MM, Fitzgerald VK, Ryan EP, Lewis MR, Thompson HJ, Brick MA.. Evaluation of diversity among common beans (Phaseolus vulgaris L.) from two centers of domestication using 'omics' technologies. BMC Genomics 2010;11:686.
    1. Borresen EC, Jenkins-Puccetti N, Schmitz K, Brown DG, Pollack A, Fairbanks A, Wdowik M, Rao S, Nelson TL, Luckasen G, et al. . A pilot randomized controlled clinical trial to assess tolerance and efficacy of navy bean and rice bran supplementation for lowering cholesterol in children. Global pediatric health 2017;4:2333794X17694231.
    1. Stobaugh HC, Ryan KN, Kennedy JA, Grise JB, Crocker AH, Thakwalakwa C, Litkowski PE, Maleta KM, Manary MJ, Trehan I.. Including whey protein and whey permeate in ready-to-use supplementary food improves recovery rates in children with moderate acute malnutrition: a randomized, double-blind clinical trial. Am J Clin Nutr 2016;103:926–33.
    1. LaGrone LN, Trehan I, Meuli GJ, Wang RJ, Thakwalakwa C, Maleta K, Manary MJ.. A novel fortified blended flour, corn-soy blend “plus-plus,” is not inferior to lipid-based ready-to-use supplementary foods for the treatment of moderate acute malnutrition in Malawian children. Am J Clin Nutr 2012;95:212–9.
    1. Trucksess MW, Weaver CM, Oles CJ, Fry FS, Noonan GO, Betz JM, Rader JI.. Determination of aflatoxins B(1), B(2), G(1), and G(2) and ochratoxin A in ginseng and ginger by multitoxin immunoaffinity column cleanup and liquid chromatographic quantitation: collaborative study. J AOAC Int 2008;91:511–23.
    1. Environmental Protection Agency Method 7471B: mercury in solid or semisolid waste (manual cold-vapor technique) [Internet]. 1998. [cited 2017 Sep 1]. Available from: .
    1. Hong B.. Technical regulations on mycotoxin and heavy metals MRLs in foods. USDA; 2013.
    1. National Grain and Feed Association Mycotoxin regulatory guidance: FDA. A guide for grain elevators, feed manufacture rs, grain processors and exporters. Arlington (VA): National Grain and Feed Association; 2011.
    1. Zarei I, Brown DG, Nealon NJ, Ryan EP.. Rice bran metabolome contains amino acids, vitamins & cofactors, and phytochemicals with medicinal and nutritional properties. Rice (N Y) 2017;10:24.
    1. WHO Complementary feeding of young children in developing countries: a review of current scientific knowledge (WHO/NUT/98.1). Geneva (Switzerland): WHO; 1998.
    1. National Academy of Medicine [Internet]. Dietary Reference Intakes tables and applications [cited 2017 Mar 8]. Available from: .
    1. Lagishetty CV, Naik SR.. Polyamines: potential anti-inflammatory agents and their possible mechanism of action. Indian J Pharmacol 2008;40:121–5.
    1. Bischoff SC, Mailer R, Pabst O, Weier G, Sedlik W, Li ZS, Chen JJ, Murphy DL, Gershon MD.. Role of serotonin in intestinal inflammation: knockout of serotonin reuptake transporter exacerbates 2,4,6-trinitrobenzene sulfonic acid colitis in mice. Am J Physiol Gastrointest Liver Physiol 2009;296:G685–95.
    1. Lawson BR, Belkowski SM, Whitesides JF, Davis P, Lawson JW.. Immunomodulation of murine collagen-induced arthritis by N, N-dimethylglycine and a preparation of Perna canaliculus. BMC Complement Altern Med 2007;7:20.
    1. Hara K, Nakamura M, Haranishi Y, Terada T, Kataoka K, Sata T.. Antinociceptive effect of intrathecal administration of hypotaurine in rat models of inflammatory and neuropathic pain. Amino Acids 2012;43:397–404.
    1. Szabó C, Dawson VL.. Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol Sci 1998;19:287–98.
    1. Granados-Soto V, Terán-Rosales F, Rocha-González HI, Reyes-García G, Medina-Santillán R, Rodríguez-Silverio J, Flores-Murrieta FJ.. Riboflavin reduces hyperalgesia and inflammation but not tactile allodynia in the rat. Eur J Pharmacol 2004;492:35–40.
    1. Reiter E, Jiang Q, Christen S.. Anti-inflammatory properties of α- and γ-tocopherol. Mol Aspects Med 2007;28:668–91.
    1. Dwiyanti MS, Maruyama S, Hirono M, Sato M, Park E, Yoon SH, Yamada T, Abe J.. Natural diversity of seed alpha-tocopherol ratio in wild soybean (Glycine soja) germplasm collection. Breed Sci 2016;66:653–7.
    1. Singh GB, Singh S, Bani S, Gupta BD, Banerjee SK.. Anti-inflammatory activity of oleanolic acid in rats and mice. J Pharm Pharmacol 1992;44:456–8.
    1. Gupta MB, Bhalla TN, Gupta GP, Mitra CR, Bhargava KP.. Anti-inflammatory activity of taxifolin. Jpn J Pharmacol 1971;21:377–82.
    1. García-Lafuente A, Guillamón E, Villares A, Rostagno MA, Martínez JA.. Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflamm Res 2009;58:537–52.
    1. Kao ES, Wang CJ, Lin WL, Yin YF, Wang CP, Tseng TH.. Anti-inflammatory potential of flavonoid contents from dried fruit of Crataegus pinnatifida in vitro and in vivo. J Agric Food Chem 2005;53:430–6.
    1. Camuesco D, Comalada M, Rodriguez-Cabezas ME, Nieto A, Lorente MD, Concha A, Zarzuelo A, Galvez J.. The intestinal anti-inflammatory effect of quercitrin is associated with an inhibition in iNOS expression. Br J Pharmacol 2004;143:908–18.
    1. Gutiérrez-Uribe JA, Romo-Lopez I, Serna-Saldívar SO.. Phenolic composition and mammary cancer cell inhibition of extracts of whole cowpeas (Vigna unguiculata) and its anatomical parts. J Funct Foods 2011;3:290–7.
    1. Callaghan-Gillespie M, Schaffner AA, Garcia P, Fry J, Eckert R, Malek S, Trehan I, Thakwalakwa C, Maleta KM, Manary MJ, et al. . Trial of ready-to-use supplemental food and corn-soy blend in pregnant Malawian women with moderate malnutrition: a randomized controlled clinical trial. Am J Clin Nutr 2017. Aug 9 (Epub ahead of print; ).
    1. Rogers BL, Wilner LB, Maganga G, Walton SM, Suri DJ, Langlois BK, Chui KK, Boiteau JM, Vosti SA, Webb P.. Program changes are effective and cost-effective in increasing the amount of oil used in preparing corn soy blend porridge for treatment of moderate acute malnutrition in Malawi. Matern Child Nutr 2017. Jan 12 (Epub ahead of print; ).
    1. Cao KF, Zhang HH, Han HH, Song Y, Bai XL, Sun H.. Effect of dietary protein sources on the small intestine microbiome of weaned piglets based on high-throughput sequencing. Lett Appl Microbiol 2016;62:392–8.
    1. Ordiz MI, Stephenson K, Agapova S, Wylie KM, Maleta K, Martin J, Trehan I, Tarr PI, Manary MJ.. Environmental enteric dysfunction and the fecal microbiota in Malawian children. Am J Trop Med Hyg 2017;96:473–6.
    1. Weiss G.. Iron and immunity: a double-edged sword. Eur J Clin Invest 2002;32(Suppl 1):70–8.
    1. Jonker FA, Calis JC, van Hensbroek MB, Phiri K, Geskus RB, Brabin BJ, Leenstra T.. Iron status predicts malaria risk in Malawian preschool children. PLoS One 2012;7:e42670.
    1. Titilayo A, Palamuleni ME, Omisakin O.. Sociodemographic factors influencing adherence to antenatal iron supplementation recommendations among pregnant women in Malawi: analysis of data from the 2010 Malawi Demographic and Health Survey. Malawi Med J 2016;28:1–5.
    1. Wang AZ, Shulman RJ, Crocker AH, Thakwalakwa C, Maleta KM, Devaraj S, Manary MJ, Trehan I.. A combined intervention of zinc, multiple micronutrients, and albendazole does not ameliorate environmental enteric dysfunction or stunting in rural Malawian children in a double-blind randomized controlled trial. J Nutr 2017;147:97–103.
    1. Paganini D, Uyoga MA, Zimmermann MB.. Iron fortification of foods for infants and children in low-income countries: eff ects on the gut microbiome, gut inflammation, and diarrhea. Nutrients 2016;8.
    1. Lazzerini M, Wanzira H.. Oral zinc for treating diarrhoea in children. Cochrane Database Syst Rev 2016;12:CD005436.
    1. Lajolo FM, Genovese MI.. Nutritional significance of lectins and enzyme inhibitors from legumes. J Agric Food Chem 2002;50:6592–8.
    1. Gibson RS, Bailey KB, Gibbs M, Ferguson EL.. A review of phytate, iron, zinc, and calcium concentrations in plant-based complementary foods used in low-income countries and implications for bioavailability. Food Nutr Bull 2010;31(2Suppl):S134–46.
    1. Manary MJ, Hotz C, Krebs NF, Gibson RS, Westcott JE, Broadhead RL, Hambidge KM.. Zinc homeostasis in Malawian children consuming a high-phytate, maize-based diet. Am J Clin Nutr 2002;75:1057–61.
    1. Obiro WC, Zhang T, Jiang B.. The nutraceutical role of the Phaseolus vulgaris alpha-amylase inhibitor. Br J Nutr 2008;100:1–12.
    1. Sarwar Gilani G, Wu Xiao C, Cockell KA.. Impact of antinutritional factors in food proteins on the digestibility of protein and the bioavailability of amino acids and on protein quality. Br J Nutr 2012;108(Suppl 2):S315–32.
    1. Queiroz Kda S, de Oliveira AC, Helbig E, Reis SM, Carraro F.. Soaking the common bean in a domestic preparation reduced the contents of raffinose-type oligosaccharides but did not interfere with nutritive value. J Nutr Sci Vitaminol (Tokyo) 2002;48:283–9.
    1. Zaheer K, Humayoun Akhtar M.. An updated review of dietary isoflavones: nutrition, processing, bioavailability and impacts on human health. Crit Rev Food Sci Nutr 2017;57:1280–93.
    1. Kennedy G, Hambidge KM, Manary M.. A reduced phytate diet does not reduce endogenous fecal zinc in children on a habitual high-phytate diet. J Pediatr Gastroenterol Nutr 2010;51:678–9.
    1. Manary MJ, Krebs NF, Gibson RS, Broadhead RL, Hambidge KM.. Community-based dietary phytate reduction and its effect on iron status in Malawian children. Ann Trop Paediatr 2002;22:133–6.
    1. Manary MJ, Hotz C, Krebs NF, Gibson RS, Westcott JE, Arnold T, Broadhead RL, Hambidge KM.. Dietary phytate reduction improves zinc absorption in Malawian children recovering from tuberculosis but not in well children. J Nutr 2000;130:2959–64.
    1. Michalak A, Mosinska P, Fichna J.. Polyunsaturated fatty acids and their derivatives: therapeutic value for inflammatory, functional gastrointestinal disorders, and colorectal cancer. Front Pharmacol 2016;7:459.
    1. Zentek J, Ferrara F, Pieper R, Tedin L, Meyer W, Vahjen W.. Effects of dietary combinations of organic acids and medium chain fatty acids on the gastrointestinal microbial ecology and bacterial metabolites in the digestive tract of weaning piglets. J Anim Sci 2013;91:3200–10.
    1. Michaelsen KF, Hoppe C, Roos N, Kaestel P, Stougaard M, Lauritzen L, Mølgaard C, Girma T, Friis H.. Choice of foods and ingredients for moderately malnourished children 6 months to 5 years of age. Food Nutr Bull 2009;30(3Suppl 3):S343–404.
    1. Jin Y, Wu S, Zeng Z, Fu Z.. Effects of environmental pollutants on gut microbiota. Environ Pollut 2017;222:1–9.
    1. Turner PC, Flannery B, Isitt C, Ali M, Pestka J.. The role of biomarkers in evaluating human health concerns from fungal contaminants in food. Nutr Res Rev 2012;25:162–79.
    1. US FDA Guidance for industry: action levels for poisonous or deleterious substances in human food and animal feed. Silver Spring (MD): Food and Drug Administration; 2000.
    1. Perera T, Young MR, Zhang Z, Murphy G, Colburn NH, Lanza E, Hartman TJ, Cross AJ, Bobe G.. Identification and monitoring of metabolite markers of dry bean consumption in parallel human and mouse studies. Mol Nutr Food Res 2015;59:795–806.
    1. Phull AR, Eo SH, Kim SJ.. Oleanolic acid (OA) regulates inflammation and cellular dedifferentiation of chondrocytes via MAPK signaling pathways. Cell Mol Biol (Noisy-le-Grand) 2017;63:12–7.
    1. Dueñas M, Fernández D, Hernández T, Estrella I, Muñoz R.. Bioactive phenolic compounds of cowpeas (Vigna sinensis L): modifications by fermentation with natural microflora and with Lactobacillus plantarum ATCC 14917. J Sci Food Agric 2005;85:297–304.
    1. Chirumbolo S.. The role of quercetin, flavonols and flavones in modulating inflammatory cell function. Inflamm Allergy Drug Targets 2010;9:263–85.
    1. Tamura M, Kurusu Y, Hori S.. Effect of dietary l-arabinose on the intestinal microbiota and metabolism of dietary daidzein in adult mice. Biosci Microbiota Food Health 2012;31:59–65.
    1. Kelly GS.. Larch arabinogalactan: clinical relevance of a novel immune-enhancing polysaccharide. Altern Med Rev 1999;4:96–103.
    1. Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L.. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 2016;7:979.
    1. Jan AT, Azam M, Siddiqui K, Ali A, Choi I, Haq QMR.. Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. Int J Mol Sci 2015;16:29592–630.

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