Bioavailability of Micronutrients From Nutrient-Dense Whole Foods: Zooming in on Dairy, Vegetables, and Fruits

Alida Melse-Boonstra, Alida Melse-Boonstra

Abstract

In order to fully exploit the nutrient density concept, thorough understanding of the biological activity of single nutrients in their interaction with other nutrients and food components from whole foods is important. This review provides a narrative overview of recent insights into nutrient bioavailability from complex foods in humans, highlighting synergistic and antagonistic processes among food components for two different food groups, i.e., dairy, and vegetables and fruits. For dairy, bioavailability of vitamins A, B2, B12 and K, calcium, phosphorous, magnesium, zinc and iodine are discussed, whereas bioavailability of pro-vitamin A, folate, vitamin C and K, potassium, calcium, magnesium and iron are discussed for vegetables and fruits. Although the bioavailability of some nutrients is fairly well-understood, for other nutrients the scientific understanding of uptake, absorption, and bioavailability in humans is still at a nascent stage. Understanding the absorption and bioavailability of nutrients from whole foods in interaction with food components that influence these processes will help to come to individual diet scores that better reflect absorbable nutrient intake in epidemiologic studies that relate dietary intake to health outcomes. Moreover, such knowledge may help in the design of foods, meals, and diets that aid in the supply of bioavailable nutrients to specific target groups.

Keywords: bioavailability; dairy; fruits; minerals; vegetables; vitamins.

Copyright © 2020 Melse-Boonstra.

References

    1. Gibson R. The role of diet and host related factors in nutrient bioavailability. Food Nutr Bull. (2007) 28:S77–100. 10.1177/15648265070281S108
    1. Davidsson L, Tanumihardjo S. New frontiers in science and technology: nuclear techniques in nutrition. Am J Clin Nutr. (2011) 94:691S−5S. 10.3945/ajcn.110.005819
    1. Fairweather-Tait SJ, Lynch S, Hotz C, Hurrell RF, Abrahamse L, Beebe S, et al. . The usefulness of in vitro models to assess iron and zinc bioavailability. Int J Vitam Nutr Res. (2005) 75:371–4. 10.1024/0300-9831.75.6.371
    1. Etcheverry P, Grusak MA, Fleige LE. Application of in vitro bioaccessibility and bioavailability methods for calcium, carotenoids, folate, iron, magnesium, polyphenols, zinc, and vitamins B6, B12, D, and E. Front Physiol. (2012) 3:317. 10.3389/fphys.2012.00317
    1. Elwood PC, Pickering JE, Ian Givens D, Gallacher JE. The consumption of milk and dairy foods and the incidence of vascular disease and diabetes: an overview of the evidence. Lipids. (2010) 45:925–39. 10.1007/s11745-010-3412-5
    1. Huth PJ, Park KM. Influence of dairy product and milk fat consumption on cardiovascular disease risk: a review of the evidence. Adv Nutr. (2012) 3:266–85. 10.3945/an.112.002030
    1. de Goede J, Soedamah-Muthu SS, Pan A, Gijsbers L, Geleijnse JM. Dairy consumption and risk of stroke: a systematic review and updated dose-response meta-analysis of prospective cohort studies. J Am Heart Assoc. (2016) 5:e002787. 10.1161/JAHA.115.002787
    1. Drouin-Chartier J-P, Brassard D, Tessier-Grenier M, Côté JA, Labonté M-È, Desroches S, et al. . Systematic review of the association between dairy product consumption and risk of cardiovascular-related clinical outcomes. Adv Nutr An Int Rev J. (2016) 7:1026–40. 10.3945/an.115.011403
    1. Thorning TK, Raben A, Tholstrup T, Soedamah-Muthu SS, Givens I, Astrup A. Milk and dairy products: good or bad for human health? An assessment of the totality of scientific evidence. Food Nutr Res. (2016) 60:32527. 10.3402/fnr.v60.32527
    1. Soedamah-Muthu SS, de Goede J. Dairy consumption and cardiometabolic diseases: systematic review and updated meta-Analyses of prospective cohort studies. Curr Nutr Rep. (2018) 7:171–82. 10.1007/s13668-018-0253-y
    1. Van Den Heuvel EGHM, Steijns JMJM. Dairy products and bone health: how strong is the scientific evidence? Nutr Res Rev. (2018) 31:164–78. 10.1017/S095442241800001X
    1. Drewnowski A. The contribution of milk and milk products to micronutrient density and affordability of the U.S. Diet J Am Coll Nutr. (2011) 30:422S−8S. 10.1080/07315724.2011.10719986
    1. Dugan CE, Fernandez ML. Effects of dairy on metabolic syndrome parameters: a review. J Biol Med. (2014) 87:135–47.
    1. Vissers PAJ, Streppel MT, Feskens EJM, de Groot LCPGM. The contribution of dairy products to micronutrient intake in the Netherlands. J Am Coll Nutr. (2011) 30:415S−21S. 10.1080/07315724.2011.10719985
    1. Bath SC, Sleeth ML, McKenna M, Walter A, Taylor A, Rayman MP. Iodine intake and status of UK women of childbearing age recruited at the University of Surrey in the winter. Br J Nutr. (2014) 112:1715–23. 10.1017/S0007114514002797
    1. Olza J, Aranceta-Bartrina J, González-Gross M, Ortega RM, Serra-Majem L, Varela-Moreiras G, et al. . Reported dietary intake and food sources of zinc, selenium, and vitamins a, e and c in the Spanish population: findings from the anibes study. Nutrients. (2017) 9:697. 10.3390/nu9070697
    1. Herrick KA, Perrine CG, Aoki Y, Caldwell KL. Iodine status and consumption of key iodine sources in the U.S. population with special attention to reproductive age women. Nutrients. (2018) 10:874. 10.3390/nu10070874
    1. Partearroyo T, De Lourdes Samaniego-Vaesken M, Ruiz E, Olza J, Aranceta-Bartrina J, Gil Á, et al. . Dietary sources and intakes of folates and vitamin B12 in the Spanish population: findings from the ANIBES study. PLoS ONE. (2017) 12:e0189230. 10.1371/journal.pone.0189230
    1. Obeid R, Heil SG, Verhoeven MMA, van den Heuvel EGHM, de Groot LCPGM, Eussen SJPM. Vitamin B12 intake from animal foods, biomarkers, and health aspects. Front Nutr. (2019) 6:93. 10.3389/fnut.2019.00093
    1. Górska-Warsewicz H, Rejman K, Laskowski W, Czeczotko M. Milk and dairy products and their nutritional contribution to the average polish diet. Nutrients. (2019) 11:771 10.3390/nu11081771
    1. Powers HJ. Riboflavin (vitamin B-2) and health 1, 2. Am J Clin Nutr. (2003) 77:1352–60. 10.1093/ajcn/77.6.1352
    1. Saedisomeolia A, Ashoori M. Riboflavin in human health: a review of current evidences. Adv Food Nutr Res. (2018) 83:57–81. 10.1016/bs.afnr.2017.11.002
    1. Auclair O, Han Y, Burgos SA. Consumption of milk and alternatives and their contribution to nutrient intakes among Canadian adults: evidence from the 2015. Canadian community health survey-nutrition. Nutrients. (2019) 11:1–17. 10.3390/nu11081948
    1. Guéguen L, Pointillart A. The bioavailability of dietary calcium. J Am Coll Nutr. (2000) 19:119S−36. 10.1080/07315724.2000.10718083
    1. Fishbein L. Multiple sources of dietary calcium - some aspects of its essentiality. Regul Toxicol Pharmacol. (2004) 39:67–80. 10.1016/j.yrtph.2003.11.002
    1. Nordin BEC, Marshall DH. Calcium in biology. In: Nordin BEC, editor. Calcium in Biology. Berlin: Springer-Verlag; (1988). p. 447–71.
    1. Heaney R, Recker R, Stegman M, Moy A. Calcium absorption in women: relationships to calcium intake, estrogen status, and age. J Bone Miner Res. (1989) 4:469–75. 10.1002/jbmr.5650040404
    1. Avioli L. Calcium and osteoporosis. Annu Rev Nutr. (1984) 4:471–91. 10.1146/annurev.nu.04.070184.002351
    1. Kaushik R, Sachdeva B, Arora S, Kapila S, Wadhwa BK. Bioavailability of vitamin D2 and calcium from fortified milk. Food Chem. (2014) 147:307–11. 10.1016/j.foodchem.2013.09.150
    1. Lee YS, Noguchi T, Naito H. Intestinal absorption of calcium in rats given diets containing casein or amino acid mixture: the role of casein phosphopeptides. Br J Nutr. (1983) 49:67–76. 10.1079/BJN19830012
    1. Mykkanen H, Wasserman R. Enhanced absorption of calcium by casein phosphopeptides in rachitic and normal chicks. J Nutr. (1980) 110:2141–8. 10.1093/jn/110.11.2141
    1. Li Y, Tome D, Desjeux JF. Indirect effect of casein phosphopeptides on calcium absorption in rat ileum in vitro. Reprod Nutr Dev. (1989) 29:227–33. 10.1051/rnd:19890210
    1. Bronner F. Current concepts of calcium absorption: an overview. J Nutr. (1992) 122(Suppl. 3) :641–3. 10.1093/jn/122.suppl_3.641
    1. Whiting S, Draper H. The role of sulfate in the calciuria of high protein diets in adult rats. J Nutr. (1980) 110:212–22. 10.1093/jn/110.2.212
    1. Kerstetter J, Allen L. Protein intake and calcium homeostasis. Adv Nutr Res. (1994) 9:167–81. 10.1007/978-1-4757-9092-4_10
    1. Massey LK. Issues and opinions in nutrition does excess dietary protein adversely affect bone? J Nutr. (1998) 128:1054–7. 10.1093/jn/128.6.1048
    1. Van Beresteijn ECH, Brussaard J, Van Schaik M. Relationship between the calcium-to-protein ratio in milk and the urinary calcium excretion in healthy adults - a controlled turnover study. Am J Clin Nutr. (1990) 52:142–6. 10.1093/ajcn/52.1.142
    1. Linkswiler H, Zemel M, Hegsted M, Schuette S. Protein induced hypercalciuria. Fed Proc. (1981) 40:2429.
    1. Hegsted M, Schuette S, Zemel M, Linkswiler H. Urinary calcium and calcium balance in young men as affected by level of protein and phosphorus intake. J Nutr. (1981) 111:553–62. 10.1093/jn/111.3.553
    1. Allen L, Oddoye E, Margen S. Protein-induced hypercalciuria: a longer term study. Am J Clin Nutr. (1979) 32:741–9. 10.1093/ajcn/32.4.741
    1. Allen LH. Calcium bioavailability and absorption: a review. Am J Clin Nutr. (1982) 35:783–808. 10.1093/ajcn/35.4.783
    1. Miller D. Calcium in the diet; food sources, recommended intakes, and nutritional bioavailability. Adv Food Nutr Res. (1989) 33:104–55. 10.1016/S1043-4526(08)60127-8
    1. Pansu D, Bellaton C, Bronner F. Effect of Ca intake on saturable and nonsaturable components of duodenal Ca transport. Am J Physiol Gastrointest Liver Physiol. (1981) 3:32–7. 10.1152/ajpgi.1981.240.1.G32
    1. Cochet B, Jung A, Griessen M, Bartholdi P, Schaller P, Donath A. Effects of lactose on intestinal calcium absorption in normal and lactase-deficient subjects. Gastroenterology. (1983) 84:935–40. 10.1016/0016-5085(83)90194-4
    1. Griessen M, Cochet B, Infante F, Jung A, Bartholdi P, Donath A, et al. . Calcium absorption from milk in lactase-deficient subjects. Am J Clin Nutr. (1989) 49:377–84. 10.1093/ajcn/49.2.377
    1. Tremaine WJ, Newcomer AD, Lawrence Riggs B, McGill DB. Calcium absorption from milk in lactase-deficient and lactase-sufficient adults. Dig Dis Sci. (1986) 31:376–8. 10.1007/BF01311672
    1. Nickel KP, Martin BR, Smith DL, Smith JB, Miller GD, Weaver CM. Calcium bioavailability from bovine milk and dairy products in premenopausal women using intrinsic and extrinsic labeling techniques. J Nutr. (1996) 126:1406–11. 10.1093/jn/126.5.1406
    1. Schuette S, Yasillo N, Thompson C. The effect of carbohydrates in milk on the absorption of calcium by postmenopausal women. J Am Coll Nutr. (1991) 10:132–9. 10.1080/07315724.1991.10718137
    1. Abrams SA, Griffin IJ, Davila PM. Calcium and zinc absorption from lactose-containing and lactose-free infant formulas. Am J Clin Nutr. (2002) 76:442–6. 10.1093/ajcn/76.2.442
    1. Szilagyi A. Review article: lactose - A potential prebiotic. Aliment Pharmacol Ther. (2002) 16:1591–602. 10.1046/j.1365-2036.2002.01321.x
    1. Whisner CM, Martin BR, Schoterman MHC, Nakatsu CH, McCabe LD, McCabe GP, et al. . Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br J Nutr. (2013) 110:1292–303. 10.1017/S000711451300055X
    1. Hodges JK, Cao S, Cladis DP, Weaver CM. Lactose intolerance and bone health: the challenge of ensuring adequate calcium intake. Nutrients. (2019) 11:718. 10.3390/nu11040718
    1. Rizzoli R, Biver E, Bonjour JP, Coxam V, Goltzman D, Kanis JA, et al. . Benefits and safety of dietary protein for bone health—an expert consensus paper endorsed by the European Society for Clinical and Economical Aspects of Osteopororosis, Osteoarthritis, and Musculoskeletal Diseases and by the International Osteoporosis Foundation. Osteoporos Int. (2018) 29:1933–48. 10.1007/s00198-018-4534-5
    1. Bonjour JP, Kraenzlin M, Levasseur R, Warren M, Whiting S. Dairy in adulthood: from foods to nutrient interactions on bone and skeletal muscle health. J Am Coll Nutr. (2013) 32:251–63. 10.1080/07315724.2013.816604
    1. Buchowski MS, Miller DD. Calcium bioavailability from ripening cheddar cheese. J Food Sci. (1990) 55:1293–5. 10.1111/j.1365-2621.1990.tb03919.x
    1. Spencer H, Kramer L, Osis D. Do protein and phosphorus cause calcium loss? J Nutr. (1988) 118:657–60. 10.1093/jn/118.6.657
    1. Calvo MS, Tucker KL. Is phosphorus intake that exceeds dietary requirements a risk factor in bone health? Ann N Y Acad Sci. (2013) 1301:29–35. 10.1111/nyas.12300
    1. Takeda E, Yamamoto H, Yamanaka-Okumura H, Taketani Y. Dietary phosphorus in bone health and quality of life. Nutr Rev. (2012) 70:311–21. 10.1111/j.1753-4887.2012.00473.x
    1. Recker R, Heaney R. The effect of milk supplements on calcium metabolism, bone metabolism and calcium balance. Am J Clin Nutr. (1985) 41:254–63. 10.1093/ajcn/41.2.254
    1. Herrero C, Granado F, Blanco I, Olmedilla B. Vitamin A and E content in dairy products: their contribution to the recommended dietary allowances (RDA) for elderly people. J Nutr Heal Aging. (2002) 6:57–9. 10.1007/s00394-006-0612-0
    1. Dainty JR, Bullock NR, Hart DJ, Hewson AT, Turner R, Finglas PM, et al. . Quantification of the bioavailability of riboflavin from foods by use of stable-isotope labels and kinetic modeling. Am J Clin Nutr. (2007) 85:1557–64. 10.1093/ajcn/85.6.1557
    1. Gille D, Schmid A. Vitamin B12 in meat and dairy products. Nutr Rev. (2015) 73:106–15. 10.1093/nutrit/nuu011
    1. Fedosov SN, Nexo E, Heegaard CW. Vitamin B 12 and its binding proteins in milk from cow and buffalo in relation to bioavailability of B 12. J Dairy Sci. (2019) 102:4891–905. 10.3168/jds.2018-15016
    1. Russell RM, Baik H, Kehayias JJ. Older men and women efficiently absorb vitamin B-12 from milk and fortified bread. J Nutr. (2001) 131:291–3. 10.1093/jn/131.2.291
    1. Doets EL, In't Veld PH, Szczecinska A, Dhonukshe-Rutten RAM, Cavelaars AEJM, Van 't Veer P, et al. . Systematic review on daily vitamin B 12 losses and bioavailability for deriving recommendations on vitamin B 12 intake with the factorial approach. Ann Nutr Metab. (2013) 62:311–22. 10.1159/000346968
    1. Naik S, Mahalle N, Greibe E, Ostenfeld MS, Heegaard CW, Nexo E, et al. . Hydroxo-B12 for supplementation in B12 deficient lactovegetarians. (2019) 12:1–14. 10.3390/nu11102382
    1. Walther B, Karl JP, Booth SL, Boyaval P. Menaquinones, bacteria, and the food supply: the relevance of dairy and fermented food products to vitamin K requirements. Adv Nutr. (2013) 4:463–73. 10.3945/an.113.003855
    1. Geleijnse JM, Vermeer C, Grobbee DE, Schurgers LJ, Knapen MHJ, van der Meer IM, et al. . Dietary intake of menaquinone is associated with a reduced risk of coronary heart disease: the Rotterdam study. J Nutr. (2004) 134:3100–5. 10.1093/jn/134.11.3100
    1. Gast GCM, de Roos NM, Sluijs I, Bots ML, Beulens JWJ, Geleijnse JM, et al. . A high menaquinone intake reduces the incidence of coronary heart disease. Nutr Metab Cardiovasc Dis. (2009) 19:504–10. 10.1016/j.numecd.2008.10.004
    1. Fu X, Harshman SG, Shen X, Haytowitz DB, Karl JP, Wolfe BE, et al. . Multiple vitamin K forms exist in dairy foods. Curr Dev Nutr. (2017) 1:e000638. 10.3945/cdn.117.000638
    1. Vermeer C, Raes J, van 't Hoofd C, Knapen MHJ, Xanthoulea S. Menaquinone content of cheese. Nutrients. (2018) 10:446. 10.3390/nu10040446
    1. Knapen MHJ, Braam LAJLM, Teunissen KJ, Van't Hoofd CM, Zwijsen RML, Van Den Heuvel EGHM, et al. . Steady-state vitamin K2 (menaquinone-7) plasma concentrations after intake of dairy products and soft gel capsules. Eur J Clin Nutr. (2016) 70:831–6. 10.1038/ejcn.2016.3
    1. Marles RJ, Roe AL, Oketch-Rabah HA. US pharmacopeial convention safety evaluation of menaquinone-7, a form of vitamin K. Nutr Rev. (2017) 75:553–78. 10.1093/nutrit/nux022
    1. St-Jules DE, Jagannathan R, Gutekunst L, Kalantar-Zadeh K, Sevick MA. Examining the proportion of dietary phosphorus from plants, animals, and food additives excreted in urine. J Ren Nutr. (2017) 27:78–83. 10.1053/j.jrn.2016.09.003
    1. McClure ST, Rebholz CM, Phillips KM, Champagne CM, Selvin E, Appel LJ. The percentage of dietary phosphorus excreted in the urine varies by dietary pattern in a randomized feeding study in adults. J Nutr. (2019) 149:816–23. 10.1093/jn/nxy318
    1. Blakeborough P, Salter DN, Gurr MI. Zinc binding in cow's milk and human milk. Biochem J. (1983) 209:505–12. 10.1042/bj2090505
    1. Sandström B, Cederblad ALB. Zinc absorption from human milk, cow's milk, and infant formulas. Am J Dis Child. (1983) 137:726–9. 10.1001/archpedi.1983.02140340010002
    1. Talsma EF, Moretti D, Ly SC, Dekkers R, van den Heuvel EGHM, Fitri A, et al. . Zinc absorption from milk is affected by dilution but not by thermal processing, and milk enhances absorption of zinc from high-phytate rice in young Dutch women. J Nutr. (2017) 147:1086–93. 10.3945/jn.116.244426
    1. Lönnerdal B. Dietary factors influencing zinc absorption 1. J Nutr. (2000) 130:1378S−83S. 10.1093/jn/130.5.1378S
    1. Ekmekcioglu C. Intestinal bioavailability of minerals and trace elements from milk and beverages in humans. Nahrung Food. (2000) 44:390–7. 10.1002/1521-3803(20001201)44:6<390::AID-FOOD390>;2-Y
    1. Vegarud GE, Langsrud T, Svenning C. Mineral-binding milk proteins and peptides; occurrence, biochemical and technological characteristics. Br J Nutr. (2000) 84:91–8. 10.1017/S0007114500002300
    1. Brink EJ, Dekker PR, Van Beresteijn ECH, Beynen AC. Bioavailability of magnesium and calcium from cow's milk and soya-bean beverage in rats. Br J Nutr. (1992) 68:271–82. 10.1079/BJN19920084
    1. Brink EJ, van Beresteijn ECH, Dekker PR, Beynen AC. Urinary excretion of magnesium and calcium as an index of absorption is not affected by lactose intake in healthy adults. Br J Nutr. (1993) 69:863–70. 10.1079/BJN19930086
    1. van den Heuvel EGHM, Muijs T, Brouns F, Hendriks HFJ. Short-chain fructo-oligosaccharides improve magnesium absorption in adolescent girls with a low calcium intake. Nutr Res. (2009) 29:229–37. 10.1016/j.nutres.2009.03.005
    1. Whisner CM, Castillo LF. Prebiotics, bone and mineral metabolism. Calcif Tissue Int. (2018) 102:443–79. 10.1007/s00223-017-0339-3
    1. van der Reijden OL, Zimmermann MB, Galetti V. Iodine in dairy milk: sources, concentrations and importance to human health. Best Pract Res Clin Endocrinol Metab. (2017) 31:385–95. 10.1016/j.beem.2017.10.004
    1. van de Kamp ME, Saridakis I, Verkaik-Kloosterman J. Iodine content of semi-skimmed milk available in the Netherlands depending on farming (organic versus conventional) and heat treatment (pasteurized versus UHT) and implications for the consumer. J Trace Elem Med Biol. (2019) 56:178–83. 10.1016/j.jtemb.2019.08.008
    1. Van Der Reijden OL, Galetti V, Bürki S, Zeder C, Krzystek A, Haldimann M, et al. . Iodine bioavailability from cow milk: a randomized, crossover balance study in healthy iodine-replete adults. Am J Clin Nutr. (2019) 110:102–10. 10.1093/ajcn/nqz092
    1. Aune D, Giovannucci E, Boffetta P, Fadnes LT, Keum NN, Norat T, et al. . Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality-A systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol. (2017) 46:1029–56. 10.1093/ije/dyw319
    1. Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W, et al. . Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. BMJ. (2014) 349:g4490. 10.1136/bmj.g4490
    1. Hall JN, Moore S, Harper SB, Lynch JW. Global variability in fruit and vegetable consumption. Am J Prev Med. (2009) 36:402–9.e5 10.1016/j.amepre.2009.01.029
    1. Lock K, Pomerleau J, Causer L, Altmann DR, Mckee M. The global burden of disease attributable to low consumption of fruit and vegetables: implications for the global strategy on diet. Bull WHO. (2005) 83:100–8.
    1. Auestad N, Hurley JS, Fulgoni VL, Schweitzer CM. Contribution of food groups to energy and nutrient intakes in five developed countries. Nutrients. (2015) 7:4593–618. 10.3390/nu7064593
    1. Cassidy A, Minihane AM. The role of metabolism (and the microbiome) in defining the clinical efficacy of dietary flavonoids. Am J Clin Nutr. (2017) 105:10–22. 10.3945/ajcn.116.136051
    1. Scholz-Ahrens KE, Schrezenmeir J. Inulin, oligofructose and mineral metabolism — experimental data and mechanism. Br J Nutr. (2002) 87:S179–86. 10.1079/BJN/2002535
    1. Riedl J, Linseisen J, Hoffmann J, Wolfram G. Some dietary fibers reduce the absorption of carotenoids in women. J Nutr. (1999) 129:2170–6. 10.1093/jn/129.12.2170
    1. Bohn T. Dietary factors affecting polyphenol bioavailability. Nutr Rev. (2014) 72:429–52. 10.1111/nure.12114
    1. Bohn T. Bioavailability of Non-Provitamin A carotenoids. Curr Nutr Food Sci. (2008) 4:240–58. 10.2174/157340108786263685
    1. Sandberg A. The effect of food processing on phytate hydrolysis and availability of iron and zinc. Adv Exp Med Biol. (1991) 289:499–508. 10.1007/978-1-4899-2626-5_33
    1. Castenmiller JJM, West CE, Linssen JPH, van het Hof KH, Voragen AGJ. The food matrix of spinach is a limiting factor in determining the bioavailability of β-Carotene and to a lesser extent of lutein in humans. J Nutr. (1999) 129:349–55. 10.1093/jn/129.2.349
    1. van het Hof KH, Tijburg LBM, Pietrzik K, Weststrate JA. Influence of feeding different vegetables on plasma levels of carotenoids, folate and vitamin C. Effect of disruption of the vegetable matrix. Br J Nutr. (1999) 82:203–12. 10.1017/S0007114599001385
    1. Schweiggert RM, Mezger D, Schimpf F, Steingass CB, Carle R. Influence of chromoplast morphology on carotenoid bioaccessibility of carrot, mango, papaya, and tomato. Food Chem. (2012) 135:2736–42. 10.1016/j.foodchem.2012.07.035
    1. Schweiggert RM, Kopec RE, Villalobos-Gutierrez MG, Högel J, Quesada S, Esquivel P, et al. . Carotenoids are more bioavailable from papaya than from tomato and carrot in humans: a randomised cross-over study. Br J Nutr. (2014) 111:490–8. 10.1017/S0007114513002596
    1. Van Loo-Bouwman CA, Naber THJ, Schaafsma G. A review of vitamin A equivalency of β-carotene in various food matrices for human consumption. Br J Nutr. (2014) 111:2153–66. 10.1017/S0007114514000166
    1. Institute of Medicine Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium and Zinc. Washington DC: National Academy Press; (2001).
    1. Burri BJ. Beta-cryptoxanthin as a source of vitamin A. J Sci Food Agric. (2015) 95:1786–94. 10.1002/jsfa.6942
    1. Burri BJ, La Frano MR, Zhu C. Absorption, metabolism, and functions of β-cryptoxanthin. Nutr Rev. (2016) 74:69–82. 10.1093/nutrit/nuv064
    1. Brown MJ, Ferruzzi MG, Nguyen ML, Cooper DA, Eldridge AL, Schwartz SJ, et al. . Carotenoid bioavailability is higher from salads ingested with full-fat than with fat-reduced salad dressings as measured with electrochemical detection. Am J Clin Nutr. (2004) 80:396–403. 10.1093/ajcn/80.2.396
    1. Goltz SR, Campbell WW, Chitchumroonchokchai C, Failla ML, Ferruzzi MG. Meal triacylglycerol profile modulates postprandial absorption of carotenoids in humans. Mol Nutr Food Res. (2012) 56:866–77. 10.1002/mnfr.201100687
    1. White WS, Zhou Y, Crane A, Dixon P, Quadt F, Flendrig LM. Modeling the dose effects of soybean oil in salad dressing on carotenoid and fat-soluble vitamin bioavailability in salad vegetables. Am J Clin Nutr. (2017) 106:1041–51. 10.3945/ajcn.117.153635
    1. Melse-Boonstra A, Verhoef P, West CE, Van Rhijn JA, Van Breemen RB, Lasaroms JJP, et al. . A dual-isotope-labeling method of studying the bioavailability of hexaglutamyl folic acid relative to that of monoglutamyl folic acid in humans by using multiple orally administered low doses. Am J Clin Nutr. (2006) 84:1128–33. 10.1093/ajcn/84.5.1128
    1. Melse-Boonstra A, West CE, Katan MB, Kok FJ, Verhoef P. Bioavailability of heptaglutamyl relative to monoglutamyl folic acid in healthy adults. Am J Clin Nutr. (2004) 79:424–9. 10.1093/ajcn/79.3.424
    1. Pietrzik K, Bailey L, Shane B. Folic acid and L-5-methyltetrahydrofolate comparison of clinical pharmacokinetics and pharmacodynamics. Clin Pharmacokinetics. (2010) 49:535–48. 10.2165/11532990-000000000-00000
    1. Melse-Boonstra A. Dietary Folate: Bioavailability Studies in Humans (PhD thesis). Wageningen University; (2003). p. 1–166.
    1. Institute of Medicine Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline. Washington DC: National Academy Press; (1998).
    1. Packer JE, Slater TF, Willson RL. Direct observation of a free radical interaction between vitamin E and vitamin C [13]. Nature. (1979) 278:737–8. 10.1038/278737a0
    1. Carr AC, Vissers MCM. Synthetic or food-derived vitamin C-are they equally bioavailable? Nutrients. (2013) 5:4284–304. 10.3390/nu5114284
    1. Padayatty SJ, Levine M. Vitamin C: the known and the unknown and goldilocks. Oral Dis. (2016) 22:463–93. 10.1111/odi.12446
    1. Tanaka K, Hashimoto T, Tokumaru S, Iguchi H, Kojo S. Interactions between vitamin C and vitamin E are observed in tissues of inherently scorbutic rats. J Nutr. (1997) 127:2060–4. 10.1093/jn/127.10.2060
    1. Song J, Kwon O, Chen S, Daruwala R, Eck P, Park JB, et al. . Flavonoid inhibition of sodium-dependent vitamin C transporter 1 (SVCT1) and glucose transporter isoform 2 (GLUT2), intestinal transporters for vitamin C and glucose. J Biol Chem. (2002) 277:15252–60. 10.1074/jbc.M110496200
    1. Corpe CP, Lee JH, Kwon O, Eck P, Narayanan J, Kirk KL, et al. . 6-Bromo-6-deoxy-L-ascorbic acid: an ascorbate analog specific for Na +-dependent vitamin C transporter but not glucose transporter pathways. J Biol Chem. (2005) 280:5211–20. 10.1074/jbc.M412925200
    1. Park JB, Levine M. Intracellular accumulation of ascorbic acid is inhibited by flavonoids via blocking of dehydroascorbic acid and ascorbic acid uptakes in HL-60, U937 and jurkat cells. J Nutr. (2000) 130:1297–302. 10.1093/jn/130.5.1297
    1. Bolton-Smith C, Price RJG, Fenton ST, Harrington DJ, Shearer MJ. Compilation of a provisional UK database for the phylloquinone (vitamin K1) content of foods. Br J Nutr. (2000) 83:389–99.
    1. Halder M, Petsophonsakul P, Akbulut AC, Pavlic A, Bohan F, Anderson E, et al. . Vitamin K: double bonds beyond coagulation insights into differences between vitamin K1 and K2 in health and disease. Int J Mol Sci. (2019) 20:896. 10.3390/ijms20040896
    1. Gijsbers BLMG, Jie K-SG, Vermeer C. Effect of food composition on vitamin K absorption in human volunteers. Br J Nutr. (1996) 76:223–9. 10.1079/BJN19960027
    1. Novotny JA, Kurilich AC, Britz SJ, Baer DJ, Clevidence BA. Vitamin K absorption and kinetics in human subjects after consumption of 13C-labelled phylloquinone from kale. Br J Nutr. (2010) 104:858–62. 10.1017/S0007114510001182
    1. Beulens JWJ, Booth SL, Van Den Heuvel EGHM, Stoecklin E, Baka A, Vermeer C. The role of menaquinones (vitamin K2) in human health. Br J Nutr. (2013) 110:1357–68. 10.1017/S0007114513001013
    1. Geleijnse JM, Kok FJ, Grobbee DE. Blood pressure response to changes in sodium and potassium intake: a metaregression analysis of randomised trials. J Hum Hypertens. (2003) 17:471–80. 10.1038/sj.jhh.1001575
    1. Binia A, Jaeger J, Hu Y, Singh A, Zimmermann D. Daily potassium intake and sodium-to-potassium ratio in the reduction of blood pressure: a meta-analysis of randomized controlled trials. J Hypertens. (2015) 33:1509–20. 10.1097/HJH.0000000000000611
    1. Naismith DJ, Braschi A. An investigation into the bioaccessibility of potassium in unprocessed fruits and vegetables. Int J Food Sci Nutr. (2008) 59:438–50. 10.1080/09637480701690519
    1. MacDonald-Clarke CJ, Martin BR, McCabe LD, McCabe GP, Lachcik PJ, Wastney M, et al. . Bioavailability of potassium from potatoes and potassium gluconate: a randomized dose response trial. Am J Clin Nutr. (2016) 104:346–53. 10.3945/ajcn.115.127225
    1. Stone MS, Martyn L, Weaver CM. Potassium intake, bioavailability, hypertension, and glucose control. Nutrients. (2016) 8:444. 10.3390/nu8070444
    1. Heaney RP, Weaver CM. Calcium absorption from kale. Am J Clin Nutr. (1990) 51:656–7. 10.1093/ajcn/51.4.656
    1. Weaver CM, Heaney RP, Nickel KP, Packard PI. Calcium bioavailability from high oxalate vegetables: Chinese vegetables, sweet potatoes and rhubarb. J Food Sci. (1997) 62:524–5. 10.1111/j.1365-2621.1997.tb04421.x
    1. Charoenkiatkul S, Kriengsinyos W, Tuntipopipat S, Suthutvoravut U, Weaver CM. Calcium absorption from commonly consumed vegetables in healthy Thai women. J Food Sci. (2008) 73:H218–21. 10.1111/j.1750-3841.2008.00949.x
    1. Heaney RP, Weaver CM, Hinders S, Martin B, Packard PT. Absorbability of calcium from brassica vegetables: broccoli, bok choy, and kale. J Food Sci. (1993) 58:1378–80. 10.1111/j.1365-2621.1993.tb06187.x
    1. Bohn T, Davidsson L, Walczyk T, Hurrell RF. Fractional magnesium absorption is significantly lower in human subjects from a meal served with an oxalate-rich vegetable, spinach, as compared with a meal served with kale, a vegetable with a low oxalate content. Br J Nutr. (2004) 91:601–6. 10.1079/BJN20031081
    1. Vormann J. Magnesium : nutrition and metabolism. Mol Aspects Med. (2003) 24:27–37. 10.1016/S0098-2997(02)00089-4
    1. Schuchardt JP, Hahn A. Intestinal absorption and factors influencing bioavailability of magnesium - An update. Curr Nutr Food Sci. (2017) 13:260–78. 10.2174/1573401313666170427162740
    1. McMillan T, Johnston F. The absorption of iron from spinach by six young women, and the effect of beef upon the absorption. J Nutr. (1951) 44:383–98. 10.1093/jn/44.3.383
    1. Crispin DJ, Street G, Varey JE. Kinetics of the decomposition of [2Fe-2S] ferredoxin from spinach: implications for iron bioavailability and nutritional status. Food Chem. (2001) 72:355–62. 10.1016/S0308-8146(00)00236-3
    1. Hallberg L, Brune M, Rossander L. Effect of ascorbic acid on iron absorption from different types of meals. Studies with ascorbic-acid-rich foods and synthetic ascorbic acid given in different amounts with different meals. Hum Nutr Appl Nutr. (1986) 40:97–113.
    1. Lane DJR, Bae DH, Merlot AM, Sahni S, Richardson DR. Duodenal cytochrome b (DCYTB) in iron metabolism: an update on function and regulation. Nutrients. (2015) 7:2274–96. 10.3390/nu7042274
    1. Hallberg L, Brune M, Rossander L. Iron absorption in man: ascorbic acid and dose-dependent inhibition by phytate. Am J Clin Nutr. (1989) 49:140–4. 10.1093/ajcn/49.1.140
    1. Bonsmann SSG, Walczyk T, Renggli S, Hurrell RF. Oxalic acid does not influence nonhaem iron absorption in humans: a comparison of kale and spinach meals. Eur J Clin Nutr. (2008) 62:336–41. 10.1038/sj.ejcn.1602721
    1. Scheers N, Rossander-Hulthen L, Torsdottir I, Sandberg AS. Increased iron bioavailability from lactic-fermented vegetables is likely an effect of promoting the formation of ferric iron (Fe3+). Eur J Nutr. (2016) 55:373–82. 10.1007/s00394-015-0857-6

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