A Review of Mushrooms as a Potential Source of Dietary Vitamin D
Abstract
:1. Introduction
2. Requirements and Intake of Dietary Vitamin D
3. Vitamin D Metabolism in Mushrooms
4. Vitamin D Content of Fresh Mushrooms
4.1. Fresh Wild Mushrooms
4.2. Fresh Retail Mushrooms
4.3. Fresh Mushrooms Exposed to Sunlight
4.4. Fresh Mushrooms Exposed to UV Radiation from Lamps
5. Dried Mushrooms Exposed to UV Radiation from Lamps
5.1. Sun-Dried Mushrooms
5.2. Hot-Air Dried Mushrooms
5.3. Freeze-Dried Mushrooms
6. Stability of Vitamin D2 in Vitamin D-Enhanced Mushrooms after Storage and Cooking
6.1. Storage
6.2. Cooking
7. Bioavailability of Vitamin D2 from Mushrooms
8. Conclusions
Author Contributions
Funding
Acknowledgements
Conflicts of Interest
References
- Jones, G. Vitamin D. Modern Nutrition in Health and Disease, 11 ed.; Wolters Kluwer Health: Baltimore, MD, USA, 2014. [Google Scholar]
- Lips, P. Vitamin D physiology. Prog. Biophys. Mol. Biol. 2006, 92, 4–8. [Google Scholar] [CrossRef] [PubMed]
- Girgis, C.M.; Clifton-Bligh, R.J.; Hamrick, M.W.; Holick, M.F.; Gunton, J.E. The roles of vitamin D in skeletal muscle: Form, function, and metabolism. Endocr. Rev. 2013, 34, 33–83. [Google Scholar] [CrossRef] [PubMed]
- Hossein-nezhad, A.; Holick, M.F. Vitamin D for health: A global perspective. Mayo Clin. Proc. 2013, 88, 720–755. [Google Scholar] [CrossRef] [PubMed]
- Ford, J.A.; MacLennan, G.S.; Avenell, A.; Bolland, M.; Grey, A.; Witham, M.; Group, R.T. Cardiovascular disease and vitamin D supplementation: Trial analysis, systematic review, and meta-analysis. Am. J. Clin. Nutr. 2014, 100, 746–755. [Google Scholar] [CrossRef] [PubMed]
- Koduah, P.; Paul, F.; Dörr, J. Vitamin D in the prevention, prediction and treatment of neurodegenerative and neuroinflammatory diseases. EPMA J. 2017, 8, 313–325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gaksch, M.; Jorde, R.; Grimnes, G.; Joakimsen, R.; Schirmer, H.; Wilsgaard, T.; Methiesen, E.B.; Njølstad, I.; Løchen, M.; März, W.; et al. Vitamin D and mortality: Individual participant data meta-analysis of standardized 25-hydroxyvitamin D in 26916 individuals from a European consortium. PLoS ONE 2017, 12, e0170791. [Google Scholar] [CrossRef] [PubMed]
- Theodoratou, E.; Tzoulaki, I.; Zgaga, L.; Ioannidis, J.P.A. Vitamin D and multiple health outcomes: Umbrella review of systematic reviews and meta-analyses of observational studies and randomised trials. BMJ 2014, 348, g2035. [Google Scholar] [CrossRef] [PubMed]
- Phillips, K.M.; Horst, R.L.; Koszewski, N.J.; Simon, R.R. Vitamin D4 in mushrooms. PLoS ONE 2012, 7, e40702. [Google Scholar] [CrossRef] [PubMed]
- Keegan, R.J.; Lu, Z.; Bogusz, J.M.; Williams, J.E.; Holick, M.F. Photobiology of vitamin D in mushrooms and its bioavailability in humans. Dermatoendocrinology 2013, 5, 165–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Urbain, P.; Valverde, J.; Jakobsen, J. Impact on vitamin D2, vitamin D4 and agaritine in Agaricus bisporus mushrooms after artificial and natural solar UV light exposure. Plant Food Hum. Nutr. 2016, 71, 314–321. [Google Scholar] [CrossRef] [PubMed]
- Taofiq, O.; Fernandes, A.; Barros, L.; Barreiro, M.F.; Ferreira, I.C.F.R. UV-irradiated mushrooms as a source of vitamin D2: A review. Trends Food Sci. Technol. 2017, 70, 82–94. [Google Scholar] [CrossRef]
- Calvo, M.S.; Whiting, S.J.; Barton, C.N. Vitamin D intake: A global perspective of current status. J. Nutr. 2005, 135, 310–316. [Google Scholar] [CrossRef] [PubMed]
- Lamberg-Allardt, C.J.E. Vitamin D in foods and as supplements. Prog. Biophys. Mol. Biol. 2006, 92, 33–38. [Google Scholar] [CrossRef] [PubMed]
- Mau, J.L.; Chen, P.R.; Yang, J.H. Ultraviolet irradiation increased vitamin D2 content in edible mushrooms. J. Agric. Food Chem. 1998, 46, 5269–5272. [Google Scholar] [CrossRef]
- Nölle, N.; Argyropoulos, D.; Ambacher, S.; Muller, J.; Biesalski, H.K. Vitamin D2 enrichment in mushrooms by natural or artificial UV-light during drying. Food Sci. Technol. 2016, 85, 400–404. [Google Scholar]
- Simon, R.R.; Phillips, K.M.; Horst, R.L.; Munro, I.C. Vitamin D mushrooms: Comparison of the composition of button mushrooms (Agaricus bisporus) treated post-harvest with UVB light or sunlight. J. Agric. Food Chem. 2011, 59, 8724–8732. [Google Scholar] [CrossRef] [PubMed]
- Royse, D.J. A global perspective on the high five: Agaricus, Pleurotus, Lentinula, Auricularia & Flammulina. In Proceedings of the 8th International Conference on Mushroom Biology and Mushroom Products (ICMBMP8), New Delhi, India, 19–22 November 2014. [Google Scholar]
- Nutrient Reference Values for Australia and New Zealand; National Health and Medical Research Council, Commonwealth of Australia: Canberra, Australia, 2006.
- Dietary Reference Intakes for Calcium and Vitamin D; Institute of Medicine, The National Academies Press: Washington, DC, USA, 2011.
- Dietary Reference Values for Nutrients: Summary Report; European Food Safety Authority: Parma, Italy, 2017.
- Dietary Reference Intakes. Available online: https://www.canada.ca/en/health-canada/services/food-nutrition/healthy-eating/dietary-reference-intakes/tables/reference-values-vitamins-dietary-reference-intakes-tables-2005.html (accessed on 11 October 2018).
- Vitamin D and Health; Scientific Advisory Committee on Nutrition, The Stationary Office: London, UK, 2016.
- Bailey, R.L.; Dodd, K.W.; Goldman, J.A.; Gahche, J.J.; Dwyer, J.T.; Moshfegh, A.J.; Sempos, C.T.; Picciano, M.F. Estimation of total usual calcium and vitamin D intakes in the United States. J. Nutr. 2010, 140, 817–822. [Google Scholar] [CrossRef] [PubMed]
- Vatanparast, H.; Calvo, M.S.; Green, T.J.; Whiting, S.J. Despite mandatory fortification of staple foods, vitamin D intakes of Canadian children and adults are inadequate. J. Steroid Biochem. Mol. Biol. 2010, 121, 301–303. [Google Scholar] [CrossRef] [PubMed]
- Black, L.J.; Walton, J.; Flynn, A.; Cashman, K.D.; Kiely, M. Small increments in vitamin D intake by Irish adults over a decade show that strategic initiatives to fortify the food supply are needed. J. Nutr. 2015, 145, 969–976. [Google Scholar] [CrossRef] [PubMed]
- Shrapnel, W.; Truswell, S. Vitamin D deficiency in Australia and New Zealand: What are the dietary options? Nutr. Diet. 2006, 63, 206–212. [Google Scholar] [CrossRef]
- Liu, J.; Arcot, J.; Cunningham, J.; Greenfield, H.; Hsu, J.; Padula, D.; Strobel, N.; Fraser, D.R. New data for vitamin D in australian foods of animal origin: Impact on estimates of national adult vitamin D intakes in 1995 and 2011–13. Asia Pac. J. Clin. Nutr. 2015, 24, 464–471. [Google Scholar] [PubMed]
- Margulis, L.; Chapman, M.J. Kingdoms and Domains: An Illustrated Guide to the Phyla of Life on Earth; Academic Press: Cambridge, MA, USA, 2010. [Google Scholar]
- Weete, J.D.; Abril, M.; Blackwell, M. Phylogenetic distribution of fungal sterols. PLoS ONE 2010, 5, e10899. [Google Scholar] [CrossRef] [PubMed]
- Quackenbush, F.W.; Peterson, W.H.; Steenbock, H. A study of the nutritive value of mushrooms. J. Nutr. 1935, 10, 625–643. [Google Scholar] [CrossRef]
- Jasinghe, V.J.; Perera, C.O.; Sablini, S.S. Kinetics of the conversion of ergosterol in edible mushrooms. J. Food Eng. 2007, 79, 864–869. [Google Scholar] [CrossRef]
- Mattila, P.H.; Piironen, V.I.; Uusi-Rauva, E.J.; Koivistoinen, P.E. Vitamin D contents in edible mushrooms. J. Agric. Food Chem. 1994, 42, 2449–2453. [Google Scholar] [CrossRef]
- Teichmann, A.; Dutta, P.C.; Staffas, A.; Jägerstad, M. Sterol and vitamin D2 concentrations in cultivated and wild grown mushrooms: Effects of UV irradiation. LWT-Food Sci. Technol. 2007, 40, 815–822. [Google Scholar] [CrossRef]
- Kristensen, H.L.; Rosenqvist, E.; Jakobsen, J. Increase of vitamin D2 by UV-B exposure during the growth phase of white button mushroom (Agaricus bisporus). Food Nutr. Res. 2012, 56, 7114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koyyalamudi, S.R.; Jeong, S.C.; Song, C.H.; Cho, K.Y.; Pang, G. Vitamin D2 formation and bioavailability from Agaricus bisporus button mushrooms treated with ultraviolet irradiation. J. Agric. Food Chem. 2009, 57, 3351–3355. [Google Scholar] [CrossRef] [PubMed]
- Phillips, K.M.; Ruggio, D.M.; Horst, R.L.; Minor, B.; Simon, R.R.; Feeney, M.J.; Byrdwell, W.C.; Haytowitz, D.B. Vitamin D and sterol composition of 10 types of mushrooms from retail suppliers in the United States. J. Agric. Food Chem. 2011, 59, 7841–7853. [Google Scholar] [CrossRef] [PubMed]
- United States Department of Agriculture, USDA Food Composition Database. Available online: https://ndb.nal.usda.gov/ndb/ (accessed on 11 October 2018).
- Phillips, K.M.; Rasor, A.S. A nutritionally meaningful increase in vitamin D in retail mushrooms is attainable by exposure to sunlight prior to consumption. J. Nutr. Food Sci. 2013, 3, 1. [Google Scholar]
- Urbain, P.; Jakobsen, J. Dose-response effect of sunlight on vitamin D2 production in Agaricus bisporus mushrooms. J. Agric. Food Chem. 2015, 63, 8156–8161. [Google Scholar] [CrossRef] [PubMed]
- Koyyalamudi, S.R.; Jeong, S.C.; Pang, G.; Teal, A.; Biggs, T. Concentration of vitamin D2 in white button mushrooms (Agaricus bisporus) exposed to pulsed UV light. J. Food Compos. Anal. 2011, 24, 976–979. [Google Scholar] [CrossRef]
- Kalaras, M.D.; Beelman, R.B.; Elias, R.J. Effects of postharvest pulsed UV light treatment of white button mushrooms (Agaricus bisporus) on vitamin D2 content and quality attributes. J. Agric. Food Chem 2012, 60, 220–225. [Google Scholar] [CrossRef] [PubMed]
- Jasinghe, V.J.; Perera, C.O. Ultraviolet irradiation: The generator of vitamin D2 in edible mushrooms. Food Chem. 2006, 95, 638–643. [Google Scholar] [CrossRef]
- Ko, J.A.; Lee, B.H.; Lee, J.S.; Park, H.J. Effect of UV-B exposure on the concentration of vitamin D2 in sliced shiitake mushroom (Lentinus edodes) and white button mushroom (Agaricus bisporus). J. Agric. Food Chem. 2008, 56, 3671–3674. [Google Scholar] [CrossRef] [PubMed]
- Wittig, M.; Krings, U.; Berger, R.G. Single-run analysis of vitamin D photoproducts in oyster mushroom (Pleurotus ostreatus) after UV-B treatment. J. Food Compos. Anal. 2013, 31, 266–274. [Google Scholar] [CrossRef]
- Jasinghe, V.J.; Perera, C.O. Distribution of ergosterol in different tissues of mushrooms and its effect on the conversion of ergosterol to vitamin D2 by UV irradiation. Food Chem. 2005, 92, 541–546. [Google Scholar] [CrossRef]
- Jasinghe, V.J.; Perera, C.O.; Barlow, P.J. Vitamin D2 from irradiated mushrooms significantly increases femur bone mineral density in rats. J. Toxicol. Environ. Health 2006, 69, 1979–1985. [Google Scholar] [CrossRef] [PubMed]
- Huang, G.; Cai, W.; Xu, B. Vitamin D2, ergosterol, and vitamin B2 content in commercially dried mushrooms marketed in China and increased vitamin D2 content following UV-C irradiation. Int. J. Vitam. Nutr. Res. 2016, 1, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Guan, W.; Zhang, J.; Yan, R.; Shao, S.; Zhou, T.; Lei, J.; Wang, Z. Effects of UV-C treatment and cold storage on ergosterol and vitamin D2 contents in different parts of white and brown mushroom (Agaricus bisporus). Food Chem. 2016, 210, 129–134. [Google Scholar] [CrossRef] [PubMed]
- Perera, C.O.; Jasinghe, V.J.; Ng, F.L.; Mujumdar, A.S. The effect of moisture content on the conversion of ergosterol to vitamin D in shiitake mushrooms. Dry. Technol. 2003, 21, 1091–1099. [Google Scholar] [CrossRef]
- Krings, U.; Berger, R.G. Dynamics of sterols and fatty acids during UV-B treatment of oyster mushroom. Food Chem. 2014, 149, 10–14. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.J.; Ahn, B.Y. Statistical optimization of ultraviolet irradiate conditions for vitamin D2 synthesis in oyster mushrooms Pleurotus ostreatus) using response surface methodology. PLoS ONE 2014, 9, e95359. [Google Scholar] [CrossRef] [PubMed]
- Rangel-Castro, J.I.; Staffas, A.; Danell, E. The ergocalciferol content of dried pigmented and albino Cantharellus cibarius fruit bodies. Mycol. Res. 2002, 106, 70–73. [Google Scholar] [CrossRef]
- Nölle, N.; Argyropoulos, D.; Müller, J.; Biesalski, H.K. Temperature stability of vitamin D2 and color changes during drying of UVB-treated mushrooms. Dry. Technol. 2018, 36, 307–315. [Google Scholar] [CrossRef]
- Slawińska, A.; Fornal, E.; Radzki, W.; Skrzypczak, K.; Zalewska-Korona, M.; Michalak-Majewska, M.; Parfieniuk, E.; Stachniuk, A. Study on vitamin D2 stability in dried mushrooms during drying and storage. Food Chem. 2016, 199, 203–209. [Google Scholar] [CrossRef] [PubMed]
- Lee, N.K.; Aan, B.Y. Optimization of ergosterol to vitamin D2 synthesis in Agaricus bisporus powder using ultraviolet-B radiation. Food Sci. Biotechnol. 2016, 25, 1627–1631. [Google Scholar] [CrossRef] [PubMed]
- Chien, R.C.; Yang, S.C.; Lin, L.M.; Mau, J.L. Anti-inflammatory and antioxidant properties of pulsed light irradiated Lentinula edodes. J. Food Process. Preserv. 2017, 41, e13045. [Google Scholar] [CrossRef]
- Roberts, J.S.; Teichert, A.; McHugh, T.H. Vitamin D2 formation from post-harvest UV-B treatment of mushrooms (Agaricus bisporus) and retention during storage. J. Agric. Food Chem. 2008, 56, 4541–4544. [Google Scholar] [CrossRef] [PubMed]
- Slawińska, A.; Fornal, E.; Radzki, W.; Jablonska-Rys, E.; Parfieniuk, E. Vitamin D2 stability during the refrigerated storage of ultraviolet B-treated cultivated culinary-medicinal mushrooms. Int. J. Med. Mushrooms 2017, 19, 249–255. [Google Scholar] [CrossRef] [PubMed]
- Mattila, P.; Ronkainen, R.; Lehikoinen, K.; Piironen, V. Effect of household cooking on the vitamin D content in fish, eggs, and wild mushrooms. J. Food Compos. Anal. 1999, 12, 153–160. [Google Scholar] [CrossRef]
- Ložnjak, P.; Jakobsen, J. Stability of vitamin D3 and vitamin D2 in oil, fish and mushrooms after house-hold cooking. Food Chem. 2018, 254, 144–149. [Google Scholar] [CrossRef] [PubMed]
- Outila, T.A.; Mattila, P.H.; Piironen, V.I.; Lamberg-Allardt, C.J.E. Bioavailability of vitamin D from wild edible mushrooms (Cantharellus tubaeformis) as measured with a human bioassay. Am. J. Clin. Nutr. 1999, 69, 95–98. [Google Scholar] [CrossRef] [PubMed]
- Jasinghe, V.J.; Perera, C.O.; Barlow, P.J. Bioavailability of vitamin D2 from irradiated mushrooms: An in vivo study. Br. J. Nutr. 2005, 93, 951–955. [Google Scholar] [CrossRef] [PubMed]
- Calvo, M.S.; Babu, U.S.; Garthoff, L.H.; Woods, T.O.; Dreher, M.; Hill, G.; Nagaraja, S. Vitamin D2 from light-exposed edible mushrooms is safe, bioavailable and effectively supports bone growth in rats. Osteoporos. Int. 2013, 24, 197–207. [Google Scholar] [CrossRef] [PubMed]
- Urbain, P.; Singler, F.; Ihorst, G.; Biesalski, H.K.; Bertz, H. Bioavailability of vitamin D2 from UV-B-irradiated button mushrooms in healthy adults deficient in serum 25-hydroxyvitamin D: A randomized controlled trial. Eur. J. Clin. Nutr. 2011, 65, 965–971. [Google Scholar] [CrossRef] [PubMed]
- Stephensen, C.B.; Zerofsky, M.; Burnett, D.J.; Lin, Y.; Hammock, B.D.; Hall, L.M.; McHugh, T. Ergocalciferol from mushrooms or supplements consumed with a standard meal increases 25-hydroxyergocalciferol but decreases 25-hydroxycholecalciferol in the serum of healthy adults. J. Nutr. 2012, 142, 1246–1252. [Google Scholar] [CrossRef] [PubMed]
- Stepien, M.; O’Mahony, L.; O’Sullivan, A.; Collier, J.; Fraser, W.D.; Gibney, M.J.; Nugent, A.P.; Brennan, L. Effect of supplementation with vitamin D2-enhanced mushrooms on vitamin D status in healthy adults. J. Nutr. Sci. 2013, 2, e29. [Google Scholar] [PubMed]
- Mehrotra, A.; Calvo, M.S.; Beelman, R.B.; Levy, E.; Siuty, J.; Kalaras, M.D.; Uribarri, J. Bioavailability of vitamin D2 from enriched mushrooms in prediabetic adults: A randomized controlled trial. Eur. J. Clin. Nutr. 2014, 68, 1154–1160. [Google Scholar] [CrossRef] [PubMed]
- Lee, G.; Byun, H.; Yoon, K.; Choi, K.; Jeung, E. Dietary calcium and vitamin D2 supplementation with enhanced Lentinula edodes improves osteoporosis-like symptoms and induces duodenal and renal active calcium transport gene expression in mice. Eur. J. Nutr. 2009, 48, 75–83. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.Y.; Yu, H.T.; Kao, J.P.; Yang, C.C.; Chiang, S.S.; Mishchuk, D.O.; Mau, J.L.; Slupsky, C.M. Consumption of vitamin D2 enhanced mushrooms is associated with improved bone health. J. Nutr. Biochem. 2015, 26, 696–703. [Google Scholar] [CrossRef] [PubMed]
- Wilson, L.R.; Tripkovic, L.; Hart, K.H.; Lanham-New, S.A. Vitamin D deficiency as a public health issue: Using vitamin D2 or vitamin D3 in future fortification strategies. Proc. Nutr. Soc. 2017, 76, 392–399. [Google Scholar] [CrossRef] [PubMed]
- Tripkovic, L.; Wilson, L.R.; Hart, K.H.; Johnsen, S.; de Lusignan, S.; Smith, C.P.; Bucca, G.; Penson, S.; Chope, G.; Elliot, R.; et al. Daily supplementation with 15 μg vitamin D2 compared with vitamin D3 to increase wintertime 25-hydroxyvitamin D status in healthy South Asian and white European women: A 12-wk randomized, placebo-controlled food-fortification trial. Am. J. Clin. Nutr. 2017, 106, 481–490. [Google Scholar] [CrossRef] [PubMed]
- Feeney, M.J.; Miller, A.M.; Roupas, P. Mushrooms-biologically distinct and nutritionally unique. Nutr. Today 2014, 49, 301–307. [Google Scholar] [CrossRef] [PubMed]
- McCance and Widdowson’s Composition of Food Integrated Dataset; Institute of Food Research, Public Health England: London, UK, 2015.
Age (Years) | |||||
---|---|---|---|---|---|
1–18 | 19–30 | 31–50 | 51–70 | 71+ | |
United States of America a | 15 | 15 | 15 | 15 | 20 |
Canada b | 15 | 15 | 15 | 15 | 20 |
United Kingdom c | 10 | 10 | 10 | 10 | 10 |
Europe d | 15 | 15 | 15 | 15 | 15 |
Australia and New Zealand e | 5 | 5 | 5 | 10 | 15 |
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Cardwell, G.; Bornman, J.F.; James, A.P.; Black, L.J. A Review of Mushrooms as a Potential Source of Dietary Vitamin D. Nutrients 2018, 10, 1498. https://doi.org/10.3390/nu10101498
Cardwell G, Bornman JF, James AP, Black LJ. A Review of Mushrooms as a Potential Source of Dietary Vitamin D. Nutrients. 2018; 10(10):1498. https://doi.org/10.3390/nu10101498
Chicago/Turabian StyleCardwell, Glenn, Janet F. Bornman, Anthony P. James, and Lucinda J. Black. 2018. "A Review of Mushrooms as a Potential Source of Dietary Vitamin D" Nutrients 10, no. 10: 1498. https://doi.org/10.3390/nu10101498
APA StyleCardwell, G., Bornman, J. F., James, A. P., & Black, L. J. (2018). A Review of Mushrooms as a Potential Source of Dietary Vitamin D. Nutrients, 10(10), 1498. https://doi.org/10.3390/nu10101498