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Review of Agaricus Bisporus: White Button, Creminis, and Portobello Mushrooms

James Odell, OMD, ND, L.Ac.

Edible mushrooms are one of the most valuable and least expensive sources of beneficial nutrients, and medicinal compounds in the world.1 More than 2000 species of mushrooms exist in nature; however, less than 25 species are widely accepted as foods. Among the various mushrooms, the button mushroom and mature portabella (Agaricus Bisporus) are the most common and cultivated worldwide. The fungal genus Agaricus as late as 2008 was believed to contain about 200 species worldwide but since then, molecular phylogenetic studies have revalidated several disputed species, as well as resolved some species complexes, and aided in the discovery and description of a wide range of mostly tropical species that were formerly unknown to science.


When immature, Agaricus bisporus is the small button mushroom that we commonly see in produce markets. It has two color states – white and brown – both of which have various names, with additional names for the mature state. When fully mature it grows and develops a brown cap measuring up to 5-10 centimeters. Its mature form is known as the portobello. Creminis, sometimes called "baby bellas", are sized in between button mushrooms and portabellas. Mushroom growers in different parts of the world sell these under different names, but portobello mushroom is the most common name.


Agaricus bisporus is popular not only because of its delicious taste, but also due to its high level of nutrients: dietary fiber, essential and semi-essential amino acids, unsaturated fatty acids including linoleic and linolenic acids, easily digestible proteins, sterols, phenolic and indole compounds, vitamins − especially provitamin D2 and B1, B2, B6, B7, and C, and minerals - phosphorus, potassium, selenium, and copper. Like many mushrooms, its ergocalciferol (vitamin D2) content increases substantially after exposure to UV light. Agaricus bisporus is low in carbohydrates and for this reason, they can be included in the diabetic diet.


Agaricus bisporus also contains conjugated linoleic acid (CLA), a beneficial fatty acid. They are one of the only plant/non-meat sources of CLA, making them unique and valuable in vegetarian diets. Additionally, they are a rich source of selenium, zinc, and other elements such as magnesium, copper, iron, potassium, sodium, calcium, phosphorus, sulfur, and manganese. The presence of these compounds and elements with biological activity in fruiting bodies of Agaricus bisporus confirms their unique nutraceutical and medicinal properties.


The high nutritional value of button mushrooms and portabellas, along with their good flavor, has greatly increased the demand for this mushroom species. In the U.S., the white button form of Agaricus Bisporus alone accounts for about 90% of mushrooms sold.


Recently, studies have demonstrated the presence of other potentially bioactive compounds particularly glucans and terpenes. However, some still consider Agaricus Bisporus to be of lesser medicinal value than the other mushrooms grown predominantly in Asia, such as shiitake (Lentinula edodes), maitake (Grifola frondose), lion’s mane (Hericium erinaceus), oyster mushrooms (Pleurotus ostreatus), etc. However, this is not necessarily true.


Medicinal Properties


Agaricus Bisporus has a long traditional history of use not only as a culinary mushroom but also as a medicinal mushroom. Agaricus Bisporus extracts and/or their bioactive compounds have been identified as possessing antioxidant, antibacterial, anti-inflammatory, antidiabetic, antitumor, and immunomodulatory activity.2, 3, 4, 5


Toxicity and Side Effects


Agaricus bisporus has been consumed for centuries, if not millennia, with no reported severe adverse effects. Although there have been relatively few direct intervention trials of Agaricus bisporus mushroom consumption in humans, those that have been completed to date indicate that these mushrooms and their extracts are generally well-tolerated with few, if any, side effects.6

A 2018 toxicological study of Agaricus Bisporous Aqueous Enzymatic Extracts (AbAEE) in rats demonstrated that “AbAEE cannot be classified for its acute toxicity, as it did not cause either lethality or adverse changes in the general behavior of the animals when the highest dose (5000 mg/kg) was administrated orally.”7


However, it is known that the Agaricus genus, including the species Agaricus Bisporus (button mushroom, cremini, and portabella), is occasionally reported to cause adverse gastrointestinal symptoms (diarrhea, vomiting, cramps, nausea) in some individuals acting 1–2 hours after consumption. This adverse effect may be somewhat related to consuming them in a raw state and can be avoided if they are cooked.


Toxic Agaritine Presence in Agaricus Bisporus

Agaritine, a water-soluble γ-glutamyl-hydroxymethyl-phenyl hydrazine or simply hydrazine toxin closely related to gyromitrin is present along with metabolites including diazonium ions and free radicals, in many Agaricus species.8 Fortunately, these hydrazines are heat unstable, so the good news is if you cook them well, then most hydrazines are destroyed and the mushrooms usually present no problem. If you do not cook them well, then these hydrazines may be potentially problematic. Thus, consumers should cook the button and portobello mushrooms before consuming them because they contain potentially toxic hydrazines. Also, because the concentration of hydrazine in button mushrooms decreases with the age of the mushroom, a button or cremini will have more of it than a portobello.

An agaritine risk assessment analysis was done in 2010 by an Australian team.9 They concluded that agaritine from the consumption of cultivated Agaricus Bisporus mushrooms poses no known toxicological risk to healthy humans. However, this assertion was mainly based on studies on patient groups having different diseases, in clinical trials lasting up to one year and using other mushroom species than Agaricus Bisporus, so it is not very relevant for the estimation of potential toxicity or cancer risk resulting from consumption of Agaricus Bisporus. In short, cooking them well is the best and safest way to prepare this mushroom.


Agaricus Bisporus Antioxidant Properties


Total phenolics and antioxidant properties of Agaricus Bisporus have been reported by many authors.10, 11, 12, 13, 14, 15, 16 Interestingly, Agaricus Bisporus, especially portabellas, had higher antioxidant capacity relative to Lentinula edodes, Pleurotus ostreatus, Pleurotus eryngii, and Grifola frondosa.17


Phenolic compounds in the ethanolic extract of Agaricus Bisporus suggest that the ethanolic extract of this mushroom had a potent antioxidant effect and could be explored as a novel natural antioxidant. Phenolic compounds have been reported as the major antioxidant components in mushrooms.18 A close relationship between antioxidant activity and phenolic contents suggests that phenolic compounds could be the foremost contributors to the antioxidant activity of this mushroom.19 The presence of antioxidant ergothioneine in Agaricus Bisporus (which also displays antimutagenic, chemo- and radioprotective activity) is also noteworthy.


Agaricus Bisporus Anticancerous Properties


White button mushrooms are a widely consumed food containing phytochemicals beneficial to cancer prevention. Glucan polysaccharides are highly anti-cancerous and immune-modulatory. Agaricus Bisporus contain three main medicinal polysaccharides α- glucan, β-glucan, and galactomannan20, and galactomannan is the main polysaccharide with 55.8%.21 The most common glucans extracted from Agaricus Bisporus are (1→3), (1→6)-d-glucans. On the other hand, unlike other medicinal mushrooms, Agaricus Bisporus does not present very high β-glucan content.22


Agaricus Bisporus exhibits health benefits for improving mucosal immunity. The dietary intake of A. bisporus significantly accelerates secretory immunoglobulin-A secretion.23, 24 Also, Agaricus Bisporus extracts express an immunostimulating effect on activated human peripheral blood mononuclear cells (PBMCs) and induce synthesis of interferon-gamma (IFN-γ) which are both strongly immune enhancing.25 Lastly, extracts from Agaricus Bisporus have been shown to inhibit cell proliferation of HL-60 leukemia cells and other leukemia human cell lines via the induction of apoptosis.26


Agaricus Bisporus Inhibits Aromatase


Numerous studies indicate that Agaricus bisporus suppresses aromatase and thus can decrease the risk of breast cancer and other estrogen-related cancers. As a natural aromatase inhibitor, it prevents the breakdown of testosterone into estrogen. It is shown that an inhibition of aromatase activity and subsequent reduction of estrogen using Agaricus bisporus provide a physiologically suitable mechanism for influents on estrogen receptor-positive tumors.27, 28, 29 Moreover, Agaricus Bisporus contains a high amount of lovastatin.30 Yang et al. (2016) demonstrated that lovastatin exerts anti-cancer effects in the triple-negative breast cancer cell line MDA-MB-231.31


Agaricus Bisporus Antimicrobial Properties


Studies show that the extracts of Agaricus Bisporus prepared with methyl alcohol revealed antimicrobial activities against some bacteria, yeasts, and dermatophytes.32, 33, 34, 35 There is a need for further studies to isolate and characterize the antibacterial moieties in this fungus for practical disease control measures.


Conclusion


Mushrooms have been recognized as important food items since ancient times because of their nutritional value and therapeutic properties. There is an increasing interest in extracting bioactive ingredients from mushrooms for developing functional foods and medicine. Agaricus Bisporus has a very long history of cross-cultural use in many traditional therapies. As such, this species may provide significant support against malnutrition due to its high nutritional values, especially in developing and undeveloped countries. Consumption of Agaricus Bisporus also has proven medicinal benefits as an anticancer, antidiabetic, antioxidant, and antimicrobial.


However, its toxicity profile indicates that this species should be not only washed well before preparation but should be thoroughly cooked before consumption. Heat appears to destroy the hydrazine toxin that may be present in this mushroom. Actually, many common mushrooms have elevated levels of hydrazine in them and should be cooked thoroughly before eating.

Certainly, most investigations have shown that the nutraceutical and medicinal value of Agaricus Bisporus are a promising source of new therapeutics against many life-threatening diseases.

References:

1. Bilal, Ahmad Wani. "Nutritional and medicinal importance of mushrooms." Journal of Medicinal Plants Research 4, no. 24 (2010): 2598-2604.

2. Dhamodharan, G., Mirunalini, S. (2010). A novel medicinal characterization of Agaricus bisporus (white button mushroom). Pharmacologyonline, 2, 456-463.

3. Adams, Lynn S., Shiuan Chen, Sheryl Phung, Xiwei Wu, and Lui Ki. "White button mushroom (Agaricus bisporus) exhibits antiproliferative and proapoptotic properties and inhibits prostate tumor growth in athymic mice." Nutrition and cancer 60, no. 6 (2008): 744-756.

4. Dhamodharan, G., Mirunalini, S. (2012). Dose response study of Agaricus bisporus (White button mushroom) and its encapsulated chitosan nanoparticles against 7,12 Dimethylbenz(a)anthracene induced mammary carcinogenesis in female Sprague-dawley rats. International Journal of Pharmacy and Pharmaceutical Sciences, 4(4), 348-354.

5. Jeong, Sang Chul, Yong Tae Jeong, Byung Keun Yang, Rezuanul Islam, Sundar Rao Koyyalamudi, Gerald Pang, Kai Yip Cho, and Chi Hyun Song. "White button mushroom (Agaricus bisporus) lowers blood glucose and cholesterol levels in diabetic and hypercholesterolemic rats." Nutrition research 30, no. 1 (2010): 49-56. https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=6e6745e4db1c306afbe727dd7b8071f4a26cb9e6

6. Volman, J.J., Mensink, R.P., van Griensven, L.J. & Plat, J. (2010). Effects of aglucans from Agaricus bisporus on ex vivo cytokine production by LPS and PHA-stimulated PBMCs; a placebo-controlled study in slightly hypercholesterolemic subjects. European Journal of Clinical Nutrition,64, 720– 726. https://doi.org/10.1038/ejcn.2010.32

7. Carbonero Aguilar, María del Pilar, Gonzalo Falcón García, Paloma Gallego Yerga, J. A. del Campo, Isabel María Moreno Navarro, and Juan Dionisio Bautista Palomas. "Preliminary Studies of the Toxicity of Agaricus Bisporous Aqueous Enzymatic Extracts (AbAEE) In Rats." Journal of Toxins, 5 (1), 1-7. (2018).

8. Lagrange, Emmeline, and Jean-Paul Vernoux. "Warning on false or true morels and button mushrooms with potential toxicity linked to hydrazinic toxins: an update." Toxins 12, no. 8 (2020): 482.

9. Roupas, P.; Keogh, J.; Noakes,M.; Margetts, C.; Taylor, P. Mushrooms and agaritine: Amini-review. J. Funct. Foods 2010, 2, 91–98.

10. Czapski, Janusz. "Antioxidant activity and phenolic content in some strains of mushrooms (Agaricus bisporus)." Veg Crops Res Bull 62 (2004): 165-173. https://library.wur.nl/WebQuery/wurpubs/fulltext/27701#page=164

11. Tsai, Shu-Yao, Tsai-Ping Wu, Shih-Jeng Huang, and Jeng-Leun Mau. "Antioxidant properties of ethanolic extracts from culinary-medicinal button mushroom Agaricus bisporus (J. Lange) Imbach (Agaricomycetideae) harvested at different stages of maturity." International Journal of Medicinal Mushrooms 10, no. 2 (2008). https://www.researchgate.net/profile/Jeng-Leun-Mau/publication/240299771_Antioxidant_Properties_of_Ethanolic_Extracts_from_Culinary-Medicinal_Button_Mushroom_Agaricus_bisporus_J_Lange_Imbach_Agaricomycetideae_Harvested_at_Different_Stages_of_Maturity/links/0f31752ff79897c3ae000000/Antioxidant-Properties-of-Ethanolic-Extracts-from-Culinary-Medicinal-Button-Mushroom-Agaricus-bisporus-J-Lange-Imbach-Agaricomycetideae-Harvested-at-Different-Stages-of-Maturity.pdf

12. Liu, Jun, Liang Jia, Juan Kan, and Chang-hai Jin. "In vitro and in vivo antioxidant activity of ethanolic extract of white button mushroom (Agaricus bisporus)." Food and chemical toxicology 51 (2013): 310-316. https://www.sciencedirect.com/science/article/abs/pii/S027869151200751X

13. Ramírez-Anguiano, A.C., Santoyo, S., Reglero, G. & Soler-Rivas, C. (2007). Radical scavenging activities, endogenous oxidative enzymes and total phenols in edible mushrooms commonly consumed in Europe. Journal of the Science of Food and Agriculture, 87, 2272–2278. https://doi.org/10.1002/jsfa.2983

14. Savoie, J.M., Minvielle, N., Largeteau, M.L. (2008). Radical-scavenging properties of extracts from the white button mushroom, Agaricus bisporus. Journal of Science of Food and Agriculture, 88(6), 970–975. https://doi.org/10.1002/jsfa.3175

15. Barros, L., Cruz, T., Baptista, P., Estevinho, L.M. & Ferreira, I.C.F.R. (2008). Wild and commercial mushrooms as source of nutrients and nutraceuticals. Food and Chemical Toxicology, 46, 2743-2747. https://doi.org/10.1016/j.fct.2008.04.030

16. Savoie, Jean‐Michel, Nathalie Minvielle, and Michele L. Largeteau. "Radical‐scavenging properties of extracts from the white button mushroom, Agaricus bisporus." Journal of the Science of Food and Agriculture 88, no. 6 (2008): 970-975. https://www.researchgate.net/profile/Jean-Michel-Savoie/publication/229729702_Radical-scavenging_properties_of_extracts_from_the_white_button_mushroom_Agaricus_bisporus/links/5a8a899c0f7e9b1a95546f85/Radical-scavenging-properties-of-extracts-from-the-white-button-mushroom-Agaricus-bisporus.pdf

17. Liu, J., Jia, L., Kan, J. & Jin, C. (2013). In vitro and in vivo antioxidant activity of ethanolic extract of white button mushroom (Agaricus bisporus). Food and Chemical Toxicology, 51, 310–316. https://doi.org/10.1016/j.fct.2012.10.014

18. Barros, L., Cruz, T., Baptista, P., Estevinho, L.M. & Ferreira, I.C.F.R. (2008). Wild and commercial mushrooms as source of nutrients and nutraceuticals. Food and Chemical Toxicology, 46, 2743-2747. https://doi.org/10.1016/j.fct.2008.04.030

19. Guo, Y.J., Deng, G.F., Xu, X.R., Wu, S., Li, S. & Xia, E.Q. (2012). Antioxidant capacities, phenolic compounds and polysaccharide contents of 49 edible macrofungi. Food and Function, 3, 1195–1205. https://doi.org/10.1039/c2fo30110e .

20. Smiderle, F.R., Ruthes, A.C., Van Arkel, J., Chanput, W., Lacomin, M., Wichers, H.J. & Van Griensven, L.J.L.D. (2011). Polysaccharides from Agaricus bisporus and Agaricus brasiliensis show similarities in their structures and their immunomodulatory effects on human monocytic THP-1 cells. BMC Complementary and Alternative Medicine, 11, 58. https://doi.org/10.1186/1472-6882-11-58

21. Smiderle, F.R., Alquini, G., Tadra-Sfeir, M.Z., Iacomini, M., Wichers, H.J. & Van Griensven, L.J..LD. (2013). Agaricus bisporus and Agaricus brasiliensis (1 → 6)-β-d-glucans show immunostimulatory activity on human THP-1 derived macrophages. Carbohydrate Polymers, 94, 91−99. https://doi.org/10.1016/j.carbpol.2012.12.073

22. McCleary, B.V., Draga, A. (2016). Measurement of β-glucan in mushrooms and mycelial products. Journal of AOAC International, 99(2), 364-373. https://doi.org/10.5740/jaoacint.15-0289

23. Jeong, S.C., Koyyalamudi, S,R. & Pan, G. (2012). Dietary intake of Agaricus bisporus white button mushroom accelerates salivary immunoglobulin A secretion in healthy volunteers. Nutrition, 28, 527–531. https://doi.org/10.3329/jdnmch.v18i1.12243.

24. Smiderle, Fhernanda R., Giovana Alquini, Michelle Z. Tadra-Sfeir, Marcello Iacomini, Harry J. Wichers, and Leo JLD Van Griensven. "Agaricus bisporus and Agaricus brasiliensis (1→ 6)-β-d-glucans show immunostimulatory activity on human THP-1 derived macrophages." Carbohydrate polymers 94, no. 1 (2013): 91-99. https://d1wqtxts1xzle7.cloudfront.net/43915271/Agaricus_bisporus_and_Agaricus_brasilien20160320-10245-7lr52q-libre.pdf?1458470794=&response-content-disposition=inline%3B+filename%3DAgaricus_bisporus_and_Agaricus_brasilien.pdf&Expires=1673018226&Signature=Gq-Meaqo8thcya0zat0Ymg5aqVnAGAxPrdeYp82CL6sRKRSpQIepAvE-eOvf~bXb8X7-nxOjXcBnqPEbgyOaKDKU7dG62qZEJGjW8ognsuVgh8j2gKdl7nxzxXsBXxly1~OM-4zbqjXaZFxKQIiycLpU4rF45LiirDcY-CzZJbCEdZir~fXYtFoAo93r46fJ6MGURiZ-EMvpe6SkkYmjdZomvhwQQOztiZjpqXLAxhCT5BGDwML9KCU2kVD3Ok5CAaOnUqy3ZvjHx8rdBxXwTnC2ZTLtarKo-Zwr396IVFt4mFULYkgYmYBOqMo4R2ADgtF52H1Z6gPXKFyC6a5N4g__&Key-Pair-Id=APKAJLOHF5GGSLRBV4ZA

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26. Jagadishm L,K., Krishnan, V.V., Shenbhagaraman, R. & Kaviyarasan, V. (2009). Comparitive study on the antioxidant, anticancer and antimicrobial property of Agaricus bisporus (J. E. Lange) Imbach before and after boiling. African Journal of Biotechnology, 8(4), 654-661.

27. Chen, Shiuan, Sei-Ryang Oh, Sheryl Phung, Gene Hur, Jing Jing Ye, Sum Ling Kwok, Gayle E. Shrode, Martha Belury, Lynn S. Adams, and Dudley Williams. "Anti-aromatase activity of phytochemicals in white button mushrooms (Agaricus bisporus)." Cancer research 66, no. 24 (2006): 12026-12034. https://www.researchgate.net/profile/Martha-Belury/publication/6621136_Anti-Aromatase_Activity_of_Phytochemicals_in_White_Button_Mushrooms_Agaricus_bisporus/links/0046352401ef392fcf000000/Anti-Aromatase-Activity-of-Phytochemicals-in-White-Button-Mushrooms-Agaricus-bisporus.pdf

28. Roupas, P., Keogh, J., Noakes, M., Margetts, C. & Taylor, P. 2012. The role of edible mushrooms in health: Evaluation of the evidence. Journal of Functional Foods, 4, 687-709. https://doi.org/10.1016/j.jff.2012.05.003

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30. Chen, Shin-Yu, Kung-Jui Ho, Yun-Jung Hsieh, Li-Ting Wang, and Jeng-Leun Mau. "Contents of lovastatin, γ-aminobutyric acid and ergothioneine in mushroom fruiting bodies and mycelia." Lwt 47, no. 2 (2012): 274-278.

31. Yang, Tao, Hui Yao, Guangchun He, Liujiang Song, Ning Liu, Yan Wang, Yingke Yang, Evan T. Keller, and Xiyun Deng. "Effects of lovastatin on MDA-MB-231 breast cancer cells: an antibody microarray analysis." Journal of Cancer 7, no. 2 (2016): 192. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4716852/

32. Abah, S.E., Abah, G. (2010). Antimicrobial and antioxidant potentials of Agaricus bisporus. Advances in Biological Research, 4(5): 277-282. Ahlavat, O.P., Manikandan, K. & Singh, M. (2016). Proximate composition of different mushroom varieties and effect of UV light exposure on vitamin D content in Agaricus bisporus and Volvariella volvacea. Mushroom Research, 25(1), 1-8.

33. Akyüz, M., Onganer, A.N., Erecevit, P. & Kirbağ, S. (2010). Antimicrobial Activity of some Edible Mushrooms in the Eastern and Southeast Anatolia Region of Turkey. Gazi University Journal of Science, 23(2), 125-130.

34. Ndungutse, V., Mereddy, R. & Sultanbawa, Y. 2015. Bioactive properities of mushroom (Agaricus bisporus) stipe extracts. Journal of Food Processing and Preservation, 39, 2225-2233. https://doi.org/10.1111/jfpp.12467 .

35. Tehrani, M.H.H., Fakhrehoseini, E., Nejad, M.K., Mehregan, H. & Hakemi-Vala, M. (2012). Search for proteins in the liquid extract of edible mushroom, Agaricus bisporus, and studying their antibacterial effects. Iranian Journal of Pharmaceutical Research, 11(1), 145- 150. https://doi.org/10.1016/j.foodchem.2006.10.073 .


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