Evaluation of Nutritional Composition, Antioxidant Activities and Anti-cancer Effect of Edible and Medicinal Mushroom Hericium erinaceus

Yıl 2023, Cilt: 13 Sayı: 4, 2622 - 2633, 01.12.2023

Özlem Erdal Altıntaş

https://doi.org/10.21597/jist.1309800

Öz

Mushrooms have attracted interest since ancient times due to their nutritional composition and medicinal properties. In recent years, the antioxidant compounds of mushroom extracts have become an source of alternative synthetic antioxidant substances in pharmaceutical and food industries. In this context, researchers have become increasingly interested in edible and medicinal mushrooms. The aim of this study was to determine the nutritional composition, antioxidant potential, phenolic and flavonoid content of commercially purchased Hericium erinaceus mushroom and to evaluate its anticancer effect against A549 (lung adenocarcinoma) and HT-29 (human colon adenocarcinoma) cells. In this context, the nutrient composition was analyzed according to the Association of Official Analytical Chemists (AOAC) procedure. Hericium erinaceus showed a high nutritional value with protein, carbohydrate, dietary fiber and glucan content. The total phenolic and total flavonoid contents of water, ethanol and methanol extracts of this mushroom were determined and it was found that the methanol extract had the highest phenolic (27.12±1.05 mg GAE/g extract) and flavonoid (13.48±1.13 mg QE/g extract) contents among the three extract types. In addition, the antioxidant capacity of the extracts was compared by different methods (DPPH, ABTS, FRAP and CUPRAC). Methanol extract showed the highest DPPH (38.88±1.59 µM TE/g extract), FRAP (21.44±0.79 µM TE/g extract) and CUPRAC (30.05±1.80 µM TE/g extract) activities among the other extracts, while ABTS (24.44±1.07 µM TE/g extract) activity was the highest for ethanol extract. Finally, when the anticancer effects of these extracts against A549 and HT-29 cells were evaluated, it was observed that water, ethanol and methanol extracts inhibited A549 cells by 49.08%, 52.08% and 57.91% and HT-29 cells by 52.82%, 63.71% and 71.07%, respectively, at the end of 24 hours.

Anahtar Kelimeler

• antioxidant, • anticancer activity, • nutritional composition, • phenolic content, • Hericium erinacues

Yenilebilir ve Tıbbi Mantar Hericium erinaceus’un Besin Bileşimi, Antioksidan Aktiviteleri ve Anti-kanser Etkisinin Değerlendirilmesi

Öz

Mantarlar antik çağlardan itibaren besin bileşimleri ve tıbbi özellikleri sayesinde ilgi görmektedir. Son yıllarda mantar ekstrelerinin antioksidan bileşikleri, ilaç ve gıda endüstrilerinde sentetik antioksidan maddelerin alternatif kaynağı haline gelmiştir. Bu kapsamda araştırmacılar yenilebilir ve tıbbi özellikteki mantarlarla daha fazla ilgilenmeye başlamışlardır. Bu araştırmanın amacı ise, ticari olarak satın alınan Hericium erinaceus mantarının besin bileşimi, antioksidan potansiyeli, fenolik ve flavonoid içeriğini ortaya çıkarmak ayrıca A549 (akciğer adenokarsinomu) HT-29 (insan kolon adenokarsinomu) hücrelerine karşı antikanser etkisini değerlendirmektir. Bu bağlamda, besin bileşimi Association of Official Analytical Chemists (AOAC) prosedürüne uygun olarak analiz edilmiştir. Hericium erinaceus protein, karbonhidrat, diyet lifi ve glukan içeriği ile yüksek bir besin değeri göstermiştir. Bu mantarın su, etanol ve metanol ekstrelerinin toplam fenolik ve toplam flavonoid içerikleri belirlenmiş ve metanol ekstresinin üç ekstre türü arasında en yüksek fenolik (27.12±1.05 mg GAE/ g ekstre) ve flavonoid (13.48±1.13 mg QE/g ekstre) içeriğe sahip olduğu bulunmuştur. Ayrıca, ekstrelerin antioksidan kapasitesi farklı yöntemlerle (DPPH, ABTS, FRAP ve CUPRAC) karşılaştırılmıştır. Metanol ekstresi diğer ekstreler arasında en yüksek DPPH (38.88±1.59 µM TE/g ekstre), FRAP (21.44±0.79 µM TE/g ekstre) ve CUPRAC (30.05±1.80 µM TE/g ekstre) aktivitelerini gösterirken, etanol ekstresi için ABTS (24.44±1.07 µM TE/g ekstre) aktivitesi en yüksek olarak belirlenmiştir. Son olarak, bu ekstrelerin A549 ve HT-29 hücrelerine karşı antikanser etkileri değerlendirildiğinde, 24 saatin sonunda su, etanol ve metanol ekstrelerinin A549 hücrelerini sırasıyla %49.08, %52.08 ve %57.91 oranında HT-29 hücrelerini ise %52.82, %63.71 ve %71.07 oranında inhibe ettiği gözlenmiştir.

Anahtar Kelimeler

antioksidan, antikanser aktivite, besin kompozisyonu, fenolik içerik, Hericium erinaceus

Kaynakça

• Abd Razak, D.L., Mohd Fadzil, N.H., Jamaluddin, A., Abd Rashid, N.Y., Sani, N.A. & Abdul Manan, M. (2019). Effects of Different Extracting Conditions on Anti-Tyrosinase and Antioxidant Activities of Schizophyllum Commune Fruit Bodies. Biocatalysis and Agricultural Biotechnology, 19, 101116. https://doi.org/10.1016/j.bcab.2019.101116
• Abdelshafy, A.M., Belwal, T., Liang, Z., Wang, L., Li, D., Luo, Z. & Li, L. (2022). A comprehensive review on phenolic compounds from edible mushrooms: Occurrence, biological activity, application and future prospective, Critical Reviews in Food Science and Nutrition, 62:22, 6204-6224.
• Ahmed, A.F., Mahmoud, G.A-E., Hefyz, M., Liu,Z. &Ma, C. (2023). Overview on the edible mushrooms in Egypt. Journal of Future Foods, 3(1), 8-15.
• Apak, R., Güçlü, K., Özyürek, M., & Karademir, S.E. (2004). A novel total antioxidant capacity index for dietary polyphenols, vitamin C and E, using their cupric ion reducing capability in the presence of neocuproine: The CUPRAC method. Journal of Agricultural and Food Chemistry, 52(26), 7970-7981.
• Assemie, A., & Abaya, G., (2022). The Effect of Edible Mushroom on Health and Their Biochemistry, International Journal of Microbiology, 2022(7), Article ID 8744788.
• Association of Official Analytical Chemists. (2012). Official Methods of Analysis, 19th edition, Washington, DC.
• Association of Official Analytical Chemists. (2017). Official Methods of Analysis, 18th edition, Arlington, VA, USA.
• Atila, F., Tuzel, Y., Fernández, J.A., Cano, A.F. & Sen, F. (2018). The effect of some agro– industrial wastes on yield, nutritional characteristics and antioxidant activities of Hericium erinaceus isolates. Scientia Horticulturae, 238, 246-254, https://doi.org/10.1016/j.scienta.2018.04.049
• Benzie, I.F.F., & Strain, J.J. (1996). The Ferric Reducing Ability of Plasma (FRAP) as a Measure of “Antioxidant Power”: The FRAP Assay. Analytical Biochemistry, 239(1), 70-76.
• Boa, E. (2004). Wild edible fungi. A global overview of their use and importance to people. Rome, Italy: Food and Agriculture Orga¬nization of the United Nations.
• Brand-Williams, W., Cuvelier, M.E., & Berset, C. (1995). Use of free radical method to evaluate antioxidant activity. LWT-Food Science and Technology, 28(1), 25-30.
• Chang, C., Yang, M., Wen, H., & Chern, J. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis, 10(3), 178-182
• Chen, S.N., Chang, C.S., Yang, M.F., Chen, S., Soni, M. & Mahadevan, B. (2022). Subchronic toxicity and genotoxicity studies of Hericium erinaceus β-glucan extract preparation, Current Research in Toxicology, 3, 100068, https://doi.org/10.1016/j.crtox.2022.100068
• Contato, A.G., Inácio, F.D., de Araújo, C.A.V., Brugnari, T., Maciel, G.M., Haminiuk, C.W.I., Bracht, A., Peralta, R.M. & de Souza, C.G.M. (2020). Comparison between the aqueous extracts of mycelium and basidioma of the edible mushroom Pleurotus pulmonarius: chemical composition and antioxidant analysis. Food Measure, 14, 830–837.
• Darmasıwı, S., Aramsırırujıwet, Y. & Kımkong, I. (2022). Biological activities and chemical profile of Hericium erinaceus mycelium cultivated on mixed red and white jasmine rice. Food Science and Technology, 42, e08022.
• Das, A.K., Nanda, P.K., Dandapat, P., Bandyopadhyay, S., Gullón, P., Sivaraman, G.K., McClements, D.J., Gullón, B., & Lorenzo, J.M. (2021). Edible mushrooms as functional ingredients for development of healthier and more sustainable muscle foods: A flexitarian approach. Molecules, 26(9), 2463.
• DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (19569. Colorimetric method for determination of sugars and related substances. Analytical Cehmistry, 28, 350-356. El Sheikha, A.F. & Hu, D-M. (2018). How to trace the geographic origin of mushrooms? Trends Food Science Technolgy 78, 292–303.
• Egwim, E.C., Elem, R.C., & Egwuche, R.U. (2011). Proximate composition, phytochemical screening and antioxidant activity of ten selected wild edible Nigerian mushrooms. Amerıcan Journal of Food And Nutrıtıon, 1(2), 89-94.
• Fogarasi, M., Diaconeasa, Z.M., Pop, C.R., Fogarasi, S., Semeniuc, C.A., Fărcaş, A.C., Țibulcă, D., Sălăgean, C.-D., Tofană, M. & Socaci, S.A. (2020). Elemental Composition, Antioxidant and Antibacterial Properties of Some Wild Edible Mushrooms from Romania. Agronomy, 10, 1972. https://doi.org/10.3390/agronomy10121972
• Friedman, M. (2015). Chemistry, Nutrition, and Health-Promoting Properties of Hericium erinaceus (Lion’s Mane) Mushroom Fruiting Bodies and Mycelia and Their Bioactive Compounds. Journal of Agricultural and Food Chemistry, 63, 7108–7123.
• Gamez-Meza, N., Noriega-Oriega-Rodriguez, J.A., Medina-Juarez, L.A., Ortega-Garcia, J., Cazarez-Casanova, R., & Angulo-Guerrero, O. (1999). Antioxidant activity in soybean oil of extracts from thompson grape bagasse. Journal of the American Oil Chemists' Society, 76, 14-45.
• Gong, P., Wang, S., Liu, M., Chen, F., Yang, W., Chang, X., Liu, N., Zhao, Y., Wang, J. & Chen, X. (2020). Extraction methods, chemical character¬izations and biological activities of mushroom polysaccharides: A mini-review. Carbohydrate Research, 494, 108037
• Grand View Research. Mushroom market size & trends analysis report, 2021–2028. Accessed 10 Dec 2021. Available from: https://www.grandviewresearch.com/industry-analysis/mushroom-market
• Hassan, F.R.H. (2007). Cultivation of the Monkey Head Mushroom (Hericium erinaceus) in Egypt. Journal of Applied Sciences Research, 3(10), 1229-1233.
• Khan, M.A., Tania, M., Liu, R. & Rahman, M.M. (2013). Hericium erinaceus: An edible mushroom with medicinal values. Journal of Complementary and Integrative Medicine , 10, 253–258.
• Khodavirdipour, A., Zarean, R., & Safaralizadeh, R. (2021. Evaluation of the Anti-cancer Effect of Syzygium cumini Ethanolic Extract on HT-29 Colorectal Cell Line. Journal of Gastrointestinal Cancer, 52, 575-581.
• Koutrotsios, G., Larou, E., Mountzouris, K.C., Zervakis, G.I. (2016). Detoxification of Olive Mill Wastewater and Bioconversion of Olive Crop Residues into High-Value-Added Biomass by the Choice Edible Mushroom Hericium erinaceus. Applied Biochemistry and Biotechnology, 180(2),195-209.
• Kopylchuk, H.P., Voloshchuk, O. M. & Pasailiuk, M.V. (2023). Comparison of total amino acid compositions, total phenolic compounds, total flavonoid content, β-carotene content and hydroxyl radical scavenging activity in four wild edible mushrooms. Italian Journal of Mycology, 52, 112-125.
• Li, G., Yu, K., Li, F., Xu, K., Li, J., He, S., Cao, S. & Tan, G. (2014).Anticancer potential of Hericium erinaceus extracts against human gastrointestinal cancers. Journal of Ethnopharmacology, 153(2), 521-530. https://doi.org/10.1016/j.jep.2014.03.003
• Liu, T., Wang, N., Xu, X. & Wang, D. (2022). Effect of high quality dietary fiber of Hericium erinaceus on lowering blood lipid in hyperlipidemia mice. Journal of Future Foods, (2), 1, 61-68, https://doi.org/10.1016/j.jfutfo.2022.03.018
• Ma, B.J., Shen, J.W., Yu, H.Y., Ruan, Y., Wu, T.T. & Zhao, X. (2010). Hericenones and erinacines: Stimulators of nerve growth factor (NGF) biosynthesis in Hericium erinaceus. Mycology, 1, 92–98.
• Maity, P., Sen, I.K., Chakraborty, I., Mondal, S., Bar, H., Bhanja, S.K., Mandal, S. & Maity, G.N. (2021). Biologically active polysaccharide from edible mushrooms: A review. International Journal of Biological Macromolecules, 172, 408–417.
• Mori, K., Inatomi, S., Ouchi, K., Azumi, Y. & Tuchida, T. (2009). Improving Effects of the Mushroom Yamabushitake (Hericium erinaceus) on Mild Cognitive Impairment: A Double-blind Placebo-controlled Clinical Trial. Phytotherapy Research, 23, 367–372.
• Pérez-Montes, A., Rangel-Vargas, E., Lorenzo, J.M., Romero, L. & Santos, E.M. (2021). Edible mushrooms as a novel trend in the develop¬ment of healthier meat products. Current Opinion In Food Science, 37, 118–124.
• Rai, M., Tidke, G. & Wasser, S.P.(2005). Therapeutic potential of mushrooms. Natural Product Radiance, 4(4), 246–257.
• Ramos, M., Burgos, N., Barnard, A., Evans, G., Preece, J., Graz, M., Ruthes, A.C., Jiménez-Quero, A., Martínez-Abad, A., Vilaplana, F., Ngoc, L.P., Brouwer, A., van der Burg, B., Garrigós, M.D.C. & Jiménez, A. (2019). Agaricus bisporus and its by-products as a source of valu¬able extracts and bioactive compounds. Food Chemistry, 292, 176–187.
• Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yan, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9), 1231-1237.
• Rodrigues, D.M.F., Freitas, A.C., Rocha-Santos, T.A.P. Vasconcelos, M.W., Roiz, M., Rodriguez-Alcala, L.M., Gomes, A.M.P., Duarte, A.C. (2015). Chemical composition and nutritive value of Pleurotus citrinopileatus var cornucopiae, P. eryngii, P. salmoneo stramineus, Pholiota nameko and Hericium erinaceus . Journal of Food Science and Technology, 52, 6927–6939.
• Rosa, G.B., Sganzerla, W.G., Ferreira, A.L.A., Xavier, L.O., Veloso, N.C., da Silva, J., Oliveira, G.P., Amaral, N.C., Veeck, A.P.L. & Ferrareze, J.P. (2020). Investigation of nutritional composition, antioxidant compounds, and antimicrobial activity of wild culinary-medicinal mush¬rooms Boletus edulis and Lactarius deliciosus (Agaricomycetes) from Brazil. International Journal of Medicinal Mushrooms, 22(10), 931–942.
• Shamim, M.Z., Mishra, A.K., Kausar, T., Mahanta, S., Sarma, B., Kumar, V., Mishra, P.K., Panda, J., Baek, K.-H. & Mohanta, Y.K. (2023). Exploring Edible Mushrooms for Diabetes: Unveiling Their Role in Prevention and Treatment. Molecules 28, 2837. https://doi.org/10.3390/molecules28062837
• Szydłowska-Tutaj, M., Szymanowska, U., Tutaj, K., Domagała, D. & Złotek, U. (2023). The Addition of Reishi and Lion’s Mane Mushroom Powder to Pasta Influences the Content of Bioactive Compounds and the Antioxidant, Potential Anti-Inflammatory, and Anticancer Properties of Pasta. Antioxidants 12, 738.
• Tachabenjarong, N., Rungsardthong, V., Ruktanonchi, U., Poodchakarn, S., Thumthanaruk, B., Vatanyoopaisarn, S., Suttisintong, K., Iempridee, T. & Uttapap, D. (2022). Bioactive compounds and antioxidant activity of Lion’s Mane mushroom (Hericium erinaceus) from different growth periods. Research, Invention, and Innovation Congress- E3S Web Conf. 355, 02016. https://doi.org/10.1051/e3sconf/202235502016
• Yu, Y., Liu, Z., Song, K., Li, L. & Chen, M. (2023). Medicinal value of edible mushroom polysaccharides: a review, Journal of Future Foods, 3(1), 16-23, https://doi.org/10.1016/j.jfutfo.2022.09.003