Wild mushrooms from East Black Sea Region (Turkiye): Element concentrations and their health risk assessment

Abstract

The aim of this study is to determine the mineral contents of wild edible mushrooms. The potassium (K), magnesium (Mg), calcium (Ca), manganese (Mn), iron (Fe), zinc (Zn), copper (Cu), nickel (Ni), cadmium (Cd) and lead (Pb) contents of twenty four edible mushrooms, collected from East Black Sea Region, Türkiye, were analyzed. The studied mushrooms varied widely in their content of both essential and toxic deleterious elements. The minimum and maximum mineral contents of mushrooms were determined as mg/kg dw for K (4573-15645), Mg (173-1421), Ca (24-711), Mn (5.34-90.64), Fe (44.78-236.95), Zn (24.81-119.03), Cu (11.02-174.01), Ni (0.95-2.86), Cd (0.05-22.57) and Pb (0.01-2.07). The potassium content was found to be higher than those of the other minerals in all the mushrooms. In addition to the metal contents, the daily intakes of metal (DIM) and Health Risk Index (HRI) values of edible mushrooms were also calculated. Lead and cadmium were present but at concentrations that are not hazardous to human health except for Russula vinosa. The K, Mg, Zn, and Ni concentrations were determined to be high in Russula integra. Mushrooms have become increasingly attractive as functional foods for their potential beneficial effects on human health. Due to the toxic minerals they carry, mushrooms should be taken into consideration during their consumption as human food. The differences and similarities between mineral contents were established by Principal Component Analysis. Also, mushrooms are important in the ecosystem because they are able to biodegrade the substrate and to collect heavy metal.

Keywords

• edible mushrooms
• minerals
• toxic element

Project Number

yok

Doğu Karadeniz Bölgesi (Türkiye)’den yabani mantarlar: Element konsantrasyonları ve sağlık risk değerlendirmesi

Abstract

Bu çalışmanın amacı, yenilebilir yabani mantarların mineral içeriklerini belirlemektir. Doğu Karadeniz Bölgesi'nden toplanan yirmi dört yenilebilir mantarın mineral içerikleri Potasyum (K), magnezyum (Mg), kalsiyum (Ca), mangan (Mn), demir (Fe), çinko (Zn), bakır (Cu), nikel (Ni), kadmiyum (Cd) ve kurşun (Pb) analiz edilmiştir. İncelenen mantarlar, hem temel hem de toksik elementleri büyük farklılıklar göstererek içermektedirler. Mantarların minimum ve maksimum mineral içerikleri K (4573-15645), Mg (173-1421), Ca (24-711), Mn (5.34-90.64), Fe (44.78-236.95), Zn (24.81-119.03), Cu (11.02-174.01), Ni (0.95-2.86), Cd (0.05-22.57) ve Pb (0.01-2.07) için mg/kg km olarak belirlenmiştir. Tüm mantarlarda potasyum içeriği diğer minerallerden daha yüksek bulunmuştur. Metal içeriklerinin yanı sıra yenilebilir mantarların Günlük Metal Alımları ve Sağlık Risk İndeksi değerleri de hesaplanmıştır. Kurşun ve kadmiyum Russula vinosa dışında insan sağlığına zararlı olmayan konsantrasyonlarda belirlenmiştir. Russula integra da K, Mg, Zn ve Ni konsantrasyonlarının yüksek olduğu belirlenmiştir. Mantarlar, insan sağlığı üzerindeki potansiyel yararlı etkileri nedeniyle fonksiyonel gıdalar olarak giderek daha çekici hale gelmiştir. Mantarlar, taşıdıkları toksik mineraller nedeniyle insan gıdası olarak tüketilmeleri sırasında dikkate alınmalıdır. Mineral içerikleri arasındaki farklılıklar ve benzerlikler Temel Bileşen Analizi ile de belirlenmiştir. Ayrıca mantarlar, ağır metal toplamak için substratı biyolojik olarak parçalayabildikleri için ekosistemde önemlidirler.

Keywords

• Yenen mantarlar
• mineraller
• zehirli element

Supporting Institution

yok

Project Number

yok

References

1. Abernethy DR, DeStefano AJ, Cecil TL, Zaidi K, Williams RL (2010). Metal impurities in food and drugs. Pharmaceutical Research 27(5): 750-755.
2. Agrawal DC, Dhanasekaran M (Eds.). (2019). Medicinal mushrooms: recent progress in research and development.
3. Alaimo M, Dongarrà G, La Rosa A, Tamburo E, Vasquez G, Varrica D (2018). Major and trace elements in Boletus aereus and Clitopilus prunulus growing on volcanic and sedimentary soils of Sicily (Italy). Ecotoxicol Environ Saf 157: 182-190.
4. AOAC (1990). Official Methods of Analysis of AOAC International (17.Edition). USA: AT Verlag Aarau.
5. Ayaz FA, Torun H, Özel A, Col M, Duran C, Sesli E, Colak A (2011) Nutritional value of some wild edible mushrooms from Black Sea Region (Turkey). Turkish J Biochem 36: 213-221.
6. Bernhoft RA (2013). Cadmium toxicity and treatment. The Scientific World Journal.
7. Breitenbach J, Kranzlin F (1984-2000). Fungi of Switzerland (Vol. 1-5).
8. Bresinsky A, Besl H (1990). A Colour Atlas of Poisonous Fungi (pp. 295). Stuttgart: Wolfe Publishing Ltd.

9. Buczacki S (1989). Fungi of Britain and Europe (pp. 320). Glasgow: William Collins Switzerland: Verlag Mykologia Lucerne.
10. Cui YJ, Zhu YG, Zhai RH, Chen DY, Huang YZ, Qiu Y, Liang JZ (2004). Transfer of metals from soil to vegetables in an area near a smelter in Nanning. China Environ Int 30: 785-791.
11. Cvetkovic JS, Mitic VD, Stankov-Jovanovic VP, Dimitrijevic MV, Nikolic-Mandic SD (2015). Elemental composition of wild edible mushrooms from Serbia. Analytical Letters 48(13): 2107-2121.
12. Çayır A, Coşkun M, Coşkun M (2010). The heavy metal content of wild edible mushroom samples collected in Çanakkale Province, Turkey. Biological Trace Element Research 134(2): 212-219.
13. Dahncke MR, Dahncke SM (1989). 700 Pilze in Farbfotos (pp. 686). Stuttgart.
14. De Silva DD, Rapior S, Sudarman E, Stadler M, Xu J, Aisyah Alias S, Hyde KD (2013). Bioactive metabolites from macrofungi: ethnopharmacology, biological activities and chemistry. Fungal Diversity 62(1): 1-40.
15. Demirbaş A (2000). Accumulation of heavy metals in some edible mushrooms from Turkey. Food Chemistry 68(4): 415-419.
16. Duru ME, Çayan GT (2015). Biologically active terpenoids from mushroom origin: a review. Records of Natural Products 9(4): 456.
17. EFSA (2011). Scientific Opinion of the Panel on Contaminants in the Food Chain on a request from the European Commission on cadmium in food. EFSA J 980: 1-139.
18. Falandysz J, Borovička J (2013). Macro and tracemineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol 97: 477-501.
19. Falandysz J, Kunito T, Kubota R, Bielawski L, Frankowska A, Falandysz J, Tanabe S (2008). Multivariate characterization of elements accumulated in King Bolete Boletus edulis mushroom at lowland and highmountain regions. J Environ Sci Heal A 43: 1692-1699.
20. Falandysz J, Sapkota A, Dryżałowska A, Mędyk M, Feng X (2017). Analysis of some metallic elements and metalloids composition and relationships in parasol mushroom Macrolepiota procera. Environmental Science and Pollution Research 24(18): 15528-15537.
21. Fu Z, Liu G, Wang L (2020). Assessment of potential human health risk of trace element in wild edible mushroom species collected from Yunnan Province, China. Environ Sci Pollut Res 27: 29218-29227.
22. Gargano ML, van Griensven LJ, Isikhuemhen OS, Lindequist U, Venturella G, Wasser SP, Zervakis GI (2017). Medicinal mushrooms: Valuable biological resources of high exploitation potential. Plant Biosystems-An International Journal Dealing with all Aspects of Plant Biology 151(3): 548-565.
23. Gast CH, Jansen E, Bierling J, Haanstra L (1988). Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere 17(4): 789-799.
24. Gençcelep H, Uzun Y, Tunçtürk Y, Demirel K (2009). Determination of mineral contents of wild-grown edible mushrooms. Food Chemistry 113(4): 1033-1036.
25. Guggenheim AG, Wright KM, Zwickey HL (2014). Immune modulation from five major mushrooms: application to integrative oncology. Integrative Medicine: A Clinician's Journal 13(1): 32-44.
26. Guillamón E, García-Lafuente A, Lozano M, Rostagno MA, Villares A, Martínez JA (2010). Edible mushrooms: role in the prevention of cardiovascular diseases. Fitoterapia 81(7): 715-723.
27. Gupta GK (2014). Introduction to data mining with case studies. PHI Learning Pvt. Ltd.
28. IARC (2020). Preamble to the IARC Monographs, amended January. https:// monographs.iarc. fr/ wp-content/uploads/ 2019/07/Preamble-2019.pdf [accessed 4 September 2019].
29. Işıldak Ö, Türkekul İ, Elmastaş M, Tüzen M (2004). Analysis of heavy metals in some wild-grown edible mushrooms from the middle black sea region, Turkey. Food Chem 86: 547-552.
30. Işıloğlu M, Yılmaz F, Merdivan M (2001). Concentrations of trace elements in wild edible mushrooms. Food Chemistry 73(2): 169-175.
31. JECFA (1993). Joint FAO/WHO expert Committee on Food Additives. Evaluation of certain food additives and contaminants: 41st report of the Joint FAO/WHO expert Committee on Food Additives. World Health Organization, Technical Reports Series No. 837, Geneva.
32. Kalač P (2001). A review of edible mushroom radioactivity. Food Chemistry 75(1): 29-35.
33. Kalač P (2009). Chemical composition and nutritional value of European species of wild growing mushrooms: A review. Food Chemistry 113(1): 9-16.
34. Kalač P (2010). Trace element contents in European species of wild growing edible mushrooms: a review for the period 2000-2009. Food Chem 122: 2-15.
35. Kalač P, Svoboda L (2000). A review of trace element concentrations in edible mushrooms. Food Chemistry 69(3): 273-281.
36. Kalač P, Svoboda L, Havlíčková B (2004). Contents of cadmium and mercury in edible mushrooms. Journal of Applied Biomedicine 2(1): 15-20.
37. Karaman M, Vesic M, Stahl M, Novakovic M, Janjic L, Matavuly M (2012). Bioactive properties of wild-growing mushroom species Ganorderma applanatum (Pers.) Pat. from Fruska Gora Forest (Serbia). Ethnomed. Ther. Valid 32: 361-377.
38. Kaya A, Bağ H (2010). Trace element contents of edible macrofungi growing in Adıyaman, Turkey. Asian Journal of Chemistry 22(2): 1515-1521.
39. Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrović P, Van Griensven L (2015). Antioxidants of edible mushrooms. Molecules 20(10): 19489-19525.
40. Li N, Chen F, Cui F, Sun W, Zhang J, Qian L, Yang H (2017). Improved postharvest quality and respiratory activity of straw mushroom (Volvariella volvacea) with ultrasound treatment and controlled relative humidity. Scientia Horticulturae 225: 56-64.
41. Li T, Wang Y, Zhang J, Zhao Y, Liu H (2011). Trace element content of Boletus tomentipes mushroom collected from Yunnan, China. Food Chemistry 127(4): 1828-1830.
42. Liu B, Huang Q, Cai H, Guo X, Wang T, Gui M (2015). Study of heavy metal concentrations in wild ediblemushrooms in Yunnan Province. China Food Chem 188: 294-300.
43. Liu H, Zhang J, Li T, Shi Y, Wang Y (2012). Mineral element levels in wild edible mushrooms from Yunnan, China. Biological Trace Element Research 147(1): 341-345.
44. Markowitz M (2000). Lead poisoning. Pediatrics in Review 21(10): 327-335.
45. Mendil D, Uluözlü ÖD, Hasdemir E, Çaǧlar A (2004). Determination of trace elements on some wild edible mushroom samples from Kastamonu, Turkey. Food Chemistry 88(2): 281-285.
46. Mendil D, Uluözlü ÖD, Hasdemir E, Tüzen M, Sarı H, Suiçmez M (2005). Determination of trace metal levels in seven fish species in lakes in Tokat, Turkey. Food Chemistry 90(1-2): 175-179.
47. Miracle DB (2017). High-entropy alloys: A current evaluation of founding ideas and core effects and exploring “nonlinear alloys”. JOM: The Journal of The Minerals, Metals & Materials Society (TMS) 69(11): 2130-2136.
48. Mleczek M, Budka A, Kalač P, Siwulski M, Niedzielski P (2020). Family and species as determinants modulating mineral composition of selected wild-growing mushroom species. Environ Sci Pollut Res In press 28: 389-404.
49. Mleczek M, Niedzielski P, Kalač P, Budka A, Siwulski M, Gąsecka M, Sobieralski K (2016a). Multielemental analysis of 20 mushroom species growing near a heavily trafficked road in Poland. Environmental Science and Pollution Research 23(16): 16280-16295.
50. Mleczek M, Niedzielski P, Kalač P, Siwulski M, Rzymski P, Gąsecka M (2016b). Levels of platinum group elements and rare-earth elements in wild mushroom species growing in Poland. Food Additives & Contaminants: Part A 33(1): 86-94.
51. Muszyńska B, Grzywacz-Kisielewska A, Kała K, Gdula-Argasińska J.(2018). Anti-inflammatory properties of edible mushrooms: A review. Food Chemistry 243: 373-381.
52. National Research Council (US) (1975). Committee on Mineral Resources, the Environment, National Research Council, National Research Council (US). Commission on Natural Resources, Etats-Unis. Committee on mineral resources, the environment, ... & Population Council. Mineral resources and the environment (Vol. 1). National Academy of Sciences.
53. Niemiec M, Sikora J, Chowaniak M, Szelag-Sikora A, Kubon M (2018). Bioaccumulation of Iron, Manganese, Boron, Lithium and Cobalt in Lactarius salmonicolor and Abies alba M. in the Przedbabiogorski Range in the Western Carpathians. Rocz Ochr Srodowiska 20: 1386-1401.
54. Nowakowski P, Markiewicz-Żukowska R, Soroczyńska J, Puścion-Jakubik A, Mielcarek K, Borawska MH, Socha K (2021). Evaluation of toxic element content and health risk assessment of edible wild mushrooms. Journal of Food Composition and Analysis 96: 103698.
55. Nygård T, Steinnes E, Røyset O (2012). Distribution of 32 elements in organic surface soils: contributions from atmospheric transport of pollutants and natural sources. Water, Air, & Soil Pollution 223(2): 699-713.
56. Pelkonen R, Alfthan G, Järvinen O (2006). Cadmium, lead, arsenic and nickel in wild edible mushrooms. Finnish Environ. 17. ISBN 952-11-2275-7.
57. Rakić M, Karaman M, Forkapić S, Hansman J, Kebert M, Bikit K, Mrdja D (2014). Radionuclides in some edible and medicinal macrofungal species from Tara Mountain, Serbia. Environmental Science and Pollution Research 21(19): 11283-11292.
58. Rasalanavho M, Moodley R, Jonnalagadda SB (2020). Elemental bioaccumulation and nutritional value of five species of wild growing mushrooms from South Africa. Food Chemistry 319: 126596.
59. Rashid MH, Rahman MM, Correll R, Naidu R (2018). Arsenic and other elemental concentrations in mushrooms from Bangladesh: health risks. International Journal of Environmental Research and Public Health 15(5): 919.
60. Rzymski P, Mleczek M, Siwulski M, Gąsecka M, Niedzielski P (2016). The risk of high mercury accumulation in edible mushrooms cultivated on contaminated substrates. Journal of Food Composition and Analysis 51: 55-60.
61. Sanmee R, Dell B, Lumyong P, Izumori K, Lumyong S (2003). Nutritive value of popular wild edible mushrooms from northern Thailand. Food Chemistry 82(4): 527-532.
62. Sarıkürkçü C, Tepe B, Solak MH, Çetinkaya S (2012). Metal concentrations of wild edible mushrooms from Turkey. Ecology of Food and Nutrition 51(4): 346-363.
63. Sesli E, Dalman Ö (2006). Concentrations of trace elements in fruiting bodies of wild growing fungi in Rize Province of Turkey. Asian J Chem 18: 2179-2184.
64. Sesli E, Tüzen M (1999). Levels of trace elements in the fruiting bodies of macrofungi growing in the East Black Sea region of Turkey. Food Chemistry 65(4): 453-460.
65. Sesli E, Tüzen M, Soylak M (2008). Evaluation of trace metal contents of some wild edible mushrooms from Black sea region, Turkey. Journal of Hazardous Materials 160(2-3): 462-467.
66. Severoğlu Z, Sümer S, Yalçın B, Leblebici Z, Aksoy A (2013). Trace metal levels in edible wild fungi. Int J Environ Sci Te 10: 295-304.
67. Širić I, Kasap A, Bedeković D, Falandysz J (2017). Lead, cadmium and mercury contents and bioaccumulation potential of wild edible saprophytic and ectomycorrhizal mushrooms, Croatia. Journal of Environmental Science and Health Part B 52(3): 156-165.
68. Širić I, Kasap A, Kos I, Markota T, Tomić D, Poljak M (2016). Heavy metal contents and bioaccumulation potential of some wild edible mushrooms. Šumarski List 140(1-2): 29-37.
69. Soylak M, Saraçoğlu S, Tüzen M, Mendil D (2005). Determination of trace metals in mushroom samples from Kayseri, Turkey. Food Chemistry 92(4): 649-652.
70. Tüzen M, Özdemir M, Demirbaş A (1998). Study of heavy metals in some cultivated and uncultivated mushrooms of Turkish origin. Food Chemistry 63(2): 247-251.
71. USEPA (2002.) A review of the reference dose and reference concentration processes.
72. Wang S-H, Zhang J-D, Xu H, Li D-H (2017). Metal content of Armillaria mellea in the Tumen River Basin. Int J Food Prop 20: 2052-2059.
73. Wang XM, Zhang J, Wu LH, Zhao YL, Li T, Li JQ, Liu HG (2014). A mini-review of chemical composition and nutritional value of edible wild-grown mushroom from China. Food Chemistry 151: 279-285.
74. WHO (1989). World Health Organization. Strengthening the performance of community health workers in primary health care: report of a WHO Study Group [meeting held in Geneva from 2 to 9 December 1987]. World Health Organization.
75. WHO (1996). Agriculture Organization (FAO), International Atomic Energy Association (IAEA). Trace elements in human nutrition and health.
76. WHO (2004). World Health Organization. Guidelines for drinking-water quality (Vol. 1). World Health Organization.
77. Yellen G (2002). The voltage gated potassium channels and their relatives. Nature 419: 35-42.
78. Zhu F, Qu L, Fan W, Qiao M, Hao H, Wang X (2011). Assessment of heavy metals in some wild edible mushrooms collected from Yunnan Province, China. Environmental Monitoring and Assessment 179(1): 191-199.