Abstract
Mushrooms are rich sources of organic nutrients (especially proteins). However, they can excessively accumulate metals in their fruiting bodies that pose a risk to human health. The aim of this study was the determination of Cd, Co, Cu, Fe, Mn, Ni, Pb, and Zn contents, daily intake, and health risk index values of some mushroom species collected from the eastern Black Sea region of Turkey (Arsin, Trabzon). The samples were collected from hazelnut gardens that are free from industrial pollution and have a low population density. As a result of elemental analysis, it was determined that the concentration ranges of Cd, Co, Cu, Fe, Mn, Ni, Pb, and Zn in the mushrooms were as follows: 0.29–9.11, 0.04–3.70, 0.01–8.29, 0.18–20.82, 3.1–79.8, 5.2–673.0, 14.9–752.0, 63.0–7769.0 mg/kg dry weight. Daily intakes of all the elements were found to be below the reference dose in Fistulina hepatica, Hydnum repandum, Macrolepiota procera, and Tapinella atrotomentosa. Amanita caesarea, Agrocybe praecox, Amanita vaginata, Cantharellus cibarius, Craterellus cornucopioides, Daedalea quercina, Gymnopus dryophilus, Ganoderma lucidum, and Infundibulicybe gibba were found to have high risk index values especially with respect to Cd, Co, and Pb. According to Pearson correlation analysis, the correlations between Fe–Mn (0.840, p < 0.01) and Pb–Ni (0.7540, p < 0.01) couples are significant.
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References
Abbaspour N, Hurrell R, Kelishadi R (2014) Review on iron and its importance for human health. J Res Med Sci 19:164–174
Ajmone-Marsan F, Biasioli M (2010) Trace elements in soils of urban areas. Water Air Soil Pollut 213:121–143
Alonso J, García MA, Pérez-López M, Melgar MJ (2003) The concentrations and bioconcentration factors of copper and zinc in edible mushrooms. Arch Environ Contam Toxicol 44:0180–0188
Aloupi M, Koutrotsios G, Koulousaris M, Kalogeropoulos N (2012) Trace metal contents in wild edible mushrooms growing on serpentine and volcanic soils on the island of Lesvos, Greece. Ecotoxicol Environ Saf 78:184–194
Argyraki A, Kelepertzis E (2014) Urban soil geochemistry in Athens, Greece: the importance of local geology in controlling the distribution of potentially harmful trace elements. Sci Total Environ 482:366–377
Árvay J, Tomáš J, Hauptvogl M, Kopernická M, Kováčik A, Bajčan D, Massányi P (2014) Contamination of wild-grown edible mushrooms by heavy metals in a former mercury-mining area. J Environ Sci Health, Part B 49:815–827
Árvay J, Tomáš J, Hauptvogl M, Massányi P, Harangozo, Tóth T, Stanovič R, Bryndzová, Bumbalová M (2015) Human exposure to heavy metals and possible public health risks via consumption of wild edible mushrooms from Slovak Paradise National Park, Slovakia. J Environ Sci Health Part B 50:833–843
Árvay J et al (2019) Determination of elements in wild edible mushrooms: levels and risk assessment. J Microbiol Biotechnol Food Sci 8:999–1004
Barros L, Cruz T, Baptista P, Estevinho LM, Ferreira ICFR (2008) Wild and commercial mushrooms as source of nutrients and nutraceuticals. Food Chem Toxicol 46:2742–2747
Barthel S, Isendahl C (2013) Urban gardens, agriculture, and water management: sources of resilience for long-term food security in cities. Ecol Econ 86:224–234
Bernard A (2008) Cadmium & its adverse effects on human health. Indian J Med Res 128:557–564
Borovička J, Braeuer S, Sácký J, Kameník J, Goessler W, Trubač J, Strnad L, Rohovec J, Leonhardt T, Kotrba P (2019) Speciation analysis of elements accumulated in Cystoderma carcharias from clean and smelter-polluted sites. Sci Total Environ 648:1570–1581
Brzezicha-Cirocka J, Mędyk M, Falandysz J, Szefer P (2016) Bio-and toxic elements in edible wild mushrooms from two regions of potentially different environmental conditions in eastern Poland. Environ Sci Pollut Res 23:21517–21522
Brzezicha-Cirocka J, Grembecka M, Grochowska I, Falandysz J, Szefer P (2019) Elemental composition of selected species of mushrooms based on a chemometric evaluation. Ecotoxicol Environ Saf 173:353–365
Brzostowski A, Falandysz J, Jarzyńska G, Zhang D (2011) Bioconcentration potential of metallic elements by poison pax (Paxillus involutus) mushroom. J Environ Sci Health A 46:378–393
Campos JA, Tejera NA (2011) Bioconcentration factors and trace elements bioaccumulation in sporocarps of fungi collected from quartzite acidic soils. Biol Trace Elem Res 143:540–554
Campos JA, Tejera NA, Sánchez CJ (2009) Substrate role in the accumulation of heavy metals in sporocarps of wild fungi. Biometals 22:835–841
Çayan F, Tel G, Duru ME, Öztürk M, Türkoğlu A, Harmandar M (2014) Application of GC, GC-MSD, ICP-MS and spectrophotometric methods for the determination of chemical composition and in vitro bioactivities of Chroogomphus rutilus: the edible mushroom species. Food Anal Method 7:449–458
Chellan P, Sadler PJ (2015) The elements of life and medicines. Philos Trans R Soc A Math Phys Eng Sci 373:20140182
Chen X-H, Zhou H-B, Qiu G-Z (2009) Analysis of several heavy metals in wild edible mushrooms from regions of China. Bull Environ Contam Toxicol 83:280–285
Chiocchetti GM, Latorre T, Clemente MJ, Jadán-Piedra C, Devesa V, Vélez D (2020) Toxic trace elements in dried mushrooms: effects of cooking and gastrointestinal digestion on food safety. Food Chem 306:125478
Cocchi L, Vescovi L, Petrini LE, Petrini O (2006) Heavy metals in edible mushrooms in Italy. Food Chem 98:277–284
Colak A, Faiz O, Sesli E (2009) Nutritional composition of some wild edible mushrooms. Turk J Biochem 34:25–31
Coroian A, Odagiu A, Marchiș Z, Mireșan V, Răducu C, Oroian C, Longodor AL (2018) Heavy metals and the radioactivity in boletus (Boletus edulis), and chanterelle mushrooms (Cantharellus cibarius) in Transylvanian area. AgroLife Scientific Journal 7:17–21
Cotzias GC (1958) Manganese in health and disease. Physiol Rev 38:503–532
Cui Y-J, Zhu Y-G, Zhai R-H, Chen D-Y, Huang Y-Z, Qiu Y, Liang J-Z (2004) Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China. Environ Int 30:785–791. https://doi.org/10.1016/j.envint.2004.01.003
Čurdová E, Vavrušková L, Suchánek M, Baldrian P, Gabriel J (2004) ICP-MS determination of heavy metals in submerged cultures of wood-rotting fungi. Talanta 62:483–487
Demirbaş A (2000) Accumulation of heavy metals in some edible mushrooms from Turkey. Food Chem 68:415–419
Demirbaş A (2001) Concentrations of 21 metals in 18 species of mushrooms growing in the East Black Sea region. Food Chem 75:453–457
Doĝan HH, Şanda MA, Uyanöz R, Öztürk C, Çetin Ü (2006) Contents of metals in some wild mushrooms. Biol Trace Elem Res 110:79–94
Drewnowska M, Hanć A, Barałkiewicz D, Falandysz J (2017) Pickling of chanterelle Cantharellus cibarius mushrooms highly reduce cadmium contamination. Environ Sci Pollut Res 24:21733–21738
Duda-Chodak A, Blaszczyk U (2008) The impact of nickel on human health. J Elem 13:685–693
Elekes CC, Busuioc G, Ionita G (2010) The bioaccumulation of some heavy metals in the fruiting body of wild growing mushrooms. Not. Bot Horti Agrobo 38:147–151
Essien EE, Mkpenie VN, Akpan SM (2015) Phytochemical and mineral elements composition of Bondazewia berkeleyi, Auricularia auricula and Ganoderma lucidum fruiting bodies. Res J Pharm Biol Chem Sci 6:200–204
Falandysz J, Drewnowska M (2015) Macro and trace elements in common Chanterelle (Cantharellus cibarius) mushroom from the European background areas in Poland: composition, accumulation, dietary exposure and data review for species. J Environ Sci Health, Part B 50:374–387
Falandysz J, Drewnowska M, Jarzyńska G, Zhang D, Zhang Y, Wang J (2012) Mineral constituents in common chanterelles and soils collected from a high mountain and lowland sites in Poland. J Mt Sci 9:697–705
Falandysz J, Chudzińska M, Barałkiewicz D, Drewnowska M, Hanć A (2017a) Toxic elements and bio-metals in Cantharellus mushrooms from Poland and China. Environ Sci Pollut Res 24:11472–11482
Falandysz J, Sapkota A, Dryżałowska A, Mędyk M, Feng X (2017b) Analysis of some metallic elements and metalloids composition and relationships in parasol mushroom Macrolepiota procera. Environ Sci Pollut Res 24:15528–15537
Falandysz J, Mędyk M, Treu R (2018) Bio-concentration potential and associations of heavy metals in Amanita muscaria (L.) Lam. from northern regions of Poland. Environ Sci Pollut Res 25:25190–25206
Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49
García MÁ, Alonso J, Melgar MJ (2009) Lead in edible mushrooms: levels and bioaccumulation factors. J Hazard Mater 167:777–783
Georgescu AA, Danet AF, Radulescu C, Stihi C, Dulama ID, Buruleanu CL (2017) Nutritional and food safety aspects related to the consumption of edible mushrooms from Dambovita County in correlation with their levels of some essential and non-essential metals. Rev Chim 68:2402–2406
Giannaccini G, Betti L, Palego L, Mascia G, Schmid L, Lanza M, Mela A, Fabbrini L, Biondi L, Lucacchini A (2012) The trace element content of top-soil and wild edible mushroom samples collected in Tuscany, Italy. Environ Monit Assess 184:7579–7595
Golubkina N, Mironov V (2018) Element composition of mushrooms in contrasting anthropogenic loading. Geochem Int 56:1263–1275
Gong W, Wang Y, Xie C, Zhou Y, Zhu Z, Peng Y (2020) Whole genome sequence of an edible and medicinal mushroom, Hericium erinaceus (Basidiomycota, Fungi). Genomics 112:2393–2399
Gucia M, Jarzyńska G, Kojta AK, Falandysz J (2012a) Temporal variability in 20 chemical elements content of parasol mushroom (Macrolepiota procera) collected from two sites over a few years. J Environ Sci Health Part B 47:81–88
Gucia M, Jarzyńska G, Rafał E, Roszak M, Kojta AK, Osiej I, Falandysz J (2012b) Multivariate analysis of mineral constituents of edible parasol mushroom (Macrolepiota procera) and soils beneath fruiting bodies collected from northern Poland. Environ Sci Pollut Res 19:416–431
Hefnawy AE, El-Khaiat HM (2015) The importance of copper and the effects of its deficiency and toxicity in animal health. Int J Livest Res 5:1–20
Isildak Ö, Turkekul I, Elmastas M, Tuzen M (2004) Analysis of heavy metals in some wild-grown edible mushrooms from the middle black sea region, Turkey. Food Chem 86:547–552
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72
Jamnická G, Bučinová K, Havranová I, Urban A (2007) Current state of mineral nutrition and risk elements in a beech ecosystem situated near the aluminium smelter in Žiar nad Hronom, Central Slovakia. For Ecol Manag 248:26–35
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
Jedidi IK, Ayoub IK, Philippe T, Bouzouita N (2017) Chemical composition and nutritional value of three Tunisian wild edible mushrooms. J Food Meas Charact 11:2069–2075
Kalač P (2013) A review of chemical composition and nutritional value of wild-growing and cultivated mushrooms. J Sci Food Agric 93:209–218
Karaman MA, Matavulj MN (2005) Macroelements and heavy metals in some lignicolous and tericolous fungi. Zbornik Matice srpske za prirodne nauke:255–267
Kaya A, Bag H (2010) Trace element contents of edible macrofungi growing in Adiyaman, Turkey. Asian J Chem 22:1515–1521
Kojta AK, Jarzyńska G, Falandysz J (2012) Mineral composition and heavy metal accumulation capacity of bay bolete (Xerocomus badius) fruiting bodies collected near a former gold and copper mining area. J Geochem Explor 121:76–82
Kojta AK, Gucia M, Krasińska G, Saba M, Nnorom IC, Falandysz J (2016) Mineral constituents of edible field parasol (Macrolepiota procera) mushrooms and the underlying substrate from upland regions of Poland: bioconcentration potential, intake benefits, and toxicological risk. Pol J Environ Stud 25:2445–2460
Kokkoris V, Massas I, Polemis E, Koutrotsios G, Zervakis GI (2019) Accumulation of heavy metals by wild edible mushrooms with respect to soil substrates in the Athens metropolitan area (Greece). Sci Total Environ 685:280–296
Konuk M, Afyon A, Yagiz D (2007) Minor element and heavy metal contents of wild growing and edible mushrooms from western Black Sea region of Turkey. Fresenius Environ Bull 16:1359–1362
Kosanić M, Ranković B, Rančić A, Stanojković T (2016) Evaluation of metal concentration and antioxidant, antimicrobial, and anticancer potentials of two edible mushrooms Lactarius deliciosus and Macrolepiota procera. J Food Drug Anal 24:477–484
Kula I, Solak MH, Uğurlu M, Işıloğlu M, Arslan Y (2011) Determination of mercury, cadmium, lead, zinc, selenium and iron by ICP-OES in mushroom samples from around thermal power plant in Muğla, Turkey. Bull Environ Contam Toxicol 87:276–281
Kułdo E, Jarzyńska G, Gucia M, Falandysz J (2014) Mineral constituents of edible parasol mushroom Macrolepiota procera (Scop. ex Fr.) Sing and soils beneath its fruiting bodies collected from a rural forest area. Chem Pap 68:484–492
Liu Y-T, Sun J, Luo Z-Y, Rao S-Q, Su Y-J, Xu R-R, Yang Y-J (2012) Chemical composition of five wild edible mushrooms collected from Southwest China and their antihyperglycemic and antioxidant activity. Food Chem Toxicol 50:1238–1244
Massas I, Ehaliotis C, Kalivas D, Panagopoulou G (2010) Concentrations and availability indicators of soil heavy metals; the case of children’s playgrounds in the city of Athens (Greece). Water Air Soil Pollut 212:51–63
Matute RG, Serra A, Figlas D, Curvetto N (2011) Copper and zinc bioaccumulation and bioavailability of Ganoderma lucidum. J Med Food 14:1273–1279
Mazurkiewicz N, Podlasińska J (2014) Bioaccumulation of trace elements in wild-growing edible mushrooms from Lubuskie voivodeship, Poland. Chem Ecol 30:110–117
Michelot D, Poirier F, Meléndez-Howell LM (1999) Metal content profiles in mushrooms collected in primary forests of Latin America. Arch Environ Contam Toxicol 36:256–263
Mirończuk-Chodakowska I, Socha K, Zujko ME, Terlikowska KM, Borawska MH, Witkowska AM (2019) Copper, manganese, selenium and zinc in wild-growing edible mushrooms from the eastern territory of “green lungs of Poland”: nutritional and toxicological implications. Int J Environ Res Public Health 16:3614
Mleczek M, Siwulski M, Stuper-Szablewska K, Rissmann I, Sobieralski K, Goliński P (2013a) Accumulation of elements by edible mushroom species: part I. Problem of trace element toxicity in mushrooms. J Environ Sci Health Part B 48:69–81
Mleczek M, Siwulski M, Stuper-Szablewska K, Sobieralski K, Magdziak Z, Goliński P (2013b) Accumulation of elements by edible mushroom species II. A comparison of aluminium, barium and nutritional element contents. J Environ Sci Health Part B 48:308–317
Mleczek M, Rzymski P, Budka A, Siwulski M, Jasińska A, Kalač P, Poniedziałek B, Gąsecka M, Niedzielski P (2018) Elemental characteristics of mushroom species cultivated in China and Poland. J Food Compos Anal 66:168–178
Murati E, Hristovski S, Karadelev M, Melovski L (2019) The impact of thermal power plant Oslomej (Kichevo Valley, Macedonia) on heavy metal contents (Ni, Cu, Zn, Fe, Mn, Pb, Cd) in fruiting bodies of 15 species of wild fungi. Air Qual Atmos Health 12:353–358
Ndimele CC, Ndimele PE, Chukwuka KS (2017) Accumulation of heavy metals by wild mushrooms in Ibadan, Nigeria. J Health Pollut 7:26–30
Ouzouni PK, Veltsistas PG, Paleologos EK, Riganakos KA (2007) Determination of metal content in wild edible mushroom species from regions of Greece. J Food Compos Anal 20:480–486
Ouzouni PK, Petridis D, Koller W-D, Riganakos KA (2009) Nutritional value and metal content of wild edible mushrooms collected from West Macedonia and Epirus, Greece. Food Chem 115:1575–1580
Podlasińska J, Proskura N, Szymańska A (2015) Content of Pb, Hg, Zn, Mn, Cu, and Fe in macrofungi collected from Wkrzanska forest in northwestern Poland. Pol J Environ Stud 24:651–656
Poe MR, LeCompte J, McLain R, Hurley P (2014) Urban foraging and the relational ecologies of belonging. Soc Cult Geogr 15:901–919
Pratush A, Kumar A, Hu Z (2018) Adverse effect of heavy metals (As, Pb, Hg, and Cr) on health and their bioremediation strategies: a review. Int Microbiol 21:97–106
Radulescu C, Stihi C, Busuioc G, Popescu IV, Gheboianu AI, Cimpoca VG (2010) Evaluation of essential elements and heavy metal levels in fruiting bodies of wild mushrooms and their substrate by EDXRF spectrometry and FAA spectrometry. Rom Biotech Lett 15:5444–5456
Rasalanavho M, Moodley R, Jonnalagadda SB (2019) Elemental distribution including toxic elements in edible and inedible wild growing mushrooms from South Africa. Environ Sci Pollut Res 26:7913–7925
Reczyński W, Muszyńska B, Opoka W, Smalec A, Sułkowska-Ziaja K, Malec M (2013) Comparative study of metals accumulation in cultured in vitro mycelium and naturally grown fruiting bodies of Boletus badius and Cantharellus cibarius. Biol Trace Elem Res 153:355–362
Roohani N, Hurrell R, Kelishadi R, Schulin R (2013) Zinc and its importance for human health: an integrative review. Journal of research in medical sciences: J Res Med Sci 18:144–157
Sarikurkcu C, Tepe B, Semiz DK, Solak MH (2010) Evaluation of metal concentration and antioxidant activity of three edible mushrooms from Mugla, Turkey. Food Chem Toxicol 48:1230–1233
Sarikurkcu C, Copur M, Yildiz D, Akata I (2011) Metal concentration of wild edible mushrooms in Soguksu National Park in Turkey. Food Chem 128:731–734. https://doi.org/10.1016/j.foodchem.2011.03.097
Sarikurkcu C, Tepe B, Kocak MS, Uren MC (2015) Metal concentration and antioxidant activity of edible mushrooms from Turkey. Food Chem 175:549–555. https://doi.org/10.1016/j.foodchem.2014.12.019
Sesli E, Dalman O (2006) Concentrations of trace elements in fruiting bodies of wild growing fungi in Rize Province of Turkey. Asian J Chem 18:2179–2184
Sesli E, Tuzen M (2006) Micro-and macroelement contents of edible wild growing mushrooms in Artvin Province of Turkey. Asian J Chem 18:1423–1429
Sesli E, Tuzen M, Soylak M (2008) Evaluation of trace metal contents of some wild edible mushrooms from Black Sea region, Turkey. J Hazard Mater 160:462–467
Severoglu Z, Sumer S, Yalcin B, Leblebici Z, Aksoy A (2013) Trace metal levels in edible wild fungi. Int J Environ Sci Technol 10:295–304
Širić I, Humar M, Kasap A, Kos I, Mioč B, Pohleven F (2016a) Heavy metal bioaccumulation by wild edible saprophytic and ectomycorrhizal mushrooms. Environ Sci Pollut Res 23:18239–18252
Širić I, Kasap A, Kos I, Markota T, Tomić D, Poljak M (2016b) Heavy metal contents and bioaccumulation potential of some wild edible mushrooms. Šumar List 140:29–37
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. J Environ Sci Health Part B 52:156–165
Stefanović V, Trifković J, Mutić J, Tešić Ž (2016) Metal accumulation capacity of parasol mushroom (Macrolepiota procera) from Rasina region (Serbia). Environ Sci Pollut Res 23:13178–13190
Svoboda L, Chrastný V (2008) Levels of eight trace elements in edible mushrooms from a rural area. Food Addit Contam 25:51–58
Tel G, Çavdar H, Deveci E, Öztürk M, Duru ME, Turkoğlu A (2014) Minerals and metals in mushroom species in Anatolia. Food Addit Contam Part B 7:226–231. https://doi.org/10.1080/19393210.2014.897263
Tel-Çayan G, Öztürk M, Duru ME, Yabanli M, Türkoğlu A (2017) Content of minerals and trace elements determined by ICP-MS in eleven mushroom species from Anatolia, Turkey. Chiang Mai J Sci 44:939–945
Tüzen M, Özdemir M, Demirbaş A (1998) Study of heavy metals in some cultivated and uncultivated mushrooms of Turkish origin. Food Chem 63:247–251
USEPA (2002) A review of the reference dose and reference concentration processes
Vukojević V, Đurđić S, Mutić J (2019) Accumulation of U, Th, Pb, V, Rb, and Ag in wild mushrooms Macrolepiota procera (Scop.) Singer from Goč, Serbia. Environ Sci Pollut Res 26:13147–13158
Wang C, Hou Y (2011a) Determination of trace elements in three mushroom samples of basidiomycetes from Shandong, China. Biol Trace Elem Res 142:843–847
Wang L, Hou Y (2011b) Determination of trace elements in anti-influenza virus mushrooms. Biol Trace Elem Res 143:1799–1807
Wei B, Yang L (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J 94:99–107
Yamaç M, Yıldız D, Sarıkürkcü C, Celikkollu M, Solak MH (2007) Heavy metals in some edible mushrooms from the Central Anatolia, Turkey. Food Chem 103:263–267
Yildiz S, Gurgen A, Cevik U (2019) Accumulation of metals in some wild and cultivated mushroom species. Sigma 37:1371–1380
Zavastin DE, Biliută G, Dodi G, Macsim AM, Lisa G, Gherman SP, Breabăn IG, Miron A, Coseri S (2018) Metal content and crude polysaccharide characterization of selected mushrooms growing in Romania. J Food Compos Anal 67:149–158
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Sarikurkcu, C., Akata, I., Guven, G. et al. Metal concentration and health risk assessment of wild mushrooms collected from the Black Sea region of Turkey. Environ Sci Pollut Res 27, 26419–26441 (2020). https://doi.org/10.1007/s11356-020-09025-3
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DOI: https://doi.org/10.1007/s11356-020-09025-3