Multi-elemental analysis of Lentinula edodes mushrooms available in trade

Journal of Environmental Science and Health, Part B Pesticides, Food Contaminants, and Agricultural Wastes ISSN: 0360-1234 (Print) 1532-4109 (Online) Journal homepage: http://www.tandfonline.com/loi/lesb20 Multi-elemental analysis of Lentinula edodes mushrooms available in trade Mirosław Mleczek, Marek Siwulski, Piotr Rzymski, Przemysław Niedzielski, Monika Gąsecka, Agnieszka Jasińska, Sylwia Budzyńska & Anna Budka To cite this article: Mirosław Mleczek, Marek Siwulski, Piotr Rzymski, Przemysław Niedzielski, Monika Gąsecka, Agnieszka Jasińska, Sylwia Budzyńska & Anna Budka (2017) Multi-elemental analysis of Lentinula edodes mushrooms available in trade, Journal of Environmental Science and Health, Part B, 52:3, 196-205, DOI: 10.1080/03601234.2017.1261551 To link to this article: http://dx.doi.org/10.1080/03601234.2017.1261551 Published online: 25 Jan 2017. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=lesb20 Download by: [The UC San Diego Library] Date: 26 January 2017, At: 14:13 JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B 2017, VOL. 52, NO. 3, 196–205 http://dx.doi.org/10.1080/03601234.2017.1261551 Multi-elemental analysis of Lentinula edodes mushrooms available in trade a
skab, Miros»aw Mleczeka, Marek Siwulskib, Piotr Rzymskic, Przemys»aw Niedzielskid, Monika Gasecka ˛ , Agnieszka Jasin a e
ska , and Anna Budka Sylwia Budzyn a
University of Life Sciences, Department of Chemistry, Pozna
n University of Life Sciences, Pozna
n, Poland; bDepartment of Vegetable Crops, Poznan Pozna
n, Poland; cDepartment of Environmental Medicine, University of Medical Sciences, Poznan, Poland; dFaculty of Chemistry, Adam Mickiewicz University in Pozna
n, Pozna
n, Poland; eDepartment of Mathematical and Statistical Methods, Poznan University of Life Sciences, Pozna
n, Poland ABSTRACT KEYWORDS The present study investigated the content of 62 elements in the fruiting bodies of Lentinula edodes (Shiitake mushroom) cultivated commercially in Poland on various substrates from 2007–2015. The general mean content (mg kg¡1 dry weight (DW)) of the studied elements ranked in the following order: K (26,335) > P (11,015) > Mg (2,284) > Ca (607) > Na (131) > Zn (112) > Fe (69) > Mn (33) > B (32) > Rb (17) > Cu (14.5) > Al (11.2) > Te (2.9) > As (1.80) > Cd (1.76) > Ag (1.73) > Nd (1.70) > Sr (1.46) > Se (1.41) > U (1.11) > Pt (0.90) > Ce (0.80) > Ba (0.61) > Co (0.59) > Tl (0.58) > Er (0.50) > Pb (0.42) > Li (0.40) > Pr (0.39) > Ir (0.37) > In (0.35) > Mo (0.31) > Cr (0.29) > Ni (0.28) > Sb (0.26) > Re (0.24) > Ti (0.19) > Bi (0.18) > Th (0.12) > La (0.10) D Pd (0.10) > Os (0.09) D Zr (0.09) > Rh (0.08) > Ho (0.07) > Ru (0.06) > Sm (0.04) D Eu (0.04) D Tm (0.04) > Gd (0.03) > Sc (0.02) D Y (0.02) > Lu (0.01) D Yb (0.01) D V (0.01). The contents of Au, Be, Dy, Ga, Ge, Hf, and Tb were below the limits of detection (0.02, 0.02, 0.01, 0.01, 0.01, 0.01, 0.02 mg kg¡1 respectively). The concentrations of Al, As, B, Ba, Ca, Cd, Cr, Er, Fe, In, Lu, Mn, Nd, Sr, Ti, Tm, and Zr were comparable over the period the mushrooms were cultivated. The study revealed that Lentinula edodes contained As and Cd at levels potentially adverse to human health. This highlights the need to monitor these elements in food products obtained from this mushroom species and ensure that only low levels of these elements are present in cultivation substrates. Lentinula edodes; multielemental analyses; food safety Introduction Mushrooms have long been known for their ability to accumulate high levels of various elements in both unpolluted and mildly and highly polluted areas.[1] Numerous reasons influencing this quality have been evidenced.[2,3] In general, the concentration of trace elements in mushrooms varies across taxa and is highly associated with substrate composition and bioavailability of the elements for mushroom mycelium.[4] The relationship between the abundance and bioavailability of trace elements from soil or cultivation substrates is, however, very complex and results from natural factors such as bedrock geochemistry, pH/Eh conditions, organic matter content, chelates, metalliferous areas, and environmental pollution. Accumulation in mushrooms can also be very element- and species-specific.[5–10] Over the years, various studies have determined the presence and distribution of numerous trace elements in mushroom fruiting bodies. The most common and highly concentrated elements (BAF > 1) in some macrofungi include gold (Au), silver (Ag), arsenic (As), bromine (Br), cadmium (Cd), chlorine (Cl), cesium (Cs), copper (Cu), mercury (Hg), rubidium (Rb), selenium (Se), vanadium (V), and zinc (Zn). Those which are concentrated at lower levels (BAF < 1) are cobalt (Co), chromium (Cr), fluorine (F), iodine (I), nickel (Ni), antimony (Sb), tin (Sn), thorium (Th), uranium (U), and rare earth elements (REEs).[11–14] CONTACT Miros»aw Mleczek © 2017 Taylor & Francis Group, LLC mirekmm@up.poznan.pl The levels of various elements (including toxic metals) in cultivated mushrooms are usually lower than in wild ones due to differences between chemical composition of soil and substrate composition and age of the mycelium which may grow for several years in natural conditions but for only a few months during the cultivation process.[15] World consumption of mushrooms has generally increased over the past 15 years from approximately 1 kg in 1997 to 4 kg per person in 2012.[16] Lentinula edodes (Berk.) Pegler (Shiitake mushroom) is one of the most cultivated edible mushrooms globally (after Agaricus and Pleurotus mushrooms), particularly in East Asian countries where almost 90% of the world production of Lentinula edodes is done.[16,17] In the United States its production had exceeded 9 million pounds per year in 2009.[18] Lentinula edodes is well known for its unique flavor, nutritional value, and medicinal properties. It contains high levels of several bioactive compounds, i.e. dietary fiber,[19] ergosterol, vitamins B1, B2, and C, folates, niacin, minerals, antitumor polysaccharides, nucleic acids of antiviral activity, antithrombotic agents, and compounds decreasing low-density lipoprotein (LDL) cholesterol levels.[20–26] Recent investigations have shown that Lentinula edodes can be enriched in particular trace elements, such as selenium, and serve as potential nutraceuticals.[27–30] The increasing popularity and consumption of Lentinula edodes underlines the need to evaluate the quality of food products available commercially. Department of Chemistry, Pozna
n University of Life Sciences, Pozna
n, Poland. JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B The aim of the present study was to make an assessment of the concentration of 62 elements in fruiting bodies of Lentinula edodes cultivated in Poland for commercial use from 2007–2015. This is the broadest multi-elemental analyses conducted so far on Lentinula edodes, while its findings add to the general discussion on the occurrence of various elements, including those which are rarely studied, in the environment and in food products. The obtained results were discussed in view of provisional or established limits of element content in food to indicate whether consumption of commercially available Lentinula edodes in Poland poses any threat to human health. Materials and methods Experimental material Carpophores of Lentinula edodes, derived from the cultivations conducted throughout the year on 12 mushroom farms in Poland, were collected directly before being made available in the market. The tested carpophores were obtained from each mushroom producer in 3–4 cultivation cycles each year from 2007–2015. Numbers of samples (n) obtained each year were different (2007 – n D 48; 2008 – n D 48; 2009 – n D 48; 2010 – n D 48; 2011 – n D 39; 2012 – n D 42; 2013 – n D 37; 2014 – n D 47; and 2015 – n D 48). None of the samples were spoiled or decayed, and all collected samples (fruit bodies) were analyzed. The weight of a single carpophore sample amounted to 1 kg each. Cultivation substrates of different compositions were applied by producers of Lentinula edodes depending on the cultivation method. The main components of substrates were oak, beech, alder, poplar, and birch sawdust. The addition of chopped wheat straw was used by some mushroom growers. The substrates were supplemented with wheat bran, soybean meal, corn meal, rye or millet grains, and sucrose. Chalk and gypsum were also applied as additives. The proportions of substrate components used by individual growers were highly differentiated in relation to their availability in the market and the cultivation method. Sample preparation The fruiting bodies were transported to the laboratory and carefully cleaned with distilled water (Milli-Q Advantage A10Water, Merck, Darmstadt, Germany) to remove any contamination adsorbed on their surface. Mushroom samples were then dried using an electric drying oven (SLW 53 STD, PolEko, Wodzis»aw
Slaski, ˛ Poland) for 70 h at 65 § 1 C and homogenized in a Cutting Mill SM 200 (Retsch GmbH, Haan, Germany) for 1 min to a powdered fraction. Three analytical replicates prepared from each of the five samples collected from each producer were weighed (0.400 § 0.001 g) and digested using 7 mL of 65% HNO3 (Merck, Darmstadt, Germany) in a closed Teflon tube (55 mL) in a microwave mineralization system Mars 5 (CEM, Matthews, NC, USA): ramp time to temperature 180 C: 20 min, hold time 20 min, cooling 20 min, and power 800 W. The obtained solutions were filtered using 45-mm filters (Qualitative Filter Papers Whatman, Grade 595: 4–7 mm), and diluted to a final volume of 15.0 mL. 197 Analytical method The following groups of elements were analyzed in samples prepared from the fruiting bodies of Lentinula edodes: (1) alkali metals – lithium (Li), sodium (Na), potassium (K), and Rb, (2) alkaline earth metals – beryllium (Be), magnesium (Mg), calcium (Ca), strontium (Sr), and barium (Ba), (3) REEs – cerium (Ce), europium (Eu), gadolinium (Gd), lanthanum (La), neodymium (Nd), praseodymium (Pr), and samarium (Sm) as light rare earth elements (LREEs), and also dysprosium (Dy), erbium (Er), holmium (Ho), lutetium (Lu), scandium (Sc), terbium (Tb), thulium (Tm), yttrium (Y), and ytterbium (Yb) as heavy rare earth elements (HREEs), (4) noble elements—Ag, Au, iridium (Ir), osmium (Os), palladium (Pd), platinum (Pt), rhenium (Re), rhodium (Rh), and ruthenium (Ru), (5) transition metals – Co, Cu, iron (Fe), manganese (Mn), molybdenum (Mo), Ni, V, and Zn, and (6) semimetals and selenium – As, Sb, boron (B), germanium (Ge), Se, and tellurium (Te). In the last group the following elements were included: aluminum (Al), bismuth (Bi), Cd, Cr, hafnium (Hf), indium (In), phosphorus (P), lead (Pb), Th, titanium (Ti), thallium (Tl), U, and zirconium (Zr). Inductively coupled plasma optical emission spectrometry with Agilent 5100 ICP-OES (Agilent, Santa Clara, CA, USA) was used for the determination of 62 elements. Dichroic spectral combiner (DSC) technology was applied, which allowed an axial and radial view analysis simultaneously in a synchronous vertical dual view (SVDV). The following common instrumental conditions were adopted[31]: plasma gas—argon, radio frequency (RF) power 1.2 kW, nebulizer gas flow 0.7 L min¡1, auxiliary gas flow 1.0 L min¡1, plasma gas flow 12.0 L min¡1; charge coupled device (CCD)—temperature –40 C, viewing height for radial plasma observation 8 mm, accusation time 5 s, five replicates. The microwave digestion system Mars 5 (CEM) was used for sample preparation. The traceability has been checked using four certified reference materials (CRMs; biological and geological): CRM S-1—loess soil; CRM CSM1— mushrooms; CRM NCSDC (73349)—bush branches and leaves; and CRM 2709—soil. The CRM CS-M1 analysis has been performed in duplicate to find the precision for real (matrix) sample. The results of the certified reference materials analysis are collated in Table 1. Statistical analysis To characterize concentration of particular elements in mushrooms collected during the studied period (2007–2015), a descriptive statistics were used (median, range, variance, and coefficient of variation). In addition, skewness (measure of the lack of symmetry) and kurtosis (similarity of the shape of the data distribution to the Gaussian distribution) were estimated. The criterions of skewness estimation were: 0—a symmetrical distribution; higher values—an asymmetrical distribution (right side); and lower values—an asymmetrical distribution (left side), while in case of kurtosis: 0—-a Gaussian distribution; higher values—more peaked than a Gaussian distribution; and lower values—a flatter distribution. 198 Determined values (mg kg¡1) Element Al As B Ba Ca Cd Ce Co Cr Cu Dy Eu Fe Gd K La Li Lu Mg Mn Mo Na Nd Ni Pb Sb Sc Se Sr Te Tl Y Yb Zn Certified values (mg kg¡1) Recovery (%) A B B C D A B B C D A B B C D 7,011 2.8 8.4 360 1,959 0.32 32 3.4 40 5.5 2.2 0.37 7,898 2.5 11,210 22 6.1 0.27 1,113 181 <0.01 3,623 1.3 11 12 0.43 3.4 <0.01 50 0.66 0.21 5.6 2.64 34 72 0.36 2.0 1.9 321 0.24 0.34 0.56 0.79 7.7 <0.01 <0.01 105 <0.01 15,545 0.12 0.12 <0.01 646 14 <0.01 545 0.24 0.30 0.48 <0.01 <0.01 1.5 1.1 <0.01 <0.01 <0.01 <0.01 71 68 0.40 2.0 1.9 311 0.26 0.36 0.57 0.78 7.1 <0.01 <0.01 108 <0.01 15,538 0.17 0.15 <0.01 654 12 <0.01 534 0.23 0.30 0.46 <0.01 <0.01 1.4 1.0 <0.01 <0.01 <0.01 <0.01 69 721 0.99 32 16 15,194 0.41 1.9 0.44 2.2 5.5 <0.01 <0.01 945 0.19 8,456 0.96 3.1 <0.01 4,231 59 0.29 7,678 0.95 1.6 42 0.08 0.2 0.3 262 0.43 <0.01 0.55 <0.01 54 19,879 12 65 388 17,200 0.40 33 12.3 127 29 3.1 0.63 29,459 2.7 3,694 11 41 0.25 4,111 435 <0.01 5,591 20 71 15 1.2 11 1.7 110 0.61 0.63 2.1 2.2 89 x 3.4 x 304 2,600 0.3 44 3.9 38 6.3 x 0.6 9,880 x 12,500 21 x 0.3 1,550 266 x 4,440 x 13 15 0.5 4 x 55 x x x 2.5 35 x 0.344 x x x 0.273 x x x x x x x x x x x x x x x x x x 0.476 x x 1.37 x x x x x 60.94 x 0.344 x x x 0.273 x x x x x x x x x x x x x x x x x x 0.476 x x 1.37 x x x x x 60.94 2,000 1.25 38 18 16,800 0.38 2.2 0.41 2.6 6.6 0.13 0.039 1,070 0.19 9,200 1.25 2.6 0.011 4,800 61 0.28 19,600 1 1.7 47 0.095 x x 246 x x 0.68 0.063 55 73,700 10.5 74 x 19,100 0.371 42 12.8 130 x 3 0.83 33,600 3 2,1100 21.7 x 0.3 14,600 529 x 12,200 17 85 17.3 1.55 11.1 1.5 x 0.5 0.58 2 x 103 x 82.4 x 118.4 75.3 106.7 72.7 87.2 105.3 87.3 x 61.7 79.9 x 89.7 104.8 x 90.0 71.8 68.0 x 81.6 x 84.6 80.0 86.0 85.0 x 90.9 x x x 105.6 97.1 x 104.7 x x x 87.9 x x x x x x x x x x x x x x x x x x 100.8 x x 109.5 x x x x x x x 116.3 x x x 95.2 x x x x x x x x x x x x x x x x x x 96.6 x x 102.2 x x x x x 113.2 36.1 79.2 84.2 88.9 90.4 107.9 86.4 107.3 84.6 83.3 x x 88.3 100.0 91.9 76.8 119.2 x 88.1 96.7 103.6 39.2 95.0 94.1 89.4 84.2 x x 106.5 x x 80.9 x 98.2 27.0 114.3 87.8 x 90.1 107.8 78.6 96.1 97.7 x 103.3 75.9 87.7 90.0 17.5 50.7 x 83.3 28.2 82.2 x 45.8 117.6 83.5 86.7 77.4 99.1 113.3 x 122.0 108.6 105.0 x 86.4 x: not certified value; A: CRM S-1; B: CRM CS-M-1; C: CRM NCSDC; D: CRM 2709. M. MLECZEK ET AL. Table 1. Traceability studies for certified reference materials. JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B Results and discussion Content of elements in fruiting bodies From the 62 elements analyzed in this study, the content of Au, Be, Dy, Ga, Ge, Hf, and Tb, was below the limit of detection: 0.02, 0.02, 0.01, 0.01, 0.01, 0.01, and 0.02 mg kg¡1, respectively, in all the studied samples. The presence of other elements in the fruiting bodies of Lentinula edodes was detected at varying levels. For the purpose of elaboration, the studied elements were divided into the following groups: alkali metals, alkaline earth metals, REEs (with subdivision of LREEs and HREEs), transition metals, noble metals, semimetals, and other elements. In addition to the median values presented in Table 2, the significant range values (mg kg¡1 DW) were observed for the following: Al (39.2), B (79), Ca (7,132), Cu (21), K (34,986), Mg (7,408), Mn (141), Na (211), Nd (19.2), P (16,990), Rb (89), Sr (18), and Zn (215). Differences between the highest and the lowest values of these elements in the studied mushrooms were further confirmed by the increased values of variance: Al (83), B (334), Ca (1,850,102), Cu (34), K (117,402,891), Mg (2,371,465), Mn (988), Na (3,625), Nd (13.9), P (23,897,006), Rb (665), Sr (12.3), and Zn (3,036). Values of coefficient of variance indicated a diverse elementary content in mushrooms obtained in different years. A low variability was observed for As, Cu, Fe, K, Lu, Na, P, Re, Sc, Th, Tm, and Zn. The variability for Al, Cd, Mn, Mo, Pb, Pt, Se, Te, 199 Ti, and U was moderate, while for the rest of the studied elements it was high. The latter particularly concerned Ba, Ca, Nd, Sr, and Zr. Analysis of skewness allowed to show that content of As and Te in majority of the mushroom samples was lower than the mean values of these elements. Kurtosis values lower than 0 point at a great amount of outmost values were observed for As, Cu, Ir, K, Na, P, Pt, Re, Sc, Se, Te, Th, Tm, U, and Zn, while for other elements the kurtosis values were higher than 0. The highest values of kurtosis was found for Ba (23.9), Ca (23.4), Nd (21.0), and Sr (22.9), which, especially in the case of Ca, Nd, and Sr, explains a little amount of outmost values of their content in the studied mushrooms. Alkali metals and alkaline earth metals The content of alkali metals (Li, Na, K, and Rb) and alkaline earth metals (Mg, Ca, Sr, and Ba) was diverse; therefore the obtained results were presented using a logarithmic scale (Fig. 1). The mean content of Li, Na, K, and Rb was: 0.4 § 0.2, 131 § 59, 26,335 § 10,633, and 17 § 25 mg kg¡1 DW, respectively, while that of Mg, Ca, Sr, and Ba was: 2,284 § 1,511, 607 § 355, 1.4 § 3.4, and 0.6 § 1.1 mg kg¡1 DW respectively. The obtained results pointed to a wide range for the majority of these elements present in mushrooms which was probably related to the variety of substrates used for mushroom cultivation. Rare earth elements Table 2. Characteristics of statistical parameters estimated for studied elements content in all Lentinula edodes fruit bodies obtained during 2009–2015 period. Median Range Element (mg kg¡1) (mg kg¡1) Al As B Ba Ca Cd Cr Cu Er Fe In Ir K Lu Mg Mn Mo Na Nd P Pb Pt Rb Re Sc Se Sr Te Th Ti Tm U Zn Zr 8.55 1.88 32.78 0.23 274 1.35 0.15 13.43 0.48 67.58 0.29 0.38 26,263 0.01 2,033 25.39 0.30 123 0.68 10,405 0.42 0.83 6.15 0.23 0.02 0.98 0.45 3.68 0.15 0.14 0.04 0.99 107 0.03 39.23 3.45 78.98 6.88 7,132 6.15 1.46 21.45 1.59 118.58 0.83 0.86 34,986 0.02 7,408 141 1.01 211 19.20 16,990 1.07 2.18 89 0.41 0.03 3.75 18.23 6.29 0.21 0.56 0.06 2.71 215 0.62 Variance 82.67 0.74 334 1.69 1,850,101 2.77 0.12 34.19 0.12 839 0.05 0.05 117,402,890 0.00 2,371,465 988 0.05 3,625 13.85 23,897,006 0.07 0.36 665 0.01 0.00 1.63 12.33 4.31 0.00 0.02 0.00 0.77 3036 0.02 Coefficient of variation (%) Skewness Kurtosis 80.9 48.4 56.5 225 224 94.8 117.3 40.2 64.1 44.0 61.8 60.3 41.1 49.0 67.4 96.7 75.8 45.9 222.1 44.4 61.1 66.8 149.2 48.3 40.3 86.1 256.1 71.5 48.0 66.8 43.2 78.9 49.4 173.7 1.64 ¡0.06 0.77 4.77 4.73 1.44 2.45 0.61 1.64 0.48 1.04 0.56 0.17 1.73 1.95 2.54 1.51 0.30 4.45 0.48 0.83 0.76 2.01 0.00 0.12 0.62 4.68 ¡0.12 0.22 1.69 0.32 0.28 0.18 2.88 3.16 ¡0.61 0.91 23.86 23.37 1.19 6.25 ¡0.20 3.56 0.23 0.36 ¡0.22 ¡1.15 3.42 5.75 7.15 3.17 ¡0.86 21.01 ¡0.78 0.66 ¡0.15 2.82 ¡0.45 ¡1.06 ¡1.12 22.88 ¡1.55 ¡0.87 3.81 ¡0.15 ¡1.28 ¡0.41 8.02 Among the 17 analyzed REEs (LREEs and HREEs), 13 of these were detected in each of the studied fruiting bodies. In the case of LREEs, the mean content of Ce, La, Nd, Pr, and Sm was: 0.8 § 1.0, 0.10 § 0.05, 1.7 § 3.7, 0.4 § 0.3, and 0.04 § 0.01 mg kg¡1 DW respectively (Fig. 2). Concentrations of Eu and Gd above detection limits were presented only in selected fruiting bodies. The mean content of these elements was: 0.04 § 0.02 and 0.025 § 0.004 mg kg¡1 DW respectively. The mean content of particular HREEs (Fig. 2) in the tested Lentinula edodes fruit bodies was similar: 0.5 § 0.3 (Er), 0.07 § 0.01 (Ho), 0.01 § 0.01 (Lu), 0.02 § 0.01 (Sc), 0.04 § 0.02 (Tm), 0.02 § 0.02 (Y), and 0.01 § 0.01 (Yb) mg kg¡1 DW. The mean and the highest contents of total LREEs (3.2 and 22.6 mg kg¡1 DW respectively) were higher than the mean and the highest contents of total HREEs (0.8 and 2.0 mg kg¡1 DW respectively). Transition metals As shown in Fig. 3, the content of transition metals was significantly diverse. The highest mean content for Zn, Fe, Mn, and Cu was observed as follows: 112 § 54, 69 § 28, 33 § 31, and 14.5 § 5.7 mg kg¡1 DW respectively. For the rest of the transition metals the mean content of these elements was lower and the following values were obtained: 0.60 § 0.29 (Co), 0.31 § 0.23 (Mo), 0.28 § 0.33 (Ni), and 0.01 § 0.01 (V) mg kg¡1 DW. Noble metals The highest mean content in this element group was observed for Ag (1.73 § 1.35 mg kg¡1 DW) (Fig. 4). For the rest of the 200 M. MLECZEK ET AL. Figure 1. Minimal, maximal, and mean content (logarithmic scale) of alkali and alkaline earth metals (mg kg¡1 DW) in bodies. metals the mean content was lower: 0.90 § 0.59 (Pt), 0.37 § 0.22 (Ir), 0.24 § 0.11 (Re), 0.10 § 0.03 (Pd), 0.09 § 0.05 (Os), 0.08 § 0.04 (Rh), and 0.06 § 0.02 (Ru) mg kg¡1 DW. Semimetals and selenium The highest mean content was observed for B (32.4 § 18.0 mg kg¡1 DW; Fig. 5). In the case of Te and Se, the mean content was lower (2.90 § 2.04 and 1.48 § 1.25 mg kg¡1 DW), while it was the lowest for Sb (0.26 § 0.19 mg kg¡1 DW). The mean content of As was 1.77 § 0.84 mg kg¡1 DW, while the highest mean content of this metalloid was 3.60 mg kg¡1 DW in mushrooms collected in 2014. Other elements The content of elements included in the last group was characterized by the highest diversity (Fig. 6). The highest mean content was observed for P and Al (11,015 § 4,797 and 11.2 § 8.9 mg kg¡1 DW respectively). The mean content of toxic Cd, Cr, Pb, and Tl was: 1.76 § 1.63, 0.29 § 0.34, 0.42 § 0.25, and 0.58 § 0.44 mg kg¡1 DW. In the case of In, Ti, and Zr, nonessential for humans, their mean content was: 0.35 § 0.21, 0.19 § 0.12, and 0.09 § 0.15 mg kg¡1 DW respectively. A low mean content of Bi, used for medicinal purposes, was stated (0.19 § 0.11 mg kg¡1 DW), while the mean content of toxic actinides (Th and U) was 0.12 § 0.06 and 1.11 § 0.86 mg kg¡1 DW. Toxicological and nutritional aspects The present study is one of the first to analyze such a broad spectrum of elements in mushrooms and the first to report their content in commercially cultivated species. Our previous investigations demonstrated concentrations of platinum group elements and rare-earth elements in wild above-ground and wood-growing mushroom species collected in Poland.[32] Here, the content of other elements, including those belonging to transition, noble, alkali and alkaline earth metals, and semimetals is additionally reported. The mean content (mg kg¡1 DW) of detected elements generally decreased in the following order: K (26,335) > P (11,015) > Mg (2,284) > Ca (607) > Na (131) > Zn (112) > Fe (69) > Mn (33) > B (32) > Rb (17) > Cu (14.5) > Al (11.2) > Te(2.9) > As (1.80) > Cd (1.76) > Ag Figure 2. Minimal, maximal, and mean content (logarithmic scale) of light and heavy rare earth elements (mg kg¡1 DW) in bodies. JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B 201 Figure 3. Minimal, maximal, and mean content (logarithmic scale) of noble elements (mg kg¡1 DW) in bodies. (1.73) > Nd (1.70) > Sr (1.46) > Se (1.41) > U (1.11) > Pt (0.90) > Ce (0.80) > Ba (0.61) > Co (0.59) > Tl (0.58) > Er (0.50) > Pb (0.42) > Li (0.40) > Pr (0.39) > Ir (0.37) > In (0.35) > Mo (0.31) > Cr (0.29) > Ni (0.28) > Sb (0.26) > Re (0.24) > Ti (0.19) > Bi (0.18) >Th (0.12) > La (0.10) D Pd (0.10) > Os (0.09) D Zr (0.09) > Rh (0.08) > Ho (0.07) > Ru (0.06) > Sm (0.04) D Eu (0.04) D Tm (0.04) > Gd (0.03) > Sc (0.02) D Y (0.02) > Lu (0.01) D Yb (0.01) D V (0.01). It should also be noted that content of most of these elements was determined in every studied sample with the exception of Eu and Gd, which were detected only in selected fruiting bodies. The content of seven other elements (Au, Be, Dy, Ga, Ge, Hf, and Tb) was, in turn, below the limit of detection in every studied sample. It is widely known that the content of various elements in mushroom fruiting bodies is closely related to their levels in overgrown substrate in both wild-growing species [33–35] and cultivated mushrooms due to highly effective (although species-dependent) uptake of elements via spacious mycelium.[36–38] The generally high variation of elements observed in the present study in the fruiting bodies of Lentinula edodes, reflected by standard deviation (SD) values, was therefore most likely associated with differences in the chemical composition of the cultivation substrate. In the case of Lentinula edodes, a wide spectrum of cultivation of substrates can be applied, including sorghum stalk, banana, coffee pulp, sawdust, cotton seed hulls bran, sugar cane leaves, corncobs, bracts of pineapple, cotton seed meal, peanut meal, wheat bran, rice bran, and soybean meal as well as wastes from paddy, sugar cane bagasse, sugar cane, or wheat.[39–42] These substrates, due to distinctively different origin, may largely vary in chemical composition, including concentrations of particular elements.[43] The production of safe fungi for human food requires the use of high quality substrates to avoid contamination with elements at levels which pose a risk to human health.[44] This is particularly important in the case of Lentinula edodes as previous studies have experimentally shown that the mycelium growth of this species may be tolerant to substrate contamination with some nonessential and toxic metals, such as Pb, or biologically essential elements, which can reveal toxicities at certain concentrations or forms, including Cu or Zn.[45] A market survey conducted recently in China demonstrated that commercially available Lentinula edodes can contain relatively high concentrations of Cd, As, Pb, Fe, and Zn compared with other investigated species such as Auriculariaauricula-judae (Bull.) Qu
el., Pleurotus ostreatus (Jacq.) P. Kumm., Tremella fuciformis Figure 4. Minimal, maximal, and mean content (logarithmic scale) of transition metals (mg kg¡1 DW) in bodies. 202 M. MLECZEK ET AL. Figure 5. Minimal, maximal, and mean content (logarithmic scale) of semimetals and selenium (mg kg¡1 DW) in bodies. Berk., Flammulina velutipes (Curtis) Singer, Agrocybe chaxingu, Armillaria mellea (Vahl) P. Kumm., Agaricus bisporus (J.E. o) S. Ito and S. Lange) Imbach, and Pholiota nameko (T. It^ Imai.[46] Compared with the results of this survey, the fruiting bodies of Lentinula edodes from Polish cultivation contained a higher mean concentration of As (0.636 vs 1.77 mg kg¡1), comparable mean levels of Cd (1.67 vs 1.76 mg kg¡1) and Zn (111 vs 112 mg kg¡1), and lower mean content of Pb (2.85 vs 0.42 mg kg¡1) and Fe (194 vs 69 mg kg¡1).[46] However, although specific point pollution sources, smoking, or occupational activities are associated with increased human exposure to certain elements,[47] dietary intake is recognized as a significant contributor in this regard.[48,49] Lentinula edodes is not only one of the most consumed mushrooms in East Asia but it has also gained worldwide popularity due to its nutritional value and postulated medicinal effects.[50] Its production in Europe for food purposes is, however, rare as its cultivation procedures are extremely laborious and timeconsuming.[51] Regardless of the origin of production, the concentrations of toxic or potentially toxic elements in fruiting bodies of Lentinula edodes should be as low as possible to avoid adverse human exposures. Numerous elements included in our analyses are well known to induce toxicity in humans. Evaluations conducted by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) have established a provisional tolerable weekly intake (PTWI) of some toxic elements, including Al (PTWI – 2 mg kg¡1 body weight (bw)), As (PTWI withdrawn in 2011 – 0.015 mg kg¡1 bw), Cd (PTWI – 0.0058 mg kg¡1bw), and Pb (PTWI withdrawn in 2011 – 0.025 mg kg¡1 bw).[52] Considering that average weekly edible mushroom intake was assumed to be 210 g week¡1,[15,53] the consumption of fruiting bodies of Lentinula edodes cultivated in Poland by an adult of 60-kg body weight would generally constitute as low as 2.0% of PTWI for Al and 5.9% of PTWI for Pb, and as much as 41.3% of PTWI for As and 106% of PTWI for Cd. The findings of the present study clearly highlight that consumption of the investigated mushrooms would contribute significantly to dietary As and Cd intake. This is most likely to be a consequence of the contamination of substrates. Importantly, no significant differences in the content of these elements were noted in mushrooms obtained during different years (2007– 2015), indicating that As and Cd contamination of the studied mushrooms is a permanent condition and requires further action. As demonstrated in previous studies, Lentinula edodes can be characterized by relatively high bioaccumulation of Cd compared with other cultivated mushrooms,[54] and this element is generally sequestered preferentially over Pb or As by this mushroom species.[55] This is also supported by the observation that commercially available Chinese specimens of this Figure 6. Minimal, maximal, and mean content (logarithmic scale) of other elements (mg kg¡1 DW) in bodies. JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B mushroom contain Cd levels significantly contributing to PTWI.[46] Another study has demonstrated that Lentinula edodes available in the Spanish market not only contains high As levels but that the majority of total As is constituted from inorganic forms, which are known to reveal the greatest toxicities.[56] Altogether, these findings highlight the need to monitor As and Cd levels in Lentinula edodes cultivated for food production as well as in the substrates used in their cultivation. Elements such as K, P, Mg, Ca, Na, Zn, Fe, Mn, Cu, Se, Co, Cr, and Ni are known to be biologically essential for specific metabolic functions. The studied specimens of Lentinula edodes were demonstrated to be a particularly rich nutritional source of K, P, Mg, Ca, and Na, which is consistent with the observations made on different species, including wild-growing mushrooms.[33,57] As found in other studies, mineral composition of Lentinula edodes ranges from 3.7 to 7.0% of fruiting body dry mass, and apart from a high macroelement content, it also contains relatively high levels of trace elements such as Cu, Fe, or Zn,[13,28,54,58] which is consistent with the results of the present study. Altogether these findings further add to already proven high nutritional value of Lentinula edodes, particularly exhibited by increased carbohydrate content in comparison with other popularly cultivated species.[59] The food content of numerous elements determined in the present study remains unregulated due to a lack of sufficient toxicological and/or monitoring data. Most of these elements were present at low levels in the studied specimens of Lentinula edodes with mean content for the studied period not exceeding 0.4 mg kg¡1 (Li, Pr, Ir, In, Mo, Sb, Re, Ti, Bi, and Th) or even 0.1 mg kg¡1 (La, Pd, Os, Zr, Rh, Ho, Ru, Sm, Eu, Tm, Gd, Sc, Y, Lu, Yb, and V). Particularly high levels were, however, found for Rb with the mean content of this element amounting to 17 mg kg¡1. On the other hand, wild-growing species were shown to contain higher concentrations by at least one order of magnitude. For example, Cantharellus cibarius Fr., was demonstrated to contain from 102 to 1,500 mg kg¡1 of Rb,[32,60,61] while caps of Xerocomus subtomentosus L. contained 320 mg kg¡1 of Rb.[62] Nevertheless, it is important to highlight that toxicity (and biological role) of Rb remains controversial and requires further studies.[63] However, compared with other mushrooms, cultivated Lentinula edodes does not appear to be a significant source of this element. Recently, more attention has been paid to the occurrence of REEs in the human environment and food.[64] This group of elements remains unregulated in many world regions and the content of REEs in the environment requires further research, while the knowledge of their effects on health is still limited. The REE content in fruiting bodies of the studied Lentinula edodes amounted to 3.775 mg kg¡1, with LREEs generally making a greater contribution to the total REEs quota than HREEs. The greater share of LREEs was previously demonstrated in wild-growing mushroom species.[32] The total REE concentrations observed in Lentinula edodes investigated in the present study were decidedly lower than those demonstrated for other food products, including vegetables.[65] On the other hand, the studied fruiting bodies exceeded a maximum tolerable level of REEs in China, which was provisionally set at 0.7 mg kg¡1.[66] For the first time, Lentinula edodes from cultivated production 203 has been indicated as a potential dietary source of REEs for humans. It is, however, unknown whether it may significantly contribute to total dietary REEs quota. There still remains a need to screen the content of REEs in other food goods and to establish the toxicological risks (if any) that may arise from their dietary intake. Conclusions In conclusion, the present study is so far the most comprehensive investigation of element concentration in Lentinula edodes from commercial production. 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